Endophytes: Mineral Nutrient Management [3, 1 ed.] 303065446X, 9783030654467

Citation preview

Sustainable Development and Biodiversity 26

Dinesh Kumar Maheshwari Shrivardhan Dheeman   Editors

Endophytes: Mineral Nutrient Management, Volume 3 123

Sustainable Development and Biodiversity Volume 26

Series Editor Kishan Gopal Ramawat, Botany Department, Mohanlal Sukhadia University, Udaipur, India

This book series provides complete, comprehensive and broad subject based reviews about existing biodiversity of different habitats and conservation strategies in the framework of different technologies, ecosystem diversity, and genetic diversity. The ways by which these resources are used with sustainable management and replenishment are also dealt with. The topics of interest include but are not restricted only to sustainable development of various ecosystems and conservation of hotspots, traditional methods and role of local people, threatened and endangered species, global climate change and effect on biodiversity, invasive species, impact of various activities on biodiversity, biodiversity conservation in sustaining livelihoods and reducing poverty, and technologies available and required. The books in this series will be useful to botanists, environmentalists, marine biologists, policy makers, conservationists, and NGOs working for environment protection.

More information about this series at http://www.springer.com/series/11920

Dinesh Kumar Maheshwari · Shrivardhan Dheeman Editors

Endophytes: Mineral Nutrient Management, Volume 3

Editors Dinesh Kumar Maheshwari Department of Botany and Microbiology Gurukula Kangri Vishwavidyalaya Haridwar, Uttarakhand, India

Shrivardhan Dheeman Department of Microbiology Sardar Bhagwan Singh University Dehradun, India

ISSN 2352-474X ISSN 2352-4758 (electronic) Sustainable Development and Biodiversity ISBN 978-3-030-65446-7 ISBN 978-3-030-65447-4 (eBook) https://doi.org/10.1007/978-3-030-65447-4 © Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

The present book entitled Endophytes: Mineral Nutrient Management, Volume 3 is in continuation of two previous volumes published on endophytes, their biology, biodiversity, crop productivity, and their role in crop protection. Based on the idea that endophytic microbes are far stronger than the other bacteria in the rhizospheric microbial world, scientists are paying great attention to the understanding of the beneficial nature of endophytes in particular as they bear enormous potentialities for boosting the sustainable growth of crops and agroecosystems. This book is a comprehensive collection of reviews on current science and evidence of biofertilizer ability of endophytes for nutrient management. Some chapter on the endophytic lifestyle in the plant tissues is an attraction of the book. There is an elaborated account of their special traits like competence, root colonization, and/or endophytic phytohormone secretion which act for plant protection and stress sequestration. Entirely, the synergism of practical and theoretical wisdom on endophytes makes this book alive. An elaborated content has also been available in the book on the science of enhancement of nutrient utilization efficiency. Endophytes increase the availability of important nutrients to enrich soil fertility and fulfill the nutritional demand of plants. Further, plant-endophyte interaction evidences a mutual alleviation of biotic and abiotic stresses in diverse habitat and agroclimatic conditions. Genomic tools and techniques can further identify endophytes with the ability of mineral nutrient management which can be utilized in the production of microbial inoculants for future farming. The book presented under the series “Sustainable development and biodiversity” is entirely dedicated to various endophytic genera, able to mineralize micro and macronutrients in the soil and rhizosphere. This book will not only benefit the scientific diaspora but also to the teachers, researchers, graduation and postgraduation students in various streams of life sciences such as Agriculture, Horticulture, Biotechnology, Microbiology, Phytopathology, Agronomy, and Environmental Sciences. We desire to pay our thanks to all the subject specialists and contributors, who lent their cooperation and patience in the completion of this book. Our research team members, who generously assisted in the compilation and completion of this task also deserve a big thanks. We v

vi

Preface

extend our sincere thanks to Dr. Ineke and her colleagues for their valuable support in the completion of this project. Support from MHRD UGC—BSR is also duly acknowledged. Haridwar, Uttarakhand, India August 2020

Dinesh Kumar Maheshwari Shrivardhan Dheeman

Contents

Part I

Endophytes in Agriculture

1

Endophytes in Mineral Nutrient Management: Introduction . . . . . . Dinesh Kumar Maheshwari and Shrivardhan Dheeman

3

2

Bioefficacy of Endophytes in the Control of Plant Diseases . . . . . . . . Fernando Matias Romero, Amira Susana Nieva, Oscar Adolfo Ruiz, Andrés Gárriz, and Franco Rubén Rossi

11

3

Microbial Endophytes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils . . . . . . . . . . . . . . . . . . . . . Anupma Dahiya, Rakesh Kumar, and Satyavir S. Sindhu

4

5

Cattle Dung Manure Microbiota as a Substitute for Mineral Nutrients and Growth Management Practices in Plants . . . . . . . . . . . Sandhya Dhiman, Sandeep Kumar, Nitin Baliyan, Shrivardhan Dheeman, and Dinesh Kumar Maheshwari

35

77

Fluorescent Pseudomonads in Iron Chelation and Plant Growth Promotion in Abiotic Stresses . . . . . . . . . . . . . . . . . . . . . . . . . . . 105 C. Dileep, C. G. Sreekala, T. S. Reshma, and Surabhi Sankar

Part II

Endophytes and Mineral Nutrition

6

Microbial Endophytes: New Direction to Natural Sources . . . . . . . . . 123 Azim Ghasemnezhad, Arezou Frouzy, Mansour Ghorbanpour, and Omid Sohrabi

7

Tropical Endophytic Bacillus Species Enhance Plant Growth and Nutrient Uptake in Cereals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157 Camila Cristina Vieira Velloso, Vitória Palhares Ribeiro, Chainheny Gomes de Carvalho, Christiane Abreu de Oliveira, Ubiraci Gomes de Paula Lana, Ivanildo Evódio Marriel, Sylvia Morais de Sousa, and Eliane Aparecida Gomes

vii

viii

Contents

8

Biotechnology and Bioinformatics of Endophytes in Biocontrol, Bioremediation, and Plant Growth Promotion . . . . . . 181 Houda Ben Slama, Hafsa Cherif-Silini, Ali Chenari Bouket, Allaoua Silini, Faizah N. Alenezi, Lenka Luptakova, Armelle Vallat, and Lassaad Belbahri

9

Phosphate Solubilization by Endophytes from the Tropical Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207 Paulo Teixeira Lacava, Paula Cristiane Machado, and Paulo Henrique Marques de Andrade

Part III Beneficial Microbes and Mineral Nutrient Management 10 Endophytic Actinobacteria Associated with Mycorrhizal Spores and Their Benefits to Plant Growth . . . . . . . . . . . . . . . . . . . . . . 229 Krisana Lasudee, Pharada Rangseekaew, and Wasu Pathom-aree 11 Endophytes as Plant Nutrient Uptake-Promoter in Plants . . . . . . . . . 247 Carlos García-Latorre, Sara Rodrigo, and Oscar Santamaría 12 Endophytic Rhizobacteria for Mineral Nutrients Acquisition in Plants: Possible Functions and Ecological Advantages . . . . . . . . . . 267 Becky Nancy Aloo, Vishal Tripathi, Ernest R. Mbega, and Billy A. Makumba 13 Plant Growth-Promoting Bacteria: Effective Tools for Increasing Nutrient Use Efficiency and Yield of Crops . . . . . . . . . 293 Chitra Pandey, Shrivardhan Dheeman, Deepti Prabha, Yogesh Kumar Negi, and Dinesh Kumar Maheshwari 14 Siderophore in Plant Nutritional Management: Role of Endophytic Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315 Gunjan Garg, Sandeep Kumar, and S. Bhati 15 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 Dinesh Kumar Maheshwari Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335

Contributors

Faizah N. Alenezi Environmental Technology and Management Department, College of Life Sciences, Kuwait University, Kuwait City, Kuwait Becky Nancy Aloo Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania; Department of Biological Sciences, University of Eldoret, Eldoret, Kenya Paulo Henrique Marques de Andrade Laboratory of Microbiology and Biomolecules – LaMiB, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil; Evolutionary Genetics and Molecular Biology Graduation Program – PPGGEv, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil Nitin Baliyan Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Lassaad Belbahri NextBiotech, Agareb, Tunisia; Laboratory of Soil Biology, University of Neuchatel, Neuchatel, Switzerland S. Bhati School of Biotechnology, Gautam Buddha University, Greater Noida, Uttar Pradesh, India Ali Chenari Bouket Plant Protection Research Department, East Azarbaijan Agricultural and Natural Resources Research and Education Center, AREEO, Tabriz, Iran Chainheny Gomes de Carvalho Centro (UNIFEMM), Sete Lagoas, MG, Brazil

Universitário

de

Sete

Lagoas

Hafsa Cherif-Silini Laboratory of Applied Microbiology, Department of Microbiology, Faculty of Natural and Life Sciences, University Ferhat Abbas Setif-1, Setif, Algeria ix

x

Contributors

Anupma Dahiya Department of Microbiology, CCS Haryana Agricultural University, Hisar, India Shrivardhan Dheeman Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Balawala, Dehardun, India; Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Sandhya Dhiman Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India C. Dileep Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Arezou Frouzy Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran Carlos García-Latorre School of Agricultural Engineering. Institute of Dehesa Research, University of Extremadura, Badajoz, Spain Gunjan Garg School of Biotechnology, Gautam Buddha University, Greater Noida, Uttar Pradesh, India Andrés Gárriz Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Azim Ghasemnezhad Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran Mansour Ghorbanpour Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran Eliane Aparecida Gomes Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Rakesh Kumar Department of Microbiology, CCS Haryana Agricultural University, Hisar, India Sandeep Kumar Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Paulo Teixeira Lacava Laboratory of Microbiology and Biomolecules – LaMiB, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil; Biotechnology Graduation Program – PPGBiotec, Center of Exact Sciences and Technology, Federal University of São Carlos, São Carlos, SP, Brazil; Evolutionary Genetics and Molecular Biology Graduation Program – PPGGEv, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil Krisana Lasudee Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand

Contributors

xi

Lenka Luptakova Department of Biology and Genetics, Institute of Biology, Zoology and Radiobiology, University of Veterinary Medicine and Pharmacy, Kosice, Slovakia Paula Cristiane Machado Biotechnology Graduation Program – PPGBiotec, Center of Exact Sciences and Technology, Federal University of São Carlos, São Carlos, SP, Brazil Dinesh Kumar Maheshwari Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Billy A. Makumba Department of Biological Sciences, Moi University, Eldoret, Kenya Ivanildo Evódio Marriel Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil; Centro Universitário de Sete Lagoas (UNIFEMM), Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Ernest R. Mbega Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania Yogesh Kumar Negi Department of Basic Sciences, College of Forestry (VCSG UUHF), Ranichauri, Tehri Garhwal, Uttarakhand, India Amira Susana Nieva Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Christiane Abreu de Oliveira Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Chitra Pandey Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India Wasu Pathom-aree Research Center of Microbial Diversity and Sustainable Utilization, Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand Ubiraci Gomes de Paula Lana Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Deepti Prabha Department of Seed Science and Technology, Chauras Campus, HNB Garhwal University, Srinagar, Uttarakhand, India Pharada Rangseekaew Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand

xii

Contributors

T. S. Reshma Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Vitória Palhares Ribeiro Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil Sara Rodrigo School of Agricultural Engineering. Institute of Dehesa Research, University of Extremadura, Badajoz, Spain Fernando Matias Romero Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Franco Rubén Rossi Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Oscar Adolfo Ruiz Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Surabhi Sankar Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Oscar Santamaría Department of Construction and Agronomy, University of Salamanca, Zamora, Spain Allaoua Silini Laboratory of Applied Microbiology, Department of Microbiology, Faculty of Natural and Life Sciences, University Ferhat Abbas Setif-1, Setif, Algeria Satyavir S. Sindhu Department of Microbiology, CCS Haryana Agricultural University, Hisar, India Houda Ben Slama NextBiotech, Agareb, Tunisia Omid Sohrabi Department of Horticultural Sciences, Guilan University, Rasht, Iran Sylvia Morais de Sousa Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil; Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil C. G. Sreekala Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Vishal Tripathi Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, UP, India

Contributors

xiii

Armelle Vallat Neuchatel Platform of Analytical Chemistry, Institute of Chemistry, University of Neuchatel, Neuchatel, Switzerland Camila Cristina Vieira Velloso Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil

Part I

Endophytes in Agriculture

Chapter 1

Endophytes in Mineral Nutrient Management: Introduction Dinesh Kumar Maheshwari and Shrivardhan Dheeman

Abstract The second green revolution can beat the challenge of food requirement, which will be a game-changer of this decade. It will boost the fertility of the soil, food security, and global crop production. The microbial world of endophytes having the ability of nutrient mineralization has been proved a boon to mitigate hunger of the global population. In this scenario, crop yields must be increased substantially to glorify the coming decades and mitigate global food demand using endophytesbased biofertilizers. Over the past few years, researchers are engaged to re-discover endophytes to help us to produce healthier crops with higher yields while reducing the need for fertilizer and other chemicals. This is a summary account of reviews of the subject experts from the entire globe bringing their idea(s), commentaries, and views on the current research on endophytes and the mechanistic role of endophytes to sustain agriculture production in major and micro mineral nutrient management precisely. Keywords Endophytes · Mineral nutrients · Soil · Rhizosphere

1.1 Introduction Research of plant growth-promoting bacteria (PGPR) and endophytes is entering in the third decade of the twenty-first century. Scientific chronicles are converting old policies of agriculture into golden policies for sustainable agriculture, to achieve a new revolution and combat against food security. Like plant growth-promoting bacteria, endophytes are also known for providing several direct and indirect benefits to their host friend. Hence, newer studies become important to understand and D. K. Maheshwari · S. Dheeman Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India S. Dheeman (B) Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Dehradun, Uttarakhand 248 161, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_1

3

4

D. K. Maheshwari and S. Dheeman

harness the beneficial influence of the past and future of mineral nutrient management and sustainable agriculture by endophytes. Nutrient management is an approach of sustaining mineral nutrients in plants and soil systems. Originally, this approach is a derivation of integrated nutrient management (INM) holding focus on nitrogen (N), phosphorus (P), and potassium (K) nutrients by blending agrochemicals with effective microorganisms (EM). In the insights of mineral nutrient management (MiNuM), endophytes have been used to increase the spectrum of soil fertility and mineralization or immobilization of various trace elements like N, P, K, Zn, Fe, Cu, Mg, and S. The soil microorganisms can improve plant responses against biotic and abiotic stresses and aid them in health management are called ‘beneficial bacteria’. Altogether the plant-microbe-soil creates a tripartite relationship in soil ecology, which is often studied under plant-microbe interaction. Plant-microbe interaction (PMI) is a complex relationship that exists above-ground and below-ground. The belowground PMI is more complex than the above, because of consisting complex interface with soil. The soil affects these relationships via its physico-chemical properties in addition to abiotic and biotic factors. Few PGPR develops an intimate relationship with plants and becomes colonized inside tissues without any visible symptoms that are usually termed as endophytes. Endophytes are also found in the seeds of few plants, thus, these are termed as ‘seed endophytes’. Basically, in the below-ground PMI, they are known for their versatility and helping plant via several mechanisms such as nitrogen fixation, phosphate solubilization, potassium (K) and zinc (Zn) solubilization, siderophores production, phytohormone production, volatile production of hydrogen cyanic (HCN) acid, 1aminocyclopropane, 1-carboxylic acid (ACC) deaminase production, biocontrol of fungal phytopathogens, induced systemic resistance (ISR) and systemic acquired resistance (SAR). Endophytes are important to consider in the usage of nutrient mineralization due to their significant traits (Maheshwari and Dheeman 2019). The heterogeneous community of endophytes includes root-nodulating Rhizobia to facultative endophytes such as Bacillus, Pseudomonas, Azotobacter, etc. The abundant existence of Bacillus in soil may be attributed due to spore formation, resistance to high temperature, and cold shock resistance (Pandey et al. 2018). Endophytes can solubilize phosphorus (P) and potassium (K) along with the ability to mineralize Zinc (Zn) and oxidize sulfur (S). On the other hand, few endophytes involve in Nfixation (mineralization of N to fix in the form of Ammonia). This way, endophytes have emerged as a versatile candidate. They endure in harsh environments with their feasible strategies and deals with the limitation of agricultural production caused by soil factors. The exact mechanism by which endophytes improve plant health remains largely speculative; however, possible explanation includes mineral nutrient management (include acquisition of nutrients as direct involvement in plant growth promotion largely reviewed in this book by eminent scholars). Endophyte to serve as biofertilizer or Phyto-stimulator helps in maintaining the soil. These include the acquisition of nutrients as a direct involvement in plant growth promotion; however, other mechanisms support indirectly toward plant growth and sustainable agriculture.

1 Endophytes in Mineral Nutrient …

5

The beneficial microorganisms have been established for efficient mineral solubilization, mobilization, and acquisition of soil nutrients. Being major tissue colonizer of plant’s interior and to improve plant growth by enhancing nutrient use efficiency (NUE) with phosphorus (P) from the organic stock to available form via nutrient mineralization. Biological control against few soil-borne diseases and improved water uptake in drought conditions via the maintenance of ACC-deaminase activity and ethylene regulation influence growth promotion (Aeron et al. 2019). A revised scheme of the utilization of endophyte as bioformulation is depicted in Fig. 1.1. The use of fertilizers, including mineral fertilizers and organic manures, to enhance soil fertility and crop productivity (Etesami and Maheshwari 2018) has often influenced the complex system of the biogeochemical cycles. The synthetic fertilizer and chemicals caused leaching and nutrients run-off, especially N and P, leading to environmental degradation. Low fertilizer use efficiency and continuous long-term use are important causes of this aggravated problem. Thus, it necessitates the involvement of endophytes to acquire suitable strategies for the plant’s mineral nutrient management.

Fig. 1.1 A revised scheme of isolation and characterization of endophytes for plant growth promotion, molecular identification, and use as bioinoculant for raising agricultural crops

6

D. K. Maheshwari and S. Dheeman

1.2 Frontiers of Endophyte The frontiers of endophyte research have been determined with unique mixes of varied contributions of the chapters and unification of the most influential researches, and historical advances. It finds more about how endophyte owns their frontiers and go beyond.

1.2.1 Avenues in Pharmaceuticals Metabolism is a universal phenomenon of all living creatures and science evidenced the beneficial and harmful gears of metabolites. Most in cases secondary metabolites are considered toxic, and due to antibiosis mechanisms, some sort of bacterial metabolites is considered beneficial for therapeutic purposes. Chapter 6 encased with direct shreds of evidence to understand the usage of secondary metabolites from endophytic fungi. It is focused on biological activity correlated to chemical diversity and exclusive use in agriculture, medicine, and industry.

1.2.2 Fungal Endophytes In the micro-niche of mycorrhizal spore, actinobacterial endophyte creates a scope of future research. As a plant growth promoter, they bear vast applications in agriculture. Actinobacteria lives in association with arbuscular mycorrhizal (AM) spores under abiotic and biotic stresses and, therefore, can alleviate climatic adversity in grain crops like rice; fairly reviewed in Chapter 10. A few endophytic fungi living asymptomatically within the plants can confer improvement in plant nutrient uptake, as a need of a sustainable farming and soilrecharge with biogeochemical cycle. Fungi boost nutrient uptake via several mechanisms understood in Chapter 3. This countered on how fungi hold multiple benefits to plants under stressed conditions and mineral nutrient uptake.

1.2.3 Spore Bearing Endophyte Enhancing Plant Nutrient Uptake Abiotic factors are determinantal for plant growth but, a few endophytes like sporeforming bacilli are resistant to the climatic adversity and contributing to the agricultural productivity. These microorganisms can enhance crop growth with great potential while having an endophytic life. Especially in tropical ecosystems, they colonize the internal tissues of plants and bear an ecological advantage explored

1 Endophytes in Mineral Nutrient …

7

by their genomics. Thus, opportunities to commercialize these beneficial bacteria, create a deep-down sense to investigating more about their roles and mechanisms has been covered in Chapter 7.

1.2.4 Endophyte for Crop Protection Plant-microbe interactions have many faces of benefit and deleterious effects. In this trend, endophytes diminish disease development by several mechanisms but, precisely by involving antagonistic and parasitic interaction with pathogens. ISR and SAR contributed by endophytes using a sum of different strategies. Hence, endophytes are now utilizing as a source of biological control. Endophyte in biological control and an image that they’re intertwined in the network for mineral nutrient uptake/management.

1.2.5 Phosphorus Management by Endophytes Phosphorus (P) is the second most essential mineral nutrient after nitrogen for plant growth and development. Phosphate solubilizers have been characterized as an important candidate for soil microbes. Like PGPR, endophytic microorganisms associated with different plants release organic acids and solubilize phosphate complexes into ortho-phosphate for easy uptake by plants. Genetic manipulation in the strains of phosphate solubilizing (PS) bacteria can increase the capacity and efficacy of PS biofertilizer for sustainable agriculture, significantly covered in Chapter 3. Along with several mechanisms of PGPR, phosphate solubilization facilitates the conversion of insoluble P and intertwines in the biogeochemical cycle. Chapter 9 reviews the urgency of industrial agriculture to move for modern agricultural biotechnology and exploiting microbial inoculants, which can enhance plant growth and thereby reduce the use of agrochemicals. In this way, giant information on endophyte involved in P solubilization becomes crucial to be collected. This chapter focused on endophytic phosphate solubilization and its role in mineral management.

1.2.6 Endophytes: Ecological Advances The realization that the plant microbiome can improve the management of plant health, soil fertility, and crop productivity is one of the most fascinating scientific discoveries in the world. Endophytic bacteria are unique plant microbiome that establishes them within their tissues. Chapter 12 is enhancing wisdom on putative functions of endophyte for plant mineral nutrients acquisition and is advantageous to provide better opportunities and viable strategies for sustainable agriculture.

8

D. K. Maheshwari and S. Dheeman

1.2.7 PGPB: Nutrient Use Efficiency Plant growth-promoting bacteria (PGPB) has a potential tool for sustainable agriculture utilizing for a long time in plant growth and development. Also, these PGPB increase plant nutrient uptake capacity and nutrient use efficiency. Chapter 13 illustrates several studies focusing on PGPRs in nutrient use efficiency of various crops and covered their long-term application to reduce the use, cope with the negative effects of chemical fertilizer thereby.

1.2.8 Iron Management: Endophytes in Siderophore Production Iron is an essential nutrient for plant growth and soil salinity is a leading cause for iron limitation. Plants and microbes overcome this iron limitation by producing ironchelating agents known as Siderophores. Effect of Iron on siderophore production, pH levels, antagonism, and root colonization was identified. Chapter 5 is providing a case study for salinity stress by managing iron via siderophore by Pseudomonads being the most dominant bacteria in the soil ecosystem after bacilli. This further strengthens how siderophore is important for soil nutrient management and sustainable farming. In the plant-soil interaction uptake of nutrients specifically, phosphorus, nitrogen, iron, and potassium is facilitated by plant growth-promoting rhizobacteria. Recently, endophyte was identified to produce a variety of siderophores such as pyoverdine, hydroxymate, ferrioxamines increase three times iron transportation efficiency to the plant for the development of root and shoot growth. Chapter 14 understands the applications of siderophore in bioremediation, weathering of soil-mineral particles, and plant growth as a major account.

1.2.9 Endophyte: Biotechnology and Bioinformatics Endophytes have emerged as an important tool for plant growth promotion and crop productivity enhancement. Their application is extending the frontiers of medicine industry and environmental remediation. Chapter 8 is an important part of elaborating major findings of endophytes and their applications in emerging ‘omic’ tools and to cast the light on biotechnological and bioinformatics aspects.

1 Endophytes in Mineral Nutrient …

9

1.3 Conclusions In current scenario, due to the abundant use of synthetic chemicals on crops, the sustainability of agriculture systems has distorted; the cost of cultivation has increased at a high rate; the income of farmers stagnated, and the provision of food security and safety has become a frightening challenge. For these reasons, estimation and re-investigation of the endeavors of endophytes via mineral nutrient mineralization become important. The harmless inputs in safeguarding soil health and the quality of crop products are holding the inspiration to scientists to re-discover multi-faceted roles of endophytes in plant interaction and benefits to agriculture. The use of endophytes is a relevant strategy for the efficient and rational use of agricultural resources with minimal effects of adverse environmental impacts that may boost water resources, ecosystems, or the quality of human life.

References Aeron A, Khare E, Jha CK, Meena VS, Aziz SM, Islam MT, Kim K, Meena SK, Pattanayak A, Rajashekara H, Dubey RC (2019) Revisiting the plant growth-promoting rhizobacteria: lessons from the past and objectives for the future. Arch Microbiol 28:1–2 Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Safe 156:225–246 Maheshwari DK, Dheeman S (2019) Field crops: sustainable management of PGPR. Springer, Switzerland, p 458 Pandey C, Bajpai VK, Negi YK, Rather IA, Maheshwari DK (2018) Effect of plant growthpromoting Bacillus spp. on nutritional properties of Amaranthus hypochondriacus grains. Saudi J Biol Sci 25(6):1066–1071

Chapter 2

Bioefficacy of Endophytes in the Control of Plant Diseases Fernando Matias Romero, Amira Susana Nieva, Oscar Adolfo Ruiz, Andrés Gárriz, and Franco Rubén Rossi

Abstract Plants establish multiple kinds of interactions with microorganisms, which can be neutral, beneficial, or detrimental for the plant host. Interactions also occur between endophytic microorganisms that colonize inner parts of plants, beneficial in nature, and able to promote plant growth both directly or indirectly. Direct plant-growth promotion includes the production of phytohormones, nitrogen fixation, and an increase in nutrient availability. On the other hand, endophytes can promote plant growth indirectly by contributing some beneficial attributes to plant health. Direct interaction between pathogens and endophytes also induces systemic resistance in the host, which allows the plant to respond faster and/or more intensively upon pathogen infection. Usually, endophytes share more than one of these mechanisms so the outcome of the interaction is the sum of different strategies. In this chapter, review on bacterial and fungal endophytes as potential biological control agents and their mechanisms of action have been documented. Besides it analyzes the most recent information about the nutrient uptake/management, specifically iron and nitrogen nutrition, with the biological control exerted by beneficial microorganisms. Keywords Endophytes · Biological control · Plant protection · Biological control agents

2.1 Introduction Control of plant diseases that reduce crop yields is a pressing need in modern agriculture, as the demands of stable and healthy food supplies by a growing human population must be guaranteed (Emmert and Handelsman 1999; Maheshwari 2013; Maheshwari and Annapurna 2017). Although there are several strategies to control plant diseases, there is an increasing interest in finding new technologies that can F. M. Romero (B) · A. S. Nieva · O. A. Ruiz · A. Gárriz · F. R. Rossi Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_2

11

12

F. M. Romero et al.

diminish or replace the use of agrochemicals, which can result in negative consequences to human health and the environment. In this way, biological control has attracted the interest of researchers over the last few years as a non-polluting alternative. One of the many strategies is to adopt microbial inoculants since they have several benefits compared to traditional chemical pest management. Being effective in small quantities, because they can multiply themselves, and at the same time, the host and the native microbial community control their spread (Berg 2009). Another advantage of bioinoculants is that the development of resistance is limited because of the involvement of different control mechanisms simultaneously. Moreover, microbial inoculants can be used in conventional or integrated pest management (Berg 2009). Thus, it can be achieved by (i) creation of environmental conditions favorable for the action of controlling microorganisms already present in the crops, (ii) through the genetic improvement of the host’s ability to interact with such microorganisms and (iii) by the genetic manipulation of the controlling microorganisms to give them advantageous characteristics, or the massive introduction of beneficial microorganisms into the host during the interaction process. The first microorganisms receiving attention as potential bioinoculants were those inhabiting the host-rhizosphere because they were proven to have several traits regarding plant promotion and antagonistic activity against plant pathogens (Bhattacharyya and Jha 2012). However, the microorganisms able to colonize the inner cells and tissues of plant hosts also improve plant growth and health and seem to be excellent candidates as biological control agents (BCAs) as observed by several workers (Berg and Hallmann 2006; Kloepper and Ryu 2006; Maheshwari 2017). It is due to endophytic nature which is better protected from harsh environmental conditions (i.e. extreme temperatures and UV light) and is in closer contact with their host’s cells and tissues than that of rhizosphere or phyllosphere microbes (Hallmann et al. 1997; Lindow and Brandl 2003). A great diversity of microorganisms were reported to exist as endophytes in cultivation-based studies (Reinhold-Hurek and Hurek 2011; Suryanarayanan 2013). Among the bacterial endophytes, most isolates belong to the phylum Proteobacteria, even though Firmicutes, Actinobacteria, and Bacteroidetes were also represented (Rosenblueth and Martinez-Romero 2006). However, diversity and richness of endophytic communities are much greater than those reported in culture-dependent studies (Dissanayake et al. 2018). In this trend, the use of next-generation sequencing (NGS) techniques has helped to unravel the structure and composition of endophytic communities more truly (Bulgarelli et al. 2012; Hong et al. 2019; Romero et al. 2014). The rapid development and the relative low costs of NGS have contributed to study microbial communities associated to different plant genotypes and/or growth stages (Manter et al. 2010; Marques et al. 2014) and is helping to get new insights into dynamics of plant-endophyte-pathogen interactions (Ardanov et al. 2012; Bulgari et al. 2014; Tian et al. 2019). Moreover, these culture-independent technologies not only exhibit the composition of the endophytic communities but also, facilitate the study of the functions performed by communities in the system. However, the analysis of biological control (BC) related traits in endophyte microbial communities is

2 Bioefficacy of Endophytes in the Control of Plant Diseases

13

still scarce. This information could lead to the development of improved and more efficient BCAs for sustainable agriculture. In this chapter, we will review and summarize some of the works reporting the use of microbial endophytes as biological control agents for different plant diseases and their mechanisms of action. Finally, we will discuss the nutrient uptake/management during biological control mediated by beneficial microorganisms.

2.2 Bacterial Endophytes as BCAs Endophytic microorganisms can display one or more mechanisms of action toward a specific pest or pathogen including direct interactions between endophytes, pathogens, and their hosts and this is one of the reasons why the use of microbial inoculants has notable advantages against chemical treatments (Fig. 2.1). The most commonly described mechanisms include inhibition of the pathogen by the

Fig. 2.1 Modes of action in plant-microbe interactions promoting plant growth and health

14

F. M. Romero et al.

production of antimicrobial compounds, competition for nutrients and space, induction of plant defense mechanisms, and parasitism. However, other modes of action remain to be explored in-depth, as the inactivation of pathogen germination factors or even degradation of virulence factors such as toxins produced by phytopathogens (Whipps 2001). Further, endophytes possess significant efficiency of protection since it is possible to prepare bioformulations with more than one microorganism for multiple trait benefits to combine desired traits and/or efficacy (Aeron et al. 2011; Baliyan et al. 2018; Pandey and Maheshwari 2007). For instance, Varo et al. (2016) tested several BCAs alone or in combinations, which showed great levels of protection against wilt in olives caused by Verticillium dahlia, reducing the incidence and mortality up to 90% (Varo et al. 2016).

2.2.1 Antagonism Since endophytes share a similar niche as of many phytopathogens colonizing plant cells and tissues, with different degrees of association direct antagonism between them is a reliable screening technique to screen potential BCAs from a collection of endophytic isolates. Microbial balance in the tissue of plant, as a micro-niche microbial homeostasis is also important to notice, where microbe-microbe interactions interplay. The native microbe of endophytic nature sometimes competes with the other invading microbe under natural conditions. The in vitro proves of this phenomenon are constant and yet few. Direct inhibition of pathogens is mainly mediated by the synthesis of antibiotics, volatile production of hydrogen cyanide (HCN), and antifungal metabolites (Raaijmakers et al. 2002, 2010). Antibiotics encompass a chemically heterogeneous group of organic, low-molecular-weight compounds. At low concentrations, these are deleterious to the growth or metabolic activities of other microorganisms, and most BCAs bacteria produce multiple antibiotics with different degrees of efficacy against pathogens, some of them with overlapping activity. Several compounds have been purified and identified from biocontrol bacteria. For example, pyrrolnitrin is produced by bacteria from the genus Pseudomonas and Burkholderia, which has been proven to be effective against a wide variety of plant pathogens such as Rhizoctonia solani, Botrytis cinerea, V. dahliae, and Sclerotinia sclerotiorum (Raaijmakers et al. 2002). Moreover, mutant strains unable to produce this compound lost the in vitro and in planta ability to control R. solani (Hill et al. 1994). In turn, 2,4diacetylphloroglucinol (DAPG) is a phenolic antibiotic produced by BCAs from the genus Pseudomonas that exhibits antibacterial, antifungal, and anthelminthic activity (Haas and Defago 2005; Weller et al. 2007). DAPG not only was proven to inhibit the growth of pathogens directly but also, it has been demonstrated that Arabidopsis thaliana inoculated with Pseudomonas sp. mutant strains unable to produce DAPG are impaired in developing induced systemic resistance (ISR) against Pseudomonas syringae pv. tomato (Weller et al. 2012). Phenazines are also a class of well-studied natural antibiotics that are produced by diverse plant-associated bacteria, exhibiting

2 Bioefficacy of Endophytes in the Control of Plant Diseases

15

unique redox properties and broad-spectrum antibiotic activity, and playing a wide variety of roles in nature (Mavrodi et al. 2006). Endophytes are essential to the production of several secondary metabolites in grasses, in the process of gummosis in trees, and the production of useful metabolites such as alkaloids, pestaloside, cryptocandin, enfumafungin, subglutinols, etc., for the host plant (Maheshwari and Annapurna 2017). The transformation of P. fluorescens strain Q8r1-96 with the biosynthetic locus leading to the production of phenazine-1-carboxylic acid, a precursor of several phenazine compounds, conduces to an increase in the biocontrol efficacy against Rhizoctonia root rot in wheat. In this trend, a lower dose of the transformant antagonist is required to exert the similar level of control exerted by the parental strain (Huang et al. 2004). The presence of these traits in soils is thought to explain disease decline in suppressive soils, in which specific soil-borne plant pathogens cause only limited disease although the pathogen and susceptible host plants are both present. However, the quantification of these characteristics in different types of soils has no clear correlation between the presence of antibiotic synthetic genes and disease suppression (Garbeva et al. 2004; Imperiali et al. 2017). Further analysis is required to understand how these are expressed genetically and regulated in soil and/or inside plants. Other metabolites with direct action against bacteria and fungi are lipopeptides such as iturin, surfactin, thanamycin, and fengycin (Ongena and Jacques 2008; Raaijmakers et al. 2010); and also the polyketide antibiotics bacillaene, difficidin, and macrolactin produced mainly, but not exclusively, by different strains of the genus Bacillus. The role of these compounds in biocontrol activity was also evidenced by the use of mutant strains defective in their production. For instance, the biocontrol activity of B. subtilis strain 6051 against P. syringae in Arabidopsis was impaired when a mutant strain unable to produce surfactin was used (Bais et al. 2004). Similarly, Pseudomonas strain SH-C52 reduces the incidence of stem rot disease of groundnut, whereas a thanamycin-deficient mutant strain was less effective (Le et al. 2012). Non-ribosomal peptides also contribute to the antagonism against bacteria and fungi (Abdalla and Matasyoh 2014). For instance, Tontou et al. (2015) demonstrated that an endophytic strain of P. synxantha isolated from Actinidia chinense showed antagonism against P. syringae pv. actinidiae (Psa) in vitro. To find out the molecular mechanisms involved in the antagonism, a mini transposon-mutant library was constructed and antagonism-deficient mutants were selected. Molecular characterization of these mutants showed that three genes could be involved in antagonistic activity, an acyl-homoserine lactone acylase gene, a glucose-6-phosphate dehydrogenase gene, and an mbtH-like gene. As these genes are directly or indirectly involved in the synthesis of non-ribosomal peptides, the authors claimed that these molecules are involved in the antagonistic ability of P. synxantha (Tontou et al. 2015). However, it is worthy to mention that these genes could also be affecting other antagonismassociated mechanisms. Thus, it has been shown that quorum sensing perturbation by the action of acyl-homoserine lactone degrading enzymes can interfere with interspecies competition (Amara et al. 2011; Kusari et al. 2014).

16

F. M. Romero et al.

Even though the identity of the antimicrobial molecules has not been determined so far, several other studies proved that endophytic bacteria produce compounds with antimicrobial activity. These studies typically used cell-free supernatants from the cultures of these isolates and to inhibit the in vitro growth of phytopathogens. For instance, bacterial endophytes identified as Pseudomonas, Bacillus, and Pantoea isolated from field-grown tomato leaves showed antagonism against bacterial (P. syringae) and fungal (Botrytis cinerea) pathogens in vitro and planta (Romero et al. 2016). Moreover, their cell-free supernatants were able to inhibit the germination of conidia from B. cinerea for about 30–60% and also stopped the growth of P. syringae when added to growth media. Additional pieces of evidence of antibiotic production were demonstrated using a semi-purified ethyl acetate extract of the endophyte B. velezensis EB-39 against Xanthomonas campestris subsp. citri (Rabbee et al. 2019). Interestingly, this extract showed similar inhibitory activity to that observed in confrontation assays between EB-39 and X. campestris. Purification and identification of new compounds from new isolates will increase the possibility to develop new biocontrol strategies using whole microbes or their cell free metabolites alone. The presence of genes involved in the biosynthesis of different antimicrobial compounds was also used as an indication of the ability to produce this kind of metabolites. An analysis performed on cultivable bacterial endophytes from mulberry cultivars having different resistance to sclerotiniosis showed that endophytic communities from resistant genotypes are more diverse than those from the sensible ones (Xu et al. 2019). In this work, dual-culture assays were performed with these endophytes against S. sclerotiorum, B. cinerea, and Colletotrichum gloeosporioide and most of the isolates that inhibit fungal growth were positive for the presence of genes involved in the biosynthesis of antimicrobial compounds, such as polyketides, non-ribosomal peptides, surfactin, iturin, and fengycin (Xu et al. 2019). Following this approach, Cui et al. (2019) isolated a B. amyloliquefaciens strain from Chinese cabbage with antagonistic activity against Pectobacterium carotovorum subsp. carotovorum, the causal agent of soft rot, possess genes involved in polyketides and dipeptide biosynthesis and showed a level of protection up to 75% in greenhouse experiments (Cui et al. 2019). It is worthy to mention that the mere presence of these biosynthetic genes is not sufficient to confirm the production of the antimicrobial molecules. For instance, Hazarika et al. (2019) demonstrated that a B. subtilis strain isolated from sugarcane as well as cell-free supernatants obtained from its culture showed antagonism against several pathogens. Moreover, it was positive for the presence of different genes involved in the synthesis of antimicrobial compounds, even though only one of them was detected in supernatants (surfactin) (Hazarika et al. 2019). This observation indicates that gene expression in combination with gene presence would be a more accurate indicator of antagonistic potential. Volatile organic compounds (VOCs) are also responsible for the ability of certain isolates to inhibit the in vitro growth of different pathogens. For instance, an endophytic isolate from black pepper roots identified as P. putida inhibits the growth of several plant pathogens due to the production of volatile compounds as revealed by Gas Chromatography/Mass Spectrometry (GC/MS) (Sheoran et al. 2015). Moreover, the application of some of these chemically synthesized VOCs showed a high

2 Bioefficacy of Endophytes in the Control of Plant Diseases

17

percentage of protection on black pepper shoots against Phytophthora capsici, especially when these compounds were applied at low concentrations (Agisha et al. 2019). The production of VOCs was also evidenced and identified in two isolates from cocoa that showed antagonism against the causal agent of a black pod, Phytophthora palmivora, both in vitro and in planta (Alsultan et al. 2019). The role of VOCs in plant protection is not only due to the direct effect on pathogen’s growth as there is evidence that 2,3-butanediol and acetoin can induce systemic resistance to pathogens (Ryu et al. 2004).

2.2.2 Induction Disease Resistance in Plants The recognition of microbial cell components and/or their metabolites can induce in the host’s physiological state allowing them to respond faster and/or to a greater extent to future pathogenic attacks. This phenomenon is called induced systemic resistance (ISR) and shares characteristics with another type of systemic resistance triggered by a previous attack of the necrosis-producing pathogen (SAR, systemic acquired resistance). There are two possible molecular mechanisms activated during ISR. Thus, endophyte-inoculation can induce the expression of defense-related genes per se, or on the other hand, the presence of beneficial microorganisms primes plants for enhanced defense responses. In primed plants, defense responses are not activated directly but are potentiated upon pathogen attack, resulting in enhanced resistance (van Wees et al. 2008). Both ISR and SAR contribute to resistance to a wide range of pathogens in systemic host´s tissues. However, the molecular mechanisms underlying both processes may differ. It was initially proposed that ISR is independent of salicylic acid (SA) signaling pathways but dependant of jasmonic acid (JA) and ethylene (ET), while SAR is dependant of SA and variable dependant of JA and ethylene (van Loon et al. 1998). However, a great number of systems studied afterward demonstrated that beneficial microorganisms induce resistance by activating both SA- and JA-signaling pathways (Mathys et al. 2012; Niu et al. 2011, 2012) or the SA-signaling pathway alone (Tjamos et al. 2005; van de Mortel et al. 2012). Thus, it is probable that nature and the molecular mechanisms underlying ISR depends on particular combinations of plant-beneficial microorganism-pathogen. Regarding endophyte-ISR induction, it would be strictly necessary to test that endophyte and pathogen are physically separated in the plant to ensure that the mechanism involved in protection is ISR (Kloepper and Ryu 2006). This is difficult to perform with microbial endophytes that colonize the entire plant. In this section, we will discuss some examples of bacterial endophytes inducing defense responses in their host independently of their colonization pattern. Changes in gene expression due to endophyte inoculation can be both local (at the site of inoculation) and systematic (in inoculated and not inoculated tissues). A clear example of systematic responses is the interaction between olives and the endophytic bacterium P. fluorescens PICF7, which conduce to the overexpression of defense-related genes in both roots and

18

F. M. Romero et al.

leaves (Gómez-Lama Cabanás et al. 2014; Schilirò et al. 2012). Another example of induced resistance was described by Sahu et al. (2019), where three Bacillus strains from a collection of endophytes from tomato plants were selected due to their antagonism to Sclerotium rolfsii. These isolates reduced disease incidence up to 67% under greenhouse conditions (Sahu et al. 2019). Moreover, endophyte-inoculation reduced the reactive oxygen species (ROS) generated at the site of the S. rolfsii infection and induced the expression of pathogenesis-related (P R) genes. In this trend, one of the isolates was able to induce the expression of genes PR1a, PR2b, and PR3 in absence of the pathogen, while others showed a mild induction of these genes that was enhanced upon infection with the pathogen. Further, these isolates were able to induce the activity of defense-related enzymes such as phenylalanine ammonia-lyase (PAL), peroxidase, polyphenol oxidase, and ascorbic acid oxidase (Sahu et al. 2019). Importantly, besides their roles in the synthesis of bioactive molecules, these enzymes are involved in plant cell wall reinforcement. Thus, it is probable that their activities can help to prevent the infection by necrotrophic pathogens. This might explain also the mechanism of protection exerted by two Stenotrophomonas strains with the ability to colonize Arabidopsis leaves, which modified the expression of different enzymes involved in cell wall synthesis and reduce lesion sizes provoked by the necrotrophic pathogens S. sclerotiorum and B. cinerea (Marina et al. 2019). Accordingly, when cell wall extracts obtained from inoculated leaves were used as a substrate for pathogens growth on agar plates, there was a reduction in fungal colony radius compared to plates supplemented with cell wall extracts from mockinoculated leaves. Besides, Stenotrophomonas inoculation induced callose deposition and expression of PR genes associated with the SA and JA signaling pathways. Similarly, endophytes isolated from Solanum tuberosum able to induce resistance to Pectobacterium atrosepticum in potato and are able to increase defense-related enzyme activities both before and after pathogen challenge. Moreover, these isolates primed the expression of PR genes involved in both, the SA and JA signaling pathways (Ardanov et al. 2011). The ability to induce the expression of genes involved in phytohormones signaling was also reported by an apoplast-colonizing endophyte from canola leaves (Romero et al. 2019). This isolate showed antagonism against different phytopathogens in vitro and planta. The mechanisms proposed to be involved include the production of antimicrobial compounds as well as the ability to induce defense mechanisms mediated by SA and JA in the host. Transcriptional changes induced by beneficial microbes usually differ from the changes induced by pathogens, mainly in the intensity of induction (Romero et al. 2017). Burkholderia phytofirmans PsJN induced the expression of defense-related genes in grapevine cell suspension but to a lesser extent than non-host bacterium P. syringae pv. pisi. Both bacteria-induced medium alkalization, but the endophyte did not provoke ROS production or cell death, which are observed in pathogentreated cells (Bordiec et al. 2011). This isolate also primed the expression of PR genes involved in the SA and JA signaling pathways upon pathogen infection in Arabidopsis, showing more sustained expression of PDF1.2, a JA dependent PR gene (Su et al. 2017).

2 Bioefficacy of Endophytes in the Control of Plant Diseases

19

Several plants possess different compounds with antimicrobial activity; this is the case of Allium sativum (garlic) that produces alliin, an alkyl cysteine sulphoxide that is converted to allicin by the enzyme alliinase. Wang et al. (2019) isolated endophytes from garlic and selected two strains showing antagonism against Sclerotium cepivorum, the causal agent of white rot disease. Also, these isolates reduced the disease index by up to 66% in greenhouse assays. The authors proposed that there is not only a direct antagonistic effect due to the production of extracellular enzymes, but also an induction in the production of antimicrobial products in the host. Thus, inoculation with one of the isolates primed the expression of alliinase and the accumulation of alliin (Wang et al. 2019).

2.2.3 Parasitism This kind of interaction is more commonly observed in bacteria-fungi and fungi-fungi interactions. During these interactions, fungal cells are lysed due to breaking down to mycelial cell wall. These effects are due to the action of extracellular enzymes such as glucanases, chitinases, and proteases as well as antifungal compounds (Chauhan et al. 2016; Whipps 2001). For instance, poplar canker provoked by Cytospora chrysosperma, Phomopsis macrospora, and Fusicoccum aesculi can be controlled with an efficiency up to 90% by bacterial endophytes with antagonistic activity against these pathogens due to production of extracellular enzymes such as β-1,3glucanases, proteases, and chitinases (Ren et al. 2011). The important role of βglucanases was evidenced recently in the interaction between B. halotolerans, a cotton endophytic strain, and the pathogen V. dahliae. This endophyte was selected because of the ability to inhibit conidial germination and mycelial growth of the pathogen in vitro and showed β-glucanase activity. Mutant and overexpressing strains were generated to elucidate the role of β-glucanase. In vitro antagonism assays using the mutant strain exhibited diminished antifungal activity against V. dahliae compared to wild type or the complementary strain. In turn, bioassays using the overexpressing strain showed a greater protective effect compared to wild type, as the disease indexes diminished from 17.86 (wild type strain) to 8.33 (overexpressing strain) after 45 days post-inoculation (Zhang et al. 2019a). As mentioned earlier, the protective effects observed by endophyte inoculation usually involved more than one mechanism. For instance, an Enterobacter strain isolated from finger millet roots, has been found as an endophyte in other crops such as maize and wheat showed antagonism against Fusarium graminearum among other pathogens, and it was able to reduce disease symptoms up to 90% in greenhouse trials (Mousa et al. 2016). Interestingly, during confrontation assays, Enterobacter sp. seemed to be attracted to fungal cells, formed biofilms over fungal hyphae, and finally destroy fungal cells. Moreover, when inoculated on roots, the isolates showed the ability to induce proliferation of root hairs and establish a physicochemical barrier to trap and degrade the pathogen hyphae. Biocontrol and antagonistic ability of these endophytes require the production of phenazine, c-di-GMP-dependent signaling

20

F. M. Romero et al.

pathway, and resistance to a Fusarium-derived antibiotic. This was evidenced due to the construction of a Tn5-mutant library, selecting mutant strains that have lost the ability to inhibit the growth of F. graminearum. We here described just some examples of bacterial endophytes with different mechanisms of action, but there is a consistent reporting on the isolation of new endophytic strains from diverse genera of plants to inhibit different phytopathogens. Most of them demonstrated significant effects as BCAs with high levels of protection in planta (Asghari et al. 2019; Etesami and Alikhani 2016; Ferrigo et al. 2017; Ghazalibiglar et al. 2016; Zhang et al. 2019b). Although the exact mechanism of biocontrol exerted by these endophytes has not fully explored so far, these constitute a valorous collection of microorganisms for the development of biotechnological applications (Maheshwari and Annapurna 2017).

2.3 Fungal Endophytes The term “endophyte” is applied to fungi which has been redefined according to the permanence of the microorganism inside host tissues, the symptomless character of the infection, and the benefits provided by the fungi to the plant host. This is because, over the years, research regarding fungal endophytes has incorporated functional information besides infection traits. In this trend, several functions such as defensive mutualism, nutritional uptake, and the production of secondary metabolites improving plant fitness have been considered (Rodriguez et al. 2009; Schulz et al. 2002). Hyde and Soytong (2008) analyzed several definitions of fungal endophytes taking into account different traits, from infection and symptom development to ecological functions. This changed the study of fungal endophytes into new perspectives taking into consideration the permanence of mutualism, stability of the interaction, and evolutionary features. Fungal endophytes belong to a group with great taxonomic diversity (Arnold et al. 2000, 2001; Rodriguez et al. 2009), which are classified according to their identity and functional roles. Thus, fungal endophytes were divided into two groups: Clavicipitaceous and Non-Clavicipitaceous (Rodriguez et al. 2009). Nevertheless, it has been exhibited that most fungal endophytes studied to date corresponds to the phylum Ascomycetes (Lugtenberg et al. 2016).

2.3.1 Clavicipitaceous Fungal Endophytes (Grass-Endophytes Interactions) Epichlöe-temperate grasses are the most studied models included in this category (Omacini et al. 2012). The interactions between grasses and endophytes are clustered in Group I, belonging to the Clavicipitaceae family in correspondence with the

2 Bioefficacy of Endophytes in the Control of Plant Diseases

21

classification proposed by Rodriguez et al. (2009). In these interactions, fungi inside plant tissues can produce ergot alkaloids that prevent against parasitoid infections, mainly represented by herbivores insects (Bacon et al. 1986; Torres et al. 2008). These plant-fungal interactions affect directly the insect abundance with consequences in the balance of the food-web dynamics (Omacini et al. 2001). Also, a recent study has demonstrated another protective mechanism involved in Epichlöe-grass systems that are based on the alteration of the plant odor to attract aphid predators (Fuchs and Krauss 2019). Endophytes-grass interactions have been described as mutualism. In this sense, Clay (1988) has described endophyte-grass interactions as a “defensive mutualism.” Further studies have demonstrated that the effects of these interactions depend on global factors, such as plant genotype and environmental conditions, leading to neutral situations or turning into a pathogenic outcome (Faeth and Fagan 2002; Müller and Krauss 2005; Saikkonen et al. 2006). The research conducted on endophyte-grass interactions is oriented to a better understanding of the effects on all the components of the ecosystem. For example, it has been studied the relation between grass-endophytes, growth and fecundity of their hosts, and the further reconstruction of the plant community with the implication in the restoration of prairies (Moore et al. 2019). On the other hand, some studies analyzed the effect of endophytes on other soil microorganisms such as mycorrhizal fungi (Kalosa-Kenyon et al. 2018), and the cattle in agro-ecosystems (Bultman et al. 2018). Since transmission of grass-endophytes occurs horizontally as well as vertically, it protects all the plant tissues in every plant generation (Rodriguez et al. 2009). This phenomenon would help the establishment of certain plant species in particular environments, which denotes the evolutionary impact of this kind of interaction, in which the permanence of plant species may be a consequence of the interaction with particular fungal endophytes (Saikkonen et al. 2004). Thus, grassland protection conferred by endophytes makes these microbes beneficial for augmenting integrated pest management programs and considering sustainable agriculture premises (Kauppinen et al. 2016).

2.3.2 Non-Clavicipitaceous Fungal Endophytes Despite most research on fungal endophytes is represented by the grass-endophytes interactions, there is increasing interest in fungal endophytes belonging to the NonClavicipitaceous group, as these fungal endophytes are also able to impair the proliferation of pathogens and decrease the severity of symptoms by direct interaction (Arnold et al. 2000). Interestingly, fungal endophytes can reduce pathogenic infections even when both organisms are closely related. For example, Colletotrichum magna can infect Cucumis sativus and confer protection against C. orbiculare and F. oxysporum (Redman et al. 1999). This evidence demonstrates that despite the pathogenic role of certain fungi, such as Fusarium species, they are also able to

22

F. M. Romero et al.

perform endophytic interactions and even promote plant growth as evidenced by Nieva et al. (2019) who demonstrates growth promotion effects by F. solani in the model legume Lotus japonicus (Nieva et al. 2019). Root fungal endophytes play an important role in plant growth due to involvement in nutrient and water acquisition (Lugtenberg et al. 2016). Dark septate endophytes (DSE) constitute a group of fungal endophytes characterized by their ability to colonize roots without causing damage and having melanin in their hyphae. They have been defined as multifunctional, taking part in different processes such as nutritional uptake improvement, abiotic stress tolerance, and heavy metal sequestration (Mandyam and Jumpponen 2005). Besides, they might play important roles as BCAs. In this trend, there is evidence of DSE fungi controlling V. dahliae in tomato, showing a reduction of up to 30% in disease symptoms (Andrade-Linares et al. 2011). Another example is the endophytic fungus Phialocephala fortinii, exhibited75% of inhibition against F. oxysporum in Asparagus officinalis (Narisawa 2018). Besides, in vitro antagonism between DSE, ectomycorrhizal fungi, and pathogens such as Pythium intermedium, Phytophthora citricola, and Heterobasidion annosum has been evaluated (Berthelot et al. 2019). These results could help the development of fungal consortia to be used as phytostimulant and/or biocontrol products. Fungi belonging to the Trichoderma genus have been demonstrated to be important biocontrol agents as they manage to induce ISR by activating the JA and SA signaling pathways (Mukherjee et al. 2012). To date, this organism is the most important bio-fungicide developed and commercialized around the world (Verma et al. 2007), where the use of different Trichoderma spp. strains in disease biocontrol have been extended to several crops and landscapes. Moreover, colonization of maize plants by T. atroviride also induces resistance against herbivores such as Spodoptera frugiperda (Contreras-Cornejo et al. 2018). In turn, yeast endophytes have been scarcely studied to date. There are evidence that these organisms survive as endophytes in Z. mays (Nassar et al. 2005) and in stomata and xylem vessels of Citrus sinensis (Gai et al. 2009), but their potential as biocontrol agents is yet to be evaluated. Recently, Rhodotorula and Cryptococcus sp. have been proposed as biocontrol agents against the “witches’ broom disease” of cacao (Ferraz et al. 2019).

2.3.3 Mechanisms of Biological Control by Fungal Endophytes Biological control mediated by fungal endophytes involves the production of secondary metabolites, such as alkaloids, antibiotics, and/or lytic enzymes (Gao et al. 2010). Also, as mentioned earlier for bacterial BCAs, volatile compounds produced by fungal endophytes have been proposed as good biological control agents (Morath et al. 2012). For example, volatile metabolites produced by the endophyte

2 Bioefficacy of Endophytes in the Control of Plant Diseases

23

F. oxysporum CanR-46 control the impact of S. sclerotiorum in Brassica napus, demonstrating a 94.5% mycelial growth inhibition (Zhang et al. 2014). Moreover, fungal endophytes have been proposed as sources of useful secondary metabolites (Petrini et al. 1993; Schulz et al. 2002; Shukla et al. 2014). In this trend, there is an interesting research field focused on the bioactive compounds produced by endophytic fungi and their applications in agriculture, medicine, and industry (Zhao et al. 2011). The use of endophytes to promote plant fitness could improve the production of medicinal plants as well as their bioactive-derivate compounds in medicinal plants (Jia et al. 2016). Besides parasitism and antibiosis, Trichoderma spp. can manage to induce lipid transferase proteins to confer defense against Phytophthora capsici (Bae et al. 2011). Induction of systemic resistance was also evidenced by the activation of defenserelated enzymes on cucumber plants inoculated with a non-pathogenic strain of Colletotrichum magna (Redman et al. 1999). Timing is an important factor to ensure a successful biocontrol strategy. In this trend, the order of arrival of endophytes and pathogens in Phaseolus lunatus was analyzed (Adame-Álvarez et al. 2014). Interestingly, the antagonist effect of the endophytes on the pathogen was only successful when the endophyte colonization occurs first; otherwise, endophyte inoculation after pathogen infection rather facilitates disease development (Adame-Álvarez et al. 2014). As mentioned earlier, fungal endophytes can trigger ISR in the host. The mechanisms involved in this response are analogous to those imposed by mycorrhizal fungi, involving the SA and JA signaling pathways (Jung et al. 2012; Pozo and AzcónAguilar 2007). In a previous study, it has been demonstrated that JA is necessary for the biocontrol response in tomato triggered by the infection of a non-pathogenic F. solani strain (Kavroulakis et al. 2007). In this system, F. solani can elicit ISR against Septoria lycopersici by expression of pathogenesis-related (PR) genes in roots. In agreement with the effects reported for bacterial endophytes, it has been demonstrated that ethylene, as well as JA, is required for ISR triggered by fungal endophytes (Kavroulakis et al. 2007). Nevertheless, a recent study has demonstrated that inoculation with an endophytic Fusarium strain can trigger the systemic response independently of JA, SA, and ethylene (Constantin et al. 2019). As exposed above, the interactions between grasses and fungi belonging to the Clavicipitaceous group constitute protective mutualisms. The effect of the endophyte-infected grasses (E+) on the dynamic population of the insect pest has been extensively compared with the non-endophyte infected grasses (E−). For example, Lolium multiflorum-E. occultans interaction reduces the aphid population by 64% and the nymph by 81%, consequently, the fecundity of the aphid populations is strongly affected (Bastias et al. 2017b). Complementary to the protection conferred by the alkaloids production, recent studies on the endophyte-grass interactions has demonstrated the ability of the endophyte to enhance the plant immunity through mechanisms involving the JA-mediated response, by the promotion of JA-signaling and repression of SA-signaling defenses (Bastias et al. 2017a). Besides, the interaction between Lolium pernenne-Epichlöe

24

F. M. Romero et al.

festucae var lolii system displays the differential expression of 38% of the genes expressed between E+ and E− plants (Dupont et al. 2015). The property of some entomopathogenic fungi to control insect pests, and at the same time survive as endophytes, may also improve ISR and confer dual protection (Jaber and Ownley 2018). In this trend, it might be possible that biological control transcends the plant-microorganism system which can be extrapolated to other components of the ecosystem.

2.4 The Relation Between Nutrient Management and Biological Control Besides the roles played by endophytes in biological control described in this chapter, many pieces of evidence show that they are also involved in mineral nutrition. This is important since the facilitation of nutrient uptake by their hosts contributes to plantgrowth promotion (Maheshwari and Annapurna 2017). Even though there is little information regarding the relation of nutrient uptake/management with biological control traits displayed by beneficial microorganisms, there is evidence of crosstalk between iron starvation responses and ISR triggered by beneficial rhizobacteria. The comparison of the genes induced by Pseudomonas spp. WCS417 with the iron-deficiency root transcriptome showed that 20% of the regulated genes are activated in both conditions (Zamioudis et al. 2015). One of these genes is the rootspecific R2R3-type MYB transcription factor MYB72, that was described as a key component of ISR triggered by beneficial microbes (Segarra et al. 2009; Van der Ent et al. 2008) as well as an important player in the iron deficiency response (Buckhout et al. 2009; Colangelo and Guerinot 2004). Interestingly, a deeper insight into the molecular mechanisms involved in WCS417-induced ISR showed a set of five MYB72-dependent transcripts. Among them, three genes have been reported previously to be controlled by FIT1 (Fe-deficiency Induced Transcription Factor 1), the central transcriptional regulator of the iron deficiency response in Arabidopsis roots. These three FIT- and MYB72-regulated genes encode the nitrate transporter NRT1.8, the β-glucosidase BGLU42, and the cytochrome P450 monooxygenase CYP71B5 (Zamioudis et al. 2014). Interestingly, BLU42 over-expression in Arabidopsis gives resistance to different pathogens. On the other hand, bglu42 mutant line is unable to trigger WCS417-mediated ISR. Moreover, the mutant lines myb72 and bglu42 are impaired in the accumulation and secretion of fluorescent phenolic compounds that are produced via the phenylpropanoid route and excreted in the root vicinity playing a critical role in iron acquisition by facilitating its mobilization (Zamioudis et al. 2014). The induction in MYB72 expression was also observed in plants treated with VOCs produced by WCS417, and this expression was accompanied by the induction of different genes involved in iron uptake and transport such as Iron-Regulated Transporter 1 (IRT1), Ferric Reduction Oxidase 2 (FRO2) and FIT1. Also, it has been

2 Bioefficacy of Endophytes in the Control of Plant Diseases

25

shown that VOCs from other Arabidopsis native rhizospheric bacteria induced the expression of MYB72. Strikingly, the induction of iron deficiency markers (FRO2 and IRT1) was only observed when plants were inoculated with ISR-inducing bacteria, while the inoculation with similar bacteria that do not induce ISR was unable to induce the expression of iron management genes. This indicates a close relationship between the induction of ISR and the activation of iron management response (Zamioudis et al. 2015). It is important to mention that both the induction of MYB72 and the iron-related genes by VOCs is independent of the availability of iron in roots, but it is dependent on signals from above-ground parts of the plant (Zamioudis et al. 2015). Recently, it has been shown that the induction of the iron-deficiency response mediated by WCS417 does not depend on iron nutrition. In this trend, the plant growth promotion effect triggered by this bacterium was also observed under iron limitation conditions (Verbon et al. 2019). Since the response triggered in the roots by WCS417 inoculation showed to be dependent on shoot-to-root signaling, the authors evaluated if iron content in the leaves could affect this response. However, they demonstrated that iron content in the aerial parts of the plant did not affect the WCS417-induced response on roots. Also, this response was independent of the iron transport in the phloem mediated by the phloem-specific iron transporter (OPT3) (Verbon et al. 2019). Altogether, the information generated in these works confirms that the induction of ISR triggered by beneficial microbes is intimately related to an activation of the iron metabolism and this response is independent of the iron content that requires shoot-to-root signaling. More research is needed to determine the exact mechanisms involved in this process. As described early, some endophytic fungi can diminish disease symptoms caused by pathogens. This is the case of an endophyte strain of Colletotrichum tropicale that reduces the infection provoked by P. palmivora in cocoa plants (Christian et al. 2017). Recently, the authors analyzed the uptake and distribution of nitrogen in response to endophyte and pathogen inoculation by pulsing the soil with nitrogen-15 (15 N) and then tracing 15 N uptake and its subsequent distribution to whole plants and individual leaves. They demonstrated that endophyte-inoculated plants showed significantly greater 15 N uptake than endophyte-free plants. However, the total nitrogen amount did not vary in each treatment (Christian et al. 2019). Moreover, pathogen inoculation did not affect the 15 N content, but the co-inoculation with the endophyte and the pathogen showed a correlation between the 15 N content and the pathogen damage (Christian et al. 2019). These results suggest that endophyte colonization can modify nutrient acquisition and affect N distribution within plant tissues under pathogenic conditions.

2.5 Conclusions The main goal of the research in the field of biocontrol is to provide new and improved tools for the development of biotechnological products for disease management.

26

F. M. Romero et al.

Thus, the first step for novel product development is the exploration and discovery of new potential candidates as BCAs. Ultimately, the success of biocontrol relies on how well the search and screening process is done. Although there is not a unique and correct way to perform it, researchers should always keep in mind the final goal of the product. For example, looking for microorganisms to control postharvest diseases requires screening of microbes able to grow and colonize the surface of the fruits quickly to exclude pathogens. Another strategy to take into consideration is to conduct the isolation of potential candidates from the same or similar habitats that they will be used. If the BCAs were pretended to be used to control tomato diseases under greenhouse cultivation, it would be recommendable to isolate microbes from tomato plants cultivated under these conditions, so microorganisms will be better adapted. Moreover, screening should be performed in a way that mimics the conditions under which the agent will be used to increase control efficiency. Besides, ideal BCAs should be efficient in a wide range of environmental conditions. Then, it is important to test potential BCAs at field conditions during different years and climate conditions, and unless the BCAs is being intended to be used in a relatively constant environment it is important to determine to what extent environmental parameters such as temperature, moisture, and soil type affect biological control efficacy. On the other hand, understanding the mechanisms involved in the control by the BCAs will also help to develop a better and more efficient control strategy. For instance, parasitic BCAs will require the application of large doses of biocontrol microbes to ensure a population high enough to improve control. However, if the main control mechanism is the induction of resistance in the host, lower doses will be necessary. Finally, another important aspect that needs to be considered is the composition of native microbial communities where the BCAs will be inserted. Also, the modification in the communities’ structure provoked by the application of BCAs must be analyzed because unwanted effects could be originated. For example, there could be negative effects if the incorporation of biocontrol agents reduces the number of other beneficial microbes in the plant-associated communities. Nowadays, the use of nextgeneration sequencing techniques has led to a better understanding of the structure of plant-associated microbial communities, which will be essential to improve the design and application of biological control strategies. Regarding the relationship between nutrient management and biological control, the available information is scant. Certain reports relate the iron deficiency response with the induction of ISR mediated by beneficial microorganisms. Also, evidence has been provided on the uptake and distribution of nitrogen during the plant-endophytepathogen interaction. However, the mechanisms involved in these processes, as well as the true biological meaning of these responses yet to be explored for their bioefficacy in a befitting manner. Acknowledgments This work was supported by grants of Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) (PICT 2014-3718, 2014-3648, 2015-1803). A.G, F.R.R and O.A.R are members of the Research Career of CONICET. F.M.R is member of the Research Career of Comisión de Investigaciones Científicas (CIC). A.S.N is a postdoctoral fellow of CONICET.

2 Bioefficacy of Endophytes in the Control of Plant Diseases

27

References Abdalla MA, Matasyoh JC (2014) Endophytes as producers of peptides: an overview about the recently discovered peptides from endophytic microbes. Nat Prod Bioprospect 4:257–270. https:// doi.org/10.1007/s13659-014-0038-y Adame-Álvarez R-M, Mendiola-Soto J, Heil M (2014) Order of arrival shifts endophyte–pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol Lett 355:100–107. https://doi.org/10.1111/1574-6968.12454 Aeron A, Dubey RC, Maheshwari DK, Pandey P, Bajpai VK, Kang SC (2011) Multifarious activity of bioformulated Pseudomonas fluorescens PS1 and biocontrol of Sclerotinia sclerotiorum in Indian rapeseed (Brassica campestris L.). Eur J Plant Pathol 131:81–93. https://doi.org/10.1007/ s10658-011-9789-z Agisha VN, Kumar A, Eapen SJ, Sheoran N, Suseelabhai R (2019) Broad-spectrum antimicrobial activity of volatile organic compounds from endophytic Pseudomonas putida BP25 against diverse plant pathogens. Biocontrol Sci Technol:1–21. https://doi.org/10.1080/09583157.2019. 1657067 Alsultan W et al (2019) Isolation, identification and characterization of endophytic bacteria antagonistic to Phytophthora palmivora causing black pod of cocoa in Malaysia. Eur J Plant Pathol. https://doi.org/10.1007/s10658-019-01834-8 Amara N, Krom BP, Kaufmann GF, Meijler MM (2011) Macromolecular inhibition of quorum sensing: enzymes, antibodies, and beyond. Chem Rev 111:195–208. https://doi.org/10.1021/cr1 00101c Andrade-Linares DR, Grosch R, Restrepo S, Krumbein A, Franken P (2011) Effects of dark septate endophytes on tomato plant performance. Mycorrhiza 21:413–422. https://doi.org/10.1007/s00 572-010-0351-1 Ardanov P, Ovcharenko L, Zaets I, Kozyrovska N, Pirttilä AM (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49. https:// doi.org/10.1016/j.biocontrol.2010.09.014 Ardanov P, Sessitsch A, Häggman H, Kozyrovska N, Pirttilä AM (2012) Methylobacterium-induced endophyte community changes correspond with protection of plants against pathogen attack. PLoS ONE 7:e46802. https://doi.org/10.1371/journal.pone.0046802 Arnold AE, Maynard Z, Gilbert GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105:1502–1507. https://doi.org/10.1017/S09537 56201004956 Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274. https://doi.org/10.1046/j.1461-0248.2000.00159.x Asghari S, Harighi B, Mozafari AA, Esmaeel Q, Ait Barka E (2019) Screening of endophytic bacteria isolated from domesticated and wild growing grapevines as potential biological control agents against crown gall disease. Biocontrol. https://doi.org/10.1007/s10526-019-09963-z Bacon CW, Lyons PC, Porter JK, Robbins JD (1986) Ergot toxicity from endophyte-infected grasses: a review. Agron J 78:106–116. https://doi.org/10.2134/agronj1986.00021962007800010023x Bae H et al (2011) Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol Plant-Microbe Interact 24:336–351. https://doi.org/10.1094/mpmi-09-10-0221 Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319. https://doi.org/10.1104/pp.103.028712 Baliyan N, Dheeman S, Maheshwari DK, Dubey RC, Vishnoi VK (2018) Rhizobacteria isolated under field first strategy improved chickpea growth and productivity. Environ Sustain 1:461–469. https://doi.org/10.1007/s42398-018-00042-0 Bastias DA, Martínez-Ghersa MA, Ballaré CL, Gundel PE (2017a) Epichloë fungal endophytes and plant defenses: not just alkaloids. Trends Plant Sci 22:939–948. https://doi.org/10.1016/j.tpl ants.2017.08.005

28

F. M. Romero et al.

Bastias DA, Ueno AC, Machado Assefh CR, Alvarez AE, Young CA, Gundel PE (2017b) Metabolism or behavior: explaining the performance of aphids on alkaloid-producing fungal endophytes in annual ryegrass (Lolium multiflorum). Oecologia 185:245–256. https://doi.org/10. 1007/s00442-017-3940-2 Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18. https:// doi.org/10.1007/s00253-009-2092-7 Berg G, Hallmann J (2006) Control of plant pathogenic fungi with bacterial endophytes. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes, vol 9. Soil Biology. Springer, Berlin Heidelberg, pp 53–69. https://doi.org/10.1007/3-540-33526-9_4 Berthelot C, Leyval C, Chalot M, Blaudez D (2019) Interactions between dark septate endophytes, ectomycorrhizal fungi and root pathogens in vitro. FEMS Microbiol Lett 366. https://doi.org/10. 1093/femsle/fnz158 Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. https://doi.org/10.1007/s11274-0110979-9 Bordiec S et al (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62:595–603. https://doi.org/10.1093/jxb/erq291 Buckhout TJ, Yang TJW, Schmidt W (2009) Early iron-deficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genom 10:147. https://doi.org/ 10.1186/1471-2164-10-147 Bulgarelli D et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. https://doi.org/10.1038/nature11336 Bulgari D, Casati P, Quaglino F, Bianco PA (2014) Endophytic bacterial community of grapevine leaves influenced by sampling date and phytoplasma infection process. BMC Microbiol 14:198. https://doi.org/10.1186/1471-2180-14-198 Bultman TL et al (2018) Complex interactions among sheep, insects, grass, and fungi in a simple New Zealand grazing system. J Chem Ecol 44:957–964. https://doi.org/10.1007/s10886-0180993-6 Chauhan AK, Maheshwari DK, Kim K, Bajpai VK (2016) Termitarium-inhabiting Bacillus endophyticus TSH42 and Bacillus cereus TSH77 colonizing Curcuma longa L.: isolation, characterization, and evaluation of their biocontrol and plant-growth-promoting activities. Can J Microbiol 62:880–892. https://doi.org/10.1139/cjm-2016-0249 Christian N, Herre EA, Clay K (2019) Foliar endophytic fungi alter patterns of nitrogen uptake and distribution in Theobroma cacao. New Phytol 222:1573–1583. https://doi.org/10.1111/nph. 15693 Christian N, Herre EA, Mejia LC, Clay K (2017) Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc R Soc B 284:20170641. https://doi.org/ 10.1098/rspb.2017.0641 Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16. https://doi.org/10.2307/1943155 Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412. https://doi.org/10.1105/tpc.104.024315 Constantin ME, de Lamo FJ, Vlieger BV, Rep M, Takken FLW (2019) Endophyte-mediated resistance in tomato to Fusarium oxysporum is independent of ET, JA, and SA. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.00979 Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J (2018) The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Appl Soil Ecol 124:45–53. https://doi.org/10.1016/j.apsoil.2017.10.004 Cui W et al. (2019) Biocontrol of soft rot of chinese cabbage using an endophytic bacterial strain. Frontiers in Microbiology 10. https://doi.org/10.3389/fmicb.2019.01471

2 Bioefficacy of Endophytes in the Control of Plant Diseases

29

Dissanayake AJ et al (2018) Direct comparison of culture-dependent and culture-independent molecular approaches reveal the diversity of fungal endophytic communities in stems of grapevine (Vitis vinifera). Fungal Divers 90:85–107. https://doi.org/10.1007/s13225-018-0399-3 Dupont P-Y et al (2015) Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol 208:1227–1240. https://doi.org/10.1111/nph.13614 Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiol Lett 171:1–9. https://doi.org/10.1111/j.1574-6968.1999.tb13405.x Etesami H, Alikhani HA (2016) Rhizosphere and endorhiza of oilseed rape (Brassica napus L.) plant harbor bacteria with multifaceted beneficial effects. Biol Control 94:11–24. https://doi.org/ 10.1016/j.biocontrol.2015.12.003 Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42:360–368. https://doi.org/10.1093/icb/42.2.360 Ferraz P, Cássio F, Lucas C (2019) Potential of yeasts as biocontrol agents of the phytopathogen causing cacao witches’ broom disease: is microbial warfare a solution? Frontiers in Microbiology 10. https://doi.org/10.3389/fmicb.2019.01766 Ferrigo D, Causin R, Raiola A (2017) Effect of potential biocontrol agents selected among grapevine endophytes and commercial products on crown gall disease. Biocontrol 62:821–833. https://doi. org/10.1007/s10526-017-9847-3 Fuchs B, Krauss J (2019) Can Epichloë endophytes enhance direct and indirect plant defence? Fungal Ecology 38:98–103. https://doi.org/10.1016/j.funeco.2018.07.002 Gai CS, Lacava PT, Maccheroni W Jr, Glienke C, Araújo WL, Miller TA, Azevedo JL (2009) Diversity of endophytic yeasts from sweet orange and their localization by scanning electron microscopy. J Basic Microbiol 49:441–451. https://doi.org/10.1002/jobm.200800328 Gao F-k, Dai C-c, Liu X-z (2010) Mechanisms of fungal endophytes in plant protection against pathogens. Afr J Microbiol Res 4:1346–1351 Garbeva P, Voesenek K, Elsas JDv (2004) Quantitative detection and diversity of the pyrrolnitrin biosynthetic locus in soil under different treatments. Soil Biology and Biochemistry 36:1453– 1463. https://doi.org/10.1016/j.soilbio.2004.03.009 Ghazalibiglar H, Hampton JG, van ZijlldeJong E, Holyoake A (2016) Evaluation of Paenibacillus spp. isolates for the biological control of black rot in Brassica oleracea var. capitata (cabbage). Biocontrol Sci Technol 26:504–515. https://doi.org/10.1080/09583157.2015.1129052 Gómez-Lama Cabanás C, Schiliro E, Valverde-Corredor A, Mercado-Blanco J (2014) The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Frontiers in Microbiology 5. https://doi.org/10. 3389/fmicb.2014.00427 Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319 Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914. https://doi.org/10.1139/m97-131 Hazarika DJ, Goswami G, Gautom T, Parveen A, Das P, Barooah M, Boro RC (2019) Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiol 19:71. https://doi.org/10.1186/s12866-019-1440-8 Hill DS et al (1994) Cloning of genes involved in the synthesis of pyrrolnitrin from Pseudomonas fluorescens and role of pyrrolnitrin synthesis in biological control of plant disease. Appl Environ Microbiol 60:78–85 Hong CE, Kim JU, Lee JW, Bang KH, Jo IH (2019) Metagenomic analysis of bacterial endophyte community structure and functions in Panax ginseng at different ages. 3 Biotech 9:300. https:// doi.org/10.1007/s13205-019-1838-x Huang Z, Bonsall RF, Mavrodi DV, Weller DM, Thomashow LS (2004) Transformation of Pseudomonas fluorescens with genes for biosynthesis of phenazine-1-carboxylic acid improves biocontrol of rhizoctonia root rot and in situ antibiotic production. FEMS Microbiol Ecol 49:243–251. https://doi.org/10.1016/j.femsec.2004.03.010 Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

30

F. M. Romero et al.

Imperiali N et al (2017) Relationships between root pathogen resistance, abundance and expression of Pseudomonas antimicrobial genes, and soil properties in representative Swiss agricultural soils. Front Plant Sci 8:427. https://doi.org/10.3389/fpls.2017.00427 Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45. https://doi.org/10.1016/j. biocontrol.2017.01.018 Jia M, Chen L, Xin H-L, Zheng C-J, Rahman K, Han T, Qin L-P (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906. https://doi.org/10.3389/fmicb.2016.00906 Jung S, Martinez-Medina A, Lopez-Raez J, Pozo M (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol:1–14. https://doi.org/10.1007/s10886-012-0134-6 Kalosa-Kenyon E, Slaughter LC, Rudgers JA, McCulley RL (2018) Asexual Epichloë endophytes do not consistently alter arbuscular mycorrhizal fungi colonization in three grasses. Am Midl Nat 179:157–165. https://doi.org/10.1674/0003-0031-179.2.157 Kauppinen M, Saikkonen K, Helander M, Pirttilä AM, Wäli PR (2016) Epichloë grass endophytes in sustainable agriculture. Nature Plants 2:15224. https://doi.org/10.1038/nplants.2015.224 Kavroulakis N, Ntougias S, Zervakis GI, Ehaliotis C, Haralampidis K, Papadopoulou KK (2007) Role of ethylene in the protection of tomato plants against soil-borne fungal pathogens conferred by an endophytic Fusarium solani strain. J Exp Bot 58:3853–3864. https://doi.org/10.1093/jxb/ erm230 Kloepper JW, Ryu C-M (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin Heidelberg, pp 33–52. https://doi.org/10.1007/3-540-33526-9_3 Kusari P, Kusari S, Lamshöft M, Sezgin S, Spiteller M, Kayser O (2014) Quorum quenching is an antivirulence strategy employed by endophytic bacteria. Appl Microbiol Biotechnol:1–11. https://doi.org/10.1007/s00253-014-5807-3 Le CN, Kruijt M, Raaijmakers JM (2012) Involvement of phenazines and lipopeptides in interactions between Pseudomonas species and Sclerotium rolfsii, causal agent of stem rot disease on groundnut. J Appl Microbiol 112:390–403. https://doi.org/10.1111/j.1365-2672.2011.05205.x Lindow SE, Brandl MT (2003) Microbiology of the Phyllosphere. Appl Environ Microbiol 69:1875– 1883. https://doi.org/10.1128/aem.69.4.1875-1883.2003 Lugtenberg BJJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92. https://doi.org/10.1093/femsec/fiw194 Maheshwari DK (2013) Bacteria in agrobiology: disease management. Springer Science & Business Media. Springer-Verlag, Berlin, Germany Maheshwari DK (2017) Endophytes: Biology and Biotechnology. Springer, Gewerbestrasse, Switzerland. https://doi.org/10.1007/978-3-319-66541-2 Maheshwari DK, Annapurna K (2017) Endophytes: crop productivity and protection, vol 2. Springer, Gewerbestrasse, Switzerland. https://doi.org/10.1007/978-3-319-66544-3 Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189. https://doi.org/10.3114/sim.53.1.173 Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166. https://doi.org/10.1007/s00248-010-9658-x Marina M et al (2019) Mechanisms of plant protection against two oxalate-producing fungal pathogens by oxalotrophic strains of Stenotrophomonas spp. Plant Mol Biol 100:659–674. https:// doi.org/10.1007/s11103-019-00888-w Marques JM, da Silva TF, Vollu RE, Blank AF, Ding G-C, Seldin L, Smalla K (2014) Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. FEMS Microbiol Ecol 88:424–435. https://doi.org/10.1111/1574-6941.12313 Mathys J et al (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci 3. https://doi.org/ 10.3389/fpls.2012.00108

2 Bioefficacy of Endophytes in the Control of Plant Diseases

31

Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445. https://doi.org/ 10.1146/annurev.phyto.44.013106.145710 Moore JD, Carlisle AE, Nelson JA, McCulley RL (2019) Fungal endophyte infection increases tall fescue’s survival, growth, and flowering in a reconstructed prairie. Restor Ecol 27:1000–1007. https://doi.org/10.1111/rec.12960 Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biology Reviews 26:73–83. https://doi.org/10.1016/ j.fbr.2012.07.001 Mousa WK, Shearer C, Limay-Rios V, Ettinger CL, Eisen JA, Raizada MN (2016) Roothair endophyte stacking in finger millet creates a physicochemical barrier to trap the fungal pathogen Fusarium graminearum. Nature Microbiol 1:16167. https://doi.org/10.1038/nmicro biol.2016.167 Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S (2012) Trichoderma-plant-pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52:522–529. https://doi.org/10.1007/s12088-012-0308-5 Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456. https://doi.org/10.1016/j.pbi.2005.05.007 Narisawa K (2018) The inhibitory role of dark septate endophytic fungus Phialocephala fortinii against Fusarium disease on the Asparagus officinalis growth in organic source conditions. Biol Control 121:159–167. https://doi.org/10.1016/j.biocontrol.2018.02.017 Nassar AH, El-Tarabily KA, Sivasithamparam K (2005) Promotion of plant growth by an auxinproducing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fertil Soils 42:97–108. https://doi.org/10.1007/s00374-005-0008-y Nieva AS et al (2019) The fungal endophyte Fusarium solani provokes differential effects on the fitness of two Lotus species. Plant Physiol Biochem 144:100–109. https://doi.org/10.1016/j.pla phy.2019.09.022 Niu D-D, Wang C-J, Guo Y-H, Jiang C-H, Zhang W-Z, Wang Y-p, Guo J-H (2012) The plant growthpromoting rhizobacterium Bacillus cereus AR156 induces resistance in tomato with induction and priming of defence response. Biocontrol Sci Technol 22:991–1004. https://doi.org/10.1080/ 09583157.2012.706595 Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant-Microbe Interact 24:533–542. https://doi.org/10.1094/MPMI-09-10-0213 Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 409:78–81. https://doi.org/10.1038/35051070 Omacini M, Semmartin M, Pérez LI, Gundel PE (2012) Grass–endophyte symbiosis: a neglected aboveground interaction with multiple belowground consequences. Appl Soil Ecol 61:273–279. https://doi.org/10.1016/j.apsoil.2011.10.012 Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009 Pandey P, Maheshwari DK (2007) Two-species microbial consortium for growth promotion of Cajanus cajan. Curr Sci 92:1137–1142 Petrini O, Sieber TN, Toti L, Viret O (1993) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Toxins 1:185–196. https://doi.org/10.1002/nt.2620010306 Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. https://doi.org/10.1016/j.pbi.2007.05.004 Raaijmakers J, Vlami M, de Souza J (2002) Antibiotic production by bacterial biocontrol agents. Antonie Leeuwenhoek 81:537–547. https://doi.org/10.1023/a:1020501420831 Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. https://doi.org/10.1111/j.1574-6976.2010.00221.x

32

F. M. Romero et al.

Rabbee MF, Ali MS, Baek K-H (2019) Endophyte Bacillus velezensis isolated from Citrus spp. controls streptomycin-resistant Xanthomonas citri subsp. citri that causes citrus bacterial canker. Agronomy 9:470. https://doi.org/10.3390/agronomy9080470 Redman RS, Freeman S, Clifton DR, Morrel J, Brown G, Rodriguez RJ (1999) Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of Colletotrichum magna. Plant Physiol 119:795–804. https://doi.org/10.1104/pp.119.2.795 Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443. https://doi.org/10.1016/j.pbi.2011.04.004 Ren JH, Ye JR, Liu H, Xu XL, Wu XQ (2011) Isolation and characterization of a new Burkholderia pyrrocinia strain JK-SH007 as a potential biocontrol agent. World J Microbiol Biotechnol 27:2203–2215. https://doi.org/10.1007/s11274-011-0686-6 Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. https://doi.org/10.1111/j.1469-8137.2009.02773.x Romero FM, Marina M, Pieckenstain FL (2014) The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS Microbiol Lett 351:187–194. https://doi.org/10.1111/1574-6968.12377 Romero FM, Marina M, Pieckenstain FL (2016) Novel components of leaf bacterial communities of field-grown tomato plants and their potential for plant growth promotion and biocontrol of tomato diseases. Res Microbiol 167:222–233. https://doi.org/10.1016/j.resmic.2015.11.001 Romero FM, Marina M, Pieckenstain FL, Rossi FR, Gonzalez ME, Vignatti P, Gárriz A (2017) Gaining insight into plant responses to beneficial and pathogenic microorganisms using metabolomic and transcriptomic approaches. In: Kalia VC, Saini AK (eds) Metabolic Engineering for Bioactive Compounds: Strategies and Processes. Springer Singapore, Singapore, pp 113–140. https://doi.org/10.1007/978-981-10-5511-9_6 Romero FM, Rossi FR, Gárriz A, Carrasco P, Ruíz OA (2019) A bacterial endophyte from apoplast fluids protects canola plants from different phytopathogens via antibiosis and induction of host resistance. Phytopathology 109:375–383. https://doi.org/10.1094/PHYTO-07-18-0262-R Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19:827–837. https://doi.org/10.1094/MPMI-19-0827 Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. https://doi.org/10.1104/pp. 103.026583 Sahu PK, Singh S, Gupta A, Singh UB, Brahmaprakash GP, Saxena AK (2019) Antagonistic potential of bacterial endophytes and induction of systemic resistance against collar rot pathogen Sclerotium rolfsii in tomato. Biol Control 137:104014. https://doi.org/10.1016/j.biocontrol.2019. 104014 Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte–grass literature. Trends Plant Sci 11:428–433. https://doi.org/10.1016/ j.tplants.2006.07.001 Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9:275–280. https://doi.org/10.1016/j.tplants.2004.04.005 Schilirò E, Ferrara M, Nigro F, Mercado-Blanco J (2012) Genetic responses induced in olive roots upon colonization by the biocontrol endophytic bacterium Pseudomonas fluorescens PICF7. PLoS ONE 7:e48646. https://doi.org/10.1371/journal.pone.0048646 Schulz B, Boyle C, Draeger S, Römmert A-K, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004. https://doi.org/10.1017/ S0953756202006342 Segarra G, Van der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11:90–96. https://doi.org/10.1111/j.1438-8677.2008.00162.x Sheoran N et al (2015) Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemoprofiling of its antimicrobial volatile organic compounds. Microbiol Res 173:66–78. https://doi. org/10.1016/j.micres.2015.02.001

2 Bioefficacy of Endophytes in the Control of Plant Diseases

33

Shukla S, Habbu P, Kulkarni VH, Jagadish K, Pandey A, Sutariya V (2014) Endophytic microbes: a novel source for biologically/pharmacologically active secondary metabolites. Asian Journal of Pharmacology and Toxicology 02:1–16 Su F, Villaume S, Rabenoelina F, Crouzet J, Clément C, Vaillant-Gaveau N, Dhondt-Cordelier S (2017) Different Arabidopsis thaliana photosynthetic and defense responses to hemibiotrophic pathogen induced by local or distal inoculation of Burkholderia phytofirmans. Photosynth Res 134:201–214. https://doi.org/10.1007/s11120-017-0435-2 Suryanarayanan TS (2013) Endophyte research: going beyond isolation and metabolite documentation. Fungal Ecology 6:561–568. https://doi.org/10.1016/j.funeco.2013.09.007 Tian X, Wang D, Mao Z, Pan L, Liao J, Cai Z (2019) Infection of Plasmodiophora brassicae changes the fungal endophyte community of tumourous stem mustard roots as revealed by highthroughput sequencing and culture-dependent methods. PLoS ONE 14:e0214975. https://doi.org/ 10.1371/journal.pone.0214975 Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant-Microbe Interact 18:555–561. https://doi.org/10.1094/MPMI-180555 Tontou R, Gaggia F, Baffoni L, Devescovi G, Venturi V, Giovanardi D, Stefani E (2015) Molecular characterisation of an endophyte showing a strong antagonistic activity against Pseudomonas syringae pv. actinidiae. Plant Soil:1–10. https://doi.org/10.1007/s11104-015-2624-0 Torres MS, Singh AP, Vorsa N, White J (2008) An analysis of ergot alkaloids in the Clavicipitaceae (Hypocreales, Ascomycota) and ecological implications. Symbiosis 46:11–19 van de Mortel JE et al (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160:2173–2188. https://doi.org/ 10.1104/pp.112.207324 Van der Ent S et al (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146:1293–1304 van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. https://doi.org/10.1146/annurev.phyto.36.1.453 van Wees SC, van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448. https://doi.org/10.1016/j.pbi.2008.05.005 Varo A, Raya-Ortega MC, Trapero A (2016) Selection and evaluation of micro-organisms for biocontrol of Verticillium dahliae in olive. J Appl Microbiol 121:767–777. https://doi.org/10. 1111/jam.13199 Verbon EH, Trapet PL, Kruijs S, Temple-Boyer-Dury C, Rouwenhorst TG, Pieterse CMJ (2019) Rhizobacteria-mediated activation of the Fe deficiency response in Arabidopsis roots: impact on Fe status and signaling. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.00909 Verma M, Brar SK, Tyagi RD, Surampalli RY, Valéro JR (2007) Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochem Eng J 37:1–20. https://doi.org/10.1016/j.bej.2007. 05.012 Wang J, Shi L, Wang D, Li L, Loake GJ, Yang X, Jiang J (2019) White rot disease protection and growth promotion of garlic (Allium sativum) by endophytic bacteria. Plant Pathol. https://doi. org/10.1111/ppa.13066 Weller DM et al (2007) Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biol 9:4–20. https://doi.org/10.1055/s-2006-924473 Weller DM, Mavrodi DV, van Pelt JA, Pieterse CMJ, van Loon LC, Bakker PAHM (2012) Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403–412. https://doi.org/10.1094/phyto-08-11-0222 Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511. https://doi.org/10.1093/jexbot/52.suppl_1.487

34

F. M. Romero et al.

Xu W et al (2019) Diversity of cultivable endophytic bacteria in mulberry and their potential for antimicrobial and plant growth-promoting activities. Microbiol Res 229:126328. https://doi.org/ 10.1016/j.micres.2019.126328 Zamioudis C, Hanson J, Pieterse CMJ (2014) β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytol 204:368–379. https://doi.org/10.1111/nph.12980 Zamioudis C et al (2015) Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and irondeficiency responses. Plant J 84:309–322. https://doi.org/10.1111/tpj.12995 Zhang L, Li W, Tao Y, Zhao S, Yao L, Cai Y, Niu Q (2019a) Overexpression of the key virulence factor 1,3–1,4-β-d-glucanase in the endophytic bacterium Bacillus halotolerans Y6 to improve Verticillium resistance in cotton. J Agric Food Chem 67:6828–6836. https://doi.org/10.1021/acs. jafc.9b00728 Zhang P et al (2019b) Screening, identification, and optimization of fermentation conditions of an antagonistic endophyte to wheat head blight. Agronomy 9:476. https://doi.org/10.3390/agrono my9090476 Zhang Q, Zhang J, Yang L, Zhang L, Jiang D, Chen W, Li G (2014) Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biol Control 72:98–108. https://doi.org/10.1016/j.biocon trol.2014.02.018 Zhao J, Shan T, Mou Y, Zhou L (2011) Plant-derived bioactive compounds produced by endophytic fungi. Mini-Rev Med Chem 11:159–168. https://doi.org/10.2174/138955711794519492

Chapter 3

Microbial Endophytes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils Anupma Dahiya, Rakesh Kumar, and Satyavir S. Sindhu

Abstract Phosphorus (P) is the second most essential mineral nutrient after nitrogen for plant growth and development. The available form of P for plants is generally low even in fertile soils throughout the world. Phosphorus deficiency in soil is traditionally overcome by adding the phosphatic fertilizers, which also gets fixed into insoluble unavailable forms due to the high reactivity of soluble P with calcium, iron, or aluminum. The repeatedly applied fertilizer to agricultural fields led to the loss of soil fertility disturbs the soil microbial flora and causes pollution problems. Phosphate solubilizing microbial endophytes have played a significant role in phosphate solubilization. Endophytic microorganisms associated with different parts of the plants release organic acids into the soil, which solubilize the bound form of phosphate complexes and converts them into ortho-phosphate for uptake and utilization by plants. Inoculation of endophytic phosphate solubilizing microorganisms is a reliable technique for increasing soluble P in the soil leading to improved plant biomass and yield of crops. The rhizospheric bioengineering of bacterial strains to enhance phosphate solubilizing capacity will further help in improving the efficacy of biofertilizer inoculants for increasing crop productivity in sustainable agriculture. Thus, the use of plant growth-promoting bacterial endophytes as microbial biofertilizers provides a promising eco-friendly and cost-effective alternative to chemical fertilizers in sustainable agriculture. Keywords Endophytes · Plant colonization · Phosphate solubilization · Plant growth promotion · Biofertilizers

3.1 Introduction In the endophytic growth, microorganisms invade and develop close mutualistic relationships with the plants. They live in cells and tissues, and establish their interaction with different degrees of dependence, surface-sterilized plant tissues. They do not A. Dahiya · R. Kumar · S. S. Sindhu (B) Department of Microbiology, CCS Haryana Agricultural University, Hisar 125 004, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_3

35

36

A. Dahiya et al.

cause any noticeable symptoms to their host plants (Santoyo et al. 2016). These microbes can exist within the aboveground and underground parts of crop plants and even in the seeds, which can be isolated from surface-disinfested plant tissue or extracted from inside the plant (Hallmann et al. 1997; Chebotar et al. 2015). These endophytic microorganisms use the plant endosphere as a unique protective ecological niche that provides a safe and unperturbed environment under fluctuating conditions (Senthilkumar et al. 2011). Most of the endophytic microorganisms possess a biphasic life cycle that alternates between plants and soil environments. Thus, endophytic microorganisms are a specialized group of rhizosphere microbes that have acquired the ability to invade their plant host (Reinhold-Hurek and Hurek 2011). They share all the important traits consistent with the host plant growth promotion of beneficial rhizosphere microbes. Endophytes can communicate and interact with the plant more efficiently than rhizospheric bacteria (Ali et al. 2012; Coutinho et al. 2015). Usually, the plant growth promotion effects observed due to the inoculation of endophytic microbes to host plants are greater than those provided by many rhizospheric microorganisms. These may benefit crop plants directly by enhancing nutrient availability and may improve plant growth by modulating growth-related hormones under normal as well as stressed environmental conditions (Ma et al. 2015). Indirectly, endophytic microbes may improve plant growth by inhibiting the growth of phytopathogens using mechanisms like production of antibiotic, siderophores, lytic enzyme, and by priming plant immunity (Luo et al. 2012; Coutinho et al. 2015; Miliute et al. 2015; Maheshwari et al. 2017). Phosphorus is the second most important nutrient for the growth and development of plants after nitrogen. Plants require approximately 30 μmol l−1 of soil phosphorus for maximum productivity, but its availability is only about 1 μmol l−1 in many soils. Therefore, the unavailability of phosphorus in many soils has been recognized as a major growth-limiting factor in agricultural and horticultural systems (Daniels et al. 2009). On the other hand, the efficiency of applied phosphorus rarely exceeds 30% due to fixation as calcium, iron, or aluminum phosphates in soil (Sharma et al. 2013). Some of the phosphorus is also lost as a result of run-off and leaching (Sashidhar and Podile 2009). Thus, phosphorus deficiency in soil is traditionally overcome by adding either phosphatic fertilizers (Khan et al. 2007) or it may be incorporated as leaf litter, plant residues, or animal remains. The phosphatic fertilizers are the world’s secondlargest bulk chemical used in agriculture on earth (Goldstein 2007). After the addition of chemical phosphatic fertilizers, the extremely reactive soluble phosphate anions (H2 PO4 − , HPO4 2− ) may form metal complexes with Ca in calcareous soils (Lindsay et al. 1989) and Fe3+ and Al3+ in acidic soils (Norrish and Rosser 1983). Thus, a large portion, i.e., 75–90% of added P fertilizer in agricultural soils is precipitated/immobilized rapidly by iron, aluminum, manganese, and calcium complexes depending on soil type, soil pH, and existing minerals (Bünemann et al. 2006; Vu et al. 2008; Miller et al. 2010). Moreover, the phosphatic fertilizers are being prepared from phosphate-containing rocks, which is a non-renewable resource. The current global reserves of rock phosphates may be depleted in the next 50–100 years (Cordell et al. 2009). Therefore, endophytes having phosphate solubilization ability could

3 Microbial Endophytes: Sustainable Approach …

37

provide phosphorus to crops. The inoculation of crops with phosphate solubilizing microbes (PSM) has the potential to reduce the application of phosphatic fertilizer without significantly reducing crop yield (Jilani et al. 2007; Yazdani et al. 2009). Recently, many phosphate solubilizing endophytes have been characterized from different plant tissues to develop effective phosphatic biofertilizers. The inoculation of these endophytes improved P solubilization capacity and resulted in increased plant growth and crop yield.

3.2 Phosphorus Availability in Soil Soil phosphorus exists either in inorganic or organic forms (Richardson 2001). Inorganic phosphorus accounts for 35–70% of total soil P (Sharon et al. 2016) and it occurs mostly in insoluble mineral complexes such as apatite, hydroxyapatite, oxyapatite, mono-, di-, and tricalcium phosphates. The organic compounds making up the humus fraction are derived from surface vegetation, microbial protoplasm, or metabolic products of the microflora. The various inositol phosphates or related substances in the organic matter frequently account for 20–80% of the entire organic P fraction. Most of the organic P sources are phytin, inositol phosphates, phospholipids, nucleic acids, sugar phosphates, polyphosphates, and phosphonates. Phosphorus held within soil microorganisms constitutes a significant component of the total soil P and is estimated to account for around 2–10% of total soil P (Achat et al. 2010). Usually, soils rich in organic matter contain abundant organic P. Moreover, a good correlation exists between the concentrations of organic P, organic C, and total N. Ratios of organic C to organic P of 100–300:1 are common for mineral soils. The soil type, soil use, and management strategies differ considerably for a proportion of different phosphorus fractions (Li et al. 2007). Besides organic P, large quantities of the inorganic forms of P occur in minerals where the phosphate is part of the mineral structure, as insoluble calcium iron or aluminum phosphates (Turan et al. 2006; Vu et al. 2008). Mineral phosphate also found related to the surface of hydrated oxides of Fe and Al, which are inadequately dissolvable and assimilable. Inorganic phosphorus (IP) in acidic soil is associated with Al and Fe compound, though in alkaline soil calcium phosphate is predominant (Khan et al. 2009). According to the compilation of about 9.6 million soil tests for available P in Indian soils, it was reported that 49.3% of areas covering different states and union territories are in a low category, 48.8% in the medium and 1.9% have high category phosphorus status (Hasan 1994). Therefore, the application of phosphatic fertilizers is unavoidable in an intensive farming system. The source of P is only from phosphatic and sulfur rocks, which are non-renewable sources and the use of phosphatic fertilizers leads to the depletion of these resources. Thus, the problem of P management in the soil is also very tricky and more than 70–90% of the applied phosphatic fertilizers get fixed in the soil rendering them unavailable for plant uptake under the ideal conditions (Holford 1997).

38

A. Dahiya et al.

3.3 Colonization of Endophytic Microbes in Tissues The endophytic colonization of plants is a complex process that requires the capacity of microorganisms to compete in the rhizosphere soil and find a niche to communicate and interact with the plant tissues. Endophytic microbes have been isolated and characterized from a diverse type of plant hosts including agronomic crops, prairie plants, plants growing in extreme environments, wild and perennial plants (Zinniel et al. 2002; Nair and Padmavathy 2014; Yuan et al. 2014). Different plant parts including roots, stems, leaves, seeds, fruits, tubers, ovules, and nodules, have the presence of endophytes but the population of endophytes is larger in the roots as compared to above-ground tissues (Rosenblueth and Martínez-Romero 2006; Senthilkumar et al. 2011). Microorganisms residing in the rhizosphere have the potential to enter and colonize the plant roots and this micro-ecosystem has been widely known as one of the primary sources for endophytic colonization (Hallmann et al. 1997). Therefore, organisms in the rhizosphere, either potentially beneficial or pathogenic, are highly competitive in colonizing plant tissues and assimilate nutrients, that possibly affect plant growth and development (Haas and Keel 2003). Endophytes employ different mechanisms to gain entry into the plant tissues (Truyens et al. 2014). They usually enter the plants through the root zone but the aerial parts of the plants, including stems, leaves, flowers, and cotyledons, may also contain endophytic microorganisms (Zinniel et al. 2002). The most common mode of entry of endophytic microbes into plant tissues is through primary and lateral root cracks, and diverse tissue wounds occurring as a result of plant growth (Sprent and de Faria 1998; Sorensen and Sessitsch 2015). The leaves (stomata) and young stems are the other sites through which endophytes may enter (Roos and Hattingh 1983) through lenticels, which are usually present in the periderm of stems and roots (Scott et al. 1996), and by germinating radicles (Gagné et al. 1987) (Fig. 3.1). Bacteria can also enter via the emergence of lateral roots or root hair cells (Huang 1986). Hallmann et al. (1997) demonstrated that entry of the endophytic bacterium Enterobacter asburiae JM22 in cotton plants was assisted by the ability of the bacterium to hydrolyze plant cell wall-bound cellulose. The endophytic colonization of the host plant by the bacteria is determined by various bacterial traits. These traits are collectively referred to as colonization traits. Moreover, endophytic colonization involves a suite of environmental and genetic factors that allow a bacterium to enter the plant endosphere (Compant et al. 2010). The colonization process involves complex communication or signaling between the microbe and the host plant particularly root. It requires recognition of specific compounds in the root exudates by the endophytic bacteria (de Weert et al. 2002; Rosenblueth and Martínez-Romero 2006). Plants produce these root exudates to interact with beneficial bacteria for their ecological advantage (Compant et al. 2005). Once inside the roots, endophytic bacteria can now systemically infect the adjacent plant tissues.

3 Microbial Endophytes: Sustainable Approach …

39

Fig. 3.1 Entry of endophytes into plant tissues and their beneficial characteristics

3.3.1 Rhizosphere and Root Colonization Rhizosphere population can range up to 109 cfu/g of bacteria and 106 cfu/g of fungi (Foster 1988; Benizri et al. 2001). Rhizoplane population ranges from 105 to 107 cfu/g fresh weight and up to 108 bacteria/g are found on leaves (Lindow and Brandel 2003; Bais et al. 2006). The colonization of the host plant root system by the bacteria is not uniform. For example, the distribution and density of Pseudomonas fluorescens strain A6RI varied according to the root zone while colonizing tomato plants (Gamalero et al. 2003). Root colonization is controlled by different factors including root exudation patterns, bacterial attachment and motility, quorum sensing, bacterial growth rate, and minimizing competition by producing antagonistic substances and acquiring nutrients efficiently (Compant et al. 2010). The chemically diverse molecules present in the root exudates are involved in chemotaxis and attract microorganisms to the root, or in the case of endophytes, to be able to colonize the internal plant tissues. The gene expression analysis of Pseudomonas putida KT2440 competently colonizing corn rhizosphere showed that bacterial genes involved in metabolism and oxidative stress were upregulated (Matilla et al. 2007). Moreover, every endophytic microbe has a distinct colonization pattern and colonization site preferences (Zachow et al. 2010). Once these bacteria have established themselves on the root’s surfaces, they penetrate the root interior using specialized mechanisms. Furthermore, another way by which endophytic bacteria avoid being detected as a pathogen by the plant is maintaining low cell densities (2–6

40

A. Dahiya et al.

log cfu) as compared to pathogenic bacteria (7–10 log cfu) (Zinniel et al. 2002). Hence, the endophytic presence of bacteria is determined by genetic determinants that enable bacterial-plant crosstalk, leading to an active endophytic colonization process (Hardoim et al. 2008). The plant host also plays a critical role in selecting an endophytic partner where secretion of specific root exudates and a selective plant defense response are considered important factors in the selection of suitable endophytes (Rosenblueth and Martínez-Romero 2006).

3.3.2 Colonization of Aerial Plant Tissues After entry into the roots, the endophytic bacteria can spread systemically to colonize above-ground tissues. These can establish stem and leaf population densities between 103 and 104 cfu under natural conditions (Compant et al. 2010). The final sink for these specialized endophytic bacteria is leaf tissue wherein they gain entry into the leaves from the phyllosphere via leaf stomata (Senthilkumar et al. 2011).

3.4 Occurrence and Diversity of Bacterial Endophytes The earth planet has been reported to contain about 300,000 species of plants. The endophytes (bacteria and fungi) have been documented in the vast majority of plants that have been analyzed so far (Smith and Read 2008). Partida-Martínez and Heil (2011) stated that an endophyte-free plant is a rare exception and such a plant without endophytes would be more susceptible to phytopathogens and environmental stress conditions (Timmusk et al. 2011). Endophytic bacterial diversity has been reported for several plant species. The population estimates of endophytic bacteria in plants may also vary depending on the type of growth media used for isolation, growth conditions of the host plant, and method used for sterilization of plant tissue (Lodewyckx et al. 2002; Eevers et al. 2015). Moreover, cultivationdependent methods can also strongly underestimate the number of bacteria present in plant tissues (Bogas et al. 2015) because culturable bacteria usually represents only 0.001–1% of the actual endophyte counts (Torsvik and Øvreås 2002; Alain and Querellou 2009). Therefore, culture-independent methods (metagenomics) which mostly rely on the total bacterial genomic DNA extraction from plant tissues, tend to be less biased in analyzing the true endophytic diversity. The emergence of molecular techniques in microbial ecology has validated more comprehensive studies of endophyte abundance, community composition, and function using genetic analysis. A broad-spectrum of endophytic bacteria have been detected from plant tissues by using culture-independent molecular biological techniques, which assess the diversity and composition of uncovering endophytes with obligate host associations such as RFLP analysis and sequencing of rDNA or rRNA. Techniques like fluorescence in situ hybridization (FISH) have also allowed studying the endophytic bacteria in

3 Microbial Endophytes: Sustainable Approach …

41

the natural habitat (Picollo et al. 2010). The application of molecular techniques will continue to enable extensive research on environmental factors that shape endophyte communities (Gaiero et al. 2013). Combinatorial approaches, combining both culture-dependent and culture-independent methods can increase the possibility of complete structural and functional analysis of the endophytic bacterial community of a plant (Sessitsch et al. 2004; Hallmann and Berg 2006). Sessitsch et al. (2012) observed rice’s endorhizosphere using the metagenomics approach and deciphered many traits shared by the endophytic inhabitants that might be crucial in their competence and success. The 16S-rRNA pyrosequencing approach was used in determining the composition of endophytic bacterial communities in tomato leaves (Romero et al. 2001). The endophyte communities were mainly comprised of five phyla, with Proteobacteria as the most highly represented (90%), including the classes α-, β-, and γ-Proteobacteria and later is the most diverse and dominant (Miliute et al. 2015;). Other phyla detected were Actinobacteria (1.5%), Planctomycetes (1.4%), Verrucomicrobia (1.1%), and Acidobacteria (0.5%) (Santoyo et al. 2016). However, a predominance of these phyla can vary with the type of host plant species (Bodenhausen et al. 2013; Ding and Melcher 2016). Among the most commonly isolated endophytes, bacterial genera were Bacillus, Burkholderia, Microbacterium, Micrococcus, Pantoea, Pseudomonas, and Stenotrophomonas, where Bacillus and Pseudomonas are the predominant genera (Hallmann et al. 1997; Romeo et al. 2014; Chaturvedi et al. 2016). Using PCR-based Illumina pyrosequencing, the dynamics of endophytic bacterial communities of sugar beet (Beta vulgaris L.) was analyzed with different plant genotypes and their growth stages (Shi et al. 2014). The greatest numbers of OTUs (Operational Taxonomic Units) were detected during tuber growth and rosette formation, respectively. Interestingly, 43 OTUs were common to all analyzed periods. Proteobacteria was the most abundant division, with 98% of the total microbial endophyte community being composed of Enterobacteriales, Pseudomonadales, Xanthomonadales, Rhizobiales, Sphingomonadales, Burkholderiales, Actinomycetales, and Flavobacteriales. All of them were common inhabitants of the rhizosphere and therefore, suggested that the endophyte microbiome may be a subpopulation of the rhizosphere inhabiting bacteria (Marquez-Santacruz et al. 2010; Germida et al. 1998). The occurrence of Acinetobacter sp. along with Bacillus sp. was reported in the medicinal plant Echinacea (Lata et al. 2018). Bacillus sp. such as B. pumilus, B. subtilis, and B. megaterium were isolated from the roots of medicinal plant Chlorophytum borivilianum (Safed musli) and demonstrated as the major contributors to the endophytic bacterial diversity in medicinal plants (Panchal and Ingle 2011). Apart from medicinal plants, the endophytic occurrence of Acinetobacter and Bacillus species have also been reported in other crops like soybean (Li et al. 2008), sugarcane (Velázquez et al. 2008), the grapevine (Trotel-Aziz et al. 2008), sweet corn, and cotton (McInroy and Kloepper 1995; Joe et al. 2016). Gagne-Bourgue et al. (2013)

42

A. Dahiya et al.

characterized 31 indigenous and culturable bacterial endophytes from three switchgrass leaf cultivars: (Cave-in-Rock, Blue Jacket, and Tecumseh). Bacterial endophytes were identified as Microbacterium testaceum, Curtobacterium flaccumfaciens, Bacillus subtilis, Bacillus pumilus, Pseudomonas fluorescens, Sphingomonas parapaucimobilis, Serratia sp., and Pantoea ananatis. Various positive attributes viz. high biomass production, efficient water use, relatively low demand for nutritional inputs, and less use of agrochemicals were also reported in these endophytes that contributed to the adaptation of switchgrass leaf cultivars to marginal soils (Sanderson et al. 2006). Kang et al. (2018) isolated 30 endophytic and non-endophytic isolates from Medicago sativa. Other plant growth-promoting traits such as phosphate solubilization and production of indole-3-acetic acid (IAA) were also exhibited by most of the tested strains during colonization of plant tissues and soil. Schmidt et al. (2018) isolated endophytes from Miscanthus x giganteus. Genera Pantoea ananatis and Pseudomonas savastanoi exhibited as the predominant bacteria in leaves, whereas other pseudomonads prevailed in roots. Chinnaswamy et al. (2018) isolated Gram-positive, endophytic bacterium B. megaterium NMp082 from root nodules of Medicago polymorpha. The isolate co-inhabited nodules with the symbiotic Ensifer medicae, the nif H and nodD genes in the B. megaterium NMp082 were 100% identical to those of Ensifer meliloti. Although the endophyte possessed nodulation and nitrogen fixation genes, the bacterium failed to form effective nodules. However, it induced nodule-like unorganized structures in alfalfa roots. Many fungi belonging to different groups have also been reported as plant endophytes. The first group includes fungal species with a broad range of host plants, and the second group includes a smaller number of specialized fungal species that colonize some monocotyledonous hosts. Most of the endophytic fungi belong to the phylum Ascomycota and Glomeromycota whereas some fungi belong to phylum Basidiomycota and Zygomycota. The fungi from the genera Acremonium, Alternaria, Chaetomium, Cladosporium, Cryptocline, Cryptosporiopsis, Leptostroma, Phoma, Phomopsis, Phyllosticta, and Trichoderma are well represented in endophyte assemblages. Fungal endophytes within the host may inhabit different tissues of roots, stems, branches, leaves, flowers, fruits, seeds, twigs, bark, and petioles, including xylem of all available plant organs. These endophytes are classified into four classes. Class 1 endophytes form systemic associations with the aboveground tissues of grasses and are defined as the Claviciptaceous endophytes (including Balansia spp. and Epichloe spp.) (Johnson et al. 2013). These species are one of the most economically important examples of plant–endophyte interactions. The diverse class 2 endophytes include both Ascomycota and a few Basidiomycota. Their most exclusive characteristic is the ability to colonize roots, stems, and leaves, and form extensive plant infections. Class 3 comprises endophytes that form highly localized infections in aboveground tissues, such as in the leaves of tropical trees and non-vascular and vascular plants. The dark septate endophytes (DSE) constitute class 4 and these facultative biotrophic fungi colonize plant roots and have the distinguishing feature of having melanized dark septate hyphae (Jumpponen 2001; Rodriguez et al. 2009; Lugtenberg et al. 2016). Fungal endophytes play a major role in habitat adaptation

3 Microbial Endophytes: Sustainable Approach …

43

of plants resulting in improved plant performance and plant protection against biotic and abiotic stresses. Besides, the host plant, environmental factors have been found to strongly influence the endophytic diversity of a particular plant. Moreover, host plant age, genotype, geographical location, and even the tissue being analyzed can determine the type of endophytic bacteria it harbors (Hallmann and Berg 2006). Besides this, host plant growth stages can also determine the endophytic diversity of a plant, where plant stages enriched in nutrient availability tend to have increased bacterial diversity (Shi et al. 2014). Climatic conditions have also been reported to influence the endophytic colonizers of a plant species. Earlier, Penuelas et al. (2012) reported that changes in a climate significantly altered the abundance and composition of endophytic bacteria within the leaf tissues. Different plant species growing in the same soil can have distinctly different endophytic diversity, suggesting that the type of endophytic community of a plant is strongly influenced by the nature of the plant host species (Ding et al. 2013; Ding and Melcher 2016). Germida et al. (1998) reported that canola and wheat plants grown in the same field had a very different spectrum of bacterial species as endophytes. Even the different cultivars of a plant species grown in the same soil can also differ in their endophytic diversity. Graner et al. (2003) reported that four different cultivars of Brassica napus possessed different endophytic bacterial inhabitants. Song et al. (1999) also reported significantly different endophytic bacterial diversity for peanut cultivar grown in different fields. Moreover, Rashid et al. (2012) isolated different types of endophytic bacteria by growing one cultivar of tomato in 15 different agricultural soils. Similarly, Graner et al. (2003) reported that wilt resistant cultivar of Brassica napus contained a higher proportion of endophytic bacteria antagonistic to the wilt-causing Verticillium longisporum than the susceptible cultivar. The restructured endophytic communities of asymptomatic and symptomatic Paullinia cupana plants were observed when challenged by Colletotrichum spp. Bogas et al. (2015), suggested that the presence of phytopathogens in plants is an important factor in the restructuring of endophytic bacterial communities. Hence, the selection of endophytic bacterial communities is a dynamic process that is tightly controlled by the host plant (Berg and Hallmann 2006; Trivedi et al. 2010).

3.5 Phosphorus Solubilization by Endophytic Microorganisms The mechanisms of plant growth promotion employed by endophytic microorganisms are similar to the mechanisms used by rhizospheric bacteria. Endophytic microbes help in the acquisition of nutrients for plant growth and development. The main difference being that endophytic microbes are no longer subject to the vagaries of changing soil conditions, once they have been established within the tissues of the host plant, These changing conditions include variations in temperature, soil pH,

44

A. Dahiya et al.

and water content, and the presence of soil bacteria that may compete for binding sites and nutrients on host plant root surfaces (Glick 2012; Sindhu and Dadarwal 2000). Endophytic bacteria have been shown to impart several beneficial effects on their plant host directly or indirectly. They can benefit plants directly by assisting plants in getting nutrients and improve plant growth by modulating growth-related hormones, which can help plants grow better under normal and stressed conditions (Ma et al. 2016) and indirectly by the improvement of plant growth due to inhabition of phytopathogens (Miliute et al. 2015). Nitrogen, phosphorus, and potassium are usually available in limited quantities for plant growth in agricultural soils. The endophytic bacteria help their host plants in getting increased amounts of limiting plant nutrients (Glick 2012). Endophytic bacteria have been found to contribute toward solubilization of phosphate, potassium, and zinc, and also provide fixed nitrogen and plant growth-promoting substances to the host plants under a wide range of environmental conditions. These bacteria release certain organic acids such as citric acids, oxalic acid, gluconic acid, lactic acid, fumaric acid, etc., which contribute toward solubilization of bound phosphorus in soil. Numerous genera with the ability to solubilize phosphorus and synthesize auxins include Pseudomonas, Bacillus, Rhizobium, Xanthomonas, Serratia, Piriformospora, Burkholderia, Achromobacter, Agrobacterium, Micrococcus, Flavobacterium, Erwinia, Enterobacter, and Paenibacillus (Whitelaw 2000; Fraga et al. 2001; Mota et al. 2008; Ribeiro and Cardoso 2012). Phosphorous is the second most abundant plant nutrient after nitrogen, which is crucial for enzymatic reactions responsible for different plant physiological processes (Sindhu et al. 2014; Ahemad 2015). The majority of the soil phosphorus is insoluble, therefore, it cannot support the plant growth due to its unavailability. Moreover, almost 75% of phosphorus applied as fertilizer forms complexes with iron, aluminum, and calcium in the soil and becomes unavailable for the plants (Ezawa et al. 2002). Phosphorus deficiency causes stunted growth, forms dark leaves, causes inhibition of flowering, and adversely affects the development of the root system. Phosphorus compounds in the soil can be present in bound forms either as: (i) inorganic compounds, (ii) organic compounds of the soil humus, and (iii) organic and inorganic P compounds associated with the cells of living matter. Mineral compounds of P usually contain aluminum (Al), iron (Fe), manganese (Mn), and calcium (Ca) and vary in different kinds of soils. For example, under acidic conditions phosphorus forms a complex with Al, Fe, and Mn, where as it reacts very strongly with Ca in alkaline soils (Khan et al. 2014). Thus, the applied P fertilizers are easily precipitated into insoluble forms, i.e., CaHPO4 , Ca3 (PO4 )2 , FePO4 , and AlPO4− , and are not efficiently taken up by the plants, which lead to an excess application of P fertilizer to achieve maximum plant productivity (Omar 1998). These agricultural practices disrupted natural ecological nutrient cycling, health hazards, environmental disturbance, and damage to biological communities. Many endophytic microorganisms enhance the availability of phosphorus for plants by solubilization of precipitated phosphates (Nautiyal et al. 2000; Zhao et al. 2015; Adhikari and Pandey 2019) (Table 3.1). These microorganisms increase phosphorus availability in the soil either by secreting acid phosphatase that can mineralize

3 Microbial Endophytes: Sustainable Approach …

45

Table 3.1 Phosphorus-solubilizing endophytic microorganisms Species

Microorganisms involved

Bacteria

Bacillus megaterium, B. circulans, B. subtilis, B. polymyxa, B. sircalmous, Pseudomonas striata, Pseudomonas sp., Enterobacter sp., Enterobacter cloacae, Beggiatoa, Thiomargarita sp., Leifsonia xyli, Burkholderia cenocepacia, Burkholderia caribensis, Burkholderia ferrariae, Achromobacter, Acinetobacter, Pantoea agglomerans

Actinobacteria Actinobispora yunnanensis, Actinomodura citrea, Microtetrospora astidiosa, Micromonospora echinospora, Sacchromonospora viridis, Saccharopolyspora hirsute, Streptomyces albus, Streptoverticillium album, Streptomyces cyaneus, Thermonospora mesophila Fungi

Aspergillus awamori, Fomitopsis sp., Penicillium bilaii, Piriformospora indica, dark septate endophytes

Mycorrhiza

Glomus, Funneliformis, Rhizophagus, Sclerocystis, Claroideoglomus, Gigaspora, Scutellospora, Racocetra, Acaulospora, Entrophospora, Pacispora, Diversispora, Otospora, Paraglomus, Geosiphon, Ambispora, Archaeospora sp.

organic phosphorus (Van Der Heijden et al. 2008) or by the release of organic acids that solubilize the bound phosphorus (Fig. 3.2). Moreover, endophytic bacteria can prevent phosphate adsorption and fixation under phosphate limiting conditions by

Fig. 3.2 Different mechanisms employed by microbes for phosphate solubilization

46

A. Dahiya et al.

assimilating solubilized phosphorus (Khan and Joergensen 2009). Thus, endophytic bacteria can act as a sink to provide need-based phosphorus to the plants.

3.5.1 Phosphate Solubilization by Endophytic Bacteria Phosphate solubilization feature is commonly found in endophytic bacteria. About 59–100% of endophytic populations obtained form cactus, strawberry, sunflower, soybean, and other legumes were found to possess the ability to solubilize phosphate (Kuklinsky-Sobral et al. 2004; Forchetti et al. 2007; Dias et al. 2009; Puente et al. 2009a; Palaniappan et al. 2010). The role of phosphate solubilizing endophytic bacteria was established by growing bacteria-free cacti on mineral phosphate supplemented with either endophytes or nutrients, and these plants were compared with plants grown under sterile conditions (Puente et al. 2009b). The growth of inoculated plants without nutrient addition was comparable to the fertilized plants, whereas the bacteria-free unfertilized cacti failed to grow. These results suggested that endophytic bacteria provided the developing plantlets with the limiting nutrient phosphorus. Longback, Gaur (1990) observed a gradual increase of available P and acidity of the medium up to a certain period by Pseudomonas striata, the available P level corresponded with an increase of pH to a certain extent. Many phosphate solubilizing microbes are responsible for the production of organic acids and gluconic acid is known as the principal organic acid for mineral phosphate solubilization.. The highest phosphate solubilization capacity was observed in isolates EB-47 and EB-64 (Bacillus sp. and Bacillus pumilus). The isolate EB-53 (Lysinibacillus sp.) showed high solubilization index, whereas 73% of the isolates showed low solubilization indices. These endophytic bacteria were subsequently used as growthpromoting microbial inoculants in nurseries growing banana suckers (Andrade et al. 2014). Endophytic isolates of P. fluorescens were obtained from the silver grass (Miscanthus giganteus) crop (Oteino et al. 2013). Maximum phosphate solubilization was recorded in P. fluorescens strain L228 and Pseudomonas sp. strain L132 in comparison to negative control E. coli JM109. All strains showed the production of gibberellic acid (GA) with a concentration ranging from 2840 to 33240 ± 230 mg L−1 (14–169 mM). Kumar et al. (2013) isolated root endophytes from nodules of legume plants. Large numbers of Gram-positive bacterial endophytes were present in legume nodules than in its roots, which showed 56 and 47.8% phosphate solubilizing ability, respectively. From legume roots, 56.9% isolates showed phosphate solubilizing activity, whereas only 35.9% showed from non-legume roots. Moreover, the highest numbers of phosphate solubilizing isolates (73.3%) were observed from field pea roots and the lowest numbers of phosphate solubilizing isolates (20%) were observed in oat roots. The amount of P solubilization was higher in isolates from chickpea than oat roots. The significant phosphate solubilizing bacterial isolates were obtained from legume roots and nodules (CRE1 and CNE215) and non-legume roots (WRE10, WRE20, and

3 Microbial Endophytes: Sustainable Approach …

47

ORE35). Isolate ORE35 was the most potential P solubilizers among all these endophytic isolates. Three promising isolates were identified by 16S rRNA sequencing for instance from chickpea nodules B. subtilis strain CNE215; whereas roots have B. licheniformis strain CRE1; in case of wheat root B. flexus strain WRE 20. B. methylotrophicus strain CKAM was selected from the root endosphere of healthy apple trees based on higher P-solubilization (687 mg/L) and other plant growth-promoting attributes (Mehta et al. 2014). Five rhizospheric and two root endophytic actinobacteria were isolated from wheat plants (Jog et al. 2014). Maximum phosphate solubilizing activity in tricalcium phosphate supplemented medium was exhibited by actinobacterial isolate Streptomyces mhcr 0816. Zhao et al. (2015) isolated 48 endophytic bacteria from surface-sterilized tissues of the medicinal plant Lonicera japonica wherein few isolates showed a zone of phosphate solubilization on the Pikovskaya agar medium. These bacterial strains were identified as Paenibacillus and Bacillus strains. Pandya et al. (2015) isolated 26 non-rhizobial and one fungal endophyte from Vigna radiata root nodules and only 11 endophytes solubilized phosphate. Maximum phosphorus solubilization was observed in Paenibacillus xylanilyticus strain M15 (134.483 μg ml−1 ). The free phosphate release ranged from 37.4 μg ml−1 in strain M13 to 134.48 μg ml−1 in the strain M15. However, free phosphate released by strain M15 was significantly lower than free phosphate released by the endophyte B. cereus strain P31 (354.3 μg ml−1 ) isolated from potato roots (Dawwam et al. 2013). The most efficient phosphate solubilizing strains belong to species of Klebsiella (M13), Dyadobacter, Blastobacter, Bacillus, and Paenibacillus spp. Bacterial endophytes were also isolated and characterized from the root and shoot tissues of Lavandula dentate plants growing under organic management (Pereira et al. 2016). These were identified as Pseudomonas brassicacearum subsp. neoaurantiaca, Pseudomonas moorei, Variovorax soli, Pseudomonas frederiksbergensis, Pseudomonas fuscovaginae, B. cereus, Bacillus aerophilus, Bacillus drentensis, Pseudomonas graminis, Bacillus aryabhattai, and Pseudomonas lutea. The higher bacterial diversity of endophytes was observed in roots having to six different genera (Pseudomonas, Variovorax, Rhizobium, Caulobacter, Bacillus, and Paenibacillus), while in shoots, 91% of the endophytic isolates were characterized and identified as Bacillus and Pseudomonas, whereas only one belongs to genus Xanthomonas. Matos et al. (2017) isolated 40 endophytic bacterial isolates from banana tree roots. Approximately 67.5% of the isolates solubilized phosphorus from soy lecithin. Acid phosphatase activity was detected in 65% of the isolates and Aneurinibacillus sp. and Lysinibacillus sp. isolates showed the best solubilization indexes. Bacillus sp. isolate EB78 exhibited P solubilization capacity in solid media when Ca3 (PO4 )2 and soy lecithin were used as P sources. This isolate significantly reduced the pH of the liquid medium and exhibited acid phosphatase activity. The salt-tolerant endophytic and phosphate solubilizing bacterial isolates Acinetobacter sp. ACMS25 and Bacillus sp. PVMX4 was isolated from Phyllanthus amarus (Govindasamy et al. 2018). These isolates showed a higher zone of clearance and solubilization index when compared with standard B. megaterium strain MTCC446 in the presence of 160 mM NaCl (Chen et al. 2006; Tao et al. 2008; Verma et al. 2013).

48

A. Dahiya et al.

Kshetri et al. (2018) isolated Arthrobacter luteolus S4C7, Enterobacter asburiae S5C7, Klebsiella pneumoniae S4C9, S4C10, and S6C1, and K. quasipneumoniae S6C2 from the rhizosphere of Allium hookeri. All the isolates released a substantial amount of soluble phosphate.

3.5.2 Phosphate Solubilization by Endophytic Fungi Several rhizospheric fungi such as arbuscular mycorrhizal (AM) fungi support plant mineral nutrition in exchange for photosynthetic carbon and colonize the root zone (Smith and Read 2008). The root endophytic fungus Piriformospora indica, which is an anamorphic strain of the Sebacinales (Basidiomycota) was isolated from the Thar Desert of India (Verma et al. 1998). P. indica can colonize roots and promote plant growth independent of phosphate concentrations in the soil (Yadav et al. 2010). Nath et al. (2012) isolated P-solubilizing endophytic Penicillium species from tea leaves which showed significant phosphate solubilizing activity with an increase of acidity of the medium. The decrease in the pH of the medium was associated with an increased amount of available P in the medium. Dark septate endophytes (DSE) are root colonizing soil fungi, which establish a wide range of symbiotic interactions with the host plants. Occurrence of these fungi has been associated with more than 600 plant species, including non-mycorrhizal plants (Mandyam and Jumpponen 2005; Sieber and Grünig 2006). They can grow in both biotrophic and saprophytic ways, hence have different effects on their hosts (Mandyam et al. 2012). Barrow and Osuna (2002) showed that Aspergillus ustus (DSE strain) can solubilize soil phosphate and increase P availability to Atriplex canescens (Hernandez et al. 2011; Rinu and Pandey 2010). Bashan et al. (2013) isolated DSE fungi from wheat (T. aestivum) and two forages (Panicum coloratum and Chloris gayana) which solubilized calcium, aluminum, and iron phosphates, in vitro methodologies. Rinu et al. (2013) reported that the carbon and nitrogen sources can influence the phosphate solubilizing efficiency of the fungi. Comparatively, the efficiency of the strain of Ophiosphaerella sp. was found similar to that of the filamentous fungus Paecilomyces lilacinus. Spagnoletti et al. (2017) isolated dark septate endophytes from the roots of wheat (Triticum aestivum) and forage crops Panicum coloratum and Chloris gayana, grown in slightly acidic and alkaline soils of Argentina. The isolates showed the ability to solubilize calcium phosphate, three strains solubilized aluminum phosphate, and none of them solubilized iron phosphate on solid media. Maximum calcium phosphate solubilization was carried out by Ophiosphaerella sp., Cochliobolus sp., and Setosphaeria rostrata. Endophytic strains Drechslera sp. and Ophiosphaerella herpotricha showed maximum aluminum phosphate solubilization. Priyadharsini and Muthukumar (2017) isolated Curvularia geniculata, a dark septate endophytic fungus from Parthenium hysterophorus L. to solubilize different sources of phosphorus.

3 Microbial Endophytes: Sustainable Approach …

49

Recently, Adhikari and Pandey (2019) isolated endophytic fungi of genera Penicillium and Aspergillus from the roots of Taxus wallichiana. The endophytes solubilized phosphate by utilizing the substrates, namely, calcium, aluminum, and iron phosphate along with the production of phosphatase and phytase enzymes. Maximum phosphate solubilization and phytase activity were recorded in P. daleae, which produced maximum calcium phytase. The phosphatase activity was higher in acidic conditions in comparison to alkaline conditions due to release of different organic acids.

3.6 Beneficial Traits of Endophytic Microorganisms Some of the phosphate solubilizing endophytes have also been found to possess other beneficial traits, i.e., nitrogen fixation, hormone production, growth inhibition of phytopathogenic fungi, stress amelioration by reduction of ethylene concentration by the production of ACC deaminase, and solubilization of metals in the soil.

3.6.1 Nitrogen Fixation by Endophytes The endophytic bacteria of the genera Gluconacetobacter diazotrophicus, Herbaspirillum seropedicae, H. rubrisubalbicans, Azotobacter, Beijeinckia, Methylobacterium, and Azospirillum showed nitrogen fixation capacity in different cultures with nonleguminous plants and have been used as a prominent alternative of nitrogen fertilizers (Cavalcante et al. 2007). Endophytic bacteria increase the nitrogen availability for their host plants. These bacteria can supply fixed atmospheric nitrogen to their host plants by expressing nitrogenase activity (Montanez et al. 2012). Nitrogenfixing bacteria like Azoarcus sp. BH72, Azospirillum brasilense, Burkholderia spp., Gluconacetobacter diazotrophicus, and Herbaspirillum seropedicae have also been reported to increase the host plant biomass by N2 fixation under controlled conditions (Bhattacharjee et al. 2008). Strains of G. diazotrophicus have been identified living in symbiosis with sugarcane and pine plants (Carrell and Frank 2014). Shabanamol et al. (2018) obtained nitrogen-fixing endophytic diazotrophic isolates from surface-sterilized leaf, stem, and root samples of various rice cultivars using Dobereiner’s semisolid N free bromothymol blue media. Associative nitrogen-fixing endophytes perform better than rhizosphere microorganisms in enabling plants to thrive in nitrogen-limited soil environments and promoted plant health and growth (Hurek and Reinhold-Hurek 2003). Nitrogen-fixing endophyte Paenibacillus strain P22 has been found in a poplar tree, and have been demonstrated to contribute to the total nitrogen pool of the host plant (Scherling et al. 2009). Gupta et al. (2013) reported that endophytic nitrogen-fixing bacteria may also enhance the rate of nitrogen fixation and accumulation in plants residing in nitrogen-limited soils but these are not as efficient as root nodule associated Rhizobium in nitrogen fixation ability.

50

A. Dahiya et al.

3.6.2 Phytohormone Mehta et al. (2014) obtained endophytic P-solubilizing rhizobacteria from 20 healthy apple roots and found that endophyte B. methylotrophicus CKAM obtained from root endosphere showed the higher phosphate solubilization (on PVK agar plates in vitro). B. methylotrophicus also showed nitrogenase activity, IAA, siderophore, and antifungal activity against F. oxysporum, Phytophthora sp., D. necatrix, S. rolfsii, and P. aphanidermatum. Pirhadi et al. (2018) isolated bacterial endophytes from roots, stems, and leaves of sugarcane grown in saline and non-saline soil. The authors observed a prevalence of Bacillaceae, with Bacillus sp. being the most frequently isolated bacterium and salinity affected the bacterial community structure and higher diversity of root entophytic P-solubilizing bacteria. Earlier, Kruasuwan and Thamchaipenet (2016) reported that bacterial endophytes isolated from sugarcane rhizosphere exhibited plant growth-promoting traits especially indole-3acetic acid, nitrogen fixation, ACC deaminase, phosphate solubilization, siderophore production, etc. Shabanamol et al. (2018) observed that three diazotrophic isolates inhibited the growth of rice sheath blight pathogen Rhizoctonia solani, also produced indole-3-acetic acid, gibberellic acid, and cytokinins. Ribeiro et al. (2018) reported that Bacillus strains produced high levels of IAA in the presence of tryptophan. Sun et al. (2019) observed that the production of indole acetic acid significantly enhanced root biomass and root–shoot ratio on medicinal plant Astragalus mongholicus.

3.6.3 Endophytic Microbes as a Biocontrol Agent A few endopytic microorganisms also act as potential biocontrol agents. An endophytic bacteria Pantoea vagans C9-1 was commercialized as a bacterial biocontrol agent for fire blight (Smits et al. 2011). Aravind et al. (2009) reported for suppression of phyto-parasitic burrowing nematode (Radopholus similis Thorne) by endophytic bacteria Bacillus megaterium BP17 and Curtobacterium luteum TC10. Similar to B. thuringiensis, endophytic bacteria active against plant pests have also been demonstrated, where genetically modified endophytic P. fluorescens expressing Bacillus thuringiensis toxin and Serratia marcescens chitinase effectively targeted Eldana saccharina (sugarcane borer) larvae (Downing et al. 2000). Niu et al. (2011) showed that B. cereus AR156 triggered both the SA and JA/ET signaling pathways in Arabidopsis to induce ISR, which led to an additive effect of plant protection. Earlier, similar to the above studies, Conn et al. (2008) indicated that A. thaliana plants inoculated with endophytic actinobacteria showed upregulation of both defense pathways, thereby protecting against subsequent infection by phytopathogenic bacteria E. carotovora and fungus F. oxysporum. However, the primed defense pathways differed for the two pathogen types. The resistance to E. carotovora involved JA/ET pathway, while resistance toward F. oxysporum was mainly followed the SA pathway. It is

3 Microbial Endophytes: Sustainable Approach …

51

interesting to note that the same bacterium was able to prime two different pathways to confer resistance to the different pathogens (Conn et al. 2008). Mehta et al. (2014) reported that phosphate solubilizing endophytic bacteria showed maximum antagonistic effect against S. rolfsii followed by F. oxysporum, D. necatrix, P. aphanidermatum, and Phytophthora sp. by producing various antifungal compounds such chitinase, proteases, pectinase, and the antibiotic lipopeptides surfactin, fengycin, and iturin A. Shabanamol et al. (2018) reported that three diazotrophic isolates, showed in vitro antifungal activities against rice sheath blight pathogen R. solani. All the isolates produced IAA, GA, and cytokinins. Morphological, physiological, biochemical characteristics, and 16S rDNA sequence analysis identified the isolates as Lysinibacillus sphaericus, Klebsiella pneumonia, and Bacillus cereus. Endophytic bacteria Pseudomonas stutzeri strain E25 and Stenotrophomonas maltophilia strain CR71 produced volatile compound dimethyl disulfide, which exhibited significant antifungal activity against Botrytis cinerea (Rojas-Solis et al. 2018). Recently, Manganyi et al. (2019) determined the antimicrobial metabolites produced by endophytic fungi Sceletium tortuosum L. The endophytic fungi produced secondary metabolites that displayed a narrow spectrum of activity against the bacterial strains. None of the fungal extracts inhibited the growth of Enterococcus faecalis (ATCC S1299) and Enterococcus gallinarum (ATCC 700425) while Bacillus cereus (ATCC 10876) was the most susceptible agent against the fungal extracts. In general, Fusarium oxysporum (GG 008) displayed significance because it was linked to high levels of 5-hydroxymethylfurfural (HMF) and octadecanoic acid as revealed by GC-MS.

3.6.4 Endophytes in ACC Deaminase and Stress Amelioration As a consequence of the presence of an ACC deaminase-containing organisms, a plant that has been exposed to either biotic or abiotic stress conditions may be partially or even completely protected from the ethylene inhibition of plant growth (Glick 2014). Thus, ACC deaminase-containing microbes effectively protect against growth inhibition by flooding, high salt, drought, against fungal and bacterial pathogens, nematode damage, the presence of high levels of metals and organic contaminants, as well as low-temperature stress condition (Khandelwal and Sindhu 2012; Glick 2015). Involvement of ACC deaminase in endophytic plant growth promotion was reported in Burkholderia phytofirmans PsJN (Sessitsch et al. 2005). The mutants of this bacterium lacking ACC deaminase activity were no longer able to promote canola seedling root elongation (Sun et al. 2009). Besides, two of these ACC deaminaseproducing endophytic PGPB (compared to ACC deaminase minus mutants of the same strains) have also been tested for the ability to promote tomato plant growth in the presence of very high levels of salt and to delay the senescence of mini carnation cut flowers (Ali et al. 2012). ACC deaminase-producing endophytic PGPB were

52

A. Dahiya et al.

readily taken up through the stems of cut flowers, subsequently delaying flower senescence by several days (Ali et al. 2012). The endophytic bacterium B. megaterium NMp082 isolated from root nodules of Medicago polymorpha reported to exhibit ACC deaminase activity in vitro and its inoculation promoted growth in M. polymorpha, Medicago lupulina, Medicago truncatula, and Medicago sativa. B. megaterium NMp082 also induced tolerance to salt stress in alfalfa and Arabidopsis plants (Chinnaswamy et al. 2018).

3.6.5 Metals Solubilization by Endophytes Soil contamination with heavy metals due to anthropogenic activities such as mining, combustion of fossil fuel, agrochemicals, and sewage sludge has become one of the most severe environmental hazards throughout the world. Interactions between plants and beneficial microorganisms have received much attention worldwide for the bioremediation and phytoremediation of polluted sites as a cleaning technology for removing metals from soils. Pereira and Castro (2014) isolated distinctive microbial communities from woody tree species to herbaceous crop plants, which showed predominant existence in all higher plants (Luo et al. 2011) and able to colonize different plant compartments such as roots, stem, leaves, flowers as well as fruits and seeds (Compant et al. 2011; Sun et al. 2010). These endophytes may act as bioinoculants in the recovery of metal contaminated soils, constituting a biological alternative to improve phytoremediation efficiency. Several bacterial endophytes were isolated from the Zn/Cd hyperaccumulator plant Sedum plumbizincicola (Ma et al. 2015; Ullah et al. 2015). On the other hand, the effect of the rhizobial endosymbiont Sinorhizobium meliloti strain CCNWSX0020 under copper stress was recently evaluated (Kong et al. 2015). This strain increased both plant growth and nitrogen content. Besides, the rhizobial symbiosis promoted Cu accumulation in plant shoots and roots. Also, several plant genes involved in antioxidant responses were upregulated in plants treated with the bacterium in the presence of high levels of Cu. Thus, the symbiosis with S. meliloti not only enhanced plant growth and metal uptake but also induced the plant’s antioxidative defense responses under Cu stress. Verma et al. (2014) isolated endophytic bacteria Delftia and Micrococcus from wheat and six percent isolates showed the highest potassium (K) solubilization, i.e., some other bacterial genera such as Stenotrophomonas maltophilia and IARI-IIWP27 Pseudomonas monteilii also showed significant K-solubilization. Wagh et al. (2016) found that two endophytic microorganisms Hs (pJNK5) and Hs (pJNK6) of species H. seropedicae that showed K-solubilization on Aleksandrov agar plates.

3 Microbial Endophytes: Sustainable Approach …

53

3.7 Inoculation Responses of Endophytes on Plants Numerous reports exist regarding the application of endophytic bacteria in the growth promotion of wheat, rice, canola, potato, tomato, etc. (Mei and Flinn 2010; Sturz and Nowak 2000) (Table 3.2). Most of the studies involve the growth promotion potential of the endophytes isolated from the same plants or the plants which are very closely related to their natural host (Long et al. 2008). However, some endophytic bacteria have been reported to cause growth promotion on non-host or diverse host plants (Sessitsch et al. 2005; Ma et al. 2011), indicating contrasting observations about the host specificity of endophytes. The broad-host-range of endophytes makes a powerful tool in agriculture biotechnology and, therefore, endophytes have a great potential to be used as biofertilizers and biopesticides in sustainable agrobiological practices. Our understanding of endophyte communities and the ability to predict the success of endophytes to promote plant growth under field conditions is limited. Various soil, plant, and microbial factors have been reported to affect the survival, colonization, and compatibility of the endophyte to survive within the root. Moreover, the plant growth-promoting ability of endophytic microbes can be influenced by the genotype of the plant host. Bacterial genotype has been found to strongly influence the growth-promoting effects on host plants. Trognitz et al. (2008) demonstrated that different strains of B. phytofirmans differed markedly in their abilities to promote the growth of the same potato cultivar. Few decades back, Dong et al. (1994) reported that four strains of endophytic Salmonella enterica colonized alfalfa roots and hypocotyl differently. Hence, plant colonization and growth promotion by the endophytic bacteria are controlled by the genetic factors of both partners. Long et al. (2008) observed that PGP bacteria of Solanum nigrum proved highly host-specific, where these bacteria were unable to produce growth enhancement in Nicotiana attenuate, a non-host plant. However, the broad-host-range of endophytic bacteria has been demonstrated in the case of B. phytofirmans PsJN, isolated from onion roots (Pillay and Nowak 1997), which can promote the growth of A. thaliana, grape, maize, potato, switchgrass, tomato, and wheat (Sessitsch et al. 2005; SheibaniTezerji et al. 2015). Also, Thomas and Upreti (2014) demonstrated that endophytic bacterial isolates of crop plants could inhibit wilt pathogen Ralstonia solanacearum and also suppressed the disease effects of Ralstonia solanacearum on a non-host tomato plant. Moreover, endophytic bacteria from tomato grown in different agricultural soils, were able to promote canola growth under gnotobiotic conditions (Rashid et al. 2012). Afzal et al. (2015) showed that endophytic bacteria selectively isolated from Cannabis sativa rhizosphere induced growth promotion of canola. Thus, these reports suggested that endophytic bacteria have a broad-host-range potential in plant growth and development. Earlier, Wu and Guo (2008) observed that inoculation of Saussurea involucrata with a DSE fungus promoted plant growth and especially plant height similar in case of DSE inoculation in pigeon pea. Fakhro et al. (2010) inoculated tomato with Penicillium indica and observed the colonization of tomato roots by P. indica. The inoculation resulted in increased biomass of the leaves up to 20% and also reduced the

Source Root exudates Leaves

Root, stem, and leaf

Stems and roots Roots and stems Stems and fruits

Twigs and leaves Roots, stem, and leaves

Roots, stems, and leaves

Endophytic species

Azorhizobium caulinodans, Azospirillum brasilense and Serratia spp.

Bacillus, Methylobacterium, Delftia, Stenotrophomonas, Microbacterium, Paenibacillus and Staphylococcus

Bacillus and Paenibacillus

Bacillus pumilus, B. subtilis, Pseudomonas aeruginosa and P. fluorescens

Serratia sp., S. marcescens, Klebsiella sp., K. variicola and Stenotrophomonas sp.

Pseudomonas sp. and Brevibacillus brevis

Bacillus sp. and Pantoea sp.

B. cereus, B. licheniformis, Bacillus sp, Burkholderia gladioli, Paracoccus halophilus, and Stenotrophomonas sp.

Enterobacter ludwigii, Pantoea agglomerans, and Variovorax paradoxus

Table 3.2 Inoculation effect of endophytic bacteria on different hosts

Isolates showed IAA production, phosphate solubilization and plant growth promotion in soybean

Endophytes promoted plant growth and 50–64% enhanced biomass accumulation of tomato

Enhanced seedling growth in rice

Production of phytohormones, antifungal activity, chromium tolerance, phosphate solubilization, and PGPR activity in tomato

Plant growth promotion in rice

Effect on population densities in maize

Deformity of fungal mycelia, IAA and siderophore production, ACC utilization, phosphate solubilization, increase in shoot length, root length, fresh weight, dry weight, and chlorophyll content in wheat seedlings

Biological control of plant diseases and plant growth promotion in common bean

ACC deaminase production, stress reduction, and increased root growth in wheat and rice

Effect on plant

(continued)

de Almeida Lopes et al. (2016)

Xia et al. (2015)

Deivanai et al. (2014)

Patel et al. (2012)

Mbai et al. (2015)

Rai et al. (2007)

Zhao et al. (2015)

Costa et al. (2012)

Hardoim et al. (2008)

References

54 A. Dahiya et al.

Source Seed

Rhizome tissues

Roots

Endophytic species

Flavobacterium sp., Pseudomonas sp., Microbacterium sp., and Xanthomonas sp.

Serratia, Enterobacter, Acinetobacter, Pseudomonas, Stenotrophomonas, Agrobacterium, Ochrobactrum, Bacillus and Tetrathiobacter

Enterobacter and Pseudomonas

Table 3.2 (continued)

Mn tolerance, antifungal activity, ammonia and IAA production in chickpea

IAA production, N, P, and K uptake, plant height, leaf area, and biomass yield in maize

High tolerance to salinity and osmotic stress, hormone modulation, nitrogen fixation, siderophore production, and phosphate solubilization in rice

Effect on plant

Brígido et al. (2019)

Zhang et al. (2018)

Walitang et al. (2017)

References

3 Microbial Endophytes: Sustainable Approach … 55

56

A. Dahiya et al.

disease severity caused by Verticillium dahliae by more than 30%. In hydroponics, P. indica increased fresh fruit biomass of tomato, the numbers of fruits, and the dry matter content. Uninoculated Pisum sativum plants treated with the soluble phosphate (positive control) produced the highest quantity of biomass (total weight, root weight, and shoot weight) in comparison to uninoculated control plants grown in sand containing insoluble phosphate (Oteino et al. 2013). Thus, inoculation with bacterial strain L132 showed the highest whole plant dry weight, enhanced plant growth, increased root, and shoot dry weight as compared to uninoculated treatments. This suggested that these strains solubilize the insoluble phosphate compound by release of gluconic acid present in the sand medium resulting in plant growth promotion as compared to E. coli JM109 strain (negative control). Increased plant growth and phosphate uptake have been reported in many crop species as a result of the inoculation of PSB Pseudomonas sp. particularly in rice (Gusain et al. 2015), soybean (Fankem et al. 2015), and wheat (Babana and Antoun 2006). Demissie et al. (2013) stated that the inoculation of fababean (Vicia faba L.) with phosphate solubilizing Pseudomonas and Rhizobium isolates resulted in enhanced plant growth under soluble phosphate limiting conditions as compared to uninoculated plants. Inoculation with PSB to the plants produced gluconic acid in the rhizosphere, resulted in the release of soluble phosphate, which was subsequently assimilated by the plant. However, these endophytic bacteria are also known to express other plant growth promotion traits such as IAA production and ACC deaminase activity, which may also have contributed to the enhanced growth of the inoculated plants (Otieno et al. 2015). Inoculation of the phosphate solubilizing endophytic isolate CKAM showed a remarkable increase in seed germination, shoot length and root length, shoot dry weight, and root dry weight of tomato under net house condition (Mehta et al. 2014). When the endophytic isolate CKAM was inoculated/co-inoculated with E. adhaerens (native rhizobia) to V. radiata, it significantly increased root length, shoot length, a number of lateral roots and plant dry weight of mungbean plants in a small field trial (Pandya et al. 2015). Endophytic bacterial strains isolated from the medicinal plant Lonicera japonica showed growth-promoting activities in wheat (Zhao et al. 2015). The inoculation of phosphate solubilizing endophytic fungi C. geniculata significantly promoted the growth of pigeon pea without expressing any pathogenic symptoms (Priyadharsini and Muthukumar 2017). Similarly, co-inoculation of endophytic diazotrophs and actinobacteria, i.e., Bacillus, Enterobacter, Microbispora, and Streptomyces significantly increased the growth parameters of sugarcane plants as compared to individual inoculation and uninoculated plants (Kruasuwan and Thamchaipenet 2016). Nitrogen-fixing endophytic bacteria P. stutzeri A15 from the rhizosphere of rice stimulated its growth (Pham et al. 2017). The endophytic bacterial strains isolated from rice seeds, i.e., Micrococcus yunnanensis RWL-2, Micrococcus luteus RWL-3, Enterobacter soli strain RWL-4, Leclercia adecarboxylata RWL5, Pantoea dispersa RWL-6, and Staphylococcus epidermidis RWL-7 produced a significant amount of IAA and such bacterial inoculation increased shoot and root length, fresh and dry biomass, and chlorophyll content of rice plants significantly (Shahzad et al. 2017). Inoculation of P. stutzeri strain E25 and Stenotrophomonas

3 Microbial Endophytes: Sustainable Approach …

57

maltophilia strain CR71, which produced antifungal volatile compound dimethyl disulfide, promoted the shoot and root length, chlorophyll content, and total fresh weight of tomato plants (Lycopersicon esculentum cv Saladette) and their coinoculation further improved the plant growth-promoting effect (Rojas-Solis et al. 2018). Schmidt et al. (2018) reported that several endophytes including pseudomonads, Variovorax paradoxus, Verticillium leptobactrum, Halenospora sp., and Exophiala sp. enhanced growth of Miscanthus giganteus in gamma-sterilized soil in pot experiments. Moreover, co-inoculation of bacteria or fungi originating from Miscanthus promoted the growth of their host, especially on the heavy metals-polluted site. Similarly, inoculation of endophytic bacterium B. megaterium NMp082 isolated from root nodules of Medicago polymorpha promoted plant growth of Medicago lupulina, Medicago truncatula, and Medicago sativa. The co-inoculation of B. megaterium NMp082 with E. medicae further enhanced the growth and nodulation of Medicago spp. plants compared with inoculation with either bacterium alone (Chinnaswamy et al. 2018). Intrestingly, B. megaterium NMp082 also induced tolerance to salt stress in alfalfa and Arabidopsis plants due to salt stress alleviation effects. Pirhadi et al. (2018) reported that inoculation of bacterial endophyte Pseudomonas sp. SugS_49 isolated from sugarcane grown in saline soils showed more phosphorus dissolution ability and its inoculation increased the growth, grain yield, and phosphorus uptake of wheat. During the same year, Ribeiro and his colleagues reported that inoculation of Fe-P solubilizing endophytic Bacillus strains, produced high levels of IAA in the presence of tryptophan, enhanced the shoot and root dry weight, and the NPK content in plants cultivated in soil with no P fertilization (Ribeiro et al. 2018). Specifically, Bacillus strain B1923 enhanced shoot and root dry weight and root NP content of plants cultivated with no P added and Bacillus strains B2084 and B2088 showed positive performance on biomass production and accumulation of NPK in the shoot. Similarly, Kshetri et al. (2018) also reported that treatment with PSB obtained from the rhizosphere of Allium hookeri, resulted in enhanced growth of A. hookeri Thwaites. K. quasipneumoniae strain S6C2 increased root length and weight in TCP amended soil and increased available P in soil. Heydari et al. (2019) reported that under P deficiency, the dry root weight of barley significantly decreased the total root length with a decrease of root diameter under pot experiments. The results suggested that the root structure and root extension are directly and indirectly affected by soil fertility and especially P nutrient of the soil, which further determines plant growth and crop production. Sun et al. (2019) explored the beneficial effects of IAA-producing endophytic Pseudomonas poae strain S61 on medicinal plant Astragalus mongholicus. The combination trial also increased calycosin-7-O-glucoside and ononin accumulations in the roots, suggesting that the strain executed beneficial effects on A. mongholicus only when it grew under drought stress.

58

A. Dahiya et al.

3.8 The Genetics Involved in Endophytic Behavior and Phosphate Solubilization The genomic analysis could help to understand the mechanisms involved in decisionmaking regarding the influence of bacteria to act as endophyte because the capacity to penetrate and survive inside plant tissues are multifactorial. Moreover, rhizospheric bacteria colonize tissues inside plants, so that both lifestyles share a variety of mechanisms. In addition to testing of individual biochemical/genetic mechanisms involved in the interaction of a bacterial endophyte with a plant, it is possible to use a bioinformatics approach to predict some of the key features that distinguish endophyte from rhizospheric PGPB (Ali et al. 2014). The genomic DNA sequences of rhizospheric and endophytic PGPB (both Burkholderia spp.) were compared and the genes encoded by the rhizospheric strain were subtracted from the endophytic strain. Then, the remaining, putative endophytic genes, were compared with the complete genomes of eight different endophytic PGPB (B. phytofirmans PsJN, Burkholderia spp. strain JK006, A. lipoferum 4B, E. cloacae ENHKU01, K. pneumoniae 342, P. putida W619, Enterobacter spp. 638, Azoarcus spp. BH72, and S. proteamaculans 568). Genes that were common to all of these strains were considered to be potentially involved in endophytic behavior, including genes encoding transporter proteins, secretion and delivery systems, plant polymer degradation or modification, transcriptional regulation, detoxification, redox potential maintenance, unknown functions, and functions like 2-isopropylmalate synthase and diaminopimelate decarboxylase. Most of the (~40) genes identified by this procedure encode functions previously suggested by separate biochemical/genetic studies involved in endophytic behavior. Most of the genetic studies have been carried out on B. phytofirmans strain PsJN, a model endophytic bacterium, with the ability to competently colonize (both rhizosphere and endosphere) and promote the growth of a variety of different plant hosts, including A. thaliana, grape, maize, potato, switchgrass, tomato, and wheat (Sessitsch et al. 2005; Sheibani-Tezerji et al. 2015). Moreover, strain PsJN also increases tolerance of host plants to abiotic stress such as chilling and drought (Barka et al. 2006, Naveed et al. 2014), and biotic stress like inhibition of fungal phytopathogens (Sharma and Nowak 1998; Barka et al. 2006). Strain PsJN has been shown to require IAA degradation, ACC deaminase, and quorum sensing to colonize host plants and produce beneficial effects (Sun et al. 2009; Zuniga et al. 2013). Moreover, in planta gene expression profiling revealed that, during its growth inside host plants, the bacterium expresses several different traits related to cellular homeostasis, cell redox homeostasis, energy production, general metabolism (amino acids, lipids, nucleotides, sugars), and transcription regulation (Sheibani-Tezerji et al. 2015). The nitrogen-fixing endophyte Azocarus sp. was reported to infect plants through the emergence points of lateral roots and root tips via the action of bacterial endoglucanase (Rheinhold-Hurek et al. 2006). Also, transposon mutants lacking the activity of this endoglucanase colonized rice plants to a significantly lesser extent. This group subsequently showed that deletion mutants of the pilT and pilA genes in this

3 Microbial Endophytes: Sustainable Approach …

59

bacterium abolished bacterial twitching and motility as well as the endophytic colonization of the roots of rice plants (Bohm et al. 2007), where pilT and pilA genes encode the pilus retraction protein and the pilin structural protein, respectively. On the other hand, the colonization of host plants by bacterial endophytes, showed that the gumD gene from the nitrogen-fixing endophyte G. diazotrophicus, involved in exopolysaccharide biosynthesis, is required for biofilm formation and subsequent root colonization (Meneses et al. 2011). It was later demonstrated the significance of endophyte colonization in rice plants of the gor and sod genes, a glutathione reductase, and a superoxide dismutase, analyzed in the N2 -fixing strain G. diazotrophicus (Alquéres et al. 2013). A series of DNA cytosine methylation changes were observed as a consequence of plant inoculation with the endophytic PGPB B. phytofirmans PsJN (Da et al. 2012). In this study, 30 plant proteins (thought to be involved in growth and signaling) and their methylation status was significantly altered (increased or decreased) and identified following interaction with the bacterium. When the effect of the endophytic PGPB G. diazotrophicus on sugarcane plants was assessed, using the proteomics approach of the more than 400 proteins that were analyzed, 78 were differentially expressed in the presence of the bacterium (Lery et al. 2011). To improve phosphate-dissolving capacity by PGPB strains, genetic transfer of any isolated gene involved in mineral phosphate solubilization (MPS) is an interesting approach. An attempt was made to improve MPS in PGPR strains, using a PQQ synthase gene from E. herbicola (Rodriguez et al. 2001). This gene was subcloned in a broad-host-range vector pKT230 and the recombinant plasmid was expressed in E. coli and subsequently transferred to PGPR strains of B. cepacia and P. aeruginosa. Several of the ex-conjugants that were recovered in the selection medium showed a larger clearing halo in medium with tricalcium phosphate as the sole P source. This indicated the heterologous expression of this gene in the recombinant strains and gave rise to improved MPS ability in these PGPRs. However, expression of the mineral phosphate solubilizing (mps) genes in a different host may also be influenced by the genetic background of the recipient strain, the copy number of the indigenous plasmids, and metabolic interactions. Mineral P solubilization involves the synthesis of gluconic acid, which is produced from glucose involving glucose dehydrogenase (GDH) enzyme (Goldstein and Liu 1987). The cofactor pyrroloquinoline quinone (PQQ) is required for GDH activity (Goldstein 1995). In pqq operon, pqqA, pqqB, pqqC, pqqD, and pqqE genes are conserved and arranged in an orderly manner, whereas, pqqF and pqqG are located either proximal or distal to the pqq operon (Shen et al. 2012). Moreover, a twocomponent regulatory system, consisting of a DNA-binding transcriptional regulator (PhoB) and transmembrane histidine kinase (PhoR) involved in regulation and secretion of various enzymes such as alkaline phosphatases, acid phosphatases, phytases, and phosphodiesterase in response to inorganic phosphate (Pi) scarcity (Santos-Beneit 2015). The alkaline phosphatase enzyme (encoded by gene phoA) of E. coli was fully induced when the Pi concentration was reduced from 100 mM to 0.16 mM (Lopez-Bucio et al. 2003), suggesting that a regulatory element called as Pi transport operon and the sensor-activator operon, both are involved in this mechanism. The genes controlled by Pi and activated by PhoB constituted the PHO

60

A. Dahiya et al.

regulon (Sashidhar and Podile 2009). The overexpression of phosphate uptake ABC transporter permease protein (PhoT) and the phosphate uptake ABC transporter ATP binding protein (phoC) in S. meliloti was found to enhance phosphate solubilization and yield in Medicago (Carmen and Roberto 2010).

3.9 Conclusion Plant beneficial endophytic microbes have great potential to act as biofertilizers and biopesticides for growth enhancement and protection from plant disease, respectively. Many bacterial endophytes can solubilize phosphorus, potassium, metals, and other toxic substances by producing various organic acids and enzymes. Moreover, the complex interactions in the rhizosphere and endophytic PSB with, other microorganisms, plant, and the environment-influenced solubilization of bound phosphates, Pi uptake, and plant growth promotion. Under field conditions, plant genotypes have been found as an important determinant in the development of a positive plantendophyte association. Majority of them containing endophytes tend to survive the harshness of the environment and challenge biotic and abiotic stresses. Altough, inconsistency in the performance of these inoculant strains is a major constraint to the widespread use of microbial inoculants in commercial agriculture (Rodriguez et al. 2006). It is, therefore, identification of the rare and promising bacterial endophytes with general plant beneficial characteristics would require a combination of culture-dependent and culture-independent techniques. With a further understanding of the functioning of bacterial endophytes, in the future scientists may be able to engineer bacterial endophytes to facilitate their potential to improve plant growth and development (Miller et al. 2010). The knowledge generated on biodiversity and genetic manipulation of P solubilizing endophytic bacteria thus require to design strategies for their efficient potential for sustainable and organic agriculture. This includes ecological consideration of single/group of microbial communities, their interactions in the rhizosphere or within roots (endophytes), their ability to mobilize P from different soil fractions, and farm management practices that influence these processes. More problems are yet to be resolved so as to utilize them in product development of biotechnological significance. The manipulation of bacterial traits with improved efficiency of P solubilization in endophytic bacteria and their inoculation as phosphatic biofertilizers may boost plant growth leading to improved soil health and crop productivity.

References Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240

3 Microbial Endophytes: Sustainable Approach …

61

Adhikari P, Pandey A (2019) Phosphate solubilization potential of endophytic fungi isolated from Taxus wallichiana Zucc. roots. Rhizosphere 9:2–9 Afzal I, Iqrar I, Shinwari ZK, Yasmin A (2017) Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. Plant Growth Regul 81(3):399–408 Afzal I, Zabta KS, Irum I (2015) Selective isolation and characterization of agriculturally beneficial endophytic bacteria from wild hemp using canola. Pak J Bot 47(5):1999–2008 Ahemad M (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. 3 Biotech 5:111–121 Ahemad M, Khan M (2012) Biotoxic impact of fungicides on plant growth promoting activities of phosphate-solubilizing Klebsiella sp. isolated from mustard (Brassica campestris) rhizosphere. J Pest Sci 85:29–36 Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13:583–594 Ali S, Charles TC, Glick BR (2012) Delay of flower senescence by bacterial endophytes expressing 1-aminocyclopropane-1-carboxylate deaminase. J Appl Microbiol 113(5):1139–1144 Ali S, Duan J, Charles TC, Glick BR (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198 Alquéres S, Meneses C, Rouws L, Rothballer M, Baldani I, Schmid M, Hartmann A (2013) The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol Plant-Microbe Interact 26:937–945 Andrade LF, de Souza GLOD, Nietsche S, Xavier AA, Costa MR, Cardoso AMS, Pereira DFGS (2014) Analysis of the abilities of endophytic bacteria associated with banana tree roots to promote plant growth. J Microbiol 52(1):27–34 Andrade-Linares DR, Müller A, Fakhro A, Schwarz D, Franken P (2013) Impact of Piriformospora indica on tomato. In: Varma A et al (eds) Piriformospora indica. Soil Biology 33. Springer-Verlag, Berlin, pp 107–117 Andreazza R, Okeke BC, Lambais MR, Bortolon L, de Melo GWB, de Oliveira CFA (2010) Bacterial stimulation of copper phytoaccumulation by bioaugmentation with rhizosphere bacteria. Chemosphere 81:1149–1154 Andreolli M, Zapparoli G, Angelini E, Lucchetta G, Lampis S, Vallini G (2019) Pseudomonas protegens MP12: a plant growth-promoting endophytic bacterium with broad-spectrum antifungal activity against grapevine phytopathogens. Microbiol Res 219:123–131 Aravind R, Kumar A, Eapen S, Ramana K (2009) Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identification and evaluation against Phytophthora capsici. Lett Appl Microbiol 48:58–64 Babana A, Antoun H (2006) Effect of Tilemsi phosphate rock- solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L.) in Mali. Plant Soil 287:51–58 Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266 Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–592 Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252 Barrow JR, Osuna P (2002) Phosphorus solubilization and uptake by dark septate fungi in four wing saltbush, Atriplex canescens (Pursh) Nutt J Arid Environ 51: 449–459 Bashan Y, Holguin G (1995) Root-to-root travel of the beneficial bacterium Azospirillum brasilense. Appl Environ Microbiol 60:2120–2131 Bashan Y, Kamnev AA, Bashan L (2013) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479

62

A. Dahiya et al.

Benizri E, Baudoin E, Guckert A (2001) Root colonization by inoculated plant growth promoting rhizobacteria. Biocontrol Sci Technol 11:557–574 Berg G, Hallmann J (2006) Control of plant pathogenic fungi with bacterial endophytes. Springer, In Microbial root endophytes, pp 53–69 Bhattacharjee RB, Singh A, Mukhopadhyay S (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209 Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8(2):e56329 Bogas AC, Ferreira AJ, Araújo WL, Astolfi-Filho S, Kitajima EW, Lacava PT, Azevedo JL (2015) Endophytic bacterial diversity in the phyllosphere of Amazon Paullinia cupana associated with asymptomatic and symptomatic anthracnose. SpringerPlus 4:258 Bohm M, Hurek T, Rheinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2 -fixing endophyte Azocarus sp. strain BH72. Mol Plant-Microbe Interact 20:526–533 Bonafante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383 Brígido C, Singh S, Menéndez E, Tavares MJ, Glick BR, Félix MD, Oliveira S, Carvalho M (2019) Diversity and functionality of culturable endophytic bacterial communities in chickpea plants. Plants 8(2):42–49 Bünemann EK, Heenan DP, Marschner P, McNeill AM (2006) Long term effects of crop rotation, stubble management and tillage on soil phosphorus dynamics. Aust J Soil Res 44:611–618 Carmen B, Roberto D (2010) Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl Environ Microbiol 76:4626–4632 Carrell AA, Frank AC (2014) Pinus flexilis and Picea engelmannii share a simple and consistent needle endophyte microbiota with a potential role in nitrogen fixation. Front Microbiol 5:333 Cavalcante JJV, Vargas C, Nogueira EM, Vinagre F, Schwarcz K, Baldani JI, Hemerly AS (2007) Members of the ethylene signalling pathway are regulated in sugarcane during the association with nitrogen-fixing endophytic bacteria. J Exp Bot 58:673–686 Chagas Junior AF, Oliveira LA, Oliveira AN, Willerding AL (2010) Phosphate solubilizing ability and symbiotic efficiency of isolated rhizobia from Amazonian soils. Acta Sci 32:359–366 Chanway C, Shishido M, Nairn J, Jungwirth S, Markham J, Xiao G, Holl F (2000) Endophytic colonization and field responses of hybrid spruce seedlings after inoculation with plant growthpromoting rhizobacteria. For Ecol Manage 133:81–88 Chaturvedi H, Singh V, Gupta G (2016) Potential of bacterial endophytes as plant growth promoting factors. J Plant Pathol Microbiol 7:2–14 Chebotar V, Malfanova N, Shcherbakov A, Ahtemova G, Borisov AY, Lugtenberg B, Tikhonovich I (2015) Endophytic bacteria in microbial preparations that improve plant development. Appl Biochem Microbiol 51:271–277 Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33– 41 Chinnaswamy A, Coba de la Pena T, Stoll A, de la Pena RD, Bravo J, Rincon A, Lucas MM, Pueyo JJ (2018) A nodule endophytic Bacillus megaterium strain isolated from Medicago polymorpha enhances growth, promotes nodulation by Ensifer medicae and alleviates salt stress in alfalfa plants. Ann Appl Biol 172:295–308 Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678 Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microbial Ecol 62(1):188–197

3 Microbial Endophytes: Sustainable Approach …

63

Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693 Conn VM, Walker A, Franco C (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant-Microbe Interact 21:208–218 Coombs JT, Franco CM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69(9):5603–5608 Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Change 19:292–305 Costa LE, Queiroz MV, Borges AC, Moraes CA, Araujo EF (2012) Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris). Brazilian J Microbiol 43(4):1562–1575 Coutinho BG, Licastro D, Mendonca-Previato L, Camara M, Venturi V (2015) Plant-influenced gene expression in the rice endophyte Burkholderia kururiensis M130. Mol Plant-Microbe Interact 28(1):10–21 Da K, Nowak J, Flinn B (2012) Potato cytosine methylation and gene expression changes induced by a beneficial bacterial endophyte, Burkholderia phytofirmans PsJN. Plant Physiol Biochem 50:24–34 Daniels C, Michan C, Ramos JL (2009) New molecular tools for enhancing methane production, explaining thermodynamically limited lifestyles and other important biotechnological issues. Microbiol Biotechnol 2:533–536 Dawwam GE, Elbeltagy A, Emara HM, Abbas IH, Hassan MM (2013) Beneficial effect of plant growth promoting bacteria isolated from the roots of potato plant. Ann Agric Sci 58(2):195–201 de Almeida Lopes KB, Carpentieri-Pipolo V, Oro TH, Stefani Pagliosa E, Degrassi G (2016) Culturable endophytic bacterial communities associated with field-grown soybean. J Appl Microbiol 120(3):740–755 de Weert S, Vermeiren H, Mulders IH, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant-Microbe Interact 15:1173–1180 Deivanai S, Bindusara AS, Prabhakaran G, Bhore SJ (2014) Culturable bacterial endophytes isolated from mangrove tree (Rhizophora apiculata Blume) enhance seedling growth in rice. J Natur Sci Biol Med 5(2):437 Demba Diallo M, Reinhold-Hurek B, Hurek T (2008) Evaluation of PCR primers for universal nif H gene targeting and for assessment of transcribed nif H pools in roots of Oryza longistaminata with and without low nitrogen input. FEMS Microbiol Ecol 65:220–228 Demissie S, Muleta D, Berecha G (2013) Effect of phosphate solubilizing bacteria on seed germination and seedling growth of faba bean (Vicia faba L.). Intern J Agric Res 8:123–136 Dias AC, Costa FE, Andreote FD, Lacava PT, Teixeira MA, Assumpção LC, Araújo WL, Azevedo JL, Melo IS (2009) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195 Ding T, Melcher U (2016) Influences of plant species, season and location on leaf endophytic bacterial communities of non-cultivated plants. PLoS ONE 11:e0150895 Ding T, Palmer MW, Melcher U (2013) Community terminal restriction fragment length polymorphisms reveal insights into the diversity and dynamics of leaf endophytic bacteria. BMC Microbiol 13:1 Dong Z, Canny MJ, McCully ME, Roboredo MR, Cabadilla CF, Ortega E, Rodes R (1994) A nitrogen-fixing endophyte of sugarcane stems (a new role for the apoplast). Plant Physiol 105:1139–1147 Downing KJ, Leslie G, Thomson JA (2000) Biocontrol of the sugarcane borer Eldana saccharina by expression of the Bacillus thuringiensis cry1Ac7 and Serratia marcescens chiA genes in sugarcane-associated bacteria. Appl Environ Microbiol 66:2804–2810

64

A. Dahiya et al.

Duvauchelle D (2009) Plant fact sheet for hopbush (Dodonaea viscose (L) J acq). USDA-National Resources Conservation Service Hawaii Plant Materials Center, Hoolehua 96729 Eaglesham ARJ (1989) Global importance of Rhizobium as an inoculant. In: Microbial inoculation of crop plants, Chapter 3 (Campbell R and Macdonald R eds.). Oxford University Press, Oxford Eevers N, Gielen M, Sánchez- López A, Jaspers S, White J, Vangronsveld J, Weyens N (2015) Optimization of isolation and cultivation of bacterial endophytes through addition of plant extract to nutrient media. Microbiol Biotechnol 8:707–715 Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221– 230 Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R, Schwarz D, Franken P (2010) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20(3):191–200 Fankem H, Nwaga D, Deubel A, Dieng L, Merbach W, Etoa FX (2006) Occurrence and functioning of phosphate solubilizing microorganisms from oil palm tree (Elaeis guineensis) rhizosphere in Cameroon. Afr J Biotechnol 5:2450–2460 Fankem HT, Chakounte GVT, Ngonkot L, Mafokoua HL, Dondjou DT, Simo C (2015) Common bean (Phaseolus vulgaris L.) and soybean (Glycine max) growth and nodulation as influenced by rock phosphate solubilizing bacteria under pot grown conditions. Int J Agric Policy Res 5:242–250 Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152 Foster RC (1988) Microenvironments of soil microorganisms. Biol Fertil Soils 6:189–203. https:// doi.org/10.1007/BF00260816 Fraga R, Rodriguez H, Gonzalez T (2001) Transfer of the gene encoding the NapA acid phosphatase of Morganella morganii to a Burkholderia cepacia strain. Acta Biotechnol 21(4):359–369 Franken F (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464 Gagné S, Richard C, Rouseau H, Antoun H (1987) Xylem-residing bacteria in alfalfa roots. Can J Microbiol 33:996–1000 Gagne-Bourgue F, Aliferis KA, Seguin P, Rani M, Samson R, Jabaji S (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol 114(3):836–853 Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: Bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750 Gamalero E, Lingua G, Berta G, Lemanceau P (2003) Methods for studying root colonization by introduced beneficial bacteria. Agron J 23:407–418 Gardner JM, Feldman AW, Zablotowicz RM (1982) Identity and behavior of xylem-residing bacteria in rough lemon roots of Florida citrus trees. Appl Environ Microbiol 43:1335–1342 Gaur AC (1990) Phosphate solubilizing microorganisms as biofertilizers. In: Gaur AC (eds), Omega Scientific Publishers. New Delhi, pp 16–72 Germida JJ, Siciliano SD, Renato de Freitas J, Seib AM (1998) Diversity of root associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26:43–50 Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374 Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica. http:// sci-hub.tw/10.6064/2012/963401 Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39 Glick BR (2015) Beneficial plant-bacterial interactions. Springer, Heidelberg, pp 123–157. https:// doi.org/10.1007/978-3-319-13921-0 Goldstein AH (1995) Recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by Gram-negative bacteria. Biol Agric Hortic 12:185–193

3 Microbial Endophytes: Sustainable Approach …

65

Goldstein AH (2007) Future trends in research on microbial phosphate solubilization: one hundred years of insolubility. In: Velazquez E, Roderguez-Barrueco C (eds) Proc First International Meeting on Microbial Phosphate Solubilization. Springer-Verlag, Berlin, pp 91–96 Goldstein AH, Liu ST (1987) Molecular cloning and regulation of a mineral phosphate solubilizing gene from Erwinia herbicola. Biotechnology 5:72–74 Govindasamy V, George P, Raina SK, Kumar M, Rane J, Annapurna K. (2018) Plant-associated microbial interactions in the soil environment: role of endophytes in imparting abiotic stress tolerance to crops. In: Advances in Crop Environment Interaction (pp. 245–284). Springer, Singapore Graner G, Persson P, Meijer J, Alstrom S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224:269–276 Grossmann K (2010) Auxin herbicides: current status of mechanism and mode of action. Pest Manag Sci 66:113–120 Gupta G, Panwar J, Jha PN (2013) Natural occurrence of Pseudomonas aeruginosa, a dominant cultivable diazotrophic endophytic bacterium colonizing Pennisetum glaucum (L.) R. Br. Appl Soil Ecol 64:252–261 Gusain YS, Kamal R, Mehta CM, Singh US, Sharma AK (2015) Phosphate solubilizing and indole3-acetic acid producing bacteria from the soil of Garhwal Himalaya aimed to improve the growth of rice. J Environ Biol 36:307 Hallmann J, Berg G (2006) Spectrum and population dynamics of bacterial root endophytes. Springer, In Microbial root endophytes, pp 15–31 Hallmann J, Quadt-Hallmann A, Mahaffee W, Kloepper J (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914 Hansen M, Kragelund L, Nybroe O, Sørensen J (1997) Early colonization of barley roots by Pseudomonas fluorescens studied by immunofluorescence technique and confocal laser scanning microscopy. FEMS Microbiol Ecol 23:353–360 Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471 Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Ann Rev Phytopathol 41(1):117–153 Hasan R (1994) Phosphorus fertility status of soils in India. Phosphorus research in India. In: Dev G (ed) Proceedings of Group Discussion, Indian Agricultural Research Institute, New Delhi. Principal Publications, Gurgaon, pp 8–12 Huang JS (1986) Ultrastructure of bacterial penetration in plants. Ann Rev Phytopathol 24:141–157 Hernandez T, Carrion G, Heredia G (2011) Solubilizacion in vitro de fosfatos por una cepa de Paecilomyces lilacinus (Thom) Samson. Agrociencia 45:881–892 Heydari MM, Brook RM, Jones DL (2019) The role of phosphorus sources on root diameter, root length and root dry matter of barley (Hordeum vulgare L.). J Plant Nutr 42(1):1–5 Hilda R, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339 Holford ICR (1997) Soil phosphorus: its measurement and its uptake by plants. Aust J Soil Res 35:227–239 Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178 Ivleva NB, Groat J, Staub JM, Stephens M (2016) Expression of active subunit of nitrogenase via integration into plant organelle genome. PLoS ONE 11:e0160951 Jilani G, Akram A, Ali RM, Hafeez FY, Shams IH, Chaudhry AN (2007) Enhancing crop growth, nutrients availability, economics and beneficial rhizosphere microflora through organic and biofertilizers. Ann Microbiol 57:177–183 Joe MM, Devaraj S, Benson A, Sa T (2016) Isolation of phosphate solubilizing endophytic bacteria from Phyllanthus amarus Schum & Thonn: Evaluation of plant growth promotion and antioxidant activity under salt stress. J Appl Res Med Aromat Plants 3(2):71–77

66

A. Dahiya et al.

Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160(4):778–788 Johnson LJ, de Bonth AC, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA (2013) The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers 60(1):171–188 Jumpponen A (2001) Dark septate endophytes - are they mycorrhizal? Mycorrhiza 11(4):207–211 Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic rootcolonizing fungi. New Phytol 140:295–310 Kang W, Shi S, Xu L (2018) Diversity and symbiotic divergence of endophytic and non-endophytic rhizobia of Medicago sativa. Ann Microbiol 68:247–260. https://doi.org/10.1007/s13213-0181333-3 Khan AA, Jilani G, Akhtar MS, Naqvi SMS, Rasheed M (2009) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J Agric Biol Sci 1:48–58 Khan KS, Joergensen RG (2009) Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresour Technol 100:303–309 Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Phosphate solubilizing microorganisms (pp. 31–62). Springer, Cham Khan MS, Zaidi A, Wani PA (2007) Role of phosphate solubilizing microorganisms in sustainable agriculture-a review. Agron Sustain Dev 27:29–43 Khandelwal A, Sindhu SS (2012) Expression of 1-aminocyclopropane-1-carboxylate deaminase in rhizobia promotes nodulation and plant growth of clusterbean (Cyamopsis tetragonoloba L.). Res J Microbiol 7:158–170 Kim J, Rees DC (1994) Nitrogenase and biological nitrogen fixation. Biochemistry 33:389–397 Kim S, Lowman S, Hou G, Nowak J, Flinn B, Mei C (2012) Growth promotion and colonization of switchgrass (Panicum virgatum) cv. Alamo by bacterial endophyte Burkholderia phytofirmans strain PsJN. Biotechnol Biofuels 5:37–45 Knauth S, Hurek T, Brar D, Reinhold-Hurek B (2005) Influence of different Oryza cultivars on expression of nif H gene pools in roots of rice. Environ Microbiol 7:1725–1733 Kong Z, Mohamad OA, Deng Z, Liu X, Glick BR, Wei G (2015) Rhizobial symbiosis effect on the growth, metal uptake, and antioxidant responses of Medicago lupulina under copper stress. Environ Sci Pollut Res 22:12479–12489 Kouas S, Labidi N, Debez A, Abdelly C (2005) Effect of P on nodule formation and N fixation in bean. Agron Sustain Dev 25(3):389–393 Kruasuwan W, Thamchaipenet A (2016) Diversity of culturable plant growth-promoting bacterial endophytes associated with sugarcane roots and their effect of growth by co-inoculation of diazotrophs and actinomycetes. J Plant Growth Regul 35(4):1074–1087 Kshetri L, Pandey P, Sharma GD (2018) Rhizosphere mediated nutrient management in Allium hookeri Thwaites by using phosphate solubilizing rhizobacteria and tricalcium phosphate amended soil. Journal of Plant Interactions 13(1):256–269 Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean- associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251 Kumar V, Pathak DV, Dudeja SS, Saini R, Giri R, Narula S, Anand RC (2013) Legume nodule endophytes more diverse than endophytes from roots of legumes or non legumes in soils of Haryana. Indian J Microbiol Biotech Res 3(3):83–92 Lata R, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66(4):268–276 Lee JC, Kim CJ, Yoon KH (2011) Paenibacillus telluris sp. nov., a novel phosphate solubilizing bacterium isolated from soil. J Microbiol 49:617–621 Lehr P (2010) Biopesticides: the Global Market, Report code CHM029B, BCC Research

3 Microbial Endophytes: Sustainable Approach …

67

Lery LMS, Hemerly AS, Nogueira EM, von Krüger WMA, Bisch PM (2011) Quantitative proteomic analysis of the interaction between the endophytic plant-growth-promoting bacterium Glucanoacetobacter diazotrophicus and sugarcane. Mol Plant Microbe Interact 24:562–676 Li JH, Wang ET, Chen WF, Chen WX (2008) Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biol Biochem 40:238–246 Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natn Acad Sci USA 104:11192–11196 Lindow SE, Brandel MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883. https://doi.org/10.1128/AEM.69.4.1875-1883.2003 Lindsay WLP, Vlek LG, Chien SH (1989) Phosphate minerals. In: Dixon JB, Weed SB (eds) Minerals in soil environment, 2nd edn. Soil Science Society of America, Madison, USA, pp 1089–1130 Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, der Lelie DV (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606 Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE 3:e2702 Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287 Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556 Lugtenberg BJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92(12):fiw194. https://doi.org/10.1093/femsec/fiw194 Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90 Luo S, Chen L, J-l C, Xiao X, Xu T, Wan Y, Rao C, Liu C, Liu Y, Lai C, Zeng G (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd hyper accumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138 Luo S, Xu T, Chen L, Chen J, Rao C, Xiao X, Wan Y, Zeng G, Long F, Liu C, Liu Y (2012) Endophyteassisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. Appl Microbiol Biotechnol 93:1745–1753 Lynch JM (1983) Soil Biotechnology. Blackwell Scientific Publications, Oxford, UK Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyper accumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manage 156:62–69 Ma Y, Prasad M, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258 Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manage 174:14–25 Maheshwari DK, Dheeman S, Annapurna K (2017) Endophytes as contender of plant productivity and protection: an introduction. In: Maheshwari D, Annapurna K (eds) Endophytes: crop productivity and protection. Sustainable development and biodiversity, Vol 16. Springer, Cham. pp 1–9. https://doi.org/10.1007/978-3-319-66544-3_1 Malik DK, Sindhu SS (2011) Production of indole acetic acid by Pseudomonas sp.: effect of coinoculation with Mesorhizobium sp. Cicer on nodulation and plant growth of chickpea (Cicer arietinum). Physiol Mol Biol Plants 17:25–32 Mandyam K, Fox C, Jumpponen A (2012) Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie. Mycorrhiza 22:109–119

68

A. Dahiya et al.

Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root- colonising dark septate endophytic fungi. Stud Mycol 53:173–189 Manganyi MC, Coutlyne M, Regnier T, Tchatchouang C-D K, Bezuidenhout CC, Ateba CN (2019) Antibacterial activity of endophytic fungi isolated from Sceletium tortuosum L. (Kougoed). Ann Microbiol 69(6):659–663 Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS ONE 7:e48479 María SO, María ES, María MR et al (2013) Toxigenic profile and AFLP variability of Alternaria alternata and Alternaria infectoria occurring on wheat. Braz J Microbiol 44:447–455 Marquez-Santacruz HA, Hernandez-Leon R, Orozco-Mosqueda MC, Velazquez-Sepulveda I, Santoyo G (2010) Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Gen Mol Res 9:2372–2380 Matilla MA, Espinosa-Urgel M, Rodríguez-Herva JJ, Ramos JL, Ramos-González MI (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol 8:R179 Matos AD, Gomes IC, Nietsche S, Xavier AA, Gomes WS, Dos Santos Neto JA, Pereira MC (2017) Phosphate solubilization by endophytic bacteria isolated from banana trees. An Acad Bras Ciênc 89(4):2945–2954 Mbai FN, Magiri EN, Matiru VN, Nganga J, Nyambati VCS (2015) Isolation and characterization of bacterial root endophytes with potential to enhance plant growth from Kenyan Basmati rice. Amer Intern J Contem Res 3(4):25–40 McInroy JA, Kloepper JW (1995) Population dynamics of endophytic bacteria infield-grown sweet corn and cotton. Can J Microbiol 41(10):895–901 Meena KK, Mesapogu S, Kumar M, Yandigeri MS, Singh G, Saxena AK (2010) Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol Fertil Soils 46(2):169–174 Mehta P, Walia A, Kakkar N, Shirkot CK (2014) Tricalcium phosphate solubilisation by new endophyte Bacillus methylotrophicus CKAM isolated from apple root endosphere and its plant growth-promoting activities. Acta Physiol Plantarum 36(8):2033–2045 Mei C, Flinn BS (2010) The use of beneficial endophytes for plant biomass and stress tolerance improvement. Recent Pat Biotechnol 4:81–95 Meneses CHSG, Rouws LFM, Simões-Araújo V, Idal MS, Baldani JI (2011) Exopolysaccharide production is required for biofilm formation and plant colonization by the nitrogen-fixing endophyte Gluconacetobacter diazotrophicus. Mol Plant Microbe Interact 24:1448–1458 Miliute I, Buzaite O, Baniulis D, Stanys V (2015) Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agriculture 102(4):465–478 Miller SH, Browne P, Prigent-Cambare C, Combes-Meynet E, Morrissey JP, O’Gara F (2010) Biochemical and genomic comparison of inorganic phosphate solubilisation in Pseudomonas species. Environ Microbiol Rep 2:403–411 Montanez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28 Mortvedt JJ (1996) Heavy metal contaminants in inorganic and organic fertilizers. Fert Res 43:55–61 Mota FF, Gomes EA, Seldin L (2008) Auxin production and detection of the gene coding for the auxin efflux carrier (AEC) protein in Paenibacillus polimyxa. J Microbiol 46:257–264 Nadarajan R, Brodie EL, Lynch SV (2015) Use of 16S rRNA gene for identification of a broad range of clinically relevant bacterial pathogens. PLoS ONE 10:e0117617 Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J Naseem M, Dandekar T (2012) The role of auxin-cytokinin antagonism in plant-pathogen interactions. PLoS Pathog 8(11):e1003026

3 Microbial Endophytes: Sustainable Approach …

69

Nath R, Sharma GD, Barooah M (2012) Efficiency of tricalcium phosphate solubilization by two different endophytic Penicillium sp. isolated from tea (Camellia sinensis L.). Eur J Exp Biol 2(4): 1354–1358 Nautiyal CS (1999) An effect microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270 Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D (2000) Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182:291–296 Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39 Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth– promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate-and jasmonate/ethylene dependent signaling pathways. Mol Plant-Microbe Interact 24:533–542 Norrish K, Rosser H (1983) Mineral phosphate. Soils, an Australian viewpoint. Academic Press, Melbourne, CSIRO/London, UK, Australia, pp 335–361 Omar SA (1998) The role of rock-phosphate-solubilizing fungi and vesicular-arbuscular-mycorrhiza (VAM) in growth of wheat plants fertilized with rock phosphate. World J Microbiol Biotechnol 14:211–218 Oteino N, Culhane J, Germaine KJ, Ryan D, Brazil D, Dowling DN (2013) Screening of large collections of plant associated bacteria for effective plant growth promotion and colonization. In: Association of Applied Biologists (AAB) Conference 2013 - Positive plant microbial interactions: their role in maintaining sustainable agricultural and natural ecosystems (North Linconshire), pp 13–18 Otieno N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Fron Microbiol 6:745 Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils 46:807–816 Panchal H, Ingle S (2011) Isolation and characterization of endophytes from the root of medicinal plant Chlorophytum borivilianum (Safed musli). J Adv Develop Res 2(2):205–209 Pandya M, Rajput M, Rajkumar S (2015) Exploring plant growth promoting potential of non rhizobial root nodules endophytes of Vigna radiata. Microbiology 84(1):80–89 Partida-Martínez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100 Patel HA, Patel RK, Khristi SM, Parikh K, Rajendran G (2012) Isolation and characterization of bacterial endophytes from Lycopersicon esculentum plant and their plant growth promoting characteristics. Nepal J Biotechnol 2(1):37–52 Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801 Penuelas J, Rico L, Ogaya R, Jump A, Terradas J (2012) Summer season and long- term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biol 14:565–575 Pereira SIA, Castro PML (2014) Diversity and characterization of culturable bacterial endophytes from Zea mays and their potential as plant growth-promoting agents in metal-degraded soils. Environ Sci Pollut Res 21(24):14110–14123 Pereira SI, Monteiro C, Vega AL, Castro PM (2016) Endophytic culturable bacteria colonizing Lavandula dentata L. plants: isolation, characterization and evaluation of their plant growthpromoting activities. Ecol Enginer 87:91–97 Perotti R (1926) On the limits of biological enquiry in soil science. Proc Int Soc Soil Sci 2:146–161 Pham VT, Rediers H, Ghequire MG, Nguyen HH, De Mot R, Vanderleyden J, Spaepen S (2017) The plant growth-promoting effect of the nitrogen-fixing endophyte Pseudomonas stutzeri A15. Arch Microbiol 199(3):513–517

70

A. Dahiya et al.

Picollo SL, Ferraro V, Alfonzo A, Settanni L, Ercolini D, Burruano S, Moschetti G (2010) Presence of endophytic bacteria in Vitis vinifera leaves as detected by fluorescence in situ hybridization. Ann Microbiol 60:161–167 Pillay V, Nowak J (1997) Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can J Microbiol 43:354–361 Pirhadi M, Enayatizamir N, Motamedi H, Sorkheh K (2018) Impact of soil salinity on diversity and community of sugarcane endophytic plant growth promoting bacteria (Saccharum officinarum l. Var. Cp48). Appl Ecol Environ Res 16(1):725–739 Priyadharsini P, Muthukumar T (2017) The root endophytic fungus Curvularia geniculata from Parthenium hysterophorus roots improves plant growth through phosphate solubilization and phytohormone production. Fungal Ecol 27:69–77 Puente ME, Li CY, Bashan Y (2009a) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401 Puente ME, Li CY, Bashan Y (2009b) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408 Rai R, Dash PK, Prasanna BM, Singh A (2007) Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World J Microbiol Biotechnol 23(6):853–858 Rajamanickam V, Rajasekaran A, Anandarajagopal K, Sridharan D, Selvakumar K, Rathinaraj BS (2010) Anti-diarrheal activity of Dodonaea viscosa root extracts. Int J Pharm Biol 1(4):182–185 Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth promoting bacterial endophytes. Appl Soil Ecol 61:217–224 Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443 Reissinger A, Vilich V, Sikora RA (2001) Detection of fungi in planta: effectiveness of surface sterilization methods. Mycol Res 105(5):563–566 Reiter B, Sessitsch A (2006) Bacterial endophytes of the wildflower Crocus albiflorus analyzed by characterization of isolates and by a cultivation-independent approach. Can J Microbiol 52:140– 149 Rheinhold-Hurek B, Maes T, Gemmer S, Van Montagu M, Hurek T (2006) An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus sp. strain BH72. Mol Plant Microbe Interact 19:181–188 Ribeiro CM, Cardoso EJBN (2012) Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil pine (Araucaria angustifolia). Microbiol Res 167:69–78 Ribeiro VP, Marriel IE, Sousa SM, Lana UG, Mattos BB, Oliveira CA, Gomes EA (2018) Endophytic Bacillus strains enhance pearl millet growth and nutrient uptake under low-P. Braz J Microbiol 49:40–46 Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906 Richardson AE, Barea JM, McNeill AM (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339 Rinu K, Malviya MK, Sati P, Tiwari SC, Pandey A (2013) Response of cold tolerant Aspergillus spp. to solubilization of Fe and Al phosphate in presence of different nutritional sources. ISRN Soil Sci. 10. http://dx.doi.org/10.1155/ 2013/598541 Rinu K, Pandey A (2010) Temperature-dependent phosphate solubilization by cold- and pH-tolerant species of Aspergillus isolated from Himalayan soil. Mycoscience 51:263–271 Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth promoting bacteria. Plant Soil 287:15–21 Rodrıguez H, Gonzalez T, Selman G (2001) Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. J Biotechnol 84(2):155–161 Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

3 Microbial Endophytes: Sustainable Approach …

71

Rojas-Solis D, Zetter-Salmon E, Contreras-Perez M, del Carmen R-GM, Macías-Rodríguez L, Santoyo G (2018) Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growthpromoting effects. Biocatal Agric Biotechnol 13:46–52 Romero A, Carrion G, Rico-Gray V (2001) Fungal latent pathogens and endophytes from leaves of Parthenium hysterophorus (Asteraceae). Fungal Divers 7:81–87 Roos IMM, Hattingh MJ (1983) Scanning electron microscopy of Pseudomonas syringae pv. morspmnorum on sweet cherry leaves. Phytopathol Z 108:18–25 Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19:827–837 Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9 Sanderson MA, Adler PR, Boateng AA, Casler MD, Sarath G (2006) Switchgrass as a biofuels feedstock in the USA. Can J Plant Sci 86:1315–1325 Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402. https://doi.org/10.3389/fmicb.2015.00402 Santoyo M, Moreno-Hagelsieb G, del Carmen O-MM, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99 Sashidhar B, Podile AR (2009) Transgenic expression of glucose dehydrogenase in Azotobacter vinelandii enhances mineral phosphate solubilization and growth of sorghum seedlings. Microbiol Biotechnol 2:521–529 Savary S, Ficke A, Aubertot JN, Hollier C. (2012) Crop losses due to diseases and their implications for global food production losses and food security. Springer Scherling C, Ulrich K, Ewald D, Weckwerth W (2009) A metabolic signature of the beneficial interaction of the endophyte Paenibacillus sp. isolate and in vitro–grown poplar plants revealed by metabolomics. Mol Plant-Microbe Interact 22:1032–1037 Schmidt CS, Mrnka L, Frantík T, Lovecka P, Vosatka M (2018) Plant growth promotion of Miscanthus giganteus by endophytic bacteria and fungi on non-polluted and polluted soils. World J Microbiol Biotechnol 34:48. https://doi.org/10.1007/s11274-018-2426-7 Schulz B, Wanke U, Draeger S, Aust HJ (1993) Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycol Res 97:1447–1450 Scott RI, Chard JM, Hocart MJ, Lennard JH, Graham DC (1996) Penetration of potato tuber lenticels by bacteria in relation to biological control of black leg disease. Potato Res 39:333–344 Sehrawat A, Sindhu SS (2019) Exploitation of rhizosphere microorganisms to reduce pesticide application for improving food safety. Defence Life Sci J 4(4):220–225 Senthilkumar M, Anandham R, Madhaiyan M, Venkateswaran V, Sa T (2011) Endophytic 895 bacteria: perspectives and applications in agricultural crop production. In: Bacteria in Agrobiology: Crop 896 Ecosystems: Springer, pp 61–96 Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Van Elsas JD, Faure D (2005) Burkholderia phytofirmans sp. nov., a novel plant associated bacterium with plant-beneficial properties. Intern J Syst Evol Microbiol 55:1187–1192 Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36 Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 50:239–249 Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39:23–32 Shabanamol S, Divya K, George TK, Rishad KS, Sreekumar TS, Jisha MS (2018) Characterization and in planta nitrogen fixation of plant growth promoting endophytic diazotrophic Lysinibacillus sphaericus isolated from rice (Oryza sativa). Physiol Mol Plant Pathol 102:46–54

72

A. Dahiya et al.

Shahzad R, Waqas, M, Khan, AL, Al-Hosni K, Kang SM, Seo CW Lee IJ (2017) Indole acetic acid production and plant growth promoting potential of bacterial endophytes isolated from rice (Oryza sativa L.) seeds. Acta Biol Hung 68(2):175–186 Sharma S, Aneja M, Mayer J, Schloter M, Munch J (2004) RNA fingerprinting of microbial community in the rhizosphere soil of grain legumes. FEMS Microbiol Lett 240:181–186 Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilising microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587 Sharma VK, Nowak J (1998) Enhancement of Verticillium wilt resistance in tomato transplants by in vitro co-culture of seedlings with a plant growth promoting rhizobacterium (Pseudomonas sp. strain PsJN). Can J Microbiol 44(6):528–536 Sharon JA, Hathwaik LT, Glenn GM, Imam SH, Lee CC (2016) Isolation of efficient phosphate solubiling bacteria capable of enhancing tomato plant growth. J Soil Sci Plant Nutr 16:525–536 Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B (2015) Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. MBio 6: e00621–15 Shen YQ, Bonnot F, Imsand EM, Rose FJM, Sjolander K, Klinman JP (2012) Distribution and properties of the genes encoding the biosynthesis of the bacterial cofactor, pyrroloquinoline quinone. Biochemistry 51:2265–2275 Shi Y, Yang H, Zhang T, Sun J, Lou K (2014) Illumina-based analysis of endophytic bacterial diversity and space-time dynamics in sugar beet on the north slope of Tianshan mountain. Appl Microbiol Biotechnol 98:6375–6385 Shidore T, Dinse T, Öhrlein J, Becker A, Reinhold-Hurek B (2012) Transcriptomic analysis of responses to exudates reveal genes required for rhizosphere competence of the endophyte Azoarcus sp. strain BH72. Environ Microbiol 14:2775–2787 Sieber TN, Grünig CR (2006) Biodiversity of fungal root-endophyte communities and populations in particular of the dark septate endophyte Phialocephala fortinii. In: Schulz B, Boyle C, Sieber TN (eds) Microbial Root Endophytes. Springer, Berlin, pp 107–132 Sindhu SS, Dadarwal KR (2000) Competition for nodulation among rhizobia in Rhizobium-legume symbiosis. Indian J Microbiol 40:211–246 Sindhu SS, Sharma R (2019) Amelioration of biotic stress by application of rhizobacteria for agriculture sustainability. Sayyed RZ, Tabassum B (eds). In: Plant Growth promoting rhizobacteria for sustainable stress management, microorganisms for sustainability. Springer Nature Singapore Pte Ltd. Chapter 5, https://doi.org/10.1007/978-981-13-6986-5_5 Sindhu SS, Sharma R, Sindhu S, Sehrawat A (2019) Soil fertility improvement by symbiotic rhizobia for sustainable agriculture. D. G. Panpatte, Y. K. Jhala (eds.), In: Soil fertility management for sustainable development, Springer Nature Singapore Pte Ltd. pp. 101–166. https://doi.org/10. 1007/978-981-13-5904-0_7 Sindhu SS, Verma MK, Mor S (2009) Molecular genetics of phosphate solubilization in rhizosphere bacteria and its role in plant growth promotion. In: Khan MS, Zaidi A (eds) Phosphate Solubilizing Microbes and Crop Productivity. Nova Science Publishers, U.S.A, pp 199–228 Sindhu SS, Phour M, Choudhary SR, Chaudhary D (2014) Phosphorus cycling: prospects of using rhizosphere microorganisms for improving phosphorus nutrition of plants. In: Parmar N, Singh A (eds) Geomicrobiology and Biogeochemistry. Springer-Verlag, Berlin, Heidelberg, pp 199–237 Sloger C, van Berkum P (1992) Approaches for enhancing nitrogen fixation in cereal crops. In: Dutta SK, Sloger C (eds) Biological nitrogen fixation associated with rice production. Oxford and IBH Publishing, New Delhi, India, pp 229–234 Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London, UK Smits TH, Rezzonico F, Kamber T, Blom J, Goesmann A, Ishimaru CA, Frey JE, Stockwell VO, Duffy B (2011) Metabolic versatility and antibacterial metabolite biosynthesis are distinguishing genomic features of the fire blight antagonist Pantoea vagans C9-1. PLoS One 6(7):e22247 Song Z, Ding L, Ma B, Li W, Mei R (1999) Studies on the population and dynamic analysis of peanut endophytes. Acta Phytophyl Sin 26:309–314

3 Microbial Endophytes: Sustainable Approach …

73

Sorensen J, Sessitsch A (2015) Plant-associated bacteria lifestyle and molecular interactions. In: van Elsas JD, et al (eds) Modern soil Microbiology, 2nd edn. CRC Press, 2006, pp 211–236 Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3(4):a001438 Spagnoletti FN, Tobar NE, Di Pardo AF, Chiocchio VM, Lavado RS (2017) Dark septate endophytes present different potential to solubilize calcium, iron and aluminum phosphates. Appl Soil Ecol 111:25–32 Sprent JI, deFaria SM (1998) Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110:157–165 Sturz A, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15:183–190 Sturz AV, Christie BR, Matheson BG, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25:13–19 Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30 Sun H, Kong L, Du H, Chai Z, Gao J, Cao Q (2019) Benefits of Pseudomonas poae s61 on Astragalus mongholicus growth and bioactive compound accumulation under drought stress. J Plant Interact 14(1):205–212 Sun LN, Zhang YF, He LY, Chen ZJ, Wang QY, Qian M, Sheng XF (2010) Genetic diversity and characterization of heavy metal resistant- endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Biores Technol 101:501–509 Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296:131–136 Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53:1195– 1202 Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, vander Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75:748–757 Tao GC, Tian SJ, Cai MY, Xie GH (2008) Phosphate- solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523 Thakore Y (2006) The biopesticide market for global agricultural use. Indust Biotechnol 2:194–208 Thomas P, Upreti R (2014) Testing of bacterial endophytes from non-host sources as potential antagonistic agents against tomato wilt pathogen Ralstonia solanacearum. Adv Microbiol 4:656 Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6:e17968 Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245 Trivedi P, Duan Y, Wang N (2010) Huanglongbing, a systemic disease, restructures the bacterial community associated with citrus roots. Appl Environ Microbiol 76:3427–3436 Trognitz F, Scherwinski K, Fekete A, Schmidt S, Eberl L, Rodewald J, Schmid M, Compant S, Hartmann A, Schmitt-Kopplin P (2008) Interaction between potato and the endophyte Burkholderia phytofirmans Trotel-Aziz P, Couderchet M, Biagianti S, Aziz A (2008) Characterization of new bacterial biocontrol agents Acinetobacter Bacillus, Pantoea and Pseudomonas spp. mediating grapevine resistance against Botrytis cinerea. Environ Exp Bot 64:21–32 Truyens S, Weyens N, Cuypers A, Vangronsveld J (2014) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50 Turan M, Ataoglu N, Sahin F (2006) Evaluation of the capacity of phosphate solubilizing bacteria and fungi on different forms of phosphorus in liquid culture. J Sustain Agric 28:99–108

74

A. Dahiya et al.

Ullah A, Heng S, Munis MF, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40 van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310 Varma A, Verma S, Sudah SN, Franken P (1999) Piriformospora indica, a cultivable plant growthpromoting root endophyte. Appl Environ Microbiol 65:2741–2744 Velázquez E, Rojas M, Lorite MJ, Rivas R, Zurdo-Pineiro JL, Heydrich M, Bedmar EJ (2008) Genetic diversity of endophytic bacteria which could be find in the apoplastic sap of the medullary parenchyma of the stem of healthy sugarcane plants. J Basic Microbiol 48:118–124 Verma N, Singh NA, Kumar N, Raghu HV (2013) Screening of different media for sporulation of Bacillus megaterium. Intern J Microbiol Res Rev 1:68–73 Verma P, Yadav AN, Kazy SK, Saxena AK, Suman A (2014) Evaluating the diversity and phylogeny of plant growth promoting bacteria associated with wheat (Triticum aestivum) growing in central zone of India. Intern J Curr Microbiol Appl Sci 3(5):432–447 Verma S, Varma A, Rexer K-H, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. nov. sp. nov., a new root-colonizing fungus. Mycologia 90:896–903 Vu DT, Tang C, Armstrong RD (2008) Changes and availability of P fraction following 65 years of P application to a calcareous soil in a Mediterranean climate. Plant Soil 304:21–33 Wagh J, Chanchal K, Sonal S, Praveena B, Archana G, Kumar GN (2016) Inoculation of genetically modified endophytic Herbaspirillum seropedicae Z67 endowed with gluconic and 2-ketogluconic acid secretion, confers beneficial effects on rice (Oryza sativa) plants. Plant Soil 409(1–2):51–64 Walitang DI, Kim K, Madhaiyan M, Kim YK, Kang Y, Sa T (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of rice. BMC Microbiol 17(1):209 Wang LW, Xu BG, Wang JY, Su ZZ, Lin FC, Zhang CL, Kubicek CP (2012) Bioactive metabolites from Phoma species, an endophytic fungus from the Chinese medicinal plant Arisaema erubescens. Appl Microbiol Biotechnol 93(3):1231–1239 Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52(suppl 1):487–511 Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate solubilizing fungi. Adv Agron 69:99–151 Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov LO, Wuichet K, Hurst GB, McDonald WH, Robertson JS et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7:e1002430 Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735 Wu L, Guo S (2008) Interaction between an isolate of dark-septate fungi and its host plant Saussurea involucrata. Mycorrhiza 18:79–85 Xia Y, DeBolt S, Dreyer J, Scott D, Williams MA (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Frontiers Plant Sci 6:490 Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544 Yazdani M, Bahmanyar MA, Pirdashti H, Esmaili MA (2009) Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). World Acad Sci Eng Technol 49:90–92 Yuan M, He H, Xiao L, Zhong T, Liu H, Li S, Deng P, Ye Z, Jing Y (2014) Enhancement of Cd phytoextraction by two Amaranthus species with endophytic Rahnella sp. JN27. Chemosphere 103:99–104 Zachow C, Fatehi J, Cardinale M, Tilcher R, Berg G (2010) Strain-specific colonization pattern of Rhizoctonia antagonists in the root system of sugar beet. FEMS Microbiol Ecol 74:124–135

3 Microbial Endophytes: Sustainable Approach …

75

Zhang Y, Kang X, Liu H, Liu Y, Li Y, Yu X, Zhao K, Gu Y, Xu K, Chen C, Chen Q (2018) Endophytes isolated from ginger rhizome exhibit growth promoting potential for Zea mays. Arch Agron Soil Sci 64(9):1302–1314 Zhao L, Xu Y, Lai XH, Shan C, Deng Z, Ji Y (2015) Screening and characterization of endophytic Bacillus and Paenibacillus strains from medicinal plant Lonicera japonica for use as potential plant growth promoters. Brazilian J Microbiol 46(4):977–989 Zhao S, Wei H, Lin CY, Zeng Y, Tucker MP, Himmel ME, Ding SY (2016) Burkholderia phytofirmans inoculation-induced changes on the shoot cell anatomy and iron accumulation reveal novel components of Arabidopsis-endophyte interaction that can benefit downstream biomass deconstruction. Front Plant Sci 7:24–35 Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68:2198–2208 Zuniga A, Poupin MJ, Donoso R, Ledger T, Guiliani N, Gutierrez RA, González B (2013) Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant-Microbe Interact 26:546–553

Chapter 4

Cattle Dung Manure Microbiota as a Substitute for Mineral Nutrients and Growth Management Practices in Plants Sandhya Dhiman, Sandeep Kumar, Nitin Baliyan, Shrivardhan Dheeman, and Dinesh Kumar Maheshwari Abstract Minerals are ubiquitous and found in two forms “macronutrients and micronutrients” in soil. To meet out their requirements to crops. Cow dung is high in organic materials rich in nutrients and contains (3-2-1 NPK) besides rich in ammonia. On the other hand, dung and manure is the source of potentially beneficial bacteria used as a rich fertilizer and produce biogas which is eco-friendly and an alternative to fossil fuels. Cow dung has been used in various forms for centuries, like fires, for heating, cooking. Hindu rituals performed during popular festivals. A diverse group of microbes inhabiting in dung mainly bacteria has multiple roles such as plant growth promotion and protection from diseases in plants. The addition of dung corroborates nutrients, micronutrients, and organic matter availability to soil and favors growth/activity of symbiotic bacteria resulting in improved biomass. Composting for agricultural benefits is the need of today to help in the reclamation of degraded soil of wastelands. The application of dung/compost and microorganisms act as catalysis for farmers in developing countries to exploit microbiota for augmenting the crop productivity, and ensuring continued maintenance and building up of the soil fertility for greater sustainability. Keywords Dung · Nutrients · Microorganisms · Soil fertility · Plants

S. Dhiman (B) · S. Kumar · N. Baliyan · S. Dheeman · D. K. Maheshwari Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India e-mail: [email protected] S. Dheeman e-mail: [email protected] S. Dheeman Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Dehradun 248 161, Uttarakhand, India © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_4

77

78

S. Dhiman et al.

4.1 Introduction Today’s challenge in modern agriculture is to attain high agrobiological sustainability in terms of crop productivity and soil health. Although during green revolution, the exhibited use of synthetic fertilizers accomplished crop’s high yield but at the same time also led to adverse effects such as degradation and acidification of soil, mismanaged ecology, deterioration of soil fertility, and decrease in the yield of the crop (Ju et al. 2009). The major goal of nutrient management is to enhance agronomic crop productivity to meet the food demands of the ever-increasing population. The chemical fertilizers disturb the soil physiochemical properties viz., soil texture, porosity, water holding capacity, and beneficial soil microbial flora. The usage of inorganic fertilizers has drastically dropped due to the energy crisis, which has immensely affected most of the developing countries (Gulshan et al. 2013). A low-input agricultural system which relies on the input of organic materials holds great promise not only to diminish the use of synthetic fertilizer but also to recover crop productivity and ensure ecosystem sustainability against nutrient mining and degradation of soil and water resources (Tilman et al. 2002; Kravchenko et al. 2017). Soil is a sink of plant nutrients that remain in both soluble and insoluble forms. Plants can easily take up the former but difficult to get assessed with insoluble forms which are transformed into a soluble form by various mechanisms (Maathuis and Diatloff 2013). A large group of diverse microbiota inhabiting in the soil transform insoluble minerals into accessible form for their uptake by plants. Microbial activity is essential for the release of nutrients from dung without such release the available plant nutrient supply would soon be hampered and the soil would become infertile (Jin et al. 2016). Microbes inhabiting in dung complete the cycle by returning into the soil those nutrients the plants’ uptake from it (Chen et al. 2015). An active, thriving microbial population is a good bio-indicator of fertile soil. The shortage of fuelwood is a major problem hence, forces the rural people to use the dung for their fuel purpose, which affects the productivity status of cultivated land. In India tons of the livestock dung produced annually, it remains unutilized or is not being fully utilized results in a loss of buffalo dung 12.20 kg dung in a day and cow dung 11.6 kg animal/day and goat dung 0.70 kg animal in a day (Chauhan and Singh 2012). Further, livestock waste acted as the chief source of noxious gases (greenhouse gas), pollution, pathogens, and odor having communal health and environmental pollution (Martinez et al. 2009) which adversely affect air quality especially in rural areas dung acts as cooking fuel coupled with poor ventilation (https://www.indiatimes.com/news/india/pollution-due-to-burningof-cow-dung-wood-as-fuel-killed-1-24-lakh-people-in-one-year-332719.html). The share of the Indian population relies on traditional biomass for cooking stands at 72%. Bekele et al. (2013), observed 943 metric tonnes of, dung used by households annually. As a result, N, P, K, Ca, Mg, and Fe nutrients are lost per year, This practice hurts the nutrient balance of the soil and consequently affects agricultural productivity. Investigators found that while the dung burnt in the kitchen contains as much as 25% of the arsenic in fumes (indoor) absorbed by the respiratory tract of people thus leads to diseases such as persistent cough and chronic

4 Cattle Dung Manure Microbiota as a Substitute …

79

bronchitis (https://www.downtoearth.org.in/news/cow-dung-smoke-could-cause-ars enic-poisoning–4002). Hence, its proper management is yet to be done to mitigate these pollutants to shield the environment from obnoxious gases. Air pollution (methane, CO2 , etc.) also contributes to greenhouse gases (GHGs) leading to climate change (Ramanathan and Feng 2009). Various workers reported management strategies to reduce the wastage of animal dung and minimize soil toxicity (Li et al. 2016a). The proper utilization of livestock waste into biogas (Afazeli et al. 2014), compost formation (Bernal et al. 2009), and vermicomposting (Garg et al. 2005) assisted to accomplish an increase in crop yield and sustainability (Chadwick et al. 2015). Likewise, utilization of them in terms of organic fertilizers provides an opportunity for the agricultural sector for organic farming thus, lessen their reliance on chemical fertilizer (Bandyopadhyay et al. 2010). Dung is a mixture of many mineral nutrients found to contain crude fiber, crude protein, cellulose, hemicellulose, and 24 types of minerals such as nitrogen, potassium, along with trace amount of sulfur, iron, magnesium, copper, cobalt, manganese, etc. Generally, dung contains approximately 80% water and matrix of undigested plant material, rich in nutrients, microorganisms, and their by-products. Whereas, indigenous Indian cow comprises a higher sum of calcium, phosphorus, zinc, and copper than the other minerals (Garg and Mudgal 2007; Randhawa and Kullar 2011). Therefore, the nutrient management of dung is essential to enhance agronomic productivity (Gholamhoseini et al. 2013). Animals play an important role in energy generation processes such as by converting plant energy into useful work, e.g. dung used for fuel through dung cakes and biogas to replace for soil fuel, i.e. charcoal, fuelwood, firewood, etc. (Raj et al. 2014). Available literature revealed that dung acts as a disinfectant for the home in a rural area and now available in the form of wood used for fuel purposes.

4.2 Microbiology of Dung Although, animal dung has been extensively exploited for its use as organic agricultural fertilizers, as well as alternative fuel/biogas due to high methane content (Abdulkareem 2005). But research on the microbial diversity and other potential applications of cattle dung (Gattinger et al. 2007) is yet to be established (Yokoyama et al. 2007; Dhiman et al. 2019). Microbial flora of dung includes both aerobic and anaerobic microorganisms including an abundant number of bacilli, lactobacilli, cocci, and some identified and unidentified fungi and yeasts (Muhammad and Amusa 2003; Vijayaraghavan et al. 2006; Swain et al. 2012). Various bacterial genera viz., Citrobacter koseri, Enterobacter aerogenes, Escherichia coli, Klebsiella oxytoca, Klebsiella pneumoniae, Kluyvera spp, Morgarella morganii, Pasteurella spp, Providencia alcaligenes, Providencia stuartii, and Pseudomonas spp. have been reported from cow dung (Sawant et al. 2007). In addition, the lower part of animal gut includes Lactobacillus plantarum, Lactobacillus casei, Lactobacillus acidophilus, Bacillus subtilis, Enterococcus

80

S. Dhiman et al.

diacetylactis, Bifidobacterium spp. and yeasts (commonly Saccharomyces cerevisiae), possessing probiotic activity (Ware Fungsin et al. 1988). Dung inhabiting methanogens particularly Archaea and the phylum Euryarchaeota including Methanomicrobium, Methanobrevibacter ruminantium, Methanobacterium formicicum, Methanomicrobium mobile, Methanosarcina barkeri, etc., are not only confined to the rumen in cattle and other ruminants but proved an excellent source of bioenergy. Swain and Ray (2009) studied that B. subtilis isolated from cow dung enhanced plant growth, phosphorous solubilization, sulfur oxidation and was found to yield industrial products. Their presence has now been discovered in the soil since dung is has been accepted as a soil fertilizer since pre-historic time (Hook et al. 2010). Recently, cow dung has been proved an excellent source of the management of soil nutrients (Dhiman et al. 2020). Few of them are listed in Table 4.1. Table 4.1 Diversity and distribution of microorganisms in cattle dung Microbial strains

References

Bacillus cereus, Bacillus Subtilis

Muhammad and Amusa (2003)

Paenibacillus favisporus

Velazquez et al. (2004)

Bacillus subtilis

Swain et al. (2012)

B. pumilus, B. macereans, B. sphearicus, B. laterosporus, Micrococcus varians, Proteus mirabilis, E. aerogens

Adegunloye et al. (2007)

Pseudomonas spp., Bacillus spp.

Akinde and Obire (2008)

Enterobacter spp., Rahnella spp.

Fuentes et al. (2009)

Citrobacter spp.

Pandey et al. (2009)

Pseudomonas jessenii, P. synxantha

Srivastava et al. (2010)

Thermoanaerobacterium thermostercus

Romano et al. (2010)

Ruminococcus sp., Enterococcus casseliflavus/gallinarum

Wahyudi et al. (2010)

Bacillus sp.

Teo and Teoh (2011)

Clostridium cellulosi

Carillo et al. (2012)

Bacteroides, Fermicutes, Proteobacteria

Girija et al. (2013)

Lysinibacillus xylanilyticus, B. licheniformis, B. subtilis, B. cereus

Radha and Rao (2014)

Pseudomonas xanthomarina, P. stutzeri, and Bacillus niacin Das et al. (2017) Pseudomonas otitidis, Stenotrophomonas korensis, Serratia marcescens

Vyas and Kumar (2018)

Bacillus cereus

Croos et al. (2019)

Proteus mirabilis

Dhiman et al. (2019)

4 Cattle Dung Manure Microbiota as a Substitute …

81

4.3 Dung: Bioresource of Energy At present, the consciousness of organic matter and the concept of sustainable agriculture have been achieving impetus among Indian farmers to produce good quality consumable agricultural products (Eastman et al. 2001). Natural resources to generate energy always proved to be an important issue in the enhancement of the economy of India. In this context animal waste can be cost-effectively used to produce energy while contributing a significant portion of energy independence, and reducing disposal costs and pollution (Kemausuor et al. 2016). As stated earlier, the availability of animal dung is produced in large quantities, thus forms a sound base for nonconventional energy. Chynoweth et al. (1993) suggested as potential sources of biogas production include cattle waste, buffalo waste, piggery waste, chicken waste including human excreta. Due to an abundance of dung availability and rich in organic matter, it is easily accessible for biogas production and acts as a rich habitat for various microbes such as methanogens, hydrogen-producing, and cellulose-degrading bacteria. In India, methane is popularly called “gobar gas” and produced by anaerobic microorganisms. The scientists engaged this work stated that organisms work synergistically that it can do more than is estimated by “summing.” Although, a large number of facultative anaerobic or obligate anaerobes have been involved in various microbial reactions for energy (biogas) generation processes the exact role of individual organism is yet to be determined (Güllert et al. 2016). Some of the microorganisms involved in synthesizing various products given in Table 4.2. A diverse group of bacteria such as Pseudomonas sp., Azotobacter sp., and other purple sulfur or purple non-sulfur bacteria is the main inhabitants of dung responsible for the production of the maximum amount of methane gas in comparison to other photosynthetic bacteria (Zhao et al. 2013). The anaerobic fermentation of animal wastes does not require the addition of seed bacteria for biogas production, and this feature differentiates animal waste from other organic wastes (Yokoyama et al. 2007). The animal waste on this planet produces around 55–65% methane, which upon release in the atmosphere can affect global warming 21 times higher than the rate CO2 does (Abbasi et al. 2012). Methanogens, a dominant heterogeneous group of and/or bacteria/archaea ferment organic matter of the dung anaerobically produce biogas which is a mixture of different gases mainly constitutes methane (50–65%) and CO2 (25–45%). Dung excreted by 3–5 cattle/day can run a biogas plant of 8–10 m3 which can yield 1.5– 2 m3 biogas per day, enough for the family of 6–8 persons, can cook a meal for 2 or 3 times or may light two lamps for 3 h or run a refrigerator for all day and can also operate a 3-KW motor-generator for 1 h (Stanley et al. 2013). Earlier, Ranade et al. (1990) analyzed the effect of different total solid contents on biogas production and reported that the optimum production occurred at 8%. Interestingly, Garg et al. (2005) reported that buffalo dung contained 22.3% solid contents. A 1-m3 biogas plant produced 28.78 l/kg (0.028 m3 ) to 32.76 l/kg (0.032 m3 ) of biogas, respectively, when daily feed with 22 kg of dung/m3 which is mixed with an equal amount of water

82

S. Dhiman et al.

Table 4.2 Methanogenic bacteria and products formed from their respective substrates Bacterium

Substrate

Products

Methanobacterium formicum

CO H2 + CO2 Formate

CH4

M. mobilis

H2 + CO2 Formate

CH4

M. propionicum

Propionate

CO2 + acetate

M. ruminaticum

Formate H2 + CO2

CH4

M. soehngenii

Acetate butyrate

CH4 + CO2

M. suboxydans

Caproate and butyrate

Propionate & Acetate

Methanococcus mazei

Acetate and butyrate

CH4 + CO2

M. vannielli

H2 + CO2 Formate

CH4

Methanosarcina barkerii

H2 + CO2 Methanol acetate

CH4 CH4 CH4 + CO2

M. methanica

Acetate butyrate

CH4 + CO2

Source Chawla OP (1986) Advances in biogas technology

with 9–10% of total solids. The maximum production of biogas from that plant is 39.00 l/kg (0.039 m3 ) and 40.04 l/kg (0.04 m3 ), respectively, when operated at the temperature of 23.5 °C (Carotenuto et al. 2016). On the other hand, the farmers also obtain 13.87 metric tons of organic fertilizer per year from the biogas plant. Romano et al. (2010) investigated the suitability of buffalo manure bacterial community for biogas production. Stimulation of biogas production from dung mixing with cattle urine reported four times in comparison to dung alone. Cattle urine dung-slurry gives increased biogas production (Mutesasira et al. 2015). Studies suggested that the microbial populations in dung come from endophytic bacteria of fodder grasses. It has been established by workers that some of the bacteria have the ability of colonization in interior tissues of a host plant and form a beneficial symbiotic association to improve the growth of the host plant (Li et al. 2016b). Sphingomonas, Bacillus, Pantoea, Enterobacter, Pseudomonas, etc., are some of the reported endophytes in fodder grasses. Other than these, few more endophytes have also been reported as given in host in Table 4.3.

4 Cattle Dung Manure Microbiota as a Substitute …

83

Table 4.3 Endophytic bacteria associated with animal feed Source

Genera

References

Zoysia japonica

Acremonium endophytes

Zhibiao (1996)

Vitis vinifera, Panicum virgatum

Burkholderia phytofirmans, Burkholderia sp.

Compant et al. (2010)

Melinis minutiflora

Azospirillum melinis

Peng et al. (2006)

Zea mays kernels

Pantoea sp., Frigoribacterium sp.,

Rijavec et al. (2007)

Brachiaria decumbens

Bradyrhizobium sp.

Kelemu et al. (2011)

Medicago sativa

Micromonospora sp.

Martínez-Hidalgo et al. (2014)

Deschampsia flexuosa

Pedobacter sp., Enterobacter sp.a , Xanthomonas sp., Paracoccus sp.

Poosakkannu et al. (2015)

Pennisetum purpureum, Medicago sativa

Sphingomonas paucimobilis, Bacillus megateriuma

Li et al. (2016a), Stajkovi´c et al. (2009)

Cymbopogon citratus

Bacillus spp.a , Escherichia colia , Klebsiella pnuemoniae, Micrococcus spp.a , Pseudomonas sppa .

Inuwa et al. (2017)

Beta vulgaris, Phragmites australis

Pseudomonas sp.a , Xanthomonadale sp. Piernik et al. (2017), White et al. (2018)

Leersia oryzoides

Microbacterium sp., Pseudomonas baetica, Pantoea hericii, Paenibacillus sp.a , Pseudomonas oryzihabitans, Pantoea vagans

a Dung

Verma et al. (2018)

inhabitants

4.4 Dung: Source of Industrial Products By advantage of the microbial inhabitants bacteria and other microorganisms of extremophilic nature, scientists took advantage of the microbiota for industrial applications. The bacteria or their metabolites are extraordinary and play an important role in nature and at industrial level. Such as they secrete stable enzymes at extreme temperature and pressure, can be used for biodegradation and bioremediation, can be a good source of biofuel and bioenergy. These are the source of specialized pigments for solar cells able to work in extreme conditions such as polar caps (Arora and Panosyan 2019). There is a non-stop search for the plausible microorganisms that are in a position to synthesize industrially viable chemicals of biotechnological importance. The range of microbes in cow dung makes an attainable supply for the discovery of novel major and secondary metabolites (Meena et al. 2013). Bacillus spp. inhabiting in cow dung can produce cellulases, pectinases, and hydrogenases, etc. (Singh et al. 2013; Vijayaraghavan et al. 2016). Novel thermotolerant endoglucanase (CMCase) has been purified and characterized from Bacillus strain inhabiting in cow dung (Sadhu et al. 2013). Few thermotolerant bacteria with the capability of producing thermotolerant enzymes like protease, lipase, and esterase

84

S. Dhiman et al.

Table 4.4 Organic acids secreted by bacteria isolated from dung Bacteria

pH

Temperature (°C)

Acids formed

Bacillus cereus

5.2

25–30

Acetic, lactic

Bacillus knelfelkamipi

5.2–8.0

25–35

Acetic, lactic

Bacillus megaterium

5.2–7.5

28–35

Acetic, lactic

Bacteroides succinogenes

5.2–7.5

25–35

Acetic, succinic

Clostridium carnofoetidum

5.0–8.5

25–37

–

Clostridium cellobioparus

5.0–8.5

36–38

Formic, acetic, lactic, ethanol, CO2

Clostridium dissolvens

5.0–8.5

35–51

Formic, acetic, lactic, succinic

Clostridium theymocellulaseum

5.0–8.5

55–65

Formic, acetic, lactic, succinic, ethanol

Pseudomonas formicans

–

33–42

Formic, acetic, lactic, succinic, ethanol

Ruminococcus flavifaciens

–

33–38

Formic, acetic, succinic

Source Chawla OP (1986) Advances in biogas technology

lipase have been detected in manure compost (Charbonneau et al. 2012). Previously, xylanolytic bacteria have obtained growing industrial activity in numerous industries such as enzyme-aided bleaching of paper (Velazquez et al. 2004), production of ethanol from plant biomass, animal feed additives). A member of xylanolytic bacteria Paenibacillus favisporus sp., from cow dung, produced an extensive range of hydrolytic enzymes such as xylanases, cellulases, amylases, gelatinase, urease, and β-galactosidase (Velazquez et al. 2004) showed feasible for industrial applications. The occurrence of naturally occuring steroid hormones in dung has also been reported by several workers (Ermawati et al. 2007; Andaluri et al. 2012). Mohanta et al. (2017) reported Bacillus sp. as amino acid-producing bacteria from cow dung and amino acids namely cysteine, serine, and methionine were characterized by Bacillus sp. These amino acids are the building blocks of proteins, constitute a major part of the body, involved in building cells and repairing tissues, and form antibodies to combat foreign bodies like bacteria and viruses. Longback, Chawla (1986) mentioned both strong and weak organic acids, ethanol, and other metabolites are produced by a different group of bacteria as given in Table 4.4.

4.5 Dung and the Mineral Nutrients Management The interest in the use of dung has increased exponentially especially to preserve soil fertility for the long term. Dung contains small portions of plant nutrients in inorganic forms that do not require mineralization to be solubilized in the soil water solution. This solubilized fraction has a direct influence; its nutrients are easily available for plant uptake, while the organic forms of plant nutrients in dung provide the slow

4 Cattle Dung Manure Microbiota as a Substitute …

85

release effect for nutrients through the growing season, given the reason for suitability for environmental and soil conditions because of the gradual release of plant nutrients (Eghball et al. 2002). It is yet to consider a match between nutrient release from dung and plant demand for nutrients; mismatch might result in nutrient leaching (main nitrate in humid areas), toxicity, or nutrient deficiency. Nevertheless, sole compost is not enough to satisfy the farm production to cover the whole nutrients requirements in a short-term period. Besides, meeting crop demand for nutrients through organic matter supply does not guarantee optimum supply of minerals require for crop yield due to the fact that the decomposition of organic matter is a climate-dependent process (Wall et al. 2008). On the other hand, organic matter amendments in soil stimulate the biological activity, which makes the nutrients cycle less predictable (Tao et al. 2015). Therefore, organic farming practices include rotation of legume crops, green manuring, returning uncomposted agricultural wastes to soil, and crop residues incorporation in the fertilization schemes assist to provide, soluble fractions of the essential nutrients (Reckling et al. 2016). Incorporation of green manure crops into soil provides a considerable amount of soluble nutrients into the soil system. Ewulo et al. (2007) observed the comparative effect of cow dung manure on soil and leaf nutrient and yield of pepper. The nutrient analysis in different manure is given in Table 4.5. Since historic times in India, cattle dung is accepted and utilized in many ways. The potential of dung in enhancing soil fertility was known to Indian sub-continental farmers for centuries, but little was known regarding role of dung microorganisms in mediating nutrients cycling in soil (Nopparat et al. 2007). Various workers have reported that these microorganisms play a significant role in composting by the decomposing organic substrate (aerobically) into carbon dioxide, water, minerals, and stabilized organic matter (Bernal et al. 2009; Kala et al. 2009; Vakili et al. 2015). Current literature revealed that researches related to the isolation and characterization of the beneficial bacteria present in biodynamic preparations are few (Giannattasio et al. 2013). A definitive proof is required to know whether bacteria in such formulations have plant growth-promoting rhizobacteria (PGPR) attributes and can improve Table 4.5 Average nutrient content of bio-compost of animal’s origin

Manure type

Nutrient content (%) N

P

K

Cow

0.30–0.45 0.15–0.25 0.05–0.15

Buffalo

0.5–0.9

0.21–0.3

0.05–0.17

Chicken

3.15

1.64

2.07

Poultry manure

2.87

2.93

2.35

Cattle waste vermicompost 0.51–1.61 0.19–1.02 0.15–0.73 Vermicompost

1.20

0.004

0.37

Farm yard manure

0.80

0.41

0.74

Source Miner JR, Smith RJ (1975) Livestock waste management with pollution control

86

S. Dhiman et al.

plant growth under defined conditions in soil microcosms, that overcome the drawbacks of field experiments by eliminating the errors arising from spatial variability of soil physicochemical and fertility properties occur in field gradients (Kalita et al. 2015).

4.6 Dung on Nutrient Uptake in Plants Nowadays, quality not the quantity of crop considered its merit from a commercial marketing point of view. This is the reason organic fertilizers raised crops have been fetching good markets and presently being used as a common agricultural best practices (Ahmad et al. 2019). Moreover, from awareness of the health consciousness point of view consumers are more interested in food of good nutritional quality having devoid of chemical residues in the edible part of the plant. The production of such organic products accomplished due to environmentally friendly and sustainable agricultural practices from economic point of view (Roberts and Mattoo 2018). Amendment of dung increases pH, total nitrogen, and organic carbon, loss on ignition, and exchangeable magnesium and calcium and decreased sulfate sorption in soil (Raj et al. 2014). The dung manure played a noteworthy role in maintaining the nutrient status of the plant (Sukartono et al. 2011). Nevertheless, nutrients contained in animal manures are released more slowly and are stored for a longer time in the soil ensuring longer residual effects similar to the long-term effect of some beneficial plant growth and health supporting bacteria (Maheshwari 2011) on growth and development of crops (Sharma and Mittra 1991; Abou El-Magd et al. 2005). Animals excrete N (nitrogen), phosphorus (P), and potassium (K) in the ingested feed, and these elements also appear in the manures. Thus, manure composition depends on the quality of the animal feed offered to the animals; feeds high in protein would give high nitrogen manures. The more phosphorous and potassium are in the feed, the richer is the manure of these nutrients (Ghosh et al. 2004). Hence it would be a noteworthy and eco-friendly farm practice, besides improving soil fertility by activating soil mineral status and microbial biomass (Ayuso et al. 1996). The manure nourishes soil organisms which gradually provide nutrients accessible to plants. Manures have dual role (i) it contains all necessary nutrients in available forms and (ii) improve the physical and biological properties of the soil (Abou ElMagd et al. 2006). Murmu et al. (2013) observed that organic manure increased crop productivity, nitrogen utilization efficiency, and soil health in tomatoes (Lycopersicon esculentum) and corn (Zea mays) in acidic soil and if animal manures applied optimally an outstanding effect on the growth and yield of crops remains visible (Makinde and Ayoola 2008). Manures withstand cropping system through improved nutrient recycling (Powell et al. 2002). Goat dung manure also exhibited significant influence on nutrient availability in soil, nutrient status, depicted as an effective source of N, P, K, Ca, Mg, and organic matter for promotion of healthy pepper production. Samuel et al. (2003), observed in pepper crop productivity (Awodun et al. 2007), improved yield of

4 Cattle Dung Manure Microbiota as a Substitute …

87

okra, amaranthus, celosia, and maize (Odiete et al. 1999; Ojeniyi and Adegboyeaga 2003a) by adding organic manure. Kaur et al. (2005) also reported that organic manure increased the soil of organic C, N, P, and K, thus highlighting its importance in tropical farmland. Poultry manure, a good source of organic matter, played a vigorous role in soil fertility enhancement, as well as furnishing micronutrients for crop production. Earlier, Amiri, and Fallahi (2009) observed that the application of poultry manure improved the availability of the mineral in soil, hence assisted to facilitate nutrient uptake in the plant. Nowadays improper utilized poultry waste becomes a foremost problem, thereby polluting the environment. Since poultry farm holders use concentrates for feeding as a result of which the excreta cannot be used as fuel, except as a good source of manure in the crop fields (Zake et al. 2010). Olasekan (2018), observed the effect of poultry manure on soil properties, growth and fruit yield of tomato. Adekiya et al. (2019) reported the effect of poultry manure to improved soil physical and chemical properties, leaf nutrient concentrations, and yield components of radish.

4.7 Dung Applications: Success and Bottleneck It reminds us of an era of the late 1960s that was the food security for the everincreasing population, particularly in India. Scientists started using agrochemicals for productivity enhancement of some major crops such as wheat and rice. Later, it was realized that the application of chemical fertilizers not only injurious to humans but also have adverse consequences on the soil water ecosystem. Soil productivity maintenance is a major constraint of the tropical agriculture system. Low soil fertility was one of the greatest biophysical constraints to the production of crops across the world (Ajayi 2007). Tropical soils are unfavorably affected by suboptimal soil fertility and erosion, instigating deterioration of the nutrient status, and changes in soil organism populations (Akande et al. 2010). Scientifically, soil amended with animal dung proved a very good source for sustaining crop production and increasing the beneficial microbial population in the soil (Raj et al. 2014). All animal origin wastes such as farmyard manure, poultry manure, and cattle/cow dung have dual advantages being cheap and contain nutrients that support healthier root development leading to higher crop yield (Abou El-Magd et al. 2005). Chemical fertilizers are costly and are not easily available to the majority of the smallholder farmers, particularly in hilly states of India having marginal farm income, hence compelled farmers toward the organic sources to substitute soil nutrients. Besides organic resources are frequently projected as an alternative to commercial chemical fertilizers. In this scenario, dung is easier and cheaper to transport, handling, and storage. It has multiple benefits due to the balanced supply of nutrients, including micronutrients, increased soil nutrient availability due to soil microbial activity. Such activities occur due to various biochemical reactions involved in soil respiration and another bioactivity. The alteration of pH, temperature resulted in a change in soil structure and function (Pettersson and Bååth 2003; Samuel et al. 2003) (Fig. 4.1).

88

S. Dhiman et al.

Fig. 4.1 Merits of dung over chemical fertilizers

The decomposition of harmful elements, soil structure improvements, root development, and increased soil water availability are added advantages (Zingore et al. 2008). On the other hand, chemical fertilizer reduces crop protein content, carbohydrate quality, etc., (Marzouk & Kassem 2011) while excess potassium content on chemically overfertilized soil quality further decreases several components of vegetable and crop (vitamin C, carotene content, and antioxidant compounds) as observed by Toor et al. (2006). Whereas, vegetables and fruits grown-up on overfertilized soils (chemically) are more disposed to insecticidal attacks and disease (Karungi et al. 2006) and crops become more vulnerable to abiotic stresses. Dungbased manures have a long-term impact on soil, maintaining fertility for a longer time (Table 4.6). Scientists also worked upon Physicochemical properties with special reference to dung properties such as total solid content, moisture content, dry matter content, etc. It was noticed that the total solids (TS) content in the dung obtained after the evaporation of water comprises neither too high nor too low (around 12%) as the concentration of TS contents affects the survival of microorganisms (Gunnerson and Stuckey 1986). Earlier, Garg et al. (2005) reported pH 8.4 in the case of buffalo dung whereas Murphy (2006) found that manure pH was typically neutral (7.0) to alkaline. Due to the fact, Schnurer and Jarvis (2010) stated and enumerated a maximum number

4 Cattle Dung Manure Microbiota as a Substitute … Table 4.6 Comparison of soil properties with addition of dung

Characteristics

89 Dung

Dung+Soil (1:3)

pH

5.1

6.5

OC (%)

37.1

40.2

N (ppm)

40.1

86.3

P (kg/ha)

121

135.3

K (g/kg)

0.276

0.997

Moisture (%)

68

71

Lab unpublished data. Values are mean of three replicates

of microorganisms prefer a neutral pH range 7.0–7.5 (Schnurer and Jarvis 2010). The optimum moisture content remained in the range of 60–95% (Demetriades 2008). Hollmann et al. (2008) examined the dung obtained from Holstein and Jersey cows produced 5.80 kg/d of total solids. Similarly, Wang et al. (2007) estimated that 16.7% dry matter content whereas Gautam et al. (2016) obtained the average dry matter percentage in cow and buffalo dung in the range of 38% and 14%, respectively. The manure or compost equally important for plant-soil-microbe interactions and is safe for health and environment. To achieve enhanced environmental conditions, advocating the use of organic materials is indispensable (Bayu et al. 2006). Studies revealed the significant effect of compost pig manure and cattle dung on the enhancement of yield and quality leafy vegetables like spinach, lettuce, and cabbage (Yamazaki and Roppongi 1998). Sharma and Bhalla (1995) also reported enhanced growth and yield in okra with the application of fermented dung and slurry. In the last decade, Jawale et al. (2009) obtained the highest yield and quality of spinach with use of dung, urine slurry followed by sheep, goat, and buffalo. The improper use of dung needs to be stopped and should only be applied in the farmland so that the productivity and sustainability of soil could be maintained for the production capacity of food treasure (Bhattacharyya et al. 2007). Various workers reported advantageous effects of organic manure on plant-soil properties (Adeleye et al. 2010), with reference to bulk density, water holding capacity, and other soil physical properties (Fawole et al. 2010). Effect of organic manure enhanced aeration, drainage, and friability of the soil (Schjønning et al. 1994; Maheswarappa et al. 1999; De Silva and Cook 2003). The organic matter of manure facilitates plants to use the nutrients for a long time, due to its slow decomposition and reduces the loss of what is not utilized by the plants (Bhandari et al. 2002). This property leads organic manure for sustained crop production through better nutrient recycling and improvement of soil physical attributes, environmental conditions, and public health (El-Shakweer et al. 1998; Ojeniyi 2000; Maritus and Vleic 2001). In fact, amendment of organic manures in soil attained maximum and sustainable crop yield, besides enhancing soil fertility and productivity (Sanwal et al. 2007). Due to abundance, cattle and swine manure have been extensively used in agricultural fields in India. The composted form of these manure proved better in comparison to that of fresh manure because it eradicates the risk of loss of nitrogen by

90

S. Dhiman et al.

leaching and surface runoff, suppress soil-borne pathogens, increase soil organic matter, and to mitigate greenhouse gas emissions (Darby et al. 2004; Evanylo et al. 2008; Escribano 2016). Mbah (2006) observed that poultry, cow dung, and swine manure increased uptake of K, Ca, and Mg in maize. The addition of cow dung in the soil enhances the physical and chemical properties of soil by increasing its fertility (by adding nutrients), moisture-absorbing capacity, etc. If used in clay soils where water logging is a problem cow dung increases the porosity of soil but if the soil is porous not retaining the water such as sandy soil, then cow dung acts as water holding carriers (Gbenou et al. 2017), increases the geotechnical properties like bulk density, dry density, porosity, infiltration (Ekwue et al. 2009). Cow dung is an important source of organic matter in soils, especially in small-scale farming systems across the globe. For degraded soil, the soil’s physical properties are usually destroyed, because the organic matter has declined in the soils. Thus, cow dung/organic has a significance in increasing the soils buffering capacity, to regulate soil acidity. This reduces soil aggregation and soil bulk density, water holding capacity, and nutrient holding capacity. The presence of organic matter ensures that soil biological properties are optimally functional in soil system. Increase the water holding capacity of soil corresponds to increase the growth of the plant and sustain productivity as stated by various workers (Zheng et al. 2018). Replacing chemical fertilizers with organic manure reduced the environmental pollution and also minimizes organic waste (Ram et al. 2007). Application of organic manure improves chlorophyll content in leaf and N, P, K, Fe, Zn, and Mn contents in olive trees (Abdel-Nasser and Harash 2001; Abou El-Khashab et al. 2005), and enhanced vegetative growth parameters of guava tree (Ram et al. 2007). In case of poultry manure, increased yield, quality production, and nutrient uptake were recorded in mustard (Zamil et al. 2004) and Foeniculum vulgare (Dhiman et al. 2019). Earlier, Sobulo and Babalola (1992) also studied the role of poultry dropping and cattle dung on the growth and enhancement of maize root growth. Continuous use of cattle manure increases crop yields with fertilizer phosphorus (Reddy et al. 2000). Ghosh et al. (2004) checked the comparative effect of cattle manure, poultry manure, phosphor-compost, and fertilizer-NPK on three cropping systems in vertisols of semi-arid tropics and concluded their significance on nutrient management in plants. Cattle manure has been recognized as an effective strategy to maintain an adequate supply of organic matter in the soil. It was also observed that animal manure improves the physical and chemical conditions of soil along with the enhancement in crop performance (Ikpe and Powell 2002; Powell et al. 1998). Various workers revealed the significance of poultry, cattle, goat, sheep, and pig manure to improve soil fertility and crop yield (Adeniyan and Ojeniyi 2003; Ojeniyi and Adegboyega 2003b). Nyakatawa et al. (2001) also reported that the application of organic manure increased yield of crops, besides maintaining soil fertility after adopting appropriate tillage practices. The addition of compost into the soil tends to improve nutrients and water holding capacity (Arslan et al. 2008; Vakili et al. 2015). Ewulo (2005) examined the relative effect of poultry and cattle dung on the chemical properties of soil. Adediran et al. (2003) studied different kinds of manures and reported high nutrient contents in

4 Cattle Dung Manure Microbiota as a Substitute …

91

poultry manure which increased the yield of tomato. Akande and Adediran (2004) also examined the beneficial effect of manure on tomato and dry matter yield, soil pH, N, P, K, Ca, and Mg and nutrient uptakes. Later, Aluko and Oyedele (2005) studied the effects of organic waste on the physical properties of soil and reported the significance of animal manure on soil density and porosity. Among all organic manure sources, poultry manure was found to be concentrated maximally concerning nutrient content (Lombin et al. 1991), since it mineralizes more rapidly than other animal manure, thereby rapidly releasing nutrients for plant uptake and utilization (Brady and Weils 1999). Senjobi et al. (2010) reported the growth-promoting effect of poultry, plant, and sheep/goat manures in the enhancement of vegetable growth parameters. Similarly, increment in chlorophyll content and grain yield of maize and sorghum was also observed by Amujoyegbe et al. (2007). Although, the application of a supra-optimal quantity of fertilizer proved a suitable strategy for optimizing high productivity (Kumar et al. 2009; Calabi-Floody et al. 2018) quality food nutrients is obtained only by the application of organic manure including dung.

4.8 Effect of the Blending of Organic and Inorganic Fertilizers On the contrary, amendments of organic manure alone may not offer satisfactory nutrient supply (Palm et al. 1997; Gentile et al. 2011; Bedada et al. 2014). To achieve the demand, amendment of a combination of organic and inorganic resources viz. (ISFM, Integrated Soil Fertility Management) outsourced resulting in better yield and nutrient storage (Bedada et al. 2014; Ewusi-Mensah et al. 2015) For instance, a combination of cow dung with NPK, significantly increased the yield of potato tuber (Onwudike 2010). Earlier, combined application of NPK and compost (50 + 50%) influenced the increment in carbohydrate content (Haukioja et al. 1998) and enhancement of tomato and cucumber yield (Marzeh et al. 2012). EI-Sherbeny et al. (2005) observed application of compost showed a remarkable increase in plant pigments and total carbohydrate in Sideritis montana. Such a combination revealed more cobs to borne and increase the crop yield in maize (Ayoola and Makinde 2008; Bedada et al. 2014). The combination of inorganic and organic manure boosted soil organic matter, phosphate availability, exchangeable ions, effective cation exchange capacity, and soil pH (Onwudike 2010) required to increase soil fertility. Earlier, Moyin-Jesu (2007) exhibited that a combination of plant and animal wastes with NPK (15:15:15) increased uptake of N, P, K, Ca, and Mg in coffee seedlings. Earlier, Chand et al. (2006) reported that the mixed use of NPK and organic manure increased N, P, K in soil and the growth of Mentha arvensis and Brassica juncea. Recently, Francioli et al. (2016) observed the integrated use of extremely low dosage of chemical fertilizer along with farmyard manure. The increased soil organic matter, total nitrogen content, and soil microbial biomass carbon (MBC) and crop yield were recorded. Application

92

S. Dhiman et al.

of NPK + cattle manure and NPK + swine manure increased total organic carbon (TOC), total nitrogen, and crop yield, in comparison to NPK fertilization (Li et al. 2017). Further, the combined application of organic (cattle manure compost) and inorganic (NPK) fertilization increased soil organic carbon (SOC), total nitrogen and also improved the bacterial community involved in the breakdown of complex organic matter and in transferring soil carbon, nitrogen, and phosphorus transformations (Li et al. 2019). Some of the properties of nature of organic and inorganic fertilizers are given in Table 4.7. The use of plant nutrients from inorganic fertilizer materials, i.e. N, P2 O5, and K2 O has increased dramatically and the most remarkable increase has been noted in N, P, K, and S. But, the nonrenewable nature of fertilizer raw material is a disadvantage revealed by lack of nitrogen through denitrification. Dung can meet out the plantmineral requirements in the form of compost as nutrient supply occurs via intake from the soil. When the dung was mixed with grassland soil under controlled conditions the size of the soil microbial biomass, respiration rate also increased as supported by Lopes et al. (2010). It is now established that the specific respiration was higher in treated with cattle dung in comparison to that of non-amended soil always, hence acted as good resource for maintaining the status of agro-productivity and improves the beneficial microbial population of soil (Lovell and Jarvis 1996). In few countries, buffalo farms produce extra manure, i.e. dung (Nanda and Nakao 2003) resulting increase in a treasured source of biogas, instead of representing a waste, due to its optimal C: N ratio of about 30 (Yasin and Wasin 2011). Huws et al. (2012) investigated the effects of nourishing sorghum as opposed to maize on rumen microbial diversity. Carillo et al. (2012) studied the microbial diversity and analyzed the community on the manure and also reported the isolation of different eubacteria Table 4.7 Comparison of organic and inorganic fertilizers Basis

Organic

Inorganic

Meaning

It is a natural material, obtained by decaying plant and animal waste, that can apply to the soil to enhance its fertility

It is a human-made or synthetic substance, that can be added to the soil to improve its fertility and increase the productivity

Preparation

Prepared in fields

Products of factories

Humus

It provides humus to the soil

It does not provide humus to the soil

Nutrients

Comparatively less rich in plant nutrients

Rich in plant nutrients

Absorption

Slowly absorbed by plants

Quickly absorbed by plants

Side effect

There is no side effect; in fact it It causes harm to the living organisms, improves the physical condition of soil disturb soil ecology and pollute ground water

Safety

Safe

Harmful

Longivity

Sustainable

Non-sustainable

Cost

Cost effective

Expensive

4 Cattle Dung Manure Microbiota as a Substitute …

93

microbial communities, after anaerobic fermentation in batch reactors, as affected by the different fermentation conditions.

4.9 Dung in Agrobiological Practices Dung came into focus as a potential antimicrobial agent (Chitnis et al. 2000) against multidrug resistant and Vancomycin resistant bacteria causing human infections. Evidence showed that fresh dung and urine have antifungal and antiseptic properties due to the secretion of some of the antimicrobial metabolites (Nene 2003). Certain phytopathogenic fungi such as Fusarium solani, F. oxysporum, and Sclerotinia sclerotiorum also suppressed by antifungal nature of dung (Basak et al. 2002). Bacterial blight disease of rice was found to be controlled by the spray of dung extract and acts as effective as penicillin, paushamycin, and streptomycin (Mary et al. 1986). The research revealed that Aspergillus niger, Trichoderma harzianum, Bacillus cereus, and Bacillus subtilis inhabiting in dung reduce the growth of Sclerotium rolfsii, F. oxysporum, Pythium aphanidermatum, Helminthosporium maydis, and Rhizoctonia solani. On the other hand, a number of antibiotic resistant strains were also isolated from dung which may act as antibiotic resistant markers in rhizosphere biology (David and Odeyemi 2007). Dung is considered as an integral component of most of the biodynamic preparations and serves as a source of inoculum of beneficial microorganisms (Dhiman et al. 2019). The biodynamic products contain macro and micronutrients, amino acids, and growth-promoting substances like IAA, gibberellins, and beneficial microorganisms. The beneficial effects of biodynamic preparations have been reported on lentil and wheat (Carpenter-Boggs et al. 2000). Biodynamic sprays increased the yields of cereals and vegetables (Raupp and Koenig 1996). In addition, spraying a 3% solution of biodynamic products prepared by dung along with soil application of biogas slurry improved the yields of maize and sunflower (Somasundaram et al. 2007). In agricultural practices, it utilizes as manure because of the presence of humic compounds thus played an important role to increase crop growth (Girija et al. 2013). Low C: N ratio in dung manure is an indication of good source of protein for microbes resides in it and involved in the decomposition of organic matter (Adegunloye et al. 2007). From ancient times, numbers of formulations were prepared either alone or in combination with herbal, animal, or mineral origin drugs (Sathasivam et al. 2010). Farm animals such as cows, bullocks, and milk buffaloes provide dung and urine to enrich the soil, while crop residues and fodder form the bulk of the feed for these animals (Kesavan and Swaminathan 2008). Studies revealed that dung remained the most important source of bio-fertilizer and at the same time urine, horn, and dead bodies can be the sources for effective bio-fertilizer. In mixed farming systems, most livestock products are derivatives of animals that fed on local resources such as crop residues, pasture, fodder trees, and shrubs. In India, farming and agricultural cultivation is used to be done with animal dung and serving as manure as per the traditional age-old system. There are a variety

94

S. Dhiman et al.

of animal dung and urine products, which can be used as fertilizers and pest repellent, respectively (Katzen 1978). Recently, in India, dung soaps, paper, and dyes have been introduced due to beneficial properties toward skin infections and other dermal diseases (https://www.amarujala.com/business/business-diary/nitingadkari-launches-soap-made-from-cow-dung-and-bamboo-bottles). These dungbased commercial products and their microbiota are widespread and being augmented for the sustainable plant-soil ecosystem. Acknowledgements The authors gratefully acknowledges the Department of Botany and Microbiology, Gurukul Kangri University, Haridwar for providing all the infrastructural facilities to carry out this research.

References Abbasi T, Tauseef SM, Abbasi SA (2012) Anaerobic digestion for global warming control and energy generation—an overview. Renew Sust Ene Rev 16(5):3228–3242 Abdel-Nasser G, Harash MM (2001) Studies on some plant growing media for olive cultivation in sandy soils under Siwa oasis conditions. J Adv Agric Res 6:487–510 Abdulkareem AS (2005) Refining biogas produced from biomass: an alternative to cooking gas. Leonardo J Sci 7:1–8 Abou El-Khashab AM, Abou Taleb SA, Said WT (2005) Aggezi and Koroneki olive trees as affected by organic and bio-fertilizers, calcium citrate and potassium. Arab Univ J Agric Sci Ain Shams Univ 13:419–440 Abou El-Magd MM, El-Bassiony AM, Fawzy ZF (2006) Effect of organic manure with or without chemical fertilizers on growth, yield and quality of some varieties of Broccoli plants. J Appl Sci Res 2(10):791–798 Abou El-Magd MM, Hoda AM, Fawzy ZF (2005) Relationship, growth and yield of broccoli with increasing N, P or K ratio in a mixture of NPK fertilizers. Annal Agri Sci Mosh 43(2):791–805 Adediran JA, Taiwo LB, Sobulo RA (2003) Organic wastes and their effect on tomato (Lycopersicum esculentus) yield. Afr Soil 33:99–116 Adegunloye DV, Adetuyi FC, Akinyosoye FA, Doyeni MO (2007) Microbial analysis of compost using cowdung as booster. Pak J Nut 6(5):506–510 Adekiya AO, Agbede TM, Aboyeji CM, Dunsin O, Simeon VT (2019) Effects of biochar and poultry manure on soil characteristics and the yield of radish. Sci Hortic 243:457–463 Adeleye EO, Ayeni LS, Ojeniyi SO (2010) Effect of poultry manure on soil physico-chemical properties, leaf nutrient contents and yield of yam (Dioscorea rotundata) on Alfisol in Southwestern Nigeria. J Amer Sci 6(10):871–878 Adeniyan ON, Ojeniyi SO (2003) Comparative effectiveness of different levels of poultry manure with NPK fertilizer on residual soil fertility, nutrient uptake and yield of maize. Moor J Agri Res 4(2):191–197 Afazeli H, Jafari A, Rafiee S, Nosrati M (2014) An investigation of biogas production potential from livestock and slaughterhouse wastes. Renew Sustain Energy Rev 34:380–386 Ahmad AT, Bello IU, Jibril SM, Kolawole OS, Ogah JJ, Daniel S (2019) Comparative evaluation of the effects of organic and inorganic fertilizers on the vegetative growth of spleen amaranth (Amaranthus dubius L). J Appl Sci Environ Manag 23(2):359–363 Ajayi OC (2007) User acceptability of sustainable soil fertility technologies: lessons from farmers’ knowledge, attitude and practice in Southern Africa. J Sustain Agri 30(3):21–40

4 Cattle Dung Manure Microbiota as a Substitute …

95

Akande MO, Adediran JA (2004) Effects of terralyt plus fertilizer on growth nutrients uptake and dry matter yield of two vegetable crops. Moor J Agric Res 5(2):12–107 Akande MO, Oluwatoyinbo FI, Makinde EA, Adepoju AS, Adepoju IS (2010) Response of okra to organic and inorganic fertilization. Nature Sci 8(11):261–266 Akinde SB, Obire O (2008) Aerobic heterotrophic bacteria and petroleum-utilizing bacteria from cow dung and poultry manure. World J Microbiol Biotechnol 24(9):1999–2002 Aluko OB, Oyedele DJ (2005) Influence of organic incorporation on changes in selected soil physical properties during drying of a Nigerian alfisols. J Appl Sci 5(2):357–362 Amiri ME, Fallahi E (2009) Impact of animal manure on soil chemistry, mineral nutrients, yield, and fruit quality in ‘Golden Delicious’ apple. J Plant Nutr 32(4):610–617 Amujoyegbe BA, Opabode JT, Olayinka A (2007) Effect of organic and inorganic fertilizer on yield and chlorophyll content of maize (Zea mays L) and Sorghum (Sorghum bicolour L Moench). Afr J Biotech 6(16):1869–1873 Andaluri G, Suri RP, Kumar K (2012) Occurrence of estrogen hormones in biosolids, animal manure and mushroom compost. Environ Monit Assess 184(2):1197–1205 Arora NK, Panosyan H (2019) Extremophiles: applications and roles in environmental sustainability. Env Sust 2:217–218 Arslan EI, Obek E, Kirba S, Pek U, Topal M (2008) Determination of the effect of compost on soil microorganisms. Int J Sci Technol 3(1):151–159 Aruna Olasekan A (2018) Legume mulch materials and poultry manure affect soil properties, and growth and fruit yield of tomato. Agriculturae Conspectus Scientificus 83(2):161–167 Awodun MA, Omonijo LI, Ojeniyi SO (2007) Effect of goat dung and NPK fertilizer on soil and leaf nutrient content, growth and yield of pepper. Inter J Soil Sci 2(2):142–147 Ayoola OT, Makinde EA (2008) Performance of green maize and soil nutrient changes with fortified cow dung. Afr J Plant Sci 2(3):19–22 Ayuso MA, Pascal JA, Garcia C, Hernandez T (1996) Evaluation of urban waste for agricultural use. Soil Sci Plant Nutr 42(1):105–111 Bandyopadhyay KK, Misra AK, Ghosh PK, Hati KM (2010) Effect of integrated use of farmyard manure and chemical fertilizers on soil physical properties and productivity of soybean. Soil Tillage Res 110(1):115–125 Basak AB, Lee MW, Lee TS (2002) Inhibitive activity of cow urine and cow dung against Sclerotinia sclerotiorum of cucumber. Mycobiol 30(3):175–179 Bayu W, Rethman NFG, Hammers PS, Alemu G (2006) Effects of farmyard manure and inorganic fertilizers on sorghum growth, yield and Nitrogen use in a semiarid area of Ethiopia. J Plant Nutr 29(2):391–407 Bedada W, Karltun E, Lemenih M, Tolera M (2014) Long-term addition of compost and NP fertilizer increases crop yield and improves soil quality in experiments on smallholder farms. Agric Ecosyst Environ 195:193–201 Bekele K, Hager H, Mekonnen K (2013) Woody and non-woody biomass utilization for fuel and implications on plant nutrients availability in the Mukehantuta watershed in Ethiopia. Afri Crop Sci J 21(3):625–636 Bernal MP, Alburquerque JA, Moral R (2009) Composting of animal manures and chemical criteria for compost maturity assessment. A review. BioresTechnol 100(22):5444–5453 Bhandari AL, Ladha JK, Pathak H, Padre AT, Dawe D, Gupta RK (2002) Yield and soil nutrient changes in a long-term rice-wheat rotation in India. Soil Sci Soci America J 66(1):162–170 Bhattacharyya R, Chandra S, Singh RD, Kundu S, Srivastva AK, Gupta HS (2007) Long-term farmyard manure application effects on properties of a silty clay loam soil under irrigated wheat– soybean rotation. Soil Tillage Res 94(2):386–396 Brady C, Weils RR (1999) Nature and properties of Soil, Twelfth edn. Prentice Hall, New Delhi, pp 74–114 Calabi-Floody M, Medina J, Rumpel C, Condron LM, Hernandez M, Dumont M, de la Luz Mora M (2018) Smart fertilizers as a strategy for sustainable agriculture. Adv Agron Acad Press 147:119– 157

96

S. Dhiman et al.

Carillo P, Carotenuto C, Cristofaro F, Kafantaris I, Lubritto C, Minale M, Woodrow P (2012) DGGE analysis of buffalo manure eubacteria for hydrogen production: effect of pH, temperature and pretreatments. Mol Biol Rep 39(12):10193–10200 Carotenuto C, Guarino G, Morrone B, Minale M (2016) Temperature and pH effect on methane production from buffalo manure anaerobic digestion. Inter J Heat Technol 34(2):425–429 Carpenter-Boggs L, Reganold JP, Kennedy AC (2000) Biodynamic preparations: short term effect on crops, soils, and weed populations. Am J Altern Agric 15(3):110–118 Chadwick D, Wei J, Yanan T, Guanghui Y, Qirong S, Qing C (2015) Improving manure nutrient management towards sustainable agricultural intensification in China. Agri Eco Environ 209:34– 46 Chand S, Anwar M, Patra DD (2006) Influence of long-term application of organic and inorganic fertilizer to build up soil fertility and nutrient uptake in mintmustard cropping sequence. Comm Soil Sci Plant Anal 37(2):63–76 Charbonneau DM, Meddeb-Mouelhi F, Boissinot M, Sirois M, Beauregard M (2012) Identification of thermophilic bacterial strains producing thermotolerant hydrolytic enzymes from manure compost. Ind J Microbiol 52(1):41–47 Chauhan HK, Singh K (2012) Effect of binary combinations of buffalo, cow and goat dung with different agro wastes on reproduction and development of earthworm Eisenia fetida (Haplotoxida: Lumbricidae). World J Zool 7(1):23–29 Chawla OP (1986) Advances in biogas technology. Adv Biogas Technol 136 Chen X, Li Z, Liu M, Jiang C, Che Y (2015) Microbial community and functional diversity associated with different aggregate fractions of a paddy soil fertilized with organic manure and/or NPK fertilizer for 20 years. J Soils Sediments 15(2):292–301 Chitnis V, Patil S, Kant R (2000) Hospital effluent: a source of multiple drug resistant bacteria. Curr Sci 79:83–89 Chynoweth DP, Turik CE, Owens JM, Jerger DE, Peck MW (1993) Biochemical methane potential of biomass and waste feed stocks. Biomass Bioenerg 5(1):95–111 Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochemis 42(5):669–678 Croos AMB, Rajendran S, Ranganathan K (2019) Isolation of a cellulase producing Bacillus cereus from cow dung and determination of the kinetic properties of the crude enzyme. J Nat Sci Found Sri Lanka 47(2). Darby HM, Stone AG, Dick R (2004) Compost and manure mediated impacts on soil borne pathogens and soil quality. Soil Sci Soc Am J 70(2):347–358 Das S, Jeong ST, Das S, Kim PJ (2017) Composted cattle manure increases microbial activity and soil fertility more than composted swine manure in a submerged rice paddy. Front Microbiol 8:1702 David OM, Odeyemi AT (2007) Antibiotic resistant pattern of environmental isolates of Listeria monocytogenes from Ado-Ekiti. Nigeria Afr J Biotechnol 6(18):2135–2139 De Silva ASH, Cook HF (2003) Soil physical conditions and physiological performance of cowpea following organic matter amelioration of sandy substrates. Comm Soil Sci Plant Anal 34:1039– 1058 Demetriades P (2008) Thermal pre-treatment of cellulose rich biomass for biogas production. Swedish Uni Agri Sci ISSN:1101-8151 Dhiman S, Baliyan N, Maheshwari DK (2020) Buffalo dung-inhabiting bacteria enhance the nutrient enrichment of soil and proximate contents of Foeniculum vulgare Mill. Arc Microbiol 1–10 Dhiman S, Dubey RC, Maheshwari DK, Kumar S (2019) Sulfur-oxidizing buffalo dung bacteria enhance growth and yield of Foeniculum vulgare Mill. Can J Microbiol 65(5):377–386 Eastman BR, Kane PN, Edwards CA, Trytek L, Gunadi B, Stermer AL, Mobley JR (2001) The effectiveness of vermiculture in human pathogen reduction for USEPA biosolids stabilization. Compost Sci Utilization 9:38–49

4 Cattle Dung Manure Microbiota as a Substitute …

97

Eghball B, Wienhold BJ, Gilley JE, Eigenberg RA (2002) Mineralization of manure nutrients. J Soil Water Conserv 57(6):470–473 EI-Sherbeny SE, Khalil MY, Naguib NY (2005) Influence of compost levels and suitable spacing on the productivity of Sideritis Montana L. plants recently cultivated under Egyptian condition. Bull Fac Agric Cairo Univ 56:373–392 Ekwue EI, Bharat C, Samaroo K (2009) Effect of soil type, peat and farmyard manure addition, slope and their interactions on wash erosion by overland flow of some Trinidadian soils. Biosyst Eng 102(2):236–243 El-Shakweer MHA, EL-Sayad EA, Ewees MSA (1998) Soil plant analysis as a guide for interpretation of the improvement efficiency of organic conditions add to different solid in Egypt. Comm Soil Sci Plant Ana 29:2067–2088 Ermawati R, Morimura S, Tang Y, Liu K, Kida K (2007) Degradation and behavior of natural steroid hormones in cow manure waste during biological treatments and ozone oxidation. J Biosci Bioeng 103(1):27–31 Escribano, AJ (2016) Organic livestock farming—challenges, perspectives, and strategies to increase its contribution to the agrifood system’s sustainability—a review. In: Konvalina P (ed) Organic farming—a promising way of food production, 1st edn, pp 229–260 Evanylo G, Sherony C, Spargo J, Starner D, Brosius M, Haering K (2008) Soil and water environmental effects of fertilizer-, manure-, and compost based fertility practices in an organic vegetable cropping system. Agric Ecosyst Environ 127:50–58 Ewulo BS (2005) Effect of poultry dung and cattle manure on chemical properties of clay and sandy clay loam soil. J Anim Vet Adv 4(10):839–841 Ewulo BS, Hassan KO, Ojeniyi SO (2007) Comparative effect of cow dung manure on soil and leaf nutrient and yield of pepper. Inter J Agri Res 2(12):1043–1048 Ewusi-Mensah N, Logah V, Akrasi EJ (2015) Impact of different systems of manure management on the quality of cow dung. Commun Soil Sci Plant Anal 46:137–147 Fawole OB, Ajayi TJ, Aduloju MO, Olaniyan JO (2010) The use of parkia husk and melon wastes as soil amendments. J Agric Res Dev 9(2) Francioli D, Schulz E, Lentendu G, Wubet T, Buscot F, Reitz T (2016) Mineral vs. organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long term fertilization strategies. Front Microbiol 7:14–46 Fuentes B, Jorquera M, de la Luz Mora M (2009) Dynamics of phosphorus and phytate-utilizing bacteria during aerobic degradation of dairy cattle dung. Chemosphere 74(2): 325–331 Garg AK, Mudgal V (2007) Organic and mineral composition of Gomeya (cow dung) from Desi and crossbred cows a comparative study. Int J Cow Sci 3:1–2 Garg VK, Chand S, Chhillar A, Yadav A (2005) Growth and reproduction of Eisenia Foetida in various animal wastes during vermicomposting. Appl Ecol Environ Res 3(2):51–59 Gattinger A, Höfle MG, Schloter M, Embacher A, Böhme F, Munch JC, Labrenz M (2007) Traditional cattle manure application determines abundance, diversity and activity of methanogenic Archaea in arable European soil. Env Microbiol 9(3):612–624 Gautam S, Edwards R, Yadav A, Weltman R, Pillarsetti A, Arora NK, Smith KR (2016) Probe-based measurements of moisture in dung fuel for emissions measurements. Energy Sustain Dev 35:1–6 Gbenou B, Adjolohoun S, Ahoton L, Houndjo DBM, Saidou A, Houinato M, Sinsin AA (2017) Animal dung availability and their fertilizer values in a context of low soil fertility conditions for forage seed and crops production in Benin (West Africa). Am J Agric Res 2(12):1–16 Gentile R, Vanlauwe B, Chivenge P, Six J (2011) Trade-offs between the shortand long-term effects of residue quality on soil C and N dynamics. Plant Soil 338:159–169 Gholamhoseini M, Ghalavand A, Khodaei-Joghan A, Dolatabadian A, Zakikhani H, Farmanbar E (2013) Zeolite-amended cattle manure effects on sunflower yield, seed quality, water use efficiency and nutrient leaching. Soil Tillage Res 126:193–202 Ghosh PK, Bandyopadhyay KK, Manna MC, Mandal KG, Misra AK, Hati KM (2004) Comparative effectiveness of cattle manure, poultry manure, phosphocompost and fertilizer-NPK on

98

S. Dhiman et al.

three cropping systems in vertisols of semi-arid tropics, dry matter yield, nodulation, chlorophyll content and enzyme activity. Biores Technol 95(1):85–93 Giannattasio M, Vendramin E, Fornasier F, Alberghini S, Zanardo M, Stellin F, Concheri G, Stevanato P, Ertani A, Nardi S, Rizzi V, Piffanelli P, Spaccini R, Mazzei P, Piccolo A, Squartini A (2013) Microbiological features and bioactivity of a fermented manure product (preparation 500) used in biodynamic agriculture. J Microbiol Biotech 23:644–651 Girija D, Deepa K, Xavier F, Antony I, Shidhi PR (2013) Analysis of cow dung microbiota—a metagenomic approach. Indian J Biotechnol 12:372–378 Güllert S, Fischer MA, Turaev D, Noebauer B, Ilmberger N, Wemheuer B, Grundhoff A (2016) Deep metagenome and metatranscriptome analyses of microbial communities affiliated with an industrial biogas fermenter, a cow rumen, and elephant feces reveal major differences in carbohydrate hydrolysis strategies. Biotechnol Biofuels 9(1):121 Gulshan AB, Saeed HM, Javid S, Meryem T, Atta MI, Amin-ud-Din M (2013) Effects of animal manure on the growth and development of okra (Abelmoschus esculentus L.). J Agri Bio Sci 8(3):213–219 Gunnerson CG, Stuckey DC (1986) Anaerobic digestion: principles and practices for biogas systems. World Bank technical paper (No. PB-86-194750/XAB). International Bank for Reconstruction and Development, Washington, DC (USA) Haukioja E, Ossipov V, Koricheva J, Honkanen T, Larsson S, Lempa K (1998) Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization. Chemoecol 8:133–139 Hollmann M, Knowlton KF, Hanigan MD (2008) Evaluation of solids, nitrogen, and phosphorus excretion models for lactating dairy cows, american dairy science association. J Dairy Sci 91:1245–1257 Hook SE, Wright ADG, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archaea 1–11 Huws SA, Chiariotti A, Sarubbi F, Carfì F, Pace V (2012) Effects of feeding Mediterranean buffalo sorghum silage versus maize silage on the rumen microbiota and milk fatty acid content. J Gen Appl Microbiol 58:107–112 Ikpe FN, Powell JM (2002) Nutrient cycling practices and changes in soil properties in the croplivestock farming systems of western Niger Republic of West Africa. Nut Cyc Agroeco 62(1):37– 45 Inuwa AB, Maryam YA, Arzai AH, Hafsat YB, Kawo AH, Usman AU, ... Ibrahim KH (2017) Distribution of culturable endophytic bacteria in lemon grass (Cymbopogon citratus). Bayero Journal of Pure and Applied Sciences 10(1):95–98. Jawale SA, More SD, Zade KK, Arbad BK (2009) Effect of dung, urine and slurry of different farm animals on yield and quality of spinach. Inter J Agri Sci 5(2):445–447 Jin Y, Liang X, He M, Liu Y, Tian G, Shi J (2016) Manure biochar influence upon soil properties, phosphorus distribution and phosphatase activities: a microcosm incubation study. Chemosphere 142:128–135 Ju XT, Xing GX, Chen XP, Zhang SL, Zhang LJ, Liu XJ (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci 106:3041–3046 Kala DR, Rosenani AB, Fauziah CI, Thohirah LA (2009) Composting oil palm wastes and sewage sludge for use in potting media of ornamental plants. Malays J Soil Sci 13:77–91 Kalita M, Bharadwaz M, Dey T, Gogoi K, Dowarah P, Unni BG, Saikia I (2015) Developing novel bacterial based bioformulation having PGPR properties for enhanced production of agricultural crops. Indian J Exp Biol 53:56–60 Karungi J, Ekbom B, Kyamanywa S (2006) Effects of organic versus conventional fertilizers on insect pests, natural enemies and yield of Phaseolus vulgaris. Agri Ecosys Environ 115:51–55 Katzen S (1978) U.S. Patent No. 4,078,094. U.S. Patent Trademark Office, Washington, DC

4 Cattle Dung Manure Microbiota as a Substitute …

99

Kaur K, Kapoor KK, Gupta AP (2005) Impact of organic manures with and without mineral fertilizers on soil chemical and biological properties under tropical conditions. J Plant Nutr Soil Sci 168(1):117–122 Kelemu S, Fory P, Zuleta C, Ricaurte J, Rao I, Lascano C. (2011) Detecting bacterial endophytes in tropical grasses of the Brachiaria genus and determining their role in improving plant growth. African Journal of Biotechnology 10(6):965–976 Kemausuor F, Bolwig S, Miller S (2016) Sustainable energy technologies and assessments Kesavan PC, Swaminathan MS (2008) Strategies and models for agricultural sustainability in developing Asian countries. Philos Trans Royal Soc 363:877–891 Kravchenko AN, Snapp SS, Robertson GP (2017) Field-scale experiments reveal persistent yield gaps in low-input and organic cropping systems. Proc Natl Acad Sci 114:926–931 Kumar S, Pandey P, Maheshwari DK (2009) Reduction in dose of chemical fertilizers and growth enhancement of sesame (Sesamum indicum L.) with application of rhizospheric competent Pseudomonas aeruginosa LES4. Eur J Soil Biol 45(4):334–340 Li F, Chen L, Zhang J, Yin J, Huang S (2017) Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front Microbiol 8:187–196 Li F, Cheng S, Yu H, Yang D (2016a) Waste from livestock and poultry breeding and its potential assessment of biogas energy in rural China. J Cle Prod 126:451–460 Li F, Liang X, Niyungeko C, Sun T, Liu F, Arai Y (2019) Effects of biochar amendments on soil phosphorus transformation in agricultural soils. In: Advances in Agronomy. Academic Press, pp 132–172 Li X, Geng X, Xie R, Fu L, Jiang J, Gao L, Sun J (2016b) The endophytic bacteria isolated from elephant grass (Pennisetum purpureum Schumach) promote plant growth and enhance salt tolerance of Hybrid Pennisetum. Biotechnol Biofuels 9(1):190 Lombin LG, Adeputu JA, Ayetade KA (1991) Complementary use of organic manures and inorganic fertilizers in arable crop production. In Proceeding of National organic fertilizer seminar held in October 20th–22nd at University of Ibadan, Ibadan, pp 146–162 Lopes MM, Salviano AAC, Araujo ASF, Nunes LAPL, Oliveira ME (2010) Changes in soil microbial biomass and activity in different Brazilian pastures. Spa J Agri Res 8(4):1253–1259 Lovell RD, Jarvis SC (1996) Effect of cattle dung on soil microbial biomass C and N in a permanent pasture soil. Soil Biol Biochem 28(3):291–299 Maathuis FJ, Diatloff E (2013) Roles and functions of plant mineral nutrients. Plant Min Nutr. Humana Press, Totowa, pp 1–21 Maheshwari DK (2011) Bacteria in agrobiology: crop ecosystems. Springer Science & Business Media, Germany Maheswarappa HP, Nanjappa HV, Hegde MR, Prabhu SR (1999) Influence of planting material, plant population and organic manures on yield and East Indian galangal (Kaempferia galanga), soil physicochemical and biological properties. Ind J Agron 44:651–657 Makinde EA, Ayoola AA (2008) Residual influence of early season crop fertilization and cropping system on growth and yield of cassava. Am J Agri Biol Sci 3(4):712–715 Maritus CHT, Vleic PLG (2001) The management of organic matter in tropical soils. What are the priorities? Nutrient Cycling in Agro Ecosystem 61:1–6 Martinez J, Dabert P, Barrington S, Burton C (2009) Livestock waste treatment systems for environmental quality, food safety, and sustainability. Biores Technol 100(22):5527–5536 Martínez-Hidalgo P, Galindo-Villardón P, Trujillo ME, Igual JM, Martínez-Molina E (2014) Micromonospora from nitrogen fixing nodules of alfalfa (Medicago sativa L.). A new promising Plant Probiotic Bacteria. Scientific Reports 4(1):1–11 Mary CA, Dev VPS, Karunakaran K, Nair NR (1986) Cowdung extract for controlling bacterial blight. Inter Rice Res News 11:19–28 Marzeh GJ, Abdolhossein A, Mehdi HF (2012) Influence of different levels of garden compost (garden wastes and cow manure) on growth and stand establishment of tomato and cucumber in greenhouse condition. Afri J Biotechnol 11:9036–9039

100

S. Dhiman et al.

Marzouk HA, Kassem HA (2011) Improving fruit quality, nutritional value and yield of Zaghloul dates by the application of organic and/or mineral fertilizers. Sci Horticul 127:249–254 Mbah CN (2006) Influence of organic wastes on plant growth parameters and nutrient uptake by maize (Zea mays L.). Nig J Soil Sci 16:104–108 Meena VS, Maurya BR, Bohra JS, Verma R, Meena MD (2013) Effect of concentrate manure and nutrient levels on enzymatic activities and microbial population under submerged rice in alluvium soil of Varanasi. Crop Res 45(1):2–9 Miner JR, Smith RJ (1975) Livestock waste management with pollution control Mohanta MK, Mohua MSA, Islam MS, Fazlul M (2017) Isolation and characterization of amino acid producing bacteria from cow dung. J Microbiol. Biomed Res 3:1–8 Moyin-Jesu EI (2007) Effect of some organic fertilizers on soil and coffee (Coffea arabica L.) chemical composition and growth. Univ Khartoum J Agric Sci 15:52–70 Muhammad and Amusa (2003) In vitro inhibition of growth of some seedling blight inducing pathogens by compost inhibiting microbes. Afr J Biotechnol 2(6):161–164 Murmu K, Swain DK, Ghosh BC (2013) Comparative assessment of conventional and organic nutrient management on crop growth and yield and soil fertility in tomato-sweet corn production system. Aust J Crop Sci 7(11):1617–1626 Murphy S (2006) Manure sampling and analysis. Bull E 306:2006 Mutesasira J, Mukasa-Tebandeke IZ, Wasajja HZ, Nankinga R (2015) Assessing performance of cattle dung and waste cooked foods in producing biogas as single substrate and mixed substrates in Kampala Uganda. J New Developments Chem 2(2):29 Nanda AS, Nakao T (2003) Role of buffalo in the socioeconomic development of rural Asia: current status and future prospectus. Ani Sci J 74:443–447 Nene YL (2003) Crop diseases management practices in ancient, medieval, and premodern India. Asian Agri Hist 7(3):185–201 Nopparat C, Jatupornpipat M, Rittiboon A (2007) Isolation of Phosphate Solubilizing Fungi in soil from Kanchanburi, Thailand. Kmitl Sci Tech J 7:2–11 Nyakatawa EZ, Reddy KC, Sistani KR (2001) Tillage, cover cropping, and poultry litter effects on selected soil chemical properties. Soil Tillage Res 58(1–2):69–79 Odiete I, Ojeniyi SO, Akinola OM, Achor AA (1999) Effect of goat dung on soil chemical composition and yield components of okra, Amaranthus and Maize. In: Proceedings of the 25th Conference of Soil Science Society of Nigeria, Benin, pp 174–184 Ojeniyi SO (2000) Effects of goat manure on the soil physical properties and okra yield in a rainforest area of Nigeria. App Trop Agri 5:20–23 Ojeniyi SO, Adegboyega AA (2003a) Effect of combined use of urea and goat dung manure on celosia. Nig Agri J 34(1):87–90 Ojeniyi SO, Adegboyega AA (2003b) Effect of combined use of urea and goat manure in Celosia. Nigerian Agric J 54:87–90 Onwudike SU (2010) Effectiveness of cow dung and mineral fertilizer on soil properties, nutrient uptake and yield of sweet potato (Ipomoea batatas) in Southeastern Nigeria. Asian J Agric Res 4(3):148–154 Palm CA, Robert JKM, Stephen MN (1997) Combined use of organic and inorganic nutrient sources for soil fertility maintenance and replenishment. In: Hatfield J, Bigham JM, Krai DM, Viney MK (eds) Replenshing soil fertility in Africa. SSSA, Madison Pandey A, Sinha P, Kotay SM, Das D (2009) Isolation and evaluation of a high H2- producing lab isolate from cow dung. Int J Hyd Energy 34(17):7483–7488 Peng G, Wang H, Zhang G, Hou W, Liu Y, Wang ET, Tan Z (2006) Azospirillum melinis sp. nov., a group of diazotrophs isolated from tropical molasses grass. International Journal of Systematic and Evolutionary Microbiology 56(6):1263–1271 Pettersson M, Bååth E (2003) Temperature-dependent changes in the soil bacterial community in limed and unlimed soil. FEMS Microbiol Ecol 45(1):13–21

4 Cattle Dung Manure Microbiota as a Substitute …

101

Piernik A, Hrynkiewicz K, Wojciechowska A, Szyma´nska S, Lis MI, Muscolo A (2017) Effect of halotolerant endophytic bacteria isolated from Salicornia europaea L. on the growth of fodder beet (Beta vulgaris L.) under salt stress. Archives of Agronomy and Soil Science 63(10):1404–1418 Poosakkannu A, Nissinen R, Kytöviita MM (2015) Culturable endophytic microbial communities in the circumpolar grass, D eschampsia flexuosa in a sub-Arctic inland primary succession are habitat and growth stage specific. Environ Microbiol Rep 7(1):111–122 Powell JM, Ikpe FN, Somda ZC, Fernandez-Rivera S (1998) Urine effects on soil chemical properties and the impact of urine and dung on pearl millet yield. Exp Agri 34(3):259–276 Powell JM, Jackson-Smith DB, Satter LD (2002) Phosphorus feeding and manure nutrient recycling on Wisconsin dairy farms. Nutr Cycl Agroecosyst 62(3):277–286 Radha TK, Rao DLN (2014) Plant growth promoting bacteria from cow dung based biodynamic preparations. Ind J microbiol 54(4):413–418 Raj A, Jhariya MK, Toppo P (2014) Cow dung for eco-friendly and sustainable productive farming. Environ Sci 3(10):201–202 Ram RA, Bhriguvanshi SR, Pathak RK (2007) Integrated plant nutrient management in guava (Psidium guajava L.) cv. Sardar Acta Hort 735:345–350 Ramanathan V, Feng Y (2009) Air pollution, greenhouse gases and climate change: global and regional perspectives. Atm Eviron 43(1):37–50 Ranade DR, Nagarwala NN, Dudhbhate JA, Gadre RV, Godbole SH (1990) Ind J Environ Health 32:63–65 Randhawa GK, Kullar JS (2011) Bioremediation of pharmaceuticals, pesticides, and petrochemicals with gomeya/cow dung. ISRN Pharmacol 2011:1–7 Raupp J, Koenig UJ (1996) Biodynamic preparations cause opposite yield effects depending upon yield levels. Biol Agric Hortic 13:175–188 Reckling M, Hecker JM, Bergkvist G, Watson CA, Zander P, Schläfke N, Bachinger J (2016) A cropping system assessment framework—evaluating effects of introducing legumes into crop rotations. Eur J Agron 76:186–197 Reddy DD, Rao AS, Rupa TR (2000) Effects of continuous use of cattle manure and fertilizer phosphorus on crop yields and soil organic phosphorus in a Vertisol. Biores Technol 75(2):113– 118 Rijavec T, Lapanje A, Dermastia M, Rupnik M (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53(6):802–808 Roberts DP, Mattoo AK (2018) Sustainable agriculture-Enhancing environmental benefits, food nutritional quality and building crop resilience to abiotic and biotic stresses. Agri 8(1):8–12 Romano I, Dipasquale L, Orlando P, Lama L, d’Ippolito G, Pascual J, Gambacorta A (2010) Thermoanaerobacterium thermostercus sp. nov., a new anaerobic thermophilic hydrogen-producing bacterium from buffalo-dung. Extremophiles 14(2):233–240 Sadhu S, Saha P, Sen SK, Mayilraj S, Maiti TK (2013) Production, purification and characterization of a novel thermotolerant endoglucanase (CMCase) from Bacillus strain isolated from cow dung. Springer Plus 2(1):10–16 Salter PJ, Berry G, Williams JB (1967) The effect of farmyard manure on matric suctions prevailing in a sandy loam soil. J Soil Sci 18(2):318–328 Samuel RC, Ikepe FN, Osakire JA, Tenkonamo A, Okerter IC (2003) Effects of wood based compost and fertilizer application on the growth and yield of cooking banana hybrid and soil chemical properties in South Eastern Nigeria. Afr J Environ Stud 4:64–68 Sanwal SK, Lakminarayana K, Yadav RK, Rai N, Yadav DS, Mousumi B (2007) Effect of organic manures on soil fertility, growth, physiology, yield and quality of turmeric. Ind J Horti 64(4):444– 449 Sathasivam A, Muthuselvam M, Rajendran R (2010) Antimicrobial activities of cow urine distillate against some clinical pathogens. Global J Pharmacol 4(1):41–44 Sawant AA, Hegde NV, Straley BA, Donaldson SC, Love BC, Knabel SJ, Jayarao BM (2007) Antimicrobial-resistant enteric bacteria from dairy cattle. Appl Environ Microbiol 73:156–163

102

S. Dhiman et al.

Schjønning P, Christensen BT, Carstensen B (1994) Physical and chemical properties of a sandy loam receiving animal manure, mineral fertilizer or no fertilizer for 90 years. Eur J Soil Sci 45(3):257–268 Schnurer A, Jarvis A (2010) Microbiological handbook for biogas plants. Swedish Waste Manage U 2009:1–74 Senjobi BA, Peluola CO, Senjobi CT, Lawal IO, Ande OT, Salami BT (2010) Performance of Cochorus olitorius as influenced by soil type and organic manure amendments in Yewa North Local Government Area. Ogun State Afr J Biotechnol 9(33):5309–5312 Sharma AR, Mittra BN (1991) Effect of differentrates of application of organic and c. J Agric Sci (Cambridge) 117:313–318 Sharma NK, Bhalla PL (1995) Influence of integrated nutrient management on growth, yield and economics in okra (Ablemoshous esculentus L.Monech) Veg Sci 22(1):1–4 Singh S, Moholkar VS, Goyal A (2013) Isolation, identification, and characterization of a cellulolytic Bacillus amyloliquefaciens strain SS35 from rhinoceros dung. ISRN Microbiol, pp 1–6 Sobulo RA, Babalola O (1992) Improved organic fertilizer and soil condition. In: Toward efficiency fertilizer use in Nigeria. Federal Ministry of Agriculture, Water Resources and Rural Development, Lagos, pp 90–110 Somasundaram E, Amanullah MM, Vaiyapuri K, Thirukkumaran K, Sathyamoorthi K (2007) Influence of organic sources of nutrients on the yield and economics of crops under maize based cropping system. J Appl Sci Res 3:1774–1777 Srivastava R, Aragno M, Sharma AK (2010) Cow dung extract: a medium for the growth of pseudomonads enhancing their efficiency as biofertilizer and biocontrol agent in rice. Indian J Microbiol 50(3):349–354 Stajkovi´c O, De Meyer S, Miliˇci´c B, Willems A (2009) Isolation and characterization of endophytic non-rhizobial bacteria from root nodules of alfalfa (Medicago sativa L.). Botanica Serbica 33(1): 107–114 Stanley AM, Stanley DM, Dadu DW, Abah AM (2013) Appraising the combustion of biogas for sustainable rural energy needs. Afr J Environ Sci Technol 7(6):350–357 Sukartono UW, Kusuma Z, Nugroho WH (2011) Soil fertility status, nutrient uptake, and maize (Zea mays L.) yield following biochar and cattle manure application on sandy soils of Lombok, Indonesia. J Tropical Agric 49(1–2): 47–52 Swain MR, Laxminarayana K, Ray RC (2012) Phosphorus solubilization by thermotolerant Bacillus subtilis isolated from cow dung microflora. Agri Res 1(3):273–279 Swain MR, Ray RC (2009) Biocontrol and other beneficial activities of Bacillus subtilis isolated from cowdung microflora. Microbiol Res 164:121–130 Tao R, Liang Y, Wakelin SA, Chu G (2015) Supplementing chemical fertilizer with an organic component increases soil biological function and quality. Appl Soil Ecol 96:42–51 Teo KC, Teoh SM (2011) Preliminary biological screening of microbes isolated from cow dung in Kampar. Afr J Biotechnol 10(9):1640–1645 Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677 Toor RK, Savage GP, Heeb A (2006) Influence of different types of fertilizers on the major antioxidant components of tomatoes. J Food Comp Anal 19:20–27 Vakili M, Zwain HM, Rafatullah M, Gholami Z, Mohammadpour R (2015) Potentiality of palm oil biomass with cow dung for compost production. KSCE J Civil Eng 19:1994–1999 Velazquez E, De Miguel T, Poza M, Rivas R, Rossello-Mora R, Villa TG (2004) Paenibacillus favisporus sp. nov., a xylanolytic bacterium isolated from cow faeces. Inter J Syst Evol Microbiol 54(1):59–64 Verma SK, Kingsley K, Bergen M, English C, Elmore M, Kharwar RN, White JF (2018) Bacterial endophytes from rice cut grass (Leersia oryzoides L.) increase growth, promote root gravitropic response, stimulate root hair formation, and protect rice seedlings from disease. Plant and Soil 422(1-2):223–238

4 Cattle Dung Manure Microbiota as a Substitute …

103

Vijayaraghavan K, Ahmad D, Ibrahim MKB, Herman HNB (2006) Isolation of hydrogen generating microflora from cow dung for seeding anaerobic digester. Inter J Hydr Energ 31(6):708–720 Vijayaraghavan P, Vincent SP, Dhillon GS (2016) Solid-substrate bioprocessing of cow dung for the production of carboxymethyl cellulase by Bacillus halodurans IND18. Waste Manag 48:513–520 Vyas P, Kumar A (2018) Biochemical and molecular characterization of cellulase producing bacterial isolates from cattle dung samples. J Adv Res Biotechnol 2475–4714 Wahyudi A., Cahyanto MN, Soejono M, Bachruddin Z (2010) Potency of lignocell lose degrading bacteria isolated from buffalo and horse gastrointestinal tract and elephant dung for feed fiber degradation. J Indo Trop Animal Agric 35(1):34–41 Wall DH, Bradford MA, St. John MG, Trofymow JA, Behan-Pelletier V, Bignell DE, Wolters V (2008) Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Global Change Biol 14(11):2661–2677 Wang C, Liu JX, Yuan ZP, Wu YM, Zhai SW, Ye HW (2007) Effect of level of metabolizable protein on milk production and nitrogen utilization in lactating dairy cows. J Dairy Sci 90(6):2960–2965 Ware Fungsin DR, Read PL, Manfredi ET (1988) Lactation performance of two large dairy herds fed Lactobacillus acidophilus strain BT 1386. J Dairy Sci 71:219–222 White JF, Kingsley KI, Kowalski KP, Irizarry I, Micci A, Soares MA, Bergen MS (2018) Disease protection and allelopathic interactions of seed-transmitted endophytic pseudomonads of invasive reed grass (Phragmites australis). Plant and Soil 422(1-2):195–208 Yamazaki H, Roppongi K (1998) The effect of organic matters application for leaf vegetable yield and quality. Bull Saitama Hortic Exp Stat 21:7–20 Yasin M, Wasin M (2011) Anaerobic digestion of buffalo dung, sheep waste and poultry litter for biogas production. J Agri Res 49:73–79 Yokoyama H, Waki M, Ogino A, Ohmori H, Tanaka Y (2007) Hydrogen fermentation properties of undiluted cow dung. J Biosci Bioeng 104:82–85 Zake J, Tenywa JS, Kabi F (2010) Improvement of manure management for crop production in central Uganda. J Sust Agri 34(6):595–617 Zamil SS, Quazi QF, Mah CD, Al Wahid A (2004) Effects of different animal manures on yield quality and nutrient uptake by mustard cv. Agrani 1(2):59–66 Zhao HY, Jie Li, Liu JJ, Lu YC, Wang XF, Cui ZJ (2013) Microbial community dynamics during biogas slurry and cow manure compost. J Integ Agri 12(6):1087–1097 Zheng W, Zeng S, Bais H, LaManna JM, Hussey DS, Jacobson DL, Jin Y (2018) Plant growthpromoting rhizobacteria (PGPR) reduce evaporation and increase soil water retention. Water Resour Res 54(5):3673–3687 Zhibiao N (1996) Effects of acremonium endophyte on the growth of hordeum bodganii [J]. Pratacultural Science 1 Zingore S, Delve RJ, Nyamangara J, Giller KE (2008) Multiple benefits of manure: the key to maintenance of soil fertility and restoration of depleted sandy soils on African smallholder farms. Nut Cyc Agroeco 80(3):267–282

Chapter 5

Fluorescent Pseudomonads in Iron Chelation and Plant Growth Promotion in Abiotic Stresses C. Dileep, C. G. Sreekala, T. S. Reshma, and Surabhi Sankar

Abstract Iron is an essential nutrient for plant growth and plays a pivotal role in the energy metabolism of plants. But abiotic stress such as soil salinity is a leading cause of iron limitation by excessive acquisition by plants. Soil salinity arises as a result of climatic changes and it will be one of the major threats to crop production. It affects the soil characteristics and thus the nutrient uptake for plant growth in saline soils. Plants and microbes overcome this iron limitation by producing iron-chelating agents known as Siderophores. Fluorescent pseudomonads are being considered as most promising organisms which are free-living and endophytic nature, hence be exploited as potential iron chelators of sustainable solution for plant health management. Effect of Iron on siderophore production, pH levels, antagonism, and root colonization are crucial factors which are found to be effective for raising crop in sustainable manner. In the presence of Iron, their fluorescence is masked due to the formation of the siderophore complex. Thus, iron deficiency induces siderophore production and root colonization of such efficient native strains, ensures nutrient uptake, and promotes plant growth. Keywords Siderophore · Antagonism · Root colonization · Pseudobactin · Pyoverdin

5.1 Introduction Agricultural productivity is curtailed by various types of biotic and abiotic stresses. Salinity stress is one of the major abiotic stresses among them. Climatic changes accelerate the process of soil sanitization. The biological properties of the soil are potentially affected by climatic changes (Patil 2018). Fluorescent pseudomonads are the most promising group of plant growth-promoting rhizobacteria (PGPR) involved C. Dileep (B) · C. G. Sreekala · T. S. Reshma · S. Sankar Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Sanatanapuram P.O., Alappuzha 688003, Kerala, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_5

105

106

C. Dileep et al.

in biocontrol of plant diseases (Gardner et al. 1984). Various species mainly Pseudomonas fluorescens, Pseudomonas aeruginosa, Pseudomonas aureofaciens, Pseudomonas putida, and Pseudomonas pyrrocinia demonstrated florescent with varying degrees of the antagonism (de Weger et al. 1986). Some of the fluorescent pseudomonads have currently received world-wide attention due to the production of a wide range of antifungal compounds (Minaxi and Saxena 2010); siderophores; volatile compounds such as HCN (Defago and Haas 1990), antibiotics such as phenazine-1-carboxylic acid; pyoluteorin (Hu et al. 2005); viscosinamide and tesin (Chin et al. 2003); 2,4-diacetylphloroglucinol (Shanahan et al. 1992); and lytic enzymes. The suppression of phytopathogens depends on the ability of the bacteria to colonize the roots and production of an antibiotic phenazine-1-carboxylic acid (PCA), siderophores, and some antifungal factor (AFF). Iron-regulated, non-siderophore antibiotics may be produced by fluorescent pseudomonads more frequently than previously recognized, and could be partly responsible for beneficial effects that were attributed in the past to fluorescent siderophores (Thomashow and Weller 1990). This will lead to the nutrient imbalance in the soil. The high pH and high T.S.S (Total Soluble Salts) creates a complex microenvironment in the rhizosphere. The nutrient uptake by plants will be challenged in this environment and adversely affects crop productivity (Chaudhari et al. 2013). Iron is one of the essential micronutrients and its availability to plants is limited by its non-solubility in soil. Salinity increases the non-solubility of the iron. Iron limitation in saline soil is a multistress condition (Ferreira et al. 2019). PGPR proved effective in stress alleviation and can be modified rhizosphere by these organisms (Backer et al. 2018). The fluorescent Pseudomonas, a reliable game-changer of iron chelation by siderophores converts insoluble iron into available form for plant-uptake (Bakker and Schippers 1987). This chapter focuses on the mechanism of plant growth-promoting fluorescent Pseudomonads to avoid iron limitation and assist in facilitation for the growth and development of plants.

5.2 Interaction Between Deleterious Rhizo Bacteria (DRB) and PGPR Seed bacterization with fluorescent rhizosphere pseudomonads suppressed deleterious (growth-inhibiting) rhizosphere bacteria (Geels et al. 1983, 1985; Kloepper and Schroth 1981; Schippers et al. 1985; Schroth and Hancock 1982; Suslow 1982; Suslow and Schroth 1982). This draws support from the fact that growth promotion is accompanied by a decrease in the number of rhizosphere microorganisms that when reintroduced in the rhizosphere are found to adversely affect the root growth (Suslow and Schroth 1982). The suppression of DRB and the yield decrease is the result of at least two properties, (i) fluorescent pseudomonad isolates interfere with the iron metabolism in the soil by converting Fe3+ ions to a form, by complexing

5 Fluorescent Pseudomonads …

107

with its siderophore, which cannot be used by harmful DRB, resulting in a decrease in their number and activities, and (ii) to the harmful microorganisms effectively, the fluorescent pseudomonads must be capable of colonizing and thus protecting the whole root system of the plant. The interactions between the DRB and PGPR as mediated by siderophores are depicted in Fig. 5.1. When the DRB colonize the roots they produce HCN from a rhizosphere metabolite using iron from the surrounding soil environment with the siderophores they produce. The HCN affects the energy metabolism and the consequent loss of uptake of essential elements like N, P, and K. Cyanide production is thus dependent on the availability of iron (Fe3+ ). The PGPR first hit here by scavenging all the Fe3+ availability by their more efficient siderophores and also by their capability to use the siderophores of the DRB also. Thus, the interaction is competition for Fe3+ and the iron starved DRB lose their hold on the root yielding place to the PGPR. The absence of DRB and hence the nonproduction of HCN explain the release from growth suppression (Dileep and Dileepkumar 2000). It is interesting to note that the designation “growth promotion” or “crop yield increase” is applicable only in the short rotation of crops. All strains

Fig. 5.1 Interaction between Deleterious Rhizo Bacteria (DRB) and PGPR

108

C. Dileep et al.

have common property of antagonism against Gram-positive and Gram-negative pathogenic bacteria and this gives the “double-action” of PGPR—they control the pathogens and thus control disease, besides adding to growth and yield. This antagonistic activity is exerted usually only when the iron is deficient, as only under conditions of iron limitation the PGPR produce the siderophores that chelate the iron. Thus, the term PGPR is a misnomer because their action is by antagonism of deleterious bacteria or “minor pathogens” rather than as plant growth promotor as such. What happens is the removal of growth inhibition, rather than growth promotion. Hence, something is to work against as infrequently or over-cropped potato soils where about 50% of Pseudomonas isolates observed deleterious, and not in sterile soils or when the DRB are absent. Thus the modus operandi for plant growth promotion is competition for iron supported by the following in vitro experiments (a) addition of dissolved iron (Fe3+ ) to the environment abolishes in vitro antagonism and also prohibits the plant growth promotion by PGPR strains and (b)siderophorenegative mutants, obtained by exposure of wild type of PGPR strains to UV light or mutagenic chemicals or obtained by transposon mutagenesis, also lost their PGPR activities, although they colonized roots as well as similar to the wild type PGPR (Bakker et al. 1987).

5.3 Iron Deficiency and Siderophore Production Iron is an essential element for living organisms under its two stable valences that act as cofactors in various oxidative-reductive enzymatic reactions. Although iron is abundant, comprising 4–5% of the average soil, iron deficiency of crop plants is common in calcareous soils that represent over one-third of the world’s land surface area. In well-aerated soils with a high pH, the concentration of Fe2+ and Fe3+ becomes negligible. The concentration of chelated iron required for optimal growth is of the order of 10−6 –10−5 M. Cultivars that grow in alkaline soils without developing symptoms of lime-induced chlorosis are called “iron efficient” while those that become “chlorotic” are iron-defficient. Fe is reflected by the number of mechanisms developed by plants and microorganisms for its acquisition. Plants undergo in iron deficiency overcome by several mechanisms: (i) secretion of protons by roots (Marschner et al. 1974) (ii) secretion of reducing compounds by roots and (iii) secretion of phytosiderophores (Suguira and Nomato 1984). Although, phytosiderophores are widely distributed in higher plants (Rippenger and Schreiber 1982), they have only been isolated from root washings of graminaceous plants. These are amino hydroxyl carboxylates with high affinity for Fe3+ (Kf 10s) although not as high as those possessed by bacterial and fungal siderophores. Besides, plants’ supporting fluorescent pseudomonad flora is a mechanism to make iron available to itself (Dileep and Dileepkumar 2000). Microorganisms have evolved efficient uptake systems to obtain sufficient amounts of iron. Most aerobic and facultative aerobic bacteria possess a highaffinity iron-transport system in which siderophores are excreted and the consequent

5 Fluorescent Pseudomonads …

109

iron complex is taken up via the cognate-specific receptor and a transport pathway (Neilands 1981; Neilands et al. 1987). Microorganisms have developed following methods of iron acquisition, membrane-bound chelator (Royt 1988), and reduction of iron chelates (Emery 1987; Lesuisse and Labbe 1989; Zimmermann et al. 1989).

5.4 Siderophores The production of siderophores by microorganisms in slightly acidic, neutral, or alkaline soils is a general phenomenon (Kloepper et al. 1980) . No system analogous to the siderophores has been found for any other metal ion and Fe3+ seems to be unique in requiring such specific ligands. Siderophores are low molecular weight iron-chelating agents produced by virtually all bacteria and fungi under iron-limiting conditions. The fluorescent pseudomonads producing siderophores (water-soluble, yellow-green fluorescent pigments) viz. P. aeruginosa, P. putida, and P. fluorescens all belong to the same inter-generic homology group (Palleroni et al. 1973; Palleroni and Doudoroff 1974). Turfreijer (1942) proposed the term “pyoverdine” for the pigment of P. fluorescens by its analogy with that of phenazine pigment, pyocyanine produced by P. aeruginosa. The term pyoverdine has been extended to include all pigments produced by fluorescent pseudomonads. However, due to differences in structure, these are now named differently. Mayer and Abdallah (1978) like to designate the pigments of this class by a suffix including the species responsible for their production e.g., pyoverdine Pf for the pyoverdine of P. fluorescens. The main differences observed between those produced by different strains are the number, composition, and sequence of their L- and Damino acids which are thought to give the molecule their receptor specification (Hohnadel and Mayer 1988). During the past years, the chemical structure of a large number of microbial siderophores has been elucidated by NMR spectroscopy, Mass spectroscopy, Chemical degradation, and X-ray diffraction. Two different names have been used for siderophores of Pseudomonas sp. pyoverdine, and pseudobactin. The complete structure for pseudobactin, the siderophore of Pseudomonas BlO, has been determined. It consists of a linear hex peptide: L-Lys-D-Threo-BOH-Asp-L-Ala-D-allo-Thr-L-AlaD-N-OH-Orn, in which the ornithine residue is cyclized into an N-hydroxypiperidone ring and the lysine residue, is linked to a fluorescent quinoline derivative. The iron chelation to the hydroxamate, the a-hydroxy acid, and the -o-dihydroxy group1, establishes pseudobactin as one of the unique groups of siderophores. The occurrence of both L- and D-amino acids is also unusual and their alternate sequence in pseudobactin explains why the compound is not affected by proteolytic enzymes. The pyoverdine for P. fluorescens has been partially characterized. It contains seven amino acid residues with two hydroxamate groups and an o-dihydroxy aromatic group. The complete structure of pyoverdine Pa from P. aeruginosa has been determined (Dileep et al. 1998).

110

C. Dileep et al.

All the siderophores in this family are related by having a cyclic or linear peptide containing D- and L- amino acids, mixed ligand groups with at least one hydroxamate group or and a-hydroxy acid. Structurally at least eight amino acid residues are required for cyclic compounds. Even different strains of the same organism produce different pseudobactins which are discriminated in the uptake process of the various strains. The affinity of siderophores for Fe3+ is expressed as a binding or stability constant log 10 K Fe (pH 7.0). It is pH-dependent, varies widely among the various siderophores, and is thus an important ecological factor in the microbial competition for iron. The solubility of organic iron might be relative to the soil type (Benjamini and Hochberg 1995). Iron is more soluble and biologically available at low pH (Wandersman and Delepelware 2004). Increasing pH siderophore production ceased, this may be since alkaline pH help in excess solubilization of iron, which increases the iron content of the soil. Acidity affects metal speciation and bio-availability to microbes through various mechanisms (Lofts et al. 2004; Gobran and Huang 2011). P. aeruginosa species from acidic soil shows siderophore production in iron-deficient succinate medium in varying degree of absorbance and peaks. A potent siderophore, such as the ferric-siderophore complex plays an important role in iron uptake by plants in the presence of other metals, such as nickel and cadmium (Beneduzi et al. 2012).

5.5 Plant Responses to Salinity The ability of the plant to the saline environment depends on its genetic makeup and physiological responses. Cereals and vegetables are very sensitive to salinity (Paul and Lade 2014). Plant response to salinity starts by the osmotic adjustments and later by the specific ion effects. High salinity causes structural and functional impairments in plants and affects crop productivity (Meng et al. 2017). Plants exposed to salinity show stunted growth, delay or absence of germination, low seedling growth, decrease in root length, and root meristems (Ameixa et al. 2016; Konuskan et al. 2017; Taibi et al. 2016; Acosta-Motos et al. 2017). Salt stress creates nutrient imbalances (Grattan and Grieve 1998). Physiological responses to salinity results in the reduction of crop production by altering the protein synthesis, photosynthesis (Pessarakli 2014).

5.6 Unavailability of Iron in Saline Soils Limited iron availability in soil is one of the leading causes of a reduction in crop productivity. Iron is playing a key role in photosynthesis, electron transport, enzymatic processes involving oxygen (Ferreira et al. 2019). Iron catalysis the chlorophyll synthesis (Hu et al. 2017) and is the second most abundant metal in the earth’s crust; rather it is not accessible to plants. This is due to the insolubility of Iron. Fe2+ and

5 Fluorescent Pseudomonads …

111

Fe3+ are the two interconvertible forms of iron; pH, salinity, and alkalinity influence the conversion of Fe2+ and Fe 3+ . Iron combines with phosphates, carbonates, calcium magnesium, and hydrogen ions and its limitation increases due to its non-solubility corresponding to salinity. The downregulation of iron transportation in response to salinity may lead to iron limitation (Cotsaftis et al. 2011). Another context of a reduction in iron availability is the inhibition of proton pumps required for the uptake processes (Rabhi et al. 2007).

5.7 Avoidance of Iron Limitation in Saline Soils Plants under iron deficiency exhibit various mechanisms to avoid the Iron limitation. This is also including root exudates and phytosiderophores production. Bacterial siderophores are more efficient when compared to phytosiderophores and efficient siderophores have been observed in different genera of plant growth-promoting rhizobacteria which can avoid deleterious phytopathogens (Dileep 2012). The root exudate secretions and other metabolites include amino acids, organic acids, and phenolic compounds which lower pH of the soil and avoid to interfere iron availability. These root exudates attract the PGPRs to the rhizosphere regions by root colonization and chemotaxis, thus facilitate to chelate iron (Singh et al. 2010; Aeron et al. 2020). The iron-siderophore complexes, having membrane receptors, can easily access the Iron. Iron limitation in saline soils can be alleviated through the inoculation of halo-tolerant PGPR as given in Fig.5.1.

5.8 Fluorescent Pseudomonads—A Sustainable Solution for Iron Limitation in Saline Soils The effective strategy for avoiding Iron limitation by the application of P. fluorescens, P. stuzeri on Tomato (Tank and Saraf 2010), on common bean by P. fluorescens (Younesi and Moradi 2014); Growth promotion reports on Groundnut by P. fluorescens (Saravanakumar and Samiyappan 2007), and in Peanut (Sharma et al.2016) and various other crop plants (Maheshwari 2011; Maheshwari et al. 2013). In a case study, saline tolerant fluorescent pseudomonads are collected from the saline Pokkali rice field, with an average 5.9 pH and 5.0 T.S.S (Total soluble salt). Pokkali is a salt-tolerant, GI tagged rice variety; cultivated in saline soils. The primary screening of the organism, by its ability to fluorescence under UV light. The King’s B medium (Peptone 20 g; MgSO4 .7H2 O 1.5 g; K2 HPO4 1.5 g; Agar 15 g; Distilled water 1L) is modified by varying concentrations of NaCl to screen the salt tolerance of the organism. Selected strains are inoculated in iron-deficient, synthetic, succinate medium (Mayer and Abdallah 1978), incubated for 48 h at 30 °C. The culture supernatants were centrifuged at 10000 rpm for 20 min. The supernatants were filtered

112 Table 5.1 Siderophore production in Pseudomonas isolates

C. Dileep et al. Bacterial strains

Incubation period (h)

Peak

Absorbance

P6 1

48

404

0.788

PK7

48

403

2.137

Fig. 5.2 Absorbance spectra of Pseudomonas isolates

and measure OD at 300–600 nm in UV Visible spectrophotometer (SHIMADZU UV 2600), to measure the siderophore production. Obtaining a peak at or near 404 nm indicates the presence of siderophore (Table 5.1; Fig. 5.2). The graph shows a clear peak at 404 nm by the strain P6 1 and the strain PK 7 shows the same at 403 nm. These two strains belong to fluorescent pseudomonas and can be considered as a reliable source of siderophore. Also, they produce phytohormones, ACC-deaminase, enzymes, etc. The increase of shoot and root length and promotion in the early vegetative growth parameters were observed (Da Silva et al. 2018). The number of roots and its length is significant in iron uptake. These two are directly proportional to each other (Fig. 5.3). The crop protection under salinity can be well played by fluorescent pseudomonads. Considering all these facts, the exploitation of these microbes and its application in saline soils ensure the sustainable strategy for Iron chelation and plant health management.

5.9 Root Colonization and Plant Growth Promotion Root colonization study of acidic tolerant Pseudomonas species Rhizobacteria can indirectly lead to reduced pathogen attack through induction of systemic resistance (Kloepper and Beuchamp 1992). Colonization of roots by inoculated bacteria is an important step in the interaction between beneficial bacteria and the host plant

5 Fluorescent Pseudomonads …

113

Fig. 5.3 Effect of salinity on PGPR activity

(Benziri et al. 2001). The use of naturally occurring rhizobacteria, which protect and promote plant growth by colonizing and multiplying in the rhizosphere/root cortex, could be an alternative method for plant protection. Rhizobacteria and especially the fluorescent pseudomonads have emerged in the last two decades as organisms of great importance that modulate the growth of plants by providing freedom from growth inhibition of deleterious rhizosphere microorganisms and, thus, restoring normal growth and yield. Under being antagonistic to some major pathogens they also provide “biological control” which is more eco-friendly and needs of the time in face of a threat from pollution by the use of chemical disease-controlling agents (Dileep Kumar and Dube 1992). Nature practices biological control as evidenced by the existence of disease suppressive soils for various diseases. We have only to learn nature’s ways and try to simulate or support it. Their study has injected anew interest in plant microbial interactions in recent years. The plant growth-promoting substance produced by P. fluorescens might have exerted a synergistic action and enhanced the growth promotion of seasonal crop plants. Pseudomonas spp. were reported producing amino acids, salicylic acid, and IAA (Sivamani and Gnanamanickam 1988; O’ Sullivan and O’ Gara 1992). Growth promotion studies of acidic tolerant strains show a high rate of plant growth promotion which might have improved the plant growth and seedling vigor. PGPR is an ecofriendly tool for keeping soil fertility by nutrient enrichment. The production of secondary metabolites change the root architecture and enhance the nutrient uptake and provide the opportunity to enhance the beneficial effects of PGPR (Table 5.2).

114

C. Dileep et al.

Table 5.2 Data represent values of 5 replicates of 15 plants. Data in parenthesis represent percentage over control Treatments

Germination (%)

Shoot (length in cm)

Root (length in cm)

Fresh weight (g)

Dry weight (g)

RP12 + Rice

98.1 (11)

18.76 (49.59)

10.43 (34.94)

1.237 (40.9)

0.199 (91.8)

MIP + Rice

95.8 (8.87)

18.53 (48.96)

8.32 (18.44)

1.5048 (51.42)

0.182 (15.6)

FPO4 + Rice

93.8 (6.9)

14.744 (35.86)

6.17 (9.96)

0.765 (4.44)

0.173 (11.21)

Control

87.3

9.456

6.785

0,731

0.1536

5.10 Effect of Iron and PH Levels FeCl3 amended media were fluorescent. In the case of pH, the results varied in different media. The strains were capable of producing siderophore even in an extremely acidic pH of 4.2 being isolated from the acidic fields. The use of resident organisms is advocated over the alien ones as the formers are well adapted to the prevalent edaphic and agroclimatic conditions (Fonseca-García et al. 2016). Based on these findings it is clear that root exudates, pH, and the presence of FeCl3 are major factors in the rhizosphere that influence growth, metabolic production, and root colonization of the microflora.

5.11 Effect of Iron on Antagonism The effect of iron on antibiosis by the four maximally inhibitory organisms was examined by the “dual culture test” suggested by Utkhede and Rahe (1983) on the Kings B Medium. No effect on inhibition by iron inclusion in the medium will mean noninvolvement of siderophore and a change in inhibition would suggest the involvement of siderophore (Andrews et al. 2003). It was noted that in all cases the addition of iron curtailed fluorescence, siderophore production caused a reduction in their inhibition of the test fungal pathogens. The inhibition ranged varied for the test fluorescent pseudomonads as, P6 1, 22.3–68.4%; RP12, 32.3–70.0%; PK12, 11.8–77.8% and MIP shown 18.2–64.3%. The loss in inhibition is quite appreciable which points out to involvement of siderophores in the growth inhibition of the fungal pathogens. The role of other chemicals is not ruled out.

5 Fluorescent Pseudomonads …

115

5.12 Influence of Amino Acids, Organic Acids, and Sugars on Growth, Fluorescence, and Siderophore Production The organic substrates in the rhizosphere lead to greater growth and activity of the microorganisms around the roots. The influence of amino acids, organic acids, and six sugars, commonly encountered in root exudates showed siderophore production, plant growth promotion, and disease suppression. Among the eight amino acids tested (L-alanine, D-L-arginine, L-glutamine. L-lysine, D-methionine, D-L-proline, D-L-serine, L-tyrosine) for growth of the organisms, amino acids (methionine and serine) did not support the growth of any of the organisms and thus were not an energy source for these bacteria (Dileep et al. 1998). Among the rest six amino acids, three (L-alanine, D-L-proline, and L-tyrosine) supported both growth and fluorescence. Six organic acids screened were L-aspartic acid, citric acid, D or L-glutamic acid, L (+) lactic acid, D-maleic acid, and succinic acid that supported growth curtailing fluorescence and not supported siderophore production. Arabinoses among several sugars not supported growth and it supported only growth (not fluorescence) of the rest two organisms. It is interesting to note that in the presence of sugars (except glucose) the siderophore production was arrested (Dileep et al. 1998). Thus, sugars do not support siderophore production. But keeping in view the ubiquity of glucose, it does not affect much in nature (Table 5.3).

5.13 Siderophores as Iron Storage Compounds Although siderophores were identified and confirmed as iron transporting agents, there is evidence that they may have further intracellular functions. Several spectroscopic studies confirmed the possible involvement siderophores on iron storage (Kraemer et al. 2006). Recent research on the occurrence of siderophores in P. aeruginosa has indicated well-known hydroxamate type Siderophores. Uptake of iron-mediated by siderophores is energy-dependent and requires the specific interaction with siderophores is transport systems in the cytoplasmic membranes. Iron from siderophores is transported to the cellular metabolism by a reductive removal, which is not operating in the corresponding aluminum, chromium, or gallium complexes (Römheld and Marschner 1986). Transport studies using various hydroxamate type siderophores revealed that the absolute configuration of the metal center, the number, and kind of irons surrounding N-acetyl residues and the overall structure of the various hydroxamate families. Besides the function in iron chelation and transport, the third function in iron storage has recently been confirmed by the hydroxamate siderophores.

116

C. Dileep et al.

Table 5.3 Influence of various root exudates on growth, fluorescence, and siderophore production of two fluorescent Pseudomonas Growth and fluorescence

Siderophore production (ODa )

P61

RP12

P61

RP12

L-alanine

+

+

0.201

0.370

L-glutamine

NF

+

0.313

0.132

L-lysine

NF

NF

0.071

0.063

L-tyrosine

+

+

0.275

0.314

Substrate Amino acids

D-methionine

NG

NG

NT

NT

D-(L)-arginine

NF

+

0.085

0.164

D-(L)-proline

+

+

0.497

1.279

D- (L)-serine

NG

NG

NT

NT

L-aspartic acid

+

+

0.271

0.285

D-maleic acid

NF

NG

0.000

0.000

Succinic acid

+

+

0.151

0.080

Citric acid

NF

NG

0.000

0.000

D/L-glutamic acid

NG

NF

0.000

0.202

L (+) lactic acid

NG

NG

NT

NT

D (−) fructose

NF

+

0.000

0.000

D (+) mannose

+

NF

0.000

0.000

D (−) galactose

NF

NF

0.000

0.000

D (−) ribose

NF

NF

0.000

0.000

D (+) glucose

+

NF

0.362

0.023

L (+) arabinose

NG

NG

0.000

0.000

Organic acids

Sugars

+ = growth with fluorescence; NG = no growth; NF = Growth with no fluorescence; NT = not tested a Absorbance at 404 nm after 48 h

5.14 Conclusion and Future Aspects Soil rhizosphere competence for Fe is supposed to be controlled by the Fe affinity of the siderophores, which is the hexadentate ligand produced by the fluorescent pseudomonads in higher concentration than the pathogen. In this study we found that a notable proportion of rhizosphere and rhizoplane soil fluorescent pseudomonads are able to make use of the Fe in pure or complex form of the hydroxamate siderophores as an Fe source. The Fe-siderophore could be utilized by most of the strains isolated and their ability to scavenge the siderophore produced by other microorganisms conferring an ecological advantage.

5 Fluorescent Pseudomonads …

117

Competition for Fe can be considered as occurring in two stages (a) competition for the metal by the siderophores and (b) competition between the microorganism particularly fluorescent pseudomonas for the Fe-siderophore complex, The former is controlled by proton dissociation and formation constant of each siderophores as well as by their concentration and kinetics of exchange, while the latter is governed by existence of an uptake mechanism for, and its affinity to, the Fe complex (Edouard et al. 1992). Soil salinity and acidity also alter the soil characteristics which negatively affects the Fe uptake of pseudomonads, which influence the nutrient uptake of plant community. Saline and acidic tolerant pseudomonads have to compensate in this with improved osmo-tolerance and could play a pivotal role in the benefit to the plants grown in saline soils, in better growth, colonization, and yield. A potential application of microbial inoculants to improve crop growth and yield in saline environments is a potential strategy for saline soil agriculture. Plant root exudates mainly amino acids, organic acids, and sugars have a positive role in colonization of fluorescent pseudomonas in the microenvironment of the plant root system. A consortium of different PGPRs with known functions that could act symbiotically as they offer multiple modes of action, with variability. The data presented in this article supports that some saline acidic tolerant pseudomonads which are intrinsically less available to rhizosphere utilizes the Fe in faster rates with their siderophores which is an important finding as one of the parameters in reducing the availability of Fe to other microorganisms in the rhizosphere. Interaction between these soil fluorescent pseudomonads colonizing on the rhizosphere and rhizoplane of plant root system will progress to harness, thus, improving the general health growth, yield of the plant, and overcoming the stress.

References Acosta-Motos JR, Ortuno M F, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA. (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy, pp 1– 38 Aeron A, Maheshwari DK, Meena VS (2020) Endophytic bacteria promote growth of the medicinal legume Clitoria ternatea L. by chemotactic activity. Arch Microbiol 1–10. https://doi.org/10. 1007/s00203-020-01815-0 Ameixa OMCC, Marques B, Fernandes VS, Soares AMVM, Calado R, Lillebø AI (2016) Dimorphic seeds of Salicorniaramosissima display contrasting germination responses under different salinities. EcolEng 87:120–12 Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. https://doi.org/10.1016/S0168-6445(03)00055-X Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473 Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp mediated plant stimulation. Soil Biol Biochem 19(4):451–457 Bakker PAHM, Bakker AW, Marugg JD, Peter JW, Schippers B (1987) A bio-assay for studying the role of siderophores in potato growth stimulation by Pseudomonas spp in V.; short potato rotations. Soil Biol Biochem 19:443–449

118

C. Dileep et al.

Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetics Mol Biol 35:1044–1051 Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate; a practical powerful approach to multiple testing. J R Stat Soc 57:289–300 Benziri E, Baudoin E, Guckert A (2001) Root colonization by inoculated plant growth promoting rhizobacteria. J Biocontrol Sci Technol 11:555–574 Chaudhari S.K, Chinchmalatpure A.R, Sharma D.K (eds) (2013) Climate change impact on saltaffected soils and their crop productivity. ICAR-CSSRI Technical manual. 1–51 Chin-A-Woeng TFD, Bloemberg GV, Lugtenberg BJ (2003) Phenazine and their role in biocontrol by Pseudomonas bacteria. New Phytol 157:520–523 Cotsaftis O, Plett D, Johnson AA, Walia H, Wilson C, Ismail AM, Close TJ, Tester M, Baumann U (2011) Root-specific transcript profiling of contrasting rice genotypes in response to salinity stress. Mol Plant 4:25–41 Da Silva CDF, Brito TLD, Taniguchi CA, Lopes LA, Pinto GA, de Carvalho AC (2018) Growthpromoting potential of bacterial biomass in the banana micropropagated plants. Revista Brasileira de Engenharia Agrícola e Ambiental 22(11):782–787 De Weger LA, van Boxtel R, der Burg B, Gruters RA, Geels FP (1986) Siderophores and outer membrane proteins of antagonistic, plant-growth- stimulating, root-colonizing Pseudomonas spp. J Bacteriol 165:585594 Defago G, Haas D (1990) Pseudomonads as antagonists of soil borne plant pathogens: mode of action and genetic analysis. Soil Biochem 6:249–291 Dileep C (2012) Rhizosphere fluorescent pseudomonads—a new perspective. Plant–Microbe Interaction. LAP-LAMBERT Publication, p 125–130 Dileep C, Dileepkumar BS (2000) Influence of Metham -Sodium on suppression collar rot disease of peanut, in vitro antibiosis, siderphore production and root colonization by fluorescent Pseudomonad strain FPO4. Ind J Exp Biol 38:1245–1250 Dileep C, Dileepkumar BS, Dube HC (1998) Influence of aminoacids, organic acids and sugars on growth, fluorescence and siderophore production of fluorescent Pseudomonads. Ind J Exp Biol 36:429–431 Dileep Kumar BS, Dube HC (1992) Seed bacterization with a fluorescent Pseudomonas for enhanced plant growth, yield and disease control. Soil Biol Biochem 24(6):539–542 Edouard J, Yitzhak H, Yona C (1992) Differential siderophore utilization and iron uptake by soil and rhizhosphere bacteria. Appl Environ Microbiol 58(1):119–124 Emery T (1987) Reductive mechanisms of iron assimilation. Iron transport in microbes, plants and animals. In: Winkelmann G, van der Helm D, Neilands JB (eds.) Iron transport in animals, plants and microorganisms. VCH Chemie, Weinhein, Germany, pp 235–248 Ferreira MJ, Silva H, Cunha A (2019) Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: A review. Pedosphere 29(4):409– 420 Fonseca-García C, Coleman-Derr D, Garrido E, Visel A, Tringe SG, Partida-Martínez LP (2016) The cacti microbiome: interplay between habitat-filtering and host-specificity. Front Microbiol 7:150. https://doi.org/10.3389/fmicb.2016.00150 Gardner JM, Chandler L, Feldman AW (1984) Growth promotion and inhibition by antibiotics producing fluorescent Pseudomonads on citrus root. Plant Soil 77:103–113 Geels FP, Schmidt EDL, Schippers B (1985) The use of 8-hydroxy quinoline for the isolation and pre-qualification of plant growth-stimulating rhizosphere pseudomonads. Biol Fert Soils 1(4):167–173 Gobran GR, Huang P (2011) Biogeochemistry of trace elements in the rhizosphere. Elsevier, Amsterdam, The Netherlands Grattan SR, Grieve CM (1998) Salinity-mineral nutrient relations in horticultural crops. Sci Hortic 78:127–157 Hohnadel D, Mayer JM (1988) Specificity of pyorerdin mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol 170:4865–4873

5 Fluorescent Pseudomonads …

119

Hu HB, Xu YQ, Cheng F, Zhang XH, Hur B (2005) Isolation and characterization of a new Pseudomonas strain produced both phenazine 1-carboxylic acid and pyoluteorin. J Microbiol Biotech 15:86–90 Hu XY, Page MT, Sumida A, Tanaka A, Terry MJ, Tanaka R (2017) The iron-sulfur cluster biosynthesis protein sufb is required for chlorophyll synthesis, but not phytochrome signaling. Plant J 89:1184–1194 Kloepper J, Beauchamp C (1992) A review of issues related to measuring colonization of plant roots by bacteria. Can J Microbiol 38:1219–1232 Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886 Kloepper JW, Schroth MN (1981) Development of powder formulation of rhizobacteria of inoculum of potato seed pieces. Phytopathology 712:590–592 Konuskan O, G¨oz¨ubenli H, Ati¸s ˙I, Atak M (2017) Effects of salinity stress on emergence and seedling growth parameters of some maize genotypes (Zea mays L.). Turk J Agric-Food Sci Technol 5:1668–1672 Kraemer SM, Crowley DE, Kretzschmar R (2006) Geochemical aspects of phytosiderophore promoted iron acquisition by plants. Adv Agron 91:1–46 Lesuisse E, Labbe P (1989) Reductive and non-reductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J Gen Microbiol 136:257–263 Lofts S, Spurgeon DJ, Svendsen C, Tipping BE (2004) Deriving soil critical limits for Cu, Zn, Cd and Pb: a method based on free ion concentrations. Env Sci Technol 38:3623–3631 Maheshwari DK (2011) Bacteria in agrobiology: Crop ecosystems. Springer Science & Business Media Maheshwari DK, Saraf M, Aeron A (2013) Bacteria in agrobiology: crop productivity. Springer Science & Business Media, Berlin Marschner H, Kalisch A, Romheld V (1974) Mechanism of iron uptake indifferent plant species. Proc. 7th Internation Coll. Plant Analysis Fertilizer Problems, p 273–281 Mayer JM, Abdallah MA (1978) The flourescent pigment of pseudomonads fluorescence: biosynthesis, purification and physico chemical properties. J Gen Microbiol 107:319–328 Meng R, Saade S, Kurtek S, Berger B, Brien C, Pillen K, Tester M, Sun Y (2017) Growth curve registration for evaluating salinity tolerance in barley. Plant Methods 13:18 Minaxi, Saxena J (2010) Characterization of Pseudomonas aeruginosa RM-3 as a potential biocontrol agent. Mycopathol. 170:181-193 Neilands JB (1981) Microbial iron compounds; Annu Rev Biochem. 50:715–731 Neilands JB, Konopka K, Schwyn B, Coy M, Francis RT, Paw H, Bagg A (1987) Comparative biochemistry of microbial iron assimilation. In: Winkelmann G, vander Helm D and Neilands J.B (eds.) Iron transport in animals,plants, and microorganisms. VCHchemie,Weinheim, Germany, p 3–34 O’ Sullivan DJ, O’ Gara F (1992) Traits of Fluorescent Pseudomonas spp involved in suppressionof plant pathogens. Microbiol Rev. 56(4):662–676 Palleroni NI, Doudoroff M (1974) The genus Pseudomonas. In: Buchananand RE and Gibbons NE (eds) Bergey’s manual of determinative bacteriology, Baltimore, Williams and Wilkin, 8th edn. p 217–243 Palleroni NJ, Kuvisawa R, Contopoulou R, Doudoroff M (1973) Nucleic acid homologies in the genus Pseudomonas. Int J Syst Bacteriol 23:333–339 Patil A (2018) Impact of climate change on soil health: a review. Sci Int 6:2399–2404 Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752 Pessarakli M (2014) Handbook of plant and crop physiology, 3rd edn. CRC Press, Boca Raton, FL, USA, pp 563–568 Rabhi M, Barhoumi Z, Ksouri R, Abdelly C, Gharsalli M (2007) Interactive effects of salinity and iron deficiency in Me- dicagociliaris. CR Biol 330:779–788

120

C. Dileep et al.

Rippenger H, Schreiber K (1982) Nicotianamine and analogous amino acids, enologenous iron carriers in higher plants. Heterocycles 17:447–461 Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180 Royt PW (1988) Isolation of a membrance associated iron chelator from Pseudomonas aeruginosa. Biochem Biophys Acta 939:493–502 Saravanakumar D, Samiyappan R (2007) ACC deaminasefro Pseudomonas uorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102(5):1283–1292 Schippers B, Geels PP, Hoekstra O, Lamers JG, Maenhous CAAA (1985) Yield depressions in narrow rotations caused by unknown microbial factors and their suppression by selected Pseudomonads. In: Parker CA, Rovira AD, Moore KJ, Wong PT, Kollmorgen JF (eds.) Ecology and management of soil-borne plant pathogens. Am. Phytopathol, Soc. St. Paul, p 127–130 Schroth MN, Hancock JG (1982) Disease-suppressive soil and root colonizing bacteria. Science 216:1376–1381 Shanahan P, O’Sullivan DJ, Simpson P, Glennon JD, O’Gara F (1992) Isolation of 2, 4diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiologic parameters influencing its production. Appl Environ Microbiol 58:353–358 Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol. 7:1600 Singh N, Kumar S, Bajpai VK, Dubey RC, Maheshwari DK, Kang SC (2010) Biological control of Macrophomina phaseolina by chemotactic fluorescent Pseudomonas aeruginosa PN1 and its plant growth promotory activity in chir-pine. Crop Protec 29(10):1142–1147 Sivamani E, Gnanamanickam SS (1988) Biological control of Fusarium oxysporumf .sp.Cubense in Banana by inoculation with Pseudomonas fluorescens. Plant Soil 107:3–9 Suguira Y, Nomato K (1984) Phytosiderophores. Struct Bond 58:107–135 Suslow TV (1982) Role of root-colonizing bacteria in plant growth. In: Mount MS and Lacy GH (eds.) Phytopathogenic prokaryotes (Vol. I). Academic Press, p 123–187 Suslow TV, Schroth MN (1982) Role of deleterious rhizobacteria as minor pathogens in reducing crop growth. Phytopathol 72:111–115 Taıbi K, Taıbi F, Ait Abderrahim L, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South Afr J Bot 105:306–312 Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58 Thomashow LS, Weller DM (1990) Role of antibiotics and siderophores in biological control of take-all disease of wheat. Plant Soil 129:93–99 Turfreijer A (1942) Pyoverdinen de fluorescen de kleurstoffen van Pseudomonas fluorescens. Thesis, University of Amsterdam. British Abstracts. 16:16578 Utkhede RS, Rahe IE (1983) Interaction of antagonistsand pathogen in biological control of white rot. Phytopathol 73:890–893 Wandersman C, Delepelware P (2004) Bacterial iron sources; from siderophore to hemophores. Annu Rev Microbiol 58:611–647 Younesi O, Moradi A (2014) Effects of plant growth-promoting rhizobacterium (PGPR) and arbuscular mycorrhizal fungus (AMF) on antioxidant enzyme activities in salt-stressed bean (Phaseolus vulgaris L.). Agriculture 60(1):10–21 Zimmermann L, Angerer AM, Braun V (1989) Mechanically novel iron (III) transport system in Serratia marcescens. J Bacteriol 171:238–243

Part II

Endophytes and Mineral Nutrition

Chapter 6

Microbial Endophytes: New Direction to Natural Sources Azim Ghasemnezhad, Arezou Frouzy, Mansour Ghorbanpour, and Omid Sohrabi

Abstract The concept of endophytes and their beneficial relationship with the plant is widely accepted as an important step in the co-evolution and diversity of plants. The symbiotic relationship between plants and fungi and rhizobia with legumes have a long evolutionary history. During exploration, fossils have shown close associations between endophytic fungi and plants roughly, 400 million years ago. The common symbiotic relationship between fungi and plants facilitated the evolution of large group of primary and secondary metabolites of considerable chemical diversity, have a unique structure and high biological activity. During the last two decades, a growing interest in the study of endophytes, origin, biodiversity, interactions between endophytes and host plants, their role in ecology as well as biological activities of metabolites have been established. Several novel and beneficial activities for these microorganisms are evident by available literature, reveals their role as multifarious biologicals. The diversity and dynamics of endophyte populations, use of microbial inoculants to improve plant growth and health, and their role as a new bio-resource for metabolites are considerable interests of the twenty-first century. The exploration of active secondary metabolite is one of the most important reasons for the endophytes of industrial significance. Keywords Ecology · Bacteria · Endophyte · Fungi · Metabolites · Symbiosis

A. Ghasemnezhad · A. Frouzy Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran M. Ghorbanpour (B) Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak 38156-8-8349, Iran e-mail: [email protected] O. Sohrabi Department of Horticultural Sciences, Guilan University, Rasht, Iran © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_6

123

124

A. Ghasemnezhad et al.

6.1 Introduction To understand why endophytes have received great attention in the field of antimicrobial research, there is a need to examine their intended role in nature. Microbial groups residing in plant tissue have been identified as symbiotic or pathogenic (Larran et al. 2016; Martinez-Klimova et al. 2017). According to Wilson (1995), endophyte (Gr. Endon, within; Phyton, plant) is an organism that lives within the plant. Usually, the organisms found inside the plant are fungi and bacteria. Endophytic host plants show no signs of disease symptoms at least during the endophytic phase of their life cycle (Wilson 1995). Endophytic fungi are found in all plant families worldwide and almost in all climatic conditions (Larran et al. 2016; Martinez-Klimova et al. 2017; Santoyo et al. 2016). Microbes enter plant tissues through wounds or roots or the creation of wounds by secreting enzymes such as pectolytic and cellulolytic enzymes. It is unclear, why plants and endophytes co-exist or why plants do not defend themselves against internal colonization (Martinez-Klimova et al. 2017; Wilson 1995) yet to be understood. So far, the relationship between plant co-existence and endophyte seems to be beneficial to both parties and has dual advantages. It is beneficial for endophyte due to plant nutrients and habitat while for the plant because of the protection against pathogens, increased nutrient uptake, plant growth promotion (Martinez-Klimova et al. 2017; Santoyo et al. 2016) and stress resistance (Larran et al. 2016) Bacterial endophytes facilitate the acquisition of essential mineral nutrients through the environment such as nitrogen, phosphorus, and iron (Zhang et al. 2006; Gangwar et al. 2014) and also produce vitamins or modulate phytohormone levels in the plant because of their nature of producing auxin, cytokinin, gibberellins, etc. (Santoyo et al. 2016). Endophytes increase the root volume of the plant (Zhang et al. 2006), and increased plant growth thus, may eliminate the cellular apoptosis caused by the pathogen infection (Alvin et al. 2014). However, according to Hyde and Suetong (2008), more research is yet to be done to confirm the beneficial properties of endophytes toward plants. Endophytic plants are believed to be healthier than non-endophytic plants (Zhang et al. 2006), because endophytes produce metabolites that promote plant growth and protect the plant, act against insects, pests, and plant diseases (Golinska et al. 2015; Abdalla and Matasyoh 2014). Since, the natural products of endophytes act as antimicrobial, antifungal, anticancer, and antioxidant agents as reported by Zhang et al. (2006), hence, secondary metabolites produced by endophytes might be useful in the pharmaceutical industries (Golinska et al. 2015) (Table 6.1; Fig. 6.1). Endophytes are capable of biosynthesis of some chemical compounds like their host plant, possibly as an adaptor to the host micro-environment (Zhang et al. 2006). The most common example is taxol, but several other anticancer compounds such as comptotcin and podophylotoxine have also been reported (Alvin et al. 2014). Endophytes secrete antibiotics and hydrolytic enzymes to prevent the colonization of plant pathogenic microbes or to prevent insects and nematodes penetration and produce metabolites capable of activating the plant defense mechanism or enhancing plant growth (Fig. 6.2).

6 Microbial Endophytes: New Direction to Natural Sources

125

Table 6.1 Benefit of endophyte and plants in coexistence Endophyte

Host-plant

Feeding by host plant

• • • • • • • • • • •

Protection against pathogens Increased nutrient absorption Promoting plant growth Stress resistance Nutrient uptake such as nitrogen, phosphorus, and iron Production of vitamins Modulation of auxin, cytokinin, and gibberellin Increase the amount of root of the plant Compensate for cellular apoptosis caused by pathogen infection Preventing colonization of plant pathogens Preventing the penetration of insects and nematodes

Fig. 6.1 Effect of endophyte on biomass and artemisinin production of in Artemisia (Hussain et al. 2017) Fig. 6.2 Influence of endophyte on root growth in rice plant (Korzekwa 2015)

126

A. Ghasemnezhad et al.

Thus endophytes try to eliminate apoptosis of infected tissue (Alvin et al. 2014). Induction of plant defense mechanisms by endophyte against pathogens is an attractive phenomenon and acts as control tool used in modern and sustainable farming methods (Martinez-Klimova et al. 2017).

6.2 What Is Endophyte? The most important use of the term ‘endophyte’ is for microorganisms whose intrusions are intangible (Kobayashi and Palumbo 2000). Although, their origin dates to the nineteenth century, its contemporary meaning differs from its original meaning (Carroll 1986). Today’s applications of this term have not been consistent and none have been accepted by all researchers. The definition has changed many times and numerous terms and definitions of endophytic fungi have been proposed by researchers. Carroll (1986), identified endophytes as cooperative fungi that occupy the aerial parts of living plant tissues, but do not cause any symptoms. This definition does not include plant pathogenic fungi and mycorrhizal fungi. Endophytes are closely related to plant pathogens but are of limited pathogenicity and may have evolved from plant pathogenic fungi. Petrini (1991) proposed a broader definition of endophytes than Carroll’s definition, which includes all living organisms living in plant organs and can partially occupy host plants without pathogenic effect. According to this definition, endogenous plant pathogens that live within the host tissue without symptoms, and have an epiphytic phase in their life cycle, are also endophytes. Wilson (1995) defined endophytes as fungi or bacteria that invade living plant tissues throughout or part of their life cycle and induce completely non-obvious, symptomatic, infection within the plant tissue. On the other hand, Sikora et al. (2007) noted that, endophytic fungi reside within the plant tissue and are useful for their host or have no effect on their host. A special term, ‘endophyte’ is used when we refer to microorganisms present in plants. They could be considered as bacteria or fungi or actinobacteria, which spend their whole or part of their life cycle in the inter or intracellular tissues of different plant parts (stems, petioles, roots, leaves) without causing any apparent diseases to their host plants (Singh 2019). According to the researchers, endophytic fungi have three classes. The first category is the pathogenic fungi that are in their non-pathogenic form in the other host plant, the second group belongs to fungi that are generally pathogenic, and the third group has mutated and become non-pathogenic fungi for example, Colletotrichum magna (Backman and Sikora 2008). In general, the definition of the term endophyte is varied in articles and books that have ever been published. But most mycologists use the term for fungi that can occupy living and internal host tissues and do not cause visible disease symptoms (Petrini 1991; Wilson 1995). Endophytes are microorganisms (mostly fungi and bacteria) that live in the interstitial and intracellular areas of healthy plant tissues at a specific time and can colonize without harming the host (Bacon et al. 2000; Strobel and Daisy 2003; Khan 2010). The presence of endophytes in plan ts can alter the food cycle and symbiotic composition,

6 Microbial Endophytes: New Direction to Natural Sources

127

ecosystem processes and are important for the structure, function, and health of the plant community (Molina-Montenegro et al. 2015) (Table 6.2).

6.3 Classification of Endophytic Fungi Fungal endophytes are a diverse group of microorganisms that are broadly divided into two groups, clavicipitaceous (C) and non-clavicipitaceous (NC) based on their life cycle, evolutionary dependence, host plant range, and ecological class function (De Silva et al. 2019). On the other hand, Clavicipitaceous endophytes (family of Clavicipitaceae) including Atkinsonella, Balansia, Balansiopsis, Echinodothis, Epichloe, Myriogenospora, Neotyphodium, and Parepichloe are usually associated with the herbaceous plants of the Poaceae family (De Silva et al. 2019). Nonclavicipitaceous endophytes such as Fusarium sp., Colletotrichum sp., Phomopsis sp. and Xylaria sp. are associated with several plants and does not spend their complete life cycle inside the host plant (De Silva et al. 2019; Rodriguez et al. 2009; Jayawardena et al. 2016). A significant attention on endophytes includes various disciplines because of their ability to switch between endophytic, pathogenic, and saprophytic lifestyles (De Silva et al. 2019; Rodriguez et al. 2009) (Table 6.3). Clavicipitaceous endophytes, live as intracellular symbionts are mainly transmitted from mother plants to off-spring and systematically grow in the leaves and stems, by vertical transfer from the mother plant to their off-spring. The off-spring are seed-borne and have systemic growth within the plant’s tissues (De Silva et al. 2019; Arnold et al. 2003; Santangelo et al. 2015). In contrast, endophytes associated with the foliage of woody plants are transmitted horizontally by sexual or asexual spores (De Silva et al. 2019; Arnold et al. 2003). The above examples confirm about the importance of endophytic fungi that are biological control agents. The next important question arises how endophytes reduce disease and pests.

6.4 Plant Defense Responses in Relation to Endophyte-Pathogen and Host Plant Sustainable agriculture can be achieved by reducing or eliminating chemical fertilizers and agrochemicals, which are resulting in harmful environmental impact. Recently, application of antagonist endophytes as biological control agents (BCA) has gained momentum and received special attention for plant diseases management with comparatively low negative impacts on the environment (De Silva et al. 2019). Symptom-free colonization of endophytes can be explained by the hypothesis of “balanced antagonism” (Kusari et al. 2012). Balanced adaptation between host and endophyte is maintained by avoiding activation of host defense, activation, and production of toxic metabolites by host. On the other hand, if plant defense becomes

strawberry tree (A. unedo)

Mahonia fortunei

Artemisia argyi

Artemisia argyi

Talaromyces pinophilus

Pleosporales sp.F46 &Bacillus wiedmannii Com1

Trichoderma koningiopsis QA-3,

Trichoderma koningiopsis QA-3,

Burkholderia stabilis Panax ginseng EB159 (PG159) Meyer

Picea glauca

Phialocephala scopiformis

Pyrrolnitrin

Vinale et al. (2017)

Sumarah and Miller (2009)

Zhou et al. (2014)

Taechowisan et al. (2006)

Tawfike et al. (2019)

Aboobaker et al. (2019)

Chen et al. (2019)

Reference

Aquatic pathogen Vibrio alginolyticus

Cylindrocarpon destructans

(continued)

Kim et al. (2020)

Shi et al. (2020)

Shi et al. (2020)

Staphylococcus aureus, Wang et al. Bacillus subtilis, Pseudomonas (2019) aeruginosa and Escherichia coli

Acyrthosiphon pisum

Choristoneura Fumiferana & Lambdina fiscellaria

14-hydroxykoninginin E, koninginin U and 14-ketokoninginin B Ceratobasidium cornigerum QDAU-8

15-hydroxy-1,4,5,6-tetra-epi-koninginin G

23R-hydroxy-(20Z,24R)-ergosta-4,6,8(14),20(22)-tetraen-3-one and (22E,24R)-ergosta-4,6,8(14),22-tetraen-3-one

3-O-methyl-funicone

Yellow pigment rugulosin

Antioxidant activity

Alpinia oxyphylla

Streptomyces sp.

2,6-dimethoxy terephthalic acid and yangjinhualine A

Antiinflammatory agents

5,7-dimethyloxy-4-p-methoxylphenylcoumarin and 5,7-dimethoxy-4-phenylcoumarin

S. aureus and E. coli

Alpinia galanga

Dibutyl phthalate (antimicrobial activity)

Aspergillus flavus

Target cells/microorganism

Streptomyces aureofaciens

Pelargonium sidoides root

Penicillium skrjabinii

Phosphate solubilization, siderophore production

Bioactive compounds

Anticancer and antitrypanosomal

Peanut (Arachis hypogaea L.)

Bacillus velezensis LDO2

Aspergillus flocculus Markhamia platycalyx stem

Host plant

Endophyte species

Table 6.2 Endophytes in plant life: action and significance

128 A. Ghasemnezhad et al.

Host plant

Phlegmariurus taxifolius

Polyalthia debilis (Pierre)

Quercus macranthera

Endophyte species

Fusarium sp.

Trichoderma polyalthiae

Neurospora udagawae

Table 6.2 (continued)

Staphylococcus aureus, Macabeo et al. Rhodoturula (2020) glutinisandcytotoxicity against KB3.1 cells

Udagawanones A and B (new α-pyrone)

Cruz-Miranda et al. (2020)

Reference

Staphylococcus saprophyticus, Nuankeaw Staphylococcus aureus, et al. (2020) Methicillin-Resistant S. aureus, Bacillus subtilis, Bacillus cereus, Salmonella typhimurium, Shigella sonnei, and Candida albicans

Treatment of Alzheimer disease

Target cells/microorganism

Violaceol I and II

Huperzine A

Bioactive compounds

6 Microbial Endophytes: New Direction to Natural Sources 129

130 Table 6.3 Endophyte classification

A. Ghasemnezhad et al. Non-clavicipitaceous (NC)

Clavicipitaceous (C)

Fusarium Colletotrichum Phomopsis Xylaria

Atkinsonella Balansia Balansiopsis Echinodothis Epichloe Myriogenospora Neotyphodium Parepichloe

active and fights with fungal agents, the fungus will not be able to colonize plant tissues (De Silva et al. 2019; Kusari et al. 2012; Suryanarayanan et al. 2016). Further, plants produce an array of secondary metabolites against weeds and pathogens. As known, fungi and bacteria produce specialized enzymes and secondary metabolites to overcome these plant defense barriers and defend to cause disease, if pathogenic. For example, endophytic fungi produce toxic compounds, while plants produce antifungal metabolites such as condensed tannins (Schulz et al. 1999; Randriamanana et al. 2018). Some endophytes become pathogens when they are influenced by certain intrinsic and environmental factors to express the factors that lead to pathogenesis (Kusari et al. 2012). The above said phenomenon is common due to excessive moisture or nutrient deficiencies that alter the susceptibility of the host to the natural conditions (De Silva et al. 2019; Fisher and Petrini 1992). Endophyte, such as Epichloe festucae express the mitogen-activated protein kinase (sakA) gene to maintain interaction with the host Lolium perenne (perennial ryegrass). If the fungus is unable to express the gene, the endophyte becomes pathogenic and or disadvantaged in environmental conditions (De Silva et al. 2016). It has recently been observed that gene conferring secondary metabolite production in fungi is non-expressible in pure culture and can be activated in dual experiments with antagonist microbes (De Silva et al. 2019). Fungi act as stimulator for host defense via two mechanisms: (i) acquired systemic resistance (SAR) and (ii) inducible systemic resistance (ISR) (De Silva et al. 2019; Busby et al. 2016). Other various mechanisms of antagonistic activity of an BCA have been described as mycoparasitism, lytic and/or antibiotic production, induction of plant defense, and competition for nutrients and ecological niches (De Silva et al. 2019; Busby et al. 2016). Plant defense responses include altering the biochemistry of cell wall, producing pathogenesis-related proteins (PR), and/or generating specific resistance ISR. In natural conditions, BCAs must tolerate a wider range of climatic factors (temperature, humidity, UV light), soil (soil type), and biotic agents (antagonists), that are not ruling-out under laboratory conditions (Chow et al. 2019). As a result, the levels of defense enzymes are unlikely remain stable at elevated levels and are likely to decrease after several hours or days (Chow et al. 2019). Evidence suggests that endophyte colonization reproduces plant gene expression, reducing physiological

6 Microbial Endophytes: New Direction to Natural Sources

131

and biological stresses, improving plant nitrogen utilization, and altering host development (Chow et al. 2019, Dupont et al. 2015). However, the underlying mechanisms of interaction between endophyte BCA, host plant, and pathogen at the transcriptional level remain largely unknown (Chow et al. 2019). Consequently, plant–endophyte interaction involves complex and precise controlled interactions that balance host defense, fungal virulence, and production of secondary metabolites (De Silva et al. 2019) (Table 6.4). Table 6.4 Plant defense responses in relation to endophyte-pathogen and host plant Endophyte kind of endophyte

Biological effect

Results

References

Epichloe festucae

Activation of stress induced protein kinases

Resistance against stress

De Silva et al. (2019)

Endophyte

Lytic and/or antibiotic enzymes

Resistance against stress and diseases

De Silva et al. (2019)

Endophyte

Cell wall alteration, production of proteins associated with pathogenesis (PR) and/or specific resistance (ISR)

Balancing inappropriate plant conditions

De Silva et al. (2019)

endophytic rhizobacteria

Changes in Resistance against plantphysiological stress droughttolerance mechanisms, up-regulation of specific abiotic stress responsivegenes

Govindasamy et al. (2020)

Trichoderma asperellum T1 Productionof volatile antifungal compounds

Antifungal activity against leaf spot fungi C. cassiicola and C. aeria, inducing defense response, and promoting plant growth

Wonglom et al. (2020)

Colletotrichum tropicale

Inducing the expression of Greater plant hundreds of host immunity defense-related genes

Mejía et al. (2014)

Arthrobacter agilis UMCV2

Emission of dimethylhexadecylamine, a volatile compound that induces plant iron uptake mechanisms

Promoting plant growth

Aviles-Garcia et al. (2016)

Bacillus sp.TP1LA1B and Pantoea sp. AP1SA1

Production of phytohormones, siderophores, and organic acids

Improve plant growth and overall fitness

Purushotham et al. (2020)

132

A. Ghasemnezhad et al.

6.5 Plant Growth Stimulating Endophytic Bacteria Even, Dharni et al. (2014) and Ma et al. (2016) noted that it is known that PGPB participates in plant growth-promotion and heavy-metal phytoremediation. Various workers resumed that there is little knowledge about plant endophytic bacteria interactions and their potential role in phytoremediation (He et al. 2013; Chen et al. 2014; Babu et al. 2015; Ma et al. 2015). Phetcharat and Duangpaeng (2012) named these bacteria as plant growth-promoting endophytic (PGPE) bacteria and suggested the role of internal colonization for plant-propagation, enhancement of soil fertility, and stimulation of host plant growth by plant growth regulators production. It also has been demonstrated by Ma et al. (2011) that endophytic bacteria may help host plants to adapt under unfavorable environmental conditions and increase the phytoremediation efficiency, promoting the plant growth, alleviating the metal stress, reducing metal phytotoxicity, and finally altering the metal bioavailability and translocation inside the plants. Plant growth-promoting bacteria are a broad group of bacteria that are present in the soil rhizosphere and enter into root-cells and tissues under complex signaling mechanisms. A group of these bacteria called ‘endophyte–s’ which are able to reach toward plant host using chemotaxis, and enter into plant tissues through the lenticels, wounds caused by trichome breaks, stomata, exit zone of lateral roots and the area of root radical (Hallmann et al. 1997; 1998). These microorganisms grow in the apoplast or simplest space of plant root tissues without causing obvious damage (Gimenez et al. 2007). They often proliferate in the intercellular space of the root or may enter the peripheral circular cells. These develop systemic-infection and enter into parenchymal cells (Hallmann et al. 1997; 1998). Specific genetic systems are then activated between the bacterium and plant (Hardoim et al. 2008). The above symbiotic bacteria provide various benefits, such as increased level of resistance to stress and improvement of plant growth conditions (Dheeman et al. 2017). This relationship provides a balance between the plant and endophyte, but if environmental conditions are manipulated in favor of endophyte, the endophyte becomes pathogenic to disturb homeostasis drastically (Aly et al. 2010). There are various ways by which bacterial endophytes can confer resistance or tolerance to the host plant from different biotic and abiotic stresses (Santoyo et al. 2016). Endophytic bacteria utilize the nutrients, assimilated in plants and stabilizing nitrogen in-turn. These are also involved in production of 2-, 3-butanol, and acetone (Sturz et al. 2000), as well as secreting hormones such as ethylene, auxin, cytokinin, gibberellin, etc. By the production of terpenoids, flavonoids, isoflavonoids they help plant in developing resistance against pathogens and counter-acting environmental stresses. In addition to these, endophytic bacteria produce antifungal compounds, i.e., siderophore, which enhance iron-absorption, competition for food, limiting ecological-niche, and favoring plant-resistance mechanisms. Hence, it is worthy to understand that, PGPR is an important player of biological control (Hardoim et al. 2008; Jha et al. 2013). Research on Chinese medicinal plant Ferula songorica revealed that this plant is a rich reservoir of endophytic bacteria with an ability to solubilize phosphate and producing enzymes such as protease and cellulose (Yadav

6 Microbial Endophytes: New Direction to Natural Sources

133

et al. 2020). In the endophytic relationship, microbes provide a unique opportunity indirectly for control of the deleterious impact of phytopathogens on health of plant and soil, via synthesis of innumerable compounds, for example, antibiotics, immunesuppressants, biocontrol agents, hydrogen cyanide (HCN), and ammonia, induced systemic tolerance, production of hydrolytic enzymes (Yadav et al. 2017). In addition, few endophytic bacteria are also used in genetic engineering to transfer specific genes to the host plant (Tomasino et al. 1995). Endophytic microbes can maintain sustainable agriculture, i.e., enhanced the health, yield, productivity of plants via numerous independent or linked mechanisms. There are many reports on isolation of endophytic bacteria from roots, stems, leaves, seeds, needles, twigs, and barks of different plant species and their agricultural applications (Yadav et al. 2020). Nitrogen-fixing endophytes make up a small portion of the total population of endophytes and they are mainly considered for nitrogen fixation. Nitrogen-fixing endophytes have been found in seed and root of some rice cultivars (Mano and Morisaki 2008). Recently, more focus is laid on the isolation and identification of nitrogen-fixing endophytic bacteria in cereal crops (Verma et al. 2015, 2019).

6.6 Biodiversity of Bacterial Endophytes Previous reviews have described the diversity of bacterial endophytes in multiple plant species, especially those with agronomical interest (Rosenblueth and MartínezRomero 2006). More recently, Romero et al. (2014) demonstrated the power of the 16S-rRNA pyrosequencing approach in determining the position of endophytic bacterial communities in tomato. The endophyte communities were mainly comprised of five phyla, with Proteobacteria as the most highly represented as 90%. Other phyla detected were actinobacteria by 1.5%, Planctomycetes 1.4%, Verrucomicrobia 1.1%, and Actinobacteria is only about 0.5%. In addition, the dynamics of endophytic bacterial communities of sugar beet (Beta vulgaris L.) with different plant genotypes and plant growth stage changes was recently analyzed by PCR-based llumina pyrosequencing (Shi et al. 2014). The most abundant division was the Proteobacteria, with 98% of the total microbial endophyte community being composed of Enterobacteriales, Pseudomonadales, Xanthomonadales, Rhizobiales, Sphingomonadales, Burkholderiales, Actinomycetales, and flavobacteriales. In general, the Phylum Proteobacteria, including the classes α, β, and γ -Proteobacteria, are reported to be dominant in diversity analysis of endophytes. Although, members of the Firmicutes and Actinobacteria are also among this classes as most consistently found as endophytes. Other classes such as Bacteroidetes, Planctomycetes, Verrucomicrobia, and Acidobacteria are less commonly found as endophytes. The most commonly found genera of bacterial endophytes are Pseudomonas, Bacillus, Burkholderia, Stenotrophomonas, Micrococcus, Pantoea, and Microbacterium (Romero et al. 2014; Rosenblueth and Martínez-Romero 2006; MarquezSantacruz et al. 2010; Shi et al. 2014). All these genera, described as bacterial

134

A. Ghasemnezhad et al.

endophytes, are also common inhabitants of the rhizosphere. Therefore, it has been suggested that the endophyte microbiome may be a sub-population of the rhizosphere inhabiting bacteria (Marquez-Santacruz et al. 2010). The genus Pseudomonas is ubiquitous in nature and part of the core endo-microbiome of many plants ranging from model plants like Arabidopsis thaliana to medicinal plants like Cannabis sativa. Pseudomonas sp. can confer unique characteristics to the host plant and are well known for plant (Purushotham et al. 2020). More than 300 endophytic actinobacteria and bacteria belonging to the genera Streptomyces, Nocardiopsis, Brevibacterium, Microbacterium, Tsukamurella, Arthrobacter, Brachybacterium, Nocardia, Rhodococcus, Kocuria, Nocardioides, Pseudonocardia etc., were isolated from different tissues of Dracaena cochinchinensis Lour. (a traditional Chinese medicine known as dragon’s blood). Of these, 17 strains having antimicrobial and anthracyclines-producing activities also showed antifungal and cytotoxic activities against two human cancer cell lines, MCF-7 and Hep G2 (Salam et al. 2017). The majority of endophytic bacteria produce different kinds of antibiotics. Ecomycin, pseudomycins, and kakadumycins are some of the novel antibiotics produced by endophytic bacteria (Christina et al. 2013).

6.7 Interactions of Endophytes and the Host Plant Importantly, similar to any other living organism, plants are flexible and can adapt themselves and integrate with a different environment by strategically facing external stresses. For instance, the healthy growth and complex adaptive response of plants, often categorized as an intelligent response by a few authors (Chamovitz 2018), is associated with this world of microbes. It is intriguing to note that even after 500 million years of evolution, plants still need the assistance of the endophytic community to be able to resist stress tolerance including climate change and adapt themselves to their continuously changing environments (Deng and Cao 2017). This adaptation behavior is directly buttressed by the production of bioactive compounds known as secondary metabolites (Singh 2019). The endophytes survive on the nutrients produced by the plants and in return, these endophytes yield functional metabolites for their host plants. There is a positive linear relationship between endophytes and their host plants in terms of the production of these bioactive compounds (Palanichamy et al. 2018). Since endophytic fungal elicitors belong to extracellular materials and cannot directly enter the cell to play a role, the process of endophytic fungal elicitors to influence the secondary metabolism of plant cells through signal pathways will first identify and bind to the plant specific receptors on the cell membrane, change the structure of the cell to promote the production of specialized intracellular messenger substances. These messenger substances can regulate the expression of related genes in the nucleus through a series of signal transduction pathways. Finally, the defensive secondary metabolic system is activated, and the synthesis of secondary metabolites (Yan et al. 2020). Hernández-Soberano et al.

6 Microbial Endophytes: New Direction to Natural Sources

135

(2020) described Arthrobacter agilis UMCV2 and Bacillus methylotrophicus M496 as bacteria that stimulate plant growth in vitro. A. agilis UMCV2 behaves as an endophytic bacterium of Medicago truncatula (Aviles-Garcia et al. 2016) and promotes plant growth by emission of dimethylhexadecylamine, a volatile compound that induces plant iron uptake mechanisms and systemic resistance (Raya-González et al. 2017), and modulates plant morphogenesis (Castulo-Rubio et al. 2015; VázquezChimalhua et al. 2019). B. methylotrophicus M4-96 promotes growth in Arabidopsis and strawberries by emission of the phytostimulant volatile compound acetoin, and the production of the plant growth regulators (PGR), indole acetic acid and gibberellic acid (Pérez-Flores et al. 2017; Vicente-Hernández et al. 2019). Because, endophytes reside within plants and are continuously interacting with their hosts, it is conceivable that plants would have a substantial influence on the in planta metabolic processes of the endophytes. For example plants homoserine and asparagine act as host signals to activate expression of a lethal gene in virulent strains of Nectria hematococca that is only expressed in planta. Furthermore, expression of the gene cluster for lolitrem biogenesis in endophytic Neotyphodium lolii resident in perennial ryegrass is high in planta, but low to undetectable in fungal cultures grown in vitro, lending support to the notion that plant signaling is required to induce expression (Young et al. 2006). Another convincing example is that of the symbiotic association between dicotyledonous plants (Convolvulaceae) and clavicipitaceous fungi leading to synthesis of ergoline alkaloids by the fungus, and question the origin of these compounds in plants (Leistner and Steiner 2009). Recently, it was found that a camptothecin-producing endophyte, F. solani isolated from C. acuminata, could indigenously produce the precursors of camptothecin. However, a host plant enzyme absent in the fungus, strictosidine synthase, was employed in planta for the key step in producing camptothecin. This was the main reason for substantial reduction of camptothecin production on subculturing under axenic conditions. Such plant-fungus interactions compel reconsidering whether horizontal gene transfer (plant to endophyte genome or vice versa) is the only mechanism by virtue of which endophytes produce associated plant compounds (Kusari et al. 2012). The production of natural products by endophytic fungi, once considered exclusive to plants, also raises intriguing questions regarding the original source organism. Actually, it is possible that various so-called ‘plant metabolites’ could in fact be the biosynthetic products of their endophytes. An important example is the production of the very potent antitumor maytansinoid ansamitocin, originally isolated from higher plants, by the actinobacteria Actinosynnema pretiosum ssp. auranticum (Yu et al. 2002). This study substantiated the possibility that the true biosynthetic source of the maytansinoid backbone could be a bacterial endophyte. Although, horizontal gene transfer may explain the production of maytansinoids by plants, a more likely scenario is the production of maytansinoids by symbionts. Because, the interaction between endophytic fungi with the host plant and other endophytes remains versatile, even slight variations in the in vitro cultivation conditions can impact the kind and range of secondary metabolites they produce. It is well established that the metabolic processes of microorganisms are critically dependent on the culture parameters. This is especially exemplified by endophytes because their range of interactions is so

136

A. Ghasemnezhad et al.

broad. For example, the plant associated Paraphaeosphaeria quadriseptata starts producing six new secondary metabolites when only the water used to make the media is changed from tap water to distilled water (Kusari et al. 2012).

6.8 Endophytes and Abiotic Stresses Human activities such as smelting, mining, electroplating, refineries, fertilizer use and fungicides, sewage sludge have accumulated heavy metals such as cadmium (Cd) in natural resources, soil and climate. The accumulation of Cd in plants causes severe damage to the cell membrane, organelle and nucleus as a result of reduced metabolism, photosynthesis and absorption of water and nutrients. In addition, Cd enrichment in crops can pose a risk to human health (Tang et al. 2019). Recently, studies on plant growth-promoting endophytes have shown the potential role of selected endophytes for improving plant growth, development and mineral uptake, and resistance to stress under harsh environmental conditions (Tang et al. 2019) (Fig. 6.3). The Acinetobacter guillouiae EU-B2RT.R1 with multifarious plant growthpromoting activity has emerged as one of the efficient biofertilizers that need to be explored for sustainable agriculture (Rana et al. 2020). Li et al. (2007) reported that Gram-negative Burkholderia cepacia increased biomass, metal uptake, and tolerance index in S. alfredii. Xinxian et al. (2011) isolated 14 endophytic strains from S. alfredii roots and demonstrated that stimulatory activity of plant growth was associated with heavy metal accumulation in different plant organs in response to metal stress. Similar results with B. juncea (Belimov et al. 2005), Salix caprea L. (Kuffner et al. 2008), and H. Annus (Kolbas et al. 2015) were obtained. Similarly K. rhizophila has been reported as a bio-sorbent for cadmium (Cd) and chromium (Cr) and can remove metal ions from aqueous solutions. Metal-resistant bacteria increase plant growth and accumulation of heavy metals in plant organisms in association with application (EDTA) (Afridi et al. 2019) (Table 6.5).

Fig. 6.3 Positive effect of endophyte coexistence with poplar seedlings (Khan et al. 2016)

6 Microbial Endophytes: New Direction to Natural Sources

137

Table 6.5 Endophytes and abiotic stresses Endophyte

Biological role

References

Burkholderia cepacia

Increasing biomass, metal uptake, and tolerance index

Li et al. (2007)

K. rhizophila

Inducing the uptake of Cd and Cr Afridi et al. (2019)

Bacillus pumilus

Improving salinity tolerance and Khan et al. (2016a, b) alleviating heavy metals toxicity

Bacillus pumilus

Enhancing drought stress resistance

Xie et al. (2019)

Scenedesmus obliquus, Euglena Detoxification of DDT, parathion Ardal (2014) gracilis Chlamydomonas sp.

Detoxification of Lindane, naphthalene, phenol

Bacillus cereus strain XMCr-6

Alleviating heavy metals toxicity Dong et al. (2013) (Cr)

Aspergillus fumigatus

Alleviating heavy metals toxicity Kumar et al. (2011) (Pb)

Acinetobacter calcoaceticus

Nitrogenase activity and enhancing the capability of growing under nitrogen-limited conditions

Doty et al. (2009)

Pantoea alhagi

Improving growth and drought tolerance

Chen et al. (2017)

Acinetobacter guillouiae EUB2RT. R1

Increasing biomass, enhancing Fe and Zn content

Rana et al. (2020)

Epichloe gansuensis

tolerate physiological conditions Ahmad et al. (2020) i.e. salinity, pH, temperature, photoperiod and light variation

Calvibacter sp.

Improving chilling tolerance

Ding et al. (2011)

Group strains of Bacillus, Microbacterium, and Halomonas

Biodegradation Textile effluent

Wang et al. (2017)

Bacillus thuringiensis GDB-1

Alleviating heavy metals toxicity Wang et al. (2018) (As, Cu, Pb, Ni, and Zn)

Aspergillus sp. A31, C. geniculata P1, Lindgomycetaceae P87 and Westerdykella sp. P71

Mercury resistance and bioremediation

Pietro-Souza et al. (2020)

Other studies of endophyte–plant cooperation in stressful conditions reveal good results. For example, endophytes help pepper plants tolerate nitrogen deficiency conditions (Fig. 6.4). In other studies, resistant endophyte species were detected in the seeds of C4 and CAM plants from resistant strains of C4 and CAM plants of the phylum Firmicutes. These bacteria are known to be involved in the thermal

138

A. Ghasemnezhad et al.

Fig. 6.4 Comparison of un-inoculated and endophyte-inoculated pepper plants under nitrogen deficiency conditions (Khan et al. 2012)

regulation and protection of plants through enzymes, antibiotic synthesis, and strong adaptation to C4 and CAM plants (Girsowicz et al. 2019). Plant growth-promoting bacteria (PGPB), a type of endophyte bacteria, are extremely capable of adjusting physiological responses to water deficiency, which ensures plant survival in stressful conditions. Bacillus pumilus is an important PGPB that plays a key role in improving salt-tolerance of rice (Khan et al. 2016b) and alleviating metal toxicity in tomatoes (Khan et al. 2016a). Drought stress resistance of Glycyrrhiza uralensis (Fisch) was improved by B. pumilus, possibly through increased activity of antioxidant enzymes and improved synthesis of glycyrrhizic acid, which is associated with the expression of proteins like HMGR, SQS, and β-AS (Xie et al. 2019). Colonization of B. amyloliquefaciens SB9 was also able to counteract the adverse effect of salt and drought-induced stresses by reducing the production of malondialdehyde (MDA) and reactive oxygen species (ROS) in grape-wine roots (Jiao et al. 2016). There have been a large number of studies (Glick 2010, 2014; BecerraCastro et al. 2013; Sessitsch et al. 2013; Muehe et al. 2015) indicating that plantassociated microorganisms are indeed essential players in metal phytoextraction or phytomining, enhancing the plant growth and health by the increase of nutrient uptake and improving their resistance to pathogens and stress (Lugtenberg and Kamilova 2009). It is known that most of the phosphate-solubilizing bacteria and siderophore producers, bacteria with ACC deaminase activity and phytohormone producers, improve plants’ growth and transform heavy metals into soluble and bioavailable forms, favoring that plants take up contaminants (Ullah et al. 2015; Guerrero-Zúñiga et al. 2020). Thus, these kinds of bacteria can assist in the phytoremediation of heavy metals, either directly or indirectly: directly involving the solubilization and removal of them from solid matrices, such as soil, dumps, sediments, and other industrial and municipal wastes, giving more bioavailability and final accumulation by plants, and indirectly, by the improvement of plants’ growth to prevent the

6 Microbial Endophytes: New Direction to Natural Sources

139

effect of phytopathogens, facilitating the accumulation of heavy metals (Glick 2010; Guerrero-Zúñiga et al. 2020).

6.9 Antimicrobial Activity of Endophytes Endophytes are recognized as valuable sources of biologically active secondary metabolites and various structures. However, most of their gene clusters are still silent, indicating a greater biosynthetic potential for the production of diverse metabolites. Several methods have been developed to activate biosynthetically silent gene clusters in order to produce hidden natural products. One of them is co-cultivation that is recognized as a powerful way to enhance chemical diversity. A reason why the structural diversity of natural products is expanding is the interspecific interference among microorganisms, especially those that reside in a similar ecological environment (Wang et al. 2019). Trait propagation, e.g., antibiotic production, through activating biosynthetically silent gene clusters is typically associated with interspecific interference. Wang et al. (2019) isolated, detected, and biologically assessed a new derivative of ergosterol (23R-hydroxy-(20Z,24R)-ergosta-4,6,8(14),20(22)tetraen3-one) and a biosynthetically known compound from the co-cultivation of the endophytic fungus Pleosporales sp. F46 and the endophytic bacterium Bacillus wiedmannii sp., both residing in the medicinal plant Mahonia fortune. This is the first ergosterol derivative with a double Z20 bond in the side chain and shows strong antibacterial activity. Peanut endophyte Bacillus velezensis LDO2 is highly capable of synthesizing various antimicrobial metabolites and shows strong antagonistic activities against fungal and bacterial pathogens of peanut. The gene clusters responsible for their antifungal metabolites (fengycin, surfactin, and bacilysin) and antibacterial metabolites (butirosin, bacillaene, difficidin, macrolactin, surfactin, bacilysin) were detected (Chen et al. 2019). Li et al. (2016) investigated the antifungal activity of crude extracts of 93 endophytic fungi, isolated from five kinds of tissues of Zanthoxylum bungeanum on F. sambucinum and P. zanthoxyli. Another study on strawberry plants revealed that the soil application of endophyte in the strawberry medium improved growth conditions and viability of the plants significantly (Fig. 6.5). Aboobaker et al. (2019) were the first to report Penicillium skrjabinii as an endophyte that synthesizes dibutyl phthalate. This compound contributes to endophytic– host plant interactions and has an antimicrobial effect against S. aureus and E. coli. Fructose and peptone are the best sources of carbon and nitrogen for the production of most antimicrobial metabolites of PG159. Biological metabolites synthesized by bacteria are generally regarded as bio-pesticides. Bacterial metabolites contain bioactive compounds with antagonistic activities such as pyrrolnitrin, phenazine, cepabactin, and other unknown compounds. Pyrrolnitrin is produced as a fungicide against soil-borne fungal pathogens, such as Rhizoctonia solani that is the cause of seedling death (Kim et al. 2019). Cui et al. (2020) reported that the healthy potatoes can carry endophytic bacterium which have the antagonistic ability against potato

140

A. Ghasemnezhad et al.

Fig. 6.5 The effect of the fungus Beauveria bassiana as an endophyte on strawberries (Dara and Dara 2015)

diseases. The antagonistic bacteria B. velezensis strain 8-4 could control not only potato scab, but also potato anthracnose, gangrene, blight, and black shank as a broad-spectrum antagonistic agent with potential applications in the disease control (Cui et al. 2020). Worldwide, powdery mildew (PM) is a common disease of plants caused by obligate biotrophic fungal pathogens (Liang et al. 2018). Bacillus spp. have been found to be effective biocontrol agents of PM (Panstruga and Kuhn 2019). Jakuschkin et al. (2016) also found that endophytes Mycosphaerella punctiformis and Monochaetia kansensis have antagonistic activities against oak PM. Clark et al. (2014) reported that the extract of Seimatosporium sp. isolated from the Canadian medicinal plant Hypericum perforatum exhibited better antifungal and antimycobacterial activity. Spry et al. (2018) also found that the fermentation broth of Seimatosporium sp. CL28611 displayed excellent anti-plasmodial activity in vitro. Zhao et al. (2020) reported that the isolate Seimatosporium sp. M7SB 41 from the PM resistance Rosa variety may play an important role in host plant PM resistance through producing some antimicrobial metabolites.

6 Microbial Endophytes: New Direction to Natural Sources

141

6.10 Endophytic Bioactive Alkaloids Endophytes are an active source of bioactive alkaloids that protect their host plants. The positive effect of Epichloë endophytes on plant defense has been traditionally attributed to fungal alkaloids. Alkaloids are nitrogen-rich compounds, four groups of which have been detected in endophytes: ergot alkaloids (e.g., ergopeptine and ergovaline), indole-diterpene (e.g., lolitrem B and epoxy-janthitrem), pyrrolizidine (e.g., lolines), and pramine. All enzymes involved in their synthesis are encoded in the fungal genome and all biosynthetic pathways are mainly defined. Alkaloid profiles depend on the species and strain of endophyte and the amount of alkaloids is related to plant phenological stage, plant tissue, and environmental conditions. In addition, the effectiveness of an alkaloid defense against an invader depends on the concentration and chemical type of the alkaloid produced by the endophyte (Bastias et al. 2017). Endophytic Bacillus cereus, Aranicola proteolyticus, Serratia liquefaciens, Bacillus thuringiensis, and Bacillus licheniformis isolated from Pinellia ternata have the ability to produce alkaloids (guanosine and inosine) in fermentation broth similar to their host plant (Liu et al. 2015). The capsular endophyte Acinetobacter SB1B in Opium poppy unregulated the expression of key genes for the benzylisoquinoline alkaloid (BIA) biosynthesis except thebaine and codeine. In contrast, Marmoricola sp. SM3B, another endophyte, could up-regulate the biosynthesis of both thebaine and codeine. Acinetobacter and Marmoricola sp. as microbial inoculants modulated the alkaloid producing genes in Opium poppy (Pandey et al. 2016). The impairment of the cholinergic neurotransmission in the central nervous system is one of the bases of memory deficit related to Alzheimer’s disease (AD), with the administration of acetylcholinesterase (AChE) inhibitors representing the most acceptable strategy for treating this illness. Huperzine A (Hup A) is an alkaloid, which was first isolated from the Chinese Huperzia serrata (Thunb. ex Murray) Trev., and gained attention due to its potent, reversible, and selective inhibition of AChE. Furthermore, the molecule penetrates the hemato-encephalic barrier more effectively, has greater oral bioavailability and the AChE inhibitory action lasts longer than other commercial drugs (donepezil and rivastigmine) (wang et al. 2006; Cruz-Miranda et al. 2020). For this reason, in the last few years, there is an increased interest in the discovery of a microbial source with the potential to produce Hup A. Some reports have described fungal endophytes that were isolated from different species of lycophytes producing Hup A. The fungi Shiraira sp. SIf14, Cladosporium cladosporioides, and Colletotrichum gloeosporioides ES026 were isolated from H. serrata (Shu et al. 2014), whereas the endophytic fungi Ceriporialacerata and Hypoxylon investiens were isolated from Phlegmariurus phlegmaria (Zhang et al. 2015; Cruz-Miranda et al. 2020). Some endophytic fungi can produce the same bioactive compounds as their host plants, e.g., camptothecin, hypericin, vinblastine, paclitaxel, podophyllotoxin, and diosgenin. For example, Taxomyces andreanae is an endophytic fungus isolated from the Taxus brevifolia tree and has the potential to produce the anticancer compound Taxol. In addition, endophytic fungi can produce the antidepressant hypericin and

142

A. Ghasemnezhad et al.

Table 6.6 Some endophyte fungi as a medicinal source Endophyte

Medicinal compound

References

Cylindrocarpon lucidum

Immunosuppressant cyclosporine

Abdel-Azeem et al. (2019)

Tolypocladium inflatum

Immunosuppressant cyclosporine

Abdel-Azeem et al. (2019)

Aspergillus terreus

Lovastatin

Abdel-Azeem et al. (2019)

Penicillium sp.

Antibiotic penicillin

Abdel-Azeem et al. (2019)

Chaetomium globosum

Anti-rheumatoid activity

Abdel-Azeem et al. (2016)

Taxomyces andreanae

Taxol

Stierle et al. (1993)

Acremonium sp.

Paclitaxel (Taxol)

El-Bialy and El-Bastawisy (2020)

Pestalotiopsis microspora

Paclitaxel (Taxol)

Kusari et al. (2014)

Fusarium solani

Camptothecin (topoisomerase inhibitor)

Kusari et al. (2012)

Actinomycete Actinosynnema pretiosum ssp. auranticum

Maytansinoid ansamitocin

Yu et al. (2002)

Diaporthe sp.

Diaporone A (new dihydroisocoumarin), α-dibenzopyrones

Guo et al. (2020)

Fusarium sp.

Huperzine A

Cruz-Miranda et al. (2020)

Ceriporia lacerata

Huperzine A

Zhang et al. (2015)

Trichoderma polyalthiae

Violaceol I and II

Nuankeaw et al. (2020)

B. amyloliquefaciens SB-9

Melatonin

Jiao et al. (2016)

Streptomyces Strain MS-6-6

Treponemycin (Anti-tuberculous)

Mahmoud et al. (2015)

Streptomyces sp. MK932-CF8

Androprostamines (Anti-prostate cancer)

Yamazaki et al. (2015)

Pseudomonas syringae

Pseudomycin

McEvoy et al. (2016)

emodin, deoxypodophyllotoxin, antineoplastic camptothecin (CPT), as well as the natural insecticides azadirachtin A and B (Table 6.6).

6.11 Endophytes in Agriculture and Medicine: Future Prospects Since the emergence of mankind, plants have always been a major nutritional source, along with animals, for us so that they have been used as a source of food and treatment. Today, given the industrial development and population growth in most countries, land fragmentation into small parcels has reduced farmlands and crop

6 Microbial Endophytes: New Direction to Natural Sources

143

production, which has had negative impacts in the face of population growth. As such, the application of proper and optimal management practices for the efficient use of lands has drawn the attention of scientific circles. On the other hand, it can be useful to apply methods that can improve production efficiency. Producers are always concerned about the limiting factors of crop production, e.g., adverse climatic and nutritional conditions, pathogens, and spatial limitations. As already described, endophytes are bacteria or fungi that penetrate a plant and influence it positively without creating disease symptoms (although they may turn out to be pathogenic in some unfavorable growth conditions) (Wilson 1995). In this regard, it is important and practical to understand endophytes, their relationships with their host, and their various ecological and nutritional needs (Nair and Padmavathy 2014). Since endophytes can be present in different parts of a plant, this is an advantage for us as we will not be restricted in their application (Pirttilä et al. 2000, 2003). In the first place, various studies have been carried out on endophyte symbiosis with plants in agriculture, suggesting different ways to isolate endophytes (Hallmann et al. 1997; Reinhold-Hurek and Hurek 1998). It is important to answer the questions as to how to extract endophytes, how to cultivate them, and where to cultivate them to obtain them in great deals. This encompasses different environments, research on which is underway and should be expanded in the future (Rai et al. 2007; Hata and Sone 2008). Based on the research already conducted, some endophytes can be applied in production processes (Table 6.7). Today, given the change of climates in the world and the diversity of agricultural production sites, the climatic conditions should always be considered (Nair and Padmavathy 2014). For example, a study showed that changes in climatic conditions and the resulting changes in plant size may affect endophyte abundance (Rai et al. 2007; Chareprasert et al. 2006). In this light, future research should focus on the ecological requirements of endophytes to figure out the optimal conditions for the individual endophytes. Research on endophytes has been undertaken in a variety of fields, and environmental conditions should be properly assessed to obtain better results. Given the modern advances in biotechnology, endophytes can be presented as an important and useful tool. Diverse studies have addressed using endophytes as molecular markers and transporter genes. In addition to these roles, their beneficial side effects can be utilized for the benefit of the plants (Dheeman et al. 2017). The technology needs developments in the consideration of science expansion and well-being of humans (Nair and Padmavathy 2014; Araujo et al. 2002). It is known that plants need a wide range of elements for survival and the deficiency of any of these elements can influence their growth and production negatively. Some important agriculture-related measures can be enumerated as endophytes in nutrient uptake, balanced establishment, stress-free conditions for plants, and production of secondary metabolites those are not just limited to farming but also expanded into other biological fields, like in biological control, organic farming, antimicrobial compound, synthesis of important enzymes, and in tissue culture as major tool in agriculture (Nair and Padmavathy 2014). Overall, endophytes can be considered as plant contributors, their roles are not limited to a single field but encompass various sequential fields. On the other hand, with respect to the close relationship of medical

144

A. Ghasemnezhad et al.

Table 6.7 Some fungi used as endophytes in different plants (Nair and Padmavathy 2014) Endophytes

Plant species

References

Phomopsis sp.

Neolitsea sericea

Santangelo et al. (2015)

Pasania edulis

Arnold et al. (2003)

Ginkgo biloba L.

Mano and Morisaki (2008)

Tectona grandis and Samanea saman Merr.

Tomasino et al. (1995)

Taxus chinensis

Stone et al. (2000)

Cladosporium sp.

Opuntia ficus indica

Hallmann et al. (1998)

Cinnamomum camphora

Zhao et al. (2010)

C. herbarum

Lycopersicum esculentum Mill.

Pirttilä et al. (2003)

Triticum aestivum

Hallmann et al. 1997

Triticum aestivum

Hallmann et al. 1997

Colletotrichum sp.

Citrus plants

Belimov et al. (2005)

Cinnamomum camphora

Zhao et al. (2010)

Pasania edulis

Arnold et al. (2003)

Ginkgo biloba L.

Mano and Morisaki (2008)

Tectona grandis and Samanea saman Merr.

Tomasino et al. (1995)

Huperzia serrate

Porter et al. (1976)

Cinnamomum camphora

Zhao et al. (2010)

C. gloeosporiodes

Lycopersicum esculentum Mill.

Pirttilä et al. (2003)

Phyllosticta sp.

Citrus sp.

Belimov et al. (2005)

Pasania edulis

Arnold et al. (2003)

Coffea Arabica

Reinhold-Hurek and Hurek (1998)

Centella asiatica

Rai et al. (2007)

Panax quinquefolium

Hata and Sone (2008)

Ginkgo biloba L.

Mano and Morisaki (2008)

Lycopersicum esculentum Mill.

Pirttilä et al. (2003)

Huperzia serrate

Porter et al. (1976)

Taxus chinensis

Stone et al. (2000)

Huperzia serrate

Belimov et al. (2005)

Trichoderma koningiopsis QA-3,

Artemisia argyi

Shi et al. (2020)

Fusarium solani

C. acuminata

Kusari et al. (2012)

Diaporthe sp.

Pteroceltis tatarinowii Maxim.

Guo et al. (2020)

Ceriporia lacerata

Phlegmariurus phlegmaria

Zhang et al. (2015)

Aspergillus versicolor strain Eich.5.2.2

Eichhornia crassipes

Ebada and Ebrahim (2020)

Penicillium sp. Acremonium sp.

(continued)

6 Microbial Endophytes: New Direction to Natural Sources

145

Table 6.7 (continued) Endophytes

Plant species

References

Bacillus sp. TP1LA1B and Pantoea sp. AP1SA1

Pseudowintera colorata

Purushotham et al. (2020)

science and agriculture, these can supply active and pharmaceutical ingredients for disease prevention and cure, endophytes can be a good topic of research in medical science too. For example, they have a high potential in the production of raw material for drugs as they produce antimicrobial compounds and bioactive compounds that have beneficial pharmacological effects. A reason for the importance of plantderived endophytes is their antimicrobial role, which can be effective in both plants and animals (Sette et al. 2006; Kumar et al. 2011). For example, 18 compounds from Tectona grandis L. and 37 compounds from Samanea saman Merr have antibacterial activities (Chareprasert et al. 2006). In addition, endophytes have biological constituents that can be used in targeted drug delivery. Some of them can also be effective as anticancer and immune enhancer compounds (Joseph and Priya 2011). Some major medicinal compounds (Fig. 6.6), which have been derived from endophytes and have anti-pathogenic and medicinal activities, include Maytansinoids (Pullen et al. 2003), Siderophores, etc. (Neilands 1993), Taxol as an important compound in the treatment of cancers, and Huperzine A (Liu et al. 2009). Acremonium sp. showed the presence of BAPT gene that is responsible for paclitaxel production and encoding C-13 phenylpropanoid side chain-acetyl coenzyme A acetyltransferase. Therefore, the selected endophyte has an individual metabolic system that can be activated in the absence of the host or changing its ecology (El-Bialy and El-Bastawisy 2020). Nuankeaw et al. (2020) showed the broad spectrum of violaceol which had the potential antimicrobial activities against human pathogens. This is the first report of phenol violaceol produced by a species of Trichoderma. Pyrrolnitrin is a broad-spectrum antibiotic produced by many strains of the genera Burkholderia, Pseudomonas, Enterobacter, Acinetobacter, Myxococcus, Serratia

Fig. 6.6 Chemical structures of some bioactive compounds produced by endophytic microorganisms (a) Taxol (b) Huperzine A

146

A. Ghasemnezhad et al.

etc. (Mujumdar et al. 2014; Kim et al. 2020). Pyrrolnitrin is also an important antimicrobial agent for plant protection (Dheeman et al. 2017). The mode of action of pyrrolnitrin is not clear, but interference in fungal plasma membranes has been demonstrated. Four genes in chromosomal DNA (6.2-kb region) are responsible for pyrrolnitrin production in Pseudomonas fluorescens, while plasmid-encoded genes are responsible in Acinetobacter haemolyticus A19 (Kim et al. 2020). Endophytic bacterial strain, EML-CAP3 isolated from Capsicum Annum L. (red pepper) leaf, showed potent antiangiogenic activity. This endophytic bacterial strain produced lipophilic peptides which inhibited the proliferation of human umbilical vein endothelial cells and also exhibited antiangiogenic potential in tumor progression (Jung et al. 2015). In general, endophytes have many unsolved mysteries, each of which can add to human knowledge and make it easier for human beings to deal with anomalies in various fields.

References Abdalla MA, Matasyoh JC (2014) Endophytes as producers of peptides: an overview about the recently discovered peptides from endophytic microbes. Nat Prod Bioprospect 4(5):257–270. https://doi.org/10.1007/s13659-014-0038-y Abdel-Azeem AM, Abdel-Azeem MA, Khalil WF (2019) Endophytic fungi as a new source of antirheumatoid metabolites. In: Bioactive food as dietary interventions for arthritis and related inflammatory diseases, pp 355–384 Abdel-Azeem AM, Zaki SM, Khalil WF, Makhlouf NA, Farghaly LM (2016) Anti-rheumatoid activity of secondary metabolites produced by endophytic Chaetomium globosum. Front Microbiol 7:1477 Aboobaker Z, Viljoen A, Chen W, Crous PW, Maharaj VJ, van Vuuren S (2019) Endophytic fungi isolated from Pelargonium sidoides DC: antimicrobial interaction and isolation of a bioactive compound. South Afr J Bot 122:535–542. https://doi.org/10.1016/j.sajb.2019.01.011 Afridi MS, Mahmood T, Salam A et al (2019) Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: involvement of ACC deaminase and antioxidant enzymes. Plant Physiol Biochem 139:569–577. https://doi.org/10.1016/j.plaphy.2019.03.041 Ahmad RZ, Khalid R, Aqeel M, Ameen F, Li CJ (2020) Fungal endophytes trigger Achnatherum inebrians germination ability against environmental stresses. South Afr J Bot. https://doi.org/10. 1016/j.sajb.2020.01.004 Alvin A, Miller KI, Neilan BA (2014) Exploring the potential of endophytes from medicinal plants as sources of antimycobacterial compounds. Microbiol Res 169(7–8):483–495. https://doi.org/ 10.1016/j.micres.2013.12.00 Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41(1):1–16 Araújo WL, Marcon J, Maccheroni W, van Elsas JD, van Vuurde JW, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68(10):4906–4914 Ardal E (2014) Phycoremediation of pesticides using microalgae. Department of Plant Breeding. SLU, Swedish University of Agricultural Sciences, Alnarp 10–35 Arnold AE, Mejía LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci 100(26):15649–15654

6 Microbial Endophytes: New Direction to Natural Sources

147

Aviles-Garcia ME, Flores-Cortez I, Hernández-Soberano C, Santoyo G, Valencia-Cantero E (2016) The plant growth-promoting rhizobacterium Arthrobacter agilis UMCV2 endophytically colonizes Medicago truncatula. Rev Argent Microbiol 48(4):342–346. https://doi.org/10.1016/j.ram. 2016.07.004 Babu AG, Shea PJ, Sudhakar D, Jung IB, Oh BT (2015) Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal(loid)-contaminated mining site soil. J Environ Manag 151:160–166 Backman PA, Sikora RA (2008) Endophytes: an emerging tool for biological control. Biol Control 46(1):1–3 Bacon CW, White JF, Stone JK (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, pp 29–33 Bastias DA, Martínez-Ghersa MA, Ballaré CL, Gundel PE (2017) Epichloë fungal endophytes and plant defenses: not just alkaloids. Trends Plant Sci 22(11):939–948. https://doi.org/10.1016/j.tpl ants.2017.08.005 Becerra-Castro C, Kidd P, Kuffner M et al (2013) Bacterially induced weathering of ultramafic rock and its implications for phytoextraction. Appl Environ Microbiol 79:5094–5103 Becerra-Castro C, Monterroso C, Prieto-Fernández A et al (2012) Pseudometallophytes colonizing Pb/Zn mine tailings: a description of the plant-microorganism-rhizosphere soil system and isolation of metal-tolerant bacteria. J Hazard Mater 217–218:350–359 Belimov AA, Hontzeas N, Safronova VI et al. (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37(2): 241–250 Busby PE, Ridout M, Newcombe G (2016) Fungal endophytes: modifiers of plant disease. Plant Mol Biol 90(6):645–655 Carroll GC (1986) The biology of endophytism in plants with particular reference to woody perennials. Microbiol Phyll 203–222 Castulo-Rubio DY, Alejandre-Ramírez NA, del Carmen Orozco-Mosqueda M, Santoyo G, MacíasRodríguez LI, Valencia-Cantero E (2015) Volatile organic compounds produced by the rhizobacterium Arthrobacter agilis UMCV2 modulate Sorghum bicolor (strategy II plant) morphogenesis and SbFRO1 transcription in vitro. J Plant Growth Regul 34(3):611–623. https://doi.org/10.1007/ s00344-015-9495-8 Chamovitz DA (2018) Plants are intelligent; now what? Nat Plants 4:622–623 Chareprasert S, Piapukiew J, Thienhirun S, Whalley AJ, Sihanonth P (2006) Endophytic fungi of teak leaves Tectona grandis L. and rain tree leaves Samanea saman Merr. World J Microbiol Biotechnol 22(5):481–486 Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y et al (2017) Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 7:41564. https://doi.org/10.1038/srep41564 Chen L, Luo SL, Li XJ, Wan Y, Chen JL, Liu CB (2014) Interaction of Cd hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308 Chen L, Shi H, Heng J, Wang D, Bian K (2019) Antimicrobial, plant growth-promoting and genomic properties of the peanut endophyte Bacillus velezensis LDO2. Microbiol Res 218:41–48. https:// doi.org/10.1016/j.micres.2018.10.002 Chow YY, Rahman S, Ting ASY (2019) Evaluating the host defense responses in oil palm to complex biocontrol endophyte-pathogen-host plant interaction via Fluidigm® real-time polymerase chain reaction (RT-PCR). Biol Control 129:148–157. https://doi.org/10.1016/j.biocontrol.2018.10.011 Christina A, Christapher V, Bhore SJ (2013) Endophytic bacteria as a source of novel antibiotics: an overview. Pharmacog Rev 7:11–16. https://doi.org/10.4103/0973-7847.112833 Clark TN, Bishop AI, McLaughlin M, Calhoun LA, Johnson JA, Gray CA (2014) Isolation of (−)-avenaciolide as the antifungal and antimycobacterial constituent of a Seimatosporium sp. Endophyte from the medicinal plant Hypericum perforatum. Nat Prod Commun 9:1495–1496

148

A. Ghasemnezhad et al.

Cruz-Miranda OL, Folch-Mallol J, Martínez-Morales F, Gesto-Borroto R, Villarreal ML, Taketa AC (2020) Identification of a Huperzine A-producing endophytic fungus from Phlegmariurus taxifolius. Mol Biol Rep 47(1):489–495. https://doi.org/10.1007/s11033-019-05155-1 Cui L, Yang C, Wei L, Li T, Chen X (2020) Isolation and identification of an endophytic bacteria Bacillus velezensis 8-4 exhibiting biocontrol activity against potato scab. Biol Control 141:104– 156 Dara SK, Dara SR (2015) Soil application of the entomopathogenic fungus, Metarhizium brunneum protects strawberry plants from spider mite damage. In: UCANR eNewsletter strawberries and vegetables. Available via DIALOG. https://ucanr.edu/blogs/strawberries-vegetables/index.cfm? start=54. Accessed 18 Feb 2015 De Silva N, Lumyong S, Hyde KD, Bulgakov T, Phillips AJ, Yan JY (2016) Mycosphere essays 9: defining biotrophs and hemibiotrophs 7(5):545–559 De Silva NI, Brooks S, Lumyong S, Hyde KD (2019) Use of endophytes as biocontrol agents. Fungal Biol Rev 33(2):133–148. https://doi.org/10.1016/j.fbr.2018.10.001 Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106 Dharni S, Srivastava AK, Samad A, Patra DD (2014) Impact of plant growth promoting Pseudomonas monteilii PsF84 and Pseudomonas plecoglossicidas F610 on metal uptake and production of secondary metabolite (monoterpenes) by rose-scented geranium (Pelargonium graveolens cv. bourbon) grown on tannery sludge amended soil. Chemosphere 117:433–439 Dheeman S, Maheshwari DK, Baliyan N (2017) Bacterial endophytes for ecological intensification of agriculture. In: Maheshwari D (eds) Endophytes: biology and biotechnology. Sustainable development and biodiversity, vol 15. Springer, Cham, pp 193–231. https://doi.org/10.1007/9783-319-66541-2_9 Ding S, Huang C, Sheng H, Song C, Li Y, Li A (2011) Effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plant 141:141–151 Dong G, Wang Y, Gong L, Wang M, Wang H, He N, Zheng Y, Li Q (2013) Formation of soluble Cr (III) end-products and nanoparticles during Cr (VI) reduction by bacillus cereus strain XMCr-6. Biochem Eng J 70:166–172 Doty SL, Oakley B, Xin G, Kang JW, Singleton G, Khan Z et al (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 47(1):23–33 Dupont PY, Eaton CJ, Wargent JJ et al (2015) Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol 208(4):1227–1240 Ebada SS, Ebrahim W (2020) A new antibacterial quinolone derivative from the endophytic fungus Aspergillus versicolor strain Eich. 5.2. 2. S Afr J Bot El-Bialy HA, El-Bastawisy HS (2020) Elicitors stimulate paclitaxel production by endophytic fungi isolated from ecologically altered Taxus baccata. J Rad Res Appl Sci 13(1):79–87 Fisher PJ, Petrini O (1992) Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L.). New Phytol 120(1):137–143 Gangwar M, Dogra S, Gupta UP, Kharwar RN (2014) Diversity and biopotential of endophytic actinomycetes from three medicinal plants in India. Afr J Microbiol Res 8(2):184–191 Gimenez C, Cabrera R, Reina M, Gonzalez-Coloma A (2007) Fungal endophytes and their role in plant protection. Curr Org Chem 11(8):707–720 Girsowicz R, Moroenyane I, Steinberger Y (2019) Bacterial seed endophyte community of Annal plants modulated by plant photosynthetic pathways. Microbiol Res 223:58–62 Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374 Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39 Golinska P, Wypij M, Agarkar G, Rathod D, Dahm H, Rai M (2015) Endophytic actinobacteria of medicinal plants: diversity and bioactivity. Antonie Van Leeuwenhoek 108(2):267–289

6 Microbial Endophytes: New Direction to Natural Sources

149

Govindasamy V, George P, Kumar M et al (2020) Multi-trait PGP rhizobacterial endophytes alleviate drought stress in a senescent genotype of sorghum [Sorghum bicolor (L.) Moench]. 3 Biotech 10(1):13. https://doi.org/10.1007/s13205-019-2001-4 Guerrero-Zúñiga AL, López-López E, Rodríguez-Tovar AV, Rodríguez-Dorantes A (2020) Functional diversity of plant endophytes and their role in assisted phytoremediation. In: Bharagava R, Saxena G (eds) Bioremediation of industrial waste for environmental safety. Springer, Singapore, pp 237–255 Guo L, Niu S, Chen S, Liu L (2020) Diaporone A, a new antibacterial secondary metabolite from the plant endophytic fungus Diaporthe sp. J Antibiot 73(2):116–119 Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43(10):895–914 Hallmann J, Quadt-Hallmann A, Rodriguez-Kbana R, Kloepper JW (1998) Interactions between meloidogyne incognita and endophytic bacteria in cotton and cucumber. Soil Biol Biochem 30(1):925–937 Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends microbial 16(10):463–471 Hata K, Sone K (2008) Isolation of endophytes from leaves of Neolitsea sericea in broadleaf and conifer stands. Mycoscience 49(4):229–232 He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965 Hernández-Soberano C, Ruíz-Herrera LF, Valencia-Cantero E (2020) Endophytic bacteria Arthrobacter agilis UMCV2 and Bacillus methylotrophicus M4-96 stimulate achene germination, in vitro growth, and greenhouse yield of strawberry (Fragaria× ananassa). Scientia Horticulturae 261:109005 Hussain MA, Mahajan V, Rather IA et al (2017) Isolation and identification of growth promoting endophytes from Artemisia Anna L. and its effects on artemisinin content. Trends Phytochem Res 1(4):207–214 Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33(163):173 Jakuschkin B, Fievet V, Schwaller L, Fort T, Robin C, Vacher C (2016) Deciphering the pathobiome: intra- and interkingdom interactions involving the pathogen Erysiphe alphitoides. Microb Ecol 72:870–880 Jayawardena RS, Hyde KD, Damm U et al (2016) Notes on currently accepted species of Colletotrichum. Mycosphere 1192–1260 Jha PN, Gupta G, Jha P, Mehrotra R (2013) Association of rhizospheric/ endophytic bacteria with plants: a potential gateway to sustainable agriculture. Gr J Agric Sci 3(2):73–84. https://doi.org/ 10.15580/GJAS.2013.2.010313354 Jiao J, Ma Y, Chen S, Liu C, Song Y, Qin Y et al (2016) Melatonin producing endophytic bacteria from grapevine roots promote the abiotic stress-induced production of endogenous melatonin in their hosts. Front Plant Sci 7:1387 Joseph B, Priya RM (2011) Bioactive compounds from endophytes and their potential in. Am J Biochem Mol Biol 1(3):291–309 Jung HJ, Yonghyo K, Hyang BL, Kwon HJ (2015) Antiangiogenic activity of the lipophilic antimicrobial peptides from an endophytic bacterial strain isolated from Red Pepper leaf. Mol Cells 38:273–278 Khan A, Ali L, Chaudhary HJ, Munis MFH, Bano A, Masood S (2016a) Bacillus pumilus alleviates boron toxicity in tomato (Lycopersicum esculentum L.) due to enhanced antioxidant enzymatic activity. Sci hort 200:178–185 Khan A, Zhao XQ, Javed MT, Khan KS, Bano A, Shen RF, Masood S (2016b) Bacillus pumilus enhances tolerance in rice (Oryza sativa L.) to combined stresses of NaCl and high boron due to limited uptake of Na+ . Environ Exp Bot 124:120–129 Khan S (2010) Resistance mechanism in plants under stress conditions. Am J Sci 6:34–41

150

A. Ghasemnezhad et al.

Khan Z, Guelich G, Phan H, Redman R, Doty S (2012) Bacterial and yeast endophytes from poplar and willow promote growth in crop plants and grasses. ISRN Agron Khan Z, Rho H, Firrincieli A et al (2016c) Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Curr Plant Biol 6:38–47 Kim H, Mohanta TK, Park YH et al (2020) Complete genome sequence of the mountain-cultivated ginseng endophyte Burkholderia stabilis and its antimicrobial compounds against ginseng root rot disease. Biol Control 140:104126 Kim H, Rim SO, Bae H (2019) Antimicrobial potential of metabolites extracted from ginseng bacterial endophyte Burkholderia stabilis against ginseng pathogens. Biol Control 128:24–30 Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (eds) Microbial Endophytes. Marcel Dekker, New York, pp 199–236 Kolbas A, Kidd P, Guinberteau J, Jaunatre R, Herzig R, Mench M (2015) Endophytic bacteria take the challenge to improve Cu phytoextraction by sunflower. Environ Sci Pollut Res 22(7):5370–5382 Korzekwa K (2015) News Releases. In: Probiotics—for plants. American Society of Agronomy. Available via DIALOG. https://www.agronomy.org/news/media-inquiries/releases. Accessed 8 July 2015 Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A (2008) Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304(1–2):35–44 Kumar A, Bisht BS, Joshi VD, Dhewa T (2011) Review on bioremediation of polluted environment: a management tool. Int J Environ Sci 1(6):1079–1093 Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19(7):792–798 Kusari S, Singh S, Jayabaskaran C (2014) Rethinking production of Taxol (Paclitaxel) using endophyte biotechnology. Trends Biotechnol 32:304–311. https://doi.org/10.1016/j.tibtech.2014. 03.011 Larran S, Simón MR, Moreno MV, Siurana MPS, Perelló A (2016) Endophytes from wheat as biocontrol agents against tan spot disease. Biol Control 92:17–23 Leistner E, Steiner U (2009) Fungal Origin of Ergoline Alkaloids Present in Dicotyledonous Plants (Convolvulaceae). In: Anke T, Weber D (eds) Physiology and Genetics. The Mycota (A comprehensive treatise on fungi as experimental systems for basic and applied research). Springer, Berlin, Heidelberg, pp 197–208 Li P, Wu Z, Liu T, Wang Y (2016) Biodiversity, phylogeny and antifungal functions of endophytic fungi associated with Zanthoxylum bungeanum. Int J Mol Sci 17:1541–1564. https://doi.org/10. 3390/ijms17091541 Li WC, Ye ZH, Wong MH (2007) Effects of bacteria on enhanced metal uptake of the Cd/Znhyperaccumulating plant, Sedum alfredii. J Exp Bot 58(15–16):4173–4182 Liang P, Liu S, Xu F, Jiang S, Yan J, He Q et al (2018) Powdery mildews are characterized by contracted carbohydrate metabolism and diverse effectors to adapt to obligate biotrophic lifestyle. Front Microbiol 9:3160 Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. J Ind Microbiol Biotech 36(9):1171–1177 Liu Y, Liu W, Liang Z (2015) Endophytic bacteria from Pinellia ternata, a new source of purine alkaloids and bacterial manure. Pharm Biol 5:1545–1548. https://doi.org/10.3109/13880209.101 6580 Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556 Ma Y, Oliveira RS, Nai FJ, Rajkumar M, Luo YM, Rocha I, Freitas H (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69 Ma Y, Rajkumar M, Luo YM, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants effects on plant growth and Ni uptake. J Hazard Mater 195:230–237

6 Microbial Endophytes: New Direction to Natural Sources

151

Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25 Macabeo AP, Cruz AJ, Narmani A, Arzanlou M, Babai-Ahari A, Pilapil LA, Garcia KY, Huch V, Stadler M (2020) Tetrasubstituted α-pyrone derivatives from the endophytic fungus, Neurospora udagawae. Phytochem Lett 35:147–151 Mahmoud AY, Abdallah HM, El-Halawani MA, Jiman-Fatani AAM (2015) Anti-tuberculous activity of Treponemycin produced by a Streptomyces strain MS-6-6 isolated from Saudi Arabia. Molecules 20:2576–2590. https://doi.org/10.3390/molecules20022576 Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microb Environ 23(2):109–117 Marquez-Santacruz HA, Hernandez-Leon R, Orozco-Mosqueda MD, Velazquez-Sepulveda I, Santoyo G (2010) Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Genet Mol R 9(4):2372–2380 Martinez-Klimova E, Rodríguez-Peña K, Sánchez S (2017) Endophytes as sources of antibiotics. Biochem Pharmacol 134:1–7. https://doi.org/10.1016/j.bcp.2016.10.010 McEvoy A, O’Regan F, Fleming CC et al (2016) Bleeding canker of horse chestnut (Aesculus hippocastanum) in Ireland: incidence, severity and characterization using DNA sequences and real-time PCR. Plant Pathol 65:1419–1429 Mejía LC, Herre EA, Sparks JP et al (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 5:479 Molina-Montenegro MA, Oses R, Torres-Díaz C, Atala C, Núñez MA, Armas C (2015) Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem. Perspect Plant Ecol 17(3):218–226 Muehe EM, Weigold P, Adaktylou IJ et al (2015) Rhizosphere microbial community composition affects cadmium and zinc uptake of the metalhyperaccumulating plant Arabidopsis halleri. Appl Environ Microbiol 81:2173–2181 Mujumdar SS, Bashetti SP, Chopade BA (2014) Plasmid pUPI126-encoded pyrrolnitrin production by Acinetobacter haemolyticus A19 isolated from the rhizosphere of wheat. World J Microbiol Biotechnol 30:495–505. https://doi.org/10.1007/s11274-013-1426-x Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J Neilands JB (1993) Perspectives in biochemistry and biophysics-siderophores. Arch Biochem Biophys 302:1–3 Nuankeaw K, Chaiyosang B, Suebrasri T, Kanokmedhakul S, Lumyong S, Boonlue S (2020) First report of secondary metabolites, Violaceol I and Violaceol II produced by endophytic fungus, Trichoderma polyalthiae and their antimicrobial activity. Mycoscience 61(1):16–21. https://doi. org/10.1016/j.myc.2019.10.001 Palanichamy P, Krishnamoorthy G, Kannan S, Marudhamuthu M (2018) Bioactive potential of secondary metabolites derived from medicinal plant endophytes. Egypt J Basic Appl Sci 5:303– 312 Pandey SS, Singh S, Babu CSV, Shanker K, Shrivastava NK, Kalra A (2016) Endophytes of opium poppy differentially modulate host plant productivity and genes for the biosynthetic pathway of benzylisoquinoline alkaloids. Planta 243:1097–1114 Panstruga R, Kuhn H (2019) Microreview: mutual interplay between phytopathogenic powdery mildew fungi and other microorganisms. Mol Plant Pathol 20:463–470 Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J et al (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254:2201–2213. https://doi.org/10. 1007/s00709-017-1109-9 Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Brock/Springer Series in Contemporary Bioscience, Springer, New York, NY, pp 179–197 Phetcharat P, Duangpaeng A (2012) Screening of endophytic bacteria from organic rice tissue for indole acetic acid production. Procedia Eng 32:177–183

152

A. Ghasemnezhad et al.

Pietro-Souza W, de Campos Pereira F, Mello IS (2020) Mercury resistance and bioremediation mediated by endophytic fungi. Chemosphere 240:124874 Pirttilä AM, Laukkanen H, Pospiech H, Myllylä R, Hohtola A (2000) Detection of intracellular bacteria in the buds of scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66(7):3073–3077 Pirttilä AM, Pospiech H, Laukkanen H, Myllylä R, Hohtola A (2003) Two endophytic fungi in different tissues of Scots pine buds (Pinus sylvestris L.). Microb Ecol 45(1):53–62 Porter JR (1976) Antony van Leeuwenhoek: tercentenary of his discovery of bacteria. Bacteriol rev 40(2):260 Pullen CB, Schmitz P, Hoffmann D et al (2003) Occurrence and non-detectability of maytansinoids in individual plants of the genera Maytenus and Putterlickia. Phytochem 62(3):377–387 Purushotham N, Jones E, Monk J, Ridgway H (2020) Community structure, diversity and potential of endophytic bacteria in the primitive New Zealand medicinal plant Pseudowintera colorata. Plants 9(2):156 Rai R, Dash PK, Prasanna BM, Singh A (2007) Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World J Microbiol Biotechnol 23(6):853–858 Rana KL, Kour D, Kaur T et al (2020) Endophytic microbes from diverse wheat genotypes and their potential biotechnological applications in plant growth promotion and nutrient uptake. Proc Natl Acad Sci, India Sect B Biol Sci 18:1–11 Randriamanana TR, Nissinen K, Ovaskainen A et al (2018) Does fungal endophyte inoculation affect the responses of aspen seedlings to carbon dioxide enrichment? Fungal Ecol 33:24–31 Raya-González J, Velázquez-Becerra C, Barrera-Ortiz S, López-Bucio J, Valencia-Cantero E (2017) N, N-dimethyl hexadecylamine and related amines regulate root morphogenesis via jasmonic acid signalling in Arabidopsis thaliana. Protoplasma 254:1399–1410. https://doi.org/10.1007/s00709016-1031-6 Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends Microbiol 6(4):139–144 Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330 Romero FM, Marina M, Pieckenstain FL (2014) The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS microbiology letters 351(2):187–194 Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19(8):827–837 Salam N, Khieu T, Liu M et al. (2017) Endophytic actinobacteria associated with Dracaena cochinchinensis Lour.: isolation, diversity, and their cytotoxic activities. BioMed Res Int. https:// doi.org/10.1155/2017/1308563 Santangelo JS, Turley NE, Johnson MT (2015) Fungal endophytes of Festuca rubra increase in frequency following long-term exclusion of rabbits. Bot 93(4):233–241 Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growthpromoting bacterial endophytes. Microbiol Res 183:92–99 Schulz B, Römmert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103(10):1275–1283 Sessitsch A, Kuffner M, Kidd P et al (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194 Sette LD, Passarini MRZ, Delarmelina C, Salati F, Duarte MCT (2006) Molecular characterization and antimicrobial activity of endophytic fungi from coffee plants. World J Microbiol Biotechnol 22(11):1185–1195 Shi XS, Li HL, Li XM et al (2020) Highly oxygenated polyketides produced by Trichoderma koningiopsis QA-3, an endophytic fungus obtained from the fresh roots of the medicinal plant Artemisia argyi. Bioorganic Chem 94:103448. https://doi.org/10.1016/j.bioorg.2019.103448

6 Microbial Endophytes: New Direction to Natural Sources

153

Shi Y, Yang H, Zhang T, Sun J, Lou K (2014) Illumina-based analysis of endophytic bacterial diversity and space-time dynamics in sugar beet on the north slope of Tianshan mountain. Appl Microbiol Biotechnol 98(14):6375–6385 Shu S, Zhao X, Wang W, Zhang G, Cosoveanu A, Ahn Y, Wang M (2014) Identification of a novel endophytic fungus from Huperzia serrata which produces huperzine A. World J Microbiol Biotechnol 30(12):3101–3109. https://doi.org/10.1007/s11274-014-1737-6 Sikora RA, Schäfer K, Dababat AA (2007) Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas Plant Path 36(2):124–134 Singh BP (2019) Advances in endophytic fungal research: present status and future challenges, 1st edn. Springer, Switzerland Spry C, Sewell AL, Hering Y, Villa MV, Weber J, Hobson SJ et al (2018) Structure-activity analysis of CJ-15,801 analogues that interact with Plasmodium falciparum pantothenate kinase and inhibit parasite proliferation. Eur J Med Chem 143:1139–1147 Stierle A, Strobel G, Stierle D (1993(Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Sci 260:214–216 Stone JK, Bacon CW, White JF (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF (eds) Microbial endophytes. Dekker, New York, pp 3–30 Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502 Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19(1):1–30 Sumarah MW, Miller JD (2009) Anti-insect secondary metabolites from fungal endophytes of conifer trees. Nat Prod Commun 4(11):1497–1504 Suryanarayanan TS, Rajulu G, Vidal S (2016) Biological control through fungal endophytes: gaps in knowledge hindering success. Curr Biotechnol 5:1–13 Taechowisan T, Wanbanjob A, Tuntiwachwuttikul P, Taylor WC (2006) Identification of Streptomyces sp. Tc022, an endophyte in Alpinia galanga, and the isolation of actinomycin D. Ann Microbiol. 2006(56):113–117. https://doi.org/10.1007/BF03174991 Tang L, Hamid Y, Sahito ZA, Gurajala HK, He Z, Yang X (2019) Effects of CO2 application coupled with endophyte inoculation on rhizosphere characteristics and cadmium uptake by Sedum alfredii Hance in response to cadmium stress. J Environ Manage 239:287–298 Tawfike AF, Romli M, Clements C et al (2019) Isolation of anticancer and anti-trypanosome secondary metabolites from the endophytic fungus Aspergillus flocculus via bioactivity guided isolation and MS based metabolomics. J Chromatogr B 1106:71–83. https://doi.org/10.1016/j. jchromb.2018.12.032 Tomasino SF, Leister RT, Dimock MB, Beach RM, Kelly JL (1995) Field performance of Clavibacter xyli subsp. cynodontis expressing the insecticidal protein gene cryIA (c) of Bacillus thuringiensis against European corn borer in field corn. Biol Control 5(3):442–448 Ullah A, Heng S, Farooq M, Munis H, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40 Vázquez-Chimalhua E, Ruíz-Herrera LF, Barrera-Ortiz S, Valencia-Cantero E, López-Bucio J (2019) The bacterial volatile dimethyl-hexa-decylamine reveals an antagonistic interaction between jasmonic acid and cytokinin in controlling primary root growth of Arabidopsis seedlings. Protoplasma 256(3):643–654. https://doi.org/10.1007/s00709-018-1327-9 Verma P, Yadav AN, Khannam KS, Mishra S, Kumar S, Saxena AK et al (2019) Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of India. Saudi J Biol Sci 26(7):1882–1895. https://doi.org/10.1016/j.sjbs.2016.01.042 Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK et al (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65(4):1885–1899. https://doi.org/10.1007/s13213-014-1027-4 Vicente-Hernández A, Salgado-Garciglia R, Valencia-Cantero E et al (2019) Bacillus methylotrophicus M4-96 stimulates the growth of strawberry (Fragaria x ananassa “Aromas”) plants in vitro

154

A. Ghasemnezhad et al.

and slows Botrytis cinerea infection by two different methods of interaction. J Plant Growth Regul. https://doi.org/10.1007/s00344-018-9888-6 Vinale F, Nicoletti R, Lacatena F et al (2017) Secondary metabolites from the endophytic fungus Talaromyces pinophilus. Nat Prod Res 31(15):1778–1785 Wang L, Lin H, Dong YB et al (2018) Isolation of vanadiumresistanceendophytic bacterium PRE01 from Pteris vittata in stone coal smelting district and characterization for potential use in phytoremediation. J Hazard Mater 341:1–9 Wang R, Yan H, Tang XC (2006) Progress in studies of huperzine A, a natural cholinesterase inhibitor from Chinese herbal medicine. Acta Pharmacol Sin 27(1):1–26. https://doi.org/10.1111/j.17457254.2006.00255.x Wang YH, Li HH, Feng GJ et al (2017) Biodegradation of diuron by an endophytic fungus Neurospora intermedia DP8-1 isolated from sugarcane and its potential for remediating diuron-contaminated soils. PLoS One 12(8):e0182556 Wang ZR, Li G, Ji LX et al (2019) Induced production of steroids by co-cultivation of two endophytes from Mahonia fortunei. Steroids 145:1–4 Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73(2):274–276. https://doi.org/10.2307/3545919 Wonglom P, Ito SI, Sunpapao A (2020) Volatile organic compounds emitted from endophytic fungus Trichoderma asperellum T1 mediate antifungal activity, defense response and promote plant growth in lettuce (Lactuca sativa). Fungal Ecol 43:100867 Xie Z, Chu Y, Zhang W, Lang D, Zhang X (2019) Bacillus pumilus alleviates drought stress and increases metabolite accumulation in Glycyrrhiza uralensis Fisch. Environ Exp Bot 158:99–106. https://doi.org/10.1016/j.envexpbot.2018.11.021 Xinxian L, Xuemei C, Yagang C, Woon-Chung WJ, Zebin W, Qitang W (2011) Isolation and characterization endophytic bacteria from hyperaccumulator Sedum alfredii Hance and their potential to promote phytoextraction of zinc polluted soil. World J Microbiol Biotechnol 27(5):1197–1207 Yadav AN, Kumar R, Kumar S et al (2017) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5(6):45–57. https://doi.org/10.7324/JABB.2017.50607 Yadav AN, Singh J, Rastegari AA, Yadav N (2020) Plant microbiomes for sustainable agriculture. Springer, Cham Yamazaki Y, Someno T, Igarashi M, Kinoshita N, Hatano M, Kawada M et al (2015) Androprostamines A and B, the new anti-prostate cancer agents produced by Streptomyces sp. MK932-CF8. J Antibiot 68:279–285. https://doi.org/10.1038/ja.2014.135 Yan K, He L, Yang K (2020) Effects of SA and H2 O2 mediated endophytic fungal elicitors on essential oil in suspension cells of Cinnamomum longepaniculatum. Open Acc Lib J 7(1):1–12. https://doi.org/10.4236/oalib.1106009 Young CA, Felitti S, Shields K et al (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43:679–693 Yu TW, Bai L, Clade D et al (2002) The biosynthetic gene cluster of the maytansinoid antitumor agent ansamitocin from Actinosynnema pretiosum. Proc Natl Acad Sci USA 99:7968–7973 Zhang FF, Wang MZ, Zheng YX, Liu HY, Zhang XQ, Wu SS (2015) Isolation and characterization of endophytic huperzine A-producing fungi from Phlegmariurus phlegmaria. Microbiology 84(5):701–709. https://doi.org/10.1134/s0026261715050185 Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23(5):753–771. https://doi.org/10.1039/b609472b Zhao J, Zhou L, Wang J et al (2010) Endophytic fungi for producing bioactive compounds originally from their host plants. Curr Res, Technol Educ Trop Appl Microbiol Microbial Biotechnol 1:567– 576 Zhao Y, Ji XL, Shen T et al (2020) Fungal endophytic communities of two wild Rosa varieties and the role of an endophytic Seimatosporium sp. in enhancing host plant powdery mildew resistance. Plant Soil 3:1–12

6 Microbial Endophytes: New Direction to Natural Sources

155

Zhou H, Yang Y, Peng T, Li W, Zhao L, Xu L, Ding Z (2014) Metabolites of Streptomyces sp., an endophytic actinomycete from Alpinia oxyphylla. Natural Product Research 28(4):265–267

Chapter 7

Tropical Endophytic Bacillus Species Enhance Plant Growth and Nutrient Uptake in Cereals Camila Cristina Vieira Velloso, Vitória Palhares Ribeiro, Chainheny Gomes de Carvalho, Christiane Abreu de Oliveira, Ubiraci Gomes de Paula Lana, Ivanildo Evódio Marriel, Sylvia Morais de Sousa, and Eliane Aparecida Gomes Abstract Several abiotic factors, such as nutrient deficiency and drought, contribute to reducing agricultural productivity in the world. Plant growth-promoting bacteria can enhance crop growth and sustainable crop production. Bacillus is the most common genus within the Firmicutes group and one of the most predominant plants endophytic bacteria. Once established within the plant, the ability of these endophytes to promote plant growth occurs due to several mechanisms that include the acquisition of essential mineral nutrients and modulation of phytohormones. Especially in tropical ecosystems, the ability of endophytic microorganisms to colonize the internal tissues of plants suggests an ecological advantage. The post-genomic era is allowing the characterization of unknown genes and the identification of genes expressed during colonization. A better understanding of how beneficial bacteria colonize different plant niches will lead to more successful and reliable use of bacterial inoculants. The commercialization of bioinoculants is a reality, however, the exploration of the more efficient use of these nutrients have the potential to increase the field of the inoculants and create confidence among the farmers for their use. Keywords Endophytic bacteria · Phytohormones · Abiotic and biotic stresses · Inoculant

C. C. V. Velloso · V. P. Ribeiro · I. E. Marriel · S. M. de Sousa Universidade Federal de São João Del-Rei (UFSJ), Praça Dom Helvécio 74, São João del-Rei-MG, MG 36301-160, Brazil C. G. de Carvalho · C. A. de Oliveira · U. G. de Paula Lana · I. E. Marriel · S. M. de Sousa Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG 35701-242, Brazil C. A. de Oliveira · U. G. de Paula Lana · I. E. Marriel · S. M. de Sousa · E. A. Gomes (B) Embrapa Milho e Sorgo, Rodovia MG 424—Km 45—Caixa Postal 285, Sete Lagoas, MG 35701-970, Brazil e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_7

157

158

C. C. V. Velloso et al.

7.1 Introduction Cereals play an important role in the world’s agriculture economy, considering their area sown and annual production volume, being used as food, feed, and industry. Although maize, wheat, and rice are the most important to feed the world, other crops such as sorghum and millet are also relevant, especially in Asia and Africa (FAO 2019). The world’s population today is around 7 billion and is estimated to reach 9 billion by 2050. Challenges to feed the ever-growing population coupled with global climate change increase the need for sustainable and environmentally sound agricultural production (FAO 2019; Naumann et al. 2018; Ngumbi and Kloepper 2016). However, the productivity enhancement system is highly dependent on chemical inputs, especially nitrogen, phosphate, and potassium fertilizers (Ladha et al. 2016), which not only increases the production cost (Haygarth et al. 2014; Kvaki´c et al. 2018) but cause environmental adverse impacts such as groundwater pollution, soil degradation, micronutrient deficiency, eutrophication of water sources, toxicity to different beneficial organisms and plummeting of microbiota biodiversity, and overall management of ecology (Sharma and Singhvi 2017; Maheshwari and Annapurna 2017). Endophytic bacteria, microorganisms that spend at least part of their life cycle inside plants without causing apparent damage, have emerged as an economically and environmentally sustainable alternative to traditional methods. Microbial inoculants, characterized as products that contain strains of beneficial microorganisms to the plant growth and development, such as plant growth-promoting bacteria (PGPB) play an important role in the production of sustainable crops, reducing environmental impact and human health hazards. Various names have been given to PGPB according to their efficacy and use in plant ecosystem. Maheshwari (2010) has coined the term as plant growth- and health-promoting bacteria. Such organisms are capable to provide better adaptability and survival under biotic and abiotic stress conditions, and have the potential to mitigate the excessive use of pesticides and fertilizers in agriculture (Alori et al. 2017; Alori and Babalola 2018; Bashan et al. 2014; Singh et al. 2016). These are able to stimulate plant growth at different stages of development using direct mechanisms as phytohormones, enzyme production and nutrient uptake, and indirect mechanisms including biological control and induced systemic resistance (Nazir et al. 2018; Saini et al. 2015; Varma et al. 2017). Various workers consider the plant microbiome, i.e., the collective genomes of microorganisms living in association with plants, as a second genome, due to its close proximity between both partners and its impact on the host plant. It comprises a broad and diverse group of microorganisms, although most of them belong to relatively small phylogenetic group, comprising mainly of Firmicutes and Proteobacteria. The most important genera of Proteobacteria are Rhizobium, Agrobacterium, and Sphingomonas (α-proteobacteria); Burkholderia (β-proteobacteria); Enterobacter, Klebsiella, Pantoea, and Pseudomonas (γ-proteobacteria). Among all, Bacillus is the most common genus within the Firmicutes group followed by Paenibacillus and Staphylococcus (Wallace and May 2018; Rodriquez et al. 2019).

7 Tropical Endophytic Bacillus Species …

159

Members of the Bacillus are reported as one of the most predominant plant endophytic bacteria presenting several plant growth-promoting traits. Once established within the plant, the ability of these endophytes to promote plant growth occurs because of mechanisms that include the acquisition of essential nutrients (biofertilization), such as nitrogen (N), phosphorus (P), and potassium (K) (Fig. 7.1), the modulation of the level of phytohormones, essential for plant development (Calvo et al. 2010), such as auxins, cytokinins, gibberellins, etc. (Bhattacharyya et al. 2015; Pérez-Flores et al. 2017). In addition, other mechanisms include synthesis and excretion of antibiotics and enzymes proteases, chitinases, bacteriocins, production of siderophores, biofilms, secretion of exopolysaccharide, volatile organic compounds, and induction of systemic resistance (Barriuso et al. 2008; Santoyo et al. 2016; Walker et al. 2011). Bacillus is promising candidate for use as plant microbial inoculants due to important traits to alleviate or eliminate the negative effects of saline, drought, and oxidative stresses. In addition, sporulation of this bacterial genus promotes its survival under different environmental conditions, thus facilitating the adaptation of strains to commercial formulation and field application (Ghyselinck et al. 2013; Pinter et al. 2017; Tiwari et al. 2019). Therefore, the association of cereals, such as maize, wheat,

Fig. 7.1 Plant nutrient uptake (NPK) enhancement mediated by plant growth-promoting bacteria (PGPB)

160

C. C. V. Velloso et al.

rice, millet, and sorghum, with PGPB bacilli can increase productivity and food security, and reduce the use of agrochemicals and production costs contributing to a more sustainable agriculture. This chapter provides an overview of the importance of endophytic Bacillus from tropical soils associated with different cereals with main emphasis on plant nutrition.

7.2 Plant Colonizing Endophytic Bacteria Plant growth-promoting bacteria (PGPB) colonize the rhizosphere, the foliar surface (epiphytic) or the interior of plant tissue (endophytic) providing plants with nutrients and protection against biotic and abiotic stresses (Ahmad et al. 2008; Boddey et al. 2003; Doty et al. 2016; Franche et al. 2009; Santoyo et al. 2016; Maheshwari and Annapurna 2017). Although, most of the research on PGPB focuses on rhizobacteria, knowledge of endophytic bacteria has grown extensively in recent years creating a relatively new niche and very promising approach to the development of sustainable agriculture (Miliute et al. 2015; Santoyo et al. 2016; Xia et al. 2015). Currently, endophytic microorganisms have been reported from nearly all host plants studied, including crops of agronomic importance, natural and extreme conditions environments, wild and perennial plants (Nair and Padmavathy 2014; Yuan et al. 2014; Zinniel et al. 2002). Endophytic bacteria live, at least a part of their life cycle inside plants, apparently without causing any damage to their hosts (Assumpção et al. 2009), which differentiates them from phytopathogenic microorganisms. Even though roots have the highest number of endophytes compared to the shoot (Rosenblueth and Martínez-Romero 2006), endophytes have been isolated from flowers, fruits, leaves, stems, and seeds of various plant species (Kobayashi and Palumbo 2000; Melnick et al. 2008; Piccolo et al. 2010; Thomas et al. 2007). They present different mechanisms of colonization, particularly roots hence considered as a subgroup of rhizospheric bacteria that have acquired the ability to colonize plants without inducing the host defense pathway (Marquez-Santacruz et al. 2010; Misko and Germida 2002). Once within the plant, endophytic bacteria can exert a direct and more effective beneficial effect compared to rhizospheric bacteria due to consistent nutrient supply and, as they occupy the same habitat as phytopathogenic microorganisms, therefore efficient in disease control (Compant et al. 2010). In addition, being more competitive than non-endophytic microorganisms inside the host plant assist in the endophyte-plant interaction an evolutionary process controlled by genes of both organisms (Rosenblueth and Martínez-Romero 2006). According to life strategies, endophytes are classified as obligate or facultative organisms in nature. The obligate ones are those strictly dependent on the host plant for their growth and survival, usually transmitted by seeds and spread in the plant by vertical colonization or by the action of a vector. Facultative endophytes have some phases of the life cycle inside the host plant and another in which they live outside (Hardoim et al. 2008). They constitute the majority of endophytic microorganisms showing as characteristic of the biphasic lifestyle alternating between plant and

7 Tropical Endophytic Bacillus Species …

161

Fig. 7.2 Endophytic bacteria colonization. Bacteria can colonize plants entering roots cracks and wounds, or hydrolyzing root cells. Other pathways include stomata, particularly in young leaves and stems, lenticels, and germinating seeds

rhizospheric soil. The distinction between the rhizosphere population and endosymbionts of a host plant may represent a true continuum, with microbes able to move between the soil, the rhizosphere, and inside the root (Farrar et al. 2014) (Fig. 7.2). Indeed, several species of microorganisms use the nutrient niche in the rhizosphere and change from a free-living condition to an endophytic state (Rosenblueth and Martínez-Romero 2006). Bacterial endophytes that were injected into stems moved to the roots and the rhizosphere, thereby confirming the existence of a continuous shift in microbial community within the root microbiome (Gaiero et al. 2013). A battery of different mechanisms that involve complex communication between partners and include motility, adhesion, plant-cell wall degradation, and escape from plant defences determines endophytic colonization. The highly competitive process, involve only those bacteria that can occupy spaces or niche near the root and get nutrients may succeed. The most common mode of entry of these bacteria into plant tissues is through cracks in the primary and lateral roots (Agarwal and Shende 1987; Liu et al. 2006; Sørensen and Sessitsch 2006; Sprent and de Faria 1998) (Fig. 7.2). Root cracks allow plant metabolites to exudate, becoming sites that attract these bacteria (Hallmann et al. 1997). Although, endophytic bacteria usually enter the host plant from the roots, shoot, including stomata, particularly young leaves and stems (Roos and Hattingh 1983), lenticels, which are usually present in the stem and root periderm (Scott et al. 1996), flowers and cotyledons (Zinniel et al. 2002). Once inside the plant, endophytic bacteria can systematically infect adjacent plant tissues via xylem or phloem vessels.

162

C. C. V. Velloso et al.

On the other hand, plants can select endophytic bacteria through steps that function as filters primarily in the rhizosphere, then rhizoplane, and endosphere. The rhizosphere is described as the main compartment or “gateway” that deeply influences the plant’s endophytic microbiome. The different physicochemical and biological properties of the carbon-rich molecules and antimicrobial compounds exuded in this region may favor the growth and multiplication of certain groups of microorganisms while inhibit others. Rhizoplane functions as a second selection point for microorganisms, where only those capable of binding to the root surface are allowed to enter the endosphere (Edwards et al. 2015; Reinhold-Hurek et al. 2015). On the other hand, the plant’s immune system actively excludes specific groups of microorganisms (Lundberg et al. 2012). Root colonization often begins with chemotaxis, i.e., bacterial recognition of certain compounds in root exudates. Although there is no direct evidence of the presence of a specific compound, flavonoids are considered as an important player in plant-microorganism communication (Shaw et al. 2006). Once in the rhizosphere, endophytic bacteria must bind to the root surface (rhizoplane) to reach entry sites such as lateral emergence and root tips or regions with cracks caused by pathogens or predators. Bacterial traits such as motility, polysaccharide production, and adhesins are important in the root surface adhesion process (Hori and Matsumoto 2010). As they bind to the root surface, bacteria multiply resulting in the establishment of microcolonies or biofilms thus, become successful in the colonization process. The host penetration process can be passive or active. In passive, the bacterium uses fissures already present in the root and in the active, penetration occurs through the production of lipopolysaccharides, flagella, pili, and quorum sensing (Böhm et al. 2007; SuárezMoreno et al. 2010). In the active process, secretion of cell wall degrading enzymes such as pectinases and cellulases are described as important mechanisms for the penetration and colonization of bacteria within host plants (Compant et al. 2005). As endophytic bacteria enter the plant, they respond to host stimuli to induce the cellular processes necessary for the maintenance of the endophytic stage and distribution to cortical tissue of the root. At this point, they can multiply within the tissues often reaching high populations, depending on the stage of plant development (Hardoim et al. 2008). Migration of root bacteria to shoot tissues requires the production of cell wall degrading enzymes. It can also occur through xylem elements, directed by plant transpiration, which allow the movement of bacteria mainly reaching the leaf tissues. Only few bacteria can migrate and adapt to the shoot, as this colonization requires specific physiological signals to occupy plant niche (Hallmann 2001). In general, endophytic microbial communities are less diverse than the rhizospheric communities, for both bacteria and fungi. This suggests that roots select the endosphere community members that consequently present more defined groups (Bulgarelli et al. 2013). The bacterial endophyte community patterns in leaf, stem, and root of three tropical rainforest plant species show a lower diversity of OTU richness, species richness, and community diversity (inversed Simpson’s index) in comparison to that of rhizospheric soil community (Haruna et al. 2017). This emphasizes that, the bacteria rhizospheric community from these three plant species is relatively

7 Tropical Endophytic Bacillus Species …

163

distinct from the endophytic community. Recent studies from our research group show that maize root-associated microbial communities have lower diversity indices than the rhizospheric communities (Gomes et al. 2018). These results are evidenced and consistent with previous studies showing that maize endophytic microbiota differ from those of the rhizosphere (Edwards et al. 2015; Miliute et al. 2015; Robbins et al. 2018).

7.3 Endophytic Bacillus and Plant Growth Promotion in Tropical Soils Tropics occupy approximately one-third of the Earth’s surface, with different climate, vegetation, geomorphology, lithology, and, consequently, soils in the region which are more diverse than temperate and arctic soils (Kalpage 1974), which contributes to the microorganism diversity. There is a growing interest in understanding the role of endophytic microorganisms in tropical soils. The investigation of bacterial diversity in these soils may help to describe new species and to elucidate traits related to plant growth promotion under adverse tropical conditions. Major factors that constrain tropical soil fertility and sustainable agriculture are low nutrient capital, moisture stress, erosion, high P fixation, and high acidity with aluminum toxicity (Santos et al. 2010; Camenzind et al. 2017; Garland et al. 2018). Phosphate soluble fertilizers applied to soils can be complexed by adsorption to iron and aluminum oxides (mainly in clayey tropical soils) and calcium precipitation (alkaline soils), making it unavailable to plants (Novais and Smyth 1999). Phosphorus can also be complexed in organic form reaching values of up to 80% of total P in no-till soils (Marschner et al. 2006). The fragility of many tropical soils limits food production in annual cropping systems. Since some tropical soils under natural conditions have high biological activity, an increased use of the biological potential of these soils to counter the challenges of food production problems is proposed (Cardoso and Kuyper 2006). Phosphate solubilizing and mineralizing microorganism have a high potential to be used in the management of P deficient soils. The mechanisms of P solubilization by PGPB are associated with the production of organic and inorganic acids, proton excretion, and phosphatase activity. Organic acids decrease the rhizosphere pH favoring the solubility of precipitated P forms. They can compete or even replace phosphate sorbed on the surfaces of soil clays and chelate Al and Fe avoiding thus the precipitation of phosphate (Vega 2007). Among the common members of PGPB community, Bacillus is the most naturally abundant and universally present endophytic genus in tropical plants (Tiwari et al. 2019). Although Bacillus is well known, there is still a range of information on endophytes that needs to be interpreted in tropical soils so that new metabolites and biotechnological characteristics of these bacteria can be used in medicine, industry, and agriculture.

164

C. C. V. Velloso et al.

Bacillus comprises a heterogeneous group of Gram-positive bacteria widely distributed in the environment, consisting of approximately 360 species that have distinct physiological, metabolic, and phenotypic characteristics (www.bacterio.net/ bacillus.html). Numerous Bacillus sp. are known to enhance nutrient solubilization and facilitate nutrient mobilization in the soil. Our research group reported that maize plants inoculated separately with different Bacillus strains capable of producing indole-3-acetic acid (IAA) and solubilizing phosphate enhanced root system, dry matter, and nutrient accumulation in hydroponics. Under field conditions, strains increased maize yield and P grain accumulation by around 36 and 58%, and P grain in 21% in soils with no P added. Even in soils fertilized with triple superphosphate, maize yield increase and P grain accumulation was observed around 20% after inoculation comparing to non-inoculated control (unpublished results). In another study, pearl millet (Pennisetum glaucum) seeds inoculated with endophytic Bacillus strains isolated from maize grown in the Brazilian Cerrado, showed increased shoot and root dry weight, N and P content in the roots and N, P, and K in the shoot, promoting growth and nutrient uptake in greenhouse conditions. Probably the main mechanism involved in these processes are the production of IAA, siderophores, and solubilization of phosphate (Ribeiro et al. 2018). Interestingly, these strains showed high organic acid production, which is one of the mechanisms involved in solubilization of mineral phosphates, due to lowering soil pH (Abreu et al. 2017). Other examples of endophytic Bacillus in tropical soil show that inoculation of strains isolated from medicinal plants, crops and weed enhanced seed germination, and seedlings vigor of pearl millet crop plants. In addition, the vegetative (height of the plant, number of basal tillers, fresh and dry weight) and reproductive growth parameters (early flowering, length and girth of ear heads, 1000-seed weight, plant height, and tillering) were higher than control due to the treatment of maize seeds with the endophytic bacteria (Chandrashekhara et al. 2007). The Bacillus strains were also efficient in reducing the incidence of downy mildew caused by Sclerospora graminicola under greenhouse and field condition, demonstrating their potential as a biocontrol agent (Chandrashekhara et al. 2007). In addition to agricultural crops, various studies have shown evidence of the benefits of Bacillus endophytic in forestry of Eucalyptus, particularly in tropical and subtropical regions, due to its rapid growth, adaptability, and the commercial value of its wood (Brooker 2000). However, the Eucalyptus–endophytic bacteria interaction is poorly described, and the majority of previous studies have focused on rhizosphere microorganisms (Bonito et al. 2014; Silva et al. 2014). One of the first studies describing Bacillus, including B. licheniformis and B. subtilis, as endophytes of eucalyptus exhibited an increase of the root and shoot growth of plantlets after inoculation under greenhouse conditions, during the summer and winter seasons (Paz et al. 2012). Other studies have shown evidence of the benefits of endophytic inoculation in eucalyptus plantlets; for instance, increasing the rooting indexes and vegetative biomass or acting as biocontrol agents in improving plant resistance when challenged with different pathogens (Ferreira et al. 2008; Mafia et al. 2005; Procópio et al. 2009). Related to nutrient efficiency, the potential for biological nitrogen fixation

7 Tropical Endophytic Bacillus Species …

165

(BNF) of endophytic species was assessed in E. urograndis roots using culturedependent and culture-independent techniques. The data suggests that Eucalyptus benefit from BNF, with many abundant genera closely related to nitrogen-fixing bacteria. Under N-depleted media, 25% of the bacterial isolates are able to grow and present the nif H gene. As the most dominant members were related to Bacillus, the conclusion is that the naturally high abundance of these bacteria makes them the most promising bacterial inoculant for plant growth promotion. In addition to high P fixation and aluminum toxicity, tropical agriculture suffers the effect of the continuous attack of plant pathogens as these environments present ideal water, temperature, and nutrient conditions for their proliferation. The identification and development of locally adapted biological control agents are extremely pertinent as native strains have greater adaptability, performance, and suitability than introduced microorganisms. Considering the seriousness of diseases in tropical agriculture, native B. amyloliquefaciens, B. cereus, B. megaterium, and B. pumilus strains from tropical soils of Trinidad were isolated and characterized as antibiotic lipopeptide producers, such as iturin, bacillomycin, bacilysin, fengycin, surfactin, and zwittermycin. Testing of these Bacillus species against pathogens such as Alternaria, Fusarium, Ralstonia, Cercospora, and Colletotrichum revealed greater antagonistic activity of all lipopeptide produced by B. amyloliquefaciens strains as compared with non-producers being promising for the development of bioagents suitable for disease management in tropical conditions (Saravanakumar et al. 2018). Antifungal lipopeptides inhibiting plant pathogens as F. moniliforme as well as inducing the up-regulation of pathogenesis-related (PR) genes of host plants (systemic acquired resistance) were also reported in endophytic Bacillus spp. isolated from maize from Indian popcorn and yellow dent corn. The presence of antifungal iturin A, fengycin, and bacillomycin were also detected using MALDI-TOF mass spectrometry (Gond et al. 2015). In tropical ecosystems, the ability of endophytic microorganisms to colonize the internal tissues of plants suggests an ecological advantage. Mangrove forests, typical tropical ecosystems situated between land and sea, are among the most productive and diverse communities worldwide, particularly in Brazil, Indonesia, and Australia. These ecosystems are important sources of endophytic microorganisms with biotechnological potential, which deserves further studies (Sebastianes et al. 2017). Interesting, Bacillus is the most frequent genus, comprising 42 and 28% of the endophytic isolates from plant species from two mangrove systems in Brazil. In other study, Bacillus spp. isolated from mangrove trees in Malaysia show efficacy in promoting seedling growth in rice. The inoculation of rice seeds with endophytic strains of B. cereus and B. amyloliquefaciens significantly increased the root and shoot length, suggesting that endophytic bacteria from mangrove trees can increase the fitness of rice seedlings under controlled conditions (Deivanai et al. 2014). Other studies evaluated the enzyme production of endophytic Bacillus from mangrove forest in India and Brazil. Enzymes protease and endoglucanase activity are observed in 70% of the isolates and bacteria exhibit the highest activity rates for amylase, esterase, and endoglucanase. In addition, the antimicrobial activity against important pathogens,

166

C. C. V. Velloso et al.

such as Fusarium, Staphylococcus aureus, Vibrio parahaemolyticus, and V. anguillarum, indicating biological control potential have also been observed (Castro et al. 2014).

7.4 Bacillus in Post-Genomic Era The development of bioinformatics tool coupled to constant innovation in sequencing platforms enabled genome sequencing and annotation, metabolic pathway construction, new bioactive molecules as well as their biochemical properties allowing the clarification of new mechanisms related to plant growth-promoting (Blin et al. 2017; Blom et al. 2016; Conesa et al. 2005; Kanehisa et al. 2016; Koskinen et al. 2015; Seemann 2014). In addition, advances in DNA sequencing technologies reduced the sequence cost per base, allowing sequencing complete genomes with an affordable price, allowing a deeper and global knowledge that considers gene and metabolic pathways instead of isolated information. Complete or draft of PGPB genome allows the characterization of gene content, genome structure, PGP mechanisms, and in silico physiological, ecological, and evolution studies (Belbahri et al. 2017; Chaudhry et al. 2017; Ma et al. 2018). The first Gram-positive PGPB to have the fully sequenced genome mapped was B. amyloliquefaciens subsp. plantarum, FZB42T (Chen et al. 2007). Subsequently, several genomes of Bacillus capable of PGP and acting on biocontrol were available (Table 7.1). To date, more than 4,600 genomes of this genus have been sequenced, ranging from approximately 0.56 to 9.84 Mb in different assembly level and are available in the GenBank database (https://www.ncbi.nlm.nih.gov/genome/browse/#!/pro karyotes/bacillus). The genome content of different endophytic Bacillus strains reveals that a significant portion of the genome encodes proteins related to molecules with biotechnological applications. A comparative study of 31 Bacillus genomes showed that plantrelated Bacillus strains contain more genes involved in intermediary metabolism and secondary metabolites production than non-plant associated strains. In addition, plant-related Bacillus strains possess additional genes involved in utilization of plant-derived substrates and synthesis of antibiotics, which have arisen via horizontal gene transfer events during the evolutionary process (Zhang et al. 2016). For example, endophytic B. velezensis CC09 genome, capable of promoting growth and preventing fungal disease in plants, is related to nonribosomal peptide synthetase, polyketide synthetase, as well as genes related to iron acquisition, colonization, and synthesis of volatile organic compounds (Cai et al. 2016). Clusters of genes responsible for antifungal (fengicin, surfactin, bacillisin) and antibacterial metabolites (butyrosine, bacillene, difficidine, macrolactin, surfactin, bacillisin), as well as genes associated with PGP including phosphate solubilization, siderophores production, and pathogen growth inhibition were also found in the genome of the endophytic B. velezensis LDO2 (Chen et al. 2019).

Nonribosomal peptide synthetase for the production of antibiotics such as surfactin, bacillibactin, and bacilysin, indole3-acetaldehyde and 2,3-butanediol, swarming and biofilm formation Sporulation transcription factors related to biofilm formation, Sun et al. (2015) antimicrobial biosynthesis, bacteriocins, siderophore-synthesis, and production of endoglucanases, cellulases, and glucanases Synthesis of polyketide and nonribosomal peptides such as Cai et al. (2016) surfactin, iturin A, fengycin, bacillibacti, genes associated with iron acquisition, colonization, and volatile organic compounds synthesis Phosphate utilization, iron acquisition, biosynthesis of exopolysaccharides and bacteriocin production Nitrogen fixation, siderophore, cobalamin, spermidine, phenazine, and acetoin synthesis

B. pumilus INR7

B. amyloliquefaciens XK-4-1

B. velezensis CC09

B. mycoides M2E15

B. flexus KLBMP 4941

Wang et al. (2017)

Yi et al. (2016)

Jeong et al. (2014)

Gold et al. (2014)

Operons for biosynthesis of antifungal compounds, a bacillibactin-like siderophore, antibiotic bacilysin, and biosynthesis of volatile compounds

B. mojavensis RRC101

Reference

Plant growth promotion genes, operons, and coding DNA sequence (CDS)

Bacillus strain

Table 7.1 Examples of Bacillus strains with complete genome sequence and plant growth promotion properties

(continued)

7 Tropical Endophytic Bacillus Species … 167

Nitrogen metabolism pathway and two main transcriptional factor genes, glnR and tnrA responsible for the regulation of nitrogen fixation Heat shock resistance, hydrocarbon metabolism, heavy metal tolerance, biofilm formation, siderophore, and IAA biosynthesis Indole-3-acetic acid acetyltransferase, indole-3-acetaldehyde dehydrogenase; gene clusters including ribosomally synthesized peptides, nonribosomal peptide synthetases, and polyketide synthases

Proteins involved in the biosynthesis of IAA, synthesis of Pinto et al. (2018) volatile compounds, nitrate reduction pathways, protein nifU, and a cysteine desulfurase nifS, which are involved in the Fe-S cluster assembly and required for the activation of nitrogenase, nitric oxide synthase, phytase, and siderophores synthesis, ABC transporters for iron and iron uptake

B. paralicheniformis KMS 80

B. pumilus SCAL1

B. velezensis PEBA20

B. amyloliquefaciens subsp. plantarum Fito_F321

Kong et al. (2018)

Mukhtar et al. (2018)

Annapurna et al. (2018)

ACC deaminase, several putative siderophore biosynthesis, Yaish (2017) binding, and transport proteins, ampicillin-resistant beta-lactamase proteins, and biosynthesis gene of locillomycin, asukamycin, and iturin antibiotic

B. aryabhattai SQU-R12

Reference

Plant growth promotion genes, operons, and coding DNA sequence (CDS)

Bacillus strain

Table 7.1 (continued)

(continued)

168 C. C. V. Velloso et al.

Secondary metabolite production, including 3 nonribosomal Wemheuer et al. (2018) polyketide synthetase, bacteriocin production, paeninodin, and siderophores biosynthesis Virulence, disease and defense, stress response, iron, phosphorous, and sulphur metabolism Siderophore production, nutrition utilization such as nitrogen, magnesium, phosphate, and potassium, growth-promoting hormones (IAA) and stress response

B. mycoides GM6LP

B. toyonensis COPE52

Bacillus sp. MHSD28

Makuwa and Serepa-Dlamini (2019)

Contreras–Pérez et al. 2019

Potshangbam et al. (2018)

Antioxidant enzymes, such as catalase, peroxidase, and superoxide dismutase, pathways related to phosphorous solubilization, iron uptake, cellulose degradation, chitinolytic activity, glucanase, acetoin dehydrogenase, protease, trehalose metabolism, exopolysaccharides, cytokinin, and tryptophan biosynthesis, as well as nitrogen-fixing proteins

B altitudinis Lc5

Reference

Plant growth promotion genes, operons, and coding DNA sequence (CDS)

Bacillus strain

Table 7.1 (continued)

7 Tropical Endophytic Bacillus Species … 169

170

C. C. V. Velloso et al.

B. paralicheniformis strain KMS 80, isolated from rice root is able to fix nitrogen presenting almost 21 genes involved in nitrogen metabolism pathway such as glnA, glnL, glnR, glnT, tnrA, and nif H gene, etc. (Annapurna et al. 2018). In the genome of Bacillus sp. MHSD28 strain, endophytic bacteria isolated from the medicinal plant Dicoma anomala, several genes associated with PGP have also been identified (Makuwa and Serepa-Dlamini 2019). In addition, due to the growing number of sequenced endophytic Bacillus genomes, the identification of bioactive compounds has been predicted and their production confirmed, revealing that endophytic bacillus species are underexploited sources of new molecules of biotechnological interest (Radhakrishnan et al. 2017; Lopes et al. 2018). For example, genome studies of B. amyloliquefaciens showed an increase of new strain-specific secondary metabolite clusters that play key roles in pathogen suppression and PGP (Belbahri et al. 2017). Recently, our research group sequenced the genome of two PGP strains: B. thuringiensis B116 and B. megaterium B119 isolated from tropical maize capable of increasing yield and phosphorus content in maize grains in field experiments (Vieira Velloso et al. 2020). The draft genome of these two strains shows the genes related to endospore formation, chemotaxis, motility, competition in the rhizosphere, and several mechanisms of PGP. Both Bacillus species are able to produce exopolysaccharides (EPS) and fix nitrogen. However, B. megaterium produces higher amounts of IAA and siderophores, whereas B. thuringiensis is characterized as the best biofilm producer and is capable to solubilize more insoluble phosphate (Vieira Velloso et al. 2020). Overall, new molecular and genomic techniques accelerate the identification of bioactive compounds useful for agricultural and medical applications; reveal mechanism and pathways; and help to optimize in vitro isolation and biochemical characterization. Moreover, these techniques allow rapid identification of microorganisms and enable the characterization of microbiome diversity, since uncultivable microorganisms can also be detected. Thus, understanding the dynamics of the microbial community in different environments increases the discovery of new proteins and metabolites and the comprehension of stress tolerance and biotechnological applications (Hirel and Lea 2018; Imam et al. 2016; Krishnamurthy et al. 2018; Upadhyay et al. 2017).

7.5 Commercialization and Challenge of Bacillus Biotechnological Products Bacillus is one of the main microorganisms involved in the generation of biotechnological products for agriculture, representing the most important group for use in biological control in the form of insecticides, fungicides, bactericides, nematicides, as well as stress tolerance stimulants, and plant growth promoters. Among bacterial biocontrol agents, Bacillus species account for over 50% of marketed products, with B. thuringiensis contributing over 70% of this market (Ongena and Jacques

7 Tropical Endophytic Bacillus Species …

171

2008). This is due to different properties of this group of bacteria, including the ability to form endospores, allowing them to adapt to extreme abiotic conditions such as temperatures, pH, radiation, desiccation, ultraviolet light, or pesticide exposure (Bahadir et al. 2018). In addition, endospores enable greater resistance of stock products by increasing shelf life of Bacillus-based products. The commercial success of a PGPB-based product requires viable and economical market demand, consistent and broad spectrum of action, safety and stability, low cost and availability of adjuvants, marketing of bioinoculant products, and interaction between academia and industry. As part of the future of bioinoculants, research should focus on optimizing growth conditions and increasing the shelf life of PGPBbased, the product should not be toxic to plants and animals must tolerate severe environmental conditions, increase crops production and be cost-effective for farmers use (Mustafa et al. 2019). Most of these conditions are observed in Bacillus-based products, which have great potential to be used in integrated agricultural production systems, which justifies the screening and characterization of new strains. Many products both soild and liquid of PGPB formulated with Bacillus strains are already available in the market in different countries where they are applied as biofertilizers, phytostimulators, rhizoremediators, and bio-pesticides to attain varied benefits for better plant growth (Table 7.2). Recently, the microbiology research group of Embrapa Maize & Sorghum in a partnership with the Bioma Company (bioma.ind.br) registered and started the commercialization of BiomaPhos® , a consortium of two Bacillus strains, B. megaterium (CNPMS B119) and B. subtilis (CNPMS B2084) inoculants for phosphate solubilization. This liquid inoculant, recommended for seed treatment or in sowing furrow spray, associates with the plant since the beginning of root formation. The bacteria present in the product multiply and colonize the plant rhizosphere initiating the production of organic acids that solubilize the phosphorus fixed calcium, aluminum, and iron present in the soil portion in contact with the plant roots (rhizosphere), making it readily available for plant absorption and assimilation. In addition, BiomaPhos® also acts in the mineralization of phosphorus present in soil organic matter (phytate), giving greater contribution to the crop. The Biomaphos® is an interesting example of the different stages between the beginning of the scientific research and the product available to the farmers in tropical conditions. One of the strains, B. megaterium (CNPMS B119) was isolated from rhizosphere of tropical P-efficient maize genotypes and characterized as P solubilizing and mineralizing, presenting high phosphatase activity (Oliveira et al. 2009). The other strain, B. subtilis (CNPMS B2084), is an endophytic strain isolated from maize roots, characterized as high organic acids producer and P solubilizer (Abreu et al. 2017). Both strains separately can increase biomass, shoot nutrient content, and root surface area in controlled and field condition. When maize was inoculated with strain B2084, there was 12% increase in yield and the inoculation with B119 improved grain P accumulation by 21% comparing with the non-inoculated control. Under TSP fertilization, there was a significant increment on yield of approximately 26% of maize plants inoculated with B119. Moreover, plants inoculated with B119 strain showed 24% increase in P grain content comparing with the non-inoculated

Company

Total Biotecnologia/Biotrop

Bioma/Simbiose

Special Biochem (P) Ltd

Total Biotecnologia/Biotrop

FMC Corporation

Varsha Bioscience And Technology India Private Ltd

Biosoja

Total Biotecnologia/Biotrop

Bayer

Total Biotecnologia/Biotrop

Product name

Accelerate max

BiomaPhos

Bio-Phospho

Enduro

Nemix C

Phosphomax

Rizolyptus

Rudder

Serenade Prime

Vult

Brazil

Australia

Brazil

Brazil

India

Brazil

Brazil

India

Brazil

Brazil

Country

Phytohormones, antibiotics, hydrolytic enzymes, elicitation of plant defense

Higher yields, better crop uniformity, improved harvest crop quality, improved shelf life

Production of exopolysaccharides, biofilm

Phytohormones, nitrogen fixation

Phosphate solubilization

Phytohormones, nutrients uptake, biofilm

Nutrients uptake, nitrogen fixation, biological control

Phosphate solubilization

Phosphate solubilization/mineralization

Nutrient solubilization, mineralization of organic compounds, acid organic production

Benefit/mechanism

B. subtilis

B. amyloliquefaciens

B. amyloliquefaciens

B. subtilis

B. megaterium

B. subtilis B. licheniformis

B. pumilus

B. subtilis

B. megaterium, B. subtilis

B. subtilis, B. amyloliquefaciens, B. pumilus

Composition

Crops

Vegetable crops, berries, tree crops

Crops

Eucalyptus

Crops

Sugarcane

Crops

Crops

Crops

Crops

Suitable for

Table 7.2 Outline of selected PGPB-based Bacillus formulation available commercially in the market of tropical countries

http://biotrop.com.br/

https://www.crop.bayer.com.au/findcrop-solutions/by-product/bayer-biolog ics/serenade-prime#tab-2

http://biotrop.com.br/

http://biosoja.com.br/media/89_RIZ OLYPTUS.pdf

https://www.indiamart.com/proddetail/ phosphobacteria-bio-fertilizer-115502 43355.html

https://www.fmcagricola.com.br/con teudo/produtos/boletim_tecnico_nemix_ a4.pdf

http://biotrop.com.br/

https://www.indiamart.com/proddetail/ bio-phospho-bio-fertilizer-7618252062. html

https://www.bioma.ind.br/product/ bioma-phos

http://biotrop.com.br/

Site

172 C. C. V. Velloso et al.

7 Tropical Endophytic Bacillus Species …

173

control (de Sousa et al. 2020). After testing for different mechanisms of PGP in vitro, the strains were co-inoculated in maize seeds, tested in controlled conditions and in the field. The selection of the adjuvant and method required for inoculation is based on the microorganism’s viability, crops, and application method. Positive results in the field attract the attention of inoculant-producing industries, an important step for the formulation, large-scale production, product marketing, and training to farmers.

7.6 Conclusion and Future Prospects Tropical endophyte Bacillus is well known for their capacity to confer plant growth promotion and to increase resistance toward various diseases as well as abiotic stresses. However, some strains fail to confer these beneficial effects when applied in the field. The lack of various characteristics, which are important for efficient colonization of the plant environment and the limited supply of the appropriate formulation, could explain poor plant host colonization. Further analysis of sequenced genomes, the characterization of unknown genes and the identification of genes expressed during colonization may lead to a better understanding on how beneficial bacteria colonize different plant niches, thus result not only in scientific knowledge on plant microbe interactions, but also in a more successful and reliable use of bacterial inoculants. The use of PGPB for mineral solubilization and N fixation has progressed well, but yet to be done more for zinc and potassium solubilization and sulphur oxidation. The exploration of the more efficient use of these nutrients has the potential to increase the field of the inoculants and create confidence among the farmers for their use. In order to accomplish this, there is a need to invest more in research regarding plant–microorganism–soil interaction, growth condition optimization, tolerance to adverse environmental condition, and provide higher yield and longer shelf life with cost-effective for farmers for long-term applications.

References de Abreu CS, Figueiredo JEF, Oliveira CA et al (2017) Maize endophytic bacteria as mineral phosphate solubilizers. Genet Mol Res 16:1–13. https://doi.org/10.4238/gmr16019294 Agarwhal S, Shende ST (1987) Tetrazolium reducing microorganisms inside the root of Brassica species. Curr Sci 56:187–188 Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181. https://doi.org/10.1016/j.micres. 2006.04.001 Alori ET, Babalola OO (2018) Microbial inoculants for improve crop quality and human health. Front Microbiol 9:2213. https://doi.org/10.3389/fmicb.2018.02213 Alori ET, Dare MO, Babalola OO (2017) Microbial inoculants for soil quality and plant health. In: Lichtfouse E (eds) Sustainable agriculture reviews, vol 22, Springer, Cham, pp 281–307. https:// doi.org/10.1007/978-3-319-48006-0_9

174

C. C. V. Velloso et al.

Annapurna K, Govindasamy V, Sharma M, Ghosh A, Chikara SK (2018) Whole genome shotgun sequence of Bacillus paralicheniformis strain KMS 80, a rhizobacterial endophyte isolated from rice (Oryza sativa L.). 3 Biotech 8:223. https://doi.org/10.1007/s13205-018-1242-y Assumpção LC, Lacava P, Dias ACF, Azevedo JL, Menten JOM (2009) Diversidade e potencial biotecnológico da comunidade bacteriana endofítica de sementes de soja. Pesq Agropec Bras 44:503–510. https://doi.org/10.1590/S0100-204X2009000500010 Bahadir PS, Liaqat F, Eltem R (2018) Plant growth promoting properties of phosphate solubilizing Bacillus species isolated from the Aegean Region of Turkey. Turk J Bot 42:183–196. https://doi. org/10.3906/bot-1706-51 Barriuso E, Benoit P, Dubus IG (2008) Formation of pesticide nonextractable (bound) residues in soils: magnitude, controlling factors and reversibility. Environ Sci Technol 42:1845–1854. https:// doi.org/10.1021/es7021736 Bashan Y, De-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33. https://doi.org/10.1007/s11104-013-1956-x Belbahri L, Chenari Bouket A, Rekik I et al (2017) Comparative genomics of Bacillus amyloliquefaciens strains reveals a core genome with traits for habitat adaptation and a secondary metabolites rich accessory genome. Front Microbiol 8:1438. https://doi.org/10.3389/fmicb.2017.01438 Bhattacharyya D, Garladinne M, Lee YH (2015) Volatile indole produced by rhizobacterium Proteus vulgaris JBLS202 stimulates growth of Arabidopsis thaliana through auxin, cytokinin, and brassinosteroid pathways. J Plant Growth Regul 34:158–168. https://doi.org/10.1007/s00344014-9453-x Blin K, Wolf T, Chevrette MG et al (2017) antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 45:W36–W41. https://doi.org/10. 1093/nar/gkx319 Blom J, Kreis J, Spänig S, Juhre T, Bertelli C, Ernst C, Goesmann A (2016) EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 44:W22–W28. https://doi.org/10.1093/nar/gkw255 Boddey RM, Urquiaga S, Alves BJ, Reis V (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252:139–149. https://doi.org/10.1023/A: 1024152126541 Böhm M, Hurek T, Reinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2 -fixing endophyte Azoarcus sp. strain BH72. Mol Plant Microbe In 20:526– 533. https://doi.org/10.1094/MPMI-20-5-0526 Bonito G, Reynolds H, Robeson MS et al (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol Ecol 23:3356–3370. https://doi.org/10. 1111/mec.12821 Brooker MIH (2000) A new classification of the genus Eucalyptus L’Hér. (Myrtaceae). Aust Syst Bot 13:79–148. https://doi.org/10.1071/SB98008 Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. https://doi.org/ 10.1146/annurev-arplant-050312-120106 Cai X, Kang X, Xi H, Liu C, Xue Y (2016) Complete genome sequence of the endophytic biocontrol strain Bacillus velezensis CC09. Genome Announc 4:e01048–16. https://doi.org/10.1128/gen omeA.01048-16 Calvo P, Ormeño-Orrillo E, Martínez-Romero E, Zúñiga D (2010) Characterization of Bacillus isolates of potato rhizosphere from andean soils of Peru and their potential PGPR characteristics. Braz J Microbiol 41:899–906. https://doi.org/10.1590/S1517-83822010000400008 Camenzind T, Hättenschwiler S, Treseder KK, Lehmann A, Rillig MC (2017) Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr 88(1):4–21. https://doi.org/10.1002/ ecm.1279 Cardoso I, Kuyper T (2006) Mycorrhizas and tropical soil fertility. Agr Ecosyst Environ 116:72–84. https://doi.org/10.1016/j.agee.2006.03.011

7 Tropical Endophytic Bacillus Species …

175

Castro RA, Quecine MC, Lacava PT et al (2014) Isolation and enzyme bioprospection of endophytic bacteria associated with plants of Brazilian mangrove ecosystem. Springerplus 3:382. https://doi. org/10.1186/2193-1801-3-382 Chandrashekhara SN, Deepak SA, Amruthesh KN, Shetty NP, Shetty HS (2007) Endophytic bacteria from different plant origin enhance growth and induce downy mildew resistance in pearl millet. Asian J Plant Pathol 1:1–11 Chaudhry V, Sharma S, Bansal K, Patil PB (2017) Glimpse into the genomes of rice endophytic bacteria: diversity and distribution of firmicutes. Front Microbiol 7:2115. https://doi.org/10.3389/ fmicb.2016.02115 Chen L, Shi H, Heng J, Wang D, Bian K (2019) Antimicrobial, plant growth-promoting and genomic properties of the peanut endophyte Bacillus velezensis LDO2. Microbiol Res 218:41–48. https:// doi.org/10.1016/j.micres.2018.10.002 Chen XH, Koumoutsi A, Scholz R et al (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–10014. https://doi.org/10.1038/nbt1325 Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. https://doi.org/10.1016/j.soilbio.2009.11.024 Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693. https://doi.org/10.1128/AEM.71.4.1685-1693.2005 Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610 Contreras-Pérez M, Hernández-Salmerón J, Rojas-Solís D et al (2019) Draft genome analysis of the endophyte, Bacillus toyonensis COPE52, a blueberry (Vaccinium spp. var. Biloxi) growthpromoting bacterium. 3 Biotech 9:370. https://doi.org/10.1007/s13205-019-1911-5 de Sousa SM, de Oliveira CA, Andrade DL et al (2020) Tropical bacillus strains inoculation enhances maize root surface area, dry weight, nutrient uptake and grain yield. J Plant Growth Regul. https:// doi.org/10.1007/s00344-020-10146-9 Deivanai S, Bindusara AS, Prabhakaran G, Bhore SJ (2014) Culturable bacterial endophytes isolated from Mangrove tree (Rhizophora apiculata Blume) enhance seedling growth in rice. J Nat Sc Biol Med 5:437. https://doi.org/10.4103/0976-9668.136233 Doty SL, Sher AW, Fleck ND et al (2016) Variable nitrogen fixation in wild Populus. PLoS ONE 11:e0155979. https://doi.org/10.1371/journal.pone.0155979 Edwards J, Johnson C, Santos-Medellín C et al (2015) Structure, variation, and assembly of the root associated microbiome of rice. Proc Natl Acad Sci USA 112:E911–E920. https://doi.org/10. 1073/pnas.1414592112 FAO (2019) FAOSTAT statistical database. Food and Agriculture Organization of the United Nations, Rome, Italy. Available in http://www.fao.org/faostat/home. Accessed 20 Jul 2019 Farrar K, Bryant D, Cope-Selby N (2014) Understanding and engineering beneficial plant-microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12:1193–1206. https:// doi.org/10.1111/pbi.12279 Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14. https://doi.org/10.1111/j.1574-6968.2008.01258.x Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. https://doi.org/10.1007/s11104-008-9833-8 Gaiero JR, Mc Call CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. https://doi.org/10.3732/ajb.1200572

176

C. C. V. Velloso et al.

Garland G, Bünemann EK, Oberson A, Frossard E, Snapp S, Chikowo R, Six J (2018) Phosphorus cycling within soil aggregate fractions of a highly weathered tropical soil: a conceptual model. Soil Biol Biochem 116:91–98. https://doi.org/10.1016/j.soilbio.2017.10.007 Ghyselinck J, Velivelli SLS, Heylen K et al (2013) Bioprospecting in potato fields in the Central Andean Highlands: screening of rhizobacteria for plant growth-promoting properties. Syst Appl Microbiol 36:116–127. https://doi.org/10.1016/j.syapm.2012.11.007 Gold SE, Blacutt AA, Meinersmann RJ, Bacon CW (2014) Whole-genome shotgun sequence of Bacillus mojavensis strain RRC101, an endophytic bacterium antagonistic to the mycotoxigenic endophytic fungus Fusarium verticillioides. Genome Announc 2:e01090–14. https://doi.org/10. 1128/genomeA.01090-14 Gomes EA, Lana UGP, Quensen JF et al (2018) Root-associated microbiome of maize genotypes with contrasting phosphorus use efficiency. Phytobiomes J 2:129–137. https://doi.org/10.1094/ PBIOMES-03-18-0012-R Gond SK, Bergena MS, Torres MS, White JF Jr (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and inducehost defence gene expression in maize. Microbiol Res 172:79–87. https:// doi.org/10.1016/j.micres.2014.11.004 Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914. https://doi.org/10.1139/m97-131 Hallmann J (2001) Plant Interactions with Endophytic Bacteria (ed) CABI Publishing, New York, pp 87–119 Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. https://doi.org/10.1016/j.tim.2008. 07.008 Haruna E, Zin NM, Kerfahi D, Adams JM (2017) Extensive overlap of tropical rainforest bacterial endophytes between soil, plant parts, and plant species. Microb Ecol 75:88–103. https://doi.org/ 10.1007/s00248-017-1002-2 Haygarth PM, Jarvie HP, Powers SM et al (2014) Sustainable phosphorus management and the need for a long-term perspective: the legacy hypothesis. Environ Sci Technol 48:8417–8419. https:// doi.org/10.1021/es502852s Hirel B, Lea PJ (2018) Genomics of nitrogen use efficiency in maize: From basic approaches to agronomic applications. In: Bennetzen J, Flint-Garcia S, Hirsch C, Tuberosa R (eds) The Maize Genome, Springer, Cham, pp 259–286. https://doi.org/10.1007/978-3-319-97427-9_16 Hori K, Matsumoto S (2010) Bacterial adhesion: from mechanism to control. Biochem Eng J 48:424–434. https://doi.org/10.1016/j.bej.2009.11.014 Imam J, Singh PK, Shukla P (2016) Plant microbe interactions in post genomic era: perspectives and applications. Front Microbiol 7:1488. https://doi.org/10.3389/fmicb.2016.01488 Jeong H, Choi SK, Kloepper JW, Ryu CM (2014) Genome sequence of the plant endophyte Bacillus pumilus INR7, triggering induced systemic resistance in field crops. Genome Announc 2:e01093– 14. https://doi.org/10.1128/genomeA.01093-14 Kalpage FSCP (1974) Tropical soils: classification, fertility and management. The Macmillan Company of India Limited, pp 306 Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2016) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361. https://doi.org/10. 1093/nar/gkw1092 Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. Marcel Dekker, New York, pp 199–236 Kong WJ, Yan YC, Li XY, Liu ZY (2018) Draft Genome Sequence of Bacillus velezensis PEBA20, a strain with a plant growth-promoting effect and biocontrol potential. Genome Announc 6:e00286– 18. https://doi.org/10.1128/genomeA.00286-18 Koskinen P, Törönen P, Nokso-Koivisto J, Holm L (2015) PANNZER: high-throughput functional annotation of uncharacterized proteins in an error-prone environment. Bioinformatics 31:1544– 1552. https://doi.org/10.1093/bioinformatics/btu851

7 Tropical Endophytic Bacillus Species …

177

Krishnamurthy P, Qingsong L, Kumar PP (2018) Proteomics perspectives in post-genomic era for producing salinity stress-tolerant crops. In: Kumar V, Wani S, Suprasanna P, Tran LS (eds) Salinity Responses and Tolerance in Plants, vol 2. Springer, Cham, pp 239–266. https://doi.org/10.1007/ 978-3-319-90318-7_10 Kvaki´c M, Pellerin S, Ciais P et al (2018) Quantifying the limitation to world cereal production due to soil phosphorus status. Global Biogeochem Cy 32:143–157. https://doi.org/10.1002/2017GB 005754 Ladha JK, Tirol-Padre A, Reddy CK et al (2016) Global nitrogen budgets in cereals: a 50-year assessment for maize, rice, and wheat production systems. Sci Rep 6:19355. https://doi.org/10. 1038/srep19355 Liu X, Zhao H, Chen S (2006) Colonization of maize and rice plants by strain Bacillus megaterium C4. Curr Microbiol 52:186–190. https://doi.org/10.1007/s00284-005-0162-3 Lopes R, Tsui S, Gonçalves PJ, de Queiroz MV (2018) A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World J Microbiol Biotechnol 34:94. https://doi.org/10.1007/s11274-018-2479-7 Lundberg DS, Lebeis SL, Paredes SH et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237 Ma J, Wang C, Wang H et al (2018) Analysis of the complete genome sequence of Bacillus atrophaeus GQJK17 reveals its biocontrol characteristics as a plant growth-promoting rhizobacterium. Biomed Res Int 947:3542. https://doi.org/10.1155/2018/9473542 Mafia RG, Alfenas AC, Ferreira EM, Zarpelon TG, de Siqueira L (2005) Crescimento de mudas e produtividade de minijardins clonais de eucalipto tratados com rizobactérias selecionadas. Rev Árvore 29:843–851 Maheshwari DK (ed) (2010) Plant growth and health promoting bacteria, vol 18. Microbiology monographs. Springer, Munster Makuwa SC, Serepa-Dlamini MH (2019) Data on draft genome sequence of Bacillus sp. strain MHSD28, a bacterial endophyte isolated from Dicoma anomala. Data Brief 36:104524. https:// doi.org/10.1016/j.dib.2019.104524 Marquez-Santacruz H, Hernandez-Leon R, Orozco-Mosqueda M, Velazquez-Sepulveda I, Santoyo G (2010) Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Genet Mol Res 9:2372–2380. https://doi.org/10. 4238/vol9-4gmr921 Marschner P, Solaiman Z, Rengel Z (2006) Rhizosphere properties of Poaceae genotypes under P-limiting conditions. Plant Soil 283:11–24. https://doi.org/10.1007/s11104-005-8295-5 Maheshwari DK, Annapurna K (2017) Endophytes: crop productivity and protection. Springer International Publishing, Switzerland Melnick RL, Zidack NK, Bailey BA, Maximova SN, Guiltinan M, Backman PA (2008) Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Bio Control 46:46–56. https://doi.org/10.1016/j.biocontrol.2008.01.022 Miliute I, Buzaite O, Baniulis D, Stanys V (2015) Bacterial endophytes in agricultural crops and their role in stress tolerance. Zemdirbyste 102:465–478. https://doi.org/10.13080/z-a.2015.102.060 Misko AL, Germida JJ (2002) Taxonomic and functional diversity of pseudomonads isolated from the roots of field-grown canola. FEMS Microbiol Ecol 42:399–407. https://doi.org/10.1111/j. 1574-6941.2002.tb01029.x Mukhtar T, Afridi MS, McArthur R et al (2018) Draft genome sequence of Bacillus pumilus scal1, an endophytic heat-tolerant plant growth-promoting bacterium. Genome Announc 6:e00306–18. https://doi.org/10.1128/genomeA.00306-18 Mustafa A, Naveed M, Saeed Q et al (2019) Application potentials of plant growth promoting rhizobacteria and fungi as an alternative to conventional weed control methods. In: Hasanuzzaman M, Fujita M (eds) Crop production, 1st edn. IntechOpen, China, pp 1–23 Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:250693. https://doi.org/10.1155/2014/250693

178

C. C. V. Velloso et al.

Naumann G, Alfieri L, Wyser K et al (2018) Global changes in drought conditions under different levels of warming. Geophys Res Lett 45:3285–3296. https://doi.org/10.1002/2017GL076521 Nazir N, Kamili AN, Shah D (2018) Mechanism of plant growth promoting rhizobacteria (PGPR) in enhancing plant growth-a Review. Int J Eng Res Manag Technol 8:709–721 Ngumbi E, Kloepper J (2016) Bacterial-mediated drought tolerance: current and future prospects. Appl Soil Ecol 105:109–125. https://doi.org/10.1016/j.apsoil.2016.04.009 Novais RF, Smyth TJ (1999) Fósforo em solo e planta em condições tropicais. Universidade Federal de Viçosa, Viçosa, p 399 Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP, Sa NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787. https://doi.org/10.1016/j.soi lbio.2008.01.012 Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009 Paz ICP, Santin RCM, Guimarães AM et al (2012) Eucalyptus growth promotion by endophytic Bacillus spp. Genet Mol Res 11:3711–3720. https://doi.org/10.4238/2012.August.17.9 Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254:2201–2213. https://doi.org/10.1007/s00709-017-1109-9 Piccolo SL, Ferraro V, Alfonzo A, Settanni L, Ercolini D, Burruano S, Moschetti G (2010) Presence of endophytic bacteria in Vitis vinifera leaves as detected by fluorescence in situ hybridization. Ann Microbiol 60:161–167. https://doi.org/10.1007/s13213-010-0023-6 Pinter IF, Salomon MV, Berli F, Bottini R, Piccoli P (2017) Characterization of the As (III) tolerance conferred by plant growth promoting rhizobacteria to in vitro-grown grapevine. Appl Soil Ecol 109:60–68. https://doi.org/10.1016/j.apsoil.2016.10.003 Pinto C, Sousa S, Froufe H, Egas C, Clément C, Fontaine F, Gomes AC (2018) Draft genome sequence of Bacillus amyloliquefaciens subsp. plantarum strain Fito_F321, an endophyte microorganism from Vitis vinifera with biocontrol potential. Stand Genomic Sci 1:30. https:// doi.org/10.1186/s40793-018-0327-x Potshangbam M, Sahoo D, Verma P, Verma S, Kalita MC, Devi SI (2018) Draft Genome Sequence of Bacillus altitudinis Lc5, a biocontrol and plant growth-promoting endophyte strain isolated from indigenous black rice of Manipur. Genome Announc 6:e00601–18. https://doi.org/10.1128/ genomeA.00601-18 Procópio RE, Araujo WL, Maccheroni W Jr, Azevedo JL (2009) Characterization of an endophytic bacterial community associated with Eucalyptus spp. Genet Mol Res 8:1408–1422. https://doi. org/10.4238/vol8-4gmr691 Radhakrishnan R, Hashem A, Abd_Allah EF (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667. https://doi.org/10. 3389/fphys.2017.00667 Reinhold-Hurek Bünger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403–424. https://doi.org/ 10.1146/annurev-phyto-082712-102342 Ribeiro VP, Marriel IE, Sousa SM, Lana UGP, Matos BB, Oliveira CA, Gomes EA (2018) Endophytic Bacillus strains enhance pearl millet growth and nutrient uptake under low-P. Braz J Microbiol Suppl 1:40–46. https://doi.org/10.1016/j.bjm.2018.06.005 Robbins C, Thiergart T, Hacquard S et al (2018) Root-associated bacterial and fungal community profiles of Arabidopsis thaliana are robust across contrasting soil P levels. Phytobiomes 2:24–34. https://doi.org/10.1094/PBIOMES-09-17-0042-R Rodriguez PA, Rothballer M, Chowdhury SP, Nussbaumer T, Gutjahr C, Falter-Braun P (2019) Systems biology of plant-microbiome interactions. Mol Plant 12(6):804–821

7 Tropical Endophytic Bacillus Species …

179

Roos IMM, Hattingh MJ (1983) Scanning electron microscopy of Pseudomonas syringae pv: morspmnorum on sweet cherry leaves. J Phytopathol 108:18–25. https://doi.org/10.1111/j.1439-0434. 1983.tb00559.x Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe In 19:827–837. https://doi.org/10.1094/MPMI-19-0827 Saini R, Kumar V, Dudeja SS, Pathak DV (2015) Beneficial effects of inoculation of endophytic bacterial isolates from roots and nodules in chickpea. Int J Curr Microbiol Appl Sci 4:207–221 Santos SN, Kavamura VN, da Silva JL, de Melo IS, Andreote FD (2010) Plant growth promoter rhizobacteria in plants inhabiting harsh tropical environments and its role in agricultural improvements. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Microbiol Monographs, Springer-Verlag, Berlin, Heidelbergp, Piracicaba, pp 251–272 Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.mic res.2015.11.008 Saravanakumar D, Thomas A, Banwarie N (2018) Antagonistic potential of lipopeptide producing Bacillus amyloliquefaciens against major vegetable pathogens. Eur J Plant Pathol 154:319–335. https://doi.org/10.1007/s10658-018-01658-y Scott RI, Chard JM, Hocart MJ, Lennard JH, Graham DC (1996) Penetration of potato tuber lenticels by bacteria in relation to biological control of blackleg disease. Potato Res 39:333–344. https:// doi.org/10.1007/BF02357937 Sebastianes FLS, Azevedo JL, Lacava PT (2017) Diversity and biotechnological potential of endophytic microorganisms associated with tropical mangrove forests. In: De Azevedo JL, Quecine MC (eds) Diversity and benefits of microorganisms from the tropics. Springer International Publishing, Cham, pp 37–56 Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153 Sharma N, Singhvi R (2017) Effects of chemical fertilizers and pesticides on human health and environment: a review. IJAEB 10:675–679. https://doi.org/10.5958/2230-732X.2017.00083.3 Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880. https://doi.org/10.1111/j.14622920.2006.01141.x Silva LR, Azevedo J, Pereira MJ et al (2014) Inoculation of the nonlegume Capsicum annum (L.) with Rhizobium strains. 1. Effect on bioactive compounds, antioxidant activity, and fruit ripeness. J Agric Food Chem 62:557–564. https://doi.org/10.1021/jf4046649 Singh JS, Koushal S, Kumar A, Vimal SR, Gupta VK (2016) Book review: microbial inoculants in sustainable agricultural productivity-Vol. II:functional application. Front Microbiol 7:2105. https://doi.org/10.3389/fmicb.2016.02105 Sørensen J, Sessitsch A (2006) Plant-associated bacteria lifestyle and molecular interactions. In: Elsas JDV, Jansson JK, Trevors, JT (eds) Modern soil microbiology, CRC Press, Boca Raton, USA, pp 211–236 Sprent JI, De Faria SM (1998) Mechanisms of infection of plants by nitrogen fixing organisms. In: Skinner FA, Boddey RM, Fendrik I (eds) Nitrogen fixation with non-legumes. Developments in plant and soil sciences, vol 35. Springer, Dordrecht, pp 3–11. https://doi.org/10.1007/978-94009-0889-5_1 Suárez-Moreno ZR, Devescovi G, Myers M, Hallack L, Mendonça-Previato L, Caballero-Mellado J, Venturi V (2010) Commonalities and differences in regulation of N-Acyl Homoserine lactone quorum sensing in the beneficial plant-associated Burkholderia species cluster. Appl Environ Microbiol 76:4302–4317. https://doi.org/10.1128/AEM.03086-09 Sun Z, Hsiang T, Zhou Y, Zhou J (2015) Draft genome sequence of Bacillus amyloliquefaciens XK4-1, a plant growth-promoting endophyte with antifungal activity. Genome Announc 3:e01306– 15. https://doi.org/10.1128/genomeA.01306-15

180

C. C. V. Velloso et al.

Thomas P, Kumari S, Swarna GK, Prakash DP, Dinesh MR (2007) Ubiquitous presence of fastidious endophytic bacteria in field shoots and index-negative apparently clean shoot-tip cultures of papaya. Plant Cell Rep 26:1491–1499. https://doi.org/10.1007/s00299-007-0363-2 Tiwari S, Prasad V, Lata C (2019) Bacillus: Plant growth promoting bacteria for sustainable agriculture and environment. In: New and future developments in microbial biotechnology and bioengineering, Elsevier, pp 43–55. https://doi.org/10.1016/b978-0-444-64191-5.00003-1 Upadhyay J, Joshi R, Singh B et al (2017) Application of bioinformatics in understanding of plant stress tolerance. In: Hakeem K, Malik A, Vardar-Sukan F, Ozturk M (eds) Plant Bioinformatics, Springer, Cham, pp 347–374. https://doi.org/10.1007/978-3-319-67156-7_14 Varma PK, Uppala S, Pavuluri K, Chandra KJ, Chapala MM, Kumar KVK (2017) Endophytes: role and functions in crop health. In: Singh D, Singh H, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 291–310. https://doi.org/10.1007/978981-10-6593-4 Vega NOW (2007) A review on beneficial effects of rhizosphere bacteria on soil nutrient availability and plant nutrient uptake. Rev Fac Nac Agron Medellin 60:3621–3643. https://doi.org/10.1007/ s40011-013-0297-0 Vieira Velloso CC, de Oliveira CA, Gomes EA, Lana UGP, de Carvalho CG, Guimarães LJM, Pastina MM, de Sousa SM, (2020) Genome-guided insights of tropical Bacillus strains efficient in maize growth promotion. FEMS Microbiology Ecology 96(9) Walker V, Bertrand C, Bellvert F, Moënne-Loccoz Y, René B, Comte G (2011) Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growthpromoting rhizobacteria of the genus Azospirillum. New Phytol 189:494–506. https://doi.org/ 10.1111/j.1469-8137.2010.03484.x Wallace JG, May G (2018) Endophytes: the other Maize Genome. In: Bennetzen J, Flint-Garcia S, Hirsch C, Tuberosa R (eds) The Maize genome. compendium of plant genomes. Springer, Cham, pp 213–246. https://doi.org/10.1007/978-3-319-97427-9_14 Wang TT, Ding P, Chen P et al (2017) Complete genome sequence of endophyte Bacillus flexus KLBMP 4941 reveals its plant growth promotion mechanism and genetic basis for salt tolerance. J Biotechnol 260:38–41. https://doi.org/10.1016/j.jbiotec.2017.09.001 Wemheuer F, Hollensteiner J, Poehlein A, Liesegang H, Daniel R, Wemheuer B (2018) Draft genome sequence of the endophyte Bacillus mycoides strain GM6LP isolated from Lolium perenne. Genome Announc 6:e00011–18. https://doi.org/10.1128/genomeA.00011-18 Xia Y, DeBolt S, Dreyer J, Scott D, Williams MA (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Front Plant Sci 6:490. https://doi.org/10.3389/fpls.2015.00490 Yaish MW (2017) Draft genome sequence of the endophytic Bacillus aryabhattai strain SQU-R12, identified from Phoenix dactylifera L. roots. Genome Announc 5:e00718–17. https://doi.org/10. 1128/genomeA.00718-17 Yi Y, de Jong A, Spoelder J, Elzenga JTM, van Elsas JD, Kuipers OP (2016) Draft genome sequence of Bacillus mycoides M2E15, a strain isolated from the endosphere of potato. Genome Announc 4:e00031–16. https://doi.org/10.1128/genomeA.00031-16 Yuan M, He H, Xiao L, Zhong T, Liu H, Li S, Deng P, Ye Z, Jing Y (2014) Enhancement of Cd phytoextraction by two Amaranthus species with endophytic Rahnella sp. JN27. Chemosphere 103:99–104. https://doi.org/10.1016/j.chemosphere.2013.11.040 Zhang N, Yang D, Kendall JR et al (2016) Comparative genomic analysis of Bacillus amyloliquefaciens and Bacillus subtilis reveals evolutional traits for adaptation to plant-associated habitats. Front Microbiol 7:2039. https://doi.org/10.3389/fmicb.2016.02039 Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P (2002) Ishimaru CA (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68:2198–2208. https://doi.org/10.1128/AEM.68.5.2198-2208

Chapter 8

Biotechnology and Bioinformatics of Endophytes in Biocontrol, Bioremediation, and Plant Growth Promotion Houda Ben Slama, Hafsa Cherif-Silini, Ali Chenari Bouket, Allaoua Silini, Faizah N. Alenezi, Lenka Luptakova, Armelle Vallat, and Lassaad Belbahri Abstract Endophytes have been known for more than a century and recent studies highlighted their endless potentialities in plant growth promotion through several direct and indirect mechanisms. Competent microbial endophytes have been acknowledged in several fields including medicine, industry, pharmacology, bioremediation, and phytoremediation of pollutants due to their safe handling and environment-friendly effects. Modern genomic approaches are considered an effective tool to get a better knowledge of the microbial modes of action. This chapter focuses on endophytes taxonomic affinities and lifestyle, their plant growthpromoting mechanisms, their applications as well as the potential of emerging “omic” tools including genomic, transcriptomic, metabolomics, and proteomics to shed the light on the wealth of their genomic and metabolic potentialities. H. B. Slama · L. Belbahri (B) NextBiotech, 98 Rue Ali Belhouane, 3030, Agareb, Tunisia e-mail: [email protected] H. Cherif-Silini · A. Silini Laboratory of Applied Microbiology, Department of Microbiology, Faculty of Natural and Life Sciences, University Ferhat Abbas Setif-1, Setif, Algeria A. C. Bouket Plant Protection Research Department, East Azarbaijan Agricultural and Natural Resources Research and Education Center, AREEO, Tabriz, Iran F. N. Alenezi Environmental Technology and Management Department, College of Life Sciences, Kuwait University, Kuwait City, Kuwait L. Luptakova Department of Biology and Genetics, Institute of Biology, Zoology and Radiobiology, University of Veterinary Medicine and Pharmacy, Kosice, Slovakia A. Vallat Neuchatel Platform of Analytical Chemistry, Institute of Chemistry, University of Neuchatel, Neuchatel, Switzerland L. Belbahri Laboratory of Soil Biology, University of Neuchatel, Neuchatel, Switzerland © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_8

181

182

H. B. Slama et al.

Keywords Rhizosphere · Genomics · Omics · Endophytes · Bioremediation

8.1 Introduction Since last decade, microbial endophytes have attracted attention. They are occupying a considerable position due to their ubiquitous association with almost all plants (Nair and Padmavathy 2014; Hardoim et al. 2015; Selim et al. 2017; Sharma et al. 2018; Goulart et al. 2019). Therefore, extensive studies have provided information about their endless potentialities in promotion of plant growth (Jasim et al. 2014; Cheffi et al. 2019; Slama et al. 2019) and inhibition of phytopathogens (Mefteh et al. 2017; Slama et al. 2018; Cherif-Silini et al. 2019). In addition to that, endophytes have been exploited in several other fields such as medicine, industry, pharmacology, bioremediation, and phytoremediation of pollutants (Eevers et al. 2015; Wani et al. 2015; Ma et al. 2016; Kumar and Verma 2018; Paramanantham et al. 2019). Modern next-generation sequencing involving genomic, proteomic, metabolomics, and metatranscriptomic technologies, have given deep learning of endophytic potentialities as well as mechanisms and metabolic pathways of secondary metabolites (Fakruddin and Mannan 2013; Finkel et al. 2019; Hong et al. 2019; Srivastava et al. 2019). Based on account of informations, this paper first attempts to define endophytes, followed by a brief insight into bacterial and fungal classification and taxonomic diversity. This chapter is also an account on role of endophytes in plant growth-promoting activities via direct and indirect ways. Their widespread environment-friendly applications in biotic and abiotic stress alleviation, in medicinal, industrial, and environmental applications have also been described. An overall overview of the advanced “omic” tools that could be used to get complete informations about endophytic genome and proteome functions and their interactions with hosts, potentialities, and secondary metabolites.

8.2 Definition of Endophytes Microbial endophytes have been known for more than a century, they mainly include fungi, bacteria, and actinomycetes. Their definition changed over time, in 1866 the term “endophyte” was first introduced by de Bary, it was originated from the Greek words endon: within and phyte: plant (Bary 1866). In 1926 endophytic behavior was defined as a particular stage (symbiotic mutualism) in the bacterial life cycle (Perotti 1926). From that moment, endophytes were defined as microorganisms being isolated from host plants after surface sterilization (Henning and Villforth 1940). Hollis defined endophytes more accurately as being microorganisms existing inside plant organs without causing disease symptoms (Hollis 1951). Several other definitions, differing from one another, were attributed to the term endophyte. Quispel

8 Biotechnology and Bioinformatics of Endophytes …

183

(1992) mentioned that they are microorganisms that establish beneficial cooperation (endosymbiosis) with plants. In the same year, Kado (1992) included neutral bacteria (reside in the interior of living plants and benefit from a secure residence) to the endophytic community. In 1997, James and colleagues stated that all microorganisms colonizing internal plant tissues, including active and latent pathogens were considered endophytes (James et al. 1997). In agronomy, endophyte definition was expanded to cover all microorganisms emerging from surface-sterilized plant tissues and establishing mutualistic associations with host plants, but cause no symptoms of the disease (Hallmann et al. 1997; Azevedo et al. 2000). Schulz and Boyle (2006) defined endophytes as microorganisms colonizing internal plant tissues without causing any injuries and or adverse reaction on their host, whereas Thrall et al. (2007) pointed out that endophytes result from a positive selection to invade the plants’ tissues, during at least a period of their life cycle and perform mutualistic associations with them. The concept of endophytism was defined in several ways, however many scientists approved that endophytic microbial communities reside inside plant tissues with no harmful effect to hosts (Johnston-Monje and Raizada 2011; Hardoim et al. 2012; Gupta et al. 2013; Sarethy et al. 2019).

8.3 Endophytes Ongoing Researches and Major Trends An active international community has specialized in endophyte research (Fig. 8.1). Ongoing researches are multidisciplinary and involve many fields mainly Plant

Fig. 8.1 Bar-chart of international scientific community studies on endophytes

184

H. B. Slama et al.

sciences, Microbiology, Mycology, Biotechnology, Ecology, and Agronomy. The publication rate was doubled during last 5 years suggesting that the field is more and more attractive to researchers. USA, China, Germany, and India are the main countries for such scientific research.

8.4 Endophyte Taxonomic Affinities Endophyte taxonomic affinity is constantly updated by the huge mass of sequences that are being deposited in databases. In this report, we checked the taxonomic affinity of endophytes by monitoring bacterial 16S-rDNA and fungal ITS-rDNA sequences in GenBank. Two taxonomic divisions have been checked the phylum and the genus levels. a. Bacterial endophytes taxonomic affinities Our analysis documented that bacterial endophyte communities are dominated by proteobacteria (57.24%). This is in line with the results reported by Santoyo et al. (2016) and Belbahri et al. (2017). α, β, γ, and δ proteobacteria represented respectively 17.67, 22.94, 16.6, and 0.03% of the reported bacterial endophyte community in GenBank. Less abundant phyla were represented by Firmicutes (18.38%), Actinobacteria (13.89%), and Enterobacteria (8.74%). Remaining phyla represent all together lesser than 2% of the endophytic bacterial communities (Fig. 8.2). Similar results have also been reported in many endophytes targeted studies (Cheffi et al. 2019; Cherif-Silini et al. 2019; Slama et al. 2018, 2019). The most commonly reported endophytic genera are Burkholderia (16.88%), Bacillus (15.13%), Methylorubrum (12.04%), Enterobacter (6.02%), Herbaspirillum (5.94%), Streptomyces (5.43%), Pseudomonas (5.41%), and Pantoea (4.37%). (Alenezi et al. 2016; Slama et al. 2018, 2019). b. Fungal endophytes taxonomic affinities Our survey of fungal endophyte ITS-rDNA attested that belongs to Ascomycota (96.82%). Basidiomycetes represented 3.06% and Glomeromycota represented only 0.12%. These results corroborate earlier findings (Mefteh et al. 2017, 2018, 2019; White et al. 2019; Haro and Benito 2019). At the genus level Ustilago (13.42%), Fusarium (5.82%), Gibberella (5.7%), Colletotrichum (4.96%), Alternaria (4.48%), and Diaporthe (4.47%) dominated fungal endophyte communities (Fig. 8.3).

8.5 Endophyte Lifestyle The host-associated microbial communities are classified into obligate and facultative endophytes. Obligate endophytes are culture-independent and are revealed through molecular approaches, whereas facultative endophytes are culture-dependent and

8 Biotechnology and Bioinformatics of Endophytes …

185

Fig. 8.2 Pie-chart of endophytic bacteria community based on 16S-rDNA

can be revealed through the application of diversified nutrient media (Christina et al. 2013; Goulart et al. 2019; Srivastava et al. 2019). These approaches have several advantages and drawbacks that are discussed in the two following sections. a. Culture dependent approach Cultivable endophytes could be easily isolated, manipulated, and further exploited in the development of different fields (agricultural, medical, industrial, etc.) as reviewed by Maela and Serepa-Dlamini (2019). The inherent limitation of this approach is that it is estimated to detect 0.1–1% of the existing microbiome (Stewart 2012; Belbahri et al. 2017; Mefteh et al. 2017, 2019).

186

H. B. Slama et al.

Fig. 8.3 Pie-chart of endophytic fungal community based on ITS-rDNA

b. Culture-independent approach The main advantage of this culture-dependent approach is that it allows the detection of endophyte fraction missed by plating (>99%) by using polymerase chain reaction (PCR) and multiple sequencing techniques (Ma et al. 2016; Doherty et al. 2017). The main drawbacks of this approach are that it does not recover the entire microbial strains (Srivastava et al. 2019) and that the use of low specific primers could interfere with the amplification process (Mefteh et al. 2019). The combination of these two methods for endophytic isolation, therefore, gave a broad comprehension of the endophytic diversity within host plants (Maropola et al. 2015; Santoyo et al. 2016, Mefteh et al. 2019).

8 Biotechnology and Bioinformatics of Endophytes …

187

8.6 Plant Growth-Promoting Mechanisms The mechanisms employed by soil bacteria and mycorrhizal (AM) fungi to enhance plant growth have been well studied (Glick 2012; Pereira and Castro 2014; Vimal et al. 2017). These microbes may affect plant growth either directly or indirectly (Fig. 8.4) (Paungfoo-Lonhienne et al. 2014; Gond et al. 2015). a. Direct plant growth promotion Endophytic bacteria and fungi possess direct plant growth-promoting potentials through, improving nutrient acquisition or mobilization, regulating or producing phytohormones, and through enhancing the antioxidant system, etc. (Vardharajula et al. 2011; White et al. 2019).

Fig. 8.4 Mechanisms employed by soil bacteria and mycorrhizal (AM) fungi to enhance plant growth

188

H. B. Slama et al.

The nutrient acquisition enhancement includes typically: atmospheric nitrogen fixation, siderophores production, and phosphorus solubilization. Although, some workers have also studied the potassium and zinc solubilization (Bhatt and Maheshwari 2020). Sulphur oxidation studies have recently been observed from the nonrhizospheric bacteria (Dhiman et al. 2020). Modulation of hormone levels may entail the synthesis or regulation of one or more plant phytohormones such as auxins (Gaby and Buckley 2011; Verma et al. 2014) mostly indole acetic acid (IAA), gibberellins, and cytokinins. Some PGPB reduces ethylene levels by synthesizing 1aminocyclopropane-1-carboxylate (ACC) deaminase enzyme, which cleaves ACC, the precursor of ethylene in all higher plants (Zahir et al. 2011). Maheshwari and colleague have been reported the role of Bacillus sp. with ACC deaminase production ability and other endophytes such as Sinorhizobium meliloti bear acdS gene conferring ACC deaminase (Kumar et al. 2012; Maheshwari et al. 2015; Aeron et al. 2014).

8.6.1 Atmospheric Nitrogen Fixation Nitrogen (N) belongs to the most essential elements that are responsible for plant growth. Plants are not able to use atmospheric nitrogen directly (Santi et al. 2013). Therefore, the use of beneficial microbes is an environment-friendly technique that enhances nitrogen fixation (Gaby and Buckley 2011; Verma et al. 2014) in both leguminous and non-leguminous plants.

8.6.2 Phosphorus Solubilization Phosphorus (P) is an important nutrient for plant growth and sustainability. It is involved in several metabolic processes (Li et al. 2017). Yet, it cannot be easily assimilated by plants because of its insoluble form (Ahemad and Kibret 2014). Microbial phosphate solubilization is required to enhance phosphate availability by secreting several organic acids (Haile et al. 2016; Chauhan et al. 2017) and other mechanisms involved in P-solubilization.

8.6.3 Siderophore Production Iron is extremely necessary for plants (Curie and Mari 2017; Tsai and Schmidt 2017). The predominant iron form in nature is a ferric ion (Fe3+ ), it is only sparingly soluble, which explains the difficulty of its assimilation by plants. Microbes are the major precursors of iron uptake through specific pathways, including siderophores production (Ahemad and Kibret 2014; Ahmad et al. 2017).

8 Biotechnology and Bioinformatics of Endophytes …

189

Bacterial siderophores are implicated directly by stimulating nutrient uptake and indirectly by sequestering Fe3+ in the areas around the roots, to prevent its assimilation by pathogenic microorganisms and thus help in disease inhibition (Hayat et al. 2010).

8.6.4 Phytohormones Synthesis and Regulation Indole-3-acetic acid (IAA): Microbial auxin is a vital regulatory phytohormone (Kuhn et al. 2017). Synthesis of phytohormone auxin by microbes is well known for a long time ago. Also, IAA contributes to plant cell elongation by increasing cell osmosis, increasing cell permeability to water, increasing cell wall synthesis, decreasing wall pressure, and inhibiting or decaying leaves abscission (Muday et al. 2012; Mohite 2013). Tryptophan is an amino acid synthesized by beneficial microbes and acts as the major precursor of IAA (Gamalero and Glick 2015) and determines the induced and constitutive nature of IAA in various microorganisms. Cytokinins (CKs): Cytokinins (CKs) are compounds with a structure resembling adenine (Sakakibara et al. 2006). Their name comes from their capacity of cytokinesis or plants mitosis enhancement. Cytokinins are synthesized by plants, and several soil microorganisms (Dodd et al. 2003). Cytokine mediating-beneficial microbes act as plant growth promotors and biotic and abiotic stress inhibitors by producing or altering CKs homeostasis (O’Brien and Benkova 2013; Ritika and Mohinder 2016; Großkinsky et al. 2016). Gibberellins: The phytohormone gibberellin has an important effect on host plant development as it could regulate numerous biological processes, starting from cell division, elongation, and differentiation to fruit development and senescence (Bueso et al. 2016). Gibberellic acid (GA), is the main gibberellin product. GA producing PGPRs act by regulating GA levels in plants by increasing root surface and length (Sharma and Kaur 2018; Khan et al. 2018) and enhance plant growth and development. Abscisic Acid (ABA): Abscisic acid (ABA) is a critical plant stress hormone (Sah et al. 2016). It is responsible for the regulation of various physiological processes in stressed plants, such as limiting seed germination, inhibiting the growth of shoots and roots, and stomatal sealing (Cohen et al. 2015). PGPM’s ability to alter ABA levels in plants suggests their importance in influencing plant growth and abiotic stress resistance (Dodd et al. 2003). Jasmonic acid (JA): Being a signal molecule, jasmonic acid (JA) responds to wound and pathogenesis attacks, by upholding secondary metabolites production in plants (Gu et al. 2012; Du et al. 2013). It also increases the abundances of bacterial populations, having phytopathogens, and insects suppressive abilities (Carvalhais et al. 2013). Additionally, plants under pathogenic attack may evolve mechanisms to recruit symbionts that synthesize JA to enhance their tolerance to both the biotic and abiotic stresses (Liu et al. 2017; Ahmad et al. 2017).

190

H. B. Slama et al.

Ethylene and ACC Deaminase: Ethylene is a gaseous hormone that is responsible for plant growth. The biosynthesis of ethylene starts by converting Sadenosylmethionine (SAM) to 1-aminocyclopropane-1-carboxylate (ACC) by 1aminocyclopropane-1-carboxylate synthase (ACS) enzyme. Ethylene level gets elevated when exposed to stress conditions, resulting in reducing plant growth (Hardoim et al. 2008). In this case, bacteria could interfere by sequestering plant ACC and breaking it down into ammonia and α-ketobutyrate, thus reducing ethylene negative effect, enhancing plant stress resistance, and plant development (Naveed et al. 2014; Noumavo et al. 2016). b. Indirect plant growth promotion Bacterial indirect plant growth promotion is achieved by limiting abiotic stresses or preventing the deleterious effects of pathogenic organisms, via (i) biological control of pathogens (producing inhibitory allelochemicals, antibiotics, and cell walldegrading enzymes), (ii) parasitism, (iii) competition for niches and bioavailable nutrients, (iv) signal interference (quorum sensing), (v) volatile compounds synthesis (VOCs), and (vi) inducing systemic resistance (ISR) (Glick 2012; Alvin et al. 2014; Sheoran et al. 2015).

8.6.5 Production of Cell Wall-Degrading Enzymes Microbial cell wall-degrading enzymes play a major role in host plant protection from biotic stresses (Goswami et al. 2016). Extracellular enzymes produced by endophytic strains include chitinases, dehydrogenases, β-glucanases, amylases, cellulases, lipases, etc. (Gupta et al. 2015). Both chitinase and β-glucanase are effective in inhibiting the proliferation of hyphal by lysis and detangling of mycelia and other morphologies of fungal pathogens (Vejan et al. 2016).

8.6.6 Hydrogen Cyanide Production (HCN) Volatile compounds production include hydrogen cyanide (HCN), aldehydes, alcohols, ketones, etc. (Ulloa-Ogaz et al. 2015). Particularly, HCN is a key factor of disease proliferation (Ramette et al. 2003), since cyanide is a metabolic inhibitor that acts by protecting plants from colonization or competition (Passari et al. 2016).

8.6.7 Volatile Organic Compounds (VOCs) The low molecular weight volatile organic compounds (VOCs) involve phenylpropanoids, terpenoids, and fatty acid derivatives, they are endowed with

8 Biotechnology and Bioinformatics of Endophytes …

191

antipathogenic and plant growth capacities. The endophytic bacteria act as biocontrol agents that synthesize VOCs as a part of their metabolism (Liu and Zhang 2015). VOCs pass freely through biological membranes and may be released into the soil or the atmosphere (Cappellari et al. 2019).

8.6.8 Competition for Space and Nutrients The rhizospheric soil is very rich in carbon. Therefore, it represents a source of attraction to diverse microbes, including phytopathogens (Ramamoorthy et al. 2001). Biological control agents occupy similar niches as pathogens and gradually outcompete them for occupancy (Handelsman and Stabb 1996) and “precious” nutrients, leading to a reduction in nutrient availability to phytopathogens (Thakur and Singh 2018).

8.6.9 Antibiosis and Antibiotics Antibiosis is a mechanism by which the biocontrol agent produces several secondary metabolites to inhibit or suppress pathogens (Haas and Défago 2005). Antibiotics production is the main biocontrol mechanism employed by a variety of antagonistic microbes in the rhizosphere. They are defined as a group of low-molecular weight organic compounds that are effective in suppressing bacterial growth (Glick et al. 2007).

8.6.10 Detoxification and Degradation of Pathogens Virulence Factors Microbial pathogens could produce toxins aiming at inhibiting antagonistic microorganisms. Moreover, it was recently demonstrated that certain beneficial bacteria could attenuate pathogen quorum-sensing abilities. Thus, they block virulence genes expression, because bacterial phytopathogens require series of quorum-sensing signals to activate their virulence factors (von Bodman et al. 2003).

8.6.11 Induced Systemic Resistance (ISR) Induced systemic resistance (ISR) is a defense mechanism enhanced by microbial endophytes to enhance the plant’s protective levels against a wide range of pathogens

192

H. B. Slama et al.

(Alvin et al. 2014). ISR activation majorly occurs through the SA-independent pathway involving jasmonate and ethylene signals (Pettersson and Baath 2004). They increase the sensitivity to these hormones, to activate several defense genes (Hase et al. 2003).

8.7 Biological Applications of Endophytic Microorganisms Nowadays, endophytic microorganisms have been used in multiple fields as biological alternatives to chemical compounds. These microbial populations were involved in biocontrol of phytopathogens, plant growth stimulation, phytoremediation, bioremediation, medicinal and industrial applications (Strobel and Daisy 2003; Schulz 2006; Jalgaonwala et al. 2011; Godstime et al. 2014; Shukla et al. 2014; Chaudhry et al. 2017; Uzma et al. 2018). a. Biological control Biological control or Biocontrol is the use of microbial antagonists to manage or inhibit plant pathogens (bacteria, fungi, viruses, and nematodes) (Mehta et al. 2014). This environment-friendly approach may be an effective solution to get rid of chemical pesticides in the agricultural sector. Therefore, the bioformulation of beneficial microorganisms could help in enhancing and maintaining plant productivity naturally and cost-effectively (Guédez et al. 2008; Griffin 2014; Nion and Toyota 2015; Kergunteuil et al. 2016; Alenezi et al. 2017; Høyer et al. 2019). b. Bioremediation Bioremediation process implies the use of microbial populations to remove or lessen pollutants (heavy metals, dye, organic compounds, crude oil, etc.) toxicity from the biosphere (Kinoshita et al. 2008; Zhou et al. 2014; Limcharoensuk et al. 2015; Govarthanan et al. 2016; Ijaz et al. 2016; Bharagava et al. 2017; Mefteh et al. 2019). It is achieved through two major mechanisms: biosorption which is one of the most convenient techniques of sequestration. It binds contaminants onto the cell walls of microorganisms (Kousha et al. 2012; Bera et al. 2016; Chew and Ting 2016; Ting et al. 2016) and bioaccumulation consisting of transporting and precipitating toxic elements into microbial cells (Kiran et al. 2017) and transforming them into non-toxic forms (Sathish et al. 2012; Sim et al. 2018, 2019). c. Phytoremediation The association of plant-microbes is a perfect combination to solve environmental pollution/contamination in a maintained, cost-effective, and environment-friendly manner (Glick 2010; Shin et al. 2012; Chen et al. 2014; Dharni et al. 2014; Ma et al. 2015; Chirakkara et al. 2016, Rekik et al. 2017; Mefteh et al. 2019). Recently, heavy metal removal/alleviation by endophytes has been highly studied (Weyens et al. 2009; Luo et al. 2011; Langella et al. 2014), it is achieved via multiple methods

8 Biotechnology and Bioinformatics of Endophytes …

193

including metal precipitation, biodegradation, biotransformation, bioaccumulation, and sequestration (Zhu et al. 2014; Babu et al. 2015). d. Medicinal application Medicinal plants constitute a reservoir of tremendous bioactive metabolites used for disease treatments from ancient times (Paramanantham et al. 2019). During the last few decades, researchers have discovered several interesting medicinal/pharmaceutical drugs and antibiotics originating from diverse endophytic microbes living inside medicinal and non-medicinal plants. They have inherent potentials to produce bioactive metabolic compounds possessing therapeutic properties to treat numerous infections and diseases (Kusari et al. 2014) such as cancer, diabetic, microbial, fungal, and viral diseases (Strobel and Daisy 2003; Huang et al. 2007; Yu et al. 2010; Kharwar et al. 2011; Akone et al. 2016; Mefteh et al. 2017; Venieraki et al. 2017). Singh and Dubey (2015) reported that natural compounds originating from the medicinal plants-endophytes association, constitute above 50% of natural products in the market and this was further confirmed by Passari et al. (2017). The same endophytic strain isolated from several medicinal plants could produce diverse biological activities through the production of several medicinal compounds (Tan and Zou 2001; Khiralla et al. 2017).

8.8 Omic Approaches for Endophytes Traditional methods used to identify and characterize endophytic microbes were supported by in silico approaches which help in understanding the functional potentialities of endophytes (Gianoulis et al. 2012; Nicolas et al. 2014; Chetia et al. 2019). The number of microbial omic studies have been developed rapidly in the recent years due to the next generation sequencing (NGS) methods which are increasingly lowering their costs (Kodama et al. 2011; Kaul et al. 2016; Belbahri et al. 2017; Slama et al. 2018; Cheffi et al. 2019). Nowadays, there is a large amount of whole bacterial and fungal genomes that have been sequenced and stored in several open-access databases and platforms (Figs. 8.5 and 8.6). The combination of omic approaches (genomic, transcriptomic, metabolomics, and proteomics) allowed exploration of endophytes potentials and their interactions with hosts. In fact, (i) genomic is the technology of total genome sequencing of microorganisms (Campisano et al. 2014; Akinsanya et al. 2015; Belbahri et al. 2017; Sengupta et al. 2017; Correa-Galeote et al. 2018), (ii) transcriptomic studies provide instructions about gene status (AguiarPulido et al. 2016), (iii) metabolomic allow identification of novel secondary metabolites exhibited by microbes (Rasmussen et al. 2011; Chetia et al. 2019), (iv) lastly proteomic is a multivariate technology of endophytic proteins expression (Kaul et al. 2016; Peng et al. 2019).

194

H. B. Slama et al.

Fig. 8.5 Pie-chart of endophytic bacteria community based on whole genome

8.9 Conclusion and Prospects While endophytes have been known for more than a century, they only recently found their way to applied research. Present applications include diverse fields including agriculture, medicine, industry, pharmacology, bio, and phytoremediation. It has been proven that endophytes could be more reliable and low-cost sources of natural drugs than chemical compounds because of their intimate associations with plants and their non-harmful effects on the environment. In the prospects, it is essential to understand the mechanisms interfering in plant–endophytes and endophyte–endophyte

8 Biotechnology and Bioinformatics of Endophytes …

195

Fig. 8.6 Pie-chart of endophytic fungal community based on whole genome

interactions to accomplish all biotechnological applications. Additionally, further research in emerging “omic” technologies involving transcriptomics, metagenomics, and metatranscriptomics approaches predict discoveries that will unravel plant–endophytes relationships and will strengthen the potential use of endophytes in applied research. Microbial secretomes and volatiles are also widely investigated. It is estimated that the genomic and metabolic data mining will ultimately provide new insights into their successful implementation in all the above discussed fields.

References Aeron A, Chauhan PS, Dubey RC et al. (2014) Root nodule bacteria from Clitoria ternatea L. are putative invasive nonrhizobial endophytes. Can J Microbiol 61(2):131–142 Aguiar-Pulido V, Huang W, Suarez-Ulloa V, Cickovski T, Mathee K, Narasimhan G (2016) Metagenomics, metatranscriptomics, and metabolomics approaches for microbiome analysis: supplementary issue: bioinformatics methods and applications for big metagenomics data. Evol Bioinform 12. http://doi.org/10.4137/EBO.S36436

196

H. B. Slama et al.

Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20. https://doi.org/10.1016/j.jksus.2013.05.001 Ahmad P, Alyemeni MN, Wijaya L, Alam P, Ahanger MA, Alamri SA (2017) Jasmonic acid alleviates negative impacts of cadmium stress by modifying osmolytes and antioxidants in faba bean (Vicia faba L.). Arch Agron Soil Sci 63:1889–1899. https://doi.org/10.1080/03650340.2017. 1313406 Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6:159–163. https://doi.org/10.1016/j. gdata.2015.09.004 Akone SH, Mándi A, Kurtán T, Hartmann R, Lin W, Daletos G, Proksch P (2016) Inducing secondary metabolite production by the endophytic fungus Chaetomium sp. through fungal– bacterial co-culture and epigenetic modification. Tetrahedron 72:6340–6347. https://doi.org/10. 1016/j.tet.2016.08.022 Alenezi FN, Rekik I, Belka M, Ibrahim AF, Luptakova L, Jaspars M, Woodward S, Belbahri L (2016) Strain-level diversity of secondary metabolism in the biocontrol species Aneurinibacillus migulanus. Microbiol Res 182:116–124. https://doi.org/10.1016/j.micres.2015.10.007 Alenezi FN, Rekik I, Chenari Bouket A, Luptakova L, Weitz HJ, Rateb ME, Jaspars M, Woodward S, Belbahri L (2017) Increased biological activity of Aneurinibacillus migulanus strains correlates with the production of new gramicidin secondary metabolites. Front Microbiol 8:517. https://doi. org/10.3389/fmicb.2017.00517 Alvin A, Miller KI, Neilan BA (2014) Exploring the potential of endophytes from medicinal plants as sources of antimycobacterial compounds. Microbiol Res 169:483–495. https://doi.org/10.1016/ j.micres.2013.12.009 Azevedo JL, Maccheroni W Jr, Pereira JO, de Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:15–16. https://doi.org/10.2225/vol3-issue1-fulltext-4 Babu AG, Shea PJ, Sudhakar D, Jung I-B, Oh B-T (2015) Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal (loid)-contaminated mining site soil. J Environ Manag 151:160–166. https://doi.org/10.1016/j.jenvman.2014.12.045 Bary A (1866) Morphologie und physiologie der pilze, flechten und myxomyceten. W Engelmann. https://doi.org/10.5962/bhl.title.120970 Belbahri L, Chenari Bouket A, Rekik I, Alenezi FN, Vallat A, Luptakova L, Petrovova E, Oszako T, Cherrad S, Vacher S (2017) Comparative genomics of Bacillus amyloliquefaciens strains reveals a core genome with traits for habitat adaptation and a secondary metabolites rich accessory genome. Front Microbiol 8:1438. https://doi.org/10.3389/fmicb.2017.01438 Bera S, Sharma VP, Dutta S, Dutta D (2016) Biological decolorization and detoxification of malachite green from aqueous solution by Dietzia maris NIT-D. J Taiwan Inst Chem E 67:271–284 Bharagava RN, Chowdhary P, Saxena G (2017) Bioremediation: an eco-sustainable green technology: its applications and limitations. In: Environmental pollutants and their bioremediation approaches. CRC Press, Boca Raton, pp 1–22 Bhatt K, Maheshwari DK (2020) Zinc solubilizing bacteria (Bacillus megaterium) with multifarious plant growth promoting activities alleviates growth in Capsicum annuum L. 3 Biotech 10(2):36 Bueso E, Muñoz-Bertomeu J, Campos F, Martínez C, Tello C, Martínez-Almonacid I, Ballester P, Simón-Moya M, Brunaud V, Yenush L (2016) Arabidopsis COGWHEEL 1 links light perception and gibberellins with seed tolerance to deterioration. The Plant J 87:583–596. https://doi.org/10. 1111/tpj.13220 Campisano A, Antonielli L, Pancher M, Yousaf S, Pindo M, Pertot I (2014) Bacterial endophytic communities in the grapevine depend on pest management. PLoS One 9:e112763. https://doi. org/10.1371/journal.pone.0112763 Cappellari L del R, Chiappero J, Banchio E (2019) Invisible signals from the underground: A practical method to investigate the effect of microbial volatile organic compounds emitted by rhizobacteria on plant growth. Biochem Mol Biol Educ 47(4):388–393. http://doi.org/10.1002/ bmb.21243

8 Biotechnology and Bioinformatics of Endophytes …

197

Carvalhais LC, Dennis PG, Badri DV, Tyson GW, Vivanco JM, Schenk PM (2013) Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLoS One 8:e56457. https://doi.org/10.1371/journal.pone.0056457 Chaudhry V, Sharma S, Bansal K, Patil PB (2017) Glimpse into the genomes of rice endophytic bacteria: diversity and distribution of firmicutes. Front Microbiol 7:2115. https://doi.org/10.3389/ fmicb.2016.02115 Chauhan A, Guleria S, Balgir PP, Walia A, Mahajan R, Mehta P, Shirkot CK, Chauhan A, Guleria S, Balgir PP, Walia A, Mahajan R, Mehta P, Shirkot CK (2017) Tricalcium phosphate solubilization and nitrogen fixation by newly isolated Aneurinibacillus aneurinilyticus CKMV1 from rhizosphere of Valeriana jatamansi and its growth promotional effect. Brazilian J Microbiol 48:294–304. https://doi.org/10.1016/j.bjm.2016.12.001 Cheffi M, Chenari Bouket A, Alenezi FN, Luptakova L, Belka M, Vallat A, Rateb ME, Tounsi S, Triki MA, Belbahri L (2019) Olea europaea L. root endophyte Bacillus velezensis OEE1 counteracts oomycete and fungal harmful pathogens and harbours a large repertoire of secreted and volatile metabolites and beneficial functional genes. Microorganisms 7(9):E314. https://doi. org/10.3390/microorganisms7090314 Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014) Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308. https://doi.org/10.1016/j.soilbio.2013.10.021 Cherif-Silini H, Thissera B, Chenari Bouket A, Saadaoui N, Silini A, Eshelli M, Alenezi FN, Vallat A, Luptakova L, Yahiaoui B (2019) Durum wheat stress tolerance Induced by endophyte Pantoea agglomerans with genes contributing to plant functions and secondary metabolite arsenal. Int J Mol Sci 20(16):3989. https://doi.org/10.3390/ijms20163989 Chetia H, Kabiraj D, Bharali B, Ojha S, Barkataki MP, Saikia D, Singh T, Mosahari PV, Sharma P, Bora U (2019) Exploring the benefits of endophytic fungi via Omics. In: Advances in endophytic fungal research. Springer, Cham, pp 51–81 Chew SY, Ting ASY (2016) Common filamentous Trichoderma asperellum for effective removal of triphenylmethane dyes. Desalin Water Treat 57:13534–13539. https://doi.org/10.1080/19443994. 2015.1060173 Chirakkara RA, Cameselle C, Reddy KR (2016) Assessing the applicability of phytoremediation of soils with mixed organic and heavy metal contaminants. Rev Environ Sci Biotechnol 15:299–326. https://doi.org/10.1007/s11157-016-9391-0 Christina A, Christapher V, Bhore SJ (2013) Endophytic bacteria as a source of novel antibiotics: an overview. Pharmacogn Rev 7(13):11–16. https://doi.org/10.4103/0973-7847.112833 Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 153(1):79–90. https://doi.org/10.1111/ppl. 12221 Correa-Galeote D, Bedmar EJ, Arone GJ (2018) Maize endophytic bacterial diversity as affected by soil cultivation history. Front Microbiol 9:484. https://doi.org/10.3389/fmicb.2018.00484 Curie C, Mari S (2017) New routes for plant iron mining. New Phytol 2:521–525. https://doi.org/ 10.1111/nph.14364 Dharni S, Srivastava AK, Samad A, Patra DD (2014) Impact of plant growth promoting Pseudomonas monteilii PsF84 and Pseudomonas plecoglossicida PsF610 on metal uptake and production of secondary metabolite (monoterpenes) by rose-scented geranium (Pelargonium graveolens cv. bourbon) grown on tannery sludge amended soil. Chemosphere 117:433–439. https://doi.org/ 10.1016/j.chemosphere.2014.08.001 Dhiman S, Baliyan N, Maheshwari DK (2020) Buffalo dung-inhabiting bacteria enhance the nutrient enrichment of soil and proximate contents of Foeniculum vulgare Mill. Arch Microbiol 30:1 Dodd IC, Tan LP, He J (2003) Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation? J Exp Bot 54:1281–1288. https://doi.org/10.1093/ jxb/erg122

198

H. B. Slama et al.

Doherty M, Yager PL, Moran MA, Coles VJ, Fortunato CS, Krusche AV, Medeiros PM, Payet JP, Richey JE, Satinsky BM (2017) Bacterial biogeography across the Amazon River-ocean continuum. Front Microbiol 8:882. https://doi.org/10.3389/fmicb.2017.00882 Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397. https://doi.org/10.3389/fpls.2013. 00397 Eevers N, Gielen M, Sánchez-López A, Jaspers S, White JC, Vangronsveld J, Weyens N (2015) Optimization of isolation and cultivation of bacterial endophytes through addition of plant extract to nutrient media. Microb Biotechnol 8:707–715. https://doi.org/10.1111/1751-7915.12291 Fakruddin M, Mannan K (2013) Methods for analyzing diversity of microbial communities in natural environments. Ceylon J Sci (Biol Sci) 42(1):19–33. https://doi.org/10.4038/cjsbs.v42i1. 5896 Finkel OM, Salas-González I, Castrillo G, Spaepen S, Law TF, Teixeira PJPL, Jones CD, Dangl JL (2019) The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLoS Biol 17(11):e3000534. https://doi.org/10.1371/journal.pbio.3000534 Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity. Environ Microbiol 13:1790– 1799. https://doi.org/10.1111/j.1462-2920.2011.02488.x Gamalero E, Glick BR (2015) Bacterial modulation of plant ethylene levels. Plant Physiol 169:13– 22. https://doi.org/10.1104/pp.15.00284 Gianoulis TA, Griffin MA, Spakowicz DJ, Dunican BF, Sboner A, Sismour AM, Kodira C, Egholm M, Church GM, Gerstein MB (2012) Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet 8:e1002558. https://doi.org/10. 1371/journal.pgen.1002558 Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. https://doi.org/10.1016/j.biotechadv.2010.02.001 Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012. http://doi.org/10.6064/2012/963401 Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242. https://doi.org/10.1080/073526807 01572966 Godstime CO, Felix OE, Augustina OJ, Christopher OC (2014) Mechanisms of antimicrobial actions of phytochemicals against enteric pathogens—a review. J Pharm Chem Biol Sci 2:77–85 Gond SK, Bergen MS, Torres MS, White JF, Kharwar RN (2015) Effect of bacterial endophyte on expression of defense genes in Indian popcorn against Fusarium moniliforme. Symbiosis 66:133–140. https://doi.org/10.1007/s13199-015-0348-9 Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500. https://doi.org/10.1080/233 11932.2015.1127500 Goulart MC, Cueva-Yesquén LG, Hidalgo Martinez KJ, Attili-Angelis D, Fantinatti-Garboggini F (2019) Comparison of specific endophytic bacterial communities in different developmental stages of Passiflora incarnata using culture-dependent and culture-independent analysis. Microbiol Open 8(10):e896. https://doi.org/10.1002/mbo3.896 Govarthanan M, Mythili R, Selvankumar T, Kamala-Kannan S, Rajasekar A, Chang Y-C (2016) Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech 6:242. https://doi.org/10.1007/s13205-0160560-1 Griffin MR (2014) Biocontrol and bioremediation: two areas of endophytic research which hold great promise. In: Advances in endophytic research. Springer, New York, pp 257–282 Großkinsky DK, Tafner R, Moreno MV, Stenglein SA, García de Salamone IE, Nelson LM, Novák O, Strnad M, van der Graaff E, Roitsch T (2016) Cytokinin production by Pseudomonas fluorescens G20-18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis. Sci Rep 6:23310. https://doi.org/10.1038/srep23310

8 Biotechnology and Bioinformatics of Endophytes …

199

Gu X-C, Chen J-F, Xiao Y, Di P, Xuan H-J, Zhou X, Zhang L, Chen W-S (2012) Overexpression of allene oxide cyclase promoted tanshinone/phenolic acid production in Salvia miltiorrhiza. Plant Cell Rep 31:2247–2259. https://doi.org/10.1007/s00299-012-1334-9 Guédez C, Castillo C, Cañizales L, Olivar R (2008) Biological control a tool for sustaining and sustainable development. Control Biol 7:50–74. https://doi.org/10.1098/rstb.2007.2182 Gupta G, Panwar J, Jha PN (2013) Natural occurrence of Pseudomonas aeruginosa, a dominant cultivable diazotrophic endophytic bacterium colonizing Pennisetum glaucum (L.) R. Br Appl Soil Ecol 64:252–261. https://doi.org/10.1016/j.apsoil.2012.12.016 Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:096–102. https://doi.org/10.4172/1948-5948.100018 Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307. https://doi.org/10.1038/nrmicro1129 Haile D, Mekbib F, Assefa F (2016) Isolation of phosphate solubilizing bacteria from white Lupin (Lupinus albus L.) rhizosphere soils collected from Gojam, Ethiopia. J Fertil Pestic 7:172. https:// doi.org/10.4172/2471-2728.1000172 Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Canadian J Microbiol 43:895–914. https://doi.org/10.1139/m97-131 Handelsman J, Stabb E (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8:1855–1869. https://doi.org/10.1105/tpc.8.10.1855 Hardoim PR, Hardoim CC, Van Overbeek LS, Van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438. https://doi.org/10.1371/journal. pone.0030438 Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10. 1128/MMBR.00050-14 Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. https://doi.org/10.1016/j.tim.2008. 07.008 Haro R, Benito B (2019) The role of soil fungi in K + plant nutrition. Int J Mol Sci 20(13):3169. https://doi.org/10.3390/ijms20133169 Hase S, Van Pelt JA, Van Loon LC, Pieterse CMJ (2003) Colonization of Arabidopsis roots by Pseudomonas fluorescens primes the plant to produce higher levels of ethylene upon pathogen infection. Physiol Mol Plant Pathol 62:219–226. https://doi.org/10.1016/S0885-5765(03)000 59-6 Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. https://doi.org/10.1007/s13213-0100117-1 Henning K, Villforth F (1940) Experimentelle untersuchungen zur frage der bacteriesymbiose in höheren pflanzen und ihre beeinflussung durch ‘Leitemente’. Biochem Z 305:299–309 Hollis EV (1951) Social work education in the United States: the report of a study made for the National Council on Social Work Education. Columbia University Press. https://doi.org/10.5860/ crl_13_04_395 Hong CE, Kim JU, Lee JW, Bang KH, Jo IH (2019) Metagenomic analysis of bacterial endophyte community structure and functions in Panax ginseng at different ages. 3 Biotech 9:300. https:// doi.org/10.1007/s13205-019-1838-x Høyer AK, Jørgensen HJ, Jensen B, Murphy BR, Hodkinson TR (2019) Emerging methods for biological control of barley diseases including the role of endophytes. In: Endophytes for a growing world. Cambridge University Press,Cambridge, pp. 93–119 Huang H, She Z, Lin Y, Vrijmoed LLP, Lin W (2007) Cyclic peptides from an endophytic fungus obtained from a mangrove leaf (Kandelia candel). J Nat Prod 70:1696–1699. https://doi.org/10. 1021/np0605891

200

H. B. Slama et al.

Ijaz A, Imran A, ul Haq MA, Khan QM, Afzal M (2016) Phytoremediation: recent advances in plantendophytic synergistic interactions. Plant Soil 405:179–195. http://doi.org/10.1007/s11104-0152606-2 Jalgaonwala RE, Mohite BV, Mahajan RT (2011) A review: natural products from plant associated endophytic fungi. J Microbiol Biotechnol Res 1:21–32 James EK, Olivares FL, Baldani JI, Döbereiner J (1997) Herbaspirillum, an endophytic diazotroph colonizing vascular tissue 3 Sorghum bicolor L. Moench J Exp Bot 48:785–798. https://doi.org/ 10.1093/jxb/48.3.785 Jasim B, Joseph AA, John CJ, Mathew J, Radhakrishnan EK (2014) Isolation and characterization of plant growth promoting endophytic bacteria from the rhizome of Zingiber officinale. 3 Biotech 4:197–204. https://doi.org/10.1007/s13205-013-0143-3 Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396. https:// doi.org/10.1371/journal.pone.0020396 Kado CI (1992) Plant pathogenic bacteria. Prokaryotes, pp 660–662 Kaul S, Sharma T, K Dhar M (2016) “Omics” tools for better understanding the plant–endophyte interactions. Front Plant Sci 7:955. http://doi.org/10.3389/fpls.2016.00955 Kergunteuil A, Bakhtiari M, Formenti L, Xiao Z, Defossez E, Rasmann S (2016) Biological control beneath the feet: a review of crop protection against insect root herbivores. Insects 7:70. https:// doi.org/10.3390/insects7040070 Khan N, Martínez-Hidalgo P, Ice TA, Maymon M, Humm EA, Nejat N, Sanders ER, Kaplan D, Hirsch AM (2018) Antifungal activity of Bacillus species against Fusarium and analysis of the potential mechanisms used in biocontrol. Front Microbiol 9:2363. https://doi.org/10.3389/fmicb. 2018.02363 Kharwar RN, Mishra A, Gond SK, Stierle A, Stierle D (2011) Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat Prod Rep 28:1208–1228. https:// doi.org/10.1039/c1np00008j Khiralla A, Spina R, Yagi S, Mohamed I, Laurain-Mattar D (2017) Endophytic fungi: occurrence, classification, function and natural products. In: Endophytic fungi: diversity, characterization and biocontrol. Nova Science, pp 1–38 Kinoshita K, Tamaki S, Yoshioka M, Srithonguthai S, Kunihiro T, Ohwada K, Tsutsumi H (2008) Bioremediation of organically enriched sediment deposited below fish farms with artificially mass-cultured colonies of a deposit-feeding polychaete Capitella sp. I Fish Sci 74:77–87. https:// doi.org/10.1111/j.1444-2906.2007.01498.x Kiran YK, Barkat A, Cui X, Ying F, Pan F, Lin T, Yang X (2017) Cow manure and cow manurederived biochar application as a soil amendment for reducing cadmium availability and accumulation by Brassica chinensis L. in acidic red soil. J Integr Agric 16:725–734. http://doi.org/10. 1016/S2095-3119(16)61488-0 Kodama Y, Shumway M, Leinonen R (2011) The sequence read archive: explosive growth of sequencing data. Nucleic Acids Res 40:D54–D56. https://doi.org/10.1093/nar/gkr854 Kousha M, Daneshvar E, Sohrabi MS, Koutahzadeh N, Khataee AR (2012) Optimization of CI Acid black 1 biosorption by Cystoseira indica and Gracilaria persica biomasses from aqueous solutions. Int Biodeter Biodegr 67:56–63. https://doi.org/10.1016/j.ibiod.2011.10.007 Kuhn BM, Nodzy´nski T, Errafi S, Bucher R, Gupta S, Aryal B, Dobrev P, Bigler L, Geisler M, Zažímalová E, Friml J, Ringli C (2017) Flavonol-induced changes in PIN2 polarity and auxin transport in the Arabidopsis thaliana rol1-2 mutant require phosphatase activity. Sci Rep 7:41906. https://doi.org/10.1038/srep41906 Kumar A, Verma JP (2018) Does plant-microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52. https://doi.org/10.1016/j.micres.2017.11.004 Kumar P, Dubey RC, Maheshwari DK (2012) Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res 167(8):493–499

8 Biotechnology and Bioinformatics of Endophytes …

201

Kusari S, Singh S, Jayabaskaran C (2014) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303. https://doi.org/10.1016/j.tibtech.2014. 03.009 Langella F, Grawunder A, Stark R, Weist A, Merten D, Haferburg G, Büchel G, Kothe E (2014) Microbially assisted phytoremediation approaches for two multi-element contaminated sites. Environ Sci Pollut Res 21:6845–6858 Li Y, Ai M-J, Sun Y, Zhang Y-Q, Zhang J-Q (2017) Spirosoma lacussanchae sp. nov., a phosphatesolubilizing bacterium isolated from a freshwater reservoir. Int J Sys Evol Microbiol 67:3144– 3149. https://doi.org/10.1099/ijsem.0.001778 Limcharoensuk T, Sooksawat N, Sumarnrote A, Awutpet T, Kruatrachue M, Pokethitiyook P, Auesukaree C (2015) Bioaccumulation and biosorption of Cd2+ and Zn2+ by bacteria isolated from a zinc mine in Thailand. Ecotox Environ Safe 122:322–330. https://doi.org/10.1016/j.eco env.2015.08.013 Liu H, Carvalhais LC, Schenk PM, Dennis PG (2017) Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci Rep 7:41766. https://doi.org/10.1038/srep41766 Liu X-M, Zhang H (2015) The effects of bacterial volatile emissions on plant abiotic stress tolerance. Front Plant Sci 6:774. https://doi.org/10.3389/fpls.2015.00774 Luo S, Chen L, Chen J, Xiao X, Xu T, Wan Y, Rao C, Liu C, Liu Y, Lai C (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cdhyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138. https://doi.org/10.1016/j.chemosphere.2011.07.053 Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69. https://doi.org/10. 1016/j.jenvman.2015.03.024 Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25. https://doi.org/10.1016/j.jenvman.2016. 02.047 Maela PM, Serepa-Dlamini MH (2019) Current understanding of bacterial endophytes, their diversity, colonization and their roles in promoting plant growth. Appli Microbiol Open Access 5:157. https://doi.org/10.4172/2471-9315.1000157 Maheshwari DK, Dubey RC, Agarwal M, Dheeman S, Aeron A, Bajpai VK (2015) Carrier based formulations of biocoenotic consortia of disease suppressive Pseudomonas aeruginosa KRP1 and Bacillus licheniformis KRB1. Ecol Eng 81:272–277 Maropola MKA, Ramond J-B, Trindade M (2015) Impact of metagenomic DNA extraction procedures on the identifiable endophytic bacterial diversity in Sorghum bicolor (L. Moench). J Microbiol Methods 112:104–117. https://doi.org/10.1016/j.mimet.2015.03.012 Mefteh FB, Chenari Bouket A, Daoud A, Luptakova L, N Alenezi F, Gharsallah N, Belbahri L (2019) Metagenomic insights and genomic analysis of phosphogypsum and its associated plant endophytic microbiomes reveals valuable actors for waste bioremediation. Microorganisms 7(10):382. https://doi.org/10.3390/microorganisms7100382 Mefteh FB, Daoud A, Chenari Bouket A, Alenezi FN, Luptakova L, Rateb ME, Kadri A, Gharsallah N, Belbahri L (2017) Fungal root microbiome from healthy and brittle leaf diseased date palm trees (Phoenix dactylifera L.) reveals a hidden untapped arsenal of antibacterial and broad spectrum antifungal secondary metabolites. Front Microbiol 8:307. https://doi.org/10.3389/fmicb.2017. 00307 Mefteh FB, Daoud A, Chenari Bouket A, Thissera B, Kadri Y, Cherif-Silini H, Eshelli M, Alenezi FN, Vallat A, Oszako T, Kadri A, Ros-García JM, Rateb ME, Gharsallah N, Belbahri L (2018) Date palm trees root-derived endophytes as fungal cell factories for diverse bioactive metabolites. Int J Mol Sci 19(7):E1986. https://doi.org/10.3390/ijms19071986 Mehta CM, Palni U, Franke-Whittle IH, Sharma AK (2014) Compost: its role, mechanism and impact on reducing soil-borne plant diseases. Waste Manag 34:607–622. https://doi.org/10.1016/ j.wasman.2013.11.012

202

H. B. Slama et al.

Mohite B (2013) Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. J Soil Sci Plant Nutr 13:638–649. https://doi.org/ 10.4067/S0718-95162013005000051 Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195. https://doi.org/10.1016/j.tplants.2012.02.001 Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J. http://doi.org/10.1155/2014/250693 Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39. https://doi.org/10.1016/j.envexpbot.2013. 09.014 Nicolas C, Hermosa R, Rubio B, Mukherjee PK, Monte E (2014) Trichoderma genes in plants for stress tolerance-status and prospects. Plant Sci 228:71–78. https://doi.org/10.1016/j.plantsci. 2014.03.005 Nion YA, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ 30(1):1–11. https://doi.org/10.1264/jsme2.ME1 4144 Noumavo PA, Agbodjato NA, Baba-Moussa F, Adjanohoun A, Baba-Moussa L (2016) Plant growth promoting rhizobacteria: beneficial effects for healthy and sustainable agriculture. Afr J Biotechnol 15:1452–1463. https://doi.org/10.5897/AJB2016.15397 O’Brien JA, Benkova E (2013) Cytokinin cross-talking during biotic and abiotic stress responses. Front Plant Sci 4:451. https://doi.org/10.3389/fpls.2013.00451 Paramanantham P, Pattnaik S, Siddhardha B (2019) Natural Products from endophytic fungi: synthesis and applications. In: Advances in endophytic fungal research. Springer, Cham, pp 83–103 Passari AK, Mishra VK, Leo VV, Gupta VK, Singh BP (2016) Phytohormone production endowed with antagonistic potential and plant growth promoting abilities of culturable endophytic bacteria isolated from Clerodendrum colebrookianum Walp. Microbiol Res 193:57–73. https://doi.org/10. 1016/j.micres.2016.09.006 Passari AK, Mishra VK, Singh G, Singh P, Kumar B, Gupta VK, Sarma RK, Saikia R, Singh BP (2017) Insights into the functionality of endophytic actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci Rep 7:11809. https://doi.org/ 10.1038/s41598-018-22947-w Paungfoo-Lonhienne C, Lonhienne TG, Yeoh YK, Webb RI, Lakshmanan P, Chan CX, Lim PE, Ragan MA, Schmidt S, Hugenholtz P (2014) A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microb Biotechnol 7:142–154. https://doi.org/10.1111/ 1751-7915.12105 Peng W, Ming Q, Zhai X, Zhang Q, Rahman K, Wu S, Qin L, Han T (2019) Polysaccharide fraction extracted from endophytic fungus Trichoderma atroviride D16 Has an influence on the proteomics profile of the Salvia miltiorrhiza hairy roots. Biomolecules 9:415. https://doi.org/10. 3390/biom9090415 Pereira SIA, Castro PML (2014) Diversity and characterization of culturable bacterial endophytes from Zea mays and their potential as plant growth-promoting agents in metal-degraded soils. Environ Sci Pollut Res 21:14110–14123. https://doi.org/10.1007/s11356-014-3309-6 Perotti R (1926) On the limits of biological enquiry in soil science. Proc Int Soc Soil Sci 2:146–161 Pettersson M, Baath E (2004) Effects of the properties of the bacterial community on pH adaptation during recolonisation of a humus soil. Soil Biol Biochem 36:1383–1388. https://doi.org/10.1016/ j.soilbio.2004.02.028 Quispel A (1992) A search for signals in endophytic microorganisms. In: Verma DPS (ed) Molecular signals in plant-microbe communications. CRC Press, Boca Raton, FL, pp 471–490 Ramamoorthy V, Viswanathan R, Raguchander T, Prakasam V, Samiyappan R (2001) Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protect 20:1–11. https://doi.org/10.1016/S0261-2194(00)00056-9

8 Biotechnology and Bioinformatics of Endophytes …

203

Ramette A, Frapolli M, Défago G, Moënne-Loccoz Y (2003) Phylogeny of HCN synthase-encoding hcnBC genes in biocontrol fluorescent pseudomonads and its relationship with host plant species and HCN synthesis ability. MPMI 16:525–535. https://doi.org/10.1094/MPMI.2003.16.6.525 Rasmussen S, Lane GA, Mace W, Parsons AJ, Fraser K, Xue H (2011) The use of genomics and metabolomics methods to quantify fungal endosymbionts and alkaloids in grasses. In: Plant metabolomics. Springer, Cham, pp 213–226 Rekik I, Chaabane Z, Missaoui A, Chenari Bouket A, Luptakova L, Elleuch E, Belbahri L (2017) Effects of untreated and treated wastewater at the morphological, physiological and biochemical levels on seed germination and development of sorghum (Sorghum bicolor L.), alfalfa (Medicago sativa L.) and fescue (Festuca arundinacea Schreb.). J Hazard Mat 326:165–176. https://doi.org/ 10.1016/j.jhazmat.2016.12.033 Ritika K, Mohinder KG (2016) Cytokinins production by fluorescent Pseudomonas isolated from rhizospheric soils of Malus and Pyrus. Afr J Microbiol Res 10(32):1274–1279. https://doi.org/ 10.5897/AJMR2016.8211 Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. https://doi.org/10.3389/fpls.2016.00571 Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448. https://doi.org/10.1016/j.tpl ants.2006.07.004 Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767. https://doi.org/10.1093/aob/mct048 Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.mic res.2015.11.008 Sarethy IP, Srivastava N, Pan S (2019) Endophytes: the unmapped repository for natural products. In: Natural bio-active compounds. Springer, Singapore, pp 41–70 Sathish L, Pavithra N, Ananda K (2012) Antimicrobial activity and biodegrading enzymes of endophytic fungi from eucalyptus. Int J Pharmaceut Sci Res 3:2574 Schulz B (2006) What are endophytes? In: Schulz BJE, Boyle CIC, Sieber TN (eds) Microbial root endophytes. Springer-Verlag, Berlin, pp 1–13 Schulz B, Boyle C (2006) What are endophytes? In: Microbial root endophytes. Springer, New York, pp 1–13 Selim KA, Nagia MM, Ghwas DEE (2017) Endophytic fungi are multifunctional biosynthesizers: ecological role and chemical diversity. In: Endophytic fungi: diversity, characterization and biocontrol. Nova Publishers, New York, The United States, 39–91 pp Sengupta S, Ganguli S, Singh PK (2017) Metagenome analysis of the root endophytic microbial community of Indian rice (O. sativa L.). Genom Data 12:41–43 Sharma M, Kansal R, Singh D (2018) Endophytic microorganisms: their role in plant growth and crop improvement. Crop improvement through microbial biotechnology. Elsevier, India, pp 391–413 Sharma S, Kaur ASM (2018) Extraction and evaluation of gibberellic acid from Pseudomonas sp.: plant growth promoting rhizobacteria. J Pharmacogn Phytochem 7:2790–2795 Sheoran N, Valiya Nadakkakath A, Munjal V, Kundu A, Subaharan K, Venugopal V, Rajamma S, Eapen SJ, Kumar A (2015) Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol Res 173:66–78. https://doi.org/10.1016/j.micres.2015.02.001 Shin M-N, Shim J, You Y, Myung H, Bang K-S, Cho M, Kamala-Kannan S, Oh B-T (2012) Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. J Hazard Mat 199:314–320 Shukla ST, Habbu PV, Kulkarni VH, Jagadish KS, Pandey AR, Sutariya VN (2014) Endophytic microbes: a novel source for biologically/pharmacologically active secondary metabolites. Asian J Pharmacol Toxicol 2:1–6

204

H. B. Slama et al.

Sim CSF, Chen SH, Ting ASY (2019) Endophytes: emerging tools for the bioremediation of pollutants. In: Bharagava RN, Chowdhary P (eds) Emerging and eco-friendly approaches for waste management. Springer, Singapore, pp 189–217 Sim CSF, Cheow YL, Ng SL, Ting ASY (2018) Discovering metal-tolerant endophytic fungi from the phytoremediator plant Phragmites. Water Air Soil Pollut 229:68 Singh R, Dubey AK (2015) Endophytic actinomycetes as emerging source for therapeutic compounds. Indo Global J Pharm Sci 5:106–116 Slama HB, Cherif Silini H, Ali CB, Qader M, Silini A, Yahiaoui B, Alenezi FN, Luptakova L, Triki M-A, Vallat A (2018) Screening for Fusarium antagonistic bacteria from contrasting niches designated the endophyte Bacillus halotolerans as plant warden against Fusarium. Front Microbiol 9:3236. https://doi.org/10.3389/fmicb.2018.03236 Slama HB, Triki MA, Chenari Bouket A, Ben Mefteh F, Alenezi FN, Luptakova L, Cherif-Silini H, Vallat A, Oszako T, Gharsallah N (2019) Screening of the high-rhizosphere competent Limoniastrum monopetalum’culturable endophyte microbiota allows the recovery of multifaceted and versatile biocontrol Agents. Microorganisms 7(8):249. https://doi.org/10.3390/microorganisms7 080249 Srivastava N, Gupta B, Gupta S, Danquah MK, Sarethy IP (2019) Analyzing functional microbial diversity: an overview of techniques. In: Microbial diversity in the genomic era. Elsevier, London, pp 79–102 Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160. https://doi.org/10. 1128/JB.00345-12 Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502 Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448– 459 Thakur P, Singh I (2018) Biocontrol of soilborne root pathogens: an overview. In: Giri B, Prasad R, Varma A (eds) Root biology. Springer International Publishing, Cham, pp 181–220 Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2007) Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 22:120–126 Ting ASY, Lee MVJ, Chow YY, Cheong SL (2016) Novel exploration of endophytic Diaporthe sp. for the biosorption and biodegradation of triphenylmethane dyes. Water Air Soil Pollut 227:109 Tsai HH, Schmidt W (2017) Mobilization of iron by plant-borne coumarins. Trends Plant Sci 22:538–548. https://doi.org/10.1016/j.tplants.2017.03.008 Ulloa-Ogaz AL, Muñoz-Castellanos LN, Nevárez-Moorillón GV (2015) Biocontrol of phytopathogens: antibiotic production as mechanism of control. In: Méndez-Vilas A (ed) The battle against microbial pathogens: basic science, Technological advances and educational programs, 1st edn. Formatex, Chihuahua, pp 305–309 Uzma F, Mohan CD, Hashem A, Konappa NM, Rangappa S, Kamath PV, Singh BP, Mudili V, Gupta VK, Siddaiah CN (2018) Endophytic fungi—alternative sources of cytotoxic compounds: a review. Front Pharmacol 9:309. https://doi.org/10.3389/fphar.2018.00309 Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14 Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Molecules 21:573. https://doi. org/10.3390/molecules21050573 Venieraki A, Dimou M, Katinakis P (2017) Endophytic fungi residing in medicinal plants have the ability to produce the same or similar pharmacologically active secondary metabolites as their hosts. Hellenic Plant Protect J 10:51–66 Verma P, Yadav AN, Kazy SK, Saxena AK, Suman A (2014) Evaluating the diversity and phylogeny of plant growth promoting bacteria associated with wheat (Triticum aestivum) growing in central zone of India. Int J Curr Microbiol Appl Sci 3:432–447

8 Biotechnology and Bioinformatics of Endophytes …

205

Vimal SR, Singh JS, Arora NK, Singh S (2017) Soil-plant-microbe interactions in stressed agriculture management: a review. Pedosphere 27:177–192. https://doi.org/10.1016/S1002-0160(17)603 09-6 von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Ann Rev Phytopathol 41:455–482. https://doi.org/10.1146/annurev.phyto.41.052002.095652 Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965 Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598. https://doi.org/10.1016/j.tibtech.2009.07.006 White JF, Torres MS, Verma SK, Elmore MT, Kowalski KP, Kingsley KL (2019) Evidence for widespread microbivory of endophytic bacteria in roots of vascular plants through oxidative degradation in root cell periplasmic spaces. In: PGPR amelioration in sustainable agriculture. Elsevier, Cambridge, pp 167–193 Yu H, Zhang L, Li L, Zheng C, Guo L, Li W, Sun P, Qin L (2010) Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiol Res 165:437–449 Zahir ZA, Zafar-ul-Hye M, Sajjad S, Naveed M (2011) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for coinoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil. Biol Fertil Soils 47:457–465. https://doi.org/ 10.1007/s00374-011-0551-7 Zhou Y, Tang L, Zeng G, Chen J, Cai Y, Zhang Y, Yang G, Liu Y, Zhang C, Tang W (2014) Mesoporous carbon nitride-based biosensor for highly sensitive and selective analysis of phenol and catechol in compost bioremediation. Biosens Bioelectron 61:519–525. https://doi.org/10. 1016/j.bios.2014.05.063 Zhu L-J, Guan D-X, Luo J, Rathinasabapathi B, Ma LQ (2014) Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 113:9–16. https://doi.org/10.1016/j.chemosphere.2014.03.081

Chapter 9

Phosphate Solubilization by Endophytes from the Tropical Plants Paulo Teixeira Lacava, Paula Cristiane Machado, and Paulo Henrique Marques de Andrade

Abstract Currently, agriculture depends heavily on a variety of agrochemicals, such as mineral fertilizers and pesticides, that often have adverse effects on human health and environmental ecosystems. Furthermore, the indiscriminate application of pesticides has severe effects on soil ecology that may lead to alterations in plant and soil microbiomes. Modern agricultural biotechnology has shown that microbial inoculants can be used to enhance plant growth and can thereby reduce the use of agrochemicals. In this context, the utilization of endophytic microorganisms for agricultural purposes has increased recently, especially their use for plant growth promotion. Endophytes are microorganisms that live in plant tissues without causing apparent disease in the host plant. Endophytic microorganisms promote plant growth in three major ways: they synthesize particular compounds that are useful for the plants, they facilitate the uptake of certain nutrients from the soil, and they control or prevent diseases. Growth promotion mediated by endophytes occurs via several mechanisms: the production of vital enzymes; the production of hormones such as auxin (indoleacetic acid [IAA]); the symbiotic fixation of nitrogen; the production of siderophores, chitinases, or antibiotics for protection from phytopathogens; and the solubilization and mineralization of nutrients, particularly insoluble mineral phosphates. Endophytic microorganisms can be used to improve nutrient utilization because they solubilize phosphate, making it available for absorption by plants. Among these microorganisms are phosphate-solubilizing bacteria and fungi that P. T. Lacava (B) · P. H. M. de Andrade Laboratory of Microbiology and Biomolecules – LaMiB, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, Via Washington Luís km 235, PO BOX 676, São Carlos, SP 13565-905, Brazil e-mail: [email protected] P. T. Lacava · P. C. Machado Biotechnology Graduation Program – PPGBiotec, Center of Exact Sciences and Technology, Federal University of São Carlos, Via Washington Luís km 235, São Carlos, SP 13565-905, Brazil P. T. Lacava · P. H. M. de Andrade Evolutionary Genetics and Molecular Biology Graduation Program – PPGGEv, Center for Biological and Health Sciences, Federal University of São Carlos, Via Washington Luís km 235, São Carlos, SP 13565-905, Brazil © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_9

207

208

P. T. Lacava et al.

participate in the phosphorus cycle and facilitate the conversion of insoluble P to soluble forms via the secretion of organic acids and phosphatases. In this way, they make P available to the plant. Over the past two decades, much information on the role of endophytes in nature has been collected. Their ability to colonize internal host tissues has made endophytes valuable as a tool for improving crop performance. Most studies on endophytes have been carried out using hosts from temperate countries, but data from tropical regions remain scarce. Tropical plants host a great diversity of endophytic microorganisms, many of which are not yet classified and possibly belong to new genera and species. In this chapter, we focus on examples of endophytic microorganisms, especially those that have the potential to promote plant growth through phosphate solubilization. Keywords Biofertilizers · Endophytic microbes · Phosphate solubilization · Plant growth promotion · Sustainable agriculture

9.1 Introduction The significance of endophytic microorganisms for agricultural purposes has increased recently, especially their use for pest and disease control (biological control) and plant growth promotion (Vyas and Bansal 2018; Maheshwari and Annapurna 2017; Gautam and Avasthi 2019). Endophytes promote plant growth in many ways, such as by producing enzymes and hormones and acting against phytopathogens via the production of siderophores, chitinolytic enzymes, or antibiotics; and solubilizing nutrients such as phosphates (Azevedo and Quecine 2019). A large number of macronutrients and other minerals are required for the balanced growth of the plants. One of them is Phosphorus. Phosphorus which promotes root development, tillering, and early flowering and has a role in other functions such as metabolic activities, particularly protein synthesis (Tanwar and Shaktawat 2003). Phosphorus in soil is present in both inorganic and organic insoluble forms. Phosphate solubilization by endophytes is an interesting component of plant growth promotion because endophytic bacteria are compatible with host plants and can colonize the tissues of host plants without being identified as phytopathogens (Rosenblueth and Martínez-Romero 2006). The interactions between endophytes and plants can promote plant health and play a significant role in low-input sustainable agriculture for both food and nonfood crops (Rai et al. 2014; Golinska et al. 2015). In the past two decades, large number of publications have appeared on the role of endophytic microorganisms in nature (Azevedo and Quecine 2019). The ability of endophytes to colonize internal host plant tissues has made them valuable as a tool for improving crop performance (Araújo et al. 2008). The exploration of endophytes in unstudied hosts, such as tropical plants, is important for assessing the potential of these microorganisms in different application areas and for identifying natural compounds that could be used in agriculture

9 Phosphate Solubilization by Endophytes from the Tropical Plants

209

and biotechnology (Golinska et al. 2015). Still a large number of plants have yet to be investigated.

9.2 Phosphorus Solubilization by Microorganisms Phosphorus (P) is one of the major growth-limiting macronutrients required for proper plant growth, particularly in tropical areas (Santana et al. 2016). Based on the availability of P to plants, the different forms of P can be categorized as soluble P and insoluble P. The soluble form is easily available for uptake by plants. In contrast, an insoluble form is very stable in soil and persists in an unavailable form (Ahemad et al. 2009). Inspite of its abundance in soil and therefore cannot support the plant growth due to its unavailability. Moreover, almost 75% of phosphorus applied as fertilizer forms complexes with soil and becomes unavailable for the plants (Ezawa et al. 2002). More details about the identification of the major processes of the soil P cycle that affect soil solution P concentrations as dissolution–precipitation, sorption desorption, and mineralization–immobilization (biologically mediated conversions of P between inorganic and organic forms) are presented in a review by Sims and Pierzynski (2005) and other publications. Microorganisms play an important role in all three major components of the soil P cycle such as (1) release of complexing or mineral dissolving compounds, e.g., organic acid anions, siderophores, protons, hydroxyl ions, CO2 , (2) liberation of extracellular enzymes (biochemical P mineralization), and (3) the release of P during substrate degradation (biological P mineralization) (Sharma et al 2013). Some bacterial species have mineralization and solubilization potential for organic and inorganic phosphorus, respectively (Hilda and Fraga 2000; Khiari and Parent 2005). Phosphorus solubilizing activity is determined by the ability of microbes to release metabolites such as organic acids, which through their hydroxyl and carboxyl groups chelate the cation bound to phosphate, the latter being converted to soluble forms (Sagoe et al. 1998).

9.3 Endophytic Microorganisms: A Way to Reduce the Application of Agrochemicals in Agrobiology Systems Agriculture is anti-ecological by nature, and the large-scale use of chemical fertilizers, insecticides, fungicides, herbicides, and antibiotics has led to profound biological changes. The increasing use of fertilizers and highly productive systems has also created environmental problems such as the deterioration of soil quality, surface water, and groundwater, as well as air pollution, reduced biodiversity, and suppressed ecosystem function (Vance 2001). Additionally, chemical pesticides and fertilizers

210

P. T. Lacava et al.

can cause significant damage to ecosystems through the processes of bioaccumulation and biomagnification due to their synthetic nature (Sarbadhikary and Mandal 2018). Consequently, interest in the development of new strategies to achieve more sustainable agricultural practices has increased significantly in recent years (Azevedo and Quecine 2019). In this context, biofertilizers are an interesting alternative to the use of agrochemicals, as biofertilizers may be a safe substitute for agrochemicals that would greatly minimize ecological disturbance from agriculture. Biofertilizers are low-cost, eco-friendly tools, and their persistent use increases soil health and fertility (Ngamau et al. 2014). In this context, there is renewed scientific and commercial interest in the use of endophytic microorganisms as biofertilizers because of their potential to improve plant quality and growth and their close association with internal tissues of the host plant (Schulz et al. 1998, 1999; Ngamau et al. 2014). Biofertilizers can improve crop health by fixing nitrogen (Islam et al. 2013), solubilizing phosphate (Ghosh et al. 2016), or promoting plant growth by producing plant growth-promoting factors such as auxin (IAA) and gibberellins (Kang et al. 2014; Reetha et al. 2014). Plant growth-promoting rhizobacteria (Vessey 2003) and vesicular-arbuscular mycorrhizae (Abbasi et al. 2015) are the microorganisms that are used most often as biofertilizers. Recently, many researchers have also reported the use of endophytic microorganisms in agricultural fields for crop improvement (Ngamau et al. 2014). The term endophyte is applied to microorganisms that live within plant tissues for all or part of their life cycles and cause no apparent infections or symptoms of a disease (Strobel et al. 2004). Hallmann et al. (1997) described endophytes as organisms that can be isolated from surface-sterilized plant parts or extracted from inner tissues and that cause no damage to the host plant. Also, Azevedo and Araújo (2007) suggested that endophytes are all microorganisms, whether culturable or not, that inhabit the interior of plant tissues, cause no harm to the host, and do not develop external structures. Endophytes have an intimate interaction with plants and are capable of promoting plant growth. The use of these microorganisms at certain stages of agricultural production can lead to a significant increase in productivity or a reduction in inputs such as nitrogen and phosphate fertilizers (Malboobi et al. 2009; Rukshana-Begum and Tamilselvi 2016). The plant growth-promoting effects of endophytes include increased plant height and biomass in shoots, stems, and roots; formation of leaf and root hairs; lignification of the xylem vessels; and increased crop yield, as the ability of endophytes to stimulate plant growth has been attributed to mechanisms such as phytohormone production and phosphate solubilization (Ahmad et al. 2008). Some soil microorganisms solubilize the unavailable forms of inorganic P in the soil (Son et al. 2006; Chai et al. 2011), and recent studies have confirmed that endophytic microorganisms also possess this capacity (Vitorino et al 2012). After nitrogen, phosphorus (P) is the second most limiting nutrient for plant development. It is only taken up in monobasic or dibasic soluble forms (Zaidi et al. 2006). Phosphorus constitutes 0.2% of plant dry weight and is a structural component of macromolecules such as nucleic acids, phospholipids, and adenosine triphosphate (ATP) (Martins 2004). Phosphorus is an essential element for the establishment and

9 Phosphate Solubilization by Endophytes from the Tropical Plants

211

development of plants because it improves the entire root system, which consequently improves the shoot (Raven et al. 2001). However, phosphates applied to agricultural soils are rapidly immobilized and rendered inaccessible to plants. Due to this rapid immobilization, many agricultural soils have large reservoirs of phosphates in inaccessible forms (Rodríguez and Fraga 1999; Rodríguez et al. 2006). In this scenario, the ability of microorganisms to solubilize phosphorus is determined by their ability to release metabolites such as organic acids, which chelate the cation bound to the phosphate through their hydroxyl and carboxyl groups, converting the inaccessible phosphate to a soluble form (van der Heijden et al. 2008). Even in a phosphorus-rich soil, only a small fraction of the phosphorous is available to plants because most of it is found in insoluble forms, and plants are not able to absorb it (Gyaneshwar et al. 2002). Some kinds of the microorganism may be used to improve plant nutrient utilization because they solubilize phosphate, making it available for absorption by the plant. Among these microorganisms are phosphate-solubilizing bacteria and fungi that participate in the phosphorus cycle and facilitate the conversion of insoluble phosphorus to soluble forms via the secretion of organic acids and phosphatases, thus making phosphorus available to the plant (Oliveira et al. 2003). Besides, phosphatesolubilizing microorganisms could play an important role in supplying phosphate to plants in an eco-friendly and sustainable way (Oliveira et al. 2009; Gomes et al. 2014). Phosphate-solubilizing microorganisms are found in soil, especially in rhizospheric microbial populations, and their numbers vary depending on the type of soil (Mohammadi 2012). These microorganisms release low molecular-weight organic acids that solubilize mineral phosphates and reduce the pH of the soil (Pérez et al. 2007; Gomes et al. 2014). Additionally, they have been widely tested as biofertilizers and inoculants to increase crop yield through phosphate solubilization (Karpagam and Nagalakshmi 2014; Baliah et al. 2016; Gurikar et al. 2016). Endophytes represent a group of microorganisms that can colonize plants without inducing the host defense pathway (Azevedo et al. 2000). Thus, the distinction between free-living soil microorganisms, the rhizosphere population, and the symbionts of a host plant may represent a true continuum, with microbes able to move between the soil, the rhizosphere, and the inside of the plant as endophytes (Farrar et al. 2014; de Abreu et al 2017). In this case, several species of Bacillus and Pseudomonas use nutrient niches in the rhizosphere and change from a freeliving condition to an endophytic state (Rosenblueth and Martínez-Romero 2006; Gaiero et al. 2013). In this way, endophytes can be transported from the seeds into the roots and tissues, reducing the need for continuous inoculation (Johnston-Monje and Raizada 2011). However, the ability of endophytic microorganisms to solubilize phosphates in tropical and subtropical soils has not been sufficiently studied (de Abreu et al. 2017). Endophytes, as phosphate solubilizers, are more competitive than free-living or facultative microorganisms inside the host plant since the endophyte– plant interaction is the result of an evolutionary process that is controlled by genes of both organisms (Rosenblueth and Martínez-Romero 2006). Endophytes can increase the availability of P for the plants by solubilizing precipitated phosphates, using mechanisms like acidification, chelation, ion exchange, and

212

P. T. Lacava et al.

production of organic acids (Nautiyal et al. 2000). They can also increase P availability in the soil by secreting acid phosphatase that can mineralize organic phosphorus (van der Heijden et al. 2008). Moreover, these microorganisms can prevent phosphate adsorption and fixation under phosphate-limiting conditions by assimilating solubilized P (Khan and Joergensen 2009). In a recent review presented by Afzal et al. (2019), they discussed the role of plant beneficial endophytic bacteria with special reference to phosphate solubilization as commonly found in PGPR. For instance, around 59–100% of endophytic populations from cactus, strawberry, sunflower, soybean, and other legumes proved to be mineral phosphate solubilizers (Dias et al. 2009a; Forchetti et al. 2007; Kuklinsky-Sobral et al. 2004; Palaniappan et al. 2010; Puente et al. 2009).

9.4 Endophytic Bacteria from Tropical Plants of Economic Importance: Phosphorus Solubilization Potential 9.4.1 Endophytic Bacteria from Coffea arabica Similar to the free living bacteria and rhizobia, the endophytes generally influence the plant for their growth and development. These bacteria have potential to exhibit their effects in order to benefit the plants in a befitting manner. Some of them are given below. Coffee (Coffea arabica L.) is a perennial plant widely cultivated in many tropical countries. It belongs to the family Rubiaceae, which has approximately 500 genera and more than 6,000 species. It is the most important genus in economic terms, mainly due to coffee production used as beverage (Mendes et al. 1995). Due to its continental dimensions, Brazil has a variety of climatic conditions, reliefs, altitudes, and latitudes. Such bio-geography allows for the production of many types and qualities of coffee, including specialty coffees and organic coffee, whose consumption has increased as society has begun to question the sustainability of the current conventional agricultural model (Brasil 2015). The microbiota associated with coffee plants may play a critical role in coffee quality. However, the microbial diversity and agricultural potential associated with coffee plants are still poorly characterized. There are some examples of studies of microorganisms associated with coffee, such as Muleta et al. (2013), who reported phosphate-solubilizing rhizobacteria associated with Coffea arabica L. in the natural coffee forests of southwestern Ethiopia. In this study, a total of 395 rhizobacterial isolates tested for P solubilization formed visible dissolution haloes on the Pikovskaya’s agar (PA) culture. According to these authors, two Erwinia species and a Pseudomonas chlororaphis produced the highest solubilization index, and the production of organic acids by these coffee-associated strains could be considered the major mechanism involved in the solubilization of insoluble hydroxyapatite/tricalcium. Earlier, Musson (1994) suggested that endophytes can act as efficient growth promoters, probably in the same manner as rhizobacteria, by producing

9 Phosphate Solubilization by Endophytes from the Tropical Plants

213

hormones and other growth factors. Additionally, bio-priming and seed coating appeared as an efficient method in growth-promotion because endophytes as organisms can be adhered onto the seed surface (Rosenblueth and Martínez-Romero 2006; Ryan et al. 2008). The endophytic microbiota plays a role not only in supplying plants with the basic nutrients that are indispensable for their growth but also in the mechanisms of adaptation to various environmental stresses, important in terms of crop yields (Ku´zniar et al. 2019). The rational method of plant growth promotion by endophytes is the improvement of plant nutrient acquisition. However, the mechanisms for direct nutrient transfer from endophytic bacteria to plants have been elusive (Pandey et al. 2018; Roley et al. 2018). In some cases, endophytes have been shown to increase the solubilization of bound phosphates in the rhizosphere and thus have been hypothesized to function by increasing the plant phosphate supply in the rhizosphere for its uptake by plants(Shehata et al. 2017). In a recent publication, White et al. (2018) proposed that many host plants acquire some nutrients directly from symbiotic microbes by a process called the ‘rhizophagy cycle’. In this cycle, symbiotic microbes alternate between an endophytic phase and a free-living soil phase. The authors hypothesize that microbes acquire soil nutrients in the free-living soil phase and that those nutrients are extracted from microbes oxidatively in the intracellular/endophytic phase. In this review, White et al. (2018) discuss the proposed mechanisms that plants employ to manipulate symbiotic microbes to transport nutrients from the soil into root cell periplasmic spaces. Oliveira et al (2013) investigated endophytic diversity in Coffea arabica L. cherries from southeastern Brazil by using culture-independent approaches to identify the associated microorganisms with the goal of better understanding their ecology and potential role in determining coffee quality. In our research group, we isolated endophytic bacteria from coffee cherries (Fig. 9.1), and identification by 16S rRNA genes and fatty acid methyl esters (FAMEs) revealed 3 major genera: Bacillus agaradhaerens, Paenibacillus sp.; and Pantoea agglomerans. According to Oliveira et al. (2013), the bacterial sequences showing high similarity with cultured and uncultured

Fig. 9.1 Endophytic bacteria isolated from Coffea arabica L. cherries. Details of endophytic growth indicated by black arrows (Photo credit: Corresponding Author)

214

P. T. Lacava et al.

bacteria belonged to the Betaproteobacteria, Gammaproteobacteria, and Firmicutes phyla. Phylogenetic analyses of cloned sequences from Firmicutes revealed that most sequences fell into 3 major genera: Bacillus, Staphylococcus, and Paenibacillus. In this case, we found similar results to those reported by Oliveira et al. (2013) regarding the diversity of endophytic bacteria isolated from C. arabica L. cherries. Silva et al. (2012) reported the potential of endophytic bacteria isolated from healthy Coffea arabica L. and Coffea robusta L. from Pedreira, Mococa, and Pindorama counties, State of São Paulo, Brazil. Previously, promising growthpromoter endophytic strains were evaluated qualitatively in vitro for the production of phosphatase, indole acetic acid (IAA), siderophores, cytokinins, and gibberellins (CYT/GIB). A total of two hundred seventeen strains were evaluated for their potential to promote the growth of coffee seedlings in vivo. According to the authors (Silva et al. 2012), the growth-promoting indexes of 119 bacterial strains were higher than those of the control. Additionally, the Scott–Knott cluster test indicated that the indexes of six bacterial strains, 85G (Escherichia fergusonii), 161G, 163G, 160G, 150G (Acinetobacter calcoaceticus), and 109G (Salmonella enterica), differed significantly from that of the control. However, of these six strains showed with the best performance in vivo, only two (161G and 160G) produced phosphatase as a positive plant-growth promotion parameter when tested in vitro. In our research, we have investigated the ability of endophytes from different host plants to promote plant growth, including phosphate solubilization. In this context, Andrade (2019) performed a study that included the isolation, biochemical characterization, identification, and analysis of the genetic diversity of the endophytic bacterial community associated with C. arabica L. from conventional and organic cultivation sources. The results demonstrated that 342 endophytic bacterial isolates were evaluated for in vitro growth factors, where, about 64.33% isolates were solubilized inorganic phosphate. The identification of endophytic strains was performed by bacterial cell protein analysis by matrix-assisted laser desorption/ionization-time-offlight (MALDI-TOF) and by partial sequencing of the 16S rDNA gene. The genera identified were Arthrobacter, Bacillus, Cronobacter, Enterobacter, Erwinia, Klebsiella, Kosakonia, Kurthia, Lysinibacillus, Microbacterium, Pantoea, Pseudomonas, and Rhizobium. In this case study (Andrade 2019), the endophytic strains with the best performance for in vitro growth factors, including phosphate solubilization, were selected for inoculation in coffee seedlings. Ten endophytic strains were selected based on the biochemical characterization previously performed in vitro about the potential for plant growth promotion. The treatments consisted of a control (C) with 8 replicates where the seedlings were inoculated only with PBS buffer and 10 treatments (T1 to T10) with 8 replicates which consisted of weekly inoculation of the seedlings with a bacterial suspension of CRM 162 - Erwinia bilingiae (T1); CRM 202 - Kosakonia cowanii (T2); CRA 241 Enterobacter tabaci (T3); CRA 250 Enterobacter tabaci (T4); CRA 298 - Pantoea brenneri (T5) from conventionally grown coffee; OFR 175 - Lysinibacillus mangiferihumi (T6); OFR 176-Lysinibacillus mangiferihumi (T7); OFR 164 - Klebsiella pneumoniae (T8); OFO 340 - Enterobacter bugandensis (T9); or ORM 326 - Klebsiella michiganensis (T10). A total of 180 days after the first

9 Phosphate Solubilization by Endophytes from the Tropical Plants

215

Fig. 9.2 Average root system length (RL) in millimeters (mm) of 8 plants per treatment (T1 to T10), measured 180 days after the first inoculation of bacteria with the potential for plant growth promotion

inoculation, the following variables were evaluated: aerial height (AH), root length (RL), stem diameter (SD), aerial dry weight (ADW), and dry weight of the root system (DWRS). All treatments of plants inoculated, except for the T3 treatment, all caused a reduction in AH corresponding to the plants of a control group. For RL, all treatments differed significantly from the control, showing an increase in root system length of 77.76%, on an average. For the variables SD, ADW, and DWRS, and the analysis of macro- and micronutrients in the leaf tissue, it was possible to observe that none of the treatments differed significantly from the control. All statistical analyses were performed considering p ≤ 0.05. A principal component analysis showed that RL explained 99% of the total variation in the observed morphological characteristics; that is, the tested bacterial strains were able to promote the growth of the coffee seedlings (Fig. 9.2).

9.4.2 Endophytic Bacteria from Jatropha curcas Jatropha (Jatropha curcas L.), which belongs to the Euphorbiaceae family, is a plant that is genetically close to the castor plant (Ricinus communis L.); it originates from Central America and is currently distributed in all tropical regions of the globe (Kumar and Tewari 2015; Kumar et al. 2016). Jatropha cultivation has received more attention in the last few decades due to its role in biodiesel production. Jatropha is also recommended for cultivation for soil health improvement, climate change mitigation, carbon sequestration, and socio-economic development (Islam et al. 2014). The yield of jatropha varies from 0.2 kg to >2 kg seeds from a single plant or 2–12 t ha−1 (Tikkoo et al. 2013; Singh et al. 2014). In Brazil, jatropha has received special attention as an alternative supply of vegetable oil as a raw material for biodiesel manufacturing due to the biotechnological potential of its seeds (Laviola et al. 2011; 2015). Several studies on climatic adaptation and productivity have been developed on the genetic variability of jatropha (Reddy et al. 2008; Behera et al. 2010; Laviola et al. 2010;

216

P. T. Lacava et al.

2012; Edrisi et al. 2015), but only a few studies in Brazil have focused on the analysis of the microbial community associated with this species (Moniruzzaman et al. 2016). Jatropha can survive with limited nutrients and under harsh environmental conditions. Planting jatropha is also recommended for pest control, bioremediation, and soil reclamation. Jatropha exhibits drought tolerance, rapid growth, easy propagation, and adaptation to a wide range of environmental stress conditions. These features make it the most popular second-generation biofuel resource (Abhilash et al. 2011). It is not clear how jatropha adapts to extreme conditions. However, Mohanty et al. (2017) hypothesize that its ability to adapt to environmental stresses could be due to its endophytes (Qin et al. 2012; Madhaiyan et al. 2013). Our research group reported the characterization of seventy-two endophytic bacteria associated with J. curcas plants that had the potential to promote plant growth. Of the tested isolates, 43% solubilized inorganic phosphate. These endophytic strains were identified by partial sequencing of the 16S rDNA gene, and the most common genera were Bacillus, Citrobacter, Curtobacterium, Enterococcus, Klebsiella, Microbacterium, Promicromonosporaceae, Sanguibacter, and Serratia (Machado 2015). Among the endophytic genera identified and acted as potential phosphate solubilizers, Bacillus, Citrobacter, Curtobacterium, Klebsiella, and Serratia showed a high phosphate solubilization index. Bacillus spp. exist as endophytes that help the host plant in different ways, one of which is supplying soluble phosphorus by solubilizing phosphorous (Kang et al. 2014; Pérez-García et al. 2011). Andrade (2012) reported six different species of Bacillus sp. that were capable of solubilizing calcium phosphate, with solubilization indexes varying from 0.42 to 2.28 cm. Dias et al. (2009b) analyzed endophytes isolated from strawberry, mainly Bacillus subtilis and B. megaterium, both of which were able to solubilize phosphate. In vitro phosphate solubilization activity has also been documented in Citrobacter sp. strains; this genus belongs to the Enterobacteriaceae family (Kämpfer 2003). In studies conducted by Reginatto (2008), a strain of Citrobacter werkmanni with the ability to solubilize phosphate was endophytically isolated from Vriesea friburgensis. Recently, Machado (2019) reported on the inoculation in corn seeds of eight endophytic bacterial strains consisted of a control (C1) containing only TSB culture medium and the application of bacterial suspensions of EPM-2 Serratia sp. strain (T1), EPM-4 Klebsiella sp. strain (T2), EPM-34 Curtobacterium sp. strain (T3), EPM-41A Bacillus sp. strain (T4), EPM-54 Bacillus sp. strain (T5), EPM-63 Klebsiella sp. strain (T6), EPM-63B Citrobacter sp. strain (T7) and EPM-92 Bacillus sp. strain (T8). Need-based irrigation was carried out, the plants were grown in a greenhouse, and Hoagland and Arnon (1950) nutrient solution was added to the plants after 30 and 60 days of the experiment. At 30 and 60 days after sowing, the plant vegetative parameters such as: shoot height (APA), shoot diameter (DM), shoot dry weight (PSPA), and dry weight of the root system were examined. In the evaluations performed at 30 and 60 days, it was observed that for the variable APA, none of the treatments differed significantly from each other; however, the control presented a significant difference in stem diameter from the other treatments. The DM value of the control treatment was greater than those of the other treatments, and at the 60-day

9 Phosphate Solubilization by Endophytes from the Tropical Plants

217

evaluation, the dry weight of the aerial part (PSPA) and the dry weight of the root system (PSSR), in the control treatment were higher than those in the other treatments. Among the treatments inoculated with endophytic strains, the T1 treatment (EPM2- Serratia marcescens) exhibited significantly higher values for all growth parameters in comparison to other treatments (Unpublished data). Recently, Mohanty et al. (2017 characterized the endophytic bacteria of J. curcas and evaluated their plant growth-promoting effect on maize (Zea mays L.). Fifteen isolates were sequenced by their 16S rRNA genes and characterized based on their carbon source utilization and plant growth-promoting activities. The main genera found were Brevibacillus, Paenibacillus, Rhizobium, and Sphingomonas. These strains preferred to grow on methanol, ethanol, glucose, fructose, sucrose, and gelatin and these strains exhibited catalase, nitrate reductase, ACC deaminase, and phosphatase activities. All isolates were positive for phosphate and IAA production. Inoculation of the endophytic strains on maize seeds significantly increased the shoot and root length of seedlings compared with those of noninoculated seedlings. Potassium solubilization is important for K-assimilation. The phosphatase activity of endophytic bacteria and its relationship to plant growth promotion is interesting. The authors presumed P-mineralization in the rhizosphere by the enzymatic reaction carried by root-tissue exudates containing phosphatases, was also postulated.

9.4.3 Plant Growth-Promoting Potential of Phosphate Solubilization by Endophytic Bacteria Isolated from Tropical Mangrove Forests Mangroves are typical tropical ecosystems situated between the land and the sea. These biological communities are frequently found in tropical and subtropical areas and occupy approximately 18.1 million hectares of the planet. These ecosystems demand high nutrient availability at the start of the trophic chain, which confers high importance on the activities of microorganisms, such as bacteria, that are responsible for the processes of degradation and formation of essential compounds and most of the carbon flow in the sediments of mangrove forests (Holguin et al. 2001). The adaptation of bacterial species to mangrove conditions indicates a potential source of biotechnological resources to be explored, including the discovery of new bacterial species that produce organic acids and enzymes that can be used for agriculture and industry (Dias et al. 2009b). In this scenario, endophytic bacteria are of agronomic interest because these organisms can enhance plant growth and improve plant nutrition through diverse mechanisms such as phosphorus solubilization (Quecine et al. 2014; Rukshana-Begum and Tamilselvi 2016). Gayathri et al. (2010) isolated endophytic bacteria from the healthy leaves of mangrove species from the Pichavaram mangrove forest in Tamil Nadu, India. In total, 104 endophytic bacteria only six endophytic isolates showed phosphate solubilization activity. This study demonstrated that mangroves are sources of endophytic

218

P. T. Lacava et al.

bacteria with the potential for phosphate solubilization. Janarthine and Eganathan (2012) isolated endophytic bacteria from surface-sterilized pneumatophores of Avicennia marina, a plant common to all mangroves of India. Among 13 endophytic bacteria, four isolates were genotypically identified as Bacillus spp., B. cereus, Enterobacter sp., and Sporosarcina aquimarina. The potential of the endophytic strain S. aquimarina SjAM16103 to promote plant growth was analyzed in vitro and in vivo. The results indicated that SjAM16103 produced 2.37 µmol/mL IAA, siderophores and was able to solubilize insoluble phosphate. Gayathri and Muralikrishnan (2013), observed that 24 endophytic bacteria exhibited phosphate solubilization in vitro according to the method described by Pandey et al. (2008). Tam et al. (2018) reported the isolation of P- solubilizing endophytic bacteria associated with Rhizophora mucronate and Avicennia alba, naturally growing mangrove species. The inorganic phosphate solubilizing ability by endophytes was tested on the National Botanical Research Institute’s phosphate (NBRIP) medium and the P2 O5 concentration was measured by the ammonium molybdate method (Nautiyal et al. 2000). All 86 endophytic isolates grew well on the NBRIP medium showed phosphate solubilization abilities. Brazilian mangroves are primarily made up of three tree species, Rhizophora mangle, Laguncularia racemosa, and Avicennia sp. (Dias et al. 2009b), from which several diverse endophytic bacteria (Castro et al. 2014) have been isolated. Our research group evaluated a large number of endophytic bacterial strains, from three different plant species, namely, R. mangle, L. racemosa, and Avicennia sp., to examine phosphate solubilization (Castro et al. 2018). All 115 strains examined produced a halo during the phosphate solubilization test in vitro. The endophytic strain MCR1.48 (Enterobacter sp.), which has a high P solubilization index, was selected for in vivo assays in Acacia polyphylla. We selected the commonly used reforestation tree A. polyphylla, which has few published studies involving inoculation by bacteria of agronomic interest and used for the reforestation of degraded areas in Brazil and reflects the ability of this leguminous tree species to recover degraded soils, thereby decreasing costs and increasing benefits to the environment (Rao et al. 2007). Inoculation with Enterobacter sp. strain MCR1.48 increased the dry mass of A. polyphylla shoots and roots, suggesting that the presence of the endophyte generates important benefits that promote the growth and fitness of this plant. In this context, Castro et al. (2018) reported that the inoculation of a highly P-solubilizing strain, MCR1.48, increased the shoot dry mass of A. polyphylla. This result indicates that phosphorous solubilization plays a key role in plant growth in trees.

9.4.4 The Agronomic Potential of Phosphate Solubilization by Endophytic Fungi from the Tropical Savanna Sustainable agriculture requires the use of strategies to increase or maintain the current rate of food production while reducing damage to the environment and human

9 Phosphate Solubilization by Endophytes from the Tropical Plants

219

health. Because of the health effects of pollution related to chemical fertilizers and pesticides, interest in finding alternative green methods (Abo Nouh 2019). The use of microbial plant growth promoters is an alternative to conventional agricultural technologies. In this context, endophytes play an important role in growth promotion and resistance to various biotic and abiotic stresses and diseases in plants (Abo Nouh 2019; Azevedo and Quecine 2019). Similar to PGPR, these microorganisms have great potential to be used as safe and cost-effective alternatives to chemical fertilizers due to their wide range of plant growth-promoting activities (Abo Nouh 2019). The reduced availability of P in potentially productive acidic soils such as the Brazilian savanna requires plants to associate symbiotically with microorganisms, such as endophytes, that are adapted to those soil conditions (Zapata and Axmann 1995) and alter complexes that adsorb phosphate under acidic conditions, including FePO4 and AlPO4 (Andrade et al. 2003). The plant growth-promoting effects of endophytes include increased plant height and biomass of shoots, stems, and roots; lignification of the xylem vessels; and increased crop yield (Azevedo and Quecine 2019). In this context, phosphorus deficiency limits agricultural production, especially in acidic soils such as those of the Brazilian savanna (Nakayama et al. 1998). In this biome, the water-soluble P is transformed into iron phosphate (FePO4 ) and aluminum phosphate (AlPO4 ) (Silva et al. 2011), which are moderately soluble complexes (Son et al. 2006; Yadav et al. 2010; Chai et al. 2011). On the other hand, Vitorino et al. (2012) reported the capacity of endophytic fungi isolated from roots of Hyptis marrubioides Epling, a Brazilian savanna species, to solubilize calcium phosphate in GELP medium and iron phosphate in modified Reyes basal medium. Of six fungal strains analyzed by solubilization assays, none of the fungi tested solubilized CaHPO4 . In contrast, all of these fungi demonstrated the capacity to solubilize high levels of FePO4 . These authors suggested that none of the fungi strains tested solubilized CaHPO4 may be related to the fact that these fungi were isolated from the root system of H. marrubioides Epling, a plant adapted to acidic soil, in which P is bound to Fe3+ and to Al3+ (Khan et al. 2009). According to Sharma and Roy (2015), fungal endophytes were isolated from root, stem, and leaves of the plant Amaranthus spinosus, a species occurring in the savanna biome, stated that endophytic fungal isolates of the plant A. spiunosus showed a positive test for phosphate solubilization. The phosphate solubilization efficiency was found to be highest for the fungal genera Aspergillus isolated from the stem of the plant. In our research group, Torres (2018) studied 66 endophytic fungi isolated from Stryphnodendron adstringens and Solanum lycocarpum St. Hill collected in the Brazilian Tropical Savanna Reserve of the Federal University of São Carlos, Brazil. Healthy leaves and stems of both plants were collected and submitted to superficial asepsis. After incubation of the botanical material, isolation and molecular identification of the endophytic fungi were performed. The endophytic strains were evaluated in vitro for the solubilization of inorganic phosphate. These strains showed promise because of their ability to solubilize inorganic phosphate with mean phosphate solubilization indexes ranging from 1.46 to 1.93 and 1.19 to 2.61 for the strains isolated from S. adstringens and S. lycocarpum, respectively.

220

P. T. Lacava et al.

9.5 Conclusion The search for interesting natural biological activities has been the basis for the development of various biotechnological and agricultural applications. The microbial world, and endophytes, in particular, exhibit vast genetic and metabolic biodiversity that has not yet been thoroughly explored. According to Azevedo and Quecine (2019), most studies on endophytes have been carried out using hosts from temperate countries, while data from tropical regions remain scarce. Available literature revealed that tropical plants host a great diversity of endophytic microorganisms, many of which are yet to be studied. The Phosphate-solubilizing endophytes are important not only because they contribute to plant growth but also because of their prospective commercialization to manufacture bio-fertilizers. An understanding of the ability and efficiency of microorganisms in solubilizing phosphates can allow the selection of lines with high potential for using them as biofertilizers. This application of microorganisms can replace or reduce the use of soluble phosphate fertilizers by better using the existing naturally or after amendments to the soil. Acknowledgements This work was supported by grants from the São Paulo Research Foundation, FAPESP (Proc. Nos. 2015/10974-8 and 2019/08867-0).

References Abbasi H, Akhtar A, Sharf R (2015) Vesicular arbuscular mycorrhizal (VAM) fungi: a tool for sustainable agriculture. Am J Plant Nutr Fert Technol 5:40–49 Abhilash PC, Srivastava P, Jamil S, Singh N (2011) Revisited Jatropha curcas as an oil plant of multiple benefits: critical research needs and prospects for the future. Environ Sci Pollut Res 18:127–131 Abo Nouh FA (2019) Endophytic fungi for sustainable agriculture. Microbial Biosystems 4:31–44 Afzal I, Shinwaria ZK, Sikandarb S, Shahzadc S (2019) Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol Res 221:36–49 Ahemad M, Zaidi A, Khan MS, Oves M (2009) Biological importance of phosphorus and phosphate solubilizing microbes - An overview. In: Khan MS, Zaidi A (eds) Phosphate solubilising microbes for crop improvement. Nova Science Publishers Inc, New York, pp 1–14 Andrade FV, Mendonça ES, Alvarez VH, Novais RF (2003) Adição de ácidos orgânicos e húmicos em latossolos e adsorção de fosfato. R Bras Ci Solo 27:1003–1011 Andrade, LF (2012) Bactérias endofíticas de bananeira prata-anã: fixação de nitrogênio, solubilização de fosfato de cálcio e produção de ácido indol-3- acético. PhD. Thesis, Universidade Estadual de Montes Claros Andrade, PHM (2019) Análise da diversidade genética e potencial biotecnológico da comunidade bacteriana associada a Coffea arabica L. de cultivo convencional e orgânico. PhD. Thesis, Universidade Federal de São Carlos Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181 Araújo WL, Lacava PT, Andreote FD, Azevedo JL (2008) Interaction between endophytes and plant host: Biotechnological aspects. In: Ait Barka E, Clément C (eds) Plant-microbe interactions, vol 1. Research Signpost, Kerala, pp 1–21

9 Phosphate Solubilization by Endophytes from the Tropical Plants

221

Azevedo JL, Araújo WL (2007) Diversity and applications of endophytic fungi isolated from tropical plants. In: Ganguli BN, Deshmukh SK (eds) Fungi: multifaceted microbes. CRC Press, Boca Raton, pp 189–207 Azevedo JL, Quecine MC (2019) Biodiversity and biotechnological applications of microorganisms associated with tropical plants. Microbiome in plant health and disease, pp 293–313 Azevedo JL, Maccheroni W, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65 Baliah NT, Pandiarajan G, Kumar BM (2016) Isolation, identification and characterization of phosphate solubilizing bacteria from different crop soils of Srivilliputtur Taluk, Virudhunagar District, Tamil Nadu. Trop Ecol 57:465–474 Behera SK, Srivastava P, Tripathi R, Singh JP, Singh N (2010) Evaluation of plant performance of Jatropha curcas L. under different agro-practices for optimizing biomass—a case study. Biomass Bioenergy 34:30–41 Brasil. (2015) Ministério da Agricultura. Café: Saiba mais. http://www.agricultura.gov.br/vegetal/ culturas/cafe/saiba-mais Castro RC, Quecine MC, Lacava PT, Batista BD, Luvizotto DM, Marcon J, Ferreira A, Melo IS, Azevedo JL (2014) Isolation and enzyme bioprospection of endophytic bacteria associated with plants of Brazilian mangrove ecosystem. Springerplus 3:1–9 Castro RA, Dourado MN, Almeida JR, Lacava PT, Nave A, Melo IS, Azevedo JL, Quecine MC (2018) Mangrove endophyte promotes reforestation tree (Acacia polyphylla) growth. Braz J Microbiol 49:59–66 Chai B, Wu Y, Liu P, Liu B, Gao M (2011) Isolation and phosphate-solubilizing ability of a fungus, Penicillium sp. from soil of an alum mine. J Basic Microbiol 51:5–14 Dias AC, Costa FE, Andreote FD, Lacava PT, Teixeira MA, Assumpção LC, Araújo WL, Azevedo JL, Melo IS (2009a) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195 Dias AC, Andreote FD, Dini-Andreote F et al (2009b) Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment. World J Microbiol Biotechnol 25:1305– 1311 de Abreu CS, Figueiredo JEF, Oliveira CA, dos Santos VL, Gomes EA, Ribeiro VP, Barros BA, Lana UGP, Marriel IE (2017) Maize endophytic bacteria as mineral phosphate solubilizers. Genet Mol Res 16:gmr16019294 Edrisi SA, Dubey RK, Tripathi V, Bakshi M, Srivastava P, Jamil S et al (2015) Jatropha curcas L.: a crucified plant waiting for resurgence. Renew Sustain Energy Rev 41:855–862 Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221– 230 Farrar K, Bryant D, Cope-Selby N (2014) Understanding and engineering beneficial plant-microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12:1193–1206 Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152 Gaiero JR, McCall CA, Thompson KA, Day NJ et al (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750 Gautam AK, Avasthi S (2019) Fungal endophytes: Potential biocontrol agents in agriculture. In: Kumar A, Singh AK, Choudhary KK (eds) Role of plant growth promoting microorganisms in sustainable agriculture and nanotechnology. Woodhead Publishing, USA., pp 241–283 Gayathri S, Saravanan D, Radhakrishnan M, Balagurunathan R, Kathiresan K (2010) Bioprospecting potential of fast growing endophytic bacteria from leaves of mangrove and salt-marsh plant species. Indian J Biotechnol 9:397–402 Gayathri P, Muralikrishnan V (2013) Isolation of endophytic bacteria from mangrove, bananas and sugarcane for their biological activities. AJRBPS 1:19–27

222

P. T. Lacava et al.

Ghosh R, Barman S, Mukherjee R, Mandal NC (2016) Role of phosphate solubilizing Burkholderia spp. for successful colonization and growth promotion of Lycopodium cernuum L. (Lycopodiaceae) in lateritic belt of Birbhum district of West Bengal, India. Microbiol Res 183:80–91 Golinska P, Wypij M, Agarkar G, Rathod D, Dahm H, Rai M (2015) Endophytic actinobacteria of medicinal plants: diversity and bioactivity. Anton Leeuw Int J G 108:267–289 Gomes EA, Silva UC, Marriel IE, Oliveira CA et al (2014) Rock phosphate solubilizing microorganisms isolated from maize rhizosphere soil. Rev. Bras. Milho Sorgo 13:69–81 Gurikar C, Naik MK, Sreenivasa MY (2016) Azotobacter: PGPR activities with special reference to effect of pesticides and biodegradation. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity: research perspectives. Springer, New Delhi Gyaneshwar P, Kumar GN, Parekh LJ, Poodel PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93 Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914 Hilda R, Fraga R (2000) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotech Adv 17:319–359 Holguin G, Vazquez P‚ Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soils 33:265– 278. https://doi.org/10.1007/s003740000319 Islam MR, Sultana T, Joe MM, Yim W, Cho JC, Sa T (2013) Nitrogen-fixing bacteria with multiple plant growth-promoting activities enhance growth of tomato and red pepper. J Basic Microb 53:1004–1015 Islam AA, Yaakob Z, Ghani JA, Anuar N (2014) Jatropha curcas L.: a future energy crop with enormous potential. In: Biomass and bioenergy. Springer, p 31–61 Janarthine SRS, Eganathan P (2012) Plant growth promoting of endophytic Sporosarcina aquimarina SjAM16103 isolated from the pneumatophores of Avicennia marina L. Int J Microbiol 2012:532060. https://doi.org/10.1155/2012/532060 Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6:e20396 Kämpfer, P (2003) Taxonomy of phosphate solubilizing bacteria. In: Development in Plant and soil science: First International Meeting on Microbial phosphate Solubilization, Salamanca, Spain, Anais. Netherlands, p 10–106 Kang SM, Khan AL, You YH, Kim JG, Kamran M, Lee IJ (2014) Gibberellin production by newly isolated strain Leifsonia solise and its potential to promote plant growth. J Microbiol Biotechn 24:106–112 Karpagam T, Nagalakshmi PK (2014) Isolation and characterization of phosphate solubilizing microbes from agricultural soil. Int J Curr Microbiol Appl Sci 3:601–614 Khan AA, Jilani G, Akhtar MS, Naqvi SMS, Rasheed M (2009) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J Agric Biol Sci 1:48–58 Khan KS, Joergensen RG (2009) Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresour Technol 100:303–309 Khiari L, Parent LE (2005) Phosphorus transformations in acid light-textured soils treated with dry swine manure. Can J Soil Sci 85:75–87 Kang S, Radhakrishnan R, You YH‚ et al (2014) Phosphate solubilizing bacillus megaterium mj1212 regulates endogenous plant carbohydrates and amino acids contents to promote mustard plant growth. Indian J Microbiol 54:427–433. https://doi.org/10.1007/s12088-014-0476-6 Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251 Ku´zniar A, Włodarczyk K, Woli´nska A (2019) Agricultural and other biotechnological applications resulting from trophic plant-endophyte interactions. Agronomy 9:779. https://doi.org/10.3390/ agronomy9120779

9 Phosphate Solubilization by Endophytes from the Tropical Plants

223

Laviola BG, Alves AA, Gurgel FDL, Rosado TB, Rocha RB, Albrecht JC (2012) Estimates of genetic parameters for physic nut traits based in the germplasm two years evaluation. Ciênc Rural 42:429–435 Laviola BG, Alves AA, Kobayashi, Formighieri AK (2015) Situação atual do pinhão-manso no Brasil e no mundo. Brasília, DF: Embrapa Agroenergia 7p. (Embrapa Agroenergia. Comunicado técnico, 012) Laviola BG, Bhering LL, Mendonca S, Rosado TB, Albrecht JC (2011) Caracterização morfoagronômica do banco de germoplasma de pinhão manso na fase jovem. Biosci J 27:371–379 Laviola BG, Rosado TB, Bhering LL, Kobayashi AK, Resende MDVD (2010) Genetic parameters and variability of physic nut accessions during early developmental stages. Pesq Agropec Bras 45:1117–1123 Machado PC (2015) Identificação molecular e caracterização bioquímica de bactérias endofíticas associadas à cultura do pinhão-manso (Jatropha curcas L.) com potencial biotecnológico. Master. Thesis, Universidade Federal de São Carlos Machado PC (2019) Diversidade e potencial biotecnológico da comunidade bacteriana associada ao pinhão-manso (Jatropha curcas L.). PhD. Thesis, Universidade Federal de São Carlos Madhaiyan M, Jin TY, Roy JJ, Kim S-J, Weon HY, Kwon S-W, Ji L (2013) Pleomorphomonas diazotrophica sp. nov., an endophytic N-fixing bacterium isolated from root tissue of Jatropha curcas L. Int J Syst Evol Microbiol 63:2477–2483 Maheshwari DK, Annapurna K (2017) Endophytes: crop productivity and protection. Springer Gewerbestrasse, Switzerland Malboobi MA, Owlia P, Behbahani M, Sarokhani E, Moradi S, Yakhchali B, Deljou A, Heravi KM (2009) Solubilization of organic and inorganic phosphates by three highly efficient soil bacterial isolates. World J Microbiol Biotechnol 25:1471–1477 Martins NGS (2004) Os fosfatos na cana-de-açúcar. Dissertation University of São Paulo - Escola Superior de Agricultura Luiz de Queiroz, Piracicaba-SP p. 87 Mendes ANG, et al. (1995) Recomendações Técnicas para a cultura de cafeeiros no sul de Minas. In: Encontro sul mineiro de cafeicultores, Lavras. Anais. Lavras: UFLA, 1995. 76 p Mohammadi K (2012) Phosphorus solubilizing bacteria: Occurrence, mechanisms and their role in crop production. Resources Environ 2:80–85 Mohanty SR, Dubey G, Kollah B (2017) Endophytes of Jatropha curcas promote growth of maize. Rhizosphere 3:20–28‚ ISSN 2452–2198. https://doi.org/10.1016/j.rhisph.2016.11.001 Moniruzzaman M, Yaakob Z, Khatun R (2016) Biotechnology for Jatropha improvement: a worthy exploration. Renew Sust Energ Rev 54:1262–1277 Muleta D, Assefa F, Börjesson E, Granhall, U (2013) Phosphate-solubilising rhizobacteria associated with Coffea arabica L. in natural coffee forests of southwestern Ethiopia. J Saudi Soc Agri Sci 12:73–84. https://doi.org/10.1016/J.JSSAS.2012.07.002 Musson G (1994) Ecology and effects of endophytic bacteria in plants. Auburn: Auburn University 114p. (Ms Thesis) Nakayama LHI, Caceres NT, Alcarde JC, Malavolta E (1998) Eficiência relativa de fontes de fósforo de diferentes solubilidades na cultura do arroz. Sci Agr 55:183–190 Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D (2000) Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182:291–296 Ngamau CN, Matiru VN, Tani A, Muthuri CW (2014) Potential use of endophytic bacteria as biofertilizer for sustainable banana (Musa spp.) Production. AJHS 8:1–11 Oliveira ALM, Urquiaga S, Baldani JI (2003) Processos e mecanismos envolvidos na influência de microrganismos sobre o crescimento vegetal. Embrapa Agrobiologia, Jaguariúna, p 40 Oliveira CA, Alves VM, Marriel IE, Gomes EA et al (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado biome. Soil Biol Biochem 41:1782–1787 Oliveira MNV, Santos TMA, Vale HMM, Delvaux JC, Cordero AP, Ferreira AB, Miguel PSB, Tótola MR, Costa MD, Moraes CA, Borges AC (2013) Endophytic microbial diversity in coffee cherries of Coffea arabica from southeastern Brazil. Can J Microbiol 59:221–230

224

P. T. Lacava et al.

Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils 46:807–816 Pandey A, Das N, Kumar B, Rinu K, Trivedi P (2008) Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region. World J Microbiol Biotechnol 24:97–102 Pandey C, Negi YK, Maheshwari DK, Rawat D, Prabha D (2018) Potential of native cold tolerant plant growth promoting bacilli to enhance nutrient use efficiency and yield of Amaranthus hypochondriacus. Plant Soil 428(1–2):307–320 Pérez-García A, Diego R, Antonio de Vicente (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotech 22(2):187–193. ISSN 0958–1669. https://doi.org/10.1016/j.copbio.2010.12.003 Pérez E, Sulbarán M, Ball MM, Yarzábal LA et al (2007) Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biol Biochem 39:2905–2914 Puente ME, Li CY, Bashan Y (2009) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401 Qin S, Yuan B, Zhang Y-J, Bian G-K, Tamura T, Sun B-Z, Li W-J, Jiang J-H (2012) Nocardioides panzhihuaensis sp. nov., a novel endophytic actinomycete isolated from medicinal plant Jatropha curcas L. Anton Leeuw Int J G 102:353–360 Quecine MC, Batista BD, Lacava PT (2014) Diversity and biotechnological potential of plantassociated endophytic bacteria. In: Kumar AP, Govil JN (eds) Biotechnology: plant biotechnology, vol 2. Studium Press LLC, Houston, pp 377–423 Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Marostica MR Jr (2014) Fungal growth promoter endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79 Rao KPC, Verchot LV, Joshi LM (2007) Adaptation to climate change through sustainable management and development of agroforestry systems. J SAT Agric Res 4:1–30 Raven HP, Evert FR, Eichhorn ES (2001) Biologia vegetal. Guanabara Koogan S.A, Rio de Janeiro, pp 698–719 Reddy BVS, Ramesh S, Ashok Kumar A, Wani SP, Ortiz R, Ceballos H et al (2008) Bio-fuel crops research for energy security and rural development in developing countries. Bioenergy Res 1:248–258 Reginatto, TSC (2008) Diversidade de bactérias associadas a bromélias do Parque Estadual de Itapuã/RS. PhD. Thesis, Universidade Federal do Rio Grande do Sul Reetha S, Bhuvaneswari G, Thamizhiniyan P, Mycin TR (2014) Isolation of indole acetic acid (IAA) producing rhizobacteria of Pseudomonas fluorescens and Bacillus subtilis and enhance growth of onion (Allim cepa L.). Int J Curr Microbiol Appl Sci Int J Curr Microbiol Appl Sci 3:568–574 Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339 Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth promoting bacteria. Plant Soil 287:15–21 Roley SS, Duncan DS, Liang D, Garoutte A, Jackson RD, Tiedje JM, Philip Robertson G (2018) Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient. PLoS ONE 13:e0197320 Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837 Rukshana-Begum S, Tamilselvi KS (2016) Endophytes are plant helpers: an overview. Int J Curr Microbiol App Sci 5:424–436 Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9 Sagoe CI, Ando T, Kouno K, Nagaoka T (1998) Relative importance of protons and solution calcium concentration in phosphate rock dissolution by organic acids. Soil Sci Plant Nutr 44:617–625

9 Phosphate Solubilization by Endophytes from the Tropical Plants

225

Santana EB, Marques ELS, Dias JCT (2016) Effects of phosphate-solubilizing bacteria, native microorganisms and rock dust on Jatropha curcas L. growth. Genet Mol Res 15(4). https://doi. org/10.4238/gmr.15048729 Sarbadhikary SB, Mandal NC (2018) Elevation of plant growth parameters in two solanaceous crops with the application of endophytic fungus. Indian J Agr Sci 52:424–428 Schulz B, Guske S, Dammann U, Boyle C (1998) Endophytes host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227 Schulz B, Rommert AK, Dammann U, Aust HJ (1999) The endophyte-host interaction: a balanced antagonism? Mycol. Res 103:1275–1283 Sharma et al (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587 Sharma S, Roy S (2015) Isolation and identification of a novel endophyte from a plant Amaranthus spinosus. Int J Curr Microbiol App Sci 4:785–798 Shehata HR, Dumigan C, Watts S, Raizada MN (2017) An endophytic microbe from an unusual volcanic swamp corn seeks and inhabits root hair cells to extract rock phosphate. Sci Rep 7:1347 Silva ACS, Chagas Junior AF, Oliveira LA, Chagas LFB (2011) Ocorrência de bactérias solubilizadoras de fosfato nas raízes de plantas de importância econômica em Manaus e Rio Preto da Eva, Amazonas. J Biotec Biodivers 2:37–42 Silva HSA, Tozzi JPL, Terrasan CRF, Bettiol W (2012) Endophytic microorganisms from coffee tissues as plant growth promoters and biocontrol agents of coffee leaf rust. Biol Control 63:62–67 Sims JT, Pierzynski GM (2005) Chemistry of phosphorus in soil. In: Tabatabai AM, Sparks DL (eds) Chemical processes in soil, SSSA book series 8. SSSA, Madison, pp 151–192 Singh K, Singh B, Verma SK, Patra DD (2014) Jatropha curcas: a ten years story from hope to despair. Renew Sustain Energy Rev 35:356–360 Son HJ, Park GT, Cha MS, Heo MS (2006) Solubilization of insoluble inorganic phosphates by a novel salt- and pH-tolerant Pantoea agglomerans R-42 isolated from soybean rhizosphere. Bioresource Technol 97:204–210 Strobel GA, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268 Tam HT, Phuong TV, Diep CN (2018) Isolation and identification of endophytic bacteria associated with Rhizophora mucronate and Avicennia alba of Nam Can district, Ca Mau Mangrove Ecosystem. IJIET 10:147–159 Tanwar SPS, Shaktawat MS (2003) Influence of phosphorus sources, levels and solubilizers on yield, quality and nutrient up-take of soybean (Glycine max)—wheat (Triticum aestivum) cropping system in southern Rajasthan. Indian J Agric Sci 73:3–7 Tikkoo A, Yadav SS, Kaushik N (2013) Effect of irrigation, nitrogen and potassium on seed yield and oil content of Jatropha curcas in coarse textured soils of northwest India. Soil Tillage Res 134:142–146 Torres FL (2018) Isolamento, caracterização e potencial biotecnológico de fungos endofíticos associados às plantas de cerrado. MS. Thesis, Universidade Federal de São Carlos van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310 Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable sources. Plant Physiol 127:390–397 Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586 Vitorino LC, Silva FG, Soares MA, Souchie EL, Costa AC, Lima WC (2012) Solubilization of calcium and iron phosphate and in vitro production of indoleacetic acid by endophytic isolates of Hyptis marrubioides Epling (Lamiaceae). Int Res J Biotechnol 3:47–54 Vyas P, Bansal A (2018) Fungal endophytes: role in sustainable agriculture. In: Gehlot P, Singh J (eds) Fungi and their role in sustainable development: Current Perspectives. Springer, Singapore, pp 107–120

226

P. T. Lacava et al.

White JF, Kingsley KL, Verma SK, Kowalski KP (2018) Rhizophagy cycle: an oxidative process in plants for nutrient extraction from symbiotic microbes. Microorganisms 6:95. https://doi.org/ 10.3390/microorganisms6030095 Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544 Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997 Zapata F, Axmann H (1995) 32P isotopic techniques for evaluating the agronomic effectiveness of rock phosphate material. Nutr Cycl Agroecosys 41:189–195

Part III

Beneficial Microbes and Mineral Nutrient Management

Chapter 10

Endophytic Actinobacteria Associated with Mycorrhizal Spores and Their Benefits to Plant Growth Krisana Lasudee, Pharada Rangseekaew, and Wasu Pathom-aree

Abstract Actinobacteria are a large group of Gram-positive bacteria with a unique high G + C content(%) in their genome. They are best known as major producers of bioactive compounds in particular secondary metabolites. Arbuscular mycorrhiza or endomycorrhiza are the most common symbionts between plant roots and fungi with long historical practices in agriculture. Recently, it has become apparent that there are actinobacteria live in association with arbuscular mycorrhizal spores as “endophytes.” This special niche harbors diverse actinobacterial taxa with potential in the production of plant growth-promoting substances. The application of some of these actinobacteria exhibited growth enhancement in several plant species including those grown under abiotic and biotic stresses. Plant growth-promoting properties are common within members of actinobacteria occurring endophytically in mycorrhizal spores. A study of Streptomyces from Funneliformis mosseae spores to alleviate adverse effects of drought on Thai jasmine rice KDML105 is a neat evidence of its potential to promote plant growth sustainably. The diversity of endophytic actinobacteria from mycorrhizal spores and their possible application in agriculture as plant growth promoters are the main focus of this chapter. Keywords Actinobacteria · Mycorrhizal spores · Endophyte · Plant Growth-Promoting rhizobacteria · Drought

10.1 Introduction Actinobacteria are a large group of Gram-positive mostly filamentous bacteria with the characteristic of their high G+C content (%) in their DNA. Based on their genome K. Lasudee · P. Rangseekaew · W. Pathom-aree Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand W. Pathom-aree (B) Research Center of Microbial Diversity and Sustainable Utilization, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_10

229

230

K. Lasudee et al.

analysis, the actinomycetes group of organisms is now renamed as actinobacteria. They are widely distributed in natural environments and established in cells and tissues of plants. Members of actinobacteria in particular Streptomyces spp. are major producers of antimicrobial agents and bioactive compounds, some of which are being used today as antibacterial, antifungal, anticancer, or cholesterol-lowering drugs (Barka et al. 2016). On the other hand, they have the potential to produce plant growth-promoting compounds and have biocontrol properties (Singh et al. 2018; Suarez-Moreno et al. 2019; Liotti et al. 2019). Actinobacteria can be used to improve plant growth and promote growth of plants under both abiotic and biotic stresses. Similar to other PGP bacteria, they can promote plant growth via direct and indirect mechanisms (Olanrewaju et al. 2017; Sathya et al. 2017; Vurukonda et al. 2018). Nitrogen fixation, phytohormones production, phosphate solubilization, siderophore production, etc., are considered as direct (Glick 2012; Hamadi and Mohammadipanah 2015; Vurukonda et al. 2018). Whereas indirect mechanisms include antibiotics production (Dinesh et al. 2017; Singh and Dubey 2018) and production of lytic enzymes to degrade the cell wall of fungal pathogens (Singh and Gaur 2016; Sathya et al. 2017; Gasmi et al. 2019). Thus, actinobacteria are attractive microorganisms with high potential for agricultural applications in terms of environmental sustainability and safety. The term mycorrhiza (from the Greek “mycos” meaning fungus and “rhiza” meaning root) was coined to describe the symbiotic association between plant root and fungi (Parniske 2008; Bonfante and Anca 2009). To date, at least 50,000 fungal species are suggested to form mycorrhizal associations with 250,000 plant species (van der Heijden et al. 2015). Arbuscular mycorrhiza (AM) is a type of endomycorrhiza in which the fungal hyphae penetrate host root cells. It is widespread in natural environments and can be found in more than 80% of living land plant species, liverworts, ferns, woody gymnosperms, angiosperms, and grasses (Bonfante and Anca 2009). Arbuscular mycorrhizal fungi (AMF) are obligate symbionts (Owen et al. 2015) and meant to improve the plant’s nutrient uptake and in turn plant provides AM fungi with carbon sources and habitat (Smith and Smith 2011). Several microbial taxa including members of both Gram-negative bacteria (Xavier and Germida 2003; Bharadwaj et al. 2008a, b; Battini et al. 2016; Lasudee et al. 2017) and Gram-positive bacteria including actinobacteria of the genus Streptomyces (Schrey et al. 2012; Mohandas et al. 2013; Poovarasan et al. 2013; Battini et al. 2016; Lasudee et al. 2018; Chaiya et al. 2019) associated with AM fungal spores have recently been reported. These mycorrhizal associated bacteria usually exhibited interesting biocontrol and plant growth-promoting activities (Mohandas et al. 2013; Poovarasan et al. 2013; Battini et al. 2016) thus make them attractive for application in sustainable agriculture. Drought stress induces damage to the biochemical and physiological processes of plants thus interfere with their normal functions (Pandey and Shukla 2015). Moreover, drought influences the nutrient availability and transportation in soil (GontiaMishra et al. 2016; Vurukonda et al. 2016). Currently, climate change is causing a reduction in precipitation and changed rainfall patterns. This changing climate leads

10 Endophytic Actinobacteria Associated …

231

to more frequent drought events that threaten crop productivity and global food security (Anjum et al. 2011; Fahad et al. 2017). Crop yields in more than 70% of global arable lands are affected by water deficits especially in Africa and Asia (Eke et al. 2019). About 85% of damage and loss in agriculture from 2010 to 2016 are related to drought with an estimated economical value of at least USD 29 billion (FAO 2018). For these reasons, drought is emerging as the most deleterious abiotic stress to crop production and yields worldwide. This chapter aims to summarize the current information on the diversity of actinobacteria associated with arbuscular mycorrhizal spores and their beneficial applications to promote plant growth. Special attention has been given to actinobacteria associated with Funneliformis mosseae spores and their ability to promote rice growth under drought conditions.

10.2 Endophytic Actinobacteria from Mycorrhiza Mycorrhizal fungi interact with several actinobacteria in all stages of their life cycle (Frey-Klett et al. 2007). This associated actinobacterial population has a versatile role in health promotion in positive ways by way of root colonization, stimulate hyphal, and spore germination of their mycorrhizal host (Roesti et al. 2005). In turn, mycorrhizal fungi support the growth of associated bacteria by providing habitat and nutrients. However, the exact role of these associated bacteria is yet to be established. Endophytic bacteria adhere to the arbuscular mycorrhiza hyphae (Bianciotto et al. 1996; Manfeld-Giese et al. 2002) and or embeded within the outer AM spore wall layer (Walley and Germida 1996) or penetrate inner layer of spore (Roesti et al. 2005). Actinobacteria frequently found inside the mycorrhizal spores. Mycorrhizal spore-associated actinobacteria have been isolated, characterized, and applied to the plants for their growth as summarized in Table 10.1. Most of the actinobacteria isolated from mycorrhizal spores are filamentous including species of Amycolatopsis, Intrasporangium, Nocardioides, Pseudonocardia, Streptomyces, Streptoverticillium, etc. From all filamentous genera, Streptomyces spp. remained the most abundant actinobacteria found from several mycorrhizae for example Glomus mosseae (Mohandas et al. 2013), Rhizophagus intraradices (Battini et al. 2016), and F. mosseae (Lasudee et al. 2018). Other nonfilamentous actinobacteria including Arthrobacter, Cellulomonas, Corynebacterium, Curtobacterium, Leifsonia, Mycobacterium, Nocardia, Propionibacterium, and Streptosporangium (Bharadwaj et al. 2008b; Poovarasan et al. 2013; Battini et al. 2016; Long et al. 2017) were also found invarious genera of mycorrhizal spores. The standard isolation methods for actinobacteria occurring inside mycorrhizal spores generally involve 3 steps (i) surface sterilization of mycorrhizal spores, (ii) destruction of the spore cell wall, and (iii) cultivation of actinobacteria on selective media. For surface sterilization, different chemicals were used including 2% Clorox (Lee and Koske 1994), chloramine (Mohandas et al. 2013), 4% (w/v) chloramine T trihydrate (Chaiya et al. 2019), 2% sodium hypochlorite, and 70% (v/v) ethanol

Taxa

Nocardia sp. Streptomyces sp.

Streptomyces spp. Nocardia spp. Streptosporangium Streptoverticillium Intrasporangium Norcardiodes

Arthrobacter spp. Micrococcus spp. Cellulomonas flavigena Aureobacterium saperdae Clavibacter michiganense subsp. nsidiosum Curtobacterium citreum Corynebacterium bovis

Streptomyces fradiae Streptomyces avermitilis Streptomyces cinnamonenesis Streptomyces canus Leifsonia poae Streptomyces netropis Streptomyces scabies Streptomyces griseus Streptomyces violarus Streptomyces albidoflavus

Mycorrhiza

Gigaspora gigantia

Glomus macrocarpum

Glomus mosseae or Glomus intraradices

Glomus mosseae

Table 10.1 Actinobacteria from mycorrhizal spores and isolation media

Rhizophere of guava (Psidium guajava L. cv Arka Mridula), Karnataka State, southern India

Rhizopheres soils of Festuca ovina or Leucanthemum vulgare

Soils from the edge of a non-irrigated barley field in Yolo Country, California, USA

Barrier sand dune at Moonstone Beach, Rhode Island (RI)

Source of AM spore

Ames et al. (1989)

Lee and Koske (1994)

References

Ken Knight agar, incubated at 28 °C ± 2 for 2–7 days

(continued)

Poovarasan et al. (2015)

Mohandas et al. (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

Tryptic soy broth agar at Bharadwaj et al. 25 °C in the dark for 48 h (2008b)

Solidified chitin water agar at 25–27 °C for 4 weeks

MYPT agar at room temperature (21–27 °C) for up to two weeks

Media

232 K. Lasudee et al.

• Curtobacterium luteum M060824-7 the Ministry of • Mycobacterium mucogenicum M060824-8 Agriculture, Forestry, and • Streptomyces sp. Fisheries Gene bank, Tsukuba, Japan

• • • • • •

Amycolatopsis eburnea sp. nov

Gigaspora margarita MAFF 520054 spores

Funneliformis mosseae CMU-RYA08

Funneliformis mosseae RYA08

Agarwood (Aquilaria crassna Pierre ex Lec.) rhizophere soil,Klaeng, Rayong province, Thailand

Pseudonocardia nantongensis isolate SP Soil of a Aquilaria crassna Streptomyces thermocarboxydus isolate 48 plantation in Rayong Streptomyces spinoverrucosus isolate S1 Province, Thailand Streptomyces thermocarboxydus isolate S3 Streptomyces pilosus isolate S4 Streptomyces pilosus isolate S4-1

Pot-culture maintained in the collection of Microbiology Labs of the Department of Agriculture, Food and Environment, University of Pisa, Italy

Streptomyces spp. Arthrobacter phenanthrenivorans Nocardiodes albus

Rhizophagus intraradices isolate IMA6

Source of AM spore

Taxa

Mycorrhiza

Table 10.1 (continued) References

Lasudee et al. (2018)

Long et al. (2017)

Actinomycetes isolation Chaiya et al. (2019) agar at 30 °C for a month

Starch casein agar and humic acid vitamin agar at 30 for up to 4 week

Tryptic Soy Agar (TSA) at 26 °C for 7 days

Waksman’s agar at 28 °C Battini et al. (2016) for 7 days

Media

10 Endophytic Actinobacteria Associated … 233

234

K. Lasudee et al.

(Lasudee et al. 2018). The treatment time given for each chemical is varied depending on the concentration for example, Glomus mosseae spores were decontaminated with chloramine-T for 30 min (Mohandas et al. 2013). Alternatively, F. mosseae CMURYA08 spores were surface sterilized by 2% sodium hypochlorite for 1 min followed by 70% (v/v) ethanol (Lasudee et al. 2018) or by 4% (w/v) chloramine T trihydrate for 10 min (Chaiya et al. 2019). The spore cell wall could be broken by simple grinding with a sterile micro pestle. However, the suspending solution varied depending on author preferences. These solutions are steriled distilled water, phosphate buffer saline (PBS), and 0.75% sodium chloride. Several selective media have been used for isolation of endophytic actinobacteria from mycorrhizal spore namely ken knight agar (Poovarasan et al. 2015), Waksman’s agar (Battini et al. 2016), starch casein agar, humic acid vitamin agar (Lasudee et al. 2018), actinomycetes isolation agar (Chaiya et al. 2019), etc. Furthermore, a general cultivation medium such as tryptic soy agar (TSA) was also used for isolation (Long et al. 2017). Special media such as solidified chitin water agar was reported for isolation of chitinase producing actinobacteria from calcareous soil (Ames et al. 1989). Moreover, the enrichment procedure proved successful for the isolation of endophytic actinobacteria from F. mosseae spores. Lasudee et al. (2018) soaked the spores in soil extract broth and shaken at 120 rpm at room temperature for 1 h to enrich endophytic actinobacteria. This procedure was considered to be essential because the isolation of actinobacteria without an enrichment step led to the possibility of not getting actinobacterial growth on selective media.

10.3 Plant Growth-Promoting (PGP) Activities of Endophytic Actinobacteria Mycorrhiza is the association of a fungus and root plants (Mohandas et al. 2013) that play an important role in the agriculture ecosystem. The colonization of mycorrhizal fungi in root helps to promote plant growth via nutrient mobilization, biocontrol activity, etc. Interestingly, there are reports considering actinobacteria that can promote plant growth by different mechanisms both directly and indirectly.

10.3.1 Endophytic Actinobacteria Associated with Nutrient Uptake in Plants Endophytic actinobacteria promote plant growth directly by facilitating the nutrient acquisition of plants via many mechanisms including siderophore production and solubilization of phosphate, phytate, or zinc as summarized in Table 10.2. Phosphorus (P) is an essential macronutrient for the growth and development of plants (Behera et al. 2014). However, most phosphorus in the soil is available

10 Endophytic Actinobacteria Associated …

235

Table 10.2 Bioactivities related to nutrient uptake of endophytic actinobacteria from mycorrhizal spores Mycorrhiza

Taxa

Bioactivities

Glomus mosseae

Streptomyces avermitilis Streptomyces canus Leifsonia poae

• Production Mohandas of et al. siderophore (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

Streptomyces avermitilis Streptomyces canus Leifsonia poae Streptomyces fradiae Streptomyces netropis Streptomyces scabies Streptomyces griseus Streptomyces violarus Streptomyces albidoflavus Streptomyces cinnamonenesis

• Phosphate and zinc solubilization • Organic acid production (such as gluconic acid)

Streptomyces spp. Nocardiodes albus

• Phosphate Battini and phytate et al. (2016) solubilization

Arthrobacter phenanthrenivorans

• Siderophore production

Rhizophagus intraradices isolate IMA6

Funneliformis Pseudonocardia sp. isolate SP mosseae CMU-RYA08 • Streptomyces pilosus isolate S4 • Streptomyces pilosus isolate S4-1 • Streptomyces thermocarboxydus isolate 48 • Streptomyces spinoverrucosus isolate S1 • Streptomyces thermocarboxydus isolate S3

References

• Siderophore Lasudee production et al. (2018)

• Siderophore production • Phosphate solubilization

in insoluble forms which plants cannot uptake (Glick 2012). In soils, phosphorus usually exists in two forms insoluble inorganic and insoluble organic forms. Phosphorus can be bound with hydrated oxides such as aluminum (Al), iron (Fe), and manganese (Mn) that are poorly dissolved and assimilated (Behera et al. 2014). Similar to bacteria in soil, actinobacteria solubilize phosphate via mechanism: (i) production of organic acids (ii) secretion of enzymes. Some actinobacteria synthesize organic acids to solubilize inorganic phosphorus. Actinobacteria isolated from G. mosseae were able to solubilize tricalcium phosphate and aluminum phosphate by producing at least four organic acids (Poovarasan et al. 2015). In general, these

236

K. Lasudee et al.

actinobacteria produced gluconic acid as the major organic acid for phosphate solubilization (Mohandas et al. 2013; Poovarasan et al. 2015). Similarly, S. thermocarboxydus isolates S3 from F. mosseae CMU-RYA08 produced gluconic acid, malonic acid, oxalic acid, and propionic acid to solubilize tricalcium phosphate (Lasudee et al. 2018). Also, Streptomyces spp. and Arthrobacter phenanthrenivorans isolated from Rhizophagus intraradices were able to solubilize both insoluble organic (inositol phosphate) and insoluble inorganic phosphates (tri-calcium phosphate). Phosphate solubilizing ability was reported as solubilization efficiency (SE) (Battini et al. 2016). Also, zinc solubilization was reported in some Streptomyces species isolated from G. mosseae (Poovarasan et al. 2015). Iron is an important micronutrient for the growth of both plants and bacteria. Although iron is abundant in soils, it exists in the form of ferric iron which is insoluble. Thus, the amount of iron available to plants and bacteria is low (Glick 2012; Sathya et al. 2017). Siderophores are ferric iron (Fe3+ ) specific chelators that can promote plant growth both by direct and indirect mechanisms. Under limiting iron environment, actinobacteria secrete siderophores directly to bind with ferric iron before uptake. Siderophores also act as a biocontrol agent for indirect mechanisms. With a higher affinity for iron than fungal pathogens, siderophores from biocontrol actinobacteria outcompete pathogens causing insufficient iron necessary for phytopathogen proliferation (Glick 2012). Siderophores have been detected from Streptomyces species isolated from mycorrhiza by observing yellow-orange halo around the colony. Unfortunately, the determination of siderophore types was not investigated in the paper published (Mohandas et al. 2013; Battini et al. 2016). The only report by Lasudee et al. (2018) determined the type of siderophore produced by actinobacteria isolated from F. mosseae spores and it comes out as hydroxamate and catecholate type siderophores.

10.3.2 Biocontrol Activities of Endophytic Actinobacteria Actinobacteria can also promote plant growth via indirect mechanisms as biocontrol agents as summarized in Table 10.3. Several actinobacteria associated with mycorrhizal spores have been reported to suppress the growth of plant pathogens (Bharadwaj et al. 2008b; Mohandas et al. 2013; Poovarasan et al. 2013). For example, Streptomyces and Leifsonia species isolated from G. mosseae inhibited Fusarium oxysporum (guava wilt) and Alternaria solani (early blight of tomato) up to 96.4– 98.8% that is possible by the production of chitinase to degrade fungal cell wall. (Mohandas et al. 2013). Other hydrolytic enzymes such as amylase, cellulase, lipase, and protease were also reported from Streptomyces spp. and L. poae from G. mosseae (Poovarasan et al. 2015). Later, the similar set of actinobacteria was found to inhibit Xanthomonas axonopodis pv punicae (bacterial blight disease) as studied by (Poovarasan et al. 2013). Actinobacteria isolated from G. moseae or G. intraradices such as Arthrobacter spp., Micrococcus spp., and Cellulomonas flavigena exhibited antagonistic activity against Rhizoctonia solani (damping-off, cutting

10 Endophytic Actinobacteria Associated …

237

Table 10.3 Biocontrol activities of endophytic actinobacteria from mycorrhizal spores Mycorrhiza

Taxa

Biocontrol activities

Glomus macrocarpum

Streptomyces spp. Nocardia spp.

• Chitinase activity Ames et al. (1989) • Antimicrobial activity

References

Streptosporangium Streptoverticillium Intrasporangium Norcardiodes

• Chitinase activity

Glomus mosseae or Glomus intraradices

Arthrobacter spp. Micrococcus spp. Cellulomonas flavigena

Inhibition of Rhizoctonia solani

Bharadwaj et al. (2008b)

Glomus mosseae

Streptomyces fradiae Streptomyces avermitilis Streptomyces cinnamonenesis Streptomyces canus Leifsonia poae

• Chitinase activity • Hydrolytic enzymes (chitinase, cellulose, amylase, protease, and lipase) • Antifungal activity (Fusarium oxysporum and Alternaria solani) • Antibacterial activity against Xanthomonas axonopodis pv punicae

Mohandas et al. (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

Streptomyces netropis Streptomyces scabies Streptomyces griseus Streptomyces violarus Streptomyces albidoflavus

• Chitinase activity • Hydrolytic enzymes (chitinase, cellulose, amylase, protease, and lipase)ara>

Poovarasan et al. (2015)

decay, stem girdling, and aerial blight). The potential antagonistic isolates were identified as Arthrobacter oxydans, Cellulomonas flavigena, and Micrococcus kristinae (Bharadwaj et al. 2008b). Earlier, Streptomyces spp. and Nocardia sp. isolated from G. macrocarpum showed antibacterial activity against 11 tested bacteria including rhizobia and fluorescent Pseudomonas sp. and six fungi (Ames et al. 1989).

10.3.3 Phytohormone Production by Endophytic Actinobacteria Actinobacteria from mycorrhizal spores can produce phytohormones as summarized in Table 10.4. In vitro, actinobacteria produced IAA in tryptophan supplemented culture broth for the synthesis of IAA (Spaepan and Vanderleyden 2011). Streptomyces species produced IAA at a varying quantity of 4.44–11.12 µg/ml. S. thermocarboxydus isolate S3 isolated from F. mosseae CMU-RYA08 produced the

• Streptomyces thermocarboxydus isolate S3 IAA

IAA

• • • •

Funneliformis mosseae CMU-RYA08

Streptomyces thermocarboxydus isolate 48 Streptomyces spinoverrucosus isolate S1 Streptomyces pilosus isolate S4 Streptomyces pilosus isolate S4-1

• Curtobacterium luteum isolate M060824-7 ND • Mycobacterium mucogenicum M060824-8

Gigaspora margarita MAFF 520054 spores

IAA

Streptomyces spp.

IAA

Streptomyces avermitilis

Rhizophagus intraradices isolate IMA6

IAA and gibberellin

Streptomyces fradiae Streptomyces cinnamonenesis Streptomyces canus Leifsonia poae

Glomus mosseae

Hormone production

Taxa

Mycorrhiza

Table 10.4 Plant growth-promoting activities of endophytic actinobacteria from mycorrhizal spores

• Promotion of mung beans (Vigna radiata) growth • Promotion of rice (Oryza sativa) growth in low nutritional soil under induced drought stress

ND

• Promotion of alfafa (Medicago sativa) growth

ND

• Promotion of growth of guava (Psidium guajava L.) • Promotion of pomegranate (Punica granatum L.cv Bhagwa) growth

• Promotion of growth of guava (Psidium guajava L.) • Promotion of pomegranate (Punica granatum L.cv Bhagwa) growth

Plant growth-promoting activities

Lasudee et al. (2018)

Long et al. (2017)

Battini et al. (2016)

Mohandas et al. (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

References

238 K. Lasudee et al.

10 Endophytic Actinobacteria Associated …

239

maximum IAA of 11.12 µg/ml (Lasudee et al. 2018). In addition, Leifsonia poae associated with Glomus mosseae produced IAA at 8.3 µg/ml (Mohandas et al. 2013). Similarly, Gibberellin (GA) is another plant hormone stimulating stem elongation, bolting, and flowering (Hamadi and Mohammadipanah 2015). Various species such as S. fradiae, S. cinnamonenesis, S. canus, and L. poae isolated from Glomus mosseae were reported to produce gibberellin in culture broth with the maximum GA of 12 µg/ml. reported by S. canus (Mohandas et al. 2013).

10.4 Beneficial Effects of Endophytic Actinobacteria on Plant Actinobacteria can promote plant growth by their ability to produce plant growth regulators. Several endophytic actinobacteria were reported to produce plant growth regulators such as IAA or siderophores in vitro as a result of these can promote plant growth under controlled environmental conditions (El-Tarabily et al. 2009; Mohandas et al. 2013). Mohandas et al. 2013 tested five actinobacteria associated with G. mosseae namely S. fradiae, S. avermitilis, S. cinnamonensis, S. canus, and L. poae for growth promotion of guava (Psidium guajava L.). Except for S. fradiae all of them increased height, leaf area, fresh weight, and dry weight of 10 months guava seedlings. Also, these actinobacteria promoted the growth of pomegranate, increased shoot and root length, leaf area, and total biomass in 6-month-old seedlings (Poovarasan et al. 2013). S. canus, increased dry weight over control possibly by its ability to produce growth hormones IAA and GA3 in vitro. Endophytic actinobacteria from Gigaspora margarita spores have recently been reported to promote the growth of alfalfa (Medicago sativa) seedlings. Similarly, Curtobacterium luteum M0608247 and Mycobacterium mucogenicum M060824-8 enhanced fresh and dry weight of leaf/stem and root fresh weight of alfalfa seedlings. Besides, these two actinobacteria also increased AMF colonization in alfalfa root (Long et al. 2017). Funneliformis belongs to a member of AMF in the family Glomeraceae, which form symbiotic relationships with many angiosperm plant roots. It was formerly known as Glomus mosseae until the genus Funneliformis was established in the year 2010 with F. mosseae as a type species (Schubler and Walker 2010). Being its wide occurrence and richness of literature, F. mosseae widely used as bioinoculant (Kruger et al. 2012). Its symbiosis with host plants improves the nutrient uptake and provides AM fungi with carbon sources (Rouphael et al. 2015; Wang et al. 2017; Begum et al. 2019). In the authors’ laboratory, S. thermocarboxydus spp have been isolated from F. mosseae spores (Fig. 10.1). The isolate S3 exhibited as plant growth-promoting bacteria due to its ability to produce IAA, ACC deaminase, and siderophore and solubilize insoluble phosphate. Interestingly, this species grew at a low water activity (aw 0.919) and was able to produce IAA under such conditions in vitro (Lasudee et al. 2018). Mung bean (Vigna radiata) inoculated with S. thermocarboxydus isolate S3

240

K. Lasudee et al.

Fig. 10.1 Spores of arbuscular mycorrhiza, Funneliformis mosseae; a under stereo microscope, b under light microscope (100x)

showed an increase in fresh weight, root and shoot length. Intense roots were also observed in both treatments. These results suggested that the beneficial effects on mung bean were responsible due to IAA production by S. thermocarboxydus isolate S3. IAA is known for its effect on the production of lateral roots and the promotion of root length (Etesami et al. 2015). Interestingly, under drought and low nutrient soil, S. thermocarboxydus isolate S3 can promote the growth of Thai jasmine rice (Oryza sativa) KDML105. This world-famous rice variety is sensitive to drought (Cha-um et al. 2010). After 46 d S. thermocarboxydus isolate S3 mitigated adverse effects of rice plants under induced drought conditions as observed in enhancement of the root, stem, total length, and dry weight which were higher than control plants (Fig. 10.2). Besides, S. thermocarboxydus isolate S3 benefited the physiological conditions of the rice plants as exemplified by increased in total chlorophyll and proline contents. Proline accumulation was proposed as one of the mechanism of drought tolerance in rice (Pandey and Shukla 2015). S. thermocarboxydus isolate S3 also maintain high relative water content (RWC) in inoculated leaves under drought conditions as shown in Fig. 10.3. The rice plants in the control treatment were withered and did not survive, whereas, in the treatment with S. thermocarboxydus isolate S3, some plants were still green at the end of the experiment. These positive effects on Thai jasmine rice (Oryza sativa) KDML105 are likely the effect of inoculation of S. thermocarboxydus isolate S3 which showed long-term effect as this isolate was re-isolated from rice roots (Lasudee et al. 2018). This finding suggested that S. thermocarboxydus isolate S3 could survive and live within the root tissues of rice. The beneficial effects of S. thermocarboxydus isolate S3 inoculation suggested to be a result of its PGP properties, in particular ACC deaminase activity and IAA production. Mycelium of S. thermocarboxydus isolate S3 was also observed on rice root as shown in Fig. 10.4. The observation of these typical filamentous cells of Streptomyces on the root surface and detection of S. thermocarboxydus isolate S3 from the root tissues strongly

10 Endophytic Actinobacteria Associated …

241

Fig. 10.2 Growth promotion of Thai jasmine rice (O. sativa) KDML105 by S. thermocarboxydus isolate S3 under drought conditions. a root, stem and total length; b dry weight, chlorophyll content; c proline content

Fig. 10.3 Thai jasmine rice (O. sativa) KDML105 inoculated with S. thermocarboxydus isolate S3 under drought. 1a isolate S3; 2a control; b root of inoculated rice; c root of uninoculated rice

indicated that this isolate was able to colonize rice roots. Similar results of bacterial colonization in rice roots have been reported (Etesami et al. 2014; Qin et al. 2017). This root colonization is an important factor in both plant growth-promoting activities and the survival of bacteria under drought conditions(Gontia-Mishra et al. 2016).

242

K. Lasudee et al.

Fig. 10.4 Photomicrograph of S. thermocarboxydus isolate S3 colonization surface of Thai jasmine rice (O. sativa) KDML105 under light compound microscope (100x)

10.5 Conclusions Based on the data from previous literature and our laboratory, it is evident that endophytic actinobacteria exist inside several species of arbuscular mycorrhizal spores. Several cultivable taxa have been isolated comprising Streptomyces as the most dominant genus. These actinobacteria exhibit plant growth-promoting properties in vitro and planta. S. thermocarboxydus isolate S3 was successfully isolated as an endophyte of F. mosseae spores. This endophytic Streptomyces showed potential to support the growth of Thai jasmine rice KDML105 under drought by improving nutrient uptake possibly through the production of IAA, siderophores, and phosphate solubilization. Other Streptomyces also efficiently suppressed the growth of important plant pathogens. The ability of actinobacteria from mycorrhizal spores to control plant pathogens and produce plant growth-promoting agents supports the possibility of using these actinobacteria for sustainable agriculture. The potential of non-filamentous or rare actinobacteria is yet to be explored to their full potential. The development of new or improved isolation methods is in urgent need to tap into the complete diversity of endophytic actinobacteria within mycorrhizal spores. Thus the role of these endophytic actinobacteria on their mycorrhizal host remains to be clarified which merits future investigation.

10 Endophytic Actinobacteria Associated …

243

References Ames RN, Mihara KL, Bayne HG (1989) Chitin-decomposing actinomycetes associated with a vesicular-arbuscular mycorrhizal fungus from a calcareous soil. New Phytol 111:67–71. https:// doi.org/10.1111/j.1469-8137.1989.tb04219.x Anjum SA, Xie X-Y, Wang L-C, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6(9):2026–2032. https:// doi.org/10.5897/AJAR10.027 Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clement C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 80(1):1–43. https://doi.org/10.1128/MMBR.00019-15 Battini F, Cristani C, Giovannetti M, Agnolucci M (2016) Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol Res 183:68–79. https://doi.org/10.1016/j.micres. 2015.11.012 Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068 Behera BC, Singdevsachan SK, Mishra RR, Dutta SK, Thatoi HN (2014) Diversity, mechanism and biotechnology of phosphate solubilizing microorganisms in mangrove-A review. Biocatal Agric Biotechnol 3(2):97–110. https://doi.org/10.1016/j.bcab.2013.09.008 Bharadwaj DP, Lundquist P-O, Perrsson P, Alström S (2008a) Arbuscular mycorrhizal fungal sporeassociated bacteria affect mycorrhizal colonization, plant growth and potato pathogens. Soil Biol Biochem 40:2494–2501. https://doi.org/10.1016/j.soilbio.2008.06.012 Bharadwaj DP, Lundquist P-O, Perrsson P, Alström S (2008b) Evidence for specificity of cultivable bacteria associated with arbuscular mycorrhizal fungal spores. FEMS Microbiol Ecol 65:310– 322. https://doi.org/10.1111/j.1574-6941.2008.00515.x Bhatti AA, Haq S, Bhat RA (2017) Actinomycetes benefaction role in soil and plant health. Microb Pathog 111:458–467. https://doi.org/10.1016/j.micpath.2017.09.036 Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62(8):3005–3010 Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. https://doi.org/10.1146/annurev.micro.091208.073504 Chaiya L, Matsumoto A, Wink J, Inahashi Y, Risdian C, Pathom-aree W, Lumyong S (2019) Amycolatopsis eburnea sp. nov., an actinomycete associated with arbuscular mycorrhizal fungal spores. Int J Syst Evol Microbiol 69(11):3603–3608. https://doi.org/10.1099/ijsem.0.003669 Cha-um S, Yooyongwech S, Supaibulwatana K (2010) Water deficit stress in the reproductive stage of four indica rice (Oryza sativa L.) genotypes. Pak J Bot 42:3387–3398 Dinesh R, Srinivasan V, Sheeja TE, Anandaraj M, Srambikkal H (2017) Endophytic actinobacteria: diversity, secondary metabolism and mechanisms to unsilenced biosynthetic gene clusters. Crit Rev Microbiol 43(5):546–566. https://doi.org/10.1080/1040841X.2016.1270895 Eke P, Kumar A, Sahu KP, Wakam LN, Sheoran N, Ashajyothi M, Patel A, Fekam FB (2019) Endophytic bacteria of desert cactus (Euphorbia trigonas Mill) confer drought tolerance and induce growth promotion in tomato (Solanum lycopersicum L.). Microbiol Res 228:126302. http://doi.org/10.1016/j.micres.2019.126302 El-Tarabily KA, Nassar, AH, Hardy GEStJ, Sivasithamparam K (2009) Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J Appl Microbiol 102:13–26. doi:https://doi.org/10.1111/j.1365-2672.2008.039 26.x Etesami H, Hosseini HM, Alikhani HA (2014) Bacterial biosynthesis of 1-aminocyclopropane-1caboxylate (ACC) deaminase, a useful trait to elongation and endophytic colonization of the roots

244

K. Lasudee et al.

of rice under constant flooded conditions. Physiol Mol Biol Plants 20(4):425–434. https://doi. org/10.1007/s12298-014-0251-5 Etesami H, Alikhani HA, Hosseini HM (2015) Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents. MethodsX 2:72–78. https://doi.org/10.1016/j.mex.2015.02.008 Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147. https://doi.org/10. 3389/fpls.2017.01147 Food and Agricultural Organization of the United Nation (2018) The impact of disasters and crises on agriculture and food security 2017. Available via http://www.fao.org/3/I8656EN/i8656en.pdf. Accessed 24 Dec 2019 Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x Gasmi M, Kitouni M, Carro L, Pujic P, Normand P, Boubakri H (2019) Chitinolytic actinobacteria isolated from an Algerian semi-arid soil: development of an antifungal chitinase-dependent assay and GH18 chitinase gene identification. Ann Microbiol 69:395–405. https://doi.org/10/1007/s13 213-018-1426-z Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15. http://dx.doi.org/106064/2012/963401 Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Amelioration of drought tolerance in wheat by the interaction of plant growth-promoting rhizobacteria. Plant Biol 18:992–1000. https://doi. org/10.1111/plb.12505 Hamadi J, Mohammadipanah F (2015) Biotechnological application and taxonomical distribution of plant growth promoting actinobacteria. J Ind Microbiol Biotechnol 42(2):157–171. https://doi. org/10.1007/s10295-014-1537-x Kruger M, Kruger C, Walker C, Stockinger H, Schubler A (2012) Phylogenetic reference data of systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984. https://doi.org/10.1111/j.1469-8137.2011.03962.x Lasudee K, Tokuyama S, Lumyong S, Pathom-aree W (2017) Mycorrhizal spores associated Lysobacter soli and its plant growth promoting activity. Chiang Mai J Sci 44(1):94–101 Lasudee K, Tokuyama S, Lumyong S, Pathom-aree W (2018) Actinobacteria associated with arbuscular mycorrhizal Funneliformis mosseae spores, taxonomic characteriazation and their beneficial traits to plants: evidence obtaind from mung bean (Vigna radiata) and Thai jasmine rice (Oryza sativa). Front Micorbiol 9:1247. https://doi.org/10.3389/fmicb.2018.01247 Lee P-J, Koske RE (1994) Gigaspora gigantea: parasitism of spores by fungi and actinomycetes. Mycol Res 98(4):458–466 Liotti RG, da Silva Figueiredo MI, Soares MA (2019) Streptomyces griseocarneus R132 controls phytopathogens and promotes growth of pepper (Capsicum annuum). Biol Control 138:104065. https://doi.org/10.1016/j.biocontrol.2019.104065 Long L, Lin Q, Yao Q, Zhu H (2017) Population and function analysis of cultivable bacteria associated with spores of arbuscular mycorrhizal fungus Gigaspora margarita. 3Biotech 7:8. https://doi.org/10.1007/s13205-017-0612-1 Manfeld-Giese K, Larsen J, Bodker L (2002) Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol 41:133–140. https:// doi.org/10.1111/j.1574-6941.2002.tb00974.x Mohandas S, Poovarasan S, Panneerselvam P, Saritha B Upreti KK, Kamal R, Sita T (2013) Guava (Psidium guajava L.) rhizaphere Glomus mosseae spores harbor actinomycetes with growth promoting and antifungal attributes. Sci Hortic 150:371–376. https://doi.org/10.1080/01448765. 2012.741108 Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197. https://doi.org/10.1007/s11274-017-2364-9

10 Endophytic Actinobacteria Associated …

245

Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorus. Appl Soil Ecol 86:41–54. https:// doi.org/10.1016/j.apsoil.2014.09.012 Pandey V, Shukla A (2015) Acclimatization and tolerance strategies of rice under drought stress. Rice Sci 22:147–161. https://doi.org/10.1016/j.rsci.2015.04.001 Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbiosis. Nature Rev Microbiol 6:763–775. https://doi.org/10.1038/nrmicro1987 Poovarasan S, Mohandas S, Paneerselvam P, Saritha B, Ajay KM (2013) Mycorrhizae colonizing actinomycetes promote plant growth and control bacterial blight disease of pomegranate (Punica granatum L. cv Bhagwa). Crop Prod 53:175–181. https://doi.org/10.1016/j.croppro.2013.07.009 Poovarasan S, Mohandas S, Sita T (2015) Functional characterization of actinomycetes isolated from the AM fungal (Glomus mosseae) spores. Int J Curr Microbiol Appl Sci 4(9):598–612 Qin S, Feng WW, Wang TT, Ding P, Xing K, Jiang JH (2017) Plant growth-promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp. KLBMP5084 isolated from halophyte Limonium sinense. Plant Soil 416:117–132. https://doi.org/10.1007/s11104-0173192-2 Roesti D, Ineichen K, Braissant O, Redecker D, Wiemken A, Aragno M (2005) Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl Environ Microbiol 71(11):6673–6679. https://doi.org/10.1128/AEM.71.11.6673-6679.2005 Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, De Pascale S, Bonini P, Colla G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hort 196:91–108. https://doi.org/10.1016/j.scienta.2015.09.002 Sathya A, Vijayabhharathi R, Gopalakrishnan S (2017) Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7:102. https://doi.org/10.1007/s13205-017-0736-3 Schrey SE, Erkenbrack E, Fruh E, Fengler S, Hommel K, Horlacher N, Schulz D, Ecke M, Kulik A, Fiedler HP, Hampp R, Tarkka MT (2012) Production of fungal and bacterial growth modulating secondary metabolites is widespread among mycorrhiza-associated streptomycetes. BMC Microbiol 12:146. https://doi.org/10.1186/1471-2180-12-164 Schubler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. CreateSpace Independent Publishing Platform, Gloucester Singh DP, Patil HJ, Prabha R, Yandigeri MS, Prasad SR (2018) Actinomycetes as potential plant growth-promoting microbial communities. In: Prasad R, Gill SS, Tuteja N (eds) New and future developments in microbial biotechnology and bioengineering: Crop improvement through microbial biotechnology. Elsevier, pp 27–38 Singh R, Dubey AK (2018) Diversity and applications of endophytic actinobacteria of plants in special and other ecological niches. Front Microbiol 9:1767. https://doi.org/10.3389/fmicb.2018. 01767 Singh SP, Gaur R (2016) Evaluation of antagonistic and plant growth promoting activities of chitinolytic endophytic actinomycetes associated with medicinal plants against Sclerotium rolfsii in chickpea. J Appl Microbiol 121:506–518. https://doi.org/10.111/jam.13176 Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/ 10.1146/annurev-arplant-042110-103846 Spaepan S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3(4):a001438. https://doi.org/101101/cshperspect.a001438 Suarez-Moreno ZR, Vinchira-Villarraga DM, Vergara-Morales DI, Castellanos L, Ramos FA, Guarnaccia C, Degrassi G, Venturi V, Moreno-Sarmiento N (2019) Plant-growth promotion and biocontrol properties of three Streptomyces spp. isolates to control bacterial rice pathogens. Front Microbiol 10:290. https://doi.org/10.3389/fmicb.2019.00290 van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10. 1111/nph.13288

246

K. Lasudee et al.

Vurukonda SSKP, Giovanardi D, Stefani E (2018) Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int J Mol Sci 19:952. https://doi.org/10.3390/ijms19040952 Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24. https:// doi.org/10.1016/j.micres.2015.12.003 Walley FL, Germida JJ (1996) Failure to decontaminate Glomus clarum NT4 spores is due to spore wall-associated bacteria. Mycorrhiza 6:43–49. https://doi.org/10.1007/s005720050104 Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E (2017) Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol Plant 10:1147–1158. https://doi.org/10.1016/j.molp.2017.07.012 Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478. https://doi.org/10.1016/S0038-0717(03)000 03-8

Chapter 11

Endophytes as Plant Nutrient Uptake-Promoter in Plants Carlos García-Latorre, Sara Rodrigo, and Oscar Santamaría

Abstract Endophytic fungi, while living asymptomatically within plants, may confer competitive advantages such as resistance against biotic and abiotic stresses. Among them, the improvement in plant nutrient uptake is a phenomenon that has been explored for its potential use in agriculture, especially considering the need for a more sustainable farming model that integrates soil regeneration cycle and mitigation of the climate change effects. The utilization of fungal endophytes may enhance the absorption of macro and micronutrients for a wide diversity of plant species, which may reduce the application of chemical fertilizers. The processes involved in this higher nutrient uptake range from (i) the production of phytochemicals-like substances that favor root growth and increase mass flow or root interception of nutrients, (ii) by production of siderophores that bind Fe3+ , (iii) performing beneficial interaction with other soil organisms (iv) the interception of nutrients via hyphae, and (v) due to the secretion of substances such as hydrolytic enzymes that increase nutrient solubilization. These effects may counter multiple benefits to plants growing under stressful conditions. The main role of endophytes in mineral nutrient uptake in plants has been elucidated. Keywords Fungal endophytes · Nutrient uptake · Biotic and abiotic stress

11.1 Introduction Fungal endophytes are an important group of plant microbes living asymptomatically and sometimes systemically within plant tissues (Carroll 1991; Hardoim

C. García-Latorre · S. Rodrigo School of Agricultural Engineering. Institute of Dehesa Research, University of Extremadura, Avda., Adolfo Suárez s/n 06007 Badajoz, Spain O. Santamaría (B) Department of Construction and Agronomy, University of Salamanca, Avenida Cardenal Cisneros 34, 49029 Zamora, Spain e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_11

247

248

C. García-Latorre et al.

et al. 2015). Initially, it was presumed that endophytic fungi only colonized aboveground plant tissues (leaves, stems, bark, petioles, and reproductive structures), which distinguished them from mycorrhizal fungi. Later, numerous studies nowadays have demonstrated that fungal endophytes may also inhabit root tissues (Huang et al. 2019; Li et al. 2019; Strom et al. 2019; Yamaji et al. 2016). Overall, endophytic fungi are ubiquitous and extremely diverse in host plants; in fact, every plant examined with this purpose has been found to harbor at least one species of endophytic fungus (Arnold et al. 2000; Saikkonen et al. 2000). Furthermore, it is interesting to note that such a high diversity, i.e. more than 100 different species can be found in a single plant species (Sánchez et al. 2012). Researches on fungal endophytes have increased in recent years and an increasing number of studies exhibited the beneficial effects of diverse endophyte species on their plant hosts. Several endophytes have been shown to confer resistance to plants against herbivores and phytopathogens (Clay and Schardl, 2002; Rodrigo et al. 2017; Romeralo et al. 2015), to improve the nutritional status of the plant host (Lledó et al. 2016), and its competitiveness toward other plant species (Vázquez de Aldana et al. 2013), to increase its photosynthetic efficiency (Spiering et al. 2006), antioxidant capacity (Hamilton and Bauerle 2012) and increase plant adaptation to stressful habitats such as of drought (Giauque and Hawkes 2013), salinity (Redman et al. 2011), and heavy metals (Zamani et al. 2015). These studies provide pieces of evidence regarding the important role played by endophytes in the adaptation and survival of plants even under stressful habitats and conditions. The endophytes have been identified as an important source of novel and diverse active secondary metabolites of great scientific and industrial interest (Brader et al. 2014; Dheeman et al. 2017; Schulz et al. 2002; Surup et al. 2018). These active metabolites, often involved in the beneficial effects observed in plant hosts, might confer their adaptation capacity toward stressful conditions, and their resistance in adverse field conditions. For instance, metabolites produced by Penicillium citrinum Thom isolated from Ixeris repens (L.) A.Gray, when applied in Carex kobomugi Ohwi showed better growth, higher chlorophyll and carotenoids content, as well as higher efficiency in carboxylation and the water use (Hwang et al. 2011).

11.2 Enhancing Plant Nutrient Uptake In the last decades of the twentieth century, the importance of soil as a basic environmental component has been highlighted, recognizing that soil is a nonrenewable resource that virtually needs time for its regeneration or nutrients replacement (Nortcliff 2002). Sustainable soil management practices are essential for maintaining proper soil health for the future production of crops. However, the intensification of the cropping systems, which is causing salinization in many soils especially in arid and semi-arid regions (Khan et al. 2005), and climate change (reducing the amount of available water for crops) are contributing to the soil quality deterioration and decreasing the availability of the nutrients for plants. Under this scenario, the

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

249

design of agricultural systems that aims to reduce inputs of chemicals and using the endophyte microbes to maximize the efficiency of such resources might be of great importance (Maheshwari 2017; Tilman et al. 2002). Thus, the endophytic fungi that enhance the nutrient uptake by their plant hosts (Lledó et al. 2015) could play an important role in more sustainable agriculture systems. This may allow reducing the number of chemical fertilizers for enhancing plant growth, and consequently productivity (Silveira and Kohmann 2020), or by improving food or feed nutritional quality by increasing the concentration of some minerals in the edible parts, especially when considering the requirement of some essential minerals for animals and humans, such as I, Fe, Zn, and Se, that usually present deficiency (Graham et al. 2007; White and Broadley 2005). As supporting knowledge for the eventual use of endophytes with that purpose, several studies have reported the enhancement of the nutrient uptake in plants caused by endophytes, as summarized in Table 11.1. The endophyte Epichloë festucae Leuchtm., Schardl and Siegel has been found to increase the uptake of P, N, Zn, Ca, or Mg by Festuca rubra L. plants (Vázquez de Aldana et al. 2013; Zabalgogeazcoa et al. 2006) and accumulation of Mn by Lolium perenne L. in its herbage (Soto-Barajas et al. 2016). Other endophytes belonging to Neotyphodium genus have been reported in increasing the concentration of Zn and Mo in L. perenne (Malinowski et al. 2004) and the concentration of P, Ca, or Zn in Festuca arundinacea Schreb. (Malinowski et al. 2000). According to Lledó et al. (2015), when the endophyte Stemphylium globuliferum (Vestergr.) Simmons was inoculated in Poa pratensis L., its herbage showed higher values in the concentration of Ca (from 0.78 to 0.90 mg/kg), Mg (from 0.31 to 0.36 mg/kg), and Sr (from 68.07 to 77.68 mg/kg) in comparison to that of uninoculated plants. Authors reported a significant increase in the Al, B, Fe, Li, Mo, Ni, and Ti uptake when plants were inoculated with Epicoccum nigrum Link, while the inoculation of Fusarium lateritium Nees in P. pratensis caused an increase in the concentration of Fe, Ni, and Zn in the herbage by 31%, 32%, and 16%, respectively, in comparison with the uninoculated controls. An increase in the Fe uptake by endophyte-infected plants has also been reported by Bartholdy et al. (2001), and Johnson et al. (2013), when studied the influence of Phialocephala fortinii Wang and Wilcox, and Epichloë/Neotyphodium on forest tree species and Lolium perenne, respectively. Also, Phomopsis liquidambari Chang, Jiang, and Chi, a mutualistic rice symbiont, promoted rice growth and grain yield at the same time that significantly reduced the amount of soil N fertilizer required for optimum plant growth (Li et al. 2009; Yuan et al. 2007). Although most of the studies have been focused on grass species hosts, the positive influence of endophytes on the uptake and later accumulation of minerals has also been reported in other host families, such as legumes. Thus, in Ornithopus compressus L. plants, the endophytes Stemphylium sp., Fusarium sp., Sordaria fimicola (Roberge ex Desm.) Ces. and De Not., and Sporormiella intermedia (Auersw.) Ahmed and Cain ex Kobayasi were found to cause a higher accumulation of B, Mo, P, S and Zn in the herbage than in controls (endophyte-free plants) in a study conducted by Santamaria et al. (2017). Likewise, Stemphylium globuliferum caused a higher accumulation of Ca, Cd, Cu, Mn, Pb and Zn (more than 31, 217, 66, 14, 305 and

250

C. García-Latorre et al.

Table 11.1 Summary of the effects on the nutrient uptake produced by endophytic fungi on different plant species Endophyte species

Plant host

Functional effect (nutrient uptake increase)

Reference

Phialocephala fortinii

Pinus contorta Douglas

N, P

Jumpponen et al. (1998)

Trichoderma sp.

Cucumis sativus L.; Fe, Zn, Cu, Mn, Solanum lycopersicum (influence on AM L. fungi)

Yedidia et al. (1999); Nzanza et al. (2012)

Neotyphodium sp.

Festuca arundinacea Schreb

P, Ca, or Zn

Malinowski et al. (2000)

Phialocephala fortinii

In vitro

Fe (siderophores)

Bartholdy et al. (2001)

Neotyphodium sp.

Lolium perenne L.

Zn, Mo

Malinowski et al. (2004)

Epichloë festucae

Festuca rubra L.

P, N, Zn, Ca, Mg

Zabalgogeazcoa et al. (2006); Vázquez de Aldana et al. (2013)

Phomopsis liquidambari

Oryza sativa L.

N Rice growth promoter

Yuan et al. (2007); Li et al. (2009)

Order Helotiales

Deschampsia Antarctica Desvaux

N

Upson et al. (2009)

Epichloë festucae

Lolium perenne L.

Fe

Johnson et al. (2013)

Stemphylium globuliferum

Poa pratensis L.

Ca, Mg, Sr

Lledó et al. (2015)

Epiccocum nigrum

Poa pratensis L.

Al, B, Fe, Li, Mo, Ni, Ti

Fusarium lateritium

Poa pratensis L.

Fe, Ni, Zn

Trichoderma atroviridae and AM 1 fungi (Glomus sp.)

Triticum durum Wesf

Grain Protein, P, K, Fe Leaf N, P, K, Fe, Zn

Colla et al. (2015)

Stemphylium globuliferum

Trifolium subterraneum L.

Ca, Cd, Cu, Mn, Pb, Zn

Lledó et al. (2016)

Order Pleosporales

Trifolium subterraneum L.

K, Pb

Epichloë festucae

Lolium perenne L.

Mn

Soto-Barajas et al. (2016)

Stemphylium sp.

Ornithopus compressus L.

B, Mo, P, S

Santamaría et al. (2017)

Fusarium sp.

Ornithopus compressus L.

B, Mo, P, S, Zn (continued)

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

251

Table 11.1 (continued) Endophyte species

Plant host

Functional effect (nutrient uptake increase)

Sordaria fimicola

Ornithopus compressus L.

B, Mn, Mo, S, Zn

Sporormiella intermedia

Ornithopus compressus L.

B, Mn, Mo, P, S, Zn

DSE 2 endophytes

Solanum lycopersicum N, P, K, Ca, Mg, L. Fe, Mn, Zn

1 AM:

Reference

Vergara et al. (2017)

Arbuscular mycorrhizal fungi; 2 DSE: Dark septate endophyte

60%, respectively in comparison with free-endophyte plants) when it was inoculated in Trifolium subterraneum L. plants cultivated under greenhouse conditions (Lledó et al. 2016). Such effects were dependent on environmental conditions, because when the same endophytic species was inoculated in the parent host T. subterraneum, under field conditions, the increase in the concentration of minerals was recorded in Al, Fe, Pb, and Li (Lledó et al. 2016). In a similar study, in the experiments performed in the field, an endophyte belonging to Pleosporales order named as E244, was found to increase concentration of K (72%) and Pb (225%) when compared to the control (uninfected plants) which inoculated in the aerial tissues of the plant host. On the other hand, the enhancement of nutrient uptake in plants caused by fungal endophytes is mainly achieved indirectly. In the case of Trichoderma spp. in addition to their biocontrol activity, this endophyte can improve the solubility of soil micronutrients such as Fe, Zn, Cu, and Mn, due to its influence on arbuscular mycorrhiza (AM) activity (Yedidia et al. 1999; Nzanza et al. 2012). Thus, in order to understand it more, wheat seeds coated with an AM fungus and Trichoderma atroviride Karst., once cultivated in the field, produced grain with a higher nutritive value in terms of protein, P, K, and Fe (Colla et al. 2015). According to authors, it was probably due to the higher chlorophyll content and the higher photochemical activity of the pigment-protein complex, photosystem II (PSII), besides better nutritional status (higher leaf content of N, P, K, Fe, and Zn) of the wheat plant. On the other hand, a specific group of endophytes named as dark septate endophytes (DSE) has also been observed to cause an enhancement of the mineral uptake in pine seedlings (Jumpponen et al. 1998), by increasing their uptake of P and N in presence of DSE, and in Deschampsia antarctica Desvaux plants inoculated with DSE, which increased their N uptake (Upson et al. 2009). Furthermore, Vergara et al. (2017) reported the potential of DSE fungi to promote the uptake of macro and micronutrients more efficiently, resulting in increased tomato plant growth.

252

C. García-Latorre et al.

11.3 Endophytes Mediated Mechanisms of Action to Enhance Nutrients Uptake Several mechanisms have been proposed to be involved in the enhancement of the mineral uptake by host plant as a consequence of the endophyte infection (Fig. 11.1). The production of substances with plant growth promoting (PGP) properties, such as phytohormone-like substances (i.e. auxins, gibberellins, etc.) and phytochemicals has highly beneficial effects on the growth enhancement of the host plant (Khan et al. 2016). Earlier, Assuero et al. (2006) reported enhancement of root growth which resulted in a greater mineral absorption due to their larger soil colonization and exploration capacity. This finding has also been evidenced by Harman et al. (2004) while observing the effects of Trichoderma species, or by Ferus et al. (2019), who described a higher root growth in red oak seedlings inoculated with the

Fig. 11.1 Main mechanisms involved in the increase of nutrient uptake by endophyte-infected plants

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

253

endophyte Beauveria bassiana (Bals.-Criv.) Vuill. On the other hand, Lledó et al. (2015, 2016) observed genus Penicillium and Chaetosphaeronema increased the total root biomass in Poa pratensis, and Chaetosphaeronema, Sordaria fimicola, and Epicoccum nigrum exhibited a similar effect in Trifolium subterraneum. Studies performed by Bartholdy et al. (2001) and Johnson et al. (2013) stated the enhacement of Fe uptake in plants growth and development. One of the mechanisms of such an effect might be due to the production of siderophores, which strongly bind Fe3+ . This is supported by the fact that several endophytic fungi, such as species of Epichloë/Neotyphodium, contain a non-ribosomal peptide synthetase gene (sidN) encoding a siderophore synthetase (Johnson et al. 2013). Earlier, Altomare et al. (1999) reported the secretion of siderophores by endophyte Trichoderma harzianum Rifai, increasing Fe uptake by their host plants. In general, nutrient uptake in plants through roots is mediated, among others, by mass flow, and/or root interception (Jungk 2002). Mass flow takes place when nutrients are transported to root by the movement of water in the soil, hence any modification in the above or below ground biomass in a plant could affect the nutrient acquisition (White et al. 1997). In plants with a more proliferation of roots, mass flow tends to increase corresponding to increased nutrients uptake due to the presence of endophytic fungi. This fact was reported by Soto-Barajas et al. (2016) in a study conducted with Epichloë endophytes, wherein N, Ca, Mg, S, Mn, and Mo increased in endophyte-infected plant, Lolium perenne. Root interception occurs when nutrients play physical contact with the root surface and thus when a plant-endophyte interaction stimulates larger root biomass, root interception might be positively altered. This interaction can also modify rhizosphere conditions, affecting the presence, survival, or development of different rhizospheric organisms, which in turn may facilitate nutrient uptake (Antunes et al. 2008; Liu et al. 2011; Omacini et al. 2006). Nutrient transfer between many plant-fungal symbioses is a common strategy, where fungal symbionts facilitate the uptake of soil nutrients by plant hosts, and the plant may supply plant-derived carbohydrates to the developing fungus (Kiers et al. 2011). Under this nutrient-transfer perspective, root-associated endophytes were able to mobilize different nutrients via fungal hyphae, thus helping plants in their nutrient uptake (Behie and Bidochka 2014). Usuki and Narisawa (2007) found that the endophyte Heteroconium chaetospira (Grove) Ellis, transfered N to Chinese cabbage plants, and Newsham (2011) stated that Phialocephala fortinii transfered both, N and P from soil to plant roots via fungal hyphae, thus an increase in minerals concentration occurred in plant roots and shoots. Similarly, studies conducted with the ascomycete root-inhabiting endophyte, Colletotrichum tofieldiae (Pat.), demonstrated their role to facilitate the transfer of P to non-mycorrhizal plant hosts via their hyphae (Almario et al. 2017; Hiruma et al. 2016). This fact is especially interesting for plants growing in nutrient-limited conditions. Studies conducted with the fungal endophyte Piriformospora indica Sav. showed its capacity to induce a normal growth of maize plants cultivated under nutrient-stress conditions, by facilitating the transfer of P from soil to plant roots (Yadav et al. 2010). Chen et al. (2013) observed Phomopsis liquidambari causing growth promotion, nitrification, and NH4+ –N release. Further, the fungal endophyte P. indica has been reported stimulating the expression of the

254

C. García-Latorre et al.

gene encoding nitrate reductase, activating also the uptake of trace elements (Mo, B, Fe, Zn, and Mn) in the rhizosphere (Su et al. 2016, 2019). The higher nutrient uptake in endophyte-infected plants occurred due to the endophytic borne secretion of substances that facilitate the mineral uptake by plant roots. In this scenario, Curvularia geniculata (Tracy and Earle) Boedijn has been found to secrete enzymes exhibiting P solubilization in sufficient amounts so as to enhance plant growth and development (Priyadharsini and Muthukumar 2017). On the other hand, the release of root exudates containing some phenolic compounds secreted by Epichloë endophytes, were found to increase the P solubility in soil, increasing the P uptake and the subsequent P concentration in the plants (Malinowski et al. 1998). Similar studies have also reported an increased capability to bind Cu in the rhizosphere of endophyte-infected plants (Malinowski et al. 2004). Increment of P and other mineral solubilization occurred due to the secretion of substances by root endophytes which acidifies the soil, thus P becomes more available in the soil solution by its conversion from insoluble phosphates or other insoluble fertilizers (Aciego and Brookes 2009; Narsian and Patel 2000). Special mention deserves (DSE) which have been found to make mineral nutrients available by facilitating access to complex C, N, and P present in the soil for their host plant (Mandyam 2008). Such an effect could be explained by the production of hydrolytic enzymes by the endophyte, which could induce the release of nutrients to be uptaked by plants. Long back, Jumpponen and Trappe (1998) reported the uptake of organic compounds (amino acids, small peptides, etc.) by DSE fungi, which might be transferred directly to host plants, resulting in more efficient use of organic nutrient resources (Reeve et al. 2008). As stated earlier, DSE and mycorrhizal fungi establish a kind of symbiosis with several plant taxa, where hyphae grow endophytically in roots, extending their mycelia into the soil, to acquire nutrients and to mobilize them to plants (Marschner and Dell 1994). Thus, interactions between DSE and host plants improved plant fitness due to an increment in the N and P transfer and uptake, and nutrient provision to host plants (Gasoni and De Gurfinkel 1997; Usuki and Narisawa 2007). A few of these mechanisms are summarized in Table 11.2. Most of these results have been found to be considerably variable depending on the host plant, fungal strains, and environmental conditions (Haselwandter and Read 1982; Jumpponen 2001; Svenningsen et al. 2018). Thus varying results are obtained under different environmental conditions as observed in rice with Phomopsis liquidambari, where analyzing the transcript levels of several genes in endophyte-infected tissues, it was found that the genes with higher transcript levels, OsAMT1;1, OsAMT1;3, OsAMT2;2, OsAMT3;2, OsAMT3;2 and Os- NRT2;1 increased under low-N conditions (Li et al. 2018).

11.4 Plant Growth Under Alleviation of Stress Conditions The accumulation of mineral salts in soils has become nowadays one of the most serious and growing environmental problems in arid and semi-arid areas causing

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

255

Table 11.2 Summary of the main mechanisms that affect the nutrient absorption by endophyteinfected plants Mechanism of action

Endophyte species

Plant host

Reference

–

Harman et al. (2004)

Neotyphodium coenophialum

Festuca arundinacea Schreb

Assuero et al. (2006)

Chaetosphaeronema sp.

Poa pratensis L.

Lledó et al. (2015)

Chaetosphaeronema sp.

Trifolium subterraneum L.

Lledó et al. (2016)

Sordaria fimicola

Trifolium subterraneum L.

Lledó et al. (2016)

Epiccocum nigrum

Trifolium subterraneum L.

Lledó et al. (2016)

Epichloë festucae

Lolium perenne L.

Soto-Barajas et al. (2016)

Beauveria bassiana

Quercus rubra L.

Ferus et al. (2019)

Trichoderma harzianum

–

Altomare et al. (1999)

Phialocephala fortinii

–

Bartholdy et al. (2001)

Epichloë festucae

Lolium perenne L.

Johnson et al. (2013)

Neotyphodium occultans

Lolium multiflorum L.

Omacini et al. (2006)

Neotyphodium coenophialum

Festuca arundinacea Schreb

Antunes et al. 2008

Neotyphodium lolii

Lolium perenne L.

Liu et al. (2011)

Heteroconium chaetospira

Brassica rapa ssp. pekinensis (Lour.) Hanelt

Usuki and Narisawa (2007)

Piriformospora indica

Zea mays L.

Yadav et al. (2010)

Phialocephala fortinii

–

Newsham (2011)

Metarhizium sp.

Phaseolus vulgaris L.; Panicum virgatum L.; Glycine max L.

Behie and Bidochka, (2014)

Colletotrichum tofieldiae Serendipita indica

Arabidopsis thaliana L.

Hiruma et al. (2016); Almario et al. (2017)

Curvularia geniculata

Cajanus cajan L.

Priyadharsini and Muthukumar (2017)

Neotyphodium coenophialum

Festuca arundinacea Schreb

Malinowski et al. (1998)

Plant root growth Trichoderma sp. promotion

Production of siderophores

Interaction with rhizospheric microorganisms

Nutrient interception via hyphae

Release of root exudates

(continued)

256

C. García-Latorre et al.

Table 11.2 (continued) Mechanism of action

Endophyte species

Plant host

Reference

Aspergillus aculeatus

–

Narsian and Patel (2000);

Neotyphodium sp.

Lolium perenne L.

Malinowski et al. (2004)

Periconia macrospinosa; Microdochium sp.

Grasses and crops

Mandyam (2008)

severe physiological stress, and thus reducing the growth and yield of different crops (Ruiz-Lozano et al. 2012). Salt accumulation into soil reduces the osmotic potential of water, which reduces consequently the nutrient and water uptake by plant roots (Porcel et al. 2016). Phomopsis indica confers salt tolerance to plants by increasing the uptake of nutrients such as N, P, and Ca, or improving K +/Na+ homeostasis (Waller et al. 2005). This action, according to Ghorbani et al. (2019) is regulated by the expression of NHXs, SOS1, and CNGC15 genes, maintaining water status through the regulation in the expression of aquaporins, and diminishing the negative effects of salinity stress. Similarly, Epichloë coenophiala caused a better osmotic adjustment of the grass tiller meristems in infected tall fescue plants during periods of drought, allowing plants a quicker growth after the end of the drought period (Elmi and West 1995). On the other hand, metal pollution in soils has dramatically increased during the last few decades. It is expected to continue in the future, causing important losses in the biodiversity and environmental sustainability (Rozp˛adek et al. 2018). Consequently, through soil–plant interaction, in addition to the negative effects caused by plant fitness and growth, toxic metals accumulate in the food chain, arising severe risks for both human and animals. Under such situation, any investigation aiming to reduce the uptake of toxic metals in plant-degraded lands ecosystem might be really welcome. Deng and Cao (2017) indicated that metal availability for plants is governed by the pseudo-equilibrium between aqueous and solid soil phases rather than by the total metal content. They stated that interactions between root exudates and soil components can prevent the increase of water-soluble organo-metallic chelates in the rhizosphere, suggesting that the organic compounds exuded by roots/microbes rapidly absorbed into soil. With this action, a reduction in water-soluble pools of metals occurred for their availability in plants. Rhizosphere usually suffers changes in biochemical, chemical, and physical properties when compared with the rest of the soil, as a consequence of the release of rhizodeposits by roots and/or the secretion of some chemicals by microbes living in the root zone or adjacent soil (Kumar et al. 2013). In general, rhizosphere microorganisms can increase solubility or change the speciation of metals and metalloids by producing organic ligands. This fact is regulated via microbial decomposition of soil organic matter, exudation of metabolites, and microbial siderophores that can form complex cationic metals or desorb anionic species by ligand exchange. Microbes may immobilize metals such as Cd,

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

257

Cu, Zn, etc., by controlling soil pH (Wenzel 2009). In this context, eukaryotes are more sensitive to metal toxicity in comparison to that of prokaryotes, i.e. bacteria, and their typical mechanisms to regulate metal concentration is the expression of some metal-chelating proteins such as metallothioneins (Durán et al. 2011). The easiest mechanisms for the endophytes to regulate metal uptake by plants could be explained by the extracellular immobilization and/or cell wall binding. Thus, Green and Clausen (2003) observed the use of chelators in immobilizing metals in the soil. Such chelators are mainly organic acids as citrate and oxalate, easily created by fungi (Marina et al. 2019; Odoni et al. 2017). Bilal et al. (2018) co-inoculated Sphingomonas and Paecilomyces formosus and bacteria Sphingomonas sp. in soybean plants; an improvement was observed in plant growth under Al and Zn stresses. The inhibition in the metal uptake and translocation resulted in the enhancement of the nutrients uptake caused by the endophyte and modulate soil extracellular enzymatic activities. Ikram et al. (2018) found the IAA producer endophyte Penicillium roqueforti to increase the uptake of several nutrients, showing a low concentration of heavy metals in shoot and roots when allowed to grow in wastewater. This increase in nutrients uptake by plants growing in contaminated soils was mainly due to their association with endophytes (Khan et al. 2010), which increased the solubility of the nutrients of the soil. DSE fungus Exophiala pisciphila, can accumulate Pb and Cd up to 20% and 5% dry weight, respectively, in the roots (Zhang et al. 2008). This fact is especially interesting in pasture species growing in metal-polluted soils because the accumulation might take place in roots, remaining the aerial part of these plants thus, acted as safe feed to the animals. Thus, the poisoning by lead of the cattle, which is the most reported cause of poisoning in farm livestock (Suttle 2010), might be, at some extent, avoided. Inoculation with Mucor sp. in some plants of Brassicaceae in degraded soils due to heavy metals (van der Ent et al. 2013; Verbruggen et al. 2009) resulted in lower metal accumulation in plant tissues. Facilitating metal transport from the cytosol into the vacuole help in increasing metal tolerance of its plants (Rozpadek et al. 2018). Always depending on the interaction of the symbiont with the environmental conditions (Ahlholm et al. 2002), a large number of fungal endophytes induce growth and development in polluted soils that occurred due to the removal of heavy metals as summarized in Table 11.3. Various workers (Dennis et al. 1998; Soleimani et al. 2010; Soto Barajas et al. 2016) reported that endophytes can be considered as a solution for cropping in heavy metal-polluted areas. Likar and Regvar (2013) showed that Phialophora endophytes allowed Salix plants to live and grow normally in Cdpolluted soils due to the decrease in the metal uptake. Reductions in the Cu uptake by plants were also reported by Zabalgogeazcoa et al. (2006), while Monnet et al. (2001) and Malinowski and Belesky (1999) indicated a decrease of Cu and Al uptake by plants. Lledó et al. (2015, 2016, 2017) reported the endophytic fungus Stemphylium globuliferum to cause a dicrease in the Al content in the aerial biomass of legumes and in the Cr concentration in herbage of P. pratensis when cultivated in greenhouse conditions. However, field experiments with the same endophyte in subterranean clover showed an increase in the Al content in aerial biomass of the plant (Lledó et al. 2016). More consistent results were obtained in case of endophyte Fusarium

258

C. García-Latorre et al.

Table 11.3 Plant growth enhancement under stress conditions mediated by endophytic fungi Stress source

Mechanism

Endophyte species

Plant host

Reference

Piriformospora indica

Oryza sativa L.

Porcel et al. (2016)

Regulation in the expression of aquaporins

Piriformospora indica

Solanum lycopersicum L.

Ghorbani et al. (2019)

Drought tolerance

Osmotic adjustment of the grass tiller meristems

Epichloë coenophiala Festuca Waller et al. arundinacea Schreb (2005)

Waste water

Secretion of IAA; Lower concentration of heavy metals

Penicillium roqueforti Triticum aestivum L.

Ikram et al. (2018)

–

–

Khan et al. (2010)

Heavy metals accumulation as Fusarium oxysporum nanoparticles within intracellular spaces

–

Durán et al. (2011)

Al

Stemphylium globuliferum

Trifolium subterraneum L.

Lledó et al. (2016)

Fusarium lateritium

Trifolium subterraneum L.

Lledó et al. (2016)

Stemphylium globuliferum

Ornithopus compressus L.

Lledó et al. (2017)

Fusarium lateritium

Ornithopus compressus L.

Lledó et al. (2017)

Phialophora sp.

Salix sp.

Likar and Regvar (2013)

Salt tolerance Nutrient uptake increase; K +/Na+ homoeostasis improvement

Contaminated Increase in the soils nutrient solubility of the soil

Mineral uptake decrease

Cd

Mineral uptake decrease

Cd and Pb

Root accumulation Exophiala pisciphila

–

Zhang et al. (2008)

Facilitating metal transport from the cytosol into the vacuole

Brassicaceae

van der Ent et al. (2013); Verbruggen et al. (2009)

Mucor sp.

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

259

lateritium, which caused a decrease in the Al concentration in the aboveground biomass in both greenhouse and field conditions (Lledó et al. 2016). The high Al content in forage is not desirable due to the antagonistic metabolism of Al and P, and the negative effects of Al on lambs’ appetite (Krueger et al. 1984). These findings may allow the use of the forage produced in soils with a high concentration of Al by the livestock more safely.

11.5 Conclusion Although not many studies have exclusively dealt with the enhanced capacity of fungal endophytes-infected plants for nutrients uptake, the available literature revealed promising results in this field. Thus, fungal endophytes have been proved to be a suitable strategy to increase nutrient uptake and to reduce soil metal pollution or salinization due to anthropogenic activities or climate change. Several mechanisms have been proposed for the enhancement of nutrient uptake in the plant caused by endophytes. The secretion of siderophores to bind Fe, the solubilization of P to make it more absorbable by root, or the transport of N via hyphae from soil to roots are well documented. Besides, fungal endophytes can secrete compounds favoring the chelation of heavy metals into soil, avoiding their uptake by plants, as well as the accumulation in the mycelia to help plants living in polluted soils. These findings are considered to resolve the issue of lowering the plant sustainability by the involvement of endophytes in plant nutrients uptake.

References Aciego Pietri JC, Brookes PC (2009) Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil. Soil Biol Biochem. https://doi.org/ 10.1016/j.soilbio.2009.03.017 Ahlholm JU, Helander M, Lehtimäki S, Wäli P, Saikkonen K (2002) Vertically transmitted fungal endophytes: Different responses of host-parasite systems to environmental conditions. Oikos. https://doi.org/10.1034/j.1600-0706.2002.990118.x Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M (2017) Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.1710455114 Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth- promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65:2926–2933 Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman JA (2008) Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct Ecol. https://doi.org/10.1111/j.1365-2435.2008.01432.x Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett. https://doi.org/10.1046/j.1461-0248.2000.00159.x

260

C. García-Latorre et al.

Assuero SG, Tognetti JA, Colabelli MR, Agnusdei MG, Petroni EC, Posse MA (2006) Endophyte infection accelerates morpho-physiological responses to water deficit in tall fescue. New Zeal J Agric Res. https://doi.org/10.1080/00288233.2006.9513726 Bartholdy BA, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals. https://doi.org/10.1023/ A:1016687021803 Behie SW, Bidochka MJ (2014) Nutrient transfer in plant-fungal symbioses. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2014.06.007 Bilal S, Shahzad R, Khan AL, Kang SM, Imran QM, Al-Harrasi A, Yun BW, Lee IJ (2018) Endophytic microbial consortia of phytohormones-producing fungus Paecilomyces formosus lhl10 and bacteria Sphingomonas sp. lk11 to Glycine max l. regulates physio-hormonal changes to attenuate aluminum and zinc stresses. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01273 Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Opin. Biotechnol, Curr. https://doi.org/10.1016/j.copbio.2013.09.012 Carroll GC (1991) Beyond Pest Deterrence—Alternative strategies and hidden costs of endophytic mutualisms in vascular plants. In: Andrews JH, Monano SS (eds) Microbial ecology of leaves. Springer-Verlag, New York, pp 358–378 Chen Y, Ren CG, Yang B, Peng Y, Dai CC (2013) Priming effects of the endophytic fungus Phomopsis liquidambari on soil mineral N Transformations. Microb Ecol. https://doi.org/10. 1007/s00248-012-0093-z Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. https://dx.doi.org/10.1086/342161 Colla G, Rouphael Y, Bonini P, Cardarelli M (2015) Coating seeds with endophytic fungi enhances growth, nutrient uptake, yield and grain quality of winter wheat. Int J Plant Prod. https://doi.org/ 10.22069/ijpp.2015.2042 Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: A review. Chemosphere. https://doi.org/10.1016/j.chemosphere.2016.10.097 Dennis SB, Allen VG, Saker KE, Fontenot JP, Ayad JYM, Brown CP (1998) Influence of Neotyphodium coenophialum on copper concentration in Tall Fescue. J Anim Sci. doi 10(2527/1998):76102687x Dheeman S, Maheshwari DK, Baliyan N (2017) Bacterial endophytes for ecological intensification of agriculture. In: Maheshwari DK (ed) Endophytes: Biology and biotechnology, Springer, Cham, pp 193–231. https://doi.org/10.1007/978-3-319-66541-2_9 Durán N, Marcato PD, Durán M, Yadav A, Gade A, Rai M (2011) Mechanistic aspects in the biogenic synthesis of extracellular metal nanoparticles by peptides, bacteria, fungi, and plants. Microbiol. Biotechnol, Appl. https://doi.org/10.1007/s00253-011-3249-8 Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol. https://doi.org/10.1111/j.1469-8137.1995.tb0 3055.x Ferus P, Barta M, Konôpková J (2019) Endophytic fungus Beauveria bassiana can enhance drought tolerance in red oak seedlings. Trees - Struct Funct. https://doi.org/10.1007/s00468-019-01854-1 Gasoni L, De Gurfinkel BS (1997) The endophyte Cladorrhinum foecundissimum in cotton roots: Phosphorus uptake and host growth. Mycol Res. https://doi.org/10.1017/S0953756296003462 Ghorbani A, Omran VOG, Razavi SM, Pirdashti H, Ranjbar M (2019) Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+ /Na+ homeostasis and water status. Plant Cell Rep. https://doi.org/10.1007/s00 299-019-02434-w Giauque H, Hawkes CV (2013) Climate affects symbiotic fungal endophyte diversity and performance. Am J Bot. https://doi.org/10.3732/ajb.1200568 Graham RD, Welch RM, Saunders DA, Ortiz-Monasterio I, Bouis HE, Bonierbale M, de Haan S, Burgos G, Thiele G, Liria R, Meisner CA, Beebe SE, Potts MJ, Kadian M, Hobbs PR, Gupta RK, Twomlow S (2007) Nutritious Subsistence Food Systems. Agron, Adv. https://doi.org/10.1016/ S0065-2113(04)92001-9

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

261

Green F, Clausen CA (2003) Copper tolerance of brown-rot fungi: Time course of oxalic acid production. Int Biodeterior Biodegrad. https://doi.org/10.1016/S0964-8305(02)00099-9 Hamilton CE, Bauerle TL (2012) A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers. https://doi.org/10.1007/s13225-0120156-y Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: Ecological and evolutionary considerations for defining functioning of Microbial Endophytes. Microbiol Mol Biol Rev. https://doi.org/10.1128/mmbr.000 50-14 Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—Opportunistic, avirulent plant symbionts. Rev. Microbiol, Nat. https://doi.org/10.1038/nrmicro797 Haselwandter K, Read DJ (1982) The significance of a root-fungus association in two Carex species of high-alpine plant communities. Oecologia. https://doi.org/10.1007/BF00389012 Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ, Schulze-Lefert P (2016) Root endophyte Colletotrichum tofieldiae Confers plant fitness benefits that are phosphate status dependent. Cell. https://doi.org/10.1016/ j.cell.2016.02.028 Huang G, Jin Q, Peng H, Zhu T, Ye H (2019) Effect of a fungus, Hypoxylon spp., on endophytes in the roots of Asparagus. FEMS Microbiol Lett FEMS https://doi.org/10.1093/femsle/fnz207 Hwang J-S, You Y-H, Bae J-J, Khan SA, Kim J-G, Choo Y-S (2011) Effects of endophytic fungal secondary metabolites on the growth and physiological response of Carex kobomugi Ohwi. J Coast Res. https://doi.org/10.2112/jcoastres-d-10-00090.1 Ikram M, Ali N, Jan G, Jan FG, Rahman IU, Iqbal A, Hamayun M (2018) IAA producing fungal endophyte Penicillium roqueforti Thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils. PLoS One. https://doi.org/10.1371/journal.pone. 0208150 Johnson LJ, Koulman A, Christensen M, Lane GA, Fraser K, Forester N, Johnson RD, Bryan GT, Rasmussen S (2013) An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne. PLoS Pathog. https://doi.org/10.1371/jou rnal.ppat.1003332 Jumpponen A (2001) Dark septate endophytes—Are they mycorrhizal? Mycorrhiza. https://doi. org/10.1007/s005720100112 Jumpponen A, Trappe JM (1998) Dark septate endophytes: A review of facultative biotrophic root-colonizing fungi. New Phytol. https://doi.org/10.1046/j.1469-8137.1998.00265.x Jungk A (2002) Dynamics of nutrient movement at the soil-root interface. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. CRC Press, New York, pp 455–481 Khan AL, Al-Harrasi A, Al-Rawahi A, Al-Farsi Z, Al-Mamari A, Waqas M, Asaf S, Elyassi A, Mabood F, Shin JH, Lee IJ (2016) Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS ONE. https://doi.org/10.1371/ journal.pone.0158207 Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi—Current perspective. Arch Agron Soil Sci. https://doi.org/10.1080/036503 40902806469 Khan NM, Rastoskuev VV, Sato Y, Shiozawa S (2005) Assessment of hydrosaline land degradation by using a simple approach of remote sensing indicators. Water Manag, Agric. https://doi.org/ 10.1016/j.agwat.2004.09.038 Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. https://doi.org/ 10.1126/science.1208473 Krueger GL, Morris TK, Suskind RR, Widner EM, Berlyne GM (1984) The health effects of aluminum compounds in mammals. Crit Rev Toxicol. https://doi.org/10.3109/104084484090 29320

262

C. García-Latorre et al.

Kumar D, Shivay YS, Dhar S, Kumar C, Prasad R (2013) Rhizospheric flora and the influence of agronomic practices on them: A review. Natl. Acad. Sci. India Sect. B - Biol. Sci, Proc. https:// doi.org/10.1007/s40011-012-0059-4 Li X, He X-L, Zhou Y, Hou Y-T, Zuo Y-L (2019) Effects of dark septate endophytes on the performance of Hedysarum scoparium under water deficit stress. Front Plant Sci. https://doi.org/10. 3389/fpls.2019.00903 Li X, Wang C, Ren CG, Dai CC (2009) Effect of endophytic fungus B3 and different amounts of nitrogen applied on growth and yield in rice (Oryza sativa L.). Jiangsu J Agric Sci 25:1207–1212 Li X, Zhou J, Xu RS, Meng MY, Yu X, Dai CC (2018) Auxin, cytokinin, and ethylene involved in rice N availability improvement caused by Endophyte Phomopsis liquidambari. J Plant Growth Regul. https://doi.org/10.1007/s00344-017-9712-8 Likar M, Regvar M (2013) Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil. https://doi.org/10.1007/s11104-013-1656-6 Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol. https://doi.org/ 10.1111/j.1365-2435.2011.01853.x Lledó S, Rodrigo S, Poblaciones MJ, Santamaria O (2015) Biomass yield, mineral content, and nutritive value of Poa pratensis as affected by non-clavicipitaceous fungal endophytes. Mycol Prog. https://doi.org/10.1007/s11557-015-1093-4 Lledó S, Rodrigo S, Poblaciones MJ, Santamaria O (2016) Biomass yield, nutritive value and accumulation of minerals in Trifolium subterraneum L. as affected by fungal endophytes. Plant Soil. https://doi.org/10.1007/s11104-015-2596-0 Maheshwari DK (2017) Endophytes: Biology and biotechnology. Springer, Gewerbestrasse, Switzerland. ISBN 978-3-319-66541-2 Malinowski DP, Alloush GA, Belesky DP (1998) Evidence for chemical changes on the root surface of fall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil. https://doi.org/10.1023/A:1004331932018 Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil. https://doi.org/10.1023/A:1026518828237 Malinowski DP, Belesky DP (1999) Tall fescue aluminum tolerance is affected by Neotyphodium coenophialum endophyte. J Plant Nutr. https://doi.org/10.1080/01904169909365716 Malinowski DP, Zuo H, Belesky DP, Alloush GA (2004) Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant Soil. https://doi.org/10.1007/s11104-005-2575-y Mandyam K (2008). Dark Septate Fungal Endophytes from a Tallgrass Prairie and their Continumum of Interactions with Host Plants. Kansas State University. Available via https://krex.k-state.edu/ dspace/handle/2097/1127 Accesed 30 Oct 2019 Marina M, Romero FM, Villarreal NM, Medina AJ, Gárriz A, Rossi FR, Martinez GA, Pieckenstain FL (2019) Mechanisms of plant protection against two oxalate-producing fungal pathogens by oxalotrophic strains of Stenotrophomonas spp. Plant Mol Biol. https://doi.org/10.1007/s11103019-00888-w Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil. https://doi.org/ 10.1007/BF00000098 Monnet F, Vaillant N, Vernay P, Coudret A, Sallanon H, Hitmi A (2001) Relationship between PSII activity, CO2 fixation, and Zn. J Plant Physiol, Mn and Mg contents of Lolium perenne under zinc stress. https://doi.org/10.1078/S0176-1617(04)70140-6 Narsian V, Patel HH (2000) Aspergillus aculeatus as a rock phosphate solubilizer. Soil Biol Biochem. https://doi.org/10.1016/S0038-0717(99)00184-4 Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol. https://doi.org/10.1111/j.1469-8137.2010.03611.x Nortcliff S (2002) Standardisation of soil quality attributes. Ecosyst. Environ, Agric. https://doi. org/10.1016/S0167-8809(01)00253-5

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

263

Nzanza B, Marais D, Soundy P (2012) Response of tomato (Solanum lycopersicum L.) to nursery inoculation with Trichoderma harzianum and arbuscular mycorrhizal fungi under field conditions. Acta Agric Scand Sect B Soil Plant Sci. https://doi.org/10.1080/09064710.2011.598544 Odoni DI, van Gaal MP, Schonewille T, Tamayo-Ramos JA, Martins dos Santos VAP, Suarez-Diez M, Schaap PJ (2017) Aspergillus niger secretes citrate to increase iron bioavailability. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01424 Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol. https://doi.org/10. 1111/j.1365-2435.2006.01099.x Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza. https://doi.org/10.1007/s00 572-016-0704-5 Priyadharsini P, Muthukumar T (2017) The root endophytic fungus Curvularia geniculata from Parthenium hysterophorus roots improves plant growth through phosphate solubilization and phytohormone production. Fungal Ecol. https://doi.org/10.1016/j.funeco.2017.02.007 Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: A strategy for mitigating impacts of climate change. PLoS ONE. https://doi.org/10.1371/journal.pone.0014823 Reeve JR, Smith JL, Carpenter-Boggs L, Reganold JP (2008) Soil-based cycling and differential uptake of amino acids by three species of strawberry (Fragaria spp.) plants. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2008.06.015 Rodrigo S, Santamaria O, Halecker S, Lledó S, Stadler M (2017) Antagonism between Byssochlamys spectabilis (anamorph Paecilomyces variotii) and plant pathogens: Involvement of the bioactive compounds produced by the endophyte. Ann Appl Biol. https://doi.org/10.1111/aab.12388 Romeralo C, Santamaría O, Pando V, Diez JJ (2015) Fungal endophytes reduce necrosis length produced by Gremmeniella abietina in Pinus halepensis seedlings. Biol Control. https://doi.org/ 10.1016/j.biocontrol.2014.09.010 Rozp˛adek P, Domka A, Wa˙zny R, Nosek M, J˛edrzejczyk R, Tokarz K, Turnau K (2018) How does the endophytic fungus Mucor sp. improve Arabidopsis arenosa vegetation in the degraded environment of a mine dump? Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2017.11.009 Ruiz-Lozano JM, Porcel R, Azcón C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: New challenges in physiological and molecular studies. J Exp Bot. https://doi.org/10.1093/jxb/ers126 Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography (Cop). https://doi.org/10.1111/j.1600-0587. 2000.tb00292.x Sánchez Márquez S, Bills GF, Herrero N, Zabalgogeazcoa Í (2012) Non-systemic fungal endophytes of grasses. Fungal Ecol. https://doi.org/10.1016/j.funeco.2010.12.001 Santamaria O, Lledó S, Rodrigo S, Poblaciones MJ (2017) Effect of fungal endophytes on biomass yield. Nutritive Value and Accumulation of Minerals in Ornithopus compressus, Microb Ecol. https://doi.org/10.1007/s00248-017-1001-3 Schulz B, Boyle C, Draeger S, Römmert AK, Krohn K (2002) Endophytic fungi: A source of novel biologically active secondary metabolites. Res, Mycol. https://doi.org/10.1017/S09537562020 06342 Silveira ML, Kohmann MM (2020). Maintaining soil fertility and health for sustainable pastures. In: Rouquette M, Aiken GE (eds) Management Strategies for Sustainable Cattle Production in Southern Pastures. Academic Press, pp 35 – 58. https://doi.org/10.1016/B978-0-12-814474-9. 00003-7 Soleimani M, Afyuni M, Hajabbasi MA, Nourbakhsh F, Sabzalian MR, Christensen JH (2010) Phytoremediation of an aged petroleum contaminated soil using endophyte infected and noninfected grasses. Chemosphere. https://doi.org/10.1016/j.chemosphere.2010.09.034

264

C. García-Latorre et al.

Soto-Barajas MC, Zabalgogeazcoa I, Gómez-Fuertes J, González-Blanco V, Vázquez-de-Aldana BR (2016) Epichloë endophytes affect the nutrient and fiber content of Lolium perenne regardless of plant genotype. Plant Soil. https://doi.org/10.1007/s11104-015-2617-z Spiering MJ, Greer DH, Schmid J (2006) Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann Bot. https://doi.org/10.1093/aob/mcl108 Strom N, Hu W, Haarit D, Chen S, Bushley K (2019) Corn and soybean host root endophytic fungi with toxicity towards the soybean cyst nematode. Phytopathology. https://doi.org/10.1094/ PHYTO-07-19-0243-R Su CL, Wang HW, Xie XG, Zhang W, Li XG, Wang XX, Dai CC (2016) Effects of endophytic fungi and Atractylodes lancea powder on rhizosphere microflora and trace elements during continuous peanut cropping. Acta Ecol Sin. https://doi.org/10.5846/stxb201409171842 Su C-L, Zhang F-M, Sun K, Zhang W, Dai C-C (2019) Fungal endophyte Phomopsis liquidambari improves iron and molybdenum nutrition uptake of peanut in consecutive monoculture soil. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-019-0011-2 Surup F, Halecker S, Nimtz M, Rodrigo S, Schulz B, Steinert M, Stadler M (2018) Hyfraxins A and B, cytotoxic ergostane-type steroid and lanostane triterpenoid glycosides from the invasive ash dieback ascomycete Hymenoscyphus fraxineus. Steroids. https://doi.org/10.1016/j.steroids. 2018.03.007 Suttle NF (2010) Mineral nutrition of livestock, 4th edn. CABI Publishing, Wallingford Svenningsen NB, Watts-Williams SJ, Joner EJ, Battini F, Efthymiou A, Cruz-Paredes C, Nybroe O, Jakobsen I (2018) Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. https://doi.org/10.1038/s41396-018-0059-3 Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature. https://doi.org/10.1038/nature01014 Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza. https://doi.org/10.1007/s00572-0090260-3 Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant. Mycologia, Chinese cabbage. https:// doi.org/10.3852/mycologia.99.2.175 van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil. https://doi.org/10.1007/s11104-0121287-3 Vázquez-de-Aldana BR, Zabalgogeazcoa I, García-Ciudad A, García-Criado B (2013) An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species. Plant Soil. https://doi.org/10.1007/s11104-012-1283-7 Verbruggen N, HermansC Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776 Vergara C, Araujo KEC, Urquiaga S, Schultz N, Balieiro F de C, Medeiros PS, Santos LA, Xavier GR, Zilli JE (2017) Dark Septate endophytic fungi help tomato to acquire nutrients from ground plant material. Front Microbiol. https://doi.org/10.3389/fmicb.2017.02437 Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.0504423102 Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil. https://doi.org/10.1007/s11104-008-9686-1 White J, Bacon CW, Hinton DM (1997) Modifications of host cells and tissues by the biotrophic endophyte Epichloe amarillans (Clavicipitaceae. Can J Bot, Ascomycotina). https://doi.org/10. 1139/b97-117 White PJ, Broadley MR (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2005.10.001

11 Endophytes as Plant Nutrient Uptake-Promoter in Plants

265

Yadav V, Kumar M, Deep AK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem. https://doi.org/10.1074/jbc.M110. 111021 Yamaji K, Watanabe Y, Masuya H, Shigeto A, Yui H, Haruma T (2016) Root fungal endophytes enhance heavy-metal stress tolerance of Clethra barbinervis growing naturally at mining sites via growth enhancement, promotion of nutrient uptake and decrease of heavy-metal concentration. PLoS ONE. https://doi.org/10.1371/journal.pone.0169089 Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the Biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061– 1070 Yuan ZL, Dai CC, Li X, Tian LS, Wang XX (2007) Extensive host range of an endophytic fungus affects the growth and physiological functions in rice (Oryza sativa L.). Symbiosis. 43:21–28 Zabalgogeazcoa Í, Ciudad AG, Vázquez de Aldana BR, Criado BG (2006) Effects of the infection by the fungal endophyte Epichloë festucae in the growth and nutrient content of Festuca rubra. Eur J Agron. https://doi.org/10.1016/j.eja.2006.01.003 Zamani N, Sabzalian MR, Khoshgoftarmanesh A, Afyuni M (2015) Neotyphodium Endophyte Changes Phytoextraction of Zinc in Festuca arundinacea and Lolium perenne. Int J Phytoremediation. https://doi.org/10.1080/15226514.2014.922919 Zhang Y, Zhang Y, Liu M, Shi X, Zhao Z (2008) Dark septate endophyte (DSE) fungi isolated from metal polluted soils: Their taxonomic position, tolerance, and accumulation of heavy metals in Vitro. J Microbiol. https://doi.org/10.1007/s12275-008-0163-6

Chapter 12

Endophytic Rhizobacteria for Mineral Nutrients Acquisition in Plants: Possible Functions and Ecological Advantages Becky Nancy Aloo, Vishal Tripathi, Ernest R. Mbega, and Billy A. Makumba

Abstract Nutrient-deficiency in agricultural soils is a major problem in many parts of the world, it is, therefore, artificial fertilizers are widely used to boost crop production. Unfortunately, these fertilizers are associated with a myriad of environmental problems hence, there is a need for viable alternatives. The realization that the plant microbiome can improve plant health, soil fertility, and crop productivity is one of the most fascinating scientific discoveries in the world. For several decades, rhizobacteria have been studied due to their various plant growth-promoting (PGP) traits. Endophytic rhizobacteria are unique plant microbiome that establish themselves within plant root tissues and exert beneficial functions to their hosts without harming them. A lot of emphases have been put on these bacteria as viable tools for sustainable agriculture and it is advanced that they could be better plant growth promoters than their external counterparts. However, this theory is not yet clearly understood. This chapter provides the current state of understanding of the putative functions of endophytic rhizobacteria and their future prospects for plant mineral nutrients acquisition. Their advantageous traits that largely advanced to facilitate these PGP functions are also discussed. Such informations can provide better opportunities for improved plant mineral nutrients acquisition and enhance the application of these microbes as viable strategies for sustainable agriculture. Keywords Endophytes · Rhizobacteria · Sustainable agriculture · Plant growth promotion B. N. Aloo (B) · E. R. Mbega Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, P. O. Box 447, Arusha, Tanzania e-mail: [email protected] B. N. Aloo Department of Biological Sciences, University of Eldoret, P. O. Box 1125-30100, Eldoret, Kenya V. Tripathi Institute of Environment and Sustainable Development, Banaras Hindu University, P. O. Box 221005, Varanasi, UP, India B. A. Makumba Department of Biological Sciences, Moi University, P. O. Box 3900-30100, Eldoret, Kenya © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_12

267

268

B. N. Aloo et al.

12.1 Introduction Agricultural activities are quickly gaining momentum to feed the rapidly growing population across the globe. One of them is excessive use of chemicals established as an effective tool to increase crop productivity of different crops. However, conventional agricultural practices have a lot of undesirable outcomes as the chemical inputs have commonly been linked to land degradation, environmental pollution, global warming, climate change, etc. (Steffen et al. 2015; Di Benedetto et al. 2017). For many decades, researchers all over the world have focused on alternative crop fertilization mechanisms such as the use of plant growth-promoting bacteria (PGPB) to replace the contemporary fertilization practices (Smith et al. 2016). In fact, these are free-living bacteria with unique capabilities of stimulating plant growth, either directly or indirectly through different mechanisms (Archana et al. 2013; Ahemad and Kibret 2014; Kumar et al. 2014). Glick (2014) and later, Baliyan et al. (2018) described the exploitation of such organisms as a viable and environment friendly technology befitting for sustainable crop production in eco-safe ways. Among them, endophytes are organisms that spend all or part of their lives in plant cells or tissues with different degrees of dependence without harming their hosts (Compant et al. 2010; Hardoim et al. 2015; Brader et al. 2017; Lata et al. 2019) and can be recovered from surface-sterilized plant tissues (Santoyo et al. 2016). As many plant species as exist on earth host bacterial endophytes (Ryan et al. 2008), and several endophytic bacteria like the Proteobacteria, Firmicutes Actinobacteria, and Bacteroidetes have putative PGP functions (Rosenblueth and Martinez-Romero 2006; Bulgarelli et al. 2013; Hardoim et al. 2015; Liu et al. 2017). Endophytic bacteria have been isolated from various plant parts including stems, roots, seeds, leaves, fruits, ovules, tubers, nodules, etc. (Benhizia et al. 2004; Pandey et al. 2018). Nevertheless, below ground potential i.e., plant roots harbor the greatest populations of these bacteria in comparison to aerial parts (Rosenblueth and Martinez-Romero 2006; Taghavi et al. 2010), at approximately 104 –106 per g of root tissue (Compant et al. 2010; Bulgarelli et al. 2013). Depsite occupying different ecological niches, endophytic bacterial populations employ PGP mechnaisms similar to those of free-living rhizosphere bacteria (Compant et al. 2005). The common PGP mechanisms can either be direct such as nitrogen-fixation, solubilization of nutrients, production of siderophores and phytohormones or indirect such as the suppression of plant pathogens and diseases (Suman et al. 2016; Lata et al. 2018). Diverse PGP bacterial endophytes have been explored and applied for crop yield enhancement under nutrient-poor conditions (Rosenblueth and Martinez-Romero 2006; Liu et al. 2017). Several studies demonstrate their positive effects in different food and cash crops such as the banana (Musa spp.) (Patel et al. 2017b), maize (Zea mays) (Alves et al. 2015), tomato (Lycopersicon esculentum) (Upreti and Thomas 2015), groundnut (Arachis hypogaea) (Dhole et al. 2016), and many more outlined by various workers (Hardoim et al. 2015; Pandey et al. 2018; Maheshwari 2018). Literature documents that endophyte-elicited PGP activities culminate into increased seed germination rates, biomass, chlorophyll, N

12 Endophytic Rhizobacteria for Mineral Nutrients …

269

and protein contents, root and shoot lengths, yield, and tolerance to abiotic stresses (Verma et al. 2013, 2015). The rhizobia which are the best-understood endophytes are critical for Nitrogen (N) nutrition in leguminous plants (Santoyo et al. 2016). Although endophytic rhizobacteria have widely been investigated, their significance in improving plant mineral nutrient acquisition has emerged quite recently (Harman and Uphoff 2019), and literature propounds that they could be better plant growth promoters and possess certain advantageous traits that give them an edge over their external counterparts (Coutinho et al. 2015; Asaf et al. 2017). However, this theory is not yet clearly understood as both are similar to their facilitation of plant mineral nutrients acquisition. This chapter reviews the potential functions of endophytic rhizobacteria in the acquisition of certain plant mineral macronutrients such as N, P, K and micronutrients like Zn and Fe. The putative advantageous traits that facilitate these functions and make them suitable candidates for enhancing mineral nutrients acquisition in plants are also discussed. Such information will enrich our knowledge on these important plant endophytic microbiome and possibly pave the way for their complete understanding and utilization as biofertilizers for sustainable crop production.

12.2 Putative Functions of Endophytic PGPR for Mineral Nutrients Acquisition in Plants Several studies demonstrate the diversity and functions of endophytic rhizobacteria toward plant mineral nutrients acquisition and general PGP activities. In this section, we outline some of these studies and functions to demonstrate the importance of these bacteria in plant mineral nutrition.

12.2.1 Endophytic Rhizobacteria and Nitrogen Acquisition in Plants Nitrogen is the most important nutrient required for plant growth (Verma et al. 2019). Although the atmosphere contains about 78% N, most of this is present in inert form and inaccessible to plants, making it a major plant-limiting nutrient. Artificial Nfertilizers are commonly applied to supply N to plants. However, out of every 100 Tg of N applied in agricultural fields globally, only about 17 Tg are utilized by plants and the rest is either lost or accumulates in the environment with serious implications to the soil and environment (Erisman et al. 2008; Howarth 2008). The microorganisms can convert excess ammonium or nitrate in the soil into nitrous oxide (N2 O), a potent greenhouse gas (GHG) (Kandel et al. 2017), whose effects are reportedly much worse than that of CO2 (Ramaswamy et al. 2001).

270

B. N. Aloo et al.

Endophytic N2 -fixing rhizobacteria are now emerging as one of the most efficient and environmentally sustainable approaches for increasing N acquisition for crops (Suman et al. 2016; Defez et al. 2017). Their potential has been illustrated in many studies, examples of which are provided in Table 12.1. It is proposed that endophytic N2- fixers can enable plants to survive under N-limiting conditions better than their external rhizobacterial counterparts (Gupta et al. 2013). For instance, the N2 fixation process requires energy to reduce the bonds in the N2 molecules and the endophytic N2- fixers can obtain the required energy from plant host tissues (Olivares et al. 2013). Similarly, their internal plant habitats offer favorable micro-aerobic environments that are more conducive to the nitrogenase enzyme complex that catalyzes the N2 fixation process (Doty et al. 2016). Although all diazotrophs are important for providing N to plants and enhancing their growth (Kumar et al. 2017), endophytic rhizobacteria not only provide the fixed N to their plant hosts more directly but also more efficiently (Suman et al. 2016; Lata et al. 2019). This is because the BNF process is largely mediated by the nif and fix genes whose transcriptions are primarily induced under low-oxygen conditions as in the interior plant tissues parts that host the endophytes (Bhagya and Rajkumar 2017). Literature suggests that the fixed N2 is converted to NH4 + in the bacterial cytoplasm and subsequently excreted into the host cytoplasm (Mia and Shamsuddin 2010), where it is assimilated into glutamate and transported in the xylem from the plant roots to their shoots as the major source of organic N (Nawaz et al. 2017). Thus the endophytic diazotrophs can release NH4 easily and directly into the plant host cell cytoplasm. Although some N2 -fixers can assimilate the produced NH4 into organic compounds, most N2 -fixing strains have unique regulatory mechanisms to secrete the NH4 outside their cells by diffusion instead of assimilating it (Day et al. 2001). This has a significant implication on the utilization of rhizobacteria as biofertilizers since the absence of this negative feedback mechanism can allow the nitrogenase enzyme complex to produce NH3 continuously for plant uptake. The symbiotic N2 -fixing rhizobia inhabiting in the cortial tissues of roots have been researched for several decades (Santoyo et al. 2016). The inoculation of crops and agricultural fields with such PGPR can help to maintain the N levels (Daman et al. 2016). For instance, about 1–2 kg N ha−1 day−1 can be obtained for all legumes by rhizobial N2 fixation alone (Lesueur et al. 2016). Apart from legumes, rhizobia have also been found living endophytically with rice, sweet corn, cotton, maize, bean, barley, and wheat among others as outlined in the review by Bhagya and Rajkumar (2017). This shows that there is a great possibility that several rhizobial interactions can similarly enhance N acquisition with non-leguminous crops. For instance, the discovery of N2 -fixing endophytic rhizobacteria in sugarcane (Ohyama et al. 2014; Mus et al. 2016) and cereals (Annapurna et al. 2004; Suman et al. 2016) especially sparked a substantial interest. Rhizobia have also been found to infect Brassica campestris and enhance its growth by increasing its N content (Chandra et al. 2007). Gluconacetobacter diazotrophicus which is the main endophytic diazotroph in sugarcane can fix up to 150 kg N ha−1 year−1 (Muthukumarasamy et al. 2005), and previous in vivo studies on this species also showed that it can promote the growth, germination, height, and nutrient uptake of sugarcane (Suman et al. 2008). Recently, a study

12 Endophytic Rhizobacteria for Mineral Nutrients …

271

Table 12.1 Some important nitrogen-fixing endophytic rhizobacteria and their associated host plants Source

Endophytic rhizobacteria

Reference

Banana (Musa spp.)

Klebsiella sp., Bacillus sp., Microbacterium sp., Enterobacter sp.,

Patel et al. (2017b)

B. subtilis

Andrade et al. (2014)

Cassava (Manihot esculenta)

Pantoea dispersa

Chen et al. (2014)

Cowpea (Vigna unguiculata)

Bradyrhizobium, Streptomyces griseoflavus

Htwe et al. (2019)

Groundnut (Arachis hypogaea)

Enterobacter ludwigii

Dhole et al. (2016)

Bradyrhiziobium

Taurian et al. (2013)

Maize (Zea mays)

Pseudomonas aeruginosa, E. asburiae, Acinetobacter brumalii

Sandhya et al. (2017)

Klebsiella sp., K. pneumoniae, B. pumilus Acinetobacter Kuan et al. (2016) sp., B. subtilis Bacillus sp., Enterobacter sp.

Szilagyi-Zecchin et al. (2014)

P. pseudoalcaligenes, P. aeruginosa

Jha (2019)

Mungbean (Vigna radiata)

Bradyrhizobium, Streptomyces griseoflavus

Htwe et al. (2019)

Rice (Oryza sativa)

Microbacterium, Bacillus, Klebsiella spp. Paenibacillus Ji et al. (2014) kribbensi, B. aryabhattai, K. pneumoniae, B. subtilis, M. trichotecenolyticum Rhizobium

Patel et al. (2017a)

Burkholderia, Herbaspirillum, Azospirillum, Rhizobium leguminosarum

Choudhary and Kennedy (2004), Doty (2011)

P. stutzeri

Pham et al. (2017)

Lysinibacillus sphaericus

Shabanamol et al. (2018)

Rhizobium sp., Azospirillum sp.

Sev et al. (2016)

Soybean (Glycine max)

Bradyrhizobium, Streptomyces griseoflavus

Htwe et al. (2019)

Sugarcane (Saccharum officinarum L)

Gluconacetobacter diazotrophicus

Suman et al. (2008)

Pantoea agglomerans

Quecine et al. (2012)

K. variicola DX120E

Wei et al. (2014) (continued)

272

B. N. Aloo et al.

Table 12.1 (continued) Source

Endophytic rhizobacteria

Reference

G. diazotrophicus

Ahmed et al. (2016)

Kosakania sp. ICB117

Kleingesinds et al. (2018)

Wheat (Triticum Achromobacter insolitus, Azospirillum brasisilense aestivum) Stenotrophomonas maltophilia, Chryseobacterium, Flavobacterium, Pseudomonas mexicana

Silveira et al. (2016) Youseif (2018)

involving other endophytes in a mixed inoculum also showed increased N uptake in sugarcane under N-limiting conditions (Marcos et al. 2016), an implication that there could be other beneficial diazotrophs in this plant. Ngamau et al. (2014), reviewed a number of endophytic banana rhizobacteria with BNF potential. As evidenced by these studies and many others, diazotrophic endophytes hold immense potential for enhancing N acquisition in various non-leguminous plants and further investigations in this regard are necessary.

12.2.2 Endophytic Rhizobacteria and Potassium Acquisition in Plants Potassium is the third most important quality macronutrient required for plant metabolism and growth (Ahmad et al. 2016; Proença et al. 2017). However, over 90% of K occurs in soil in fixed forms and only about 2% is readily available for plant use (Tsegaye et al. 2017; Meena et al. 2018). The application of K-based/potash fertilizers is a contemporary practice in extensive and intensive agricultural systems worldwide (Dasan 2012; Yagedari et al. 2012; Zhang et al. 2013). However, these synthetic fertilizers decrease agricultural profitability (Mohammadi and Sohrabi 2012; Ahmad et al. 2016) and sustainable crop yield. Potassium solubilizing bacteria (KSB) are an important source of the rhizosphere microbiome where they promote plant growth by solubilizing K-bearing minerals. Recent literature shows that KSB can be used to ameliorate K-deficient soils for crop production (Suman et al. 2016; Dhiman et al. 2019), and are quickly gaining momentum in the wake of calls for sustainable crop production (Ahmad et al. 2016). The burgeoning evidence of the large diversity of KSB associated with different plants shows that they have an immense potential for application in K-deficient soils (Meena et al. 2016; Velázquez et al. 2016). However, K solubilization abilities are less reported among endophytic rhizobacteria (Proença et al. 2017; Dhiman et al. 2019). For instance, in a study by Patel et al. (2017b), none of over 50 endophytic banana rhizobacteria were associated with K solubilization despite them showing

12 Endophytic Rhizobacteria for Mineral Nutrients …

273

other essential PGP functions including the solubilization abilities for other important plant nutrients. Nevertheless, there are studies that demonstrate the existence of K solubilizing endophytes. Potassium solubilizing endophytic rhizobacteria have been identified from wheat (Verma et al. 2013, 2015), more recently, from pearl millet (Kushwaha et al. 2019), maize (Jha 2019), and other crops (Dhiman et al. 2019). Rhizobia are the best-studied endophytes and are widely known for symbiotic N2 fixation in leguminous plants (Santoyo et al. 2016). However, of late, these novel rhizobacteria have also been shown to solubilize K in plant rhizospheres. For instance, K solubilization by rhizobia in rice has recently been reported by Patel et al. (2017a). Thirumal et al. (2017) demonstrated 5 rhizobial cultures associated with K solubilization in vitro. These new discoveries suggest that apart from enhancing N nutrition in plants, rhizobia can also be exploited for their K solubilizing abilities to enhance K availability in plant rhizosphere. Indigenous KSB are currently in the limelight for sustainable cropping systems and environmental conservation and have emerged as one of the viable technologies for mitigating K-deficiency in soils (Meena et al. 2015). Potassium solubilization indeed holds a lot of potential for PGP and the K solubilizing abilities of endophytic rhizobacteria are worth exploring. According to Meena et al. (2018), KSB are precious bio-resources that can mitigate K-deficiency in agricultural soils but their experimental evidence at the field level is still inadequate. Such processes may need to be exploited in detail so as to increase their usability.

12.2.3 Endophytic Rhizobacteria and Phosphorus Acquisition in Plants Phosphorus is the second most important plant nutrient after N (Goswami et al. 2016). Although soils contain P reserves, most of this is available in insoluble forms and inaccessible to plants (Verma et al. 2019). This non-availability is recognized as a major plant growth-limiting factor in agricultural systems (Sharma et al. 2013). The P solubilization potential of soil microorganisms is one of the most essential traits of PGPR for enhancing P-nutrition acquisition in plants (Walia and Shirkot 2012; Ouattara et al. 2019). While P solubilizing rhizobacteria are widely investigated, recent literature maintains that only a few endophytic rhizobacteria possess this ability (Brigido et al. 2019). Nevertheless, there is mounting evidence on the role of endophytes in P solubilization and mobilization compared to their widely reported rhizospheric counterparts (Ji et al. 2014; Oteino et al. 2015; Walitang et al. 2019). PSB can proliferate both in plant rhizospheres and endosphere (Hui et al. 2011), and according to Suman et al. (2016), P solubilization is a common trait among endophytic bacteria. However, the P solubilizing bacteria (PSB) still tend to be more abundant in plant rhizospheres in comparison to plant cells and tissues (Chen et al. 2006; Mwajita et al. 2013; Mehta

274

B. N. Aloo et al.

et al. 2015; Walia et al. 2017). Generally, the population of endophytic PSB range between 102 and 104 bacteria/g of root tissue (Kumar et al. 2013; Saini et al. 2015). A number of endophytic rhizobacterial populations belonging to Burkholderia, Enterobacter, Pantoea, Pseudomonas, Citrobacter, Azotobacter genera from wheat, rice, maize, legumes, and sunflower, respectively, are reported to solubilize mineral P in plate assays, and a vast number of P solubilizing PGPR are documented (Verma et al. 2013, 2015). In a recent study, Patel et al. (2017b), examined that 36% of over 50 endophytic rhizobacterial isolates belonging to genera Bacillus, Klebsiella, Microbacterium, and Enterobacter showed P solubilization. Further reports on P solubilizing endophytic rhizobacteria are depicted in Table 12.2. The P solubilizing PGPR can greatly impact plant growth by increasing P availability in the rhizospheric soils but must maintain an intimate relationship with the host plants (Walia et al. 2017). Numerous studies have highlighted the importance and mechanisms of P solubilization by PSB (Chhabra and Dowling 2017; Varma et al. 2017; Walia et al. 2017; Shrivastava et al. 2018; Billah et al. 2019; Goswami et al. 2019; Rafi et al. 2019; Dheeman et al. 2020). The solubilization of P is purportedly mediated through acidification, chelation, or exchange reactions (Li et al. 2017). According to Rosenblueth and Martinez-Romero (2006), endophytic PSB are more competitive than free-living rhizobacteria since the plant-endophyte interactions are the result of complex evolutionary processes. Moreover, endophytic rhizobacteria can prevent the adsorption and fixation of P under P-limiting conditions by assimilating the solubilized P (Khan and Joergersen 2009; Shakeela et al. 2017).

12.2.4 Endophytic Rhizobacteria in Zinc Acquisition in Plants Zinc is an important micronutrient required for primary and secondary metabolism in plants (Goteti et al. 2013; Bhatt and Maheshwari 2020). For instance, Zn is a cofactor in many enzymes (Hafeez et al. 2013) and it is critical for membrane function, photosynthesis, protein synthesis, and auxin metabolism in plants (Tavallali et al. 2010). Reports show that Zn deficiency is a common problem worldwide due to nutrient mining during crop harvesting and increased use of NPK fertilizers containing lesser amounts of Zn micronutrients (Sharifi and Paymozd 2016; Sindhu et al. 2019). Synthetic Zn fertilizers are often applied to overcome these deficiencies at rates of about 25 kg ha−1 ZnSO4 heptahydrate (equivalent to 5 kg ha−1 Zn). Nevertheless, these artificial fertilizers are not cost-effective and quickly get converted into insoluble forms that are inaccessible to plants (Bapiri et al. 2012; Sindhu et al. 2019). Rhizobacterial Zn solubilization abilities are widely reported phenomenon (Mishra et al. 2013; Shaikh and Saraf 2017). Reports also exist on endophytic Zn solubilization. For instance, Zn solubilizing bacteria (ZSB) have been reported to enhance Zn uptake in soybean up to 21% (Sharma et al. 2014), various G. diazotrophicus strains showed solubilization potential for various Zn compounds (Suman et al. 2016)

12 Endophytic Rhizobacteria for Mineral Nutrients …

275

Table 12.2 Studies demonstrating phosphate-solubilization by endophytic rhizobacteria in different crops Source

Endophytic rhizobacteria

Reference

Bananas (Musa spp.)

B. subtilis, Agrobacterium tumefaciens, Streptomyces sp., B. thuringiensis, B. amyloliquefaciens, Micrococcus luteus

Matos et al. (2017)

B. subtilis, Lysinibacillus sp.

Andrade et al. (2014)

Black pepper (Piper nigrum)

Klebsiella sp., Enterbacter sp.,

Jasim et al. (2013)

Cassava (Manihot esculenta)

Pantoea dispersa

Chen et al. (2014)

Chickpea (Cicer arietinum)

B. subtilis, B. licheniformis

Saini et al. (2015)

Bacillus sp., Klebsiella sp., Pseudomonas sp.

Chhabra and Sharma (2019)

P. agglomerans, B. cereus, B. sonorensis

Maheshwari et al. (2019a)

Cocoa (Theobroma cacao)

Not determined

Ouattara et al. (2019)

Common bean (Phaseolus vulgaris)

Pseudomonas sp.

Dini´c et al. (2014)

Common pea (Pisum sativum)

P. agglomerans, B. cereus, B. sonorensis

Maheshwari et al. (2019a)

Tumeric (Curcuma longa L.)

B. cereus, B. thuringiensis, B. pumilis, P. putida, Calvibacter michiganensis

Kumar et al. (2016)

Faba bean (Vicia faba L.)

Rhizobium nepotum, R. tibeticum

Rfaki et al. (2015)

Ginseng (Panax ginseng)

Lysinibacillus fusiformis, B. megaterium, B. cereus Vendan et al. (2010)

Maize (Zea mays)

Bacillus spp., Klebsiella sp., E. ludwigii, Pantoea spp.

de Abreu et al. (2017)

P. aeruginosa, E. asburiae, Acinetobacter brumalii Sandhya et al. (2017) Klebsiella sp., K. pneumoniae, B. pumilus Acinetobacter sp. and B. subtilis

Kuan et al. (2016)

Non-identified species

Manzoor et al. (2017)

P. pseudoalcaligenes, P. aeruginosa

Jha (2019)

Peach (Prunus persica) Brevundimonas diminuta, Agrobacterium tumefaciens, Stenotrophonomas rhizosphilia

Liaqat and Eltem (2016)

Peanut (Arachis hypogaea)

Taurian et al. (2013)

P. agglomerans

(continued)

276

B. N. Aloo et al.

Table 12.2 (continued) Source

Endophytic rhizobacteria

Reference

Pearl millet (Pennisetum glaucum)

Bacillus spp.

Ribeiro et al. (2018), Kushwaha et al. (2019)

Potato (Solanum tuberosum L.)

Bacillus spp., Pseudomonas spp., Serratia spp.

Abd El-Moaty et al. (2018)

Rice (Oryza sativa)

Paenibacillus kribbensi, B. aryabhattai, K. pneumoniae, B. subtilis, Microbacterium trichotecenolyticum

Ji et al. (2014)

Serratia sp., Pseudomonas sp.

Yasmin et al. (2016)

B. subtilis, B. megaterium

Dias et al. (2009)

Strawberry (Fragaria ananassa)

Soybean (Glycine max) E. sakazakii, P. straminae, Acinetobacter calcoaceticus

Kuklinsky-Sobral et al. (2004)

Sugarcane (Saccharum Herbaspirillum spp., Bacillus spp. Silva et al. (2015) officinarum L) Burkholderia mallei, B. cepacia, Proteus vulgaris, Awais et al. Pasteurella multocida, K. pneumoniae, K. oxytoca, (2019) E. cloacae, C. freundii Gluconacetobacter diazotrophicus

Crespo et al. (2011)

Tea (Camellia sinensis Bacillus, Brevibacterium, Paenibacillus, L.) Lysinibacter

Borah et al. (2019)

Tomato (Solanum lycopersicum)

Lysinibacillus spp.

Sahu et al. (2018)

Wheat (Triticum aestivum)

Stenotrophomonas maltophilia, Chryseobacterium, Youseif (2018) Flavobacterium, P. mexicana

Wild mint (Mentha arvensis)

Non-identified strains

Batool and Iqbal (2018)

Bacillus sp.

Prakash and Arora (2019)

and the endophytic G. diazotrophicus inhabiting sugarcane have shown to possess Zn solubilization abilities alongside other multifarious PGP activities (Saravanan et al. 2007; Natheer and Muthukkaruppan 2012). Yaish et al. (2015), isolated endophytic bacteria from the date palm tree (Phoenix dactylifera L.), identified as P. aeruginosa, P. monteilii, P. putida, Acitenobacter brumalii, E. asburiae, Sinorhizobium meliloti, P. thivervalensis, P. fulva, and P. lini were capable of solubilizing Zn oxide (ZnO). The Gram-positive B. aryabhattai was also shown to improve the growth of soybean and wheat due to Zn solubilizing processes (Ramesh et al. 2014). Investigations on rhizobial and Pseudomonas cultures demonstrated the in vitro solubilization of different forms of insoluble Zn (Thirumal et al. 2017). The ability to solubilize various sources of insoluble Zn

12 Endophytic Rhizobacteria for Mineral Nutrients …

277

has been emphasized in the selection of potential endophytes for enhancement of Zn uptake in plants (Singh et al. 2018). Other endophytic ZSB include species of Bacillus, Chryseobacterium, Paenibacillus, Rhodococcus, Staphylococcus, Achromobacter, Acinetobacter, Enterobacter, and Klebsiella (Suman et al. 2016). Recently, Kushwaha et al. (2019) also observed that endophytic Bacillus strains from pearl millet exhibited Zn solubilization potential and had multiple roles in stress tolerance of the plant. The use of such ZSB can increase Zn uptake by filed crops, which would in turn lead to their improved growth and yield (Suman et al. 2016).

12.2.5 Endophytic Rhizobacteria and Iron Acquisition in Plants Iron is the fourth most abundant element in soil and is an important micronutrient required by plants for many physiological processes (Saha et al. 2016). However, most agricultural soils are Fe-deficient because the element occurs in the insoluble ferric (Fe3+ ) form that is unavailable for plant uptake (Rajkumar et al. 2010; Arora and Verma 2017; Singh et al. 2019). Some microorganisms have developed a special Fe acquisition mechanism under these Fe-limiting conditions by producing certain special metabolites known as siderophores (Maheshwari et al. 2019b). Siderophores are secondary metabolites with high affinity for Fe3+ (Goswami et al. 2016; Arora and Verma 2017), and under Fe-limiting conditions, siderophores complex with Fe3+− , a phenomenon which is important for enhancing Fe availability in the rhizosphere (Ferna´ndez-Scavino and Pedraza 2013; Boiteau et al. 2016; Chhabra and Dowling 2017). It is proposed that once the siderophores bind onto Fe3+ , the acquisition of the bound Fe by plants can occur by the degradation of the chelates or complexes (Rajkumar et al. 2009). According to Loaces et al. (2011), siderophore production is a common trait among the free-living PGPR (Souza et al. 2015) and is rarely reported for the endophytic rhizobacteria. Recent literature suggests that only a few endophytic bacterial isolates possess this trait (Brigido et al. 2019), investigated mainly as a bio-control agent against plant pathogens (Suman et al. 2016). In such cases, the siderophores chelate most of the Fe present in the rhizosphere and prevent the proliferation of pathogens due to its non-availability in the rhizosphere soil (Mitter et al. 2013; Olanrewaju et al. 2017). Nevertheless, endophytic rhizobacteria can also produce these metabolites under Fe-stress and aid in plant Fe acquisition (Ghavami et al. 2017; Perez-Rosales et al. 2017), and endophytic genera like Pantoea, Bacillus, Burkholderia, and Pseudomonas can increase the concentration of bioavailable Fe in plant tissues (Maheshwari et al. 2019a). Endophytic siderophore producers that include Brevundimonas diminuta, Leifsonia shinshuensis, Sphingomonas parapaucimobilis, Brevundimonas vesicularis, and Agrobacterium tumefaciens have been identified from pear and peach roots (Liaqat and Eltem 2016). Bacillus sp., Pseudomonas sp., and Stenotrophomonas sp. are also recognized among the effective siderophore-producing endophytes (Jasim

278

B. N. Aloo et al.

et al. 2014). Serratia sp. and Pseudomonas sp. from rice have been recently reported to produce siderophores by Yasmin et al. (2016). Siderophore-producing endophytic P. agglomerans from peanuts (Taurian et al. 2013), and in turmeric (Kumar et al. 2016) have also been reported. The endophytic Bacillus sp. and P. putida were also associated with siderophore production. Similar studies on pepper endophytic Paenibacillis polymyxa by Phi et al. (2010) also exhibited such abilities by Vendan et al. (2010). The endophytic bacteria such as B. cereus, B. flexus, B. megaterium, Lysinibacillus fusiformis, L. sphaericus, Microbacterium phyllosphaerae, Micrococcus luteus isolated from maize also showed excellent siderophore production. Investigations by Youseif (2018) also demonstrated siderophore production capabilities by wheat-root endophytic Stenotrophomonas maltophilia, Chryseobacterium sp, Falvobacterium sp., and Pseudoxanthomonas mexicana. In another study, Maheshwari et al. (2019b), characterized siderophore-producing endophytic bacteria from chickpea (Cicer arietinum) and pea (Pisum sativum). Earlier, Wani and Khan (2010) stated that chickpea endophytic Pseudomonas sp. was one of the dominant siderophore-producing genera of the plant. Patel et al. (2017b), observed endophytic rhizobacterial isolates identified as Bacillus, Klebsiella, Microbacterium, and Enterobacter species which showed excellent siderophore production abilities. Similarly, siderophore-producing endophytes have also been isolated from maize and canola (Ghavami et al. 2017), corn (Szilagyi-Zecchin et al. 2014), banana, etc. (Ouma et al. 2014). Siderophore-producing endophytes are important to crops not only directly by improving Fe availability for plant uptake but also indirectly by depriving Fe required to plant pathogens (Chhabra and Dowling 2017; Aloo et al. 2019b). The completed genome analyses of endophytic microbes like Enterobacter species have shown that they contain a large number of genes that code for siderophore transporter proteins (Taghavi et al. 2010). The production of siderophores is a classic example of how rhizobacteria can improve Fe availability in the plant rhizosphere and due to its indisputable role in plant nutrition, further investigations on siderophore-producing rhizobacteria are necessary (Aloo et al. 2019a).

12.3 Ecological Significance of Endophytes in Mineral Nutrients Acquisition by Plants Endophytic rhizobacteria are considered as sub-sets of rhizosphere microbiome that have acquired the ability to colonize plant root tissues and exhibit specialized and unique lifestyles (Compant et al. 2010; Dheeman et al. 2017). Despite their special interaction with plants, endophytes share all the important PGP traits with other rhizobacteria (Compant et al. 2005). However, they possess characteristics that are distinct from rhizospheric bacteria, suggesting that not all rhizospheric bacteria can enter plants, and/or that once inside their hosts, they change their lifestyles to adapt to internal habitats within plants (Monteiro et al. 2012; Sessitsch et al.

12 Endophytic Rhizobacteria for Mineral Nutrients …

279

2012). For instance, a study on plant colonization and the establishment of symbionts by Hardoim et al. (2015) showed the presence of significant putative properties in endophytes compared to other types of bacteria interacting with plants. There is an increasing interest in harnessing the potential of endophytic microbes to develop sustainable crop production systems. Although endophytic rhizobacteria are considered a subset of the rhizospheric microflora, their endophytic lifestyle offers them a myriad of advantages over rhizospheric growth (Compant et al. 2010). For instance, they establish themselves in sheltered micro-environments within the plant root tissues (Castanheira et al. 2017), which are protective ecological niches that provide them with safe, consistent, and undisturbed environments as opposed to external rhizobacteria (Senthilkumar et al. 2011). Literature advances that endophytic microbes are relatively protected from external biotic and biotic environmental stresses, unlike their external counterparts whose survivability and colonizability are largely dependent on extrinsic soil factors (Rajkumar et al. 2009; Suman et al. 2016; Waghunde et al. 2017; Lata et al. 2019; Dubey et al. 2020). Living endophytically allows these bacteria to maintain close contact with plant root tissues for the direct and constant supply of nutrients and their beneficial effects can be exerted onto the host plants more directly (Lata et al. 2019). The plant endosphere niche presents a unique habitat, and bacterial endophytes possibly have differential functions, specializations, adaptations, and competence (Compant et al. 2010). The diversity of endophytic communities also varies depending on host plant species and genotypes, location, developmental stages, and local environmental conditions (Shi et al. 2014). Nevertheless, the direct and intimate interactions that endophytic rhizobacteria form with plant root tissues makes them highly valuable tools and suitable candidates for improving mineral nutrient acquisition in plants more directly and efficiently (Sreejith et al. 2019).

12.4 Conclusions and Future Prospects The need for eco-friendly crop fertilization alternatives is increasingly becoming urgent. However, endophytic rhizobacteria have not been fully understood and the prospects of finding unique and interesting bacteria are great. Identifying endophytic rhizobacterial strains with multiple PGP functions for specific plants can definitely pave way for more benefits in terms of plant mineral nutrients acquisition. As such, present and future research work should focus on the largely unexplored rhizobacterial endophytes and their potential uses for mineral nutrients acquisition in plants (Turner et al. 2013). Most plant-endophyte interactions have involved rhizobia and legumes and future research should explore fresh alternatives on their application for other agronomically important crops (Suman et al. 2016). Although there is a wealth of information on culture-dependent and independent characterization of endophytic rhizobacterial diversity and their associated in vitro PGP mechanisms, reports on their practical applications as plant inoculants under

280

B. N. Aloo et al.

field conditions are extremely scarce (Liu et al. 2017). Several endophytic rhizobacteria have been identified in laboratory studies but generally fail to give consistent results under field conditions and there is need to understand the complex dynamics that control plant-endophyte associations probably by identifying genes that govern these relationships at the molecular level. Although some studies have been conducted in this area, they remain limited and genomic analyses can decipher into the capabilities of endophytes and their roles in plant mineral acquisition. Our knowledge about the plant-microbe interactions can greatly be enhanced using metabolomic, genomic, and transcriptomic methods (Dubey et al. 2020). At the moment, only a limited number of genes that contribute to endophytic invasion and colonization have been identified. Perhaps whole-genome sequencing of these organisms will facilitate the identification of novel isolates and their successful exploitation for plant mineral nutrients acquisition. Further analysis of the sequenced genomes and characterization of the involved genes can also help to improve our understanding of their interaction with plants (Compant et al. 2010) for full exploitation. These efforts can also lead to the identification of some new genes required for endophytic lifestyle but there would be a need to separate the common genes for rhizosphere colonization from those involved in the endophytic lifestyle. Additionally, a more comprehensive understanding of whether these organisms are likely to establish themselves in plants if applied as biofertilizers is needed (Compant et al. 2010). Numerous reports have revealed a range of beneficial features of the endophytic rhizobacteria for plant mineral nutrients acquisition. Nevertheless, there is still a great scope of further exploration and identification of more novel functions. For instance, research on N2 fixation and P solubilization abilities by endophytic plant rhizobacteria continues to expand, but very little strides have been made regarding K solubilization yet K is the third major essential macronutrient for plant growth. Similarly, limited work has been carried out on S-oxidation (Dhiman et al. 2019). A combination of both traditional and modern biotechnological methods will help in advancements toward improved plant mineral nutrients acquisition and sustainable agriculture (Waghunde et al. 2017). Although a broad range of endophytes with traits for enhancing mineral nutrient acquisition in different plants have been described, only a few of these have conclusively been studied to demonstrate their significance in plants (Chhabra and Dowling 2017). Furthermore, the impact of endophytic colonization and enhanced nutrient uptake in plants can be varied depending on plant host species/cultivars, endophyte strains, and environmental conditions (Shi et al. 2014). The successful manipulation of the plant microbiome can substantially contribute to sustainable agricultural production (Bakker et al. 2012; Tkacz et al. 2015), by reducing the need for chemical inputs (Adesemoye et al. 2009; Kandel et al. 2017) and GHG emissions (Singh et al. 2010). This chapter provides a comprehensive review of the putatie functions and ecological significance of endophytic PGPR for mineral nutrient acquisition in plants. Taking into consideration the intimate relationships they form with their plant hosts, these rhizobacteria present special tools for improving plant mineral nutrients acquisition and could be better plant growth promoters than their external counterparts (Lata et al. 2019). Endophytes are

12 Endophytic Rhizobacteria for Mineral Nutrients …

281

indeed fascinating life forms and there is no doubt that their intricate lifestyles and plant interactions still require better understanding to facilitate their application as viable alternatives to artificial fertilizers for agricultural sustainability.

References Abd El-Moaty NM, Khalil HMA, Gomaa HH, Ismail MA, El-Dougdoug KA (2018) Isolation, characterization, and evaluation of multi-trait plant growth promoting rhizobacteria for their growth promoting. Middle East J Appl Sci 8:554–566 Adesemoye AO, Torbert H, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929 Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ-Sci 26:1–20. https://doi.org/10.1016/j.jksus.2013.05.001 Ahmad M, Nadeeem SM, Naveed M, Zahid ZA (2016) Potassium-solubilizing bacteria and their application in agriculture. In: Meena V, Maurya B, Verma J, Meena R (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 293–313 Ahmed HF, Badawy HH, Mahmoud SM, El-Dosouky MM (2016) Characterization of Gluconacetobacter diazotrophicus isolated from sugarcane (Saccharum officinarum) cultivated in Upper Egypt. Assiut J Agric Sci 47:569–582 Aloo BN, Mbega ER, Makumba BA (2019a) Rhizobacteria-based technology for sustainable cropping of potato (Solanum tuberosum L.). Potato Res: 1–21. https://doi.org/10.1007/s11540-01909432-1 Aloo BN, Makumba BA, Mbega ER (2019b) The potential of Bacilli rhizobacteria for sustainable crop production and environmental sustainability. Microbiol Res 219:26–39. https://doi.org/10. 1016/j.micres.2018.10.011 Alves GC, Videira SS, Urquiaga S, Reis VM (2015) Differential plant growth promotion and nitrogen fixation in two genotypes of maize by several Herbaspirillum inoculants. Plant Soil 387:307–321. https://doi.org/10.1007/s11104-014-2295-2 Andrade LF, de Souza GLOD, Nietsche S, Xavier AA, Costa MR, Cardoso AMS, Pereira MCT, Pereira DFGS (2014) Analysis of the abilities of endophytic bacteria associated with banana tree roots to promote plant growth. J Microbiol 52:27–34. https://doi.org/10.1007/s12275-0143019-2 Annapurna J, Chowdary I, Lalitha G, Ramakrishna S, Iyengar D (2004) Phytochemical screening and in vitro bioactivity of Cnidoscolus aconitifolius (Euphorbiaceae). Pharm Biol 42:91–93 Archana DS, Nandish MS, Savalagi VP, Alagawadi AR (2013) Characterization of potassium solubilizing bacteria (KSB) from rhizosphere soil. Bioinfolet 10:248–257 Arora NK, Verma M (2017) Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech 7:381. https://doi.org/10.1007/s13205-017-1008-y Asaf S, Khan MA, Khan AL, Waqas M, Shahzad R, Kim AY, Kang SM, Lee IJ (2017) Bacterial endophytes from arid land plants regulate endogenous hormone content and promote growth in crop plants: an example of Sphingomonas sp. and Serratia marcescens. J Plant Interact 12:31–38 Awais M, Tariq M, Ali Q, Khan A, Ali A, Nasir IA, Husnain T (2019) Isolation, characterization and association among phosphate solubilizing bacteria from sugarcane rhizosphere. Cytol Genet 53:86–95. https://doi.org/10.3103/S0095452719010031 Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13 Baliyan N, Dheeman S, Maheshwari DK, Dubey RC, Vishnoi VK (2018) Rhizobacteria isolated under field first strategy improved chickpea growth and productivity. Environ Sustain 1:461–469 Bapiri A, Asgharzadeh A, Mujallali H, Khavazi K, Pazira E (2012) Evaluation of zinc solubilization potential by different strains of fluorescent Pseudomonads. J Appl Sci Environ Manag 16:295–298

282

B. N. Aloo et al.

Batool S, Iqbal A (2018) Phosphate solubilizing rhizobacteria as alternative of chemical fertilizer for growth and yield of Triticum aestivum (Var. Galaxy 2013). Saudi J Biol Sci. https://doi.org/ 10.1016/j.sjbs.2018.05.024 Benhizia Y, Benhizia H, Benguedouar A, Muresu R, Giacomini A, Squartini A (2004) Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27:462–468 Bhagya I, Rajkumar S (2017) Host specificity and plant growth promotion by bacterial endophytes. Curr Res Microbiol Biotechnol 5:1018–1030 Bhatt K, Maheshwari DK (2020) Zinc solubilizing bacteria (Bacillus megaterium) with multifarious plant growth promoting activities alleviates growth in Capsicum annuum L. 3 Biotech 10:36. https://doi.org/10.1007/s13205-019-2033-9 Billah M, Khan M, Bano A, Hassan TU, Munir A, Gurmani AR (2019) Phosphorus and phosphate solubilizing bacteria: keys for sustainable agriculture. Geomicrobiol J 36:904–916. https://doi. org/10.1080/01490451.2019.1654043 Boiteau RM, Mende DR, Hawco NJ, Mcllvin MR, Fitzsimmons JN, Saito MA, Sedwick PN, DeLong EF, Repeta DJ (2016) Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean. Proc Natl Acad Sci U S Am Natl Acad Sci US 113:14237–14242 Borah A, Das R, Mazumdar R, Thakur D (2019) Culturable endophytic bacteria of Camellia species endowed with plant growth promoting characteristics. J Appl Microbiol 127:825–844. https:// doi.org/10.1111/jam.14356 Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma LJ, Sessitsch A (2017) Ecology and genomic insights into plant-pathogenic and plant-non pathogenic endophytes. Annu Rev Phytopathol 55:61–83 Brigido C, Singh S, Menéndez E, Tavares MJ, Glick BR, Felix MR, Oliveira S, Carvalho M (2019) Diversity and functionality of culturable endophytic bacterial communities in chickpea plants. Plants 8:42 Bulgarelli D, Schlaeppi K, Spaepen S, van Thermaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol: 807–838. https://doi.org/ 10.1146/annurev-arplant-050312-120106 Castanheira NL, Dourado AC, Pais I, Samedo J, Scotti-Campos P, Borges N, Fareleira P (2017) Colonization and beneficial effects on annual ryegrass by mixed inoculation with plant growth promoting bacteria. Microbiol Res 198:47–55 Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz J Microbiol 38(1):124–130 Chen PY, Pekha PD, Arunshen AB, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41 Chen Y, Fan JB, Du L, Zhang QH, He YQ (2014) The application of phosphate solubilizing endophyte Pantoea dispersa triggers the microbial community in red acidic soil. Appl Soil Ecol 84:235–244 Chhabra S, Dowling DN (2017) Endophyte-promoted nutrient acquisition: phosphorus and iron. In: Doty SL (ed) Functional importance of the plant microbiome. Springer, Cham, pp 21–42 Chhabra S, Sharma P (2019) Non rhizobial endophytic bacteria from Chickpea (Cicer arietinum L.) tissues and their antagonistic traits. J Appl Nat Sci 11:346–351 Choudhary ATMA, Kennedy IR (2004) Prospects and potentials for systems of biological nitrogen fixation in sustainable rice production. Biol Fertil Soils 39:219–227 Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo and endosphere of plants their role, organization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678 Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Biol 71:4951–4959

12 Endophytic Rhizobacteria for Mineral Nutrients …

283

Coutinho BG, Licastro D, Mendonca-Previato L, Cámara M, Venturi V (2015) Plant influenced gene expression in the rice endophyte Burkholderia kururiensis M130. Mol Plant Microbe Interact 28:10–21 Crespo JM, Boiardi JL, Luna MF (2011) Mineral phosphate solubilization activity of Gluconacetobacter diazotrophicus under P-limitation and plant root environment. Agric Sci 2:16–22 Daman M, Kaloori K, Gaddam B, Kausar R (2016) Plant growth promoting substances (phytohormones) produced by rhizobacterial strains isolated from the rhizosphere of medicinal plants. Int J Pharm Sci Rev Res 37:130–136 Dasan AS (2012) Compatibility of agrochemicals on the growth of phosphorous mobilizing bacteria Bacillus megaterium var. phosphaticum potassium mobilizing bacteria Frateuria aurantia. Appl Res Dev Inst J 6:118–134 Day DA, Poole PS, Tyermanc SD, Rosendahl L (2001) Ammonia and amino acid transport across symbiotic membranes in nitrogen fixing legume nodules. Cell Mol Life Sci 58:61–71 de Abreu CS, Figueiredo JEF, Oliveira CA, dos Santos VL, Gomes EA, Ribeiro VP, Lana UGP, Marriel IE (2017) Maize endophytic bacteria as mineral phosphate solubilizers. Genet Mol Res 16:1–13 Defez R, Anna Andreozzi A, Bianco C (2017) The overproduction of Indole-3-acetic acid (IAA) in endophytes upregulates nitrogen fixation in both bacterial cultures and inoculated rice plants. Microb Ecol 74:441–452 Dheeman S, Baliyan N, Dubey RC, Maheshwari DK, Kumar S, Chen L (2020) Combined effects of rhizo-competitive rhizosphere and non-rhizosphere Bacillus in plant growth promotion and yield improvement of Eleusine coracana (Ragi). Can J Microbiol 66(2):111–124 Dheeman S, Maheshwari DK, Baliyan N (2017) Bacterial endophytes for ecological intensification of agriculture. In: Maheshwari DK (ed) Endophytes: biology and biotechnology. Springer International Publishing, Cham, pp 193–231 Dhiman S, Dubey RC, Baliyan N, Kumar S, Maheshwari DK (2019a) Application of potassiumsolubilising Proteus mirabilis MG738216 inhabiting cattle dung in improving nutrient use efficiency of Foeniculum vulgare Mill. Environ Sustain 2:401–409 Dhiman S, Dubey RC, Maheshwari DK, Kumar S (2019b) Sulfur-oxidizing buffalo dung bacteria enhance growth and yield of Foeniculum vulgare Mill. Can J Microbiol 65(5):377–386 Dhole A, Shelat H, Vyas P, Jhala Y, Bhange M (2016) Endophytic occupation of legume root nodules by nifH-positive non-rhizobial bacteria, and their efficacy in the groundnut (Arachis hypogaea). Ann Microbiol 66:1397–1407 Di Benedetto NA, Corbo MR, Campaniello D, Cataldi MP, Bevilacqua A, Sinigaglia M, Flagella Z (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiol 3:413–434 Dias ACF, Costa FEC, Andreote FD, Lacava PT, Teixeira MA, Assumpção LC, Araújo WL, Azevedo JL, Melo IS (2009) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195 Dini´c Z, Ugrinovi´c M, Bosni´c P, Mijatovi´c M, Zdravkovi´c J, Miladinovi´c M, Joši´c D (2014) Solubilization of inorganic phosphate by endophytic Pseudomonas sp. from French bean nodules. Ratar Povrt 51:100–105. https://doi.org/10.5937/ratpov51-6222 Doty SL (2011) Nitogen-fixing endophytic bacteria for improved plant growth. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer-Verlag, Berlin, Heidelberg, pp 183–199 Doty SL, Sher AW, Fleck ND, Khorosani M, Bumgarner RE, Khan Z, Ko AWK, Kim SH, Deluca TH (2016) Variable nitrogen fixation in wild populus. PLoS ONE 11:e0155979 Dubey RK, Tripathi V, Prabha R, Chaurasia R, Singh DP, Rao CS, El-Keblawy A, Abhilash PC (2020) Belowground microbial communities: key players for soil and environmental sustainability. In: Dubey RK, Tripathi V, Prabha R, Chaurasia R, Singh DP, Rao CS, El-Keblawy A, Abhilash PC (eds) Unravelling the soil microbiome: perspectives for environmental sustainability. Springer International Publishing, Cham, pp 5–22

284

B. N. Aloo et al.

Erisman JW, Sutton MA, Galloway JN, Klimont Z, Winiwarter W (2008) How a century of ammonia synthesis changed the world. Nat Geosci 1:636–639. https://doi.org/10.1038/ngeo325 Ferna´ndez-Scavino A, Pedraza RO (2013) The role of siderophores in plant growth-promoting bacteria. In: Maheshwari DK, Saraf M, Aeron A (eds) Bacteria in agribiology: crop productivity. Springer, Heidelberg, pp 265–285 Ghavami N, Alikhani HA, Pourbabei AA, Besharati H (2017) Effects of two new siderophoreproducing rhizobacteria on growth and iron content of maize and canola plants. J Plant Nutr 40:736–746. https://doi.org/10.1080/01904167.2016.1262409 Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39 Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Congent Food Agric 2:1–9 Goswami SP, Maurya BR, Dubey AN, Singh NK (2019) Role of phosphorus solubilizing microorganisms and dissolution of insoluble phosphorus in soil. Int J Chem Stud 7:3905–3913 Goteti PK, Emmanuel LAE, Desai S, Shaik MHA (2013) Prospective zinc solubilising bacteria for enhanced nutrient uptake and growth promotion in maize (Zea mays L.). Int J Microbiol 2013:869697. https://doi.org/10.1155/2013/869697 Gupta G, Panwar J, Jha PN (2013) Natural occurrence of Pseudomonas aeruginosa, a dominant cultivable diazotrophic endophytic bacterium colonizing Pennisetum glaucum (L.) R. Br. Appl Soil Ecol 64:252–261 Hafeez B, Khanif YM, Saleem M (2013) Role of zinc in plant nutrition—a review. Am J Exp Agric 3:374–391 Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S, Campisano A, Doring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol 79:293–320 Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 9106395 Howarth RW (2008) Coastal nitrogen pollution: a review of sources and trends globally and regionally. Harmful Algae 8:14–20 Htwe AZ, Moh SM, Soe KM, Moe K, Yamakawa T (2019) Effects of Biofertilizer produced from Bradyrhizobium and Streptomyces griseoflavus on plant growth, nodulation, nitrogen fixation, nutrient uptake, and seed yield of Mung Bean, Cowpea, and Soybean. Agronomy 9:77. https:// doi.org/10.3390/agronomy9020077 Hui L, Xiao QW, Jia-Hong R, Jian-Ren Y (2011) Isolation and identification of phosphobacteria in poplar rhizosphere from different regions of China. Pedosphere 21:90–97 Jasim B, Jimtha JC, Jyothis M, Radhakrishnan EK (2013) Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regul 71:1–11 Jasim B, Joseph AA, John CJ, Mathew J, Radhakrishnan EK (2014) Isolation and characterization of plant growth promoting endophytic bacteria from the rhizome of Zingiber officinale. 3 Biotech 4:197–204 Jha Y (2019) Endophytic bacteria as a modern tool for sustainable crop management under stress. In: Giri B, Prasad R, Wu QS, Varma A (eds) Biofertilizers for sustainable agriculture and environment. Springer International Publishing, Cham, pp 203–223 Ji SH, Gururani MA, Chun SC (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169:83–98. https:// doi.org/10.1016/j.micres.2013.06.003 Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5:77. https://doi.org/10.3390/microorganisms5040077 Khan KS, Joergersen RG (2009) Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresour Technol 100:303–309 Kleingesinds CK, de Santi Ferrara FI, Floh ELS, Aldar MPM, Barbosa HR (2018) Sugarcane growth promotion by Kosakania sp. ICB117 an endophytic and diazotrophic bacterium. Afr J Microbiol Res 12:105–114. https://doi.org/10.5897/AJMR2017.8738

12 Endophytic Rhizobacteria for Mineral Nutrients …

285

Kuan KB, Othman R, Rahim KA, Shamsuddin ZH (2016) Plant growth-promoting rhizobacteria inoculation to enhance vegetative growth, nitrogen fixation and nitrogen remobilization of maize under Greenhouse conditions. PLoS ONE 11:1–19 Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251 Kumar A, Maurya BR, Raghuwanshi R (2014) Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatal Agric Biotechnol 3:121–128 Kumar A, Singh R, Yadav A, Giri DD, Singh KP, Pandey KD (2016) Isolation and characterization of bacterial endophytes of Curcuma longa L. 3 Biotech 6:60 Kumar SS, Ram KR, Kumar DR, Panwar S, Prasad CS (2013) Biocontrol by plant growth promoting rhizobacteria against black scurf and stem canker disease of potato caused by R. Solani. Arch Phytopathol Plant Prot 46:487–502 Kumar U, Paneerselvam P, Govindasamy V, Vithakumar L, Senthikumar M, Banik A, Annapuma K (2017) Long-term aromatic rice cultivation effect on frequency and 16 diversity of diazotrophs in its rhizosphere. Ecol Eng 101:227–236 Kushwaha P, Kashyap PL, Kuppusamy P, Srivastava AK, Tiwari RK (2019) Functional characterization of endophytic bacilli from pearl millet (Pennisetum glaucum) and their possible role in multiple stress tolerance. Plant Biosyst. https://doi.org/10.1080/11263504.2019.1651773 Lata RK, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276. https://doi.org/10.1111/lam.12855 Lata RK, Divjot K, Nath YA (2019) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162 Lesueur D, Deaker R, Herrmann L, Bräu L, Jansa J (2016) The production and potential of biofertilizers to improve crop yields. In: Arora NK, Menhaz S, Balestrini R (eds) Bioformulations for sustainable agriculture. Springer, New Delhi, pp 71–92 Li Y, Liu X, Hao T, Chen S (2017) Colonization and Maize growth promotion induced by phosphate solubilizing bacterial isolates. Int J Mol Sci 18:1253 Liaqat F, Eltem R (2016) Identification and characterization of endophytic bacteria isolated from in vitro cultures of peach and pea rootstocks. 3 Biotech 6:2–9 Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. https://doi.org/10.3389/fmicb.2017.02552 Loaces I, Ferrando L, Scavino AF (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microb Ecol 61:606–618 Maheshwari DK (2018) Endophytes: biology and biotechnology. Springer International Publishing, Cham Maheshwari R, Bhutani N, Bhardwaj A, Suneja P (2019a) Functional diversity of cultivable endophytes from Cicer arietinum and Pisum sativum: bioprospecting their plant growth potential. Biocatal Agric Biotechnol 20:101229. https://doi.org/10.1016/j.bcab.2019.101229 Maheshwari R, Bhutani N, Suneja P (2019b) Screening and characterization of siderophore producing endophytic bacteria from Cicer arietinum and Pisum sativum plants. J Appl Biol Biotechnol 7:7–14. https://doi.org/10.7324/JABB.2019.70502 Manzoor M, Abbasi MK, Sultan T (2017) Isolation of phosphate solubilizing bacteria from maize rhizosphere and their potential for rock phosphate solubilization-mineralization and plant growth promotion. Geomicrobiol J 34:81–95. https://doi.org/10.1080/01490451.2016.1146373 Marcos FCC, Io´rio RPF, Silveira APDD, Ribeiro RV, Machado EC, Lagoˆa AMA (2016) Endophytic bacteria affect sugarcane physiology without changing plant growth. Bragantia 75:1–9 Matos ADM, Gomez ICP, Nietsche S, Xavier AA, Gomes WS, Dos Santos N, Jose A, Pereira MCT (2017) Phosphate solubilization by endophytic bacteria isolated from banana trees. An Acad Bras Ciênc 89:2945–2954

286

B. N. Aloo et al.

Meena VS, Maurya BR, Verma JP, Aeron A, Kim K, Bajpai V (2015) Potassium solubilizing rhizobacteria (KSR): isolation, identification, and K-release dynamics from waste mica. Ecol Eng 81:340–347 Meena VS, Maurya BR, Verma JP, Verma RS (eds) (2016) Potassium solubilizing microorganisms for sustainable agriculture. Springer, India Meena SV, Maurya BR, Meena SK, Mishra PK, Bisht JK, Pattanayak A (2018) Potassium solubilization: strategies to mitigate potassium deficiency in agricultural soils. Glob J Biol Agricluture Health Sci 7:1–3 Mehta P, Walia A, Shirkot CK (2015) Functional diversity of phosphate solubilizing plant growth promoting rhizobacteria isolated from apple trees in the Trans Himalayan region of Himachal Pradesh, India. Biol Agric Hortic 31:265–288. https://doi.org/10.1080/01448765.2015.1014420 Mia MAB, Shamsuddin ZH (2010) Nitrogen fixation and transportation by rhizobacteria: a scenario of rice and banana. Int J Bot 6:235–242 Mishra DJ, Mishra UK, Shahi SK (2013) Role of bio-fertilizer inorganic agriculture: a review. Res J Recent Sci 2:39–41 Mitter B, Petric A, Shin MW, Ghain PSG, Hauberg-Lotte L, Reinhold-Hurek B, Nowak J, Sessitsch A (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120 Mohammadi K, Sohrabi Y (2012) Bacterial biofertilizers for sustainable crop production: a review. ARPN J Agric Biol Sci 7:307–316 Monteiro RA, Balsanelli E, Wassem R, Marin AM, Brussamarello-Santos LCC, Schmidt MA, Tadra-Sfeir MZ, Pankievicz VCS, Cruz LM, Chubatsu LS, Pedrosa FO, Souza EM (2012) Herbaspirillum-plant interactions: microscopical, histological and molecular aspects. Plant Soil 356:175–196 Mus F, Crook MB, Garcia K, Costas AG, Geddes BA, Kouri ED, Paramasivan P, Ryu H, Oldroyd GED, Poole PS, Udvardi MK, Voigt TA, Ane JM, Peters JW (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710. https:// doi.org/10.1128/aem.01055-16 Muthukumarasamy R, Clenwerck I, Revathi G, Vadivelu M, Janssens D, Hoste B, Park KD, Son CY, Sa T (2005) Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28:277–286 Mwajita MR, Murage H, Tani A, Kahangi EM (2013) Evaluation of rhizosphere, rhizoplane and phyllosphere bacteria and fungi isolated from rice in Kenya for plant growth promoters. SpringerPlus 2:606 Natheer SE, Muthukkaruppan S (2012) Assessing the in vitro zinc solubilization potential and improving sugarcane growth by inoculating Gluconacetobacter diazotrophicus. Ann Microbiol 62:435–441 Nawaz F, Khan N, Shah JA, Khan A, Liaqat A, Ullah S (2017) Yield and yield components of chickpea as affected by various levels of FYM and rhizobium inoculation. Pure Appl Biol 6:346– 351. https://doi.org/10.19045/bspab.2017.60033 Ngamau C, Matiru V, Tani A, Muthuri C (2014) Potential use of endophytic bacteria as biofertilizer for sustainable banana (Musa spp.) production. Afr J Hortic Sci 8:1–11 Ohyama T, Momose A, Ohtake N, Sueyoshi K, Sato T, Nakanishi Y, Asis CA, Ruamsungsri S, Ando S (2014) Nitrogen fixation in sugarcane. Adv Biol Ecol Nitrogen Fix 3:49–70 Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197 Olivares J, Bedmar EJ, Sanjuan J (2013) Biological nitrogen fixation in the context of global change. Mol Plant Microbe Interact 26:486–494 Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745

12 Endophytic Rhizobacteria for Mineral Nutrients …

287

Ouattara K, Coulibaly K, Konate I, Kebe BI, Tidou AS, Filali-Maltouf A (2019) Selection of Cocoa tree (Theobroma cacao Linn) endophytic bacteria solubilizing tri-calcium phosphate, isolated from seedlings grown on soils of six producing regions of Côte d’Ivoire. Biomed Life Sci 9:842–852 Ouma SO, Magiri EN, Maritu VN, Mugweru J, Ngamau C (2014) Evaluation of nitrogen fixation ability of endophytic bacteria in Kenyan bananas (Musa Spp.) using biochemical and molecular techniques. Int J Sci Technoledge 2:156–163 Pandey PK, Singh S, Singh MC, Singh AK, Yadav SK, Pandey AK, Heisnam P (2018) Diversity, ecology, and conservation of fungal and bacterial endophytes. In: Sharma S, Varma A (eds) Microbial resource conservation. Springer, Cham, pp 393–430 Patel A, Vyas RV, Mankad M, Subbash N (2017a) Isolation and biochemical characterization of rhizobia from rice rhizosphere and their effect on rice growth promotion. Int J Pure Appl Biosci 5:441–451 Patel DH, Naik JH, Amaresan N (2017b) Synergistic effect of root-associated bacteria on plant growth and certain physiological parameters of banana plant (Musa acuminate). Arch Agron Soil Sci 64:1021–1031. https://doi.org/10.1080/03650340.2017.1410703 Perez-Rosales E, Alcaraz-Melendez L, Puente ME, Vázquez-Juárez R, Quiroz-Guzmán E, ZentenoSavín T, Morales-Bojórquez E (2017) Isolation and characterization of endophytic bacteria associated with roots of jojoba (Simmondsia chinensis [Link] Schneid). Curr Sci 112:396–401. https:// doi.org/10.18520/cs/v112/i02/396-401 Pham VTK, Rediers H, Ghequire MGK, Nguyen HH, De Mot R, Vanderleyden J, Spaepen S (2017) The plant growth-promoting effect of the nitrogen-fixing endophyte Pseudomonas stutzeri A15. Arch Microbiol 199:513–517. https://doi.org/10.1007/s00203-016-1332-3 Phi QT, Yu MP, Keyung-Jo S, Choong-Min R, Seung-Hwan P, Jong-Guk K, Sa-Youl G (2010) Assessment of root-associated Paenibacillus polymyxa groups on growth promotion and induced systemic resistance in pepper. J Microb Biotechnol 20:1605–1613 Prakash J, Arora NK (2019) Phosphate-solubilizing Bacillus sp. enhances growth, phosphorus uptake and oil yield of Mentha arvensis L. 3 Biotech 9:126. https://doi.org/10.1007/s13205-0191660-5 Proença DN, Schwab S, Baldani JI, Morais PV (2017) Diversity and function of endophytic microbial community of plants with economical potential. In: De Azevedo JL, Quecine MC (eds) Diversity and benefits of microorganisms from the tropics. Springer, Cham, pp 209–243 Quecine MC, Araujo WL, Rossetto PB, Ferreira A, Tsui S, Lacava PT, Mondin M, Azevedo JL, Pizzirani-Kleiner AA (2012) Sugarcane growth promotion by the endophytic bacterium Pantoea agglomerans 33.1. Appl Environ Microbiol 78:7511–7518. https://doi.org/10.1128/AEM.008 36-12 Rafi MM, Krishnaveni MS, Charyulu PBBN (2019) Phosphate-solubilizing microorganisms and their emerging role in sustainable agriculture. In: Buddolla V (ed) Recent developments in applied microbiology and biochemistry. Academic Press, Dordrecht, pp 223–233 Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 153e160 Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149 Ramaswamy V, Boucher O, Haigh J, Hauglustaine D, Haywood J, Myhre G, Nakajina T, Solomon S (2001) Radiative forcing of climate change. Cambridge University Press, Cambridge, UK, pp 349–416 Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization and biofortification of zinc in soybean and wheat cultivated in vertisols of central India. Appl Soil Ecol 73:87–96. https://doi. org/10.1016/j.apsoil.2013.08.009 Rfaki A, Nassiri L, Ibijbijen J (2015) Isolation and characterization of phosphate solubilizing bacteria from the rhizosphere of faba bean (Vicia faba L.) in Meknes region. Morocco Microbiol Res J Int 6:247–254. https://doi.org/10.9734/BMRJ/2015/14379

288

B. N. Aloo et al.

Ribeiro VP, Marriel IE, Sousa SM, Lana UGP, Mattos BB, Oliveira CA, Gomes EA (2018) Endophytic Bacillus strains enhance pearl millet growth and nutrient uptake under low-P. Braz J Microbiol 49:40–46. https://doi.org/10.1016/j.bjm.2018.06.005 Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837 Ryan PR, Germaine KJ, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9 Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res 23:3984–3999 Sahu PK, Shivaprakash MK, Subbarayappa CT, Brahmaprakash GP (2018) Effect of bacterial Endophytes Lysinibacillus sp. on plant growth and fruit yield of tomato (Solanum lycopersicum). Int J Curr Microbiol Appl Sci 7:3399–3408 Saini R, Dudeja SS, Giri R, Kumar V (2015) Isolation, characterization, and evaluation of bacterial root and nodule endophytes from chickpea cultivated in Northern India. J Basic Microbiol 55:74– 81 Sandhya V, Shrivastava M, Ali SZ, Prasad VSK (2017) Endophytes from maize with plant growth promotion and biocontrol activity under drought stress. Russ Agric Sci 43:22–34 Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008 Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798. https://doi.org/10.1016/j.chemosphere.2006.07.067 Senthilkumar M, Anandham R, Madhaiyan M, Venkateswaran V, Sa T (2011) Endophytic bacteria: perspectives and applications in agricultural crop production. In: Maheshwari DK (ed) Bacteria in agribiology: crop ecosystems. Springer, Berlin, Heidelberg, pp 61–96 Sessitsch A, Hardoim PR, Döring J, Weilhater A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Sarkar A, Bodrossy L, Van Overbeek LS, Brar D, Van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36 Sev TM, Khai AA, Aung A, Yu SS (2016) Evaluation of endophytic bacteria from some rice varieties for plant growth promoting activities. J Sci Innov Res 5:144–148 Shabanamol S, Divya K, George TK, Rishad KS, Sreekumar TS, Jisha MS (2018) Characterization and in planta nitrogen fixation of plant growth promoting endophytic diazotrophic Lysinibacillus sphaericus isolated from rice (Oryza sativa). Physiol Mol Plant Pathol 102:46–54. https://doi. org/10.1016/j.pmpp.2017.11.003 Shaikh S, Saraf M (2017) Zinc biofortification: strategy to conquer zinc malnutrition through zinc solubilizing PGPR’s. Biomed J Sci Tech Res 1:224–226. https://doi.org/10.26717/BJSTR.2017. 01.000158 Shakeela S, Padder SA, Bhat ZA (2017) Isolation of phosphate solubilising rhizobacteria and endorhizobacteria from medicinal plant Picrorhiza kurroa and their optimization for tricalcium phosphate solubilization. The Pharma Inn 6:160–170 Sharifi P, Paymozd M (2016) Effect of zinc, iron and manganese on yield and yield components of green beans. Curr Opin Agric 5:15–18 Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587. https:// doi.org/10.1186/2193-1801-2-587 Sharma P, Kumawat KC, Kaur N (2014) Assessment of zinc solubilization by endophytic bacteria in legume rhizospheres. Microbiology 4:439–441 Shi Y, Yang H, Zhang T, Sun J, Lou K (2014) Illumina-based analysis of endophytic bacterial diversity and space-time dynamics in sugar beet on the north slope of Tianshan mountain. Appl Microbiol Biotechnol 98:6375–6385

12 Endophytic Rhizobacteria for Mineral Nutrients …

289

Shrivastava M, Srivastava PC, D’Souza SF (2018) Phosphate-solubilizing microbes: diversity and phosphates solubilization mechanism. In: Meena V (ed) Role of rhizospheric microbes in soil. Springer, Singapore, pp 137–165 Silva JM, Santos TMC, Albuquerque LS, Montaldo YC, Oliveira JUL, Silva SGM, Nascimento MS, Teixeiria RRO (2015) Potential of endophytic bacteria (Herbaspirillum spp. and Bacillus spp.) to promote sugarcane growth. Aust J Crop Sci 9:754–760 Silveira APDD, Sala VMR, Cardoso BN, Labanca EG, Cipriano MAP (2016) Nitrogen metabolism and growth of wheat plant under diazotrophic endophytic bacteria inoculation. Appl Soil Ecol 107:313–319. https://doi.org/10.1016/j.apsoil.2016.07.005 Sindhu SS, Sharma R, Sindhu S, Phour M (2019) Plant nutrient management through inoculation of zinc-solubilizing bacteria for sustainable agriculture. In: Giri B, Prasad R, Wu QS, Varma A (eds) Biofertilizers for sustainable agriculture and environment. Springer, Cham, pp 173–201 Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedback and mitigation options. Nat Rev Microbiol 8:779–790 Singh D, Geat N, Rajawat MVS, Prasanna R, Kar A, Singh AM, Saxena AK (2018) Prospecting endophytes from different Fe or Zn accumulating wheat genotypes for their influence as inoculants on plant growth, yield, and micronutrient content. Ann Microbiol 68:815–833. https://doi.org/ 10.1007/s13213-018-1388-1 Singh M, Singh D, Gupta AD, Pandey KD, Singh KP, Kumar A (2019) Plant growth promoting rhizobacteria. In: PGPR amelioration in sustainable agriculture. Elsevier, pp 41–66 Smith P, House JI, Bustamante M, Sobocká J, Harper R, Pan G, West PC, Clark JM, Adhya T, Rumpel C, Paustian K, Kuikman P, Cotrufo MF, Elliott JA, McDowell R, Griffiths RI, Asakawa S, Bondeau A, Jain AK, Meersmans J, Pugh TAM (2016) Global change pressures on soils from land use and management. Glob Change Biol 22:1008–1028. https://doi.org/10.1111/gcb.13068 Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419 Sreejith S, Aswani R, Radhakrishnan EK (2019) Agriculturally important biosynthetic features of endophytic microorganisms. In: Verma S, White J Jr (eds) Seed endophytes. Springer, Cham, pp 423–447 Steffen W, Richardson K, Rockstrom J, Cornell SE, Fetzer I, Bennett EM (2015) Planetary boundaries: guiding human development on a changing planet. Science 347:1259855. https://doi.org/ 10.1126/science.1259855 Suman A, Srivastava AK, Gaur A, Singh P, Singh J, Yadav RL (2008) Nitrogen use efficiency of sugarcane in relation to its BNF potential and population of endophytic diazotrophs at different N levels. Plant Growth Regul 54:1–11 Suman A, Yadav A, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh DP, Singh H, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity. Springer, New Delhi, pp 117–143 Szilagyi-Zecchin VJ, Ikeda AC, Hungria M, Adamoski D, Kava-Cordeiro VK, Glienke C, GalliTerasawa LV (2014) Identification and characterization of endophytic bacteria from corn (Zea mays L.) roots with biotechnological potential in agriculture. AMB Express 4:1–9. https://doi. org/10.1186/s13568-014-0026-y Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, Newman L, Monchy S (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLOS Genet 6:e1000943 Taurian T, Anzuay MS, Luduena L, Angelini JG, Munoz V, Valetti L, Fabra A (2013) Effects of single and co-inoculation with native phosphate solubilising strain Pantoea sp J49 and the symbiotic nitrogen fixing bacterium Bradyrhizobium sp SEMIA 6144 on peanut (Arachis hypogaea L.) growth. Symbiosis 59:77–85 Tavallali V, Rahemi M, Eshghi S, Kholdebarin B, Ramezanian A (2010) Zinc alleviates salt stress and increases antioxidant enzyme activity in the leaves of pistachio (Pistacia vera L’.Badami’) seedlings. Turk J Agric For 34:349–359

290

B. N. Aloo et al.

Thirumal G, Reddy RS, Triveni S, Nagaraju Y, Prasannakumar B (2017) Screening of native Rhizobia and Pseudomonas strains for plant growth promoting activities. Int J Curr Microbiol Appl Sci 6:616–625 Tkacz A, Cheema J, Chandra G, Grant A, Poole PS (2015) Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. Multidiscip J Microb Ecol 9:2349– 2359. https://doi.org/10.1038/ismej.2015.41 Tsegaye Z, Assefa F, Beyene D (2017) Properties and application of plant growth promoting rhizobacteria. Int J Curr Trends Pharmacobiology Med Sci 2:30–43. https://doi.org/10.15413/ ajmr.2017.0104 Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209. https://doi. org/10.1186/gb-2013-14-6-209 Upreti R, Thomas P (2015) Root-associated bacterial endophytes from Ralstonia solanacearum resistant and susceptible tomato cultivars and their pathogen antagonistic effects. Front Microbiol 6:1–12 Varma PK, Uppala S, Pavuluri K, Chandra KJ, Chapala MM, Kumar KVK (2017) Endophytes: role and functions in crop health. In: Singh D, Singh H, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 291–310 Velázquez E, Silva LR, Ramírez-Bahena MH, Peix A (2016) Diversity of potassium-solubilizing microorganisms and their interactions with plants. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, India, pp 99–110 Vendan RT, Yu YJ, Lee SHH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J Microbiol 48:559 Verma P, Yadav AN, Kazy SK, Saxena AK, Suman A (2013) Elucidating the diversity and plant growth promoting attributes of wheat (Triticum aestivum) associated acidotolerant bacteria from Southern hills zone of India. Natl J Life Sci 10:219–226 Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK, Suman A (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the Northern hills zone of India. Ann Microbiol. https://doi.org/ 10.1007/s13213-014-1027-4 Verma M, Mishra J, Arora NK (2019) Plant growth-promoting rhizobacteria: diversity and applications. In: Sobti R, Arora NK, Kothari R (eds) Environmental biotechnology: for sustainable future. Springer, Singapore, pp 129–173 Waghunde RR, Shelake RM, Shinde MS, Hayashi H (2017) Endophyte microbes: A weapon for plant health management. In: Microorganisms for Green Revolution. Singapore, pp 303–325 Walia A, Shirkot CK (2012) Screening of PGPR to promote early growth of tomato seedlings. Lap Lambert Academic Publishing, Deutschland Walia A, Guleira S, Chauhan A, Mehta P (2017) Endophytic bacteria: role in phosphate solubilization. In: Maheshwari DK, Annapuma K (eds) Endophytes: crop productivity and protection. Springer, Cham, pp 61–93 Walitang D, Samaddar S, Choudhary A, Chatterjee C, Ahmed S, Sa T (2019) Diversity and plant growth promoting potential of bacterial endophytes in rice. In: Sayyed R, Reddy M, Antonius S (eds) Plant growth promoting rhizobacteria (PGPR): prospects for sustainable agriculture. Springer, Singapore, pp 3–17 Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267 Wei CY, Lin L, Luo LJ, Xing YX, Hu CJ, Yang LT, Li YR, An Q (2014) Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol Fertil Soils 50:657–666 Yagedari M, Farahani GHN, Mosadeghzad Z (2012) Biofertilizers effects on quantitative and qualitative yield of Thyme (Thymus vulgaris). Afr J Agric Res 7:4716–4723 Yaish MW, Antony I, Glick BR (2015) Isolation and characterization of endophytic plant growthpromoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in

12 Endophytic Rhizobacteria for Mineral Nutrients …

291

salinity tolerance. Antonie Van Leeuwenhoek 107:1519–1532. https://doi.org/10.1007/s10482015-0445-z Yasmin S, Zaka A, Imran A, Zahid MA, Yousaf S, Rasul G, Arif M, Mizra MS (2016) Plant growth promotion and suppression of bacterial leaf blight in rice by inoculated bacteria. PLoS ONE 11:e0160688 Youseif SH (2018) Genetic diversity of plant growth promoting rhizobacteria and their effects on the growth of maize plants under greenhouse conditions. Ann Agric Sci 63:25–35. https://doi. org/10.1016/j.aoas.2018.04.002 Zhang A, Zhao G, Gao T, Wang W, Li J, Zhang S, Zhu B (2013) Solubilization of insoluble potassium and phosphate by Paenibacillus kribensis CX-7: a soil microorganism with biological control potential. Afr J Microbiol Res 7:41–47

Chapter 13

Plant Growth-Promoting Bacteria: Effective Tools for Increasing Nutrient Use Efficiency and Yield of Crops Chitra Pandey, Shrivardhan Dheeman, Deepti Prabha, Yogesh Kumar Negi, and Dinesh Kumar Maheshwari Abstract Agrochemicals or fertilizers are essential to optimize crop production but their excessive and unwanted application is posing a myriad of adverse effects such as declining soil fertility besides contaminating surface and groundwater. These synthetic chemicals mismanage the soil ecology leading to disturbed ecosystem and loss of beneficial bacteria inhabiting in soil. Traces of such chemicals have also been deposited in agricultural products that cause serious illnesses in human beings. Considering such facts, the use of plant growth-promoting bacteria (PGPB) renamed as plant beneficial bacteria being promoted to enhance nutrient availability, plant growth, and yield promotion to maintain sustainable agriculture. These bacteria have been in use for a long time for increasing plant growth and development and to reduce the subsistence farmer’s dependence on agrochemicals. The scientific community observed that beneficial effects are now befitting for the sustainable growth promotion and crop yield enhancement due to the influence of PGPR in order to augment nutrient uptake capacity and nutrient use efficiency. The aim of the present study is focusing on the PGPRs which work as a tool to enhance nutrient use efficiency of various crops. Long-term application of such bacteria could act as a newer alternative to C. Pandey Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India e-mail: [email protected] S. Dheeman Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Balawala, Dehardun, India S. Dheeman · D. K. Maheshwari Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India D. Prabha Department of Seed Science and Technology, Chauras Campus, HNB Garhwal University, Srinagar, Uttarakhand, India Y. K. Negi (B) Department of Basic Sciences, College of Forestry (VCSG UUHF), Ranichauri, Tehri Garhwal, Uttarakhand, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_13

293

294

C. Pandey et al.

chemical fertilizer and able to cope its adverse effects on both soil and ecology and reverse plant–soil ecosystem. Keywords PGPR · Crop yield · Rhizosphere · Nutrient management

13.1 Introduction Agriculture has been and will continue to be the backbone of food availability and food security. It directly sustains the livelihood of about two-third of the global population, and is the lifeline of agro-industries. However, over time, the sustainability of agricultural growth has emerged as a central issue confronting many countries in the world. This issue has become even more important as the pressure on land and other natural resources has increased manifold with an increase in population and per capita consumption of food grains (Negi 2005). As the world population is dwelling, food availability has to be increased corresponding to meet out the increasing food demand. The current world population of 7.6 billion and is expected to reach 8.6 billion in the year 2030 and 9.8 billion in 2050 (UNDESA 2017). Therefore, the use of agrochemicals has become important to sustain agriculture production and fulfill the food requirement of all human beings worldwide. Initially, the use of these chemicals was much promoted among the farmers to grow the crops at their best. However, their long-term headforemost application results in low soil fertility and increases the dependency of farmers on these agrochemicals. Farmers use a variety of agrochemicals and depend on them for the successful production of their crops. Another constraint of agriculture production is decreasing land availability for farming. This will further lead to the enhancement of nutrient load per unit area in soil. The depletion of nutrients in the soil is, therefore resulting in poor plant growth and productivity. Plants require 16 essential nutrients or elements for adequate growth and production. Three of these, carbon (C), oxygen (O), and hydrogen (H) are drawn from water and the air. The remaining elements are taken up from the soil (Gellings and Parmenter 2016). These nutrients have been divided into three categories viz. macronutrients, micronutrients, and trace elements (Table 13.1). Crop health and productivity depend on the availability of these nutrients and their uptake as well. However, this is well known that most of the nutrients in the soil are present in complex or unavailable forms. Inorganic fertilizers are thus manufactured in plant-available forms. Therefore, as these fertilizers are amended in soil, the nutrients get quickly released and become available for plant uptake. Fertilizers undoubtedly increase productivity and fulfill the food demand but, at the same time, their adverse effects on soil, environment, and human beings increase many-fold. Unfortunately, residual accumulation of these harmful chemicals in grains, fruits, and other edible parts has been reported in recent years by many researchers (Bhanti and Taneja 2007; Gurusubramanian et al. 2008; Singh et al. 2008). Consumption of such contaminated produces may cause serious health problems (e.g., allergic reactions, intestinal disorders, hormonal imbalance, and even cancer) in human beings

13 Plant Growth-Promoting Bacteria …

295

Table 13.1 Plant nutrients and their role S.

Nutrient types

Element

Role in plant growth

no. 1.

Macronutrients Nitrogen (N) (Required in large quantities and their deficiency or unavailability affect plant survival) Phosphorous (P)

Potassium (K)

2.

3.

Micronutrients Calcium (Ca) (Required in fewer amounts and their deficiency or unavailability may result in poor plant health and low productivity)

The basic component of proteins and chlorophyll. Plays an essential role in plant growth Plays an important role in root growth and promotes the establishment of young plants, flowering, fruiting and ripening, photosynthesis, respiration, and overall plant growth Promotes the movement of sugars, turgor, and stem rigidity. It also increases the plant’s overall resistance to cold, diseases, insect pests, etc. Promotes the formation of flower buds, the hardening off of woody plants, and fruiting It plays a vital role in plant structure because it is part of cell walls and holds them together. Promotes the development of the root system and the ripening of fruit and seeds. Also, found in the growing parts of plants (apex and buds)

Magnesium (Mg)

An important part of chlorophyll. Helps in fruit ripening and seed germination. Reinforces cell walls and promotes the absorption of phosphorous, nitrogen, and sulfur by plants

Sulfur (S)

A component of several proteins, enzymes, and vitamins. Contributes to chlorophyll production. It helps plants absorb potassium, calcium, and magnesium

Trace elements Iron (Fe) (Required in very fewer amounts and their deficiency or unavailability may result in poor metabolic functions, health, and Boron (B) low productivity)

Essential for chlorophyll production. It also contributes to the formation of some enzymes and amino acids Essential to overall plant health and tissue growth. Promotes the formation of fruit and the absorption of water (continued)

296

C. Pandey et al.

Table 13.1 (continued) S.

Nutrient types

Element

Role in plant growth

Manganese (Mn)

Promotes seed germination and speed-up plant maturity. Plays an important role in photosynthesis by contributing to chlorophyll production. Essential for nitrogen assimilation and protein formation

no.

Molybdenum (Mo) Essential for nitrogen assimilation by plants and nitrogen fixation by bacteria. This means that it is needed for the production of nitrogen-based proteins Chlorine (Cl)

Stimulates photosynthesis

Copper (Cu)

Activates various enzymes. It also plays a role in chlorophyll production

Zinc (Zn)

Plays an important role in the synthesis of proteins, enzymes, and growth hormones

(Bhanti and Taneja 2007; Singh et al. 2008). Another side of the coin is that the fertility of the soil has decreased over time resulting in decreased productivity due to deprived soil nutrients. So many chemicals are there in use to control pests, insects, and pathogens with an instant effect. However, irrelevant and indiscriminative use of these chemicals is leading to a very harmful effect on human health (Lawrence et al. 2004; Chaturvedi et al. 2013), soil environment (Aktar et al. 2009; Lin et al. 2019; Tiryaki and Temur 2010), and animals (Dalvie et al. 2011; Odukkathil and Vasudevan 2013). It is well known that (i) these chemicals are recalcitrant and not fully degradable, and (ii) their degradation depends on their half-life, the amount applied, chemical reaction, etc. (Pandey et al. 2017). All these factors have arisen questions among the scientific community, environmentalists, and social organizations regarding food security, soil, water, and air pollution, crop nutrition, soil fertility, etc. These problems provoked the scientific community to search for environment-friendly commercial alternatives that could act as good as chemicals to increase soil fertility and crop productivity to ensure food security. A large number of publications have appeared during the last decade on the use of plant growth-promoting bacteria (PGPR), organic manures, botanicals, etc., and come up as a vivacious and viable alternative to agrochemicals. Such biological alternatives not only enhance the nutrient availability but also increase their uptake by host plants. Besides this, PGPRs secrete plant

13 Plant Growth-Promoting Bacteria …

297

growth hormones, antibacterial and antifungal metabolites, induce systemic resistance against many diseases and thereby ensure higher crop production and another advantage of these microbes is that they can be applied with other biological inputs.

13.1.1 Organic Manures: An Alternative Source of Plant Nutrients Generally, plant and animal residues or by-products come under this category such as compost, manure, and animal residues. Being organic, these fertilizers have a good amount of different nutrients and therefore increase soil fertility (Li et al. 2018). Unlike inorganic chemicals, these fertilizers do not show any harmful effects on plants or human beings. Also, they are biodegradable, renewable, and sustainable. However, beneficial microorganisms help in the adequate release of nutrients in the soil from these fertilizers. Their strategic use may not only enhance the crop production but also improves the soil quality and fertility. Organic manures viz., FYM, vermicompost, poultry compost, cattle dung, etc., improve the physical properties of soil (water hold-ing capacity, soil aeration, soil aggregation, etc.), prevent soil degradation and increase the population of beneficial soil microorganisms. These organic amendments contain most of the nutrients in a plant-available form such as nitrates, phosphates, exchangeable calcium, zinc, and soluble potassium (Orozco et al. 1996). Similarly, forest litter also plays a fundamental role in nutrient turnover and the transfer of energy between plants and soil. This is also a good source of the nutrients that are accumulated in the upper layers of the soil. FYM is used in between 10 and 30 t ha−1 in different crops including cereals, pulses, vegetables, etc. Vermicompost and Forest litter are used 6–10 t ha−1 . However, the rate of application of organic manures can be reduced if applied along with microbial inoculants biofertilizers. Several reports suggest a 25–50% reduction in organic manure requirements if beneficial microbes are combined with them (Yildrim et al. 2011; Singh et al. 2015; Rahman et al. 2018).

13.2 Plant Growth-Promoting Bacteria Although, much has been said about PGP bacteria (Maheshwari 2011; Maheshwari et al. 2015, 2017) it is pertinent to give a brief description about their role and efficacy. Plant growth-promoting rhizobacteria (PGPR) are the beneficial bacteria closely associated with plant rhizosphere and possess plant growthpromoting abilities (Kloepper and Schroth 1978). These are used to improve soil fertility and crop productivity and also as biocontrol agents to reduce crop losses. To commemorate their spectrum of action, they are designated with several terms

298

C. Pandey et al.

including plant growth-promoting bacteria, plant health-promoting bacteria, bioinoculant, biofertilizers, biocontrol agents, etc. PGPRs generally represent a wide range of root colonizing bacteria belonging to Azotobacter, Azospirillum, Bacillus, Burkholderia, Rhizobium, Pseudomonas, Serratia, etc. Along with plant growth promotion, they reforest eroded areas, restore the contaminated sites, and thereby render a positive effect on the degraded soil ecosystem (Gupta et al. 2015). It seems inevitable that fewer agrochemicals with their low dosages will be used in the coming time and more emphasis would be put on the use of environmentally and biologically safe alternatives including the use of beneficial microbes. PGPRs have been found successful in getting established in the soil ecosystem due to their high adaptability in a wide variety of environments, faster growth rate, and biochemical versatility to metabolize a wide range of natural and xenobiotic compounds. Successful studies using PGPRs including genera Acinetobacter, Alcaligenes, Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Caulobacter, Chromobacterium, Enterobacter, Erwinia, Flavobacterium, Micrococcus, Rhizobium, Serratia, Xanthomonas, Proteus, and Pseudomonas on the growth enhancement of various crops have been achieved in laboratory and field conditions (Glick 1995; Gray and Smith 2005; Verma et al. 2010; Negi et al. 2011; Maheshwari et al. 2015; Agarwal et al. 2017b) in Table 13.2. PGPRs produce growth hormones, enzymes, and other metabolites that facilitate solubilization of soil nutrients (phosphate, nitrogen, potassium, etc.) and thereby enhance nutrient uptake with subsequent augmentation of the plant growth (Baligar et al. 2001; Mishra et al. 2009). The interaction between plant, soil, and microbes is influenced by abiotic (physical, chemical) and biotic (soil biota) factors (Jackson and Prat 1996; Putten et al. 2013). Abiotic factors such as temperature (low and high), high salt, pH, soil fertility, moisture content have been reported to influence enzyme activities nutrient, concentration (Chapin 1980), and nutrient uptake (Gavito et al. 2001) which have shown to affect plant growth directly or indirectly (Heinze et al. 2017). Plant growth-promoting bacteria secrete various phytohormones such as GA (Bottini et al. 2004; Hayat et al. 2010), IAA (Spaepen et al. 2007), Cytokinin, Salicylic acid (Jochum et al. 2019), abscisic acid (Cohen et al. 2015). Phytohormones like auxins, cytokinins, and gibberellin production have been observed for the significant enhancement of seedling parameters (Melnykova et al. 2013; Talboys et al. 2014). The broad spectrum antagonistic activities of PGPRs are executed by secretion of several metabolites including antibiotics (Guo et al. 2014; Lee et al. 2016), volatile compound HCN (Khabbaz et al. 2015), siderophores (Kesaulya et al. 2018), enzymes chitinase and β-1, 3-glucanase, etc. (Huang et al. 2005). These beneficial microbes can easily be applied in different crops by seed, root treatments, foliar sprays, mixing in soil or organic manure, etc., to various crop plants (Fig. 13.1). The demerits include (i) requirements for long-term storage, and (ii) generally crop-specific or site-specific.

13 Plant Growth-Promoting Bacteria …

299

Table 13.2 Different PGPR strains found effective to increase plant growth of various crops S. no.

Bacterial strains used

Crop

References

1.

Pseudomonas fluorescence (ATCC13525)

Vigna radiata

Katiyar and Goel (2004)

2.

Pseudomonas putida (B0)

Zea mays var. QPM-1

Pandey et al. (2006)

3.

Serratia marcescens SRM (MTCC 8708)

Curcurbita pepo

Selvakumar et al. (2007)

4.

Serratia marcescens SRM

Triticum sp. cv. VL 802 Selvakumar et al. (2008)

5.

Acinetobacter rhizosphaerae BIHB 723

Pisum sativum var. Palam priya, Zea mays var. Girija, Hordeum vulgare var. Dolma

Gulati et al. (2009)

6.

Pseudomonas spp.

Triticum aestivum L.

Mishra et al. (2011)

7.

Pseudomonas fluorescence

Phseolus vulgaris var Pusa contendor

Negi et al. (2011)

8.

Rhizobium, Pseudomonas, Serratia, Bradyrhizobium japonicum-SB1, Bacillus thuringiensis KR1

Lens culinaris Medikus Kaur et al. (2015)

9.

Pseudomonas sp. JJS2, Enterobacter sp. AAB8

Cajanus cajan (L.) and Shukla et al. Eleusine coracana (2015)

10.

Rhizobium sp.

Lentil (Lens culinaris Medikus)

Singh et al. (2018)

11.

Bacillus subtilis and B. pumilus

Amaranthus hypochondriacus

Pandey et al. (2018a, b)

13.2.1 Potential Role of Microbes in Nutrient Availability Plant growth-promoting bacteria are known for their ability to increase nutrients concentration in rhizospheric and non-rhizospheric soil. PGPR can increase phosphorus, nitrogen, potassium, and other micronutrients concentration in the soil (Vejan et al. 2016). These nutrients are in unavailable form in the soil and PGPR achieve availability of these by solubilization, due to siderophore production and oxidation of sulfur, etc. A significant amount of nitrogen (from 20 to 22 TgN per year up to 40 Tg N per year) has been contributed to the agriculture system due to N-fixation (Galloway et al. 2008; Herridge et al. 2008). Other nutrients such as Fe and Zn are also required to increase plant growth, and PGPR increases the availability by using different mechanisms. Zn mobilizing bacteria have been observed to increase Zn uptake along with the crop yield (Ramesh et al. 2014; Shakeel et al. 2015). The isolation, identification, and characterization of Zn and K solubilizing bacteria

300

C. Pandey et al.

Fig. 13.1 Effects of PGPR applications on plants

have been reported. Along with that PGPR (Microbacterium oxydans JYC17, Pseudomonas thivervalensis Y1-3-9, and Burkholderia cepacia J62) having metal resistance increased Cu uptake (maximum 113.38%) by Rape plant and improved copper remediation capacity and also increased antioxidant content in leaves, the biomass of remediation plant (Ren et al. 2019). Canbolat et al. (2006) reported a significant effect of Bacillus M-13 and Bacillus RC01 on nitrogen fixation and phosphate solubilization and increased availability promotes the uptake of these nutrients by barley (Hordeum vulgare). In another case, Maize plant grew on nutrient-deficient calcisol soil when treated with the Pseudomonas alkaligenes PSA15, Bacillus polymyxa BcP26, and Mycobacterium phlei MbP18, improved soil nutrients and uptake of the nutrients (N, P, K), was observed. Bacterial inoculants have been observed as a better plant growth promoter in nutrient-deficient soil (Egamberdiyeva 2007). Strains of Pseudomonas fluorescens, Pseudomonas putida, and Pseudomonas fluorescens were found effective to increase nutrient uptake and field in paddy (Lavakush et al. 2014). Recently, Pandey et al. (2018a) reported that biopriming of amaranth seeds by the selected Bacillus isolates exhibited a significant increase in all three macronutrients (N: 36.18%, P: 32.45%, K: 17.11%) in soil. Authors also reported that the higher solubilization and availability of these nutrients significantly increased the grain yield in Amaranthus hypochondriacus.

13 Plant Growth-Promoting Bacteria …

301

13.2.2 Nutrient Use Efficiency (NUE) Nutrient use efficiency reflects the ability of a plant to use the available nutrients at its maximum potential. It can be defined as yield (biomass) per unit input of fertilizer/nutrient content). NUE, therefore, depends on the plant’s ability to take up nutrients efficiently from the soil but also depends on internal transport, storage, and remobilization of nutrients. NUE is a critically important concept for evaluating crop production systems and can be greatly impacted by fertilizer management (Baligar et al. 2001). It is classified into four different subtypes (i) Agronomic efficiency, (ii) Physiological efficiency, (iii) Apparent recovery efficiency, (iv) Utilization efficiency as described in Table 13.3 (Baligar et al. 2001). Nutrient use efficiency of chemical fertilizers is very low which ultimately leads to increased fertilizer amount in the field and subsequently, that remaining fertilizer vanished in the environment. Even if fertilizer could apply in an adequate amount, plants use only 50% and the remaining 50% leached out in the environment, for instance, plant uptake 50% of nitrogen fertilizer and remaining polluting water (Chandini et al. 2019). Since plants primarily depend on soil for all their nutrients, it is important to make them available in a utilizable form. Different nutrients have their specific role in plant growth and development and therefore, must be available at the required concentration. By the application of agrochemicals, farmers try to amend the soil with sufficient nutrients. Therefore, it is necessary to manage the nutrient application Table 13.3 Types of Nutrient use efficiency S. no. 1.

Type of nutrient use efficiency Physiological efficiency (PE)

Definition and description Physiological efficiency is defined as the Yield F (kg) Yield C (kg) Nutrient uptake F (kg)

Nutrient uptake C (kg)

Where Yield F is the biological yield of a fertilized plot (kg), Yield C is the biological yield of an unfertilized plot (kg), Nutrient uptake F is nutrient uptake of a fertilized plot (kg), Nutrient uptake C is nutrient uptake of an unfertilized plot (kg) 2.

Agronomic efficiency (AE)

Grain Yield F (kg) Grain Yield C (kg) Quantity of nutrient applied (kg) Agronomic efficiency expressed as the additional amount of economic yield per unit nutrient applied

3.

4.

Apparent recovery efficiency (ARE)

Utilization efficiency (EU)

Source Baligar et al. (2001)

Nutrient uptake F (kg)

Nutrient uptake C (kg)

Quantity of nutrient applied (kg) ARE has been used to reflect the plant’s ability to acquire applied nutrients from the soil Nutrient utilization efficiency was calculated by formula: EU (kg/kg) = PE X ARE

302

C. Pandey et al.

and also to increase the plant potential to produce more with the recommended dose of fertilizers. This is quite possible by increasing the “Nutrient use efficiency” (NUE) of the plants. It is the key component to enhance crop productivity. Generally, the NUE is crop or variety-specific but, there are reports, which suggest that PGPRs can effectively increase the NUE in different plants, result in higher crop productivity and nutrient quality. Recent research on plant–microbe interaction has revealed that PGPRs affect the ability of host plants to efficiently utilize the absorbed nutrients and increase yield and nutritive quality of the produce (Pandey et al. 2018a, b; Rahman et al. 2018).

13.2.3 PGPRs in NUE Enhancement High crop yield is the result of adequate availability of nutrients in the soil and their optimum uptake and accumulation in the plant systems. This, in turn, may enhance the NUE of the plant. It has been reported that PGPR provides the optimum level of nutrients to the plants and thereby increasing plant growth and yield (Pandey et al. 2018b; Rahman et al. 2018). Usually, nutrients are present in the soil but, generally, they remain in plant unavailable form and PGPRs can convert them into the available form (Adesemoye and Kloepper 2009). PGPR group of bacteria are soluble in nature. Some of the bacterial genera increase soil N, P, and K availability by solubilization and fixation reaction. PGPRs possess different mechanisms for higher nitrogen availability which include ammonification, nitrification, denitrification, mineralization, etc. (Ogunseitan 2005). A diverse range of PGPRs are known to enhance nitrogen use efficiency, for instance, Acetobacter, Azoarcus, Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Nitrobacter, Nitrosomonas, Rhizobium, etc. (Table 13.4). Nitrogen use efficiency is the plants’ ability to utilize available nitrogen in the field to enhance plant growth and productivity. To achieve the best NUE scientific researches were based on 4R principle, i.e., right source, right rate, right time, and right placement. NUE depends on the transport, storage, recycling, remobilization, and plant growth stage along with the nutrient uptake. The synchronization of nitrogen availability with nitrogen demand can increase nitrogen use efficiency significantly. Spolaor and coworkers (2016) suggested consortium of A. brasilense Ab-V5 + V6 and consortium of A. brasilense Ab-V5 and Rhizobium sp 53GRM1 to be effective to enhance the NUE of popcorn and enhanced the grain yield. Zeffa et al. (2019) applied A. brasilense Ab-V5 to improve maize growth and concluded that it increased NUE in N limiting conditions along with the improved root architecture, N assimilation, uptake, and increased biomass. Authors concluded that the morphological and structural changes in the plant occured because of the production of phytohormones by A. brasilense Ab-V5. Ahmad et al. (2017) reported that the PGPR impregnation with the DAP and urea enhanced nitrogen and phosphorus use efficiency of wheat and thereby increased photosynthetic rate, growth, and yield.

Enhancement in nutrient use efficiency. Rice (Oryza sativa) Enhancement in nitrogen use efficiency. Sunflower (Helianthus annuus) Increased N, P uptake and nutrient use efficiency High nutrient uptake and nutrient use efficiency. High nitrogen, phosphorus and potassium uptake, increased nutrient use efficiency. High nitrogen, phosphorus and potassium uptake, increased nutrient use efficiency. Also, high residual availability of nutrients after crop harvest

Burkholderia cepacia RRE25

Pseudomonas aeruginosa QS-40

Bacillus amyloliquifaciens IN937a, Bacillus pumilus T4

Pseudomonas fluorescens, Bacillus megaterium, Azospirillum brasilense

Pantoea agglomerans, Rahnella aquatilis and Pseudomonas orientalis

Bacillus subtilis and B. pumilus

Amaranth (Amaranthus hypochondriacus)

Rice (Oryza sativa)

Maize (Zea maizae)

Tomato (Solanum lycopersicum)

Wheat (Triticum aestivum)

Nutrient uptake

Pseudomonas sp.

Crop

NUE/nutrient uptake

PGPR

Table 13.4 Plant growth-promoting bacteria reported to enhance nutrient use efficiency and nutrient uptake

Pandey et al. (2018b)

Khanghahi et al. (2018)

Gulnaz et al. (2017)

Fan et al. (2017)

Arif et al. (2017)

Singh et al. (2013)

Shaharooma et al. (2008)

Reference

13 Plant Growth-Promoting Bacteria … 303

304

C. Pandey et al.

Wu et al. (2005) evaluated the effect of biofertilizers (AMF, A. chroococcum, B. megaterium, B. mucilaginous) on the maize growth and its nutritional properties and reported enhanced growth, soil properties, and nutritional value (total N, P and K). Increased N and P use efficiency was reported when the wheat plant was treated with P. fluorescens ACC50 and P. fluorescens biotype F (ACC73) (Shaharooma et al. 2008). Arif et al. (2017) observed that the combination of N-enriched compost and P. aeruginosa increased uptake efficiency of a sunflower plant, and a significant difference was observed in seed and quality of oil. Study also revealed that the inoculation of wheat by Azospirillum spp. effectively enhanced P and N use efficiency of wheat along with increased grain yield (Kivi et al. 2014). Ahmad et al. (2017) reported that the combination of PGPRs with a decreased amount of urea and DAP increases plant growth, yield (20%) along with nitrogen, and phosphorus use efficiency of wheat. This can be helpful to heel decreased soil fertility slowly and can add beneficial microbes in the soil. Bacteria in agrobiology have multifarious role including nutrient efficiency in crop plants (Maheshwari et al. 2013). Phosphate solubilizing microbes were found as an effective tool for providing applied nutrients to the rice, few genera, and bean. They increased nutrient uptake (N, P, K) and NUE (Duarah et al. 2011). Those PGPRs having phosphate solubilizing, IAA producing, and disease suppressing ability are known to enhance nutrient uptake and nutrient use efficiency as reported by various workers. According to their study N, P, K uptake, and use efficiency of rice plants increased due to application of hyperproducing IAA mutants of Burkholderia cepacia (RRE25), Bacillus cereus, Brevibacillus reuszeri, and Rhizobium rubi have been reported to increase growth and organic manure use efficiency of strawberry (Karlidag et al. 2009). A concurrent increase in wheat productivity and uptake of N and P was observed by the application of consortium of P. striata, A. chroococcum, and Glomus fasciculatum. Moreover, increased uptake leads to augmented nutrient use efficiency (Khan and Zaidi 2007). PGPRs also influence the micronutrient availability for the plants by using different mechanisms: Root exudates alteration by the symbiotic and non-symbiotic association with their respective host plants; enhancement of soil nutrient availability by increasing the solubility (Adesemoye and Kloepper 2009; Fitter et al. 2011). The plant growth significantly influenced by the micronutrients along with the macronutrients supported metabolic and enzymatic activities in the plant. The effects of PGPRs on nutrient availability and their use efficiency are depicted in Fig. 13.2. In this context, Shabayev (2012) studied the effect of PGPRs and reported increased iron and zinc contents in wheat while Sharma et al. (2015) demonstrated that P. putida and Bacillus sp. BN30 treatment enhanced zinc content rice. Increased Zn content was observed in Jaya and Pusa basmati-1 varieties of rice when treated with Bacillus sp. BN30. Recently, Adak et al. (2016) studied the effect of PGPRs on micronutrient enhancement and reported an increase in iron and zinc content in rice. On the other hand, Pandey et al. (2018b) observed a positive correlation between different treatments and NUE on amaranth using PGP bacilli. The study depicts that NUE of amaranth for N, P, and K were increased with different treatments that would

13 Plant Growth-Promoting Bacteria …

305

Fig. 13.2 Effects of PGPR treatments on nutrient availability, plant growth, and yield

have facilitated their better utilization through different biochemical and metabolic processes to produce higher crop yield.

13.3 Impact on Crop Yield Enhancement PGPRs ameliorate plant health and productivity by enhancing the nutrient status of soil and host plants (Dey et al. 2004). The bioavailability of nutrients and their increased uptake may significantly enhance the nutrient use efficiency of plants. Increased solubilization of nutrients (macro and micro) by PGPRs enhanced their uptake and accumulation (Parmar and Patel 2009; Dhiman et al. 2019; Bhatt and

306

C. Pandey et al.

Maheshwari 2019). Nutrient availability has been influenced by solubilization, chelation, and oxidation-reduction reaction in soil (de Santiago et al. 2011). Several workers (Puente et al. 2004; Sharma et al. 2012; Prasanna et al. 2013) studied the nutrient enhancement and nutrient availability in the soil as well as in plants that resulted in the bacterial inoculation. Goteti et al. (2013) observed a significant enhancement in nitrogen and phosphorus contents of the maize when inoculated with Bacillus sp. in comparison to that of plants treated with Pseudomonas spp. This implies that PGPRs competence strongly enhanced crop growth with nutrients as well. Han et al. (2006) and Supanjani et al. (2006) applied two species of bacilli, i.e., Bacillus megaterium var. phosphaticum and Bacillus mucilaginosus in nutrient-limited stressed soil where the strains increased bioavailability of minerals, their uptake and thereby enhanced growth of pepper and cucumber. In the same year, Hafeez et al. (2006) suggested the use of Bacillus pumilus as a bioinoculant to promote the crop yield in wheat. Beneduzi et al. (2008) reported Bacillus isolate SVPR30 as an efficient bioinoculant for growth enhancement of the rice. On the other hand, Zongzheng et al. (2010) also evaluated the growth promoter effect of Bacillus subtilis SY1. Their study revealed a significant increase in seedling parameters such as sprout tendency, germination percentage, sprout index, and vigor index. Bacillus isolates exhibited good PGP activities and significantly influenced seedling length, fresh weight, and dry weight of cowpea (Thomas et al. 2010). Bacillus sp. RM-2 was reported to enhance the seedling value parameters of cowpea with an increase in the number of seeds, the weight of seeds, and total grain weight (Minaxi et al. 2011). Agrawal and Agrawal (2013) reported the growth promotion of tomato by Bacillus sp. showing PGP traits. In the same year, Mehta et al. (2015) supported the fact of planting value parameter enhancement by the treatment of bioinoculants. Significant increase in seed germination, shoot length, root length, shoot dry weight, root dry weight, along with an increase in nitrogen, potassium, and phosphorus was observed after the application of Bacillus circulans CB7. Dubey et al. (2014) suggested that the combination of a half dose of chemical fertilizers with the Bacillus BSK17 was effective for the growth promotion of Cicer aerietinum and reported a significant increase in germination, yield. Recently, Refish et al. (2016) accounted for the role of Bacillus subtilis BS87 in the growth promotion of Anoectochilus roxburghii and A. formosanus. Similarly, multifarious bacilli influence was reported to influence the growth promotion of different crops such as Curcuma longa (Chauhan et al. 2016), Fagopyrum esculentum (Agarwal et al. 2017b). Awasthi et al. (2011) recorded enhanced growth and biomass yield of Artemisia annua L. (Asteraceae) when treated with the consortium of Glomus mosseae and B. subtilis. Biocoenotic consortium of P. aeruginosa KRP1 and B. licheniformis was suggested for bioformulation to enhance the productivity of Brassica campestris by Maheshwari et al. (2015). Recently, Vurukonda et al. (2016) evaluated the effect of a consortium of B. cereus, B. subtilis, and Serratia spp. on cucumber plants that exhibited darker green leaves, fewer wilt symptoms increased chlorophyll content and drought resistance. Kumar et al. (2016) suggested consortium of Bacillus spp., Pseudomonas spp., and R. leguminosarum in enhancement for the growth and grain yield of Phaseolus vulgaris. These PGPRs have not only been

13 Plant Growth-Promoting Bacteria …

307

found effective to promote plant growth but also reported to increase soil fertility by solubilizing nutrients in the soil and thereby suggested as an ecofriendly approach toward sustainable agriculture (Bishnoi 2015; Romao-Dumaresq et al. 2017; Singh et al. 2018).

13.4 Conclusion Given the above, it can be concluded that plant growth-promoting bacteria are useful to enhance nutrient availability in soil and nutrient uptake by host plants. If these are used in the long run, they can, therefore, sustain the soil fertility and higher crop yield. The use of potential strains can effectively trigger and enhance the nutrient use efficiency of host plants. The enhanced nutrient use efficiency will not only increase the crop yield but also ensure the sustainable availability of nutrients in the soil even after crop harvest. Such residual amounts may reduce the nutrients quantity required in subsequent crop and thereby will reduce the input cost of the crop. Such strategies can be very effective for the sustainability of crop production and yield essential for food security.

References Adak A, Prasanna R, Babu S, Bidyarani N, Verma S, Pal M, Nain L (2016) Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices. J Plant Nutr 39(9):1216– 1232 Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85(1):1–12 Agarwal BD, Broutman LJ, Chandrashekhara K (2017a) Analysis and performance of fiber composites. Wiley, New York, USA Agrawal DPK, Agrawal S (2013) Characterization of Bacillus sp. strains isolated from rhizosphere of tomato plants (Lycopersicon esculentum) for their use as potential plant growth promoting rhizobacteria. Int J Curr Microbiol Appl Sci 2(10):406–417 Agarwal M, Dheeman S, Dubey RC, Kumar P, Maheshwari DK, Bajpai VK (2017b) Differential antagonistic responses of Bacillus pumilus MSUA3 against Rhizoctonia solani and Fusarium oxysporum causing fungal diseases in Fagopyrum esculentum Moench. Microbiol Res 205:40–47 Ahmad S, Imran M, Hussain S, Mahmood S, Hussain A (2017) Bacterial impregnation of mineral fertilizers improves yield and nutrient use efficiency of wheat. J Sci Food Agric 97:11 Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2(1):1–12 Arif MS, Shahzad SM, Riaz M, Yasmeen T, Shahzad T, Akthar MJ, Bragazza L, Buttler A (2017) Nitrogen-enriched compost application combined with plant growth-promoting rhizobacteria (PGPR) improves seed quality and nutrient use efficiency of sunflower. J Plant Nutri Soil Sci 180(4):464–473 Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Appl Soil Ecol 49:125–130

308

C. Pandey et al.

Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 32:921–950 Beneduzi A, Peres D, Vargas LK, Bodanese-Zanettini MH, Passaglia LMP (2008) Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing bacilli isolated from rice fields in South Brazil. App Soil Eco 39(3):311–320 Bhanti M, Taneja A (2007) Contamination of vegetables of different seasons with organophosphorous pesticides and related health risk assessment in northern India. Chemosphere 69:63–68 Bhatt K, Maheshwari DK (2019) Decoding multifarious role of cow dung bacteria in mobilization of zinc fractions along with growth promotion of C. annuum L. Sci Rep 9:14232 Bishnoi U (2015) PGPR interaction: an ecofriendly approach promoting the sustainable agriculture system. Adv Bot Res 1(75):81–113 Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. App Microbiol Biotech 65(5):497–503 Canbolat MY, Bilen S, Cakmakcr R, Sahin F, Aydm A (2006) Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biol Fertil Soils 42:350–357 Chandini KR, Kumar R, Prakash O (2019) The impact of chemical fertilizers on our environment and ecosystem. In: Research trends in environmental sciences, Vol 2, AkiNik Publications, New Delhi, pp 69–86 Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Sys 11:233–260 Chaturvedi M, Sharma C, Tiwari M (2013) Effects of pesticides on human beings and farm animals: a case study. Res J Chem Environ Sci 1(3):14–19 Chauhan AK, Maheshwari DK, Kim K, Bajpai VK (2016). Termitarium-inhabiting Bacillus endophyticus TSH42 and Bacillus cereus TSH77 colonizing Curcuma longa L.: isolation, characterization, and evaluation of their biocontrol and plant-growth-promoting activities. Can J Microbiol 62(10):880–892 Cohen AC, Bottini R, Piccoli P (2015) Role of abscisic acid producing PGPR in sustainable agriculture. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agro-ecosystem. Springer, New York, pp 259–282 Dalvie MA, Naik I, Channa K, London L (2011) Urinary dialkyl phosphate levels before and after first season chlorpyrifos spraying amongst farm workers in the Western Cape, South Africa. J Environ Sci and Health, Part B 46(2):163–172 de Santiago A, Quintero JM, Aviles M, Delgado A (2011) Effect of Trichoderma asperellum strain T34 on iron, copper, manganese, and zinc uptake by wheat grown on a calcareous medium. Plant Soil 342(1–2):97–104 Dey RK, Pal KP, Bhatt KK, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159(4):371–394 Dhiman S, Dubey RC, Baliyan N, Kumar S, Maheshwari DK (2019) Application of potassiumsolubilising Proteus mirabilis MG738216 inhabiting cattle dung in improving nutrient use efficiency of Foeniculum vulgare Mill. Environ Sustain 2(4):401–409 Duarah I, Deka M, Saikia N, Boruah HD (2011) Phosphate solubilizers enhance NPK fertilizer use efficiency in rice and legume cultivation. 3 Biotech 1(4):227–238 Dubey RC, Khare S, Kumar P, Maheshwari DK (2014) Combined effect of chemical fertilisers and rhizosphere-competent Bacillus subtilis BSK17 on yield of Cicer arietinum. Arch Phytopatho Plant Prot 47(19):2305–2318 Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189 Fan XH, Zhang SA, Mo XD, Li YC, Fu YQ, Liu ZG (2017) Effect of PGPR and N source on plant growth and N, P uptake by tomato grown in Calcareous soils. Pedosphere Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biol Reviews 25(1):68–72

13 Plant Growth-Promoting Bacteria …

309

Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Marinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878):889–892 Gavito ME, Curtis PS, Mikkelsen TN, Jakobsen I (2001) Interactive effects of soil temperature, atmospheric carbon dioxide and soil N on root development, biomass and nutrient uptake of winter wheat during vegetative growth. J Exp Bot 52(362):1913–1923 Gellings CW, Parmenter KE (2016) Energy efficiency in fertilizer production and use. In: Gellings CW (ed) Efficient use and conservation of energy: encyclopedia of life support systems. Eolss Publishers, Oxford, pp 123–136 Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbial 41(2):109–117 Goteti PK, Emmanuel LDA, Desai S, Shaik MHA (2013) Prospective zinc solubilising bacteria for enhanced nutrient uptake and growth promotion in maize (Zea mays L.). Int J Microbiol 32(1):15–19 Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37(3):395–412 Gulati A, Vyas P, Rahi P, Kasana RC (2009) Plant growth-promoting and rhizosphere-competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of the Himalayas. Curr Microbiol 58:371–377 Gulnaz Y, Fathima PS, Denesh GR, Kulmitra AK, Shivrajkumar HS (2017) Effect of Plant Growth Promoting Rhizobacteria (PGPR) and PSB on root parameters, nutrient uptake and nutrient use efficiency of irrigated maize under varying levels of phosphorus. J Entomol Zool Stud 5(6):166– 169 Guo Q, Dong W, Li S, Lu X, Wang P, Zhang X, Ma P (2014) Fengycin produced by Bacillus subtilis NCD-2 plays a major role in biocontrol of cotton seedling damping-off disease. Microbiol Res 169(7–8):533–540 Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7(2):096–102 Gurusubramanian G, Rahman A, Sarmah M, Ray S, Bora S (2008) Pesticide usage pattern in tea ecosystem, their retrospects and alternative measures. J Environ Biol 29:813–826 Hafeez FY, Yasmin S, Ariani D, Zafar Y, Malik KA (2006) Plant growth-promoting bacteria as biofertilizer. Agr Sustain Dev 26(2):143–150 Han CS, Xie G, Challacombe JF, Altherr MR, Bhotika SS, Brown N, Bruce D, Campbell CS, Campbell ML, Chen J, Chertkov O, Cleland C, Dimitrijevic M, Doggett NA, Fawcett JJ, Glavina T, Goodwin LA, Green LD, Hill KK, Hitchcock P, Jackson PJ, Keim P, Kewalramani AR, Longmire J, Lucas S, Malfatti S, McMurry K, Meincke LJ, Misra M, Moseman BL, Mundt M, Munk AC, Okinaka RT, Parson-Quintana B, Reilly LP, Richardson P, Robinson DL, Rubin E, Saunders E, Tapia R, Tesmer JG, Thayer N, Thompson LS, Tice H, Ticknor LO, Wills PL, Brettin TS, Gilna P (2006) Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J Bacteriol 188:3382–3390 Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Annals Microbiol 60(4):579–598 Heinze J, Gensch S, Weber E, Joshi J (2017) Soil temperature modifies effects of soil biota on plant growth. J Plant Ecol 10(5):808–821 Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18 Huang Y, Krauss G, Cottaz S, Driguez H, Lipps G (2005) A highly acid-stable and thermostable endo-β-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochemical J 385(2):581–588 Jackson SD, Prat S (1996) Control of tuberisation in potato by gibberellins and phytochrome B. Physiol Plant 98(2):407–412

310

C. Pandey et al.

Jochum MD, McWilliams KL, Borrego EJ, Kolomiets MV, Niu G, Pierson EA, Jo YK (2019) Bioprospecting plant growth promoting rhizobacteria that mitigate drought stressin grasses. Front Microbiol 10:1–9 Karlidag H, Yildirim E, Turan M (2009) Salicylic acid ameliorates the adverse effect of salt stress on strawberry. Scientia Agricola 66(2):180–187 Katiyar V, Goel R (2004) Siderophore-mediated plant growthpromotion at low temperature by mutant of fluorescentpseudomonad. Plant Growth Regul 42:239–244 Kaur J, Khanna V, Kumari P, Sharma R (2015) Influence of psychrotolerant plant growth-promoting rhizobacteria (PGPR) as coinoculants with Rhizobium on growth parameters and yield of lentil (Lens culinaris Medikus). Afr J Microbiol Res 9(4):258–264 Kesaulya H, Hasinu JV, Tuhumury GN (2018) Potential of Bacillus spp produces siderophores insuppressing the wilt disease of banana plants. In: IOP conference series: and environmental science (vol. 102, no. 1, p. 012016). IOP Publishing Khabbaz SE, Zhang L, Cáceres LA, Sumarah M, Wang A, Abbasi PA (2015) Characterization of antagonistic Bacillus and Pseudomonas strains for biocontrol potential and suppression of damping-off and root rot diseases. Ann Appl Biol 166(3):456–471 Khan MS, Zaidi A (2007) Synergistic effects of the inoculation with plant growth-promoting rhizobacteria and an arbuscular mycorrhizal fungus on the performance of wheat. Turkish J Agricul Forestry 31(6):355–362 Khanghahi MY, Pirdashti H, Rahimian H, Nematzadeh G, Sepanlou MG (2018) Potassium solubilising bacteria (KSB) isolated from rice paddy soil: from isolation, identification to K use efficiency. Symbiosis 76(1):13–23 Kivi MP, Hokmalipour S, Darbandi MH (2014) Nitrogen and phosphorus use efficiency of spring wheat (Triticum aestivum L.) as affected by seed inoculation with plant growth promoting rhizobacteria (PGPR). International J Ad Biol Biomed Res 2(4):1038–1050 Kloepper JW, Schroth MN (1978) Plant growth promoting rhizobacteria on radishes. Proc. 4th Int. Conf. Plant path. Bact, Angers, pp 879–882 Kumar A, Patel JS, Bahadur I, Meena VS (2016) The molecular mechanisms of KSMs for enhancement of crop production under organic farming. In Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 61–75 Lavakush YJ, Verma JP, Jaiswal DK, Kumar A (2014) Evaluation of PGPR and different concentration of phosphorous level on plant growth, yield and nutrient content of rice (Oryza sativa). Ecol Eng 62:123–128 Lawrence G, Richards CA, Cheshire L (2004) The environmental enigma: why do producers professing stewardship continue to practice poor natural resource management? J Environ Policy Plan 6(3–4):251–270 Lee MH, Lee J, Nam YD, Lee JS, Seo MJ, Yi SH (2016) Characterization of antimicrobial lipopeptides produced by Bacillus sp. LM7 isolated from chungkookjang, a Korean traditional fermented soybean food. Int J Food Microbiol 221:12–18 Li YC, Li ZW, Lin WW, Jiang YH, Weng BQ, Lin WX (2018) Effects of biochar and sheep manure on rhizospheric soil microbial community in continuous ratooning tea orchards. Chin J Appl Ecol 29:1273–1282 Lin W, Lin M, Zhou H, Wu H, Li Z, Lin W (2019) The effects of chemical and organic fertilizer usage on rhizosphere soil in tea orchards. PLoS One 14(5):e0217018 Maheshwari DK (ed) (2011) Bacteria in agrobiology: crop ecosystems. Springer Science & Business Media Maheshwari DK, Agarwal M, Dheeman S, Saraf M (2013) Potential of rhizobia in productivity enhancement of Macrotyloma uniflorum L. and Phaseolus vulgaris L. cultivated in the Western Himalaya. In: Maheshwari DK, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin, Heidelberg, pp 127–165 Maheshwari DK, Dheeman S, Annapurna K (2017) Endophytes as contender of plant productivity and protection: an introduction. In: Endophytes: crop productivity and protection. Springer, Cham, pp 1–9

13 Plant Growth-Promoting Bacteria …

311

Maheshwari DK, Dubey RC, Agarwal M, Dheeman S, Aeron A, Bajpai VK (2015) Carrier based formulations of biocoenotic consortia of disease suppressive Pseudomonas aeruginosa KRP1 and Bacillus licheniformis KRB1. JEE 81:272–277 Mehta P, Walia A, Kulshrestha S, Chauhan A, Shirkot CK (2015) Efficiency of plant growthpromoting P-solubilizing Bacillus circulans CB7 for enhancement of tomato growth under net house conditions. J Basic Microbiol 55(1):33–44 Melnykova N, Gryshchuk O, Mykhalkiv L, Mamenko P, Sergii KOTS (2013) Plant growth promoting properties of bacteria isolated from the rhizosphere of soybean and pea. Natura Montenegrina 12(3–4):915–923 Minaxi RP, Acharya KO, Santosh N (2011) Impact of climate change on food security. Inter J Agricul Environ Biotechnol 4(2):125–127 Mishra PK, Bisht SC, Ruwari P, Selvakumar G, Joshi GK, Bisht JK, Bhatt JC, Gupta HS (2011) Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant Pseudomonads from NW Himalayas. Arch Microbiol 193:497–513 Mishra PK, Mishra S, Selvakumar G, Kundu S, Shankar Gupta H (2009) Enhanced soybean (Glycine max L.) plant growth and nodulation by Bradyrhizobium japonicum-SB1 in presence of Bacillus thuringiensis-KR1. Acta Agriculturae Scand Sect B–Soil and Plant Sci 59(2):189–196 Negi YK (2005) Strain improvement of fluorescent Pseudomonas spp. with respect to their PGPR activity using molecular approaches. Ph.D. thesis submitted to Dr. RML Avadh University, Faizabad, UP, India Negi YK, Prabha D, Garg SK, Kumar J (2011) Genetic diversity among cold-tolerant fluorescent Pseudomonas isolates from Indian Himalayas and their characterization for biocontrol and plant growth promotion activities. J Plant Growth Regul 30:128–143 Odukkathil G, Vasudevan N (2013) Toxicity and bioremediation of pesticides in agricultural soil. Rev Env Sci Bio/Tech 12(4):421–444 Ogunseitan O (2005) Microbial diversity: form and function in prokaryotes. Blackwell Science Ltd., Massachusetts, USA, p 142 Orozco FH, Cegarra J, Trujillo LM, Roig A (1996) Vermicomposting of coffee pulp using the earthworm Eisenia fetida: effects on C and N contents and the availability of nutrients. Bio Fertil Soil 22:162–166 Pandey A, Trivedi P, Kumar B, Palni LMS (2006) Characterization of a phosphate solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a Sub-Alpine Location in the Indian Central Himalaya. Curr Microbiol 53:102–107 Pandey C, Bajpai VK, Negi YK, Rather IA, Maheshwari DK (2018a) Effect of plant growth promoting Bacillus spp. on nutritional properties of Amaranthus hypochondriacus grains. Saudi J Biol Sci 25:1066–1071 Pandey C, Negi YK, Maheshwari DK, Rawat D, Prabha D (2018b) Potential of native cold tolerant plant growth promoting bacilli to enhance nutrient use efficiency and yield of Amaranthus hypochondriacus. Plant Soil 428(1–2):307–320 Pandey C, Prabha D, Negi YK (2017) Mycoremediation of common agricultural pesticides. In: Prasad R (ed) Mycoremediation and environmental sustainability, vol. 2. Springer Publications, Cham, pp 155–179 Parmar JK, Patel JJ (2009) Effect of organic and inorganic nitrogen and biofertilizer on nutrient content and uptake by amaranth (Amaranthus hypochondriacus L.). An Asian J Soil Sci 4:135–138 Prasanna R, Sharma E, Sharma P, Kumar A, Kumar R, Gupta V, Nain L (2013) Soil fertility and establishment potential of inoculated cyanobacteria in rice crop grown under non-flooded conditions. Paddy Water Environ 11(1–4):175–183 Puente ME, Li CY, Bashan Y (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. II. Growth promotion of cactus seedlings. Plant Bio 6(5):643–650 Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski, Schweitzer jA, Suding KN, Van de Voorde TFJ, Wardle DA, Suding KN (2013). Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101(2):265–276

312

C. Pandey et al.

Rahman M, Sabir AA, Mukta JA, Khan MA, Mohi-Ud-Din M, Miah MG, Rahman M, Islam MT (2018) Plant probiotic bacteria Bacillus and Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Scient Rep 8:2504 Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization and biofortification of zinc in soybean and wheat cultivated in Vertisols of central India. Appl Soil Ecol 73:87–96 Refish NMR, Talib AJ, Jian-Wei G, Fu C, Yu L (2016) Promoting role of Bacillus subtilis BS87 on the growth and content of some natural products in the medicinal plants Anoectochilus roxburghii and A. formosanus. Adv Life Sci 6(2):31–38 Ren X, Guo S, Tian W, Chen Y, Han H, Chen E, Li BL, Li YY, Chen Z (2019) Effects of Plant GrowthPromoting Bacteria (PGPR) inoculation on the growth, antioxidant activity, Cu uptake, and bacterial community structure of rape (Brassica napus L.) grown in Cu-contaminated agricultural soil. Front Microbiol 10:1455 Romao-Dumaresq AS, Franco HCJ, Borges BMMN, Batista BD, Quecine MC (2017) Beneficial microorganisms associated with sugarcane crops: the green gold for clean energy. Diversity and benefits of microorganisms from the tropics. Springer, Cham, pp 313–339 Selvakumar G, Mohan M, Kundu S, Gupta AD, Joshi P, Nazim S, Gupta HS (2007) Cold tolerance and plantgrowth promotion potential of Serratia marcescensstrain SRM (MTCC 8708) isolated from flowers of summer squash (Cucurbita pepo). Lett Appl Microbiol 46:171–175 Selvakumar G, Mohan M, Kundu S, Gupta AD, Joshi P, Nazim S, Gupta HS (2008) Cold tolerance and plant growth promotion potential of Serratia marcescens strain SRM (MTCC 8708) isolated from flowers of summer squash (Cucurbita pepo). Lett Appl Microbiol 46:171–175 Shabayev VP (2012) Mineral nutrition of plants inoculated with plant growth-promoting rhizobacteria of Pseudomonas genus. Bio Bull Rev 2(6):487–499 Shaharooma B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155 Shakeel M, Rais A, Hassan MN, Hafeez FY (2015) Root associated Bacillus sp. improves growth, yield and zinc translocation for basmati rice (Oryza sativa) varieties. Front Microbiol 6:1286 Sharma A, Shankhdhar D, Shankhdhar SC (2015) Plant growth promoting rhizobacteria—an approach for biofortification in cereal grains. Physiological Efficiency for Crop Improvement, pp 460–545 Sharma P, Bhatt D, Zaidi MGH, Saradhi PP, Khanna PK, Arora S (2012) Silver nanoparticlemediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167(8):2225–2233 Shukla A, Dhauni N, Suyal DC, Kumar S, Goel R (2015) Comparative plant growth promoting potential of psychrotolerant diazotrophs, Pseudomonas sp. JJS2 and Enterobacter sp. AAB8 against native Cajanuscajan (L.) and Eleusinecoracana (L.). Afr J Microbiol Res 9(20):1371– 1375 Singh AK, Karambeer Pal AK (2015) Effect of vermicompost and biofertilizers on strawberry: growth, flowering and yield. Ann Plant Soil Res 17:196–199 Singh N, Singh G, Aggarwal N, Khanna V (2018) Yield enhancement and phosphorus economy in lentil (Lens culinaris Medikus) with integrated use of phosphorus, Rhizobium and plant growth promoting rhizobacteria. J Plant Nutrition 41(6):737–748 Singh PB, Singh V, Nay PK (2008) Pesticide residues and reproductive dysfunction in different vertebrates from north India. Food Chem Toxicol 46:2533–2539 Singh RK, Malik N, Singh S (2013) Improved nutrient use efficiency increases plant growth of rice with the use of IAA-overproducing strains of endophytic Burkholderia cepacia strain RRE25. Microbial Ecol 66(2):375–384 Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganismplant signaling. FEMS Microbiol Rev 31(4):1–24

13 Plant Growth-Promoting Bacteria …

313

Spolaor LT, Gonçalves LSA, Santos OJAPD, Oliveira ALMD, Scapim CA, Bertagna FAB, Kuki MC (2016) Plant growth-promoting bacteria associated with nitrogen fertilization at topdressing in popcorn agronomic performance. Bragantia 75:33–40 Supanjani HH, Jung JS, Lee KD (2006) Rock phosphate-potassium and rock-solubilising bacteria as alternative, sustainable fertilizers. Agron Sustain Dev 26:233–240 Talboys PJ, Owen DW, Healey JR, Withers PJA, Jones DL (2014) Auxin secretion by Bacillus amyloliquifaciens FZB42 both stimulates root exudation and limits phosphorus uptake in Triticum aestivium. BMC Plant Biol 14:51 Thomas L, Gupta A, Gopal M, George P, Thomas GV (2010) Plant growth promoting potential of Bacillus spp. isolated from rhizosphere of cocoa (Theobroma cacao L.). J Plant Crops 38:97–104 Tiryaki O, Temur C (2010) The fate of pesticide in the environment. J Biol Environ Sci 4:29–38 UNDESA (2017) World population prospects: the 2017 revision. United Nations Department of Economics and Social Affairs, New York, USA Vejan P, Abdullah R, Khadiran T, Ismail S, Boyce AN (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecule 21:573 Verma JP, Yadav J, Tiwari KN, Lavakush SV (2010) Impact of plant growth promoting rhizobacteria on crop production. Int J Agric Res 5:954–983 Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24 Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166 Yildrim E, Karlidag H, Turan M, Dursun A, Goktepe F (2011) Growth, nutrient uptake, and yield promotion of broccoli by plant growth promoting rhizobacteria with manure. Hort Sci 46:932–936 Zeffa DM, Perini LJ, Silva MB, de Sousa NV, Scapim CA, Oliveira ALMd, Junior ATdA, Goncalves LSA (2019) Azospirillum brasilense promotes increases in growth and nitrogen use efficiency of maize genotypes. PLoS One 14:e0215332. http://doi.org/10.1371/Journal.Pone.0215332 Zongzheng Y, Xin L, Zhong L, Jinzhao P, Jin Q, Wenyan Y (2010) Effect of Bacillus subtilis SY1 on antifungal activity and plant growth. Int J Agri Bio Eng 2:55–61

Chapter 14

Siderophore in Plant Nutritional Management: Role of Endophytic Bacteria Gunjan Garg, Sandeep Kumar, and S. Bhati

Abstract Plants uptake nutrients specifically phosphorus, nitrogen, iron, and potassium with the help of beneficial bacteria in its available form. Bacteria helps in the enhancement of plant growth via direct or indirect ways are considered as a Plant Growth Promoting Rhizobacteria (PGPR). These are green alternatives to conserve soil fertility sustainably by leveraging nutrition supports to plants in many ways. Bacteria also produce siderophores and many phytohormones which support the plant life in adverse stressful conditions. Recently, in this group of bacteria and endophytic fungi many candidates are involved in the production of pyoverdine, hydroxamate, ferrioxamines siderophores in rhizosphere region, which increases three times Iron (Fe) transportation efficiency of root and shoot growth of the plants. Siderophores reflect significant application in metal binding along with the iron and ranked as “Fe-biosensors.” How siderophores production by bacteria facilitate bioremediation, weathering of soil-mineral particles that enhance the plant growth have been reviewed in further. Keywords Siderophore · Phytohormone · Rhizobacteria · Iron deficit soil · Microbiome · Root secretion

14.1 Introduction There is a demand for more yield and production of crops for the food security, while the production rate is adversely affected by different kinds of biotic (insect/pest/fungus, etc.) and abiotic stresses (salt/water/temperature, etc.). Using the biotechnological method, we can contrive transgenic stress tolerance plant, which counterbalances the adverse effects of the environment. Endophytic microbiota plays G. Garg (B) · S. Bhati School of Biotechnology, Gautam Buddha University, Greater Noida 201 308, Uttar Pradesh, India e-mail: [email protected] S. Kumar Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar 249 404, Uttarakhand, India © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_14

315

316

G. Garg et al.

an important role in the host plant’s growth either by the production of secondary metabolite or nutrient assimilation. This helps the plant to adapt themselves to various environmental stresses (i.e., salt and water), an important aspect of crop yields. In the current scenario, enormous knowledge of endophytes, their roles for increasing crop yields, disease-resistant plants, and facilitating the survival under environmental stress is a requirement for the agricultural prosperity. Bacteria, actinobacteria, and some fungi comprise the endophytic microbial system. Endophytic microbiota forms a network surrounding their host plants (Wang et al. 2011; Pahari and Mishra 2017). Generally, they inhabit the intercellular spaces of the host plant. The most common mode of entry for endophytic bacteria into plant tissues is through primary and lateral root cracks, and diverse tissue wounds arising as a result of plant growth (Sprent and de Faria 1998; Agarwhal and Shende 1987; Sørensen and Sessitsch 2015). Endophytic bacteria not only escalate nitrogen fixation/phosphate solubilization but under stress conditions (abiotic and biotic), they mount the production of phytohormones and regulate the biosynthetic pathway of ethylene. Endophytes in plant system synthesize many biologically active novel compounds without any observable damage to the host tissue like alkaloids, terpenoids, steroids, peptides, poly-ketones, quinols, flavonoids, phenols, and insecticide azadirachtin (Kusari et al. 2012; Molina et al. 2012; Zinniel et al. 2002) antifungal compounds include cryptocandin, pestaloside, cryptocin, ecomycins, pestalopyrone, and pseudomycins. Endophytic microorganism increases plant resistance against the pathogen by inducing defense mechanisms, the so-called induced systematic resistance (ISR) (Zamioudis and Pieterse 2012). Another most significant and important mechanism for endophyte inhabitation in plants is the production of the extracellular enzyme exhibiting enormous industrial significance in different fields such as fermentation process and biotechnological applications. Some of the extracellular hydrolase enzymes augmented the plant responses to pathogenic infection (Leo et al. 2016). Endophytic strains of endophytic microflora are harnessed for commercialscale production as biofertilizers and biopreparations. Biofertilizers are defined as substances that contain living organisms tending to inhabit with the rhizosphere or the plant interior which are coalesced to seeds, plant surfaces, or soil. They increase the availability and supply of the nutrient which boost plant growth. The common bacteria’s, such as Azospirillum, Herbaspirrilum, Acetobacter, Azotobacter, and Azoarocus, have been successfully used as biofertilizers. Nowadays, there is a quest for microbial strains which can contribute to the development of bioinoculants, biofertilizers, and biopreparations, consequentially enhances the growth and yield of crop plants. Biopreparations are the products that originate from either living organisms or their metabolites, used in organic farming for environmental stress regulation. In the plant–soil interaction, there is a narrow region called as rhizosphere, which directly influenced by root microbiome and root secretion. This symbiotic association influenced the ability of the plant to absorb nutrients specifically phosphorus, nitrogen, iron, and potassium. In the soil symbiotic zone bacteria’s grow, which directly and indirectly enhanced the growth of plants and hence considered as plant growth-promoting rhizobacteria (PGPB)/bioinoculants/microbial inoculants. In the agricultural field, PGPB is considered a green alternative to boost

14 Siderophore in Plant Nutritional Management …

317

sustainable soil fertility as well as plant growth (Tilak et al. 2005). PGPB supports the growth of plants through phosphorus solubilization, nitrogen fixation, absorption and assimilation of minerals/nutrients. These Endophytic bacteria also produce siderophore and many phytohormones which support the plant life in adverse stressful condition (Glick 1995; Bhardwaj et al. 2014; Pahari et al. 2016) (Table 14.1). Siderophores have potential roles and applications in various areas of environmental research due to their affinity in metal binding especially with iron. Chemically siderophores are the iron-containing low molecular weight chelating agents, showing specific affinity with ferric ions, therefore, siderophores can be termed as “Fe-biosensors.” They facilitate bioremediation, weathering of soil-mineral particles, and enhanced plant growth. Most of the aerobic and facultative anaerobic microorganisms like Pseudomonas, Azotobacter, Bacillus, Enterobacter, Serratia, Azospirillum, and Rhizobium (Glick et al. 1999; Loper and Henkels 1999; Pahari and Mishra 2017) synthesize siderophore under iron-limited conditions (Neilands 1981). As per research report, all microbes do not require iron and siderophores. There are some lactic acid-producing bacteria which showed poor growth in iron-containing medium because they don’t have iron regulating ribotide reductase enzyme. Iron is the fourth most abundant element on the earth, an essential micronutrient for plant growth, though deemed as most lacking micronutrients due to its insoluble nature of Fe+3 . The preliminary role of siderophores is scavenging of Fe. They also form complex molecules with other essential micro-elements like Mo, Mn, Co, and Ni in the environment and make them available for microbial cells (Bellenger et al. 2008; Braud et al. 2009a, b). There are no specific and defined procedures for the isolation of siderophores, as they differ substantially in their structures. Detection of siderophores can be finished by paper electrophoresis method whereas; structural characterization is best carried out by NMR and mass spectroscopy. In this chapter we will focus on the structure, functions, and applications of siderophores specifically in nutrient absorption by crop plants in the agriculture field.

14.2 Types of Siderophore At present nearly 500 siderophores are reported from selected microorganisms. A great variation is seen in siderophore structure from one species to another. Broadly such siderophore is classified into two (a) Microbial siderophore, and (b) Phytosiderophore. (a) Microbial siderophores: According to the oxygen ligands for Fe3+ organization bacterial siderophores can be differentiated into three main categories, namely, catecholate (i.e., enterobactin), carboxylates (i.e., rhizobactin), and hydroxamates (i.e., ferrioxamine B) (Matzanke1991). However, there is also a certain type of microbial siderophores that contain a mix of the main functional groups (i.e., pyoverdine) (Cornelis 2010). One such most common fungal siderophores is hydroxamates belonging to the ferrichrome family (i.e., ferrichrome), which is further divided into

Unknown Unknown Unknown Desferrioxamine

Escherichia coli

Pseudomonas putida

Micrococcus luteus

Streptomyces coelicolor

Ferrichromes) Ferricrocin Coprogens Fusigen

Ustilago sphaerogena

Aspergillus fumigates

Trichoderma sp

Fusarium sp

(B) Fungi

Ferribactin

Pseudomonas fluorescens

Name of siderophore ferrioxamines

(A) Bacteria

Hydroxamate type characteristics: • hydroxamate belongs to C(= O)N-(OH)R • -R: is an amino acid • hydroxamate siderophore forms a complex of hexadentate octahedral structure with Fe3+ form

Erwinia, Nocardia, Streptomyces, Arthrobacter, Chromobacterium and Pseudomonas

Siderophore-producing microbial cell

Type of siderophore

Table 14.1 List of different types of siderophore produced by different groups of microbes

(continued)

Diekmann and Zahner (1967)

Diekmann and Zahner (1967)

Wallner et al. (2009)

Emery (1971)

Saharan and Nehra (2011)

Cabaj and Kosakowska (2009)

Sayyed et al. (2005)

Kannahi and Senbagam (2014)

Maurer and Keller-Schierlein (1968)

Winkelmann (2007)

References

318 G. Garg et al.

Siderophore-producing microbial cell

Carboxylate type characteristics: Such siderophores exhibits hydroxy and carboxylate donor groups

Staphyloferrin B

Staphylococcus aureus

Paracoccus denitrificans

Staphyloferrin A

Parabactin

Agrobacterium tumefaciens

Staphylococcus hyicus Staphylococcus aureus

Agrobactin

Vibrio cholera

Rhizobactin

Vibriobactin

Bacillus cereus, Bacillus anthracis and Bacillus thuringiensis

Rhizobium meloti

Petrobactin Bacillibactin

Bacillus cereus, Bacillus anthracis

Bacillibactin

Bacillus anthracis Bacillus subtilis

Beasley et al. (2011)

Meiwes et al. (1990) Beasley et al. (2011)

Drechsel et al. (1995)

Dave et al. (2006)

Dave et al. (2006)

Saharan and Nehra (2011)

Wilson et al. (2006)

May et al. (2001)

Saharan and Nehra (2011)

Saharan and Nehra (2011)

Sayyed et al. (2005)

Salmochelins

Pyoverdine

References Saharan and Nehra (2011)

Name of siderophore Enterobactin (or enterochelin or cyclic trimester of 2.3-dihydroxy ben-zoylserine) First tricatechol siderophore

Salmonella enteric

Catecholate type E. coli, Aerobacter aerogenes, and Salmonella typhimurium (the most intensively analyzed siderophores) Characteristics: • Structure backbone of Catecholate siderophore is polyamine (a) peptide or (b) a macrocyclic lactone Pseudomonas aeruginosa

Type of siderophore

Table 14.1 (continued)

14 Siderophore in Plant Nutritional Management … 319

320

G. Garg et al.

five groups, depending on their side chain group hydroxamate (Renshaw et al. 2002; Winkelmann 2007). (b) Phytosiderophore: Iron is one metal, available in abundance in the soil, an essential microelement for plant growth but even then, the plant faces the deficit condition for this microelement. To escape such adverse conditions plant has secreted specific chelating compounds “Phytosiderophore.” Phytosiderophores (PS) are the organic substances (such as nicotinamine, mugineic acids (MAs), and avenic acid, etc.) secreted by the roots of plants of graminae family (e.g., wheat, rice, maize, sorghum, oat, barley, etc.) under Fe-deficient conditions (Mori and Nishizawa 1987). The Phytosiderophore can form organic complexes or chelates with Fe3+ and increase the movement of iron in soil (Ueno et al. 2007). The iron (Fe)-phytosiderophore complex enters the roots through an iron transporter channel present in the root plasma membrane and endorsed the efficiency of Fe mainly in the area having low soil Fe availability. The phytosiderophores are hexadentate ligands that coordinate Fe+3 with their amino and carboxyl groups (Singh et al. 2011). According to Wallace (1991) phytosiderophore are non-proteineous, low molecular weight acids released by the plants under the iron and zinc deficiency stress. The phytosiderophore mobilizes nutrient elements (like Fe, Zn, Mn, and Cu) from the soils to plant in deficient condition (Takagi et al. 1984). Fe-chelates are highly soluble and stable over a wide pH range. In comparison with the molecular mass of microbial siderophores (ranged 200–2000 Da) phytosiderophores are ranged between 500 and 1000 Da (Neilands 1981). Mugineic acid (MA) is the most common siderophore and the firstly identified in plants (Takemoto et al. 1978). The stability constant of the MAFe+3 complexes is very low as compared with the stability constant of ferrichrome, ferrioxamine B, and enterobactin microbial siderophores (Raymond et al. 1984; Schwarzenbach and Schwarzenbach 1963; Harris et al. 1979). Some important phytosiderophore which has been isolated from the gramineous plants are distichonic acid from Hordeum vulgare (beer barley) (Nomoto et al. 1981) avenic acid A from Avena sativa (oat). A plant releases phytosiderophore at higher amounts about a few hours (± 3 h) to the onset of the light period. Under continuous darkness or continuous light, the rate of release of phytosiderophore is lower. Further release of siderophores varies along the root and is most pronounced in the apical root zone compared to the other zones of the root. Morphologically highest uptake rates were found in highly branched root system; whereas the lowest uptake rates were found in the thicken root system (Romheld and Marschner 1990). Nature released of phytosiderophores is studied with the help of high-performance liquid chromatography (HPLC) (Mori et al. 1991). According to Cakmak et al. (1994) amount and composition of phytosiderophores are affected by plant age, type and properties of soil, root morphology, crop varieties, nutritional status of the plant, temperature, light duration, daytime vs light intensity. Releasing rate of phytosiderophores by plants differs between plant to plant species and is positively correlated with the plant resistance capacity to Fe deficiency.

14 Siderophore in Plant Nutritional Management …

321

14.3 Shuttling Mechanism Through Siderophore Mediated Iron Transporter System Fe is considered as the key regulatory element of cellular metabolic pathway. It regulates the activity of many antioxidative enzymes like catalase, peroxidase (POD), ascorbate, and superoxide dismutase. Deficiency of Fe in plant system may affect oxidative defensive system and cause oxidative injury. Therefore, all the living beings are required a well-organized and controlled system of Fe absorption and utilization. Siderophore by forming a multi-complex system with the nutrient molecules play an important role in the transportation of ferric ions into the plant cell. Specific siderophore receptors are present on the cell membrane which helps in transporting the siderophore–iron complex to the cell interior.

14.4 Cell Membrane Siderophore Receptors There are different types of siderophore specific receptors present in different types of gram-positive and gram-negative bacteria. Gram-negative bacteria (e.g., Escherichia sp.) possess receptor specifically on the outer membrane that recognize the Fe (III)– siderophore complexes at the cell surface (Krewulak and Vogel 2008) whereas grampositive bacteria (e.g., Bacillus sp.), lacks the outer membrane and their receptor molecules. Therefore, periplasmic siderophore receptor helps in binding Fe (III)– siderophore complexes (Fukushima et al. 2013). Fec A and Fep A protein receptors are present on the outer membrane, whereas Ton B-Exb B complex siderophore receptor is present on the inner membrane. Fec CDE- Fep CDE- ATP dependent carrier molecules are present as an inner membrane and periplasmic transporting proteins.

14.5 Channel of Fe Transportation in Microbes and Plants When the siderophore is released from the cell, the membrane receptors protein binds with iron and forms iron–siderophore complex and transported into the cell via Fec A and Fep A (an outer membrane receptor), then it is transported to Fec CDE- Fep CDE an ATP-dependent transporter systems (or ABC-Transporter systems). Finally, siderophore–iron complex is released into the cytosol with the help of membrane receptor protein Ton B. In the cytoplasm, iron is released from the complex via hydrolytic breakdown in the presence of NADPH linked siderophore reductase and Ent ABCD protein. Such produced Fe++ does not have a high affinity with siderophore and it separates from the siderophore–iron complex. The released siderophores either get degraded or recycled by excretion through efflux pumping system (Table 14.2).

322

G. Garg et al.

Table 14.2 List protein Channel of Fe transportation in microbes Model system

Location

Receptor proteins

References

Bacteria

An outer membrane receptor

Fec A and Fep A

Sajeed Ali and Vidhale (2013)

An inner membrane receptor

Fec CDE- Fep CDE (an ATP dependent transporter systems/or ABC-Transporter systems) and Ton B

Sajeed Ali and Vidhale (2013)

Cytosol

Ent ABCD protein

Sajeed Ali and Vidhale (2013)

Fungi

Siderophore mediated Fe transport system Mechanisms

Process

References

The shuttle mechanism • Fe-siderophore complex is Ardon et al. (1998) transported across the cell membrane and released the Fe+3 ions from the ligands and reduced by the reductive enzymes • Recycle the free siderophore • e.g., transporting ferrichrome in Ustilago maydis The taxicab mechanism

• Fe+3 extracellular siderophore is transferred across the cell membrane to intracellular membrane ligands e.g., Rhodotorula species

The hydrolytic mechanism

• After the transportation of Adjimani and Fe+3 siderophore complex Emery (1988) inside the cell, it undergoes reductive and degenerative steps and release the Fe+3 • Fe+3 is then reduced into Fe+2 and the siderophore is further released out e.g., uptake of Fe+3 tri-acetyl-fusarinine complexes by Mycelia sterilia

Winkelmann and Huschka (1987)

(continued)

14 Siderophore in Plant Nutritional Management …

323

Table 14.2 (continued) Model system

Location

Receptor proteins

The reductive mechanism

• Fe+3 –siderophore complex Ecker and Emery is not transported across (1983) the cell membrane • Reduction of Fe+3 into Fe+2 occurs at the surface of the cell membrane • Reduced Fe is taken up by the cell e.g., uptake of Fe+3 from ferrichrome by Ustilago sphaerogena

References

14.6 Approaches Use in Fe and Zn Acquisition by Plants Plants grown in alkaline or calcareous soil generally showed chlorosis types of nutritional disorder due to low soil solubility for Fe and Zn ions. Fe absorbing and storing mechanisms in higher plants have been categorized into two types as Type I and II. 6.1 Type I plants (dicotyledons and non-graminaceous monocotyledons): These plants respond to Fe paucity by extruding the protons from the plasma membrane of the root surface. Fe+3 form reduced into the soluble Fe+2 form on the root plasma membrane and then penetrates inside the root cell through the specific Fe+2 transporter molecules (Tagliavini and Rombola 2001). 6.2 Type II plants (graminaceous species): These plants synthesize and secrete Fe-chelating substances like mugineic acids (MAs) from their roots, which increases the dissolving efficiency of Fe compounds in the rhizospheric zone (Marschner et al. 1986). After this, iron molecules are transported across the plasma membrane in the form of complex molecule (PS-Fe+3 ) through a specific transport system without the reduction reaction. The quantity of mugineic acid synthesized and secreted into the rhizosphere may fluctuate among species to species (Xiong et al. 2013). The amount of MAs secreted correlates positively with the ability of the plants to tolerate Fe deficiency (Xiong et al. 2013).

14.7 Occupations of Siderophore-PGPR in Crop Field 7.1 Siderophore as a Plant Growth Promoter: Siderophores are used in agricultural field as an ecofriendly and alternative approach to reduce the adverse effect of hazardous chemical pesticide. Recently many species of Pseudomonas have been identified that can enhances plant growth by producing pyoverdine, hydroxamate type of siderophores (Kloepper et al. 1980; Gamalero and Glick 2011; Mahmoud and Abd-Alla2001). Bacteria like Azadirachta indica produce ferrioxamines siderophore

324

G. Garg et al.

in rhizosphere region, increases Fe transportation efficiency within the plant for the root and shoot growth (Verma et al. 2011; Crowley 2006). Gangwar and Kaur (2009) and Rungin et al. (2012) isolated some bacteria [Escherichia coli from ryegrass (Loliumperenne sp.)] and an endophytic fungus Streptomyces sp. from the roots of Thai jasmine rice that enhances plant growth and significantly improved the root and shoot biomass and lengths. It has been correlated that excessive accumulation of heavy metals is toxic for most of the plants and responsible for the contamination of soil which decreases soil fertility and soil microbial activity (McGrath et al. 1995). In this context, hydroxamate type of siderophore present in soil will play an important role to immobilize the metals and act as plant growth promoter. 7.2 Siderophore as inhibitor for phytopathogenic attack: Siderophore acts as an inhibitor for phytopathogenic attacks and restrains the growth of phytopathogens. Molecules of siderophores bind with iron and make it unavailable for the plant pathogens (Beneduzi et al. 2012; Ahmed and Holmstrom 2014). Siderophores synthesized by Pseudomonas and Bacillus sp. (a type of rhizobacteria) inhibited the attack of Phytophthora parasitica (Seuk et al.1988), Fusarium oxysporum veridianthi (Buysens et al. 1996), Pythium ultimum (Hamdan et al. 1991), and Sclerotinia sclerotiorum (Mc Loughlin et al. 1992). For example: different strains of Pseudomonas fluorescens (like A1, BK1, TL3B1) act as a biological controlling agent against Erwinia carotovora and Fusarium oxysporum. F. oxysporum causes wilt diseases in potatoes (Kloepper et al. 1980; Schippers et al. 1987). 7.3 Siderophore as Bioremediation: There is release of heavy metals and metalloids from petroleum industry, chemical industry, etc., which contaminates the soil and water and for this siderophores is of prime prominence for metal bioremediation apart from binding with ferric iron, siderophores also regulate the gelatinization the other toxic metals, e.g., Cr3+ , Al3+ , Cu2+ , Eu3+ , and Pb2+ via the production of pyoverdine siderophore (P. aeruginosa), azotochelin (Azotobacter vinelandii), schizokinen, and N-di-oxyschizokinen production (Bacillus megaterium) stimulates molybdenum and aluminium biosynthesis, respectively (Braud et al. 2009a, b; Duhme et al. 1998; Hu and Boyer 1996). Specific siderophores showed very strong ligands affinity with specific metallic ions and form siderophore–metal complex molecule, which depends upon the ligand functionalities and siderophore–metal complex formation (Hernlem et al. 1999). 7.4 Endophytes and their role in Fe (iron) management in soil: It has been iterated that iron (Fe) is an essential element for plant growth and development. PGPR can increase Fe absorption by plants through reduction of Fe (III) to Fe (II) at the root surface. The bacterial strains with high Fe (III) reduction ability were able to stimulate plant growth in vitro and on a broad level. Plants grown in inoculated soil were generally bigger and with higher Fe content than those grown in sterilized soil. This contributes significantly due to Fe absorption by plants likely through increased Fe (III) reduction in the rhizosphere Valencia-Cantero et al. 2007. The role of bacterial endophytes in the acquisition of iron (Fe) solubilization and acquisition systems by plant-associated microbes with respect to improving plant growth and health used to enhance the supply of iron often limiting nutrients to the host plant (Chhabra and Dowling 2017). Siderophore-producing endophytes Arthrobacter sulfonivorans

14 Siderophore in Plant Nutritional Management …

325

DS-68 and Enterococcus hirae DS-163 enhanced biofortification of grains with Fe and yield in four genotypes of wheat (Triticum aestivum L.) in soils with low and high available Fe content. Endophyte inoculation increases the surface area, volume, length of roots, and the number of root tips. Such siderophore-producing endophytes can be recommended as bioinoculants to mitigate iron deficiencies in the soil and enhance crop productivity (Singh et al. 2020).

14.8 Conclusion Siderophore-producing plant growth-promoting rhizobacteria (PGPR) are microbes that colonize in the rhizospheric zone of the crop plant and significant increases the agricultural yield in the stressed soil. Phytosiderophores production acts as a lifesaving mechanism in the plants by substantiating the function of Fe and Zn, in Fe and Zn deficiency soil. Pytosiderophores increases 5–10 times mobilization of Fe and Zn under stress conditions. They chelated Fe3+ irons and reduce into the Fe2+ form. Using the biotechnological approaches, tools, and techniques, we can develop transgenic field crops, which possess phytosiderophores secretion responsible gene, resulting in the increase of the minerals absorption in nutrient-deficient conditions and thus increasing the crop yield. In the current scenario, this kind of organic farming practices with microbial diversity has added significant consideration to enhance the crop yield. Applications of the organic manures increase soil microbiome, which directly or indirectly increases soil fertility in the agricultural field, beside this, they also inhibit iron-dependent soil-borne phytopathogens. Hence siderophores will play an importation role when applied in the agriculture field, increasing the plant growth and biomass, enhancing the productivity and crop yield.

References Adjimani JP, Emery T (1988) Stereochemical aspects of iron transport in Mycelia sterilia EP-76. J Bacteriol 170:1377–1379 Agarwhal S, Shende ST (1987) Tetrazolium reducing microorganisms inside the root of Brassica species. Curr Sci 56:187–188 Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. J Microbial Biotechnol 7:196–208 Ardon O, Nudelman R, Caris C, Libman J, Shanzer A, Chen Y, Hadar Y (1998) Iron uptake in Ustilago maydis: tracking the iron path. J Bacteriol 180:2021–2026 Beasley FC, Marolda CL, Cheung J, Buac S, Heinrichs DE (2011) Staphylococcus aureustrans porters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79:2345–2355 Bellenger JP, Wichard T, Kustka AB, Kraepiel AML (2008) Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246

326

G. Garg et al.

Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051 Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fac 13:66 Braud A, Hannauer M, Mislin GLA, Schalk IJ (2009a) The pseudomonas aeruginosa pyochelin— iron uptake pathway and its metal specificity. J Bacteriol 191:3517–3525 Braud A, Jézéquel K, Bazot S, Lebeau T (2009b) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286 Buysens S, Heungens K, Poppe J, Hofte M (1996) Involvement of pyochelin and pioverdin in sup-pression of pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol 62(3):865–871 Cabaj A, Kosakowska A (2009) Iron-dependent growth of and siderophore production by two heterotrophic bacteria isolated from brackish water of the southern Baltic Sea. Microbiologic Res 164(5):570–577 Cakmak S, Gulut KY, Marschner H, Graham RD (1994) Effect of zinc and iron deficiency on phytosiderophores release in wheat genotypes differing in zinc efficiency. J Plant Nutrition 7:1–17 Chhabra S, Dowling DN (2017) Endophyte-promoted nutrient acquisition: phosphorus and iron. In: Doty S (ed) Functional importance of the plant microbiome. Springer, Cham Cornelis P (2010) Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol 86:1637–1645 Crowley DA (2006) Microbial siderophores in the plant rhizosphere. In: Barton LL, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 169–189 Dave BP, Anshuman K, Hajela P (2006) Siderophores of halophilic archaea and their chemical characterization. Indian J Exp Biol 44:340–344 Diekmann H, Zahner H (1967) Konstitution von Fusigen and dessenAbbauzu 2-Anhydromevalonsaurelacton. Eur J Biochem 3(2):213–218 Drechsel H, Tschierske M, Thieken A, Jung G, Zahner H, Winkelmann G (1995) The carboxylate type siderophore rhizoferrin and its analogs produced by directed fermentation. J Ind Microbiol 14:105–112 Duhme AK, Hider RC, NaldrettMJand Pau RN (1998) The ability of the molybdnem-azotochelin complex and its effect on siderophore production in Azotobactervnelandii. J Biol Inorg Chem 3(5):520–526 Ecker DJ, Emery T (1983) Iron uptake from ferrichrome A and iron citrate in Ustilagosphaerogena. J Bacteriol 155:616–622 Emery T (1971) Role of ferrochrome as a ferric ionophore in Ustilagosphaerogena. Biochemistry 10:1483–1488 Fukushima T, Allred BE, Sia AK, Nichiporuk R, Andersen UN, Raymond KN (2013) Grampositive siderophore-shuttle with iron-exchange from Fe-siderophore to apo-siderophore by Bacillus cereus YxeB. Proc Natl Acad Sci USA 110:13821–13826 Gamalero E, Glick BR (2011) Mechanisms used by plant growth promoting bacteria. In: Bacteria in agrobiology: plant nutrient management. Springer, Berlin, Heidelberg, pp 17–46 Gangwar M, Kaur G (2009) Isolation and characterization of endophytic bacteria from endorhizosphere of sugarcane and ryegrass. Internet J Microbiol 7:139–144 Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109– 117 Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London Hamdan H, Weller D, Thomashow L (1991) Relative importance of fluorescens siderophores and other factors in biological control of gaeumannomyces graminis var. Tritici by Pseudomonas fluorescens 2–79 and M4-80R. Appl Environ Microbiol 57(11):3270–3277 Harris WR, Carranao CJ, Cooper SR, Sofen SR, Avdeef AE, McArdle JV, Raymond KN (1979) Coordination chemistry of microbial iron transport compounds. 19. Stability constants

14 Siderophore in Plant Nutritional Management …

327

and electrochemical behavior of ferric enterobactin and model complexes. J Am Chem Soc 101:6097–6104 Hernlem BJ, Vane LM, Sayles GD (1999) The application of siderophores for metal recovery and waste remediation: examination of correlations for prediction of metal affinities. Water Res 33:951–960 Hu X, Boyer GL (1996) Siderophore-mediated aluminium uptake by Bacillus megaterium ATCC 19213. Appl Environ Microbiol 62:4044–4048 Kannahi M, Senbagam N (2014) Studies on siderophore production by microbial isolates obtained from rhizosphere soil and its antibacterial activity. J Chem Pharm Res 6:1142–1145 Kloepper JW, Leong J, Teintze M, Schiroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286:885–886 Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta 1778:1781–1804 Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19(7):792–798 Leo VV, Passari AK, Joshi JB, Mishra VK, Uthandi S, Ramesh N, Gupta VK, Saikia R, Sonawane VC, Singh BP (2016) A novel triculture system (CC3) for simultaneous enzyme production and hydrolysis of common grasses through submerged fermentation. Front Microbiol 7 Loper JE, Henkels MD (1999) Utilization of heterologous siderophore enhances levels of iron available to pseudomonas putida in the rhizosphere. Appl Environ Microbiol 65:5357–5363 Mahmoud ALE, Abd-Alla MH (2001) Siderophore production by some microorganisms and their effect on Bradyrhizobium-Mung Bean symbiosis. Int J Agric Biol 03(2):157–162 Marschner H, Romheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9:695–713 Matzanke BF (1991) Structures, coordination chemistry and functions of microbial iron chelates. In: Winkelmann G (ed) CRC handbook of microbial iron chelates. CRC Press, Boca Raton, FL, USA, pp 15–64 Maurer B, Keller-Schierlein W (1968) Ferribactin, a siderochrome from Pseudomonas fluores-cens Migula: 61. Mitteilung Ferribactin, einSiderochromaus Pseudomonas fluorescens Migula. Arch Microbiol 60:326–339 May JJ, Wendrich TM, Marahiel MA (2001) The dhb Operon of Bacillussubtilis encodes the biosynthetic template for the catecholicsiderophore 2, 3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276:7209–7217 Mc Loughlin T, Quinn J, Bettermann A, Bookland R (1992) Pseudomonas cepacia suppression of sunflower. Pseudomonas cepacia. Wilt fungus and role of antifungal compounds in controlling the disease. Appl Environ Microbiol 58(3):1760–1763 McGrath SP, Chaudri AM, Giller KE (1995) Long-term effects of metals in sewage sluge on soils, microorganisms and plants. J Ind Microbiol 14(2):94–104 Meiwes J, Fiedler HP, Haag H, Zahner H, Konetschny-Rapp S, Jung G (1990) Isolation and characterization of staphyloferrin A, a compound with siderophore activity from Staphylococcus hyicus DSM 20459. FEMS Microbiol Lett 67:201–206 Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in graminaceae plants. Plant Cell Physiol 28:1081–1092 Mori S, Nishizawa S, Hayashi N, Chino H, Yoshimurs E, Ishihara J (1991) Why are young rice plants highly susceptible to iron deficiency. Plant Soil 130:143–156 Neilands JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731 Nomoto K, Mino Y, Ishida T, Yoshioka H, Ota N, Inoue M et al (1981) X-ray crystal structure of the copper (II) complex of mugineic acid, a naturally occurring metal chelator of graminaceous plants. J Chem Soc, Chem Commun 7:338–339 Pahari A, Dangar TK, Mishra BB (2016) Siderophore quantification of bacteria from Sundarban and its effect on growth of Brinjal (Solanum melongena. L). The Bioscan 11(4):2147–2151 Pahari A, Mishra BB (2017) Characterization of Siderophore producing rhizobacteria and its effect on growth performance of different vegetables. Int J Curr Microbiol App Sci 6(5):1398–1405

328

G. Garg et al.

Passari AK, Mishra VK, Singh G, Singh P, Kumar B, Gupta VK, Sarma RK, Saikia R, Donovan AO, Singh BP (2017) Insights into the functionality of endophytic actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci Rep 7:11809 Raymond KN, Muller G, Matzanke BF (1984) Complexation of iron by siderophores a review of their solution and structural chemistry and biological function. In: FL Boschke (ed) Topics in current chem, vol 123, structural chemistry. Springer-Verlag, Berlin, Heidelberg, Germany, pp 49–102 Renshaw JC, Robson GD, Trinci APJ, Wiebe MG, Livens FR, Collison D, Taylor RJ (2002) Fungal siderophores: structures, functions and applications. Mycol Res 106:1123–1142 Romheld V, Marschner H (1990) Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phtytosiderophores. Plant Soil 123:147–153 Rungin S, Indananda C, Suttiviriya P, Kruasuwan W, Jaemsaeng R, Thamchaipenet A (2012) Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek 102(3):463– 472 Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30 Sayyed RZ, Badgujar MD, Sonawane HM, Mhaske MM, Chincholkar SB (2005) Production of microbial iron chelators (siderophores) by fluorescent pseudomonads. Indian J Biotechnol 4:484– 490 Schippers B, Bakker AW, Bakker PAH (1987) Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Ann Rev Phytopathol 25:339–358 Schwarzenbach G, Schwarzenbach K (1963) Hydroxamate complexes. I. The stabilities of the iron (III) complexes of simple hydroxamic acids and desferriferrioxamine. B HelvChim Acta 46:1390–1400 Sajeed Ali S, Vidhale NN (2013) Bacterial siderophore and their Application: a review. Int J Curr Microbiol App Sci 2(12):303–312 Seuk C, Paulita T, Baker R (1988) Attributes associate with increased biocontrol activity of fluorescent pseudomonads. J Plant Pathol 4(3):218–225 Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140:339–353 Singh D, Geat N, Rajawat MVS (2020) Performance of low and high Fe accumulator wheat genotypes grown on soils with low or high available Fe and endophyte inoculation. Acta Physiol Plant 42:24 Sørensen J, Sessitsch A (2015) Plant-associated bacteria lifestyle and molecular interactions. In: JD van Elsas et al. (Eds.), Modern soil microbiology, 2nd ed, CRC Press, 2006 (2015), pp 211–236 Sprent JI, de Faria SM (1998) Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110:157–165 Molina G, Pimentel MR, Bertucci TCP, Pastore GM (2012) Application of fungal endophytes in biotechnological processes. Chem Eng Trans 27:289–294 Tagliavini M, Rombola AD (2001) Iron deficiency and chlorosis in orchard and vineyard ecosystems. Eur J Agron 15:71–92 Takagi S, Nomoto K, Takemoto T (1984) Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. J Plant Nutr 7:469–477 Takemoto T, Nomoto K, Fushiya S, Ouchi R, Kusano G, Hikino H et al (1978) Structure of mugineic acid, a new amino acid possessing an iron chelating activity from roots washings of water cultured Hordeum vulgare. L Proc Jpn Acad Ser B 54:469–473 Tilak KVBR, Ranganayaki NL, Pal KK, De R, Saxena AK, Nautiyal CS, Mittal S, Tripathi AK, Johri BN (2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89:136–149 Ueno D, Rombola AD, Iwashita T, Nomoto K, Ma JF (2007) Identification of two novel phytosiderophores secreted by perennial grasses. 174(2174) (2): 304–310

14 Siderophore in Plant Nutritional Management …

329

Valencia-Cantero E, Hernández-Calderón E, Velázquez-Becerra C (2007) Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common bean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant Soil 291:263–273 Verma VC, Singh SK, Prakash S (2011) Bio-control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica Juss. J Basic Microbiol 51:550–555 Wallace A (1991) Rational approaches to control of iron deficiency other than plant breeding and choice of resistant cultivars. Plant Soil 130:281–288 Wallner A, Blatzer M, Schrettl M, Sarg B, Lindner H, Haas H (2009) Ferricrocin, a siderophore involved in intra- and transcellular iron distribution in Aspergillus fumigatus. Appl Environ Microbiol 75:4194–4196 Wang Q, Xiong D, Zhao P, Yu X, Tu B, Wang G (2011) Effect of applying an arsenic-resistant and plant growth-promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05–17. J Appl Microbiol 111:1065–1074 Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392 Winkelmann G, Huschka HG (1987) Molecular recognition and transport of siderophores in fungi. In: Winkelmann G, Vander HD, Neilands JB (eds) Iron transport in microbes, plants and animals. VCH, Weinheim, Germany, pp 317–336 Wilson M, Smith NC, Chattington M, Ford M, Dilwyn E, Horvat M (2006) The role of effort in moderating the anxiety–performance relationship: testing the prediction of processing efficiency theory in simulated rally driving. J Sport Sci 24(11):1223–1233 Xiong H, Kakei Y, Kobayashi T, Guo X, Nakazono M, Takahashi H, Nakanishi H, Shen H, Zhang F, Nishizawa NK, Zuo Y (2013) Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant, Cell Environ 36(10):1888–1902 Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150 Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68:2198–2208

Chapter 15

Conclusion Dinesh Kumar Maheshwari

The scientists so far have paid much attention to the understanding of plant beneficial free-living and symbiotic bacteria and only recently realized to look deeper into those microorganisms inhabiting inside the plant tissues and remain asymptomatic (Nerva et al. 2019). The symptomless plants bear certain group of microorganisms which play a vital role in growth and health, promotion of the plants, named as “Endophytes.” These microorganisms include bacteria, actinobacteria, and fungi having the main source of agrobiological interest. They create a host plant–endophyte relationship to provide a beneficial alternative for synthetic fertilizers and pesticides due to their diverse potential for sustainable agroecosystem. Information is given about endophytic microorganisms particularly bacteria for acting as a source of N, P, K, Zn, Fe, S, etc., for enriching the soil in a balanced ecosystem (Pandey et al. 2018). Thus, the major emphasis has been laid down on the promising role of endophytes for green agriculture and to understand them for evolving in plant–microbe interaction processes in the holobionts. The endophytic microbial communities are intimately associated with a different degree with cells and tissues of the plant and form a microbial hub composed of strongly interconnected taxa that grow under the neutral benefit. We undoubtedly made great advances in the commercialization of biofertilizers as biopesticides in bioremediation and microbial inoculants. The advancement of knowledge realized us that endophytes living in plant tissues are significantly more potential to mineralize soil nutrients than free-living bacteria . It has given us a wake-up call to reboot our scientific quest and pay much more attention to those hidden microbes and turn toward mother nature for solutions to the problems of today, i.e., lack of food for humans and animal feed (Arora 2018). The past two D. K. Maheshwari (B) Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_15

331

332

D. K. Maheshwari

decades were evidenced by a growing interest in the investigations aimed at origins, interactions of endophytes, as a new source of asymptomatic establishment in the plants opening horizon of studies in agrobiology. These microorganisms are not limited to bacteria and actinobacteria, even some important groups like fungi are also involved in the production of bioactive compounds. Their beneficial association of mycorrhizal fungi to boost plant growth and productivity enhancement was involved in the book venture. For all these purposes, minimal nutrient uptake and balanced accumulation modulate is an utmost requirement which only met-out by the exploitation of different endophytes genera in crop production (Jayakumar et al. 2019; Guo et al. 2019). Similar to biofertilizers, the commercialization of endophytic organisms as bioinoculants is a reality of the hour and covered in many chapters of the book, this, however, explores the use of the more efficient organisms concerning their potential in crop productivity enhancement via a suitable and sustainable way. This involves resistance mechanisms to the major abiotic and biotic stresses which often create confidence among the farmers (Firrincieli et al. 2020). But to isolate such multifarious endophytes, we have to go back into the biblical era to the present era. For example, dung as a novel source of microbes, if amended with its inhabited bacteria, acted as a catalyst for augmenting the crop productivity and soil fertility for sustainable nutrient management practices. Sometimes nutrient deprivation specifically iron may be proved most beneficiary in the mechanism of plant disease control. This also includes a couple of chapters in the last of the book. On the other hand, endophytes also provide a firm substitute for lack of phosphorus, zinc, potassium, nitrogen, etc., and besides their application, support soil biology (Arya et al. 2020). Considering such viable strategies, the endophytic microorganisms are now established as good as pure chemical fertilizer for boosting crop yield. Harnessing beneficial endophytic microorganisms for delivering macro and micronutrients may provide new trends and prospects to agroeconomy if it meets out the requirements to apply as a formulation product for a wider application similar to the free-living plant growth-promoting rhizobacteria (Etesami and Maheshwari 2018). This complex association is evident in the information provided in this volume. Almost all plants inhabit some endophytic microorganisms and only a few have been studied so far—the diverse plants of different habitats such as temperate, tropical zones. In the last, this is to say that characterization of endophytes using advanced tools can help in finding more bacterial inoculants. Modern tools and techniques of including metagenomics, proteosomes, metabolome, transcriptomes, etc., may help in defining characteristics of endophytes for better improvement of crop productivity. Scientists may reap benefits of day to day increasing publications on endophytes.

15 Conclusion

333

References Arora NK (2018) Environmental sustainability—necessary for survival. https://doi.org/10.1007/s42 398-018-0013-3 Arya R, Pandey C, Dheeman S, Aeron A, Dubey RC, Maheshwari DK, Lei C, Ahmad P, Bajpai VK (2020) Fertilizer adaptive bacteria Acidovorax valerianellae and Sinorhizobium fredii in integrated nutrient management of pigeon pea (Cajanus cajan L.). Afr J Bot. https://doi.org/10. 1016/j.sajb.2020.03.018 Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Safe 156:225–246 Firrincieli A, Khorasani M, Frank AC, Doty SL (2020) Influences of climate on phyllosphere endophytic bacterial communities phyllosphere endophytic bacterial communities of Wild poplar. Front Plant Sci 11:203 Guo Y, Gao P, Li F, Duan T (2019) Effects of AM fungi and grass endophytes on perennial ryegrass Bipolaris sorokiniana leaf spot disease under limited soil nutrients. Euro J Plant Pathol 154(3):659–671 Jayakumar A, Krishna A, Mohan M, Nair IC, Radhakrishnan EK (2019) Plant growth enhancement, disease resistance and elemental modulatory effects of plant probiotic endophytic Bacillus sp. Fcl1. Probiot Antimicrob Prot 11(2):526–534 Nerva L, Turina M, Zanzotto A, Gardiman M, Gaiotti F, Gambino G, Chitarra W (2019) Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants. Environmen Microbiol 21(8):2886–2904 Pandey C, Negi YK, Maheshwari DK, Rawat D, Prabha D (2018) Potential of native cold tolerant plant growth promoting bacilli to enhance nutrient use efficiency and yield of Amaranthus hypochondriacus. Plant Soil 428(1–2):307–320

Index

A Abscisic acid, 189 ACC, 49–51, 54, 56, 58, 188, 190. See also 1-aminocyclopropane, 1-carboxylic acid ACC deaminase, 49–51, 54, 56, 58. See also ACC Acinetobacter, 41, 45, 47, 55 Actinobacteria, 6, 229, 231, 232, 234–237, 239 Actinobacterial endophyte. See Actinobacteria Actinomycetales, 133 Adenosine triphosphate, 210 Agricultural production, 4 Agrobacterium, 158 Agrobiology, 332 Agrochemicals, 207, 209, 210, 293, 294, 296, 298, 301 Agroeconomy, 332 Agroecosystem, 331 Alkaloids, 141 AMF. See Arbuscular mycorrhizal fungi 1-aminocyclopropane, 1-carboxylic acid, 4 Amycolatopsis, 231, 233 Anaerobic fermentation, 81, 93 Animal feed, 331 Animal waste, 81 Ansamitocin, 135 Antagonist, 127 Antibiotic production, 139, 230 Antibiotic(s), 14, 36, 51, 207–209 Anticancer, 124 Antifungal, 124 Antimicrobial, 124 Antioxidant, 124

Apatite, 37 Apoptosis, 124 Arabidopsis, 135 Arbuscular mycorrhiza, 6 Arbuscular mycorrhizal fungi, 230 Arthrobacter, 135, 231–233, 235–237 Ascorbic acid oxidase, 18 Auxin, 124, 189, 207, 210, 298 Azadirachta indica, 323 Azospirillum, 316, 317 Azotobacter, 4, 298, 302, 304

B Bacillomycin, 165 Bacillus, 4, 15, 16, 18, 41, 44–47, 50–52, 54– 57, 79, 80, 82–84, 93, 158–160, 163– 173, 211, 213, 214, 216, 218, 271, 274–277, 298–300, 302–304, 306 amyloliquefaciens, 165–168, 170, 172 cereus, 165 megaterium, 165, 170–172 pumilus, 165, 167, 168, 172 Bacterial blight, 236 Bacteriocins, 159, 167 Basidiomycota, 42, 48 BCA. See Biological control agents Betaproteobacteria, 214 Bifidobacterium, 80 Bioactive metabolic compounds, 193 Bioavailability, 138 Biocontrol, 4, 19, 230 Biodiesel, 215 Biodiversity, 133, 158 diversity, 162, 163, 170 Biofertilizers, 210, 331

© Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4

335

336 Biofilms, 159, 162 Biofuel, 216 Bio-gas, 79, 81, 92, 93 biogas production, 81, 82. See also gobar gas Bioinformatics, 8 Biological control. See Biocontrol Biological control agents, 11–13, 22, 127 Bioremediation, 8, 181, 182, 192, 324 Biotechnology, 8, 207, 209 Brassica napus, 43 Brazilian mangroves, 218 Buffalo dung, 78, 81, 89 Burkholderia, 14, 18, 41, 44, 45, 49, 51, 54, 58, 59, 158, 298, 300, 302–304 Burkholderiales, 133

C Camptothecin, 135, 141 Castor, 215 Catecholate siderophores, 236 Cellulomonas, 231, 232, 236, 237 Cell wall, 236 Cepabactin, 139 Cereals, 158 Charcoal, 79 Chemotaxis, 132 Chickpea, 278 Chitinases, 159, 207, 208 Chloramine –T, 234 Chlorophytum, 41 Chryseobacterium, 272, 276–278 Citrobacter, 79, 80 Clavicipitaceae, 127 Claviciptaceous endophytes, 42 Climate change, 247, 248, 259 Coffea arabica, 212–214 Colletotrichum, 126, 127, 130, 141, 144 Compost, 297, 304 Comptotcin, 124 Convolvulaceae, 135 Corynebacterium, 231, 232 Cow dung, 90 dung, 79, 81, 83, 84, 86–89, 92, 93 Cow urine, 82 Cronobacter, 214 Crop-fertilization, 268 Crop production, 293, 297, 301 Crop productivity, 78, 86, 267, 332 Crop protection. See Biocontrol Curtobacterium, 42, 50, 231–233, 238, 239

Index Cytokinins, 124, 189, 298

D DAPG 2,4-diacetylphloroglucinol, 14 2,4-diacetylphloroglucinol, 14 Diazotrophic endophytes, 272 disease control. See Biocontrol Diterpene, 141

E Ecological niche, 36 Ecomycin, 134 Ecosystem, 78, 87, 94, 207, 210, 217, 331 Endophytes, 3, 12–14, 16–24, 36, 38–43, 45–53, 57, 59, 60, 159, 160, 164, 181, 183, 207, 208, 210, 211, 247–249, 251, 253, 254, 257, 259, 331, 332 colonization, 160–162, 166, 167, 173 Eucalyptus–endophytic bacteria, 164 facultative endophytes, 160, 184 migration, 162 obligate endophytes, 184 oligate endophytes, 181–185, 191–195 penetration, 162 Endophytic fungi, 6, 247 Endophytic rhizobacteria, 267 Endosphere, 36, 38, 47, 50, 58, 273, 279 Enterobacter, 79, 80, 82, 83, 158, 214, 218, 271, 274, 277, 278 Enterobacteriales, 133 Enterobactin, 317, 320 Environmental pollution, 268 Epichloë, 249, 250, 253–256, 258 Epoxy-janthitrem, 141 Ergopeptine, 141 Ergosterol, 139 Ergovaline, 141 Erwinia, 212, 214 Escherichia, 79, 83 Ethylene, 17, 23 Euryarchaeota, 80 Exopolysaccharide, 159 Extracellular enzymes, 190 amylases, 190 cellulases, 190 Chitinase, 190 dehydrogenase, 190 lipases, 190

Index F Falvobacterium, 278 Fengycin, 165 Fermentation, 140 Ferrichrome, 317, 320, 322, 323 Ferrioxamines, 8 Fertilizers, 5, 78–80, 82, 88, 90–93, 158, 163, 207, 209, 210, 219, 220, 247, 249, 254, 267, 269, 272, 274, 281, 293, 294, 297, 301, 302, 306 inorganic fertilizers, 78, 91, 92 NPK, 90–92 Ferula songorica, 132 Firewood, 79 Firmicutes, 12, 158, 214 Flavobacteriales, 133 Flavonoids, 132 Fluorescence in situ hybridization, 40 Food security, 294, 296, 307, 315 Free-living bacteria, 331 Fuelwood, 78, 79 Funneliformis mosseae, 231, 233, 235, 238, 240 FYM, 297 G GA3 Gibberellin, 239 Gammaproteobacteria, 214 Genomic, 181, 182, 193, 195 Gibberellic acid, 46, 50 Gibberellin, 124, 189, 239, 298 Global warming, 268 Glomus mosseae, 231, 232, 234, 235, 237– 239 Gluconacetobacter, 270, 271, 276 Gluconic acid, 236 Glycyrrhizic acid, 138 Gobar gas, 81 Gram-positive, 229, 230 H HCN, 298 Herbaspirrilum, 316 Homeostasis, 132, 256 Hydrogen cyanic (HCN) acid production, 4 Hydrogen cyanide, 190 Hydrolytic enzymes, 247, 254 amylases, 84 cellulases, 84 gelatinase, 84 urease, 84

337 xylanases, 84 Hydroxamate siderophores, 236 Hydroxyapatite, 37 Hydroxymate, 8 I IAA. See Auxin IAA production. See Auxin Illumina pyrosequencing, 41 Immobilization, 209, 211 Indole-3-acetic acid, 42, 50, 65 Induced systemic resistance, 4, 191, 297. See also ISR Industrial agriculture, 207 Inorganic phosphorus, 37 Intrasporangium, 231, 232, 237 Isoflavonoids, 132 ISR, 14, 17, 22–26. See also Induced systemic resistance J JA-signalling pathways, 17 Jasmonic acid, 17, 189, 197 Jatropha, 215, 216 Jatropha curcas, 215 K Kakadumycins, 134 Klebsiella, 79, 83, 158, 214, 216 Kluyvera, 79 Kosakonia, 214 KSB, 272, 273. See also Potassium solubilizing bacteria Kurthia, 214 L Lactobacillus, 79 Land degradation, 268 Lateral roots, 132 Leifsonia, 231, 232, 235–239 Lenticels, 132 Livestock, 78, 79, 93 Livestock dung, 78 Lysinibacillus, 214 Lytic enzyme, 36 M Macronutrients, 294, 300, 304 Mahonia fortune, 139

338 Maize cereals, 158, 159, 163–165, 170, 171, 173 MALDI-TOF, 214 Malonic acid, 236 Mangrove forests, 217 Maytansinoid, 135 Medicago truncatula, 135 Medicine, 8 Metabolomics, 181, 182, 193, 195 Metagenomics, 40, 41 Metatranscriptomic, 182 Methanobacterium, 80, 82 Methanobrevibacter, 80 Methanomicrobium, 80 Methanosarcina, 80, 82 Microbacterium, 41, 42, 54, 55, 214, 216, 271, 274, 276, 278, 300 Microbial inoculants, 207 Micrococcus, 275, 278 Micronutrients, 236, 247, 251, 294, 299, 304 Millet, 158, 160, 164 Mineralization, 207, 209, 217 Mineral nutrients acquisition, 267, 269, 278– 280 Mineral nutrient uptake, 247 Mineral phosphate, 37 Minerals, 36, 37, 78, 79, 85, 208, 249, 251, 253, 272, 306, 317, 325 Mineral solubilization, 254 Modern agriculture, 11 Morgarella, 79 Municipal wastes, 138 Mycobacterium, 231, 233, 238, 239 Mycoparasitism, 130 Mycorrhiza, 231–235, 237, 238 Mycorrhizal fungi, 332

N Nif H, 42 Nitrogen fixation, 4, 42, 49, 50, 55 Nocardia, 231, 232, 237 Nocardioides, 231 NodD, 42 NUE. See Nutrient use efficiency Nutrient-deficiency, 267 Nutrient management, 78 Nutrient solubilization, 247 Nutrients replacement, 248 Nutrient uptake, 293, 298, 300, 302–304, 307 Nutrient use efficiency, 5, 301, 302

Index O Organic manures, 5 Oryza sativa, 240 Oxalic acid, 236 Oxidative stress, 39 Oxyapatite, 37 P Paenibacillus, 158, 213, 217 Pantoea, 16, 158, 213, 214 Parasitism, 19 Pasteurella, 79 Pathogenesis-related gene. See PR gene PCR, 186 Penicillium skrjabinii, 139 Peroxidase, 18, 321 Pesticides, 207, 209, 219, 222 Pest-management, 12 PGPB. See PGPR; Plant growth-promoting rhizobacteria PGPR, 85, 296, 297, 299, 300, 302, 303, 305. See also Plant growth-promoting rhizobacteria Pharmaceutical, 6 Pharmacology, 181, 182, 194 Phenazine, 139 Phenylalanine ammonia-lyase, 18 Phosphate buffer saline, 234 Phosphate solubilization, 4, 35, 36, 42, 45– 50, 54, 55, 58–60, 208, 210–212, 214, 216–219 Phosphate-solubilizing bacteria, 207, 211 Phosphate-solubilizing microbes, 37, 46, 304 Phosphatic fertilizers, 35–37 Phosphorus. See Phosphorus solubilization Phosphorus cycle, 208, 211 Phosphorus deficiency, 35, 36, 44 Phosphorus solubilization, 43, 47, 188, 209, 212, 217, 317 Phytoextraction, 138 Phytohormone production, 4 Phytohormones, 159, 298 Phytomining, 138 Phytopathogens, 182, 189, 191, 192, 207, 208 Phytophthora, 17, 22, 23 Phytoremediation, 132, 138, 181, 182, 192, 194 Phytosiderophore, 317, 320 Phytotoxicity, 132 Plant-fungal symbioses, 253 Plant growth hormones, 297

Index Plant growth-promoting bacteria, 158, 159, 297–299 Plant growth-promoting rhizobacteria, 8, 332. See also PGPR Plant growth promotion, 181, 187, 190 Plant immunity, 36 Plant-microbe interaction, 4 Plant microbiome, 267, 269, 280 Podophylotoxine, 124 Polymerase chain reaction, 186 Polyphenol oxidase, 18 Potassium solubilization, 273 Potassium solubilizing bacteria, 272 Potato diseases, 140 Powdery mildew, 140 Pramine, 141 PR gene, 18 Propagation, 139 Propionibacterium, 231 Propionic acid, 236 Proteases, 159 Proteobacteria, 158, 184 Proteomics, 181, 193 Providencia, 79 PSB, 273, 274. See also P solubilizing bacteria Pseudomonadales, 133 Pseudomonas, 4, 14–16, 24, 39, 41, 42, 44– 47, 51, 52, 54–57, 59, 79–84, 158, 211, 212, 214, 271, 272, 274–277, 298–300, 302–304, 306 Pseudomycins, 134, 316 Pseudonocardia, 231, 233, 235 Pseudoxanthomonas, 278 PSM, 37. See also Phosphate-solubilizing microbes P solubilization index, 218 P solubilizing bacteria, 273 Pyoverdine, 8 Pyrosequencing, 41, 133 Pyrrolizidine, 141 Pyrrolnitrin, 14, 139 Q Quorum sensing, 39, 58 R Reactive oxygen species, 18. See also ROS Reclamation, 216 Remediation. See Bioremediation Rhizobacteria, 267–280 Rhizobia, 4

339 Rhizobiales, 133 Rhizobium, 158, 214, 217 Rhizoctonia solani, 139 Rhizophagus intraradices, 236 Rhizophagy cycle, 213 Rhizosphere, 36, 38, 39, 41, 48, 49, 53, 56– 58, 60, 160–164, 170, 171, 253, 254, 256, 264 Rice cereals, 158, 160, 165, 170 Ricinus communis, 215 Rock phosphates, 36 Root-nodulating. See Rhizobia Root radical, 132 ROS, 18 Ryegrass, 135

S Salicylic acid, 17 SAR, 17. See also Systemic acquired resistance SA-signalling pathway, 17 Secretomes, 195 Sediments, 138 Siderophore production, 4, 50, 54, 55, 277, 278 Siderophores, 8, 36, 207–209, 214, 218, 247, 250, 253, 255, 256, 259, 277, 317, 323, 324 Soil ecology, 4, 207 Soil fertility, 5, 78, 84–87, 89–91, 293, 294, 296, 297, 304, 307 Soil microbiomes, 207 Soil microorganisms, 4 Soil phosphorus, 37 apatite, 37 hydroxyapatite, 37 oxypatite, 37 Soil-P solubilization, 254 Soil regeneration cycle, 247 Soil toxicity, 79 Sorghum, 158, 160 Sphingomonadales, 133 Sphingomonas, 42, 158 Spore-forming Bacillus. See Bacillus Staphylococcus, 158, 166, 214 Stenotrophomonas, 18, 41, 51, 52, 54–56, 272, 276, 277 Stomata, 132 Streptomyces, 230–233, 235–238, 240, 242 Streptosporangium, 231, 232, 237 Streptoverticillium, 231, 232, 237

340 Sugar beet, 133 Sustainable agriculture, 35, 267, 280 Sustainable farming model, 247 Sustainable soil management, 248 Swine manure, 89, 92 Symbiotic mutualism, 182 Systemic acquired resistance, 4. See also SAR

T Tannins, 130 Terpenoids, 132 Transcriptomic, 181, 193 Trichome, 132

V Vermicompost, 297 Verticillium dahlia, 14 Vitamins, 124 VOC, 16. See also Volatile organic compounds VOCs, 24. See also VOC Volatile organic compounds, 16

Index HCN, 159, 166, 167

W Waksman’s agar, 233, 234 Wheat cereals, 158, 159

X Xanthomonadales, 133 Xanthomonas campestris, 16 Xanthomonas campestris, 16 Xylanolytic bacteria, 84 Xylaria, 127

Z Zinc solubilization, 235, 236, 274, 277 Zn solubilizing bacteria, 274 Zn uptake, 274, 277 ZSB, 274, 277. See also Zn solubilizing bacteria Zygomycota, 42