Advances in Plant Microbiome and Sustainable Agriculture: Diversity and Biotechnological Applications [1st ed.] 9789811532078, 9789811532085

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Microorganisms for Sustainability 19 Series Editor: Naveen Kumar Arora

Ajar Nath Yadav Ali Asghar Rastegari Neelam Yadav Divjot Kour  Editors

Advances in Plant Microbiome and Sustainable Agriculture Diversity and Biotechnological Applications

Microorganisms for Sustainability Volume 19

Series editor Naveen Kumar Arora, Environmental Microbiology, School for Environmental Science, Babasaheb Bhimrao Ambedkar University, Lucknow, Uttar Pradesh, India

More information about this series at http://www.springer.com/series/14379

Ajar Nath Yadav  •  Ali Asghar Rastegari Neelam Yadav • Divjot Kour Editors

Advances in Plant Microbiome and Sustainable Agriculture Diversity and Biotechnological Applications

Editors Ajar Nath Yadav Department of Biotechnology Eternal University Sirmour, Himachal Pradesh, India Neelam Yadav Food Nutrition and Engineering Veer Bahadur Singh Purvanchal University Ghazipur, Uttar Pradesh, India

Ali Asghar Rastegari Department of Molecular and Cell Biochemistry Islamic Azad University Isfahan, Iran Divjot Kour Department of Biotechnology Eternal University Sirmour, Himachal Pradesh, India

ISSN 2512-1901     ISSN 2512-1898 (electronic) Microorganisms for Sustainability ISBN 978-981-15-3207-8    ISBN 978-981-15-3208-5 (eBook) https://doi.org/10.1007/978-981-15-3208-5 © Springer Nature Singapore Pte Ltd. 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Foreword

Microbes are ubiquitous in nature. The vast microbial diversity has been found to associate with the plant systems. The plant-microbe interactions are the key strategy to colonize and establish in a variety of diverse habitats. Microbes are associated in three ways with any plant systems in the form of epiphyte, endophyte, and rhizosphere, which are collectively termed as plant microbiomes. Plant microbiomes play an important role in the growth and development of plants and in the health of soil. The rhizospheric soil is a valuable natural resource harboring hotspots of microbes and plays critical roles in the maintenance of global nutrient balance and ecosystem function. The rhizospheric microbial diversity present in rhizospheric zones has a sufficient amount of nutrients release by plant root systems in the form of root exudates for growth, development, and activities of microbes. Endophytic microbes are referred to those microorganisms that colonize in the interior of the plant parts. They enter in host plants mainly through wounds, naturally occurring as a result of plant growth or through root hairs and at epidermal conjunctions. The diverse group of microbes is key components of soil-plant systems, where they are engaged in an intense network of interactions in the rhizosphere/endophyte/phyllosphere and has emerged as an important and promising tool for sustainable agriculture. Plant microbiomes help to promote plant growth directly or mechanisms indirectly by using plant growth-promoting (PGP) attributes. The PGP microbes belonged to all three domains of archaea, bacteria, and eukarya. The most dominant and efficient plant growth-promoting microbes belong to different genera of Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Gluconacetobacter, Methylobacterium, Paenibacillus, Pantoea, Penicillium, Piriformospora, Planomonospora, Pseudomonas, Rhizobium, Serratia, and Streptomyces. These PGP microbes could be used as biofertilizers/bioinoculants in place of chemical fertilizers for sustainable agriculture. The present book, Advances in Plant Microbiome and Sustainable Agriculture: Diversity and Biotechnological Applications, is a very timely publication, providing state-of-the-art information in the area of agricultural and microbial biotechnology focusing on microbial biodiversity, plant-microbe interaction, and their biotechnological application in plant growth and soil fertility for sustainable agriculture. It comprises 11 chapters. In Chap. 1, Mahadevakumar and Sridhar describe plant-­microbe v

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interaction and the role of plant-associated microbes for sustainable agriculture. In Chap. 2, Mokran and El-Hafid highlight the culturable rhizospheric microbial communities and their biodiversity and biotechnological applications for agricultural sustainability. In Chap. 3, Mozhgan Ghiasian describes the genetic diversity of endophytic microbiomes from diverse host plants and their ecological significances for agricultural productivity. Chap. 4 by Waghunde et al. highlights the opportunities and challenges of endophytic microbial communities from leguminous and nonleguminous crops. Parihar et al. describe arbuscular mycorrhizal fungi and their abundance, interaction with plants, and potential biological applications in the Chaps. 5 and 6, by Rawool and team, deals with the functional attributes of endophytic microbes for plant health. In Chap. 7, Roy et al. highlight the recent advancements in taxonomical progress in phylum Actinobacteria and its biotechnological applications in agriculture. In Chap. 8, Guruvu and his colleagues describe in detail the endophytic Bacillus and related genera and their roles in agricultural applications. Sharma et al. highlight the role of microbes in improving plant growth and soil health for sustainable agriculture in Chap. 9. Leila and El-Hafid highlight biofertilizers and biopesticides for sustainable agriculture and environment in Chap. 10. Finally, in Chap. 11, Upadhyay et al. explore the role of microbes and their impact on environment. Overall, Dr. Ajar Nath Yadav, his editorial team, and scientists from different countries carried out great efforts to compile this book as a unique and up-to-date source on plant microbiomes for students, researchers, teachers, and academicians. I am sure the readers will find this book highly useful and interesting during their pursuit on plant microbiomes.

Dr. H. S. Dhaliwal is presently the Vice Chancellor of Eternal University, Baru Sahib, Himachal Pradesh, India. He completed his PhD in Genetics from the University of California, Riverside, USA (1975). He has 50 years of research, teaching, and administrative experience in various capacities. He is also a Professor of Biotechnology at Eternal University, Baru Sahib, from 2011 to date. He had worked as Professor of Biotechnology at IIT, Roorkee (2003–2011); Founder Director of Biotechnology Centre, Punjab Agricultural University, Ludhiana (1992–2003); Visiting Professor, Department of Plant Pathology, Kansas State University, Kansas, USA, (1989); Senior Research Fellow, CIMMYT, Mexico, (1987); Senior Scientist and Wheat Breeder-cum-Director, PAU Regional Research Station, Gurdaspur (1979–1990); Research Fellow FMI, Basel, Switzerland (1976–1979); and D.F. Jones Postdoctoral Fellow, University of California, Riverside, USA (1975–1976). He was elected as Fellow of the National Academy of Agricultural Sciences, India (1992). He has many national and international awards such as

Foreword

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Cash Award from the Federation of Indian Chambers of Commerce and Industry (FICCI) in 1985 and Pesticide India Award from Mycology and Plant Pathology Society of India in 1988. He has to his credit more than 300 publications including 250 research papers, 12 reviews, 15 chapters contributed to books, 105 abstracts and papers presented in meetings, conferences, 18 popular articles, and a number of project report/books/bulletins/manuals. His important research contributions are the identification of a new species of wild diploid wheat Triticumu urartu; gathering of evidences to implicate it as one of the parents of polyploid wheat; being the Team Leader in the development of seven wheat varieties, namely, PBW 54, PBW 120, PBW 138, PBW 175, PBW 222, PBW 226, and PBW 299, approved for cultivation in Punjab and North Western Plain Zone of India; molecular marker-assisted pyramiding of bacterial blight resistance genes Xa5, Xa21, and xa13 and the green revolution semidwarfing gene sd1 in Dehraduni basmati; and development of elite wheat lines biofortified for grain iron and zinc through wide hybridization with related non-­ progenitor wild Aegilops species and molecular breeding. Dr. Dhaliwal made a significant contribution to the development of life and epidemiology cycle of Tilletia indica fungus, the causal organism of Karnal bunt disease of wheat, and development of Karnal bunt-tolerant wheat cultivars. He has been the Member/Chairperson of several task forces and committees in the Department of Biotechnology, Ministry of Science and Technology, Government of India, New Delhi, and ICAR, New Delhi. Currently, he is a Member of an expert committee of DBT for DBT-UDSC Partnership Centre on Genetic Manipulation of Crop Plants at UDSC, New Delhi (2016 onwards), SAC of NABI (DBT), and RAC of IIAB, Ranchi, ICAR.

Vice Chancellor  H. S. Dhaliwal Eternal University, Baru Sahib, Himachal Pradesh, India

Preface

Microbes are ubiquitous in nature. The vast microbial diversity has been found to associate with the plant systems. The plant-microbe interactions are the key strategy to colonize and establish in a variety of diverse habitats. Plant microbiomes (rhizospheric, endophytic, and epiphytic) play important role in plant growth promotion and nutrient recycling. The diverse group of microbes is key components of soil-­plant systems, where they are engaged in an intense network of interactions in the rhizosphere/ endophyte/phyllosphere and has emerged as an important and promising tool for sustainable agriculture. Plant microbiomes help to promote plant growth directly or mechanisms indirectly by using plant growth-promoting attributes. The PGP microbes belonged to all three domains of archaea, bacteria, and eukarya. The most dominant and efficient plant growth-promoting microbes belongs to different genera of Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Gluconacetobacter, Methylobacterium, Paenibacillus, Pantoea, Penicillium, Piriformospora, Planomonospora, Pseudomonas, Rhizobium, Serratia, and Streptomyces. These PGP microbes could be used as biofertilizers/bioinoculants in place of chemical fertilizers for sustainable agriculture. The present book, Advances in Plant Microbiome and Sustainable Agriculture: Diversity and Biotechnological Applications, covers biodiversity of plant-associated microbes and their role in plant growth promotion and soil fertility for sustainable agriculture. It will be immensely useful to biological sciences, especially to microbiologists, microbial biotechnologists, biochemists, researchers, and scientists of microbial and plant biotechnology. We are honored that the leading scientists who has extensive, in-­depth experience and expertise in plant-microbe interaction and microbial biotechnology took the time and effort to develop these outstanding chapters. Each chapter is written by internationally recognized researchers/ scientists, providing readers with an up-to-date and detailed account of the microbial biotechnology and innumerable agricultural applications of plant microbiomes. Sirmour, Himachal Pradesh, India  Ajar Nath Yadav Isfahan, Iran   Ali Asghar Rastegari Mau, Uttar Pradesh, India   Neelam Yadav Sirmour, Himachal Pradesh, India   Divjot Kour ix

Acknowledgments

All authors are sincerely acknowledged for contributing up-to-date information on the plant microbiomes, their biodiversity, and biotechnological applications for sustainable agriculture and environment. We are thankful to all authors for their valuable contributions. We would like to thank their families who were very patient and supportive during this journey. Our sincere thanks to the whole Springer team who was directly or indirectly involved in the production of the book. Our special thanks to Prof. Naveen Kumar Arora, Ms. Aakanksha Tyagi, and Mr. Beracah John Martyn for the assistance and supports. We are very sure that this book will interest scientists, graduates, undergraduates, and postdocs who are investigating on “plant microbiomes” microbial and plant biotechnology.

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Contents

1 Plant-Microbe Interaction: Current Developments and Future Challenges������������������������������������������������������������������������������������������������    1 Shivannegowda Mahadevakumar and Kandikere Ramaiah Sridhar 2 Rhizospheric Microbiome: Biodiversity, Current Advancement and Potential Biotechnological Applications ����������������������������������������   39 Slimane Mokrani and Nabti El-Hafid 3 Endophytic Microbiomes: Biodiversity, Current Status, and Potential Agricultural Applications������������������������������������������������   61 Mozhgan Ghiasian 4 Culturable Plant-Associated Endophytic Microbial Communities from Leguminous and Nonleguminous Crops��������������   83 Rajesh Ramdas Waghunde, Mrugesh Dhirajlal Khunt, Rahul Mahadev Shelake, and Vijay Adhar Patil 5 Arbuscular Mycorrhizal Fungi: Abundance, Interaction with Plants and Potential Biological Applications��������������������������������  105 Manoj Parihar, Manoj Chitara, Priyanaka Khati, Asha Kumari, Pankaj Kumar Mishra, Amitava Rakshit, Kiran Rana, Vijay Singh Meena, Ashish Kumar Singh, Mahipal Choudhary, Jaideep Kumar Bisht, Hanuman Ram, Arunava Pattanayak, Gopal Tiwari, and Surendra Singh Jatav 6 Endophytic Microbiomes and Their Plant Growth–Promoting Attributes for Plant Health ����������������������������������  145 Prachiti P. Rawool, Vikrant B. Berde, P. Veera Bramha Chari, and Chanda Parulekar-Berde 7 Diversity and Biotechnological Potential of Culturable Rhizospheric Actinomicrobiota��������������������������������������������������������������  159 Sudipta Roy, Hiran Kanti Santra, and Debdulal Banerjee

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8 Bacillus and Endomicrobiome: Biodiversity and Potential Applications in Agriculture ��������������������������������������������������������������������  189 Guruvu Nambirajan, Ganapathy Ashok, Krishnan Baskaran, and Chandran Viswanathan 9 Role of Microbes in Improving Plant Growth and Soil Health for Sustainable Agriculture ��������������������������������������������������������������������  207 Devender Sharma, Navin Chander Gahtyari, Rashmi Chhabra, and Dharmendra Kumar 10 Biofertilizers and Biopesticides: Microbes for Sustainable Agriculture������������������������������������������������������������������������������������������������  257 Bensidhoum Leila and Nabti El-Hafid 11 Impact of Biopesticides in Sustainable Agriculture������������������������������  281 Hina Upadhyay, Anis Mirza, and Jatinder Singh

About the Series Editor

Naveen Kumar Arora is a Professor and Head of the Department of Environmental Science at Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India. He received his PhD in Microbiology. He is a renowned researcher in the field of environmental microbiology and biotechnology. His specific area of research is plant-microbe interactions, particularly plant growth-­ promoting rhizobacteria. He has more than 75 research articles published in premium international journals and several articles published in magazines and dailies. He is an editor of 25 books, published by Springer. He is a Member of several national and international societies, Fellow of International Society of Environmental Botanists (FISEB), Secretary General of Society for Environmental Sustainability, in editorial board of 4 journals, and reviewer of several international journals. He is also the editor in chief of the journal Environmental Sustainability published by Springer Nature. He has delivered lectures in conferences and seminars around the globe. He has a long-standing interest in teaching at the PG level and is involved in taking courses in bacteriology, microbial physiology, environmental microbiology, agriculture microbiology, and industrial microbiology. He has been advisor to 134 postgraduate and 11 doctoral students. He has been awarded for excellence in research by several societies and national and international bodies/organizations. Although an academician and researcher by profession, he has a huge obsession for the wildlife and its conservation and has authored a book, Splendid Wilds. He is the President of the Society for Conservation of Wildlife and has a dedicated website www.naveenarora.co.in for the cause of wildlife and environment conservation.  

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Editors and Contributors

About the Editors Ajar Nath Yadav is an Assistant Professor (Sr. Scale) in the Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Himachal Pradesh, India. He has 11 years of teaching/research experiences in the fields of Microbial Biotechnology, Microbial Diversity, and Plant-Microbe Interactions. He obtained his doctorate degree in Microbial Biotechnology jointly from IARI, New Delhi, and BIT, Mesra, Ranchi, India, his MSc in Biotechnology from Bundelkhand University, and his BSc in CBZ from the University of Allahabad, India. He has 174 publications, with h-index of 37, i10-index of 75, and 3242 citations (Google Scholar). He has published 115 research communications in different international and national conferences and has received 12 Best Paper Presentation Awards and 1 Young Scientist Award (NASI-Swarna Jayanti Puraskar). Dr. Yadav received “Outstanding Teacher Award” in the 6th Annual Convocation 2018 from Eternal University, Baru Sahib, Himachal Pradesh. He has a long-standing interest in teaching at the UG, PG, and PhD level and is involved in taking courses in microbiology and microbial biotechnology. He is currently handling two projects and is guiding three scholars for PhD degree and one for MSc dissertations. He has been serving as an Editor/Editorial Board Member and Reviewer for more than 35 national and international peer-reviewed journals. He has a lifetime  

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membership in the Association of Microbiologist in India and Indian Science Congress Council, India. Please visit https://sites.google.com/site/ajarbiotech/ for more details. Ali Asghar Rastegari currently works as an Assistant Professor in the Faculty of Biological Science, Department of Molecular and Cellular Biochemistry, Falavarjan Branch, Islamic Azad University, Isfahan, Islamic Republic of Iran. He has 13  years of experiences in the fields of Enzyme Biotechnology, Nanobiotechnology, Biophysical Chemistry, Computational Biology, and Biomedicine. He received his PhD in Molecular Biophysics in 2009 from the University of Science and Research, Tehran Branch, Iran; MSc in Biophysics in 1994 from the Institute of Biochemistry and Biophysics, University of Tehran; and BSc in Microbiology in 1990 from the University of Isfahan, Iran. To his credit, he has 39 publications [21 research papers, 2 books, 16 book chapters] in various supposed international and national journals and publishers. He is editor of 7 books. He has issued 12 abstracts in different conferences/symposiums/workshops and has presented 2 papers presented at national and international conferences/symposiums. He is a Reviewer of different national and international journals. He is a Lifetime Member of Iranian Society for Trace Elements Research (ISTER) and Biochemical Society of Islamic Republic of Iran, and is a Member of the Society for Bioinformatics in Northern Europe (SocBiN), Boston Area Molecular Biology Computer Types (BAMBCT), Bioinformatics/Computational Biology Student Society (BIMATICS Membership), Ensembl Genome Database, and Neuroimaging Informatics Tools and Resources Clearinghouse (NITRC).  

Neelam Yadav currently works on microbial diversity from diverse sources and their biotechnological applications in agriculture and allied sectors. She obtained her postgraduate degree from Veer Bahadur Singh  Purvanchal  University, Uttar Pradesh, India. She has research interest in the area of beneficial microbiomes and their biotechnological application in agriculture, medicine, environment, and allied sectors. To her credit, she has  51 research/review/book chapter  

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publications  in different reputed international and national journals and publishers. She is editor of 8 books. She is Editor/Associate Editor/Reviewer of different international and national journals. She has a lifetime membership in Association of Microbiologist in India; Indian Science Congress Council, India; and National Academy of Sciences, India. Divjot  Kour currently works as Project Assistant in DEST-funded project “Development of Microbial Consortium as Bio-inoculants for Drought and Low Temperature Growing Crops for Organic Farming in Himachal Pradesh.” She obtained her doctorate degree in Microbial Biotechnology from the Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Himachal Pradesh, India; her MPhil in Microbiology in 2017 from Shoolini University of Biotechnology and Management Sciences, Solan, Himachal Pradesh; and her MSc in Microbiology (2015) and her BSc (2014) both from the University of Jammu, Jammu and Kashmir. She has research experience of 5 years. To her credit, she has 45 publications  in different reputed international and national journals and publishers. She is Editor of two books in Springer. She has published 18 abstracts in different conferences/symposiums/workshops. She has presented 9 papers in national and international conferences/symposiums, and she has received 5 Best Paper Presentation Awards. To her credit, she has isolated more than 700 microbes (bacteria and fungi) from diverse sources. She is a Member of the National Academy of Sciences and Agro  – Environmental Development Society, India.  

Contributors Ganapathy  Ashok  Department of Biotechnology, Sree Narayana Guru College, Coimbatore, Tamilnadu, India Debdulal  Banerjee  Microbiology and Microbial Biotechnology Laboratory, Vidyasagar University, Midnapore, West Bengal, India Krishnan Baskaran  Department of Biochemistry, Sree Narayana Guru College, Coimbatore, Tamilnadu, India

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Vikrant B. Berde  Department of Zoology, Arts, Commerce and Science College, Lanja, Maharashtra, India Jaideep Kumar Bisht  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India P.  Veera  Bramha  Chari  Department of Biotechnology, Krishna University, Machilipatnam, Andhra Pradesh, India Dharmendra  Kumar  Division of Crop Physiology, Biochemistry and Post Harvest Technology, ICAR-CPRI, Shimla, India Rashmi  Chhabra  Division of Genetics, ICAR  – Indian Agricultural Research Institute, New Delhi, India Manoj Chitara  Department of Plant Pathology, College of Agriculture, GBPUAT, Panatnagar, India Mahipal Choudhary  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Nabti El-Hafid  Laboratoire de Maitrise des Énergies Renouvelables, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria Navin  Chander  Gahtyari  Crop Improvement Division, ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Mozhgan  Ghiasian  Department of Microbiology, Falavarjan Branch, Islamic Azad University, Isfahan, Iran Surendra  Singh  Jatav  Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences, Banaras Hindu University (BHU), Varanasi, Uttar Pradesh, India Priyanaka  Khati  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Mrugesh  Dhirajlal  Khunt  Department of Plant Pathology, N.  M. College of Agriculture, Navsari Agricultural University, Navsari, Gujarat, India Asha  Kumari  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Bensidhoum Leila  Laboratoire de Maitrise des Énergies Renouvelables, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria Shivannegowda Mahadevakumar  Department of Studies in Botany, University of Mysore, Mysore, Karnataka, India Vijay  Singh  Meena  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India

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Anis Mirza  Department of Horticulture, Lovely Professional University, Phagwara, Punjab, India Pankaj  Kumar  Mishra  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Slimane  Mokrani  Laboratoire de Maitrise des Énergies Renouvelables, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria Guruvu Nambirajan  Department of Microbiology, Sree Narayana Guru College, Coimbatore, Tamilnadu, India Manoj  Parihar  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Chanda  Parulekar-Berde  Department of Microbiology, Gogate Jogalekar College, Ratnagiri, Maharashtra, India Vijay  Adhar  Patil  National Agricultural Research Project, SWMRU, Navsari Agricultural University, Navsari, Gujarat, India Arunava Pattanayak  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Amitava Rakshit  Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences, Banaras Hindu University (BHU), Varanasi, Uttar Pradesh, India Hanuman  Ram  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Kiran Rana  Department of Agronomy, Institute of Agricultural Sciences, Banaras Hindu University (BHU), Varanasi, Uttar Pradesh, India Prachiti  P.  Rawool  Department of Microbiology, Gogate Jogalekar College, Ratnagiri, Maharashtra, India Sudipta Roy  Microbiology and Microbial Biotechnology Laboratory, Vidyasagar University, Midnapore, West Bengal, India Hiran  Kanti  Santra  Microbiology and Microbial Biotechnology Laboratory, Vidyasagar University, Midnapore, West Bengal, India Devender  Sharma  Crop Improvement Division, ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India Rahul Mahadev Shelake  Division of Applied Life Science (BK21 Plus program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, Korea Ashish Kumar Singh  ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India

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Jatinder  Singh  Department of Horticulture, Lovely Professional University, Phagwara, Punjab, India Kandikere Ramaiah Sridhar  Department of Biosciences, Mangalore University, Mangalore, Karnataka, India Centre for Environmental Studies, Yenepoya (deemed to be) University, Mangalore, Karnataka, India Gopal Tiwari  Division of Soil Resource Studies, ICAR-NBSS&LUP, Nagpur, India Hina  Upadhyay Department of Agronomy, Lovely Professional University, Phagwara, Punjab, India Chandran  Viswanathan Department of Biotechnology, Sree Narayana Guru College, Coimbatore, Tamilnadu, India Rajesh  Ramdas  Waghunde  Department of Plant Pathology, College of Agriculture, Navsari Agricultural University, Bharuch, Gujarat, India

Chapter 1

Plant-Microbe Interaction: Current Developments and Future Challenges Shivannegowda Mahadevakumar and Kandikere Ramaiah Sridhar

Abstract  Microbial interactions with plants result in beneficial as well as harmful impacts, which have a major role in ecosystem processes. Negative interactions by microorganisms (bacteria and fungi) end up with plant diseases threatening the agriculture worldwide. On the contrary, positive interactions have beneficial implications useful in pharmaceutical, biotechnological and agricultural applications. In the recent past, research has been focused towards understanding the complex molecular mechanisms of host-pathogen interactions to develop microbe-based fertilizers (bioprotectants), phytosanitizers, management of rhizosphere microbes for improved nutrient uptake and disease control. The current research has focused towards following the mechanisms of interaction between host and pathogen for sustainable agriculture. This chapter addresses the recent advances in interactions of plant and microbes to understand the beneficial impacts (PGPR and PGPF) followed by applications of OMICS, small RNAs, systems biology and metabolomics engineering with notes on challenges in future agriculture. Keywords  Genomics · Growth promotion · Metabolomics · Microbiome · Mutualism · Pathogens · Signaling · Systems biology

S. Mahadevakumar Department of Studies in Botany, University of Mysore, Mysore, Karnataka, India K. R. Sridhar (*) Department of Biosciences, Mangalore University, Mangalore, Karnataka, India Centre for Environmental Studies, Yenepoya (deemed to be) University, Mangalore, Karnataka, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_1

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S. Mahadevakumar and K. R. Sridhar

1.1  Introduction Plant species are in continuous association and interaction with diverse group of microorganisms. The magnitude of such associations is highly diverse in the vicinity, surface areas and within the live plant tissues (Bulgarelli et al. 2013; Verma et al. 2016; Vorholt 2012). From the agricultural point of view, plants and microbes interact in many ways resulting in manifestation of mutualistic or hostile changes. If the interaction is mutualistic, this will be beneficial or advantageous to both organisms like fertile soil composed of a large number of beneficial bacteria and fungi (e.g. rhizobia and mycorrhizas). Such interactions result in beneficial effects like nitrogen fixation as well as uptake of nutrients. On the other hand, plants are constantly threatened by a wide range of pathogens (e.g. bacteria, fungi and others), which result in the development of defense mechanisms in plants to combat against pathogens (Kour et al. 2020d; Rana et al. 2020c). Microorganisms interact with plants at different magnitude, while plants have strategies to deal with or exploit the associated microorganisms. Several microbes are known to influence plant growth as well as development without entering the plant tissues (e.g. Azotobacter and Cyanobacteria), and some microbes are helpful as endophytic (entering the intercellular spaces, Azospirillum and ectomycorrhizae; intracellular association, Rhizobium and endomycorrhizae). Stability of such positive plant-microbial relationships results in the development of sustainable eco-friendly agroecosystems (Kour et al. 2019a; Verma et al. 2019; Yadav 2017; Yadav et al. 2017). Characterizations of plant-microbe interaction with biotic and abiotic factors are the essential steps to understand the beneficial effects (Kumar et al. 2016). Plants’ successful foothold as land dwellers is partly due to the ability of plants to team up with microbes for which Rhynie chert (the oldest land plant fossils) gave evidence for the presence of fungal structures within the plant cells (Remy et al. 1994). It is known that arbuscular mycorrhizal (AM) fungi colonized more than 70% of existing higher plants (Wang and Qiu 2006). In most of the mutualistic plant-fungal interactions in the rhizosphere, the fungal partner provides mineral nutrients to plants (e.g. phosphorus), and in turn plant provides carbohydrates to the fungi as energy source. Many pathogenic and beneficial microbes thrive in the host rhizosphere; their interaction is dependent on the physiology and genetics of the host and associate (Rey and Schornack 2013). Understanding the interactions such as the mechanism of association, pathogenesis and adaptations is highly crucial. Many molecular studies have been carried out to follow the role of functional genes those are encoding the extracellular proteins (e.g. sequencing and bioinformatics). However, the impact of environmental conditions on plant-microbe interactions is not greatly explored at molecular level. Further enrichment of our knowledge on the impact of environmental factors on plant-microbe interactions demands systems-­level approaches (Cheng et al. 2019; Sergaki et al. 2018; Verma et al. 2017; Yadav et al. 2019a). The recent research focused on the small proteinaceous effectors produced by the microbes within the plant tissues during the interaction. These effectors alter the plant processes and facilitate colonization viewed as complicated interplay of mutualism. The effectors influence the plant defense circuit and colonization of pathogens. Recognition of effectors assisted to follow the plant-microbe interactions

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more critically by supporting sequencing especially next-generation sequencing (NGS) (Knief 2014). The system-wide approach has demonstrated that plant growth and development is highly dependent on coordination of different plant-microbe interactions. This chapter addresses up-to-date developments which pertain to plant-microbe interactions with a background note on beneficial aspects (plant growth-promoting bacteria and fungi) followed by current views on small RNAs in plant-pathogen interactions, systems biology and metabolomics engineering with a note on challenges ahead for future agricultural progress.

1.2  Background Prior to addressing the plant-microbe interactions, we quote the lines by Jackson and Taylor (1996) on plant-microbe relations: ‘Life and death at the interface: Interactions between microorganisms and plants have undoubtedly had major effects on the development of civilization since humans began to rely extensively on cultivated crops for food’. The plant-microbe interactions portray a broad range of scientific studies especially how microorganisms interact with plants at various levels including ecological, morphological and more recently at the molecular levels. The plants and microbes develop specific communications among themselves, and these interactions (mutualistic, pathogenic and associative) ultimately influence the growth, efficiency (yield potential and biomass production), tolerance (to stress and other biotic and abiotic factors) and development of disease resistance in plants. The plant-microbe interactions could be beneficial, neutral and harmful, which influences directly on growth and health of the plant species (Newton et al. 2010; Scheiawski and Perlin 2018). Plants will be host for a restricted species of microbes, or it may harbour several species. The existence of host-specific microbes has been well-documented. The specificity of plant-microbe communications has evolved more than millions of years (Galagan et al. 2005). Plant phenotype and ecology will be influenced by the impact of the mutualistic microbes on the environment and their competition for soil nutrients. Beyond doubt, ancient records of famines and epidemics revealed serious plant diseases caused by rusts (e.g. coffee rust and wheat rust), smuts and mildews. Constant interaction between the host plant and pathogen will determine the ability of pathogen to influence the host plant or the ability of host plant to deter the pathogen (Ho et al. 2017). In many occasions, the association of microbes with plant species could be pathogenic leading to manifestation of disease (Strange and Scott 2005). Previously, it was assumed that pathogens and virulence will be normal and epidemic, which end up in severe loss of crop yield and represents one of the major threats of food security worldwide. Several questions pertaining to plant-pathogen associations, which influence plant health, remain unanswered. Mutualistic as well as pathogenic relations necessitate precise signaling pathways for sharing benefits or disease response similar to the development of root nodule (e.g. rhizobia) or specific disease (e.g. blast, dieback, spots and blights) (Riely et al. 2004, 2006; Imam et al. 2014a, b; 2015a, b; 2016).

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In the last few decades, outbreaks of plant disease end up with catastrophic crop failure, which resulted in famines and caused severe socioeconomic change. The effects of such epidemics have resulted in Irish potato famine (1840–1847) owing to dependence on a monocrop as principal food source. Even after attaining so much of advancement in science and technology, the possibility for such catastrophic epidemics still persists. Leaf blight of tomato, southern corn leaf blight, Victoria blight of oats, and many others all pose challenges as well as lessen sustainable agricultural production. Most of these diseases resulted from various agricultural practices, especially monocrop cultivation of narrowly related crop species in a wide range of geographical regions (Jackson and Taylor 1996). Thus, plant-microbe interactions can be studied under two major headings: beneficial interactions and harmful interactions. The beneficial interactions address the exploitation of microbes existing in the rhizosphere and phyllosphere for their capability to support plant growth and associated internal processes. Such microbes include plant growth-promoting rhizobia (PGPR) and plant growth-promoting fungi (PGPF) (Rastegari et  al. 2020b; Singh and Yadav 2020). There are several patents for biotechnological products that are formulated by exploitation of beneficial traits of microbes.

1.3  Harnessing Plant-Microbe Interactions Currently, the world is confronting non-stop challenges to sustain the abounding populace as almost one billion individuals go hungry (Reid 2011). Low profitability, productivity, restricted arable land, shortage of water and yield loss by diseases are mainly responsible for tilting the supply and demand of food commodities. Fertilizer application, the practice of advanced breeding of plants and approaches like genetic engineering have expanded the yield; however, they are expensive and explicit to apply under wide geographic conditions (Kaur et al. 2020; Reid 2011; Singh et al. 2020). The need of the day is to investigate different methodologies using genetic approaches to improve plant resistance to the pathogens. A few studies have brought out diverse perspectives and emphasized harnessing of plant-associated microbes for the benefit of plants (Farrar et  al. 2014). One of the advantages of plant-­ microorganism associations is the mutual relationship that developed between plants and microorganisms, which enables improvement of host plant protection from a wide range of stresses (e.g. drought, diseases, toxins, nutrient, salinity, heavy metals and temperature) (Smith et  al. 1999; Berg 2009; Reid 2011; Kour et  al. 2019b; Yadav et al. 2015c, 2018a). Such low-cost biotechnological applications of mutualistic partnership will result in increased crop productivity (Fig. 1.1). These are relatively new understudied approaches that possess potential for the global new Green Revolution (Reid 2011). The harmful/pathogenic microorganisms ceaselessly interfere with one another in the roots of the host plant species. Plant wellbeing relies on the nature of microbe-­ microbe and plant-microbe interactions. Plants endure when their underlying roots are affected by disease-causing microorganisms, while they flourish by colonization

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Fig. 1.1  Schematic illustration of plant microbiome and its exploitation: biotechnological application of plant-microbe interactions (PGPR, PGPF and mycorrhiza) in biocontrol, systemic-­ acquired resistance, biopesticides and biofertilizers

of beneficial microbes. Environmentally sound and sustainable crop production is the major challenge for the twenty-first century, and enhanced production not only provides adequate food for the increasing population but also offers raw materials for various industries. Currently farmers are fairly dependent on the use of chemical pesticides, owing to their lack of awareness on the implications of its application: environmental degradation and deterioration of human/livestock health. On the other hand, there are various emerging, resistant and endemic plant pathogens that pose serious threat to food grain production, and it continues to be a major challenge to safeguard plant health for improved quality and high productivity. New technology is in demand to achieve ecologically compatible strategies to mitigate the loss due to pests or pathogens with improved quality of agricultural produce. Advances in plant biotechnology resulted in the addition of new crop varieties with high yield, disease resistance and drought/salinity tolerance, with better nutritional benefit. Plant-microbe interaction has been disregarded in breeding methods despite the fact that soil beneficial microbes interacting with plants have a key role in favour of the ecosystem and environment. Important role performed by these

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microbes in association with host plants includes increased plant growth, improved stress tolerance, development of disease resistance, enhanced nutrient uptake and biodiversity promotion (Lugtenberg et al. 2002; Morrissey et al. 2004; Verma et al. 2015a, b; Egamberdieva et al. 2017). A wide variety of products and formulations have been invented recently based on the plant-microbe interaction or exploiting their interactions to promote agriculture for better productivity and improved quality. In this section, biotechnological applications are discussed under three main headings: (1) plant growth-promoting rhizobacteria (PGPR); (2) plant growth-promoting fungi (PGPF); and (3) mycorrhizal association with their signaling molecules.

1.3.1  Plant Growth-Promoting Rhizobacteria Microbes existing in the rhizosphere perform several functions towards host growth and development. Rhizobacteria that facilitate plant growth promotion and resistance to diseases are classified as PGPR (plant growth-promoting rhizobacteria), a class of organisms that enhance plant growth and improve yield via a variety of plant growth-promoting substances, which serve as biofertilizers or bioprotectants (Verma et al. 2016; Yadav et al. 2015a, b) (Table 1.1). Their plant growth-promoting performance is usually attributed to improved nutrient acquisition through hormonal stimulation. Bacteria residing in the rhizosphere of plants have special role and known to possess plant growth-promoting attributes, which improve nutrient cycling as well as help in reducing the use of chemicals (Cakmakci et  al. 2007; Saxena et al. 2016; Yadav et al. 2015a). Many rhizosphere bacteria are used as biofertilizers extensively in organic farming for sustainable agriculture. It is well established that PGPR are biofertilizers as well as efficient soil-inhabiting bacteria for sustainable agriculture (Yadav et al. 2020). The PGPR are well-known and commercially harnessed by government and private organizations across the globe (Glick 1995; Okon and Labandera-Gonzalez 1994). The PGPR are known to produce a number of special metabolites, which are soluble and volatile, and help in inhibiting the growth of pathogenic bacteria by antibiosis or by cell signaling through induction of resistance and tolerance to plants against various pathogenic and environmental stresses. They are also known to enhance the nodulation upon co-inoculating with Bradyrhizobium japonicum leading to enhanced plant development and yield in soybean (Zhang et al. 1996; Stefan et al. 2010). Examination of biochemical and metabolomics of different PGPR has recognized a few potential candidate molecules for advancement and deployment in agribusiness. Chemical profiling and functional examinations have given crucial insights into the idea of various soluble and volatile compounds produced by PGPR. Although many studies focused on elucidating the molecules produced by the PGPR, complete mechanisms of their impact with the host and surrounding environment are yet to be studied (Kour et al. 2020b; Rana et al. 2020b). These studies provided a solid base for further progress on the areas to unravel the chemical basis of functions of PGPR. There is further scope to develop new PGPR to serve the eco-friendly agriculture.

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Table 1.1  Plant growth-promoting rhizobacteria (PGPR) and their applications PGPR Achromobacter xylosoxidans_Ax10 Achromobacter sp. Azospirillum brasilense_Cd. A Azospirillum brasilense_Az39 Bacillus cereus Bacillus subtilis_RR4 Bacillus sp. NRRU-D40 Bradyrhizobium japonicum_E109 Burkholderia phytofirmans_PsJN Burkholderia pyrrocinia (R-46)

Erwinia herbicola Enterobacter sp._NRRU-N13; NRRU-N20, NRRU-N21, NRRU-D47 Exiguobacterium oxidotolerans Klebsiella sp. SBP-8 Methylobacterium fujisawaense Pseudomonas aeruginosa_OSG41

Pseudomonas putida Planomicrobium chinense

Applications Phytoremediation (copper)

References Ma et al. (2009)

Stimulation of ionic transport

Bertrand et al. (2000) Burdman et al. (1996) Cassán et al. (2009) Khan et al. (2018) Rekha et al. (2018) Saengsanga (2018) Cassán et al. (2009) Ait Barka et al. (2006) Rêgo et al. (2014)

Promotion of nod gene inducers and nodulation Promote seed germination and early seedling growth Promotes plant growth under stressed/ drought tolerance and phytoremediation Induces malic acid biosynthesis in rice root and plant growth promotion Growth at the early stage of Thai jasmine rice Promote seed germination and early seedling growth Provides resistance to chilling effect Root plasticity in rice as well as biochemical changes which lead to the growth promotion Contribution to production of indole-3-­ acetic acid Growth at the early stage of Thai jasmine rice Improves yield and content of secondary metabolites Induced systemic tolerance in wheat under stress condition Regulation of ethylene levels Plant growth promotion and phytoremediation (chromium accumulation) Helps in production of indole acetic acid which helps in root development Promotes plant growth under stressed/ drought tolerance and phytoremediation

Brandl and Lindow (1998) Saengsanga (2018) Bharti et al. (2013) Singh et al. (2015) Madhaiyan et al. (2006) Oves et al. (2013) Patten and Glick (2002) Khan et al. (2018)

1.3.2  Plant Growth-Promoting Fungi Fungi residing in various habitats in a plant system (roots, leaves, stem, rhizosphere and phyllosphere) are exploited for their ability to support plant growth promotion, thereby activating several key pathways during plant development or disease resistance during pathogenesis or combating stressful environments (Kumar et al. 2019;

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Rajawat et al. 2020). Interactions between plants and their associated fungi in rhizosphere and phyllosphere as endophytes promote the plant development and induction of resistance systemically (ISR) on invading pathogens are known as plant growth-promoting fungi (PGPF). A large number of heterogeneous classes of fungi from different habitats have the capacity to augment plant growth promotion (Kour et al. 2019c; Rana et al. 2019; Yadav 2019; Yadav et al. 2018b). The important fungal genera recorded to have the PGPF traits are Aspergillus, Fusarium, Penicillium, Piriformospora, Phoma, Trichoderma and many others (Meera et al. 1994; Sudisha et al. 2013; Murali et al. 2013; Hossain et al. 2017; Elsharkawy et al. 2015). The PGPF interacts with host plants, and their interactions will positively influence the below-ground as well as the above-ground parts. The PGPF are also known to significantly improve the seed germination, seedling vigour, biomass, root hair growth, efficiency of photosynthesis, flowering, yield of seeds and biochemical composition of seeds (Sudisha et  al. 2013; Murali et  al. 2013). Other than these traits, the PGPF are also known to control several foliar pathogens by inducing systemic resistance. It is now known that the PGPF are also capable to control numerous foliar and root pathogens by triggering ISR in the hosts. They enhance the abilities of host plants to increase nutrient uptake and hormone production, which in turn reprogram the gene expression through differential activation of plant signaling pathways (Hossain et al. 2017). The PGPF have attracted substantial attention as biofertilizers due to their beneficial effects on plant quantity and efficiency of their positive relationship with the environment. Representative PGPF, their hosts, habitats and applications are presented in (Table 1.2).

1.3.3  Mycorrhizal Implications in Agriculture Mycorrhizas are symbiotically associated fungi with plant roots, which enhance the uptake of water and nutrients (Ortas et al. 2001). The mycorrhizosphere represents a significant environmental niche for exceptionally adapted diverse microbial communities. At present it is known that the density of bacteria in the mycorrhizosphere will be higher (4–5-fold) than the rhizosphere of plant (Heinonsalo et al. 2000). The arbuscular mycorrhizal (AM) association is the vital mutualistic interaction resulting in significant beneficial impact worldwide, and over 65% of known land plants have this association (Ryan and Graham 2002; Wang and Qiu 2006). The AM fungi associate with plants without morphological modification from the Devonian period (~400 my), and thus the AM fungal mutualism played a crucial role in plant evolution (Remy et al. 1994; Taylor et al. 1995; Delaux et al. 2015; Yadav et al. 2020). Nearly 10,000 of ectomycorrhizal fungal species have been recognized, and many of them show host specificity. The mycorrhizal fungi form their extensive hyphal network in soils, and the extra-radical mycelia (ERM) serve as artificial root system to increase the nutrient uptake. The ERM with its mycorrhizosphere act as a vital link of microbial communities as well as host plant species (Kaiser et al. 2014). The mycorrhizal fungi enhance the nutrient uptake by host plant and are capable to

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Table 1.2  Plant growth-promoting fungi (PGPF) and their applications (–, not defined) PGPF Host Habitat Alternaria sp._ A13 Salvia Endophyte miltiorrhiza

Applications Stimulates S. miltiorrhiza root growth and boosts the secondary metabolism Induces systemic resistance against anthracnose of cucurbits Mediates resistance in tomato against bacterial wilt disease, promotes growth and induces expression of defense-­ related genes Enhances plant growth and induces resistance in pearl millet against downy mildew disease Induces resistance in Arabidopsis thaliana by activation of multiple defense signals Promotes growth and increases yield

Fusarium sp.

Zoysia sp.

Rhizosphere

Penicillium chrysogenum_ PenC_JSB41

–

Rhizosphere

Penicillium oxalicum UOM-PGPF16

Pearl millet

Rhizosphere

Penicillium simplicissimum GP17-2

Zoysia tenuifolia

Rhizosphere

Penicillium sp.

Zoysia sp.

Rhizosphere

Penicillium sp. GP16-2

Zoysia tenuifolia

Rhizosphere Induces defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana Rhizosphere Induce resistance and promote growth Rhizosphere Promotes growth and confers protection against damping off and anthracnose in the cucumber Rhizosphere Induces systemic resistance against anthracnose of cucurbits – Induces systemic resistance against anthracnose disease in cucumber Rhizosphere Mediates resistance in tomato against bacterial wilt disease

Penicillium Pearl millet sp._UOM-PGPF27 Penicilliumspp.GP15- Zoysia sp.

Phoma sp.

Zoysia sp.

Phoma sp._GS8-1, GS8-2 and GS8-3

–

Trichoderma harzianum_ TriH_JSB27

–

References Zhou et al. (2018) Koike et al. (2001) Sudisha et al. (2013) and Murali et al. (2013)

Murali and Amruthesh (2015) Hossain et al. (2007) and Elsharkawya et al. (2012) Shivanna et al. (1994) and Koike et al. (2001) Hossain et al. (2008)

Murali et al. (2012) Hossain et al. (2014)

Koike et al. (2001) Elsharkawy et al. (2015)

Sudisha et al. (2013) and Nagaraju et al. (2012) (continued)

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Table 1.2 (continued) PGPF Trichoderma longibrachiatum_ T6

Host –

Trichoderma sp.

Zoysia sp.

Trichoderma sp.

–

Habitat –

Applications Promotes wheat growth; induces plant resistance to parasitic nematodes; enhances tolerance of wheat to salt stress Rhizosphere Promotes growth and increases yield Rhizosphere Promotes growth and nutrient uptake; induces systemic resistance

References Zhang et al. (2016)

Shivanna et al. (1994) and Koike et al. (2001) Azarmi et al. (2011) and Fontenelle et al. (2011)

distribute substantial quantities of essential macroelements (N, P, K and S) as well as trace elements (Cu, Zn). Many mycorrhizal fungi also provide benefits beyond nutrition by development of fitness apposing abiotic stresses (e.g. drought, heavy metals and salinity) as well as biotic (pathogens) stresses (Redecker et  al. 2000; Heckman et al. 2001; Wright et al. 1998). Their symbiotic associations with the host plants influence the plant relationships in the ecosystems (Smith and Read 2008). However, mycorrhizal fungal mycelia influence the qualitative and quantitative alterations in the microbial community in rhizosphere (Nuccio et al. 2013). Presence of mycorrhizal hyphae also plays a vital role in the assembly of bacterial community in decomposition process, which facilitates access of carbon to other communities of microbes in the rhizosphere (Herman et al. 2012; Nuccio et al. 2013). Mycorrhizas also benefit their host by influencing the plant morphology and physiology under different conditions (stress, diseases and others). Thus, they produce growth-regulating substances, increase photosynthetic rate and improve osmotic adjustment under drought and salinity stresses, which lead to adverse impact on pests and soilborne pathogens (Plenchette et al. 2005; Al-Karaki 2006). Mycorrhizas are ubiquitous and serve as major microbial biomass in forests and flux carbon to below-ground organisms leading to substantial assimilation of carbon in the vegetation. The changes in climate influence below-ground plant-allocated carbon leading to a shift in composition of soil microbial communities, and thus, it is hypothesized that such change in community shapes carbon mitigation in forest ecosystems (Churchland and Grayston 2014).

1.3.4  Signaling Molecules in Plant-Mycorrhizae Interactions Interactions between plant and plant-associated mycorrhizae exhibit varied functions (structural, functional and ecological). A few root and hyphal exudates could possibly instigate mycorrhizal colonization and modify the microbial network of the rhizosphere. The proteins produced are called effectors which serve as signaling molecules to help plant-mycorrhizal association (Lowe and Howlett 2012). The

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effector proteins support colonization by reducing the immunity and in addition stimulate defense reactions in plants (Stergiopoulos and de Wit 2009). Laccaria bicolor is known to deliver the effector mycorrhiza-induced small secreted protein 7 (MISSP7) at the time of root colonization because of diffusible signals received from the exudates of roots (Plett et  al. 2011). The secretion and uptake of these MISSP7 proteins by the plants (through PI-3-P intervened endocytosis) influence the chemical structure of the cell which help hyphal infiltration of the root apoplast. MISSP7 is one of the most upregulated proteins at the time of mycorrhization and without which the mutualism will not build up (Plett et al. 2011). After this revelation, another effector protein called SP7 was detected (Maffei et al. 2012). The SP7 produced by the AM fungus Gigaspora intraradices interfaces the plant pathogenesis-­related transcription factor. The SP7 has a significant role to oversee the formation of mutualistic response with roots through concealment of the plant immune framework (Kloppholz et al. 2011). In addition, plants are known to produce strigolactones in nutrient-deficient conditions (Maffei et al. 2012). The strigolactones trigger fungal spore germination and branching of hyphae (Bonfante and Requena 2011; Maffei et al. 2012) through signaling close to mycorrhizae to expand the extent of colonization. Significantly less information about AM parasitic signaling, albeit as of late it has been indicated that they produce diffusible active signals like ‘Nod’ factors discharged by the rhizobia and these signs are fundamental for the development mycorrhizal network (Bonfante and Requena 2011). Correspondingly, effectors secreted by plants are known to influence the relationships of free-living microorganisms with roots (Hogenhout et al. 2009).

1.4  Current Concepts on Plant-Pathogen Interaction Plants have endowed with a set of innate capacity to resist the pathogen attack at different stages of growth and development. Resistance to plant pathogens is the first line of defense: If the host is successful in combating the infection by a pathogen, it develops resistance; if not the plant succumbs to the disease caused by pathogen. Other factors that influence the resistance and susceptibility of the plant-pathogen interactions include the environment, genetic factors of the host and the virulence of pathogen. Plants have evolved to develop effective mechanisms to defend the attack of microbes that are always in contact with hosts (Kour et al. 2020a; Rana et al. 2020a). The first line of defense of a plant against pathogen is its surface, where the pathogen penetrates to cause infection. Even though the structural properties provide some degree of defense to plant against attack of pathogens, the resistance of plants depends mainly on secretion of substances prior to infection or after infection (Agrios 2005). During the long history of coevolution between the host and pathogen, immune response of plant has culminated a profound defense framework that is able to oppose the potential infections by microbial pathogens (Rashid et al. 2010). Early response of the pathogen by host is significant if the host needs to prepare the accessible biochemical and structural defense molecules for its protection. When a specific plant particle perceives and responds with a molecule (elicitor) originated

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from a pathogen, it is accepted that host perceives the pathogen effectively. Following such response, a series of biochemical responses and structural changes will happen in the plant cells to discover the pathogen, its catalysts and toxins. The crop plants are endowed with numerous defense genes, which encode various proteins responsible for the synthesis and accumulation of defense arsenals on the surface. However, these defense genes are quiescent in healthy plants and activated when pathogens come in contact with the hosts by release of signals (Vidhyasekaran 1993; Vidhyasekaran and Velazhahan 1996). When these signals are activated upon infection by a biotic agent (usually a pathogen), it transfers a signal to the plant nucleus through a signal transduction to activate defense genes. One of the most important signal molecules identified is salicylic acid, in addition to jasmonic acid, methyl jasmonate and ethylene (Xu et al. 1994; Schweizer et al. 1997). To establish the ‘disease’ during the course of plant-microbe interactions, a pathogen has to cross various obstacles to get into the plant system and successfully cause the disease. The primary obstruction being the plant cell surface, entry could happen through stomata and wounds or by direct infiltration through production of enzymes. When the pathogens get entrance by penetrating the cuticle, they need to confront the subsequent obstruction, the plant cell wall. After crossing cell wall infiltration, the pathogen is isolated from plant cytoplasm by the plasma membrane. Plasma membranes contain specific proteins and extracellular surface receptors, which invoke the pathogen-associated molecular patterns (PAMP) to trigger immune reactions. Chitin in the cell wall has been considered as one of the major fungal PAMP. Plants are outfitted with constitutive and inducible defense response. The constitutive factor incorporates strength and thickness of cell walls with pre-framed antimicrobial compounds, while the inducible factor responds by production of toxins. On pathogen recognition, plant regulatory genes start a multi-segment defense reaction, whose components are initiated in an exceptionally controlled temporal and spatial scale. Such responses result in the production of several compounds (e.g. phytoalexins, PR proteins and reactive oxygen species) and defense responses (e.g. stimulation of signal pathways, strengthening of cell wall, acquired resistance and apoptosis) (Fig.  1.2). In compatible interactions these defense responses are not initiated or enacted, which happens just at later stage if the associated microbe applies negative impact on development of the host plant. It has been accepted that plants shield themselves against pathogenic fungi by production of various toxic substances like pathogenesis-related proteins (PRP), glycoproteins and extensions of phenolic compounds, phytoalexins and others.

1.4.1  Hypersensitive Response One of the ubiquitous features of interactions of plant pathogen is the death of host cell due to speedy collapse of tissues, which is a hypersensitive response (HR) (Dangl et  al. 1996). Higher plants are known to shield themselves from different stresses such as plant pathogenic microbes, wound, impact of chemicals (e.g.

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Fig. 1.2  Schematic representation of pathogenesis-related (PR) gene activation during systemic-­ acquired resistance (SAR)

phytohormone and heavy metals) and growth conditions by changing their physiological setup. These defensive reactions are called defense responses of plants, and the proteins produced in such defense response are designated as defense-related proteins (Bowles 1990). The major strategy of defense of plants against stress-inducing pathogens includes the production of an array of stress proteins. Such plantcoded PRP play a major role in plant defense under stressful environment. The accomplishment of the plant avoiding the pathogenic attack relies on the coordination among various defense reactions and speed of the response. It is by and large accepted that plants defend themselves against pathogenic fungi through production of toxic substance (glycoproteins, expansions of phenolic mixes, phytoalexins and PRP). The PRP have been classified based on the structure and function (Van Loon 1997, 1999, 2010; Van Loon and Van Strien 1999; Van Loon et al. 2006; Ma and Liu 2016). The PRP found in several plant species to date are categorized into 17 families (Table  1.3). The sequence similarity, immunologic or serologic relationships and enzyme properties will be useful in classification. The hormones produced by plants include abscisic acid (ABA), auxins (AU), brassinosteroids (BR), cytokinins (CK), ethylene (ET), gibberellins (GA), jasmonates (JA), salicylic acid (SA) and strigolactones (SL), which are very important in plant-microbe interaction. Many of these hormones help in combating the entry of pathogen at various levels. Among the hormones, ABA, SA, JA and ET have significant function in intervening plant defense reaction against pathogens and also

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Table 1.3  Families of PR proteins and their functions in plant defense Family PR-1 PR-2 PR-3 PR-4 PR-5 PR-6 PR-7 PR-8 PR-9 PR-10 PR-11 PR-12 PR-13 PR-14 PR-15 PR-16 PR-17

Type member Tobacco PR-1a Tobacco PR-2 Tobacco P,Q Tobacco R

Properties Antifungal?, 14-17kD Class I, II and III endo-beta-1,3-glucanases, 25-35kD Class I, II, IV, V, VI and VII endochitinases, about 30kD Antifungal, win-like proteins, endochitinase activity, similar to prohevein C-terminal domain, 13-19kD Tobacco S Antifungal, thaumatin-like proteins, osmotins, zeamatins, permeatins, similar to alpha-amylase/trypsin inhibitors Tomato inhibitor Protease inhibitors, 6-13kD Tomato P69 Endoproteases Cucumber chitinase Class III chitinases, chitinase/lysozyme Lignin-forming Peroxidases, peroxidase-like proteins peroxidase Parsley PR-1 Ribonucleases, Bet v 1-related proteins Tobacco class V Endochitinase activity chitinase Radish Ps-AFP3 Plant defensins Arabidopsis THI2.1 Thionins Barley LTP4 Nonspecific lipid-transfer proteins (ns-LTPs) Oxalate oxidase Barley OxOa (germin) Barley OxOLP Oxalate oxidase-like proteins Tobacco PRp27 Unknown

Source: Van Loon et al. (2006)

against abiotic stresses (Bari and Jones 2009; Nakashima and Yamaguchi-Shinozaki 2013). The noticeable commitment of ABA towards plant defense reaction opposing to abiotic stresses has long been examined. The ABA generally helps in plant defense against abiotic stresses like drought, salinity, cold, heat and wound (Lata and Prasad 2011; Zhang et al. 2006). On the contrary, SA, JA and ET levels increase with pathogen infection, which plays main role in response to pathogen attack (viruses, bacteria, fungi and other pathogen-associated biotic factors) (Bari and Jones 2009). There are substantial evidences for the interaction of ABA, SA, JA and ET with AU, GA and CK to regulate plant defense reactions (Navarro et al. 2008; Bari and Jones 2009; Nishiyama et al. 2013).

1.5  The PMI in the Era of OMICS The genomic information, transcriptomics, proteomics and other OMICS-related data will enhance our knowledge on the biology, evolution and functional aspects of host in a specific environment and its interaction with several microbes (including beneficial and pathogenic). Based on the OMICS platforms, one can dissect the mechanism of symbiosis, parasitism and other associated processes during

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development. With minimum expense high-throughput DNA sequence technology allowed plant pathology to enter into the genomics era. Specifically, studies in large-scale sequencing of cDNAs (expressed sequence tags or ESTs) are progressing for a wide assortment of several crop plants. In the advanced molecular era, meta-genomic studies will provide high-quality references and begin to reveal the diversity, evolution and interaction with other organisms and environment. It is also true for bacteria, fungi, viruses, viroids, nematodes, insect pests, plants, animals and others those thrive in extreme environments. Even though there are several hundreds of important plant pathogens widespread causing significant economic loss and productivity, we attempted to explore the recent developments in plant-pathogen interaction of three major plant pathogens that cause major disease outbreaks in the history of plant pathology (Fig. 1.3). They are (1) Ceylon coffee rust by Hemileia vastatrix; (2) late blight of potato by Phytophthora infestans; and (3) stalk rot of maize by Fusarium verticillioides.

1.5.1  Hemileia vastatrix Coffee leaf rust disease caused by Hemileia vastatrix is one of the most prominent diseases in coffee plantations. Commercially viable arabica coffee (Coffea arabica) and robusta coffee (Coffea canephora) distributions in coffee-growing regions were susceptible to rust infection. The rust pathogen has been reported in multiple outbreaks in several coffee-growing regions which resulted in high yield loss. New races are constantly evolving as evidenced by the presence of fungus in plants that were previously resistant. To understand the nature of their evolution and success of breaking, the resistance of the host plants lies with the genome of pathogen and its interactions with host genome factors. Genomic studies have opened up new approaches to assess the evolution of pathogens over a period of time. However, the fungal genome called secretome deciphered that various traits housed in the pathogen and interact with hosts at various stages of development. Owing to the limited knowledge on the genome of H. vastatrix, identification was possible for only a fraction of secretome. Porto et al. (2019) were successful in comprehension of H. vastatrix secretome by sequencing and assembly of the whole genome utilizing next-generation sequencing platforms (NGS) and hybrid assembly methods. With the result a 547 Mb genome of H. vastatrix race XXXIII (Hv33) with 13,364 anticipated genes encoding 13,034 putative proteins along with transcriptomic support were recognized, which contain 615 proteins putative peptides, and absence of transmembrane areas. By this putative secretome, 111 proteins have been recognized as candidate effectors (EHv33) elite to H. vastatrix. Porto et al. (2019) have chosen a subset of 17 EHv33 genes for expression analysis during disease development and reported that incompatible interaction of five genes was altogether induced early, portraying their job as effectors of pre-haustoria in the resistant coffee germplasm. Thus, in compatible interaction, nine genes were fundamentally expressed after the formation of haustorium. With the proteomic and secretome contemplates, Porto et  al.

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Fig. 1.3  Most devastating plant pathogens that cause significant damage to agricultural food production: late blight of potato (Phytophthora infestans) (a–c); coffee rust (Hemileia vastatrix) (d, e); stalk rot of maize (Fusarium verticillioides) (f–h)

(2019) proposed that H. vastatrix is competent to specifically mount its endurance approach with effectors, which relies upon the host genotype associated with the disease development (infection process).

1.5.2  Phytophthora infestans The causative agent of late blight Phytophthora infestans occurs on high numbers in solanaceous crops (potato, brinjal, tomato and many other recorded hosts) around the world. Lately a sensational advancement in molecular examinations of

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P. infestans includes the buildup of novel devices for gene silencing and transformation and the assets for genetic, physical and transcriptional mapping of the genome. Various developmental processes are required for successful cause of disease by P. infestans in host (e.g. development of zoospores, encystment, formation of a germ tube, advancement of appressoria, haustoria, hyphae and sporangiophores) (Birch and Whisson 2001; Birch et al. 2003). In potato-Phytophthora pathosystem, collections of core RXLR effectors were identified for potential long-lasting late blight-­resistant genes. Ten Avr RXLR genes disclosed the genes responsible for resistance (e.g. R2, Rpi-blb2, Rpi-vnt1, Rpi-Smira1 and Rpi-Smira2) in cultivars of potato. Further, investigation on eight SFI (inhibitor of early Flg22-induced response) and RXLR effector genes (e.g. SFI2, SFI3 and SFI4) has shown highly expressive nature in all strains, suggesting their function in the early stages of infection of pathogen (Yin et al. 2017). The first draft genome of P. infestans described by Haas et al. (2009) (240 Mb) results from a proliferation of repetitive DNA account about 74% of the genome. The proteome of incompatible and compatible interactions among potato and P. infestans differ and provide valuable information on the role of some important proteins expressed during incompatible reactions, which could be exploited by molecular biologists to develop resistant lines against late-blight fungus. Xiao et al. (2019) provided the quantitative proteomic data of potato leaves infected with P. infestans in an incompatible reaction during early as well as late stages of disease. Xiao et  al. (2019) also demonstrated that the changes in protein abundance over 80% were upregulated during the early stages of infection and differentially expressed proteins (61%) were downregulated in the advanced stage of disease. Significant coordination and enrichment of cell wall-associated defense of proteins in the early stage of infection was observed. The advanced disease stage was evidenced by membrane protein complex formation and cellular protein modification followed by induction of cell death.

1.5.3  Fusarium verticillioides Fusarium verticillioides has dual role in maize as an endophyte without disease symptoms and cause disease as a pathogen (seedlings, stalks, ears and roots) (Brown et al. 2008). The molecular mechanisms of infection are understood poorly, which hampers breeding programmes. The genetic mechanism underpinning this pathosystem has been recently explored by Kim et al. (2018). They showed that striatin-­ like protein called Fsr1 plays an important role in development of stalk-rot disease. They also explored the NGS technology to record the relative abundance and to infer the co-expression of networks utilizing the preprocessed expression. Kim et al. (2018) further analyzed the RNA-seq data through cointegration-correlation-­ expression, where genes of maize have been jointly analyzed by known virulent genes of F. verticillioides to disclose the genes involved in defense. Using these mechanisms, several computational models have been developed to identify the

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genetic subnetwork involved in defense response of maize against F. verticillioides (Kim et al. 2015, 2018). Wang et al. (2016) revealed the disease resistance of BT-1, the maize inbred line, which has high protection against ear rot utilizing RNA high-throughput sequence. Analysis of RNA sequence data from the BT-1 kernels prior and after inoculation of F. verticillioides resulted in dramatic change of transcript levels of genes involved in key pathways in comparison with control. Wang et al. (2016) affirmed differential gene articulation in ear-rot resistant as well as susceptible maize by RNA microarray and qRT-PCR investigations. Subsequent examination revealed the involvement of family of small heat-shock protein, secondary metabolites and the signaling pathways (abscisic corrosive, jasmonic corrosive and salicylic acids) in pathogen-related molecular pattern-activated immunity against F. verticillioides. Such data explain the molecular mechanism of resistance of ear rot as well as depict the molecular resistance against the invading pathogen. F. verticillioides can synthesize fumonisins at any stage (mycotoxins family similar to the sphingolipid sphinganine). Intake of maize contaminated with fumonisin causes several animal diseases such as cancer in rodents and oesophageal cancer in humans, with some evidence suggesting neural tube defects. There are several challenges that need to be tackled especially to eliminate contamination of fumonisin in maize as well as maize products. Knowledge on such toxins produced during F. verticillioides-­maize disease leads to develop suitable strategies to control tissue destruction (by rot) as well as production of fumonisin. To achieve this goal, data on the genomic sequence, expressed sequence tags (EST) along with microarrays, are used in precise identification of genes of F. verticillioides engaged in the synthesis of toxins involved in pathogenesis.

1.5.4  Molecular Biology Tools In the past, study of plant-microbe interaction was not easy owing to difference in sequencing systems and constraints to overcome the interruption of errors. Molecular biology tools are precise and highly powerful, becoming handy towards reliable understanding of the plant-microbe interactions. Research developments in the last two decades offered powerful and precise tools to unravel the complexity of the plant-microbe interaction. Introduction of NGS offers a large number of nucleotide data within a short time to pursue metagenomics, which allows clear-cut study of microbiota including non-culturable microbes associated with an organism or in a specific environment. Thus, the NGS technologies have revolutionized the biological research during the last few years. Advances in molecular biology resulted in use of metagenomics to follow plant-­ microbe interactions more precisely (Rincon-Florez et  al. 2013). Due to high-­ throughput technique of NGS, it is easy to produce a huge amount of sequencing data at low cost (Kumari et al. 2017). To understand the nature of plant-microbe communities explicitly, knowledge on the metagenomics (DNA),

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metatranscriptomics (RNA) and metaproteomics (amino acid) plus spectral analysis of metabolites of the microbial communities associated with the host are necessary (Singh and Reddy 2015). Microbial metabolomics is capable to evaluate the metabolites present within microbial communities. Through metabolomics it is possible to assess the whole set of metabolites of host microbial communities, which provide a precise picture of the actual physiological state of the microbiome associated with the host (Kothari et al. 2016). The US Department of Energy Joint Genome Institute (US DOE JGI) has generated the integrated microbial genome system (IMG) accessible to the scientific community worldwide for evaluation of microbial genome distribution as well as datasets of metagenome (Markowitz et al. 2014). It integrates the genomes from all domains of life and provides tools for analysis and review of structural as well as functional annotations of genomes on a comparative basis. Likewise, the IMG/W (http://img.jgi.doe.gov/w) allows analysis of available genomes in public domain, the IMG/ER (http://img.jgi.doe.gov/er) provides precise review on genome annotations, and the IMG/EDU (http://img.jgi.doe.gov/edu) assists teaching as well as research in the area of analysis of genome including editing (Gómez-Merino et al. 2015). Obtaining information of microbial communities through different OMICS techniques must be the future goal to represent high-resolution authoritarian maps of the activities as well as physiological potential of host microbiome in plant-­ microbe associations. The data generated through various higher-end technologies like genome sequencing, proteomics, transcriptomics and metabolomics will explain differentially expressed genes at various conditions (stress, defense or climate change) of microbially mediated host processes for further advances.

1.6  Small RNAs’ Role in PMI Small RNAs are approximately 20–40-bp-long noncoding RNA molecules which exist in most eukaryotes and play a significant role in gene regulation and expression in a sequence-specific way transcriptionally or post-transcriptionally (Baulcombe 2004; Chapman and Carrington 2007; Jin 2008; Vaucheret 2006; Vazquez 2006). Based on their biological origin and precursor structure, the small RNAs are grouped into two specific groups: (1) microRNAs (miRNAs) and (2) small interfering RNAs (siRNAs). The sRNAs control enormous biological processes like metabolism, development and maintenance of genome integrity in plants including abiotic stress reactions and immunity against pathogens. Expanding proof recommends that the sRNAs assume a key role in controlling the communication of pathogens associated with plants (Katiyar-Agarwal and Jin 2010). Plant protection reactions against pathogens are intervened by activation and suppression of a large number of genes involved in pathogenesis. Host’s endogenous sRNAs are fundamental in the gene expression reprogramming process. Katiyar-Agarwal and Jin (2010) provided an exhaustive review on pathogen-regulated host miRNAs as well as siRNAs and their functions in plant-microbe interaction. They presented sRNA

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pathway during host-pathogen interaction and involvement of Dicer-like proteins, twofold stranded RNA binding proteins, RNA-dependent RNA polymerases, sRNA methyltransferase HEN1 and Argonaute (AGO) proteins in immune responses. The significant function of sRNAs in plant development and improvement was demonstrated (Palatnik et al. 2003; Mallory and Vaucheret 2006). Additional proof is available regarding sRNAs association in control of plant responses under undesirable conditions (e.g. biotic stress) (Chellappan et al. 2009; Chisholm et al. 2006). The sRNA pathways in plants have been explicitly portrayed in Arabidopsis. Advance and reverse genetic screens have outlined the cell proteins engaged in origin and function of miRNAs as well as siRNAs. Strategies of pathogens developed to stifle the host’s small RNA (sRNA) pathways are additional proof. By and large, the host sRNAs and RNA silencing apparatus constitute a basic layer of barrier in defense to control interactions between pathogens with plants (Katiyar-Agarwal and Jin 2010). Plants have developed different layers of protection because of pathogens, and bacterial pathogens exhibit their experience at different levels. The primary interaction among the pathogen and the host triggers pathogen-associated molecular pattern (PAMP) and pathogen-­ triggered immunity (PTI) in plants. Bacterial pathogens oppose against PTI by transporting effector proteins into plant cells, which suppress the PTI.  The host plants thus have developed resistance segments, for example, resistance (R) proteins that perceive effectors and evoke effector-triggered immunity (Chisholm et al. 2006; Jones and Dangl 2006). Development of defense through virus-derived sRNAs is an important example for interaction between the plant and pathogen involving sRNAs. These sRNAs are derived from infectious virus and exogenous in origin. Plant pathogenic viruses multiply inside the host cell by utilizing the host machinery for its survival, but others such as bacteria, fungi, nematodes and viroids interact with plants without replication of genetic material, and transcription takes place using the host machinery. In these connections, host endogenous sRNAs have a significant role in checking the pathogens. Current reports have demonstrated that plant endogenous siRNAs, miRNAs and siRNAs are the necessary regulatory segments of plant resistance against various plant pathogens.

1.7  Systems Biology and Metabolomics Engineering Understanding the characteristics of interactions of microorganisms and other biotic factors are the essential primary steps. This helps to follow the association as well as functions of microbial communities in different ecosystems. In the recent era of systems biology (SB) and modeling world, bioinformatics approach plays a major role in deciphering the gene to gene interactions and organism to environment interactions. SB investigates genes, proteins and their associative interactions inside a cell, tissue or entire living being and empowers to comprehend the complex biological framework through demonstrating with the assistance of computational systems. SB and genome-level metabolic models (GEM) computationally depict

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gene-­protein reaction and associations for whole metabolic genes in an organism and could be simulated to understand the metabolic fluxes for various systems-level metabolic aspects like plant-microbe interactions (endophytic, parasitic, mycorrhizal and others). In SB, the presence of well-devised tools such as flux balance analysis (FBA), OptKnock and constraint-based modeling helps in understanding plant-microbe interactions as a whole and specifically the gene interactions within the system. The availability of gene editing tools developed strategically facilitates to follow the development of disease-free plants and elucidating several other gene-­ to-­gene interactions. The secondary data of high-throughput sequencing sources including single-nucleotide polymorphism detection, DNA whole genome sequencing, RNA-seq, proteomics and transcriptomics are available from public databases (NCBI, NIH and other public libraries) that could be used to construct metabolic models. Thus, network biological modeling in SB will be helpful to understand the insight of network as well as interactions (Kumar et al. 2016; Yadav et al. 2019b). Plants create a nutritionally enriched environment that favours colonization of diverse microbes (e.g. epiphytes and endophytes). Thus, the microbial communities and their interaction greatly influence positively or negatively plant physiology (e.g. amensalism, commensalism, mutualism and pathogenic consequences) (Kour et al. 2020c; Rastegari et al. 2020a). In endophytic microbe-host interaction (bacteria and fungi), the microbes live in a noncompetitive conditions of host plant tissue without causing any severe harm to the host cell (James and Olivares 1998; Kumar et al. 2016). These endophytic microbes are present in almost all plant species, and they were believed to be developed from the aerial part of plants, seeds and rhizosphere (Gao et  al. 2004; Seghers et  al. 2004; Castro-Sowinski et  al. 2007; Imam et  al. 2013). Several facultative endophytes have been reported from the crop plants like Arabidopsis, cotton, maize, potato, rice, sorghum and wheat. In addition, many endophytic microbes have been isolated from a single plant. Study of such interaction by microbes conventionally leads to laborious experimental bioassays (laboratory and field trials) (Kato et al. 2005; Harcombe 2010; Zeidan et al. 2010). The bioinformatics approaches facilitate to overcome these constraints by understanding plant-microbe interactions for validation (Freilich et al. 2011; Buffie et al. 2014; Lima-Mendez et al. 2015). These approaches provide different types of predictable species abundance measurement from high-throughput sequencing or reconstructed metabolic models and community interactions. There are several reports in related fields, involving advanced technology like gene editing and genome engineering, which help significantly with other in silico methods to analyse interactions (Pritchard and Birch 2011; Xu et al. 2013; Gupta and Shukla 2015a, b, 2016; Dix et al. 2016; Kumar et al. 2016). There are a few important studies on tools of SB and molecular modeling to follow the microbial enzymes and like proteins, but there is no much scope for assessment of role of proteins in plant-microbe interaction (Singh and Shukla 2011, 2015; Karthik and Shukla 2012; Baweja et al. 2015, 2016; Singh et al. 2016).

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1.7.1  The Technique of Systems Biology Metabolic designing of various microbes for the production of different products has lead application of metabolic engineering in different aspects of agricultural, industrial and medical microbiology (Chotani et al. 2000; Nakamura and Whited 2003). Interactions between host and pathogen assume a key role in increased signaling cascade to change the protein leading to phenotypic articulation. In silico transcriptome analysis of the host and pathogen during the infection (host-pathogen interaction) will provide information on events occurring during the disease development. There is a dynamic complexity in the plant-microbe interactions, which manifest since boundaries represent processes in biological networks, which are subject to different factors in the system (Kumar et al. 2016). The accumulations metabolites in metabolic and signaling processes change after some time accordingly there could be a few different means to develop model this time-consuming process. The metabolic networks and their dynamic qualities might be significant, and these procedures ought to be affirmed with substantial test models. The topologies identified with metabolomics of cell are dynamic among the compartments, and they change with time. The targeted motive of metabolic engineering could be different, but the innovation, technology and platform remain unchanged. In the era of molecular biology, computational modeling finds its place and changed the view of metabolic engineering. The computational modeling foresees the impact of genetic controls on metabolism. However, they should be supplemented with enzyme kinetics (Tepper and Shlomi 2010). The constraint-based modeling (CBM) is another technique, which is a substitute to beat the issues by analysing the capacity of metabolic systems by depending on physical-chemical impediments (Price et al. 2003). The genome-scale network models for some microorganisms are available (Förster et al. 2003; Reed et al. 2003; Duarte et al. 2004). The CBM has demonstrated to be effective for large-scale microbial systems, which includes metabolic engineering investigations for various applications (Kumar et  al. 2016). Metabolic remaking (reconstruction) is a well-organized portrayal of the network topology that empowers inference of genome-scale models (GEMs), which are utilized to impersonate distinctive metabolic conditions of a life form (Satish Kumar et al. 2007; Thiele and Palsson 2010; Esvelt and Wang 2013). All these SB approaches have gained popularity as they are coordinated with OMICS in complete examination of interaction of metabolic systems (Saha et al. 2014). A portion of the model plants for those metabolic reproductions are accessible for Arabidopsis, maize, sorghum and sugarcane (Poolman et al. 2009; de Oliveira Dal’Molin et al. 2010a, b; Saha et al. 2011). The SB could be applied to examine the effectors and their pathogenesis in host-­ pathogen interactions. The OptKnock is another system that searches bunch of gene knockouts results in generation of desired products (Burgard et  al. 2003) and encourages comprehending obstruction of plants from pathogen or pathogen-­ determined factors. The OptStrain performs two functions: (1) it allows gene knockouts and (2) consolidates novel enzyme coding genes from various species of the microbial genome (Pharkya et al. 2004). The OptReg is the most recently developed platform, which searches manipulation in up- and downregulation of metabolic

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enzymes in addition to gene knockouts to meet the desired metabolic production (Pharkya and Maranas 2006).

1.7.2  The CRISPR-Cas in Plant-Microbe Interaction Advancement of effective and reliable source to develop precise, directed (targeted) alterations to the genome of cells is a long-pending objective for biomedical specialists. Genome altering with site-specific nucleases permits inverts genetics, genetic engineering (genome engineering) and targeted transgene incorporation in a proficient way. Along these lines, the molecular scissors (engineered nucleases) are used in altering their ability to change the ideal DNA piece. The CRISPR-Cas9 is an interesting innovation empowers medical researchers or geneticists to modify portions of the genome by drive out and comprise or alter areas of the DNA sequence. The CRISPR-Cas is an effective, simple and straightforward framework, which is otherwise called third-age programmable nuclease (Kanchiswamy et al. 2016; Xu et al. 2014). Up to this point, 11 CRISPR-Cas frameworks have been accounted for assuming key job in crop security (Ma and Liu 2016). Each category has its own particular Cas protein segment, which is named by the model living being. The CRISPR clusters were first distinguished in the Escherichia coli during 1987 without elucidation of their biological properties (Ishino et al. 1987). In 2005, it was demonstrated that the spacers were homologous to viral and plasmid sequences proposing their function in adaptive immunity (Bolotin et al. 2015; Mojica et al. 2005; Pourcel et al. 2005). Further research on Cas provided insights of CRISPR role in pathogenesis and protection against invading pathogens. The CRISPR-Cas have been reported playing a key role in crop protection against attacks or infections (Barrangou et al. 2007). The component of this resistant framework dependent on RNA-interceded DNA focusing has been illustrated by various workers (Brouns et  al. 2008; Deltcheva et  al. 2011; Garneau et  al. 2010; Marraffini and Sontheimer 2008). The presence of multiple cloning sites in a cell was exploited for multiple editing using different gRNAs (e.g. genetic variations through genes which are practically identified with control complex characteristics) (Ma et  al. 2015; Xie et  al. 2015; Zhou et al. 2014). In an examination, articulation of Cas9 and sgRNA qualities in tobacco and Arabidopsis caused a cleavage on targeted site of a non-useful green fluorescent protein (GFP) gene. Further, changes by nonhomologous end joining (NHEJ) DNA fix prompted the generation of a solid green fluorescence in changing cells of leaf (Jiang et al. 2013, 2014). To increase the Cas9 expression in plants, codon streamlining is frequently followed deliberately (Fauser et  al. 2014). The constitutive promoters of ubiquitin genes present in Arabidopsis, maize and rice are capable to govern the expression of Cas9 gene in monocots and dicots. The bacterial CRISPR-Cas could be employed to hinder the viral genetic material with the activity of Cas9 as a nuclease to understand viral infection in the plants (Ali et al. 2015; Baltes et al. 2015; Chaparro-Garcia et al. 2015; Ji et al. 2015).

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1.8  Challenges and Future Outlook Even though significant contributions are made towards understanding of plant-­ microbe interactions at various levels, there are several lacunae which need to be addressed to exploit the beneficial traits. Harnessing microbiome plays a key role to build up new technology, products and process to benefit farmers, environment and policymakers. There are diverse rhizosphere microbiomes that have the potential to defeat the invading soil pathogen and promote the growth of host, thereby increasing the yield. There are several microbes thriving in extreme habitats (high temperature, low temperature, deserts, deep sea and other niches) which need to be documented, and their survival mechanisms have to be elucidated to adapt strategies to derive benefit from plant-microbe interactions. Microbes play major role in a wide range of ecosystems by interactions with host plants, biotic and abiotic conditions of the habitat, which helps sustained plant health as well as ecological sustainability. Thus, comprehension of such interactions and their specific knowledge is very important to improve the plant health for agricultural and ecosystem stability. The ecological behaviour of microbes and their interaction with eukaryotes need to be assessed. Such studies will help to document the rich biodiversity and its potential exploitation and also to understand the risks before commercialization. A large number of bioinoculants have been released into the field, and most of them are having beneficial traits. However, multifaceted studies will help to reduce the risks associated with negative effect of such bioinoculants in the long run. Legislative support is obvious for effective commercialization of bioinoculants. Research need to be performed to assess the future risks on environment and other life forms. The growing demand for disease-resistant crops necessitates screening better bioinoculants for sustainable biofertilizers employing mutualistic microbes. This area needs more advances to develop viable technology-based molecular platforms. The modulation of plant development through microbial effectors is an emerging area of research, and these modulations hold the key for the success of their exploitation in many ways. Unraveling plant target processes will aid an insight to develop genetic control of pathogens to keep unwanted defects in control. It is necessary to understand and explore the nature of interaction explicitly (type-specific, host-­ specific and other specificity interlinked to their ecological interactions at molecular level). Currently, high-throughput OMICS approaches including genomics (to understand the structural and functional processes of genes and for compression of the degree of gene expression in genotypes), transcriptomics (quantitative study of mRNA transcripts), proteomics (protein composition analyses) and metabolomics (identification and quantification metabolites of cells) are available. It is important to have a better understanding of signaling pathways and metabolic networks to follow the plant-microbe interactions. In the near future, the CRISPR-Cas is expected to be a significant tool to engineer plants to overcome constraints like low yields, low nutritional value and susceptibility to diseases. This technique could be developed into a main weapon to prevent the viral diseases of crop plants.

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Pathogen-derived small RNAs and their functional annotations need to be exploited in various groups of phytopathogens including bacteria, fungi, nematodes, viruses and viroids. In most of the plant-microbe interactions during pathogenesis, pathogen-derived small RNAs suppress the host’s mRNA, which result in least expression and enhancement of pathogenesis. It is more effective particularly in subcellular pathogens like viruses, viroids and Phytoplasma. Further research need to be focused to explore the pathogen-derived small RNAs and host’s response to revert such signaling small RNAs. Innovative research progress in agricultural sector will play a key role for future agri-production and improvement of quality. In order to enhance our current knowledge on PMI, an integrated approach by computational biology with genomic tools will be crucial to follow the communication, metabolic and other associated regulatory pathways towards harnessing beneficial traits of plants. The success of industrialization of bioinoculants is dependent on innovations in product development, marketing and awareness among the farmers to achieve the goal. Plant-associated microorganisms remain as an integral part, and plant’s surrounding environment influences plant health, yield potential and increased biomass production. Therefore, precise knowledge on interactions and their genetic makeup is necessary to determine their significance in exploitation to combat diseases in crops. Rhizosphere, being an interlinked complex ecosystem, accommodates a large number of microbes that influence plant growth and development by various mechanisms. Most studies performed on plant-microbe interactions are gene-based and OMICS-based, but very few followed metabolomics. However, there is an ample scope to study the early stages of synthesis of various signaling molecules and their modulation to predict their destiny in primary as well as secondary metabolism. The involvement of secondary stimuli perceived by the host plant species greatly helps fighting the invaders (biotic constraints) through production of PRPs and other proteins. There are several changes associated with host’s physiological state, which reflects modification of expression of certain genes, proteomics and metabolomics to trigger secondary stimuli. Further investigations by targeted and untargeted metabolomics approaches would shed light to follow the underpinning mechanisms. However, most of the research focused on individual organisms rather than the complex consortium of plant-soil rhizomicrobes (rhizobiome, endophytes and pathogens). With the technological advances in the recent years, targeting biological and chemical changes associated with plant-microbe interactions through metabolomics and targeted phytobiomes would be the future targets to unravel the complexity of chemical and biological communications in such complex associations. Acknowledgements  The first author (SM) is grateful to the Council of Scientific and Industrial Research (CSIR), Government of India, New Delhi for the award of Research Associate Fellowship and also acknowledges the support and encouragement by the Department of Studies in Botany, University of Mysore. The corresponding author (KRS) is grateful to Mangalore University and Yenepoya (deemed to be) University for the award of Adjunct Professorship.

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opments in microbial biotechnology and bioengineering, pp  13–41. https://doi.org/10.1016/ B978-0-444-63994-3.00002-3 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018b) Biodiversity of the genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering, Penicillium system properties and applications. Elsevier, Amsterdam, pp  3–18. https://doi.org/10.1016/ B978-0-444-63501-3.00001-6 Yadav AN, Gulati S, Sharma D, Singh RN, Rajawat MVS, Kumar R, Dey R, Pal KK, Kaushik R, Saxena AK (2019a) Seasonal variations in culturable archaea and their plant growth promoting attributes to predict their role in establishment of vegetation in Rann of Kutch. Biologia 74:1031–1043. https://doi.org/10.2478/s11756-019-00259-2 Yadav AN, Kour D, Rana KL, Yadav N, Singh B, Chauhan VS, Rastegari AA, Hesham AE-L, Gupta VK (2019b) Metabolic engineering to synthetic biology of secondary metabolites production. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  279–320. https://doi.org/10.1016/ B978-0-444-63504-4.00020-7 Yadav AN, Singh J, Rastegari AA, Yadav N (2020) Plant microbiomes for sustainable agriculture. Springer International Publishing, Cham Yin J, Gu B, Huang G, Tian Y, Quan J, Lindqvist-Kreuze H, Shan W (2017) Conserved RXLR effector genes of Phytophthora infestans expressed at the early stage of potato infection are suppressive to host defense. Front Plant Sci 8:2155. https://doi.org/10.3389/fpls.2017.02155 Zeidan AA, Rådström P, van Niel EWJ (2010) Stable coexistence of two Caldicellulosiruptor species in a de novo constructed hydrogen-producing co-culture. Microb Cell Factories 9:102. https://doi.org/10.1186/1475-2859-9-102 Zhang F, Dashti N, Hynes RK, Smith DL (1996) Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann Bot 77:453–459. https://doi.org/10.1006/anbo.1996.0055 Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119. https://doi.org/10.1016/j.fcr.2005.08.018 Zhang S, Gan Y, Xu B (2016) Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front Plant Sci 7:1405. https://doi.org/10.3389/ fpls.2016.01405 Zhou H, Liu B, Weeks DP, Spalding MH, Yang B (2014) Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9inrice. Nucleic Acids Res 42:10903–10914. https://doi.org/10.1093/nar/gku806 Zhou LS, Tang K, Guo SX (2018) The Plant Growth-Promoting Fungus (PGPF) Alternaria sp. A13 markedly enhances Salvia miltiorrhiza root growth and active ingredient accumulation under greenhouse and field conditions. Int J Mol Sci 19:270. https://doi.org/10.3390/ijms19010270

Chapter 2

Rhizospheric Microbiome: Biodiversity, Current Advancement and Potential Biotechnological Applications Slimane Mokrani and Nabti El-Hafid

Abstract  The extinction of species and reducing of biodiversity is a global problem increasingly threatening food chain, balance, and life on earth. This problem also concerns underground life in the soil and more particularly the microorganisms in the plant rhizosphere. The rhizospheric region is undoubtedly among the most populated natural microenvironment in terms of microorganisms. This is due to the particular composition of these areas and the specific integrations between soil, microorganisms, and plants. Rhizospheric microbiomes are endowed with interactive metabolism and function. On the other hand, many researches are being focused on the impact of rhizospheric microbial biodiversity on plant health. The study of the biodiversity of rhizospheric soil microorganisms is currently developing many applications including agricultural, therapeutical, environmental, human and animal health, and industrial. Keywords  Biodiversity · Biotechnological applications · Rhizospheric microbiome

2.1  Introduction Microbiome inhabits the entire ecosystems and consists of numerous microbial communities (Lewin et al. 2013; Sheth et al. 2016; Foo et al. 2017; Wolfe 2018). The rhizosphere represents the attenuate strata of soil that enclose plant roots, and the soil, occupied by roots, supports significant energetic groups concerning microorganisms (Richardson and Simpson 2011; Bengtson et  al. 2012; Geetanjali and Jain 2016; Yadav 2017; Bahram et al. 2018). Rhizosphere is an important exchange interface of nutrient resource between plants and the surrounding soil (Berendsen

S. Mokrani · N. El-Hafid (*) Laboratoire de Maitrise des Énergies Renouvelables, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_2

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et al. 2012; Berg et al. 2014; Meena et al. 2017; Yadav et al. 2019a). The present chapter describes the biodiversity of rhizosphere microbiome, metabolism, and function, also its biotechnological applications in different areas as producer of bioactive compounds and current advancement.

2.2  Biodiversity of Rhizospheric Microbiomes In the soil ecosystem, plant-associated rhizosphere represents the close potential ecosystem imparting a close affiliation between plant root and rhizosphere-­ associated microbial communities (Pattnaik and Busi 2019; Yadav et al. 2019e). The plant microbiomes are agriculturally essential bioresources as they play a chief role in plant growth and improving the plant nutrition via solubilization of P, K, and Zn, nitrogen fixation, and exceptional mechanisms including the production of siderophores (Yadav et al. 2017a, b, c). Furthermore, rhizosphere is one well-investigated example; the root-soil interface is influenced through using the plant metabolism by means of root exudates (Philippot et al. 2013). The rhizosphere microflora consists of bacteria, fungi, nematodes, protozoa, microalgae, and microarthrops (Kour et al. 2020a; Raaijmakers et al. 2002; Rana et  al. 2020a). Plants apply a fundamental function in choosing and enriching the kinds of microbes by the elements concerning their root exudates. Rhizosphere microorganism concentration may reach to 1010 or 1012 cells by gram of soil (Foster 1988; Borozan et al. 2017). Thus, depending on the nature and concentrations of organic elements in exudates or the potent of the microbes to utilize it as sources on energy, the microbial community develops into the interaction (Yadav 2018; Yadav and Yadav 2018). The microbial diversity with roots is fundamental for plant survival (Ortíz-Castro et al. 2012; Verma et al. 2017b; Yadav et al. 2020) (Fig. 2.1).

2.2.1  Bacteria Bacteria are the most numerous living beings on earth, and solely a fraction of them have been recognized (Pindi and Sultana 2013); also most of the rhizospheric microbial range studies are restrained to bacteria (Dubey et  al. 2016). Bacterial communities existing in the rhizosphere of distinct plants play a crucial key function in biogeochemical cycles, plant nutrition, and disease biocontrol (Osman et al. 2017). Furthermore, it is well known that plants have an effect on the biodiversity of microorganism in soils (Gaikwad and Sapre 2015). Through their rent of compounds such as amino acids, sugars, and increase elements in plant root exudates, microbial activity and growth are influenced (Rovira 1956; Mendes et al. 2013). On the other hand, many researches certainly advise that the Proteobacteria and the Actinobacteria form the most common and dominant populations (> 1%, generally much more) in the rhizosphere of many distinctive plant species (Singh et al. 2007).

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Fig. 2.1  Categories of rhizospheric soil microbiome

The composition of microbial communities in the rhizosphere is usually determined through neighborhood biotic and abiotic conditions (Nihorimbere et al. 2011; Van der Putten et al. 2013; Wang et al. 2014; Na et al. 2018). Or, diversity can’t be affected (Stafford et al. 2005; Yamamoto et al. 2018). For example, Schmid et al. (2018) mentioned that ten most abundant phyla accounted in eight plants rhizosphere are Proteobacteria (35.4%), Bacteroidetes (10.5%), Planctomycetes (8.9%), Chloroflexi (7.1%), Actinobacteria (4.7%), Verrucomicrobia (4.7%), Acidobacteria (4.5%), Gemmatimonadetes (4.3%), Parcubacteria (3.3%), and Firmicutes (3.2%). Furthermore, a number of bacterial species related with the plant’s rhizosphere belonging to genera Azospirillum, Alcaligenes, Arthrobacter, Acinetobacter, Bacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Pseudomonas, Rhizobium, and Serratia are able to exert a really useful impact on plant increase (Kour et  al. 2019a, b; Suman et  al. 2016; Yadav et  al. 2019b). Particularly, Streptomyces are fundamental species of Actinobacteria that are in many instances located in roots of plants and terrestrial flora (Liu et al. 2015).

2.2.2  Fungi Fungi are an essential component of soil microbiota greater in abundance than bacteria, relying on soil depth and nutrient conditions (Chandrashekar et al. 2014). Soil fungi are equally fundamental element of agroecosystems, and the rhizosphere fungal communities play necessary roles in plant growth and health (Qiao et al. 2018). They are ubiquitous microorganisms that play necessary functions as primary decomposers of organic matter, and they release nutrients for the duration of nutrient cycling that stimulate plant increase (Lodge 1995; Zhang et al. 2019). On the other hand, mycorrhizal fungi are a heterogeneous group of various fungal taxa, associated

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with the roots of most, over 90% plant species affecting plant health and nutrition and soil structure (Read 1991; Rillig and Mummey 2006; Bonfante and Genre 2010). Examination of vegetables and rhizospheric soil of distinct plants revealed 61 species of filamentous fungi, of which 12 belonged to the genus Penicillium, 4 to the genus Fusarium, and 2 species every to the genera: Aspergillus, Cladosporium, and Trichoderma (Kłapeć et  al. 2018). The fungal communities determined in potato rhizospheric soil were Ascomycota, Zygomycota, Basidiomycota, Chytridiomycota, and other unidentified fungal communities (Qin et al. 2017). In tomato rhizosphere Ascomycota was once of the most abundant phylum; Oomycota and Zygomycota were the other constituents. Totally, eight genera have been recovered, and these have been dominated through Aspergillus. A total of 12 fungal species have been found. The most frequent species were Aspergillus quadrilineatus, Cephaliophora sp., Mortierella sp., Penicillium corylophilum, Chaetomium sp., Cladosporium tenuissimum, Aspergillus pachycristatus, A. rugulosus, Fusarium nygamai, F. solani, and Pythium aphanidermatum (Kazerooni et al. 2017; Yadav 2019; Yadav et al. 2019c, d, 2020). Especially, among the fungal community in the rhizospheric soil, Ascomycota was discovered to be the dominant fungi genus (Qin et al. 2017). It is apparent that the special plant kinds support distinct fungal populations (Bailey et al. 2006). Soil pH has an important influence on the composition of the fungal community in rhizospheric soil (Song et al. 2018), as well as environmental factors such as nutrient resources, biotic and abiotic factors, tillage device, and microbial interactions that forestall the occurrence or survival of the species in the surroundings (Gałązka and Grządziel 2018). Sampling season as well as the taxonomy, nativeness (native or alien), life-form (herbaceous or woody), and mycorrhizal kind of host plants may contribute to variation in fungal microbiome compositions among distinctive co-occurring plant species (Toju et al. 2019). Furthermore, plant developmental stage and soil type, rhizospheric and bulk soil, can have an effect on fungal community and diversity (Qiao et al. 2018).

2.2.3  Nematodes Nematodes (also known as roundworms, threadworms, or eelworms) are some of the most numerous multicellular organisms in a large vary of soil. They proliferate in the water-filled pores of soil, as do protozoa and rotifers. The rhizosphere is especially an energetic region for nematode proliferation (Franzluebbers 2009). Most nematodes in soil are free-living; however some appear on the root exterior (migratory ectoparasitic), and other penetrate then pass in the root interior (migratory endoparasitic), while others improve the feeding site in the root (Mendes et  al. 2013). They usually consist of phytoparasitic nematodes that feed on roots and microbes (Chen et al. 2007). The rhizosphere microbiome can influence the invasion and the reproductive success of plant-parasitic nematodes and thus influence plant damage (Elhady et al. 2018). Plant parasitic nematodes in particular pose a serious risk to the global economic system and are responsible for exquisite losses

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in production structures worldwide (Abd-Elgawad and Askary 2015). In addition, all plant-parasitic nematodes have a stiletto, a strong, hollow, needle-like structure used to puncture plant cells, inject nematode secretions, and feed on plant cell contents (Bonkowski et al. 2009). For example, the most frequent genera of plant parasitic nematodes related with banana were Pratylenchus, Meloidogyne, Helicotylenchus, Tylenchorhynchus, Hoplolaimus, Rotylenchulus, Hirschmanniella, and Criconemoides (Khan and Hasan 2010). Another illustration of plant-parasitic nematode variety was determined in potato plants in Dakahlia Governorate, Egypt, and associated genera were Criconemoides, Helicotylenchus, Heterodera, Longidorus, Meloidogyne, Pratylenchus, Rotylenchulus, Tylenchorhynchus, Xiphinema, and Tylenchus (Gad et al. 2018).

2.2.4  Protozoa Protozoa are unicellular, heterotrophic, eukaryotic organisms including four organization types: amoebae, flagellates, ciliates, and parasitic sporozoans (Foissner 2005; Franzluebbers 2009). Like bacteria in the rhizosphere, protozoa are particularly functional in addition to the roots. The typical number of protozoa in soil varies widely, from a thousand per teaspoon in low fertility soils to one million per teaspoon in some noticeably fertile soils. Mastigophora or flagellates dominate in drier soils, while Ciliophora or ciliates are only significant if the soil moisture level is too high (Hoorman 2011). It has been shown that the ratio of soil protozoa in the rhizosphere and the presence of protozoa significantly prolong plant growth (Zwart et al. 1994). Experiments on planted microcosms provided robust evidence of the importance of protozoan willow in the rhizosphere (Bonkowski 2004). The evidence reveal that the sowing of wheat in presence of protozoa had larger and longer L-type side roots, which are fundamental factors in building a strong fiber root system used to absorb nutrients (Bonkowski and Brandt 2002).

2.2.5  Microalgae Algae are less several than fungi in soil. Algae can also be unicellular (Chlamydomonas) or filamentous (Spirogyra and Ulothrix). Algae contain chlorophyll, and they are phototrophic organisms. They use CO2 from the atmosphere and produce O2. Some of the frequent green algae occurring in most soils belong to the genera Chlorella, Chlamydomonas, Chlorococcum, Oedogonium, Chlorochitrum and Protosiphon (Lynch 1990). Since investigations on the ecology of soil algae have proven that this microbial group constitutes an essential element of the soil biota (Florenzano et  al. 1978), among which microalgae that form an important group include eukaryotic and prokaryotic cyanobacteria or blue-green algae (Chiaiese et al. 2018).

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Considering the modern system of eukaryotes, soil microalgae contain photoautotrophic microorganisms that are phylogenetically nested inside five kingdoms Archaeplastida, Excavata, Stramenopila, Alveolata, and Cryptophyceae. Particularly, cyanobacteria play an essential function in the upkeep and build up of soil fertility, hence growing rice increase and yield as a natural biofertilizer (Song et al. 2005). Also, cyanobacteria are a team of microorganism that can repair atmospheric nitrogen. Blue-green algae (BGA) can adapt to a range of soil kinds and surroundings which has made it cosmopolitan in distribution. Efficient nitrogen-fixing strains like Nostoc linckia, Anabaena variabilis, Aulosira fertilisima, Calothrix sp., Tolypothrix sp., and Scytonema sp. were identified from a variety of agroecological areas and utilized for rice manufacturing (Prasad and Prasad 2001).

2.2.6  Microarthropods Soil microarthropods are an essential element of terrestrial ecosystems due to their function as regulators of key processes, such as plant litter decomposition and mineralization (Kampichler and Bruckner 2009). In addition, there is little research into the interactions between microfauna and arthropods, but many of the microarthropods that are commonly considered saprophagic can actually be omnivorous (Bonkowski et al. 2000). Soil microarthropods, principally mites and collembolans, are among the unseen faunal diversity in nearly all agricultural soils. They take part in the complicated food webs of soils, but their significance is seldom appreciated. Laboratory and field effects exhibit that microarthropods affected organic debris, microbial decomposers, nematodes, roots, and pathogenic fungi (Crossley Jr et al. 1992). The distribution of certain arthropod taxa was correlated with physical and chemical soil properties and additionally with the distribution of different arthropod groups. Species diversity was extensively decreased by means of the manuring (El-Gayar et al. 2009).

2.3  Rhizospheric Microbiome Metabolism and Function The physiochemical environment over the rhizosphere helps a microbial community to differentiate compositionally and metabolically from the amount in the soil (Kaur et al. 2020; Mendes et al. 2013; Singh et al. 2020). Plants are successful in modulating the density, identity, and relationship of the microbial population and influencing functional activities as mediated by soil microbial communities (Essarioui et al. 2017). Microbial genomics is also suddenly advancing, including extensive collections of isolated rhizosphere strains and mutant libraries that provide up-to-date knowledge of the metabolic mechanisms related to root colonization (Jacoby and Kopriva 2018).

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Rhizospheric microbiome affects plant life thru a range concerning mechanisms consisting of production of siderophores, phytohormones (as gibberellins and indole-3-acetic acid), phosphate solubilization, bacteriocins, lytic enzymes (proteases, lipases, chitinase, B-glucanase), antibiotics, and volatile compounds like hydrogen cyanide (Khamna et al. 2009; Gutiérrez-Mañero et al. 2001; Majeed et al. 2015; Santos et al. 2013; Subramanian and Smith 2015; Verma et al. 2016, 2019; Mazurier et al. 2009; Rijavec and Lapanje 2016). In return, existing plants deposit their photosynthetically regular carbon within their direct surroundings (spermosphere, phyllosphere, rhizosphere, and mycorrhizosphere) thereby maintaining the microbial community and influencing its composition and activities (Mendes et al. 2013). Rhizospheric microbes help the plants to assemble different nutrients and indirectly provide protection from pathogens (Gkarmiri et  al. 2017). In addition, according to the direct consequences of harmful microbes in the rhizosphere, many useful soil-based microorganisms have been identified to improve the ability of aboveground components to protect plant parts (Rastegari et al. 2020b; Singh and Yadav 2020; Zamioudis and Pieterse 2012). A mechanism that is recognized as induced systemic resistance (ISR), plants keep their resistance toward pathogen attacks, so much should be fatal without these bacterial strains occurring (Quiza et  al. 2015). The effectiveness of the rhizosphere microbiome in activating plant tolerance to abiotic stress such as drought and heavy metals was investigated by many researchers (Rolli et al. 2015; Coleman-Derr and Tringe 2014; Hussain et al. 2018; Lo Shllev et al. 2001). Direct and indirect interactions take place in the rhizosphere, such as plant-plant, microbe-microbe and plant-microbe (De-la-Peña et  al. 2012; Kour et  al. 2020b; Rana et al. 2020b). Furthermore, interactions within exudates and soil microbiome exhibited a dynamic effects on rhizospheric and change plant phenotypes through the use of complex feedback mechanisms (Kumar et  al. 2019; Lu et  al. 2018; Rajawat et al. 2020). Figure 2.2 showed rhizospheric microbiome diversity, mechanisms, and interactions.

2.4  Potential Biotechnological Applications New microbial metabolites are strongly requested to increase the resitance to pathogens, diseases and toxic  compounds (Demain 1999). Microorganisms produce a prosperity concerning structurally various specialized metabolites together with a remarkable range of natural activities and a significant range of functions between medicine and agriculture, certain as much the treatment of infectious diseases and cancer and the prevention of crop plants damage (Rutledge and Challis 2015). The potential biotechnological applications of rhizospheric microbiome include therapeutical, industrial, agricultural, environmental, human and animal health (Saxena et al. 2016; Verma et al. 2017a; Yadav et al. 2018). These plant growth-promoting microbes could be utilized as bioresources for sustainable agriculture and environment (Kour et al. 2020c; Rastegari et al. 2020a) (Table 2.1 and Fig. 2.3).

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Fig. 2.2 Rhizospheric microbiome diversity, mechanisms, and interactions. (SAR systemic acquired resistance, ISR induced systemic resistance)

2.4.1  Agricultural Usage The use of microbial inoculants in agriculture represents an attractive eco-friendly alternative to fertilizers and chemical pesticides (Bashan 1998; Adesemoye and Kloepper 2009; Owen et al. 2015; Baez-Rogelio et al. 2017). Members of the bacterial genera Azospirillum, Rhizobium, Bacillus, Pseudomonas, Serratia, Stenotrophomonas, and Streptomyces or the fungal genera Ampelomyces, Coniothyrium, and Trichoderma are well-studied examples because of plant growth promotion (Berg 2009). Plant growth-promoting rhizobacteria (PGPR) are free-­ living microorganisms with an advantageous agricultural importance (Kour et al. 2020d; Rana et al. 2020c). The PGPR contemporaries have excellent consequences for plant health and plant growth, suppress disease-causing microbes, and accelerate nutrient availability and assimilation (Babalola 2010). Biofertilization improves macro- or micronutrient acquisition (uptake and assimilation) by plants (De Jesus Sousa and Olivares 2016). Mycorrhiza represents a symbiotic association between

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Table 2.1  Examples of rhizosphere-associated microorganisms and their applications Microorganisms Lychnophora ericoides Streptomyces albogriseolus Pseudomonas grimontii Bacillus amyloliquefaciens Bacillus subtilis SL-44 Serratia marcescens strain B2 Serratia sp. SY5 Trichoderma harzianum Pseudomonas sp.

Associated root plant Lychnophora ericoides Mart.

Mechanism Anti-cancer (cytotoxic activity) Aloe indica Antibacterial activity Vicia sativa Biological control Phaseolus vulgaris Biofertilization L. Gossypium Biological herbaceum control Solanum Biological lycopersicum L. control Echinochloa crus-galli Macrophominaph aseolina Calotropis sp.

Biofertilization Biological control Soil bioremediation Wastewater bioremediation Probiotic

Azospirillum lipoferum Bacillus sp.

Oryza sativa

Penicillium fellutanum

Rhizophora mangle Amylase

Streptomyces sp. MM-3

Psidium guajava

Triticum aestivum

Protease

Application Therapeutical

References Conti et al. (2016)

Human health Ramakrishnan et al. (2009) Agricultural Mokrani et al. (2019) Agricultural Mokrani et al. (2018) Agricultural Huang et al. (2017) Agricultural Someya et al. (2005) Agricultural

Koo and Cho (2009) Agricultural Sreedevi et al. (2011) Environmental Shukla et al. (2012) Environmental Mann (2011) Human health Mohkam et al. (2016) Industrial Kathiresan and Manivannan (2006) Industrial Shaikh et al. (2019)

a soil fungus and plant root. Unlike rhizobia and their legume partners, mycorrhizal associations are ubiquitous taking place in ~ 80% of angiosperms and among whole gymnosperms (Wilcox 1991). Thus, biofertilization effectively improves soil fertility (Wu et al. 2005; Mallik and Williams 2008) and controls plant diseases (Caron 1989; Linderman 2000; Garcia-Garrido 2009).

2.4.2  Therapeutic Applications A range of pigments are produced by microorganisms like carotenoids, melanins, flavins, quinones, prodigiosins, and more in particular monascins, violacein, or indigo (Mumtaz et al. 2018). Pigment-producing bacteria are ubiquitous and current in a variety of ecological niches, such as rhizospheric soil (Peix et al. 2005). For

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Fig. 2.3  Biotechnological applications of rhizospheric microbiome

example, numerous researches have shown carotenoids can be used as therapeutic agent toward a range of cancers and other diseases that are appropriate according to their antioxidant and/or provitamin properties (Ungureanu et al. 2011). These pigments also have a critical role in defense against oxidative damage (Scolnik and Bartley 1995). As potential biological antioxidants, carotenoids successfully absorb the excitation energy of singlet oxygen radicals in their complex ring chain and at the same time protect tissue alongside chemical damage. They additionally prolong the generation in relation to those chain reactions which are triggered by degradation via polyunsaturated fatty acids (Guerin et al. 2003).

2.4.3  Environmental Utilization Microbial functions are particularly important for solving major environmental problems. In particular bioremediation of soil and organic/inorganic water pollution (Ahmad et al. 2011). The underground diversity of longevity can also be practiced by insurance, since plant productivity is preserved under certain environmental conditions (Tilman et al. 2001; Wagg et al. 2011). Plant-related bacteria, such as rhizosphere microorganisms, have proven to contribute to biodegradability (Dowling and

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Doty 2009). Bioremediation is an important pollutant removal technology to catalyze consumption and convert a number of types of pollution to less unfavorable types (Gałązka et al. 2012). A contribution and a use for larger cellular and/or cell-­ free enzymes have also been proposed, namely, a modern remediation technique. However, some bottlenecks avoid their useful use in restoring polluted environments (Gianfreda and Rao 2004).

2.4.4  Human and Animal Health Uptake Antibiotics are probably the most important molecules with low molecular weight (Schofield 2018). The use of antibiotics in sub-therapeutic concentrations for agricultural functions is believed to remain a fundamental difficulty in the spread of antibiotic-resistant microorganisms (Ghosh and LaPara 2007). In addition, these are typically used, namely, feed elements, to improve animal health and growth (Call et al. 2013). Actinomycetes are known by the production of many antibiotics. These antibiotics consist of amphotericin, nystatin, chloramphenicol, gentamycin, erythromycin, vancomycin, tetracycline, novobiocin, neomycin, etc. (Sharma et  al. 2014). Antimicrobial agents have greatly contributed to the obstruction and therapy of infectious diseases in feed animals (Niewold 2007; McEwen and Fedorka-Cray 2002). It is estimated that the amount of antimicrobial agents used in feed animals exceeds the use between people worldwide. Then almost all classes of antimicrobial agents that are used by humans are also used between feed animals (Aarestrup et al. 2008). Moreover, rhizospheric soil microorganisms continue to be used, namely, efficient probiotics, since the health of human and animal is improved.

2.4.5  Industrial Application Among the active metabolites that are created by the rhizospheric microbiome, microbial surfactants and then biosurfactants are the surface-active molecules that come from a widespread variety of microorganisms. These microbial surface-active compounds are suitable for the surface and interfacial tension limitation of two immiscible liquids. Biosurfactants are a key feature of remedial methods, because of their environmentally friendly properties, such as low toxicity and excessive biodegradability (Silva et al. 2014; Gudiña et al. 2013). Biosurfactants have the strength to be developed commercially for extensive capabilities in the pharmaceutical, cosmetic, agricultural, and food industries (Sachdev and Cameotra 2013; Fakruddin 2012). Rhizospheric microorganism synthesizes a variety of enzymes such as amylases and proteases which has a range of utility among distinct industries including food, fermentation, textiles, or paper industries (Pandey et al. 2000).

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2.5  Current Advancement Biodiversity degradation has emerged as a global problem, and to this extent, evidence is accumulating that intent will negatively impact the ecosystem features on which the community depends. Thus, saving biodiversity in soil communities has private consequences because the normal overall performance in relation to an ecosystem remains unsolved (Wagg et al. 2014). It is well established that agricultural practices affect the arrangement and the diversity of soil microbial communities. However, the impact regarding altering soil microbial communities over the functioning of the agroecosystems is still poorly understood (Köhl et al. 2014). Regarding the relationship between microbial diversity and enzyme activity in the rhizosphere, research into the enzyme activity of the rhizosphere continues through fundamental methodological limitations that are capable of mimicking the complexity of the rhizosphere between sampling conditions and that correspond to the susceptibility of the rhizosphere to artifacts during rhizosphere sampling (Egamberdieva et  al. 2010). In addition, improvements in antibiotic resistance in a variety of sectors, such as health, agriculture, and the environment, have suggested that pathogens can help prevent PGPR, according to researchers (Olanrewaju and Babalola 2019). The use of antibiotics in agriculture is believed to help mimic the level of antibiotic resistance, but the mechanisms by which many agricultural practices affect resistance remain unclear (Udikovic-Kolic et al. 2014).

2.6  Conclusion and Future Prospects This review provided information on the diversity and application of rhizospheric microbiome as a promising alternative in the modern biotechnology. Since soil microorganisms are very different and some of them are only recognized and characterized, larger studies are required to better understand the interactions between plant microbes. The versatility and efficiency that has been shown in several works on the technological use of these microorganisms and their biomolecules makes them a promising source of safety and efficiency.

References Aarestrup FM, Wegener HC, Collignon P (2008) Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti-Infect Ther 6:733–750. https://doi. org/10.1586/14787210.6.5.733 Abd-Elgawad MMM, Askary TH (2015) Impact of phytonematodes on agriculture economy. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CAB International, Wallingford, pp 3–49. https://doi.org/10.1079/9781780643755.0003

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Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-­ resistant bacteria in soil following manure fertilization. Proc Nat Acad Sci 111:15202–15207. https://doi.org/10.1073/pnas.1409836111 Ungureanu C, Ferdes M, Chirvase AA, Mocanu E (2011) Method for torularhodin separation and analysis in the yeast Rhodotorula rubra aerobically cultivated in lab bioreactor. In: Icheap-10: 10th international conference on chemical and process engineering, pts 1–3. S. Pierucci 24, pp 943–48 Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, et al. (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. https:// doi.org/10.1111/1365-2745.12054 Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016) Molecular diversity and multifarious plant growth promoting attributes of bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58. https://doi.org/10.1002/jobm.201500459 Verma P, Yadav AN, Khannam KS, Saxena AK, Suman A (2017a) Potassium-solubilizing microbes: diversity, distribution, and role in plant growth promotion. In: Panpatte DG, Jhala YK, Vyas RV, Shelat HN (eds) Microorganisms for green revolution: Volume 1: Microbes for sustainable crop production. Springer Singapore, Singapore, pp  125–149. https://doi. org/10.1007/978-981-10-6241-4_7 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017b) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-­ ecological perspectives: Volume 2: Microbial interactions and agro-ecological impacts. Springer Singapore, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22 Verma P, Yadav AN, Khannam KS, Mishra S, Kumar S, Saxena AK, Suman A (2019) Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of India. Saudi J Biol Sci 26:1882–1895. https://doi.org/10.1016/j.sjbs.2016.01.042 Wagg C, Jansa J, Schmid B, van der Heijden MG (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009. https://doi. org/10.1111/j.1461-0248.2011.01666.x Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270. https://doi.org/10.1073/pnas.1320054111 Wang H, Wang SD, Jiang Y, Zhao SJ, Chen WX (2014) Diversity of rhizosphere bacteria associated with different soybean cultivars in two soil conditions. Soil Sci Plant Nutr 60:630–639. https://doi.org/10.1080/00380768.2014.942212 Wilcox HE (1991) Mycorrhizae. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 731–765 Wolfe BE (2018) Using cultivated microbial communities to dissect microbiome assembly: challenges, limitations, and the path ahead. MSystems 3:e00161–e00161. https://doi.org/10.1128/ msystems.00161-17 Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166. https://doi.org/10.1016/j.geoderma.2004.07.003 Yadav AN (2017) Agriculturally important microbiomes: biodiversity and multifarious PGP attributes for amelioration of diverse abiotic stresses in crops for sustainable agriculture. Biomed J Sci Tech Res 1:1–4 Yadav AN (2018) Biodiversity and biotechnological applications of host-specific endophytic fungi for sustainable agriculture and allied sectors. Acta Sci Microbiol 1:01–05 Yadav AN (2019) Endophytic fungi for plant growth promotion and adaptation under abiotic stress conditions. Acta Sci Agric 3:91–93 Yadav N, Yadav A (2018) Biodiversity and biotechnological applications of novel plant growth promoting methylotrophs. J Appl Biotechnol Bioeng 5:342–344

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Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan V, Dhaliwal HS, Saxena AK (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57. https://doi. org/10.7324/JABB.2017.50607 Yadav AN, Verma P, Kour D, Rana KL, Kumar V, Singh B, Chauahan VS, Sugitha T, Saxena AK, Dhaliwal HS (2017b) Plant microbiome and its beneficial multifunctional plant growth promoting attributes. Int J Environ Sci Nat Resour 3:1–8. https://doi.org/10.19080/ IJESNR.2017.03.555601 Yadav AN, Verma P, Singh B, Chauhan VS, Suman A, Saxena AK (2017c) Plant growth promoting Bacteria: biodiversity and multifunctional attributes for sustainable agriculture. Adv Biotechnol Microbiol 5:1–16 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, Cambridge, MA, pp 305–332 Yadav AN, Gulati S, Sharma D, Singh RN, Rajawat MVS, Kumar R, Dey R, Pal KK, Kaushik R, Saxena AK (2019a) Seasonal variations in culturable archaea and their plant growth promoting attributes to predict their role in establishment of vegetation in Rann of Kutch. Biologia 74:1031–1043. https://doi.org/10.2478/s11756-019-00259-2 Yadav AN, Kour D, Sharma S, Sachan SG, Singh B, Chauhan VS, et al. (2019b) Psychrotrophic microbes: biodiversity, mechanisms of adaptation, and biotechnological implications in alleviation of cold stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting Rhizobacteria for sustainable stress management: Volume 1: Rhizobacteria in abiotic stress management. Springer, Singapore, pp 219–253. https://doi.org/10.1007/978-981-13-6536-2_12 Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in White biotechnology through Fungi. Volume 2: perspective for value-added products and environments. Springer International Publishing, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019d) Recent advancement in White biotechnology through Fungi. Volume 3: perspective for sustainable environments. Springer International Publishing, Cham Yadav AN, Yadav N, Sachan SG, Saxena AK (2019e) Biodiversity of psychrotrophic microbes and their biotechnological applications. J Appl Biol Biotechnol 7:99–108 Yadav AN, Singh J, Rastegari AA, Yadav N (2020) Plant microbiome for sustainable agriculture. Springer, Cham Yamamoto K, Shiwa Y, Ishige T, Sakamoto H, Tanaka K, Uchino M, Tanaka N, Oguri S, Saitoh H, Tsushima S (2018) Bacterial diversity associated with the rhizosphere and endosphere of two halophytes: Glaux maritima and Salicornia europaea. Front Microbiol 9:2878. https://doi. org/10.3389/fmicb.2018.02878 Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact 25:139–150. https://doi.org/10.1094/mpmi-06-11-0179 Zhang T, Wang Z, Lv X, Li Y, Zhuang L (2019) High-throughput sequencing reveals the diversity and community structure of rhizosphere fungi of Ferula sinkiangensis at different soil depths. Sci Rep 9:6558. https://doi.org/10.1038/s41598-019-43110-z Zwart KB, Kuikman PJ, Van Veen JA (1994) Rhizosphere protozoa: their significance in nutrient dynamics. In: Darbyshire JF (ed) Soil protozoa. CAB International, Wallingford, pp 93–122

Chapter 3

Endophytic Microbiomes: Biodiversity, Current Status, and Potential Agricultural Applications Mozhgan Ghiasian

Abstract  Endophytes are considered as endosymbiotic microorganisms which are widely found in plants through which the intercellular and intracellular spaces of all parts of a plant are colonized. Plant disease or morphological changes which are of importance are not caused by such plants. Function and soil structure as well as endophytic microbial populations are noticeably influenced by agricultural practices including soil tillage, irrigation, use of pesticides, and fertilizers. Accordingly, the application of such practices via which the natural variety of plant endophytes is maintained has played a significant role in sustainable agriculture that could lead to plant productivity and increase in quality of agricultural production. A variety of endophytic microbial communities contribute greatly to the agro-ecosystems function. It has been denoted that endophyte affect their host plant in terms of growth-­ promoting activity, modulation of plant metabolism, and phytohormone signaling which causes them to adapt to environmental abiotic or biotic stress. Keywords  Abiotic stresses · Agriculture · Biotic stresses · Endophytes · Microbiomes · Phytohormones

3.1  Introduction Plant microbiomes (microbial community that typically interacts extensively with a plant) can be classified as rhizospheric microbes (living in soil near the roots), epiphytic microbes (living on the surface of plants), and endophytic microbes (living within a plant). In general, there are three kinds of plant–microbes interactions, that is, endophytic, rhizospheric, and epiphytic (Yadav et  al. 2017a, 2020). The term “endophyte” is derived from “endon” meaning within and “phyton” meaning plant.

M. Ghiasian (*) Department of Microbiology, Falavarjan Branch, Islamic Azad University, Isfahan, Iran e-mail: [email protected] © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_3

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Endophytes are bacteria, archaea, fungi, and protists that spend their entire life or part of their life cycle inside plants (inter- or intra-cellular spaces), videlicet, root, stem, or seed, without damaging plant tissues or inducing defense responses. Plant microbiomes can have profound impacts on plant growth and health (Kandel et al. 2017). Rhizosphere is the narrow zone surrounding and influenced by plant roots. Root exudates are essential in determining rhizosphere microbiome structure. The composition of root exudates is not the same for all plants and it can change from one plant species to another or from one cultivar to another; moreover, age and developmental stage of plants can contribute to this variation (Mendes et  al. 2013). Moreover, soil type, soil moisture, pH, and temperature are known to have effects on the types of rhizospheric microbes. Attaching the rhizosphere microorganisms to the root surfaces result in the use of root exudates. Microbial communities of different crop plants rhizosphere are typically dominated by Acinetobacter, Alcaligenes, Arthrobacter, Aspergillus, Azospirillum, Bacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Haloarcula, Halobacterium, Halococcus, Haloferax, Methylobacterium, Paenibacillus, Penicillium, Piriformospora, Pseudomonas, Rhizobium, and Serratia (Rana et  al. 2019c; Yadav 2018; Yadav et  al. 2017b, c). Endophytes are for the most part distinguished from epiphytes that are found on the external surfaces of the plants. Upon internal tissues exposure, endophytes may change to epiphytes and help keep the exposed tissues safe from the environment (Porras-Alfaro and Bayman 2011).

3.2  Origin and Emerging Concepts of Endophytes The main source of endophytes is the microorganisms associated with the rhizosphere, phyllosphere, and seeds (Maheshwari et al. 2017; Singh and Dubey 2018). Endophytic bacterial variety can be propounded a subset of the rhizosphere and/or root-associated bacterial population (Suman et al. 2016; Verma et al. 2017; Yadav et al. 2018a). It has been discovered that bacterial endophytes are found in the inner parts of endorhiza of stems, leaves, and flowers of quite a few plant species (Reinhold-Hurek and Hurek 2011). Based on their life strategies, bacterial endophytes can be classified into obligate endophytes that can only live inside plant tissues, facultative endophytes that can live both inside the plants and in the rest of habitats, and opportunistic endophytes which are able to sporadically enter plants and live inside their tissues (Gamalero and Glick 2015). Obligate endophytes are strictly dependent on the host plant for their growth and durability and transition to other plants. Facultative endophytes have a phase in their life cycle in which they live outside host plants. Facultative endophytes life is biphasic, alternating between plants and the environment (principally soil) (Hardoim et al. 2008). Microbes attain the rhizosphere by chemotaxis to root exudates components, then they attach to the root (Kour et al. 2019c; Rana et al. 2019a; Rana et al. 2019b). The exopolysaccharides (EPS) synthesized by bacterial cells and bacterial lipopolysaccharide (LPS) have been shown to play roles for attachment and subsequent

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endophytic colonization of plant roots (Meneses et al. 2011; Kandel et al. 2017). Flagella, fimbriae, or cell surface polysaccharides of bacteria are also presumably involved in the attachment of bacteria to the plant surface (Kandel et  al. 2017). Bacterial endophytes at first attach to the root surface, and then explore the potential entry sites to access the internal plant tissues. Endophytic microbes enter via wounds caused by microbial or nematode phytopathogens and the stomata found in leaf tissue or the natural wounds resulting from plant growth at absorbent hair and epidermal conjunctions. Sometimes enzymes such as cellulase and pectinase dissolve cell walls and make bacterial entry possible (Hardoim et  al. 2008; Singh and Dubey 2018) (Fig. 3.1). Endophytes transfer happen either vertically (via seeds from one generation to another) or horizontally (allied species through plant part decay/soil) (Singh and Dubey 2018; Yadav 2019b) (Fig. 3.2). The plant endophytic microbiome can be modified by factors such as plant growth stage, the plant tissue analyzed, the physicochemical structure of the soil and its condition (including pH and moisture content), plant physiological state, the nutritional state of the plant, and environmental factors (such as temperature) (Santoyo et  al. 2016; Yadav and Yadav 2018). There are complex interactions between the plant and its microbiome structure. Specifically, the plant immune

Fig. 3.1  Types of endophytes and their root colonization process. Red cells = passenger endophytes (they are often restricted to the root cortex tissue) Blue cells = Opportunistic endophytes (colonize the rhizoplane and then invade the internal plant tissues) Yellow cells = Competent endophytes (they are proposed to have all properties of opportunistic endophytes, and, in addition, be well adapted to the plant environment). (Hardoim et al. 2008)

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Fig. 3.2  Infection of host plant and transmission of endophytes from generation to generation (vertical) through infection of reproductive parts, seeds, and allied plants (horizontal) through movement in soil. Endophytes enter through cuts, wounds, and natural openings like stomata. (Arora and Ramawat 2017)

system plays a key role in determining the microbiome structure of the plant (Turner et al. 2013).

3.3  E  ffects of Agricultural Practices on Endophytic Microbial Communities Bacteria form the largest number of microorganisms in soil, and many endophytic bacteria are derived from rhizosphere microorganisms. The soil microbial population determines the microbial diversity of the rhizosphere. Microorganisms are

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absorbed by the root exudates to the plant (Tamosiune et al. 2017). Agricultural land management procedures including tillage or irritation can have an impact on physical, chemical, and biological characteristics of the soil (Miliute et  al. 2015). The microbial population of the soil is affected by the excessive use of pesticides. Pesticides may have inhibitory effects on microbial growth and metabolism; furthermore, if the structure of agricultural ecosystems changes, it may result in changes in the microbial diversity. The quantity and quality of plant residues which enter the soil may change due to changes in agricultural management procedures (Kumar et al. 2019; Verma et al. 2015, 2016; Yadav et al. 2019). Changes in nutrients and their inputs alter the spatial distribution of plants. Also, the composition of microbial community and microbial biomass is affected by mineral or organic fertilizers. The use of organic manure leads to increased microbial diversity and metabolic activity. However, the use of manures makes the fecal bacteria enter the soil and is capable of changing the combination of the endogenous microbial population and posing environment-related dangers (Miliute et al. 2015; Yadav 2018; Yadav et al. 2018c). Several studies have shown that the composition of the rhizosphere bacteria is not the only factor determining the endophytic spectrum (Kour et al. 2019c; Yadav et al. 2018b). Differences in plant biochemistry due to the organic amendment, such as enhanced chitinase and peroxidase concentrations, might have changed the bacterial endophytes (Schulz and Boyle 2006). The life style of most bacteria in the plant’s endosphere is facultative endophyte (Miliute et al. 2015). Endophytes at first infect the host plant’s roots which in turn colonizes the plant apoplast. Therefore, the microbial population of the rhizosphere is represented by the endophytic community as one of its subcategories which differentiates the agronomic practices characterizing the microbial community of the soil (Miliute et al. 2015). Acetobacter diazotrophicus is nitrogen-fixing endophytic bacterium. Studies have denoted that in the sugarcane plants which experienced fertilization through high levels of nitrogen, Acetobacter diazotrophicus’s ability to colonize was alleviated to a great extent (Tamosiune et al. 2017). Sasaki et al. (2013) showed that the level of nitrogen fertilization influenced the structure of rice root endophytic population. Considering observations, agricultural plants can be regarded as a source plentiful of human pathogens and also an opening for the removal of illnesses caused by food (Brandl 2006). Pathogenic bacteria Enterobacteriaceae containing pathogenic Salmonella genus strains and Vibrio choleras trains as well as the human opportunistic pathogen Pseudomonas aeruginosa were found on plants or inside plants (Akhtyamova 2013). Colonizing plants through human pathogens may be in relation to using manures which have been contaminated by fecal bacteria. Manure is commonly applied to fields in order to dispose of animal waste and to fertilize soils (Brandl 2006). Meanwhile, the use of practices that lead to a decrease in the antagonistic ability of species to the pathogenic bacteria available in soil and endosphere was connected to plant colonization which takes place through human pathogen species (Latz et al. 2012). Biological suppression of soil-borne diseases is the cause of soil microbial activity and composition. Competition for space and nutrients is the reason of their mechanism. This mechanism is indeed an antagonism is the result of producing secondary metabolites and eliciting induced systemic resistance (Philippot et  al.

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2013; Pieterse et al. 2014). It was revealed that the genera Streptomyces, Bacillus, Pseudomonas which end in endophytic lifestyle were responsible for the disease suppressive properties of soil (Yadav 2019a; Kinkel et al. 2012).

3.4  Biodiversity of Endophytes Endophytes are categorized into two general groups based on their taxonomy, functional diversity, biology, and mode of transmission: systemic/true endophytes and non-systemic/ transient endophytes (Wani et al. 2015). Certain endophytes are sensitive to hosts. The quantity of specific species that a host can have is assumed to be constant and the number of plant species can help in extrapolation of the total number of endophytic species. Concerning the greater variation of plants in tropical regions, endophytic diversity may be higher in tropical areas. According to a meta-­ analysis conducted lately, tropics, compared to temperate regions, are more abundant in leaf endophytes which are rich in a variety of species (Porras-Alfaro and Bayman 2011). Proteobacteria, including the Classes alpha-, beta-, and gammaProteobacteria, are reported to be major in diversity analysis of endophytes, although members of the Firmicutes and Actinobacteria are also among the classes most consistently found as endophytes. Other classes such as Bacteroidetes, Planctomycetes, Verrucomicrobia, and Acidobacteria are less generally found as endophytes (Santoyo et al. 2016). A great number of endophytic microbial genera are Pseudomonas, Bacillus, Burkholderia, Stenotrophomonas, Micrococcus, Pantoea, Microbacterium, Achromobacter, Azoarcus, Collimonas, Curtobacterium, Enterobacter, Flavobacterium, Gluconoacetobacter, Herbaspirillum, Klebsiella, Microbiospora, Micromomospora, Nocardioides, Planomonospora, Serratia, Streptomyces, and Thermomonospora (Rana et  al. 2019a, b; Saxena et  al. 2016; Verma et  al. 2019; Yadav 2017). Although a large diversity of microorganisms can live endophytically, principally bacteria, specifically Alphaproteobacteria, were identified as plant inhabitants (Kour et al. 2019a, b, c). In contrast, there is little information about endophytic Archaea. Archaea constitute a domain of single-celled microorganisms. Recently, few studies have been done on endophytic archaea, but their distribution, significance, function, and activity remain unclear (Müller et al. 2015). In quite a few of the plants, a variety of classes such as Dothideomycetes, Sordariomycetes, Leotiomycetes, Eurotiomycetes, and Pezizomycetes defeat fungal endophyte communities (Porras-Alfaro and Bayman 2011). The most prevalent endophytic microbial isolates detected were summarized and their hosts are demonstrated in (Table 3.1). Since the endophytic microbes and plant association contain a wide variety of endophytic microbes and plant hosts, this list is not complete.

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Table 3.1  Endophytes from different host plants Plant species Bacterial endophytes Carrot (Daucus carota L. var. sativus)

Endophyte

References Surette et al. (2003)

Pogonatherumpaniceum

Rhizobium (agrobacterium) radiobater, Klebsiellaterrigena, Pseudomonas putida, P. fluorescens, P. chlororaphis, Bacillus megaterium Bacillus pumilus, B. subtilis, Pseudomonas aeruginosa, P. fluorescens Bacillus megaterium, Brevibacilluschosinensis, and Microbacterium richothecenolyticum Pseudomonas spp., Serratia,Bacillus spp., Arthrobacter spp., Micrococcus spp., Curtobacterium sp. Microbacterium spp.

Raphanussativus L.

Proteobacteria sp.

Avicennia marina

Bacillus sp., Enterobacter sp., and Sporosarcina aquimarina

Tomato

Brevibacillus brevis

Tomato (Lycopersiconesculentum) Oryza sativa

Pseudomonas aeruginosa

Maize (Zea mays L.) Medicagosatavia L. Piper nigrum L.

Coffeaarabica Musa spp. Oleaeuropaea L. Dendrobiumandidum Fungal endophytes Taxuschinensis Pinushalepensis

Soybean

Pseudomonas spp., Bacillus spp., Enterobacter spp. and Micrococcus spp. Bacillus firmus, Bacillus cereus, Paenibacillus sp. B. amyloliquefaciens, B. subtilis, and B. thuringiensis Pelomonas sp., Ralstonia sp., Pseudomonas sp., Actinobacter sp. Pseudomonas saponiphila

Diaporthe, Phomopsis (anamorph of Diaporthe), Acremonium, and Pezicula Naemacyclus minor, Brunchorstiapinea, Lophodermiumpinastri, Phomopsis sp., Diplodiapinea, Pestalotiopsisbesseyi, Truncatella angustata Cladosporium, Alternaria, Diaporthe, Epicoccum

Solanumnigrum

Fusarium tricinctum, Alternaria alternate

Phaseolus vulgaris

Fusarium oxysporum, Xylaria sp., and Cladosporium cladosporioides

Rai et al. (2007) Stajković et al. (2009) Aravind et al. (2009) Koskimäki et al. (2010) Seo et al. (2010) Sona Janarthine et al. (2011) Yang et al. (2011) Patel et al. (2012) Mbai et al. (2013) Oliveira et al. (2013) Souza et al. (2014) Müller et al. (2015) Wu et al. (2016) Liu et al. (2009) Botella and Diez (2011)

Impullitti and Malvick (2013) Khan et al. (2015) Parsa et al. (2016) (continued)

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Table 3.1 (continued) Plant species Archaealendophytes Coffeaarabica Oleaeuropaea L. Other endophytes Alternantherasessilis

Endophyte

References

Methanobacteriales,Thermoplasmatales, Crenarchaeota Nitrososphaera, Halobacteriales, Methanomicrobiales, Crenarchaeota

Oliveira et al. (2013) Müller et al. (2015)

Oscillatoria, Obscura, and Nostoc. Punctiforme

Keshri and Chatterjee (2010)

3.5  Methods for Detecting Endophytes Within the Plant Despite studies conducted over centuries microorganisms are still unknown, and it is due to the fact that just a part (0.001) of it has the potential for culture, thereby making us encounter a little-known world. To begin with, through the application of polymerase chain reaction (PCR)-based techniques, and later on through the use of 16S ribosomal RNA (rRNA) sequences, researchers could look into the little-­ recognized diversity of microbes and these altogether made some information available on uncultured microbes (Sharma et  al. 2015).There are two methods for identifying endophytes in a plant: culture-dependent and culture-independent methods. Each method has advantages and disadvantages (Collinge et al. 2019).

3.5.1  Culture-Dependent Methods Culture-dependent techniques seem to be truly effective to provide information on some sets of microorganisms which have been cultured, for the most part information on certain behaviors and traits of endophytic microbiome under culture (Turner et  al. 2013; Sharma et  al. 2015). The plant tissue surface should be sterilized to make sure that organisms isolated are endophytic and not epiphytic. This is particularly important for roots and tubers. Often, alcohol and sodium hypochlorite treatment are used for this. Gentle treatment allows too many epiphytic or rhizospheric organisms to survive, and harsh treatment penetrates the tissue and kills its microorganisms. Since the harsh treatments can reduce fungal survival inside the tissue, the conditions must be standardized before working with a new species or tissue (Collinge et al. 2019). A variety of nutrient media and growth conditions, considering the target organisms, can be applied to isolate microbes from their environment. Microorganisms need specific conditions to grow, which they get readily in their natural environment (Turner et al. 2013).

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A number of endophytes are not cultivated; hence, they cannot be used in crop production. To increase the chances of isolating, and thus cultivating and utilizing endophytes, the media can be completed with plant extracts, which has been shown to increase the number of endophytes recovered (Collinge et al. 2019). In spite of the fact that an organism’s pure culture is essential to be achieved to investigate its genetics and physiology in detail, culture-dependent techniques are deprived of retaining the greater part of microbial variation present in an environment (Turner et al. 2013). Disadvantages of using cultivation methods include the following: • Determining the number of microbes encounters a problem, because microbes can only be cultivated if their metabolic and physiological requirements can be reproduced in vitro. • An artificial homogeneous medium often results in the growth of a small fraction of microorganisms; as a result, community analysis is difficult. • When mixed microbial communities are under investigation, counting bacteria by culture-dependent method may produce incorrect results. • Some microorganisms require symbiotic partners, and in case such partners are not available, their growth will be hindered (Carraro et al. 2011). • In certain cases, access to some nutrient requirements or surfaces essential for growth might be limited. The tissue from which endophytes are isolated should be fresh, and symptoms of disease are not observed or are few in number (Santoyo et al. 2016). • Non-competitiveness happens during culture by virtue of factors including slow growth rates and negative feedback from some metabolites during culture or quick distribution from colonies (Simu and Hagström 2004).

3.5.2  Culture-Independent Methods It has been recognized that different sets of microorganisms are available which do exist and affect the life of plants, although they cannot be cultured (Sharma et al. 2015). The inability of certain microorganisms to be cultured can also be caused by inhibitory compounds as well as an amalgamation of such factors as temperature, pressure, or atmospheric gas (Simu and Hagström 2004). The use of certain new techniques is required in such conditions: Brock submerged the glass slides in the pools for a week to 10 days and observed them under a microscope. He also used fluorescent antibodies against the known cultured bacteria, which he thought might suppress the uncultured bacteria. Such technique was effective in a way that the size of population and rate of growth of all members of the community could be roughly calculated (Bohlool and Brock 1974; Brock 1985). As prokaryotes from environmental samples are often hardy to isolation by culture-­ dependent methods, culture-independent molecular methods have been greatly used to determine microbial communities in situ (Reinhold-Hurek and

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Hurek 2011). Many culture-independent molecular methods are based on ribosomal RNA (rRNA) gene analysis. For studying prokaryotes, 16S rRNA gene is generally used. The sequencing of different regions of this gene results in accurate taxonomic identification (species- and strain-level). To study eukaryotic microorganisms like fungi, adequate taxonomic differentiation could not be prepared by 18S rRNA gene; therefore, the hyper variable internal transcribed spacer is mostly applied (Turner et al. 2013). Quite a few molecular techniques are independent of culture and rest on16S ribosomal RNA (16S rRNA) gene analysis including PCR amplification of 16S rDNAs, ITS region, amplified ribosomal DNA restriction analysis (ARDRA), denaturing gradient gel electrophoresis (DGGE), and terminal restriction fragment length polymorphism (T-RFLP) bacterial-automated ribosomal intergenic spacer analysis (ARISA). Pyrosequencing and metagenome analyses have been used in microbial ecology (Sun et  al. 2008; Manter et  al. 2010; Sessitsch et  al. 2012; Impullitti and Malvick 2013). Modern high-throughput techniques, which are often performed for uncultured microbes, has made it possible to analyze community variation. The combination of all high-throughput studies with microbiota is studied in metagenomics (Sharma et  al. 2015). In 2004, 454 Life Sciences launched the first commercial next-­ generation sequencing (NGS) platform based on pyrosequencing (Cuadros-Orellana et al. 2013). NGS enables rapid analysis of the composition and diversity of microbiota in plant tissues, and this can improve the understanding of the microbial plant– host interactions (Akinsanya et al. 2015). Identification of a group of microorganisms or any particular species from a population sometimes becomes very important. Fluorescence in situ hybridization (FISH) is a powerful technique for the group or species to be identified and quantified from the rest of the members in a population (Wagner and Haider 2012). This is known as a culture-independent technique for which certain prior information about particular genomic sequences of organisms is required. FISH needs small subunit (SSU) ribosomal RNA (rRNA) oligonucleotide probes; in this method, both SSU rRNA probe hybridization is merged with fluorescent microscopy (Vági et al. 2014). The culture-independent methods allow detection and identification of bacteria, archaea, and fungi including those that are cryptic, sterile, and unculturable, while culture-independent methods can potentially detect a more diverse endophyte population than culture-dependent methods (Manter et al. 2010; Impullitti and Malvick 2013; Ma et al. 2015).

3.6  Endophytes in Agriculture Concerning economy, the most important activity of millions of people especially in developing countries is agriculture. Endophytes are important in virtue of their role in plant growth stimulation, protection against biotic and abiotic stresses and

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Fig. 3.3  Use of associative bacteria to have sustainable agriculture, and thus production of substances required for plant growth and also elimination of the growth of pathogens and competitive plants. (Arora and Ramawat 2017)

pests through modulation of growth hormone signaling, higher seed yield, and plant growth hormones (Miliute et  al. 2015). Based on genome sequences of 304 Proteobacteria, the dispersion of 23 genes that could enable these bacteria to further plant growth was analyzed (Bruto et  al. 2014). Therefore, this bears significant impacts on agricultural properties of crop plants that are promising for eco-friendly and economically sustainable agriculture (Arora and Ramawat 2017) (Fig. 3.3).

3.7  Role of Endophytes in Promoting Plant Growth Plant growth is facilitated by plant growth–promoting bacterial endophytes (PGPBEs) through phytostimulation, biofertilization, and biocontrol.

3.7.1  Phytostimulation Plant growth is promoted by phytostimulators and through production of phytohormones (Bloemberg and Lugtenberg 2001; Gaiero et al. 2013). For example, the reduction of plant hormoneethylene levels by 1-aminocyclopropane-­1-carboxylate(ACC)

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deaminase is a sample of phytostimulation. It has been denoted that endophytes like Arthrobacter spp., Bacillus spp. in pepper plants (Capsicum annuum) and Pseudomonas putida, Rhodococcus spp. in peas (Pisum sativum) that release ACC deaminase promote plant growth (Belimov et al. 2001; Sziderics et al. 2007). Abiotic stress such as salinity stress can be alleviated by producing ACC deaminase as an immediate precursor through balancing the ethylene-level production of plants. This happens since increased ethylene levels hinder cell division, DNA synthesis, and root/ shoot growth (Sarkar et al. 2018). Plant growth can also be stimulated by producing the other plant hormones including indole-3-acetic acid (IAA), jasmonates, and abscisic acid (ABA) by bacterial strains (Leveau and Lindow 2005; Forchetti et al. 2007; Cohen et al. 2009).

3.7.2  Biofertilization Nitrogen fixation, which is the conversion of atmospheric nitrogen to ammonia, is a form of biofertilization. Endophytic N2–fixing bacteria are important in promoting plant growth. Endophytic bacteria with the best characteristics include Azoarcus spp., Gluconacetobacter diazotrophicus, and Herbaspirillum seropedicae (Siddiqui 2006). Through phosphorus solubilization, phosphorus access to the plant can be enhanced by some plant growth–promoting bacterial endophytes. Indeed, when low molecular weight acid is released, it makes possible the chelation of the metal cation attached to phosphorus, thereby making it accessible to the plant (Gaiero et al. 2013).

3.7.3  Biocontrol Biocontrol is defined as protecting phytopathogens which leads to increase in plant growth. In this process, mechanisms such as producing siderophores or antibiotics can probably have contribution. Siderophores are organic compounds with low molecular masses that are produced by microorganisms and plants growing under low iron conditions. More than 500 various kinds of siderophores are available, which are the products of microorganisms (Ahmed and Holmström 2014). Iron access to microorganisms and plants can be immediately ameliorated by siderophores which are the outcomes of microorganisms through direct chelation from soil. Furthermore, access to iron can be enhanced considering the microorganisms’ competition for iron with other microorganisms and pathogens. As an example, pyochelin and salicylic acid (that are siderophores) chelate iron, and by competing with phytopathogens for trace metals, it can indirectly help control the disease (Chhabra and Dowling 2017; Kumar et al. 2019). Antimicrobial metabolites produced by PGPBEs include 2,4 Diacetylphloroglucinol, phenazine-1-carboxyclic acid, phenazine-1-carboxamide,

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pyoluteorin, pyrrolnitrin, oomycinA, viscosinamide, butyrolactones, kanosamine, zwittermycin-A, aerugine, rhamnolipids, cepaciamide A, ecomycins, pseudomonic acid, azomycin, antitumor antibiotics FR901463, cepafungins, and antiviral antibiotic karalicin. These antibiotics are known to have antiviral, antimicrobial, insect and mammalian antifeedant, antihelminthic, phytotoxic, antioxidant, cytotoxic, antitumor, and plant growth-promoting activities (Siddiqui 2006). In the case of banana, it is worth noting that it can be protected against fungal (Fusarium oxysporum f. spcubense and Colletotrichum guaranicola) pathogens through endophytic bacteria (Bacillus amyloliquefaciens, B. subtilis subsp. Subtilis, and B. thuringiensis) (Souza et al. 2014). It has been revealed that endophytic fungi isolated from a variety of plants have antifungal activity. Piriformospora indica (Waller et al. 2005), Acremonium strictum (Hol et al. 2007), and some Stagonospora species (Ernst et al. 2003) protect host and growth promotion.

3.8  R  ole of Endophytes in Adapting Agricultural Crops to Biotic and Abiotic Stress Stresses of different types and levels are exposed to plants respectively, all of which are capable of plant growth and development hindrance. Biotic factors including viruses, nematodes, insects, bacteria, or fungi or by abiotic factors including extremes of temperature, high light, flooding, drought, the presence of toxic metals, and organic contaminants may be responsible for these stresses. Stimulating growth and protecting a variety of crops against pathogens and abiotic stressors through endophytes is well researched under both controlled conditions (Gamalero and Glick 2015).

3.8.1  I nduction of Accumulation of Stress-Related Metabolites and Enzymes Plants are able to overcome stress factors by changing physiology and adaption to environmental stresses. Stress factors include dehydration, mechanical injury, nutrient deficiency, high solar radiation, or stress-induced increase in concentration of reactive oxygen species. This adaption is connected to increase in the compounds production through which osmotic adjustment is mediated, cell components are stabilized, and which play the role of free radical scavengers. Inoculating plants through endophytic bacteria results in the reposition of compounds such as proline, phenolic compounds, carbohydrates, and antioxidants (Tamosiune et  al. 2017). Fernandez et al. (2012) showed that Burkholderia phytofirmans PsJN, which is an endophytic bacterium, increases cold tolerance of grapevine plants through

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changing photosynthetic activity and carbohydrates metabolism entailed in cold stress tolerance. The bacterium available in the plant encouraged adaption to cooling temperatures which in turn leads to less cell damage, more photosynthetic activity, and reposition of cold stress-related metabolites such as starch, proline, and phenolic compounds (Barka et  al. 2006). It was demonstrated that the bacterium had the same positive impact on metabolic balance, and dryness stress had alleviated impact in wheat plants grown under decreased irrigation conditions. Inoculating with the bacterium enhanced plants’ antioxidant activity in comparison to control which experienced dryness stress (Naveed et al. 2014). Protecting against dryness stress was in relation with augmentation in total soluble sugars, glucose, fructose, and starch contents. It was depicted that a twofold increment in soluble sugar content was the consequence of bacterizing grapevine plants. Inoculating the grapevine plantlets with bacterium resulted in higher concentrations of the sugars recognized to contribute to low-temperature tolerance, such as glucose, sucrose, and raffinose with its precursor, and galactinol (Fernandez et  al. 2012). Studies revealed that Pseudomonas pseudoalcaligenes, which is an endophytic bacterium, encouraged reposition of higher concentrations of glycine betain-like compounds, thereby ameliorating salinity stress tolerance in rice (Jha et al. 2011). The effect of Pseudomonas aeruginosa PW09, which is wheat endophytic bacterium, is reduced due to the cross-species stress in cucumber. Pseudomonas aeruginosa PW09 leads to an increase in proline and accumulation of phenolics under NaCl stress and pathogen Sclerotiumrolfsii inoculation. Additionally, biosynthesis of phenolic compounds, polyphenol oxidase, and phenylalanine ammonia lyase was involved in the increment of the enzymes activities; further, the antioxidative enzyme superoxide dismutase (SOD) was noticed under both biotic and abiotic stress conditions (Pandey et al. 2012). In the same vein, Damodaran et al. (2014) differentiated the impact of six bacterial strains on gladiolus plants’ stress-related biochemical traits (Damodaran et al. 2014). Arthrobacter sp. and Bacillus sp. have a stimulating effect on proline accumulation in pepper (Capsicum annuum L.) plants in culture condition. Osmotic stress has the same contribution to augmentation of the quantity of proline which is free in the leaves of plants which have been and not have been inoculated. Nonetheless, in comparison to unstressed plants which have not been inoculated, concentration of proline was higher in leaves of unstressed plants inoculated through one of the two strains. The bacterization led to dramatic reduction of upregulation or downregulation of the stress-inducible genes, recommending that Arthrobacter sp. and Bacillus sp. caused decrease in abiotic stress in pepper under osmotic stress conditions (Sziderics et  al. 2007). It was indicated that endophytic bacteria Sphingomonas SaMR12 affected the contents of root exudates, which were of significance to chelating cadmium ions, and led to reduction of the toxic metal stress in Sedum alfredii. Inoculating the endophytic bacterium through a technique relied upon cadmium treatment levels crucially influenced the secretion of oxalic acid, malic acid, and tartaric acid (Chen et al. 2014).

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3.8.2  Effects on Phytohormone Balance Ethylene (ET) contributes to plant growth regulator that functions in the processes of root initiation, fruit ripening, seed germination, flower wilting, leaf abscission, biosynthesis of other phytohormones, and as mediator of plant stress response signaling. Plants usually synthesize only small amounts of ethylene: levels that typically yield beneficial effects on plant growth and development (except during fruit ripening when the ethylene concentration is much higher). However, in response to various stresses, there is often a significant rise in endogenous ethylene biosynthesis, called “stress ethylene” (Abeles et al. 2012). These stresses may include chilling, heat, wounding, pathogen infection, flooding, salinity, heavy metals, and nutritional stress (Stearns and Glick 2003). In all vascular plants, ethylene is formed from S-adenosyl-methionine through the enzyme 1-aminocyclopropane-1-carboxylate [ACC] synthase activity, not only over normal plant development but also in a condition where the plant is subjected to a variety of environmental stresses (Gamalero and Glick 2015). When ethylene levels are balanced, one of the leading bacterial physiological activities is displayed by ACC deaminase, which is supportive for plant growth under stressed conditions. Such conditions are those where the ethylene level inside the plant may otherwise reach levels which hinder plant growth. Endophytes can presumably generate the enzyme ACC deaminase that does not play any function in bacteria but is of importance in plant growth propagation and ameliorates stress tolerance by splitting the ET precursor ACC (Glick 2014). Qin et  al. (2014) isolated 13 ACC deaminase-­ producing putative endophytic bacteria from the halophyte plant Limonium sinense. The endophytic bacteria were Bacillus, Pseudomonas, Klebsiella, Serratia, Arthrobacter, Streptomyces, Isoptericola, and Microbacterium. It was recommended that ACC deaminase-producing habitat-adapted symbiotic bacteria isolated from halophyte had the potential to augment plant growth under saline stress conditions. Salinity is regarded as one chief factor which limits plant growth and crop productivity. In Qin et al.’s (2014) study, it was depicted that four of the chosen ACC deaminase-producing strains could stimulate the host plants growth. In another study, it was indicated that the concentration of sodium in tomato plant shoots was restricted by wild-type bacterial endophytes (P. fluorescens YsS6 and P. migulae 8R6) (Ali et al. 2014). Another phytohormone is abscisic acid (ABA), which contributes to plant stress responses and plays a key role in adjusting the plant water balance and tolerate osmotic stress (Tuteja 2007; Yang et al. 2009). It was revealed that accumulating ABA generated by endophytic Azospirillum spp. causes water stress tolerance in maize plants to be decreased and its impact was later increased through hormones which encourage plant growth such as indole acetic acid (IAA) and gibberellins (Leveau and Lindow 2005; Cohen et  al. 2009). Indole acetic acid production is prevalent in plant-associated bacteria, especially in the rhizobia, and certain Bacillus spp. have the potential to generate gibberellins (Gutiérrez-Mañero et  al. 2001; Ghosh et al. 2011).

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3.8.3  Induced Systemic Resistance Induced systemic resistance (ISR) and systemic acquired resistance (SAR) are two major players in induced plant resistance. One of the major differences between these systems occurs in the inducers. Pathogens stimulate systemic acquired resistance, and this leads to further protection against infections resulting from a wide variety of attackers. ISR is activated by nonpathogenic plant-associated microorganisms. ISR is a phenomenon in which resistance to infectious diseases and herbivorous insects is systematically caused by localized infection or treatment with microbial components, products, or a variety of structurally unrelated organic compounds and inorganic compounds. Signaling pathways which have interconnections and their regulation is done through signal molecules/hormones regulate induced systemic resistance and systemic acquired resistance. ISR of plants against pathogens is an extensive phenomenon that has been extremely investigated with respect to the underlying signaling ways and also to its potential use in plant protection. Jasmonic acid (JA) and ethylene, which are plant hormones, have much contribution to the regulation of the group of inter-related signaling pathways required in ISR induction, while SAR is controlled by salicylic acid (SA) (Pieterse et  al. 2014). Non-pathogenic microbes can raise the level of disease resistance in plants. Suppressing pathogenic soil organisms and inducing host systemic resistance help effective organisms including plant growth–promoting rhizobacteria (PGPR) and plant growth–promoting fungi (PGPF) control plant diseases. PGPR-mediated ISR has been demonstrated in many plant species and has a broad spectrum of effectiveness (Nadarajah 2017). It was demonstrated that Acinetobacter, Azospirilium, Rhizobium, Pseudomonas, and Bacillus are beneficial inducers of systemic resistance in two types of plants: leguminous and non-­ leguminous. Moreover, Trichoderma spp., Penicillium simplicissimum, Piriformospora indica, Phoma sp. nonpathogenic Fusarium oxysporum, and arbuscular mycorrhizal fungi are considered as PGPF which could have achieved success in the suppression of diseases in quite a few plant systems (Bakker et al. 2013).

3.9  Conclusion and Future Prospects Endophytes have great contributions in the physiology of plants and agricultural system performance. These microbes can increase nutrient availability for plants through nitrogen fixation, phosphate solubilization, and siderophore production. The use of endophytes presents a special interest for development of agricultural applications that ensure improved crop performance under cold, draught, or contaminated soil stress conditions or enhanced disease resistance. Many endophyte strains are capable of producing hormones or modulating the host phytohormones, improving both plant growth and stress tolerance. Biotechnology has created new opportunities for the use of these microbes in soil for the promotion of plant growth and the biological control of soil-borne pathogens. As far as nutrition and environment are concerned, the microbes’ needs are truly various. The use of molecular

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biology tools and techniques provides information into their diversity and structure of the genome. Biosynthesis of the drug is controlled by several genes; therefore, producing useful drugs is still a challenge. In case helpful genes are detected in the endophyte genome, such detection can be beneficial in explaining the route and thus biosynthesis of the respective secondary metabolites in required amounts.

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Chapter 4

Culturable Plant-Associated Endophytic Microbial Communities from Leguminous and Nonleguminous Crops Rajesh Ramdas Waghunde, Mrugesh Dhirajlal Khunt, Rahul Mahadev Shelake, and Vijay Adhar Patil

Abstract  Almost 20–40% of global agricultural productivity loss has been recorded due to pathogen, weeds, and animals. Endophytes are symptomless microbes residing in the plant without harming it. Endophytes are the best alternative for agrochemicals utilized for plant health management. The complexity of the plant-endophyte interaction, such as saprophytic, facultative, reciprocal, and pathogenic, is a mystery to scientists and must be understood together with their communication system with the host. The modern molecular applications and advanced tools can be used for interaction study. The mode of action for pest management varies as per host, season, and ecology of plants; it has a profound effect on endophytic microbial activity. The tripartite interaction study of endophytes should be initiated by interdisciplinary approaches in an appropriate combination of input required to understand the endophyte mechanisms. Keywords  Biotechnological applications · Endophytes · Legumes · Nonlegumes · PGP attributes

R. R. Waghunde (*) Department of Plant Pathology, College of Agriculture, Navsari Agricultural University, Bharuch, Gujarat, India M. D. Khunt Department of Plant Pathology, N. M. College of Agriculture, Navsari Agricultural University, Navsari, Gujarat, India R. M. Shelake Division of Applied Life Science (BK21 Plus program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, Korea V. A. Patil National Agricultural Research Project, SWMRU, Navsari Agricultural University, Navsari, Gujarat, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_4

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4.1  Introduction The increasing human population requires optimum food with proper nutrition for better health. The cereals and legumes are rich in carbohydrates and proteins and many other nutrients beneficial for health. These are known as poor’s man meat and good sources of complex dietary carbohydrates (starch and dietary fiber), protein, minerals, and B vitamins (Kumari and Sangeetha 2017). The climate change and excessive use of chemical pesticides/fertilizers lead to concern over quality food production (Kour et al. 2019a; Verma et al. 2016). Pests and diseases pose a major threat to the cultivation/storage of crops and cause economic losses for the producer/industry. The excess use of agrochemicals causes pollution, hazardous effect on human health, and residue problems in the plant. The endophytes have diversified taxonomical positions with the vast range of ecological adaptations and mode of action. It’s a useful tool for biological control for modern agriculture for plant health management and sustainable crop production (Waghunde et al. 2016, 2017). Endophytic microbes are the new weapon for biological control of plant disease, insect, and pest management (Khare et al. 2018; Suman et al. 2016). Different bioagents are present in the market, but they are not effective and reliable. The endophytes are associated with plants >400  million years as per fossil record which presented colonization power of endophytes with the host. The mutualistic nature and high colonization rate are vital features of endophytes to use as an active biocontrol agent. Endophytes are the best alternative source for eco-friendly management of the plant as well as human disease.

4.2  Ecology of Endophytes The complex theories were reported by the scientist in connection with the endophyte-­host plant interaction. Mutualistic microbes, an opportunistic pathogen, and competitor role with host/core microbes were described in various experiments (Waghunde et al. 2019). Endophytes are reported from different habitats, i.e., tropical, temperate, xerophyte, and aquatic niches; during ecological studies of H. indicus and A. racemosus endophytes, it was found that some endophytes are host specific in particular environmental condition, while others have wide host range (Rather et al. 2018). The bacterial endophytes (Bacillus and Arthrobacter) are not found in all ecosystems of poplar trees, but Pseudomonas sp. is found in another tissue belonging to the same soil. The variation in the colonization of endophytic bacteria has been observed in hybrid aspen plants. Tripartite interaction, i.e., host-­ plant-­pathogen study, is the most important thing to understand the mechanism of endophytic microbes (Anyasi and Atagana 2019). The root endophytic fungi are much competing with other fungi belonging to the same phylogenetically related species because of homogenous ecological preference and demand of the same nutrition sources (Kia et al. 2019). The production of

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biological compounds, and siderophores by endophytic microbes help the plants to sustain under the extreme condition. Endophytes are site (a core fungi maximum in Sothern valley than the rest of the sample area) and host specific (variations in endophytic microbe populations in H. formosana and another host) (Thomas et al. 2019). The activities of endophytic microbes are influenced by plant ecology and its surroundings, physiochemical properties of the soil, microbiota of the host plant, tissue type, genotype host specificity, macro-/micro-host climate, and the growth/ cultivation season (Murphy and Hodkinson 2018; Saxena et  al. 2016; Yadav et al. 2020).

4.3  Mode of Action The endophytic microbes reside in different parts of the plant with different nature of the host. Endophytes possess plant growth-promoting attributes, are resistant to abiotic stress, produce bioactive compounds, and are thus beneficial for human and plant health (Rana et  al. 2019c; Yadav 2017). The different modes of actions of endophytes are elaborated in Fig. 4.1 (Waghunde et al. 2017). A variety of antimicrobial compounds, i.e., bioactive compounds and secondary metabolites (alkaloids, flavonoids, peptides, polyketides, and volatile organic compounds with terpenoids), are known to be produced by endophytic microbes which inhibit/kill the growth of pathogens. The mycoparasitim and competition type of mode of action have not been confirmed or not reliable by endophytes. The conditions required for biocontrol agent are not fulfilled by endophytic microbes. Furthermore, there is a need to study its activities by modern molecular techniques and effective microscopy methods (confocal or light microscopy). The antibiosis and induced resistance mechanisms of endophytes have been successfully demonstrated in researches (Latz et al. 2018). Endophytes have various activities, i.e., they promote plant growth by IAA, gibberellin and cytokinin production, phosphate solubilization, and nitrogen fixation (Kour et al. 2020d; Rana et al. 2020c; Verma et al. 2019; Yadav 2019). The synthesis of biological compounds, production of siderophore, and alternation of metabolisms result in resistance to environmental stress in plants (Anyasi and Atagana 2019; Shelake et al. 2018; Yadav et al. 2017).

4.4  Applications of Leguminous Endophytes in Plant 4.4.1  Phytostimulation Nutrients are indispensible for normal growth and development of the plant, available from the surrounding environment. The plant continuously absorbs nutrient from soil and when nutrients are not absorbs by plant, the symptoms of deficiency

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Fig. 4.1  Diagrammatic representation of the plant growth-promoting (PGP) mechanisms for abiotic and biotic stress tolerance mediated by endophytic microbes is drawn (adapted with permission from Waghunde et al. 2017). The various chemicals/effects produced by endophytic microbes are mentioned inside the cell (top-left panel). The top-right panel (marked with green) depicts the various mechanisms positively regulated by endophytes for the host plant. At the bottom, left panel (−endophytes), plant growth without the use of endophyte microbes is shown, and in the right panel (+endophytes), improved plant growth occurs due to the beneficial effects of applied endophytes. Abbreviations used: ACC 1-aminocyclopropane-1-carboxylate, ABA abscisic acid, ISR/ SAR induced systemic resistance/systemic acquired resistance

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become apparent first on the older leaves. Nutrient deficiency in the soil can be overcome by applying chemical fertilizers. However, injudicious use of chemical fertilizers for prolonged period results in deterioration of soil health. Alternatively, many endophytic microbes have a great potential to reduce environmental impact due to use of chemical fertilizers, specifically nitrogenous chemical fertilizers. Endophytic microbes help in the nutrient absorption by plants (Nair and Padmavathy 2014). Endophytic microbes in terms of nitrogen fixation potential have been studied in detail from leguminous and nonleguminous plants (Yadav et al. 2018). Several root-inhabiting endophytic microbes such as Acetobacter diazotrophicus, Herbaspirillum, and Azoarcus can fix atmospheric nitrogen (Baldani et  al. 1997; Reinhold-Hurek and Hurek 1998; Yadav et al. 2017); however, their nitrogen fixation efficacy is much inferior over root nodule-forming Rhizobium in leguminous plants (Dalla Santa et al. 2004). Exceptionally, higher nitrogen fixation efficacy in nonleguminous plant sugarcane is due to a symbiotic relation with endophytic strains of Gluconacetobacter diazotrophicus (Carrell and Frank 2014). Apart from nitrogen fixation, numerous leaf endophytic bacteria elicit different mechanisms to confer tolerance against phosphorus deficiency in tall fescue (Malinowski et  al. 2000). Additionally, several plant-associated sulfur-oxidizing endophytes oxidize elemental sulfur to plant utilizable sulfate (Banerjee and Yesmin 2009) and increase availability of micronutrient sulfur for plant metabolism. Thus, different microbes can stimulate plant growth by increasing availability of microand macronutrients by different mechanisms such as fixation, solubilization, mobilization, and phytostimulation. Phytostimulation by root-associated microbes is a well-known and explored area in terms of plant-microbe interactions. Bacteria residing in the plant tissues have been found to secrete a wide a range of phytohormones like auxins, gibberellins, and cytokinins and cause morphological as well as structural changes in the plant (Kour et al. 2020a; Rana et al. 2020a). Due to these mechanisms, endophytes have a great potential in sustainable agriculture (Sturz et al. 2000; Rana et al. 2019b). Microbial-mediated indole acetic acid production increases plant growth and nutrient absorption and, therefore, favors interaction between plant and soil microbes (Spaepen and Vanderleyden 2011; Gamalero and Glick 2011). Endophytic microbial consortia comprising phytohormone-producing fungi Paecilomyces formosus and bacterium Sphingomonas sp. considerably reduced aluminum and zinc stresses with higher plant attributes over uninoculated control in leguminous plant, Glycine max (Bilal et al. 2018).

4.4.2  Bioactive Compounds Endophytes have been explored for their efficacy of producing broad-spectrum, bioactive secondary metabolites such as alkaloids, benzylpyranones, chinones, phenolic acid, quinines, steroids, terpenoids, xanthones, and many other bioactive compounds (Tan and Zou 2001). Production of bioactive compounds is helpful in

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the plant defense mechanisms and also important in the pharmaceutical industries (Rana et al. 2019a). Dasari et al. (2015) reported bioactive compound production from endophytic bacteria and fungi isolated from rose and mango plants, and both were found potent in terms of plant growth promotion efficacy of wheat under pot conditions. Surprisingly, isolates were also secreting bioactive compounds that inhibit various human pathogenic bacteria. Medicinally important, nonlegume plant Azadirachta indica harbor diversified endophytic fungi population that could secrete bioactive metabolites like phenol, tannin, flavonoid, ascorbic acid, and β-carotene (Kumaresan et  al. 2015). Rajagopal et  al. (2011) studied endophytic fungus Diaporthe for bioactive compound melanin production in Azadirachta indica and concluded that the fungus partner provide adaptation to the plant by overcoming the host barrier, competing with other fungi, and surviving in harsh condition. A leguminous plant pigeon pea supports endophytic Fusarium solani that secreted natural antioxidative bioactive cajaninstilbene acid (Zhao et al. 2012). Thus, various endophytic microbes, particularly fungi, have the capacity to secrete many bioactive compounds in association with plants that could confer plant tolerance toward biotic stresses. Biotechnological exploitation of plant endophytic microbes is an easy tool for extraction of novel bioactive compounds that could be the effective agent in the medical field as antibiotics, anticancer drugs, and biological control agents (Kour et al. 2020b; Rana et al. 2020b). Taxol, a chemical compound secreted by the plant-­ associated fungus Metarhizium anisopliae from a bark of the Taxus tree, possesses a very good anticancer activity (Jalgaonwala et  al. 2011). Moreover, terpenoids, another bioactive compound, possess antineoplastic, antibacterial, and antiviral activities (Jalgaonwala et al. 2011). Potential fungal endophyte Armillaria mellea produced a large number of antimicrobial compounds such as alkaloids, steroids, peptides, phenols, terpenoids, quinines, and flavonoids with antimicrobial activities against Gram-positive bacteria, yeast, and mold (Momose et  al. 2000). Marinho et al. (2005) isolated Penicillium janthinellum from fruits of Melia azedarach that produced a bioactive compound polyketide citrinin that showed percent antibacterial activity against Leishmania sp. Endophytes have also been explored for bioactive compound production for pharmacological applications and as a food preservative (Yadav et al. 2019a).

4.4.3  Enzyme Secretion Enzymes are the proteinic product of endophytic bacteria and fungi that provide selective advantage in the growth of plant partner. Microbes have the capacity to secrete diverse enzymes, namely, proteases, cellulases, pectinases, tyrosinases, hemicellulases, phytases, asparaginases, chitinases, and amylases (Yadav et  al. 2016, 2019c). Rashed et al. (2016) isolated different bacterial endophytes form various parts of leguminous (Vicia faba, Pisum sativum, Trigonella foenumgracum, Lupinus spp., Phaseolus vulgaris) and nonleguminous plant (Oryza sativa). Among

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167 isolates, 55 were positive for cellulases and pectinases, 12 for IAA production, and 44 and 19 for ammonia production and phosphate solubilization, respectively. Application of such multi-trait plant growth-promoting endophytes in legumes and nonlegumes may save agrochemicals and may be helpful in minimizing the use of harmful agrochemicals. Majority of extracellular enzymes producing endophytes have been isolated, characterized, and explored from plants of medicinal value. Patil et al. (2015) isolated different fungi of endophytic nature, viz., Aspergillus sp., Biosporus sp., Chaetomium sp., Cladosporium sp., Colletotrichum sp., Curvularia sp., Fusarium sp., Rhizoctonia sp., etc., from seven medicinal plants, and fungi were found potent in terms of extracellular enzyme secretion such as proteases, cellulases, and lipases. This strong enzyme production ability may find its application in the clinical microbiology and therapeutic purposes. Apart from this, an extracellular enzyme from endophytic fungi is also useful in food processing, confectionery, textile, and leather industries (Sunitha et al. 2013). Many endophytic fungi form mutualistic relation with the grass plant and confer advantages to the hosts by reducing herbivory by insects and animals due to the mechanism of extracellular enzyme secretion and therefore protect the plant from biotic stress (Yadav et al. 2020). Moy et al. (2002) explored an interaction between Poa ampla and the fungal endophyte Neotyphodium sp., as endophyte partner secrete β-1,6-glucanase to provide positive benefits to plant partner against biotic stress. Abiotic stresses are also a major concern as they produce plant metabolic by-­ products like reactive oxygen species (ROS) and reactive nitrogen species (RON) and can cause extensive damage in plant tissues by oxidizing biomolecules of the cell. Many endophytic microorganisms have the capacity to produce detoxification enzymes like glutathione, peroxidase, catalase, etc. to confer plant tolerance against abiotic stress-mediated oxidative damage (Hardoim et al. 2015). Though explored less over endophytic fungi, plant-associated actinobacteria also produce wide ranges of extracellular hydrolytic enzymes. Twenty three actinobacterial endophytic isolates from tomato plants produced considerable extracellular enzymes such as amylase, pectinase, cellulase, lipase, esterase, caseinase, gelatinase, and catalase (Minotto et al. 2014), of which majority of these isolates produced the highest enzymes at 30  °C.  These enzymes may be useful in protecting plant tissues against stress as well as also useful in human and veterinary pharmaceuticals.

4.4.4  Antagonistic Potential Plant diseases caused by different microbes such as fungi, bacteria, and viruses cause biotic stress in the plant that could result in the loss of productivity. Management of plant diseases in agriculture is based on the use of agrochemicals that are not only costly but also harmful to soil, plant, and human health. The use of antagonistic microorganisms in plant disease management may be the eco-friendly

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and cost-effective strategy to manage such problems, a step ahead in the direction of sustainable agriculture. Various endophytic fungi such as Colletotrichum, Cladosporium, Fusarium, Pestalotiopsis, and Trichoderma possess antagonistic potential against different plant pathogens by mechanisms like mycoparasitism, lytic enzyme secretion, antibiosis, and induced systemic resistance (ISR) (Kaur et al. 2020; Silva et al. 2019; Singh et al. 2020). Soybean (Glycine max L.), a leguminous plant, harbors a variety of endophytic bacteria such as Enterobacter, Acinetobacter, Pseudomonas, Ochrobactrum, and Bacillus that could strongly inhibit plant pathogenic fungi Phytophthora sojae under in vitro conditions. Further analysis revealed that Acinetobacter calcoaceticus showed very strong inhibitory activity (71.14%) against P. sojae, by causing abnormality in fungal mycelium due to fracture, lysis, protoplast formation, and split end (Zhao et  al. 2018). Nuraini et  al. (2017) reported antagonism by endophytic fungi against Fusarium oxysporum, responsible for eggplant wilt. Six different endophytic fungi, FEB1 (Rhizopus sp.), FEB2, FEB3, FEB5 (Helicomyces spp.), FED1 (Mucor sp.), and FED2 (Penicillium sp.), were inhibiting F. oxysporum by different mechanisms such as competition, antibiosis, and parasitism. Chitinolytic Trichoderma sp. has great antagonistic potential against Ganoderma boninense, a fungus responsible for basal stem rot infecting oil palm (Yurnaliza et  al. 2014). Inhibition of plant pathogen G. boninense by the biocontrol agent was recorded up to 80% under in vitro conditions, and microscopic data suggested that endophytic Trichoderma was attached to the hyphae of G. boninense at the interaction zone, causing abnormalities in the G. boninense (Yurnaliza et al. 2014). Thus, endophytic bacteria and fungi could reduce incidence and severity of the disease and helpful in preventing biotic stress in plants. The plant-associated microbes secrete chemical compound (siderophore) that chelates iron and increases its availability to plants and at the same time deprives iron to the plant pathogens (Compant et al. 2005). Endophytes have been characterized and explored for their efficacy of different types of siderophore production; however, catecholate, hydroxamate, and phenolate possess excellent biocontrol properties (Rajkumar et al. 2010).

4.4.5  Pigment Production Fungi are capable of producing wide ranges of pigments like carotenoids, flavins, melanins, and quinines. The plant Ixora coccinea L. harbors endophytic fungus Bartalinia sp. that could produce pigment with the potential application in healthcare, to minimize the detrimental effect of synthetic pigments (Murugan and Mugesh 2013). Prodigiosin, a red pigment produced by Gram-negative, catalase-­ positive, endophytic bacterium Serratia marcescens isolated from plant Beta vulgaris, is a promising textile and food colorant (Bushra and Chandra 2015). Many endophytic pigments also find its application in the pharmaceutical industries. Endophytic fungus Monodictys castaneae produces pigments that show

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antibacterial activities against human disease-causing bacteria such as Klebsiella pneumoniae, Staphylococcus aureus, and Vibrio cholerae (Visalakchi and Muthumary 2009). Thus, use of endophytic fungal pigments may be helpful in the treatment of human diseases caused by bacteria, somehow to reduce the problem of antibiotic resistance among different human pathogenic bacteria. Huang et  al. (2011) reported that mangrove endophytic fungi Alternaria sp. produced anticancer molecule anthraquinone. An endophytic fungus Aspergillus flavus from medicinally important plant Ocimum sanctum produced a red colored pigment under lab conditions, with the highest amount of production at 30 °C temperature, 6.5 pH, after 15 days of incubation which showed good antioxidative and cytotoxic properties (Gurupavithra et al. 2017).

4.4.6  Bioremediation With the advancement of industrialization and urbanization, a huge amount of organic and inorganic wastes are generated due to man-made activities that usually pollute the environment. The most problematic wastes include heavy metals and xenobiotic compounds. Large numbers of microorganisms are involved in the bioremediation process, and their efficacy depends on the chemical nature of the waste material and also its properties and environmental conditions (Yadav et al. 2019d). Endophytic microbes might be more superior to others because they follow the process of bioaugmentation (Newman and Reynol 2005; Shelake et al. 2018). Endophytic microorganisms, especially for the purpose of heavy metal bioremediation, could be isolated from the plant growing in the contaminated soil. It is hypothesized that the plant could tolerate heavy metal in the soil due to the existence of endophytic partner. A convincing study on heavy metal arsenic (AS) bioremediation was performed by Mukherjee et  al. (2018). They isolated different endophytic microbes from AS tolerant-Lantana camara plant and successfully established that microbes in the surrogate plant Solanum nigrum. The most effective endophytes improved bioaccumulation of AS metal with improving plant growth-­ promoting parameters such as photosynthetic activity, phosphate nutrient, and elevated glutathione levels under AS stress condition. Many endophytic bacteria isolated from inner tissues of legumes and nonlegumes could detoxify heavy metals, and it may be the promising tool for increasing the efficacy of phytoremediation by plant-microbe symbiotic association (Rajkumar et al. 2009). A nonlegume, cadmium hyper-accumulator plant Solanum nigrum L. harbors endophytic population of bacteria Serratia with plant growth-promoting capability by IAA secretion, siderophore activity, and phosphate solubilization potential along with tolerance against the toxic effect of heavy metals (Luo et al. 2011). The diverse metabolic pathways of endophytes have also been studied for their efficacy of bioremediation against complex substances. An endophytic bacterium Methylobacterium populi, isolated from poplar trees, possesses tremendous potential of degrading complex compounds like 2,4,6-trinitrotoluene (TNT),

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hexahydro-­1,3,5-trinitro- 1,3,5-triazine (HMX), and hexahydro-1,3,5- trinitro-1,3,5triazine (RDX) (Van Aken et al. 2004). Riskuwa-­sehu and Ismail (2018) studied the effect of microbes on phytoremediation of polycyclic aromatic hydrocarbons (PAHs) on legumes Cajanus cajan as well as Lablab purpureus and revealed that soils treated with C. cajan and L. purpureus reduced PAHs to 2.34  ppm and 4.88  ppm, respectively, from 19.21  ppm PAHs. Naphthalene was completely degraded in both cases and pyrene, fluorene, and fluoranthene were either completely degraded or significantly reduced. The study indicated a positive role of endophytic partner in the phytoremediation process. Root nodules of leguminous plants Vicia faba and Lupinus albus possess useful bacterial consortia that could be explored for oil utilization and nitrogen fixation. Legume plants V. faba and L. albus were cultivated and compared with nonlegume plant, Solanum melongena, in the sand contaminated with oil. There was more oil attenuation in the plant-­cultivated samples than in uncultivated samples. Oil attenuation was more prominent in the legumes than the nonlegume crops. Therefore, it can be concluded that legumes, with the help of endophytic partner, possess great potential of oil degradation (Dashti et al. 2009).

4.4.7  Production of Volatile Organic Compounds Chemically volatile organic compounds (VOCs) are the carbon-based, low-­ molecular-­weight, and vaporizable molecules produced by living organisms during metabolic processes (Bennett and Inamdar 2015). Endophytic fungal-produced volatile organic compounds have been studied for their role as a biological control agent of insects, bacteria, and fungi, due to its potential as a biofumigants and also as a biofuel and flavoring compounds (Wani et al. 2015). Fungi secrete many broad spectrums of VOCs, including terpenes, flavonoids, alkaloids, cyclohexanes, and hydrocarbons. Such compounds possess antimicrobial, antioxidant, antineoplastic, antileishmanial, and antiproliferative activities (Naik 2018). Endophytic bacteria are known to produce VOCs in different plants and confer tolerance to plant partner against many biotic stresses. One of such endophytic bacteria is Enterobacter aerogenes in the maize plant. An association of bacterial partner with the maize plant produced VOC 2,3-butanediol that conferred plant resistance toward the fungus Setosphaeria littoralis responsible for northern corn leaf blight (D’Alessandro et al. 2014). Microbial-mediated VOCs are ubiquitous in environments and useful for the bio-­ communication with other organisms. Nowadays, many cryptic fungal symbionts from healthy plant tissues produce volatile compounds with strong antibiotic activity and also carbon chains identical to those found in the petroleum (Yuan et  al. 2012). Fungal endophytes Phomopsis sp. isolated from plant Odontoglossum sp. was explored in terms of VOC production such as sabinene, 1-butanol, 3-methyl, benzene ethanol, 1-propanol, 2-methyl, and 2-propanone with broad spectrum antifungal activities against potential plant pathogens such as Botrytis, Colletotrichum,

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Fusarium, Pythium, Phytophthora, Rhizoctonia, Sclerotinia, and Verticillium (Singh et al. 2011). One of the potential VOCs producing fungal endophyte Hypoxylon sp. showed biological control potential against different plant pathogenic fungi such as Botrytis cinerea, Cercospora beticola, Phytophthora cinnamomi, and Sclerotinia sclerotiorum (Tomsheck et al. 2010), suggesting positive interaction between VOCs producing endophytes and its plant partner. The fungus Hypoxylon sp. was also explored for many other VOCs such as 1-methyl-1,4-cyclohexadiene and 1,8-cineole for their mycodiesel potential (Tomsheck et al. 2010). Wang et al. (2017) isolated the plant-­ associated fungus Annulohypoxylon sp. from plant Neolitsea pulchella and studied for its potential of VOC 1,8-cineole production and suggested that 1,8-cineole reached up to 94.95% in the PDA medium and up to 91.25% of the relative area in the raw poplar dust. Such VOCs can be produced on agricultural wastes, and it can be an alternate fuel additive for the diesel as well as gasoline engines.

4.4.8  Application in Tissue Culture Tissue culturing of agriculturally important plants involves basic steps such as explant selection, sterilization of explants, inoculation into artificial media, callus formation, root and shoot multiplication, hardening, and acclimatization. The ultimate success of micropropagation depends on the successful establishment of micropropagated plantlets in the soil (Saxena and Dhawan 1999). Bio-hardening or biotization of the micropropagated plant is the metabolic response of the plant to microbial inoculants, resulting in developmental and physiological changes that enhance biotic and abiotic stress tolerance of the derived propagules (Chikkalaki et al. 2017). Philipp et al. (2016) reported the positive role of endophytic microbes in micropropagated medicinal and aromatic plants. Biotization of micropropagated plants with endophytes can improve plant growth, yield, and survival as well as induce tolerance against abiotic stresses. Bacteria with endophytic origin, Microbacterium sp. and Rhodopseudomonas sp., were detected in the easily propagated Prunus avium L. and not in the difficult to propagate P. avium plants (Quambusch et  al. 2014), indicating a positive role of bacterial endophytes in the success of micropropagation.

4.5  Biotechnological Applications Biotransformation is gaining great attention due to its advantages over many chemical synthetic compounds. Biotransformation is important in the synthesis of the novel compound with enhancement of productivity, elucidation of basic biosynthetic pathways in living systems, and overcoming many problems associated with

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the chemical synthesis of compounds (Suresh et al. 2006). Apart from biotransformation, endophytes have diversified native biological compounds, viz. camptothecin, hypericin, paclitaxel, podophyllotoxin, and vinblastine, with great industrial and biotechnological potential in agriculture and pharmaceutical industries (Joseph and Priya 2011; Zhao et al. 2011). Molina et al. (2012) investigated biotechnological and biotransformation potential of endophytic fungi from plant Dipteryx alata Vog. Five fungi were evaluated, and most of the fungal extracts inhibited the growth of Candida albicans, Escherichia coli, and Staphylococcus aureus. All showed potential of amylase and lipase production, and three fungal strains were showing biotransformation of α-pinene into verbenol, a compound of great industrial significance. Thus, exploring these endophytes in the biotransformation process is of great economic importance to synthesize high-value compounds.

4.5.1  Stress Tolerance in the Plant Different stresses are responsible for limiting growth and development of the plant. The major abiotic stresses affecting plants are drought, chilling injury, high temperature, salinity stress, acid and alkaline conditions, heavy metal stress, and nutrient deficiency (Chaves and Oliveira 2004; Yadav et  al. 2019b; Yadav and Yadav 2018). Apart from the above listed abiotic stresses, many biotic stresses such as plant pathogenic microbes, weeds, and insects also affect plant growth (Kumar et al. 2019a, b; Rajawat et al. 2020). Abiotic stresses are affecting plant population on a larger area and difficult to manage over biotic stresses. The initial effects of abiotic stresses are production of ROS (reactive oxygen species) and RNS (reactive nitrogen species), resulting in the modification of enzyme and gene regulation (Wilkinson and Davies 2010; Mittler et al. 2011). Additionally, plants exposed to abiotic stresses produce a higher amount of plant growth-retardant hormones such as abscisic acid (ABA) and ethylene (Goda et al. 2008) that can cause growth retardation and death of the plant in extreme conditions. Drought stress usually produces deleterious effect on crops by limiting productivity (Kour et al. 2020c; Rastegari et al. 2020a). Application of the plant-associated fungal and bacterial endosymbiotic microbes during the seed production of the F1 endosymbiotic plant considerably improved seed germination and root and shoot growth (Kumari et al. 2018). Downregulation of antioxidant genes, proline, SOD, and dehydrin, was seen due to endosymbionts, resulting in enhanced oxidative stress tolerance and reduction in ROS in the host cells. Endophyte-associated plants require significantly less water and produce more biomass than plants without endophytes. Possible mechanisms of drought tolerance conferred to plants by its endophytic partner could be augmented by the accumulation of solutes, reduced leaf conductance, lower transpiration in a stream, and formation of a thick cuticle layer (Malinowski and Beleskey 2000).

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Bacterial endophytes, that is, Arthrobacter sp. and Bacillus sp., isolated from pepper plants reduced stress of plants by regulation of stress-inducible genes over plants (Sziderics et  al. 2007). The fungal endophytes Penicillium sp. and Phoma glomerata from the cucumber plant significantly improved plant biomass, nutrient assimilation, and plant growth parameters and reduced sodium toxicity under salinity and drought stress induced by artificial ingression of sodium chloride and polyethylene glycol, respectively, when compared with a control plant. The endophyte-infected plant downregulated abscisic acid and elevated the level of salicylic acid to survive and tolerate abiotic stresses such as salinity and drought (Waqas et al. 2012). Microbes with ACC (1-aminocyclopropane-1-carboxylate) deaminase potential can reduce ACC level by degrading it into ammonia and alpha-ketobutyrate (Glick et al. 2007), thus promoting plant growth by reducing the growth-retardant ethylene level in plants (Hardoim et al. 2008; Glick 2014). The degradation of the ACC by ACC deaminase activity stimulates ACC efflux into plant, thus increasing growth and development of roots (Glick et al. 2007). Etesami et al. (2014) isolated 80 endophytic Pseudomonas fluorescens from roots of the rice seedling, and application of these endophytes on the rice seedling increased root elongation and endophytic root colonization as compared to control plant under constant flooded conditions, suggesting the role of ACC degradation-positive endophytic bacteria in plant growth and root colonization under stress conditions. Salicylic acid (SA)- and jasminic acid (JA)-mediated pathways play a vital role in the plant stress tolerance against plant pathogenic microbes (Khare et al. 2016). Salicylic acid- and jasminic acid-mediated biochemical pathways are responsible for the ISR induction in the plant (Pieterse et al. 2012), creating plant resistance against pathogens. Different bacterial endophytic genera, including Pseudomonas (P. fluorescens, P. syringae), Bacillus (B. amyloliquefaciens, B. pumilus, B. subtilis), Serratia (S. marcescens), etc., are the chief microbes responsible for ISR in plants (Kloepper and Ryu 2006).

4.6  Endophytes with Multiple Traits Recently, endophytic microbes have been explored for their multiple plant growth-­ promoting potential under changing micro and macro environmental conditions (Rastegari et al. 2020b; Singh and Yadav 2020). It can be hypothesized that multi-­ trait endophytes are helpful in the promotion of plant growth under normal environmental conditions and also provide plant tolerance against microbial-mediated biotic stresses as well as abiotic stresses that compromise plant growth and productivity (Kour et  al. 2019b; Kumar et  al. 2019a, b; Yadav et  al. 2019e). Sansanwal et al. (2018) studied 41 multi-trait endophytic microbes from mung bean root and reported that 46% isolates could tolerate 45 °C temperature, 19% are grown at 5% NaCl, most of the isolates were IAA and ammonia producers, 49% were phosphate solubilizers, and 24, 29, and 76% endophytic isolates were ACC deaminase,

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siderophore, and HCN positive, respectively. Therefore, isolates were multi-trait and could be utilized in sustainable agriculture. Maize, a nonlegume plant, irrigated with industrial and municipal wastewater, harbors diversity of the culturable endophytic bacterial population that could possess multi-trait plant growth promotion potential (Abedinzadeh et al. 2019). Rohini et al. (2018) isolated endophytic bacteria from the rhizome part of Zingiber officinale and analyzed for multiple plant growth-promoting traits under in vitro conditions. Plant growth-promoting characters such as N2 fixation, ammonia production, IAA secretion, phosphate solubilization, and ACC deaminase activity were recorded. Multi-trait endophytic fungi Mucor sp., isolated from nonlegume Brassica campestris, was found potent in terms of IAA production, ACC deaminase activity, and phosphate solubilization potential under lab conditions. Additionally, the fungus was tolerant to multiple heavy metals such as chromium, cobalt, copper, manganese, and zinc. Thus, the fungus could be a potential agent for phytostimulation in the heavy metal-affected fields (Zahoor et al. 2017). Shan et  al. (2018) screened 46 actinobacteria from Camellia sinensis; 16  s RNA analysis revealed that they were encompassing 11 families and 13 genera, including Actinomadura, Kribbella, Kytococcus, Leifsonia, Microbacterium, Micromonospora, Mobilicoccus, Mycobacterium, Nocardia, Nocardiopsis, Piscicoccus, Pseudonocardia, and Streptomyces. Further, 21.7% isolates were showing ACC deaminase potential and 93.5% IAA production. Thus, plant-associated endophytic actinobacteria can be helpful for phytostimulation and tolerance of abiotic stresses.

4.7  Conclusion and Future Thrust The various chemicals used for pest management have hazardous effects on human health and environment. Endophytes are one of the best alternatives for bioagent having wide host range, i.e., cereals, pulses, oilseeds and forest tress. Almost 1–2% terrestrial plant association with endophytes has been reported but scanty of research done on endophyte-aquatic plants. They may be the best source for environment cleanup and anticancer bioactive compounds. There is meager research on bioformulation development of endophytes and their applications methods; thus, focus should be given on development of these techniques. There is a scope for database development of bioactive compounds and secondary metabolites and their applications in agriculture, forestry, and environmental and human health solutions. Genetically engineered endophytes can be used to remediate metal stress, disease management, and environment cleanup. The study on the mode of transmission of endophytes from seed to seed is the prominent feature of endophytes in biological control. The current approaches based on “omics,” i.e., genome sequencing, comparative genomics, microarray, next-generation sequencing, metagenomics, and metatranscriptomics, will help to know interactions between endophytes and plants and thus can be exploited for understanding the interactions.

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Chapter 5

Arbuscular Mycorrhizal Fungi: Abundance, Interaction with Plants and Potential Biological Applications Manoj Parihar, Manoj Chitara, Priyanaka Khati, Asha Kumari, Pankaj Kumar Mishra, Amitava Rakshit, Kiran Rana, Vijay Singh Meena, Ashish Kumar Singh, Mahipal Choudhary, Jaideep Kumar Bisht, Hanuman Ram, Arunava Pattanayak, Gopal Tiwari, and Surendra Singh Jatav

Abstract  Beneficial microbes associated with plant roots play an important role to achieve higher agriculture production for burgeoning population in sustainable way. Among various microbes, arbuscular mycorrhizal (AM) fungi interaction with higher land plants is unique as they occupy position both inside and outside of roots. AM fungi as a natural symbionts of land plants provide various ecological services, in particular by improving plant water and nutrition availability, soil health and fertility, alleviating stress condition and wasteland management. Mycorrhizae as a broader group of fungi include seven types of members, i.e. arbuscular, ecto, ectendo, arbutoid, monotropoid, ericoid and orchidaceous, while arbuscular and ectomycorrhizae are the most abundant and ubiquitous. In this chapter, we focus on AM fungi and provide an overview on mycorrhizal interaction, benefits, processes,

M. Parihar (*) · P. Khati · A. Kumari · P. K. Mishra · V. S. Meena · A. K. Singh · M. Choudhary · J. K. Bisht · H. Ram · A. Pattanayak ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India e-mail: [email protected] M. Chitara Department of Plant Pathology, College of Agriculture, GBPUAT, Panatnagar, India A. Rakshit · S. S. Jatav Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences, Banaras Hindu University (BHU), Varanasi, Uttar Pradesh, India K. Rana Department of Agronomy, Institute of Agricultural Sciences, Banaras Hindu University (BHU), Varanasi, Uttar Pradesh, India G. Tiwari Division of Soil Resource Studies, ICAR-NBSS&LUP, Nagpur, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_5

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production development and potential application domain under various conditions. Along with recent advances in AM fungi role under various stress condition, reclamation of problematic wastelands and production aspects, we also discuss about the basic features of AM fungi with past developments to provide an overall glimpse of this plant-fungal interaction. In spite of its growing trends, AM fungi’s current application and market sharing are far below to full potential. Regarding this, current challenges, constraints and strategies for future road map to overcome these problems are also discussed briefly. Keywords  AM fungi · Biotic stress · Nutrient loss · Symbiosis · Agroecosystem

5.1  Introduction Beneficial microbes associated with plant systems play an important role to achieve higher agriculture production. Recently, Ponce-Toledo et al. (2017) made evident that early land plant evolved from freshwater algal charophyte lineage with some obvious adaptation including protection against high radiation, a water-impermeant cuticle and vascular systems with water-conductive nature. At early stage, in the absence of root development, some important innovations were required in plants to absorb the water and nutrients from soil or other growth medium. In such circumstances, fungal symbiosis was imperative for freshwater algae to allow them to colonize the land (Delwiche and Cooper 2015; de Vries and Archibald 2018). Although AM fungi may not have been the earliest fungal symbiont with first land plants but they are coevolved with roots of vascular plants (Yadav et al. 2019a, b). Phylogenetic analysis suggested that AM symbiosis appeared in early Devonian period (~393–419 Ma) when land was colonized with plants which are having rhizoid-type absorbing site (Remy et al. 1994; Brundrett 2002). The origin of arbuscules during early Devonian period presents the mutualism for nutrient transfer which came into existence during the invasion of land by plants (Fig. 5.1). Remy et al. (1994) reported occurrence of AM in extant species of bryophytes, pteridophytes and gymnosperms. Wang et al. (2010) suggested the crucial role of AM symbiosis for the origin of land plants through investigation of three genes (IPD3, DMI1 and DMI3) which are required for the formation of mycorrhiza in different legumes and rice. AM fungal symbiosis is one of the remarkable adaptation for land plants and was so successful that still majority of plants are engaged in this association. Moreover, AM fungi as the most ubiquitous partner of land plants are successfully reported from the world’s most complex and diverse habitats like mangrove, forest, coastal regions, desert, grassland, agriculture and polar region (Shi et  al. 2006; D’Souza and Rodrigues 2013; Öpik et al. 2013; Oehl et al. 2017; Yakop et al. 2019; de Assis et al. 2018). Brundrett (2009) after considering the literature containing data for 336 plant families revealed that almost 74%, 9%, 2%, 1% and 6% of Angiosperm species roots

Angiosperms

Monilophytes Lycophytes

Gymnosperms

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Mycorrhizal colonization

Bryophytes

Vegetation Development

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485

444

Ordovician

420 Silurian

359

Devonian

200

Carboniferous Permian/Triassic

145 Jurassic

66 Cretaceous

Time Interval (Mya) Fig. 5.1  Estimated time period of AM fungi origin, divergence with land plant development

were colonized with arbuscular, orchid, ectomycorrhizae and ericoid mycorrhizae and non-mycorrhizal, respectively. Microbes are ubiquitous in nature. Different groups of microbes have been reported from diverse sources and have a beneficial impact on plant growth promotion and crop productivity (Rastegari et al. 2020b; Singh and Yadav 2020). Plantassociated and soil microbiomes with plant growth-promoting attributes could be utilized as biofertilizers and biopesticides from crops growing under the abiotic stress condition and natural conditions for agricultural sustainability (Kumar et al. 2019; Rajawat et  al. 2020). These plant growth-promoting microbes have been reported from three domains, namely, archaea, bacteria and eukarya (Kour et  al. 2020c; Rastegari et al. 2020a). The rhizospheric and endophytic microbes promote the plant growth when inoculated with crop (Kour et al. 2020a; Rana et al. 2020a). AM fungi as an obligate symbionts share a distinct feature called arbuscules as a site of nutrient exchanges between host and fungi. Arbuscules developed between cell wall and plasma membrane of root cortical cells and differentiated from plant plasma membrane by periarbuscular membrane (Lambais and Ramos 2010). The main morphological structure of AM fungi is arbuscules, vesicles, auxiliary cells, hyphae and spores which perform diverse function. Extraradical hyphae as a root extension provide large surface area for the absorption of water and nutrients from

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soil solution. These nutrients and water transported to the intraradical hyphae and plants in exchange with photosynthetic fixed carbon. Another important characteristic of AM fungi is their spore production ability with single or multiple layers and size ranges from 22 to 1050 μm in diameter. AM fungal spores contain very unique characteristics and structures such as subtending hypha, sporiferous saccule, sporogenous cell, pregermination structures, peridium, cicatrix or pedicel, and these structures are important for good morphological identification study at species level (Walker 1983; Goto and Maia 2006; Souza 2015). However, recent molecular tools revealed that AM fungi have a great genomic variation with size of 16.54 Mb in Rhizophagus intraradices to 1058.4 Mb in Racocetra gregaria (Hijri and Sanders 2004). Further it is continuously improving our understanding in genetical and evolutionary history of AM fungi and improves the species concept in such complex group of organism.

5.2  Taxonomy of AMF Several classifications have been proposed to categorize the AM fungi from 1800 to present day. In the past, many taxa at all levels in Glomeromycota had created considerable confusion and ambiguity among researcher. In this regard, to clarify the evolutionary history of AM fungi, consensus-based classification of Glomeromycota was established to provide a framework to understand the new taxa and their phylogenetic relationships. In consensus-based classification, Redecker et  al. (2013) found that many previous classifications were based on poor quality data with poor systematic and lack of robust taxonomy. Redecker et al. (2013) classified the AMF in single class Glomeromycetes and maintained the four orders, i.e. Archaeosporales, Diversisporales, Glomerales and Paraglomerales given by Schüßler et  al. (2001) and Walker and Schüßler (2004). Moreover, they rejected the order Gigasporales as proposed by Oehl et al. (2011a, b, c, d, e, f) due to the absence of molecular phylogeny. Within these four orders, 11 families and 25 genera are characterized, and they retained some genera such as Septoglomus as described by Oehl et al. (2011a, b, c, d, e, f) while rejected Albahypha, Entrophospora, Fuscutata, Intraspora, Kuklospora, Orbispora, Quatunica, Simiglomus and Viscospora genera in their consensus-based classification (Table  5.1). The molecular application in the identification of Glomeromycota fungi has increased considerably in various ecosystems (Öpik et al. 2009; Varela-Cervero et  al. 2015) and allowed the discrimination of these root-­ inhabiting microorganisms at species level. In addition to identify the natural diversity of AMF, molecular tools are able to overcome the limitation resulting from previously used morphological-based identification process.

Class Glomeromycetes

Sources: Redecker et al. (2013)

Phylum Glomeromycota

Table 5.1  Taxonomic classification of Glomeromycota

Paraglomerales

Glomerales

Diversisporales

Order Archaeosporales

Paraglomeraceae

Pacisporaceae Sacculosporaceae Claroideoglomeraceae Glomeraceae

Gigasporaceae

Family Archaeosporaceae Ambisporaceae Geosiphonaceae Acaulosporaceae Diversisporaceae

Genera Archaeospora Ambispora Geosiphon Acaulospora Corymbiglomus Diversispora Otospora Redeckera Tricispora Cetraspora Dentiscutata Gigaspora Intraornatospora Paradentiscutata Racocetra Scutellospora Pacispora Sacculospora Claroideoglomus Funneliformis Glomus Rhizophagus Sclerocystis Septoglomus Paraglomus

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5.3  M  ultilateral Interaction Among AMF, Plants and Microbes There are innumerable interactions taking place in the soil system, which determine its structure and properties as a medium responsible for the growth and different activities of plants and soil microorganisms. AM fungi are found to be mutually associated with most of the land plants. Along with plant roots, AM fungi interact continuously with a wide range of soil component (Fig. 5.2) in which rhizospheric microbes are very important. Their interactions in soil can have several important implications in agriculture. The interaction between the AM fungi and soil bacteria starts with binding of soil bacteria to spore of fungi, which inject the molecules into the fungal spore; the molecules like volatiles cause degradation of fungal cell wall. These interactions may alter the gene expression in AM fungi and hence their performance (Miransari 2011) (Fig. 5.2). The number and growth rate of aerobic bacteria in rhizosphere affects the mycorrhizal colonization in roots (Posta et al. 1994). The soil around the external mycelium of mycorrhizal fungi represents a unique habitat as it differs drastically in community composition of bacteria (Timonen et al. 1998). The effect of mycorrhiza on the bacterial community composition in soil may be due to the differences in root exudation and carbohydrate metabolism of plants (Dixon et al. 1989; Shachar-Hill et al. 1995). The microbial community populating the mycorrhizal roots differs in its composition from non-mycorrhizal roots as mycorrhiza stimulates some microbial groups while suppressing others (Vázquez et al. 2000). Some studies also indicate that mycorrhizal species presents differential effect on different bacterial communities present in rhizosphere (Marschner and Baumann 2003). Like plant roots mycorrhizal fungi produce certain substances that may have a selective effect on some microbial community (Marschner and Timonen 2005). Fig. 5.2  Interaction of AM fungi with plant and soil system

Soil environment

Plant

Fungus

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Interactions between bacterial and fungal species play important roles for the formation of mycorrhiza and ultimately affect plant health. The presence of AMF also alters the plant community structure by affecting the type of microorganism and soil which impact the relative abundance of plant species and its diversity (Sanders and Koide 1994; Yadav et al. 2019c). Grime et al. (1987) suggested that the diversity of plant communities is affected by the transport of plant assimilates from the dominant species to subordinate plant species through AMF.  Mycorrhizal dependency is another mechanism for AMF to affect plant community structure in which AMF colonization affects the growth response of plant species differentially (Habte and Manjunath 1991).

5.4  Symbiosis Development Between AMF and Plants Symbiosis development can be categorized in three stages which include asymbiotic phase, pre-symbiotic phase and symbiotic phase (Fig. 5.3). Asymbiotic phase initiates with the spore germination which includes various chain-like steps and ultimately results in germ tube and initial hyphae development (Siqueira et  al. 1985a, b). However, this process does not require availability of host plant but necessarily depends on favourable external condition like adequate soil moisture levels and/or soil pH, temperature, soil fertility, other microbes, etc. (Juge et  al. 2002; Bonfante 2003; Tamasloukht et al. 2003; Bianciotto et al. 2004; Dalpé et al. 2005; Bais et al. 2006; Lambais 2006). Under favourable condition, synthesis of metabolites will increase and enhance the nuclear division and vesicle production (Maia and Yano-Melo 2001). These changes will lead to develop germ tube which may

Symbiotic  Root Colonization  Symbiosis establishment  Intra-radical mycelium development  Extra-radical mycelium development sporulation

A M F U N GI L IF E C Y CL E

Pre-symbiotic Pre-symbiotic  Chemotropism activated  Physical contact with root  Appressorium formation

Fig. 5.3  AM fungi life cycle

Asymbiotic  Quiescent AMF spore  Spore germination  Initial mycelium development

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either produce from peripheral components, spore wall or subtending hyphae (Mosse 1959; Spain et al. 2006; Oehl et al. 2008). Further, this germ tube will produce initial asymbiotic mycelium and cannot survive for longer period if symbiosis will not occur before consuming the store lipids (Oehl et al. 2008; Gamper et al. 2009). Therefore to complete the life cycle, initial asymbiotic mycelium establishes the contact with plant roots and initiates the pre-symbiotic phase. In contrast to asymbiotic phase, pre-symbiotic phase mostly depends on host plants as they produce ramification factors such as flavonoids, CO2 and 5-­desoxiestrigol as activators of the chemotropism to develop membrane potential (Buee et al. 2000 and Besserer et al. 2006). In addition to this, alteration in metabolism to improve the mitochondrial activity, respiration, lipids catabolism, protein synthesis and ATP synthesis by using inorganic phosphorous stored into vacuoles enhances the mycelium growth and establishes a physical contact between AMF and plants root (Ramos et al. 2008a, b, c). While making physical contact, AMF produces myc factor that will start appressorium formation and initiate symbiotic phase (Lanfranco et al. 2005). In symbiotic phase appressorium will penetrate the root epidermal cell and differentiated into intra- and extraradical hyphae (Cruz et  al. 2008). At later stage, intraradical hyphae start moving in cortical cell, while extraradical mycelium moves externally in rhizospheric region and helps in absorption of various low diffusive nutrients. In symbiotic phase for various processes such as active appressorium formation, root penetration, mycorrhiza development, channel activation, molecular signals, protein synthesis, arbuscules formation, Ca 2+ uptake and enzyme activity, five genes are found to be responsible, i.e. DMI, SYMRK, CASTOR, Nup and CYCLOPS (Stracke et al. 2002; Radutoiu et al. 2003; Yoshida and Parniske 2005; Lambais and Takahashi 2006; Kiriacheck et al. 2009). Based on gene function, host plants are categorized in four classes by Yoshida and Parniske (2005): 1. Myc – Type 0: unable to stimulate initial mycelium growth 2. Myc – Type 1: unable to develop initial mycelium growth 3. Myc – Type 2: no intra and extra radical hyphal growth 4. Myc – Type 3: no arbuscules development After the establishment of symbiotic phase, activation of H+-dependent enzymes such as H+ ATPase and H+ pyrophosphatase facilitate the nutrients exchange and utilization by the AM fungi. After symbiosis development, mainly two exchange interfaces are found, i.e. intercellular interface and intracellular interface. The intracellular interface is the interface between periarbuscular and arbuscular membranes (develop from intraradical hyphae) leading to form a cell membrane across all intraradical mycelium of AM fungi which depends on the status of host plant. The H+ ATPase pump located on exchange interface develops H+ gradient, in order to exchange nutrient transfer from AM fungi to host plants and sucrose and amino acids from plant to fungi (Fig. 5.4). Therefore exchange interface forms a basis of symbiosis between both partners to get benefited from each other.

5  Arbuscular Mycorrhizal Fungi: Abundance, Interaction with Plants and Potential…

Environmental protection Enhance N fixation efficiency

Biotic & abiotic stress management

AM fungi

Ecosystem restoration

113

Enhance root absorption capacity

Production of plant growth hormones

Antibiotic secretion

Increase nutrient mobility

Fig. 5.4  Various ecological services provided by AM fungi

5.5  Ecological Function of AMF As it is well understood that agriculture is the largest connecting link between humans and environment, therefore stabilizing crop production and environmental integrity, in other sense sustainable crop production, is a major challenge for agriculture and future farmers (Robertson and Swinton 2005; Yadav et al. 2020). This shows that it is required to develop crop management strategies that optimize soil fertility, biological diversity and crop robustness (Altieri 1995) by creating forms of agroecosystems that respect natural ecological processes and support productivity in the long term (Altieri 1999). In this context, large number of ecological services provided by soil biota for sustainable crop production is extremely important (Smith and Read 2008). In particular, soil microorganisms that form symbiotic relationships with roots of the plant have become a researchable issue in agriculture because they provide a biological way to promote plant growth and reduce dependency on inputs in sustainable cropping systems (Hart and Trevors 2005). Regarding this, AM fungi as one of the important biotic components and key functional groups are profoundly effecting ecosystem processes that can contribute to the ecosystem services in

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In plant

Sucrose

Periarbuscular space

Glycogen

Hexose

Monosaccharide

TAG

NO3-

Amino acid

Pi

Pi

K

K

PPM

FPM

Transporter

Xylem

Glycogen

TAG

Fungal monosaccharide transporter Amino acid

PPM

ERM

Fungal cytoplasm

Vacuole

Phloem

Plant cytoplasm

In soil

NH4+ Amino acid

Pi K FPM

Fig. 5.5  Diagram showing nutrient exchange between AM fungi and host plant through periarbuscular space. (Adopted from Parihar et al. 2019b)

agroecology (Fig. 5.5). These ecosystem services offered by AM fungi will be discussed in coming sections and summarized below in Table 5.2.

5.5.1  Biotic Stress AM fungi results in alteration in the physiology of host plant by implying a reprogramming of functions in both the symbiotic partner which have a direct influence on plant ability to respond the biotic stress. Root colonization done by arbuscular mycorrhizal fungi (AMF) has been frequently reported to reduce the root infection by various soilborne pathogens (Azcón-Aguilar and Barea 1996; Zhu and Yao 2004; Khaosaad et al. 2007; Elsen et al. 2008), root parasitic plants (Akiyama et al. 2005; López-Ráez et  al. 2009a, b) and phytophagous insects (Guerrieri et  al. 2004; Koricheva et al. 2009). The correct mechanisms involved in this biocontrol are not clear, but localized and systemic-induced resistance (Cordier et al. 1998) as well as increase in plant P status in response to mycorrhiza formation (Graham and Abbott 2000) appears to be involved. The first mechanism followed by AM fungi could be the improvement in plant nutrition which works as a regulatory approach to manage or compensate the damage control. In addition to nutritional aspect modification, plant architecture, root exudation, interaction with other microbes and regulation of other defence mechanism may be responsible. Mycorrhizal plants have been reported with altered levels of various phytohormones such as salicylic acid (SA), ethylene (ET), jasmonates

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Table 5.2  Various ecological functions of AM fungi species studied in different crops Ecological function

Crops

References

Common bean

Al-Askar and Rashad (2010)

Fusarium wilt

AM fungi Biotic stress Glomus mosseae, G. intraradices, G. clarum, Gigaspora gigantea, Gigaspora margarita Glomus intraradices

Tomato

Panama wilt

Glomus mosseae

Banana

Rhizoctonia solani Meloidogyne incognita Early blight

Glomus sinuosum, Gigaspora albida Glomus coronatum

French bean

Srivastava et al. (2010) Mohandas et al. (2010) Singh (2011)

Funneliformis mosseae

Tomato

Basal stem rot

Glomus intraradices, Glomus clarum Glomus mosseae

Oil palm

Pigeon pea

Drought

Funneliformis mosseae, Glomus cerebriforme, Rhizophagus irregularis Funneliformis mosseae Rhizophagus irregularis Abiotic stress Glomus intraradices

Drought tolerance Waterlogging

Glomus versiforme, Paraglomus occultum Diversispora spurca

Sacha Inchi

Salinity tolerance

Rhizophagus intraradices, Claroideoglomus etunicatum and Septoglomus constrictum Septoglomus constrictum, Diversispora aunantia, Archaespora trappei, Glomus versiforme, Paraglomus occultum Glomus mosseae, Glomus microcarpum, Glomus fasciculatum, Glomus intraradices, Gigaspora margarita, Gigaspora heterogama Glomus intraradices

Maize

Fusarium root rot

Bacterial wilt Fusarium wilt

Neonectria ditissima

Drought tolerance

Salt stress

Saline-alkali

Balsam

Tobacco

Banuelos et al. (2014) Song et al. (2015) Sundram et al. (2015) Yuan et al. (2016) Dehariya et al. (2018)

Apple

Berdeni et al. (2018)

Maize and tomato

Bárzana et al. (2012) Tian et al. (2013a, b) Wu et al. (2013) Estrada et al. (2013)

Citrus

Maize

Armada et al. (2015)

Jatropha

Kumar et al. (2015)

Oat

Xun et al. (2015) (continued)

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Table 5.2 (continued) Ecological function Drought

Heavy metal stress Drought stress Cold stress

P N, P, K, Fe and Zn C, N, P and K

N and P

C, N and P N Macro- and micronutrients Cd Pb and Cd

Cd Cd, Cu, Pb, Cr, Zn and Ni Cu Coal mine tailings Coal mining

AM fungi Septoglomus constrictum, Diversispora aunantia, Archaeospora trappei, Glomus versiforme, Paraglomus occultum Glomus versiforme, Rhizophagus intraradices Glomus sp. Glomus versiforme Rhizophagus irregularis Nutrient management Glomus mosseae Glomus mosseae

Crops White clover

References Ortiz et al. (2015)

Lonicera japonica

Jiang et al. (2016) Li et al. (2019) Hajiboland et al., (2019)

Leymus chinensis and Hemarthria altissima Barley

Okra and pea Rice

Glomus spp.

Gliricidia, Leucaena finger millet, peanut pigeon pea Rhizophagus intraradices, Glomus Tomato aggregatum, Glomus viscosum, Claroideoglomus etunicatum and Claroideoglomus claroideum Funneliformis mosseae Apple Rhizophagus irregularis Funneliformis mosseae Chrysanthemum Diversispora versiformis morifolium Eight AMF species Wheat/faba bean Ecosystem restoration Glomus versiforme

Solanum nigrum

Funneliformis mosseae, Glomus versiforme, Rhizophagus intraradices Rhizophagus irregularis

Brassica chinensis

Funneliformis mosseae F. Caledonium Funneliformis mosseae and Rhizophagus intraradices Rhizophagus clarus, Acaulospora colombiana Funneliformis mosseae, Rhizophagus intraradices

Sunflower

Phragmites australis

Pepper Enterolobium contorstisiliquum Amygdalus pedunculata

Kumar et al. (2015) Hoseinzade et al. (2016) Balakrishna et al. (2017) Bona et al. (2017)

Berdeni et al. (2018) Wang et al. (2018) Ingraffia et al. (2019) Liu et al. (2015) Zhipeng et al. (2016) Wang et al. (2017a, b) Zhang et al. (2018) Ruscitti et al. (2017) dos Santos et al. (2017) Bi et al. (2018) (continued)

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Table 5.2 (continued) Ecological function Si

AM fungi Rhizophagus irregularis

C sequestration

Environmental protection Funneliformis mosseae

Crops Pigeon pea

References Garg and Singh (2018) Wang et al. (2016)

Nutrient leaching

Sp. not mentioned

Wild cherry, apricot, shiny leaf yellow horn, Cerasus humilis Tomato

N2O emission

–

Tomato

Greenhouse gas – emissions N2O emission Rhizophagus irregularis

Solanum lycopersicum Maize

Asghari and Cavagnaro (2012) Bender et al. (2015) Lazcano et al. (2014) Storer et al. (2018)

(JAs) and abscisic acid. These phytohormones found to be effective in defence mechanism through intricate regulatory network in plants (Pieterse et  al. 2009; López-Ráez et al. 2010). In addition to this, higher synthesis of insect antifeedant compounds and activation of defence-related genes in host plant have been reported in mycorrhizal plants compared to non-mycorrhizal (Gange 2007; Liu et al. 2007; Pozo et al. 2009). Pozo et al. (2009) have confirmed that AM fungi colonization upregulate the expression of defence gene which is managed or governed by JA and higher expression of JA signalling pathway enables mycorrhizal plants more resistant to necrotrophic pathogens and JA-susceptible insects (Pozo and Azcón-­ Aguilar 2007).

5.5.2  Abiotic Stress Agriculture production is severely constrained by various abiotic stress conditions such as salinity, drought, cold, heat and metal toxicity (Verma et al. 2017; Yadav et al. 2018; Saxena et al. 2013; Latef et al. 2016). To cope with the negative impacts of abiotic stress, the role of different plant biotic associations such as AM fungi is well known to improve overall plant growth and production using various mechanisms (Kaur et al. 2020; Singh et al. 2020). Contribution of AM fungi to improve overall plant performance is confirmed under various stress conditions including salinity (Abdel Latef and Chaoxing 2014; Hashem et al. 2014; Talaat and Shawky 2014; Borde et al. 2017; Fileccia et al. 2017; Parihar et al. 2019a), drought (Kapoor et al. 2013; Pagano 2014; Wu and Zou 2017), cold (Gamalero et al. 2009; Liu et al. 2013; Chu et al. 2016; Hajiboland et al. 2019), heat (Gavito et al. 2005; Zhu et al. 2012) and metal toxicity (Abdel Latef 2011, 2013; Nadeem et  al. 2014; Elhindi

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et al. 2018). Under abiotic stress condition, better plant growth by AM fungi inoculation can be ascribed to greater nutrient and water acquisition; higher photosynthesis and stomatal conductance; lower oxidative damage by enhancing various antioxidant enzymes such as catalase (CAT), superoxide dismutase (SOD), ascorbate peroxidase (APX), peroxidase (POD) and glutathione reductase (GR); and accumulation of osmolytes/osmoprotectants to maintain osmotic potential and modulate organic acid production in rhizosphere to maintain the soil chemical and nutrient condition, production of glomalin protein for aggregate stability, better water availability, etc. (Zhang et al. 2003; Rillig 2004; Wright 2005; Sheng et al. 2008; Porcel et  al. 2012; Evelin and Kapoor 2014; Hameed et  al. 2014; Pagano 2014; Talaat and Shawky 2014).

5.5.3  Nutrient Management The optimum soil nutrient availability is vital for plant growth, functioning of antioxidant defence system, enzyme synthesis, photosynthesis and many other important processes (Kour et al. 2020b; Rana et al. 2020b). Nutrient deficiency causes plant susceptibility to various stress conditions which result in stunted and poor plant growth. Plant-associated AM fungi improve the availability of various soil mineral nutrients having low mobility, i.e. phosphorus (P), zinc (Zn), copper (Cu), iron (Fe), manganese (Mn), etc. (Tarafdar and Marschner 1994; Ortas et al. 2001). Various studies revealed that lower phosphorus and nitrogen fertilization in soil found suitable for AM fungi development and to enhance the AMF-mediated macroand micronutrient concentration in plant tissue (Baslam et al. 2013; Xie et al. 2014). Smith et al. (2000) revealed that ~80% of the total P absorbed by Medicago truncatula was made available due to extraradical hyphae of AM fungi. Recently, characterization of high affinity transporter for various nutrients has been studied from physiological and molecular perspective. AM symbiosis induces the expression of Pi transporters MtPT4 and LjPT4  in Medicago truncatula and Lotus japonicas, ammonium transporter (AMT), sulphate transporters and plant K+ transporter to facilitate the respective nutrient transfer from the periarbuscular apoplast to the cortical cell (Guether et al. 2009; Kobae et al. 2010; Javot et al. 2011; Bapaume and Reinhardt 2012; Casieri et  al. 2013; Koegel et  al. 2013; Giovannetti et  al. 2014; Volpe et al. 2015). To improve the bioavailability of soil micronutrients to the plants, AM fungi could be a sustainable tool in nutrient biofortification programme. In addition to this, enrichment of macro- and micronutrient concentration enhances the crop quality for better food security. Moreover, AM fungi’s role in nutrient loss management has been reported in various studies. In a microcosms study, van der Heijden (2010) found that AMF symbiosis reduced 60% phosphorus and 7.5% ammonium leaching compared to the control plants. In another study, AM fungi mediated greater stomatal conductance and water uptake ability found to be effective to regulate N2O emission (Lazcano et al. 2014). Storer et al. (2018) reported that AM fungi suppress the growth of slow-growing nitrifiers and modulate the soil nitrification process.

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Moreover, denitrification process is complex and closely related with the availability of organic carbon, water regime and terminal electron (e−) acceptor sp., and AM fungi’s association with this process is needed to be investigated further.

5.5.4  Soil Health Management Soil health is defined as the capacity of the soil to maintain environmental quality, sustain biological productivity and promote animal, human and plant health (Doran and Parkin 1994; Kour et al. 2019a, b). AM fungi as important class of beneficial microbes improve the soil health by improving soil physical, chemical and biological health. AM fungi’s role in nutrient cycling and interaction with other soil-­ inhabiting microbes has already been described in the previous section. Soil physical health and its association with AM fungi can be described mainly by their aggregation stabilization ability. The greater soil aggregation ability is further explained by substantial amount of extraradical hyphae of AMF as dominant component of soil microbial biomass (Miller et al. 1995; Rillig et al. 1999) and the production of glomalin as an abundant and persistent extracellular protein by AMF hyphae (Wright and Upadhyaya 1996). Rillig and Mummey (2006) have described hierarchical model at various levels, i.e. plant community, root region and the mycelium biomass, to explain the AM fungi contribution to soil structure. It is well established that AM fungi influence the plant diversity and community composition which may differ in soil aggregation ability (Grime et  al. 1987; Klironomos 2000) due to their effects on net primary productivity which eventually controls net carbon accumulation in soil, as a strong determinate of soil structure. In another mechanism AM fungi invoke significant changes in root morphology and architecture which result in better soil aggregation via modulating root entanglement, soil water regime, rhizodeposition and root decomposition process (Smith and Read 1997; Augé 2001, 2004; Langley and Hungate 2003; Jones et al. 2004). Apart from indirect mechanism (plant and root), AM fungi itself influence the soil structure using their mycelium products, influencing soil biota and through biophysical mechanism such as enmeshment, alignment, and altered water relations. All these mechanisms do not occur in isolation but rather a complex interaction process which involves various factors in cycling way.

5.6  Potential Domain of AMF Application Potential of enhanced nutrient uptake (particularly phosphorus mobilization), drought tolerance, soilborne disease resistance, and building microporous soil structure has made AMF as an efficient natural biofertilizer. In the recent past, AMF applicability as a natural biofertilizer has been extended to various fields of agriculture, horticultural crops and agroforestry.

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5.6.1  Agriculture AMF colonizes within roots of plant and enhances growth to ensure high yield of crops, thus ensuring food security. Nutrient supply to the plant is one of the major functions of AMF.  Naturally grown crop under agroecosystem largely relies on mycorrhizae for nutrient supply in required amount for normal growth of the plant. Mycorrhizae indirectly play a crucial role in abiotic and biotic stress tolerance (Brundrett 1991). The presences as well diverse functionality of AMF have shown promises in agroecosystem productivity (Oehl et  al. 2003). AMF provides nutritional benefit to the associated plant in terms of P, N and different micronutrients like Zn, Cu, etc. under poor soil fertility conditions (Kayama and Yamanaka 2014). The phosphorus (P) is a highly immobile element in soil that renders inaccessibility to the plant roots resulting limited growth of plants. Mutualistic association of plant roots and mycorrhizae increases accessibility of P nutrient by the plants (Mosse 1973; Abbott and Robson 1982; Harley and Smith 1983). Additionally, water-use efficiency, drought, salinity, heat and rhizospheric pollutant stress have been known to improve by the use of AMF in plants (Aranda et  al. 2013; Maya et  al. 2012; Chandrasekaran et al. 2016; Bowles et al. 2016). Total fertilizer consumption on per unit area decreased by the use of AMF quantitatively particularly for phosphatic fertilizers (Charron et al. 2001; Ortas 2012). By reviewing several advantages of AMF in plant growth to soil reclamation, it is highly required to manage indigenous strain of AMF within field under poor fertile soils. Nutrient management under sustainable agriculture is inevitable, and AMF holds promise to fulfil the needs of sustainability against abiotic as well biotic stress. Application of AMF at large field level required mass production of AMF in large quantity and can be applied by spore coating over seed; further approach includes adopting indigenous AMF-promoting cultural practices (Roy-Bolduc and Hijri 2012; Vosátka et  al. 2012). Identification of indigenous host-specific even genotype-­specific strain, selection, cumbersome mass multiplication, and adaptive environment are the important bottlenecks regarding targeted AMF application in different crops and agroecological conditions in cost-effective manner. So far, various greenhouse studies on AMF conducted in different field crops and showed promising potential under different soil conditions to increased plant growth and enhanced nutrient uptake. There are various instances in which field crops have shown increased yield due to the use of AMF. Wheat seed coated with AMF showed reduced requirement of inoculum, cost-effectiveness and efficient approach of delivery of AMF in field condition (Oliveira et  al. 2016). Similarly field trial of wheat showed increased biomass of aboveground parts, harvest index, grain yield and good nutritional content in grain in AMF-treated plot (Pellegrino et al. 2015). A promising potential of yield advantage and enhanced nutrient uptake has been well proven in various field crops including cotton, soybean, maize, etc. (Mostafavian et al. 2008; Ortas 2012; Cely et al. 2016).

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5.6.2  Horticultural Crops Soil is a complex medium and harbours diverse fauna including beneficial and harmful. Harmful organisms like soilborne pathogen including fungus, bacteria and nematodes keep assaulting plant roots in hidden manner and ultimately reduce plant health and yield. Incidence of soilborne pathogen largely affects horticultural crops such as vegetables, fruits and ornamentals. Seedling or seed treated with AMF increases resistance to soilborne pathogens and reduces fertilizer requirements and cost of cultivation in horticultural crops. AMF (G. intraradices, G. versiforme and G. etunicatum) application in onion found to reduce soilborne pathogens, increased bulb quality, plant growth and tolerance against environmental stress (Aliasgharzad et  al. 2009; Bettoni et  al. 2014; Baum et  al. 2015). Mycorrhizae-treated tomato plants showed reduced phosphatic fertilizer requirements and increased seedling growths and biomasses (Sylvia and Chellemi 2001; Ortas et al. 2003). Commercial level of fruit cultivation requires high-quality seedlings in terms of vigour to sustain early stage of environmental and pathogenic stress after transplantation in the main field. To overcome the aforementioned challenges, AMF treatment becomes an important armour for the plants. In an investigation in citrus plant by using different AMF species, G. clarium showed positive increase in plant growth, nutrient uptake, plant biomass and plant height (Ortas et al. 2002). AMF-­ treated apple plant showed enhanced uptake of primary and secondary nutrients like N, P, K, S, Cu, Fe, Mn and Mo (Gastol et al. 2016). Plum faces one of the major challenges of salt sensitivity in transplanted field; AMF (G. mosseae) application found to compensate salt stress in rhizosphere (Zai et al. 2015). A greenhouse-based experiment suggested beneficial effect of AMF on enhanced nutrient uptake and increased growth by grapevine plants under different soil conditions. Ultisol showed high dependency on AMF in comparison with mollisols (Schreiner 2007). Similarly, in strawberry fruit yield increased upon AMF inoculation 90% in comparison to uninoculated trees (Sharma and Adholeya 2004). Phosphatase enzyme is directly known to be involved in assisting phosphorus acquisition by plants. Plants having higher phosphatase activity uptake less phosphorus and vice versa. AMF have been found affecting phosphatase activity in plant roots (Joner and Jakobsen 1995). Garcia-Gomez et al. (2002) reported higher activity of RAPA (root acid phosphatase activity) in Glomus claroideum in papaya plants.

5.6.3  Forestry Forestry sector always serves as a major renewable source on this planet contributing to the basic need of a country. Increasing productivity of forest on limited land availability to fulfil increasing demand requires efficient production technology applicable to diverse climate condition. The use of AMF in forestry sector has shown potential to increase productivity, profitability and sustainability. Forest tree

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mostly shows mycorrhizal association due to stable nature of ecosystem and long-­ term association within soil system. Forest land is a rich source of AMF diversity to find new strain. The application of AMF reduces the transplantation injury to saplings and improves the water and nutrient uptake (particularly P deficient soil) due to increased root surface area by mycelium. AMF has been found to increase Rhizobium nodulation in various leguminous trees by supplying adequate amount of phosphorus to the plant. Thus, AMF reduces additional requirement of adding chemical fertilizer in leguminous forest trees (Azcon et al. 1979; Hayman 1986). Additionally, AMF used in forest tree are known to reduce soil erosion and loss of nutrient by retaining soil nutrient ions and aggregating soil particle in rhizosphere zone. AMF inoculation in the root increases resistance to soilborne pathogens including Phytophthora, Pythium and Fusarium species causing root rot to the newly planted saplings (Dehne 1982). Due to several benefits of AMF use in forestry, treatment of saplings before tree plantation at main site should be made mandatory for establishing new forestry and afforestation.

5.6.4  Wasteland Management The management practices comprise of all types of physical, chemical and biological disturbances in the soil such as soil fertility, soil pH, microbial diversity and nutrient cycles that improve the degraded land productivity and restore the ecological integrity and sustainability of wasteland areas. AMF have a great potential in the recovery of disturbed lands and reclamation of wastelands. In addition to this, they also act as a stress alleviator by bioremediating soils polluted with heavy metals. For binding of soil particles and to improve soil aggregation and soil conservation, AMF’s role is very important (Dodd 2000). A mutual beneficial relationship that exists between arbuscular mycorrhizal fungi (AMF) and most of the vascular plants plays a very crucial role in enhancing soil fertility by producing glomalin that promotes soil stability and to boost up the microorganism growth (Johnson et al. 2002). This mutual relationship helps in acquisition of phosphorus (P) and other mineral nutrients from the soil and enhances host plant growth and development. Nicolson (1967) explained that AMF-incorporated wastelands help in effective plant growth. The absorptive surface area contributed by soil mycelium allows phosphorus uptake from a much greater volume. The growth of host plant is also enhanced particularly in phosphorus-deficient soils (Mosse 1973). AMF positively show to improve revegetation of coal mines, wastelands, road tracks and other disturbed sites (Jha et al. 1994). Nursery seedlings, pre-inoculated with AMF, would result in regeneration of flora in disturbed land (Rani et al. 1998a, b, 1999, 2001). Thus, besides providing nutritional advantage, AMF also provides possible resistance to low pH, heavy metal toxicants and high temperature to plants in association with.

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5.7  AMF Production and Globalization Widespread occurrence of AM fungi with natural plant species and rhizospheric soil system confines the pressing needs for the application of these naturally symbiotic fungi (Newman 1988). Broader application regime and growing scientific understanding improve the commercialization and implementation of AMF technology globally. AMF production as a multifarious procedure needs profit-oriented enterprises to create indispensable biotechnological proficiency and ability to counter permissible, educational, ethical and marketable demands (Pal et al. 2016). AMF products in markets are available in different forms such as granular, powder, liquid and tablet forms and formulation including liquid and solid type. These products are available in different sizes ranging from 5 to 20 mm of dusts to large blocks of several cubic centimetres and contain inert carrier material, i.e. charcoal, clay minerals (perlite, vermiculite, and bentonite), lignite, starch polymers, ground plant residues and dry fertilizers. Presently various companies are producing AMF inoculum across the globe with different formulations of varying species and different percentage of spore number and additive type. In the last couple of years, remarkable development has been recorded in the market producing AMF inoculum and allied services particularly in retail and wholesale sector. However most of the AMF-­ related production market dominated by privatively owned small firms and public information about their market share are very limited. According to a survey conducted by Chen et al. (2018), major AMF-producing companies are located in North America, Europe, Asia and Latin America (Fig. 5.6). India dominated in Asian region followed by China and had shown tremendous growth in the last decade. Overall the European market dominated in the production of mycorrhizal biofertilizer, and major firms were reported from the Germany, Italy, Spain, the United Kingdom, The Netherlands, France, Czech Republic, Belgium, Austria Estonia and Switzerland. The major domain of mycorrhiza application is in landscaping, horticulture crops, agro-farm, forestry, golf courses (in particular greens), restoration of degraded land, roof cultivation, soil remediation and research purpose (Chen et al. 2018). In fact, demand for organic food in developed nations is growing continuously, and application of AMF inoculum in this sector could provide resistance against pathogenic organism with possible restriction on the use of inorganic fertilizers, pesticides and fungicides. Similarly, farmers/growers of developing nations cannot afford recurring application of fertilization, and in that respect, single application of AMF inoculum in appropriate amount could do away with this problem. In spite of colossal potential of AM fungi, obstacles such as limited knowledge diffusion, poor consultancy services and lack of hope generators restricted the transforming of this idea into successfully venture.

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Fig. 5.6  Major AM fungi-producing countries (Germany (DE), Italy (IT), Spain (SP), the United Kingdom (UK), France (FR), and the Netherlands (NL)) and main domain of application (Chen et al. 2018)

5.8  Determinates of AMF Response in Agroecosystem Agriculture practices have significant impact on soil properties and microbial diversity which in turn influence various ecological processes and possibilities to develop a sustainable food production approach for growing population. Intensive agriculture practices may influence AM fungal distribution and abundance due to disruption of fungal hyphal network. However there are some contradictory results of land use on AM fungi and need to be revisited the functional implication represented by community difference. Therefore in this section, we will discuss in details about

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various agriculture practices and their influence on AMF and possible mechanisms to manage triangle relationship of plant-fungus-soil in best possible way.

5.8.1  Soil Fertility Mineral fertilizer applications are necessary and important practice for crop nutrition and replenish the soil nutrients pool removed or harvested by crops (Rana et al. 2019a, b). A high input management system reduces the plant’s dependency on AM fungi and subsequently their diversity and abundance (Egerton et al. 2007; Liu et al. 2012). Among different mineral nutrients, soil phosphorus seems to play the most significant role in regulation of plant fungal symbiosis (Lin et al. 2012; Kowalska et al. 2015). Recently, Cheng et al. (2013) found that higher P application reduces the root colonization and AMF diversity. However P application in nutrient-deprived condition and their lower application up to 20 Kg ha−1 may improve the mycorrhizal-­ mediated benefits to the plants (Al-Karaki 2002; Treseder 2004). Other than P, nitrogen fertilization also has direct and indirect influence on symbiotic intensity and observed that N application under N-limiting condition may enhance sporulation and root colonization. Moreover, Wang et  al. (2018) reported that under nutrient-­deprived condition as described previously, AMF can reduce N availability to plants and restrict the grain yield also. Under nutrient-enriched condition plant allocates less C to AMF and roots which ultimately effect the development of spore and hyphae production as more sensitive to fertilization (Marshcner et  al. 1996; Johnson et al. 2003; Tian et al. 2013a, b). Nitrogen application in soils where P is not limited generally results in a lower AMF extraradical biomass, while under P-deficient soils due to greater C allocation to AMF, N (Johnson et  al. 2003) enrichment improves AMF biomass in soil (Treseder and Allen 2002). In addition to mineral fertilizer, organic application had also observed both positive (Douds and Reider 2003; Borie et al. 2008; Wilson et al. 2009) and negative (Oehl et al. 2004; Treseder et al. 2007; Gryndler et al. 2008; Liu et al. 2014) impacts on AMF diversity. Further, Zhu et al. (2016) reported a significant correlation between organic matter and the AMF community composition resulting positive activation of AMF species to interact with other species in the maize rhizosphere. In conclusion, low input agroecosystem and organic nutrient may thus prove to be the best possible way to optimize the plant fungal symbiosis rather than long-term application of only mineral fertilizer (Kour et al. 2020d; Rana et al. 2020c).

5.8.2  Soil Tillage Tillage as a mechanical manipulation of soil is commonly followed in modern agriculture system. The basic idea to perform tillage is the residue decomposition and incorporation, levelling, seedbed preparation, management of post-emergence

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weeds and mixing of inputs such as manure, fertilizer and pesticide into the soil system. However extensive tillage may lead to soil and environmental degradation. The community composition of AM fungi is greatly influenced by land use types and agricultural management practices (Xiang et  al. 2014; Zhao et  al. 2015). Generally soil disturbance caused by tillage influenced the soil’s permeability, texture and microbial food substrates which ultimately affect the soil microbial activity and their habitat type (Wang et al. 2017a, b). In a direct way, tillage practices reduce the AMF hyphal extension, colonization rate and diversity structure (Anderson et al. 1987; Kabir 2005). In numerous studies, it has been found that conservation or no till improved the AMF diversity and abundance which results better plant growth (Boddington and Dodd 2000; Wetzel et al. 2014; Hu et al. 2015). Recently, a study conducted by Lu et al. (2018) reported that no tillage with crop straw return enhances the soil organic carbon by improving the extent of large macroaggregates which further positively correlated with soil AM fungal biomass (Qin et al. 2017). However, some studies exception to previous one revealed that continuous no till increases the soil bulk density and reduces the C utilization efficiency of soil microbes compared to conventional tillage system (Fu et al. 2000; Curaqueo et al. 2011; Schlüter et al. 2018). The variation in results might be due to difference in climatic and soil condition and duration of study.

5.8.3  Crop Rotation Crop rotation is a management strategy to maintain and improve the nutrient availability and soil health and minimize the pest and disease incidence to achieve the sustainable agriculture production. AM fungi as a key component of crop rotation reduce the crop dependency on fertilizer application by supplying 90% of phosphorus and 20% of nitrogen demands of the plants in exchange of photosynthetic fixed carbon (Smith and Read 2008). In addition to this, greater exploration of soil system due to extended hyphae of AMF enhances the inception of nutrients and reduces their leaching and other losses from soil system (Parihar et al. 2019b). The AMF abundance is usually found lower in bare or non-mycorrhizal crops including the Brassica family which produces antimicrobial isothiocyanates (ITCs) as a result of glucosinolate due to the decomposition of root residues (Paul Schreiner and Koide 1993; Kirkegaard et al. 2000). Inclusion of such non-mycorrhizal crops reduces the symbiotic benefits conferred to the crops, while just reverse effect was observed when mycorrhizal crops grow in rotation (Arihara and Karasawa 2000; Angus et al. 2015). Intercropping and crop rotation result in more diverse AMF assemblages and restrict some specific mycorrhizal species. Intercropping system is preferentially associated with different AMF species where various plant species grow simultaneously in similar condition. In a study, AMF spore density was recorded higher in maize crop than soybean (Troeh and Loynachan 2003), while legume intercropped with coffee has also given similar response (Colozzi and Cardoso 2000). Moreover,

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to maintain the higher number of AMF spore density and root colonization in maize crop, selection of soybean as preceding crops found suitable (Higo et  al. 2010). Recently, Bakhshandeh et al. (2017) explained higher wheat yield after the chickpea rotation compared to canola rotation is likely due to higher colonization of AMF rather than biological N fixation. Therefore to understand the complex relationship between crop plants and microorganism under field condition, our future research should be focused more on this for sustainable food production.

5.8.4  Use of Agrochemicals Variable responses have been reported following inorganic pesticide application ranging from positive to negative and neutral on AM fungi. The AMF persistence to pesticide will depend on pesticide application in preceding crops and postharvest herbicide treatment. Some in vitro studies revealed that fungicides such as flutolanil, azoxystrobin, fenpropimorph and fenhexamid hamper the spore germination of Rhizophagus irregularis; however after eliminating the fungicide stress, spores can germinate (B Zocco et  al. 2008; Buysens et  al. 2015). Fungicide generally applies as foliar method, and by using good agriculture practices, direct effect on AMF can be avoided. Contrasting to this, herbicide is mostly applied as pre- or post-­ emergence, and therefore, its exposure chances to AMF are higher. Mostly, herbicide concentration up to recommended dose exhibited neutral or positive results on AMF. In this context, some studies revealed that herbicide such as glyphosate was found suitable for AMF when used within prescribed rate in field (Malty et al. 2006; Pasaribu et al. 2011), while in the above recommended level, the direct inhibition of AMF species, i.e. Claroideoglomus etunicatum than for Scutellospora heterogama and Gigaspora margarita, is well reported (Malty et al. 2006). AM fungal symbiosis can be directly affected by active substances via root or hyphal uptake from the soil system or indirectly when pesticide treatment influences the metabolism of host plants (Hage-Ahmed et al. 2019). Interestingly, some species-specific response of different plant protection agrochemicals has been observed in various studies. In this regard application of oxamyl which is a systemic insecticide reduced the root colonization of Funneliformis mosseae but did not influence native Glomus sp. (Marin et al. 2002). Similarly, azadirachtin as a growth disruptor and feeding deterrent for many insects has shown negative effects on C. etunicatum and causes significant AMF community shift under field condition (Ipsilantis et al. 2012). Further glyphosate reduces the spore viability of F. caledonium and F. constrictum but not the F. mosseae and C. etunicatum (Druille et al. 2015) which reflect the specificity of various AMF strains as in the case of other agriculture practices (Jansa et al. 2002; Sale et al. 2015). The effect of pesticide on AM fungi is very much contradictory and ambiguous even when similar products were used, and these variations can be explained due to difference in application rate, mode, experiment duration, quantity and composition of substances, AMF sp.tested crop/plants and soil used.

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5.9  Conclusion and Future Prospects Despite the fact that AM fungi is the most frequent symbionts of natural land plants providing a large number of ecological services, very limited species have been identified so far. Advanced molecular tools revealed that total AMF diversity may be much larger than our actual database. Functional diversity of these different taxa may play an important role in deciding the plant productivity, diversity and ecosystem variability which need to be studied in details. Another important aspect is agriculture management practices that influence the symbiosis and thus related functioning/services. To minimize the negative effect of such agriculture practices, development of a suitable package of agriculture practices is required to enable the proper functioning of AMF. AMF diversity with optimum abundance is critical to induce maximum benefit to the host plant and to achieve this external application of AMF inoculum is necessary when our crop fields are having low viable propagules. Despite its growing trend, AMF commercial production and application are far behind from its full potential in developing country like India. In this regard, production of cost-effective inoculum in bulk amount using adequate quality standard or protocol with legislative intervention at governmental level is desirable to enhance their contribution in sustainable food production.

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Chapter 6

Endophytic Microbiomes and Their Plant Growth–Promoting Attributes for Plant Health Prachiti P. Rawool, Vikrant B. Berde, P. Veera Bramha Chari, and Chanda Parulekar-Berde

Abstract  Plant growth–promoting endophytic bacteria plays a major role in plant health. Endophytes are the group of microorganisms that inhabit plant, live inside the host microenvironment, receive protection from environmental stresses, and have greater access to nutrients with lesser competition from other microbes. Those bacterial endophytes that also offer some advantage to plants may be considered to be plant growth–promoting bacteria (PGPB) and can facilitate plant growth by a number of different mechanisms. Other attributes of the endophytes such as seedling emergence, plant growth, and protection of plant under adverse conditions are also known. The contribution of endophytes as biofertilizers is significant and this is due to its metabolic acclimatization within the host plant. Exploiting the usefulness of endophytic microorganisms for improvement of soil quality, plant growth promotion, phytoremediation, and reclamation of problem soils are the crucial reasons that will lead to the replacement of substantial agrochemical input in agricultural systems. Therefore, understanding of composition and functioning of plant associated microbial communities has a large probability of augmenting plant growth and restoration of soil quality. This chapter summarizes the effective role of endophytic microbiomes in growth promotion and the mechanisms involved in these interactions. Keywords  Endophytes · Health · Microorganisms · PGPR · Plant growth promotion

P. P. Rawool · C. Parulekar-Berde (*) Department of Microbiology, Gogate Jogalekar College, Ratnagiri, Maharashtra, India V. B. Berde Department of Zoology, Arts, Commerce and Science College, Lanja, Maharashtra, India P. Veera Bramha Chari Department of Biotechnology, Krishna University, Machilipatnam, Andhra Pradesh, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_6

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6.1  Introduction Agriculture is most common human activity that contributes maximally to the ever-­ growing demand for chemicals such as synthetic chemical fertilizers and pesticides, which eventually cause further environmental hazards and in turn risks to human well-being. One example is that of nitrous oxide (N2O), a chemical pollutant that is a result of excessive use of nitrogen fertilizer and is a main source of greenhouse gases causing global warming. In addition to this, nitrogen fertilizers decrease the rate of nitrogen fixation in the soil. Application of fertilizers such as ammonium nitrate in high concentration results in ample amount of ammonium availability in the soil for plant growth. As a result, the plants do not depend on symbiotically associated microbes and this affects symbiotic associations. Due to the presence of high concentrations of ammonium, nitrate production by nitrifying bacteria increases. The nitrates are further converted to N2O by denitrifying bacteria. The unutilized nitrates leach out in the water sources (Galloway et al. 2008; Butterbach-­ Bahl et al. 2013). For the development of sustainable agricultural, crops should have properties such as disease resistance, salt tolerance, heavy metal stress tolerance, drought tolerance, and nutritional value. To equip these phenotypic properties, use of plant endophytes as well as soil microorganisms such as bacteria, fungi, and algae can be done, which will increase the nutrient uptake capacity of plants as well as increase their water uptake efficacy (Armada et al. 2014).

6.2  Plant–Microbes Interaction For plant growth, development, and soil health plant–microbes interaction is the vital key. Generally, plant–microbes interactions of three kinds have been identified, that is, epiphytic, endophytic, and rhizospheric (Verma et al. 2017b; Yadav et al. 2020). An understanding of plant microbiome and their beneficial attributes could have multiple benefits toward sustainable agriculture (Yadav et al. 2018a). Microbial diversity plays a very important role in the maintenance of sustainability in agriculture (Yadav et al. 2017b). Endophytic bacteria are abundant in most plant species, found in plant tissues. The endophytic microbes are colonized in the interior part of the plant such as root, stem, or seeds without any destructive effect on host plant. The word endophyte meaning ‘in the plant’ and is obtained from the Greek words endon means ‘within’ and python means ‘plant’ (Yadav et al. 2017a). Several definitions have been developed for endophytic bacteria; endophytes are those bacteria that can be isolated from plant tissue that are initially surface-­ sterilized and then extracted using suitable solutions (Verma et al. 2017b). Recently, endophytic bacteria are believed to be responsible for beneficial effects on host plants, such as plant growth elevation and improved resistance against pathogens and parasites. A large number of endophytic microbial species including Achromobacter, Azoarcus, Burkholderia, Collimonas, Curtobacterium,

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Enterobacter, Flavobacterium, Gluconoacetobacter, Herbaspirillum, Klebsiella, Microbiospora, Micromomospora, Nocardioides, Pantoea, Planomonospora, Pseudomonas, Serratia, Streptomyces, and Thermomonospora have been reported from different host plants (Rana et al. 2019b; Suman et al. 2016; Yadav et al. 2019b). The plant growth–promoting rhizobacteria (PGPR) are the most useful for the growth and development of plants. The microbial activity around the roots of plants, that is, the rhizosphere, is influenced by the release of exudates. Most of the rhizosphere bacteria are either free or may be attached to the root surfaces. A number of microbial species belonging to different genera Acinetobacter, Alcaligenes, Arthrobacter, Aspergillus, Azospirillum, Bacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Halobacterium, Halococcus, Haloferax, Penicillium, Pseudomonas, Rhizobium, and Serratia are mostly found associated with rhizosphere of different crop plants (Kour et al. 2019d; Yadav et al. 2015b, 2017c). These bacteria promote plant growth directly by making certain nutrients available to the plants or by helping in defense mechanism. Nowadays development in genomics and in classical microbiology techniques aids to develop the science of plant– microbe interactions. The use of these natural symbionts such as endophytes as well as rhizosphere bacteria offers an opportunity to increase crop productivity while decreasing the environmental impacts of agriculture.

6.3  Plant-Associated Bacteria The rhizosphere is the region of activity as compared to soil further from the roots of the plants. This activity is due to the exudates of the plant roots that attract number of microorganisms toward it (Hiltner 1904). This phenomenon is called as the ‘rhizosphere effect’. The rhizosphere as described by Dobbelaere et al. (2003) is a narrow zone, rich in nutrients due to the build-up of a range of plant exudates, such as organic acids, phytosiderophores, sugars, vitamins, amino acids, nucleosides, mucilage, which serve as nutrients for bacteria (Gray and Smith 2005; Ahemad and Kibret 2014; Hasan et al. 2014). The major advantages of these bacteria to the host plant are as follows: (a) They provide nutrients to crops, which the crops are unable to avail. (b) They improve plant growth by producing hormones responsible for plant growth enhancement. (c) They provide protection to the plants by producing compounds that reduce or inhibit the activity of plant pathogens. (d) They help to improve soil structure through their activity. (e) They play a role in the bioaccumulation or leaching of inorganic compounds (Davison 1988; Ehrlich 1990; Kour et al. 2019d; Yadav et al. 2018b). So, these advantages of PGPR help in plant growth promotion and based on the above properties, the selection criteria for good PGPR may be enlisted as high competence in rhizosphere against other bacteria, having broad spectrum of action against plant pathogens, should have ultraviolet tolerance and should be non-pathogenic to plants as well as humans (Calvo et al. 2014; Glick 2012).

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PGPR can also be termed as plant health–promoting rhizobacteria (PHPR) or nodule-promoting rhizobacteria (NPR). The rhizosphere bacteria that have ability to attach to the surface of the roots may enter the root hair and localize in different tissues of the plant organs (Khan 2005). This is a kind of symbiotic association seen between the bacteria and host plant. These bacteria are called the endophyte. Both bacteria and fungi have the ability to colonize the plant internally. Research on fungal endophytes in various plants has progressed significantly. Fungal species that were majorly reported as endophytes in agricultural crops include Acremonium, Alternaria, Arthrobotrys, Aspergillus, Beauveria, Chaetomium, Cladosporium, Cladosporium, Colletotrichum, Curvularia, Epicoccum, Fusarium, Gilmaniellas, Paecilomyces, Penicillium, Saccharomyces, Scolecobasidium, Trichoderma, and Xylaria (Rana et  al. 2019b; Suman et  al. 2016; Verma et  al. 2017a; Yadav 2019; Yadav et al. 2019a).

6.4  Mode of Action of PGPR Plant microbe interactions are symbiotic in which costs and benefits are shared by both of them. There are two modes of action of PGPR on plant growth, direct and indirect mechanism. The direct mechanism includes nitrogen fixation, phosphate solubilization, phytohormone production, and providing iron for plant growth (Glick 1995). The indirect mechanism involves the protection of the plant from plant pathogens by producing antimicrobial compounds (Glick 1995). Bacteria that are involved in protecting the plants are often referred to as biocontrol agents (Beattie 2006). Activities included in indirect mechanism, responsible for protection by reducing the severity of diseases and also exhibiting antagonism, are as follows: synthesis of hydrolytic enzymes such as chitinases, glucanases, proteases, and lipases; competition for nutrients and suitable colonization of niches at the root surface: regulation of plant ethylene levels; production of siderophores and antibiotics (Neeraja et al. 2010; Maksimov et al. 2011). A mechanism called as herbivory is reported (Parisi et  al. 2014). Production of alkaloids by endophytes is responsible for this effect. This effect was observed in case of the plant Trifolium repens when growing in the vicinity of Lolium multiflorum. The incidence of aphid infection in was reduced Trifolium repens due to alkaloid production by endophyte of plant Lolium multiflorum, Neotyphodium occultans. This is a type of associative protection of non-host plants by production of hostile volatile compounds by endophytes of neighboring plants. Due to changes in host-volatile compounds, this indirect effect is observed.

6.4.1  Direct Mechanism The direct mechanism of PGPR includes nitrogen fixation, phytohormones production, phosphate solubilization and increasing iron availability. The influence of each of the direct methods on plant growth varies with from species to species as well as

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strain to strain. Mineral uptake is enhanced due to increased influx of mineral ions at the root surfaces (Bertrand et al. 2000). Arshad and Frankenberger (1998) reported the influence of PGPR growth regulators, on the physiological and morphological properties as well as metabolism of plant, at very low concentrations. 6.4.1.1  Phytohormone Production Phytohormones are the chemicals that influence plant growth at low concentration. Plants reduce the effects of stresses on growth by producing phytohormones and adjusting their levels (Salamone et al. 2005; Glick et al. 2007). Auxins are produced by several rhizobacterial genera, for example, Azospirillum, Agrobacterium, Pseudomonas, and Erwinia (Costacurta and Vanderleyden 1995; Yadav et al. 2018a). Indole-3-acetic acid (IAA) is one of the most common as well as the most studied auxins (Spaepen et al. 2007). It is involved in cell division, cell elongation, differentiation, and extension. It is responsible for cell wall extension in young stems as well as auxiliary bud and bud formation. Further, IAA also plays a crucial role in leaf and flower abscission. Soil bacteria or PGPR contributes to the pool of IAA along with the plant and thus interferes with developmental process of plant (Glick 2012). Plants produce ethylene endogenously and it induces different physiological changes in plants at molecular level. Ethylene is a stress-induced hormone that can inhibit plant growth. Ethylene levels are controlled by 1-aminocyclopropane-1-­ carboxylic acid (ACC)-deaminase-producing microbes and these ensure that ethylene levels stay below the point where growth is impaired. Thus, ethylene is a crucial regulator of the bacterial colonization of plant tissues, which suggests that the ethylene inhibiting effects of the enzyme ACC-deaminase may be a microbial colonization strategy. Microbial strains exhibiting ACC deaminase activity have been identified in a wide range of genera such as Acinetobacter, Achromobacter, Agrobacterium, Alcaligenes, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Ralstonia, Serratia, and Rhizobium (Kour et al. 2019b; Rana et al. 2019a; Verma et al. 2017b). 6.4.1.2  Sequestering Iron Plants and bacteria both require iron for growth and bacteria have developed iron uptake systems which involve siderophores production. Siderophores chelate iron by the formation of soluble Fe3+ complexes. However, machinery of siderophores is active only under low iron availability. The siderophore-producing ability of rhizobacteria also contributes to antibiosis, as proved by number of studies (Maksimov et al. 2011; Crosa and Walsh 2002; Andrews et al. 2003). The active transport system through the membrane commences with the recognition of the ferric-­siderophore by specific membrane receptors of Gram-negative and Gram-positive bacteria (Boukhalfa and Crumbliss 2002). Siderophores can chelate ferric ion with high affinity following which it can be solubilized and extracted from most mineral or organic complexes (Wandersman and Delepelaire 2004).

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6.4.1.3  Nitrogen Fixation Nitrogen fixation is the conversion of atmospheric nitrogen into utilizable nitrogen that is converted to ammonia. Nitrogen-fixing microorganisms, widely distributed in nature, carry out biological nitrogen fixation (Raymond et al. 2004). These bacteria harbor the nitrogenase complex, the enzyme which is responsible for the process of N2 fixation. The nitrogenase gene (nif) encodes the nitrogenase enzyme, which is inactive in the presence of oxygen. A variety of bacterial species belonging to genera Azospirillum, Alcaligenes, Arthrobacter, Acinetobacter, Bacillus, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Pseudomonas, Rhizobium, and Serratia can bring about nitrogen fixation in the plant rhizosphere and exert beneficial effects on plant growth (Tilak et al. 2005; Yadav et al. 2017a). 6.4.1.4  Phosphate Solubilization Phosphorus is an essential nutrient for plant growth. However, phosphorus is present in insoluble forms, mostly and hence not available to plants (Kour et al. 2019c). Thus, solubilization and mineralization of phosphorus by phosphate-solubilizing bacteria (PBS) are a very important property from plant growth promotion point of view. PBS produces low molecular weight organic acids that solubilize inorganic phosphorus to soluble form. Conversely, phosphorus present bound in organic forms can be released by catalyzing the hydrolysis of phosphoric esters, which causes mineralization of organic phosphorus (Yadav et  al. 2015b). This may be made available to the plants. Interestingly, both phosphate solubilization and mineralization can co-occur in the same bacterial strain (Tao et  al. 2008). Bacillus, Rhizobium, and Pseudomonas genera are among the most efficient phosphate solubilizers (Verma et al. 2016; Yadav et al. 2015a). Within Rhizobia, two species nodulating chickpea, Mesorhizobium ciceri and Mesorhizobium mediterraneum, are reported to have very good phosphate solubilizing activity (Rivas et al. 2006).

6.4.2  Indirect Mechanism Indirect mechanism involves the ability of PGPR to reduce the deleterious effects of plant pathogens on the growth. This is achieved by various mechanisms. 6.4.2.1  Antibiotic Production and Lytic Enzyme This involves synthesizing the lytic enzymes such as chitinases, cellulases, 1,3-­glucanases, proteases, and lipases. Several antibiotics are also secreted in order to destroy the plant pathogens. However, the action of antibiotic compounds being specific, the producers cannot be relied upon completely. The PGPR having ability to produce more than one antibiotic compound is preferred for use as antagonistic

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agents (Glick et al. 2007). The antagonistic compounds are low molecular weight compounds that retard the growth of pathogen by interfering with its metabolism. 6.4.2.2  Induced Systemic Response (ISR) There is another mechanism called induced systemic resistance (ISR), which shows increased resistance at particular sites of plants, at which induction had occurred (Van Loon et al. 1998). Verhagen et al. (2004) have reported the production of jasmonate and ethylene which are plant hormones and formed as ISR to range of plant pathogens. It is a nonspecific response. Similarly, siderophores are also produced in response to certain plant pathogens. These sequester iron and make it unavailable for the pathogens, due to having higher affinity for iron than the pathogens (Schippers et al. 1987). Rhizobacteria-mediated ISR is similar to pathogen-induced systemic acquired resistance (SAR) as in both cases, uninfected plant parts gain more resistant to plant pathogens (Van Wees et al. 1997; Van Loon et al. 1998). Induction of SAR is through salicylic acid (SA) and ISR requires jasmonic acid (JA) and ethylene (ET) signaling pathways (Van Loon et al. 1998). These molecules act like signaling molecules that can induce resistance and are actually involved in coordinating the defense responses (Ryals et al. 1996). The resistance facilitated by ISR is considerably less than that gained by SAR (Van Loon et  al. 1998) and a dependence on plant genotype is observed in the generation of ISR. Hence, ISR and SAR are both required for complete protection as they give an added effect in presence of each other (Van Wees et al. 2000). 6.4.2.3  Hydrogen cyanide Production Bacteria-producing Hydrogen cyanide have an application as biocontrol agents. Cyanide being toxic is produced by most microorganisms including bacteria, algae, fungi, and plants as a means of survival by competing with weeds. Rhizobacteria produces Hydrogen cyanide that has a deleterious effect on the weeds growing on plants. The host plant is unaffected by the bacteria or the Hydrogen cyanide produced by it. Thus, it serves as a weed control agent. Pseudomonas and Bacillus species are also known to produce Hydrogen cyanide (Kour et  al. 2019a; Verma et al. 2019). Suslow et al. (1979) reported the PGPR producing Hydrogen cyanide to inhibit the proper functioning of enzymes and also inhibit the action of cytochrome oxidase 6.4.2.4  Competition The rhizosphere of plant contains bacteria that depend on the plat exudates and other nutrients supplied by the plants, which are in trace amounts. Non-pathogenic microbes in the rhizosphere utilize the nutrients available and colonize the root

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surfaces, hence preventing the colonization of pathogenic microorganisms. Thus, this competition indirectly protects the plant from pathogen colonization and eventual infection. 6.4.2.5  Antibiotics The basis of antibiosis, activity of biocontrol based on secretion of molecules that kill or reduce the growth of the target pathogen, has become better understood over the past two decades (Dowling and O’Gara 1994; Whipps 2001; Lugtenberg and Kamilova 2009). The production of one or more antibiotics is the mechanism most commonly associated with the ability of plant growth–promoting bacteria to act as antagonistic agents against phytopathogens (Glick et  al. 2007), for example, Pseudomonas, besides siderophore production, aggressively roots colonization, induction of systemic resistance in the plant, and production of antifungal antibiotics (Haas and Keel 2003). Biocontrol Agents Induced Resistance (ISR and SAR). The inducing rhizobacteria and the pathogens were inoculated, kept confined, and spatially separated on the same plant so that microbial antagonism was excluded, and the protective effect was plant mediated.

6.5  Plant Growth Enhancement by PGP Microbes PGP microbes plays crucial role in augmenting plant growth through wide-ranging mechanisms. The mode of action of PGPR that promotes plant growth includes the following: 1. Abiotic stress tolerance in plants 2. Nutrient fixation for easy uptake by plant 3. Plant growth regulators 4. Siderophores production 5. Volatile organic compounds production 6. The production of protection enzyme such as chitinase, glucanase, and ACC-­ deaminase (Choudhary et al. 2011) However, the mode of action of different PGPR varies depending on the type of host plants. Plant growth is influenced by a variety of stresses due to the soil environment, which is a major constraint for sustainable agricultural production. Two groups of stresses are described: biotic and abiotic. Biotic stresses include archaea, viruses, fungi, bacteria, nematodes, and insects, while abiotic stresses refer to the content of heavy metal in soils, nutrient deficiency, high and low temperature, drought, salinity, etc.

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6.5.1  Abiotic Stress Tolerance in Plants Abiotic stresses are mainly responsible for agricultural yield reduction and depend on soil type and plant factors. Despite these facts, application of PGPR can help reduce the stress (Kumar et al. 2019). PGPR could reduce the toxic effects of cadmium pollution on barley plants due to their ability to bind to cadmium and remove it thereby reducing the concentration in the soil (Pishchik et al. 2002). In the presence of PGPR, plants under abiotic stress conditions of salinity and drought showed improvement in leaf water status. Sarma and Saikia reported that Pseudomonas aeruginosa strain has improved the growth of Vigna radiata (mung beans) plants under drought conditions. The water utility by plants depends upon the stomata, thus balancing the water content of leaf and uptake by roots (Sarma and Saikia 2014).

6.5.2  Nutrient Availability for Plant Uptake Plant nutrients are made available by the activities of PGPR in the soil. PGPR activities such as nitrogen fixation and phosphate solubilization help in making nutrients available for the host plant. Fixation of nutrients prevents the leaching out of these nutrients, which goes unutilized. Nitrogen fixation helps in making available atmospheric nitrogen to the plants in organic forms that can be assimilated by plants. Azotobacter sp., Azospirillum sp. are examples of nitrogen fixers, associated with crop plants. Similarly, phosphate solubilizers make available inorganic phosphorus that is unavailable for plants, by solubilizing it to organic form. Kocuria turfanensis strain 2M4 isolated from rhizospheric soil was found to be a phosphate solubilizer, an IAA producer, and a siderophores producer (Goswami et al. 2014).

6.6  C  hallenges in Selection and Characterization of PGP Microbial Strains Soviet Union in 1958 pioneered the process of applying Rhizobacteria in soil and plant parts to eradicate bacterial and fungal pathogens (Suslow and Schroth 1982). Selecting the strain is crucial so that the most beneficial bacteria are screened for the experiment to be successful. For this reason, effective strategies need to be considered. Primary screening of PGPR from the isolated lot, having the required properties, can be done based on physiological, nutritional, and biochemical characteristics as described by Holt et al. (1994). Compant et al. (2005) have reported mass screening technique for the selections of effectual PGPR strains. Bowen and Rovira (1999) have suggested criteria such as host plant specificity, adaptability to a particular soil, climatic conditions, or pathogens, to be considered in selecting the isolation methods. Antibiotic production, siderophores production,

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and root colonization are other traits that can be basis for selection. Thus, selection of most effective strains can be facilitated by the development of high throughput assay systems and useful bioassays (McSpadden Gardener and Fravel 2002). The agriculture scenario is changing slowly with the replacement of chemicals by organic farming methods which promote the use of PGPR-based bioformulations. The last decade has witnessed lot of research on PGPR isolation and inoculation of PGPR into rhizosphere for enhanced growth and yield of wide range of crop plants, the molecular mechanism of action of these microbes as well as the biotechnological approach to modify PGPR for better yield and sustainability (von der Weid et  al. 2000). Here we witness the application of nanotechnology to PGPR research, but cost-effective and quality nano-product is still expected. Bulk of research is limited either to laboratory or greenhouse scale and needs to come out on a larger scale and reach the stakeholders. Research on PGPR should be focused on microbiome interactions especially their diversity, effect of environmental stresses on microbiome, technologies such as rhizo-engineering, nanotechnology and metaproteomics for better formulations, different formulations, field experiments, cost-effective formulations with good shelf life, farmer education about PGPR biofertilizers, and so on.

6.7  Conclusion and Future Prospects PGPR-related awareness has resulted in the achievement of sustainable agriculture and maintaining the plant health against biotic and abiotic factors. Future research should concentrate on in-depth study of plant–microbe interactions, for example, innovative improvements in root environments, particularly with respect to their mode of action and adaptability to conditions under extreme environments. Genetic engineering, rhizo-engineering, and metatranscriptomics, use of safest bacteria-­ based silver nanoparticles to introduce new formulation and screening of bacterial strains through molecular techniques such as proteomics and docking methods will be the focused area of researchers in the coming years. PGPR used as fertilizer by traditional methods is not most effective because 90% are lost to the air during application and thus they affect application costs to the farmer but nanoencapsulation technology could be used to protect PGPR and thus enhancing their service life and dispersion in fertilizer formulation and allowing the controlled release of the PGPR. Another major aspect is the handover of this product information via local farmers training along with information about handling of PGPR. So PGPR will be evolved as a potent alternative to chemical fertilizer in an eco-friendly manner and in sustainable development and will be accepted in agriculture, horticulture, silviculture, and environmental clean-up strategies. Acknowledgment  The authors are grateful to their educational institutions for support.

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Chapter 7

Diversity and Biotechnological Potential of Culturable Rhizospheric Actinomicrobiota Sudipta Roy, Hiran Kanti Santra, and Debdulal Banerjee

Abstract  The interface of plant root and soil is the most active region where major parts of maximum number of cycles occur that leads to the accumulation of diverse chemicals of microbial origin. Soil is one of the most diverse terrestrial ecosystems. Within soil, rhizosphere is the most active fraction where interaction between biotic and abiotic components attracts enumerable microorganisms. Thus rhizosphere becomes the important hotspot of biotechnological interest. The root secreted compounds play significant roles either as chemo attractants or as repellants in the rhizospheric region immediately surrounding the root system. Plant root exudates are able to control the soil microbial community in their immediate proximity; interact with herbivores, i.e., primary consumers; encourage positive interactions like beneficial symbioses; influence some physicochemical soil parameters; and also restrict the growth of competitor species. Root-microbe cross talk are either positive, i.e., mutualistic to the plant, or negative, i.e., antagonistic to the plant species. Members of phylum actinobacteria are widely distributed in nature and have been isolated from several extreme environments (drought, high temperatures, pressure, pH, salinities) and are associated with plants growing in different habitats. Actinobacteria are of agricultural importance as they can promote plant growth and improve nutrition of plant by direct plant growth-promoting mechanisms, like fixation of nitrogen; solubilization of phosphorus, potassium, and zinc; production of plant growth promotors; and ACC deaminases, or by indirect mechanisms such as the production of ammonia, antibiotics, hydrogen cyanide, lytic enzymes, and siderophores. Keywords  Actinobacteria · Diversity · Rhizosphere · Soil

S. Roy · H. K. Santra · D. Banerjee (*) Microbiology and Microbial Biotechnology Laboratory, Vidyasagar University, Midnapore, West Bengal, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_7

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7.1  Introduction Plant roots are known to be the most vital part of the plant as they perform numerous functions including anchorage on soil and accumulation, uptake of vital macro- and micronutrients with water which is a first and foremost need for growth. The interface of plant root and soil is known to be the most active portion, and it harbors a huge diversity of microbial flora ranging from fungus to action-bacteria. The biochemical processes happening here has a large role in regulating the biogeochemical cycles as it is the store house of decomposers. These processes have direct effect on plant growth and also the composition of the microbial community in a variety of ecosystem level processes (van der Heijden et al. 1998; Wardle et al. 2004; Berg and Smalla 2009). Actinobacteria represent a huge proportion of the soil microbiota and are designated as the most important beneficial flora among the rhizospheric population. Actinomycetes are the producers of large number of natural bioactive compounds especially antibacterial antibiotics. Till now approximately a number of 10,000 antibiotics have been known and almost 50% of them are from Streptomyces that populates in the soil (Lazzarini et al. 2000). In recent past the rate of isolation of novel or unique actinobacterial species from rhizosphere is slow. So emphasis is given on the effective isolation of those species from regions of extreme environments like marine salty habitats, thermal hot spring, and hydrothermal vents (Rastegari et al. 2020b; Singh and Yadav 2020). These extremophilic actinobacteria with their tolerant extremozymes can be a new area of actinobacterial research. They are also found as endophytes in nature colonizing plants and being free-living they can colonize almost any surface of the earth.

7.2  Soil and Rhizosphere Soils are basically composed of a large variety of organics and minerals forming a complex mosaic of microenvironments (Ranjard and Richaume 2001). Soil is one of the most diverse terrestrial ecosystems. Rhizosphere in soil is the most active fraction where interaction between biotic and abiotic components attracts enumerable microorganisms and thus becomes the rich hotspot of biotechnological interest (Kumar et al. 2019; Rajawat et al. 2020). Efforts are being made to face the global climate change and escalating global population that might unavoidably necessitate higher productivity of energy, food, feed, and fiber on less optimal lands even on infertile domain (Tilman et al. 2002; Yadav et al. 2020). A better understanding and management of rhizospheric processes will help to meet these horrible global demands of climate change and population growth (Kour et  al. 2020c; Rastegari et al. 2020a). Productivity cannot be described only by the plant growth per hectare in the agriculture field but defined by the food production, fitness, and also healthy development of plants (Boyer 1982; Edgerton 2009). Healthy soils are always a fundamental factor for better agroproduction and, so, an important support for

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accomplishing food security for the present and future (Kour et  al. 2020d; Rana et  al. 2020c). Some soil-dwelling microbes execute an array of valuable eco-­ functioning (nutrient cycling, carbon storage, and soil remediation), thus enhancing plant growth as well as vigor results higher productivity (Daily et al. 1997). The specific region of soil that interacts with plant root is colonized by a diverse population of microorganisms. This is so far evidenced that Lorenz Hiltner was a German agronomist and plant physiologist who have first coined the name “rhizosphere” in 1904 to demonstrate the segment of the most dynamic plant-root interface. This word belonged in part from the Greek word “rhiza,” signifying root (Hiltner 1904; Hartmann et al. 2008). Rhizosphere is the segment of soil surrounds a plant root where an exclusive population of microorganisms with comparatively higher population density is found. Studies have shown clearly that such interesting phenomena are constantly induced by the chemicals released from plant roots (Fitter 1996; Estabrook and Yoder 1998; Yoder 2001). After careful observation and thorough scientific investigations, the rhizosphere region has been refined into three separate zones according to their relative proximity to root with distinct characteristics found. The outer most layer of plant root including the cortex and endodermis, where the free space (apoplastic space) is dominantly occupied by microbes, is called endorhizosphere. The medial zone, right adjacent to the root system including epidermis and mucilage, is the rhizoplane. Extending from the rhizoplane toward the bulk soil is the ectorhizosphere. So, the rhizosphere does not bear any definite size or shape, but it can have a gradient in root exudates and biological and physical properties that can change both radically and longitudinally along the roots.

7.3  R  oot Exudates in Connection to Rhizospheric Microbial Community Plant roots are remarkable system exerting tremendous pressure which is nearly 7 kg/cm2 or ~100 psi at its growing tip point just to push their way into the soil. Survival of any plant within rhizosphere depends primarily on its ability to respond to the changes in the local environment that certainly require a specific adaptation. Principally the cells of root cap and epidermis secrete mucilage, a viscous, insoluble, high molecular weight, and polysaccharide-rich material during root tip growth within soil, thus lubricating and protecting itself. Such organics also contribute in desiccation tolerance, assists in acquisition of nutrient, and also helps in aggregating soil particles, thus improving soil quality by mounting water permeation and soil ventilation (Bengough and McKenzie 1997). Even it is surprising that the cell linings that are sloughed off continue to secrete mucilage for several days to attract beneficial microorganisms and also sequester many toxic metal ions (Hawes et al. 2000). The chemicals secreted by roots into the soil are broadly recognized as root exudates. Root exudates are thought to be secreted due to osmo-difference root cells

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and soil environment or due to autolysis of epidermal and/or cortical cells. The released compounds belong to a wide range of molecular weight though the lower molecular weight compounds (LMW) are our prime interest that includes amino acids, organic acids, proteins, phenolics, sugar, and other secondary metabolites which are generally utilized by microorganisms. The root-secreted compounds play significant roles as chemoattractants or repellants in the rhizospheric region immediately surrounding the root system (Estabrook and Yoder 1998; Bais et al. 2001). Plant root exudates may control the diverse soil microbial community in their immediate proximity, interact with herbivores, encourage beneficial symbioses, influence some physicochemical soil parameters, and also restrict the growth of competitor species (Nardi et al. 2000; Kaur et al. 2020; Singh et al. 2020). The plant root exudates account for nearly 5–21% of all photosynthetically fixed carbon being transferred to the rhizosphere through root (Clarkson and Marschner 1995). The rhizosphere which is colonized by microorganism and other living creatures at significantly higher density always shares a tough competition for both shelter and food. In this regard root microbe interaction is a major subject of understanding to explore the localized microbial population as well as their exploration of their biotechnological potential (Yadav et  al. 2017a; Yadav and Yadav 2019). Root-­ microbe cross talk are either positive, i.e., mutualistic to the plant, such as the association of epiphytic microbes and endophytic association such as mycorrhizal, root nodule nitrogen-fixing bacteria, or antagonism to the plant species, including parasitism and pathogenicity (Saxena et al. 2016; Verma et al. 2016).

7.3.1  Root Microbe Cross Talk Root exudates or better to say rhizo deposits make the rhizosphere an attractive habitat for microbial colonization and proliferation. A 10 gm of fertile soil contains 1000–2000 times more number of microorganisms than human population in earth that accounts to about 1010–1012 cells per gram of soil making it a pretty swarming niche. Root-microbe communication is an important phenomenon to characterize the whole dynamic process underground. Root exudates act as inducers to communicate and enhance a wide variety of biological and physical interactions between roots and soil-dwelling microorganisms (Kour et  al. 2020b; Rana et  al. 2020b). Most individuals of the rhizospheric microbiome are belonging to diverse food web utilizing various complex nutrients released by the plant roots. Root and root hair cells are delicate in nature and are devoid of any physical protection but they are continuously exposed to invading microorganisms which are pathogenic in nature and may cause temporary or permanent damage to the plant tissues. Roots secret a various combination of chemicals i.e. phytoalexins, defense proteins etc. (Flores et al. 1999) to combat parasitic infections. Flavonoids from legume root exudates activate Rhizobium meliloti genes responsible for the nodulation process and it has been assumed that they induce Vesicular-Arbuscular Mycorrhiza (VAM) (Yadav et al. 2019). Microbial cell wall components are also found to elicit some specific chemical secretion from roots.

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Besides, a significant drop in reducing sugar and total amino acid content in root exudates were observed from mycorrhizal sudangrass (Sorghum vulgare Pers.) when verified with non-mycorrhizal control set (Graham et al. 1981). Rosmarinic acid (RA) was identified sweet basil (Ocimum basilicum L.) hairy root exudates. Its secretion was found almost threefold increase in response to wall elicitors (CWE) from Phytophthora cinnamoni. Interestingly when these roots were exposed to Pythium ultimum, no increase of RA was found, which indicates high specificity among plant roots and selective microbes. RA also has high antimicrobial activity against an array of soilborne microorganisms. This observation certainly advocates that such cross talk in rhizosphere might influence the composition into rhizospheric soil microbiome. High rise in production of pigmented naphthoquinone derivatives of shikonin from root hairs and root border cells of Lithospermum erythrorhizon observed when grown in vitro in presence of fungal cell wall elicitors. The external elicitor not only enhances the amount of total pigment but also changes the ratios of its various derivatives produced in the tissues and initiates its de novo synthesis in epidermal cells (Brigham et  al. 1999). Besides, acetylated homo-serine lactones (AHLs) and some signal peptide molecule are well-established diffusible small molecule root exudates today providing signals in microbial gene expression. The interactions between root system and associate microbes have been studied extensively with gene expression studies and investigating small molecule exchange between both systems. Roots can establish close contact with different microorganisms in the rhizosphere by establishing various integral protein exchanges. Root-secreted various proteins play chemo-attractant role to microbes whereas microbial proteins activating plant innate immunity is well documented at present (De-la-Pena and Vivanco 2010). Microbial gene expression regulation by root exudates was directly documented by Fray (2002) as restoration of pathogenicity of an avirulent Erwinia carotovora mutant (AHL−) strain was found upon being introduced with AHL-producing transgenic tobacco plants. Some components of root exudates mimicking ALH were also identified stimulating AHL-regulated behaviors in some bacterial strains while inhibiting such behaviors in other strains (Knee et al. 2001). Thus there is an obvious communication between plant roots and underground microbial population with responses such as signal mimics and/or signal blockers. Study was also conducted to observe differential gene expression in response to root exudates. In an approach reporter genes were employed to determine specificity of members of the rhizosphere microbiome to recognize their habitat with respect to different abiotic and biotic stimuli. The in  vivo gene expression in Pseudomonas fluorescence into rhizopheric environment was identified adopting promoter trapping strategy by Rainey 1999. Genes that are expressed at elevated level during rhizospheric colonization included genes involved in nutrient acquisition, stress response, secretory proteins engaged in control of gene expression, environmental sensing, metabolic reactions, and also membrane transport (Barr et al. 2008). It have been found that some root proteins are expressed constitutively regardless of the any microbial occurrences and others are exclusively induced (Mathesius et  al. 2003) by specific microorganism, and a similar situation is observed in the proteins found in the root exudates (De la Peña et al. 2008).

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A significant fraction of total soil bacteria is possessed by a specialized group called actinobacteria. This group of bacteria belong to an extensively diverse that varies from morphologically, physiologically, and also the metabolic point of view. Such Gram-positive, mostly aerobic (few are anaerobic,  capnophilic; example - Actinobaculum suis, Actinomyces israelii (anaerobe), Trueperella pyogens (facultative anaerobe or capnophilic)) mycelia bacteria play crucial role in soil ecology and nutrient cycling (Ames et al. 1984). Due to their metabolic vastness, they have been considered as factory of so many value-added natural product (Roy and Banerjee 2014). Such group of bacteria is usually important in qualitatively and quantitatively at rhizospheric region where they help in plant growth as well as inhibit plant pathogens (Lechevalier 1988). Frankia species have been extensively studies for their root associative nitrogen fixation (Loria et al. 1997).

7.4  Diversity of Rhizospheric Actinobacteria Actinobacteria are the most profuse microorganisms forming threadlike filaments in the soil (Fig. 7.1). The actinobacteria, conceding the largest genera Streptomyces, with 961 distinct species represent one of the largest taxa among the overall 18 major lineages currently present in the bacterial domain (Ventura et  al. 2007). Members of phylum actinobacteria are diverse in nature and have been obtained from several extreme environmental conditions (drought, high temperatures, pH, pressure, salinities, etc.) and are related with plants growing in separate habitats (Verma et  al. 2019; Yadav 2017; Yadav et  al. 2015). The actinomycetes occur in various habitats in nature (George et al. 2012) and also represent a diverse group of microorganisms largely distributed in natural ecosystems in different parts of the world (Srinivasan et al. 1991). Microbiome research has great impact for better understanding of ecosystem processes like nutrient recycling and the host microbe interaction. This field of research also grasps immense potential for exploring role of soil microbes on the green gross productivity and agro-ecosystems (Kour et al. 2020a; Rana et al. 2020a). Researchers have utmost focused on the soil microbiome where fewer have focused on rhizosphere and endosphere microbes in agroecosystems (Wang et  al. 2017). Bacteria, invading plant roots, are actually plant growth-promoting rhizobacteria (PGRR) playing more crucial role to plant health than others in bulk soil. The common PGPRs so far well documented in the rhizosphere belong to the genera Acinetobacter, Arthrobacter, Bacillus, Burkholderia, Enterobacter, Pseudomonas, and Paenibacillus (Zhang et  al. 2017; Yadav et  al. 2018b; Yadav et  al. 2017b). Actinobacteria are mainly Gram-positive soil-residing bacteria, and their diversity in rhizosphere is positively related to the amount of humus, that is, the organic matter, carbon content, amount of decomposer, microbial load, etc. and plant species diversity (Henis 1986; Germida et al. 1998; Hayakawa et al. 1988). However, the rhizospheric actinobacteria are the most dominant in nature having great economic importance to us due to their huge contributions to soil systems.

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Fig. 7.1  Culture morphology of some endophytic actinomycetes

Comprehensive literature study reveals members of phylum actinobacteria are reported from diverse genera like Microbacterium, Micrococcus, Mycobacterium, Sanguibacter, Streptomyces, Bifidobacterium, Cellulomonas, Clavibacter, Corynebacterium, Frankia, Nocardia, Propionibacterium, Pseudonocardia, Rhodococcus, Acidimicrobium, Actinomyces, and Arthrobacter (Verma et al. 2017; Yadav et  al. 2017a; Yadav et  al. 2018a) (Table  7.1). Rhizosperic actinobacterial population influences the growth of wild Thymis zygis L., and the actinobacterial population was isolated from the rhizosphere in a culture-dependent or culture-­ independent manner. It has been found that Proteobacteria (mostly Alpha- and Beta-­ proteobacteria), Actinobacteria, Acidobacteria, and Gemmatimonadetes are the dominating participants. Interestingly with the overall biodiversity observed within the cultured bacterial collection, around 61.5% belonged to the phylum Actinobacteria, most of which fall into the subclass Actinobacteridae, and pyrosequencing result revealed the most common phyla were Actinobacteria (33.9%) just after Proteobacteria (39.5%) of all pyrotags (Pascual et al. 2016). Recently, it had been found that root-derived carbon was assimilated by populations of Actinobacteria (Ai et al. 2015). Many strains of Actinobacteria have been described as plant-growth promoters and synthesizers of a variety of biologically active secondary metabolites (Suzuki et al. 2000).

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Table 7.1  Different genera of actinomycetes and their uses Actinomycetes genera Acidimicrobium Actinomyces Arthrobacter

Bifidobacterium Cellulomonas Clavibacter Corynebacterium Frankia Microbacterium Micrococcus

Mycobacterium Nocardia Propionibacterium Pseudonocardia Rhodococcus Sanguibacter Streptomyces

Role in environment/applications Ferrous-iron-oxidizing, moderately thermophilic and acidophilic bacteria Produce a number of enzymes that help to degrade organic plant material, lignin, and chitin Used for industrial production of L-glutamate. In industrial applications, it is often grown with low-cost sugar sources such as cane or beet molasses, starch hydrolysates from corn or cassava tubers, or tapioca Fond in the intestinal microbiota of breast-fed infants, used as a probiotic to conventional treatment of ulcerative colitis Degrade cellulose, using enzymes such as endoglucanase and exoglucanase The causal agent of bacterial wilt and canker of tomato Have been used in the mass production of various amino acids including glutamic acid, produce metabolites similar to antibiotics: bacteriocins Form nodule in non-leguminous host and fix nitrogen Mineralize sulfamethoxazole and other sulfonamides, produce bioemulsifier Catabolically versatile, with the ability to utilize a wide range of unusual substrates, such as pyridine, herbicides, chlorinated biphenyls, and oil, likely involved in detoxification or biodegradation of many other environmental pollutants Human and animal pathogen Human and animal pathogen Used in the production of vitamin B12, tetrapyrrole compounds, and propionic acid, as well as in the probiotics Have antibiotic properties provided to the leaf-cutter ant Catabolize a wide range of compounds and produce bioactive steroids, acrylamide, and acrylic acid and involve in fossil fuel biodesulfurization Found as endophyte in different plants Found in soil and decaying vegetation, are noted for their distinct “earthy” odor that results from production of a volatile metabolite (geosmin), produce complex secondary metabolism, produce over two-thirds of the clinically useful antibiotics

Agronomically beneficial rhizospheric actinobacterial strains are also well established. Such strains are reported as biocontrol agents and producing plant growth-­ promoting substances. Such groups of bacteria are also considered as good source of variety of decomposing enzymes, and it is assumed that they can protect plant roots from soil-dwelling plant pathogenic fungi by producing fungal cell wall-­ lysing enzymes (Goodfellow and Williams 1983; Valois et al. 1996). Streptomyces was found most predominating among any actinobacteria inhabiting rhizosphere; however, non-streptomycetes including Actinomadura sp., Microbispora sp., Micromonospora sp., Nocardia sp., and Nonomurea sp. are also found in rhizosphere of some medicinally important plants (Khamna et al. 2009a, b).

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7.5  Translating into Technology Microbial bioengineering uses knowledge and basic ideas to design or modify microbial systems for biotechnological application. Novel technologies with high-­ throughput screening and sophisticated instrumentations are available to advance the development of microbial cell factories. Use of genome-scale metabolic studies with integrated genomic approach accelerates the target-oriented biotechnological application of designed source strains. A large number of metabolic reactions take place in single microbial cells which convert nutrients into new products, and some of them have bioactive potentials. Enzymes are involved in strict controlling and coordinating reactions that happen simultaneously or consecutively. Microbial biotechnology since the ancient time is used as one of the oldest technologies (fermentation history) and even presently exploited as the newest and most rapidly developing industries. The field shares a long lineage of knowledge and experimentation and is presently enjoying an outstanding period of random innovation. Applications of microbial biotechnology research are diverse including different sectors like pharmaceuticals, microbial therapies, diagnostics, fermented foods, PGPs (plant growth promoters), enzymes, biomaterials and biopolymers, bio-­ surfactants and emulsifiers, bioenergy from renewable sources, fossil fuel recovery and valorization, recycling technologies, wastewater treatment, bio-mining, bioremediation, and so on. Biocontrol agents can be described as bacteria that aid in reducing plant disease incidence/severity. On the other hand, antagonists are those bacteria that exhibit antagonistic activity toward a pathogen (Beattie 2011). Biological control is used as a tool for the management of pathogens (bacterial, fungal, viral), nematodes (stem borer, root borer, etc.), and weeds or herbs. Tools of biological control like actinobacterial or fungal agents act as the substitute for the harmful xenobiotic chemicals that are used as fungicide, herbicide, or weedicides and finally reducing the risk of contamination of food products and toxicity related to their consumption by human body. The interacting populations of microorganisms inhabiting the rhizospheric zones have profound ecological significance for biocontrol strategies. Significant reduction in pathogenic populations of Fusarium oxysporum, Gaeumannomyces graminis, Pythium, and Phytophthora species is due to the soil conditions related to the soil microbial load and soil physiochemical properties. The reduction is specific and includes various mechanisms like antibiosis, production of siderophores (chelating compounds) or VOCs (volatile organic compounds), parasitism (+,- interactions between two organisms), competition for nutrients (−,- interactions), and competition for the area of functioning of two species, i.e., ecological niches. Bacterial antagonistic activities include synthesis of hydrolytic enzymes (chitinases (chitin; component of fungal cell wall degrading enzyme), glucanases (perform hydrolysis of polysaccharides), proteases (finalize proteins into amino acids), and lipases (breaks down the fatty substances)) that lyse pathogenic fungal cells certainly by producing some low molecular weight organic metabolites inhibiting growth of other microbes somehow. Actinomycetes have a

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wide range of genes encoding proteins with useful bioactive compounds, such as antibiotics (antibacterial and antifungal), antioxidative compounds, antitumor agents, and immunosuppressive agents (Bérdy 2005). The urge for novel microbial metabolites has initiated researches in these popular fields, and it has been found that diverse strains of the same species of actinomycetes can synthesize a variety of secondary metabolites acting as the pool of bioactive compounds (Waksman and Schatz 1943). Actinomycetes are important from their agricultural point of view due to their ability to promote plant growth and also betterment of plant nutrition either by direct plant growth-promoting mechanisms (like nitrogen fixation, solubilization of phosphorus (P), potassium (K), and zinc (Zn)); production of indole acidic acid (IAA) and other auxinlike growth-inducing substances, gibberellic acid (GA), and zeatin (kinetin like substances); and production of siderophores and ACC deaminase activity or by involving indirect mechanisms such as the production of ammonia (NH3), antibiotics, hydrolyzing enzymes (glucanase, chitinase, lipase, protease etc.), hydrogen cyanide (HCN), and siderophores (metal chelators) like compounds, etc. (Yadav et al. 2018) (Fig. 7.2). Actinobacteria are most renowned candidates for production of secondary metabolites, thus inhibiting other group of competitive microbes. A large number of antibacterial and antifungal compounds like staurosporine, 3-acetonylidene-7-­ prenylindolin-2-one, diastaphenazine, and antimycin A18 are produced by Streptomyces sp. colonizing on root tissues (Yan et al. 2010; Li et al. 2014; Zhang et  al. 2014). In the year 2009, El-Tarabily worked on three actinomycetes Actinoplanes campanulatus, Micromonospora chalcea, and Streptomyces spiralis and inoculated them on cucumber plants (Cucumis sativus) that exhibited less occurrence of root and crown rot. Several other examples include where actinobacteria inoculated on roots of plant provide protection from invasion of harmful pathogens (Xue et al. 2013; Nabti et al. 2014; Solans et al. 2016). The unique ability of rhizospheric actinomycetes to facilitate the production of a diverse array of

Fig. 7.2  Biotechnological potentials of rhizospheric actinobacteria

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metabolites with antagonistic effect toward phytopathogens has made them a potent agent that ensures plant health and primary productivity. Recently, rhizospheres of Vitis vinifera in different soil condition and vineyard management have been characterized. This result showed that grapevine rhizosphere-­ associated bacteria may exert some beneficial effects on the host plants, particularly in providing protection from harmful ROS (reactive oxygen species) (Salomon et  al. 2016), no specific report available on actinobacteria and streptomycetes to control phytopathogenic fungi that cause trunk diseases on grapevines. Loqman et al. (2009) isolated 142 actinobacterial species from rhizospheric soils of V. vinifera in Morocco, and some of these isolates were found efficient in treating fungal infection other than the causal organism of trunk diseases (Alvarez-Perez et  al. 2017). From wheat and tomato rhizospheric soil, about 98 actinomycetes strains were isolated. These actinobacterial isolates were screened for growth-promoting activities in plant, and 30 of them were found positive in initial screening (Anwar et al. 2016). A total of 89 actinomycetes were obtained from rhizosphere, and vermicomposts were screened to test their antagonistic behavior toward fungal pathogens of chickpea (Cicer arietinum) by dual culture method and assays that involve metabolite production. Among these isolates, four most promising actinomycetes were found effective in their physiological parameters and plant growth-promoting properties (Sreevidya et al. 2016).

7.6  R  ecent Landmarks on Diversity and Bioactivity of Rhizospheric Actinomicrobiota Actinomycetes from soil have been an area of immense interest and a never-ending field of study. The isolation of actinobacteria from soil source includes the use of selective media, and special care is also taken for the avoidance of fungal contamination (Fig. 7.3). Actinomicrobiota from rhizospheric soil always has been a repository of bioactive compounds with wide range of biotechnological potential (Figs. 7.4 and 7.5). Large quantities of antibiotics are known to be produced till date from these ray fungi or branched bacterial sources (Fig.  7.6). Their multidimensional application includes their affectivity as PGR, biocontrol agent, and potent antimicrobial compound producers (Table  7.2). They have been searched from various plant rhizospheres all over the world almost from every type of ecosystem ranging from mangrove to medicinal plants and salty habitats. The rhizospheric actinobacterial population associated with Theobroma cacao was evaluated for the plant growth-promoting activity and ability to be used as a biocontrol agent (Barreto et al. 2008). They also evaluated the in vitro extracellular enzyme production ability like cellulase, chitinase, and xylanase, also indole acetic acid production, and phosphate solubilization. It is revealed from the performed study that the population densities of culturable actinobacteria in soil and cacao plants are more or less similar and of genetically diverse type. The isolates are identified as Streptomyces sp. by analyzing the rpoB gene (that functionally codes for β-subunit of the RNA polymerase).

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Fig. 7.3  Flowchart of actinomycetes isolation and screening for bioactivities

The actinobacterial populations in rhizospheric soil of a desert plant Artemisia tridentata (sagebrush) are of high variation depending upon season to season and stages of plant growth (Gonzalez et al. 2009). The isolates were analyzed by both molecular (16S rDNA-based PCR along with DGGE-denaturing gradient gel electrophoresis) and cultural methods (agar plate enumeration using three different media). Results obtained from PCR-DGGE studies revealed that though bacterial counts are higher in winter, actinomycetes are diverse in spring time soils than in winter time soils. They reported that the soil associated with the roots of young plants exhibited higher diversity of actinobacterial species than the soil of old plants. Intra et al. in the year 2011 worked on screening of actinomycetes from plant rhizospheric soil having antifungal potency against Colletotrichum sp., the causal agent of anthracnose disease. Anthracnose disease has been a serious problem for

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Fig. 7.4  Different bioactivities of actinomycetes: (a) Liquid culture morphology of actinomycetes. (b) Actinomycetes forms ball like colonies in culture broth. (c) Antibacterial activity of the actinobacterial isolates. (d) DPPH radical scavenging assay, a test for antioxidative property. Yellow colored are of high radical scavenging ability and the purple one has the lowest scavengability. (e) Exopolysaccharide production by actinomycetous culture extract. (f) Protease activity shown by the actinomycetes. (g) Culture of actinomycetes on GC glass vials for volatile detection. (h) GC chromatogram of the volatiles emitted by the actinomycetous isolate

agricultural crops, and the possible measures for its control include the use of chemical fungicides with high degree of side effects. Here actinobacteria could be used as a biological control agent to minimize the disease occurrence events. In total 304 actinobacteria were isolated and screened for their antifungal activity against species of Colletotrichum: Colletotrichum gloeosporioides strains DoA d0762 and DoA c1060, Colletotrichum capsici strain DoA c1511, and also non-pathogenic

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Fig. 7.5  Bioactivities and microscopic images of actinomycetes: (a) Light microscopic view of actinomycetes. (b) Scanning electron microphotograph of actinomycetes isolate. (c) Amylolytic activity of the actinobacterial isolates seen after iodine application. (d) Halo zone produced by the actinomycetes on casein-rich media as a result of protease activity. (e) Antagonistic activity of actinomycetes against plant pathogenic fungus Colletotrichum sp.]

Saccharomyces cerevisiae strain IFO 10217. Results include that 222 isolates inhibited the growth of at least one of the phytopathogens tested. 54 actinobacterial isolates were effective in inhibiting the growth of the three phytopathogens. 17 could block the growth of all the four fungi tested. Most of the isolates were identified as Streptomyces sp. Other genera include Saccharopolyspora, Nocardiopsis, and

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Fig. 7.6  Chemical structures of bioactive secondary metabolites of actinomycetes origin

Nocardia. Out of the 304 isolates only 1 isolate identified as Streptomyces cavurensis with high percentage similarity of 98% probably produces a unique antifungal compound in its crude extract preparation when tested in HPLC technique. Poomthongdee et al. in the year 2014 worked on rhizospheric soil samples from 21 different regions and isolated 351 actinobacterial isolates by the help of acidified

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Table 7.2  Actinomycetes with their source and bioactivity Actinomycetes Rhizospheric source Nocardiopsis lucentensis Rhizosphere soil of and Mycobacterium sp. Cipadessa baccifera and Clausena dentata (Kolli Hills, Namakkal, Tamil Nadu, India) Rhizosphere soil of Streptomyces sp., fodder leguminous Micromonospora sp., plant Vigna Nocardia sp. unguiculata and Saccharopolyspora sp. Trifolium Actinopolyspora sp. alexandrinum (Ludhiana, Punjab) Rhizosphere of birch Streptomyces galbus, Streptomyces espinosus, (Betula pendula) (coal mine dump in Streptomyces Silets, Ukraine) beijiangensis, Streptomyces parvus, Amycolatopsis saalfeldensis Streptomyces sp. Mangrove mud rhizosphere of Rhizophora mucronata (Segara Anakan lagoon, Indonesia)

Bioactivity and diversity References Antibacterial against Bacillus Gopinath subtilis CFU for each plant soil et al. (2018) 22.41 × 10−5 Colony/g of soil and 17.33 × 10−5 colony/g of soil, respectively

Isolated from rhizospheric soil in Egypt Isolated from mangrove sediments of Coastal Waters in Pahang, Malaysia

Abd-Allah et al. (2012)

Streptomyces atrovirens

Streptomyces sp., Micromonospora sp., Micrococcus sp., Gordonia sp., Nocardia sp., Dietzia sp., Pseudonocardia sp., Saccharopolyspora sp., and Verrucosispora sp.

Biocontrol activity as antifungal against phytopathogenic fungi Fusarium oxysporum, Fusarium moniliforme, and Sclerotinia sclerotiorum 94 actinomycete isolated Produce siderophores and antibacterial (Bacillus cereus, B. subtilis, Staphylococcus albus, S. aureus, Micrococcus luteus) compounds 5 actinomycetes strain

Kaur et al. (2015)

Antibacterial against MDR bacteria Staphylococcus aureus, Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Enterococcus cloacae, and Enterobacter sp. Production of Indole-3-acetic acid (IAA)

Ryandini et al. (2018)

Antimicrobial against Bacillus subtilis, Escherichia coli, Serratia marcescens, Staphylococcus aureus, and Candida albicans

Abidin et al. (2018)

Ostash et al. (2013)

(continued)

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Table 7.2 (continued) Actinomycetes Streptomyces sp., Streptosporangium sp., Actinomadura sp., Nocardia sp., Nocardiodes sp., Saccharopolyspora sp., Thermoactinomyces sp., Amycolatopsis sp., Micromonospora sp., Microbispora sp., Intrasporangium sp., Planobispora sp., Nocardiopsis sp. Geodermatophilus sp. Nonomuraea sp. JAJ18

Streptomyces marokkonensis sp. nov.

Streptomyces sp.

Streptomyces spp.

Rhizospheric source Rhizosperic soils of Uttarakhand (Rishikesh, Dehradun, Srinagar, Devprayag, Bageshwar, Narendranagar, Almora Uttarakashi, Chamba, Pauri, Tehri, Ranikhet), India

Bioactivity and diversity S. aureus, S. aureus (MRSA), B. subtilis, E. coli, E. coli clinical, P. aeruginosa, A. baumannii, Acinetobacter sp. clinical M. smegmatis 512 isolates

Indian Coastal Solar Antibacterial potency against Saltern Bacillus subtilis, Klebsiella pneumonia, Salmonella Typhi, Proteus vulgaris Rhizosphere soil of Candida albicans, Candida Argania spinosa L. tropicalis, Saccharomyces cerevisiae, Fusarium oxysporum f. sp. albedinis, Fusarium oxysporum f. sp. lycopercidi, Verticillium dahliae Aspergillus niger, Staphylococcus aureus, Bacillus subtilis, Bacillus cereus, Micrococcus luteus Escherichia coli, Salmonella Typhi, Klebsiella pneumoniae Soybean rhizosphere PGPR (plant growth promoting) activity; IAA production is significant amounts and in vivo enhancement of soybean plantlet. 53 isolates were obtained in total Rhizosphere soils of Alternaria brassicicola (rose apple anthracnose), Alternaria pandanus palm porri (shallot (Pandanus amaryllifolius), Thai blotch),Colletotrichum gloeosporioides (potato dry medicinal plant rot), Fusarium oxysporum (Chinese cabbage leaf spot), Penicillium digitatum (orange green mold), Sclerotium rolfsii (damping-off of balsam)

References Kumar et al. (2013)

Jose et al. (2014)

Bouizgarne et al. (2009)

Wahyudi et al. (2019)

Khamna et al. (2009a, b)

(continued)

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Table 7.2 (continued) Actinomycetes Streptomyces sp. Majority fall under the group of Streptomyces sp., Actinoplanes sp., Micromonospora sp., Nocardiopsis sp., Actinomyces sp., Actinopolyspora sp., Dactylosporium sp. Thirty-six isolates

Rhizospheric source Soil of Hosudi, Karnataka, India Black pepper (Piper nigrum L.) rhizosphere

Bioactivity and diversity Antibacterial and antioxidative property Inhibits pathogens of black pepper P. capsici, S. rolfsii, C. gloeosporioides 129 actinobacteria isolated in total

References Rakesh et al. (2013) Anusree and Suseela (2017)

Javadi Hill forest soil, Tamil Nadu, India

Antibacterial activity against Escherichia coli, Bacillus cereus, Staphylococcus aureus, Pseudomonas aeruginosa, Proteus mirabilis, Klebsiella pneumonia Antifungal against A. alternata, F. moniliforme, M. phaseolina, R. solani A. niger Two actinomycetes strain were isolated

Velayudham and Kasi Murugan (2012)

Streptomyces violatus

Rhizosphere of cotton crop

Streptomyces sp.

Rhizospheric soils of medicinal plant Alpinia galanga

Sujatha (2018) Rani et al. (2016)

media maintaining the pH at 5.5 (strictly acidic) and screened the isolates for their antifungal potency, siderophore-producing ability, and phosphate-solubilizing efficiency. Out of total 351 isolates, 212 isolates and 139 isolates were reported to be acidophiles and neutrophiles, respectively. The isolates were tested for their antagonistic activity against three selected rice pathogens Fusarium moniliforme, Helminthosporium oryzae, and Rhizoctonia solani. Greater than 50% of the isolates inhibited at least one of the tested phytopathogen, and nearabout 25% exhibited antifungal activities against all the tested fungi. Acidophilic isolates, R9-4, R14-1, R14-5, and R20-5, are known to be in close similarity with Streptomyces misionensis NBRC13063T (AB184285). 96.3% (338) of the isolates are siderophore producers, and 75.8% (266) are potent phosphate solubilizers. A large number of acidophilic actinomycetes exhibited antifungal, siderophore, and phosphate solubilization activity in comparison with neutrophiles. 325 isolates (92.6% of the total isolates) were classified as Streptomyces sp. confirmed by morphology and occurrence of LL-isomeric form of DPA (diaminopimelic acid) in complete cell lysate. The non-­ streptomycete genus was confirmed as Allokutzneria, Amycolatopsis, Mycobacterium, Nocardia, Nonomuraea, Saccharopolyspora, and Verrucosispora by 16S rRNA analysis. Rhizospheric actinobacterial population of sediments of tropical mangrove forests of Malaysia were screened for their diversity and bioactivity (antimicrobial property) (Lee et al. 2014). Researchers isolated 87 actinobacterial species from 4 different sites. They firstly reported Streptomyces sp., Mycobacterium sp., Leifsonia

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sp., Microbacterium sp., Sinomonas sp., Nocardia sp., Terrabacter sp., Streptacidiphilus sp., Micromonospora sp., Gordonia sp., and Nocardioides sp. from east coast mangrove vegetation of Malaysia. Eighty-seven isolates were isolated from soil samples collected from four different sites. Out of total 87 isolates, 5 were represented to be putative novel taxa, and 9 were known to be potent antimicrobial producers. A novel species identified as Streptomyces pluripotens sp. nov. MUSC135T is effective in inhibiting the growth of the MRSA (methicillin-resistant Staphylococcus aureus). The antibacterial metabolite synthesizing ability was confirmed by PKS (polyketide synthetase) and NRPS (nonribosomal polyketide synthetase) gene detection. This type of work supports the fact that mangrove rhizospheres are potent sources of antimicrobial compound producing actinobacteria (Fig. 7.6). Muangham and his co-workers (2015) isolated 210 melanogenic (ability to produce melanin) actinomycetes from 75 rhizospheric soil samples of rice field and rubber trees of 21 provinces of Thailand using ISP6 and ISP7 agar medium with antimicrobial (antibacterial and antifungal) compounds added in it. Most of the isolates were confirmed as Streptomyces sp. by their presence of unique chalk dust like appearance of morphological colony and presence of LL- diaminopimelic acid in whole-cell hydrolysate. Two pathogenic rice bacteria Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola were inhibited (agar overlay technique) by most (61.9% inhibited at least one rice pathogen) of the isolates. Isolate coded as TY68-3 identified as Streptomyces bungoensis showed the highest antibacterial activity. So this rhizospheric actinobacteria could be exploited for the biocontrol of Xanthomonas oryzae rice pathogen. Sakure and his co-workers (2015) isolated ten actinobacterial species from rhizospheric soil of some medicinally important plants (turmeric, Curcuma longa; aloe vera, Aloe vera; Hibiscus sp.) near brick factory from Pune, India, and screened them for their in vitro antifungal potency against phytopathogens (Fusarium oxysporum, Fusarium solani, Alternaria alternata, Aspergillus flavus, and Colletotrichum gloeosporioides) by agar streak method. Isolates were characterized by slide culture technique, salt tolerance, growth at different pH and temperatures, biochemical characterization, and enzymatic activity. The isolates named A3 and BF5 were identified as Streptomyces sp. by microscopic morphology and 16  s rDNA partial sequencing. Antifungal activity by dual culture assay showed significant inhibitory activity of Streptomyces sp. (A3 and BF5) isolates against C. gloeosporioides (86.66%) and A. alternate (70.49%). Stress tolerance tests are also performed to assess their ability to withstand against ecologically abnormal conditions. Their scientific work contributes to the knowledge of application of actinomycetes as biocontrol agents for improvement of field qualities. Tropical and subtropical regions of southern part of China are characterized by the presence of red soils which are actually low in organic carbon contents and high in amounts of iron oxides and acidity. These are probably the best suitable conditions for acidophilic actinobacterial species to grow. Prior to the investigations of Guo et al. (2015), the actinomicroflora of these soils has not been explored well. Guo and his co-workers isolated 600 species of actinomycetes from Jiangxi Province

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(Southeast China) that belonged to 26 genera, 10 families, and 7 orders. The identities were confirmed by 16S rRNA gene sequence analysis. A total number of 193 secondary metabolites were reported from 52 of the actinobacterial isolates and 125 compounds of them are new and novel. The known compounds mostly belong to the chemical classes of diketopiperazines, macrolides, polyethers, and siderophores. They elucidated structures of six novel compounds and two of them are of unique skeleton. Results are indicative that red soils are reservoirs of culturable actinomicroflora with potent bioactive compound-producing abilities. The major synthesizers of the family include species of Streptomycetaceae, Pseudonocardiaceae, and Streptosporangiaceae. Damam et al. in the year 2016 isolated 62 actinomycetes from rhizospheric soil of some selected medicinal plants like Calycopteris floribunda (Combretaceae), Maerua oblongifolia (Capparaceae), exotic species Lantana camara (Verbenaceae), Zingiber officinale (Zingiberaceae), and Schleichera oleosa (Sapindaceae) found in the Pakhal forest of Pakhal wildlife sanctuary of Warangal (Dt.) situated in Telangana district of India. They screened the isolates for several bioactive properties including PGPs (plant growth promoters), ammonia production as a conversion from urea, IAA (indole acetic acid) production, HCN (hydrogen cyanide production), and phosphate solubilization. Results were indicative that 72% of the isolates were potent indole acetic acid production, an important requirement for proper growth of plant, and 755 of the total isolates responded in ammonia production increasing the amount of free soluble ammonia in soil for the plant to uptake for their enhanced growth. Almost half of all isolates screened yield positive result in HCN production followed by the phosphate solubilization by only 29% of the isolates screened for that purpose. So it could be drawn in conclusion from the above reports that actinomycetes from rhizospheric soil are potent tools for biotechnological exploitation and they can be further used as plant growth-promoting actinobacteria or biofertilizer for the enhancement of economic productivity of commercially valuable medicinal plants. Rante et al. (2017) isolated actinomycetes from the rhizosphere of Orthosiphon stamineus (a member of Lamiaceae) and screened them for their biotechnological potential to be used as potent compound synthesizers of antibacterial interest. Isolates were found to be effective against MDR (multidrug resistant) strains of Staphylococcus aureus and Escherichia coli. The antibacterial activity was determined by two ways: direct antagonism and use of culture extracts. The actinobacterial isolate named KC3 was inoculated in starch nitrate broth medium for a time period of 2 weeks, and after separating the biomass, the supernatants were extracted by organic solvent (ethyl acetate). MDR (multidrug resistant) pathogens are a serious challenge for the medical world to deal with, but the use of actinobacterial component for combating parasitic infections has opened up new horizons in this field. Adegboye and Babalola (2016) explored the rhizospheric soils of Ngaka Modiri Molema district of North West Province of South Africa for isolation and identification of actinomycetes with unique metabolite production having antibacterial potency and tested against 11 human pathogenic bacterial test organisms

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(Staphylococcus aureus, Streptococcus pyogenes, Campylobacter coli, Bacillus subtilis, Bacillus cereus, Proteus mirabilis, Enterococcus faecalis, Shigella boydii, Klebsiella pneumonia, Pseudomonas aeruginosa, Salmonella typhimurium). The isolates are identified (16S rDNA analysis) as Actinomadura, Nocardiopsis, Promicromonospora, Nocardia, Arthrobacter, Pseudonocardia, Micrococcus, Nonomuraea, Rhodococcus, Streptosporangium, and Saccharothrix spp.. Out of the total 88 actinobacterial isolates 19 of them showed bactericidal or bacteriostatic activity that fall under 11 phylotypes. The phylogenetic analysis revealed that the newly isolated strains come in close association with other potent antibiotic-­ producing strains in the phylogenetic tree. It is another evidence of the immense biotechnological potential of the rhizospheric actinomicroflora. Gad (2017) for the first time isolated 358 salt-tolerant actinomycetes from the 30 soil samples of vegetated and flat sites of extreme halophilic Great Salt Plains of Oklahoma using four different types of selective media and tested their antibacterial ability against MRSA (Staphylococcus aureus) and revealed a huge diversity of microorganisms in that regions. 155 isolates were chosen based on their morphological and physiological activities for screening of salt tolerance ability, antibacterial affectivity, and also phylogenetic diversity. Isolates were separated on two groups based on the 16S rRNA gene sequence analysis. Groups include Streptomyces sp. (phylotypes that are detected at high frequency) and Nocardiopsis sp. (phylotypes detected in low frequency). Only 38% of the isolates were found slightly halophilic (can withstand 10% of salinity) in nature, and 7% can survive up to 15% of salinity (high salt-tolerant species). 44 isolates showed anti MRSA activity. This type of study is not only indicative of the fact that actinobacterial diversity is ubiquitous in nature and not endemic to only normal forest soils and also focuses on the pharmaceutical potential of these species to fight against severe bacterial infections. Thangapandian and his co-workers (2007) collected soil samples associated with medicinal plants (subabul, Leucaena leucocephala; mahua, Madhuca indica; bhangra, Eclipta alba; akven, Gliricidia maculata; henna, Lawsonia inermis; neem, Azadirachta indica; karanja, Pongamia glabra; paneer, Chromolaena odorata) of Kolli Hills of Salem district, Tamil Nadu, India, and screened them for their antibacterial activity against serious human pathogenic microorganisms (Streptococcus faecalis, Pseudomonas aeruginosa, Escherichia coli, Bacillus amyloliquefaciens, Staphylococcus aureus, Candida albicans, Cryptococcus neoformans) to be used as a tool of biotechnological importance. Most of the effective isolates are identified as Streptomyces sp. Kaur and his co-workers (2017) isolated 40 actinobacterial species from the rhizospheric soils of economically important floricultural species Gladiolus sp. and assessed their plant growth-promoting activity. Isolates were screened for several parameters like IAA (indole acetic acid) production (16 isolate with positive response), phosphate solubilization (18 potent solubilizers), siderophore (15 potent producers) and gibberellic acid production (12.5–50.6 μg/ml by 50 bacterial species), catechol (produced by 9 isolates) and hydroxamate formation (12 isolates with potent response), HCN production (10 bacterial species with remarkable production), and ACC deaminase activity (5 rhizospheric isolate showing positive

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result). Biocontrol ability includes the antagonistic activity against Fusarium oxysporum, a potent wilt pathogen of Gladiolus sp. Isolate Sc9 is identified as Streptomyces sp. further analyzed in green house study to be used as a potent biocontrol agent against Fusarium wilt. Retnowati and his co-workers (2017) studied the diversity and distribution of antibiotic-producing actinomycetes in different locations of mangrove forest of Torosiaje, Gorontalo, Indonesia, which has unique type of geomorphological features, and the forest is surrounded by karst type of ecosystems. Sampling procedure includes the collection of soil sample at a depth of 0–10 cm and immediately subjected to detailed physiochemical character analysis. Selective culture media (starch casein agar media) supplemented with common standard antifungal agents nystatin and cycloheximide were used for the culture of actinomycetes. The screening methods include the agar block method against pathogenic microorganisms. Grouping and diversity determination of actinomycetes were done by ARDRA and 16S rDNA technology, respectively. Rhizophora mucronata rhizospheric soil (over wash type) harbors the highest density of actinobacterial species, and R. apiculata represents the lowest value (middle zone of fringe type). 77 isolates out of 167 had strong antibacterial activity, and 47 of them are partially characterized by ARDRA, and 16S rDNA study reveals their probable nomenclature as Streptomyces sp., Amycolatopsis sp., Saccharomonospora sp., and Nocardiopsis sp. Streptomyces qinglanensis and Streptomyces champavatii are commonly present here. Over wash types and fringe types were usually dominated by Saccharomonospora sp. and Nocardiopsis sp. and Amycolatopsis sp. Genera Saccharomonospora and Nocardiopsis were mostly found at the over wash type. Raut and Kulkarni (2018) tested the rhizospheric soils of medicinal plants (Aloe barbadense, Emblica officinalis, Zingiber officinale, Tinospora cordifolia, Nerium oleander, Eucalyptus camaldulensis, Mentha arvensis, Santalum album, Hibiscus rosa-sinensis, Ocimum sanctum, and Curcuma longa) of Barshi, Solapur, M.S. India. The soil sample was serially diluted and plated on glycerol asparagine agar medium. 71 isolates were studied morphologically, culturally, and biochemically. The isolates are identified (by the help of MICRO-IS software and 16  s rRNA) as Streptomyces sp., Streptoverticillium sp., Nocardia sp., Micromonospora sp., and Micropolyspora sp.

7.7  Conclusion and Future Prospects Actinomycetes are ubiquitous in nature and have been one of the wonders of nature in terms of their bioactivity and diversity of occurrence. They are known to produce a variety of bioactive compounds with global values on industries like pharmaceutical, textiles, etc. They have been scavenged from all type of normal or extreme ecosystems till date, but it has been proved that rhizospheric actinomicrobiota being associated with root and soil is the most diverse niche of actinomycetes and is of diverse potential applications. Popular selective medium like ISP2 and ISP5 which

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are used for the isolation of actinobacteria only are outcome of the International Streptomyces project, and this type of project emphasizes the fact that modern world largely depends on actinobacteria for antibiotics. So the focus of modern civilization and medical world for their ultimate survival from pathogenic microorganisms is narrowed down to this group of microorganisms with unique branched hyphal like bacterial cell and characterized with the earthy odor called as geosmin that is smelled after the first rain. Actinobacterial metabolites are all-square ranging from antimicrobial (antibacterial, antifungal), antioxidative (antiaging, scavengers of oxidative stress) compounds to VOCs (volatile organic compounds) and industrially valuable enzymes (tannase), etc. Scientific communities are still hoping for better discoveries from these groups of organisms for solving a many of irreparable problems of modern medical world.

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Yadav N, Yadav AN (2019) Actinobacteria for sustainable agriculture. J Appl Biotechnol Bioeng 6:38–41 Yadav AN, Verma P, Kumar M, Pal KK, Dey R, Gupta A et  al (2015) Diversity and phylogenetic profiling of niche-specific Bacilli from extreme environments of India. Ann Microbiol 65:611–629 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B et al (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Verma P, Kour D, Rana KL, Kumar V, Singh B et al (2017b) Plant microbiomes and its beneficial multifunctional plant growth promoting attributes. Int J Environ Sci Nat Resour 3:1–8. https://doi.org/10.19080/IJESNR.2017.03.555601 Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Sugitha TCK, Singh BP, Saxena AK, Dhaliwal HS (2018) Actinobacteria from rhizosphere: molecular diversity, distributions, and potential biotechnological applications. In: Singh BP, Gupta VK, Passari AK (eds) New and future developments in microbial biotechnology and bioengineering, pp  13–41. https://doi.org/10.1016/ B978-0-444-63994-3.00002-3 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018a) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, Los Angeles, pp 305–332 Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP et al (2018b) Actinobacteria from rhizosphere: molecular diversity, distributions and potential biotechnological applications. In: Singh B, Gupta V, Passari A (eds) New and future developments in microbial biotechnology and bioengineering, pp 13–41. https://doi.org/10.1016/B978-0-444-63994-3.00002-3 Yadav AN, Mishra S, Singh S, Gupta A (2019) Recent advancement in white biotechnology through fungi. Volume 1: Diversity and enzymes perspectives, Springer International Publishing, Cham Yadav AN, Singh J, Rastegari AA, Yadav N (2020) Plant microbiomes for sustainable agriculture. Springer International Publishing, Cham Yan LL, Han NN, Zhang YQ, Yu LY, Chen J, Wei YZ, et  al. (2010) Antimycin A18 produced by an endophytic Streptomyces albidoflavus isolated from a mangrove plant. J Antibiot 63(5):259–261 Yoder JI (2001) Host-plant recognition by parasitic Scrophulariaceae. Curr Opin Plant Biol 4:359–365 Zhang J, Wang JD, Liu CX, Yuan JH, Wang XJ, Xiang WS (2014) A new prenylated indole derivative from endophytic actinobacteria sp. neau-D50. Nat Prod Res 28(7):431–437 Zhang X, Zhang R, Gao J, Wang X, Fan F, Ma X (2017) Thirty-one years of rice-rice-green manure rotations shape the rhizosphere microbial community and enrich beneficial bacteria. Soil Biol Biochem 104:208–217

Chapter 8

Bacillus and Endomicrobiome: Biodiversity and Potential Applications in Agriculture Guruvu Nambirajan, Ganapathy Ashok, Krishnan Baskaran, and Chandran Viswanathan

Abstract  Traditional methods of crop production or agricultural practices improve the soil fertility in earlier periods, whereas excess use of chemical fertilizers and pesticides leads to soil infertility, environmental pollution, and various health hazards to human being. In recent years, excessive amounts of synthetic fertilizers were used in agricultural field to overcome the scarcity of food for the increased human population. Similarly, a strong dependence on inorganic substances can lead to a decrease in biodiversity, insect resistance to insecticides, a decrease in soil fertility, and a negative impact on nontarget species. An alternative to traditional methods of using microorganisms can serve as a growing demand for new and safer methods to replace and to avoid overuse of synthetic fertilizer. In this book chapter, wide range of application of Bacillus and endomicrobiomes in agriculture and biodiversity aspects were reviewed and discussed. Keywords  Biodiversity · Bacillus · Endomicrobiomes · Inorganic · Organic

8.1  Introduction In agriculture field, synthetic fertilizers have been overexploited to fulfil the food demand of the increasing population. The concentration levels of various insecticides are increasing in recent years to improve crop yield. In chemical industries, synthetic fertilizers are composed of some major chemicals like nitrogen, G. Nambirajan (*) Department of Microbiology, Sree Narayana Guru College, Coimbatore, Tamilnadu, India G. Ashok · C. Viswanathan Department of Biotechnology, Sree Narayana Guru College, Coimbatore, Tamilnadu, India K. Baskaran Department of Biochemistry, Sree Narayana Guru College, Coimbatore, Tamilnadu, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_8

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phosphorous, potassium, and other synthetic derivatives that cause groundwater pollution and eutrophication of water bodies and also have adverse effect on human beings and nontargetted organisms. Further, synthetic chemicals indirectly affect food chain and food web of agricultural ecosystem (Youssef and Eissa 2014). In recent years, the research world directed alternative efforts towards the environmentally friendly production of ‘high-quality, high-nutrient foods’ in a sustainable assortment to ensure biosafety and crop improvement, as well as to control the plant pathogens. In agriculture, microbes play a fundamental role in improving the nutrient supply and the fertility of soil, so microbes can be used as biofertilizers as they do not have any adverse effects on the ecosystem (Araujo et al. 2008; Raja 2013; Sahoo et al. 2014). Similarly, microbial formulations can be used as insecticides instead of harmful chemical pesticides, as some microbes have tendency of controlling agricultural pests (Kumar et al. 2019a, b; Yadav et al. 2017a, 2020). The microbes associated with the plant are naturally beneficial for plants, and they also help the plant for maintaining their growth and yield during abiotic and biotic stresses and create a special environment to rooting and attracting beneficial soil bacteria (Hallmann et al. 1997). Bacillus species are widely distributed and used to promote  plant growth either directly or indirectly promoting the dissolution of nutrients, nitrogen fixation, biosynthesis of phytohormones, antibiotics, hydrolytic enzymes, siderophores, cause systematic resistance and antiphytopathogenic properties (Kour et al. 2019b; Suman et al. 2016; Verma et al. 2015; Yadav et al. 2019d). Biofertilizers are generally known as single or mixture of two or more microorganisms that help in the enhancement of plant growth by producing phytohormones and availing several nutrients like nitrogen and phosphate solubilization. In addition, biofertilizers protect the crop from phytopathogens. Bacillus and Bacillus-derived genera are being used commonly as biofertilizers to enhance plant growth without affecting soil fertility (Kour et  al. 2020c; Rastegari et  al. 2020a; Verma et  al. 2016; Yadav et  al. 2016b). Endomicrobiome refers to one or more combination/collection of bacteria, including actinomycetes, cyanobacteria, fungi which  play a crucial role in plant defence mechanism and plant growth promotion (Popa et  al. 2012; Gibson and Hunter 2010; De Bary 1866). Endophytic microorganisms are associated with various parts of the plant including seeds, roots, stems, leaves, flowers, and fruits (Clay and Holah 1999; Guo et al. 2008; Yadav et al. 2017c). The microbes associated with plants play an important role in mitigation of different abiotic stresses (Kumar et al. 2019a, b; Rajawat et  al. 2020). The endophytic microbes belonging to different genera have been sorted out from plants (Khan et al. 2015; Kour et al. 2020d; Rana et al. 2020c). The species of fungi that resides inside the plants varies from different plant species and its habitat such as deserts (Bashyal et al. 2005), geothermal lands (Redman et al. 2002), rainforests (Strobel et al. 2002), mangrove swamps (Lin et al. 2008), Artic (Fisher et  al. 1995), Antarctic (Rosa et  al. 2009), and coastal forests (Suryanarayanan et al. 2005). Endophytic fungus produce wide range of secondary metabolites such as alkaloids, cyclohexanes, flavonoids, hydrocarbons, quinines,

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and terpenes, which have various biological properties like antimicrobial and anticancer activity (Fernandes et al. 2015; Naik and Krishnamurthy 2010; Ruma et al. 2013; Yadav et al. 2019b), and also produce different levels of extracellular enzymes like hydrolases, oxidoreductases, and lyases (Yadav et al. 2016a; Traving et al. 2015). Endophytic microbes produce different extracellular hydrolytic enzymes (Hallmann et al. 1997; Krishnamurthy and Naik 2017; Naik et al. 2009; Oses et al. 2006). These enzymes have capabilities to degrade different agricultural wastes (Kudanga and Mwenje 2005; Tomita 2003). These endophytic microbes thus play important role in plant growth promotion and soil fertility for sustainable agriculture (Kour et al. 2019a; Yadav et al. 2017b, 2019a). Plant growth stimulation is stimulated directly or indirectly with the help of microbial association. Microbes colonize inside the host plant and enhance the plant growth by  using various direct and indirect mechanism  such as solubilization of phosphorous, potassium, and zinc; production of siderophores and plant growth hormones like cytokinin, auxin, and gibberellins; and atmospheric nitrogen fixation are the mechanisms that directly stimulate plant growth. Also, microbes secrete some antagonistic substances that help in controlling several microbes as well as plant pest growth (Glick et al. 1999; Tilak et al. 2005; Yadav et al. 2017d; 2019d). Pathogens in the soil are suppressed by a biological control agent, such as plant growth-promoting microbes (PGPMs) that increase germination rate, biomass, leaf area, chlorophyll content, nitrogen content, protein content, hydraulic activity, the length of the roots and shoots, yield, and resistance to abiotic stresses such as drought, temperature, floods, and salinity (Kour et al. 2020a; Rana et al. 2020a).

8.2  Biodiversity of Bacillus Bacillus is Gram-positive, rod-shaped, endospore-forming bacteria that have an ability to survive in both aerobic and anaerobic conditions and tolerate biotic and abiotic stress, which is widely distributed in the environment. Bacteria of this genera are the most abundant (95%) in the rhizosphere of plants and are being known to be effective plant growth stimulators by producing a number of substances, such as antibiotics and antifungal metabolites (Turnbull 1996). The most registered formulations are Bacillus based which are commercially successful as biocontrol agents (Pérez et al. 2011). Bacillus was the most noteworthy genus in the analysed cultures due to its high frequency (Bredow et al. 2015) which is most common in various species of cultivated plants and soils (Hallmann and Berg 2006) and is able to form endospores, which shows resistance to environmental conditions (Fig. 8.1). The Bacillus spp. produces different degrading enzymes (chitinases, glucanases, and proteases) that help suppress pathogens. Lipopeptide can be classified into iturins, fengycins, and surfactins which shows antibacterial activity (Shoda 2000). Some Bacillus sp. has been reported as biocontrol agents (Guido and Ben 2001; Koumoutsi et al. 2004).

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Fig. 8.1  Applications of endophytic Bacillus for sustainable agriculture

The plant microbes that stimulate plant growth promotion (PGP) are more resistant against the pathogens and suppress the growth of pathogen that enhances the health of plant and reduces the harvest loss (Kamilovaa et  al. 2015; Kour et  al. 2020b; Rana et al. 2020b). Dunlap et al. (2015) reported that B. amyloliquefaciens colonized  with subspecies plantarum (methylotrophicus) are distinguished from B. amyloliquefaciens in their ability to form endospores and colonize the plant rhizosphere to stimulate plant growth and suppress the phytopathogens of bacteria and fungi. Due to their activity, an alternative source of chemical pesticide and agrochemicals is becoming increasingly important (Borriss 2011). Wu et  al. (2015) reported genetically modified Bacillus species can be used in the future for improving biopesticides and biofertilizers and as an alternative to synthetic fertilizers.

8.3  Bacillus in Agriculture Bacillus and Bacillus-derived genera are used as biocontrol agent, a promising option in the elimination of chemicals from soil (Rastegari et al. 2020b; Singh and Yadav 2020). It has many advantages over other bacteria, because it is easy to cultivate, store, and use as spores on plant seeds or in inoculants; it is able to promote the growth of plant and protect plants from the various microbial pathogen effects (Forchetti et al. 2007). Members of the Bacillus have huge set of biologically active molecules that inhibit potential growth of fungi/are antagonistic towards fungi (isolated from soil) and prevent cultivation of crops and plant growth (Schallmey et al. 2004). Similarly, it suppresses root diseases, foliar diseases, and postharvest diseases and plant parasite nematodes (Cazorla et  al. 2007; Jayaraj et  al. 2009; Liu et  al. 2009; Romero et  al. 2007; Pertot et  al. 2008; Leelasuphakul et  al. 2008; Arrebola et al. 2008) (Fig. 8.2).

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Fig. 8.2  Biotechnological applications of Bacillus in agriculture

Endophytic Bacillus alter plant physiology and direct stimulation of plant growth through the production of phytohormones and some species can stimulate root proliferation and nutrient absorption capable of producing auxins (Tsavkelaova et al. 2006; Spaepen et  al. 2007). Bacterial pathogens communicate through quorum sensing mechanisms by utilizing N-acyl homoserine lactones (AHLs), which act as signal molecule, to increase virulence factors. Bacillus thuringiensis synthesize the enzyme  N-acyl homoserine lactone lactonases to breakdown AHLs (quorum quenching) it significantly silencing the bacterial virulence and also act as a microbial bactericides (Zhou et al. 2008). Bacillus-based products have great potential in integrated pest management (IPM) systems, but they have some disadvantages, as the system affects the efficacy of the commercial products (Sorokulova et al. 2008) (Table 8.1).

8.4  Endomicrobiome Endophytic microbes are ubiquitous in nature in most plant species, penetrate plants through wounds and enhance plant growth through root hairs and epidermal connections, without affecting host plants and actively penetrate cellulase and pectinase enzymes in plant tissues using hydrolytic enzymes (Quadt-Hallmann et al. 1997). Endophytic  microbes colonize in flowers, stomata, and lenticels were reported  (Kluepfel 1993). Most of the Plant colonizing bacteria belong to Acidobacteria, Ascomycota, Bacteroidetes, Basidiomycota, and Deinococcus-­ Thermus and dominant bacterial genus such as Actinobacteria, Proteobacteria and Firmicutes.

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Table 8.1  Biodiversity of Bacillus Bacillus sp. Bacillus sp.

B. subtilis B. thuringiensis B. megaterium

B. cereus B. amyloliquefaciens B. simplex B. polymyxa B. aryabhattai B. pumilus B. licheniformis

Host plant Pigeon pea Wheat Chickpea Mung bean Maize Peanuts Tomato Soybean Banana Sunflower Bean Tobacco Soybeans Wheat Soybeans Maize, corn, carrot, citrus Soybean Mung bean Wild legumes Common bean Sophora Mung bean Tomato Wild legumes Various plants, pea Soybean Common bean Mung bean Saffron Saffron

Reference Rajendran et al. (2008a, b) Selvakumar et al. (2008) Saini et al., (2013) Pandya et al. (2013) Ikeda et al. (2013) Figueredo et al. (2014) Wei et al. (2015) Oehrle et al. (2000) Kesaulya et al. (2018) Pourbabaee et al. (2018) Sabaté et al. (2017) Wu et al. (2016)) Bai et al. (2003) Li et al. (2013) Bai et al. (2003) Surette et al. (2003) Subramanian et al. (2015) Bhutani et al. (2018) Muresu et al. (2008) Korir et al. (2017) Zhao et al. (2011) Bhutani et al. (2018) Tan et al. (2013) Muresu et al. (2008) Schwartz et al. (2013) Hung et al. (2007) Korir et al. (2017) Bhutani et al. (2018) Sharma et al. (2015) Sharma et al. (2015)

The dominant endophytic genera that resides in most plants are Achromobacter, Bacillus, Burkholderia, Enterobacter, Herbaspirillum, Pantoea, Pseudomonas, Rhizobium, and Streptomyces which can be used as biofertilizers and biocontrol agent for sustainable agriculture (Kour et al. 2019a; Rana et al. 2019c; Yadav et al. 2018). The endophytes and plant interactions can promote plant health (Suman et al. 2016). Endophytic microbes can promote plant growth in terms of increasing germination rate, biomass, leaf area, chlorophyll content, nitrogen content, protein content, root and shoot lengths, yield, and resistance to abiotic stresses such as drought, temperature, floods, salinity, and pH (Hallmann et al. 1997; Rosenblueth and Martínez-Romero 2006). Endophytic microbes colonized in the root of the plant initially and migrate to other parts of the plants (Jacobs et al. 1985; Ashok and Sivakumar 2018) and lives

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in vascular or intracellular space (Bell et  al. 1995). The ecological advantage of microbes is in the form of protecting plants from adverse environmental conditions: temperature, drought, pH, salinity, osmotic potentials, and ultraviolet radiation. Endophytic microbes form symbiotic associations with plant tissues, which are slightly pathogenic for plants but do not cause significant harm to the host. Mycorrhizal fungi are a heterogeneous group of diverse fungal taxa associated with the roots of more than 90% of all plant species, which contribute to and improve agricultural developments and exchange of nutrients between the host plant and the soil. Endomycorrhizae facilitate the exchange of nutrients between the host plant and the soil. Mycorrhizae help plants absorb water, inorganic phosphorus, mineral or organic nitrogen, and amino acids, as well as supply nutrients with carbon (Bonfante and Genre 2010; Finlay 2008; Yadav et al. 2019c). Endophytic microbes can be used in next generation of agriculture practice to support plant growth in environmental friendly and to control wide range of plant pathogens. The rhizospheric regions have different beneficial plant growth-promoting microbes (Bulgarelli et al. 2013; Berg et al. 2013). Endophytic microbes live in a chemically unique microenvironment, which develop potential properties and adapt primary functions to those useful for plants. Thus, the properties of chemical interactions of endophytes are a potential source for various natural products with widespread use in medicine, industries, and agriculture (Rana et al. 2019a, b). In modern agriculture plant-associated Bacillus sp. have significant role in growth enhancement property and toxic agrochemical, due to lipopeptide production which inhibits the phytopathogens, environmental accumulation, and resistance development also prevented by isolates with ideal organism for field application (Jasim et al. 2016). The microbiome is highly dependent on crop production under the influence of the environment surrounding the host plant, the type of influence such as soil pH, rainfall, temperature, soil content, and soil salinity (Kaur et al. 2020; Singh et al. 2020). To find out the distribution and diversity among different groups of microbes associated with different cultures in the form of epiphytic, endophytic, and rhizospheric, it is necessary to isolate them using cultivated and cultured methods. Endophytic isolation requires attention to avoid contamination; first sterilize the entire surface of the samples and sterilize the knife, then cut pieces of their organs and tissues, and if necessary, use sodium hypochlorite as a disinfectant. Explants are sterilized by immersion in 70% ethanol for 1–3  min and 1%–3% sodium hypochlorite for 3–5  min, followed by repeated washing in sterile water to remove residual sodium hypochlorite (Suman et al. 2016) and twice or triple surface sterilization to eliminate epiphytic microbes with a combination of ethanol or other disinfectants. To isolate endophytic microbes, the samples were macerated independently with 10 mL of sterile 0.85% NaCl using a mortar and pestle and then homogenized by vortexing for 60 s at high speed. The solution was used for further isolation of microbes by standard microbiological methods, such as serial dilution, and then using the pour plate method, use different media to isolate archaea, eubacteria, and fungi. The microbes are then screened using the previously described methods for resistance to temperature, salt (NaCl concentration), drought, and pH (Suman et al. 2016).

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8.4.1  E  ndomicrobiome: Potential Value of Beneficial Microbes in Sustainable Agriculture Plants such as dune grass, panic grass, rice, and tomato, salinity tolerance was conferred by Fusarium culmorum (Rodriguez et al. 2009). The endomicrobiome exhibits stronger symbiotic associations with higher degree of host specificity, and majority of the microbes appeared pathogen due to inappropriate response in non-­ host species (Schulz and Boyle 2005). Endomicrobiomes have been reported from different host plants (Pirttilä et al. 2000; Strzelczyk and Li 2000; Cankar et al. 2005; Izumi et al. 2008; Bal et al. 2012; Carrell and Frank 2015; Hernández-García et al. 2017) and their functional pathways, common for both communities. Dendroctonus bark beetles have certain metabolic functions (such as starch, esters, xylan, hydrolysis of lipids, cellulose and xenobiotic biodegradation). Endophytic bacterial isolates are involved in metabolic pathways including carbohydrate metabolism, amino and nucleotide sugar metabolism, glutathione metabolism, xenobiotic degradation and oxidative phosphorylation (Morales-Jiménez et al. 2012, 2013; Hu et  al. 2014; Cano-Ramírez et  al. 2016; Van Aken et  al. 2004; Parmentier et  al. 2011; Sheibani- Tezerji et  al. 2015; Ruiz-Pérez et  al. 2016; Sánchez-López et al. 2017). Sometimes endophytic bacteria with plants also exhibit different environmental reactions depending on the habitat or the environment (Escobedo et al. 2018). Endophytes are located in the apoplastic intracellular spaces of parenchymal tissues and xylem vessels, which suppress pathogens, remove contaminants, and produce fixed nitrogen or new substances that can increase crop yields (Quadt-Hallmann et al. 1997; Suman et al. 2001; Verma et al. 2016; James et al. 1994; Lacava and Azevedo 2013; Glick 2015). It was established that fungal endophytes colonize the plant, and it was isolated from boreal forests, tropical climate, diverse xeric environments, extreme arctic environments, ferns, gymnosperms, and angiosperms (Mohali et al. 2005; Selim et al. 2017; Šraj-Krzic et al. 2006; Suryanarayanan et al. 2000). Plant colonized with endophytic microbes showed increased growth when compared to control plant. This faster growth of plant is due to availability of sufficient amount of nutrients, minerals, and plant growth hormones and also protection against pathogens (Cheplick et al. 1989; de Bruijn et al. 1997; Suman et al. 2001; Iniguez et al. 2004; Rashid et al. 2012; Nath et al. 2013; Lin and Xu 2013; Jasim et al. 2014; Verma et al. 2016).

8.5  Conclusion and Future Prospective In recent years, the use of chemical fertilizers has increased due to food shortages for growing population that adversely affect the natural environment. In order to achieve sufficient amount of food for feeding the world population, PGPM usage as biofertilizer is the best alternative to chemical fertilizers without affecting nature.

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Microorganisms, as an alternative source to solving problems, increase productivity without affecting ecosystem and provide sustainable agriculture production. So, in conclusion, plant growth-promoting microbes with multifarious plant growth-­ promoting attributes should be used as biofertilizers and biopesticides for sustainable agriculture and environment.

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Chapter 9

Role of Microbes in Improving Plant Growth and Soil Health for Sustainable Agriculture Devender Sharma, Navin Chander Gahtyari, Rashmi Chhabra, and Dharmendra Kumar

Abstract  Symbiotic (Rhizobia, Frankia, and VAM) or free-living (Azotobacter, and Clostridium) association of plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF) is essential for plant and soil health. Nitrogen (N), phosphorus (P) and potassium (K) as major and iron (Fe) and zinc (Zn) as the minor elements are key to plant health. They are important constituents of plant genetic material (N, P) and chlorophyll content (N, Fe) and important for enzymatic activities (Fe, Zn) and are involved in many biochemical and physiological activities. The ‘microbiome’ around the rhizosphere is specific to plant type and involved in nutrient cycling through various processes such as fixation (N), solubilization, mineralization (P, K) and uptake, with the help of various organic acids (gluconic acid, oxalic acid, and tartaric acid), siderophore activity (Fe uptake) and enzymatic actions (nitrogenase, phytases, and acid phosphatases). Phytohormones essential to plant growth and development are produced by microbes themselves or induce their production via other hormones or communication chemicals, viz., volatile organic compounds (VOCs) like 2-pentylfuran, 2,3-butanediol and acetonin. PGPR (Pseudomonas, Trichoderma and Streptomyces) helps the host plant to fight against various abiotic and biotic stresses by the release of bactericidal and fungicidal enzymes, metabolite accumulation and induced systemic resistance (ISR), systemic acquired resistance (SAR) by phytohormones (jasmonic acid, salicylic acid, and ethylene) and VOCs. Attributing to so many benefits, microbes are increasingly becoming part of sustainable agriculture where PGPR (Rhizobium and Pseudomonas) and fungi (Aspergillus, Trichoderma D. Sharma (*) · N. C. Gahtyari Crop Improvement Division, ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS), Almora, Uttarakhand, India R. Chhabra Division of Genetics, ICAR – Indian Agricultural Research Institute, New Delhi, India D. Kumar Division of Crop Physiology, Biochemistry and Post Harvest Technology, ICAR-CPRI, Shimla, India © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_9

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and VAM) are being used as biofertilizers either single strained or in consortia approach, where the latter is found to be more beneficial for plant and soil health. Keywords  Biofertilizers · Bioagents · Microbes · Rhizosphere · Volatile organic compounds (VOCs)

9.1  Introduction Soil is living and dynamic and the resultant of a million years of evolution. The rhizosphere is the area around the root zone which is very important for a plant to fulfil its water and nutrient requirement. Different microbes form microbial community vis-à-vis plant roots and perform the exchange of chemicals and nutrient cycling in the zone of the rhizosphere (Jacoby et al. 2017). Together the plant exudates and microbial community in the rhizosphere called as ‘microbiome’ are the result of millions of years of co-evolution. C, H, O, N, P, K, Ca, Mg and S are the macro-elements needed by plants to complete their life cycle. In addition, plants also need elements like Fe, Cu, Zn, etc. in traces. Carbon, hydrogen and oxygen are freely available and plants act as great machinery to convert these elements into an organic form from the air and water (Taiz and Zeiger 2000). However, for other macro- and micronutrients, it has to depend upon the soil. Nitrogen, phosphorus and potassium are the three major elements important in the life cycle of the plant which are artificially added into the soil by means of organic and chemical fertilizers (Gouda et al. 2018). The share of the organic fertilizers is very less in comparison to the chemical fertilizers added into the soil on a global scale. A total of 213 million tons of NPK fertilizers were produced in 2016–2017 worldwide, of which 92% was used for agricultural purpose (FAOSTAT 2017). The production of this huge amount of chemical fertilizers requires a great amount of energy and causes environmental pollution as well. Increasing global temperature and eutrophication of water bodies are the reported ill-effects of chemical fertilizers to the environment. Moreover, fertilizer production, distribution and use are a burden to the national exchequer. The fertilizers applied in the soil have limited bioavailability to the plants due to various environmental losses (leaching, chelation, and fixation). Hence, there comes the role of beneficial microbes in the rhizosphere which can increase the bioavailability of the macro- and micro-elements (Reganold and Wachter 2016). Both macro- and micronutrients have an important role in maintaining various physiological and molecular processes and sustaining the structures and functions of plants. Microbes make nutrients available to plants from the rhizosphere and ultimately help in their mobilization in the plant system. Nitrogen, phosphorus and potassium are the key elements involved in plant growth and development. Nitrogen absorption and fixation in the soil are accompanied by Azotobacter, Nitrosomonas and Nitrobacter, respectively. Denitrification and ammonification are the major microbe-mediated processes which make the nitrogen available to plants in nitrate form (Verma et  al. 2016; Yadav et  al. 2017a). The act of solubilization of the

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important minerals is performed by the microbes either directly or by eliciting the response in the plants. Various bacterial genera are involved in potassium uptake, mobilization and solubilization known as potassium-solubilizing bacteria (Sharma et al. 2013; Rana et al. 2019b). Siderophores and organic acids are the elicitor responses from the plants and are released in the soil with the help of microbes. Siderophores help in chelating the elements, and organic acids solubilize various elements to help them convert from unavailable to available form. Iron and zinc ions are made available for plants through chelation-based strategy via Fe/Zn-siderophore complex formation. Siderophores are organic chelators with a very high and specific affinity for Fe+3 and have a less molecular weight (Schalk et al. 2011; Kour et al. 2019c; Yadav et al. 2018b). The lively interaction between the plant roots and microbes improves the soil porosity, aggregation and ultimately soil health. Many beneficial fungi in the soil help in soil aggregation by virtue of their hyphal networks (Degens 1997; Miller and Jastrow 2000). Exudates from the roots, bacteria and fungi; decaying roots, bacteria and fungi; and added organic matter improve the soil structure, function and ultimately the soil health (Yadav et al. 2020). Further, bacteria, fungi, virus and protozoans act as biocontrol agents against various plant pathogens. Various genera of bacteria and fungi are involved in producing variety of lytic enzymes (Yadav et al. 2016a) and signalling molecules (salicylic acid, ethylene, and jasmonic acid) for providing induced systemic resistance (ISR) and systemic acquired resistance (SAR) against plant pathogens (Makandar et al. 2010; Pieterse et al. 2012). Enzymes (ACC deaminase), hormones (IAA) and organic acids are produced by microbes which help in mitigating the multiple abiotic stresses in plants (Brotman et al. 2013). Phytohormones also play a major role in imparting biotic and abiotic stress tolerance to the host plant (Egamberdieva et al. 2017). Bioremediation is the cheapest and eco-friendly microbe-mediated approach for remediating soil and aquifer contamination approach which helps in restoring the fertility of soil. Biological agents including microbes (microremediation), plants (phytoremediation) or both (rhizoremediation) are involved in the bioremediation process (Azubuike et al. 2016). Bioremediation by microbes involves the mechanisms of biosorption, bioaccumulation, aerobic and anaerobic degradation and biotransformation, employing the basic chemical processes of oxidation, binding, immobilization, volatilization and transformation (Yadav et al. 2019c; Rayu et al. 2012; Rana et al. 2019a). The demand for eco-friendly agricultural applications is the key to sustainable agriculture. Agriculture is said to be sustainable when the system is socially supportive, resource-conserving, competitive in the market and environment-friendly. Organic farming is the key player in the sustainable agriculture, admitting the use of organic fertilizers such as bone meal, compost manure and green manure in place of chemical fertilizers (Samac et al. 2003; Yadav et al. 2019b). A number of different soil microorganisms are significantly involved in various biological processes and play an important role in organic farming. Biofertilizers such as living culture of bacteria, fungi and algae alone or in amalgamation enhance the nutrient accessibility to the plants (Mishra et al. 2016). Beneficial microbes in the rhizosphere are commonly called as plant growth-promoting rhizobacteria (PGPR) attributed to their

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ability to enhance plant growth and development (Verma et al. 2017b). However, not only bacteria but other microorganisms like fungi, protozoan, etc. help in improving plant and soil health (Kour et al. 2019b; Yadav et al. 2017b). PGPR have the ability of exogenously synthesizing many phytohormones like auxin, gibberellins, cytokinins, salicylic acid and abscisic acid. These phytohormones are involved in many physiological processes which directly improve the plant growth and development. Owing to all the benefits, the use of PGPR as biofertilizers is steadily increasing in the quest of making agriculture sustainable again. Due to microbe-microbe interaction and interaction of microbes with the plant, the future research is directed towards the finding of appropriate ‘microbial consortia’ which can improve the plant and soil health gradually and can make agriculture sustainable in the long run.

9.2  Mechanisms of Plant Growth Promotion and Soil Health Plants release a large amount of carbon in the rhizosphere that nurtures soil microorganisms. But, what do plants get back? In natural soils, the vast majority of N, P and K atoms are organically bound, while in the atmosphere the vast majority of N is contained in the dinitrogen (N2) molecule. Due to the different metabolic activities of the plants and microbes, the bioavailability of the NPK to plants is variable but can be metabolized by various soil microbes. The genes that involved N, P, K uptake mediated by soil microbes are summarized in (Table 9.1).

9.2.1  Nitrogen 9.2.1.1  Role of Nitrogen in Physiological Processes of Plants Since nitrogen is a central constituent of many structural molecules of the plant, involved in various metabolic processes, it is considered as a paramount element for plant growth. The availability of this essential nutrient enhances the plant’s metabolic processes including absorption, excretion, growth and transportation (https:// www.greenwaybiotech.com). It plays the following significant roles: • Being an essential element in amino acids, it is required for the growth and development of vital plant tissues and cells. • DNA, the genetic material, also has nitrogen as one of the elements. • Nitrogen is a major part of chlorophyll, which is a pigment giving green colour to the plants and essential for the formation of food by photosynthesis. • Regardless of its abundance in the atmosphere, its deficiency due to the addition of other minerals like carbon to the soil leads to severe plant disorders. • Soil retention is favoured by nitrate’s nitrogen. • Nitrogen fertilizers enhance its availability to plants in hydroponic and soil gardening.

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Table 9.1  Genes involved in nitrogen fixation, phosphorus and potassium uptake and solubilization Element Nitrogen

Gene nifD, nifH, nifK

Function Nitrogen fixation

apr, npr, sub

Protein depolymerization

ureA, ureB, ureC

Urea catabolism

Phosphorus phoA, phoD, phoX, ACPase, Phosphate ester cleavage glpQ, ushA, appA, phyA, phyB phnJ, phnX Phosphonate breakdown Potassium

ktr gene KT/KUP/HAK family, homologous to bacterial KUP (TrkD) ktrA and ktrB (Vibrio alginolyticus) Umacu1, Umacu2 (Ustilago maydis and Pichia sorbitophila

Potassium uptake Potassium transporters

References Rasche et al. (2014) Xue et al. (2013a, b) Bowles et al. (2014) Fraser et al. (2015) Bergkemper et al. (2016) Meena et al. (2014)

Bacterial K+ uptake system Encode P-type ATPases of a novel type of K+ transporters

9.2.1.2  Absorption and Fixation of Nitrogen The absorption of nitrates by plants takes place through diffusion and active transport. Nitrogen is passed through the food chain when plants are fed by other organisms. Approximately three-fifths of nitrogen gas present in the atmosphere is fixed by nitrogen-fixing bacteria through biological nitrogen fixation (https://microbiologysociety.org). The conversion of nitrogen from gaseous N2 to ammonia (NH3) requires a complex set of enzymes and consumes 16 moles of ATP. A few nitrogen-­ fixing bacteria carry out this reaction. Free nitrogen is available to plants when free-­ living N2-fixing bacteria are broken down or symbiotic association of some N2-fixing bacteria with plants occurs. 9.2.1.3  Nitrogen-Fixing Bacteria Some aerobic (Azotobacter) and anaerobic (Clostridium) nitrogen-fixing bacteria are free-living, while some other form symbiotic associations with plants including Rhizobium in root-nodulated legumes. Rhizobia form an infection thread in the root hair with the help of root cells of the plant that invades legumes, which then penetrates other neighbouring root cells on branching and proliferates to form a root nodule. Frankia is another genus helping in fixing N in root-nodulated non-legumes, e.g. alder tree (Santi et al. 2013). An enzyme complex, nitrogenase, is found in nitrogen-fixing bacteria that catalyze the formation of ammonia from nitrogen gas. It supplies hydrogen ions and energy in the form of ATP. This enzyme complex has sensitivity towards oxygen

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and becomes inactive in the presence of oxygen. Different nitrogen fixers behave differently when exposed to oxygen: • This problem does not happen in the case of free-living anaerobic bacteria such as Clostridium (Jean et al. 2004). • Azotobacter, being the highest rate of respiration than any other organism, overcomes this problem, thus sustaining with less oxygen in their cells (Oelze 2000). • Accumulation of free oxygen in the cells can destroy the activity of nitrogenase. Therefore, Rhizobium delivers oxygen for the metabolic functions of the bacteroids, when leghaemoglobin contained in it binds to oxygen and inhibits its accumulation (https://microbiologysociety.org). • Frankia and Anabaena carry out fixation in specialized structures known as vesicle and heterocyst, respectively, and exclude oxygen. 9.2.1.4  Nitrification Nitrites are formed from the oxidation of ammonium compounds which are further converted to nitrates with the aid of nitrifying bacteria. Nitrification is a two-step process: 1. Nitrosomonas bacteria convert ammonium ions to nitrites (NO2−), which is lethal to animals and plants in high amounts. 2. Nitrobacter converts nitrites to nitrates (NO3–), which can then be taken in by plants. 9.2.1.5  Denitrification Nitrification is followed by denitrification, in which nitrates are converted mainly into nitrogen gas, but also to nitrous oxide gas by the denitrifying bacteria, e.g. Pseudomonas. Denitrifying bacteria convert nitrate in swampy grounds and highly humid soils having very little oxygen, i.e. the conditions are anaerobic. The bacteria fulfil their requirement of oxygen for respiration from the breakdown of nitrates. The gases formed during the process escape into the atmosphere completing the nitrogen cycle. As the removal of fixed nitrogen from the soil makes it less fertile, this process is regarded as harmful. 9.2.1.6  Ammonification The conversion of different organic forms of nitrogen present in dead organisms and their excretions, into inorganic nitrogen, is called ammonification. The process of ammonification is carried out by the decomposers, which include an extensive range of soil fungi and bacteria. The organic matter and nitrogen present in the dead organism are consumed by the microbes, and they convert that nitrogen to ammonium ions and further to nitrates.

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9.2.2  Phosphorus Being a part of the genetic material of plants, phosphorus (P) is involved in the central dogma of molecular biology. Phosphorus performs a significant function in new tissue formation and cell division. Complex energy transfers carried out by plants also require phosphorus. 9.2.2.1  Role of Phosphorus in Physiological Processes of Plants Phosphorus is accountable for various functions carried out in plants, some of which are the following: • It stimulates the development of root for efficient uptake of nutrients from the soil. • It is required in storage and transportation of the nutrients throughout the plant and in photosynthesis boosting plant development. • Phosphorus is responsible for crop maturity at the right time. Its deficiency increases the maturity time and reduces the number and quality of fruits/seeds. • Nitrogen fixation is also stimulated by phosphorus. • The formation of genes and their development include phosphorus. • Phosphorus also makes the plant resistant to diseases. 9.2.2.2  Mechanism of Inorganic Phosphate Solubilization The production of mineral-dissolving compounds such as hydroxyl ions, organic acids, protons, siderophores and CO2 is the principal process for solubilization mechanism (Sharma et al. 2013). Organic acids are produced in periplasmic space by direct oxidation, cation chelation or pH reduction which acidifies microbial cells and the surroundings to release P (Fig. 9.1). The release of H+ to the external surface with the help of H+ translocation ATPase or in exchange for cation is another mechanism for organic acid production in order to solubilize mineral phosphates. The solubilization of phosphorus without generating any organic acids occurs from the assimilation of NH4+ within microbial cells accompanying the release of protons (Sharma et al. 2013). Gluconic acid is the most recurrent agent for P solubilization by chelating the cations bound to phosphate and making the phosphate available to plants. Another mechanism for this process is enzymolysis carried out by microbes involved in phosphate solubilization in lecithin-containing medium where high acidity caused by enzymes breaks down lecithin into choline (Zhu et al. 2011). 9.2.2.3  Mechanisms of Organic Phosphorus Mineralization Phosphorus mineralization refers to the solubilization of organic phosphorus and the degradation of the remaining portion of the molecule. Organic matter contains a major amount of organic phosphorus (30–50% of the total P in soil), which is mostly

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Inorganic phosphate solubilisation Tartaric acid

Malonic acid

Fumaric acid Glyoxalic acid Asparatic acid Lactic acid

Succinic acid

Organic Acids Gluconic acid

Maleic acid

Periplasmic space

Isobutyric acid Acetic acid

Chelate cations/Reduce pH

Acidification of microbial cells and surroundings

Phosphorus released by substitution of H+ for Ca+2 Fig. 9.1  Inorganic phosphate solubilization

in the form of soil phytate, i.e. inositol phosphate. Additional organic P compounds include phosphodiesters, phosphomonoesters, nucleic acids, phospholipids and phosphotriesters. Moreover, repeatedly releasing into the environment, high molecular weight xenobiotic phosphonates including pesticides, antibiotics and flame retardants also contain organic phosphorus in huge quantities. These compounds are resistant to chemical hydrolysis; therefore, their bio-conversion for assimilation by the cell, to either low molecular weight organic phosphate or soluble ionic phosphate, i.e. HPO42−, Pi, H2PO4−, is required (Peix et al. 2001; Kumar et al. 2016, 2017). The solubilization of organic phosphorus is based on the ‘sink theory’. This refers to the continuous removal of P which results in the dissolution of Ca-P compounds involving different groups of enzymes, known as phytases and non-specific acid phosphatases (NSAPs). Phytases release phosphorus from organic materials in soil (plant seeds and pollen) stored in the form of phytate. NSAPs dephosphorylate the phosphoanhydride and phosphor-ester bond of organic compounds.

9.2.3  Potassium Potassium (K) is a principal abundant macro-element for the survival of living organisms. Being a crucial constituent for the precise development of plants, after nitrogen and phosphorus, it is also termed ‘the quality nutrient’ for its contribution in various biochemical processes in plants (https://www.greenwaybiotech.com). Essentially, potassium is accountable for so many vital processes, viz., transportation of water and nutrient and synthesis of protein and starch.

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9.2.3.1  Role of Potassium in Physiological Processes in Plants • It is required in photosynthesis, for the regulation of plant responses to light through the opening of stomata and its closure, which regulates the uptake of CO2, further resulting in enhancing photosynthesis. • Important biochemical enzymes are being activated by potassium for the generation of ATP. • It plays a role in osmoregulation in plant tissues. • Potassium also accelerates starch and protein production in plants. • Its deficiency leads to chlorosis, stunted growth and poor resistance to ecological changes. 9.2.3.2  Potassium Uptake, Mobilization and Solubilization Bioavailability, the process of uptake and transportation of K in plants through the soil, depends on a number of different factors, the importance of which is the rate of respiration. Its uptake requires sufficient energy of ATP. The various forms of potassium present in the soil include: 1. Mineral K: 90–98% of soil potassium and unavailable for plant uptake, e.g. feldspar and mica. 2. Non-exchangeable K: constitutes 1–10% of soil potassium trapped in between the sheets or layers of clay minerals. 3. Exchangeable K: freely available potassium, absorbed by the plants. It is present on the external layer of clay particles and organic matter. 4. Solution K: 2–5 mg/l for normal agricultural soils. It is directly and readily taken up by plants and microbes in the soil. The solubilization of insoluble K is carried out by a wide range of actinomycetes, fungal strains and saprophytic bacteria through the production of polysaccharides, inorganic and organic acids, acidolysis, chelation, complex lysis and exchange reactions. 9.2.3.3  Action Mechanisms of Potassium Solubilization So far, few studies have been carried out on solubilization of potassium and hence less information is available. Similar to P solubilization, the K solubilization mechanism also includes the production of organic and inorganic acids and protons by acidolysis (Meena et al. 2015) that ultimately convert insoluble K mainly present in biotite feldspar, mica and muscovite to soluble K for easy uptake by the plant (Meena et al. 2014; Verma et al. 2017a; Yadav et al. 2019d). The production of various organic acids by KSBs, effective in releasing K from K-bearing minerals, has been reported, viz., oxalic acid, tartaric acid, gluconic acid, 2-keto-gluconic acid, citric acid, malic acid, succinic acid, lactic acid, propionic acid, glycolic acid, malonic acid, fumaric acid, etc., among which tartaric acid, citric acid, succinic acid,

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α-keto-gluconic acid and oxalic acid are the most prominent acids released (Saiyad et al. 2015). While decreasing soil pH, these acids can release K ions from the mineral K by chelating (complex formation) Si4+, Al3+, Fe2+ and Ca2+ ions associated with K minerals. Microorganisms provide K to plants by storing K in their biomass, which is a fixed form and is potentially available to plants. It was also reported that a few microbes like IAA-producing bacteria, which are a plant growth-promoting rhizobacteria (PGPR), increase secretion from roots and hence deliver K to plants (Etesami et al. 2015). Generally, K solubilization carried out by KSBs is achieved through (i) enhancing cation chelation which is bound to K, (ii) lowering down the pH and (iii) acidolysis of the neighbouring area of microorganism.

9.2.4  Iron and Zinc Iron (Fe) is among the 16 crucial elements for plant growth and reproduction. The role played by iron in plants is very basic as a plant can’t produce chlorophyll without iron, hence, no oxygen and no greenery. Iron is required by the plants in smaller amounts than macronutrients, that’s why it is classified as a micronutrient; however, among the micronutrients, it is required in the largest quantity. Its accessibility is pH dependent on the growth medium. Mostly, plants absorb iron from a chemical present in the soil that gives dirt a distinctive red colour, known as ferric oxide. It is also available from decomposed plant material; therefore, the addition of compost to the soil can help to add iron to plants’ diet. • Iron is involved in the formation of chlorophyll, which is a pigment giving green colour to plants. • Fe helps the plant to move oxygen through its system. • Iron is required for some of the enzyme’s functions in several plants and assists in nitrate and sulphate reduction and energy production within the plant. • Iron is found in the heme proteins of plants, e.g. cytochromes, a major part of electron transfer systems in mitochondria and chloroplasts. • It is also found in certain non-heme proteins such as ferredoxin. Zinc is an essential micronutrient required in optimal amounts, the deficiency of which acts as a yield-reducing factor, particularly in the Asian countries. • Zinc performs an important role in different metabolic processes in plants and its deficiency in crop plants results in significant decreases in both productivity and nutritional quality of the produce. • In plants, zinc is a key component and functional element (cofactor) of around 350 enzymes and proteins. It performs a significant functional role in a wide range of processes, like internode elongation and growth hormone production. • As some photosynthetic enzymes are susceptible to Zn deficiency, it restricts photosynthetic CO2 fixation.

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• It is the only metal which is present in all the six enzyme classes, viz., oxidoreductase, transferase, hydrolases, lyases, isomerases and ligases. • The role of Zn in membrane integrity and stabilization, in the alleviation of oxidative stress and as an intracellular second messenger has also been reported (Gupta et al. 2016). 9.2.4.1  M  echanism of Action Involved in Fe and Zn Uptake, Transport and Accumulation Fe and Zn are vital for the growth of the plant. However, Fe is highly reactive and thus lethal because of the Fenton reaction. The uptake mechanism depends upon the availability of iron. When there is Fe deficiency or Fe overload, plants strongly govern Fe homeostasis. Due to this homeostasis, it eventually affects human nutrition, both in terms of Fe concentration of edible tissues and crop yield. Thus, for breeding crops fortified with essential nutrients and which are more tolerant of Fe-deficient soils, the mechanisms of action for Fe uptake and transport have to be deciphered. Plants commonly take Fe and Zn from the rhizosphere. As a result, if Fe is deficient, it can change the chemical and physical properties of rhizospheric soils, which in turn affect microbes found in the rhizosphere and their abundance. Fe deficiency induces root exudates, which transform the microbial population in the rhizosphere by modifying the antimicrobial and growth-promoting effects and physicochemical properties of the soil. This altered microbial community further benefits plant Fe attainment via the production of phytosiderophores (PS) and protons, improving the bioavailability of iron in the soil, and through hormone production triggering the enhancement of Fe uptake capacity in plants. Moreover, symbiotic interactions between host plants and microbes could also increase plant Fe uptake, including Rhizobium nodulation augmenting the capacity of the plant to take Fe and mycorrhizal fungal infection which increases root length and the area of nutrient attainment of the root system, in addition, to increase in the production of Fe3+ chelators and protons. 9.2.4.2  Reduction-Based Strategy (Strategy I) Reduction-based strategy (strategy I) is best explained in Arabidopsis but also characterized in some non-graminaceous species. This strategy depends upon the acidification of the rhizosphere that upsurges the solubility of ferric compounds through trans-plasma membrane electron transfer and proton extrusion to reduce iron to more soluble form through ferric chelate reductase (FRO2) and further transportation of Fe into root cells by iron-regulated transporter 1 (IRT1). Strategy I in Zn uptake involves efflux of organic acids, reductants and H+ ions, which increase the solubility of Zn complexes and release Zn2+ ions for absorption by root epidermal cells. The organic acids released either in root exudates, mucilage

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or directly by epidermal cells include malic acid, citric acid, oxalic acid or tartaric acid, etc. 9.2.4.3  C  helation-Based Strategy (Strategy II): Via Fe/Zn-Siderophore Complex Formation Siderophores are organic chelators with very high and specific affinity for Fe+3 and have less molecular weight. As a consequence of less solubility of Fe hydroxides in aerobic soils with abundant calcium (calcareous soil), Fe becomes deficient in those types of soils; therefore, to tackle this problem of less Fe availability, several microbes produce and release siderophores (Schalk et al. 2011). Siderophores form siderophore-Fe complexes which increase Fe solubility by chelation (Saha et  al. 2012). The production of siderophores in the rhizosphere has been suggested to be the vital microbial activity that benefits plant Fe acquisition due to their solubilizing effect on Fe hydroxides. In a cultivation study of soil, it was perceived that Fe attainment of common bean plants was enhanced by siderophore-producing microorganisms (Carrillo-Castañeda et al. 2005). Furthermore, various microbial Fe-siderophore chelates have been reported to serve as good sources of Fe for plants, viz., Fe-ferrioxamine for oat (Crowley et  al. 1991), Fe-pyoverdine (Arabidopsis) (Vansuyt et  al. 2007), Fe-aerobactin for oat and soybean (Chen et  al. 1998) and Fe-rhizoferrin for barley, corn and tomato (Yehuda et al. 2000) using hydroponic culture. Furthermore, on incubation of Pseudomonas with phenolic root exudates of Fe-deficient red clover plants, it secretes a siderophore that dissolves Fe from an insoluble Fe source, and that dissolved Fe is easily exploited by plants (Jin et al. 2010). Grasses largely depend on the acquisition of Fe chelated by soluble siderophores with a high affinity for Fe3+. When Fe is deficient, phytosiderophores of the mugineic acid family are synthesized from L-methionine and released from the root epidermis, through anionic channels or vesicles. In barley, the genes required for methionine synthesis, PS synthesis and sulphur uptake are radically upregulated in the first 24 h of Fe deficiency. In rice, the expression of the OsIRO2 transcription factor increases dramatically during the first 5 days of Fe starvation and is supposed to activate the expression of genes related to PS synthesis and Fe uptake. The Fe(III)-PS complexes thus formed are then transported via a high-affinity uptake system to the root epidermis. The chelation strategy is less pH sensitive than the reduction strategy, and the resistance to Fe-limiting soils and the volume of PS released are strongly correlated (Morrissey and Guerinot 2009). A similar mechanism is followed in the case of Zn uptake via Zn-siderophore complex formation. Mycorrhizae excrete low molecular weight organic chelating compounds such as citric acid, oxalic acid and siderophores as well as H+ (Bharadwaj et  al. 2012), which enable the movement of less available Fe in the rhizosphere soil and therefore also supposedly endorse plant Fe and Zn acquisition.

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9.3  Microbe-Plant Interactions Phytohormones or plant growth regulators play a vital role in the growth and development of the plant. Their production is non-localized in plants, unlike many animals which have specialized glands meant for their production. However, their action may be stage and site specific as it regulates activities like gene expression, cell division, cell differentiation and cell enlargement (Taiz and Zeiger 2000). Both endogenous and exogenous applications of growth regulators are found to affect plant growth and development (Yadav 2017). There are plenty of microbes capable of producing phytohormones exogenously and thus are highly beneficial to the plant health (Egamberdieva et al. 2017; Yadav et al. 2018a). Plant root exudates the carbon compounds in the form of various sugars, organic acids, mucilages, amino acids, etc. which act as a food source for the microbial community in the rhizosphere (Bais et al. 2006). The amount and type of carbon compound released in the rhizosphere depend upon the type of plant (maize, barley, pea, etc.) and have genotype specificity as well (Bulgarelli et al. 2015). Rhizodeposition of the energy-rich carbonic compounds can also attract harmful pathogenic microorganisms, and thus, plants have developed mechanisms to selectively attract and repel microorganisms through root-derived signals. The chemical released by plant roots includes terpenoids, flavonoids, strigolactones, etc. (Bais et al. 2006; Massalha et al. 2017) which possess the differentiating abilities in the form of either attracting or repelling the selective microbes. Flavonoids play an important role in inducing NOD gene expression in Rhizobium for increased root nodulation in leguminous plants and promoting hyphal branching for mycorrhizal interactions, thus improving both plant and soil health (Abdel-­ Lateif et al. 2012; Weston and Mathesius 2013). However, not only plants through their root exudate exclude pathogenic microorganisms, there are plenty of microbes helping plants in their endeavour, thereby benefitting themselves to colonize in a larger amount. Thus, it is a complex system of plant-microbe and microbe-microbe interaction. There are reports of microbes releasing antibiotics, bactericidal proteins, HCN, siderophores and enzymes like chitinase, cellulase, lyases, etc. to ward off the pathogenic bacteria and fungi (Solano et al. 2009). Antibiotics not only suppress pathogenic bacterial growth but also induced systemic resistance in plants (Jha et al. 2011a, b). Vitamins are another class of organic molecules released in the root exudates for microbial growth and development (Mozafar and Oertli 1993). In turn, certain microbes also produce vitamins, benefitting the plant health (Dahm et  al. 1993). Pseudomonas fluorescence colonizes in larger number and helps Rhizobium in N2 fixation due to its vitamin-producing ability (Marek-Kozaczuk and Skorupska 2001). Together the type of root exudates and signals govern the type of microbiome flourishing around the rhizosphere (Hartmann et al. 2009; Massalha et al. 2017). Conversely, bacterial genus, species and strain have many roles to play in the type of hormone produced exogenously (Boiero et al. 2007). Thus, it becomes a win-win situation for both plant and microbiome in the rhizosphere. Sequence analysis and

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genome-wide association studies (GWAS) have helped to understand the taxonomical composition of the microbiome around the plant. In Arabidopsis thaliana, GWAS has helped in identifying single-nucleotide polymorphisms (SNPs) associating to the quantitative phenotypes of root and leaf around the microbiome. Microbiome around the plant helps in improving quantitative traits like cell wall synthesis, cuticle synthesis, ethylene signalling, primary and lateral root proliferation, fresh weight gain in roots, etc. The genetic loci associated with such traits have been reported in the past (Horton et al. 2014; Wintermans et al. 2016).

9.3.1  Phytohormones and Volatile Organic Compounds Auxins, cytokinins, gibberellins and ethylene are the important plant growth regulators whose relative proportion in the plant dictates the development of either roots or shoots (Taiz and Zeiger 2000). Several microbial genera like Azospirillum, Pseudomonas, Klebsiella, Rhizobium, Mesorhizobium, Bradyrhizobium, Paenibacillus and Bacillus are reported to increase the root volume by facilitating the increase in lateral roots, adventitious roots and root architecture (Egamberdieva et al. 2017; Kumar et al. 2019; Yadav et al. 2017b, c) (Table 9.2). Indole acetic acid (IAA) is the predominant auxin produced by these microbes to increase the surface area of the roots, thereby benefitting themselves to colonize in masses and benefitting much fold to the inhabitant plant to extract more nutrients and water from the soil attributed to enlarged root surface area (Ahemad and Kibret 2014). IAA is important for bacterial own physiology as it is found to be a bacterial signalling molecule (Spaepen et al. 2007). Gibberellins are also reported to act as signalling molecule towards the host plant, thereby inducing growth and development as reported for a few species in Azospirillum and Bacillus (Bottini et  al. 2004; Gutierrez-Manero et al. 2001; Yadav et al. 2019d). IAA can be produced by either L-tryptophan-dependent or L-tryptophan-independent pathway. However, a meta-­ analysis in more than 7000 prokaryotic genomes showed L-tryptophan-dependent pathway predominantly operating in the rhizospheric microbes where IAA can be synthesized from tryptophan or intermediates (Zhang et  al. 2019). L-tryptophan-­ enriched soils are reported to increase IAA concentration in leaves and found to have positive effect on plant growth and development (Lee et al. 2012). Several bacterial strains such as Pseudomonas stutzeri, Stenotrophomonas maltophilia and Pseudomonas putida were visualized to have a commercial bioformulation possibility due to their ability to produce indole-3-acetic acid (IAA), gibberellic acid and cytokinin (kinetin and 6-benzyladenosine) (Patel and Saraf 2017). The release of volatile organic compounds (VOCs) by the microbes in the rhizosphere is another indirect way of affecting plant growth and development. Arthrobacter agilis, Bacillus spp., Burkholderia pyrrocinia, Chromobacterium violaceum, Pseudomonas fluorescens, Azospirillum brasilense, etc. are some of the bacterial species capable of producing various kinds of volatile organic compounds (Yadav and Yadav 2018; Santoro et  al. 2011). 2-Pentylfuran (Zou et  al. 2010),

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Table 9.2  List of PGPR involved in the release of different phytohormones for various abiotic stresses in important agricultural and horticultural crops Crop Wheat

Barley Rice

PGPR Streptomyces isolates C, B. pumilus, Pseudomonas mendocina, Arthrobacter sp., Halomonas sp., Nitrincola lacisaponensis Pseudomonas sp., Pseudomonas lurida strain M2RH3, Exiguobacterium acetylicum strain 1P (MTCC 8707)

Hormone IAA

Bacillus licheniformis, Bacillus subtilis, Arthrobacter sp., Marinobacterium sp., Pseudomonas sp., Rhizobium sp., Sinorhizobium sp., Acinetobacter faecalis, Bacillus cereus, Enterobacter hormaechei, Pantoea agglomerans, Streptomyces coelicolor, Streptomyces geysiriensis Azospirillum lipoferum

IAA

IAA

P. putida (N21), P. aeruginosa (N39), Serratia proteamaculans (M35) Azospirillum lipoferum

ACC deaminase GA

Staphylococcus arlettae strain Cr11

IAA and ACC deaminase IAA

Curtobacterium flaccumfaciens, Ensifer, garamanticus Enterobacter cloacae GS1, Bacillus sp. SVPR30, P. polymyxa ATCC, 10343

IAA

IAA

IAA

Agrobacterium sp. SUND BDU1, Bacillus sp. strains SUND LM2, Can4, Can6 Bacillus amyloliquefaciens

ABA

Herbaspirillum seropedicae

GA

Normal/ stress Salinity stress

References Sadeghi et al. (2012) and Tiwari et al. (2010) Heat and Mishra et al. cold stress (2011) and Selvakumar et al. (2011) Salt stress Singh and Jha (2016), Sorty et al. (2016) and Egamberdieva (2009)

Normal conditions Salinity stress Drought stress Heat and cold stress

Belimov et al. (2004) Zahir et al. (2009) Creus et al. (2004) Sagar et al. (2012)

Salt stress Cardinale et al. (2015) Normal Shankar et al. conditions (2011) and Beneduzia et al. (2008) Salinity Barua et al. stress (2012) Salt stress Shahzad et al. (2017) Normal Araujo et al. conditions (2009) (continued)

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Table 9.2 (continued) Crop Maize

Sorghum

Sunflower

PGPR Hormone Acinetobacter CR 1.8, Klebsiella SN 1.1, IAA Azospirillum brasilense, Bradyrhizobium japonicum Azotobacter sp. C5, C7, C8 and C9 IAA Pseudomonas strains 3–3.5-1, TLC 6–6.5-1, TLC 6–6.5

IAA

Pseudomonas sp.

IAA

Leifsonia sp., Bacillus sp.

IAA

Serratia marcescens

SA

Micrococcus luteus

CK

Pseudomonas sp. DGS6

A. brasilense SM

IAA and ACC deaminase IAA

Pseudomonas sp. strain AKM-P6

IAA

Bacillus sp. SLS18

IAA and ACC deaminase IAA

P. fluorescens biotype F and P. fluorescens CECT 378T Pseudomonas strains 3–3.5-1, TLC 6–6.5-1, TLC 6–6.5 Achromobacter xylosoxidans, Bacillus pumilus Pseudomonas sp. DGS6

IAA

SA IAA and ACC deaminase

Normal/ stress References Normal Chaiharn and conditions Lumyong (2011) Salinity Rojas-Tapias stress et al. (2012) Heat and Li and cold stress Ramakrishna (2011) Mishra et al. Salt and (2017) heat stresses Cd stress Ahmad et al. (2016) Salt stress Lavania and Nautiyal (2013) Drought Raza and stress Faisal (2013) Heat and Yang et al. cold stress (2013) Normal Malhotra and conditions Srivastava (2009) Heat and Ali et al. cold stress (2009) Heat and Luo et al. cold stress (2012) Salinity stress Heat and cold stress

Shilev et al. (2012) Li and Ramakrishna (2011) Drought Forchetti stress et al. (2010) Heat and Yang et al. cold stress (2013) (continued)

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Table 9.2 (continued) Crop PGPR B. napus/B. Bacillus subtilis juncea Achromobacter xylosoxidans Ralstonia sp. J1-22-2, P. agglomerans Jp3-3, Pseudomonas thivervalensis Y1-3-9 A. xylosoxidans Ax10

Cotton

Streptomyces cyaneofuscatus ZY-153, S. kanamyceticus B-49, S. rochei X-4, S. flavotricini Z-13 Serratia plymuthica, Stenotrophomonas rhizophila, Pseudomonas fluorescens, Pseudomonas extremorientalis

ACC deaminase

IAA and ACC deaminase Fungal cell wall degrading enzymes IAA

Phoma glomerata, Penicillium sp.

GA

Ochrobactrum haematophilum H10

Burkholderia sp.

IAA and ACC deaminase IAA, GA, ABA Auxin production IAA

Bacillus amyloliquefaciens CM-2, T-5

IAA

Trichoderma asperellum Tomato

IAA

IAA and ACC deaminase IAA and Achromobacter sp., Klebsiella sp., ACC Pseudomonas sp., Pantoea sp., Chryseobacterium sp., Methylobacterium deaminase fujisawaense strains CBMB 20, CBMB 10 P. putida Rs-198 IAA Raoultella planticola Rs-2

Cucumber

Hormone IAA

B. subtilis FZB24 and FZB41

P. fluorescens NT1, P. aeruginosa T15, P. ACC stutzeri C4 deaminase Pseudomonas strain, PCI2 Fungal cell wall degrading enzymes

Normal/ stress Ni stress

References Zaidi et al. (2006) Cu stress Ma et al. (2009) Heat and Zhang et al. cold stress (2011)

Heat and Ma et al. cold stress (2009) Normal Madhaiyan conditions et al. (2008)

Salinity stress Drought stress

Yao et al. (2010) Wu et al. 2012

Pathogen

Xue et al. (2013a, b)

Salt stress Egamberdieva et al. (2011) and Egamberdieva et al. (2013) Drought Waqas et al. stress (2012) Normal Zhao et al. conditions (2012) Salt stress Zhao and Zhang (2015) Salinity Stavropoulou stress (2011) Cd stress Dourado et al. (2013) Pathogen Tan et al. (2013) Salinity Tank and stress Saraf (2010) Pathogen Pastor et al. (2012)

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2,3-butanediol, acetonin (Ryu et al. 2003), jasmonates, cyclohexanes, methyl decane, 1-chlorooctadecane, tetradecane (Kanchiswamy et al. 2015), etc. are the volatile chemicals released by the PGPR to communicate with the plants. VOCs released in sufficient amount act as a signalling molecule to trigger the plant response against various bacterial and fungal pathogens and induced systemic resistance (ISR) (Santoro et  al. 2016). They are reported to increase biomass (Velazquez-Becerra et  al. 2011), chlorophyll content (Orozco-Mosqueda et  al. 2012) and oil content (Santoro et al. 2011) in some of the plant species.

9.3.2  M  icrobe-Mediated Stress Mitigation Through Phytohormones Abiotic stresses such as salinity, drought, heavy metals, etc. are reported to decline auxin (Hu et al. 2013), cytokinin and gibberellin (Atici et al. 2005) concentration in the plants. IAA in low concentration is found to increase tolerance towards Pb, Zn (Fässler et al. 2010), Al (Wang et al. 2016) and Cd (Ahmad et al. 2016) toxicities. Moreover, auxins indirectly help the plant by inducing other hormones, i.e. gibberellins and salicylic acid, to mitigate the abiotic stresses (Wolbang et  al. 2004). Similarly, kinetin is reported to act against Cd toxicity and salt stress (Singh and Prasad 2014). Cytokinins produced by the various bacterial strains like Micrococcus luteus, Bacillus subtilis, Arthrobacter, Azospirillum, Pseudomonas, etc. are reported to increase root and shoot biomass (Raza and Faisal 2013). Abscisic acid (ABA) provides a tolerance mechanism to the plants by inducing root growth, anti-transpiration, reduction in canopy area and expression of ABA-­ induced stress-responsive genes (Sah et al. 2016). Exogenous application of ABA has helped in mitigating the abiotic stress in various crops, viz., wheat, rice, potato, tea, maize, citrus, etc. (Egamberdieva et al. 2017). Abscisic acid (ABA)-producing PGPR such as B. megaterium, B. licheniformis, B. cereus, B. amyloliquefaciens, Klebsiella pneumoniae, Proteus mirabilis, P. fluorescens, etc. (Karadeniz et  al. 2006) helps the host plant to mitigate osmotic stress by inducing ABA synthesis in the roots (Shahzad et al. 2017). Gibberellins are also reported to stimulate growth and development and impart osmotic stress tolerance to plants (Tuna et al. 2008). Several bacterial strains, viz., Bacillus amyloliquefaciens, Acetobacter sp., Bacillus pumilus, Bacillus licheniformis, etc., and endophytic fungi, viz., Aspergillus fumigatus, attached to the roots of crop plants synthesize various kinds of gibberellic acid (Bottini et al. 2004; Khan et al. 2011). Salicylic acid (SA) released by the microbes helps the plants to fight against abiotic stresses by elevating the levels of ABA, proline and various other osmolytes (Shakirova et al. 2003) and decreasing the ethylene levels (Khan et al. 2014). Salicylic acid (SA)-producing bacteria like A. xylosoxidans, B. licheniformis, B. pumilus and Serratia marcescens are reported to enhance host plant tolerance towards drought and salt stress (Forchetti et al. 2010; Lavania and Nautiyal 2013).

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9.4  Biofertilizers Modern agriculture suggests the deployment of high-yielding cultivars/varieties and hybrid seeds. However, chemical fertilizers and irrigation affect them badly, and their continuous use pollutes and contaminates the soil and water bodies, resulting in depletion of essential organic matter and necessary soil nutrients. It results in the reduction of beneficial microorganisms and insects, thereby decreasing the fertility of the soil, making crops prone to diseases and threatening long-term farm productivity. The demand for eco-friendly agricultural applications is increasing dramatically which is further driving the use of microbe-based fertilizers, known as biofertilizers. Biofertilizers are defined as the living culture of bacteria, fungi and algae alone or in an amalgamation that enhances the nutrient accessibility to plants. These biofertilizers have special significance in agriculture especially to small and marginal farmers, particularly in the context of unaffordable prices of chemical-based fertilizers and their menacing effects on soil health. Biofertilizers, when applied through seed or soil, interact with the rhizosphere, thus helping in nutrient uptake by the plants. Due to multifaceted plant growth-promoting characteristics of microbes, they can be employed as biofertilizers for crop improvements and soil health for sustainable agriculture and are referred to as BSMs, the beneficial soil microbes (Mishra et  al. 2016; Rana et  al. 2019b). BSMs are majorly categorized as plant growth-promoting rhizobacteria (PGPR) and plant growth-promoting fungi (PGPF) (mycorrhiza) and cyanobacteria in sustainable agriculture (Fig. 9.1).

9.4.1  Plant Growth-Promoting Rhizobacteria These microbes colonize the plant root facilitating plant growth (Goswami et  al. 2016). The production of phytohormones, nitrogen fixation and siderophores synthesizing inorganic minerals [phosphorus (P), potassium (K) and zinc (Zn) solubilization] to make them ready for plant growth come under the direct role of PGPR, whereas growth inhibition activities against phytopathogens describe their indirect role (Yadav et al. 2017c, 2019b). These are also regarded to be the potential plant rescuers from various environmental stresses (Kang et al. 2013) while helping in the restoration of degraded land and reducing environmental pollutants from the soil.

9.4.2  Plant Growth-Promoting Fungi An extensive variety of valuable and pathogenic fungi is present in the soil that affects plant parts at different phases. The content of soil nutrient is an important feature that affects the propagation and biological activity of plant growth-­promoting

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fungi. The fungi of different classes and habitations act as PGPF, including the most prevalent PGPF fungal genera Aspergillus, Fusarium, Penicillium, Piriformospora, Phoma and Trichoderma (Yadav et al. 2019a). The interaction of PGPF with plants affects all the plant organs positively, including the noteworthy improved germination, biomass production, seedling vigour, flowering, development of root hairs, photosynthetic efficacy and yield (Hossain et al. 2017).

9.4.3  Cyanobacteria The cyanobacteria, commonly called blue-green algae, multiply and fix atmospheric N2, thus releasing the nitrogen into the environment in the form of building blocks, i.e. amino acids and growth-promoting substances. The biomass of cyanobacteria acts as a good source of biofertilizer which improves physicochemical properties of soil including nutrients and water-holding capacity of the disturbed and degraded lands. Cyanobacteria have some exclusive features, viz., universal occurrence, less generation time and atmospheric N2-fixing properties. These bioinoculants are helpful in improving soil fertility and environmental quality (Singh et al. 2016). On the basis of their mode of action (Fig. 9.2), PGPR, PGPF and cyanobacteria are further divided into: 1. Nitrogen fixers: Rhizobium spp., Azospirillum spp., Azotobacter spp., Cyanobacteria, Azolla, Nostoc 2. Phosphate solubilizers: Pseudomonas, Bacillus subtilis, Rhizobium, Burkholderia, Mycorrhiza, Phosphaticum, B. circulans

BIOFERTILIZERS

(On the basis of their mode of action) Azospirillum spp. Azotobacter spp. Penicillin bilaiae Pseudomonas

Azolla

Cyanobacteria Rhizobium spp.

Nitrogen fixers Phosphate solubilisers Glomex sp. Mycorrhiza

Acaulospora sp. Gigaspora sp. Scutellospora

Phytohormones producers Bacillus

Burkholderia

Zinc solubilisers

Phosphate mobilizing

Potassium solubilisers Fig. 9.2  Classification of biofertilizers on the basis of their mode of action with major examples

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Zinc solubilizers: Bacillus, Pseudomonas Potassium solubilizers: Bacillus, Burkholderia, Pseudomonas Phosphate mobilizing: Acaulospora spp., Gigaspora spp., Scutellospora Phytohormone producer: Bacillus, Rhizobium, Burkholderia, Mycorrhiza Vesicular Arbuscular Mycorrhiza

9.4.4  Mode of Action of Biofertilizers 9.4.4.1  Rhizobium Rhizobium is a symbiotic bacterium, which occurs in the roots of different legumes and pulses, produces nodules and fixes atmospheric dinitrogen inside the nodules. Rhizobium inoculants are the best known inoculants exploited for their symbiotic nitrogen-fixing ability and also known to increase the grain yields in lentil (Rashid et  al. 2011), pea, alfalfa, berseem (Hussain et  al. 2002), bengal gram (Patil and Medhane 1974), groundnut (Sharma et al. 2011), soybean (Grossman et al. 2011) and sugar beet (Ramachandran et al. 2011) in diverse locations and soil types. The widespread genera used are Azorhizobium, Allorhizobium, Bradyrhizobium, Mesorhizobium and Sinorhizobium (https://www.mordorintelligence.com). 9.4.4.2  Pseudomonas Pseudomonas is one of the best-characterized biocontrol PGPR. Fluorescent pseudomonads are appropriate to be applied as biocontrol agents because of their abundance in natural soils and in the plant-root system and their ability to use plant exudates in the form of the nutrient. Furthermore, Pseudomonas also possesses traits for plant growth, viz., nitrogen fixation, iron chelation, phytohormone production and phosphate solubilization. Such multi-dimensional efficacy of fluorescent Pseudomonas makes them a bioagent of choice to be exploited in the field of agriculture (Panpatte et al. 2016). 9.4.4.3  Bacillus Due to the power of persistence in different biotic and abiotic environments, Bacillus spp. have been recognized as principal populations among various other species of PGPB. Biofertilizers based on Bacillus are more dynamic as compared to that based on Pseudomonas because the former has a spore-forming property and also produces metabolite more effectively, which boosts the sustainability of cells in commercially available formulations of biofertilizers (Radhakrishnan et al. 2017; Verma et al. 2019) (Table 9.3).

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Table 9.3  Commercially available single strain biofertilizers Microbe Rhizobium Cyanobacterium Bacillus VAM Pseudomonas Azospirillum Azotobacter Acetobacter

Commercially available biofertilizers Rhizobium biofertilizer, Green Rhizo, Cell-Tech, Agrolutions, Rhizolutions Blue-green algae Phosphomax (B. Megaterium), Mitushi B. subtilis, Rudra B. amyloliquefaciens, Anand Agro Care B. subtilis MYKO-WIN, MYKO-JNN, BioVam, Nutrich, OK VAM, Agri Life Agri VAM, BIOPROMOTER VAM MONAS, BioStar NitroMax, Genewin Biotech, AzospiPower, Manidharma White Azospirillum K-AZO, Varsha Azotobacter, ORGA-AZOTO ACETOPOWER, ORGA-ACT, Orgogrowth, BioAceto

9.4.4.4  Vesicular Arbuscular Mycorrhiza Mycorrhizae are the symbionts with root and get the nutrients from the plant and deliver minerals such as N, P, K, S, Zn and Ca to the host plant. The deployment of cost-effective, energy-efficient and environment-friendly VAM fungi as a biofertilizer is a promising approach. Roots colonized by VAM fungi, sometimes, also anchor more actinomycetes which compensate the nutrient absorption system from damage to roots by pathogens (Secilia and Bagyaraj 1987). The importance of VAM in supplementing the production of food is widespread and, therefore, can be deployed in sustainable agriculture. 9.4.4.5  Azospirillum It is commonly present in cereals inhabiting root cells and their surroundings. It increases the nitrogen-fixing potential of the cereal plant while staying in a symbiotic relationship with the cereal plant. It can fix 20–40  kg/ha nitrogen in non-­ leguminous plants such as cereals, cotton, millets, oilseeds, etc. Azospirillum inoculants are available commercially as nitrogen-supplying biofertilizer and save approximately 25–30% of the nitrogenous fertilizers. 9.4.4.6  Azotobacter It is present in neutral arable and alkaline soils of India and considered as a heterotrophic free-living nitrogen-fixing bacteria that can also synthesize growth-­ promoting substances like auxins, gibberellins and vitamins (up to a small extent). Several strains also possess fungicidal properties. Cotton, maize, pearl millet, rice, sugarcane, vegetables and a few plantation crops are benefitted. It is the heaviest living organism which requires a huge amount of organic carbon for its growth and fixes 20–40 mg N/g of C source.

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9.4.4.7  Azolla It is a naturally available branched free-floating fern, commonly found in humid soils, trenches and marshy ponds, and fixes N in the soil in the form of NH4+ ion which is available as a soluble N for the rice crop. The application of 10–12 tonnes/ ha Azolla increases soil N by 50–60 kg/ha, thus reducing 30–35 kg of N fertilizer requirement of rice. 9.4.4.8  Acetobacter It benefits only sugarcane crop. Under field conditions, sugarcane yield increases after Acetobacter inoculation and production of auxins and substances similar to antibiotics have also been observed. It has a capacity of solubilizing inorganic phosphorus. 9.4.4.9  Actinomycetes Reports on the inclusion of actinomycetes in the soil to use it as a biofertilizer are limited. However, a study carried out by Pragya et al. (2012) suggested that the use of actinomycetes isolates in multifunctional biofertilizers improves the soil fertility. 9.4.4.10  I ndividual Strains vs. Microbial Consortia Approach – Recent Trends Numerous single strain inoculants with biofertilizer functions are commercially available these days. However, with the purpose to exploit beneficial additive interactions and enhance the flexibility of responses in diverse environmental conditions, combination products based on microbial and non-microbial biostimulants are increasingly being used. These consortiums can be endosymbiotic or ectosymbiotic. Microbial consortia products, abbreviated as MCPs, are made up of compatible strains of microbes having different mechanisms of action to provide an extensive range of usage. Diverse strains are selected on the basis of their functions and survivability in different environments, such as soil pH, moisture and temperature. The idea behind these types of products is built on the hypothesis that members of the microbial communities used as inoculants are selectively stimulated by signals given by the rhizosphere and ecophysiological responses of the host plant, under diverse environmental conditions, to have prompt benefits on plant growth. On the other hand, the cost of single strain production is also very high as compared to that of microbial consortia. Inoculation with different PGPR with/without arbuscular mycorrhiza alone usually results in enhanced growth and yield through improved nutrient uptake, as compared to using single inoculant. In a study carried out by Akintokun and Taiwo (2016), single culture and the consortium of microbes were compared and found better and consistent than single inoculants in the case of

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tomato, where four isolates, Bacillus subtilis, Pseudomonas aeruginosa, Klebsiella pneumoniae and Citrobacter youngae, were compared. In another study, nodule number was quadrupled when plants were supplied with a combination of Glomus deserticola and Rhizobium trifolii; in comparison to single R. trifolii, the inoculation and improved mycorrhization and nodulation were acquired with co-­ encapsulated R. trifolii and Yarrowia lipolytica (Vassilev et  al. 2001). All these instances suggest usefulness and higher efficiency of biofertilizers composed of more species having different mechanisms of growth promotion. The availability of several strains of PGPR (Lucy et al. 2004) and arbuscular mycorrhizal fungi (AMF) (Koide and Mosse 2004) tested in different crop species and under different field conditions should allow the definition of consortia suitable for commercial uses. Some of the examples of commercially available multi-strain consortia are Bio-­ N® consisting of two species of the nitrogen-fixing bacteria Azospirillum isolated from the roots of a Saccharum spontaneum L. It can fix and convert atmospheric nitrogen into a usable form and improve shoot growth and development of root, thus making plant pest resistant and drought tolerant, reducing chances of rice tungro, corn earworm and corn borer infestation and increasing yield and milling recovery of rice and corn (FNCA 2007). Other multi-strain consortia are Bio-Spark® which is a microbial inoculant consisting of three different species of Trichoderma (T. parceramosum, T. pseudokoningii and UV-irradiated strain of T. harzianum). Such combinations of microbial isolates that can be developed as multifunctional biofertilizers would be a good opportunity for sustainable agriculture.

9.5  M  icrobes as Biocontrol Agents/Microbes in Biotic Stress Tolerance Plant and soil health are affected by various factors. Microorganisms improve soil and plant health by imparting biotic and abiotic stress tolerance. There are various genera of bacteria, fungi, protozoans, etc. which act as biocontrol agents. Plants in the natural environment are exposed to a number of pathogenic bacteria, fungi and protozoans which cause the ailment in the plants that ultimately results in the reduction of yield and productivity (Yadav et al. 2015, 2016b). Therefore these ailments need to be suppressed to maintain the nutritional status and plant health. A number of approaches are there to control biotic stresses and maintain plant health: (1) chemical uses of fungicides and pesticides but have severe limitations due to persistence in the environment; (2) conventional plant breeding, which is more time-­ consuming and requires a resistant source; (3) genetic engineering for developing genetically modified organisms (GMO) which are not favoured by various nations due to GM regulations. A novel environment-friendly approach, i.e. the use of biocontrol agents, presents an opportunity to strengthen natural plant defence which minimizes yield loss and maintain plant health (Table 9.4). Plant root exudates hydrogen ions, water, mucilaginous substances and enzymes which act as a signalling agent to attract beneficial microorganisms to the plant rhizosphere. Biocontrol agents include predator’s parasitoids and microorganisms

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Table 9.4  Biocontrol agents for various plant pathogens Biocontrol agent A. radiobacter strain 84 A. radiobacter strain K 1026 Azospirillum spp. B. subtilis strain Bacillus thuringiensis Pseudomonas spp. P. aureofaciens strain TX-1 P. chlororaphis P. chlororaphis strain P. fluorescens strain A506 P. syringae ESC10 and ESC11 P. cepacia P. fluorescence Streptomyces spp. Streptomyces griseoviridis K61 Trichoderma viride T. harzianum T. harzianum T-22 T. harzianum T-39 T. harzianum, T. polysporum, T. viride T. harzianum

Target pathogen/crop A. tumefaciens A. tumefaciens

References Butt et al. (2001) Junaid et al. (2013)

Paddy, millets, oilseeds, fruits, vegetables, sugarcane, banana Rhizoctonia, Fusarium, Aspergillus, Pythium, Phytophthora R. solani, all phytopathogen Rhizoctonia solani Pythium, Rhizoctonia solani

Junaid et al. (2013) Burges (1998) Shaikh and Sayyed (2015) Berg (2009) Butt et al. (1999, 2001)

Leaf stripe, net blotch, leaf spot, etc. on Mark et al. (2006) barley and oats Leaf stripe, net blotch, spot blotch, leaf Haissam (2011) spot Fire blight, bunch rot Junaid et al. (2013) Penicillium spp., Mucor piriformis, Geotrichum candidum Bipolaris maydis Erwinia carotovora, Puccinia, Fusarium S. sclerotiorum Phomopsis spp., Botrytis spp., Pythium spp., Phytophthora spp. Sclerotium rolfsii Rhizoctonia solani, Sclerotium rolfsii, Pythium and other fungal diseases Pythium spp., Rhizoctonia solani, Fusarium spp. Botrytis cinerea Wilt-causing fungi, soil and foliar pathogens Botrytis cinerea, Meloidogyne javanica

Burges (1998) Shaikh and Sayyed (2015) Shaikh and Sayyed (2015) Shaikh and Sayyed (2015) Mark et al. (2006) Hirpara et al. (2017) Haissam (2011) Berg (2009) Berg (2009) Burges (1998) Sahebani and Hadavi (2008) and Puyam (2016)

(bacteria, fungi, virus, protozoans, etc.) which act as beneficial agents for maintaining the plant health. In addition to plant growth-promoting rhizobacteria (PGPR), plant growth-promoting bacteria (PGPB) and growth-stimulating fungi also provide protection against biotic stresses. Plants communicate with microbes through various signalling molecules during plant-microbe interactions. Microbes are capable of releasing various compounds which are recognized by plants and ultimately impart defence against biotic stresses. The plant and microbe interaction leads to the activations of systemic and local defence by plant signalling molecules such as jasmonic acid (JA), salicylic acid (SA) and ethylene (ET). Plants can detect directly extracellular molecules referred to as microbe-associated molecular patterns or

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pathogen-associated molecular patterns (MAMPs/PAMPs), e.g. Ef-TU proteins, peptidoglycans, bacterial flagellin and lipopolysaccharides (Boller and Felix 2009), or intracellular effector proteins, e.g. Avrk, Avr3a and Avra10 proteins (Rivas and Thomas 2005; Boller and Felix 2009). The defence mechanism initiated against pathogens in two ways is referred to as systemic acquired resistance (SAR) and induced systemic resistance (ISR) (Pieterse et  al. 2012). The plant hormones SA, JA and ET are also involved in providing defence through SAR and ISR (Makandar et al. 2010; Pieterse et al. 2012). Both SAR and ISR defence mechanisms can be differentiated on the basis of nature of the elicitor and differences in regulatory signalling pathways demonstrated in a model plant system (Schenk et al. 2000; Yan et al. 2002). Several reports have shown that various genes are responsible for producing chitinase, glucanase and other enzymatic activities which are involved in providing the defence mechanism to the broad spectrum of the pathogens (Van Loon et al. 2006). The SAR can be activated by exposing pathogenic and non-pathogenic microbes or chemicals to the plants such as SA, 2,6-dichloro-isonicotinic acid (INA) and S-methyl ester (BTH) (Sticher et al. 1997). Typical for SA-mediated SAR is the initiation of pathogenesis-related (PR) proteins like PR-1, PR-2 and PR-5 (Van Loon 1997; Jones and Dangl 2006). PGPR (Pseudomonas) on the colonization of Arabidopsis root result in induced systemic resistance on exposing JA and ET (Kloepper et al. 2004).

9.5.1  Microbes in Abiotic Stress Tolerance Plants under natural environment conditions get exposed to various abiotic stresses such as drought, salt stress, osmotic stress, extreme temperature, cold stress, high wind, floods, etc. which ultimately negatively impact plant growth and development. Tolerance to abiotic stress is polygenic and quantifiable in nature which includes the accumulation of stress metabolites, such as glycine-betaine, proline, poly-sugars, abscisic acid and various antioxidants, as catalase (CAT), superoxide dismutase (SOD), ascorbic acid, glutathione reductase, ascorbate peroxidase (APX), alpha-tocopherol and glutathione (Agami et  al. 2016; Kour et  al. 2019a). Plant growth-promoting rhizobacteria (PGPR) are involved in providing abiotic stress tolerance (Saxena et al. 2016; Verma et al. 2015; Yadav 2019) (Table 9.5). The bacterial strains of PGPR such as Pseudomonas putida and P. fluorescens have the ability to scavenge the cadmium ions from the soil to neutralize the effect of cadmium pollutant (Baharlouei et  al. 2011). The improvement of leaf water status under severe abiotic stress and salinity conditions also has been reported as an effect of PGPR (Naveed et al. 2014a). The term induced systemic tolerance (IST) is being excessively used for abiotic stress tolerance mediated by microbes. Microbes were the key players from a few decades for alleviating the abiotic stress tolerance in plants (Nadeem et  al. 2014; Souza et al. 2015). Various PGPR belonging to several genera, Azotobacter (Sahoo et al. 2014), Azospirillum (Omar et al. 2009), Bacillus (Vardharajula et al. 2011; Sorty et al. 2016), Bradyrhizobium (Swaine et al. 2007; Panlada et al. 2013), Burkholderia

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Table 9.5  List of various microbe inoculations and their tolerance strategy on the different plant host Abiotic stress Salt

Microbe inoculation Plant host Bacillus subtilis GB03 Arabidopsis thaliana Pseudomonas simiae

Glycine max

Pseudomonas syringae DC3000, Bacillus sp. strain L81 Root-associated plant growth-promoting rhizobacteria (PGPR) Cyanobacteria and cyanobacterial extracts

Arabidopsis thaliana

Pseudomonas koreensis strain AK-1 Glomus etunicatum

Burkholderia, Arthrobacter and Bacillus Glomus intraradices

Oryza sativa

Tolerance strategy/ physiological changes Regulation of tissue-­ specific sodium transporter HKT1 Promotes soybean seed germination SA-dependent pathway

Enhanced expression of RAB18 salt stress-related plant gene Phytohormones act as elicitor molecule

Oryza sativa. Triticum aestivum. Zea mays, Gossypium hirsutum Glycine max Increase in K+ level and L. Merrill reduction in Na + level Glycine max Decreased shoot proline concentrations but increased root Enhanced accumulation of Vitis vinifera. proline Capsicum annuum Glycine max Carbohydrate accumulation

References Zhang et al. (2008) Vaishnav et al. (2016) Barriuso et al. (2008) Jha et al. (2014) Singh (2014)

Kasotia et al. (2015) Sharifi et al. (2007) Barka et al. (2006) Porcel and Ruiz-Lozano (2004) (continued)

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Table 9.5 (continued) Abiotic stress Microbe inoculation Drought Rhizobium tropici and Paenibacillus polymyxa (co-inoculation) Trichoderma hamatum DIS 219b

Plant host Phaseolus vulgaris

Theobroma cacao

Trichoderma harzianum TH-56

Oryza sativa

Gluconacetobacter diazotrophicus

Saccharum officinarum cv. SP70 1143 Zea mays

Burkholderia phytofirmans, Enterobacter sp. FD17 Bacillus thuringiensis AZP2 Pseudomonas chlororaphis O6 Pseudomonas putida strain GAP-P45 Bacillus licheniformis strain K11 Bacillus cereus AR156, B. subtilis SM21 and Serratia sp. XY21

Triticum aestivum Arabidopsis thaliana Helianthus annuus Capsicum annum Cucumis sativa

Tolerance strategy/ physiological changes Stress tolerance gene upregulation

Delayed changes in net photosynthesis and stomatal conductance Upregulation of dehydrin, aquaporin and malondialdehyde genes Proline and IAA production Increased root, shoot biomass and photosynthesis under drought stress Volatile organic compound production Production of volatile compound Epoxypolysaccharide production Stress-related genes and proteins Production of proline, monodehydroascorbate and antioxidant enzyme

References Figueiredo et al. (2008)

Bae et al. (2009) Pandey et al. (2016) Vargas et al. (2014) Naveed et al. (2014b)

Timmusk and Wagner (1999) Cho et al. (2008) Sandhya et al. (2009) Lim and Kim (2013) Wang et al. (2012)

(continued)

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Table 9.5 (continued) Abiotic stress Salinity

Microbe inoculation Azospirillum brasilense and Pantoea dispersa (co-inoculation) Glomus intraradices BAFC 3108

Plant host Capsicum annuum

Pseudomonas pseudoalcaligenes along with Bacillus pumilus Achromobacter xylosoxidans UM54

O. sativa

Pantoea agglomerans Glomus clarum, Glomus etunicatum

Bacillus subtilis

Lotus glaber

Salt-sensitive rice GJ-17 Zea mays mexicana Vigna radiata. Capsicum annuum. Triticum aestivum Arabidopsis

Glomus intraradices BEG121 Pseudomonas putida Rs-198

Lactuca sativa Gossypium hirsutum

Azospirillum brasilense strain Cd Bacillus subtilis

Phaseolus vulgaris Lactuca sativa

Arsenic toxicity

Staphylococcus arlettae

Brassica juncea

Cd, As, Cu and Pb toxicity

Pseudomonas koreensis AGB-1 Neotyphodium uncinatum

Miscanthus sinensis Perennial ryegrass

Tolerance strategy/ physiological changes High photosynthesis and stomatal conductance

Enhanced root K+ concentrations and decreased shoot and root Na + accumulation Decline in proline content by 5% and accumulation of glycine betaine Reduced superoxide dismutase activity and lipid peroxidation Upregulation of aquaporins The increased concentration of K+ in root and decreased Na + in root and shoot Decreased transcriptional expression of a high-­ affinity K+ transporter (AtHKT1) in the roots Reduced concentration of ABA Prevented ABA accumulation in seedlings during salinity stress Persistent exudation of flavonoids Stimulation of shoot biomass Increased soil phosphatase, dehydrogenase and available phosphorus IAA and ACC deaminase production Reduced leaf elongation and enhanced tillering

References del Amor and Cuadra-­ Crespo (2012) Sannazzaro et al. (2006)

Jha et al. (2011a, b)

Jha et al. (2011a, b) Gond et al. (2015) Rabie (2005)

Zhang et al. (2008)

Aroca et al. (2008) Yao et al. (2010) Dardanelli et al. (2008) Arkhipova et al. (2007) Srivastava et al. (2013)

Babu et al. (2015) Rabie (2005) (continued)

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Table 9.5 (continued) Abiotic stress Heat

Microbe inoculation Bacillus amyloliquefaciens, Azospirillum brasilense Curvularia protuberata isolate Cp4666D

Hg Photobacterium spp. toxicity Osmotic Bacillus megaterium stress P. indica

Pseudomonas sp.

Glomus intraradices BEG 123

Zn toxicity

Pseudomonas aeruginosa Pseudomonas koreensis AGB-1

Enterobacter intermedius MH8b

Cold

Pseudomonas brassicacearum, Rhizobium leguminosarum Paecilomyces formosus LHL10

Plant host Triticum aestivum

Tolerance strategy/ physiological changes Reduced regeneration of ROS, changes in the metabolome

References El-Daim et al. (2014)

Dichanthelium lanuginosum, Solanum lycopersicum Phragmites australis Zea mays

Colonization of roots

de Zelicourt et al. (2013)

A. thaliana

Su et al. Induced cold response pathway and accumulation (2015) of pigments

Mercury reductase activity Mathew et al. (2015) Increased root expression Marulanda et al. (2010) of two transporters, ZmPIP isoforms Sziderics Capsicum annum Gene encodes ACC et al. (2007) oxidase enzyme which encodes a lipid transfer protein Genes for the glucan-­ Sarma et al. Epacrids, water dikinase (2011) Nicotiana tabacum and A. thaliana Aroca et al. Phaseolus Enhanced root hydraulic (2007) vulgaris conductance due to enhanced solute transport through roots Triticum Improved biomass, P and Islam et al. aestivum N uptake (2014) Babu et al. Miscanthus High tolerance to Zn, As (2015) sinensis and Pb by extracellular sequestration, enhanced SOD and catalase activities in plants Plociniczak Sinapis alba IAA, ACC deaminase, et al. (2013) hydrocyanic acid and P solubilization Brassica juncea Metal-chelating molecules Adediran et al. (2016)

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(Oliveira et al. 2009), Cyanobacteria (Singh et al. 2011), Enterobacter (Grichko and Glick (2001); Sorty et  al. 2016), Methylobacterium (Meena et  al. 2012), Pantoea (Sorty et  al. 2016), Pseudomonas (Ali et  al. 2009; Sorty et  al. 2016), Rhizobium (Alami et al. 2000; Sorty et al. 2016) and Trichoderma (Ahmad et al. 2015), which have greater role in the mitigation of multiple abiotic stresses have been reported. Soil-occupant microbes belonging to the genera Aeromonas, Azospirillum, Azotobacter, Achromobacter, Bacillus, Enterobacter, Klebsiella, Pseudomonas and Variovorax have been documented to promote plant growth under unfavourable environmental conditions (Dardanelli et al. 2008; Kaushal and Wani 2016). The role of Trichoderma harzianum was demonstrated for abiotic stress mitigation due to the upregulation of dehydrins, aquaporins and malonaldehyde genes (Pandey et  al. 2016). The application of Trichoderma harzianum resulted in the more uptake of essential mineral nutrients along with the higher accumulation of osmolytes and antioxidants and less Na + uptake (Ahmad et al. 2015). Trichoderma also ameliorates salinity stress by producing ACC deaminase (Brotman et  al. 2013). Pseudomonas sp. and Acinetobacter sp. in barley and oats resulted in enhanced production of ACC deaminase and IAA in salt-affected soil (Chang et al. 2014).

9.6  Bioremediation to Improve Soil and Plant Health Soil constitutes a top 5–10 cm layer of material on the Earth’s surface. Plant roots, small insects, animals and microorganisms form almost 20% of soil by proportion. It is estimated that 1 g of fertile agriculture soil contains about 2.5 × 109 bacteria, 5  ×  105 fungi, 50,000 algae and 30,000 protozoa. The importance of fertile soil which maintains plant growth is linked to the question of food security for mankind. If the soil becomes devoid of nutrients and organic matter in addition to polluted with materials which are toxic to the growth of plants and microbes, it is classified as infertile soil. Bioremediation is the cheapest and eco-friendly approach for remediating soil and aquifer contamination approach which helps in restoring the fertility of soil (Fig. 9.3). Types of contaminants of soil include: 1. Metals (such as lead, cadmium, mercury, chromium and nickel). 2. Volatile organic compounds, viz., benzene, trichloroethylene and toluene. 3. Semi-volatile organic compounds, viz., total petroleum hydrocarbon, polycyclic aromatic hydrocarbons (PAHs: most widespread) and polychlorinated biphenyls (PCBs). 4. Agricultural activities like an application of agrochemicals (fertilizers, pesticides and herbicides), the use of sewage sludge in agricultural practices and irrigation with polluted water also add significant amounts of contaminants of organic and inorganic nature to the soils. Biological agents including microbes (microremediation), plants (phytoremediation) or both (rhizoremediation) are used for bioremediation purposes. Bioremediation strategy involves some basic steps summarized in Fig. 9.3. Processes of bioremediation could be in situ or ex situ. In situ bioremediation is an on-site

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Strategy of Bioremediation Identify the type of soil pollution If soil contains xenobiotics

Addition of suited initial inoculum of organisms in compost heap Improves structural porosity

Identify the communities of microbes and organisms according to pollution type

Selection of plants as a colonization support for the selected organisms in soil If soil supports organism growth

Application of compost Allow easy access to the air flow

Provides easily degradable organic nutrients required for the sustenance Fig. 9.3  Strategy of bioremediation

cleaning up of polluted environments comprising supplementation of polluted soils with nutrients to activate microorganisms for destroying contaminants, the addition of new microorganisms to the environment and improvement of native microbes to degrade specific contaminants using biotechnological tools (Rayu et al. 2012). Ex situ bioremediation refers to taking the polluted media from its native site to some other location for remediation with the beneficial microbe, based on different criteria of cost, extent and type of contamination and pollutant, origin and geology of the contaminated site (Azubuike et al. 2016). Bioremediation by microbes involves the mechanisms of biosorption, bioaccumulation, aerobic and anaerobic degradation and biotransformation, employing the basic chemical processes of oxidation, binding, immobilization, volatilization and transformation.

9.6.1  Microremediation Microremediation is an effective technology of eliminating lethal pollutants from the surroundings and stabilizing the environment by using indigenous microorganisms capable of degrading heavy metals or employing recombinant microbes to treat contaminated atmosphere by transforming toxic metals into harmless forms (Gupta et al. 2016). BSMs including Azospirillum lipoferum, Enterobacter cloacae, Pseudomonas putida and P. fluorescens have potential to remediate polycyclic aromatic hydrocarbons, total petroleum hydrocarbons and trichloroethylene-­ contaminated soils (Glick 2010), by acting directly on these pollutants. Moreover, it would be more successful if consortia of microorganisms is used instead of a single strain culture; e.g. the cooperative influence of microbial cocktail

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of four strains, Viridibacillus arenosi B-21, Sporosarcina soli B-22, E. cloacae KJ-46 and E. cloacae KJ-47, on bioremediation of lead, cadmium and copper from contaminated soils was investigated by Kang et al. (2016), and they reported that these cocktails are more efficient and had greater resistance for the remediation of heavy metals in contrast to single strain culture with efficiencies of 85.4% for Cd, 98.3% for Pb and 5.6% for Cu. Siderophores, as explained under Fe and Zn uptake strategies, enhance mobility of metals and diminish their bioavailability and subsequent removal from soil. Desulfovibrio desulfuricans, a sulphate-reducing bacterium, possesses the ability to change sulphate to hydrogen sulphate which produces insoluble forms of cadmium and zinc sulphides on reacting with them.

9.6.2  Phytoremediation and Rhizoremediation Phytoremediation deals with the cleaning of organic pollutants and heavy metal contaminants using plants and rhizospheric microorganisms (Dixit et al. 2015) in an inexpensive and eco-friendly manner (Fig.  9.4). The types of phytoremediation used are explained in Fig. 9.4. Plants used for phytoremediation are classified into two categories: (a) Hyperaccumulators possess very high potential for heavy metal accumulation and reduced biomass efficiency. About 500 taxa have been identified as hyperaccumulators for some metals, and the prevalent ones belong to the families of

Phytodegradation Phytovolatilization Breakdown of organic pollutants into non-hazardous forms by enzymes

Greater capacity to take up heavy metals, detoxify and sequester them from soil to shoots from soil

Phytoextraction Metal chelation and solubilization

Phytostabilization Heavy metal sequestration only within rhizosphere

Fig. 9.4  Methods of phytoremediation

Soil contaminants readily changing into vapour and released in atmosphere

Phytostimulation Roots release exudates

Phytofiltration

Enhancement of microbial activity

Blastofiltration Rhizofiltration Caulofiltration

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Brassicaceae, Caryophyllaceae, Violaceae, Fabaceae, Euphorbiaceae, Lamiaceae, Asteraceae, Cyperaceae, Poaceae, Cunoniaceae and Flacourtiaceae. (b) Non-hyperaccumulators are fast-growing species which possess minor extraction potential in contrast to hyperaccumulators. However, their total biomass yield is considerably greater. For example, willow, poplar and Brazilian leguminous trees, viz., Erythrina speciosa, Mimosa caesalpiniaefolia and Schizolobium parahyba, have been reported for their potential in phytoremediation of areas contaminated with lead (Souza et al. 2013). Among the microorganisms, rhizospheric and rhizoplane microorganisms play a significant role in the phytoremediation, and the attention has increased the importance of metabolism of the soil microbial community in contaminated soils. Legume crops like alfalfa and soybean have been used to eliminate organic pollutants from contaminated soils. Sedum plumbizincicola and Elsholtzia splendens are the two major plant species that are widely used in soil polluted with hazardous toxic inorganic elements and have proven an ability to extract copper and zinc from polluted soils (Zhu et al. 2018). Successful degradation of xenobiotics and other pollutants by several microorganisms is carried out effectively by different hydrolytic enzymes, viz., esterases, peroxidases and oxygenase enzymes. These hydrolytic enzymes play a key role in their degradation, and many Enterobacteriaceae and Pseudomonas members are well known for degrading persistent xenobiotics. Among the six methods of phytoremediation, phytoextraction is the most favoured method used by plants for remediation of polluted environments as it is enhanced by plant growth-promoting rhizobacteria (PGPR) associated with the plant roots, whereas phytostabilization is a superior alternative to capture metals in situ because the contaminants are not available in tissues of the plants and do not spread into the atmosphere; and phytodegradation is restricted only to removal of organic pollutants since heavy metals are nonbiodegradable.

9.6.3  R  ole of Biotechnology, Genomics and Nanotechnology in Bioremediation Biotechnology played a significant role in bioremediation processes by genetically engineering the microbes (designer microbe approach) and plants (designer plant approach), manipulating plant-microbe symbiosis and rhizosphere engineering. However, these technologies are confined to limited microbes or plants (Dixit et al. 2015). For example, genetic modification of rhizospheric bacteria and endophytes for plant-associated destruction of soil pollutants is considered as the most potential technology for remediation of sites contaminated with heavy metals. But, this approach is applicable to confined bacterial strains like Bacillus subtilis, Escherichia coli, Pseudomonas putida, etc. Similarly, designer plant approach solves the major limitation of phytoremediation of accumulating pollutants in the plant tissues. Plants like poplar, willow and Jatropha which are fast-growing as well as

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high-­biomass-­yielding could be used for both phytoremediation and energy production. However, for energy production, burning of these plants transfers the problem from soil and water to air. Thus, proper storage and disposal of metal-accumulating biomasses is necessary to ensure that they do not cause any harm to the surroundings. The technology involving microbial nanoparticles with enhanced potential to remove toxic contaminants is called nanobioremediation. It not only reduces the costs of cleaning polluted sites at a bigger scale but also diminishes the processing time. The characteristics like small size, genetic manipulability, greater physiological diversity and controlled cultures make microbes the perfect fabricators of nanostructures. For example, with the ability to survive in radiation well beyond the naturally occurring levels, Deinococcus radiodurans’ use in the cleaning of radioactive waste was funded by the US Department of Energy. This novel method can effectively address the escalating problem of organic contaminants and heavy metals in the environment. Knowledge of genomics to understand microbe-­mediated remediation provides a sketch of genes related to the behaviour of various microbes towards toxic metals in the soil. This information would probably examine the microorganism not only on the basis of biochemical properties but also at molecular levels related to their mechanisms of action. Anthropogenic activities, rapid urbanization, industrialization and development of innovative technologies are dramatically posing contrary side effects of degradation of soil health through its contamination. To revive these effects, the use of microbes has been proven as a time-saver for bioremediation as other chemical methods are very complex in nature and are also expensive. However, bioremediation also has some limitations, but future studies can be stressed on developing more potential microbes/plants by manipulating their metabolic activity as per the requirements, employing new technologies of genetic engineering. Moreover, there is an urgent need to popularize and prove among the public that the developed technologies are beneficial and non-toxic to the environment, for a successful acceptance of bioremediation involving genetic engineering among the society.

9.7  M  icrobes in Organic Farming and Sustainable Agriculture Agriculture is regarded as sustainable when the system is socially supportive, resource-conserving, competitive in the market and environment-friendly. Organic farming is an alternative agricultural approach originated in the early twentieth century in response to frequently changing agricultural practices. It is demarcated by using fertilizers which are organic in origin such as bone meal, compost manure, green manure and pest control and also the mixed cropping. In organic farming systems, microorganisms perform an essential role as the chief lively forces. Since soil is the base of many of the biological processes, viz., biological nitrogen fixation, residue decomposition, mineralization/immobilization turnover, nutrient

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cycling and denitrification, all these processes are predominantly regulated by microbes. A number of different soil microorganisms are significantly involved in these processes and play a considerable role in organic farming: 1. Microorganisms play a key role in the formation of soil and its stability by aggregating soil particles with the help of hyphae and secretion of exudates. 2. Several microbes show potential biocontrol features against crop diseases, pests and weeds, while rhizobacteria and mycorrhizal species perform a significant role in fertility management in a sustainable way. 3. Streptomycetes are active and obstinate soil saprophytes which are usually associated with plant roots and are also recognized as ‘antibiotics and extracellular hydrolytic enzymes’ producers. They have the capability to add on the benefits of integrated disease management to various crops such as alfalfa, potato, maize and soybeans, as they can colonize plants and reduce harm from a range of pathogens (Samac et al. 2003). 4. Mycorrhizal fungi provide defence against heavy metals’ uptake by adsorption on hyphae. We have already discussed the biofertilizers and different microorganisms which are progressively replacing the harmful synthetic chemical fertilizers that not only affect the crop yields but also the soil microflora. With the goal of protecting the natural resources by adopting sustainable and diverse organic farming, farmers are conserving resources, produce more better-quality products and achieve higher incomes. Moreover, organic products create added value and deliver market access and hence organic farming upsurges self-confidence and makes new partnerships. Microbes allow the natural production of nutrients in the soil throughout the crop season; that role played by them in organic agriculture and hence in sustainable agriculture is comprehensive.

9.8  Conclusion and Future Prospective Microbiome around the root and leaf significantly affects the plant health. Microbes in the rhizosphere not only affect plant health but are important to soil health as well as they exert a positive effect on soil aggregation, porosity and its physical and chemical properties. Microbes also help in remediating the contaminated soils by microremediation and rhizoremediation. Both plants and microbial community in the rhizosphere are beneficial to each other’s growth and development. A plant selectively chooses the type of microorganisms in the surrounding rhizosphere with the help of root exudates. Similarly, microbes communicate with the plant by releasing volatile organic compounds. Plant growth-promoting rhizobacteria (PGPR) and plant growth-promoting fungi (PGPF) help in the biological fixation, solubilization and mineralization of important macro- and micro-elements. Microbes are capable of producing phytohormones endogenously and exogenously which are directly involved in the plant growth and development, especially root and shoot growth.

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Apart from nutritional benefits to plants, microbes play a great role in providing biotic and abiotic stress tolerance to plants. This can be achieved by induced systemic resistance (ISR), systemic acquired resistance (SAR) or induced systemic tolerance (IST) with the help of various stress metabolites (catalases, superoxide dismutases, ascorbic acid, etc.) or hormones like salicylic acid (SA), jasmonic acid (JA), ethylene (ET) and abscisic acid (ABA). All these benefits are making the role of microorganisms imperative in sustainable agriculture. Commercial formulations either single strained or in consortia are being used as biofertilizers and greatly helping in the sustainability of the agriculture. Thus it is important to discover new strains, to increase efficiency of the existing strains and to study the plant-microbe interactions in more detail for increasing the productivity of crops.

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Chapter 10

Biofertilizers and Biopesticides: Microbes for Sustainable Agriculture Bensidhoum Leila and Nabti El-Hafid

Abstract  Human efforts to develop agriculture have been known for a long time. Since becoming aware of the importance of this field, farmers and researchers have not ceased looking for methods and products to improve crop productivity and quality and to protect it from various aggressions and stress that it might undergo. Mechanisms using microbes as biofertilizers and biocontrol agents have been adopted recently as an alternative to agrochemicals. The use of beneficial microbes is an environment-friendly strategy, which play a major role in the stimulation of plant growth and in the biocontrol of plant pathogens. A better understanding of the use of these bacterial populations could allow a reduction of chemical inputs and pollutant pesticides in agricultural soils. The present review is limited to plant growth-promoting bacteria (PGPB); it summarizes the role of PGPB in soil fertilization and plant protection with a special emphasis on their mechanisms of action. Several examples of PGPB chosen from the literature are cited in this chapter. This review includes also examples of the agricultural application of these microbes. Keywords  Agriculture · Biofertilizers · Biopesticides · Microorganisms · Soil

10.1  Introduction Human activities to improve crop yields and to reduce production costs had a negative impact at several levels. Chemical products are considered the most effective solution; however, the increased use of these substances has a negative effect on human health and the environment (Kouassi 2001; Thakore 2006). Besides chemical products, desert regions, heavy metals, and salinity constitute other obstacles for agriculture. Actually, with strong population growth, the rising living standards of

B. Leila · N. El-Hafid (*) Laboratoire de Maitrise des Énergies Renouvelables, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia, Algeria © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_10

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the most developed countries, and the globalization of markets, agriculture has become intensive based on mechanization and modern means of agronomy, which has improved crop production. Owing to environmental degradation, intensive agriculture is increasingly criticized. These environmental degradations have raised many questions and caused the development and the emergence of new preoccupations for agricultural science (depollution, waste management, rural development, biological control) (Nyembo et al. 2012). Because of their devastating effects on plant health and crop yields, plant pathogens require another threat to food production and ecosystem stability. Recently, the producers became dependent on chemical products as the most effective method of crop protection. However, these products have harmful effects on human health as a consequence of the residues in food products, in addition to exposing the beneficial soil microbial community to an excessive concentration of agrochemicals (Yadav et al. 2017a). Biofertilization and biological control have been adopted as an alternative to intensive agriculture, with the aim of reducing the risks associated with the use of pesticides. It is a land policy that excludes the use of chemical plant protection products and uses natural treatments (COLEACP 2011). In recent years, several products have been developed within the agricultural input market, which aim to improve soil and plant functioning or plant-soil interactions. These products called biostimulants provide often innovative solutions in the field of fertilization and crop protection. These stimulating molecules of biological origin are mainly the plant growth-promoting bacteria (PGPB) (Faessel et al. 2014). This group of microorganisms is making an important contribution to strengthening sustainable agriculture, by their ability to regulate the biological functioning of the rhizosphere and to protect and to improve plant growth and health (De Salamon et al. 2006). The selection of plant growth-promoting microorganisms and their products can be advantageous to enhance the colonization of plant rhizosphere and offers many possibilities for agriculture and preserves environment. Indeed, a better understanding of the use of these bacterial populations could allow a reduction of chemical inputs and pollutant pesticides in agricultural soils (Bensidhoum and Nabti 2019).

10.2  Plant Growth-Promoting Bacteria The microorganisms, mainly bacteria belonging to the genus of Arthrobacter, Azotobacter, Azospirillum, Bacillus, Enterobacter, Pseudomonas, Serratia, and Streptomyces spp. have a beneficial effect on plant growth and development by stimulating the growth of plants and by protecting them against biotic and abiotic stresses (Gray and Smith 2005; Tokala et  al. 2002; Yadav et  al. 2017b, 2018a). These microbes are able to grow and to compete with other soil microbes for nutrients and rhizospheric space. These bacteria are then referred to as plant growth-­ promoting bacteria (PGPB), and they are also called rhizobacteria stimulating plant nodulation (Rifat et al. 2010; Yadav et al. 2017c).

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The PGPR (plant growth-promoting rhizobacteria) is the most studied group of PGPBs (Compant et al. 2005). By using root exudates as nutritious substrates, these bacteria colonize plant rhizosphere, but unlike other rhizosphere bacteria, these bacteria offer to plants many beneficial effects via a multitude of direct and indirect mechanisms (Vacheron et al. 2013; Kour et al. 2019c; Verma et al. 2015) (Fig. 10.1). Direct mechanisms involve the supply of unavailable nutrients, the nitrogen fixation, the production of phytohormones (auxins, cytokinins, and gibberellins) and siderophores (O’sullivan and O’gara 1992; Patten and Glick 2002; Lugtenberg and Kamilova 2009), and the repression of ethylene synthesis by the production of 1-aminocyclopropane-1-carboxylic deaminase (ACC-deaminase) enzyme (Glick 1995). Indirect mechanisms involve the suppression of phytopathogenic agents through competition for space and nutrients, the synthesis of hydrolytic enzymes, the inhibition of enzymes or toxins produced by pathogens, and the induction of plant resistance mechanisms (Glick 1995; Antoun and Prévost 2006; Kaymak 2010). The diversity of PGPB varies widely depending on the type of plant and soil, and nutrient availability. Among the identified PGPB, Pseudomonas and Bacillus are the most distributed and studied. Strains belonging to the genera Aeromonas, Azospirillum, Azotobacter, Arthrobacter, Clostridium, Enterobacter, Gluconacetobacter, Klebsiella, and Serratia are also classified as PGPB (Fernando et al. 2005; Fuentes-Ramirez and Caballero-Mellado 2005; Verma et al. 2019; Yadav et al. 2017a). PGPB has the ability to improve the development of all plant growth

Fig. 10.1  Soil management microbiome and crop enhancement by PGPR. (Bensidhoum and Nabti 2019)

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parameters (seed germination; root and shoot length and weight; leaf area and chlorophyll content); besides this, they are good biofertilizers and with their enzymes (lipase, esterase, protease, phosphatase, urease, chitinase, and amylase), these microbes hydrolyze all types of organics polymers (Verma et al. 2016; Yadav et al. 2019a). Thus, they contribute to the enrichment of soil by the nutritive elements and facilitate their plant uptake (Fuentes-Ramirez and Caballero-Mellado 2005; Tripathi et al. 2007; Yadav et al. 2020). PGPB can be used as biofertilizers (enrich soils and facilitate nutrients uptake by plants), phytostimulators (stimulate the growth and the development of different plant growth parameters), rhizoremediers (degrade organic pollutants and mitigate their toxicity), and biopesticides (protect the plants from different aggressions caused by phytopathogenic agents) (Somers et al. 2004; Yadav et al. 2018a, 2019b).

10.3  PGPB as Biofertilizers Biofertilizers are defined as a material that contains efficient microorganisms (living or dormant) whose function when applied to soil is to enrich soil with nutrient element and to stimulate plant growth by improving nutrient uptake, nutrient efficiency, tolerance to abiotic stress, and enhancing crop productivity and quality. Biofertilizers are also defined as preparations containing living or dormant cells of strains, with the ability to fix nitrogen, to solubilize phosphate, and to produce cellulase (Kumar Sethi et  al. 2015). Several mechanisms are applied by PGPBs to fertilize soil and to enhance plant productivity, e.g., nitrogen fixation, phosphate solubilization, siderophores, and hydrolytic enzyme production (Kour et al. 2019d; Rana et  al. 2019; Yadav et  al. 2018b). Biofertilizers improve nutrients uptake by plants, e.g., nitrogen is provided by nitrogen-fixing bacteria (Bashan et al. 2004), iron is provided by siderophore-producing bacteria (Scher and Baker 1982), sulfur is derived from sulfur-oxidizing bacteria (Stamford et al. 2008), and phosphorus by phosphate solubilizing bacteria (Chabot et al. 1996). These microorganisms act in consortium with other rhizospheric microbes, by understanding the plant-microbial consortia interactions; we can exploit these beneficial microorganisms and improve more crop productivity (Raja et al. 2006).

10.3.1  Enzymatic Activities The microbial enzymes are used in biotechnology (agro-food, detergents, textile, pharmacy, medicine, molecular biology) (Carrim et al. 2006); however, in agriculture the wide interest aroused by these microorganisms is based on their application as biofertilizers. Enzymes such as proteases, esterase, lipases, amylases, and cellulases are of considerable agricultural interest due to their involvement in soil fertilization by the degradation of organic polymers (Kour et al. 2019a). Through these

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activities, these microorganisms release into the soil the nutrients such as phosphorus, iron, carbon, nitrogen, potassium, and sulfur which will subsequently be used by plants and other soil microorganisms. One of the main mechanisms used by biocontrol agents to control plant pathogens involves the production of cell wall degrading enzymes (Chet et al. 1990; Kobayashi et al. 2002), such as glucanases, chitinases, cellulases, and proteases secreted by PGPR (Labuschagne et al. 2010; Yadav et al. 2016a, b). Cellulose degradation plays a fundamental role in the carbon cycle (Ponnambalam et al. 2011); it is essentially converted by microorganisms into carbon dioxide or methane (Ljungdahl and Eriksson 1985). Cellulases produced by soil microorganisms have attracted a lot of attention due to their potential use in the agricultural waste conversion. Sindhu and Dadarwal (2001) have reported that cellulases produced by bacterial strains belonging to the genus Pseudomonas can enhance the formation of nodules by rhizobia in legumes. This enzyme facilitates the penetration of these bacteria into the root hear or the intercellular space and thus increases the number of nodules (Sindhu and Dadarwal 2001). Esterases and lipases were found in 1901 in bacteria such as Bacillus prodigiosus, Bacillus pyocyaneus, Pseudomonas fluorescens, and Pseudomonas aeruginasa (Eijkmann 1901; Fickers et  al. 2007). The synthesis of lipases and esterases by bacteria contributes to the degradation of the fatty substances and therefore these bacteria could participate in the recycling of organic matter by providing the necessary elements to the plants. Amylase enzymes hydrolyze starch or glycogen; they are widely distributed in soil and plants. These enzymes play an important role in the conversion of starch to glucose and/or oligosaccharides (Thoma et  al. 1971). The synthesis of these enzymes by PGPB allows degradation of the organic matter and provides the necessary elements for plant growth. Many strains of Bacillus sp. were revealed to produce considerable amounts of α-amylases., (Whipps, 2001; Siddiqui 2006). Viollet (2010) have also shown that amylase-producing Pseudomonas stimulates plant growth and health. Protein degradation by microbial proteases plays a fundamental role in the nitrogen cycle in soil by making it available to plants and micro-organisms (Petit and Jobin 2005). It is well established that the production of lytic enzymes such as proteases is one of the indirect mechanisms applied by PGPR in the elimination of harmful microorganisms (Twisha and Desai 2014). Several authors (Chet et  al. 1990; Kobayashi et  al. 2002; Labuschagne et  al. 2010) have shown the effect of microbial proteases in biological control. Lian et al. (2007) revealed the application of proteases in the degradation of nematode cuticles. Dunne et al. (1997) demonstrated that the inhibition of the phytopathogenic fungus Pythium ultimum in the sugarcane rhizosphere is due to the development of extracellular protease by Stenotrophomonas maltophilia W81. The protease activity may indirectly influence the synthesis of auxin by releasing amino acids such as tryptophan, which is the precursor for the synthesis of the IAA (Mansour et al. 1994). A considerable amount of urea is constantly released into the environment through biological activities. Urease is an extracellular enzyme that represents 63%

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of total soil activity, its role is the hydrolysis of urea to CO2 and ammonia (NH3). It is used as an indicator of soil quality because its concentration depends on the rate of organic matter (Martinez-Salgado et al. 2010). The activity of urease in soils has received much attention since it was reported by Rotini (1935) (Kumar Das and Varma Kumar and Varma 2011). According to Polacco (Polacco 1977), soil urease is produced mainly by plants and microorganisms which produce both types of enzymes (intra- and extra-cellular) (Mobley and Hausinger 1989).

10.3.2  Nitrogen Fixation Nitrogen is one of the most important nutrients for plant growth. The major part of this element is in gaseous form (N2), not available to animals and plants (Pujic and Normand 2009). To provide the needs of plants in nitrogen, and in order to improve productivity, agriculture has become dependent on chemical fertilizers; however, the damage caused by these products was considerably more than their beneficial effect. In addition to their impact on the environment, the US National Institutes of Health has published a report on the damage that can be caused by synthetic nitrogen fertilizers on human health; it suggested that increased nitrate concentrations in drinking water could contribute to cancer, and nitrogen-related air pollution could be elevating the incidence of cardiopulmonary ailments (Doty 2011; Townsend and Howarth 2010). Consequently, farmers relied more on biological processes to provide nitrogen for plants. Bacteria ensure the fixation of this element and transform it into ammonia (assimilable form). Free-living bacteria (Azotobacter, Bacillus, Acetobacter, Clostridium, Klebsiella, Corynebacterium, Arthrobacter, Diazotrophicus, and Pseudomonas) (Vessey 2003), symbiotic (Rhizobium) or bacteria in association with certain plants (Azospirillum) (Okon and Kapulnik 1986; Gray and Smith 2005; Suman et al. 2016). One of the benefits of diazotrophic bacteria is to provide nitrogen to plants in exchange for released carbon as root exudates. However, the availability of carbon as a source of energy is required for the intensive nitrogen fixation. This requires these diazotrophs to live near plants either in the rhizosphere, the rhizoplan, or as endophytes. Nitrogen fixation plays a potential role in improving soil fertility and productivity. Plants inoculation by nitrogen-fixing bacteria has been the subject of several studies, and the role of PGPR in nitrogen fixation and improvement of nodulation in root plants has been demonstrated by several authors (Bensidhoum and Nabti 2019). The use of these bacteria can reduce considerably the use of chemical fertilizers. It has been proved that the plant stimulating effect of the endophytic bacteria Azoarcus sp., Burkholderia sp., Gluconacetobacter diazotrophicus and Herbaspirillum sp. and the rhizospheric bacteria Azotobacter sp. and Paenibacillus polymyxa is strongly related to their ability to fix nitrogen (Vessey 2003). Several nitrogen-fixing bacteria live in the plant rhizosphere, particularly in the plant roots: Azotobacter diazotrophicus, Herbaspirillum seropedicae, and Azoarcus spp.; these microorganisms

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improve the yield of barley, wheat, rice, and sugar cane (Döbereiner 1997). Recently, Naqqash et al. (2016) found that inoculation of plants with nitrogen-fixing bacteria, Azospirillum, Enterobacter, and Rhizobium, under axenic conditions, increased potato yield. For example, Azospirillum sp. TN10 increased the fresh and dry weight of the potato compared to control (non-inoculated) plants. In addition, a significant increase in the nitrogen content of the stems and roots of the inoculated plants was observed.

10.3.3  Phosphate Solubilization Like nitrogen, phosphorus (P) is an essential element for the development of plants; it is also a nutritive element which limits their growth (Vessey 2003). It is an essential component of genetic material (DNA) and adenosine triphosphate (ATP) (Przemieniecki et al. 2015). This element is immobilized in the soil by chemical precipitation where it becomes less soluble and therefore unavailable to plants (Nabti 2007). Most of the absorbed phosphorus is transferred to the fruits and seeds during the development stages; however, phosphorus-deficient plants show growth retardation (reduction of growth of cells and leaves, disruption of respiration and photosynthesis). In agricultural soils, the solubilization of inorganic phosphates is closely related to the activity of microorganisms (Richardson 2001; Przemieniecki et  al. 2015). Bacterial species of the genus Bacillus, Pseudomonas, Rhizobium, Aspergillus, and Penicillium have the ability to convert phosphorus to its available form to plant (Qureshi et al. 2012; Kour et al. 2019b; Yadav et al. 2018c). The main mechanisms employed by PGPRs to convert phosphate into assimilable form include solubilization and mineralization. The solubilization is the consequence of the release of low molecular weight organic acids, such as gluconic acid and citric acid (Glick 2012; Oteino et al. 2015). These molecules lower the pH and chelate the cations attached to the insoluble phosphates and convert them into soluble forms (H2PO4−) (Trivedi and Sa 2008), The mineralization is done by the release of extracellular enzymes, phosphatase and phytases catalyzing the hydrolysis of the phosphoric esters. Both of these mechanisms can coexist in the same bacterial species (Glick 2012). Several authors have shown the ability of bacteria to solubilize phosphate (Kour et al. 2019b). Gull et al. (2004) reported that species of the genus Bacillus and Pseudomonas have great potential for phosphate solubilization in soil. Irving and Cosgrove (1971) and Singh et al. (2013) found that Pseudomonas solubilizes phosphate and improves the bioavailability of essential nutrients. According to Tri-Wahyudi et al. (2011), the ability of bacteria to solubilize phosphate suggests their use in crop fields. Among the great diversity of PGPR, the species Achromobacter xylosoxidans (Ma et  al. 2009), Bacillus polymyxa (Nautiyal 1999), Pseudomonas putida (Malboobi et  al. 2009), Acetobacter diazotrophicus (Dutta and Podile 2010), Agrobacterium radiobacter (Leyval and Berthelin 1989), Bradyrhizobium mediterranium (Peix et  al. 2001), Enterobacter aerogens and Pantoea agglomerans (Chung et  al. 2005), Gluconacetobacter diazotrophicus

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(Crespo et  al. 2011), Pseudomonas protegens (Bensidhoum et  al. 2016) and Rhizobium meliloti (Krishnaraj and Dahale 2014) are known as phosphate solubilizing bacteria in soil and as plant growth promoters. Rodríguez and Fraga (1999) reported that Pseudomonas and other phosphate solubilizing bacteria are able to increase the availability of phosphate in the soil. According to Tilak et al. (2005), Pseudomonas species improve plant growth by enhancing their ability to absorb several minerals from the soil. Pseudomonasstrriata, P. cissicola, P. fluorescens, P. pinophillum, P. putida, P. syringae, P. aeruginosa, P. putrefaciens, and P. stutzeri isolated from the rhizosphere of chickpea, corn, soybean, and other cereals, solubilize considerably phosphates (Tilak et  al. 2005). Some studies have linked the growth stimulation of Pisum sativum L. grown in soil poor in soluble phosphate, to the production of high concentrations of gluconic acid (Oteino et  al. 2015). Elkoca et  al. (2008) have reported that the inoculation of Chickpea by single and dual phosphate-solubilizing Bacillus megaterium (M3) and nitrogen-fixing Bacillus subtilis (OSU-142) has improved all its parameters growth compared to control equal to or higher than N, P, and NP treatments (Kaymak 2010; Elkoca et al. 2008).

10.4  PGPB as Biocontrol Agents Biological control or biocontrol is the protection of plants from the different aggressions by using living organisms. In entomology, it describes the use of predatory insects or the entomopathogenic nematodes to suppress the various pathogenic insects. In phytopathology, this term describes the use of microorganisms to inhibit disease and to control pathogenic herbs. IOBC (International Organization for Biological Control) has defined biological control as the use of living organisms to prevent or reduce damage caused by pests. These microorganisms are named “Biological Control Agent” (Pal and Gardener 2006). Numerous studies concerning the use of these microorganisms as an alternative to pesticides have shown that these biocontrol agents can play an important role in improving the performance of agriculture and horticulture (Niranjan et al. 2005). Several bacteria and fungi have been reported as antagonistic microorganisms, particularly strains belonging to the genus Bacillus, Pseudomonas, and Burkholderia (Lee et  al. 2001). The search for new biological control strategies to inhibit the growth of phytopathogenic micro-organisms has become widespread, due to environmental concerns. Several mechanisms have been proposed to explain the inhibition of phytopathogenic fungi by bacteria, including the production of antibiotics, the secretion of hydrolytic enzymes, induction of plant resistance, the competition for nutrients and space or the combination of these mechanisms (Marschner and Timonen 2006; Jamali et al. 2009; Calvo et al. 2010; Bensidhoum et al. 2015, 2016; Tabli et al. 2018). Changing environmental characteristics (pH, plant area, etc.) is one of the mechanisms used by some biocontrol agents to control indirectly plant pathogens (Manteau et al. 2003).

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10.4.1  Siderophores Production Siderophore is a protein molecule, which can solubilize and sequester iron from the soil and provide it to plant cells, these low-molecular-weight iron-binding molecules have the affinity for Fe3+. This molecule is used by PGPRs as biofertilization mechanisms and in the biocontrol of phytopathogens. Once secreted by PGPRs, siderophores bind Fe3+ from the soil and transport it back to PGPRs cell, where it will be converted to an available form for plants and microbial growth (Beneduzi and Passaglia 2011; Leong 1986). The production of significant quantities of siderophores in soil allows PGPRs to appropriate all the iron necessary for their growth and consequently make it inaccessible to phytopathogen microorganisms. Numerous authors (Meyer and Abdallah 1978; Zahir et al. 2004; Mezaache 2012; Ji et al. 2014; Przemieniecki et al. 2015; Bensidhoum et al. 2016) have shown the production of siderophores by Bacillus and Pseudomonas species. Several studies have confirmed that the sidorophores produced by the PGPR influence significantly plant uptake of various metals, including Fe, Zn, and Cu (Egamberdieva 2007; Dimkpa et al. 2008; Gururani et al. 2012). The bacterial siderophores can influence plant nutrition, they are known for their ability to sequester iron from the rhizosphere, making it unavailable to pathogenic fungi, thus limiting their growth (O’sullivan and O’gara 1992). The role of the pseudobactin and pyoverdin siderophores produced by Pseudomonas fluorescens has been clearly demonstrated in the control of Fusarium species (Alabouvette et al. 1998; Chincholkar et al. 2007). The sidorophores produced by Pseudomonas spp. were involved in the biocontrol of plant pathogens such as Aspergillus niger (Sindhu et al. 2010). These compounds play an important role in the stimulation of plant growth (De-Souza et al. 2015), and certain plants assimilate the iron directly from Pseudomonas siderophore (Bar-Ness et  al. 1991). Inoculation of seeds by siderophore-­producing PGPRs improves plant growth and increases chlorophyll content (Sharma and Johri 2003). The exploitation of PGPRs producing siderophores in agriculture as agents of biocontrol and plant growth-promoting bacteria is an avenue of research to be explored.

10.4.2  Chitinase Production Chitinase is an enzyme that hydrolyze the insoluble linear polymers of ß (1,4) N-acetylglucosamine, which are the major components of the cell wall of several fungi, insect exoskeleton, and crustacean shells (Bhushan and Hoondal 1998). The microorganisms producing this enzyme are classified as biological control agents (Bhushan and Hoondal 1998; Huang et al. 2005), this is the case of Bacillus cereus, which inhibits the growth of Botrytis elliptica (Huang et al. 2005) and Bacillus sp. S7LiBe inhibiting the growth of B. cinerea (Bensidhoum et al. 2015). In addition, several researchers have shown that chitinases are involved in antifungal activity

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and can enhance the insecticidal activity of Bacillus sp. (Quan et al. 2010). According to Quecine et al. (2008), the majority of Bacillus sp. exhibit high chitinase activity. Some studies have established the relationship between the chitinase of Bacillus sp. and Pseudomonas sp., and their ability to inhibit mycelial growth of Fusarium oxysporum and Fusarium solani (El-Hamshary et al. 2008). Recently, Yandigeri et al. (2015) reported the role of chitinase-producing actinomycete (Streptomyces vinaceusdrappus S5MW2) in improving tomato growth and its competence as a biocontrol agent against Rhizoctonia solani. According to Lim et al. (1991), the biocontrol of Fusarium solani is performed mainly through the chitinase activities in Pseudomonas stutzeri YPL-1. Nielsen et al. (1998) reported that in the rhizosphere of sugar beet, the fluorescents Pseudomonas spp. inhibited the growth of R hizoctonia solani by the production of an endochitinase. The production of chitinases is a biocontrol mechanism, which inhibits the germination of the spores of phytopathogenic fungi (Nandakumar et  al. 2002). In a greenhouse experiment, the soil enrichment with chitin, using bacterial strain S5MW2, has significantly increased the growth of tomato plants and significantly reduced the symptoms induced by the pathogen Rhizoctonia solani. The microorganisms producing chitinase have been reported as potential biocontrol agents (Ordentlich et al. 1988; Inbar and Chet 1991).

10.4.3  Competition for Space and Nutrients In soil, essentially in the rhizosphere, numerous and diverse microorganisms interact with each other and the plant roots, frequently the nutritive sources, are not enough for the entire microbial flora. To ensure their growth and development, and to exercise their activities, these microbes compete over all nutritive elements. Competition consists of the consumption or the control of the access to nutrients, space or any other factor whose availability is limited (Widen et al. 1994). Hattori (1988) has defined the biocontrol competition as the ability of PGPRs to compete with pathogenic organisms by sequestering most of the nutrients and colonizing appropriate niches, so that it constitutes a significant proportion of the rhizosphere– rhizoplane population. Antagonist PGPRs can repress the growth of certain phytopathogenic agents through competition for nutrients such as nitrogen, carbon, or macro- or micronutrients (Elad and Stewart 2007). A special case of competition for nutrients is based on the competition for iron. As described previously, to survive, microorganisms secrete siderophores depriving phytopathogenic agents of one of their growth factors (Pal and Gardener 2006). Johansson (2003) reported that bacteria of the genus Pseudomonas have a great chelating power using siderophores synthesized by other bacteria (Johansson 2003). An important colonization of plant roots by beneficial bacteria can reduce plant disease; this colonization reduces the number of habitable sites for pathogenic microorganisms and consequently their growth. Competition for iron by siderophores (Raaijmakers et al. 1995) and the competition for substrate (Couteaudier and

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Alabouvette 1990) have been suggested as mechanisms of biocontrol agents to suppress plant (Pandey et al. 2013).

10.4.4  Antibiosis Antibiosis is the inhibition of pathogens through the production of substances with antifungal and/or antibiotic properties (Johansson 2003). Several metabolic products with bioactive activities were produced by PGPR, e.g., lytic enzymes (chitinase, protease, glucanase, etc.), antimicrobial proteins or peptides, polyketides, phenolic compounds, bio-surfactants, etc. (Fernando et al. 2005). Fengycin A and B, iturin A mycosubtilin, bacillomycin D and pyochelin, are categories of antibiotics produced by Bacillus and Pseudomonas to control aflatoxigenic fungi (Ghahfarokhi et al. 2013). Another type of antibiotic compound is the volatile compounds, and several authors have reported the ability of PGPR to produce volatile compounds such as ammonia, hydrogen cyanide, acetoin, and 2,3-butanediol (Ryu et al. 2003; Charest et al. 2005; Wani et al. 2007; Ahmad et al. 2008). Yuan et al. (2012) have attributed the significant inhibition of the mycelial growth and spores germination of Fusarium oxysporum to the volatile compound produced by bacteria. The complementation of A cyanide-negative mutant of CHA0 by hcn+genes restored its ability to control the “take-all” of wheat caused by Gaeumannomyces graminis var. tritici (Voisard et al. 1989). Pseudomonas is known for its ability to produce a high level of chitinase and β-1,3-glucanase which hydrolyze the chitin and the glucan present in the cell wall of the phytopathogenic fungi (Arora et al. 2007); Pseudomonas is also a producer of antifungal metabolites (Haas and Défago 2005). Cyanogenic Pseudomonas spp. such as P. fluorescens CHA0 was involved in the suppression of various plant pathogens, particularly fungi (Voisard et al. 1989; Blumer and Haas 2000). By the production of this compound, the rhizosphere bacteria induce systemic resistance of plants to various infections (Kumar et al. 2012). The biocontrol of plant pathogen fungi by P. protegens is related to the production of antimicrobial substances (Notz 2002; Haas and Keel 2003; Ramette et al. 2003; Haas and Défago 2005; Ramette et  al. 2011) and the competition for the nutrients by the production of siderophores (Garrido-Sanz et al. 2016; Bensidhoum et  al. 2016). Certain strains of Pseudomonas fluorescens produce antimicrobial metabolites with a broad spectrum of antifungal activity such as P. protegens CHA0 synthesizing 2,4-diacetylphloroglucinol (DAPG), pyoluteorin (PLT), and pyrrolnitrin (PRN) (Haas and Keel 2003). Weller (2007) has classified several strains of P. fluorescens in which the production of compounds such as phenazines and DAPG is directly related to an antagonistic activity against various pathogens, such as the antagonist activity of P. fluorescens 2-79 and CHAO on Gaeumannomyces graminis. Siddiqui (2006) has also shown the effect of Pseudomonas PsJN on reducing the tomato disease caused by Botrytis cinerea. Nandakumar et  al. (2002) have reported the reduction of Rhizoctonia solani sclerotia germination by the strains Pseudomonas fluorescens PF1, FP7, and PB2.

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It was hypothesized that competition for nutrients, specially competition for carbon, is one of the mechanisms responsible of fungistatic effect which is characterized by the inhibition of spore germination in soil (Alabouvette et al. 2006). Whipps (2001) suggests that the ability of bacteria to parasitize and degrade spores or hyphae of fungal pathogens is due to the production of several enzymes. During the first phase of the host-pathogen interaction, the synthesis of hydrolytic enzymes is crucial for the infection process (Baarlen et al. 2004).

10.4.5  Induced Systemic Resistance PGPRs-plant interaction involved in the control of pathogens consists of the stimulation of plant defense mechanisms. This phenomenon has been termed induced systemic resistance or ISR (Van Loon et  al. 1998), making the host much more resistant to future pathogen aggression. ISR is therefore phenotypically similar to RSA (aquise systemic resistance) which is triggered by phytopathogenic agents. As SAR, ISR is effective against different types of pathogens but differs from SAR in that the inducing PGPR bacterium is colonizing roots and does not cause visible symptoms on the host plant (Borriss 2011; Van Loon et al. 1998). When PGPRs interact with plants, they cause structural and physiological changes that lead to the production of molecules involved in plant defense mechanisms. Bacterial lipopolysaccharides, siderophores, and salicylic acid (SA) are found to be the major determinants of ISR (Antoun and Prévost 2006). Systemic resistance may be induced by various microorganisms, Gram-positive bacteria such as Bacillus pumilus, or Gram-­ negative bacteria belonging to the genus Pseudomonas (fluorescens, putida, aeruginosa) (Jourdan et al. 2008). Arabidopsis seedlings exposed in divided Petri dishes to PGPR B. subtilis GB03 and B. amyloliquefaciens IN937a for 10 days developed significantly less symptomatic leaves 24 h after inoculation with the soft rot-causing pathogen Erwinia carotovora ssp. Carotovora, this suggests that the volatile compounds play an important role in the induction of plant resistance (Borriss 2011; Ryu et al. 2005). Jetiyanon et al. (2003) reported that in an experiment realized in field, a mixture of B. amyloliquefaciens strain IN937a and B. pumilus strain IN937b induced systemic resistance against southern blight of tomato (Lycopersicon esculentum) caused by Sclerotium rolfsii, anthracnose of long cayenne pepper (Capsicum annuum var. acuminatum) caused by Colletotrichum gloeosporioides, and mosaic disease of cucumber (Cucumis sativus) caused by cucumber mosaic virus (CMV) (Antoun and Prévost 2006). Benhamou et al. (1996) have shown that the roots of peas inoculated with the strain P. fluorescens 63–28 produced more chitinase in the penetration site of Fusarium oxysporum. Radjacommare et  al. (2004) have also reported the inhibition of Rhizoctonia solani by Pseudomonas fluorescens by the induction of plant resistance system. Kempster et al. (2002) reported that P. fluorescens spp. produce insecticidal toxin and induce the resistance of plants to the aphids attack. PGPR belonging to Pseudomonas spp. are commercially exploited to

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protect plants by inducing their systemic resistance against various pests and diseases; therefore, it can be said that PGPR will be of great interest, especially to protect plants and avoid problems encountered when pesticides fail to control pathogens populations that have developed resistance (Wang et al. 2002).

10.5  Agricultural Application The use of PGPB as agricultural inoculants is a promising alternative based on the biofertilization and biocontrol properties of these bacteria. The application and fate of inoculants on field-grown crops needs to be carefully validated to ensure that they can produce some demonstrable benefit to yields (Cummings and Orr 2010; Rana et al. 2019; Yadav et al. 2020). Understanding the factors that control and regulate the biosynthesis of bioactive compounds by PGPBs is an essential step to improve the level and reliability of their activity. The study of the influence of these parameters on the activities of PGPBs in  vitro can serve as a preliminary step for the optimization of these activities in vivo or the production of bioactive metabolites. The influence of environmental factors on the performance of PGPR, such as soil type, pH, plant surface, and climatic conditions, has been well documented. Moreover, the abiotic factors are the major factors that determine the efficiency of PGPR (Egamberdieva 2012). Nandakumar et  al. (2002), have also reported that antagonist activity is influenced by the pH and the incubation temperature. The effect of the different abiotic factors such as temperature and nutrients elements on the production of the antifungal molecules by biocontrol agents was published by several authors (Upadhyay et al. 1991). According to Naik and Sakthivel (2006), the bacteria belonging to the genus Pseudomonas are able to use several carbon sources as substrate and can adapt to different environments. The production of the antifungal compounds is affected by a large number of abiotic factors such as: Fe+ 3, Zn+ 2, Cu+ 2, Mo+ 2, and glucose. Fe+ 3 and the sucrose increased the production of DAPG (diacetyl-phloroglucinol) in P. fluorescens strain F113, whereas in the case of P. fluorescens Pf-5 and CHA0, its production is stimulated by glucose (Duffy and Dé-fago 1999). Nutrients elements and environmental factors can influence the antifungal activity of P. cepacia, this is the case of the carbon source which promotes the antagonist activity and inhibits the germination of the spores (Upadhyay et al. 1991). According to Landaa et al. (2004), the temperature influences significantly the ability of bacteria to produce antifungal metabolites. Another parameter that can affect the bioactive potential for bacterial inoculants is their competitiveness; it is obvious that a competitive inoculant will adapt to the soil conditions and it will compete with the indigenous organisms (Cummings and Orr 2010). By using a mathematical modeling and computer-based simulation, Strigul and Kravchenko (2006) have attempted to evaluate microbial inoculant in the rhizosphere, and the impact of the different abiotic and biotic stress on PGPBs survival and activities (Cummings and Orr 2010). As a result of their study, Strigul and Kravchenko (2006) have proved that the

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most important factor determining inoculants survival was the competition for limiting resources between the introduced population and the resident microorganisms. Inoculants survival was also affected by the compatibility between the composition of the host plant roots exudates, and the ability of the inoculated bacteria to utilize those compounds. Knowledge of different mechanisms involved in plant growth promotion and disease suppression is essential for the selection and utilization of appropriate biocontrol strains for sustainable agriculture (Pathma et al. 2011). As mentioned previously, to ensure an improvement in field-grown crop yields by using PGPBs inoculants, it is necessary to select these inoculants and to take account of the influence of the different environmental parameters. The mode of application of bacterial inoculants (foliar spray, post-harvest treatment, seed treatment, etc.) can also influence the activity of inoculants.

10.6  Conclusion and Future Prospects The use of PGPBs in agriculture is a promising alternative that can positively influence plant performance and health. Understanding the methods of protection and improvement of plant growth allows to improve crop yields and therefore meet ever-increasing demands. The results obtained with the PGPBs support the transition to a culture “bio-agriculture” healthy and beneficial to human health and the national economy. The exploitation of PGPBs in agriculture is a promising alternative to chemical products (fertilizers and pesticides) that are harmful for both environment and public health. All that has been previously reported about the potential of PGPBS in soil biofertilization and biocontrol of phytopathogenic agents as well as the promotion of plant growth encourage their commercial exploitation and use as inoculants.

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Whipps JM (2001) Microbial interaction and biocontrol in the rhizosphere. J Exp Bot 52:487–511 Widen B, Cronberg N, Widen M (1994) Genotypic diversity, molecular markers and spatial distribution of genets in clonal plants, a literature survey. Folia Geobot 29:245–263 Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016a) Cold active hydrolytic enzymes production by psychrotrophic bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56:294–307 Yadav AN, Sachan SG, Verma P, Saxena AK (2016b) Bioprospecting of plant growth promoting psychrotrophic Bacilli from cold desert of north western Indian Himalayas. Indian J Exp Biol 54:142–150 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B et al (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Verma P, Kour D, Rana KL, Kumar V, Singh B et al (2017b) Plant microbiomes and its beneficial multifunctional plant growth promoting attributes. Int J Environ Sci Nat Resour 3:1–8. https://doi.org/10.19080/IJESNR.2017.03.555601 Yadav AN, Verma P, Singh B, Chauhan VS, Suman A, Saxena AK (2017c) Plant growth promoting bacteria: biodiversity and multifunctional attributes for sustainable agriculture. Adv Biotechnol Microbiol 5:1–16 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018a) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, Amsterdam, pp 305–332 Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP et  al (2018b) Actinobacteria from rhizosphere: molecular diversity, distributions and potential biotechnological applications. In: Singh B, Gupta V, Passari A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  13–41. https://doi.org/10.1016/ B978-0-444-63994-3.00002-3 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N et  al (2018c) Biodiversity of the genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering. Penicillium system properties and applications. Elsevier, Amsterdam, pp  3–18. https://doi.org/10.1016/ B978-0-444-63501-3.00001-6 Yadav AN, Gulati S, Sharma D, Singh RN, Rajawat MVS, Kumar R et al (2019a) Seasonal variations in culturable archaea and their plant growth promoting attributes to predict their role in establishment of vegetation in Rann of Kutch. Biologia 74:1031–1043. https://doi.org/10.2478/ s11756-019-00259-2 Yadav AN, Singh S, Mishra S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. Volume 2: Perspective for value-added products and environments. Springer International Publishing, Cham Yadav AN, Singh J, Rastegari AA, Yadav N (2020) Plant microbiomes for sustainable agriculture. Springer International Publishing, Cham Yandigeri MS, Malviya N, Solanki MK, Shrivastava P, Sivakumar G (2015) Chitinolytic Streptomyces vinaceus drappus S5MW2 isolated from Chilika Lake, India enhances plant growth and biocontrol efficacy through chitin supplementation against Rhizoctonia solani. World J Microbiol Biotechnol 31:1217–1225 Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. Cubense. Appl Environ Microbiol 78:5942–5944 Zahir ZA, Arshad M, Frankenberger WTJ (2004) Plant growth promoting rhizobacteria: application and perspectives in agriculture. Adv Agro 81:97–198

Chapter 11

Impact of Biopesticides in Sustainable Agriculture Hina Upadhyay, Anis Mirza, and Jatinder Singh

Abstract  Chemical pesticides are used to control fungi, bacteria, insects, plant diseases, and weeds. Synthetic pesticides may regulate several kinds of insect pests effectively and completely; however, they have a negative impact on biodiversity and the entire ecosystem. Biopesticides are currently introduced in the market, produced from natural materials, especially from local flora  and microorganism. By using such kind of materials, use of lethal and harmful, man-made synthetic chemicals can be reduced to a great extent. The materials used during production of biopesticides may be secondary metabolites of different organisms. Biopesticides may be readily available from commonly occurring natural materials like fungi, animals, bacteria, and some plant products. Apart from this, another example of plant-based biopesticides includes chili, garlic, ginger, neem, and their products. These are some of the best one, considered as effective biopesticides. However, such formulations are facing challenges for their registration, accepted formulation, adoption, and commercialization. Moreover, consumer awareness is increasing day by day regarding the quality and safety of crop produce. This is the main reason in rejecting harmful chemicals used  for crop production for sustainable agriculture. This book chapter highlights the potential sources of biopesticides; their production, registration, and challenges during usage; and their importance in sustainable insect pest management. Keywords  Bioformulation · Biopesticide · Bioproduct · Sustainable agriculture

H. Upadhyay Department of Agronomy, Lovely Professional University, Phagwara, Punjab, India A. Mirza · J. Singh (*) Department of Horticulture, Lovely Professional University, Phagwara, Punjab, India e-mail: [email protected] © Springer Nature Singapore Pte Ltd. 2020 A. N. Yadav et al. (eds.), Advances in Plant Microbiome and Sustainable Agriculture, Microorganisms for Sustainability 19, https://doi.org/10.1007/978-981-15-3208-5_11

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11.1  Introduction Since primitive times, several efforts have been done to guard harvest produce against insect pests. During ancient time, Indian and Egyptian farmers used to mix ashes with the stored grains (Bhargava 2009). False hellebore (bot. name – Veratrum album) are used to control rats. It contains insecticidal properties as that of Derris species. While in some parts of the world, local flora is used to protect stored produce against insect invasion. In our country, farmers use neem plant extracts for the regulation of storage insect pests (Sharon et al. 2014). Furthermore, increasing population, pressure on land, and food requirement and higher food production that entails increased use of inputs and fertilizers made the situation worst. Day by day new kinds of pesticides/weedicides are introduced, which are very costly, and after some time particular type of insect/weed. And the same insect/pest becomes epidemic, with some resistant features. To control insect-pests, several pesticide companies have introduced some kind of pest-resistant varieties (which have genetic resistant feature against the same) or some mixture of highly poisonous mixture of pesticides, but they are too costly, and you have to purchase repeatedly from the company. The importance of biopesticides is difficult to ignore under such circumstances. Under such situation, we are left with no alternative. Perhaps we may get rid of this problem as biopesticides are secondary metabolites and by-products of living substances such as insects or different microorganisms as well as plants which are found in nature (Gasic and Tanovic 2013). Biopesticides comprise wide-ranging microbial insecticides, microorganisms (biochemicals derived), and other sources of nature and advancements including the genetic combination of DNA in farming products that deliberate protection counter to the damage done by pest (Gupta and Dikshit 2010). As a result, there has been advancement in worldwide market diffusion, but biopesticides still account for a slight portion of pest regulator goods (Glare et al. 2012). Major sources of biopesticides are plants and microorganisms because they contain high components of bioactive compounds (Nefzi et al. 2016). Various plants have wide-ranging antimicrobial bioactive combinations of compounds, which may contain various oil components such as α-/β-phillandrene, limonene camphor, linalool, and β-caryophyllene, etc. (Ali et al. 2017). Biopesticides demonstrate several types of action to counter particular harmful germs such as competition lysis, predation, or hyperparasitism (Vinale et al. 2008). There are huge number of plant growth Promoting bacteria (PGPB) used as biopesticides such Agrobacterium, Microbacterium, Ensifer, Pseudomonas, Bacillus, and Rhizobium, Rhodococcus (Abbamondi et al. 2016; Yadav et al. 2020; Yadav et al. 2017). They help the environment by living around or in plant parts like roots to fix environmental nitrogen and also increase phosphate solubilization process and consequent improvement in plant yield (Compant et al. 2010; Kour et al. 2020a; Rana et  al. 2020a). These PGP microbes are also used as biofertilizers (Esitken et  al. 2010; Kour et  al. 2020b; Rana et  al. 2020b). Predators and pathogens including some insects are also used in managing insect-pest problem. These include different

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types of beetles (ladybirds), parasitoids, bugs, wasps, and lacewings which are used in controlling some destructive insect/pests such as bollworms (Helicoverpa armigera) in specific crops (Knutson and Ruberson 2015). Besides this, some filtrates and compost teas from compost extracts are used as biopesticides in crops (Ghorbani et al. 2005). The use of oils in stored produce for pest control was an old practice. Several botanical insecticides like pyrethrum, nicotine, derris, and oil of citronella have been used for many years. At present more than 150 species (almost) of roadside and forest trees in India produce such oilseeds, and these have been normally used for homeopathic purposes and also as insecticides. Calotropis, castor, turmeric, ginger, Datura, Aristolochia, Agave americana, Ipomoea, coriander, and garlic are some commonly used botanical materials to regulate crop pests (Rajashekar et al. 2012; Verma et al. 2010). This chapter deliberates the recent situation and prestige of biopesticides and their significance in sustainable agriculture. It provides the several categories of biopesticides, confirming their use against insect/pests in various crops. There are some success stories regarding application of biopesticides and agents in Indian agriculture, which include: 1 . Controlling diamondback moths by Bacillus thuringiensis 2. Controlling mango hoppers/mealy bugs/coffee pod borer by Beauveria 3. Controlling Helicoverpa on cotton and tomato by Bacillus thuringiensis 4. Controlling white fly in cotton 5. Controlling Helicoverpa on gram 6. Controlling sugarcane borers In India, the area under organic crops is over 1,00,000 ha (Kalra and Khanuja 2007). Moreover, the area under forests is also certified as organic. Uttaranchal and Sikkim have been declared as organic states. Still, this type of crop cultivation may cover more area because of the growing demand for organic products, which is a result of a society more conscious about health. This reveals a huge potential in expanding the use of biopesticides like in India (Gupta and Dikshit 2010). Presently in the US market, more than 200 bioproducts are being vended whereas in the EU market 60 products. Above all, more than 225 microbial biopesticides are prepared in 30 OECD (Organization for Economic Co-operation and Development) countries. Some countries like the USA, Canada, and Mexico use nearly half of the biopesticide products, while in Asia only 5% of biopesticides are sold. North America was the first place in the world biopesticides market, by donating for around 40% of the global biopesticides requirement in 2011 was reported. Europe is seen to be the fastest growing bazaar in the near future, owing to the strict regulations on the use of pesticides and the reported growing demand for organic products (Nagappan Raja 2013). Our country, only 14–15 biopesticides have been registered so far according to Insecticides Act 1968 (Table 11.1). Today, in most parts of the world, use of biopesticides is emphasized as they are recyclable and non-phytotoxic. As a result, several botanical constituents have been verbalized for applying as biopesticides in eco-friendly administration and are being applied as alternative to synthetic compounds in protection of the plant. In spite of

Viruses

Fungi

Nematode

Neem

2.

3.

4.

5.

Type of S.N. organism 1. Bacteria Name of biopesticide Bacillus thuringiensis var. israelensis (Bti)

Antifeedant, repellent, and repugnant agent

Azadirachtin acts as an insecticidal ingredient Cymbopogon, garlic

Bacillus thuringiensis var. aizawai Bacillus sphaericus Bacillus popilliae Bacillus firmus Bacillus thuringiensis var. galleriae Agrobacterium radiobacter Pseudomonas fluorescens Kill insects when ingested. Insects’ digestive Baculoviruses: nuclear polyhedrosis virus (NPV) system is disrupted; thus it starves and dies Baculoviruses: granulosis virus (GV) Baculoviruses: Group C entomopox NPV of Helicoverpa armigera NPV of Spodoptera litura Control insects by growing on them secreting Trichoderma viride, Trichoderma harzianum enzymes that weaken the insect’s outer coat Heterorhabditis bacteriophora and then getting inside the insect and continuing to grow, eventually killing the infected pest There it releases its bacteria, which multiply Phasmarhabditis hermaphrodita and kill the host insect Steinernema carpocapsae Heterorhabditis bacteriophora

Mode of action Use to kill a particular organism Crystal proteins that poison, paralyze, and kill targeted pests after ingestion

Table 11.1  Details of biopesticides and their uses

Black vine weevil, Japanese beetles Various slugs and snails Black vine weevil, strawberry root weevil, cranberry girdler Against various borers Against white fly and other insects

Against root rots and wilt

Uses against Mosquito larvae, fungus gnat larvae, blackfly larvae Lepidoptera: moths, butterflies Controlling insect vectors Japanese beetle Root-knot nematodes Japanese and Oriental beetles Crown gall disease Fungal and nematode diseases Lepidopteran and Hymenopteran Lepidopteran Arthropods Helicoverpa Spodoptera litura

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many complications, research studies in plant-derived such pesticides, has persuaded prominently (Rahman and Islam 2007); Rahman and Talukder 2006 and Murti et al. 2010). Moreover, unnecessary use of pesticides may result in the devastation of biodiversity and nontarget species, secondary pest occurrences, and water, soil, and air adulteration (Recena et al. 2006).

11.2  Challenges in the Use of Pesticides 11.2.1  Direct Effect on Humans Few pesticides may bring adverse effects to the immune system as it has been found out that long-term or contact (exposure) to such chemicals progressively results in various effects such as hormone disruption, reduced brainpower, immune suppression, cancer, and generative irregularities (Hurley 1998; Crisp et  al. 1998). An example is the use of Agent Orange, a herbicide and defoliant chemical, of the US military during the Vietnam War. There were some  reports on cancer hazard in Vietnam occupationally unprotected to weedicides or dioxins and of the Vietnamese population (Frumkin 2003). Environmental acquaintance to various noxious pesticides is a prominent health hazard to all living beings (Rothlein et al. 2006; Keifer and Firestone 2007; Azmi et al. 2006; Singh 2011). Absorption, inhalation, and diffusion are some common courses of pesticide to enter the body (Spear 1991). Youngsters, especially kids, less than 10 years, persons who apply these pesticides, and other farm employees are more vulnerable to pesticide’s venomousness than others. The removal of pesticide is accomplished by the body, but some scums of injurious pesticides are engrossed by blood system (Jabbar and Mallick 1994). Richter (2002) reported that 3 million tons of pesticides is used worldwide, which may result in non-fatal pesticide poisoning.

11.2.2  Impact Through Food Commodities The first report of pesticide poisoning in India came from Kerala state in 1958, where more than 100 people died after consuming wheat flour contaminated with parathion chemical (Karunakaran 1958). However, considering that the use of pesticides in agriculture is quite frequent, it has been estimated that the normal daily ingestion of DDT and HCH by Indians was between 48 and 115 mg per person, which was noticeably higher than that reported in developed nations (Kannan et al. 1992). It is important to note here that DDT is banned nowadays. Worldwide researchers have accredited the inclined and insensitive use of chemicals for pests in the large-scale manufacturing courses to meet the increasing need for world’s food productivity though, recently, pertinent issues associated with human safety,

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health, and the environment are intimidating the continued application of man-made pesticides (Mazid et  al. 2011). Subsequently, several researchers (Anilmahajan et al. 2004; Ashutosh and Paul 2004) have described the occurrence of various synthetic insecticides in different food products. Moreover, these studies highlight the increasing risks of agrochemicals to human beings and the increasing resistance to embattled pests and its unmaintainable nature. Some chlorinated OCPs may persist constantly for a long period, many years after application (Afful et al. 2010). Many of chemical pesticides are un-degradable in nature (Darko and Acquaah 2007; Afful et al. 2010; Kumar and Singh 2017). Consequently, living beings are subjected to the injurious influence of micropollutants through contaminated food, water, or soil.

11.2.3  Effect on Environment Udeigwe et  al. 2015 reported that the greater use of agricultural chemicals can increase the economic productivity, but very less attention is given to the environmental aspects. An example is Japan where pesticides are normally detected in environments and childcare services following the application of chemical pesticides. It should be noted that there have been alarming issues of chemical residues in soil, water, air, agricultural products, and even human blood and adipose tissue (Alvarez et al. 2017; Ridolfi et al. 2014; Kawahara et al. 2005). The chemical pesticides are toxic to a host plant as well as to various organisms like beneficial insects and birds, along with nontarget ones. Most insecticides are included in highly toxic grouping of insecticides, but chemicals as weedicides can also present maltreatment to various nontarget organisms. Moreover, the research described that acquaintance to pesticides can happen through various sources like food, water, and inhabited or occupation pathways which lead to combined toxicological influences on the environment and humans (Boobis et al. 2008). Pesticides are organochlorines in nature. These are least decomposable and they are expelled in many countries. These are exceptionally used in several locations. This leads to considerable threats regarding health. Pollution especially (water) rises due to such pesticides, even if used at lower concentrations. These lethal substances pose severe danger to the surrounding environment (Agrawal et al. 2010). But unfortunately, many growers/farmers are ignorant about their potential hazards as they have no or very poor knowledge about classes of pesticides, lethal dose, protection procedures, and subsequent hazards. Eventually, persistent and poisonous chemicals are used to eradicate the pests which results in supplementary, deliberately, or job-related contact. Such chemicals have long-term effects on human health. Farmers should be given information to lessen the uses of such poisonous pesticides (Sharma et  al. 2012). Accordingly, there is a crucial necessity to discourse the environmental and toxicological effects of augmented pesticide consumption worldwide. This is a serious threat to food production and sustainable environmental protection specifically against the backdrop of appeals to prevent the forthcoming impacts of climate change comprising global warming in susceptible developing countries. Hence, the advancement and

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adoption of innovative approaches, procedures, and products are immediately obligatory. Further, various chemical pesticides could be used mixed with normal treatments which leads to sustainable eradication of insect-pests.

11.2.4  Surface Water Contamination Indiscriminate pesticide uses in agriculture result in disturbances among natural enemies, populations of soil, and aquatic arthropods considerably. The results submitted by the US Geological Survey (USGS) agency on prime river basins through the country were surprising. According to a report submitted by this organization, more than 90 percent of samples (fish and water) contained several kinds of pesticides (Kole et al. 2001). Furthermore, the USGS recognized that concentrations of various chemicals in urban (particularly) watercourses normally surpassed limits to safeguard of life in water (US Geological Survey 1999). Insecticides and weedicides, like diuron, prometon, chlorpyrifos, diazinon, and 2, 4-D, frequently used by urban landholders, were get accumulated frequently on soil surface and groundwater all over the country (US Geological Survey 1998). Adsorption of these pesticides reduces their transference to surface water and natural wetlands or built one. However, adsorption in man-made or natural wetlands may depend on several hydraulic parameters as recognized by Gaullier et al. (2018). The influence of pesticides on water environment is affected by their solubility and ability (Khare 2012).

11.2.5  Groundwater Contamination Groundwater can be defined as the water found below the surface of the earth, in soil pores and cracks in rock developments (The Groundwater Foundation, Lincoln, NE, USA 2018. Toccalino et al. 2014 and Ouedraogo et al. 2016). Among various herbicides like triazine group (simazine atrazine, cyanazineterbuthylazine, prometrynpropazine, terbutryn), phenylureas (chlortolurondiuron, isoproturonlinuron), anilides (metolachloralachlor and acetochlor) and insecticides/pesticides such as organophosphorus (parathion-methyl malathion, dimethoatechlorfenvinphos, fenitrothionazinphos-­ethyl and organochlorine) and some of its derivative products are some common pesticides occurred in groundwater. Because of these pesticides, pollution of groundwater is the foremost worldwide occurring problem. According to the USGS organization, 143 types of pesticides (chemicals) and 21 resulting products have been accessed from groundwater. According to one survey in India, 58 percent of the samples of drinking water collected from various water sources and hand pumps around Bhopal area were contaminated with organochlorine chemicals, and they were above the EPA standards (Kole and Bagchi 1995). Once water is adulterated with toxic chemicals, it requires a lot of time for purification. Moreover, the process is very complex and costly (Waskom 1994; O’Neil et  al.

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1998; US EPA 2001). It has been described that important herbicide named Roundup (glyphosate) may have a lot of undesirable effects on nontarget amphibians (Relyea 2012). Farmers and farm laborers, handling the pesticides, are at a high risk of exposure to these harmful chemicals while mixing and applying pesticides or operating in treated fields (Soares and de Souza Porto 2009). Different factors such as physicochemical properties of chemicals pesticide, the soil penetrability, organic matter and texture, crop root uptake, volatilization, and the method of application are mainly responsible for the leaching process. Leaching constitutes an environmental risk because they can reach the water table and contaminate shallow groundwater and deeper aquifer. Moreover pesticides having low perseverance do vanish rapidly, and hence the risk of groundwater pollution decreases (Pérez-Lucas et  al. 2018). They have posed a hazard on the integrity (especially biological) of aquatic and marine environment. We can make a multidisciplinary study to comprehend the direct and indirect influences of these pesticides for sustainable environment (Macneale et al. 2010).

11.3  Microorganisms as Sources of Biopesticides Biopesticides have been of great interest in the research community and have attracted great attention to synthetic pesticides in controlling pests (Rastegari et al. 2020b; Singh and Yadav 2020). Biopesticides are chemicals or natural materials made from plants, animals, bacteria, and certain minerals to control harmful organisms (Kour et  al. 2020c; Rastegari et  al. 2020a). Some plant products used as a source for major biopesticides. Pesticidal activity is also reported in the oil of some plants such as neem and canola. More often, various types of microbes have also been used effectively as a biopesticides. The cited literature suggests that biopesticides have been successfully used to enhance plant growth and ultimately to increase yields (Kaur et al. 2020; Singh et al. 2020). Generally, biopesticides affect only target pests and closely related organisms. Secondary metabolites of a certain group of organisms acting as a biocontrol agent include biofungicides (Trichoderma sp.), bioherbicides (Phytophthora sp.), and bioinsecticides (Bacillus thuringiensis). Furthermore, biopesticide serves as chemical pesticide substitutes, which contains a broad array of biochemicals, derived from microbes and other natural plant-based sources. By FAO’s definition, biopesticides include biocontrol agents, such as plant-derived products, semiochemicals (pheromones), parasites and predators, many species of entomopathogenic nematodes, and their secondary metabolites. Nevertheless, many agents were used at very small scale because it is very difficult to multiply them by large volumes. In spite of these, several organisms are potentially presented as biological control of some deadly organisms like mosquito including bacteria, viruses, fungi, invertebrates, nematodes, and fish (Yadav et al. 2018, 2020; Verma et al. 2017). It is important to mention here that particular species of organisms are induced from elsewhere and used to control pests, etc. in some other parts of the world.

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11.3.1  P  roduction, Formulation, and Commercialization of Biopesticides The research gap could be filled for the expected anticipated future trends in formulation and development of biopesticides for sustainable insect pest management. Seaman (1990) and Boyetchko et al. (1999) also stated that the problem in preparing biopesticide products is a fairly and completely fundamental understanding of the process. According to their physical state, biopesticide formulations can be divided into liquid and dry formulations. Liquid formulation has water-based, oil-based, polymer-based, or combinations thereof. Suspension, suspension-emulsion, and capsule suspensions are the examples of water-based formulations. Inert ingredients such as stabilizers, stickers, surfactants, coloring agents, antifreeze compounds, and other additional nutrients are required to be added during biopesticide formulation. Tadros (2005), and Brar et  al. (2006) stated that by using different methods, dry formulations can be prepared through spray drying and freeze drying. With the help of binder, dispersers, and wetting agents, dry formulations can be made. Each formulation strain is produced in a determined way. Knowles (2006) also reported that biopesticides are commonly formulated in different forms. The example of dry formulations, to be used for direct application include dusts, seed dressing formulations –seed dressing powders, granules, and micro granules. Some important liquid formulations for dilution in water comprise suspension concentrates, emulsions, suspo-emulsions, oil dispersions, capsule suspensions and ultra-low volume formulations. In most cases, the active ingredients of biopesticides are prepared like synthetic pesticides. It is considered as one of the best suitable methods for users as it permits them to use the like equipment/devices for unlike treatments. Almost all biopesticides are based on living organisms. The feasibility of these living organisms must be retained under favorable conditions during the operation and storage. Whenever its application is needed, the living organism should regenerate from its dormant state. Seaman (1990) also stated in this regard that problems in formulation of biopesticidal products are considerable and thorough fundamental considerate of the processes causing loss of viability is mandatory for further advancement.

11.4  Plant Biopesticides Commercialization of plant biopesticides is still in the initial stage, so a lot of development and research has been required in this direction for the sustainable insect-­ pest management. Therefore, product development formulation, standardization, and application need to be invested in simple active ingredients from simple crude extracts. Pesticide plants are still considered an alternative to synthetic pesticides with an increase in organic farming methods. Various crude and/or processed products are being discovered in many countries for commercial production of biopesticides. But in the present time, there are still very few successful commercial pesticidal plant products in use.

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Currently one of the most successful insecticide plants in the world is Azadirachta indica, which is an example from the successful plant biopesticide as neem product. Azadirachtin is the active pesticide component of neem oil. A relatively small number of such biopesticides are operated by manufacturers and formulators of active ingredients in Asia and Europe. Technically the high cost of research and registration of new pesticides excludes smaller companies.

11.5  Modes of Action of Biopesticides Use of Bt (Bacillus thuringiensis) began in the late 1970–1980 and continued till date, employing an unlike molecular method to advance market acceptance of biopesticides. Previously, numerous attempts were made to establish microbial pesticides similar to Bt. • Afterward, several other Bacillus species like Bacillus thuringiensis israelensis (Bt) and Bacillus sphaericus (BS) 2362 were discovered effective for mosquitoes and some other dipteran larvae. Bt is promoted globally for regulation of various plant pests, primarily mosquito larvae, caterpillars, and black flies. Genes which are toxic in nature are isolated from Bt and have been engineered genetically in crops. Such type of genes are quite common in some crops like cotton, sarson, etc. Marketable Bt-based products comprise powders combining crystal toxins and dried spores. Leaves and other infected plant parts are treated with such biopesticides or where insect larvae feed. • Various species of bacteria including their species, particularly Pseudomonas, etc., have been recognized to be used as biopesticides and are frequently used to govern various pests and diseases of the plants like bollworm control in cotton, etc. • Bt generates crystalline protein materials that kills insect lepidopteran. The binding of crystalline protein material to the insect receptor regulates the target insect. Bt and their subspecies generate various pesticide crystal proteins (endotoxins), and their toxic property is resolute. Such endotoxins, when swallowed by larvae, etc., can be proved harmful for intestinal tissue, causing intestinal paralysis. The infested larvae stopover consumption and as a result they die from the combined influence of starvation. Constant monitoring of microbial pesticides is needed to confirm that they are not proficient in injuring nontarget animals, including all mammals (Mazid et al. 2011). • In earlier experiments, pesticide of microbial natural advances has led to a significant lessening of synthetic pesticide usage. It was described Bt toxins originating from rhizobacteria promoting plant growth, which also develop bactericidal compounds of pesticide characteristics. • Genes with toxic properties have been genetically engineered from Bt in many crops. Many entomopathogenic fungi along with their derivatives are used as microbial insecticides, too. For example, Metarhizium species (Metchnikoff) Sorokin, also recognized as green muscadine fungi, Metarhizium anisopliae, are hyphomycete entomopathogenic type of fungus and commonly used for regula-

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tion of insect and are abundant globally. This species has long been known for their biological control probably against arthropods. This particular species encompasses a large number of various strains that can be isolated from different geographical backgrounds and from diverse categories of hosts. • In normal circumstances, Metarhizium occurs in earth, wherever humid circumstances allow solitary growth and the production of infectious spores, named as conidia that infect insects that live in exposed soil. M. anisopliae is also a suitable candidate for further development and research. Nowadays, such fungi have been itemized as microbial mediators and are also under advancement for biological regulation of many insects.

11.6  Biopesticides and Eco-friendly Insect Pest Management Around the world, nature is considered as the most important approach to healing. However, the use of synthetic chemicals surpassed biochemicals due to their reliability, efficacy, and quick knockdown effect. This is a common and scientific fact that synthetic pesticides are injurious to human health and the environment as they are toxic and complex in nature. Biopesticides have been considered as potential substitutes to synthetic pesticides (Kumar et al. 2019; Rajawat et al. 2020). These are readily available, perform a wide variety of actions, are easily biodegradable, and are economically affordable and have lower toxicity to all the biotic and abiotic components of our environment. Many plant species including tobacco, neem, and cotton are well-known sources of botanical natural insecticides and have already been marketed. Moreover, other sources of biopesticides include citrus, garlic, chili, and black pepper which are not so commercially available in the market. Sustainable fortification needs execution of policies that involve biological agents for control and use of bioproducts. Such kind of formulations should be encouraged for management of problem of pest and advancement of crop production. Some strains of Bacillus, Trichoderma, and Pseudomonas have already been commercialized as microbicides (Kour et al. 2020d; Rana et al. 2020c). Many aspects on bio-agricultural development are described in this paper; as of now they are not restricted to their sources, production, roles in manufacturing, commercialization, effectiveness, and sustainable agriculture. Therefore, in present scenario, there is a vital necessity to improve production of food, pest abolition and management of disease, etc. before harvesting through the adoption of new, economical, cost-effective farming practices. In recent years, biopesticides are becoming increasingly popular, and they are considered safer than traditional pesticides. As we know these compounds are used in small amounts and are effective, and in addition, they are able to decompose quickly, without leaving problematic residues; therefore, they can be used as traditional pesticides for sustainable agriculture. Damalas and Koutroubas (2018) also reported research on the market for biological control agents, which are important for the protection of our natural ecosystem. Many scientists from diverse research institutes have done some preliminary research, but systematic work for the development of biopesticides is required.

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11.7  Limitations Pesticides are chemical substances used to destroy pests or other organisms harmful to plants. Pesticides can cause short-term or long-term adverse effects to the environment and human health, and they can be classified as acute or chronic. Vaishali Kandpal (2014) stated that farmers are using pesticides which are well packaged and readily available. Even though growers recognize the importance of using plant products as substitute to synthetic pesticides, the extensive use of these natural plant products will take some time to become common. Farmers are using only chemical pesticides. Government and private companies are not taking initiative for the production of biopesticides. That is why in the market, there is a scarcity of biopesticides available. Biopesticides can be produced in large scale and popularized, and make it readily available to farmers.

11.8  Conclusion and Future Prospects Pesticides are chemical substances used to destroy pests or other organisms harmful to plants. Biopesticides are active ingredients based on microorganisms as well as some plant-based products. As a future trend in quality manufacturing and their development as biopesticides, bacteria, fungi, viruses, nematodes, and other naturally occurring substances such as plant extracts and semiochemicals such as pheromones may be involved. With this concept, the future improvement and developments of manufacturing biopesticides can be enlightened. Noteworthy progress has been made in the applications of biopesticides, formulations methods, still much work to be done for plant protection, and for the sustainable management of agroecosystem. As the climate is changing day by day, in this situation diversity of insect and microbes are changing its behavior, so in the present scenario, improvements on plant protection techniques and multidisciplinary research are required. This will be helpful and are likely to provide safe, good, and economical crop production. Acknowledgments  Authors are highly thankful to central library, Lovely Professional University, Jalandhar for providing relevant literature for review along with Department of Horticulture and Agronomy.

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