Bioinoculants: Biological Option for Mitigating global Climate Change [1st ed. 2023] 9819929725, 9789819929726

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Surender Singh Radha Prasanna Kumar Pranaw   Editors

Bioinoculants: Biological option for mitigating global climate change

Bioinoculants: Biological Option for Mitigating global Climate Change

Surender Singh • Radha Prasanna • Kumar Pranaw Editors

Bioinoculants: Biological Option for Mitigating global Climate Change

Editors Surender Singh Department of Microbiology Central University of Haryana Mahendergarh, India

Radha Prasanna Division of Microbiology ICAR-Indian Agricultural Research Institute New Delhi, India

Kumar Pranaw Department of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology University of Warsaw Warsaw, Poland

ISBN 978-981-99-2973-3 ISBN 978-981-99-2972-6 https://doi.org/10.1007/978-981-99-2973-3

(eBook)

# The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 This work is subject to copyright. All rights are solely and exclusively licensed 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 Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Preface

This book was conceptualized to address the impact of climate change on biota and the environment, which are vital to feeding the world's population, and provide mitigation options through microbiology. Climate change-mediated drought and salinity are major environmental stresses that alter plant physiological, biochemical, and molecular processes, resulting in a significant loss in agricultural yields. Chemical overuse has become a serious concern to human health and the environment. An environmentally friendly method for increasing crop productivity under environmental stress is the use of beneficial microbes. The diversity of microorganisms including bacteria, fungi, and other microbes that coexist in the rhizosphere around plant roots is extraordinary. In the soil root zone, PGPMs are considered excellent competitors that aid in promoting plant development or squelching disease. Beneficial microorganisms used as inoculants not only improve plant development by addressing nutritional requirements but also assist in countering environmental fluctuations and constraints. The primary goal and purpose of this book are to highlight key aspects related to the use of microbial bioinoculants (especially plant growth-promoting microbes) in agricultural crop production, as a biological alternative for mitigating climate change to assist scientists worldwide working on this subject. Crop simulation models are receiving a lot of attention as researchers investigate the influence of climate change on agricultural output and food security, and the inclusion of microbiological data can further refine the predictions. Under the current climatic conditions, the opportunities for increasing agro-productivity presented by PGPMs are urgently required to feed the burgeoning global population. Thus, using PGPMs as options to counteract diseases, drought, salt, and heavy metal stress and impart tolerance in plant types, thereby enhancing the nutritional value, may aid in achieving the objective of sustainable agriculture. This book titled Bioinoculants: Biological Option for Mitigating Global Climate Change explores the role of microbes in sync with the current efforts for sustainable agricultural development. Comprising 14 chapters, this book covers how bioinoculants of diverse types, and having unique modes of action, influence and increase the robustness of crop plants under changing climatic conditions. The authors, who belong to diverse nations, including India, Indonesia, Italy, and Poland, highlight the function of microbial bioinoculants in promoting the growth of different crop plants and mitigating the effects of climate change. v

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We anticipate that the readers of this book—students, educators, researchers, and entrepreneurs engaged in PGPMs and allied fields—will find it useful and motivating. Editing this book has been enjoyable, and we appreciate the active engagement of all the authors who provided timely information to facilitate its consolidation in the shape of this book. We would like to extend our sincere gratitude to the Springer team in India for their cooperation and support in this endeavor of putting this book together in a publishable form. Mahendragarh, India New Delhi, India Warsaw, Poland

Surender Singh Radha Prasanna Kumar Pranaw

Contents

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Microbial Inoculants in the Climate Change Scenario: An Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Surender Singh, Kumar Pranaw, Radha Prasanna, Pawan Kumar, and Vikram Poria Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in Mitigating Climate Change . . . . . . . . . . . . . . . . Kulandaivelu Velmourougane and Radha Prasanna Emerging Weeds Under Climate Change and Their Microbial Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Himanshu Mahawar, Apekcha Bajpai, Dasari Sreekanth, Deepak Pawar, and K. K. Barman Climate Change and Agriculture: Impact Assessment and Sustainable Alleviation Approach Using Rhizomicrobiome . . . . . . . Ravi Kumar, Ajay Kumar, Rahul Kumar Dhaka, Madhvi Chahar, Sandeep Kumar Malyan, Arvind Pratap Singh, and Anuj Rana

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Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115 Devendra Singh, Anil Kumar Verma, Mahipal Choudhary, Himanshu Mahawar, Shobit Thapa, and Moti Lal Mehriya

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Legume–Rhizobium Symbiosis and Beyond: Producing Synthetic Communities for Increasing Crop Production Under Climate Change Challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 Francesca Vaccaro and Alessio Mengoni

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Salinity Mitigation Using Microbial Inoculants . . . . . . . . . . . . . . . . 163 Vikram Poria, Sandeep Kumar, Radha Prasanna, Somu Yadav, Pawan Kumar Maurya, and Surender Singh

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Cyanobacterial Bioinoculants for Abiotic Stress Management in the Changing Climate Scenario . . . . . . . . . . . . . . . . . . . . . . . . . . 179 Shobit Thapa, Ritu Vishwakarma, and Yalavarthi Nagaraju vii

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Alleviation of Drought Stress and Amelioration of Tomato Plant Growth by Bacterial Inoculants for Mitigating Climate Change . . . 201 K. Tamreihao, Rakhi Khunjamayum, H. Shingmuan, Wahengbam Pusparani Chanu, Pintubala Kshetri, Thangjam Surchandra Singh, Ngangkham Umakanta, A. Thirugnanavel, Susheel Kumar Sharma, and Subhra Saikat Roy

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Associative Nitrogen Fixers- Options for Mitigating Climate Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 Minakshi Grover, Sivakumar Yaadesh, and Anegundi Jayasurya

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Trichoderma-Based Bioinoculant: A Potential Tool for Sustainable Rice Cultivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 Sulistya Ika Akbari, Nur Syafikah Abdullah, Nandang Permadi, Nia Rossiana, Nurul Shamsinah Mohd Suhaimi, Norman Uphoff, and Febri Doni

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Photosynthetic Microorganisms and Their Role in Mitigating Climate Change Through C Sequestration and Plant-Soil Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265 Venkatesh Kokila, Bidisha Chakrabarti, and Radha Prasanna

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Arbuscular Mycorrhizal Fungi: A Keystone to Climate-Smart Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283 Seema Sangwan, Garima Saxena, Pratibha Barik, and Ram Swaroop Bana

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Microbial Siderophores in Sustainable Applications—Preventing and Mitigating Effects of Climate Change . . . . . . . . . . . . . . . . . . . . 297 Marcin Musiałowski and Klaudia Dębiec-Andrzejewska

Editors and Contributors

About the Editors Surender Singh received his B.Sc. (Hons.) Agriculture from Chaudhary Charan Singh Haryana Agricultural University, Hisar (India). He obtained his M.Sc. and Ph. D. in Microbiology from Indian Agricultural Research Institute (IARI), New Delhi, in 2005 and 2009 respectively before joining as Scientist (ARS) in IARI, New Delhi. He joined Central University of Haryana in 2018. His current research focuses on the development of multi-stress tolerant bioinoculants and organic matter recycling including bioethanol production from lignocellulosic material. He was awarded the prestigious Endeavour Research Fellowship (2011) by the Government of Australia for his academic excellence to carry out 6-month research at the University of South Australia, Adelaide. He was also awarded the Young Scientist award 2015 by Association of Microbiologists of India (AMI), Young Scientist Award (2015-16) by National Academy of Agricultural Sciences (NAAS), New Delhi, and Haryana Yuva Vigyan Ratan (2018) by the Department of Science and Technology, Government of Haryana. Dr. Singh has been involved in 6 research projects funded extramurally by ICAR, DBT, DST, and MoEF (Government of India). He is currently supervising 6 doctoral scholars and has supervised more than 15 PG dissertations in the past. He has authored more than 80 research articles, one book, 15 book chapters, and is an active reviewer for many reputed journals in microbiological research. He is also an editorial board member of Electronic Journal of Biotechnology and Frontiers of Microbiology. Prof. Singh is a Life Member of Association of Microbiologists of India (AMI) and Indian Science Congress. Radha Prasanna completed her master’s and Ph.D. programs from Indian Agricultural Research Institute (ICAR-IARI), joined as Scientist in 1996, and presently serving as Head & Principal Scientist, Division of Microbiology, ICAR-IARI, New Delhi. Her major research interests focus in the areas of natural resource management and crop protection, through deploying integrated nutrient/disease management strategies and modern omics tools. She is passionate about diversifying the role of cyanobacteria and their consortia in crops, besides rice, and their significant role as plant growth-promoting inoculants for wheat, maize, cotton, legumes, and

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vegetable crops and as biocontrol agents against phytopathogenic fungi in cereal and vegetable crops. She is actively involved in postgraduate teaching and research guidance of M.Sc./ Ph.D. students at ICAR-IARI. She has been recognized as Outstanding Reviewer by Elsevier, Springer, and Wiley journals, besides being identified as Top Peer Reviewer by Publons. She is serving as Associate Editor, BMC Microbiology and CABI Agriculture and Bioscience, and Member, Editorial Advisory Board, Journal of Basic Microbiology. She has published more than 230 research papers in peerreviewed journals, most of them highly cited. She is the recipient of NAAS Fellowship (2022), Fellowship of the Academy of Microbiological Sciences (FAMSc 2019), Hari Krishna Shastri Award (2017), ICAR Panjabrao Deshmukh Outstanding Woman Scientist Award (2012), and IARI Best Teacher Award (2008) for her outstanding contributions to research and teaching. Kumar Pranaw completed his bachelor’s in 2006 with a B.Sc. (Hons.) Microbiology from Sam Higginbottom Institute of Agriculture, Technology & Sciences (formerly known as Allahabad Agricultural Institute-Deemed University), Allahabad, India. He obtained his master’s degree in Applied Microbiology from Vellore Institute of Technology, Vellore, India, in 2008. He joined Indian Agricultural Research Institute in 2009 as Senior Research Fellow and started working on microbial enzymes and their role in bio-pesticidal activity as well as in bioremediation. He registered for his doctoral study at the National Institute of Technology, Durgapur, India, in collaboration with the Indian Agriculture Research Institute, New Delhi, India, and received his Ph.D. (Biotechnology) in 2014. His expertise has been enriched by academic as well as industrial research experience at eminent national and international institutions. Currently, he leads a multinational research group at the University of Warsaw, Poland, which works towards innovative solutions for realizing the zero-waste circular economy concept by probing plant growth-promoting bacteria for sustainable agriculture and utilizing the generated agro-wastes for high value-added products. Presently, he is supervising 2 postdocs and 2 doctoral scholars and has supervised several PG/UG dissertations in the past. He has authored more than 30 research articles in different peer-reviewed journals and is an active reviewer for many reputed international journals in the field of applied microbiology, sustainable agriculture and environment, and waste valorization. He has presented his research achievements at several national and international conferences. He is actively engaged in different professional societies like Life Member of the Association of Microbiologists of India, Life Member of the Biotech Research Society, India, Member of American Society for Microbiologists, USA, and Member of European Federation of Biotechnology, Switzerland.

Contributors Nur Syafikah Abdullah Institute for Advanced Studies, University of Malaya, Kuala Lumpur, Malaysia

Editors and Contributors

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Sulistya Ika Akbari Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Padjadjaran, Jatinangor, West Java, Indonesia Apekcha Bajpai ICAR-Indian Institute of Soil Science, Bhopal, India Ram Swaroop Bana Division of Agronomy, ICAR-Indian Agricultural Research Institute, New Delhi, India Pratibha Barik Division of Microbiology, ICAR Indian Agricultural Research Institute, New Delhi, India K. K. Barman ICAR—Directorate of Weed Research, Jabalpur, Madhya Pradesh, India Madhvi Chahar Department of Bio-Nanotechnology, Guru Jambheshwar University of Science and Technology, Hisar, India Bidisha Chakrabarti Division of Environment Science, ICAR-Indian Agricultural Research Institute, New Delhi, India Wahengbam Pusparani Chanu Microbial Biotechnology Research Laboratory (MBRL), Department of Biochemistry, Manipur University, Canchipur, India Mahipal Choudhary ICAR—Central Arid Zone Research Institute, Jodhpur, Rajasthan, India Klaudia Dębiec-Andrzejewska Department of Geomicrobiology, Faculty of Biology, Institute of Microbiology, University of Warsaw, Warsaw, Poland Rahul Kumar Dhaka Department of Chemistry, College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India Febri Doni Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Padjadjaran, Bandung, West Java, Indonesia Minakshi Grover ICAR-Indian Agricultural Research Institute, New Delhi, India Anegundi Jayasurya ICAR-Indian Agricultural Research Institute, New Delhi, India Rakhi Khunjamayum Microbial Biotechnology Research Laboratory (MBRL), Department of Biochemistry, Manipur University, Canchipur, India Venkatesh Kokila Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India Pintubala Kshetri ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India Ajay Kumar Department of Microbiology, College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India

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Editors and Contributors

Pawan Kumar Department of Microbiology, Central University of Haryana, Mahendragarh, India Ravi Kumar Department of Botany and Plant Physiology (Environmental Science), College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India Sandeep Kumar Department of Microbiology, Central University of Haryana, Mahendragarh, India Himanshu Mahawar ICAR—Directorate of Weed Research, Jabalpur, Madhya Pradesh, India Sandeep Kumar Malyan Department of Environmental Studies, Dyal Singh Evening College, University of Delhi, New Delhi, India Pawan Kumar Maurya Department of Biochemistry, Central University of Haryana, Mahendragarh, India Moti Lal Mehriya Agricultural Research Station, Mandor, Agriculture University, Jodhpur, Rajasthan, India Alessio Mengoni Department of Biology, University of Florence, Florence, Italy Marcin Musiałowski Department of Geomicrobiology, Faculty of Biology, Institute of Microbiology, University of Warsaw, Warsaw, Poland Yalavarthi Nagaraju ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India Deepak Pawar ICAR—Directorate of Weed Research, Jabalpur, Madhya Pradesh, India Nandang Permadi Program in Biotechnology, Graduate School, Universitas Padjadjaran, Bandung, West Java, Indonesia Vikram Poria Department of Microbiology, Central University of Haryana, Mahendragarh, India Kumar Pranaw Department of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland Radha Prasanna Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India Anuj Rana Department of Microbiology, College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India Nia Rossiana Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Padjadjaran, Jatinangor, West Java, Indonesia

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Subhra Saikat Roy ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India ICAR-Central Citrus Research Institute, Nagpur, Maharashtra, India Seema Sangwan Division of Microbiology, ICAR Indian Agricultural Research Institute, New Delhi, India Garima Saxena Division of Microbiology, ICAR Indian Agricultural Research Institute, New Delhi, India Susheel Kumar Sharma ICAR-Indian Agricultural Research Institute, New Delhi, India H. Shingmuan Microbial Biotechnology Research Laboratory (MBRL), Department of Biochemistry, Manipur University, Canchipur, India Arvind Pratap Singh School of Biotechnology, Jawaharlal Nehru University, New Delhi, Delhi, India Devendra Singh ICAR—Central Arid Zone Research Institute, Jodhpur, Rajasthan, India Surender Singh Department of Microbiology, Central University of Haryana, Mahendragarh, India Thangjam Surchandra Singh ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India Dasari Sreekanth ICAR—Directorate of Weed Research, Jabalpur, Madhya Pradesh, India Nurul Shamsinah Mohd Suhaimi Faculty of Science, Institute of Biological Sciences, University of Malaya, Kuala Lumpur, Malaysia Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, Kuala Lumpur, Malaysia K. Tamreihao Department of Botany, St. Joseph College, Ukhrul, Manipur, India ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India Shobit Thapa ICAR-National Bureau Microorganisms, Mau, Uttar Pradesh, India

of

Agriculturally

Important

A. Thirugnanavel ICAR-Central Citrus Research Institute, Nagpur, Maharashtra, India Ngangkham Umakanta ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India Norman Uphoff Department of Global Development, Cornell University, Ithaca, NY, USA

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Francesca Vaccaro Department of Biology, University of Florence, Florence, Italy Kulandaivelu Velmourougane ICAR-Central Institute for Cotton Research, Nagpur, Maharashtra, India Anil Kumar Verma Agricultural Research Station, Mandor, Agriculture University, Jodhpur, Rajasthan, India Ritu Vishwakarma ICAR-National Bureau Microorganisms, Mau, Uttar Pradesh, India

of

Agriculturally

Important

Sivakumar Yaadesh ICAR-Indian Agricultural Research Institute, New Delhi, India Somu Yadav Department of Biochemistry, Central University of Haryana, Mahendragarh, India

Abbreviations

ABA ACC ACW AHL AMF APX BLB BNF BSC BSMR Ca CASH CAT CO2 COD CRISPR/Cas9 CWDE DAP DREB DWR EC eCO2 EPS EPSP ET FAO FBA Fur GENRE GHGs GM GPX

Abscisic acid 1-Aminocyclopropane-1-carboxylate Asbestos containing waste N-acyl homoserine lactone Arbuscular mycorrhizal fungi Ascorbate peroxidase Bacterial leaf blight Biological nitrogen fixation Biological soil crusts BioMetal Sludge Reactor Calcium Cornell’s Comprehensive Assessment of Soil Health Catalase Carbon dioxide Chemical oxygen demand Clustered regularly interspaced short palindromic repeats/ CRISPR-associated protein 9 Cell wall-degrading enzyme Diammonium phosphate Dehydration element-binding protein Directorate of Weed Research Electrical conductivity Elevated carbon dioxide Exopolysaccharides 5-enolpyruvylshikimate-3-phosphate Ethylene Food and Agricultural Organization Flux Balance Analysis Ferric uptake regulation Genome-Scale Metabolic Network Reconstruction Greenhouse gases Genetic modification Glutathione peroxidase xv

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GS GSM ha HCN HSP IAA IAPs IPCC ISR IST JA MDA MPa MT MW NADPH NN NUE P PCA PEG PEPC PGP PGPB PGPF PGPM PGPR PPM PR REE RFA RGB ROS RuBisCO RuBP SA SAR SIAREB SMAF SOC SOD SPB SRI SynCom TALEN

Abbreviations

Glutamine synthetase Genome-Scale Modeling Hectare Hydrogen cyanide Heat shock protein Indole acetic acid Invasive alien plants Inter-Governmental Panel on Climate Change Induced systemic resistance Induced systemic tolerance Jasmonic acid Malondialdehyde Mega Pascal Metric tonne Molecular weight Nicotinamide adenine dinucleotide phosphate Neural network Nitrogen use efficiency Phosphate Principal component analysis Polyethylene glycol Phosphoenol pyruvate carboxylase Plant growth promotion Plant growth-promoting bacteria Plant growth-promoting fungi Plant growth-promoting microorganisms Plant growth-promoting rhizobacteria Parts per million Pathogen defense-related Rare earth elements Random Forest Analysis Red, green, and blue Reactive oxygen species Ribulose bisphosphate carboxylase/oxygenase Ribulose bisphosphate Salicylic acid Systemic acquired resistance ABA-responsive element binding protein Soil Management Assessment Framework Soil organic carbon Superoxide dismutase Siderophores producing bacteria System of Rice Intensification Synthetic community Transcription activator-like effector nucleases

Abbreviations

TCA TFs UV ViNE VOC ZFN Zn

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Tricarboxylic acid Transcription factors Ultraviolet Virtual Nodule Environment Volatile organic compounds Zinc-finger nucleases Zinc

1

Microbial Inoculants in the Climate Change Scenario: An Overview Surender Singh, Kumar Pranaw, Radha Prasanna, Pawan Kumar, and Vikram Poria

Abstract

Agriculture accounts for approximately 11% of the total global GHG (greenhouse gases) emissions, and with the increase in emissions globally, efforts need to focus on improving farm management practices and the options used, more effectively and efficiently. Drought, rising temperatures, and greenhouse gas emissions all directly or indirectly impact human health and productivity of natural and agricultural ecosystems. The current farming practices also harm the food chain and ecosystem functioning. Applying beneficial microbial inoculants is one of the various techniques suggested to combat this widespread agricultural issue sustainably and mitigate the detrimental effects of the climate change. Beneficial microorganisms used as inoculants not only promote plant growth by addressing nutrient needs but also contribute significantly to manage environmental challenges. These microorganisms produce different types of substances such as extracellular polysaccharides (EPS), 1-aminocyclopropane1-carboxylate (ACC) deaminase, siderophores, antioxidants, and volatile organic compounds (VOCs) that facilitate plants to negate the effects of climate change. This book chapter emphasizes the benefits of microbial inoculants and explores the mechanisms deployed in the mitigation of climate change on agricultural practices and balancing the ecosystem faction. S. Singh (✉) · P. Kumar · V. Poria Department of Microbiology, Central University of Haryana, Mahendergarh, India K. Pranaw Department of Environmental Microbiology and Biotechnology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland e-mail: [email protected] R. Prasanna Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_1

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Keywords

Bacteria · Climate change · Stress management · Abiotic stress · Phytohormones

1.1

Introduction

With its far-reaching consequences on human and environmental health and agricultural output, climate change is currently the world’s top-ranked concern in terms of priority and challenge. Persistent deforestation and relentless use of fossil fuels have led to the rise in the atmospheric concentration of CO2 from 280 μmol-1 to 400 μmol-1. Scientists believe that by the end of this century, atmospheric CO2 levels would increase twofold, reaching 800 mol-1 (Raza et al. 2019). The repercussions of climate change and ecological diversity are evaluated mostly based on the duration of stress phases, their influence on everyday life, and crop damage. Stresses from the environment have a significant impact on plant development and productivity. Waterlogging, drought, extreme heat or cold, and salinity are some of the climatic challenges that plants must endure in their natural environments. According to information published in 2016, the Food and Agriculture Organization (FAO) predicts that, if the current trend of greenhouse gas emissions and climate change continues, there will be a reduction in the yields of major cereal crops such as maize (20–45%), wheat (5–50%), and rice (20–30%) by the year 2100 (Arora 2019). Using microbial inoculants is not only a practical method for boosting plant growth in these conditions, but it can also play a crucial role in maintaining environmental harmony. Microbial inoculants improve crop production, even under stress, through the release of numerous types of biological compounds, such as phytohormones, exopolysaccharides, biofilm, antioxidants (Singh et al. 2020), cryoprotectants (Harun-Or-Rashid and Chung 2017), and enhanced enzyme activity, such as that of ACC deaminase (Ansari et al. 2019; Goswami and Deka 2020). Besides their role in plant growth promotion, microbes also play an essential role by balancing the soil dynamics, e.g., methane production and carbon sequestration (Disi et al. 2019).

1.2

Classification of Microbial Inoculants

In sustainable production and the mitigation of climate change, microbial inoculants play a dynamic role in reducing the risks associated with environmental and agricultural practices. They can be classified into different categories based on the microorganisms involved viz. bacteria, algae, fungi, or in terms of their mechanisms of action as biofertilizers, biocontrol agents, and bioremediation agents (Fig. 1.1).

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Microbial Inoculants in the Climate Change Scenario: An Overview

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Fig. 1.1 Classification of microbial inoculants based on microorganism type and mode of action

1.2.1

Microbial Inoculants as Biofertilizers

1.2.1.1 Nitrogen Fixers Biological nitrogen fixation is accomplished to a great extent by symbiotically associated N2 fixers, especially rhizobia, which develop symbiotic relationships with the roots of legume crops. A complex organization and the transmission of biochemical signals between the host plant and symbionts, in other words, rhizobia, result in the formation of nodules (Kumar et al. 2022b). Nodules utilize the enzyme nitrogenase to convert atmospheric nitrogen into ammonia. Aside from rhizobia, free-living diazotrophs also possess the nitrogenase enzyme and can create non-obligate associations (Glick et al. 1999) and facilitate N2 fixation in non-leguminous plants. Azotobacter and Clostridium are classic examples of freeliving diazotrophic bacterium. Other important examples of free-living nitrogenfixing microbes include cyanobacteria/blue-green algae (BGA), including genera such as Anabaena, Aulosira, Nostoc, and Calothrix, symbiotic cyanobacteria (Azolla-Anabaena system), and the association between Azospirillum and plant often referred to as “associative symbiosis.” It refers to the loose association between microsymbionts and their hosts (Gosal and Kaur 2017). 1.2.1.2 Mineral Solubilizers Mineral viz. Phosphorus (P), Potassium (K), Zinc (Zn), and Iron (Fe) solubilization in the soil can occur by several mechanisms including the production of organic acids, a decrease in pH, chelation, acidolysis, production of enzymes, and EPS (Devi et al. 2022). Microbes aid in mineral solubilization mostly through the production of organic acids (Hocking 2001). These acids bind to cations like Ca2+ and produce 2H+, which lowers the pH of the solution and solubilizes the minerals.

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Pseudomonas, Bacillus, Rhizobium, Burkholderia, Agrobacterium, Micrococcus, Flavobacterium, and Erwinia are the most reported mineral-solubilizing genera found in soil (Gosal and Kaur 2017).

1.2.1.3 Phytohormone Producers Microbial phytohormones can fulfill the plant’s hormonal needs while sparing metabolic energy for growth and development. There are several types of plant hormones viz. indole acetic acid (IAA), cytokinin (CK), abscisic acid (ABA), ethylene (ET), and gibberellic acid (GA), produced by microbes, which are not only vital for the plant in normal circumstances but also serve efficiently in stress alleviation (Kudoyarova et al. 2019; Egamberdieva et al. 2017). Some major phytohormone-producing microbial genera are Pseudomonas, Bacillus, Azospirillum, and Paenibacillus (Kumar et al. 2022b).

1.2.2

Microbial Inoculants as Biocontrol Agents

Microbial biocontrol agents (BCAs) protect plants from pathogen infections through a variety of mechanisms such as the secretion of metabolites with antimicrobial activity (lipopeptides, antibiotics, biosurfactants, bacteriocins), lytic enzymes, volatile compounds, siderophore production, inducing host systemic response (Köhl et al. 2019) (Fig. 1.2). Moreover, BCA may obstruct the pathogens’ quorum sensing (QS) system by blocking the synthesis of infection-initiating signal molecules or promoting their enzymatic degradation (Kalia et al. 2019). BCA can indirectly protect plants by triggering the defense mechanism (such as the IRS-induced systematic response) that helps the plant to survive (Köhl et al. 2019) and improves host defensive mechanisms leading to systemic resistance. This causes the host to mount a defensive mechanism by assembling a series of structural barriers and releasing a collection of biochemical and molecular defense responses, exerting resistance to a broad spectrum of infections. Some reported potential microbial genera as biocontrol agents are Azospirillum, Trichoderma, Bacillus, Enterobacter, Pseudomonas, and Streptomyces (Kumar et al. 2022b).

1.2.3

Microbial Inoculants as Bioremediation Agents

A variety of microorganisms are being employed to detoxify the environment. Through the action of specialized enzymes and gene systems, some microbes can biodegrade both organic (polycyclic aromatic hydrocarbons, dyes, and pesticides) and inorganic (such as heavy metal/metalloid samples) pollutants. Industrial effluents containing azo-dyes, polycyclic aromatic hydrocarbons (PAH), and pesticides can be decontaminated and decolorized by microbes through biosorption, enzymatic degradation, or both processes (Wu et al. 2012). Heavy metal pollutants are eliminated by microbes through a variety of mechanisms, including bioaccumulation, biosorption, complexation, precipitation, biotransformation,

Fig. 1.2 Roles and major mechanisms adopted by microbial inoculants under climate change

1 Microbial Inoculants in the Climate Change Scenario: An Overview 5

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phytoremediation, and by enzymatic transformation (Ojuederie and Babalola 2017; Xu and Zhou 2016) (Fig. 1.2). Microbial genera such as Pseudomonas (Dary et al. 2010), Psychrobacter, Ochrobactrum, Lysinibacillus, Bacillus (Emenike et al. 2016), and Paecilomyces (Xu et al. 2017) are reported for their efficient bioremediation ability.

1.3

Major Stresses Affecting Crop Production, as a Result of Climate Change

The climate is one of the primary elicitors of the different types of stresses, which can reduce agricultural output. Changing climate conditions have a direct consequence on crop productivity in a variety of ways, including variations in global CO2 or Ozone levels, alterations in annual rainfall, temperature patterns, and pathogen life cycles. Stresses are categorized into two types based on their interactions with plants and environmental factors: abiotic stress and biotic stress. High salinity, drought, flooding, extreme temperatures, radiation, and heavy metals are examples of abiotic stresses, whereas biotic stresses include a range of pest and diseasecausing organisms, such as bacteria, viruses, fungi, and insect, etc.

1.3.1

Abiotic Stress

1.3.1.1 Salinity Stress Recent estimates suggest that roughly 1060 to 1128 Mha of land is impacted by salt stress worldwide, compared to Sparks’s (2003) estimate of 932.2 Mha (Eswar et al. 2021; Kumar and Sharma 2020). Plants flourishing in soils affected by salinity are subjected to osmotic stress, in addition to nutrient stress (Ashrafi et al. 2014). Plants undergo osmotic stress when the soil’s osmotic potential is diminished by excessive aggregation of Na+ and Cl- ions. The toxicity of nutrients like Na, B, and Cl is one problem salinity-stressed plants confront, while deficiencies of nutrients like N, P, K, and Fe are another. Higher intensities of Cl- and Na+ ions, as well as water intake, reduce N uptake in salty soils because Na+ ions bind with NH4+ and Cl- ions bind with NO3-. Likewise, when (PO4)3- ion precipitates with Ca2+ ions to create calcium phosphate, the plant’s ability to take in P is diminished (Bano and Fatima 2009; Shrivastava and Kumar 2015). In contrast, elevated Na+ ion concentrations drastically slow down the absorption of K+ ions (Raddatz et al. 2020). The production of free oxygen radicals, which advances to lipid peroxidation, enzyme or protein inactivation, etc., is another effect of high salinity (Ahmad et al. 2010). 1.3.1.2 Drought Stress Drought stress arises when the availability of water in the soil decreases. Drought affects roughly half of the arable area, affecting the majority of crops and their yields. According to Goswami and Deka (2020), the drought distressed area has increased twofold between 1970 and 2000, and it is predicted to affect half of the

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world’s agricultural lands by 2050. All features of a plant’s metabolism and physiology are impacted by drought, including membrane integrity, pigment content, photosynthesis, growth, and yield. The principal components of photosynthesis that are disrupted by drought include the stomatal regulation and ETC of thylakoid, thereby modulating lipid profiles of chloroplast, and photosynthetic pigments and protein levels (Anjum et al. 2011). According to Kaur and Asthir (2017), RuBisCO activity also drops dramatically in extreme drought conditions. Drought conditions pose significant challenges to seed germination and stand establishment.

1.3.1.3 Temperature Stress High-temperature stress can alter the physical, physiological, and biochemical processes that occur within a plant throughout its life cycle. High temperatures reduce the germination rate and standing ability of seedlings because of altered enzyme activity in starch breakdown and also reduce phytohormone (ABA and GA) production (Begcy et al. 2018). Because of the decline in the activity of RuBisCO, loss of grana, reduced functionality of electron donor and acceptor sites of photosystem II, and disorganization of thylakoid, a profound effect on photosynthesis is observed (Hassan et al. 2020). Furthermore, high temperatures inhibit photosynthesis by altering the intercellular CO2 levels, which in turn closes stomata. The lipid peroxidation reactions occurring in the chloroplasts also damage the chlorophyll pigments altering photosynthesis rates (Hassan et al. 2020). High temperature inhibits plant development in several other ways, including altering the plant’s relative water content and reducing nutrient intake through increased evaporation and decreased root amplification (Giri et al. 2017). Plants in temperate and alpine zones are more vulnerable to the harmful impacts of low-temperature. Reduced plant development, leaf yellowing, and the death of transplanted seedlings are all the result of low temperatures (Arun-Chinnappa et al. 2017). Low temperatures also induce pollen sterility by breaking down starch granules, stopping germination, and shortening the pollen tube (Shinada et al. 2013). Low temperatures not only harm several biological components but also hinder photosynthesis by disrupting the normal arrangement of chlorophyll and thylakoids (Zhao et al. 2020). Cellular dehydration is generated by freezing stress in leaf cells due to water crystallization in the apoplastic region, which facilitates stomatal closing and alters cellular functions (Arun-Chinnappa et al. 2017). 1.3.1.4 Flooding Stress Anoxia is caused by flooding or submersion, which affects around 15 Mha rain-fed area of Asia and around 13% of the world’s agricultural land (Meena et al. 2017). Hypoxic situations reduce the endogenous IAA, GA, and CK concentration, resulting in increased ABA and ET concentration in shoots, which promotes premature senescence (Glick 2014) and initiates the formation of O2 free radicals, which causes irreparable damage to the plant (Meena et al. 2017). Conversely, the enzyme ACC synthase, which facilitates the translation of S-adenosyl-L-methionine (SAM) to 1-aminocyclopropane-1-carboxylate (ACC), is upregulated in roots. However, hypoxia reduces the newly synthesized ACC from being oxidized and their transport

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to the shoot, which subsequently causes necrosis, chlorosis, and decreased plant efficiency resulting in reduced output (Ali and Kim 2018; Glick et al. 2007; Paul et al. 2016).

1.3.1.5 Heavy Metals Stress Excessive accumulation of heavy metals inside the plant cell impairs plant growth by altering the enzyme activity in the cellular matrix and generating oxidative stress or through modification of plant–microbe cross-talk and reduction in the uptake of essential elements from the rhizosphere (Dotaniya and Saha 2016). Heavy metals, such as arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg), are extremely poisonous to plants even at low concentrations and have no positive effects on plant growth (Chibuike and Obiora 2014). Signs of Cd toxicity include stunting, chlorosis, and leaf rolls. Cd and As cause oxygen-free radical generation and reduce the plant’s natural antioxidant defenses. Because heavy metals are most concentrated in the roots, it is the roots that show the most evidence of phytotoxicity, including reddishbrown discoloration of the leaves, browning of the roots, and chlorosis of the leaves. On the other hand, Hg disrupts plant metabolism and causes a variety of other physiological problems. Metabolites like ascorbic acid are produced at higher rates, and they are harmful to plants and can disrupt chlorophyll and anthocyanin synthesis (Bharti and Sharma 2022).

1.3.2

Biotic Stress

Biotic stress in plants is produced by living things, especially macro–meso–microfauna, microflora, and weeds. Roughly ~20–40% of yearly worldwide crop yield is lost as a consequence of disease infection, herbivory, and weeds. Pathogen infection alters the physiochemical functions such as water absorption and turgidity of cells. Pathogen infection harms photosynthesis because it reduces stomatal conductance and causes a reduction in the leaf area index, both of which change the role of the photosynthetic pigments (Rho et al. 2022; Tseliou et al. 2021). In the case of biotic stress, reactive oxygen species (ROS) are typically associated with disease resistance responses in plants that have been infected by a pathogen; nevertheless, necrotrophs increase ROS formation for their benefit by secreting toxins and hydrolytic enzymes. The ROS produced by necrotizing organisms (necrotrophs) cause membrane damage, allowing pathogens to get access to the cytoplasm and exploit it for their growth and expansion (Rossi et al. 2017).

1.4

Desirable Properties of Microbial Inoculants to Combat Climate Change

As a result of climate changes (temperature and precipitation patterns), plant physiology and its interactions with the environment are disrupted, leading to reduced crop yields and increased disease infestation. Those microbes that are a part of the

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plant microbiome and help the plant flourish and mature are called plant growth-promoting microbes and play a significant role in crop production. Several traits are desirable for a microbial inoculant to survive and confront changing climates such as efficient nutrient utilization and recycling of energy, production of plant growth regulators, the ability of abiotic stress management, and biocontrol of phytopathogens and biotic elicitor molecules.

1.4.1

Efficient Nutrient Utilization and Recycling of Energy

By breaking down both organic and inorganic materials and biogeochemical cycling organic leftovers in the earth’s crust, microorganisms play a significant role in nutrient management. Microbial inoculants associated with plant roots use root exudates for their growth and increase the availability of nutrients like N, P, K, Zn, and other macro- and microelements in return. This assures the delivery and turnover of nutrients required for soil and crop health (Kumar et al. 2022b). Estimates for the amount of atmospheric nitrogen fixed symbiotically by various legume crops range from about 200 to 300 kg of Nha-1 per year, making them a potentially sustainable source of nitrogen for agricultural use (Kebede 2021; Peoples et al. 1995; Zahran 1999). The nitrogen-fixing efficiency of free-living nitrogen fixers is around 20 kg N/ha/year. Higher crop yields have been observed when using Azospirillum and Azotobacter on cauliflower, carrot, cotton, maize, wheat, potato, rice, sorghum, sugarcane, and tomato (Raffi and Charyulu 2021; Wani et al. 2016). Rhizobium and Frankia fix nitrogen through symbiotic association by forming root nodules and free-living nitrogen-fixing bacteria viz. Azospirillum, Azotobacter, Clostridium, Rhodospirillum, Chlorobium sp., and cyanobacteria (Anabaena, Nostoc, Aphanocapsa, Chroococcus, Oscillatoria, and Phormidium) perform non-symbiotic N2 fixation (Daniel et al. 2022). Minerals such as P, K, Zn, and Fe are essential for plant growth and are present in the soil in an insoluble complex, and microbial inoculants can transform these insoluble minerals into forms that plants can use. Potassium-solubilizing microbial (KSM) inoculants have been utilized in places with low potassium levels in the soil and have been shown to benefit the cultivation of various crops around the world such as in Korea and China where potassium levels are lower (Bachani et al. 2016; Fu-chun et al. 2006; Olaniyan et al. 2022). Several microorganisms produce siderophores, which are high-affinity ferric ion-specific chelators used for iron sequestration (Kramer et al. 2020; Wang et al. 2022). Siderophores not only meet the plant’s iron requirements, but they also limit the infectious microbes in the rhizosphere (Gu et al. 2020).

1.4.2

Production of Plant Growth Regulators

Bioinoculants are reported to deliver several phytohormones that are significant growth regulators and have a paramount impact on a plant’s physiology and metabolism. The phytohormones generated by beneficial microorganisms in the

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rhizosphere help plants cope with these stresses. They are crucial for triggering plants’ defensive systems in response to stresses (Egamberdieva et al. 2017; El Sabagh et al. 2022; Shahzad et al. 2016). Auxins moderate and promote tolerance to salt, drought, and heavy metals, in addition to their crucial function in a wide range of plant developmental processes (Amara et al. 2015). Nevertheless, bioinoculants that can produce phytohormones can reduce heavy metal toxicity and increase root biomass (Egamberdieva et al. 2017; Liu et al. 2022). High auxin concentrations may hinder quick root propagation into soils, which is important during water scarcity (Loper and Schroth 1986; Patten and Glick 2002; Zamioudis et al. 2013). Rhizospheric microbes have been reported to produce the phytohormone ACC deaminase, which plays a pivotal role in protecting plants from the adverse effects of climate change (Husain et al. 2020; Iqbal et al. 2017). The synthesis of cytokinins by microorganisms is a crucial factor in plants for promoting cell division and shoot elongation under stress (Asif et al. 2022). Agronomically advantageous plant–microbe interactions that occur in response to drought stress are facilitated by the sensitivity of plants to microbial cytokinins. ABA protects plants from excessive water loss during drought by promoting the production of dehydrins (Hara 2010; Nakashima et al. 2014; Shakirova et al. 2016). Rhizobacteria with ABA-producing ability utilized as bioinoculants can modify ABA-mediated processes in plants and regulate the expression of ABA-responsive genes, imparting drought resistance. On the other hand, bioinoculants can also alleviate high ABA accumulation in the soil during droughts by metabolizing ABA (Belimov et al. 2014). Furthermore, microbial ABA help plants overcome the effects of salinity by synthesizing suitable solutes such as proline, sucrose, and K+ ions (Kumar and Sharma 2020). Bacillus sp., Pseudomonas sp., Azospirillum lipoferum, and Gluconacetobacter diazotrophicus have been reported to produce ABA, which has resulted in their favorable effects on drought stress mitigation (Cohen et al. 2015; Salomon et al. 2014; Shakirova et al. 2016; SkZ et al. 2018; Vargas et al. 2014). Ethylene is an epicentral phytohormone engaged in plant survival under diverse biotic and abiotic stimulants, and it affects physiological and developmental processes significantly, emphasizing a vital role in plant adaptation to climate change. Higher ethylene concentration in plants prepares them to withstand stress, but it harms plant development and production. In saline conditions, ethylene is responsible for osmotic equilibrium, stomatal function, and water consumption efficiency. Nonetheless, it upregulates and expedites the expression of hypoxia response genes and ethylene response factors when plants sense hypoxia and heat stress, respectively (Berkowitz et al. 2021; Eichmann et al. 2021; Hartman et al. 2021; Loreti and Perata 2020; Shekhawat et al. 2023).

1.4.3

Abiotic Stress Management

Microbial bioinoculants secrete exopolysaccharides that interact with sodium ions and modulate their availability, thus enhancing water potential and nutrient intake and ameliorating saline stress. Under stress impact, bioinoculants can activate

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several genes responsible to produce antioxidants, heat shock proteins, and various secondary metabolites (Al Khateeb et al. 2020; Chen et al. 2022; Rahman et al. 2022). Under drought, microbial bioinoculants secrete osmolytes, which help in maintaining the turgor pressure in sync with plants’ osmolytes (Ma et al. 2020). Several indirect interactions between microbial secondary metabolites viz. EPS, siderophores, growth hormones, and heavy metals contribute to the detoxification process via biosorption or bioaccumulation (Mitra et al. 2018; Pramanik et al. 2017; Zahoor et al. 2017) (Fig. 1.2). Mung bean and wheat treated with Bacillus sp. and Streptomyces strains showed improved growth owing to enhanced activities of antioxidant enzymes (Akbari et al. 2020; Islam et al. 2016). Similarly, Enterobacter sp. with biochar reduced Cd bioavailability in Pea while increasing growth (Naveed et al. 2020). Several excellent reviews have discussed Klebsiella sp., Bacillus sp., and Mucor sp. inoculants that have been observed to increase plant development by lowering heavy metal stress in soil (Khanna et al. 2022; Kumar et al. 2022a; Tiwari and Lata 2018).

1.4.4

Biocontrol of Phytopathogens

Beneficial microbes inhibit the growth of phytopathogens in a variety of ways, including competing for nutrients and space, reducing the accessibility of nutrients to pathogens, synthesis of hydrolytic enzymes (chitinase, cellulase, proteases, glucanase), and secretion of secondary metabolites, such as antimicrobial (antibacterial, antifungal, and antinematode) including volatile organic compounds. The microbial flora of disease-suppressive soils can exhibit a variety of broadspectrum antibiotics. Fungal inoculants such as Trichoderma sp., on the other hand, can predate and parasitize the plant pathogenic fungi (Bhattacharyya et al. 2016; El-Saadony et al. 2022). Elicitors, on the other hand, are chemical moieties that are generally found in plant defense systems and can be promoted by beneficial microflora, giving systemic resistance that can be acquired or induced in nature. Plant defense mechanisms are activated by chemicals such as salicylic acid, methyl jasmonate, ethylene, and nitric oxide (NO) (El-Saadony et al. 2022). Induced systemic resistance-related genes are induced by jasmonic acid and ethylene, whereas salicylic acid can promote the translation of pathogenesis-related (PR) genes and impart systemic acquired resistance (SAR) in plants (Gao et al. 2015; Mathys et al. 2012).

1.5

Major Mechanisms Adopted by Microbes to Alleviate Global Climate Change-Induced Stresses

Microorganisms can support plant growth through direct or indirect strategies, with certain processes acting in both directions. The direct strategy involves microorganisms making it easier for plants to mobilize or sequester nutrients, whereas indirect strategies require the regulation of phytohormones or the

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production of chemical compounds. Several amino acids, sugars, isoprenoid compounds, lipids, and polymeric compounds of high molecular weight along with certain vitamins are major components of root exudates, thus making them an abundant supply of resources for the microbial inhabitants in the rhizospheric niche (Bais et al. 2006; Devi et al. 2022; Yarzábal and Chica 2019), thereby providing a foundation for implementing direct strategies for plant growth promotion. Tryptophan and methionine are amino acids that serve as precursors for IAA and ethylene, respectively. Similarly, gibberellin and strigolactone stimulate root nodule formation in legume rhizospheres (Ryu et al. 2012; Shekhawat et al. 2023). Beneficial bacteria and fungi inhabit the plant’s rhizosphere and feed on these organic chemicals to proliferate and exert their beneficial effects as discussed above. Mineral solubilization by microbial inoculants is mostly accomplished through pH decrease via the formation of organic acids and secretion of extracellular polysaccharides. However, various alternative methods have been described, including capsule absorption, chelation, acidolysis (mineral-solubilizing bacteria or fungi secrete protons that acidify the milieu around them, causing dissolution of inorganic minerals), and enzymolysis (e.g., aminotransferase, arylsulfatase, carboxylesterase, dehydrogenases, dextransucrase, inulinase, dextransucrase, inulase, phytase, phosphatase, and xylanase) (Devi et al. 2022; Kageyama et al. 2011; Kour et al. 2021; Olanrewaju et al. 2017). Potent bioinoculants can mobilize micronutrients through chelation or sequestration by siderophore synthesis, allowing them to be absorbed by the plants or enhancing the bioavailability of these nutrients in the soil (Olanrewaju et al. 2017; Orozco-Mosqueda et al. 2021; Rojas-Sánchez et al. 2022). Furthermore, ethylene levels in plants can be reduced by the activity of ACC deaminase, which is produced by a variety of bioinoculants. The enzyme converts ACC to alpha-ketobutyrate and ammonia, which is used by the plant and provide resistance toward the deleterious outcomes of abiotic stresses (Fadiji et al. 2022; Kumar et al. 2022a; Orozco-Mosqueda et al. 2021; Pandey and Gupta 2020). Antimicrobial chemical synthesis is a widespread and well-studied indirect method of promotion of growth and development. Pathogens can be destroyed or their population can be reduced by volatile organic molecules such as HCN produced by many bacterial and fungal inoculants. Another indirect process is the synthesis of lytic enzymes, which are linked to the microorganism’s ability to parasitize and eliminate the pathogen. Plants can develop resistance to pathogen infection through a signaling pathway known as induced stress response (ISR), which can be induced by a variety of factors, such as stress hormones. Pathogen-associated molecular patterns (PAMPs) are molecules conceded by plant cells and are essential for the excitation of ISR (Adeleke et al. 2022; Glick 2012; Kumar et al. 2022b; Mukherjee et al. 2022; Olanrewaju et al. 2017; Olowe et al. 2022; Orozco-Mosqueda et al. 2021; Shah et al. 2021).

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Future of Microbial Inoculants in Sustaining Crop Production

The world biofertilizer market is currently growing at a very high rate (compound annual growth rate of 12.8%), and it is expected to grow from USD 1.2 billion markets in 2020 to USD 2.70 billion markets by 2027. Although microbial inoculants cannot completely replace agricultural chemicals, which had a 208.6 billion USD market in 2020, and with a high growth rate (compound annual growth rate of 3.4%), it is expected to become USD 246.1 billion market by 2025 (Zobir et al. 2021). As compared to the agrochemical market, the biofertilizer market is growing faster and at a very high rate. Isolation of effective and stress-tolerant inoculants with increased shelf life, developing conglomerates of small companies selling microbial inoculants, incentivization of microbial inoculant use, and a simple registration process is required to further increase the market size of biofertilizers (Alori and Babalola 2018; O'Callaghan et al. 2022). The excessive use of agrochemicals for different purposes has lead to several environmental problems (Nikita and Puneet Singh 2020), and many pathogens are also reported to have become resistant to chemicals that are used for their control (Hawkins et al. 2019). Both these problems can be minimized by using microbial inoculants as these are environment friendly and use specific mechanisms to control pathogens. Therefore, there is scope for using microbial inoculants for sustainable agricultural practices. Changing environmental conditions are also affecting crops adversely. Different stresses like salinity, temperature, drought, flooding, alkaline/acidic, and biotic stresses lead to unimaginable crop productivity loss (Devi et al. 2022). Microbial inoculants with multi-stress-tolerant ability are currently being developed and have shown promising results under stress conditions, but their commercialization on a large scale has not been done suitably, which makes their availability difficult (Ali et al. 2022; Backer et al. 2018). The multi-stress-tolerant ability of microbial inoculants can be used to tackle the stresses faced in modern agriculture, as the environment is continuously changing and global warming is a major concern nowadays (Kavadia et al. 2020). Recently, the focus is increasing on organic farming, which highlights the significant role microbial inoculants can play, with a huge scope. Various governments are encouraging farmers to produce organic crops and promote their products, through different subsidy programs (Azam and Shaheen 2019; Qiao et al. 2019). In organic farming, microbial inoculants can be used as mineral solubilizers, nitrogen fixers, biocontrol agents, abiotic stress alleviators, and for various other plant growth-promoting activities (Alori and Babalola 2018; Devi et al. 2022). In 2021, organic farming was practiced in 72.3 million ha worldwide and it was worth 113 billion USD in 2019 (Willer et al. 2021). Integrated use of microbial inoculants, in which the use of chemicals is minimized, may be the best way to increase crop production shortly in a sustainable manner.

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Conclusions

Agroecosystem functions and services are affected by climate change, and microbial inoculation can be an importrant way to alleviate and mitigate the negative effects. This involves both the direct effects of microbial inoculants as they possess specialized functions and the cascading effects facilitated through the plant and/or microbial or at the ecosystem level. Designing new strategies to combat climate change may be made easier by understanding these cascading impacts, although still a challenge to determine how microbial inoculation-induced effects alter over time and how they may extend beyond the desired uses because of variables, such as the long-lasting persistence of microbial inoculants in rhizospheric soil and its effects on the rhizospheric ecosystem or genotype–environment–microbiome interactions. So, there exists a strong focus on reliable microbial inoculants, which regulate agroecosystem functions and predominantly address the issue of climate change. Microbial inoculation is becoming indispensable for environmental sustainability and can aid in achieving food security in the coming future if the package of practices for major crops includes them as integral inputs.

References Adeleke BS, Ayilara MS, Akinola SA, Babalola OO (2022) Biocontrol mechanisms of endophytic fungi. Egypt J Biol Pest Control 32(1):46. https://doi.org/10.1186/s41938-022-00547-1 Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress [review]. Crit Rev Biotechnol 30(3):161–175. https:// doi.org/10.3109/07388550903524243 Akbari A, Gharanjik S, Koobaz P, Sadeghi A (2020) Plant growth promoting Streptomyces strains are selectively interacting with the wheat cultivars especially in saline conditions. Heliyon 6(2): e03445. https://doi.org/10.1016/j.heliyon.2020.e03445 Al Khateeb W, Muhaidat R, Alahmed S, Al Zoubi MS, Al-Batayneh KM, El-Oqlah A, Alkaraki AK et al (2020) Heat shock proteins gene expression and physiological responses in durum wheat (Triticum durum) under salt stress. Physiol Mol Biol Plants 26(8):1599–1608. https://doi.org/ 10.1007/s12298-020-00850-x Ali S, Kim W-C (2018) Plant growth promotion under water: decrease of waterlogging-induced ACC and ethylene levels by ACC deaminase-producing bacteria. Front Microbiol 9:1096. https://doi.org/10.3389/fmicb.2018.01096 Ali S, Moon Y-S, Hamayun M, Khan MA, Bibi K, Lee I-J (2022) Pragmatic role of microbial plant biostimulants in abiotic stress relief in crop plants. J Plant Interact 17(1):705–718. https://doi. org/10.1080/17429145.2022.2091801 Alori ET, Babalola OO (2018) Microbial inoculants for improving crop quality and human health in Africa [Review]. Front Microbiol 9:2213. https://doi.org/10.3389/fmicb.2018.02213 Amara U, Khalid R, Hayat R (2015) Soil bacteria and phytohormones for sustainable crop production. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agroecosystem. Springer International, Berlin, pp 87–103. https://doi.org/10.1007/978-3-319-24654-3_5 Anjum SA, Xie XY, Wang LC, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress [review]. Afr J Agric Res 6(9):2026–2032. https://doi.org/10.5897/AJAR10.027

1

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Ansari FA, Ahmad I, Pichtel J (2019) Growth stimulation and alleviation of salinity stress to wheat by the biofilm forming Bacillus pumilus strain FAB10 [article]. Appl Soil Ecol 143:45–54. https://doi.org/10.1016/j.apsoil.2019.05.023 Arora NK (2019) Impact of climate change on agriculture production and its sustainable solutions. Environ Sustain 2(2):95–96. https://doi.org/10.1007/s42398-019-00078-w Arun-Chinnappa KS, Ranawake L, Seneweera S (2017) Impacts and management of temperature and water stress in crop plants. In: Abiotic stress management for resilient agriculture. Springer, Berlin, pp 221–233. https://doi.org/10.1007/978-981-10-5744-1_9 Ashrafi E, Zahedi M, Razmjoo J (2014) Co-inoculations of arbuscular mycorrhizal fungi and rhizobia under salinity in alfalfa [article]. Soil Sci Plant Nutr 60(5):619–629. https://doi.org/ 10.1080/00380768.2014.936037 Asif R, Riffat Y, Madiha M, Ana A, Modasrah M, Abdul R, Mukhtiar A et al (2022) Phytohormones as plant growth regulators and safe protectors against biotic and abiotic stress. In: Christophe H (ed) Plant hormones. IntechOpen, London. https://doi.org/10.5772/ intechopen.102832 Azam MS, Shaheen M (2019) Decisional factors driving farmers to adopt organic farming in India: a cross-sectional study. Int J Soc Econ 46(4):562–580. https://doi.org/10.1108/IJSE-052018-0282 Bachani P, Bhattacharya S, Jain D, Patidar SK, Soundarya R, Tirkey SR, Mishra S et al (2016) Bioprospecting of halotolerant bacterial isolates for potassium recovery from K-feldspar. Chem Eng Technol 39(9):1645–1652. https://doi.org/10.1002/ceat.201500561 Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Smith DL et al (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture [Review]. Front Plant Sci 9:1473. https://doi.org/10.3389/fpls.2018.01473 Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interaction with plants and other organisms. Annu Rev Plant Biol 57(1):233–266. https://doi. org/10.1146/annurev.arplant.57.032905.105159 Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45(4):405–413. https://doi.org/10.1007/s00374-008-0344-9 Begcy K, Sandhu J, Walia H (2018) Transient heat stress during early seed development primes germination and seedling establishment in rice. Front Plant Sci 9:1768. https://doi.org/10.3389/ fpls.2018.01768 Belimov AA, Dodd IC, Safronova VI, Dumova VA, Shaposhnikov AI, Ladatko AG, Davies WJ (2014) Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiol Biochem 74:84–91. https://doi.org/10.1016/j.plaphy.2013. 10.032 Berkowitz O, Xu Y, Liew LC, Wang Y, Zhu Y, Hurgobin B, Whelan J et al (2021) RNA-seq analysis of laser microdissected Arabidopsis thaliana leaf epidermis, mesophyll and vasculature defines tissue-specific transcriptional responses to multiple stress treatments. Plant J 107(3): 938–955. https://doi.org/10.1111/tpj.15314 Bharti R, Sharma R (2022) Effect of heavy metals: an overview. Mater Today Proc 51:880–885. https://doi.org/10.1016/j.matpr.2021.06.278 Bhattacharyya PN, Goswami MP, Bhattacharyya LH (2016) Perspective of beneficial microbes in agriculture under changing climatic scenario: a review. J Phytology 8:26–41. https://doi.org/10. 19071/jp.2016.v8.3022 Chen D, Mubeen B, Hasnain A, Rizwan M, Adrees M, Naqvi SAH, Din GMU et al (2022) Role of promising secondary metabolites to confer resistance against environmental stresses in crop plants: current scenario and future perspectives [review]. Front Plant Sci 13:881032. https://doi. org/10.3389/fpls.2022.881032 Chibuike GU, Obiora SC (2014) Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci 2014:752708. https://doi.org/10.1155/2014/752708

16

S. Singh et al.

Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Piccoli PN et al (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 Daniel AI, Fadaka AO, Gokul A, Bakare OO, Aina O, Fisher S, Klein A et al (2022) Biofertilizer: the future of food security and food safety. Microorganisms 10(6):1220. https://mdpi-res.com/ d_attachment/microorganisms/microorganisms-10-01220/article_deploy/microorganisms-1001220-v2.pdf?version=1655359795 Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177(1–3):323–330. https://doi.org/10.1016/j.jhazmat.2009. 12.035 Devi R, Kaur T, Kour D, Yadav A, Yadav AN, Suman A, Saxena AK et al (2022) Minerals solubilizing and mobilizing microbiomes: a sustainable approach for managing minerals’ deficiency in agricultural soil. J Appl Microbiol 133(3):1245–1272. https://doi.org/10.1111/ jam.15627 Disi J, Simmons J, Zebelo S (2019) Plant growth-promoting rhizobacteria-induced defense against insect herbivores, pp 385–410. https://doi.org/10.1007/978-3-030-30926-8_14 Dotaniya M, Saha J (2016) Heavy metal polluted soils in India: status and countermeasures. JNKVV Res J 49:320–337 Egamberdieva D, Wirth SJ, Alqarawi AA, Abd Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness [review]. Front Microbiol 8:2104. https://doi.org/10.3389/fmicb.2017.02104 Eichmann R, Richards L, Schäfer P (2021) Hormones as go-betweens in plant microbiome assembly. Plant J 105(2):518–541. https://doi.org/10.1111/tpj.15135 El Sabagh A, Islam MS, Hossain A, Iqbal MA, Mubeen M, Waleed M, Abdelhamid MT et al (2022) Phytohormones as growth regulators during abiotic stress tolerance in plants [review]. Front Agron 4:765068. https://doi.org/10.3389/fagro.2022.765068 El-Saadony MT, Saad AM, Soliman SM, Salem HM, Ahmed AI, Mahmood M, AbuQamar SF et al (2022) Plant growth-promoting microorganisms as biocontrol agents of plant diseases: mechanisms, challenges and future perspectives. Front Plant Sci 13:923880. https://doi.org/ 10.3389/fpls.2022.923880 Emenike C, Agamuthu P, Fauziah SJEES (2016) Blending Bacillus sp, Lysinibacillus sp and Rhodococcus sp for optimal reduction of heavy metals in leachate contaminated soil. Environ Earth Sci 75(1):1–8. https://doi.org/10.1007/s12665-015-4805-9 Eswar D, Karuppusamy R, Chellamuthu S (2021) Drivers of soil salinity and their correlation with climate change. Curr Opin Environ Sustain 50:310–318. https://doi.org/10.1016/j.cosust.2020. 10.015 Fadiji AE, Babalola OO, Santoyo G, Perazzolli M (2022) The potential role of microbial biostimulants in the amelioration of climate change-associated abiotic stresses on crops [review]. Front Microbiol 12:829099. https://doi.org/10.3389/fmicb.2021.829099 Fu-chun L, Sha L, Yong-zhao Y, Liang-juan C (2006) Advances in the study of weathering products of primary silicate minerals, exemplified by mica and feldspar. Acta Petrol Mineral 5:440–448 Gao Q-M, Zhu S, Kachroo P, Kachroo A (2015) Signal regulators of systemic acquired resistance [review]. Front Plant Sci 6:228. https://doi.org/10.3389/fpls.2015.00228 Giri A, Heckathorn S, Mishra S, Krause C (2017) Heat stress decreases levels of nutrient-uptake and -assimilation proteins in tomato roots. Plants (Basel) 6(1):6. https://doi.org/10.3390/ plants6010006 Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012: 963401. https://doi.org/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. https://doi.org/10.1016/j.micres.2013.09.009

1

Microbial Inoculants in the Climate Change Scenario: An Overview

17

Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press and distributed by World Scientific Publishing, London. https://doi.org/10.1142/p130 Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminaseproducing soil bacteria. In: New perspectives and approaches in plant growth-promoting Rhizobacteria research, pp 329–339. https://doi.org/10.1007/978-1-4020-6776-1_8 Gosal S, Kaur J (2017) Microbial inoculants: a novel approach for better plant microbiome interactions. In: Probiotics in Agroecosystem, pp 269–289. https://doi.org/10.1007/978-98110-4059-7_14 Goswami M, Deka S (2020) Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: a review [review]. Pedosphere 30(1):40–61. https://doi.org/10.1016/S1002-0160(19) 60839-8 Gu S, Wei Z, Shao Z, Friman V-P, Cao K, Yang T, Jousset A et al (2020) Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol 5(8): 1002–1010. https://doi.org/10.1038/s41564-020-0719-8 Hara M (2010) The multifunctionality of dehydrins: an overview. Plant Signal Behav 5(5): 503–508. https://doi.org/10.4161/psb.11085 Hartman S, Sasidharan R, Voesenek LACJ (2021) The role of ethylene in metabolic acclimations to low oxygen. New Phytol 229(1):64–70. https://doi.org/10.1111/nph.16378 Harun-Or-Rashid M, Chung YR (2017) Induction of systemic resistance against insect herbivores in plants by beneficial soil microbes [review]. Front Plant Sci 8:1816. https://doi.org/10.3389/ fpls.2017.01816 Hassan M, Chattha M, Khan I, Chattha M, Barbanti L, Aamer M, Aslam MT et al (2020) Heat stress in cultivated plants: nature, impact, mechanisms, and mitigation strategies—a review. Plant Biosyst 155:1–56. https://doi.org/10.1080/11263504.2020.1727987 Hawkins NJ, Bass C, Dixon A, Neve P (2019) The evolutionary origins of pesticide resistances. Biol Rev 94(1):135–155. https://doi.org/10.1111/brv.12440 Hocking PJ (2001) Organic acids exuded from roots in phosphorus uptake and aluminum tolerance of plants in acid soils. Adv Agron 74:63–97. https://doi.org/10.1016/S0065-2113(01)74031-X Husain T, Fatima A, Suhel M, Singh S, Sharma A, Prasad SM, Singh VP (2020) A brief appraisal of ethylene signaling under abiotic stress in plants. Plant Signal Behav 15(9):1782051. https://doi. org/10.1080/15592324.2020.1782051 Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR (2017) Ethylene role in plant growth, development and senescence: interaction with other phytohormones [review]. Front Plant Sci 8:475. https://doi.org/10.3389/fpls.2017.00475 Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, Zhou W (2016) Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul 80(1):23–36. https://doi.org/10.1007/s10725-0150142-y Kageyama H, Tripathi K, Rai AK, Suriyan CU, Waditee-Sirisattha R, Takabe T (2011) An alkaline phosphatase/phosphodiesterase, PhoD, induced by salt stress and secreted out of the cells of Aphanothece halophytica, a halotolerant cyanobacterium. Appl Environ Microbiol 77:5178– 5183. https://doi.org/10.1128/AEM.00667-11 Kalia VC, Patel SK, Kang YC, Lee J-K (2019) Quorum sensing inhibitors as antipathogens: biotechnological applications. Biotechnol Adv 37(1):68–90 Kaur G, Asthir B (2017) Molecular responses to drought stress in plants. Biol Plant 61(2):201–209. https://doi.org/10.1007/s10535-016-0700-9 Kavadia A, Omirou M, Fasoula D, Ioannides IM (2020) The importance of microbial inoculants in a climate-changing agriculture in eastern Mediterranean region. Atmosphere 11(10):1136. https:// doi.org/10.3390/atmos11101136 Kebede E (2021) Contribution, utilization, and improvement of legumes-driven biological nitrogen fixation in agricultural systems [review]. Front Sustain Food Syst 5:767998. https://doi.org/10. 3389/fsufs.2021.767998

18

S. Singh et al.

Khanna K, Kohli SK, Kaur R, Handa N, Bakshi P, Sharma P, Bhardwaj R et al (2022) Reconnoitering the efficacy of plant growth promoting Rhizobacteria in expediting phytoremediation potential of heavy metals. J Plant Growth Regul. https://doi.org/10.1007/ s00344-022-10879-9 Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy [review]. Front Plant Sci 10:845. https://doi. org/10.3389/fpls.2019.00845 Kour D, Rana KL, Kaur T, Yadav N, Yadav AN, Kumar M, Saxena AK et al (2021) Biodiversity, current developments and potential biotechnological applications of phosphorus-solubilizing and -mobilizing microbes: a review. Pedosphere 31(1):43–75. https://doi.org/10.1016/S10020160(20)60057-1 Kramer J, Özkaya Ö, Kümmerli R (2020) Bacterial siderophores in community and host interactions. Nat Rev Microbiol 18(3):152–163. https://doi.org/10.1038/s41579-019-0284-4 Kudoyarova G, Arkhipova T, Korshunova T, Bakaeva M, Loginov O, Dodd IC (2019) Phytohormone mediation of interactions between plants and non-symbiotic growth promoting bacteria under edaphic stresses [review]. Front Plant Sci 10:1368. https://doi.org/10.3389/fpls.2019. 01368 Kumar P, Sharma PK (2020) Soil salinity and food security in India [review]. Front Sustain Food Syst 4:533781. https://doi.org/10.3389/fsufs.2020.533781 Kumar P, Singh S, Pranaw K, Kumar S, Singh B, Poria V (2022a) Bioinoculants as mitigators of multiple stresses: a ray of hope for agriculture in the darkness of climate change. Heliyon 8(11): e11269. https://doi.org/10.1016/j.heliyon.2022.e11269 Kumar S, Diksha, Sindhu SS, Kumar R (2022b) Biofertilizers: an ecofriendly technology for nutrient recycling and environmental sustainability. Curr Res Microb Sci 3:100094. https:// doi.org/10.1016/j.crmicr.2021.100094 Liu X, Le Roux X, Salles JF (2022) The legacy of microbial inoculants in agroecosystems and potential for tackling climate change challenges. iScience 25(3):103821. https://doi.org/10. 1016/j.isci.2022.103821 Loper JE, Schroth MN (1986) Influence of bacterial sources of indole-3-acetic acid on root elongation of sugar beet. Phytopathology 76:386–389. https://doi.org/10.1094/Phyto-76-386 Loreti E, Perata P (2020) The many facets of hypoxia in plants. Plan Theory 9(6):745 Ma Y, Dias MC, Freitas H (2020) Drought and salinity stress responses and microbe-induced tolerance in plants [review]. Front Plant Sci 11:591911. https://doi.org/10.3389/fpls.2020. 591911 Mathys J, De Cremer K, Timmermans P, Van Kerkhove S, Lievens B, Vanhaecke M, De Coninck B et al (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection [original research]. Front Plant Sci 3:108. https://doi.org/10.3389/fpls.2012.00108 Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Gupta VK et al (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172. https://doi.org/10.3389/fpls.2017.00172 Mitra S, Pramanik K, Ghosh PK, Soren T, Sarkar A, Dey RS, Maiti TK et al (2018) Characterization of Cd-resistant Klebsiella michiganensis MCC3089 and its potential for rice seedling growth promotion under Cd stress. Microbiol Res 210:12–25. https://doi.org/10.1016/j.micres.2018. 03.003 Mukherjee PK, Mendoza-Mendoza A, Zeilinger S, Horwitz BA (2022) Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biol Rev 39:15– 33. https://doi.org/10.1016/j.fbr.2021.11.004 Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat [review]. Front Plant Sci 5:170. https://doi.org/10.3389/fpls.2014.00170

1

Microbial Inoculants in the Climate Change Scenario: An Overview

19

Naveed M, Mustafa A, Majeed S, Naseem Z, Saeed Q, Khan A, Chen J-T et al (2020) Enhancing cadmium tolerance and pea plant health through Enterobacter sp. MN17 inoculation together with biochar and gravel sand. Plants 9(4):530. https://doi.org/10.3390/plants9040530 Nikita B, Puneet Singh C (2020) Excessive and disproportionate use of chemicals cause soil contamination and nutritional stress. In: Marcelo LL, Sonia S (eds) Soil contamination. IntechOpen, London. https://doi.org/10.5772/intechopen.94593 O'Callaghan M, Ballard RA, Wright D (2022) Soil microbial inoculants for sustainable agriculture: limitations and opportunities. Soil Use Manage 38(3):1340–1369. https://doi.org/10.1111/sum. 12811 Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14(12):1504. https://doi.org/ 10.3390/ijerph14121504 Olaniyan FT, Alori ET, Adekiya AO, Ayorinde BB, Daramola FY, Osemwegie OO, Babalola OO (2022) The use of soil microbial potassium solubilizers in potassium nutrient availability in soil and its dynamics. Ann Microbiol 72(1):45. https://doi.org/10.1186/s13213-022-01701-8 Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33(11):197. https://doi.org/10.1007/s11274-017-2364-9 Olowe OM, Nicola L, Asemoloye MD, Akanmu AO, Babalola OO (2022) Trichoderma: potential bio-resource for the management of tomato root rot diseases in Africa. Microbiol Res 257: 126978. https://doi.org/10.1016/j.micres.2022.126978 Orozco-Mosqueda MD, Flores A, Rojas-Sánchez B, Urtis-Flores CA, Morales-Cedeño LR, Valencia-Marin MF, Santoyo G et al (2021) Plant growth-promoting bacteria as bioinoculants: attributes and challenges for sustainable crop improvement. Agronomy 11(6):1167. https://doi. org/10.3390/agronomy11061167 Pandey S, Gupta S (2020) Evaluation of pseudomonas sp. for its multifarious plant growth promoting potential and its ability to alleviate biotic and abiotic stress in tomato (Solanum lycopersicum) plants. Sci Rep 10(1):20951. https://doi.org/10.1038/s41598-020-77850-0 Patten CL, Glick BR (2002) Role of pseudomonas putida Indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68(8):3795–3801. https://doi.org/10.1128/ AEM.68.8.3795-3801.2002 Paul MV, Iyer S, Amerhauser C, Lehmann M, van Dongen JT, Geigenberger P (2016) Oxygen sensing via the ethylene response transcription factor RAP2. 12 affects plant metabolism and performance under both normoxia and hypoxia. Plant Physiol 172(1):141–153. https://doi.org/ 10.1104/pp.16.00460 Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: An efficient source of nitrogen for sustainable agricultural production? In: Ladha JK, Peoples MB (eds) Management of biological nitrogen fixation for the development of more productive and sustainable agricultural systems: extended versions of papers presented at the Symposium on Biological Nitrogen Fixation for Sustainable Agriculture at the 15th Congress of Soil Science, Acapulco, Mexico, 1994. Springer, Dordrecht, pp 3–28. https://doi.org/10.1007/978-94-011-0055-7_1 Pramanik K, Mitra S, Sarkar A, Soren T, Maiti TK (2017) Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ Sci Pollut Res 24(31):24419–24437. https://doi.org/10.1007/s11356-0170033-z Qiao Y, Martin F, He X, Zhen H, Pan X (2019) The changing role of local government in organic agriculture development in Wanzai County, China. Can J Dev Stud 40(1):64–77. https://doi.org/ 10.1080/02255189.2019.1520693 Raddatz N, de los Ríos LM, Lindahl M, Quintero FJ, Pardo JM (2020) Coordinated transport of nitrate, potassium, and sodium. Front Plant Sci 11:247. https://doi.org/10.3389/fpls.2020.00247 Raffi MM, Charyulu PBBN (2021) Chapter 18—Azospirillum-biofertilizer for sustainable cereal crop production: current status. In: Viswanath B (ed) Recent developments in applied microbiology and biochemistry. Academic Press, New York, pp 193–209. https://doi.org/10.1016/ B978-0-12-821406-0.00018-7

20

S. Singh et al.

Rahman MA, Woo JH, Song Y, Lee S-H, Hasan MM, Azad MA, Lee K-W (2022) Heat shock proteins and antioxidant genes involved in heat combined with drought stress responses in perennial Rye grass. Life 12(9):1426. https://doi.org/10.3390/life12091426 Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, Xu J (2019) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants (Basel) 8(2):34. https:// doi.org/10.3390/plants8020034 Rho H, O’Shaughnessy SA, Colaizzi PD, Workneh F, Paetzold L, Rush CM (2022) Impacts of zebra chip disease and irrigation on leaf physiological traits in potato. Agric Water Manag 269: 107705. https://doi.org/10.1016/j.agwat.2022.107705 Rojas-Sánchez B, Guzmán-Guzmán P, Morales-Cedeño LR, Orozco-Mosqueda MD, SaucedoMartínez BC, Sánchez-Yáñez JM, Santoyo G et al (2022) Bioencapsulation of microbial inoculants: mechanisms, formulation types and application techniques. Appl Biosci 1(2): 198–220. https://doi.org/10.3390/applbiosci1020013 Rossi FR, Krapp AR, Bisaro F, Maiale SJ, Pieckenstain FL, Carrillo NJTPJ (2017) Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea. Plant J 92(5):761–773. https://doi.org/10.1111/tpj.13718 Ryu H, Cho H, Choi D, Hwang I (2012) Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Mol Cells 34(2):117–126. https://doi.org/10.1007/s10059-012-0131-1 Salomon MV, Bottini R, de Souza Filho GA, Cohen AC, Moreno D, Gil M, Piccoli P (2014) Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses, induce abscisic acid accumulation and synthesis of defense-related terpenes in in vitro cultured grapevine. Physiol Plant 151(4):359–374. https://doi.org/10.1111/ppl.12117 Shah A, Nazari M, Antar M, Msimbira LA, Naamala J, Lyu D, Smith DL et al (2021) PGPR in agriculture: a sustainable approach to increasing climate change resilience [review]. Front Sustain Food Syst 5:667546. https://doi.org/10.3389/fsufs.2021.667546 Shahzad R, Waqas M, Khan AL, Asaf S, Khan MA, Kang SM, Lee IJ et al (2016) Seed-borne endophytic bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol Biochem 106:236–243. https://doi.org/10.1016/j. plaphy.2016.05.006 Shakirova F, Allagulova C, Maslennikova D, Fedorova K, Yuldashev R, Lubyanova A, Avalbaev A et al (2016) Involvement of dehydrins in 24-epibrassinolide-induced protection of wheat plants against drought stress. Plant Physiol Biochem 108:539–548. https://doi.org/10.1016/j. plaphy.2016.07.013 Shekhawat K, Fröhlich K, García-Ramírez GX, Trapp MA, Hirt H (2023) Ethylene: a master regulator of plant–microbe interactions under abiotic stresses. Cell 12(1):31 Shinada H, Iwata N, Sato T, Fujino K (2013) Genetical and morphological characterization of cold tolerance at fertilization stage in rice. Breed Sci 63:197–204. https://doi.org/10.1270/jsbbs. 63.197 Shrivastava P, Kumar R (2015) Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation [review]. Saudi J Biol Sci 22(2): 123–131. https://doi.org/10.1016/j.sjbs.2014.12.001 Singh DP, Singh V, Gupta VK, Shukla R, Prabha R, Sarma BK, Patel JS (2020) Microbial inoculation in rice regulates antioxidative reactions and defense related genes to mitigate drought stress. Sci Rep 10(1):4818. https://doi.org/10.1038/s41598-020-61140-w SkZ A, Vardharajula S, Vurukonda SSKP (2018) Transcriptomic profiling of maize (Zea mays L.) seedlings in response to pseudomonas putida stain FBKV2 inoculation under drought stress. Ann Microbiol 68(6):331–349. https://doi.org/10.1007/s13213-018-1341-3 Sparks DL (2003) The chemistry of saline and sodic soils. Environ Soil Chem, 285–300. https://doi. org/10.1016/b978-012656446-4/50010-4 Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview [review]. Front Plant Sci 9:452. https://doi.org/10.3389/fpls.2018.00452 Tseliou E, Chondrogiannis C, Kalachanis D, Goudoudaki S, Manoussopoulos Y, Grammatikopoulos G (2021) Integration of biophysical photosynthetic parameters into one

1

Microbial Inoculants in the Climate Change Scenario: An Overview

21

photochemical index for early detection of tobacco mosaic virus infection in pepper plants. J Plant Physiol 267:153542. https://doi.org/10.1016/j.jplph.2021.153542 Vargas L, Santa Brígida AB, Mota Filho JP, de Carvalho TG, Rojas CA, Vaneechoutte D, Hemerly AS et al (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PloS One 9(12):e114744. https:// doi.org/10.1371/journal.pone.0114744 Wang Y, Zhang G, Huang Y, Guo M, Song J, Zhang T, Liu H et al (2022) A potential biofertilizer—Siderophilic bacteria isolated from the rhizosphere of Paris polyphylla var. yunnanensis [original research]. Front Microbiol 13:870413. https://doi.org/10.3389/fmicb. 2022.870413 Wani SA, Chand S, Wani MA, Ramzan M, Hakeem KR (2016) Azotobacter chroococcum—a potential biofertilizer in agriculture: an overview. In: Hakeem KR, Akhtar J, Sabir M (eds) Soil science: agricultural and environmental Prospectives. Springer International, Berlin, pp 333–348. https://doi.org/10.1007/978-3-319-34451-5_15 Willer H, Trávníček J, Meier C, Schlatter B (2021) The World of Organic Agriculture Statistics and Emerging Trends 2021. In: FiBL & IFOAM—Organics International (2021): The world of organic agriculture, 20th edn. Frick and Bonn. http://www.organic-world.net/yearbook/ yearbook-2021.html Xu Y, Zhou N-Y (2016) Microbial remediation of aromatics-contaminated soil. Front Environ Sci Eng 11(2):1. https://doi.org/10.1007/s11783-017-0894-x Wu Y, Li T, Yang L (2012) Mechanisms of removing pollutants from aqueous solutions by microorganisms and their aggregates: a review. Bioresour Technol 107:10–18. https://doi.org/ 10.1016/j.biortech.2011.12.088 Xu X, Xia L, Chen W, Huang Q (2017) Detoxification of hexavalent chromate by growing Paecilomyces lilacinus XLA. Environ Pollut 225:47–54. https://doi.org/10.1016/j.envpol. 2017.03.039 Yarzábal LA, Chica EJ (2019) Chapter 3—Role of Rhizobacterial secondary metabolites in crop protection against agricultural pests and diseases. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 31–53. https://doi.org/10.1016/B978-0-444-63504-4.00003-7 Zahoor M, Irshad M, Rahman H, Qasim M, Afridi SG, Qadir M, Hussain A (2017) Alleviation of heavy metal toxicity and phytostimulation of Brassica campestris L. by endophytic Mucor sp. MHR-7. Ecotoxicol Environ Saf 142:139–149. https://doi.org/10.1016/j.ecoenv.2017. 04.005 Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989., table of contents. https://doi.org/10. 1128/mmbr.63.4.968-989.1999 Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ (2013) Unraveling root developmental programs initiated by beneficial pseudomonas spp. bacteria. Plant Physiol 162(1): 304–318. https://doi.org/10.1104/pp.112.212597 Zhao Y, Han Q, Ding C, Huang Y, Liao J, Chen T, Yuan M et al (2020) Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of Rice seedlings during greening. Int J Mol Sci 21(4):1390. https://doi.org/10.3390/ijms21041390 Zobir SA, Ali A, Adzmi F, Sulaiman MR, Ahmad K (2021) A review on Nanopesticides for plant protection synthesized using the supramolecular chemistry of layered hydroxide hosts. Biology 10(11):1077. https://doi.org/10.3390/biology10111077

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Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in Mitigating Climate Change Kulandaivelu Velmourougane and Radha Prasanna

Abstract

Global warming and its effect on soil health are a potential threat to global agriculture with regard to providing ecosystem services to the ever-growing population. Climate change-induced soil degradation and subsequent crop loss lead to unfavorable effects on food security and economic issues, besides resulting in competition for available land resources. Though research efforts toward protecting soil health through several integrated approaches such as conservation agriculture, organic farming, integrated nutrient, water, and pest and disease management are in place, the targeted yield for the future population may not be achieved. The world still largely depends on chemical agri-inputs to achieve food security targets, which in the long run deteriorate the soil health. Recent developments in agriculture and molecular technology have resulted in innovative technologies, including breeding of climate-resilient crops or development of stress-tolerant crops using genetic modifications; such technologies take a long time to reach the farmers due to environmental policies and consumer health consciousness. Hence, attention needs to also focus on the use of bioinoculants or microbial technologies to stabilize soil health and subsequent crop productivity. The literature survey illustrates the promise of several microorganisms, which help mitigate climate change-induced harmful effects on soil and crop plants. In this review, we briefly address the prospective use of bioinoculants in alleviating the climate change-induced stress in soil and crop plants. K. Velmourougane (✉) ICAR-Central Institute for Cotton Research, Nagpur, Maharashtra, India e-mail: [email protected] R. Prasanna Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_2

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K. Velmourougane and R. Prasanna

Keywords

Climate change mitigation · Climate smart agriculture · Soil health indicators · Microbial technologies · Biofilms · Crop productivity

2.1

Introduction

The global population is predicted to hit 8.5, 9.7, and 11.2 billion by 2030, 2050, and 2100, respectively (UN 2015). However, the availability of cultivable land is diminishing considerably due to developmental activities, which render greater pressure on agriculture and global food security. Though agricultural innovations in nutrient management, crop production, and crop protection contribute significantly to higher crop productivity, chemical-free agriculture is still a challenge to attaining sustainable development with reference to managing environmental pollution and consumer health (Glare et al. 2012). This situation has forced society to look for safer biological alternatives to supplement chemical inputs in agriculture (Berg 2009; Prasad et al. 2015). Among several options, the utility of microorganisms and microbial technologies serves as a favorite savior for enhancing soil and agricultural production eventually (Hutchins et al. 2019; Fiodor et al. 2021; Kumar et al. 2022). In this chapter, we briefly discuss climate change, soil health indicators, climate change effects on soil health, and the important role of microorganisms and microbial technologies in the path toward climate change mitigation through environmentally safe options.

2.2

Climate Change, Soil Health, and Agriculture

Climate change denotes any alteration in climate over time due to natural variability or anthropogenic activity (IPCC 2007). From the agricultural perspective, “climate change and climate variability” are the primary risks faced by the farmers, which have direct effects on soil health and, consequently, crop productivity (Fig. 2.1). Climate change refers to long-term alterations in the climate attributes (IPCC 2012), while short-term changes in weather variables (precipitation, temperature, and other climatic factors) are referred to as climate variability (IPCC 2012; Thornton et al. 2014). As per the climate records, 125% increment in the global temperature since 2000 has been recorded (GISTEMP Team 2018). Though anthropogenic activities mainly contribute to global climate warming through the release of greenhouse gases (GHGs) including carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O), and other chemicals such as sulfur dioxide (SO2), hydrofluorocarbons (HFCs), perfluorocarbons (PFCs), and sulfur hexafluoride (SF6) are also major contributors to global warming (Yue and Gao 2018; Wu and Mu 2019). The rise in GHGs is reasoned to be the leading factor causing climate change, globally (IPCC 2013, 2014).

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Fig. 2.1 Climate change impacts on soil and plant productivity

Soils are directly linked to aberrations in climatic change, as they act as both a source and a sink for GHG emissions (Ghee et al. 2013; Fang et al. 2017; Singh et al. 2017; Bhattacharyya et al. 2019). Climate change evoked changes in soil properties demand site-specific soil use management in terms of assisted irrigation and chemical inputs, which upon irrational use leads to further degradation of soils and their biological properties (Arneth et al. 2019; Tabari 2020) affecting global crop productivity (Sandalio et al. 2018; Ortiz-Bobea et al. 2021). Increased use of chemical inputs in agriculture to meet the food demand in terms of chemical fertilizers, plant protection chemicals, and growth hormones find a way in the soil ecosystems rapidly under climate change situation through higher precipitation causing soil and water pollution, affecting agricultural productivity (Arora 2019; Hutchins et al. 2019); though prediction of global warming using first-generation climate models was made before five decades (Hausfather et al. 2020), the role of anthropogenic activities on the acceleration of climate change was accepted much later (Cook et al. 2013). Sustainable agriculture, ecosystem restoration, and enhanced silicate weathering were recognized as the possible areas for climate change mitigation as per the recent global report (IPCC 2022). An interactive approach to integrate and implement these identified areas in a framework of “Enhanced Natural Climate Solutions” may enhance carbon capture as a means to alleviate climate change (Amelung et al. 2020; Bomfim et al. 2022; Giebink et al. 2022; Silva 2022; Silva et al. 2022; Zhang et al. 2022).

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Soil Health Indicators and Its Assessment Methods

Soils are the principal constituents of the terrestrial ecosystems upon which our existence and well-being rely (Steffan et al. 2018; Ye et al. 2020). Hence, the protection of soil in terms of its functions, fertility, and degradation is essential for sustainable agriculture to feed the rising population (Bindraban et al. 2012; Bhattacharyya et al. 2013). The adoption of inappropriate and defective soil management practices has effects on soil health in terms of compaction, soil erosion, groundwater pollution, nutrient deficiencies, loss of soil biodiversity, etc., which affect agricultural productivity (Lal 2000; DeLong et al. 2015; Al-Kaisi et al. 2017). Under changing climate conditions, these effects on soils will be further accelerated and affect soil, plant, and human health (Cassman et al. 2010; Lal 2013). Though agricultural experimentation mainly centered on enhancing soil fertility and crop productivity worldwide, soil fertility deterioration and its consequences on biodiversity, ecosystem functions, and food security have been realized only recently (Keesstra et al. 2016; Cimpoiasu et al. 2021; Evans et al. 2022). Under the climate change era, soils have become a more vulnerable natural resource, worldwide (Titeux et al. 2016), due to rising temperature and evaporation rates leading to extended drought and moisture deficits (Kasei 2010; Hijioka et al. 2014). Around 25–40 billion tons of fertile soil is estimated to be lost globally each year (FAO and ITPS 2015). Therefore, soil health and its protection have become a vital societal responsibility for future food security and environmental health (Singh et al. 2011; Mehra et al. 2018). Considering the importance of soil health, FAO proclaimed 2015 as the “International Year of Soils,” to increase worldwide consciousness on the significance of soil health in human welfare. Food quality and human health are also linked to soil and its composition (Bruulsema 2015). The phrases—“soil fertility,” “soil quality,” and “soil health”—are often used synonymously (Karlen et al. 2001; Brevik 2018; Jian et al. 2020; Lehmann et al. 2020; Powlson 2020). However, soil quality primarily relates to the “suitability of a specific kind of soil to function within a natural or man-made ecosystem,” which may include the sustenance of plant, animal, and human health (Arshad et al. 1996; Karlen et al. 1997, 2003), while “soil health refers to soil as a non-renewable and dynamic living resource, with its capacity to function within a natural or artificial ecosystem” (Doran et al. 1999; Doran and Zeiss 2000). The term soil quality mostly describes soil physicochemical attributes, while soil health includes soil quality plus its biological elements, and soil health is regarded as comprehensive, as it encompasses whole soil management, which influences agricultural sustainability and environmental quality (Doran et al. 1999). Recently, Harris et al. (2022) proposed a new theory for soil health assessment, where they proposed a whole system approach, which embraces interrelated signs of life, function, complexity, and emergence in ecological succession. Soil quality cannot be measured directly (Stewart 1992; Sojka and Upchurch 1999), still there remain questions about how to measure soil health (Wood and Litterick 2017; Baveye 2021). Addiscot (2010a, b) suggested considering entropy production in soil systems as soil health indicators. Since soil health cannot be

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Table 2.1 Soil indices/indicators used in soil health assessments Physical indicators Soil texture/structure Bulk density

Chemical indicators pH Electrical conductivity

Biological indicators Soil organic carbon Microbial biomass (C, N, P, S) Soil respiration

Aggregate stability Porosity Soil compaction Soil crusting

Major, secondary, and minor nutrients Carbonate content Base saturation Leachable salts

Stoniness Hydraulic conductivity

Cation exchange capacity Exchangeable Na/Mg%

Available water capacity Topsoil depth

Toxic elements

Potentially mineralizable N Soil enzymes Microbial population/ diversity Mycorrhiza and glomalin Macro-, meso, and microfauna FDA

Color

Microbial quotients

quantified innately, their properties can be used as an indicator to correlate their functions in an environment for societal benefits (Janzen et al. 2021). Consequently, some soil parameters, which are related to basic soil functions, were proposed as minimum datasets to act as indicators or indices to quantify soil quality (Andrews et al. 2004; Gregorich et al. 1994). Soil quality indicators act as a decision tool for managing soil (Bhattacharyya et al. 2014a, b). Sensitivity, ease in measurement, verifiable, repeatability, and robustness in detecting soil management and environmental perturbation are some criteria chosen for good soil quality indicators (Carter et al. 1997; Velmourougane and Blaise 2017). Recently, apart from the conventional soil health measurements, soil metagenomics, soil metabolomics, and bioinformatics have enhanced our ability to assess soil health comprehensively (Neal et al. 2020; Powlson 2020; Evans et al. 2022). Some of the most widely used soil indices in soil health evaluation are presented in Table 2.1. Physical soil quality indicators primarily provide information on water and air movement in soils, which influence soil chemical and biological attributes and regulate plant growth under given climatic conditions (Allen et al. 2011). Some major physical soil quality indicators include soil structure and texture, porosity, compaction (Blaise et al. 2022), crusting, water infiltration and hydraulic conductivity (Reynolds et al. 2009; Tiwary et al. 2014; Raychaudhuri et al. 2014), available water, soil bulk density (Pattison et al. 2008), aggregate stability, and soil depth (Dalal and Moloney 2000). Soil chemical attributes influence plant growth and development in terms of nutrient adsorption capacity, nutrient availability and mobility (Doran et al. 1999; Weil and Magdoff 2004), toxicity, deficiency, and environmental pollution in terms of soil acidification, sodicity, alkalinity, and salinity, which directly affect biological processes in the soils. Chemical soil quality includes soil pH (Idowu et al. 2009; Kumar and Sharma 2020), electrical conductivity (Dalal and Moloney 2000; Arnold et al. 2005), soil and plant nutrients

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(Hartemink 2006), base saturation, cation exchange capacity, salts, toxic elements (Ross et al. 2008). Though soil biological indicators are dynamic and no threshold levels have been so far, soil organic carbon (SOC) (Dalal and Moloney 2000; Janzen 2005; Kuzyakov and Gavrichkova 2010), microbial biomass (Post and Kwon 2000; Weil and Magdoff 2004; Allen et al. 2010; Velmourougane et al. 2013a), soil respiration (Chou et al. 2008; Wixon and Balser 2009; Velmourougane and Sahu 2013), potentially mineralizable nitrogen, soil enzymes (Dick 1994; Fließbach et al. 2007; Dorodnikov et al. 2009; Blaise and Velmourougane 2014; Velmourougane et al. 2013b, c; Srivastava et al. 2014; Kumar et al. 2015), macro-, meso- and microfauna population (Barrios 2007), and microbial population and their diversity (Arias et al. 2005; Singh et al. 2006; Kuramae et al. 2011, 2012; Srivastava et al. 2014; Velmourougane et al. 2014a, b; Blaise et al. 2021) constitute some of the biological indicators (Lal et al. 2007; Kibblewhite et al. 2008; Ritz et al. 2009). Consequently, several soil quality indicators have been evaluated for their credibility under various bioclimates, crop models, and land use change (Chatterji et al. 2014; Mandal et al. 2014; Patil et al. 2014; Ray et al. 2014; Sidhu et al. 2014; Venugopalan et al. 2014; Ghorai et al. 2022). A detailed appraisal of soil health indicators and evaluation methods has been critically reviewed (Karlen et al. 2019, 2021a, b; Veum et al. 2021). Some of the popular and widely accepted soil health assessment methods include based on visual methods (Shepherd 2000), agro-ecosystem approach (Liebig et al. 2004), visual assessment of soil structural attributes (Ball et al. 2007; Guimaraes et al. 2011), soil conditioning indices (Zobeck et al. 2008), soil health tests (Haney 2014; Congreves et al. 2015), soil quality indices (Bosarge 2015; Mitchell et al. 2015), soil security (Koch et al. 2015), and soil health scorecards (Mann 2017). Though several soil health assessment methods have been developed and evaluated, the SMAF protocol (Andrews et al. 2004) developed from the work by Karlen et al. (1994) and the CASH protocol developed by Cornell (Idowu et al. 2008; Schindelbeck et al. 2008) were the predominantly used as soil health assessment protocols, presently (Chang et al. 2021). The data reduction techniques (PCA and RFA) were primarily used in SMAF and CASH protocols (Chang et al. 2021), and further refinements in the data attributes of these two protocols are proposed to be improvised in the future soil health assessment protocols such as “Integrated Soil Health Index (ISHI),” which further reassesses and refines the current soil health scoring curves (Nunes et al. 2021). Based on the meta-analysis of eleven soil assessment methods and fourteen soil health scores, Chang et al. (2021) concluded that though the methods were helpful for researchers, farmers, and stakeholders in assessing soil health, an inconsistent and wide variability based on the selection of method was observed. Thus, they suggested combining or altering these methods to suit the local climate, soil conditions, and agricultural practices for accurate soil health evaluation.

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Climate Change Impacts on Soil and Crop Health

Climate change is expected to bring about aberrations in weather parameters, which may trigger severe events such as drought, floods, cyclones, heat and cold waves, frost, hail storm, and tsunami, which may have intense effects on agriculture and food security (Srinivasarao et al. 2020). Increased levels of CO2 in the atmosphere due to climate change may result in additive warming and variation in rainfall patterns (Denman et al. 2007), which will significantly affect environmental quality in terms of changes in soil mineralogy, soil chemistry, crop productivity, food security, and food quality (Qafoku 2010, 2015). Increased levels of GHGs may also enhance the frequency and variations in droughts and floods (Yahdjian and Sala 2008). Higher intensity of precipitation, especially in dry regions and tropics, may bring on loss of soil nutrients through runoff and erosion depending on the soil type and structure, leading to soil degradation (Xu et al. 2016). Organic matter loss may also influence nutrient transformation in soils and will affect soil reactions, i.e., soil pH (De Vries and Breeuwsma 1987; Reth et al. 2005). Further, elevated temperatures can enhance decomposition rates of SOM (Davidson and Janssens 2006), which may influence the cation exchange capacities (CEC) of the soils, where low soil CEC will induce leaching of higher base cations from soils creating alkalinity in the event of high rainfall. Intense rainfall significantly affects the attraction and detachment of materials from the soil surface (Bryan 2000; Nearing et al. 2004), while the increased temperature was reported to lengthen the crop season and subsequent soil cover resulting in lesser detachment of soil particles (Evans and Brazier 2005; Morgan 2005; Christidis et al. 2007). Higher evapotranspiration rates (Hulme et al. 2002) in those soils may increase the disassembly of the particles (Bradley et al. 2005; Falloon and Betts 2010). Bare soils, especially sandy and peat exposed to high temperatures, are highly vulnerable to the detachment of mineral particles in the soil (Elhassanin et al. 1993) apart from wind erosion (Nanney et al. 1993) and raindrop splash (Sharma et al. 1995). Lower levels of SOC decrease the aggregate stability and soil structure (Tisdall and Oades 1982; Oades 1984; Shepherd et al. 2002) resulting in greater soil erosion (Colborne and Staines 1985; Guerra 1994). High rainfall after prolonged dry spells causes greater loss of dissolved SOC in rewetted soils (Worrall and Burt 2005). Climate-induced extreme temperatures have profound impacts on soil–plant–microbe interactions (Marchand et al. 2006), and increased soil temperatures greatly influence soil chemical and biological processes (Jenkinson et al. 1991) including acceleration of microbial activities and consequent carbon mineralization (Ciais et al. 2005). A significant and positive interaction between temperature and rainfall is well established in different agroecological systems (Luo et al. 2008). Climate changeinduced rise in temperature affects ecosystem health through the intensification of the water cycle, i.e., increased precipitation with accompanying surface overflow resulting in higher erosion, soil nutrient loss, and groundwater pollution (Arheimer et al. 2005; Monteith et al. 2007; Polizzotto et al. 2008; Granger et al. 2010; Ghaly and Ramakrishnan 2015). Generally, an increase in temperature speeds up the rates

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of nutrient cycling (C, N, P) (Macleod et al. 2012). Climate change-induced increase in temperature accelerates the breakdown of SOM (Maracchi et al. 2002), SOC (Bellamy et al. 2005; Smith 2012), and organic nitrogen mineralization (Sierra 1997; Ineson et al. 1998). Increased precipitation accelerates the erosion and sediment flow (Nearing et al. 2004; Thodsen et al. 2008) resulting in greater loss of nutrients through leaching, including nitrates and phosphates (Blake et al. 2002; Dueri et al. 2007; Quinton and Catt 2007; Hatfield et al. 2008). Plant protection chemicals, fertilizers, and associated heavy metals applied to agricultural lands too pollute surface and groundwaters under high rainfall circumstances based on their solubility and persistence (Donald et al. 2005; Bloomfield et al. 2006; Rothwell et al. 2008; Rohr et al. 2008; Biswas et al. 2018). Linkages between changes in weather patterns and infectious disease transmission have also been recognized (Lake et al. 2005; Boxall et al. 2009). Alterations in weather parameters influence plant development and their physiology and will have direct consequences on soil health including soil biology. Plant phenology and physiology are highly influenced by the elevated CO2 (Ainsworth and Long 2005), which affects their soil carbon allocation (Drigo et al. 2008), thereby affecting soil and plant-associated microbiome, their community structure, and functions (Garrett et al. 2006; Carney et al. 2007; Lesaulnier et al. 2008; Drigo et al. 2009, 2010; Compant et al. 2010; Nguyen et al. 2011; Chakraborty et al. 2012). Agricultural intensification was also demonstrated to bring down the network complexity and abundance of root microbiome (Banerjee et al. 2019). Global warming-induced climatic variations can also affect host–plant characteristics (Sharma et al. 2010). Noticeable decline in the induction of plant jasmonic acid and ethylene production and associated increases in pest and disease incidence were observed under elevated CO2 (Plazek et al. 2001; Casteel 2010; Pritchard 2011) necessitating higher chemical inputs and associated resistance development and soil pollution (Juroszek and von Tiedemann 2011). Elevated temperature increases transpiration, resulting in less photosynthetic rate and biomass addition to soils (Qaderi et al. 2012). In addition to higher CO2 and temperature, water stress remarkably affects soil health through alteration of soil attributes apart from plant development and connected soil microbiome (de Boer et al. 2005; Guenet et al. 2012; Schnepf et al. 2022). In contrast to water stress, climate change-induced sporadic floods can also affect the microbial diversity and their community composition in soils and biogeochemical cycles (Shrestha et al. 2008; Rui et al. 2009). Flooding lowers oxygen availability, supports the anaerobic situation, and promotes methanogenesis and enhanced methane variability in soils (Angel et al. 2012; King and Henry 2019).

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Role of Bioinoculants in Enhancing Soil Health/Crop Productivity Under Climate Change Situations

Variations in the climatic factors induce several stresses in the soil such as heat, drought, waterlogging, salinity, and metal stress, which greatly affect soil physicochemical and biological attributes and subsequent crop productivity (Lobell and Gourdji 2012; Mishra et al. 2017; Teshome et al. 2020). Further, stressed environments weaken crop growth and metabolic functions such as the composition of biochemical constituents, altered rhizodeposition, and biological activities related to plant-associated microbes and microbial community structure (Phillips et al. 2004; Neumann and Römheld 2007; Wakelin et al. 2007; Wu et al. 2008; Trivedi et al. 2012). Climate change can also weaken the plant defense systems, which leads to its vulnerability against several biotic stresses including pest and disease incidence. Beneficial microorganisms and their functionality in terms of plant–soil– microbiome interactions play an essential role in climate change situations by providing the host plants a stable nutrient and moisture supply and protection against biotic stress with a concomitant reduction in synthetic agri-inputs (Mitter et al. 2013; Velmourougane et al. 2017e; Ali et al. 2020; Fiodor et al. 2021; Velmourougane et al. 2021). As discussed earlier, climate change mostly affects soil health and consequent crop productivity through temperature or moisture fluctuations at spatial and time scale. High- or low-temperature (heat/frost)-coupled extreme moisture regimes (waterlogged/drought) directly affect soil biological quality, thereby influencing soil physicochemical properties. Disturbances in the soil properties in terms of disruption of soil structure, hydraulic properties, infiltration, aeration, moisture retention, nutrient transformations, and biological activities make them an ill environment for normal plant functions and its productivity (Tikhonovich and Provorov 2011; De Vries et al. 2020). However, the evolutionary adaptions acquired by the microorganisms play an essential role in the restoration of soil attributes to support crop plants under climate change situations (More et al. 2014; Basu et al. 2021; Coban et al. 2022). Microorganisms in general and bioinoculants, biopesticides, bioherbicides, bioremediators specifically act as an eco-friendly and cost-effective technology, which aids in building up of soil and crop health through beneficial plant–soil–microbial interactions (Badri et al. 2009; Evangelisti et al. 2014; Kang et al. 2014; Rehman et al. 2019; Huang et al. 2020; Fiodor et al. 2021; Mahmud et al. 2021), which includes growth promotion, alleviation of stresses, production of compatible solutes, polysaccharides, antioxidant and plant defense enzymes, scavenging of reactive oxygen species (ROS) (Mhamdi and Van Breusegem 2018; Batool et al. 2020; Kerchev et al. 2020), production of insecticidal/bactericidal/ fungicidal molecules, nutrient fixation, solubilization, and mobilization of soil nutrients. Some of the primary mechanisms elicited by the microorganisms to mitigate climate change-induced stress in soil and crop plants are presented in Fig. 2.2. Apart from rhizospheric beneficial microorganisms, phyllosphere colonizing microorganisms also help in plant development, nutrient availability, and biocontrol

Fig. 2.2 Mechanisms elicited by microorganisms to mitigate climate change-induced stress in soil and crop plants

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by inducing natural plant defense machinery (Thapa et al. 2017, 2018a, b, 2021; Sivakumar et al. 2020; Bashir et al. 2021; Li et al. 2022; Mir et al. 2022). Several microbial technologies help sustain agricultural productivity in stressed environments and prevent land degradation, apart from the restoration of marginal lands for agricultural expansion (Vergani et al. 2017; Riva et al. 2019). Developments in synthetic biology, soil–plant–microbiome engineering, cropspecific obligate endophytes/endosymbionts, plant–microbe signaling, biofilm formation and quorum sensing, and stress tolerance microbial genes further provide adaptive attributes to mitigate climate change (Ryan et al. 2009; Farrar et al. 2014; Ahkami et al. 2017; Velmourougane and Blaise 2021). Heat stress is another crucial abiotic factor, which influences plant functioning by interfering in plant phenology, cellular activities, and gene expression (Ahmad et al. 2022). Though plants have their own survival mechanisms to overcome heat stress (Hassan et al. 2021; Jagadish et al. 2021), natural or exogenous application of microorganisms eases the heat stress through enhanced plant growth hormone production, modulation of ethylene, abscisic acid, and ion transporters (Ali et al. 2009; Abd El-Daim et al. 2014; Egamberdieva et al. 2017; Issa et al. 2018; Bruno et al. 2020; Dastogeer et al. 2022), production of heat shock proteins (Ali et al. 2011), production of ACC deaminase enzyme, induction of plant antioxidant defense enzymes, compatible solutes, etc. (Srivastava et al. 2008; Maitra et al. 2021). Soil salinity as a abiotic stress affects soil and crop health through osmotic imbalance (Shrivastava and Kumar 2015) Similarly, several beneficial microorganisms confer salinity tolerance in crop plants (Chu et al. 2019; Bhat et al. 2020) through the phytohormone production, regulation of ethylene production, the induction of plant antioxidant defense enzymes, quorum sensing, etc. (Khan et al. 2011; Ramadoss et al. 2013; Singh et al. 2015; Hashem et al. 2016; Mukhtar et al. 2020; Nawaz et al. 2020). Climate change is projected to reduce water availability by 30% and increase agricultural drought by twofold by 2050 (Falkenmark 2013). Among the climateinduced abiotic factors, drought stress in agriculturally important crops is a major challenge faced worldwide, as drought significantly affects crop growth and subsequent agricultural productivity. Though the breeding of drought-tolerant crops (Philippot et al. 2013; Coleman-Derr and Tringe 2014) and soil management practices (Jongdee et al. 2006) have been proposed, future drought mitigation technologies under climate change are a big challenge. The use of biostimulants has been proposed as an eco-friendly approach to enhance agricultural productivity under future climate change situations (Chiaiese et al. 2018). Biostimulant application enhanced plant growth hormone production, metabolic activities, nutrient transport, defense mechanisms, yield, and product quality (Backer et al. 2018; Shukla et al. 2019). Several microbial species act as plant growth promoters in easing the detrimental effects of drought (Enebe and Babalola 2018; Camaille et al. 2021; Fiodor et al. 2021; Kumar et al. 2022). Microorganisms mitigate drought stress in crops through their beneficial associations and production of biosurfactants, phytohormones, siderophores, etc. (Sandhya et al. 2009; Sathya et al. 2017; Singh et al. 2018; Jayakumar et al. 2020).

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Siderophore production in bacteria was significantly and positively correlated with drought stress, where higher levels of siderophores were detected in drought resistance plants (Arzanesh et al. 2011). Drought induces the generation of ROS (hydroxyl radical and singlet oxygen), which causes severe cellular oxidative damage in plants (Cruz De Carvalho 2008). Bacteria scavenge ROS (Coleman-Derr and Tringe 2014) through the production of proline (Hayat et al. 2012) and other defense enzymes (Rezayian et al. 2018). Several antioxidant enzymes and phenolic compounds, including peroxidase, polyphenol oxidase, and catalase, have also been implicated in the scavenging of drought-induced ROS in plants (Apel and Hirt 2004; Zandalinas et al. 2018; Laxa et al. 2019; Singh et al. 2020). The microbial elicitation of these antioxidant enzymes in plants against stresses is well documented (Velmourougane et al. 2017d, 2019a). Drought stress is also mitigated through the production of salicylic acid (Habibi 2012; Arun et al. 2020), which regulates plant growth and physiological processes (Khan et al. 2014; Miura and Tada 2014). Production of extracellular polysaccharide substances (EPS) by bacteria also helps crop plants mitigate drought stress (Sandhya et al. 2009; Ozturk and Aslim 2010; Qurashi and Sabri 2012; Costa et al. 2018). Microorganisms protect their cells from stressed-induced oxidative damage through osmoregulation, antioxidant properties, and biofilm-forming capabilities (Bashan and de Bashan 2010). Microbial production of biosurfactants, which act as solubilizing, complexing, and chelating agents, also helps in nutrient supply and biocontrol agents in stressed environments (Sheng et al. 2008; Akladious et al. 2019). Several macro- and micronutrient solubilizing bioinoculants help in nutrient availability by solubilizing fixed forms of soil nutrients to plant-available forms (Santosh et al. 2022). Recently, Serratia sp. and Acinetobacter sp. solubilized fixed zinc, indicating their prospects of overcoming zinc deficiencies in agricultural crops and replacement of chemical micronutrient fertilizers in crop nutrient management (Othman et al. 2022). In contrast to the drought, prolonged waterlogging causes hypoxic and minimal free oxygen conditions in plant roots affecting their growth (Glick 2014; Paul et al. 2016). Though plants mitigate waterlogging stress through several mechanisms (Voesenek and Sasidharan 2013; Osakabe et al. 2014), higher levels of ethylene build-up from the precursor (1-aminocyclopropane-1-carboxylate; ACC) during waterlogging conditions cause plant growth retardation, chlorosis, necrosis, and plant senescence (Mayak et al. 2004; Glick et al. 2007). Several beneficial bacteria, which encode ACC deaminase, help crop survival under waterlogged conditions by lowering the biosynthesis of ethylene by catabolizing the ACC into α-ketobutyrate and ammonia (Sasidharan et al. 2017; Ali and Kim 2018) helping plant productivity (Farwell et al. 2007; Barnawal et al. 2012; Nascimento et al. 2012, 2018; Li et al. 2013; Ravanbakhsh et al. 2017). Further, it was reported that the availability of ACC to ACC deaminizing bacteria enhances the expression of acdS (ACC deaminase gene) and subsequent ACC deaminase activity (Glick et al. 1998, 2007; Li and Glick 2001; Nascimento et al. 2018). Recently, the utility of microbial biofilms in crop production and soil fertility has gained momentum due to their multifunctional benefits in terms of enhanced

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colonization potential, increased plant growth, soil health, and metabolic and genetic changes in host plants (Bharti et al. 2017; Velmourougane et al. 2017a, b, c, d, e, 2019a, b, 2022; Kour et al. 2020; Jiang et al. 2021; Khan et al. 2022; Sun et al. 2022). Biofilms are an assemblage of microbial cells in polymeric substances, mostly composed of polysaccharides nature (O’Toole et al. 2000). Generally, microorganisms form biofilms to mitigate environmental stress, and several species of bacteria, fungi, yeast, and cyanobacteria form biofilm in nature (Velmourougane et al. 2017b). Apart from naturally occurring microbial biofilms, agriculturally important cyanobacterial and fungal-based bacterial biofilms have also been developed under laboratory conditions and evaluated for their plant growth promotion, soil health enhancements, nutrient availability (Prasanna et al. 2012, 2015a, b, 2021; Triveni et al. 2013; Velmourougane and Prasanna 2017; Velmourougane et al. 2022), biocontrol potential (Prasanna et al. 2008, 2010, 2011, 2013, 2015c, 2016a, b, c; Triveni et al. 2015), and environmental remediation (Prasanna et al. 2002) for several crops under field conditions (Prasanna et al. 2014, 2017, 2018). Microorganisms form biofilms in soil and different plant parts (Seneviratne et al. 2011; Velmourougane and Prasanna 2017; Nayak et al. 2020) and enhance soil and plant production in stressed environments (Velmourougane et al. 2017d, 2019a; Khan et al. 2022). Biofilm-forming microorganisms benefit the host plants for enhanced growth through effective colonization and production of growth-promoting hormones, increase soil nutrient availability through solubilization, mobilization, and plant nutrient uptake, induce systemic resistance through elicitation of natural plant defense and antioxidant enzymes, induce stress tolerance through altered gene expression, etc. (Velmourougane et al. 2017d, 2019a; Kumar and Singh 2020; Bhat and Bhat 2022). Recent studies have reported the role of biofilm-forming microorganisms and their EPS in providing safeguarding against stresses such as heat, drought, and salinity in host plants (Dobrowolski et al. 2017; Abd El-Ghany and Magdy 2020; Sharma et al. 2021; Shaffifique et al. 2022a). Further, biofilms play a major role in the remediation of metal contaminants and pollutants in soils and water through their uptake and adsorption in the polymeric matrix (Parker et al. 2000; Williams et al. 2013; Bai et al. 2016). Microbial biofilms can thus impart stress tolerance in host plants (Bhagat et al. 2021; Ciofu et al. 2022; Shaffifique et al. 2022b), enhance crop productivity (Admassie et al. 2022), and provide protection against phytopathogens and other abiotic/biotic stresses (Chandwani and Amaresan 2022). In addition to the developed microbial biofilms, periphytic biofilms have gained economic value in agriculture and environmental remediation (Bharti et al. 2017; Wu 2017), recently, because of their beneficial role in soil nutrient transformation (Su et al. 2017; Wu et al. 2016; Beheshti et al. 2021), nutrient fixation, energy flows (Liu et al. 2017), and remediation of soil and water pollution (Lu et al. 2014; Shabbir et al. 2017), thereby enhancing soil health. Periphytic biofilms are generally present in the submerged soils and sediments of wetland ecosystems and principally represent a mixed population of unicellular and multicellular algae, cyanobacteria, and other photo- and heterotrophic microorganisms united by polymeric substances

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attached to soils (Miao et al. 2021). Periphytic biofilms largely help in the removal of nutrients from the runoff water through the production of a polymeric matrix and their adsorption (Wu et al. 2018). Cyanobacteria along with other microbial groups including lichens, mosses, fungi, and bacteria help in the rehabilitation of deteriorated lands, especially in arid and desert regions, through the formation of biological soil crusts (BSC) (Belnap and Eldridge 2001), which improve soil aggregation (Neuman et al. 1996; Bu et al. 2014), soil structure (Sadeghi et al. 2017), soil stability (Belnap 2003; Kheirfam et al. 2017), and water and nutrient retention capacity, through the production of exopolymers (Bowker et al. 2002; Belnap and Lange 2003). Hence, the promotion and application of BSC-forming microorganisms are a feasible and promising option for improving soil health through the prevention of soil degradation and reclamation of arid and desert environments (Kamennaya et al. 2015; Sole et al. 2015).

2.6

Summary and Future Prospects

Under the climate change era, drought, waterlogging, salinity, alkalinity, heat and cold stress, metal toxicity, weeds, pest and disease incidence, and human health are some of the major concerns worldwide. The accelerated rate of climate change is foreseen to cause further decline in soil health and agricultural production, through additional use of chemical fertilizers (for plant nutrition), plant protection chemicals (to manage the higher incidence of pests and diseases), herbicides (to manage the higher weed problems), plant growth hormones (to regulate plant growth), etc. The additional cost of cultivation, apart from affecting the livelihood of the farmers, is also expected to cause further stress to the environment in addition to pollution of soil and water demanding suitable remedial measures. Though several climate mitigation strategies, including efficient soil and water management, conservation agriculture, restoration of degraded lands, breeding of climate-resilient crops, etc., were adopted, the use of beneficial microorganisms is central to soil and crop health, apart from acting as bioremediators of environmental pollution and alleviator of stresses in agriculturally important crops. Though several studies have established the beneficial roles of microorganisms in mitigating climate change with respect to soil and crop health, most studies are of an academic nature and have not produced practical utility. Since drought and waterlogging are the major future challenges, microorganisms with drought-tolerant and waterlogging survival traits must be identified and integrated into the plant systems through molecular approaches. The recent concepts of core microbiome, multi-species microbial biofilms, microbialbased volatiles, and rhizo-engineering can be further explored for better soil–plant– microbe interactions to enhance soil and plant health. Further, exploring carbon sequestering microbes in harsh environments and less GHG-producing microbes in wetland systems can increase soil health and reduce GHG emissions. The development and evaluation of microbial consortia with multiple benefits, such as plant growth promotion, soil nutrient availability, biocontrol control potential, elicitation

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of natural plant defense enzymes, and mitigation of environmental stresses, are the most beneficial strategy toward environment-friendly agricultural practices.

References Abd El-Daim IA, Bejai S, Meijer J (2014) Improved heat stress tolerance of wheat seedlings by bacterial seed treatment. Plant and Soil 379:337–350 Abd El-Ghany MF, Magdy A (2020) Effect of exopolysaccharide-producing bacteria and melatonin on faba bean production in saline and non-saline soil. Agronomy 10:316. https://doi.org/10. 3390/agronomy10030316 Addiscott TM (2010a) Soil mineralization: an emergent process? Geoderma 160:31–35 Addiscott TM (2010b) Entropy, non-linearity and hierarchy in ecosystems. Geoderma 160:57–63 Admassie M, Woldehawariat Y, Alemu T et al (2022) The role of plant growth-promoting bacteria in alleviating drought stress on pepper plants. Agric Water Manag 272:107831 Ahkami AH, Allen White R, Handakumbura PP et al (2017) Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere 3:233–243 Ahmad M, Imtiaz M, Shoib Nawaz M et al (2022) What did we learn from current progress in heat stress tolerance in plants? Can microbes be a solution? Front Plant Sci 13:794782. https://doi. org/10.3389/fpls.2022.794782 Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372 Akladious SA, Gomaa EZ, El-Mahdy OM (2019) Efficiency of bacterial biosurfactant for biocontrol of Rhizoctonia solani (AG - 4) causing root rot in faba bean (Vicia faba) plants. Eur J Plant Pathol 153:15–35 Ali S, Kim WC (2018) Plant growth promotion under water: Decrease of waterlogging-induced ACC and ethylene levels by ACC deaminase-producing bacteria. Front Microbiol 9:1096 Ali SZ, Sandhya V, Grover M et al (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils 46:45–55 Ali SZ, Sandhya V, Grover M et al (2011) Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J Plant Interact 6:239–246 Ali J, Ali F, Ahmad I et al (2020) Mechanistic elucidation of germination potential and growth of Sesbania sesban seedlings with Bacillus anthracis PM21 under heavy metals stress: an in vitro study. Ecotoxicol Environ Saf 208:111769 Al-Kaisi MM, Lal R, Olson KR et al (2017) Fundamentals and functions of soil environment. In: Al-Kaisi MM, Lowery B (eds) Soil health and intensification of agroecosystems. Elsevier Academic Press, London, pp 1–20 Allen DE, Pringle MJ, Page KL et al (2010) A review of sampling designs for the measurement of soil organic carbon in Australian grazing lands. Rangel J 32:227–246 Allen DE, Singh BP, Dalal RC (2011) Soil health indicators under climate change: a review of current knowledge. In: Singh BP et al (eds) Soil Health and climate change. Springer‐Verlag, Berlin, pp 25–45 Amelung W, Bossio D, de Vries W et al (2020) Towards a global-scale soil climate mitigation strategy. Nat Commun 11:5427 Mahmud AM, Upadhyay SK, Srivastava AK, Bhojiya AA (2021) Biofertilizers: a Nexus between soil fertility and crop productivity under abiotic stress. Curr Res Environ Sustain 3:100063. https://doi.org/10.1016/j.crsust.2021.100063 Andrews SS, Karlen DL, Cambardella CA (2004) The soil management assessment framework: a quantitative soil quality evaluation method. Soil Sci Soc Am J 68:1945–1962

38

K. Velmourougane and R. Prasanna

Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862 Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399 Arheimer B, Andreasson J, Fogelberg S et al (2005) Climate change impact on water quality: model results from southern Sweden. Ambio 34:559–566 Arias ME, Gonzalez-Perez FJ, Gonzalez-Vila ASB (2005) Soil health: a new challenge for microbiologists and chemists. Int Microbiol 8:13–21 Arneth A, Denton F, Agus F et al (2019) Framing and context. In climate change and land. In: Shukla PR et al (eds) An IPCC Special Report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. The Intergovernmental Panel on Climate Change (IPCC), Geneva, pp 77–128 Arnold SL, Doran JW, Schepers J et al (2005) Portable probes to measure electrical conductivity and soil quality in the field. Commun Soil Sci Plant Anal 36:2271–2287 Arora NK (2019) Impact of climate change on agriculture production and its sustainable solutions. Environ Sustain 2:95–96 Arshad MA, Lowery B, Grossman B (1996) Physical tests for monitoring soil quality. In: Doran JW, Jones AJ (eds) Methods for assessing soil quality. Society of America Special Publication, Madison, WI, pp 123–141 Arun K, Sabarinathan D, Gomathy KG et al (2020) Mitigation of drought stress in rice crop with plant growth-promoting abiotic stress-tolerant rice phyllosphere bacteria. J Basic Microbiol 60: 768–786 Arzanesh MH, Alikhani HA, Khavazi K et al (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27: 197–205 Backer R, Rokem JS, Ilangumaran G et al (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 871:1–17 Badri DV, Weir TL, Van Der Lelie D et al (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650 Bai L, Xu H, Wang C (2016) Extracellular polymeric substances facilitate the biosorption of phenanthrene on cyanobacteria Microcystis aeruginosa. Chemosphere 162:172–180 Ball BC, Batey T, Munkholm LJ (2007) Field assessment of soil structural quality—a development of the Peerlkamp test. Soil Use Manage 23:329–337 Banerjee S, Walder F, Büchi L et al (2019) Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J 13:1722–1736 Barnawal D, Bharti N, Maji D et al (2012) 1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiol Biochem 58:227–235 Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64:269–285 Bashan Y, de Bashan LE (2010) How the plant growth-promoting bacterium azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136. https://doi.org/10.1016/S00652113(10)08002-8 Bashir I, Assad R, War AF et al (2021) Application of phyllosphere microbiota as biofertilizers. In: Dar GH et al (eds) Microbiota and biofertilizers, vol 2. Springer, Berlin, pp 311–327 Basu A, Prasad P, Das SN et al (2021) Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13:1140 Batool T, Ali S, Seleiman MF et al (2020) Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Sci Rep 10:16975 Baveye PC (2021) Soil health at a crossroad. Soil Use Manage 37:215–219

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

39

Beheshti M, Alikhani HA, Pourbabaee AA et al (2021) Periphytic biofilm and rice rhizosphere phosphate-solubilizing bacteria and fungi: a possible use for activating occluded P in periphytic biofilms in paddy fields. Rhizosphere 19:100395 Bellamy PH, Loveland PJ, Bradley RI et al (2005) Carbon losses from all soils across England and Wales 1978–2003. Nature 437:245–248 Belnap J (2003) Biological soil crusts in deserts: a short review of their role in soil fertility, stabilization, and water relations. Algol Stud 109:113–126 Belnap J, Eldridge D (2001) Disturbance and recovery of biological soil crusts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer-Verlag, Berlin, pp 363–383 Belnap J, Lange OL (2003) Biological soil crusts: structure function and management. SpringerVerlag, Berlin 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 Bhagat N, Raghav M, Dubey S et al (2021) Bacterial exopolysaccharides: Insight into their role in plant abiotic stress tolerance. J Microbiol Biotechnol 28:1045–1059 Bharti A, Velmourougane K, Prasanna R (2017) Phototrophic biofilms: diversity, ecology and applications. J Appl Phycol 29:2729–2744 Bhat KU, Bhat DP (2022) Microbes–surfaces interactions. In: Inamuddin Ahamed MI, Prasad R (eds) Application of microbes in environmental and microbial biotechnology. Springer, Singapore, pp 473–499 Bhat MA, Kumar V, Bhat MA et al (2020) Mechanistic insights of the interaction of plant growth promoting rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Front Microbiol 20:1952 Bhattacharyya T, Pal DK, Mandal C et al (2013) Soils of India: their historical perspective, classification and recent advances. Curr Sci 104:1308–1323 Bhattacharyya T, Sarkar D, Ray SK et al (2014a) Soil information system: use and potentials in humid and semi-arid tropics. Curr Sci 107:1550–1564 Bhattacharyya T, Sarkar D, Ray SK et al (2014b) Georeferenced soil information system: assessment of database. Curr Sci 107:1400–1419 Bhattacharyya P, Munda S, Dash PK (2019) Climate change and greenhouse gas emission. New India Publishing Agency, New Delhi, p 195 Bindraban PS et al (2012) Assessing the impact of soil degradation on food production. Curr Opin Environ Sustain 4:478–488 Biswas B, Qi F, Biswas JK et al (2018) The fate of chemical pollutants with soil properties and processes in the climate change paradigm—a review. Soil Syst 2:51. https://doi.org/10.3390/ soilsystems2030051 Blaise D, Velmourougane K (2014) Dynamics of soil dehydrogenase and alkaline phosphatase activities under organically and conventionally grown cotton on rainfed vertisols of Central India. Cotton Res J 6:54–57 Blaise D, Velmourougane K, Santosh S et al (2021) Intercrop mulch affects soil biology and microbial diversity in rainfed transgenic Bt cotton hybrids. Sci Total Environ 794:148787. https://doi.org/10.1016/j.scitotenv.2021.148787 Blaise D, Majumdar G, Manikandan A et al (2022) Subsoiling and crop rotation improved root growth of Bt-cotton grown on Vertisols. Curr Sci 123:874–880 Blake L, Hesketh N, Fortune S et al (2002) Assessing phosphorus ‘Change-Points’ and leaching potential by isotopic exchange and sequential fractionation. Soil Use Manage 18:199–207 Bloomfield JP, Williams RJ, Gooddy DC et al (2006) Impacts of climate change on the fate and behaviour of pesticides in surface and groundwater—a UK perspective. Sci Total Environ 369: 163–177 Bomfim B, Pinagé ER, Emmert F et al (2022) Improving sustainable tropical forest management with voluntary carbon markets. Plant and Soil 479:53–60

40

K. Velmourougane and R. Prasanna

Bosarge T (2015) A soil quality index for Alabama. Master dissertation, Auburn University, Auburn, Alabama Bowker MA, Reed SC, Belnap J et al (2002) Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microb Ecol 43:13–25 Boxall ABA, Hardy A, Beulke S et al (2009) Impacts of climate change on indirect human exposure to pathogens and chemicals from agriculture. Environ Health Perspect 117:508–514 Bradley RI, Moffat AJ, Falloon PD (2005) Climate change and soil function. Defra final report SP0538. Defra, London Brevik EC (2018) A brief history of the soil health concept. Soil Science Society of America, Madison, WI Bruno LB, Karthik C, Ma Y et al (2020) Amelioration of chromium and heat stresses in Sorghum bicolor by Cr6+ reducing-thermotolerant plant growth promoting bacteria. Chemosphere 244: 125521. https://doi.org/10.1016/j.chemosphere.2019.125521 Bruulsema T (2015) Human health depends on soil fertility. Plant Nutr Today Spring(1) http:// www.ipni.net/publication/pnt-na.nsf/0/74C55C99F86E902C85257DFD0064D7F8/$FILE/ PNT-2015-Spring-01.pdf. Accessed 2 Aug 2022 Bryan RB (2000) Soil erodibility and processes of water erosion on hillslope. Geomorphology 32: 385–415 Bu C, Wu S, Yang Y et al (2014) Identification of factors influencing the restoration of cyanobacteria-dominated biological soil crusts. PloS One 9:e90049 Camaille M, Fabre N, Clément C et al (2021) Advances in wheat physiology in response to drought and the role of plant growth promoting rhizobacteria to trigger drought tolerance. Microorganisms 9:687 Carney KM, Hungate BA, Drake BG et al (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci U S A 104:4990–4995 Carter MR, Gregorich EG, Anderson DW et al (1997) Concepts of soil quality and their significance. In: Gregorich EG, Carter MR (eds) Soil quality for crop production and ecosystem health. Elsevier, Amsterdam Cassman KG, Grassini P, van Wart J (2010) Crop yield potential, yield trends, and global food security in a changing climate. In: Hillel D, Rosenzweig C (eds) Handbook of climate change and agroecosystems: impacts, adaptation, and mitigation. Imperial College Press, London, pp 37–51 Casteel CL (2010) Impacts of climate change on herbivore induced plant signaling and defenses. Dissertation, University of Illinois Chakraborty S, Pangga IB, Roper AM (2012) Climate change and multitrophic interactions in soil: the primacy of plants and functional domains. Glob Chang Biol 18:2111–2125 Chandwani S, Amaresan N (2022) Role of ACC deaminase producing bacteria for abiotic stress management and sustainable agriculture production. Environ Sci Pollut Res 20:1–17 Chang T, Feng G, Paul V et al (2021) Soil health assessment methods: progress, applications and comparison. Adv Agron 172:129–210 Chatterji S, Tiwary P, Sen TK et al (2014) Land evaluation for major crops in the Indo-Gangetic Plains and black soil regions using fuzzy model. Curr Sci 107:1502–1511 Chiaiese P, Corrado G, Colla G et al (2018) Renewable sources of plant biostimulation: microalgae as a sustainable means to improve crop performance. Front Plant Sci 871:1–6 Chou WW, Silver WL, Jackson RD et al (2008) The sensitivity of annual grassland carbon cycling to the quantity and timing of rainfall. Glob Chang Biol 14:1382–1394 Christidis N, Stott PA, Brown S et al (2007) Human contribution to the lengthening of the growing season during 1950–99. J Climate 20:5441–5454 Chu TN, Tran BTH, Van Bui L et al (2019) Plant growth-promoting rhizobacterium Pseudomonas PS01 induces salt tolerance in Arabidopsis thaliana. BMC Res Notes 12:11 Ciais P, Reichstein M, Viovy N et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

41

Cimpoiasu MO, Dowdeswell-Downey E, Evans DL et al (2021) Contributions and future priorities for soil science: Comparing perspectives from scientists and stakeholders. Eur J Soil Sci 72: 2538–2557 Ciofu O, Moser C, Jensen P et al (2022) Tolerance and resistance of microbial biofilms. Nat Rev Microbiol 3:1–15 Coban O, De Deyn GB, Van Der Ploeg M (2022) Soil microbiota as game-changers in restoration of degraded lands. Science 375:abe0725. https://doi.org/10.1126/science.abe0725 Colborne GJN, Staines SJ (1985) Soil-erosion in South Somerset. J Agric Sci 1:107–112 Coleman-Derr D, Tringe SG (2014) Building the crops of tomorrow: advantages of symbiont based approaches to improving abiotic stress tolerance. Front Microbiol 5:283. https://doi.org/10. 3389/fmicb.2014.00283 Compant S, van der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plantmicroorganism interactions. FEMS Microbiol Ecol 73:197–221 Congreves KA, Hayes A, Verhallen EA et al (2015) Long-term impact of tillage and crop rotation on soil health at four temperate agroecosystems. Soil Tillage Res 152:17–28 Cook J, Nuccitelli D, Green SA et al (2013) Quantifying the consensus on anthropogenic global warming in the scientific literature. Environ Res Lett 8:031003 Costa OYA, Raaijmakers JM, Kuramae EE (2018) Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front Microbiol 23:1636 Cruz De Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165 Dalal RC, Moloney D (2000) Sustainability indicators of soil health and biodiversity. In: Hale P et al (eds) Management for sustainable ecosystems. Centre for Conservation Biology, Brisbane, pp 101–108 Dastogeer KMG, Zahan MI, Rhaman MS et al (2022) Microbe-mediated thermotolerance in plants and pertinent mechanisms a meta-analysis and review. Front Microbiol 13:833566. https://doi. org/10.3389/fmicb.2022.833566 Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173 de Boer W, Folman LB, Summerbell RC et al (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811 De Vries W, Breeuwsma A (1987) The relationship between soil acidification and element cycling. Water Air Soil Pollut 35:293–310 De Vries FT, Griffiths RI, Knight CG et al (2020) Harnessing rhizosphere microbiomes for droughtresilient crop production. Science 368:270–274 DeLong C, Cruse R, Wiener J (2015) The soil degradation paradox: compromising our resources when we need them the most. Sustainability 7:866–879 Denman KL, Brasseur G, Chidthaisong A et al (2007) Coupling between changes in the climate system and biogeochemistry. In: Solomon S et al (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 499–587 Dick RP (1994) Soil enzyme activities as indicators of soil quality. In: Doran JW et al (eds) Defining soil for a sustainable environment. SSSA Special Publication, Madison, WI. https://doi.org/10. 2136/sssaspecpub35.c7 Dobrowolski R, Szcześ A, Czemierska M et al (2017) Studies of cadmium (II), lead (II), nickel (II), cobalt (II) and chromium (VI) sorption on extracellular polymeric substances produced by Rhodococcus opacus and Rhodococcus rhodochrous. Bioresour Technol 225:113–120 Donald DB, Hunter FG, Sverko E et al (2005) Mobilization of pesticides on an agricultural landscape flooded by a torrential storm. Environ Toxicol Chem 24:2–10 Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15:119–127

42

K. Velmourougane and R. Prasanna

Doran JW, Jones AJ, Arshad MA et al (1999) Determinants of soil quality and health. In: Pankhurst CE et al (eds) Biological Indicators of Soil Health. CABI, Wallingford Dorodnikov M, Blagodatskaya E, Blagodatsky S et al (2009) Stimulation of microbial extracellular enzyme activities by elevated CO2 depends on soil aggregate size. Glob Chang Biol 15:1603– 1614 Drigo B, Kowalchuk G, Van Veen A (2008) Climate change goes underground: effect of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679 Drigo B, van Veen JA, Kowalchuk GA (2009) Specific rhizosphere bacterial and fungal groups respond differently to elevated atmospheric CO2. ISME J 3:1204–1217 Drigo B, Pijl AS, Duyts H et al (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci U S A 107:10938– 10942 Dueri S, Calanca PL, Fuhrer J (2007) Climate change affects farm nitrogen loss—a Swiss case study with a dynamic farm model. Agr Syst 93:191–214 Egamberdieva D, Wirth SJ, Alqarawi AA et al (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104 Elhassanin AS, Labib TM, Gaber EI (1993) Effect of vegetation cover and land slope on runoff and soil losses from the watersheds of Burundi. Agric Ecosyst Environ 43:301–308 Enebe MC, Babalola OO (2018) The influence of plant growth-promoting rhizobacteria in plant tolerance to abiotic stress: a survival strategy. Appl Microbiol Biotechnol 102:7821–7835 Evangelisti E, Rey T, Schornack S (2014) Cross-interference of plant development and plantmicrobe interactions. Curr Opin Plant Biol 20:118–126 Evans R, Brazier R (2005) Evaluation of modelled spatially distributed predictions of soil erosion by water versus field-based assessments. Environ Sci Policy 8:493–501 Evans DL, Janes-Bassett V, Borrelli P et al (2022) Sustainable futures over the next decade are rooted in soil science. Eur J Soil Sci 73:e13145 Falkenmark M (2013) Growing water scarcity in agriculture: future challenge to global water security. Phil Trans R Soc A 371:20120410 Falloon P, Betts R (2010) Climate impacts on European agriculture and water management in the context of adaptation and mitigation—the importance of an integrated approach. Sci Total Environ 408:5667–5687 Fang Y, Singh BP, Matta P et al (2017) Temperature sensitivity and priming of organic matter with different stabilities in a vertisol with aged biochar. Soil Biol Biochem 115:346–356 FAO and ITPS (2015) Status of the World’s Soil Resources (SWSR)—Main report. Food and Agriculture Organization of the United Nations and Intergovernmental Technical Panel on Soils, Rome 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 Farwell AJ, Vesely S, Nero V et al (2007) Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal-contaminated field site. Environ Pollut 147:540–545 Fiodor A, Singh S, Pranaw K (2021) The contrivance of plant growth promoting microbes to mitigate climate change impact in agriculture. Microorganisms 30:1841. https://doi.org/10. 3390/microorganisms9091841 Fließbach A, Oberholzer HR, Gunst L et al (2007) Soil organic matter and biological soil quality indicators after 21 years of organic and conventional farming. Agric Ecosyst Environ 118:273– 284 Garrett KA, Dendy SP, Frank EE et al (2006) Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509 Ghaly AE, Ramakrishnan VV (2015) Nitrogen sources and cycling in the ecosystem and its role in air, water and soil pollution: a critical review. J Pollut Effect Control 3:2. https://doi.org/10. 4172/2375-4397.1000136

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

43

Ghee C, Neilson R, Hallett PD et al (2013) Priming of soil organic matter mineralisation is intrinsically insensitive to temperature. Soil Biol Biochem 66:20–28 Ghorai PS, Biswas S, Purakayastha TJ et al (2022) Indicators of soil quality and crop productivity assessment at a long term experiment site in the lower Indo-Gangetic plains. Soil Use Manage 39:503–520. https://doi.org/10.1111/sum.12847 Giebink CL, Domke GM, Fisher RA et al (2022) The policy and ecology of forest-based climate mitigation: challenges, needs, and opportunities. Plant and Soil 479:25–52 GISTEMP Team (2018) GISS Surface Temperature Analysis (GISTEMP). NASA Goddard Institute for Space Studies. https://data.giss.nasa.gov/gistemp/graphs_v3/Fig.A2.txt. Accessed 22 Sept 2022 Glare T, Caradus J, Gelernter W et al (2012) Have biopesticides come of age? Trends Biotechnol 30:250–258 Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39 Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68 Glick BR, Cheng Z, Czarny J et al (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339 Granger SJ, Bol R, Anthony S et al (2010) Towards a holistic classification of diffuse agricultural water pollution from intensively managed grasslands on heavy soils. Adv Agron 105:83–115 Gregorich EG, Carter MR, Angers DA et al (1994) Towards a minimum data set to assess soil organic matter quality in agricultural soils. Can J Soil Sci 74:367–385 Guenet B, Lenhart K, Leloup J et al (2012) The impact of long-term CO2 enrichment and moisture levels on soil microbial community structure and enzyme activities. Geoderma 170:331–336 Guerra A (1994) The effect of organic-matter content on soil-erosion in simulated rainfall experiments in W-Sussex, UK. Soil Use Manage 10:60–64 Guimaraes RML, Ball BC, Tormena CA (2011) Improvements in the visual evaluation of soil structure. Soil Use Manage 27:395–403 Habibi G (2012) Exogenous salicylic acid alleviates oxidative damage of barley plants under drought stress. Acta Biol Szeged 56:57–63 Haney RL (2014) Soil health. USDA-ARS. http://www.nrcs.usda.gov/Internet/FSE_ DOCUMENTS/nrcs144p2_043902.pdf Harris JA, Evans DL, Mooney SJ (2022) A new theory for soil health. Eur J Soil Sci 73:e13292 Hartemink AE (2006) Assessing soil fertility decline in the tropics using soil chemical data. Adv Agron 89:179–225 Hashem A, Abd Allah EF, Alqarawi AA et al (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:1089 Hassan MU, Chattha MU, Khan I et al (2021) Heat stress in cultivated plants: nature, impact, mechanisms, and mitigation strategies—a review. Plant Biosyst Int J Deal Aspects Plant Biol 155:211–234 Hatfield RG, Maher BA, Pates JM et al (2008) Sediment dynamics in an upland temperate catchment: changing sediment sources, rates and deposition. J Paleo 40:1143–1158 Hausfather Z, Drake HF, Abbott T et al (2020) Evaluating the performance of past climate model projections. Geophys Res Lett 47:e2019GL085378 Hayat S, Hayat Q, Alyemeni MN et al (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466 Hijioka Y, Lasco R, Surjan A et al (2014) ‘Africa,’ Climate Change 2014: impacts, adaptation and vulnerability: Part B: Regional aspects: Working Group II Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 1199–1266

44

K. Velmourougane and R. Prasanna

Huang H, Zhao Y, Fan L et al (2020) Improvement of manganese phytoremediation by Broussonetia papyrifera with two plant growth promoting (PGP) Bacillus species. Chemosphere 260:127614 Hulme M, Jenkins G, Lu X et al (2002) Climate change scenarios for the United Kingdom: the UKCIP02 Scientific Report. Tyndall Centre for Climate Change Research, School of Environmental Sciences, Norwich Hutchins DA, Jansson JK, Remais JV et al (2019) Climate change microbiology—problems and perspectives. Nat Rev Microbiol 17:391–396 Idowu OJ, van Es HM, Abawi GS et al (2008) Farmer-oriented assessment of soil quality using field, laboratory, and VNIR spectroscopy methods. Plant and Soil 307:243–253 Idowu OJ, van Es HM, Abawi GS et al (2009) Use of an integrative soil health test for evaluation of soil management impacts. Renew Agric Food Syst 24:214–224 Ineson P, Benham DG, Poskitt J et al (1998) Effects of climate change on nitrogen dynamics in upland soils. 2. A soil warming study. Glob Chang Biol 4:153–161 IPCC (2007) Climate change (2007). The fourth assessment report. Impacts, adaptation and vulnerability. https://www.ipcc.ch/publications_and_data/publications_ipcc_fourth_assess ment_report_wg2_report_impacts_adaptation_and_vulnerability.htm. Accessed 11 Sept 2022 IPCC (2012) Managing the risks of extreme events and disasters to advance climate change adaptation. In: Stocker TF et al (eds) A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change. IPCC and Cambridge University Press, Cambridge, New York IPCC (2013) Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of IPCC. Cambridge University Press, Cambridge IPCC (2014) Climate Change 2014. Impacts, adaptation, and vulnerability. Summaries, frequently asked questions, and cross-chapter boxes. In: A working group II contribution to the fifth assessment report of IPCC. Cambridge University Press, Cambridge IPCC (2022) Climate change 2022: mitigation of climate change. In: Shukla PR et al (eds) Contribution of working group III to the Sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York. https://doi. org/10.1017/9781009157926 Issa A, Esmaeel Q, Sanchez L et al (2018) Impacts of Paraburkholderia phytofirmans strain PsJN on tomato (Lycopersicon esculentum L.) under high temperature. Front Plant Sci 9:1397 Jagadish SK, Way DA, Sharkey TD (2021) Plant heat stress: concepts directing future research. Plant Cell Environ 44:1992–2005 Janzen HH (2005) Soil carbon: a measure of ecosystem response in a changing world? Can J Soil Sci 85:467–480 Janzen HH, Janzen DW, Gregorich EG (2021) The ‘soil health’ metaphor: Illuminating or illusory? Soil Biol Biochem 159:108167 Jayakumar A, Padmakumar P, Nair IC et al (2020) Drought tolerant bacterial endophytes with potential plant probiotic effects from Ananas comosus. Biologia 75:1769–1778 Jenkinson DS, Adams DE, Wild A (1991) Model estimates of CO2 emissions from soil in response to global warming. Nature 351:304–306 Jian J, Du X, Stewart RD (2020) A database for global soil health assessment. Sci Data 7:1–8 Jiang Y, Liu Y, Zhang X et al (2021) Biofilm application in the microbial biochemicals production process. Biotechnol Adv 48:107724. https://doi.org/10.1016/j.biotechadv.2021.107724 Jongdee B, Pantuwan G, Fukai S et al (2006) Improving drought tolerance in rainfed lowland rice: an example from Thailand. Agric Water Manag 80:225–240 Juroszek P, von Tiedemann A (2011) Potential strategies and future requirements for plant disease management under a changing climate. Plant Pathol 60:100–112 Kamennaya NA, Ahn SE, Park H et al (2015) Installing extra bicarbonate transporters in the cyanobacterium Synechocystis sp. PCC6803 enhances biomass production. Metab Eng 29:76– 85

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

45

Kang SM, Khan AL, Waqas M et al (2014) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682 Karlen DL, Stott DE, Stewart BA (1994) A framework for evaluating physical and chemical indicators of soil quality. In: Doran JW et al (eds) Defining soil quality for a sustainable environment, vol 34. Soil Science Society of America, Madison, WI, pp 53–72 Karlen DL, Mausbach MJ, Doran JW et al (1997) Soil quality: a concept, definition, and framework for evaluation. Soil Sci Soc Am J 61:4–10 Karlen DL, Andrews SS, Doran JW (2001) Soil quality: current concepts and applications. Adv Agron 74:1–40 Karlen DL, Doran JW, Weinhold BJ et al (2003) Soil quality: humankind’s foundation for survival. J Soil Water Conserv 58:171–179 Karlen D, Veum KS, Sudduth KA et al (2019) Soil health assessment: past accomplishments, current activities, and future opportunities. Soil Tillage Res 195:104365. https://doi.org/10. 1016/J.STILL.2019.104365 Karlen DL, Stott DE, Mikha MM et al (2021a) Soil health: an overview and goals for these volumes. In: Karlen DL et al (eds) Soil health: approaches to soil health analysis. Soil Science Society of America (SSSA), Madison, WI Karlen DL, De M, McDaniel MD et al (2021b) Evolution of the soil health movement. In: Karlen DL et al (eds) Soil health: approaches to soil health analysis, vol 1. Soil Science Society of America (SSSA), Madison, WI Kasei RA (2010) Modelling impacts of climate change on water resources in the Volta Basin, West Africa. Bonn, Dissertation, Rheinische Friedrich-Wilhelms-Universität Bonn Keesstra SD, Bouma J, Wallinga J et al (2016) The significance of soils and soil science towards realization of the United Nations Sustainable Development Goals. Soil 7:111–128 Kerchev P, van der Meer T, Sujeeth N et al (2020) Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol Adv 40:107503 Khan AL, Hamayun M, Kim YH et al (2011) Gibberellins producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, isoflavonoids production and plant growth in salinity stress. Process Biochem 6:440–447 Khan MIR, Asgher M, Khan NA (2014) Plant physiology and biochemistry alleviation of saltinduced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74 Khan MA, Kang S-M, Adhikari A et al (2022) Evaluating the adhesive potential of the newly isolated bacterial strains in research exploitation of plant microbial interaction. Front Plant Sci 13:1004331. https://doi.org/10.3389/fpls.2022.1004331 Kheirfam H, Sadeghi SH, Zarei DB et al (2017) Controlling rainfall induced soil loss from small experimental plots through inoculation of bacteria and cyanobacteria. Catena 152:40–46 Kibblewhite MG, Ritz K, Swift MJ (2008) Soil health in agricultural systems. Philos Trans R Soc B 363:685–701 King GM, Henry K (2019) Impacts of experimental flooding on microbial communities and methane fluxes in an Urban Meadow, Baton Rouge, Louisiana. Front Ecol Evol 7:288. https://doi.org/10.3389/fevo.2019.00288 Koch A, Chappell A, Eyres M et al (2015) Monitor soil degradation or triage for soil security? An Australian challenge. Sustainability 7:4870–4892 Kour D, Rana KL, Kaur T et al (2020) Microbial biofilms: functional annotation and potential applications in agriculture and allied sectors. In: Yadav MK, Singh BP (eds) New and future developments in microbial biotechnology and bioengineering: microbial biofilms. Elsevier, Amsterdam, pp 283–301 Kumar P, Sharma PK (2020) Soil salinity and food security in India. Front Sustain Food Syst 4: 533781

46

K. Velmourougane and R. Prasanna

Kumar A, Singh J (2020) Biofilms forming microbes: diversity and potential application in plant– microbe interaction and plant growth. In: Yadav AN et al (eds) Plant microbiomes for sustainable agriculture, vol 25. Springer, Cham. https://doi.org/10.1007/978-3-030-38453-1_6 Kumar A, Srivastava AK, Velmourougane K et al (2015) Urease activity and its kinetics in selected bench mark soils of Indo-Gangetic Plains. Proc Natl Acad Sci India Sect B Biol Sci 85:407–413 Kumar P, Singh S, Kumar P et al (2022) Bioinoculants as mitigators of multiple stresses: a ray of hope for agriculture in the darkness of climate change. Heliyon 8:e11269 Kuramae EE, Gamper H, van Veen JA et al (2011) Soil and plant factors driving the community of soilborne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiol Ecol 77:285–294 Kuramae EE, Yergeau E, Wong LC et al (2012) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79:12–24 Kuzyakov Y, Gavrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Chang Biol 16:3386–3406 Lake IR, Bentham G, Kovats RS et al (2005) Effects of weather and river flow on cryptosporidiosis. J Water Health 3:469–474 Lal R (2000) Soil management in the developing countries. Soil Sci 165:57–72 Lal R (2013) Climate-strategic agriculture and the water-soil-waste nexus. J Plant Nutr Soil Sci 176: 479–493 Lal R, Follett RF, Stewart BA et al (2007) Soil carbon sequestration to mitigate climate change and advance food security. Soil Sci 172:943–956 Laxa M, Liebthal M, Telman W et al (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8:94. https://doi.org/10.3390/antiox8040094 Lehmann J, Bossio DA, Kögel-Knabner I et al (2020) The concept and future prospects of soil health. Nat Rev Earth Environ 1:544–553 Lesaulnier C, Papamichail D, McCorkle S et al (2008) Elevated atmospheric CO2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10:926–941 Li J, Glick BR (2001) Transcriptional regulation of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (acdS). Can J Microbiol 47:359– 367 Li J, McConkey BJ, Cheng Z, Guo S, Glick BR (2013) Identification of plant growth-promoting bacteria-responsive proteins in cucumber roots under hypoxic stress using a proteomic approach. J Proteomics 84:119–131 Li M, Hong L, Ye W et al (2022) Phyllosphere bacterial and fungal communities vary with host species identity, plant traits and seasonality in a subtropical forest. Environ Microbiome 17:29. https://doi.org/10.1186/s40793-022-00423-3 Liebig MA, Miller ME, Varvel GE et al (2004) AEPAT: software for assessing agronomic and environmental performance of management practices in long-term agroecosystem experiments. Agron J 96:109–115 Liu J, Wu Y, Wu C et al (2017) Advanced nutrient removal from surface water by a consortium of attached microalgae and bacteria: a review. Bioresour Technol 241:1127–1137 Lobell DB, Gourdji SM (2012) The influence of climate change on global crop productivity. Plant Physiol 160:1686–1697 Lu H, Yang L, Shabbir S et al (2014) The adsorption process during inorganic phosphorus removal by cultured periphyton. Environ Sci Pollut Res 21:8782–8791 Luo YQ, Gerten D, Le Maire G et al (2008) Modeled interactive effects of precipitation, temperature, and [CO2] on ecosystem carbon and water dynamics in different climatic zones. Glob Chang Biol 14:1986–1999 Macleod CJA, Falloon PD, Evans R et al (2012) The effects of climate change on the mobilization of diffuse substances from agricultural systems. Adv Agron 115:41–77 Maitra S, Pramanick B, Dey P et al (2021) Thermotolerant soil microbes and their role in mitigation of heat stress in plants. In: Yadav AN (ed) Soil microbiomes for sustainable agriculture.

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

47

Sustainable development and biodiversity, vol 27. Springer, Cham. https://doi.org/10.1007/9783-030-73507-4_8 Mandal C, Mandal DK, Bhattacharyya T et al (2014) Revisiting agro-ecological sub-regions of India—a case study of two major food production zones. Curr Sci 107:1519–1536 Mann C (2017) A dark Laboratory: Exploring soil health perceptions and assessments in the Maritimes. Master dissertation, Dalhousie University, Halifax, Nova Scotia Maracchi G, Sirotenko O, Bindi M (2002) Impacts of present and future climate variability on agriculture and forestry in the temperate regions: Europe. In: International workshop on reducing vulnerability of agriculture and forestry to climate variability and climate change, Ljubljana, Slovenia, pp 117–135 Marchand FL, Kockelbergh F, van de Vijver B et al (2006) Are heat and cold resistance of arctic species affected by successive extreme temperature events? New Phytol 170:291–300 Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572 Mehra P, Singh BP, Kunhikrishnan A et al (2018) Soil health and climate change: a critical nexus. In: Reicosky D (ed) Managing soil health for sustainable agriculture: fundamentals, vol 1. Burleigh Dodds Science, Cambridge, pp 1–30 Mhamdi A, Van Breusegem F (2018) Reactive oxygen species in plant development. Development 145:dev164376 Miao L, Wang C, Adyel TM et al (2021) Periphytic biofilm formation on natural and artificial substrates: comparison of microbial compositions, interactions, and functions. Front Microbiol 12:684903. https://doi.org/10.3389/fmicb.2021.684903 Mir MY, Hamid S, Parray JA (2022) Phyllosphere microbiomes: implications and ecofunctional diversity. In: Gunjal A, Shinde S (eds) Microbial diversity in hotspots. Academic Press, New York, pp 81–95 Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706 Mitchell CC, Huluka G, Bosarge T (2015) Measuring soil health in Alabama. In: ASA Annual Meeting, Minneapolis, MN Mitter B, Brader G, Afzal M et al (2013) Advances in elucidating beneficial interactions between plants, soil, and bacteria. Adv Agron 121:381–445 Miura K, Tada Y (2014) Regulation of water, salinity , and cold stress responses by salicylic acid. Front Plant Sci 5:4–9 Monteith DT, Stoddard JL, Evans CD et al (2007) Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450:537–540 More TT, Yadav JSS, Yan S et al (2014) Extracellular polymeric substances of bacteria and their potential environmental applications. J Environ Manage 144:1–25 Morgan RPC (2005) Soil erosion and conservation, 3rd edn. Blackwell, Oxford Mukhtar S, Zareen M, Khaliq Z et al (2020) Phylogenetic analysis of halophyte-associated rhizobacteria and effect of halotolerant and halophilic phosphate-solubilizing biofertilizers on maize growth under salinity stress conditions. J Appl Microbiol 128:556–573 Nanney RD, Fryrear DW, Zobeck TM (1993) Wind erosion prediction and control. Water Sci Technol 28:519–527 Nascimento F, Brígido C, Alho L et al (2012) Enhanced chickpea growth-promotion ability of a Mesorhizobium strain expressing an exogenous ACC deaminase gene. Plant and Soil 353:221– 230 Nascimento FX, Rossi MJ, Glick BR (2018) Ethylene and 1-Aminocyclopropane-1-carboxylate (ACC) in plant–bacterial interactions. Front Plant Sci 9:114. https://doi.org/10.3389/fpls.2018. 00114 Nawaz MS, Arshad A, Rajput L et al (2020) Growth-stimulatory effect of quorum sensing signal molecule n-acyl homoserine lactone-producing multi-trait Aeromonas spp. on wheat genotypes under salt stress. Front Microbiol 11:553621

48

K. Velmourougane and R. Prasanna

Nayak SK, Nayak S, Patra JK (2020) Rhizobacteria and its biofilm for sustainable agriculture: a concise review. In: Yadav MK, Singh BP (eds) New and future developments in microbial biotechnology and bioengineering: microbial biofilms. Elsevier, Amsterdam, pp 165–175 Neal AL, Bacq-Labreuil A, Zhang X (2020) Soil as an extended composite phenotype of the microbial metagenome. Sci Rep 10:10649 Nearing MA, Pruski FF, O’Neal MR (2004) Expected climate change impacts on soil erosion rates: a review. J Soil Water Conserv 59:43–50 Neuman CM, Maxwell CD, Boulton JW (1996) Wind transport of sand surfaces with photoautotropic microoganisms. Catena 27:229–247 Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R et al (eds) The rhizosphere biochemistry and organic substances at the soil– plant interface, 2nd edn. CRC Press/Taylor and Francis, New York, pp 23–72 Nguyen LM, Buttner MP, Cruz P et al (2011) Effects of elevated CO2 on rhizosphere soil microbial communities in a Mojave Desert ecosystem. Arid Environ 75:917–925 Nunes MR, Veum KS, Parker PA et al (2021) The soil health assessment protocol and evaluation applied to soil organic carbon. Soil Sci Soc Am J 85:1196–1213 O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79 Oades JM (1984) Soil organic-matter and structural stability—mechanisms and implications for management. Plant and Soil 76:319–337 Ortiz-Bobea A, Ault TR, Carrillo CM et al (2021) Anthropogenic climate change has slowed global agricultural productivity growth. Nat Clim Chang 11:306–312 Osakabe Y, Osakabe K, Shinozaki K et al (2014) Response of plants to water stress. Front Plant Sci 5:86. https://doi.org/10.3389/fpls.2014.00086 Othman NMI, Othman R, Zuan ATK et al (2022) Isolation, characterization, and identification of zinc-solubilizing bacteria (ZSB) from wetland rice fields in Peninsular Malaysia. Agriculture 12: 1823. https://doi.org/10.3390/agriculture12111823 Ozturk S, Aslim B (2010) Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ Sci Pollut Res 17:595–602 Parker DL, Mihalick JE, Plude JL et al (2000) Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa f. flos-aquae strain C3-40. J Appl Phycol 12:219–224 Patil NG, Tiwary P, Bhattacharyya T et al (2014) Natural resources of the Indo-Gangetic Plains: a land-use planning perspective. Curr Sci 107:1537–1549 Pattison AB, Moody PW, Badcock KA et al (2008) Development of key soil health indicators for the Australian banana industry. Appl Soil Ecol 40:155–164 Paul MV, Iyer S, Amerhauser C et al (2016) Oxygen sensing via the ethylene response transcription factor RAP2. 12 affects plant metabolism and performance under both normoxia and hypoxia. Plant Physiol 172:141–153 Philippot L, Raaijmakers JM, Lemanceau P et al (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799 Phillips DA, Fox TC, King MD et al (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894 Plazek A, Hura K, Rapacz H et al (2001) The influence of ozone fumigation on metabolic efficiency and plant resistance to fungal pathogens. J Appl Bot 75:8–13 Polizzotto ML, Kocar BD, Benner SG et al (2008) Nearsurface wetland sediments as a source of arsenic release to ground water in Asia. Nature 454:505–508 Post WM, Kwon KC (2000) Soil carbon sequestration and land-use change: processes and potential. Glob Chang Biol 6:317–328 Powlson DS (2020) Soil health-useful terminology for communication or meaningless concept? Or both? Front Agr Sci Eng 7:246–250 Prasad PVV, Djanaguiraman M, Perumal R et al (2015) Impact of high temperature stress on floret fertility and individual grain weight of grain sorghum: sensitive stages and thresholds for temperature and duration. Front Plant Sci 6:1–11

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

49

Prasanna R, Kumar V, Kumar S et al (2002) Methane production in rice soils is inhibited by cyanobacteria. Microbiol Res 157:1–6 Prasanna R, Nain L, Tripathi R et al (2008) Evaluation of fungicidal activity of extracellular filtrates of cyanobacteria-possible role of hydrolytic enzymes. J Basic Microbiol 48:186–194 Prasanna R, Sood A, Jaiswal P et al (2010) Rediscovering cyanobacteria as valuable sources of bioactive compounds. Appl Biochem Microbiol 46:133–147 Prasanna R, Pattnayak S, Sugitha TCK et al (2011) Development of cyanobacterium-based biofilms and their in vitro evaluation for agriculturally useful traits. Folia Microbiol 56:49–58 Prasanna R, Joshi M, Rana A et al (2012) Influence of co-inoculation of bacteria-cyanobacteria on crop yield and CN sequestration in soil under rice crop. World J Microbiol Biotechnol 28:1223– 1235 Prasanna R, Kumar A, Babu S et al (2013) Deciphering the biochemical spectrum of novel cyanobacterium-based biofilms for use as inoculants. Biol Agric Hortic 29:145–158 Prasanna R, Triveni S, Bidyarani N et al (2014) Evaluating the efficacy of cyanobacterial formulations and biofilmed inoculants for leguminous crops. Arch Agron Soil Sci 60:349–366 Prasanna R, Bidyarani N, Babu S et al (2015a) Cyanobacterial inoculation elicits plant defense response and enhanced Zn mobilization in maize hybrids. Cogent Food Agric 1:998507 Prasanna R, Adak A, Verma S et al (2015b) Cyanobacterial inoculation in rice grown under flooded and SRI modes of cultivation elicits differential effects on plant growth and nutrient dynamics. Ecol Eng 84:532–541 Prasanna R, Babu S, Bidyarani N et al (2015c) Prospecting cyanobacteria-fortified composts as plant growth promoting and biocontrol agents in cotton. Exp Agric 51:42–65 Prasanna R, Kanchan A, Ramakrishnan B et al (2016a) Cyanobacteria based bioinoculants influence growth and yields by modulating the microbial communities favourably in the rhizospheres of maize hybrids. Eur J Soil Biol 75:15–23 Prasanna R, Ramakrishnan B, Ranjan K et al (2016b) Microbial inoculants with multifaceted traits suppress Rhizoctonia populations and promote plant growth in cotton. J Phytopathol 164:1030– 1042 Prasanna R, Kanchan A, Simranjit K et al (2016c) Chrysanthemum growth gains from beneficial microbial interactions and fertility improvements in soil under protected cultivation. Hortic Plant J 2:229–239 Prasanna R, Ramakrishnan B, Kaur S et al (2017) Cyanobacterial and rhizobial inoculation modulates the plant physiological attributes and nodule microbial communities of chickpea. Arch Microbiol 199:1311–1323 Prasanna R, Saxena G, Singh B et al (2018) Mode of application influences the biofertilizing efficacy of cyanobacterial biofilm formulations in chrysanthemum varieties under protected cultivation. OpenAgri 3:478–489 Prasanna R, Renuka N, Nain L (2021) Natural and constructed cyanobacteria-based consortia for enhancing crop growth and soil fertility. In: Seneviratne G, Zavahir JS (eds) Microbes for sustainability: role of microbial communities. Springer, Berlin, pp 333–362 Pritchard SG (2011) Soil organisms and global climate change. Plant Pathol 60:82–99 Qaderi MM, Kurepin LV, Reid DM (2012) Effects of temperature and watering regime on growth, gas exchange and abscisic acid content of canola (Brassica napus) seedlings. Environ Exp Bot 75:107–113 Qafoku NP (2010) Terrestrial nanoparticles and their controls on soil/geo processes and reactions. Adv Agron 107:33–91 Qafoku NP (2015) Climate-change effects on soils: accelerated weathering, soil carbon and elemental cycling. Adv Agron 131:111–172 Quinton JN, Catt JA (2007) Enrichment of heavy metals in sediment resulting from soil erosion on agricultural fields. Environ Sci Technol 41:3495–3500 Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43:1183–1191

50

K. Velmourougane and R. Prasanna

Ramadoss D, Lakkineni VK, Bose P et al (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. SpringerPlus 2:6. https://doi.org/10.1186/ 2193-1801-2-6 Ravanbakhsh M, Sasidharan R, Voesenek LA et al (2017) ACC deaminase-producing rhizosphere bacteria modulate plant responses to flooding. J Ecol 105:979–986 Ray SK, Bhattacharyya T, Reddy KR et al (2014) Soil and land quality indicators of the IndoGangetic Plains of India. Curr Sci 107:1470–1486 Raychaudhuri M, Kundu DK, Kumar A et al (2014) Soil physical quality of the Indo-Gangetic Plains and black soil region. Curr Sci 107:1440–1451 Rehman B, Hassan TU, Bano A (2019) Potential of indole-3-acetic acid-producing rhizobacteria to resist Pb toxicity in polluted soil. Soil Sediment Contam 28:101–121 Reth S, Reichstein M, Falge E (2005) The effect of soil water content, soil temperature, soil pH value and root mass on soil CO2 efflux. Plant and Soil 268:21–33 Reynolds WD, Drury CF, Tan CS et al (2009) Use of indicators and pore volume function characteristics to quantify soil physical quality. Geoderma 152:252–263 Rezayian M, Niknam V, Ebrahimzadeh H (2018) Effects of drought stress on the seedling growth, development, and metabolic activity in different cultivars of canola. Soil Sci Plant Nutr 64:360– 369 Ritz K, Black HIJ, Campbell CD et al (2009) Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecol Indic 9:1212–1221 Riva V, Terzaghi E, Vergani L et al (2019) Exploitation of rhizosphere microbiome services. In: Reinhardt D, Sharma AK (eds) Methods in rhizosphere biology research, rhizosphere biology. Springer, Berlin, pp 105–132 Rohr JR, Schotthoefer AM, Raffel TR et al (2008) Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235–1239 Ross DS, Matschonat G, Skyllberg U (2008) Cation exchange in forest soils: the need for a new perspective. Eur J Soil Sci 59:1141–1159 Rothwell JJ, Evans MG, Daniels SA et al (2008) Peat soils as a source of lead contamination to upland fluvial systems. Environ Pollut 153:582–589 Rui J, Peng J, Lu Y (2009) Succession of bacterial populations during plant residue decomposition in rice field soil. Appl Environ Microbiol 75:4879–4886 Ryan PR, Dessaux Y, Thomashow LS et al (2009) Rhizosphere engineering and management for sustainable agriculture. Plant and Soil 321:363–383 Sadeghi SH, Kheirfam H, Homaee M et al (2017) Improving runoff behavior resulting from direct inoculation of soil micro-organisms. Soil Tillage Res 171:35–41 Sandalio LM, Romero-Puertas MC, Bellin D et al (2018) Climate change and the impact of greenhouse gasses: CO2 and NO, friends and foes of plant oxidative stress. Front Plant Sci 9:273 Sandhya V, Ali SK, Minakshi G et al (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAPP45. Biol Fertil Soils 46:17–26 Santosh S, Velmourougane K, Idapuganti RG et al (2022) Potassium solubilizing potential of native bacterial isolates from cotton rhizosphere of rainfed Vertisols. Natl Acad Sci Lett:1–4. https:// doi.org/10.1007/s40009-022-01113-x Sasidharan R, Hartman S, Liu Z et al (2017) Signal dynamics and interactions during flooding stress. Plant Physiol 176:1106–1117 Sathya A, Vijayabharathi R, Gopalakrishnan S (2017) Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7: 1–10 Schindelbeck RR, van Es HM, Abawi GS et al (2008) Comprehensive assessment of soil quality for landscape and urban management. Landsc Urban Plan 88:73–80 Schnepf A, Carminati A, Ahmed MA et al (2022) Linking rhizosphere processes across scales: opinion. Plant and Soil 478:5–42

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

51

Seneviratne G, Jayasekara A, De Silva M et al (2011) Developed microbial biofilms can restore deteriorated conventional agricultural soils. Soil Biol Biochem 43:1059–1062 Shabbir S, Faheem M, Ali N et al (2017) Periphyton biofilms: A novel and natural biological system for the effective removal of sulphonated azo dye methyl orange by synergistic mechanism. Chemosphere 167:236–246 Shaffifique S, Khan MA, Imran M et al (2022a) Research progress in the field of microbial mitigation of drought stress in plants. Front Plant Sci 13:870626 Shaffifique S, Khan MA, Wani SH et al (2022b) Biopriming of maize seeds with a novel bacterial strain SH-6 to enhance drought tolerance in south Korea. Plants 11:1674 Sharma PP, Gupta SC, Foster GR (1995) Raindrop-induced soil detachment and sediment transport from interrill areas. Soil Sci Soc Am J 59:727–734 Sharma HC, Srivastava CP, Durairaj C et al (2010) Pest management in grain legumes and climate change. In: Yadav SS et al (eds) Climate change and management of cool season grain legume crops. Springer Science + Business Media, Dordrecht, pp 115–140 Sharma S, Chandra D, Sharma AK (2021) Rhizosphere plant–microbe interactions under abiotic stress. In: Gupta VVSR, Sharma AK (eds) Rhizosphere biology: interactions between microbes and plants, rhizosphere biology. Springer, Singapore, pp 195–216 Sheng X, He L, Wang Q et al (2008) Effects of inoculation of biosurfactant producing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil. J Hazard Mater 155: 17–22 Shepherd TG (2000) Field guide for cropping and pastoral grazing on flat to rolling country. In: Visual soil assessment, vol 1. Horizons.mw/Landcare Research, Palmerston North, pp 5–84 Shepherd MA, Harrison R, Webb J (2002) Managing soil organic matter-implications for soil structure on organic farms. Soil Use Manage 18:284–292 Shrestha M, Abraham WR, Shrestha PM et al (2008) Activity and composition of methanotrophic bacterial communities in planted rice soil studied by flux measurements, analyses of pmoA gene and stable isotope probing of phospholipid fatty acids. Environ Microbiol 10:400–412 Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131 Shukla PS, Mantin EG, Adil M et al (2019) Ascophyllum nodosum-based biostimulants: sustainable applications in agriculture for the stimulation of plant growth, stress tolerance, and disease management. Front Plant Sci 10:1–22 Sidhu GS, Bhattacharyya T, Sarkar D et al (2014) Impact of management levels and land-use changes on soil properties in rice–wheat cropping system of the Indo-Gangetic Plains. Curr Sci 107:1487–1501 Sierra J (1997) Temperature and soil moisture dependence of N mineralization in intact soil cores. Soil Biol Biochem 29:1557–1563 Silva LCR (2022) Expanding the scope of biogeochemical research to accelerate atmospheric carbon capture. BioGeoChem 161:19–40 Silva LCR, Wood MC, Johnson BR et al (2022) A generalizable framework for enhanced natural climate solutions. Plant and Soil 479:3–24 Singh BK, Munro S, Reid E et al (2006) Investigating microbial community structure in soils by physiological, biochemical and molecular fingerprinting methods. Eur J Soil Sci 57:72–82 Singh BP, Cowie AL, Chan KY (2011) Soil health and climate change, soil biology series 29. Springer-Verlag, Berlin Singh RP, Jha P, Jha PN (2015) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol 184:57–67 Singh M, Sarkar B, Biswas B et al (2017) Relationship between soil clay mineralogy and carbon protection capacity as influenced by temperature and moisture. Soil Biol Biochem 109:95–106 Singh R, Glick BR, Rathore D (2018) Biosurfactants as a biological tool to increase micronutrient availability in soil: a review. Pedosphere 28:170–189

52

K. Velmourougane and R. Prasanna

Sivakumar N, Sathishkumar R, Selvakumar G et al (2020) Phyllospheric microbiomes: diversity, ecological significance, and biotechnological applications. In: Yadav A et al (eds) Plant microbiomes for sustainable agriculture. Sustainable development and biodiversity, vol 25. Springer, Cham. https://doi.org/10.1007/978-3-030-38453-1_5 Smith P (2012) Soils and climate change. Curr Opin Environ Sustain 4:539–544 Smith P, Ashmore MR, Black HIJ, Burgess PJ, Evans CD, Quine TA, Thomson AM, Hicks K, Orr HG (2013) The role of ecosystems and their management in regulating climate, and soil, water and air quality. J Appl Ecol 50:812–829 Sojka RE, Upchurch DR (1999) Reservation regarding the soil quality concept. Soil Sci Soc Am J 63:1039–1054 Sole R, Duran-Nebreda S, Montanez R (2015) Synthetic circuit designs for Earth terraformation. Biol Direct 10:37 Srinivasarao C, Rao KV, Gopinath KA et al (2020) Agriculture contingency plans for managing weather aberrations and extreme climatic events: development, implementation and impacts in India. Adv Agron 159:35–91 Srivastava S, Yadav A, Seem K et al (2008) Effect of high temperature on Pseudomonas putida NBRI0987 biofilm formation and expression of stress sigma factor RpoS. Curr Microbiol 56: 453–457 Srivastava AK, Velmourougane K, Bhattacharyya T et al (2014) Impacts of agro-climates and land use systems on culturable microbial population in soils of the Indo-Gangetic Plains, India. Curr Sci 107:1464–1469 Steffan JJ, Brevik EC, Burgess LC et al (2018) The effect of soil on human health: an overview. Eur J Soil Sci 69:159–171 Stewart BA (1992) Advances in soil science. Springer-Verlag, New York Su J, Kang D, Xiang W et al (2017) Periphyton biofilm development and its role in nutrient cycling in paddy microcosms. J Soil Sediment 17:810–819 Sun P, Chen Y, Liu J et al (2022) Periphytic biofilms function as a double-edged sword influencing nitrogen cycling in paddy fields. Environ Microbiol 24:6279–6289. https://doi.org/10.1111/ 1462-2920.16277 Tabari H (2020) Climate change impact on flood and extreme precipitation increases with water availability. Sci Rep 10:1–10 Teshome DT, Zharare GE, Naidoo S (2020) The threat of the combined effect of biotic and abiotic stress factors in forestry under a changing climate. Front Plant Sci 11:601009 Thapa S, Prasanna R, Ranjan K et al (2017) Nutrients and host attributes modulate the abundance and functional traits of phyllosphere microbiome in rice. Microbiol Res 204:55–64 Thapa S, Ranjan K, Ramakrishnan B et al (2018a) Influence of fertilizers and rice cultivation methods on the abundance and diversity of phyllosphere microbiome. J Basic Microbiol 58: 172–186 Thapa S, Prasanna R, Ramakrishnan B et al (2018b) Interactive effects of Magnaporthe inoculation and nitrogen doses on the plant enzyme machinery and phyllosphere microbiome of resistant and susceptible rice cultivars. Arch Microbiol 200:1287–1305 Thapa S, Prasanna R, Ramakrishnan B et al (2021) Microbial inoculation elicited changes in phyllosphere microbial communities and host immunity suppress Magnaporthe oryzae in a susceptible rice cultivar. Physiol Mol Plant Pathol 114:101625. https://doi.org/10.1016/j.pmpp. 2021.101625 Thodsen H, Hasholt B, Kjarsgaard JH (2008) The influence of climate change on suspended sediment transport in Danish rivers. Hydrol Process 22:764–774 Thornton PK, Ericksen PJ, Herrero M et al (2014) Climate variability and vulnerability to climate change: a review. Glob Chang Biol 20:3313–3328 Tikhonovich IA, Provorov NA (2011) Microbiology is the basis of sustainable agriculture: an opinion. Ann Appl Biol 159:155–168 Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33: 141–163

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

53

Titeux N, Henle K, Jean-Baptiste M et al (2016) Biodiversity scenarios neglect future land-use changes. Glob Chang Biol 22:2505–2515 Tiwary P, Patil NG, Bhattacharyya T et al (2014) Pedotransfer functions: a tool for estimating hydraulic properties of two major soil types of India. Curr Sci 107:1431–1439 Trivedi P, He ZL, Van Nostrand JD et al (2012) Huanglongbing alters the structure and functional diversity of microbial communities associated with the citrus rhizosphere. ISME J 6:363–383 Triveni S, Prasanna R, Shukla L et al (2013) Evaluating the biochemical traits of novel Trichoderma-based biofilms for use as plant growth-promoting inoculants. Ann Microbiol 63: 1147–1156 Triveni S, Prasanna R, Kumar A et al (2015) Evaluating the promise of Trichoderma and Anabaena based biofilms as multifunctional agents in Macrophomina phaseolina-infected cotton crop. Biocontrol Sci Technol 25:656–670 UN (2015) World population projected to reach 9.7 billion by 2050. www.un.org/en/development/ desa/news/population/2015-report.html. Accessed 30 Sept 2022 Velmourougane K, Blaise D (2017) Soil health, crop productivity and sustainability challenges. In: Bhat R (ed) Sustainability challenges in the agrofood sector. Wiley, Sussex, pp 509–531 Velmourougane K, Blaise D (2021) Rhizoengineering: a strategy to enhance soil and crop productivity. In: Pudake RN et al (eds) Omics science for rhizosphere biology, rhizosphere biology. Springer, Berlin. https://doi.org/10.1007/978-981-16-0889-6_13 Velmourougane K, Prasanna R (2017) Influence of L-amino acids on aggregation and biofilm formation in Azotobacter chroococcum and Trichoderma viride. J Appl Microbiol 123:977–991 Velmourougane K, Sahu A (2013) Impact of transgenic cottons expressing cry1Ac on soil biological attributes. Plant Soil Environ 59:108–114 Velmourougane K, Venugopalan MV, Bhattacharyya T et al (2013a) Microbial biomass carbon in agro-ecological sub regions of black soil in India. Proc Natl Acad Sci India Sect B Biol Sci 84: 519–529 Velmourougane K, Venugopalan MV, Bhattacharyya T et al (2013b) Soil dehydrogenase activity in agro-ecological sub regions of black soil regions in India. Geoderma 197-198:186–192 Velmourougane K, Venugopalan MV, Bhattacharyya T et al (2013c) Urease activity in various agro-ecological sub regions of black soil regions in India. Proc Natl Acad Sci India Sect B Biol Sci 83:513–524 Velmourougane K, Venugopalan MV, Bhattacharyya T et al (2014a) Impacts of bioclimates, cropping systems, land use and management on the cultural microbial population in black soil regions of India. Curr Sci 107:1452–1463 Velmourougane K, Singh J, Nalayini P (2014b) Field assessment of transgenic cotton expressing Cry1 AC gene on selected soil biological attributes and culturable microbial diversity in deep vertisols. Cotton Res J 6:18–27 Velmourougane K, Prasanna R, Saxena AK et al (2017a) Modulation of growth media influences aggregation and biofilm formation between Azotobacter chroococcum and Trichoderma viride. Appl Biochem Microbiol 53:546–556 Velmourougane K, Prasanna R, Saxena AK (2017b) Agriculturally important microbial biofilms: present status and future prospects. J Basic Microbiol 57:548–573 Velmourougane K, Prasanna R, Singh SB et al (2017c) Sequence of inoculation influences the nature of extracellular polymeric substances and biofilm formation in Azotobacter chroococcum and Trichoderma viride. FEMS Microbiol Ecol 93. https://doi.org/10.1093/femsec/fix066 Velmourougane K, Prasanna R, Singh S et al (2017d) Modulating rhizosphere colonisation, plant growth, soil nutrient availability and plant defense enzyme activity through Trichoderma virideAzotobacter chroococcum biofilm inoculation in chickpea. Plant and Soil 421:157–174 Velmourougane K, Saxena G, Prasanna R (2017e) Plant-microbe interactions in the rhizosphere: mechanisms and their ecological benefits. In: Singh DP et al (eds) Plant-microbe interactions in agro-ecological perspectives. Microbial interactions and agro-ecological impacts, vol 2. Springer, Berlin, pp 193–219

54

K. Velmourougane and R. Prasanna

Velmourougane K, Prasanna R, Chawla G et al (2019a) Trichoderma-Azotobacter biofilm inoculation improves soil nutrient availability and plant growth in wheat and cotton. J Basic Microbiol 59:632–644 Velmourougane K, Prasanna R, Supriya P et al (2019b) Transcriptome profiling provides insights into regulatory factors involved in Trichoderma viride-Azotobacter chroococcum biofilm formation. Microbiol Res 227:126292. https://doi.org/10.1016/j.micres.2019.06.002 Velmourougane K, Manikandan A, Blaise D et al (2021) Cotton stalk compost as a substitution to farmyard manure along with mineral fertilizers and microbials enhanced Bt cotton productivity and fibre quality in rainfed Vertisols. Waste Biomass Valor 13:2847–2860. https://doi.org/10. 1007/s12649-022-01689-x Velmourougane K, Thapa S, Prasanna R (2022) Prospecting microbial biofilms as climate-smart strategies for improving plant and soil health: a review. Pedosphere 33:129–152. https://doi.org/ 10.1016/j.pedsph.2022.06.037 Venugopalan MV, Tiwary P, Ray SK et al (2014) InfoCrop-cotton simulation model - its application in land quality assessment for cotton cultivation. Curr Sci 107:1512–1518 Vergani L, Mapelli F, Zanardini E et al (2017) Phyto-rhizoremediation of polychlorinated biphenyl contaminated soils: an outlook on plant-microbe beneficial interactions. Sci Total Environ 575: 1395–1406 Veum KS, Nunes MR, Sudduth KA (2021) The future of soil health assessments: tools and strategies. In: Karlen DL (ed) Soil health series: approaches to soil health analysis, vol 1, 1st edn. Soil Science Society of America, Wiley, Madison, WI Voesenek LA, Sasidharan R (2013) Ethylene–and oxygen signalling–drive plant survival during flooding. Plant Biol 15:426–435 Wakelin SA, Colloff MJ, Harvey PR et al (2007) The effects of stubble retention and nitrogen application on soil microbial community structure and functional gene abundance under irrigated maize. FEMS Microbiol Ecol 59:661–670 Weil RR, Magdoff F (2004) Significance of soil organic matter to soil quality and health. In: Weil RR, Magdoff F (eds) Soil organic matter in sustainable agriculture. CRC, Boca Raton, pp 1–43 Williams KH, Wilkins MJ, N’Guessan AL et al (2013) Field evidence of selenium bioreduction in a uranium-contaminated aquifer. Environ Microbiol Rep 5:444–452 Wixon DL, Balser TC (2009) Complexity, climate change and soil carbon: a systems approach to microbial temperature response. Syst Res Behav Sci 26:601–620 Wood M, Litterick AM (2017) Soil health–what should the doctor order? Soil Use Manage 33:339– 345 Worrall F, Burt TP (2005) Predicting the future DOC flux from upland peat catchments. J Hydrol 300:126–139 Wu Y (2017) Periphyton: functions and application in environmental remediation. Elsevier, Amsterdam Wu B, Mu C (2019) Effects on greenhouse gas (CH4, CO2, N2O) emissions of conversion from over-mature forest to secondary forest and Korean pine plantation in northeast China. Forests 10:788 Wu T, Chellemi DO, Graham JH et al (2008) Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 55:293–310 Wu Y, Liu J, Lu H et al (2016) Periphyton: an important regulator in optimizing soil phosphorus bioavailability in paddy fields. Environ Sci Pollut Res Int 23:21377–21384 Wu Y, Liu J, Rene ER (2018) Periphytic biofilms: a promising nutrient utilization regulator in wetlands. Bioresour Technol 248:44–48 Xu R, Qafoku NP, Ranst EV et al (2016) Adsorption properties of subtropical and tropical variable charge soils: implications from climate change and biochar amendment. Adv Agron 135:1–58 Yahdjian L, Sala OE (2008) Climate change impacts on South American rangelands. Rangelands 30:34–39 Ye L, Zhao X, Bao EC et al (2020) Bio-organic fertilizer with reduced rates of chemical fertilization improves soil fertility and enhances tomato yield and quality. Sci Rep 10:177

2

Climate Change, Its Effects on Soil Health, and Role of Bioinoculants in. . .

55

Yue XL, Gao QX (2018) Contributions of natural systems and human activity to greenhouse gas emissions. Adv Clim Chang Res 9:243–252 Zandalinas SI, Mittler R, Balfagón D et al (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12 Zhang Z, Wang Y, Zhu Y et al (2022) Carbon sequestration in soil and biomass under native and non-native mangrove ecosystems. Plant and Soil 479:61–76 Zobeck TM, Halvorson AD, Wienhold B et al (2008) Comparison of two soil quality indexes to evaluate cropping systems in northern Colorado. J Soil Water Conserv 63:329–338

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Emerging Weeds Under Climate Change and Their Microbial Management Himanshu Mahawar, Apekcha Bajpai, Dasari Sreekanth, Deepak Pawar, and K. K. Barman

Abstract

By the end of this century, the forecasts for climate variables and ensuing emission projections envisage an average of 2.4–6.4 °C rise in planetary temperature. If these predictions come true, significant changes in the geographical range of cropping systems are foreseen due to harmful endemic species of weed and increased susceptibility to exotic weed incursions. Characterizing the plant– microbe interactions and associated environmental factors that cause specific weed species to be abundant, competitive, and thereby detrimental to the production of particular crops is necessary to anticipate these changes and to develop microbe management strategies for addressing them proactively. Microorganisms are among the core elements for ecosystem functioning and account for the credibility of soil health. This chapter highlights the microbe-mediated weed management strategies to provide crop plants with an edge over the competing weed species like upgrading the crop competitiveness, increasing nutrient acquisition, drought tolerance, and herbicide tolerance in crop plants under climate change scenarios. With the advancement in techniques, screening of climate resilience, C-sequestering microbes, and their further application as bio-herbicides hold potential. Keywords

Climate change · Weed management · Microbes · Bioherbicides

H. Mahawar (✉) · D. Sreekanth · D. Pawar · K. K. Barman ICAR—Directorate of Weed Research, Jabalpur, Madhya Pradesh, India e-mail: [email protected] A. Bajpai ICAR-Indian Institute of Soil Science, Bhopal, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_3

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Introduction

Climate change (increase in temperature, CO2 levels, and water scarcity) along with increasing atmospheric greenhouse gas (GHGs) has potential effects on agricultural productivity and pest dynamics. Among different pests, weeds are anticipated to respond rapidly to ever-increasing environmental CO2 levels (Patterson 1995). Concentrations of CO2 in the atmosphere increased to a record-breaking concentration of 419.05 parts per million (ppm) in 2021 (https://www.co2.earth/), and reports state that by the end of this century it could go beyond 700 ppm (IPCC 2007). By the end of the twenty-first century, the IPCC, i.e. the Inter-Governmental Panel on Climate Change, expects a rise in temperature somewhere between 1.1 °C and 6.4 °C (IPCC 2007). Given the need to reduce the impact of farming and human activities on the environment, and their potential to contribute to climate change, it is getting harder to increase or even sustain crop yields. However, the problems are getting intensified beyond higher temperature or concentration of greenhouse gases in the environment, as it creates a hostile environment for the weed species to proliferate more rapidly. Among the various pests, genetic adaptability, and physicochemical flexibility, weeds are able to survive and thrive in various situations and adapt quickly to resource fluctuations. The changing climatic conditions will probably boost weed competitiveness (Miri et al. 2012), resulting in a high yield drop by unfitting weed management practices (Valerio et al. 2013). The microflora can be considered as the engineer of soil and ecological activities relating to terrestrial ecosystems, including plant growth, potable water preservation, and carbon sequestration, in addition to those that are intimately dependent on microbial activities and their functional traits. According to Sangakkara et al. (2014), microbial inoculants boost soil respiration, organic carbon, nitrogen, and potassium levels. As a result, they may be an efficient way to improve the soil’s fertility and quality in impoverished areas. This chapter deals with how microbes will behave under changing climatic conditions and microbe-mediated management of weeds.

3.2

Weeds’ Effect on Agriculture Production

Weeds are noxious species of plants that are especially well-suited to infiltrate and, in many cases, dominate an environment by developing a sizable population. In addition to having large ecological amplitudes, weeds have unique biological traits that allow them to thrive in a plethora of challenging environmental conditions in disturbed habitats like crop fields. These traits include competitiveness, aggression, plasticity, and high fertility (Chandrasena 2009). In contrast to other crop pests, weeds drastically reduce agricultural yields by competing with crops for finite resources like nutrients and water. (Ramesh et al. 2017). Weeds are also known to have a deleterious influence on rangelands, along with reducing crop (Smith et al. 1987), forest ecosystems (Webster et al. 2006), and ecological mechanics besides diversity species (Pejchar and Mooney 2009).

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Therefore, efficient weed management and control are essential to maintain crop productivity.

3.2.1

Ecology and Biology of Weeds

Certain ineffective weeds may predominate weed richness due to climate change (Bazzaz and Carlson 1984). Besides geographic distribution, climatic change may impact the species population biology (Ziska and Goins 2006), enabling them to relocate to unfamiliar regions at greater latitudes and altitudes (Ziska and Dukes 2011). Due to climate change, Striga spp. will probably extend its range geographically (Mohamed et al. 2006). It is projected that a complex stand of weeds in a cultivated region will undergo dynamics in uprising and modifications in weed population (Das et al. 2012). Investigating the range extension of invasive and arable weeds in response to climate change is vital for understanding crop–weed interactions. Opportunistic weed species may be possible to perceive climatic change due to their complex dissemination and better adaptability (Bergmann et al. 2010). Once established, weeds persist in preserving their new environment (Smith et al. 2012). Due to natural selection, range shifts are typically accompanied by genetic and evolutionary adaptations to the suitable climate (Richardson et al. 2013). Arable crops and pastures will grow slowly due to a lack of precipitation and a prolonged drought, leaving bare land and enabling extra hardy, drought-tolerant weeds to invade. Furthermore, it is necessary to take into account how elevated CO2 affects the spatial extent of weeds in managed ecosystems (McDonald et al. 2009). Weeds are opportunist invasive species or the precursors of subsequent succession that are best equipped to thrive when disturbances caused by human actions or natural occurrences have created fresh habitat. Due to their competitiveness, adaptability, high fecundity, and capacity to endure diverse environmental circumstances, particularly those in damaged ecosystems or agricultural fields, certain species have the possibility to become weeds. Weeds can generate large populations, colonize disturbed habitats, and occasionally take over landscapes due to a mixture of shared biological traits (Baker 1965). A species, however, may only spread across a landscape if a unique set of circumstances renders its characteristics, particularly beneficial to its expansion and persistence. This possibility typically manifests as a result of a lack of certain herbivores or parasites, or natural enemies, giving them an edge over native plants or crops (Naylor and Lutman 2002). Because of their enormous reproduction rates and the extensive choice of habitats they can occupy, most weeds have a high rate of evolutionary success or the continuation of a genetic line across duration. Therefore, regarding the Darwinian concept of “struggle for existence”, weeds are the group of plants that have progressed most successfully on our planet (Auld 2004).

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Weed Invasion

Many weed species spread out of their native range to new locations through human activity or natural processes, which adversely impact native species of the agricultural region (Mack et al. 2000). According to several surveys, 10% of newly imported species are invasive in their changing environments, posing a serious threat to habitats and their biological diversity (Kathiresan and Gualbert 2016). It is anticipated that weeds will have an opportunity to invade new ecosystems due to climate change. Climate change is anticipated to make invasive plants more adaptable to their expanded host range and raise the menace of invasion in native and protected ecosystems (Hellmann et al. 2008) and well adapted to new habitats and more successful in utilizing resources under high CO2 concentrations (Singh et al. 2016). Genetic variability, various biotic and abiotic, or environmental conditions influence the invasiveness of a plant species. Among other things, genetic variables affect the photosynthetic pathway, the development and spreading of propagules, the dormancy of seeds, the lifetime of seed banks, and herbivore tolerance. In contrast, climatic conditions include temperature, CO2 concentration, precipitation, and other things (Kathiresan and Gualbert 2016). A species that is normally benign may develop invasive traits and have a high likelihood of spreading worldwide and remarkably influence agricultural productivity due to interactions between climate change and management approaches (Irmaileh 2011). Evidence suggests that weeds can adapt rapidly to elevated CO2 enrichment, which may promote plant invasiveness. As a result of increased seed production during the hot summer months, Singh and Singh (2010) noticed Parthenium hysterophorus L. covering a large area of fallow agricultural land throughout the summer. Therefore, temperature intensification may promote weed propagation and encourage the spread of invasive weeds into new regions (Singh et al. 2011). Several studies suggest that invasive species may or may not benefit from a new habitat brought about by climate change, mainly when enhanced resource consumption capacity is inconsistent with increasing temperature, CO2 levels, and precipitation (Bradley et al. 2010). Conversely, increasing CO2 concentrations alone has been confirmed to intensify the risk of invasiveness. In the light of the various concurrent changes in climatic variables, including CO2, temperature, and precipitation, calculating the threat of plant invasiveness is challenging. To address this problem, it will be beneficial to comprehend the mechanisms that lead weeds to colonize new areas successfully.

3.2.3

Factors Affecting Weed Emergence and Growth

Two environmental variables that encourage germination have been noticed that involve light signals are as follows: (1) agriculture operations disturb the soil and (2) the gaps in compact canopies. In certain weeds, the seeds emerge from dormancy after being subjected to temperature variations. Nine diurnal temperature cycles are assumed to affect development. These are number of cycles, magnitude, high and

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low temperatures, time spent in each condition, rate of heating and chilling, and duration of the cycles concerning the commencement of imbibition. The breakdown of the dormancy effect in Chenopodium album can rise from just 2.4 °C to 15 °C (Murdoch et al. 1989). Texas weed (Caperonia palustris) seed germination was limited by saturated soil moisture or flooding, and temperatures that range from 30 and 40 °C were stated to be appropriate for germination (Koger et al. 2004). The germination of P. hysterophorus seeds is negatively impacted by soil moisture levels of 60% or below and by monthly usual temperatures of >34 °C (Kathiresan et al. 2005). One of the main components contributing to the invasive field sheath of T. portulacastrum has been identified to be the removal of seed dormancy due to concentrated heat waves and thermo-induction of seed germination, which results in mass or synchronized weed germination and formation (Kathiresan 2006). Its dense germination and increased seedling appearance from June to August were caused by rising soil temperatures brought on by rising atmospheric temperatures beginning in the summer season (April, May, and June) when the temperature reached 35 °C. According to a study, Solanum nigrum can germinate effectively at a neutral pH (Suthar et al. 2009). Flooding of agri-ecosystem was seen to suppress the germination of old corn weed seeds, but it was also seen to encourage the germination of new seeds (Oyewole and Ibikunle 2010).

3.3

Weeds in Changing Climate

3.3.1

Factors Influencing Climatic Variations

Changes in climatic conditions (upsurge in CO2 concentrations and temperatures and famines) along with greenhouse gas (GHGs) production are becoming a significant concern over possible impacts on agricultural sustainability and pest dynamics. Changes in core climatic parameters like temperature and rainfall patterns, and meteorological elements, including CO2 and UV solar irradiance, can shift present species’ distribution (Garrett et al. 2006). These climatic variations have been linked to floods, drought, hunger, agricultural catastrophes, trends of certain pathogen infections, and population changes (Parmesan 2006). Concentrations of CO2 in the atmosphere increased at a record-breaking speed of 419.05 parts per million (ppm) in 2021 (https://www.co2.earth/). This rise is going to enhance in the upcoming days and reports state that it could exceed 600 ppm (Schimel et al. 1995), while the IPCC also proposed a conventional prediction of 700 ppm by the conclusion of the twentyfirst century. Temperatures are predicted to have risen by 0.1 to 0.3 °C per decade worldwide, as per the long-term warming patterns since pre-industrial times. Among different pests, weeds are expected to respond directly to the eCO2 levels in the earth’s atmosphere (Patterson 1995). Climate change is likely to cause differential crops in addition to weed growth, which could have greater consequences for agricultural production and weed control. eCO2 concentrations, temperature levels, and shifts are proposed to have primary (CO2-induced growth) and secondary (climatic variability) impacts on the weed population. A

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comprehensive understanding of the potential interfaces between weed population and major crops in view of the changes in climatic conditions, especially eCO2, elevated temperatures, and drought, is important for evaluating the amenability of crop production (Valerio et al. 2013).

3.3.2

Impacts of Climatic Variabilities on Weed Physiology

Weeds are genetically diverse and physiologically more flexible than crops. Thus, weeds adapt rapidly to alterations in resource availability and have a stronger capacity to live and flourish in various environments. Changes in climate factors are proposed to escalate weed competitiveness, resulting in larger output losses if weed control is not properly implemented (Valerio et al. 2013). Climate alterations are supposed to alter crop–weed–pest interactions and agricultural livestock systems, directly affecting crop growth and productivity. Generally, C3 and C4 plants react differently to eCO2 and raised temperature levels. At eCO2, carboxylation of ribulose bisphosphate (RuBP; initial acceptor of CO2) is promoted in C3 plants. Once temperatures intensify beyond 25 °C, RuBP oxygenation is preferred, increasing photorespiration and inhibiting CO2 assimilation. The temperature does not influence C4 plants because decreased photorespiration rates are always maintained due to CO2 pumps in mesophyll cells. Because of these distinctions in the CO2 fixation mechanisms, C3 plants have a strong capacity to react positively to high CO2; however, C4 crops are well-suited to heat stress and drought (Morgan et al. 2001). Weeds have the edge over crops (mainly C3) under increasing temperatures and drought conditions, as most weeds possess a C4 photosynthetic pathway. Furthermore, the potential consequences of climatic variations on weed population and crops—such as moisture, eCO2, and temperature patterns—allow weeds to perform successfully and flourish even under unfavourable circumstances (Hartfield et al. 2011). Accordingly, eCO2 and high temperatures can have major consequences for crop–weed interactions, necessitating further attention. Instances of droughts, floods, heat stress, and freezing menaces will increase with climatic variabilities, which can have a detrimental influence on agricultural output. Climate change, particularly increased CO2 levels, will have a favourable impact on the yield and quality of several C3 crops (like wheat, rice, barley, and soybean). By 2050, eCO2 levels are assumed to improve food yields by up to 13% (Jaggard et al. 2010). However, the benefits of CO2 enrichment on growth and production are negated by the adverse impacts of concomitant temperature rises for most food crops (Prasad et al. 2005). eCO2 levels, on the contrary, cause partial closure of stomata resulting in a rise of plant tissue temperature, which might have a detrimental impact on plant growth and output. Different climate change-related concerns, such as irregular rainfall patterns and high temperatures, may impair agricultural output and quality (Kadam et al. 2014).

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Impacts of Climatic Variabilities on Crop Production

The earth’s population is forecasted to exceed 9.7 billion in 2050, increasing the strain upon agriculture to satisfy expanding food requirements, which are already impacted by climate change’s adverse effects. Climatic variations are anticipated to result in altered crop plants and weed growth, which might severely affect the productivity of agriculture and weed control. According to predictions, the consequences of global warming on crop–weed interplay will vary depending on the location and cropping practices. It is hypothesized that CO2 concentration and temperature changes have both primary (CO2-induced growth) and secondary (climatic variability) impacts on weeds, affecting crop–weed interactions or promoting weed invasion. A wider idea of the potential crop–weed interactions in climatic variations, especially eCO2, raised temperatures, and drought, is vital for evaluating the vulnerability of agriculture at the global level (Valerio et al. 2013).

3.3.4

Impacts of Climatic Variabilities on Crop–Weed Interaction

Worldwide range extensions, alterations in reproductive life cycles, and especially alterations in weed species flora population demographics are all potential concerns of climatic variabilities.

3.3.4.1 Impacts of Elevated CO2 on Crop–Weed Interaction Raised concentrations of CO2 had a remarkable impact on biomass accumulation and yield of various crop plants (Sage 1995). Reaction to high CO2 in plants varies due to differential photosynthetic pathways (C3/C4). Predicting the impacts of raised CO2 levels on crop–weed interaction in an isolated environment leads to inadequate quantification of crop–weed interaction, as it is very rare to see a single-weed plant infested in a field (Ziska and Goins 2006). The interaction between crops and weeds towards increased CO2 levels has been quantified in a limited number of studies (Ziska and George 2004; Ziska and Goins 2006), and further work with combined crop plants and their associated weed species is urgently needed. Greater photosynthetic rates in C3 plants (rice, wheat, soybean, etc.) were high under enhanced CO2 than the C4 weeds palmer amaranth (A. palmeri), water hemp (Amaranthus rudis), kochia (K. scoparia), etc. (Elmore and Paul 1983). In the case of C3 crop plants like rice and wheat, high CO2 with C4 weeds can benefit crop competitiveness (Yin and Struik 2008). Phalaris minor was, however, more competitive at eCO2 conditions over wheat under drought (Naidu and Varshney 2011). Under eCO2 conditions, the relative crop production and productivity of C3 plants, soy lamb and lamb quarters are considerably more than C4 plants, millet, and pigweeds (Hamid et al. 2012). However, Ziska et al. (2010) observed higher growth and production of seeds of weedy rice compared to rice grown at eCO2, which suggests a decrease in the yield of cultivated rice in future CO2 concentrations by the interference of C3 weeds. C3 weeds like C. album, A. theophrasti, Ambrosia artemisiifolia, and Ambrosia trifida will perform further constructively to increased

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CO2 levels and offer more competition to C4 crops (maize, sorghum, sugarcane, etc.). Also, there was no improvement in the biomass of Amaranthus retroflexus at raised CO2, and the yield of soybean fell from 45% to 30% (Ziska et al. 2010).

3.3.4.2 Impacts of Elevated Temperature on Crop–Weed Interaction High temperatures favour vegetation possessing C4 photosynthetic systems, which are primarily weed species, over agricultural plants that follow the more prevalent C3 route (Yin and Struik 2008). It is observed that a 3 °C rise in the atmospheric temperature can cause a significant enhancement in the biomass of Rottboellia cochinchinensis, a major weed in various cropping systems (Patterson et al. 1999). C4 weed species like red root pigweed Amaranthus retroflexus and Sorghum halepense are anticipated to fix CO2 at a greater rate than C3 crops like soybean and cotton around noon when light intensity and temperature both reach peak levels. Because high temperatures increase evaporative demand, plants possessing C4 photosynthetic pathways are well-suited to temperatures because of their better adaptability. With CO2 doubling, Ziska and Bunce (1997) found that weedy C4 species stimulate photosynthesis and biomass more than C4 crop species. At the early growth stage, a major portion of the leaves performs the C3 pathway of photosynthesis and, therefore, gets benefitted at eCO2. In warmer situations, Setaria viridis weed germinates in later-half of the season in the month of August (Dekker 2003). This was an advantageous spatial non-synchrony towards maize, which prevented crop–weed competition. 3.3.4.3 Combined Impacts of Enhanced CO2 and Temperature on Crop– Weed Interaction The impact of raised CO2 concentrations and temperatures was studied on winter maize and its weed species Phalaris minor and Chenopodium album. The results suggested that raised CO2 levels alone and in combination with the raised temperatures showed a positive response on overall performance of maize and C. album and P. minor (DWR 2017–2018). Similarly, raised CO2 concentration and temperature positively affected soybean and its major weeds E. colona and I. rugosum (DWR 2018–2019). Plant height and leaf area were greatly enhanced in Alternanthera paronychioides (C3) and Leptochloa chinensis (C4) at raised CO2 concentrations and temperature conditions (DWR 2020–2021). 3.3.4.4 Impacts of Drought on Crop–Weed Interaction Drought and arid conditions favour the growth of C4 weeds owing to their strong internal physiological mechanisms. Patterson et al. (1988), observed that in famine circumstances, Abutilon theophrasti and Anoda cristata became more competitive towards cotton crops. Relative to moisture-stressed soybean crops, the yield drop caused by Xanthium strumarium was far more evident in well-watered crops (Mortensen and Coble 1989). Wheat yield and production faced more pressure with C. arvense due to a rise in precipitation (Donald and Khan 1992). However, scarce information is available in this area. Therefore, there is an exigent necessity to explore this aspect to cope with the upcoming climate change challenges.

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Impacts of Climatic Variations on the Effectiveness of Weedicides

Weedicides are the most common means to manage weed species for attaining sustainable agricultural output. It is already reported that eCO2 levels and enhanced temperatures can change the efficacy of herbicides (Varanasi et al. 2016). For instance, eCO2-induced weed growth could lower the time at the sapling phase, which is the important and sensitive stage of herbicide action. Herbicide assimilation also declined due to CO2-induced stomatal conductance. However, elevated temperatures enhance the effectivity of herbicides due to the speedy assimilation and translocation of foliage herbicides application. However, this leads to quick catabolism, ultimately reducing the herbicide’s effectivity on weed plants (Johnson and Young 2002). It is suggested that eCO2 and raised temperature could modify the structure of plant leaves and morphology by enhancing thickness and altering the viscidness of cuticular wax deposition, which causes a decrease in herbicide effectiveness (Ziska and Bunce 2006). The effectiveness of herbicides is affected by environmental parameters like temperature, precipitation, wind and moisture levels (Archambault et al. 2001). Most herbicides need optimum temperature (function) for their operation, but the effectiveness and selectivity can be disturbed by prolonged high temperatures after application (pre-plant pre- and post-emerging herbicides), which means selective herbicides may become non-selective at high temperatures. Earlier experiments have observed a reduced effectivity of herbicides at eCO2 (Ziska and Teasdale 2000), but some studies proposed that CO2 enhances the accumulation of biomass in some weeds (C3), and plants can develop immunity that can withstand or detoxify mechanisms (high volume of tissue). It has been observed that in Canada thistle monoculture at field situations showed a better root:shoot ratio and succeeding glyphosate dilution influence under CO2 (Ziska and George 2004). The studies found that CO2 decreases herbicide efficacy. However, more research is required to establish the herbicide specificity, concentration, and levels of application as potential means of adaptation.

3.3.5.1 Effect of Elevated CO2 on Effectiveness of Weedicides The elevated CO2 levels cause morpho-physiological alterations in plants, which impacts the level of herbicide assimilation and translocation, thereby reducing the herbicide’s effectiveness (Manea et al. 2011). Archambault et al. (2001) found that eCO2 decreased the effectiveness of the commonly used herbicide glyphosate. The total stomatal density and their conductivity were also reduced in C3 plants; nonetheless, leaf thickness increased, perhaps interfering with herbicide foliar assimilation (Nowak et al. 2004). The root/shoot ratio enhancement is also necessary for herbicide effectiveness (Ziska and George 2004). Higher root biomass accumulation caused by increasing CO2 can make perennial weed plants harder to manage. Therefore, more studies need to be conducted to compare and explore the performance and physiological reactions of various C3 and C4 weed species of various

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ages and their genotypic and physiological underpinnings for the development of resistance towards herbicides at raised CO2 concentrations.

3.3.5.2 Impact of Elevated Temperature on the Effectiveness of Weedicides It is reported that with an upsurge in temperature, some herbicides, like trifluralin volatilization, are enhanced, thereby reducing their effectiveness (Beestman and Deming 1974). However, the efficacy of acifluorfen showed a greater influence of moisture level on their effectiveness on X. strumarium and A. artemisiifolia (Ritter and Coble 1981). Also, for herbicides classified as imidazolinone, sulfonanilide, and sulphonylurea categories the degradation was significantly decreased owing to the rise in the temperatures of soil (Mcdowell et al. 1997). Sharma and Singh 2001, observed that glyphosate herbicide assimilation varies with fluctuations in temperature. It is also reported that the upsurge in moisture levels and temperatures enhanced the effectivity of mesotrione herbicide on X. strumarium and A. theophrasti weeds by threefold (Johnson and Young 2002). 3.3.5.3 Impact of Drought on the Effectiveness of Weedicides Weeds under moisture stress can react by thickening their leaf cuticles, slowing down vegetative growth, and can quickly flower. Weeds growing under drought stress are more problematic to control using post-emergence herbicide application than weeds growing nicely under well-watered conditions. It is due to the requirement of active systemic translocation of systemic weedicides to be more effective. For intake of the pre-emergence herbicides by the plant, roots require soil moisture to enter their target sites and effectively grow roots. Drought incidence can lessen the effectiveness of pre-emergent weedicides (Singh et al. 2011). Owing to the reaction towards moisture stress, enhanced cuticle accumulation can also decrease the weedicide penetration into foliage (Patterson 1995). Increased droughts and dryness would boost weedicide volatilization, whereas regular downpours would shorten the “rain-safe intervals” allowed for applying herbicides in a particular agricultural system, creating a variety of problems for weed control. Unusually high precipitation amounts might encourage the leaching of weedicides used in soil applications, which would lead to groundwater pollution.

3.3.6

Impact of Drought on Weed Flora Shift

Determining the variables indicating invasive alien plants (IAPs) appropriate ecosystems and how these are impacted by global warming is critical for implementing efforts to control the invasion of IAPs. The spread of native and introduced IAPs has been anticipated to be impacted by the temperature extremes and unusual rainfall patterns at global levels (IPCC 2018), and the overall temperature increase is supposed to be accountable for latitudinal and altitudinal shifts in certain weed species’ geological variations (Imholt et al. 2010). Various initiatives, including advance warning prediction, stronger biocontrol, and database

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construction, need to be implemented to manage the intrusion of alien species to manage the escalating biological invasion of IAPs. The list of emerging weeds under climatic variations and their invasive behaviour is given in Table 3.1. The increasing occurrence of woody vines in forests worldwide due to an increment in CO2 levels is linked to higher tree mortality and impaired tree regeneration (Phillips et al. 2005). Preliminary findings revealed that many weeds were more tolerant of cooler conditions at increased CO2 concentration (Boese et al. 1997), indicating that numerous weeds may expand poleward (Ziska and Dukes 2011). The dissemination of P. hysterophorus is linked to its higher acclimatization towards climate change conditions, particularly high CO2 levels (Naidu 2013).

3.4

Microbial Resilience to Changing Climate

Enormous data on climate change are available involving abiotic factors like heat stress, radiation stress, increase in water level and precipitation, and their global impact on planet Earth, but how microbes get impacted by them and their resilience strategy regarding climate change remains an intriguing topic among the scientific community, however, warrants further streamlined research. Being an important component of ecosystem, impact of climate change on agriculture system necessitates microbial studies pertaining to crop production, soil health, and disease and weed control. As microbes are pervasive in nature and regulate the biogeochemical cycles, they can have either good or bad feedback on climate-resilient systems. Therefore, microorganisms, particularly plant-associated microbes, exhibit enormous potential in agro-practices. The mechanistic understanding involved to mitigate changes occurring due to climatic variables is discussed below.

3.4.1

Microbial Physiological Alterations

The frequently changing climatic circumstances have evolved various physiological adaptations in microbes to sustain themselves under stressed environment. Selective physiological adaptation in thermal environment is more common and also in areas undergoing climatic changes at a faster pace. Research indicated that smaller volume of fungal spores was connected with higher temperatures, whereas larger spore volumes were linked to higher humidity (Andrew et al. 2016). High humidity favoured species that have veined hymenial layer, e.g. Cantharellus and Craterellus. Heat stress, another climatic variable, promotes hyphal branching, lateral expansion rate, and hyphal penetration, leading to altered fungal morphology (A'Bear et al. 2012). The time of spore formation is impacted by even a little shift of 0.2 °C in average yearly temperature, which can have negative effect on fungal reproduction timing, subsequently their survival rate (Andrew et al. 2016). Heat stress is increasing the fungal diversity in warmer regions as they adapt to develop thermal resistance and their ability to adapt makes them a potential candidate to be explored for weed management under changing climate. As evidenced by mushroom

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Table 3.1 List of emerging weeds under climatic variations and their invasive behaviour Sr. no. 1.

Weed Parthenium hysterophorus

Climate change parameter eCO2

Elevated temperature

2.

Woody vines (Lianas)

eCO2

3.

Ischaemum rugosum

4.

Striga spp.

5.

Orobanche spp.

6.

8.

Dactyloctenium aegyptium, Eleusine indica, Leptochloa chinensis Ageratum conyzoides; Praxelis clematidea; Solidago canadensis; Anredera cordifolia; Lantana camara; Conyza sumatrensis; Chenopodium ambrosioides; Parthenium hysterophorus; Avena fatua; Pharbitis purpurea; Aster subulatus Centaurea maculosa

Elevated temperature Drought stress Drought stress Drought stress

9.

Datura stramonium

7.

Invasive behaviour Increased root and shoot biomass, plant height, number of branches, number of leaves, total leaf area, Net photosynthesis, water use efficiency, seed production; decreased stomatal density; transpiration rate Shortening life cycle, stomatal closure; rosette growth stage under elevated temperature; resource efficiency and energy-efficient partially developed Kranz anatomy Higher tree mortality and impaired tree regeneration Higher abiotic stress tolerance Higher abiotic stress tolerance Higher abiotic stress tolerance Higher abiotic stress tolerance

Reference Mao et al. (2021)

Bajwa et al. (2017) and Kaur et al. (2017)

Changing climate set-up

Higher abiotic stress tolerance

Phillips et al. (2005) Mahajan et al. (2012) Mohamed et al. (2006) Mohamed et al. (2006) Chauhan et al. (2014) and Matloob et al. (2015) Guan et al. (2020)

Changing climate set-up Changing climate set-up

Higher abiotic stress tolerance

Broennimann et al. (2007)

Production of heavy seeds, shortening life cycle

Warwick (1990) (continued)

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Table 3.1 (continued) Sr. no. 10.

Weed Hypericum perforatum

11.

Echinochloa crus-galli

12.

Panicum miliaceum

13.

Setaria faberi

14.

Setaria viridis

15.

Sorghum halepense

Climate change parameter Changing climate set-up Changing climate set-up Changing climate set-up Changing climate set-up Changing climate set-up Changing climate set-up

Invasive behaviour Larger leaf size

Reference Maron et al. (2004)

Shortening life cycle

Potvin (1986)

Higher seed germination and seed dispersal

Bourchier and Van Hezewijk (2010) Warwick et al. (1987)

Shortening life cycle

Higher abiotic stress tolerance

Swanton et al. (1999)

Annual life cycle instead of perennial

Warwick et al. (1986)

assemblages that grow noticeably darker by amassing melanin in regions with cold conditions, the physiological adaptations aid in their reproductive success (Krah et al. 2019). Another example of reproduction success is Neurospora, which exhibits adapted strains that produce more energetically intensive spores per unit biomass and greater mass-specific respiration while maintaining the same mycelial growth rate and biomass (Romero-Olivares et al. 2015). Climate change implies enormous selection pressure on fungi, as exhibited by Ophiocordyceps kimflemingiae (zombie ant fungus) and their potential to adjust with environmental variations. Carpenter ants are infected by this fungus without their brains getting affected, and while they consume insects for food, they also regulate their behaviour of biting trees (de Bekker et al. 2015). Another striking example is lichens, which are good source of metabolites but are also highly susceptible to varying climatic conditions. In the Arctic and Alpine areas, where vascular plants currently predominate to a large extent, lichens are experiencing population decline. To counteract this amid dry spells and to retain more water under pressure, they modify their morphology by increasing mass per area. Migration or switching photosynthetic partners is another feature common in lichens under drought (Larsson et al. 2012). These protective adaptations in the light of changing climate scenarios could make them potential candidates for the management of weed infestation.

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Microbial-Mediated Plant Physiological Alterations

Plants are in direct contact of external environment and are highly vulnerable to climate change. Plant-associated microbes under abiotic stress alter plant physiology and impart their resistance against harsh environmental conditions. The ability of microbes to thrive under high-temperature variations and modulate plant growth has been studied, wherein the microbiome with thermal origins has been reported to induce the plant heat shock response by enhancing Hsp70 and jasmonic acid production in Sphagnum, which regulates evapotranspiration (Carrell et al. 2022). Phytohormones secreted by microbes or plants act as an elicitor to control plant physiology in such a way that it confers resistance against heat or water stress. Plant hormones like auxins, brassinosteroids, abscisic acids, cytokinins, ethylene, jasmonate, and salicylic acids, released by microorganisms, are also known to control plant defences against thermal stress by modulating stomatal conductance (Li et al. 2021). In particular, abscisic acid imparts heat tolerance by increasing reactive oxygen species, expression of plant NADPH oxidases, and level of carbohydrates to induce thermal tolerance in plants (Santiago and Sharkey 2019). Moreover, phytohormones are endogenous signals required in minor quantity to manage the plant physiological responses and are fundamentally essential for the development and growth of the plants (Li et al. 2021). Rhizosphere bacteria modulate the plant root morphology and deposit chemicals like suberin and callose in the cell wall that protects plant against allelopathic effects of invasive weeds (Cheng et al. 2017). Microbes also promote lateral root formation via volatile compounds secreted by spores of mycorrhizal fungi in Lotus japonicus. Such altered architecture of roots leads to variation in infection sites by parasitic weeds (Sun et al. 2015). Another advantage associated with improvement in root architecture is nutrient allocation; the competition between weeds and plant lowers the chances of survival of plant improves.

3.4.3

Metabolite-Mediated Plant: Microbe Interaction

Under abiotic stress condition, the association of plants with microbes provides them with the chance of survival by altering their root architecture, selectively recruiting beneficial microbes through root exudates. The increase in temperature has a direct impact on soil respiration rates and microbial abundance, resulting in accelerated metabolic activity. However, studies also revealed an increase in pathogenicity under heat stress. Secondary metabolites secreted by microbes are crucial for the two-way plant–microbe interaction. For instance, secretion of glycerol-3-phosphate from plant roots under drought condition selectively recruits Actinobacterial population in root zone that can utilize glycerol-3-phosphate and transport moisture to water-stressed plants (Xu et al. 2018). Similarly, reduction in iron also causes reduced availability of iron in the rhizosphere and Actinobacteria that can inhabit in iron-deficient soil improve both plant performance and soil health (Xu et al. 2021). Water stress can alter the phyllosphere’s microbial communities, triggering them to

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activate stomata’s hydraulic stimulation apparatus, thus improving foliar uptake of water (Vigani et al. 2019). Endophytes also take part in this process by increasing stomatal conductance, while bacteria can regulate opening and closing of stomata (Friesen et al. 2011). A selected category of methylotrophs contains carotenoid in their cell membrane that protect plants from increased UV radiations due to climate change by acting as a sunscreen over exposed plant surfaces (Bajpai et al. 2022). These studies suggest that the microbes associated with plants offer a lot of prospects to strengthen plants’ resistance to drought stress in future (Xu et al. 2021). Microbes without being in physical contact with plant can alter their growth, hormonal regulation, root development, and physiology through root-mediated volatiles (Schulz-Bohm et al. 2017). Under water-stressed conditions, Bacillus and Klebsiella are drawn to the endosphere and rhizosphere of pepper plant roots, respectively, improving the root architecture to boost uptake of water and photosynthetic efficiency in plants (Marasco et al. 2012). Interestingly, even at molecular level plant root vacuolar proton pumps are over-expressed under drought conditions and especially over-expression of H+-PPase type vacuolar proton pump in pepper roots is under the control of endophytic microbes by secreting biosurfactant and different volatiles (Vigani et al. 2019). This suggests that microbes and plants share intricate molecular networking and fine-tuning that confers stress tolerance to changing climate.

3.4.4

Metabolite-Mediated Microbe: Microbe Interaction

Microbe–microbe interaction is carried out mainly by a process called quorum sensing. N-acyl homoserine lactone (AHL) is synthesized by bacteria that act as signalling molecule for communication within microbial community (Fuqua et al. 2001). Apart from AHL, several other molecules secreted by Gram-negative bacteria, such as pyrones, dialkylresorcinols, and diffusible signal factors, play a significant part in influencing the rhizosphere microbial community. Proteobacteria share a major portion of bacterial population in rhizosphere and the AHL as the main signal is released by them for interkingdom communication. Major rhizo-bacterial genera like Pseudomonas, Bacillus, Ralstonia, and Burkholderia possess the capacity to produce AHLs. Volatile organic compounds (VOCs), a class of small molecular weight metabolites that includes alkenes, alcohols, terpenes, and ketones, are also responsible for communication at the inter- and intra-species levels (Schulz-Bohm et al. 2017). Both the bacteria and fungi have been reported to produce these volatile compounds with significant role in long-distance communications. Microbes that show tolerance towards climatic variation and secrete volatiles could serve as potential antimicrobial agents under those conditions (Rajer et al. 2017). They aid in both inter- and intra-species signalling, to coordinate gene expression during formation of biofilms. For example, the volatiles secreted by Pseudomonas, 1-methyl naphthalene and benzothiazole, have been reported to exhibit bacteriostatic effects against Ralstonia solanacearum in tomato crop (Raza et al. 2016). VOCs also control stress resistance and plant development and plant gene transcription involved

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in defence against pathogens. VOCs thus provide resistance to stress and aid in plant development by regulating the transcription of plant genes involved in defence against pathogens. Compounds like 2, 3-butanediol and acetoin trigger the synthesis of virulence factor in other microbes, making them probable agents to exhibit antagonistic properties against weeds (Audrain et al. 2015). In some studies, it was also encountered that VOCs have a profound role in growth of nearby microbes in the rhizosphere milieu. The growth of P. fluorescens strain Pf0–1 is stimulated in the presence of S. plymuthica and Collimonas pratensis, which has also improved bacteria’s ability to fight against pathogens (Garbeva et al. 2014). This implies that the microbial VOCs bridge the communication with other microbes resulting in either antagonistic behaviour against pathogens or synergistic effects on growth of bacteria thriving in nutrient-limited conditions (Schulz-Bohm et al. 2017). Contrary to this, some fungal VOCs also suppress bacterial species; for instance, VOCs from Pleurotus ostreatus exhibit inhibitory effects on B. cereus and B. subtilis (Werner et al. 2016). Apart from VOCs, rhizosphere microflora also secrete secondary metabolites such as hymeglusin and BELACTOSINS that suppresses the root parasitic weeds and display an eventual role for management of parasitic weeds (Masteling et al. 2019).

3.5

Microbe-Mediated Management

3.5.1

Upgrading the Competitive Nature of Crop Plants

3.5.1.1 Increasing Nutrient Acquisition of Native Crop or Plants With erratic weather conditions, weed species tends to develop dominance in crop– weed competition, credited to their superior heritable diversity, plasticity, and versatility, making them robust with better growth than the crops. Correspondingly, it results in nutritional imbalance causing poor growth and development of crop plants (Bukhari et al. 2019). Therefore, the use of microorganisms as plant growth developers for enhancing the nutrient acquisition ability of crop plants, to impart an edge over the robustly flourishing weeds, could be a fruitful strategy. Microbes play primary role in nutrient cycling, and therefore, they should be further investigated to improve the solubility of nutrients bound to minerals in soil solution and organic complexes, to facilitate plants’ uptake of nutrients. Numerous microbial taxa, such as Pseudomonas, Bacillus, Rhizobium, Arthrobacter, and Azotobacter, as well as mycorrhizal fungi, through their cellular metabolism have been shown to increase the amount of nutrients available to be taken up by crop plants (Pattnaik et al. 2021). Bioincoulation of wheat rhizosphere with P. putida, P. mendocina, P. stutzeri, and Azotobacter vinelandii significantly enhanced the migration of Zn, K, Mg, and Ca from soil to plant’s shoot. The strains lowered the pH and electrical conductivity in the inoculated soil over the uninoculated one (Ullah et al. 2022). Reports suggest that microbes can also impose modifications of root structural architecture in rhizosphere region (Grover et al. 2021). The primary channel through which plants explore soil for nutrient acquisition is through their roots. Being highly plastic, the architecture of

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roots is structured considerably by soil solution, microorganisms, plant species type, and environmental factors. In addition to alterations in root architecture, an increased uptake of nitrogen and phosphorus was reported in soybean plant upon inoculation with salt-tolerant P. putida and B. japonicum (Egamberdieva et al. 2017). These microorganisms significantly increase the surface area available for absorption, the number of root tips and hairs, and the formation of lateral roots (El Zemrany et al. 2007). Of many such root modifications, the majority are attributed to rhizobacterial genome and hormone secretion such as cytokinin, auxins, and gibberellins (Ambreetha and Balachandar 2019), regulation of auxin functional genes (Ambreetha et al. 2018), regulation of plant hormonal mechanisms by microbial metabolites (Zamioudis et al. 2013), etc.

3.5.1.2 Improving Resilience to Drought in Crop Plants Another condition brought on by climate change that has become worrisome for crop productivity and survival is drought. Weeds synthesize allelochemicals, upon encountering drought, to prosper well and compete with native plants or crops (Amare 2016). A recently conducted study reveals that weeds alone have adversely affected the crop productivity (28%) and drought-like conditions further lower the yield (29.85%) (Vila et al. 2021). Microorganisms are equipped with several strategies such as biosynthesis of ACC deaminase, exopolysaccharides, osmolytes, and phytohormones that alleviate the stress associated with drought, for instance, inoculation of maize rhizosphere with Bacillus spp. BEB1 under the water stress (25% 6000 MW PEG) resulted in improved vigour as evaluated by increased plant biomass, enhanced photosynthetic machinery, and improved nutrient uptake (Azeem et al. 2022). Saberi Riseh et al. (2021) published a cumulative literature on improved strategy about encapsulation of beneficial PGPR for combating drought stress. Polysaccharide coating such as starch, chitosan, cellulose, Na-alginate, or their derivatives has been used. Since polysaccharides have inherent property of absorbing and retaining water molecules in interstitial spaces, they provide protection to PGPR and concurrent plant growth. This strategy is particularly important in waterstressed climatic aberrations.

3.5.2

Improving Herbicide Tolerance in Crop Plants

Over-application of agrochemicals and herbicides for control of weeds is ecologically risky and unfeasible, and it has caused significant water, soil, and air pollution. Therefore, it is necessary to develop weed management biocontrol strategies that are affordable, environmentally benign, and long-lasting. These strategies could incorporate microbes or their by-products to partition bioresources (water, nutrients, space, and space) in a way that encourages the crop development and simultaneously prevents the proliferation of weed species (Dahiya et al. 2019). The compromising herbicide efficacy owing to climatic variations could raise severe concerns on existing weed managing options, provoking excessive application of herbicide than recommended doses. Evidences also suggest that using

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herbicides at higher-than-recommended doses has resulted in a significant decrease population of total soil microbes, P-solubilizers, cellulose decomposers, nitrifiers, etc., and activity of critical soil microbial enzymes (Rose et al. 2016). As the temperature rises and moisture regimes changes, the herbicide efficacy is compromised and therefore to counteract the negative effects of herbicides on soil biology and subsequently on crop growth, augmenting the crop rhizosphere with beneficial microorganisms could be a way forward.

3.5.2.1 Bioaugmentation with Herbicide-Tolerant PGPRs The herbicide-tolerant or herbicide-resistant PGPRs could be the new line of defence to minimize the deleterious repercussions of herbicides on soil microbial function and structure. Several microorganisms have developed metabolic plasticity that involves modulation of enzyme activities that in turn makes them resistant to the harmful effects of contaminants like herbicides (Rovida et al. 2021). Herbicide exposure results in the generation of ROS, which damages the membrane potential and causes severe harm to microbes and plants. Several microbes synthesize antioxidant enzymes in response to ROS as their defence mechanism. For example, glyphosate resistance was acquired in microbes by upregulation of EPSP synthase gene, elevating its production and in that way lowering their sensitivity to glyphosate (Hertel et al. 2021). The authors also reported two glyphosate-sensitive ESPS variants that reduce uptake of glyphosate, Burkholderia anthina and Burkholderia cenocepacia having ability to tolerate high glyphosate levels (Hertel et al. 2022). In another study, the PGPR traits of herbicide-tolerant P. putida strain PS9 were evaluated with 3X concentration of quizalofop-ethyl. The authors reported substantial increase levels of exopolysaccharides as the mechanism adopted by the microbe to prevent contact with the herbicide (Ahemad and Khan 2012). The promising way to develop herbicide-tolerant PGPRs following climatic aberrations is to isolate associated microbes from weeds emerging in those conditions. A comparable study was carried out where three native PGPRs were isolated from rhizosphere of Medicago sativa. Under imazethapyr stress, inoculation of these PGPRs namely Serratia rubidaea, Sinorhizobium meliloti, and P. putida enhanced the microbial population and plant biomass. Also, a rise in expression of antioxidant enzymatic machinery (CAT, GPX, APX) was noted, besides accumulation of higher malondialdehyde content. Alongside promoting plant growth, bioaugmentation strengthens the plant’s resistance to imazethapyr by lowering redox stress and lipid peroxidation (Motamedi et al. 2022). Similar research findings were also presented earlier by Ahemad and Khan (2012) wherein Bradyrhizobium sp. MRM6 with multiple PGPR traits was evaluated to improve the greengram productivity under herbicide-stressed soils. The strain was shown to tolerate three times the recommended doze (400 μg kg-1 soil) of quizalofop-p-ethyl with improved plant biomass (102%), nodulation (14–60%), yield (72%), and grain protein (4%) compared to uninoculated soils. PGPR strains mutant for herbicide resistance were also studied and developed. For example, inoculation of rice with diazotrophic cyanobacteria, Anabaena variabilis, a mutant for herbicide-resistant against arozin-R, alachlor-R, butachlor-R, and 2, 4-D-R, was shown to enhance

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growth and increased the yield by 76% compared to uninoculated crop (Singh and Datta 2007). These microbes with cumulative benefits could be promoted as rhizobio-augmentations for maintaining soil fertility and crop productivity under intense herbicide stress. The injudicious use of herbicides causes their accumulation in soil that can negatively affect the biological makeup and soil quality. By ingesting too many herbicides, the metabolically active, naturally occurring PGPR is rendered inactive. These discoveries provide fresh perspectives on how to prepare biofertilizers to lessen environmental pressures.

3.5.3

Microorganisms in Lowering Greenhouse Gases and Their Impact

Life depends on carbon, the basis for life’s basic building blocks, including the lipids, proteins, nucleic acids, and carbohydrates that make up our cells. Climate change, the most immediate issue globally, is the direct outcome of carbon emissions. The atmospheric CH4 and CO2 levels are at historic highs, which trap the atmosphere’s heat. The survival of all the higher trophic life forms relies directly or indirectly on microorganisms as they regulate the state of carbon (sequestration and release) into the atmosphere, seas, and biosphere. Researchers have been examining whether bacteria may boost carbon sequestration by iron fertilization, which involves adding iron to ocean waters that are otherwise deficient in it for the purpose of fostering development of phytoplankton with the aim to rapidly lower the atmospheric CO2 levels (Boyd et al. 2000). A green and sustainable method for reducing global warming is offered by microbial CO2 sequestration, which also simultaneously generates biofuels and chemicals. Taking CO2 out of the atmosphere and storing it in a land unit’s soil through unit plants, plant waste, and other organic substances, this technique enhances soil organic carbon storage (Olson 2013). The success of microbial CO2 fixing is still quite low, though, and furthermore, the concurrent microbial CO2 release reduces carbon yield of desirable compounds. To combat these problems, techniques have been developed to improve the efficiency of CO2 fixation in both autotrophic and heterotrophic microbes, including developing CO2-fixing routes and energy-harvesting systems. Researchers assert that carbon could accumulate as persistent, durable forms of organic matter in soils. Increased levels of difficult-todegrade organic matter will lead to long-term carbon storage in soils with concurrent reduction in carbon emissions (Six et al. 2006; Powlson et al. 2011). Furthermore, by customizing the energy metabolism and biochemical pathways, the carbon yield of high-value products can be increased simultaneously cutting down on microbial CO2 emissions (Hu et al. 2019). Soil bacteria also contribute to carbon sequestration by their ability to construct sediment carbonates, develop resilient vegetative tissues and products, and create sturdy forms like soil aggregates that conserve carbon-containing soil organic forms. Findings suggest that certain types of bacteria possess the capacity to reduce CO2

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and could lower the atmospheric CO2 levels by carbon sequestration (Ahmed et al. 2019). For example, using Pseudomonas fluorescens, a PGPR, might help sequester carbon and lower climate change adversities (Nie et al. 2015). Microbial inoculants containing P. fluorescens enhance the plant biometrics and could reduce eCO2 levels by boosting terrestrial carbon sequestration, particularly in high-CO2 habitats. Some bacteria could possibly sequester carbon and collect ambient CO2 through the synthesis of carbonate (Peng et al. 2010). The bacterium Bacillus mucilaginosus produces carbonic anhydrase that absorbs ambient CO2 and then fix it through microbial activities (Zhang et al. 2011). By absorbing atmospheric CO2, this mechanism stimulates carbonate production, resulting in the formation of organic materials or carbonated minerals. This in turn reduces the atmospheric CO2 levels and boosts the soil carbon retention. Several Bacillus strains including B. pasteurii (Stocks-Fischer et al. 1999), B. mucilaginosus (Zhang et al. 2011), B. cereus (Han et al. 2013), and B. pumilus (Komala and Khun 2014) were reported to sequester carbonates, thus lowering lower CO2 and aiding in carbon sequestration. Fungi outperform bacteria in regard to carbon sequestration, organic matter production, and soil stability as they have refractory biomass tissues and by-products that increase carbon preservation and stability by way of soil aggregate formation (Six et al. 2006; Li et al. 2015). Fungal tissues also contribute a significant quantity of carbon to soil, causing it to assimilate more carbon. The hyphae and spore of mycorrhizal fungi like Entrophospora, Acaulospora, Gigaspora, Glomus, and Scutellospora avoid becoming dehydrated by exuding an insoluble aqueous adhesive proteinaceous substance called glomalin (Pal and Pandey 2014). It has two effects on carbon sequestration, firstly, glomalin production aids in the development of soil aggregates, which in turn has an impact on carbon sequestration, and secondly, glomalin’s resistant character, making it arduous to break down, thus increasing its stability in soils for long time. Methane is the second-largest greenhouse gas after carbon dioxide, and 11% of the planet’s anthropogenic methane production emanate from paddy fields. As sulphate reducers and methanogens have the same receptors for their substrates, sulphate amendment could be a feasible mitigating strategy to curb rice field methane emission. Electrogenic sulphide oxidation is a process used by filamentous bacteria known as cable bacteria to raise sulphate levels. Scholz et al. (2020) demonstrated that single inoculation of cable bacteria escalates the sulphate stockpile by fivefold and lowers emission of methane by 93%, compared to uninoculated rice pots. These findings are encouraging for application of cable bacteria for management methane emissions from rice cultivating areas. Agriculture is among the prominent sources of another potent GHG emission, i.e. nitrous oxide (N2O). The administration of microbial cocktails (N2O reductase harbouring denitrifiers) into biologically competitive soil habitats has shown tremendous potential for increased N2O mitigation benefits. Strategies for reducing emissions in agriculture are aided by breakthroughs in our comprehension of the ecophysiology of the bacteria that convert N2O to innocuous N2. N2O emissions from soybean have been significantly reduced by deploying bacterial strains with greater N2O reductase activity, and it has been observed that both naturally occurring

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and genetically engineered strains with higher N2O reductase activity provide potential solutions for N2O emission reduction (Itakura et al. 2013). The richness, content, and organization of the soil’s microbial community have been demonstrated to be influenced by eCO2, with the effect being more pronounced near the roots and in active microbial communities. The capacity of fungi to acquire nutrients and act as biological nitrogen fixers are favourably affected by high C: N ratios under eCO2. Compared to ecosystems with bacterial soil communities, fungal soil communities may hold onto more carbon. However, the plenty of nutrients and nitrogen necessary for biological fixation of nitrogen substantially influence soil C-sequestration through plant development. Although they come with a carbon cost, nitrogenous and other chemical fertilizers have a favourable impact on carbon sequestration. It might be feasible to maintain the soil’s nutritional balance for increased C-sequestration by promoting the activities of biological nitrogen fixers, nutrient solubilizers, and nutrient mobilizers (Grover et al. 2015). Microbes modulate the magnitude of earthly greenhouse gases, which requires considering the intricate relationships between microbes and other biotic and abiotic elements. Prospects are exciting because they include the possibility of lowering greenhouse gas emissions by controlling terrestrial microbial activities. Microorganisms significantly impact how much greenhouse gas is present in the atmosphere. By altering the structure and composition of their microbial communities, the principal feedback–response mechanism for climate change can resolve this environmental issue. Agricultural approaches that use microbial inoculants may help the soil develop desired properties. In the “bio-sequestration” process, soil bacteria and photosynthetic organisms take in and store CO2 organically (Macreadie et al. 2014). The microbial communities in the soil are crucial to carbon release and sequestration, and therefore, intake and output of carbon in soil can be regulated using these microbial inoculants (Fang et al. 2014).

3.5.4

Microbial Genetics in Changing Environment

The genetic variability and adaptation allow microbes to evolve and function more efficiently under climate change vis-à-vis microbes that can be genetically engineered to withstand these variations. The poor efficiency of CO2 capture and fixing might be addressed by genetically engineering microorganisms. The prospects for using microorganisms as biostimulants for carbon sinks in agricultural fields might then be further investigated. Synechococcus elongatus PCC 7942, a cyanobacterium, genetically altered to fix CO2 biologically along with chemical process. Utilizing genetic engineering, it might be possible to increase CO2 bio-mitigation by CO2 capturing or transformation via carbonic anhydrase, assisting in biomass accumulation by biological fixation of captured CO2 (Chen et al. 2012). In contrast to fungus, bacteria have shown enormous potential to develop as bio-herbicide agents more quickly, and they also have simpler propagation requirements and are highly suitable for genetic alteration by either mutagenesis or gene transfer (Johnson et al. 1996; Li et al. 2003).

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Metagenomic Approaches to Advance Microbial Weed Management Tactics

Recent advancements in molecular biology have enabled researchers to identify novel plant–microbial relationships that are important for weed management (Kao-Kniffin et al. 2013). The rapidly developing science of metagenomics eliminates the requirement to isolate and cultivate microbes by allowing both microbial identification and function to be identified by simply collecting DNA and RNA from the environment. The variety of the recovered microbial strains rises with direct DNA isolation from the environment, and according to metagenomic research, a single gram of soil contains between 2000 and over 52,000 microbial species or genomes. The fraction of microbial species discovered using conventional growing techniques is substantially below this estimate. Herbicide like glufosinate is an example of herbicidal chemicals isolated from soil bacteria through culturing techniques. The advance of metagenomic technologies for weed control in relation to culture-independent and methods of natural product separation several different climatic circumstances can be fruitful. Herbicide resistance genes may be isolated using the same methods. Metagenomic techniques for pest management research can open the doors for development of innovative crop and landscape pest control strategies. Besides this, this will also serve as base for identification of climateresilient microbes that can serve as building block to develop microbial strategies for management of weeds. Climate-resilient microbes including thermo-tolerant, halophiles, drought-tolerant, xerophiles, can be studied for improved control of weeds in hot environments, elevated GHGs, drought, etc., conditions.

3.6

Conclusion

Weeds are anticipated to spread farther due to climate change, resulting in significant production loss in farming and forest ecosystems. Additionally to what has been covered above, microorganisms display an array of different evolutionary adaptations that allow them to strategically manage weeds for biotic and abiotic stress in response to climate change. We need to explore the microbial genetic material, especially related to degradation and elimination of pollutants (herbicides) or gases that cause worldwide warming and activate their nutrition cycle processes. Microbial communities and nutrient recycling can be effectively coupled to address climate change. The capacity of microbes to exploit greenhouse gases as an energy source and improve their growth is crucial. With ever-increasing use of chemicalbased herbicides, there is need to explore biological control options for weed management that can sustain eCO2 and other climatic changes. In these circumstances, microorganisms fixing nitrogen, mobilization and solubilization of nutrients, may be essential for preserving the soil nutritional balance. In the domain of plat–microbe interaction, strenuous multidisciplinary scientific research at the grassroots with the option of scaling up to the global basis will be required to comprehend the long-term responses of microbial communities in soil to changing

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climate and ascertain the prerequisites needed for effective weed management. In future, the performance-based screening of microorganisms may help to manage emerging weeds, and biological systems including rhizosphere bacteria will undoubtedly be impacted by the changing climatic conditions.

References A'Bear AD, Boddy L, Hefin Jones T (2012) Impacts of elevated temperature on the growth and functioning of decomposer fungi are influenced by grazing collembola. Glob Chang Biol 18(6): 1823–1832 Ahemad M, Khan MS (2012) Evaluation of plant-growth-promoting activities of rhizobacterium Pseudomonas putida under herbicide stress. Ann Microbiol 4:1531–1540 Ahmed AAQ, Odelade KA, Babalola OO (2019) Microbial inoculants for improving carbon sequestration in agroecosystems to mitigate climate change. In: Handbook of climate change resilience. Springer International, Cham, pp 1–21 Amare T (2016) Review on impact of climate change on weed and their management. Am J Agric Biol Environ Stat 2(3):21–27 Ambreetha S, Balachandar D (2019) Rhizobacteria-mediated root architectural improvement: a hidden potential for agricultural sustainability. In: Kumar A, Meena VS (eds) Plant growth promoting Rhizobacteria for agricultural sustainability, vol 6. Springer Nature Singapore Pte Ltd, Singapore, pp 111–128 Ambreetha S, Chinnadurai C, Marimuthu P, Balachandar D (2018) Plant-associated bacillus modulates the expression of auxin-responsive genes of rice and modifies the root architecture. Rhizosphere 5:57–66 Andrew C, Heegaard E, Halvorsen R, Martinez-Peña F, Egli S, Kirk PM, Basselur C, Büntgen U, Aldea J, Klaus Høiland K, Boddy L, Kauserud H (2016) Climate impacts on fungal community and trait dynamics. Fungal Ecol 22:17–25 Archambault J, Robinson D, O’Donovan J, Klein K (2001) The effects of elevated CO2 and temperature on herbicide efficacy and weed/crop competition. Rept Prairie Adapt Res Collab 29 Audrain B, Farag MA, Ryu CM, Ghigo JM (2015) Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev 39:222–233 Auld BA (2004) The persistence of weeds and their social impact. Int J Soc Econ 31:879–886 Azeem M, Haider MZ, Javed S, Saleem MH, Alatawi A (2022) Drought stress amelioration in maize (Zea mays L.) by inoculation of bacillus spp. strains under sterile soil conditions. Agriculture 12(1):50 Bajpai A, Mahawar H, Dubey G, Atoliya N, Parmar R, Devi MH, Mohanty SR (2022) Prospect of pink pigmented facultative methylotrophs in mitigating abiotic stress and climate change. J Basic Microbiol 62:889. https://doi.org/10.1002/jobm.202200087 Bajwa A, Chauhan B, Adkins S (2017) Morphological, physiological and biochemical responses of two Australian biotypes of Parthenium hysterophorus to different soil moisture regimes. Environ Sci Pollut Res 24(19):16186–16194. https://doi.org/10.1007/s11356-017-9176-1 Baker HG (1965) Characteristics and modes of origin of weeds. In: Genetics of colonizing species. Academic Press, New York, pp 147–172 Bazzaz FA, Carlson RW (1984) The response of plants to elevated CO2. Oecologia 62:196–198 Beestman G, Deming J (1974) Dissipation of acetanilide herbicides from soils. Agron J 66:308–311 Bergmann J, Pompe S, Ohlemüller R, Freiberg M, Klotz S, Kühn I (2010) The Iberian Peninsula as a potential source for the plant species pool in Germany under projected climate change. Plant Ecol 207:191–201 Boese S, Wolfe D, Melkonian J (1997) Elevated CO2 mitigates chilling-induced water stress and photosynthetic reduction during chilling. Plant Cell Environ 20:625–632

80

H. Mahawar et al.

Bourchier R, Van Hezewijk BH (2010) Distribution and potential spread of Japanese knotweed (Polygonum cuspidatum) in Canada relative to climatic thresholds. Invas Plant Sci Manag 3(1): 32–39 Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, Murdoch R, Bakker DC, Bowie AR, Buesseler KO, Chang H, Charette M (2000) A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407(6805):695–702 Bradley BA, Blumenthal DM, Wilcove DS, Ziska LW (2010) Predicting plant invasions in an era of global change. Trends Ecol Evol 25:310–318 Broennimann O, Treier U, Müller-Schärer H, Thuiller W, Peterson A, Guisan A (2007) Evidence of climatic niche shift during biological invasion. Ecol Lett 10(8):701–709 Bukhari SAH, Peerzada AM, Javed MH, Dawood M, Hussain N, Ahmad S (2019) In: Hasanuzzaman M (ed) Growth and development dynamics in agronomic crops under environmental stress in agronomic crops. Springer, Singapore. https://doi.org/10.1007/978-981-329151-5_6 Carrell AA, Lawrence TJ, Cabugao KGM, Carper DL, Pelletier DA, Lee JH, Weston DJ (2022) Habitat-adapted microbial communities mediate Sphagnum peatmoss resilience to warming. New Phytol 234:2111–2125 Chandrasena N (2009) How will weed management change under climate change? Some perspectives. J Crop Weed 5:95–105 Chauhan B, Prabhjyot K, Mahajan G, Randhawa R, Singh H, Kang M (2014) Global warming and its possible impact on agriculture in India. Adv Agron 123:65–121 Chen PH, Liu HL, Chen YJ, Cheng YH, Lin WL, Yeh CH, Chang CH (2012) Enhancing CO2 bio-mitigation by genetic engineering of cyanobacteria. Energ Environ Sci 5(8):8318–8327 Cheng X, Etalo DW, van de Mortel JE, Dekkers E, Nguyen L, Medema MH, Raaijmakers JM (2017) Genome-wide analysis of bacterial determinants of plant growth promotion and induced systemic resistance by Pseudomonas fluorescens. Environ Microbiol 19(11):4638–4656 Dahiya A, Sharma R, Sindhu S, Sindhu SS (2019) Resource partitioning in the rhizosphere by inoculated bacillus spp. towards growth stimulation of wheat and suppression of wild oat (Avena fatua L.) weed. Physiol Mol Biol Plants 25(6):1483–1495 Das TK, Sharma AR, Pathak H (2012) Crop-weed balance studies under climate change. In: Climate change impact, adaptation and mitigation in agriculture: methodology for assessment and application. Indian Agricultural Research Institute, New Delhi, p 131 de Bekker C, Ohm RA, Loreto RG, Sebastian A, Albert I, Merrow M et al (2015) Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genomics 16(1):620. https://doi.org/10.1186/s12864-015-1812-x Dekker J (2003) Evolutionary biology of the foxtail (Setaria) species-group. In: Inderjit K (ed) Weed biology and management. Kluwer Academic, Dordrecht, pp 65–114 Donald W, Khan M (1992) Yield loss assessment for spring wheat (Triticum aestivum) infested with Canada thistle (Cirsium arvense). Weed Sci 40:590–598 DWR, Annual report (2017–2018). https://dwr.icar.gov.in/DWR%20Annual%20Report/2017-201 8.pdf DWR, Annual report (2018–2019). https://dwr.icar.gov.in/DWR%20Annual%20Report/2018-201 9.pdf DWR, Annual report (2020–2021). https://dwr.icar.gov.in/DWR%20Annual%20 Report/2020-2021.pdf Egamberdieva D, Wirth S, Jabborova D, Räsänen LA, Liao H (2017) Coordination between Bradyrhizobium and pseudomonas alleviates salt stress in soybean through altering root system architecture. J Plant Interact 12(1):100–107 El Zemrany H, Czarnes S, Hallett PD, Alamercery S, Bally R, Jocteur Monrozier L (2007) Early changes in root characteristics of maize (Zea mays) following seed inoculation with the PGPR Azospirillum lipoferum CRT1. Plant and Soil 291(1):109–118 Elmore C, Paul R (1983) Composite list of C4 weeds. Weed Sci 31:686–692

3

Emerging Weeds Under Climate Change and Their Microbial Management

81

Fang H, Cheng S, Wang Y, Yu G, Xu M, Dang X, Li L, Wang L (2014) Changes in soil heterotrophic respiration, carbon availability, and microbial function in seven forests along a climate gradient. Ecol Res 6:1077–1086 Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46 Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439 Garbeva P, Hordijk C, Gerards S, de Boer W (2014) Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 87:639–649. https://doi.org/10.1111/1574-6941. 12252 Garrett K, Dendy S, Frank E, Rouse M, Travers S (2006) Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489 Grover M, Maheswari M, Desai S, Gopinath KA, Venkateswarlu B (2015) Elevated CO2: plant associated microorganisms and carbon sequestration. Appl Soil Ecol 95:73–85 Grover M, Bodhankar S, Sharma A, Sharma P, Singh J, Nain L (2021) PGPR mediated alterations in root traits: way toward sustainable crop production. Front Sustain Food Syst 4:618230 Guan B, Guo H, Chen S, Li D, Liu X, Gong X, Ge G (2020) Shifting ranges of eleven invasive alien plants in China in the face of climate change. Eco Inform 55:101024 Hamid R, Ahmad R, Ali R (2012) The impact of elevated CO2 on growth and competitiveness of C3 and C4 crops and weeds. Eur J Exp Biol 2(4):1144–1150 Han J, Lian B, Ling H. (2013) Induction of calcium carbonate by Bacillus cereus. Geomicrobiol J 30:682–689 Hartfield J, Boote K, Kimball B, Ziska L, Izaurralde R, Ort D, Thomson A, Wolfe D (2011) Climate impacts on agriculture: implications for crop production. Agron J 103:351–370 Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22:534–543 Hertel R, Gibhardt J, Martienssen M, Kuhn R, Commichau FM (2021) Molecular mechanisms underlying glyphosate resistance in bacteria. Environ Microbiol 6:2891–2905 Hertel R, Schöne K, Mittelstädt C, Meißner J, Zschoche N, Collignon M, Kohler C, Friedrich I, Schneider D, Hoppert M, Kuhn R (2022) Characterization of glyphosate-resistant Burkholderia anthina and Burkholderia cenocepacia isolates from a commercial roundup® solution. Environ Microbiol Rep 14(1):70–84 Hu G, Li Y, Ye C, Liu L, Chen X (2019) Engineering microorganisms for enhanced CO2 sequestration. Trends Biotechnol 37(5):532–547 Imholt C, Gibbins C, Malcolm I, Langan S, Soulsby C (2010) Influence of riparian cover on stream temperatures and the growth of the mayfly Baetis rhodani in an upland stream. Aquat Ecol 44: 669–678 IPCC (2007) IPCC fourth assessment report. In: Climate change 2007: the physical science basis, vol 2. IPCC, Geneva, pp 580–595 IPCC (2018) Global warming of 1.5 °C. In: Masson-Delmotte V, Zhai P, Pörtner HO, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, Matthews JBR, Chen Y, Zhou X, Gomis MI, Lonnoy E, Maycock T (eds) An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. Intergovernmental Panel on Climate Change (IPCC), Geneva Irmaileh BA (2011) Climate change impact on weeds. In: Solh M, Saxena MC (eds) Food security and climate change in dry areas, Proceedings of the International Conference, Amman, Jordan, 1–4 February 2010. International Center for Agricultural Research in the Dry Areas (ICARDA), Aleppo, Syria, pp 170–175 Itakura M, Uchida Y, Akiyama H, Hoshino YT, Shimomura Y, Morimoto S, Tago K, Wang Y, Hayakawa C, Uetake Y, Sánchez C (2013) Mitigation of nitrous oxide emissions from soils by Bradyrhizobium japonicum inoculation. Nat Clim Chang 3(3):208–212 Jaggard K, Qi A, Ober E (2010) Possible changes to arable crop yields by 2050. PhilosTrans R Soc B Biol Sci 365:2835–2851

82

H. Mahawar et al.

Johnson B, Young B (2002) Influence of temperature and relative humidity on the foliar activity of mesotrione. Weed Sci 50:157–161 Johnson DR, Wyse DL, Jones KJ (1996) Controlling weeds with phytopathogenic bacteria. Weed Technol 10(3):621–624 Kadam N, Xiao G, Melgar R, Bahuguna R, Quinones C, Tamilselvan A, Prasad P, Jagadish S (2014) Agronomic and physiological response to high temperature, drought, and elevated CO2 interaction in cereals. Adv Agron 127:111–156 Kao-Kniffin J, Carver SM, DiTommaso A (2013) Advancing weed management strategies using metagenomic techniques. Weed Sci 61(2):171–184 Kathiresan RM (2006) Effect of global warming on invasion of alien plants in Asia. In: India Symposium. Annamalai University, Annamalainagar Kathiresan R, Gualbert G (2016) Impact of climate change on the invasive traits of weeds. Weed Biol Manag 16:59–66 Kathiresan RM, Gnanavel I, Anbhazhagan R, Padmaria SP, Vijayalakshmi NK, Arulchezhian MP (2005) Ecology and control of Parthenium invasion in command area. In: Proceedings of Second International Conference on Parthenium Management, December, pp 5–7 Kaur A, Batish D, Kaur S, Singh H, Kohli R (2017) Phenological behaviour of Parthenium hysterophorus in response to climatic variations according to the extended BBCH scale. Ann Appl Biol 171(3):316–326 Koger CH, Reddy KN, Poston DH (2004) Factors affecting seed germination, seedling emergence, and survival of Texas weed (Caperonia palustris). Weed Sci 52:989–995 Komala T, Khun TC (2014) Biological carbon dioxide sequestration potential of Bacillus pumilus. Sains Malays 43(8):1149–1156 Krah FS, Büntgen U, Schaefer H, Müller J, Andrew C, Boddy L et al (2019) European mushroom assemblages are darker in cold climates. Nat Commun 10(1):2890 Larsson P, Solhaug KA, Gauslaa Y (2012) Seasonal partitioning of growth into biomass and area expansion in a cephalolichen and a cyanolichen of the old forest genus Lobaria. New Phytol 194(4):991–1000 Li Y, Sun Z, Zhuang X, Xu L, Chen S, Li M (2003) Research progress on microbial herbicides. Crop Prot 22(2):247–252 Li N, Xu YZ, Han XZ, He HB, Zhang XD, Zhang B (2015) Fungi contribute more than bacteria to soil organic matter through necromass accumulation under different agricultural practices during the early pedogenesis of a Mollisol. Eur J Soil Biol 67:51–58 Li N, Euring D, Cha JY, Lin Z, Lu M, Huang LJ, Kim WY (2021) Plant hormone-mediated regulation of heat tolerance in response to global climate change. Front Plant Sci 11:627969 Mack RN, Simberloff D, Lansdale WF, Evans H (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710 Macreadie PI, Baird ME, Trevathan-Tackett SM, Larkum AW, Ralph PJ (2014) Quantifying and modelling the carbon sequestration capacity of seagrass meadows—a critical assessment. Mar Pollut Bull 83(2):430–439 Mahajan G, Samunder S, Bhagirath S (2012) Impact of climate change on weeds in the rice-wheat cropping system. Curr Sci 102(9):1254–1255 Manea A, Leishman M, Downey P (2011) Exotic C4 grasses have increased tolerance to glyphosate under elevated carbon dioxide. Weed Sci 59:28–36 Mao R, Ali A, Steve A (2021) A superweed in the making: adaptations of Parthenium hysterophorus to a changing climate. A review. Agron Sustain Dev 41(4):1–18 Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PloS One 7(10):e48479 Maron J, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74(2):261–280 Masteling R, Lombard L, De Boer W, Raaijmakers JM, Dini-Andreote F (2019) Harnessing the microbiome to control plant parasitic weeds. Curr Opin Microbiol 49:26–33

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Matloob A, Khaliq A, Tanveer A, Husssain S, Aslam F, Chauhan B (2015) Weed dynamics in dry direct-seeded fine rice as influenced by tillage system, sowing time and weed competition duration. Crop Prot 71:25–38 McDonald A, Riha S, DiTommaso A, DeGaetano A (2009) Climate change and the geography of weed damage: analysis of US maize systems suggests the potential for significant range transformations. Agric Ecosyst Environ 130:131–140 Mcdowell R, Condron L, Main B, Dastgheib F (1997) Dissipation of imazapyr, flumetsulam and thifensulfuron in soil. Weed Res 37:381–389 Miri HR, Rastegar A, Bagheri AR (2012) The impact of elevated CO2 on growth and competitiveness of C3 and C4 crops and weeds. Eur J Exp Biol 2:1144–1150 Mohamed K, Papes M, Williams R, Benz B, Peterson T (2006) Global invasive potential of 10 parasitic witchweeds and related Orobanchaceae. Ambio 35:281–288 Morgan J, LeCain D, Mosier A, Milchunas D (2001) Elevated CO2 enhances water relations and productivity and affects gas exchange in C3 and C4 grasses of the Colorado shortgrass steppe. Glob Chang Biol 7:451–466 Mortensen D, Coble H (1989) The influence of soil water content on common cocklebur (Xanthium strumarium) interference in soybeans (Glycine max). Weed Sci 37:76–83 Motamedi M, Zahedi M, Karimmojeni H, Motamedi H, Mastinu A (2022) Effect of rhizosphere bacteria on antioxidant enzymes and some biochemical characteristics of Medicago sativa L. subjected to herbicide stress. Acta Physiol Plant 44(8):1–2 Murdoch AJ, Roberts EH, Goedert CO (1989) A model for germination responses to alternating temperatures. Ann Bot 63:97–111 Naidu V (2013) Invasive potential of C3-C4 intermediate Parthenium hysterophorus under elevated CO2. Indian J Agric Sci 83:176–179 Naidu V, Varshney J (2011) Interactive effect of elevated CO2, drought and weed competition on carbon isotope discrimination in wheat. Indian J Agric Sci 81:1026–1029 Naylor REL, Lutman PJ (2002) What is a weed? In: Naylor REL (ed) Weed management handbook, 9th edn. British Crop Protection Council, Blackwell Science, Oxford, pp 1–15 Nie M, Bell C, Wallenstein MD, Pendall E (2015) Increased plant productivity and decreased microbial respiratory C loss by plant growth-promoting rhizobacteria under elevated CO2. Sci Rep 5(1):1–6 Nowak R, Ellsworth D, Smith S (2004) Functional responses of plants to elevated atmospheric CO2–do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280 Olson KR (2013) Soil organic carbon sequestration, storage, retention and loss in US croplands: issues paper for protocol development. Geoderma 195:201–206 Oyewole CI, Ibikunle BAO (2010) The germination of corn weed (Rottboellia cochinchinensis Lour Clayton) seed: induction and prevention of germination in seed. Thai J Agric Sci 43:47–54 Pal A, Pandey S (2014) Role of glomalin in improving soil fertility. Int J Plant Soil Sci 3:112–129 Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669 Patterson D (1995) Weeds in a changing climate. Weed Sci 43:685–701 Patterson D, Highsmith M, Flint E (1988) Effects of temperature and CO2 concentration on the growth of cotton (Gossypium hirsutum), spurred anoda (Anoda cristata), and velvet leaf (Abutilon theophrasti). Weed Sci 36:751–757 Patterson D, Westbrook J, Joyce R (1999) Weeds, insects and diseases. Clim Change 47:711–727 Pattnaik S, Mohapatra B, Gupta A (2021) Plant growth-promoting microbe mediated uptake of essential nutrients (Fe, P, K) for crop stress management: microbe–soil–plant continuum. Front Agron 2021:58 Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504 Peng Y, Abercrombie LL, Yuan JS, Riggins CW, Sammons RD, Tranel PJ, Stewart CN Jr (2010) Characterization of the horseweed (Conyza canadensis) transcriptome using GS-FLX

84

H. Mahawar et al.

454 pyrosequencing and its application for expression analysis of candidate non-target herbicide resistance genes. Pest Manag Sci 66(10):1053–1062 Phillips O, Vásquez M, Monteagudo M, Baker T, Núñez V (2005) Large lianas as hyperdynamic elements of the tropical forest canopy. Ecology 86(5):1250–1258 Potvin C (1986) Biomass allocation and phenological differences among southern and northern populations of the C4 grass Echinochloa crus-galli. J Ecol 74:915–923 Powlson DS, Whitmore AP, Goulding KW (2011) Soil carbon sequestration to mitigate climate change: a critical re-examination to identify the true and the false. Eur J Soil Sci 62(1):42–55 Prasad P, Allen L, Boote K (2005) Crop responses to elevated carbon dioxide and interaction with temperature: grain legumes. J Crop Improv 13:113 Rajer FU, Wu H, Xie Y, Xie S, Raza W, Tahir HAS, Gao X (2017) Volatile organic compounds produced by a soil-isolate, Bacillus subtilis FA26 induce adverse ultra-structural changes to the cells of Clavibacter michiganensis ssp. sepedonicus, the causal agent of bacterial ring rot of potato. Microbiology 163(4):523–530 Ramesh K, Matloob A, Aslam F, Florentine SK, Chauhan BS (2017) Weeds in a changing climate: vulnerabilities, consequences, and implications for future weed management. Front Plant Sci 8: 95 Raza W, Ling N, Liu D, Wei Z, Huang Q, Shen Q (2016) Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiol Res 192:103–113. https://doi.org/10.1016/j.micres.2016.05.014 Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173 Ritter R, Coble H (1981) Influence of temperature and relative humidity on the activity of acifluorfen. Weed Sci 29:480–485 Romero-Olivares AL, Taylor JW, Treseder KK (2015) Neurospora discreta as a model to assess adaptation of soil fungi to warming. BMC Evol Biol 15(1):1–8 Rose MT, Cavagnaro TR, Scanlan CA, Rose TJ, Vancov T, Kimber S, Kennedy IR, Kookana RS, Van Zwieten L (2016) Impact of herbicides on soil biology and function. Adv Agron 136:133– 220 Rovida AF, Costa G, Santos MI, Silva CR, Freitas PN, Oliveira EP, Pileggi SA, Olchanheski RL, Pileggi M (2021) Herbicides tolerance in a pseudomonas strain is associated with metabolic plasticity of antioxidative enzymes regardless of selection. Front Microbiol 2021:1430 Saberi Riseh R, Ebrahimi-Zarandi M, Gholizadeh Vazvani M, Skorik YA (2021) Reducing drought stress in plants by encapsulating plant growth-promoting bacteria with polysaccharides. Int J Mol Sci 22(23):12979 Sage R (1995) Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture? Glob Chang Biol 1:93–106 Sangakkara UR, Wijesinghe DB, Attanayake KB (2014) Soil quality and crop yields as affected by microbial inoculants in nature farming. Building Organic Bridges 3:987–990 Santiago JP, Sharkey TD (2019) Pollen development at high temperature and role of carbon and nitrogen metabolites. Plant Cell Environ 42(10):2759–2775 Schimel D, Enting LG, Heimann M, Wigley TM, Raynaud D, Alves D, Siegenthaler U, Brown S, Emanuel WR, Fasham M, Field C (1995) C02 and the carbon cycle. In: Houghton JT, Filho LGM, Callander BA, Harris N, Kattenberg A, Maskell A (eds) Climate Change: The Science of Climate Change. Cambridge University Press, Cambridge, pp 65–131 Scholz VV, Meckenstock RU, Nielsen LP, Risgaard-Petersen N (2020) Cable bacteria reduce methane emissions from rice-vegetated soils. Nat Commun 11:1878 Schulz-Bohm K, Martín-Sánchez L, Garbeva P (2017) Microbial volatiles: small molecules with an important role in intra-and inter-kingdom interactions. Front Microbiol 8:2484 Sharma S, Singh M (2001) Environmental factors affecting absorption and bio-efficacy of glyphosate in Florida beggarweed (Desmodium tortuosum). Crop Prot 20:511–516

3

Emerging Weeds Under Climate Change and Their Microbial Management

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Singh S, Datta P (2007) Outdoor evaluation of herbicide resistant strains of Anabaena variabilis as biofertilizer for rice plants. Plant and Soil 296(1):95–102 Singh MK, Singh RK (2010) Alien invasive weeds—an emerging threat to agricultural biodiversity in India. In: Souvenir-Cum-Abstract, SAARC Workshop on Biodiversity Conservation. Department of Plant Physiology, Institute of Agricultural Sciences, BHU, Varanasi, India, p 91 Singh RP, Singh RK, Singh MK (2011) Impact of climate and carbon dioxide change on weeds and their management—a review. Indian J Weed Sci 43:1–11 Singh MC, Dubey SC, Yaduraju NT (2016) Climate change and its possible impacts on weeds. Int J Sci Environ Technol 5:1530–1539 Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70(2):555–569 Smith SD, Strain BR, Sharkey TD (1987) Effects of CO2 enrichment on four Great Basin grasses. Funct Ecol 1:139–143 Smith C, van Klinken RD, Seabrook L, McAlpine C (2012) Estimating the influence of land management change on weed invasion potential using expert knowledge. Divers Distrib 18: 818–831 Stocks-Fischer S, Galinat JK, Bang SS (1999) Microbiological precipitation of CaCO3. Soil Biol Biochem 31(11):1563–1571 Sun XG, Bonfante P, Tang M (2015) Effect of volatiles versus exudates released by germinating spores of Gigaspora margarita on lateral root formation. Plant Physiol Biochem 97:1–10 Suthar AC, Naik VR, Mulani RM (2009) Seed and seed germination in Solanum nigrum Linn. Am Eurasian J Agric Environ Sci 5:179–183 Swanton C, Huang J, Deen W, Tollenaar M, Shrestha A, Rahimian H (1999) Effects of temperature and photoperiod on Setaria viridis. Weed Sci 47(4):446–453 Ullah S, Bano A, Ullah A, Shahid MA, Khan N (2022) A comparative study of plant growth promoting rhizobacteria (PGPR) and sowing methods on nutrient availability in wheat and rhizosphere soil under salinity stress. Rhizosphere 23:100571 Valerio M, Tomecek M, Lovelli S, Ziska L (2013) Assessing the impact of increasing carbon dioxide and temperature on cropweed interactions for tomato and a C3 and C4 weed species. Eur J Agron 50:60–65 Varanasi A, Prasad P, Jugulam M (2016) Impact of climate change factors on weeds and herbicide efficacy. Adv Agron 135:107–146 Vigani G, Rolli E, Marasco R, Dell'Orto M, Michoud G, Soussi A, Daffonchio D (2019) Root bacterial endophytes confer drought resistance and enhance expression and activity of a vacuolar H+-pumping pyrophosphatase in pepper plants. Environ Microbiol 21(9):3212–3228 Vila M, Beaury EM, Blumenthal DM, Bradley BA, Early R, Laginhas BB, Trillo A, Dukes JS, Sorte CJ, Ibañez I (2021) Understanding the combined impacts of weeds and climate change on crops. Environ Res Lett 16(3):034043 Warwick S (1990) Genetic variation in weeds—with particular reference to Canadian agricultural weeds. In: Biological approaches and evolutionary trends in plants, pp 3–18 Warwick S, Phillips D, Andrews C (1986) Rhizome depth: the critical factor in winter survival of Sorghum halepense (L.) Pers. (Johnson grass). Weed Res 26(6):381–388 Warwick S, Thompson B, Black L (1987) Life history and allozyme variation in populations of the weed species Setaria faberi. Can J Bot 65(7):1396–1402 Webster CR, Jenkins MA, Jose S (2006) Woody invaders and the challenges they pose to forest ecosystems in the eastern United States. J For 104:366–374 Werner S, Polle A, Brinkmann N (2016) Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Appl Microbiol Biotechnol 100:8651–8665. https://doi.org/10.1007/s00253-016-7792-1 Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, Coleman-Derr D (2018) Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci 115(18):E4284–E4293

86

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Xu L, Dong Z, Chiniquy D, Pierroz G, Deng S, Gao C, Coleman-Derr D (2021) Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics. Nat Commun 12(1):1–17 Yin X, Struik P (2008) Applying modelling experiences from the past to shape crop. New Phytol 179:629–642 Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM (2013) Unraveling root developmental programs initiated by beneficial pseudomonas spp. bacteria. Plant Physiol 162(1): 304–318 Zhang Z, Lian B, Hou W, Chen M, Li X, Shen W, Li Y (2011) Optimization of nutritional constituents for carbonic anhydrase production by bacillus mucilaginosus K02. Afr J Biotechnol 10(42):8403–8413 Ziska L, Bunce J (1997) Influence of increasing carbon dioxide concentration on the photosynthetic and growth stimulation of selected C4 crops and weeds. Photosynth Res 54:199–208 Ziska L, Bunce J (2006) Plant responses to rising atmospheric carbon dioxide. In: Plant growth and climate change, vol 2006, pp 17–47 Ziska L, Dukes J (2011) Weed biology and climate change. Blackwell, Ames, IA, pp 68–205 Ziska L, George K (2004) Rising carbon dioxide and invasive, noxious plants: potential threats and consequences. World Resour Rev 16:427–447 Ziska L, Goins E (2006) Elevated atmospheric carbon dioxide and weed populations in glyphosate treated soybean. Crop Sci 46:1354–1359 Ziska L, Teasdale J (2000) Sustained growth and increased tolerance to glyphosate observed in a C3 perennial weed, quackgrass (Elytrigia repens (L.) Nevski), grown at elevated carbon dioxide. Aust J Plant Physiol 2:159–164 Ziska L, Tomecek M, Gealy D (2010) Competitive interactions between cultivated and red rice as a function of recent and projected increases in atmospheric carbon dioxide. Agron J 102:118–123

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Climate Change and Agriculture: Impact Assessment and Sustainable Alleviation Approach Using Rhizomicrobiome Ravi Kumar, Ajay Kumar, Rahul Kumar Dhaka, Madhvi Chahar, Sandeep Kumar Malyan, Arvind Pratap Singh, and Anuj Rana

Abstract

Climate change is one of the challenges of the twenty-first century towards sustainability, environment, energy supply, and health. The greenhouse gas (GHG) emission alters the climate of biosphere leading to change in frequency and pattern of natural phenomena like precipitation (snowfall and rain), cyclones, and storms. The climate change imposes stresses like salinity, drought, and rise in temperature that negatively impact the growth of plants, microorganisms, and animals. Climate change can potentially hamper the world food security goals via affecting the growth and development of plants resulting in yield loss. Further, the climate change impacts microbial diversity including rhizomicrobiome, which R. Kumar Department of Botany and Plant Physiology (Environmental Science), College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India A. Kumar · A. Rana (✉) Department of Microbiology, College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India e-mail: [email protected] R. K. Dhaka Department of Chemistry, College of Basic Sciences and Humanities, CCS Haryana Agricultural University, Hisar, India M. Chahar Department of Bio-nanotechnology, Guru Jambheshwar University of Science and Technology, Hisar, India S. K. Malyan Department of Environmental Studies, Dyal Singh Evening College, University of Delhi, New Delhi, India A. P. Singh School of Biotechnology, Jawaharlal Nehru University, New Delhi, Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_4

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has an important role to maintain ecosystem under different environmental thresholds. Microorganisms can produce and sequester greenhouse gases (GHGs) during their metabolic activities. The microorganisms such as methanotrophs, archaebacteria, halophytes, and plant growth-promoting rhizobacteria (PGPRs) have been applied to develop plant tolerance under different abiotic and biotic stresses via various mechanisms such as ACC deaminase production, solubilization of nutrients (potassium, phosphorous, iron), nitrogen fixation, and production of siderophores, phytohormone, osmolytes, antioxidants, and exopolysaccharides. These beneficial microorganisms can be used as a tool for sustainable agriculture to cultivate crops under adverse climatic conditions. Keywords

Climate change · Microorganisms · Abiotic stress · Rhizomicrobiome · Greenhouse gases · Drought · Salinity

4.1

Introduction

Climate change is altering the pattern of weather phenomena such as rainfall, temperature, etc., due to enhanced greenhouse gas effect. The usage of fossil fuels and biological activities of organisms have emitted gases that have shifted earth’s weather patterns and increased atmospheric temperature (Farooqi et al. 2022). Anthropogenic activities have contributed to increase annual mean temperature by 1 °C on earth following industrialization. It has been anticipated that by 2052, the annual mean temperature will rise by 1.5 °C in comparison with the pre-industrialization (Fawzy et al. 2020). Greenhouse gases (GHGs) such as CO2, CH4, and N2O are the major contributors to increase the temperature and lead to greenhouse effect globally that are the threats to ecosystems (Fiodor et al. 2021). The elevated climate change is directly or indirectly affecting the plant– microbiome association. Climate change is affecting ecosystems on the earth by changing the environmental conditions (such as temperature, light, humidity, salinity, drought, and floods) (Barnes and Tringe 2022). Anthropogenic activities have also affected the climate and caused diversity loss of animals and plants (Cavicchioli et al. 2019). The rise in levels of CO2 impacts the growth, quality, and yield of crops (Tripathi et al. 2022). The agriculture sector has been adversely affected by climate change in comparison with other sectors as it is more sensitive to climate change (Warsame et al. 2021). The changes in climate limit the growth, development, and yield of the agricultural crops worldwide. Climate change affects the photosynthesis rate and physiological responses in different plants (Chaudhry and Sidhu 2022). The ecosystem on earth contains flora and fauna and is susceptible to changes in temperature and other adverse conditions. The microorganisms are the most diverse organisms on earth and contribute around 60% of its total biomass (Bar-On et al. 2018). Soil provides a habitat and nutrients that support billions of macro- and microorganisms (Dubey et al. 2019). Microorganisms living in soil are very diverse

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as the soil properties and nutrients vary according to the geographical conditions. The microorganisms developed adaptations according to the environmental conditions via modulation of biogeochemical cycles in that particular niche. For example, the halophilic microorganisms proliferate more under high salinity and pH conditions. The changes in type of soil organic matter, redox potential, minerals, and nutrients affect the microbiome in soil and develop richness of specific microorganisms that can survive/adopt under altering conditions (Jansson and Hofmockel 2020). The soil microorganisms have a complex networking system between the microbial communities and plants that influenced the abundance of specific community and shape the host plant. The climate change directly or indirectly affects the interlinking networks between microbes and plants and affects the function and composition of the ecosystem (Classen et al. 2015). Plant and microorganisms have a significant interkingdom interaction in soil. The species richness of higher plants increases the microbial growth and biomass. However, the microbial respiration and carbon use efficiency were not affected significantly (Naylor et al. 2020). The elevation in level of CO2 alters the amount and quality of plant C allocated belowground that change functional microbial communities related to the C and N cycle in response to climate change (de Vries and Griffiths 2018). Microorganisms such as algae utilized the atmospheric CO2 and help to alleviate the abundance of CO2 in the atmosphere resulting to control the climate change. Microbial communities in soil sequester and decompose the C from the environment and maintain the soil topography, texture, and plant species in that particular ecosystem (Classen et al. 2015). Climate change has also been altered due to increase in the release of reactive nitrogen into the soil, water, and atmospheric systems. The rise in the anthropogenic nitrous oxide emissions from agriculture into the atmosphere is one of the factors for the increase in the concentration of the reactive nitrogen. Nitrogen-fixing microorganisms have the ability to reduce the emission of N2O from rhizosphere. The decomposition of nodules in the soil is the main source of the emissions of the N2O into the atmosphere. In a study, an engineered (nosZ+) nitrogen-fixing strain Bradyrhizobium diazoefficiens having improved efficiency of nitrous oxide reductase enzyme significantly reduced the emission of nitrous oxide in soya bean nodules under field conditions. Such engineered strains can be used to reduce the emission of nitrous oxide in leguminous crops that help to mitigate greenhouse gas emissions (Minamisawa 2022). It is well known that microorganisms have very fast adaptability and diverse in nature (Dubey 2021). Microorganisms may also emit GHGs via decomposition of organic matter during their metabolic activities (Ishfaq et al. 2021). However, they also have the potential to minimize the emission of these GHGs via their utilization as energy source from environment and through decomposition of organic matter under anaerobic conditions (Tang et al. 2022). Microorganisms help to remediate the soil and environmental pollutants either their remediation to non-toxic substances or accumulation to minimize their adverse effects on plant growth (Guarino et al. 2017). The rhizospheric region is a complex network for plant–microbe

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communications and rich source of nutrients for active microbial communities. The rhizospheric microbial community play a significant role in adaptation to climate changes for plant growth and protection (Alshaal et al. 2017). PGPRs are the main microorganisms that thrive in the rhizospheric region and are the driving force for enriching soil nutrients and improving soil fertility (Basu et al. 2021). These microorganisms are influenced by the root exudates and show a symbiotic relationship with the plants (Chai et al. 2022). These factors such as root exudates and metabolites can be used for engineering of microbial communities in rhizosphere to combat with different biotic and abiotic stresses. The microorganisms either directly or indirectly influence the growth and development of plants under different stress conditions via production of stress-responsive proteins, enzymes in the cells, and various extracellular metabolites. The biochemical compounds produced by microorganisms modulate the root architecture and elongation of roots and promote healthy growth of roots and increase the biomass of plants.

4.2

Rhizomicrobiome

Rhizomicrobiome refers to all the culturable and unculturable microbial populations inhabiting the rhizospheric region as presented in Fig. 4.1 (Vandana et al. 2021). It plays a vital role in growth promotion and protection of plants under various stress

Fig. 4.1 Microbial communities in rhizosphere region

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conditions. These microbial communities are changed and adopted according to the metabolites and root exudates secreted by the host plants. Rhizosphere is the specific region in soil for interaction of plant and microorganisms. This interface is well known for the presence of nutrients, greater microbial activities, and biodegradation of several chemical compounds. The presence of enriched microbial diversity in the rhizosphere is attributed to the “Rhizospheric effect”. This phenomenon involves the attraction of microbial population towards the organic compounds secreted by budding plant roots (Morgan et al. 2005). It creates an exclusive niche that allows greater plant–microbe interaction in response to certain signals via activation of several regulatory pathways (Alawiye and Babalola 2019). The beneficial plant–microbe interaction leads to enhanced plant growth and soil fertility via nutrient recycling in soil (Nadarajah and Abdul Rahman 2021). Rhizospheric microbial communities have changed according to the climate zones within different rhizospheric regions such as endo-rhizosphere (most active zone with rhizospheric activities), rhizoplane (intermediate zone with actual plant root– soil interface), and ecto-rhizosphere (rhizospheric outer layer up to bulk soil) (Eckstein et al. 2018). Rhizomicrobiome comprises with diversity of bacteria, archaea, algae, fungi, oomycetes, protozoans, viruses, nematodes, and arthropods. However, bacteria and fungi are found most prominently to cover the maximum diversity. Soil microbial enzymatic activities are responsible for plants’ growth and development that are affected by various environmental factors like water potential, humidity, salinity, light, pH, and temperature (Burns and Strauss 2013). The changes in climate affect variety of agroecosystem functions including plant–microbe interactions and biogeochemical cycles, that eventually affect the plant productivity (Burns and Strauss 2013; Bojko and Kabala 2017; Dutta and Dutta 2016). Climate change is a consequence of global warming and it results in rise in mean air temperature, rise sea level, increased CO2, threats to flooding, extreme rainfall events and droughts (Dutta and Dutta 2016) (IPCC 2013). The co-evolution of microbiome under the different climatic conditions is dependent to host plants via providing the essential vitamins, amino acids, and other effector molecules that regulate growth of plant-associated microbial communities and maintain their composition in the rhizosphere (Banerjee and Roychoudhury 2018). The plant-linked microbial communities help plants for better development by solubilization and transportation of nutrients such as phosphorus, iron and potassium, phytohormone production, and nitrogen fixation. Additionally, it protects the plant via induction of systematic resistance and controls the pathogens through production of antimicrobial compounds (Haider et al. 2022). The microbiome composition is affected by various abiotic and biotic components like soil type, climatic conditions, and signalling molecules released by either plants or microorganisms (Zhang et al. 2021). The population of microorganisms within rhizosphere has a direct relation with the soil type, its properties (physical and chemical such as bulk density, porosity, pH, electrical conductivity, water-holding capacity), and plant-secreted metabolites (Jamil et al. 2022). The metabolites of plants play a vital role in framing rhizomicrobiome

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composition by altering the chemical properties in rhizospheric region and regulate the growth for specific microbial communities (Mahmud et al. 2021). The root exudates and nutritional components of the plants vary according to the developmental stage that directly affects the microbial composition at different maturity stages. For example, the exudates from roots of Arabidopsis thaliana gathered during fast- and slow-growing stage. It was observed that the density of bacteria in the soil treated with fast-growing exudates of root did not vary remarkably from the control, but in the soil treated with slow-growing root exudates, the bacterial density was significantly low (Zhao et al. 2021). Rhizomicrobiome guard plant health via acquisition of nutrients, induced resistance to abiotic and biotic stresses, production of siderophores, phytohormones, and increase soil fertility. A number of studies have been done on diverse microbial populations to analyse the beneficial effects and raise the economic value of different agricultural crops such as rice, maize, wheat, medicinal plants, and vegetables (Baez-Rogelio et al. 2017; Kumar 2016). The use of microorganisms beneficial to plants is a sustainable approach to ensure continuous food supply without deteriorating soil health and environment. Additionally, these microorganisms have greater adaptability towards the climate change and promote plant growth under different abiotic stress conditions.

4.3

Rhizomicrobiome under Climate Change

Microorganisms play a vital role to regulate biogeochemical cycle of elements that are essential for life such as sulphur (S), phosphorous (P), carbon (C), and nitrogen (N) under different climatic conditions. The climate change is mainly due to production of three major greenhouse gases (CO2, CH4, and N2O), and these gases are produced by different natural and anthropogenic activities, while a fraction of these GHGs are produced by few microorganisms during their metabolic activities in nature. The rhizomicrobiome population like algae, fungi, bacteria, and archaea affect climate change in both ways. These can contribute to global warming through degradation of soil organic matter and as a result increases the flux of CO2 in the atmosphere. The degradation of soil organic matter by microorganisms contributes positively to rising global temperature. Microorganisms have the dual abilities to produce and consume these GHGs in the environment, and they can transform and recycle these gases (Abatenh et al. 2018). Microorganisms can easily uptake, store, and release the gases during its metabolic activities. Anthropogenic activities enhanced the carbon and nitrogen in the environment that leads to microbial activities to convert them into GHGs (Tiedje et al. 2022). On other side, microorganisms have the ability to utilize these GHGs during their metabolic pathways such as methanotrophs utilize methane as a source of energy for their metabolic activity and survival (Mistry et al. 2019). The climate change affects the below- and above-ground terrestrial ecosystems directly or indirectly. The direct effects that are felt above the ground include increase in CO2 and N2O concentration, increase in temperature, and changes in

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rainfall pattern. These changes affect the metabolic activities of the microorganisms that modulate different ecosystem processes like carbon sequestration, nitrogen mineralization, and decomposition of organic matter (Kannojia et al. 2019). The composition, function, and abundance of microbial community changed under extreme environmental conditions such as climate warming or environmental changes (Abatenh et al. 2018). The agricultural ecosystem is predominantly dependent on the microbial communities associated with plants under climate change as they play an integral role in tolerance to different biotic and abiotic stresses. The wide variety of the microorganisms in various ecosystems plays a very vital role in controlling the climatic variations because of versatility in their metabolism and adaptability in different environmental conditions (Kannojia et al. 2019). The climate change effects tend to cause more stresses over the crops worldwide (Backer et al. 2018). Microorganisms can lower the negative impacts of climate change on plants by improving soil texture and secreting extracellular compounds like hormones, secondary metabolites, antibiotics, and different signalling molecules. The rhizomicrobiome has shown a great potential in improving plant yields and developing resilience towards the stresses under different climatic conditions (Sinha et al. 2022).

4.3.1

Effects of Temperature

Emission of GHGs has increased the temperature globally. The change in temperature is one of the most important factors that influenced the soil microbial community and organic matter in soil. The microorganisms control the carbon loses from the soil to atmosphere, although their response to the warming of the climate is uncertain and generally short-lived (Backer et al. 2018). Climate change and global warming have strongly affected the plant-associated microbial communities and pronounced variabilities in C and N cycling. A study by Donhauser et al. (2021) reported the impact of rise in temperature on metabolic activities and microbial communities in high mountain soils. The microbial communities for carbon substrate decomposition were more capable for decomposition of recalcitrant organic matter under high-temperature conditions as compared to lower. Conversely, at 35 ° C the genes involved in degeneration and alteration of microbial cell walls were up-regulated. Moreover, a shift in microbial communities towards mineralization and assimilation of N were observed at high temperature (Donhauser et al. 2021). The richness of bacterial population may increase in the presence of elevated temperature conditions (Lin et al. 2017). The temperature cannot directly impact the microbial community linked to plants, but it affects indirectly by changing the plant physiology, vegetation, root exudation, and evo-transpiration, which eventually affects the plant-associated microorganisms (Deltedesco et al. 2020). An increase in microbial biomass was observed under different experimental conditions with elevated temperature. However, the biomass was decreased under long exposure of high temperature (Kannojia et al. 2019). Another study by Dastagir

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(2019) observed that the rise in temperature likely increased the carbon emission via increased rate of fungal decomposition. The temperature rise has also increased the levels of nitrogen (N) in the soil, which negatively impacts the growth of microbial communities. The effect of temperature increases to alleviate CO2 emission, and change in microbial diversity in tropical forest was observed by Nottingham et al. (2022). The microbial growth specific to bacterial taxa was shifted towards thermophilic microorganisms with a temperature change from 3 to 8 °C. The overall composition of microbial communities was adapted and enriched towards thermophilic taxa and lost with microbial groups detected at lower temperature (Nottingham et al. 2022). The temperature rise or warming increased the population of saprophytic fungi and actinomycetes in soil, increased microbial diversity related to C and N assimilation (Gang 2019), and reduced population of arbuscular mycorrhizal fungi in wheat (Peñuelas-Rubio et al. 2022). Notably, the temperature increase and warming affected diversity of soil microorganisms and their activity of enzymes that leads to change in soil texture and biogeochemical cycles.

4.3.2

Effects of CO2 Elevation

Climate change occurs due to elevation of CO2 concentration in the atmosphere. A rise in concentration of CO2 (280–415 PPM) in 2022 was detected by Mount Loa Observatory, Hawaii. It is also predicted that the CO2 concentration can reach up to 936 PPM by 2100 (IPCC report 2013). The latest modelling suggests that the global average mean temperature could rise by 2.5–5 °C by the end of this century (Waqas et al. 2021). It has been expected that in future due to changes in climate the temperature and CO2 concentration will rise. The rise in CO2 level boosts the photosynthesis process in different plant species, which increases the photosynthetic carbon input into the soil and that is utilized by the microorganisms in different metabolic activities. Although the research observations have not been consistent regarding the effects of increased CO2 concentration on the soil nitrogen, phosphorous, and carbon, the varying change in soil carbon and nutrient availability with increased CO2 levels is due to response of the soil microorganisms, which are the drivers of the nitrogen, phosphorous, carbon, and other nutrients (Jin et al. 2020). The lesser availability of nitrogen combined with elevated levels of CO2 supports more growth of fungi over bacteria as fungal hyphae uptake the nitrogen more efficiently (Deltedesco et al. 2020). Gang (2019) reported that elevation in CO2 levels decreased gram-positive bacterial population in soil. The long-term exposure of elevated CO2 and temperature increased nitrification rate of ammonia-oxidizing microbial communities under controlled conditions (Waqas et al. 2021). The nitrifier community was stable under elevated CO2 and temperature, while the sensitivity in ammonia-oxidizing bacteria was higher than ammonia-oxidizing archaea. The impact of CO2 elevation on microbial communities thriving in rhizosphere was observed in desert ecosystem

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of Mojave by Nguyen et al. (2011). The elevation in CO2 level changed the shape and structure of the microbial communities. There was an increment in the population of Basidiomycota (fungi) and decrease (43%) in the population of gram-positive microorganisms under the elevated CO2 levels.

4.3.3

Effect of Salinity

The measure of salts and minerals that can dissolve in water is regarded as soil salinity. The soil–water extract contains minerals like Cl- (chloride), Na+ (sodium), HCO3- (bicarbonate), Ca++ (calcium), NO3- (nitrate), K+ (potassium), Mg++ (magnesium), and SO4- (sulphate). The higher amount of these minerals causes salinity (Yan et al. 2015). The problem of salinization is affecting several countries around the world (Srivastava et al. 2019). The soil salinity affects the water movement (water logging), soil structure, growth of plants, and diversity of microorganisms in the soil. The soil salinity can occur by different natural sources and elevated by anthropogenic activities. In arid and semi-arid climates where the annual rainfall is less than 27 cm, soil salinity occurs naturally. Salinity in soils that have shallow water table can be developed due to loss of water through evaporation that leads to the concentration of the salts in the soil. The improper irrigation practices and low water quality also increase soil salinity to the agricultural lands (Artiola et al. 2019). The increased demand of food with growing population is a challenge for producers and agri-entrepreneurs with dealing the issues of deteriorating soil health under climate change globally. The elevation in temperature, changes in rain patterns, reduction in supply of fresh water, and rise in the frequency of extravagant events such as drought, tsunamis, floods, cloud burst need to be addressed jointly using a combination of integrated approaches. It also requires depth investigations to the cause for dealing with these issues. Salinity is a major challenge globally that affected 20% of the cultivated land and 30% of the irrigated land (Shilev 2020). Yan et al. (2015) reported that the electrical conductivity >4 dSm-1, pH > catechols)

Wheat

Tomato

Astragalus sp.

Strawberry

44–53% increase in Fe content of wheat cultivars (HD-3086 and HD-2967)

Fe concentration roots was threefold higher

Increase in the expression of FRO2, IRT1, AHA2, and FIT1 genes

Improved the iron concentration up to 33.12% Increase in chlorophyll content and reduced phenolic contents

Potato

Maize

Groundnut

Siderophore and chelation

Auxin production and cellular Fe transport Siderophore production

Tomato

Raspberry

Maize

Siderophore production

Acidification, chelation and exchange reactions Siderophore production

13–32% increase in shoot length and 62–84% increase in root length After 3 weeks, Fe content was only detectable in inoculated plants 75% increase in the Fe content of leaves and 34% increase in yield 47% increase in the Fe content of 70-day old iron-starved plant, compared to control 34.75% increase in soil available Fe compared to control Fe uptake with increased plant allocation

Mung bean

(continued)

Yadav et al. (2021)

Nagata (2017)

Kumari et al. (2018) Sharma et al. (2016) Orhan et al. (2006) Radzki et al. (2013) Pratiwi et al. (2016) Housh et al. (2021) Mushtaq et al. (2022) DelaporteQuintana et al. (2020) Zhou et al. (2018)

Reference Roriz et al. (2021)

Microorganisms Sphingobium fuliginis

Improvements 62% increase in Fe content in roots

Table 5.1 List of iron-solubilizing microbes using various mechanisms Crop Soybean

Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability

Mechanism(s) Ferric chelation, FRO2, IRT1, and FER4 genes expression increased Siderophore production

5 119

Lentil

Alfalfa

Maize Wheat

Siderophore production

Fe transporters, ferric chelate reductase

Fe transporters

Organic acid production

Rhizobium leguminosarum-PR1, Pseudomonas sp. PGERs 17

Glomus intraradices, Glomus mosseae, Glomus aggregatum, Glomus etunicatum Rhizophagus irregularis DAOM197198 Arthrobacter sulfonivorans DS-68

Crop Wheat

Mechanism(s) Siderophore production

Microorganisms Arthrobacter sulfonivorans (DS-68) and enterococcus hirae (DS-163)

Table 5.1 (continued)

Iron concentration increase by 2.0- and 2.4fold in root and shoot, respectively

Increase in the root Fe content

Improvements 14–20% increase in plant growth and yield. Fe or Zn content was enhanced by 75% in wheat grains over chemical fertilizer treatment Increase in nodulation (1.6-fold) and Fe content (2.1-fold) was recorded compared to control Increased expression of MsFRO1 in roots, 1.2-fold increase in Fe acquisition in roots Kobae et al. (2014) Singh et al. (2017b)

Rahman et al. (2020)

Mishra et al. (2011)

Reference Singh et al. (2018)

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5.2.1.5 Mechanism of Fe-Solubilizing Microbes The enriched uptake of Fe as augmented by iron-solubilizing microbes or PGPR can be accredited to the number of mechanisms deployed by these microbes. Some of those mechanisms are discussed here and also briefed in Table 5.1. Siderophores are the low-molecular weight compounds that are principally involved in sequestering Fe3+ ions from the surrounding. On the basis of ligands formed to chelate Fe3+, catecholates, hydroxymates, and carboxylates are the three classes of siderophore and are produced by both gram-negative and gram-positive bacteria (Hider and Kong 2010). The concentration of available iron in soil is to the tune of 10-18 M, low enough to make the microbes produce siderophores for their own survival. These microbial siderophores chelate the Fe3+ and transform it to Fe2+, which is readily taken up by the plants. Diverse genera microbes such as Pseudomonas, Bacillus, Agrobacterium, and Rhizobium have been reported to produce a varied range of Fe-chelators (Esitken 2011). Several microbes secrete organic acids and thereby lowering the soil pH and increasing availability of Fe. Organic acids such as citrate, malate, oxalate, and formate have been secreted by microbes and facilitate increased nutrient availability. It was reported for dicotyledonous plants that citrate is the prominent supplier of Fe in the xylem as Fe3+-citrate. This mechanism is well-adapted and recommended for facilitating Fe availability in calcareous and high pH soils (İpek and Eşitken 2017). Certain microbes can regulate the root structure architecture in the rhizosphere zone by secreting metabolites or signaling hormones. Indole-3-acetic acid (IAA) is the active form of auxin produced by several rhizosphere-dwelling microbes. IAA plays an important role in signaling responses under Fe-deficit induced conditions. Reports suggest that addition of IAA induces signaling that reduces ferric ion (Sadeghi et al. 2012) and upregulates the expression of IRT1 and FRO2 genes, besides architectural changes in root (increase in root hairs and formation for lateral roots) (Wu et al. 2012). The indirect inducible mechanisms executed by ironsolubilizing microbes include improvement in the photosynthetic ability of the plant by increasing the chlorophyll content and by stimulating the expression of defense-related genes (Zhang et al. 2009).

5.2.2

Zinc (Zn)

5.2.2.1 Zn Status in Soils Primarily through geochemical and pedochemical weathering processes, small elements, such as zinc, are inherited by soils from rocks. Zn content in the lithosphere is approximately 800 ppm on average (Goldschmidt 1954). Most minerals have 10 to 300 mg/kg zinc. Zn in soils depends on parent materials. Granite and gneiss can produce low-zinc soils (Helmke et al. 1977). In leached, acidic, or sandy coastal soils, Zn concentrations are low (Alloway 2008a, b). Zn presence in soil varies on pH, soil type, weathering, climate, and other factors (Saeed and Fox 1977). Zinc deprivation can occur in any part of the world, and practically, all plant species benefit from the addition of zinc to their growing medium. The deficit can be

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found in a diverse collection of semi-arid regions. It has a propensity to be more severe in areas with calcareous soils, tropical regions with severely weathered soils, and sandy soils in a wide range of climate zones. More than 30% of the world’s arable land has insufficient zinc levels (FAO WHO 2002). Zn deficits can be found all over the world, although they are most prevalent in rice-based ecosystems in the Asia-Pacific area (Tisdale et al. 2009). About 36.5% of Indian soils do not have adequate zinc (0.6 mg/kg) (Shukla et al. 2017, 2018, 2021).

5.2.2.2 Roles of Zn in Plants Zn is a cofactor and metal activator for a wide range of enzyme functions in enzymatic systems. Due to zinc’s poor translocation in plants, a steady, easily accessible source is essential for proper plant growth. Zinc was the first element proven vital for all life, including humans, animals, plants, and microorganisms (Kabata-Pendias 2000). Zinc plays a critical role in plant metabolism because of its influence on enzymatic activities (Tisdale et al. 1984). Detoxification of the superoxide radical is facilitated as a result. Cu-Zn-SOD is the enzyme that is in play here (copper–zinc superoxide dismutase). The metabolism of carbohydrates is affected by the presence of zinc. Carbonic anhydrase also contains Zn as a cofactor (Alloway 2004). In addition to its role in a plant’s ability to ward against disease, zinc is involved in photosynthesis, the metabolism of proteins, and the formation of pollen (Gurmani et al. 2012). In addition to this, zinc causes an increase in the amount of chlorophyll and antioxidant enzymes present in plant tissues (Sbartai et al. 2011). 5.2.2.3 Zn-Solubilizing Microbes Zn-solubilizing microorganisms are more effective than chemical fertilizers. Microorganisms are gaining popularity for sustainable agricultural production and fertility restoration. Zn-solubilizing microorganisms from agriculture soils have been studied as plant growth promoters (Goteti et al. 2013). Chemical fertilizer application partially satisfies plant demands because 96–99% of applied Zn is precipitated in soil through different physicochemical processes (Saravanan et al. 2004). A wide variety of bacteria, such as Thiobacillus thiooxidans, Acinetobacter, Bacillus, Pseudomonas, and Thiobacillus ferrooxidans, have the ability to convert an inaccessible form of zinc into an easily accessible form (Cunninghan and Kuiack 1992; Saravanan et al. 2007; Goteti et al. 2013). In addition, endophytic microbes also have a crucial impact on Zn accumulation in food grains (Gosal et al. 2010). In our earlier studies, Bacillus subtilis DS-178 and Arthrobacter sp. DS-179 increased Zn concentration in wheat tissues in Zn-deficient soils by 75% over the uninoculated control (Singh et al. 2017a, b, 2018). Sirohi et al. (2015) reported that Pseudomonas fluorescens was suitable for enhancing Zn content in wheat grains. In Argentina, Rosas et al. (2009) found that inoculation of Pseudomonas aurantiaca increased wheat grain production by 36% on sandy loam soil. The benefits that diverse crops receive from the application of various Zn-solubilizing microbial strains are outlined in Table 5.2.

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Table 5.2 Benefits of different crops through using various Zn-solubilizing microbial strains Microbial Strain Pseudomonas spp.

Crops Okra

Bacillus altitudinis (BT3 and CT8)

Chickpea

Bacillus megaterium

Chili pepper

Bacillus subtilis + AM fungi

Wheat

Bacillus sp. ZM20, Bacillus aryabhattai ZM31, B. subtilis ZM63, and B. aryabhattai S10 Bacillus subtilis QST713

Maize

Bacillus pumilus Pseudomonas pseudoalcaligenes

Paddy

Pseudomonas fluorescens Sasm05

Sedum alfredii

AMF Rhizophagus irregularis

Barley

Rahnella sp. strain JN6

Rapeseed

Wheat

Benefit to crops Effective on plant growth promotion and the enhancing Zn content in the Okra fruit Chickpea growth was improved and Zn uptake by the plant was enhanced by 3.9–6.0%. Enhanced plant growth, nutrient uptake and yield Bacillus subtilis + AM fungi enhanced total chlorophyll and Zn content 23% higher Zn was recorded in treated plants compared to uninoculated control Increments in the concentration of P and Zn in grains and Zn harvest index Enhancing growth-related parameters, such as chlorophyll, carotenoid, and antioxidant enzymes catalase (CAT), peroxidase (PO) Promoted rooting and root development, in which the specific root length (SRL), average number of root tips (ART), plant growth, elevated Zn uptake of plant, biomass and the chlorophyll content by more than 40%, and root Zn content by 40% A Zn concentration was enhanced in barley due to AMF inoculation

Inoculation of Rahnella significantly enhanced dry weights, as well as Zn content in rapeseed tissues than those without inoculation grown in soils amended with Zn (200 mg kg-1)

Reference Karnwal (2021) Kushwaha et al. (2021) Bhatt and Maheshwari (2020) Yadav et al. (2020) Mumtaz et al. (2020) MorenoLora et al. (2019) Jha (2019)

Wang et al. (2019)

WattsWilliams and Cavagnaro (2018) He et al. (2013)

5.2.2.4 Mechanism of Zn-Solubilizing Microbes Microbes enhance Zn availability in soil, plant parts, and food grains through different mechanisms. Plant and microbial-derived phytosiderophores and

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Zn-chelating compounds can mobilize and solubilize Zn (Obrador et al. 2003). Whiting et al. (2001) found that Zn chelator metallophores generated by bacteria affect Zn bioavailability and uptake by plant roots. Bioinoculants of Azospirillum lipoferum and Pseudomonas sp. can solubilize ZnO, Zn(OH)2, Zn3(PO4)2, ZnCO3, and ZnSO4, increasing rice plant Zn availability in soil (Tariq et al. 2007). Root exudates, through a series of biochemical reactions, increase the amount of zinc that is soluble in soil solution (Zhang et al. 2010). The patterns of root exudation and the activities in the rhizosphere can both be influenced by microorganisms (da Silva et al. 2014; Singh et al. 2017b). Organic acids dominate root exudates, especially in rhizosphere metal solubilization (Luo et al. 2014). According to Kim et al. (2010), the micronutrient absorption and translocation in plant tissues were greatly increased by the oxalic and citric acids that were released by Echinochloa crusgalli. Chen et al. (2014a, b) found that plant growth-promoting rhizobacteria changed root exudate patterns and solubilized precipitated metals. Microorganism proton excretion may acidify the rhizosphere and boost nutrient availability. Organic acid profile of wheat root exudates was modified because of inoculation of Arthrobacter sulfonivorans DS-68 and Arthrobacter sp. DS-179 (Singh et al. 2017b). Plant growth-promoting microbes also enhance Zn accumulation in crop plants by modifying root morphology and anatomy (Wang et al. 2014; Singh et al. 2017b). Plant growth-promoting microbes can enhance expression level of Zn transporter genes (ZIP gene) in crop plants resulting in increased accumulation of Zn in plant tissues (Krithika and Balachandar 2016; Watts-Williams and Cavagnaro 2018). In addition, plant growth-promoting microbes can reduce antinutritional factors such as phytic acid in grains resulting in increased bioavailability of micronutrients in food grains (Vaid et al. 2014).

5.2.3

Copper (Cu)

5.2.3.1 Cu Status in Soil Chalcopyrite (CuFeSO2) mineral is the main source of copper in the earth’s crust copper and is mainly found as sulfides. Additionally, it can be found in secondary minerals and organic complexes, a portion of which can be found in soil solutions and on the exchange site of soil colloids. The amount of copper in various rocks varies greatly. Sandstone (8 ppm) and limestone (7 ppm) had some of the lowest copper contents, whereas granite schist had the highest quantity (87 ppm Cu). The age of the soil and the length of leaching appear to have an impact on the distribution of Cu in addition to climate and parent material. According to Kanwar and Randhawa (1974), the total Cu status of Indian soils is between 1.8 and 960 ppm, whereas the available Cu content is between traces and 1.8 ppm. 5.2.3.2 Role of Copper in Plant The criteria for essentiality of copper were first time clearly given by Sommer in 1931. The oxidase activity of the catalases, peroxidases, and polyphenols is increased by copper. It affects metabolic activity of N. Even though copper is not

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a part of the chlorophyll molecules, it is necessary for the synthesis of porphyrin, which is a precursor to chlorophyll. It helps in translocation of sugar. Most famous plant diseases like “dieback” or “exanthema” in fruit trees and “reclamation disease” in cereals are caused by deficiency of Cu. Numerous metalloproteins that can participate in oxidation/reduction reactions and accept and donate electrons are known to be connected to Cu. The fact that Cu is present in cytochrome oxidase indicates that it plays a crucial metabolic role and that its ability to build organic complexes is equally important. Typically, copper is found as a component of proteins, primarily enzymes, and these play an essential role in metabolism (Shorocks and Alloway 1988).

5.2.3.3 Cu-Solubilizing Microbes Cu-solubilizing microbes (Cu-SM) are those microorganisms, which have capacity to solubilize the insoluble Cu. Bacteria can produce plant growth-promoting substances, which improve growth and uptake of copper (Dell’Amico et al. 2008). Microorganisms capable of solubilizing Cu have enormous potential in comparison with chemical sources of plant nutrition like fertilizers. It is becoming increasingly popular to employ microorganisms in reviving depleted soils and ensuring the continued growth of crops. Many crop soils have been found to contain Cu-solubilizing microorganisms, which have been studied for their potential as plant growth enhancers (Goteti et al. 2013). Bacterial cultures engineered to produce enzymes capable of Cu solubilization can transform Cu from an insoluble form into a soluble one. Zinc-solubilizing microorganisms, which have the remarkable capacity to convert various inaccessible forms of metals to readily available forms, can alleviate this shortfall. Cu-solubilizing bacteria are effective replacements because they can supply plants with copper by dissolving copper complexes in soil. The solubilized Cu metals are produced through a reaction involving complexing compounds, hydrogen ions, and the redox reactions occurring on cell surfaces and in cell membranes. These bacteria have the ability to produce siderophores, growthstimulating substances, antimicrobial compounds, and vitamins (Goteti et al. 2013). Different plant growth-promoting microbial strains and their effect on different crops are presented in Table 5.3. 5.2.3.4 Mechanism of Cu-Solubilizing Microbes In order to promote plant growth, PGPR microorganisms colonize root zones, multiply, and compete with other rhizobacteria (Kloepper and Okon 1994). These bacteria stimulate plant growth through the processes of nutrient mobilization and absorption, as well as through the production of phytohormones (Glick 2012). The colonization of root zones by PGPR, which also simplifies complex copper compounds by dissolving them into simpler ones, stimulates plant growth (Fig. 5.1). The three mechanisms include redox reaction, acidification, and chelation (Brandl and Faramarzi 2006) and are related to increase Cu availability in soil by microbes. Bacteria that oxidize sulfur, including Acidithiobacillus species, are the catalysts behind the transformation of insoluble metal sulfides, like copper sulfide (CuS), into

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Table 5.3 Inoculation effect of different microbial strains of Cu-solubilizing microbes on crops Microbial strain Bacillus sp. EhS5 and EhS7

Crop Ryegrass

Stenotrophomonas maltophilia

Maize

Microbacterium oxydans, Pseudomonas thivervalensis, and Burkholderia cepacia

Rape

Pseudomonas libanensis TR1 Pseudomonas reactans Ph3R3

Brassica oxyrrhina

Bacillus megaterium BHU1, Arthrobacter chlorophenolicus BHU3, Enterobacter sp. Enterobacter cloacae subsp. dissolvens MDSR9

Wheat

Burkholderia sp. GL12, Bacillus megaterium JL35, Sphingomonas sp. YM22

Maize

Stenotrophomonas maltophilia

Oatmeal

Anabaena

Rice

Providencia sp. PW5

Wheat

Soybean and wheat

Effect on crop Single or combination inoculation enhanced ryegrass root length, diameter, surface area, forks, biomass yield, and Cu content Enhanced plant growth, biomasses and uptake of Cu in root (77.4%) and stem (112.0%) in maize as compared to control M. oxydans, P. thivervalensis, and B. cepacia increased Cu uptake by 113.38, 66.26, and 67.91%, respectively, in rape TR1 and Ph3R3 inoculation improved B. oxyrrhina growth, leaf water, and Cu content Significantly enhanced content of Cu 83.0%, under pot condition and 98.6%, under field condition

Reference Ke et al. (2021)

Inoculation with Enterobacter cloacae subsp. dissolvens MDSR9 increased yield, plant height, root dry weight, root volume, and Cu content in soybean (R5) and wheat (panicle initiation stage), as well as in seed at maturity. Inoculation with the bacteria increased maize root (48–83%) and above-ground tissue (33–56%) dry weights compared to uninoculated controls. Cu content of roots and above-ground tissues increased by 69% to 107% and 16% to 86% in bacterialinoculated plants, respectively Stenotrophomonas maltophilia inoculation in Oatmeal increased the Cu accumulation in shoot by twofold over the uninoculated control Anabaena led to enhance Cu content by 16–26% in root, 10–35% in leaves and 70–206% in grain over the uninoculated control Providencia sp. PW5 increased the wheat grain yield significantly over the uninoculated control. Cu accumulation was also 45% higher than uninoculated control due to Providencia sp. PW5 inoculation

Ramesh et al. (2014)

Gopi et al. (2020)

Ren et al. (2019)

Ma et al. (2016) Kumar et al. (2014)

Sheng et al. (2012)

Andreazza et al. (2010)

Adak et al. (2016)

Rana et al. (2015)

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Fig. 5.1 Mechanism of uptake of copper from soil by plant through Cu-solubilizing microbes

soluble metal sulfates (e.g., CuSO4). Metal ions are released from the surface of solids when protons produced by microbes bind to the surface of minerals during the acidification process (Brandl and Faramarzi 2006). It is important to note that a fall in soil pH is also caused by the dissociation of organic acids that are generated by microbes. During the process of complexation, interactions between metals and microbial chelators lead to the formation of complexes at the surface of metalbearing phases. This permits metals to be released from the surface and cationic components to be removed from the crystal lattice (Brandl and Faramarzi 2006) (Grybos et al. 2011). Chelating siderophores for iron have an affinity for copper cations as well (Ferret et al. 2015). A number of the features of methanobactin produced by methanotrophs are similar to those of iron siderophores, including the capacity to remove Cu from insoluble Cu compounds and a binding affinity with pyoverdine (Cornu et al. 2014).

5.2.4

Manganese (Mn)

5.2.4.1 Role of Mn in Plants Manganese (Mn) being an essential micronutrient is critical for plant growth, reproduction, and development. It serves two important functions: one as an enzyme cofactor and second, in biological clusters, as a metal having a catalytic activity

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(Andresen et al. 2018). Mn is an indispensable metal in enzymes like Mn superoxide dismutases (SOD) and oxalate oxidases. However, in many other cases, Mn can be substituted with other bivalent cations viz. copper, zinc, cobalt, magnesium, or calcium. Mn involves in photosynthesis and plant signaling pathways. It acts as cofactors of many respiratory enzymes in plants (Alejandro et al. 2020). Mn is also essential for the neutralization of harmful reactive oxygen species (ROS) generated mainly in the mitochondria, peroxisomes, chloroplasts, and cytosol. It is indispensable in the Mn-SOD (superoxide dismutases), which is found in the mitochondria and peroxisomes and is required for the detoxification of harmful superoxide free radicals (Bowler et al. 1994). In addition to that, another Mn-dependent enzyme is the oxalate oxidase, which is located in the apoplast, where it catalyzes the oxidation of oxalate to CO2 with subsequent reduction of O2 to H2O2 (Requena and Bornemann 1999). Mn also plays an important role in the fatty acid synthesis of the cell membrane, which can be known by the fact that Mn-deficient leaves have been observed to show a 50% decreased concentration of glycolipids and fatty acids in their thylakoid membrane (Constantopoulos 2008). Mn concentration in plants can also affect the cellular elongation and division processes (Broadley et al. 2007). Mn is also an essential cofactor of enzymes for isoprenoid biosynthesis (Kollner et al. 2008). Even Mg can serve as a cofactor of the enzyme terpene synthase, along with Mn, which can alter the plant terpene profile pattern depending on the Mg/Mn ratio in the growth media (Rohdich et al. 2006). Lignin biosynthesis also requires the involvement of Mn. Interestingly, Mg can also be replaced with Mn in the active sites of the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo) with a change in the functional role of the enzyme in the photosynthetic pathway (Bloom and Kameritsch 2017). Mn is also cofactor of Golgi-localized glycosyl transferases, which are vital for protein glycosylation and the formation of hemicellulose and pectin polymers (Eskandari and Gineau 2020; He et al. 2022; Yang et al. 2021). Many other enzymes also need Mn as a cofactor; however, their requirement can be supplemented by Mg in certain instances. Some examples are acid phosphatases (Venkidasamy et al. 2019), decarboxylase like NAD-malic enzyme, dehydrogenaselike PEP carboxylase (Gregory et al. 2009), and also enzymes for abscisic acid and auxin signaling (Schweighofer et al. 2004). Mn can also play a role in various processes associated with plant metabolism like Ca+2 signaling (Hashimoto et al. 2012), purine and urea catabolism (Cao et al. 2010), chloroplast development (Hsieh et al. 2008), DNA repair (Szurmak et al. 2008), and even deposition of cuticular waxes (Hebbern et al. 2009). A deficiency of Mn in plants may lead to chlorosis, delayed maturity, and premature leaf fall. However, an excess of Mn may cause stunted growth and reduced yields.

5.2.4.2 Manganese Status in Soils Mn along with iron plays an important role in forming the organic top layer of the soil where the plant roots are situated and a majority of microbial activities are taking place (Bartlett and James 1993). Therefore, it becomes quite essential to know their content in the soil as its uptake by the plant will be critical in maintaining the food

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quality and improving food production (Adriano 2001). Mn deficiency will take place in plants growing on overlimed acid soils and coarse-textured sandy soils (Martens and Westermann 1991). Soil properties mainly organic carbon and pH affect the availability of Mn to the plants. It has been reported that with every one-unit increase in pH, the solubility of Mn decreases by about 100-fold (Lindsay 1979). Also, organic matter improves the availability of Mn to plants. Tropical soils contain a high content of Mn as compared to other locations, which makes toxicity a more common problem than deficiency (Tena and Beyene 2011). A wide variation has been reported in the total Mn content all over India where 187 to 814 mg kg-1 was estimated from eight soil orders representing 57 benchmark soils (Katyal and Sharma 1991). Similarly, total Mn content from various cultivated acid soils of India viz. Orissa, Jharkhand, Himachal Pradesh, and Kerala were in the range of 159–318 mg kg-1 (Behera and Shukla 2014). However, the average content of DTPA-extractable Mn was found to be 4–7% of the total Mn content representing only a small portion. Moreover, total Mn in the soils was influenced by soil pH and exchangeable cations like K, Ca, and Mg whereas extractable Mn in the soils was only affected by exchangeable cations like K, Ca, and Mg. Even though the total content fails to give an idea of the bioavailability of the metal, it gives a glimpse of the finite soil reserve for the metal present. It has also been reported that high manganese content in the soil can fix native cobalt in the soil, which may restrict the uptake of Co and even show negligible responsiveness toward Co fertilizer treatments (Li et al. 2004). Sharma et al. (2003) also found out that total Mn content in the soil increases with an increase in the clay content of the soil. Also, a positive correlation has been observed between available Zn content and Mn in the soil; however, a negative correlation is seen between B and Mn (Sarker et al. 2018). According to a mapping study of micronutrients in India, recently it was shown that almost 17% of Indian soils are deficient in Mn with 10%, 6%, and 1% being latent deficient, deficient, and acute deficient, respectively. Mn deficiency was particularly observed in rice and wheat-growing sandy loam areas (Shukla and Behera 2019).

5.2.4.3 Mn-Solubilizing Microbes The importance of microorganisms in Mn cycling is becoming much better appreciated. Cycling involves the transformation of manganous ion (Mn+2) to MnO2 (Mn+4), which might occur in hydrothermal vents, bogs, and as an important part of rock varnishes. This oxidation is thermodynamically favored at normal oxygen levels and neutral, albeit its activation energy is very high and the process is slow (Gounot 1994). Leptothrix, Arthrobacter, Pedomicrobium, and Metallogenium are important in Mn oxidation. Microorganisms that can reduce Mn oxides have been known to occur in a wide variety of habitats such as freshwater sediments, manganiferous ores, ocean sediments (Rusin and Ehrlich 1995), Antarctic lakes (Bratina et al. 1998), and in the rhizosphere (Posta et al. 1994). Shewanella, Geobacter, and other chemoorganotrophs can carry out the complementary manganese reduction processes. The number of microbes involved in solubilization of Mn is listed in Table 5.4.

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Table 5.4 Mn-solubilizing organisms from various habitats along with their mechanism of solubilization Microorganism Aspergillus terreus, Aspergillus oryzae, Penicillium species, Penicillium species, Penicillium dalea, and Penicillium Bacillus, Staphylococcus, Synecoccus, Propionibacterium, Micrococcus, Pseudomonas and Vibrio Pantoea sp. MFG10

Habitat Mining sites in Odisha, India

Mechanism of solubilization Organic acid production

Reference Mohanty et al. (2017)

Tuticorin Harbor waters, India

Mn oxidation

Palanichamy et al. (2002)

Lijiahe reservoir, China

Gao et al. (2022)

Leptothrix discophora (Mn Oxidizing Bacteria) and Bacillus polymyxa (Mn Reducing Bacteria) Bacillus altitudinis Cq-3, Pseudomonas flexibilis Cq-32, Bacillus pumilus Cq-35, Pseudomonas furukawaii Cq-40, Pontibacter lucknowensis Cq-48, and Ensifer sp. Cq-51 Lysinibacillus sp.

Soil samples from different districts of Pakistan Chenopodium quinoa rhizosphere

Dissimilatory manganese reduction by transfer of electrons to terminal electron acceptors via extracellular electron transfer causing denitrification simultaneously Production of organic acids and lowering of oxidation– reduction potential of soil Production of organic acids, including malic, gluconic, tartaric, ascorbic, lactic, and oxalic acids

Rafique et al. (2022)

Organic acids production along with bioreduction and direct dissolution of metals Citric acid or gluconic acid

Ghosh et al. (2021)

Bacteria—Roseospira sp. and Sphingomonas sp., Fungi—Cladosporium sp. and Penicillium chrysogenum

Mining sites in Odisha, India Silver mine in in Coahuila, México

Babar et al. (2022)

Huerta-Rosas et al. (2020)

5.2.4.4 Mechanism of Mn-Solubilizing Microbes Mn can exist in a variable number of oxidation states (2 to 7) with 2, 3, and 4 being the most common in biological systems. Mn+2 is the divalent form that is the most soluble and easily accumulated by plants. Soil pH invariably determines the oxidation state of Mn in soil, where at neutral or higher pH insoluble Mn (Mn+3, Mn+4) oxides will form. Microorganisms can also influence their availability to the plant by their oxidation–reduction potential.

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Microorganisms can oxidize Mn by either direct or indirect mechanisms. As compared to abiotic Mn oxidation, microbe-assisted one is five times faster. The production of various chemical metabolites like hydrogen peroxide, free radicals, or any oxidant can cause these types of reactions. Leptothrix and Arthrobacter are known to produce H2O2 to oxidize Mn (Dubinina 1978; Ghiorse 1984). Direct oxidation can occur by enzymatic reactions facilitated through Mn-binding and oxidizing enzymes found in crude or purified extracts. Phanerochaete chrysosporium can use Mn-dependent peroxidase, which oxidizes Mn (II) to Mn (III) with the assimilation of H2O2 (Glenn et al. 1986). Mn reduction process can also be direct or indirect. Indirectly, the metabolic activity of the microorganisms causes a reduction of pH and oxidation–reduction potential values, which often promotes the reduction of Mn. However, the reduction of Mn can directly occur at high pH, which means that bacteria produced a chemical substance causing the reduction. Achromobacter sp. produced citric and malic acid, whereas Acinetobacter johnsonii reduced Mn via an uncharacterized diffusible product (Rusin and Ehrlich 1995). Fungi like Aspergillus and Penicillium also use indirect means to reduce Mn by producing oxalic acid (Mohanty et al. 2017). Reports have confirmed the secretion of formate, oxalate, pyruvate, and salicylate to reduce Mn (Keshavarz et al. 2021). The indirect reduction also occurs via the production of inorganic compounds such as ferrous, sulfide, or different reduced compounds, which may be formed during anaerobic respiration. Moreover, directly the Mn oxides can sometimes act as terminal electron acceptors causing a reduction to take place. Direct reduction involves intimate contact of Mn oxides with the microorganisms. They are reduced directly via an electron transport chain. An experiment was conducted with filtered and cell-free extracts of Bacillus MBX2, which confirmed the requirement of contact between the two (Rusin et al. 1991). Under anaerobic conditions, Mn+4 can act as an electron sink for the re-oxidation of nicotinamide adenine dinucleotide (NADH) rather than oxidative phosphorylation (Francis and Dodge 1988). In such conditions, iron may act as an electron shuttle. Shewanella putrefaciens contain c-type cytochrome when grown anaerobically (Myers and Myers 1992). Cells adapted to Mn(IV) reduction use MnO2 in preference to O2 as a terminal electron acceptor.

5.2.5

Boron

Boron is a non-metal micronutrient essential for plant growth and development (Silva et al. 2011; Warington 1923). Boron is the second most deficient micronutrient, severely affecting the growth of crops on a global scale (Alloway 2008a, b). In India, nearly one-fourth or 23.2% soil samples analyzed exhibited B deficiency (Shukla et al. 2021). Boron is mostly taken by plants as boric acid (H3BO3). However, it can also be absorbed in certain of its anionic forms when soil pH is greater than 7. Normal boron-sufficient plants have B levels between 10 and 200 mg kg-1. Boron is neither an enzyme component nor does it activate any

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enzymes. Boron (boric acid) forms stable complexes with cis-diol-configured chemical molecules (Bolaños et al. 2004).

5.2.5.1 Role of Boron in Plant Metabolism Boron is important for the structural integrity of the cell wall, including its development and stabilization, lignification, and xylem differentiation. B is cross-linked with pectin assembly, glycosylinositol phosphorylceramides (GIPCs), and rhamnogalacturonan-II (RG-II) that regulate the tensile strength and porosity of the cell wall (O’Neill et al. 2004; Voxeur and Fry 2014) (Fleischer et al. 1999; Ryden et al. 2003). B deficiency leads to changes in the chemical composition and ultrastructure of the cell wall, the buildup of hazardous phenols, and the suppression of lignin formation. B-deficit lowers the formation of indole acetic acid (IAA), which causes calcium deficiency in plants. Boron is involved in the calcium uptake process in plants. Boron is essential for the formation of actively growing plant parts, such as root tips, new leaves, and buds. It ensures the health of plant storage tissues and conductive tissues that transmit water, nutrients, and organic compounds to actively growing plant sections (Dordas et al. 2000; Goldbach and Wimmer 2007). All plants require sugars for root development, as well as for the creation of root nodules in legumes such as alfalfa, soybeans, and peanuts. It enhances flower production and retention, pollen tube elongation and germination, and seed and fruit development. It provides crops with drought resilience. Spraying boric acid regularly mitigates the detrimental effects of drought. It promotes pollen germination and pollen tube formation (Cheng and Rerkasem 1993). It facilitates ion absorption by increasing the activity of plasma membrane-bound H + -adenosine triphosphatase (H +-ATPase). It promotes both potassium transport in guard cells and stomatal opening. 5.2.5.2 Deficiency Symptoms and Critical Limits It is thought that plants with B values between 5 and 30 mg kg-1 are B-deficient. The critical B deficiencies for cereals vary from 5 to 10 mg kg-1, while the critical B deficiencies for pulses range from 20 to 70 mg kg-1. Boron soil critical limits are only 0.50 mg kg-1. Boron deficiency symptoms become evident on the terminal buds or the youngest leaves, which yellow and may die under acute B-deficient situations (Brdar-Jokanovic 2020). The internodes become shorter and develop a bushy or rosette-like look. Boron deficiency symptoms include thickened, wilted, or curled leaves; thickened, cracked, or water-soaked petioles and stems; and discoloration, cracking, or decay of fruit, tubers, or roots (Goldbach 2020). In citrus fruits, irregular peel thickness, lumpy fruit, and gelatinous deposits develop because of B deficiency. The disintegration of root crops’ interior tissues manifests as darkening patches known as brown heart or black heart. Increased stem and petiole diameters result in the usual celery stem’s cracking. Typical names given to boron deficiency in different crops are as follows: 1. Heart rot of sugarbeet and marigold. 2. Browning and hollow stem of cauliflower. 3. Top sickness of tobacco.

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4. Internal cork of apple. 5. Cracked stem of celery.

5.2.5.3 Boron Mobilizers or Solubilizes Higher plants’ roots have symbiotic relationships with soil-microorganisms like bacteria and fungus because they serve a critical role in N fixation, chitinase synthesis (a pathogen hazardous to roots), ion acquisition, and improving plant fitness under conflicting ecological conditions (Johansson et al. 2004; Parihar et al. 2020a). Mycorrhizae are the best example of symbiotic relationship with fungi, and roots of higher plants play an important role in improvement of soil fertility and nutrient transportation (Parihar et al. 2020b). Miscanthus sacchariflorus plants infected with mycorrhizae cultivated in naturally sterilized soil conditions showed an increase in total ion concentration of macro- and micronutrients in the root, stem, and leaf, reported by Sarkar et al. (2015). The activity of organic substances generated from plant roots and fungus boosted the availability of these minerals to plants. Mycorrhizae inoculation has an impact on the boron content in plants. Studies have found reduced (Clark et al. 1999), unaltered (Lu and Miller 1989), and improved (Kothari et al. 1990). The boron acquisition in the shoots of mycorrhizae-inoculated plants, but the precise function of mycorrhizal fungi for boron has not yet been established and needs more research. Dixon et al. (1989) reported that boron concentration increased by 11–18% in leaves of rough lemon (Citrus Jambhiri Lush) as well as the exudation of root sugars and amino acids due to inoculation of Glomus fasciculatum over non-inoculation. Inoculation with Glomus etunicatum (WV579A), Glomus diaphanum (WV579B), and Glomus intraradices (WV894) increased boron concentration by 331–689, 261–510, and 284–531% in the shoot of maize plant (Clark and Zeto 1996). Furthermore, mycorrhizae Laccaria sp. had found to increase by 5.0–19, 5.0, and 3.0 boron concentration in the root, stem, and leaves of silver birch (Betula pendula) plant (Lehto et al. 2004; Ruuhola and Lehto 2014). Lavola et al. (2011) showed that in inoculation with Paxillus involutus, the concentration of boron increased from 0.01 to 280 mg Kg-1, demonstrating the potential of mycorrhizae in boron acquisition. Clark and Zeto (1996) found that maize plants inoculated with Glomus intraradices translocate more boron to shoots under acidic and alkaline environments. It has been demonstrated that bacteria are responsible for some of the excessive boron absorption that occurs from the soil solution. Bacillus, Chimaereicella, Gracilibacillus, Lysinibacillus, Boronitolerans, Variovorax, Pseudomonas, Mycobacterium, and Rhodococcus are among the boron-tolerant bacterial strains that have been shown to absorb hazardous quantities of boron from soil (Samreen et al. 2019; Mehboob et al. 2021). The boron availability enhanced in the soil–plant system by increasing soil acidity, and Bacillus pumilus inoculation may improve plant uptake of boron (Masood et al. 2019). According to Deubel et al. (2000), the cause is plant growthpromoting rhizobacteria-induced release of organic acids into the soil, which may lower soil pH and improve the availability of boron to plants. There is mounting evidence that rhizobacteria inoculation that promotes plant growth lowers soil pH by producing organic acids as secondary metabolites (Turan et al. 2006).

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Role of Biotechnology to Develop Efficient Strain of Microorganisms for Micronutrient Solubilization

In order to obtain a holistic picture of microbial community dynamics in the rhizosphere, OMIC approaches are the path ahead. Techniques like proteomics, genomics, transcriptomics, metabolomics, and other OMICs along with bioinformatics can help in unraveling many aspects of nutrient mobilization and solubilization. These high-throughput methodologies can be used in microbial systems to quantify protein abundance (proteomics), gene copy number (genomics), mRNA transcript levels (transcriptomics), and small cellular metabolites (metabolomics) to establish the communities associated with micronutrient solubilization patterns and their change during the crop growth. The OMIC technologies help improve nutrient solubilization efficiency by isolating non-culturable microorganisms and discovering the new characteristics of microbes arising from the interaction of genes, proteins, metabolites, and the environment (Jerez 2008). Other high-throughput approaches like microarray-based profiling of bacterial communities and nextgeneration sequencing can help us comprehend distinct microbial communities and their synergistic interactions with the plant and rhizosphere (Trivedi et al. 2012). Moreover, the past few decades have witnessed the development of a number of genetic tools, which are employed by researchers to improve crop productivity and reduce the damage inflicted by pests or pathogens. Genetic manipulations on desired microbes are a fast and reasonably effective tool as it incorporates the direct introduction of individual or heterologous traits into well-defined microorganisms (Qiu et al. 2019). CRISPR/Cas9 is another technology that has allowed gene and genome editing in an accurate and reliable way. Cas9 is an RNA-guided DNA endonuclease that helps in the targeted complexing with sequence-specific singleguided RNA (sgRNA) to facilitate movement into the cell (Cong et al. 2013). This has made possible the insertion or removal of any desired or unwanted sequence, respectively, from the cell. With these gene-editing technologies, genetically modified organisms can be utilized in the agricultural system to promote rapid solubilizing of micronutrients for availability to the plants. Also, the genetic engineering of bacteria is much easier as compared to that of the plant, which is a eukaryote (Kumawat et al. 2017). Furthermore, the application of these biotechnological tools to create mutant strains that have increased organic acid production is also an indirect method to improve solubilization efficiency (Meena et al. 2016). However, the incorporation of transgenic microbes into farming systems is a controversial issue owing to the limited survival of these microbes in soil and also genetic transfer between non-related strains, which is considered an environmental hazard associated with newly introduced GMOs (Wang et al. 2011). Apart from these biotechnological interventions, the selection of indigenous microbes as inoculants and optimizing microbial delivery methods can successfully improve the survival and efficacy of microbial inoculants (Qiu et al. 2019). Approaches targeting the core microbiome can provide the most effective outcome in the long term.

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Conclusion

Microbes play the important role in solubilizing/mobilizing or recycling of micronutrients. Their populations in soils are often too low to mobilize nutrients. Application of nutrient-solubilizing rhizobacteria (NSR) can replace chemical fertilizers. Microbial inoculants, or biofertilizers, are artificially multiplied cultures of soil bacteria that boost soil fertility and crop productivity. Biofertilizers improved crop productivity, soil health, and product nutrition. Microbe-mediated biofortification may become an economically viable agricultural method for meeting the nutritional demands of malnourished people worldwide. Plant growth-promoting abilities of microorganisms can be increased through genome modification in molecular biotechnology. As a result, multifunctional plant growth-promoting microorganisms reduce pollution by reducing the consumption and leakage of chemical fertilizers. The identification of plant growth-promoting rhizobacteria strains and their traits is the main research issue in this sector. Thus, microbiological, soil scientist, and biotechnologist collaboration is needed to examine, refine, and develop possible inoculants for numerous critical nutrients under varied environmental situations.

References Adak A, Prasanna R, Babu S, Bidyarani N, Verma S, Pal M, Shivay YS, Nain L (2016) Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices. J Plant Nutr 39(9):1216–1232 Adriano DC (2001) Trace elements in terrestrial environments. Springer-Verlag, New York, NY Alejandro S, Höller S, Meier B, Peiter E (2020) Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci 11:300 Alloway BJ (2004) In zinc in soil and crop nutrition. International Zinc Association, Brussels Alloway BJ (2008a) Micronutrient deficiencies in global crop production. Springer Alloway BJ (2008b) Zinc in soils and crop nutrition, 2nd edn. IZA and IFA, Brussels Andreazza R, Okeke BC, Lambais MR, Bortolon L, de Melo GWB, de Oliveira Camargo FA (2010) Bacterial stimulation of copper phytoaccumulation by bioaugmentation with rhizosphere bacteria. Chemosphere 81(9):1149–1154 Andresen E, Peiter E, Küpper H (2018) Trace metal metabolism in plants. J Exp Bot 69:909–954 Babar S, Jilan G, Mihoub A, Jamal A, Ahmad I, Chaudhary AN, Saeed MF, Alam T (2022) Bacterial redox cycling of manganese in calcareous soil enhances the nutrients bioavailability to wheat. J Soil Sci Plant Nutr:1–9 Bartlett RJ, James BR (1993) Redox chemistry of soils. Adv Agron 50:151–208 Behera SK, Shukla AK (2014) Total and extractable manganese and iron in some cultivated acid soils of India: status, distribution, and relationship with some soil properties. Pedosphere 24(2): 196–208 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 Bloom AJ, Kameritsch P (2017) Relative association of Rubisco with manganese and magnesium as a regulatory mechanism in plants. Physiol Plant 161(4):545–559 Bolaños L, Lukaszewski K, Bonilla I, Blevins D (2004) Why boron? Plant Physiol Biochem 42: 907–912

136

D. Singh et al.

Bowler C, Van Camp W, Van Montagu M, Inzé D, Asada K (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218 Brandl H, Faramarzi MA (2006) Microbe–metal-interactions for the biotechnological treatment of metal-containing solid waste. Chin Particuol 4:93–97 Bratina BJ, Stevenson BS, Green WJ, Schmidt TM (1998) Manganese reduction by microbes from oxic regions of the Lake Vanda (Antarctica) water column. Appl Environ Microbiol 64(10): 3791–3797 Brdar-Jokanovic M (2020) Boron toxicity and deficiency in agricultural plants. Int J Mol Sci 21: 1424. https://doi.org/10.3390/ijms21041424 Brear EM, Day DA, Smith PM (2013) Iron: an essential micronutrient for the legume-rhizobium symbiosis. Front Plant Sci 4:359 Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173(4): 677–702 Cao FQ, Werner AK, Dahncke K, Romeis T, Liu LH, Witte CP (2010) Identification and characterization of proteins involved in rice urea and arginine catabolism. Plant Physiol 154: 98–108. https://doi.org/10.1104/pp.110.160929 Chen B, Shen J, Zhang X, Pan F, Yang X, Feng Y (2014a) The endophytic bacterium, Sphingomonas SaMR12, improves the potential for zinc phytoremediation by its host, Sedum alfredii. PLoS One 9(9):e106826 Chen B, Zhang Y, Rafiq MT, Khan KY, Pan F, Yang X, Feng Y (2014b) Improvement of cadmium uptake and accumulation in sedum alfredii by endophytic bacteria Sphingomonas SaMR12: effects on plant growth and root exudates. Chemosphere 117:367–373 Cheng C, Rerkasem B (1993) Effects of boron on pollen viability in wheat. Plant Soil 155:13–315 Clark RB, Zeto SK (1996) Mineral acquisition by mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1495–1503 Clark RB, Zobel RW, Zeto SK (1999) Effects of mycorrhizal fungus isolate on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176 Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121): 819–823 Constantopoulos G (2008) Lipid metabolism of manganese-deficient algae: I. effect of manganese deficiency on the greening and the lipid composition of Euglena gracilis Z. Plant Physiol 45(1): 76–80. https://doi.org/10.1104/pp.45.1.76 Cornu JY, Elhabiri M, Ferret C, Geoffroy VA, Jézéquel K, Leva Y, Lollier M, Schalk IJ, Lebeau T (2014) Contrasting effects of pyoverdine on the phytoextraction of Cu and Cd in a calcareous soil. Chemosphere 103:212–219 Cunninghan JE, Kuiack C (1992) Production of citric acid and oxalic acid and solubilization of calcium phosphate by Penicillium billai. Appl Environ Microbiol 58:1451–1458 da Silva LL, Olivares FL, De Oliveira RR, Vega MRG, Aguiar NO, Canellas LP (2014) Root exudate profiling of maize seedlings inoculated with Herbaspirillum seropedicae and humic acids. Chem Biol Tech Agric 1(1):1 Delaporte-Quintana P, Lovaisa NC, Rapisarda VA, Pedraza RO (2020) The plant growth promoting bacteria Gluconacetobacter diazotrophicus and Azospirillum brasilense contribute to the iron nutrition of strawberry plants through siderophores production. Plant Growth Regul 91(2): 185–199 Dell’Amico E, Mazzocchi M, Cavalca L, Allievi L, Andreoni V (2008) Assessment of bacterial community structure in a long-term copper-polluted ex-vineyard soil. Microbiol Res 163(6): 671–683 Deubel A, Gransee A, Merbach W (2000) Transformation of organic rhizodeposits by rhizoplane bacteria and its influence on the availability of tertiary calcium phosphate. J Plant Nutr Soil Sci 163:387–392 Dixon RK, Garrett HE, Cox GS (1989) Boron fertilization, vesicular-arbuscular mycorrhizal colonization and growth of Citrus jambhiri lush. J Plant Nut 12:687–700

5

Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability

137

Dordas C, Chrispeels MJ, Brown PH (2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124:1349–1361 Dubinina GA (1978) Functional significance of bivalent iron and manganese oxidation in Leptothrix pseudoochraceae. Mikrobiologiia 47(5):783–789 Esitken A (2011) Use of plant growth promoting rhizobacteria in horticultural crops. In: Bacteria in agrobiology: crop ecosystems. Springer, Berlin, Heidelberg, pp 189–235 Eskandari S, Gineau E (2020) The effects of foliar-applied manganese on major cell wall polysaccharide fractions and soluble sugar composition of cucumber leaves. Acta Physiol Plant 42(9): 1–9 FAO WHO (2002) Human vitamin and mineral requirements. Food and Agriculture Organization of the United Nations, Bangkok. ISBN 1014–9228 Ferret C, Cornu JY, Elhabiri M, Sterckeman T, Braud A, Jézéquel K, Lollier M, Lebeau T, Schalk IJ, Geoffroy VA (2015) Effect of pyoverdine supply on cadmium and nickel complexation and phytoavailability in hydroponics. Environ Sci Pollut R 22:2106–2116 Fleischer A, O’Neill MA, Ehwald R (1999) The pore size of nongraminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol 121:829–838 Francis AJ, Dodge CJ (1988) Anaerobic microbial dissolution of transition and heavy metal oxides. Appl Environ Microbiol 54(4):1009–1014 Gao Z, Su J, Ali A, Wang X, Bai Y, Wang Y, Wang Z (2022) Denitrification strategy of Pantoea sp. MFG10 coupled with microbial dissimilatory manganese reduction: deciphering the physiological response based on extracellular secretion. Bioresour Technol 355:1272–1278 Ghiorse WC (1984) Biology of iron-and manganese-depositing bacteria. Annu Rev Microbiol 38(1):515–550 Ghosh S, Gandhi M, van Hullebusch ED, Das AP (2021) Proteomic insights into Lysinibacillus sp.mediated biosolubilization of manganese. Environ Sci Pollut Res 28(30):40249–40263 Ghumare V, Rana M, Gavkare M, Khachi B (2014) Bio-fertilizers- increasing soil fertility and crop productivity. Jr Industrial Pollu Cont 30:196–201 Glenn JK, Akileswaran L, Gold MH (1986) Mn (II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium. Arch Biochem Biophys 251(2):688–696 Glick B (2012) Plant growth-promoting bacteria: mechanisms and applications. Hindawi, New York Goldbach HE (2020) Advances in understanding boron cycling in soils, uptake/use by plants and ways of optimizing boron use efficiency in crop production. In: Rengel Z (ed) Achieving sustainable crop nutrition. Burleigh Dodds Science Publishing, Cambridge, pp 355–406 Goldbach HE, Wimmer MA (2007) Boron in plants and animals: is there a role beyond cell-wall structure? J Plant Nutr Soil Sci 170:39–48 Goldschmidt VM (1954) Geochemistry. Oxford University Press (Clarendon), London Gong Z, Xiong L, Shi H, Yang S, Herrera-Estrella LR, Xu G, Chao DY, Li J, Wang PY, Qin F, Li J, Ding Y, Shi Y, Wang Y, Yang Y, Guo Y, Zhu JK (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63(5):635–674. https://doi.org/10.1007/s11427-0201683-x Gopi K, Jinal HN, Prittesh P, Kartik VP, Amaresan N (2020) Effect of copper-resistant Stenotrophomonas maltophilia on maize (Zea mays) growth, physiological properties, and copper accumulation: potential for phytoremediation into biofortification. Int J Phytoremediation 22(6):662–668 Gosal S, Karlupia A, Gosal S, Chhibba I, Varma A (2010) Biotization with Piriformospora indica and Pseudomonas fluorescens improves survival rate, nutrient acquisition, field performance and saponin content of micropropagated Chlorophytum sp. Indian J Biotechnol 9:289–297 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 2013: 1–7

138

D. Singh et al.

Gounot AM (1994) Microbial oxidation and reduction of manganese: consequences in groundwater and applications. FEMS Microbiol Rev 14(4):339–349 Gregory AL, Hurley BA, Tran HT, Valentine AJ, She YM, Knowles VL et al (2009) In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphatestarved Arabidopsis thaliana. Biochem J 420:57–65. https://doi.org/10.1042/BJ20082397 Grybos M, Billard P, Desobry-Banon S, Michot LJ, Lenain JF, Mustin C (2011) Bio-dissolution of colloidal-size clay minerals entrapped in microporous silica gels. J Colloid Interface Sc 362: 317–324 Gurmani AR, Khan SU, Andaleep RK, Waseem KA (2012) Soil application of zinc improves growth and yield of tomato. Int J Agric Biol 14:91–96 Hashimoto K, Eckert C, Anschütz U, Scholz M, Held K, Waadt R et al (2012) Phosphorylation of calcineurin B-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins. J Biol Chem 287:7956–7968. https://doi.org/10.1074/jbc.M111.279331 He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T et al (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 He J, Yang B, Hause G, Rössner N, Peiter-Volk T, Schattat MH, Voiniciuc C, Peiter E (2022) The trans-Golgi-localized protein BICAT3 regulates manganese allocation and matrix polysaccharide biosynthesis. Plant Physiol 190(4):2579–2600 Hebbern CA, Laursen KH, Ladegaard AH, Schmidt SB, Pedas P, Bruhn D et al (2009) Latent manganese deficiency increases transpiration in barley (Hordeum vulgare). Physiol Plant 135: 307–316. https://doi.org/10.1111/j.1399-3054.2008.01188.x Helmke PA, Koons RD, Schomberg PJ, Iskandar IK (1977) Determination of trace element contamination of sediments by multielement analysis of the clay-size fraction. Environ Sci Technol 11:984–989 Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27(5):637–657 Housh AB, Powell G, Scott S, Anstaett A, Gerheart A, Benoit M, Ferrieri RA (2021) Functional mutants of Azospirillum brasilense elicit beneficial physiological and metabolic responses in Zea mays contributing to increased host iron assimilation. ISME J 15(5):1505–1522 Hsieh MH, Chang CY, Hsu SJ, Chen JJ (2008) Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis. Plant Mol Biol 66:663–673. https://doi.org/10.1007/s11103-0089297-5 Huerta-Rosas B, Cano-Rodríguez I, Gamiño-Arroyo Z, Gómez-Castro FI, Carrillo-Pedroza FR, Romo-Rodríguez P, Gutiérrez-Corona JF (2020) Aerobic processes for bioleaching manganese and silver using microorganisms indigenous to mine tailings. World J Microbiol Biotechnol 36(8):1–16 İpek M, Eşitken A (2017) The actions of PGPR on micronutrient availability in soil and plant under calcareous soil conditions: an evaluation over Fe nutrition. In: Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 81–100 Jerez CA (2008) The use of genomics, proteomics and other OMICS technologies for the global understanding of biomining microorganisms. Hydrometallurgy 94(1–4):162–169 Jha Y (2019) The importance of zinc-mobilizing rhizosphere bacteria to the enhancement of physiology and growth parameters for paddy under salt-stress conditions. Jordan J Biol Sci 12(2):167–173 Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13 Kabata-Pendias A (2000) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton Kanwar JS, Randhawa NS (1974) Micronutrient research in soils and plants in India. Tech Bull Agric No 50 ICAR, New Delhi, p 185

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Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability

139

Karnwal A (2021) Zinc solubilizing pseudomonas spp. from vermicompost bestowed with multifaceted plant growth promoting properties and having prospective modulation of zinc biofortification in Abelmoschus esculentus L. J Plant Nutr 44:1023–1038 Katyal JC, Sharma BD (1991) DTPA extratable and total Zn, Cu, Mn and Fe in Indian soils. Geoderma 49:165–179 Ke T, Zhang J, Tao Y, Zhang C, Zhang Y, Xu Y, Chen L (2021) Individual and combined application of cu-tolerant bacillus spp. enhance the Cu phytoextraction efficiency of perennial ryegrass. Chemosphere 263:127952 Keshavarz S, Faraji F, Rashchi F, Mokmeli M (2021) Bioleaching of manganese from a low-grade pyrolusite ore using Aspergillus niger: process optimization and kinetic studies. J Environ Manag 285:112153 Kim S, Lim H, Lee I (2010) Enhanced heavy metal phytoextraction by Echinochloa crus-galli using root exudates. J Biosci Bioeng 109(1):47–50 Kloepper JW, Okon Y (1994) Plant growth-promoting rhizobacteria (other systems). In: Okon Y (ed) Azospirillum/plant associations. CRC Press, Boca Raton, FL, pp 111–118 Kobae Y, Tomioka R, Tanoi K, Kobayashi NI, Ohmori Y, Nishida S, Fujiwara T (2014) Selective induction of putative iron transporters, OPT8a and OPT8b, in maize by mycorrhizal colonization. Soil Sci Plant Nutr 60(6):843–847 Kobayashi T, Nozoye T, Nishizawa NK (2018) Iron transport and it is regulation in plants. Free Radic Biol Med 10:439 Kollner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482–494 Kothari SK, Marschner H, Römheld V (1990) Direct and indirect effects of VA mycorrhizal fungi and rhizosphere microorganisms on acquisition of mineral nutrients by maize (Zea mays L.) in a calcareous soil. New Phytol 116:637–645 Krithika S, Balachandar D (2016) Expression of zinc transporter genes in rice as influenced by zincsolubilizing Enterobacter cloacae strain ZSB14. Front Plant Sci 7:446 Kroh GE, Pilon M (2020) Regulation of iron homeostasis and use in chloroplasts. Int J Mol Sci 21(9):3395 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.). Biocat and Agric Biotechnol 3(4):121–128 Kumar A, Jha MN, Singh D, Pathak D, Rajawat MVS (2021) Prospecting catabolic diversity of microbial strains for developing microbial consortia and their synergistic effect on Lentil (Lens esculenta) growth, yield and iron biofortification. Arch Microbiol 203(8):4913–4928. https:// doi.org/10.1007/s00203-021-02446-9 Kumari P, Meena M, Gupta P, Dubey MK, Nath G, Upadhyay RS (2018) Plant growth promoting rhizobacteria and their biopriming for growth promotion in mung bean (Vigna radiata (L.) R. Wilczek). Biocatal Agric Biotechnol 16:163–171 Kumawat N, Kumar R, Kumar S, Meena VS (2017) Nutrient solubilizing microbes (NSMs): its role in sustainable crop production. In: Agriculturally important microbes for sustainable agriculture. Springer, Singapore, pp 25–61 Kushwaha P, Srivastava R, Pandiyan K, Singh A, Chakdar H, Kashyap PL et al (2021) Enhancement in plant growth and zinc biofortification of chickpea (Cicer arietinum L.) by Bacillus altitudinis. J Soil Sci Plant Nutr 21:922–935. https://doi.org/10.1007/s42729-021-00411-5 Lack AJ, Evans DE (2005) Instant notes in plant biology, vol 7, 1st edn. Bios Scientific Publishers, Oxford, pp 68–71 Lavola A, Aphalo PJ, Lehto T (2011) Boron and other elements in sporophores of ectomycorrhizal and saprotrophic fungi. Mycorrhiza 21:155–165 Lehto T, Lavola A, Kallio E, Aphalo PJ (2004) Boron uptake by ectomycorrhizas of silver birch. Mycorrhiza 14:209–212

140

D. Singh et al.

Li Z, McLaren RG, Metherell AK (2004) The availability of native and applied soil cobalt to ryegrass in relation to soil cobalt and manganese status and other soil properties. N Z J Agric Res 47(1):33–43 Lindsay WL (1979) Chemical equilibria in soils. Wiley, New York, NY Lu S, Miller HM (1989) The role of VA mycorrhizae in the absorption of P and Zn by maize in field and growth chamber experiments. Can J Soil Sci 69:97–109 Luo Q, Sun L, Hu X, Zhou R (2014) The variation of root exudates from the hyperaccumulator sedum alfredii under cadmium stress: metabonomics analysis. PLoS One 9(12):e115581 Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Inoculation of Brassica oxyrrhina with plant growth promoting bacteria for the improvement of heavy metal phytoremediation under drought conditions. J Hazard Mater 320:36–44 Marastoni L, Pii Y, Maver M, Valentinuzzi F, Cesco S, Mimmo T (2019) Role of Azospirillum brasilense in triggering different Fe chelate reductase enzymes in cucumber plants subjected to both nutrient deficiency and toxicity. Plant Physiol Biochem 136:118–126. https://doi.org/10. 1016/j.plaphy.2019.01.013 Martens DC, Westermann DT (1991) Fertilizer applications for correcting micronutrient deficiency. In: Mortvedt JJ, Fox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture. Soil Science Society of America, Madison, WI Masood S, Zhao XQ, Shen RF (2019) Bacillus pumilus increases boron uptake and inhibits rapeseed growth under boron supply irrespective of phosphorus fertilization. Aob plants 11(4):plz036. https://doi.org/10.1093/aobpla/plz036 Meena VS, Bahadur I, Maurya BR, Kumar A, Meena RK, Meena SK, Verma JP (2016) Potassiumsolubilizing microorganism in evergreen agriculture: an overview. In: Potassium solubilizing microorganisms for sustainable agriculture, pp 1–20 Mehboob N, Hussain M, Minhas WA, Yasir TA, Naveed M, Farooq S, Alfarraj S, Zuan ATK (2021) Soil-applied boron combined with boron-tolerant bacteria (Bacillus sp. MN54) improve root proliferation and nodulation, yield and agronomic grain biofortification of chickpea (Cicer arietinum L.). Sustainability 13:9811 Mishra PK, Bisht SC, Ruwari P, Joshi GK, Singh G, Bisht JK, Bhatt JC (2011) Bioassociative effect of cold tolerant Pseudomonas spp. and Rhizobium leguminosarum-PR1 on iron acquisition, nutrient uptake and growth of lentil (Lens culinaris L.). Eur J Soil Biol 47(1):35–43 Mohammadi K, Sohrabi Y (2012) Bacterial biofertilizers for sustainable crop production: a review. ARPN J Agril Bio Sci 7:307–316 Mohanty S, Ghosh S, Nayak S, Das AP (2017) Isolation, identification and screening of manganese solubilizing fungi from low-grade manganese ore deposits. Geomicrobiol J 34(4):309–316 Morcillo RJ, Singh SK, He D, An G, Vílchez JI, Tang K, Yuan F, Sun Y, Shao C, Zhang S, Yang Y, Liu X, Dang Y, Wang W, Gao J, Huang W, Lei M, Song CP, Zhu JK, Macho AP, Paré PW, Zhang H (2020) Rhizobacterium-derived diacetyl modulates plant immunity in a phosphatedependent manner. EMBO J 39(2):e102602. https://doi.org/10.15252/embj.2019102602 Moreno-Lora A, Recena R, Delgado A (2019) Bacillus subtilis QST713 and cellulose amendment enhance phosphorus uptake while improving zinc biofortification in wheat. Appl Soil Ecol 142: 81–89 Mumtaz MZ, Malik A, Nazli F, Latif M, Zaheer A, Ali Q et al (2020) Potential of zinc solubilizing bacillus strains to improve growth, yield, and quality of maize (Zea mays). Intl J Agric Biol 24: 691–698 Mushtaq Z, Asghar HN, Zahir ZA, Maqsood M (2022) The interactive approach of rhizobacteria and l-tryptophan on growth, physiology, tuber characteristics, and iron concentration of potato (Solanum tuberosum L.). J Plant Growth Regul 41(3):1359–1366 Myers CR, Myers JM (1992) Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1. J Bacteriol 174(11):3429–3438 Nagata T (2017) Effect of Pseudomonas fluorescens inoculation on the improvement of iron deficiency in tomato. Plant Root 11:1–9

5

Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability

141

O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139 Obrador A, Novillo J, Alvarez JM (2003) Mobility and availability to plants of two zinc sources applied to a calcareous soil. Soil Sci Soc Am J 67:564–572 Orhan E, Esitken A, Ercisli S, Turan M, Sahin F (2006) Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Sci Hortic 111(1):38–43 Palanichamy S, Maruthamuthu S, Manickam ST, Rajendran A (2002) Microfouling of manganeseoxidizing bacteria in Tuticorin harbour waters. Curr Sci 82(7):865–869. http://www.jstor.org/ stable/24106732 Parihar M, Chitara M, Khati P, Kumari A, Mishra PK, Rakshit A, Rana K, Meena VS, Singh AK, Choudhary M, Bisht JK, Ram H, Pattanayak A, Tiwari G, Jatav SS (2020a) Arbuscular mycorrhizal fungi: abundance, interaction with plants and potential biological applications. In: Yadav AN et al (eds) Advances in plant microbiome and sustainable agriculture, microorganisms for sustainability, vol 19, pp 105–143. https://doi.org/10.1007/978-98115-3208-5_5 Parihar M, Rakshit A, Meena VS, Gupta VK, Rana K, Choudhary M, Tiwari G, Mishra PK, Pattanayak A, Bisht JK, Jatav SS, Khati P, Jatav HS (2020b) The potential of arbuscular mycorrhizal fungi in C cycling: a review. Arch Microbiol 202:1581–1596 Patel KS, Chikhlekar S, Ramteke S, Sahu BL, Dahariya NS, Sharma R (2015) Micronutrient status in soil of Central India. Am J Plant Sci 6:3025–3037 Patel P, Trivedi G, Saraf M (2018) Iron biofortification in mungbean using siderophore producing plant growth promoting bacteria. Environ Sustain 1:357–365 Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5(2):119–124 Pratiwi H, Aini N, Soelistyono R (2016) Effects of Pseudomonas fluorescens and sulfur on nutrients uptake, growth and yield of groundnut in an alkaline soil. J Degraded Min Lands Manag 3(2): 507 Qiu Z, Egidi E, Liu H, Kaur S, Singh BK (2019) New frontiers in agriculture productivity: optimised microbial inoculants and in situ microbiome engineering. Biotechnol Adv 37(6): 107371 Radzki W, Manero FG, Algar E, García JL, García-Villaraco A, Solano BR (2013) Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Antonie Van Leeuwenhoek 104(3):321–330 Rafique E, Mumtaz MZ, Ullah I, Rehman A, Qureshi KA, Kamran M, Rehman MU, Jaremko M, Alenezi MA (2022) Potential of mineral-solubilizing bacteria for physiology and growth promotion of Chenopodium quinoa Willd. Front Plant Sci 13:1004833. https://doi.org/10. 3389/fpls.2022.1004833 Rahman MA, Parvin M, Das U, Ela EJ, Lee SH, Lee KW, Kabir AH (2020) Arbuscular mycorrhizal symbiosis mitigates iron (Fe)-deficiency retardation in alfalfa (Medicago sativa L.) through the enhancement of Fe accumulation and sulfur-assisted antioxidant defense. Int J Mol Sci 21(6): 2219 Rai A, Jha MN, Singh D, Thapa S, Chaurasia SK, Jha G (2021) Detection of endophytic association between Aeschynomene nodulating Bradyrhizobium sp. and traditional Desariya rice roots under rice-Aeschynomene ecosystem of chaur land. Biologia Futura, Bihar, pp 1–11 Rajawat MVS, Singh R, Singh D, Saxena AK (2019a) Psychrotrophs of the genus Janthinobacterium with potential to weather potassium aluminosilicate mineral. 3 Biotech 9: 142. https://doi.org/10.1007/s13205-019-1672-1 Rajawat MVS, Ansari WA, Singh D, Singh R (2019b) Potassium solubilizing bacteria (KSB). In: Microbial interventions in agriculture and environment. Springer, Singapore, pp 189–209 Rajawat MVS, Singh R, Singh D, Yadav AN, Singh S, Kumar M, Saxena AK (2020) Spatial distribution and identification of bacteria in stressed environments capable to weather potassium aluminosilicate mineral. Braz J Microbiol 51(2):751–764

142

D. Singh et al.

Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Plant growth-promoting traits in Enterobacter cloacae subsp. dissolvens MDSR9 isolated from soybean rhizosphere and its impact on growth and nutrition of soybean and wheat upon inoculation. Agric Res 3(1):53–66 Rana A, Kabi SR, Verma S, Adak A, Pal M, Shivay YS, Prasanna R, Nain L (2015) Prospecting plant growth promoting bacteria and cyanobacteria as options for enrichment of macro-and micronutrients in grains in rice–wheat cropping sequence. Cogent Food Agric 1(1):1037379 Ren XM, Guo SJ, Tian W, Chen Y, Han H, Chen E, Li BL, Li YY, Chen ZJ (2019) Effects of plant growth-promoting bacteria (PGPB) 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 Requena L, Bornemann S (1999) Barley (Hordeum vulgare) oxalate oxidase is a manganesecontaining enzyme. Biochem J 343:185–190. https://doi.org/10.1042/bj3430185 Rohdich F, Lauw S, Kaiser J, Feicht R, Köhler P, Bacher A, Eisenreich W (2006) Isoprenoid biosynthesis in plants–2C-methyl-d-erythritol-4-phosphate synthase (IspC protein) of Arabidopsis thaliana. FEBS J 273(19):4446–4458 Roriz M, Pereira SI, Castro PM, Carvalho SM, Vasconcelos MW (2021) Iron metabolism in soybean grown in calcareous soil is influenced by plant growth-promoting rhizobacteria–a functional analysis. Rhizosphere 17:100274 Rosas SB, Avanzini G, Carlier E, Pasluosta C, Pastor N, Rovera M (2009) Root colonization and growth promotion of wheat and maize by Pseudomonas aurantiaca SR1. Soil Biol Biochem 41: 1802–1806 Rudnick RL, Gao S, Holland HD, Turekian KK (2003) Composition of the continental crust. The crust 3:1–64 Rusin PA, Ehrlich H (1995) Developments in microbial leaching—mechanisms of manganese solubilization. In: Microbial and enzymatic bioproducts. Advances in biochemical engineering/ biotechnology, vol 52. Springer, Berlin, Heidelberg Rusin PA, Quintana L, Sinclair NA, Arnold RG, Oden KL (1991) Physiology and kinetics of manganese-reducing Bacillus polymyxa strain D1 isolated from manganiferous silver ore. Geomicrobiol J 9(1):13–25 Ruuhola T, Lehto T (2014) Do ectomycorrhizas affect boron uptake in Betula pendula? Can J For Res 44:1013–1019 Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132:1033–1040 Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28(4):1503–1509 Saeed M, Fox RL (1977) Relation between suspension pH and zinc solubility in acid and calcareous soils. Soil Sci 124:199–204 Samreen T, Zahir ZA, Naveed M, Asghar M (2019) Boron tolerant phosphorus solubilizing Bacillus spp. MN-54 improved canola growth in alkaline calcareous soils. Intl J Agric Biol 21:538–546 Saravanan VS, Subramoniam SR, Raj SA (2004) Assessing in vitro solubilization potential of different zinc solubilizing bacterial (ZSB) isolates. Braz J Microbiol 35:121–125 Saravanan VS, Kalaiarasan P, Madhaiyan M, Thangaraju M (2007) Solubilization of insoluble zinc compounds by Gluconacetobacter diazotrophicus and the detrimental action of zinc ion (Zn2+) and zinc chelates on root knot nematode Meloidogyne incognita. Lett Appl Microbiol 44:235– 241 Sarkar A, Asaeda T, Wang Q, Rashid MH (2015) Arbuscular mycorrhizal influences on growth, nutrient uptake, and use efficiency of Miscanthus sacchariflorus growing on nutrient-deficient river bank soil. Flora 212:46–54 Sarker MMH, Moslehuddin AZM, Jahiruddin M, Islam MR (2018) Available status and changing trend of micronutrients in floodplain soils of Bangladesh. SAARC J Agric 16(1):35–48

5

Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability

143

Sbartai H, Djebar M, Rouabhi R, Sbartai I, Berrebbah H (2011) Antioxidative response in tomato plants Lycopersicon esculentum L. roots and leaves to zinc. Am Eurasian J Toxicol Sci 3:41–46 Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9:236–243. https://doi.org/10.1016/j.tplants.2004.03.007 Sharma A, Johri B, Sharma A, Glick B (2003) Plant growth-promoting bacterium pseudomonas sp. strain GRP 3 influences iron acquisition in mung bean (Vigna radiata L. Wilczek). Soil Biol Biochem 35(7):887–894 Sharma M, Mishra V, Rau N, Sharma RS (2016) Increased iron-stress resilience of maize through inoculation of siderophore-producing Arthrobacter globiformis from mine. J Basic Microbiol 56(7):719–735 Sheng X, Sun L, Huang Z, He L, Zhang W, Chen Z (2012) Promotion of growth and Cu accumulation of bio-energy crop (Zea mays) by bacteria: implications for energy plant biomass production and phytoremediation. J Environ Manag 103:58–64 Shorocks VM, Alloway BJ (1988) Copper in plant animal and human nutrition. Copper Development Association, Herts, p 84 Shukla AK, Behera SK (2019) All India coordinated research project on micro-and secondary nutrients and pollutant elements in soils and plants: research achievements and future thrusts. Indian J Fert 15(5):522–543 Shukla AK, Sinha NK, Tiwari PK, Prakash C, Behera SK, Lenka NK, Singh VK, Dwivedi BS, Majumdar K, Kumar A, Srivastava PC, Pachauri SP, Meena MC, Lakaria BL, Siddiqui S (2017) Spatial distribution and management zones for sulfur and micronutrients in Shiwalik Himalayan region of India. Land Degrad Dev 28(3):959–969 Shukla AK, Sinha NK, Tiwari PK, Prakash C, Behera SK, Surendra Babu P, Patnaik MC, Somasundaram J, Singh P, Dwivedi BS, Datta SP (2018) Evaluation of spatial distribution and regional zone delineation for micronutrients in a semiarid Deccan Plateau Region of India. Land Degrad Dev 29(8):2449–2459 Shukla AK, Behera SK, Prakash C, Tripathi A, Patra AK, Dwivedi BS, Trivedi V, Rao C, Chaudhari SK, Das S, Singh AK (2021) Deficiency of phyto-available Sulphur, zinc, boron, iron, copper and manganese in soils of India. Sci Rep 11(1):1–13 Silva CAT, Cagol A, Silva TRB, Nobrega LHP (2011) Boron application before sowing of sunflower hybrid. J Food Agric Environ 9:580–583 Singh D, Prasanna R (2020) Potential of microbes in the biofortification of Zn and Fe in dietary food grains. A review. Agron Sustain Dev 40:1–21 Singh D, Rajawat MVS, Kaushik R, Prasanna R, Saxena AK (2017a) Beneficial role of endophytes in biofortification of Zn in wheat genotypes varying in nutrient use efficiency grown in soils sufficient and deficient in Zn. Plant Soil 416(1):107–116. https://doi.org/10.1007/s11104-0173189-x Singh D, Geat N, Rajawat MVS, Mahajan MM, Prasanna R, Singh S, Kaushik R, Singh RN, Kumar K, Saxena AK (2017b) Deciphering the mechanisms of endophyte-mediated biofortification of Fe and Zn in wheat. J Plant Growth Regul 37(1):174–182 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(12):815–833 Singh BN, Rajawat MVS, Hidangmayum A, Ansari WA, Singh D, Zeyad MT, Kumar SC, Roy M, Kumar M (2019) Importance and utilization of plant-beneficial rhizobacteria in agriculture. In: Microbial interventions in agriculture and environment. Springer, Singapore, pp 171–187 Singh D, Geat N, Rajawat MVS, Prasanna R, Saxena AK (2020a) 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(2):1–13 Singh D, Prasanna R, Sharma V, Rajawat MVS, Nishanth S, Saxena AK (2020b) Prospecting plantmicrobe interactions for enhancing nutrient availability and grain biofortification. In: Gupta OP, Pandey V, Narwal S, Sharma P, Ram S, Singh GP (eds) Wheat and barley grain biofortification. Woodhead Publishing, Elsevier, pp 203–228

144

D. Singh et al.

Singh D, Thapa S, Geat N, Mehriya ML, Rajawat MVS (2021) Biofertilizers: mechanisms and application. In: Rakshit A, Meena VS, Parihar M, Singh HB, Singh AK (eds) Biofertilizers volume 1: advances in bio-inoculants, Woodhead publishing series in food science, technology and nutrition. Elsevier, pp 151–162 Singh D, Thapa S, Mahawar H, Kumar D, Geat N, Singh SK (2022) Prospecting potential of endophytes for modulation of biosynthesis of therapeutic bioactive secondary metabolites and plant growth promotion of medicinal and aromatic plants. Antonie Van Leeuwenhoek 115(6): 699–730 Sirohi G, Upadhyay A, Srivastava PS, Srivastava S (2015) PGPR mediated zinc biofertilization of soil and its impact on growth and productivity of wheat. J Soil Sci Plant Nutr 15(1):202–216 Szurmak B, Wysłouch-Cieszyńska A, Wszelaka-Rylik M, Bal W, Dobrzańska M (2008) A diadenosine 5′,5″-P1P4 tetraphosphate (Ap4A) hydrolase from Arabidopsis thaliana that is activated preferentially by Mn2 + ions. Acta Biochim Polon 55:151–160. https://doi.org/10. 18388/abp.20083173 Tariq M, Hameed S, Malik KA, Hafeez FY (2007) Plant root associated bacteria for zinc mobilization in rice. Pak J Bot 39(1):245 Tena W, Beyene S (2011) Identification of growth limiting nutrient(s) in alfisols: soil physicochemical properties, nutrient concentrations and biomass yield of maize. Am J Plant Nutr Fertil Technol 1:23–35 Terry N (1980) Limiting factors in photosynthesis: I. use of iron stress to control photochemical capacity in vivo. Plant Physiol 65(1):114–120 Tisdale SL, Nelson WL, Beaten JD (1984) Zinc in soil fertility and fertilizers, 4th edn. Macmillan, New York, pp 382–391 Tisdale SL, Nelson WL, Beaton JD, Havlin JL (2009) Soil fertility and fertilizer-an introduction to nutrient management, 7th edn. Prentice Hall of India, New Delhi Trivedi P, Pandey A, Palni LMS (2012) Bacterial inoculants for field applications under mountain ecosystem: present initiatives and future prospects. In: Maheshwari DK (ed) Bacteria in agrobiology: plant probiotics. Springer, Berlin/Heidelberg, pp 15–44 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 Uzoh IM, Babalola OO (2020) Review on increasing iron availability in soil and its content in cowpea (Vigna unguiculata) by plant growth promoting rhizobacteria. Afr J Food Agric Nutr Dev 20(3):15779–15799 Vaid SK, Kumar B, Sharma A, Shukla AK, Srivastava PC (2014) Effect of Zn solubilizing bacteria on growth promotion and Zn nutrition of rice. J Soil Sci Plant Nutr 14(4):889–910 Venkidasamy B, Selvaraj D, Ramalingam S (2019) Genome-wide analysis of purple acid phosphatase (PAP) family proteins in Jatropha curcas L. Int J Biol Macromol 123:648–656. https://doi. org/10.1016/j.ijbiomac.2018.11.027 Vigani G, Zocchi G, Bashir K, Philippar K, Briat JF (2013) Signals from chloroplasts and mitochondria for iron homeostasis regulation. Trends Plant Sci 18:305–311 Voxeur A, Fry SC (2014) Glycosylinositol phosphorylceramides (GIPCs) from Rosa cell cultures are boron-bridged in the plasma membrane and form complexes with rhamnogalacturonan-II. Plant J 79:139–149 Wang S, O’Brien TR, Pava-Ripoll M, St. Leger RJ (2011) Local adaptation of an introduced transgenic insect fungal pathogen due to new beneficial mutations. Proc Natl Acad Sci 108(51): 20449–20454 Wang Y, Yang X, Zhang X, Dong L, Zhang J, Wei Y, Feng Y, Lu L (2014) Improved plant growth and Zn accumulation in grains of rice (Oryza sativa L.) by inoculation of endophytic microbes isolated from a Zn hyperaccumulator, Sedum alfredii H. J Agric Food Chem 62:1783–1791 Wang Q, Ye J, Wu Y, Luo S, Chen B, Ma L et al (2019) Promotion of the root development and Zn uptake of Sedum alfredii was achieved by an endophytic bacterium Sasm05. Ecotoxicol Environ Saf 172:97–104. https://doi.org/10.1016/j.ecoenv.2019.01.009

5

Micronutrient Mobilizer Microorganisms: Significance in Crop Sustainability

145

Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot 37:629–672 Watts-Williams SJ, Cavagnaro TR (2018) Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar. Plant Sci 274:163–170 Whiting SN, De Souza M, Terry N (2001) Rhizosphere bacteria mobilize Zn for hyper accumulator by Thlaspi caerulescens. Environ Sci Technol 35:3144–3150 Wu T, Zhang HT, Wang Y, Jia WS, Xu XF, Zhang XZ, Han ZH (2012) Induction of root Fe (lll) reductase activity and proton extrusion by iron deficiency is mediated by auxin-based systemic signalling in Malus xiaojinensis. J Exp Bot 63(2):859–870 Yadav R, Ror P, Rathore P, Ramakrishna W (2020) Bacteria from native soil in combination with arbuscular mycorrhizal fungi augment wheat yield and biofortification. Plant Physiol Biochem 150:222–233 Yadav R, Ror P, Rathore P, Kumar S, Ramakrishna W (2021) Bacillus subtilis CP4, isolated from native soil in combination with arbuscular mycorrhizal fungi promotes biofortification, yield and metabolite production in wheat under field conditions. J Appl Microbiol 131(1):339–359 Yang CH, Wang C, Singh S, Fan N, Liu S, Zhao L, Cao H, Xie W, Yang C, Huang CF (2021) Golgi-localised manganese transporter PML3 regulates Arabidopsis growth through modulating Golgi glycosylation and cell wall biosynthesis. New Phytol 231(6):2200–2214 Zeyad MT, Rajawat MVS, Kumar M, Malik A, Anas M, Ansari WA, Singh BN, Singh D, Saxena AK (2021) Role of microorganisms in plant adaptation towards climate change for sustainable agriculture. In: Lone SA, Malik A (eds) Microbiomes and the global climate change. Springer, Singapore. https://doi.org/10.1007/978-981-33-4508-9_14 Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency inducible mechanisms. Plant J 58(4):568–577 Zhang F, Shen J, Jing J, Li L, Chen X (2010) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity. In: Molecular environmental soil science at the interfaces in the earth’s critical zone. Springer, pp 52–54 Zhou C, Zhu L, Ma Z, Wang J (2018) Improved iron acquisition of Astragalus sinicus under low iron-availability conditions by soil-borne bacteria Burkholderia cepacia. J Plant Interact 13(1): 9–20

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Legume–Rhizobium Symbiosis and Beyond: Producing Synthetic Communities for Increasing Crop Production Under Climate Change Challenges Francesca Vaccaro and Alessio Mengoni

Abstract

Rhizobia are a polyphyletic group of soil bacteria, belonging to alpha- and betaproteobacteria classes, able to colonize the rhizosphere and endosphere of plants and form symbiotic associations with legumes. The rhizobia–legume plant symbiotic interaction is a pivotal part of the input of fixed nitrogen in the agroecosystems. However, rhizobia are only a component of the plant microbiome, which is helping the plant cope with environmental stresses. The application of rhizobia as bioinoculants can then be improved by the creation of synthetic microbial communities, which include rhizobia and other plant growthpromoting bacteria and fungi. The creation of these synthetic communities is challenging since the single members should synergistically cooperate in their effects on the host plant. Systems biology can help to address the rational design of synthetic communities by providing predictions and testable models of interactions among the members of the community and the plant. Here, we will review the most recent advances in the creation of synthetic communities to increase symbiotic nitrogen fixation under climate change scenarios, such as drought and excess soil salinity. Keywords

Rhizobium · Nitrogen fixation · Drought · Synthetic communities · Metabolic modeling · Microbiome

F. Vaccaro (✉) · A. Mengoni Department of Biology, University of Florence, Florence, Italy e-mail: francesca.vaccaro@unifi.it # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_6

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6.1

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The Importance of Rhizobium–Legume Symbiosis in Climate Change

Conventional agriculture has relied on the Haber–Bosch synthesis process to produce the nitrogen fertilizers needed to grow crops. The conversion of hydrogen and nitrogen to ammonia is typically conducted at pressures above 10 MPa (100 bar) and between 400 and 500 °C (Gamble 2019). A century after its invention, the process is still applied to produce more than 100 million tons of artificial nitrogen fertilizers per year, but it is responsible for 1–2% of global energy consumption and ~1% of global energy-related CO2 emissions (~420 Mt./year) (Tang and Qiao 2019), these latter well known to have an impact on climate change. In contrast, biological nitrogen fixation (BNF) is a natural process carried out by a specialized group of prokaryotes that convert atmospheric nitrogen (N2) to ammonia (NH3), using the nitrogenase enzyme. Prokaryotes able to perform BNF include (1) aquatic organisms, such as cyanobacteria; (2) free-living soil bacteria, such as Azotobacter; and (3) bacteria that form associative relationships with plants, such as Azospirillum, and most importantly rhizobia. Rhizobia are diffused within alpha and beta classes of Proteobacteria. They colonize the rhizosphere and endosphere of different plant species, with leguminous plants, and they induce the formation and colonize symbiotic structures, called nodules, where nitrogen fixation takes place. Rhizobium–legume symbioses are a key element in the biogeochemical nitrogen cycle since they provide more than half of the world’s biologically fixed nitrogen. Concerning agricultural systems, rhizobial nitrogen fixation introduces 40–48 million tons of nitrogen each year (Herridge et al. 2008), thus representing a pivotal part of the input of fixed nitrogen in the agroecosystems. In the last few years, climate change has gained importance due to its severe environmental consequences, such as extreme temperatures, abundant rainfalls, drought, high salinity, and soil erosion, which are affecting the productivity of agricultural ecosystems (Kavadia et al. 2020). Heavy reliance on chemical fertilizers for yield increase in traditional management systems led to environmental problems, including massive use of energy from fossil fuels and excess of nitrogen leakage to water bodies leading to eutrophication and poor drinking water quality. New strategies must be found in order to reduce the impact of the agricultural production system and mitigate the negative effects of climate change (Kavadia et al. 2020). A promising strategy to face the main effects of climate change is represented by the rational use of the wide genetic and functional diversity of the microorganisms (not just nitrogen fixation) that colonize plant’s external surfaces (e.g., rhizosphere/ rhizoplane and phyllosphere) and internal tissues (endophytes) and constantly interact with their hosts (Qiu et al. 2019). Plant growth-promoting microorganisms (PGPM) are of particular interest because of their ability to increase plant productivity through various activities, including biological nitrogen fixation, but also other relevant properties for plant growth as soil phosphorus and potassium solubilization, siderophores production, and stimulation of plant defense mechanisms (Kavadia et al. 2020), mitigating both abiotic and biotic stresses.

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Fig. 6.1 Abiotic and biotic stresses faced by plants

Typical abiotic stresses faced by plants include water stress, salinity, heavy metals, soil nitrate, temperature, pH, and biocides (Zahran 1999) (Fig. 6.1). In dry and semiarid regions, drought is obviously one of the crucial abiotic stresses affecting the growth and yield of many crops (Jabborova et al. 2021). Recent studies showed that rhizobium inoculation can ameliorate the effects of salt stress on host plants. Indeed, salt-responsive changes in gene expression in the host legume Medicago sativa (alfalfa) can be reduced by rhizobium inoculation (Chakraborty et al. 2021). A study on proteomic changes in alfalfa plants grown under salinity stress suggested that the symbiotic relationship between S. meliloti and alfalfa can give the host plant a better capacity to adjust key processes in presence of salinity stress, leading to more efficient use of energy and resources, oxidative stress tolerance, ion homeostasis, and health (Y. Wang et al. 2022). Moving forward to just the use of rhizobia, considering the whole panoply of microbes, which positively affect plant growth and tolerance, recent efforts are put into the development of consortia of microbes. The exploitation of the genetic and functional diversity of beneficial microorganisms allows for the rationally formulate of consortia including plant growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi (AMF), and plant growth-promoting bacteria (PGPB) to enhance plants stress tolerance (Vaccaro et al. 2022). A recent study revealed that inoculation with rhizobium/PGPB consortia and AMF/PGPB consortia was more efficient in stimulating shoot biomass growth of Lathyrus cicera (Gritli et al. 2022) than the single bacterial or fungal strain. In another study, soybean plants inoculated with Rhizobium sp. SL42, Hydrogenophaga sp. SL48, and Bradyrhizobium japonicum

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532C showed a triggering of multiple signaling pathways regulating growth and stress tolerance mechanisms, coupled with better growth and salinity tolerance (Ilangumaran et al. 2022). Co-inoculation of B. japonicum USDA 110 and P. putida strain NUU 8 significantly improved the seed germination, root length, shoot length, root dry weight, shoot dry weight, and nodule number under drought stress (Jabborova et al. 2021). Not only plants are subjected to abiotic stresses, but in the era of climate change, the incidence of pests and pathogens on plants has amplified, thus requesting an effort to new management strategies (Tyagi et al. 2022). In plants, typical biotic stresses are bacteria, viruses, fungi, nematodes, insects, spiders, and weeds. They take nutrients away from their host, reduce vigor, and cause host death in severe cases, leading to pre-and post-harvest yield losses all over the globe (Kumar and Nautiyal 2022). The synergistic effects of co-inoculations, briefly pointed out in the previously reported studies, can be also appreciated in plant protection against soilborne pathogens. Co-inoculation of Bradyrhizobium sp. BXYD3 and Glomus mosseae, an arbuscular mycorrhizal fungus, could decrease soybean red crown rot caused by a soilborne fungal pathogen Cylindrocladium parasiticum, through the inhibition of pathogen growth and reproduction, and increase the expression of some plant pathogen defense-related (PR) gene. Interestingly, the synergistic effect was stronger at a low phosphorus level, suggesting that bioinoculants formulated with multiple plant growth-promoting bacteria and fungi, together with nutrient management, should be considered as an efficient method to control plant diseases in sustainable soybean production (X. Gao et al. 2012). In another study, the combined effects of the rhizobium Sinorhizobium medicae and the arbuscular mycorrhizal (AM) fungus Funneliformis mosseae on alfalfa growth, nutrient uptake, and disease severity showed a mutually promoting effect, with increased formation of root nodules, AM fungus colonization, and tolerance to Phytophthora medicaginis infection (Gao et al. 2018).

6.2

The Challenge of Creating Synthetic Communities

When it comes to microbial communities associated with a plant host, one of the crucial aspects worth remembering is that they are not random assemblages. Microbial communities are structured entities and show a defined phylogenetic organization that is dependent on soil type, host genotype, environmental conditions, and plant developmental stage (de Souza et al. 2020). The host genome plays an important role in influencing microbiome composition, thanks for instance to the presence of a high chemical variety of root exudates that provide the basis for crosstalking and recognition, as well as immune response. Microbial inoculants have long been applied in agriculture to promote plant growth. Usually, bioinoculants are composed of a single strain, isolated by in vitro techniques, characterized by plant growth-promoting (PGP) activities (de Souza et al. 2020). However, usually, although showing good performances in vitro, they

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display unsatisfying results in the field, suggesting that functionality and persistence of microorganisms in the soil rely on many factors, which are not taken not account under in vitro studies, from interactions with the environment to the coexistence with other microorganisms of the plant microbiome, to the interaction with the host plant (Trivedi et al. 2020). More recently, synthetic microbial communities (SynComs) are receiving increasing interest. SynComs are assemblages of microorganisms designed to mimic the functions and structure of the microbiome in natural conditions (de Souza et al. 2020). They also allow us to discover plant–microbe interactions and predict host–plant phenotypes (Vaccaro et al. 2022). However, SynCom construction is not trivial, since many aspects of plant–microbe interaction should be considered, and consequently, they are for the moment mostly developed and studied in model plant species.

6.2.1

Not Only Rhizobia and New Host–Microbiome Model Systems

One of the greatest challenges to putting into practice the knowledge on microbial inoculants and on rhizobium inoculation is needed to define methods and principles to translate the acquired results on model plant species to real crops. In other words, in order to design and construct a functional microbial system (a SynCom), firstly, great efforts should be made toward the development of host–microbiome model systems for crop plants, through sharing resources such as genome annotation projects, curated microbial collections, standardized protocols, and growth platforms (Busby et al. 2017). Non-agricultural model plant species have been deeply investigated. However, some of them, such as Arabidopsis thaliana, show some limitations, such as short life span (limiting the studies on microbiota seasonal dynamics), lack of interactions with part of the soil microbiota capable of closely interacting with the plant (e.g., Brassicaceae do not form a symbiosis with arbuscular mycorrhizal fungi (Cosme et al. 2018)), and genomic and phenotypic differences from important crops (Busby et al. 2017). Thus, new model systems are needed to translate laboratory-scale evidence of SynComs to field application (Sessitsch et al. 2019). Ideally, in order to allow a smoother translation of knowledge and methods, both laboratory methods and computational ones, from such model species to relevant crops, agricultural germplasms for which close relatives exist as model species, should be prioritized (Vaccaro et al. 2022). Crops, such as alfalfa, chickpea, lentil, landraces of rice, maize, and wheat, represent an excellent opportunity to take advantage of since they hold their own specific features, but at the same time, they can have relatives as model species (such as Medicago truncatula for alfalfa) (Vaccaro et al. 2022). Some years ago, a study on barley (Hordeum vulgare) comparing modern model crops, wild relatives and landraces rhizospheric microbiomes shed light on the combined effect of microbe–microbe and host–microbe interactions in driving root–soil microbiota assemblage (Bulgarelli et al. 2015). These kinds of studies are offering the possibility to investigate the structure and the evolution of the

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microbiota and provide insights into the design of synthetic communities (Vaccaro et al. 2022). Another microbiome study on a Mexican indigenous maize landrace showed that in this case biological nitrogen fixation is supported by a microbiota associated with the mucilage secreted by aerial roots (Van Deynze et al. 2018). Diazotrophic microbial associations with cereals are stirring great interest due to cereal’s economic relevance. Shifting from microbiomes to single-strain interaction models, studies on local varieties of alfalfa (M. sativa) crop revealed the existence of genotypic interactions that influence the symbiosis with the nitrogen-fixing rhizobium S. meliloti (Fagorzi et al. 2021). In particular, nearly two-thirds of differentially expressed genes in the rhizobium were influenced by the strain genotype and strain-by-host plant genotype interactions. Moreover, the genotype of the variety of host plants contributed by one-sixth of total differentially expressed genes. These data indicate that alfalfa can largely benefit from breeding programs considering the selectivity of symbiotic rhizobia recruitment (Vaccaro et al. 2022). However, due to the severe consequences of climate change on food and nutritional security, studies should be extended to climate-resilient nonmodel crops, such as Amaranthus spp., Chenopodium quinoa (quinoa), Eragrostis tef (teff), and Setaria italica (foxtail millet), which are important local sources of food, typical of marginal environments and characterized by high biological value protein content (Gregory et al. 2019) and which could benefit from nitrogen-fixing bioinoculants to increase yield and nutritional value (Vaccaro et al. 2022).

6.2.2

Core Plant Microbiome in Host–Microbiome Systems and Rules of SynCom Assembly

One of the challenges of formulating bioinoculants is to identify and incorporate strains belonging to the “core microbiome,” a set of microbial taxa with a robust capacity of plant colonization and shared between model and nonmodel species (Busby et al. 2017; Vaccaro et al. 2022) in order to increase SynCom stability. Studies on core microbiomes through meta-omics approaches represent a valid tool for identifying the most recurrent taxa associated with a certain host phenotype, as well as for the understanding of host genotype-driven differences that guide microbiome assembly of different. On the other hand, the analysis of distinct plant groups can reveal the functional traits that influence microbiome assembly, while the comparison of plants grown under different environmental conditions can reveal the strains and genes that contribute to tolerance (Busby et al. 2017). In order to predict plant phenotype in presence of the SynCom, multi-omics approaches, metagenome wide association analysis, network analysis, genome mining reconstruction of transcriptional and regulatory networks, and statistical modeling approaches should be used to integrate different data (for further information see par.3). Investigating the functional potential of a microbial community by multiple approaches (e.g., by Phenotype Microarray™) could help to understand the mechanisms driving plant– microbiome interactions and could allow to model the fundamental microbial

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community functions for plant growth. Indeed, there are several pieces of evidence that hosts select for functions rather than taxonomy in their microbiome (Doolittle and Booth 2017). Many functions provided by the plant microbiome belong to the accessory genome, so they are not necessarily related to a specific taxon. The ideal SynCom, once in the soil, should be active and persist as the indigenous microbiome faces local environmental conditions. Approaches such as statistical inference, neural networks (NN), machine learning, and reinforcement learning should be used to maximize predictive performance (de Souza et al. 2020; Herrera Paredes et al. 2018). Recently, software called DISCo-microbe has been designed in order to construct a diverse community of organisms that can be distinguished through low-cost, high-throughput amplicon sequencing for use in in vivo experiments (Carper et al. 2020). The development of SynComs cannot rely only on in silico analysis. Isolation of microorganisms and culturing remain important steps. Generally, wet laboratory techniques for the construction of SynCom systems are based on the physical separation of the strains that form the community. A possible limiting factor can be found in the culturability of strains of the microbiota. Strategies of culturomics should be implemented to increase the culturable fraction of the microbiota (Riva 2019; Vaccaro et al. 2022). Recently, microfluidic platforms have been shown to be a promising method to bring to culturability microorganisms into complex communities (Kehe et al. 2019). Another study proposed the cultivation of a broad diversity of taxa by microfluidics and microfabricated arrays where bacterial strains grew physically separated but could exchange small molecules (Chodkowski and Shade 2017). Beyond the knowledge of the core microbiome, the understanding of the driving forces that rule microbe–microbe interaction is fundamental. For rhizobia, which are included in the core plant microbiome, three main aspects of their interaction with the host and other microbes should be considered, to develop or select elite (viz. highly performing) inoculants: trade, diplomacy, and warfare (Checcucci et al. 2017). Trade is referred to as the host–rhizobium interaction, where the rhizobia exchange fixed nitrogen for space to grow and carbon sources with the leguminous plant, their symbiotic partner. Ideally, SynComs should include rhizobia strains more efficiently in rewarding the plant through fixed nitrogen. The second component of the sociobiological behavior, diplomacy, refers to the capacity, of both host and symbiont, to discriminate the partner through the production of specific Nod factors and flavonoids (the two signaling molecules exchanged prior to symbiosis, from the bacterial and the plant side, respectively). Other genes related to diplomacy are the ones involved in quorum sensing, biofilm, and phytohormones production. Elite inoculants should be able to have all these improved functions, in order to better modulate the interaction. Finally, warfare refers to antagonistic interaction between the strains in competition, as already explained in the previous chapter. SynCom strains should be able not to be overwhelmed by indigenous microbes. The cultivarspecific response to microbiota would provide a better understanding of strain behavior in the synthetic community, thus resulting pivotal to the bioinoculant formulation (Vaccaro et al. 2022) (Fig. 6.2).

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Fig. 6.2 An ideal SynCom should incorporate core microbiome strains with a robust capacity of plant colonization and persistence in soil in presence of an indigenous microbiome. Improved features, such as host-SynCom recognition, quorum sensing, biofilm formation phytohormone production, and better efficiency in rewarding the host plant with fixed nitrogen, should be prioritized in the pursuit of the best microbial candidates. All these aspects should be predicted with in silico modeling, thus the importance of having host–microbiome model systems

In addition to this, community ecology theories are essential to disentangle the rules behind plant microbiome assembly. For further details, see par.3.

6.2.3

Delivery Systems

Finally, one of the main challenges in transferring the SynCom, including rhizobia and other PGPB from the laboratory to the field is to find delivery systems, such as by seed coating, inoculation, or by spraying on flowers, so that the SynComs can be established into the progeny seeds (Table 6.1). High-resolution tools (e.g., in situ sensors and omics analyses) could be used to reveal the presence of chemical markers (e.g., root exudates or volatiles) associated with microorganisms that indicate the presence of desired taxa and specific reactions, while optical techniques, such as RGB (red, green and blue), infrared and hyperspectral imagery, are already used to monitor in crop breeding and detect plant diseases (de Souza et al. 2020). Hyperspectral sensors on drones could be a desirable tool to evaluate changes in the plant phenotype after successful plant colonization of SynComs. Although there are still limitations in omics data integration and analysis, the combined use of the abovementioned methods will allow a rational design of SynComs

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Table 6.1 delivery methods for bioinoculant application. (Modified from Lobo et al. 2019) Delivery method Arabic gum

Microorganism Bradyrhizobium spJ-81

Seed coating by polyvinyl alcohol (PVA)

Pantoea agglomerans ISIB55 and Burkholderia caribensis ISIB40 Bacillus sp. A30 and Burkholderia sp. L2 S. mexicanum ITTG R7T, R. calliandra LBP2-1 and R. etli CFN42T Bacillus sp. CaB5

Biochar Peat

Seed coating by talc, carboxymethyl cellulose, and calcium carbonate Seed coating by polyvinyl alcohol (PVA), polyvinylpyrrolidone (PVP), glycerol

Bacillus subtilis NH-100, and Serratia marcescens FA-4

Shelf life 6 months at room temperature (108 CFU/ml) N/A

8 months at 27 °C (107 CFU/ml) 8 months at room temperature (109CFU/ml) 45 days, unspecified storage temperature (around 108 CFU/ml) 15 days at room temperature (5.675 ± 0.48 log 10 CFU/seed)

for agricultural purposes and could create novel opportunities for sustainable production.

6.3

Translating Symbiotic Rhizobial Microbiomes from Model Plant to Nonmodel Crops: The Importance of Systems Biology and Predictive Models

Mutualistic interactions can be considered as biological systems, where two or more metabolic networks interact, giving rise to emergent properties of the holobiont and unexpected phenotypic traits (diCenzo et al. 2020). The holobiont concept, which has gained more and more attention during the last decades, assumes that the host and its microbiota form a unit of selection in evolution, co-evolving in order to maintain the overall functionality and fitness of the system (Zilber-Rosenberg and Rosenberg 2008). As a consequence, for a full comprehension of the mechanisms that drive symbiosis between plants and microbes, a systemic perspective is required. Recently, systems biology is emerging as an effective top-down approach for rationally assembling microbial consortia, allowing us to predict the behavior of microbial populations and how their application can affect nonmodel crop health and yield (Vaccaro et al. 2022). When translating acquired laboratory-scale knowledge to field applications, it is necessary to take into consideration the impact and synergy of factors, such as the management, the climatic conditions, and the soil properties, over the bioinoculant (Vaccaro et al. 2022). The simulation of a SynCom behavior can be done by various methods, including dynamic models, stoichiometric models, and agent-based models (McCarty and Ledesma-Amaro 2019). These modeling approaches allow

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us to predict the response of the community to environmental changes, determine the flux of metabolites inside the biochemical reactions and the output in terms of growth, and simulate the changes over time. Such systems biology-based mathematical modeling and simulations offer the opportunity to reduce the gap between laboratory studies efficacy in the field (Vaccaro et al. 2022). This systemic approach not only predicts nitrogen fixation abilities and PGP capability of a microbial assemblage (de Souza et al. 2020) but also gives the opportunity to integrate them with plant metabolism, overcoming the limitation of just considering a single partner of the symbiotic process. An example of the potentiality of such an approach has been demonstrated by the integrated metabolic reconstruction of the holobiont Medicago truncatula–Sinorhizobium meliloti (diCenzo et al. 2020). The model, called “virtual nodule environment” (ViNE), includes plant tissues (shoot, root, nodule) and the nodule developmental zones, which demarcate spatially and transcriptionally different stages of symbiosis between S. meliloti and M. truncatula. By this model, the rate of fixed nitrogen with respect to the investment in symbiotic nodules is predicted, which can allow estimating of the maximum nitrogen-fixing capacity by the system and the design of a genetic improvement program toward an increase in nitrogen fixation in field conditions. In addition to systems biology, the integration of community ecology theories is essential to plant microbiome research. As a matter of fact, once inoculated in the soil, the ideal synthetic microbial community should grow and persist under both abiotic and biotic stresses, such as the presence of an indigenous microbiome and local environmental conditions (representing deterministic factors) and it will also be affected by stochastic processes (Dini-Andreote et al. 2015). The synthetic community will be therefore influenced by four high-level processes, namely (1) selection, (2) dispersal, (3) drift, and (4) speciation (Dini-Andreote and Raaijmakers 2018). This approach allows to understand to what extent deterministic and stochastic factors can influence a system over time and space (Dini-Andreote et al. 2015).

6.4

Application of Synthetic Communities in Improving Symbiotic Nitrogen Fixation

While many rhizobial inoculants for grain legumes and forage crops (from soybean to alfalfa, Table 6.2) are available on the market (Maitra et al. 2022), to date, few are the synthetic communities applied to leguminous crops (Shayanthan et al. 2022; Wang et al. 2021). Research projects are testing out consortia of rhizobia and PGPR for improving legume growth and resilience toward climate change-related stress, such as drought and soil salinity. Apart from legume crops, research projects and activities toward developing nitrogen-fixing solutions for cereals are receiving increasing attention. The ENSA project for instance (https://www.ensa.ac.uk/) is looking for various solutions, including the exploitation of legume rhizosphere, the managing of the rhizosphere of cereals, and cereal modification that could allow the recognition of rhizobia as symbionts. However, the path toward symbiotic nitrogen

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Table 6.2 Rhizobial bioinoculants already used in agriculture (modified from Adeleke et al. 2019). In some cases, the species present is not reported and a simple mention of the group is reported (e.g., rhizobium) Bioinoculant BIOFIX

Microorganisms Rhizobia

Chickpea nodulator

Mesorhizobium ciceri

Cowpea peat inoculant

Rhizobia

Graph-Ex

Bradyrhizobium japonicum

Green gram peat and Groundnut peat Histick

Rhizobia

Legume fix (common bean)

Rhizobium spp.

Legume fix (soybean)

Bradyrhizobium japonicum

Likuiq Semia

Bradyrhizobium elkanii

N-bean

Rhizobium phaseolus

Nitrasec Alfalfa (Lucerne)

Sinorhizobium meliloti

Nitrasec

Rhizobium tropici

Nodumax

Bradyrhizobia

N-Soy

Bradyrhizobium japonicum

Organo

Bacillus spp. Enterobacter spp., Pseudomonas, Stenotrophomonas, Rhizobium Bradyrhizobium sp.

Rizo-Liq (green gram, common bean, soybean, groundnut, chickpea Rizo-Liq top

Bradyrhizobium japonicum

Bradyrhizobium japonicum

Soyflo

Bradyrhizobium japonicum

Twin N

Azorhizobium sp., Azoarcus sp., Azospirillum sp. Bradyrhizobium spp. Bradyrhizobium japonicum

Vault HP Vault NP

Company MEA Fertilizer Ltd, Kenya Becker Underwood, USA Becker Underwood, USA America’s Best Inoculant, USA Becker Underwood, USA BASF SA (Pty), South Africa Legume Technology (UK) Legume Technology (UK) Microbial solution (Pty) Ltd, South Africa Biocontrol Products SA (Ltd) Ltd Microbial solution (Pty) Ltd, South Africa Lage y Cia, S.A, Uruguay IITA Business Incubation Platform, Nigeria Biocontrol Products SA (Ltd) Ltd Amka Products (Pty) Ltd, South Africa Rizobacter, Argentina Rizobacter, Argentina Soygro (Ltd) Ltd, South Africa Mapleton Ltd, UK BASF, Canada Becker Underwood, USA

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fixation in cereals is still long (Nag et al. 2020; Roell and Zurbriggen 2020; Silva Pankievicz et al. 2021), while the strategies for engineering and exploiting the rhizosphere microbiome are closer to the application. Microbiome transplantation has been shown to have a dramatic impact on plant resistance (Schmitz et al. 2022), and root nodule symbiosis “per se” modifies the surrounding root microbiome (Gao et al. 2022; Liu et al. 2021; Zgadzaj et al. 2016). This modification can play favorable roles in improving nitrogen fixation and consequently plant nutrition. Assays of co-inoculation in soybean are the most abundant, and in some cases, results have reached the market of bioinoculants. The rationale of many of these very small-scale synthetic communities (indeed only two strains, a rhizobium, and a PGPB) was to combine a good nitrogen-fixing rhizobium with a plant hormone producer (see for instance (Bai et al. 2003; Kumawat et al. 2019; Tu et al. 2021). A systematic review of published papers on soybean co-inoculation, containing goodquality quantitative data and statistical analysis, in a range of more than 30 years (from 1987 to 2018) (Zeffa et al. 2020), allows drawing some preliminary indication for the application of a true synthetic community. The authors of this review identified that a large part of the studies was done in Brazil, followed by Argentina, North America, India, Egypt, Iran, and Germany. Strains used as nonsymbiotic partners were from genus Azospirillum (37% of total) and then Pseudomonas, Serratia, Bacillus, and other various genera from Proteobacteria, Firmicutes, and Cyanobacteria. However, even if such trials resulted in an increase in biomass, no significant increase was observed for grain yield and shoot nitrogen content. These results are suggesting that co-inoculant formulation done without prior careful evaluation of trophic exchanges in the rhizosphere and endosphere of the plant is not useful for improving nitrogen fixation. This lack of predictability is also highlighted by the response to the co-inoculation. This response varied according to the genus of the PGPR, as well as with the experimental conditions (pot experiments giving better results than field conditions). All that in hands, this means that predictive modeling and rational design of synthetic communities (which are by far more complex than co-inoculation with two strains only), as described in the previous paragraphs of this chapter, are critical and obliged steps to accelerate the progress in bioinoculants development for increasing nitrogen fixation in harsh conditions.

6.5

Conclusion and Future Perspectives

Where are we now? Previous paragraphs reported the state of the art of rhizobial exploitation and bioinoculant formulation strategies, as well as perspectives on the methods for the rational design of synthetic communities. It seems that the way is settled, but we must figure out that many missing points are still there. In particular, we still miss clearly interpretable models of biotic interactions. Large advancements have been done (see, for instance, the virtual nodule environment mentioned before (diCenzo et al. 2020), but they are strongly dependent on good-quality experimental data, especially quantitative data on biotic interactions, and on edaphic and climatic

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conditions. In other words, the future challenge we see is to obtain more data on real legume microbiota under harsh conditions, using also synthetic communities as probes to explore the response to challenges of natural microbiomes (Vorholt et al. 2017). Recent data on Arabidopsis show that interpreting such data is not trivial (Durán et al. 2022), because climate and plant genotypes are both drivers of the response of the microbiome and then of the success of a synthetic community. Moreover, we need to translate knowledge from a few model species (such as Arabidopsis) to several crops. In doing that, we probably also need novel experimental setups, which can better simulate field conditions and a more diffused use of predictive and decision-making statistical modeling, which can guide experiments reducing unnecessary and uninformative trials. Competing Interests All the authors declare that they have no competing interests. Index All the words we would like to see indexed are highlighted in the chapter.

References Adeleke RA, Raimi AR, Roopnarain A, Mokubedi SM (2019) Status and prospects of bacterial inoculants for sustainable management of agroecosystems. In: Biofertilizers for sustainable agriculture and environment, pp 137–172. https://doi.org/10.1007/978-3-030-18933-4_7 Bai Y, Zhou X, Smith DL (2003) Crop ecology, management and quality: enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43(5):1774–1781. https://doi.org/10.2135/cropsci2003.1774 Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, SchulzeLefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17(3):392–403. https://doi.org/10.1016/j.chom.2015.01.011 Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J, Bennett A, Morsy M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15(3):1–14. https://doi.org/10.1371/journal.pbio.2001793 Carper DL, Lawrence TJ, Carrell AA, Pelletier DA, Weston DJ (2020) DISCo-microbe: design of an identifiable synthetic community of microbes. PeerJ 8:e8534. https://doi.org/10.7717/peerj. 8534 Chakraborty S, Driscoll HE, Abrahante JE, Zhang F, Fisher RF, Harris JM (2021) Salt stress enhances early symbiotic gene expression in Medicago truncatula and induces a stress-specific set of rhizobium-responsive genes. Mol Plant-Microbe Interact 34(8):904–921. https://doi.org/ 10.1094/MPMI-01-21-0019-R Checcucci A, DiCenzo GC, Bazzicalupo M, Mengoni A (2017) Trade, diplomacy, and warfare: the quest for elite rhizobia inoculant strains. Front Microbiol 8:1–7. https://doi.org/10.3389/fmicb. 2017.02207 Chodkowski JL, Shade A (2017) A synthetic community system for probing microbial interactions driven by exometabolites. MSystems 2(6). https://doi.org/10.1128/msystems.00129-17 Cosme M, Fernández I, Van der Heijden MGA, Pieterse CMJ (2018) Non-mycorrhizal plants: the exceptions that prove the rule. Trends Plant Sci 23(7):577–587. https://doi.org/10.1016/j. tplants.2018.04.004 de Souza RSC, Armanhi JSL, Arruda P (2020) From microbiome to traits: designing synthetic microbial communities for improved crop resiliency. Front Plant Sci 11:1–7. https://doi.org/10. 3389/fpls.2020.01179

160

F. Vaccaro and A. Mengoni

diCenzo GC, Tesi M, Pfau T, Mengoni A, Fondi M (2020) Genome-scale metabolic reconstruction of the symbiosis between a leguminous plant and a nitrogen-fixing bacterium. Nat Commun 11(1). https://doi.org/10.1038/s41467-020-16484-2 Dini-Andreote F, Raaijmakers JM (2018) Embracing community ecology in plant microbiome research. Trends Plant Sci 23(6):467–469. https://doi.org/10.1016/j.tplants.2018.03.013 Dini-Andreote F, Stegen JC, Van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci U S A 112(11):E1326–E1332. https://doi.org/10.1073/pnas.1414261112 Doolittle WF, Booth A (2017) It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol Philos 32(1):5–24. https://doi.org/10.1007/s10539-016-9542-2 Durán P, Ellis TJ, Thiergart T, Ågren J, Hacquard S (2022) Climate drives rhizosphere microbiome variation and divergent selection between geographically distant Arabidopsis populations. New Phytol 236:608. https://doi.org/10.1111/nph.18357 Fagorzi C, Bacci G, Huang R, Cangioli L, Checcucci A, Fini M, Perrin E, Natali C, diCenzo GC, Mengoni A (2021) Nonadditive transcriptomic signatures of genotype-by-genotype interactions during the initiation of plant-rhizobium symbiosis. MSystems 6(1):1–15. https://doi.org/10. 1128/msystems.00974-20 Gamble A (2019) Ullmann’s encyclopedia of industrial chemistry. Charlest Advis 20(4):46–50. https://doi.org/10.5260/chara.20.4.46 Gao X, Lu X, Wu M, Zhang H, Pan R, Tian J, Li S, Liao H (2012) Co-inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS One 7(3):1–10. https://doi.org/10.1371/journal.pone.0033977 Gao P, Li Y, Guo YY, Duan T (2018) Co-inoculation of lucerne (Medicago sativa) with an AM fungus and a rhizobium reduces occurrence of spring black stem and leaf spot caused by Phoma medicaginis. Crop Past Sci 69(9):933–943. https://doi.org/10.1071/CP18135 Gao J, Chen S, Wang Y, Qi J, Li X, Wei G, Jiao S (2022) Variation in soybean root-associated microbiome between lateral roots with and without nodules. Plant Soil 0123456789:481. https:// doi.org/10.1007/s11104-022-05535-w Gregory PJ, Mayes S, Hui CH, Jahanshiri E, Julkifle A, Kuppusamy G, Kuan HW, Lin TX, Massawe F, Suhairi TASTM, Azam-Ali SN (2019) Crops For the Future (CFF): an overview of research efforts in the adoption of underutilised species. Planta 250(3):979–988. https://doi. org/10.1007/s00425-019-03179-2 Gritli T, Boubakri H, Essahibi A, Hsouna J, Ilahi H, Didier R, Mnasri B (2022) Salt stress mitigation in Lathyrus cicera by combining different microbial inocula. Physiol Mol Biol Plants 28(6): 1191–1206. https://doi.org/10.1007/s12298-022-01205-4 Herrera Paredes S, Gao T, Law TF, Finkel OM, Mucyn T, Teixeira PJPL, Salas González I, Feltcher ME, Powers MJ, Shank EA, Jones CD, Jojic V, Dangl JL, Castrillo G (2018) Design of synthetic bacterial communities for predictable plant phenotypes. PLoS Biology 16: e2003962. https://doi.org/10.1371/journal.pbio.2003962 Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311(1–2):1–18. https://doi.org/10.1007/s11104-008-9668-3 Ilangumaran G, Subramanian S, Smith DL (2022) Soybean leaf proteomic profile influenced by Rhizobacteria under optimal and salt stress conditions. Front Plant Sci 13:1–15. https://doi.org/ 10.3389/fpls.2022.809906 Jabborova D, Kannepalli A, Davranov K, Narimanov A, Enakiev Y, Syed A, Elgorban AM, Bahkali AH, Wirth S, Sayyed RZ, Gafur A (2021) Co-inoculation of rhizobacteria promotes growth, yield, and nutrient contents in soybean and improves soil enzymes and nutrients under drought conditions. Sci Rep 11(1):1–9. https://doi.org/10.1038/s41598-021-01337-9 Kavadia A, Omirou M, Fasoula D, Ioannides IM (2020) The importance of microbial inoculants in a climate-changing agriculture in eastern mediterranean region. Atmos 11(10):1–18. https://doi. org/10.3390/atmos11101136

6

Legume–Rhizobium Symbiosis and Beyond: Producing Synthetic. . .

161

Kehe J, Kulesa A, Ortiz A, Ackerman CM, Thakku SG, Sellers D, Kuehn S, Gore J, Friedman J, Blainey PC (2019) Massively parallel screening of synthetic microbial communities. Proc Natl Acad Sci U S A 116(26):12804–12809. https://doi.org/10.1073/pnas.1900102116 Kumar V, Nautiyal CS (2022) Plant abiotic and biotic stress alleviation : from an endophytic microbial perspective. Curr Microbiol 79:311. https://doi.org/10.1007/s00284-022-03012-2 Kumawat KC, Sharma P, Sirari A, Singh I, Gill BS, Singh U, Saharan K (2019) Synergism of Pseudomonas aeruginosa (LSE-2) nodule endophyte with Bradyrhizobium sp. (LSBR-3) for improving plant growth, nutrient acquisition and soil health in soybean. World J Microbiol Biotechnol 35(3):1–17. https://doi.org/10.1007/s11274-019-2622-0 Liu Y, Ma B, Chen W, Schlaeppi K, Erb M, Stirling E, Hu L, Wang E, Zhang Y, Zhao K, Lu Z, Ye S, Xu J (2021) Rhizobium symbiotic capacity shapes root-associated microbiomes in soybean. Front Microbiol 12:709012. https://doi.org/10.3389/fmicb.2021.709012 Lobo CB, Juárez Tomás MS, Viruel E, Ferrero MA, Lucca ME (2019) Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. Microbiol Res 219:12–25. https://doi.org/10.1016/j.micres.2018.10.012 Maitra S, Brestic M, Bhadra P, Shankar T, Praharaj S, Palai JB, Shah MMR, Barek V, Ondrisik P, Skalický M, Hossain A (2022) Bioinoculants—natural biological resources for sustainable plant production. Microorganisms 10(1):1–35. https://doi.org/10.3390/microorganisms10010051 McCarty NS, Ledesma-Amaro R (2019) Synthetic biology tools to engineer microbial communities for biotechnology. Trends Biotechnol 37(2):181–197. https://doi.org/10.1016/j.tibtech.2018. 11.002 Nag P, Shriti S, Das S (2020) Microbiological strategies for enhancing biological nitrogen fixation in nonlegumes. J Appl Microbiol 129(2):186–198. https://doi.org/10.1111/jam.14557 Qiu Z, Egidi E, Liu H, Kaur S, Singh BK (2019) New frontiers in agriculture productivity: optimised microbial inoculants and in situ microbiome engineering. Biotechnol Adv 37(6): 107371. https://doi.org/10.1016/j.biotechadv.2019.03.010 Riva V (2019) MINIREVIEW A meta-analysis approach to defining the culturable core of plant endophytic bacterial communities. 13:1–10 Roell MS, Zurbriggen MD (2020) The impact of synthetic biology for future agriculture and nutrition. Curr Opin Biotechnol 61:102–109. https://doi.org/10.1016/j.copbio.2019.10.004 Schmitz L, Yan Z, Schneijderberg M, de Roij M, Pijnenburg R, Zheng Q, Franken C, Dechesne A, Trindade LM, van Velzen R, Bisseling T, Geurts R, Cheng X (2022) Synthetic bacterial community derived from a desert rhizosphere confers salt stress resilience to tomato in the presence of a soil microbiome. ISME J 16(8):1907–1920. https://doi.org/10.1038/s41396-02201238-3 Sessitsch A, Pfaffenbichler N, Mitter B (2019) Microbiome applications from lab to field: facing complexity. Trends Plant Sci 24(3):194–198. https://doi.org/10.1016/j.tplants.2018.12.004 Shayanthan A, Ordoñez PAC, Oresnik IJ (2022) The role of synthetic microbial communities (SynCom) in sustainable agriculture. Front Agron 4:1–13. https://doi.org/10.3389/fagro.2022. 896307 Silva Pankievicz VC, do Amaral FP, Ané JM, Stacey G (2021) Diazotrophic bacteria and their mechanisms to interact and benefit cereals. Mol Plant-Microbe Interact 34(5):491–498. https:// doi.org/10.1094/MPMI-11-20-0316-FI Tang C, Qiao SZ (2019) How to explore ambient electrocatalytic nitrogen reduction reliably and insightfully. Chem Soc Rev 48(12):3166–3180. https://doi.org/10.1039/c9cs00280d Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18(11):607–621. https://doi.org/10. 1038/s41579-020-0412-1 Tu TC, Lin SH, Shen FT (2021) Enhancing symbiotic nitrogen fixation and soybean growth through co-inoculation with bradyrhizobium and pseudomonas isolates. Sustainability (Switzerland) 13(20). https://doi.org/10.3390/su132011539

162

F. Vaccaro and A. Mengoni

Tyagi S, Shah A, Karthik K, Rathinam M, Rai V, Chaudhary N, Sreevathsa R (2022) Reactive oxygen species in plants: an invincible fulcrum for biotic stress mitigation. Appl Microbiol Biotechnol 106:5945. https://doi.org/10.1007/s00253-022-12138-z Vaccaro F, Cangioli L, Mengoni A, Fagorzi C (2022) Synthetic plant microbiota challenges in nonmodel species. Trends Microbiol 30(10):922–924. https://doi.org/10.1016/j.tim.2022. 06.006 Van Deynze A, Zamora P, Delaux PM, Heitmann C, Jayaraman D, Rajasekar S, Graham D, Maeda J, Gibson D, Schwartz KD, Berry AM, Bhatnagar S, Jospin G, Darling A, Jeannotte R, Lopez J, Weimer BC, Eisen JA, Shapiro HY et al (2018) Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota. PLoS Biol 16(8):1–21. https://doi.org/10.1371/journal.pbio.2006352 Vorholt JA, Vogel C, Carlström CI, Müller DB (2017) Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22(2):142–155. https://doi.org/10.1016/j.chom.2017.07.004 Wang C, Li Y, Li M, Zhang K, Ma W, Zheng L, Xu H, Cui B, Liu R, Yang Y, Zhong Y, Liao H (2021) Functional assembly of root-associated microbial consortia improves nutrient efficiency and yield in soybean. J Integr Plant Biol 63(6):1021–1035. https://doi.org/10.1111/jipb.13073 Wang Y, Yang P, Zhou Y, Hu T, Zhang P, Wu Y (2022) A proteomic approach to understand the impact of nodulation on salinity stress response in alfalfa (Medicago sativa L.). Plant Biol 24(2): 323–332. https://doi.org/10.1111/plb.13369 Zahran HH (1999) Rhizobium-legume Symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989. https://doi.org/10.1128/mmbr.63.4. 968-989.1999 Zeffa DM, Fantin LH, Koltun A, De Oliveira ALM, Nunes MPBA, Canteri MG, Gonçalves LSA (2020) Effects of plant growth-promoting rhizobacteria on co-inoculation with Bradyrhizobium in soybean crop: a meta-analysis of studies from 1987 to 2018. PeerJ 8:e7905. https://doi.org/10. 7717/peerj.7905 Zgadzaj R, Garrido-Oter R, Jensen DB, Koprivova A, Schulze-Lefert P, Radutoiu S (2016) Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. Proc Natl Acad Sci U S A 113(49):E7996–E8005. https:// doi.org/10.1073/pnas.1616564113 Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32(5):723–735. https://doi. org/10.1111/j.1574-6976.2008.00123.x

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Salinity Mitigation Using Microbial Inoculants Vikram Poria, Sandeep Kumar, Radha Prasanna, Somu Yadav, Pawan Kumar Maurya, and Surender Singh

Abstract

Salinity is among the most debilitating abiotic factors that affect the plant growth severely through the generation of reactive oxygen species, hormonal imbalance, and reduced nutrient mobilisation. High salinity affects microbial diversity and functioning, besides modulating physicochemical properties of soil, thereby, depleting soil health. The agricultural area under salinity is increasing very rapidly and is anticipated to increase to nearly 40 million acres by 2050. There are a number of salinity mitigation options (physical, chemical, hydrological, and biological), and among these biological strategies, particularly, deploying microorganisms such as bacteria, fungi, and algae which can aid plants to fortify themselves against salinity stress is the most efficient. In sustainable agriculture, microbial solutions in particular are in high demand because they offer a natural, affordable, and ecologically safe approach for improving plant growth and productivity. This chapter focuses on different mitigation strategies that help plants to overcome salinity stress and improve the quantum and quality of yield. In addition to highlighting the important role that microorganisms play in salt mitigation, this chapter also discusses the drawbacks and difficulties associated with using them as salinity mitigators, and the path forward.

V. Poria · S. Kumar · S. Singh (✉) Department of Microbiology, Central University of Haryana, Mahendragarh, India R. Prasanna Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India S. Yadav · P. K. Maurya Department of Biochemistry, Central University of Haryana, Mahendragarh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_7

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Keywords

Salinity · PGPB · Microbial inoculants · Soil reclamation · Salinity mitigation

7.1

Introduction

Globally, soil salinity is the primary factor for land degradation, resulting in a considerable reduction in crop yields and more than 20% of irrigated land is composed of saline soil (Imadi et al. 2016). According to FAO Soils Portal (FAO Soils Portal 2022), more than 833 million hectares of subsoil (10% sodic, 85% saline, and 5% saline-sodic) and 424 million hectares of topsoil (24% sodic, 62% saline, and 14% saline-sodic) are affected by salinity, and between 20% and 50% of all irrigated land has become saline worldwide. About 25% (2000 million acres) of the land is unusable for economic purposes due to the high salt concentrations (Mohanavelu et al. 2021). Salinity and sodicity have already affected 6.73 million acres of land and 32% to 84% of groundwater in various States in India; by 2050, it is anticipated to affect up to nearly 40 million acres. According to estimates, India loses 17 million tonnes of food grains each year due to salinity, amounting to a USD 3.0 billion yearly economic loss that is anticipated to rise to USD 5.6 billion by the end of the next decade (Kumar et al. 2022b). Globally, losses from soil salinisation amount to about USD 27.3 billion per year, or roughly USD 441 per hectare. If salt levels increase from low to medium or from medium to high, losses from soil salinisation are predicted to reach USD 1604 and USD 2748 per hectare, respectively (Kumar and Sharma 2020; Mohanavelu et al. 2021). Salinity affects plant growth severely by decreasing photosynthetic activity, increasing oxidative damage to plant, reducing seed germination and nutrient availability, and diminishing plant growth. Salinity decreases photosynthetic activity by inhibiting stomatal conductance, decreasing intercellular CO2, diminishing activity of photosynthetic enzymes, decreasing photosynthetic pigments, reducing PS II quantum yield, and decreasing electron transport. Increased reactive oxygen species (ROS) production, membrane disintegration, increased ion toxicity, leaf development inhibition, imbalance of cellular homeostasis, and retarded growth are some other detrimental effects of salinity on crops (Kamran et al. 2020). Various mitigation strategies can be adopted to remediate salinity-affected land (physical, chemical, and biological) and among these microbe-assisted strategies are most important, due to their efficiency, optimal pricing, and environment friendly approach. Also, microbes use several methods to counteract the ill effects of salinity on soil and on crops. These strategies include activation of antioxidant defence enzymes, release of phytohormones, and exopolysaccharide production (Kumar et al. 2022a). In this chapter, the focus is on the different salinity mitigation methods used and role of microorganisms, as ecologically beneficial options serving both to minimise salinity and enhance crop productivity.

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Salinity Mitigation Strategies

Soil salinity is a measure of the amount of salts in the soil and is frequently represented as electric conductivity. The soil under salt stress contains either large levels of exchangeable sodium, soluble salts, or both as a result of inadequate baseforming cation leaching (Kumar and Sharma 2020). Soil sodicity is the build-up of sodium salts in relation to other salt cations, particularly calcium, and is expressed as either sodium adsorption ratio or percentage. Soil sodicity develops when Na+ cations accumulate at the expense of primarily Ca2+ or other exchangeable cations (Bleam 2017). There are several mitigation strategies used to reclaim salinityaffected land (Fig. 7.1). One of the earliest treatises and practical approaches outlined was by Professor R.N. Singh, who advocated several strategies by demonstrating the efficacy of biological approaches, and his research papers in Nature and ICAR publication are monumental contributions to this area (Singh 1950, 1961). These mitigation approaches are broadly classified under the major categories: physical, chemical, hydrological, and biological (Shahid et al. 2018).

Fig. 7.1 Salinity stress, response of plants, and various mitigation strategies

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Physical Mitigation Strategies

Saline soil reclamation can be done using different physical methods like levelling, subsoiling, sanding, tillage practices, and scraping salts (Shahid et al. 2011, 2018). For uniform water distribution, levelling of soil is important which also improves the leaching of salts (Mohanavelu et al. 2021). The dispersion of clay particles in sodicity-affected soil forms a dense clay-sodic layer beneath the top soil and obstructs the soil’s conducting pores, which stops water from moving through the soil. In subsoiling, gypsum (which helps to remove exchangeable Na+ from the soil) and water are added to the soil before ploughing is done to break up the thick claysodic layer for soil reclamation (Shahid et al. 2018). Another physical reclamation method is sanding, which involves adding the right amount of sand to heavytextured soil in order to permanently change its texture and make it more permeable and thus easier to reclaim (Shahid et al. 2011). Based on the soil bed shape and irrigation, the accumulation of salts occurs at certain zones. In scrapping, mechanical or manual methods are used to remove the salt crusts formed as a result of capillary rise followed by evaporation (Shaygan and Baumgartl 2022). Tillage also helps to improve the physical state of the soil and aids in the soil reclamation by bringing the saline layer to the surface, facilitating its easy removal (Lal 2015).

7.2.2

Chemical Mitigation Strategies

Chemical techniques are unable to restore saline soils completely. Chemicals such as gypsum, acids (sulfuric and hydrochloric acids), and elemental sulphur are all employed in chemical reclamation, and the techniques used depend on the extent and severity of salinity (Shahid et al. 2018; Bello et al. 2021).

7.2.3

Hydrological Mitigation Strategies

Irrigation, leaching, flushing, and drainage of leached water are all elements of hydrological strategies. In order to achieve the goals of soil reclamation, hydrological approaches such as effective utilisation of irrigation water, salt leaching beneath the root zone, improved drainage to alleviate a waterlogged situation are used. Through effective leaching and salt dissolution, soluble salt-rich soils can be recovered. For saline soils, this can be achieved through flooding or surface water ponding. In arid and semi-arid regions, when there is insufficient rainfall to adequately drain the salts, flushing is an excellent method for saline soils with salt crusts. With this method, the salts on the soil surface are flushed away, and the saline water that was flushed enters the drainage system, where it concentrates the salts (Shahid et al. 2018; Mukhopadhyay et al. 2021).

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Biological Mitigation Strategies

For the reclamation of salinity-affected land, various biological mitigating strategies are in use. This approach entails the application of organic amendments, salt-tolerant plant cultivars, genetic engineering, plant growth promoters, salt-tolerant microbial inoculants, etc. (Egamberdieva et al. 2019; Hoque et al. 2022; Shahid et al. 2018). Land that is affected by salinity frequently lacks nutrients and organic materials. Dispersed sodium impairs the soil structure while limiting root growth and water flow in this soil. Organic amendments like crop residue, pressmud, humic acid, biochar, green manure, farm yard manure, compost, etc. can be utilised to increase the organic matter and enhance the physical qualities of soil (Saidimoradi et al. 2019; Mukhopadhyay et al. 2021; Poria et al. 2022). The capacity of various organic amendments to restore saline soil is also well established. The organic amendments improve physical (bulk density, porosity, aggregate stability, structural stability, infiltration rate, and saturated hydraulic conductivity), chemical (pH, electrical conductivity, exchangeable sodium percentage, nutrient availability, and cycling), and biological (microbial population, enzymatic activity, microbial biomass carbon, etc.) properties of soil (Mukhopadhyay et al. 2021; Shaygan and Baumgartl 2022). The crop varieties which are resistant to the high salt concentrations can also be used in salinity-affected lands, these crops are sorghum (2502-IPA, 1011-IPA, 76 T1#23, Raj 4, Raj 27, PAYAM, SEPIDEH, Raj 30) (Guimarães et al. 2019; Hailu et al. 2020; Kulhari and Chaudhary 2008; Rajabi Dehnavi et al. 2020), wheat (KRL 210, KRL 213, Pasban-50, Bakhar-02, S-24, LU-26S) (Sheoran et al. 2021; Jakhar et al. 2018; Irshad et al. 2022; Hussain et al. 2021), rice (Pokkali, Kala Rata 1–24, Bhura Rata, VNIIR8207, Fontan, FL530, Jhona 349, Goa Dhan-1-4) (Fernando 1949; Adorada et al. 2004; Safeena et al. 2003; Ahmed et al. 2016), barley (Ratna, RD 2794, NDB 1173, Narendra Barley-1&3, ISABON3) (Katerji et al. 2006; Singh et al. 2014), etc. For the production of food or biomass, genetic engineering techniques can be utilised to create varieties that are tolerant to salt and resistant to marginal environments (drylands and saline lands) (Afzal et al. 2022). The development of cultivars with low water requirements, decreased transpiration, improved photosynthetic efficiency, nitrogen-fixing genes, heat shock resistance, salinity and water stress resistance, etc. can be facilitated by genetic engineering (Wani et al. 2020). Microbial agents with salt tolerant ability are also used to enhance crop production in saline soil. These microbial agents promote plant growth with different mechanisms and help in salinity mitigation through various strategies (Kumar et al. 2020). Nanoparticles are also reported for their role in drought and salinity mitigation. By altering hormone concentrations, ion homeostasis, antioxidant enzyme activity, gene expression, and defence systems, nanoparticles impart salinity tolerance in a variety of plants but these effects may differ depending on the size, shape, and concentrations of nanoparticles used, environment, or plant species (Etesami et al. 2021).

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Role of Microbial Inoculants in Salinity Mitigation

Abiotic stresses can be reduced by microorganisms, which are well known for a variety of beneficial activities. Salinity stress is the most detrimental abiotic stress for sustainable agriculture production. Salinity has many adverse effects on the physical state of soil as Na+ accumulation in soil hampers water conductivity, soil porosity, and aeration. Plant experiences physiological, morphological, and molecular alterations due to salinity stress that results in poor growth and development. Soil salinity adversely disturbs the microbial diversity around the plant root. Likewise, the rate of photosynthesis, stomatal conductance, and enzyme activity are all impacted by excessive salt concentrations. By increasing the creation of ROS, salinity stress harms lipids, cell membranes, proteins, and nucleic acids (DNA & RNA) of plant cells, leading to oxidative stress. ROS can also trigger apoptosis pathways. Salinity also causes hypertonic conditions due to excessive build-up of Na+ and Cl- ions in the plant body (Kumar et al. 2022a). Plants have different biochemical and physiological mechanisms to combat the salinity stress. Changes in anatomy, morphology, water relations, hormonal profile, photosynthesis, the distribution of toxic ions, and biochemical adaptations like the antioxidative metabolism response are a few examples of such systems as shown in Fig. 7.1 (El Sabagh et al. 2020). Numerous halophytes combat salinity stress by altering phytohormones and related enzymes, producing osmoprotectants and solutes, modulating K+/Na+ relationships, selective ion intake and extrusion, synthesising polyamides that participate in ROS modulation, producing antioxidant compounds, regulating salt-oversensitive genes, and generating nitric oxide (Shilev 2020). Various mechanisms, including the release of ACC (1-aminocyclopropane-1-carboxylic acid) deaminase which lowers the stress induced by ethylene, the synthesis of phytohormones, the production of extracellular polysaccharides that binds to excess sodium ions and blocks their transfer to plant leaves thereby reduce the build-up of sodium ions in plant roots, stimulation of plant osmolyte synthesis (such as proline, glycine betaine, and sugars), high K+/Na+ ratio maintenance by regulating the expression of ion transporters to protect against ion toxicity, upregulating plant antioxidant enzymes (glutathione reductase, catalase, ascorbate peroxidase, and superoxide dismutase), absorption of vital nutrients (mineral solubilisation, nitrogen fixation, siderophore production, etc.), and preserving high photosynthetic activity and stomatal conductance, are reported mechanisms used by microorganisms to alleviate salt stress and promote plant growth (Kumar et al. 2020; Evelin et al. 2019; Bhise and Dandge 2019).

7.3.1

Bacteria as Salinity Mitigators

Halotolerant bacteria survive in diverse salt concentrations (up to 30%). Bacteria overcome the salt stress by various physiological processes including maintenance of osmoregulation, activation of Na+/H+ antiporters, and production of extracellular

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proteases (Kumar et al. 2020). The use of salt-tolerant bacteria to promote plant growth in saline and alkaline soil is an ideal option. These plant growth-promoting rhizobacteria (PGPR) can increase crop yield through different plant growthpromoting mechanisms and also alleviate salt stress through various mechanisms due to their capability to colonise plant roots (Yasmin et al. 2020). Several salttolerant PGPR genera are reported for their salinity mitigation ability so far (Table 7.1). The major genera include Bacillus, Pseudomonas, Anabaena, Nostoc, Azotobacter, Agrobacterium, Arthrobacter, Ochromobacter, Azospirillum, Alcaligenes, Enterobacter, Burkholderia, Microbacterium, Klebsiella, Streptomyces, Rhizobium, and Pantoea (Kumar et al. 2022a; Sagar et al. 2022).

7.3.2

Fungi as Salinity Mitigators

Fungi are a diverse group of microbes that play a crucial role in every ecosystem and aid plants in surviving adverse conditions. Arbuscular mycorrhizal fungi (AMF) in particular are helpful in nutrient absorption and growth of plant in high saline environments. Furthermore, strengthening the relationship between plants and advantageous rhizosphere fungi could encourage plant growth and increase plant biomass production (Li et al. 2017). Arbuscular mycorrhizal fungus symbiotically exists with the roots of 80% of land plants. This symbiosis is a unique system that transfers and absorbs mineral nutrients from the soil more effectively than roots alone. AMF can colonise roots, enhance turf quality, increase chlorophyll content, and promote plant development and photosynthesis (Evelin et al. 2019). There are many fungi that are reported for their salinity mitigation and plant growth improvement (Table 7.1).

7.3.3

Algae as Salinity Mitigator

Numerous studies have reported the activities of algae in reducing salinity and promoting plant growth. Seaweeds, particularly brown algae, have been shown to increase plant growth and yield by improving antioxidant qualities; as a result, they may be able to adapt to saline stress. Polysaccharides, sterols, N-containing compounds (like betaines), macro- and micronutrients, as well as growth-promoting molecules like auxins, cytokinins, gibberellins, and brassinosteroids are all found in seaweed extracts. Even at low concentrations, their application can trigger a variety of physiological and growth responses that affect plant growth and production, seedling establishment, nutrient mobilisation, chlorophyll content, root structure, flowering, and fruit setting. Additionally, it has been shown that applying several commercial seaweed extract types to crops and medicinal shrubs can increase their resistance to a variety of abiotic challenges, including heat, nutrition, and drought stress (Rouphael et al. 2017; Latique et al. 2017). Several cyanobacterial isolates belonging to genera such as Aphanothece sp., Chlorogloeopsis sp., and Nodularia sp. which can tolerate up to 15% salt

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Table 7.1 Different microbial inoculants and their role in salinity mitigation in various crops Microorganism Bacteria Pseudomonas sp.

Crop

Mitigation mechanism

Reference

Rapeseed

Szymańska et al. (2019)

Enterobacter sp.

Rice & millet

Bacillus subtilis and Pseudomonas pseudoalcaligenes

Soybean

Azotobacter chroococcum and Azospirillum lipoferum Pseudomonas putida

Maize

Production of cellulose, IAA (Indole acetic acid), and siderophore, nitrogen fixation, antioxidant activity Producing an array of PGP traits, ACC-deaminase, and antioxidant enzymes. PGP activity (IAA, siderophores and ACC deaminase), activation of osmoregulators and antioxidant enzymes Antioxidant activity, increased selective absorption of Na+ and K+ ions PGP activity and activation of antioxidant defence enzymes

Bacillus sp.

Alfalfa

Rhizobium sp.

Chickpea

Bacillus aryabhattai and Arthrobacter woluwensis

Soybean

Pseudomonas spp., Alcaligenes sp., Klebsiella sp.,

Alfalfa

Enterobacter ludwigii, Acinetobacter bereziniae, and Alcaligenes faecalis

Pea

Fungi Aspergillus aculeatus

Arabidopsis thaliana

Perennial ryegrass

PGP activity and activation of antioxidant defence enzymes Antioxidant activity, enhanced photosynthesis, increased cell viability PGP traits, formation of EPS, and organic acid, IAA production. PGP activities (HCN production, nitrogen fixation, IAA production, phosphate solubilisation, siderophore production), antioxidant activity ACC deaminase, IAA production, Zn solubilisation, accumulation of osmolytes, antioxidant enzymes Improvement in plant photosynthetic efficiency, reduction of antioxidant enzymes activity (CAT and POD), decrease in oxidative stress

Sagar et al. (2020) Yasmin et al. (2020)

Abdel Latef et al. (2020) Srivastava and Srivastava (2020) Zhu et al. (2020) Mushtaq et al. (2021) Khan et al. (2021) Tirry et al. (2021)

Sapre et al. (2022)

Li et al. (2017)

(continued)

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Table 7.1 (continued) Microorganism Rhodotorula mucilaginosa

Crop Lactuca sativa

Trichoderma harzianum

Cucumber

Aspergillus ochraceus

Barley

Aspergillus terreus

Triticum aestivum

Yarrowia lipolytica

Zea mays

Piriformospora indica

Lycopersicon esculentum

Glomus spp.

Eucalyptus camaldulensis

Rhizophagus irregularis and Funneliformis mosseae Algae Codium taylorii or Pterocladia capillacea

Peanut

Radish

Ecklonia maxima

Cucurbita pepo

Fucus spiralis Ascophyllum nodosum seaweed extracts

Triticum durum Asparagus aethiopicus

Grateloupia filicina

Rice

Lessonia nigrescens

Triticum aestivum

Dunaliella salina

Maize

Mitigation mechanism Increase in photosynthetic pigment contents, reduction in proline and MDA contents, antioxidant activity Antioxidant activity, osmoregulation, maintenance of metabolic homeostasis. IAA production, antioxidant and antifungal activity IAA production, ACC deaminase, solubilised phosphate, siderophores activity High IAA, IAM production, antioxidant activity Maintained ion homeostasis (N, P, Ca, K, Na), increased water regulating genes Increased K+/Na+ ratio, chlorophyll content, and decreased leaf profiling content Antioxidant activity, regulated redox process, cell wall assembly, cell growth Synthesis of stress proteins, increased proline, total soluble proteins, alkaloids and phenolic content Increased chlorophyll content, improved nutritional status, and total biomass production Increased seed germination, growth, antioxidant activity Increased chlorophylls, phenolics, sugars, gas exchanges, proline, antioxidant activity Increased proline production, antioxidant activity Increased chlorophyll, antioxidant activities, regulation of intracellular ion Increased chlorophyll and total sugar content, antioxidant activity, and other PGP traits

Reference Silambarasan et al. (2019)

Zhang et al. (2019) Badawy et al. (2021) Khan et al. (2022)

Gul Jan et al. (2019) Ghorbani et al. (2019) Klinsukon et al. (2021)

Qin et al. (2021)

Kasim et al. (2016)

Rouphael et al. (2017) Latique et al. (2017) Al-Ghamdi and Elansary (2018) Liu et al. (2019) Zou et al. (2019) Dineshkumar et al. (2019) (continued)

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Table 7.1 (continued) Microorganism Dunaliella salina, Arthrospira maxima, Aphanothece sp., and Chlorella ellipsoidea, Chlorella vulgaris

Crop Tomato

Seaweed extract (Ascovip®)

Tomato

Maize

Mitigation mechanism Improved osmoregulation, ion homeostasis & absorption and reduced oxidative stress absorption Antifungal, antioxidant, and antimicrobial activity Antioxidant activity, reduced cell membrane oxidation

Reference Mutale-joan et al. (2021)

Gonçalves (2021) Zhang et al. (2023)

concentration; however, most cyanobacterial species do not tolerate concentrations above 5% (Kirkwood et al. 2008). Halotolerant cyanobacteria synthesise various osmoregulators under salt stress since osmotic adjustments enable them to gain resilience and adapt to the saline condition. They produce Exopolysaccharides (EPS) which form biofilms with other microorganisms and biosorb Na+. EPS enhance soil aggregation and produce plant-growth-promoting (PGP) substances. Several cyanobacteria are known for their important role in mitigating salinity, particularly in soil through exchanging the sodium with K or other less problematic metals (Kaushik and Subhashini 1985; Li et al. 2019). The successful use of cyanobacteria in salt-affected soils remediation extends across several soil types and climatic conditions, supporting the much-needed upscaling of technologies for large-scale applications (Chamizo et al. 2018; Pathak et al. 2018).

7.4

Challenges Faced in the Application of Microorganisms as Salinity-Mitigating Agents

Although there are a number of challenges to overcome before they can be successfully applied, microbial agents are being used more and more in sustainable agriculture to reduce salinity. Numerous potential microorganisms have been reported that have a high capacity for survival under salt stress, as they possess a number of mechanisms that improve the ability of crops to withstand and survive salinity stress (Ma et al. 2020; Egamberdieva et al. 2019). However, there aren’t many commercially viable solutions in the market that can be used to reduce crop salinity stress. This can be because microbial inoculants are not popular among farmers and have different formulation costs and difficult registration procedures. The quantity needed will be more for applications at a large scale with ideal functionality (Alori and Babalola 2018). Due to dynamic soil environment, microbial inoculants face difficulty in their establishment. To overcome this, co-inoculation with some organic amendment (Poria et al. 2022; Mukhopadhyay et al. 2021) or plant biostimulant (humic and fulvic acids, seaweed extracts, protein hydrolysates, chitosan, inorganic compounds, beneficial fungi, and bacteria) can be a promising option (Rouphael et al. 2017).

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173

Conclusion

With the increase in area coming under salinity, it is a major concern for the agricultural economy due to its severe effects on crop productivity. There are several mitigation strategies in practice including the use of microbial agents which is highly economic, effective, and sustainable. Salinity also suppresses the diversity of beneficial soil microbes through its detrimental effects which requires the use of multistress tolerant/salt tolerant microbial agents for enhancing crop yield and to support the crop in enduring salinity stress. Microbes produce 1-aminocyclopropane-1carboxylate deaminase, synthesise phytohormones, produce extracellular polysaccharides, stimulate the synthesis of plant osmolyte, maintain high K+/Na+ ratio, redox balance, increase the uptake of vital nutrients, and preserve high photosynthetic activity and stomatal conductance. Still, there are no microbial origin commercial products available in market due to their high-cost production, tedious registration process, and low awareness among farmers. In conclusion, we believe that the combination of these strategies has the potential to solve the problem of salinity stress. It is important that policymakers take initiative to aware the farmer community with these strategies. More focus should be given on commercialisation of stress-tolerant microbial inoculants to make them available globally. Acknowledgements VP acknowledges the DBT-JRF fellowship (award letter no. DBTHRDPMU/JRF/BET-22/I/2022-23/45) provided by the Department of Biotechnology, Government of India. SY (09/1152(0013)/2019-EMR-I) is a recipient of a fellowship from the Council of Scientific and Industrial Research (CSIR), Government of India. The agencies had no role in the interpretation or writing the manuscript.

References Abdel Latef AAH, Abu Alhmad MF, Kordrostami M, Abo-Baker A-BA-E, Zakir A (2020) Inoculation with Azospirillum lipoferum or Azotobacter chroococcum reinforces maize growth by improving physiological activities under saline conditions. J Plant Growth Regul 39(3): 1293–1306. https://doi.org/10.1007/s00344-020-10065-9 Adorada D, Ocampo R, Mendoza R, Singh R, Gregorio G (2004) Identification of alternate sources of salinity tolerance for rice breeding program. Plant breeding, genetics biotechnology division biennial report 2005:22 Afzal M, Hindawi SES, Alghamdi SS, Migdadi HH, Khan MA, Hasnain MU, Arslan M, Habib ur Rahman M, Sohaib M (2022) Potential breeding strategies for improving salt tolerance in crop plants. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10797-w Ahmed AU, Hernandez R, Naher F (2016) Adoption of stress-tolerant Rice varieties in Bangladesh. In: Gatzweiler FW, von Braun J (eds) Technological and institutional innovations for marginalized smallholders in agricultural development. Springer, Cham, pp 241–255. https://doi.org/10.1007/978-3-319-25718-1_15 Al-Ghamdi AA, Elansary HO (2018) Synergetic effects of 5-aminolevulinic acid and Ascophyllum nodosum seaweed extracts on Asparagus phenolics and stress related genes under saline irrigation. Plant Physiol Biochem 129:273–284. https://doi.org/10.1016/j.plaphy.2018.06.008 Alori ET, Babalola OO (2018) Microbial inoculants for improving crop quality and human health in Africa. Front Microbiol 9:2213. https://doi.org/10.3389/fmicb.2018.02213

174

V. Poria et al.

Badawy AA, Alotaibi MO, Abdelaziz AM, Osman MS, Khalil AMA, Saleh AM, Mohammed AE, Hashem AH (2021) Enhancement of seawater stress tolerance in barley by the endophytic fungus Aspergillus ochraceus. Meta 11(7):428. https://doi.org/10.3390/metabo11070428 Bello SK, Alayafi AH, Al-Solaimani SG, Abo-Elyousr KAM (2021) Mitigating soil salinity stress with gypsum and bio-organic amendments: a review. Agronomy 11(9):1735. https://doi.org/10. 3390/agronomy11091735 Bhise KK, Dandge PB (2019) Mitigation of salinity stress in plants using plant growth promoting bacteria. Symbiosis 79(3):191–204. https://doi.org/10.1007/s13199-019-00638-y Bleam W (2017) Chapter 6 - Acid-base chemistry. In: Bleam W (ed) Soil and environmental chemistry, 2nd edn. Academic Press, pp 253–331. https://doi.org/10.1016/B978-0-12804178-9.00006-9 Chamizo S, Rodríguez-Caballero E, Cantón Y, De Philippis R (2018) Soil inoculation with cyanobacteria: reviewing its’ potential for agriculture sustainability in Drylands. Agri Res Tech Open Access J 18(556046):001–005. https://doi.org/10.19080/ARTOAJ.2018.18.556046 Dineshkumar R, Subramanian J, Gopalsamy J, Jayasingam P, Arumugam A, Kannadasan S, Sampathkumar P (2019) The impact of using microalgae as biofertilizer in maize (Zea mays L.). Waste Biomass Valoriz 10(5):1101–1110. https://doi.org/10.1007/s12649-017-0123-7 Egamberdieva D, Wirth S, Bellingrath-Kimura SD, Mishra J, Arora NK (2019) Salt-tolerant plant growth promoting Rhizobacteria for enhancing crop productivity of saline soils. Front Microbiol 10:2791. https://doi.org/10.3389/fmicb.2019.02791 El Sabagh A, Hossain A, Barutçular C, Iqbal MA, Islam MS, Fahad S, Sytar O, Çiğ F, Meena RS, Erman M (2020) Consequences of salinity stress on the quality of crops and its mitigation strategies for sustainable crop production: an outlook of arid and semi-arid regions. In: Fahad S, Hasanuzzaman M, Alam M et al (eds) Environment, climate, plant and vegetation growth. Springer, Cham, pp 503–533. https://doi.org/10.1007/978-3-030-49732-3_20 Etesami H, Fatemi H, Rizwan M (2021) Interactions of nanoparticles and salinity stress at physiological, biochemical and molecular levels in plants: a review. Ecotoxicol Environ Saf 225:112769. https://doi.org/10.1016/j.ecoenv.2021.112769 Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci 10:470. https://doi.org/10.3389/fpls.2019.00470 FAO Soils Portal (2022) Food and Agriculture Organization of the United Nations. https://www. fao.org/soils-portal/data-hub/soil-maps-and-databases/global-map-of-salt-affected-soils/en/. Accessed 26 Dec 2022 Fernando L (1949) The performance of salt resistant paddy, Pokkali in Ceylon. Trop Agric 105: 124–126 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 38(9):1151–1163. https://doi.org/10.1007/s00299-019-02434-w Gonçalves AL (2021) The use of microalgae and cyanobacteria in the improvement of agricultural practices: a review on their Biofertilising, biostimulating and biopesticide roles. Appl Sci 11(2): 871. https://doi.org/10.3390/app11020871 Guimarães MJM, Simões WL, Oliveira AR, Araujo GGL, Silva ÊFF, Willadino LG (2019) Biometrics and grain yield of sorghum varieties irrigated with salt water. Revista Brasileira de Engenharia Agrícola e Ambiental 23:285. https://doi.org/10.1590/1807-1929/agriambi. v23n4p285-290 Gul Jan F, Hamayun M, Hussain A, Jan G, Iqbal A, Khan A, Lee I-J (2019) An endophytic isolate of the fungus Yarrowia lipolytica produces metabolites that ameliorate the negative impact of salt stress on the physiology of maize. BMC Microbiol 19(1):3. https://doi.org/10.1186/s12866018-1374-6 Hailu B, Mehari H, Tamiru H (2020) Evaluation of sorghum for salt stress tolerance using different stages as screening tool in Raya Valley, Northern Ethiopia. Ethiop J Agric Sci 30(4):265–276

7

Salinity Mitigation Using Microbial Inoculants

175

Hoque MN, Imran S, Hannan A, Paul NC, Mahamud MA, Chakrobortty J, Sarker P, Irin IJ, Brestic M, Rhaman MS (2022) Organic amendments for mitigation of salinity stress in plants: a review. Life 12(10):1632. https://doi.org/10.3390/life12101632 Hussain N, Ghaffar A, Zafar ZU, Javed M, Shah KH, Noreen S, Manzoor H, Iqbal M, Hassan IFZ, Bano H, Gul HS, Aamir M, Khalid A, Sohail Y, Ashraf M, Athar H-u-R (2021) Identification of novel source of salt tolerance in local bread wheat germplasm using morpho-physiological and biochemical attributes. Sci Rep 11(1):10854. https://doi.org/10.1038/s41598-021-90280-w Imadi SR, Shah SW, Kazi AG, Azooz MM, Ahmad P (2016) Chapter 18 - Phytoremediation of saline soils for sustainable agricultural productivity. In: Ahmad P (ed) Plant metal interaction. Elsevier, pp 455–468. https://doi.org/10.1016/B978-0-12-803158-2.00018-7 Irshad A, Ahmed RI, Ur Rehman S, Sun G, Ahmad F, Sher MA, Aslam MZ, Hassan MM, Qari SH, Aziz MK, Khan Z (2022) Characterization of salt tolerant wheat genotypes by using morphophysiological, biochemical, and molecular analysis. Front Plant Sci 13:956298. https://doi.org/ 10.3389/fpls.2022.956298 Jakhar D, Kumar N, Kumar S (2018) Performance of salt tolerant wheat varieties in salt affected soils. J Krishi Vigyan 6(2):184–186. https://doi.org/10.5958/2349-4433.2018.00071.5 Kamran M, Parveen A, Ahmar S, Malik Z, Hussain S, Chattha MS, Saleem MH, Adil M, Heidari P, Chen J-T (2020) An overview of hazardous impacts of soil salinity in crops, tolerance mechanisms, and amelioration through selenium supplementation. Int J Mol Sci 21(1):148. https://doi.org/10.3390/ijms21010148 Kasim WAE-A, Saad-Allah KM, Hamouda MM (2016) Seed priming with extracts of two seaweeds alleviates the physiological and molecular impacts of salinity stress on radish (Raphanus sativus). Int J Agric Biol 18:653–660. https://doi.org/10.17957/IJAB%2F15.0152 Katerji N, van Hoorn JW, Hamdy A, Mastrorilli M, Fares C, Ceccarelli S, Grando S, Oweis T (2006) Classification and salt tolerance analysis of barley varieties. Agric Water Manag 85(1): 184–192. https://doi.org/10.1016/j.agwat.2006.04.006 Kaushik B, Subhashini D (1985) Amelioration of salt-affected soils with blue-green algae. II. Improvement in soil properties. Proceedings of the Indian National Science Academy Part B: biological sciences 51:386–389 Khan MA, Sahile AA, Jan R, Asaf S, Hamayun M, Imran M, Adhikari A, Kang S-M, Kim K-M, Lee I-J (2021) Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant Biol 21(1):176. https:// doi.org/10.1186/s12870-021-02937-3 Khan MI, Ali N, Jan G, Hamayun M, Jan FG, Iqbal A, Hussain A, Lee I-J (2022) Salt stress alleviation in Triticum aestivum through primary and secondary metabolites modulation by Aspergillus terreus BTK-1. Front Plant Sci 13:779623. https://doi.org/10.3389/fpls.2022. 779623 Kirkwood AE, Buchheim JA, Buchheim MA, Henley WJ (2008) Cyanobacterial diversity and halotolerance in a variable hypersaline environment. Microb Ecol 55(3):453–465. https://doi. org/10.1007/s00248-007-9291-5 Klinsukon C, Lumyong S, Kuyper TW, Boonlue S (2021) Colonization by arbuscular mycorrhizal fungi improves salinity tolerance of eucalyptus (Eucalyptus camaldulensis) seedlings. Sci Rep 11(1):4362. https://doi.org/10.1038/s41598-021-84002-5 Kulhari PS, Chaudhary L (2008) Association studies for salinity tolerance in sorghum [Sorghum bicolor (L.) Moench]. Indian J Plant Genet Res 21(1):81–84 Kumar P, Sharma PK (2020) Soil salinity and food security in India. Front Sustain Food Syst 4: 533781. https://doi.org/10.3389/fsufs.2020.533781 Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP (2020) Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol 11:1216. https:// doi.org/10.3389/fmicb.2020.01216 Kumar P, Singh S, Pranaw K, Kumar S, Singh B, Poria V (2022a) Bioinoculants as mitigators of multiple stresses: a ray of hope for agriculture in the darkness of climate change. Heliyon 8(11): e11269. https://doi.org/10.1016/j.heliyon.2022.e11269

176

V. Poria et al.

Kumar R, Singh A, Bhardwaj AK, Kumar A, Yadav RK, Sharma PC (2022b) Reclamation of saltaffected soils in India: progress, emerging challenges, and future strategies. Land Degrad Dev 33(13):2169–2180. https://doi.org/10.1002/ldr.4320 Lal R (2015) Restoring soil quality to mitigate soil degradation. Sustainability 7(5):5875–5895. https://doi.org/10.3390/su7055875 Latique S, Mohamed Aymen E, Halima C, Chérif H, Mimoun EK (2017) Alleviation of salt stress in durum wheat (Triticum durum L.) seedlings through the application of liquid seaweed extracts of Fucus spiralis. Commun Soil Sci Plant Anal 48(21):2582–2593. https://doi.org/10.1080/ 00103624.2017.1416136 Li X, Han S, Wang G, Liu X, Amombo E, Xie Y, Fu J (2017) The fungus Aspergillus aculeatus enhances salt-stress tolerance, metabolite accumulation, and improves forage quality in perennial ryegrass. Front Microbiol 8:1664. https://doi.org/10.3389/fmicb.2017.01664 Li H, Zhao Q, Huang H (2019) Current states and challenges of salt-affected soil remediation by cyanobacteria. Sci Total Environ 669:258–272. https://doi.org/10.1016/j.scitotenv.2019.03.104 Liu H, Chen X, Song L, Li K, Zhang X, Liu S, Qin Y, Li P (2019) Polysaccharides from Grateloupia filicina enhance tolerance of rice seeds (Oryza sativa L.) under salt stress. Int J Biol Macromol 124:1197–1204. https://doi.org/10.1016/j.ijbiomac.2018.11.270 Ma Y, Dias MC, Freitas H (2020) Drought and salinity stress responses and microbe-induced tolerance in plants. Front Plant Sci 11:591911. https://doi.org/10.3389/fpls.2020.591911 Mohanavelu A, Naganna SR, Al-Ansari N (2021) Irrigation induced salinity and Sodicity hazards on soil and groundwater: an overview of its causes, impacts and mitigation strategies. Agriculture 11(10):983. https://doi.org/10.3390/agriculture11100983 Mukhopadhyay R, Sarkar B, Jat HS, Sharma PC, Bolan NS (2021) Soil salinity under climate change: challenges for sustainable agriculture and food security. J Environ Manag 280:111736. https://doi.org/10.1016/j.jenvman.2020.111736 Mushtaq Z, Faizan S, Gulzar B, Hakeem KR (2021) Inoculation of rhizobium alleviates salinity stress through modulation of growth characteristics, physiological and biochemical attributes, stomatal activities and antioxidant defence in Cicer arietinum L. J Plant Growth Regul 40(5): 2148–2163. https://doi.org/10.1007/s00344-020-10267-1 Mutale-joan C, Rachidi F, Mohamed HA, Mernissi NE, Aasfar A, Barakate M, Mohammed D, Sbabou L, Arroussi HE (2021) Microalgae-cyanobacteria–based biostimulant effect on salinity tolerance mechanisms, nutrient uptake, and tomato plant growth under salt stress. J Appl Phycol 33(6):3779–3795. https://doi.org/10.1007/s10811-021-02559-0 Pathak J, Rajneesh, Maurya PK, Singh SP, Häder D-P, Sinha RP (2018) Cyanobacterial farming for environment friendly sustainable agriculture practices: innovations and perspectives. Front Environ Sci 6:7. https://doi.org/10.3389/fenvs.2018.00007 Poria V, Jhilta P, Rana A, Khokhar J, Singh S (2022) Pressmud: a sustainable source of value-added products. Environ Technol Rev 11(1):187–201. https://doi.org/10.1080/21622515.2022. 2144767 Qin W, Yan H, Zou B, Guo R, Ci D, Tang Z, Zou X, Zhang X, Yu X, Wang Y, Si T (2021) Arbuscular mycorrhizal fungi alleviate salinity stress in peanut: evidence from pot-grown and field experiments. Food Energ Secur 10(4):e314. https://doi.org/10.1002/fes3.314 Rajabi Dehnavi A, Zahedi M, Ludwiczak A, Cardenas Perez S, Piernik A (2020) Effect of salinity on seed germination and seedling development of sorghum (Sorghum bicolor (L.) Moench) genotypes. Agronomy 10(6):859. https://doi.org/10.3390/agronomy10060859 Rouphael Y, De Micco V, Arena C, Raimondi G, Colla G, De Pascale S (2017) Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. J Appl Phycol 29(1):459–470. https://doi.org/ 10.1007/s10811-016-0937-x Safeena M, Sumanasinghe V, Bandara D (2003) Identification of RAPD markers for salt tolerance in rice. Postgraduate Institute of Agriculture, University of Peradeniya, Peradeniya Sagar A, Sayyed RZ, Ramteke PW, Sharma S, Marraiki N, Elgorban AM, Syed A (2020) ACC deaminase and antioxidant enzymes producing halophilic Enterobacter sp. PR14 promotes the

7

Salinity Mitigation Using Microbial Inoculants

177

growth of rice and millets under salinity stress. Physiol Mol Biol Plants 26(9):1847–1854. https://doi.org/10.1007/s12298-020-00852-9 Sagar A, Rai S, Ilyas N, Sayyed RZ, Al-Turki AI, El Enshasy HA, Simarmata T (2022) Halotolerant Rhizobacteria for salinity-stress mitigation: diversity, mechanisms and molecular approaches. Sustainability 14(1):490. https://doi.org/10.3390/su14010490 Saidimoradi D, Ghaderi N, Javadi T (2019) Salinity stress mitigation by humic acid application in strawberry (Fragaria x ananassa Duch.). Sci Hortic 256:108594. https://doi.org/10.1016/j. scienta.2019.108594 Sapre S, Gontia-Mishra I, Tiwari S (2022) Plant growth-promoting Rhizobacteria ameliorates salinity stress in pea (Pisum sativum). J Plant Growth Regul 41(2):647–656. https://doi.org/ 10.1007/s00344-021-10329-y Shahid SA, Taha FK, Ismail S, Dakheel A, Abdelfattah M (2011) Turning adversity into an advantage for food security through improving soil quality and providing production systems for marginal saline lands: ICBA perspectives and approach. In: Behnassi M, Shahid SA, D’Silva J (eds) Sustainable agricultural development: recent approaches in resources management and environmentally-balanced production enhancement. Springer, Dordrecht, pp 43–67. https://doi. org/10.1007/978-94-007-0519-7_3 Shahid SA, Zaman M, Heng L (2018) Salinity and sodicity adaptation and mitigation options. In: Zaman M, Shahid SA, Heng L (eds) Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. Springer, Cham, pp 55–89. https://doi.org/10.1007/978-3319-96190-3_3 Shaygan M, Baumgartl T (2022) Reclamation of salt-affected land: a review. Soil Systems 6(3). https://doi.org/10.3390/soilsystems6030061 Sheoran P, Kumar A, Sharma R, Singh M, Parjapat K, Singh RK, Sharma PC, Chahal VP (2021) Better resilience of wheat KRL 210: a boom for salt-affected ecologies. Indian Farm 70(12) Shilev S (2020) Plant-growth-promoting bacteria mitigating soil salinity stress in plants. Appl Sci 10(20):7326. https://doi.org/10.3390/app10207326 Silambarasan S, Logeswari P, Cornejo P, Abraham J, Valentine A (2019) Simultaneous mitigation of aluminum, salinity and drought stress in Lactuca sativa growth via formulated plant growth promoting Rhodotorula mucilaginosa CAM4. Ecotoxicol Environ Saf 180:63–72. https://doi. org/10.1016/j.ecoenv.2019.05.006 Singh RN (1950) Reclamation of ‘Usar’ lands in India through blue-green Algæ. Nature 165(4191): 325–326. https://doi.org/10.1038/165325b0 Singh RN (1961) Role of blue-green algae in nitrogen economy of Indian agriculture. Indian Council of Agricultural Research, pp 151–159 Singh R, Kumar A, Kharub AS, Kumar V, Chhokar RS, Selvakumar R, Chand R, Sharma I (2014) Barley cultivation in India (pocket guide), vol 53. Extention Buletin edn, Karnal Srivastava S, Srivastava S (2020) Prescience of endogenous regulation in Arabidopsis thaliana by pseudomonas putida MTCC 5279 under phosphate starved salinity stress condition. Sci Rep 10(1):5855. https://doi.org/10.1038/s41598-020-62725-1 Szymańska S, Dąbrowska GB, Tyburski J, Niedojadło K, Piernik A, Hrynkiewicz K (2019) Boosting the Brassica napus L. tolerance to salinity by the halotolerant strain Pseudomonas stutzeri ISE12. Environ Exp Bot 163:55–68. https://doi.org/10.1016/j.envexpbot.2019.04.007 Tirry N, Kouchou A, Laghmari G, Lemjereb M, Hnadi H, Amrani K, Bahafid W, El Ghachtouli N (2021) Improved salinity tolerance of Medicago sativa and soil enzyme activities by PGPR. Biocatal Agric Biotechnol 31:101914. https://doi.org/10.1016/j.bcab.2021.101914 Wani SH, Kumar V, Khare T, Guddimalli R, Parveda M, Solymosi K, Suprasanna P, Kavi Kishor PB (2020) Engineering salinity tolerance in plants: progress and prospects. Planta 251(4):76. https://doi.org/10.1007/s00425-020-03366-6 Yasmin H, Naeem S, Bakhtawar M, Jabeen Z, Nosheen A, Naz R, Keyani R, Mumtaz S, Hassan MN (2020) Halotolerant rhizobacteria Pseudomonas pseudoalcaligenes and Bacillus subtilis mediate systemic tolerance in hydroponically grown soybean (Glycine max L.) against salinity stress. PLoS One 15(4):e0231348. https://doi.org/10.1371/journal.pone.0231348

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V. Poria et al.

Zhang F, Wang Y, Liu C, Chen F, Ge H, Tian F, Yang T, Ma K, Zhang Y (2019) Trichoderma harzianum mitigates salt stress in cucumber via multiple responses. Ecotoxicol Environ Saf 170: 436–445. https://doi.org/10.1016/j.ecoenv.2018.11.084 Zhang L, Freschi G, Rouphael Y, De Pascale S, Lucini L (2023) The differential modulation of secondary metabolism induced by a protein hydrolysate and a seaweed extract in tomato plants under salinity. Front Plant Sci 13:1072782. https://doi.org/10.3389/fpls.2022.1072782 Zhu Z, Zhang H, Leng J, Niu H, Chen X, Liu D, Chen Y, Gao N, Ying H (2020) Isolation and characterization of plant growth-promoting rhizobacteria and their effects on the growth of Medicago sativa L. under salinity conditions. Antonie Van Leeuwenhoek 113(9):1263–1278. https://doi.org/10.1007/s10482-020-01434-1 Zou P, Lu X, Zhao H, Yuan Y, Meng L, Zhang C, Li Y (2019) Polysaccharides derived from the Brown algae Lessonia nigrescens enhance salt stress tolerance to wheat seedlings by enhancing the antioxidant system and modulating intracellular ion concentration. Front Plant Sci 10:48. https://doi.org/10.3389/fpls.2019.00048

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Cyanobacterial Bioinoculants for Abiotic Stress Management in the Changing Climate Scenario Shobit Thapa, Ritu Vishwakarma, and Yalavarthi Nagaraju

Abstract

Global climate change and subsequent anthropogenic activities have led to significant degradation of soil health ultimately affecting agriculture. Under such conditions, biofertilizers/bioinoculants play an important role in providing nutrients and other plant growth-promoting substances in an eco-friendly manner. Cyanobacteria are ecologically versatile microorganisms, occupying diverse habitats, from hot deserts to deep oceans and from saline lakes to thermal springs. They are known to improve soil and plant health by fixing atmospheric nitrogen, the release of nutrients from insoluble forms, and improving the texture and water-holding capacity of the soil. Cyanobacteria can ameliorate abiotic stress, mainly drought, salinity, and chemicals, by producing biological soil crusts, extracellular polysaccharides (EPS), and antimicrobial compounds to enhance plant growth and fertility by increasing the soil carbon content. Many are also helpful in heavy metal removal through the process of biosorption and bioaccumulation. The recent development of genetic engineering approaches has ensured the development of cyanobacterial strains with better stress-tolerant ability making agriculture more sustainable. Keywords

Biofertilizers · Exopolysaccharide · Osmoprotectants · Usar soil · Genetic engineering · Agriculture

S. Thapa (✉) · R. Vishwakarma · Y. Nagaraju ICAR- National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_8

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Introduction

The current global population is approximately 7.4 billion, with a projected increase to 9.8 billion by 2050 (DESA UN 2015). Global hunger and food instabilities are continuously increasing as a result of the remarkable growth in population worldwide and the stagnant performance of the agricultural sector. Future food security demands are expected to rise as a result of the growing world population. In developing and economically developed nations, agriculture is a significant source of an economy that employs about half of the working population, generates revenue for the rest, and provides raw materials for many industries (Chandio et al. 2019). Climate change is seriously affecting biodiversity and human resources by decreasing agricultural output (Naz et al. 2022). Major agricultural crops are being affected by climate changes (Murshed and Dao 2022) brought along by increasing yearly temperatures, changing rainfall patterns, floods, and declining water reserves and humidity levels in the surrounding environment. Moreover, incidences of land degradation and abiotic stresses have been on an increase owing to all these changes. Therefore, conditions like drought, salinity, heat, or heavy metals are causing extensive economic losses worldwide. The vast repertoire of microorganisms provides a chance to exploit and unravel the previously hidden resources by enhancing the efficacy of agricultural production to improve the adaptation and amelioration for encountering the detrimental effects of climate change so as to achieve the target of climate-smart agriculture. Among the variety of microorganisms, cyanobacteria are an important constituent of microbial diversity. They were the first microorganisms to produce gaseous oxygen which changed the atmosphere from anaerobic to mostly aerobic. Their spread is fairly extensive, having cosmopolitan distribution. They are even found in extreme habitats having high salinities, pH levels, and light irradiances (Castenholz 1996). Owing to their typical primitive characteristics and ubiquitous distribution they are often considered model organisms for depicting microbial distribution across continents and their evolution (Prasanna et al. 2009; Ahmed et al. 2010; Gupta et al. 2013). According to several pieces of research, cyanobacteria are widespread in various cultivable land and play a pivotal role in nutrient recycling through phosphate solubilization, biological nitrogen fixation, and mineral release to improve soil fertility for enhancing crop yield (Prasanna et al. 2009; Osman et al. 2010; Singh 2014). Numerous physiologically active compounds, including polysaccharides, amino acids, proteins, vitamins, carbohydrates, and phytohormones, which function as signal molecules to promote plant development, are produced and released by them. Therefore, they help to protect plants against various environmental stresses. Cyanobacteria potentially contribute to major biogeochemical cycles (e.g., nitrogen, carbon, and oxygen), which ultimately contribute to the production of biomass on Earth (Hader et al. 2007). In order to ensure better human health along with sustainable utilization of resources, it is imperative to produce clean foods without the use of chemical fertilizer. Presently, inorganic chemical-based fertilizers are

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mostly used in agricultural activities, which poses a significant threat to the ecosystem and human health (Itelima et al. 2018). In sustainable agriculture, chemical fertilizers are replaced by biofertilizers for enhanced crop productivity and soil health. Biofertilizers are a term used to describe products containing microorganisms that fix nitrogen from the atmosphere or release growth-promoting substances which promote dissolving soil nutrients (FAO 2006). Cyanobacteria-based bioinoculants aid in plant development and growth, increase agricultural yield, and assist plants in overcoming various challenges (Chaudhary et al. 2020). Given their potential for improving food quality and sustaining crop productivity, the utilization of cyanobacteria-based biofertilizers is increasing in demand. Various information is existing on the biofertilizer potential of cyanobacteria, however, their role in the mitigation of abiotic stress has been sparsely discussed. This chapter aims in discussing the role of cyanobacteria as bio inoculum to ameliorate various abiotic stress in light of the changing climate. Furthermore, we have discussed various biotechnological approaches to strain improvement using molecular tools.

8.2

Changing Climate and Agriculture

Climate and weather have a significant impact on agriculture. Climate change and agriculture are mostly interconnected with each other. Climate change drastically affects agriculture in several ways, through fluctuations in average temperatures (heat and cold stress), erratic distribution of rainfall (drought and floods), and higher occurrence of biotic stresses (pests and diseases). There is a huge level of transformation to the local climate as laid out framework, neighborhood rural practices, and individual experience, despite the fact that farmers are regularly versatile in adapting to the climate and its year-to-year uncertainty. Thus, it is reasonable to anticipate that climate change will have an effect on agriculture, potentially posing a danger to existing components of farming systems while also offering prospects for advancement. Climate change refers to the continuing modulations in temperatures and weather patterns ranging from a few decades to several million years (Enete and Amusa 2010). Food quality and access are also impacted by climate change, which can also affect the food supply (Battisti and Naylor 2009). Crop suitability and productivity are expected to rise and spread northward in mid- and high-latitude regions, notably for cereals and rabi crops (Olesen et al. 2007). For instance, decreasing agricultural output may be a result of expected temperature rises, modifications to precipitation patterns, modifications to extreme weather events, and decreases in water availability. There are several ways that agriculture may be impacted by climate change. Warming tends to decrease yields over a specific temperature range because crops develop more quickly and produce less grain as a result. Additionally, rising temperatures hinder plants’ capacity to absorb and utilize rainfall. Due to increasing temperature, the rate of transpiration in plants increases, leading to a subsequent loss of moisture from their leaves, which speeds up soil evaporation. Moreover, one of the main causes of climate change, carbon emissions,

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may also benefit agriculture by boosting photosynthesis in a number of C3 crops (e.g., rice, wheat, and cotton). C4 crops (e.g., maize and sugarcane), which make up roughly one-fourth of all crops in terms of value, are not greatly aided by this occurrence, however, they are benefitted during low water availability (Hamim 2005).

8.3

Cyanobacterial Bioinoculants for Sustainable Agriculture

Cyanobacteria are a primitive group of organisms showing resemblance to bacteria in cell structure, however, exhibiting plant-like functional characteristics of oxygenic photosynthesis. They are known to sequester carbon and fix nitrogen, thereby helping in nutrient recycling. They can also be used as potential food supplements with nutritional, therapeutic, and beneficial values. With the onset of the Green Revolution, chemical fertilizer use is on the increase causing depletion in human health and soil quality. Therefore, microbe-based technological interventions, mainly biofertilizers, are an eco-friendly option to mitigate chemical problems. Living microorganisms known as “bio-fertilizers” can enhance soil quality, contribute nutrients to the soil, solubilize insoluble phosphate compounds, and generate chemicals that encourage plant development. As a result, they are helpful to the general health of the plants and their ability to thrive. On application to soil, seeds, or plants, biofertilizers encourage plant development by boosting the host plant’s nutrient availability. Cyanobacteria-based bio inoculum, because of its low cost and ease of maintenance, has developed numerous biotechnological applications. They are known to improve soil fertility, texture, porosity, and water-holding capacity of the soil. They can also metabolize a number of pollutants while performing multiple roles in the terrestrial ecosystem to sustain soil fertility. Owing to its prominent role in the conservation and maintenance of soil fertility, it can be used as a biofertilizer. The presence of cyanobacteria in the root region (rhizosphere) has improved its effectiveness owing to its close proximity to the root. In an interesting study, cyanobacterial strains were reported near the root until the wheat crop harvest, where they also gained entry into the roots (Karthikeyan et al. 2009) revealed through electron microscopic observations (Jaiswal et al. 2008). They reported an increase in soil fertility and plant growth parameters along with improved crop biomass and yield. Cyanobacteria can benefit the soil and plant in a number of ways; (1) improve the porosity of soil and produce adhesive substances; (2) produce bioactive metabolites like phytohormones, vitamins, and amino acids; (3) enhance the water-holding capacity of soil; (4) improve the organic matter of soil through death and decomposition; (5) decrease soil salinity; (6) control weed growth; (7) solubilization of inorganic phosphates through organic acids; and (8) bioremediate heavy metals through the exopolysaccharide layer. Cyanobacteria are less studied as PGPR (Plant growth promoting rhizobacteria) but have been studied for nitrogen dynamics in paddy crops. They play a key role in rice fields, growing on the paddy soil’s surface, and in waterlogged paddy fields.

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Due to its capacity for fixing nitrogen and its simultaneous release of several bioactive chemicals into the soil advantageous to rice plant growth, cyanobacteria can be employed as a biofertilizer in paddy fields. Some of the most common cyanobacteria used in rice fields are Calothrix, Scytonema, Nostoc, Tolypothrix, Anabaena, and Aulosira, where they can fix 20–30 kg nitrogen ha-1 along with organic matter. Also, the inoculation of cyanobacteria can raise rice yields by 5% to 20% (Nayak et al. 2004, 2009). Additionally, it has been demonstrated that Anabaena spp. can biologically suppress phytopathogenic fungi. The capacity of Nostoc, Phormidium, and Oscillatoria to break down and remove herbicides and organophosphorus pesticides results in better soil for farming. Their role has undergone a drastic change in recent years where they have been used as bioinoculants in not only rice but also a number of diverse crops (Nain et al. 2010; Manjunath et al. 2016). Karthikeyan et al. (2007, 2009) demonstrated that cyanobacterial bioinoculants when inoculated into the soil release various bioactive metabolites (phytohormones, amino acids, and organic acids) into their vicinity, thereby improving the microbial load, which demonstrated the agronomic potential of these strains, providing evidence as ideal candidates for the development of inoculants for the wheat crop. Interaction between agriculturally useful heterotrophic and autotrophic bacteria and cyanobacteria can be effective as biofertilizers and biocontrol agents. Plant– microbe interaction increases nutrient uptake and improves biomass production and remediation of polluted/inhospitable environments. Field evaluation of promising cyanobacterial and bacterial strains revealed the promise of combinations of cyanobacteria–bacteria in enhancing crop biomass and yields. It has been observed that any bioinoculant has to compete with the native flora of the soil in order to establish itself in that particular niche. Cyanobacteria can survive in their exopolysaccharide sheath for a longer period of time and also form biofilms in combination with other bacteria or fungi which can further increase their competence. A number of compilations on cyanobacteria from different soils of India exist, but the emphasis has been solely with respect to their nitrogen-fixing potential and limited published work exists on the production of bioactive compounds and their interactions with crop plants.

8.4

Cyanobacterial Bioinoculants for Abiotic Stress Management

Crops are currently facing a problem due to changing climate and are prone to a number of abiotic and biotic stress factors. Abiotic stress can be categorized into different types like water shortage or excess, which can be represented as drought and floods, respectively, temperature, which can be high or low, or chemical, which is represented by the saline environment of the soil, containing high concentrations of ions like K+, Ca+2, Mg+2, and Na+ as well as heavy metals. Plants deal with these abiotic stresses (salinity tolerance, drought tolerance, nutrient-poor or saline-alkali

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Fig. 8.1 Cyanobacteria and abiotic stress management. ROS reactive oxygen species, POX peroxidase, APX ascorbate peroxidase, SOD superoxide dismutase, CAT catalase, HSP heat shock protein (molecular chaperones), smtA metallothionein gene (heavy metal remediation)

soils, and heavy metal pollution) in interactions with microbial communities, which are vital to plants’ survival and health. The dynamic change in their activity and composition in response to different environmental conditions is a reflection of soil health which needs to be carefully monitored (Cramer et al. 2011; Sneha et al. 2021). Cyanobacteria employ a wide range of mechanisms to combat this abiotic stress (Fig. 8.1). Cyanobacteria can synthesize a wide range of bioactive chemicals to combat abiotic stresses in nature (Saijo and Loo 2020). Production of vitamins, amino acids, hormones, exopolysaccharides, antioxidant molecules, and compatible solutes is important in ameliorating a number of stressful conditions. Moreover, the potential for nitrogen fixation along with the regulation of ion metabolism is an important tool in stress management. Plant germination can also be enhanced by utilizing cyanobacterial bioinoculum under drought stress or contaminated water supply with heavy metals (Poveda 2020). Chua et al. (2020) demonstrated that cyanobacterial inoculations improve the chances of plant growth and colonization in order to restore desert environments. Plants are often subjected to a number of environmental stresses that retard their development and yield (Gull et al. 2019). Cyanobacteria produce a variety of bioactive compounds to shield them from those abiotic stresses. It was previously emphasized that the cyanobacterial strains can augment the plant’s tolerance to stress manifestations through different types of mechanisms, including either or a combination of them as (1) Release of osmoprotectants in salinity stress conditions, (2) An increase in the rhizosphere’s biological activity (CO2 evolution, nitrogenase activity, and dehydrogenase activity), (3) Increasing root length and promoting seedling growth, (4) Production of gibberellins, auxin (IAA), and cytokinins that maintain plant hormone homeostasis, (5) Production of ACC to regulate the ethylene concentration (plant stress phytohormone), (6) Plant transformation with stress responsive gene, (7) Produce exopolysaccharides that protect plant roots from desiccation and

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assist in the nutrients solubilization that is poorly available to plant, (8) Modulation of plant antioxidant machinery to decrease the concentration of reactive oxygen species, (9) Improve plants performance through incorporation of beneficial cyanobacterial gene through genetic engineering, (10) To reduce mobility and transport of heavy metals and xenobiotics in plant, and (11) Plant growth stimulation is a function of their features that promote plant growth (Jittawuttipoka et al. 2013; Chittapun et al. 2018; Usharani and Naik 2019; Mutale-Joan et al. 2021). A summary of various cyanobacterial-mediated amelioration mechanisms of different abiotic stresses has been provided in Table 8.1.

8.4.1

Salinity Tolerance

Salinization encompasses the deposition or accumulation of water-soluble salts in the soil surface to an amount that has a negative influence on soil health, environmental health, and agricultural productivity. Salinity is a massive problem for the agricultural field in many regions of the world. Around 831 million hectares of soils, including saline and clay soils, are affected by salt on a worldwide scale. Saline soil is defined as soil with an electrical conductivity (EC) of >4 dS/m, which produces an osmotic pressure of 0.2 MPa (Karthika and Govintharaj 2022). Cyanobacteria strains can use various strategies to decrease Na+ uptake and its active efflux through the Na+/H+ antiport. The production of organic substances to maintain the osmotic pressure, the development of the antioxidative defense mechanism to detoxify reactive oxygen species, and the expression of a group of salt-inducible proteins to effectively deal with salinity stress along with the accumulation of compatible solutes when exposed to salt stress are some of the defense responses used by cyanobacteria (Tijen and Ismail 2006; Rezayian et al. 2019). Compatible solute’s main purpose is to increase internal osmolality and protect against water loss and plasmolysis. Additionally, these compounds have direct anti-denaturation properties for membranes and enzymes under salt stress (Bremer and Kramer 2000; Borges et al. 2002). Common osmoprotectants in cyanobacteria include glucosyl glycerol, sucrose, trehalose, glycine betaine, and glutamate. Cyanobacteria are currently believed to be tolerant to salinity making them appropriate bioinoculant material for use under field conditions (Apte and Bhagwat 1989; De Philippis and Vincenzini 1998; Malam et al. 2007; Singh and Dhar 2010). They can colonize different stressful conditions by excreting a wide variety of physiologically active metabolites into rhizospheric soil, which helps plants in their colonization. These metabolites might trigger severe reactions in plants against many stress conditions. Regarding their protein synthesis, the cyanobacteria respond to salt stress in various ways: (1) by downregulating the expression of some protein molecules, (2) by enhancing the expression of some proteins, and (3) by expressing specific salt-stress proteins. As a response to high salinity stress, Anabaena torulosa and Anabaena sp had some critical changes in their protein profile (Apte and Bhagwat 1989; Pandhal et al. 2009). Rodríguez et al. (2006) studied the growth of rice plants in the presence of the cyanobacterium Scytonema hofmanni under salt

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Table 8.1 Summary of various tolerance mechanisms adopted by cyanobacteria against abiotic stresses Cyanobacterial strains Scytonema hofmanni

Plant/ Substrate Rice

Stress Salinity

Dunaliella salina

Wheat

Salinity

Anabaena variabilis

Medicago

Salinity

Nostoc muscorum, Anabaena anomala, A. fertilissima

Rice

Salinity

Arthrospira maxima, Aphanothece sp. Chlorella ellipsoidea and Dunaliella salina Anabaena and N. kihlmani

Tomato

Salinity

Wheat

Degraded soil

Oscillatoria prínceps, Lyngbya mucicola, Leptolyngbya, Gloeocapsa, Microcoleus Scytonema tolypothricoides, Hapalosiphon intricatus, Calothrix braunii, and Tolypothrix ceylonica Nostoc punctiforme and N. ellipsosporum

Rice

Salinity

Rice

Pearl milletwheat system

Stress tolerance mechanisms Production of extracellular substances that act as plant growth regulators similar to gibberellin Exopolysaccharides from the microalgae enhanced the germination of the plant Expression of flavodoxin from the cyanobacteria improved the nitrogen fixation under stress Improved nutrient content and microbial enzymes of the soil. Proline content was enhanced in the plant Better plant growth and increased antioxidant enzyme activities

Reference Rodríguez et al. (2006)

El Arroussi et al. (2016)

Coba de la Pena et al. (2010)

Abbas et al. (2015)

Mutale-joan et al. (2021)

Enhanced soil physicochemical properties Enhanced nutrient content and organic matter in the soil

Gheda and Ahmed (2015)

Sodic soil

Decrease in electrical conductivity, pH, and exchangeable Na

Kaushik and Subhashini (1985)

Salinity and nutrient poor

Enhancement of nutrient status, physical structure, and improved microbial activity

Nisha et al. (2018)

Jan et al. (2017)

(continued)

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Table 8.1 (continued) Cyanobacterial strains Anabaena torulosa

Plant/ Substrate Coastal soils

Nostoc microscopicum, Microcoleus paludosus Leptolyngbya ohadi

Acacia hilliana, Senna notabilis Sandy substrate Greenhouse trial

Dryland

Increased germination and seedling growth

Nutrient poor Salinesodic soil

Oscillatoria agardhii

Wheat

Dry land

Spirulina platensis

Maize

Heavy metal (Cd)

Aulosira fertilissima, Nostoc muscorum, Anabaena variabilis, and Tolypothrix tenuis Oscillatoria sp., Synechocystis sp.

Coal fly ash

Heavy metal (Cu, Zn, Cr, Pb)

Cyanobacteria help in the formation of BSCs Increased microbial activity and soil aggregate stability Increase in the activity of hydrolytic and defense enzymes (catalase, superoxide dismutase, and peroxidase) that improved plant growth Accelerates seed germination and enhances plant development by preventing Cd accumulation and translocation Bioleaching of heavy metals from coal fly ash

Wheat

Heavy metal (Cr)

Culture conditions

Salt and metal stress (Co, Cd)

Nostoc muscorum

Synechocystis PCC6803

Stress Sodic soils

Stress tolerance mechanisms Nitrogen fixation and EPS

Biotransformation of Cr into non-toxic forms Exopolysaccharides

Reference Apte and Thomas (1997) Munoz-Rojas et al. (2018), Ibraheem (2007) Mugnai et al. (2018) De Caire et al. (1997) Haggag et al. (2018)

Seifikalhor et al. (2019)

Kaur and Goyal (2018)

Faisal et al. (2005) Jittawuttipoka et al. (2013)

stress and found out that the bioactive metabolites released by the cyanobacterium helped the plant to evade stressful conditions. Additionally, enhancing plant tolerance through nitrogen fixation, extracellular polysaccharide production, active ion export, and the formation of appropriate soluble compounds, hormones, and antioxidant enzymes, significantly influenced the interaction between various microbial groups (Li et al. 2019). In an interesting study, the cyanobacterial flavodoxin gene was introduced into the legume Medicago truncatula and under salinity stress, the

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gene provided an enhanced legume symbiont performance (Coba de la Pena et al. 2010). Bell pepper (Capsicum annum L.) plants cultivated by the hydroponics method under salt stress observed an increase in growth parameters, the water content of leaves, and the antioxidant machinery when a foliar spray of cyanobacteria Roholtiella sp. was applied (Bello et al. 2021). Mutale-Joan et al. (2021) using the cyanobacterial-microalgal formulations of Arthrospira maxima, Aphanothece sp., Chlorella ellipsoidea, and Dunaliella salina enhanced the growth of tomato plants under salt stress by improving pigment content, ion homeostasis, and nutrient uptake.

8.4.2

Drought Tolerance

The most concerning abiotic stress types are those that include water since they are one of the key factors limiting plant growth and production worldwide (Martins et al. 2018). In addition to economic losses, this stress decreases the amount of food available for humans and animals (Verma et al. 2018). Therefore, it is highly imperative to mitigate the effects of drought manifestations so that plant growth could be maintained in order to meet the world’s food production demand (Goswami and Deka 2020). The growing frequency of drought is a challenge to agricultural output, according to estimates, almost half of the world’s fertile land would experience drought by 2050, which will have an impact on global output (Jochum et al. 2019). The use of some drought-tolerant cyanobacterial bioinoculants to protect against drought conditions provides a better answer for restoring soil fertility and productivity. Inoculation of Acacia hilliana, and Senna notabilis by Nostoc sp. and Microcoleus sp., can enhance seedling growth and improve germination in drought conditions, thereby promoting dryland restoration (Munoz-Rojas et al. 2018). Similar results were obtained by Ibraheem (2007) in lettuce plants, where inoculation with Anabaena oryzae and Spirulina meneghiniana in arid conditions improved the plant’s vigor. In an interesting study, a transformation of the acidic water stress protein from Nostoc commune, wspa1 gene, was inserted into the model plant Arabidopsis thaliana conferring the host with resistance to osmotic stress (Ai et al. 2014). Similarly, drnf1 gene from the drought-tolerant cyanobacteria Nostoc flagelliforme containing P loop NTPase responsible for cellular processes and stress response increases tolerance to salinity by improving germination in Arabidopsis (Cui et al. 2018).

8.4.3

Heavy Metal Tolerance

The term “heavy metal” describes metallic elements with atomic masses between 54.63 and 200.59 and a relatively high density (5 g/cm3), as well as those that are toxic even at low concentrations (Dias 2002; Li et al. 2019). Two general categories may be used to categorize heavy metals. The first category includes metals that are necessary for many species in trace amounts, while others are not required in any

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amount and are poisonous at higher concentrations. As, Fe, Cr, Co, Cu, Ni, Se, Va, and Zn are members of the former group, whereas Pb, Hg, Cd, Ur, and Ag are all members of the second group and extremely hazardous even at very low concentrations (Inthorn 2001). It is widely recognized that many different cyanobacterial species could bioremediate soils and bodies of water from pollutants like heavy metals or pesticides, which have significant agricultural uses (Kumar et al. 2020). Cyanobacteria are known to cope with heavy metal stress by modification of their protein profile which can be expressed during various stages of their growth (Chakdar et al. 2022). According to research, many cyanobacterial species could remove lead, chromium, copper, and zinc from coal fly ash, including Aulosira fertilissima, Anabaena variabilis, Tolypothrix tenuis, and Nostoc muscorum (Kaur and Goyal 2018). Oscillatoria sp. and Synechocystis sp removed 62.1% and 39.9% of Cr, respectively, and also improved various growth parameters in wheat seedlings (Faisal et al. 2005). Through seed priming, the use of Spirulina platensis helps accelerate seed germination and enhance plant development by preventing Cd from moving from roots to shoots (Seifikalhor et al. 2019). On the other hand, Xu et al. (2010) demonstrated that the SmtA gene, which codes for metallothionein from Synechococcus sp., transforms A. thaliana plants to increase Zn tolerance by increasing its antioxidant enzyme activity. Cyanobacterial species, Spirulina platensis, interact with positive charges in heavy metals due to the various negative charges contained in their released exopolysaccharides, acting as a chelating agent. In many investigations using heavy metals, Cd biosorption by Spirulina platensis has been described (Rangsayatorn et al. 2002; Murugesan et al. 2008).

8.4.4

Nutrient Poor or Saline-Alkali Soils

The main benefit of using cyanobacteria to restore salt-damaged soil is that it is more environmentally friendly than chemicals. In the remediation process, no more salts are used. Cyanobacteria promote soil fertility in a sustainable manner while also improving soil structure. According to research, some cyanobacterial strains such as Calothrix braunii, Hapalosiphon intricatus, Scytonema tolypothricoides, and Tolypothrix ceylonica grown for 105 days can act as gypsum and reclaim sodic soils (Kaushik and Subhashini 1985). Alkaline or excessively salty soil is not suitable for the development of plants. There are typically three types of soils that are influenced by salt: saline soil, sodic soil, and saline-sodic soil (Nouri et al. 2017). Usar soils are highly saline soils that are nonproductive in nature due to the hard impervious layer they form on the surface. They can be divided into sodic and saline soils. Sodic soils are specialized saline soils containing a high proportion of sodium ions as compared to other cations. These soils are deficient in major nutrients like nitrogen, phosphorus, and zinc. As the salt leaches down, more sodium ions get bound to clay particles displacing useful cations like Ca2+. This can interfere with soil structure. Cyanobacteria or salt-tolerant plants used individually or together might be an efficient technique to mitigate high soil salt levels thereby promoting soil fertility

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(Jesus et al. 2015). Cyanobacteria usually grow in these soils by accumulating certain osmolytes or compatible solutes like inorganic ions, and organic compounds to increase their internal osmotic pressure so as to withstand the external osmotic situation. Over a period of time with the help of cyanobacteria, soil quality is improved by a decrease in the pH due to the release of organic acids, a reduction in exchangeable sodium content, and an increase in nutrient content, organic matter, and water-holding capacity of soils. Secretion of organic acids also helps in the solubilization of nutrients and the dissolving of insoluble carbonate nodules. They also improve soil aggregation by increasing hydraulic conductivity. Pyrite, a chemical used to reclaim sodic soils, often causes toxicity due to incomplete oxidation and releasing ferrous and sulfide ions. Cyanobacterial inoculation can significantly reduce the sulfide and iron in soils (Aiyer et al. 1972). Pandey et al. (2005) used N. calcicola to reclaim alkaline soils in the laboratory. They also used a mutant (bicarbonate resistant) strain which showed better growth. Cyanobacteria also help in the maintenance of the fertility of nutrient-poor soils. They are involved in the cycling of macro and micronutrients as well. Inoculating soil with cyanobacteria-based formulations has been known to enhance the concentration of micronutrients in the soil as well as in plants such as Zn in maize leaves and Fe, Zn, Mn, and Cu in wheat grains (Rana et al. 2012). Although the mechanics of soil microalgal inoculations enriching plants with micronutrients are not fully known, one theory puts the creation of siderophores by cyanobacteria as a potential method (Rana et al. 2012). Siderophores are low-molecular-weight nitrogenous compounds having a high affinity for Fe+3 and help the binding of iron or other metals from outside to within the cells (Prasanna et al. 2015; Chakraborty et al. 2019). When it comes to crop production, nitrogen (N) is commonly the most expensive and abundant nutrient (Sharma et al. 2011). The quantity of nitrogenous fertilizers used worldwide for agriculture increased from 84 to 109 megatons between 2002 and 2018 (FAOSTAT 2020), yet approximately most of the applied fertilizer is not utilized by the crops and is lost to the environment (Bouwman et al. 2009). For example, about 50–60% of nitrogen fertilizer applied to rice fields is lost due to nitrification and denitrification, leaching, volatilization, and surface runoff, or it might be incorporated by microbes as biomolecules (De Datta 1987). Some cyanobacteria can fix atmospheric nitrogen and provide it to the host for growth. This group of cyanobacteria contains the enzyme nitrogenase which is responsible for the fixation of gaseous nitrogen into ammonium ions utilizing ATP in the process (Magnuson 2019). Cyanobacteria can also convert insoluble organic phosphates into soluble forms and mobilize them to plants with the aid of phosphatase enzymes. The insoluble forms of calcium such as Ca3(PO4)2, FePO4, AlPO4, and hydroxylapatite [Ca5(PO4)3OH] may all be dissolved by cyanobacteria in soils and sediments (Prasanna et al. 2012; Cameron and Julian 1988). Solubilization can be brought about by two methods

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1. They synthesize a chelator for Ca2+ without changing the pH of the growing medium, which causes the dissolution to move to the right (Roychoudhury and Kaushik 1989). Ca10ðOHÞ2ðPO4Þ6 → 10Ca2 þ þ2OH - þ 6PO4 3 2. They can also solubilize phosphorus using organic acids using the following equation (Bose et al. 1971) Ca3ðPO4Þ2 þ 2H2CO3 → 2CaHPO4 þ CaðHCO3Þ2 In a study by Prasanna et al. (2013), cyanobacterial strains viz. Anabaena doliolum, A. torulosa, Nostoc carneum, and N. piscinale grown with rice crop under non-flooded conditions produced acid phosphatases and alkaline phosphatases for the solubilization of phosphate, and it was observed that available P was more in the cyanobacterial amended treatments as compared to the control ones.

8.5

Biotechnological Interventions for Strain Improvement

Cyanobacteria are photosynthetic prokaryotes with an untapped potential for the production of a variety of metabolic products. The short life cycle, simpler cellular structure, and amenability to genetic changes make them attractive both as models to study photosynthesis and as hosts for biotechnological applications. Integration of system biology and synthetic biology to transform or construct an efficient cyanobacterial strain has further broadened the scope of genetic engineering. Modern tools like promoter engineering, riboswitches, and genome editing tools like CRISPR/Cas 9, TALENS, and ZFN are being used to obtain cyanobacteria with desired properties (Verma et al. 2022). Table 8.2 provides an overview of the various genetic approaches used to modify cyanobacteria or plant hosts with the desired gene of interest for enhanced stress management. Host selection for conventional metabolic engineering depends on a higher growth rate as well as the productivity of cyanobacteria which is often a prerequisite for the inoculum for induction of Biological Soil Crust (BSCs) formation. EPS production is generally carried out in two types of hosts, native and heterologous hosts. Heterologous hosts are often employed when the native hosts are slow growing or unculturable. However, with the help of synthetic biology tools like gene knockout and overexpression, the native hosts can be used for the production of various stress protectants (Tiwari et al. 2019). EPS is an example of secondary metabolites easily expressed in native producers. Heterologous hosts could be metabolically engineered to boost production. System biology tools like media optimization and Genome-Scale modeling (GSM) have also shown good potential in this regard. GSM incorporates mathematical models that are used to engineer metabolic pathways for strain improvement through the optimization of metabolic fluxes for enhanced product formation (Fang et al. 2020). Certain transcriptional regulators like sigma factors can also regulate the transcriptional

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Table 8.2 Genetic improvement strategies using cyanobacterial-based gene for enhanced stress management Cyanobacteria Synechococcus PCC 7942

Expression Host Arabidopsis thaliana

Gene of interest Overexpression of bacterial metallothionein SmtA

Aphanothece halophytica

Populus alba

Overexpression of molecular chaperone DnaK

Nostoc commune

Arabidopsis thaliana

Nostoc flagelliforme

Synechocystis sp. PCC 6803 and Arabidopsis thaliana

Heterologous expression of water stress protein Wspa1 Heterologous expression of drnf1 gene containing P loop NTPase

Anabaena PCC 7119

Nicotiana tabacum

Incorporation of cyanobacterial flavodoxin in the host

Synechococcus elongatus PCC6301

S. elongatus PCC 7942

Overexpression of rbcLS gene

Synechococcus PCC 7942, Synechocystis PCC6803

Synechococcus PCC 7942

Promoters from different cyanobacteria were inserted with Rubisco gene from Allochromatium vinosum

Trait Enhanced Zn tolerance by increased activities of antioxidant enzymes Salinity, drought, and low temperature tolerant Enhanced protection against osmotic stress

Reference Xu et al. (2010)

Enhance respiration metabolism and expression of salt tolerant genes in cyanobacteria; improve seed germination of plants under saline conditions Improved tolerance against a variety of stresses, including high irradiation, UV, herbicides, drought, and extreme temperatures Efficient CO2 sequestration by increased activity of Rubisco to produce isobutyraldehyde and isobutanol Increased photosynthetic activity under high irradiance and high CO2 concentration

Cui et al. (2018)

Takabe et al. (2008) Ai et al. (2014)

Tognetti et al. (2006)

Atsumi et al. (2009)

Iwaki et al. (2006)

(continued)

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Table 8.2 (continued) Cyanobacteria Synechocystis PCC6803

Nostoc HK-01

Expression Host Synechocystis PCC6803

Anabaena PCC 7120

Gene of interest petE promoter sequence was inserted in PEP carboxylase

Expression of sigma factor sigJ

Trait PEP carboxylase activity was regulated for increased carbohydrate content Enhanced release of EPS

Reference Yan et al. (2015)

Yoshimura et al. (2007)

activity in the cells. Overexpression of sigJ in Anabaena sp. PCC7120 caused a 3.2fold higher production of EPS (Yoshimura et al. 2007). The rapid increase in the levels of atmospheric CO2 levels and other greenhouse gases has necessitated their sequestration from the planet. Therefore, the fixation of CO2 by cyanobacteria through the Calvin cycle is an important biochemical process where CO2 is converted to photosynthetic metabolic products. It has been reported that the low catalytic rate and specificity of RuBisCO is the major bottleneck for high C fixation rates in cyanobacteria (Whitney et al. 2011). Rubisco enzyme consists of two subunits which are encoded by rbcL and rbcS genes that are co-transcribed through the same promoter in cyanobacteria. RuBisCO activity was found to improve 1.4fold after overexpression of both genes from Synechococcus elongatus sp. PCC6301 in S. elongatus PCC 7942 (Atsumi et al. 2009). Similarly, after the incorporation of two different promoters, it could be enhanced four times in Synechococcus sp. PCC 7942 (Iwaki et al. 2006). As RuBisCO is conserved across species, where some wild-type variants are slightly more effective than others, superior RuBisCO mutants can be identified and engineered for improved carbon fixation. Phosphoenolpyruvate carboxylase (PEP Case) is another enzyme having an important role in CO2 fixation which helps in the conversion of oxaloacetic acid from Phosphoenolpyruvate. Cyanobacteria PEPcase has been reported to fix one-fourth of the total assimilable CO2 along with malic enzyme. Yan et al. (2015), with the aid of petE promoter, expressed pepC gene in Synechocystis PCC6803 which improved the fixed carbon content and further decreased the loss of fixed carbon in the TCA cycle through the PEPC pathway. In another experiment, pepC mutated in Anabaena sp. PCC 7120 showed blockage of dark respiration (Jia et al. 2015). Incorporating a synthetic carbon fixation pathway from a thermophile has also been reported recently where multiple genes of the 3-hydroxy propionate pathway were inserted into Synechococcus sp. PCC 7942 (Shih et al. 2014). Cyanobacteria usually contain chlorophyll and carotenoid molecules for the absorption of light. Additionally, they even contain phycobilisomes which can absorb light energy across variable wavelengths and shuttle it to the reaction center. Therefore, the genes responsible for their regulation can be probable targets for augmenting light exploitation in cyanobacteria. Moreover, heterologous expression

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of genes like EPS, metallothioneins, and phytochelatins can confer heavy metalresistant ability in the engineered cyanobacteria.

8.6

Conclusions and Future Prospects

Recent changes in climatic conditions have posed a considerable risk to global food and nutritional security. It is very important to reorient and change agriculture to make it stronger for environmental changes. Appropriate management and utilization of microbial formulations will help adapt and mitigate climate change. Cyanobacteria are an essential component of the microbial world, with structural similarity to bacteria albeit plant-like photosynthesis ability. Cyanobacteria-based biofertilizers are known to improve soil fertility, texture, porosity, and water-holding capacity of the soil. They also produce several bioactive metabolites, like phytohormones, vitamins, and amino acids, which when released into the soil can help the plant in its growth and development. Cyanobacteria have developed several lines of defense mechanisms to evade various abiotic stresses. Thicker exopolysaccharide covering, presence of nitrogen-fixing ability, carbon sequestration potential, heavy metal remediation, and interaction with other bacteria and fungi often confer them with additional advantages. The choice of cyanobacterial strains often becomes imperative in selecting biofertilizers as they should be able to survive in difficult conditions and act quickly to modify the surroundings. With the help of recent genetic engineering tools, it is easier to introduce the desired trait into the native hosts. Heterologous expression of the desired gene into the target host (cyanobacteria/plant) confers them with additional advantages. Future work on the utilization of cyanobacterial biofertilizers warrants a complete understanding of the mechanisms utilized by them for sustainable crop production. Moreover, with the advent of OMICs technologies, it is easier to develop suitable strains with improved properties. They are mostly underutilized in the current agricultural scenario as compared to their industrial potential but their importance in the field of global food security cannot be overlooked. Acknowledgments Shobit Thapa acknowledges the Director, ICAR-NBAIM for the financial assistance and infrastructural facilities provided under the project titled “Bioprospecting cyanobacterial diversity from the Himalayan region and its potential for bioactive metabolites production.” Competing Interests All the authors declare that they have no competing interests.

References Abbas HH, Ali ME, Ghazal FM, El-Gaml NM (2015) Impact of Cyanobacteria inoculation on rice (Oryza sativa) yield cultivated in saline soil. J Am Sci 11(2):13–19 Ahmed M, Stal MJ, Hasnain S (2010) Association of non-heterocystous cyanobacteria with crop plants. Plant Soil 336:363–375

8

Cyanobacterial Bioinoculants for Abiotic Stress Management in the. . .

195

Ai Y, Yang Y, Qiu B, Gao X (2014) Unique WSPA protein from terrestrial macroscopic cyanobacteria can confer resistance to osmotic stress in transgenic plants. World J Microbiol Biotechnol 30:2361–2369 Aiyer RS, Salahudeen S, Venkataraman GS (1972) Long term algalization field trial with high yielding varieties of rice (Oryza sativa L). Indian J Agric Sci 42:380–383 Apte SK, Bhagwat AA (1989) Salinity-stress-induced proteins in two nitrogen-fixing Anabaena strains differentially tolerant to salt. J Bacteriol 171:909–915 Apte SK, Thomas J (1997) Possible amelioration of coastal soil salinity using halotolerant nitrogenfixing cyanobacteria. Plant Soil 189:205–211 Atsumi S, Higashide W, Liao JC (2009) Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat Biotechnol 27(12):1177–1180 Battisti DS, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323(5911):240–244 Bello AS, Saadaoui I, Ahmed T, Hamdi H, Cherif M, Dalgamouni T, Ben-Hamadou R (2021) Enhancement in bell pepper (Capsicum annuum L) plants with application of Roholtiella sp. (Nostocales) under soilless cultivation. Agronomy 11(8):1624 Borges NA, Ramos NDH, Raven RJ, Sharp, Santos H (2002) Comparative study of the thermostabilizing properties of mannosylglycerate and other compatible solutes on model enzymes. Extremophiles 6:209–216 Bose P, Nagpal US, Venkataraman GS, Goyal SK (1971) Solubilization of tricalcium phosphate by blue green algae. Curr Sci 40:165–166 Bouwman AF, Beusen AHW, Billen G (2009) Human alteration of the global nitrogen and phosphorus soil balances for the period 1970-2050. Global Biogeochem Cycles 23(4):GB0A04 Bremer E, Kramer R (2000) Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solute in bacteria. In: Hengge-Aronis R (ed) Bacterial stress responses. ASM Press, Washington, DC, pp 79–96 Cameron HJ, Julian GR (1988) Utilization of hydroxyapatite by cyanobacteria as their sole source of phosphate and calcium. Plant Soil 109(1):123–124 Castenholz RW (1996) Endemism and biodiversity of thermophilic cyanobacteria. Nova Hedwig Beih 112:33–47 Chakdar H, Thapa S, Srivastava A, Shukla P (2022) Genomic and proteomic insights into the heavy metal bioremediation by cyanobacteria. J Haz Mater 424:127609 Chakraborty S, Verma E, Singh SS (2019) Cyanobacterial siderophores: ecological and biotechnological significance. In: Cyanobacteria. Academic Press, pp 383–397 Chandio AA, Jiang Y, Gessesse AT, Dunya R (2019) The nexus of agricultural credit, farm size and technical efficiency in Sindh Pakistan a stochastic production frontier approach. J Saudi Soc Agric Sci 18(3):348–354 Chaudhary T, Dixit M, Gera R, Shukla AK, Prakash A, Gupta G et al (2020) Techniques for improving formulations of bioinoculants. 3 Biotech 10:199 Chittapun S, Limbipichai S, Amnuaysin N, Boonkerd R, Charoensook M (2018) Effects of using cyanobacteria and fertilizer on growth and yield of rice (Pathum Thani I) a pot experiment. J Appl Phycol 30:79–85 Chua M, Erickson TE, Merritt DJ, Chilton AM, Ooi MKJ, Muñoz-Rojas M (2020) Bio-priming seeds with cyanobacteria: effects on native plant growth and soil properties. Restor Ecol 28: S168–S176 Coba de la Pena T, Redondo FJ, Manrique E, Lucas MM, Pueyo JJ (2010) Nitrogen fixation persists under conditions of salt stress in transgenic Medicago truncatula plants expressing a cyanobacterial flavodoxin. Plant J Biotech 8:954–965 Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants a systems biology perspective. BMC Plant Biol 11:163 Cui L, Liu Y, Yang Y, Ye S, Luo H, Qiu B, Gao X (2018) The drnf1 gene from the drought-adapted cyanobacterium Nostoc flagelliforme improved salt tolerance in transgenic Synechocystis and Arabidopsis plant. Genes 9:441

196

S. Thapa et al.

De Caire GZ, De Cano MS, Zaccaro de Mulé MC, Palma RM, Colombo K (1997) Exopolysaccharide of Nostoc muscorum (Cyanobacteria) in the aggregation of soil particles. J Appl Phycol 9(3):249–253 De Datta SK (1987) Nitrogen transformation processes in relation to improved cultural practices for lowland rice. Plant Soil 100:47–69 De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175 DESA UN (2015) World population prospects: the 2015 revision key findings and advance tables. Working Paper No ESA/P/WP 241 United Nations Department of Economic and Social Affair Population Division, New York Dias MA (2002) Removal of heavy metals by an Aspergillus terreus strain immobilized in polyurethane matrix. Lett Appl Microbiol 34:46–50 El Arroussi H, Elbaouchi A, Benhima R, Bendaou N, Smouni A, Wahby I (2016) Halophilic microalgae Dunaliella salina extracts improve seed germination and seedling growth of (Triticum aestivum L) under salt stress. Acta Hortic 1148:13–26 Enete AA, Amusa TA (2010) Challenges of agricultural adaptation to climate change in Nigeria a synthesis from the literature. Field Act Sci Rep J Field Actions 29(4):243–249 Faisal M, Hameed A, Hasnain S (2005) Chromium-resistant bacteria and cyanobacteria: impact on Cr (VI) reduction potential and plant growth. J Ind Microbiol Biotechnol 32:615–621 Fang X, Lloyd CJ, Palsson BO (2020) Reconstructing organisms in silico: genome-scale models and their emerging applications. Nat Rev Microbiol 18(12):731–743 FAO (2006) Expert Committee on Food Additives meeting and World Health Organization. Safety evaluation of certain contaminants in food, Vol 82. Food Agriculture Org FAOSTAT (2020) FAOSTAT food and agriculture organization of the United Nations - Statistics Division [WWW Document]. URL http://www.fao.org/faostat/en/#data/RFN. Accessed 28 Dec 2020 Gheda SF, Ahmed DA (2015) Improved soil characteristics and wheat germination as influenced by inoculation of Nostoc kihlmani and Anabaena cylindrica. Rend Lincei 26:121–131 Goswami M, Deka S (2020) Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: a review. Pedosphere 30(1):40–61 Gull A, Lone AA, Wani NUI (2019) Biotic and abiotic stresses in plants; abiotic and biotic stress in plants. London, Intech Open, pp 1–19 Gupta V, Ratha SK, Sood A, Chaudhary V, Prasanna R (2013) New insights into the biodiversity and applications of cyanobacteria (blue-green algae) prospects and challenges. Algal Res 2:79– 97 Hader DP, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285 Haggag W, Hoballah M, Ali R (2018) Applications of nano biotechnological microalgae product for improve wheat productivity in semi-arid areas. Int J Agric Technol 14:675–692 Hamim H (2005) Photosynthesis of C3 and C4 species in response to increased CO2 concentration and drought stress. Hayati J Biosci 12(4):131–131 Ibraheem IB (2007) Cyanobacteria as alternative biological conditioners for bioremediation of barren soil. Egyptian J Phycol 8:99–107 Inthorn D (2001) Removal of heavy metal by using microalgae. In: Photosynthetic microorganisms in environmental biotechnology. Springer, Hong Kong, pp 111–169 Itelima JU, Bang WJ, Onyimba IA, Sila MD, Egbere OJ (2018) Bio-fertilizers as key player in enhancing soil fertility and crop productivity: a review. Direct Res J Agric Food Sci 6:73–83 Iwaki T, Haranoh K, Inoue N, Kojima K, Satoh R, Nishino T, Wada S, Ihara H, Tsuyama S, Kobayashi H, Wadano A (2006) Expression of foreign type I ribulose-1, 5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39) stimulates photosynthesis in cyanobacterium Synechococcus PCC7942 cells. Photosynth Res 88(3):287–297 Jaiswal P, Prasanna R, Nayak S, Sood A, Suseela MR (2008) Characterization of rhizo cyanobacteria and their associations with wheat seedlings. Egypt J Biol 10:20–27

8

Cyanobacterial Bioinoculants for Abiotic Stress Management in the. . .

197

Jan Z, Ali S, Sultan T, Ahmad W (2017) The role of cyanobacteria in availability of major plant nutrients and soil organic matter to rice crop under saline soil condition. SJA 33:566–572 Jesus JM, Danko AS, Fiuza A, Borges MT (2015) Phytoremediation of salt-affected soils: a review of processes applicability and the impact of climate change. Environ Sci Pollut Res 22:6511– 6525 Jia XH, Zhang PP, Shi DJ, Mi HL, Zhu JC, Huang XW, He PM (2015) Regulation of pepc gene expression in Anabaena sp. PCC 7120 and its effects on cyclic electron flow around photosystem I and tolerances to environmental stresses. J Integ Plant Biol 57(5):468–476 Jittawuttipoka T, Planchon M, Spalla O, Benzerara K, Guyot F, Cassier-Chauvat C et al (2013) Multidisciplinary evidences that Synechocystis PCC6803 exopolysaccharides operate in cell sedimentation and protection against salt and metal stresses. PLoS One 8(2):e55564 Jochum MD, McWilliams KL, Borrego EJ, Kolomiets MV, Niu G, Pierson EA, Jo YK (2019) Bioprospecting plant growth-promoting rhizobacteria that mitigate drought stress in grasses. Front Microbiol 10:2106 Karthika G, Govintharaj P (2022) Breeding climate-resilience crops for future agriculture. In: Climate change and crop stress. Academic Press, pp 1–32 Karthikeyan N, Prasanna R, Lata, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30 Karthikeyan N, Prasanna R, Sood A, Jaiswal P, Nayak S, Kaushik BD (2009) Physiological characterization and electron microscopic investigations of cyanobacteria associated with wheat rhizosphere. Folia Microbiol 54:43–51 Kaur R, Goyal D (2018) Heavy metal accumulation from coal fly ash by cyanobacterial biofertilizers. Part Sci Technol 36:513–516 Kaushik BD, Subhashini D (1985) Amelioration of salt affected soils with blue green algae: II, Improvement soil properties. Proc Ind Nat Sci Acad B51:386–389 Kumar C, Chatterjee A, Wenjing W, Yadav D, Singh PK (2020) Cyanobacteria: potential and role for environmental remediation. In: Abatement of environmental pollutants. Elsevier, pp 193–202 Li H, Zhao Q, Huang H (2019) Current states and challenges of salt-affected soil remediation by cyanobacteria. Sci Total Environ 669:258–272 Magnuson A (2019) Heterocyst thylakoid bioenergetics. Life 9:13 Malam IO, Defarge C, Le Bissonais Y (2007) Effects of the inoculation of cyanobacteria on the microstructure and the structural stability of a tropical soil. Plant Soil 290:209–219 Manjunath M, Kanchan A, Ranjan K, Venkatachalam S, Prasanna R, Ramakrishnan B, Hossain F, Nain L, Shivay YS, Rai AB, Singh B (2016) Beneficial cyanobacteria and eubacteria synergistically enhance bioavailability of soil nutrients and yield of okra. Heliyon 2(2):e00066 Martins SJ, Rocha GA, de Melo HC, de Castro Georg R, Ulhoa CJ, de Campos Dianese É, Oshiquiri LH, da Cunha MG, da Rocha MR, de Araújo LG, Vaz KS (2018) Plant-associated bacteria mitigate drought stress in soybean. Environ Sci Pollut Res 25(14):13676–13686 Mugnai G, Rossi F, Felde VJMNL, Colesie C, Büdel B, Peth S, Kaplan A, De Philippis R (2018) The potential of the cyanobacterium Leptolyngbya ohadii as inoculum for stabilizing bare sandy substrates. Soil Biol Biochem 127:318–328 Munoz-Rojas M, Chilton A, Liyanage GS, Erickson TE, Merritt DJ, Neilan BA, Ooi MKJ (2018) Effects of indigenous soil cyanobacteria on seed germination and seedling growth of arid species used in restoration. Plant Soil 429:91–100 Murshed M, Dao NTT (2022) Revisiting the CO2- emission induced EKC hypothesis in South Asia: the role of export quality improvement. GeoJournal 87(2):535–563 Murugesan A, Maheswari S, Bagirath G (2008) Biosorption of cadmium by live and immobilized cells of Spirulina platensis. Int J Environ Res 2:307–312 Mutale-Joan C, Rachidi F, Mohamed HA, Mernissi NE, Aasfar A, Barakate M, Mohammed D, Sbabou L, Arroussi HE (2021) Microalgae-cyanobacteria-based biostimulant effect on salinity tolerance mechanisms, nutrient uptake, and tomato plant growth under salt stress. J Appl Phycol 33:3779–3795

198

S. Thapa et al.

Nain L, Rana A, Joshi M, Jadhav SD, Kumar D, Shivay YS, Paul S, Prasanna R (2010) Evaluation of synergistic effects of bacterial and cyanobacterial strains as biofertilizers for wheat. Plant Soil 331(1):217–230 Nayak S, Prasanna R, Pabby A, Dominic TK, Singh PK (2004) Effect of BGA-Azolla biofertilizers on nitrogen fixation and chlorophyll accumulation at different depths in soil cores. Biol Fert Soil 40:67–72 Nayak S, Prasanna R, Prasanna BM, Sahoo DB (2009) Genotypic and phenotypic diversity of Anabaena isolates from diverse rice agro-ecologies of India. J Basic Microbiol 49:165–177 Naz S, Fatima Z, Iqbal P, Khan A, Zakir I, Ullah H, Ahmad S (2022) An introduction to climate change phenomenon. In: Building climate resilience in agriculture. Springer, Cham, pp 3–16 Nisha R, Kiran B, Kaushik A, Kaushik CP (2018) Bioremediation of salt affected soils using cyanobacteria in terms of physical structure, nutrient status and microbial activity. Int J Environ Sci Technol 15:571–580 Nouri H, Borujeni SC, Nirola R, Hassanli A, Beecham S, Alaghmand S, Saint C, Mulcahy D (2017) Application of green remediation on soil salinity treatment a review on halo phytoremediation. Process Saf Environ 107:94–107 Olesen JE, Carter TR, Diaz-Ambrona CH, Fronzek S, Heidmann T, Holt T, Minguez MI, Morales P, Palutikof JP, Quemada M (2007) Uncertainties in projected impacts of climate change on European agriculture and terrestrial ecosystems based on scenarios from regional climate models. Clim Chang 81(1):123–143 Osman MEH, El-Sheekh MM, El-Naggar AH, Gheda SF (2010) Effect of two species of cyanobacteria as biofertilizers on some metabolic activities, growth, and yield of pea plant. Biol Fertil Soils 46:861–875 Pandey KD, Shukla PN, Giri DD, Kashyap AK (2005) Cyanobacteria in alkaline soil and the effect of cyanobacteria inoculation with pyrite amendments on their reclamation. Biol Fertil Soils 41(6):451–457 Pandhal J, Ow SY, Wright PC, Biggs CA (2009) Comparative proteomics study of salt tolerance between a nonsequenced extremely halotolerant cyanobacterium and its relative using in vivo metabolic labelling and in vitro isobaric labelling. J Proteome Res 8:818–828 Poveda J (2020) Cyanobacteria in plant health: biological strategy against abiotic and biotic stresses. Crop Prot 141:105450 Prasanna R, Jaiswal P, Nayak S, Sood A, Kaushik BD (2009) Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian J Microbiol 49:89–97 Prasanna R, Joshi M, Rana A, Shivay YS, Nain L (2012) Influence of co-inoculation of bacteria cyanobacteria on crop yield and C-N sequestration in soil under rice crop. World J Microbiol Biotechnol 28:1223–1235 Prasanna R, Chaudhary V, Gupta V, Babu S, Kumar A, Singh R, Shivay YS, Nain L (2013) Cyanobacteria mediated plant growth promotion and bioprotection against Fusarium wilt in tomato. Eur J Plant Pathol 136:337–353 Prasanna R, Bidyarani N, Babu S, Hossain F, Shivay YS, Nain L (2015) Cyanobacterial inoculation elicits plant defense response and enhanced Zn mobilization in maize hybrids. Cogent Food Agric 1:998507 Rana A, Joshi M, Prasanna R, Singh Shivay Y, Nain L (2012) Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur J Soil Biol 50:118– 126 Rangsayatorn N, Upatham E, Kruatrachue M, Pokethitiyook P, Lanza G (2002) Phytoremediation potential of spirulina (Arthrospira) platensis: biosorption and toxicity studies of cadmium. Environ Pollut 119:45–53 Rezayian M, Niknam V, Ebrahimzadeh H (2019) Stress response in cyanobacteria. Iran J Plant Physiol 9(3):2773–2787 Rodríguez AA, Stella AM, Storni MM, Zulpa G, Zaccaro MC (2006) Effects of cyanobacterial extracellular products and gibberellic acid on salinity tolerance in (Oryza sativa L.) Saline. System 2:7

8

Cyanobacterial Bioinoculants for Abiotic Stress Management in the. . .

199

Roychoudhury P, Kaushik BD (1989) Solubilization of Mussorie rock phosphate by cyanobacteria. Curr Sci 58(10):569–570 Saijo Y, Loo EPI (2020) Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol 225:87–104 Seifikalhor M, Hassani SB, Aliniaeifard S (2019) Seed priming by cyanobacteria (Spirulina platensis) and salep gum enhances tolerance of maize plant against cadmium toxicity. J Plant Growth Regul 39:1009–1021 Sharma NK, Tiwari SP, Tripathi K, Rai AK (2011) Sustainability and cyanobacteria (blue-green algae): facts and challenges. J Appl Phycol 23:1059–1081 Shih PM, Zarzycki J, Niyogi KK, Kerfeld CA (2014) Introduction of a synthetic CO2- fixing photorespiratory bypass into a cyanobacterium. J Biol Chem Integ Plant Biol 57(5):468–476 Singh S (2014) A review on possible elicitor molecules of cyanobacteria: their role in improving plant growth and providing tolerance against biotic or abiotic stress. J Appl Microbiol 117: 1221–1244 Singh NK, Dhar DW (2010) Cyanobacterial reclamation of salt-affected soil. In: Lichtfouse E (ed) Genetic engineering, Biofertilisation, soil quality and organic farming. Springer, Dordrecht, pp 243–275 Sneha GR, Yadav RK, Chatrath A, Gerard M, Tripathi K, Govindsamy V, Abraham G (2021) Perspectives on the potential application of cyanobacteria in the alleviation of drought and salinity stress in crop plants. J Appl Phycol 33:3761–3778 Takabe T, Uchida A, Shinagawa F, Terada Y, Kajita H, Tanaka Y et al (2008) Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances growth rate as well as abiotic stress tolerance of poplar plants. Plant Growth Regul 56:265–273 Tijen D, Ismail T (2006) Exogenous glycinebetaine affects growth and proline accumulation and retards senescence in two rice cultivars under NaCl stress. Environ Exper Bot 56:72–79 Tiwari ON, Bhunia B, Mondal A, Gopikrishna K, Indrama T (2019) System metabolic engineering of exopolysaccharide-producing cyanobacteria in soil rehabilitation by inducing the formation of biological soil crusts: a review. J Clean Product 211:70–82 Tognetti VB, Palatnik JF, Fillat MF, Melzer M, Hajirezaei MR, Valle EM, Carrillo N (2006) Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broadrange stress tolerance. Plant Cell 18:2035–2050 Usharani K, Naik D (2019) Cyanobacteria: role in agriculture. A review. Trends Biosci 12:15–26 Verma R, Kumar R, Nath A (2018) Drought resistance mechanism and adaptation to water stress in sorghum [Sorghum bicolor (L.) Moench]. Int J Bio-Resour Stress Manag 9:167–172 Verma S, Thapa S, Siddiqui N, Chakdar H (2022) Cyanobacterial secondary metabolites towards improved commercial significance through multi omics approaches. World J Microbiol Biotechnol 38(6):1–22 Whitney SM, Houtz RL, Alonso H (2011) Advancing our understanding and capacity to engineer nature’s CO 2-sequestering enzyme Rubisco. Plant Physiol 155(1):27–35 Xu J, Tian YS, Peng RH, Xiong AS, Zhu B, Hou XL, Yao QH (2010) Cyanobacteria MT gene SmtA enhance zinc tolerance in Arabidopsis. Mol Biol Rep 37:1105 Yan F, Quan L, Wei Z, Cong W (2015) Regulating phosphoenolpyruvate carboxylase activity by copper-induced expression method and exploring its role of carbon flux distribution in Synechocystis PCC 6803. J Appl Phycol 27(1):179–185 Yoshimura H, Okamoto S, Tsumuraya Y, Ohmori M (2007) Group 3 sigma factor gene, sigJ, a key regulator of desiccation tolerance, regulates the synthesis of extracellular polysaccharide in cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 14(1):13–24

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Alleviation of Drought Stress and Amelioration of Tomato Plant Growth by Bacterial Inoculants for Mitigating Climate Change K. Tamreihao, Rakhi Khunjamayum, H. Shingmuan, Wahengbam Pusparani Chanu, Pintubala Kshetri, Thangjam Surchandra Singh, Ngangkham Umakanta, A. Thirugnanavel, Susheel Kumar Sharma, and Subhra Saikat Roy

Abstract

Tomato (Solanum lycopersicum) is an important horticultural crop cultivated worldwide. The production and consumption of tomatoes are still increasing because of their high nutritional content and anti-oxidative qualities. However, a variety of abiotic factors, including heat, salt, and drought, have a significant negative impact on the growth resulting in yield loss. Tomato is drought sensitive plant and affects throughout their life cycle exerting negative effects on both

K. Tamreihao Department of Botany, St. Joseph College, Ukhrul, Manipur, India ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India R. Khunjamayum · H. Shingmuan · W. P. Chanu Department of Biochemistry, Microbial Biotechnology Research Laboratory (MBRL), Manipur University, Canchipur, India P. Kshetri · T. S. Singh · N. Umakanta (✉) ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India A. Thirugnanavel ICAR-Central Citrus Research Institute, Nagpur, Maharashtra, India S. K. Sharma ICAR-Indian Agricultural Research Institute, New Delhi, India S. S. Roy ICAR-NEH Quality Analysis Laboratory, ICAR Research Complex for NEH Region, Manipur Centre, Imphal, India ICAR-Central Citrus Research Institute, Nagpur, Maharashtra, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_9

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morphology and biochemistry. However, many wild tomato varieties have genes that could tolerate drought stress. For sustainable production under adverse environmental conditions especially drought, water-stress tolerant bacterial inoculants can be a good candidate as they have a great potential to confer the stress resistance and ameliorate the growth and development. Drought stresstolerant bacteria aid in the growth of tomatoes through the production of phytohormones, ACC deaminase, solubilization of minerals, induction of systemic resistance, increasing the antioxidant activity and osmolytes level in plant cells. The present chapter focused on the response and detrimental effects of drought stress in tomato plants. It will also deal with the functions of bacterial inoculants in conferring tolerance to water stress and positive effect on the growth of tomato plant under drought for mitigating climate change. Keywords

Tomato · Drought · Bacterial inoculants · Phytohormones · Mineral solubilization · Antioxidant · Osmolytes · Systemic resistance

9.1

Introduction

Tomato (Solanum lycopersicum) is an important horticultural crop sensitive to drought stress. It is a warm-season crop and can survive various types of soil including clay, black soil, and red soil (Krishna et al. 2022; Motamedzadegan and Tabarestani 2018). The crop is rich in health-beneficial phytochemicals such as carotenoids, lycopene, vitamin C, flavonoids, and phenolics. Lycopene is responsible for the red color of the matured fruit. Hence, they represent an excellent source of natural antioxidants. China is the world’s largest tomato producer, generating 64.768 million mT from 1,107,485 hectares of cultivation, which is about 34.67% of global production, with a yield of 58.5 mT/ha per square meter. India is the second largest producer of tomatoes in 2020, producing 20.573 million mT of tomatoes on 812,000 hectares with an average output of 25.3 mT/ha (FAOSTAT 2020). Because of its importance as a food and nutritional source, researchers have been working to produce a better variety of tomatoes (having higher fruit quality and productivity; resistant to biotic and abiotic stress) through classical and modern breeding techniques (Horneburg and Myers 2012; Kimura and Sinha 2008). Besides its significance as economically and nutritionally, the tomato plant also serves as an excellent plant model for research. Some of the features which made a tomato an ideal plant model include fleshy fruits, compound leaves, sympodial shoots, short life cycles, small genome size, etc. (Kimura and Sinha 2008; Krishna et al. 2022). The productivity of horticultural crops is influenced by many factors such as lack of scientific knowledge in farming, climatic conditions, low soil quality, and biotic and abiotic stress. Abiotic and biotic stressors are one of the causes of undernourishment and hunger because they lower agricultural production, which creates a condition of food insecurity (Kogan et al. 2019). Drought, salinity, extremely high

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and extremely low temperatures, and intense light are important abiotic stresses that hinder agricultural productivity (Salehi-Lisar and Bakhshayeshan-Agdam 2016). Abiotic stressors, especially drought, have a negative impact on agricultural productivity because they lower the yields of crucial crops like tomatoes. Nearly 1 billion people worldwide go hungry every year, and about 25% of people lack access to enough food for basic survival because of an increase in food insecurities, especially in underdeveloped countries of Asian and African continents. Each year, drought has a bigger impact on agricultural productivity than all diseases put together (Gupta et al. 2020). Drought stress is one of the major abiotic factors that contribute to the dehydration of plant cells and tissues. It is expected to worsen in the coming decades particularly in arid and semi-arid regions significantly retarding the productivity to feed the world’s population. Among the abiotic stressors, drought stress is recognized as the most destructive abiotic stress (Francesca et al. 2021). It necessitates the plant to undergo a multitude of morpho-anatomical, physiological, and biochemical modifications to decrease water loss and boost water usage efficiency, which eventually results in low quality and quantity of crop yield (Kapoor et al. 2020). Nevertheless, bacterial inoculants that are tolerant to water stress have the potential to directly or indirectly aid in the growth by alleviating the stress through various mechanisms and rescuing the tomato plants from the negative effects imposed by drought. The potent stress-tolerant bacterial inoculants can be used for application as growth promoter and abiotic stress mitigator for sustainable production of drought-sensitive important horticultural crops especially tomatoes.

9.2

Deleterious Effect of Drought on Tomato Plant

Abiotic stressors, especially drought, are regarded as the most destructive stress limiting the growth and 70% loss in productivity of tomatoes (Krishna et al. 2022). The whole life cycle of tomatoes starting from seed germination, seedlings growth, development, and yield is affected by drought. The impact of drought stress on tomato plant growth metrics is shown in Fig. 9.1.

9.2.1

Seed Germination and Growth

As reported by Bhatt and Srinivasa (1987), tomato seedlings under water deficit stress exhibit a steady drop in seed germination as water potential falls. The early phase of radicle growth is affected by water potential, suggesting that the watersensitive phase for tomato germination takes place before the formation of its radicle. According to a different study, the non-germinated seeds under osmotic stress conditions could be fully recovered if transferred to a stress-free environment which enables them to fully germinate (Esan et al. 2018). Drought inhibits the growth of plants by reducing the photosynthetic and respiration process (Chaves et al. 2009). Under drought stress, the level of ethylene

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Fig. 9.1 Detrimental effects of drought stress on tomato plant

increases inhibiting the root growth and development. It also triggers the generation of reactive oxygen species (ROS) that causes oxidative damage to nucleic acid, proteins, and lipids. Prolonged imposition of drought induces lipid peroxidation impacting the membrane function leading to apoptosis and even death (Kumar and Verma 2018). Imposition of drought reduced the chlorophyll content, photosynthesis reaction, stomatal activity, and soluble protein of tomato plant (Pervez et al. 2009; Sivakumar and Srividhya 2016; Zhou et al. 2017; Liang et al. 2020). Evaluation of negative effects of drought and heat stress on tomatoes using three cultivars revealed that drought has more detrimental effects on growth and development (Zhou et al. 2017). Investigation on the various growth morphology showed characteristics of wilting, decrease in the number of leaves, and stunted growth in tomato plants imposed with drought (Tamreihao et al. 2022).

9.2.2

Yield and Fruit

Drought stress during the flowering, fruit development phase, and fruit ripening phase significantly reduces the production of tomatoes (Chen et al. 2013). The water stress has been reported to accelerate the flower abscission (Sivakumar and Srividhya 2016). It reduces the number of fruits and seeds, weight of fruits, and seeds quality. Seeds collected from water stress-tolerant plants significantly exhibit a lower vigor index (Pervez et al. 2009; Salinas-Vargas et al. 2021). However, fruit quality such as total soluble solids, soluble sugar, organic acids, fruit firmness, and vitamin C increased in response to a limited water supply. The lycopene content was

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also enhanced in a water stress fruits (Lu et al. 2019; Cui et al. 2020; Tamreihao et al. 2022).

9.3

Induction of Stress Response Genes to Endure Drought Stress

In plants, numerous genes relevant to metabolic and physiological pathways are activated in stressful conditions, particularly drought stress. Induction of various genes occurs to endure the drought which includes erd15, asr2, mkp1, tas14, tsw12, and cip1. These stress-induced genes regulate the synthesis of amino acids (proline) and plant hormones (ethylene and abscisic acid), aggregation of distinct types of protein (LEA and HSPs), and osmolytes (Cushma and Bohnert 2000). These genes further induce the downstream genes and activate transcription factors (TFs). The activated genes are involved in the synthesis of enzymes neutralizing the ROS. Gene expression is altered during drought stress thereby producing new proteins, especially LEA protein that play an important role in retaining water in tissue due to their hydrophilic nature (Jangid and Dwivedi 2016). Exposure of tomato plants to water stress induces the increase in the level of abscisic acid (ABA) and this in turn up-regulates the expression of stress-response genes (Krishna et al. 2022). Water and salt stress imposition in tomatoes enhances the expression of ABA-responsive element binding protein (SIAREB). SIAREB have been reported to maintain PSII and cell membrane integrities and regulate the water levels of the plant. Expression of these genes downregulates the stress-related response genes such as AtRD29A, AtCOR47, and SIC17 (Hsieh et al. 2010). Drought stress induced the upregulation of leucine zipper transcription factor (SIAREB). Further investigation of this TF expression in transforming tomato and tobacco using Agrobacterium reveals the upregulation of stress-responsive genes in the leaves (Yáñez et al. 2009). Induction of SIAREB (SIAREB1 and SIAREB2) by drought and salt stress in tomatoes has also been reported by Orellana et al. (2010). They also reported that the expression is mostly seen in leaves and roots induced by ABA. Similarly, upregulation of SIAREB in drought-imposed Arabidopsis has been reported. The genes are also activated by ABA (Uno et al. 2000). ABA also signals the increase in the level of trehalose and this compound increases the tolerance of tomatoes to drought (Maclntyre et al. 2022). An increase in the levels of ABA also enhanced the expression of dehydration element-binding protein (DREB) (Islam and Wang 2009). DREB is reported to be mainly expressed in leaf and stem and regulates the moisture stress in tomato plants by inhibiting the leaf growth and elongation of internodes resulting in stunted growth. However, the growth can be recovered by application of gibberellic acid (Li et al. 2012). However, investigation on induction of drought response genes in moisture tolerant wild type tomato cultivar S. pennellii showed that ROS-neutralizing enzymes like quinone reductase and ascorbate peroxidase were upregulated and the production of ABA was downregulated. Gene responsive to dehydration 19A was upregulated. Moisture stress increases the amino acid metabolism which was

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shown by the increase in the activity of enzymes for assimilation of nitrogen. Jasmonic acid (JA) and ethylene (ET) synthesis genes were up-regulated (Egea et al. 2018).

9.4

Role of Bacterial Inoculants in Mitigation of Drought Stress in Tomato

Crop plants have experienced a number of biotic and abiotic challenges as a result of global climate change posing a great challenge in the sustainable production of horticultural crops. Loss of arable land, a decline in soil fertility, and negative effects of synthetic agrochemicals will all contribute to this. Extreme situations require a variety of adaptations and mitigations in order to survive. Drought stress has major negative effects on plant growth and yield globally impacting on crop production affecting economic aspects directly and indirectly (Gowtham et al. 2020). To augment production in order to feed the world’s growing population has put a significant strain on our agroecosystems, escalating the environmental stresses. The use of agrochemicals has made it possible to increase agricultural output. However, the environment and human health are seriously affected by the widespread use of agrochemicals. To deal with the consequences of drought, a number of technologies have been devised, including genetic engineering and traditional breeding. However, the process of developing crop varieties that can withstand stress through genetic engineering and plant breeding is time-consuming and expensive (Chaudhary et al. 2019). A viable alternative to enhance the crop production under environmental stresses particularly drought is to include the use of bacterial inoculants that can resist the stress, and aid the growth and yield of important crops that are consumed worldwide especially water-stress-sensitive tomatoes. Drought-tolerant bacterial inoculants have been reported to promote the tomato growth under water stress conditions by the production of phytohormones, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, solubilization of soil minerals, antioxidant defenses, osmotic adjustment by accumulation of compatible solutes, induction of systemic resistance, etc. The tomato plant growth by the beneficial bacterial inoculants under water stress is illustrated in Fig. 9.2.

9.4.1

Secretion of Phytohormones

Most important mechanisms deployed by plant-associated microbes for growth promotion under drought stress include the production of phytohormones. Most microbes maintain the hormonal balance through phytohormone production viz. gibberellins and indole-3-acetic acid (IAA), and resistance pathways, which in turn defend the plant from various stresses (Cassán et al. 2001; Dreischhoff et al. 2020). Phytohormones produced by the bacterial inoculants promote seed

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Fig. 9.2 Alleviation of drought stress and growth promotion of tomato plants by bacterial inoculants under drought stress

germination, root developments, apical growth cell division, and differentiation helping in the overall growth of plants. Phytohormones-producing bacteria are reported to augment the tomato plant growth under drought stress. Moisture stress-tolerant Microbacterium oxydans producing IAA and gibberellic acid aid the growth of tomatoes imposed with drought under pot conditions (Siraj et al. 2022). Haque et al. (2020) inoculated the tomato plants with IAA-producing Pseudomonas spp., Bacillus aryabhattai and evaluated the growth potential under drought stress in pot experiments. The bioinoculants treated plants exhibited higher height, primary branches, leaves, and dry matter over the untreated plants. Priming of tomato seedlings with IAA-producing bacterial inoculants Pseudomonas fluorescens, Bacillus aryabhattai, Bacillus subtilis, and Pseudomonas moraviensis increase the root growth and developments under in vitro conditions (Cochard et al. 2022). Endophytic and rhizospheric bacteria isolated from tomato roots belonging to Bacillus sp., Pseudomonas sp., Agrobacterium sp., and Rhizobium sp. increase the root hair formation in Arabidopsis seedling (Abbamondi et al. 2016).

9.4.2

Mineral Solubilization

Most of the mineral nutrients present in the soil are in insoluble form leading to deficiency and stunting the growth of plants. Also the majority of the applied mineral fertilizers are quickly immobilized in soil and are unavailable to plants. Excessive application for plant growth creates environmental problems by contaminating the groundwater causing eutrophication. Nevertheless, bacteria can solubilize the minerals and make them available for plant uptake through the production of organic acids and enzymes (Alori et al. 2017). Soil minerals are not only required for plant

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growth but it also plays an important role in the mitigation of water stress by regulating the stomatal function, antioxidant defence pathway (Hasanuzzaman et al. 2018; Hassan et al. 2020). Root treatment of tomato seedlings of phosphate (P), potassium (K), and zinc (Zn) solubilizing moisture-tolerant bacterial inoculants belonging to Bacillus sp., Burkholderia sp., and Streptomyces sp. alleviate the drought stress and promote the growth in pot experiments. The bioinoculants also increase the antioxidant enzyme activity such as catalase, glutathione reductase, and ascorbate peroxidase of tomato leaves. Further evaluation of nutrient uptake by the plants such as nitrogen, P, and K showed considerable increase in the accumulation in the treated plants when compared with the untreated control plants (Tamreihao et al. 2022). Similarly, treatments of drought-tolerant rhizobacteria bioinoculant Microbacterium oxydans solubilizing P promote the growth of tomatoes grown under water stress (Siraj et al. 2022). K solubilizing bacterial isolates Bacillus licheniformis and Bacillus cenocepacia enhance the root and shoot growth of tomato plants under greenhouse conditions. Investigation on the content of K in the post-harvest soils showed a higher deposition of minerals in the bioinoculant-treated soils. The deposited mineral has the potential to help in the growth promotion of subsequent plants (Raji and Thangavelu 2021). Enterobacter hormaechei isolated from the saline water could solubilize K and calcium (Ca). Treatment of this salt-tolerant bioinoculant alleviates the salt stress and augments the tomato growth and yield grown in saline soils. The untreated plants showed Ca deficiency symptoms whereas none of the bioinoculant-treated tomato fruit exhibited the symptoms (Ranawat et al. 2021).

9.4.3

ACC Deaminase Production

Plants generate ethylene in a stressful environment and increased ethylene levels affect the growth and development of the plant causing chlorosis, leaf abscission, etc. Plant-beneficial bacteria producing ACC deaminase can cleave ACC the immediate precursor of ethylene lowering the ethylene level, thereby protecting the plants from the harmful impact (Abdelaal et al. 2021; Glick 2014). ACC deaminase-producing bacterial strain Bacillus subtilis significantly enhances the germination of seedlings growth of tomato. Tomato seeds treated with the bioinoculants and grown in water-stress soils showed significant growth. Further study on the plants ethylene revealed higher content in the untreated plants; however, considerable decrease in the levels was determined in the treated plants. The bioinoculant-treated plants also showed higher antioxidant activity. The authors conclude that the drought stress-tolerant isolate protects the plants from the oxidative damage and promotes the growth of plants under water stress by degrading the stress-ethylene (Gowtham et al. 2020). Achromobacter piechaudii isolated from the arid soils could degrade ACC. The isolate could aid the tomato and pepper seedlings growth exposed to short water stress. The beneficial bioinoculant also considerably reduced the production of ethylene in tomato seedlings. Exposure to water stress does not exhibit a reduction in the relative water content when compared with the

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untreated control plants (Mayak et al. 2004). Similarly, Pseudomonas spp., Bacillus aryabhattai positive for ACC deaminase promote the tomato growth under water stress (Haque et al. 2020). Inoculations of salt-tolerant Pseudomonas spp. positive for ACC deaminase have been reported to alleviate the stress and ameliorate the tomato plant growth grown in saline soils (Orozco-Mosqueda et al. 2019; Pandey and Gupta 2020).

9.4.4

Antioxidant Defence and Stress-Related Osmolytes

Drought stress generates ROS and other stress-related compounds that enhance the oxidative damage cell components leading to cell apoptosis and even death. However, stress tolerance can be improved with the production of antioxidant enzymes that neutralize the ROS or reactive compounds and osmolytes that regulate the osmotic potential of cells (Jalili et al. 2009). The antioxidant defense enzymes include glutathione reductase, ascorbate peroxidase, superoxide dismutase, catalase, etc. The osmolytes components include proline, total sugars, amino acids, and vitamin C. The antioxidants activity and osmotic compatible solutes induced by bacterial inoculants in tomato plants alleviating the drought stress are shown in Table 9.1.

Table 9.1 Alleviation of drought stress in tomato plants by bacterial inoculants antioxidant machinery and osmolytes

Bacterial inoculant(s) Bacillus sp.

Bacillus amyloliquefaciens Pseudomonas chlororaphis Pseudomonas sp.

Bacillus sp. Pseudomonas spp. Streptomyces sp. Bacillus sp. Burkholderia sp., Streptomyces sp.

Antioxidant enzymes Superoxide dismutase, catalase, glutathione reductase

Elevation of osmolytes component

Proline Superoxide dismutase, catalase

Proline and total sugar Trehalose

Catalase

Proline

Ascorbate peroxidase, Guaiacol peroxidase Catalase, ascorbate peroxidase, glutathione reductase

Proline

Reference Bindu et al. (2018) Bindu et al. (2018) Brilli et al. (2019) OrozcoMosqueda et al. (2019) Haque et al. (2020) Abbasi et al. (2020) Tamreihao et al. (2022)

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Induced Systemic Tolerance (IST)

Plants have the ability to defend themselves from a variety of biotic and abiotic stress situations by interacting with microbes as part of a defense response. The interaction can take place by production of signaling molecules, exopolysaccharide (EPS), and/or biofilm formation by the bacteria. It activates plant immune mechanisms inducing systemic resistance resulting in increased tolerance to various stresses. Biofilm-forming rhizobacterial isolates Pseudomonas spp., Bacillus aryabhattai augment the growth of tomato plants exposed to water stress under pot conditions. The treated plants showed higher antioxidant activity (Haque et al. 2020). Colonization of tomato roots by Bacillus subtilis increased the salicylic and/or jasmonic acid signaling pathway. The signaling pathway ISR to tomato plants (Samaras et al. 2021). The signaling hormones such as salicylic acid (SA) and jasmonic acid and molecules sphingosine and psychosine produced by Bacillus and Pseudomonas sp. induced systemic tolerance to drought in Sorghum (Carlson et al. 2020). EPS produced by bacterial inoculants Bacillus subtilis and Azospirillum brasilense augment the ABA levels and promote the growth of wheat under drought stress by alleviating the stress through induction of systemic resistance (Ilyas et al. 2020). EPS protects the plant against abiotic stresses and promotes the growth by enhancing the availability of nutrients in the rhizosphere (Goswami and Deka 2020).

9.4.6

Volatile Compounds Production

Microbial volatile compounds (VOC) have the ability to reduce abiotic stress especially drought and salinity. 2,3-butanediol produced by rhizobacteria have been reported to alleviate drought stress conditions through nitric oxide synthesis. Some examples of bacterial VOCs that assist in enhancing tolerance to drought stress include geranyl, benzaldehyde, b-pinene (Liu and Zhang 2015; Cho et al. 2013), acetoin, 2-pentylfuran (Zou et al. 2010), 2-butanone, 2-methyl-n-1-tridecene, and 13-tetradecadien-1-ol (Park et al. 2015).

9.5

Transgenic Approach for Alleviation of Drought Stress

Genetic engineering and cultural practices are seen as essential tools for managing abiotic stress and mitigating its effects. Classical breeding has reportedly improved agronomic features in tomato cultivars, but it has fallen short when it comes to drought resistance. With the ever-increasing environmental stresses, crop production has become a serious threat Worldwide. Abiotic stress, especially drought stress has led to change in plants growth and development including their metabolism (Mishra et al. 2012; Wahid et al. 2007). Therefore, in order to improve various environmental stress tolerances, genetic modification (GM technology) has become significant practice. Several researchers have reported GM technology as a more efficient and faster approach to enhance stress tolerance including drought stress, leading to

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higher yield (Vincour and Altman 2005; Gerszberg and Hnatuszko-Konka 2017, Barriuso et al. 2008). Vannini et al. (2007) reported that overexpression of Osmyb4 gene in transgenic tomato coding with the MYB TF exhibited drought stress tolerance and also resistance to Tomato Mosaic Virus (ToMV).

9.6

Conclusions

As tomatoes are very sensitive to drought, it has become a great challenge for sustainable production to feed the world’s population. Water stress significantly affected the whole life cycle of tomatoes inhibiting the growth, development, and yield production. However, bacteria that are tolerant to water stress have the potential to directly or indirectly aid in the growth by alleviating the stress through various mechanisms such as production of phytohormones and ACC deaminase, solubilization of minerals, and induction of systemic resistance, increasing the antioxidant defenses and levels of osmotic compatible solutes. These plantbeneficial properties of bacterial inoculants have the great potential in rescuing the tomato plants from the negative effects imposed by drought. The potent stresstolerant bacterial inoculants can be used for application as growth promoters and abiotic stress mitigator for sustainable production of drought-sensitive important horticultural crops especially tomato. Another feasible approach for the development of drought tolerance cultivars is through genetic approach whereby a transgenic cultivar can overexpress stress-related genes for induction of tolerance against drought or other important environmental stressors.

References Abbamondi GR, Tommonaro G, Weyens N, Thijs S, Sillen W, Gkorezis P, Iodice C, de Rangel WM, Nocolaus B (2016) Plant growth-promoting effects of rhizospheric and endophytic bacteria associated with different tomato cultivars and new tomato hybrids. Chem Biol Technol Agric 3:1 Abbasi S, Sadeghi A, Safaie N (2020) Streptomyces alleviate drought stress in tomato plants and modulate the expression of transcription factors ERF1 and WRKY70. Sci Hortic 265:109206. https://doi.org/10.1016/j.scienta.2020.109206 Abdelaal K, AlKahtani M, Attia K, Hafez Y, Király L, Künstler A (2021) The role of plant growthpromoting bacteria in alleviating the adverse effects of drought on plants. Biology 10(6):520. https://doi.org/10.3390/biology10060520 Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorous solubilization and its potential for use in sustainable agriculture. Fron Microbiol 8:971 Barriuso J, Solano BR, Fray RG, Cámara M, Hartmann A, Gutierrez Manero FJ (2008) Transgenic tomato plants alter quorum sensing in plant growth- promoting rhizobacteria. Plant Biotech J 6: 442–452 Bhatt RM, Srinivasa Rao NK (1987) Seed germination and seedling growth responses of tomato cultivars to imposed water stress. J Hortic Sci 62(2):221–225 Bindu GH, Selvakumar G, Shivashankara KS, Kumar NS (2018) Osmotolerant plant growth promoting bacterial inoculation enhances the antioxidant enzyme levels of tomato plants under water stress conditions. Int J Curr Microbiol App Sci 7:2824–2833

212

K. Tamreihao et al.

Brilli F, Pollastri S, Raio A, Baraldi R, Neri L, Bartolini P, Podda A, Loreto F, Maserti BE, Balestrini R (2019) Root colonization by pseudomonas chlororaphis primes tomato (Lycopersicum esculentum) plants for enhanced tolerance to water stress. J Plant Physiol 232: 82–93 Carlson R, Tugizimana F, Steenkamp PA, Dubery IA, Hassen AI, Labuschagne N (2020) Rhizobacteria-induced systemic tolerance against drought stress in Sorghum bicolor (L.) Moench. Microbiol Res 232:126388 Cassán F, Bottini R, Schneider G, Piccoli P (2001) Azospirillum brasilense and Azospirillum lipoferum hydrolyze conjugates of GA20 and metabolize the resultant aglycones to GA1 in seedlings of rice dwarf mutants. Plant Physiol 125:2053–2058 Chaudhary J, Alisha A, Bhatt V, Chandanshive S, Kumar N, Mir Z, Kumar A, Yadav SK, Shivaraj SM, Sonah H, Deshmukh R (2019) Mutation breeding in tomato: advances, applicability and challenges. Plants 8:128. https://doi.org/10.3390/plants8050128 Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103(4):551–560 Chen J, Kang S, Du T, Qiu R, Guo P, Chen R (2013) Quantitative response of greenhouse tomato yield and quality to water deficit at different growth stages. Agric Water Manag 129:152–162 Cho S-M, Kim YH, Anderson AJ, Kim YC (2013) Nitric oxide and hydrogen peroxide production are involved in systemic drought tolerance induced by 2R, 3R-butanediol in Arabidopsis thaliana. Plant Pathol J 29:427 Cochard B, Giroud B, Crovadore J, Chablais R, Arminjon L, Lefort F (2022) Endophytic PGPR from tomato roots: isolation, in vitro characterization and in vivo evaluation of treated tomatoes (Solanum lycopersicum L.). Microorganisms 10:765 Cui J, Shao G, Lu J, Keabetswe L, Hoogenboom G (2020) Yield quality and drought sensitivity of tomato to water deficit during different growth stages. Sci Agric 77(2). https://doi.org/10.1590/ 1678-992x-2018-0390 Cushma JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3(2):117–124 Dreischhoff S, Das IS, Jakobi M, Kasper K, Polle A (2020) Local responses and systemic induced resistance mediated by ectomycorrhizal fungi. Front Plant Sci 11:590063 Egea I, Albaladejo I, Meco V, Morales B, Sevilla A, Bolarin MC, Flores FB (2018) The droughttolerant solanum penellii regulates leaf water loss and induces genes involved in amino acid and ethylene/jasmonate metabolism under dehydration. Sci Rep 8:2791 Esan VI, Ayanbamiji TA, Adeyemo JO, Oluwafemi S (2018) Effect of drought on seed germination and early seedling of tomato genotypes using polyethylene glycol 6000. Int J Sci 2:36–43 FAOSTAT (2020). https://www.fao.org/faostat/en/#data/QCL/visualize Francesca S, Cirillo V, Raimondi G, Maggio A, Barone A, Rigano MM (2021) A novel protein hydrolysate-based biostimulant improves tomato performances under drought stress. Plan Theory 10(4):783 Gerszberg A, Hnatuszko-Konka K (2017) Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul 83:175–198 Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39 Goswami M, Deka S (2020) Plant growth-promoting rhizobacteria-alleviators of abiotic stresses in soil: a review. Pedosphere 30:40–61 Gowtham HG, Brijesh Singh S, Murali M, Shilpa N, Prasad M, Aiyaz M, Amruthesh KN, Niranjana SR (2020) Induction of drought tolerance in tomato upon the application of ACC deaminase producing plant growth promoting rhizobacterium Bacillus subtilis Rhizo SF 48. Microbiol Res 234. https://doi.org/10.1016/j.micres.2020.126422 Gupta A, Rico-Medina A, Caño-Delgado AI (2020) The physiology of plant responses to drought. Science 368(6488):266–269 Haque MM, Mosharaf MK, Khatun M, Haque MA, Biswas MS, Islam MS, Islam MM, Shozib HB, Miah MM, Molla AH, Siddiquee MA (2020) Biofilm producing rhizobacteria with multiple

9

Alleviation of Drought Stress and Amelioration of Tomato Plant Growth. . .

213

plant growth-promoting traits promote growth of tomato under water-deficit stress. Front Microbiol 11:542053 Hasanuzzaman M, Bhuyan MHMB, Nahar K, Hossain MS, Mahmud JA, Hossen MS, Masud AAC, Moumita FM (2018) Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8:31 Hassan MU, Aamer M, Chattha MU, Haiying T, Shahzad B, Barbanti L, Nawaz M, Rasheed A, Afzal A, Liu Y, Guoqin H (2020) The critical role of zinc in plants facing the drought stress. Agriculture 10:0396 Horneburg B, Myers JR (2012) Tomato: breeding for improved disease resistance in fresh market and home garden varieties. In: Lammerts van Bueren ET, Myers JR (eds) Organic crop breeding, pp 239–249. https://doi.org/10.1002/9781119945932.ch15 Hsieh T-S, Li C-W, Su R-C, Cheng C-P, Sanjaya TY-C, Chan M-T (2010) A tomato bZIP transcription factor, SIAREB, is involved in water deficit and salt stress response. Planta 231: 1459–1473 Ilyas N, Mumtaz K, Akhtar N, Yasmin H, Sayyed RZ, Khan W, El Enshasy HA, Dailin DJ, Elsayed EA, Ali Z (2020) Exoploysaccharide producing bacteria for the amelioration of drought stress in wheat. Sustainability 12:8876 Islam MS, Wang M-H (2009) Expression of dehydration responsive element-binding protein-3 (DREB3) under different abiotic stresses in tomato. BMB Rep 42:611–616 Jalili F, Khavazi K, Pazira E, Nejati A, Rahmani HA, Sadaghiani HR et al (2009) Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166:667–674 Jangid KK, Dwivedi P (2016) Physiological responses of drought stress in tomato: a review. Int J Agric Environ Biotechnol 9(1):53–61 Kapoor D, Bhardwaj S, Landi M, Sharma A, Ramakrishnan M, Sharma A (2020) The impact of drought in plant metabolism: how to exploit tolerance mechanisms to increase crop production. Appl Sci 10(16):5692 Kimura S, Sinha N (2008) Tomato (Solanum lycopersicum): a model fruit-bearing crop. Cold Spring Harb Protoc 2008(11):pdb-emo105 Kogan F, Guo W, Yang W (2019) Drought and food security prediction from NOAA new generation of operational satellites. Geomat Nat Haz Risk 10(1):651–666 Krishna R, Ansari WA, Soumia PS, Yadav A, Jaiswal DK, Kumar S, Singh AK, Singh M, Verma JP (2022) Biotechnological interventions in tomato (Solanum lycopersicum) for drought stress tolerance: achievements and future prospects. Biotech 11:48 Kumar A, Verma JP (2018) Does plant-microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52 Li J, Ouyang B, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y, Feng Y, Hao Y, Ye Z (2012) Tomato SIDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. J Exp Bot 63:6407–6420 Liang G, Liu J, Zhang J, Guo J (2020) Effects of drought stress on photosynthetic and physiological parameters of tomato. J Am Soc Hort Sci 145(1):12–17 Liu X-M, Zhang H (2015) The effects of bacterial volatile emissions on plant abiotic stress tolerance. Front Plant Sci 6:774 Lu F, Xu F, Li Z, Liu Y, Wang J, Zhang L (2019) Effect of vibration on storage quality and ethylene biosynthesis-related enzyme genes expression in harvested apple fruit. Sci Hortic 249:2011-6 Maclntyre AM, Meline V, Gorman Z, Augustine SP, Dye CJ, Hamilton CD, Iyer-Pascuzzi AS, Kolomiets MV, McCulloh KA, Allen C (2022) Trehalose increases tomato drought tolerance, induces defences, and increses resistance to bacterial wilt disease. PLoS One 17:e0266254 Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530 Mishra KB, Ianacone R, Petrozza A, Mishra A, Armentano N, La Vecchia G, Trtilek M, Cellini F, Nedbal L (2012) Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Sci 182:79–86

214

K. Tamreihao et al.

Motamedzadegan A, Tabarestani HS (2018) Tomato production, processing, and nutrition. In: Handbook of vegetables and vegetable processing. Wiley, Hoboken, NJ, pp 839–861 Orellana S, Yanez M, Espinoza A, Verdugo I, Gonzalez E, Ruiz-Lara S, Casaretto JA (2010) The transcription factor SIAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2208 Orozco-Mosqueda MC, Duan J, DiBernardo M, Zetter E, Campos-Garcia J, Glick BR, Santoyo G (2019) The production of ACC deaminase and trehalose by the plant growth promoting bacterium pseudomonas sp. UW4 synergistically protect tomato plants against salt stress. Front Microbiol 10:1392 Pandey S, Gupta S (2020) Evaluation of pseudomonas sp. for its multifarious plant growth promoting potential and its ability to alleviate biotic and abiotic stress in tomato (Solanum lycopersicum) plants. Sci Rep 10:20951 Park YS, Dutta S, Ann M, Raaijmakers JM, Park K (2015) Promotion of plant growth by Pseudomonas fluorescens strain SS101 via novel volatile organic compounds. Biochem Biophys Res Commun 461:361–365 Pervez MA, Ayub CM, Khan HA, Shahid MA, Ashraf I (2009) Effect of drought stress on growth, yield and seed quality of tomato (Lycopersicon esculentum L.). Pak J Agric Sci 46:174–178 Raji M, Thangavelu M (2021) Isolation and screening of potassium solubilizing bacteria from saxicolous habitat and their impact on tomato growth in different soil types. Arch Microbiol 203:3147–3161 Ranawat B, Mishra S, Singh A (2021) Enterobacter hormaechei (MF957335) enhanced yield, disease and salinity tolerance in tomato. Arch Microbiol 203:2659–2667 Salehi-Lisar SY, Bakhshayeshan-Agdam H (2016) Drought stress in plants: causes, consequences, and tolerance. In: Drought stress tolerance in plants, vol 1. Springer, Cham, pp 1–16 Salinas-Vargas D, de los Ángeles Maldonado-Peralta M, Rojas-Garcia AR, León-Villanueva A, Álvarez-Vázquez P, Maldonado-Peralta R (2021) Response of tomato varieties (Solanum lycopersicum L.) to water stress. Agro Productividad 13(12). https://doi.org/10.32854/agrop. v13i12.1897 Samaras A, Roumeliotis E, Ntasiou P, Karaoglanidis G (2021) Bacillus subtilis MBI600 promotes growth of tomato plants and induces systematic resistance contributing to the control of soilborne pathogens. Plan Theory 10:1113 Siraj S, Khan MA, Hamayun M, Ali S, Khan SA, Hussain A, Iqbal A, Khan H, Kang S-M, Lee I-J (2022) Microbacterium oxylans regulates physio-hormonal and molecular attributes of Solanum lycopersicum under drought stress. Agronomy 12:3224 Sivakumar R, Srividhya S (2016) Impact of drought on flowering, yield and quality parameters in diverse genotypes of tomato (Solanum lycopersicum L.). Adv Hortic Sci 30:3–11 Tamreihao K, Devi AK, Langamba P, Singh HN, Singh TS, Rajiv C, Kshetri P, Choudhury BU, Sharma SK, Roy SS (2022) Growth kinetics, improved plant growth and alleviation of water stress in tomato by water stress tolerant bacteria. Antonie Van Leeuwenhoek 115(12): 1437–1453 Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. PNAS 97:11632–11637 Vannini C, Campa M, Iriti M, Genga A, Faoro F, Carravieri S, Rotino GL, Rossoni M, Spinardi A, Bracale M (2007) Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. Plant Sci 173:231–239 Vincour B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech 16:123–132

9

Alleviation of Drought Stress and Amelioration of Tomato Plant Growth. . .

215

Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223 Yáñez M, Cáceres S, Orellana S, Bastías A, Verdugo I, Ruiz-Lara S, Casaretto JA (2009) An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stressrelated genes. Plant Cell Rep 28:1497–1507 Zhou R, Yu X, Ottosen C-O, Rosenqvist E, Zhao L, Wang Y, Yu W, Zhao T, Wu Z (2017) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol 17(1). https://doi.org/10.1186/s12870-017-0974-x Zou C, Li Z, Yu D (2010) Bacillus megaterium strain XTBG34 promotes plant growth by producing 2-pentylfuran. J Microbiol 48:460–466

Associative Nitrogen Fixers- Options for Mitigating Climate Change

10

Minakshi Grover, Sivakumar Yaadesh, and Anegundi Jayasurya

Abstract

Nitrogen (N2), a crucial element for all living beings, is present abundantly (78%) in Earth’s atmosphere but in an unreactive form that cannot be directly incorporated into the living biomass. It needs to be fixed in usable forms by biological or chemical processes. Nitrogen demand in agriculture is met majorly through the use of nitrogenous fertilizers manufactured chemically through the Haber–Bosch process. This process, although efficient in the fixation of N2, requires conditions of very high temperature and pressure which are achieved at the cost of large amounts of fossil fuel and release of high volume of CO2, a greenhouse gas (GHG). Moreover, the nitrogenous fertilizers applied to agricultural soils are not fully consumed by the crops; rather a major portion is lost through chemical and biological processes to the atmosphere as GHGs and to the deeper soil layers as leachates, causing air, soil and water pollution and adding to global warming. Microorganisms possessing functional nitrogenase enzyme complexes can fix the naturally available inert N2 into plant usable form (ammonia) and hence can supplement chemically synthesized nitrogen in agriculture. Biologically, nitrogen can be fixed symbiotically or nonsymbiotically. Symbiotic-nitrogen fixation involves an obligatory relationship between the microorganism and the host. The Rhizobium-legume symbiosis, an obligatory system, is the most well-studied biological nitrogen-fixing system till date and is thought to be most efficient in terms of nitrogen benefits to the host plants. The nonsymbiotic nitrogen fixers do not need to form obligatory relationships with the host plant and can be free living or associative in nature. The associative N2 fixers colonize the roots (surface/interiors) without causing any structural changes in the host plant and can play an important role in saving nitrogenous fertilizers in M. Grover (✉) · S. Yaadesh · A. Jayasurya ICAR-Indian Agricultural Research Institute, New Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_10

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agriculture if used strategically. Several researchers have demonstrated the contribution of associative N2 fixers in plant growth promotion and N nutrition. By using effective strains, not only nitrogenous fertilizers doze can be reduced, but the energy inputs and the GHG emission associated with the manufacturing and application of nitrogenous fertilizers can also be checked. The associative N2 fixers also exhibit phyto-stimulatory effects by expressing various plant growthpromoting traits. Literature also reports efficient mitigation of abiotic stress effects in host plants inoculated with associative N2 fixers. The mechanisms exhibited by the associative N2 fixers are similar to those observed in other plant growth-promoting bacteria, however, the complete picture is still not clear. Here in this chapter, we discuss the disadvantages related to the use of nitrogenous fertilizers, role of associative N2 fixers in reducing the dependence on nitrogenous fertilizers, and the benefits associated in terms of GHG emission and energy saving. We also discuss the climate change, related abiotic stress in agriculture, and the potential of associative N2 fixers in mitigating the effect of climate change in agriculture by giving special emphasis on model associative N2 fixers, Azopsirillum spp. The chapter will be valuable for the researcher and the policymakers working on climate change mitigation through the use of microorganisms. Keywords

Azopsirillum · BNF · Nitrogenase · Associative N2 fixer · Abiotic stress

10.1

Introduction

Nitrogen is a critically essential element in the living biomass as an important constituent for amino acids, nucleic acid, hormones, vitamins, and chlorophyll (in photosynthetic organisms). It is the key input in agricultural production systems. This element is present in the atmosphere in abundance (78% of the air) as molecular nitrogen (N2), however, it cannot be utilized as such by living organisms due to its inert nature. The source of nitrogen in agriculture can be biological (nitrogen fixation and mineralization) and/or chemically synthesized nitrogen-containing fertilizers (urea, DAP, etc.). With the advent of the green revolution, more emphasis was given on the use of chemical inputs in agricultural systems, globally. Agriculture in the postindustrialization era (1961 to 2016) has witnessed an exponential increase in the input of nitrogenous fertilizers from 10 to 77 Tg ha-1 (Martínez-Dalmau et al. 2021). The increasing demand of nitrogen has put more pressure on the fossil fuel reserves as very high temperature and pressure conditions are required in the chemical synthesis of urea through the Haber–Bosch process which also has the disadvantage of producing huge volumes of CO2. The nitrogenous fertilizers applied to the agricultural systems are not utilized fully by the cultivated plants and a major chunk is lost into the environment through

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different processes such as volatilization, run-off into the water bodies, and leaching into deeper soil layers. The lost nitrogenous compounds cause environmental concerns by increasing the levels of greenhouse gases (GHGs) in the air, contaminating the water, soil acidification, and/or biodiversity reduction, etc. Urea applied as nitrogen source gets volatilized to ammonia gas, especially in warm and moist surface soils. This ammonia gets oxidized to nitrite (NO2) and then to nitrate (NO3) by different groups of nitrifying bacteria, whereas other denitrifying microbes sequentially reduce soil NO3 to NO2 and further to nitric oxide (NO), which gets reduced to nitrous oxide (N2O) and/or finally to N2 (Mahmud et al. 2021). Among these nitrogenous compounds nitrous oxide is a major GHG with a much higher warming potential (nearly 310 times more) than that of CO2 (Fagodiya et al. 2017). Also, the high ozone depletion potential of N2O (similar to hydrochlorofluorocarbons) poses threat to the environment (Fagodiya et al. 2017). The atmospheric level of N pollution is expected to increase by up to 156% from 2010 to 2050, with the agricultural sector as the major contributor (nearly 60%) for this increase (Martínez-Dalmau et al. 2021). Nitrogen emitted from the added nitrogenous fertilizer forms the major source of N pollution from the agriculture sector (Olivares et al. 2013). Thus, the nitrogen lost from the agricultural soil into the atmosphere contributes significantly to global warming.

10.2

Nitrogen Management in Agriculture: Share of Biologically Fixed Nitrogen

In order to mitigate global warming, there is an urgent need to reduce N2O emissions and NH3 volatilization from agricultural sources by developing and implementing appropriate strategies. Many developed countries have started to act in this direction. A good example is, “Consistent 4R (right source, rate, time and place) Nitrogen Stewardship” program, being promoted among the farmers of Alberta (Canada), with the aim to reduce N2O emissions by optimizing the N application in agriculture (Beaty et al. 2015). The program advocates the use of slow-release N fertilizers, urease, and nitrification inhibitors, and crop demand (real-time) based N fertilization rates. Attempts are also being made worldwide, to improve the N use efficiency (NUE) in agriculture through biotechnological and agronomical interventions (Mahmud et al. 2021; Bloch et al. 2020). In this direction, biological nitrogen fixation if exploited properly can be of great help in simplifying the nitrogen management. According to published estimates, BNF systems fix nearly 1.95 × 1011 to 2.5 × 1011 kg of N-NH3 yearly (Aasfar et al. 2021). The leguminous plants form symbiotic relationship with diazotrophic rhizobia living as bacteroids within the nodules and are benefitted in terms of N fixed biologically by the symbiotic partner. Rhizobium-legume symbiosis is estimated to fix up to 300 kg N h-1 every year (Aasfar et al. 2021). Therefore, the inclusion of legume crops in cropping systems shows residual effect on the N status of soil as well as on succeeding crops, thus helping in saving chemical nitrogenous fertilizers (Kebede 2021).

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Similarly, there are nonsymbiotic nitrogen-fixing microorganisms that do not form obligatory association with the plants but can contribute immensely through BNF and diverse other mechanisms, in improving plant growth and yield parameters. Nonsymbiotic BNF in cereal production systems (maize, wheat, and rice) is estimated to contribute nearly 15 kg of N h-1 y-1 (Ladha et al. 2016). These estimates indicate that there is a lot of scope for interventions in cereal crops for the management of N through nonsymbiotic BNF (Bloch et al. 2020).

10.3

Microorganisms Involved in Biological Nitrogen Fixation

The BNF involves a series of microbiological processes that transform inert atmospheric N2 into ammonium, which gets incorporated into microbial cell components via amino acids. The organic N incorporated into the microbial biomass gets transformed by mineralization and nitrification to plant-usable inorganic forms (NH4+ and NO3-). These microbiological processes are controlled by several factors including soil moisture, temperature, aeration, nutrient availability, etc. Therefore, the amount of biologically fixed N in the soil under natural conditions is generally small, making it the critical nutrient in the terrestrial agroecosystems required for plant growth (Martínez-Dalmau et al. 2021). Some prokaryotes have the ability to break the triple bond in the inert (N  N) molecule to produce ammonium, using the catalytic activity of the oxygen-sensitive enzyme nitrogenase and high input of energy. Beijerinck (1888) isolated nodule bacteria and named it as Bacillus radicicola, later renamed as Rhizobium. Nitrogenfixing ability in nonsymbiotic microorganisms was initially reported in Azotobacter and Clostridium spp. Several bacterial and archaeal genera are now known to possess the ability to capture molecular nitrogen, convert it to fixed N-NH3 form, and transfer to the plants through establishing mutualistic relationships. The distribution of nitrogen-fixing traits and the related genes are now found to be much more common among the microbial genomes (Dos Santos et al. 2012). The highly conserved and oxygen-sensitive nitrogenase enzyme complex present in the diazotrophs enables them to develop various types of interactions/associations with the host plant (Rosenblueth et al. 2018).

10.3.1 Symbiotic and Free Living N Fixers The Rhizobium-legume symbiosis is the most efficient and extensively studied nitrogen-fixing system (Olivares et al. 2013). It is obligatory symbiosis where soil bacteria collectively known as rhizobia (include Rhizobium, Bradyrhizobium, Mesorhizobium, and Sinorhizobium) recognize the plant signals and form nodule in the cortical region of legume roots. Inside the nodules, rhizobia get transformed into bacteroides and fix N2 with the aid of nitrogenase enzyme complex. Nodules provide oxygen-limited and energy-rich conditions favorable for BNF. The N2 thus

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fixed as NH3 by bacteroides is also channelized to the host and the host in turn provides energy and shelter to the bacteria. Free-living N2 fixers are found in diverse habitats (soil, water, organic matter, in or on the plants, etc.). They can interact with the plants to primarily inhabit the soil– root interface as free living or associative partners. Sometimes, they can gain entry inside the plant tissues and establish internally (in the roots and/or aerial parts) and are referred to as endophytes (Ladha et al. 2022). The free-living nitrogen fixers, as indicated, can fix N2 while living freely. Azotobacter spp. are good examples of freeliving nitrogen fixers and have been exploited commercially. However, they have also been reported to establish in the internal plant tissues indicating their associative nature. Döbereiner et al. (1972) observed the cultivar-specific association of nitrogen-fixing Azotobacter paspali with Paspalum notatum. However, its plant growth-enhancing potential may be attributed to other traits than N2 fixation, like production of phytohormones (Olivares et al. 2013). The nitrate and ammonium transporters expression could be improved by free-living nitrogen fixers of Bacillus spp. leading to improved nutrient uptake in Arabidopsis plants (Calvo et al. 2019). Among other free-living N2 fixers are blue-green algae (cyanobacteria) that have evolved strategies (specialized thick-walled cells for nitrogen fixation called heterocysts) that provide protection to the enzyme nitrogenase from the oxygen produced during photosynthesis. Some cyanobacteria (including Nostoc, Anabaena spp.) form associations with higher organisms like fungi, bryophytes, aquatic ferns, gymnosperms, and angiosperms and can transfer the biologically fixed N2 (ammonia) to the host directly (Olivares et al. 2013). Although able to fix N2 in the freeliving form, these cyanobacteria form more heterocyst cells and exhibit higher rates of nitrogen fixation when in association with the host (Meeks and Elhai 2002). Also the glutamine synthetase (GS) activity is reported to be very low in symbiotic cyanobacteria as compared to that in free-living form, supporting the ammoniaexcreting nature of the symbiotic cyanobacteria.

10.3.2 Associative N Fixers In addition to the free living and symbiotic nitrogen fixers, there are the associative nitrogen fixing bacteria which form close associations with the roots. As BNF is an energy-intensive process, plant-associated N2 fixers have higher agronomic significance as compared with free-living N2 fixers, as they can fulfill their energy needs from the nutrients present in the root exudates (Olivares et al. 2013). In associative symbiotic systems, diazotrophic bacteria colonize the rhizoplane and eventually may get entry inside the root tissues to inhabit and colonize the intercellular spaces in the root cortex. However, no structural modification occurs in the roots for N2 fixation and direct transfer of ammonia to the host plant is not evident. Most diazotrophs found associated with plant roots belong to α- (Azospirillum, Gluconacetobacter spp.), β- (e.g., Azoarcus, Burkholderia, Derxia, Herbasprillum

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spp.), and γ- (e.g., Azotobacter, Klebsiella, Pantoea, Pseudomonas, Serratia spp.) Proteobacteria. However, members of other groups, for example, Firmicutes (Paenibacillus spp.), actinobacteria (Frankia spp.), cyanobacteria (Nostoc spp.), etc. have been observed in the rhizosphere of many crop plants (van Dommelen and Vanderleyden 2007; Rosenblueth et al. 2018). The associative diazotrophs that can also colonize the intercellular spaces in the inner plant tissues without showing any negative effect are considered as endophytes (Herbaspirillum, Gluconacetobacter, Azoarcus, Burkholderia, etc.). Nitrogen fixed by associative diazotrophs may or may not be directly available to the plants. However, there are other mechanisms than N2 fixation exhibited by associative diazotrophs (phytohormones production, nutrient acquisition, disease control, abiotic stress tolerance, etc.) which help in plant growth promotion (Franche and associates 2009). A number of commercial products based on diazotrophic PGPR, particularly Azospirillum spp., are in use worldwide. Application of Azospirillum-based inoculants has been demonstrated to reduce the dose of industrially synthesized N fertilizer in cereals and other crops (Dobbelaere et al. 2001). Experiments have shown that symbiotically fixed N contributes significantly to the plant N content and this contribution varies in different host-diazotroph interactions (Bashan and Bashan 2010).

10.4

Climate Change, Related Abiotic Stresses, and Role of Microorganisms

Agriculture is considered among the highly vulnerable sectors regulated and influenced by climatic conditions. The increasing incidences of climate-changeinduced biotic and abiotic stressors are causing threat to sustainable production in principal crops. Decline in the yields of major crops like paddy and wheat has been reported in the South Asian region primarily due to decreasing moisture availability, rising air temperature, and reduced number of rainy days. According to IPCC, the average temperature at global levels is predicted to rise by up to 5.8 °C by 2100, relative to 1990. The irrigation demands are projected to increase under high temperatures particularly in the arid and semi-arid zones. Changing global climate is increasing the intensities of various abiotic stresses like elevated CO2, high and low temperatures, droughts, erratic and extreme rainfall events, floods, cyclones, salinity, etc. that cause serious pressure on agriculture and economy (He et al. 2018). In general, all biotic and abiotic stresses trigger an oxidative stress response in living organisms that can damage the cellular structures due to the overproduction of reactive oxygen species (ROS). The ROS triggers oxidative stress reactions resulting in disturbed enzyme activities and cellular processes (Bhargava et al. 2013). The effect of abiotic stresses is observed at cellular as well as whole plant level due to change in the morphology and altered physiological parameters thus resulting in poor growth and productivity (Shao et al. 2007; Farooq et al. 2009; Bhargava et al. 2013; Meena et al. 2017). In response to abiotic stress conditions, plants employ a variety of mechanisms such as osmotic adjustment through accumulation of

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osmoprotectants, scavenging of ROS through antioxidant systems, and synthesis of specific proteins which help in sustaining physiological functions under stress conditions. Under moderate stress conditions, antioxidant defense systems can scavenge the free radicals efficiently; however, under severe stress conditions particularly in sensitive plants, the scavenging system becomes saturated and the damage caused by amassed production of radicals becomes unavoidable. Under stress conditions, the channelization of energy toward survival mechanisms affects the plant growth, agronomic yield, and quality. Moreover, severe and/or prolonged abiotic stress conditions may lead to plant death and crop losses (Simova-Stoilova et al. 2006; Ngumbi and Kloepper 2016). Worldwide, prioritized research is being conducted to evolve strategies and methods to manage abiotic stress effects in agriculture, including the development of resistant/tolerant varieties through breeding and biotechnological tools, resource management practices, agronomic interventions, etc. (Venkateswarlu and Shanker 2009). In this direction, the application of microorganisms to combat abiotic stress in crop plants is widely reported as a low-cost, eco-friendly strategy. Microorganisms including diverse bacteria, viruses, and fungi have exhibited the ability to induce stress tolerance in plants (Grover et al. 2011, 2021; Meena et al. 2017). Deploying stress adapted/tolerant microorganisms can help the plants by improving water relations by improving root traits, producing exopolysaccharides, enhancing nutrient availability, and helping the plants in neutralizing the ROS. Enhanced levels of different antioxidant enzymes and higher accumulation of antioxidants have been observed in PGPR-inoculated plants under drought, thereby helping the plant mitigate the stress effects. Contrastingly, PGPR-inoculated drought-stressed plants have also shown reduced antioxidant enzyme activities indicating reduced stress levels due to inoculation (Sandhya et al. 2010). Diverse groups of beneficial bacteria including Klebsiella, Pseudomonas, Azospirillum, Bacillus, Raoultella, Paenibaclillus, Azotobacter, Rhizobium, and many more have been found to improve plant growth under abiotic stress conditions. However, the mechanisms underlying it are still not fully understood. Several studies have demonstrated the responsiveness of inoculated plants to different types of stresses at agronomical (root, shoot length and biomass, leaf area, stem diameter, nutrient status, and yieldrelated parameters), physiological (photosynthetic rate, chlorophyll content, water relations, osmolytes, etc.), genomic (altered expression of stress-responsive genes), and proteomic (altered protein profile) levels in diverse crops (Sandhya et al. 2011; Bodhankar et al. 2020; Grover et al. 2021). Plant growth promoting rhizobacteria with the ability to induce systemic tolerance in plants may be employed as a strategy to enhance crop productivity (Yang et al. 2009). PGPR including diazotrophs have exhibited potential to aid plant abiotic stress tolerance through exhibiting various traits like ability to produce plant growth regulators, EPS, volatile compounds, ACC (1-aminocyclopropane-1carboxylate) deaminase, induce osmolyte accumulation and antioxidants, regulae stress-responses at genetic levels, and cause changes in the root traits (Grover et al. 2011, 2021; Sarma and Saikia 2014; Kaushal and Wani 2016). Their interactions

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with the plants elicit a variety of local and systemic responses that improve metabolic capacity of the plants to overcome abiotic stresses. Microbially produced phytohormones like IAA promote the growth of longer roots by increasing the root hair density and root flanks that help in nutrient and water uptake (Grover et al. 2021). Abscisic acid (ABA) a plant hormone also controls the plant development as well as its response to stress conditions, by regulating the stomatal behavior. Some PGPR including Azospirillum, Achromobacter, and Rhizobium spp. could produce ABA or stimulate ABA production under abiotic stress conditions (Cohen et al. 2015; Egamberdieva et al. 2017). Under stressful conditions, microorganisms produce an increased amount of exopolysaccharide (EPS) as an adaptive response. The extracellular polysaccharides aid in soil structure formation through aggregation. Plants pre-inoculated with EPS-producing bacteria exhibited improved tolerance to moisture deficit conditions due to better water retention in the rhizosphere (Vurukonda et al. 2016). Rice plants inoculated with a root colonizing EPS-producing Pseudomonas sp. exhibited increased salinity tolerance (Sen and Chandrasekhar 2014). EPS production also aids in biofilm formation on the soil and root surface which acts as a barrier against the harsh environmental conditions, thus increasing the chance of survival under stressful environments (Flemming and Winger 2010). Biofilms also act as a matrix for the storage and channelization of nutrients and water from the soil to plants. Accumulation of compatible solutes like glycine betaine, trehalose, proline, etc. indicates osmoadaptive response in plants and bacteria (Rodriguez et al. 2009). The compatible solutes are the water-soluble organic molecules that being physiologically consistent with cellular components help in osmoadaptation (Bolen and Baskakov 2001). Inoculation with PGPR has been reported to enhance the osmolyte accumulation in host cells thus leading to osmoadaptation (Bacilio et al. 2004). Certain PGPRs carrying the enzyme ACC deaminase can remove ACC from plants (Orozco-Mosqueda et al. 2020). These bacteria metabolize ACC to form ketobutyrate and ammonia, reducing the amount of substrate required for ethylene synthesis and thus controlling the levels of ethylene. Inoculation with ACC deaminase-producing bacterial strains of B. phytofirmans, B. amyloliquefaciens, and P. oryzihabitans increased root elongation in the host plants (Oleńska et al. 2020). Furthermore, VOCs produced by microbes govern plant growth (Mohanty et al. 2021; Ullah et al. 2021). Recent results also show that microbial inoculation alters the expression of stress-sensitive genes in plants, suggesting their regulatory role at genomiclevel (Tiwari et al. 2016; Bodhankar et al. 2019; Abd El-Daim et al. 2019). A number of the mechanisms outlined earlier, as well as other undiscovered mechanisms, may well be involved in providing plants with abiotic stress tolerance as reviewed earlier (Meena et al. 2017; Grover et al. 2021).

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10.4.1 Associative Nitrogen Fixers in Mitigation of Abiotic Stress Responses in Plants Inoculation with diazotrophic bacteria has helped in better survival and higher growth and yield parameters of plants under stress conditions. However, there is no evidence of direct involvement of microbial nitrogen-fixing ability in providing protection to the host plant against abiotic stresses. Rather, various other mechanisms as reported in non-diazotrophic stress-alleviating PGP bacteria have been observed in diazotrophs which might be working behind the alleviation of abiotic stress in host plants. Majority of the work reported on nonsymbiotic diazotrophs-induced abiotic stress alleviation in plants is on Azospirillum and Azotobacter spp. (Table 10.1). Abundant studies have demonstrated the Azospirillum spp. mediated mitigation of abiotic stresses like salinity, drought, etc. indicating the benefits associated with Azospirillum inoculations (García et al. 2017). Inoculating sorghum plants with A. brasilense resulted in higher leaf water content and lower canopy temperature under drought stress. Maize plants inoculated with A. brasilense had higher relative and absolute water content as well as an increased proline and biomass than uninoculated control plants (Casanovas et al. 2002). Similarly, trehalose-producing A. brasilense strain improved plant growth and drought tolerance of maize (Rodriguez et al. 2009). Pre-inoculation with Azospirillum improved the water status and coleoptile length of wheat exposed to osmotic stress. Drought-stressed canola plants pre-inoculated with A. lipoferum showed improved germination, water status, leaf chlorophyll, and surface area of root (Saeed et al. 2016). Similarly, as reported by Cohen et al. (2015), pre-inoculating A. brasilense resulted in higher plant growth and better physiological status of Arabidopsis plants. The inoculation also reduced stomatal conductance thus improving water use efficiency. Curá et al. (2017) studied the bio-protective effect of A. brasilense strain SP-7 inoculation in maize under normal and drought conditions. In comparision to the uninoculated plants, the pre-inoculated plants showed higher tolerance toward negative effects of moisture deficit stress and produced higher biomass, carbon, nitrogen, and chlorophyll contents; and recorded less membrane injury and reduction in the levels of abscisic acid and ethylene, the plant stress hormones. Furthermore, the oxidative stress levels in the inoculated plants were similar to those in un-inoculated well-watered plants. Also, higher relative water content and significantly low proline levels showed better osmoregulation in the inoculated plants under drought conditions. The results clearly demonstrate that the bacteria could help in mitigating the abiotic stress effects in plants. Foliar application of Azospirillum spp. in maize induced stress-responsive genes, mediated through phytohormone signaling (Fukami et al. 2017). It has been demonstrated that root association with Azospirillum spp. encourages vegetative growth in different plant species. Azospirillum inoculation generally increases root extension, root hair density, number of lateral, and adventitious roots owing to IAA production. Improvement in plant root traits increases plant’s

Wheat (Triticum aestivum L.) (pots, 90 days) Maize (Zea mays) (pots, 4 weeks)

Salinity

Wheat (field)

Maize (pots)

Drought

Drought

Drought

Azotobacter spp. strains Az63, Az69 and Az70

A. brasilense cd

Common bean (Phaseolus vulgaris L.) (PVC-tube growth system)

Maize (seedling stage)

Salinity

Crop/stage Pearl millet (Pennicetum glaucum L.)/(seedling stage)

Stress Osmotic

Salinity

Azotobacter chroococcum strains C5 and C9 Azospirillum lipoferum, Azotobacter chroococcum Azospirillum brasilense Sp245

Name of the organism Azospirillum formosense strains AIM3, AIM19, AIM38, AIM57, AIM82 Azotobacter spp. strain ST24

Phosphate and potassium solubilization, siderophore production, tolerance to osmotic stress Increases root length and root area

N2 fixation, biosynthesis of plant growth regulators, etc.

Not reported

IAA production, P-solubilization, N2 fixation under salinity stress

N2 fixation, salinity tolerance

PGP tratis/mechanisms observed in the microorganism/s IAA production, siderophores, N2 fixation, biofilm formation, proline accumulation under osmotic stress

Table 10.1 Associative diazotrophs in mitigating abiotic stress in crop plants

Improved polyphenol and chlorophyll content and K+/Na+ ratio, reduced proline levels Enhanced growth parameters, pigments, osmolytes, K+/Na+ ratio, and the activity of CAT, POD, and APX Improved water relations and additional “elastic adjustment”, higher yield and mg, K, and ca in grain Increased shoot dry weight, plant height, chlorophyll content, nitrogen, phosphorous, and iron concentration Increased root length, root projection area, and specific root projection area of inoculated plants

Increased plant growth and N conrtent

Observed effects on host plant Increase in percent germination and seed vigor indices

German et al. (2000)

Shirinbayan et al. (2019)

Creus et al. (2004)

Latef et al. (2020)

Rojas-Tapias et al. (2012)

Chaudhary et al. (2013)

Reference Jayasurya and Grover (2023)

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Chickpea (Cicer arietinum L.) (pots)

Wheat (pots)

Salinity

Drought

Drought

Azospirillum lipoferum AZ1, AZ9 and AZ45

A. brasilense Sp. 245

Arabidopsis thaliana ()

Maize (pots)

Drought

A. Lipoferum USA 59b A. Lipoferum FK1

Maize (pots)

Osmotic

A. Brasilense BR11005

Modulating osmolytes, antioxidants machinery, and stressrelated genes expression Induces decrease in leaf water potential, increase in leaf water content, enhanced root growth and production of IAA Increases ABA content

Produces ABA and gibberellins

Increases root growth, proline accumulation, and water potential

Inoculation improved plant’s ABA content

Improved leaf RWC and WC, increased root growth and proline accumulation in both leaves and roots Improved plant length, leaf area, and RWC Improved growth, photosynthetic pigments, osmolytes, phenols, flavonoids and antioxidants Inoculation decreased leaf water potential and increased leaf water relative content Cohen et al. (2008)

Arzanesh et al. (2011)

Cohen et al. (2009) El-Esawi et al. (2018)

Casanovas et al. (2002)

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ability to acquire water and nutrients from the deeper soil layers thus improving its survival under moisture-deficit conditions (Grover et al. 2021). The increased production of abscisic acid (ABA), which causes stomatal closure, has also been linked to beneficial benefits of Azospirillum inoculation under drought conditions (Cohen et al. 2015). Also, the accumulation of osmoprotectants, like free amino acids and sugars, helps in mitigating the dehydration-related stresses at cellular level (Bacilio et al. 2004; Saharan and Nehra 2011; Hungria et al. 2015). Commercial Azospirillum-based bio-inoculants (liquid and carrier based) are widely employed for nitrogen benefits in many nations (Aasfar et al. 2021). Inoculating pearl millet with A. brasilense improved the root biomass and caused significant yield increment under diverse Indian agro-climatic conditions, particularly under low N doses indicating their potential application across diverse agroecologies (Tilak and Subba Rao 1987). Similarly, studies have revealed the potential of Azotobacter spp. to tolerate abiotic stress and to colonize and improve the plant performance under the imposed stress. The EPS secreted by Azotobacter spp. helps in maintaining the cells hydrated and also helps in biofilm formation under desiccation. Inoculation with Azotobacter spp. strains improved the plant growth of wheat and maize under saline conditions (Chaudhary et al. 2013; Rojas-Tapias et al. 2012). Inoculating maize plants with Azotobacter resulted in improved sodium exclusion and potassium uptake under salt stress (Latef et al. 2020). Similarly, several other workers have also demonstrated the potential of Azotobacter spp. in the alleviation of drought effects in different plants (Creus et al. 2004; Shirinbayan et al. 2019) as presented in Table 10.1.

10.4.2 Associative Nitrogen Fixers and GHG Emissions Agricultural soils contribute up to 6.8 Tg of N2O-N y-1 to the atmosphere, which is nearly 60% of the total N2O released into the atmosphere globally (Olivares et al. 2013). Nearly 4.2 Tg N2O-N per year is emitted directly by the nitrogenous fertilizers N added to the soil (Baggs and Philippot 2011), indicating a major contribution in GHG emission from agricultural soils. Associative N fixers can help in this regard by reducing the doses of nitrogenous fertilizers in nonlegume crops. Similar to legume crops, cereal crops, having associative diazotrophs as partners, can have their own source of N, thus greatly reducing the dependence on chemically synthesized nitrogenous fertilizers (Fig. 10.1) in addition to having other plant-beneficial effects. It is estimated that almost two tons of chemically fixed N is needed to produce the effects equal to that produced with just one ton of biologically fixed N in agriculture (Cheng 2008). Studies have reported that inoculation with nonsymbiotic N fixers can save nearly 25% of chemical nitrogen in nonlegumes (Sangwan et al. 2021). Supplementing 25% chemical nitrogen by using associative N fixers as bioinoculants in nonlegume crops like cereals can have huge impact in terms of effects in terms of amount of energy saved and reduction in GHG emissions. In addition, the negative effect of nitrogenous leachates on soil health can be controlled to some extent.

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Fig. 10.1 Benefits of using associative nitrogen fixers, (a) energy savings and reduction in GHG emissions (dotted lines) due to savings on chemical N inputs; (b) benefit to the host plant

10.5

Azospirillum: A Model Associative Nitrogen Fixing Microorganisms with Multifarious Traits as Bioinoculant

Diazotrophs are of great interest, due to their ecological as well as agronomic importance. Diazotrophs belonging to genus Azospirillum are known to exhibit plant-beneficial functions in addition to N2 fixation which may include the production of plant growth hormones, minerals solubilization and nutrient acquisition, biotic and abiotic stress tolerance, and bioremediation (Cassán et al. 2020; Ladha et al. 2022). Thus, depending on their inherent traits, mode of interaction, and competitiveness, Azospirillum can function as biofertilizers, phyto-stimulators, and/or abiotic stress mitigating agents for the plants (Fig. 10.2). Plant hormone production is a key feature of Azospirillum spp. that has been observed in practically all research explaining the PGP capabilities of this significant diazotrophic species. Amongst phytohormones, IAA has been linked to Azospirillum inoculation-mediated changes in root characteristics (root hair length and density, as well as lateral branching) (Grover et al. 2022). Such an effect upon root architecture could have a significant impact on the plant’s nutrition and moisture absorption by improving accessibility to lateral as well as deeper soil zones (Grover et al. 2021).

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Fig. 10.2 Multi-dimensional properties observed in Azospirillum spp.

Azospirillum spp. strains can also synthesize gibberellins and cytokinins, which are vital in the growth of plants (Cakmakci et al. 2020). Production of ABA in vitro is also reported in Azospirillum spp. (Kolb and Martin 1985; Perrig et al. 2007) and inoculation with Azospirillum spp. has been found to improve ABA content in the A. thaliana under drought stress (Cohen et al. 2008). Nitric oxide (NO) is a signal molecule able to regulate diverse processes in plants including stress responses. Inoculation with A. brasilense increased NO release by tomato plants exposed to salinity (Creus et al. 2005). The regulatory role of NO in hormonal cascade has been linked to root growth and biofilm formation by the inoculated Azospirillum spp. strain (Molina-Favero et al. 2008). Another extensively reported PGP feature in Azospirillum is the formation of siderophores that aid in the chelation of iron, a metabolically vital nutrient that is difficult to get given its plentiful availability. Azospirillum spp. require Fe as a cofactor for enzyme nitrogenase to operate (Bashan and Bashan 2010; Reis et al. 2015). Siderophore-producing PGPRs not only aid in iron intake, but they also assist in suppression of dangerous microbe populations by increasing competition for iron. Because of the substantial ATP requirement of the biological nitrogen fixation pathway, phosphorus is yet another mineral that acts as a major constraint for nitrogen fixation. The organic and insoluble inorganic phosphorus molecules in the soil could be digested into the available forms, assisting in plant P feeding (Khan et al. 2007). Phosphate solubilizing capacity has been established in various Azospirillum species, notably A. brasilense strains and A. lipoferum strains able to produce gluconic acid that promotes phosphate solubilization in rock strata (Puente et al. 2004; Rodriguez et al. 2004). Deposition of suitable solutes during response to stressful circumstances is an effective adaptation mechanism that aids in the maintenance of cell turgor and the stability of cell organelles. Proline, proline betaine, glycine betaine, carnitine, trehalose, glucosylglycerol, and ectoine are examples of suitable solutes absorbed by eubacteria (Kempf et al. 1998; Roesser and Müller 2001;

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Pade et al. 2014). Osmoadaptation processes were evident in A. brasilense under osmotic stress as greater levels of compatible solutes including glycine, betaine, proline, and trehalose were observed under stress conditions (Tripathi et al. 1998). Cesari et al. (2016) observed that under osmotic stress conditions, A. brasilense resulted in cell membrane reorganization caused by altered lipid composition so as to maintain the optimal membrane fluidity. Similarly, exopolysaccharide production and biofilm formation have been reported to increase under osmotic stress conditions (Jayasurya and Grover 2023) indicating their ability to survive under stress conditions. Moreover, members of genus Azospirillum are known to form cysts, a stage with minimal metabolic activity that is induced under unfavorable conditions. Cyst formation is highly advantageous under stressed ecosystems where intermittent dry or hot spells are common. With the return of favorable conditions, the cysts get converted into vegetative cells with normal metabolism. Thus, the population of inoculated strains is not wiped out completely and can build up gradually along with the cropping cycle. Thus, a multifaceted group of microorganisms might provide multifarious benefits to the host plant under stress conditions if they are able to express PGP traits under stress conditions. Few studies in vitro have reported the expression of PGP traits in Azospirillum spp. strains under imposed osmotic stress, however, to a lesser extent when compared with that under normal conditions (Jayasurya and Grover 2023). Nonetheless, the expression of PGP traits under abiotic stress conditions indicates their survival and metabolic potential which may resume to normal once the conditions turn favorable.

10.6

Conclusions and Way Forward

Plant-microbial interactions are crucial for both the partners for survival under varied environmental conditions. The relevance of these interactions appears more for sustainable agriculture under the climate change scenario. It is clear that diazotrophic microorganisms can inexpensively contribute toward supply of N through symbiotic and nonsymbiotic BNF indicating their potential as biofertilizers. The phytostimulatory role of associative biological N fixers in plant growth promotion has been demonstrated in many plants owing to multiple PGP traits including, BNF. To estimate their contribution in N nutrition of the plants, there is a need to closely study these interactions in different plants and to quantify the contribution of biologically fixed nitrogen in supplementing the chemically synthesized N fertilizers. The models can be developed which can help in calculating the benefits of associative BNF in terms of savings on energy required for the manufacturing of equivalent amount of nitrogenous fertilizers and in the reduction in GHG emissions due to supplementation of chemically synthesized nitrogenous fertilizers with associative BNF. Initially, the efforts should be on maximizing the benefits of associative BNF in cereal crops as the interactions and effects are well documented in cereals, later on the acquired experience and strategies may be extended to other crops. Focused research efforts on increasing the ammonia excreting efficiency of the known associative

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diazotrophic strains can help in maximizing the benefits in terms of N. Also there is need to understand and explore the potential of less-known groups of associative and free-living nitrogen fixers other than Azospirillum and Azotobacter. In addition to the biofertilizer and phyto-stimulatory role, the abiotic stress mitigation potential of the diazotroph needs to be harnessed commercially. A deeper understanding of the underlying mechanisms can help in identifying regulatory metabolites that may be utilized for modulating the abiotic stress response in different crop plants. The strains with efficient nitrogen fixation, PGP trait expression, and colonization ability under abiotic stress conditions may be the key for agricultural sustainability under climate change scenarios. Acknowledgment The authors of this chapter are thankful to Director ICAR-Indian Agricultural Research Institute for providing all the support required in preparing this manuscript.

References Aasfar A, Bargaz A, Yaakoubi K, Hilali A, Bennis I, Zeroual Y, Meftah Kadmiri I (2021) Nitrogen fixing Azotobacter species as potential soil biological enhancers for crop nutrition and yield stability. Front Microbiol 12:628379. https://doi.org/10.3389/fmicb.2021.628379 Abd El-Daim IA, Bejai S, Meijer J (2019) Bacillus velezensis 5113 induced metabolic and molecular reprogramming during abiotic stress tolerance in wheat. Sci Rep 9:16282. https:// doi.org/10.1038/s41598-019-52567-x Arzanesh MH, Alikhani HA, Khavazi K et al (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27: 197–205 Bacilio M, Rodriguez H, Moreno M, Hernandez JP, Bashanet Y (2004) Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biol Fertil Soils 40:188–193. https:// doi.org/10.1007/s00374-004-0757-z Baggs EM, Philippot L (2011) Nitrous oxide production in the terrestrial environment. In: Moir JWB (ed) Nitrogen cycling in bacteria: molecular analysis. Caister Academic Press, Norfolk, pp 23–37 Bashan Y, de Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136. https://doi.org/10.1016/S00652113(10)08002-8 Beaty PH, Fischer JJ, Muench DG, Good AG (2015) Environmental and economic impacts of biological nitrogen-fixing (BNF) cereal crops. In: de Bruijn FJ (ed) Biological nitrogen fixation, vol 2, 1st edn. John Wiley & Sons, Hoboken, NJ, pp 1103–1116 Beijerinck MW (1888) Die Bacterien der Papilionaceen-knöllchen. Botanische Zeitung 46:797–804 Bhargava S, Sawant K (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breed 132:21–32. https://doi.org/10.1111/pbr.12004 Bloch SE, Ryu M, Ozaydin B, Broglie R (2020) Harnessing atmospheric nitrogen for cereal crop production. Curr Opin Biotechnol 62:181–188 Bodhankar S, Grover M, Reddy G (2019) In planta screening of maize seed endophytic bacteria for potential applications under dryland conditions. Indian J Dryland Agric Res Dev 34:53–62 Bodhankar S, Grover M, Mallappa M, Reddy G, Ghosh D, Mohapatra S (2020) Expression of selected drought responsive genes of maize as influenced by endophytic bacterial inoculation. J Microbiol Biotechnol Food Sci 10:267–272 Bolen DW, Baskakov IV (2001) The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 310:955–963. https://doi.org/10.1006/jmbi.2001.4819

10

Associative Nitrogen Fixers- Options for Mitigating Climate Change

233

Cakmakci R, Mosber G, Milton AH, Alatürk F, Ali B (2020) The effect of auxin and auxinproducing bacteria on the growth, essential oil yield, and composition in medicinal and aromatic plants. Curr Microbiol 77:564–577. https://doi.org/10.1007/s00284-020-01917-4 Calvo P, Zebelo S, McNear D, Kloepper J, Fadamiro H (2019) Plant growth-promoting rhizobacteria induce changes in Arabidopsis thaliana gene expression of nitrate and ammonium uptake genes. J Plant Interact 14(1):224–231. https://doi.org/10.1080/17429145.2019.1602887 Casanovas EM, Barassi CA, Sueldo RJ (2002) Azospirillum inoculation mitigates water stress effects in maize seedlings. Cereal Res Commun 30:343–350. https://doi.org/10.1007/ BF03543428 Cassán F, Coniglio A, López G, Molina R, Nievas S, de Carlan CLN et al (2020) Everything you must know about Azospirillum and its impact on agriculture and beyond. Biol Fertil Soils 56(4): 461–479. https://doi.org/10.1007/s00374-020-01463-y Cesari AB, Paulucci NS, Biasutti MA, Reguera YB, Gallarato LA, Kilmurray C, Dardanelli MS (2016) Reorganization of Azospirillum brasilense cell membrane is mediated by lipid composition adjustment to maintain optimal fluidity during water deficit. J Appl Microbiol 120:185– 194. https://doi.org/10.1111/jam.12994 Chaudhary D, Narula N, Sindhu SS, Behl RK (2013) Plant growth stimulation of wheat (Triticum aestivum L.) by inoculation of salinity tolerant Azotobacter strains. Physiol Mol Biol Plants 19: 515–519. https://doi.org/10.1007/s12298-013-0178-2 Cheng Q (2008) Perspectives in biological nitrogen fixation research. J Integr Plant Biol 50:786 Cohen AC, Bottini R, Piccoli PN (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103. https://doi.org/10.1111/j.1744-7909.2008.00700.x Cohen AC, Travaglia CN, Bottini R et al (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87: 455–462 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 153:79–90. https://doi.org/10.1111/ppl. 12221 Creus CM, Sueldo RJ, Barassi CA (2004) Water relations and yield in Azospirillum inoculated wheat exposed to drought in the field. Can J Bot 82:273–281 Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303. https://doi.org/10.1007/s00425-005-1523-7 Curá A, Franz DR, Filosofía JE, Balestrasse KB, Burgueño LE (2017) Inoculation with Azospirillum sp. and Herbaspirillum sp. bacteria increases the tolerance of maize to drought stress. Microorganisms 5:41. https://doi.org/10.3390/microorganisms5030041 Dobbelaere S, Croonenborghs A, Amber T, Ptacek D, Vanderleyden J, Dutto P, LabanderaGonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Shimon B, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879 Döbereiner J, Day JM, Dart PJ (1972) Nitrogenase activity and oxygen sensitivity of the Paspalum notatum-Azotobacter paspali association. J Gen Microbiol 71:103–116 Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13:162 Egamberdieva D, Wirth SJ, Alqarawi AA, Abd Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104. https://doi.org/10.3389/fmicb.2017.02104 El-Esawi MA, Al-Ghamdi AA, Ali HM, Alayafi AA (2018) Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stress-related genes expression. Environ Exp Bot 159(1):55. https://doi.org/10. 1016/j.envexpbot.2018.12.001

234

M. Grover et al.

Fagodiya R, Pathak H, Kumar A, Bhatia A, Jain N (2017) Global temperature change potential of nitrogen use in agriculture: a 50-year assessment. Sci Rep 7:44928. https://doi.org/10.1038/ srep44928 Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212. https://doi.org/10.1051/ agro:2008021 Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. https://doi. org/10.1038/nrmicro2415 Franche C, Lindström C, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous. Plant Soil 321:35–59 Fukami J, Ollero FJ, Megías M, Hungria M (2017) Phytohormones and induction of plant stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth. AMB Express 7:153. https://doi.org/10.1186/s13568017-0453-7 García JE, Maroniche G, Creus C, Suárez-Rodríguez R, Ramirez-Trujillo JA, Groppa MD (2017) In vitro PGPR properties and osmotic tolerance of different Azospirillum native strains and their effects on growth of maize under drought stress. Microbiol Res 202:21–29 German M, Burdman S, Okon Y, Kigel J (2000) Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol Fertil Soils 32:259–264. https://doi.org/10.1007/s003740000245 Grover M, SkZ A, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agricultural crops to abiotic stresses. World J Microbiol Biotechnol 27:1231– 1240. https://doi.org/10.1007/s11274-010-0572-7 Grover M, Bodhankar S, Sharma A, Sharma P, Singh J, Nain L (2021) PGPR mediated alterations in root traits: way toward sustainable crop production. Front Sustain Food Syst 4:618230. https://doi.org/10.3389/fsufs.2020.618230 Grover M, Bana RS, Bodhankar S (2022) Prevalance of multifunctional Azospirillum formosense strains in the rhizosphere of pearl millet across diverse edaphoclimatic regions of India. Vegetos 1:1; (Springer) Accepted for publication He M, He CQ, Ding NZ (2018) Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front Plant Sci 9:1771. https://doi.org/10.3389/fpls.2018. 01771 Hungria M, Nogueira MA, Araujo RS (2015) Soybean seed coinoculation with Bradyrhizobium spp. and Azospirillum brasilense: a new biotechnological tool to improve yield and sustainability. Am J Plant Sci 6:811–817. https://doi.org/10.4236/ajps.2015.66087 Jayasurya A, Grover M (2023) Studies on endurance of Azospirillum formosense strains to osmotic stress and modulation of early stage pearl millet growth. Appl Biochem Microbiol 59:206–215. https://doi.org/10.1134/S0003683823020023 Kaushal M, Wani SP (2016) Rhizobacterial-plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agric Ecosys Environ 231:68–78 Kebede E (2021) Contribution, utilization, and improvement of legumes-driven biological nitrogen fixation in agricultural systems. Front Sustain Food Syst 5:767998. https://doi.org/10.3389/ fsufs.2021.767998 Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high osmolality environments. Arch Microbiol 170:319–330. https://doi.org/10. 1007/s002030050649 Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture-a review. Agron Sustain Dev 27:29–43. https://doi.org/10.1051/agro:2006011 Kolb W, Martin P (1985) Response of plant roots to inoculation with Azospirillum Brasilense and to application of indole acetic acid. In: Klingmüller W (ed) Azospirillum III. Springer, Berlin, pp 215–221

10

Associative Nitrogen Fixers- Options for Mitigating Climate Change

235

Ladha JK, Tirol-Padre A, Reddy CK, Cassman KG, Verma S, Powlson DS, Kessel CV, Richter DB, Chakraborty D, Pathak H (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 Ladha JK, Peoples MB, Reddy PM, Biswas JC, Bennett A, Jat ML, Krupnik TJ (2022) Biological nitrogen fixation and prospects for ecological intensification in cereal-based cropping systems. Field Crop Res 283:108541. https://doi.org/10.1016/j.fcr.2022.108541 Latef AAHA, Alhmad MFA, Kordrostami M, Abo-Baker ABAE, Zakir A (2020) Inoculation with Azospirillum lipoferum or Azotobacter chroococcum reinforces maize growth by improving physiological activities under saline conditions. J Plant Growth Regul 39:1293–1306 Mahmud K, Panday D, Mergoum A, Missaoui A (2021) Nitrogen losses and potential mitigation strategies for a sustainable agroecosystem. Sustainability 13:2400. https://doi.org/10.3390/ su13042400 Martínez-Dalmau J, Berbel J, Ordóñez-Fernández R (2021) Nitrogen fertilization. A review of the risks associated with the inefficiency of its use and policy responses. Sustainability 13:5625. https://doi.org/10.3390/su13105625 Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in freeliving and plant associated symbiotic growth states. Microbiol Mol Biol Rev 65:94–121 Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbemediated mitigation in plants: the omics strategies. Front Plant Sci 8:172. https://doi.org/10. 3389/fpls.2017.00172 Mohanty P, Singh PK, Chakraborty D, Mishra S, Pattnaik R (2021) Insight into the role of PGPR in sustainable agriculture and environment. Front Sustain Food Syst 5:667150. https://doi.org/10. 3389/fsufs.2021.667150 Molina-Favero C, Creus CM, Simontacchi M, Puntarulo S, Lamattina L (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant-Microbe Interact 21:1001–1009. https://doi.org/10.1094/mpmi-21-7-1001 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 Oleńska E, Małek W, Wójcik M, Swiecicka I, Thijs S, Vangronsveld J (2020) Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: a methodical review. Sci Total Environ 743:140682. https://doi.org/10.1016/j. scitotenv.2020.140682. Epub 2020 Jul 7 Olivares J, Bedmar EJ, Sanjuán J (2013) Biological nitrogen fixation in the context of global change. Mol Plant-Microbe Interact 26:486–494. https://doi.org/10.1094/MPMI-12-120293-CR Orozco-Mosqueda MC, Glick BR, Santoyo G (2020) ACC deaminase in plant growth-promoting bacteria (PGPB): an efficient mechanism to counter salt stress in crops. Microbiol Res 235: 126439. https://doi.org/10.1016/j.micres.2020.126439 Pade N, Hagemann M, Pade N, Hagemann M (2014) Salt acclimation of cyanobacteria and their application in biotechnology. Life 5:25–49. https://doi.org/10.3390/life5010025 Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75:1143–1150. https://doi.org/10.1007/s00253-007-0909-9 Puente ME, Bashan Y, Li CY, Lebsky VK (2004) Microbial populations and activities in the rhizosphere of rockweathering desert plants. Root colonisation and weathering of igneous rocks. Plant Biol 6:629–642. https://doi.org/10.1055/s-2004-821100 Reis VM, Baldani VLD, Baldani JI (2015) Isolation, identification and biochemical characterization of Azospirillum spp., and other nitrogen-fixing bacteria. In: Cassán FD, Okon Y, Creus CM (eds) Handbook for Azospirillum. Springer, Switzerland, pp 3–26

236

M. Grover et al.

Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555. https://doi.org/10.1007/s00114-004-0566-0 Rodriguez JS, Suárez R, Jesús Caballero JM, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59. https://doi.org/10.1111/j.1574-6968.2009.01614.x Roesser M, Müller V (2001) Osmoadaptation in bacteria and archaea: common principles and differences. Environ Microbiol 3:743–754. https://doi.org/10.1046/j.1462-2920.2001.00252.x Rojas-Tapias D, Moreno-Galván A, Pardo-Díaz S, Obando M, Rivera D, Bonilla R (2012) Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl Soil Ecol 61:264–272. https://doi.org/10.1016/j.apsoil.2012.01.006 Rosenblueth M, Ormeño-Orrillo E, López-López A, Rogel MA, Reyes-Hernández BJ, MartínezRomero JC, Reddy PM, Martínez-Romero E (2018) Nitrogen fixation in cereals. Front Microbiol 9:1794. https://doi.org/10.3389/fmicb.2018.01794 Saeed M, Ilyas N, Mazhar R, Bibi F, Batool N (2016) Drought mitigation potential of Azospirillum inoculation in canola (Brassica napus). J Appl Bot Food Qual 278:270–278. https://doi.org/10. 5073/JABFQ.2016.089.035 Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30 Sandhya V, SkZ A, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30. https://doi.org/10.1007/s10725-010-9479-4 Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 62:21–30 Sangwan S, Grover M, Prasanna R, Nain L (2021) Biofertilizers as an integral component of integrated nutrient management for revitalizing Indian agriculture. Indian J Fertil 17:398–408 Sarma RK, Saikia R (2014) Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 377:111–126 Sen S, Chandrasekhar CN (2014) Effect of PGPR on growth promotion of rice (Oryza sativa L.) under salt stress. Asian J Plant Sci Res 4:62–67 Shao HB, Chu LY, Wu G, Zhang JH, Lu ZH, Hu YC (2007) Changes of some anti-oxidative physiological indices under soil water deficits among 10 wheat (Triticum aestivum L.) genotypes at tillering stage. Colloids Surf B Biointerfaces 54:143–149. https://doi.org/10. 1016/j.colsurfb.2006.09.004 Shirinbayan S, Khosravi H, Malakouti MJ (2019) Alleviation of drought stress in maize (Zea mays) by inoculation with Azotobacter strains isolated from semi-arid regions. Appl Soil Ecol 133: 138–145 Simova-Stoilova L, Vassileva V, Petrova T, Tsenov N, Demirevska K, Feller U (2006) Proteolytic activity in wheat leaves after drought stress and recovery. Gen Appl Plant Physiol Spec 91-100: 1. https://doi.org/10.1016/j.plaphy.2009.11.003 Tilak KVBR, Subba Rao NS (1987) Association of Azospirillum brasilense with pearl millet (Pennisetum americanum (L.) Leeke). Biol Fert Soil 4:97–102. https://doi.org/10.1007/ BF00280358 Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117. https://doi.org/10.1016/j. plaphy.2015.11.001 Tripathi AK, Mishra BM, Tripathi P (1998) Salinity stress responses in the plant growth promoting rhizobacteria. Azospirillum spp. J Biosci 23:463–471. https://doi.org/10.1007/BF02936140 Ullah A, Bano A, Khan N (2021) Climate change and salinity effects on crops and chemical communication between plants and plant growth-promoting microorganisms under stress. Front Sustain Food Syst 5:618092. https://doi.org/10.3389/fsufs.2021.618092

10

Associative Nitrogen Fixers- Options for Mitigating Climate Change

237

van Dommelen A, Vanderleyden J (2007) Associative nitrogen fixation. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 179–192. https://doi. org/10.1016/B978-044452857-5.50013-8 Venkateswarlu B, Shanker AK (2009) Climate change and agriculture: adaptation and mitigation strategies. Indian J Agron 54:226–230 Vurukonda SSKP, Sandhya V, Manjari S, 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 Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4. https://doi.org/10.1016/j.tplants.2008.10.004

Trichoderma-Based Bioinoculant: A Potential Tool for Sustainable Rice Cultivation

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Sulistya Ika Akbari, Nur Syafikah Abdullah, Nandang Permadi, Nia Rossiana, Nurul Shamsinah Mohd Suhaimi, Norman Uphoff, and Febri Doni

Abstract

Rice is the staple food for more than 3.5 billion of the world’s population, especially in Asia, where about 90% of the world’s rice is produced and consumed. However, for the last two decades, increases in rice production have stagnated in part to limitations of water for irrigation and environmental problems caused by the excessive use of chemical fertilizers and biocides. One means to increase the production of rice is the use of microbial inoculants, such as the plant-beneficial fungus, Trichoderma. The many species of this microorganism are ubiquitous plant symbionts, generally abundant in soil and in decaying wood. Their heterotrophic interactions include decomposition of organic matter, parasitism of other microorganisms, and opportunistic endophytic cohabitation within plants. Trichoderma species are used increasingly as bioinoculants because of S. I. Akbari · N. Rossiana · F. Doni (✉) Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Padjadjaran, Jatinangor, West Java, Indonesia e-mail: [email protected] N. S. Abdullah Institute for Advanced Studies, University of Malaya, Kuala Lumpur, Malaysia N. Permadi Doctorate Program in Biotechnology, Graduate School, Universitas Padjadjaran, Bandung, West Java, Indonesia N. S. M. Suhaimi Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, Kuala Lumpur, Malaysia N. Uphoff Department of Global Development, Cornell University, Ithaca, NY, USA # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_11

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their ability to establish beneficial symbiotic associations with plants, control root and foliar pathogens, facilitate nutrient uptake, increase root development, modulate plants’ genetic potentials, and aid plants in activating their systemic resistance against phytopathogens. This chapter reviews the current understanding of the roles of Trichoderma species as growth-promoting and biocontrol agents in rice cultivation. It also discusses technical challenges related to the large-scale production and use of Trichoderma-based bioinoculants. We need a better understanding of the potentials for these biofertilizers to enhance rice production and of the mechanisms involved in this if we have to derive maximum benefit from their exploitation. Keywords

Rice · Biocontrol agent · Endophytic fungi · Biofertilizers · Symbiosis · Sustainable rice cultivation

11.1

Introduction

Rice is a major cereal crop consumed as a staple food by about half of the world’s population (Chakraborty et al. 2018; Priya et al. 2019; Abdullah et al. 2021a). Two species of rice, namely, Oryza sativa L. and O. glaberrima Steudel (Lahari et al. 2020), are grown around the world on all six continents of the world where there is crop production; only not on the continent of Antarctica where there is no cultivation (Prasad et al. 2017). Record increases in rice production have been observed since the start of the Green Revolution which introduced new rice varieties and required greater use of external inputs, fertilizers, agrochemicals, and irrigation (Pingali 2012; Ray et al. 2012). In the past two decades, increases in rice yield and cultivation area have stagnated, however, due to the increasing scarcity of resources (land, water, and labor), and inefficient use of inputs, with declining marginal productivity of inputs (fertilizer, water, herbicides, insecticides, etc.) and rising costs of cultivation (Prasad et al. 2017; FAO 2020; Abdullah et al. 2021a). Global rice production increased between 1960 and 2020, from 221 to 756 million tons (FAO 2020). However, supply is not keeping up with increasing demand. Consumer demand for rice is expected to rise by a further 60% by 2050 to accommodate population growth (Fischer et al. 2014; Rahman and Zhang 2022). Thus, efforts must be made to increase the production of rice, and one of the innovations that should be considered because it is eco-friendly and low cost is the use of microbial-based inoculation, both to increase crop yield and to safeguard rice crops against biotic and abiotic stresses. Sustainable agricultural management requires methods and strategies that promote soil systems’ biological processes, decrease the need for exogenous inputs that have environmental as well as economic costs, and improve soil structure and fertility (Shaheen et al. 2014; Abd-Alhamid et al. 2015). Microbial inoculants are

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formulations, either in liquid or solid form, containing beneficial microorganisms that play essential roles in soil ecosystems and in plants (Babalola and Glick 2012; Ambrosini et al. 2015; Basu et al. 2021). Microbial-based inoculants are widely recommended as plant growth-promoting and biocontrol agents (Rojas-Sánchez et al. 2022). One subset of microbial-based inoculants is based on beneficial fungi classified as plant growth-promoting fungi (PGPF), and these are widely used as active agents for bioinoculation (Baron and Rigobelo 2022). PGPF are a broad group of non-pathogenic fungi found in plants that mediate favorable changes in plant development and health (Bent 2006; Hossain et al. 2017). The majority of the fungi classified as PGPF belong to the phylum Ascomycota, e.g., Aspergillus, Cladosporium, Colletotrichum, and Trichoderma, with a few belongings to the phyla Basidiomycota, e.g., Limonomyces, and Rhodotorula, or Zygomycota, e.g., Mucor and Rhizopus (Debbarma et al. 2021). Trichoderma, a ubiquitous, free-living filamentous fungus, is one such beneficial microorganism that has gained popularity due to its capacity for the decomposition of solid waste materials, disease control, and growth enhancement of many crops (Shobha et al. 2020; Yu et al. 2021; Akbar et al. 2022). As an effective growthpromoting biocontrol agent, Trichoderma inhibits the growth of phytopathogens mainly through competition, antibiosis, and mycoparasitism (Gajera et al. 2016). In addition, Trichoderma species can induce plant tolerance to several abiotic stresses through their involvement in root growth promotion, maintenance of nutritional uptake, and triggering protective mechanisms to minimize oxidative damage (Ahmad et al. 2015; De Padua and Dela Cruz 2021; Tegene et al. 2021). Trichoderma species when endophytically colonizing plants’ internal organs establish a molecular dialogue that positively affects plants’ growth and development (Manganiello et al. 2018; Macías-Rodríguez et al. 2018). The fungal genus Trichoderma is becoming economically important as it is now used in a wide range of crop plants as a microbial inoculant for plant growth promotion and in the management of different pathogens in various crops including rice (Harman 2019). Consequently, the search for Trichoderma species with significant antagonistic and biofertilizer potentials in rice production has increased in recent years (Abdullah et al. 2021b). This chapter discusses associations between Trichoderma and rice plants that result in improved plant growth and resistance toward biotic and abiotic stresses, and Trichoderma’s potential applications in rice cultivation as well as other benefits that should be explored for maximizing their utilization in sustainable rice cultivation. This chapter also provides insights into various aspects of Trichoderma-based bioinoculation, its prospects and constraints for large-scale production, and a roadmap to its commercialization.

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Trichoderma as a Growth-Promoting Agent in Rice Cultivation

Trichoderma species display a number of beneficial effects on plants, increasing plant growth and development and facilitating nutrient uptake (Yedidia et al. 2001). The efficacy of Trichoderma in increasing plant growth is partly due to the ability of these fungi to colonize the plant root (Harman et al. 2004). Trichoderma’s colonization of roots can improve root growth and the acquisition and storage of water in plants (Shukla et al. 2012). More robust root growth facilitates the plant’s absorption and utilization of nutrients (Cai et al. 2015; Chagas et al. 2017). As an endophytic symbiont, Trichoderma establishes direct interactions with the plant by colonizing its internal organs (Martinez-Medina et al. 2016). Many Trichoderma species can produce the auxin phytohormone indole-3-acetic acid (IAA), and their production of auxin has been suggested to play a crucial role in promoting root growth (Nicolás et al. 2014; Nieto-Jacobo et al. 2017). Trichoderma also secretes secondary metabolites and other compounds that are important in elevating plant growth and yield (Abdullah et al. 2021b). Research by Sousa et al. (2020) indicates that T. asperellum can produce swollenin, a compound that is able to facilitate the expansion of plant cell walls and increase the number of roots and rootlets, thus increasing the area of colonization, the efficiency of parasitism, and the rates of nutrient absorption by the root system. Trichoderma species are also able to facilitate nutrient acquisition in plants, resulting in increased root and shoot growth with enhanced plant greenness due to higher chlorophyll content, leading to increased carbohydrate as well as biomass production (Debnath and Saha 2020). Phosphate-solubilization capability is one important property that has commercial importance and can be exploited from the genus Trichoderma for sustainable agriculture (Tandon et al. 2020). Previously, Li et al. (2015) reported the phosphate solubilization capability of Trichoderma was through various mechanisms such as redox mediation, siderophore production, and phytase and ferric reductase activity. Fungi belonging to the genus Trichoderma have been frequently reported to be able to improve rice seedlings’ health (Swain et al. 2018). A study in Indonesia revealed that the inoculation of rice seedlings with Trichoderma significantly increased rice germination rate and vigor index as well as increased seedlings’ growth (Anhar et al. 2021). Vigorous seedlings with better root growth associated with Trichoderma treatments helped the plant to take up more nutrients and attain better plant height and biomass in the subsequent crop cycle, thereby boosting the rice production and yield. A study in Malaysia using a novel isolate growth-promoting fungus, T. asperellum SL2, has been shown to enhance rice plant canopy and root growth, tiller number, grain yield, and photosynthetic rate under greenhouse conditions (Doni et al. 2017). In a subsequent trial under field conditions, T. asperellum SL2 increased rice plants’ tillering, photosynthesis, chlorophyll content, and yields by 30% (Doni et al. 2018; Fig. 11.1). Overall, the use of Trichoderma as a biostimulant can help to increase rice production.

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Fig. 11.1 Inoculating rice plants with Trichoderma (left) resulted in increased growth and development compared to untreated control plants (right); (a) Rice plants inoculated with T. asperellum-based biofertilizer showed more robust in growth compared to untreated plants (from Doni et al. (2018), with permission). (b) T. asperellum-inoculated plants are seen to have greener leaves compared to control plants. The greener leaves indicated a better capability for photosynthesis (photo courtesy of Febri Doni). (c) T. asperellum-inoculated rice recorded larger biomass compared to control plants without T. asperellum inoculation (from Doni et al. (2017), with permission)

Further research in Nepal compared the yields of rice plants with and without Trichoderma inoculation under the System of Rice Intensification (SRI) vs. conventional cultivation methods. Trial results indicated that rice plants inoculated with Trichoderma under SRI management practices led to significant increases in rice plant growth, physiological characteristics, and yield, with favorable phenotypic responses elicited from the plants’ genotypic potential (Khadka and Uphoff 2019). Documentation regarding the contributions of Trichoderma toward the enhancement of rice plant growth and yield reported from a variety of studies is summarized in Table 11.1.

11.3

Trichoderma as a Biocontrol Agent in Rice Cultivation

The continuous use of chemical biocides to manage phytopathogens known to cause major diseases in agriculture has led to some decline in the fertility of soil systems, degradation of soil structure, and often measurable accumulations of toxic

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Table 11.1 Contributions of Trichoderma for the enhancement of rice growth and yield Trichoderma species/strains T. asperellum

Observed effects Increased root length, more aerial and root biomass

T. harzianum, T. lignorum, and T. koningii

Increased fresh weight, root mass, and leaf weight

T. harzianum, T. pinnatum, T. virens, T. asperelloides, and T. longibrachiatum T. harzianum Th-56

Increased dry mass of aerial part, root dry mass, total dry mass, and plant height

Trichoderma spp.

Enhanced plant height, leaf number, tiller number, root length, and root fresh weight Increased plant height, shoot and root length, improved shoot and root dry weight

T. harzianum strain-35

Enhanced plant height and total dry matter

References Sousa et al. (2020) Hem and Pang (2017) Chagas et al. (2017) Pandey et al. (2016) Doni et al. (2014) Gusain et al. (2014)

compounds on crops (Sharma and Singhvi 2017). An alternative method for controlling plant diseases would be by strengthening plants’ own immunity systems through the application of biocontrol agents (Gomathinayagam et al. 2012; He et al. 2021). Trichoderma species have been reported to be effective biological control agents against fungal and bacterial pathogens, nematodes, and insect pests (Ferreira and Musumeci 2021). The effective use of Trichoderma as biocontrol agents results from their ability to grow rapidly, utilize a variety of substrates, and produce a variety of extracellular lytic enzymes and many secondary metabolites (Tyśkiewicz et al. 2022).

11.3.1 Fungal Diseases Biological control methods use bioagents to suppress the growth of disease-causing pathogens in the host plants (Chinnaswami et al. 2021). As bioagents (or antagonists), Trichoderma employ several methods, which include hyperparasitism, competition for nutrients and space, antibiosis, and induction of systemic resistance in the host plants against certain pathogens so as to dominate and suppress the pathogens (Sharma et al. 2013). Several Trichoderma species are significant biocontrol agents against fungal phytopathogens (Ghorbanpour et al. 2018). Previous studies have suggested that Trichoderma can reduce sheath blight severity in rice caused by Rhizoctonia solani (Mishra et al. 2019a; Chinnaswami et al. 2021). Effector molecules released by R. solani are recognized by the receptors on the surface of Trichoderma hyphae,

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Fig. 11.2 Trichoderma hyphae (T) coiling around Rhizoctonia (R), penetrating it (P) with resulting breakdown of Rhizoctonia hyphal walls (CB). Bars: left = 5 μm; right = 10 μm. (From Neuman and Laing (2006), with permission)

which coil and suck their nutrients, leading to the destruction of the R. solani hyphae (shown in Fig. 11.2). Similarly, T. viride and T. hamatum are potential biological control agents against brown spot disease caused by Bipolaris oryzae, with an efficiency of 84% and 83%, respectively, in the soil application (Kalboush et al. 2017). According to Gomathinayagam et al. (2012), T. viride secretes gliotoxin which diminishes this particular pathogen. Furthermore, Trichoderma species are known to be potential biological control agents against bakanae disease caused by Fusarium fujikuroi in rice through their production of volatile compounds and hydrogen cyanide (HCN) (Ng et al. 2015). In addition, the production of HCN by Trichoderma species has been reported as an effective antifungal feature for soil-borne pathogen management. In this regard, Trichoderma produces cyanide that can act as a general metabolic inhibitor to avoid predation or competition without harming the host plant (Noori and Saud 2012). Further information on the capability of Trichoderma to protect rice plants against different fungal pathogens is summarized in Table 11.2.

11.3.2 Bacterial Diseases Bacterial leaf blight (BLB) is one of the most harmful bacterial diseases in rice, lowering the annual production of rice in both tropical and temperate regions of the world (Jonit et al. 2016). An alternate strategy for BLB management that is sustainable, economical, and ecologically friendly is by using biological control. Studies have reported that Trichoderma species, especially T. harzianum, are potential bioagents against BLB disease caused by Xanthomonas oryzae pv. oryzae (Abdullah et al. 2021b). Gangwar and Sinha (2014) have reported that T. harzianum reduced bacterial leaf blight disease severity following an increase in the total phenol content in rice leaves. The higher total phenolic content for a certain period in the host might be associated

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Table 11.2 Biocontrol effects of Trichoderma against fungal diseases in rice Trichoderma species/strains T. asperellum IIRRCK

T. harzianum, T. atroviride, T. longibrachiatum, T. asperellum, T. atroviride, and T. erinaceum T. harzianum BTB 022 T. harzianum

Trichoderma spp.

Fungal phytopathogens R. solani and Sclerotium oryzae R. solani

Pyricularia oryzae Sarocladium oryzae P. oryzae and R. solani

Observed effects Reduced the severity of sheath blight and stem rot

References Chinnaswami et al. (2021)

Reduced sheath blight severity and incidence

Chaudhary et al. (2020)

Reduced leaf and neck blast incidence Inhibited sheath rot pathogen growth by 65.2% Inhibited rice blast pathogen and sheath blight pathogen growth under in vitro condition

Chou et al. (2020) Bora and Ali (2019) Yadav et al. (2018)

with the activation of a plant defense mechanism. It is known that Trichoderma strains can promote the synthesis of phenolic compounds as one of the defense modes of action used by plants (Dini et al. 2021). Gangwar and Sharma (2013) reported that the combined application of T. harzianum and P. fluorescens was effective in suppressing the growth of BLB in planta. The combined application through seed treatment and foliar spray resulted in significantly lower disease intensity (just 6%) than with the application of the respective antagonists (17%). It was also found that the combined application resulted in higher rice biomass because Trichoderma and Pseudomonas showed positive interactions with other microbes which promoted growth by their synthesis of growth-promoting substances. Sutthisa (2022) screened the biocontrol capabilities of Trichoderma spp. against X. oryzae pv. oryzae isolates obtained from rice-growing areas of various states in India. Trichoderma species isolated from different locations were able to inhibit the growth of X. oryzae pv. oryzae by 90–100% under in vitro conditions. Furthermore, proteins, peptides, and low-molecular-weight substances produced by Trichoderma species were found to act as mediators for plant-defense responses (Reino et al. 2008; Sutthisa 2022). Thus, Trichoderma has a wide range of antagonistic actions that are not limited to bacterial pathogens; it can be particularly effective against fungal diseases. All of the studies discussed above highlighted that Trichoderma could be applied as an effective biocontrol agent for more profitable and sustainable rice crop cultivation, especially for controlling bacterial diseases while enhancing rice production.

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11.3.3 Nematode Pest Plant-parasitic nematodes are among the most damaging pest organisms in rice production (Le et al. 2009). One of these plant parasites, the root-knot nematode, Meloidogyne graminicola, is a severe pest in rice-producing areas of Asia (Jain et al. 2012). Plants that have been infected by this nematode display an abnormal root system, characterized by the development of galls on the roots that disrupt the uptake of water and nutrients as well as the plant’s photosynthesis capability (Kumar et al. 2017). Chemical nematicides can cause human health and environmental hazards, besides which the use of chemical nematicides is often not economical under the given field conditions (Zhang et al. 2017). Because of these limitations of chemical control, biological control has been considered a better alternative. Some studies have reported several Trichoderma species showing definite potential to control M. graminicola. For example, Kumar et al. (2017) reported that the application of a combination of neem cake, vermicompost, and Trichoderma species was superior in suppressing root gall formation on rice roots in the field. In addition, Priya (2015) reported that T. viride reduced gall formation in the root and the abundance of nematodes in root tissues, accounting for respective reductions of 89% and 60%. In another study by Le et al. (2009), Trichoderma species showed biological-control effects on nematodes by reducing galling severity by up to 38%. The direct mechanism for biological control by Trichoderma against nematodes is by destroying nematode eggs and second-phase juveniles, as well as some segments of the adult nematode population (Zin and Badaluddin 2020; Sharon et al. 2011). Metabolites and a cell wall-degrading enzyme (CWDE) produced by Trichoderma degrade nematode juveniles and eggs and inhibit the hatching of nematode eggs (TariqJaveed et al. 2021). Trichoderma also induces systemic resistance through the induction of salicylic acid (SA) and jasmonic acid (JA) defenses in the host plant (Martínez-Medina et al. 2017). Therefore, Trichoderma can be applied as an environmentally friendly alternative to controlling nematodes in rice cultivation.

11.4

Alleviation of Abiotic Stress in Rice Plant by Trichoderma

Abiotic crop stresses are major factors that negatively influence plant development and productivity (Godoy et al. 2021; Rodziewicz et al. 2014). Therefore, improving tolerance to multiple abiotic stresses will be crucial to sustaining and increasing yields for most crop plants in the future, including rice (Wang et al. 2015). Fungi belonging to the Trichoderma genus can buffer plants from abiotic stresses such as soil and water salinity, drought, and extreme temperature (Balestrini et al. 2017). In addition to these stresses, Trichoderma is also known to be able to help plants to cope with stress due to the elevated CO2 in the environment and to nutritional deficiencies (Mishra et al. 2019b).

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11.4.1 Drought Stress From an agricultural perspective, drought is a period of low precipitation, belowaverage rainfall, or higher evaporation rates that causes a loss in crop growth and productivity (Rollins et al. 2013). Trichoderma have been utilized as plant growthpromoting fungi that can induce drought tolerance in various plants, including rice (Kashyap et al. 2017). A study in India, for example, revealed that the inoculation of rice plants with Trichoderma significantly reduced the production of stress-induced metabolites such as proline, malondialdehyde (MDA), and hydrogen peroxide content while increasing total phenols in rice plants under drought stress (Shukla et al. 2012). Trichoderma inoculation induced the production of superoxide dismutase (SOD) in rice plants, which acts as scavenging enzymes to protect cells from oxidative damage in response to reactive oxygen species (ROS) accumulation under drought stress (Pandey et al. 2016). Biopriming with Trichoderma can thus aid rice plants in a multifaceted, simultaneous manner with the result of enhanced drought-stress tolerance.

11.4.2 Salinity Stress Trichoderma can also be used to abate the reduction in plant growth caused by salinity stress. For example, in saline-sodic soil in India, rice plants treated with T. harzianum showed higher length and weight of shoot and root (Rawat et al. 2012). Trichoderma produces the enzyme 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase that decreases ethylene synthesis in rice which enhances plant tolerance toward salinity stress (Zhang et al. 2016). Trichoderma species are also able to produce the majority of phytohormones that are responsive to salt tolerance; hence their association with host plants improves plant survival under salinity stress (Boamah et al. 2021). Rice seed biopriming with T. harzianum results in higher chlorophyll content, greater stomatal conductance, photosynthetic rate, proline accumulation, and membrane stability, and reduced accumulation of lipid peroxides under salt stress (Rawat et al. 2012, 2016; Yasmeen and Siddiqui 2017). T. harzianum has also been found to increase concentration of certain antioxidant enzymes, e.g., glutathione S-transferases, peroxidases, and chitinases. These enzymes act as ROS scavengers that contribute to greater membrane stability under salinity stress conditions (Gachomo and Kotchoni 2008; Hajiboland et al. 2010). All these studies indicate the capacity of Trichoderma to counteract salinity stress in rice plants and thereby to improve rice production on saline soil.

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11.4.3 Heat Stress A rise in ambient temperature above a certain threshold level for an extended period of time can disturb plant growth and development; this is referred to as heat stress (Govindaraj et al. 2018). Heat stress often reduces rice yield and quality in the major rice production areas in the Middle East (Ortiz et al. 2008). By regulating ROS production and preventing oxidative damage to plant cells, Trichoderma plays an important part in improving plant tolerance to heat stress (Tripathi et al. 2021). In addition, T. harzianum was reported to increase plants’ nutrient uptake at high soil temperatures. The availability of these plant nutrients may be caused by a rise in soil temperature, which boosts mineralization rates by stimulating microbial activity or by the breakdown of organic materials in the soil (Hossain et al. 2021). The ability of Trichoderma to increase the availability of growth nutrients under increasing soil temperatures can be significant for the agricultural sector amid climate change.

11.4.4 Elevated CO2 Conditions The level of atmospheric CO2 is predicted to reach a level of 550 ppm in the next 40 to 50 years, depending on how quickly greenhouse gases are—or are not—kept under control (IPCC 2014). Trichoderma inoculation can help rice plants survive under higher CO2 conditions. It was reported that under elevated CO2 concentrations, T. reesei-inoculated rice showed a higher rate of photosynthesis, greater stomatal conductance, and a higher rate of water transpiration (Mishra et al. 2019b). Trichoderma alters rice leaf transpiration and stomatal apertures via an abscisic acid-dependent mechanism (Contreras-Cornejo et al. 2015a). Furthermore, Trichoderma can enhance rice root development, resulting in better uptake of water along with other essential nutrients required for growing more efficiently under CO2 stress conditions (Mishra et al. 2019b).

11.4.5 Nutrient Deficiency Stress Impaired growth in rice plants can be caused by insufficient nutrient availability in soil, which eventually affects rice yield (Miller and Welch 2013). Trichoderma as growth-promoting fungi can increase rice plant growth by producing various substances that encourage nutrient absorption such as phosphatase, phytase, and nitrogenase enzymes (Abdullah et al. 2021b). For example, inoculation of T. reesei MTCC5659 increased micronutrients and macronutrient uptake under nutrientdeficient conditions in rice (Singh et al. 2019). Trichoderma species are able to solubilize mineral nutrients that are available in limited quantities in the soil through activities of chelation and reduction (Harman et al. 2004), as well as by enhancing the total of rice roots’ absorptive surface, which results in higher uptake and translocation of nutrients in the rice plant (Samolski et al. 2012).

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In the context of deficiency of essential macronutrients such as nitrogen, Trichoderma species have the ability to enhance plants’ nitrogen use efficiency (NUE) by the allocation and reuse of nitrogen, along with greater nitrogen uptake, which results in better plant growth (Brotman et al. 2012; Singh et al. 2019). Hence, Trichoderma treatment can balance macronutrient absorption and efficiency, enabling plants to more easily use macronutrients in various environmental conditions.

11.5

Understanding and Gaining from Molecular Trichoderma-Rice Plant Interactions

Trichoderma species can employ various strategies to establish a mutually advantageous connection with plants as opportunistic and avirulent plant symbionts (Alfiky and Weisskopf 2021). Trichoderma species produce elicitor molecules that permeate into the rhizosphere of plants in soil, and plants respond to those symbiotic signals by generating signaling molecules of their own that initiate beneficial fungi–plant interactions which lead to the alteration of plants’ genetic potential (Akiyama et al. 2005; Contreras-Cornejo et al. 2015b). A study by Malaysian researchers revealed that inoculation of rice seedlings with T. asperellum SL2 significantly upregulated many genes related to root development, root morphogenesis, and leaf development (Doni et al. 2019). Furthermore, Bashyal et al. (2021) have reported that T. harzianum is associated with better rice growth due to enhanced expression of proteins that are involved in growth promotion such as carbohydrate-binding module family protein, glycoside hydrolase, and polysaccharide lyase. In addition, rice plants treated with T. harzianum have shown an increase in phytohormone-related proteins, such as auxin-responsive protein and gibberellin oxidase protein. Through gene modulation, Trichoderma can also improve plants’ photosynthetic efficiency (Harman et al. 2021). A study by Doni et al. (2019) revealed that the inoculation of rice plants with T. asperellum SL2 significantly enhanced a number of upregulated genes that are linked to stomatal development and chlorophyll biosynthesis and also of more than 150 genes related to photosynthesis in rice plants. Regarding the capacity of Trichoderma to function as a biocontrol agent and abiotic stress-reliever, Trichoderma are able to increase disease resistance and abiotic stress tolerance in rice plants through their modulation of various signaling networks in rice plants (Alfiky and Weisskopf 2021). For instance, the interaction between T. asperellum with rice plants resulted in the upregulation of the genes that are involved in systemic acquired resistance (SAR) and induced systemic resistance (ISR) signaling, such as JIOsPR10 (which encodes a different type of PR10 protein), LOX-RLL (a lipoxygenase gene), and PR1b (encodes a pathogenesis-related protein class 1) (Sousa et al. 2020). Under drought stress, rice plants treated with T. harzianum showed that different genes that encode aquaporin and dehydrin were upregulated, and some were downregulated (Pandey et al. 2016). More recent research by Bashyal et al. (2021)

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on a biopriming treatment using T. harzianum on rice plants under drought-stress conditions showed that there was an increase in the expression of genes responsible for photosynthesis. Among the highly upregulated genes were Os04g0414700 (a photosystem I subunit O-related gene), Os08g0119800 (a chloroplast-related gene), and Os04g0490800 (a phosphoglycolate phosphatase-related gene). All these results have shown a remarkable influence on plants’ cellular and molecular capacities associated with endophytic colonization by Trichoderma. This beneficial fungus appears to be a key factor in inducing the beneficial expression of rice plants’ genetic potential. Figure 11.3 summarizes the molecular interactions between rice plants and Trichoderma.

11.6

Scaling Up the Use of Trichoderma Inoculants for Sustainable Rice Cultivation

The application of Trichoderma inoculants for maintaining soil quality and promoting rice yield is now proposed as an effective method for enhancing rice production in a more ecological and sustainable manner, as discussed above. However, for the most part, Trichoderma inoculants need to be mass-produced and distributed commercially, so that farmers can use this bioproduct on a large scale. Farmer production of their own inoculants is possible, as discussed below, but it is unlikely ever to match commercial culturing and distribution.

11.6.1 Industrial-Scale Production To produce reliable Trichoderma inoculants, it is first necessary to isolate and identify effective Trichoderma species from the rhizosphere (Martínez-Medina et al. 2014). Furthermore, in vitro screening needs to be carried out to determine the important characteristics of the fungus, such as its ability to dissolve phosphate and produce phytohormones (Tomer et al. 2017). Another criterion for selecting Trichoderma strains that are beneficial to plants is their ability to colonize roots (Hermosa et al. 2012). The selected isolates are then tested in planta under actual field conditions (Ortuño et al. 2013). After being evaluated, a large-scale multiplication of Trichoderma bioinoculant was carried out, namely, production using liquid or solid fermentation techniques (Kumar et al. 2014). Solid-state fermentation is more similar to the natural environment than liquidstate fermentation, and many species of Trichoderma can successfully produce spores by solid-state fermentation (Singhania et al. 2009). Trichoderma produces three kinds of propagules such as hyphae, chlamydospores, and conidia which can be used as a “starter” inoculum for mass-producing Trichoderma-based inoculant (Singhania et al. 2009; Sachdev et al. 2018). The preparation in the production laboratory is the first step for industrial-scale production of Trichoderma-based bioinoculants, in which various initial stages are carried out, including optimization of culture medium and growth factors,

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Fig. 11.3 Interactions between rice plant and Trichoderma; various effector molecules are released by Trichoderma to initiate mutualistic associations with rice plants. The effector molecules secreted by Trichoderma are recognizable to rice receptor proteins. After recognizing and transducing these fungal signals, many genes that are involved in physiological and molecular functioning are altered in the rice roots, and then the Trichoderma ascend within the plant into more rice tissues where they live symbiotically, still affecting plant gene expression. For direct mechanisms in the soil, Trichoderma species are able to mediate nutrient acquisition and protect rice plants from pathogenic microbes and pests

preparation of cultures, an inspection of samples in process, analysis of harvested bioinoculants, and analysis of finished products (Prakash and Basu 2020; Teixidó et al. 2022).

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In the laboratory “shake-flask” study, the growth of Trichoderma is usually monitored on a small scale, and then the growth conditions are optimized in a laboratory bioreactor and continued for scale production in a pilot plant bioreactor to determine its progress. However, it should be noted that the biocontrol potential of Trichoderma isolates may differ, where commonly biocontrol activities are successful at an initial scale and show excellent results in vivo but fail to replicate their properties on a large scale or field conditions (Keswani et al. 2016). This problem can be overcome by selecting superior strains and increasing their efficiency with biotechnological steps. At an advanced stage, scaling up the Trichoderma production process requires precision and zero deviation to optimize the output from pilot scale to commercial scale (Prakash and Basu 2020). Many fermentation modes were used to scale up the production of microbial cells density such as batch and fed-batch modes (Elsallam et al. 2021). However, before Trichoderma products could be successfully commercialized, there are some limitations and challenges that would need to be overcome such as production technology, developmental costs, regulation barrier, and large-scale application (Keswani et al. 2016; Elsallam et al. 2021; Mulatu et al. 2021). Another important factor in the mass production of Trichoderma is product storage. In most cases, storage temperatures are less than 4 °C with the maximum storage period being less than a year. Therefore, the production cycle should be repeated every year (Abdullah et al. 2021b; Singh and Nautiyal 2012). Hence, it is necessary to maintain good strains that support increased shelf life or organic formulations that support maximum shelf life with low levels of contaminants for the successful production of Trichoderma bioinoculants (Harman 2019). Although different Trichoderma-based products have been developed and marketed worldwide as biocontrol agents and bioinoculants (Woo et al. 2014), only a few such products are registered and most are marketed only within farmer communities (Keswani et al. 2016). This happened because the registration procedures are complicated in certain countries. The main reason that biological control agents are less demanded in Europe than the other parts of the world is that the registration process is long and costly, even when the active principle is generally regarded as being safe (Woo et al. 2014). Therefore, the regulatory system needs huge adjustments to facilitate the registration and commercialization of biological control agents. While a large proportion of the commercial products contain individual Trichoderma species, others contain mixtures of known and unknown species of the genus, sometimes in combination with other beneficial microorganisms (Abdullah et al. 2021b; Mulatu et al. 2021). Although many studies showed the superiority of products containing a consortium of microbes, quality assurance needs a careful inspection in terms of cultural methods, mass production, and microbial composition in the product, as well as quality development for registration of the product (Jain et al. 2013; Keswani et al. 2016). The development of Trichoderma as a reliable commercialized product is also tedious, laborious, time-consuming, and expensive (Harman 2019; Prakash and Basu 2020). Research and knowledge on the fungus gained by researchers are not

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Fig. 11.4 Strategies for industrial-scale production of Trichoderma. (a) Lab-scale optimization; (b) Pilot-plant optimization; (c) Large-scale field testing; (d) Production, operation, and integration; (e) Industrial plant-scale production; (f) Quality control; (g) Commercialization (redrawn from Abdullah et al. 2021b), the journal does not require permission to use materials)

enough to have a marketable product. Thus, efforts targeted at addressing these problems will facilitate commercialization and increase the accessibility to bioproducts derived from this versatile fungal genus (Fig. 11.4).

11.6.2 Farmer-Scale Production For farmer-scale production, Trichoderma propagules can be produced in liquid or by solid fermentation. In both cases, a major consideration in the choice of organic

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Table 11.3 Reports on the effects of Trichoderma using various delivery media in rice cultivation Trichoderma species/ strains T. harzianum

T. asperellum IIRRCK

Delivery media Compost of a mix of cow dung, poultry refuse, water, hyacinth, vegetable waste, sawdust, maize bran, and molasses Sorghum grains

T. harzianum AS12–2

Broom sorghum grain, rice husk, rice straw, sugar beet pulp, and cow dung

T. koningii, T. hamatum, T. virens, T. delyenses, T. viride, and T. harzianum T. asperellum SL2

Corn kernels

Trichoderma spp.

Composted straw

T. asperellum T12

Rice hull

Corn kernels

Roles in rice production Increased nutrient uptake under elevated soil temperature

References Hossain et al. (2021)

Reduced the severity of sheath blight and stem rot Effective in controlling the rice sheath blight disease Reduced brown spot percentage and severity

Chinnaswami et al. (2021)

Increased rice growth, physiological traits, and productivity Increased ISR and rice productivity Reduce sheath blight infection

Doni et al. (2017)

Naeimi et al. (2020)

Kalboush et al. (2017)

Simarmata et al. (2016) Chen et al. (2015)

materials or media for the multiplication and application of the inoculant is their cost relative to their efficacy (Ortuño et al. 2013). These organic materials can be obtained from crop residue, livestock waste, industrial waste, and any organic material that is economical to produce Trichoderma on a large-scale (Harman 2019). Any substrate used to produce Trichoderma in large quantities must be cost-effective and capable of producing huge amounts of biomass and available propagules (Parkash and Saikia 2015). Various environmental factors such as moisture content, temperature, pH, and oxygen levels affect the quality of a Trichoderma bioinoculant produced from the fermentation of organic materials (Singh and Nautiyal 2012). Various studies have reported on the use of low-cost media such as livestock wastes, rice straw, or molasses to develop Trichoderma-based bioproducts in the farmer-scale level as shown in Table 11.3. By producing and using Trichoderma-based bioinoculant, farmers can reduce their dependency on the chemical fertilizers and biocides commonly used in rice farming systems. As a model, a simple and farmer-friendly method for producing Trichoderma-based bioinoculant using corn kernels as media has been field-tested in

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Fig. 11.5 A simple protocol in producing Trichoderma-based bioinoculant using corn kernels as delivery media (redrawn from Doni et al. 2018, with permission)

Malaysia (Doni et al. 2018). According to that study, the corn-kernel formulations of Trichoderma have a shelf-life of 4 months. Simple pressure cookers can be used to provide household-level sterilization, so costly equipment is not required. Corn kernels, an inexpensive material for delivery medium, provide a sufficient amount of nutrition (in the form of carbohydrates, proteins, minerals, and amino acids) for Trichoderma to grow (El-Fattah et al. 2013; Kim et al. 2008). The method for producing Trichoderma-based bioinoculant is shown in Fig. 11.5. This method not only helps farmers to reduce the use of chemical fertilizers but can also generate wider environmental and economic benefits.

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Conclusion

Over decades, many technological and technical innovations have been introduced to boost the production of rice. Unfortunately, some of these methods have detrimental impacts on the environment. Natural and biological approaches that use beneficial microorganisms such as Trichoderma offer opportunities for increasing rice production in eco-friendly ways. Trichoderma has excellent potential as a plant growth-promoting agent for rice. It enhances plant growth and health by increasing the growth of roots and by producing phytohormones, secondary metabolites, and volatile organic compounds, and making nutrients needed by rice plants soluble. As a plant symbiont, Trichoderma enhances plants’ resistance to biotic and abiotic stresses by colonizing plant roots and then reprogramming plants’ gene expression. Trichoderma’s antagonistic mode of action and suppression of plant pathogens through mycoparasitism, competition, and antibiosis is beneficial in rice disease control and management. Accordingly, bioinoculants like Trichoderma represent an alternative to conventional practices for disease management worldwide. Resolving operational problems with regard to fermentation, formulation, modes and media of delivery, and patent protection are important factors for the commercialization of potent strains. Possibilities for farmer production of their own bioinoculants are just starting to be explored, but some initial experience with this has shown that Trichoderma is amenable to such use. An improved understanding of the various mechanisms involved in Trichoderma’s life cycle is important to develop practicable products for a sustainable agriculture sector. Acknowledgments This work was funded by Universitas Padjadjaran through Academic Leadership Grant (ALG), contract number 2203/UN6.3.1/PT.00/2022 awarded to Nia Rossiana, and Riset Percepatan Lektor Kepala (RPLK), contract number 1549/UN6.3.1/PT.00/2023 awarded to Febri Doni. Conflicts of Interest The authors declare no conflict of interest.

References Abd-Alhamid HHSA, Haggag LF, Hassan AM (2015) Effect of mineral and bio-fertilization on vegetative growth, leaf mineral contents and flowering of Manzanillo olive trees. Int J Chem Technol Res 8:51–61 Abdullah M, Zakaria N, Ahmad-Hamdani MS, Juraimi AS (2021a) Water scarcity in the rice fields: a review in water and weed interaction in the lowland rice production areas. Plant Arch 21: 1707–1712 Abdullah NS, Doni F, Mispan MS et al (2021b) Harnessing Trichoderma in agriculture for productivity and sustainability. Agronomy 11:2559 Ahmad P, Hashem A, Abd-Allah EF et al (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L.) through antioxidative defense system. Front Plant Sci 6:868

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Akbar M, El-Sabrout AM, Shokralla S et al (2022) Preservation and recovery of metal-tolerant fungi from industrial soil and their application to improve germination and growth of wheat. Sustainability 14:1–17 Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827 Alfiky A, Weisskopf L (2021) Deciphering Trichoderma–plant–pathogen interactions for better development of biocontrol applications. J Fungi 7:1–18 Ambrosini A, de Souza R, LMP P (2015) Ecological role of bacterial inoculants and their potential impact on soil microbial diversity. Plant Soil 4001(400):193–207 Anhar A, Putri DH, Advinda L et al (2021) Molecular characterization of Trichoderma strains from West Sumatera, Indonesia and their beneficial effects on rice seedling growth. J Crop Sci Biotechnol 24:441–448 Babalola OO, Glick BR (2012) The use of microbial inoculants in African agriculture: current practice and future prospects. J Food Agric Environ 10:540–549 Balestrini R, Chitarra W, Fotopoulos V (2017) Soil biological communities and ecosystem resilience. Soil Biol Communities Ecosyst Resil 1:191–207 Baron NC, Rigobelo EC (2022) Endophytic fungi: a tool for plant growth promotion and sustainable agriculture. Mycology 13:39–55 Bashyal BM, Parmar P, Zaidi NW, Aggarwal R (2021) Molecular programming of droughtchallenged Trichoderma harzianum-bioprimed rice (Oryza sativa L.). Front Microbiol 12:1–14 Basu A, Prasad P, Das SN et al (2021) Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13:1–20 Bent E (2006) Induced systemic resistance mediated by plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF). In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer Science, New York, NY, pp 225–259 Boamah S, Zhang S, Xu B et al (2021) The role of Trichoderma species in plants response to salt stress. Asian J Res Crop Sci 6:28–43 Bora B, Ali MS (2019) Evaluation of microbial antagonists against Sarocladium oryzae causing sheath rot disease of rice (Oryzae sativa L.). Int J Curr Microbiol Appl Sci 8:1755–1760 Brotman Y, Lisec J, Méret M et al (2012) Transcript and metabolite analysis of the Trichodermainduced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158:139–146 Cai F, Chen W, Wei Z et al (2015) Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant Soil 388:337–350 Chagas LFB, Colonia BSO, Rodrigues G et al (2017) Rice growth influence by Trichoderma spp. with natural phosphate fertilization under greenhouse conditions. Int J Dev Res 07:13147– 13152 Chakraborty P, Khuman SN, Kumar B, Snow D (2018) Sources of organochlorine pesticidal residues in the paddy fields along the ganga-brahmputra river basin: implications for longrange atmospheric transport. In: Varma A, Hashmi M (eds) Soil biology environmental pollution of paddy soils. Soil biology, vol 53. Springer, Cham, pp 69–83 Chaudhary S, Sagar S, Lal M et al (2020) Biocontrol and growth enhancement potential of Trichoderma spp. against Rhizoctonia solani causing sheath blight disease in rice. J Environ Biol 41:1034–1045 Chen LH, Zhang J, Shao XH et al (2015) Development and evaluation of Trichoderma asperellum preparation for control of sheath blight of rice (Oryza sativa L.). Biocontrol Sci Tech 25:316– 328 Chinnaswami K, Mishra D, Miriyala A et al (2021) Native isolates of Trichoderma as bio-suppressants against sheath blight and stem rot pathogens of rice. Egypt J Biol Pest Control 31:12 Chou C, Castilla N, Hadi B et al (2020) Rice blast management in cambodian rice fields using Trichoderma harzianum and a resistant variety. Crop Prot 135:104864

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Trichoderma-Based Bioinoculant: A Potential Tool for. . .

259

Contreras-Cornejo HA, Macías-Rodríguez L, Vergara AG, López-Bucio J (2015a) Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. J Plant Growth Regul 34:425–432 Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2015b) Fungal biomolecules in plant growth promotion. In: Fungal biomolecules: sources, applications and recent developments. pp 345–362 De Padua JC, Dela Cruz TEE (2021) Isolation and characterization of nickel-tolerant trichoderma strains from marine and terrestrial environments. J Fungi 7:1–15 de Sousa TP, Chaibub AA, da Silva GB, de MCC F (2020) Trichoderma asperellum modulates defense genes and potentiates gas exchanges in upland rice plants. Physiol Mol Plant Pathol 112:101561 Debbarma M, Rajesh T, Devi RKT et al (2021) Morphological characterization of plant growth promoting fungi (PGPF) isolated from maize rhizosphere in Meghalaya. Pharm Innov J 10:570– 575 Debnath S, Saha AK (2020) Potential of Trichoderma species as biofertilizer and biological control on Oryza sativa L. cultivation. Biotecnol Veg 20:1–16 Dini I, Pascale M, Staropoli A et al (2021) Effect of selected Trichoderma strains and metabolites on olive drupes. Appl Sci 11:8710 Doni F, Isahak A, Zain CRCM, Yusoff MW (2014) Physiological and growth response of rice plants (Oryza sativa L.) to Trichoderma spp. inoculants. AMB Express 4:1–7 Doni F, Zain CRCM, Isahak A et al (2017) Relationships observed between Trichoderma inoculation and characteristics of rice grown under system of rice intensification (SRI) vs. conventional methods of cultivation. Symbiosis 72:45–59 Doni F, Zain CRCM, Isahak A et al (2018) A simple, efficient, and farmer-friendly Trichodermabased biofertilizer evaluated with the SRI Rice management system. Org Agric 8:207–223 Doni F, Fathurrahman F, Mispan MS et al (2019) Transcriptomic profiling of rice seedlings inoculated with the symbiotic fungus Trichoderma asperellum SL2. J Plant Growth Regul 38: 1507–1515 El-Fattah DAA, Eweda WE, Zayed MS, Hassanein MK (2013) Effect of carrier materials, sterilization method, and storage temperature on survival and biological activities of Azotobacter chroococcum inoculant. Ann Agric Sci 58:111–118 Elsallam MEA, El-Moslamy SH, El-Al AA, Zahran HF (2021) Scaling-up production of costeffective and eco-friendly bio-fertilizer and its application on barley green fodder via IoT hydroponic system. J Genet Eng Biotechnol 19:1–12 FAO (2020) Crops and livestock products; https://www.fao.org/faostat/en/#data/QCL/visualize. Accessed 8 May 2022 Ferreira FV, Musumeci MA (2021) Trichoderma as biological control agent: scope and prospects to improve efficacy. World J Microbiol Biotechnol 37:1–17 Fischer T, Byerlee D, Edmeades G (2014) Crop yields and global food security: will yield increase continue to feed the world? ACIAR monograph no. 158. Australian Centre for International Agricultural Research, Canberra Gachomo EW, Kotchoni SO (2008) The use of Trichoderma harzianum and T. viride as potential biocontrol agents against peanut microflora and their effectiveness in reducing aflatoxin contamination of infected kernels. Biotechnology 7:439–447 Gajera HP, Hirpara DG, Katakpara ZA et al (2016) Molecular evolution and phylogenetic analysis of biocontrol genes acquired from SCoT polymorphism of mycoparasitic Trichoderma koningii inhibiting phytopathogen Rhizoctonia solani Kuhn. Infect Genet Evol 45:383–392 Gangwar OP, Sharma P (2013) Efficacy of seed bio-priming and foliar spray with Trichoderma harzianum and Pseudomonas fluorescens in plant growth promotion and bacterial leaf blight management in rice. J Eco-friendly Agric 8:181–164 Gangwar GP, Sinha AP (2014) Effect of fungal and bacterial bioagent application on total phenolic content in rice leaves pre-inoculated with Xanthomonas oryzae pv. Oryzae (Uyeda and Ishiyama) Dowson. J Appl Nat Sci 6:254–257

260

S. I. Akbari et al.

Ghorbanpour M, Omidvari M, Abbaszadeh-Dahaji P et al (2018) Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol Control 117:147–157 Godoy F, Olivos-Hernández K, Stange C, Handford M (2021) Abiotic stress in crop species: improving tolerance by applying plant metabolites. Plan Theory 10:1–19 Gomathinayagam S, Persaud SA, Rekha M, Shanmugaiah V (2012) Comparative study of biological agents, Trichoderma harzianum and Trichoderma viride for controlling brown spot disease in rice. J Biopest 5:28–32 Govindaraj M, Pattanashetti SK, Patne N, Kanatti AA et al (2018) Breeding cultivars for heat stress tolerance in staple food crops. In: Çiftçi YÖ (ed) Next generation plant breeding. IntechOpen Limited, London, pp 45–74 Gusain YS, Singh US, Sharma AK (2014) Enhance activity of stress related enzymes in rice (Oryza sativa L.) induced by plant growth promoting fungi under drought stress. African J Agric Res 9: 1430–1434 Hajiboland R, Aliasgharzad N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327 Harman GE (2019) 50 years of development of beneficial microbes for sustainable agriculture and society: progress and challenges still to be met—part of the solution to global warming and “hothouse earth”. In: Sing P, Gupta VJ, Ratna P (eds) Interventions in agriculture and the environment. Springer, Singapore, pp 1–28 Harman GE, Howell CR, Viterbo A et al (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56 Harman G, Doni F, Khadka R, Uphoff N (2021) Endophytic strains of Trichoderma increase plants photosynthetic capability. J Appl Microbiol 130:529–546 He DC, He MH, Amalin DM et al (2021) Biological control of plant diseases: an evolutionary and eco-economic consideration. Pathogens 10:1–15 Hem R, Pang A (2017) Bio-stimulant effects of Trichoderma spp. on rice (Oryza sativa L.): an initial evaluation using a strongly acidic clay loam soil. Am J Sustain Agric 11:42–48 Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25 Hossain MM, Sultana F, Islam S (2017) Plant growth-promoting fungi (PGPF): phytostimulation and induced systemic resistance. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer Nature, Singapore, pp 135–191 Hossain MS, Khan MHR, Islam MS (2021) Impacts of heat stress on mineral nutrition of boro rice cultivar (BR 19) as influenced by the indigenous organic fertilizers. Dhaka Univ J Biol Sci 30: 125–131 IPCC (2014) Climate change 2014: mitigation of climate change. Contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge Jain RK, Khan MR, Kumar V (2012) Rice root-knot nematode (Meloidogyne graminicola) infestation in rice. Arch Phytopathol Plant Prot 45:635–645 Jain A, Singh A, Singh BN et al (2013) Biotic stress management in agricultural crops using microbial consortium. In: Maheshwari D (ed) Bacteria in agrobiology: disease management. Springer, Berlin, Heidelberg, pp 427–448 Jonit NQ, Low YC, Tan GH (2016) Xanthomonas oryzae pv. Oryzae, biochemical tests, rice (Oryza sativa), bacterial leaf blight (BLB) disease, Sekinchan. J Appl Environ Microbiol 4:63–69 Kalboush Z, Hassan A, Saleh M (2017) Efficacy of Trichoderma spp as biocontrol agents against rice brown spot disease and biochemical approaches. J Plant Prot Pathol 8:677–686 Kashyap PL, Rai P, Srivastava AK, Kumar S (2017) Trichoderma for climate resilient agriculture. World J Microbiol Biotechnol 33:155 Keswani C, Sarma BK, Singh HB (2016) Synthesis of policy support, quality control, and regulatory management of biopesticides in sustainable agriculture. In: Singh H, Sarma B,

11

Trichoderma-Based Bioinoculant: A Potential Tool for. . .

261

Keswani C (eds) Agriculturally important microorganisms: commercialization and regulatory requirements in Asia. Springer, Singapore, pp 3–12 Khadka RB, Uphoff N (2019) Effects of Trichoderma seedling treatment with system of rice intensification management and with conventional management of transplanted rice. PeerJ 2019:1–22 Kim Y, Mosier NS, Hendrickson R et al (2008) Composition of corn dry-grind ethanol by-products: DDGS, wet cake, and thin stillage. Bioresour Technol 99:5165–5176 Kumar S, Thakur M, Rani A (2014) Trichoderma: mass production, formulation, quality control, delivery and its scope in commercialization in India for the management of plant diseases. African J Agric Res 9:3838–3852 Kumar D, Khilari K, Kumar N, Jain SK (2017) Integrated disease management of rice root knot nematode (Meloidogyne graminicola) through organic amendments, Trichoderma spp. and carbofuran. J Pharmacogn Phytochem 6:2509–2515 Lahari Z, Nkurunziza R, Bauters L, Gheysen G (2020) Analysis of asian rice (Oryza sativa) genotypes reveals a new source of resistance to the root-knot nematode meloidogyne javanica and the root-lesion nematode pratylenchus zeae. Phytopathology 110:1572–1577 Le HTT, Padgham JL, Sikora RA (2009) Biological control of the rice root-knot nematode Meloidogyne graminicola on rice, using endophytic and rhizosphere fungi. Int J Pest Manag 55:31–36 Li RX, Cai F, Pang G et al (2015) Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One 10: e0130081 Macías-Rodríguez L, Guzmán-Gómez A, García-Juárez P, Contreras-Cornejo HA (2018) Trichoderma atroviride promotes tomato development and alters the root exudation of carbohydrates, which stimulates fungal growth and the biocontrol of the phytopathogen Phytophthora cinnamomi in a tripartite interaction system. FEMS Microbiol Ecol 94:137 Manganiello G, Sacco A, Ercolano MR et al (2018) Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Front Microbiol 9:1966 Martínez-Medina A, Del Mar AM, Pascual JA, SCM VW (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J Chem Ecol 407(40):804–815 Martinez-Medina A, Pozo MJ, Cammue BPA, Vos CMF (2016) Belowground defence strategies in plants: the plant–Trichoderma dialogue. In: Vos C, Kazan K (eds) Belowground defence strategies in plants. Springer, Cham, pp 301–327 Martínez-Medina A, Fernandez I, Lok GB et al (2017) Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213:1363–1377 Miller BDD, Welch RM (2013) Food system strategies for preventing micronutrient malnutrition. Food Policy 42:115–128 Mishra D, Rajput RS, Zaidi NW, Singh HB (2019a) Sheath blight and drought stress management in rice (Oryza sativa) through Trichoderma spp. Indian Phytopathol 73:71–77 Mishra A, Singh SP, Mahfooz S et al (2019b) External supplement of impulsive micromanager Trichoderma helps in combating CO2 stress in rice grown under FACE. Plant Mol Biol Report 37:1–13 Mulatu A, Alemu T, Megersa N, Vetukuri RR (2021) Optimization of culture conditions and production of bio-fungicides from Trichoderma species under solid-state fermentation using mathematical modeling. Microorganisms 9:1675 Naeimi S, Khosravi V, Varga A et al (2020) Screening of organic substrates for solid-state fermentation, viability and bioefficacy of Trichoderma harzianum as12-2, a biocontrol strain against rice sheath blight disease. Agronomy 10:1258 Neumann B, Laing M (2006) Trichoderma: an ally in the quest for soil system sustainability. In: Uphoff N, Fernandes E, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P,

262

S. I. Akbari et al.

Sanginga N, Thies J (eds) Biological approaches to sustainable soil system. Taylor & Francis, Boca Raton, FL, pp 491–500 Ng LC, Ngadin A, Azhari M, Zahari NA (2015) Potential of Trichoderma spp. as biological control agents against bakanae pathogen (Fusarium fujikuroi) in rice. Asian J Plant Pathol 9:46–58 Nicolás C, Hermosa R, Rubio B et al (2014) Trichoderma genes in plants for stress tolerance- status and prospects. Plant Sci 228:71–78 Nieto-Jacobo MF, Steyaert JM, Salazar-Badillo FB et al (2017) Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front Plant Sci 8:102 Noori MSS, Saud HM (2012) Potential plant growth-promoting activity of Pseudomonas sp. isolated from paddy soil in Malaysia as biocontrol agent. J Plant Pathol Microbiol 03:2–5 Ortiz R, Sayre KD, Govaerts B et al (2008) Climate change: can wheat beat the heat? Agric Ecosyst Environ 126:46–58 Ortuño N, Castillo J, Claros M et al (2013) Enhancing the sustainability of quinoa production and soil resilience by using bioproducts made with native microorganisms. Agronomy 3:732–746 Pandey V, Ansari MW, Tula S et al (2016) Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 243:1251–1264 Parkash V, Saikia AJ (2015) Production and multiplication of native compost fungal activator by using different aubstrates and its influence on growth and development of Capsicum chinensis Jacq. “Bhut Jolokia”. Biotechnol Res Int 2015:1–7 Pingali PL (2012) Green revolution: impacts, limits, and the path ahead. Proc Natl Acad Sci U S A 109:12302–11208 Prakash V, Basu K (2020) Mass multiplication of Trichoderma in bioreactors. In: Trichoderma: agricultural applications and beyond. Springer, Cham, pp 113–126 Prasad R, Shivay YS, Kumar D (2017) Current status, challenges, and opportunities in rice production. In: Chauhan B, Jabran K, Mahajan G (eds) Rice production worldwide. Springer, Cham, pp 1–32 Priya S (2015) Biomanagement of rice root knot nematode, Meloidogyne graminicola Golden and Brichfield in aerobic rice. Int J Manag Soc Sci 3:591–598 Priya R, Nelson ARLE, Ravichandran K, Antony U (2019) Nutritional and functional properties of coloured rice varieties of South India: a review. J Ethn Foods 6:1–11 Rahman ANM, Zhang J (2022) Trends in rice research: 2030 and beyond. Food Energy Secur 27: e390 Rawat L, Singh Y, Shukla N, Kumar J (2012) Seed biopriming with salinity tolerant isolates of Trichoderma harzianum alleviates salt stress in rice: growth, physiological and biochemical characteristics. J Plant Pathol 94:353–365 Rawat L, Bisht TS, Upadhayay RG, Kukreti A (2016) Trichoderma harzianum enhancing plant growth parameters and reducing deleterious effects of natural saline-sodic soil in rice. Int J Trop Agric 34:1855–1867 Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA (2012) Recent patterns of crop yield growth and stagnation. Nat Commun 3:1293 Reino JL, Guerrero RF, Hernández-Galán R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123 Rodziewicz P, Swarcewicz B, Chmielewska K et al (2014) Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol Plant 36:1–19 Rojas-Sánchez B, Guzmán-Guzmán P, Morales-Cedeño LR et al (2022) Bioencapsulation of microbial inoculants: mechanisms, formulation types and application techniques. Appl Biosci 1:198–220 Rollins JA, Habte E, Templer SE et al (2013) Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J Exp Bot 64:3201–3212 Sachdev S, Singh A, Singh RP (2018) Optimization of culture conditions for mass production and bio-formulation of Trichoderma using response surface methodology. 3 Biotech 8:360

11

Trichoderma-Based Bioinoculant: A Potential Tool for. . .

263

Samolski I, Rincón AM, Pinzón LM et al (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158:129–138 Shaheen SA, El Taweel AA, Omar MNA (2014) Effect of inoculation by some plant growth promoting rhizobacteria (PGPR) on production of “Manzanillo” olive trees. Acta Hortic 1018: 245–254 Sharma N, Singhvi R (2017) Effects of chemical fertilizers and pesticides on human health and environment: a review. Int J Agric Environ Biotechnol 10:675–680 Sharma A, Diwevidi VD, Singh S et al (2013) Biological control and its important in agriculture. Int J Biotechnol Bioeng 4:175–180 Sharon E, Chet I, Spiegel Y (2011) Trichoderma as a biological control agent. Biol Control PlantParasitic Nematodes 1:183–201 Shobha B, Lakshmeesha TR, Ansari MA et al (2020) Mycosynthesis of ZnO nanoparticles using Trichoderma spp. isolated from rhizosphere soils and its synergistic antibacterial effect against Xanthomonas oryzae pv. Oryzae. J Fungi 6:1–19 Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Biochem 54:78–88 Simarmata T, Hersanti TT et al (2016) Application of bioameliorant and biofertilizers to increase the soil health and rice productivity. HAYATI J Biosci 23:181–184 Singh PC, Nautiyal CS (2012) A novel method to prepare concentrated conidial biomass formulation of Trichoderma harzianum for seed application. J Appl Microbiol 113:1442–1450 Singh SP, Pandey S, Mishra N et al (2019) Supplementation of Trichoderma improves the alteration of nutrient allocation and transporter genes expression in rice under nutrient deficiencies. Plant Physiol Biochem 143:351–363 Singhania RR, Patel AK, Soccol CR, Pandey A (2009) Recent advances in solid-state fermentation. Biochem Eng J 44:13–18 Sutthisa W (2022) Comparison of the antagonistic potential of the entomopathogenic bacterium Serratia nematodiphila GCSR38 with other effective microorganisms for the control of rice bacterial leaf blight. J Pure Appl Microbiol 16:557–566 Swain H, Adak T, Mukherjee AK et al (2018) Novel Trichoderma strains isolated from tree barks as potential biocontrol agents and biofertilizers for direct seeded rice. Microbiol Res 214:83–90 Tandon A, Fatima T, Anshu et al (2020) Phosphate solubilization by Trichoderma koningiopsis (NBRI-PR5) under abiotic stress conditions. J King Saud Univ Sci 32:791–798 TariqJaveed M, Farooq T, Al-Hazmi AS et al (2021) Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. J Invertebr Pathol 183:107626 Tegene S, Dejene M, Terefe H et al (2021) Evaluation of native Trichoderma isolates for the management of sugarcane smut (Ustilago scitaminea) in sugar plantations of Ethiopia. Cogent Food Agric 7:1–21 Teixidó N, Usall J, Torres R (2022) Insight into a successful development of biocontrol agents: production, formulation, packaging, and shelf life as key aspects. Horticulture 8:305 Tomer S, Suyal DC, Goel R (2017) Biofertilizers: a timely approach for sustainable agriculture. In: Choudhary DK, Varma A, Tuteja N (eds) Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 375–395 Tripathi R, Keswani C, Tewari R (2021) Trichoderma koningii enhances tolerance against thermal stress by regulating ROS metabolism in tomato (Solanum lycopersicum L.) plants. J Plant Interact 16:116–126 Tyśkiewicz R, Nowak A, Ozimek E, Jaroszuk-ściseł J (2022) Trichoderma: the current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. Int J Mol Sci 23:2329 Wang A, Yu X, Mao Y et al (2015) Overexpression of a small heat-shock-protein gene enhances tolerance to abiotic stresses in rice. Plant Breed 134:384–393 Woo SL, Ruocco M, Vinale F et al (2014) Trichoderma-based products and their widespread use in agriculture. Open Mycol J 8:71–126

264

S. I. Akbari et al.

Yadav RN, Mishra D, Zaidi NW et al (2018) Bio-control efficacy of Trichoderma spp. against the major diseases of rice (Oryzae sativa L.). Int J Agric Environ Biotechnol 11:543–548 Yasmeen R, Siddiqui ZS (2017) Physiological responses of crop plants against Trichoderma harzianum in saline environment. Acta Bot Croat 76:154–162 Yedidia I, Srivastva AK, Kapulnik Y, Chet I (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 2352(235):235–242 Yu Z, Wang Z, Zhang Y et al (2021) Biocontrol and growth-promoting effect of Trichoderma asperellum TaspHu1 isolate from Juglans mandshurica rhizosphere soil. Microbiol Res 242: 126596 Zhang F, Liu Z, Gulijimila M, Wang Y, Fan H, Wang Z (2016) Functional analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene of the biocontrol fungus Trichoderma asperellum ACCC30536. Can J Plant Sci 96:265–275 Zhang S, Gan Y, Ji W et al (2017) Mechanisms and characterization of Trichoderma longibrachiatum T6 in suppressing nematodes (Heterodera avenae) in wheat. Front Plant Sci 8:1491 Zin NA, Badaluddin NA (2020) Biological functions of Trichoderma spp. for agriculture applications. Ann Agric Sci 65:168–178

Photosynthetic Microorganisms and Their Role in Mitigating Climate Change Through C Sequestration and Plant-Soil Interactions

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Venkatesh Kokila, Bidisha Chakrabarti, and Radha Prasanna

Abstract

Cyanobacteria represent critical components of food webs, which are ubiquitous in diverse environments, and represent ideal candidates for eco-friendly and sustainable practices in agriculture, industry, and environmental management. Several species possess the ability to fix both carbon and nitrogen, as they have evolved novel environmental adaptations, such as the Ci-concentrating mechanism (CCM), which boosts the photosynthetic performance and efficiency of CO2 sequestration, even under limited CO2 levels, thereby surmounting the low efficiency of the key photosynthetic enzyme RuBisCO (Ribulose Bis-phosphate carboxylase/oxygenase). Being highly adaptive and flexible in their metabolic requirements, cyanobacteria represent ideal candidates in the future climate scenario predicted to be possessing increased levels of CO2 and high temperatures. This compilation reviews the significance of cyanobacterial adaptation(s) to sequester CO2, and their interactions with plants and soil biota to gainfully use this CO2 towards improving the quality of produce, crop yields, and soil fertility. Keywords

C-fixation · Cyanobacteria · Growth · SOC · Sugars

V. Kokila Division of Microbiology, ICAR-Indian Agricultural Research Institute (IARI), New Delhi, India B. Chakrabarti Division of Environment Science, ICAR-Indian Agricultural Research Institute, New Delhi, India R. Prasanna (✉) Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_12

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Introduction

Increasing awareness regarding CO2 emissions and awareness regarding their harmful effects has stimulated focussed research on biological CO2 reduction, as a promising, eco-sustainable approach, largely because of its potential downstream advantages (Bhola et al. 2014). In this context, photosynthetic microbes are gaining interest as agents for CO2 sequestration, because they can grow autotrophically using CO2, a greenhouse gas, and sunlight, an abundant source of energy, enabling them to successfully proliferate in a diverse range of environmental conditions (Ahmed et al. 2019). Among them, cyanobacteria and microalgae represent environment friendly inputs as they are highly adaptive and pioneering organisms. Some of these organisms can also be used as biofertilizers which leads to the reduced use of nitrogen-based fertilizers, while also enhancing plant development, yield, quality of produce, and also soil fertility across crops and environments (Renuka et al. 2018; Prasanna et al. 2021). With the increasing demands of the burgeoning population across the globe, intricately associated with the increasing demand for food security, WHO (World Health Organization) has advocated raising food productivity by 2050 to secure future requirements. Plant breeding and biotechnological interventions are already making efforts, however, nonconventional biotechnological measures, such as improving the efficiency of CO2 fixation in agriculture, can increase the food production from each hectare of agricultural land (Parry et al. 2011). Carbon is the largest and simplest component of organic matter (OM) to quantify, thereby, the measurement of Soil Organic Carbon (SOC) is used as an index in standard soil tests. Carbon sequestration using biological options is gaining interest among researchers, and from the context of agriculture, soil ecosystem services gain critical significance as they are important for regulating, sustaining, and provisioning our natural resources – soil, water, the composition of air, etc. (Olson et al. 2017). The main contributors to the SOC are linked to agricultural methods and changes in land use, and conservation agriculture is a promising option for enhancing C sequestration (Lal 2015). However, as most natural ecosystems are slowly being transformed into cultivated croplands, this intrinsic ability to systematically sequester and retain soil organic carbon (SOC) is gradually being lost (Lal 2004). Published reports on the role of carbon cycling in improving the SOC reserves suggest that the autotrophically fixed carbon due to the photosynthetic activity of the microbes and terrestrial plants are the major contributors (Berg 2011). In order to balance the energy gained by the fixation of carbon dioxide (CO2) into carbohydrates (source) through photosynthesis, a systematic transfer from the site of synthesis to regions of utilization and/or storage (sink) occurs; this dictates plant growth and development. Increase in the atmospheric CO2 concentration will increase the photosynthesis rate of plants and will also have an impact on the future global terrestrial carbon sinks (Fig. 12.1). In order to gainfully counteract CO2 emissions, land ecosystems sequester carbon rapidly through vitalizing the process of photosynthesis-mediated carbon fixation by photosynthetic flora and higher plants; this is regarded as an effective and

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Fig. 12.1 Multifarious effects of elevated CO2 on primary and secondary metabolism of photosynthetic microorganisms and plants, eCO2 elevated CO2, JA jasmonic acid, SA salicylic acid, RuBisCO ribulose-1, 5- bisphosphate carboxylase-oxygenase

environmentally friendly strategy (Tsai et al. 2017). In nature, photosynthetic microflora and plants stimulate the amount of CO2 fixed through photosynthesis, which in turn promotes efficient carbon fixation by terrestrial ecosystems to offset CO2 emissions (Tsai et al. 2017); additionally, this can also be engineered through biochemical or molecular interventions (Bhola et al. 2014). Therefore, it is crucial to implement creative ways or novel strategies to sustain crop productivity and maintain soil fertility, which can also counteract the erosion of C from soil, feed the ever-growing population globally, and reduce the carbon footprint. In this context, diazotrophic photosynthetic prokaryotes such as cyanobacteria are ideal as they modulate their photosynthetic machinery under different environmental/ nutritional conditions, through qualitative and quantitative changes in the chlorophyll, carotenoids and unique pigments – phycobilins, which are critical in supporting the photosynthetic ability in a single cell (Kumar et al. 2011a, b). Additionally, nitrogen fixation is a trait, present in several cyanobacteria which makes them useful in not only improving the fertility of soil, as the environment for growing crops (Gupta et al. 2013; Renuka et al. 2018), but also leads to savings in chemical fertilizers.

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C-Sequestration by Cyanobacteria

12.2.1 Mechanisms Involved Elevated CO2 and global climate change have stimulated research into developing efficient C-utilizing options. In this context, cyanobacteria have emerged as potential candidates, as they possess a unique adaptation, known as Carbon Concentrating Mechanism (CCM) for actively acquiring and transporting CO2 to discrete structures containing the C-fixing enzymes Ribulose Bis-phosphate carboxylase/oxygenase (RuBisCO), and carbonic anhydrase (CA) called as carboxysomes. In autotrophic cyanobacteria, the presence of high CO2 is known to stimulate the RuBisCO’s carboxylase activity, which results in the synthesis of a metabolite, 3-phosphoglycerate (3-PG), whereas the RuBisCO’s oxygenase activity is boosted by low CO2 levels, leading to 2-phosphoglycolate (2-PG), besides 3PGA (Eisenhut et al. 2008; Jiang et al. 2018). The 2-PG must be instantly degraded, as it inhibits the Calvin–Benson cycle enzymes viz., triosephosphate isomerase (Norman and Colman 1991) and phosphofructokinase (Kelly and Latzko 1977). In response to environmental conditions, by bundling their RuBisCO, cyanobacteria have developed a powerful photosynthetic mechanism for stimulating the carboxylation reaction (Badger and Price 1989). Eukaryotic algae and cyanobacteria can actively take up CO2 and Ci from the environment, because they have highly effective transport mechanisms that aid in concentrating the Ci near RuBisCO, the main photosynthetic carboxylating enzyme. The CCM is responsible for the high photosynthetic efficiency and affinity for Ci, leading to improved functioning to utilize Ci efficiently for the process of photosynthesis. This is also facilitated by the cell’s microenvironment and membrane-bound Ci transport mechanism, allowing the use of accumulated Ci to raise CO2 concentration at the site of RuBisCO (Price et al. 2013). In these interactions, the CA dehydrates a built-up HCO3- pool, causing a localized rise of CO2 around the RuBisCO for CO2 fixation. Price et al. (1998) identified the transcriptional regulators viz., CcmR, and CmpR which regulate the CO2-responsive genes, called as a subset of CCM genes, which serve as the main signal for their induction. In CO2-fixing organisms, due to CCM’s ability to concentrate CO2 level up to 1000 times close to the RuBisCO’s active site, CCM may be the most effective method currently in use (Sawaya et al. 2006). The carboxysomes are the vital part of the CCM, which is also called as a bacterial microcomponent (BMC) that is co-inhabited by both RuBisCO and CA (Yeates et al. 2008). Although HCO3cannot be used by RuBisCO, it can use CO2. It is established that the co-sequestration of HCO3- with CA causes the carboxysomes to quickly convert cytosolic HCO3- to CO2 (Cannon et al. 2010). The protein shell of carboxysomes functions as a barrier to prevent the outflow of produced CO2 from carboxysomes, resulting in the build-up of CO2 around the RuBisCO (Sawaya et al. 2006), besides upregulation of several functional CO2 and HCO3- transporters, which are key to the buildup of HCO3- concentration in the cytosol; this HCO3- represents the major substrate for the functioning of carboxysomes in C sequestration (Badger and Price 1989).

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12.2.2 Role of CA There are two distinct enzymatic processes performed by CA. Firstly, it acts as a hydrase, which catalyzes the equilibrium processes between the dehydration and hydration of CO2 or interconversion of CO2 to HCO3- (Kumar et al. 2017). Secondly, CA plays the role of esterase, by hydrolysing the substrate material viz., p-nitrophenyl acetate (p-NPA) to p-nitrophenol (p-NP). The multifunctional role of enzyme CA catalysing the dehydration of HCO3- to CO2 and also the hydration of CO2 to bicarbonate is crucial to CCM, and the accumulated HCO3- is converted into CO2 within the carboxysomes. In some cyanobacteria, both extracellular and intracellular CAs have been reported. The efficiency of Ci transportation is improved by the extracellular CA, which is located in the cell membrane or in the periplasm, as it can maintain the pH of the surrounding environment and contribute to cell mineralization (Braissant et al. 2003). The conversion of HCO3- to CO2 by intracellular CA (located in the carboxysomes) facilitates improving the efficiency of the fixation by the enzyme RuBisCO (Kupriyanova et al. 2007). One million CO2 molecules from HCO3- can be converted by CA per second, hence, its speed makes it one of the highly active known enzymes (Vinoba et al. 2012). External α-CAs are known in some cyanobacteria, Synechococcus sp. PCC 7942, Anabaena sp. PCC 7120, and also in a bacterium Pseudomonas fragi (Sharma et al. 2009). The leakage of available CO2 is prevented by α- and β-CAs, at alkaline pH, by the conversion of CO2 into HCO3-, due to their location in the cell envelope (Kupriyanova et al. 2007). Cyanobacteria use a variety of CAs including periplasmic CA, viz., α type CA and β type CA, called EcaA and EcaB, respectively. In the periplasmic space, both these participate in the conversion of HCO3- to CO2, thereby facilitating C transport inside the cell (So et al. 1998). Bicarbonate is converted to CO2 in the carboxysomes by another carboxysomal β-type CA (CcaA), which increases the CO2 concentration adjacent to RuBisCO, improving its performance in terms of CO2 fixation. The performance of CCM depends on the interaction of several well-known molecular chaperones, which not only help to transfer Ci into the carboxysomes and cytosol from outside the cell, but also function to match the high absorption affinity for Ci obtained by the physiological state of the CCM, in cyanobacteria. Maximum flux rates with low to moderate affinities in cyanobacteria generally aid the uptake systems. HCO3- is actively pumped into cytosol under limited CO2 conditions with the help of active transporters, such as BCT1- Ca2+ dependent, inducible transporter with high affinity and low flux, BicA with low affinity and exhibiting Na+ dependence, while SbtA- is an inducible, high-affinity, HCO3- transporter with low flux. Additionally, CO2 transporters, namely, NDH-I4- a constituent CO2 transporter based on the special NDHI complexes, located on plasma membrane, and NDH-I3-inducible under Ci limited condition, facilitate the improved activity of NDH-I complexes to exhibit high affinity for CO2 but with low flux rate. The buildup of high internal Ci levels to 1000-fold, more than the external Ci levels, is enabled by NDH-13 and NDH-14 (CAs-like proteins). The cmpABCD operon encodes the HCO3- transporter BCT1 in Synechococcus sp. PCC7942 (Omata et al. 1999).

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CcmR transcription factors, which are of the LysR type, regulate the expression of SbtA and NDH-14 (Wang et al. 2004). The active transporters are both inducible and constitutive and will convert CO2 to HCO3- at the thylakoid and cell membrane and deliver HCO3- into the cell (Shibata et al. 2001). The HCO3- accumulated is further fixed through photosynthesis in the carboxysomes by two main enzymes, RuBisCO and CA, located at the inner side. Immediately after HCO3- passively enters the carboxysomes, the enzyme CA quickly dehydrates it and brings it into equilibrium with CO2, causing the formation of substrate CO2 around the RuBisCO. Jiang et al. (2015) reported the crucial role of Ycf46 protein, encoded by the slr0374 gene, for controlling CA activity in Synechocystis sp. PCC 6803 and for total inorganic C use. This ycf46 (slr0374) gene is, however, absent in green algae and higher plants, although it is well conserved in different types of algae and known to be responsive to environmental stresses.

12.2.3 C Fixation and Interrelated Cellular Activities Ribulose 1,5-bisphosphate (RuBP), a 5C compound, enters the carboxysomes and joins with CO2 to create two intermediate molecules of 3-phosphoglycerate (3PGA) through the activity of RuBisCO. This 3PGA diffuses from the carboxysomes to the cytoplasm, through the pores present in the hexameric shell proteins. As a result, HCO3- and 3PGA can easily diffuse into and out of the carboxysomes. The Calvin cycle uses 3PGA in the cytosol to regenerate RuBP, which serves as the primary sink for ATP and NADPH produced during photosynthesis. RuBisCO along with the mechanism of CCM and CO2 supplementation also exhibits oxygenase reaction resulting in the formation of 2-phosphoglycolate (2-PG) production, which is a toxic product, and needs to be recycled through photorespiration. It is thought that carboxysomes serve as a diffusion barrier for CO2, which maximizes the carboxylation process and minimizes the oxygenation process. The CCM mechanism permits the Ci levels to increase up to 200–300 μM, which results in enhanced CO2/O2 ratio, favouring the carboxylation process over oxygenation (Mangan and Brenner 2014). Three molecules of CO2 are fixed into six molecules of 3-PGA and three molecules of RuBP. Again, three RuBP molecules are generated from five of the six 3-PGA and the remaining one 3-PGA molecule is responsible for the production of biological components (biosynthesis of cellular material) (Saini et al. 2011). However, CO2 fixation via CCM is an energy-intensive mechanism because it requires several metabolites, such as enzymes, ATP, transporters, and other compounds to ensure and support the effective performance of CCM, besides being essential for the synthesis of macromolecules viz., RNA and proteins. CCM is also a highly competitive mechanism, and when it is not able to provide sufficient energy and resources required for the photosynthetic and nitrogen fixation activities, growth will be reduced. So, growing cyanobacteria under elevated CO2 conditions will help the organisms to fulfil their requirements by alleviating the C limitation and influencing the growth of cyanobacteria via intracellular reallocation of resources

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and as well as energy to stimulate photosynthesis and nitrogen fixation. Under eCO2, several changes have been recorded, including an enhancement in cell size and volume of the vegetative cells in the filaments of Anabaena and Nostoc calcicola and sp., besides quantitative and structural changes in RuBisCO and its location, number of carboxysomes or quantum of polypeptides (Kaplan et al. 1991; Mayo et al. 1989; Turpin et al. 1984; McKay et al. 1993; Omata et al. 1999, Bloye et al. 1992; Jaiswal et al. 2004). In the cyanobacterium Synechocystis sp., under eCO2, there was an increase of 55 and 25% in amino acids, organic acids, respectively, and N compounds by 7%. Also, a transient stimulation of the Calvin-Benson pathway and RuBisCO is observed, which inactivates the alternative routes of primary C metabolism. This leads to a substantial decrease in 2OG, lowering of PEP carboxylase activity along with an increase in the Glutamine pool, and illustrating an increased N assimilation (Yang et al. 2002). The pathway of N assimilation revealed an increase in mRNA levels of narB, nirA, glnA, and nrt genes, based on transcriptome analyses. With our enhanced understanding of their molecular biology and information generated through the sequencing of several cyanobacterial genomes and databases generated, e.g. the CyanoGEBA project, engineering C- fixation of cyanobacteria seems feasible. The cyanobacterial outer sheath is also the site for a second type of CO2 fixation known as calcification, fueled by CCM-enhanced photosynthesis. Nucleation of CaCO3 in the cyanobacterial sheath is favoured by the conversion of HCO3- into CO2 extracellularly, as the pH of the sheath rises due to CO2 and OH being released, because of the photosynthetic processes (Riding 2006). HCO3- transporters play crucial roles in the regulation of the calcification mechanism, which is CCM-facilitated. The critical role of CmpA, encoding the transporter BCT1, in cyanobacterial calcification process was established by developing knockout mutants, whose expression was 30 times higher than the wild type (Jiang et al. 2015).

12.3

Soil-Plant Interactions with Cyanobacteria in the Context of C Sequestration

12.3.1 Soil-Plant Interactions with Elevated CO2 Increase in atmospheric CO2 concentration will both, directly and indirectly, affect plants by enhancing productivity (Kimball 2011; Pramanik et al. 2018; Raj et al. 2016), besides improving the use of water in a more efficient manner (WUE) (Drake and Gonzàlez-Meier 1997), but reducing plant nitrogen (Raj et al. 2019). Autotrophically fixed carbon contributes significantly towards improving the SOC (Soil Organic Carbon), facilitated by the photosynthetic activity of the microbes and terrestrial plants, SOC, and soil organic matter (SOM) reserves (Berg 2011). Out of the 1500 gigatons of carbon stored in soil, the majority is in organic form in the terrestrial biosphere, while the one-third is present in inorganic forms, mainly as calcium carbonate (Lal 2015). An important strategy for enhancing soil quality and

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boosting crop yields is soil C management, which can be made more efficient by utilizing several capturing technologies. Besides contributing to improved soil health and productivity, biosphere and global C cycle can be benefitted by sustained agricultural production. The Geochip 3.0 can give a snapshot of carbon and nitrogen cycling, by illustrating changes in the composition, structure, and functional potential of different microbial communities in the soil. Its use supported the hypothesis that eCO2 influences soil microbial carbon and nitrogen cycling, and stimulation was recorded, which led to improved plant photosynthetic activity and growth. Also, greater C allocation to belowground led to alterations in the soil microbial biomass, functional activities, community structure, and soil properties such as pH and moisture (Xu et al. 2013). Interesting results on the increased abundance of CO2 fixation genes, along with significant stimulation of genes relevant in N-cycling such as nif, substantiated the biochemical changes recorded. Elevated CO2 (eCO2) enhanced the carboxylation rate of RuBisCO, leading to increased rates of RuBP production and increased CO2 assimilation in plants and illustrating the dominance of carboxylation process, over the oxygenation of RuBP (Li et al. 2017). However, inadequate nitrogen supply could reduce the quality of the product in terms of reduced N content especially in cereals, despite the fertilization effect of elevated CO2 (Chakrabarti et al., 2020; Raj et al. 2019). There are reports of suboptimal effects of elevated CO2 in plants grown under increased CO2 concentration which was mainly attributed to limited nutrient availability to the crops (Norby et al. 2010). A balanced nutrient supply is needed to sustain the crop productivity and quality under elevated CO2 conditions. Elevated CO2 is known to reduce the plant quality by increasing the C:N ratio, besides its direct effect on plant physiology and growth as a result of re-allocation of assimilates towards the synthesis of secondary metabolite, thereby modulating its interactions with herbivores (Barbehenn et al. 2004). Zavala et al. (2009) showed that elevated CO2 led to a downregulation of the primary defence system through the activity and gene expression of cysteine proteinase inhibitors in soybean, thereby making them an easy prey to insect herbivores, while in cabbage a decrease in the emission of JA-regulated terpene volatiles was recorded (Vuorinen et al. 2004). eCO2 brought about a significant increase in theanine, phenylpropanoids, salicylic acid (SA), Jasmonic acid (JA) concentrations, (+98.6%), free amino acids, and tea polyphenols, but suppressed the expression of caffeine synthesis genes; this led to lowering of the caffeine content in the tea leaves (Li et al. 2017). In order to provide N, under elevated CO2 conditions, the use of photosynthetic diazotrophic microbial inoculants may help to alleviate such negative effects (Kokila et al. 2022). Plant growth-promoting rhizobacteria (PGPR) are a class of microorganisms, which directly and indirectly helps plants to grow and develop. They also improve nutrient availability and uptake, produce phytohormones that affect plant growth, and remove phytopathogenic organisms from the rhizosphere (Zahir et al. 2004). Photosynthetic cyanobacterial inoculants possess C sequestering ability and can be used in INM-integrated nutrient management practices (Prasanna et al. 2014). Cyanobacteria utilize atmospheric CO2 for photosynthesis and evolve oxygen,

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thus represent a potential sink for CO2 and can be used as a mitigation option for climate change (Kumar et al. 2011a, b). Reports on the benefits of cyanobacterial inoculation in crops like wheat, maize, cotton, legumes, and vegetables highlight its importance in not only flooded rice crops but also in other crop ecologies (Karthikeyan et al. 2007; Prasanna et al. 2014, 2015; Simranjit et al. 2019).

12.3.2 Cyanobacteria-Soil-Plant Interactions with Elevated CO2 In the climate change scenario, C3 crops, such as tomatoes, are greatly influenced by increased CO2 concentrations (Besford et al. 1990). Both whole plant and leaf level measurements showed that this led to a stimulation in the WUE related to photosynthesis and transpiration in tomato plants grown after exposure to various CO2 and lighting treatments (Lanoue et al. 2018). As cyanobacteria are known to sequester C, their inoculation may improve soil carbon dynamics and stimulate C-fixation in the soil, which can be utilized by plants. The adaptive capacity of cyanobacteria to diverse environmental conditions makes them a potential contributor to crop productivity under different agroecosystems. Application of cyanobacterial inoculation as nitrogen supplementing biofertilizers is commonly practiced in paddy fields in several countries of Southeast Asia. Cyanobacterial inoculation is known to benefit the plant and improve the quality of produce by improving the availability of macroand micronutrients, thereby aiding in the biofortification of grains and nutritional or value addition in flowers/fruits or phenological characteristics (Prasanna et al. 2012; Rana et al. 2012; Bharti et al. 2021; Shivay et al. 2022). Extracellular chemicals and other metabolites released by cyanobacterial strains and their biofilms can lead to both direct and indirect effects on growth and yield of crops, besides ecosystem productivity (Manjunath et al. 2011), by regulating the restoration of microbial population involved in the carbon and nitrogen cycling in soil (Acea et al. 2003). Cyanobacteria also secrete extracellular polymeric substances called exopolysaccharides (EPS), which help in alleviating water stress and facilitate the formation of soil aggregates, microbial biomass carbon, and ultimately soil organic carbon. In arid and semi-arid habitats, reported that cyanobacteria play a key role, through the addition of C and N, besides micronutrients; this helps to better stability and hydrological attributes of soil (Orlovsky et al. 2004). In high-value greenhouse crops, elevated CO2 growth conditions have stimulatory effect in terms of yield and biomass production (Hurd 1968; Kimball and Mitchell 1979). The interactions of cyanobacterial inoculation in soil, with/without tomato plants, were investigated under both ambient CO2 and elevated CO2 levels (Kokila et al. 2022). Cyanobacterial inoculation, in conjunction with/without tomato crop, led to an improvement in soil chlorophyll, soil polysaccharides, proteins, total leaf pigments, and the activity of C-N metabolizing enzymes under elevated CO2 levels. Among the different cyanobacteria used as inoculants, the performance of Anabaena laxa was superior as a significant increment in polysaccharides, along with 40–45% enhancement in available nitrogen was recorded. The activities of C-N mobilizing enzyme activities were stimulated, higher nitrogen fixation rate and an increase in

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available nitrogen were recorded, highlighting the beneficial effects on the C-N dynamics. This may, in turn, lead to fruits from An-Tr treatments under eCO2 exhibiting a higher titratable acidity, along with more ascorbic acid, carotenoids, and lycopene content. Under elevated CO2, Anabaena torulosa-Trichoderma viride (An-Tr) biofilm as an inoculant brought about 60–70% enhancement in soil microbial biomass carbon, besides 50% N savings. A. laxa treatment also increased the amount of plant pigments, carbonic anhydrase, and glutamine synthetase activity under elevated CO2. The plants grown under eCO2 conditions showed 8 days early flowering, and significantly higher yield, compared to ambient conditions. Significant enhancement in the total PLFA in soil through cyanobacterial inoculation as reported earlier in rice illustrated a beneficial impact on the culturable soil microbiome (Priya et al. 2015; Ranjan et al. 2016; Kokila 2022). Elevated CO2 conditions also minimized the damaging effects of oxygen free radicals (OFR) during vegetative stages of tomato plants, as compared to plants grown under aCO2 conditions (Reinert et al. 1997). The metabolic stimulation at flowering stage and the early fruit-forming stage, along with the significant correlation of antioxidant compounds and innate defence enzymes with the eCO2 levels, illustrates the ability of the plants to orchestrate these activities and function coordinately. This also delays the release of senescence inducing (ROX) reactive oxygen species (Mittler et al. 2004), with beneficial effects on plant development. It can be surmised that cyanobacterial inoculation modulates the activities of soil microbial communities beneficially leading to greater nutrient availability and improved plant growth in tomato crop (Kokila et al. 2022). Nutrient availability plays a vital role in influencing plant response under eCO2 conditions (Poorter et al. 1996). In a managed ecosystem, leguminous species will respond better to elevated CO2 conditions than cereal crops as they can more efficiently utilize the additional C for fixation of atmospheric N2 (Ainsworth et al. 2005; Rogers et al. 2006). Several studies have shown that legumes have more advantages over non-legumes under eCO2 levels (Serraj et al. 1998; Ross et al. 2004). Under elevated CO2 conditions, legumes fix more amounts of atmospheric nitrogen (N2), resulting in better growth responses (Rogers et al. 2006; Dey et al. 2017a). Optimum supply of essential nutrients leads to increased nitrogen fixation resulting in improved soil N status and increased ecosystem productivity. Among different nutrients, phosphorus (P) requirement by legumes may also increase under elevated CO2 conditions as P has an important role in N2 fixation (Dey et al. 2019). Cyanobacterial inoculation in leguminous crops can help in deriving additional N2 fixed by the cyanobacteria itself. There are reports of increased nitrogen fixation in cowpea under eCO2 concentration which got further stimulated by cyanobacterial inoculation (Dey et al. 2017a). Use of cyanobacterial biofilm (A. torulosa–B. japonicum) inoculation increased N2 fixation, N uptake, and soil available N under elevated CO2 and temperature interactions in soybean crop highlighting its potential in counteracting the negative impact of climate change (Sanyal et al. 2022). According to Dey et al. (2016, 2017b), phosphorus application along with cyanobacterial inoculation helps in improving the productivity of mungbean under elevated CO2 concentration. Cyanobacterial inoculation was found to facilitate P

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uptake in cowpea under elevated CO2 conditions (Dey et al. 2019). Several other studies showed that there is a significant increase in pod number, total biomass in legumes treated with Rhizobium inoculant, and other PGPRs. Chickpea, pea, and lentil inoculated with Anabaena laxa (RPAN8) and biofilm Anabaena-Pseudomonas fluorescens showed the best response in terms of biomass, pod yield, and N2 fixation (Babu et al. 2015). Comparison between nodulating and non-nodulating legumes showed that nitrogen fixers respond more to CO2 concentration than non-nitrogen fixers (Luscher et al. 2000). The legume-rhizobia symbiosis contributes one-third to half of the total nitrogen added to the crop land (Herridge et al. 2008). Increase in photosynthetic carbon uptake under eCO2 condition will increase the leaf carbohydrates in clover and soybean crops (Ainsworth et al. 2003). Previous reports showed increased length, diameter, and mass of soybean roots grown under elevated CO2 levels. Besides this, higher nodule mass of legumes led to greater nitrogen fixation. Although legumes respond positively to increased CO2 concentration in a managed ecosystem, the response may not be similar in a natural ecosystem because of the limited nutrient availability (van Groenigen et al. 2006). The changing climate accompanied with drastic enhancement in atmospheric CO2 levels and high temperature is known to affect the rhizospheric microbial population and alter the composition of root exudates.

12.4

Future Prospects and Path Ahead

The role of photosynthetic microorganisms for carbon capture and sequestration is an emerging area of interest to counteract the rising CO2 emission. Cyanobacteria is such an organism that can help in C capture as well as improve plant growth and soil N status thereby reducing the use of nitrogenous fertilizers. Efforts need to be made to stimulate the cyanobacterial growth rate and productivity by optimizing the growth conditions, such as engineering native metabolic pathways, and introducing new synthetic pathways to produce strains with superior properties. This can also provide opportunities for commercialization of their bioproducts, based on effective and efficient use of C from the atmosphere. Furthermore, the response to gradual increases in CO2 concentration and cyanobacteria-plant interactions in long-term experiments needs to be investigated. The following interventions can be envisaged to exploit the potential of cyanobacteria: • Introducing carboxysomes of cyanobacteria into plant chloroplast, e.g. carboxysomes of S. elongatus were exported into chloroplasts of tobacco. • Transformation of an exogenous RuBisCO into plants, for improved catalytic properties, to substantially increase photosynthetic yield under field conditions. • Simulation of the working of CCMs in plants to increase the CO2 concentration around RuBisCO, making changes to suppress the oxygenation reaction of the

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enzyme to enable higher CO2-fixation rates, resulting in increased CO2-fixing efficiency. • Focussed research and inclusion of microbes with carbon sequestration ability in biofertilizers and integrated nutrient management strategies. • In-depth analyses of eCO2 in relation to C-N dynamics and their feedback on plant growth and development to understand the potential for carbon sequestration in enhancing crop productivity and quality of produce. • Cyanobacterial inoculation, particularly, novel cyanobacterial biofilms can be explored as a promising option for crops under future climatic conditions. Acknowledgements The authors thank the Indian Council of Agricultural Research (ICAR) for providing funds through the Network Project on Microorganisms ‘Application of Microorganisms in Agricultural and Allied Sectors’ (AMAAS) New Delhi. The authors are also grateful to the Division of Microbiology, National Phytotron Facility (NPF), and Division of Environment Science, ICAR-IARI, for providing all the necessary facilities.

References Acea MJ, Prieto-Fernandez A, Diz N (2003) Cyanobacterial inoculation of heated soils: effect on microorganisms of C and N cycles and on chemical composition in soil surface. Soil Biol Biochem 35:513–524 Ahmed AA, Odelade KA, Babalola OO (2019) Microbial inoculants for improving carbon sequestration in agroecosystems to mitigate climate change. In: Handbook of climate change resilience. Springer International Publishing, Cham, pp 1–21 Ainsworth EA, Long SP (2005) What have we learned from 15 years of free air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372 Ainsworth EA, Rogers A, Blum H, Nosberger J, Long SP (2003) Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to free air CO2 enrichment (FACE). J Exp Bot 54:2769–2774 Babu S, Prasanna R, Bidyarani N, Singh R (2015) Analysing the colonisation of inoculated cyanobacteria in wheat plants using biochemical and molecular tools. J Appl Phycol 27(1): 327–338 Badger MR, Price GD (1989) Carbonic anhydrase activity associated with the cyanobacterium Synechococcus PCC7942. Plant Physiol 89(1):51–60 Barbehenn RV, Karowe DN, Chen Z (2004) Performance of a generalist grasshopper on a C3 and a C4 grass: compensation for the effects of elevated CO2 on plant nutritional quality. Oecologia 140:96–103 Berg IA (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microbiol 77:1925–1936 Besford RT, Ludwig LJ, Withers AC (1990) The greenhouse effect: Acclimation of tomato plants growing in high CO2, photosynthesis and ribulose-1, 5-bis phosphate carboxylase protein. J Exp Bot 41(8):925–931 Bharti A, Prasanna R, Dantuluri VS, Chawla G, Shivay YS, Nain L (2021) Cyanobacteriumamended mixes as priming options for stimulating growth and improving nutrient availability in nursery-grown Chrysanthemum rooted stem cuttings. Acta Physiol Plant 43(7):1–6 Bhola V, Swalaha F, Ranjith Kumar R, Singh M, Bux F (2014) Overview of the potential of microalgae for CO2 sequestration. Int J Environ Sci Technol 11(7):2103–2118

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Bloye SA, Silman NJ, Mann NH, Carr NG (1992) Bicarbonate concentration by synechocystis PCC6803: modulation of protein phosphorylation and inorganic carbon transport by glucose. Plant Physiol 99(2):601–606 Braissant O, Cailleau G, Dupraz GP, Verrecchia (2003) Bacterially induced mineralization of calcium carbonatea in terrestrial environments: the role of exopolysaccharides and amino acids. J Sediment Res 73:485–490 Cannon GC, Heinhorst S, Kerfeld CA (2010) Carboxysomal carbonic anhydrases: structure and role in microbial CO2 fixation. Biochim Biophys Acta Proteins Proteom 1804(2):382–392 Chakrabarti B, Singh SD, Bhatia A, Kumar V, Harit RC (2020) Yield and nitrogen uptake in wheat and chickpea grown under elevated carbon dioxide level. Natl Acad Sci Lett 43:109–113. https://doi.org/10.1007/s40009-019-00816 Dey Sumit K, Chakrabarti B, Prasanna R, Mittal R, Singh SD, Pathak H (2016) Growth and biomass partitioning in mungbean with elevated carbon dioxide, phosphorus levels and cyanobacteria inoculation. J Agrometeorol 18(1):7–12 Dey Sumit K, Chakrabarti B, Prasanna R, Pratap D, Singh SD, Purakayastha TJ, Pathak H (2017a) Elevated carbon dioxide level along with phosphorus application and cyanobacterial inoculation enhances nitrogen fixation and uptake in cowpea crop. Arch Agron Soil Sci 63(13):1927–1937. https://doi.org/10.1080/03650340.2017.1315105 Dey Sumit K, Chakrabarti B, Prasanna R, Singh SD, Purakayastha TJ, Datta A, Pathak H (2017b) Productivity of mungbean (Vigna radiata) with elevated carbon dioxide at various phosphorus levels and cyanobacteria inoculation. Legum Res 40(3):497–505 Dey SK, Chakrabarti B, Purakayastha TJ, Prasanna R, Mittal R, Singh SD, Pathak H (2019) Interplay of phosphorus doses, cyanobacterial inoculation, and elevated carbon dioxide on yield and phosphorus dynamics in cowpea. Environ Monit Assess 191(4):223. https://doi.org/ 10.1007/s10661-019-7378-3 Drake BG, Gonzàlez-Meier MA (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Biol 48:609–639 Eisenhut M, Huege J, Schwarz D, Bauwe H, Kopka J, Hagemann M (2008) Metabolome phenotyping of inorganic carbon limitation in cells of the wild type and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 148(4): 2109–2120 Gupta V, Ratha SK, Sood A, Chaudhary V, Prasanna R (2013) New insights into the biodiversity and applications of cyanobacteria (blue-green algae) prospects and challenges. Algal Res 2(2): 79–97 Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18 Hurd RG (1968) Effects of CO2-enrichment on the growth of young tomato plants in low light. Ann Bot 32(3):531–542 Jaiswal P, Prasanna R, Kashyap AK, Singh PK (2004) Response of Nostoc calcicola and Anabaena sp. and their mutants to elevated levels of inorganic carbon. Acta Bot Hungar 46(1–2):167–178 Jiang HB, Song WY, Cheng HM, Qiu BS (2015) The hypothetical protein Ycf46 is involved in regulation of CO2 utilization in the cyanobacterium Synechocystis sp. PCC 6803. Planta 241(1): 145–155 Jiang YL, Wang XP, Sun H, Han SJ, Li WF, Cui N, Lin GM, Zhang JY, Cheng W, Cao DD, Zhang ZY (2018) Coordinating carbon and nitrogen metabolic signaling through the cyanobacterial global repressor NdhR. Proc Natl Acad Sci 115(2):403–408 Kaplan A, Schwarz R, Lieman-Hurwitz J, Reinhold L (1991) Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol 97(3): 851–855 Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30 Kelly GJ, Latzko E (1977) Chloroplast phosphofructokinase: II. Partial purification, kinetic and regulatory properties. Plant Physiol 60(2):295–299

278

V. Kokila et al.

Kimball BA (2011) Lessons from FACE: CO2 effects and interactions with water, nitrogen and temperature. In: Hillel D, Rosenzweig C (eds) Handbook of climate change and agroecosystems: impacts, adaptation, and mitigation. Imperial College Press, Hackensack, NJ, pp 87–107 Kimball BA, Mitchell ST (1979) Tomato yields from CO2-enrichment in unventilated and conventionally ventilated greenhouses. J Am Soc Hortic Sci 4:515–520 Kokila V (2022) Exploring the potential of cyanobacteria in soil carbon dynamics and enhancing plant vigour in tomato. Ph.D. Thesis, Post Graduate School, ICAR-IARI, New Delhi Kokila V, Prasanna R, Kumar A, Nishanth S, Shukla J, Gulia U, Nain L, Shivay YS, Singh AK (2022) Cyanobacterial inoculation in elevated CO2 environment stimulates soil C enrichment and plant growth of tomato. Environ Technol Innov 26:102234 Kumar K, Dasgupta CN, Nayak B, Lindblad P, Das D (2011a) Development of suitable photobioreactors for CO2 sequestration addressing global warming using green algae and cyanobacteria. Bioresour Technol 102:4945–4953 Kumar M, Gupta V, Trivedi N, Kumari P, Bijo AJ, Reddy CR, Jha B (2011b) Desiccation induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ Exp Bot 72(2):194–201 Kumar M, Morya R, Gnansounou E, Larroche C, Thakur IS (2017) Characterization of carbon dioxide concentrating chemolithotrophic bacterium Serratia sp. ISTD04 for production of biodiesel. Bioresour Technol 243:893–897 Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los DA, Pronina N (2007) Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology 153(4):1149–1156 Lanoue J, Leonardos ED, Khosla S, Hao X, Grodzinski B (2018) Effect of elevated CO2 and spectral quality on whole plant gas exchange patterns in tomatoes. PLoS One 13(10):e0205861 Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123(1–2):1–22 Lal R (2015) Sequestering carbon and increasing productivity by conservation agriculture. J Soil Water Conserv 70(3):55A–62A Li X, Zhang L, Ahammed GJ, Li ZX, Wei JP, Shen C, Yan P, Zhang LP, Han WY (2017) Stimulation in primary and secondary metabolism by elevated carbon dioxide alters green tea quality in Camellia sinensis L. Sci Rep 7(1):7937 Luscher A, Hartwig UA, Sute D, Nosberger J (2000) Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Glob Chang Biol 6:655–662 Mangan NM, Brenner MP (2014) Systems analysis of the CO2 concentrating mechanism in cyanobacteria. eLife 3:e02043 Manjunath M, Prasanna R, Sharma P, Nain L, Singh R (2011) Developing PGPR consortia using novel genera—Providencia and Alcaligenes along with cyanobacteria for wheat. Arch Agron Soil Sci 57:873–887 Mayo WP, Elrifi IR, Turpin DH (1989) The relationship between ribulose bisphosphate concentration, dissolved inorganic carbon (DIC) transport and DIC-limited photosynthesis in the cyanobacterium Synechococcus leopoliensis grown at different concentrations of inorganic carbon. Plant Physiol 90(2):720–727 McKay RML, Gibbs SP, Espie GS (1993) Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of Rubisco and the mode of inorganic carbon transport in cells of the cyanobacterium Synechococcus UTEX 625. Arch Microbiol 159(1):21–29 Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Sci 9(10):490–498 Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107:19368–19373 Norman EG, Colman B (1991) Purification and characterization of phosphoglycolate phosphatase from the cyanobacterium Coccochloris peniocystis. Plant Physiol 95(3):693–698

12

Photosynthetic Microorganisms and Their Role in Mitigating Climate. . .

279

Olson KR, Al-Kaisi M, Lal R, Morton LW (2017) Soil ecosystem services and intensified cropping systems. J Soil Water Conserv 72(3):64A–69A Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci 96:13571–13576 Orlovsky L, Dourikov M, Babaev A (2004) Temporal dynamics and productivity of biogenic soil crusts in the central Karakum desert, Turkmenistan. J Arid Environ 56:579–601 Parry MA, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II Increasing photosynthetic capacity and efficiency. J Exp Bot 62(2):453–467 Poorter H, Roumet C, Campbell BD (1996) Interspecific variation in the growth response of plants to elevated CO2: a search for functional types. In: Korner C, Bazzaz FA (eds) Carbon dioxide, populations, and communities. Academic Press, San Diego, CA, pp 375–412 Pramanik P, Chakrabarti B, Bhatia A, Singh SD, Mridha N, Krishnan P (2018) Effect of elevated carbon dioxide on soil hydrothermal regimes and growth of maize crop (Zea mays L.) in semiarid tropics of indo-gangetic plains. Environ Monit Assess 190(11):1–10. https://doi.org/10. 1007/s10661-018-6988-5 Prasanna R, Joshi M, Rana A, Shivay YS, Nain L (2012) Influence of co-inoculation of bacteriacyanobacteria on crop yield and C–N sequestration in soil under rice crop. World J Microbiol Biotechnol 28(3):1223–1235 Prasanna R, Triveni S, Bidyarani N, Babu S, Yadav K, Adak A, Khetarpal S, Pal M, Shivay YS, Saxena AK (2014) Evaluating the efficacy of cyanobacterial formulations and biofilmed inoculants for leguminous crops. Arch Agron Soil Sci 60:349–366 Prasanna R, Babu S, Bidyarani N, Kumar A, Triveni S, Monga D, Mukherjee AK, Kranthi S, Gokte-Narkhedkar N, Adak A, Yadav K (2015) Prospecting cyanobacteria-fortified composts as plant growth promoting and biocontrol agents in cotton. Exp Agric 51(1):42–65 Prasanna R, Renuka N, Nain L, Ramakrishnan B (2021) Natural and constructed cyanobacteriabased consortia for enhancing crop growth and soil fertility. In: Seneviratne G, Zavahir JS (eds) Microbes for sustainability: role of microbial communities. Springer, Cham, pp 333–362. https://doi.org/10.1007/978-981-15-9912-5; ISBN 978-981-15-9912-5 (eBook) Price GD, Sültemeyer D, Klughammer B, Ludwig M, Badger MR (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances. Can J Bot 76(6):973–1002 Price GD, Pengelly JJ, Forster B, Du J, Whitney SM, von Caemmerer S, Badger MR, Howitt SM, Evans JR (2013) The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species. J Exp Bot 64(3):753–768 Priya H, Prasanna R, Ramakrishnan B, Bidyarani N, Babu S, Thapa S, Renuka N (2015) Influence of cyanobacterial inoculation on the culturable microbiome and growth of rice. Microbiol Res 171:78–89 Raj A, Chakrabarti B, Pathak H, Singh SD, Mina U, Mittal R (2016) Growth, yield components and grain yield response of rice to temperature and nitrogen levels. J Agrometeorol 18(1):1–6 Raj A, Chakrabarti B, Pathak H, Singh SD, Mina U, Purakayastha TJ (2019) Growth, yield and nitrogen uptake in rice crop grown under elevated carbon dioxide and different doses of nitrogen fertilizer. Indian J Exp Biol 57:181–187 Rana A, Joshi M, Prasanna R, Shivay YS, Nain L (2012) Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur J Soil Biol 50: 118–126 Ranjan K, Priya H, Ramakrishnan B, Prasanna R, Venkatachalam S, Thapa S, Tiwari R, Nain L, Singh R, Shivay YS (2016) Cyanobacterial inoculation modifies the rhizosphere microbiome of rice planted to a tropical alluvial soil. Appl Soil Ecol 108:195–203 Reinert RA, Eason G, Barton J (1997) Growth and fruiting of tomato as influenced by elevated carbon dioxide and ozone. New Phytol 137(3):411–420

280

V. Kokila et al.

Renuka N, Guldhe A, Prasanna R, Singh P, Bux F (2018) Microalgae as multi-functional options in modern agriculture: current trends, prospects and challenges. Biotechnol Adv 36(4):1255–1273 Riding R (2006) Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and proterozoic-cambrian changes in atmospheric composition. Geobiology 4(4):299–316 Rogers A, Gibon Y, Stitt M, Morgan PB, Bernacchi CJ, Ort DR, Long SP (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell Environ 29:1651–1658 Ross DJ, Newton PCD, Tate KR (2004) Elevated (CO2) effects on herbage production and soil carbon and nitrogen pools and mineralization in a species-rich, grazed pasture on a seasonally dry sand. Plant Soil 260:183–196 Saini R, Kapoor R, Kumar R, Siddiqi TO, Kumar A (2011) CO2 utilizing microbes—a comprehensive review. Biotechnol Adv 29:949–960 Sanyal S, Chakrabarti B, Prasanna R, Bhatia A, Kumar SN, Purakayastha TJ, Joshi R, Sharma A (2022) Influence of cyanobacterial inoculants, elevated carbon dioxide, and temperature on plant and soil nitrogen in soybean. J Basic Microbiol 2022:1–13. https://doi.org/10.1002/jobm. 202200046 Sawaya MR, Cannon GC, Heinhorst S, Tanaka S, Williams EB, Yeates TO, Kerfeld CA (2006) The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J Biol Chem 281:7546–7555 Serraj R, Sinclair TR, Allen LH (1998) Soybean nodulation and N2 fixation response to drought under carbon dioxide enrichment. Plant Cell Environ 21:491–500 Sharma A, Pandey A, Shouche YS, Kumar B, Kulkarni G (2009) Characterization and identification of Geobacillus spp. isolated from Soldhar hot spring site of Garhwal Himalaya. Indian J Microbiol 49:187–194 Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, Ogawa T (2001) Distinct constitutive and low-CO2- induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci U S A 98:11789–11794 Shivay YS, Prasanna R, Mandi S, Kanchan A, Simranjit K, Nayak S, Baral K, Sirohi MP, Nain L (2022) Cyanobacterial inoculation enhances nutrient use efficiency and grain quality of basmati rice in the system of rice intensification. ACS Agric Sci Technol 2(4):742–753 Simranjit K, Kanchan A, Prasanna R, Ranjan K, Ramakrishnan B, Singh AK, Shivay YS (2019) Microbial inoculants as plant growth stimulating and soil nutrient availability enhancing options for cucumber under protected cultivation. World J Microbiol Biotechnol 35(3):1–14 So AKC, Van Spall HGC, Coleman JR, Espie GS (1998) Catalytic exchange of O-18 from (CO)-C13-O-18-labelled CO2 by wild-type cells and ecaA, ecaB, and ccaA mutants of the cyanobacteria Synechococcus PCC7942 and Synechocystis PCC6803. Can J Bot 76:1153–1160 Tsai DDW, Chen PH, Ramaraj R (2017) The potential of carbon dioxide capture and sequestration with algae. Ecol Eng 98:17–23 Turpin DH, Miller AG, Canvin DT (1984) Carboxysome content of synechococcus leopoliensis (cyanophyta) in response to inorganic carbon 1. J Phycol 20(2):249–253 Van Groenigen KJ, Six J, Hungate BA, De Graaff MA, Van Breemen N, Van Kessel C (2006) Element interactions limit soil carbon storage. Proc Natl Acad Sci 103:6571–6574 Vinoba M, Bhagiyalakshmi M, Jeong SK, Nam SC, Yoon Y (2012) Carbonic anhydrase immobilized on encapsulated magnetic nanoparticles for CO2 sequestration. Eur J Chem 18: 12028–12034 Vuorinen T, Nerg AM, Ibrahim MA, Reddy GVP, Holopainen JK (2004) Emission of Plutella xylostella-induced compounds from cabbages grown at elevated CO2 and orientation behavior of the natural enemies. Plant Physiol 135(4):1984–1992 Xu M, He Z, Deng Y, Wu L, Van Nostrand JD, Hobbie SE, Reich PB, Zhou J (2013) Elevated CO2 influences microbial carbon and nitrogen cycling. BMC Microbiol 13(1):124

12

Photosynthetic Microorganisms and Their Role in Mitigating Climate. . .

281

Wang HL, Postier BL, Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279:5739–5751 Yang C, Hua Q, Shimizu K (2002) Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. Metab Eng 4(3):202–216 Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM (2008) Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 6(9):681–691 Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168 Zavala JA, Casteel CL, Nabity PD, Berenbaum MR, DeLucia EH (2009) Role of cysteine proteinase inhibitors in preference of Japanese beetles (Popillia japonica) for soybean (Glycine max) leaves of different ages and grown under elevated CO2. Oecologia 161(1):35–41

Arbuscular Mycorrhizal Fungi: A Keystone to Climate-Smart Agriculture

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Seema Sangwan, Garima Saxena, Pratibha Barik, and Ram Swaroop Bana

Abstract

With the inevitable demand to increase agricultural productivity in future years, agriculture production needs to be sustainable with more tolerance to changing environmental conditions so that it can be transformed into climate-smart agriculture. The potent role of soil biodiversity especially the arbuscular mycorrhiza fungi (AMF) has been shown to stabilize the ecosystem under fluctuating global climate. AMF being unique, abundant and natural biofertilizers guarantee the plant’s approach to soil resources, diminish the outflow of greenhouse gases and act as an origin and decay for carbon (C) allowing the whole ecosystem to rebound readily even under prejudiced conditions. Here, we will conglomerate the contribution of AMF in improving the soil structure by promoting soil aggregation, less and efficient use of fertilizers, resistance to pests, enhancing the plant yield and minimal release of greenhouse gases thus supporting the agroecosystem in various modes. At the end, intensive management practices will also be discussed which can shift the mycorrhizal functioning in a more productive way. In this chapter, our focus is to emphasize on the ecologically wide potential of AMF in making the agriculture climate smart and sustainable to answer the question: are AMF a keystone to climate-smart agriculture? Keywords

Arbuscular mycorrhizal fungi · Climate smart · Biofertilizer · Agriculture · Sustainable

S. Sangwan (✉) · G. Saxena · P. Barik Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India R. S. Bana Division of Agronomy, ICAR-Indian Agricultural Research Institute, New Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_13

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13.1

Introduction

For many people residing in developing countries, the main source of food, income and employment is agriculture. Over the past decades, there is a widespread consciousness about sustainable agriculture development which can be a potent solution to feed the growing population. Sustainable agriculture is based on the use of balanced ecosystem services along with fulfilment of present and future needs of society related to food, textiles, etc. This can be met holistically and effectively using climate-smart agriculture. In the scenario of changing climate conditions and increased rate of population, food and nutritional security can be assured by making the agriculture climate smart. It involves a focussed perspective to study noteworthy soil biodiversity and symbiotic relationships among plants and microbes, particularly arbuscular mycorrhiza fungi (AMF) which has remarkable out-turn in making the agriculture more resilient, making them more resistant towards severe and very common climate change events in a sustainable way. Arbuscular Mycorrhiza fungi (AMF), natural root symbionts are very attractive for increasing the sustainability in agriculture and making it smart with changing climate. The soil conditions are much more favourable to AMF in sustainability (Linderman 2015). AMF form a symbiotic relationship with roots of above 80% of cultivated plants, pteridophytes, conifers, flowering plants, monocots, etc. which are extensively widespread in natural and agricultural habitat. AMF helps the host plants with which they are associated to grow under various stressful climatic and soil conditions – like high salt and heavy metals, nutrient and moisture deficit and extreme heat (Fig. 13.1). Due to the number of complex chemical reactions and signals between the plant and the fungus, an increased photosynthetic rate and water

INCEASE PLANT A/BIOTIC TOLERANCE •

Tolerance against phytopathogenic fungi, insect pest,and phytopathogenic bacteria and nematodes

•

tolerance against salt and drought.

SOIL HEALTH

CO2 CH4

N2O CO2

SUGAR

AMF COLONIZATION

Improve soil ferlity, Water holding capacity of the soil and enhance soil quality

K P Zn

N

Fig. 13.1 Potent role of AMF in sustainable agriculture

NUTRIENT UPTAKE AND TRANSFER Reduce green house gas emmision (CO2,N2O,CH4)due to increase in nutrient uptake

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uptake take place (Linderman 1997). The symbiotic association of plants with AMF is very important as they help in crop and biomass production by assisting the plants in the regulation of metabolic pathways. Commonly known as bio-fertilizers, AMF are receiving considerable attention in agriculture. Altogether, AMF holds opportunities for management in climate-smart agriculture as they are highly relevant components of agroecosystems. This review emphasizes on the promising input of AMF for reduction of greenhouse gas emissions, carbon sequestration, pest resistance, minimal and efficient use of fertilizers and soil nutrient management. Further research goals focusing on maximizing the benefits of AMF will also be discussed.

13.2

Climate-Smart Agriculture: An Integrated Dimension of Sustainable Development

Climate-Smart Agriculture (CSA) also called Climate Resilient Agriculture is an imminent approach to develop agriculture by its transformation and reorientation towards a sustainable and secure food system under the regime of continuously changing climate. Agriculture will always be affected by fluctuations in climate as these two are very much interrelated and universal processes (Intergovernmental Panel on Climate Change (IPCC) 2007). It’s a way to support food security in a sustainable way by maintaining and enhancing the production of agriculture by responding to the challenges of climate change. The concept of CSA was first defined in 2010 by the Food and Agriculture Organization (FAO) during the Hague Conference focused on agriculture, food security and climate change. Its objectives were formulated on sustainable progress in three ways, i.e. ecological, financial and community based under a centric approach of national food security and development goals. By enhancing agricultural yields and profits, they strengthen climate change and adaptation with it that resulted in securing food demand in a sustainable manner; and reducing greenhouse gas emissions by developing various techniques and opportunities. CSA helps to achieve green economy goals along with sustainable development.

13.3

Arbuscular Mycorrhizal Fungi and Climate-Smart Agriculture

Soil microbiome determines the ecosystem resilience, sustainable agricultural production, soil and water conservation and GHG emissions. Though their activity is directly affected with changing climate conditions, but they are an essential component in virtually all ecosystem processes. Microorganisms carry out decomposition and heterotrophic respiration and help in more absorption of water and nutrients from soil contributing directly to the plant productivity thereby is an important keystone in climate-smart agriculture (Van der Heijden et al. 2008). The most widespread symbiotic association between roots and soil microorganisms is the

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CSA

SUSTAINABILITY INCREASES

PRODUCTIVITY AND INCOME

STRENTHEN RESCILENCE

TO CLIMATE CHANGE AND VARIABILTY

REDUCE AGRICULTURE CONTRIBUTUTIONTO CLIMATE CHANGE

GREEN HOUSE GAS EMISSION + CARBON STORAGE ON FARM LAND

IMPROVED STRESS TOLERANCE AND ENHANCED YEILD

PLANT STRESS TOLERANCE IncreasedResistant to foliar pathogen Increase drought tolerance Increase salt tolerance Ressistant to root pathogen

VIA SPECIFIC TRANSPORTERS

NUTRIENT UPTAKE

SOIL HEALTH Improves – Soil moisture Ferlity level Soil quality

AMF Fig. 13.2 AMF: a significant component of climate-smart agriculture

monophyletic Arbuscular Mycorrhizal fungi (AMF). They ameliorate the waterholding power of soil, control the nutrients availability and their uptake, increase fertility of soil and reduce soil greenhouse gas (GHG) emissions (Fig. 13.2) thus are a component of an extensive range of flora and fauna (Lazcano et al. 2014; Powell and Rillig 2018). Along with other diverse microbes, AMF being unique and abundant contributes in stabilization of ecosystem functioning (Sosa-Hernández et al. 2018). AMF symbiosis being better suited and highly competitive, helps in acclimatization of vegetation in several biotic as well as abiotic environment for their better ease, enhanced maturation, expansion and evolution, thereby supports the insurance hypothesis in a comprehended manner (Sosa-Hernández et al. 2019). Climate-smart agriculture is based on the concept of modern sustainable agriculture which includes a nature-based low-input system. It focuses on increase in plant growth and metabolism, plant protection, soil health and fertility, etc. by using soilloving microorganisms under stressful environmental conditions. AMF is an efficient key for climate-smart cultivation and fulfils all the demands particularly in terms of various parameters, e.g. reduced GHG emissions and nutrient management.

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Significant agricultural improvement can be obtained by exploiting AMF which will result in less use of synthetic fertilizers and other chemicals. Hence, being costefficient, eco-friendly and energy rescuer, AMF will eventually result in a promising perspective for a climate-smart agriculture.

13.4

Effect of AMF on Greenhouse Gas Emission

Agroecosystems are one of the significant wellsprings of ozone-depleting substances, i.e. a reservoir of GHG (greenhouse gases), which constitutes mainly carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O). By and large, agroecosystems are surveyed to straightforwardly contribute around 10–14% of complete worldwide anthropogenic GHG outflows yearly (Smith and Read 2010). This incorporates N2O emanations from soil (38% of farming’s immediate commitment) and compost (7%), enteric outflows of CH4 from ruminant animals (32%), and N2O and CH4 from biomass consumption (12%). Interactions between roots and AMF significantly altered the soil biochemical properties and greenhouse gas (GHG) emission mainly the carbon dioxide (CO2) and nitrous oxide (N2O) due to enhanced water and nutrients consumption (Frank and Groffman 2009; Jackson et al. 2008; Philippot et al. 2008). Being one of the most widespread symbiotic associations, AMF takes photo-assimilated carbon compounds from plants and in exchange increases the uptake of soil nutrients (Fellbaum et al. 2012a, b; Kiers et al. 2011). Some of the physical properties of soil, e.g. water holding capacity are changed due to AM symbiosis which influences further the soil biogeochemical processes and GHG emissions (Augé 2004; Cavagnaro et al. 2006). Prevailing soil moisture has a large influence on GHG emissions from it as it affects soil microbial communities which in turn alter various physiological and metabolic processes, e.g. gas diffusion, mineralization, nitrification, denitrification processes and oxygen availability (Blagodatsky and Smith 2012). AMF also makes plants more resistant when compared with non-mycorrhizal plants by modifying plant water relations which potentially alter the soil biogeochemical cycles and GHG emissions (Augé et al. 2001). Mycorrhizal plants absorb more water by maintaining higher stomatal conductance which results in lower soil moisture than non-mycorrhizal plants under water stress conditions (Augé et al. 2001, 2004).

13.4.1 Reduced Emission of Nitrogen by AMF There has been a marked increase in nitrogen emission in the form of nitrogen oxide (N2O) globally due to excessive use of N-based fertilizers in agricultural systems between the years 1940–2005. It is dangerous as nitrogen oxide gas has a very long perturbation lifetime, i.e. around 121 years making it to affect in the long term than other short-lived GHGs (Hartmann et al. 2013). Thus, the quick and main effort to

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accomplish the reduction in GHG emission focuses on the reduction of N2O. Arbuscular mycorrhiza fungi establish itself as one of the most extensive root-microorganism and play a major role in nitrogen uptake particularly N in inorganic form from soil to meet up requirements of plants and maintaining nitrogen cycling (Yawen and Zhu 2021). AMF impacts the accessibility of N substrates, i.e. ammonium (NH4+) and nitrate (NO3-) which result in the formation and further emission of N2O. Few studies conducted to show the effect of AMF symbiosis on N2O emissions (Veresoglou et al. 2012) have reported that AMF helps in modulation of plant nutrient and water uptake significantly altering the soil biochemical and microbial processes. AM prevents nitrogen loss in the form of nitrate leaching by facilitating its transportation to plants from soil. It is well documented that AMF mycelium can absorb both NH4+ and NO3- (Cavagnaro et al. 2006, 2012; Ngwene et al. 2013). The scaling down in N2O fluxes can also be obtained in AMF colonized plants if it absorbs more N substrates than other microbes and decreases its availability. It was observed in the studies of Zhang et al. (2015) where rice plants treated with AMF showed lower nitrogen gas emissions. Hence collective investigations concluded that AMF reduces the rate of nitrification which causes a significant reduction in N2O production and further emission.

13.4.2 Reduced Emission of Methane Gas by AMF CH4 is a much more potent greenhouse gas than carbon dioxide (IPCC 2021) and its concentration is increasing rapidly (Intergovernmental Panel on Climate Change (IPCC) 2013). Worldwide, paddy cultivation is considered as a crucial origin of climatic methane with 31 Tg year–1 during 2008–2017 which is moderately increased from the previous years 2000–2009 (IPCC 2021). Zhang et al. (2017) studied the diurnal pattern of CH4 emission from paddy fields. They observed reduction in methane emission by more than 50% in inoculated rice plots over the control at reflooding stage. AMF can indirectly contribute to methane uptake due to the increment of nitrate anions and ammonium cations that cause emergence of methane-oxidizing bacteria (Yue et al. 2020). According to them, the increase in methane uptake by Arbuscular mycorrhizae fungi is the first report in desert soil.

13.4.3 Reduced CO2 Emission by AMF AMF can offer carbon sequestration between plant and atmosphere through the shift of photosynthetic end products of the host plants to their hyphae and then in the soil (Parniske 2008; Fellbaum et al. 2012a, b). Storer et al. (2013) conducted a microcosm study of GHG fluxes in Zea mays plant and found increased aggregate CO2 fluxes in the presence of AMF hyphae. Therefore, it was prognosticated that the greenhouse gases were probably impacted by the AMF hyphae present in soils. According to Cavagnaro et al. (2012), the presence of arbuscular mycorrhizae in the roots of tomato enhanced soil CO2 efflux, but the efficacy of this greenhouse gas was

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much lesser, which suggest the optimistic role of AM-root symbiont on reducing soil GHG emissions. AMF is dependent on the host plant for their carbohydrate and energy intake. For this, they help to enhance the photosynthetic rate in the host plant which in turn stimulates the carbon sequestration (Zhu and Michael Miller 2003). Arbuscular mycorrhizae fungi have a remarkable role in C transformation into soils because they use relatively 4–20% of plant photosynthates (Tinker et al. 1994). Meta-analytic studies in legumes revealed that the photosynthetic rates increased by 14% in AMF-treated plants due to the result of C sink stimulation (Kaschuk et al. 2010).

13.5

Effect of AMF on Pest Resistance in Plants

Currently, most of the environmental scientists and plant pathologists are looking forward to the sustainable and economically favourable solutions to control plant illness and phytopathogenic insects (Begum et al. 2019). In farmland ecosystems, bacteria, nematodes, fungi and other infections are growing more and more resistant to pesticides as a result of the widespread use of chemicals, which are also polluting the environment and harming human health (Hage-Ahmed et al. 2019). Nowadays, biological control is receiving a lot of attention because of its great effectiveness, low consumption, environmental safety and variety of uses (Van Driesche et al. 2010; Gianinazzi et al. 2010; Lee et al. 2013). Current research has uncovered and utilized significant advances in utilizing (natural enemies) parasitic and predatory insects for controlling illnesses and pests Obrycki et al. (2009). Arbuscular mycorrhizal fungi (AMF), which make up the largest, most numerous and most significant group of beneficial fungi, have a specific inhibitory effect on illnesses that are transmitted through the soil (Allsup et al. 2021; Gabriele 2009). According to the studies, AMF can alter the phenotypical architecture of the root system of a plant and ameliorate the soil-root physiological and biochemical characteristics, through competing with phytopathogens for nutrient resources and entry sites and activating their protection mechanisms in plants. These effects can all regulate the production of secondary metabolites in host plants (Aseel et al. 2019). The likelihood that a plant disease will spread depends on the nature of infection, how arbuscular mycorrhizae interacts with the plants, how much and when the AMF is inoculated, and environmental factors. More than 30 AMF species have so far demonstrated their efficacy in eradicating plant soil-borne illnesses (Jung et al. 2012). AMF can lessen the harm done to Fragaria ananassa, Lycopersicon esculentum, Cucumis sativus, Olea europaea, and Medicago, Citrus reticulata, by fungus, nematodes, bacteria, and other diseases, Zea mays, Cucumis melo, Musa nana, Solanum tuberosum, truncatula, and many other plants (Allsup et al. 2021; Begum et al. 2019; Li et al. 2019; Rajak et al. 2021). Thus, research for biological control of plant diseases using AMF is tremendously beneficial from both a scientific and applied perspective.

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13.5.1 Biocontrol of Phytopathogenic Fungi Using AMF AMF live in the soil and colonize plant roots, having significant impact on the soilborne illness (Cruz et al. 2012; Li et al. 2021; Lin et al., 2021). For instance, Schönbeck and Dehne (1977) discovered that cotton plants treated with AMF were more immune to infection against Thielaviopsis basicola than the control roots. The reports also revealed that the amount of mycorrhizal infection has been inversely correlated with the amount of chlamydospores produced by Thielaviopsis basicola (Baltruschat et al. 1975). Pythium ultimum and Phytophthora megasper are two pathogenic fungi that were the subject of a 1974 study by Chou & Schmitthenner. They discovered that the frequency of plant mortality caused by P. megasper was reduced by the presence of mycorrhizal fungus. According to Sudhasha et al. (2020), the pathogenic fungus F. oxysporum was reported to be suppressed by G. intraradices; they also suggested that the chemical balance of mycorrhizae prevented harmful fungi from growing and reproducing. Fungus-like genera Fusarium, Pythium, Thielaviopsis Rhizoctonia, Macrophomina, Phoma, Sclerotium Pyrenochaeta, Cylindrocarpum, Phytophthora and Ophiobolus can cause diseases in a variety of plants, including, soybean, onion, kidney bean, peanut, barley, banana, strawberries, citrus, cotton, peach, tobacco and poplar (Bubici et al. 2019; D Aljawasim et al. 2020; Eke et al. 2020; Guzman et al. 2021). Aphanomyces euteiches-infected peas that established full AMF symbiosis were also reported to be crucial for plant defence against pathogens (Slezack et al. 2000). In tests utilizing, G. intraradices and the pathogen F. oxysporum on tomatoes Steinkellner et al. (2012), found that phosphate application and AM fungal pre-treatment together could lessen the disease’s severity.

13.5.2 Biological Control of Phytopathogenic Bacteria and Nematodes Using AMF According to research by Weaver et al. from 1975, mycorrhizal inoculation can lessen the effects of tomato bacterial wilt, a disease spread through soil that affects plants all over the world. According to Kamble and Agre (2014), the treatment of phosphorus and the inoculation of mulberries with G. fasciculatum or G. mosseae greatly decreased the incidence of P. syringae pv. Reduced Pseudomonas fluorescens on the root surface in the grape plant treated with AMF lessens the likelihood of the grape plants becoming sick again (Jung et al. 2012). By reducing the infection P. syringae in soybean, G. mosseae prevented the plant from becoming infected. Actinomycetes’ ability to infect apple seedling roots was lessened by AMF growth on those roots. The amount of T. basicola and Meloidogyne incognita propagules can be greatly reduced by pre-inoculation of tobacco with G. mosseae (Liu et al. 2012). AMF can also, to varied degrees, alleviate numerous nematodal diseases of various plant species like cucumbers, soybeans, cotton, tomatoes, alfalfa oats, citrus, kidney beans and peach by parasitizing cysts of soybean cyst nematodes (De Sá and Campos 2020; Rodrigues et al. 2021). According to Shrinkhala et al.

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(2011), AMF symbionts can increase nematode resistance in plants but cannot completely stop nematode damage, and at high concentrations, this impact is inhibitive. The impact of AMF on tomato root-knot nematodes was studied by Vos et al. (2013). After treatment, mycorrhizal inoculated plant roots had lesser galls in comparison to the control plant roots (Liu et al. 2012). However, the effectiveness of AMF disease resistance varies depending on the experimental setup and the materials employed by the researchers (Vos et al. 2013).

13.6

AMF: An Integral Essence of Sustainable Agriculture

To achieve an ample amount of crop growth, yield and quality, it is essential to reduce chemical inputs and exploit the innate mechanisms in a sustainable agricultural system (Devi et al. 2022; Siddiqui and Pichtel 2008). However, their viability in the existing ecosystem is very important along with social accountability. Edaphic parameters play an important role in sustainable agriculture by augmenting the growth of soil microbes and controlling the pathogens in the rhizosphere by increasing parasitism and antagonism mechanisms in the soil-root region of the plant (Knudsen et al. 1995). Agricultural sustainability is the eventual result of intriguing interaction of plants with microbes. Arbuscular mycorrhizal fungi are the essential mechanism for agriculture sustainability as they are native to soil and crop rhizoplane. Mycorrhizae-plant symbiotic relationships emerge as a life-sustaining association for plants especially when there is a scarcity of nutrients for plants. Nutrient components are mobilized into usable form by AM extraradical mycelium in these conditions. It has been observed and reported critically that AMF are a significant component of edaphic environments rather than mere crop root constituent as was thought earlier (Hamel and Strullu 2006). The AMF impact is very positive in less productive soil as it results in lower loss of nutrients in the surrounding environment and affects the nutrient supply, plant growth and production (Balzergue et al. 2013). Therefore, the role of AMF in escalating plant vigour and strengthening of soil structure and quality has drawn attention for its proliferation in the sustainable agricultural system. AM symbiosis helps in increasing productivity and yield with lesser chemical inputs such as insecticides, fertilizers, etc. AMF have significant contributions in soil biomass and nutrient cycling as they are extensively disseminated. Natural and organic mechanisms should be more focussed to improve crop yield in a sustainable manner by using microbes favourable for plant growth as they play a significant contribution in alleviating both biotic and abiotic stresses by assimilating both micro and macro mineral nutrients, especially phosphorus, and other like Zn, Cu, etc. (Sangwan and Prasanna 2022).

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Conclusion

The potential role of mycorrhizae cannot be ignored to maintain a sustainable agricultural system as they help in nutrient uptake. Native spores of AMF present in soil help in nutrient management, improved soil properties, crop productivity and sustainability by attacking the plant roots. In the present scenario of increased population rate, high food demand and climate change, AMF possesses a significant characteristic in lowering the detrimental consequences of pesticides, synthetic nutrients and other chemical inputs along with managing the pathogens. Being a non-detrimental and economic way to acquire higher yield, AMF helps in the development of minimum input and feasible cropping system. Mycorrhiza fungi can be assumed as an organic solution to bypass the limitations in crop cultivation. The recent and future progress and development in arbuscular mycorrhiza field research should be focussed on maximizing crop production, with special emphasis on its quality, being cost-effective with return profit, along with protecting the environment and conserving biodiversity. Interdisciplinary connections and associations of all researchers related to this field can help to overcome the associated limitations. Productivity efficiency and crop management in reliable cultivation systems should meet the essential needs as per the climate, soil and existing markets (Mattoo and Teasdale). In order to continue the productivity and optimize the sustainability of production at the same time in coming days, research and experimentation must focus more on exploring the effect of AMF in climatesmart agriculture and sustainability. In the future, for a climate-smart defensible agriculture, contemplate growth and progress can be made for achieving better food supply by identifying and ameliorating those characteristics which are associated with AMF availability, utility and climate strength in new cultivars. Competing Interests All the authors declare that they have no competing interests.

References Aljawasim BD, Khaeim MH, Manshood AM (2020) Assessment of arbuscular mycorrhizal fungi (glomus spp.) as potential biocontrol agents against damping-off disease Rhizoctonia solani on cucumber. J Crop Prot 9:141–147 Allsup CM, Lankau RA, Paige KN (2021) Herbivory and soil water availability induce changes in arbuscular mycorrhizal fungal abundance and composition. Microb Ecol 1:1–12 Aseel DG, Rashad YM, Hammad SM (2019) Arbuscular mycorrhizal fungi trigger transcriptional expression of flavonoid and chlorogenic acid biosynthetic pathways genes in tomato against tomato mosaic virus. Sci Rep 9:9692 Augé R (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381 Augé RM, Stodola AJ, Tims JE et al (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97 Baltruschat H, Schönbeck F (1975) The influence of endotrophic mycorrhiza on the infestation of tobacco by Thielaviopsis basicola. Phytopathology 84:172–188

13

Arbuscular Mycorrhizal Fungi: A Keystone to Climate-Smart Agriculture

293

Balzergue C, Chabaud M, Barker DG, Becard G, Rochange SF (2013) High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front Plant Sci 4:426 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 Blagodatsky S, Smith P (2012) Soil physics meets soil biology: towards better mechanistic prediction of greenhouse gas emissions from soil. Soil Biol Biochem 47:78–92 Bubici G, Kaushal M, Prigigallo MI, Gómez-Lama Cabanás C, Mercado-Blanco J (2019) Biological control agents against fusarium wilt of banana. Front Microbiol 10:616 Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225 Cavagnaro TR, Barrios-Masias FH, Jackson LE (2012) Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant Soil 353:181–194 Cruz AF, Ishii T (2012) Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil-borne plant pathogens. Biol Open 1:52–57 De Sá CSB, Campos MAS (2020) Arbuscular mycorrhizal fungi decrease Meloidogyne enterolobii infection of guava seedlings. J Helminthol 94:183 Devi NO, Tombisana Devi RK, Debbarma M et al (2022) Effect of endophytic bacillus and arbuscular mycorrhiza fungi (AMF) against fusarium wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici. Egypt J Biol Pest Control 32:1 Eke P, Adamou S, Fokom R, Dinango Nya V, Tsouh Fokou PV, Nana Wakam L, Nwaga D, Fekam Boyom F (2020) Arbuscular mycorrhizal fungi alter antifungal potential of lemongrass essential oil against fusarium solani, causing root rot in common bean (Phaseolus vulgaris L.). Heliyon 6: 705–737 Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012a) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109:2666–2671 Fellbaum CR, Mensah JA, Pfeffer PE, Kiers ET, Bucking H (2012b) The role of carbon in fungal nutrient uptake and transport: implications for resource exchange in the arbuscular mycorrhizal symbiosis. Plant Signal Behav 7:1509–1512 Frank DA, Groffman PM (2009) Plant rhizospheric N processes: what we don’t know and why we should care. Ecology 90:1512–1519 Gabriele B (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biot 84:11–18 Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530 Guzman A, Montes M, Hutchins L, GL DLC, Yang P, Kakouridis A, Dahlquist-Willard RM, Firestone MK, Bowles T, Kremen C (2021) Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytol 231:447–459 Hage-Ahmed K, Rosner K, Steinkellner S (2019) Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manag Sci 75:583–590 Hamel C, Strullu D-G (2006) Arbuscular mycorrhizal fungi in field crop production: potential and new direction. Can J Plant Sci 86:941–950 Hartmann DL, Klein Tank AMG, Rusticucci M, Alexander LV, Brconnimann S, Charabi Y, Dentener FJ, Dlugokencky EJ, Easterling DR, Kaplan A (2013) Observations: atmosphere and surface. Subsoil arbuscular mycorrhizal fungi for sustainability and climate-smart agriculture: a solution right under our feet. Front Microbiol 10:1–12 Intergovernmental Panel on Climate Change (IPCC) (2007) Climate change 2007. Mitigation of climate change. Cambridge Univ Press, New York, NY

294

S. Sangwan et al.

Intergovernmental Panel on Climate Change (IPCC) (2013) Climate change 2013 the physical science basis. Cambridge Univ Press, New York, NY IPCC (2021) Climate change 2021: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change Jackson LE, Burger M, Cavagnaro TR (2008) Roots, nitrogen transformations, and ecosystem services. Annu Rev Plant Biol 59:341–363 Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664 Kamble VR, Agre DG (2014) New report on AMF colonization in root parasite Striga gesnerioides and its host Lepidagathis hamiltoniana from high altitude region of Maharashtra. Int Multidiscip Res J 3:27–31 Kaschuk G, Peter AL, Ken EG, Odair A, Mariangela H, Thom WK (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol Biochem 42:125–127 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, Bucking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882 Knudsen IMB, Debosz K, Hockenhull J, Jensen DF, Elmholt S (1995) Suppressiveness of organically and conventionally managed soils towards brown foot rot of barley. Appl Soil Ecol 12:61– 72 Lazcano C, Barrios-Masias FH, Jackson LE (2014) Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biol Biochem 74:184–192 Lee EH, Eo JK, Ka KH, Eom AH (2013) Diversity of arbuscular mycorrhizal fungi and their roles in ecosystems. Mycobiology 41:121–125 Li Y, Nan Z, Duan T (2019) Rhizophagus intraradices promotes alfalfa (Medicago sativa) defense against pea aphids (Acyrthosiphon pisum) revealed by RNA-Seq analysis. Mycorrhiza 29:623– 635 Li Y, Duan T, Nan Z, Li Y (2021) Arbuscular mycorrhizal fungus alleviates alfalfa leaf spots caused by Phoma medicaginis revealed by RNA-seq analysis. J Appl Microbiol 130:547–560 Lin P, Zhang M, Wang M, Li Y, Liu J, Chen Y (2021) Inoculation with arbuscular mycorrhizal fungus modulates defense-related genes expression in banana seedlings susceptible to wilt disease. Plant Signal Behav 16:1884782 Linderman RG (1997) Vesicular- arbuscular mycorrhizal (VAM) fungi. In: Plant relationships Part B, pp 117–128 Linderman RG (2015) Vesicular-arbuscular mycorrhizae and soil microbial interactions. In: Mycorrhizae in sustainable agriculture, vol 11. ASA Special Publications, Madison, WI, pp 45–70 Liu RJ, Dai M, Wu X, Li M, Liu XZ (2012) Suppression of the root-knot nematode Meloidogyne incognita [(Kofoid & White) Chitwood] on tomato by dual inoculation with arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. Mycorrhiza 22:289–296 Ngwene B, Gabriel E, George E (2013) Influence of different mineral nitrogen sources (NO3 -N vs. NH4 + -N) on arbuscular mycorrhiza development and N transfer in a glomus intraradices–cowpea symbiosis. Mycorrhiza 23:107–111 Obrycki JJ, Harwood JD, Kring TJ, O’Neil RJ (2009) Aphidophagy by coccinellidae: application of biological control in agroecosystems. Biol Control 51:244–254 Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775 Philippot L, Hallin S, Börjesson G, Baggs EM (2008) Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81 Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220:1059–1075

13

Arbuscular Mycorrhizal Fungi: A Keystone to Climate-Smart Agriculture

295

Razak NA, Gange AC (2021) Multitrophic interactions between arbuscular mycorrhizal fungi, foliar endophytic fungi and aphids. Microb Ecol 85:1–11 Rodrigues E, Silva MT, Calandrelli A, Miamoto A, Rinaldi LK, da Moreno BP, Silva C, DiasArieira CR (2021) Pre-inoculation with arbuscular mycorrhizal fungi affects essential oil quality and the reproduction of root lesion nematode in Cymbopogon citratus. Mycorrhiza 31:613–623 Sangwan S, Prasanna R (2022) Mycorrhizae helper bacteria: unlocking their potential as bioenhancers of plant–arbuscular mycorrhizal fungal associations. Microb Ecol 84:1–10 Schönbeck F, Dehne HW (1977) Damage to mycorrhizal and nonmycorrhizal cotton seedlings by Thielaviopsis basicola. Plant Dis Rep 61:266–276 Shrinkhala M (2011) Study on the bioprotective effect of endomycorrhizae against M. graminicola in rice; laboratory of tropical crop improvement, department of biosys, faculty of bioscience engineering. Catholic University of Leuven, Leuven, Belgium Siddiqui ZA, Pichtel J (2008) Mycorrhixae: an overview. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Berlin, pp 1–35 Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant-Microbe Interact 13:238–241 Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic Press, Amsterdam Sosa-Hernández MA, Roy J, Hempel S, Kautz T, Köpke U, Uksa M (2018) Subsoil arbuscular mycorrhizal fungal communities in arable soil differ from those in topsoil. Soil Biol Biochem 117:83–86 Sosa-Hernández MA, Leifheit EF, Ingraffia R, Rillig MC (2019) Subsoil arbuscular mycorrhizal fungi for sustainability and climate-smart agriculture: a solution right under our feet? Front Microbiol 10:744 Steinkellner S, Hage-Ahmed K, García-Garrido JM, Illana A, Ocampo JA, Vierheilig H (2012) A comparison of wild-type, old and modern tomato cultivars in the interaction with the arbuscular mycorrhizal fungus glomus mosseae and the tomato pathogen fusarium oxysporum f. sp. lycopersici. Mycorrhiza 22:189–194 Storer A, Coggan P, Ineson A, Hodge (2013) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol 220:1285–1295 Sudhasha S (2020) Chapter-1 constructiveness of the biocontrol agents on Fusarial wilt of tomato incited by the destructive pathogen Fusarium oxysporum f. Sp. lycopersici. In: Current research and innovations in plant pathology. AkiNik Publications, Delhi Tinker PB, Durall DM, Jones MD (1994) Carbon use efficiency in mycorrhizas—theory and sample calculations. New Phytol 128:115–122 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. https://doi.org/10.1111/j.1461-0248.2007.01139.x Van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L, Smith L, Wagner DL, Blossey B, Brancatini V et al (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54:54 Veresoglou SD, Chen B, Rillig MC (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62 Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, GianinazziPearson V (2013) Mycorrhizainduced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54 Yawen S, Zhu B (2021) Arbuscular mycorrhizal fungi reduce soil nitrous oxide emission. Geoderma 402:115179. https://doi.org/10.1016/j.geoderma.2021.115179

296

S. Sangwan et al.

Yue P, Cui X, Zuo X, Li K, Wang S, Jia Y, Liu X (2020) The contribution of arbuscular mycorrhizal fungi to ecosystem respiration and methane flux in an ephemeral plants-dominated desert. Land Degrad Dev 32:1844–1853 Zhang S, Wang L, Ma F, Bloomfield KJ, Yang J, Atkin OK (2015) Is resource allocation and grain yield of rice altered by inoculation with arbuscular mycorrhizal fungi? J Plant Ecol 8:436–448 Zhang X, Wang L, Ma F, Yang J (2017) Effects of arbuscular mycorrhizal fungi on CH4 emissions from rice paddies. Int J Phytoremediation 19:39–45 Zhu YG, Michael Miller R (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil–plant systems. Trends Plant Sci 8:407–409

Microbial Siderophores in Sustainable Applications—Preventing and Mitigating Effects of Climate Change

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Marcin Musiałowski and Klaudia Dębiec-Andrzejewska

Abstract

Climate change is a major hazard to the environment, affecting almost every branch of human activity. The scale and dynamics of this process are rising, thus there is a rapid need for the development of effective tools to stop this critical situation. Secondary metabolites produced by microorganisms could play a vital role in combat climate change since they provide sustainable solutions for environmental issues associated with agriculture, industry and pollutant emission. Among them, microbial siderophores, commonly known as effective iron chelators, have recently attracted much attention, due to their possible use in various applications. In this review, microbial siderophores are presented as a valuable tool for preventing and mitigating the effects of climate change. In agriculture, siderophores could be used as a sustainable alternative to fertilizers and pesticides. Chelating properties of siderophores are used also in bioremediation, e.g., in removing heavy metal contaminants. Moreover, siderophores could be a base for biosensors, helping in environmental monitoring. Keywords

Siderophores · Climate change · Secondary metabolites · Chelators · Sustainable agriculture · Bioremediation

M. Musiałowski · K. Dębiec-Andrzejewska (✉) Department of Geomicrobiology, Faculty of Biology, Institute of Microbiology,, University of Warsaw, Warsaw, Poland e-mail: [email protected] # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 S. Singh et al. (eds.), Bioinoculants: Biological Option for Mitigating global Climate Change, https://doi.org/10.1007/978-981-99-2973-3_14

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M. Musiałowski and K. Dębiec-Andrzejewska

Introduction

Through millions of years of evolution, bacteria have adapted to various environmental conditions and established their vital role in diverse ecosystems. Crucial for this process was the development of versatile metabolism, which resulted in a wide array of secondary metabolites synthesized by bacteria. These multifaceted compounds caught the attention of biotechnology since it was possible to harness their potential for various industrial purposes and to combat hazards, which the modern world is facing (Pessione 2021). One of the most important challenges of the modern world is climate change and global warming, which are mainly caused by unsustainable industrial and agricultural activities, e.g., greenhouse gas emissions, burning of fossil fuel, emission of pollutants from industry, and extensive use of fertilizers and pesticides (Cavicchioli et al. 2019; Pessione 2021). The scale and dynamics of this problem call for rapid action, to prevent serious and irreversible effects damaging world welfare (Cavicchioli et al. 2019). Climate change is strongly affecting ecosystems, causing the loss of their biodiversity, due to the disturbance of the stability of ecological relations. The rapid rise of temperature and changes in other environmental conditions result in the collapse of networks of stable ecological relations, which were shaped through millions of years of evolution. This ecosystem disturbance eventually limits the number of species and their diversity. Environmental pollution enhances this process, by inhibiting the growth of entire groups of organisms, due to the toxicity of pollutants. In soil, it translates to lower qualities of microbiomes, which are crucial for crop productivity. Diverse microbes provide proper nutrition, enhance soil quality, and are a source of plant growth-promoting traits. Biotechnological use of microorganisms and their metabolites could be a valuable and important tool to mitigate the consequences of climate change since they provide sustainable solutions for maintaining soil biodiversity. In agriculture, bacterial inoculants or secondary metabolites could substitute or limit the use of chemical fertilizers, preventing soil degradation, e.g., the use of bacterial phytohormones and biosurfactants to improve croplands productivity (Padmavathi et al. 2015; Wong et al. 2015). On the other hand, they could mitigate the results of unsustainable cropland management, by restoring microbiome diversity and richness. Microbial approaches could also provide sustainable methods of pollution treatment, limiting their negative impact on the environment. In recent years, siderophores emerged as important bacterial secondary metabolites, which could be used in a wide array of environmentally friendly applications, due to their various environmental properties and roles. Thus, siderophores could become an important means of fighting climate change and global warming (Ahmed and Holmström 2014). An overview of siderophores applications in the context of the mitigation of climate change effects was presented in Fig. 14.1. In this chapter, the role of siderophores as compounds with great potential in sustainable applications was reviewed. At first, the chemistry, biology, and ecology of siderophores were described, to provide insight into the versatility of these compounds, which could be used in various sustainable approaches. Next, the

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Fig. 14.1 Overview of siderophores and siderophores producing bacteria (SPB) roles in prevention and mitigation of climate change effects by sustainable agriculture, bioremediation, and environment monitoring

utilization of siderophores in various fields, including agriculture, bioremediation, and environmental monitoring, was described in the context of preventing and mitigating the effects of climate change. Finally, current challenges and perspectives for the biotechnological use of siderophores were discussed.

14.2

Siderophores Chemistry, Biology, and Ecology

14.2.1 Siderophores—Iron Chelating Compounds Siderophores are a group of low molecular weight, chelating compounds with a high affinity for iron (III). Their main biological function is the increase of iron bioavailability in iron-limited conditions, although they are involved in other various roles, e.g., reduction of heavy metals toxicity, signaling, or ecological interactions. Due to their diversity, in terms of structure, functionality, and biological functions, they are

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of particular interest to various branches of biotechnology, especially agriculture, where they could limit the use of fertilizers, and bioremediation where they could facilitate removal and degradation of environmental pollutants (Hider and Kong 2010). Iron is an element necessary for the proper functioning of plants, animals, and bacteria. It participates in numerous redox reactions, which are crucial from the point of view of cell energy metabolism, e.g., in the transport of electrons in the respiratory chain (Miethke and Marahiel 2007). Iron occurs in the earth’s crust mainly in the form of minerals containing oxides (magnetite, hematite) or hydroxides (goethite). Although iron is abundant in the environment, the most frequently occurring form of this element is trivalent iron (Fe3+), which is not bioavailable due to its low solubility (Timofeeva et al. 2022). Thus, many organisms have developed evolutionary adaptations to increase iron bioavailability in soil and eventually increase its uptake from the environment. Among them, one of the most common adaptation strategies is biosynthesis and uptake of efficient iron chelators—siderophores (Hider and Kong 2010; Khan et al. 2018). Siderophores are produced by bacteria, fungi, or plants in conditions of iron deficiency, and then secreted into the environment, where they form soluble complex compounds with ferric iron(III) ions (Kramer et al. 2020; Liu Jiajia and Liu 2018; Suzuki et al. 2021). The high affinity of siderophores for iron is associated with the presence of negatively charged oxygen atoms. They can function as electron donors for iron(III), which is a strong acid according to Lewis’s theory, stimulating the formation of complex compounds (Hider and Kong 2010). The most common model of siderophores is the presence of three ligands containing negatively charged oxygen atoms, forming octahedral complexes with iron (III) ions which are the most stable and thermodynamically favorable (Hider and Kong 2010; Khan et al. 2018).

14.2.2 Microbial Siderophores Siderophore-producing bacteria (SPB) have been identified in a great many genera, including both gram-positive and gram-negative microorganisms. Convergent evolution, diverse genetic background, and environmental pressure resulted in great diversity in terms of structure and properties among bacterial siderophores (Khan et al. 2018; Kramer et al. 2020). The basic classification is based on the chemical characteristics of the ligands involved in the complexation of iron ions. On this basis, siderophores produced by microorganisms include (1) catechol, (2) hydroxamic, (3) carboxylic, and (4) mixed-type compounds (Kramer et al. 2020), which general chemical structures were presented in Fig. 14.2. Catechol siderophores have only been identified in bacteria. In the case of these compounds, the ligands are the catechol group, composed of an aromatic ring and two hydroxyl groups, which are the source of two negatively charged oxygen atoms involved in the complexation of iron (Fig. 14.2a). An example of catechol siderophores is enterobactin, synthesized by enterobacteria such as Escherichia coli or Salmonella typhimurium (Pollack et al. 1970; Wang and Zheng 2015).

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Fig. 14.2 Various chemical groups with negatively charged oxygen atoms are involved in the formation of siderophore-iron complexes. Common ligands in bacterial siderophores include (a) catechol groups, (b) hydroxamic groups, and (c) carboxyl groups

Hydroxamic siderophores (Fig. 14.2b) are synthesized by both bacteria (forming from alkylamines) and fungi (forming from ornithine). Hydroxamic groups are formed as derivatives of carboxylic acids in which the hydroxyl group has been replaced by a hydroxylamine residue (-NHOH). Two oxygen atoms from the hydroxamic and hydroxyl groups are involved in the formation of complex compounds. An example of compounds from this group is deferoxamine, synthesized by the bacteria Streptomyces pilosus, or fusarin C, synthesized by the fungus Aspergillus aculeatus (Telfer et al. 2019; Wolff et al. 2020). Carboxylic siderophores (Fig. 14.2c) are the least commonly identified siderophores produced by microorganisms. Oxygen-containing carboxyl and hydroxyl residues act as ligands. They are most often formed from citric acid or β-hydroxyaspartic acid. They are synthesized both by bacteria, e.g., staphyloferrin A produced by Staphylococcus aureus and by fungi, e.g., rhizoferrin produced by various Mucorales fungi (Conroy et al. 2019; Thieken and Winkelmann 1992). Mixed-type siderophores are compounds containing in their structure a combination of different ligands derived from catechol, hydroxamic, or carboxyl groups. An example is heterobactin produced by Rhodococcus erythropolis, containing both a catechol and a hydroxamic group (Retamal-Morales et al. 2021).

14.2.3 Biosynthesis, Transport, and Uptake of Bacterial Siderophores Bacterial siderophores are usually synthesized in pathways involving the action of non-ribosomal peptide synthetases (NRPS) (Carroll and Moore 2018). The biosynthesis of siderophores in this pathway is a multi-step process involving the incorporation of amino acids, carboxylic acids, or hydroxy acids into precursor peptide molecules. NRPS proteins are modular and multidomain enzymes, including adenylation, thiolation, and condensation domains, which are responsible for the formation and modification of siderophores (Barry and Challis 2009; Schalk et al. 2020). Siderophores biosynthesis pathways independent of NRPS proteins have also been identified, although they are the vast minority of molecules known so far. Pathways including synthetases (PKS) were identified, e.g., in Mycobacterium spp., Pseudomonas spp., and Yersinia spp. (Quadri 2000). PKS, similarly to NRPS, are multidomain enzymes, however, in the context of siderophores biosynthesis, full elucidation of their mechanism of action is missing (Quadri 2000). Siderophores are

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transported out of the cell by energy-intensive mechanisms associated with transport proteins or efflux pumps since their role is the uptake of an extracellular iron (Bonneau et al. 2020). Iron(III)–siderophores complexes are taken up by bacterial cells. The mechanism of this process differs between gram-negative and gram-positive bacteria. In the case of gram-negative bacteria, receptors with a β-barrel structure on the cell surface, located in the outer membrane, play a key role. They can bind specifically to certain types of siderophores, e.g., the FepA (enterobactin) receptor in E. coli (Barnard et al. 2001). The binding of the siderophore–iron(III) complex with the receptor causes changes in its conformation, which allows for further transport into the cell. It is usually mediated by ABC transport proteins or permeases and requires an energy input (in E. coli provided by the TonB complex) (Pawelek et al. 2006). The release of iron from the complex can occur through a variety of pathways. In the case of E. coli, it is released in the cytoplasm, while in Pseudomonas aeruginosa in the periplasmic space (Cornelis et al. 2009). In gram-positive bacteria, siderophore–iron complexes are often transported directly by ABC proteins into the cytoplasm, without the involvement of receptor proteins (Khan et al. 2018; Saha et al. 2013). Regulation of synthesis, secretion, and uptake of siderophores–iron(III) complexes is strictly related to intracellular iron homeostasis. Iron deficit triggers bacterial cell regulatory responses, which are focused on increasing iron uptake (Andrews et al. 2003). The best-known regulators involved in maintaining iron homeostasis are proteins from the Fur (ferric uptake regulator) family, identified in both gram-negative and gram-positive bacteria. In the context of siderophores, Fur proteins are transcription regulators, acting as repressors of their biosynthesis and regulatory proteins involved in their secretion and uptake (Hassan and Troxell 2013; de Souza and Bontempi 2020; Venturi et al. 1995). In the case of a sufficient intracellular supply of iron, Fur proteins form complexes with iron (II) ions and in this form attached to the regulatory regions of operons related to the biosynthesis and functioning of siderophores, blocking their expression. When the cell is in an irondeficient state, the Fur protein remains inactive, allowing expression of the relevant genes to be released. An additional level of regulation of siderophores biosynthesis and activity is associated with other transcription factors such as alternative sigma factors or binary systems (Hassan and Troxell 2013; de Souza and Bontempi 2020). These regulators usually respond to the presence of siderophore complexes with iron (III), further stimulating their synthesis. As a result, the activity of siderophores is enhanced in conditions that enable them to effectively absorb iron from the environment (Hider and Kong 2010; Saha et al. 2013).

14.3

Siderophores in Agriculture—Biofertilization and Biocontrol of Phytopathogens

Unsustainable agricultural practices, especially the extensive use of fertilizers and pesticides, are one of the most important causes of climate change. On the other hand, agriculture is also hardly affected by climate change, due to loss of crop

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productivity, loss of biodiversity, and increased phytopathogens infection rate. Thus, the search for sustainable alternatives for chemicals is one of the biggest challenges in modern agriculture (Crowley 2006). Due to various siderophore features, sustainable biofertilizers and bioinoculants could be based on these compounds (Ahmed and Holmström 2014). Moreover, siderophores could be used as a valuable alternative to hazardous pesticides (Khan et al. 2018).

14.3.1 Soil Biofertilization with Siderophores Iron-chelating properties of siderophores could be used to improve the bioavailability of this crucial plant element. Soil application with siderophores may increase its uptake by plants and prevent them, e.g., against iron chlorosis, characterized by the appearance of yellow leaves. The disease is a factor severely limiting crop productivity, especially in calcareous soils (Ferreira et al. 2019b; Soares 2022). Siderophores could increase plants’ supply of iron, however, the exact mechanism of action is still unknown. Two suggested mechanisms are possible: (1) a reduction of Fe(III)-siderophores complexes in the apoplast of the plants’ root and release of reduced iron ions or (2) ligand exchange between microbial siderophores and plant siderophores (Ahmed and Holmström 2014). Siderophores could be alternatives for chemical chelating agents used in agriculture, especially aminopolycarboxylic acids (APCAs), such as EDTA or EDDHA, characterized by low biodegradability and toxicity (Soares 2022). Siderophores-based biofertilizers and biostimulants could help to limit the extensive use of fertilizers in agriculture, which is crucial for preventing climate change. SPB could also have a positive impact on soil productivity, due to the stimulation of soil microbiome. Siderophores are involved in many ecological roles, which stimulate the growth of bacterial communities. These metabolites are used as signaling molecules, able to stimulate their production, or induce the expression of other genes, e.g., those related to virulence factors. Siderophores could also perform functions related to protection against the activity of reactive oxygen species (ROS—reactive oxygen species). For example, pyoverdine protects against the formation of ROS by absorbing UV radiation (Burke et al. 1990). Siderophores play an important role not only for individual cells but also for entire bacterial populations. Siderophore molecules secreted into the environment can be used not only by the cell producer but also by other cells with appropriate receptors (Kramer et al. 2020; West et al. 2007). This allows entire clonal populations to mutually benefit from the production of siderophores and increase the efficiency of iron uptake. This is particularly important in the case of biofilm-forming bacteria, which are especially beneficial for soil quality improvement (Kramer et al. 2020). Stimulation of soil microbiota is particularly beneficial for soils already affected by climate change and global warming, in which microbial community diversity has been disturbed. Examples of the use of siderophores in sustainable agriculture were summarized in Table 14.1.

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Table 14.1 Overview of siderophores use in sustainable agricultural applications Siderophore producing bacteria Pseudomonas GRP3A, Pseudomonas PRS9 Kosakonia radicincitans BA1, Stenotrophomonas maltophilia COA2 Bacillus subtilis MF497446, Pseudomonas koreensis MG209738 Pseudomonas sp. ANT_H12B, Bacillus sp. ANT_WA51 Pseudomonas aeruginosa JAS-25

Pseudomonas fluorescens NK4 Pseudomonas aeruginosa PAO1, Burkholderia cenocepacia Kocuria turfanensis 2 M4 Azotobacter vinelandii, Bacillus subtilis Pantoea cypripedii AF1, Kosakonia arachidis EF1

Effect on plants Improved growth in ironlimited conditions Improved growth

Plant species Zea mays

Inhibition of wilt caused by Cephalosporium maydis

Zea mays

Ghazy and El-Nahrawy (2021)

Improved plant growth, increased iron content

Medicago sativa

Styczynski et al. (2022)

Enhanced the seed germination, root length, shoot length, and dry weight Improved vegetative and root growth

Cicer arietinum, Cajanus cajan, Arachis hypogaea

Sulochana et al. (2014)

Cucumis sativus

Inhibition of phytopathogenic Ralstonia solanacearum Increased biomass and plant length Improved biomass and chlorophyll content

Solanum lycopersicum

AlKarablieh et al. (2022) Gu et al. (2020)

Improved growth

Saccharum spp.

Saccharum spp.

Arachis hypogaea Glycine max

Reference Sharma and Johri (2003) Singh et al. (2020)

Goswami et al. (2014) Ferreira et al. (2019a) Singh et al. (2021)

The positive influence of SPB inoculation on plants’ growth was shown in a study with Streptomyces sp. GMKU, a Oryza sativa endophyte strain (Rungin et al. 2012). SPB inoculation resulted in increased root and shoot biomass and lengths, especially in iron-deficit conditions. The potential of siderophores as an environmentally friendly biofertilizer was demonstrated with Azotobacter vinelandii and Bacillus subtilis. Iron chelated by siderophores produced by these strains was used in freezedried biofertilizer, designed to correct iron deficiencies in Glycine max (Ferreira et al. 2019a). This is currently one of the most advanced examples of the successful use of siderophore-based products in agriculture and is subjected to protection by patent law (Soares and F. C. S. E 2021). SPB could also possess other plant-growth-promoting activities. Production of siderophores has been observed in several nitrogen-fixing rhizobacteria (Singh et al. 2021; Timofeeva et al. 2022). Microorganisms possessing those characteristics are particularly promising in agriculture, since using them as a biofertilizer could

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simultaneously provide iron and nitrogen to plants. Their potential has been observed in the growth stimulation of five Saccharum species, by inoculation with root-derived endophytic nitrogen-fixing and siderophore-producing bacteria Pantoea cypripedii AF1 and Kosakonia arachidis (Singh et al. 2021). Phytohormones biosynthesis is another PGP property often coexisting with siderophores production in rhizobacteria. Potential plant growth promotion was shown for the psychrotolerant strain Pseudomonas sp. ANT_H12B, which exhibited efficient production of siderophores and indole acetic acid, a phytohormone from the auxin group. The utilization of metabolites produced by this strain resulted in increased biomass and shoot length of the alfalfa plants (Styczynski et al. 2022). Seed germination of Cicer arietinum, Cajanus cajan, and Arachis hypogaea was enhanced due to pretreatment with P. aeruginosa JAS-25 culture broth and an increase in root and shoot length as well as dry weight was observed (Sulochana et al. 2014).

14.3.2 Siderophores as a Biocontrol of Phytopathogens Agent In an iron-limited environment with diverse bacterial populations, iron uptake efficiency may be a key factor in survival. Efficient SPB have an advantage over populations of siderophores non-producers populations. The competition also takes place between different populations of siderophores producers, whose outcome is determined by various factors, such as the amount of siderophores produced or their affinity for iron (Kramer et al. 2020; Saha et al. 2016). Soil plant growth-promoting rhizobacteria (PGPR) could have an antagonistic effect against plant pathogens, due to siderophores production and winning the competition for iron resources. Due to these biocontrol properties, SPB and siderophores used in agriculture could result in the reduction of pesticide use, which is associated with environmental pollution, soil microbiome degradation, and climate change (Timofeeva et al. 2022). Biocontrol properties of SPB were shown with the use of Bacillus subtilis CAS15, which inhibited Fusarium oxysporum antagonistic activity against Capsicum annuum. In conditions of iron limitations, inoculation with Bacillus subtilis CAS15 resulted in a significant reduction of Fusarium wilt in plants and their enhanced height and yield (Yu et al. 2011). In another study, biocontrol activities were exhibited by Populus trichocarpa and Salix sitchensis endophytic bacteria. SPB from Burkholderia, Rahnella, Pseudomonas, and Curtobacterium genera inhibited the growth of phytopathogenic fungi (Kandel et al. 2017). Studies have shown the effective use of pyoverdine to reduce the population of such pathogens as Fusarium oxysporum or Erwinia carotovora (Saha et al. 2016). Despite many examples of phytopathogens growth and/or activity inhibition by siderophores described in the literature, the knowledge about detailed mechanisms of this process is still poor.

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Siderophores in Bioremediation

Environmental pollution is one of the main factors contributing to climate change. Contaminations of soil, water, and air are associated with greenhouse gases emission, air, and soil temperature increase, extreme precipitation, and erosion leading to loss of biodiversity and global warming. Various anthropogenic activities are mainly responsible for this environmental hazard, e.g., industrial production, pollution emission, or waste combustion (Cavicchioli et al. 2019; Pessione 2021). Moreover, the relationship between climate change and pollution is a vicious circle, since environmental pollution causes climate change, which eventually deepens the hazardous effect of environmental pollution. For example, according to the hydrological metal transport model, global warming could increase heavy metal flux from soils to surface waters (Wijngaard et al. 2017). Thus, remediation of the environment is one of the most important fields of combat against climate change. Unfortunately, various conventional chemical or physical methods are insufficient and unsustainable, due to the emission of secondary pollutants or high energy costs. Biological methods of remediation are emerging as a sustainable alternative. Since siderophores and SPB are exhibiting various beneficial bioremediation properties, their use in this field is strongly investigated (Ahmed and Holmström 2014). A summary of siderophores utilization in the context of bioremediation of the environment was presented in Table 14.2. Table 14.2 Overview of siderophores use in bioremediation of soil as well as waste and wastewater treatment SPB strain(s) Bacillus subtilis, Aspergillus fumigatus

Role of siderophores in bioremediation Cadmium hyperaccumulation, bioremediation of aqueous samples

Pseudomonas azotoformans

Removal of arsenic from contaminated soils

Ralstonia metallidurans CH34

Removal of zinc, copper, lead, and cadmium from contaminated soil

Marinobacter hydrocarbonoclasticus, Nitratireductor kimnyeongensis

Remediation of tannery wastewater— increasing reduction of COD and chromium, sulfate, phosphate and nitrate content by increasing bacterial survival due to mitigation of toxicity Bioweathering of asbestos waste— Degradation of chrysotile fiber, by iron removal Improving the rate of hydrocarbon degradation in the marine environment by increasing iron uptake by bacteria Stimulation of Zea mays phytoremediation— Increased accumulation of lead and chromium by plants

Pseudomonas aeruginosa

Marinobacter hydrocarbonoclasticus Pseudomonas aeruginosa

Reference Khan et al. (2020) Nair et al. (2007) Diels et al. (2002) Vijayaraj et al. (2020)

David et al. (2021) Butler et al. (2021) Braud et al. (2009)

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14.4.1 Siderophores-Mediated Heavy Metals Removal from an Environment Siderophores could be particularly important in the bioremediation of contaminations with heavy metals. Due to the presence of negatively charged oxygen atoms in the molecule of siderophores, they can form complex compounds not only with iron (III) but also with other trivalent ions, including heavy metals such as chromium (III), aluminum (III), cobalt (III) or manganese (III) (Hofmann et al. 2020; Saha et al. 2016). Under certain conditions, the affinity for heavy metals may be higher than for iron, e.g., it has been found that cobalt (III) can be chelated more efficiently than iron (III) at high pH by deferoxamine B (Neubauer et al. 2000). Additionally, it has been shown that complex compounds can also be formed from siderophores and divalent heavy metal ions, e.g., with zinc (II), cadmium (II), cobalt (II), copper (II), or nickel (II). In the case of divalent ions, the affinity of siderophores is usually lower than in the case of trivalent ones (Hofmann et al. 2020). Chelation of elements other than iron by siderophores may make significant sense for cell metabolism. Azotobactin, synthesized by Azotobacter vinelandii, is a fluorescent compound with a structure similar to pyoverdine. In addition to a very high affinity for iron, this compound forms strong complexes with molybdenum and vanadium, which are efficiently taken up into the cell. These elements play a very important role in the biology of A. vinelandii, as it is a nitrogen-fixing bacterium. The enzyme nitrogenase complex is involved in this process, in which molybdenum and vanadium play the role of important cofactors (Wichard et al. 2009). Another example is Yersinia pestis producing yersiniabactin, which acts as a versatile metallophore, involved in supplying the cell with iron, zinc, copper, and nickel (Bobrov et al. 2014; Kramer et al. 2020; Robinson et al. 2018). In most cases, complex compounds of siderophores with metals other than iron are not taken up into the cell or are taken up with much lower efficiency. In studies conducted on Pseudomonas aeruginosa, it was found that only complexes of pyoverdine or pyochelin with gallium (III), manganese (II), copper (II), and nickel (II) were transported into the cell, however, the efficiency of this process was 7–42 times lower, than in the case of iron (III) complexes. In the case of complex compounds formed with other metals, siderophores bound to receptors located in the cell membrane but were not taken up inside (Braud et al. 2010). Thanks to these properties, pyoverdine and pyochelin were able to reduce the accumulation of toxic metals in P. aeruginosa cells, which allowed the bacteria to grow intensively in the presence of high concentrations of heavy metals. The production of siderophores may therefore be a factor in increased resistance to heavy metals (Braud et al. 2010). The possibility of using siderophores for land bioremediation has been tested, e.g., in experiments related to the purification of sandy soil contaminated with heavy metals. The work involved the use of the Ralstonia metallidurans CH34 strain, which is characterized by resistance to many metals and the ability to produce siderophores. A special installation was constructed, the central part of which was a reactor called BSMR (BioMetal Sludge Reactor), in which contaminated soil was

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mixed with bacteria and nutrients (Diels et al. 2002). According to the assumptions of the experiment, siderophores were supposed to increase the solubility of heavy metals bound to soil particles. Then, the metals were to be accumulated by biomass, either by interaction with surface proteins or by bioprecipitation. As part of the experiment, it was possible to significantly reduce the level of pollutants in the ground. After cleaning the soil for 10–12 h with R. metallidurans, the concentration of zinc was reduced by 87.4%, lead by 87.8%, copper by 93.9%, and cadmium by 90% (Diels et al. 2002; Hofmann et al. 2020). Siderophores produced by the Pseudomonas azotoformans strain have been used to remove arsenic from the soil. These compounds were characterized as mixedstructure siderophores containing both catechol and hydroxamic groups. The experiment used garden soil that had been artificially contaminated with arsenic. It was eluted with siderophore solutions at a concentration of 3.88 μg/mL. The obtained results were compared with the effect of other extractants with chelating properties (citric acid and EDTA). As a result of the experiment, the highest arsenic removal efficiency was achieved with siderophores (92.8%), which significantly exceeded the results for EDTA (76.4%) and citric acid (70%) (Nair et al. 2007). It has been shown that siderophores could also contribute to heavy-metals contaminated soils by stimulation of microbial bioaccumulation. Partially purified hydroxamate siderophores produced by Aspergillus fumigatus were used to assist in the uptake of Cd by Bacillus subtilis, which possesses the capability of heavy metals intracellular accumulation (Khan et al. 2020). Cultures containing 0.5 mM of Cd B. subtilis exhibited 5.22 times greater intracellular concentration of this element when siderophores were added than in cultures without siderophores addition. Since B. subtilis possesses receptors for exogenous siderophores uptake, it was possible to use chelators produced by fungal strain. These results show that bioremediation strategies combining efficient siderophores produced with hyperaccumulators of heavy metals could be effective bioremediation strategies (Khan et al. 2020).

14.4.2 Siderophores-Mediated Waste Treatment Siderophores could be used as also a useful tool for industrial waste management and bioremediation, limiting environmental hazards associated with conventional treatment methods. Pyoverdine produced by Pseudomonas fluorescens has been used to bioleach ore residues from uranium mines. With this strategy, it was possible to mobilize iron, nickel, and cobalt from mine tailings (Edberg et al. 2010). Studies have also shown the potential of siderophores to mobilize radioactive elements such as uranium. In turn, hydroxamic siderophores produced by bacteria from the Atlantic Ocean are characterized by a particularly high affinity for polonium and protactinium (Chuang et al. 2013; Edberg et al. 2010). Marine siderophore-producing bacteria were successfully used for the treatment of tannery wastewater (Vijayaraj et al. 2020). Most notably, Marinobacter hydrocarbonoclasticus and Nitratireductor kimnyeongensis demonstrated the capability to reduce pollution indicators in wastewater by significant reduction (57–88%)

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of COD and chromium, sulfate, phosphate, and nitrate content. Siderophores indirectly stimulated the remediation process, due to the improvement of nutrient acquisition and detoxification of heavy metals present in wastewater (Vijayaraj et al. 2020). Asbestos-containing wastes (ACW) are an environmental and health threat, causing toxic effects in humans. Pyoverdine and pyochelin produced by Pseudomonas aeruginosa have been used to bio-ventilate asbestos. Chrysotile is one of the types of minerals classified as asbestos. It is made of silicate fibers whose structure is maintained with the use of iron. By removing this element from chrysotile, siderophores led to its degradation, which resulted in a significant reduction in its toxicity (David et al. 2021). Further improvement of siderophores-mediated asbestos bioweathering was achieved by P. aeruginosa PAO1 pyoverdine production engineering. Transcriptional regulator overexpression resulted in siderophores production independent of the iron level in the medium. Obtained modified strain P. aeruginosa PaM1 exhibited a significantly increased rate of iron and magnesium removal from flocking asbestos waste, which is associated with its degradation and reduction of toxicity (Lemare et al. 2022). Metal chelating properties of siderophores could be used for the treatment of electronic wastes, which contain large amounts of rare earth elements (REE). REE are a group of 17 metals naturally found in the environment, including 15 lanthanides, scandium, and yttrium, which are widely applied in industry and electronic devices, due to their unique physicochemical properties (Charalampides et al. 2015; Mikołajczak et al. 2017). Since mining of REE is challenging and unsustainable and electronic wastes are hazardous for the environment, there is a need for the development of sustainable approaches for REE recovery from waste and siderophores that could be applied in this field. Siderophores have been shown as compounds with the ability to efficiently mobilize REE, e.g., lithium and molybdenum. Further development of this approach could result in low cost and environmentally friendly techniques for REE recovery (Charalampides et al. 2015). In recent years, it has been shown that siderophores can also play a role in the degradation of organic compounds, e.g., petroleum hydrocarbons in marine environments. Microorganisms involved in the degradation of petroleum compounds also need iron for proper growth, however, in a polluted marine environment, there is often a deficit of bioavailable forms of this element. Siderophores produced by marine bacteria that degrade petroleum compounds may indirectly play a very important role in the bioremediation process, by supplying these microorganisms with iron and stimulating their activity (Ahmed and Holmström 2014). Petrobactin produced by Marinobacter hydrocarbonoclasticus was the first characterized siderophore, produced by marine bacteria that degrade petroleum hydrocarbons. Its specific feature is photoreactivity. As a result of the action of natural sunlight, iron (III) is reduced to the bioavailable form of iron (II) (Butler et al. 2021). Another interesting example of siderophores produced by marine bacteria degrading petroleum hydrocarbons is the amphiphilic ochrobactinates synthesized by Vibrio spp. isolated from the Gulf of Mexico after the Deepwater Horizon oil spill (Kem et al. 2014).

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14.4.3 Siderophore-Assisted Phytoremediation Phytoremediation is the use of plants to remove pollutants from the environment by, e.g., uptake of metals by hyperaccumulating plants (Simmer and Schnoor 2022). Bacteria-producing siderophores can also be used to enhance the efficiency of phytoremediation of land contaminated with heavy metals. This can be done through an indirect mechanism, related to increasing plant tolerance to heavy metals, mainly due to increased biomass, and a direct mechanism, related to increasing the bioavailability of heavy metals and their accumulation (Rajkumar et al. 2009). Many studies have shown a positive effect of bacterial siderophores on the supply of plants with iron, which is a potential application in agriculture and positively affects the yield of plants. However, also in the case of plants growing on soils contaminated with heavy metals, siderophores improved their condition and stimulated intensive growth. Higher plant biomass is also an advantage for phytoremediation, as it allows plants to accumulate greater amounts of heavy metals without causing toxicity to the organism (Ma et al. 2011; Rajkumar et al. 2009; Thijs et al. 2017). It was also shown that siderophores, due to the binding of various metals, reduce the formation of reactive oxygen species in the rhizosphere. This protects the phytohormones produced by PGPR against degradation and allows them to stimulate plants’ growth (Dimpka et al. 2009). One of the most important aspects affecting the effectiveness of phytoremediation is the bioavailability of heavy metals in the soil. The ability of siderophores to complex and mobilize metals increases the ability of plants to accumulate pollutants (Rajkumar et al. 2009). As a result of adding the Pseudomonas aeruginosa strain to the contaminated soil, a significant increase in the amount of bioavailable chromium and lead was observed, which was associated with the production of pyoverdine and pyochelin. In addition, an increased accumulation of these metals in the shoots of Zea mays was demonstrated compared to control samples in which the soil was not enriched with the tested strain (Braud et al. 2009). However, the biotechnology of siderophore-assisted phytoremediation requires further research as it has been shown to reduce the efficiency of the process in some cases. In the case of Phaseolus vulgaris, soil inoculation with metal-resistant and siderophore-producing strain Pseudomonas putida KNP9 stimulated plant growth in a polluted environment but reduced the accumulation of chromium and lead. These results suggest that the mechanisms involved in the uptake of heavy metals by bacterial siderophores are strongly related to plant species and environmental conditions (Tripathi et al. 2005).

14.5

Siderophores as Biosensors in Environmental Pollution Monitoring

Biosensors are simple and compact devices, consisting of the biological detection component, which is coupled with a single conversion unit, which transduces it to signal (most often electrochemical or optical). Siderophores have been recently developed as biosensors, which could be used in various applications, including

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monitoring of environmental contamination with heavy metals antibiotics or pesticides. Since these pollutions disturb ecosystems and contribute to climate change, precise detection is crucial for the implementation of an efficient remediation strategy. The development of siderophore-based biosensors could provide a valuable tool for environmental pollution monitoring (Nosrati et al. 2018; Soares 2022). Due to chelating properties, the most common use of siderophore-based sensors is to detect metal ions. Fluorescent pyoverdine produced by Pseudomonas aeruginosa PA1 has been used to develop biosensors for the detection of copper ions in water, seawater, and biosamples (Yin et al. 2016). It is based on the detection of fluorescence quenching, which is correlated with the amount of chelated copper in neutral conditions. Due to the optimization of the procedure, the biosensor was able to detect selectively even 50 nM of copper. Catechol siderophore 2,3-dihydroxybenzoyl glycine produced by Bacillus subtilis NRRL B-1471 was conjugated with a surface of magnetic iron particles to design nanobiosensor for aluminum detection (Raju et al. 2017). Due to the formation of a unique fluorogenic probe, it was able to specifically detect even 20 nM. Since this biosensor is nontoxic, it was used to stain and detect in vivo by fluorescence microscopy Al3+ ions in Artemia (brine shrimp), which could be regarded as a biomarker of water pollution. The ability of siderophores to monitor organic pollutants was shown by the design of biosensors for furazolidone detection (Yin et al. 2014). Furazolidone is used as a pesticide and antibiotic in veterinary for the treatment of animal infections, thus its large residuals are present in the environment. The pyoverdine-based biosensor was developed, in which fluorescence quenching was observed in the presence of furazolidone, which probably occurred as an effect of electron transfer from a siderophore to a pesticide. Furazolidone was detected with high sensitivity, with 0.5 μM as a limit of detection in aquatic samples.

14.6

Future Perspectives

Siderophores have been shown in numerous studies as compounds with the potential for broad sustainable applications in environmental biotechnology, which could contribute to combating climate change. However, there is still a need for the development of the science behind siderophores application, because currently, the number of successful commercialization of siderophores-based products is scarce. Among the biggest challenges is ensuring the reproducibility and predictability of siderophores-based products’ efficiency, which is limited by existing knowledge gaps. Current works show the potential of siderophores in plant growth promotion and bioremediation however there is still a need for research elucidating mechanisms of siderophores’ actions in both applications, e.g., interactions between these compounds, plants, and soil matrix could be more profoundly investigated. Additionally, a more precise analysis of the chemical structure of various siderophores

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could contribute to a better understanding and prediction of the environmental behavior of siderophores. Identification of siderophores production in most works is based on spectrophotometrically non-specific tests, e.g., CAS assay, whereas more insightful methods like High-Performance Liquid Chromatography (HPLC) with appropriate mass detectors (MS) or Nuclear Magnetic Resonance (NMR) are highly sought (Timofeeva et al. 2022). Progress in the field of biotechnology of siderophores production is also in high demand. Due to the strict relation between iron level and regulation of biosynthesis, siderophores production media must have controlled composition and the use of inexpensive substrates, e.g., waste materials, is not possible. Thus, to maximize siderophores production and make it economically feasible, research regarding the optimization of this process is highly sought. Moreover, research regarding the genetic modification of SPB to increase siderophores production could be beneficial for the development of this field of biotechnology.

14.7

Summary

Siderophores have been proven in numerous studies as versatile compounds, whose applications are beyond just metal chelation. It has been already established that siderophores could play significant roles in sustainable development, by providing alternatives to conventional fertilization, crop, protection and bioremediation approaches. However, siderophores-based technologies are still in the development phase and there is a need for comprehensive research of their mode of action, chemistry, and structure, especially in the context of potential sustainable applications. Acknowledgments The studies related to the investigation of bacterial siderophores’ potential in agricultural and bioremediation applications were realized in the frame of the LIDER XI project supported by the National Center for Research and Development (Poland). Grant no. LIDER/13/ 0051/L-11/NCBR/2020. Competing Interests All the authors declare that they have no competing interests.

References Ahmed E, Holmström SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7(3):196–208. https://doi.org/10.1111/1751-7915.12117 Al-Karablieh N, Al-Shomali I, Al-Elaumi L, Hasan K (2022) Pseudomonas fluorescens NK4 siderophore promotes plant growth and biocontrol in cucumber. J Appl Microbiol 133(3): 1414–1421. https://doi.org/10.1111/jam.15645 Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27(2–3):215–237. https://doi.org/10.1016/S0168-6445(03)00055-X Barnard TJ, Watson ME Jr, McIntosh MA (2001) Mutations in the Escherichia coli receptor Fep A reveal residues involved in ligand binding and transport. Mol Microbiol 41(3):527–536. https:// doi.org/10.1046/j.1365-2958.2001.02473.x

14

Microbial Siderophores in Sustainable Applications—Preventing. . .

313

Barry SM, Challis GL (2009) Recent advances in siderophore biosynthesis. Curr Opin Chem Biol 13(2):205–215. https://doi.org/10.1016/j.cbpa.2009.03.008 Bobrov AG, Kirillina O, Fetherston JD, Miller MC, Burlison JA, Perry RD (2014) The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicaemic plague in mice. Mol Microbiol 93(4):759–775. https://doi.org/10.1111/mmi.12693 Bonneau A, Roche B, Schalk IJ (2020) Iron acquisition in Pseudomonas aeruginosa by the siderophore pyoverdine: an intricate interacting network including periplasmic and membrane proteins. Sci Rep 10(1):120. https://doi.org/10.1038/s41598-019-56913-x Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Crand Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74(2):280–286. https://doi.org/10.1016/j.chemosphere.2008.09.013 Braud A, Geoffroy V, Hoegy F, Mislin GLA, Schalk IJ (2010) Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environ Microbiol Rep 2(3): 419–425. https://doi.org/10.1111/j.1758-2229.2009.00126.x Burke RM, Upton ME, McLoughlin AJ (1990) Influence of pigment production on resistance to ultraviolet irradiation in Pseudomonas aeruginosa ATCC 10145. Ir J Food Sci Technol 14(1): 51–60; http://www.jstor.org/stable/25558203 Butler A, Harder T, Ostrowski AD, Carrano CJ (2021) Photoactive siderophores: structure, function and biology. J Inorg Biochem 221:111457. https://doi.org/10.1016/j.jinorgbio.2021.111457 Carroll CS, Moore MM (2018) Ironing out siderophore biosynthesis: a review of non-ribosomal peptide synthetase (NRPS)-independent siderophore synthetases. Crit Rev Biochem Mol Biol 53(4):356–381. https://doi.org/10.1080/10409238.2018.1476449 Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Behrenfeld MJ, Boetius A, Boyd PW, Classen AT, Crowther TW, Danovaro R, Foreman CM, Huisman J, Hutchins DA, Jansson JK, Karl DM, Koskella B, Mark Welch DB, Webster NS (2019) Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17(9):569–586. https://doi. org/10.1038/s41579-019-0222-5 Charalampides G, Vatalis KI, Apostoplos B, Ploutarch-Nikolas B (2015) Rare earth elements: industrial applications and economic dependency of Europe. Proc Econ Fin 24:126–135. https:// doi.org/10.1016/S2212-5671(15)00630-9 Chuang C-Y, Santschi PH, Ho Y-F, Conte MH, Guo L, Schumann D, Ayranov M, Li Y-H (2013) Role of biopolymers as major carrier phases of Th, pa, Pb, Po, and be radionuclides in settling particles from the Atlantic Ocean. Mar Chem 157:131–143. https://doi.org/10.1016/j.marchem. 2013.10.002 Conroy BS, Grigg JC, Kolesnikov M, Morales LD, Murphy MEP (2019) Staphylococcus aureus heme and siderophore-iron acquisition pathways. Biometals 32(3):409–424. https://doi.org/10. 1007/s10534-019-00188-2 Cornelis P, Matthijs S, van Oeffelen L (2009) Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22(1):15–22. https://doi.org/10.1007/s10534-008-9193-0 Crowley DE (2006) Microbial siderophores in the plant rhizosphere. In: Barton Larry L, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 169–198. https://doi.org/10.1007/1-4020-4743-6_8 David SR, Jaouen A, Ihiawakrim D, Geoffroy VA (2021) Biodeterioration of asbestos cement by siderophore-producing pseudomonas. J Hazard Mater 403:123699. https://doi.org/10.1016/j. jhazmat.2020.123699 de Souza SRER, Bontempi BB, da SNJ F (2020) Ferric uptake regulator fur coordinates siderophore production and defense against iron toxicity and oxidative stress and contributes to virulence in Chromobacterium violaceum. Appl Environ Microbiol 86(21):e01620–e01620. https://doi.org/ 10.1128/AEM.01620-20

314

M. Musiałowski and K. Dębiec-Andrzejewska

Diels L, van der Lelie N, Bastiaens L (2002) New developments in treatment of heavy metal contaminated soils. Rev Environ Sci Biotechnol 1(1):75–82. https://doi.org/10.1023/ A:1015188708612 Dimpka C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694. https://doi.org/10.1111/j.1365-3040.2009. 02028.x Edberg F, Kalinowski BE, Holmstrom SJM, Holm K (2010) Mobilization of metals from uranium mine waste: the role of pyoverdines produced by Pseudomonas fluorescens. Geobiology 8(4): 278–292. https://doi.org/10.1111/j.1472-4669.2010.00241.x Ferreira CMH, López-Rayo S, Lucena JJ, Soares EV, Soares HMVM (2019a) Evaluation of the efficacy of two new biotechnological-based freeze-dried fertilizers for sustainable Fe deficiency correction of soybean plants grown in calcareous soils. Front Plant Sci 10:1335. https://doi.org/ 10.3389/fpls.2019.01335 Ferreira CMH, Soares HMVM, Soares EV (2019b) Promising bacterial genera for agricultural practices: an insight on plant growth-promoting properties and microbial safety aspects. Sci Total Environ 682:779–799. https://doi.org/10.1016/j.scitotenv.2019.04.225 Ghazy N, El-Nahrawy S (2021) Siderophore production by Bacillus subtilis MF497446 and Pseudomonas koreensis MG209738 and their efficacy in controlling Cephalosporium maydis in maize plant. Arch Microbiol 203(3):1195–1209. https://doi.org/10.1007/s00203-02002113-5 Goswami D, Pithwa S, Dhandhukia P, Thakker JN (2014) Delineating Kocuria turfanensis 2M4 as a credible PGPR: a novel IAA-producing bacteria isolated from saline desert. J Plant Interact 9(1):566–576. https://doi.org/10.1080/17429145.2013.871650 Gu S, Wei Z, Shao Z, Friman V-P, Cao K, Yang T, Kramer J, Wang X, Li M, Mei X, Xu Y, Shen Q, Kümmerli R, Jousset A (2020) Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol 5(8):1002–1010. https://doi.org/10.1038/s41564-0200719-8 Hassan H, Troxell B (2013) Transcriptional regulation by ferric uptake regulator (fur) in pathogenic bacteria. Front Cell Infect Microbiol 3:59. https://doi.org/10.3389/fcimb.2013.00059 Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27(5):637–657. https://doi.org/10.1039/B906679A Hofmann M, Retamal-Morales G, Tischler D (2020) Metal binding ability of microbial natural metal chelators and potential applications. Nat Prod Rep 37(9):1262–1283. https://doi.org/10. 1039/C9NP00058E Jiajia L, Liu G (2018) Analysis of secondary metabolites from plant endophytic fungi. In: Wenbo, Wolpert (eds) Plant pathogenic fungi and oomycetes: methods and protocols. Springer, New York, NY, pp 25–38. https://doi.org/10.1007/978-1-4939-8724-5_3 Kandel SL, Firrincieli A, Joubert PM, Okubara PA, Leston ND, McGeorge KM, Mugnozza GS, Harfouche A, Kim S-H, Doty SL (2017) An in vitro study of bio-control and plant growth promotion potential of salicaceae endophytes. Front Microbiol 8:386. https://doi.org/10.3389/ fmicb.2017.00386 Kem MP, Zane HK, Springer SD, Gauglitz JM, Butler A (2014) Amphiphilic siderophore production by oil-associating microbes. Metallomics 6(6):1150–1155. https://doi.org/10.1039/ c4mt00047a Khan A, Singh P, Srivastava A (2018) Synthesis, nature and utility of universal iron chelator— siderophore: a review. Microbiol Res 212–213:103–111. https://doi.org/10.1016/j.micres.2017. 10.012 Khan A, Gupta A, Singh P, Mishra AK, Ranjan RK, Srivastava A (2020) Siderophore-assisted cadmium hyperaccumulation in Bacillus subtilis. Int Microbiol 23(2):277–286. https://doi.org/ 10.1007/s10123-019-00101-4 Kramer J, Özkaya Ö, Kümmerli R (2020) Bacterial siderophores in community and host interactions. Nat Rev Microbiol 18(3):152–163. https://doi.org/10.1038/s41579-019-0284-4

14

Microbial Siderophores in Sustainable Applications—Preventing. . .

315

Lemare M, Puja H, David SR, Mathieu S, Ihiawakrim D, Geoffroy VA, Rigouin C (2022) Engineering siderophore production in pseudomonas to improve asbestos weathering. Microb Biotechnol 15(9):2351–2363. https://doi.org/10.1111/1751-7915.14099 Ma Y, Prasad MN, v, Rajkumar, M., Freitas, H. (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258. https://doi.org/10.1016/j.biotechadv.2010.12.001 Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71(3):413–451. https://doi.org/10.1128/MMBR.00012-07 Mikołajczak P, Borowiak K, Niedzielski P (2017) Phytoextraction of rare earth elements in herbaceous plant species growing close to roads. Environ Sci Pollut Res 24(16): 14091–14103. https://doi.org/10.1007/s11356-017-8944-2 Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Pollut 180(1):199–212. https://doi.org/10.1007/s11270-006-9263-2 Neubauer U, Nowack B, Furrer G, Schulin R (2000) Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environ Sci Technol 34(13):2749–2755. https://doi.org/ 10.1021/es990495w Nosrati R, Dehghani S, Karimi B, Yousefi M, Taghdisi SM, Abnous K, Alibolandi M, Ramezani M (2018) Siderophore-based biosensors and nanosensors; new approach on the development of diagnostic systems. Biosens Bioelectron 117:1–14. https://doi.org/10.1016/j.bios.2018.05.057 Padmavathi AR, Bakkiyaraj D, Pandian SK (2015) Significance of biosurfactants as antibiofilm agents in eradicating phytopathogens. In: Maheshwari DK (ed) Metabolites in sustainable agroecosystem. Bacterial Springer International Publishing, Cham, pp 319–336. https://doi. org/10.1007/978-3-319-24654-3_12 Pawelek PD, Croteau N, Ng-Thow-Hing C, Khursigara CM, Moiseeva N, Allaire M, Coulton JW (2006) Structure of ton B in complex with Fhu A, E coli outer membrane receptor. Science 312(5778):1399–1402. https://doi.org/10.1126/science.1128057 Pessione E (2021) The less expensive choice: bacterial strategies to achieve successful and sustainable reciprocal interactions. Front Microbiol 11:571417. https://doi.org/10.3389/fmicb. 2020.571417 Pollack JR, Ames BN, Neilands JB (1970) Iron transport in Salmonella typhimurium: mutants blocked in the biosynthesis of enterobactin. J Bacteriol 104(2):635–639. https://doi.org/10. 1128/jb.104.2.635-639.1970 Quadri LEN (2000) Assembly of aryl-capped siderophores by modular peptide synthetases and polyketide synthases. Mol Microbiol 37(1):1–12. https://doi.org/10.1046/j.1365-2958.2000. 01941.x Rajkumar M, Prasad MNV, Freitas H, Ae N (2009) Biotechnological applications of serpentine soil bacteria for phytoremediation of trace metals. Crit Rev Biotechnol 29(2):120–130. https://doi. org/10.1080/07388550902913772 Raju M, Srivastava S, Nair RR, Raval IH, Haldar S, Chatterjee PB (2017) Siderophore coated magnetic iron nanoparticles: rational designing of water soluble nanobiosensor for visualizing Al3+ in live organism. Biosens Bioelectron 97:338–344. https://doi.org/10.1016/j.bios.2017. 06.013 Retamal-Morales G, Senges CHR, Stapf M, Olguín A, Modak B, Bandow JE, Tischler D, Schlömann M, Levicán G (2021) Isolation and characterization of arsenic-binding siderophores from Rhodococcus erythropolis S43: role of heterobactin B and other heterobactin variants. Appl Microbiol Biotechnol 105(4):1731–1744. https://doi.org/10.1007/s00253-021-11123-2 Robinson AE, Lowe JE, Koh E-I, Henderson JP (2018) Uropathogenic enterobacteria use the yersiniabactin metallophore system to acquire nickel. J Biol Chem 293(39):14953–14961. https://doi.org/10.1074/jbc.RA118.004483 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

316

M. Musiałowski and K. Dębiec-Andrzejewska

thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek 102(3): 463–472. https://doi.org/10.1007/s10482-012-9778-z Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53(4):303–317. https://doi.org/10.1002/jobm.201100552 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(5):3984–3999. https://doi. org/10.1007/s11356-015-4294-0 Schalk IJ, Rigouin C, Godet J (2020) An overview of siderophore biosynthesis among fluorescent pseudomonads and new insights into their complex cellular organization. Environ Microbiol 22(4):1447–1466. https://doi.org/10.1111/1462-2920.14937 Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158(3):243–248. https://doi.org/10.1078/0944-5013-00197 Simmer RA, Schnoor JL (2022) Phytoremediation, bioaugmentation, and the plant microbiome. Environ Sci Technol 56(23):16602–16610. https://doi.org/10.1021/acs.est.2c05970 Singh RK, Singh P, Li H-B, Guo D-J, Song Q-Q, Yang L-T, Malviya MK, Song X-P, Li Y-R (2020) Plant-PGPR interaction study of plant growth-promoting diazotrophs Kosakonia radicincitans BA1 and Stenotrophomonas maltophilia COA2 to enhance growth and stressrelated gene expression in Saccharum spp. J Plant Interact 15(1):427–445. https://doi.org/10. 1080/17429145.2020.1857857 Singh RK, Singh P, Guo D-J, Sharma A, Li D-P, Li X, Verma KK, Malviya MK, Song X-P, Lakshmanan P, Yang L-T, Li Y-R (2021) Root-derived endophytic diazotrophic bacteria Pantoea cypripedii AF1 and Kosakonia arachidis EF1 promote nitrogen assimilation and growth in sugarcane. Front Microbiol 12:774707. https://doi.org/10.3389/fmicb.2021.774707 Soares E (2022) Perspective on the biotechnological production of bacterial siderophores and their use. Appl Microbiol Biotechnol 106(11):3985–4004. https://doi.org/10.1007/s00253-02211995-y Soares HMVM, F. C. S. E (2021). Lyophilized fertilizer composition including iron siderophore chelates, lyophilized composition including siderophores, their processes of preparation and their uses in treating plants (patent no. EP 19817824.6) Styczynski M, Biegniewski G, Decewicz P, Rewerski B, Debiec-Andrzejewska K, Dziewit L (2022) Application of psychrotolerant Antarctic bacteria and their metabolites as efficient plant growth promoting agents. Front Bioeng Biotechnol 10:772891. https://doi.org/10.3389/ fbioe.2022.772891 Sulochana MB, Jayachandra SY, Kumar SA, Parameshwar AB, Reddy KM, Dayanand A (2014) Siderophore as a potential plant growth-promoting agent produced by Pseudomonas aeruginosa JAS-25. Appl Biochem Biotechnol 174(1):297–308. https://doi.org/10.1007/s12010-0141039-3 Suzuki M, Urabe A, Sasaki S, Tsugawa R, Nishio S, Mukaiyama H, Murata Y, Masuda H, Aung MS, Mera A, Takeuchi M, Fukushima K, Kanaki M, Kobayashi K, Chiba Y, Shrestha BB, Nakanishi H, Watanabe T, Nakayama A, Namba K (2021) Development of a mugineic acid family phytosiderophore analog as an iron fertilizer. Nat Commun 12(1):1558. https://doi.org/ 10.1038/s41467-021-21837-6 Telfer TJ, Richardson-Sanchez T, Gotsbacher MP, Nolan KP, Tieu W, Codd R (2019) Analogues of desferrioxamine B (DFOB) with new properties and new functions generated using precursordirected biosynthesis. Biometals 32(3):395–408. https://doi.org/10.1007/s10534-019-00175-7 Thieken A, Winkelmann G (1992) Rhizoferrin: a complexone type siderophore of the mocorales and entomophthorales (Zygomycetes). FEMS Microbiol Lett 94(1–2):37–41. https://doi.org/10. 1111/j.1574-6968.1992.tb05285.x Thijs S, Sillen W, Weyens N, Vangronsveld J (2017) Phytoremediation: state-of-the-art and a key role for the plant microbiome in future trends and research prospects. Int J Phytoremediation 19(1):23–38. https://doi.org/10.1080/15226514.2016.1216076

14

Microbial Siderophores in Sustainable Applications—Preventing. . .

317

Timofeeva AM, Galyamova MR, Sedykh SE (2022) Bacterial siderophores: classification, biosynthesis, perspectives of use in agriculture. Plan Theory 11(22):3065. https://doi.org/10.3390/ plants11223065 Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R (2005) Isolation and functional characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas putida KNP9. Curr Microbiol 50(5):233–237. https://doi.org/10.1007/s00284-004-4459-4 Venturi V, Weisbeek P, Koster M (1995) Gene regulation of siderophore-mediated iron acquisition in pseudomonas: not only the fur repressor. Mol Microbiol 17(4):603–610. https://doi.org/10. 1111/j.1365-2958.1995.mmi_17040603.x Vijayaraj AS, Mohandass C, Joshi D (2020) Microremediation of tannery wastewater by siderophore producing marine bacteria. Environ Technol 41(27):3619–3632. https://doi.org/ 10.1080/09593330.2019.1615995 Wang J, Zheng P (2015) Muconic acid production from glucose using enterobactin precursors in Escherichia coli. J Ind Microbiol Biotechnol 42(5):701–709. https://doi.org/10.1007/s10295014-1581-6 West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007) The social lives of microbes. Annu Rev Ecol Evol Syst 38(1):53–77. https://doi.org/10.1146/annurev.ecolsys.38.091206.095740 Wichard T, Bellenger J-P, Morel FMM, Kraepiel AML (2009) Role of the siderophore azotobactin in the bacterial acquisition of nitrogenase metal cofactors. Environ Sci Technol 43(19): 7218–7224. https://doi.org/10.1021/es8037214 Wijngaard RR, van der Perk M, van der Grift B, de Nijs TCM, Bierkens MFP (2017) The impact of climate change on metal transport in a lowland catchment. Water Air Soil Pollut 228(3):107. https://doi.org/10.1007/s11270-017-3261-4 Wolff PB, Nielsen ML, Slot JC, Andersen LN, Petersen LM, Isbrandt T, Holm DK, Mortensen UH, Nødvig CS, Larsen TO, Hoof JB (2020) Acurin A, a novel hybrid compound, biosynthesized by individually translated PKS- and NRPS-encoding genes in Aspergillus aculeatus. Fungal Genet Biol 139:103378. https://doi.org/10.1016/j.fgb.2020.103378 Wong WS, Tan SN, Ge L, Chen X, JWH Y (2015) The importance of phytohormones and microbes in biofertilizers. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agroecosystem. Springer International Publishing, Cham, pp 105–158. https://doi.org/10.1007/978-3-31924654-3_6 Yin K, Zhang W, Chen L (2014) Pyoverdine secreted by Pseudomonas aeruginosa as a biological recognition element for the fluorescent detection of furazolidone. Biosens Bioelectron 51:90– 96. https://doi.org/10.1016/j.bios.2013.07.038 Yin K, Wu Y, Wang S, Chen L (2016) A sensitive fluorescent biosensor for the detection of copper ion inspired by biological recognition element pyoverdine. Sensors Actuators B Chem 232:257– 263. https://doi.org/10.1016/j.snb.2016.03.128 Yu X, Ai C, Xin L, Zhou G (2011) The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on fusarium wilt and promotes the growth of pepper. Eur J Soil Biol 47(2):138–145. https://doi.org/10.1016/j.ejsobi.2010.11.001