Plant Growth Promoting Microorganisms of Arid Region 9811941238, 9789811941238

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Ritu Mawar · R Z Sayyed Sushil K Sharma Krishna Sundari Sattiraju Editors

Plant Growth Promoting Microorganisms of Arid Region

Plant Growth Promoting Microorganisms of Arid Region

Ritu Mawar • R Z Sayyed • Sushil K Sharma • Krishna Sundari Sattiraju Editors

Plant Growth Promoting Microorganisms of Arid Region

Editors Ritu Mawar Division of Plant Improvement and Pest Management ICAR-Central Arid Zone Research Institute Jodhpur, India Sushil K Sharma National Institute of Biotic Stress Management Raipur, India

R Z Sayyed Head of the Department PSGVPM’S ASC College Shahada, India

Krishna Sundari Sattiraju Biotechnology Department Jaypee Institute of Information Technology Noida, India

ISBN 978-981-19-4124-5 ISBN 978-981-19-4123-8 https://doi.org/10.1007/978-981-19-4124-5

(eBook)

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Foreword

The Indian Thar Desert represents a harsh ecosystem with extreme climatic conditions having diverse life forms which require adaptive mechanisms for their survival. In addition to the critical role of plants in desert biodiversity, species of insects and microorganisms comprise the largest group of organisms, some of them are little known or rarely discussed. They are involved in various vital ecosystem services such as pollination, decomposition, recycling of nutrients, and enhancing plant immunity and act as important links in parasitoids, food chain, predators, herbivore, etc. However, in the food chain, indiscriminate use of agrochemicals or pesticides indirectly increases the toxic levels. To obviate these snags, the application of beneficial microorganisms in agriculture has increased in terms of biofertilizers and biopesticides as these provide sustainably higher economic yields. Systematic studies have been initiated to explore biocontrol potentials of microorganisms in order to develop a cost-effective and practical management strategy for plant diseases. This book discusses various aspects of microorganisms and their key role in development of healthy desert ecosystem. Additional, commercialization and regulatory issues concerning biopesticides have also been discussed in a manner that will be invaluable for academicians, scientists, researchers, and policymakers. I congratulate the editors for their useful efforts to publish such a good and informative book. New Delhi, India 15 Feb 2022

S. C. Dubey

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Preface

Deserts are characterized by scarce natural resources and an inhospitable climate. Rainfall is highly erratic and unpredictable. The region experiences extremes of temperature (-2 °C to 48 °C), high wind velocity, and sandy soil. The main problem hampering crop growth and productivity in an arid ecosystem is drought, which is further accentuated by global climate change events and is estimated to have reduced cereal, legumes, oil seeds, and spices productivity by 10–40%. Crop productivity can be increased by inoculating the plants facing drought stress with plant growthpromoting microorganisms (PGPM). The thin layer of soil immediately surrounding the plant roots is an extremely important and active area for root activity and metabolism and is known as rhizosphere. A large number of microorganisms such as bacteria, fungi, actinomycetes, protozoa, and algae coexist in the rhizosphere. The microorganisms that colonize the rhizosphere can be classified according to their effects on plants and the way they interact with roots, some being pathogens whereas others trigger beneficial effects. The microorganisms inhabiting the rhizosphere and beneficial to plants are termed PGPM. Various species of bacteria and fungi have been reported to enhance plant growth. There are several PGPM inoculants currently commercialized that seem to promote growth through at least one mechanism: suppression of plant disease (Bioprotectants), improved nutrient acquisition (Biofertilizers), or phytohormone production (Biostimulants). Hence agriculturally important microorganisms have come under focus for the management of various crop health due to their unique abilities to survive in the arid ecosystem and reducing the severity of the diseases. This book aims to gather contributions from leading scientists and researchers, with focus on microbial diversity in arid lands and deserts versus specific microbial assemblages associated with plants. The ecological drivers that shape this diversity, how plant-associated microbiomes are selected, and their biotechnological potential are discussed. Many of the chapters include PGPMrelated activities of microbes from arid regions and provide novel research avenues for further exploration of potential microbial candidates for their application in plant disease management strategies aiding agricultural sustainability in arid lands. Diversity and functional redundancy of these associated PGPM makes them very active in vii

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supporting plant improvement, health, and resistance to drought, salt, and other stresses. Implementing proper biotechnological applications of the arid and desertadapted PGPM constitutes the challenge to be raised. Further, commercialization and regulatory issues concerning biopesticides have also been discussed in a manner that will be invaluable for academicians, scientists, researchers, and policymakers. We expect that the book would be very useful for students, researchers, industrialists, entrepreneurs, academicians, and policymakers to understand the roles of plant growth-promoting microorganisms in sustainable agriculture and provide directions for the future course of action. Jodhpur, India Shahada, India Raipur, India Noida, India

Ritu Mawar R Z Sayyed Sushil K Sharma Krishna Sundari Sattiraju

Acknowledgments

“NO ONE CAN WHISTLE A SYMPHONY. IT TAKES A WHOLE ORCHESTRA TO PLAY IT.” The book as you see today is the work and toil of all the participating editors operating under the stewardship of the principal editor, all sticking to the adage “Together Everyone Achieves More.” As a team we realized at every step the significance of planning, execution, mutual respect to timelines, and deliverance. Writing a book is harder than we thought and more rewarding than we could have ever imagined. None of this would have been possible without the support and guidance of our mentors Prof. M.S. Reddy, Founder Chairman, Asian PGPR Society, and Prof. Satish Lodha, Principal Scientist at CAZRI. Prof. Reddy with his dynamic and enterprising nature is the emotional powerhouse to propel all such initiatives that promotes, propagates, and perpetuates research on Plant Growth-Promoting Microorganisms. Prof. Lodha was the first person whom the senior editor has met with when a proposal for the book was being made. He stood by us during this entire process. We greatly value their mentorship and sincerely acknowledge their support and encouragement. We would like to express our sincere gratitude to the contributing authors whose research works and years of experience working with PGPM have played a very significant role in enriching the content of the publication. Thanks and appreciations also to our colleagues in developing the book and people who have willingly helped us out with their abilities. We extend our sincere gratitude to Team Springer for reposing their faith in us as an Editorial team and entrusted us with this task of spreading PGPM research output across the wider scientific community. We thankfully acknowledge our families and friends for the encouragement and motivational support rendered by them.

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Acknowledgments

Finally, thanks to everyone who have been a part of this book directly or indirectly and made us realize this objective of bringing out research on contribution of PGPM with particular emphasis on dry and arid ecosystems. Ritu Mawar R Z Sayyed Sushil K Sharma Krishna Sundari Sattiraju

Contents

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Exploring Microbial Diversity of Arid Regions of Globe for Agricultural Sustainability: A Revisit . . . . . . . . . . . . . . . . . . . . . . . Ritu Mawar, Madhavi Ranawat, Sushil K Sharma, and R Z Sayyed

1

Harnessing Drought-Tolerant PGPM in Arid Agroecosystem for Plant Disease Management and Soil Amelioration . . . . . . . . . . . Ritu Mawar, Madhavi Ranawat, Ladhu Ram, and R Z Sayyed

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Role of Plant Growth-Promoting Bacteria in Rainfed and Irrigated Crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pratibha Vyas, Amrita Kumari Rana, and R. C. Kasana

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Plant Growth-Promoting Microbes: The Potential Phosphorus Solubilizers in Soils of Arid Agro-Ecosystem . . . . . . . . . . . . . . . . . . R. S. Yadav, M. Kumar, P. Santra, H. M. Meena, and H. N. Meena

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Diversity of PGPM and Ecosystem Services . . . . . . . . . . . . . . . . . . Lalit Mahatma, Jitendar Kumar Sharma, Harshal P. Patel, Nitin M. Patel, and Rupal P. Patel

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Plant Growth-Promoting Microorganisms: An Option for Drought and Salinity Management in Arid Agriculture . . . . . . . 125 Kamlesh K. Meena, Utkarsh M. Bitla, Ajay M. Sorty, M. Saritha, Shrvan Kumar, and Praveen Kumar

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Plant Growth-Promoting Microbes: Key Players in Organic Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139 Ekta Narwal, Jairam Choudhary, N. K. Jat, Amrit Lal Meena, P. C. Ghasal, Debashis Dutta, R. P. Mishra, M. Saritha, L. K. Meena, Chandra Bhanu, Raghuveer Singh, G. Chethan Kumar, A. S. Panwar, and Mahipal Choudhary

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Interceding Microbial Biofertilizers in Agroforestry System for Enhancing Productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 Sangeeta Singh, Tanmaya Kumar Bhoi, and Vipula Vyas

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Role of PGPM in Managing Soil-Borne Plant Pathogens in Horticulture Crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185 S. K. Maheshwari, D. G. S. Ramyashree, Anita Meena, Ritu Mawar, and D. L. Yadav

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The Use of Plant Growth Promoting Microorganisms in the Management of Soil-Borne Plant Pathogenic Organisms . . . . . . . . . 195 Ayodele Martins Ajayi and David Babatunde Olufolaji

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Role of Plant Growth Promoting Microbes in Managing Soil-Borne Pathogens in Forestry . . . . . . . . . . . . . . . . . . . . . . . . . . 213 Abdul Gafur, Rabia Naz, Asia Nosheen, and R Z Sayyed

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Secondary Metabolites and Bioprospecting . . . . . . . . . . . . . . . . . . . 229 Megha Sharma, Richa Bhardwaj, Mukesh Saran, Rakesh Kumar Prajapat, Deepak Sharma, and Manas Mathur

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PGPM: Fundamental, Bioformulation, Commercialization, and Success at Farmer’s Field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 Manjunath Hubballi, S. Rajamanickam, Ritu Mawar, Reshma Tuladhar, Anjana Singh, R Z Sayyed, and S. Nakkeeran

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PGPR: A Sustainable Agricultural Mitigator for Stressed Agro-Environments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303 Priyanka Patel, R Z Sayyed, and Hardik Patel

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Endophytic PGPM-Derived Metabolites and their Role in Arid Ecosystem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 319 R. Srinivasan, Sonu Kumar Mahawer, Mahendra Prasad, G. Prabhu, Mukesh Choudhary, M. Kumar, and Ritu Mawar

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Current Regulatory Requirements for PGPM Products for Management of Seed, Soil and Plant Health: An Overview . . . . . . . 349 Ritu Mawar, B. L. Manjunatha, Archana Sanyal, Sushil K Sharma, H. B. Singh, and S. C. Dubey

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Evolving Concepts of Biocontrol of Phytopathogens by Endophytic Pseudomonas Fluorescence . . . . . . . . . . . . . . . . . . . 365 P. Saranraj, R Z Sayyed, M. Kokila, V. Salomi, P. Sivasakthivelan, M. Manigandan, and Ritu Mawar

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Symbiotic Effectiveness of Rhizobium Strains in Agriculture . . . . . . 389 P. Saranraj, R Z Sayyed, P. Sivasakthivelan, M. Kokila, Abdel Rahman Mohammad Al-Tawaha, K. Amala, and Humaira Yasmin

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Inoculant Production and Formulation of Azospirillum Species . . . . 423 P. Sivasakthivelan, P. Saranraj, R Z Sayyed, K. Arivukkarasu, M. Kokila, M. Manigandan, and Sonia Seifi

Editors and Contributors

About the Editors Ritu Mawar is a Principal Scientist (Plant Pathology) at the ICAR-Central Arid Zone Research Institute (CAZRI), Jodhpur, India. She worked in management of soil-borne plant pathogens such as Macrophomina phaseolina, Fusarium, and Ganoderma by soil solarization, use of cruciferous residues, composts, biological control, etc. She has received Best Women Scientist Fellowship from DST and Indian Society of Mycology and Plant Pathology, and Indian Patents. She has published more than 75 research papers, book chapters, and popular articles in high-impact journals, success story of management of Ganoderma in ICAR Newsletter, and has authored four books. She has presented her research at various international platforms in the county and abroad and has received a number of best presentation awards. She served as peer reviewer of foreign research journals and DST-funded projects, and External Examiner for Ph.D. thesis and viva voce of many academic universities. She is a Life Member of Indian Phytopathological Society, Range Management Society, Arid Zone Research Association, Indian Society of Mycology and Plant Pathology, and Asian PGPR Society for Sustainable Agriculture and its Advisory Board Member. She is an executive member of the editorial board of Journal of Rainfed Farming and Indian Phytopathological Society newsletter. She is serving as a Zonal President (CZ) of Indian Phytopathological Society, IARI, New Delhi, and Zonal Councillor (NWZ) and executive member of Range Management Society of xv

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India for 2022–2024. She developed three bio-formulated products from native strains of bioagents viz., Trichoderma harzianum and Bacillus firmus. She received two patents on novel microbes in 2019 as Bioformulation of a biopesticide and a process for preparing the same and “Consortium of biopesticides and bioformulation comprising same.” State POP was developed for managing soil-borne plant pathogens. Techniques were developed to rejuvenate Prosopis cineraria (Khejri) from Ganoderma species. IPM technologies were developed for arid legumes, oil seed, and cumin crops.

R Z Sayyed is a Professor and Head, Department of Microbiology, PSGVP Mandal’s Arts, Science College, Shahada, India. Currently, he serves as the President of the India chapter of the Asian PGPR Society for Sustainable Agriculture (Estd 2019). To his credit, he has received the Best Teachers Award, Young Scientist Award (2005, 2008, and 2012), Prof M. M. Sharma Award, Springer-Society Award (2020), and Award for Excellence in PGPR Research (2017, 2018, and 2019). He is Associate Editor of Environmental Sustainability (Springer) and Guest editor of two special issues of Sustainability (MDPI, IF 3.251). He has over 25 years of teaching and 20 years of research experience in Microbiology and Biotechnology. He has authored and coauthored over 200 research papers in high IF international journal, 24 books with Springer, Wiley, CRC, and Cambridge press, and 43 book chapters in reputed edited books. He has trained several graduates, postgraduate, and research students and produced seven Ph.D.s under his guidance. He has delivered many invited talks at several Southeast Asian and European countries.

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Sushil K Sharma is a Principal Scientist at ICARNIBSM, Raipur, India. He works in the area of microbial resource conservation and antimicrobial peptides production by bacteria for biotic stress management in crops. He has served as officer in-charge at ICARNational Bureau of Agriculturally Important Microorganisms (NBAIM), Maunath Bhanjan, Uttar Pradesh, India. He has long experience on Soybean Research. He has delivered talks in various international conferences in the country and abroad. He has published more than 100 research articles in internationally recognized and good impact journals. His team has developed (1) a simple novel method for the detection of operation of tryptophan-independent pathway in Micrococcus aloeverae DCB-20 and (2) a low-cost preservation method of Chromobacterium violaceum using natural gums at room temperature. He received the Best Scientist award by PEARL Foundation, Madurai, India, and Excellence in PGPR Research award by Asian PGPR Society. Recently, he has been nominated as a member of Biosafety and Biosecurity Cell (B2Cell) of Indian Council of Medical Research (ICMR), New Delhi.

Krishna Sundari Sattiraju presently serves as Professor in the Department of Biotechnology at JIIT, Noida. She has 20 years of academic and research experience, working at places of national and international repute such as TERI (The Energy and Resources Institute), New Delhi; Institute Nationale Recherche Agronomie (INRA), Champenoux, France; and brief work assignments at ENSAIA, France, Universitae Henrie Poincare, France, and University of Florida, Gainesville, USA. The educational institutes where she worked earlier include Institute of Applied Medicines and Research (IAMR), Ghaziabad, Institute of Home Economics (IHE), New Delhi, Jamia Milia Islamia, New Delhi, and TERI–SAS, New Delhi. She harbors research interest in the area of Microbial Biotechnology with applications for Agriculture, Environment, and Industry. She has successfully taken up projects worth more than 2 crores funded by DBT, Govt. of India. She has published nearly 25 papers in international refereed journals and has more than 50 conference

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papers and book chapters. Prof. Krishna holds membership in various international scientific societies and presently serving as Exec. Vice President for Asian PGPR Society, Auburn, USA.

Contributors Ayodele Martins Ajayi Department of Crop, Soil and Pest Management, The Federal University of Technology, Akure, Ondo State, Nigeria Abdel Rahman Mohammad Al-Tawaha Department of Biological Sciences, AlHussein Bin Talal University, Maan, Jordan K. Amala Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, Tamil Nadu, India K. Arivukkarasu Department of Agronomy, Faculty of Agriculture, Annamalai University, Annamalai Nagar, Tamil Nadu, India Chandra Bhanu ICAR-Directorate of Rapeseed Mustard Research, Bharatpur, India Richa Bhardwaj Department of Botany, IIS University, Jaipur, Rajasthan, India Tanmaya Kumar Bhoi Arid Forest Research Institute, Jodhpur, India Utkarsh M. Bitla ICAR-National Institute of Abiotic Stress Management, Baramati, India Jairam Choudhary ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India Mahipal Choudhary ICAR-Central Arid Zone Research Institute, Jodhpur, India Mukesh Choudhary ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India S. C. Dubey Indian Council of Agricultural Research, New Delhi, India Debashis Dutta ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India Abdul Gafur Sinarmas Forestry Corporate Research and Development, Perawang, Indonesia P. C. Ghasal ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India Manjunath Hubballi University of Horticultural Sciences, Bagalkot, India N. K. Jat ICAR-Central Arid Zone Research Institute, Jodhpur, India

Editors and Contributors

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R. C. Kasana ICAR-Central Institute of Post-Harvest Engineering and Technology, Ludhiana, Punjab, India M. Kokila Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, India G. Chethan Kumar ICAR-Indian Institute of Horticultural Research, Bengaluru, India M. Kumar ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, Mau Nath Bhanjan, India ICAR-Central Arid Zone Research Institute, Jodhpur, India Mahesh Kumar ICAR-Central Arid Zone Research Institute, Jodhpur, India Praveen Kumar ICAR-Central Arid Zone Research Institute, Jodhpur, India Shrvan Kumar ICAR-Central Arid Zone Research Institute, Jodhpur, India Lalit Mahatma Department of Plant Pathology, N.M. College of Agriculture, Navsari Agricultural University, Navsari, Gujarat, India Sonu Kumar Mahawer ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India S. K. Maheshwari ICAR-Central Institute for Arid Horticulture, Bikaner, India Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India M. Manigandan Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, India B. L. Manjunatha ICAR-Central Arid Zone Research Institute, Jodhpur, India Manas Mathur School of Agriculture, Suresh Gyan Vihar University, Jaipur, Rajasthan, India Ritu Mawar Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India Amrit Lal Meena ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India Anita Meena ICAR-Central Institute for Arid Horticulture, Bikaner, India H. M. Meena ICAR-Central Arid Zone Research Institute, Jodhpur, India H. N. Meena ICAR-Agricultural Technology Application and Research Institute, Jodhpur, India Kamlesh K. Meena ICAR-Central Arid Zone Research Institute, Jodhpur, India L. K. Meena ICAR-Directorate of Rapeseed Mustard Research, Bharatpur, India

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R. P. Mishra ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India S. Nakkeeran Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore, India Ekta Narwal Shobhit Institute of Engineering and Technology, Modipuram, Meerut, India Rabia Naz Department of Biosciences, COMSATS University, Islamabad, Pakistan Asia Nosheen Department of Biosciences, COMSATS University, Islamabad, Pakistan David Babatunde Olufolaji Department of Crop, Soil and Pest Management, The Federal University of Technology, Akure, Ondo State, Nigeria A. S. Panwar ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India Hardik Patel Government Dental College and Hospital, Civil Hospital Campus, Ahmedabad, India Harshal P. Patel Pulses and Castor Research Station, Navsari Agricultural University, Navsari, Gujarat, India Nitin M. Patel Department of Horticulture, N. M. College of Agriculture, Navsari Agricultural University, Navsari, Gujarat, India Priyanka Patel Department of Microbiology and Biotechnology, University School of Sciences, Gujarat University, Ahmedabad, India Rupal P. Patel Department of Plant Pathology, N. M. College of Agriculture, Navsari Agricultural University, Navsari, Gujarat, India G. Prabhu ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India Rakesh Kumar Prajapat School of Agriculture, Suresh Gyan Vihar University, Jaipur, India Mahendra Prasad ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India S. Rajamanickam Tamil Nadu Agricultural University, Coimbatore, India Ladhu Ram College of Horticulture and Forestry, Jhalawar, Rajasthan, India D. G. S. Ramyashree ICAR-Central Institute for Arid Horticulture, Bikaner, India Amrita Kumari Rana Department of Microbiology, College of Basic Sciences and Humanities, Punjab Agricultural University, Ludhiana, Punjab, India

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Madhavi Ranawat Division of Plant Imp and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India V. Salomi Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, India P. Santra ICAR-Central Arid Zone Research Institute, Jodhpur, India Archana Sanyal ICAR-Central Arid Zone Research Institute, Jodhpur, India Mukesh Saran Department of Physics, Manipal University Jaipur, Jaipur, India P. Saranraj Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, India M. Saritha ICAR-Central Arid Zone Research Institute, Jodhpur, India M. Saritha ICAR-Central Arid Zone Research Institute, Jodhpur, India R Z Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India Division of Plant Imp and Pest Management, Central Arid Zone Research Institute, Jodhpur, India Sonia Seifi Department of Agriculture, Payame Noor University (PNU), Tehran, Iran Deepak Sharma School of Agriculture, Jaipur National University, Jaipur, Rajasthan, India Jitendar Kumar Sharma Agriculture Research Sub-station (Agriculture University, Jodhpur), Sumerpur, Pali, Rajasthan, India Megha Sharma Laboratory of Plant Pathology and Biochemistry, Department of Botany, University of Rajasthan, Jaipur, India Sushil K Sharma ICAR-National Institute of Biotic Stress Management, Raipur, Chhattisgarh, India Anjana Singh Central Department of Microbiology, Tribhuvan University, Kathmandu, Nepal H. B. Singh GLA University, Mathura, India Raghuveer Singh ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India Sangeeta Singh Arid Forest Research Institute, Jodhpur, India P. Sivasakthivelan Department of Agricultural Microbiology, Faculty of Agriculture, Annamalai University, Annamalai Nagar, Tamil Nadu, India

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Ajay M. Sorty ICAR-National Institute of Abiotic Stress Management, Baramati, India R. Srinivasan ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India Reshma Tuladhar Central Department of Microbiology, Tribhuvan University, Kathmandu, Nepal Pratibha Vyas Department of Microbiology, College of Basic Sciences and Humanities, Punjab Agricultural University, Ludhiana, Punjab, India Vipula Vyas Arid Forest Research Institute, Jodhpur, India D. L. Yadav Kota Agricultural University, Kota, India R. S. Yadav ICAR-Central Arid Zone Research Institute, Jodhpur, India Humaira Yasmin Department of Biosciences, COMSAT University, Islamabad, Pakistan

Chapter 1

Exploring Microbial Diversity of Arid Regions of Globe for Agricultural Sustainability: A Revisit Ritu Mawar, Madhavi Ranawat, Sushil K Sharma, and R Z Sayyed

1 Introduction Environmental pollutions, climate changes, emergence of deadly microbial variants, scarcity of water, and food resources are the global issues of twenty-first century’s world. Among the concerning issues, increasing world’s population leading reduction in land available for cultivation is the biggest hurdle agriculture sustainability is in face with (Shahbaz and Ashraf 2013). A vast area of planet’s land is covered by desert ecoregions which account for more than 46 million square kilometers of available land (Osborne et al. 2020). Exploring available arid land for cultivation can open various new avenues to tackle with these issues. Cultivation in dry arid zones of world is not as easy as it sounds. Brutality of environment in such land challenges the idea of successful cultivation; yet several efforts have been made to establish cultivation in unexplored arid lands. Utilizing beneficial microorganisms with exceptional potentials to not only tolerate or withstand but also thrive in extremities imposed by desert environment can aid agriculture sustainability in such land. By exploring their unique potentials, genetic diversity, biocontrol abilities, plant growth-promoting capacities, and other tendencies idea to successfully sustain agriculture in desert land can come into reality (Fig. 1.1). This chapter explores microbial diversity found in desert across of globe and provides insight to their utilization in agricultural sustainability.

R. Mawar (*) · M. Ranawat Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India S. K. Sharma National Institute of Biotic Stress Management, Raipur, India R. Z. Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_1

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Fig. 1.1 Microbes in desert ecosystems for agri-sustainability

Deserts are significant part of world’s natural and cultural heritage covering one-third of planet’s surface. Deserts are home for nearly 2.1 billion people and to diverse flora, fauna, and microbial species that are unique to dry ecosystems in terms of adaptations. Deserts have been defined in several ways—biologically, they are ecoregions with well-adapted life forms; physically, they are areas with low vegetative cover and extensions of bare soils, and climatologically, they are all the arid and semiarid regions of globe. Deserts play an important role in global ecology and environment and are significant migratory corridor for several species, trade corridors, and exporters of unique agricultural and other goods to nondesert areas (Osborne et al. 2020; United Nations Environment Programme 2006). Around 33% land is actually converted into deserts, and rest is in the process of desertification. Desert ecoregions have been addressed as dry/arid land(s) or zone(s) (Laity 2009). Deserts have been classified into three different zones around the world based on Aridity Index (AI) and are hyperarid zones, semiarid zones, and arid zones (Cherlet et al. 2018; Alsharif et al. 2020). Life thrive there endure climatic conditions imposed by environment including extreme and abrupt temperature fluctuations, high soil salinity, wind velocity, radiations and scarcity of water, nutrient and organic matter. Several other abiotic and biotic factors like soil pH, composition, depth, texture, conductivity, nutrient cycling, precipitation rate and composition, diversity, and shape of functional group of communities affect and contribute to desert ecosystem at varying degree. The desert land is essentially barren with limited number of biological communities and probably dominated with microbial coteries contributing to key desert ecosystem processes. Environmental factors play key role in shaping desert microbial communities, and findings suggest that deterministic factors favor bacterial communities over any other in deserts (Wang et al. 2013).

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Desert microbes not always provide beneficial services, but some of the communities are notorious for very long time for their pathogenic potentials. Several soilinhibiting microbes including bacteria, fungi, nematodes, and actinomycetes are known to cause serious diseases in plants worldwide. On the other side, several microbial consortia exhibit beneficial relationships with plants. Microbes are not only economic but also the most reliable option available since excessive use of chemical-based strategy has negative impact on agro-ecosystems. Chemicals also contribute to global pollution, climate change, and plant pathogens evolving to compete with them for developing resistance are debatable issues for the continuation of utilization for agri-sustainability. The collection of concerning disadvantages offered by other conventional physical and chemical approaches has necessitated the development of novel eco-friendly, durable, and cost-effective strategies that aid crop performance and productivity, as well as control loss caused by plant pathogens. Exploring microbial services in dry and arid terrains may provide us with rightful directions for agriculture sustainability. Exploring microbial communities in natural ecosystems is difficult task indeed, and vast diversity of microbes is critical and challenging factor in their characterization (Torsvik et al. 1998). Traditional culture-dependent methods are easy and inexpensive but only provide information for minor fraction of microbes than of total microbes present in environment. Similarly, the biochemical and chemotaxonomic methods are fast and sensitive but again applicable on restricted fraction of communities. Recent advantages in molecular approaches have provided us with novel culture-independent tools which are based on nucleic acid analysis, including gene coding, fingerprinting, probing, and sequencing (Kirk et al. 2004; Fakruddin and Mannan 2013). Molecular genetic tool provides information about community structure, diversity, and phylogeny and is applicable for vast range of communities without restrictions. Technical demands, error-prone approaches, misleading interpretations, and high cost are disadvantages associated with new molecular strategies for microbial characterizations and still have space for regular improvisation. Combining different complementary molecular strategies is adventitious in monitoring microbial communities in natural ecosystems than individual approaches (Kirk et al. 2004; Fakruddin and Mannan 2013). More recent advancement has expanded our abilities to characterize globe-scale microbiomes with next-generation sequencing technologies and motivated initiatives like Earth Microbiome Project (Thompson et al. 2017). Several individual maneuvers solicit to describe and compare soil microbial communities in arid environment (McHugh et al. 2017; Mandakovic et al. 2018). A variety of data have been piled up but systematic collective records targeting arid zones microbial communities have not been accomplished yet and regarding their services aiding agriculture sustainability is recent emerging subject under research concerns. Environmental microbiologist exploring metagenomes will be a ‘collective nucleic acids from natural sites including of nonviable communities’ have privileged ongoing research to explore microbes with benefits in different ecosystems. Microbial symbionts are getting appreciations for their critical roles in health of plant hosts, and studies targeting their interactions and coevolution have encapsulated specific terms like “holobiont” and “hologenome” (Moran and Sloan

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2015). Host plant with all its associated microbial communities is referred as holobiont (Rohwer et al. 2002), and genetic composition of a holobiont, i.e., collectively of host and its microbial residents, is termed as hologenome (Bordenstein and Theis 2015). A variety of metagenome studies in arid soils have been conducted with conclusion that desert soil encompasses lower functional diversity of microbes than nondesert soil. Further metagenomic studies revealed that the harshness imposed by environment is in linear relation with adaptability in communities; i.e., greater the cruelty, better the adaptive weapons (Fierer et al. 2012).

2 Adaptive Strategies of Dryland Flora Lives in desert have different weapons to fight battle against atrocities of environment. With great history of evolution of plant, animals and microbes of desert lands have advanced their adaptive mechanisms and established uncountable lineages even in the extreme of desert edges. Still the harshness limits the diversity of communities and vegetation to mostly shrubs, grasses, or trees with moisture retention capabilities or short life cycles (Monson 2014). Wide range of morphological, physiological, and genetic adaptations have been seen and studied in desert flora. To cope with high radiation, temperature, and water scarcity, popular adaptations among desert plants are reduced leaf or plant size, vertical leaf orientation, leaf reflectance (Gibson 1996), thick wax layer (Holmes and Keiller 2002), accumulation and production of phenolics as UV-absorbing sunscreens and solutes to maintain tissue turgor (Caldwell et al. 1998; Julkunen-Tiitto et al. 2015), high transpiration rate and tissue elasticity (Smith et al. 1997), photorespiration, Crassulacean acid metabolism (Batanouny 2001; Ludwig 2012; Greenville 2018), high levels of heat shock proteins (Al-Whaibi and Mohamed 2011; Zhu et al. 2018), antioxidative enzymes like superoxide dismutase, catalase, and ascorbate peroxidase to scavenge reactive oxygen species, plant growth and stress hormones including auxin, cytokinin, abscisic acid, jasmonic acid, salicylic acid, and strigolactones (Munns and Tester 2008; Deinlein et al. 2014; Evelin et al. 2019), low xylem hydraulic conductance, extended seed viability, seed dormancy (Smith et al. 1997; Norton et al. 2016), long profuse, and deep fibrous roots (Smith et al. 1997). In addition to these, plant–microbe interactions as adaptation to dry stresses are common among desert flora and have been studied in detail to understand mechanisms of such interactions. Plants interact with microbial communities colonizing and inhabiting in surrounding soil by forming plant rhizosheaths, i.e., soil aggregates firmly attached to root surface (Brown et al. 2017; Pang et al. 2017). Formation of rhizosheath has been correlated with increase number and length of root hair and thus provides drought tolerance and with enhanced nutrient uptake (Delhaize et al. 2012; James et al. 2016; Pang et al. 2017 Khan et al. 2020; Najafi et al. 2021; Kour and Sayyed 2019). Plant rhizosheaths are ideal niche for several nitrogen-fixing and plant growth-promoting bacteria (Othman et al. 2004; Tahir et al. 2015). Besides

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superficial interactions on root surface, i.e., in rhizoplane and in the zones around the roots (rhizosphere and rhizosheath), plants internally accommodate microbial communities in phyllosphere, i.e., aerial parts of plant and endosphere, i.e., inside of plant. Different factors involved in recruitment, selection, enrichment, and dynamic interactions between plant and associated microbes are location and climatic factors; host plant-dependent factors that include host genotype, selection of communities based on host immunity and defense abilities and diversity of compounds secreted by host to attract microbial communities and finally soil properties, i.e., its nature, composition, conductivity, pH, and moisture (Saad et al. 2020). Microbial communities inhabiting in rich niche provided by desert plants as rhizosphere, rhizosheath, endosphere, and phyllosphere are unexploited reservoir for biofertilizers and biocontrol agents that enhance plant health, increase plant tolerance to variety of biotic and abiotic stresses, and enhance crop productivity in eco-friendly way (Alsharif et al. 2020). Groups of beneficial soil microbes are being called as plant growthpromoting microorganisms (PGPM) that are capable of alleviating plant immunity and growth through indirect means via inducing plant defense against phytopathogens or directly promote growth by nutrient solubilization, by assimilation, by modulating phytohormones, and by secreting specific solutes and enzymes (Ma et al. 2016). Some common PGPM and their specific mechanism through which they promote plant health are listed in Table 1.1.

2.1 2.1.1

Structure of Desert Microcommunities Bacterial Communities

Desert biomes have been inspected by researchers to understand diversity, distribution, composition, and functions of soil microbial communities. Frequently reported bacterial phyla in desert soil across the globe include Proteobacteria, Actinobacteria, and Bacteroidetes (Chanal et al. 2006; Connon et al. 2007; Lester et al. 2007; Fierer et al. 2009). An effort with bacterial communities in rhizosphere of widely distributed perennial shrub Caragana in arid and semiarid regions of north China revealed dominance of bacterial phyla including Proteobacteria, Gemmatimonadetes, Firmicutes, Actinobacteria, Bacteroidetes, Acidobacteria, and Cyanobacteria, where on genus-level abundance of Pseudomonas, Acinetobacter, Bacillus, Stenotrophomonas, Burkholderia, Paenibacillus, Sphingobacterium, Chitinophaga, Arthrobacter, and Chryseobacterium reported (Na et al. 2018). Proteobacteria prosper well in nutrient-deficient arid soil by performing bacteriochlorophyll-dependent photosynthesis and are most prominent in desert soil. Data retrieved through 16S rRNA gene amplicon pyrosequencing have suggested almost twice abundance of Proteobacteria in desert soil than that of in agriculture soil type, with richness of genus Ochrobactrum, a kind of Alphaproteobacteria (Köberl et al. 2011). A Proteobacteria isolated from Gobi Desert reported to horizontally transfer their photosynthetic ability to other phyla

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Table 1.1 Plant growth-promoting microorganisms and their mechanism of action Plant growth-promoting microorganism (PGPM) Nutrient assimilation Azospirillum, Azotobacter, Achromobacter, Bradyrhizobium, Beijerinckia, Rhizobium, Clostridium, Klebsiella, Anabaena, Nostoc, Frankia Bacillus, Pseudomonas, Rhizobium, Achromobacter, Burkholderia, Micrococcus, Agrobacterium, Erwinia sp., Penicillium sp., and Aspergillus sp.

Burkholderia, Enterobacter, Grimontella, and Pseudomonas

Bacillus and Aspergillus

Rhizophagus irregularis and Funneliformis mosseae

Phytohormone production Pseudomonas sp. and Bacillus

Sphingomonas SaMR12, Phyllobacterium myrsinacearum RC6b Exopolysaccharide secretion Bacillus spp. Proteus penneri, P. aeruginosa, and Alcaligenes faecalis Osmoregulants Burkholderia sp.

Growth promotion mechanism

References

Nitrogen fixation: through reduction of nitrogen gas (N2) to ammonia (NH3)

Souza et al. (2015), Bhat et al. (2019)

Phosphate solubilization: transformation and solubilization of inorganic phosphorus into forms capable of being absorbed by plants, such as monobasic (H2PO - 4H2PO4-) or dibasic phosphate (HPO4-2) Siderophore production: improves plant nutrition and inhibits phytopathogens through iron sequestration from the environment. Potassium solubilization: produces organic and inorganic acids, acidolysis, chelation, and exchange reactions which are capable of solubilizing potassium Phytoextraction and stabilization: fungi that extract Cd and enhanced phytostabilization of Cd and Zn, respectively.

Martínez-Viveros et al. (2010)

Auxin secretion: promote plant growth by increasing auxin and ACC (amino-cyclopropane carboxylate) deaminase IAA: indole acetic acid production and root promotion

Samaddar et al. (2019), Danish et al. (2020), Khoshru et al. (2020) Chen et al. (2014), Ma et al. (2013)

Exopolysaccharides: forms a protective biofilm on root surface Exopolysaccharides: Alleviate water stress and improve plant biomass under drought stress

Hashem et al. (2019)

Metabolism: Increases plant tolerance against low temperature by modifying carbohydrate metabolism

Fernandez et al. (2012)

Souza et al. (2015), Varma et al. (2019)

Varma et al. (2019)

Hassan et al. (2013)

Naseem and Bano (2014)

(continued)

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Table 1.1 (continued) Plant growth-promoting microorganism (PGPM) Pseudomonas fluorescens

Growth promotion mechanism Osmoprotectants solutes and enzymes: promote plant tolerance by increasing the activity of catalase and peroxidase and the accumulation of proline

References Saravanakumar et al. (2011)

like Gemmatimonadetes. Gemmatimonadetes are among other most common desert bacterial phyla including Firmicutes and Cyanobacteria (Makhalanyane et al. 2015). Abundance of Gemmatimonadetes in desert soil has been found interlinked with low moisture content of arid soil, i.e., around Pearson coefficient (r) of 0.409. Not much regarding their physiology and ecology is known, and only six isolates of arid soil Gemmatimonadetes are known till date. Firmicutes are among most frequently isolated microbes from arid soil with extraordinary adaptive mechanisms such as rapid spore germination, nonfastidious growth patterns, and rapid doubling frequencies other than these Firmicutes spp. including Bacillus, Paenibacillus, and others which are known to form endospores to cope with dryness of desert environment. A 16 S rRNA gene pyrosequencing data reported more than 30% members of Firmicutes, majorly of class Clostridia dominating among Antarctic vascular plant’s rhizospheric bacterial communities suggesting their significance in arid zones (Teixeira et al. 2010). Members of Actinobacteria are common in desert soil and withstand extremities of desert habitats and mainly attribute to their capacity of sporulation, greater degradative tendency, wider metabolic range, and other competitive advantages including synthesis of secondary metabolites and error resisting or repairing mechanisms against effect of UV radiations (Ensign 1978; McCarthy and Williams 1992; Chater and Chandra 2006; Gao and Garcia-Pichel 2011). Wide spectrum of Actinobacteria has been recovered from extreme ecosystems and such includes acid-tolerant, alkaliphilic, psychrotolerant, thermotolerant, halotolerant, alkalitolerant, halo-alkalitolerant, and xerophilous Actinobacteria (Lubsanova et al. 2014). A report from Atacama desert suggested 72–88% dominance of members of Actinobacteria in desert soil, while in other arid regions they are among three most abundant arid bacterial phyla besides Firmicutes and Proteobacteria (Crits-Christoph et al. 2013; Mohammadipanah and Wink 2016). Members from phylum Bacteroidetes were unexpectedly common in desert soil for their known copiotrophic members, but then obviously not all members of phylum can only belong to same ecological category (Fierer et al. 2007). Desert soil from the Taklamakan Desert (China) found rich with Pontibacter spp. of family Cytophagaceae which is first of kind form this genus to have nitrogen fixation capability mediated through nifH gene (Xu et al. 2014). Various isolates from this phylum have shown their optimum growth at high pH supporting their habitation in alkaline character of desert soil (Lauber et al. 2009). Acidobacteria are underrepresented soil microbes distributed in almost all ecosystems and contribute

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dynamically in vital ecological processes including regulation of biogeochemical cycles, decomposition of biopolymers, and as plant growth promoters (Kalam et al. 2020). A deep diversity analysis of bacterial communities in unvegetated arid soils of the Atacama Desert reported presence of Acidobacteria along with Proteobacteria and Actinobacteria (Neilson et al. 2012). Cyanobacteria are well-known photosynthetic taxa with exceptional adaptations to desert desiccations, salt stresses, and high radiations and are functional participants in desert biogeochemical cycling processes (Chan et al. 2013). They contribute to soil nutrient profile by enhancing soil fertility through nitrogen fixation and stabilize soil by retaining moisture (Belnap and Gardner 1993). Accumulations of osmoprotectants like trehalose, sucrose, and glucosyglycerol; synthesis of UV screening lower reactive oxygen species; efficient repair mechanisms and moisture-induced chemotactic ability to migrate for survival of cynobacteria against desert stresses (Garcia-Pichel and Pringault 2001; Singh et al. 2002; Sorrels et al. 2009).

2.1.2

Fungal Communities

Arid zones have been found populated with greater diversity of fungi emphasizing their versatility as one of the most stress-tolerant life form on earth (Waller et al. 2005; Sterflinger et al. 2012). Fungi are economically versatile microbes of desert ecosystems and are crucial deciding factor for plant-associated soil microbial communities (Oren and Steinberger 2008). Evidently, it has been reported that without specific physiological adaptations fungi survive the extreme environment through spore-forming abilities and are belonging to heterogeneous group of saprophytes, parasites, pathogen, and symbionts or endophytes (Gadd 2007; Sterflinger et al. 2012). Various fungal groups including yeast, filamentous, terricolous, microcolonial, and mycorrhizal have been reported from dry soils (Sterflinger et al. 2012). Soil studies from Negev and Sonoran deserts reported high taxonomic diversity of both Basidiomycota and Ascomycota (Ranzoni 1968; Taylor-George et al. 1983). A study conducted to collect information on biodiversity of fungi in hot and dry regions through culture-independent next-generation sequencing of 18S rRNA genes along with traditional culture-dependent methods reported fungal occurrence range from 3.5% to 82.7% in different soil sample from Saudi Arabia and Jordan deserts. Similar to former report, this also suggested greater abundance of Ascomycota and Basidiomycota phyla in deserts and major fungal classes were Dothideomycetes, Pezizomycetes, and Sordariomycetes (Murgia et al. 2019). Fungal groups like mutualistic arbuscular mycorrhiza (AM) are significant plant root symbionts in desert ecosystems and known to provide resistance toward drought stresses through penetrating deep soil pores for water accessibility. A molecular assessment of AM fungi from six different desert areas, viz. northwestern Argentina, central Australia, southern Israel, southeastern Kazakhstan, central Saudi Arabia, and the southwestern USA, reported most common AM family Glomeraceae from different desert soils and other less frequently found families,

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Claroideoglomeraceae, Diversisporaceae, and Acaulosporaceae (Vasar et al. 2021). The report further emphasized on potentials of AM fungi in ecosystem restoration.

2.1.3

Archaeal Communities

Archaeal members are known for their resilience toward environmental stresses and extreme conditions of energy starvations (Maupin-Furlow et al. 2012). The communities are rare in usual biomes but extremes, including arid provinces. Principal desert archaeal phylotypes are chemolithoautotrophs and play significant roles in biogeochemical cycling processes. A common representative of dessert archaeal communities was found Thaumarchaeota (Brochier-Armanet et al. 2008). Arid microbial studies have revealed dominance of euryarchaeal Halobacteria from the orders Halobacteriales, Haloferacales, and Natrialbales and about 40% yet uncharacterized and unclassified members of community. Further potentially novel genera Halorubrum and Haloparvum were isolated (Bachran et al. 2019). Principal archaeal representative isolated from Tataouine Desert was Crenarchaeota (Chanal et al. 2006). Available data on arid archaeal dwellers are limited and advocate the need of explorations and evaluations.

2.1.4

Viral Communities

Desert ecosystems are known to driven by microbial communities and viruses are among most prevalent entities of such microbially driven systems with significant ecological roles; however been rarely evaluated. Pioneer studies on viruses in such ecosystems reveal higher diversity than expected and found high number of phagelike morphotypes that include Myoviridae, Siphoviridae, and Podoviridae, three major families of tailed phages. Namib Desert hypolith phylotypic survey reported most prevalent bacteriophages belonging to the order Caudovirales, in particular the family Siphoviridae (Adriaenssens et al. 2015). Exploration of cold Antarctic soil revealed combinatorial driving factors, such as soil factors, pH, calcium content, and site altitude. Besides they claim abundance of viral families including Myoviridae and Siphoviridae and high diversity families like Phycodnaviridae and Mimiviridae (Adriaenssens et al. 2017). Comparative studies disclosed low extracellular virus counts in hyperarid desert soils contrasting higher extracellular virus titers in colds deserts. These studies encounter fewer identity values to virus genomes of concern in public databases evince occurrence of widely distinct or not so yet characterized phylotypes in hyperarid deserts and advocate for frequent metavirome analysis to populate available sequence databases (Zablocki et al. 2015). Limited or almost negligible information is available on plant–virus associations in arid ecosystems. Studies have yet only explored diversity, driving factor, and some of phylogenic data on viral communities of extreme ecosystems and their virulence being the major concerns. Plant–viral associations are still untouched

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subject and majorly due to their relative lower occurrence than other microbial communities and because of greater encounters with phage-like morphotypes than other types. Recent epidemiological research has identified several pathogenic plant infecting viral strains from some of common desert plants that include wilt and mosaic viruses affecting tomato, cucurbits, watermelons, and cultivation of significant crops (Brown et al. 2007; Adkins and Baker 2005).

3 Microbial Communities in Deserts Across the Globe So far, we have learned of desert biology with specific focus on microbial communities and plant microbial associations in general, and we know desert systems are microbially driven one for they cooperate with limited number of higher life forms. Further sections more specifically describe some major deserts across the globe and their microbial communities.

3.1

Deserts of South and North America

Deserts of North America are climatically divided into two groups as cold and warm deserts and spread over 1,277,000 square kilometers in USA and Mexico (MacMahon 1988). Chihuahuan Desert is largest hot desert of North America which occupies nearly 35,000 square kilometers and considered one among the most biologically diverse arid desert of the world (Schmidt Jr 1979; Hoyt 2002). A Mars analogue gypsum desert soils of the Cuatro Cie’negas Basin (CCB) from Chihuahuan Desert, Mexico was explored for bacterial communities and have reported phyla including – Actinobacteria, Acidobacteria, Bacteroidetes, Firmicutes, Gemmatimonadetes, Chloroflexi, Cyanobacteria, Alpha/Gammaproteobacteria and other nitrogen fixing communities (López-Lozano et al. 2012). Several entomopathogens isolated from Chihuahuan Desert include fungi, nematodes, rickettsia, and viruses—Beauveria bassiana, Entomophaga calopteni, Entomophthora muscae, Entomophthora planchoniana, Furia vomitoriae, Nomuraea rileyi, Metarhizium anisopliae var. anisopliae, Zoophthora radicans, Paecilomyces fumosoroseus, Paecilomyces farinosus, Nosema weiseri, Rickettsiella popilliae, and the nuclear polyhedrosis viruses (Sanchez-Peña 2000). Further, cactusassociated microbiome exploration reveals endo-/epi-seminal plant growthpromoting capabilities of bacterial groups such as Kluyvera, Bacillus, Paenibacillus, Stenotrophomonas, and fungal classes like Tremellomycetes, Dothideomycetes, Eurotiomycetes, Leotiomycetes, and Sordariomycetes colonizing four cactus species—Echinocactus platyacanthus, Ferocactus latispinus, Ferocactus pilosus, and Stenocereus queretaroensis (Mascot-Gómez et al. 2021). The second largest hot-arid desert of North America is the Sonoran Desert, which rambles over 320,000 square kilometers (Dimmitt et al. 2015). A study conducted to examine soil- and

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cactus-associated rhizosphere microbial communities of the Sonoran Desert based on pyrosequencing of the 16S rRNA gene has reported abundance of bacterial phyla—Proteobacteria, Actinobacteria, Planctomycetes, Firmicutes, Bacteroidetes, Chloroflexi, and Acidobacteria and abundant Archaea like Crenarchaeota of class Thermoprotei. Members of the phyla Euryarchaeota, Gemmatimonadetes, Nitrospira, Cyanobacteria, Thermomicrobi, and Verrucomicrobiae were also isolated (Andrew et al. 2012). Fungal genera like Alternaria, Ulocladium, Phoma, Fusarium, Acremonium, Embellisia, and Chaetomium have been found dominating in Chihuahuan and Sonoran deserts (Bates and Garcia-Pichel 2009; Bates et al. 2010). Another arid desert in North America is the Mojave Desert, characterized by spread of 7000 square mile (Dibblee 1967). Studies from biological soil crust have revealed distribution of major phyla including Cyanobacteria, Proteobacteria, and Chloroflexi with dominant genera like Phormidium in this desert (Mogul et al. 2017). Pioneer reports on arbuscular mycorrhizal (AM) colonization in the rhizosphere were formulated by Titus et al. (2002) which later confirmed through co-dominant shrub communities such as Larrea tridentata and Ambrosia dumosa in varying season; yet limited count, i.e., 0–0.2 spores per gram of soil, was confirmed (Apple et al. 2005). Besides the discussed geographical arid regions, remaining some cold deserts of North America include regions like Great Basin Desert, Columbia Plateau/Basin, Snack river Plain, and the Colorado Plateau. Phylogenetic studies of biocrusts from the Colorado Plateau revealed similar bacterial composition to that of the Sonoran Desert with most abundance of Cyanobacteria followed by Actinobacteria and Proteobacteria (Redfield et al. 2002; Nagy et al. 2005; Steven et al. 2015;). A further, dominant cyanobacterium from Colorado Plateau was found as Microcoleus vaginatus and from Sonoran was Microcoleus steenstrupii. Some diazotrophic genera like Nostoc, Scytonema, Tolypothrix, and Spirirestis also found common in from the Colorado Plateau (Yeager et al. 2007) and Chihuahuan Desert (Yeager et al. 2004). Among the South American deserts, the Atacama Desert, the oldest and nonpolar temperate desert on the Earth, covers around 1000 square kilometers and is characterized by hyperaridity, exceptionally high UV radiations, and low or zero soil carbon concentrations which make Atacama a prime example of extremobiosphere (Bull et al. 2018). Atacama, considered driest in world, has been explored for their microbial diversity, and one such study by high-throughput Illumina MiSeq sequencing approach to explore the composition, diversity, and functions of fungal and bacterial communities of the rhizosphere of native plants like Baccharis scandens and Solanum chilense has revealed dominance of fungal phyla like Ascomycota and Basidiomycota and the bacterial phyla like Actinobacteria and Proteobacteria. Further at genus level, Penicillium, Oidiodendron, Nitrospira, and Arthrobacter were among preferential genera (Fuentes et al. 2020). Similarly, a high-throughput sequencing revealed abundance of bacterial communities like Rubrobacterales, Actinomycetales, Acidimicrobiales, Thermoleophilia, and low abundance of Firmicutes (Crits-Christoph et al. 2013). Besides Atacama, the Argentinian Patagonia covers vast area of 790,000 square kilometers which is arid, semiarid, or dry-sub humid desert of southern South America (Gaitan et al. 2019).

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Through high-throughput sequencing, the presence of members of Actinomycetales, Solirubrobacterales, Pedosphaerales, and Rhizobiales has been recorded from arid region of Patagonia (Marcos et al. 2019). Additional studies explored air microflora such deserts and have reported fungi like Cladosporium as most abundant genus followed by Alternaria, Epicoccum, and Botrytis (Temperini et al. 2019).

3.2

Thar and Cold Deserts of India

The Great Indian or Thar Desert is vast, hot-arid tropical desert of Asia in the northwestern part of Indian subcontinent which expanded over 200,000 square kilometers through Rajasthan and Gujarat and occupies 18th position in the list of world’s deserts by area. A significant 61% of its landmass occupies western Rajasthan and is characterized by intense winds and wide variations in temperature ranging from a minimum of 5 °C to a maximum of 55 °C. Relatively smaller population of bacteria around 1.5 × 102–5 × 104 per gram soil has been reported from Thar sand dunes where desert soil predicted to constitute actinomycetes, approximately 50% of total microbial bacterial population (Sprent and Gehlot 2010; Bhatnagar and Bhatnagar 2005; Harwani 2013). Several Actinomycetes morphotypes have been screened from Thar soil and found positively correlated with soil nitrogen for their propagation (Fig. 1.1). A molecular approach based on 16S rRNA gene sequencing identified some important species of actinomycetes bacteria including genera Streptomyces, Nocardiopsis, Saccharomonospora, and Actinoalloteichus (Kumar et al. 2021). Besides, fungal communities also have been confirmed from Thar soil; identified novel Broomeia congregate Berk from family Broomeiaceae is Basidiomycetes (Gehlot et al. 2020) and studies targeting endophytic fungi have revealed dominance of Aspergillus, Alternaria, Chaetomium, Penicillium and Nigrospora. Further, thermotolerance of isolates was tested, and Aspergillus flavus and other Aspergillus sp., Chaetomium sp., come to tolerate 40–45 °C and even promoted higher root or shoot growth under drought and temperature stresses suggesting their usefulness in such environment (Ilyas et al. 2020; Jabborova et al. 2021; Sangamesh et al. 2018). Besides, dominance of Pseudomonas pseudoalcaligenes, Azospirillum brasilense, and Rhizobium sp. has been reported in association with roots of the drought-tolerant grass Lasiurus sindicus in the Thar Desert of Rajasthan, India (Chowdhury et al. 2009). The Thar microbiota also have been explored for potential biocontrol agents and biofertilizers with exceptional drought- and temperature-tolerant capabilities, and vigorous screening at Central Arid Zone Research Institute (CAZRI), Jodhpur, India, has been done from past two decades, and still exploring such microbes has identified and confirmed some bacterial and fungal communities that include Bacillus firmus, Bacillus tequilensis, Streptomyces mexicanus, Aspergillus versicolor, Aspergillus nidulans, Trichoderma harzianum, and Trichoderma longibrachiatum (Mawar et al. 2017, 2021a, b; Lodha and Mawar 2019).

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Cold dry Indian desert includes Leh Ladakh and other Himalaya regions which represent cold niche for adaptive microorganisms. Psychrophilic microbes and other cold-adapted organisms have been investigated for their exceptional potentials and distinct metabolism. Many such microbes are valuable source for pigments, cold active enzymes or solutes, and for variety of antifreeze compounds with significance in agriculture as inoculants and biocontrol agents in extreme habitats (Yadav et al. 2015). Psychrophilic species have been isolated from Indian Himalayas including Exiguobacterium indicum (Chaturvedi and Shivaji 2006), Paenibacillus glacialis (Kishore et al. 2010), Janthinobacterium lividum, Sphingobacterium antarcticus, Psychrobacter valli (Shivaji et al. 2011), and Alishewanella sp., Brevundimonas sp. (Sahay et al. 2013). Cold-adapted microbes have been identified to act as significant agricultural inoculants and biocontrol agents in crops growing at high altitudes under cold climate condition (Table 1.2).

3.3

Deserts of China

Spreading over 346,905 square kilometers in the hinterland of the Tarim Basin in northwest China, the Taklamakan Desert is known as the largest dune field in China and one of the largest ergs on earth (Yang et al. 2006; Yang 2018). This hyperarid desert is one among the largest sand seas in the world (Rittner et al. 2016). Metagenome analysis has revealed greater bacterial diversity in such deserts. A study conducted for isolation of endophytic actinobacteria from psammophytes in Taklamakan Desert (Wang et al. 2020) has identified series of novel genera including Prauserella, Nesterenkonia, Labedella, and Aeromicrobium (Liu et al. 2015a, b; Li et al. 2019a, b). Bacterial analysis on diversity in Gobi and Taklamakan deserts revealed abundance of Firmicutes, Proteobacteria, Bacteroidetes, and Actinobacteria phyla being the most abundant (An et al. 2013). Additional screening in northwest China reported colonization of AM fungi; specifically with typical desert ephemeral plant communities in Junggar Basin, China reported fungal taxa belonging to the genera Acaulospora, Archaeospora, Entrophospora, Glomus, and Paraglomus (Shi et al. 2007). The Gurbantunggut Desert is the second largest desert in Xinjiang of Northwestern China, most of which areas are covered by biocrust (Zhang et al. 2007). These biocrusts are dominated with algal, lichens, and mosses including unidentified Ascomycota, Lecanoromycetes, Eurotiomycetes, and Dothideomycetes at class levels. Fungal communities vary with successional changes, change in soil conductivity, organic content, and other related factors. Dominant genera found in moss crust were Heteroplacidium and Endocarpon (Zhang et al. 2018). One of the most dominant pioneer salt-accumulating halophytes in the arid saline region of the Gurbantunggut Desert in China is plant Salicornia europaea L. (Chenopodiaceae) when studied for its endophytic bacteria revealed communities from different parts of the plant system like root, stem, and assimilation twigs. Isolated bacteria were identified as Bacillus endophyticus, Bacillus tequilensis, Planococcus rifietoensis,

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Table 1.2 Beneficial soil microbes boosting plant health from deserts of India Microorganisms Bacillus firmus Bacillus tequilensis Streptomyces maxicanus Trichoderma harzianum

PGP traits Biocontrol Biocontrol Biocontrol

References Lodha et al. (2013) Mawar et al. (2021b) Mawar et al. (2021a)

Biocontrol

Trichoderma longibrachiatum Aspergillus nidulans Aspergillus versicolor Aspergillus terreus

Biocontrol

Mawar et al. (2019); Mawar and Mathur (2022) Mawar et al. (2021a)

Biocontrol Biocontrol

Mawar et al. (2021a) Singh et al. (2014)

Biocontrol

Lodha and Harsh (2009) Yadav et al. (2015)

Lysinibacillus fusiformis Lysinibacillus sp. Lysinibacillus sphaericus Paenibacillus sp. Paenibacillus terrae Paenibacillus xylanexedens Planococcus antarcticus Planococcus donghaensis Planococcus kocurii Pontibacillus sp. Sinobaca beijingensis Sporosarcina aquimarina Staphylococcus arlettae Arthrobacter sulfonivorans Arthrobacter sulfureus Sanguibacter antarcticus Bacillus muralis Bacillus pumilus

Production of ammonia Production of ammonia, hydrogen cyanide Production of ammonia Production of ammonia Production of ammonia, ACC deaminase activity Production of ammonia Production of ammonia, hydrogen cyanide (HCN) Production of ammonia Production of ammonia, ACC deaminase activity Production of ammonia Production of ammonia Production of ammonia and gibberellins Production of ammonia Production of gibberellic acid Production of gibberellic acid Production of gibberellic acid Production of gibberellic acid Production of gibberellic acid

(continued)

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Table 1.2 (continued) Microorganisms Bacillus subtilis Desemzia incerta Janthinobacterium sp. P. frederiksbergensis Exiguobacterium sp.

PGP traits Production of gibberellic acid Production of gibberellic acid Solubilization of phosphorus, and production of indole-3-acetic acid (IAA) and siderophores Solubilization of phosphorus, and production of IAA and siderophores Solubilization of phosphorus, and production of IAA and siderophores

References

Variovorax paradoxus, and Arthrobacter agilis which possess tolerance to high concentration of salt and PGP activities, i.e., assist halophytic plants to tolerate abiotic stresses such as soil salinity found in the deserts (Zhao et al. 2016). Desert that covers average area of 2.3 million km2 left behind only the Sahara and Arabian deserts in size is Gobi Desert. The desert spreads across southern Mongolia and northwestern China (Sternberg et al. 2015). Studies revealed bacterial communities which mainly belong to the classes Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Bacilli, Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria from this desert show variations with dust and nondust events. Firmicutes and Bacteroidetes were prominent after the dust events. Further, low abundance of Archaea was also reported, i.e., two phyla Thaumarchaeota and Euryarchaeota (Maki et al. 2017). Besides, bacterial diversity in Gobi desert showed pattern of similarities with those isolated from Taklamakan Desert (An et al. 2013). An exploration study for endophytic fungal communities of Stipa sp. roots collected samples from six different types of steppes, i.e., subalpine meadow, alpine meadow, Gobi desert, desert steppe, typical steppe, and meadow steppe across Xinjiang, Gansu, and Inner Mongolia have revealed Ascomycota as the predominant fungi in all desert except genera like Curvularia and Rhizopus in Gobi desert were found abundantly (Shao-peng et al. 2014).

3.4

Deserts of Africa

Sahara desert is largest hot desert and third overall largest desert in world following cold deserts of the Arctic and Antarctic covering 9200,000 square kilometers. A study conducted to investigate the structure of soil bacterial communities present in the Gibson (Australia) and the Sahara (Egypt) deserts using 16S rRNA sequencing identified Actinobacteria as dominant phylum and others including Firmicutes, Proteobacteria, and Bacteroidetes phyla (Belov et al. 2018). Further, soil studies in northeastern Sahara (Egypt) identified bacterial community such as Proteobacteria—(Ochrobactrum); Actinobacteria—(Rhodococcus), and Firmicutes—(Bacillus) as dominating, and relative lower abundance of

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Gemmatimonadetes, Planctomycetes, and Deinococcus-Thermus was also found (Köberl et al. 2011). Namib is another long but narrow desert of Africa which is considered as one of oldest and driest desert. The Namib Desert spans a 2000 km longitudinal north–south zone from southern Angola to northern South Africa (Eckardt et al. 2013). Common bacteria phyla found include Bacteroidetes, Proteobacteria, and Actinobacteria. South African arid parts of Namibia have been explored for PGP bacterial endophytes from nonlegume plant Tylosema esculentum and identified Proteobacteria genera including Rhizobium, Massilia, Caulobacter Pseudorhodoferax, Pantoea, Sphingomonas, Burkholderia, Kosakonia Methylobacterium and some Firmicute like Bacillus, Actinobacteria like Microbacterium and Curtobacterium, and Bacteroidetes like Mucilaginibacter and Chitinophaga (Chimwamurombe et al. 2016). Similarly, extensive research in North African deserts such as Sahara Desert has been carried out to isolate endophytes, and a study with the date palm (Phoenix dactylifera L.) roots revealed bacterial isolates including Proteobacteria, Actinobacteria (Kalam et al. 2020), Firmicutes, and Bacteroidetes. Moreover, Pseudomonas genus was most abundant and exhibited PGP activity under drought conditions (Cherif et al. 2015). Further, two strong biocontrol agents have been isolated from Saharan including Streptomyces strain— S. rochei PTL2 with strong antagonism against soil-borne pathogenic fungus Rhizoctonia solani and Nocardiopsis dassonvillei MB22 with several PGP traits (Zamoum et al. 2017; Allali et al. 2019). The Mega Kalahari sand sea at 2.5 million km2 the largest on earth covers parts of Botswana, Namibia, and some parts of South Africa (Thomas and Shaw 1993). Microbial analysis reported presence of halophilic archaea, specifically abundant Halobacteria, and bacterial dominance of an acetogenic bacteria Acetothermia and Gemmatimonadetes, Firmicutes was confirmed (Genderjahn et al. 2018). Studies related to vesicular–arbuscular mycorrhizal (VAM) and their Vangueria infausta preferential host interactions revealed host dependency in VAM for its survival, and VAM had a significant positive effect on seedling dry mass, survival and phosphorus, nitrogen, and calcium concentration in the leaves (Bohrer 2001). A study conducted to identify phytopathological fungi causing diseases in trees of Namib and Kalahari deserts has identified Microsphaeropsis so., Drechslera sp., Botryosphaeria sp., Acremonium spp., Gliomastix sp., Trichoderma koningii, Peacilomyces variotii, Alternaria citri, and Curvularia pallescens from diseased tree including of Aloe, Acacia, Tylosema, and Syzygium (Chimwamurombe et al. 2016). The Karoo Desert or Great Karoo is semiarid desert located in South Africa. Fungal communities of Alternaria, Aspergillus, Bipolaris, Cladosporium, Fusarium, and Talaromyces have been isolated from the halophyte Sesuvium portulacastrum, one of the few species from Aizoaceae from Namaqualand, an area inside the Succulent Karoo biodiversity hot spot in South Africa. (Jacobs et al. 2016).

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Deserts of Arabia

In the parts of western Asia, bordering Yemen, the Persian Gulf, and Iraq, is the Saudi Arabian Desert. The microbial community exploration studies in such area revealed bacterial phyla like Actinobacteria, Gemmatimonadetes, Proteobacteria, and Firmicutes. Besides, these biogeochemically important microorganisms are exemplified by primary producers like Rhodoplanes and Cyanobacteria, nitrogenfixing members of the genus Rhizobium and Bradyrhizobium, and ammonia oxidizer Candidatus Nitrososphaera. Communities were also characterized (Khan et al. 2020). Arabian dust in Kuwait has been molecularly examined and identified with fungal genera including of Alternaria, Cryptococcus, Mortierella, Penicillium, Phoma, Rhodotorula, and Stemphylium (Lyles et al. 2005). Saudi Arabian soil revealed the presence of one undescribed fungal species of Chaetomium (Saadabi 2006).

4 Conclusion Vast of the planet’s landmass is covered by deserts, occupying almost 33% and one-third of available land. Deserts are extreme ecoregions and are driven mainly by their microbial habitants. Explorations of microbial communities from extreme arid ecoregions across the globe have been carried out to exploit their potentials as plant growth promoters to sustain agriculture in arid zones. Microbial diversity has been studied across the globe from arid deserts and frequently reported bacterial phyla in desert soil including Proteobacteria, Actinobacteria, Bacteroidetes, and fungal phyla like Basidiomycota and Ascomycota. Bacillus sp. and Bacillus-derived genera are most common in all arid deserts. Global scenario of microbes from arid deserts complied in this chapter may provide innovative wings to ongoing research across the planet and help to understand microbial diversity in different dryland ecosystems. The chapter discussed exceptional bioactivities of microbes, keeping agrisustainability in mind.

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Waller F, Achatz B, Baltruschat H et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391 Wang J, Shen J, Wu Y et al (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321 Wang T, Li F, Lu Q, Wu G, Jiang Z, Liu S et al (2020) Studies on diversity, novelty, antimicrobial activity, and new antibiotics of cultivable endophytic actinobacteria isolated from psammophytes collected in Taklamakan Desert. J Pharm Anal 11:241. https://doi.org/10. 1016/j.jpha.2020.06.004 Xu L, Zeng X-C, Nie Y et al (2014) Pontibacter diazotrophicus sp. nov., a novel nitrogen-fixing bacterium of the family Cytophagaceae. PLoS One 9:e92294 Yadav AN, Sachan SG, Verma P et al (2015) Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of Leh Ladakh (India). World J Microbiol Biotechnol 31:95–108 Yang W (2018) Atlas of sandy deserts in China. Science Press, Beijing Yang X, Preusser F, Radtke U (2006) Late quaternary environmental changes in the Taklamakan Desert, western China, inferred from OSL-dated lacustrine and aeolian deposits. Quat Sci Rev 25:923–932 Yeager CM, Kornosky JL, Housman DC, Grote EE, Belnap J, Kuske CR (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado plateau and Chihuahuan Desert. Appl Environ Microbiol 70:973–983 Yeager CM, Kornosky JL, Morgan RE, Cain EC, Garcia-Pichel F, Housman DC et al (2007) Three distinct clades of cultured heterocystous cyanobacteria constitute the dominant N2-fixing members of biological soil crusts of the Colorado plateau, USA. FEMS Microbiol Ecol 60: 85–97 Zablocki O, Adriaenssens EM, Cowan D (2015) Diversity and ecology of viruses in Hyperarid Desert soils. Appl Environ Microbiol 82(3):770–777 Zamoum M, Goudjal Y, Sabaou N, Mathieu F, Zitouni A (2017) Development of formulations based on Streptomyces rochei strain PTL2 spores for biocontrol of Rhizoctonia solani dampingoff of tomato seedlings. Biocont Sci Technol 27:723–738 Zhang YM, Chen J, Wang L, Wang XQ, Gu ZH (2007) The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. J Arid Environ 68(4):599–610 Zhang B, Zhang Y, Li X, Zhang Y (2018) Successional changes of fungal communities along the biocrust development stages. Biol Fertil Soils 54(2):285–294 Zhao S, Zhou N, Zhao ZY, Zhang K, Wu GH, Tian CY (2016) Isolation of endophytic plant growth-promoting bacteria associated with the halophyte Salicornia europaea and evaluation of their promoting activity under salt stress. Curr Microbiol 73:574–581 Zhu L, Bloomfield J, Hocart H, Egerton JG, O’Sullivan S, Penillard A et al (2018) Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes. Plant Cell Environ 41:1251–1262

Chapter 2

Harnessing Drought-Tolerant PGPM in Arid Agroecosystem for Plant Disease Management and Soil Amelioration Ritu Mawar, Madhavi Ranawat, Ladhu Ram, and R Z Sayyed

1 Introduction Arid zones are characterized by extremes of temperature, low precipitation, high wind velocity, and sandy soil. The Indian arid zone spreading in 31.8 million hectares of land almost covers 12% of country’s geographical area and includes parts of western Rajasthan, Gujarat, Punjab, Haryana, Maharashtra, Karnataka, and Andhra Pradesh. Despite the extremities proposed by desert environment, the cultivation of some major crops including pearl millet, cluster bean, moth bean, mung bean, cowpea, sesame, sorghum, and many others has been sustained in arid soil. The irrigated sections of Indian arid lands support cultivation of wheat, mustard, cumin, isabgol, onion, garlic, and many other important tree species. Cultivation of agricultural crops in water-scarce soil of deserts mainly depends on rain and groundwater status and continuously under threats proposed by several soil-borne plant pathogens. Legumes and oilseeds grown in these areas severely get affected by soilborne plant pathogen Macrophomina phaseolina (Tassi) Goid. and cause charcoal or dry root rot (Lodha et al. 1986; Lodha and Mawar 2019). However, varying degree of severity has been reported in different crops growing under similar ecoenvironment (Burman and Lodha 2000). The wilt causing pathogen Fusarium oxysporum f. sp. cumini has been reported frequently in cumin and tree mortality specially in Prosopis cineraria has been found associated with Ganoderma lucidum (Lodha et al. 1986; Mawar et al. 2020). Besides legumes and cereals, various fruit

R. Mawar (*) · M. Ranawat Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India L. Ram College of Horticulture and Forestry, Jhalawar, Rajasthan, India R. Z. Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_2

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crops like ber, pomegranate, aonla, and date palm have been cultivated in water deficit areas whose cultivation facing production constrains by pathogenic diseases is common concern. Lack of proper management practices reduces both quality and quantity and even clears out whole orchards. Powdery mildew of ber, suckers rot and fruit rots in date palm, leaf and fruit spots in pomegranate, and rust in aonla affect their foreign trade and affect economy. Several efforts have been made to sustain agriculture in arid zones including exploration of microbial agents aiding with plant health and providing resistance toward virulent pathogens (Mawar and Lodha 2019; Mawar and Sanyal 2021). Such biocontrol agents are effective, durable, costeffective, eco-friendly, and long-lasting solutions over chemical and other conventional management practices. This chapter provides comprehensive information on suitable plant growth-promoting microbes isolated from arid zones with tolerance against arid adversities and their applications in plant management strategies aiding stakeholders depending on cultivation for their livelihood. The chapter keeps concern with microbial biocontrol agents, root-associated microbiomes, rhizospheric networks, endophytes, mycorrhiza, symbioses, microbial formulations, volatiles, soil suppressions, amendments, and other related effects of PGPM from arid regions. The fundamental object of study is to provide directions to ongoing research explorations in arid ecosystems to harness PGPMs with drought and temperature tolerance abilities for purpose of their application in agriculture sustainability in dry– hot arid zones.

2 Mycorrhizae, Endophytes, and Symbionts in Plant Growth Promotion The synergistic relationship between mycorrhiza and mycorrhizal-associated bacterial communities plays (MAB) important role on improving soil and plant health by enhancing soil nutrient allocation through MAB-assisted nutrient solubilization and preventing intraradical colonization of soil-borne phytopathogens in arid and semiarid region of India. Further possibilities of integrating MAB having diverse PGPR attributes such as production of phytohormones, siderophores, and lignocellulose decomposing enzymes with suitable mycorrhizae type will enhance the interaction process, thereby extending the applicability of microorganisms for sustainable plant and soil health management (Mitra et al. 2019) A study highlighted arbuscular mycorrhizal fungi (AMF) as alternative option to conventional fertilization methods. However, soil inoculations require proper planning and variable results may be observed depending on nature of host plant and fungal association. Other factors affecting success rate and fungal persistence include species compatibility with the soil environment, spatial competition, and inoculation timing (Berruti et al. 2016). Recently through genomics and transcriptomic data advances in the knowledge of fungal interactions with the host-plant and other soil organisms unraveled various other important factors. Besides soil fertility, AMF is known to improve plant

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systemic resistance and can protect host plants against biotic stresses like plantparasitic nematodes through enhanced root tolerance, direct competition for nutrients and space, altered rhizospheric interactions, and induced systemic resistance and thus can be utilized as biocontrol of nematode pests (Schouteden et al. 2015). About 18 species, viz. 8 of Glomus, 3 each of Acaulospora and Sclerocystis, 2 each of Scutellospora and Gigaspora, were isolated. Glomus mosseae, G. intraradices, and G. fasciculatum had highest frequency of occurrence (100%) followed by Gigaspora albida, G. margarita, and A. bireculata (83% each), while other species ranged between 33% and 66%. Spore population showed strong positive correlations with root colonization, organic carbon and rainfall, fairly positive correlation with sand, pH, nitrogen and potassium, weak correlations with temperature, silt, clay, and electrical conductivity, and negatively significant correlation with phosphorous (Oyediran et al. 2018). Besides mycorrhizal fungi, the plant root niche is rich with various endophytic microbes contributing to plant health (Mercado-Blanco and Lugtenberg 2014; Hardoim et al. 2015). Role of root-associated bacterial endophytes in plant resistance has been confirmed through several of reports including resistance in tomato against R. solanacearum and resistance in Arka Abha cultivars. The resistant cultivars reported higher density of bacterial endophytes when compared with susceptible cultivars, which include Pseudomonas oleovorans, Pantoea ananatis, and Enterobacter cloacae. Bacterial endophytic species producing siderophores, HCN, and antibiotics resulting in bacterial antagonism also influence plant health positively (Upreti and Thomas 2015). A study with five different genetically modified Streptomyces spp. colonizing lettuce rhizosphere and on roots carried out by transforming strains with a green fluorescent protein marker and apramycin resistance reported in vitro inhibition of the soil-borne pathogen Sclerotinia sclerotiorum (Bonaldi et al. 2015). Further, the transformed strains reisolated from rhizosphere and roots suggest their rhizospheric or endophytic nature. Besides mycorrhizae and endophytes, microbial symbiont is also known to affect plant health and contribute to competitiveness of invasive plant species. Interactions of plants with their microbiome may hold biocontrol potential, and research aiming to develop novel microbe-based biocontrol strategies has already been proposed including invasive plant Phragmites australis (Kowalski et al. 2015).

3 Plant Growth-Promoting Metabolites In pot experiments, a marked increase in root length of cumin plant over control was observed in the treatment with A. versicolor and T. harzianum and their integration. However, integration of both the BCAs with Verbesina increased shoot length and weight. Synergistic effect of both the BCAs was clearly observed with the increase in shoot length and weight compared to that recorded in control. Therefore, increase in root length of cumin in A.versicolor amended soil indicating its growth promotion ability (Israel and Lodha 2005). However, further studies are required to better

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understand the interaction of BCAs before any final conclusion can be reached. This biocontrol agent also releases various hydrocarbon, alcohols, ketones, ether, and sulfur-containing compounds. Among these, S-containing compounds have also been identified as volatile metabolites toxic to fungal growth (Lewis and Papavizas 1970). Apart from release of antibiotics, various other metabolites have been also identified from A.versicolor. There are chances of variation in release of specific metabolites by a strain of biocontrol agent, which is heat-tolerant in nature. Therefore, there is a need to isolate and characterized specific metabolites quantitatively and qualitatively released by heat-tolerant stain of A.versicolor (Mawar and Lodha 2019). Similarly, in another pot experiment, guar seedlings were treated with bacterial bioagent B. firmus to know the effect on growth parameters and nodulation of guar seedlings. A significant increase in fresh and dry weights in B. firmus-treated guar seedlings compared to control and pathogen inoculated seedlings is an evidence that the bacterium is able to promote growth of test plant (Lodha et al. 2013).

4 Microbial Volatiles and Other Compounds in Plant Growth and Defense Plant roots are always in contact with soil microorganisms and flow of molecules released by them. Microbial exudates whether volatiles or particulates affect plants through a variety of mechanisms such as biochemical signaling that elicits local plant defense toward soil-borne pathogens or by inducing systemic resistance. Report evidenced volatile triggered secretion of plant root exudates which enhance or modulate overall plant fitness against fungi and bacteria and act as plant defense inducer (Kai et al. 2007; Chung et al. 2016; Yi et al. 2016). Besides providing defense to plants, soil microbes also affect plant metabolism and nutrient assimilation. A study conducted with Arabidopsis reported a novel mechanism through gene activation where plant growth-promoting (PGP) bacteria like Bacillus amyloliquefaciens GB03 activate gene responsible for sulfur assimilation and uptake by plant. Further, expression of transcripts coding for proteins which play key role in biosynthesis of sulfur-rich aliphatic and indolic glucosinolates was reported. The increased concentration of sulfur in plants favored glucosinolate biosynthesis which in turn conferred protection against the beet armyworm Spodoptera exigua (Aziz et al. 2016). In another report, members of Lysobacter spp. were found abundantly in soils that are suppressive toward the pathogen Rhizoctonia solani and were predicted to affect soil-borne pathogens through secretions of extracellular enzymes and metabolites. The isolated strains acted antagonistically, in vitro against phytopathogens including Rhizoctonia solani, Pythium ultimum, Aspergillus niger, Fusarium oxysporum, and Xanthomonas campestris, however not much suppression observed in fields of sugar beet, cauliflower, onion, and Arabidopsis thaliana implicating their poor

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rhizospheric colonization capabilities (Folman et al. 2003). Antagonistic potentials of Lysobacter spp. in disease suppressiveness need further exploration and confirmations, and they could emerge as novel source of versatile antimicrobial compounds (Gómez Expósito et al. 2015). Other than providing defense against pathogenic microorganisms, several microbial metabolites protect plants from herbivores. Foul odors and toxins from microbial exudates protect plants from gazing and act barrier for insect vectors (Mithöfer and Boland 2012). Fungal metabolites are also known to protect plants against feeding of the cereal aphid Rhopalosiphum padi upon association by Trichoderma citrinoviride isolates. Various long-chain primary alcohols (LCOHs) reported phagodeterrent effect, restraining aphids from settling on treated leaves. These LCOHs act through taste receptor neurons even at low concentrations and hold potential for insect management strategies in synergy with other control parameters (Ganassi et al. 2016).

5 Biocontrol Potential of PGPM The foregoing reveals that even under harsh climate of Indian arid region some native heat-tolerant PGPM does exist even when temperature reaches 55 °C in top layers of soil during summer period. Resting structures like chlamydospores and sclerotia of soil-borne plant pathogens withstand this temperature, but concurrently propagules of native PGPM also survive in such harsh climate. However, there is a need to improve their population to the extent these can fight well with soil-borne plant pathogens. Efforts to work out suitable food substrate for survival and multiplication of these bioagents have been achieved to a large extent in these years (Mawar et al. 2019). Amending soil with composts or suitable weed residues can also be an easy option for improving activity of bioagents. The studies done at arid zone institute CAZRI have also revealed that compatible BCA can be combined to improve pathogen control. Accordingly, T. harzianum and B. firmus were combined with suitable carrier and food substrates so that both the bioagents can survive (Mawar and Lodha 2012). Such a combination has multiple advantages of different mechanisms of biocontrol activity. Besides these, soil moisture also plays a pivotal role for the multiplication and activity of bioagents, particularly B. firmus. The biocontrol activity of bacterium is more discernible in the presence of adequate soil moisture. In recent years, large-scale mortality was witnessed in Indian mesquite (Prosopis cineraria). Easy-to-operate technology was developed where onion residues were incorporated beneath the tree after digging a pit. This improved the multiplication of Aspergillus terreus, a known bioagent against G. lucidum (Lodha and Harsh 2009). These studies have indicated that potential of biocontrol agents alone cannot be the only method of managing soil-borne plant pathogens. It must be an integral component of integrated disease management system. Usually, several other cultural methods of controlling soil-borne plant pathogens have been advocated world over. These include sound crop rotation, summer plowing, time of

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Fig. 2.1 Method of application of PGPM for disease management

sowing, use of organic amendments, moisture conservation techniques, and soil solarization. Use of PGPM as a biocontrol agent should then be incorporated using any of the several methods of application in soil, foliar spray, seed biopriming, or as seed treatment to improve disease control (Fig. 2.1). Efforts are also needed to explore more endophytic and drought-tolerant aggressive native strains of PGPM from soil.

5.1

Soil Amendments in Biocontrol

A variety of organic matter amendments were characterized and still under exploration for their potential to favor biocontrol agents and influence soil resident communities (Bailey and Lazarovits 2003; Bonilla et al. 2012). Similarly, soil amended with composted almond shell reported positive effect. Amended soil suppressed growth of pathogens including Rosellinia necatrix (a causal agent of white root rot on avocado) and favored Proteobacteria, Actinobacteria, and Ascomycota specifically Pseudomonas, Burkholderia spp., and Mortierellales (Vida et al. 2016). A study therefore was undertaken to investigate survival of bioagents, microbial population dynamics and activity, availability of micronutrients during the process

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Table 2.1 Changes in population of Bacillus spp. (× 10 6cfu g-1) and Trichoderma harzianum (× 10 3cfu g-1) in different composts during process of composting (Mawar et al. 2020)

Compost Calotropis procera Prosopis juliflora Weeds Azadirachta indica Acacia nilotica LSD(P = 0.05)

B. sp. T.H B. sp. T.H B. sp. T.H B. sp. T.H B. sp. T.H B. sp. T.H

Days 30 21 – 18 – 18 – 11 – 10 1 6 –

60 18 2.3 25 0.3 28 – 27 – 34 – 6 –

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90 15 0.3 16 13.3 20 2.3 13 2.0 33 2.6 5 2.2

120 43 1.3 24 1.3 13 1.3 10 1.3 30 0.6 8 1.0

150 14 – 17 – 24 – 14 – 23 – 6 –

of composting, and mature composts prepared from certain on-farm wastes (Mawar et al. 2020). In arid regions of India, direct incorporation of residues in soil has not been found successful due to low availability of soil moisture required for decomposition. Half-digested crop residues in turn aggravate termite infestation in rainfed crops. More so, crop residues themselves are often infected with soil-borne plant pathogens; their release in soil during slow decomposition may augment inoculum density of pathogens. Use of compost is an easy alternative for amending soil in arid soils where moisture retention is poor (Lodha and Burman 2000). Efforts were also made to inactivate released propagules of M. phaseolina from infected crop residues during heat phase of composting by increasing nitrogen concentration and exposing mature compost to dry summer heat. The changes in temperature, microbial population dynamics, and other factors were studied during the process of composting by layering residues of Calotropis procera, Prosopis juliflora, Azadirachta indica, Acacia nilotica, and weeds. Temperature began to rise soon after filling the residues and ranged between 55 and 59 °C for next 7 days with maximum being in Calotropis pit (59.2 °C). Estimation of microbial population dynamics and activity has shown that in the heat phase, fungal population remained low but reinfestation occurred after 30 days in all the composts except weed compost. There was a fluctuation in total actinomycetes and bacterial population in all the decomposing residues initially; however, at 150 days counts were maximum in Calotropis compost (Mawar et al. 2020). Trichoderma harzianum disappeared during peak heating, but reinfestation occurred at mature stage with maximum counts in P. juliflora compost, while Bacillus spp. was present throughout the composting period (Table 2.1). At maturity, total fungi were maximum in neem followed by P. juliflora compost, but total actinomycetes and bacterial population were maximum in Calotropis compost. Maximum antagonistic actinomycetes were estimated in A. nilotica, and P. juliflora composts maintained its superiority in terms of microbial activity during the process of composting as well as at maturity (Table 2.1). Among all the composts, maximum available micronutrients like Cu, Zn, Mn, and Fe were estimated in compost prepared from A. nilotica (Mawar et al. 2020). Similarly, Neem cake also came

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out as an excellent carrier as it gave a prolonged shelf life of 200 days of T. viride. Antifungal assay against plant pathogenic fungi revealed complete inhibition of growth and sporulation of fungal pathogens (Zope et al. 2019).

5.2

Suppressive Soil and Biocontrol

Once a biocontrol agent has proved its potential in control of a target pathogen, some specific aspects need investigations particularly in relation to the host and climate under which its use can be promoted. Studies are required to know its survival rate at different soil depths in fluctuating weather conditions and how other bioecological factors are governing population dynamics of the biocontrol agent. By generating this information, manipulation of soil environment and other associated bioecological factors in favor of PGPM, its population, and activity can be enhanced in order to develop soil suppressiveness. Mode of action, survival in soil, and growth promotion abilities of Trichoderma harzianum and T. viride as a biocontrol agents have been studied in detail, but no information is available on population dynamics of A. versicolor a potent BCA. Studies on population dynamics over time and space have two basic goals: (a) to identify recurring pattern in the dynamics of a population and (b) to understand how such patterns are generated. Therefore, study was undertaken to understand how biotic and abiotic factors influence population of A. versicolor at different soil depths in arid soils. Availability of organic matter and warmer temperatures at lower soil depth, in turn, favored survival of A. versicolor and other soil fungi. Positive correlation of soil moisture with fungal population has also been established by other workers. Variations in earlier findings can be attributed to seasonal conditions of both climates, particularly of arid region where soils are low in organic matter and temperature exceeds beyond 55 °C in summer months. This is also evident from the fluctuations in A. versicolor population at lower soil depth where because of lower levels of temperature compared to upper soil depth, population continued to increase up to June (Singh et al. 2014). Occurrence of highest population in October at lower soil depth when the temperature reached 51 °C is yet another evidence for the hypothesis (Singh et al. 2014). Soil suppressiveness is an uncommon property of soil to selectively affect survival of some microorganisms negatively. The infrequent phenomenon of soil suppression is known to regulate noxious organisms including root-knot nematodes Meloidogyne spp. and favor plant health (Bent et al. 2008). A number of studies have stated that Lowsonia (heena) plants can be used for suppression of the root-knot nematode Meloidogyne javanica. Significant suppression of larval hatching in the nematode M. incognita by bark extract of heena has also been reported. A rich biodiversity of plants in Indian arid region has also provided a number of plants possessing insecticidal and fungicidal activity against insect, pest, and diseases occurring in this region. Nature has bestowed arid region with diverse vegetation, which can be explored as botanical pesticides for soil suppressiveness. A study conducted in two organic horticulture greenhouses in Spain reported progressively decline in

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nematodes population with crop rotation and found associated cause as egg parasitism by the hyphomycete Pochonia chlamydosporia. Further suppressive nature of soil confirmed through the non-sterilized soil where lower egg densities and reduced Meloidogyne reproduction was observed with higher microbial density in soil (Giné et al. 2012). However, soil suppressiveness needs more exploration to reveal its potentials for common use. Entomopathogens are classical biocontrol agents for pest management which can be bacteria, fungi, virus, and nematodes that kill or seriously disable arthropods like insects, mites, and ticks (Dara 2017). Phoretically associated insect-killing bacteria attribute entomopathogenic nature to nematodes (Lewis et al. 2015). A report on entomopathogenic nematodes like Steinernema sp. and S. diaprepesi occupy habitats with different soil properties and water potential conducted in Florida reported their migration behaviors associated with soil water potential where former dominated when soil was maintained at 18% moisture, while latter preferred slight drier soil at 6% moisture. Differential expression of proteins involved in thermo or mechanosensation, movement, gene regulation, cell division, and metabolism was reported in these two to have association with soil moisture, and thus, modifying soil moisture in farmlands may favor effective entomopathogens in different environment (El-Borai et al. 2016). Disadvantages associated with chemical means of managements like environmental harms, emergence of resistant traits in pests/pathogens and pesticide bans, necessitates diversion to more effective biocontrol agents with higher specificity, reduced cost and lower environmental impacts. A variety of biocontrol agents have been explored and applied for agriculture sustainability. As an alternative to copperbased products against the oomycete Phytophthora infestans which cause late blight (the most severe disease of potato), three different Pseudomonas isolates originating from potato phyllosphere and rhizosphere were studied for their protective effect against late blight. The study suggested higher in vitro and greenhouse potentials of Pseudomonas chlororaphis R47 and their active survival for 15 days whereas for 8 days in field applications with high rate of colonization and beneficial effect against P. infestans suggesting their potentials as effective applicants (Nowicki et al. 2012; Guyer et al. 2015). A human pathogen, Pseudomonas aeruginosa, has been exploited in agriculture as model system because of its endophytism and antagonism toward plant pathogens and pests (Deredjian et al. 2014). A variety of microbial formulations are being used and produced for agricultural sustainability using biocontrol and plant growth-promoting microbial species including endospore forming Bacillus spp. as an alternative to chemical formulations and pesticides. Applications of B. amyloliquefaciens-type strain FZB42 have been reported as one such example (Wu et al. 2015).

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PGPM in Induced Resistance in Plants

The effect of disease control agent on plant growth cannot be measured directly as it involves two components; one component is the direct effect of the control agent on the plant, which may be detrimental, neutral, or beneficial (promoting growth). The second component is the indirect effect on the plant through disease control, which in turn may result in enhanced plant growth. Study conducted at arid zone where significantly better growth of seedlings of cluster bean in presence of pathogen Macrophomina and B. firmus bioagent compared to pathogen alone demonstrated that bacteria not only inhibited fungal infection but also promoted the plant growth (Lodha et al. 2013). Ryder et al. (1999) have also reported that B. subtilisB908, which showed consistent, shoot growth promotion effect in addition to its ability to reduce the severity of take-all of wheat. Singh and Mehrotra (1980) reported reduction in disease caused by R. bataticola in addition to increased plant growth and dry matter production of Bacillus treated seeds. Nitrogen-fixing ability of other species of Bacillus native to aridisols of India has been observed by Bajoria et al. (2008). Plants do possess specific mechanisms to tackle attacking pests, pathogens, and parasites. To escape from plant immunity, pathogens also have strategies and varying degree of virulence. Different exudates, formulations, toxin compounds, and enzymes are attributed to virulence shown by pathogens. A report suggested active role of abscisic acid (ABA) in interactions between blast fungal pathogen Magnaporthe oryzae and the antagonistic bacterium P. chlororaphis EA105 with rice host. The pathogen, Magnaporthe oryzae-produced ABA, enhanced plant susceptibility by affecting plant defense against fungi by acting antagonistically on salicylic acid (SA), jasmonic acid (JA), and ethylene signaling, thereby accelerating pathogenesis through higher rates of spore germination and appressoria formation. Micromonospora strains have been reported to control fungal pathogens by provoking plant immunity. The strain dwells in nitrogen-fixing nodules of healthy leguminous plants and possesses PGP effect. This Gram-positive antifungal isolate reduced leaf infection by Botrytis cinerea through durable induced systemic resistance when inoculated on tomato roots. Further, gene expression analyses revealed mechanism of action of Micromonospora, which later confirmed using defenseimpaired tomato mutants. Strain stimulated plant defense by enhancing jasmonateregulated defense pathways and appears as extraordinary biocontrol agents with additional antifungal activity than eliciting plant immunity (Martínez-Hidalgo et al. 2015). Report on Trichoderma parareesei transformants with reduced chorismate mutase (CM) activity (an intermediate of aromatic amino acids, essential in protein synthesis and precursor of many secondary metabolites) through Tparo7 gene silencing confirms reduced pathogen colonization by limiting growth rates and mycoparasite behavior against phytopathogenic fungi including R. solani, F. oxysporum, and B. cinerea in dual in vitro cultures. Transformants reported to reduce susceptibility of tomato toward pathogens and also produced higher amounts

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of aromatic metabolites like tyrosol, 2-phenylethanol, and salicylic acid (SA) (Pérez et al. 2015).

6 Omics Approaches in PGPM With recent advancements in research towards soil microbes and their potential as PGPM is also growing as the research is going on. “Omics” research has allowed more rapid, authentic, and cost-effective ways on collecting precious information and data to us, providing better understanding on many unexplored trophic interactions in rhizospheric systems and also of novel unexploited microbes from soil (Massart et al. 2015). Twelve different strains of Bacillus subtilis with PGP capabilities were studied and their genomic analysis exhibited high diversity except in extremely conserved B. amyloliquefaciens strains. The omics analysis identified various genes linked to biocontrol and colonization capacity of bacterium including 73 such genes with functions related to signaling, transport, secondary metabolites, and carbon utilization from B. amyloliquefaciens subsp. Plantarum. Deletion in these genes, for example, in conserved polyketide biosynthetic clusters encoding difficidin and macrolactin like secondary metabolites, has reported pivotal role of reducing damage by Xanthomonas axonopodis pv. vesicatoria on tomato (Hossain et al. 2015). Further genome sequencing and analysis of bacterium Pseudomonas sp. SH-C52 isolated from R. solani suppressive soil revealed their antifungal activity attributed to the chlorinated 9-amino-acid lipopeptide thanamycin, and the isolate itself was found closest to Pseudomonas corrugate. Genome size of 6.3 Mb with predicted 5579 ORFs showed six nonribosomal peptide synthetase gene clusters, including clusters for thanamycin and brabantamide from which former presents antifungal nature, whereas latter has anti-oomycete activity, affecting phospholipases of Phytophthora infestans. Third lipopeptide cluster thanapeptin, structural variants to known secondary metabolites, was found effectively active against P. infestans and remaining cluster codes for unknown products. Overall study revealed potential for SH-C52 lipopeptides with different antimicrobial, antifungal, and anti-oomycete activities (Van der Voort et al. 2015). Lichen microbiomes were tested to analyze antagonism against bacteria and fungi, and dominating communities including Stenotrophomonas, Pseudomonas, and Burkholderia showed antagonism against Lobaria pulmonaria. Seven percent of metagenome studied has shown antagonism and PGP effect. Similar effect was reported from bioactive compounds like spermidine isolated from Stenotrophomonas suggesting lichens as important reservoirs for active antagonistic bacteria that can be utilized in agricultural applications (Cernava et al. 2015).

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7 PGPM-Directed Arid Land Amelioration To sustain agriculture in arid zones, research efforts have been made from decades to develop durable management strategies to manage various soil-borne plant pathogens infecting major arid crops and trees, and these include use of moisture conservation techniques (Lodha 1996), soil solarization (Lodha 1995), use of soil amendments like cruciferous residues (Mawar and Lodha 2002), composts (Bareja et al. 2013), screening of tolerant genotypes (Lodha and Solanki 1992), biomanagements, and integration of various available control methods like soil solarization with amendments, for example, integrating sublethal heating with cruciferous residues and like synergistic application of chemicals with biocontrol agents (Singh et al. 2012; Mawar and Lodha 2009). Rising concerns over pesticides application, their environmental impacts, and resistance in pathogens toward these chemicals have advanced exploration of microbial communities with tolerance abilities to withstand arid stresses. Further, their associations with common arid plants enhanced plant resistance, boosting overall plant health and as result production and quality. PGPMs provide stress tolerance to plants against several biotic and abiotic factors and enhance plant immunity, nutrient uptake, and assimilation capabilities as depicted in Fig. 2.2. Soil samples from different arid ecosystems were collected and analyzed for isolation of effective drought-tolerant bioagents and identified native biocontrol agents showing antagonistic effect in vitro including Trichoderma harzianum, T. longibrachiatum, Aspergillus versicolor, A. nidulans, Bacillus firmus, B tequilensis, and Streptomyces mexicanus (Mawar et al. 2017; Lodha et al. 2019; Mawar et al. 2021a, b). Field efficacy of these identified bioagents on major arid

Abiotic stresses

• • • •

Biotic stresses

Drought Temperature fluctuations Precipitation fluctuations Salinity PH

• • • • •

Enhanced stress Tolerance

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Phytohormones Siderophore Production • Biocontrol • Induced Systemic Resistance 2. PGPM

Bacteria Fungi Viruses Nematodes Insects

Nutrient uptake & assimilation PGPM- Plant Growth Promoting Microorganisms

• • • •

Nitrogen fixation Nutrient uptake P-solubilization K-solubilization

Fig. 2.2 PGPM-mediated plant resistance toward various abiotic and biotic stresses and enhanced stress tolerance, nutrient uptake, and assimilation abilities

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crops and their effect on soil resident microflora need excessive field trials and additional information on their behavior. Soil amendments and a variety of natural residues have been explored including food substrates to enhance survival of these agents in arid soil. Mechanism through which these agents show antagonism includes both direct operations like parasitism, antibiosis, competition, and indirect effects through manipulating host rhizosphere, reducing host susceptibility, secreting exudation, resistance through host-mediated interactions, hypovirulence, and plant growth-promoting effects. A study conducted for 2 years to determine collective effect of two different drought-tolerant biocontrol agents which can survive up to 62 °C including Bacillus firmus and Aspergillus versicolor against plant pathogens, Macrophomina phaseolina and Fusarium oxysporum f sp. cumini induce charcoal rot in cowpea and wilt in cumin respectively suggested better root colonization with both biocontrol agents in combinational treatments. Rather, individuals and efficiency of biocontrol agents shown increment when soil amendments like radish compost, farmyard manure, and neem compost were applied along bioagents (Singh et al. 2012). Potential of Bacillus firmus as plant growth-promoting bacteria and specific biocontrol agent against phytopathogen M. phaseolina is reported with guar; successful field demonstrations of the same were carried out at Central Arid Zone Research Institute, Jodhpur, Rajasthan (Lodha et al. 2013). The efficacy of T. harzianum was also demonstrated against dry root rot of sesame and wilt of cumin. Studies revealed that seed treatment with PGPM significantly reduced incidence of root rot and wilt in all the demonstrations resulting in significant increase in seed yield. Maximum yield promotion (14.9–19.0%) due to seed treatment was recorded in sesame during experimentation at villages of Pali District. Similarly, significant reduction in wilt incidence and thereby increased seed yield (14.5–23.1%) were recorded in cumin in many districts of Rajasthan. Consortium of B. firmus and T. harzianum also increased seed yield by 22.9% in guar at Jodhpur. These demonstrations have resulted in wider acceptance by rainfed farmers and more by cumin growers under irrigated conditions (Mawar et al. 2019). Similarly, a study conducted in Indian mesquite, on a well-documented arid zone tree Khejri (Prosopis cineraria Druce), to rescue it from large-scale mortality due to root rot caused by Ganoderma lucidum has identified three major BCAs including Trichoderma harzianum, T. longibrachiatum, and Aspergillus nidulans (Mawar et al. 2020) and two bacterial antagonists including Streptomyces sp. strain AZAC1 and Bacillus sp. strain AZ-11 (Mawar et al. 2021a, b).

8 Outlook and Future Challenges This article provides polyhedral view on various subjects concerning beneficial microbes and their potential applications in agriculture sustainability. Information complied indeed demands deeper exploration for microbial reservoirs and resources with positive influence on plant health and devising proper plans for their field

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applications. With increasing populations and food demands, agriculture sustainability has become topic of concern and thereby necessitates quick solutions to emerge as permanent option. However, it indeed is not a simple task considering the huge microbial diversity present on planet. We have only explores pinch of available microbial resources however information is not enough about their ecosystem services. Challenges for future research work concern not only the exploration but also the rightful application of already explored microbial species. Deeper knowledge on biology and excessive trials is required to widen their potential in vast range of arid agricultural soils.

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Chapter 3

Role of Plant Growth-Promoting Bacteria in Rainfed and Irrigated Crops Pratibha Vyas, Amrita Kumari Rana, and R. C. Kasana

1 Introduction It is evident that the beginning of the twenty-first century around the world is pronounced with a decrease in the availability of water resources and increased environmental pollution along with soil and water salinization. The ever-rising human population and decrease in the area under cultivation are the two other threats to sustainability in agriculture in the present scenario (Shahbaz and Ashraf 2013). A number of ecological stresses including drought, flood, high and low temperatures, and salts have negatively impacted the cultivation of different crops. A greater decline in the crop productivity and quality is preferably caused by drought and soil salinity (Kannepalli et al. 2021; Sagar et al. 2022). Thus, plant growth and development along with resistance to these climatic stresses become a topic of discussion for agriculture and plant-based technologies. There exists a comprehensive study on the plant responses to these biotic and abiotic stresses with their useful and harmful impacts on the plant growth. Our current knowledge to these processes involved in the adaptation of plants to ecological stresses is limited. Thus, there exists a need to understand mechanism of the processes adopted by plants to survive under conditions of stress (Ma et al. 2020).

P. Vyas · A. K. Rana Department of Microbiology, College of Basic Sciences and Humanities, Punjab Agricultural University, Ludhiana, Punjab, India R. C. Kasana (*) ICAR-Central Institute of Post-Harvest Engineering and Technology, Ludhiana, Punjab, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_3

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2 Effect of Stress on Crop Production Abiotic stresses are considered, one of the major obstructions to crop production and food security across the world. Recent drastic and rapid changes in the climatic conditions globally have aggravated the situation. To manage these stresses in a better and effective way, it becomes important to understand their physiological, biochemical, and ecological interactions with plants. The responses of plants to these ecological stresses can be studied through changes in their morphology, physiology, and biochemical reactions (Fahad et al. 2017). These abiotic stresses include high temperature, depletion in water sources, salinity, and heavy metals contamination in soil which affect the crop sustainability worldwide (Fig. 3.1). These have been found to disturb plant growth and yield (Waqas et al. 2019).

2.1

Effect of Drought/Water Stress

It is hard to predict the extent of the damage caused by the scarcity of water as it depends on a number of factors such as the rate of precipitation, the water holding capacity of soil, and the loss of water through evapotranspiration. The adverse effects are seen as decreased development of plant, nutrient and water relations; assimilate partitioning, photosynthesis causing a significant drop in crop yields (Fig. 3.2). It has been found that the response of plants to drought stress is different from species to species and depends on the growth stage of the plant and other ecological factors (Fathi and Tari 2016; Hussain et al. 2018; Khan et al. 2020).

Fig. 3.1 Various biotic and abiotic stresses affecting plant growth

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Fig. 3.2 Effect of drought stress on plants

2.1.1 2.1.1.1

Morphological Responses Growth

The poor germination of seeds and impaired seedling establishment comprise the initial effects of drought on plants. Plant growth is accomplished by different processes comprising cell division, enlargement, and cell differentiation. It has been found that drought stress hinders the process of mitosis and cell elongation leading to impaired growth of the cell (Hussain et al. 2018). It has been found that impaired cell elongation mainly occurs due to a lesser flow of water from the xylem to nearby cells. Depletion in the leaf size and number is usually determined by turgor pressure and the utilization of assimilates. Thus, under drought conditions, the turgor pressure is reduced along with the slow rate of photosynthesis limiting the expansion of leaves (Fahad et al. 2017).

2.1.1.2

Yield

It has been found that the adverse impacts of scarcity of water on the yield of any crop are usually determined by the intensity of the stress and the growth stage of the plant. High losses have been reported in the yield of major crops due to conditions of drought (Table 3.1).

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Table 3.1 Examples of some crops with yield losses due to drought stress Crops Zea mays L. Helianthus annuus L. Cicer arietinum L. Glycine max L. Oryza sativa L. Triticum aestivum L.

Decrease in yield (%) ~87 ~60 ~69 ~71 ~92 ~57

Reference Kamara et al. (2003) Mazahery-Laghab et al. (2003) Nayyar et al. (2006) Samarah et al. (2006) Lafitte et al. (2007) Balla et al. (2011)

Enzymes such as sucrose synthase, starch synthase, starch branching enzyme, and adenosine diphosphate glucose pyrophosphorylase control the process of filling in cereals. Their decreased activity due to drought stress leads to reduction in the yield of major cereal crop plants (Najafi et al. 2021). It has been reported that the reason behind the reduction in the yield depends on different factors such as a decrease in the process of photosynthesis, assimilate partitioning imbalance, or reduced flag leaf development (Kannepalli et al. 2021). For example, a significant reduction in the yield of maize was observed when exposed to conditions of drought at the tasseling stage (Anjum et al. 2011). In cotton, lesser production of bolls and absorption of the bolls were recorded under drought stress that resulted in lower lint harvest (Khan et al. 2017a). Similarly, a 50% loss in the seed yield of pigeon pea (Cajanus cajan L.) was observed under situations of ecological stress (Nam et al. 2001).

2.1.2 2.1.2.1

Physiological Responses Water–Nutrient Balance

Exposure to drought stress affects the stomatal conductance, leaf water potential, leaf and canopy temperature, and rate of transpiration in the plants which ultimately affect the water relations. Water use efficiency defined as the ratio of the dry matter accumulated to the water consumed is considered as an important feature of the process of plant physiological regulation (Ullah et al. 2019). It has been reported that exposure to water shortage at an early-season stage can lead to loss in biomass accumulation and harvest due to reduction in the efficiency of water use in potato (Solanum tuberosum L.) (Rolando et al. 2015). Similarly, it has been reported that drought stress also impacts nutrient relations in plants. Some of the elements such as nitrogen, silicon, magnesium, and calcium are absorbed from the ground along with water by plants; however, drought stress limits their movement via diffusion and mass leading to poor plant growth (Ahanger et al. 2016). The uptake of nutrients having slow mobility, for example, phosphorus, is hindered due to reduced root growth under moisture deficient conditions. This happens because plants possess the ability to alter root length and surface area and architecture to absorb the fewer mobiles nutrients, but the process is disturbed under drought conditions (Najafi et al. 2021). Under water stress conditions, the limited nitrogen-fixing ability of legumes

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negatively affects their yield in many arid and semiarid regions around the world. The major factors that affect the process of nitrogen fixation under drought conditions are oxygen limitation, shortage of carbon, and regulation by nitrogen metabolism. It has been found that under water stress, there is an increase in the nodular oxygen diffusion resistance. However, such changes cannot be considered as the only causes of the decline in nitrogen fixation as the process cannot be brought back to same pace by simply increasing the concentration of O2 in the rhizosphere. Another reason is the reduced supply of carbon to the bacteroides. Sucrose is the main carbon source that is transported from shoots into nodules and is hydrolyzed with the help of either Suc synthase (SS) or alkaline invertase (AI). The activity of Suc synthase is essential for functioning of nodule. Under drought conditions, the activity of the enzyme SS is found to decline in both tropical and temperate legumes. To avoid nitrogenase damage, due to transient accumulation of oxygen in the infected region, an increase in the resistance of the oxygen diffusion barrier would take place. Thus, a decline in the process of nitrogen fixation occurs with the closure of oxygen diffusion barrier and decrease in the number of respiratory substrates. It has been found that nitrogen metabolism also plays an essential role in the process of regulation of nitrogen fixation under conditions of water stress by a feedback mechanism involving status of shoot nitrogen with many other molecules being involved in the process (Ladrera et al. 2007; Schwember et al. 2019).

2.1.2.2

Photosynthesis

It can be considered as the one of the important physiological process to be negatively affected under water stress conditions. It is found that reduction in leaf expansion, impaired functioning of the photosynthetic machinery, and leaf senescence happen under drought conditions (Dubey 2018). Two important functions of stomata are as follows: One is the regulation of transpiration that deals with the supply of nutrients to the plants along with temperature regulation, and the other is to the entry of carbon dioxide into the leaves. However, under drought conditions, reduction in the stomatal aperture occurs, and continuation of the water deficit conditions causes impairment of carbon metabolism and changes in the leaf photochemistry, hence negatively affecting photosynthesis. An adaptive mechanism by plants to the onset of conditions of water stress is the reduction in the width of stomatal aperture. (Saradadevi et al. 2017). Also, diffusion of carbon dioxide through mesophyll cells is affected because of the changes in the leaf biochemical interactions and permeability of membrane along with shrinkage of leaves. Low availability of carbon dioxide due to the stomatal closure in the intercellular spaces can hinder several biochemical functions in leaves. This also causes a decrease or in-activation of the enzyme ribulose1,5-bisphosphate carboxylase/oxygenase (RuBisCO) or ribulose-5-phosphate kinase or a reduction in the substrate RuBisCO (Ma et al. 2020). It has been found RuBisCO is concentrated in leaves, depending on the rate of process with which it is synthesized and utilized. It possesses the ability to remain stable under conditions of low water stress due to its half-life of a couple of

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days. Under mild drought conditions, two major factors that limit photosynthesis are the decrease in the process of phosphorylation and ATP synthesis (Fahad et al. 2017).

2.1.2.3

Assimilate Partitioning

It has been fund that under drought conditions, the assimilate balance is damaged as most of them are transported to roots so as to manage uptake of water by plant (Ullah et al. 2019). The photosynthetic rate and the amount of sucrose present in leaves affect the source to sink transport of assimilates. As under water stress conditions, the rate of process of photosynthesis is reduced so as the sucrose content in the leaves is ultimately decreased (Kim et al. 2000). The sink possesses the ability to utilize the incoming assimilates, but it is impaired under conditions of drought. Moreover, the phloem loading and unloading are disrupted as the activity of the enzyme acid invertase is impaired. Thus, under moisture stress dry matter portioning is badly affected.

2.1.3

Metabolic Responses

It has been studied that under conditions of stress, there occurs deep modifications in metabolite biosynthesis, transport, and storage. Changes in the both primary and secondary metabolic compound have been reported under such conditions. On the one hand, primary metabolites are found to be important at different growth and developmental stages of the plant; on the other hand, secondary metabolites help in the interaction of plant with the ecological niches (Jorge and António 2018). The adaptation in the process of photosynthesis and osmoregulation is one of the earliest strategies of plant under drought conditions. Osmolyte accumulation, for example, carbohydrates (e.g., glucose, trehalose, sucrose, and raffinose), polyols (e.g., sorbitol and mannitol), amino acids (e.g., proline, betaine, valine, leucine, and isoleucine), quaternary ammonium compounds (e.g., glycine betaine, b-alanine betaine, and proline betaine), and polyamines (e.g., putrescine, spermidine, and spermine) have been reported in several metabolic studies. They have been found to play an essential role in the reduction of osmotic potential as well as cell turgor pressure maintenance, thus contributing to stabilization of membranes, enzymes, and protein (Sharma et al. 2019). It has been found that exposure of plants to drought stress can technically lead to oxidative damage due to the production of reactive oxygen species (ROS). These have been reported of having destructive impacts on the cell functioning by causing damage to lipids and proteins. For example, in pea, peroxidation of lipids and proteins was found to be increased by 4 times under drought stress conditions. These are generally produced in the chloroplast, but reaction between oxygen and certain components involved in electron transport chain can also produce ROS in mitochondria. The different processes involved in the ROS production are either of enzymatic or nonenzymatic nature (Signorelli et al. 2015).

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Plants use the antioxidant defense mechanism (either enzymatic or nonenzymatic) to deal with the oxidative stress. However, enzymatic defense mechanism has been found to be most effective strategy. Enzymes such as SOD, GR, POD, and CAT play an important role in this system. Therefore, maintaining a higher level of antioxidants can be considered as an effective strategy by plants to deal with the harmful impacts of ROS (Hasanuzzaman et al. 2020). Other defense molecules in plants that help them to maintain a higher level of antioxidants are phytohormones. Plants are able to adjust to different ecological conditions with changes growth regulation process, development, source/sink transitions, and nutrient allocation (Fahad et al. 2015).

2.2

Effect of Salinity

Another major factor contributing to the loss of productivity of soils under cultivation is the soil salinization. This phenomenon has been found to be intense in cases of irrigated soils leading to an increase in the area under salinized soils. It has been found that about 45 million ha (20%) of the cultivated area producing food for one-third of the world’s population is salt affected. Furthermore, about ten million ha of land under agriculture has been destroyed by salt accumulation around the world. This rate of land degradation is found to be accelerating due to changes in climate, excessive use of groundwater, higher use of low-quality water in irrigation, and use of new irrigation techniques with intensive farming but having poor drainage. If this situation continues, then it has been estimated that by 2050, about 50% of the fertile land around the world will be adversely affected by salinity. Thus, soil salinity can reduce the productivity of many agricultural crops especially vegetable crops which are having low tolerance to salinity (Machado and Serralheiro 2017). The intensity and time interval of the salt stress impact various changes that occur in the physiology and metabolic processes of the plants leading to decrease in crop production (Fig. 3.3). Initially, it is found that osmotic stress followed by iron toxicity hamper the plant growth. The capacity of the root system to absorb water decreases during initial phase of salinity stress. This occurs along with the acceleration in the water loss from leaves due to osmotic stress, leading to condition of hyperosmotic stress. Salinity stress have been found to cause a number of changes in physiology of the plants for example; membrane interruption, imbalanced nutrient transport, disabled detoxification of reactive oxygen species (ROS), antioxidant enzyme differences and reduced activity of photosynthesis, and stomatal aperture reduction. It is also known as the hyperionic stress as one of the pernicious impacts of salinity stress is building-up of sodium (Na+)and chlorine (Cl-)ions in the plant tissue exposed to soil with higher concentrations of NaCl. Sever ion imbalance is caused due to the entry of both the Na+ and Cl- ions into the cells with excess uptake causing severe physiological disorders. It has been reported that higher concentration of Na+ negatively impacts the K+ ion uptake that plays an important role in the growth and development of the plant, thus leading to lower productivity and even

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Fig. 3.3 Effect of salinity stress on plants

death. The ROS is produced in the form of singlet oxygen, hydroxyl radical, hydrogen peroxide, and superoxide which is increased in response to salinity stress. However, salinity-induced production of ROS can cause oxidative damages in different components of the cell, for example, proteins, lipids, and DNA, hampering important plant cellular functions (Gupta and Huang 2014; Flowers and Colmer 2015). Salinity stress has been found to affect photosynthesis as it reduces area of leaf, chlorophyll content, and stomatal conductance along with the loss in the functioning of photosystem II. Under salinity stress, inhibition of microsporogenesis and elongation of stamen filament occur leading to an increased programmed cell death in some tissues with abortion of ovule and senescence of fertilized embryos. Thus, all these factors can result in hinder plant growth at physiological, biochemical, and molecular levels (Shrivastava and Kumar 2015).

3 Mechanism of Stress Tolerance in Plants By induction of a number of morphological, biochemical, and physiological changes, plants are able to thrive and adapt under stress conditions (Table 3.2). For example, tolerance to drought can be summarized as the ability of the plant to grow, flower, and produce profitable harvest under limited supply of water. Mechanisms of drought tolerance are discussed below:

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Table 3.2 Mode of action of plant growth-promoting rhizobacteria for stress tolerance in plants Crop Maize (Zea mays L.)

PGPR strain Rhizobium and Pseudomonas

Peanut (Arachis hypogaea L.)

Brachybacterium saurashtrense and Brevibacterium casei

Wheat (Triticum aestivum L.)

Pseudomonas pseudoalcaligenes

Wheat (Triticum aestivum L.) Soybean (Glycine max L.) Pea (Pisum sativum L.)

Azotobacter vinellandii (SRIAz3) Pseudomonas putida H-23 Arthrobacter protophormiae

Tomato (Solanum lycopersicum L.) Maize (Zea mays L.)

Streptomyces sp.

Barley (Hordeum vulgare) Cotton (Gossypium hirsutum L.) Wheat (Triticum aestivum L.) Mung bean (Vigna radiata L.) Beet (Beta vulgaris L.)

Hartmannibacter diazotrophicus

Bacillus sp., Arthrobacter pascens

Mode of action Increased proline synthesis, water-level maintenance along with selective uptake of ions, and reduced electrolyte leakage Increased plant length, shoot length, root length, and total biomass observed under saline conditions by halotolerant PGPR Under lower salinity levels, enhanced concentration of glycine betaine-like quaternary compounds, and increased shoot biomass Higher IAA, gibberellins (GA3), zeatin (Zt), proline, and malondialdehyde Increased chlorophyll content along with higher fresh and dry weight of shoots Higher colonization by different bacterial population, and ACC deaminase activity providing protection against salinity stress Production of proline and ACC deaminase and enhanced plant growth

References Bano and Fatima (2009)

Shukla et al. (2012)

Jha and Subramanian (2014)

Sahoo et al. (2014) Kang et al. (2014) Barnawal et al. (2014)

Palaniyandi et al. (2014)

Increased phosphate solubilization and production of siderophores under salt stress, hence promoting plant growth Ameliorate salinity stress through ACC deaminase activity

Ullah and Bano (2015)

Pseudomonas

Synthesis of phytohormone IAA aided in salinity stress

Egamberdieva et al. (2015)

Bacillus pumilus

Reduced uptake of toxic ions and enhanced antioxidant production Increase salinity tolerance due to ACC deaminase activity and plant growth promotion Under salinity conditions, increased nitrogen fixation, production of IAA, siderophores, solubilization of phosphate, and ACC deaminase activity promotes plant growth

Khan et al. (2016)

Pantoea sp. and Enterococcus Micrococcus yunnanensis, Planococcus rifietoensis, and Variovorax paradoxus

Suarez et al. (2015)

Panwar et al. (2016) Zhou et al. (2017)

(continued)

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Table 3.2 (continued) Crop Arabidopsis thaliana

3.1

PGPR strain Bacillus megaterium

Mode of action Adjustment and upregulation of jasmonic acid (JA) metabolism

References Erice et al. (2017)

Morphological Mechanisms

One of the mechanisms of the plant to deal with the conditions of stress is known as the escape; this is achieved by a reduced life span or growing season of the plant, thus allowing plants to reproduce before drying of the environment. The genotype of the crop and environment influences the crop duration and the ability to escape from climatic stress. For producing high seed yield, it is critical to match time of growth of plants to moisture content of the soil. It is found that drought escape occurs by successfully matching the phonological development with the time interval of moisture availability in the soil having shorter growing season and predominant terminal drought stress (Yang and Kim 2016; Khan et al. 2020). One of the influential traits for a crop adapting to stress conditions is the flowering time, especially under terminal drought and stress conditions. However, there exists a correlation between the duration of crop and yield under favorable conditions; thus, yield is affected if duration of crop is shortened below optimal level (Turner et al. 2001). Another mechanism is avoidance; it consists of the processes that reduce the loss of water from plant tissues due to stomatal transpiration along with maintaining uptake of water through an active and luxuriant root system. Under terminal environments, the main drought avoidance traits are the biomass, length, density, and depth of the roots that contribute to final yield. For absorbing water from considerable depths, a deep, thick, and active root system is considered essential (Abobatta 2019). It has been studied that plants usually reduce the number and area of leaves in response water stress conditions to limit water loss at the expense of loss of yield. The only source to absorb water from soil is roots; therefore, their proliferation, density, and size are the important response of plants under conditions of water stress. For example, plants with small leaves are inhabitants of dry environments and have the good ability to withstand drought although their rate of growth and biomass are relatively lower. Xerophytic plants protect themselves from excessive heat load through leaf pubescence. Hairy leaves are found to reduce rate of transpiration and leaf temperature. It is also reported that stem water content is declined to 4% and water potential to -0.25 MPa in drought-treated plants. The emerging stems of Hylocereus undatus were able to sustain their growth due to the active transportation of assimilates and associated reserves of liquid present in mature stems under conditions of stress (Wang et al. 2019). Under drought conditions, the ability of the plant to possess a thick and deep root system allowing access to deep underwater

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was considered as one of the important factor in determining resistance to water stress in upland rice. It is reported in several studies that the distribution and structure of roots compared to quantity determines the strategy for absorbing more water during the growing season of the crop. In many crops, for example, cotton, tea, onion, and food legumes, the tolerance to water stress conditions is increased by improved growth and functioning of the roots (Farooq et al. 2009; Tekle and Alemu 2016).

3.2

Physiological Mechanisms

The most important processes known under water stress conditions are the adjustment in osmotic pressure, osmoprotection, antioxidation, and an active defense system. The process of osmotic adjustment permits the cell to induce reduction in the osmotic potential. This in turn influences the gradient for influx of water and turgor pressure management. It has been found that tissue water status can be improved through osmotic adjustment or changes in the elasticity of cell wall. This helps in maintenance of physiological activity during prolonged conditions of water stress. Wild melon was found to survive severe drought conditions through maintaining its water content without causing wilting of leaves. This can be understood as the drought stress along with high light intensities led to the concentration of higher quantity of citrulline, glutamate, and arginine in higher concentrations in leaves of wild watermelon (Joshi et al. 2019). It is found that with the accumulation of solutes, there is a reduction in the osmotic potential of the cell that attracts water into the cell and aids in regulation of turgor pressure (Al-Yasi et al. 2020). In plants, the antioxidant defense mechanism consists of molecules having both enzymatic and nonenzymatic origin. These help in removal of reactive oxygen species, scavenging superoxide radicals, and hydrogen peroxide. In an important enzymatic reaction, superoxide dismutase catalyzes the dismutation of two superoxide molecules into oxygen and hydrogen peroxide; this also represents a first step in the process of removal of reactive oxygen species (Gill et al. 2015). Thus, a higher superoxide dismutase activity plays an essential part in developing tolerance to oxidative stress in plants. The maintenance of integrity of cell membrane and stability is an essential step toward developing tolerance to water stress conditions in plants. To evaluate drought tolerance, a physiological index using reciprocal of stability of cell membrane to cell membrane integrity is evaluated. Moreover, it is found to be genetic phenomenon as loci for its quantification trait have been mapped in water-deficient rice at various stages of growth (Oladosu et al. 2019). Leaf membranes of plants have been found to be very resistant to conditions of water stress as they are able to maintain polar lipid components and their stability under such conditions (Sebastiana et al. 2019). An adaptive strategy that has been reported from Brassicaceae under stress conditions is rhizogenesis, which is the formation of short, tuberized, hairless roots. These types of roots have been found to be stress-tolerant and upon

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rehydration are capable of producing a new functional root system (Farooq et al. 2009; Tekle and Alemu 2016).

3.3

Molecular Mechanisms

Under stress conditions, changes in the gene expression have been reported and these gene products function in tolerance to stress conditions. These responses may be activated by the stress conditions or from secondary stresses or as a response to an injury. Therefore, it can be said that the process of development of tolerance to drought is a complicated process involving the combined actions of a number of genes (Zia et al. 2021). The passive exchange of water across the membrane is facilitated and regulated by aquaporins. Aquaporins are a part of intrinsic membrane proteins and are abundantly present in the plasma membrane as well as in the membrane of vacuoles. They have been found to be abundantly expressed in the root system with regulated uptake of water from soil (Deshmukh et al. 2017). Stress protein synthesis have also been found to an essential response to stress conditions as these are water soluble and hence help in process of stress tolerance through hydration of cellular structures (Sharma and Dubey 2019). The abiotic stress signaling pathway involves the genes known by the name dehydration-responsive element-binding genes. By manipulating the expression of these genes, it was made possible to engineer the trait of stress tolerance in many transgenic plants. For example, effective improvement in drought tolerance was found in wheat after the inoculation of a novel gene of dehydration-responsive element-binding origin (Mehmood et al. 2020). Chaperones are a larger group of molecules belonging to the category of heat shock proteins. Heat shock proteins help in stabilizing other protein’s structure. Chaperones having low molecular weight are particularly produced under conditions of environmental stress. They have been reported to prevent denaturation of proteins under stress conditions as they participate in the unfolding of adenosine triphosphate-dependent protein. In fact, it is found that a number of chemical signals are produced under condition of stress that triggers an array of genes, resulting in different protein and metabolite synthesis, developing tolerance to stress conditions in plant species. Tolerance to salinity in plants is found to be affected by physiological mechanism, exposure to conditions of salinity, salt concentrations around roots, and interactions between soil and water along with microclimatic conditions. Decrease in the crop productivity is reported when concentration of salt is above the threshold level as high concentrations affect the growth of reproductive structures as well as translocation of nutrient reserves. Each species possesses a specific threshold value to salinity stress that leads to differences in salt tolerance among species. It is found that in glycophytes and halophytes, the adaptations to environmental conditions along with inherent generic traits help to regulate mechanisms of salt tolerance in them. Halophytes are known to posse’s high salinity tolerance as these plants grow in the saline conditions. They have been found to precipitate salts on their leaf

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surfaces as the accumulated salts are carried through xylem stream. Specialized glands called salt glands have been reported in many species; these are present over shoot surfaces and aid in excretion of salt which is then carried away with the help of water or wind (Flowers and Colmer 2015). Salinity stress causes ion toxicity and osmotic imbalance that hinders plant growth. Therefore, osmotic balance and ion homeostasis are the main factors that are considered during development of salinity tolerance in plants (Ilangumaran and Smith 2017). The role of salt overly sensitive (SOS) stress signaling pathway has been reported in the process of homeostasis and salt tolerance. The proteins SOS1, SOS2, and SOS3 are the part of SOS signaling pathway with SOS1 encoding plasma membrane Na+/H+ antiporter system. Tolerance to conditions of salinity is achieved by overexpression of this protein in the plants. SOS2 gene is activated by Ca+ signals elicited by salt stress and is found to encode for a serine/threonine kinase enzymes. The third protein SOS3 is a myristoylated Ca+ binding protein with a myristoylation site at its N-terminus. It also plays an essential part in producing salt tolerance in plants. The SOS2 and SOS3 protein interaction activates kinase that phosphorylates the SOS1 protein. The SOS1 is phosphorylated protein that promotes higher efflux of Na+ ions, leading to decreased Na+ toxic concentrations (Martínez-Atienza et al. 2007). During the period of stress, membranes along with their associated components play an important role in regulating ion concentration within the cytoplasm. A number of carrier proteins, protein channels, symporters, and antiporters regulate the process of transportation. A concentration of about 100 mM is maintained in the cytoplasm by plants to carry out different enzymatic activities. A major role is played by K+ ion in maintenance of turgor within the cell. Potassium ions are transported into the cell through K+ transporter and channels present in the membrane against the concentration gradient. Under conditions of low extracellular K+ concentration, K+ mediates a high-affinity K+ uptake mechanism. On the other hand, K+ channels carry out the low-affinity K+ uptake mechanisms. Thus, the concentration of K+ in the soil maintains the uptake mechanisms. It has been reported that the class 1HKT transporters in arabidopsis prevent excess accumulation of Na+ in its leaves, thus protecting from adverse impacts of salinity (Schroeder et al. 2013). The accumulation of a group of chemically diverse compatible solutes of organic origin or compatible osmolytes also functions in the protection of structure and osmotic balance maintenance within the cell through continuous influx of water (Slama et al. 2015). An important role is played by antioxidant mechanism in detoxifying reactive oxygen species (ROS) produced during conditions of stress. A couple of helicase proteins have been reported recently in maintaining photosynthesis as well as antioxidant machinery (Gill et al. 2013; Tuteja et al. 2013). ABA has been identified as a hormone which remains unaffected during conditions of water deficit. Its production is increased under water stress, and its accumulation can help in mitigating the adverse impacts of salinity on the process of photosynthesis, growth, and assimilate translocation. The relationship between salinity tolerance and ABA accumulation is partially because of concentration of K+ and Ca+ and of compatible solutes like proline and sugars that prevent Na+ and Cl- uptake. It is also found to regulate the expression of many salt- and water stress-tolerant responsive genes.

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Compounds such as salicylic acid (SA) and brassinosteroids (BR) have also been found to help in plant abiotic stress-tolerant phenomenon. Under conditions of stress, there was a rise in the activity of the salicylic acid biosynthetic enzyme along with increased endogenous levels of SA in rice seedling (Gupta and Huang 2014).

4 Role of Plant Growth-Promoting Rhizobacteria (PGPR) in Stress Management Plants live in close interaction with the bacterial community present in the soil. The essential part played by the plant growth-promoting microorganisms in plant growth, nutrition, and biocontrol has been well established. These PGPMs have been found to colonize both the rhizosphere and the endorhizosphere of plants with the ability to protect the plants from both biotic and abiotic stresses (Ma et al. 2019). The processes of nutrient acquisition, solubilization of potassium and phosphate, phytohormone synthesis, production of exopolysaccharides, and ACC deaminase induction are involved in the direct mechanism of plant growth promotion. Indirect mechanisms of plant growth promotion involve biological control against phytopathogens, or induced systematic resistance of plant cell wall, antimicrobial substances synthesis as well as production of proteins related to pathogens (Hashem et al. 2019).

4.1

Amelioration of Water Stress

Recently, the application of plant growth-promoting bacteria has been put into use along with genetic engineering to deal with the harmful effects of abiotic stress conditions on the growth and development of plants. These can be understood as follows:

4.1.1

ACC Deaminase Production

Different stages during plant growth promotion are controlled by variable concentration of ethylene. It is known that transcriptional and posttranscriptional factors control the biosynthesis of ethylene that is regulated by living and nonliving stresses (e.g., water and salinity stress). It is found to regulate homeostasis in plant corresponding to stress conditions resulting in declined growth and development of plants. Bacteria producing ACC deaminase can regulate ethylene level in plants by ACC into α-ketoglutarate + ammonia, therefore providing relief to stress conditions and enhancing plant growth (Vyas and Kaur 2019). For example, A. Piechaudii

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ARV8 was found to enhance fresh and dry weight of seedling L. Esculentum and C. annuum with reduction in ethylene production (Singh et al. 2018). It was reported that plants could be protected from inhibition of growth by ethylene induction only by wild type of ACC deaminase-producing bacteria regardless of their rhizobacterial or endophytic nature (Forni et al. 2017).

4.1.2

IAA Production

Plant growth-promoting bacteria have been known to synthesize phytohormones, namely IAA, GA, and ABA, which aid in stimulating plant growth and division and provide resistance ability to different ecological stresses (Ma et al. 2019). An increase in the plant growth aspects such as height, surface area, and the number of root tips along with uptake nutrients have been positively influenced through IAA and GA synthesis by different PGPB. Plant species such as S. lycopersicum, S. pimpinellifolium, B. napus, Helianthus annuus, P. vulgaris, and L. sativa have shown improved growth with PGPB application under stress conditions (Khan et al. 2017b). Abscisic acid production by PGPB can also help in microbe-induced tolerance to drought/salinity. The application of Phyllobacterium brassicacearum STM196 to Arabidopsis thaliana has helped in improving tolerance to osmotic stress by increasing the levels of ABA leading to declined rate of transpiration (Bresson et al. 2013). B. subtilis producing cytokinin when inoculated to the shoots of Platycladus orientalis increased the concentrations of ABA in its seedlings and stomatal conductance, therefore producing stress tolerance (Liu et al. 2013).

4.1.3

Exopolysaccharide Production

The interactions involved between microorganisms, roots, and rhizospheric soil of the plants are complex and dynamic in nature and have the ability to change the physiochemical and structural properties (Ma et al. 2016). Soil microorganisms are able to produce microaggregates/macroaggregates by binding soil particles with the extracellular polysaccharides produced by them. This enables plant roots, bacteria, and fungal hyphae to fit in the pores present in the microaggregates and thus help in the neutralization of macroaggregate (Naseem et al. 2018). The PGPB producing EPS have been found to enhance tolerance to salinity and drought stresses because they possess the ability to optimize structure of soil (Sandhya et al. 2010). It was demonstrated by Khan and Bano (2019) that consortium of PGPB has increased tolerance to drought stress and growth in plants by improving soil moisture content. A rhizosheath is formed by bacterial EPS, and it is also formed around the roots of the plant in the rhizospheric soil and protects them from desiccation for longer durations.

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Osmoregulation

Plants possess the ability to reduce permeability of membrane and enhance cellular conservation of water under water stress conditions. This osmoregulation was achieved mostly with the help of osmolyte accumulation. Osmolytes are generally produced under conditions of stress, and they do not interfere with the biochemical reactions taking place within the cell; therefore, they help in maintaining osmotic balance during drought stress (Slama et al. 2015). Different types of osmolytes produced in plants are proline, trehalose, and polyamines with proline having the capacity to accumulate in greater amounts under conditions of stress. It has the ability to adjust cytosolic acidity and hamper peroxidation of lipids by scavenging ROS directly, thus leading to membranes and proteins neutralization (Gill and Tuteja 2010). It was reported by Rodríguez-Salazar et al. (2009) that inoculating Azospirillum brasilense to Zea mays overexpressed the trehalose biosynthetic genes resulting in trehalose accumulation that provides tolerance to stress conditions. In mycorrhizal plants, higher levels of trehalose were found compared to nonmycorrhizal plants under stress conditions. (Garg and Pandey 2016). Polyamines are widely present in different stages of plant growth and development comprising of differentiation of cells, root length enhancement, development of floral parts, and maturation of fruit, senescence, programmed cell death, transcription, replication, and translation of DNA. They are amines of biological origin with aliphatic chain structure of nitrogen that exist in most of the organisms. It was found that inoculating Oryza plants with A. Brasilense Az39 producing cadaverine significantly increased the growth of its seedlings as well as root under drought conditions (Cassan et al. 2009). Another experiment showed that application to the mycorrhiza stimulated the putrescine and cadaverine production with increased activity of enzymes related to polyamine catabolism and putrescine synthases under conditions of stress. Thus, mycorrhiza can regulate drought tolerance in plants through polyamine metabolism modulation (Zhang et al. 2020).

4.2

Amelioration of Salinity Stress

A large proportion of the PGPB inhabiting the root surface lives in the present area between rhizodermal layers and root hairs. However, some microorganisms are not in physical contact with the roots. An integral part of rhizospheric signaling and communication events is maintained by root exudates in symbiotic interactions between plant and different bacteria. During rhizosphere colonization, signals for chemotaxis, exopolysaccharide (EPS) secretion, formation of biofilm, and quorum sensing are produced by phenols, organic acids, and flavonoids secreted by roots (Scharf et al. 2016). These are found to regulate tolerance to abiotic stresses in plants through different (direct and indirect) mechanisms. A number of growth-promoting bacteria have been investigated and identified for their essential role in alleviating

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plant–water interactions under salinity stress, and their mechanisms of amelioration are considered complicated, thus not well-studied and analyzed.

4.2.1

Osmotic Balance

The adaptations in hydraulic conductivity and transpiration rate by plant growthpromoting bacteria can regulate water potential and opening of stomata. For example, maize plants showed higher hydraulic conductivity when inoculated with Bacillus megaterium compared to uninoculated plants (Marulanda et al. 2010). They are found to stimulate accumulation of osmolytes and phytohormone signaling enabling plants to eliminate initial osmotic shock after salt stress. In an experiment, rice (Oryza sativa) was inoculated with salt-tolerant Bacillus amyloliquefaciens SN13 which showed higher tolerance to salinity conditions (200 mM NaCl) in hydroponics and soil conditions. SN13 inoculation modulated the genes playing essential part in mechanisms of osmotic and ionic stress response (Nautiyal et al. 2013). Some of the microorganisms can also induce metabolism and translocation of carbohydrate impacting source/sink relation, photosynthesis, rate of growth, and reallocation of biomass. It was found that B. aquimaris strains enhanced content of total soluble sugars and reducing sugars in the wheat upon inoculation under conditions of salinity (Upadhyay and Singh 2015). Increased accumulation of dry matter in pepper (Capsicum annuum) plants after 36 days of inoculation of Azospirillum brasilense and Pantoea dispersa was observed due to the higher conductance of stomata and photosynthesis under saline conditions without affecting the concentration of chlorophyll and photochemical functioning of photosystem II (del Amor and Cuadra-Crespo 2012). The absorption of compatible solutes by plant roots helps in regulating osmotic balance and avoiding oxidative damage at cellular level during conditions of stress (Ilangumaran and Smith 2017).

4.2.2

Ion Homeostasis

A number of cations are trapped in the exopolysaccharide (EPS) matrix by bacteria causing decline in the uptake of salts, as this alters the structure of root with capacious rhizosheaths along with regulating the expression of ion affinity transporters. The mineral nutrient exchange of micronutrients and macronutrients along with nutrient imbalance reduction caused by inflow of sodium and chlorine ions is influenced by PGPR in a positive manner. By reducing the concentration of Na+ and Cl- in leaves, PGPR help in regulating ion homeostasis and a high K+/Na+ ratio in stems of plants. They enhance removal of Na+ via roots and help in increasing the activity of K+ transporters of high affinity. Under saline conditions, inoculation of maize plants with Azotobacter strain C5 and C9 helped in enhancing the uptake of K+ and expulsion of Na+ (Rojas-Tapias et al. 2012).

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Phytohormone Signaling

Plant hormone status is regulated by soil bacteria through release of hormones of exogenous origin, metabolites, and enzymes that may contribute in providing tolerance to salt conditions. These are synthesized de novo in the plants in reciprocation of signaling interactions between plant and microorganisms under stress conditions (Dodd et al. 2010). It was found in an experiment that Bacillus amyloliquefaciens SQR9 enhanced tolerance to salinity conditions when inoculated on maize plants along with the higher content of chlorophyll and total soluble sugars, amelioration of the activity of peroxidase and catalase, and K+/Na+ ratio (Chen et al. 2016). Pseudomonas strains producing cytokinins elevated growth up to 52% in treated plats compared to untreated plants as well salinity stimulated dormancy of seeds of wheat plant (Egamberdieva et al. 2015). Ethylene is known to regulate adaptation of plants to stress conditions at the cost of growth and development of the plant. It is found that under stress conditions, there is an inhibition of auxin response factors leading to constrained plant growth. PGPR secreting 1-aminocyclopropane1-caroxylase (ACC) deaminase hampers the biosynthesis of ethylene in plants as this enzyme transforms ACC to α-ketobutyrate. Some of examples of PGPR showing salt tolerance through ACC deaminase activity are follows: Pseudomonas putida UW4 when inoculated to tomato (Solanum lycopersicum) seedlings enhanced growth of the shoot after 6 weeks under saline conditions with 90 mM NaCl concentration. A gene called TocGTPase of the apparatus related to chloroplast protein was found unregulated; its expression may have helped in translocation of proteins involved in the stress-tolerant mechanism (Yan et al. 2014). Thus, it can be said that plant growth-promoting rhizobacteria produce both indole-3-acetic acid and ACC deaminase which possess the ability to protect the plants from a variety of environmental stresses.

4.2.4

Extracellular Molecules

A number of extracellular secretions by PGPR such as proteins, hormones, volatiles, polyamines, and various other chemical compounds have been identified to modulate different signaling pathways and interactions that help in enhancement of plant growth and defense mechanisms against diseases along with inducing tolerance to stress conditions. There are some of the VOC (volatile organic compounds) released from PGPR that can help in regulating the plant growth, enhance shoot biomass, and modulate responses to stress conditions. For example, B. subtilis GB03 VOCs can help in regulation of Na+ homeostasis under conditions of salinity (Niu et al. 2016). The application of a bacteriocin isolated from Bacillus thuringiensis NEB 17 called thuricin 17 inhabiting soybean has differentially altered the proteome of Arabidopsis plants under salt stress (Ilangumaran and Smith 2017).

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5 Conclusions and Future Prospects Organic farming practices comprise an integral component which is the use of PGPR as inoculants for biofertilizer production and a source of biocontrol. As the concept of sustainable farming, environmental protection, and food security are now taken alongside with each other, it becomes evident to emphasis on methods that grant the exploitation of soil microbiota to the fullest. Recently, agriculture system is turning fragile due the rise in the abiotic stresses due to different ecological factors, such as drought and salinity. Plant- and soil-associated microbes have been found to cause reduction in these harmful impacts of stresses in a time-saving and cost-effective way. Damaged photosynthetic machinery, oxidative damage, and instability of membrane are the noticeable impacts of stresses on the plants. It is evident that ability of plants to withstand these stresses differs from species to species. Selfprotective responses triggered by these stresses occur at the leaf level to instantly protect the photosynthetic machinery against any kind of irreversible damaged being caused. The inhibition of reactive oxygen species through enzymatic and nonenzymatic systems, stability of cell membrane, and expressing stress-responsive genes, along with proteins is some of the different methods shown by plants under conditions of stress such as drought and salinity. Metabolic adjustments strongly help in adapting to drought conditions with polyphenols, lipophilic compounds, and a few metabolites of TCA cycle synthesis. Plants reaction to salinity conditions adapts a biphasic model, whereas the early phase shows a similar response as of drought conditions. Salinity stress in long term can stimulate ion toxicity. Significant decline in the growth of the plant is seen in the first phase along with closure of stomatal aperture that happens in response to reduction in water potential. The second phase is followed with accumulation of ions, such as Na+ affecting photosynthetic pigments as well as increasing oxidative stress. Thus, plant-associated microorganism plays an essential role in the ecosystem in not only providing adaptation to ecological stress condition but also influencing the process of evolution in plants under stress conditions. However, it is unclear that the different processes involved in the induction of relief to water stress are different from that involved under salinity stress situations. Further, detailed study is needed in clarifying the similarities and differences in induction of tolerance to stress conditions by microorganisms. It is also evident that the use of genetic engineering techniques and the process of plant breeding to develop stress-tolerant crop varieties are time-consuming and costly methods. But comparatively the use of microbial inoculants to enhance tolerance to different ecological conditions can prove a costeffective and eco-friendly option in shorter duration of time. Thus, a coordinated detailed future study is needed in this area, especially focusing on evaluation in field and application of these potential inoculants as biofertilizers in deficient soils.

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Chapter 4

Plant Growth-Promoting Microbes: The Potential Phosphorus Solubilizers in Soils of Arid Agro-Ecosystem R. S. Yadav, M. Kumar, P. Santra, H. M. Meena, and H. N. Meena

1 Introduction Agriculture is the key entrepreneur and plays an important role for nutritional and livelihood security especially in developing countries like India. Though in recent years, the paradigm shift is being witnessed in the agricultural practices using intensive chemical and fertilizers which leads to land degradation, desertification, and loss of biodiversity (Carten and Mathis 2014), continuous and indiscriminate use of chemicals poses a negative impact on agricultural ecosystems which badly impact the biodiversity, nutrients’ cycling, plant growth, and crop productivity (Calderon et al. 2017). Many agricultural interventions including agro-techniques, improved genetic materials, novel compounds for plant nutrition and protection, and microorganisms are being used for improvement of agricultural productivity in different agro-ecosystems. Soil is the fundamental component of an ecosystem act as living system which provides all the mineral nutrients for plant growth. Microorganisms present in the soils are being exploited for management of abiotic and biotic stress as well as plant growth-promoting activities. The arid ecosystem is typically characterized for heat stress and moisture deficit having multiple biotic and abiotic stresses. Generally, in this region, soils are devoid of nutrients and moisture for sustainable crop production. Among mineral nutrients, phosphorus (P) is an important plant nutrient largely present in unavailable form in most soils and the available P represents a very less fraction (95%) of the soil P exists in unavailable P pool which is further aggravated in arid agro-ecosystem where only formic acid in soils of arid agro-ecosystem (Gharu and Tarafdar 2004).

6.2

Organic P Mobilization by Phosphatases

Generally, soils of arid agro-ecosystem possess less amount of organic phosphates (80%) in these soils, and the dephosphorylation of these organic phosphates occurs through enzymatic catalysis. Phosphatases are the groups of enzymes which hydrolyzes the organic P compounds. It is well established that the different fungal strains varied significantly in their capacity for hydrolysis of Po compounds exist in the soil system (Yadav and Tarafdar 2003). Moreover, the extracellularly secreted enzymes (especially Phytase) catalyzed all the Po compounds present in the soil including phytic acid which were not hydrolyzed by intra-cellular bound phosphatases enzymes (Tarafdar et al. 2002). The co-inoculation of AMF (Glomus mosseae) and fungi Aspergillus fumigates in wheat significantly enhanced the P acquisition from phytate phosphorus (Tarafdar

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and Marschner 1995). Tarafdar and Gharu (2006) reported that application of chaetomium globosum as bio-inoculants in order to mobilize the native soil P in wheat and pearl millet crops and also increased the yield of these crops. Similarly, application of penicillium purpurogenum was also efficiently mobilized the native soil Po compounds for plant nutrition in arid production system (Yadav and Tarafdar 2011). On application of these fungal strains in the soil of arid region, variable response was observed for mobilization of native soil phosphorus with highest in labile fraction to least in stable P fractions and depleting both inorganic and organic P fractions using chemical extractants of differential strength (Tarafdar and Yadav 2011).

6.3

Molecular Aspects of Phosphate Solubilization Using PSM

The genes such as pqq, mps, phyA, napA, gcd, ppc, gabY, pqqABCDEF, and CipC, were identified in numerous microorganisms like species of Erwinia, Serratia, Pseudomonas, Aspergillus, Enterobacter, Escherichia, Penicillium, etc. (Rodriguez et al. 2000; Gong and Tang 2015). Generally, these genes control the action of phosphate dissolution by activities of gluconic acid (Kumar and Shastri 2017), higher phosphatases activity (Tarafdar et al. 2002), organic acids (Lu et al. 2012), and assimilation of P in agricultural crops (Ahmed et al. 2021). Further, mineral phosphate-solubilizing genes (mps and gabY) were also identified in Erwinia herbicola and Burkholderia cepacia for gluconic acid production (Rodriguez et al. 2000; Zhao et al. 2014). Cloning of pqq genes in other soil microorganisms can generate multiple traits for interest like in rhizobium for fixation of N and solubilization of P in the same microbe (Sharma et al. 2013a). Shulse et al. (2019) articulate the phytase gene using different rhizospheric bacterial species and engineered the novel organisms for enhanced released of Pi from phytate phosphorus.

7 Factors Affecting Phosphate Solubilization Potential of PSM Various edaphic, climatic, and management factors significantly affect the phosphate solubilization potential of PSM. The interactions of these factors like ecological and climatic conditions, soil properties and fertility status, microbial diversity and density, diversity of vegetations and plant types, land use system and agronomic practices, etc., govern the microbial proliferation, their functioning, and solubilization of insoluble phosphates. For example, the soils having optimum aeration and in the tropical climate are more vulnerable for solubilization of insoluble phosphates than the soils under wet and cooler environment. Management practices like

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application of soil amendments, organic matter and composts, cropping system, crop rotation, soil pH, etc., significantly affect the phosphate solubilization in the soil system. Compatibility with native microbes, congenial conditions to support microbial proliferation, soil, and rhizospheric effects on microbial functioning, etc., are some key factors that affect the effectiveness of microbial-led P solubilization in these soils. The PSM obtained from soils facing multiple stresses (abiotic and biotic) is to be more robust and vital than the microbes recovered from optimum condition in terms of both secretion of biochemicals and for mobilization of insoluble native soil phosphates for plant nutrition (Zhu et al. 2011). Soil pH, organic carbon content, and microbial diversity are the key factors affecting the mechanisms for solubilization and mobilization of insoluble phosphates present in the soil system (Chhonkar and Tarafdar 1984). The optimum soil pH range for highest bioavailability of P is 6–7.5 in most soils. The optimal temperature range for maximum phosphorus solubilization using PSM varied widely ranged from 20 to 30 °C in normal climatic conditions (Johri et al. 1999) while 10 and 45 °C temperatures were reported as extreme cool and hot for solubilization of phosphates in desert soils (Nautiyal et al. 2000). The priming of rhizosphere soil using Pi mineralized the soil phytates for P nutrition of plants using bacterial species (Zhang et al. 2014). Zhu et al. (2011) reported that the metabolites produced in the soil system and their kinetics determine the solubilization potential of insoluble phosphates mediated by PSM.

8 Future Research Priorities Substantial depletion of phosphate rocks reserves worldwide, very poor recovery of fertilizer used in most agricultural production systems, and ever-increasing depositions of residual soil P are the key concerns which signify the current status of P cycle in global food production systems. The recycling of residual soil P is of utmost significance not only for plant nutrition point of view but also as an environmental concern. In this regard, management of natural resources like soil, water, plant, and microorganisms is important for enhanced availability of native soil P. The characterization of soil fertility status considering the availability potential like available, readily available, sparingly available, and unavailable P pools needs to be included in fertilizer management. Further the spatial and temporal appraisal of the residual soil P in different agro-ecosystems as well as in agricultural production systems entails the status and recycling potential for residual soil P for plant nutrition which may help to curtail the uncontrolled and inefficient use of P fertilizer applications. The efficient and effective microbial consortium has to be worked out specifically with respect to agro-ecosystems, cropping systems, and crop species for exploitation of residual soil P resources for plant nutrition. Picking the efficient PSM possessing the multiple traits for promotion of plant growth, compatibility with native microbial flora, and ecosystem, longer shelf life, etc., are some key component for development of bio-fertilizers. The microbial isolates having diverse ecological niches need to be isolated and identified for their exploration and metabolism for improving

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phosphate-solubilizing capability. The molecular characterization of soil systems as well as the microbes having potential for solubilization and mobilization of unavailable soil P resources needs to be strengthened. Metagenomic approach has to be used for modifications in PSM as well as the other microorganisms for enhanced phosphate solubilization efficiency and/or for multiple traits like nitrogen fixation, phosphate solubilization, plant defense, etc. The phosphate transporters of plant origin should be identified for the mechanisms for P uptake. Efforts should be made to identify the molecular mechanisms for AMF symbiosis and also strengthen the research to identify the suitable culture method for multiplication of AMF which are still unknown. Research should also focus on nano-technological applications for mobilization of insoluble P, influx and efflux studies in plants, molecular assessment of rhizosphere induced P mobilization, etc.

9 Conclusion Microbes are vital for plant and soil health having crucial role in various mechanisms including nutrient supply, growth, and protection of plants which are being governed by specific microorganisms. P is the second most important nutrient in crop production and very less amount of the total P ( 0.05) in sprayed, bee vectored with T. harzianum and control treatment than in farmer’s practice treatment (Macharia et al. 2020). This is because of easy delivery spores of Trichoderma spp., which parasitize the pathogen. Till now many scientists from the different parts of the world have explored the use of different non-pathogenic microorganisms for management of plant diseases (Sabalpara and Mahatma 2019). Many products containing different microorganism are available for the direct use. However, preparation of a commercial product of any PGPR or biological control organism with uniform quality and their field application is still a challenge job. Interestingly, the different antagonistic microbes have wide ranges irrespective of crop. Bacillus subtilis is another candidate microbial pesticide which effectively manages sigatoka of banana (Mycosphaerella musicola), bacterial leaf spot of tomato (Xanthomonas sp.), wilt (Fusarium sacchari), red rot (Colletotrichum falcatum) of sugarcane, etc. Several species of Pseudomonas and Bacillus have been identified as an effective bio control agent against Verticillium dahliae Kleb. Non-pathogenic Fusarium strains, entomopathogenic fungi such as Metarhizium brunneum and Beauveria bassiana or AM fungi, have been found to lessen both the severity of verticillium wilt in olive and its inoculum density (Montes et al. 2021). Ampelomyces quisqualis is another anamorphic super parasite found to suppress several genera of powdery mildew, i.e. Oidium, Erysiphe, Sphaerotheca, Podosphaera, Uncinula and Leveillula (Sztejnberg et al. 1989; Falk et al. 1995a, b). This super parasite can even survive without food as pycnidia and take nutrients from the spore of powdery mildew. Several commercial product containing spores of Ampelomyces quisqualis is available in the market. Powdery mildew pathogen of cucumber (Sphaerotheca fuliginea) found to parasitize by a Tilletiopsis sp. Perpetuation of apple scab pathogen, Venturia inaequalis, takes place by the production of ascospores in the fallen leaves and subsequently through the conidia on growing leaves (Carisse et al. 2000). Chaetomium globosum and Athelia bombacina when applied on the fallen foliage or growing shoot can suppress the

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pathogen. Chaetomium sp. produces certain antibiotic substances which easily diffuse and inhibit the multiplication and infection of this pathogen (Bouderau and Andrews 1987). There are many limitations of biological management of airborne diseases. Most of the antagonistic microbes applied on the foliage fail to survive and multiply on it because of lack of nutrients. The efficiency of the biological control increases with the amendments of stickers and other components improving physical properties of the preparation. Consortia of biological preparation containing effective strain of cellulose-degrading fungi, plant growth stimulant and biological control organism show better performance (Soytong and Ratanacherdchai 2005). Nectria inventa have been found to parasitize many plants pathogenic fungi. N. inventa easily colonize Alternaria brassicae, Pleospora sp. and Trichothecium roseum. Hyphae of mycoparasitic N. inventa grew towards the mycelium of susceptible fungi, form appressorium and coil the hyphae. After sometime, cytoplasm of the host cell becomes granular and wound plug-like zones can be seen below the point of contact. Gradually, vacuoles are seen in the cytoplasm, and in advance stage, the entire host cell becomes empty (Tsuneda and Skoropad 1980). Natural parasitism of Tuberculina maxima, commonly known as purple mould, has been observed on white pine blister rust fungus Cronartium ribicola. Tuberculina sp. targets the aecia and pycnia and reduces the inoculums potential of the pathogenic fungi. Similarly, parasitic fungi Darluca filum and Verticillium lecanii frequently found in the pustules of carnation rust Uromyces caryophyllinus, groundnut rust Puccinia arachidis and brown rust of wheat Puccinia recondite (Spencer and Parasitic 1981). Other noteworthy examples of biological control and mycoparasitism are Cladosporium uredinicola on Puccinia violae (Traquair et al. 1984), Alternaria alternata on Puccinia striiformis (Zheng et al. 2017). However, these hyper parasites do not have much practical and commercial application.

9.2

Postharvest Diseases

Deterioration of the fruits and vegetables between the harvesting and reaching to the mouth of consumers is most serious problem. Generally, consumers do not prefer to use any chemical for the product they directly consume. Therefore, need to search most compatible biological agent for the management of post-harvest disease is gaining much significance. Spraying the inoculums of antagonistic microbes or dipping the harvested fruit or vegetables in the inoculum solution may offer an easy and economic way of reducing post-harvest losses. Citrus green mould caused by Penicillium digitatum can be considerably managed by the application of antagonistic yeasts Candida saitoana or the fungal antagonist Trichoderma viride (Agrios 2005). Lactic acid producing bacteria (Lactobacillus plantarum, L. paracasei and L. pentosus) when grown on the surface of fruits produce lactic acids as well many other metabolites, viz., organic acids, fatty acids and antifungal peptides which act as natural disinfectant of many post-harvest rot causing microbes and enhance shelf life

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of grapes, cucumber, chilli, papaya, mango and many other perishable vegetables and fruits (Strom et al. 2002; Marín et al. 2019; Barrios et al. 2019). Natural waxy coating on the fruit prevent colonisation of these natural antagonistic microorganisms. Therefore, it is least effective in the fruits having natural wax layer.

10

Conclusion

Plant growth-promoting microorganism (PGPM), as the name indicates, are bacteria that release special metabolites during their own growth which promotes the healthy growth of the plants and ultimately increases yield. Significance of these is increasing rapidly in an agricultural ecosystem which is managed with a purpose, usually to produce crops or animal products. There are four main ecosystem services, viz., (1) provisioning, (2) regulating (3) cultural and (4) supporting services. The current trends in agriculture are focused on maximizing provisioning services (i.e. food and fuel) at the expense of regulating, cultural and supporting services of the ecosystem. Therefore, we intentionally change biotic and abiotic environment for the economic return. In the second half of the twentieth century, use of chemicals in agriculture has increased exponentially. Chemicals have increased production and productivity; however, it has irreversibly damaged our ecosystem below- and aboveground. Majority of microbes related to the agriculture found below the ground. Sustainability in ecosystem is not achieved without the conservation of mass and energy which exists in the natural ecosystem. Law of conservation of energy emphasizes that energy can neither be created nor destroyed in a closed system. We only convert it from one form of energy to another. This reveals that a system always has the same amount of total energy, unless it is added from the outside. In ecosystem, the chemical (CO2 and H2O) energy and physical (sunlight) energy are converted into the biological (carbohydrate) energy in a process called photosynthesis. For any tropic level, the percentage of consumed energy transmitted onwards cannot exceed the percentage assimilated. The assimilation percentage in most organism range 20–40%, but this varies with the nature and abundance of the food supply. This leads to generation of waste which along with the dead matters is broken down by decomposers and the nutrients are recycled into the ecosystem. Based on this principle, different nutrient cycles, viz., carbon, nitrogen and phosphorus, have been proposed. Seventeen nutrients or elements (C, H, O, N, P, K, Ca, Mg, S, Cl, Fe, Zn, Mn, B, Cu, Mo and Ni) are essential for the plants. Evolution of life is intimately linked to the environment. If these nutrients would not be present in abundance in the environment, these would not have been essential for plants. However, they are not available in the form that plants need. If this would have been present in the available form, probably, it would have been lost from the atmosphere. Our initial agricultural practices were energy conserving, however, soon through intensive agriculture practices; we have made it energy exhaustive. Due to poor understanding of nutrient cycles, we could not manage nutrients efficiently in the agricultural ecosystem. Therefore, to compensate the loss, we keep on adding nutrients. With the development of synthetic fertilizers in the

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beginning of twentieth century, we became over dependent of chemicals. PGPR play enormous roles in carbon and other nutrient cycling in the food web. Nitrogen fixing microorganisms, different nitrogen fixing microorganisms (symbiotic nitrogen fixers, non-symbiotic nitrogen and associative symbiotic nitrogen fixers), phosphate solubilizing microorganisms (PSM), phosphate absorbers, potash mobilizers, zinc solubilizers, plant growth-promoting rhizobacteria (PGPR), biocontrol agents, etc., play important role in ecosystem services.

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Chapter 6

Plant Growth-Promoting Microorganisms: An Option for Drought and Salinity Management in Arid Agriculture Kamlesh K. Meena, Utkarsh M. Bitla, Ajay M. Sorty, M. Saritha, Shrvan Kumar, and Praveen Kumar

1 Introduction Abiotic stresses including salinity and drought have emerged as the most threatening stresses to the agricultural productivity, food security, and soil health in long term. A major cause of the constantly increasing abiotic stress has been linked to the global climate change-induced erratic precipitation, temperature extremities, soil salinization due to excessive groundwater utilization, and leaching of natural stones (Wania et al. 2016). Cumulatively, these stressors are tremendously pressurizing the existing agricultural land to ensure a continuous food supply for ever-increasing global population. Relieving the production-pressure on existing land under cultivation is possible through reclamation of the degraded land (Gupta and Huang 2014). In this context, several strategies have been proposed ranging from the use of plants (phytoremediation), mechanical technologies such as subsurface drainage for reducing soil salinity, adoption of precision technology interventions under drought condition, and microbial interventions for climate smart agriculture. Owing to their cost-efficiency, eco-friendly nature, and ease-of-application, the microbial strategies are of significant interest. Microbial inoculants consisting of plant-associative microbes are applied under stress conditions, where they perform a variety of plant beneficial activities to ensure a sustainable growth and improvement of plant productivity under stress environments (Meena et al. 2017). Plant-beneficial microbes—generally termed as plant growth-promoting microbes (PGPM) are well documented for their unique metabolic capabilities—especially relating to the production of plant growth-inducing substances such as indole-3-acetic acid,

K. K. Meena (*) · M. Saritha · S. Kumar · P. Kumar ICAR-Central Arid Zone Research Institute, Jodhpur, India U. M. Bitla · A. M. Sorty ICAR-National Institute of Abiotic Stress Management, Baramati, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_6

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gibberellins, cytokinins, siderophores for iron sequestration, and biocontrol of phytopathogens, organic acids for solubilization of essential nutrients, biosynthesis of important enzymes such as ACC deaminase that lowers the levels of increasingly accumulating ethylene under stress situations in plants (Hakim et al. 2021). PGPM also produce a variety of secondary metabolites including phenolic as well as volatile organic compounds that act as messengers/signals for inducing a systemic stress tolerance in plants. Further, some of the PGPR are also capable of producing carbohydrate-rich exopolysaccharides that exhibit a multifaceted role in the microecosystem of plant rhizosphere (Gupta et al. 2019). Microbial exopolysaccharides primarily act as carbon reserves, further they also exhibit exceptionally high-water binding capacity that enables formation of a gel-matrix which also exerts a sheltering effect for the surrounding microbes (Vurukonda et al. 2016). Exopolysaccharides are also capable of forming a film-like structure on soil as well as plant (especially root) surfaces and act as an attachment factor for the colonizing microbes, which ultimately promotes the development of a biofilm. Under relatively prolonged drought spans, the water holding ability and soil aggregation promoted by microbial exopolysaccharides play a crucial role in maintaining moisture supply within the rhizosphere microhabitat (Ansari et al. 2019). Similarly, fungal symbionts of plants also perform a range of beneficial activities relating to growth, development, and stress tolerance. Arbuscular mycorrhizal fungi (AMF) form active associations with plants and extend their hyphae in the surrounding soil habitat and conduct the transfer of nutrients and moisture to the host, thus indirectly enabling plants to cover a larger area for uptake of nutrients and moisture (Ruiz-Lozano et al. 2016). AMF are also well known for their capability to solubilize inorganic phosphate and make available to the plants through the hyphal transport (Battini et al. 2017). Recently, co-operative associations of AMF and PGPM have been demonstrated under a variety of environmental conditions including biotic and abiotic stresses (Hashem et al. 2016). Thus, adoption of AMF-PGPM co-inoculation strategy for enhancing abiotic stress tolerance in plants is being seriously considered, particularly under drought and salinity stress conditions. Exploration of the yet-curtained diversity of both the AMF and PGPM from naturally stressed habitats is also being seriously attended to make available more potent strains of PGPM that can be more efficiently implemented for crop-enhancement efforts in climate-smart agriculture.

2 Plant Growth-Promoting Microorganisms (PGPM) PGPM inoculation in crop is well practiced by agriculturalists to increase crop yield and productivity but traditional microbial biofertilizers are not capable to improve crop growth in changing climatic condition. PGPM develop active associations with plants and enhance plant growth even under adverse environmental conditions such as limiting moisture, salinity, nutrient deficiency, etc.; thus, making this class of microbial communities critically important for maintaining plant health under

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normal as well as challenging environmental circumstances (Meena et al. 2017; Sorty et al. 2016). Increasing knowledge on plant-microbe interactions and their multidimensional capabilities to improve plant development under different sets of environmental conditions, encourage the application of these PGPM as plant growth agents. Further, the beneficial host microbe interactions also promote active incorporation of microbial inputs to improve crop yields, as well as components of ecosystem mending approaches (Bashan et al. 2012). PGPM that inhabit the rhizosphere and phyllosphere alleviate the impacts of abiotic stresses on plants by different mechanisms, which mainly include modulations at physiological levels. Consequently, plant responses can also be expected in terms of metabolic adjustments, antioxidant fortifications, and improved nutritional status. These effects could be typically due to higher microbial colonization and subsequent activity due to bacterial exopolysaccharides (EPS), and improved plant growth and defense mechanisms. Plant rhizosphere is considered as one of the most intricate ecosystems on the earth habituating loads of microbial communities whose content may get altered as a consequence of plant-age and environmental circumstances (Singhal et al. 2016). Within the rhizosphere region, plant roots secrete a variety of secondary metabolites that work as chemo-attractants for soil microbes (Bitla et al. 2017; Pandey et al. 2017). The plant secretions from the rhizosphere serve as signaling factors that have been thought to govern the highly selective colonization of beneficial microbes. Further, nutritionally rich organic exudations also serve as an excellent source of carbon and energy for the freshly colonizing microbial population. The vast area of the leaf surface is protected with waxy cuticles, which efficiently block water transpiration, nutrient discharge, and gas interchange. Phyllosphere microorganisms live on the leaf surface (epiphytic) and survive on trace quantities of available water and nutrients within that habitat. These epiphytes are typically pink-pigmented methylotrophic that are well known for their capability of production of plant growth hormones and alleviation of abiotic stress (es) in plant (Meena et al. 2012, 2020). However, the abundance, activities, and assortment of rhizosphere microbiome appear to be far more superior to the phyllosphere (Laksmanan et al. 2014). This is mainly because of favorable conditions available for rootassociated microbes like root exudates and sloughed off cells comprising nutrientrich combinations (Daguerre et al. 2017). Chelation and acidification of soil by PGPM also enhance the availability of mineral elements like Mn, Cu, Fe, Zn, etc., to plants (Etesami et al. 2014). Association of AM fungi with a vast diversity of terrestrial plants is well documented, with the increasing evidence of AMF-plant association in a variety of terrestrial habitats. AMF-induced abiotic stress tolerance is also emphasized; however, so far, the predominantly documented role of AMF has been linked to the increased nutrient and moisture availability within the rhizosphere zone. In stressful situations, AMF-mediated host aquaporins (channels of water and stress signals) schedule discrete arrays leading to upregulation of cascades responsible to boost water and nutrient uptake, and a subsequent downregulation of the excretory cascades to limit water loss (Sharma et al. 2021). Plant-associated mycorrhizae alleviate

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abiotic stresses including salt, drought, and heavy metals. Besides aquaporins, it sets eminence on polyamines, the primeval stress-response molecules that significantly modulate plant-physiology and metabolism and induce beneficial responses (Sharma et al. 2021). AMF affect plant diversity and development, and participate in determining the ecosystem reliability and sustainability (van der Heijden et al. 1998, 2006). Plant secrets strigolactones through the root exudate which is an important signaling molecule that principally controls primary development of root and root hair. Presence of strigolactones have been validated in root exudates of both monocotyledonous and dicotyledonous plants and have been shown to be involved in mutualistic communications with AMF in the rhizosphere (Breuillin et al. 2010). Under water-deficit conditions, AMF confer tolerance to the host plant through a range of biochemical and physiological cascades. Primarily, they improve water availability by aiding as stretched plant roots, improving photosynthetic efficacy, osmoregulation, strengthening antioxidant metabolism, upholding nutrients, ions, and ensuring an optimal redox homeostasis (Evelin et al. 2019). AMF also play an important role in mitigation of salinity stress in plants. Navarro et al. (2014) have shown that inoculation with AM fungi increases plant growth under salt stress condition. They hinder the uptake of Na or Cl in citrus plants under saline conditions, and also reduce oxidative stress through deteriorating membrane lipid peroxidation (Abdel Latef and Chaoxing 2014).

3 PGPM Interactions Under Drought Stress Plant-associated microbes execute several strategies to alleviate harmful influence of drought on plant and soil (Table 6.1). Irrespective of the water content within the soil regime, the associative microbes—mainly AM fungi deliver nutrients to the plants and also ensure a healthier environmental condition for the constant growth. A major part of beneficial interaction of associative microbes is attributed to their unique capability to biosynthesize cytokinins, indole-3-acetic acid, and abscisic acid like phytohormones, apart from the exopolysaccharides, volatile organic compounds, and enzymes like ACC deaminase, discussed in previous sections (Khan et al. 2020a, b; Kannepalli et al. 2021; Fallah et al. 2021; Najafi et al. 2021; Kour and Sayyed 2019; Ilyas et al. 2020). Plant hormones synthesized by PGPM are capable to enhance plant growth and development even under stress conditions. IAA is a central signaling molecule that controls the vascular tissue diversity, adventitious and adjacent root disparity, cell division, and shoot development under drought stress (Goswami et al. 2015; Bitla et al. 2017). Under drought conditions, ABA works as a crucial growth regulator. PGPM inoculated plants exhibit enhanced concentration of ABA (Abscisic acid) which regulates physiological responses that improve drought tolerance. ABA mitigates drought stress via eliciting transcription of drought-associated genes and root hydraulic conductivity (Daszkowska-Golec 2016). Inoculation of IAA and SA (Salicylic acid) producing Bacillus sp. and

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Table 6.1 Case reports on microbe-mediated mitigation of abiotic stresses in plants Microorganism H. diazotrophicus

Crop H. vulgare

Mitigate effect of stress Salinity

Streptomyces sp. GMKU 336

Oryza sativa L.

Salinity

P. fluorescens

Maize

Salinity

P. vancouverensis

Solanum lycopersicum Solanum lycopersicum L. lycopersicum

Cold

Black gram

Drought

Glomus mosseae A. brasilense

Cold Drought

O. pseudogrignonense RJ12, Pseudomonas sp. RJ15, B. subtilis RJ46 Rhizophagus intraradices Funneliformis mosseae Funneliformis geosporum Glomus versiforme

Triticum aestivum

Drought

Zea mays L.

Drought

Funneliformis mosseae Rhizophagus intraradices Paecilomyces formosus

Robinia pseudoacaciaL. Glycine max L.

Lead (Pb)

Bacillus aquimaris

Wheat

Heavy metals (Ni, Cd, and Al), Salinity

Curtobacterium albidum strain SRV4

Wheat

Salinity

Bacillus cereus SA1

Soybean

Heat

Bacillus cereus

Solanum lycopersicum L. Wheat

Heat

B. amyloliquefaciens 5113 and A. brasilense NO40

Heat

Reference Suarez et al. (2015) Jaemsaeng et al. (2018) Cheng et al. (2007) Subramanian et al. (2016) Abdel Latef and Chaoxing (2011) Romero et al. (2014) Saikia et al. (2018) Mathur et al. (2018) Begum et al. (2019) Yang et al. (2015) Bilal et al. (2019) Upadhyay and Singh (2015) Vimal et al. (2019) Khan et al. (2020a, b) Mukhtar et al. (2020) El-Daim et al. (2014)

Enterobacter sp. in Triticum aestivum and Zea mays enhances drought tolerance and plant growth (Jochum et al. 2020). The phyllosphere microbial community is also known to produce regulatory biomolecules like SA and IAA which induce salinity tolerance, for instance, in wheat (Meena et al. 2020). In addition to the phytohormones, phyllosphere microbes also synthesize osmoprotectants, vitamin B12, and polysaccharides into their environments (Bustillos-Cristales et al. 2017). Drought and salinity stress reduce the water availability to phyllosphere microbes. Under these conditions, the mycorrhizosphere formed by roots and AMF mycelium in soil-microaggregates

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effectively improves water and nutrient uptake due to their higher spread (Smith and Smith 2012).

3.1

PGPM Interactions Under Salinity Stress

Some of the microbial communities associated with plant exposed to salinity stress adapt themselves to unusually high salt concentrations, and acquire exceptional capabilities of nutrient uptake and retain routine metabolic processes while simultaneously, promoting plant growth and development (Sagar et al. 2020, 2022; Kapadia et al. 2021) (Table 6.1). A major role of PGPR microbes is in preserving ion homeostasis, osmotic stability, and turgor pressure to battle with the salt-induced toxicity in plants (Obledo et al. 2003). Bhise et al. (2017) and Kusale et al. (2021a, b) observed that synthesis of ACC deaminase and decreased ethylene content are the key causes for PGPB-mediated plant sustenance under salinity stress. Some of the salt-tolerant bacteria produce EPS that play important role in mitigating salt stress (Upadhyay et al. 2011). EPS endorse bacterial existence due to improving water holding capability and also control the diffusion of organic carbon bases. Bacteria also synthesize high molecular weight lipopolysaccharide–protein and polysaccharide–lipid complexes that can enhance drought and salinity tolerance (Vurukonda et al. 2016). PGPM secrete exopolysaccharides in soil in the form of mucus material that integrate with soil particles through hydrogen bonding, Van-derWaals forces, cation bonds, and anion adsorption phenomenon (Ansari et al. 2019). Therefore, microbially originated slime material develops a defensive cover around soil aggregates, and when plants are inoculated with EPS-producing microorganisms, they establish an enhanced resistance against salinity. Secretion of EPS by soil microbes surrounding the roots also rises plants’ water potential and uptake of nutrients (Naseem and Bano 2014). Halotolerant bacteria isolated from halophytic weed Psoralea corylifolia L. are able to solubilize phosphate, fix atmospheric nitrogen, and produce siderophores, IAA under saline stress (Sorty et al. 2016). This proficiency of PGPB under high salinity can be correlated to the capability of PGPM to synthesize a variety of bioactive compounds, e.g., organic acids responsible for phosphate solubilization, also 2-ketogluconic, acetic, gluconic, oxalic, succinic, citric, and malic acids that are important for decreasing alkaline pH in saline soils (Zaidi et al. 2009; Wei et al. 2018). Application of salt-tolerant bacteria as direct inoculant, or as a gene resource for the development of transgenic plants was helpful in revealing plant stress tolerance mechanisms. For instance, the codA gene from Arthrobacter globiformis encoding choline oxidase when expressed in tomato, induced synthesis of glycine betaine and improved plant salt tolerance capability (Goel et al. 2011).

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3.2

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PGPM Interactions Under Other Abiotic Stress(es)

PGPM maintain availability and transport of water and nutrients in plants under high temperature environments (Table 6.1), while thermotolerant phosphate solubilizing bacteria work as biostimulants and contribute to the phosphorous cycle (Paulucci et al. 2015). AMF Glomus mosseae and Glomus intraradices increase level of P, K, Zn, and Mn in Pistachio plants under drought conditions (Bagheri et al. 2012). Pepper plants inoculated with a gibberellin-producing PGPR strain were shown to have enhanced synthesis of GA and ABA, while the same plants regulated low levels of jasmonate and salicylate. This modification in phytohormone and plant growth regulators causes proliferation in plant growth under low-temperature stress and PGPR associated with plants growing in low temperature have effective biofertilizer capacity in low-temperature conditions (Kang and So 2016). Plant growthpromoting psychrotolerant bacteria Arthrobacter nicotianae, Flavimonas, Flavobacterium, Massilia, Pedobacter, and Pseudomonas also have been shown to improve germination and growth, and enhance tolerance to cold stress in Solanum lycopersicum Mill (Meena et al. 2015; Subramanian et al. 2016). AMF Glomus etunicatum alleviates impact of low temperature in maize plants through enhanced water conservation (WC) and water use efficiency (WUE) which also has been thought to play a subsidiary role in enhancing nutrient uptake, osmotic adjustment, the capability of gas exchange, and the efficacy of photochemistry of PSII (Zhu et al. 2010). Moreover, although the underpinning mechanisms are less understood, AMF can also contribute beneficial effects under acidic soil conditions (Rohyadi 2008; Suri et al. 2011). Some of the PGPM are able to survive under acidic and alkaline soil and promote plant growth; Sinorhizobium meliloti LPU63 shows ability to nodulate under low PH and enhances growth in Alfalfa (Segundo et al. 1999). Bacillus sp. NBRI YN4.4 inoculated in corn enhanced chlorophyll and sugar content and reduced proline level in alkaline soil condition (Dixit et al. 2020). Inoculation of Bacillus simplex promoted a substantial reduction in pH of the wheat rhizosphere and improved plant growth and P content within the roots (Hansen et al. 2020).

4 Recent Advancements in PGPM Interactions Under Abiotic Stress and Future Outlook Plant–PGPM interactions are pointers of plant health, productivity, as well as soil fertility. Increasing knowledge on role of plant-associative microorganisms in plant growth promotion under abiotic stress conditions has opened new avenues in the area of beneficial plant-microbe interactions under abiotic stress conditions. Finer insights to the mechanisms governing plant-microbe interactions under abiotic stress conditions are now possible with the advent of omic strategies such as metabolomics (Meena et al. 2017; Sharma et al. 2020; Hong et al. 2021), genomics (Kumar et al.

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2020; Perrone and Martinelli 2020; Sharma et al. 2020), and transcriptomics (Rigo et al. 2019; Shekhawat et al. 2021). Metabolomic studies highlight the role of different bio-active molecules synthesized in plants in response to stresses and microbial associations. Besides the phytohormones and organic acids, microorganisms secrete secondary metabolites like harzianolide which enhances plant growth (Vinale et al. 2008). PGPM also produce siderophores which are low-molecular weight molecules with high Fe affinity that make iron available to the plants. Plants, on the other hand, accumulate metabolites like trehalose, glycine betaine, IAA, etc. to combat stresses as well as in response to microbial associations. A recent investigation of polar metabolite and lipid fluctuations during early development of Brachypodium demonstrated that PGPB initially elicited a defense response in roots while at later stages, reduced the stress caused by phosphorus deficiency, and improved root development (Schillaci et al. 2021). Recent studies have shown that the plants and their associated microorganisms have co-evolved and this “holobiont” shapes the plant fitness (Hassani et al. 2018). Next-Generation Sequencing techniques conducted to decipher the bacterial communities that support plant growth have demonstrated largely the presence of Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, and Acidobacteria in plant-related ecosystems (Sharma et al. 2020). Recently, Vílchez et al. (2020) reported that active DNA demethylation is needed for plant root secretion of myo-inositol involved in mutualism between plants and beneficial bacteria, thereby suggesting the involvement of epigenetic regulatory mechanisms in plant-microbe interactions. A research into the Stenotrophomonas maltophilia-mediated tolerance to nitrogen starvation conditions in Arachis hypogaea revealed an overexpression of the AhCytb6 gene (coding for Cytochrome B6f Complex) that maintained high photosynthesis and protected plants from reactive oxygen species build up during stress conditions (Alexander et al. 2021). In the same study, microarray-based whole-transcript expression of host plants showed that nearly 8704 genes were significantly expressed under nitrogen starvation and 24,409 genes were differentially expressed under salt stress conditions. Such transcriptome profiling techniques have also revealed that the root endophyte Enterobacter sp. induces thermotolerance in plants by constitutive chromatin modification at heat stress memory gene loci (Shekhawat et al. 2021). Such studies have also been done in AM Fungi wherein their association with plants under drought stress resulted in an upregulation of genes involved in the mitogen-activated protein kinase (MAPK) cascades, which are response regulators to stresses in plants and AMF (Huang et al. 2020). These studies have significantly strengthened the existing knowledge on plant-responses to abiotic stress conditions, as well as the factors governing microbe-mediated enhancement of plants’ indigenous stress-combat mechanisms. Additionally, these techno-advancements have also promoted keen investigations on plant-microbe associations in chronically stressed habitats where both the plants as well as associative microflora have been supposed to have acquired a significant degree of resilience. For instance, keen investigations on microbes associated with xerophytic plants could reveal the key factors governing the establishment and smooth functioning of the beneficial associations, and microbe-mediated

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enhancement of stress-combat mechanisms under severe drought conditions. Similarly, plants thriving under highly saline conditions are also being increasingly attended for possible diversity of agriculturally important microbes that could be efficiently utilized for developing sustainable strategies to promote plant growth and productivity under saline conditions.

5 Conclusions Associative microbes comprise an integral part of the plant phyllosphere that actively contributes toward sound growth and development of plants under varying biogeochemical circumstances. Rhizosphere microbes—mainly AM fungi, along with other bacterial inhabitants can substantially reduce the ill-effects of drought stress in plants. Similarly, microbial associations can strengthen the plant performance under hostile saline conditions. Overall, plant-beneficial microbes exhibit promising capabilities that could be favorably exploited for developing microbebased strategies to mitigate the abiotic stress-induced adversities in plants. Thus, keen investigations aiming at exploration of plant-microbial associations from chronically stressed natural habitats are critical to harvest the yet-curtained diversity of agriculturally important microbes. Acknowledgments Authors are grateful to the Indian Council of Agricultural Research for financial support through the Network Project on Application of Microorganisms in Agriculture and Allied Sectors.

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Chapter 7

Plant Growth-Promoting Microbes: Key Players in Organic Agriculture Ekta Narwal, Jairam Choudhary, N. K. Jat, Amrit Lal Meena, P. C. Ghasal, Debashis Dutta, R. P. Mishra, M. Saritha, L. K. Meena, Chandra Bhanu, Raghuveer Singh, G. Chethan Kumar, A. S. Panwar, and Mahipal Choudhary

1 Introduction With the advent of green revolution, productivity of crops has been increased significantly by using improved plant varieties and agrochemicals such as chemical fertilizers and pesticides. Presently agriculture completely rely on the application of synthetic fertilizers, pesticides, herbicides or other inputs for crop production to satisfy the food demand of blasting global population. Therefore, with the increased production to fulfill the human demands, we are also subjected to several problems such as nitrate leaching, soil erosion, ecosystem degradation, reduction in the productivity in long-term, soil and water pollution, contamination of food and fodder, and ultimately affecting the health of animals and humans (Dotaniya et al. 2020; Zope et al. 2019; Shaikh et al. 2016a, b). Intensive use of chemicals is deteriorating the soil health specially the biological properties which will result in the reduction in the productivity in long-term. Subsequently fertilizers are costlier and availability is limiting, it has become ever more challenging for developing countries to afford the cost on purchase/production of these fertilizers. Around 25%

E. Narwal Shobhit Institute of Engineering and Technology, Modipuram, Meerut, India J. Choudhary · A. L. Meena · P. C. Ghasal · D. Dutta · R. P. Mishra · R. Singh · A. S. Panwar ICAR-Indian Institute of Farming Systems Research, Modipuram, Meerut, India N. K. Jat (*) · M. Saritha · M. Choudhary ICAR-Central Arid Zone Research Institute, Jodhpur, India L. K. Meena · C. Bhanu ICAR-Directorate of Rapeseed Mustard Research, Bharatpur, India G. C. Kumar ICAR-Indian Institute of Horticultural Research, Bengaluru, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_7

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reduction in yield is occurring year to year for banana, wheat, citrus, and vegetables. Therefore, more focus to find an alternative ecological approach for food security and safety is much needed. According to an estimate, 40% of deaths globally are because of soil, water, and air pollution (Glick 2012). Therefore, to maintain a sustainable production system, adoption of practices which reduces the application of agrochemicals is required. Capacity of soil to function within ecosystem and land use boundaries to ensure biological productivity, quality environment, and support plant and animal health is known as soil quality (El Enshasy et al. 2020). Researchers have investigated the physical, chemical, and biological properties of soil under both conventional and organic farming systems. Several researchers have observed significant improvement in soil quality under organic production systems as compared to conventional agriculture (Mader et al. 2002). Soil microbes are key player in several ecological processes like nutrient recycling, organic matter decomposition, and mineralization. Microbiological activity is very crucial in organic production system as the inputs used for crop production are organic. Microbial communities which are active in soil are crucial in synchronized release of nutrients from organic matter in respect to nutrient demand for better crop growth in organic farming. They also help in suppression of soil borne diseases via antibiosis and competition for nutrients (Jadhav et al. 2017; Mazzola 2002; Garbeva et al. 2004). Microbial diversity study of soil could be beneficial to forecast the effects of ecosystem perturbations by conventional and organic management practices (van Bruggen and Semenov 2000; Poudel et al. 2002) which will be helpful in designing the management practices in the field to improve soil health. Therefore, organic farming which has the potential to combat the ill effects of agrochemicals and restoration of soil health to achieve the sustainability in agricultural production system is the suitable alternative. Organic production system which is based on nutrient (residue) recycling concept largely excludes or avoids the applications of agrochemicals. Presently organic farming is gaining the interest/attention worldwide as it has been growing at an annual rate of 20% in the past 3 years (2004–2007) accounting for 32.3 million hectares worldwide, and this tendency seems to be increasing (Willer and Yussefi 2005). After soil health, quality of produce is very important. The increasing risk to the environment and human health with the loss of sustainability in the agriculture productivity due to extensive application of agrochemicals has diverted the focus of the consumers toward the organically produced food. Organic farming ensures the optimal use of natural resources of soil and its microbiome through methods like selection of native crop cultivars, and the production of crops suitable to prevailing soil conditions. A number of soil microorganisms are involved in these processes. Many show potential bio-control activities against weeds, crop diseases, and pests, while rhizobacteria and mycorrhizal fungi play crucial role in long-term fertility management. Microbes are presently being used as an alternative for synthetic pesticides and fertilizers for many different crops (Jadhav et al. 2017; Patel et al. 2016; Reshma et al. 2018) (Table 7.1).

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Table 7.1 Brief comparison between conventional and organic agriculture Particulars Nutrient management system Use of agrochemicals

Conventional agriculture Feeding of crop is given more preference rather than soil Conventional farms heavily rely on chemical fertilizers, pesticides, antibiotics, and growth hormones

Pesticide residues in farm and produce Pest management system

Present

Synthetic pesticides are used as silver bullet solution

Microbiological quality of food Cost of production

Chances of food borne infection are very low Higher due to costlier inputs (agrochemicals)

Inputs used for production

Chemical fertilizers, growth hormones, antibiotics, etc

Crop production

Crop production is higher presently but not sustainable for long term due to deterioration of soil quality

Environmental impact

It has a negative impact on soil, water, and atmosphere. Results in soil quality deterioration Destroy biodiversity

Effect on biodiversity Weed control

By the use of herbicides

Insect control

By the use of insecticides

Handling of farm animals

Use of growth hormones, antibiotics, and another form of medication to the animals to improve their growth and for disease prevention

Organic agriculture Feeding the soil rather than feeding the crop Use of agrochemicals is strictly prohibited. Mainly dependent on the crop, animal waste, biofertilizers, manures, etc Absent

Ecological approaches and organic/herbal formulations are key for managing pest and diseases Comparatively higher as inputs are biological in nature Production varies from crop to crop but comparatively higher at initial stages. Cost incurred in production is higher due to increased labor charges, higher nutrient cost, certification process, etc. Premium price of organic produce can maintain the benefit: cost ratio Compost, vermicompost, farm yard manure, NPK biofertilizers, mycorrhiza, bio-pesticides, oil cakes, neem oil, etc Organic production system is sustainable and ensures food and nutritional security to the population in long term Environment friendly. Helps in maintaining or restoring the soil fertility Promotes the natural balance and helps in preserving biodiversity Crop rotation, mulching as soil cover or hands weeding to control weed Relies on birds, predator insects or biocontrol agents Animals are permitted to roam around freely and feed on strictly organic foods to ensure balanced diet and their house remains clean to avoid disease outbreak (continued)

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Table 7.1 (continued) Particulars Recycling of farm waste for nutrient management

Conventional agriculture No preference is given for recycling of farm waste. Chemical fertilizers are key to feed the crop

Organic agriculture Recycling of farm waste (animal waste and crop residue) is key for supplementing the drained-out nutrients from the farm. It is an integrated system of crop production which could not be maintained without animal component

2 Soil Microorganisms and Organic Agriculture Organic farming can be the most effective tool for achieving the sustainability in agriculture. At present, organic farming has gained much attention due to its demand and necessity. Organic farming establishes a harmony between crop production, livestock, soil fertility, and genetic diversity of an ecosystem thereby ensures the sustainability. Altogether, there is an increased demand for providing toxic chemicals free, highly nutritious food to provide a better and healthy future. Microorganisms in soil are key players in various ecological functions such as soil formation process, plant nutrition, protection from the plant pathogens, weeds and pests, etc. Conventional agriculture, heavily dependent on usage of manufactured inputs has threatened soil microbes badly. The microorganisms in soil may vary depending upon the soil physical, chemical, and biological conditions. Microbes which benefit the crop plants either by direct or indirect mechanisms are known as plant growth-promoting microorganisms. Microbes in organic farming can be used as biofertilizers (nitrogen fixers, P solubilizer or mobilizer, organic matter decomposer, Fe, Zn, K solubilizers, etc.), biocontrol agents, growth hormone producers, disease suppressors, soil amendments to remove heavy metals, etc. (Prasad et al. 2020; Renjith et al. 2020; Sharma et al. 2013) (Fig. 7.1; Table 7.2).

3 Plant Growth-Promoting Rhizobacteria (PGPR) Rhizosphere is the area of intense microbiological activity around the roots of plant. It is the hotspot of plant-microbe interactions probably due to the root exudates released by plant which is key source of food for microbes and acts as a driving force to increase their population and activities. According to Bais et al. (2006), rhizosphere is the area around the roots where biological and ecological processes happen. Bulky soil has comparatively much lower microbial activity which is possibly due to absence of plant root’s penetration. PGPR can be used as useful bio-fertilizers having advantages over chemical fertilizers. These PGPR must be colonized for longer duration in the rhizosphere to have a beneficial impact on the plants. Sometimes, associative connections between bacteria and plant are accomplished with the

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Fig. 7.1 Plant growth-promoting activities of microbes in the rhizosphere

support of rhizo-deposits, which can similarly pose growth-promoting effects for the existence of the microbes (Maheshwari et al. 2019). Just like symbiotic interactions, associative interactions are of great importance as they have a positive impact on crop yield after inoculation (Hoflich et al. 1994). Contrariwise, rhizosphere is the infection platform where several soil-borne pathogens begin a parasitic association with plants. To start the infection process, pathogens have to compete with the other microbes for micro niche and available nutrients (Chapelle et al. 2016). The leftover effect on the assembly of the “rhizosphere microbiome”, i.e., the microbial proliferation in rhizosphere has crucial implications for the co-evolution of plant-microbe interactions in natural ecosystems. Rhizosphere comprises microbial dispersal from inoculum source to the plant roots, growth or proliferation in rhizosphere. Successful colonization of free-living bacteria in rhizosphere requires proper process for root colonization which mainly depends on rhizospheric conditions. Modulation of rhizosphere via rhizosphere engineering is important to support crop productivity. Successful root colonizers have the features to survive under diverse rhizospheric conditions and huge competition of the native microflora in the growth enhancement processes and in refining homeostatic mechanisms in response to biotic and abiotic stress challenges. The ecological adaptation in the plant rhizosphere safeguards it against a wide range of pathogens. Also, as a result,

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Table 7.2 Role of different microorganisms used in organic agriculture Group Nitrogen fixers Free living Symbiotic Associative symbiotic Endophytic Phosphatic biofertilizer Phosphate solubilizers

Phosphate mobilizers

K solubilizers

Zn solubilizers Fe biofertilizer Growth hormone producers Bio-control agent Compost enhancer and enrichers Disease suppressors Green manuring Amelioration of degraded or contaminated soils Drought evading Xenobiotic scavengers Microbial weedicides

Examples Azotobacter, Clostridium, Beijerinckia, Klebsiella, Nostoc, Anabaena Rhizobium, Anabaena azollae, Frankia Azospirillum Gluconoacetobacter Pseudomonas putida, P. striata, P. rathonia, Bacillus megaterium, B. firms, B. polymyxa, B. circulans, Enterobacter agglomerans, Bradyrhizobium japonicum Gigaspora sp., Glomus sp., Scutellospora sp., Acaulospora sp., Sclerocystis sp., Pisolithus sp., Laccaria sp., Amanita sp., Boletus sp., etc. Acidothiobacillus sp., B. mucilaginosus, B. edaphicus, B. circulanscan, Ferrooxidans sp., Burkholderia sp., and Paenibacillus sp. Bacillus sp. Acidithiobacillus Azospirillum brasilense, Gluconacetobacter diazotrophicus, Pseudomonas sp., Klebsiella variicola, Enterobacter cloacae Metrarhizium, Paenibacillus, Bacillus thuringiensis, NPV virus, Entomopthora sp., Nosema locustae, etc. Aspergillus, Trichoderma, Phanerchaete, Azospirillum, Azotobacter Pseudomonas, Bacillus, Trichoderma, Azolla Pseudomonas, Xanthomonas, Thiobacillus, Hydrocarbon-utilizing bacteria, Rhodococcus, Phanerochaete chrysosporium, etc. Vesicular arbuscular mycorrhiza (VAM) Pseudomonas Phytophthora palmivora, Colletotrichum gloeosporioides

plant shifts on downstream signaling pathways and produces antimicrobial compounds to destroy the pathogens and uphold homeostasis (Thormar and Hilmarsson 2007). This is precisely controlled complex process which involves a large number of genes and signaling pathways (Zipfel 2009). It is the intricacy of plant-PGPRpathogen interactions, which makes it challenging to discern, due to which metabolites, anatomical features, and signaling pathways become activated. The traditional, biochemical, and genetic experimental approaches are insufficient tools for the task. Rhizospheric competence is prerequisite for the growth and development of the plants. PGPR play most important role in plants growth and development either directly or indirectly. Both direct and indirect mechanisms support the plant to

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ensure sustainability for major crops. For this, helpful bacterial inoculants are used to coat the seeds and allowing them to raise the plants resulting in better growth and yield. Rhizospheric competency affects root and plant biology in relation to plant nutrition, growth promotion, development positively (Aragno 2005). Therefore, to ensure the sustainability in the agriculture production system, beneficial bacteria with greater rhizospheric competence can occupy the rhizosphere of other plants to ensure the better plant health.

4 Plant Growth Promotion Mechanisms 4.1

Direct Mechanisms

PGP microbe supports the plant growth directly by the growth hormone production or by improving nutrient uptake and nutrient availability by direct mechanisms such as biological nitrogen fixation (BNF), mineralization, solubilization of nutrient complexes, siderophore production of siderophores to sequester micronutrient.

4.1.1

Biological Nitrogen Fixation

BNF is the capacity of bacteria to transform atmospheric nitrogen to combined nitrogen, commonly in ammonical (NH4+) form (Bellenger et al. 2020; Shahrajabian et al. 2019). This combined nitrogen could be given to the plants which provide carbon source to nitrogen-fixing bacteria. The legume-Rhizobium association is highly specific and both symbiotic partners are supported by each other such as mutualistic symbiosis (Choudhary et al. 2019). The interaction between legumeRhizobium is most effective in BNF but significant in nonlegume except few plants such as sugarcane in which free-living endophytic bacteria Gluconacetobacter diazotrophicus (Sevilla et al. 2001) perform the BNF. Though, few grasses exhibited high levels of nitrogen gained through BNF process (Herridge et al. 2008). The freeliving bacteria which have capability to fix nitrogen via BNF include Beijerinckia sp., Pseudomonas fluorescens, Azotobacter sp., Azoarcus sp., Burkholderia unamae, Herbaspirillum sp., Gluconacetobacter diazotrophicus, Azospirillum brasilense, Nostoc sp., etc. (Defez et al. 2016; Fibach-Paldi et al. 2012; Kaschuk and Hungria 2017).

4.1.2

Phosphate Solubilization and Mobilization

Phosphorus is fundamental element of plant metabolism. It is key structural component in deoxy ribonucleic acid, ribonucleic acid, phosphor-lipids, and communication signals. Phosphorus features most importantly in plant growth and development for nearly all metabolic processes like energy transfer, respiration, signaling between

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plant receptors, macromolecules biosynthesis, and photosynthesis (Anand et al. 2016). Phosphorus is present in soil in plenty but in unavailable form (more than 95%) and therefore cannot be taken up by the plants. Monobasic and dibasic forms of phosphorus are soluble and therefore available to the plants (Gouda et al. 2018; Bhattacharyya and Jha 2012). Therefore, solubilization of unavailable P by the use of microbes is important strategy to improve the P availability in the organic farming. Several bacteria and fungi are capable to solubilize phosphate and improve plant uptake (Castagno et al. 2011; Ahmed et al. 2021). The capability of rhizobia to solubilize the phosphate has been investigated previously (Pandey et al. 2005) and later on various free-living aerobic bacteria were reported (Khan et al. 2007). Some PGPR solubilize phosphates from organic or inorganic compounds by the use of nonspecific phosphatases, phytases, phosphatases, and C-P lyases (Molina-Romero et al. 2015). Production of organic acids by the bacteria may chelate P, rendering it available to the plants (Aeron et al. 2011; Vyas and Gulati 2009). Bacteria with the capability to solubilize phosphorus complexes include Pseudomonas putida, P. striata, P. rathonia, Bacillus megaterium, B. firms, B. polymyxa, B. circulans, Enterobacter agglomerans, Bradyrhizobium japonicum, and Rhizobium leguminosarum (Molina-Romero et al. 2017). Besides these, other mechanisms of P solubilization are the inorganic acid production by some chemoautotrophs and the H+ pump witnessed in Penicillium rugulosum (Khan et al. 2014). Apart from solubilization, mobilization of phosphorus from the deeper zones of soil by the fungal hyphae associated in the mycorrhizal associations is very important in improving the bioavailability of phosphorus to the plant (Narwal et al. 2018; Singh et al. 2017).

4.1.3

Potassium Solubilization

Potassium is the third most essential nutrient required for the plant growth and development. Soil contains enormous amount of potassium than other nutrients, but availability to plants is partial as more than 90% of K is present in the form of silicates and rock (Parmar and Sindhu 2013). Four different forms of potassium are present in soil such as mineral K, exchangeable K, nonexchangeable K, and solution K. Moreover, imbalanced and irregular K fertilizer application has negative impact on plant growth and development. Deficiency of potassium resulted slow root development, reduced plant growth, reduced seed size, and ultimately poor yield. To ensure better plant growth and development, it is obligatory to find an in situ substitute that improves the availability of the potassium to the plant (Kumar and Dubey 2012). PGPR which support the plant growth and development, help to solubilize the potassium rocks by producing organic acids and convert them into available form for plants (Han and Lee 2006). Among these rhizobacteria, frequently studied by the researchers are K solubilizing bacteria (KSB), namely, Acidothiobacillus sp., B. mucilaginosus, B. edaphicus, B. circulanscan, Ferrooxidans sp., Burkholderia sp., and Paenibacillus sp. (Liu et al. 2012; Meena et al. 2014). The major mechanisms involved are (1) chelation of the cations bound

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to K; (2) lowering of pH; (3) acidolysis (Maurya et al. 2014; Meena et al. 2014). Therefore, the application of PGPRs in integrated nutrient management is essential for limiting the use of chemicals.

4.1.4

Siderophore Production

Iron is indispensable micronutrient as it acts as cofactor for several metabolic enzymes and obligatory in various physiological functions of plants and microbes like photosynthesis, biological nitrogen fixation, respiration, etc. Under oxygenic conditions, Fe occurs mainly in the oxidized form (Fe3+) which forms insoluble complexes with hydroxides and oxy-hydroxides, thereby making it unavailable to microbes as well as plants (Rajkumar et al. 2010). Microbes and plants obtain Fe through production of siderophores which are low-molecular mass Fe chelators. In bacteria, bio-synthesis of these siderophores is induced by the low Fe3+ level. Siderophores produced by microbes form the complex with iron (Fe3+), which is further reduced to Fe2+ on bacterial membrane. Chelation of iron by siderophores makes it unavailable to the pathogens thereby helps in suppressing plant pathogens also (Wani and Gopalakrishnan 2019).

4.1.5

Phytohormone Production

Phytohormones such as auxins, gibberellins, and cytokinins production are widely distributed mechanisms in bacteria associated with plant (Kang et al. 2014). In plant growth, some phytohormones such as IAA, gibberellins, and cytokinin have vital role in the root development, root surface area expansion, chlorophyll accumulation, leaf growth, seed dormancy, seed germination, enzyme function initiation, leaves and fruits senescence, etc. (Imriz et al. 2014; Sureshbabu et al. 2016). Indole acetic acid which is an auxin molecule, is the most studied phytohormone promoting the plant growth. Azospirillum is most studied for the biosynthetic pathway of IAA (Cassán et al. 2014). IAA promotes the division and elongation of root cells, induced root growth, and has greater root surface enabling plants with greater nutrient absorption and growth. Azospirillum brasilense, Pseudomonas sp., Klebsiella variicola, Bacillus amyloliquefaciens, Gluconacetobacter, diazotrophicus, and Enterobacter cloacae have been reported as producers both induced and constitutive IAA in vitro (Defez et al. 2016; Idris et al. 2007; Malik and Sindhu 2011).

4.1.6

ACC Deaminase Production

Ethylene is an essential plant signal hormone which is produced in larger amounts in quick duration under stress conditions. Under field conditions, plants are exposed to different biotic and abiotic stresses affecting their growth and development. Ethylene is very important in regulating germination of seeds, root growth, nodulation,

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flowering, and fruit ripening (Imriz et al. 2014). Under the stress conditions, plants activate ethylene-mediated systemic defense response resulting excessive energy consumption to the plants. Some rhizobacteria produce 1-aminocyclopropane-1carboxylate (ACC) deaminase which decreases the ethylene levels and improves the growth of plants (Sagar et al. 2020; Bal et al. 2013; Glick 2014). The ACC deaminase enzyme breaks ethylene precursor thereby avoiding its biosynthesis and also releases ammonium which can later be used as nitrogen source by plants (Singh et al. 2015). ACC deaminase production can also be considered as an indirect mechanism of plant growth promotion as it blocks out an intensive defense response avoiding needless energy consumption by plants. Researchers have reported several bacteria-producing ACC deaminase such as Achromobacter, Agrobacterium, Ralstonia, Pseudomonas fluorescens, Burkholderia unamae, Enterobacter cloacae, Azospirillum lipoferum, Agromyces, and Bacillus sp. (Nadeem et al. 2007; EsquivelCote et al. 2013; Zahir et al. 2009).

4.2 4.2.1

Indirect Mechanisms Antibiosis

Phytopathogens are main causative agents of plant diseases resulted in crop losses. Several researchers have reported P; the plant growth-promoting bacteria capable of eliminating/suppressing these pathogens; therefore can be used as a bio-control agent (Beneduzi et al. 2012; Liu et al. 2017). Inhibitory mechanisms by PGPB with bio-control potential include production of bacteriocins, siderophore, lytic enzymes, broad-spectrum antibiotics, antifungal metabolites, and lipopeptides (Molina-Romero et al. 2015; Mohamed et al. 2017; Sivasakthi et al. 2014). Researchers have reported numerous plant growth-promoting bacteria such as Burkholderia tropica, Gluconacetobacter diazotrophicus, Bacillus amyloliquefaciens, Lysinibacillus sphaericus, P. fluorescens, B. subtilis, B. altitudinis, Rhizobium etli, Azospirillum brasilense, Kosakonia radicincitans, Rhizobium leguminosarum, etc. which are able to eliminate the deleterious effects of phytopathogens by producing inhibitory substances (Cawoy et al. 2015; Krishnan et al. 2007; Lambrese et al. 2018; Naureen et al. 2017; Príncipe et al. 2018).

4.2.2

Volatile Organic Compounds

Volatile organic compounds (VOCs) are small gaseous molecules produced by bacteria, identified as proficient signal molecules functioning as chemical repellents or attractants (Hernandez-Calderon et al. 2018). In soil, VOCs interact with plants and may promote the growth of the plant by inducing the induced systemic resistance (ISR), phytopathogens suppression, increased photosynthesis, and modulating phytohormone signaling (Sharifi and Ryu 2018; Santoro et al. 2015). Researchers

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have identified several VOCs such as aldehydes, ketones, alcohols, terpenes, indoles, jasmonate, and fatty acids (Pieterse et al. 2014). VOCs produced by the rhizobacteria also improve the resistance of plants against abiotic stresses like drought, salinity, and heavy metals (Farag et al. 2013). Volatile organic compounds play crucial role as phytohormones and also in helping iron acquisition, regulating the growth and morphogenesis of the plant, and also in bio-control of plant pathogens either by induced systemic resistance or antibiosis (Park et al. 2013; Zhang et al. 2009). Researchers have reported several bacteria-producing VOCs are Bacillus subtillis, B. amyloliquefaciens, Pseudomonas fluorescens, P. stutzeri, Erwinia carotovora, P. polimyxa, and Stenotrophomonas maltophilia (Cheng et al. 2017; Rojas-Solis et al. 2018; Tahir et al. 2017). VOCs can be a sustainable, cost-effective, and eco-friendly strategy for agriculture (Kanchiswamy et al. 2015).

4.2.3

Bioremediation

Modern agriculture is heavily dependent on toxic agrochemicals such as herbicides, fungicides, and pesticides. The indiscriminate and excessive use of these agrochemicals imposed a negative impact on our soil, water, and environment and ultimately animal and human health. Researchers have found the negative impact of agrochemicals on microbial activity and diversity in soil which is instrumental for the plant growth and development (Berendsen et al. 2012; Kour et al. 2021) which may result in the loss of soil fertility in long run. Therefore, elimination of these agrochemicals from the soil is necessary for the better growth of the plants in sustainable manner. Researchers have reported numerous bacteria having the capability to remove the toxic residues from soil. Few extensively studied bacteria are Sphingomonas sp., P. putida, Burkholderia tropica, Burkholderia unamae, B. subtillis, Pseudomonas rhizophila, etc. (Hassen et al. 2018).

4.2.4

Induced Systemic Resistance

The plant-microbe (pathogen or beneficial) interaction activates the systemic response of plants which includes induced systemic resistance (ISR) and systemic acquired resistance (SAR). SAR is triggered by disease-causing microorganisms whereas ISR is triggered by nonpathogenic/beneficial microorganisms. SAR is a mechanism where plants obtain an increased defensive response to counter attack plant pathogens as a result of a primary, limited infection which is mediated by salicylic acid. This reaction for plant is relatively aggressive causing necrosis in some instances (Pieterse et al. 2014; Patel et al. 2016). ISR is mediated by jasmonate and ethylene. This phenomenon inhibits the pathogen’s establishment in the plant (van Loon 2007; Su et al. 2017). ISR is the mechanism to vaccinate the plants by beneficial microbes against phytopathogens and confer considerably increased levels of polyphenol oxidase, peroxidase, phenylalanine ammonia lyase, β–1, 3 glucanase, and chitinase as a measure of the systemic response (Sharma et al. 2018).

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Application of PGPR with the capability to activate a systemic response in plants might prevent the pathogen attack resulting in increased yield in different crops (Gkizi et al. 2016). Other than PGPR, other bacterial components like lipopolysaccharides, siderophores, flagella, and cyclic lipopeptides also induce the ISR response (Ramamoorthy et al. 2001). Several bacteria able to trigger the induced systemic response have been identified by researchers and are Bacillus altitudinis, B. subtilis, B. cereus, B. pasteuri, B. amyloliquefaciens, B. mycoide, B. pumila, B. sphaericus, Pseudomonas fluorescens FB11, P. putida 89B-27, Burkholderia phytofirmans, Serratia marcescens, Rhizobium leguminosarum bv. viceae FBG05, Paenibacillus alvei K165, and Rhodopseudomonas palustris (Elbadry et al. 2006; Gkizi et al. 2016; Kloepper et al. 2004).

4.2.5

Modulation of Environmental Stresses

Plants face a battery of biotic and abiotic stresses which arise due to inherent soil factors and anthropogenic activities. Field crop environments and associated factors most commonly enforce changing levels of abiotic stresses on crops and thereby prevent the complete realization of genetic potential of crop in terms of quality and yield (Selvakumar et al. 2012). Growth and survival of the plant under stress may be boosted by the involvement of stress-tolerant microorganisms specially PGPM and Arbuscular mycorrhizal (AM) fungi (Nadeem et al. 2014; Narwal et al. 2021). Microorganisms use several direct and indirect mechanisms for the promotion of the plant growth under adverse conditions. These mechanisms involve several biochemical and molecular modulations beneficial for plant growth and development under stress. PGPR perform several ecological functions which promote the plant growth therefore, their inoculation, promote the plant growth by controlling nutritional and hormonal balance, growth hormone production, and inducing resistance against different plant pathogens (Spence and Bais 2015; Kapadia et al. 2021; Khan et al. 2021; Kusale et al. 2021). PGPR produce certain metabolites like siderophores which restrict the growth and development of phytopathogens in rhizosphere (Złoch et al. 2016). PGPR also play crucial role in nitrogen fixation, solubilization of different nutrients (phosphate, potash, zinc, iron, etc.), nutrient uptake, water uptake, antibiotic production, hydrolytic enzymes production, growth factors production, deconstruction of undecomposed material which directly or indirectly benefits the plant growth and development. Several other processes for example nutrient mobilization, exopolysaccharide (EPS) production, rhizobitoxine production, heavy metal detoxification, etc. also help the plant to sustain under adverse climatic conditions. Rhizobitoxine promotes the growth and development of plant under unfavorable conditions by inhibiting ethylene production (Kumar et al. 2009). Moreover, PGPR may have the capability to promote plant growth and development by some key enzymes like chitinase, glucanase, and ACC-deaminase under unfavorable conditions (Farooq et al. 2009). Moreover, some bacteria have sigma factors which play important role in changing gene expression under stress to alleviate harmful effect (Gupta et al. 2013).

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Fig. 7.2 Role of mycorrhiza in improving plant health

Mycorrhiza, a mutualistic association between fungi and higher plant roots, is also an important aspect playing significant role in growth and development of plant under adverse conditions. Arbuscular mycorrhiza often mycorrhiza in agricultural field. In this association, fungal partner performs nutrient cycling, absorption, and translocation of different nutrients. In drought conditions, mycorrhiza improves the water uptake and prevents the desiccation of plant roots thereby helps the plant in sustaining under water scarcity conditions. Therefore, PGPR can be a potential substitute for inorganic fertilizers and pesticides to make the agriculture sustainable to ensure the food security of worlds blasting population. PGP bacteria such as Bacillus and Paenibacillus uphold the growth and health of the plant in different ways like improvement of host plant nutrition and growth, antagonism to control pathogens, and activate defense mechanism and promote sustainable agriculture (Govindasamy et al. 2010). The sustainable agriculture exercise with the use of stress-tolerant PGPM may increase the yield and improve nutritional quality of food grains under changing climate as well as saving of 20–25% cost of chemical fertilizers and pesticides (Fig. 7.2). Using of these practices by the farmers can enhance the financial income with production of organic foods and vegetables. Several researchers have studied different mechanisms of plant growth promotion employed by different microorganisms in different crops (Table 7.3).

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Table 7.3 Brief description of different mechanisms that offer plant growth promotion in various crops Bacterial inoculant Alcaligenes faecalis, Bacillus cereus Pantoea phytobeneficialis MSR2

Crop Sorghum bicolor –

Rhizoglomus irregular (AM) and Pseudomonas Bacillus aryabhattai and Pseudomonas auricularis Bacillus megaterium

Solanum lycopersicum

Plant growth promotion mechanism Alleviation of heavy metal toxicity Biological nitrogen fixation, phosphate solubilization, ACC deaminase activity, cytokinin biosynthesis, indoleacetic acid, and jasmonic acid metabolism Organic and inorganic phosphate mobilization

Camellia oleifera

Improved available N, P, and K in rhizospheric soil

Wu et al. (2019)

Capsicum annuum

Zinc solubilization

Pseudomonas libanensis EULWNA33 Achromobacter xylosoxidans Rhizobium, Pseudomonas

Triticum aestivum

Phosphate solubilization under drought conditions

Bhatt and Maheshwari (2020) Kour et al. (2019)

Vigna radiata

Influence plat homeostasis

Medicago sativa, Trigonella sp., Vigna radiata Soybean, wheat, Vigna radiata

Biological nitrogen fixation

Bradyrhizobium

Pseudomonas sp. PS1

Vigna radiata

Pseudomonas aeruginosa Pseudomonas fluorescens

Cicer arietinum

Pseudomonas fluorescens Bradyrhizobium sp.750, Ochrobactrum cytisi, Pseudomonas sp.

Hordeum vulgare, Triticum aestivum Camellia sinensis Lupinus luteus

Herbicide-tolerant Rhizobium strain MRP1 increased the growth parameters at all tested concentrations of herbicides Effectively increased plant dry weight, total chlorophyll content, nodule numbers, leg-hemoglobin, root and shoot N, root and shoot P, seed yield, and protein content in seed Improved P and K uptake Prevent Fusarium culmorum

Increased nutrient use efficiency Improved nitrogen content and biomass, heavy metal accumulation (phytostabilization potential)

References El-Meihy et al. (2019) Nascimento et al. (2020)

Sharma et al. (2020)

Ma et al. (2009) Choudhary et al. (2017)

Ahemad and Khan (2012a)

Ahemad and Khan (2012b)

Ahemad and Kibret (2014) Santoro et al. (2016)

Thomas et al. (2010) Dary et al. (2010)

(continued)

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Table 7.3 (continued) Bacterial inoculant AM Fungi, Streptococcus, and Bacillus sp.

Crop Zea mays

Pseudomonas and Azospirillum Pseudomonas sp. Polymyxa Paenibacillus

Piper nigrum Piper nigrum, Zea mays

Azotobacter chroococcum Acinetobacter sp.

Triticum aestivum Oryza sativa

Bacillus sp.

Glycine max

Plant growth promotion mechanism Improved mineralization of P and growth parameters including shoot, root yield, height, nutrient uptake as compared to control Improved phosphate solubilization and availability Improved soil enzyme activities, nutrient uptake, productivity, plant biomass, and stimulated ISR against bacterial spot pathogen Xanthomonas axonopodis pv. Vesicatoria BNF and P solubilization Improved Zn solubilization thereby improved and growth and yield of rice P solubilization

References Wahid et al. (2016)

Ramachandran et al. (2007) Sharma et al. (2011)

Bhattacharyya and Jha (2012) Gandhi and Muralidharan (2016) Wahyudi et al. (2011)

5 Conclusion and Future Perspectives Presently, due to indiscriminate application of synthetic fertilizers, pesticides, and herbicides on crops, the sustainability in agriculture has distorted. The cost of cultivation has increased at a very high rate; the farmer’s income is stagnated and the target of attaining of food security and safety has become a frightening challenge. Conventional agricultural practices have become a major cause of soil degradation. Due to this reason, application of PGPR instead of synthetic agrochemicals is known to promote the plant growth by enhanced availability of nutrients and may support to sustain human, environmental health, and soil fertility. Several bacterial species associated with the plant roots and rhizosphere have been isolated, tested, and determined for their positive effect on plant growth, yield, and quality in the laboratories so far but, it is quite necessary to know their beneficial effects under field conditions. Therefore, to achieve the food security and sustainable plant productivity, while maintaining environmental quality, basic and strategic research must be undertaken to improve the knowledge regarding plant-microbe interactions in the rhizosphere. Considering the good impact of PGPR on crop productivity and ecosystem functioning, much emphasis should be given for its implementation in sustainable agriculture.

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Shahrajabian MH, Sun W, Cheng Q (2019) Sustainable agriculture and soybean, a legume in traditional Chinese medicine with great biological nitrogen fixation. J Biol Environ Sci 13(38): 71–78 Shaikh SS, Reddy MS, Sayyed RZ (2016a) Plant growth-promoting rhizobacteria: an eco-friendly approach for sustainable agro-ecosystem. In: Plant soil-microbes. Springer, Cham, pp 182–201 Shaikh SS, Wani SJ, Sayyed RZ (2016b) Statistical-based optimization and scale-up of siderophore production process on laboratory bioreactor. 3 Biotech 6(1):69 Sharifi R, Ryu CM (2018) Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot 122:349–358 Sharma SK, Johri BN, Ramesh A (2011) Selection of plant growth-promoting Pseudomonas spp. that enhanced productivity of soybean-wheat cropping system in central India. J Microbiol Biotechnol 21:1127–1142 Sharma SB, Sayyed RZ, Trivedi MH et al (2013) Phosphate-solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2(1):1–14 Sharma CK, Vishnoi VK, Dubey RC (2018) A twin rhizospheric bacterial consortium induces systemic resistance to a phytopathogen Macrophomina phaseolina in mung bean. Rhizosphere 5:71–75 Sharma S, Compant S, Ballhausen MB et al (2020) The interaction between Rhizoglomus irregulare and hyphae attached phosphate-solubilizing bacteria increases plant biomass of Solanum lycopersicum. Microbiol Res 240:1–10 Singh RP, Shelke GM, Kumar A et al (2015) Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol 6:1–14 Singh G, Sangwan S, Narwal E et al (2017) Microbial proteins and soil carbon sequestration. In: Adaptive soil management: from theory to practices. Springer, Singapore, pp 131–139 Sivasakthi S, Usharani G, Saranraj P (2014) Biocontrol potentiality of plant growth-promoting bacteria (PGPR)-Pseudomonas fluorescens and Bacillus subtilis: a review. Afr J Agric Res 9: 1265–1277 Spence C, Bais H (2015) The role of plant growth regulators as chemical signals in plant-microbe interactions: a double-edged sword. Curr Opin Plant Biol 27:52–58 Su P, Tan X, Li C et al (2017) Photosynthetic bacterium Rhodopseudomonas palustris GJ-22 induces systemic resistance against viruses. Microb Biotechnol 10:612–624 Sureshbabu K, Amaresan N, Kumar K (2016) Amazing multiple function properties of plant growth-promoting rhizobacteria in the rhizosphere soil. Int J Curr Microbiol Appl Sci 5:661– 683 Tahir HAS, Gu Q, Wu H et al (2017) Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front Microbiol 8:1–11 Thomas J, Ajay D, Kumar R et al (2010) Influence of beneficial microorganisms during in vivo acclimatization of in vitro-derived tea (Camellia sinensis) plants. Plant Cell Tissue Organ Cult 101:365–370 Thormar H, Hilmarsson H (2007) The role of microbicidal lipids in host defense against pathogens and their potential as therapeutic agents. Chem Phys Lipid 150:1–11 van Bruggen AHC, Semenov AM (2000) In search of biological indicators for plant health and disease suppression. Appl Soil Ecol 15:13–24 van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. In: Bakker PAHM, Raaijmakers JM, Bloemberg G, Hofte M, Lemanceau P, Cooke BM (eds) New perspectives and approaches in plant growth-promoting rhizobacteria research. Springer, Dordrecht, pp 243–254 Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:1–15 Wahid F, Sharif M, Steinkellner S et al (2016) Inoculation of arbuscular mycorrhizal fungi and phosphate-solubilizing bacteria in the presence of rock phosphate improves phosphorus uptake and growth of maize. Pak J Bot 48:739–747

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Wahyudi AT, Astuti RP, Widyawati A et al (2011) Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting rhizobacteria. J Microbiol Antimicrob 3:34–40 Wani SP, Gopalakrishnan S (2019) Plant growth-promoting microbes for sustainable agriculture. In: Plant growth promoting rhizobacteria (PGPR): prospects for sustainable agriculture. Springer, Singapore, pp 19–45 Willer H, Yussefi M (2005) The world of organic agriculture: statistics and emerging trends. International Federation of Organic Agriculture Movements, Bonn. https://orgprints.org/id/ eprint/4297/ Wu F, Li J, Chen Y et al (2019) Effects of phosphate-solubilizing bacteria on the growth, photosynthesis, and nutrient uptake of Camellia oleifera Abel. Forests 10(4):348 Zahir ZA, Ghani U, Naveed M (2009) Comparative effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of pea (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963 Zhang H, Sun Y, Xie X et al (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577 Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12(4): 414–420 Złoch M, Thiem D, Gadzala-Kopciuch R et al (2016) Synthesis of siderophores by plant-associated metallotolerant bacteria under exposure to Cd2+. Chemosphere 156:312–325 Zope VP, El Enshasy HA, Sayyed RZ (2019) Plant growth-promoting rhizobacteria: an overview in agricultural perspectives. In: Plant growth-promoting rhizobacteria for sustainable stress management. Springer, Singapore, pp 345–362

Chapter 8

Interceding Microbial Biofertilizers in Agroforestry System for Enhancing Productivity Sangeeta Singh, Tanmaya Kumar Bhoi, and Vipula Vyas

1 Introduction India has a severely unbalanced natural resource base. Approximately 18% of the world’s population and 15% of livestock are supported by 2.4% of geographic areas, 1.5% of forests and pastures, and 4.2% of water resources (FAO 2018). To cope up the growing requirement for food, silage, vegetables, firewood, wood, medicine, etc., the increase in living population is forced to obtain more arable land. The increased need for food and timber has resulted in forest overuse. Therefore, it is necessary to significantly increase agroforestry production systems by managing suitable environmental conditions and maintaining soil fertility (Glaser and Lehr 2019). Agroforestry is one of the most feasible alternative land-use systems for maximizing long-term productivity (fuel, feed, and food) while also safeguarding the environment. Increasing the agroforestry area of the country can help cope with some major challenges (CAFRI Vision 2050 2015; Dhyani et al. 2016). In order to achieve higher yields within the limited land resources, chemical fertilizers are used inadvertently every year, which seriously damage the vitality of the soil and reduce the soil productiveness of a huge area of land. In addition, the use of microbial bioinoculants may have a positive impact on overall growth and quality of plants (Babalola 2010). In this case, microbial biofertilizers and agroforestry will be chosen to increase land efficiency in a sustainable manner (Yadav and Sarkar 2019), and it also might play a key part in addressing the worldwide concerns for food, feed, as well as fuel needs in the twenty-first century. The role includes climate change. This book chapter contains short and in-depth information on the many features of PGPRbased biofertilizers, as well as their possibilities and limits, as well as the ultimate commercialization roadmap.

S. Singh (*) · T. K. Bhoi · V. Vyas Arid Forest Research Institute, Jodhpur, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_8

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2 Agroforestry Importance in Arid Regions (In Western Rajasthan) Agroforestry is a well-defined land use system in western Rajasthan that dates back centuries. Even though a huge number of trees and shrubs are planted on agricultural areas, Khejri (Proscopis cineraria) and bordi (Ziziphus nummularia) remain to be the most significant multipurpose woody components of traditional agroforestry systems. Land utilization changes linked with agriculture and cattle have altered native dry zone ecosystems, generating diverse landscapes with parks of converted and unprocessed regions (Shachak et al. 2005). Agroforestry systems have piqued the interest of several researchers and policymakers as a promising means of achieving these objectives (Perfecto and Vandermeer 2008). Agroforestry helps to relieve and reduce the effects of harsh and erratic climatic conditions, as well as poor soils, by increasing soil fertility and enhancing symbiotic activities that aid crop growth, sustainable food and feed production, fuel, timber, fiber, tools, draught power, medicines, and a variety of other farm products. During droughts, traditional agroforestry methods using tree species such as P. cineraria, Tecomella undulata, Salvadora oleoides, Dalbergia sissoo, and Azadirachta indica have shown to be a vital life support system. Because there is limited room to improve food output by expanding the area under cultivation, India's demand for food and fodder has risen to worrisome levels. Only land that is already under cultivation or land that is not traditionally considered arable can be used to improve food production. It is necessary to design a management system capable of generating food from marginal agricultural land while simultaneously preserving and enhancing environmental quality. Agroforestry has the potential to be both productive and protective, and it can help us increase the productivity of our land to fulfill the needs of both human and animal populations (Table 8.1).

3 PGPR Plant growth-promoting rhizosphere (PGPR) is a bacterial group that is found in the rhizosphere (Ahmad et al. 2008). The term “plant growth-promoting bacteria” refers to bacteria designated to be planted in the roots (rhizosphere) of plants to promote overall plant development. The rhizosphere is the soil environment in which plant roots interact with soil microbes. It is the area with the greatest microbial activity, in which essential macro and micronutrients are being provided to plants. Root secretions serve as source of nutrients for microbial development (Basu et al. 2021). The microbial populations existing in the rhizosphere are relatively different from the microbial populations in the surrounding environment (Burdman et al. 2000). Weller and Thomasshow (1994) proved that compared to bulk soil, the narrow rhizosphere is rich in nutrients for microorganisms; this can be demonstrated by the number of bacteria present around the roots of plants, which are usually higher than in bulk soil

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Table 8.1 Components of traditional agroforestry system of Rajasthan (Harsh et al. 1992) Name of district Jaisalmer

Sri Ganganagar

Bikaner

Barmer

Jodhpur

Churu, Jhunjhunu, and Sikar Nagaur Jalore

Pali

Main tree/shrub species Calligonumpolygonoides, Ziziphus nummularia, Prosopis cineraria, Acacia senegal, Capparis deciduas Prosopis cineraria, Acacia nilotica subsp. indica, Acacia tortilis Prosopis cineraria, Ziziphus nummularia, Calligonum polygonoides, Acacia jacquemontii Prosopis cineraria, Tecomellaundulata, Ziziphus nummularia, Capparis deciduas, Acacia senegal Prosopis cineraria, Ziziphus nummularia, Capparis decidua, Acacia senegal Prosopis cineraria, Gymnosporiamontana, Ziziphus nummularia, Prosopis cineraria, Acacia nilotica Prosopis cineraria, Salvadoraoleoides, Acacia nilotica, Punica granatum (fruit tree) Acacia nilotica subsp. indica, Acacia nilotica. var. cupressiformis, Acacia leucophloea, Acacia catechu, Salvadoraoleoides

Main crops Mung bean, cluster bean, and pearl millet

Prominent grass species Lasiurus sindicus

Pearl millet, mung bean, and cluster bean (rainfed), wheat, cotton, rice, and mung bean (irrigated) Moth-bean, Pearl millet, mung bean, and cluster bean

Lasiurus sindicus

Pearl millet, mung bean, and cluster bean

Lasiurus sindicus

Pearl millet, mung bean, and cluster bean (rainfed) wheat chilli, mung bean, and mustard (irrigated) Pearl millet, mung bean, and cluster bean Pearl millet and mung bean (rainfed), wheat, mung bean, and mustard (irrigated) Pearl millet, mung bean, isabgol, sorghum, and cumin

Cenchrus ciliaris

Sorghum, pearl millet, mung bean, and cluster bean

Lasiurus sindicus

Lasiurus sindicus Cenchrus ciliaris Cenchrus ciliaris

Cenchrus ciliaris, Cenchrus setigerus

10–100 times. Bacteria, fungus, actinomycetes, protozoa, and algae are among the microorganisms that populate the rhizosphere. Bacteria, on the other hand, are the most common microbes in the rhizosphere (Kaymak 2010; Shaikh et al. 2016). The use of these microbial populations to promote plant growth is well known and proven (Saharan and Nehra 2011; Bhattacharyya and Jha 2012). Kloepper and Schroth (1981) introduced the term plant growth-promoting rhizobacteria (PGPR) for these beneficial microorganisms in 1978, paving the way for more discoveries of PGPR. PGPR are not only related to roots and have a beneficial effect on plant development, but also have a positive effect on the control of plant pathogenic

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microorganisms (Son et al. 2014). Therefore, PGPR is one of the active ingredients in biological fertilizer formulations. According to their interaction with plants, PGPRs are classified as symbiotic, i.e., they live inside plants and exchange metabolites directly with them, or free-living rhizosphere bacteria, which reside outside plant cells and exchange metabolites with them (Gray and Smith 2005). The working mechanism of PGPR can also be divided into the direct mechanism and indirect mechanism. The direct mechanism is biological fertilization, stimulating root growth, rhizosphere repair, along with them plant stress control is also present. On the other hand, rhizosphere bacteria serve as an indirect biological control mechanism to promote plant growth by reducing the effects of diseases, including antibacterial, inducing system resistance, and competition for nutrients and niche (Egamberdieva and Lugtenberg 2014). The majority of symbiotic bacteria can be found. Certain bacteria can create symbiotic relationships with the host and infiltrate plant cells in the intercellular spaces of host plants. Furthermore, a select number have the ability to integrate their physiology with that of the plant, resulting in the creation of specialized structures. Rhizobia, a well-known mutualistic symbiotic bacterium, could form symbiotic relationships with leguminous crop plants, fixing atmospheric nitrogen in nodules on the plant’s roots.

3.1

Attributes of Ideal PGPR

A rhizosphere bacterial strain is regarded a potential PGPR if it exhibits particular plant growth-promoting traits and can enhance plant development following inoculation. The ideal PGPR strain should meet the following criteria (Vejan et al. 2016): 1. 2. 3. 4. 5.

It should have a high rhizosphere capacity and eco-friendliness. After inoculation, it should be planted in large quantities in the roots of plants. It should be capable to help with the development of plants. It should exhibit a diverse wide range of implications. It must be able to reconcile with other beneficial microbes present in the rhizosphere. 6. It must withstand physical and chemical factors such as heat, drying, radiation, and oxidizing agents. 7. Compared with the existing rhizosphere bacterial community, it should show better competitiveness.

3.2

Potential Role of PGPR in Agroforestry

Searches for PGPR and its mode of action are quickly growing in order to employ the finest PGPR strains as commercial biofertilizers. Effective PGPR support plant growth by modifying the architecture of the entire microbial population in the rhizosphere (Kloepper and Schroth 1981). PGPR promote plant growth by binding

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nitrogen, lowering ethylene levels, creating siderophores and plant hormones, inducing disease resistance, dissolving nutrients, boosting mycorrhizal function, and reducing pollutant toxicity, according to Glick et al. (1999). PGPR strains can, directly and indirectly, promote plant growth and development. The production of plant hormones such as auxins, cytokinins, and gibberellins, the dissolution of minerals, e.g., phosphorus and iron, siderophores production and production of enzymes, and systemic resistance induction are all examples of direct stimulation, whereas biological control is an example of indirect stimulation. Extracellular enzymes are synthesized to hydrolyze the fungal cell wall and compete for the rhizosphere habitat. Antibiotics are created, accessible iron in the rhizosphere is chelated, and extracellular enzymes are synthesized to hydrolyze the fungal cell wall and compete for the rhizosphere niche (Zahir et al. 2004; Van Loon 2007). The most promising candidates for indirect stimulation are PGPR bacteria, particularly Pseudomonas fluorescens and Bacillus subtilis (Damayanti et al. 2007). In addition, nitrogen conversion, enhanced phosphate bioavailability, iron acquisition, the display of specific enzyme activity, and antibiotic synthesis to protect plants from dangerous infections can all help to improve crop quality (Spaepen et al. 2007). Therefore, in accordance to their mechanism of actions, PGPRs can be divided into three general forms: biological fertilizers, plant stimulants, and biological pesticides. The phenomenon of population regulation affects the expression of each of these characteristics because PGPRs interact regularly with the resident microbial community in the rhizosphere (Lugtenberg and Kamilova 2009). Recent studies on PGPR have shown that it mainly promotes plant growth in the following ways: 1. Production ACC deaminase is known to lower the amount of ethylene that is being developed in the roots of the plants (Dey et al. 2004; Sagar et al. 2020). 2. They produce plant growth regulators such as IAA (Mishra et al. 2010), GA (Narula et al. 2006), cytokinin (Castro et al. 2008), and ethylene (Saleem et al. 2007). 3. Nitrogen fixation that is nonsymbiotic in nature (Ardakani et al. 2010). 4. By producing siderophores, it exhibits resistance to plants antagonistic activity of pathogenic microorganisms, 3-glucanase, fluorescent pigments, antibiotics, chitinase, and cyanide (Pathma et al. 2011; Wani et al. 2016). 5. Solubilization of mineral phosphate and other nutrients (Hayat et al. 2010). Plant growth stimulation is the result of a number of processes that can all be triggered at the same time, and PGPR can take advantage of more than one of these mechanisms to boost plant growth (Martinez-Viveros et al. 2010). Biochemical and molecular approaches have recently provided fresh insights into the genetic foundation, regulation, and relevance of these processes in biological control (Joshi and Bhatt 2011). Despite the fact PGPR inoculation may momentarily increase population number, in order to be more effective in the rhizosphere, PGPR must maintain a critical population density for a longer length of time (Fig. 8.1; Table 8.2).

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Fig. 8.1 Diagram depicting different function of PGPR

3.3

Synthetic Pesticide v/s PGPR

The Green Revolution, which began in the second part of the twentieth century, brought in a period of global agricultural prosperity. By introducing new highyielding seed varieties and boosting the use of synthetic fertilizers, pesticides, and other agrochemicals, the Green Revolution has made a significant contribution to enhancing plant productivity and agricultural yields (Kesavan and Swaminathan 2018; Hamid et al. 2021). Since then, the global agricultural landscape has undergone tremendous changes. Excessive use of synthetic agrochemicals to boost crop yield has harmed arable soils’ biological, physical, and chemical health, resulting in a declining trend in worldwide agricultural productivity over the last few decades (Pingali 2012; Yang and Fang 2015; Bishnoi 2018). Under the current scenario, land resources are shrinking and biological wealth is exhausted. In order to meet the growing demand for sustainable agriculture, crop output and productivity must improve in tandem with agricultural-related commodity production (Zope et al. 2019). The above-mentioned multidimensional, ecological, socioeconomic, and technological inadequacies in promoting sustainable agriculture have no single or direct answer (Kesavan and Swaminathan 2018). Promoting sustainable agriculture by gradually reducing the use of synthetic agrochemicals and promoting the biological and genetic potential of crops and microorganisms (Fascella et al. 2015, 2018) are effective methods for dealing with rapid climate change. In addition to

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Table 8.2 PGPR used in different plant attributing characters PGPR mechanism Phytohormone production Indole acetic acid (IAA)

Examples

References

Bradyrhizobium sp.

Cytokinin Gibberelin

R. leguminosarum Bacillus sp.

N2- Fixation

Rhizobium sp. Frankia, Azosprillum, Azotobacter B. subtilis P. striata B. mucilaginosus B. edaphicus Thiobacillus thioxidans

Antoun et al. (1998) Noel et al. (1996) GutierrezManero et al. (2001) Dakora (2003) Kizilkaya (2009)

P- solubilizer K- Mobilizer Micronutrient supplier Siderophores production Siderophores

Azotobacter vinelandii Bacillus cereus Bacillus megaterium Pseudomonas putida

Antibiotics production 2,4-Diacetyl phloroglucinol (DAPG), Phenazine-1-carboxylic acid (PCA) Subtilin, Subtilosin A, Tasa, Sublancin, Bacilysin Tomato mottle virus

Pseudomonas fluorescens, P. aeruginosa Bacillus subtilis 168, B. amyloliquefaciens FZB42 B. amyloliquefaciens

Tobacco necrosis virus

P. fluorescens

Rhizoctonia bataticola

Pseudomonas sp.

Dominguez et al. (2011) Meena et al. (2016) Ijaz et al. (2019) Husen (2003) Chakraborty et al. (2006) Gangwar and Kaur (2009) Husen (2003) Bharti and Tewari (2015) Fernando et al. (2005) Murphy et al. (2000) Park and Kloepper (2000) Gupta et al. (2002)

genetically manipulating the crop physiology and metabolic activities, some members of soil microflora, particularly those located in plant’s rhizospheres, may benefit plants in preventing or partially overcoming environmental stress (Ilangumaran and Smith 2017; De Souza et al. 2015; Khan et al. 2019). The search for ecologically friendly alternatives to harmful agrochemicals ended in the discovery and subsequent use of biological fertilizers and other microbial-based products, such as organic extracts and earthworm feces (Mishra et al. 2017; Arancon et al. 2019). These microbial compounds are nontoxic and environmentally acceptable, and they could be utilized to help plants thrive and control diseases. The biological potential

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and fertility of the soil may be increased, and the detrimental effects of agrochemicals can be reduced, by using microbial agents to fertilize crops (Raklami et al. 2019; Jabborova et al. 2020; Sharma et al. 2013). The use of plant growth-promoting rhizobacteria (PGPR) as biofertilizers and biological control agents is being considered as a viable alternative to synthetic agrochemicals in crop production (Anli et al. 2020; Dong et al. 2019; Atieno et al. 2020).

3.4

Classification of PGPR

PGPR can be classified into four major groups namely nitrogen-fixing microbes, phosphorous-fixing microbes (Bacillus sp. and Pseudomonas sp.), potassium-fixing microbes (Burkholderia sp. and Pseudomonas sp.), and others microbes. Nitrogenfixing microbes are further classified into symbiotic, nonsymbiotic (Azotobactor, Azospirillum, and Cyanobacteria), and free-living (Azolla). Further symbiotic nitrogen-fixing microbes are classified into two groups viz., symbiotic leguminous (Rhizobium) and nonsymbiotic leguminous (Frankia). The other microbes belonging to PGPR include micronutrient-fixing microbes (Thiobacillus and Xanthobacter) and biocontrol agents (Bacillus sp. and Pseudomonas sp.) (Fig. 8.2).

3.4.1

N2-Fixing Microbes

Nitrogen is the primary building block for the production of amino acids and proteins, as well as the most important nutrient for plant growth and development.

Fig. 8.2 Overall classification of major group of PGPR

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Unfortunately, the most prevalent manifestation is plants' inability to acquire nitrogen from the atmosphere. Plants can only get fixed forms of nitrogen, such as ammonia and nitrate, through biological nitrogen fixation (Wagner 2012; Sengupta and Gunri 2015). In general, the biological technique of nitrogen fixing (N2) fixes 180 metric tons per year, 80% of this fixation comes from symbiotic associations, and the rest comes from free-living microorganisms or other related systems in the rhizosphere (Tilak et al. 2005). The ability to capture such a considerable amount of atmospheric N2 and replenish soil N2 in a fixed form is attributed to nitrogen-fixing microorganisms (Tilak et al. 2005). These include (1) symbiotic nitrogen-fixing forms, namely rhizobia, specific to legumes, and Frankia, specific to nonlegumes, and (2) nonsymbiotic nitrogen-fixing (N2 fixation) forms that survive outside plants, e.g., cyanobacteria, nitrogen fixation Spirulina and Azotobacter. Santi et al. (2013) described the relevance of biological nitrogen fixation in afforestation and the biological nitrogen fixation by blue-green algae and bacteria (Rhizobium and Frankia) in forest tree species.

3.4.1.1

Symbiotic Nitrogen-Fixing

3.4.1.1.1

Nonleguminous Plant

Frankia Frankia is a N2-fixed actinomycete. They form nitrogen-fixing nodules in a variety of nonlegume (actinomycetes) plants, such as Casuarina equisetifolia (Saravanan et al. 2012). These bacteria live in symbiotic partnerships with more than 200 plant species from eight families (Wall 2000; Tilak et al. 2005). These bacteria fix nitrogen from the atmosphere and transfer it to the soil in enormous volumes. The PlantFrankia Association is important for land reclamation, reforestation, restoration, and soil stabilization on an ecological level (Joel et al. 2001). Even under harsh conditions, Actinorhizal plants can grow quickly on nitrogen-deficient soils. They increase the productivity of agroforestry organizations used for timber, feed and firewood production, land restoration, and multipurpose cultivation (Schwenke and Caru 2001). 3.4.1.1.2

Leguminous Plant

Rhizobium Rhizobium is a kind of soil habitat bacteria that can colonize the roots of legumes and symbiotically fix nitrogen in the atmosphere. The morphology and physiology of rhizobia range from free-living state to tuberculosis bacteria. In terms of the amount of fixed nitrogen, they are the most effective biological fertilizers. They have seven genera and form nodules in legumes highly specifically, which are called crossinoculation groups. Inoculation with Rhizobium can add 50–230 kg N2 per acre. In this field, these nodules are thought to be miniature nitrogen-producing plants.

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Rhizobia supply nitrogen to the plant in an interdependent interaction, while the plant shields the bacteria from O2 by incorporating it in the nodular structure. Rhizobium organisms release biochemical substances, such as auxins, cytokinins, abscisic acid, luminescent pigments, riboflavin, lipochitooligosaccharides, and vitamins that promote plant growth (Dakora 2003; Matiru and Dakora 2004; Hayat and Ali 2004, 2010; Hayat et al. 2008a, b; Laranjo et al. 2014). Rhizobia also protects plants from pathogens and adverse environmental conditions (Ghosh and Basu 2002; Dakora 2003; Bardin et al. 2004; Matiru and Dakora 2004). Leguminous trees create a nodular structure with fast-growing rhizobia or the slow-growing Bradyrhizobium sp. and bioremediate N2 with 84,000 tons of nitrogen in the air per hectare of soil. Woody plants account for only 7200 of the 18,000 legumes, with just 18% forming nodular structures. Most Mimosa and Papilio plants have nodular structures, while only a few Caesalpiniaceae species have been documented to have nodular structures (Allen and Allen 1981; Brewbaker et al. 1982; Dobereiner 1984). In the case of crops, it is reported to have a strict symbiotic relationship with rhizobia. A wide range of Rhizobium species tend to form nodules in crops (Räsänen 2002). Rhizobium can survive in cold temperatures and can withstand temperatures of up to 50 °C for several hours. Plant protection agents and other biochemicals have an easy way affecting it. Under dry holding circumstances, it may persist in the soil for several years; however, the process by which it does so is unknown. Although numerous microorganisms and bacteriophages have been shown to impede the growth of rhizobia, the action of these antagonistic microorganisms seldom hinders the formation of nodules in nature. Rhizobium can live in saline-alkaline soil because it is more salt-tolerant than its host legumes (Kapadia et al. 2021). Rhizobia may live under adverse soil conditions even without a host plant (Odee et al. 2002). Rhizobium has a number of functions that help it adapt to adverse conditions.

3.4.1.2 3.4.1.2.1

Nonsymbiotic Nitrogen-Fixing Azotobacter

Azotobacter is Gram-negative bacteria that live freely in arable soils and fix atmospheric N2 in a nonsymbiotic manner. According to Kizilkaya (2009), Azotobacter can bio-fix roughly 20 kg nitrogen per hectare per year. A. chroococcum is the most common. Azotobacter relies on the excretions of plant roots, which include a variety of essential macromolecules such as amino acids, vitamins, and organic acids, to survive. They convert N2 to ammonia in the soil, which plants can use. These bacteria also produce and release nicotinic acid, thiamine, riboflavin, pyridoxine, pantothenic acid, cyanocobalamin, and gibberellins, IAA or gibberellin-like compounds (Kizilkaya 2009). Antifungal antibiotics are also produced, which suppress a range of soil fungus. It is also renowned for producing ether-soluble fungicidal chemicals, which prohibit bacteria from infecting plants. As a result, by preventing the growth of hazardous bacteria, these microorganisms naturally restrict the transmission of infection. These two properties of Azotobacter may explain why the

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microbes promote optimal seed germination (Sokolova et al. 2011). Its production of auxins, vitamins, growth-promoting chemicals, and antifungal antibiotics, in addition to its capacity to fix nitrogen, provides it with extra advantages. These characteristics are responsible for a significant increase in seed germination, plant development, and ultimately yield. Azotobacter is also identified to develop nodules to survive in harsh environments. A live cell with two coats is present in each cyst. Polyhydroxy butyric acid builds in the cyst. Resistance to heat, resistivity toward desiccation, and unfavorable circumstances have improved in these encapsulated cysts (Chadha et al. 2011). In favorable conditions, these cysts renew and produce microbial cells. Polysaccharides are also released, which aid in soil agglomeration. In Indian soils, the population of Azotobacter is impacted mostly by the presence of other microorganisms, and it ranges from 10,000 to 100,000 per gram. Some soil bacteria promote Azotobacter population, which boosts Azotobacter's bio-reduction of N2. Azotobacter growth has been demonstrated to be aided by cellulolytic bacteria, which decompose plant waste in soil. 3.4.1.2.2

Azospirillum

A microorganism belonging to the genus Azospirillum. It is one of the important microbes that is involved in the process of biological nitrogen fixation under aerobic circumstances, and it is commonly mixed with the roots and rhizosphere of a wide range of agricultural plants. Since they are ubiquitous in the rhizosphere, these are also considered to be associated with nitrogen-fixing bacteria. Azospirillum has been presented as a bacteria that promote plant development without being specialized (Bashan and Holguin 2004). They are called associative endosymbionts that promote plant growth (Okon 1985; Bashan and Holguin 1997). A. lipoferum and A. brasilense are the main inhabitants of the intercellular space of the soil, rhizosphere, and root cortex of gramineous plants. They form an associated symbiotic relationship with gramineous plants. Bacteria of the genus Azospirillum are nitrogenfixing organisms isolated from the roots and above-ground parts of various crop plants. They are gram-negative bacteria. Inoculation with Azospirillum provides additional benefits like as nitrogen fixation, the generation of growth-promoting chemicals such as indole-3-acetic acid (IAA), disease resistance, and drought tolerance. Despite having a nitrogen fixation capability of 1–10 kg per hectare, the increase in product output is mostly due to the release of growth-promoting biomolecules that promote root development and hence improve plant water and mineral absorption (Fallik et al. 1994; Okon and Kapulnik 1986). 3.4.1.2.3

Cyanobacteria

Cyanobacteria, often known as blue-green algae (BGA), are a kind of microbe that belongs to the Nostocales and Stigonematales families that can undertake photosynthesis and nitrogen fixation at the same time. They use nitrogenase to fix nitrogen in a nonsymbiotic way. Anabaena, Phalaenopsis, Aulosira, Caothrix, Plectonema, and other nitrogen-fixing blue-green algae are the most common (Mishra and Pabbi

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2004). In blue-green algae, nitrogen is fixed in “miscellaneous capsules,” which are unique cells. Somatic cells and miscellaneous capsules participate in the biological fixation of nitrogen. The heterocyst obtains the energy required for fixing nitrogen from the cells that perform photosynthesis and the heterocyst meets the nitrogen demand of the nutrient cells. Phosphate application can promote algae reproduction on clay for 2 weeks and sandy soil for 3–4 weeks (Subbarao 1997). Since cyanobacteria are photosynthetic, they have the added benefit of carbon fixation in addition to nitrogen fixation, which can feed any intact heterotrophic soil microorganisms.

Free-Living N2 Fixers

3.4.1.3 3.4.1.3.1

Azolla

Azolla is a sort of water fern that grows in puddles and ditches. It supports Anabaena azollae, an endosymbiont that thrives in association with algae that bio-fix atmospheric N2. But the major constraints are that it requires high amount of water to survive, for that it has limited scope in arid region. It has great potential in rice ecosystem.

3.4.2

The Phosphate-Solubilizing Biofertilizers

It is one of the plant’s important macronutrients. Elevated stalk and stem strength, enhanced flower formation and seed yield, more consistent and sooner crop maturity, increased N-fixing capacity of legumes, crop quality enhancement, and improved resistance to phytopathogens are just a few of the biochemical reactions that require phosphorus. It is also found in large amounts in seeds and fruits. Plant growth and development may be hampered if this essential mineral is deficient. Phosphorus makes up 0.2–0.08% of the dry weight of plants (Sharma et al. 2013). Phosphorus is also found in a variety of biomolecules such as nucleic acids, nucleotides, and phospholipids, and thus plays an important role in plant growth and development at all levels, from molecular to physiological and biochemical (Sharma et al. 2013). Many researchers have looked into the role of bacteria in phosphorus uptake (Sharma et al. 2016). Because of its limited solubility, phosphorus is a vital plant nutrient that must be made available to plants. Mineral P fertilizer causes quick fixation of phosphorus into insoluble compounds, and its consumption in India is insufficient. Due to its inferior quality, large reserves of rock phosphate in India go unused as fertilizer. Phosphorous-solubilizing biofertilizers have been proven to be effective at solubilizing phosphorus for plants, converting low-grade rock phosphate to fertilizer, and increasing crop output. Because soluble P is fixed with other insoluble phosphates of iron, aluminum, and calcium in the soil, its availability is relatively limited. The majority of phosphorus absorbed in the soil occurs in the form of phosphate anions H3PO42- and H3PO4-,which are dependent

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on the pH of the soil (McVickar et al. 1963; Mahdi et al. 2011). The rhizospheric soil is home to a diverse range of microorganisms, including bacteria and fungus, which are known to solubilize phosphorus (Roychoudhury and Kaushik 1989). Several reports show that soil containing phosphorous-solubilizing bacteria (PSB) has improved solubilization of soil P and applied phosphate thus resulting in better yields (Kumar et al. 2001; Venkateswarlu et al. 1984; Nautiyal et al. 2000). The synthesis of organic acids such as malic acid, lactic acid, fumaric acid, chelating chemicals (2-ketogluconic acid), humic substances, and different mineral acids such as sulfuric acids, etc., plays an important role in the entire phosphorus solubilization process (Illmer et al. 1995; Vassilev et al. 1996). The soil microbes that are said to effectively solubilize and mineralize the insoluble P are Pseudomonas spp., Agrobacterium spp., and Bacillus circulans (Babalola and Glick 2012),various strains of Azotobacter (Kumar et al. 2014), Bacillus (Jahan et al. 2013), Burkholderia (Istina et al. 2015; Zhao et al. 2014), Enterobacter, Erwinia (Chakraborty et al. 2006), and Kushneria (Zhu et al. 2011). Fungal species with similar functions include the strains of Chrothcium, Alternaria, Curvularia, Helminthosporium, Penicillium, and Trichoderma (Srinivasan et al. 2012). Therefore, the use of PSBs is a promising approach to solve the problems related to soil infertility and it improves food production by increasing yields (Babalola and Glick 2012).

3.4.2.1

Pseudomonas and Bacillus

Pseudomonas and Bacillus spp. are two of the most significant plant growthpromoting rhizobacteria among the many fungal pathogen antagonists. They provide a more ecologically sustainable way to boost agricultural output and overall wellness. Many plants' growth has been reported to improve significantly as a result of their application (Manasa et al. 2021). Dominguez et al. (2012) discovered that inoculating Pinus halpensis seedlings with the mycorrhizal fungus Tuber melanosporum and the rhizobacterium P. fluorescens CECT 844 increased seedling development and nutrient absorption under nonlimiting greenhouse conditions.

3.4.2.2

Arbuscular Mycorrhiza and Its Role in Agroforestry

Mycorrhiza that is the relationship of plant roots with fungus, is one of the most important members of this category of biofertilizers (Sieverding et al. 1991). Because they promote nutrient intake, release growth-promoting chemicals, and give tolerance to stress and salt, mycorrhizal fungi help host species develop better (Sreenivasa and Bagyaraj 1989). Ectomycorrhizas and endomycorrhizas are the two main forms of mycorrhizas. Ectomycorrhiza produces external fungal growth in the root cortex, whereas endomycorrhiza produces vesicles and arbuscules, which are inter and intracellular fungal components. Due to their characteristics, endomycorrhiza is also referred to as the vesicular-arbuscular mycorrhiza (VAM).

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VAM has been utilized as a biocontrol agent because it competes with diseases for space and nutrients, resulting in the production of antibiotics or the resistance of the host to pathogens (Berg et al. 2007). AM fungus is widely dispersed in India, with 14 different types of spores (Bakshi 1974). Currently, there are around 180 species of AM Fungi (Morton and Redecker 2001). The family Glomaceae (Pirozynski and Dalpé 1989), which comprises the genera Glomus and Sclerocystis, contains the bulk of known AMF. AMF boosts the host plant's intake of nutrients like N, P, K, Zn (Zinc), Cu (Copper), S (Sulfur), Fe (Ferrous), Ca (Calcium), Mg (Magnesium), and Mn (Manganese) (Marschner and Dell 1994; Smith et al. 1994; Abdul Mallik 2000). These fungi help to carbon storage in the soil by altering the organic materials in the soil (Rygiewicz and Andersen 1994). As a result, mycorrhizal fungi play a significant role in agricultural productivity and nutrient cycling (Smith and Read 2010). Arbuscular mycorrhizal fungi play a critical role in the decomposition of organic materials in soil, mineralization of plant nutrients, and nutrient recycling in dry habitats (Pare et al. 2000). Piriformospora indica (a mycorrhizal root endophyte) has gotten a lot of interest recently (Verma et al. 1998). It is a unique root invading endophytic fungus that can increase plant growth and biomass production. It was isolated from the rhizosphere of xerophytic plants in the Thar desert, India. Bryophytes, pteridophytes, gymnosperms, and many monocot and dicot plants are all hosts for the endophytic fungus (Fakhro et al. 2010; Verma et al. 2001).

3.4.3

The Potassium-Solubilizing Biofertilizers

Potassium is required by plants for numerous activities such as stomatal regulation and the activation of various enzymes such as starch synthesis, nitrate reduction, and energy metabolism. It is the seventh most common element on planet’s surface and the third most necessary nutrient (Almeida et al. 2015; Yang et al. 2015). It aids in the production of proteins and amino acids from NH4+ ions absorbed by the roots from the soil. It is also in charge of transporting carbs and proteins from the leaves to the roots. Although it is abundant in soil, only 1–2% of it is available to plants (Sparks and Huang 1985). The rest is bound with other minerals and is unavailable to the plants. It was revealed that the potassium (K)-solubilizing bacterium (KSB) is capable of extracting potassium from both physical and chemical sources (Ai-min et al. 2013). As a wide range of saprophytic bacteria, fungal strains, and actinomycetes complete the process of potassium solubilization, the plant rhizosphere contains a significant amount of KSB (Ahmad et al. 2016; Bakhshandeh et al. 2017). Certain bacterial spp. which has been described to be effective K solubilizers include Bacillus mucilaginosus, B. edaphicus, and B. circulanscan (Meena et al. 2016). The creation of a complex between organic acids and metal ions (Fe2+, Al3+, and Ca2+) leads to potassium solubilization as well (Styriakova et al. 2003). Organic acids such as oxalic acid, tartaric acid, malic acid, and citric acid have been found in KSBs, making them effective for releasing potassium from potassium-bearing minerals, according to several researchers (Hu et al. 2006; Keshavarz Zarjani et al. 2013; Sheng and He 2006). When the seed and seedlings were infected with the KSBs

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under greenhouse and field settings, there was a considerable increase in plant growth and yield, as well as K uptake and germination percentage (Zhang and Kong 2014).

4 Roadmap to Commercialization Green alternatives to traditional agrochemicals include bio formulations of compounds for plant growth stimulation, soil fertility, and phytopathogen control (Arora et al. 2016). The following steps suggest the commercialization of PGPR (Fig. 8.3).

5 Future Prospects and Challenges PGPR are now considered a safe agroforestry method because it can increase yields and because it has promising solutions for environmental safety. The most important thing is to protect plants from pesticides, which have negative consequences for the ecology. Plant diseases and insect pests account for one-third of plant losses, so PGPR can affect yield by reducing them. PGPR seem to have beneficial effects on laboratory and greenhouse experiments. An emerging field for improving and exploring PGPR strains is through genetic engineering, which can overexpress these traits to obtain strains with desired traits. In addition to all the progress, some environmental barriers and disadvantages affect PGPR activities. The problem of different efficacies can be achieved through strain mixing, improved inoculation technology, or the transfer of the active genetic source gene of the antagonist to the host plant. Different conditions will also affect PGPR as biological control because biological control agents need similar niches to grow and survive. Therefore, under different environmental conditions, the efficacy of the biological control agent can

Fig. 8.3 Roadmap to commercialization of PGPR

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be improved by using a compatible mixed inoculum of the biological control agent with consistent performance. In addition to its benefits, PGPR face some challenges. These changes could happen quickly and have an impact on the entire experiment. Another issue is that PGPR must reproduce in the field to maintain its vitality and biological activity. This kind of propagation might be seasonal or based on the plant type. Because isolating and characterizing PGPR in vitro does not appear to be easy, the challenge may be that the workplace should be highly sterile and proper equipment should be employed.

6 Conclusion The use of bacterial fertilizers has made significant improvements in plant growth, health, and yield. The mechanism of PGPR stimulation can be direct or indirect. PGPR also support growth by reducing plant pathogens that reduce yield and growth. The result of PGPR inoculation is greatly affected by plant age and soil chemical, physical, and biological characteristics. There are some challenges in using PGPR, such as natural mutation, but with advanced technology and applied biotechnology, the challenges PGPR face can be overcome. Therefore, the future prospects can be to replace chemical fertilizers and support the ecosystem in terms of safety. A better understanding of the complete mechanism of PGPR helps to obtain more specific strains that can work under more unfavorable and variable conditions.

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Chapter 9

Role of PGPM in Managing Soil-Borne Plant Pathogens in Horticulture Crops S. K. Maheshwari, D. G. S. Ramyashree, Anita Meena, Ritu Mawar, and D. L. Yadav

1 Introduction A bottleneck for production of horticultural crops is the plant diseases caused by soil-borne phyto-pathogenic fungi affecting seeds from germination and throughout development. Consequently, up to 30% yield reductions have been reported (Das et al. 2015). There have always been attempts to combat with the problems of management of soil-borne plant pathogens using fungicides/chemicals. Plant growth promoting microorganisms (PGPM) have importance due to their dual benefits of managing plant diseases as well as promoting plant growth and are used as microbial inoculants in improving of productivity of agricultural produce. Use of PGPM and their mixtures and integration has much useful in various disease management problems. Practical use of PGPM-based products has several formulations which are made available in commercial scale. Microorganisms constitute the major players in the rhizosphere, and their composition and biomass significantly alter the plants response to the environment. In recent years, a substantial amount of work has been done in the area of PGPM. There are numerous species of PGPM which flourish in the rhizosphere of the crops, shrubs and trees but which may grow in or S. K. Maheshwari (*) ICAR-Central Institute for Arid Horticulture, Bikaner, India Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India D. G. S. Ramyashree · A. Meena ICAR-Central Institute for Arid Horticulture, Bikaner, India R. Mawar Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India D. L. Yadav Kota Agricultural University, Kota, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_9

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around the tissues of these plants and stimulate plant growth that is why we can collectively pronounce as PGPM. Some PGPM are promoting plant growth by supporting as both bio-fertilizer and bio-pesticide. Mode of PGPM includes N fixation, augmenting the availability of nutrients in the rhizosphere, influencing root growth, nodulation and other beneficial plant microbe symbiosis. The research for these beneficial microorganisms is very interesting day by day as a rapid fire and is made to exploit them commercially as bio-pesticide. This chapter discusses the role of PGPMs in enhancing productivity of arid and semi-arid horticultural crops by effectively addressing of important biotic constraints associated. Additionally, how the ways in PGPMs help horticultural crops in overcoming harsh climatic conditions existing in arid and semi-arid regions are also reviewed.

2 Plant Rhizosphere and Microorganisms The root of the plants is surrounded by the soil which contains microbe ‘storehouse’ also called as rhizosphere (Gouda et al. 2017). Based on their interaction with plants, PGPMs viz., rhizobacteria, actinomycetes, fungi and endophytes in the rhizosphere can be symbiotic showing direct beneficial interaction with plant or non-symbiotic action (Kundan et al. 2015). The root system acts as a chemical factory which is synthesized and releases the phenolic compounds to carry out other underground interactions in rhizosphere (Gouda et al. 2017). A large number of microbial communities or populations are attracted to the plant’s roots by these chemical compounds and different types of mechanisms (Souza et al. 2015). The physiological status of plants affects the chemical composition. The rhizospheric zone is made up of the rhizoplane and the root itself. The PGPMs growth promoting activity around the rhizosphere is regulated and affected by the release of various chemical compounds. The rhizoplane and root surface strongly interact with rhizospheric soil for the colonization of soil-borne microorganisms and PGPMs (Barea et al. 2005). There is a competition among rhizosphere microbes for the nutrients’ utilization and mobilization in order to maintain their beneficial effects on the sustainable agriculture and environment. The main interaction between rhizospheric microbes and plants, mainly bacteria, fungus and arbuscular mycorrhiza fungi (AMF), plays an important role in obtaining water and nutrients from the rhizospheric zone and soil. Soil quality and plant growth are directly affected by the microbes of soil. This characteristic feature of microbes has grabbed the attention of people involved in enhancing the plant growth using microorganisms for sustainable development, because the microbes are present in this environment and beneficial for plant development. Presently, PGPM include representatives from very diverse fungal and bacterial taxa.

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3 Plant Growth Promoting Rhizobacteria PGPRs microbial population mainly promote plant health, they stimulate growth promoting activity directly by changing and producing the plant growth regulators concentrations (Suman et al. 2016) like cytokinins, GA, IAA, etc. In that case, auxins are the main key hormones which control plant health and growth. The ability to produce ACC-deaminase (ACCD) is to reduce the ethylene production level in the roots system of the growing plants (Dey et al. 2004), asymbiotic nitrogen fixation, antagonism activity by producing antibiotics, siderophores, fluorescent, pigment, chitinases, micro-macro nutrients mobilization and solubilization, thereby increasing the plant growth (Glick 1995). Pathogenic microorganisms can affect the plant health on a major scale. Antibiotic, anti-fungal metabolites, enzyme, plays a key role for enhancement of plant health and development of crop production in agriculture. Many rhizospheric microbial genus are being used like Pseudomonas, Azotobacter, Bacillus, Rhizobium, Azospirillum, Enterobacter, Caulobacter, Micrococcous and Chromobacterium. It is reported that about 2–5% rhizo-bacteria are involved in the PGP activity. One of the most important PGPM of the microbial network present in the rhizospheric is actinobacteria or actinomycetes which assume a crucial job in soil supplement cycling (Franco-Correa et al. 2010). They are the producers of biologically compounds like metabolites, antibiotics, enzymes and vitamins. Streptomyces and Micromonospora are the most commonly described actinomycetes. To date, the largest bioactive source of natural products is Streptomyces. Actinomycetes are the producers of two-third of natural antibiotics out of which 75% is produced by Streptomyces genus due to their ability to sustain in harsh soil conditions.

3.1

Endophytes

Endophytes can protect host plants from fungal pathogens and others. Nitrogen fixation can result in growth stimulation by endophytes synthesis of various plant hormones such as cytokines and IAA, antagonistic activity of plant pathogens by the formation of antifungal-bacterial agents, siderophore production and induction of the acquired host resistance. Endophytic PGPM colonization may result in improved plant growth and it provides tolerance against various stresses such as biotic and abiotic. They can be used as bio-regulators and biological control agents to induce resistance against diseases and certain plant pathogens, respectively.

3.2

Plant Growth Promoting Fungus

Several research articles and reviews on PGPF have shown that species of sustainable agriculture beneficial fungi belonging to the genus are being used like

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Penicillium, Fusarium, Penicillium, Mycorrhiza, Phoma, Gliocladium, Metarhizium, Trichoderma, Colnostachysrosea, Phythium and Aspergillus. Majority of the reviews on PGPF have been done to understand the mechanisms stimulating plant growth. The hormones production by PGPF and these hormones allow plants and soil interaction to decompose the organic matter through mineral solubilization. The most important characteristics of PGPF are colonization of the roots which help them in microbial interaction mechanisms to enhance productivity and protection of host. These PGPM can be used for fungal and other disease control. Soil microorganisms secrete a potent enzyme, which destroys other cells by digesting their cell walls, and degrade the cellular material as well as released protoplasmic material. Aspergillus has an antagonistic effect on Cladosporium and Penicillium as well as Pseudomonas on Cladosporium. An attempt was discussed to explore the potential of native microflora especially PGPM that are capable of managing soil-borne plant pathogens (Pythium sp., Phytopthora sp., Rhizoctonia sp., Fusarium sp. and Macrophomina phaseolina) in horticultural crops. This chapter discusses the role of PGPMs in enhancing productivity of arid and semi-arid horticultural crops by effectively addressing of important biotic constraints associated. An overview of impact of PGPM in plant growth promotion and management of plant diseases and their pathogens, focusing attention on the development and application of biological control strategies is mentioned. It will help to reduce the usage of inorganic fertilizers and also fungicides if these PGPMs are used as a bio-inoculum or bio-fertilizer on plant and environment that will give more natural food for human welfare.

4 Bio-control for Managing Soil-Borne Plant Pathogens Biological control of plant diseases can be defined by the use of living organisms to depress plant pathogen activities (Fig. 9.1). Bio-agents are natural inhabitants of the soil and the environment. Trichoderma is reported to be one of the most widely distributed soil fungi which protects plant against pathogens by exploiting their antagonistic potential. It also induces plant-mediated systemic resistance against above ground microbial pathogens. The use of PGPM as a biocontrol agent has become an effective method of crop protection (Lodha and Mawar 2010). Trichoderma is a potent biocontrol agent applied extensively for management of soil-borne plant pathogens in horticultural crops. Trichoderma viride and Trichoderma harzianum are also used as seed treatment, bio-priming, foliar spraying and soil treatment. Trichoderma species are fast growing, prolific spore producers and powerful antibiotic producers. Effectiveness of Trichoderma viride against important fungal pathogens like Alternaria, Colletotrichum, Phytophthora, Pythium, Rhizoctonia, Sclerotinia, Verticillium, etc. The dual culture technique described by Morton and Stroube (1955) was used to test the antagonistic ability of Trichoderma spp. against Sclerospora rolfsii. The

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FROM NATURE TO NATURE’ Selection of efficient antagonistic microbes against pathogen and apply BIO-CONTROL AGENTS for Managing Soil borne Phyto Pathogens

Fig. 9.1 Mechanism of biocontrol agents against phytopathogens

potential of rhizosphere microflora for the biological control of Phytophthora colocasiae causing taro (colocasia) leaf blight was studied (Sriram et al. 2003). Methods of biological control provide plant protection against fungal diseases and also horticultural protection against soil-borne plant pathogens. In one of the field experiments on management of powdery mildew using native isolates of Trichoderma (CIAH-240) and Pseudomonas fluorescens (CIAH-196) with 50% less concentration than recommended dose of fungicides was worked out. Spray of bioagents on susceptible cultivars (Gola and Umran) at the pea stage at monthly intervals resulted in 90.7% control. Spraying 5% culture filtrate of Trichoderma (CIAH-240) followed by spray of conidial suspension of Trichoderma (5 and 10%) spray resulted in 82.2 and 83.2% control, respectively. In case of cv. Gola per cent control efficacy was 95.8 by combined application of P. fluorescens and 0.05% Karathane (Nallathmbi et al. 2003). Therefore, it seems that the PGPMs can have great importance as an alternative component in integrated disease management.

4.1

Criteria of Selection and Identification of a Biological Control Agents

Bacterial communities show antagonistic effects toward phytopathogens which can be exploited in biological control. The mechanisms of action are involved in BC activity for the safe development of the application processes and as a basis for selecting the most efficient bacterial strains (Nikolić et al. 2019). They are identified by chemical and molecular biology methods, and several tests to determine safe the environment, plants, and human and animal health (Liu et al. 2013).

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Siderophores

Wilt diseases in horticulture crops were suppressed strongly by high-fluorescent siderophore producers. The most important mechanism by Pseudomonas spp. is siderophore-mediated competitions for iron. Antagonistic activity of Pseudomonas spp. in the rhizosphere has suppressed many plant pathogens. Strains of Ps. fluorescens showed biological activity against certain soil-borne phyto-pathogenic fungi and produce secondary metabolites (siderophore and protease) having antagonistic activity against Rhizoctonia solani, Phythium sp. and Fusarium sp. Fruit rots are not a major problem in different parts of the country, but in arid regions these are the major problem than the powdery mildew in ber. Nallathmbi and Thakore (2003) studied in detail about different kinds of rots due to various fungal pathogens and found that in almost all the major varieties of ber growing in arid regions, different types of fruit rots occur. The cumulative analysis of data from 2-year survey of ber orchards in different locations of arid region revealed that the fruit rot infection index was up to 20–25% with the total yield loss up to 20–30%. Therefore, native PGPMs were explored to manage the rots. Different native isolates of Trichoderma inhibit the pathogen by different mechanisms. The superior isolate CIAH-240 was found mycoparasitic as well as secreted toxic metabolites. Some of the isolates secreted antifungal metabolites in growth medium to suppress A. alternata. Out of 14 native bacterial isolates, CIAH-196 inhibited maximum mycelial growth. Production of toxic metabolites like phenazine, pyocyanin and pyrrolnitrin and lytic enzymes is the characteristic features in virulent strains of P. fluorescens. Interestingly, sporulation of test pathogen was suppressed by some of the native isolates. P. fluorescens isolates viz., CIAH-226, SBI-48 and SBI-62175 could secrete the siderophores (yellowish pink), which checked the mycelial growth of the pathogen.

4.3

Antibiosis

The condition in which one or more metabolites excreted by an organism have a harmful effect on one or more other organisms. They produced in soil may be absorbed by plant roots. Antibiosis can also be performed through the production of volatile organic compounds having direct effect to soil-borne phyto-pathogens. The main antagonistic bacterial antibiotics are iturin, antifungal peptide, produced by Bacillus subtilis, and pyrrolnitrin, produced by Ps. cepacia. Bajoria et al. (2008) isolated B. subtilis, B. cereus, B. pumilus and B. sphaericus from hot arid region having biocontrol potential against many phyto-pathogenic fungi. Presence of certain compounds in crucifers and release of volatiles during their hydrolysis could be attributed for stimulating multiplication of Bacillus firmus. Development of scarlet colour of bacterial colony and formation of inhibition zone against Macrophomina indicated release of some antibiotic after interaction of both the microorganisms in the media, a phenomenon attributed to antibiosis. However, B. firmus has shown

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high-specific antagonistic activity only against M. Phaseolina (Lodha et al. 2013). Absence of scarlet pigmentation in interactions with other fungi further supports that antibiotic is exclusively present only in this pigmentation. The possibility of production of this active principle only in response to stimulation by some metabolites of extra cellular nature from pathogen can be expected.

4.4

Parasitism and Induced Resistance

Once Trichoderma is introduced into soil, it grows rapidly by consuming essential nutrients from the soil environment that other soil inhibiting organisms fail to compete with it and, finally, is killed due to competition and scarcity of food. Another mechanism of biocontrol by Trichoderma is induced resistance in plants (Elad et al. 1982). Species of Trichoderma are known to solubilize rock phosphate, metallic zinc, manganese, iron and copper, and also enhances the nitrogen use efficiency in plants. Because of these properties, the Trichoderma not only becomes a bioagent for disease control but also an agent which enhances the growth of plants by providing soil nutrition in soluble forms for absorption by the roots resulting in better health of plants. A native heat tolerant strain of Trichoderma has been isolated from arid soils. This isolate was found effective against many soilborne plant pathogens.

4.5

Management of Phyto-pathogens of Horticultural Crops Through PGPM Including Antagonistic Activities

Potential bio-control agents were effective against Fusarium oxysporum f. sp. Melonis causing Fusarium wilt of melon (Cucumis melo L.). The most common species, F. oxysporum, causes vascular wilt disease in a wide variety of economically important crops (Beckman 1987). Ahn and Hwang (1992) isolated actinomycetes that were antagonistic to Phytophthora capsici from rhizosphere soils in chilli growing areas. Similarly, soil treatment with three Sri Lankan bacteria, Brevibacterium linens (DF-3101), Bacillus thuringiensis (DF-7197) and B. Pumilus (DF-1481) in greenhouse studies, suppressed the disease on cowpea caused by Phytophthora vignae (Fernando and Linderman 1995). However, Bacillus sp. Str. C18 protected tomato plants against infection by Botrytis cinerea and Phytophthora infestans (Sadlers 1996). Similarly, by using Bacillus amyloliquefaciens CPA-8 under field conditions was found very effective against brown rot in stone fruit (Gotor-Vila et al. 2017). Pan et al. (1997) reported that Trichoderma viride, T. harzianum and Gliocladium virens isolates were antagonistic to Phytophthora colocasiae and they found that mycoparasite activities of these

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bio-agents were brought about through several morphological changes. Eight isolates were tested for their antagonistic ability against pathogenic cultures; however, only one isolate fluorescent Pseudomonas showed antagonistic activity with 52.6 and 61.8% inhibition after 5 days against Botryosphaeria ribis causing stem bark canker and Dematophora necatrix causing white root rot of apple, respectively. This fluorescent Pseudomonas isolate also exhibited moderate phosphate solubilizing activity and tested positive for siderophore production (Krishna et al. 2014). In case of Pseudomonas sp. AF7, highest antifungal activity against Aspergillus flavus and A. niger, F. oxysporum, respectively was tested (Das et al. 2015). Endophytic bacteria have isolated from banana and prepared talc-based formulation and applied bacteria against management of soil-borne (wilt) pathogen. The talc-based bioformulation of T20 mutant of T. asperellum strain used as a soil treatment was able to manage effectively the foot rot or gummosis of citrus and also exhibited the high yield in Kinnow orchards of Abohar region (Choudhary et al. 2021). Similar results have been achieved by T. harzianum (AZNF 4) strain in Prosopis cineraria in arid region (Mawar et al. 2021). Wilt in cucurbits (muskmelon) can be suppressed by Pseudomonads isolates. Antagonistic bacterium could effectively inhibit the occurrence of Botrytis cinerea after tomato harvest and E. cowanii has biocontrol potential against B. cinerea after harvest of fruits and vegetables (Shai and Sun 2017). Paenibacillus jamilae HS-26 has a high-antagonistic activity against several soilborne pathogens. The bacterium released extracellular antifungal metabolites for inhibiting fungal mycelial growth (Wang et al. 2019).

5 Search for New Antagonists Endophyte microorganisms including bacteria against phytopathogens are promising candidates for bio-control strategies. Bibi et al. (2018) reported that compost produced secondary metabolites for phyto-pathogen control.

6 Future Research Need Identification the efficacy of PGPM, botanicals and bio-agents against major diseases including soil borne of horticultural crops. The rearing feasibilities of the promising bio-agents should be explored in the natural field conditions. Collaboration between Research Institutes and Pesticides Industries for developing new molecules for their commercialization.

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7 Conclusions PGPM is the new approach for controlling the losses by soil-borne fungal and other plant pathogens, and for reducing the pollution that results from the use of chemical fungicides. The use of antagonists as an alternative to synthetic products has been a focus of research worldwide. Fungi and bacteria showed a significant antagonistic activity toward different soil-borne phyto-pathogenic fungi. These isolates were synthesized antifungal agents which act to protect plants against pathogenic fungi. PGPM including biological control agents play an important role in managing soilborne plant pathogens, owing to their capabilities of crop-yields by multiple role (bio-pesticides and plant growth promotion). Faster metabolic rates and antimicrobial metabolites are the key factors which chiefly contribute to antagonism against fungi. Mass multiplication of PGPM including effective fungal and bacterial isolates will help in managing soil-borne plant pathogens of horticultural and other crops. Exploitation of interesting PGPM including BCAs would be maximized in future.

References Ahn SJ, Hwang BK (1992) Isolation of antibiotic-producing actinomycetes antagonistic to Phytophthora capsici from chilli growing soils. Kor J Mycol 20:259–268 Bajoria S, Varshney AK, Pareek RP, Mohan MK, Ghosh P (2008) Screening and characterization of antifungal guar (Cyamopsis tetragonoloba) rhizobacteria. Biocontrol Sci Technol 18:139–156 Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778 Beckman CH (1987) The nature of wilt diseases of plants. American Phytopathological Society, St Paul, MN Bibi F, Strobel GA, Naseer MI, Yasir M, Khalaf Al-Ghamdi AA, Azhar EI (2018) Halophytesassociated endophytic and rhizospheric bacteria: Diversity, antagonism and metabolite production. Biocontrol Sci Technol 28:192–213 Choudhary AK, Singh N, Singh D (2021) Evaluation of potent native strains of Trichoderma spp. Against the foot rot/gummosis of Kinnow mandarin. Egypt J Biol Pest Cont 31:90 Das MP, Devi PV, Yasmine Y (2015) A study on antagonistic potential of bacteria against phytopathogenic fungi. Int J Pharm Sci Rev Res 34(1):191–193 Dey RKKP, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159(4):371–394 Elad Y, Chet I, Henis Y (1982) Degradation of plant pathogenic by Trichoderma harzianum. Can J Microbiol 28:719–725 Fernando WGD, Linderman RG (1995) Inhibition of Phytophthora vignae and stem and root rot of cowpea by soil bacteria. Biol Agric Hortic 12(1):1–14 Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea JM (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45(3):209–217 Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41(2): 109–117

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Gotor-Vila A, Teixidó N, Casals C, Torres R, De Cal A, Guijarro B, Usall J (2017) Biological control of brown rot in Stone fruit using Bacillus amyloliquefaciens CPA-8 under field conditions. Crop Prot 102:72–80 Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2017) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206: 131–140 Krishna H, Grover M, Das B, Attri BL, Maheshwari SK, Ahmed N (2014) Antagonistic activity of Pseudomonas isolate against stem bark canker and white root rot of apple. Ann Plant Prot Sci 22(2):452–454 Kundan R, Pant G, Jadon N, Agrawal PK (2015) Plant growth promoting rhizobacteria: mechanism and current prospective. J Fertil Pestic 6(2):9 Liu J, Sui Y, Wisniewski M, Droby S, Liu Y (2013) Utilization of antagonistic yeast to manage postharvest fungal diseases of fruit. Int J Food Microbiol 167:153–160 Lodha S, Mawar R (2010) Efficacy of native bio-control agents on soil microflora, dry root rot incidence and seed yield of rainfed arid crops. Indian Phytopathol 61:313–317 Lodha S, Mawar R, Chakarbarty PK, S B (2013) Managing Macrophomina phaseolina causing dry root rot of legumes by a native strain of Bacillus firmus. Indian Phytopathol 66(4):356–360 Mawar R, Deepesh Sharma, Ladhu Ram (2021) Potential of biocontrol agents against Ganoderma lucidum causing basal stem rot in mesquite (Prosopis cineraria) growing in arid region of India. J For Res 32:1269–1279. https://doi.org/10.1007/s11676-020-01161-3 Morton DT, Stroube NH (1955) Antagonistic and stimulatory effect of microorganism upon Sclerotium rolfsii. Phytopathology 45:419–420 Nallathmbi P, Thakore BBL (2003) Management of ber (Zizziphus mauritiana Lamk) fruit rot using fungicides. J Mycol Plant Pathol 33:503 Nallathmbi P, Umamaheswari C, Joshi HK, Dhandar DGBS (2003) Management of ber (Ziziphus mauritiana Lamk) powdery mildew using Fluroscent Pseuomonads. In: Proc. 6th International workshop on plant growth rhizobacteria, pp 184–187. Held at Indian Institute of spices research, Calicut, Kerala, India, 5-10 October Nikolić I, Berić T, Dimkić I, Popović T, Lozo J, Fira D, Stanković S (2019) Biological control of Pseudomonas syringae pv. aptata on sugar beet with Bacillus pumilus SS-10.7 and Bacillus amyloliquefaciens (SS-12.6 and SS-38.4) strains. J Appl Microbiol 126:165–176 Pan S, Ghosh SK, Pan S (1997) Antagonistic potential of some soil fungi on Phytophthora colocasiae Racib. J Mycopathol Res 35(2):153–157 Sadlers HM (1996) Use of bacteria in controlling Bacillus sp. Str. C18 protected tomato plants against infectionungal diseases. Gemuse Muchen 32:180–181 Shai JF, Sun C-Q (2017) Isolation, identification, and biocontrol of antagonistic bacterium against Botrytis cinerea after tomato harvest. Braz J Microbiol 48(4):706–714. https://doi.org/10.1016/ j.bjm.2017.03.002 Souza RD, Ambrosini A, Passaglia LM (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38(4):401–419 Sriram S, Misra RS, sahu AK, Maheshwari SK (2003) Rhizobacterial: potential biocontrol agents against taro leaf blight pathogen Phytophthora colocasiae. J Root Crops 29(1):50–53 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Microbial inoculants in sustainable agricultural productivity. Springer, New Delhi, pp 117–143 Wang X, Li Q, Sui J, Zhang J, Liu Z, Du J, Xu R, Zhou Y, Liu X (2019) Isolation and characterization of antagonistic bacteria Paenibacillus jamilae HS-26 and their effects on plant growth. Biomed Res Int 2019:3638926. https://doi.org/10.1155/2019/3638926

Chapter 10

The Use of Plant Growth Promoting Microorganisms in the Management of Soil-Borne Plant Pathogenic Organisms Ayodele Martins Ajayi and David Babatunde Olufolaji

1 Introduction Plant disease is any deviation from normal growth or structure that is caused by biotic or abiotic agents, and that is sufficiently pronounced and permanent as to produce visible symptoms and to impair quality and economic value (Stackman and Harrar 1975). The biotic agents that incite plant diseases are called pathogens or pathogenic organisms. Pathogenic organisms are found in air (air-borne), water (water-borne) and soil (soil-borne) amongst others. Diseases of plants that result from contact with the inoculum of pathogens that inhabit the soil are called soilborne diseases (SBD). Soil-borne diseases of plants (SBDP) are known to cause significant annual yield losses in crops globally. Africa is one of the worst hits, owing to the subsistent nature of farming and crop production in most parts of the continent. The situation is made worst by the fact that most farmers have very little knowledge of the existence of these soil-borne plant pathogens. In places where adequate knowledge of their existence exists, there is a near-total reliance on synthetic chemicals that are used as soil treatment agents, for their management. Apart from not being economical, this practice is also associated with several health hazards and ecological issues. Plant growth-promoting microorganisms (PGPM) inhabit and grow freely in soils where conditions are favorable. In their natural state, they occupy the rhizosphere and protect plant roots against invading soil-borne pathogens. Some infect plant roots as biotrophs, form symbiotic relationships with their hosts and enhance nutrient availability, thus boosting the tolerance of crops to infection and disease. Others act as endophytes that confer protection on host plants against plant pathogens. Lately, attention has shifted to these beneficial microorganisms in the management of plant diseases. These biocontrol organisms are

A. M. Ajayi (*) · D. B. Olufolaji Department of Crop, Soil and Pest Management, The Federal University of Technology, Akure, Ondo State, Nigeria © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_10

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particularly best suited for the management of some SBDP that are often very difficult to manage with conventional chemical control agents. The numerous advantages associated with this method of plant disease control have endeared it to conservationists, environmentalists and medical practitioners. The level of awareness and adoption of these novel disease control strategies are, however, still very low in most African countries. It is hoped that this will change in no distant future.

2 Groups of Microorganisms That Incite Soil-Borne Diseases of Crops (SBDC) 2.1

Fungi

The most common soil-inhabiting group of microorganisms that incite diseases in crops are fungi. Fungi in the genera Aspergillus, Ceratocystis, Fusarium, Macrophomina, Sclerotium, Verticillium and Pythium are amongst the most common disease-causing organisms. They are found in almost all soil types and agroecologies. They produce mycelia that grow extensively in the soil, infecting the sub-aerial parts of plants from one season to another, especially when environmental conditions are favorable. The symptoms of these infections are as varied as the infecting fungi themselves. Germination failure, damping-off, root rot, root necrosis, wilt and chlorosis are some of the most common. Some of these fungi produce resistant structures such as chlamydospores, teliospores and sclerotia, that aid their survival during periods of adverse environmental conditions and absence of susceptible hosts. These resting stages have thick layers made up of lipid/protein. The protective layer can detoxify harmful chemicals and protect the DNA and other constituents of the spore from damage. Some of these resting stages can survive and remain infective in soil for several years (Couteaudier and Alabouvette 1999).

2.2

Bacteria

Bacteria, though with less incidence when compared to fungi, also form an important group of soil-borne pathogens (SBP). Diseases incited by bacteria are mostly vascular in nature and may be very severe and difficult to manage. They are characterized by soft rot, wilting, chlorosis, premature defoliation and death of infected plants. Members of the genus Rhizoctonia, Erwinia, Agrobacterium and Streptomyces are some of the common examples. Soil-borne plant pathogenic bacteria survive from one cropping season to another on the debris of infected plants, protected from dehydration and other unfavorable environmental condition by a thick mass of their dead cell and the dead tissues of the host plants. A new cycle of infection is initiated after the disintegration of the debris and the release of the surviving cells.

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Nematodes

Nematodes are an integral part of soils in Africa. Their diversity and population vary from one agro-ecology to another, depending on soil type, vegetation, soil moisture, pH and other physicochemical and environmental factors. Plant-parasitic nematodes pierce root hairs with their stylets and force their way into the intercellular spaces to obtain nutrients. Water and nutrient absorption in the infested plant is disrupted as a result of the disintegration of the middle lamella, hyperplasia and gall formation. Members of the genera Meloidogyne, Scutellonema, Heterodera, Ditylenchus and several others are common parasites of plants in Africa. The symptoms they produce on infested plants are similar to and are often confused with those of fungal, bacterial and viral infections. These symptoms include wilting, chlorosis and poor growth amongst others. Some species of plant-parasitic nematodes survive from one cropping season to the other by hiding in plant’s tissues. Long-term survival is achieved through cryptobiosis, a resting state characterized by decreased surface area and cuticular permeability.

2.4

Viruses

Soil-borne viral pathogens of crops are less studied, compared to aerial ones, in Africa, and little information is available about them. This, however, does not suggest that the diseases they cause are of less significance. Common genera of soil-borne viruses include Necrovirus, Nepovirus, Ophiovirus, Tombusvirus and Varicosavirus. Just like aerial virus, soil-borne plant pathogenic virus requires vectors and openings, natural or wound, to gain entrance into their hosts’ tissue. Fungi, Plasmodiophorids and Nematodes are examples of such vectors. Symptoms of infections are diverse but consistent with those of aerial viral pathogens. For shortterm survival, some of these viral pathogens infect several hosts, while others remain as propagules on the dead tissues of their hosts. Long-term survival is through adsorption into colloidal particles of clay, where they retain their infective ability for a long period. Others form a close association with the resting/resistant stages of fungi and can remain dormant for several years.

3 Dispersal of SBDC The infestation of soil with pathogenic organisms and their dispersal occurs through several means, animate and inanimate. Animate means can be through the activities of man, such as the movement of infested soil, attachment to farm tools and machinery, from one location to another. It can also be through planting of infected seeds/seedlings and the use of infected plants and crop debris as mulch materials.

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Nomadic cattle, borrowing rodents and birds are also important agents of dispersal. These cattle move several kilometres in the savannah region of Africa, transferring muddy soil from one location to the other with their hoofs. Burrowing rodents infest soil with their claws and hairs, while birds disperse infected seeds they feed on through their droppings. Moving water, from rain or irrigation, is an important inanimate agent that can disperse SBP from one location to another. Wind can move fungal spores and resistant/resting stages of some pathogens to a considerable distance, especially during dry weather. These propagules eventually find their way into and infest soil in new locations.

4 Incidence of SBDC in Africa Soil-borne diseases of crops (SBDC) are found across almost all the agrological zones of the continent where farming activities occur. Painfully, however, most farmers in rural communities have very little knowledge of the presence of the pathogens that incite them, probably because of the microscopic nature of these pathogens. Some of the symptoms that characterize infections from these pathogens are usually mistaken for nutrient deficiency or declining soil fertility. Weirdly, some locals even regard these diseases as some kind of punishment meted out by an angry god on his subjects for their wrongdoings or for failing to give him his desired reference (Westerlund 2006). In urban African communities where some knowledge of SBP and their associated diseases exists, the use of crop debris as mulch materials and mechanized land ploughing has helped to disperse and perpetuate some of these soil-borne plant pathogens (SBPP). Almost all the crops grown in the continent are known to be host to one or more SBP (Table 10.1). Yam, a popular tuber commonly cultivated in West Africa, is susceptible to yam dieback and soft rot diseases (Rhizoctonia solani and Erwinia carotovora pv. Carotovora, respectively), while maize, a popular staple crop in East Africa, is susceptible to seedling damping-off (Curvularia eragostidis). Tomato, a crop that thrives in the savannah region of the continent, especially during the cooler months is host to bacterial and fungal wilt pathogens (Ralstonia solanacearum and Verticillium albo-atrum, respectively). The list is almost endless (Table 10.1).

4.1

Implications of SBD on Crop Growth and Productivity

Germination and seedling failure, necessitating replanting with attendant extra cost, crop failure, poor growth and yield loss are some of the problems associated with infections from SBD. These diseases have contributed significantly to hunger, starvation, food insecurity and migration of unskilled labor with its associated socio-economic problems. The loss of income, resulting from poor harvest, has also contributed greatly to the problem of poverty and financial insecurity for

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Table 10.1 Selected crops cultivated in Africa and some of their SBD Crops Banana (Musa paradisiaca)

Diseases Fusarium wilt Root necrosis/lesion

Cassava (Manihot esculenta)

Cassava root rot

Cocoa (Theobroma cacao)

Cocoa brown root rot Cocoyam root rot

Cocoyam (Colocasia esculenta) Cowpea (Vigna unguiculata) Maize (Zea mays)

Onion (Allium cepa) Pepper (Capsicum annuum) Rice (Oryza sativa) Tomato (Solanum lycopersicum)

Sugarcane (Saccharum officinarum) Sweet potato (Ipomea batata) Yam (Dioscorea alata)

Charcoal rot Seedling blight Seedling damping off Basal rot Pepper root rot Rice root rot Bacterial wilt Fusarium wilt

Causative organisms (soil-borne) Fusarium oxysporum f. sp. cubense Radopholus similis Helicotylenchus multicinctus Fusarium spp. Botryodiplodia theobromae Phellinus noxius Pythium myriotylum Fusarium solani Macrophomina phaseolina Rhizoctonia solani Curvularia eragostidis

Verticillium wilt Sett rot

Fusarium oxysporum f. sp. cepae Rhizoctonia solani Fusarium verticillioides Ralstonia solanacearum Fusarium oxysporum f.sp. lycopersci Veritcillium albo-atrum Ceratocystis paradoxa

Sweet potato soil rot Yam dieback Yam soft rot Yam dry rot Tubber galling

Streptomyces ipomoea Rhizoctonia solani Erwinia carotovora pv. carotovora Scutellonema bradys Meloidogyne incognita

many farmers. These problems were highlighted in the work of Okonya et al. (2019), who reported on the impact of pests and diseases of roots tubers and bananas on the income and livelihood of farmers in Rwanda and Burundi. The cocoa black pod rot disease has impoverished many cocoa farmers and brought about a decline in the revenue and foreign exchange earning of some West and East African countries (Table 10.1). It has also led to instability in the price of chocolate in some countries in Europe and America that depend on cocoa imports from Africa (Bowers et al. 2001).

4.2

Management of SBDC in Africa

4.2.1

Bush Burning and Land Fallowing

Some cultural practices and farming systems operated by traditional African farmers may have kept some soil-borne pathogens of crops (SBPC) at bay. One of such

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practices is the burning of cleared vegetation and crop debris before planting, a system sometimes referred to as slash and burn (Olufolaji and Ajayi 2021). This practice destroys pathogen’s inoculum in crop residue and prevents them from building up in the soil. Reports from other parts of the world also point to this fact. The burning of debris from rice and wheat was reported to have brought about a significant reduction in the incidence of stem rot disease of rice (Sclerotium oryzae), in many Asian countries, and flag smut disease of maize (Urocystis agropyri) in Australia, respectively (Dale and Ogle 1997). The heat generated during burning is also deleterious to some SBP and their propagules, especially fungal spores on the soil surface. Similarly, land fallowing, a practice that was common in the traditional African farming system in the past, may have contributed significantly to the reduction or outright elimination of inoculum of some SBP. The non-availability of susceptible hosts during the fallow period starves obligate SBP of nutrients and ultimately bring about their death (Olufolaji and Ajayi 2021). Dale and Ogle (1997) also reported on the successful management of Pseudocercospora herpotrichoides, in many parts of the world, through land fallowing. It is worthy of note, however, that burning has several undesirable effects on the soil, environment and the natural ecosystem. Decreased biodiversity and loss of soil nutrients are two of the most serious consequences of large-scale bush burning. Others include the destruction of beneficial microorganisms, air pollution and the formation of acid rain (Palese et al. 2004; Sanyaolu 2015). It is for these reasons that bush burning, as a strategy for controlling SBDP, is not a wise choice and its use is being discouraged in the continent. The increasing human population in Africa, coupled with ethnic and communal unrest, has also placed serious limitations on land availability and free movement of people. This has reduced significantly the practice of shifting cultivation and land fallowing in most communities.

4.2.2

The Use of Synthetic Chemicals

Some of the most common synthetic chemicals for managing soil and seed-borne pathogens of crops include thiuram, captan, vapam, chloropicrin and pentachloronitrobenzene. Marley and Gbenga (2006) reported on the promising results obtained with the use of selected fungicides, including tetramethyl thiuram disulphide, in the management of stalk and cob rot disease of maize caused by Stenocarpella maydis, through laboratory and green house studies. The use of Fosetyl-Al was also reported to bring about a significant reduction in the incidence and severity of Phytophthora root rot disease of avocado in South Africa (Asim et al. 2019). In Kenya, copper oxychloride was used as a seed dressing agent on selected varieties of legumes to bring about a significant increase in seedling emergence. This was due to a reduction in infections from Rhizoctonia solani and Sclerotinia sclerotiorum. Seedling mortality also reduced significantly (Muthomi et al. 2007). Carbofuran 3G is another chemical that has been used against soil-borne pathogens especially plant-parasitic nematodes (Jada et al. 2011). The numerous problems associated with the use of synthetic chemicals in managing SBPP (Yamamoto

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et al. 2008; Sande et al. 2011; Meena et al. 2020) have necessitated a change of approach in favour of safe, effective, sustainable and environmental-friendly options in the management of these diseases.

5 PGPM: A Safe and Sustainable Option for Managing SBDP PGPM inhabit the soil and rhizosphere in significant numbers and produce a positive effect on plant growth. Dimkpa et al. (2009) and Spaepen et al. (2009) gave a clearer perspective of the positive effects PGPM produce on plant growth by defining them as a group of microorganisms with the ability to enhance plant growth and protect them from biotic and abiotic stress. These microorganisms may be fungi, bacteria or actinomycetes.

5.1 5.1.1

Groups of PGPM Fungi

This consist of species of morphologically, genetically and taxonomically different groups of non-achlorophyllous but multinucleated eukaryotes. Plant growthpromoting fungi (PGPF) are non-pathogenic to their hosts but aid in their growth, good health and general wellbeing. Some PGPF are host specific. They prevent infection and aid growth in one plant, while producing no effect or may even be pathogenic in another. Environmental factors play a great role in the activities of these fungi, determining their effectiveness in enhancing plant growth or otherwise. Several genera of fungi are known to promote growths in plants (Table 10.2). Some of these fungi make direct contact with plant roots through the rhizosphere/rhizoplane/plant roots interactions, while others exist within plant tissues as endophytes.

5.1.2

Bacteria/Actinomycetes

Certain bacteria and actinomycetes are also known to promote growth and good health in plants (Table 10.2). These bacteria are sometimes referred to as rhizobacteria, because they are found in abundance in the rhizosphere (Muleta et al. 2009). They divide and grow very rapidly, and the large population gives them an advantage over other potentially pathogenic microorganisms in the competition for the colonization of the rhizoplane and rhizosphere. In certain cases, infection of the roots by these biotrophs leads to the formation of symbiotic relationships and the development of root outgrowth, root nodules, in their hosts. The host plant is thus supplied with Nitrogen, in addition to protection from infection by

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Table 10.2 Selected PGPM Groups Fungi

Phylum Ascomycota

Basidiomycota Zygomycota Bacteria

Firmicutes Proteobacteria

Actinomycetes

Actinobacteria

Microalgae

Cyanobacteria Chlorophyta

Family Trichocomaceae Cladosporiaceae Glomerellaceae Nectriaceae Trichocomaceae Didymellaceae Daporthaceae Hypocreacea Ceratobasidiaceae Sporidiobolaceae Mucoraceae Mucoraceae Bacillaceae Rhodospirillaceae Burkholderiaceae Enterobacteriaceae Pseudomonadaceae Rhizobiaceae Thermomonosporaeae Frankiaceae Mycobacteriaceae Nocardiaeae Streptomycetaceae Nostocaceae Phormidiaceae Chlorellaceae Scenedesmaceae

Genus Aspergillus Cladosporium Colletotrichum Fusarium Penicillium Phoma Phomopsis Trichoderma Rhizoctonia Rhodotorula Mucor Rhizopus Bacillus Azospirillum Burkholderia Enterobacter Klebsiella Pseudomonas Rhizobium Actinomadura Frankia Mycobacterium Nocardia Streptomyces Anabaena Arthrospira Chlorella Scenedesmus

pathogens. Root nodules are particularly very common in leguminous plants. Some species of Actinomycetes, such as Streptomyces, are also known to inhabit the tissues of plants as endophytes (Jabborova et al. 2020), aiding growth and protecting their hosts from infections (Reshma et al. 2018).

5.1.3

Microalgae

Studies have shown that some species of unicellular algae, commonly referred to as microalgae, can stimulate rapid plant growth as well as enhance their resistance to diseases. Unlike fungi and bacteria, however, the effect of these microalgae is not so much on the direct activity of their cells on plants, but through the effect of the bioactive compounds and secondary metabolites that they produce. These

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compounds act as biofertilizers and soil conditioners, bringing about improved soil fertility and increased plant growth (Priyadarshani and Bath 2012). Some species have been reported to enhance seed germination (Khan et al. 2009), while others act as bio-stimulants. Some are photosynthetic and has the advantage of being able to survive in inhospitable environments with very high concentrations of toxic chemicals. Chlorella and Anabaena are the most common genera with plant growth-enhancing properties (Table 10.2).

6 Management of SBDC with PGPM in Africa: Current Status 6.1

Plant Growth-Promoting Fungi (PGPF)

Several in vitro studies have been carried out on the management of SBPD using PGPF with promising results. Yobo et al. (2013) isolated two strains of Trichoderma from compost soil in South Africa and evaluated them against Rhizoctonia solani, a soil-borne pathogen of several crop species, using the dual culture technique. Their results showed that the Trichoderma spp. evaluated were strong antagonists of the pathogen. Their mycelia grew over and completely covered that of the pathogen. Similarly, reports from two separate studies conducted at the Federal University of Technology, Akure, Nigeria, indicated that Trichoderma spp. have strong antagonistic properties against some soil-borne fungal pathogens. In the first study, T. harzianum inhibited the mycelial growth of Macrophomina phaseolina, the pathogen of charcoal rot disease of cowpea (Olufolaji et al. 2016). The inoculation of T. harzianum, 72 h before the introduction of M. phaseolina into the dual culture plate, was found to produce the highest percentage of mycelial growth inhibition of the pathogen (Fig. 10.1). In the second study, T. harzianum and T. viride both inhibited the mycelial growth of tomato Fusarium wilt and southern blight pathogens (Ayodeji et al. 2021). Results from both studies suggest that prophylactic application of the PGPF was more effective in controlling the pathogen. At the University of Nairobi in Kenya, Mwangi et al. (2018) evaluated two PGPF, T. Harzianum and Purpureocillium lilacinum, along with neem and host plant resistance, for the management of Fusarium wilt of tomato, Fusarium oxysporum f. sp. lycopersici. T. harzianum inhibited the mycelial growth of the pathogen by 51% in a dual culture at 9 days after inoculation. Tomato plants treated with the two fungi also recorded significantly lower disease severity compared to the control. Abou-Zeid et al. (2011) isolated five Trichoderma spp. from Egyptian soil and evaluated them in vitro against some soil-borne pathogens. Their results showed that T. harzianum was most effective, demonstrating the most antagonistic properties against Pythium ultimum and Rhizoctonia solani in about 5 days after inoculation. Some of the Trichoderma isolates were also effective in managing the damping-off disease of chick-pea and chocolate spot of faba bean (Vicia faba) in the greenhouse.

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Fig. 10.1 Percentage inhibition of mycelial growth of M. phaseolina on the 5th day after inoculation with T. harzianum. Means followed by the same letter on bars are not significantly different at 5% probability, according to Duncan’s Multiple Range Test (DMRT). (a) M. phaseolina and T. harzianum simultaneous inoculation. (b) 24 h T. harzianum before M. phaseolina. (c) 48 h T. harzianum before M. phaseolina. (d) 72 h T. harzianum before M. phaseolina. (e) 24 h M. phaseolina before T. harzianum. (f) 48 h M. phaseolina before T. harzianum. (g) 72 h M. phaseolina before T. harzianum. (Source: Olufolaji et al. (2016). Reproduced)

Trichoderma harzianum has also been reported to possess some nematophagous properties. In a study in Ethiopia, Feyisa et al. (2016) reported that spore suspension of T. harzianum had 80.6% mortality on Meloidogyne incognita isolated from tomato. New findings on the efficacy of PGPF in the management of SBPP are reported across the continent almost daily. Trichoderma spp. are most widely evaluated. Their relative abundance, the ease of isolation and their rapid growth in generalpurpose media like potato dextrose agar, even without an incubator in most cases, maybe the reason for this observation.

6.2

Plant Growth-Promoting Bacteria (PGPB) and Actinomycetes (PGPA)

The efficacy of these organisms in the management of SBDC in the continent has also been reported. In Tunisia, where the incidence of Rhizoctonia root rot of pepper was high a few years back, Mannal et al. (2018) evaluated some PGPF and PGPB against R. solani, the causative organism of the disease. The PGPB evaluated were in the genera Burkholderia, Pseudomonas, and Bacillus. Results from the dual culture evaluation showed that the PGPB inhibited the mycelial growth of R. solani by 9–12%. Also, the inoculation of pepper plants with the PGPB led to the suppression of damping-off in the seedlings by some of the bacterial isolates, while also enhancing some growth parameters (Table 10.3). Cocoa pod rot, Phytophthora palmivora, is a

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Table 10.3 Damping-off incidence, severity and growth parameters noted on pepper plants inoculated with Rhizoctonia solani and treated with bacterial isolates Treatments T1 T2 T3 T4 T5 T6 T7 T8 T9

Damping-off (%) 0.00a 50.00c 0.00a 30.00b 10.00ab 30.00b 20.00ab 20.00ab 0.00a

Plant weight (g) 0.54a 0.37b 0.40b 0.27b 0.37b 0.30b 0.33b 0.38b 0.40b

Plant height (cm) 4.70ab 3.55d 4.86a 3.87 cd 4.30abc 3.95bcd 4.23abcd 4.40abc 4.53abc

Disease severity 0.00b 2.70a 0.50ab 1.60ab 0.70ab 1.50ab 1.00ab 1.00ab 0.60ab

Note: Values followed by the same letter in each column are not significantly different according to SNK test (P ≤ 0.05) T1 uninoculated pepper plants, T2 inoculated but untreated pepper plant, T3 inoculated and treated with Pseudomonas aureofaciens, T4 inoculated and treated with Burkholderia giaithei, T5 inoculated and treated with Bacillus pumitus, T6 inoculated and treated with P. hutiensis, T7 inoculated and treated with Bacillus subtilis, T8 inoculated and treated with P. fluorescence, T9 inoculated and treated with P. patida. (Source: Mannal et al. (2018))

serious disease of cocoa globally. Annual yield loss runs into several millions of dollars. The disease is particularly severe in the West African sub-region where a very virulent strain of the pathogen, P. megakarya, has evolved. A study on the management of the pathogen with PGPB in Ghana was reported by Akrofi et al. (2017). Species of Enterobacter, Pseudomonas and Neisseria were evaluated in vitro against P. palmivora, using agar plate and detached pod assay. It was reported that a good number of the evaluated bacteria inhibited the mycelial growth of P. palmivora significantly. One hundred and thirty-three strains of Actinomycetes were isolated from Saharan soil in Algeria and evaluated for antimicrobial properties against Fusarium culmorum, the causative organism of barley seedling blight, using the streak assay technique (Yekkour et al. 2012). Barley seeds were also inoculated with the PGPA isolates before planting. Findings from the study showed that Streptomyces spp. were the most effective, exhibiting strong antimicrobial properties against F. culmorum. Barley seeds inoculated with the isolate also produced seedlings with significantly low incidence and severity of seedling blight.

6.3

Plant Growth-Promoting Microalgae

The efficacy of some Cyanobacteria in the management of damping-off and root rot diseases of lupine plants in Egypt was reported by Abdel-Monaim et al. (2016). Four microalgae, Anabaena sphaerica, Oscillatori agarghii, Nostoc muscorum and Spirulina platensis, were evaluated against three pathogens of root rot and damping-off

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diseases of Lupinus spp., R. solani, M. phaseolina and F. solani. Significant reductions in the mycelial growth of the fungal pathogens were recorded with the use of all the microalgae evaluated.

7 In Vivo Application of PGPM for the Management of SBDC The adoption of PGPM for on-field management of plant diseases in Africa is still at a very low level. The good news, however, is that some in vivo studies and field trials have confirmed their efficacy. A field evaluation of the efficacy of T. koningii in the management of sett rot disease of sugarcane, Ceratocystis paradoxa, was carried out by Ajayi et al. (2016). Two conidial concentrations, 105/mL and 107/mL, were evaluated separately by spraying on cane setts prophylactically and therapeutically. The prophylactic application of fungal conidial suspension at 107/mL gave the highest sett germination percentage, while disease incidence and severity in the treatment were significantly lower than the other treatments from the 4th month after planting. Two strains of Trichoderma and Bacillus subtilis, along with extracts from Moringa oleifera, were applied to the soil as a drench and also as seed treatments agent in a study to determine their efficacy in the management of damping-off and stem rot of cowpea, Sclerotium rolfsii, in Benin republic (Adandonon et al. 2006). The Trichoderma-treated, seeds and soil recorded a significantly low incidence of the diseases. In Pretoria, South Africa, significant suppression of root rot disease of sorghum, Pythium ultimum, was achieved in the greenhouse with the use of PGPB in the genus Bacillus, Pseudomonas, Serratia and Brevibacterium (Idris et al. 2008). Commercial production of some PGPM formulations has also commenced in some countries in the continent, while farmers are being encouraged to adopt them for crop protection. The University of Pretoria, South Africa, has been at the forefront of this drive. The institution developed and patented one of the earliest biocontrol formulations, Avogreen®, in the continent. Avogreen®, Bacillus subtilis, has been used to manage many fields and post-harvest diseases of Avocado successfully in South Africa (Korsten 2004). More recently, the International Institute of Tropical Agriculture (IITA) developed a biocontrol agent for the management of Aspergillus flavus infections and aflatoxin contamination in maize and groundnut. The biocontrol agent, Aflasafe™, was developed from the atoxigenic strain of A. flavus, using sorghum grains as the carrier. Application of the non-toxic strain on maize or groundnut fields, at the recommended rate, bring about the suppression of the toxic A. flavus, through competition, and protect treated crops from infection by the toxic and pathogenic strain. This, not only leads to the production of healthy maize and groundnut plants and produce, but also protects humans and farm animals from aflatoxin poisoning. The campaign to encourage local farmers in the continent to use Aflasafe™ is already on (Fig. 10.2).

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Fig. 10.2 Local farmers applying Aflasafe™ on a maize farm in Nigeria. Credit (IITA Nigeria)

Other biocontrol formulations in the continent include PL Gold® (Pochonia chlamydosporia) and Romulus® (T. harzianum). Both are formulated as wettable powders that can be applied as a soil drench for the management of root-knot and cyst nematodes.

8 Mechanism of Action of PGPM in the Management of Plant Diseases 8.1

Solubilization and Enhancement of Nutrient Uptake

Nitrogen, phosphorus and iron are some of the most important nutrients required for plant growth. Nitrogen is oftentimes not available in the required quantity in the soil, while phosphorous and iron may be inaccessible. Some PGPM fix atmospheric nitrogen and make nitrate available to plants (Sharma et al. 2013, 2016). Trichoderma spp. are known to solubilize phosphorous and iron (through siderophores and secondary metabolite production) making them available to plants (Bitas et al. 2013; Wani et al. 2016; Sayyed et al. 2019) but depriving pathogens of much-needed iron. The direct effect is the alteration in the physiology of such pathogens, bringing about reduced virulence or death. On the other hand, the growth and productivity of associated plants are enhanced with increased vigour, making them more tolerant of some diseases.

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Mycoparasitism

The first step in parasitism is the detection of invading pathogen by the PGPF, the mycoparasite. A contact is then established between the two. It is at this point that the cell wall of the pathogen is lysed, through the production of cell wall degrading enzymes by mycoparasite, as it seeks to penetrate the cell interior of the pathogen. After successful entry, toxins that kill the pathogen are released (Harmon et al. 2004). In some cases, the hyphae of the mycoparasites simply coil around that of the pathogen. The mycoparasite then produces numerous appressoriae that exert mechanical impact, along with the production of lytic enzymes, to break open the cell wall of the invading pathogen (Ownley et al. 2010).

8.3

Induced Systemic Resistance

The infection and colonization of plant roots by non-pathogenic micro-organisms have been reported to lead to the activation of some pathways (salicylic acid, jasmonic acid and root/non-pathogenic induced pathways) through which such plant responds to subsequent infection from pathogenic microbes. Salicylic and jasmonic acids are known to bring about the production of certain proteins (glucanases, chitinases and oxidative enzymes) as soon as infection from a pathogenic microbe occurs. These proteins stop the progression of pathogenesis and protect the host plant from further damage (Harmon et al. 2004).

8.4

Competition

Competition can be for nutrients or binding sites on the root surface or tissues of the host plant. Protection is achieved when the PGPM outcompete the pathogen and take up the nutrients required by the pathogen, causing it to starve to death. Alternatively, the PGPM may divide and produce several cells within a short period. This mass of cell protects the surface of the root or tissue and deprives the pathogen of biding sites where infection and pathogenesis can be initiated.

8.5

Antibiosis

Antibiosis describes a phenomenon in which a PGPM produce certain anti-microbial compounds that have inhibitory effects or that can kill other microorganisms (pathogens) in the same vicinity and within the reach of the compounds. Research has shown that these anti-microbial compounds, sometimes referred to as secondary

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metabolites, are strain or specie specific and have been grouped into three main types, namely water-soluble compounds, volatile antibiotics and peptaibols (Zeilinger et al. 2016).

9 Benefits of PGPM in the Management of SBDP Some PGPM produce the dual benefit of enhancing plant growth and yield while also protecting crops from infections (Mishra et al. 2016). This has the effect of reducing the cost of production since extract cost is not incurred in the purchase of manure. The issue of mammalian and phytotoxicity, commonly associated with conventional chemicals, is also eliminated; PGPMs are usually non-toxic. They also do not leave toxic residue behind in the soil after use; hence, the problem of land and water pollution is avoided. PGPM have no adverse effect on the soil structure and microbial population as beneficial and not target organisms are unaffected. On the whole, the management of SBDP with PGPM is more effective, economical and sustainable.

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Problems/Limitations of PGPM in the Management of SBDP

One of the biggest challenges in Africa is the scarcity of PGPM in commercially formulated forms. Most farmers do not have access to them. There is also the problem of specificity of each PGPM as regards the plant diseases and pathogens they control. This is a major limitation to their wide acceptability, owing to the mixed cropping system that is still very common in rural communities. The poor adaptability of some PGPM to some soil types is another factor. An unfavorable pH may be all that is required to prevent a PGPM from functioning. There is also the problem of poor competitive ability with plant pathogens. This may result from decreased efficiency of the PGPM or increased virulence on the part of the pathogen. In some cases, the PGPM may have lost viability through inappropriate storage conditions. Wrong application, in terms of insufficient quantity of the PGPM or wrong timing, will also lead to poor disease control by PGPM. These constraints are highlighted by Basu et al. (2021).

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Conclusion

The use of beneficial microorganisms for protection of crops from biotic and abiotic stress, as well as the enhancement of growths and productivity, has gained wide acceptability and usage in Asia, America and Europe. The same cannot be said about

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Africa. Commercially formulated PGPMs are either not readily available or are priced out of the reach of most peasant farmers. This has led to a very low level of PGPM utilization in the management of plant diseases generally. There is an urgent need for all stakeholders, agriculturists, cooperative organizations and multinational companies, to address this problem and take up the challenge of producing and making commercially formulated PGPMs readily available to farmers. The market is huge and the opportunities are limitless.

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Chapter 11

Role of Plant Growth Promoting Microbes in Managing Soil-Borne Pathogens in Forestry Abdul Gafur, Rabia Naz, Asia Nosheen, and R Z Sayyed

1 Introduction According to the official Government publication (Badan Pusat Statistik 2019) in 2018, Indonesia’s estate forests spanned more than 8 million ha, most of which (ca. 94%) were distributed over the islands of Sumatera (50%) and Kalimantan (44%). The Forestry Section provided more than USD 12 billion to the national income in the same year (PPID KLHK 2019). Pests and diseases have long been regarded as essential determinants in the long-term sustainability of estate forests in the country. New pests and diseases have arisen as new species of Acacias and Eucalyptus were introduced commercially as fast-growing trees. Since the beginning, different fungal and bacterial pathogens have been observed in the Indonesian estate forests. These include Ceratocystis manginecans, Ganoderma philippii, Phellinus noxius (Pyrrhoderma sp.), Fusarium spp. (Gafur et al. 2007a, 2010), Ralstonia spp., and Xanthomonas spp. (Tjahjono et al. 2011a, b; Yuvika et al. 2013). Biocontrol measures play an important role in mitigating soil-borne diseases as part of the integrated pest management (Reshma et al. 2018; Yasmin et al. 2020). Plant growth promoting microorganisms (PGPM) development is a priority research topic for a number of forestry organizations. PGPM has been isolated from diverse ecosystems for this scenario (Zope et al. 2019a). The importance of PGPM in controlling soil-borne diseases in estate forests is covered in this chapter, with the emphasis on the red root rot disease.

A. Gafur (*) Sinarmas Forestry Corporate Research and Development, Perawang, Indonesia e-mail: [email protected] R. Naz · A. Nosheen Department of Biosciences, COMSATS University, Islamabad, Pakistan R. Z. Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_11

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Table 11.1 Estimated losses of Acacia mangium plantations at different ages due to Ganoderma philippii Country Indonesia Malaysia The Philippines India

Age (months) 36–60 (second rotation) 168 72–120 108–168

Loss (%) Up to 28 Up to 40 Up to 25 Up to 40

Source Irianto et al. (2006) Lee (2000) Militante and Manalo (1999) Mehrotra et al. (1996)

The red root rot, incited primarily by G. philippii, is the most common root rot disease in the Indonesian estate forests (Coetzee et al. 2011; Glen et al. 2009, 2014; Yuskianti et al. 2014). It was once reported to be the most serious acacia disease, especially on Acacia mangium (Gafur et al. 2007a; Lee 2000; Rimbawanto et al. 2014; Wingfield et al. 2010). In A. mangium plantations of age 9–14 year old, disease-related losses were estimated to be as high as 40% (Table 11.1). The disease has also been observed on a number of eucalypt species, even though at a lower intensity (Coetzee et al. 2011; Francis et al. 2008; Gafur et al. 2010). The severity and occurrence of the disease necessitated the implementation of proper management strategies to ensure the sustainability of estate forest productivity (Francis et al. 2014; Page et al. 2020; Jabborova et al. 2020a). The use of microbial consortiums as biocontrol agents (Gafur 2019a; Gafur et al. 2011a, b, 2015b, 2017a; Tjahjono et al. 2009; Luh Suriani et al. 2020) and the inclusion of resistant genotypes (Gafur et al. 2014, 2015a) are control methods feasible economically and environmentally to mitigate disease losses (Kenawy et al. 2019). To date, biocontrol agents employed include different antagonists such as Trichoderma and Gliocladium ascomycetes, Cerrena and Phlebiopsis basidiomycetes, as well as a few other species of white rot fungi.

2 The Antagonistic Fungi Trichoderma and Gliocladium The antagonists Trichoderma and Gliocladium thrive fast in different environments (Zope et al. 2019b). They are the most common culturable soil fungi with a high degree of environmental plasticity. The fungi attack and colonize other fungal species as well as invade plant roots. Other reported strategies employed by the antagonistic fungi to inhibit other fungal species include antibiosis, resource competition, induced resistance, and neutralization of the fungal enzymes (Pourakbar et al. 2021; Riaz et al. 2021). As a result, Trichoderma and Gliocladium are among the most commonly utilized antagonistic fungi to manage various plant pathogens (El Enshasy et al. 2020). Table 11.2 shows species of the fungi used to control root rot diseases. The effectiveness of rhizospheric Trichoderma and Gliocladium from various ecosystems and locations against the two root rot pathogens of Ganoderma and Phellinus were tested. Several isolates have the ability to outgrow the pathogens, as

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Table 11.2 Some species of the antagonistic Trichoderma and Gliocladium utilized to control root rot pathogens Bioagent Trichoderma harzianum Trichoderma harzianum Trichoderma spp. Gliocladium viride Trichoderma spp. Trichoderma viride Trichoderma polysporum, harzianum Trichoderma sp. Trichoderma harzianum, viride, hamatum

Pathogen Ganoderma lucidum Ganoderma boninense Ganoderma spp. Phellinus weirii Armillaria sp.

Source Bhaskaran (2000) Dharmaputra et al. (1989) Soepena et al. (2000) Susanto et al. (2005) Widyastuti (2006) Nelson et al. (1995) Berglund and Ronnberg (2004) Hagle and Shaw (1991) Raziq and Fox (2006)

Fig. 11.1 Pure culture Ganoderma (G) (left) and Ganoderma (G) overgrown by Trichoderma (T) in dual culture (right) (Gafur et al. 2011a, b)

presented in Fig. 11.1. However, there have been discussions on the reliability in plantations of the free-living isolates. Those that show good antagonistic effects in lab studies may not work well in the plantations. Furthermore, an isolate that is effective in one particular environment may not be equally good in the other. For example, two field experiments were initiated separately in two sites in Riau Province, Sumatera, i.e., A and B compartments. Trichoderma isolated from compartment A was the most effective in the experiment in compartment A, decreasing Ganoderma incidence by 7.0%. Likewise, the best performer in the experiment in compartment B was Gliocladium isolated from site B with a 10.0% reduction in Ganoderma occurrence (Tjahjono et al. 2009; Gafur et al. 2011a, 2011b). In contrast, endophytic Trichoderma is reported to be less unstable and more plastic. Endophytes establish a close symbiotic relationship with their host plants. They penetrate the host system without increasing susceptibility to pathogens (Jabborova et al. 2020b). Endophytic microbes are also better preserved against abiotic factors and other competing microorganisms than their free-living

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Fig. 11.2 Isolation and purification of potential endophytic isolates of Trichoderma (Gafur 2019a; Gafur et al. 2017a)

(rhizospheric) counterparts. Furthermore, endophytes can improve plant vigor as they survive in the plant tissue through rotation (Gafur 2021; Hill 2012; Siregar et al. 2022), indicating that more effective disease management can be achieved. The focus of research then switched toward endophytic Trichoderma. We isolated a large number of samples (more than 200) of potential endophytes (Fig. 11.2) from various habitats and locations in Riau (Gafur 2019a; Gafur et al. 2015b, 2017a). Some of the putative endophytic Trichoderma isolates evaluated in the nursery screening were able to considerably lower the occurrence of Ganoderma root rot disease on the seedlings of A. mangium (Fig. 11.3).

3 White Rot Fungal Species Other bioagents frequently employed to manage root rot pathogens include white rot fungal species. They are capable of decomposing woods quicker than the pathogen, sharing the same resources, competing for nutrients, releasing suppressive secondary metabolites, and mycoparasitizing the pathogens (Eyles et al. 2008; Peterson 2006;

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Fig. 11.3 Some of the potential endophytic Trichoderma isolates evaluated in the nursery screenings (top) are able to reduce or even eliminate Ganoderma root rot disease on the seedlings of Acacia mangium (bottom) (Gafur 2019a; Gafur et al. 2017a)

Naz et al. 2017; Butt et al. 2019). In the northern hemisphere, Phlebiopsis gigantea, which is commercially available in the market, is commonly used to manage Heterobasidion annosum. Regardless of this, in Indonesia the white rot fungal species had not been thoroughly investigated until recently as bioagents capable of competing for wood resources with root-rot pathogens. The mycelial growth of G. philippii and P. noxius is inhibited by Phlebiopsis and Cerrena. Both the species battle for space and resources with the root rot pathogens. Previous investigations have also shown their antimicrobial activity against bacteria. We also looked into how the antagonists might be applied to effectively manage red root rot diseases in estate forests (Gafur 2015; Gafur et al. 2017b; Glen et al. 2006; Hidayati et al. 2017, 2019; Indrayadi et al. 2017; Puspitasari et al. 2014, 2017; Nurrohmah et al. 2019; Naz et al. 2021a). They were sprayed onto stumps to inhibit pathogen infection and colonization (Fig. 11.4). Additionally, we acquired 107 white-rot fungal species samples from estate forests within Riau areas other than Phlebiopsis and Cerrena and explored their possibility as bioagents of root rot pathogens. The fungi were isolated from decayed woods, especially stems and branches, as well as fungal fruiting bodies, as previously described (Sitompul et al. 2011). As many as 28 samples from rotten woods and 51 samples from fungal fruiting bodies were effectively isolated out of the total 107 samples obtained. Wood block, wood disc, and malt extract agar added with wood powder were used as growing media to screen the isolated fungi. The

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Fig. 11.4 Application of Phlebiopsis spp. or Cerrena spp. to the stump to inhibit Ganoderma philippii or Phellinus noxius infection and colonization (Hidayati et al. 2019; Nurrohmah et al. 2019)

three-stage screenings revealed that the isolates of WFA033 and WFA068 (Fig. 11.5) were promising biological control agent candidates against G. philippii.

4 Antagonistic Bacteria Bacterial wilt disease (BWD) has lately loomed as a major disease in the Indonesian tropical estate forests, particularly on Eucalyptus trees (Gafur 2020; Siregar et al. 2020a, b; Tjahjono et al. 2011a, b). The causative agents of the disease, R. solanacearum and R. pseudosolanacearum, possess a broad range of more than 50 host plant families, comprising 450 species. In most cases, host infections occur through root injuries (Ullah et al. 2020; Zia et al. 2021; Arora et al. 2021). The pathogen overtakes the xylem vessels after passing the root cortex, causing abrupt plant wilting and mortality. Crop rotation, intercropping (agricultural), and the use of resistant materials have been the only controls so far. The use of fungal or bacterial antagonists obtained from the same or unrelated crops with endophytic or rhizospheric origin should also be regarded as an important integrated management component of BWD (Shaikh and Sayyed 2015; Sastrini et al. 2017). To manage BWD on Eucalyptus seedlings in nurseries, a consortium of several species of

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Fig. 11.5 The white-rot fungal isolates of WFA033 (left) as well as WFA068 (right) overgrow and inhibit Ganoderma philippii on wood disc (top) and on malt extract agar containing wood powder (bottom) media (Sitompul et al. 2011)

endophytic bacteria was produced (Tjahjono et al. 2020). Both in the laboratory and in the green house, the bacteria suppress R. solanacearum, reducing disease risk and lengthening the disease’s incubation period. The product’s efficacy has not waned over time, showing its long-term viability. A product of endophytic bacteria has also been initiated to manage C. manginecans, another serious acacia pathogen in Indonesia (Nasution et al. 2016, 2017).

5 Biofertilizers Environmental concerns have arisen as a result of the usage of chemical fertilizers and pesticides to sustain nursery productivity. The nursery should be run in an environmentally sound manner while maintaining the same level of yield. In this

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Fig. 11.6 Experiments on the impact of different AM fungal species on the growth and survival rates of Acacia crassicarpa (left) and Eucalyptus pellita (right) seedlings with less consumption of chemical fertilizers and zero pesticides (Arifin et al. 2022)

context, the ultimate goal is to develop plant resilience to abiotic and biotic stresses (Naz and Bano 2015; Naz et al. 2018; Tayyab et al. 2020; Naz et al. 2021b, c), particularly to soil-borne pathogens, in order to improve the health of estate forests. The use of PGPM in this scenario has been widely examined (Arora et al. 2021; Gafur 2022; Hamid et al. 2021; Jabborova et al. 2021; Mir et al. 2022; Saboor et al. 2021; Sarkar et al. 2021; Zul et al. 2022a, b). For example, mycorrhizae develop a symbiotic relationship with the roots of most plant species. They have been shown to boost the health and growth of host plants (Gafur et al. 2002, 2003, 2004, 2005, 2007b; Lang et al. 2006; Langenfeld-Heyser et al. 2007; Vafa et al. 2021). In light of this, a variety of arbuscular mycorrhiza (AM) species were recently isolated from peat swamp forests in various parts of Sumatera (Turjaman et al. 2019). Acaulospora sp., A. tuberculata, Entrophospora sp., Gigaspora sp., and Glomus maculosum were screened in the nursery after their isolation. Some of these AM fungal species increased the resilience and growth of seedlings of A. crassicarpa and E. pellita (Agustini et al. 2020; Bastami et al. 2021). The impact of different species of AM fungi on the growth and survival rates of A. crassicarpa and E. pellita seedlings with reduced regimes of chemical fertilizers and zero pesticides is being investigated (Arifin et al. 2022) (Fig. 11.6). Evaluation of a biofertilizer product consisting of Bacillus, Brevibacillus, Brevundimonas, Burkholderia, Microbacterium, Ochrobactrum, Pseudochrobactrum, and Pseudomonas consortium (Antonius et al. 2021; LIPI 2015) on their ability to improve seedling vigor of different acacia species was also initiated recently. Figure 11.7 shows effect of the product in increasing the vigor of A. crassicarpa and A. mangium seedlings in nursery (Gafur 2019b; Syaffiary et al.

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Fig. 11.7 Vigor of Acacia crassicarpa (top) and A. mangium (bottom) seedlings with (left) and without (right) the application of a biofertilizer product (Syaffiary et al. 2022)

2022), providing in turn more resistant stands against abiotic and biotic factors when later planted commercially in estate forests.

6 Conclusions Biotic stresses, especially pest and disease attacks, are predicted to continue to pose a threat to estate forests. There are, however, options to address them. Biocontrol, as a vital component of integrated disease management, has generated a substantial contribution to this initiative. To further improve its efficacy, future research should concentrate on isolating locally more adapted and stable isolates of single or consortium formulations. This should include all the groups of PGPM, including biostimulants. Acknowledgements Research fellowship granted by the Alexander von Humboldt Foundation of the Government of the Federal Republic of Germany to AG is gratefully acknowledged.

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high potential as biocontrol agents for root rot disease in Indonesian Acacia mangium plantations. In: Presented at the IUFRO—INAFOR Joint International Conference, Yogyakarta, Indonesia Raziq F, Fox RTV (2006) The integrated control of Armillaria mellea 2 field experiments. Biol Agric Hortic 23:235–249 Reshma P, Naik MK, Aiyaz M, Niranjana SR, Chennappa G, Shaikh SS, Sayyed RZ (2018) Induced systemic resistance by 2, 4-diacetylphloroglucinol positive fluorescent pseudomonas strains against rice sheath blight. Indian J Exp Biol 56(3):207–212. ISSN 0975-1009 Riaz R, Khan A, Khan WJ, Jabeen Z, Yasmin H, Naz R, Nosheen A, Hassan MN (2021) Vegetable associated bacillus spp. suppress the pea (Pisum sativum L.) root rot caused by fusarium solani. Biol Control 158:104610 Rimbawanto A, Tjahjono B, Gafur A (2014) Panduan hama dan penyakit Akasia dan Ekaliptus. In: Balai Besar Penelitian Bioteknologi dan Pemuliaan Tanaman Hutan, Yogyakarta, Indonesia, p 48 Saboor A, Ali MA, Hussain S, El Enshasy HA, Hussain S, Ahmed N, Gafur A, Sayyed RZ, Fahad S, Danish S, Datta R (2021) Zinc nutrition and arbuscular mycorrhizal symbiosis effects on maize (Zea mays L.) growth and productivity. Saudi J Biol Sci 28:6339. https://doi.org/10. 1016/j.sjbs.2021.06.096 Sarkar D, Sankar A, Devika OS, Singh S, Shikha PM, Rakshit A, Sayyed RZ, Gafur A, Ansari MJ, Danish S, Fahad S, Datta R (2021) Optimizing nutrient use efficiency productivity energy use efficiency and economics of red cabbage following mineral fertilization and biopriming with compatible rhizosphere microbes. Sci Rep 11:15680. https://doi.org/10.1038/s41598-02195092-6 Sastrini T, Nasution A, Gafur A (2017) Isolation and screening of microbial antagonists for control of bacterial wilt of Eucalyptus caused by Ralstonia spp. In: Presented at the 5th Asian PGPR International Conference for Sustainable Agriculture, Bogor, Indonesia Shaikh SS, Sayyed RZ (2015) Role of plant growth-promoting rhizobacteria and their formulation in biocontrol of plant diseases. In: Plant microbes symbiosis: applied facets. Springer, New Delhi, pp 337–351 Siregar BA, Gafur A, Nuri P, Halimah H, Tjahjono B, Golani GD (2020a) First report on infection of Eucalyptus pellita seeds by Ralstonia solanacearum. Environ Sci Proc 3:94. https://doi.org/ 10.3390/IECF2020-07904 Siregar BA, Giyanto HSH, Siregar IZ, Tjahjono B (2020b) Epidemiology of bacterial wilt disease on Eucalyptus pellita F. Muell. in Indonesia. In: IOP Conf Series: Earth and Environmental Science, Indonesia, vol 468, p 012033 Siregar BA, Liantiqomah D, Halimah GA, Tjahjono B (2022) Screening of endophytic Trichoderma isolates to improve the growth and health of Eucalyptus pellita seedlings. IOP Conf Ser Earth Environ Sci 974:012084 Sitompul A, Nasution A, Gafur A, Tjahjono B (2011) Screening of white rot fungi as biological control agents against Ganoderma philippii. Presented at the International Seminar and 12th National Congress of the Indonesian Phypathological Society, Solo, Indonesia Soepena H, Purba RY, Pawirosukarto S (2000) A control strategy for basal stem rot (Ganoderma) on oil palm. In: Ganoderma diseases of perennial crops. CABI, London, pp 83–88 Susanto A, Sudharto PS, Purba RY (2005) Enhancing biological control of basal stem rot disease (Ganoderma boninense) in oil palm plantations. Mycopathologia 159:153–157 Syaffiary S, Antonius S, Said D, Nugraha AK, Gafur A (2022) Effect of organic fertilizer products on the growth and health of Acacia crassicarpa seedlings. KnE Life Sciences 2022:531–540. https://doi.org/10.18502/kls.v7i3.11159 Tayyab N, Naz R, Yasmin H, Nosheen A, Keyani R, Sajjad M, Hassan MN, Roberts TH (2020) Combined seed and foliar pre-treatments with exogenous methyl jasmonate and salicylic acid mitigate drought-induced stress in maize. PLoS One 15(5):e0232269 Tjahjono B, Gafur A, Tarigan M, Nasution A, Golani GD (2009) Application of Trichoderma in the nursery and field to combat Ganoderma root rot: progress and challenges. In: Presented at the

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ACIAR Workshop on Disease Management Strategies for the Rural Sector that Help Deliver Sustainable Wood Production from Exotic Plantations, Yogyakarta, Indonesia Tjahjono B, Ernawati NML, Giyanto, Gafur A (2011a) Bacterial leaf blight on Acacia crassicarpa caused by Xanthomonas campestris in Indonesia. J ISSAAS 17:234. Abstr Tjahjono B, Gafur A, Golani GD (2011b) Occurrence of bacterial wilt on acacias and eucalypts in Indonesia. J ISSAAS 17:234. Abstr Tjahjono B, Gafur A, Kanzler A, Kartiko HDP, Pessotti PR (2020) Sinarmas Forestry R&D Quarterly Bulletin, unpublished Turjaman M, Herdyantara B, Faulina SA, Agustini L, Irianto RSB, Hidayat A, Wahno I, Murdani, Tjahjono B, Indrayadi H (2019) Mycorrhizal colonization of indigenous tropical tree species grown in peat swamp forests of Sumatera Indonesia. IOP Conf Ser Earth Environ Sci 308: 012049. https://doi.org/10.1088/1755-1315/308/1/012049 Ullah H, Yasmin H, Mumtaz S, Jabeen Z, Naz R, Nosheen A, Hassan MN (2020) Multitrait pseudomonas spp. isolated from monocropped wheat (Triticum aestivum) suppress fusarium root and crown rot. Phytopathology 110(3):582–592 Vafa ZN, Sohrabi Y, Sayyed RZ, Luh Suriani N, Datta R (2021) Effects of combinations of Rhizobacteria, mycorrhizae, and seaweeds on growth and yields in wheat cultivars under the influence of supplementary irrigation. Plan Theory 10:811 Widyastuti SM (2006) The biological control of Ganoderma root rot by Trichoderma. In: Proceedings of the heart rot and root rot in tropical acacia plantations workshop, Yogyakarta, Indonesia. ACIAR proceedings, vol 124. Centre for International Research, Canberra, pp 67–74 Wingfield MJ, Slippers B, Roux J, Wingfield BD (2010) Novel associations between pathogens, insects and tree species threaten world forests. N Z J For Sci 40:S95–S103 Yasmin H, Naz R, Nosheen A, Hassan MN, Ilyas N, Sajjad M, Anjum S, Gao X, Geng Z (2020) Identification of new biocontrol agent against charcoal rot disease caused by Macrophomina phaseolina in soybean (Glycine max L.). Sustainability 12(17):6856 Yuskianti V, Glen M, Francis A, Rimbawanto A, Gafur A, Indrayadi H, Mohammed CL (2014) Species-specific PCR for rapid identification of Ganoderma philippii and Ganoderma mastoporum from Acacia mangium and Eucalyptus pellita plantations. Forest Pathol 44:477– 485 Yuvika NA, Nasution A, Gafur A (2013) Actinomycetes isolation and in vitro screening for Xanthomonas biocontrol. J Fitopatol Indonesia 9:124–129. https://doi.org/10.14692/jfi.9.5.160 Zia MA, Riaz R, Batool A, Yasmin H, Nosheen A, Naz R, Hassan MN (2021) Glucanolytic rhizobacteria associated with wheat-maize cropping system suppress the fusarium wilt of tomato (Lycopersicum esculentum L). Sci Hortic 287:110275 Zope VP, El Enshasy HA, Sayyed RZ (2019a) Plant growth-promoting Rhizobacteria: an overview in agricultural perspectives. Plant growth promoting Rhizobacteria for sustainable stress. Management 13:345–361 Zope VP, Jadhav HP, Sayyed RZ (2019b) Neem cake carrier prolongs shelf life of biocontrol fungus Trichoderma viridae. Indian J Exp Biol 57:372–375 Zul D, Elviana M, Ismi KRN, Tassyah KR, Siregar BA, Gafur A, Tjahjono B (2022a) Potential of PGPR isolated from rhizosphere of pulpwood trees in stimulating the growth of Eucalyptus pellita F. Int J Agric Technol 18:401–420 Zul D, Mustava M, Diva AR, Siregar BA, Gafur A, Tjahjono B (2022b) Biological activity of Rhizobacteria isolated from rhizosphere acacia crassicarpa a. cunn ex benth. In timber plantations. Int J Agric Technol 18:421–436

Chapter 12

Secondary Metabolites and Bioprospecting Megha Sharma, Richa Bhardwaj, Mukesh Saran, Rakesh Kumar Prajapat, Deepak Sharma, and Manas Mathur

1 Introduction Flora, the autotrophic renewable kingdom, with huge divergence in their families, age, size, colonization, phytochemicals, and virtue of soil and flourishment in every geographical region, possesses a significant amount of metabolites which are the result of its integral phytometabolism. These indispensable biochemical factories produce both basic macromolecules (e.g., lipids, amino acids, and carbohydrates) and higher-potent employable natural products, viz., flavonoids, alkaloids, terpenes, glycosides, polyketides, volatile oils, resins, tannins, glucosinolates, cyanogenic glycosides, quinones, coumarins, etc., and are directly recommended in conventional remedial methods including Ayurveda, Unani, and Chinese medicine (Bardakjian et al. 2019) to combat various disorders for thousands of years. The amalgamation of all biochemicals (anabolic and catabolic) possessed by an individual is defined as “metabolism” (Hussain et al. 2012). The basic difference is primary metabolic pathways converge few end products responsible for fundamental vital cellular processes like protein synthesis, cellular respiration, transport of solutes, accumulation of nutrients, and photosynthesis; on the contrary secondary metabolic M. Sharma Laboratory of Plant Pathology and Biochemistry, Department of Botany, University of Rajasthan, Jaipur, Rajasthan, India R. Bhardwaj Department of Botany, IIS (Deemed to be University), Jaipur, Rajasthan, India M. Saran Department of Physics, Manipal University Jaipur, Dehmi Kalan, Jaipur, Rajasthan, India R. K. Prajapat · M. Mathur (*) School of Agriculture, Suresh Gyan Vihar University, Jaipur, Rajasthan, India D. Sharma School of Agricultural Sciences, Jaipur National University, Jaipur, Rajasthan, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_12

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pathways fork into multiple metabolites or products consuming nutrients from exterior environment like low-molecular-weight compounds for defense mechanism (Olivoto et al. 2017). It has been reported that there are three existing structured pathways for conducting metabolism in amino acids: the Embden-Meyerhof-Parnas pathway (EMP)/glycolysis (Mohiuddin 2019) existing in every living cell (bacterial, fungal, plant, yeast, and animal cells), the Entner-Doudoroff pathway, and the hexose monophosphate (HMP) pathway. The final product of EMP is two molecules of pyruvate via formation of triose phosphate (Hussain et al. 2012; Naik and Al-Khayri 2016a, b). Although advancement with age of plants, absence of plant secondary metabolites (PSMs) enervates the healthy life of plants making them prone to diseases because these metabolites impart potency to combat against biotic agents such as bacteria, viruses, fungi, and herbivores as well as other physiological conditions like high and low temperatures, drought, UV rays, etc. Moreover, they have gained keen interest as inspiring agents assisting pharmacophagy, Mycorrhiza I, oviposition, seed dispersal, and pollination and in symbiotic association of nitrogen-fixing bacteria (Kaur and Pati 2018). These incredibly diverse secondary natural compounds are integrated by plants, parasites, and microorganisms. These natural products are synthesized in response to various kinds of (a) biotic stresses, along with completion of important physiological roles, like enticing pollinators and establishment of symbiotic relationship, even to strengthen structural components like lignifications of cell walls of vascular tissues (Ncube and Van Staden 2015). The highly diverse and extensive crucial secondary metabolites, like terpenes, phenolic compounds, and alkaloids, are categorized according to their biosynthetic pathway (Mohiuddin 2019; Singh and Sharma 2015). Continuous threats are countered by plants against adverse kind of environment, like attack by predators which include fungi, viruses, insects, and nematodes and extreme physical circumstances (exposure to UV radiation, salinity, and drought) (Thakur et al. 2019). These signals are recognized as stresses by plants by their receptors and sensors, thereby activating resistance retorts to stabilize and combat in response to such kind of adverse environmental conditions (Hamann 2015). In response to stress factors, accumulation of secondary metabolites is initiated. However, when there is synthesis of secondary metabolites at elevated levels against these stress factors, the process is termed as “elicitation.” This fundamental stimulated process confirms the persistence, endurance, and affordability of the plant. Bioactives give an advantageous attribute to particular plant species providing plants a defensive approach in growth and vitality of that plant in the long term; it depends on essential metabolism. However, against different kinds of pathogen, development of resistance in plants is assisted by some phytoalexins present in them and persuaded defense pathways also. Plants modify their metabolism, as a consequence of variable environmental conditions, thereby acclimatizing to existing stress factors, which leads to variations in phytochemicals and their nutritional ingredients (Świeca et al. 2012).

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These diverse groups of secondary metabolites are categorized as terpenes, phenolics (e.g., phenolic acids), coumarins, lignans, stilbenes, flavonoids, tannins and lignins, and alkaloids. Various customized uses and side effect-abided properties of natural compounds made them commercialized leading to harnessing of particular plant species survival on this planet in question. Plants secondary metabolites (PSMs) are synthesized in little amounts, and increased applications of bioactives as bio-fear mongering, medications, colors industry, bio-fighting, poisons in farming bug sprays, and prescription (Mohiuddin 2019) unconnectedly enforced researchers to discover novel and effective approaches and methods to increase both the quantity and efficacy as per rising demands.

2 Synthesis of Secondary Metabolites by Elicitation and Precursor Feeding Since natural products are highly complex structures with stereo-specificity. The production by chemical route is not thriftily practicable because their cultivation, harvesting and extraction is labor intensive and time consuming attributing to low productivity in terms of quality and quantity and also; geographical or governmental restrictions (Almagro et al. 2013; Nandagopal et al. 2018). These chemical compounds kindle stress mechanism in plants; thus, increased yield in natural products was observed including some novel molecules (Naik and Al-Khayri 2016a, b) ensuring the survivability of plants in contrary situations. The implementation of elicitors has gained a lot of keen interest from scientific communities, which has been recommended as a useful tool to enhance natural products in medicinal plants. Different chemical and physical factors are included in abiotic elicitors which play a role as stimuli and which stimulate synthesis of phytochemicals (Owolabi et al. 2018). These stressors include different types of photoperiod rays like UV or IR along with different metal complexes like cupric chloride, selenium, silver nitrate, cadmium chloride, copper sulfate, nickel sulfate, etc. Several other factors are also included like osmolytes, viz., sorbitol, potassium chloride, PVP, mannitol, and sodium chloride, change in temperature, etc. Besides that, there are various intracellular signaling compounds like salicylic acid (SA), acetyl salicylic acid (ASA), jasmonic acid (JA), and methyl jasmonate (MJ) (Wang and Wu 2013). There are several reports based on abiotic elicitors which have been applied in complexation in different quantities in hydroponics, along with different developmental stages of plants till harvesting under natural conditions (Fig. 12.1) (Baenas et al. 2014). For molecular studies based on defensive gene expressions in plants, salicylic acid is a vital and important signal compound which assists in resistance against various pathogens like virus, bacteria, and fungi, while jasmonic acid stimulates synthesis of different proteins through octadecanoid pathway which also helps plants to fight against attack by different insects which has also been supported by several scientists (Ali and Baek 2020).

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Fig. 12.1 Showing application of elicitors on synthesis of various phytochemicals

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Besides this, jasmonic acid also acts as an endogenous molecule assisting the physiological growth of plants (Malekpoor et al. 2016; Złotek and Świeca 2016). This important signal molecule activates the expression pattern of several genes involved in defense mechanism which in turn regulates protein production by the octadecanoid pathway. Jasmonates and methyl jasmonates are categorized under cyclopentanone compounds which stimulate and direct a broad-spectrum response in plants, and they play an important role as operative and potent molecules engaged in the biosynthesis of natural products in the laboratory environment. They cope with plants when they face adverse environmental conditions (Złotek et al. 2014, 2016). The jasmonic acid signaling route acts as a precursor for many natural products like phenolics, flavonoids, terpenoids, phenylpropanoids, alkaloids, and vitamin C. Further it was observed that yeast extract (YE) also increased total phenolic content, while ascorbic acid content was not affected (Złotek and Świeca 2016). A significant increase in carotenoids was also reported recently in Origanum majorana L. using JA. Also YE showed a remarkable enhanced free radical scavenging potential in Origanum majorana L. which is co-related due to enhanced ascorbic acid and chlorophyll content (Złotek 2017). Heavy metals are crucial agents, responsible for abiotic stress, in living systems as for their proven which possess extraordinary deposition in cells and tissues and noxiousness (Cai et al. 2013). These kinds of stress cause variations in the metabolic phenomena and inhibit the pathways of plants which in turn affect different physiological phenomena, viz., sugars, proteins, and non-protein thiols and photosynthetic pigments. High temperature leads to leaf senescence initially. Acclimatization in such kind of environment, so plant cells use various defense pathways fluctuating from morphological to physiochemical. Among them is increased synthesis of bioactive compounds. Flavonoids and phenolic acids are two main natural products, which combats plants against abiotic stresses through as they eradicate free radicals prior to oxidation of cell walls integrities in cellular membranes. Such kind of stress results in elevated levels of phenolics and flavonoids as they lead to stimulation and triggering in certain enzymes responsible for this. It has been reported that when strawberries go through such kind of stress, it leads to accumulation of anthocyanins, phenolic acids, and flavonols which are responsible for antioxidant, free radical scavenging activity. There is a correlated scenario between increased temperatures during night including their harvesting leading to synthesis of polyphenols when observed at a decreased temperature. It was also observed that phenolic content increases with a rise in temperature in Saccharum officinarum at 40/35 °C as compared to 28/23 °C (diurnal/nocturnal) temperatures. To date, there is a lot of research required on comprehensive analysis to understand the exact phenomena of the same (Shamloo et al. 2017). There are some reports which proved that besides light and temperature, salinity also persuades effect on the synthesis of secondary metabolites (Bernstein et al. 2013) on the physiological growth of plants. However, saline conditions lead to enhanced level of natural products like phenolics, terpenes, and alkaloids; salinity results in loss of water content from cells and creates osmotic stress, which in turn

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Table 12.1 Effect of abiotic elicitors on the synthesis of bioactive compounds in plants S. no Plant species Heavy metals 1. Vitis vinifera 2.

Bacopa monnieri

3. Datura metel 4. Salvia castanea Temperature 1. Melastoma malabathricum 2. Rhodiola crenulata Light 1. Vitis vinifera 2.

Melastoma malabathric

Elicitor

Compound

References

Cd2+, Co2+, Ag+ Cu2+

Resveratrol

Cai et al. (2013)

Bacoside

Ag+ Ag+

Atropine Tanshinone

Sharma et al. (2015) Zahra et al. (2015) Liu et al. (2018)

Low temperature Low temperature

Anthocyanin

Chan et al. (2010)

Melatonin

Zhao et al. (2011)

Stilbene

Wang et al. (2010)

Anthocyanins

Chan et al. (2010)

GABA Sorbitol, Jasmonic acid Vinblastine, Vincristine

Bor et al. (2009) Tari et al. (2010)

Glycyrrhizic acid Steviol glycosides

Liu et al. (2014) Peteliuk et al. (2021)

UV–C irradiation Light irradiation

Salinity 1. Sesamum indicum 2. Lycopersicon esculentum 3.

Catharanthus roseus

Drought 1. Glycyrrhiz auralensis 2. Stevia rebaudiana

Water stress PEG

Fatima et al. (2015)

reduces cytosolic and vacuolar volumes and further may cause decreased level of phytochemicals. Anthocyanin content was also shown to have increased level in some plants and decreased in the salt-sensitive species under salt stress. Increase in salinity also increased polyphenolic amount in varied cells in varieties of plants (Table 12.1) (Haghighi et al. 2012).

2.1

Mechanism of Action

Elicitors act as signals, and these signals are recognized and perceived by elicitorspecific receptors present in a site-specific manner on the cell wall, resulting in the stimulation of signal transduction torrent in plants which in controls differential expression of certain genes responsible for transcription and species specific genes of normal biosynthesis routes of certain natural products. As a result, there is

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Fig. 12.2 Schematic representation of mode of action of elicitor in plant cell

elevated accumulation of phytochemicals in culture (Halder et al. 2018; Mishra et al. 2012; Wang and Wu 2013; Zhai et al. 2017) (Fig. 12.2). In a few plant species, bioactive compounds are limited to a particular specific meristematic organ as mature cultures are not able to undergo any physiological phenomena and thus possess steady growth with reduced quantity. Genetically modified (HRC) hairy root cultures (Gutierrez-Valdes et al. 2020; Halder et al. 2018) possess optimum quantity of secondary metabolites identical to their native plant (Georgiev et al. 2012). The key enzymes responsible for the plant defense mechanism are protein kinases and phosphatases, playing a pivotal role in regulating plant defense metabolic pathways via phosphorylation and dephosphorylating (Mao et al. 2020). During stress conditions, a significant role is played by kinase enzyme cascades which are activated by mitogen-activated protein kinases (MAPKs) via amplification of stress signals which are perceived at membrane receptors of plant cells. These signals are then transduced and in turn lead to altered gene expression. Several biosynthetic pathways when studied, and by standardization and addition of several organic compounds into the culture medium, enhanced the formation of specific phytochemicals. Thereby, it was observed that supplementation from outside of a biosynthetic precursor to culture media may elevate the quantity of the anticipated compound. This cost-effective and economically feasible approach is utilized for increasing the levels of bioactives in culture medium. The basic principle of precursor feeding is to select a particular compound, which can be a transitional, in or at initial stage of biosynthetic route of a particular natural product, thus marking a tremendous elevation in the amount of the final desired compound. The handling of plant cells with abiotic and biotic elicitors is a key tool to increase the quantity of natural products (Karuppusamy 2009). The commonly studied/used elicitors in some earlier reports include yeast extract, methyl jasmonates, fungal carbohydrates, and chitosan. A prominent signal compound elevates taxol synthesis in Taxus chinensis Roxb. and ginsenoside production in P. ginseng raised cultures. The participation of amino acids in the biosynthesis of adhyperforin and hyperforin

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has been observed in shoot cultures of H. perforatum. Valine and isoleucine, when induced in in vitro cultures, were assimilated into acyl side chain of hyperforin and adhyperforin, respectively. Supplementation of unlabeled isoleucine at a dose level of 2 mM induced a three- to sevenfold rise in the synthesis of hyperforin. Isolation of triterpenes in callus obtained leaves were used as explant (Hussain et al. 2012). Further there was significant enhancement in anthocyanin when amalgamation of 5 mg/L phenylalanine and 50 mg/L methyljasmonate was supplemented in culture in root callus of Panax sikkimensis (Biswas et al. 2015). These cell suspensions were found to successfully accumulate both ginsenoside and a peonidine-type anthocyanin after 3 weeks and 5 weeks of culture to the tune of 77 mg/L and 199 mg/L, respectively (Biswas et al. 2015). Efforts to successfully upregulate ginsenoside production via elicitations from these cell suspensions have been attempted in the past (Biswas et al. 2018, 2020).

2.2 2.2.1

Types of Secondary Metabolites Terpenes

They are one of the most prominent classes of natural product in plants comprising 40,000 derivatives. Chemically they are non-saponifiable lipids as there is no arbitration of fatty acids in their synthesis. Isoprene is the basic structural unit of these groups they are known as isoprenoids (Vranová et al. 2012). They have been categorized according to the repeats of different units of isoprene. The prominent category is hemiterpenes with a single isoprene unit and 5 carbons in its assembly. The basic unit is monoterpenes, with 3 units in sesquiterpenes, 4 in diterpenes, 6 in triterpenes, 8 in tetraterpenes, and around 10 in polyterpenes (Taiz and Zeiger 2010). In plants they are found in flowers and fruits as composition of instable molecules with particular smell like eucalyptus, ginger, great basil, mint, and lemon (Olivoto et al. 2017). They are an integral unit of both primary and secondary metabolisms of plants. Generally their core area is photosynthetic pigments (carotenes), responsible for the physiological growth of plants (gibberellins, brassinosteroids, strigolactones), electron carriers (ubiquinone and plastoquinone) and as part of cell membranes (phytosterols) along with protein glycosylation (Loreto et al. 2014). Further, they act as defense molecules and provide resistance against insects. Along with that they are key molecules for participation in physiological phenomena of pollination. Initially they are produced from primary metabolites by alternative routes like from mevalonic acid, present in cytosol, in which three molecules of acetyl-CoA condense as mevalonic acid which further converts in isopentenyl diphosphate (IPP) or methylerythritol phosphate (MEP) tasked in chloroplasts (Olivoto et al. 2017).

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Phenolic Compounds

These are natural products representing hydroxyl group of an aromatic hydrocarbon. Among various phytochemicals, they are most diverse. Phenol is the simplest compound that belongs to this category (Velderrain-Rodríguez et al. 2014). According to the number of carbons present in the molecule, they are categorized like hydroxyl cinnamic acids, coumarins, simple phenols, acidic phenols, benzophenones, flavonoids, phenylacetic acids, acetophenones, flavonyls, quinones, and betacyanins (Dai and Mumper 2010). The shikimic acid route is base for derivatization of phenylalanine and cinnamic acids (Vattem et al. 2005). The polyacetate pathway synthesizes quinones and xanthones. Similar scenario is observed in flavonoids (Cheynier et al. 2013). Phenolic compounds play a crucial role in plants physiologically as they are vital in acting as antioxidants (Martins et al. 2016). Along with that, they are also deposited on the surfaces of leaves, grasping about 93% of UV radiation (Verdaguer et al. 2017). Allelopathy is also one of the important phenomena possessed by them (John and Sarada 2012). Phytoalexins, one of the most promising compounds present in plants, play a crucial part in defense against the attack of pathogens as they are repellant to microorganisms and they fight against infections. Phenols also generate bitter taste in plants which is not suitable for grazing by herbivores, thus preventing them (Marsh et al. 2020).

2.2.3

Alkaloids

These are the most varied and the prominent class of natural products isolated from plants. Generally these are synthesized as a composite mixture. One of the amazing facts associated with them is that their concentration differs in every plant part (Ng et al. 2015). They are also found in fungi, bacteria, and animals. Basically they have nitrogen atom in their morphology (Matsuura and Fett-Neto 2015). Generally they are derived from anthranilic and nicotinic acids. Recently it has been reported that their important task is to provide resistance against various predators like herbivores and insects as it has prominent toxicity and restraining potential. Among the various secondary metabolites, alkaloids have gained appropriate attention of biochemists. Because of their diversified physiological function and pharmacological effects, they can be used as models for the production of new combination in the hope of synthesizing new and more effective drugs. Trigonelline is one of the metabolically active pyridine alkaloids broadly accumulated in plant kingdom as well as in animals. Evans and coworkers reported that this alkaloid acts as plant hormone that occurred in cotyledons, and it stimulates cell arrest in G2 phase during physiological growth of cell maturation in shoots and roots. Due to their excellent therapeutic effects, there is a need for extensive chemical-biological study of alkaloids. This natural product has gained a lot of attention as it possesses tremendous biological applications and acts as a therapeutic agent (Greger 2019).

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Phytosterols

Sterols present in plants are called phytosterols, and over 250 phytosterols have been isolated and characterized from them. Chemically, they have a tetracyclic cyclopenta (α)phenantrene ring confined to steroids with substitutions in methyl at C-10 and C-13, a hydroxyl group at C-3, and a flexible side chain of varying length at C-17, described by various scientists. There are some reports which proved the oxidative steadiness of phytosterols in coconut, soybean, peanut, and canola oils. As they are part of a normal diet, they have attracted local communities. Thus, innovations in the food industry assisted to recover their bioavailability, solubility, and engagement in different varieties of edible items. There are some reports which prove that phytosterols assist in decreasing blood cholesterol levels. So, phytosterols may act as an immune boost to cure and to avoid cardiovascular disorders. Therefore, a benign and sophisticated dose of phytosterols is recommended in the management of hypercholesterolemia, to combat low-density lipoprotein (LDL-c) levels prominently. To date there are so many clinical and experimental trials that have agreed that phytosterols reduce LDL-c, including tremendous variations in serum high-density lipoprotein (HDL-c) and level of triglyceride. Moreover, the effect of phytosterols on cardiovascular disease is still a point of discussion (Bicas et al. 2015).

2.3

Recent Biotechnological Approach for Synthesis of Secondary Metabolites

A specific biosynthetic pathway involves recombinant DNA technology and depiction of key enzymes. Gene cloning, regulation, and transformation have gained considerable development in secondary metabolite biosynthetic pathway (Gaosheng and Jingming 2012). Techniques based on PCR (polymerase chain reaction) and construction of genomic libraries are frequently used in the construction and cloning of genes which are involved in the biosynthetic pathway of secondary metabolites. Earlier, rapid amplification of cDNA ends (RACE) PCR and real-time PCR were used, which need gene sequence of other plant species or partial gene sequence information, to synthesize generated primers. These methods are not useful without reported reference sequence. In this condition, library-based methods can be considered for gene cloning, but these methods like BAC library and cDNA library are nonspecific. That is due to the small number of genes involved in total expressed mRNAs. Specific genes involved in secondary metabolites can be cloned with the methods of functional genomics, such as serial analysis of gene expression, microarray assay, and subtractive hybridization. Functional genomics helps in selecting and cloning genes associated with the biosynthetic pathway, for the improvement of target secondary metabolites which should be specific. In treated plant cells, substances that can create hypersensitive response are called elicitors. To increase synthesis of desired molecules in medicinal plant tissue and cell

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cultures, elicitors are widely used due to their effective gene expression up regulation leading to instigation of natural products which improvised accumulation of secondary metabolites. There are two types of elicitors, biotic and abiotic. It is believed that in plant cell culture, treating cells at the stabilization stage, secondary metabolite accumulation can be increased significantly. In recent times, a newly developed strategy has shown that the repeated elicitation results in increased accumulation of target compounds and more gene expression and enzyme activity. Therefore, to maximize yield, secondary metabolite regulation has been gaining interest (Gandhi et al. 2015). Molecular technology helped in gathering more and more genetic information about plants. Many plant species genomes have been sequenced and are available online. In addition to this, genetic techniques like miRNA, siRNA, T-DNA tagging, transformation, EST, RACEPCR, etc. have also been carried out. A lot of information provided by these techniques created possibilities for the exploitation of target compound synthesis. Rational metabolic engineering requires a systematic synthesis and monitoring facet of phytochemicals. Highly networked biosynthetic processes in a cell with a number of communications at every phase of a biosynthetic route often lead to impulsive outcomes in metabolic engineering. The biotechnologists using a systems biology approach integrate data from transcriptomics, proteomics, and metabolomics that help to engineer the metabolomics pathway with increased foreseeable outcomes (Yang et al. 2014). The knowledge of various metabolic pathways is essential in the field of metabolic engineering to rally the productivity of natural products in plant cells. This process assists in exploring new bioactive compounds contained in plants (Yue et al. 2016). Metabolic engineering has involvements such as steps that overcome rate limits; blocking of other competing pathways; suppression of catabolism of interested product; or combination of any of the above. In spite of nescience related to genes involvement and metabolic pathway, metabolic engineering is quite promising. This produces new compounds, increases the yield of existing compounds, or for the plant it biosynthesizes novel molecules. Secondary metabolite (SM) accumulation directly relies on plant growth condition and affects different metabolic pathways, correlated with stress environment, and engages signal molecules and elicitors. Due to the sessile physiology of plants, they are frequently bare to broad a range of environmental stresses, like temperature, drought, salinity, alkalinity, UV, pathogens, and herbivores, which can drastically affect physiological growth of plants (Seigler 2012). Various abiotic stresses cause physiological cellular dehydration, which ultimately creates osmotic pressure and removes water from the cytoplasm to vacuoles. External factors can unfavorably cause some pathways associated with physiological growth and development in plants, and their capacity to accumulate SMs thus causes differences in phytochemical profiles, which has crucial roles in the synthesis of phytochemicals (Verma and Shukla 2015). Therefore secondary metabolism describes the ability of plants to become accustomed and survive in response to environmental stress during their physiological growth, thus also creating an ecological inter-chain between plants and animals.

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Due to global warming, there is a rise in temperature of about 0.47 °C in the current decade. Therefore, this considerably affects the synthesis of natural products. As we know temperatures are harmful abiotic stresses which can directly affect the growth and development of plants; therefore, adapted plants hinder their metabolism when grown under such kind of stress, thus enhancing some essential metabolites and thereby surviving adverse circumstances (Karwasara and Dixit 2013). It also enhances and decreases the biosynthesis of alkaloids due to drastic variations in temperatures like morphinane, phthalisoquinoline, and benzylisoquinoline etc. It is inhibited at low temperature in plants such as Papaver somniferum. Various plant varieties of Lupinus angustifolius exposed to high temperature also have enhanced alkaloid accumulation (Jansen et al. 2009). Conversely, Catharanthus roseus leaves possessed reduced levels of vindoline and catharanthine when adapted at reduced temperatures (Dutta et al. 2007). When there is a rise in temperature, terpenes mount up at high level in Daucus carota, while terpinolene decreases in such conditions. In Zea mays seedlings, anthocyanin accumulation is enhanced according to time intervals of variation in temperatures. In Rhodiola rosea, temperature alters SM accumulation along with heavy metal stress (Zhao et al. 2016). Phenylamides have reactive oxygen species (ROS) and thus have antioxidant activities; they are accumulated in tobacco and beans when the plants are exposed to extreme heat and water stress (Edreva et al. 2008). Reduction in temperature increases accumulation of phenolic compounds and their following incorporation in the plant cell wall as lignin or suberin, while plants adapted to reduced temperature are correlated with accumulation of chlorogenic acid at high levels. Similarly, temperature affects the accumulation of ginsenosides in the root hairs of Panax ginseng, while Melastoma malabathricum produces increased concentration of anthocyanin at low temperatures (Chan et al. 2010). Salinity is a major abiotic stress that often causes cellular dehydration, which creates osmotic pressure that directly affects accumulation of specific SMs in plants. Salt stress plays a key role as an elicitor of SMs for protecting cells from the oxidative injury caused by ion accumulation at the cellular and subcellular levels; thus, SMs reduce the toxic effect of salinity (Hossain et al. 2017). Plant genotypic litheness in various saline conditions, both in vitro and in vivo, enables plants to accumulate SMs which are important for their survival in these adverse conditions. Salinity has physiological and biochemical effects on the accumulation of phytochemicals as it induces stress and defense pathways involved in ROS generation and is responsible for the assembly of SMs (Manuka et al. 2019). Besides this, efficiency of roots to absorb water reduces, thus causing water scarcity and osmotic pressure (Adak et al. 2019). Due to this, membrane fluidity, nutrient balance, and redox homeostasis are distressed, which directly affects primary metabolites which are precursors of SMs (Xu et al. 2016). Recently, the physiological and molecular effects of salt stress on the synthesis of important SMs in crop species have been reported. These SMs include terpenoids, flavonoids, alkaloids, steroids, and phenolics which play a major role in plant defensive routes against salt stress and thus protect the physiological growth of plants. It has been observed that there was an increased level of anthocyanins in higher concentrations during salt stress, while it is

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reduced in salt-susceptible species. Salt-tolerant alfalfa increases proline concentration under salt stress, and a similar trend was found in Lycopersicon esculentum and Aegiceras corniculatum (Parida and Das 2005). Further, Sesuvium portulacastrum reduces SMs which act as the strong free radical scavengers with a crucial role in the plant’s growth (Slama et al. 2017). Drought, a rampant and multidimensional abiotic stress, often exists in arid and semiarid areas globally. Drought stress causes morphological, physiological, biochemical, ecological, and molecular adaptions in plants; therefore, it directly affects the accumulation of phytochemicals (Mashilo et al. 2017). Such types of phytochemicals are terpenes, alkaloids, and phenolic complexes, via ionic or osmotic stress induction (Isah 2019). As per earlier reports, the level of phenolic compounds in Hypericum brasiliense and Pisum sativum is enhanced when they face drought stress (Dawid and Hille 2018). Phenolic compounds generally accumulate during drought stress due to variations in the phenyl propanoid pathway. It has been reported that drought stress imposes activation of the PAL gene in lettuce plants and expression of many genes engaged in flavonoid biosynthesis in Scutellaria baicalensis (Yuan et al. 2012). Similarly, the level of terpenes in Salvia officinalis is enhanced, while the accumulation of biomass is reduced (Délano-Frier et al. 2011). Drought stress assists oxidative stress, which also enhances flavonoid accumulation as they are excellent free radical scavengers and protect plants from deficiency of water. Several researchers induced and analyzed drought stress in correlation with SM accumulation in vitro; culture medium (containing nutrients, sugar sources, and osmotic stabilizers) can be designed to produce drought environment with associated outcomes on the metabolic processes which ultimately leads to SM accumulation (Ghosh et al. 2018). It has been reported that variation in culture medium results in the synthesis of camptothecin in Nothapodytes nimmoniana and Ophiorrhiza mungos, phenolic compounds in Bellis perennis, and tropane alkaloids in Brugmansia candida (Deepthi and Satheeshkumar 2017). Further total terpenes in the seedlings of Pinus sylvestris and Pinus abies were found to be about 32–39% and 35–45% higher than in control plants, respectively. Photoperiod also has direct effects on phytochemical synthesis in plants. The key components are photoperiod (in length), power (sum), and quality (repeat) (Zoratti et al. 2014). Global warming and increase in pollution which caused depletion in ozone layer also co-related with UV radiations (UV-B: 280–320 nm), which play a prominent role in the composition of plant SMs including alkaloids, terpenoids, flavonoids (Morales et al. 2010), cyanogenic glycosides, tannins, and anthocyanins (Gouvea et al. 2012). Plants have the capacity to adapt themselves in response to photoperiod by accumulating and secreting various SMs, like phenolic compounds, triterpenoids, and flavonoids, most of which have therapeutic potentials (Yang et al. 2013). There are several reports which prove that the duration of light radiation is engaged in the regulation of various phenolic phenylpropane derivatives in the Xanthium species. In Ipomoea batatas, a significant rise in phenolic acid (e.g., hydroxybenzoic acids and hydroxycinnamic) and flavonoid (e.g., flavonols,

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anthocyanins, and catechins) level was observed after a long duration of light exposure (Carvalho et al. 2010). The accumulation of SMs is also affected by light quality. The phenolic compounds of Lactuca sativa are more sensitive to monochromatic light than combined light. Further rise in duration of red light affected phenolic compounds, including caffeic acid, chicoric acid, chlorogenic acid, and kaempferol, as well as ferulic acids, which have tremendous antioxidant potentials. It has been observed that synthesis of vindoline and catharanthine from Catharanthus species was increased after exposure to UV-B radiation (Ramani and Jayabaskaran 2008). Similarly, glycosyl flavonoid level was increased post-UV irradiation. Further, there are some reports (Regvar et al. 2012) which proved the effect of UV exposure on the level of quercetin, catechin, and rutin in Fagopyrum tataricum and Fagopyrum esculentum. It was observed that there was a rise in quercetin in F. esculentum post-UV exposure. Heavy metals are also one of the major concerns as abiotic stress (Cai et al. 2013). There are a lot of reports on the effects of heavy metals on plant growth and physiology; however, there are scanty reports on their direct effects on SM synthesis. Due to them there are variations in metabolic activity of plants which affect synthesis of sugars, photosynthetic pigments, and proteins. This phenomenon occurs due to the inhibition of enzymes engaged in the synthesis of these phytochemicals (Verpoorte et al. 2002). Plants synthesize primary metabolites for essential functions such as growth and development and SMs for specific functions. Plants synthesize a large number of SMs that are required for survival under adverse environmental conditions. In plants, a wide variety of SMs has been identified. A balanced production of SMs is required for the optimum growth of plants under changing environmental conditions. SMs have various functions that include interspecies communication, enzyme activity regulation, signaling, and defense. SMs are usually colored compounds with fragrances that contribute to color, taste, and specific odor in plants. SMs also help plants to mediate interactions with other organisms, such as pollinators, pathogens, and herbivores (Hussain et al. 2012). Despite the research done on SMs, its importance is not fully understood. However, because of advancements in research and technology, their roles have been clarified. For instance, genome sequencing of some species and gene editing techniques have revealed the importance of SMs in barley, tomato, Pinus taeda, pear, and rice (Consortium 2012; Wu et al. 2013). Recently SMs became a subject of greater interest because of their significant application in several fields. In particular, their role and applications in medicine, nutrition, cosmetics, and plant stress physiology are more prominent (Ngo et al. 2013) (Fig. 12.3). SMs show a wide array of defensive functions and signaling under both biotic and abiotic stress conditions. Furthermore, research on biosynthetic pathways of a plant’s secondary metabolism could improve the knowledge of SMs in plant stress physiology. Therefore, it is necessary to develop efficient and innovative approaches to understand SM roles in improving crops against drought stress.

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Fig. 12.3 Role of secondary metabolites in various stress mechanism

3 Functional Genomics and Secondary Metabolites Functional genomics has reverse genetics as a popular tool that could be used for secondary metabolite pathway molecular elucidation. To find out the functions of genes, EST library, or a sequenced genome of plants, the RNA interference-based knockdown power is used (Alonso and Ecker 2006). However, desired natural products are produced by trees (in some cases) and exotic plants, where these methods cannot be feasible due to unreasonable time scale and lack of transgenesis protocols.

4 Fungal Endophytes for Synthesis of Secondary Metabolites There are different thoughts about natural product origin in plants (Hussain et al. 2012). One says endophytic microbes and plants evolved together with pathways for the production of these products, whereas the other says that between microbes and plants, an ancient horizontal gene transfer took place. Another one says that natural products were synthesized by either endophytic fungi or plants and carried away towards other symbionts. Radio labeled precursor amino acid in a biosynthetic pathway study reveals that the metabolic pathway for secondary metabolite production in plants and endophytic fungi is similar but distinct (Zhang et al. 2009). The question arises about the bioactive phytochemicals whether they are produced by plants itself or as a

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consequence of collaborative association with microorganisms in their tissues. Accumulation of secondary metabolites in fungi and plants increases due to a combination of inducing factors from endophytic fungi and plants; this suggests that in secondary metabolite biosynthesis, fungal endophytes have a crucial part. Therefore, it is important to explore the symbiotic association and effects of endophytes and plants on each other at the time of other bioactive compound synthesis processes. This can help in preparing the future framework for the production of natural products through metabolic and genetic engineering (Hussain et al. 2012).

5 Role of Plant Growth-Promoting Rhizobacteria in Synthesis of Secondary Metabolites Plants synthesize various secondary metabolites under unfavorable growth conditions that play an essential role in protecting plants from harmful effects of stresses; various studies suggest that the synthesis of secondary metabolites in plants during unfavorable conditions increases when plants like Dendrobium moniliforme, Rhus tripartitum, and Periploca laevigata are inoculated by PGPR. PGPR acts as a biotic elicitor which results in hypersensitivity response resulting in “induced systemic resistance” (ISR) leading to the expression of various genes, which trigger the accumulation of diverse plant defensive bioactive molecules and secondary product in plant cells (Jadhav et al. 2020; Baba et al. 2021; Basu et al. 2021). Plant growth-promoting rhizobacteria (PGPR) are classified as a group of freeliving bacteria; these bacteria colonize the rhizosphere to benefit the root growth and in turn support plant growth. Bacillus and Pseudomonas spp. are predominant PGPR; various other bacteria from diverse genera are identified as PGPR. PGPR employs various strategies to help plant growth of which solubilization of inorganic phosphates, production of phytohormones, increased iron nutrition through ironchelating siderophores, and affecting the plant signaling pathways are some of the major ways in which PGR works. PGPR decrease the populations of root pathogens and other deleterious microorganisms in the rhizosphere. Although PGPR was realized for its role as a biocontrol agent of soilborne bacterium, based on the mode of action, PGPRs were divided into two groups, viz., biocontrol-PGPBs and PGPBs (Jabborova et al. 2020a, b; Kalam et al. 2020). The microbial community is associated with the roots, i.e., rhizomicrobiome, which has appealing, diverse, and unique patterns of microbial colonization, because of which it finds its importance in agriculture due to the rich diversity of root exudates and plant cell debris. Some key roles of microbes like rhizomicrobiome are improved soil texture, nutrient acquisition and assimilation, and secreting and modulating extracellular molecules such as antibiotics, hormones, secondary metabolites, and various signal compounds, all of which are responsible for plant growth. The microbes and compounds they secrete constitute valuable bio-stimulants and play pivotal roles in modulating plant stress responses (Baker et al. 2018; Kannepalli Davranov et al. 2021; Kapadia et al. 2021).

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Based on the area inhabited by rhizobacteria, they are classified into two main types, namely, extracellular plant growth-promoting rhizobacteria (ePGPR) and intracellular plant growth-promoting rhizobacteria (iPGPR). ePGPR inhabit the rhizosphere (on the rhizoplane) or in the spaces between the cells of the root cortex, which comprises bacteria genera like Azotobacter, Serratia, Azospirillum, Bacillus, Caulobacter, Chromobacterium, Agrobacterium, Erwinia, Flavobacterium, Arthrobacter, Micrococcus, Pseudomonas, and Burkholderia, whereas iPGPR mainly inhabit inside the specialized nodular structures of root cells; these include Allorhizobium, Bradyrhizobium, Mesorhizobium, and Rhizobium, as well as Frankia species (Vedamurthy et al. 2021; Khan et al. 2015; Kour et al. 2021). Rhizobacteria induce resistance through the salicylic acid-dependent SAR pathway or require jasmonic acid and ethylene perception from the plant for ISR (Beneduzi et al. 2012). Various metabolites significantly increased upon PGPR induction include nonenzymatic antioxidants including phenols, flavonoids, DPPH radical scavenging capacity of the plant extract, and oxygenated monoterpenes of essential oil. An increase of nonenzymatic antioxidant contents helps withstand against drought stress (Asghari et al. 2020). The potential of halotolerant plant growth-promoting rhizobacteria (HT-PGPR) and their secondary metabolites was realized in improvement of salinity stress in affected plants/crops. HT-PGPR are capable of generating a vast range of secondary metabolites for protection of both the host bacterial cells and symbiotic plant and plant growth promotion even under salinity stress. Apart from producing phytohormones and siderophores and solubilization of nutrients such as phosphorus (P), zinc (Zn), potassium (K), and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase to lower stress ethylene level, HT-PGPR have been reported to produce certain metabolites playing a direct role in salt tolerance, and these include osmoprotectants, exopolysaccharides (EPS), and volatile organic compounds (VOCs). Many of these metabolites are exclusively produced during abiotic stress conditions and help in the plant’s survival under adverse environmental conditions, maintaining ionic equilibrium through Na/K transporter, improving water potential, and expressing salt overly sensitive (SOS) genes involved in stress tolerance under saline conditions (Abbas et al. 2019; Sunita et al. 2020; Kusale et al. 2021a, b). PGPR produce a variety of primary or low-molecular-weight secondary metabolites in order to function as biofertilizers, phytostimulators, rhizomediators, and biopesticides. PGPR also are involved in suppressing pathogenic fungi which adversely affect plants undergoing salinity stress (Mishra et al. 2018; Manasa et al. 2021; Najafi et al. 2021). Osmoprotectants also called compatible solutes like turanose, gentiobiose, and palatinose or solutes like amino acids, e.g., glutamate, proline, alanine, serine, threonine, and aspartic acid; quaternary amines, e.g., glycine betaine and carnitine; imino acids (pipecolate); K; and tetrahydropyrimidines (ectoines) are some of the major compounds produced by PGPR under salinity stress. PGPR consortium of S .marcescens, B. amyloliquefaciens, P. putida, P. fluorescens, and B. cereus significantly increased the number of fruits/plants; the three bacterial species, viz., B. amyloliquefaciens, B. subtilis, and B. brevis have significantly improved the activity of defense-related enzymes in tomato plants infected with bacterial canker. The rhizospheric bacteria significantly improved

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shoot and root dry weights, enhanced and modulated production of secondary metabolites, and induced resistance to various diseases caused by bacterial and fungal pathogens; they could also solubilize phosphorus and bacteriocin (Patel et al. 2018; Reshma et al. 2018; Kousar et al. 2020; Nithyapriya et al. 2021). PGPR are well known for reducing heavy metal toxicities. Pseudomonas aeruginosa and Burkholderia gladioli modulated secondary metabolites such as phenolic compounds anthocyanins, flavonoids, and osmolytes (total osmolytes, total carbohydrates, reducing sugars, trehalose, proline, glycine betaine) in plants affected by Cd toxicity (Khanna et al. 2019; Sagar et al. 2020a, b, 2022). Plants inoculated with PGPRs are benefitted with increased vigor indexes such as germination rate, dry matter production, radical growth, leaf area, chlorophyll content, disease control, drought resistance, shoot weight, and other microbial activities due to above benefits. PGPRs belonging to different genera have been commercialized for agricultural usages. The direct effects of PGPR include the secretion of plant growth promoters (indoleacetic acid, cytokinins, gibberellic acid, and ethylene), fixing of atmospheric nitrogen through the symbiotic association to form root nodules, and helping in the solubilization of phosphate in the soil. In an indirect way, PGPRs reduce or completely prevent the possible harmful effect of one or more plant pathogens by competing with nutrients, produce siderophore, and induce resistance in the plant (Swamy et al. 2016; Sayyed et al. 2015, 2016, 2019; Shaikh et al. 2018; Sharma et al. 2013, 2016). The role of PGPR especially Pseudomonas sp. in the mitigation of heavy metal toxicity is now vastly studied; it is well studied as a biocontrol agent and also acts as a xenobiotic for heavy metals (Singh et al. 2018; Vafa et al. 2021; Vinay et al. 2016; Wani et al. 2016; Zahoor et al. 2017; Zope et al. 2019; Zaman et al. 2021).

6 Therapeutic Potential of Plant Secondary Metabolites Natural products are a rich depository of wide efficacy of pharmacological effects to cure many metabolic disorders. That is why plants constitute crucial phytochemicals which have been recommended traditionally for many decades for improving health and/or curing diseases. Various efficacies include antibacterial, antioxidant, antidiabetic, insecticidal, antifertility, antitumor, and other activities (Chen et al. 2016). A lot of research has been devoted to anticancer activities which are a major cause of mortality among people globally. There are a lot of biochemical and molecular therapies for effective treatment against cancers, but still a detailed study is needed today to find novel compounds synthesized from phytochemicals with better bioefficacy (Nyaboke et al. 2018). Some of the compounds attributed are celastrol, ursolic acid, asiatic acid, auraptene, saidmanetin, lupeol, and indole-3carbinol. These phytochemicals are prominent in stromal microenvironment, immune response, signaling to control cell growth and apoptosis (Nyaboke et al. 2018). There are different medical issues that diverted attention towards medicinal plants to provide resistance against different microbes. It is estimated that around

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35,000 mortality occurs among people in the European Union, due to contaminations caused by impervious bacteria (Fischer and Bild 2019). It has been proved that the exploration of novel substances with antimicrobial potentiality is a key point of urge in base level experiments and is a prime need of the pharmaceutical companies (Othman et al. 2019). The main mechanism is that when polyphenols and DNA make complexation, they induce variations in protein synthesis in pathogens. There are some reports which prove that these polyphenols lead to disintegrating cell membranes resulting in cell apoptosis (Martelli and Giacomini 2018). There are some reports which prove that monoterpenes percolate with phospholipids of cell membranes of certain disease-causing microbes due to their lipophilic nature. The free radical scavenging potential has also been reported due to certain phytochemicals isolated from medicinal plants. The key components of such potential are flavonoids, tannins, and polyphenols. Flavonoids act primarily to control pH and arrest free radicals to induce the flavinic radical, much less reactive, thus inhibiting free radical formation. Compounds like quercetin can chelate transition metal ions like iron or copper, thus acting as a prominent antioxidant agent (Wang et al. 2018).

7 Conclusion In the present scenario, experiments based on the synthesis of secondary metabolites and their applications along with therapeutic potential have been gaining a lot of attention globally. Innovations in effective tools for the isolation of extracts of these medicinal plants require more sophisticated research in the near upcoming future. Thus, abundance of plant origin bioactive metabolites and their value in medicine is undisputed. This has generated tremendous interest and optimism among scientists and created unprecedented opportunities in the field of biotechnology and rapidly expanding natural product industries. Among such efficacious stratagems for the synthesis of these secondary metabolites from requires phytochemical analysis responsible for various biological activities thus following the protocol for purification of active compounds. Nevertheless, in order to ensure constant quality and therapeutic efficacy, one of the challenges of herbal product is standardization before making it a commercially usable product. Phytochemicals with a lot of synergistic potential should be avoided if they bear some toxicity cases of dose level required in clinical trials. Attention should be devoted towards secondary metabolites till their chemical behavior is fully elucidated, and focus should be on their standardization to incorporate what is known, since there is nil issues in overlooking the perception of experience!

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Chapter 13

PGPM: Fundamental, Bioformulation, Commercialization, and Success at Farmer’s Field Manjunath Hubballi, S. Rajamanickam, Ritu Mawar, Reshma Tuladhar, Anjana Singh, R Z Sayyed, and S. Nakkeeran

1 Introduction The ever-increasing global population in geometric progression is proposed to be 9.7 billion by 2050 (UN 2019). In this context, the ultimate concern that strikes to mind is about the capability of planet Earth to meet the basic needs of humanity. The present day situation, emphasize the fact that there is decrease in the arable land. Besides, the biotic and abiotic stress is going on emerging as a threat for crop cultivation. Further natural calamities, degradation of land and unexpected heavy downpour during non monsoon seasons also remains as a serious threat to increase the productivity. As per the recent data of United Nations, 925 million people in the world are undernourished with maximum percent of undernourished people being in Asian countries. On an average, about 795 million people, i.e., one out of nine, go hungry, and one in three is malnourished in India alone. Hence, zero hunger and

M. Hubballi University of Horticultural Sciences, Bagalkot, India S. Rajamanickam Tamil Nadu Agricultural University, Coimbatore, India R. Mawar Division of Plant Improvement and Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India R. Tuladhar · A. Singh Central Department of Microbiology, Tribhuvan University, Kathmandu, Nepal R. Z. Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India S. Nakkeeran (*) Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_13

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malnutrition is the goal, and in order to achieve this, the country needs 45–90 billion MT food every year. To achieve this goal, more food needs to be produced from less resources, which is an arduous task to achieve. In search of ways to increase food production, man has switched over from organic to chemical-dominated agriculture by name of the green revolution. The so-called green revolution has virtually brought revolution in production as witnessed by the 295 million tonnes of food grain production in 2019–2020 (DAC 2019). Under these circumstances, though we have the capability to feed the huge population, the repercussions of chemical-centered agriculture are a serious issue to be noted. The Indian pesticide market is growing at an alarming rate as witnessed by 181 billion worth in 2017, and projected growth is 292.9 billion in 2023 (https:// www.transparencymarketresearch.com/). The figure clearly emphasizes the dependency on pesticides for food grain production. At this juncture use of biological arsenals for disease management in agriculture is a wise step. Soil is an excellent habitat for microbes to grow and survive. It harbors innumerable microbes including a large population of bacteria. According to Blaine Metting (1993), 1 g of soil is composed of 108–9 bacteria, 105–8 actinomycetes, 105–6 fungi, 103–6 microalgae, 103–5 protozoa, 101–2 nematodes, and 103–5 other invertebrates. Few bacteria living in soil are having capability to colonize the roots and rhizosphere, and these bacteria are broadly termed as rhizobacteria (Kennedy 2005). These rhizobacteria are reported to have the ability to promote growth and contribute for the protection from diseases in many crops (Meena et al. 2016c). The bacteria widely used include species of Pseudomonas and Bacillus. This chapter focuses on PGPRs and their production, formulation, commercialization, and legal issues related to registration.

2 PGPRs: Plant Growth-Promoting Rhizobacteria The rhizospheric soil is reported to be nutrients rich compared to other bulk soil owing to the fact that variety of exudates of root accumulate in this vicinity. The sugars and amino acids present in the exudates yield energy and nutrients to a vast number of microorganisms (Gray and Smith 2005). In support of this, Weller and Thomashow (1994) reported the presence of 10–100 times more bacterial population in rhizospheric soil in comparison with that of bulk soil. Of the bacteria present in rhizosphere, all need not necessarily be beneficial to plants. The bacteria associated with plants are therefore grouped as beneficial, deleterious, and neutral (Dobbelaere et al. 2003). Kloepper and his coworkers late in the 1970s defined the term PGPR for the first time to the free living: beneficial bacteria present in rhizosphere which aid both in growth promotion and disease suppression. It is proved beyond doubt that only 1–2% of bacteria present in rhizosphere region aid in growth promotion (Antoun and Kloepper 2001), whereas a vast number of bacteria are reported to aid in arresting the growth of deleterious plant pathogen through multiple mode of actions (Meena et al. 2016a). The diverse genera of bacteria are identified as PGPRs,

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but among which species Pseudomonas and Bacillus constitute major group (Podile and Kishore 2006).

2.1

Classification of PGPR

PGPRs have been classified into various groups on the basis of location, activities, and functions.

2.1.1

Based on Location

Based on the location in which the bacteria reside, they are grouped as extra- and intracellular PGPRs (Martinez-Viveros et al. 2010).

2.1.1.1

Extracellular PGPRs (ePGPRs)

Extracellular PGPRs are found outside the cells in the rhizoplane and rhizosphere and in intercellular spaces in the root cortex. The species of Bacillus and Pseudomonas constitute the examples of this category of PGPRs as they either live in soil or exist as endophytes in the intercellular space of plants (Sharma et al. 2017a). Based on degree of association with plant roots, these ePGPRs can be further subdivided into three categories such as (a) PGPRs living near root but not in contact with roots; (b) root surface colonized; and (c) living in intercellular space or root cortex (Vessey 2003).

2.1.1.2

Intracellular PGPRs (iPGPRs)

These bacteria generally reside in specialized structures like nodules. The perfect examples of this category are Frankia and Rhizobia, and both of these bacteria are connected to higher plants. These exist inside the cell and help in nitrogen recycling process (Sharma et al. 2017a).

2.1.2

Based on Function

On the basis of functions that are catered by PGPR, they are categorized into three categories, viz., biocontrolling bacteria, plant growth-promoting bacteria, and stress homeoregulating bacteria.

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Plant Growth-Promoting Bacteria

The bacteria residing in the rhizoplane has the ablity to promote plant growth are classified as PGPR. The promotion of growth of plants by these bacteria would be by multiple means. It is due to the production of phtohormones including production of gibberellic acid, auxins, cytokinins, ethylene (ET), abscisic acid, or indole acetic acid (Spaepen and Vanderleyden 2011; Glick 2012; Ahemad and Kibret 2014; Wang et al. 2015); production of iron-chelating siderophore (Khan et al. 2009; Rajkumar et al. 2010; Ahemad and Kibret 2014); fixing of atmospheric (Ahemad and Khan 2012; Kuan et al. 2016); and solubilization of phosphates in soil and thereby making them available to plants easily (Ahemad and Kibret 2014; Gupta et al. 2015; Meena et al. 2016b).

2.1.2.2

Biocontrolling Bacteria

Certain bacteria residing in the rhizosphere have the capability to produce toxic compounds like antibiotics, enzymes, or any other compounds which will aid in suppressing the growth of pathogens and at the same time help in the growth of plants. The major substances produced by this group of bacteria are antibiotics, chitinase, pectinase, cellulase, ethylene, cyanides, and antimicrobial peptides (Bashan and de Bashan 2010; Bhattacharyya and Jha 2012; Meena et al. 2016a). The examples of bacteria producing various inhibitory compounds are hereunder (Bhattacharyya and Jha 2012). Mora et al. (2015) found the positive correlation between the presence of AMP gene and antibacterial activities of Bacillus spp. They reported that most Bacillus produces the AMP genes such as bacillomycin (BmyB), fengycin ( fenD), and surfactin (srfAA). However, presence of several AMP genes in group of antagonists including B. amyloliquefaciens and B. subtilis showed higher level of antagonistic activities against bacterial pathogen. Interestingly, the effective isolate B. amyloliquefaciens strain VB7 showing antifungal activity against Sclerotinia sclerotiorum produced ten different AMP genes including iturin, bacilycin, fengycin, bacillomycin, surfactin, subtilosin, and subtilin. The AMP-producing B. amyloliquefaciens delivered through root dip method effectively reduced the stem rot of carnation under protected cultivation (Vinodkumar et al. 2017). Antimicrobial activity of B. amyloliquefaciens (Bs_Abi) was confined due to presence of nine AMP genes for synthesis of iturin, bacillomycin D, subtilin, bacilycin, and surfactin. The soil application of liquid formulation of strain BsAbi significantly reduced the disease incidence of bacterial wilt caused by Ralstonia solanacearum in eggplant (Sakthivel et al. 2019). Similarly, B. methylotrophicus TA-1 isolated from rhizosphere soil of maize expressed the gene responsible for synthesis of iturin and surfactin and showed strong antifungal activity against Fusarium graminearum. The application of strain TA-1 delivered through seed biopriming effectively reduced the stalk rot of maize under greenhouse and field conditions (Cheng et al. 2019). The effective B. subtilis (AP) and B. amyloliquefaciens (VB7) showing antifungal activity against Botrytis cinerea

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Table 13.1 Inhibitory compounds produced by bacteria against target pathogens Bacteria Bacillus B. cereus, B. thuringiensis, B. subtilis B. subtilis B. subtilis Burkholderia cepacia, Pseudomonas fluorescens, Enterobacter agglomerans

Pseudomonas fluorescens

Streptomyces cacaoi Streptomyces hygroscopicus

Inhibitory compounds Bacillomycin Zwittermicin A Iturin Iturin A, surfactin Pyrrolnitrin

2,4-DAPG, pyoluteorin, phenazines Polyoxin D Geldanamycin A

Target pathogen/host Aspergillus flavus Phytophthora, Sclerotinia sclerotiorum Pythium ultimum, Rhizoctonia solani, Fusarium oxysporum Rhizoctonia solani Gaeumannomyces graminis var. tritici, Agrobacterium tumefaciens, Clavibacter michiganensis, Xanthomonas campestris, Pseudomonas syringae Xanthomonas oryzae, Pythium ultimum, Gaeumannomyces graminis var. tritici R. solani R. solani

causing blossom blight of rose exhibited the presence of genes for synthesis of iturin, subtilin, bacillomycin, bacilysin, and surfactin (Nakkeeran et al. 2020). AMP genes in the bacterial antagonist play a moajor role in the suppression of plant disease (Table 13.1).

2.1.2.3

Stress Homeoregulating Bacteria

Sgroy et al. (2009) coined the term ‘plant stress homeoregulating bacteria’ (PSHB). These bacteria have the unique ability to promote growth under ideal biotic or abiotic stress circumstances. These bacteria are also reported to improve the abiotic stress tolerance like salt, drought, and nutrient deficiency in plants by producing certain enzymes mainly abscisic acid (Cohen et al. 2015), salicylic acid (Beneduzi et al. 2012), jasmonic acid (Vejan et al. 2016), other stress-related phytohormones (George et al. 2016), and stress signaling molecules (Kaushal and Wani 2016).

2.1.3

Based on Activities

Somers et al. (2004) categorized the plant growth-promoting rhizobacteria into the following five categories.

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Biofertilizers

Many PGPRs are reported to be involved in nutrient cycling and thereby aid in the growth of plants. The important PGPRs involved in nutrient movement are nitrogen fixers such as Azospirillum, Rhizobium, Azotobacter, Bradyrhizobium, and Nitrosomonas; phosphate solubilizers such as Bacillus, Pseudomonas, and Mycorrhiza; and the general growth-promoting bacteria such as Bacillus and Pseudomonas.

2.1.3.2

Phytostimulators

Under this category bacteria having competences to promote growth by stimulation of certain phytohormones are grouped. Examples of this category are Pseudomonas, Azospirillum, Bradyrhizobium, etc. Phytohormones are the organic compounds which influence the plant biochemical, morphological, and physiological processes in extremely low concentrations, and its synthesis is regulated preciously (Fuentes-Ramirez and Caballero-Mellado 2005). It is concluded from the study that PGPRs stimulate growth of plants through production of GA (Bottini et al. 2004) and auxins (Spaepen et al. 2007) and regulating the production of ethylene and cytokinins (Glick et al. 1998; Timmusk et al. 1999).

2.1.3.3

Rhizoremediators

The agricultural wastage, industrial effluents, and hazardous chemicals being used in agricultural production contribute a lot to polluting soil and water and thereby make them unfit for usage. Under such circumstances, few bacteria PGPRs are used to degrade herbicide, pesticides, industrial chemicals, and other hazardous chemicals, thus increasing soil fertility. The examples of this category of bacteria include Alcaligenes denitrificans, Pseudomonas putida, Pseudomonas fluorescens, Pseudomonas vesicularis, Pseudomonas paucimobilis, Pseudomonas cepacia, Mycobacterium sp., Corynebacterium renale, and Micrococcus sp. (Castro et al. 2009).

2.1.3.4

Biopesticides

The bacteria having capacity to produce the toxic substance and suppress the growth of deleterious microbes/pathogens are grouped under this category. The antibiotic production potential of PGPRs is well-known and has been reported to be most promising mode of action in many plant pathogens. The classical examples include species of Bacillus and Pseudomonas.

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Bioprotectants

The International Biocontrol Manufacturers Association (IBMA) uses the term bioprotectants collectively as global term for all biocontrol technologies. It is to protect against unwanted organisms including pests and pathogens, and as such its origin is from nature. This category also includes a variety of microorganisms that aid in disease prevention and enhanced the growth, both directly and indirectly.

3 Deciphering the Mechanisms Involved in Biocontrol of Plant Diseases by PGPR Plant disease is the result of complex interaction among disease components involving susceptible host, virulent pathogen, and congenial time. The successful management practice for disease must involve breaking the interaction of these components. In order to achieve this, the PGPRs employ a vast number of actions (Castro et al. 2009). The major modes of actions are discussed hereunder.

3.1

Competition

It is one of the modes of action of PGPRs, wherein the bacteria compete with pathogenic microbes for space, water, and nutrients (Philippot et al. 2013). In general, the rhizosphere is more frequently a nutrient-limited niche from microbe’s perspective, and for microbe to be successful in colonizing, it has to compete for nutrient, water, and carbon source effectively. This will be achieved mostly by occupying the readily available sites where resource is seldom a limiting factor, for example, root exits of secondary roots, epidermis cells which are damaged, and nectarines. Sivasakthi et al. (2014) reported that the competition for iron in rhizosphere is more than other elements, and PGPRs having capability of chelating iron have an added advantage.

3.2

Antibiotic Production

The most important mechanism of PGPRs is production of deleterious antibiotics which suppresses the growth of microbial pathogens directly or by way of hindering certain enzymes associated with growth. As per Haas and Defago (2005), phloroglucinols, pyrrolnitrin, pyoluteorin, phenazines, hydrogen cyanide, and cyclic lipopeptides are the six major classes of antibiotic which play an important role in the control of plant diseases. Important antibiotics produced by PGPRs include

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phenazine, 4-diacetylphloroglucinol (DAPG), tropolone, tensin, amphisin, oomycin A, pyoluteorin, and pyrrolnitrin produced by species of Pseudomonas. The species of Bacillus produces iturin, surfactin, fengycin, xanthobaccin, kanosamine, oligomycin A, and zwittermicin A antibiotics to suppress the growth of deleterious pathogens (Lugtenberg and Kamilova 2009, add one more latest reference relating to cyclic lipopeptides). A bacterium may produce one or more antibiotics to inhibit the growth. However, the production of antibiotics depends largely on the availability of minerals, including zinc, carbon sources, pH, and temperature (Bhatia et al. 2016).

3.3

HCN Production

Glycine, an amino acid, through the action of HCN synthase produces HCN (Blumer and Haas 2002). Many PGPRs are reported to have the capability of producing HCN which inhibits the function of many metal enzymes such as cytochrome oxidase, thereby affecting energy supply system of cells leading to death. Pseudomonas, Bacillus, and Rhizobium are the species synthesizing HCN (Ahmad et al. 2008).

3.4

Polysaccharide Production

Exopolysaccharides (EPS) constitute the most important part of soil organic matter, and they account for 40–95% of dry weight of bacteria (Flemming and Wingender 2001). Bacteria are reported to produce both capsular and slime EPS. The important role of EPS is protection, surface attachment, biofilm formation, microbial aggregation, plant-microbe interaction, and bioremediation (Manca de Nadra et al. 1985).

3.5

Hydrolytic Enzyme Production

Several PGPRs employ the production of hydrolytic enzymes as means to obtain their carbon source by degrading cell wall of many plant pathogenic fungi and other organisms. The major enzymes produced by PGPR include proteases, chitinases, lipases, and cellulases (Naing et al. 2014; Patel 2015). In many cases, the cell wall being the virulence factor, by production of these enzymes, PGPRs destroy the virulence system in pathogen and thereby help to control disease development (Kumar et al. 2012).

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Induced Systemic Resistance

It is a state of enhanced defense capacity in plants elicited by one or more PGPR strains. In other words, it is a condition wherein the plants’ own defense is potentiated by PGPR against subsequent biotic stress. Induced systemic resistance in plants is achieved by jasmonic acid and ethylene signaling pathways, wherein these hormones stimulate defense response against diverse pathogens (Compant et al. 2005). The structural components of bacteria, viz., lipopolysaccharides (LPS), flagella, siderophore, and lipopeptides, and antibiotic production capability are the main determinants of ISR induction by PGPR (Pieterse et al. 2014; Naureen et al. 2015). There has been a report on wide group of PGPRs having ISR induction property, and the important one is species of Bacillus, viz., B. amyloliquefaciens, B. cereus, B. subtilis, B. sphaericus, B. pasteurii, B. pumilus, and B. mycoides and species of Pseudomonas, viz., P. putida and P. fluorescence, and endophytic actinobacteria (Bhattacharyya and Jha 2012; Jacob and Sudini 2016).

4 Commercialization of PGPRs Commercialization of any potent PGPR strain involves the following important steps (Doraisamy et al. 2001): • • • • • • • • • • • •

Isolation and identification of antagonist Screening of PGPR for the antagonistic potential Testing the efficacy of PGPR under in vitro and in vivo conditions Standardization of mass production technique Standardization of fermentation technique Development of formulation of PGPRs Assessing the shelf life of formulation Standardizing delivery systems Toxicological data generation Registration Establishment of public-private partnership Quality control

• Isolation and identification of antagonist—The success in disease management through biological methods largely depends on the isolation of PGPR strain with potential to inhibit target pathogen both under laboratory and under field conditions. This can be achieved by wide range of methods. One of the most widely used approaches is use of suppressive soil for isolation. The isolation can be done either through serial dilution technique or by bait technique. It is generally believed that location-specific strains will have more advantage of being adjusted to particular ecological niche than other strains and thereby exhibit more potential

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in arresting growth of pathogen. In addition to this, the correct identification of the antagonist both through traditional and molecular approaches is highly essential in order to commercialize the product in later stages. • Screening of PGPR for the antagonistic potential—The success or failure of PGPR as bioagents is decided at this step. The rigorous screening of bioagents for its antagonistic potential is more important from the point of its larger viability in field conditions. As such there is no generalized protocol to screen all the bioagents; it depends on the specific pathogen, type of crop, and crop cultivation method. For instance, finding out a potent bioagent against postharvest diseases may involve the screening of microbial agents that colonize on the fruit surface very quickly to exclude pathogenic organisms (Larkin et al. 1996). Despite high efficacy of bioagents under in vitro conditions to suppress the pathogen growth, many researchers report the no connection between in vitro and efficacy of the same antagonist under field conditions. For example, in the case of apple scab disease, the bacteria and yeast showing highest inhibitions under dual culture failed to reduce the disease incidence under in vivo conditions (Burr et al. 1996). This clearly explains shortfalls of screening methods. The effective antagonist should have more competitive saprophytic ability, the ability to synthesize high level of antibiotics and increased level of enzyme production involved in lysis of cell wall and also aid in plant growth promotion (Nakkeeran et al. 2005). The rigorous screening process must consider all the components with equal weightage so as to identify the right antagonist to take further for commercialization. • Testing the efficacy of PGPR under in vitro and in vivo conditions—Mere in vitro evaluation of antagonist against pathogen using dual culture, detached leaf assays on plantlets does not suffice the conditions for selecting candidate bioagents for commercialization (Fravel 1992). Ascertaining a successful antagonist must involve a rigorous test, wherein antagonist is exposed to crop plants under controlled conditions in the presence of virulent pathogen. The exposure of crop plants with specific antagonist and application of high level of pathogen inoculum can produce reliable information on efficacy of bioagents under controlled conditions (Nakkeeran et al. 2005). Further, the promising antagonist should be tested under field conditions. Influence of environmental factor on the efficacy of antagonist against particular disease can be avoided with testing under field in at least 10–15 different locations and also with different seasons and varieties (Jeyarajan and Nakkeeran 2000). In many cases, under field conditions, it is advisable to include one recommended fungicide as one of the treatments for comparison. • Standardization of mass production technique—The high cost associated with most of biocontrol agents owing to the higher cost of substrates and lower biomass productivity is a major hurdle in production of bioagents in commercial scale (Fravel et al. 1999). The very purpose of production is to produce the most potent bioagents in large quantity in very lesser duration. In many cases, even if the production technique of bioagents is producing more propagules, it may not yield the most potent propagules all the time (Jackson 1997; Brannen and Kenney

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1997). This might be due to the various factors, viz., temperature, osmotic potential, carbon source, and pH. In general, the mass multiplication of bioagents is established mainly through liquid, semisolid, and solid fermentation techniques (Lewis 1991; Manjula and Podile 2001). The success of bioagents on commercial scale depends largely on constant performance of bioagents, huge market demand, safety and stability, low investment cost, and longer shelf life (Nakkeeran et al. 2005). • Standardization of fermentation technique—The word fermentation is derived from Latin word fervere meaning to boil and was used first time by Louis Pasteur, and hence, he is aptly considered as father of fermentation. The fermentation science is also called zymology. According to Kure et al. (2016), fermentation is a process of producing specific metabolites from microorganisms that are cultured in a specific medium under said condition. There are two main categories of fermentation, viz., batch and continuous fermentation. In batch fermentation, nutrients are supplied only once to microbes at the initiation of fermentation. On the other hand, in continuous fermentation, nutrients are fed at regular interval to microbes. In case of continuous fermentation, microorganisms are maintained at exponential phase, and the production is more compared to batch fermentation (Bakri et al. 2012). The other way of classification of this technology is based on state of substrate being used, viz., solid state and submerged/liquid fermentations (Coelho et al. 2011).

4.1 4.1.1

Types of Fermentation Liquid Fermentation

This type of fermentation is generally employed for mass production of bacterial and fungal biocontrol agents. In order to mass produce, the required medium should be available easily with appropriate nutrient content. The species of Bacillus and Pseudomonas are mass produced using Kings B and nutrient broth, respectively, in large scale through this method (Manjula and Podile 2001; Nakkeeran et al. 2005).

4.1.2

Solid Fermentation

A large number of organic substrates have been documented to be used for this fermentation. Lewis (1991) reported use of solid fermentation media comprising of inert material and food bases would be useful in mass multiplication of biocontrol agents. The different substrates used are wheat bran, straws, decomposed coir pith, paddy chaff, sorghum grains, moistened bagasse, farmyard manure, sawdust, and any other substance rich in cellulose (Nakkeeran et al. 2005).

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Development of Formulation of PGPRs

Despite the fact that a large number of biocontrol agents are tested under in vitro conditions against a range of microbial pathogens, only a few out of them are coming out as formulations of bioagents intended for larger-scale usages. The probable reason for this would be an inconsistency of biocontrol agents under field conditions owing to lack of knowledge, inherent problems associated with screening, and trouble in getting an effective formulation (Emmert and Handelsman 1999). Hence, an effective formulation development constitutes a milestone in success of biocontrol agents. Formulated microbial bioagents are composed of bioagents and ingredients needed for their activity, growth, and effectiveness against a range of pathogens (Schisler et al. 2004). The formulation of biocontrol agents helps to stabilize organism at various stages of production, distribution, and storage. Further, a good formulation supports in production, maintenance, transport, and end usage of the product and also protects from hazardous environmental factors. In addition to this, it enhances the activity of organism.

4.2.1

Characteristics of Good Formulation

• The formulation should yield the increased shelf life of PGPRs. • On application, the formulation should not reflect any phytotoxic effect on intended crop plants. • It should have high dissolving ability so as to release the PGPRs immediately. • It must be compatible with all the available agrochemicals being used in particular cropping pattern. • The carrier material used must be readily available and cost economic. • It should give protection to PGPRs under all adverse conditions of environments. • It should yield effective and reliable disease control in plants (Jeyarajan and Nakkeeran 2000).

4.2.2 4.2.2.1

Solid Formulations Talc Formulation

It is one of the most widely used formulations for biocontrol agents. It is powder form and chemically known as magnesium silicate (Mg3Si4O10(OH)2) otherwise known as steatite or soapstone. It is made of chloride and carbonate with various minerals to support the growth. Talc powder, which has a low water balance, is inert, has low hygroscopicity, prevents the formation of hydrate bridges, and supports longer storage times, makes talc a widely used formulation (Nakkeeran et al. 2005). The usage of talc as a carrier material for PGPR was reported by Kloepper and

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Schroth (1981). There have been an enormous number of biocontrol agents comprising bacteria and fungi and biofertilizers developed using this carrier material. The talc-based formulation offers storage life of more than 6 months as evidenced by maintaining colony-forming unit (CFU). Bora et al. (2004) recorded the survivability of two strains of P. putida with a period up to 6 months in talc-based formulations. The talc-based formulations of Streptomyces griseus were demonstrated to have shelf life of 105 days under normal storage conditions. Further, Sundaramoorthy and Balabaskar (2012) reported the shelf life of 4 months for Bacillus subtilis and P. fluorescens in talc formulations. In addition to this, in talc formulation, a PGPR known as Ochrobactrum anthropi TRS-2 would survive up to 9 months, and this formulation helped to reduce the brown root rot of tea (Chakraborty et al. 2009).

4.2.2.2

Sawdust-Based Formulation

Sawdust is a waste wood generated out of wood workings. It is highly advisable to go for sawdust as carrier for bioagents if it is available easily as it has high waterholding capacity and also got high organic matter (Kolet 2014). Arora et al. (2008) tested various carrier materials, viz., sugarcane bagasse, charcoal, alginate beads, sawdust, and sand, for P. fluorescens and Rhizobium and reported the sawdust as best carrier material as it helped in survivability of PGPRs. In addition to this, Ambardar and Sood (2010) found sawdust as best carrier material for P. fluorescens and B. cereus. Very recently, sawdust was demonstrated to support growth and survival of B. amyloliquefaciens, B. pumilus, and Serratia marcescens up to 9 months (Chakraborty et al. 2013).

4.2.2.3

Peat Formulations

Peat is a fuel comprising of spongy tissues formed through decomposition of organic matter mainly plant tissues in wet conditions (Nakkeeran et al. 2005). The slow decay of sedges, rushes, reeds, and mosses contributes for formation of peat. Peat soils are one of the carrier materials used to formulate PGPR. The specific advantage with peat-based formulations is bacteria remain metabolically active and continue to multiply during storage as long as there is availability of nutrients and moisture and optimum temperature exists (Bashan 1998). The P. fluorescens formulated in peat enhanced the growth of soybean plants under greenhouse conditions compared to P. fluorescens formulated in tapioca flour and coconut water in palm oil. The enhanced growth is attributed to the longer survivability of the bacteria (Habazar et al. 2014). Among the four different formulations, viz., rice bran, bentonite, talc, and peat, tested for multiplication of P. fluorescens, peat was highly effective as it improved the stability and effectiveness (Ardakani et al. 2010). Though peat has been reported to be in use as carrier material in many bioagent formulations, there exists an inherent problem of unavailability, occurrence of

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contamination, and on sterilization the release of toxic substances which kill most of bacteria (Bashan 1998).

4.2.2.4

Fly Ash-Based Formulations

Fly ash otherwise called as crushed fuel ash is a byproduct of coal-burning generated at thermal power stations and is considered as hazardous to environment. Studies have confirmed that this material can be used as carrier material for formulation of PGPRs. In addition to this, application of fly ash-based PGPRs to soil is reported not only to promote crop growth but also improve structure of soil as it harbors many important minerals and is rich in potash (Kumar et al. 1999). Fly ash was recorded to be the best carrier material for species of Bacillus, Azotobacter, and Pseudomonas (Kumar 2014). The added advantage with use of fly ash-based formulation is that it raises the pH of the soil and supports in the availability of nutrients (Dwivedi and Chauhan 2007).

4.2.2.5

Press Mud Formulation

Press mud, also known as olive cake or press cake, is the residual waste after the sugarcane juice is filtered. It is cultivated as a high-quality organic fertilizer by mixing it with the used cleaning liquid of the distillery. Muthukumarasamy et al. (1999) composited the press mud using vermicomposting technique, and it was observed that it enhanced the survival rate of Azospirillum spp. compared to lignite. Bacillus circulans and Bacillus subtillis when formulated in press mud enhanced the germination and vigor index of maize, wheat, jowar, and bajra. Further, it was noticed that the shoot length of wheat increased significantly in this formulation compared with other formulations (Gunjal and Kapadnis 2020).

4.2.2.6

Vermiculite Formulation

Vermiculite is a mineral material similar to mica, available naturally and used for improving soil aeration and moisture-holding capacity. It is also used as carrier material for PGPRs. The formulation of P. fluorescens (PF1)-containing vermiculite supported the viability for 8 months, and viable count after 8 months of storage was 1 × 106 cfu/g (Vidhyasekaran and Muthamilan 1995). Further, the species of Azospirillum formulated in vermiculite could retain its viability up to 10 months (Saleh et al. 2001). Sharma et al. (2011) reported the Pseudomonas sp. formulated in vermiculite could support the growth of tomato under field conditions and also improved the productivity to a greater extent.

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Liquid-Based Formulations

Plant growth-promoting bacteria are formulated in buffers with or without protectants like sugars. There has been extensive research on this aspect of utilizing this formulation for PGPRs. The liquid formulation of Azospirillum brasilense was reported to improve vegetative growth as well as yield in the case of wheat (DiazZorita and Fernandez-Canigia 2009). The liquid formulation of P. fluorescens when delivered as seed treatment + seedling dip + soil drenching in tomato effectively reduced incidence of fusarium wilt (Manikandan et al. 2010). Further, the same formulation when applied in sugarcane could effectively manage the red rot disease (Senthil et al. 2011). Selvaraj et al. (2014) developed the liquid formulation of Pseudomonas and found the improved efficacy against two banana pathogens, viz., Fusarium oxysporum f. sp. cubense and Helicotylenchus multicinctus. The potential advantage of liquid formulation over other formulations is high cell count of bacteria, least or no contaminations, protection from environmental stresses, convenience in handling, increased shelf life as the bacteria go for dormant conditions (Vendan and Thangaraju 2006; Manikandan et al. 2010), and increased efficacy (Hegde 2002; Vendan and Thangaraju 2006). Melin et al. (2011) reported the shorter shelf life of products when stored at higher temperature and actual weight of products as disadvantages of these formulations.

4.2.2.8

Encapsulation-Based Formulations

Immobilization and encapsulation of cells of PGPRs in polymeric gel (alginate) is a popular technology wherein the gel-like matrix helps bacteria to survive for longer duration (Fravel et al. 1985; Park and Chang 2000). The major advantage associated with this formulation is protection of bacteria from environmental hazards as well its prevention of competition between natural microbes present in soil and introduced bacteria by releasing the bacteria gradually to soil, thereby facilitating colonization of host by introduced bacteria (Bashan et al. 2002). The performance of PGPR species Bacillus megaterium when immobilized in alginate as the matrix increased as reported by Cassidy et al. (1996) and Sivakumar et al. (2014). Young et al. (2006) demonstrated the establishment of B. subtilis in soil when it is encapsulated with alginate beads with humic acid. In recent studies by Namasivayam et al. (2014), it is observed that in the case of green gram and black gram, application of encapsulated Rhizobium spp., Azotobacter spp., and Azospirillum spp. improved the seedling emergence.

4.3

Strategies to Improve the Efficacy of Formulations

Rhizosphere is the one of the most precious gifts to mankind as it is the site of innumerable beneficial microbes contributing to the welfare of human life. The

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performance of biocontrol agents may vary from lab to field depending on the host, environments, and other factors. The inconsistency of particular formulation of biocontrol agents is due to many reasons as discussed in the earlier sections. However, there exists a possibility to improve the efficacy of formulations without directly going for genetic manipulation. Thus, the important strategies to improve the efficacy are as below. • Consortia development with multiple strains • Strains of bioagents that are capable to contribute for synergistic expression of biocontrol genes • Use of adjuvants, spreaders, and stickers along with formulations • Altering PGPR strains with genetic engineering approach

4.3.1

Consortia Development with Multiple Strains

The reduction in disease incidence under suppressive soils is due to actions of many microbial agents, and hence, it proves that a mixture of microbial agents having synergistic action will have more impact than the individual microbes (Lemanceau and Alabouvette 1991). Thus, combining two or more strains of biocontrol agents would create situation wherein the mixture of strains will broaden its effectiveness. Two or more strains could be combined and developed for consortia of bioagents by considering the following things (Raupach and Kloepper 1998). • Each of the strains should have different mode of actions against different pathogens. • Strains should work at different range of pH, moisture, temperature, and relative humidity. • Strains with different pattern of colonization of plants. • Of the two strains, one can have growth promotion activity alone, and the other can have inhibitory action. • Strains should not be inhibitory to each other. A large number of studies conducted worldwide at both glasshouse and field have proved that the mixtures of strains of PGPRs are more effective than individual. Domenech et al. (2006) concluded that mixture of PGPR strains could enhance the biological control activity against multiple diseases. In addition to this, mixtures of PGPR could also enhance absorption of water and tolerance to abiotic and biotic stress (Bresson et al. 2013; Sukumar et al. 2013). In a recent study, it was concluded that the mixtures of bioagents, Bacillus velezensis and B. altitudinis, have demonstrated biological control of several plant diseases and plant growth promotion in tomato against soilborne fungal and bacterial pathogens (Ke Liu et al. 2018). Similarly, consortium prepared with Bacillus firmus and Trichoderma harzianum is used for the management of soilborne plant pathogens of oil seed crops,

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horticulture crops, and arid legumes. The consortium can be delivered in vegetable crops through soil application, seed treatment, and root dip of seedlings. This bio-formulated product also increased B. firmus root colonization, giving longterm pathogen protection to the host. Its use as a seed coating, combined with the addition of a tiny amount of compost made from radish waste, increased root colonization. The demonstrations of this consortium as a crucial component of any technology at producers’ fields have yielded good results in terms of disease incidence and yield (Mawar et al. 2018, 2019).

4.3.2

Strains of Bioagents that Are Capable to Contribute for Synergistic Expression of Biocontrol Genes

The efficacy of formulations can also be increased through incorporating strains that are able to induce synergistic expression of genes responsible for biological control activity. The genes responsible for induction of diacetyl phloroglucinol were synergistically induced when the two strains of fluorescent pseudomonads, namely, CHAO and Q287, were combinedly formulated. Further, this combined formulation would improve the DAPG pool in the rhizosphere, and thereby it will suppress the pathogens (Raaijmakers et al. 1999).

4.3.3

Use of Adjuvants, Spreaders, and Stickers Along with Formulations

Adjuvants are the substances added to spray tank separately apart from pesticide to improve the efficacy of pesticide itself or sometimes to improve the physical property of pesticides and thereby improve efficacy. With addition of adjuvants and stickers, performance of formulation of biocontrol agents can be improved. The efficacy is increased by way of protecting microbes from environmental stress, and also they supply nutrients (Connick et al. 1991; Bateman et al. 1993; Barnes and Moore 1997). The carboxy methyl cellulose added in talc formulations of PGPRs helps to coat the PGPRs uniformly on seeds. One must be cautious in using adjuvants as the learned experience suggests sometimes these can reduce the establishment of PGPR on infection court especially under heavy rain and dew. Hence, a complete knowledge of the use of adjuvants is essential to increase the effectiveness of the formulation.

4.3.4

Genetic Engineering of PGPR Strains

The alteration of genetic components of effective bacteria harboring genes that are useful to plants will lead to the overexpression of desired genes, and thereby one can achieve the effective management of pest and disease. Further, this approach will have an added advantage of incorporating multiple traits in single bacteria, thus

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reducing voluminous formulation dumping in soil ecosystem. However, the release of genetically engineered bacteria for commercial usage is in the hands of policymakers, and hence, convincing policymakers about safe usage of these bacteria will definitely be a boon to production system.

4.3.5

Assessing the Shelf Life of Formulation

The success of any biocontrol agents largely depends on its shelf life as well as its availability (Shakih and Sayyed 2015). On the other hand, for most biocontrol agents, the biggest challenge during formulation is stability of the microorganism during various steps (Leggett et al. 2011). The Gram-negative bacteria have shorter shelf life when compared to Gram-positive owing to the structural arrangements they have. Since the Gram - ve bacteria has poor shelf life, formulations are prepared with high cell count so as to maintain the population of bacterial cells for effective management (Tabassum et al. 2017). Development of novel formulations with increased shelf life seems to be a big challenge in bioagent production and usage. In this direction, development of liquid formulations of various potent PGPRs is encouraging as it allows adding minimum nutrients and cell protectant required for survival of bacteria in it (Brar et al. 2012). Cassan and Diaz-Zorita (2016) reported that more than 80% of Azospirillum sp., a PGPR being commercially used in South America, is in liquid formulation and shelf life claimed would be more than 6 months. Hence, for commercialization of any formulation, its viability has to be checked very thoroughly.

5 Standardizing Delivery Systems The efficacy of bioagents is largely depending on the method in which they are delivered to target sites. According to Fravel (1992), an efficient method of delivering biological control agent should involve least amount of product and also least amount of time and labor; thereby the cost incurred is reduced, and at the same time there must not be any compromise in the intended efficacy of product. In order to achieve this, optimum quantity of product in right state of activity, in right time, and to the correct target site must be delivered. The proper time of application and method of placement of inoculum are more important than dumping a large quantity at single time. However, the type of biocontrol agent, characteristics of pathogen, and crop and cropping systems will largely dictate the method of delivery. The most common methods of delivery used are discussed hereunder. • Seed treatment • Biopriming • Encapsulation of seeds or artificial seeds

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Dipping of seedlings Application to soil Foliar application Spraying to fruits Treatment to sucker Treatment to sett Fluid drilling technology or fluid sowing or gel seeding Microbigation Co-aggregation Consortia

• Seed treatment: According to Kommedahl and Windels (1981), the reliable method of application of PGPR in close contact with germinating seeds is seed treatment. It largely helps to deliver PGPRs to spermospheres of plants where the congenial environment exists. Thus, biocontrol agents get ambient opportunity to survive, establish, multiply, and inhibit the growth of soil- and seedborne pathogens (Cook and Baker 1983). However, the major factors to be considered in selecting formulation of biocontrol agents used for seed dressing are density of inoculum present on seed coat after treatment, stability of both in terms of viability and integrity of the bioagents on seed coat, and the cost involved (Fravel 1992). It is predicted that the increasing awareness on hazards of pesticides on environment and involvement of biotechnological methods to improve the potential of microbial products will certainly enhance the seed treatment in due course of time (Chandra et al. 2006). An enormous amount of work has been done round the globe, to introduce the inoculants so close to the target that the introduced bioagent gets an opportunity to establish and colonize plant root at first. It is this selective advantage associated with this method that has fascinated many end users owing to its convincing results in terms of growth promotion and disease suppression. Murphy et al. (2000) conclude that the talc formulation of Bacillus spp. when delivered as seed treatment suppressed disease incidence of ToMoV and also increased the yield. Further, kaolin-based formulation of Pseudomonas fluorescens SP007s suppressed the fungal population in rice when delivered through seed treatment (Prathuangwong et al. 2013). Xiaojia et al. (2019) reported the seed treatment with B. subtilis BY-2 in combination with other Bacillus spp. suppress the Sclerotinia sclerotiorum on oilseed rape. • Biopriming—Seed priming is the method in which seed is immersed in solution having bioinoculants or chemical agents followed by re-drying of seed resulting in initiation of germination except radicle emergence (McDonald 1999). The process of hydrating seeds with any biological compounds is called biopriming (Ashraf and Foolad 2005). In other words, biopriming involves soaking seeds in suspension of bacteria for a known time so as to allow bacteria to get imbibed in seeds (Abuamsha et al. 2011). The immersing of seeds in microbial suspension activates the physiological functions in seeds and also prevents the development of plumule and radicle till the desired temperature and oxygen are available to seed after sowing (Anitha et al. 2013). In the process of biopriming, bacteria will

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have an advantage of being established even before germination in the spermosphere (Taylor and Harman 1990). This approach of delivery is more advantageous over seed treatment as it yields rapid and uniform emergence of seedlings, it imparts bioprimed seeds tolerate adverse conditions, and it reduces the amount of biocontrol agents required compared to seed treatment method (Ramanujam et al. 2010). A large number of case studies have proved the potential of biopriming in protecting from disease as well as the seedling growth promotion as evidenced in tomato, carrot, and sweet corn (Callan et al. 1990, 1991; Harman and Taylor 1988; Legro and Satter 1995; Warren and Bennett 1999; Jensen et al. 2002). Further, biopriming of sunflower seeds with two strains of P. fluorescens (UTPf76 and UTPf86 strains) improved the seed germination and promoted the growth seedling (Moeinzadeh et al. 2010). Similarly, Sharifi (2012) reported the effect of biopriming in safflower seeds using the bioinoculant Pseudomonas spp., and they found the increased plant growth parameters like increased no. of branches, heads/plant, diameter of head, grain no./head, grains/ plant, weight of 1000 grain, grain yield, and oil content. There are many methods and modifications of biopriming stating varying temperature and time of sowing, and hence, it’s an unclear approach that still needs to be investigated and discussed at larger forums with more scientific evidences. • Encapsulation of Seeds or Artificial Seeds This is a simple procedure involving enveloping of seeds in a gelatinous material or polymer or gel matrix having biocontrol agents, pesticides, micronutrients, etc., thereby prolonging longevity of microbial inoculants on seeds (Paau 1988). Lumsden and Lewis (1989) developed a seed encapsulation with formulation of biocontrol fungi using alginate prill to coat seeds. The gel matrix helps seeds to remain viable for longer duration. GEL COATTm is a commercial formulation of seed encapsulation developed by Plant Genetics, and it is patented as delivery system for entamopathogenic nematodes (Boyetchko et al. 1999). Rekha et al. (2007) inoculated Lactuca sativa L. seedlings with B. subtilis CC-pg104 and P. putida CC-FR2-4 encapsulated in alginate with humic acid, and the result clearly implied there was significant improvement in growth of seedlings. The activity of rice seedlings was noticed when the seeds of rice were encapsulated with Bacillus megaterium in alginate with humic acid. Further, the increased cell viability of bacteria was noticed in this case (Sivakumar et al. 2014). The merits of technology include eco-friendly and environmentally safe as the ingredients incorporated in capsule are not released till seed germinates. However, the seed inoculum density, stability of coating agents, viability of microbes and seeds, cost of production, and feasibility of usage are things to be considered. • Seedling Dip The plant pathogens gain entry through roots or seeds or foliages in many crops. Pre-potentiating of rhizosphere environment with colonization of PGPR strains will help in preventing pathogen effects on host. It is with this background concept of seedling dip was brought to aid the disease management especially while dealing with soilborne diseases. Rhizoctonia solani causing sheath blight of

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rice is a soil borne pathogen that gains entry through root. In such cases pre-colonization of rice seedling with PGPR strains will help to manage the disease. Nandakumar et al. (2001) reported that rice seedling dipped in talcbased formulation of P. fluorescens (20 g/L) for 2 h and transplanted reduced the sheath blight disease. Further, reduction of verticillium wilt in strawberry plants was recorded when their roots were dipped in P. putida (2 × 109 cfu/mL) suspension for 15 min (Berg et al. 2001). Yasar et al. (2010) documented the improvement in rooting as well as growth of roots of kiwifruit stem cuttings when treated with PGPRs. Dipping of rice seedlings in dipped in suspension containing talc-based formulation of Pseudomonas fluorescens for 2 h prior to transplanting, the incidence of leaf blight drastically reduced as the PGPR gets pre-colonized in rice seedlings (Jambhulkar and Sharma 2013). The seedling dip method of delivery is more suited to rice and vegetables in which transplanting is generally followed (Singh and Zaidi 2002). • Soil Application Soil application of biocontrol is advisable when they are sensitive to desiccation (Warrior et al. 2002). Soil being rich in organic matter and also other nutrients required for the beneficial microbes will aid in enriching the population of these and thereby suppress the development of pathogenic microbes causing diseases. According to Lumsden et al. (1995), the increase in population of introduced biocontrol agents will create shortage of essential nutrients to pathogenic microbes and other less beneficial microbes and thus cause suppression of diseases. There have been numerous studies on use of PGPRs against soilborne diseases of many crops in recent past, and the studies conclusively suggest their efficacy against these diseases when delivered as soil application. The soil application of Pseudomonas liquid formulation at a concentration of 108 cfu/g before planting of tulip bulbs resulted in reduced incidence of root rot of tulip caused by Pythium ultimum (Weststeijn 1990). The soil application of talc-based formulation of a mixture of P. fluorescens (Pf1 and FP7) @ 2.5 kg/ha + 50 kg of sand after 30 days of transplanting recorded the minimum disease incidence of sheath blight (Nandakumar et al. 2001). Soil application of Trichoderma isolated from arid soils has been proven to be effective against Ganoderma lucidum, Fusarium oxysporum f. sp. Cumini, and Macrophomina phaseolina in several experiments conducted in arid region (Mawar et al. 2020; Lodha and Mawar 2010). These studies revealed that population of T. harzianum increased gradually in compost prepared from residues of Prosopis juliflora, Calotropis, and weeds compared to farmyard manure and non-amended controls. Soil application of P. fluorescens and Bacillus subtilis at 200 g per plant in talc-based formulation along with neem cake 5 kg effectively reduced the leaf blight and anthracnose diseases of noni (Nakkeeran et al. 2010). Combined application of Pseudomonas and Trichoderma strains with neem cake enhanced suppression of root rot disease incidence in Coleus (Daniel Jebaraj et al. 2012). Manjunath et al. (2019) found that soil application of Trichoderma reesei and Pseudomonas sp. @ 125 kg each + neem cake 5 kg to each tree per year recorded the minimum disease incidence of coconut and increased the nut yield. Soil

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drenching with endophytic fluorescent Pseudomonas cell suspension (108/mL) in planting rows (at 200 mL/2 m row) was highly effective in reducing the root rot disease in sunflower (Shumaila et al. 2020). • Foliar Spray Phyllosphere is generally subjected to fluctuations of temperature, relative humidity, wind, rain, dew, and amount of radiation. This phenomenon influences to a greater extent on the survivability and efficacy of most of the bioagents. In addition to this, in many of the crops, the presence of waxy layer at the outermost region makes bioagents deprived of nutrients, thereby reducing viability. However, in the crops where leaves are not covered by waxy coat, the sugars, amino acids, and other nutrients are exuded through stomata, lenticels, and hydathodes. These nutrients and amino acids act as energy source for microbial bioagents in phyllosphere (Andrews 1992). Generally, liquid formulations of PGPRs are more suited for foliar application than any other formulations. Combined application of B. amyloliquifaciens (BS6 and E16) and Pseudomonas (PA-23 and DF41) yielded in reduction of stem rot of canola incited by Sclerotinia sclerotiorum under field conditions (Fernando et al. 2007). Mohammed et al. (2014) reported the application of Pseudomonas fluorescens formulated in water in oil formulation reduced incidence of anthracnose in banana as well as increased the yield. Further, the activity of defense-related enzymes, viz., peroxidase, polyphenol oxidase, phenylalanine ammonia lyase, catalase, and β-1,3-glucanase, was also increased with this treatment. Further, Manjunath and Rabindran (2014) reported the application of Pseudomonas fluorescens at 0.2% along with reduced dosage of azoxystrobin could effectively control both leaf and neck blast in rice. Very recently, Kgatle et al. (2020) reported the efficacy of Bacillus amyloliquefaciens along with fungicide could reduce the incidence of Alternaria leaf blight of sunflower. • Fruit Spray Janisiewicz and Jeffers (1997) reported the application of Pseudomonas syringae at 10 g/L on apple in modified packing line effectively managed the blue and gray mold of apple. For commercial use of beneficial microbes against postharvest diseases of fruits and vegetables, a large number of microbial bioagents have been developed and patented. ASPIRE, Yield Plus, and BIOSAVE-110 are the common products being used to manage postharvest disease in fruits and vegetables across the globe (Sharma et al. 2009). Research on exploration of beneficial microbes for the management of postharvest diseases needs to be emphasized to bring many more products in this line. • Sucker Treatment Soilborne diseases occurring in vegetatively propagated crops like banana can also be efficiently managed with biological control agents. Dipping of banana suckers in 500 g of P. fluorescens suspension in 50 L water after pairing and prolinage for 10 min which was later followed by capsule application, i.e., 50 mg per capsule at third and fifth month after planting, reduced the Panama wilt disease (Raguchander et al. 2000). Pushpavathi et al. (2018) found that application of T. viride and P. fluorescens @ 20 g/L for 30 min as a sucker treatment in

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banana effectively minimized the incidence of fusarium wilt disease and improved the yield. • Sett Treatment The fungal pathogen Colletotrichum falcatum causing red rot of sugarcane is one of the major threats in production of sugarcane inflicting yield losses of 10–50% depending on cultivars, environment, and strains (Ghazanfar and Kamran 2016). The disease is widespread occurring in almost 68 countries growing sugarcane (Bharti et al. 2012). Most of the commercial cultivars being cultivated are susceptible to this disease, and due to this there have been many epidemics in most of the growing countries including India (Singh 2008; Babu et al. 2009; Babu 2010). One main reason for flaring up of disease would be use of infected sets for sowing. Management of the disease involves integrated approaches encompassing cultural, biological, and chemical methods. Of the three, biological method of management using PGPR seems to be eco-friendly and safe as the product is directly consumed as raw juice. Viswanathan and Samiyappan (2002) reported that soaking of two budded sugarcane setts with formulation of P. fluorescens at 20 g/L for 1 h duration and later incubation for 18 h before sowing would reduce incidence of sett rot significantly. The reduction in the disease would be due to establishment of PGPR isolates in sett and induction of various defense mechanisms in it. In addition to this, the sett treated plants could improve the growth and sugar recovery. Hassan et al. (2010, 2012) reported the use of Bacillus strains against red rot disease under both glass house and field conditions. • Fluid Drilling Technology or Fluid Sowing or Gel Seeding Fluid drilling is a system of delivery of bioagents that has not been explored to a greater extent. It comprises sowing of germinated seeds and suspending them in a gel before transferring them to the seedbed. The biocontrol agents can be incorporated into fluid drill gel, and the gel is used to protect the radicles during sowing and early growth. Conway (1986) concluded the application of fungicides in combination with gel matrix, an adjuvant, reduced the incidence of dampingoff caused by R. solani in chili peppers. Fisher et al. (1983) proposed that the fluid drilling is one of the ideal systems of delivering bioagents for management of soilborne pathogens. Despite its popularity as sowing method, this technology has not gained much importance as delivery system of PGPRs owing to many inherent disadvantages, viz., the gels tend to attract several microbes, including the soilborne pathogens that might result in an augmented disease incidence and early emergence of seedlings which may attract the hungry insects to a greater extent. However, the technology has got an added advantage as per the sowing method is concerned. The most important advantage associated with fluid drill is it establishes better stand of crop, gives more uniform growth and uniform crop maturity, and helps in harvest. More research on exploration of this method of delivery needs to be carried out to make it a viable and feasible method of delivery of PGPRs.

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• Microbigation The use of beneficial microbes for the suppression of pathogens and insects which are soilborne and also for weeds is referred to as microbigation (Boari et al. 2008). Since it delivers the biocontrol agents at desired site so close to the target organism, the efficacy of bioagents will be very high in this method. Boari et al. (2013) delivered conidial suspensions of T. harzianum and Paecilomyces lilacinus, Fusarium oxysporum, and F. solani in greenhouse using commonly used dripper lines, drippers, and filters. They could conclude that conidial suspension can pass through drippers without blocking regardless of their size and remain viable. Many researchers opined that this method can be used for application of bioagents, mycoherbicides, and biopesticides (Copping 1999; Whipps and Lumsden 2001; Charudattan 2001). However, this technology has also not explored much for PGPR delivery, and detailed research has to be carried out to come up with formulation of PGPR suited for delivering through this method. However, the technology has specific advantage of reduction in cost of delivering PGPRs in two ways; one is it requires less quantity of bioagents as the distribution is done only to root zone and not entire field, and the second is it will not require any additional man power to do spraying. Thus the technology will be effective if standardized. • Co-aggregation It is a process of in which two genetically distinct bacteria get attached to each other via specific molecules. The adhesion is owing to biofilm formation of bacteria. The co-aggregation is very specific, and only few or some species of microbes are consortial partners. This phenomenon was first described by Gibbons and Nygard (1970) in human dental plaque. This mechanism is only effective when there are an equal number of partners and their genetics are stable. The genetic stability of co-aggregation is mediated components of the surface that are potential in recognizing the carbohydrate on the partner cell surface (Kolenbrander and Phucus 1984). Development of formulation by co-aggregating Azorhizobium with other PGPR would impart broad spectrum of action against various diseases (Sivakumar and Joe, 2008). This clearly suggests the existence of wide scope for exploring this approach for delivering PGPRs through these methods.

6 Consortia Application The integrated disease management involves use of biological control approach as one of the components in it. However, the success of biological control largely depends on the efficacy of strains under field conditions. The inconsistent performance of PGPR strains under field conditions owing to their inability to survive or inefficiency in producing antimicrobial compounds against target pathogen or many more reasons have been reviewed by many researchers (Shtienberg and Elad 1997).

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In order to address this, a consortium of bacteria which are compatible and effective against wide range of pathogens will definitely enhance the performance, and also time and cost incurred in delivery can be saved greatly. The performance of individual biocontrol agent has been found to increase in consortia (Meyer and Roberts 2002; Roberts et al. 2005). The compatibility is one important factor in consortia development as the incompatibility among the strains hampers the efficacy of consortia under field conditions. Compatibility among the strains of PGPR was demonstrated in many case studies by earlier workers (Manjunath et al. 2010; Nakkeeran et al. 2010; Mawar et al. 2018). Sundaramoorthy and Balabaskar (2012) reported the consortia developed out of B. subtilis (EPCO 16 and EPC 5) and P. fluorescens (Pf1, Py15 and Fp7) could effectively manage the leaf blight in tomato. The consortium developed from three PGPR strains, viz., Bacillus cereus AR156, Bacillus subtilis SM21, and Serratia sp. XY21, could significantly reduce the prevalence of phytophthora blight and improve fruit quality in sweet pepper (Zhang et al. 2019).

7 Toxicological Data Generation Assessing the safety of newly developed formulation of PGPR or the biocontrol agents as such is a step in commercialization. Though the PGPRs live in nature and coexist with millions of microbes in soil or rhizoplane, when the formulation is developed, its implication on soil and plant as well as nontarget organisms must be assessed thoroughly as per the international standards. This assessment is done in accordance with the standard protocol, and the process of assessing is called as toxicological data generation, and the data generated is considered as toxicological data. The cost incurred in generation of these data is very high, and hence, the industrial linkages must be established so as to bear the cost. Further, if there is mixture of strains, then toxicological data for both strains have to be generated separately (Jeyarajan and Nakkeeran 2000; Doraisamy et al. 2001).

8 Registration of Biopesticide in India India is the fourth largest manufacturer of pesticides in the world after China, the USA, and Japan. Biopesticide contributes a significant portion of pesticide market in India. The main driver for increase in biopesticide demands in the country is organic farming coupled with government emphasis on usage of biofertilizers. FAO statistics suggest that the country has got 1.9 million ha of cultivated land under organic farming in 2018 with 0.65 million growers (https://www.mordorintelligence.com/ industry-reports/indian-biopesticides-market). The annual growth of biopesticide production in India is expected to increase by 2.5%, and more than 970 companies

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registered for production (https://india.mongabay.com/2019/07/what-is-preventingthe-widespread-adoption-of-biopesticides-in-india). Hence, there is a great scope for biopesticide in the country. In India, biocontrol agents are covered under Insecticide Act (1968). Under this act, any microorganism produced or sold for management of disease must be registered with Central Insecticides Board (CIB), Ministry of Agriculture, Govt. of India. The Central Insecticide Board and Registration Committee (CIB&RC) are the two high-level bodies involved in registration of biopesticides. CIB is the apex body comprised of experts from diverse field, and they issue guidelines for registration and data requirements for registration in amenability with OECD guidelines. In addition to this, it also sets minimum infrastructural facilities for production of biopesticides. The CIB has a committee called registration committee having chairman and five board members including Drugs Controller, India, and the Plant Protection Advisor to the Government of India. This committee is responsible for registering biopesticide after the scrutiny and verification of the claims made by applicant with respect to bioefficacy and safety to human and animals (Rabindra 2005). Any company or manufacturer of biopesticide can register their product under Section 9(3b) (temporary registration) and 9(3) (regular registration) of the Insecticide Act, 1968. This system permits commercial manufacturers of these generally safe microbial pesticides to obtain pre-registration and open the market while the product is undergoing full registration; this also reduces market barriers to the developed products. The data prerequisite for registration under 9(3) B is little flexible than for 9(3) (Guidelines for Registration 2011). The CIB&RC has developed a system for the online registration called the Computerized Registration of Pesticides (CROP). The detailed data required for registration is furnished in http:// ppqs.gov.in/divisions/cib-rc/guidelines?page=1.

9 Establishment of Public-Private Partnership All the steps in commercialization for PGPR formulation development right from isolation to registration are time-consuming, are laborious, and require investment of huge money. When there is collaboration between organizations doing research and industries which are interested to take this product for marketing, the development will be easy and sustainable. In this direction many universities emphasize on the concept of public-private partnership for translation of research for the benefit of farming community. Thus linkage with industries will favour commercialization of the technology.

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Quality Control

The general blame inherently associated with most of biocontrol agents is inconsistency in performance and lack of reliability. Therefore, having vigilant eye on quality of bioagents produced, supplied, and used is of paramount importance in commercialization of any formulation of PGPR. The quality control aims in ensuring the following: • Raw materials used for production are in accordance with specifications declared by manufacturers. • The reliability between development process and products. • Products that are used at the end meet the criterion set by registration authorities. • The performance of products matches the perception of user, and thereby it results in repeated purchases. The quality control can be divided into three sections: production control, process control, and product control. The production control and process control are internal in nature, and they can be managed with ensuring stable process of production and without any failures. The product control is external, and it refers to the quality of final product before its end usage and thereby the kind of satisfaction it gives to user. Hence, quality control encompasses all aspects of quality right from procuring raw material to end use of biocontrol agents (Table 13.2).

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Bottlenecks in Commercialization of PGPRs

As per the estimation of Chandler et al. (2011), nearly 67,000 pest species encompassing the phytopathogens, weeds, vertebrate, and invertebrates tolling yield losses of 40% across the globe. In order to manage these pests, a massive number of chemicals and bioagents are being used in production system. The hazardous nature associated with the usage of chemical pesticides, aided to switch over to biological approaches. In this direction, use of PGPR sounds to be an alternate substitute for chemicals (Droby et al. 2009). However, the availability of registered biopesticides is very less when compared to chemical pesticides in the market. This is partly due to constraint in commercialization of PGPR strains.

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Farmer’s Psychology Towards PGPR

The chemical pesticides have ruled the agriculture sector for the past 60–70 years leaving rich knowledge and experience regarding their effectiveness and method of usage and availability to the farmers. Further, farmers realize the effect of chemical

Hydrolytic enzymes (amylases, proteases, lipases, and cellulases) Fengycin Phenazine, pyrrolnitrin, and DAPG

Streptomyces sp.

Bacillus subtilis 9407 Pseudomonas putida, P. fluorescens, P. aeruginosa

Pyricularia oryzae (blast)

Fusarium graminearum (head blight)

Alternaria alternata, Phytophthora sp., Fusarium solani, F. oxysporum Sclerotium rolfsii (collar rot)

F. oxysporum, R. solanacearum (Wilt)

Fusarium oxysporum f. sp. capsici (wilt)

Phytophthora capsici (damping-off, root rot, leaf blight) Phytophthora capsici, Sclerotium rolfsii

Botryosphaeria dothidea

Dematophora necatrix, Fusarium oxysporum, Phytophthora cactorum, and Pythium ultimum

Rice

Wheat

Wheat

Chickpea

Eggplant

Chili

Bell pepper

Apple

Apple

Black pepper

Bacillus mojavensis RRC101

Fusarium verticillioides

Maize

S. plicatus isolate B4-7

Streptomyces sp. NSP (1–6)

Bacillus amyloliquefaciens S20

Streptomyces sp.

Pseudomonas chlororaphis MCC2693

Bacillus velezensis RC 218

Streptomyces UPMRS4

Fengycin

Bacillus subtilis NCD-2

Antibiotic (borrelidin)

Chitinase

Iturins A

PCA, HCN, ammonia, and siderophores Host defense enzymes

Fengycin, iturin, and ericin

Chitinase, glucanase, and PR1

VOCs

Mode of action

Biological control agents

Crop Phytopathogens Fungal diseases Cotton Rhizoctonia solani (damping-off)

Table 13.2 Examples of PGPR usage plant disease management

Fan et al. (2017) Sharma et al. (2017b)

Guo et al. (2014) Rath et al. (2018) Awla et al. (2017) Palazzini et al. (2016) Jain and Pandey (2016) Singh and Gaur (2017) Chen et al. (2014) Saengnak et al. (2013) Chen et al. (2016) Thampi and Bhai (2017)

References

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Paenibacillus polymyxa Sx3

Rice

Bacillus pumilus T4 Bacillus cereus (I-35), Stenotrophomonas sp. (II-10)

Bean Common Mosaic Virus (BCMV)

TMV virus, Chili veinal mottle virus (ChiVMV)

Vigna unguiculata Chili

Seed treatment and soil drench

Seed spraying

Foliar spraying

Tomato spotted wilt virus (TSWV)

Tomato

B. amyloliquefaciens MBI600

Tobacco streak virus (TSV)

Soil drench/foliar spray

Soil drench

Phenylalanine ammonia-lyase, peroxidase, and polyphenol oxidase -

Antibiotics, ionophores, hydrolytic enzymes, and enzyme inhibitors HCN and siderophore

Siderophore

Antibiotics

Type I polyketide synthase, nonribosomal peptide synthetase

Bacillus spp.

P. fluorescens CHAO + chitin

Xanthomonas oryzae pv. oryzae

Xanthomonas oryzae pv. oryzae

Cotton

Viral diseases Banana Banana bunchy top virus (BBTV)

Bacillus subtilis GBO3, Bacillus pumilus SE34

Rice

Ralstonia solanacearum

Erwinia carotovora subsp. carotovora (Ecc1 and Ecc2)

Bacillus subtilis, Pseudomonas fluorescence, P. aeruginosa, and Streptomyces spp. Bacillus sp.

Potato

Tomato

Ralstonia solanacearum

Arthrobacter sp.

Ginger

Streptomyces sp. CB-75

Xanthomonas citri subsp. citri

Colletotrichum musae, C. gloeosporioides

Bacterial diseases Citrus Endophytic Bacillus thuringiensis

Banana

PGPM: Fundamental, Bioformulation, Commercialization, and Success. . . (continued)

Kavino et al. (2008) Vinodkumar et al. (2018) Beries et al. (2018) Shankar et al. (2009) Damayanti and Katerina (2008)

Abdalla et al. (2017)

Islam et al. (2019) Zhang et al. (2018) Salem and El-Shafea (2018) Ramadasappa et al. (2012) Chithrashree et al. (2011)

Chen et al. (2018)

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Sunflower necrosis virus (SNV)

Papaya ringspot virus (PRSV-W)/Tomato chlorotic spot virus (TCSV) Potato virus Y

Sunflower

Papaya

Potato

Phytopathogens Cucumber mosaic virus (CMV)

Crop Cucumber

Table 13.2 (continued) Biological control agents Serattia marcescens 90-166 + P. putida 89B-61/B. pumilus SE34 Bacillus licheniformis MML2501 + Bacillus sp. MML2551 + P. aeruginosa MML2212 + Streptomyces fradiae MML1042 B. amyloliquefaciens IN937a + B. pumilus SE34 + B. pumilus T4 Streptomyces netropsis DSM 40093 (SCF7), S. ambofaciens (SCF11), and S. actuosus (SCF20) Foliar application

Seed treatment

Seed treatment

Mode of action Seed spraying

Abdalla et al. (2017) Nasr-Eldin et al. (2019)

References Murphy et al. (2003) Srinivasan and Mathivanan (2009)

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pesticides so quickly and hence get convinced easily. The other benefit associated with this is in lower dosage the effectiveness can be realized. On the other hand, the usage of biopesticides is comparatively new, and farmer does not have exposure and experience in using it (Pannell 2003; Moser et al. 2008). The inconsistency in performance of biopesticides has made farmers apprehensive towards their usage, and also the huge cost of biopesticides particularly limits the usage by early adopters (Cowan 1991; Cowan and Gunby 1996). In addition to this, huge cost involved in production of many high-valued crops forces many farmers to go for chemicals owing to risk associated with their produce turning to unmarketable or lower yields. This risk particularly prevents farmers in using the biopesticides to a greater extent.

12.1

Specificity of PGPR Strains

The PGPRs may either act as growth promoter or suppress the growth of pathogen through direct or indirect effect or both. Sometimes the PGPR may act as both growth promoter and inhibitor of pathogen. In either case, it is beneficial to use in crop production. PGPRs may exhibit the broad spectrum of action against wide range of pathogens or may show very narrow spectrum of action exhibiting specificity against pathogen. Further, the specificity may vary according to crop and locations. For instance, a PGPR strain isolated from cotton may not work well for rice owing to different growth conditions of crops, and also strains from one location may not perform well in another location. This specificity of PGPR strains has created problem for industries especially by demanding introduction of crop-specific and location-specific PGPRs which sounds practically a difficult task. This is the root cause for hindrance in commercialization of many PGPR strains.

12.2

Microbial Preference for Formulation

PGPRs encompassing both Gram-negative and Gram-positive bacteria are highly effective against extensive range of pathogens as reported by many authors (Manjunath et al. 2010; Nakkeeran et al. 2010). The formulations of bacteria belonging to both groups are available across the world. Despite the formulation development, the viability of Gram-positive bacteria is more compared to Gramnegative bacteria owing to the formation of endospores (Perez-Garcia et al. 2011; Kamilova et al. 2015). Though it is tough to maintain the Gram-negatives, they are preferred over Gram-positive bacteria owing to their persistence in vivo (Tabassum et al. 2017). The problem of the viability of Gram-negative bacteria in formulations can be overcome by maintaining high inoculum level for a sufficient time. Most PGPR formulations comprise single strains, and the performance of these may not be acceptable in field conditions. However, the efficacy of formulation containing

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mixture of strains can be improved by selecting the strains having ability to have more symbiotic relationship with plants since one strain may help in the disease control, while the other strain is involved in plant growth promotion.

12.3

Handling and Reinoculation of PGPR

Since bioformulations are living entities, distinct attentions are needed at all stages right from selection to usage. The inoculums have to be identified, produced, stored, distributed and used under field conditions. At all these stages, a knowledge on biocontrol agents is required so as to maintain optimum conditions in all cases. Further, in order to maintain minimum load, it must have ability to propagate and reproduce in the carrier material. The carrier material should support the growth of PGPRs in formulation and also must help in colonization after field application. Many times, reinoculation of bacteria may be required to enrich the environment with proper PGPR load. This is so because the introduced PGPR may not survive in soil forever as it has to compete with naturally available local microbes for want of niche and basic requirements. Thus, minimum awareness on handling of PGPRs and reinoculation makes the PGPR commercialization difficult.

12.4

Inconsistency in Performance of PGPR Under Field Conditions

The strain of PGPR identified as effective under laboratory against particular pathogen may not inhibit effectively the same pathogen under field conditions or even completely fail in doing so. The lack of correlation among the laboratory and field efficacy is attributed largely to selection criterion adopted by researcher for the particular strains. Many times, biased selection would completely eliminate the formulation from market. Thus, due care has to be taken in adopting robust selection criterion, and repeated experiments have to be completed before identifying a candidate strain as potent against particular disease. The other factor attributed to inconsistency of PGPRs would be the diversified environmental conditions of the crop including rainfall, temperature, and soil type and survival ability of PGPR (Schroth and Becker 1990). The biggest difficulty lies in predicting how a strain will react to different environmental conditions under field. The only option left over to address this issue is testing the strains at multiple locations having wide range of climatic variations. Thus, inconsistency of PGPRs formulation will fail to earn the trust of farmers, and thereby it becomes an important bottleneck in commercialization.

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12.5

289

Regulatory Issues

A careful perusal of literature dictates the efficacy of innumerable number of PGPRs against diverse plant pathogens. However, only a finger-countable number of PGPRs have been formulated and commercialized. The one potential reason for this would be regulatory issues associated with PGPRs. Each and every country is having different testing policies for risk assessment and efficacy to prevent introduction of deleterious biological organisms. Furthermore, development of viable, economic, and appropriate delivery system for PGPRs is another impediment in commercialization (Ravensberg 2011; Glare et al. 2012). The registration procedures for new PGPRs are very time-consuming and expensive and require huge data on toxicology and bioefficacy. Thus, many potent bioagents may not be reflected as formulations and commercialized. In order to address this, the existing registration procedures have to be simplified.

12.6

Absence of Multidisciplinary Approach

The commercialization of biopesticides involves multiple steps right from isolation of antagonistic organism till registration and end usage. It requires research in areas of isolation and identification screening of antagonists, formulation development, standardization of delivery systems and evaluation of product at multiple locations, and advertisements and marketing. Thus, it must involve integrated and concentrated efforts of scientists across discipline, and in reality, it is not happening, and thus most of the biopesticide research is confined to only exploration, collection, isolation, and identification.

13

Conclusion and Future Prospects

The aftermath of green revolution has taught great lessons to both farming community and scientist. Under the banner of green revolution, the indiscriminate usage of chemicals has worsened the situation making million hectare of land barren across the country. It is high time to search for eco-friendly and safe methods of pest management. Utilization of naturally occurring rhizosphere microbial treasure for this purpose is an option of the time. It has been proved beyond doubt that these PGPRs have significant contribution both in terms of growth promotion and pest and disease management. Despite the fact that PGPRs are proved to have efficacy against diseases, their usage in disease management is very meager. The problem associated with this could be many bioagents identified as potent at laboratory or in the field trial remain as academic interest and do not turn to commercial product. The lack of commercialization of products is due to involvement of huge cost, stringent

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registration protocols, and lack of involvement of multidisciplinary approach of research. However, all the way forwards remained would be simplifying registration protocols of PGPRs and establishing the industrial linkage with scientific community so as to bear huge cost of registration of potent PGPRs. Further, the extending government subsidies to boost up the usage of PGPRs in crop production will largely help in making this technology more viable.

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Chapter 14

PGPR: A Sustainable Agricultural Mitigator for Stressed Agro-Environments Priyanka Patel, R Z Sayyed, and Hardik Patel

1 Introduction A potential research interest has been seen about plant growth-promoting rhizobacteria (PGPR), due to their ability to enhance plant growth, via certain direct and indirect mechanisms. Since last few years, research has constantly demonstrated a beneficial association among plants and microbes; the best example is legume rhizobia symbiosis. The plant rhizosphere is enriched with nutrients which are excreted from roots that support the microbial population and surrounding bulk soil. The Free-living beneficial bacteria that reside in the rhizosphere that exert significantly beneficial activities are known as plant growth-promoting rhizobacteria (PGPR). Root exudates are an integral part of rhizosphere signalling events and regulate communication in beneficial plant-microbe interactions. The addition of PGPR for plant growth results in increases a rate of germination, root growth, leaf area, chlorophyll content, hydraulic activity, quality and quantity of yield and tolerance to various biotic and abiotic stresses. Plant growth in agricultural soils is influenced by many biotic and abiotic factors (Mishra 2018). Abiotic stresses such as drought stress, salinity stress, heavy metal stress, flooding stress, cold stress and heat stress are the major limiting factors for plant growth and productivity (Shrivas and Saxena 2016; Etesami and Maheshwari 2018). PGPR may cause biochemical, morphological, physiological and molecular changes in the growth of plants under environmental stresses (Table 14.1). The

P. Patel (*) Department of Microbiology and Biotechnology, University School of Sciences, Gujarat University, Ahmedabad, India R. Z. Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India H. Patel Government Dental College and Hospital, Civil Hospital Campus, Ahmedabad, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_14

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Table 14.1 PGPR significantly induced changes in plant morphological, physiological and molecular traits under various environmental stresses (Goswami and Deka 2020)

PGPR Pseudomonas putida H-2-3

Paenibacillus polymyxa

Pseudomonas fluorescens DR11, Enterobacter hormaechei DR16, Pseudomonas migulae DR35 Bacillus amyloliquefaciens HYD-B17, Bacillus licheniformis HYTAPB18, Paenibacillus favisporus BKB30, Bacillus subtilis RMPB44

Plant Soybean (Glycine max L.) Oilseed rape

Foxtail millet (Setaria italica) Maize

Pseudomonas aeruginosa GGRJ21

Mung bean (Vigna radiate (L.) R. Wilczek)

Pseudomonas putida GAP-P45

Sunflower (Helianthus sp.)

Changes in plant morphological, physiological or molecular attributes Increased gibberellin production Expression of droughtresponsive gene (ERD15) and ABA-responsive gene in Arabidopsis plants Enhanced seed germination and seedling growth

Increased plant biomass, relative water content, leaf water potential, root-adhering soil and root tissue ratio, proline, sugars and free amino acid levels, antioxidant enzyme activity such as ascorbate peroxidase, catalase and glutathione peroxidase, whereas decreased leaf water and electrolyte loss Increased root length, shoot length, dry weight and relative water content along with stronger upregulation of three drought stress-responsive genes such as dehydrationresponsive element binding protein (DREB2A), catalase (CAT1) and dehydrin (DHN) Significantly increased plant survival, plant biomass, rootadhering soil and root tissue ratio of sunflower seedlings as well as increased stable soil aggregates

References Kang et al. (2014) Timmusk and Wagner (1999) Niu et al. (2017)

Vardharajula et al. (2011)

Sarma and Saikia (2014)

Sandhya et al. (2009)

rhizospheric soil is richer in nutrients as compared to the bulk soil because of the secretion of various plant exudates, such as amino acids and sugars. This is due to various chemicals secreted from microorganisms and plant’s roots such as amino acids, organic acids, flavanols, glucosinolates, indole compounds, fatty acids, polysaccharides and proteins in the rhizosphere that acts as signals for plant growth promotion (Vurukonda et al. 2016a). The activity of PGPR bioinoculants helps in enhancing the level of certain extracellular soil enzymes that simplifies the

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decomposition of soil organic matter and confirms the bioavailability of nutrients in the soil (Jabborova et al. 2020). Rhizobacteria accomplish an important role in the surface colonization of soil colloids and roots of the plant and enable proliferation in desired niche, as well as enhancing soil fertility (Ansari and Ahmad 2019). The number of rhizobacteria in rhizospheric soil is generally 10–100 times higher than that of the bulk soil (Mishra 2018). PGPR of genera Bacillus sp. and Pseudomonas sp. have been identified as the most predominant in rhizospheric soil and beneficial to plant against various abiotic stresses (Mishra 2018; Podile and Kishore 2006). Certain abiotic and biotic factors affect plant productivity globally (Patel et al. 2016). The PGPR have certain direct mechanisms such as phosphate solubilization, nitrogen fixation, IAA synthesis, etc. as well as certain indirect mechanisms antioxidant defence, volatile organic compounds, exopolysaccharide, osmotic balance, etc. for improving plant growth promotion and enhancing tolerance against various environmental stresses (Ilangumaran and Smith 2017). PGPR can directly help the proliferation of plant host system by the stimulatory phytohormone production within the root zone; these hormones stimulate the density and length of root hairs. The increase in surface area of root improves the plant uptake potential of water and mineral nutrients from soil. The auxin, indole-3-acetic acid (IAA), is a very important phytohormone produced by PGPR, and treatment with auxinproducing rhizobacteria has shown the enhanced plant growth promotion (Mishra et al. 2012; Patten and Glick 2002). These potent soil bacteria, although very abundant in the rhizosphere, are mostly under-exploited as bioinoculants for improvement of crop production (Ojuederie et al. 2019). The stress-tolerant PGPR have certain PGP properties such as production of 1-amino cyclopropane-1-carboxylate (ACC) deaminase, indole-3-acetic acid (IAA) production, ascorbic acid (ABA) synthesis, nitrogen fixation, phosphorus and potassium solubilization, antibiotic production, induction of plant antioxidant enzyme production, exopolysaccharide production, induced systematic resistance, reducing stress ethylene production, modifications in phytohormonal content, siderophore production and water uptake efficiency which result in defending various plants against stress conditions and consequently enhancing crop sustainability (Fig. 14.1) (Kumar et al. 2019; Patel et al. 2019; Etesami and Maheshwari 2018).

2 The Effects of Abiotic Stress on Agriculture Most cultivated soils in the world are considered as being suboptimal. If the stress persists too long or is too severe, it can enduringly damage plant physiology or result in plant death (Kosova et al. 2011). Abiotic stresses triggered by non-living factors are thought to be the main reason of global crop loss with reduced productivity of more than 50% annually (Atkinson and Urwin 2012). Drought and salinity stress are potent environmental threats for agriculture, particularly in arid and semi-arid regions which are already approaching the limits of crop productivity, and due to global warming and degradation of agricultural soils, these regions may no longer

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Fig. 14.1 Mechanism of action used by PGPR against abiotic stresses in plants (Etesami and Maheshwari 2018; Shahzad et al. 2014)

support crop plants in the future (Kompas et al. 2018; Tuteja 2007). Food security is positively correlated with social and economic constancy. Climate change is causally related to human activities by the production of greenhouse gases such as carbon dioxide. Soil degradation is one of the main concerns impacting agricultural productivity, particularly in tropical and subtropical areas (Lamb et al. 2005). Inappropriate agricultural procedures, together with unnecessary plant residue removal and unbalanced use of chemical fertilizers, reduce soil quality (Schillaci et al. 2019).

3 Abiotic Stress Tolerance and Plant Growth by PGPR under Environmental Stress Condition Improving stress tolerance in plants via conventional breeding is a very long and cost-intensive process, while genetic engineering is linked with moral and social acceptance issues. The role of beneficial microbes is gaining attention in stress management and the expansion of climate change-enduring agriculture (Backer et al. 2018). Stress responses were absolutely modulated by the microbes which results in differential expression of genes involved in biosynthesis of ethylene, salicylic acid, jasmonate, superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and glutathione s-transferase (GST) antioxidant enzymes, DREB1A (dehydration-responsive element binding), NAC1 (transcription factors expressed under abiotic stress), LEA and DHN (dehydrins) (Tiwari et al. 2016). Pseudomonas putida MTCC5279 ameliorated drought stress in Cicer arietinum plants by modulating membrane integrity, proline and glycine betaine osmolyte

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Fig. 14.2 Role of PGPR in alleviating various abiotic stresses (Goswami and Deka 2020)

accumulation and reactive oxidative species (ROS) scavenging ability. The thuricin17 which is produced by Bacillus thuringiensis NEB17 is applied to Glycine max under water-deficit conditions which resulted in alteration of root structures, increased root, nodule biomass, root length and total nitrogen content (Prudent et al. 2015). Beneficial microbes also help plants survive against flooding stress. ACC deaminase-producing strain of Pseudomonas fluorescens REN1 applied on Oryza sativa seedlings could increase root elongation under flooding stress (Etesami et al. 2014; Backer et al. 2018). A gibberellin-producing PGPR strain Serratia nematodiphila increases Capsicum annum growth under low-temperature stress conditions (Kang et al. 2015). Inoculation with Burkholderia phytofirmans PsJN controlled carbohydrate metabolism to reduce chilling damage to Vitis vinifera plantlets when exposed to low-temperature stress (Fernandez et al. 2012). Inoculation of Solanum lycopersicum plants with Pseudomonas vancouverensis OB155 and P. frederiksbergensis OS261 when exposed to low temperature increased expression of cold acclimation genes and antioxidant activity in leaf tissues (Backer et al. 2018; Subramanian et al. 2015). The role of PGPR in alleviating various abiotic stresses is shown in Fig. 14.2.

4 Role of PGPR in Alleviating Drought Stress Plant growth-promoting rhizobacteria (PGPR) are a significant gathering of beneficial, root-colonizing bacteria blooming in the plant rhizosphere and bulk soil (Basu et al. 2021). Certain mechanisms of drought resistance in plants have been induced

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by PGPR, through evocation of the rhizobacteria-induced drought endurance and resilience (RIDER) process that involves various physiological and biochemical changes. It includes changes in phytohormonal content (Khalid et al. 2006) and antioxidant defence (Kaushal and Wani 2015). PGPR also produce various osmolytes and bacterial exopolysaccharides to approve survival of plants under drought-stressed conditions (Table 14.2) (Vanderlinde et al. 2010). Production of heat-shock proteins (HSPs) (Berjak 2006), dehydrins (Timmusk and Wagner 1999) and volatile organic compounds (VOCs) (Ryu 2004) has been reported to impart drought tolerance to plants. The role of microbes in plant growth, nutrient management and biocontrol activity is very well recognized. These beneficial microbes colonize the rhizosphere of plants and promote plant growth by various direct and indirect mechanisms (Table 14.3) (Enebe and Babalola 2018; Grover et al. 2011). The possible explanation for the mechanism of plant drought tolerance induced by rhizobacteria includes improved physiological processes, improved biological processes and improved root architecture and modifications of plant growth substances (Vurukonda et al. 2016a). Table 14.2 Effect of drought stress on plant growth (Ojuederie et al. 2019) Plant Barley (Hordeum vulgare L.)

Chickpea (Cicer arietinum L.)

Cowpea (Vigna unguiculata L.Walp.)

Faba bean (Vicia faba L.) Maize (Zea mays L.)

Wheat (Triticum aestivum L.)

Plant growth and yield The number and weight of grains per plant were reduced, which consequently affected the yield. The grain filling period was utmost affected by drought stress Reduction of total chlorophyll contents at the vegetative and flowering stages under drought stress, whereas proline accumulation increased in both stages under water stress At vegetative and flowering stages is increased the number of days to blossoming by 4 and 7 days, respectively, under drought stress. A flowering phase significantly reduced shoot dry weight in cowpea Content of proline, soluble sugars and protein in the leaves of Faba bean was increased. Grain yield was reduced under water stress Drought decreased the relative water content of leaves to 62.7% and 49.8% after 3- and 6-day treatment which pointedly shortened the leaves. Wilting and rolling of leaves were observed with a reduction in the photosynthetic rate and efficiency of the PSII electron transport in the seedlings under drought stress The photosynthetic rate and stomatal conductance under severe and moderate water stress were reduced due to low CO2 availability. Total soluble sugars and proline content increased, whereas leaf water potential, osmotic potential, turgor osmotic potential and relative water content declined

References Samarah (2005)

Mafakheri et al. (2010)

Ndiso et al. (2016)

Abid et al. (2017) Zhang et al. (2018)

Abid et al. (2018)

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Table 14.3 Role of PGPR in the induction of drought stress tolerance by plants (Enebe and Babalola 2018) Plant species Tomato

Chickpea

Microbes Rhizophagus irregularis, Variovorax paradoxus 5C-2 Pseudomonas putida MTCC5279 (RA)

Maize

Pseudomonas putida (FBKV2)

Common bean Wheat

Rhizobium

Jatropha curcas

Azospirillum brasilense Sp245 Enterobacter cloacae, Enterobacter cancerogenus

Microbial enhanced plant productivity Photosynthetic rate enhancement, lipid oxidation reduction, root water conductivity increases and oxidative phosphorylation in the plant The expression of stress response gene is reduced, maintenance of water content, osmolyte and rate of seed germination Stimulate root and shoot growth, dried plant biomass weight and reduced stomatal conductance Plant weight, nutrient content and Phaseolus vulgaris yield increased Increased growth and expansion of xylem for easy conduction of water Low levels of ACC deaminase resultant in lower levels of endogenous ethylene, which removes the potentially inhibitory properties of stress-induced higher ethylene content

References CalvoPolanco et al. (2016) Tiwari et al. (2016) Vurukonda et al. (2016b) Yanni et al. (2016) Pereyra et al. (2012) Jha et al. (2012); Patel et al. (2019)

5 Role of PGPR in Alleviating Salinity Stress Soil salinity harshly affects crop growth, soil quality and fertility in many countries of the world (Sagar et al. 2022). Saline soils are a main problem for agriculture lands because salt turns agronomically useful lands into fruitless lands. Salinity affects plant growth promotion and is a major abiotic stress that limits plant productivity (Ilangumaran and Smith 2017). Salinity decreases the yield of many plants because salt constrains plant photosynthesis, protein synthesis and lipid metabolism. PGPR are beneficial microbes that live in the plant rhizosphere which is one of the remedies to solve these problems. Certainly, rhizobacteria counter osmotic stress and help plant growth promotion (Paul and Lade 2014). Effect of PGPR on plants under salinity stress condition is listed below (Table 14.4). In the era of climate change, there is a requirement to sustain food security for a growing global population through enhancing plant production while also forging agriculture more sustainable. The quality of land and water will be critically essential for agriculture. Excess salt content in soil and water resources degenerates agricultural productivity, which turns fertile fields to marginal lands and leads to their relinquishment (Ilangumaran and Smith 2017). Salinity is one of the major abiotic stresses that challenges plant growth and development (Pitman and Lauchli 2002). Soil salinization is caused by natural or human activities that increase the content of dissolved salts, basically sodium

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Table 14.4 Effects of PGPR on plants under salinity stress conditions (Ilangumaran and Smith 2017) PGPR Bacillus amyloliquefaciens SN13 Bacillus megaterium Bacillus thuringiensis NEB17

Crop species Oryza sativa

Beneficial effects Upregulation of SOS1, EREBP, SERK1, NADP-Me2

Reference Nautiyal et al. (2013)

Zea mays

Marulanda et al. (2010) Subramanian et al. (2016)

Enterobacter sp. UPMR18 (ACC deaminase) Pseudomonas putida UW4 (ACC deaminase)

Abelmoschus esculentus

Improved expression of two ZmPIP isoforms Upregulation of PEP carboxylase, RuBisCo oxygenase large subunit, pyruvate kinase, proteins of photosystems I and II, isocitrate lyase and antioxidant glutathione-S-transferase Upregulation of reactive oxidative species pathway genes and antioxidant enzyme activities Increased shoot growth and expression of toc GTPase

Glycine max

Solanum lycopersicum

Habib et al. (2016) Yan et al. (2014)

chloride in the soil. Primary salinity occurred by natural processes, leading to significant salt gathering in soil and groundwater till over extended time period, which result in the creation of salt lakes and marine sediments in the landscape. Salinity may arise from enduring of rocks and minerals that releases soluble salts, windborne salts from oceans and sand dunes that are deposited inland (Pitman and Lauchli 2002). PGP bacteria may survive high salinity via three main mechanisms such as pumping out the cell, intracellular adaptation procedures and cell wall construction (Mokrani et al. 2020). Microbes could stimulate plant growth through certain mechanisms including production of phytohormones, enrichment of nutrient uptake, ACC deaminase synthesis, phosphate solubilization, production of exopolysaccharide, biofilm formation and N2 fixation under saline stress (Mokrani et al. 2020).

6 Role of PGPR in Alleviating Heavy Metal Stress Plants dealing with toxic metals which involve polyphosphates and long chains of thiophosphates for metals sequester. E. coli produced biofilm under nickel stress which may help as tolerance mechanism. A presence of rhizospheric microbial population improved the heavy metal-polluted sites and boosted the accumulation of metals in shoot of the hyper-accumulator Arabidopsis halleri. Different Rhizobium leguminosarum strains showed cadmium tolerant and enhances the levels of glutathione which representing about tripeptide tolerates bacterium to deal under heavy metals stress rather than efflux systems activate (Chaudhary et al. 2019). Metal toxicity occur in cell or plant organs; at this condition potent glutathione

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antioxidant is generated to protect against environmental stress (Chaudhary et al. 2019). The algae present in marine environment may interrelate with microbes to remove contaminants from the environment. Artificially generated mixture of dried algae with bacteria can eliminate contaminants from water and soil. Combination of Ralstonia basilensis bacteria and microalga Chlorella sorokiniana successfully adsorb the metals such as cadmium, nickel, copper and zinc (Chaudhary et al. 2019). Plants possess a network of defence strategies to tolerate heavy metal intoxication. Physical barriers are the first line of defence in plants against heavy metals. Biosynthesis of different cellular biomolecules is the primary way to tolerate metal toxicity. This includes the induction of numerous low-molecular-weight chelators such as nicotinamide, organic acids, glutathione, phytochelatins and metallothioneins or cellular exudates such as flavonoid, phenolic compounds, protons, heat-shock proteins and definite amino acids such as proline and histidine and hormones such as salicylic acid, jasmonic acid and ethylene (Viehweger 2014; Dalvi and Bhalerao 2013). When the above-mentioned approaches are not able to work then metal poisoning, equilibrium of cellular redox systems in plants is upset, leading to the improved induction of reactive oxidative species (Mourato et al. 2012). To alleviate the harmful effects of free radicals, plant cells have established antioxidant defence mechanism which is composed of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (GPX) and glutathione reductase (GR) and non-enzymatic antioxidants like ascorbate (ASA), glutathione (GSH), carotenoids, alkaloids, tocopherols, proline and phenolic compounds such as flavonoids, tannins and lignins that performed as the scavengers of free radicals (Sharma et al. 2012; Rastgoo et al. 2011). Certain biological molecules involved in cellular metal detoxification have antiradical, chelating or antioxidant activities. Exploitation and upregulation of these mechanisms of biomolecules may depend on plant species, metal tolerance level (Solanki and Dhankhar 2011), stages of plant growth and type of metals (Emamverdian et al. 2015).

7 Role of PGPR in Alleviating Flooding Stress PGPR contain the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase (Glick et al. 1998; Shah et al. 1998) which can cleave the ACC, a plant ethylene precursor (Yang and Hoffmann 1984), and thereby reduce the level of ethylene in a plant under stress condition. When PGPR containing the enzyme ACC deaminase are bound to the seed coat of a developing seedling, they may act as a sink for ACC. By facilitating the formation of longer roots, these bacteria may enhance the survival of some seedlings, especially during the first few days after the seeds are sowed (Glick et al. 1998). Moreover, ACC deaminase-containing PGPR can protect a plant from the harmful effects of environmental stress (Burd et al. 1998). In flooding, ACC, which is synthesized in roots, is transported to shoots of plant where it is converted into ethylene by ACC oxidase (Else and Jackson 1998; Grichko and Glick

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2001). The molecular basis for the increase in production of ethylene which is observed in shoots of flooded tomato plants is the enhanced activity of both ACC synthase in submerged roots and ACC oxidase in shoots (Shiu et al. 1998). Since the ethylene production in the shoots of flooded tomato plants is responsible for the phenotype that is observed following flooding (Jackson 1997), tomato seeds were inoculated with ACC deaminase-containing plant growth-promoting bacteria in an attempt to reduce the content of flooding stress ethylene. It was reasoned that these bacteria might work as a sink for ACC, thereby ameliorating some of the damage to plants which is caused by flooding (Grichko and Glick 2001).

8 Role of PGPR in Alleviating Cold Stress Cold-tolerant PGPR are of great agronomic potential due to the fact that crop growing cycle in most parts of the world is subject to varying cold temperatures. They are metabolically functional at cold condition and produce metabolites such as plant growth regulators that directly promote growth and facilitate plant nutrient uptake, while beneficial activities of mesophilic microbes stop at cold temperature. PGPR enhance plant growth as well as improve their resistance to stress. PGPR can stimulate developmental changes in host plants, disrupt phytopathogen organization, induce systemic resistance to pathogens, affect production of phytohormone and recover nutrient and water management (Barka et al. 2006). Microorganisms play a major role in sustaining the production and productivity of any agro-ecosystem through numerous roles that include nitrogen fixation, nutrient solubilization, mobilization, plant growth promotion and the destruction of harmful pathogens and insects. A unique feature of temperate agro-ecosystems around the world is the short growing periods, which are scattered by suboptimal temperatures. This effect is most marked in the case of nutrient transformations where microbes play an enormous role. In such a scenario where time and temperatures are crucial determinants of both plant growth promotion and microbial growth, cold-tolerant microbes, which retain their activity in suboptimal temperature conditions, play a significant role. Since microbes are an essential part of any ecosystem, they play a major role in cycling of nutrients in cold ecosystems (Haggblom and Margesin 2005). Based on their preference for cold temperatures, microbes are classified as psychrophiles (cold loving) and psychro-tolerant (cold tolerant) (Mishra et al. 2012).

9 Role of PGPR in Alleviating Heat Stress Majority of earth biosphere have been colonized by high- and low-temperaturetolerant microbes. Microbes adapted for low temperature show plant growth properties under low temperature. Pseudomonas cedrina, Brevundimonas terrae and Arthrobacter nicotianae adapted for low temperature expressed multifunction

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plant growth-promoting ability (Yadav 2014). The PGPR isolated from root nodule of low-temperature-growing pea plant have effective biofertilizer capability in low temperature (Meena 2015). Inoculation of thermotolerant phosphate-solubilizing microbes in agriculture field acts as multifunctional biofertilizer. It works as biogeochemical phosphorus cycling in agriculture field (Kumar and Verma 2018). Heat stress adversely affects the growth and development of plant seedlings. Studies reported that a temperature increase of 3–4 °C could cause plant yields to reduce by 15–35% in Africa and Asia and by 25–35% in the Middle East (Ortiz et al. 2008). There are few physiological and molecular factors involved in signalling cascades of transcriptional control for tolerance of temperature stress such as stress proteins, osmo-protectants, free radical scavengers and ion transporters (Mishra 2018). Pseudomonas putida, able to survive at low soil moisture potential, colonized the rhizoplane and soil adhering to wheat and sunflower roots which increased the stable soil aggregate percentages. Bacillus spp. have established to be an ideal candidate for development as stable and efficient biological products because of their ability to produce heat-resistant endospores (Yanez et al. 2012). Certain PGPR produce multifunctional polysaccharides such as exopolysaccharides, active signalling molecules playing pivotal role in biofilm formation, root colonization, interaction of microbes with root appendages and abiotic stress conditions (Mishra 2018).

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Future Prospects

Genetic engineering can be used to develop PGPR strains that are effective at low inoculum doses and under a variety of environmental conditions. It is crucial to develop more effective PGPR strains with long shelf lives to achieve sustainable plant production in agricultural drylands. Recent advances in the fields of microbiology, biotechnology, molecular biology and bioinformatics have opened up the way to identify novel techniques involved in drought tolerance. Concepts of microbial biotechnology application in agriculture should be employed to isolate indigenous PGPR from the stress-affected soils, and screening on the basis of their stress may be helpful in rapid selection of efficient strains that could be used as bioinoculants for plants grown in drylands. Applications of bio-nanotechnology could also provide new paths for the development of carrier-based microbial inoculum.

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Conclusion

Occurance of Abiotic stresses simultaneously, cause the interactions of physiological processes, usage of various environmental stress-tolerant PGPR with multiple plant growth-promoting attributes which are very cost-effective and environmentfriendly strategy to alleviate plant abiotic stresses in sustainable agriculture, and

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mitigate environmental stress influences on global food supply production. In general, identifying and using various abiotic stress-tolerant PGPR with multiple plant growth-promoting efficacy could not only enhance the abiotic stress tolerance of plants but also reduce pressure on cultivable agricultural lands. The implementation of plant growth-promoting rhizobacteria into the agriculture can be a gainful alternative because of its efficacy in plant growth regulation and mitigating abiotic stress management. Acknowledgement Authors are thankful to Prof. Meenu Saraf, Prof. B. V. Patel and Department of Microbiology and Biotechnology, Gujarat University, for their support.

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Chapter 15

Endophytic PGPM-Derived Metabolites and their Role in Arid Ecosystem R. Srinivasan, Sonu Kumar Mahawer, Mahendra Prasad, G. Prabhu, Mukesh Choudhary, M. Kumar, and Ritu Mawar

1 Introduction About one third of planet Earth’s land area is occupied by arid ecosystem, with deserts alone occupying more than 46 million km2, inhabited by nearly 2.1 billion people (Osborne et al. 2020). It is home to a great diversity of plants as well as animal species, of which many are unique to this ecosystem. Arid environment is characterized by lesser annual precipitation (from 500 to 105 cfu/g fresh root) and impact plant growth positively (Spaepen et al. 2009). These soil microbes improve the input use efficiency by reducing the production cost and also environment pollution, as efficient PGPMs also reduce the use of synthetic fertilizers (Souza et al. 2015). Various microbes, viz. fungi, bacteria, actinomycetes and yeasts, are used as inoculants, and primarily they assist in plant growth and health through various beneficial activities like fixing atmospheric nitrogen, solubilizing phosphate and potassium, exopolysaccharide secretion, biocontrol activity, organic matter decomposition, siderophore production, etc. (Antoun and Prévost 2006; Srinivasan et al. 2012a, b; Gupta et al. 2015; Shaikh et al. 2016; Prasad et al. 2017; Karthikeyan et al. 2018; Prasad et al. 2019; Prasad et al. 2020; Basu et al. 2021). Generally, rhizosphere is a playground for PGPM activities, dominated mainly by indigenous bacteria and fungi (Nelson 2004; Bahadur et al. 2017; Verma et al. 2017). PGPMs’ functions such as solubilizing different inorganic compounds, decomposition and mineralization of organic residues and secretion of bioactive substances like phytohormones, chelators and antibiotics significantly help in plant growth promotion (Kapulnik and Okon 2002).

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Types and Classification of PGPMs

PGPMs are grouped into two major groups: (i) plant growth-promoting rhizobacteria (PGPR) and (ii) plant growth-promoting fungi (PGPF). PGPR are a group of bacteria capable to actively colonize the plant roots sometimes on foliages and/or within plant tissues and enhance their growth and yield (Wu et al. 2005; Glick 2012). PGPR constitute only two to five percent of total rhizospheric bacterial population (Antoun and Kloepper 2001). A vast array of free-living and associative and symbiotic rhizobacterial species from the genera Pseudomonas, Rhizobium, Azospirillum, Azotobacter, Klebsiella, Enterobacter, Alcaligenes, Arthrobacter, Burkholderia, Bacillus and Serratia were reported as PGPR (Saharan and Nehra 2011; Beneduzi et al. 2012; Ahemad and Kibret 2014). These PGPR can affect directly and/or indirectly plant growth and development through different mechanisms (Dakora and Phillips 2002; Glick 2012; Zope et al. 2019). In totality, these microbes modulate plant-soil chemistry which improved plant growth and agricultural sustainability. PGPF are saprophytes and not plant disease-causing, which help to improve soil fertility that, in turn, enhances plant growth and induce first-line defence response against pathogen infections (Hossain et al. 2017; Zhang et al. 2018; Muslim et al. 2019). Many workers also reported plant growth promotion attributes of PGPF (Salas-Marina et al. 2011; Murali et al. 2012). Under PGPF, many species of Phoma, Penicillium, Aspergillus, Fusarium, Trichoderma and arbuscular mycorrhizal fungus (AMF) are most studied due to their effective role in plant growth activities and disease suppression (Hossain et al. 2014; Murali and Amruthesh 2015; Srinivasan et al. 2020). The root colonization capability of PGPF is considered as the most important function involved in the prevention of the pathogen and also increase in nutrient uptake, hence promoting plant growth (Zhang et al. 2018). Besides, the ability of the PGPF to solubilize insoluble phosphates and to produce IAA, siderophore, cellulase, chitinase, etc. act directly or indirectly towards improving plant growth and development (Yandigeri et al. 2011a, b; Jogaiah et al. 2013; Muslim et al. 2019).

2.2

Role of PGPMs on Plant Growth Promotion

PGPMs take vital role in an ecosystem by balancing the biotic-abiotic interactions through ecological associations with biotic community as well as nutrient and mineral cycling of the abiotic components. At present, use of PGPM inoculants for sustainable crop production is getting more popularity in different parts of the world, and their use in agroecosystem and solving important environmental issues has shown remarkable results. PGPMs increase crop yield through biological nitrogen fixation, production of siderophores, ACC deaminase and plant growth hormone, phosphorus and mineral solubilization, soil characteristic enhancement, etc. In

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addition to that, microbes also function as biocontrol and biopesticide for plants. PGPMs enhance growth of plants through either direct or indirect mechanisms, which involve enhancing plant physiology and resistance to different phytopathogens through various modes and actions (Zakry et al. 2012). Direct mechanism includes soil amelioration, production of phytohormones and increasing nutrient availability by solubilizing and mobilizing soil mineral substances, while indirect mechanism includes the production of antimicrobial compounds that suppress plant pathogens, thereby providing a healthy crop environment.

2.3

Bioactive Metabolites of Endophytic PGPMs

The “bioactive metabolites” are extra-nutritional compounds present in very small quantities in lipid-rich foods and plant products (Cammack et al. 2006). These metabolites are generally produced by many plants and microbes and have multifunctional prospects (Fadiji and Babalola 2020). The endophytic PGPMs play a big role in the production of bioactive metabolites. Furthermore, 45% of bioactive metabolites obtained from microbes are produced by fungi, actinomycetes and unicellular bacteria. The bioactive secondary metabolites are produced mostly from precursors from primary metabolism with a comparatively small number (Demain and Fang 2000). Endophytic PGPMs synthesize secondary metabolites via a spread of pathways, e.g. polyketide, isoprenoid or aminoalkanoic acid derivation (Jalgaonwala 2013; Jabborova et al. 2020). However, the biosynthetic pathways are liable for the assembly of both primary and secondary metabolites (Nicolaou et al. 2011). Endophytic PGPMs produce low molecular weight secondary metabolites comprising antimicrobial compounds, phytohormones or their precursors, bioprotectants (Trotsenko and Khmelenina 2002) and vitamins such as B12 (Ivanova et al. 2006) and B1 (Mercado and Bakker 2007). Endophytic fungi are the important source for production of bioactive metabolites of higher value (Dreyfuss and Chapela 1994). Pestalotiopsis neglecta BAB-5510, an endophytic fungus of Cupressus torulosa, is considered as a main source for phenols, flavonoids, terpenoids, alkaloids, tannins, carbohydrates and saponin (Sharma et al. 2016a), while Gilmaniella sp. AL12, an endophytic fungus, can stimulate Atractylodes lancea to supply volatile oils like β-caryophyllene, caryophyllene oxide, zingiberene, hinesol, β-eudesmol, β-sesquiphellandrene and atractylone (Chen et al. 2016). Huperzia serrata (L10Q37 and LQ2F02), an endophytic fungus, also has antiacetylcholinesterase activity (Zhejian et al. 2015). Endophytic fungus Talaromyces pinophilus, isolated from Irish strawberry (Arbutus unedo), produces ferrirubin (siderophore), herquline B (platelet-aggregation inhibitor) and the antibiotic 3-Omethylfunicone. This strain also showed toxicity against the pea aphid Acyrthosiphon pisum (Homoptera aphidiidae) (Vinale et al. 2017). Fusarium oxysporum 162 produced nematode antagonistic compounds, 4-hydroxybenzoic acid, indole-3-acetic acid (IAA) and gibepyrone D (Liu et al. 2016; Bogner et al. 2017). Several endophytic bacteria also produced bioactive compounds, viz.

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alkaloids, flavonoids, steroids, terpenoids, quinols and phenols, peptides, polyketones and the natural insecticide azadirachtin (Li et al. 2008; Kusari et al. 2012; Molina et al. 2012). Amines as well as amides are normal bioactive metabolites from endophytes that are toxic to insects but not mammals. Endophytes also produce extracellular hydrolyases like proteinase, lipases, cellulases and esterases to determine resistance against plant invasions (Tan and Zou 2001). These bioactive compounds have multiple uses in agricultural, industrial and medical applications (Kobayashi and Palumbo 2000; Zinniel et al. 2002). Recently, endophytes isolated from medicinal plants have gotten much attention because they are considered containing natural products benefitting humans (Gunatilaka 2006). Several of those medicinal plants are tested for endophytes everywhere on the planet (Li et al. 2008). Many workers are trying to isolate new bioactive metabolites from newer species of endophytes for applications in medicinal, agricultural and industrial aspects, despite their failure to certify their origins, pathways and mechanisms of action (Garg et al. 2011). It is therefore very essential to motivate researchers to isolate new bioactive metabolites (Zuccaro et al. 2011).

3 Endophytic PGPMs-Derived Metabolites in Plant Growth Promotion in Arid Ecosystem Endophytic PGPMs have been proven to impart many beneficial mechanisms on their plant host directly or indirectly. Endophytic PGPMs directly promote plant growth by helping plants in obtaining nutrients and phytohormone regulation, which lead plants to grow better under normal and stressed conditions, and indirectly, PGPMs improve plant growth by inducing systemic resistance as well as discouraging phytopathogens through various means like antimicrobial compound and lytic enzyme production and nutrient unavailability for the pathogens (Miliute et al. 2015; Ma et al. 2016; Prasad et al. 2017; Khoshru et al. 2020; Ahmed et al. 2021).

3.1

Nutrient Availability

Macronutrients (nitrogen, phosphorus, potassium, calcium, magnesium and sulphur) are absorbed by the plants in more quantities from the soil. Most agricultural lands/ soils lack an optimum amount of one or more of these nutrients so that plant growth is suboptimal. To obtain higher crop productivity, farmers are increasingly depending on chemical fertilizers. Besides being costly, chemical fertilizers cause human and environmental hazards. It would be beneficial, if efficient biological means of supplying these nutrients to plants could be used to substitute partial quantity of chemical fertilizers that is currently used. Endophytic PGPMs can enhance macro- and micronutrient availability for their host plants through various

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mechanisms such as biological nitrogen fixation; solubilization of phosphorus, potassium and zinc; production of Fe-chelating molecules (siderophores); and secretion of various plant hormones (Srinivasan et al. 2012a; Jha et al. 2013; Srinivasan et al. 2018; Prasad et al. 2019).

3.2

Biological Nitrogen (N2) Fixation

Nitrogen is the major limiting element for plant growth (Munees and Mulugeta 2014). Most part of this element is in gas (N2) form, which is not accessible to most of the plants and animals (Pujic and Normand 2009). Most of the plants absorb nitrogen in the form of nitrate and ammonium ions. Biological N fixation (BNF) is the main source of nitrogen to the plants particularly in legume plants. Most of the leguminous plants are able to interact with N-fixing bacteria, collectively referred to as rhizobia that are capable to convert gaseous nitrogen (N2) into ammonia (NH3) in specialized root nodules. As per reports, global contribution of BNF is 180 × 106 MT per year, and major portion (83%) of this comes from symbiotic BNF, while rest part is contributed by free-living microbes and/or in associative systems (Graham 1988). One important diazotrophic endophyte, Gluconacetobacter diazotrophicus, which was initially isolated from sugarcane (Saccharum officinarum) had the ability to fix N approximately 150 kg N ha-1 year-1 (Dobereiner et al. 1993). Some other potential endophytes are Azoarcus and Rhizobium leguminosarum (Höflich et al. 1995; Webster et al. 1997). Rosenblueth et al. (2018) and Dent and Cocking (2017) suggested that intracellular Gluconacetobacter diazotrophicus cells (single or pellicles) act as nitrogen-fixing organelles referred to as ‘diazoplasts’ which may leak nitrogen into plant tissues. Chang et al. (2021) suggested another function called ‘nutrient trap mechanism’, for BNF and transfer from intracellular diazotrophic bacteria. In this, intracellular bacteria secrete ethylene to trigger the host root cell, i.e. root hair, to grow and provide intracellular bacteria with exudates like carbohydrates that fuel nitrogenase activity; simultaneously, the root cell produces superoxide triggering bacteria to secrete antioxidant nitrogen (nitric oxide or NH3) that combines with superoxide to produce nitrate that may be absorbed directly by the plants (Khan et al. 2020). These findings suggest that endophytic bacteria have a considerable ability to increase the sustainable N availability through BNF to plants.

3.3

Phosphorus Solubilization

Phosphorus (P) is one of the major elements required for plant growth and development. It plays a vital role in various metabolic processes including photosynthesis, respiration, energy transfer, macromolecular biosynthesis, etc. (Anand et al. 2016). It is abundantly available in soils, but very less available to plants and animals because more than 95% P present in the insoluble, immobilized and precipitated form.

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Hence, it becomes very difficult for plants to absorb it, and thus less availability of P in soil hampers the crop productivity (Hani 2012; Wang et al. 2017). Phosphorus solubilization/dissolution of mineral compounds is the essential mechanism to increase its availability (Sharma et al. 2016b; Olanrewaju et al. 2017). Endophytic PGPMs change the soil pH to solubilize inorganic phosphates. In alkaline soils, PGPMs reduce pH by secreting organic acids, such as gluconate, citrate, lactate and succinate, solubilizing Ca3(PO4)2. In acid soils, PGPMs increase the pH by production of protons, during the assimilation of ammonium (NH+4), solubilizing AlPO4 and FePO4 (Martínez-Viveros et al. 2010). Numerous bacteria species, namely, Arthrobacter, Bacillus, Beijerinckia, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Mesorhizobium, Microbacterium, Pseudomonas, Rhizobium, Rhodococcus and Serratia (Srinivasan et al. 2012a; Otieno et al. 2015; Srinivasan et al. 2018), are identified as phosphate-solubilizing microbes. Pseudomonas, Bacillus and Rhizobium are the foremost efficient phosphate-solubilizing strains (Rodriguez and Fraga 1999; Yu et al. 2012; Li et al. 2016). Many studies demonstrated the role of endophytic PGPMs as a biofertilizer. For example, endophytes isolated from the root nodule of peanut (Pantoea spp.) were reported to have more P-solubilizing activity (Yadav et al. 2018). Likewise, endophytic actinomycetes are reported to perform an important role in phosphate solubilization and also enhance its availability to plants through chelation, acidification and mineralization and redox changes of organic phosphorus (Singh and Dubey 2018). Solubilization of phosphate and secretion of phytase were also reported by an endophytic actinomycete, Streptomyces sp., which significantly improve plant growth (Jog et al. 2014).

3.4

Potassium Solubilization

Next to nitrogen and phosphorus, potassium (K) is the most essential element for plant and animal growth. It plays major roles in osmotic regulation, energy relation, protein and starch synthesis and improving resistance to pest and diseases. Mostly K is present (> 90%) as insoluble silicate minerals in rocks. Thus, potassium availability is very less in the soil (Parmar and Sindhu 2013), and insufficiency of K has raised a big challenge in sustainable plant nutrition (Nath et al. 2017; Meena et al. 2017). So, it’s essential to seek out an alternate endemic source of K for maintaining K availability in soils for sustainable crop production (Kumar and Dubey 2012). K solubilization is performed by numerous PGPMs, viz. bacteria, fungi and actinomycetes (Ahmad et al. 2016; Bakhshandeh et al. 2017; Baba et al. 2021). Potassium (rock)-solubilizing ability of PGPMs by producing and secreting organic acids has been widely reported (Sindhu et al. 2016; Bahadur et al. 2017). PGPMs, such as Acidithiobacillus ferrooxidans, Bacillus edaphicus, Bacillus mucilaginosus, Pseudomonas, Burkholderia and Paenibacillus, have been reported to release potassium in accessible form from potassium-bearing minerals in soils (Liu et al. 2012). Therefore, application of K-solubilizing PGPMs as biofertilizers could help to

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improve agriculture and reduce the use of chemical fertilizers and support sustainable crop production (Bakhshandeh et al. 2017; Wei et al. 2017; Basak et al. 2017).

3.5

Siderophore Production

Iron (Fe) is one of the most essential micronutrients for crop production. It is involved in many important metabolic processes like chlorophyll biosynthesis, photosynthesis and respiration. Fe is the fourth most abundant nutrient in Earth’s crust. But the massive quantity of iron is in the ferric ion form (Fe3+), which is either little or not assimilated by living organisms (Ammari and Mengel 2006). To meet out this difficulty and provide iron to the plant, PGPMs have developed various iron uptake strategies to survive and to adapt to their environment. Siderophore production is the well-established mechanism for increasing Fe availability to plants. Siderophores are organic compounds having low molecular weight and are produced by microbes under iron-limiting conditions that enhance Fe uptake capacity (Whipps 2001; Li et al. 2016; Wani et al. 2016; Manasa et al. 2021). Pseudomonas, Enterobacter, Burkholderia and Grimontella are capable of siderophore production. Siderophores are chelator agents, with high specificity for binding Fe, followed by transportation and deposition of Fe3+ within bacterial cells. Based on chemical function involved in chelation, siderophores are classified into three types, viz. catechol/phenol, hydroxycarboxylic acid and hydroxamate. A number of bacterial proteins are involved in Fe uptake and transport. Iron uptake by bacterial species depends on the inherent available concentration of iron in soil. Limited research is available with respect to the ability of siderophores in improvement of Fe nutrition in crop plants (Sayyed et al. 2019). Information about the capacity of siderophores to enhance iron uptake by plants is scanty; hence, in-depth research is further required in this context.

3.6

Zinc Solubilization

Zinc is another important micronutrient which is required in very little concentrations (5–100 mg kg-1) in tissues for optimum growth and reproduction of plants (Alloway 2004). At global level, deficiency of Zn in plants is due to lower solubility of Zn-containing minerals in soil resulting in low Zn availability (Iqbal et al. 2010; Gontia-Mishra et al. 2016). In Indian context, more than 50% soils are deficient in required Zn content (Ramesh et al. 2014). Deficiency of Zn can be addressed by the use of Zn-based fertilizers in the agricultural crops; however, most of the synthetic fertilizers are costly and adversely affect the natural environment. Therefore, to meet out this situation, Zn-solubilizing PGPMs are the encouraging alternatives for Zn nutrition and crop enrichment with Zn (Barbagelata and Mallarino 2013). Many bacterial genera including Pseudomonas and Bacillus have been observed for

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solubilizing zinc from insoluble Zn compounds. These PGPMs solubilize insoluble Zn compounds by protons and oxidoreductive systems present on the cell surface, membranes and chelated ligands (Hughes and Poole 1991; Wakatsuki 1995). Since Zn is taken into account as limiting thing in sustainable crop nutrition, Zn-solubilizing bacteria could play a really crucial role in Zn nutrition to field crops (Barbagelata and Mallarino 2013; Gontia-Mishra et al. 2016).

3.7

Sulphur Availability

Sulphur is one of the most abundant nutrients (13th) in Earth’s crust with an average of 0.06%. In India, more than 41% soils are deficient in sulphur (Singh 2001). Sulphur is also found in amino acids, viz. cysteine and methionine. These amino acids are essential in maintaining of protein synthesis and enzymes. Cysteine plays a major role in cell division, whereas methionine is a precursor of ethylene, responsible for fruit ripening (Taiz and Zeiger 2017). Some volatile compounds like dimethyl disulphide produced by Bacillus provide sulphur for plants. Besides Bacillus, Aspergillus also produce organic and inorganic acids and chelation and exchange reactions which are also capable of solubilizing potassium (Varma et al. 2019).

4 Endophytic Microbes-Derived Metabolites in Abiotic Stress Tolerance in Arid Ecosystem The growth promotional activities, modulation of plant secondary metabolites and phytohormone production by endophytic microbes enable the host plants to adapt to different abiotic stresses such as drought, heat, cold, salinity and alkalinity (Miliute et al. 2015; Khan and Sayyed 2019; Kour and Sayyed 2019; Nasab et al. 2021; Kusale et al. 2021). In this section, abiotic stress (particularly drought, heat and salinity) tolerance conferred by metabolites of endophytic origin is discussed.

4.1

Towards Drought Tolerance in Plants

Azospirillum spp. are nitrogen-fixing bacteria which have plant growth promotional activities through production of phytohormones as well (Khan et al. 2021). Cohen et al. have shown that plant hormones (abscisic acid and gibberellins) produced by Azospirillum spp. contribute to water stress tolerance in maize (Cohen et al. 2009). IAA produced by an endophytic fungus Alternaria alternata LQ1230 was found to enhance wheat plant growth and enhance the resistance to water deficiency (Qiang

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et al. 2019). Drought stress of tomato alleviated through inoculation of endophytic fungus Talaromyces omanensis was due to the production of high concentration of gibberellins by the fungus (Halo et al. 2020).

4.2

Towards Heat Tolerance in Plants

Culture filtrate of an endophytic fungus Aspergillus violaceofuscus improved the overall growth and chlorophyll content of sunflower and soybean seedlings under heat stress (Ismail et al. 2020). An endophytic fungus Paecilomyces formosus LWL1 with the ability to produce bioactive gibberellins and organic acids improved the growth of japonica rice varieties under prolonged heat stress. A gibberellinproducing endophytic strain Exophiala sp. LHLo8 was shown to modulate heat stress in cucumber (Khan et al. 2012). Most of the studies on endophytes alleviating heat stress were conducted with strains producing phytohormones like gibberellins and ACC deaminase (Sagar et al. 2020). Hence these metabolites can act as effective molecules for heat stress alleviation in arid ecosystem.

4.3

Towards Salinity Tolerance in Plants

An endophytic fungus Yarrowia lipolytica FH1 with the ability to produce high amounts of IAA, indole-3-acetamide, phenol and flavonoid contents was shown to enhance maize growth exposed to salt stress. This indicates the effect of these metabolites in alleviation of salt stress in crop plants (Jan et al. 2019; Fazeli-Nasab and Sayyed 2019; Kapadia et al. 2021). Exopolysaccharides secreted by an endophytic bacterium Pantoea alhagi (NX-11) alleviated salt stress in rice (japonica variety) (Sun et al. 2020).

5 Endophytic Microbial Metabolites in Plant-Microbe Interaction in an Arid Ecosystem Massive volume of money is spent for chemical pesticide application in respect to control plant insect pest and diseases globally. The application of use of PGPRderived secondary metabolites is one of the environmentally sound insect pest and disease management strategies (Raupach and Kloepper 1998; Walsh et al. 2001; Patel et al. 2016; Sharma et al. 2020; Mishra et al. 2021; Hamid et al. 2021). Relationship between PGPR, biopesticides and biocontrol agents is illustrated in Fig. 15.1. Endophytic microbes such as bacteria and actinomycetes are often found to produce secondary metabolites which are involved in plant-microbial interaction

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Fig. 15.1 Illustration of overlap/relationship between biopesticides, biocontrol agents and PGPR

in different manner (Ilyas et al. 2020). These endophytic secondary metabolites are found effective in several plant biotic stress management, for instance, direct involvement in insect pest and disease management or indirect pest and disease control by inducing systemic resistance in crop plants.

5.1

Management of Soil-Borne Diseases

Endophytic microbes are responsible for producing a variety of antifungal compounds to accomplish reducing or suppressing infection by soil-borne pathogenic fungi in several crops (Ongena et al. 1999; Bloemberg and Lugtenberg 2001). Endophytes-derived antibiotics are found as one of the most influential and studied mechanisms of PGPR for contesting plant pathogens (Zakaria et al. 2019; Suriani et al. 2020). Antibiotics comprehend an extensive and diverse group of low molecular weight organic compounds that are synthesized by numerous microbes. They are detrimental for other microorganisms even in low concentration (Thomashow Vinay et al. 2016). Several antibiotics, for example, 1996; 2,4-diacetylphloroglucinol (DAPG; 1), phenazine-1-carboxylic acid (2), phenazine-1-carboxamide (3), pyoluteorin (4), pyrrolnitrin (5), viscosinamide (6), butyrolactones (7), kanosamine (8), bacillomycin (9), iturin A (cyclopeptide; 10), aerugine (11), rhamnolipids (12), cepaciamide A (13), pseudomonic acid (14), etc. (Fig. 15.2), have been obtained from numerous PGPR representing diverse bacterial genera (Fernando et al. 2005). Secondary metabolites of pseudomonads identified and utilized for biocontrol of soil-borne pathogenic fungi are depicted in Table 15.1.

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Fig. 15.2 Secondary metabolites (antibiotics and others) of endophytic PGPR involved in plant protection

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Fig. 15.2 (continued)

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Table 15.1 Secondary metabolites of pseudomonads and Bacillus spp. identified and utilized as biological control of soil-borne pathogenic fungi

Microorganism(s) Pseudomonas fluorescens

Metabolite(s) 2,4-Diacetyl phloroglucinol (DAPG; 1)

Pseudomonas fluorescens

DAPG (1)

Pseudomonas putida

Pyoluteorin (4)

P. fluorescens

Phenazine-1-carboxylic acid (PCA; 2) Phenazine-1carboxamide (PCN) Viscosinamide (6) Hydrogen cyanide Surfactants

P. aeruginosa

P. fluorescens DR54 Pseudomonas sp. P. fluorescens P. fluorescens P. fluorescens HC1-07 Bacillus amyloliquefaciens

Massetolide A (15), cyclic lipopeptide Viscosin-like cyclic lipopeptide Iturin-like compounds

B. cereus UW85

Zwittermicin A

B. amyloliquefaciens FZB42 B. mojavensis RRC101 B. subtilis Bs 8 B-1

Bacillomycin D

Bacillus pumilus

Fengycin (16) Fengycin (16), bacillomycin (9), bacilysin (17), surfactin (18) and iturin A (10) Bacilysin (17)

Soil-borne pathogenic fungi/ disease controlled Fusarium oxysporum

Gaeumannomyces graminis var. tritici Red rot

Crop(s) Several crops

Wheat

Sugarcane

Reference(s) Schouten et al. (2004), Meyer et al. (2016) and Maurhofer et al. (1995) Kwak et al. (2009) Hassan et al. (2011) Huang et al. (2004)

Rhizoctonia root rot

Wheat

R. solani

Rice

Shanmugaiah et al. (2010)

Pythium ultimum

Sugar beet

R. solani

Rice

P. capsici

Pepper

P. infestans

Tomato

Thrane et al. (2000) Jayaprakashvel et al. (2010a, b) Özyilmaz and Benlioglu (2013) Tran et al. (2007)

Rhizoctonia root rot Sclerotinia stem rot, charcoal rot, and fusarial wilt Phytophthora medicaginis Fusarium graminearum Fusarium verticillioides Pythium, Phytophthora, Rhizoctonia

Wheat

Phytophthora

Soybean

Alfalfa Wheat Maize Cucumber and radish

Potato

Yang et al. (2014) Romero et al. (2007) Stabb et al. (1994) Gu et al. (2017) Blacutt et al. (2016) Khabbaz et al. (2015)

Caulier et al. (2018)

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Endophytic PGPR also show antagonistic action against plant pathogens through excretion of siderophores. Siderophores are compounds with low molecular weight, which favourably chelate iron (Fe3+) and carry it into the cell across the cell membrane (Neilands 1995). They bind most of the Fe3+ in the rhizosphere and meritoriously avert the explosion of fungal pathogens by making iron scantly available (Kloepper et al. 1980; O’Sullivan and O’Gara 1992; Jadhav et al. 2017). Pathogenic fungi are suppressed because deficiency of iron causes growth retardation, nucleic acid synthesis reduction, reduced sporulation and morphological changes in cells (Mathiyazhagan et al. 2004).

5.2

Metabolites with Pesticidal Properties in Plant Insect Pests and Disease Management

Endophytic microorganisms have been reported to produce secondary metabolites with anti-herbivore or anti-insect activities (Sumarah et al. 2010). For instance, many seed-transmitted endophytes synthesize alkaloids that have importance in protection of host plants from insects. Such alkaloids belong to several well-known classes of endophytic alkaloids (Table 15.2) such as ergot alkaloids, amino-pyrrolizidine (loline) alkaloids, indole diterpenoid (lolitrem) alkaloids, pyrrolo-pyrazine (peramine) alkaloids, etc. (Clay and Schardl 2002). Similar to insect pests and soil-borne plant diseases, endophytic metabolites also have been reported for their antibacterial and antifungal activities. A cluster of biocontrol strains can create single or numerous sorts of antibiotic agents including terpenoids, alkaloids, aromatics and polypeptides which have been demonstrated that plant pathogens are delicate to 3,11,12-trihydroxycadalene isolated from Phomopsis cassiae, was found among the five cadinane sesquiterpenes subordinates as antifungal active compound against Cladosporium sphaerospermum and C. cladosporioides (Silva et al. 2006). Alkaloids from endophytes were also sturdily conquering plant pathogens. For instance, an alkaloid (altersetin) from endophytic Alternaria demonstrated antibacterial activity against several pathogenic Grampositive bacteria (Hellwig et al. 2002). Similarly, volatile oils such as tetrahydrofuran (21), 2-methyl furan (22), 2-butanone (23) and aciphyllene (24) (Fig. 15.2) from Muscodor albus (an endophytic fungus from a tropical tree) reported for their antibiotic activities (Atmosukarto et al. 2005).

5.3

Role of Metabolites in Systemic Acquired Resistance Development

Apart from the direct involvement in insect pest control, PGPR endophytic secondary metabolites also are involved in plant-induced systemic resistance (ISR)

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Table 15.2 Metabolites with pesticidal properties in plant insect pests and diseases Antivertebrate/ anti-insect activity +

Metabolite Ergovaline (19), peramine

Endophyte spp. Epichloe amarillans

Peramine (20)

Epichloe elymi

Host plant(s) Agrostis, Sphenopholis, Calamagrostis Elymus spp.

Ergovaline (19), ergot alkaloids, loline alkaloids, indole-diterpenoids, peramine (20) Ergovaline (19), ergot alkaloids, loline alkaloids, peramine (20)

Epichloe festucae

Festuca, Lolium

+

Neotyphodium coenophialum

Lolium arundinaceum

+

Ergovaline (19), ergot alkaloids, indole-diterpenoids, peramine (20) Ergovaline (19), ergot alkaloids, peramine (20) Ergot alkaloids, loline alkaloids

Neotyphodium lolii

Lolium perenne

+

Neotyphodium

L. perenne

+

Neotyphodium

Achnatherum robustum

+

+

Reference(s) Siegel et al. (1990); White Jr and Glenn (1994) Siegel et al. (1990); Schardl and Leuchtmann (1999) Siegel et al. (1990); Leuchtmann et al. (2000); Wilkinson et al. (2000) Cheplick and Clay 1988; Clay (1990); Siegel et al. (1990); Christensen et al. (1993); Craven et al. (2001) Siegel et al. (1990); Christensen et al. (1993); Schardl et al. (1994) Christensen et al. (1993); Schardl et al. (1994) Petroski et al. (1992)

induction. These secondary metabolites which are responsible for ISR are commonly known as “elicitors.” The ISR mechanism involves several signalling pathways, like jasmonic acid (JA), ethylene (ET) and and salicylic acid (SA), being activated. Microbial compounds are denoted as pathogen-associated molecular patterns (PAMPs) or microbe-associated molecular patterns (MAMPs), which are recognized by plant receptors and induce PAMP/MAMP-triggered resistance (Nürnberger and Kemmerling 2009; Reshma et al. 2018). Common MAMPs are primary fungal cell wall components, viz. chitin and β-glucans (Lyon 2014). Similarly, endophytic proteins, amino acids, peptides and enzymes like xylanases, cellulases and chitinases are also identified in relation to plant response (Rotblat et al. 2002; Beliën et al. 2006; Druzhinina et al. 2011).

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6 High-Value Biochemicals from Endophytic Microorganisms in Arid Ecosystem Endophytic microorganisms live without any visible symptom in the healthy tissues of the host plants. Most of these endophytes can synthesize many bioactive primary and secondary metabolites that protect the host against pathogen and insect attacks, and also impart tolerance to other stresses (Zhang et al. 2006; Rodriguez et al. 2009; González-Menéndez et al. 2018; Sagar et al. 2022). Plants that live in desert survive extreme conditions by employing morphological and biochemical adaptations which could be attributed to microbial activity. Endophytic fungi produce biochemicals exclusive to their host plants, which increase the adaptability of both endophytic fungi and their host plants to biotic and abiotic stresses, and these compounds can contribute to production of biologically active secondary metabolites (Zhang et al. 2006; Rodriguez et al. 2009). Plants of arid environments have adaptations to drought due to associated endophytic microorganisms (Rodriguez et al. 2009; Jabborova et al. 2021). Drought-tolerant endophytic actinobacteria Streptomyces coelicolor, S. olivaceus and S. geysiriensis were isolated from arid and drought-affected areas of Rajasthan, India (Yandigeri et al. 2012). These actinobacteria produced auxin and supported plant growth under stress conditions. A thermophilic endophyte, Thermomyces lanuginosus, isolated from Cullen plicata enhanced root length of cucumber plants exposed to drought and heat (Ali et al. 2018). In plant-microbe interactions, more accumulation of carbohydrates and flavonoids in plant tissues function as ROS scavenger and signalling molecules promoting plant growth and increased tolerance to abiotic and biotic stress (Grover et al. 2011). Opuntia dillenii allows many endophytic fungi capable of producing antimicrobial substances with selective antibacterial activities. The endophytic Fusarium exhibited promising activity by producing antimicrobial substance (secondary metabolite), equisetin. By producing such biologically active compounds, the endophytic fungi help the host to successfully withstand stressful conditions and dominate the native plants in the area (Ratnaweera et al. 2015). Moreover, some of these compounds were proven to be useful for novel drug discovery (Yu et al. 2010; Yadav et al. 2014). Thus, endophytes and their secondary metabolites not only play an important ecological role but also positively influence medicine field. Original plant communities belonging to arid areas express specific characteristics for survival in extreme conditions. Many reports on bioprospecting showcase the endophytic fungi capable of producing a range of bioactive secondary metabolites (González-Menéndez et al. 2018). Many endophytes are also exploited for anticancer lead compounds (i.e. taxol, vincristine, vinblastine, camptothecin and podophyllotoxin) or for antifungal lead molecules (i.e. cryptocandin A, enfumafungin, CR377, ambuic acid, jesterone, moriniafungin, parnafungins or phaeofungin). González-Menéndez et al. (2018) isolated 349 endophyte fungi from 63 plant species from arid ecosystems of the Iberian Peninsula. Among them, 126 (36%) exhibited significant bioactivities

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(58 strains with exclusive antifungal properties and 33 strains with exclusive activity against the HepG2 hepatocellular carcinoma cell line). Khalil et al. (2021) found that new endophytic fungi isolated from A. marina survive in extreme environments by bioactive metabolite production, which can be exploited as a novel drug source. Wijeratne et al. (2008) isolated five new metabolites from endophytic fungi, Phyllosticta spinarum from Platycladus orientalis in the Sonoran Desert, and one of these compounds (Tauranin) showed anticancer promoter potential. Thus, endophytes from arid environments could enhance the resistance of their host plants to both biotic and abiotic stresses and also have potential to be an important source for the novel drug discovery.

7 Conclusion Endophytic PGPMs are a new and lesser researched group of microorganisms capable of synthesizing a wide range of bioactive compounds that can be used in arid agriculture. They are also reliable sources of bioactive and chemically novel metabolites and can be exploited for enhancing agricultural production in arid regions. In addition, they may also be used for novel drug discovery and other industrially important substances. This chapter highlighted the previous successes reported, ongoing research activities and latest developments in research associated with endophytic plant growth-promoting microorganisms and their metabolites so as to grow interest among researchers and students towards this upcoming field and possible exploitation of the available sources for enhancing agriculture production in arid ecosystem as well as uses in different sectors, such as the medical, pharmaceutical and food industries.

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Chapter 16

Current Regulatory Requirements for PGPM Products for Management of Seed, Soil and Plant Health: An Overview Ritu Mawar, B. L. Manjunatha, Archana Sanyal, Sushil K Sharma, H. B. Singh, and S. C. Dubey

1 Introduction Ensuring food security was the principal goal of the Government of India after the independence. Successful combination of improved technologies, policy support and outreach programmes helped India to achieve green revolution in the 1960s. The improved technologies viz., high yielding varieties of wheat and rice (through targeted breeding approaches) and chemical inputs in the form of fertilizer and pesticides, supported by expansion of irrigation projects and credit facilities, were the main pillars of green revolution. However, increased food production was associated with chemical inputs which carry great environmental cost including low soil fertility, groundwater contamination and human health hazard. Moreover, in continuation, there is a need for agriculture innovation to sustain the current food production under changing climate and increasing population. For this, a ‘renewed’ green revolution or bio-revolution is needed based on eco-friendly inputs with sustainability in production system. This bio-revolution could loosely base on

R. Mawar (*) Division of Plant Improvement & Pest Management, ICAR-Central Arid Zone Research Institute, Jodhpur, India e-mail: [email protected] B. L. Manjunatha · A. Sanyal ICAR-Central Arid Zone Research Institute, Jodhpur, India S. K. Sharma National Institute of Biotic Stress Management, Raipur, India H. B. Singh GLA University, Mathura, India S. C. Dubey Indian Council of Agricultural Research, New Delhi, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_16

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utilization of phyto-microbiome and improved climate smart cultivars. These microbial products are non-toxic and environment-friendly, and act as potential tools for plant growth promotion and disease control. Thus, the biological potential and fertility of soil could be increased, whereas the hazardous effects of agrochemicals could be decreased by employing microbial formulations to neutralize the agricultural crops. The great green revolution was possible because of free exchange of diverse germplasm among the countries; however, at present, there are strict provisions for accession of any kind of biological entities (plant/animal/microorganism) and their utilization. In current time, utilization of microorganisms for healthy crop growth is much needed in the form of commercial products, viz. nutrient supplier and disease and pest controlling agent (PGPM) to minimize the chemical load in the environment. Hence, India needs a clear, predefined regulatory mechanism to create a smooth path for commercialization of these PGPM products, with least technical footraces. The use of PGPM products becomes more relevant to the current period, as ‘natural farming’ is gaining momemtun worldwide including India for using natural component to produce food, feed and fibre. Thus, this chapter will discuss the current regulatory mechanisms associated with commercial production of PGPM-based products for managing seed, soil and plant health and the regulatory requirements for better adoption and diffusion in near future. India’s legislations to regulate production, distribution and quality of inputs used in agriculture (seeds, fertilizers, pesticides, etc.) were enacted and enforced around the 1950s and 1960s. Fertilizers are regulated through Fertilizers (Control) Order, 1957/1985 (FCO); Fertilizer (Movement Control) Order, 1960 (FMCO) and Essential Commodities Act (ECA) Allocation Order; Fertiliser (Inorganic, Organic or Mixed) (Control) Order, 1985; and the Fertiliser (Inorganic, Organic or Mixed) (Control) Amendment Order, 2021. Pesticides are regulated under the Insecticides Act, 1968, and Insecticides Rules, 1971. However, a lot of changes have occurred in the fertilizer and pesticide industry besides the enactment of legislations to regulate biofertilizer, biopesticide and biostimulant production.

2 Agricultural Biologicals/Plant Growth-Promoting Microorganisms (PGPM) 2.1

Biofertilizers

It refers to preparations of plant growth-promoting microorganisms containing nitrogen-fixing bacteria, phosphate-solubilizing bacteria and fungi, mycorrhizae, etc., used to solubilize/mobilize nutrients to improve plant nutrition and promote plant growth. Their roles include improving crop yields, crop nutrition, mitigating adverse effects of biotic and abiotic stresses, improving soil fertility, nutrient use efficiency, water use efficiency, quality traits and availability of nutrients in soil or rhizosphere (Tarafdar 2019).

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The Ministry of Agriculture, Government of India, brought biofertilizers and organic fertilizers under Fertilizer Control Order in 2006. The recent draft of Plant Bio-stimulants Order of Government of India includes microorganisms in the definition but does not list any of the ten microbial preparations currently classified as biofertilizers under the FCO. In the context of the FCO itself, considering the overall mechanism of their action into consideration, there is also a case for India to include some of the biopesticides (Pseudomonas, Bacillus, Trichoderma) into the FCO under biofertilizers much like what has been done in the USA and Canada for these organisms since they are also known to improve nutrient use efficiency (Reddy et al. 2021). In India, PGPM are categorized as ‘Biofertilizers’ when registered under fertilizer legislations and as ‘Biopesticides’ when registered and regulated under the plant protection category. In Europe and the USA, biofertilizers and some biopesticides are categorized as microbial plant biostimulants since they are more similar to fertilizing products than plant protection products. In addition to fertilizer, they optimize the use efficiency of the fertilizers and reducing the nutrient application rates, act on the plant’s metabolism or enrich the soil microbiome, increase plant production and improve soil health but differ from crop protection products because they do not have any direct actions against pests or diseases (Reddy et al. 2021). Microbial plant biostimulants in Europe are included under fertilizer regulations and specifically as a product stimulating plant nutrition processes independently of the product’s nutrient content with the sole aim of improving one or more of the following characteristics of the plant or the plant rhizosphere: (a) nutrient use efficiency, (b) tolerance to abiotic stress, (c) quality traits and (d) availability of confined nutrients in soil or rhizosphere. Biostimulants are however excluded from the scope of regulations on plant protection products (Reddy et al. 2021).

2.2

Biostimulants

The Farm Bill 2018 of USA describes biostimulants as ‘a substance or microorganism that, when applied to seeds, plants, or the rhizosphere, stimulates natural processes to enhance or benefit nutrient uptake, nutrient efficiency, tolerance to abiotic stress, or crop quality and yield’. Here microbial biostimulants broadly specify Rhizobium, PGPR, mycorrhizae, Trichoderma and other beneficial fungi. This brings within the ambit of microbial plant biostimulants organisms such as Trichoderma, Bacillus and Pseudomonas (allowed so long as a plant protection claim is not made on their product label). Biostimulants can also include much more complex ‘natural’ communities derived from organic matter processing. Biostimulants are regulated as microbial supplements in Canada under the Fertilizers Act. Many products offer both crop fertilization and crop protection traits. Under the current rules in Canada, manufacturers have to choose whether their product will be regulated through the Fertilizers Act or the Pest Control Products Act. Both properties of nutrient supplement and health control cannot be claimed on the same label.

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There is need to develop a process that would allow for dual registration on a single label. Azotobacter spp., mycorrhizal fungi, Rhizobium spp. and Azospirillum spp. are approved so far in the EU legislation on plant microbial biostimulants. Only these four organisms will be currently regulated, while more innovative products (e.g. consortia of microorganisms) are omitted, and manufacturers will not be allowed to market them. It is a serious restriction, and it may be noted that fortunately India has an approved NPK consortium in the FCO (Reddy et al. 2021). The list of microorganisms considered as plant biostimulants varies among the countries. Some include only biofertilizers, and some include biopesticides too with or without label claim. In India, the biofertilizers and biopesticides are distinctly defined and regulated. Further the understanding of biofertilizer and biopesticide definitions differs in different countries. The EU and USA defined them only by their physiological effects on plants and not on composition, whereas India defined them by their inherent functionality of microbes. In the recent Fertiliser (Inorganic, Organic or Mixed) (Control) Amendment Order, 2021, the Government of India defined biostimulant as a substance or microorganism or a combination of both whose primary function when applied to plants, seeds or rhizosphere is to stimulate physiological processes in plants and to enhance its nutrient uptake, growth, yield, nutrition efficiency, crop quality and tolerance to stress, regardless of its nutrient content, but does not include pesticides or plant growth regulators which are regulated under the Insecticide Act, 1968 (46 of 1968). They include botanical extracts, including seaweed extracts, biochemicals, protein hydrolysates and amino acids, vitamins, cell-free microbial products, antioxidants, anti-transpirants and humic and fulvic acid and their derivatives.

2.3

Biopesticides

In India, biopesticide is regulated under the Insecticides Act 1968. Any microbial strain developed or sold for pest and disease control should be registered with the Central Insecticide Board & Registration Committee (CIB & RC) of the MoA. Manufacturers of biopesticides can register their products temporarily or regularly under Section 9 (3) and 9 (3b). The temporary registration is less stringent than regular registration, thereby reducing commercial barriers for product development (Table 16.1).

3 Other Legislations Governing Biofertilizers and Biopesticides 3.1

Seed Legislations

Seed is a living entity containing adequate moisture and food reserve to sustain a new plant under suitable environmental conditions until it becomes

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Table 16.1 Brief overview of PGPM regulation in India Biofertilizers Rhizobia; Azotobacter; Azospirillum; P-solubilizing fungi; mycorrhiza; blue-green algae for rice; Acetobacter for sugarcane

Acts and rules (specific to products)

Insecticides Act 1968; Fertilizer (Control) Insecticides Rules 1971; Order, 1957/1985; FerPesticide Management tilizer (Movement ConBill 2008 trol) Order, 1960/1973; ECA Allocation Orders; FCO 2006/2009 The Essential Commodities Act, 1955; The Biodiversity Act, 2002; The Seeds Act 1966; The Bureau of Indian Standards Act 2016

Acts and rules (common to PGPR and other biologicals) Nodal ministry/ agency Role of central government

Role of state governments

Biopesticides Trichoderma, Pseudomonas, NPV, Bacillus; neem-based insecticides, Bacillus thuringiensis

Plant microbial biostimulants India: Specific microorganisms are not yet listed. Europe: Azotobacter spp., mycorrhizal fungi, Rhizobium spp. and Azospirillum spp. USA: Rhizobium, PGPR, mycorrhizae, Trichoderma, Bacillus, Pseudomonas, other beneficial fungi The Gazette of India Order dated 23 February 2021

Particulars Examples of technologies developed/ commercialized

Ministry of Agriculture

CIB&RC under MoA

(1) Enactment and amendment of Acts and Rules from time to time; (2) registration of new chemical/biofertilizers; (3) registration of industrial dealers; (4) ban/ restriction on use of registered products from time to time; (5) allocation orders Enforcement: (1) registration of manufacturers, importers and dealers; (2) production and distribution; (3) quality control (fertilizer inspector); (4) punitive actions for violation of provisions

(1) Enactment and amendment of Acts and Rules from time to time; (2) registration of new chemical/biopesticides; (3) ban/restriction on use of registered products from time to time

Enforcement: (1) registration of manufacturers, importers and dealers; (2) production and distribution; (3) quality control (insecticide inspector); (4) punitive actions for violation of provisions

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photosynthetically independent. PGPM products are being used as seed inoculants which need to be compatible with seed quality and marketing regulations for successful commercialization. India has the regulatory framework for PGPM products. However, their interface with seed regulation system is quite complex and dynamic. The production and marketing of seeds are regulated through Indian Seeds Act 1966 and Seed Rules 1968. Seed offered for sale should be packed according to Section 6 (b) in prescribed manner. Seed container has to be labelled as under Section (8), where the seed in container has been treated and the statement indicating that ‘the seed has been treated with the commonly accepted chemical or abbreviated chemical (generic) name of the applied substance’. However, in Seeds Act, the definition of ‘chemical’ does not include the existing definition of PGPM-based formulations, which needs to be included. Further, any disputes related to seed quality performance under field condition come under the jurisdiction of competent authority appointed under Section (12) of Seeds Control Order 1983, examining the matter related to seed only. However, it was reported that due to abiotic factors in the field conditions, seed germination may get affected under the influence of beneficial microorganisms (Pathak et al. 2013). Under these circumstances, there will be a confusion for farmers, whether they represent their concern to Appointed Authority under Seeds Control Order 1983 (Seed Inspector) or Statuary body of Consumer Protection Act 1986. Hence, there is a need for clarification from the regulatory authority dealing with PGPM-based products including biofertilizers and biopesticides. The New Policy on Seed Development (NPSD) came into force on October 1, 1988, with an objective to provide the Indian farmers with the best genetic material available anywhere in the world to increase agricultural productivity, farm income and export earnings. This policy was a result of a positive and progressive attitude of the government towards seeds. The policy aimed at liberalization of imports along with streamlining of plant quarantine procedures and encouragement to domestic seed industry through incentives.

3.2

The Biological Diversity Act, 2002

This act regulates the accession and use of biological material within India by domestic and foreign organizations and nationals, development of biological-based technologies/products and their patenting, commercialization, equitable sharing of benefits and licensing for commercial use in India and abroad. This act is enacted to provide accession and efficient utilization of biological materials (plant/animal/ microorganism) to develop technology/products from India and anywhere in the world with predefined regulatory mechanism. This act protects the interest of the environment and biodiversity conservation in the form of equitable sharing. The microorganism utilized for PGPM manufacturing must be registered under this act.

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The Bureau of Indian Standards Act 2016

This act regulates the quality of goods and products through standard conformity and quality assurance. The Bureau of Indian Standards is the national standards body for standards formulation and certification marking (Fig. 16.1).

Fig. 16.1 Regulation of PGPM at different stages of development and use in India

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4 Bottlenecks in Regulation and Promotion of Biofertilizers and Biopesticides 4.1

Relaxed Guidelines for Registration

FCO, though, regulates inorganic, organic or mixed; the emphasis so far was on chemical fertilizers. Similarly, the provisions of the Insecticide Act were to regulate chemical pesticides. However, the use of biofertilizers and biopesticides has increased in the country. The biofertilizers and biopesticides are treated at par with chemical fertilizers and chemical pesticides, respectively, for their regulation. The standards procedure for registration of the biofertilizers is same as that of chemical fertilizers. Similarly, the standards and procedure for registration of the biopesticides are same as that of chemical pesticides. Since biofertilizers and biopesticides are ecologically safer, there is a strong call for relaxed guidelines. Chronic toxicology tests should be exempted for these formulations to enable easy and speedy registration.

4.2

Efficacy

Biofertilizers and biopesticides contain living organisms. Hence, the storage, handling and use can significantly affect the count of live organisms (microbes) and affect their efficiency performance.

4.3

Availability and Choice

The production and use of biopesticides have increased in the country. However, the production is too low compared to chemical pesticides. The range of biopesticides for managing different pests in different crops is not easily available. Further, farmers are still sceptical about the efficacy of biopesticides especially under intensive and commercial cultivation of crops in irrigated conditions. Study undertaken at Sri Ganganagar district of Rajasthan reported that all the farmers engaged in commercial vegetable production used chemical pesticides for management of pests and diseases, whereas 80% disease suppression (Johansson et al. 2003). Ahmadzadeh et al. (2003) reported that antagonistic rhizobacteria, more specifically fluorescent Pseudomonas and certain Bacillus species, possessed the ability to control fungal and bacterial root diseases of agronomic crops. Seed treatment with Pseudomonas aeruginosa controlled Fusarium wilt and charcoal rot disease of chickpea in both greenhouse and field conditions (Saikia et al. 2004). Six isolates of fluorescent Pseudomonas obtained from pathogen-suppressive soil of a pigeon pea (Cajanus cajan) field were reported to have biocontrol potential against wilt disease complex in both laboratory and screen house (Siddiqui et al. 2005). Senthil et al. (2003) investigated the efficacy of talc-formulated plant growthpromoting rhizobacteria Pseudomonas spp. against red rot of sugarcane in endemic locations and found all of them to induce systemic resistance against the fungi in sugarcane plants. Pseudomonas fluorescens strains isolated from rhizosphere of rice, wheat, pigeon pea, groundnut, and chili crops produced extracellular siderophores which were antagonistic to fungal pathogens like Fusarium oxysporum, Alternaria sp., and Colletotrichum capsici (Suryakala et al. 2004). Pseudomonas fluorescens strain is a commercially available biological control agent used for the suppression of fire blight on pear and apple trees (Temple et al. 2004). Pseudomonas sp. showing significant inhibition of fungal pathogens, viz., Fusarium oxysporum, Macrophomina phaseolina, Fusarium udum, Fusarium solani, and

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Rhizoctonia solani, has been reported by Saikia et al. (2004). Out of 45 isolates of fluorescent Pseudomonas isolated from the rhizosphere of sunflower, 26 had antagonistic effects on the sclerotia of Sclerotium sclerotiorum (Behboudi et al. 2005). Fluorescent Pseudomonas were selectively isolated from black pepper (Piper nigrum) roots and screened for volatile and non-volatile metabolite production and inhibition of growth of Phytophthora capsici, the causal organism of foot rot disease. Among the isolates tested, the inhibition of Phytophthora capsici varied from 36.3 to 70.0% by non-volatile metabolites and from 2% to 23% by volatile metabolites. Fluorescent Pseudomonas was also known to benefit mushroom production by promoting formation of primordia and enhanced the development of the basidiome of Pleurotus ostreatus. Ajar Nath Yadav and Sayyed (2019) reported that 21 isolates of Pseudomonas fluorescens were isolated from the rhizosphere of rice, maize, wheat, chickpea, mung, urd, soybean, and sunflower from Raipur and Bastar regions. Among these, seven isolates which showed bright fluorescence under UV light were further tested. The isolates showed positive response of siderophore production and plant growthpromoting activity on rice cv. Bamleshwari. Among the isolates, PFR 1 and PFR 2 were found significantly superior to control in increasing the shoot length and root length. In vitro evaluation of the Pseudomonas fluorescens isolates also confirmed their antagonistic ability against both Pyricularia grisea and Rhizoctonia solani in dual culture tests (Akhtar et al. 2021). Pure culture of Pseudomonas aeruginosa was obtained from the soil and studied for siderophore production. The antifungal activity of the strain against three phytopathogenic fungi, viz., Fusarium moniliforme, Alternaria solani, and Helminthosporium halodes, was assayed by poison food technique. Inhibition of these fungal pathogens appeared to be due to production of antifungal secondary metabolites by Pseudomonas aeruginosa.

3.2

Inhibition of Bacterial Phytopathogens by Pseudomonas fluorescens

Fluorescent Pseudomonas is effective against bacterial pathogens also. It is known that the extent of inhibition zone formation is related to the ability of the organism to produce inhibitory metabolites against the test organism (Sivaprasad 2002). Manmeet and Thind evaluated in vitro antagonistic activity of Bacillus subtilis, Pseudomonas fluorescens, Trichoderma harzianum, and Penicillium notatum against Xanthomonas oryzae, the causal agent of bacterial blight of rice, and found Bacillus subtilis, Pseudomonas fluorescens, and Trichoderma harzianum to inhibit the pathogen. A foliar isolate of Pseudomonas putida was found to significantly reduce disease severity of bacterial spot caused by Xanthomonas axonopodis in sweet pepper under controlled conditions of growth chamber (Tsai et al. 2004).

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The fluorescent Pseudomonas strain has been reported to be suppressing the bacterial wilt of tomato caused by Ralstonia solanacearum (Alsulimani et al. 2021). Significant reduction in bacterial wilt disease incidence in tomato was obtained with Pseudomonas fluorescens. Among the three native in vitro efficient isolates of fluorescent Pseudomonas tested against Ralstonia solanacearum in chili and tomato under greenhouse conditions indicating the potential of native fluorescent Pseudomonas in suppressing bacterial wilt of tomato and chili. Yanqing et al. (2004) observed reduced infection of Ralstonia solanacearum in tomato plants treated with the nitrous oxide-overproducing transformants of fluorescent Pseudomonas as compared to its wild type, suggesting the possibility of increasing the level of nitrous oxide production through genetic modification of Pseudomonas as a new approach to enhance their biocontrol efficacy. The culture liquid of Pseudomonas fluorescens in a dilution of 1:9 is reported to control major cotton diseases caused by Xanthomonas campestris pv. malvacearum, Rhizoctonia solani, Fusarium vasectum, and Verticillium dahliae and also had the stimulating effect on seedling emergence and early growth and yield of cotton. Pseudomonas fluorescens reduced the incidence of Pseudomonas solanacearum by 50 percent in banana, 49 percent in brinjal, and 36 percent in tomato (Anuratha and Gnanamanickam 1990). Out of 41 strains of fluorescent Pseudomonas and Bacillus species tested as potential biological control agents against damping-off and root rot fungal diseases caused by Pythium ultimum in common bean (Phaseolus vulgaris), only two strains significantly increased the fresh weight of bean plants inoculated with Pythium ultimum under greenhouse condition (Ahmadzadeh et al. 2003).

4 Mechanism of Biocontrol by Pseudomonas fluorescens Fluorescent Pseudomonas fit into one of the three categories, viz., pathogens, biodegraders, and root colonizers or biocontrol agents. The last category exerts a protective effect on the roots through antagonism against phytopathogenic fungi and bacteria. Fluorescent Pseudomonas exhibit diverse mechanisms of biocontrol which include antibiosis, HCN production, siderophore production, competition for space and nutrients, and induced systemic resistance (ISR) (Fazeli Nasab and Sayyed 2019).

4.1

Cyanide Production

Cyanide ion is metabolized mainly to thiocyanate. The cyanide ion is exhaled as HCN and metabolized to lesser degree to other compounds. HCN inhibits the electron transport; thereby energy supply to the cells is disrupted leading to the

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death of the organism. It affects the proper functioning of the enzymes and natural receptors by reversible mechanisms of inhibition. It was also known to inhibit the action of cytochrome oxidase (Saranraj et al. 2021). Hydrocyanic acid (HCN) is produced by many rhizobacteria and is postulated to play a role in biological control of pathogens (Defago and Haas 1990). Voisard et al. (1989) presented evidence that HCN is involved in biological control by Pseudomonas fluorescens strain. Cyanide-producing strain Pseudomonas fluorescens stimulated root hair formation, indicating that the strain induced altered plant physiological activities. Keel et al. (1989) developed a disease assay for Thielaviopsis basicola on tobacco using iron-rich clays, which were conducive to biocontrol by strain Pseudomonas fluorescens. The Tn5-generated mutant strain Pseudomonas fluorescens, which lacked HCN production, gave significantly less control than Pseudomonas fluorescens. They opened two possible actions of HCN for the observed biocontrol, which include direct inhibition of Thielaviopsis basicola on roots, without damaging the plants, or inducing plant defense mechanisms (Supriya et al. 2021). Ramette et al. (2003) reported that hydrogen cyanide (HCN) is a broad-spectrum antimicrobial compound involved in biological control of root diseases by many plant-associated fluorescent Pseudomonas. Further, they noted that the enzyme HCN synthase is encoded by three biosynthetic genes (hen A, hen B, and hen C).

4.2

Siderophore-Mediated Biocontrol

Siderophores are low molecular weight ferric iron-chelating compounds that are secreted extracellularly under iron-limiting conditions and whose main function is to supply iron to the iron-starved cells. Some PGPR strains produce siderophores that bind Fe3+, making it less available to certain members of native microflora. The strains of rhizobacteria that produce siderophore under iron-limiting conditions in the rhizosphere chelate Fe3+, the form that is insoluble in water, hence not available to bacteria (Neilands 1981a, b; Leong 1986). Isolates belonging to Pseudomonas fluorescens were reported to produce extracellular siderophores when grown under iron deficiency. Instant golden yellow color is a positive test for siderophore production on succinate medium and casamino acid medium (Najafi et al. 2021). Most evidences to support the siderophore theory of biological control by rhizobacteria come from the work with pyoverdin, a class of siderophores that comprise the fluorescent pigment of fluorescent Pseudomonas (Demange et al. 1987). Loper (1988) suggested the role of siderophores in suppression of Pythium species and increased growth response of wheat by fluorescent Pseudomonas. Mutants of Pseudomonas fluorescens, deficient in siderophore production, showed reduced potential to control damping-off of cotton by Pythium ultimum than the parent strain (Bhaskar et al. 2021).

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Manwar et al. (2000) reported that the amount of siderophores produced by Pseudomonas fluorescens on different media were in the range of 50 to 57 (percent of siderophore units). Manwar et al. (2000) reported in vitro suppression of plant pathogens through siderophore production by fluorescent Pseudomonas. Kurek and Jaroszuk Scire (2003) reported that two Pseudomonas fluorescens strains (resistant to streptomycin and kanamycin) produced Fe3+-chelating compounds (including siderophores) and inhibited the in vitro growth of Fusarium culmorum (cycloheximide-resistant strain) strain by competition for Fe3+. They suggested that tri-hyobroxamate siderophores might be exploited as potent biocontrol compounds against plant pathogens as it has been reported that siderophores exerted maximum impact on Fusarium oxysporum than on Alternaria sp. and Colletotrichum capsici. Vinay et al. reported pyoverdin production by Pseudomonas aeruginosa that was able to increase the yield of barley, wheat, maize, cucumber, and spinach. However, Kloepper (1993) is of the opinion that siderophores are not always the prime mode of action for biological control by this group of bacteria.

4.3

Antibiosis

Antibiosis has been postulated to play an important role in disease suppression by rhizobacteria. The role of antimicrobial compounds in biocontrol has been studied by the generation of mutants that do not produce antibiotics. Pseudomonas fluorescens controls damping-off in cotton caused by Pythium ultimum, whereas one of its isogenic mutant deficient in the antifungal compound was significantly less effective in protecting cotton against Pythium ultimum (Moradzadeh et al. 2021). Phenazin-deficient mutants of Pseudomonas fluorescens failed to inhibit Gaeumannomyces graminis pv. tritici (Ggt) on media supportive of antibiotic production and were significantly less suppressive than the wild strain to take all of wheat (Thomashow and Weller 1988). Similarly, the antibiotic-minus mutant of Pseudomonas fluorescens exhibited reduced suppression of Gaeumannomyces graminis pv tritici (Ggt) in greenhouse experiments (Poplawsky et al. 1988). In field trials, the antifungal antibiotic-minus mutants of Pseudomonas fluorescens failed to control rice blast and sheath blight caused by Pyricularia sp. and Rhizoctonia solani, respectively (Chatterjee et al. 1996). Pseudomonas fluorescens effective against Pythium ultimum was reported to produce an antimicrobial metabolite which was missing in the mutant (Rajendran et al. 1998). Antimicrobial compounds produced by Pseudomonas cepacia were reported to inhibit the radial growth of some important soilborne pathogens, viz., Fusarium oxysporum, Macrophomina phaseolina, Sclerotium rolfsii, Rhizoctonia solani, and Pythium ultimum. An antifungal antibiotic isolated from the culture filtrate of Pseudomonas sp. was identified as N-butyl benzene sulfonamide. The ED50 values of the N-butyl benzene sulfonamide against Pythium ultimum, Phytophthora capsici,

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Rhizoctonia solani, and Botrytis cinerea were 73, 41, 33, and 102 ppm, respectively (Kim et al. 2000). Ahmadzadeh et al. (2003) reported that antimicrobial metabolites produced by antagonistic rhizobacteria play an important role in reducing most root diseases. Hydrogen cyanide, proteinase, siderophore, and some antibiotic compounds produced by fluorescent Pseudomonas have been identified and structurally characterized among which 2,4-diacetyl phloroglucinol is the most important antibiotic. The mutants of biocontrol strain of Serratia plymuthica deficient in pyrrolnitrin production, developed through replacement of GrrA, GrrS, and rpoS genes, were markedly less capable of suppressing Rhizoctonia solani and Pythium aphanidermatum under greenhouse condition (Ovadis et al. 2004). Haas and Defago (2005) reported that during root colonization, fluorescent Pseudomonas produce antifungal antibiotics, elicit induced systemic resistance in the host plant, or interfere specifically with fungal pathogenicity factors (Shahin Faridvand et al. 2021).

4.4

Competition for Infection Sites and Nutrition

The PGPR prevented deleterious rhizobacteria from colonizing sugar beet to their full potential, presumably because PGPR occupy and exclude deleterious rhizobacteria from the cortical cell junctions, where the exudation of the nutrient is maximal. Weller was of the opinion that Pseudomonas catabolized diverse nutrients and have a fast generation time in the root zone. Hence, they are projected as logical candidates for biocontrol by competition for nutrients, more so against slow-growing pathogenic fungi. Elad and Chet (1987) evaluated the antagonistic mechanisms of rhizobacteria that provided biocontrol against Pythium damping-off and noted that the competition for nutrients between germinating oospores of Pythium aphanidermatum and biocontrol rhizobacteria correlated significantly with disease suppression. The dynamics of sugar beet seed colonization by Pythium ultimum and rhizobacterial biocontrol agents was investigated by Osburn et al. (1989) who observed competition as the mechanism of biocontrol wherein the biocontrol agents protected the pericarp from occupation by the pathogen (Rasouli et al. 2020). Bell et al. (1990) studied the growth characteristics of five octopine-catabolizing Pseudomonas under octopine limitation in chemostats and their potential to compete with Agrobacterium tumefaciens. One of the Pseudomonas fluorescens strains was able to produce its peak population in the presence of octopine as nitrogen source. Competition models arrived at, based on pure culture parameters, and indicated that two of the Pseudomonas spp. dominated Agrobacterium tumefaciens when in simple competition for octopine as a limiting substrate. Mohamed and Caunter (1995) observed Pseudomonas fluorescens to inhibit Bipolaris maydis both in vitro and in vivo in infected maize plants but could not detect any inhibitory substances, assayed by a variety of methods, indicating nutrient competition as the operative component of antagonism.

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Induced Systemic Resistance (ISR)

Induced systemic resistance is broadly defined as activation of latent defense mechanisms in plants prior to pathogenic attack. The mechanism has been hypothesized in recent years to be an operable mechanism in several rhizobacterial systems. Induced systemic resistance is associated with increased synthesis of certain enzymes such as peroxidase, increased levels of certain acid-soluble proteins, and the accumulation of phytoalexins in the induced plant tissue. Fusarium wilt of carnation was significantly reduced by Pseudomonas sp. through the mechanism of increased accumulation of phytoalexins that signal the systemic resistance in bacterized plants compared with non-bacterized plants (Vanpeer et al. 1991). The seed bacterization of common bean with Pseudomonas fluorescens suppressed the halo blight caused by Pseudomonas syringae pv. phaseolicola through induced systemic resistance mechanism (Alstrom 1991). The O-antigenic side chain of lipopolysaccharides (LPS) of Pseudomonas fluorescens also has been shown to induce systemic resistance against Fusarium oxysporum in radish (Leeman et al. 1995). Pseudomonas fluorescens induced systemic resistance against Rhizoctonia solani causing sheath blight in rice with a twofold increased activity of pathogenesis-related peroxidase and chitinase proteins. Choong et al. (2004) reported that plant growth-promoting rhizobacteria in association with plant roots could trigger induced systemic resistance (ISR). Considering that low molecular weight volatile hormone analogues such as methyl jasmonate and methyl salicylate can trigger defense responses in Arabidopsis plants, the signaling pathway activated by volatiles from Bacillus subtilis is dependent on ethylene, albeit independent of the salicylic acid or jasmonic acid signaling pathways. Haas and Defago (2005) reported that fluorescent Pseudomonas during root colonization elicit induced systemic resistance in the host plant or interfere specifically with fungal pathogenicity factors.

5 Antagonistic Activity of Pseudomonas fluorescens Isolates Against Phytopathogens Plant growth-promoting rhizobacteria (PGPR) improves plant growth by preventing the proliferation of phytopathogens and thereby supports plant growth. Some PGPR synthesize antifungal antibiotics, e.g., Pseudomonas fluorescens produces 2,4-diacetyl phloroglucinol which inhibits growth of phytopathogenic fungi. Certain PGPR degrade fusaric acid produced by Fusarium sp., a causative agent of wilt, and thus prevents the pathogenesis (Sonawane et al. 2021). Some PGPR can also produce enzymes that can lyse fungal cells. For example, Pseudomonas stutzeri produces extracellular chitinase and laminarinase which lyses the mycelia of Fusarium solani. In recent years, Pseudomonas fluorescens has been suggested as potential biological control agent due to its ability to colonize

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rhizosphere and protect plants against a wide range of important agronomic fungal diseases such as black root rot of tobacco, root rot of pea, root rot of wheat, and damping-off of sugar beet and as the prospects of genetically manipulating the producer organisms to improve the efficacy of these biocontrol agents. A concern is shown on the use of Pseudomonas fluorescens in crop plants as the antifungal substances released by the bacterium, particularly 2,4-diacetyl phloroglucinol (DAPG), could affect the arbuscular mycorrhizal fungi (Kumar et al. 2002). Gaur et al. (2004) confirmed that DAPG-producing Pseudomonas recovered from wheat rhizosphere did not adversely affect arbuscular mycorrhizal colonization. However, given the toxicity of DAPG, such an inhibition may probably be dependent on the amounts released by the bacterium. Pseudomonas fluorescens exhibit strong antifungal activity against Pyricularia oryzae and Rhizoctonia solani mainly through the production of antifungal metabolites. One of the isolates of a Pseudomonas fluorescens was found to be strongly antagonistic to Rhizoctonia solani, a causal agent of damping-off of cotton. The Pyricularia oryzihabitans and Xanthomonas nematophila strains produce secondary metabolites and suppress Pythium and Rhizoctonia species which also cause damping-off of cotton (Ahmed et al. 2021). Pseudomonas fluorescens also exhibits strong antifungal activity against Rhizoctonia bataticola and Fusarium oxysporum found in rice and sugarcane rhizosphere, mainly through the production of antifungal metabolites (Kumar et al. 2002). Xanthomonas oryzae and Rhizoctonia solani—the bacterial leaf blight and sheath blight pathogens of rice (Oryza sativa)—are suppressed by indigenous Pseudomonas strains isolated from rhizosphere of rice cultivated in the coastal agri-ecosystem under both natural and saline soil conditions (Reddy et al. 2008). Isolates of Pseudomonas fluorescens from rice rhizosphere are also shown to exhibit strong antifungal activity against Pyricularia oryzae and Rhizoctonia solani mainly through the production of antifungal metabolites. Nearly, 50–60% of Pseudomonas fluorescens recovered from the rhizosphere and endorhizosphere of wheat grown in Indo-Gangetic plains are antagonistic towards Helminthosporium sativum (Manasa et al. 2021). Zadeh et al. (2008) worked to show the antagonistic potential of non-pathogenic rhizosphere isolates of Pseudomonas fluorescens in the biocontrol of Pseudomonas savastanoi which is the causative agent of olive knot disease. Pseudomonas corrugata, a form that grows at 4 °C under laboratory conditions, produces antifungals such as diacetyl phloroglucinol and phenazine compounds. Pseudomonas fluorescens suppresses black root rot of tobacco, a disease caused by the fungus Thielaviopsis basicola, and contributes in the biocontrol of Meloidogyne javanica, the root knot nematode, in situ (Siddiqui et al. 2005). In addition, certain soils are naturally suppressive to Thielaviopsis basicola-mediated black root rot of tobacco and Pseudomonas fluorescens populations producing the biocontrol compounds. Pseudomonas shows biocontrol potential against phytopathogenic fungi in in vivo and in vitro conditions from chickpea rhizosphere. Pseudomonas putida has potential for the biocontrol of root rot disease complex of chickpea by showing antifungal activity against Macrophomina phaseolina. It has also been showed that

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the anaerobic regulator ANR-mediated cyanogenesis contributes to the suppression of black root rot. Pseudomonas strains act as the effective candidates in suppressing Pseudomonas capsici in all seasons of plant growth as Pseudomonas fluorescens antagonizes all the reproductive phases of the Phytophthora capsici, the causal organism of foot rot disease (Paul and Sarma 2006). Some metabolites produced by Pseudomonas aeruginosa produce toxic volatile compound which reduces the growth of both Fusarium oxysporum and Helminthosporium sp., while Aspergillus niger is not affected (Hassanein et al. 2009). Bacillus luciferensis strain reduces Phytophthora blight of pepper by protecting infection courts through enhanced effective root colonization with protease production and an increase of soil microbial activity. Lima bean (Phaseolus lunatus L.) plants release hydrogen cyanide (HCN) in response to damage caused by natural enemies, thereby directly defending plant tissue. The bacteria Pseudomonas fluorescens showed biocontrol against the ciliated protozoa Tetrahymena pyriformis which feeds on it (Kim et al. 2009; Zakaria et al. 2019). Prasanna Reddy and Rao (2009) isolated plant growth-promoting rhizobacterial strains belonging to fluorescent Pseudomonas from the rhizosphere of rice. Among 30 strains that were confirmed as Pseudomonas fluorescens, 10 exhibited strong antifungal activity against Pyricularia oryzae and Rhizoctonia solani mainly through the production of antifungal metabolites (Nasab et al. 2021).

6 Changes in Enzymatic Activity of Plant Disease Induced systemic resistance (ISR) by Pseudomonas fluorescens is an additional mechanism by which the bacteria protect several crop plants against pest and diseases (Chen et al. 2000; Ramamoorthy et al. 2001). In tomato, seed treatment with Pseudomonas fluorescens resulted in ISR against Fusarium oxysporum by triggering the host to synthesize more phenolic substances (M’Piga et al. 1997). Seed treatment and soil application of Pseudomonas fluorescens isolate increased the accumulation of enzymes involved in phenyl propanoid pathway and pathogenesis-related protein (PR proteins) with response to Fusarium oxysporum causing wilt in tomato and Colletotrichum capsici causing fruit rot (Ramamoorthy et al. 2001). Induced resistance by Pseudomonas fluorescens has broad-spectrum activity against many fungal, bacterial, viral, and pathogenic species (Hoffland et al. 1996; Maurhofer et al. 1994; Wei et al. 1991; Zehnder et al., 2001). Pseudomonas fluorescens treatment has increased the plant vigor, height, and grain yield of wheat (Weller and Cook 1986). Mew and Rosales (1986) reported increased that the height of rice plant located whit Pseudomonas fluorescens then the control plants. Dileep Kumar and Dube (1991) reported significant increase in the emergence of tomato seedling when seeds were treated with Pseudomonas fluorescens

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appositive increase in the length of sunflower seedling by seed treatment with Pseudomonas fluorescens in 14 strains (Nithyapriya et al. 2021). Phenolic compounds may be fungi toxic in nature and increase the mechanical strength of the host cell wall. M’piga et al. (1997) reported that Pseudomonas fluorescens isolate induced the accumulation of phenolic in tomato. The hyphae of the pathogen surrounded by phenolic substances exhibited considerable morphological changes including cytoplasmic disorganization and loss of protoplasmic content. Accumulation of phenolic substances by prior application of Pseudomonas fluorescens in pea has been reported against Pythium ultimum and Fusarium oxysporum. Pseudomonas fluorescens isolate induced the accumulation of phenolic substances and PR-1 proteins in response to infection by Fusarium oxysporum in tomato (Ramamoorthy et al. 2001). Tuzun et al. (2001) described that constitutive accumulation of defense-related gene products was an integral part of both multigenic resistance and induced systemic resistance. In cucumber, rhizobacteria induced resistance against cucumber mosaic virus (CMV) and tomato mottle virus (ToMoV) (Samira Moradzadeh et al. 2021).

7 Crop Response to Pseudomonas Application of Pseudomonas fluorescens to seed resulted in yield increase in radish and potato (Kloepper and Schroth 1981). About 13 percent yield increase of sugar beet due to seed application of Pseudomonas fluorescens was reported. Increased height of rice plant with Pseudomonas fluorescens was observed (Mew and Rosales 1986). Enhanced growth of wheat plants inoculated with rhizobacteria, viz., Pseudomonas fluorescens, Pseudomonas aeruginosa, and Pseudomonas putida, was observed. Pseudomonas fluorescens treatment increased the number of heads and grain yield of wheat (Weller 2007). Increase in the emergence of tomato seedlings was observed when Pseudomonas fluorescens was applied to seeds. The inoculated seedlings showed a consistent and greater root length, shoot height, fresh weight, and dry weight than control (Kumar and Dube 1996). Gnanamanickam and Mew (1992) observed increase in the grain yields of rice due to seed treatment with Pseudomonas fluorescens. The length of safflower seedlings increased due to seed treatment with Pseudomonas fluorescens strain. Kumar and Dube (1996) reported that Pseudomonas fluorescens increased the yield of chickpea and soybean by 23.6 percent and 36.6 percent, respectively. Ishrat Izhar et al. (1999) observed the multiplication plant growth-promoting rhizobacteria Pseudomonas aeruginosa and evaluated for the control of root rot disease on sunflower (Joe Dailin et al. 2021). Radja Commare et al. (2002) reported that the application of talc formulation of Pseudomonas fluorescens strains through seed, root, soil, and foliar spray significantly reduced the incidence of sheath blight (62.1%) disease and leaf folder (56.1%) insect in rice, and it also increased the yield by 12–21%. Application of Pseudomonas fluorescens strains to black pepper rhizosphere resulted in easy mobilization of

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the essential nutrients in the rhizosphere and enhanced uptake of the same, which reflected in increased plant biomass. Pseudomonas fluorescens strain isolated from Lupinus hispanicus significantly enhanced all biometric parameters, viz., fresh weight, height, neck root diameter, and slender index (height/neck root diameter) in pepper seedlings (Garcia et al. 2003). Pseudomonas fluorescens inoculation significantly increased plant growth, dry matter production, and yield of tomato crop (Yan et al. 2003). Application of PGPR in tea plantations increased productivity without the use of additional chemical inputs. Efficacy of PGPR in plant growth promotion and biocontrol in cardamom was proved by Chakraborty et al. Lucy et al. (2004) reported that free-living plant growth-promoting rhizobacteria (PGPR) could be used to increase the plant growth. The addition of PGPR increased the germination rates, root growth, leaf area, chlorophyll content, magnesium content, nitrogen content, protein content, hydraulic activity, tolerance to drought, shoot and root weights, and delayed leaf senescence which reflected in higher grain yield. Pseudomonas inoculation significantly increases plant growth, dry matter production, and yield of Ashwagandha. Pseudomonas fluorescens enhanced biomass yield and ajmalicine production in Catharanthus roseus under water-deficit stress.

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Chapter 18

Symbiotic Effectiveness of Rhizobium Strains in Agriculture P. Saranraj, R Z Sayyed, P. Sivasakthivelan, M. Kokila, Abdel Rahman Mohammad Al-Tawaha, K. Amala, and Humaira Yasmin

1 Introduction Nitrogen is one of the major important nutrients essential for plant growth. The atmosphere contains about 1015 tonnes of nitrogen gas and the nitrogen cycle involves the transformation of some 3 × 109 tonnes nitrogen/year on the global basis (Fallah et al. 2021). Nitrogen fixations are not exclusively biological. Lightning probably accounts for about 10% of the world’s supply of fixed nitrogen. The fertiliser industry also provides very important quantities of chemically fixed nitrogen. World’s production of fixed nitrogen from dinitrogen for chemical fertiliser accounts for about 25% of earth’s newly fixed nitrogen and the biological process accounts for about 60%. The international emphasis on environmentally sustainable development with the use of renewable sources is likely to focus attention on the potential role of biological nitrogen fixation in supplying nitrogen for agriculture. Annually, biological nitrogen fixation is estimated to be around 175 million tonnes of which 79% is accounted by terrestrial fixation. Vegame-Rhizobium symbiotic

P. Saranraj (*) · M. Kokila · K. Amala Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, Tamil Nadu, India R. Z. Sayyed Division of Plant Imp & Pest Management, Central Arid Zone Research Institute, Jodhpur, India P. Sivasakthivelan Department of Agricultural Microbiology, Faculty of Agriculture, Annamalai University, Annamalai Nagar, Tamil Nadu, India A. R. M. Al-Tawaha Department of Biological Sciences, Al-Hussein Bin Talal University, Ma’an, Jordan H. Yasmin Department of Biosciences, COMSAT University, Islamabad, Pakistan © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_18

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association observed to fix 60–100 kg nitrogen ha-1 crop-1 (Baba Hamid et al. 2021). The environment has long been known to influence symbiotic nitrogen fixation. The delicate balance between the host plant and the symbiont is disturbed even by mildly adverse conditions that have no effect on plant growth supported by soil nitrogen. Salt stress is one of the major types of environmental stress adversely affecting legume production in arid and semi-arid regions, particularly because these plants depend on symbiotic nitrogen fixation for their nitrogen requirements (Saravanan et al. 2021). In recent history, cereals productivity has dramatically increased under high input system whilst legume yield has neared plateau, stagnated or even reduced. This has resulted in unbalanced cereal legume global production, and this in higher and unsustainable dependence on nitrogen chemical fertiliser inputs which reached $2 billion annually (Crouch et al. 2004). Increasing cultivation of legumes will be required to ameliorate environmental degradation, reduce depletion of non-renewable resources and provide adequate nitrogen for sustainable agriculture. Most of the new lands to be opened for legume cultivation in the developing countries are located in the dry desert areas (Rezapour et al. 2021). Symbiotic nitrogen fixation (SNF) by legumes plays major role in sustaining crop productivity of marginal lands and in small holder systems. Farmers in the dry areas depend on legumes as an important crop in their cropping systems due to the capacity of these plants to fix nitrogen from air by the interaction with nitrogen fixing Rhizobia. It is well known that nitrogen is abundant in the atmosphere, but plants cannot directly utilise the elemental nitrogen from the air (Patel et al. 2016a, b). Symbiotic nitrogen fixation occurs mainly through symbiotic association of legumes with nitrogen fixing Rhizobia that convert elemental biological nitrogen fixation (BNF) into ammonia. This type of biological nitrogen is therefore less costly and more sustainable as compared with nitrogen fertilisers for production of plant proteins. Scientific and technological progress has opened tremendous opportunities for the benefit of small farmers (Abdel Aal et al. 2004). The beneficial effects of Rhizobium inoculation to various leguminous crop plants have been investigated by several workers (Zope et al. 2016, 2019a, b; Shaikh et al. 2018; Sagar et al. 2020a, b; Arora et al. 2021). The beneficial effects of Rhizobium and Bradyrhizobium in legume in terms of biological N2 fixation has been a main focus in the past (Deshwal et al. 2003), as it is an important aspect of sustainable and eco-friendly food production and long-term productivity. It is the common observation that green gram crop nodulates. Poor nodulation may be due to various reasons such as: (a) unfavourable weather conditions like erratic and uncertain rainfall, low and high temperature and moisture stress at various crop growth stages; (b) Bradyrhizobial population below the threshold level; and (c) presence of ineffective native Rhizobial population. The specific interaction between Rhizobia and legume plants results in the most efficient form of biological nitrogen fixation, known as symbiotic nitrogen fixation, accounting for 60–80% of total fixed nitrogen in nature. The Rhizobium-host plant interaction leads to the formation of nodules, specialised structures generally found

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in roots, providing an ideal microenvironment to reduce gaseous nitrogen to ammonium. In this symbiotic interaction, the plant provides the carbon source for bacterial growth in exchange of the fixed nitrogen. The soil bacterium Rhizobium sp. established symbiotic nitrogen fixation specifically with groundnut and Bradyrhizobium japonicum establishes symbiotic nitrogen fixation specifically with soybean (Alberton et al. 2006; Soto et al. 2013). This rod-shaped Gram negative species produces abundant exopolysaccharides which display specific functions as carbon source and protective barriers at the initial colonisation steps during the bacterium-host plant interactions, increasing bacterial survival in the soil under adverse conditions. Two other Bradyrhizobium species, Bradyrhizobium elkanii and Bradyrhizobium liaoningense are capable to nodulate soybean. Bradyrhizobium japonicum shows a slow growth in culture and has been extensively used to produce liquid and solid bioinoculants for application in seeds before sowing (Jabborova et al. 2020a, b).

2 Rhizosphere Concept The rhizosphere is the zone of the soil surrounding living roots which is composed of soil particles and active communities of microorganisms (Werner 2001, 2004). Some bacterial species living in the rhizosphere can affect plant growth in either a positive or in a negative way (Seema et al. 2013; Suriani et al. 2020). Rhizosphere bacteria that favourably affect plant growth and yield of commercially important crops are known as plant growth promoting rhizobacteria (PGPR) (Imran Khan et al. 2020). In the rhizosphere, very important and intensive interactions are taking place between the plant, soil, microorganisms and soil microfauna and PGPR plays a major role in maintaining the soil ecosystem in the rhizosphere, rhizoplane and Phyllosphere that are ultimately beneficial to the plants (Sayyed et al. 2015). In fact, biochemical interactions and exchanges of signal molecules between plants and soil microorganisms have been described and reviewed by several authors. These beneficial bacteria are often referred as plant growth promoting bacteria (PGPB) or yield increasing bacteria (Wani et al. 2016; Sharma et al. 2016). Many microorganisms are attracted by nutrients exuded from plant roots and this is called Rhizosphere effect (Reshma et al. 2018). The rhizosphere and rhizoplane are colonised more intensively by microorganisms than the other region of the soil (Sayyed et al. 2019). Some of these microorganisms not only benefited from the nutrients secreted by the plant roots but also beneficially influence the plants, resulting in a stimulation of their growth (Jabborova et al. 2020a, b). For instance, rhizobacteria can fix atmospheric nitrogen, which is subsequently used by the plants; thereby improving plant growth in the soil deficient of nitrogen. Other rhizobacteria can directly promote the plant growth by the production of hormones (Jadhav et al. 2020a, b). Glick (1995) stated that the beneficial effects of these rhizobacteria may be due to their ability to produce various compounds including phytohormones, organic acids,

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siderophores, and fixation of atmospheric nitrogen, phosphate solubilisation, antibiotics and some other unidentified mechanisms. The mechanisms attributed for plant growth stimulation was mainly due to improved water and mineral uptake and production of biologically active substances, such as vitamins, amino acids, phytohormones and antibiotics. Plant growth promoting rhizobacteria (PGPR) is likely to be of great interest in sustainable crop production and have drawn much attention in recent years. The colonisation of roots by inoculated bacteria is an important step in the interaction between beneficial bacteria and the host plants. However, it is a complex phenomenon influenced by biotic and abiotic parameters (Jadhav et al. 2020a, b).

3 The Genus Rhizobium Rhizobium is a Gram negative, rod-shaped nitrogen fixing member and is a N2 fixing symbiont of soybean. Rhizobium strain was originally isolated from groundnut nodules in Florida, USA, in 1957 and has been widely used for the purpose of molecular genetics, physiology, and ecology, owing to its superior symbiotic nitrogen fixation activity with soybean, relative to other evaluated strains. The genome sequence of this strain has been determined; the bacterial genome is circular, 9.11 million bp long and contains approximately 8373 predicted genes, with an average Guanine and Cytosine content of 64.1% (Kaneko et al. 2002; Sagar et al. 2020a, b). Initially attached to the root-hair tips of soybean plants, Rhizobium colonise within the roots and are eventually localised within symbiosomes, surrounded by plant membrane. This symbiotic relationship provides a safe niche and a constant carbon source for the bacteria while the plant derives the benefits of bacterial nitrogen fixation, which allows for the use of readily available nitrogen for plant growth. Inoculation of soybean with Bradyrhizobium japonicum often increases seed yield (Ndakidemi et al. 2006; Sharma et al. 2020). Rhizobium synthesise a wide array of carbohydrates, such as lipopolysaccharides, capsular polysaccharides, exopolysaccharides (EPS), nodule polysaccharides, lipochitin oligosaccharides and cyclic glucans, all of which play a role in the biological nitrogen fixation symbiosis. Bacteria produce polysaccharide degrading enzymes, such as polygalacturonase and carboxy methyl cellulase, cleave glycosidic bonds of the host cell wall at areas where bacteria are concentrated, creating erosion pits in the epidermal layer of the roots, allowing the bacteria gain entry to the roots (Mateos et al. 2001; Ilyas et al. 2020). The energy source for Rhizobium is the sugar trehalose, which is taken up readily and converted to CO2 (Muller et al. 2001; Streeter and Gomez 2006; Sugawara et al. 2010; Kalam et al. 2020; Basu et al. 2021). On the other hand, UDP-glucose is taken up in large quantities but metabolised slowly, like sucrose and glucose. Promotion of plant growth causes more O2 to be released and more CO2 to be taken up (Mateos et al. 2001; Kaneko et al. 2002; Patel et al. 2018; Akhtar et al. 2021).

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4 Taxonomy of Rhizobium sp. Tong and Sadowsky (1994) developed a novel non-antibiotic containing medium which allows selective isolation of Bradyrhizobium japonicum and Bradyrhizobium elkanii strains from soils. The medium, BSJM, in based on the resistance of Bradyrhizobium japonicum and Bradyrhizobium elkanii to more than 40 μg of the metal ions Zn2 and CO2 per mL. BJSM does not allow the growth of Rhizobium sp. strains (Tables 18.1 and 18.2) (Hamid et al. 2021). Since 1984, two additional genera Sinorhizobium (fast growing green gram Rhizobia) and Azorhizobium (Stem nodule Rhizobia) and its species are added, and the details are presented in Table 18.3. It is now widely accepted that Rhizobium and Bradyrhizobium are distantly related. The current taxonomic classification of the Rhizobia is presented in Table 18.4.

Table 18.1 Taxonomic classification of Rhizobia according to Bergey’s MI of Systemic Bacteriology

Recognised genera Bradyrhizobium Rhizobium

Recognised species Bradyrhizobium japonicum Rhizobium leguminosarum Rhizobium leguminosarum bv trifoli Rhizobium leguminosarum bv phaseoli Rhizobium leguminosarum bv viciae Rhizobium meliloti Rhizobium loti

Table 18.2 Difference between slow-growing and fast-growing Rhizobia Character Generation time Carbohydrate nutrition Metabolic pathway

Flagellation Symbiotic gene location Nitrogen fixation Intrinsic antibiotic resistance

Fast growing 6 h Uses solely pentoses and hexoses EMP low activity ED main pathway TCA fully active Hexose cycle Sub polar Chromosome

nif H, nif D, nif K on same operon

nif H, nif D and nifA on separate operon High

Low

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Table 18.3 Recent taxonomic classification of Rhizobia Recognised genera Bradyrhizobium (Jordan 1982) Rhizobium (Jordan 1982)

Azorhizobium (Dreyfus et al. 1988) Sinorhizobium (Chen et al. 1988)

Recognised species Bradyrhizobium japonicum (Jordan 1982) Rhizobium leguminosarum (Jordan 1982) Rhizobium meliloti (Jordan 1982) Rhizobium loti (Jordan 1982) Rhizobium galgae (Lindstrom 1989) Rhizobium tropici (Martinez et al. 1991) Azorhizobium caulinodans (Dreyfus et al. 1988) Sinorhizobium fredii (Chen et al. 1988) Sinorhizobium xinjiangensis (Chen et al. 1988)

Table 18.4 Current taxonomic classification of Rhizobia Rhizobium species Rhizobium meliloti Rhizobium leguminosarum bv viciae Rhizobium leguminosarum bv trifoli Rhizobium leguminosarum bv phaseoli Rhizobium loti Rhizobium cicero Rhizobium tropici Rhizobium elti Rhizobium galegae Rhizobium fredii Bradyrhizobium japonicum Bradyrhizobium elkani Bradyrhizobium sp. strain Parasponia Azorhizobium caulinodans

Host plants Medicago, Melilotous and Trigonella spp. Pisum, Vicia, Lathrus and Lens spp. Trifolium spp. Phaseolus vulgaris Lotus spp. Cicer arietinum and tropical legumes Parasponia spp. (Non-legume) Phaseolus vulgaris, Leucaena spp. and Macroptilium spp. Phaseolus vulgaris Galega officinalis and Galega orientalis Glycine max, Glycine soja and other legumes Glycine max, Glycine soja and other legumes Glycine max, Glycine soja and other legumes Parasponia Sesbania spp. (Stem nodulating)

5 Diversity and Evolution of Rhizobium Communities Cropping history and past inoculation can have a significant impact on Rhizobium diversity in a soil (Kusale et al. 2021a, b). In a study of peanut nodulating Rhizobium in Cameroon, the highest diversity was found in sites with no history of peanut cultivation, suggesting that simply the introduction of a legume is capable of selecting for field presence of particular Rhizobium taxa (Nkot et al. 2008; Mothapo et al. 2013; Vafa et al. 2021). However, in soils after 18 years of cropping where only four strains of bacteria had been introduced, genetic diversity of soybean Rhizobium (Bradyrhizobium japonicum) was found to be much greater than these four strains.

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As these soils had previously had no native Rhizobium capable of nodulating soybean, this suggests rapid evolution in and adaptation to the harsh Cerradooxisols (Loureiro et al. 2007; Kusale et al. 2021a, b). Very little is known about native soil Rhizobium, especially about those nodulating soybeans. While evidence suggests that the Rhizobium community that typically nodulate promiscuous varieties are less efficient in terms of biological nitrogen fixation than those found in commercial inoculants, it is still unknown whether this can be improved. A vast amount of mutation and potential horizontal gene transfer can happen when inoculants are introduced into harsh tropical soil environments (Hungria et al. 2006; Barcellos et al. 2007; Nithyapriya et al. 2021). Various studies have shown that prior to soybean expansion in the 1960s, soils were devoid of Rhizobium capable of nodulating soybean (Loureiro et al. 2007), and inoculants used by farmers were primarily from the slow growing species (Bradyrhizobium japonicum and Bradyrhizobium elkanii). However, by the 2000s, isolates from soybean nodules were shown to be both slow and fast growing and classified phylogenetically as Rhizobium tropici, Rhizobium sp., Agrobacterium sp., as well as fast growing Bradyrhizobium japonicum and Bradyrhizobium elkanii indicating that either inoculants strains underwent mutations, allowing them to speed up their lifecycle, or horizontal gene transfer allowed native strains that previously were incapable of nodulating soybean to become capable or both (Hungria et al. 2006; Moradzadeh et al. 2021a, b).

6 Rhizobium Evolutionary Ecology The understanding of Rhizobium evolutionary ecology has been, until recently, complicated by the confounding of classification based on phylogenetic descent, with classification based on symbiotic partners. Historically, six species of Rhizobium, in one genus, Rhizobium, were recognised, and classification was based primarily on the host plant on which Rhizobium were able to form nodules, known as the ‘Cross inoculation’ concept. Over time this was abandoned due to wide overlap in host range, and in 1982, the first proposed classification was made based on physiological properties, with the proposal of the genera Bradyrhizobium representing slow growing acid intolerant bacteria (Jordan 1982; Young and Haukka 1996; Jabborova et al. 2021a, b, c). However, Jordan (1982) still suggests naming conventions within Bradyrhizobium to fall along host ranges with Bradyrhizobium japonicum representing soybean nodulating bacteria. However, DNA sequencing has made it possible to make distinctions based on gene structure and descent, allowing for more accurate speciation, and proposed phylogenies are continually being revised. For example, an early review in 1996 of phylogenies based on 16S sequences recognised 17 species in four genera (Young and Haukka 1996), ten while a more recent review by Graham (2009) indicates more than 50 species of nodule forming bacteria in 12 genera including both α- and β-proteobacteria (Kour et al. 2021).

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In recent years, speciation has become dependent on more than 16S sequences, with constitutive genes atpD, glnII and recA becoming increasingly important in understanding phylogeny (Vinuesa et al. 2008; Appunu et al. 2011; Su Fang et al. 2011; Khan et al. 2021). Recent work by several researchers, has demonstrated how symbiotic ecotypes can exist across multiple Rhizobium species and genera, as symbiotic regions of Rhizobium genomes have been shown to be mobile, conferring nodulation ability of the same host across multiple Rhizobium species (Silva et al. 2005; Vinuesa et al. 2005a, b; Hungria et al. 2006; Barcellos et al. 2007; Batista et al. 2007; Kapadia et al. 2021a, b).

7 Nitrogen Fixing Efficiency of Rhizobium Isolates Biological nitrogen fixation (BNF) is one of the most important phenomena occurring in nature, only exceeded by photosynthesis (Graham and Vance 2000). One of the most common limiting factors in plant growth is the availability of nitrogen. Although, 4/5th of earth’s atmosphere is comprised of nitrogen, the ability to utilise atmospheric nitrogen is restricted to a few groups of prokaryotes that are able to covert atmospheric nitrogen to ammonia and, in the case of the legume symbiosis, make some of this available to plants (Bastami et al. 2021). Groundnut and soybean have tremendous capacity for nitrogen fixation, and have thus been heavily promoted as a crop in low nitrogen settings. It was estimated that the soybean acquired up to 250 kg nitrogen ha-1, approximately 80% of the total tissue nitrogen through biological nitrogen fixation (Alves et al. 2003). In order for a legume crop to effectively add nitrogen to a cropping system, they must have appropriate Rhizobium partners. While native Rhizobium populations exist in most soils, it is difficult to predict whether there will be significant numbers capable of nodulating a particular host legume. The capacity for nitrogen fixation in differing Rhizobium sub-species or strains varies (Albareda et al. 2008). The issue is further complicated by the fact that many host legumes can be nodulated by multiple types of Rhizobium, and many Rhizobium types are capable of nodulating multiple host plant species (Sukmawati et al. 2021). In commercial agriculture, farmers will apply purchased inoculants, which tend to contain strains of Rhizobium that have been shown to effectively nodulate a legume crop and fix adequate amounts of nitrogen in controlled settings (Thies et al. 1992; Kapadia et al. 2021a, b). The amount of nitrogen accumulated in soybeans has been shown to correlate with inoculation rate of appropriate Rhizobium. However, in many regions, access to inoculants is limited, and farmers rely solely on native Rhizobium populations for legume nodulation and biological nitrogen fixation. If the population of soil Rhizobium is low, or if the existing population is unable to form nodules on a particular crop, little to no nitrogen fixation will take place. On the other hand, a large diverse Rhizobium population is likely to include Rhizobium capable of forming nodules on a wide range of legumes (Kahindi et al. 1997; Singh et al. 2021) and inoculant performance can vary according to competitiveness of indigenous

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populations and the encountered soil environment, with different strains of Rhizobium demonstrating differential competitiveness in their ability to form nodules as well in their ability to survive in various soil environments. If the native population is less efficient at nitrogen fixation than the inoculant, this can reduce overall nitrogen fixation and cause reduced growth and yield of the crop. Understanding background diversity of Rhizobium populations can provide for better use of inoculant strains, as well as improved nitrogen fixation of legumes (Bogino et al. 2008; Sarkar et al. 2021). Predominantly, members of the plant family Leguminosae have evolved with nitrogen fixing bacteria from the family Rhizobiaceae. In summary, the plants excrete specific chemical signals to attract the nitrogen fixing bacteria towards their roots. They also give the bacteria access to their roots, allowing them to colonise and reside in the root nodules, where the modified bacteria (Bacteroides) can perform nitrogen fixation (Sadowsky and Graham 1998; Graham and Vance 2003; Nayeri et al. 2021). This process is of great interest to scientists in general, and agriculture specifically, since this highly complex recognition and elicitation is coordinated through gene expression and cellular differentiation, followed by plant growth and development; it has the potential to minimise the use of artificial nitrogen fertilisers and pesticides in crop management. This biological nitrogen fixation process is complex, but has been best examined in some detail in the context of soybean-Bradyrhizobium plant-microbe interactions. Effectiveness of the symbiosis can be measured by two ways, either directly by determining the amount of nitrogen fixed or indirectly by measuring the plant dry weight. The methodology, characteristics and application of the sensitive ARA for measurement of N2 fixation rate by nitrogenase preparations and bacterial cultures in the laboratory and by legumes and free-living bacteria in situ were reported by Hardy et al. (1968). This assay was done based on the nitrogenase catalysed reduction of C2H2 to C2H4 and quantitative measurement of C2H4 using a gas chromatograph with flame ionisation detector (Selvamani et al. 2021). The effectiveness and competitive ability to Bradyrhizobium strains were studied by Narendrakumar et al. (1996). The nodulation, plant biomass, nitrogen uptake and grain yields of inoculated plants were significantly higher in loamy soils than alluvial sandy soils. Thakare et al. (1997) tested out of 39 isolates of soybean Bradyrhizobium screened, 24 isolates increased nodulation significantly over control. The symbiosis of hup+ and huphr and hup- strains of Bradyrhizobium elkanii in cowpea cultivars were studied by Souza (1999). Nitrogenase activity, haemoglobin content and nitrogen fixation are more in hup- and huphr inoculated cultivars than hup- strains inoculated plants (Jabborova et al. 2021a, b, c). The effects of lectins from soybean on the symbiotic activity of Bradyrhizobium japonicum strain was investigated by Kirichenko and Malichenko (2000) pre-incubation with lectins isolated from the specific host plant resulted in both enhancement of nodulation and stimulation of the nitrogen fixing activity of fully developed nodules but the lectin isolated from the non-specific host plant had no such effect (Jabborova et al. 2021a, b, c).

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Shaikh et al. (2021) conducted a pot culture experiment in soybean (Glycine max L.) to assess acetylene reduction activity at different stages of the plant growth and concluded that the ARA activity was maximum between flowering to early pod filling stage. Wych and Rains (1979) analysed the ARA of soybean cultivar Amsoy71 at different stages of growth. In their study, maximum acetylene reduction activity observed at early pod filling stage and thereafter is decreased. Alsulimani et al. (2021) listed the following characteristics as most desirable for the selection of effective strain: 1. Ability to form N2 fixing nodule over the range of environmental conditions 2. Competitiveness in nodule formation and survival in the presence of another Rhizobium 3. Prompt nodulation and good nitrogen fixation 4. Persistence in the soil and good growth ability in the culture medium, in the carrier and in the soil. Nodulation of soybean by effective Rhizobium results in substantial, amount of nitrogen being fixed by the symbiosis (Bhaskar et al. 2021) Bradyrhizobium japonicum Bacteroides were isolated anaerobically and were supplied with 14C-labelled trehalose, sucrose UDP-glucose, glucose or fructose under low O2 (2%) in the gas phase. The overall results support the view that, although Bacteroides metabolise sugars the rates are very low and are inadequate to support nitrogenase. The nitrogenase activity under water-logged condition in soybean inoculated with Bradyrhizobium japonicum was studied by Sung (1993). After 4 days of inoculation, the ARA was 104 μmol (C2H2 g-1 dw h-1 and 80 μmol C2H4 g-1 dw h-1 under waterlogged conditions. The normally grown plants of Vicia fabae (Vidal et al. 1992; Moradzadeh et al. 2021a, b) and Phaseolus sp. (Jamro et al. 1994; Rahimi et al. 2021) showed maximum nitrogenease activity of flowering stage and declined after pod filing. Nitrogenase activity was positively correlated with nodule number during this stage of both Vicia and Phaseolus plants. In soybean, a strong correlation existed between leghaemoglobin content, nitrogenase activity and ureide concentration in Xylem sap (Dakora and Felix 1995; Faridvand et al. 2021). The effectiveness and competitive ability to Bradyrhizobium strains were studied by Narendrakumar et al. (1996). The nodulation, plant biomass, N uptake and grain yields of inoculated plants were significantly higher in loamy soils than alluvial sandy soils. Thakare et al. (1997) tested out of 39 isolates of soybean Bradyrhizobium screened, 24 isolates increased nodulation significantly over control. The symbiosis of hup+ and huphr and hup- strains of Bradyrhizobium elkanii in cowpea cultivars were studied by Souza (1999). Nitrogenase activity, haemoglobin content and nitrogen fixation are more in hup- and huphr inoculated cultivars than hup- strains inoculated plants. The effects of lectins from soybean on the symbiotic activity of Bradyrhizobium japonicum strain was investigated by Kirichenko and Malichenko (2000) preincubation with lectins isolated from the specific host plant resulted in both enhancement of nodulation and stimulation of the nitrogen fixing activity of fully developed nodules but the lectin isolated from the non-specific host plant had no such effect.

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8 Exopolysaccharides Production by Rhizobium Exopolysaccharides (EPS) can either be homopolysaccharides or heteropolysaccharides. Cellulose is one of the important homopolysaccharides produced by plant associated bacteria such as Rhizobium and Agrobacterium (Manasa et al. 2021) whereas leaves is produced by Erwinia and Pseudomonas (Najafi et al. 2021). Sutherland et al. (1990) defined exopolysaccharides are polysaccharides found external to the structural surface of the microbial cell and the term can be applied to carbohydrate polymers of diverse composition and of different physical types. Several Rhizobial polysaccharides were found to be effective stabilising agents of most soils than either the synthetic soil conditioner or the other reference compounds. The exopolysaccharides, cellular polysaccharides and extracellular protein of Rhizobium have been identified as the root curling factor (Shaikh et al. 2016). The strains of Bradyrhizobium are diverse in their composition often varying from strain to strain (Patel et al. 2016a, b). The studies on the chemical composition of the polysaccharides of Rhizobium and Bradyrhizobium by chemical, physico-chemical and immunological methods have shown that the Rhizobium strain produce homopolysaccharides (Jadhav et al. 2017). Rhizobium meliloti SU47 can produce two EPS, a succinoglycon (EPS I) and a galacto glucan (EPS II). Most physiological and genetical studies have been performed with derivatives of this strain, which under normal growth conditions produced only EPS I (Khan and Sayyed 2019). The strains of Bradyrhizobium are diverse in their composition often varying from strain to strain (Nath Yadav and Sayyed 2019). The studies on the chemical composition of the polysaccharides of Rhizobium and Bradyrhizobium by chemical, physico-chemical and immunological methods have shown that the Rhizobium strain produce homopolysaccharides (Fazeli Nasab and Sayyed 2019). Rhizobium meliloti can produce two exopolysaccharides (EPS), a succinoglycon (EPS I) and a galactoglucan (EPS II). Most physiological and genetical studies have been performed with derivatives of this strain, which under normal growth conditions produced only EPS I (Kour and Sayyed 2019). Galactoglucan is produced under phosphate limitation conditions. Zope et al. (2019a, b) have fractioned a low molecular weight succino glycan of Rhizobium meliloti repeat unit monomers, trimers and tetramers. Each class has a varying degree of anionic character. Rasouli et al. (2020) reported that the polysaccharides of Bradyrhizobium japonicum are a bacterial product and not a plant product. Two types of polysaccharides are formed corresponding to the two DNA— homologues groups of Bradyrhizobium japonicum. The polysaccharide produced in nodules (NPS) is different in composition from that produced in culture (EPS). Bacterial polysaccharides are necessary for a functional Rhizobium legume symbiosis. exopolysaccharide (EPS), lipopolysaccharide (LPS), capsular polysaccharides and cyclic β (1-2) glucon play essential role in the formation of the infection thread and in nodule development (Enshasy et al. 2020). The exopolysaccharide production by Rhizobium meliloti is influenced by salt. The halotolerent strain

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Rhizobium meliloti EFB 1 modifies the production of EPS in response to salt. This bacterium grown in the presence of 0.3 M NaCl showed decrease in mucoidy and when grown in salt supplemented liquid medium this organism produced 40% less exopolysaccharides (Sonawane et al. 2021). The cell surface carbohydrates of bacteria within the Rhizobiaceae family provide important functions during legume nodulation. Rhizobial Lipopolysaccharides which have been shown to elicit root hair deformation cortical cell division and nodule organogenesis (Ahmed et al. 2021). Genetic studies have also provided evidence that a second class of Rhizobial cell surface carbohydrate, the exopolysaccharide is required for nodule development in plant (Nasab et al. 2021). Joe Dailin et al. (2021) reported a third class of Rhizobial cell surface carbohydrate, the cyclic β-glucans within the Glycine max root nodules Rhizobial cell surface carbohydrate, the exopolysaccharides, is required for nodule development in plants.

9 Indole Acetic Acid Production by Rhizobium Naturally occurring substances with indole nucleus possessing growth-promoting activity are referred to as auxins, chemically it is indole acetic acid (IAA). Not only plants but also microorganisms can synthesise auxins and cytokinins. The ability to synthesise phytohormones is widely distributed among plant-associated bacteria. Averagely, 80% of the bacteria isolated from plant rhizosphere produce IAA (Sahasrabudhe 2011). Sridevi and Mallaiah (2007) Rhizobium isolates from root (Sesbania procumbens) and stem nodules (Sesbania rostrata and Sesbania procumbens) of Sesbania species were shown to produce indole-3-acetic acid (IAA) in culture supplemented with L-tryptophan. Among the three isolates, maximum amount of IAA was produced by the Rhizobium isolate from Sesbania procumbens. The IAA from this isolate was extracted, purified and identified by Thin Layer Chromatography. Kumari et al. (2009) isolated Rhizobium strains from root nodules of five species of Indigofera viz., Indigofera trita, Indigofera linnaei, Indigofera astragalina, Indigofera parviflora and Indigofera viscosa on Yeast Extract Mannitol Agar (YEMA) medium. The strains were examined for production of acid, exopolysaccharide (EPS) and indole acetic acid (IAA) by utilising ten different carbon sources. Zakaria et al. (2019) suggested that the production of IAA by Rhizobium in the rhizosphere is regulated by legumes through their root exudates. The phenolic acids viz., protocatecheic acid, 8-hydroxy cinnamic acid and vanellic acid caused more growth and indole acetic acid in all three Rhizobial strains isolated from groundnut, black gram and green gram. Ferulic acid showed a slight increase in the growth and IAA production whereas quercetin and gallic acid showed inhibitory effect on both growth and IAA production of three Rhizobial strains tested. Indole acetic acid

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production by Rhizobium sp. in vitro was increased by the various levels of potassium.

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Siderophore Production by Rhizobium

Iron containing protein figures prominently in the nitrogen fixing symbiotic bacteria (i.e. Azorhizobium, Rhizobium and Bradyrhizobium) and their respective plant hosts for the synthesis of iron containing compounds such as nitrogenase, leghaemoglobin, ferridoxin, hydrogenase and cytochromes, symbiotic bacteria must require an adequate supply of iron. Availability of iron is reduced to precipitation, forming oxyhydroxide polymers of Fe(OH)3. Therefore, to compete successfully for iron, organism has evolved specific, high affinity mechanism to acquire iron. In symbiotic bacteria, these systems are composed to ferric specific ligands (siderophores) and their cognate membrane receptors (Saranraj et al. 2021). Wani et al. (2016) reported that cowpea Rhizobium produced catechol like siderophore at the rate of 6.2 mg L-1 of culture filtrate and further indicated that glycine and threonine were detected in the siderophore. Maximum siderophore production was observed at 36 h of growth in cowpea Rhizobium. Overproduction of siderophore occurs in bacteria and fungi under acute iron starvation. Siderophores dissolve the complex form of ferric ion chelated in the highly insoluble oxyhydroxides. Seema Sharma et al. (2016) reported that in Escherichia coli iron transport was regulated by a repressor protein, which bound to the ferrous ion. Cowpea Rhizobium produced catechol like siderophore, which decreased with increase in the concentration of Molybdenum (above 1 mM) and presence of iron increased the molybdenum uptake but 2,3-dihydroxy benzoic acid did not show any increase in the uptake there by confirming that entire siderophore molecule was required for the transport of molybdenum. Reshma et al. (2018) reported that cowpea Rhizobium produced catechol like siderophore at the rate of 6.2 mg L-1 of culture filtrate and further indicated that glycine and threonine were detected in the siderophore. Maximum siderophore production was observed at 36 h of growth in cowpea Rhizobium. Shaikh et al. (2018) developed a Monoclonal antibodies to ferric Pseudobactin (siderophore of Pseudomonas putida) to determine the concentration and localisation of siderophore in the rhizosphere. Patel et al. (2018) inferred that Rhizobium sp. utilised catechol up to 10 mM as sole carbon source (synthetic medium) and survived for 9 months in soil containing catechol and further inferred that in the presence of organic acids and sugars catechol was co-metabolised. Zope et al. (2019a, b) studied the uptake and metabolism of iron in Rhizobium legume symbiosis and detected that production and utilisation of siderophore affected rhizosphere and in bulk soil. Sayyed et al. (2019) developed 1021 defective in siderophore production to study their role in legume symbiosis and reported that siderophores increased the ability to fix nitrogen and resulted in an increase in plant growth.

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Studies on differential siderophore utilisation and iron uptake by soil and rhizosphere bacteria used ferrioxamine B as the sole Fe source in Fe deficient medium, while about 12%, 10%, 2% and more than 1%, respectively (TNSK2 SK3 and WCS S58), were able to use ferric chrome and Pseudobactions (Sagar et al. 2020a, b). Introduction of transposon Tn5 (km-1) in to a siderophore production Chinese Rhizobium fredii resulted in mutants of overproducing siderophore. Bradyrhizobium japonicum utilised hydroxamate type Siderophore, i.e. Ferric citrate and Rhodotortalate under iron starving conditions. In addition to this, they also used Pyoverdin type siderophore. Nodule occupancy in greenhouse experiment by these two mutants were 3% and 4% compared to 19% by wild strain proving that overproduction of Siderophore resulted in less competitive strains (Saranraj et al. 2022). Eighty-four microbial isolates were screened for their ability to produce Siderophores using four chemical assays. The siderophore-producing Penicillium chrysogenum and Pseudomonas aeruginosa significantly enhanced nodulation and nitrogen fixation of Mung bean compared to plants infected with Bradyrhizobium strain alone.

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Leghaemoglobin Content of Nodules

Leghaemoglobin, a myoglobin like pigment is an essential component for nitrogen fixation by leguminous nodules but its role is indirect since nitrogen fixation accomplished by isolated Bacteroides devoid of LB2. The relationship among the three factors was found to be positive and significant in both the plants. Not for general plants growth and development by abolishing symbiotic Leghaemoglobin synthesis in nodules of the model legume Lotus japonicus. Jadhav et al. (2020a, b) reported the natural relationship among Bacteroides Leghaemoglobin and di-nitrogen content of Egyptian clover (Trifolium alexandriunum and Gram Cicer arietinum) at different age levels. The relationship among the three factors was found to be positive and significant in both the plants. In general, the indole extracts different for their absorption spectra, leghaemoglobin and iron content. The leghaemoglobin content varied from 7.54 to 13.08 mg g-1 fresh weight and from 39.08 to 71.15 mg g-1 on dry weight basis. Symbiotic leghaemoglobin are crucial for nitrogen fixation in legume root nodules but not for general plants growth and development by abolishing symbiotic leghaemoglobin synthesis in nodules of the model legume Lotus japonicus.

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Antibiotic Resistance of Rhizobium

The effectiveness of antibiotics was lost frequently in Rhizobium sp. and the colonies are resistant to Kanamycin and Polymycin while Streptomycin resistant strains were stable in effectiveness. Streptomycin resistant mutants did not differ from the

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commercial Streptomycin sensitive strains in their ability to fix nitrogen, competition for nodulation and ability to grow in the rhizosphere. The lupine nodule bacteria Rhizobium lupini acquired resistance to Streptomycin when the antibiotic concentration in the media was gradually increased. The acquired property was well retained in the medium without Streptomycin (Suriani et al. 2020). Mourad et al. (2009) used six Rhizobium strains isolated from Algerian soil was checked for their antimicrobial activity against Pseudomonas savastanoi, the agent responsible for olive knot disease. Rhizobium sp. was found to produce antimicrobial activities against Pseudomonas savastanoi. The antimicrobial activity produced by Rhizobium sp. was perceptible with ammonium sulfate, between 1000 and 10,000 kDa molecular weight, heat resistant but sensitive to proteases and detergents. These characteristics suggest the bacteriocin nature of the antimicrobial substance produced by Rhizobium sp., named Rhizobiocin. In contrast, the antimicrobial activity produced by Rhizobium sp. was not perceptible with Ammonium sulfate. It was smaller than 1000 kDa molecular weight, heat labile, and protease and detergent resistant. These characteristics could indicate the relationship between the antimicrobial substance produced by Rhizobium sp. and the ‘small’ bacteriocins described in other Rhizobia. Seema et al. (2013) developed 1000 ppm Streptomycin resistant mutant from an efficient parent strain Rhizobium sp. Streptomycin mutant (Str+) showed better in vitro growth, polysaccharide production and competence for nodulation in both sterilised as well as normal soil. Sayyed et al. (2015) employed the variation in the intrinsic resistance of Rhizobium strains to antibiotic as a tool in differentiating 26 strains of Rhizobium leguminosarum. Patel et al. (2016a, b) first surveyed this type of resistance pattern in 48 strains of Bradyrhizobium japonicum and found over 60% of the strains were resistant to Chloroamphenicol, Polymyxin-B and erythromycin and 47% were resistant to Neomycin and Penicillin G. Wani et al. (2016) reported that the TGnstr and NEgstr strains showed poor saprophytic competence compared to native Rhizobia even the parent strains were efficient. Rhizobium phaseoli was resistant to high concentrations of streptomycin up to 200 μg mL-1. Vinay et al. (2016) investigated the intrinsic antibiotic resistance pattern among Rhizobium and Bradyrhizobium strains of different species and found that the trait could be a reliable tool for identifying strains in field collected nodules to provide standard inoculum size for application. Reshma et al. (2018) studied the correlation between colony morphology (wet and dry type) and intrinsic antibiotic resistance and found that the population as a whole was resistant to Gentamycin but varied in their resistance to Streptomycin, Rifampicin, Kanamycin and Penicillin. The strains with the same pattern of resistance had the same morphology. Streptomycin, Rifampicin and Penicillin were more effective against dry Rhizobia than they were against wet ones. Jabborova et al. (2020a, b) used intrinsic antibiotic resistance to characterise 83 isolates from nodules of cowpea and field bean. Fingerprint patterns of isolates revealed considerable heterogenicity amongst the populations. Whereas slow growing Rhizobia from Vigna unguiculata nodules were generally more resistant to the

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concentrations of antibiotics used. The reports revealed that, resistance to high levels of antibiotics by mutants might be associated with reduced symbiotic effectiveness decreased infectiveness and lower competitive ability. Jadhav et al. (2020a, b) studied the intrinsic antibiotic resistance and effect of curing treatments on plasmid pattern, loss of antibiotic resistance and symbiotic characters of slow and fast-growing Rhizobium strains nodulating green gram, black gram, cowpea, pigeonpea, mothbean, and cluster bean. Most of the slow growers were resistant to tetracycline, Viomycin, Polymycin and Rifampicin (50 μg mL-1) and fast growers showed resistant to Kanamycin, Ampicillin, Chloromphenicol and Streptomycin (750 μg mL-1) when these strains were cured by Acridine orange (25 μg mL-1) or Ethidium bromide (40 μg mL-1) continuously along with incubation at 40 °C yielded clones sensitive to 2–3 antibiotics and ineffective nodulation in strains of green gram. Khan et al. (2020) found that there are three serogroups and 18 plasmid profile groups out of 192 isolates of Rhizobium leguminosarum. Further cluster analysis of intrinsic antibiotic resistance data showed that individual clusters were dominated by one serogroup and by one or two plasmid profile groups. Plasmid profile analysis and IAR analysis grouped 72% of the isolates similar.

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Chemotactic Activity of Legume Root Exudates

Plant root exudates interact with the root nodule bacteria in different ways. Some of these compounds are known to induce nodulation (nod) genes in Rhizobium. Chemotaxis of bacteria was reported by several workers. Chemotaxis of Rhizobium towards root exudates was noticed by Sharma et al. (2020). Extracts and exudates from nodulated root systems were different from those in system without Rhizobium nodules. Ilyas et al. (2020) reported that chemotoxis and mobility have been found to make important contributions to the symbiotic interactions of Rhizobium with its host. Rhizobia have been attracted by very low concentrations of excreted compounds such as flavonoids that may have low nutritional value. Both Rhizobium and Bradyrhizobium are attracted by aminoacids, dicarboxylic acids and sugars present in the root exudates. Kalam et al. (2020) reported that soyabean plant root exudates contain sugars such as sucrose, galactose, arabinose, the organic acids such as malic acid, malonic acid, citric acid and the aminoacid such as alanine, arginine, histidine, threonine, tyrosine and valine. The chemotaxis of Bradyrhizobium japonicum towards organic acids and green gram seed exudates. Green gram exudates were strong bacterial chemoattractant, and the effect decreased when dilution increased. Organic acids showed weak effects on the micro symbiont attraction. Pigeon pea exudates not only increased the nitrogenase activity and exopolysaccharide synthesis of the microsymbiont but also induced it to synthesise the root hair deformation factor (nod factor). Basu et al. (2021) found out the chemotaxis of Rhizobium towards Cajanus cajan root exudates and its major

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components. The chemotactic response of Rhizobium sp., a slow growing Cajanus cajan isolate towards its host root exudates was examined, two classes of mutants, one non-chemotactic towards nutrients (aminoacids and sugars) and signal compounds like flavonoids and other mutant non-chemotatic towards aminoacids and sugars but positive towards naringenin.

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Thermotolerance of Rhizobium

High temperature adversely affected the survival, persistence of pigeon pea Rhizobia, competition, rhizospheric colonisation, root exudation, chemotaxis, growth of Rhizobia and hydrolytic enzyme production (Khan et al. 2020). Hamid et al. (2021) identified that room temperature between 37 and 40 °C is critical for nitrogen fixation by nodulated guar and that the critical temperature for guar dependent on mineral nitrogen was above 40 °C. The bean variety Kentwood failed to nodulate at 10 °C and took 32 days to initial nodulation at 12 °C, while cultivar Aurora nodulated in 23 days and 21 days at 10 °C and 12 °C, respectively. Akhtar et al. (2021) reported that high soil temperature prevalent in tropical soils is a major constraint for biological nitrogen fixation by legume crops. Pigeon pea nodulates poorly in northern region of India due to high temperature in summer. Soybean (Glycine Max L.) is able to nodulate and fix nitrogen when roots are continuously exposed to 33 °C but not at 37 °C. Higher inoculation rates may be required at higher temperature to maintain the nodulation in soybean. Protection of Rhizobia against thermal inactivation was obtained by alginate or clay amendments. Kusale et al. (2021a, b) reported the occurrence of heat shock proteins in Rhizobium. The Rhizobium cells entrapped in alginate beads survived more than 180 days at 28 °C. Longer storage times reduced the inoculum survival, grain yield and Rhizobial population in green gram. Arora et al. (2021) studied that the optimum temperature of growth for seven strains of pigeon pea (Cajanus cajan) was 30 °C and for five strains 44 °C.

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Salt and Drought Tolerance of Rhizobium

Severe environmental conditions are limiting factors to the growth and activity of the nitrogen fixing plants. The behaviour of some nitrogen fixing systems under severe environmental conditions (0.1%, 0.5%, 1.0%, 1.5%, 2.0%, 2.5% and 3.0%) such as salt stress, salt stress, acidity, alkalinity, nutrient deficiency, fertiliser, heavy metals, and pesticides were reviewed (Zahran 1999). These major stress factors suppress the growth and symbiotic characteristics most Rhizobia (Duzan et al. 2004). Therefore, isolation of Rhizobia strains capable to tolerate these stresses is essential for efficient nitrogen fixation (El-Halim et al. 2001). The occurrence of Rhizobial populations in desert soil and the effective nodulation of legumes growing therein emphasise the

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fact that Rhizobia can exist in soils with limiting moisture levels, however, population densities tend to be lowest under the most desolated conditions and to increase as the moisture stress in released (Abdel-Salam et al. 2002). Water deficit, simulated with polyethelene glycol, significantly reduced infection thread formation and nodulation of Vicia faba plants. A favouable rhizosphere environment is vital to legume–Rhizobium interaction; however, the magnitude of the stress effects and the rate of inhibition of the symbiosis usually depend on the phase of growth and development, as well as the severity of the stress. For example, mild water stress reduces only the number of nodules formed on roots of soybean, while moderate and severe water stress reduces both the number and size of the nodules (Diouf et al. 2007). The legumes grown under arid and semiarid lands require drought tolerant Rhizobia to form effective symbiosis. Rhizobia with survival ability, which showed effective symbiotic characteristics with their host legumes in desert soils and arid regions were identified. Essendoubi et al. (2007) evaluated the nodulation of soybean by a salt-tolerant Rhizobium strain and a salt-sensitive Bradyrhizobium strain in saline soil in the glasshouse. No significant differences in shoot and root dry weight, nodule number and nodule weight between the salt-tolerant Rhizobium strain and the salt-sensitive Bradyrhizobium strain were found. Nodulation of soybean was reduced more than 50% by the equivalent of 34.2 mM NaCl in soil. The specific activity of nodules formed by both strains was also reduced by salinity. Wild legumes (herb or tree) are widely distributed in arid regions and actively contribute to soil fertility in these environments. The N2 fixing activity and tolerance to drastic conditions may be higher in wild legumes than in crop legumes. The wild legumes in arid zones harbour diverse and promiscuous Rhizobia in their root— nodules. Specificity existed only in few Rhizobia from wild legumes, however, the majority of them are with wide host range (Zahran 1999). Frioni et al. (2001) isolated and characterised 61 Rhizobial isolates from eight species of native legume plants. The strains were isolated from nodules with high nitrogenase activity, and their growth rate, antibiotic, salinity and acidity resistances were determined. Their relationships were analysed building a matrix with the resistance characteristics. Most of the isolates were fast growers and acid-producing with high level of exopolysaccharides. In general, isolates were erythromycin resistant but sensitive to Rifampicin. All the isolates grew well at pH 5.5 while 75% did so at pH 4.4. More than 60% of the isolates grew in 2% of NaCl but this declined to 21% of the isolates in 3% NaCl. This population showed high antibiotic, salinity and pH resistance, suggesting adaptability to major ecological environment stresses, and great saprophytic competence within soil environments. Misra and Dwivedi (2003) responses of two green gram (Phaseolus aureus) cultivars differing in salt tolerance ability were compared for seed germination efficiency, seedling vigor (root and shoot length), plant growth (dry weight and fresh weight), water uptake and intracellular Na+/K+ contents during germination under the conditions of absence as well as presence of various levels of salinity. Bolaños et al. (2003) developed nodules of Pisum sativum after inoculated with Rhizobium leguminosarum and growing under saline conditions (75 mmol/L NaCl)

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are non-functional and had abnormal structure. The infected cells contained a low number of endophytic bacteria, compared to treatments without salt. Addition of Boron (up to 55.8 nmol/L) and Calcium ions (up to 2.72 mmol/L) increased bacterial population of host plant cells in salt-stressed nodules. Furthermore, symbiosomes developed inside the nodules from salt treated plants presented a degraded peribacteroid membrane. Aurag et al. (2004) studied the effect of salt stress on the Rhizobium-common bean symbiosis. The comparison of the behaviour of five cultivars of Phaseotus vulgaris differing in seed colour, growing on nitrates and different concentrations of NaCl, showed genotypic variation with respect to salt tolerance. Common bean plants inoculated with salt-tolerant Rhizobium tropici wild-type strain formed a more active symbiosis than did its decreased salt-tolerance (DST) mutant derivatives (HB8, HB10, HB12 and HB13). The mutants formed partially effective (HB10, HB12) or almost ineffective (HB8, HB 13) nodules (Fixd) under non-saline conditions. The DST mutant formed nodules that accumulated more proline than did the wild-type nodules, while soluble sugars were accumulated mainly in ineffective nodules (Tejera et al. 2004). Misra and Gupta (2005) reported the effect of salt stress on free proline accumulation, activities of pyrroline-5-carboxylate reductase, proline oxidase and glutamyl kinase, glycinebetaine levels and chlorophyll contents in two cultivars of green gram (salt tolerant and salt sensitive) under the conditions of absence as well as in the presence of various levels of salinity. Salt stress resulted in a significant accumulation of free proline in shoots of both the cultivars of green gram. The magnitude of increase in free proline accumulation was higher in the tolerant cultivar than in the sensitive cultivate. Todd et al. (2006) suggested warm season nitrogen fixing legumes move fixed nitrogen from the nodules to the aerial portions of the plant primarily in the form of ureides, allantoin and allantoate, oxidation products of Purines synthesised de novo in the nodule. Improved understanding of ureide biochemistry includes two ‘additional’ enzymatic steps in the conversion of uric acid to allantoin in the nodule and the mechanism of allantoin and allantoate breakdown in leaf tissue. There are several reports of genetically modified Rhizobial strains being more efficient in biological nitrogen fixation (BNF) under optimal condition compared to their parental strains. Suarez et al. (2008) reported that improvement of salt tolerance and grain yield in common bean by over expression of trehalose-6-phosphate synthase in Rhizobia. This strongly suggests that leaf ureides are not involved in the early stages of biological nitrogen fixation inhibition under salt, although a role in the later stages of a more severe salt (Serraj et al. 2001) cannot be discounted. Manivasagaperumal et al. (2011) studied the influence of copper on growth, dry matter yield and nutrient content of green gram (Vigna radiata L.) on a glass house earthen pot experiment. Copper was applied to the soil in the form of copper sulphate in different concentrations (0, 50, 100, 150, 200 and 250 mg kg-1) in which the green gram plants were grown. The plant samples were analysed 45 days after sowing. The results indicated that low level of copper concentrations (50 mg kg1 ) showed a significant increase in the overall growth, dry matter yield and nutrient

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content, while higher concentrations (100–250 mg kg-1) decreased the growth, dry matter production and nutrient content of green gram. Rahman et al. (2011) proposed that the salinity increase has been one of the major problems for traditional agricultural practices in coastal Bangladesh for several decades, but very few studies have been conducted on effects of salinity on agrobiodiversity in this area. Their study investigated the salinity effects on agrobiodiversity in rice (Oryza sativa L). Vegetables, and fruit trees in three coastal, rural villages; Putia (Satkhira district), Srifaltala (Bagerhat district) and Hogolbunia (Khulna district). Information was collected by participatory rural appraisal methods including transect walks, group discussions and key informant interviews. Uyanoz and Karaca (2011) conducted a study to determine the effect of salinity on Rhizobium and growth of dry bean. A commercial cultivar (Akman 98) of dry bean (Phaseolus vulgaris L.) was inoculated with Rhizobium tropici strain and native Rhizobium in solution culture with different salt concentrations (control, 5, 10, 20 and 40 mmol-1) added before inoculation. The plant root and shoot dry weight, chlorophyll content, plant height, root length, total nitrogen, symbiotic efficient and efficient rate were affected by salt stress in tested plant and both inoculations. Soil salinity is caused by natural or human induced process and considered to be a major environmental hazard. Nearly 20% of all irrigated land in India was salt affected and this proportion tends to increase in spite of considerable efforts dedicated to land reclamation. This requires careful monitoring of the soil salinity status and the variation to the curb degradation trends and secure sustainable land use and management. The Nagapattinam district of Tamil Nadu, India was affected by salinity, the situation became worse after Tsunami salinity level has increased that makes portable water unutilisable and change in cropping pattern even at some places saltpans are available for extracting salt by salt industry (Rekha et al. 2011).

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Nitrogen Fixation in Legumes

Legume plants have adopted different strategies for assimilating and transporting the fixed nitrogen. Allantoin and Allantoic acid were the major forms of organic nitrogen translocated from the nodules and ureides were stored and assimilated mainly in the shoot. Vafa et al. (2021) reported that xylem sap ureide analysis is a convenient means to account for nitrogen derived by biological nitrogen fixation. This experiment with soybean cultivar Daris under greenhouse conditions showed that, acetylene treatments to inhibit nitrogen fixation drastically reduced ureide content in xylem sap. This was clear identification that xylem sap ureides could be used as an indicator of nitrogen fixation. A linear relationship between nodulated roots and shoot axis with respect to their ureide concentration reported by Kusale et al. (2021a, b). There was an inverse relationship between nitrate and ureide contents in the different plant parts in both nodulating and non-nodulating soybean cultivars. There was an inverse relationship

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between nitrate and uride contents in the different plant parts in both nodulating and non-nodulating green gram cultivars. The nitrogenase activity was negatively correlated with NO3 content of plant. The nitrogenase activity of Greengram var. Bragg peaked at 60 DAS, which was positively correlated with the concentration of ureides. The ureide concentration was maximum at R2–R3 stages in all cultivars and gave a positive correlation with a grain yield of green gram cultivars. Nithyapriya et al. (2021) conducted the green house trails and determined the ureide content at three growth stages in leaves and stems of green gram and bean. In both cases, the ureide content was higher in stem and decreased with an increasing age. Kour et al. (2021) proposed that ureides assay method has been found to be suitable for green gram to assess nitrogen fixation in wide range of genotypes. Their results confirmed that the relative abundance of ureides was closely related to the nitrogen derived from symbiotic nitrogen fixation at vegetative and reproductive stages. Khan et al. (2021) screened eight wild cultivars of green gram for their nitrogenase activity and ureide content at different stages of growth. The ureide content in the stem was positively correlated with the nitrogenase activity.

17

Mutagenesis and Mutants of Rhizobium

The chemical mutagen EMS was most effective mutagen in inducing auxotrophy in Rhizobium trifolii. But the frequency of reversion was reported to be high in the derived mutants (Jones et al. 1981). Maier and Brill (1969) reported that a strain of Rhizobium japonicum was mutagenised using chemical mutagen N-methyl-N-nitroN-nitrosoguanidine (NTG). By a rapid effective assay, the mutants were screened in soybean plants. It was found that two mutant strains nodulated earlier than the wild type, in addition, more root nodules were reported than that of wild type. Similarly, using NTG, effective and non-effective mutants were derived from the Rhizobium (Williams and De Mallorca 1983). In certain Rhizobium–plant combinations auxotrophy in the bacterial partner is associated with specific blocks in symbiosis. One metabolic group, which is apparently important, is purines, particularly adenine. In Rhizobium leguminosarum purine auxotrophs lost the ability to nodulate pea plant and all their prototrophic revertants were Nod+. Ari auxotroph with a double growth requirement (adenine) was found to be defective in nodule development. Indole Acetic Acid (IAA) deficient mutants T10, T27 and TNB were isolated from Bradyrhizobium elkanii by Spontaneous and or N-methyl-N-nitro-NNitrosoguanidine (NTG) mutagenesis. Inoculation with these mutants significantly reduced the nodule number of soybean roots when compared to that of the parent strain. Furthermore, exogenous IAA application restored the nodule number of soybeans inoculated with TN3 to the original level (Fukuhara et al. 1994). Aird et al. (1991) reported that exo loci required for exopolysaccharide synthesis in Agrobacterium radiobacter by employing mutagenesis with Nitrosoguanidine.

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Effect of Rhizobium Bioinoculant on Agricultural Crops

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The influence of five Thai soybean cultivars on nodulation competitiveness of four Bradyrhizobium japonicum strains was investigated by Payakapong et al. (2003). At harvest, nodule occupancy by each strain was determined by fluorescent antibody technique. Nodulation competitiveness of the Bradyrhizobium japonicum strains was affected by the cultivars of soybean used. Appunu et al. (2011) reviewed the following characters of Rhizobium to be used as inoculant for pulses and they revealed their following characters. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10.

Ability to form nodules and fix nitrogen Ability to compete Ability to fix nitrogen at different environmental range Ability to grow in the artificial media Ability to persist in soil for long time Ability to migrate Ability to colonise in the soil Genetic stability Compatibility Ability to colonise in rhizosphere soil

Appunu et al. (2011) studied the symbiotic interactive effect of different Bradyrhizobium japonicum strains with six soybean cultivars. Plants inoculated with Bradyrhizobium japonicum strain produced higher plant dry matter accumulation and seed yield over all other cultivars.

18.1

Nodulation and Biomass

The effect of pre-exposure of soybean roots to Rhizobium japonicum strains and subsequent establishment of other strains in the nodules were investigated by using combination of effective strains and ineffective strains. When either of the two less competitive strains was inoculated into 2 days old seedling, their nodule occupancy increased significantly on both cultivars. These results indicate that the early events in the nodulation process of soybeans are the most critical for competition among Rhizobium japonicum strains. Kapadia et al. (2021a, b) reported that the inoculation of Rhizobium increased the grain yield, dry matter accumulation, nodulation (both number and weight) and nitrogen content of soybean plants. High doses of nitrogen reduced nodulation. The nodulation ability nodule dry weight, plant dry weight and seed yields increased and nitrogen status of soil improved with increasing inoculation load. The number and dry weight of nodules were not correlated with seed yield or soil nitrogen status (Sarkar et al. 2021). Selvamani et al. (2021) reported that inoculation with Bradyrhizobium japonicum increased nodule mass significantly in soybean.

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Shaikh et al. (2021) reported that soil inoculation with Bradyrhizobium japonicum resulted in more nodules, more uniform distribution on the root and greater nitrogen fixation. Baba Hamid et al. (2021) reported the effect of Bradyrhizobium inoculation on biomass and nodulation cowpea. Cowpea seeds inoculated with Rhizobium strains increased nodulation, fodder yield and seed yield.

18.2

Yield Components

Seeds of soybean plants were inoculated with antibiotic mutants of the Bradyrhizobium strains. Increased shoot dry weight, percentage nitrogen, total nitrogen and seed yield were a result of increased nodulation by the effective and competitive inoculant Bradyrhizobium strains. The results showed that there was high potential for increasing growth and seed yield of promiscuous soybean cultivar by inoculation with foreign Bradyrhizobium strains (Okereke et al. 2000). Seed inoculation of Bradyrhizobium increased the number of pods plant-1, number of grain pod-1 and 1000 seed weight in soybean (Manasa et al. 2021). Rahimi et al. (2021) reported that Bradyrhizobium japonicum seed inoculation increased the soybean seed yield by 11.8% over uninoculated control and improved fertility status of soil. Inoculation of green gram with Bradyrhizobium japonicum increased seed yields by 25–41% with no significant differences between seed and soil inoculation (Rezapour et al. 2021). Inoculation with Bradyrhizobium japonicum strains yielded 3.08 tonnes ha-1 while the commercial strain inoculated and uninoculated green gram control yielded 2.87 + ha-1 and 1.96 tonnes ha-1, respectively. The cell load of Bradyrhizobium japonicum in commercial inoculants on green gram seed yield possessed positive correlation with nodule number, mass and seed yield and recorded 19% yield increase when inoculum load from 105 to 106 cells/seed (Saravanan et al. 2021). The cell load of Bradyrhizobium japonicum in commercial inoculants on soybean seed yield possessed positive correlation with nodule number, mass and seed yield and recorded 19% yield increase when inoculum load from 105 to 106 cells/seed (Shaikh et al. 2016). Seed inoculation of Bradyrhizobium increased number of pods plant-1, number of grain pod-1 and 1000 seed weight in green gram (Najafi et al. 2021). Genistein, the most effective plant to bacterium signal in the soybean (Glycine max L.) nitrogen fixation symbiosis, was used to pre-treat Bradyrhizobium japonicum. The results of these experiments indicated that Genistein—pre-incubated Bradyrhizobium increased the grain yield and protein yield, the later maturing of the two cultivars tested. Genistein without Bradyrhizobium japonicum, applied onto seeds in the furrow at the time of planting also increased both grain and protein yield by stimulation of native soil Bradyrhizobium japonicum. Interactions existed between Genistein application and soybean cultivars, and indicated that the cultivar

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with the greatest yield potential responded more to Genistein addition (Fallah et al. 2021). Mendes et al. (2003) concluded that the Bradyrhizobium inoculation has successfully replaced the use of nitrogen fertiliser on green gram crops. Nitrogen rates promoted reductions of up to 50% in the nodule number at 15 days after the emergence. Regardless of the management system, these reductions disappeared at the flowering stage and there was no effect of nitrogen rates on either the number or dry weight of nodules or on green gram yields. Egamberdiyeva et al. (2004) reported the effect of Bradyrhizobium spp. strains on dry matter yield, nodulation and seed yield of soybean varieties grown in nitrogen deficient soil in pot and field experiments. They noticed the significant effects on growth, nodule number and yield of soybean were obtained after inoculation with Bradyrhizobium spp. strains. Meghvansi et al. (2005) isolated three different pH tolerant strains of Bradyrhizobium japonicum and investigated their efficiency were determined under the mist conditions in the sterilised sandy soil at pH 8.4. Maximum and minimum nodulation and vegetative growth were observed in Bradyrhizobium japonicum inoculated soybean plants respectively. Three pH tolerant strains could also pose better results in the efficiency determination experiments. Rhizobia form root nodules that fix nitrogen in symbiotic legumes, extending the ability of these bacteria to fix nitrogen in non-legumes such as cereals would be useful technology for increased crop yields. El-Shaarawi et al. (2011) stated that inoculation with Bradyrhizobium japonicum tended to compensate the adverse effect of applying lower doses of mineral nitrogen. The combinations between the inoculant and the lower doses tended to enhance most growth and yield characters compared to the lower doses applied alone. The beneficial effect of Bradyrhizobium japonicum on total dry weight of shoots and pods and seed yield was increased by decreasing the applied level of mineral nitrogen, reached the maximum with the lowest rate. The combination between 20 kg MN/fed with the higher rate of Bradyrhizobium japonicum induced the highest increase in seed yield/fed over that of the highest rate of mineral nitrogen alone in the two successive seasons, respectively. Agraw (2012) conducted an experiment to study the effects of co-inoculation of Bradyrhizobium japonicum and Phosphate solubilising bacteria (PSB) (Pseudomonas spp.), and conventional farmers’ fertiliser level (combined and individual application of 46 N kg ha-1 and 46 P2O5 kg ha-1) on nodulation, seed yield and yield components of green gram (Glycine max L.). Analyses of variance indicated that most of the parameters measured were significantly ( p > 0.05) affected by the treatments. Accordingly, dual inoculation with Bradyrhizobium japonicum and Pseudomonas sp. significantly increased plant height at harvest, number of nodules per plant, nodule volume per plant, nodule fresh weight per plant, and shoot height at late flowering and early pod setting compared to the other treatments.

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Kusale SP, Attar YC, Sayyed RZ, Malek RA, Ilyas N, Suriani NL, Khan N, El Enshasy H (2021a) Production of plant beneficial and antioxidants metabolites by Klebsiella variicola under salinity stress. Molecules 26:1894 Kusale SP, Attar YC, Sayyed RZ, El Enshasy H, Hanapi SZ, Ilyas N, Elgorban AM, Bahkali AH, Marraiki N (2021b) Inoculation of Klebsiella variicola alleviated slat stress salinity and improved growth and nutrients in wheat and maize. Agronomy 11:927–935 Lindstrom K (1989) Rhizobium galgae. A new species of legume root nodule bacteria hit. J Syst Bacteriol 39:365–367 Loureiro MDF, Kaschuk G, Alberton O, Hungria M (2007) Soybean (Glycine max (L.) merrill) Rhizobial diversity in Brazilian oxisols under various soil, cropping, and inoculation managements. Biol Fertil Soils 43:665–674 Maier R, Brill W (1969) Ureide metabolism in castor beans. Evidence for a particle bound allantoinase. Phytochemistry 8:401–404 Manasa M, Ravinder P, Gopalakrishnan S, Srinivas V, Sayyed RZ, Enshasy HE, Yahayu M, Zuan ATK, Kassem HS, Hameeda B (2021) Co-inoculation of Bacillus spp. for growth promotion and iron fortification in sorghum. Sustainability 13:12091 Manivasagaperumal R, Vijayarengan P, Balamurugan S, Thiyagarajan G (2011) Effect of copper on growth, dry matter yield and nutrient content of Vigna radiata (L.) Wilczek. J Phytol 3(3):53–62 Martinez E, Segovia L, Mercante FM (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucauna sp. trees. Int J Syst Bacteriol 41:4171–4186 Mateos PF, Baker DL, Petersen M, Velazquez E, Jimenez Zurdo JI, Martínez Molina E, Squartini A, Orgambide G, Hubbell DH, Dazzo FB (2001) Erosion of root epidermal cell walls by Rhizobium polysaccharide-degrading enzymes as related to primary host infection in the Rhizobium - legume symbiosis. Can J Microbiol 47:475–487 Meghvansi MK, Prasad K, Nandha SK (2005) Identification of pH tolerant Bradyrhizobium japonicum strains and their symbiosis effectiveness in soybean (Glycine max (L.) Merr.) in low nutrient soil. Plant Physiol 34:420–430 Mendes IC, Hungria M, Camo RJ (2003) Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol Fertil Soils 39:88– 93 Misra N, Dwivedi UN (2003) Genotypic difference in salinity tolerance of green gram cultivars. Plant Sci 166:1135–1142 Misra N, Gupta AK (2005) Effect of slat stress on proline Metabolism In two high yielding genotypes of green gram. Plant Sci 169:331–339 Moradzadeh S, Moghaddam SS, Rahimi A, Pourakbar L, Enshasy HAE, Sayyed RZ (2021a) Bio-chemical fertilizer improves the oil yield, fatty acid compositions, and macro-nutrient contents in Nigella sativa L. Horticulturae 7:345–350 Moradzadeh S, Siavash S, Moghaddam O, Rahimi A, Pourakbar L, Sayyed RZ (2021b) Combined biochemical fertilizers, ameliorate agrobiochemical attributes of black cumin (Nigella sativa L.). Sci Rep 11:11399 Mothapo NV, Grossman JM, Maul JE, Shi W, Isleib T (2013) Genetic diversity of resident soil Rhizobia isolated from nodules of distinct hairy vetch (Vicia villosa Roth) genotypes. Appl Soil Ecol 64:201–213 Mourad K, Fadhila K, Chahinez M, Meriem R, Lajudie Philippe D, Abdelkader B (2009) Antimicrobial activities of Rhizobium sp. strains against Pseudomonas savastanoi, the agent responsible for the olive knot disease in Algeria. Grasas y Aceites 60:139–146 Muller J, Boller T, Wiemken A (2001) Trehalose becomes the most abundant non-structural carbohydrate during senescence of soybean nodules. J Exp Bot 52(358):943–947 Najafi S, Nasi HN, Tuncturk R, Tuncturk M, Sayyed RZ, Mirnia RA (2021) Biofertilizer application enhances drought stress tolerance and alters the antioxidant enzymes in medicinal pumpkin (Cucurbita pepo convar. pepo var. Styriaca). Horticulturae 7:588–596 Narendrakumar R, Pareek P, Singh TA (1996) Effectiveness and competitive ability of Bradyrhizobium strains. J Ind Soc Soil Sci 44:246–249

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Sagar A, Riyazuddin R, Shukla PK, Ramteke PW, Sayyed RZ (2020a) Heavy metal stress tolerance in Enterobacter sp. PR14 is mediated by plasmid. Indian J Exp Biol 58(2):115–121 Sagar, Sayyed RZ, Ramteke PW, Sharma S, Marraiki N, Abdallah M, Elgorban AS (2020b) ACC deaminase and antioxidant enzymes producing halophilic Enterobacter sp. PR14 promotes the growth of rice and millets under salinity stress. Physiol Mol Biol Plants 26:1847–1854 Sahasrabudhe MM (2011) Screening of rhizobia for indole acetic acid production. Annu Biol Res 2(4):460–468 Saranraj P, Sayyed RZ, Sivasakthivelan P, Devi MD, Tawaha ARMA, Sivasakthi S (2021) Microbial biosurfactants sources, classification, properties and mechanism of interaction. In: Sayyed RZ, Enshasy HE, Hameeda B (eds) Biosurfactants: production and applications, vol I. CRC Press - Taylor & Francis Group, Boca Raton, FL, pp 243–265 Saranraj P, Sivasakthivelan P, Hamzah KJ, Hasan MS, Sayyed RZ, Tawaha ARMA (2022) Microbial fermentation technology for biosurfactants production. In: Sayyed RZ, Enshasy HE (eds) Biosurfactants: production and applications in food and agriculture, vol II. CRC Press Taylor & Francis Group, Boca Raton, FL Saravanan R, Nakkeeran S, Sarayna S, Senthilraja C, Renukadevi P, Krishnamoorthy AS, El Enshasy HA, Eldawi H, Malathi VG, Salmen SHMJ, Khan AN, Sayyed RZ (2021) Mining the genome of Bacillus velezensis VB7 (CP047587) for MAMP genes and non‐ribosomal peptide synthetase gene clusters conferring antiviral and antifungal activity. Microorganisms 9:2511 Sarkar DA, Sarkar, Devika OS, Singh Shikha S, Parihar M, Rakshit A, Sayyed RZ, Gafur A, Ansari MJ, Danish S, Shah F, Datta R (2021) Optimizing nutrient use efficiency, productivity, energetics, and economics of red cabbage following mineral fertilization and biopriming with compatible rhizosphere microbes. Sci Rep 11:15680 Sayyed RZ, Patel PR, Shaikh SS (2015) Plant growth promotion and root colonization by EPS producing Enterobacter sp. RZS5 under heavy metal contaminated soil. Indian J Exp Biol 53: 116–123 Sayyed RZ, Seifi S, Patel PR, Shaikh SS, Jadhav HP, El Enshasy H (2019) Siderophore production in groundnut Rhizosphere isolate, Achromobacter sp. RZS2 influenced by physicochemical factors and metal ions. Environ Sustain 1(3):295–301 Seema B, Sharma, Sayyed RZ, Trivedi MH, Gobi T (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587 Selvamani S, Dailin DJ, Gupta VK, Mohd W, Keat HC, Natasya KH, Malek RA, Hhaque S, Sayyed RZ, Abomoelak B, Sukmawati D, Varzakas T, Enshasy HEE (2021) An insight into probiotics bio-route: translocation from the mother’s gut to the mammary gland. Appl Sci 11:7247 Serraj R, Vasquez-Diaz H, Hermandez G, Drevon JJ (2001) Genotypic difference in the short-term response of nitrogenase activity (C2H2 reduction) to salinity and oxygen in the common bean. Agronomie 21:645–651 Shaikh SS, Reddy MS, Sayyed RZ (2016) Plant growth promoting rhizobacteria: An eco-friendly approach for sustainable agro-ecosystem Plant Soil-Microbes. Springer, Cham, pp 182–201 Shaikh SS, Wani SJ, Sayyed RZ, Thakur R, Gulati A (2018) Production, purification and kinetics of chitinase of Stenotrophomonas maltophilia isolated from rhizospheric soil. Indian J Exp Biol 56(4):274–278 Shaikh F, Shah TNABM, Gaber A, Alsanie WF, Ali S, Ansari S, Rafiq M, Sayyed RZ, Rind NA, Rind KH, Shar AH (2021) Frequency distribution and association of Fat-mass and obesity (FTO) gene SNP rs-9939609 variant with diabetes mellitus type-II population of Hyderabad, Sindh, Pakistan. Saudi J Biol Sci 28(8):4183–4190 Sharma S, Sayyed R, Sonawane M, Trivedi M, Thivakaran G (2016) Neurospora sp. SR8, a novel phosphate solubilizer from rhizosphere of soil of Sorghum in Kachh, Gujarat. Ind J Exp Biol 54: 644–649 Sharma A, Gupta A, Dalela M, Sharma S, Sayyed RZ, El Enshasy HA, Elsayed EA (2020) Linking organic metabolites as produced by Purpureocillium lilacinum 6029 cultured on Karanja

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deoiled cake medium for the sustainable management of root-knot nematodes. Sustainability 12(9):8276 Silva C, Vinuesa P, Eguiarte LE, Souza V, Martinez Romero E (2005) Evolutionary genetics and biogeographic structure of Rhizobium gallicum, a widely distributed bacterial symbiont of diverse legumes. Mol Ecol 14:4033–4050 Singh S, Singh V, Mishra BN, Sayyed RZ, Haque S (2021) Lilium philadelphicum flower as a novel source of antimicrobial agents: a study of bioactivity, phytochemical analysis and partial identification of antimicrobial metabolites. Sustainability 13:8471 Sonawane MS, Salunkhe RC, Sayyed RZ (2021) Insect gut bacteria and iron metabolism in insects. In: Enshasy HAE, Yang ST (eds) Probiotics, the natural microbiota in living organisms fundamentals and applications. CRC Press, Boca Raton, FL, pp 343–366 Soto N, Ferreira A, Delgado C, Enriquez GA (2013) Regeneración in vitro de plantas de soya de la variedadcubana IncaSoy-36. Appl Biotechnol 30(1):29–33 Souza L (1999) Symbiotic efficiency of Hup+, Huphr and Hup strains of Bradyrhizobium japonicum and Bradyrhizobium elkenil in cowpea cultivars. Pesqui Agropecu Bras 34(10):1925–1931 Sridevi M, Mallaiah KV (2007) Production of indole-3-acetic acid by Rhizobium isolates from Sesbania species. Afr J Microbiol Res 1(7):125–128 Streeter JG, Gomez ML (2006) Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and in bacteroid from soybean nodules. Appl Environ Microbiol 72(6):4250–4255 Su Fang Z, Fuli X, Jiang Ke Y, You Guo K (2011) Phylogeny of Bradyrhizobium from Chinese cowpea miscellany inferred from 16S rRNA, atpD, glnII, and 16S-23S intergenic spacer sequences. Can J Microbiol 57:316–327 Suarez R, Wong A, Ramírez M, Barraza A, Orozco MDC, Cevallos MA, Lara M, Hernandez G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by over expressing trehalose-6-phosphate synthase in Rhizobia. Mol Plant-Microbe Interact 21:958–966 Sugawara ME, Cytryn J, Sadowsky MJ (2010) Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol 76(4):1071–1081 Sukmawati D, Family N, Hidayat I, Sayyed RZ, Elsayed EA, Dailin DJ, Hanapi SZ, Wadaan MA, Enshasy HE (2021) Biocontrol activity of Aureubasidium pullulans and Candida orthopsilosis isolated from Tectona grandis L. phylloplane against Aspergillus sp. in post-harvested citrus fruit. Sustainability 13:7479 Sung T (1993) Nitrogenase activity of soybean (Glycine max L.) root nodules under water logging condition. Plant Physiol 31:811–818 Suriani NL, Suprapta DN, Novizar N, Parwanayoni N, Darmadi A, Dewi D, Sudatri N, Ahmad F, Sayyed RZ, Syed A, Elgorban A, Bahkali A, Enshasy H, Dalin DJ (2020) A mixture of piper leaves extracts and Rhizobacteria for sustainable plant growth promotion and biocontrol of blast pathogen of organic bali rice. Sustainability 12:8490 Sutherland TD, Bassam BJ, Schuller LJ, Gresshoff PM (1990) Early nodulation signals of the wild type and symbiotic mutants of soybean (Glycine max). Mol Plant Microbe Interact 3:122–128 Tejera NA, Campos R, Sanjuan J, Lluch C (2004) Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropica isogenic strains with varying tolerance to salt stress. J Plant Physiol 161(3):329–338 Thakare CS, Rasa PH, Patil PH (1997) Evaluation of efficient Bradyrhizobium strains for soybean. Legum Res 22(1):26–30 Thies JE, Bohlool BB, Singleton PW (1992) Environmental effects on competition for nodule occupancy between introduced and indigenous Rhizobia and among introduced strains. Can J Microbiol 38:493–500 Todd JD, Sawers G, Rodionov DA, Johnston AWB (2006) The regulator IrrA affects the transcription of a wide range of Rhizobium genes in response to Fe availability. Mol Gen Genomics 275: 564–577

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Chapter 19

Inoculant Production and Formulation of Azospirillum Species P. Sivasakthivelan, P. Saranraj, R Z Sayyed, K. Arivukkarasu, M. Kokila, M. Manigandan, and Sonia Seifi

1 Introduction Azospirillum is a curve shaped vibroid Gram negative, measuring about 1–1.5 μm in diameter, motile because of possessing Peritrichous flagella for swarming and a Polar flagellum for swimming. The reserved cell inclusion energy is stored in the form of Poly β-hydroxy butyrate (PHB) granules for preventing the cell during the lack of energy (Okon et al. 1976). Dobereiner et al. (1976) reported the Azospirillum sp. as an aerobic microorganism, but they are able to grow under microaerophilic condition too that require oxygen in low level. Surprisingly, it was observed that the Azospirillum sp. was highly effective in fixing atmospheric nitrogen under microaerophilic condition. The major problem that limits the widespread adaptation of bioinoculants technology has been the non-availability of good quality inoculum. Unfortunately, much of the inoculant produced in the world today is relatively of poor quality. Therefore, it is necessary to develop alternative new formulation of inoculants and in this context, alginate beaded and liquid inoculants play significant role (Fallah et al.

P. Sivasakthivelan (*) Department of Agricultural Microbiology, Faculty of Agriculture, Annamalai University, Annamalai Nagar, Tamil Nadu, India P. Saranraj · M. Kokila · M. Manigandan Department of Microbiology, Sacred Heart College (Autonomous), Tirupattur, India R. Z. Sayyed Department of Microbiology, PSGVPM’S ASC College, Shahada, India K. Arivukkarasu Department of Agronomy, Faculty of Agriculture, Annamalai University, Annamalai Nagar, Tamil Nadu, India S. Seifi Department of Agriculture, Payame Noor University (PNU), Tehran, Iran © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Mawar et al. (eds.), Plant Growth Promoting Microorganisms of Arid Region, https://doi.org/10.1007/978-981-19-4124-5_19

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2021). High cell count, zero contamination, longer shelf life, greater protection against environmental stresses, increased field efficacy and convenience of handling are the main advantages of the liquid biofertilisers over the conventional carrierbased biofertilisers (Hegde 2002). FAO (1991) reported that most of the international producers of biofertilisers are engaged in the production of carrier-based inoculants. Biofertilisers manufactured in India are carrier-based in general and suffer from short shelf life, poor quality, high contamination and low and unpredictable field performances (Hegde 2002). The success of inoculation technology depends on two factors such as the microbial strain and inoculant formulation. In practical terms, formulation determines potential success of inoculants (Baba Hamid et al. 2021). The technical optimisation of an inoculant formulation is independent of strains used, since most of the strains of same bacterial species share many physiological properties, it may be assumed that a technological progress developed for a particular strain is readily adaptable to another strain of the same species with only minor modifications. In spite of a central role of formulation in successful commercialisation of inoculant products, research in this area has been largely ignored. In addition to limited availability of published scientific information with regard to inoculant formulation, the information available is fragmented (Xavier et al. 2004). Development of improved formulations often rests with inoculant manufacturer’s research and development facility which are primarily located in developed countries where target market exists, but they fail to consider the unique problems in applying these inoculants in developing countries. The most important characteristic problem is common to most of the biofertilisers is unpredictability of their performance. To harness the benefits of biofertilisers in agriculture, the consistency of their performance must be improved (Saravanan et al. 2021). Formulation step is a crucial aspect for producing microbial inoculants and determines the success of a biological agent. Formulation typically consists of establishing viable bacteria in a suitable carrier together with additives that aid in stabilisation and protection of microbial cell during storage, transport and at the target (Rezapour et al. 2021). The formulation should also be easy to handle and apply so that it is delivered to target in most appropriate manner and form, one that protects bacteria from harmful environmental factors and maintain or enhance the activity of the organisms in the field. Therefore, several critical factors including user preference have to be considered before delivery of a final product (Xavier et al. 2004). A suitable carrier plays a major role in formulating microbial inoculants. Carrier is a delivery vehicle which is used to transfer live microorganism from an agar slant of laboratory to a rhizosphere. A good quality inoculant should be made of a superior carrier material. Hence, Smith (1992) has listed the characters of a superior quality carrier material for microbial inoculants. The carrier-based inoculants of bacterial biofertiliser consortium have several advantages such as increased shelf life, protection from adverse conditions, better survival on seed, etc. The carrier-based individual inoculant effect on several crop plants has been studied. The physico-chemical characters of carrier materials have profound influence on the survival of inoculants.

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The ideal characteristics of an inoculant carrier include more surface area, rich in organic matter, high water holding capacity, neutral pH, easy availability and inexpensiveness (Patel et al. 2016a).

2 Plant Growth Promotion by Azospirillum sp. Azospirillum is considered as the most valuable bioinoculant in the group of plant growth promoting rhizobacteria (PGPR) because it is not only the microorganism capable of colonising the roots of agricultural crops, along with root colonisation Azospirillum sp. have the tendency of producing more beneficial compounds which are highly beneficial to crops (Dobereiner and Day 1976). Nitrogen fixation is the key function of the Azospirillum sp. The process of fixation of atmospheric nitrogen was carried out only under anaerobic condition because the major enzyme required for nitrogen fixation is nitrogenase was sensitive to oxygen and the process will be disturbed in the presence of oxygen (Steenhoudt and Van der Leyden 2000). Further studies on the Azospirillum bioinoculant pinpointed the various beneficial effects on morphological and physiological changes in plants in the inoculated roots that would lead to an improvement in uptake multiple number of minerals and enhancement of water uptake. Other physiological changes such as getting resistance against the abiotic stresses are also reported in the Azospirillum inoculated plants. Creus et al. (2005) inoculated the Azospirillum on the wheat seedlings and observed the development of osmotic stress. The growth efficiency of wheat with Azospirillum inoculated and non-inoculated seedlings was compared. It was found that the bioinoculant inoculated seeds has showed more fresh weight and yield of wheat when compared to non-inoculated seeds (Zope et al. 2016). Plants exposed to salt stress have a possibility of suffering from water deficient. It was proved that inoculating with 108 cells of Azospirillum brasilense on root seedlings and thereafter exposed to mild and severe salt stress significantly reversed part of the negative effects. Casanovas et al. (2003) carried out the field experiments with the bioinoculant Azospirillum on Sorghum bicolour and Zea mays. Results have shown significant increase in the growth, yield and biochemical composition of crops along with better water and mineral uptake. Creus et al. (2004) reported that the Azospirillum—inoculated with the wheat seedlings were able to survive when exposed to the excess saline concentration upto 320 mM NaCl for an average of 3 days. The inoculation technology with Azospirillum sp. was extended to arid soil regions where the water scarcity was very high to protect the crops against drought condition. Results of the experiments showed the significant increase in water content of plant, relative water content, water uptaking potential, apoplastic water fraction and lower cell wall modulous of elasticity values in Azospirillum—inoculated plants (Shaikh et al. 2018). The beneficial effect of Azospirillum sp. in plants relies on the good colonisation of roots and rhizosphere region. Root colonisation is considered an important factor for creating the relationship of microorganisms with the plant, not only in infection

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caused by soil borne phytopathogens (Negative effect) but also for the beneficial association with the plant growth supporting microorganisms (Positive effect) (Zope et al. 2019). During the positive effect, the first event in the colonisation process is the adhesion of the bacteria to the plant roots. This Azospirillum—root interaction is a two-step process. The first step is adsorption mediated by the help of bacterial proteins. The second step is anchoring involved by the bacterial polysaccharides. The root colonisation of Azospirillum sp. was highly depending on the active motility and chemotaxis towards the root exudates (Creus et al. 2004). The distribution of Azospirillum isolates in the plant roots was studied by using the technique which analyses the gfp-protein and tag bacteria. Liu et al. (2003) confirmed the colonising pattern of Azospirillum sp. with plant roots. Some nitrogen fixing strains of Azospirillum lipoferum and Azospirillum brasilense are established on the plant root surface, but other strains are not capable of colonising the root interior surface in the apoplast and intercellular spaces (Sagar et al. 2020a, b). This ability means the lower vulnerability to harsh conditions that are imposed by the soil environment which in turn supports the plant growth promoting activities (Sturz and Nowak 2000). The rhizobacteria which are establishing their relationship inside the plant roots are considered as endophytes. These microorganisms stimulate the plant growth by producing plant growth promoting hormones, enhance plant disease resistance against plant pathogens or improve the mobilisation of nutrients in soil (Arora et al. 2021).

3 Azospirillum: A Promising Biofertiliser Biofertilisers are the microbial inoculants, which can promote plant growth and productivity, have internationally been accepted as a supplementary source for providing nutrients. They are applied as seed treatment or foliar spray or soil application that colonises the rhizosphere or the interior of the plant system and promotes growth by increasing the supply or availability of primary and secondary nutrients to the host plant (Jabborova et al. 2020a, b). Biofertilisers add nutrients to soil and improve the plant growth through the synthesis of growth promoting substances and it can be expected to reduce the use of chemical fertilisers and pesticides. They are extremely advantageous in enriching the soil fertility and fulfilling the plant nutrient requirements by supplying the organic nutrients through microorganisms and their derivative products (Sharma et al. 2013). Azospirillum is being considered as one of the potential beneficial bioinoculant used worldwide in promoting the growth and development of different agricultural and horticultural crops. The positive effect can be either directly or indirectly. The direct effect could be through nitrogen fixation whereby Azospirillum facilitates nitrogen nutrition for the plants, thus stimulating plant growth (Dobereiner et al. 1976). It could also be through synthesis of hormone like substances, which

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stimulate root development consequently, enhancing absorption of water and nutrients leading to improved plant growth (Okon et al. 1977). Rhizosphere colonisation by Azospirillum sp. has been shown to stimulate the growth of a variety of plant species. Initially, it was assumed that the nitrogen fixing capacity of Azospirillum was the principal mechanism by means of which it could bring about the plant growth promotion (Bashan and Levanony 1990; Bashan and Holguin 1997; Bashan et al. 2004). The production of siderophores by Azospirillum is another feature that could contribute to its proliferation in an iron-poor environment. The ability of Azospirillum sp. to produce phytohormones such as IAA and gibberellins may be the main reason for the bacteria to colonise plant roots (Martinez-Morales et al. 2003).

4 Reasons for Poor Performance of Agricultural Bioinoculants This unpredictability is due to the fact that the immediate response to soil inoculation with bioinoculants varies considerably depending on the bacteria, plant species, soil type, inoculant density and environmental conditions. Moreover, this inconsistency is also due to the reason that, shortly after the bacteria are introduced into the soil, the bacterial population declines progressively (Ni Suriani et al. 2020) The key reason for the decline of the inoculated bacterium is that soil is a heterogeneous and unpredictable environment; while abiotic soil factors such as textural type, pH, temperature, and moisture exert their direct effect on inoculant population dynamics by imposing stress of various nature on the cells. Despite many successful greenhouse experiments, the commercial application of bioinoculants on a large scale has not been a great success. The main reason attributed to this failure is the unpredictability and inconsistency of field results (Khan et al. 2020). In addition, other physical factors such as oxygen or water supply or limitation, high osmotic or matric tension, and particularly fluctuations in these conditions which are typical for the soil environment may also play a role a pivotal role in this decline. Van Veen et al. (1997) suggested ecological selectivity, i.e. the selection of an inoculant strain by some unique feature in the soil ecosystem as an important tool for effective establishment of an active inoculant cell population in soil. Moreover, this may be due to the scarcity of nutrient sources such as C, N, and P sources available to microbes in soil and due to adverse biotic and abiotic factors. Biotic factors include predation or the competition in which the inoculated bacteria must compete with the often better-adapted native micro-flora and to withstand predation by protozoans (Sayyed et al. 2015).

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5 Inoculant Production and Formulation of Azospirillum sp. Among the various rhizosphere associated bacteria, Azospirillum species are probably the most studied and appear to have significant potential for commercial applications. The inoculated Azospirillum should reach the root even if the root system is widely spread and the inoculation should be at the precise time needed by the plant. Hence, the inoculation techniques should be practical, economical and easy to accomplish for the farmers (Wani et al. 2016). Bashan and Levanony (1990) suggested that the formulated product should deliver sufficient inoculum to the plant, must be competitive with existing commercial standards and must possess a long shelf life. The most classical inoculants are based on carriers, mainly on peat, which is generally neutralised presterilised and inoculated with a culture sample of the desired strain. Okon (1985) reported that Azospirillum inoculant is efficiently used as peat-based inoculant, and this is highly adsorptive and non-toxic to Azospirillum. Large, easily accessible deposits of true peat are rare, especially in the tropics. This has led to research into alternative carrier materials such as lignite, charcoal, coir dust and compost of various organics (Singleton et al. 2002). Chemical and physical properties are indicative of the feasibility of employing a given substrate in inoculant technology. Lignite, because of its abundant availability, good water holding capacity and maintaining cells as effective as peat is now preferred and widely used as a carrier material in most of the biofertilisers manufacturing plants all over India. Biopolymers like alginate or xanthan gum have shown to be good carriers and provide products of constant quality. Although these carriers protect the organisms against stresses, the products are expensive, and their use requires more technical handling. The dehydrated dried inoculants, which contain two billion cells/g, easy to store and handle but the addition of protectants, additives, nutrients, etc., need to be standardised (Stephens and Rask 2000). Efficient strains of plant growth promoting rhizobacteria (PGPR) are mass multiplied under laboratory condition and mixed with a carrier. These carrier-based inoculants are supplied to farmers for crop inoculation. Carrier is a medium or matrix on which inoculant microorganism grow to a reasonably higher population for an initial period and thereafter decline (Gandhi and Saravanakumar 2009). The nature of the carrier often determines the subsequent performance of the inoculant. The criteria for a good carrier material are no toxicity to the introduced microorganisms, good absorption capacity, suitable pH and fine particle size for better adherence to seed, good water holding capacity and availability of material at cheaper cost (Sharma et al. 2016). Different carriers have been used for inoculation throughout the world. Some of the carriers used by different manufactures in the country and abroad are peat, lignite, vermiculite, charcoal, press mud, coal, polyacrylamide and alginates. The carrier-based inoculant improves their shelf life and efficiency of bio fertilisers (Reshma et al. 2018).

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Carrier-Based Inoculant

The carrier is a delivery vehicle for microorganisms from factory to the field. The carrier comprises major portion (by volume or weight) of the inoculants. The universal carrier for rhizobia is peat. The superiority of peat-based inoculants was reported by Burton et al. (1965) and Vincent (1958). Peat is considered as the most dependable carrier because of its high organic matter content and water holding capacity. Farmyard manure, compost, coconut shell powder, vermiculture, teak leaf powders were also used as carriers for inoculant production. Jauhri et al. (1979) reported higher survival of Rhizobium and Azotobacter in modified charcoal carrier. Jauhri and Philip (1982) reported that press mud with charcoal in a proportion of 13: 1 was a superior inoculant base. Geels and Schippers (1983) formulated the suspension of Pseudomonas cells by mixing cell suspension with 0.2% protease peptone and 2% carboxyl methyl cellulose in distilled water for potato tuber treatment (Sayyed et al. 2019). Lignite-based inoculants are widely accepted and used for seed treatment of various crops. Thangaraju (1996) recommended the use of decomposed coir pith with lignite or peat (1:1) for better survival of Rhizobium. Govindarajan (1996) studied the growth and survival of Azospirillum lipoferum in peat, coir pith and mixture of peat and coir pith. The peat supported higher proliferation of the inoculated organisms than other carriers. Lignite is the preferred and widely used carrier in most of the biofertiliser manufacturing plants all over India. Among the four different bioinoculant carriers (paddy husk, groundnut shell, lignite and sawdust), the population was maximum in lignite at all temperatures studied (Saha et al. 2001). Addition of various polymers, amendments and chemicals in both sterile and unsterile carriers resulted in increased shelf life of Azospirillum lipoferum (Sureshbabu et al. 2002). Tilak and Subba Rao (1978) found that soil + FYM in 1:1 proportion had higher Azospirillum count followed by soil + FYM + Vermiculite in 5:3:2 proportions. Sparrow and Han (1981) studied the survival at Rhizobium phaseoli in peat, powdered peanut shell, corn cobs and vermiculture and reported that vermiculture supported 107 cells of rhizobia/g of carrier after 30 weeks of storage period. Kumar Rao et al. (1982) and Subba Rao (1982) examined the survival of Rhizobium in number of locally available materials such as lignite, pressmud, charcoal, soil and coffee waste and found that pressmud was better than other carriers including peat for the survival and rate of decline of Rhizobium for a period up to 200 days. Singaravadivel and Anthoni Raj (1988) reported that black ash, paddy husk mixture, husk powder and pressmud were effective to be used as a carrier for Rhizobium inoculant as they maintained the viable cell load of 107 cells/g even after 6 months and they were on par with lignite and peat. A good carrier should have the capacity to deliver right number of viable cells in good physiological condition at right time. Lignite-based inoculants are widely accepted and used for seed treatment of various crops.

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Narendranath et al. (1996) reported that higher survival of groundnut Rhizobium in peat followed by press mud and lignite and suggested press mud amended with soy meal as an alternative carrier to peat in inoculant preparation. Thangaraju (1996) recommended the use of decomposed coir pith with lignite or peat (1:1) for better survival of Rhizobium. Govindarajan (1996) studied the growth and survival of Azospirillum lipoferum in peat, coir pith and mixture of peat and coir pith. The peat supported higher proliferation of the inoculated organisms than other carriers. The population was maximum in lignite at all temperatures studied (Saha et al. 2001). Addition of various polymers, amendments and chemicals in both sterile and unsterile carriers resulted in increased shelf life of Azospirillum lipoferum (Sureshbabu et al. 2002). Gopal (2004) showed the better shelf life and effectiveness of lignite-based rhizobacterial inoculant than other carrier-based inoculants on Ashwagandha a commercially grown medicinal plant. Vermicompost as an alternative carrier to lignite was suggested in the inoculant preparation of Phosphobacteria, Azospirillum and Acetobacter diazotrophicus. Gopal (2004) reported that industrial and agricultural waste such as cheese whey, malt sprouts, plant compost, filter mud, fly ash and wastewater sludge containing nitrogen and carbon supports the growth of Rhizobia which was used as the potential carrier for Rhizobium inoculants. Maria del Carmen Rivera compared the effectiveness of poultry manure and banana waste as inoculant carriers of a bacterial consortium constituted by strains of Azospirillum, Azotobacter and Phosphate solubiliser bacteria. Gandhi and Saravanakumar (2009) reported the effect of vermicompost as the carrier for bioinoculants in maintaining the shelf life of Azospirillum lipoferum, Bacillus megaterium and Pseudomonas fluorescens. Manoharan Melvin reported that the Azospirillum flocculated cells on comparison with normal cells were found to be superior in survival in different inoculant carriers. Vermiculite sustained the higher number of viable Azospirillum cells followed by lignite and compost and also augmented the growth and yield of sunflower. Frank Ogbo (2010) characterised Aspergillus fumigatus and Aspergillus niger isolated from decaying cassava peel and ground cassava peels satisfied many properties required for the carrier material and Azospirillum produced using Cassava peel improved the growth of pigeon pea (Jabborova et al. 2020a, b).

5.2

Alginate Beaded Inoculant

Polymers were demonstrated as potential bacterial carrier (Jung et al. 1982) offering substantial practical advantages over peat. These formulations encapsulate the living cells, protect the microorganism against many environmental stresses and release them to the soil gradually when soil microorganisms degrade the polymers. They can be stored dry at ambient temperatures for prolonged periods, offer consistent batch quality and a better-defined environment for the bacteria. Beaded inoculant can be amended with nutrient to improve the short-term survival of the bacteria as well as

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with associative plant growth promoting bacteria (PGPB) to improve their efficiency (Jadhav et al. 2020a, b). Alginate is the most common polymer material for the encapsulation of microorganisms for various industrial microbiological purposes (Fenice et al. 2000). Several alginate-based preparations were evaluated for agricultural purpose including the encapsulation of bio control agents against soil-borne pathogens and phosphate-solubilising bacteria (Jadhav et al. 2020a, b). This technology was also employed to encapsulate the PGPB like Azospirillum brasilense and Pseudomonas fluorescens that were successfully used to inoculate wheat plants under field condition. Encapsulated genetically engineered Pseudomonas fluorescens released later into soil micro ecosystem showed significantly increased survival rates over non-encapsulated cell after 3 months (Sharma et al. 2020). Pankaj Trivedi et al. (2005) evaluated for the growth promotion and rhizosphere colonisation of five different formulation using two plant growth promoting rhizobacteria (PGPR) viz., Bacillus subtilis and Pseudomonas corrugate (Sagar et al. 2020a, b). The best results were obtained in alginate-based formulation. Ricardo Yabur et al. (2007) reported that alginate extracted from the macro algae Sargassum sinicola was used as the raw material for co-immobilisation of the micro algae Choleralla sorokiniana and growth promoting bacterium Azospirillum brasilense for wastewater treatment and as an inoculant carrier of Azospirillum brasilense for plant growth promotion (Ilyas et al. 2020). Prabakaran and Hoti (2008) developed the immobilisation technique using sodium alginate as the matrix to preserve the Bacillus thuringiensis var. israelensis isolate for long time storage which enhanced the stability of both spores and toxin against several physico-chemical conditions and conferred reduced chance of contamination. Minaxi and Jyoti (2011) introduced bioinoculants in soil by encapsulating the cells in biodegradable gel matrices which gradually released the Azospirillum and also helped to increase the survival rate by protecting them against environment stress.

5.3

Gel-Based Formulations

In the last few decades, several new dry inoculants formulation in agriculture have been developed through encapsulation with various polymers followed by drying including polyacrylamide-based inoculants. The use of synthetic inoculant carriers as an effective alternative for Azospirillum was suggested by Bashan (1986). Polymers were demonstrated as potential bacterial carrier offering substantial practical advantages over peat. Bashan and Dubrovsky (1996) stated that peat and other inoculant carriers primarily designed for Rhizobia are hardly suitable for Azospirillum. These formulations encapsulate the living cells, protect the microorganism against many environmental stresses and release them to the soil gradually when soil microorganisms degrade the polymers. They can be stored dry at ambient temperatures for prolonged periods, offer consistent batch quality and a

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better-defined environment for the bacteria. Beaded inoculant can be amended with nutrients to improve the short-term survival of the bacteria as well as with associative plant growth promoting bacteria (PGPB) to improve their efficiency (Kalam et al. 2020). The gel-like matrix allows the cells to remain viable and with its catalytic ability for longer period. Several studies thus far have used alginate as the encapsulating material as it forms microbeads. In the last few years, several new microbial inoculant formulations have been proposed including alginate and agar immobilisation inoculants. El-Komy (2001) and Zohar Perez et al. (2002) reported that Azospirillum can survive in dry alginate inoculants for prolonged periods without losing effectiveness. Alginate is the most common polymer material employed for encapsulation of microorganisms for various industrial microbiological purposes (Prasad and Kadokawa 2009). Encapsulation of living cells in polymeric gel is a well-established technology in a broad and increasing range of different applications (Park and Chang 2000). Further, demonstrated that microbial immobilisation gives prolonged metabolic activity when microbial cells are reused. Alginate and agar immobilisation of the tested bacteria or co-immobilisation of Azospirillum lipoferum and Bacillus megaterium significantly enhanced phosphorus solubilisation for four consecutive cycles (El-Komy et al. 2004). Pankaj Trivedi et al. (2005) evaluated for the growth promotion and rhizosphere colonisation of five different formulation using two plant growth promoting rhizobacteria (PGPR) viz., Bacillus subtilis and Pseudomonas corrugata. The best results were obtained in alginate-based formulation reported that alginate extracted from the macro algae Sargassum sinicola was used as the raw material for co-immobilisation of the micro algae Chlorella sorokiniana and growth promoting bacterium Azospirillum brasilense for waste water treatment and as an inoculant carrier of Azospirillum brasilense for plant growth promotion developed encapsulation of plant growth promoting bacteria and green microalgae in alginate beads Kour et al. (2021). Prabakaran and Hoti (2008) developed the immobilisation technique using sodium alginate as the matrix to preserve the Bacillus thuringiensis var. israelensis isolate for long time storage which enhanced the stability of both spores and toxin against several physico-chemical conditions and conferred reduced chance of contamination. Immobilised Candida rugosa lipase by polylactic acid nanoparticle. A major role of inoculant formulation is to provide more suitable microenvironment for the prolonged survival of bacteria in the soil. It also helps in segregating the bacterial cells from adverse environment, thereby, reducing cell loss (De-Bashan et al. 2010; Trejo et al. 2012). Minaxi and Sexena (2011) introduced bioinoculants in soil by encapsulating the cells in biodegradable gel matrices which gradually released the microorganisms and also helped to increase the survival rate by protecting them against environment stress. Further, they reported two bacterial strains viz., Pseudomonas fluorescens and Burkholderia cepacia were immobilised using sodium alginate and alginate + skim

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milk as carrier to check the phosphate solubilisation in vitro and were found to have significantly higher activity than control (Basu et al. 2021).

5.4

Liquid Inoculant

First report on liquid inoculants for seed inoculation of Rhizobium was published from Holland. The liquid inoculum was as effective as peat-based inoculant when the number of Rhizobia per seed was increased 2.5 times. Schiffmann and Apler (1968) observed that liquid inoculants were particularly suited to large seeded grain legumes, which because of their bulk, made seed inoculation a formidable task. The liquid inoculation of Rhizobia provides higher cell load in the rhizosphere, but Boonkerd et al. (1978) reported that inoculation by peat or liquid formulation with any rate or strain did not affect plant growth. Wani and Rai (1980) reported that foliar spray application of Azotobacter increased the yield of paddy, wheat and sorghum. The spray method of liquid Rhizobium inoculant directly on to the soil was reported by Gault et al. (1982). It was observed that liquid form was easy to use as it spread well, mixed easily, and does not require sticker and no need of additional supply of water. Liquid inoculants generally contain high titre value. Lipha Tech (France) claimed cfu of 17 × 1011 in their liquid product (Patel et al. 2018). Rice and Olsen (1992) suggested liquid inoculation as a better method than seed treatments with carrier inoculant. The soybean nodule numbers in a tropical soil were found to be increased with increasing rates of Rhizobia applied in a liquid form. NIFTAL claimed the cell number of 1 × 1010 cells/mL in G-6 liquid inoculant. The development of suitable formulation, which would ensure survival and protection of the strain and the application technology, which would allow timely, easy and precise delivery in the field could be a major step towards this goal. The liquid Rhizobia inoculant for pea and lentil resulted in yield equal to or better than those obtained for the peat inoculant (Akhtar et al. 2021). NIFTAL, USA analysed different type of liquid inoculants including glycerolbased media, yeast extract mannitol media with various additives such as arabinose, polyvinylpyrrolidone (PVP), trehalose, Fe EDTA, glycerol, etc., and thus developed several liquid media viz., G-1, G-4, G-5, G-6, etc., and found that G-5 liquid Rhizobium inoculant increased the soybean crop seed yield above local products more than 68%. There are many other constraints in using the carriers for manufacture of biofertilisers listed by Bhattacharyya and Kumar (2000) included unavailability of good carriers, supporting poor cell number, poor moisture retention capacity, bulk sterilisation problem, pollution hazards from carrier dust, high transportation cost, etc. Biofertilisers presently manufactured in India are carrier-based and they suffer from short shelf life, poor quality, high contamination and unpredictable field performances. Hence, as an alternate, liquid inoculant formulation with a good field performance that uses low-cost materials and easily attainable

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by small producers could overcome many problems associated with processing solid carriers (Singleton et al. 2002). The development of suitable formulation, which would ensure survival and protection of the strain and the application technology, which would allow timely, easy and precise delivery in the field could be a major step towards this goal. Biofertilisers presently manufactured in India are carrier-based and they suffer from short shelf life, poor quality, high contamination and unpredictable field performances. There are many other constraints in using the carriers for manufacture of biofertilisers listed by Bhattacharyya and Kumar (2000) included unavailability of good carriers, supporting poor cell number, poor moisture retention capacity, bulk sterilisation problem, pollution hazards from carrier dust and high transportation cost. Inamdar et al. (2000) standardised cyst and spore-based liquid inoculants for Azotobacter and Phosphate solubilising Bacillus megaterium and recorded higher population and comparatively better yield. Inoculation of liquid inoculant with cell number of 2.7 × 108 cfu/mL resulted in increased growth and yield of tomato. Liquid formulation of Bradyrhizobium strain recorded higher acetylene reduction activity and better yield of soybean when compared with lignite carrier-based formulation. Singleton et al. (2002) conducted multi location field trials to evaluate the performance of G-5 and G-6 + PVP liquid formulations with local inoculant products and sterilised peat-based inoculant in 16 countries. The results revealed that average liquid inoculation responses were greater than control. The G-5 liquid inoculant inoculation increased soybean seed yield above local products more than 68% of the time, producing an average seed yield increase of 6%. High cell count, zero contamination, longer shelf life, greater protection against environmental stresses, and convenience of handling are the major advantages of liquid inoculants over the conventional carrier-based inoculants and this liquid inoculant technology can be considered as a breakthrough in the field of biofertiliser technology. Torres et al. (2003) developed liquid formulation for the biocontrol agent Candida sake by adding protectants such as lactose, trehalose and found high viability of cells and conservation of biocontrol efficacy. Gomathy et al. (2008) explained the methods and quantity of liquid formulation of Phosphobacteria required for seed inoculation, 1 mL inoculum with 1 mL of adhesive combination showed better results followed by 1.5 mL inoculum with 0.5 mL adhesive. The sporulated inoculum along with rice gruel favoured the adherence of the regenerated cells. Albareda et al. (2008) developed liquid culture media have been assayed employing mannitol or glycerol as carbon sources. Some media maintained more than 109 CFU/mL of Sinorhizobium (ensifer) fredii SMH12 or Bradyrhizobium japonicum USDA110 after 3 months of storage. Gomathy et al. (2008) explained the methods and quantity of liquid formulation of Phosphobacteria required for seed inoculation, 1 mL inoculum with 1 mL of adhesive combination showed better results followed by 1.5 mL inoculum with 0.5 mL adhesive. The sporrulated inoculum along with rice gruel favoured the adherence of the regenerated cells.

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Martin Diaz Zorita and Virginia (2009) described the beneficial effects of inoculating Azospirillum brasilense on wheat (Triticum aestivum L.). Liquid formulation of Azospirillum brasilense INTA Az-39 strain under typical dry land farming conditions exhibited more vigorous vegetative growth, with both greater shoot and root dry matter accumulation (12.9% and 22.0%, respectively). The inoculation increased the number of harvested grains by 6.1% and grain yield by 260 kg/ha (8.0%). Manikandan et al. (2010) reported the standardisation of liquid formulation of Pseudomonas fluorescens Pf1 and tested its efficacy against Fusarium wilt of tomato. The combination of seed treatment, seedling dip and soil drenching of liquid formulation recorded the minimum disease incidence of Fusarium wilt on tomato under greenhouse (17.33%) and field (4.81%) conditions, respectively. In addition, the liquid formulation increased the tomato fruit yield compared to untreated control under greenhouse and field condition (Hamid et al. 2021).

6 Chemical Amendments for Liquid Biofertiliser The quality of a microbial inoculant is primarily determined by how many viable cells are in the inoculant and how well they survive after application. Addition of cell protectants and certain chemicals (Arabinose, Glycerol, Polyvinylpyrrolidone (PVP), Trehalose, Fe EDTA, etc.) are known to keep the cells viable for long period under liquid culture.

6.1

Glycerol

Glycerol is a carbon source for Rhizobia. Lorda and Balatti (1996) described the growth characteristics of Bradyrhizobium japonicum in glycerol-based liquid media under various environmental conditions. More rapid growth was observed when 10 mL of glycerol was substituted for mannitol and populations in the glycerol medium at times reached densities in excess of 1 × 1010 cells/mL. Glycerol has high water binding capacity and may protect cells from the effects of desiccation by slowing the drying rate. Singleton et al. (2002) reported that glycerol above 8.0 mL/L recorded negative effect by slowing the growth and reducing the final cell number. Poonguzhali (2002) found that higher growth of Phosphobacteria in the medium may be attributed to the presence of glycerol. Instead of glucose in tryptone-yeast extract-glucose medium by NA-gluconate or glycerol, two new culture media were developed for mass cultivation of the commonly used plant growth promoting bacterium Azospirillum sp. after 18 h of incubation, these modifications increased population of different strains of Azospirillum to 1011 cells/mL (single cell count) and 5 × 109 CFU/mL (plant

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count method), significantly reduced generation time, and were also suitable for production of common synthetic inoculants (Bashan et al. 2011). Velineni and Brahmaprakash (2011) developed two liquid inoculant media for Bacillus megaterium. Liquid inoculant-2 contain Osmoprotectants viz., PVP, high quantity of glycerol (12 mL/L) and glucose supported higher viable population up to a storage period of 4 weeks at 48 °C (log10 10.62 CFU/mL) and desiccation (log10 10.04 CFU/mL) as compared to liquid inoculant contains Osmoprotectants viz., PVP, low quality of glycerol (1 mL/L), trehalose, arabinose and Fe EDTA. Mugilan et al. (2011) reported better survival of Pseudomonas striata in glycerol and tween 20 for longer period was observed and it could be improved by the addition of skimmed milk and controlled dehydration (Kusale et al. 2021).

6.2

Polyvinylpyrrolidone

Polyvinylpyrrolidone (PVP) has a high-water binding capacity and appears to slow drying of the inoculant after application. Singleton et al. (2002) reported that PVP appear to enhance survival of Bradyrhizobium japonicum, and the promotion is concentration dependent. Increasing amounts of PVP K 30 in the media increased survival on the seed by 100-folds at 48 h after inoculation. The authors also found that after 180 days of storage, the number of viable cells remained nearly constant for the G-6 medium with 20 g PVP/L. Sureshbabu et al. (2002) found maximum population of Azospirillum due to the addition of PVP at both 2% and 1% levels. Higher moisture content of the inoculant after the storage period of 7 months was also recorded with PVP treated inoculant. Gomathy (2003) reported that maximum survival of Bacillus megaterium in the nutrient broth amended with PVP (Vafa et al. 2021).

6.3

Trehalose

Leslie et al. (1995) reported that the protective action of trehalose has been ascribed to its ability to replace water in proteins and membrane structures. Trehalose was observed to be a very sensitive and responsive compound to stress conditions. It was found to be either hydrolysed or presumably acting as a carbon source or synthesised and accumulated likely to function as a membrane stabiliser and protectant. Trehalose is an enigmatic compound which acts as a supplementary compatible solute or as reserve carbohydrate that may be mobilised during stress. The mechanisms underlying the unique efficacy of trehalose are still under discussion and may include glass formation and formation of anhydrous crystals capable of reversibly absorbing water (Sussich et al. 2001). Fillinger et al. (2001) observed the role of trehalose in the acquisition of stress tolerance in the fungus Aspergillus nidulans. Trehalose is widely reported to

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enhance cell tolerance to desiccation and to osmotic and temperature stress. It acts by stabilising both enzymes and cell membranes and is a compatible osmoticum as well. Singleton et al. (2002) and Torres et al. (2003) reported that trehalose at 1% concentration was the best protective agent for Candida sake and showed viability of 72% after 4 months storage. Accumulation of trehalose was enhanced by supplying the disaccharide in culture media and it was found that trehalose loaded Bradyrhizobium cells survived significantly better during subsequent desiccation stress (Streeter 1985). A possible effect of trehalose protective action is that it may be incorporated into the cell or to induce the synthesis of metabolites that protect against stress (Gomez Zavaglia et al. 2003). However, more complex mechanisms of protection induced by trehalose, such as synthesis of shock proteins among them will be the subject of future analysis. Polyvinylpyrrolidone (PVP), Trehalose, Fe EDTA, etc. are known to keep the cells viable for long period under liquid culture (Nithyapriya et al. 2021).

7 Factors Affecting the Shelf Life of Azospirillum Bioinoculants The quality assured bio fertiliser product ensures presence of viable prescribed microbial load between date of manufacture and expiry so to affect its biological activity. Hence, it was desirable to use appropriate technology for longer shelf life during manufacturing processes. The following various factors such as moisture content, temperature of incubation, aeration, carrier sterility, packaging materials determines the shelf life of bio fertiliser (Moradzadeh et al. 2021a, b).

7.1

Moisture Content

Clover and cowpea type Rhizobia are adversely affected with moisture content of 30%, although other organisms occurring naturally in peat were less affected. Levels in the range of 40–50% were optimal for survival of Rhizobium. In a sterilised peat, all strains are more tolerant to higher levels of moisture and growth was optimal in the range of 40–60% moisture (Kannaiyan 2000).

7.2

Temperature of Incubation

Russo et al. (1996) studied the effect of storage temperature on the growth and survival of inoculant in sterilised and unsterilised carrier to purify the culture and the loss in moisture during storage. The moisture content of culture in cotton wool

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stopper bottles wrapped in cellophane may be kept at a constant 50% by storage at 2 °C, but storage at such temperature immediately after inoculant restricts initial multiplication and maximum numbers are not reached until 26 weeks. Saha et al. (2001) studied the survival of Rhizobium in the paddy husk as carrier at different temperature using green fluorescent protein marker and reported that survival rate of Rhizobium transformant is less at higher temperature above 28 °C.

7.3

Aeration

Canadian and European workers observed rapid death of Rhizobia in sealed containers, but with access to air their numbers remained high until the carrier became desiccated (Hedlin and Newton 1948). The growth and survival of clover and cowpea-type Rhizobia in sterilised peat using cotton wool stopper tubes, sealed cans and plastic film packets and with various gas exchange properties. The practice of putting small holes in bags is unnecessary and harmful as in that moisture loss is increased. Also, they allow entry of contaminants in sterilised peat cultures (Jabborova et al. 2021).

7.4

Carrier Sterility

The inoculant prepared with non-sterilised peat might contain 100-fold more Rhizobia than sterilised peat because the death rate is higher in sterilised peat and is progressive with increase in storage period. Sterilisation has great influence on the growth and survival of Rhizobia and important to achieve consistently high cell densities in excess of 109/g (Kour et al. 2021).

7.5

Packaging Material

The choice of a method of inoculating sterilised peat without introducing contaminants depends on the type of packaging. Rhizobium needed a definite gas exchange through packing materials. Other hand inoculants in better survival of sealed bags than in open aerated bags were observed by Iswaran (1972). Higher survival (3.5 × 108/g–62 × 108/g) in inoculants packed of high-density polythene bags of 0.31–0.31 mm gauge was reported by Strijdom and Deschodt (1976). Double polythene bag having 300-gauge thickness supported higher survival of Azospirillum compared to single polythene bag (600 gauges) at room temperature. Packing the peat-based inoculant of Azospirillum in two layered polythene bag increased the shelf life when compared to packing in single polythene bag or polythene container. Beaded inoculant of Azospirillum brasilense enhanced the

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development of wheat and tomato seedlings growing in unfertile soil. Beads get degraded within 15 days in moist soil, by releasing gradually the immobilised inoculant organism (Bashan 1990).

8 Effect of Azospirillum Isolates on Agricultural Crops The nitrogen fixing rhizobacteria Azospirillum lives in close association with plant roots, where it exerts beneficial effects on plant growth and yield of many crops of agronomic importance. The effect of Azospirillum inoculation on the total yield increases of field grown plants generally ranged from 10% to 30%. Bashan et al. (1989) reported that 70–75% of pot experiment in cotton and several vegetables resulted in yield increase. Wani (1990) evaluated the worldwide success of Azospirillum inoculant and concluded that positive effects on yield were obtained in approximately 65% of field experiments and in about 70–75% of pot culture experiments in several vegetables. A few reports indicate extremely higher values of 50–270% increase in yield over uninoculated controls. Moderate yield increase of 20% attributed to inoculation with Azospirillum is considered commercially valuable to modern agriculture, if obtained consistently (Khan et al. 2021). Plant height, number of primary and secondary branches and number of leaves increased in Coleusparvi florus by application of 60 kg N/ha along with Azospirillum 2 kg/ha at the time of planting. However, application of 100 kg N/ha along with 2 kg/ ha of Azospirillum increased the foliar N, P, Ca and Mg. Plant height, number of primary and secondary branches and number of leaves increased in Coleus by application of 60 kg N/ha along with Azospirillum 2 kg/ha at the time of planting. However, application of 100 kg N/ha along with 2 kg/ha of Azospirillum increased the foliar N, P, Ca and Mg (Kapadia et al. 2021a, b). Azospirillum alone was not sufficient to promote the growth, but the interaction effect of Azospirillum and nitrogen (80 kg/ha) had beneficial effect in improving the growth and nutrient uptake in cauliflower and Azospirillum inoculation saved up to 50% of recommended nitrogen. In a field trial of Gundu malli (Jasminum sambac), increased plant height, number of tertiary branches, shoot and leaf area, dry weight of root biomass, flower weight and yield were observed due to inoculation with Azospirillum along with nitrogenous fertiliser application. Cabellero Mellodo et al. (1992) reported that inoculation of Azospirillum in wheat caused significant yield increase in the range of 1.5–3.0 t/ha. Increased uptake of nitrogen, growth parameters and yield were obtained in wetland rice through the inoculation of Azospirillum. Azospirillum increased the grain yield and dry matter marginally by 2%–10% over the uninoculated control. Fulchieri and Frioni (1994) observed that maize (Zea mays) inoculated with Azospirillum has enhanced dry weight of seeds by 59% and also the yield, which was similar to 60 kg urea/ha. Inoculation with efficient strains of Azospirillum enhanced the yield of CSH 5 and CO 24 sorghum while K-tall and USH1 showed negligible response (Bastamia et al. 2021).

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In a field trial with banana cv. Poovan, the inoculation of Azospirillum along with nitrogenous fertilisers increased plant height, girth, total number of leaves, leaf area, sucker production, length of bunch, number of hands, fingers and total soluble solids. Significant increase in dry weight of shoot and root biomass (90% and 50%, respectively), total leaf area (90%) and root length (35%) in 18-day-old tomato plants inoculated with Azospirillum as compared to uninoculated plants (Sukmawati et al. 2021). The increase in growth characters like plant height in French marigold by Azospirillum inoculation were observed and this might be due to the added nitrogen to crop through associative symbiosis and increased production of growth hormones such as NAA, GA and cytokinins. The relative efficacy of different inoculation methods on growth and yield of paddy, the inoculation of seeds + seedlings + soil gave the highest yields compared with single inoculation method and uninoculated control. Soil inoculation was not effective. Bashan et al. (1989) reported that 70%– 75% of pot experiment in cotton and several vegetables resulted in yield increase (Kapadia et al. 2021a, b). The application of Azospirillum inoculant at 2, 4 and 6 weeks after planting increased the total and marketable yield of sweet potato by 12% and 17%, respectively, and 5% and 22%, respectively, in the second season. At 50% of the recommended dose of nitrogen (60 kg/ha) and the seedling treatment with Azospirillum as well as soil application of Azospirillum recorded the highest agronomic nitrogen use efficiency indicating that, Azospirillum inoculation in tomato saved 50% of the recommended dose of nitrogen (Singh et al. 2021). The seed treatment and seedling treatment with Azospirillum increased the growth parameter, ash content and total alkaloids in reported that soil inoculation of Azospirillum coupled with less nitrogen of 80 kg/ha had beneficial effect in improving the growth and yield of cauliflower cv. Jawahar Moti, besides saving recommended nitrogen up to 50%. Salomone and Dobereiner (1996) also found increased yield in maize when inoculated with Azospirillum. Inoculation of Azospirillum with 75% recommended dose of nitrogen was superior to uninoculated control in increasing the yield of cumbu variety UCC-5. The application of Azospirillum at reduced nitrogen levels (100 kg N/ha) resulted in higher growth and grain yield in rice varieties viz., IR-50, ADT-36 and TKM-9. Enhanced plant growth and flower yield was observed in Chrysanthemum due to the inoculation of Azospirillum (Sarkar et al. 2021). Mahesh Kumar et al. (1998) observed that Azospirillum influences the growth of bamboo seedlings. Inoculation of different wheat cultivars with the most efficient strain for N2-fixation resulted in increased growth and nitrogen to the 5 cultivars tested, but the effect varied among the cultivars. These results suggest that a potential exists for Azospirillum brasilense to supply considerable nitrogen to wheat plants, probably dependent on bacteria–cultivar interaction (Piccinin et al. 2011; Pereyra et al. 2012). Seed inoculation of Azospirillum brasilense increases the yield of wheat. Azospirillum increased the plant height, grain and fodder yield and also 25% saving in the nitrogen fertiliser was observed in Rabi sorghum.

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Gadagi et al. (1999) reported that inoculation of nitrogen fixing Azospirillum increased plant growth parameters and flower yield in Chrysanthemum, Marigold and China aster. Bekri et al. (1999) also showed substantial pectinase activity in Azospirillum irakense and explained their role of this enzyme in increasing the Azospirillum root colonisation. In roses, the early flowering due to inoculation with Azospirillum was observed. This was due to induced cytokinin synthesis and rapid assimilation of photosynthates resulting in early transformation of the axillary bulb from vegetative to reproductive phase. The yield parameters viz., number of flowers per plant, diameter of flower, ten flower weight, stalk length and flower yield per plant were increased by inoculation with Azospirillum strains DAD-2 and DAD-11 in Gaillardia (Gadagi et al. 1999). The effects of soil application of Azospirillum on growth and yield of sweet potato (Ipomoea batatas). Application of 40 kg N per ha supplemented with 10 kg Azospirillum per ha as soil application produced the highest tuber yield (28.62 t/ha) followed by 40 kg N per ha supplemented with 2 kg Azospirillum as vine dipping +10 kg Azospirillum as soil application (27.54 t/ha) and 60 kg N per ha alone (27.40 t/ha). The highest net income was obtained from 40 kg N + 10 kg Azospirillum as soil application. The rice (Oryza sativa) with Azospirillum sp., to determine the effects on seedling vigour and productivity. Seed treatment with Azospirillum increased the amylase activity during germination. This was attributed due to gibberellins secreted by the bacterium, resulting in enhanced seedling vigour, encompassing speed of germination, seedling length and dry weight (Nayeri et al. 2021). Thamizh Vendan and Subramanian (2000) reported that application of Azospirillum during first and second earthing up resulted in higher growth and kapas yield of rice fallow cotton (ADT-1). Suguna Rani (2000) studied the effect of Azospirillum on cotton (MCU-9) and reported that the growth parameters, dry matter production and yield were enhanced. Azospirillum brasilense inoculated spring wheat resulted in better germination, early development and flowering and an increase in dry weight of both the root system and the upper plant parts (Dobbelaere et al. 2001) and found a positive correlation between the increase in yield and the improvement of root development (Selvamani et al. 2021). The effect of Azospirillum inoculation methods (soil application of nursery or seedling root dip or both) and nitrogen levels (50, 75 and 100% of recommended dose of nitrogen) on growth and yield of rice. The interaction between nitrogen and Azospirillum indicated that application of 75% nitrogen with Azospirillum to nursery and seedling dip resulted in rice yields similar to those obtained with 100% nitrogen. (Alsulimani et al. 2021). The dual inoculation of maize cultivars (Seed treatment + soil spray) gave better growth and yield than a single inoculation by seed treatment. The application of Azospirillum through soil + seedling dipping recorded the highest cabbage yield (41.61 t/ha), which was 33.67% more than that obtained without Azospirillum application. The inoculation of Azospirillum along with 37.5 kg N and 25 kg P/ha increased the plant height, number of leaves, number of laterals and root diameter fresh and dry weight of root, number of berries and seed yield per hectare in Ashwagandha (Navamani and Bharathi 2002). The treatment combination of NPK

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along with Azospirillum was more effective in improving vegetative and floral characters of Dendrobium than NPK alone (Bhaskar et al. 2021). Ponnuswamy et al. (2002) recorded increased grain yield of 4830 kg/ha in rainfed sorghum by the application of recommended NPK, FYM and Azospirillum. Soil inoculation using Azospirillum improved seed germination, biometric characters and biochemical attributes such as chlorophylls, soluble carbohydrates, reducing sugars, total free amino acids, buffer soluble proteins and phenolics in silk cotton (Vijayakumari and Janardhanan 2003; Bashan et al. 2004). In culture medium, wild strain of Azospirillum brasilense was able to produce indole-3 butyric acid. The compound obtained from culture filtrate was able to increase growth of maize seedlings when sprayed on the crop under in vitro conditions (Martinez-Morales et al. 2003). Early germination, maximum shoot length, increased number of leaves and leaf area in radish was observed in the treatment which received Azospirillum inoculant with recommended close of 75% N and P, and 100% K (Kamalakannan and Manivannan 2003). The maximum increase in growth parameters and fruit and seed yield of ashwagandha treated with Azospirillum alone was recorded. Increase in vegetative growth of China aster by use of biofertilisers viz., VAM + PSB which might be related in simulating nutrient uptake and biosynthesis of plant growth regulators, thereby improving the growth and development process of the plant (Moradzadeh et al. 2021a, b). Bashan et al. (2004) reported reduction in the use of chemical fertilisers especially nitrogenous fertilisers up to 25% to 50% due to Azospirillum inoculation and incorporated with organic fertilisers. Madhaiyan et al. (2009) obtained increase in growth and nitrogen uptake of tomato, red pepper and rice by inoculation of Azospirillum brasilense, Methylobacterium oryzae and Burkoldevia pyrrocinia. The inoculation of Azospirillum with different levels of nitrogenous fertiliser significantly enhanced the growth and yield parameters in pearl millet. Nitrogen at 75% with Azospirillum was significantly higher in plant growth and grain yield parameters as compared to uninoculated control and inoculated control in pearl millet (Faridvand et al. 2021). A field experiment was conducted to study the effect of Azospirillum (ACD-15 and ACD-20) inoculation on nitrogen economy and yield of sorghum. The results revealed that Azospirillum strain ACD-20 combined with 75% nitrogen fertiliser yielded the highest grain yield (1847 kg/ha), total dry matter (8030 kg/ha), percent nitrogen content in sorghum plant (0.282%) and B:C ratio (4.77) compared to other treatments. Effect of Azospirillum biofertiliser on sugarcane yield was studied in a field experiment. The results revealed that the application of 75% nitrogenous fertilisers with Azospirillum has yielded higher cane compared to 100% RDN only. The higher yield was obtained (10% more) when Azospirillum was applied in two splits, i.e. at planting and 45 days after planting compared to only one application either at planting or 45 days after planting @ 5 or 10 kg/ha (Manasa et al. 2021). Rueda-Puente et al. (2004) reported that the pickle weed (Salicornia bigelovii) exhibited increases in growth parameters, biochemical characteristics, including

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total protein, ash and lipid content and yield parameters, when inoculated with Azospirillum halopraeferens. Seed inoculation with Azospirillum and high levels of nitrogen resulted significantly higher yields and increase in total nitrogen and total lipids content of the maize seeds in comparison to the control (Santa et al. 2004). Rueda-Puente et al. (2004) reported that the pickle weed (Salicornia bigelovii) exhibited increases in growth parameters, biochemical characteristics, including total protein, ash and lipid content and yield parameters, when inoculated with Azospirillum halopraeferens. Seed inoculation with Azospirillum and high levels of nitrogen resulted significantly higher yields and increase in total nitrogen and total lipids content of the maize seeds in comparison to the control (Najafi et al. 2021). The effect of Azospirillum on the total yield increase of field grown plants generally ranges from 10% to 30%. Several reports suggest that PGPR stimulate the plant growth by facilitating the uptake of nutrients such as nitrogen, potassium and phosphorous, and micronutrients by the plant. Azospirillum sp. Enhanced nutrient uptake from soil solution at faster rates and accumulated as dry matter at higher rates (Shaikh et al. 2016). Pectinolytic activity of Azospirillum cells contributed to an increased mineral uptake, which might be due to the hydrolysis of the middle lamellae without causing host cell collapse and accelerated water and nutrient uptake by the roots. Bekri et al. (1999) also showed substantial pectinase activity in Azospirillum irakense and explained their role of the enzyme in increasing the Azospirillum root colonisation (Patel et al. 2016b). Inoculation with efficient strains of Azospirillum enhanced the yield of CSH 5 and CO 24 sorghum while K-tall and USH1 showed negligible response. During the past 20 years, numerous reports of inoculant effect of Azospirillum on all kinds of crop plants have been published. A few reports indicate extremely higher values of 50–270% increase in yield over uninoculated controls (Jadhav et al. 2017). Moderate yield increase of 20% attributed to inoculation with Azospirillum was considered commercially valuable to modern agriculture, if obtained consistently. Plant height, number of primary and secondary branches and number of leaves increased in Coleus parviflorus by application of 60 kg N/ha along with Azospirillum 2 kg/ha at the time of planting. However, application of 100 kg N/ha along with 2 kg/ha of Azospirillum increased the foliar N, P, Ca and Mg. The improvement in plant height, number of leaves, leaf area index, shoot and dry matter was better in Coleus parviflorus inoculated with Azospirillum at 4 kg/ha at planting. Tuber yield and harvest index were also the highest. The seed treatment and seedling treatment with Azospirillum increased the growth parameter, ash content and total alkaloids in Ashwagandha (Khan et al. 2019). In culture medium, wild strain of Azospirillum brasilense was able to produce indole-3 butyric acid. The compound obtained from culture filtrate was able to increase growth of maize seedlings when sprayed on the crop under in vitro conditions (Martinez-Morales et al. 2003). The inoculation of Azospirillum along with 37.5 kg N and 25 kg P/ha increased the plant height, number of leaves, number of laterals and root diameter fresh and dry weight of root, number of berries and seed yield per hectare in Ashwagandha

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(Navamani and Bharathi 2002). The maximum increase in growth parameters and fruit and seed yield of Ashwagandha treated with Azospirillum alone was recorded. Sajid Nadeem et al. (2006) conducted a pot culture study to evaluate the effect of different PGPR strains on maize growth and ions uptake under salt stress conditions. Three salinity levels (4, 8 and 12/dSm) along with original EC were maintained in the pots using NaCl salt. Maize seeds inoculated with pre-selected strains (S5, S15 and S20) along with uninoculated control were sown in the pots (Ajar Nath Yadav and Sayyed 2019). Recommended doses of NPK were applied. In general, maize growth was decreased with the increase in salinity Results indicated that PGPR inoculation, even at higher EC (12/dSm), significantly increased shoot/root fresh weight, shoot/root dry weight, chlorophyll a, b and cartenoid contents, respectively. Similarly, inoculation restricted the uptake of Na+/Cl- ions and enhanced the accumulation of N, P and K in shoot compared to control. Among the three selected strains, S20 performed better at all EC levels. The growth promotion and increased ions uptake exhibited by strain S20 might be due to its high in vitro IAA production, chitinase activity, P – solubility and more intensive root colonisation, besides ACC-deaminase activity (Bahman Fazeli-Nasab and Sayyed 2019). Vinay et al. (2016) An in vivo study was conducted by Barassi et al. (2007) to study the response of Azospirillum (ACD-15 and ACD-20) inoculation along with reduced levels of nitrogenous fertiliser on the growth and yield of onion. The results revealed that both the strains (ACD-15 and ACD-20) individually as well as in combination with different levels of N increased the plant growth parameters viz., plant height, number of leaves, fresh and dry weight of plant and bulb yield significantly over the uninoculated control (Divjot Kour and Sayyed 2019) Among the different treatment combinations, the seed application of Azospirillum (ACD-20) along with 75% RDN produced maximum yield (82 q/ha) and was at par with 100% RDN (86 q/ha). Thus, they concluded that there was 25% saving in nitrogenous fertilisers along with increased productivity, beneficial flora of soil and improved soil health. Azospirillum strains have no preferences for crop plants or weeds, or for annual or perennial plants, and can be successfully applied to plants that have no previous history of Azospirillum in their roots Rasouli et al. (2020). Cassan et al. (2009) reported that Azospirillum brasilense promoted root growth and help to mitigate osmotic stress in rice seedlings, due to cadaverine production. The nitrogen fixing Rhizobacterium Azospirillum lives in close association with plant roots, where it exerts beneficial effects on plant growth and yield of many crops of agronomic importance (Enshasy et al. 2020). During the past 20 years, numerous reports of inoculant effect of Azospirillum on all kinds of crop plants have been published (Sridevi and Mallaiah 2007). The effect of Azospirillum inoculation on the total yield increases of field grown plants generally ranged from 10% to 30%. Several reports suggest that PGPR stimulate the plant growth by facilitating the uptake of nutrients such as N, P and K and micronutrients by the plant. Azospirillum sp. Enhanced nutrient uptake from soil solution at faster rates and accumulated as dry matter at higher rates (Bashan et al. 2004). Hoshang Naserirad et al. (2011) investigated the effects of biofertiliser on yield and its components of maize cultivars. Treatments were cultivar factor as main plots

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and biofertiliser factor (non-inoculation, inoculation with Azotobacter, Azospirillum and double inoculation of Azotobacter and Azospirillum) as subplots. Cultivar of SC704 had the highest plant height (201.1 cm), number of grains per row (42.8 grains), grain yield (10,850 kg/ha) and biological yield (22,040 kg/ha) compared with other cultivars (Sonawane et al. 2021). Double-inoculation of Azotobacter and Azospirillum had the highest plant height (212.4 cm), stem diameter (2.5 cm), number of rows per ear (14.5 row), number of grains per row (44.2 grain), 1000 grain weight (315.4 g), grain yield (10,190 kg/ha), biological yield (21,320 kg/ha) and protein content (10.7%) when compared with other treatments. The interaction effect of cultivar and plant growth promoting rhizobacteria (PGPR) on grain yield, biological yield and protein content was significant ( p < 0.01). The highest and lowest grain yield obtained from SC704 with double inoculation of Azotobacter and Azospirillum (12,320 kg/ha) and SC 604 with non-inoculation treatment (12,320 kg/ ha), respectively (Ahmed et al. 2021). Zakaria et al. (2019) Different crops inoculated with Azospirillum alone or in association with other microorganisms were promising particularly in crops such as sugarcane, sorghum and pearl millet and Moringa oleifera. Zayad (2012) and Jalilian et al. (2012) reported that combination of Azospirillum and other beneficial microbes recorded higher yield and quality of sunflower (Nasab et al. 2021). Noshin Ilyas et al. (2012) isolated and characterised Azospirillum strains from maize (Zea mays L.) grown under well watered and water stressed conditions and to evaluate the ability of bacteria to produce plant growth promoting hormones such as IAA, Gibberellic Acid, Trans-zeatin riboside and abscisic acid (Daniel Joe Dailin et al. 2021). A total of eight strains of Azospirillum were isolated from rhizosphere and roots of maize plants grown in pots and it was observed that survival efficiency of Azospirillum from well-watered plants was higher as compared to that of Azospirillum strains isolated from roots and rhizosphere samples of water stressed plants (having 8–12% soil moisture). Rajesh (2014) tested the effect of prepared liquid biofertilisers - Azospirillum, plant growth promoting rhizobacteria (PGPR) and Arbuscular Mycorrhizae (AM) in three different crop plants viz., maize, black gram and green gram. Plant growth parameters such as plant height, root length and plant weight were recorded. Plant height and weight of maize treated with PGPR significantly increased, i.e. 20 cm and 1.72 g respectively compared with the control. Root length was increased maximum in the plant treated with AM compared with the control, i.e. 18.5 cm. The study shows that the liquid biofertilisers are capable of promoting plant growth (Saranraj et al. 2021). Pragya Rathore (2014) screened the Azospirillum from the crop soils and biochemical characterisation was carried out. The effect of the isolated organism was studied on the germination of inoculated wheat. Azospirillum is a PGPB has been known to increase the productivity in terms of grain yield content and the growth of plant. The growth is stimulated because the organism also produces growth hormones like auxin. To study the effect of hormones on seed germination the seeds were inoculated with the organism and were allowed to germinate in 0.8% agar medium. Two times increase in germinated seed shoot length was observed. Pot

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culture study on wheat plant was also carried out which demonstrated significant increase in the shoot length, root length, fresh weight and dry weight. Subramanian et al. (2014) studied the influence of Azospirillum brasilense strain on morphometric characteristics of maize plants. On 30th and 40th day, pot culture of Zea mays with Azospirillum brasilense showed higher shoot and root growth, leaf length and breadth than the control plant. They have been found that inoculation of maize crops with an active strain of Azospirillum brasilense has a beneficial effect on maize vigour and yield under the identical climatic and soil conditions (Saranraj et al. 2022).

References Ahmed S, Choudhury AR, Kumar S, Choi RJ, Sayyed RZ, Sa TM (2021) Biomolecular painstaking utilization and assimilation of phosphorus under indigent stage in agricultural crops. In: Singh HB, Vaishnav A, Sayyed RZ (eds) Antioxidants in plant-microbe interaction. Springer, Singapore, pp 565–588 Akhtar N, Ilyas N, Yasmin H, Sayyed RZ, Hasnain ZA, Elsayed E, El Enshasy HA (2021) Role of Bacillus cereus in improving the growth and phytoextractability of Brassica nigra (L.) K. Koch in chromium contaminated soil. Molecules 26:1569 Albareda M, Rodnguez-Navarro DN, Camacho M, Temprano J (2008) Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biol Biochem 40:2771–2779 Alsulimani A, Hidalgo JR, Neske A, Sayyed RZ, Ameta KL (2021) Bis-and mono-substituted chalcones exert anti-feedant and toxic effects on fall armyworm Spodoptera frugiperda. Saudi J Biol Sci 28:5754–5759 Arora H, Sharma A, Sharma S, Farah F, Haron GA, Sayyed RZ, Datta R (2021) Pythium dampingoff and root rot of Capsicum annuum L.: impacts, diagnosis, and management. Microorganisms 9:823–830 Baba Hamid B, Sheikh TA, Alotaibi S, Enshasy HE, Ansari JA, Zuan ATK, Sayyed RZ (2021) Psychrotolerant Mesorhizobium sp. isolated from temperate and cold desert regions solubilize potassium and produces multiple plant growth promoting metabolites. Molecules 26:57–58 Barassi CA, Sueldo RJ, Creus CM, Carrozzi LE, Casanovas EM, Pereyra MA (2007) Azospirillum spp., a dynamic soil bacterium favorable to vegetable crop production. Dyn Soil Dyn Plant 1(2): 68–82 Bashan Y (1986) Enhancement of wheat root colonization and plant development by Azospirillum brasilense Cd. following temporary depression of the rhizosphere microflora. Appl Environ Microbiol 51:1067–1071 Bashan Y (1990) Current status of Azospirillum inoculation technology-Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608 Bashan Y, Dubrovsky JG (1996) Azospirillum spp. participation in dry matter partitioning in grasses at the whole plant level. Biol Fertil Soils 23:435–440 Bashan Y, Holguin G (1997) Nitrogen fixation and phytohormones production by Azospirillum. Can J Microbiol 54:560–568 Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology, a Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608 Bashan Y, Ream Y, Levanony HL, Sade A (1989) Non-specific response in plant growth yield and root colonization of non-cereal crop plants to inoculation with Azospirillum brasilense cd. Can J Bot 67:1317–1324 Bashan Y, Holguin G, De Bashan LE (2004) Azospirillum–plant relationships: physiological, molecular, agricultural and environmental advances (1997–2003). Can J Microbiol 50:521–577

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