Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection [1 ed.] 9819967406, 9789819967407

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Ravinder Kumar Muhammad Ahsan Altaf Milan Kumar Lal Rahul Kumar Tiwari   Editors

Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection

Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection

Ravinder Kumar • Muhammad Ahsan Altaf • Milan Kumar Lal • Rahul Kumar Tiwari Editors

Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection

Editors Ravinder Kumar Division of Plant Pathology ICAR-Indian Agricultural Research Institute New Delhi, India

Milan Kumar Lal Division of Crop Physiology Biochemistry and Post Harvest Technology ICAR-Central Potato Research Institute Shimla, Himachal Pradesh, India

Muhammad Ahsan Altaf Key Laboratory for Quality Regulation of Tropical Horticultural Crops of Hainan Province School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication) Hainan University Sanya, China Rahul Kumar Tiwari Division of Plant Protection ICAR-Central Potato Research Institute Shimla Himachal Pradesh, India

ISBN 978-981-99-6740-7 ISBN 978-981-99-6741-4 https://doi.org/10.1007/978-981-99-6741-4

(eBook)

# 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 Paper in this product is recyclable.

Preface

Recent years have seen a transformative renaissance in our understanding of melatonin's pivotal role in plant biology as a pleiotropic molecule. Initially recognized for its involvement in circadian rhythms and neuroendocrine regulation in animals, melatonin has captured the fascination of the scientific community due to its presence and multiple functions in plants. A pleiotropic molecule for abiotic stresses and pathogens, Melatonin in Plants depicts the complex interplay between melatonin and plant responses to abiotic stresses and pathogens. The chapters contained in this volume are the culmination of meticulous research and scholarly inquiry conducted by esteemed scientists and researchers who have dedicated themselves to unraveling the diverse roles of melatonin in plants. A comprehensive exploration of melatonin's effects on a variety of physiological processes, particularly plant responses to abiotic stressors and the activation of defense mechanisms against pathogens, is the purpose of this compendium. An in-depth understanding of the intricate molecular pathways of melatonin in plants is provided in the first section of the book. The following chapters present cutting-edge investigations into the pleiotropic effects of melatonin on plant responses to abiotic stresses, including drought, salinity, extreme temperatures, and heavy metal toxicity. The ability of melatonin to ameliorate the adverse effects of these environmental adversities reveals its potential as a potent bio-regulator for enhancing plant resilience. Moreover, the book describes how melatonin plays an important role in plant-pathogen interactions, revealing how it primes plant defense systems against a wide range of pathogens. These chapters provide compelling evidence of melatonin's importance in reducing the detrimental effects of plant diseases and improving global food security by elucidating the mechanisms through which it enhances plant immunity. In exploring the frontiers of melatonin research in plants, we invite readers on a journey of scientific discovery, enriched by multiple perspectives and methodologies. Our sincere hope is that this compilation will serve as an invaluable resource for students, researchers, and practitioners in the fields of plant biology, agriculture, and environmental science, inspiring further inquiry and application of melatonin-based strategies for sustainable agriculture and ecosystem management. Those who contributed to this pioneering compilation have shown unwavering dedication, expertise, and passion, and we are deeply grateful to them. Their v

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collective efforts have highlighted the profound role played by melatonin as a pleiotropic molecule in orchestrating the delicate balance between plant survival and adaptation in a dynamic and challenging environment. As a contribution to the advancement of plant science and sustainable agriculture, we present Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogens. In order to harness the potential of melatonin in strengthening plant resilience and ensuring a fruitful, secure future for our planet, I hope the knowledge and insights shared in this volume inspire new avenues of research. New Delhi, India Sanya, China Shimla, Himachal Pradesh, India Shimla, Himachal Pradesh, India

Ravinder Kumar Muhammad Ahsan Altaf Milan Kumar Lal Rahul Kumar Tiwari

Contents

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Evolution of Melatonin as an Oxidative Stress Mitigator in Plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Rahul Kumar Tiwari, Muhammad Ahsan Altaf, Ravinder Kumar, and Milan Kumar Lal Melatonin-Mediated Drought Stress Mitigation by Modulation of Physiological and Biochemical Responses in Plants . . . . . . . . . . . Hafiza Muniba Din Muhammad, Safina Naz, Ehsan Ali, Asif Nawaz, Hasan Sardar, Muhammad Ahsan Altaf, Sami Abou Fayssal, Pankaj Kumar, and Riaz Ahmad Reprogramming of Salt Stress Under the Influence of Melatonin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Safina Naz, Hafiza Muniba Din Muhammad, Saqib Ali, Muhammad Ahsan Altaf, Ishtiaq Ahmad, Sami Abou Fayssal, and Riaz Ahmad Mechanistic Insights on Melatonin-Mediated Heat Stress Regulation in Plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Muhammad Ahsan Altaf, Safina Naz, Hafiza Muniba Din Muhammad, Saqib Ali, and Riaz Ahmad

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Melatonin a Key Regulator of Cold Stress in Plants . . . . . . . . . . . . G. Vamsi Krishna, Lellapalli Rithesh, Bhanothu Shiva, and Sompalli Suresh Rao

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Illustrating Recent Development in Melatonin-Heavy Metal Research in Plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Abazar Ghorbani, Abolghassem Emamverdian, Mo-Xian Chen, Safina Naz, Hafiza Muniba Din Muhammad, Muhammad Ahsan Altaf, and Riaz Ahmad

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Contents

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Melatonin in Nutrient Use Efficiency of Regulation in Crop Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 Revati Wanikar, Sayanti Mandal, Priyanjali Dixit, Maya Khater, Mrunal Damle, Medha Dange, Rohini Yevale, Abdel Rahman Al-Tawaha, Mimosa Ghorai, and Abhijit Dey

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Melatonin-Mediated Signalling and Regulation of Viral and Bacterial Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133 Lanvin Rochal Kepngop Kouokap, Pierre Eke, Diane Yimta Youmbi, Reymond Fokom, Vanessa Nya Dinango, and Louise Nana Wakam

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Explicating the Role of Melatonin in the Mitigation of Fungal Diseases in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 Pierre Eke, Lile Christere Ngemnang Mabou, Danielle Ngongang Tchonang, Lanvin Rochal Kepngop Kouokap, Diane Yimta Youmbi, Vanessa Nya Dinango, and Reymond Fokom

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Role of Melatonin in Management of Stress Tolerance of Forest Tree Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177 K. Darshan, K. N. Harshitha, S. Shreedevasena, Aditi Tailor, Tanmaya Kumar Bhoi, Sonali Nigam, and Nitin Kulkarni

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Emerging Role of Melatonin in Integrated Management of Crop Pathogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195 Lellapalli Rithesh, Gokarla Vamsi Krishna, Sompalli Suresh Rao, and Bhanothu Shiva

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Exploring Melatonin’s Potential as an Alternative Strategy for Protecting Plants from Biotic Stresses . . . . . . . . . . . . . . . . . . . . 223 Tanmaya Kumar Bhoi, Ipsita Samal, Deepak Kumar Mahanta, J. Komal, Prasanta Kumar Majhi, and Ankur

Editors and Contributors

About the Editors Ravinder Kumar, Ph.D., Senior Scientist (Plant Pathology), ICAR-Central Potato Research Institute, Shimla, Himachal Pradesh, India has over 15 years of research experience on biotic and abiotic stresses management in plants, potato biotechnology particularly formulation of dsRNA for late blight, development of transgenic lines with ToLCNDV resistance, potato genetic resource management, developed several diagnostic tools like uniplex/multiplex RT-PCR, real-time RT-PCR, LAMP, and RT-RPA protocols for the detection of potato pathogens, molecular characterization and genome sequencing of plant pathogens. He has published over 120 research papers/reviews articles in national/international peer reviewed journals, training manuals and book chapters, edited Institute publications like newsletters and annual reports. He is the recipient of Awards like IPA-Kaushalya Sikka Memorial Award, IPA-Chandra Prabha Singh Young Scientist Award, Young Scientist Associate award, best oral/poster awards of different scientific professional societies. He is a member of editorial board in 10 international journals and Guest associate editor for many reputed International journals. Muhammad Ahsan Altaf completed his Ph.D. from the School of Life Science at Hainan University, China. He is currently employed as a postdoctoral researcher in the College of Horticulture, Hainan University, China. He has published around 50 research articles in top leading journals of the world, having high impact factor. His research interests are focused on the physiological, biochemical, and molecular aspects of horticultural plants, especially solanaceous vegetable crops. Dr Altaf is actively engaged in investigating the role of melatonin in photosynthetic efficiency and mineral nutrient uptake from root to shoot under abiotic stress conditions. Milan Kumar Lal, Doctor in Plant Physiology, works in the area of abiotic stress and the nutritional aspects of potato and other starchy crops at ICAR-Central Potato Research Institute, Shimla, India. He is an expert worker in the area of abiotic stress such as heat, drought salinity, and heavy metal. Moreover, he is also working on the aspect of effect of biotic stress such as fungus, virus, and bacteria on plant physiological, biochemical, and molecular responses. Apart from this, he also has expertise ix

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in the nutritional and quality aspects of starchy crops, including resistant starch, glycemic index, phytonutrients, functional fermented foods and beverages, bioactive compounds, and various processing techniques to enhance these components in food products of starchy crops. He is the recipient of prestigious awards such as the Best PhD Thesis Award, PhD Merit Medal Award, Young Researcher Award, and RD Asana Gold Medal Award. His findings have generated more than 120 publications in international peer-reviewed journals. Rahul Kumar Tiwari, Doctor in Plant Pathology, works as a scientist at ICARCentral Potato Research Institute, Shimla, India. The research work of Dr Tiwari is focused on the management of crop diseases, abiotic stress mitigation in horticultural crops, and the role of phytohormones in plant defense. His recent research findings on the impact of Fusarium dry rot disease on potatoes provide critical information on the pathogen, its genomics, and potential management strategies. Moreover, Dr Tiwari’s research on the development of one-step reverse transcription recombinase polymerase amplification (RT-RPA) assays for the detection of potato viruses has the potential to contribute significantly to the development of disease-free potato. His exceptional research work has been widely recognized and awarded, including the IARI Gold Medal Award for his outstanding Ph.D. research work and the Young Scientist Award. He has authored over 80 publications in highly acclaimed international and national peer-reviewed journals, book chapters, newsletters, and popular articles.

Contributors Ishtiaq Ahmad Department of Horticultural Sciences, The Islamia University of Bahawalpur, Bahawalpur, Pakistan Riaz Ahmad Department of Horticulture, The University of Agriculture, Dera Ismail Khan, Pakistan Ehsan Ali Department of Agri-Chemistry, The University of Agriculture, Dera Ismail Khan, Pakistan Saqib Ali Department of Entomology, The University of Agriculture, Dera Ismail Khan, Pakistan Muhammad Ahsan Altaf College of Horticulture, Hainan University, Haikou, China Abdel Rahman Al-Tawaha Department of Biological Sciences, Al-Hussein Bin Talal University, Maan, Jordon Ankur Department of Entomology, Maharana Pratap University of Agriculture and Technology, Udaipur, Rajasthan, India Tanmaya Kumar Bhoi ICFRE-Arid Forest Research Institute, Jodhpur, Rajasthan, India

Editors and Contributors

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Mo-Xian Chen National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, China Mrunal Damle Department of Biotechnology, MES Abasaheb Garware College (Autonomous), Pune, Maharashtra, India Medha Dange Department of Biotechnology, MES Abasaheb Garware College (Autonomous), Pune, Maharashtra, India K. Darshan Forest Protection Division, ICFRE-Tropical Forest Research Institute, Jabalpur, MP, India Vanessa Nya Dinango Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon Priyanjali Dixit Department of Biotechnology, MES Abasaheb Garware College (Autonomous), Pune, Maharashtra, India Pierre Eke Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon College of Technology, Department of Crop Production Technology, University of Bamenda, Bambili, North West Region, Cameroon Soil Microbiology Laboratory, Biotechnology Centre, Yaoundé, Cameroon Abolghassem Emamverdian Bamboo Research Institute, Nanjing Forestry University, Nanjing, China Sami Abou Fayssal Department of Agronomy, Faculty of Agronomy, University of Forestry, Sofia, Bulgaria Department of Plant Production, Faculty of Agriculture, Lebanese University, Beirut, Lebanon Reymond Fokom Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon Soil Microbiology Laboratory, Biotechnology Centre, Yaoundé, Cameroon Mimosa Ghorai Department of Life Sciences, Presidency University, Kolkata, West Bengal, India Abhijit Dey Department of Life Sciences, Presidency University, Kolkata, West Bengal, India Abazar Ghorbani National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, China

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Editors and Contributors

K. N. Harshitha Department of Plant Pathology, College of Agriculture, V. C. Farm, Mandya, Karnataka, India Maya Khater Department of Biotechnology, MES Abasaheb Garware College (Autonomous), Pune, Maharashtra, India J. Komal Department of Entomology, Navsari Agricultural University, Navsari, Gujarat, India Lanvin Rochal Kepngop Kouokap Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon Nitin Kulkarni Forest Protection Division, ICFRE-Tropical Forest Research Institute, Jabalpur, MP, India Pankaj Kumar Agro-Ecology and Pollution Research Laboratory, Department of Zoology and Environmental Science, Gurukula Kangri (Deemed to Be University), Haridwar, Uttarakhand, India Ravinder Kumar ICAR-Indian Agricultural Research Institute, New Delhi, India Milan Kumar Lal ICAR-Central Potato Research Institute, Shimla, HP, India Lile Christere Ngemnang Mabou Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon Deepak Kumar Mahanta Department of Entomology, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India Prasanta Kumar Majhi Department of Genetics and Plant Breeding, Odisha University of Agriculture and Technology, Bhubaneswar, Odisha, India Sayanti Mandal Department of Chemistry & Biochemistry, Sharda School of Basic Sciences & Research, Sharda University, Greater Noida, India Hafiza Muniba Din Muhammad Department of Horticulture, Bahauddin Zakariya University, Multan, Pakistan Asif Nawaz Faculty of Agriculture, The University of Agriculture, Dera Ismail Khan, Pakistan Safina Naz Department of Horticulture, Bahauddin Zakariya University, Multan, Pakistan Sonali Nigam Department of Botany and Microbiology, St. Aloysius College, Jabalpur, MP, India Sompalli Suresh Rao Department of Plant Pathology, ANGRAU, Andhra Pradesh, India

Editors and Contributors

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Lellapalli Rithesh Department of Plant Pathology, College of Agriculture, Thiruvananthapuram, KAU, Thiruvananthapuram, Kerala, India Ipsita Samal ICAR-National Research Centre on Litchi, Mushahari, Muzaffarpur, Bihar, India Hasan Sardar Department of Horticulture, Bahauddin Zakariya University, Multan, Pakistan Bhanothu Shiva Regional Agricultural Research Station, ANGRAU, Guntur, Andhra Pradesh, India S. Shreedevasena Directorate of Medicinal and Aromatic Plants Research (DMAPR), Anand, Gujarat, India Sompalli Suresh Rao Department of Plant Pathology, College of Agriculture, Tirupathi, ANGRAU, Guntur, Andhra Pradesh, India Aditi Tailor ICFRE-Arid Forest Research Institute, Jodhpur, Rajasthan, India Danielle Ngongang Tchonang Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon Rahul Kumar Tiwari ICAR-Central Potato Research Institute, Shimla, HP, India G. Vamsi Krishna Department of Plant Pathology, College of Agriculture, Bapatla, ANGRAU, Guntur, Andhra Pradesh, India Louise Nana Wakam Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon Soil Microbiology Laboratory, Biotechnology Centre, Yaoundé, Cameroon Revati Wanikar Department of Biotechnology, MES Abasaheb Garware College (Autonomous), Pune, Maharashtra, India Rohini Yevale Department of Biotechnology, MES Abasaheb Garware College (Autonomous), Pune, Maharashtra, India Diane Yimta Youmbi Antimicrobial & Biocontrol Agents Unit (AmBcAU), Laboratory for Phytobiochemistry and Medicinal Plants Studies, Department of Biochemistry, University of Yaoundé I, Yaoundé, Cameroon

Abbreviations

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O2 ABA AMT APX ATP CAT CBFs CKs COMT1 CRISPR CWI DHAR EC ETIs FAD2 GA GABA GM GPX GR GSH H2O2 HM HSFs HSPs IAA JA MAPK MDA MDHAR MEL MIR NBS-LRR

Singlet oxygen Abscisic acid Ammonium transporters Ascorbate peroxidase Adenosine triphosphate Catalase C-repeat-binding factors Cytokinins Caffeic acid o-methyltransferase 1 Clustered regularly interspaced short palindromic repeats Cell wall invertase Dehydroascorbate reductase Electrical conductivity Effector-triggered immunity Fatty acid desaturase Gibberellin Gamma-aminobutyric acid Gene manipulation Glutathione peroxidase Glutathione reductase Glutathione Hydrogen peroxide Heavy metals Heat shock transcription factors Heat shock proteins Indole-3-acetic acid Jasmonic acid Mitogen-activated protein kinase Malondialdehyde Monodehydroascorbate reductase Melatonin Melatonin-mediated induced resistance Nucleotide-binding site leucine-rich repeat xv

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NiR NO PAL PAMPs POD PSI PSII PTI QTL RNS ROS RWC SA SAMDC SAR SNAT SOD T5H TDC TPH ZFPs

Abbreviations

Nitrite reductase Nitric oxide Phenylalanine ammonia-lyase Pathogen-associated molecular patterns Peroxidase Photosystem I Photosystem II PAMP-triggered immunity Quantitative trait loci Reactive nitrogen species Reactive oxygen species Relative water content Salicylic acid S-adenosylmethionine decarboxylase Systemic acquired resistance Serotonin N-acetyltransferase Superoxide dismutase Tryptamine 5-hydroxylase tryptophan decarboxylase Tryptophan hydroxylase Zinc finger proteins

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Evolution of Melatonin as an Oxidative Stress Mitigator in Plant Rahul Kumar Tiwari, Muhammad Ahsan Altaf, Ravinder Kumar, and Milan Kumar Lal

Abstract

In diverse crop plants under a variety of adverse conditions, melatonin, a versatile and potent molecule, plays a significant role in reducing oxidative stress. A number of studies have demonstrated its ability to mitigate various abiotic stresses, such as drought, extreme temperatures, and salinity. As an antioxidant, melatonin plays a crucial role in this context. The antioxidant properties of melatonin reduce the oxidative damage caused by reactive oxygen species to cellular components, such as lipids, proteins, and nucleic acids. By protecting cellular membranes and enhancing their functionality, it enhances plant resilience under stress. Furthermore, melatonin promotes carbohydrates metabolism under stress conditions by increasing photosynthetic efficiency. It preserves the process of converting light energy into carbohydrates by safeguarding the photosynthetic machinery. The protection provided by photosynthesis ensures the availability of energy and metabolic intermediates for growth and development, regardless of the environmental conditions. Also, melatonin affects carbohydrate metabolism, carbon assimilation, and ATP synthesis by modulating enzyme activity. In addition, it influences sugar transport, which is crucial to carbohydrate metabolism and overall energy distribution, particularly during times of stress. Overall,

R. K. Tiwari ICAR-Central Potato Research Institute, Shimla, HP, India M. A. Altaf Hainan University, Haikou, China R. Kumar (✉) Division of Plant Pathology, ICAR-Indian Agricultural Research Institute, New Delhi, India M. K. Lal ICAR-Indian Agricultural Research Institute, New Delhi, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Kumar et al. (eds.), Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection, https://doi.org/10.1007/978-981-99-6741-4_1

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melatonin is an important mitigator of oxidative stress in crop plants. As a valuable tool for improving stress resilience and productivity in agriculture, melatonin is capable of combating oxidative damage, maintaining photosynthetic efficiency, and modulating carbohydrate metabolism. In an era of increasing environmental stress, further research into its mechanisms and potential applications could be highly advantageous. Keywords

Carbohydrate metabolism · Lipid peroxidation · Redox · Ionic homeostasis · Reactive species

1.1

Introduction

Melatonin (N-acetyl-5-methoxytryptamine) is a versatile plant regulator found in all living organisms (Hernández-Ruiz and Arnao 2018; Altaf et al. 2023). It was originally identified as a neurohormone secreted by the pineal gland in vertebrates (Lee et al. 2003). As a vital animal hormone involved in circadian rhythms, body temperature, appetite, sleep, the immune system, seasonal reproduction, and tumorigenesis, melatonin is now recognized as one of the most important hormones. Two independent research groups discovered melatonin in plants (Dubbels et al. 1995; Hattori et al. 1995) and this led to significant research into melatonin extraction, quantification, and physiological functions (Tan and Reiter 2020; Tiwari et al. 2020a, 2021b, 2022; Altaf et al. 2022b, 2023). The term “phytomelatonin” was introduced in 2004 to refer to plant-derived melatonin, and subsequent studies have established its diverse functions in regulating plant growth, seed germination, cell respiration, photosynthesis, and osmoregulation (Reiter et al. 2009; Tan and Reiter 2020). In addition to stimulating rhizogenesis, morphogenesis, and caulogenesis, melatonin also plays an important role in caulogenesis. Plants use melatonin as a phytoprotectant against various abiotic stresses, which is one of its most important roles. It has been found that it reduces the effects of drought and heat (Wei et al. 2017; Buttar et al. 2020; Jahan et al. 2021), salinity (Altaf et al. 2020; Li et al. 2012; Kostopoulou et al. 2015; Wang et al. 2016), cold (Bajwa et al. 2014; Ding et al. 2017a, b; Jannatizadeh 2019; Sharafi et al. 2019), and heavy metal toxicity (Kaya et al. 2020; Ahammed et al. 2020). Climate change exposes plants to a wide range of biotic as well as abiotic stresses, which pose threats to their growth and productivity (Kumar et al. 2017, 2019, 2022a, b). There is a strong correlation between reactive oxygen species (ROS) and oxidative stress on a molecular level. As a result of biotic or abiotic stresses, ROS like hydrogen peroxide (H2O2), singlet oxygen (11O2), and superoxide radicals like hydroxyl radicals can accumulate in plants, including oxygen radicals and their derivatives, such as hydrogen peroxide (H2O2) and singlet oxygen (11O2) (Tiwari et al. 2020b, 2022). In addition to the fact that ROS are highly reactive, they can also cause damage to plants due to their toxic effects. During the oxidation process, ROS

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Evolution of Melatonin as an Oxidative Stress Mitigator in Plant

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can damage cells by oxidizing proteins, lipids, and DNA, which can result in the death of cells. Recent studies have shown that ROS play an important role in early signaling events in plants, triggered by normal metabolic functions and environmental stressors (Tiwari et al. 2021a, 2022; Devi et al. 2022; Lal et al. 2022b; Mangal et al. 2022). ROS production and their elimination are delicately balanced under normal circumstances. There are, however, different biotic and abiotic stresses that can disrupt this balance, leading to significant increases in ROS levels that must be countered by antioxidant defense mechanisms within plant cells. It has become a critical objective for plant biologists to enhance these antioxidant defense systems in plants Kumar et al. (2021a, b). By maintaining ionic homeostasis and preventing adverse effects such as cell membrane damage, protein and DNA denaturation, lipid peroxidation, carbohydrate oxidation, pigment breakdown, and aberrant enzyme activity, melatonin maintains ionic homeostasis and prevents reactive oxygen species (ROS) and reactive nitrogen species (RNS) generated during stress (Tan et al. 2007; Reiter et al. 2009; MoustafaFarag et al. 2020). The plant’s inherent antioxidative defense system is also activated by melatonin by upregulating genes that help produce enzymes like superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), ascorbic acid (ASA), and glutathione (GSH) when stressed (Sun et al. 2019). There is also evidence that upregulation of genes involved in the ASA-GSH cycle, which protects the plant against stress, is well established (Altaf et al. 2021a, b). A number of previous studies have found that melatonin inhibits viral and fungal infections in animals both directly and indirectly (Vielma et al. 2014; Tiwari et al. 2021a). Numerous studies have demonstrated melatonin’s ability to inhibit plant pathogens indirectly and elicit systemic acquired resistance in crops (Zhang et al. 2017; Zhao et al. 2019; Sun et al. 2019). The protective properties of melatonin have been demonstrated in plants against viruses, fungal pathogens, bacterial pathogens, insects, and parasitic nematodes in crops (Zhang et al. 2017; Zhao et al. 2019; Sun et al. 2019). Plant defense is regulated by a number of processes, including activation of defense genes, scavenging of reactive oxygen species (ROS) and reactive nitrogen species (RNS), thickening of the cell wall, and hormonal interaction (Kumar et al. 2020; Altaf et al. 2022a; Behera et al. 2022; Devi et al. 2022; Lal et al. 2020, 2022c). Melatonin increases callose deposition and cellulose, galactose, and xylose accumulation in plants, leading to a series of biochemical defense responses against fungal pathogens (Sun et al. 2015; Qian et al. 2015). It has been reported that the melatoninmediated systemic acquired resistance (SAR) is activated by salicylic acid (SA) and jasmonic acid (JA), which are crucial for preventing viral diseases (Tiwari et al. 2022; Altaf et al. 2023). Additionally, plant defense responses are induced by melatonin and serotonin working synergistically (Saremba et al. 2017). It is necessary to investigate further the molecular mechanism underlying this synergistic interaction, as this interaction has not yet been fully investigated. Phytomelatonin is well known and documented for its protective effects against abiotic stress, but the

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effects on biotic tolerance have been less well recognized and documented. A greater understanding and appreciation of phytomelatonins potential in plants facing biotic stress requires additional research. A major goal of this chapter is to explain how melatonin helps plants in mitigating pathogen infections and abiotic stresses through regulation of the antioxidative and oxidative defense systems. In addition, the chapter discusses how hormonal cross-talk is mediated by melatonin and influences the triggering of immune responses by PAMPs and ETIs. Furthermore, recent studies investigating the synergistic interaction between melatonin and other phytoprotectants are discussed, underscoring the potential of melatonin as a multifunctional phytoprotectant in sustainable crop production systems.

1.2

Oxidative Stress: The Phenomenon and Associated Effects

Oxidative stress occurs when free radicals and reactive metabolites, known as oxidants, are produced in excess and their elimination is not balanced by protective mechanisms called antioxidative systems (Palma et al. 2002; Vielma et al. 2014). Damage to vital biomolecules and plant tissues and organs can result from this imbalance, potentially affecting the entire body. The redox state of cells and organisms is affected by oxidative and antioxidative processes (Reiter et al. 2009; Antoniou et al. 2017). By altering redox state, various signal proteins can be stimulated or inhibited, affecting signal pathways that impact cellular function. Many studies have shown that oxidative stress does not always damage cells. Oxidative stress can play a role in regulating other essential processes depending on the type of oxidant, the intensity and duration of redox imbalance, and the type of cell involved (Zhang and Zhang 2014; Miryeganeh 2021; Altaf et al. 2022a). Modulation of signal pathways, modulation of antioxidant enzyme synthesis, enhancement of repair processes, modulation of inflammation, and modulation of apoptosis (programmed cell death) are all part of this process. Physiological and pathological processes in the plants can be affected by the intricate balance between oxidative stress and cellular responses to it (Lei et al. 2004). Oxidative stress is a general stress response that results in cell damage and dysfunction when environmental or biotic stresses are present. In reactive oxygen species (ROS), excess molecules containing activated oxygen are produced and accumulate, resulting in oxidative stress. Oxidative stress is caused by two main factors: Disruption of normal cell physiology causes an imbalance between ROS generation and detoxification. As part of the defense and adaptation process, ROS are synthesized de novo during stress signaling. Some stress factors directly produce ROS, contributing to oxidative stress, allowing both mechanisms to coexist (Demidchik 2012; Bian et al. 2021). Oxidative stress is induced by reactive oxygen species (ROS) in biological systems. There are several ROS that can be produced, including the singlet oxygen (1O2), hydroxyl radicals (OH), hydrogen peroxide (H2O2), superoxide radicals (O•-2), and nitric oxide (NO•) (Demidchik 2012). Oxidative stress may also be caused by other ROS, such as peroxyl, alkoxyl, and hydroperoxyl radicals, peroxynitrite, ozone, and hypochlorous acid.

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Triplet oxygen (O2) can undergo a process where it loses its “spin restriction” by accepting a single electron. This electron acceptance can occur due to various reasons, such as the “leak” of electrons in the plant’s electron transport chain (ETC) or the functioning of NADPH oxidase. As a result of this process, O2 transforms into a highly reactive species known as superoxide radical (O•-2). This radical is often referred to as “superoxide anion radical,” “superoxide radical anion,” “superoxide radical,” or simply “superoxide.” The increased reactivity of superoxide makes it an important player in oxidative stress and various biological processes (Chen et al. 2019; Allen 2003). In comparison with superoxide, hydroxyl, and singlet oxygen, hydrogen peroxide (H2O2) is a weak acid without unpaired electrons. The lifespan of H2O2 in living tissues is not overly long (60% annual agricultural production boost by 2050, to meet the demand of projected nine billion world population (Alexandratos and Bruinsma 2012). Paradoxically, the low-income socio-economic strata seem to be the most vulnerable. Their inability to get access to enough food is fostered by natural resource depletion, land-use conflicts, coupled

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to the local population growth. To uphold the promise of safe and secured food provision, better disease surveillance, accurate predictive forecasting models and proper and effective disease control strategies to protect our future harvests are urgently advocated (Avery et al. 2019).

9.3

Plant Defensive Weaponry Against Fungal Pathogens

To combat pathogens, plants have evolved a sophisticated mechanism known as plant immune response. The so-called plant–pathogen interaction has always been regarded as an open warfare, whose weapons are low-molecular-mass compounds and proteins synthesized by both plant and pathogen. The outcome of each battle often results in the establishment of resistance or pathogenesis. As a result, plants have evolved structural and biochemical barriers to prevent fungal ingresses. The physical barriers are made up of waxes, special trichomes and tight cuticles that prevent pathogens from adhering to plant surfaces and entry into the tissues (Moustafa-Farag et al. 2019; Gul et al. 2022; Moon and Ali 2022). Upon successful invasion of the outer layer of plant defense system, the pathogen is recognized via two main pathways leading to the activation of the biochemical barrier. The initial phase involves the plant pattern recognition receptor (PRRs) found on plant cell surface, which automatically detects the pathogens’ epitope named pathogenassociated molecular patterns (PAMPs), such as bacterial lipopolysaccharides and fungal chitin and trigger the so-called PAMP-triggered immunity (PTI) (Khan et al. 2021). The second pathway named effector-triggered immunity (ETI) is triggered upon recognition of fungal effectors (avirulent proteins) by protein receptors (R protein) that contain nucleotide-binding domains and leucine-rich repeats (NLRs) (Agrios 2005; Shahid et al. 2019; Khan et al. 2021) (Fig. 9.1). This other recognition activates a cascade of defense responses within the plant cell leading oftentimes to the activation of the hypersensitive reaction (HR) marked by the programmed death of infected and surrounding cells aiming to confine the fungus and restrict the disease progress (Monaghan and Zipfel 2012). A number of phytohormones, encompassing jasmonic acid (JA), ethylene (ET), and salicylic acid (SA), are particularly involved in the signaling network provoked by both ETI and PTI. Hence, the SA-related immune response, namely systemic acquired resistance (SAR), is put in place after primary infection with a necrotizing pathogen is accompanied by accumulation of SA and pathogenesis-related proteins (PR-proteins) (Khan et al. 2021). While the JA and ET pathways trigger the well-known induced systemic resistance (ISR), the SAR pathway is activated in response to non-pathogenic microorganisms (Khan et al. 2021). The JA, SA and ET pathways often result in the upregulation of defence-related genes with subsequent biosynthesis of antimicrobial end-products such as phenolics, proteins, carbohydrates phytoalexin, phytoanticipins, etc. (Fortunati et al. 2019). Failure of these substances to suppress the disease entails the use of exogenous fungicides to support the plant’s immune system.

Explicating the Role of Melatonin in the Mitigation of Fungal Diseases in Plants

Fig. 9.1 Effector-triggered immunity (ETI) and pathogen-associated molecular pattern (PAMP) triggered immunity (PTI). PTI is mainly stimulated by pattern recognition receptors (PRRs) located at the surface of plant cells, capable of recognizing PAMPs and triggering non-specific defense responses (basal defense responses) in plants. The PTI-mediated signaling involves reactive oxygen species (ROS), reactive nitrogen species (RNS), calcium, and some intermediates of the mitogen activated protein kinases (MAPKs) pathway. The plant R proteins recognize effector proteins produced by pathogenic fungi and other microbes and initiate ETI, which can make plants produce specific defense responses

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Synthetic Fungicides: The Historical Solution of Crop Fungal Diseases

Over time, tremendous efforts have been deployed to ward off fungal pathologies in agriculture. Fungicide usage, the adoption of resistant cultivars, and transgenic cultivars with high yielding and resistance genes are some of the ways that are often used (Oliver and Hewitt 2014; Finckh 2008). Recently, there has been increased interest in the use of biological control agents, which are microbial agents capable of suppressing phytopathogens by either releasing antibiotics or activating plant innate defence against plant diseases (Koehl et al. 2011; Kohl et al. 2019). However, fungicides remain the most potent and widespread weapon against fungal pathogens. The latter have been employed for over two centuries to mitigate or eradicate plants fungal infections. Primarily coined to protect grape-vines and cereals, the range of fungicides brands and active ingredients available, the frequency of their use and their effectiveness, the number crop diseases targeted have augmented tremendously, especially upon the Second World War. To date, some 150 different fungicidal molecules, formulated and sold in a several-fold larger number of different proprietary products, are spread in all agricultural basins worldwide (Brent and Hollomon 2007). Our heavy reliance on fungicides could be wellexemplified by the revenues engendered by these compounds in the world market. In fact, the monetary value of the fungicides market accounted for approximately 7.4 billion US dollars in 2005. A value that raised steadily to reach ~13.4 billion USD in 2019 and is projected to grow at the rate of 4.7% per annum till the years 2026 (Phillips McDougall, Industry Overview, 2005, https://www.alliedmarketres earch. com/fungicides-market). Europe alone consumes almost 50% of the fungicide produced annually as it is also the most subjected to fungal diseases and substantial economic damages to crops. Estimates suggest that fungicides application provides about 90% or greater control of the targeted disease, securing at least 3:1 benefit: cost ratio to farmers (Brent and Hollomon 2007). The value of fungicides could further be illustrated by the drastic drop of economic costs in controlling Zymoseptoria tritici, causing Septoria tritici blotch in wheat from 20% to 5–10% in the UK (Fones and Gurr 2015). To date, azoles, strobilurins, and succinate dehydrogenase inhibitors account for more than 77% of the overall fungicides on the world market place. In spite of their specificity and the effectiveness toward a vast array of major plant fungal pathogens, these two dominant groups and single target site fungicides come with higher risk of resistance and subsequent upsurge of more virulent fungal races (Oliver and Hewitt 2014). Indeed, point mutations in the active center of their target molecule can lead to strong fungicide resistance within few years of field usage (Oliver and Hewitt 2014). Such situation represents a threat not only to the agricultural sector but to clinical applications with cross-over of resistance from crops to clinical settings, evidenced by the emergence of multidrug-resistant strains (Aspergillus fumigatus for instance) (Fisher et al. 2018). Overall, intensive agriculture has rather heightened the challenge of fungal disease, whereby planting of vast swathes of genetically uniform crops, safeguarded by few inbred resistance genes, and protected from diseases with single target site antifungals, has hastened surge of fungicide-resistant strains (Fisher et al. 2018).

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Plant Priming: A Promising Eco-Friendly Alternative to Chemical Fungicides

The increasingly stricter legislation noticed in current days has fostered steady disinterest regarding the utilization of efficient pesticides and the advocacy of safer measures to control fungal infections in crops. Consequently, studies are being carried out aiming at developing non-chemical alternatives for pests and diseases control. The so-called non-chemical strategies including cultural, genetic, and biological controls rely primarily upon strengthening of the plant immune response using exogenous compounds or metabolites which activate complex networks of the plant communication system (Hernández-Ruiz et al. 2023). Biological elicitors, standing for natural molecule that mimics a pathogen attack or a state of danger in plant cells are promising eco-friendly strategy for crops protection (Burketova et al. 2015). These biodegradable, nontoxic, and biocompatible biological and biologicallike molecules have gained widespread acceptance as effective and biological means to help plants survive fungal ingresses (Iriti and Faoro 2008). In this regard, chitosan, chitin, and others have been utilized to prime agriculturally important crops both as plant growth promoters and to help eradicate or mitigate diseases (Savvides et al. 2016). Accordingly, melatonin, pleiotropic naturally occurring biomolecule represents an excellent candidate (Burketova et al. 2015; Hernández-Ruiz et al. 2023).

9.6

State of the Art on Melatonin and Its Functions in Plants

To cope with environmental stressors, in order to effectively complete their life cycle, plants produce a set of destressing biomolecules. One of the most reputed plant destressers is melatonin (N-acetyl-5-methoxytryptamine). Also called phytomelatonin, this hormone-like compound was chronologically discovered in animals (1958), then in microbes (1991) and lastly in plants (1995) in which it regulates almost all physiological and biochemical processes (Hattori et al. 1995; Kolar et al. 1995). Research on melatonin has drawn the attention of many research teams all over the globe. Thus, their capability to alleviate the deleterious effects of abiotic (waterlogging, salinity, UV-radiation, drought, heavy metal, cold, mineral imbalance and heat) and biotic (weeds, parasitic nematodes insects, viruses, bacteria, and fungi) stressors in several plants species has been widely proven (Arnao and Hernández-Ruiz 2015, 2020, 2021). Similarly as in animal cells, several in vitro and in vivo attempts have demonstrated the direct antioxidant potential of melatonin, thanks to its free radical scavenging ability, specifically the reactive oxygen (ROS) and nitrogen species (RNS) (Reiter et al. 1993; Melchiorri et al. 1995; Arnao and Hernández-Ruiz 2019). Phytomelatonin has also been shown to trigger the upregulation of various transcription factors implicated in the biosynthesis and accumulation of antioxidant enzymes including but not limited to catalases (CAT), peroxidases (POX), superoxide dismutases (SOD), and those comprise in the ascorbate-glutathione cycle (Arnao and Hernández-Ruiz 2019; Li et al. 2020; Tan

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et al. 2020). Melatonin can down- or upregulate transcription factors related to the metabolism or the regulation of the levels and functions of key plant phytohormones, namely jasmonic acid (JA), salicylic acid (SA), ethylene (ET), cytokinins (CK), abscisic acid (ABA), gibberellins (GA), indole acetic acid (IAA), and so on (Arnao and Hernández-Ruiz 2018, 2020, 2021). Subsequently, melatonin has been pinpointed to play a role in photorespiration, photosynthesis, stomatal behavior, osmoregulation, secondary metabolism, delayed senescence, and induction of parthenocarpy and extended shelf-life of fruits (Arnao and Hernández-Ruiz et al. 2021). Melatonin is found in plant species belonging to 35 different families, the most representative being Bromeliaceae, Basellaceae, Amaryllidaceae, Araceae, Actinidiaceae, Musaceae, and Asparagaceae (Mannino et al. 2021). This multipurpose molecule can be stored in flowers, leaves, seeds, sprouts, bulbs, fruits, roots, and specialized tissues (Altaf et al. 2022, 2023; Mannino et al. 2021). Its concentration in plant varies from undetectable to very high (Hardeland 2016). Current studies have shown that plants can synthesize melatonin in different ways in the mitochondria, chloroplast, and cytoplasm (Fig. 9.2) (Back et al. 2016; Tan and Reiter 2020). The biosynthesis of melatonin is essentially divided into two steps, namely tryptophan to serotonin and serotonin to melatonin.

9.7

Melatonin Interlay with Key Modulators of Plant Immunity

The molecular similarity between melatonin and auxin has motivated pioneer studies on the interaction of melatonin with other phytohormones (Okazaki et al. 2009). A lot of researchers have established the intriguing connections between melatonin and nearly all known plant phytohormones, including but not limited to classical hormones (gibberellin, auxin, abscisic acid, cytokinins), brassinosteroids, strigolactones, and more recent hormones such as polyamines, JA, SA, the major players of plant immunity (Zuo et al. 2014). To the best of our knowledge, the very first attempt aiming at deciphering the melatonin’s ability to induce resistance to plant fungal infection was published by Yin et al. 2013, whereby melatonin was found to successfully mimic the harmful effects of Diplocarpon mali in apple plant followed by the activation of the crop innate immunity. Thereafter, Glazebrook (2005) pointed out the roles played by the jasmonic acid (JA)/ethylene-related and salicylic acid (SA)-related signaling cascades on both plant PTI and ETI. Increasing evidences claim the subsequent capabilities of melatonin to reinforce plant resistance toward biotic aggressors causing serious crop yield shortfalls and economic damages to farmers (Arnao and Hernández-Ruiz 2014, 2015; Weeda et al. 2014; MoustafaFarag et al. 2020). The sensing, signal transduction, as well as mode of actions of the melatonin-induced strengthened immune response has been investigated in detail using Arabidopsis model plant. Indeed, Lee et al. (2014) utilized the ArabidopsisP. syringae model to establish the melatonin-mediated upregulation of pathogenrelated, SA- and ethylene-dependent genes, while the reverse was recorded in SA and ET signaling defective mutants, suggestive of a SA-melatonin interaction to influence plant response to pathogens (Hernández-Ruiz and Arnao 2018). One year

MITOCHONDRION

Predominant pathway under stress condions

CHLOROPLAST

TPH

Tryptophane

TDC

SHIKIMIC ACID PATHWAY

Predominant pathway under normal condions

Explicating the Role of Melatonin in the Mitigation of Fungal Diseases in Plants

Fig. 9.2 Phytomelatonin biosynthetic pathway in chloroplasts and mitochondria. (a) Schematic of melatonin biosynthetic pathways. (b) Molecular structures of key intermediate products in the melatonin biosynthetic pathway. Plants usually synthesize melatonin in chloroplasts under normal conditions. If this pathway

b

a

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Fig. 9.2 (continued) is blocked, melatonin biosynthesis may be switched to mitochondria. Trp tryptophan, 5-HT 5-hydroxytryptamine, 5-HTP 5-hydroxytryptophan, aHT N-acetyl-5- hydroxytryptamine, 5-MT 5-methoxytryptamine, MT melatonin, TDC tryptophan decarboxylase, T5H tryptamine 5-hydroxylase, SNAT serotonin N-acetyltransferase, ASMT N-acetylserotonin-O-methyltransferase (plant type SNATs and ASMTs appear to have origins distinct from the origins in animals), COMT caffeic acid O-methyltransferase, TPH tryptophan hydroxylase, AADC aromatic amino acid decarboxylase, AANAT arylalkylamine N-acetyltransferase (also known as arylamine N-acetyltransferase), and HIOMT hydroxyindole-O-methyltransferase (also known as N-acetylserotonin O-methyltransferase)

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later, the same authors indicated that the knockout of SNAT gene in Arabidopsis displayed augmented vulnerability to P. syringae as a result of lowered SA levels and subsequent downregulation of several defense genes like PDF1.2, ICS1, and PR1 (Lee et al. 2015). Moreover, melatonin has been shown to suppress ethylene in cucumber inoculated with cucumber mosaic virus (CMV) diminishing therefore the infectivity and symptoms expansion (Ma and Ma 2016; Sharif et al. 2018). A genome-wide comprehensive study undergone in melatonin-treated Arabidopsis model further established the upregulation of ET, SA, and JA signal transduction upon melatonin treatment pinpointing once more the strong interplay between melatonin and these hormones (Lee et al. 2014). As an intermediary messenger, the above phytohormones act on the DNA by enhancing the expression of enzymes encoding genes implicated in the gossypol, phenylpropanoid, and mevalonate (MVA) pathways, leading to the accumulation of membrane reinforcing molecules such as lignin and gossypol (Li et al. 2019a), the boosted biosynthesis of several fungal cell wall depredating enzymes (β-1,3-glucanase, chitinase), and antimicrobial proteins (pathogenesis-related proteins; PR1, PR3, and PR6) and triggered biosynthesis of structural and direct antimicrobial phenolic compounds through the upregulation of the phenylalanine ammonia-lyase (PAL), the master enzyme of the overall phenylpropanoid pathway (Yin et al. 2013; Sun et al. 2021). It is worth noting that the melatonin-induced resistance toward biotic stress is a consensus action of antioxidant enzymes, endogenous hormones, and the expression of antimicrobials (Lee et al. 2015). Pathogen assaults are often accompanied by a rise in the cytoplasmic content of melatonin. The melatonintriggered plant response to fungal infections must therefore include additional players as there is no direct correlation between fungal infection and melatonin production (Arnao and Hernández-Ruiz 2015).

9.7.1

Melatonin Interplay with the MAPK Signaling Pathways

The mitogen-activated protein kinase (MAPK) cascades is one of the most important and extremely preserved pathways present in all eukaryotic organisms (Nawaz et al. 2021). It is utilized by eukaryotic cells for multiple inner transductions and the exterior signals and the activation of downstream cytoplasmic and nucleus components in response to various stressors (Nawaz et al. 2021). This cascade is essential in the conversion of extracellular signals to the final downstream cell response via sequential phosphorylation/dephosphorylation events (Kaur et al. 2019). MAPKs, in addition to being a vital plant stress signal sensor, are reported to be an integral part of the melatonin-orchestrated immunity in plants (Pitzschke et al. 2009; Lee and Back 2016). The MAPK signaling pathway is found in almost all plants and plays a vital role in the transfer of both abiotic stress signals provoked by heat, UV light, osmotic pressure, heavy metals old, injuries as well as biotic stressors such as phytoplasma, bacteria, virus, nematodes, and more importantly fungi (Sinha et al. 2011). As shown in Fig. 9.3, the components of the so-called cascade are situated under the plasma membrane and get autoactivated immediately

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Pathogen +MT

NO

ROS CBF/BREBF1

MEL

MEL

P

OXI1/MAPKKK3 MAPKK4/5/7/9 MAPK3/6

Sugar Glycerol SA NO

SA

ICSI PR1 PR2 PR5

PR1 PR2 PR5

Fig. 9.3 Relationship between the melatonin and nitric oxide in biotic stresses. SA salicylic acid, ICS1 isochorismate synthase 1, PR1 pathogenesis-related enzymes 1, PR2 pathogenesis-related enzymes 2, PR5 pathogenesis-related enzymes 5, CBF/DREB1s C-repeat-binding factors/drought response element binding 1 factors, OXI1 oxidative signal inducible 1

upon sensing the microbes’ epitopes (MAMP). MAPKs have different intermediates, e.g., MAPK1, MAPK2, MAPK3, MAPK4, MAPK5, MAPK6, and MAPK7. Reports indicate the ability of melatonin signals to effectively activate the MAPK signaling pathway through the upstream activation of MAPKK intermediates MAPK4/5/7/9 (Rasmussen et al. 2012), initiated by the starter MAPKK (Pitzschke et al. 2009). The downstream activation of MPK6/3 components leads to the expression of putative defense-related genes. The sensitivity of the MAPK intermediates MKK4/5/7/9 to melatonin was equally demonstrated by Lee and Back (2016) using MAPK-deficient Arabidopsis mutant. The role of the oxidative signal inducible 1 (OXI1) kinase and MAPK cascades on the melatonininduced innate immunity signal transduction was also shown by Lee and Back (2017) and Arnao and Hernández-Ruiz (2018). Overall, the plant tolerance to fungal attacks is mediated and fine-tuned via the MAPK cascade. Hence, as seen in the Arabidopsis-P. syringae model, melatonin is seemingly an integral part of plant defense signaling network whose activity is orchestrated by the combination of several cellular components. Collectively, these findings suggest that phytomelatonin functions in plant innate immunity against fungi not only via SA/JA/ethylene but with the downstream intervention of the MAPK-dependent pathway (Sun et al. 2021).

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Crosstalk Between Melatonin and Nitric Oxide (NO) for Disease Suppression in Plants

Plant immune system is mediated by an intricate signaling network encompassing several other actors in addition to JA, SA, ET, and the downstream MAPK system (Fig. 9.4). Clear evidences indicate that NO is another key upstream signaling element intervening in the reinforcement of plant innate immune system in response. Here, we discussed the crosstalk between melatonin and NO as well as other key orchestras of plant immunity. In fact, NO is a gasotransmitter involved in the regulation of plant development and mediates stress tolerance through the improvement of the antioxidant system (Siddiqui et al. 2011). Its properties as a powerful signaling molecule reside on its ability to easily diffuse across biological membranes without any specialized transporter (Fancy et al. 2017). Number of published papers have demonstrated that ROS, NO, and the MAPKs pathway interact to orchestrate the melatonin-triggered plant immune system (Pitzschke et al. 2009) and that NO and ROS released in the course of pathogen attack play key functions in both the early and later stages of the plant defense response (Zhang et al. 2022). Despite the vast amount of papers highlighting the relationship between melatonin and NO, their molecular interactions are intricate and require the involvement of other interlinked intermediates. Concretely, phytomelatonin stimulates the production and

Fig. 9.4 Melatonin modulates the salicylic acid (SA), jasmonic acid (JA), and ethylene (C2H4) signaling cascades to enhance plant innate immunity against infection by pathogens (Arnao and Hernández-Ruiz 2018). MAPKKK mitogen-activated protein kinase kinase kinase, ROS reactive oxygen species, OXI1 oxidative signal inducible 1, PR pathogen resistance, NPR1/2/5 nonexpressor of pathogenesisrelated genes 1/2/5, PDF 1.2 plant defensing 1.2, EIN 1 ethylene insensitive, EDS1 enhanced disease susceptibility 1 and PAD4 phytoalexin deficient

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accumulation of NO via the arginine pathway or scavenges its excess via its strong antioxidant property. Melatonin equally upregulates the NO synthase-(NOS)-related genes by enhancing NOS activity and thus, NO levels (Liu et al. 2019). Conversely, at the presence of molecular oxygen, phytomelatonin can be converted into N-Nitrosomelatonin (NOMET) by NO nitrosation. While the NOMET is a wellknown NO donor, it can additionally boost cellular phytomelatonin levels by increasing the expression of genes involved in the phytomelatonin biosynthetic pathway. Comparative metabolomics analysis showed that the treatment of A thaliana with melatonin and Pseudomonas syringae DC3000 led to enhanced endogenous soluble glycerol and sugars with subsequent accumulation of cellular SA and NO and activation of immune responses to pathogens (Reiter et al. 2021). Many other findings further highlight these interactions. For instance, Lu et al. (2019) demonstrated that the NO-dependent pathway was responsible for the melatonin mediated resistance of rice to diseases. Further, Shi et al. (2015) indicated that the cooperation between melatonin and NO caused the upregulation and the expression of multiple SA-related genes, hence conferring plant resistance to pathogen infections. Many other works have addressed NO-induced plant disease tolerance, and the synergy with SA through the use of SA-deficient (NahG-overexpressing) and NO-deficient Arabidopsis mutants (noa1 and nia1nia2) (Reiter et al. 1993, 2021). These findings clearly indicate that NO just like the MAPK pathways act ultimately as a downstream signal for melatonin in the plant immune response (Sun et al. 2021).

9.8

Antifungal Potential of Exogenous Melatonin

To date, exogenous melatonin is considered as a powerful elicitor to enhance plant disease resistance against various pathogens including fungi. Factually, the antifungal potential of this versatile compound has been widely demonstrated against a broad spectrum of fungal pathogens of agricultural importance. All started in 2013 when Yin and collaborators reported for the very first time that treatment of Apple with exogenous melatonin can enhance disease tolerance against the Marssonina apple blotch, by inducing the resistance-related enzymes such as chitinase and β-1,3-glucanase and by sustaining the intracellular hydrogen peroxide (H2O2) at a steady-state level (Yin et al. 2013). The suppressive effects of exogenous melatonin have equally been proven vis-a-vis Fusarium wilt in watermelon (Kasote et al. 2020), downy mildew in cucumbers (Sun et al. 2019; Mandal et al. 2018), Phytophthora crown rot in watermelon (Mandal et al. 2018), Verticillium wilt in cotton (Li et al. 2019a), downy blight in litchi fruit, anthracnose in banana (Li et al. 2019b), Gray mold in tomato fruit (Liu et al. 2019), and Powdery mildew in watermelon and other cucurbits (Mandal et al. 2018). Elsewhere, the incidence of Plasmodiophora brassicae alongside spore density drastically diminished upon melatonin application in Arabidopsis (Chang et al. 2018). In addition to triggering Capsicum annum L innate immune response, exogenous treatment with melatonin led to the inhibition of C. gloeosporioides, C. acutatum, and P. capsici mycelial

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expansion and thus disease suppression (Ali et al. 2021). Following the administration of melatonin, Zhang et al. (2017, 2018b) demonstrated that Phytophthora infestans was more susceptible to fungicides and that bacteria, yeast, and filamentous fungus causing postharvest losses in apples were inhibited. Melatonin is frequently applied exogenously to promote apple seedling growth, induce photosynthesis, and boost potassium levels and subsequent replant disease alleviation (Li et al. 2018). Similar outcomes were recorded with several other fungal species such as Fusarium spp., Alternaria spp., P. nicotianae, Penicillium spp., and Botrytis spp. under in situ (Moustafa-Farag et al. 2019) and on standard microbiology culture media (in vitro) (Arnao and Hernández-Ruiz 2018). Hence Zang et al. (2018b) showed that the in vitro and in vivo inhibitory effects of the synergistic combination of ethylicin and melatonin toward Phytophthora nicotianae were due to the imbalance of the fungus amino acid homeostasis. Conversely, Lin et al. (2019) found that the ROS scavenging ability of melatonin enhanced the susceptibility of citrus to green mold disease caused by Penicillium digitatum. While most of the above-mentioned fungicidal effects could be ascribed to the upregulation of PTI- and ETI-related genes (Mandal et al. 2018; Liu et al. 2019; Lee et al. 2014; Lee and Back 2016) and JA-responsive proteins (PR3 and PR4) (Chang et al. 2018), available literature corelate the antifungal effects of melatonin with its ability to maintain H2O2 cellular concentration through the modulation of its synthesis by the activities of antioxidant enzymes and molecules (Lin et al. 2019; Khan et al. 2021). More examples are given in Table 9.1.

9.9

Conclusion

The review of available literature has proven that melatonin is an indispensable signaling molecule for plant. Its role in mitigating abiotic and biotic stresses makes it a more versatile molecule. The triggered gene expression and crosstalk of melatonin with other phytohormones is another factor of paramount importance which contributes greatly to many plants biological processes under both normal and aversive environmental circumstances. However, the endogenously produced melatonin sometimes is not enough to tackle harsh conditions. In this regard, exogenous melatonin implemented to induce the level of endogenous melatonin order to sustain plant immunity has gained widespread acceptance in recent years. Evidence suggest that melatonin induces an increase in the levels of the defense hormones (SA, JA, and ET) and the signaling molecule NO and MAPKS. But the crosstalk between these intermediates and melatonin for plant’s response to fungal infections shows a certain level of complexity, as they interact independently and via multiple signaling pathway. This work has proposed extensive data from recent publication on how melatonin induces resistance in plant against fungal attacks. Conclusively, melatonin is a molecule with high potential to be used as an antifungal agent in crops, being nontoxic (eco-friendly molecule) with high possibilities of being used in agricultural and biotechnological practices, making them more sustainable. Further studies in more plant species and other fungi-crop pathosystems must be carried out to confirm

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Table 9.1 Antifungal effect of exogenous melatonin in crops Plant Musa acuminata

Pathogen Fusarium oxysporum

Citrullus lanatus

Podosphaera xanthii, Phytophthora capsici Botrytis cinerea

Solanum lycopersicum

Solanum tuberosum

Phytophthora infestans

Cucumis sativus L.

Fusarium oxysporum f. sp. cucumerinum

Cucumis sativus L.

Pseudoperonospora cubensis

Capsicum annum L.

Colletotrichum gloeosporioides

Bamboos

Shiraia sp. S9

Arabidopsis thaliana (L.) Heynh.

Plasmodiophora brassicae

Citrus limon (L.)

Penicillium digitatum

Mechanism Resistance induction via regulation of the expression of MaHSP90s gene Upregulation of PTIand ETI-associated genes

Effect Improvement of disease resistance

References Wei et al. (2017)

Induction of disease resistance

Mandal et al. (2018)

Regulating hydrogen peroxide (H2O2) level and JA signaling pathway Disorganizing cell ultrastructure, aberrant and distorted hyphae. Protecting plant from oxidative damage. Reducing stress tolerance of Phytophthora infestans Mitigation of the oxidative stress caused by Fusarium oxysporum f. sp. cucumerinum Enhancing the activity of antioxidant enzymes and the expression of antioxidant genes Increasing the transcripts level of chitinase gene CaChiIII2 Regulating nitric oxide (NO) and H2O2 leading to the suppression of Hypocrellin A toxin production Inducing high expression of the JA-responsive PR3 and PR4 genes Reduce resistance to green mold disease

Induction of disease resistance

Liu et al. (2019)

Attenuation of potato late blight

Zhang et al. (2017)

Enhancing disease resistance

Ahammed et al. (2020)

Enhancing disease resistance

Sun et al. (2019)

Enhancing disease resistance

Ali et al. (2021)

Inhibition of conidiation and spore germination of Shiraia sp. S9

Wang et al. (2022)

Reduction of number of pathogen sporangia Scavenging of defenserelated ROS in the infected fruits

Chang et al. (2018) Lin et al. (2019)

(continued)

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Table 9.1 (continued) Plant Malus prunifolia

Pathogen Diplocarpon mali

Mechanism Maintain intracellular H2O2 concentrations N activities of plant defense-related enzymes

Fragaria ananassa

Botrytis cinerea and Rhizopus stolonifer

Reduced H2O2 levels and antioxidant enzyme activities

Grapes (Vitis vinifera L.)

Botrytis cinerea

Reduction of disease incidence and severity of gray mold induced the synthesis and accumulation of total phenols and flavonoids, reduced malondialdehyde generation, and inhibited an increase in cell membrane permeability

Effect Alleviating disease damage Fungal infection resistance Lesion reduction Reduction of postharvest decay in stored strawberry fruits Increasing the defense enzyme production and activities

References Yin et al. (2013)

Aghdam and Fard (2017)

Li et al. (2022)

these incipient findings and to elucidate more details of the molecular mechanism activated by melatonin in fungal-infected plants, as it will allow the understanding of the process and determine the most effective application modes.

References Agrios GN (2005) Plant pathology. Elsevier Ahammed GJ, Mao Q, Yan Y, Wu M, Wang Y, Ren J, Guo P, Liu A, Chen S (2020) Role of melatonin in arbuscular mycorrhizal fungi-induced resistance to fusarium wilt in cucumber. Phytopathology 110(5):999–1009 Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision, ESA working paper. FAO, Rome Ali M, Tumbeh L-SA, Muhammad I, Farghal M, Khattak AM, Jan I, ul Haq S, Khan A, Gong Z-H, Lu G (2021) Melatonin mitigates the infection of Colletotrichum gloeosporioides via modulation of the Chitinase gene and Antioxidant activity in Capsicum annuum L. Antioxidants 10(1): 1–24. https://doi.org/10.3390/antiox10010007 Altaf MA, Shahid R, Altaf MM, Kumar R, Naz S, Kumar A, Alam P, Tiwari RK, Lal MK, Ahmad P (2022) Melatonin: first-line soldier in tomato under abiotic stress current and future perspective. Plant Physiol Biochem 185:188–197

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Role of Melatonin in Management of Stress Tolerance of Forest Tree Species

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K. Darshan, K. N. Harshitha, S. Shreedevasena, Aditi Tailor, Tanmaya Kumar Bhoi, Sonali Nigam, and Nitin Kulkarni

Abstract

Plant growth is hindered by the exposure to biotic and abiotic stresses. Biotic stress comprises the attack of plants by insects, fungi, bacteria, viruses, protozoa, nematodes, and phanerogamic plant parasites. Abiotic stress which includes low or high temperature, high salinity, deficient or excessive water, heavy metals, and ultraviolet radiation, etc. Melatonin which is present ubiquitously in all living organisms has a multifunctional role. It regulates plant stress response generally by inhibiting the accumulation of reactive oxygen species, and indirectly by affecting stress response pathways. Owing to protective functions of melatonin against both biotic and abiotic stresses, which has increased research attention in recent years because of the elevated harmful effects of climate change, and industrial pollution, soil salinization on timber production, which in turn affects productivity in forest. So far, this aspect has been scantily explored in forest tree species which limits our understanding of the roles that melatonin may play.

K. Darshan, K. N. Harshitha, S. Shreedevasena, Aditi Tailor, Tanmaya Kumar Bhoi and Sonali Nigam contributed equally with all other contributors. K. Darshan (✉) · N. Kulkarni Forest Protection Division, ICFRE-Tropical Forest Research Institute, Jabalpur, MP, India K. N. Harshitha Department of Plant Pathology, College of Agriculture, V. C. Farm, Mandya, Karnataka,, India S. Shreedevasena Directorate of Medicinal and Aromatic Plants Research (DMAPR), Anand, Gujarat, India A. Tailor · T. K. Bhoi ICFRE-Arid Forest Research Institute, Jodhpur, Rajasthan, India S. Nigam Department of Botany and Microbiology, St. Aloysius College, Jabalpur, MP, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Kumar et al. (eds.), Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection, https://doi.org/10.1007/978-981-99-6741-4_10

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There is a need to accelerate relevant research in the forestry species to fill the gap in knowledge and highlight the basis of melatonin-mediated alleviation of stress. Hence, this chapter highlights the importance of melatonin in the management of biotic and abiotic stress exposed to forest tree species. Keywords

Abiotic stress · Biotic stress · Disease · Forest trees · Melatonin · Pest · Toxicity

10.1

Introduction

Melatonin (N-acetyl-5-methoxytryptamine) is a ubiquitous molecule with multiple regulatory roles in various biological processes (Sun et al. 2020; Chen and Arnao 2022). Its major roles also extend to include regulating responses to stresses of both biotic and abiotic kinds (Sun et al. 2020; Rehman et al. 2021). Melatonin is biosynthesized from the precursor tryptophan and its biosynthesis majorly occurs in chloroplasts, and therefore the endogenous contents, is subject to regulation by a number of internal as well as external cues (Chen and Arnao 2022). Melatonin also harbors high antioxidant potential and serves to scavenge free radicals, and also provides a boost to the plant’s antioxidant defense by positively regulating the biosynthesis of antioxidants (enzymatic and non-enzymatic) (Khan et al. 2020). Among the many beneficial roles played by melatonin in response to stress, some important ones include protection from damage due to excess reactive oxygen species (ROS), improved photosynthetic rates, strengthening of antioxidant machinery, production of secondary metabolites, modulation of gene expression, and crosstalk with other hormones (Sun et al. 2020; Rehman et al. 2021; Chen and Arnao 2022) (Fig. 10.1). It is due to these recognized benefits of melatonin, that it has been a major focus of research aimed at improvement of growth of plants under stressful conditions. Exogenous supplementation of melatonin has been demonstrated to significantly improve growth attributes and mitigate the negative effects of stress (Sun et al. 2020; Rehman et al. 2021). The beneficial roles of melatonin in regulation of plant defense have been identified in a vast number of species, but majorly in agricultural species, with limited reports in forestry species. Forests, being a commodity vital for the operation of ecosystems, deserve particular attention as threats to them are on the rise globally, both in the form of abiotic and biotic factors. They deliver crucial ecosystem functions, including their key roles in maintaining water and nutrient cycling, carbon storage, checking erosion, and conserving biodiversity. Forest tree species are expected to be highly resilient, however, their physiological responses to different stress conditions have not been fully worked out. This disparity in the quantum of research that goes into understanding agricultural and forest tree species is also starkly visible with respect to the investigations that have been undertaken to

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Role of Melatonin in Management of Stress Tolerance of Forest Tree Species

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Tryptophan

Tryptamine t

Serotonin t

Exogenous application of melatonin

Melatonin

Drought, cold, Heat, salinity

Protein stability, Metabolic regulation, Photoperiod cycle

Carbohydrate, Nitrogen metabolism Proline, sugars

Chlorophyll content Stomatal content Biomass production Photosystem efficiency

Biotic

Viruses, Bacteria, Fungi, Nematode

Abiotic antistressor

antistressor

Biological Rhythm regulator

Plant hormone regulator

IAA, ABA, GA

Redox network

Reactive Oxygen Species Reactive Nitrogen Species

Osmoregulation

Photosynthesis regulator

Antioxidant enzymes

Catalases, Peroxidases Superoxide dismutase

Fig. 10.1 Mechanisms and its multiple roles of melatonin in stress protection in plants. ABA Abscisic Acid, GA Gibberellic Acid, IAA Indole-3-Acetic Acid

examine the possible effects of melatonin. This information might prove useful in the development of practical interventions for promoting sustainable forestry on degraded lands as well as those that constantly face adverse conditions. It might also prove useful in providing planting material with improved quality, as melatonin has many proven growth promoting roles, by way of increasing the adaptation capacity and thereby the afforestation value (Yer Celik 2021). Melatonin may be utilized as a biostimulant for forest species to prime them to reinforce their defense to allow them to respond effectively in the wake of unfavorable conditions (Rehman et al. 2021). Previously, it has been reported that external treatment with melatonin at lower concentration increases seed germination speed and germination value under Cd stress, improves uptake of N under drought, and also improves attributes like photosynthesis rate, chlorophyll contents, antioxidant levels, while mitigating the associated oxidative stress (Liang et al. 2018; Yer Çelik and Yer 2022). Pesticides can be substituted by bio pesticides (Archana et al. 2022; Tiwari et al. 2021). Considerable progress has been made in the general understanding of melatonin synthesis pathways and its role in plants since a decade (Zeng et al. 2022). It also known to promote seed germination, boost lateral root generation, and also

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controls time of flowering and delaying leaf senescence (Arnao and Hernández-Ruiz 2019). With all above uses of melatonin, the studies are required to know the significance of exogenous application of melatonin in alleviating stress in various forest ecosystem.

10.2

Melatonin-Mediated Pest Tolerance of Forest Tree Species

Around 30% of the world’s geographical area is covered by forests, which offer a variety of ecosystem services and goods vital to the sustainability of both the planet and human society (Oguh et al. 2021). Each year, pests kill millions of trees in both natural and commercial environments (Bushaj et al. 2021). Negative effects on net primary production and carbon sequestration might result from the loss of trees due to severe pest outbreaks (Marcos-Martinez et al. 2022). Melatonin is an effective tool in the fight against various insect pests, as evidenced by the growing desire to reduce the use of pesticides and convert to natural and sustainable management techniques. Moreover, it has been revealed that melatonin functions as a signal that mediates reactions to insect feeding and wounding as well as responses to infections, insect damage, and plant resistance. Dutch elm disease (Ophiostoma ulmi), a fungal pathogen whose infection is substantially assisted by elm beetle (Scolytus multistriatus Marsham) feeding, has decimated populations of American elm (Ulmus americana L.) (Saremba et al. 2017). Melatonin, serotonin, and jasmonic acid concentrations increased dramatically as a result of the trees’ response to the insect damage. Serotonin and melatonin spikes were 7000 times higher than resting levels. Jasmonic acid spikes were nearly ten times higher than resting levels, with one particularly big spike being seen (Saremba et al. 2017). As insect feeding and pathogen challenge cause antagonistic phytohormone cascades in plants, it has been discovered that disease resistance depends on proper balances of jasmonic and salicylic acid levels in the tissues. Melatonin has been suggested as one of the early signals that communicates feeding damage in plants and may contribute to resistance through interaction with signaling from salicylic acid and jasmonic acid (Sherif et al. 2016, 2017). There is a limited amount of research that has been conducted on the use of melatonin as a potential solution for insect pest in forest trees. More studies are needed to evaluate the effectiveness of melatonin and to determine the optimal application methods for its use in forest management. Understanding how melatonin and serotonin interact to protect plants against these insects and other biotic stresses will make for a fascinating study in the future. Similar to this, its potential contribution to virus acquisition and transmission on important vectors might be investigated (Kumar et al. 2021a, b). Melatonin and other insecticide interactions may be researched in order to manage insects with less pesticides overall.

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10.3

181

Melatonin-Mediated Disease Tolerance of Forest Tree Species

In the forestry and horticulture ecosystem, the loss occurs as a result of infectious diseases caused by nematodes, insects, bacteria, viruses, and fungi is a substantial contributor for economic losses (Kumar et al. 2019, 2022). These stressors have a direct relationship with plants, allowing them to both take nutrients from them and also to kill and decompose plants (Giraldo Acosta et al. 2022). Melatonin (N-acetyl5-methoxy tryptamine), a master regulator of host defense against pathogen infection and environmental challenges, has piqued the curiosity of researchers because of its numerous benefits in plant systems through melatonin-mediated reactive oxygen species scavenging and activation of antioxidative defense responses (Moustafa Farag et al. 2019) Pomegranate plants treated with 0.1 mM melatonin had higher total phenolic levels, anthocyanin concentration, antioxidant activity, and improved fruit characteristics such as firmness, total soluble solids, and total acidity content result in increased shelf-life of fruits. Hence, melatonin pretreatment could be a viable technique for increasing bioactive chemicals and improving health effects (Lorente et al. 2021). The application of exogenous melatonin in lilium leaves effectively controlled the Botrytis elliptica infection. Transcriptome studies showed the defense-related differentially expressed genes, plant hormone signal transduction, MAPK signaling pathways, phenylpropanoid biosynthesis and phenylalanine metabolism were enriched after treatment with melatonin (Xie et al. 2022). Similarly, exogenous melatonin inhibits apple blotch (Diplocarpon mali) effectively by modulating the levels of ROS by balancing intracellular hydrogen peroxide (H2O2) concentrations, increase the antioxidant enzymes and accumulate the pathogenesis-related proteins. In addition, melatonin pretreatment maintains the photosystem II and improved the total chlorophyll content (Yin et al. 2013). The Irish potato famine pathogen, Phytophthora infestans cause serious economic impact worldwide. The exogenous application of melatonin significantly reduced the Late blight incidence by changing cell ultra-structure, inhibit mycelial growth and zoospore production by interfering amino acid metabolism, overexpressing apoptosis inducing factor and dysregulating the virulence-related genes (Zhang et al. 2017). Depending on the type of host, its pathogen, and the prevailing environmental conditions, many management approaches for preventing disease or managing a pathogen have been put into effect. The antiviral properties of melatonin in plants have not been extensively studied. In this regard, treatment with exogenous melatonin (100 M, twice) decreased the viral RNA and virus concentration of the infected Nicotiana glutinosa and Solanum lycopersicum seedlings. The rise in SA concentrations in the NO-dependent pathway was attributed with this therapeutic melatonin effect (Hernandez Ruiz et al. 2023). In stress conditions, melatonin increases the tolerance response through the control of Various key transcription factors mentioned in Fig. 10.2.

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Melatonin mediated activation of Transcription factors

Abiotic Transcription factors

Hormonal Transcription factors

Transcription factors

NACs (auxin factors)

CBLs (calcineurin proteins)

DREs (dehydrationresponsive elements)

cold-responsive COR (antifreezing protein response) LTI (low-temperature induced factors)

KIN (anti-freezing protein response)

ERFs (ethylene-responsive elements)

B-like

ZATs (ROS-related responsive elements)

WRKYs transcription factors

MYBs (regulator of CBFs),

HSFs (heat shock factors) in heat-stress

CIPKs (CBL-interacting protein kinases) salt-stress

RD (responsive factors to dehydration)

Fig. 10.2 Melatonin-mediated transcriptional factors regulations for stress tolerance

10.4

Melatonin-Mediated Abiotic Stress Tolerance in Forest Ecosystem

The abiotic stress pose threat to plant growth due to excess production and accumulation of Reactive Oxygen Species (ROS) which leads to cellular and metabolic process damage (Behera et al. 2023; Mangal et al. 2023). To mitigate the harmful effects of stress-induced excessive ROS, plants show various defense strategies through enzymatic or non-enzymatic ways, which scavenges excess ROS and maintain balance in cells (Meloni et al. 2003). Enzymatic antioxidants comprise ascorbate peroxidase (APX), superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) and the non-enzymatic antioxidants involve ascorbate (AsA),

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glutathione (GSH), as well as polyphenols and vitamins in plants (Meloni et al. 2003; Lal et al. 2020, 2022). Additionally, the amplified synthesis of osmolytes such as sugars, soluble protein, proline also has a role in alleviating stress. Melatonin (N-acetyl-5-methoxytryptamine) an indoleamine discovered in pineal gland of vertebrates in 1958 and in plants identified during 1995 (Hattori et al. 1995). Melatonin a phytohormone has gained great interest in research owing to its wide applications in plant systems (Altaf et al. 2022, 2023). To cope with most of the abiotic stresses and pathogen infections the reactive oxygen species scavenging and activation of antioxidant defense responses is the two major mechanisms mediated through melatonin. Melatonin application also improve seed germination in a diverse of abiotic stress, which encompass water deficiency, high temperature, chilling, salt stress (Zhang et al. 2013) and also chelates heavy metal (Yu et al. 2021). The chloroplasts and mitochondria are the sites of synthesis of melatonin in plants (Tan et al. 2013) which is present in wide variety of plants, viz., fruit crops, agricultural crops, and also forest trees. The melatonin content varies greatly among different plant species, the developmental periods of different plants and distribution of endogenous melatonin in different organs is similar (Hernandez-Ruiz and Arnao 2008).

10.4.1 Heat Stress Heat stress has become the factor for global warming which in turn limit the productivity of forest trees. Stressed plants undergo various morphological, physiological, and biochemical changes which hamper their growth (Xu et al. 2016). The temperature/heat stress induces photoinhibition and also promotes the protein and chloroplast membrane damage leads to hampering of protein synthesis and enzyme activation in plants (Smertenko et al. 1997) and also effects at transcriptional, posttranscriptional and epigenetic levels which include DNA methylation, chromatin remodeling, histone modification (Zhao et al. 2020). Heat stress induces proteins misfolding which is self-defense phenomenon in plants. Heat shock proteins and ubiquitin-proteasome system are the chaperons which regulate the misfolding of proteins. Plant thermotolerance will be improved as the plants respond to heat stress in response to increased melatonin levels. Under heat stress, exogenous melatonin application can enhance antioxidant defense systems via control of ROS accumulation and enhancement of proline metabolism (Zeng et al. 2022). There is a limited amount of research that has been conducted on the use of melatonin in alleviating heat stress in forest stress.

10.4.2 Cold Stress Cold stress can include chilling and freezing temperatures that exerts multiple effects which leads to changes in physiology, biochemistry, molecular biology of plants and also affects the photosynthetic machinery by causing inhibition of Photosystem PS-I

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and PS-II. ROS accumulated under cold hinder carbon fixation by inactivating Calvin cycle regulating enzymes. Melatonin application is known to trigger the phenylpropanoid pathway by enhancing the activities of PAL, 4-coumarate-coenzyme A ligase (4CL), cinnamate-4-hydroxylase (4CH), and POD, which may be accompanied by accumulation of higher contents of total phenols and lignin, that may improve temperature tolerance. Treatment of Dalbargia odorifera seedlings with external melatonin and Ca2+ (0.6 mM + 5 Mm CaCl2) under cold stress improved the growth and alleviated injuries. Applied, melatonin is also known to raise the phytohormones levels like gibberellin (GA3) and auxin (IAA); however, there are reports of decrease of abscisic acid under cold stress (Pu et al. 2021).

10.4.3 Drought Stress Drought stress limits the plant growth, alters physiological, biochemical, and metabolic functions of plant. Drought incites oxidative stress and activates stress signaling pathways mediated by Ca2+, ROS, and hormones. Exogenous melatonin treatment can trigger an increase in endogenous melatonin levels, which in turn improve turgor pressure, recovery of chlorophyll, maintenance of cell and photosynthetic machinery stability under drought stress. Water; crucial factor for Davidia involucrata cultivation; stress can greatly inhibit the growth of seedlings via influencing multiple biochemical and physiological processes (Wang et al. 2011). Liu et al. (2021) studied the external pretreatment of D. involucrata seedlings with 100 μm melatonin along with drought stress. Pretreatment with melatonin reduced the accumulation of H2O2, superoxide anion (O2
-), ROS, and increased enzymatic oxidants, viz., SOD and POD in seedlings. Differential expression study revealed that 1849 genes upregulated and 888 genes downregulated under drought stress which suggested that fine-tuning of multiple phytohormone signaling and synthesis pathways, transcriptional stimulation of auxin signaling-related, and other biosynthetic genes are modulated by melatonin. More studies are required in forest ecosystem at transcription level and also various hormonal cross talk studies which help the plants to thrive under drought stress.

10.4.4 Amelioration of Salt Stress Soil salinization is a major abiotic challenge that is detrimental to plant growth and development (Shahid et al. 2020). Globally, more than 833 million hectares of land is estimated to be salt-affected, accounting for 8.7% of the total land on planet (FAO 2021). The extent of salinization is projected to gradually increase over this century. Many factors may contribute to salinization, either alone or in combination, including human mismanagement, indiscriminate use of fertilizers, irrigation with saline water, deforestation, and sea level rises due to ongoing climate change. Saline soils are characterized by the presence of excessive amounts of neutral salt, principally NaCl. High NaCl level in soils negatively affects plants as it reduces water

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availability and causes toxicity in plants as Na+ and Cl- ions over-accumulate in their body over time (Shahid et al. 2020). The indication to salinity is reduced water potential and the energy required for the intake of water and nutrients increases that result in oxidative stress. The accumulation of Na+ and Cl- ions in sensitive plant tissues triggers the salt stress (Flowers et al. 2010). In their defense, plants trigger salt stress responses involving a variety of biochemical and molecular changes so as to alleviate the stress-associated damage. These encompass selective sequestration or extrusion of Na+ and Cl- ions, reduction in ion absorption by roots and their transport to leaves, accumulation of compatible solutes or osmoprotectants (carbohydrates, proline), reduced oxidative damage via enhancement in antioxidant(s) levels and activities of antioxidant enzymes (SOD, POD, CAT), stimulation of hormones and regulation of stress-responsive gene expression (Zhao et al. 2021; Xiao and Zhou 2023). Although the effect of soil salinity has been assessed on countless agricultural crop species, however, there is no to limited reports on salt stress responses in tree species, particularly those that dominate the forests. Traits associated with salt stress adaptation have been uncovered in a few forest tree species, like Birch, Oak and Poplar species (Tikhomirova et al. 2023). These adaptive responses include improved ion homeostasis, maintenance of cell wall integrity via upregulation of endo-1,4-beta-xylanase, more pronounced antioxidant activity (POD, APX), osmoprotectant accumulation (proline and polyols), modulation of ABA, JA, and SA hormone signaling, and activation of stress-related transcription factors (WRKY, ERF, and AHL). Exogenous application of protective molecules or compounds has been a major area of focus to determine their efficacy and potential in relieving salt stress symptoms and improving overall plant growth (Khalid et al. 2022). A number of molecules or compounds, which when exogenously applied, have been implicated in improving salinity tolerance in plants by playing protective roles, melatonin being one among them (Khalid et al. 2022). Melatonin exerts beneficial effects on plants growing under stressful conditions by strengthening the antioxidative capacity and mitigating salt-induced damage symptoms (Li et al. 2019a; Zhan et al. 2019). The plant resistance to salt stress via melatonin can be regulated in two ways: one is via direct clearance of reactive oxygen species by direct pathway; other is indirect pathway by enhancing antioxidant enzyme activity, photosynthetic efficiency, and by regulating transcription factors associated with stress. The expression of genes can also affect the plants performance via melatonin (Li et al. 2019b). Interestingly, other metabolite molecules and precursors associated with melatonin can also increase the tolerance of plants to salt stress. Salt stress limits the electron transport in photosystem II (PSII) reducing the absorption of light energy and by decreasing the chlorophyll content, the actual photochemical efficiency of PSII, and photochemical quenching (qP) which affects the photosynthesis (Hao et al. 2017). The major intracellular ions are Na+, K+, Ca2+ and H+ (Amtmann and Leigh 2010). Under salt stress, Na+ can enter plant cells, at high concentrations is harmful to cytoplasmic enzymes (Fukuda et al. 2011). It is reported that Melatonin treatment could significantly reduce Na+ accumulation and K+ content under salt stress which might regulate the expression of ion channel genes (MdNHX1 and MdAKT1) to

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maintain ion homeostasis and thus improve plants salt resistance (Meloni et al. 2003). Improved ion homeostasis may be due to the upregulation of several genes, such as SOS (Salt Overly Sensitive), NHX (a vacuolar Na+/H+ exchanger), and AKT. Most evidences for the positive effects of melatonin on salt stress has been drawn from studies on plant species of agricultural, medicinal or horticultural importance, and only few studies to date have focused on woody tree species, that too mostly in horticultural species. For instance, in Malus hupehensis, treatment with 0.1 μM melatonin alleviated the salt stress-induced reduction of photosynthesis and chlorophyll contents and helped plants grow better by reducing oxidative damage (Li et al. 2012). An upregulation was also observed in the ion transporters NHX1 and AKT1, suggesting melatonin’s role in maintaining ion homeostasis. Salinity alleviation by melatonin was also recorded in Citrus aurantium seedlings as it, alone or combined with ascorbic acid, led to reduced Cl- accumulation in leaves, increased SOD and polyphenol oxidase (PPO) activity and higher proline accumulation in roots in response to salt stress (Kostopoulou et al. 2015). Exogenous treatment of melatonin (0.1 μM) alleviated salt stress-associated damage in Actinidia deliciosa (Kiwifruit) seedlings and contributed to reduced electrolytic leakage and improved antioxidant capacity in terms of higher contents of phenolics and total flavonoids (Xia et al. 2017). In Pistachio seedlings (Pistacia vera cv. Badami-Zarand), 100 μmol. L-1 of melatonin ameliorated salinity-induced growth inhibition, chlorophyll reduction and electrical leakage with a concurrent increase in levels of antioxidant enzymes, proline and endogenous polyamine and melatonin (Kamiab 2020). Melatonin treatment also promoted accumulation of phenolic compounds and antioxidant enzymes SOD, GPX, and AOX as well as improved hydroxyl radical scavenging ability in salt-stressed seedlings of Dalbergia odorifera (Cisse et al. 2021). Likewise, melatonin (100 mg L-1) resulted in significant improvement in growth traits, including height, stem girth, number and size of leaves, root length and dry weight, in Citrus rootstocks under salt stress (Al-Mousawi and Al-Tamimi 2022). A similar positive role of melatonin treatment was also documented in Populus cathayana × canadansis “Xin Lin 1,” where melatonin provided at lower concentrations (50 μM and 100 μM), reduced MDA levels, and promoted SOD and CAT contents in salt-stressed leaves (Song et al. 2022). Contrary to this, negative effects of melatonin have also been documented, for instance, in Betula platyphylla, the germination traits, including germination rate, germination potential, and germination index, were significantly lowered in seeds pretreated with melatonin (Li et al. 2019c). Authors surmised that melatonin worked to further aggravate salt stress attributing the outcome to the excess of melatonin to toxic level due to external addition of melatonin on top of the already higher levels of endogenous melatonin under salt stress.

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10.4.5 Alleviation of Metal Toxicity Plants often become exposed to high levels of heavy metals and thereby suffer metal toxicity. The grave state of soil metal contamination poses high ecological risk and bears consequential effects on both environment and human health alike (Sall et al. 2020; Ahmad et al. 2021). Metal toxicity mostly corresponds to build up of heavy metals, such as nickel (Ni), lead (Pb), mercury (Hg), cadmium (Cd), manganese (Mn), copper (Cu), cobalt (Co), aluminum (Al), zinc (Zn), arsenic (As), chromium (Cr), and iron (Fe) (Ghori et al. 2019; Angulo-Bejarano et al. 2021; Gaur et al. 2021). While some of these heavy metals are essential, like Fe, Cu, Co, and Al, as they form co-factors for many enzymes and/or are have indispensable roles in many metabolic processes, the other category, including Cd, Pb, Hg, and As, has no associated positive roles and is purely toxic to plants. These heavy metals have found their way in the environment due to anthropogenic activities, rapid industrialization, industrial activities, indiscriminate use of agrochemicals, fertilizers, and pesticides in agriculture, and unregulated discharge of contaminated effluents, like industrial waste and sewage (Gaur et al. 2021; Srivastava et al. 2017). In fact, in many regions around the globe, heavy metals in soils stand at levels far exceeding their safety standards, especially around industrial zone and waste disposal sites (Kumar et al. 2019; He et al. 2020; Mohammadi et al. 2020; Wei et al. 2022; Zhao et al. 2022). The presence of high doses of these heavy metals within the plant body adversely affects many critical aspects of growth by impairing the normal metabolism, eventually resulting in the manifestation of toxicity in the form of symptoms at multiple levels including morphology, physiology, and biochemistry (Ghuge et al. 2023). Some major symptoms associated with metal toxicity include chlorosis, necrosis, and stunted growth (Ghuge et al. 2023). They also interfere with uptake and assimilation of other vital mineral nutrients (Naeem et al. 2019). Heavy metals Hg and Pb are known to block water channels and hinder water absorption (RucińskaSobkowiak 2016; Naeem et al. 2019). They also cause severe reduction in photosynthetic efficiency and a consequent diminished growth, with part of this reduced photosynthetic ability being attributable to the inhibition of enzymes involved in the carbon assimilation, such as those involved in Calvin cycle, and disruption of electron transport chain (Dobrikova and Apostolova 2019; Huihui et al. 2020). Not only plants, but they also affect the activities of the soil-dwelling microbes involved in nutrient cycling and decomposition and thus reduce the soil fertility (Srivastava et al. 2017). While growing in heavily contaminated soils and air, trees also tend to over-accumulate heavy metals, especially over long exposure periods (Brunner et al. 2008; El-Khatib et al. 2020; Hatami-manesh et al. 2021). In order to cope, plants experiencing heavy metal build up trigger defense responses, including restriction of their uptake by secreting root exudates, accumulation of chelators, sequestration in vacuole, and induction of stress-related proteins, antioxidants, and hormones (Gaur et al. 2021). Evidence has been gathered through many investigations that melatonin may also exert a positive effect and relieve metal toxicity in plants (Hoque et al. 2021). Plants challenged with metal toxicity stimulate higher production of endogenous melatonin as a defense response (Lee et al. 2017;

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Kamiab 2020). Also, exogenous application of melatonin has also been demonstrated to help alleviate metal toxicity caused by a range of heavy metals and enhance multiple growth attributes by positively modulating plant metabolism (Hoque et al. 2021). Melatonin treatment has been shown to result in the reduction of MDA and H2O2 levels with a concomitant increase in the activity of antioxidant enzymes (SOD, POD, and CAT), enhanced accumulation of osmoprotectants, promotion of defense-related secondary metabolism (phenols, flavonoids, and upregulation of phenylalanine ammonia lyase (PAL) and polyphenol oxidase (PPO) enzymes) and stress-related transcription factors, like bZIP, ERF, MYB, and WRKY (Hoque et al. 2021; Shah et al. 2021). Exogenous treatment with melatonin was reported to be beneficial in Actinidia deliciosa (Kiwifruit) as its application lead to increased levels of antioxidants in the leaves of seedlings subjected to Cd stress (Huang et al. 2017). A similar positive effect of exogenous treatment of melatonin was observed in Cd-challenged Camellia sinensis (Tea) seedlings (Tan et al. 2022). Melatonin provided at 150 μM promoted growth, lead to an increase in photosynthetic pigments and soluble protein and strengthening of antioxidant capacity via enhanced activities of SOD and POD and reduced MDA content. Likewise, melatonin reduced Cd accumulation in aerial parts and mitigated associated toxicity in Cd-stressed apple root stocks by restoring photosynthesis, inducing antioxidant defense in terms of higher antioxidant levels and enzyme activities and transcriptionally regulating key genes responsible for Cd uptake, transport, and detoxification, and thus helped improve biomass (He et al. 2020). A positive effect of melatonin supplementation (at 100 μM, 150 μM, and 250 μM) on seed germination was also recorded as it brought the seed germination speed in Cd-stressed seeds of Red Pine (Pinus brutia Ten.) close to that observed in control conditions (Yer Çelik and Yer 2022). At higher concentrations, however, the GS considerably decreased. The research on the aspects of melatonin-mediated amelioration of salt stress and metal toxicity in woody tree species is heavily lacking. Evidence is particularly scarce in forest species in this regard. Taking into account the various protective roles of melatonin in, impetus should be given to undertaking detailed examinations in forest tree species as well as they form a major part of ecosystems.

10.5

Conclusion

Melatonin is a pleiotropic biostimulator chemical with amphiphilic nature, which alters the physiological activities of plants to protect from stress of limiting factors. The exogenous application of melatonin in agricultural plants has showed better protection from biotic and abiotic stress, but the usage of melatonin in forestry crops remains unexplored, which indeed requires detailed investigations. The detailed study on the core physiological pathways and response of genes related to particular stress on interaction of melatonin need to be focused in coming days of forest research. Chemical control is the most effective and widely used strategy, since it provides immediate protection and offers a wide range of management options for its

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usage and application. Yet, with customers’ growing desire for pesticide-free food crops and in the aftermath of environmental sustainability, there is a large demand for comparably safer chemicals to treat diseases. Notably, synergistic co-acting interaction of melatonin with fungicides, highlight melatonin could enhance the fungicide efficiency by reducing the dosage of chemicals present a novel ecofriendly strategy to reducing plant stress. To conclude, enormous research potential on pretreatment approach of melatonin in forest trees for better understanding act as a promising strategy for protecting plants from biotic and abiotic stress. Transgenic plants with increased melatonin content are likely to lead to advancements in agricultural crop production and human health in general. Nevertheless, the mechanism by which it assists in the acquisition of resistance requires further exploration.

10.6

Future Prospects

In the future, it is expected that heightened levels of melatonin will be uptained with modern breeding techniques and transgenic approaches and the changed melatonin production in these plants may be utilized as a tool to induce resistance to biotic and abiotic challenges, leading to higher forestry areas and productivity which is the backbone of rural economy. There have been few reports on the melatonin’s potential to combat disease and insects, but this field of study needs to be vigorously investigated with a characterization of the precise defense mechanisms. It would be important to establish whether melatonin increases the phytoremediative ability of the bioaccumulation in forest plant species, and if so, the mechanism involved would need to be defined. For agriculture crops, the concentration and method of exogenous melatonin application are standardized; similarly, for forest tree crops, the concentration and method of application need to be investigated; before that, the mechanism of melatonin transport systematically throughout the plant needs to be examined. As melatonin behaves like auxin and some scientists have asserted that it can be used to propagate plants in vitro, it is necessary to further investigate the use of melatonin in forest nurseries. Research on the melatonin-based receptors, physiological and biochemical functions, production pathways of melatonin in tree plants should be focused. Melatonin may also prove to be a key chemical in forestry for the protection of trees from various stress and enemies, which can assist to address global food security challenges and sustainable development.

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Emerging Role of Melatonin in Integrated Management of Crop Pathogens

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Lellapalli Rithesh, Gokarla Vamsi Krishna, Sompalli Suresh Rao, and Bhanothu Shiva

Abstract

Plants must withstand and counteract biotic and abiotic distress all across their cycle of existence. To protect themselves from biotic stress, plants employ numerous defence strategies, that ultimately lead to plant immunity. An affordable alternative method of protecting plants against disease threats is provided by the environmentally friendly melatonin molecule. Melatonin has been discovered for a crucial role in plant resistance to Botrytis cinerea by increasing resistance to fungicides and reducing Phytophthora infestans damage. Melatonin’s antibacterial effects have been demonstrated towards Xanthomonas oryzae pv. oryzicola and Xanthomonas oryzae pv. oryzae. It decreased the virus titre of tobacco mosaic virus (TMV) in infected seedlings and successfully eliminated apple stem grooving virus (ASGV) from apple stems. The diseases were successfully decreased by the combination of melatonin and biocontrol agents. Exogenous melatonin treatment can increase disease resistance and reduce the occurrence of postharvest diseases. It has clear benefits for controlling plant

L. Rithesh (✉) Department of Plant Pathology, College of Agriculture, Vellayani, Kerala Agricultural University, Thiruvananthapuram, Kerala, India G. V. Krishna Department of Plant Pathology, Agricultural College, Bapatla, Acharya N.G. Ranga Agricultural University, Guntur, Andhra Pradesh, India S. S. Rao Department of Plant Pathology, S.V. Agricultural College, Tirupati, Acharya N.G. Ranga Agricultural University, Guntur, Andhra Pradesh, India B. Shiva Plant Protection division, Regional Agricultural Research Station, Lam farm, Acharya N.G. Ranga Agricultural University, Guntur, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Kumar et al. (eds.), Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection, https://doi.org/10.1007/978-981-99-6741-4_11

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growth and resistance to different biotic and abiotic conditions. Although melatonin’s potential to withstand abiotic stimuli in plants has been thoroughly studied, it is still not clear what role it plays in biotic stress, so additional research is needed. Keywords

Phytohormone · Melatonin · Integrated management · Bacteria · Fungi · Virus · Antioxidants

11.1

Introduction

Plants must withstand and counteract biotic and abiotic distress at all stages of their life span. In order to recognise environmental cues and respond appropriately to defend themselves from a variety of abiotic and biotic conditions, plants have evolved a variety of complex processes (Kumar et al. 2019, 2021a, b, 2023). These mechanisms modify their metabolic and molecular processes to keep equilibrium within the confines of their genes, which control how plants grow as a whole (Kumar et al. 2023, 2021a). These complex plant behaviours were primarily regulated by phytohormones, which oversaw these complex molecular processes (Burger and Chory 2019). Numerous phytohormones serve vital roles in the reactions to biotic and environmental stresses (ABA, JA, and SA). Phytohormones play important regulatory roles in innate immunity in plants in addition to their main biochemical roles in the growth and evolution of plants (Lal et al. 2022; Behera et al. 2023). A sophisticated network of signalling networks, also known as hormonal cross-talk, is employed to manage these actions. The term “signalling cross-talk” describes a broad spectrum of intricate interactions that make use of related signalling molecules, genes, and their metabolites to organise well-coordinated molecular communications. Over the past two decades, research on phytohormones, transcription factors, kinase cascades, ROS, miRNAs, and new compounds like melatonin, serotonin, and spermine has been conducted in plants (Mangal et al. 2023). When plants experience biotic and abiotic stresses, these compounds have been discovered to function either synergistically or antagonistically to regulate these signalling cross-talks. (Li et al. 2020). The phytohormones ABA, JA, SA, ET, brassinosteroids (BRs), auxins, and cytokinins have been investigated for their defence-related responses to stress. Cross-talk between phytohormones is believed to influence the regulation of the initiation of protective reactions, plant development, and abiotic stress tolerance by regulating the physiology of biotic and abiotic stress reactions (Kumar et al. 2023). The production of crops is significantly impacted by biotic and abiotic challenges, which continually endanger the world’s food supply. The main stress reaction of plants can be directly impacted by many factors that are commonly prevalent in nature, such as heat, drought, salt, and diseases (Mittler 2006). Stress memory, which reflects resource-saving stress response mechanisms that are only induced and triggered upon a stressful incident, frequently affects how the plant

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reacts to consecutive stresses (Lal et al. 2021, 2022). Because of the intrinsic molecular complexity and interlinked signalling networks in plants, it has proven to be very challenging to perceive the molecular processes driving multidimensional signal interactions. Under a variety of stressors, many factors, including ROS equilibrium, inorganic ion flux, phytohormone interactions, protein kinases and transducers, modified miRNA, and different protein variations, all have an impact on the plants ability to adjust their primary and secondary metabolism. Systems biology techniques and omics-based research enabled the recent discovery of molecules that regulate this stress-regulatory cross-talk. Plants that are relatively healthy, more tolerant of abiotic stress, and more disease-resistant are being developed using hormonal cross-talk engineering (Mangal et al. 2023). In this chapter, we summarise the previous work, highlight the importance of melatonin in the integrated management of pathogens, and outline the path for future investigations.

11.2

Melatonin: A Master Regulator of Plants

Melatonin, also known as N-acetyl-5-methoxytryptamine, was chemically characterised and discovered in 1959. Subsequently, its tryptophan-based biosynthesis pathway was identified (Axelrod and Weissbach 1960). This substance was discovered in the pineal gland of cattle in frogs, other amphibians, humans, mammals, vertebrates, and invertebrates were all later found to have it (Lerner et al. 1958). It was later identified in Chenopodium rubrum L. as a substance that is typically classified as a neurotransmitter or animal hormone. Murch and Simmons (1997) studied its biosynthesis and regulatory function in plants. Melatonin exhibits auxin activity in plants and is a powerful antioxidant. It regulates the development of roots, branches, and explants, initiates seed germination and rhizogenesis, and delays the senescence of leaves (Arnao and Hernández-Ruiz 2014). Since melatonin plays many different roles and has a remarkable capacity to alter the expression of genes, it does not seem to function solely as a classical plant hormone (Altaf et al. 2022a, b, c). Here is a list of melatonin-mediated reactions that significantly up- or downregulate genes, organised didactically. 1. Melatonin controls critical factors that are released in response to stresses such as heat, cold, dehydration, salt, pH, heavy metals, chemical agents (herbicides, toxics), and high thermal and UV radiation. Abiotic stress triggers the stimulant effects of melatonin. 2. Melatonin controls bacterial and fungal plant disease infections and is a key regulator of the pathogen response, which frequently includes ethylene, ABA, salicylic acid (SA), and jasmonic acid. 3. The production of enzymes and other elements of the redox network have been shown to be influenced by melatonin. Melatonin regulates oxidative stress and ROS in plants via redox enzymes like superoxide dismutase, catalase, peroxidases, etc. as well as the compounds ascorbic acid, glutathione, and others.

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4. The first melatonin-mediated effect to be proven was that melatonin acts as an antisenescence agent (Arnao and Hernández-Ruiz 2009). Melatonin suppresses a variety of processes, including the chlorophyll degradation enzyme polyamine oxidase and an important senescence leaf gene like SAG12. 5. Melatonin also enhances or preserves photosynthesis and stomatal permeability by upregulating a number of photosystems, electron transporters, and ATPase genes. Melatonin also promotes stomatal opening under difficult circumstances by regulating guard cell anion channel proteins and dehydrins, all of which boost CO2 availability. Glyceraldehyde-3-phosphate dehydrogenases, interconversion sugar enzymes, and Rubisco components are all expressed under the influence of melatonin in the Calvin cycle. 6. Melatonin have an effect on a number of biochemical processes (Altaf et al. 2022d, e). Melatonin-treated plants performed better under abiotic stress scenarios because of elevated proline and carbohydrate content. In reaction to external melatonin treatments, a comparison transcriptional study discovered 1572 downregulated genes and 2361 upregulated genes. A pathway enrichment study revealed that plants treated with melatonin had eight pathways that were overexpressed, including nitrogen metabolism, primary carbohydrate metabolism, and osmoregulator biosynthesis. . 7. Melatonin stimulates the synthesis of flavonoids and anthocyanins during secondary metabolism (Liang et al. 2018) and controls the processes involved in the synthesis of carotenoids. 8. The generation of the genes required for melatonin synthesis is controlled by melatonin itself. Stressful situations consequently result in the production of the TDC, SNAT, ASMT, and COMT genes, which raise amounts of natural melatonin. The initial H2O2 burst is followed by a melatonin burst, which appears to be in control of the inducible expression of its receptor and its mediated reactions (Wei et al. 2018a). Enzymes involved in the production of melatonin in plants can be triggered by ROS and RNS, and melatonin itself can interact with these molecules both directly and tangentially to form a complicated redox network. 9. Melatonin’s function as a regulator in the production of plant hormone regulating enzymes and molecules is one of its most intriguing and contentious aspects (Altaf et al. 2023). Several components (enzymes, receptors, etc.) involved in the biosynthesis and catabolism of several plant hormones are regulated by melatonin. It controls polyamine metabolism as well (Gong et al. 2017). 10. There are still many unexplored areas, such as the potential role of melatonin in flowering and fructification (parthenocarpy) (Liu et al. 2018).

11.2.1 Biosynthesis Melatonin is produced differently in plants than it is in animals. In plants, several factors, including light, play a significant role in influencing how it is synthesised. The primary sites for melatonin production in plants are chloroplasts and

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mitochondria. These organelles contain various groups of enzymes that use synthetic processes to create melatonin. Since melatonin production is a two-way process, if it is stopped in the mitochondria, it will begin in the chloroplasts (Acharya et al. 2021). Phytomelatonin biosynthesis (Fig. 11.1) begins with tryptophan decarboxylase, which catalyses the conversion of tryptophan to 5-hydroxytryptophan or tryptamine to serotonin. The subsequent step in melatonin biosynthesis is catalysed by tryptophan 5-hydroxylase and is associated-hydroxylation reaction, which is primarily regulated in plants by cytochrome P450-dependent monooxygenases (P450s) and 2-oxoglutarate-dependent dioxygenases (2-ODDs). Additionally, catalyses the conversion of tryptophan to 5-hydroxytryptophan and N-acetyl tryptamine to N-acetyl serotonin. Serotonin N-acetyltransferase (SNAT), which catalyses the transferring of the acetyl group from acetylcoenzyme A to the variety of aminoglycosides and aryl alkylamine molecules, catalyses the second-to-last stage in this route. The final stage is 5-hydroxyindol O-methyltransferase, which catalyses the Acetylseratonin O-methyltransferase (ASMT) process that transforms N-acetylserotonin into phytomelatonin. Additionally, this also catalyses N-acetyl tryptamine to N-acetyl serotonin reactions and tryptophan to 5-hydroxytryptophan. The second-to-last step in this pathway is catalysed by serotonin N-acetyltransferase (SNAT), which catalyses the carrying of the acetyl group from acetylcoenzyme A to the array of aminoglycosides and aryl alkylamine molecules. The last step is 5-hydroxyindol O-methyltransferase, which catalyses N-acetylserotonin into phytomelatonin through an Acetylseratonin O-methyltransferase (ASMT) reaction.

11.3

Melatonin: An Emerging Stress Regulator

Plant stresses are usually classified as follows: biotic stresses caused by harmful organisms such as viruses, fungus, bacteria, nematodes, and insects, and abiotic stresses produced by salt, drought, cold, and heat stress (Shaik and Ramakrishna 2014). The most significant abiotic stresses that can cause losses of 50–70% in horticulture crops are drought, salt, heat, and cold. Furthermore, biotic stress, particularly from viruses, bacteria, and fungi, causes losses of 40–60%. Concerning factors include the continuous rise of consecutive and concurrent combinations of abiotic and biotic stresses, as well as global warming and the resulting environmental anomalies. In most cases, plants have a defence system to reduce these stresses, but it is only effective up to a certain threshold level (Fig. 11.2). Extreme stress reduces the plant’s natural defences, causing harm and abnormal biochemical conditions inside the cell that eventually reduce output. One class of multipurpose molecule that has been connected to a number of metabolic processes in plants is called a plant growth regulator. In addition to influencing regular physiological processes, these substances are well known for reducing a variety of diseases and physiological disorders in the majority of agricultural crops (Bari and Jones 2009). A regulating substance known as melatonin was first identified as a secreted molecule of mammalian pineal cells (Lerner et al. 1958). It is now well known that endogenous and exogenous melatonin regulate metabolic processes in plants, such as primary and

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OH HN

NH2

Tryptophan decarboxylase

NH2

TRYPTAMINE

NH Tryptamine 5hydroxylase

NH2

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HO N H

N H

SEROTONIN

IAA Serotonin Nacetyltransferase (SNAT)

acetylserotonin Omethyltransferase (ASMT)

H3C O MELATONIN

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Fig. 11.1 Melatonin synthesis pathway in plants

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BIOTIC STRESS

COLD STRESS MELATONIN DROUGHT STRESS

HEAT STRESS SALINITY STRESS

Fig. 11.2 Emerging roles of melatonin to mitigate abiotic and biotic stresses

secondary metabolism, osmoregulation, germination, photosynthesis, antisenescence, and plant hormone regulation (Arnao and Hernandez-Ruiz 2019). After its ability to scavenge ROS was found, melatonin was transformed into a phytoprotectant that can manage emerging issues such as microbial attack, heat, dehydration, and cold (Fig. 11.2). Most of these situations involve the production of ROS, which harms cells and interferes with cell balance. In addition to serving as an antioxidant for nitrogen species, this melatonin can make oxygen biologically acceptable and minimise injury brought on by stress. Melatonin, when administered exogenously, can affect a number of physiological processes in addition to helping the plant reduce stress within. Additionally, exogenous melatonin delivery prevents oxidation damage and lowers postharvest losses. The plants are protected from a severe attack after an initial infection by this melatonin, which encourages the upregulation of genes linked to salicylic acid, nitric oxide, PAMP-triggered immunity (PTI), and effector-triggered immunity (ETI) during a pathogen attack (Shi et al. 2015b). Furthermore, it has been demonstrated that melatonin treatment greatly increases the production of genes involved in the formation of auxin, ethylene, and jasmonate acid cytokinin. Multiple biotic and abiotic stresses are completely reduced as a consequence of this hormonal cross-talk (Ma et al. 2018). It also draws attention from breeders, pathologists, and physiologists in agricultural science to the reality that there is still much to learn about the possible benefits of melatonin in the ecosystem.

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11.3.1 Abiotic Stress Regulation In addition to being a powerful antioxidant, melatonin also works as a powerful free radical scavenger against potentially harmful reactive species like nitric oxide, hydrogen peroxide, singlet oxygen, hypochlorous acid, and many others. Melatonin also serves as a protective mechanism and a defence against a variety of abiotic stresses, including cold, heat, drought, and salinity. The hormone melatonin has the power to increase photosynthesis capacity, soluble protein and rubisco content, as well as nitrogen and chlorophyll content. It has the power to speed up the protein’s upregulation during leaf senescence, which is essential for photosynthesis. It plays a part in enhancing a plant’s capacity for photosynthetic activity. The following research findings are used to illustrate the distinct roles of melatonin under various stress situations.

11.3.1.1 Drought Stress The metabolism, growth, and development of vegetation are adversely affected by the prolonged drought. The plant’s defence against these harmful and deleterious impacts of stress was therefore greatly aided by the melatonin production (Sharma and Zheng 2019). Melatonin has been shown to have anti-drought stress effects. It has been shown to enhance stomatal function under drought stress. Its induction through the roots optimises a number of factors, including electrolyte leaks, chlorophyll and water content, increased photosynthesis efficiency, and stomata permeability (Naghizadeh et al. 2019). Furthermore, melatonin-treated plants that were under the drought stress had half as much ABA as melatonin-free plants. The reduced H2O2 and ABA content helps the stomata function better and withstand these stresses (Ding et al. 2018). 11.3.1.2 Heat Stress High temperatures change plant growth and development and decrease output by affecting cell permeability and enzymatic activity (Zhang et al. 2015). Under adverse circumstances, melatonin-inducing genes in plants are triggered, increasing melatonin levels. When subjected to extreme heat and thermal stress, melatonin helps increase the activity of the nitrogen-metabolising enzymes, which increases the nitrogen concentration and reduces ammonia levels. Melatonin synthesis was raised in rice under heat stress circumstances, showing melatonin’s role in heat stress resistance (Byeon and Back 2014). In a separate trial, the antioxidant qualities of melatonin improved the germination of A. thaliana seedlings by 60% when compared to the control (Hernández et al. 2015). Melotonin treatment enhanced tomato growth, the antioxidant defence system’s protection from thermal stress, and cell membrane integrity in addition to metabolic gene expression and plant development (Jahan et al. 2019). Additionally, melatonin induction significantly increased the activity of antioxidant enzymes, the transcription of genes that respond to stress, the stabilisation of the photosynthetic apparatus, and reduced the structural changes in the plants triggered by heat stress (Buttar et al. 2020). Thus, all of these studies

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showed their effectiveness in revealing the defence mechanisms of melatonin against thermal stress by minimising the damage done to different plants.

11.3.1.3 Cold Stress Cold stress deteriorates crops because it alters the molecular biology, physiology, and biochemistry of plants. Scientists are working on developing cold-tolerant crop cultivars that are commercially viable. Various plants have recently been treated with melatonin to reduce the adverse effects of cold stress. Arabidopsis thaliana plants treated with melatonin had longer roots, more fresh weight, and were taller than untreated plants (Bajwa et al. 2014). To combat oxidative damage, the activities of glutathione reductase, superoxide dismutase, and ascorbate peroxidase were increased in wheat seedlings after melatonin induction and as a result, plant growth increased (Turk et al. 2014). Recently, the resistance of Bermuda grass to cold, drought, and salt was enhanced by exogenous melatonin treatment. In this study, higher levels of secondary metabolites, including sugar, amino acids, alcohol, and organic acids, as well as the activation of antioxidant enzymes, were found to make melatonin more effective (Shi et al. 2015a). Furthermore, exogenous melatonin application on Camellia sinensis L. resulted in a reduction in oxidative stress helped to minimise the effects of the cold on the plant’s capacity to photosynthesise. The reduced morphological changes caused by cold stress are a result of melatonin’s enhanced antioxidant and redox homeostasis potential (Li et al. 2018). It has become popular to use various transgenic techniques to increase endogenous levels of melatonin in order to protect plants from a variety of abiotic stresses in addition to the exogenous application of melatonin. These exogenous treatments and endogenous melatonin-level augmentations have both been observed in a variety of plants, including tomatoes, pea seedlings, and rice. The growth, morphological alterations, photosynthetic carbon fixation, photosystem II capabilities, and general antioxidant enzyme activity of the plants have all been significantly influenced by these treatments. All of these studies demonstrated how well melatonin works to mitigate the adverse effects of cold stress. 11.3.1.4 Salinity Stress Environmental stress caused by salinity limits crop production and growth, resulting in substantial economic losses (Allakhverdiev et al. 2000). Due to osmotic stress and changes in the control of metabolic processes in plant cells, such as lipid and energy metabolism, protein production, and photosynthesis, salinity causes water shortages in plants (Li et al. 2012). Ion compartmentalisation, selective ion exclusion, altered photosynthetic pathways, compatible solute production, antioxidant enzyme induction, altered membrane structure, upregulated gene expression, and stimulation of phytohormones are just a few of the many strategies used by plants to deal with chronic stress (Parida and Das 2005). Recent research has identified auxinindependent melatonin effects in numerous plant growth regulators. Melatonin supplementation, which was crucial for preserving plant photosynthesis capability, suddenly decreased the salt stress in plants (Arnao and Hernández-Ruiz 2014). Additionally, melatonin treatment greatly boosts the activities of antioxidant

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enzymes and reduces oxidative stress, which is brought on by the production of ROS as a result of H2O2 scavenging (Li et al. 2012). Salinity has detrimental effects on plants in addition to stunted growth; it rapidly impacts them throughout their entire life cycle, from seed development to the ageing process. Salinity stress significantly impairs plant growth and seed germination. Melatonin also plays a role in the cellular production and metabolism of gibberellic acid and abscisic acid. Melatonin was shown to help with the substantial decrease in ABA that resulted from the downregulation of ABA biosynthesis genes and the increase of ABA degradation genes. In the meantime, it helps in the early stages of germination by upregulating GA biosynthetic genes, which enhance seed germination and plant growth in the initial cycles (Zhang et al. 2014). Another study found that melatonin induction improved soybeans’ resistance to dehydration and salt stress and caused the activation of genes that were repressed by salt stress. Melatonin is useful for boosting metabolic activity because it has the capacity to overexpress genes related to hormones, nitrogen and secondary metabolism, redox, transport, and tricarboxylic acid transformation. Due to melatonin’s capacity to counteract salt stress, many plants have displayed evidence of greater total plant development and other physical changes. Because it can counteract the negative effects of salinity stress and encourage plant growth and seed germination, this highlighted the importance of melatonin (Nawaz et al. 2016).

11.3.2 Biotic Stress Regulation Normally, plants have a highly advanced immune system to handle biotic stresses. The first barrier that prevents pathogens or insects from attacking plants is their physical defences, which include waxes, thick cuticles, and unique trichomes (Rahman et al. 2023; Watpade et al. 2023). In addition, plants produce chemical compounds to defend themselves from pathogens and herbivores. A mounting body of evidence from the recent past suggests that melatonin enhances plant’s resistance to biotic stress, which reduces agricultural output significantly and costs farmers around the globe (Arnao and Hernandez-Ruiz 2014, 2015; Weeda et al. 2014; Moustafa Farag et al. 2019). Melatonin’s involvement in the virulence of crop diseases was first described in 2013 by Yin et al. Even though melatonin is well recognised for its function as a biocontrol agent that stops microbial growth, In comparison to the control, they discovered that apple plants treated with melatonin had fewer damaged leaves and a delayed disease spread. Plants are able to identify viruses through two defence systems (Fig. 11.3). The first one is a sensor that recognises patterns in molecules that are linked to pathogens (PAMPs). This basic defence system is known as PAMP-triggered immunity (PTI). Here, pattern recognition kinase receptors (PRR-RLK) are stimulated by melatonin, which helps in recognition. This activates a number of defence-related genes by signalling the nucleus through the MAPK pathway. Plant resistance (R) proteins make up the second immune pathway. These proteins recognise pest- or pathogen-specific effectors (Avr proteins) and initiate the plant’s immune system in a process known

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Fig. 11.3 Zigzag model of the plant immune system. ETS Effector-Triggered Susceptibility, ETI Effector-Triggered Immunity, PAMPS Pathogen-Associated Molecular Patterns, PTI PAMPTriggered Immunity

as effector-triggered immunity (ETI). In turn, this triggers hypersensitive responses (HR), which include programmed cell death in affected cells and their environs through the production of ROS. Melatonin aids the NBS-LRR in better recognising the effectors, which in turn helps the NBS-LRR recognise the effectors more effectively. Later, after the pathogen’s infiltration, the cue for the activation of genes involved in defence hits the nucleus. Among the signalling pathways that PTI and ETI induce, ethylene (ET), jasmonic acid (JA), and salicylic acid (SA) figure out as prominent plant hormones. While the SA mechanism stimulates defence against hemibiotrophic and biotrophic pathogens, the ET and JA pathways are commonly triggered against insects and necrotrophic pathogens. Usually, the three hormones SA, JA, and ET communicate two effective defence systems against plant diseases (Rather et al. 2022; Thakur et al. 2023). The initial one is referred to as systemic acquired resistance (SAR), which is triggered after initial infection with a necrotizing pathogen and is accompanied by increasing levels of SA and associated pathogenic proteins. The second form of plant resistance is called induced systemic resistance, and it depends on JA and ET for signalling. It is brought on by specific types of non-pathogenic microbes that infect roots (Tiwari et al. 2022). The reduction of sucrose to glucose and fructose, which are then transformed into cellulose and galactose, respectively, and take part in calcium deposition and cell wall reinforcement, is another pathway that results from the activation of the cell wall invertase by melatonin in the presence of the pathogen. Based on studies into the model of the interaction between Arabidopsis and P. syringae, which demonstrated that melatonin increased the production of SA and ethylene-dependent genes while blocking those effects in mutants with a deficiency in SA and ethylene signalling (Lee et al. 2014), Arnao and Hernández-Ruiz (2015) found that the early reactive surge of a pathogen

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attack appears to increase phytomelatonin levels within recipient cells. Immune responses are mediated by a complex signalling network that also involves other factors in addition to phytohormones. Increasing data indicates that ROS and NO generated during pathogen attack play crucial roles in both the early and later phases of the plant defence response, as well as that NO and ROS play crucial roles in melatonin-mediated immunity responses and mitogen-activated protein kinases (MAPKs). Therefore, the role of melatonin and ROS NO in biological defence has been thoroughly studied. All of these findings indicate that melatonin functions in plants natural defence against microbes via a SA/JA/ethylene and NO-dependent mechanism. Thus, the role of melatonin in controlling plant pathogens has been briefly discussed.

11.3.2.1 Antifungal Effects Melatonin is well known for its ability to act as an amphiphilic free radical scavenger. By reducing stress tolerance, altering cell ultrastructure, and inhibiting mycelial growth, the exogenous application of melatonin significantly reduced the potato late blight. Notably, melatonin’s synergistic antifungal effects on Phytophthora infestans suggested that it could reduce the dosage and increase the effectiveness of fungicides against potato late blight. Melatonin was found to have a significant impact on many differentially expressed genes related to stress tolerance, fungicide resistance, and virulence, according to transcriptome analysis. These results provide a potential eco-friendly biocontrol strategy for plant diseases using a melatonin-based paradigm, advancing our knowledge of the direct effects of melatonin on pathogens (Zhang et al. 2017). Similar to this, exogenous melatonin treatment led to the accumulation of three folds more glucosinolates and markedly increased the expression of genes for glucosinolate biosynthesis, significantly contributing to Brassica rapa resistance to Sclerotinia sclerotiorum (Teng et al. 2021). In a similar way, exogenously applied melatonin may improve apple resistance to Marssonina apple blotch (Diplocarpon mali) by controlling hydrogen peroxide levels, antioxidant enzyme activity, and pathogenesis-related protein activities. By pretreating melatonin, plants were able to keep constant internal hydrogen peroxide levels and boost the activity of defence-related enzymes, potentially enhancing disease resistance (Yin et al. 2013). Because melatonin is better and more beneficial for both people and animals, exogenous application may be a viable farming strategy to protect plants against pathogens. Melatonin increased tomato crop resistance to Botrytis cinerea by regulating H2O2 generation and the signalling role of jasmonic acid (Liu et al. 2019). By changing the regulation of the genes related to ETI- and PAMPmediated defences, a rise in melatonin buildup in watermelon and other cucurbits strengthens defences against foliage diseases like powdery mildew and soil-borne oomycetes (Mandal et al. 2018). After melatonin treatment, both the frequency and the amount of Plasmodiophora brassicae infections in Arabidopsis thaliana dropped. This reduction was ascribed to the elevated expression of the JA-responsive PR3 and PR4 genes (Chang et al. 2018). By triggering antioxidant enzymes and raising the expression of genes linked to antioxidants during this preparation, melatonin treatment greatly lowered powdery mildew on cucumber

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Table 11.1 Role of exogenous melatonin treatment in plant–fungal interaction Plant Malus prunifolia

Pathogen Diplocarpon mali

Musa acuminata Fragaria ananassa

Fusarium oxysporum

Citrullus lanatus

Podosphaera xanthii and Phytophthora capsici

Botrytis cinerea and Rhizopus stolonifer

Mechanism involved Balanced hydrogen peroxide concentrations and plant defence activity of related enzymes Induced resistance regulation through the expression of resistance gene Antioxidant enzyme activity

Upregulation of immunity associated genes

Reference Yin et al. (2013) Wei et al. (2017) Aghdam and Fard (2017) Mandal et al. (2018)

plants, resulting in a lower disease score (Sun et al. 2021a). Phytophthora nicotianae is prevented from developing both in vitro and in vivo by melatonin treatment by disrupting the amino acid metabolic balance, according to a study by Zhang et al. (2018). Exogenous melatonin is used to boost apple sapling development, increase K levels, and induce photosynthesis, all of which decrease replant disease symptoms (Li et al. 2018). Similar results have been obtained in fungi including Botrytis spp., Penicillium spp., Fusarium spp., and Alternaria spp. (Li et al. 2018). Numerous studies have also looked at the role of endophytic rhizobacteria in boosting plant melatonin synthesis (Jiao et al. 2016). Multiple hypotheses have been proposed to describe how melatonin protects plants from fungal diseases. For instance, some researchers have proposed that the defence mechanism of melatonin includes its ability to maintain cells’ H2O2 levels at a specific level as well as the creation and regulation of antioxidant enzyme functions (Aghdam and Fard, 2017). Exogenous melatonin treatment triggered ETI- and PTI-associated genes in melons and Arabidopsis, according to new transcriptomic data (Mandal et al. 2018; Weeda et al. 2014). Melatonin also has a significant impact on how much ROS and reactive nitrogen species (RNS) are present in plants. ROS and RNS act as signals for a variety of cellular and physiological reactions to biotic and abiotic stresses, both directly (as ROS and RNS scavengers) and indirectly (through other mechanisms). The antifungal effects of melatonin on a few organisms are listed in Table 11.1.

11.3.2.2 Antibacterial Effects Melatonin efficiently exhibits antibacterial activities against bacteria. For instance, the application of synthetic melatonin to foliage reduced the frequency of the rice bacterial leaf streak (Chen et al. 2018). Additionally, it has been demonstrated that phytopathogenic bacteria like Xanthomonas oryzae pv. oryzae and X. oryzae pv. oryzicola are directly inhibited by melatonin (Chen et al. 2019b). Similarly, augmented melatonin treatment may be able to counteract the negative effects of Candidatus Liberibacter asiaticus (CLas) and the insect vector by raising melatonin

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levels, extending the lifespan of both healthy and infected vectors, and reducing the number of CLas bacteria in the vector psyllids (Nehela and Killiny 2018). Through a variety of signal transmission pathways, such as the increase of NO levels in plants, which work in combination with melatonin to upregulate SA-associated genes, plant defence genes like plant defensin, plant resistance 1 (PR1), and PR5 are activated against bacteria. Our knowledge of phytomelatonin signalling, which shuts stomata at night to prevent bacterial infiltration and water loss, underwent a paradigm shift with the identification of phytomelatonin receptor 1 (PMTR1) (Li et al. 2020). A different investigation discovered that the MeRAV2 and MeRAV1 genes, direct transcriptional activators of the genes involved in melatonin production, are essential for conferring disease resistance on plants to the bacterial blight of cassava (Wei et al. 2018b). The increase of defence genes like plant defensin (PDF1.2), plant resistance 1 (PR1), and PR5 through different signal transduction pathways is a hallmark of antibacterial defences against plant pathogenic bacteria. For instance, melatonin and elevated NO levels in plants upregulate genes linked with SA (Shi et al. 2015b). Melatonin can also trigger mitogen-activated protein kinase (MAPK) pathways, which in turn upregulate the gene isochorismate synthase 1 (ICS1) in A. thaliana that has been infected with Pseudomonas syringae Pst-DC3000 (Lee and Back 2017). Zhao et al. (2015) found that Pst DC3000-infected A. thaliana plants with elevated cell wall invertase activity in melatonin-treated Arabidopsis have enhanced cell wall fortification and callose-depositing factors. According to reports, melatonin treatment increases 1-aminocyclopropane-1-carboxylate synthase 6 (ACS6), a crucial enzyme in the production of ethylene, which in turn upregulates the PDF1.2 gene. Additionally, melatonin-related defences against (Pst) DC3000 in SA- and NO-dependent pathways in Arabidopsis involve the use of sucrose and glycerol. The role of SA- and NO-dependent pathways in Arabidopsis in melatoninrelated defence against (Pst) DC3000 was also discussed by Qian et al. (2015). Exogenous melatonin treatment triggered ETI- and PTI-associated genes in melons and Arabidopsis, according to new transcriptomic data (Weeda et al. 2014; Mandal et al. 2018). Some of the antimicrobial actions of melatonin, along with the underlying processes and advantageous impacts on plants, are listed in Table 11.2.

11.3.2.3 Antiviral Effects Studies on melatonin’s antiviral properties in plants are scarce. The antiviral effects of melatonin in plants are outlined in Table 11.3. More investigation is required to completely comprehend how melatonin impacts relationships between plants and pathogens as well as how it has a protective influence in plants. Tobacco mosaic virus (TMV) infection in Nicotiana glutinosa and Solanum lycopersicum plants was subsequently treated with synthetic melatonin, which decreased the virus content. The positive benefits of melatonin were ascribed to elevated SA amounts in the NO-dependent pathway (Zhao et al. 2019). Additionally, the apple stem grooving virus (ASGV) was effectively eradicated by melatonin from apple stems grown in vitro, raising the possibility that viral-free trees could be produced (Chen et al. 2019a).

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Table 11.2 The beneficial action of melatonin in plants infected with bacterial pathogens Plant Nicotiana benthamiana

Pathogen Pseudomonas syringae

Mechanism involved Defence genes expression

A. thaliana

P. syringae

A. thaliana, N. benthamiana

P. syringae

A. thaliana

P. syringae

A. thaliana

P. syringae

Production of pathogenesis-related (PR) genes Induction of pathogenies related genes through mitogen associated proteinase kinase (MAPK) signalling cascades Induction of PR1 and ICS1 expression genes through MAPK cascades in the coexistence H2O2 and NO Activities of cell wall invertase and vacuolar invertase

Resulting effect Inhibition of pathogen spread Increased resistance

Reference Lee et al. (2014)

Disease resistance

Lee and Back (2016)

Disease resistance

Lee and Back (2017)

Cell wall reinforcement

Zhao et al. (2015)

Lee et al. (2015)

11.3.2.4 Biocontrol Efficiency There are various methods for preventing, mitigating, or controlling plant diseases. The use of fungicides, which are used to treat and prevent disease, is one of them (Collinge et al. 2019). However, due to their possible damage to human health and the ecosystem, as well as their part in the emergence of new, resistant diseases, chemicals are causing concern (Raymaekers et al. 2020). Because of strict restrictions over their supply and use, the use of chemicals is currently declining (Bruce et al. 2017) Therefore, attempts are being made to create synthetic, chemicalfree alternatives for the prevention of pests and diseases, and one of the best alternatives is biological control. “Biocontrol” refers to the use of naturally existing microbes to control plant diseases or pests (Fravel 2005). There are many different types of organisms in nature that control pests and pathogens. It can prevent diseases effectively, either directly (through parasitism, antibiosis, and competition for nutrients) or indirectly by causing plant-mediated responses that help the plant respond more quickly and effectively to future pathogen attacks) (Vos et al. 2015). Table 11.3 Effect of melatonin on plant–virus pathosystem Plant Nicotiana glutinosa and Solanum lycopersicum Malus domestica

Pathogen Tobacco mosaic virus (TMV) Apple stem grooving virus (ASGV)

Resulting effect Reduction of virus concentration Eradication of virus

Reference Zhao et al. (2019) Chen et al. (2019a)

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Table 11.4 Biocontrol effects of melatonin on plants infected by phytopathogens Pathogen Phytophthora capsici

Plant Citrullus lanatus

Colletotrichum musae

Musa acuminate

Fusarium oxysporum

Cucumis sativus

Magnaporthe oryzae

Oryza sativa and Hordeum vulgare Oryza sativa and N. benthamiana Citrus sinensis

Xanthomonas oryzae pv. Oryzae Candidatus liberibacter and Diaphorina citri Tobacco Mosaic Virus (TMV) Alfalfa Mosaic Virus (AMV) Rice Stripe Virus (RSV)

Nicotiana glutinosa and S. lycopersicum Solanum melongena Oryza sativa

Resulting effect Enhanced plant defences and reduced pathogen development Delayed senescence and disease incidence Arbuscular mycorrhiza and melatonin increase resistance Reduced disease severity Reduces disease occurrence Increased disease resistance

Enhanced plant immunity Promotion of disease resistance Increased resistance

Reference Mandal et al. (2018) Li et al. (2019) Ahammed et al. (2020) Li et al. (2023) Chen et al. (2019b) Nehela and killiny (2020) Zhao et al. (2019) Sofy et al. (2021) Lu et al. (2019)

In plants, the induced resistance approach can be carried out passively, not only through an organism but also by using elicitors, which are natural compounds that mimic a disease. Plant-induced resistance could serve as a novel agricultural management technique (Burketova et al. 2015). In light of this, melatonin may be a perfect choice for use as an elicitor molecule in biocontrol treatment strategies. Studies are currently being performed on the impact of melatonin treatment on the prevention or control of infectious diseases in plants, including those brought on by fungi, bacteria, and viruses (Table 11.4). A recent study found that the microbial antagonist Meyerozyma guilliermondii and melatonin combined to effectively control Botrytis cinerea in postharvest apple fruit, greatly reducing the incidence of decay and lesion diameter. The defence-related enzyme activities, as well as the total antioxidants, phenolics, and lignin contents, were also noticeably elevated by M. guilliermondii and melatonin treatment. M. guilliermondii and melatonin treatment substantially upregulated the expression of genes linked to the pathogenesis and the jasmonic acid (JA) signalling pathway (Sun et al. 2021b).

11.3.2.5 Disease Resistance Effects of Melatonin Plant diseases caused by bacteria, fungi, and viruses pose a serious threat to plants because they are frequently infectious and even fatal. Therefore, a major goal of plant breeding is to devise a method to increase the disease resistance of plants. Recently, melatonin-treated plants were found to have a wide range of beneficial effects. According to Yin et al. (2013), pretreatment with melatonin increased the resistance of apples to the Marssonina apple blotch caused by Diplocarpon mali. It

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has been demonstrated that melatonin treatment increases photosystem efficiency as well as antioxidant and defence-related enzyme activities. Since melatonin is an eco-friendly compound, using it as a preventative measure for pathogen infections in plants could be cost-effective. Melatonin may also function as a defence signalling molecule that aids in defence against the virulent bacterium P. syringae (Pst) DC3000 in Arabidopsis (Lee et al. 2014). Further investigation revealed that Pst DC3000 significantly increased melatonin and nitric oxide (NO) levels and that melatonin treatment had no significant influence on innate immunity in NO-deficient mutants. According to these findings, melatonin increased disease resistance to bacterial pathogen infection by increasing NO production (Shi et al. 2015b). Exogenous melatonin has been shown to enhance banana plant resistance to Fusarium wilt by controlling the expression of heat shock proteins (Wei et al. 2017).

11.4

Role of Melatonin in Preharvest and Postharvest Diseases

Postharvest losses in perishable commodities such as fruits and vegetables can range from 20% to 40% and can occur at any stage of processing after harvest, which includes gathering, moving, storing, and selling. To reduce postharvest losses, postharvest control methods must be successful and efficient. Several postharvest procedures have been suggested for lowering decay, which ultimately improved the produce’s storage life. In recent years, several novel molecules have demonstrated their potential for use in the postharvest management of various fruits and vegetables, including 1-methylcyclopropene (1-MCP), nitric oxide (NO), salicylic acid (SA), and brassinosteroids (BRs) (Jayarajan and Sharma 2018). According to a review of recent literature, melatonin has the potential to assume the place of these molecules and/or methods in the postharvest management of fruits by reducing biotic and abiotic stresses. Pre-harvest applications of melatonin, such as soaking of seeds, irrigation of plants, and spraying of trees, have been suggested as useful strategies to increase yield and quality properties in various fruits. This is because melatonin is effective in promoting fruit setting and development, regulating fruit ripening in orchard trees, and inducing disease resistance against various pathogens. Grey mould, caused by the fungus Botrytis cinerea, is one of the most damaging fungi, causing significant losses in tomatoes during the pre- and postharvest stages. Due to the increase in disease resistance during storage, a postharvest melatonin supplement may reduce the growth of grey mould on cherry tomato fruit. Various fruits, including strawberries, kiwifruit, peaches, and plums, can be treated with exogenous melatonin to significantly improve disease resistance and reduce the likelihood of decay occurring while the fruits are in storage (Table 11.5). Experts are exploring the use of melatonin for a range of postharvest problems as a better option for the management of postharvest diseases of fresh vegetables and fruits, which have been on the rise. Since most fruits have a high moisture content, they are prone to microbial attack, which eventually causes spoilage in the harvested produce. Therefore, it is imperative to take precautions to avoid mechanical harm, bruises, and microbial decay. Melatonin is a potent antioxidant that has proven to

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Table 11.5 Effect of melatonin on Postharvest diseases Botanical name Citrus sp.

Crop Citrus Grape

Vitis vinifera L. Litchi chinensis

Litchi

Strawberry Plum

Fragaria ananassa Prunus salicina

Effect Decay was decreased which is caused by Penicillium digitatum Enhanced disease resistance and flavonoid biosynthesis

References Lin et al. (2019) Gao et al. (2020)

Reduced the pericarp browning and discolouration of fruits. Inhibited fungal decay caused by Peronophythora litchii. Reduction of postharvest decay caused by Botrytis rot Inhibited decay and enhanced antioxidants

Zhang et al. (2021) Aghdam and Fard (2017) Bal (2019)

be useful in avoiding decay by limiting the development of microorganisms. By removing defence-related ROS in the affected fruits, Lin et al. (2019) found that exogenous melatonin application decreased citrus green mould disease. They specifically focused on citrus green mould (Penicillium digitatum) in their investigation. Numerous hypotheses have been proposed to describe how melatonin protects plants from fungal diseases. For instance, some researchers think that melatonin’s ability to sustain hydrogen peroxide levels in cells, as well as the creation and regulation of antioxidant enzymes, are key components of its defence mechanism (Lin et al. 2019). Even though external melatonin triggers the genes that code for antioxidant enzymes, the fundamental process regulating gene expression is still not completely known. Therefore, it is important to support an interesting study that will reveal the process.

11.5

Integrated Management of Plant Diseases Through Melatonin

To combat pathogens, plants have both passive and active defence systems. The waxy cuticle on the leaves, the cell wall, and the production of secondary metabolites are their primary pre-existing defence barriers. Physical and chemical barriers like these serve as the first line of defence against phytopathogens. There are pathogens that can get past this first layer of defence. In these circumstances, plants trigger an induced immune defence known as “Induced resistance” to limit the spread of pathogens. Plants have two levels of pathogen detection depicted in the zigzag model (Fig. 11.3) (Jones and Dangl 2006): the first level uses plant protein recognition receptors to identify relatively conserved pathogen molecules known as pathogen-associated molecular patterns (PAMPs), this resistance reaction is known as PAMP-triggered immunity (PTI). However, some pathogens can subvert this initial reaction by secreting effector proteins. The recognition of these pathogen

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virulence molecules or effectors (R) by intracellular receptors then initiates the activation of a second level of immunity. These receptors have leucine-rich repeats (NLRs) and nucleotide-binding domains that initiate effector-triggered immunity (ETI), which is typically followed by responses of hypersensitivity (HR), and ultimately leads to programmed cell death (PCD), to limit biotrophic cellular pathogens and viruses (Dodds and Rathjen 2010). Various plant hormones play a critical role in resistance by engaging the plant defence signalling network downstream of ETI or PTI activation (Katagiri and Tsuda 2010). This hormonal network includes salicylic acid (SA), ethylene (ET), and jasmonic acid (JA), all of which are necessary for the microbial defence response. While necrotrophic pathogens, which consume plant tissues both during infection and in herbivorous pests, frequently require ET/JA pathways for resistance, SA signalling favourably controls plant defence against biotrophic pathogens, which require living tissue to complete their life cycle (Bari and Jones 2009). Auxin and abscisic acid (ABA), two additional plant hormones that were initially discovered for their roles in regulating plant development processes and the abiotic stress response, have also emerged as key players in the interactions between plants and pathogens (Wang et al. 2011). Every phytohormone pathway is connected by a huge, complex network (the hormonal network). For instance, the SA-JA signalling pathway’s hormonal regulators include the ET, ABA, auxin, gibberellic acid (GA), and cytokinin (CK) networks (Pieterse et al. 2012). Melatonin has been extensively documented to significantly boost the expression of genes involved in ET, JA, CK, GA, and auxin metabolism and signalling, and this hormonal cross-talk can result in a high tolerance reaction against a variety of abiotic and biotic challenges (Moustafa-Farag et al. 2019; Ma et al. 2018). Melatonin would activate the two types of immunity mentioned above: the one mediated by PTI in response to PAMP and the one generated by the response to effectors (ETI), which would successfully protect the plants from a serious pathogen attack. Melatonin would also activate signal molecules like NO and SA as well as ROS (Shi et al. 2015b). Melatonin has the ability to effectively suppress disease growth as well as improve the host plant’s capacity to protect itself by upregulating genes involved in ROS reduction and NO generation, according to numerous studies on fungus infections. On the other hand, it has been observed that melatonin raises the amounts of cellulose, xylose, and galactose in the cell wall of bacteria-infected A. thaliana leaves and increases the formation of calluses, all of which indicate a strengthening of the physical barrier against pathogen penetration (Tiwari et al. 2020). According to Zhao et al. (2019), PRs play a role in the interaction between phytopathogens and melatonin-mediated pathogen reactions (Fig. 11.4). PRs use the redox network (melatonin-ROS-NO) (Arnao and Hernández-Ruiz 2018), a significant player in the regulation of the phytohormonal network, as an intermediary in the expression of PR genes to improve plant resistance. Melatonin produces and regulates reactive oxygen species (ROS) and reactive nitrogen species (RNS), mainly nitric oxide (NO), as part of a series of defensive responses that are brought on by this awareness. These cascades simultaneously activate the melatonin natural biosynthetic pathway, the MAPK kinase cascade, carbohydrates (cell wall fortification), and other defence hormones

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Fig. 11.4 Interaction between plant pathogens (fungi, bacteria and viruses) and defence responses mediated by melatonin. PRRs Pattern recognition receptors

like ethylene (ET), salicylic acid (SA), and jasmonic acid (JA). All of this promotes the production of defence-related and WRKY genes in plants, including PR1, PR5, and other resistance genes, which in turn promote the hypersensitive response (HR) and systemic acquired resistance (SAR). Treatment with exogenous melatonin plays a major role in this response cycle, enhancing the plant’s defence because it functions by raising the natural level of melatonin in the plant cell. As a consequence, plants melatonin-mediated defence against diseases was enhanced.

11.6

Conclusions and Future Thrust

Melatonin is now recognised as a pleiotropic plant compound with a broad variety of multiple activities. This hormone functions as a growth booster, stress protector, flowering regulator, and fruit maturation regulator by influencing various redox network-related components or interacting with other phytohormones. It will be easier to understand the mechanisms by which melatonin is connected to a range of cellular and metabolic functions in plants with the help of detailed studies of the melatonin signalling pathway, including the discovery of melatonin receptors. Significant advancement has led to the revelation of the melatonin biosynthesis process. However, future studies should concentrate on how melatonin signalling is controlled. Researchers should look into melatonin biosynthesis using the genetic tractability of reference species and the diversity of accessible genomic methods. The main function of melatonin in plants is to shield them from reactive stress, which occurs in almost all adverse weather conditions. It has particular advantages for regulating plant growth and increasing plant resistance to a range of biotic and

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abiotic challenges. In view of the current study, substantial success has been achieved in analysing the various functions of melatonin in plants, and numerous attempts have been made to explain the beneficial effect of this chemical on plants. The importance of other melatonin receptor-mediated signalling pathways during biotic and abiotic stress in plants must still be explored, although transcriptome approaches have identified melatonin’s capacity to upregulate ETI and PTI defencerelated genes. The synergistic effects of combined melatonin and antifungal treatments are an intriguing way to achieve high levels of plant pathogen resistance while using lower levels of chemical fungicides, despite the fact that many regulatory components of the melatonin-related defence signalling network have been investigated. The impacts of melatonin on plant invasion by viruses, nematodes, and insects are poorly understood, necessitating further research in this field. This organic substance performs a number of functions in the control of anti-stress, effectively encouraging development and increasing resistance, making it perfect for agricultural production that is favourable to the environment and guarantees the safety of food. The understanding of how melatonin increases the production of genes linked to disease, antioxidant enzymes, and stress-specific genes to counteract the impacts of various biotic and abiotic stressors has progressed. The essential component at the centre of the redox network might be melatonin. In cells, a special triad made up of ROS, NO, and phytomelatonin regulates redox balance. Because of this, the way melatonin affects the redox network may be used as a stimulus to develop plants that are stronger and have traits like improved photosynthesis and antisenescence genes. Evaluation of the use of synthesised melatonin for agricultural uses should be done through trials. New data raise the prospect that melatonin regulates the production of a wide range of molecules, including NO, strigolactones, and brassinosteroids, as well as transcription factors, enzymes, receptors, and receptors implicated in the signalling of melatonin, GA, SA, ethylene, and ABA. Clarifying the relationships between melatonin and different phytohormones in various processes should be the primary goal of future study. Melatonin serves a variety of purposes, making it a wonderful substance for agricultural growth. It may be a master regulator of plant defence responses to pathogen invasion.

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Exploring Melatonin’s Potential as an Alternative Strategy for Protecting Plants from Biotic Stresses

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Tanmaya Kumar Bhoi, Ipsita Samal, Deepak Kumar Mahanta, J. Komal, Prasanta Kumar Majhi, and Ankur

Abstract

Biotic stress caused by pests and pathogens is a significant challenge facing the agricultural industry worldwide. Chemical pesticides have traditionally been used to manage biotic stress, but they have negative impacts on the environment and human health. Therefore, there is a growing need for alternative strategies that are effective, sustainable, and environmentally friendly. In recent years, research has focused on the potential of melatonin as a natural molecule for managing biotic stress in plants. Melatonin has been shown to have broad-spectrum activity against insect pests and pathogens, and it can induce plant defense mechanisms. This chapter aims to provide an overview of the current research on melatoninmediated biotic stress management in plants, including its mechanisms of action, applications, and limitations.

T. K. Bhoi Forest Protection Division, Indian Council of Forestry Research and Education (ICFRE) – Arid Forest Research Institute (AFRI), Jodhpur, Rajasthan, India I. Samal (✉) ICAR-National Research Centre on Litchi, Mushahari, Muzaffarpur, Bihar, India D. K. Mahanta Department of Entomology, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India J. Komal Department of Entomology, Navsari Agricultural University, Navsari, Gujarat, India P. K. Majhi Department of Genetics and Plant Breeding, Odisha University of Agriculture and Technology, Bhubaneswar, Odisha, India Ankur Department of Entomology, Maharana Pratap University of Agriculture and Technology, Udaipur, Rajasthan, India # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 R. Kumar et al. (eds.), Melatonin in Plants: A Pleiotropic Molecule for Abiotic Stresses and Pathogen Infection, https://doi.org/10.1007/978-981-99-6741-4_12

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Keywords

Biotic stress · Melatonin · Insect pest · Pathogen

12.1

Introduction

Biotic stress induced by pests and pathogens is a major threat to agricultural productivity and food security worldwide (Arora 2018; Bhoi et al. 2023; Mahanta et al. 2023). Conventional methods for managing biotic stress rely heavily on chemical pesticides, which can have negative impacts on the human health and environment (Roberts and Mattoo 2018; Bhoi et al. 2022a, b; Samal et al. 2023). Therefore, there is a growing need to develop alternative strategies that are effective, sustainable, and environmentally friendly (Kumar et al. 2021a, b, 2022). In recent years, research has focused on the potential of melatonin as a natural molecule for managing biotic stress in plants (Tiwari et al. 2020, 2022; Kumar et al. 2019). Various organisms including plants were reported to produced melatonin (Rehaman et al. 2021; Altaf et al. 2023) and it has crucial role in regulating various plant physiological processes like growth, development, and response to diverse biotic and abiotic stresses (Okazaki et al. 2009; Kumar et al. 2022). In particular, melatonin has been shown to have broad-spectrum activity against pests and pathogens, making it a potential candidate for use in biotic stress management in crops (Murch et al. 2000; Altaf et al. 2022c, d, e). Melatonin has been demonstrated to increase the activity of many antioxidant enzymes, which aid plants in reducing the negative effects of oxidative stress brought on by biotic stress (Moustafa-Farag et al. 2019; Ali et al. 2021). Melatonin has also been found to increase the expression of defense-related genes, such as pathogenesis-related (PR) proteins, which can help to activate the plant’s innate immune response against pests and pathogens (Huffaker et al. 2011; Altaf et al. 2022a). In addition, melatonin has been found to have direct toxic effects on pests and pathogens. Studies have shown that melatonin can inhibit the growth and development of a wide range of pests and pathogens, including insects, nematodes, fungi, and bacteria (Ye et al. 2021; Altaf et al. 2022b, c). For example, melatonin has been found to inhibit the growth of the fungal pathogen Botrytis cinerea, which causes gray mold disease in various crops (Li et al. 2022). It has also been found to have insecticidal activity against pests such as the cotton bollworm and the rice stem borer (Zhang et al. 2021a, b). The use of melatonin in agriculture has several potential benefits (Mohd Fauzi et al. 2022). First, it is a natural molecule that is non-toxic and environmentally friendly. Unlike chemical pesticides, which can have negative impacts on non-target organisms and the environment, melatonin is biodegradable and does not persist in the environment (Tiwari et al. 2020). Second, melatonin has broad-spectrum activity against a wide range of pests and pathogens, making it a potentially useful tool for managing multiple biotic stressors in crops (Tiwari et al. 2021a, b; Rahman and Yang 2023). Finally, the use of melatonin in agriculture could reduce reliance on chemical pesticides and promote the development of more sustainable and environmentally

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friendly farming practices (Tiwari et al. 2022; Mangal et al. 2023). Despite the promising results of research on melatonin-mediated biotic stress management in plants, there are still some gaps in our understanding of the mechanisms and applications of melatonin. For example, the optimal conditions for applying melatonin to crops, such as the timing and dose of application, have not been fully established (Thakur 2023). In addition, the effects of melatonin on non-target organisms, such as beneficial insects and soil microorganisms, have not been fully evaluated. This chapter aims to provide an overview of the current research on melatonin-mediated biotic stress management in plants, including its mechanisms of action, applications, and limitations. Additionally, this chapter will discuss the future directions for research in this field and address the gaps in knowledge that currently exist.

12.2

Overview of Melatonin in Plants

Melatonin, also known as N-acetyl-5-methoxytryptamine is a hormone reported to regulate sleep in humans, but it also plays a crucial role in plants (Lerner et al. 1958; Reiter 1991). Melatonin is synthesized in plants through a pathway that is similar to animals, including humans (Sack et al. 1986; Tan et al. 2018). Melatonin is widely distributed in various plant parts, including roots, leaves, fruits, and seeds (Hardeland 2013). The concentration of melatonin in plants varies widely, depending on various factors such as plant species, developmental stage, and environmental conditions (Xu et al. 2015). Plants can have anywhere from picograms to milligrams of melatonin per gram of tissue. Melatonin is essential for plants to develop properly and respond to different stimuli in their environment. Melatonin is not only important for dealing with biotic stress, but also with abiotic stresses as drought, salt, and heavy metal stress (McCleery et al. 2014). By decreasing oxidative damages, modulating gene expressions, and promoting the manufacture of suitable solutes, melatonin can increase plant tolerance to abiotic stresses (Wang et al. 2012). In addition, it has been demonstrated to contribute to the health and development of plants. It stimulates cell division and elongation, which in turn promotes plant growth and improves root development (Back et al. 2016). Seed germination and early plant growth are two further areas where it can be helpful. Furthermore, melatonin can affect flowering and fruit ripening in plants (Kang et al. 2011). Melatonin can increase the manufacture of phytohormones including gibberellins and auxins, which play important roles in plant growth and development, and it can also influence the expression of genes involved in floral transition and fruit ripening (Kang et al. 2010). The physiological roles of melatonin in plants are mediated through various mechanisms, including its antioxidant activity, regulation of gene expression, and stimulation of secondary metabolites biosynthesis (Li et al. 2017). Antioxidant properties of melatonin include its ability to scavenge reactive oxygen species (ROS) and mitigate damage from biotic and abiotic stressors (Wei et al. 2018). For example, melatonin can control the expression of defense genes in plants, such as PR genes and genes involved in the manufacture of

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secondary metabolites, when they are exposed to biotic stress (Nawaz et al. 2015). Antimicrobial secondary metabolites such as phenols, flavonoids, and alkaloids are synthesized in plants in response to melatonin’s stimulation of their biosynthesis (Zhang et al. 2016). Plant defense against biotic stresses involves the manufacture of phytohormones like SA, JA, and ethylene, all of which can be induced by melatonin (Debnath et al. 2019). Several biotic elements, such as the plant’s developmental stage, as well as abiotic ones such as the intensity and quality of light, temperature, and nutrition availability have been documented to affect melatonin’s functions (Hernández-Ruiz and Arnao 2018). High light intensities and blue light encourage melatonin generation in plants, while red light suppresses it. Nutrient availability can also affect plant melatonin concentration; specifically, nitrogen availability affects melatonin generation in some plant species (Tiwari et al. 2022).

12.2.1 Melatonin Biosynthesis Process The biosynthesis process of melatonin involves a series of enzymatic reactions that convert the amino acid tryptophan into serotonin and then into melatonin (Mannino et al. 2021). The bioconversion of melatonin was reported to begin with transformation of tryptophan into 5-hydroxytryptophan (5-HTP) catalyzed by tryptophan hydroxylase in the presence of tetrahydrobiopterin (BH4), iron, and oxygen (Fig. 12.1). The second step in this pathway includes the conversion of 5-HTP into serotonin (5-hydroxytryptamine) catalyzed by the enzyme aromatic amino acid decarboxylase (AADC) in the presence of pyridoxal 5′-phosphate (PLP). Lastly, the final step is the conversion of serotonin into melatonin catalyzed by the enzyme acetylserotonin O-methyltransferase (ASMT), which transfers a methyl group from S-adenosyl methionine (SAM) to the hydroxyl group on the serotonin molecule. This reaction occurs exclusively in the pineal gland and is the rate-limiting step in the synthesis of melatonin (Yu et al. 2020). Melatonin production in plants is influenced by a variety of ecological and endogenous factors, including light, temperature, and stress (Ahn et al. 2021). Blue light, for example, has been found to enhance melatonin manufacture in plants, but red light inhibits it. Furthermore, transcription factors that bind to the promoter regions of genes involved in the biosynthetic process influence melatonin production (Liu et al. 2022). MYB transcription factors, for example, have been demonstrated to promote the expression of TDC and ASMT genes, resulting in enhanced melatonin synthesis in plants (Sun et al. 2021). Melatonin is involved in many aspects of plant physiology, such as growth and development, stress tolerance, and defense against environmental stresses. Melatonin has been demonstrated to boost seed germination, root growth, and overall crop growth and production. Through increasing antioxidant defenses and altering stress-responsive genes, melatonin has additionally been demonstrated to increase plant tolerance to abiotic stresses such as drought, salt, and heavy metal toxicity (Mandal et al. 2018).

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Fig. 12.1 Schematic representation of melatonin biosynthesis in chloroplasts and mitochondria. The biosynthesis of melatonin involves multiple enzymatic reactions in different subcellular compartments (a, b). The tryptophan (Trp) is converted to serotonin (5-HT) by tryptophan hydroxylase (TPH) in the cytosol, which is then transported to the chloroplasts and mitochondria by serotonin transporter (SERT). In the chloroplast, serotonin is converted to N-acetylserotonin (NAS) by serotonin N-acetyltransferase (SNAT). NAS is further converted to melatonin by the action of N-acetylserotonin O-methyltransferase (ASMT) in the mitochondria. The final product melatonin is then transported to different tissues through the vascular system. Aromatic amino acid decarboxylase (AADC or DOPA decarboxylase)

12.2.2 Mechanisms of Melatonin-Mediated Biotic Stress Management Melatonin is a hormone that is synthesized in plants and animals. It is well known for its role in regulating sleep in humans, but in plants, it plays a crucial role in biotic stress management (Sharma and Zheng 2019). Melatonin-mediated biotic stress management in plants involves various mechanisms that work together to enhance plant defense against biotic stressors, such as pathogens and pests. One of the key mechanisms by which melatonin mediates biotic stress management in plants is through its antioxidant activity. Melatonin is a potent antioxidant that can scavenge reactive oxygen species (ROS) and reduce oxidative damage caused by biotic stressors (Tiwari et al. 2021a, b). ROS are generated in plants in response to biotic stressors, and they can cause significant damage to plant cells and tissues. Melatonin can enhance the activity of antioxidant enzymes like superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), which were reported to detoxify ROS. Furthermore, it is also capable of increasing the concentration of non-enzymatic

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antioxidants like ascorbate and glutathione, which subsequently enhances the antioxidant capacity of plants (Jahan et al. 2021). Another mechanism by which melatonin mediates biotic stress management is through the regulation of defense genes expression (Zhao et al. 2021). Melatonin is reported to have a crucial role in biosynthesis of secondary metabolites including pathogenesis-related (PR) genes like defense-related genes. PR genes such as PR1, PR2, and PR5 have been linked to systemic acquired resistance (SAR), which can provide long-term protection against biotic stressors by priming the plant’s defense response (Li et al. 2021) and code for proteins that are essential for plant defense against biotic stressors (Altaf et al. 2023). SAR can provide long-term protection against biotic stressors by priming the plant’s defense response (Li et al. 2021). Melatonin can also induce the synthesis of phytohormones, such as salicylic acid (SA), jasmonic acid (JA), and ethylene, which are involved in plant defense against biotic stress (Behera et al. 2023; Mangal et al. 2023; Lal et al. 2020, 2022). SA is associated with SAR, while JA and ethylene are involved in plant defense against insect pests and pathogens. Melatonin can increase the concentration of SA in plants, which can trigger the expression of PR genes and enhance plant defense against biotic stress (Zhan et al. 2021). Melatonin can also increase the synthesis of JA and ethylene, which can activate the plant’s defense response against insect pests and pathogens. Melatonin promotes biotic stress management by stimulating the production of secondary metabolites, which are not directly engaged in plant growth and development but play an important role in plant defense against biotic stressors (Khan et al. 2022). Melatonin can stimulate the biosynthesis of secondary metabolites, such as phenols and flavonoids, which have antimicrobial properties (Bano et al. 2022). These secondary metabolites can also act as signaling molecules and enhance plant defense against biotic stressors. Melatonin can also induce the biosynthesis of alkaloids, which are toxic to herbivores and can deter insect pests. Further, it can also enhance the expression of genes involved in cell wall fortification, lignin synthesis, and callose deposition, thus it increases the plant’s ability to repair damage caused by biotic stressors by inducing the expression of genes involved in DNA repair and protein synthesis (Fahad et al. 2021).

12.3

Melatonin-Mediated Induced (MIR) Resistance Against Insect Pests

Several studies have shown that the application of exogenous melatonin can induce resistance in plants against insect pests. Zhou et al. (2021) demonstrated that the combination of nano-selenium and melatonin might reach the best overall performance by lowering the wheat aphid, Sitobion avenae population by 52.2%. The study reveals that combining nano-Se and melatonin could boost wheat resistance to aphids more effectively by promoting volatile organic compound synthesis and modulating phenylpropane and indole metabolism pathways. One possible explanation for the induced resistance by melatonin is the activation of the jasmonic acid (JA) signaling pathway. The JA signaling pathway is a key regulator of plant defense

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against insect pests. Melatonin treatment has been shown to enhance the expression of genes involved in the JA signaling pathway, leading to an increase in the production of defensive compounds and the regulation of plant defense responses. However, the precise mechanism of action of melatonin in activating the JA signaling pathway is not fully understood and requires further investigation. Dutch elm disease (Ophiostoma ulmi), which is caused by a fungus that spreads when an elm beetle (Scolytus multistriatus Marsham) consumes an elm tree, has killed off almost all American elm (Ulmus americana L.) trees (Saremba et al. 2017). Melatonin, serotonin, and jasmonic acid concentrations skyrocketed as a result of the trees’ reaction to insect damage. The surges in serotonin and melatonin were 7000 times higher than the resting values. Spikes in jasmonic acid were roughly ten times higher than resting levels, with one particularly large spike seen (Saremba et al. 2017). Insect pests and phytopathogens were observed to induce diverse multimodal phytohormone cascades and disease – insect pest resistance is dependent on both qualitative and quantitative quantum of jasmonic and salicylic acid levels in tissues. Melatonin, being one of the earlier signaling molecules responding to plant damage has significant contributing role in conferring plant resistance either singly mediating the salicylic acid and jasmonic acid signaling or in an interactive manner (Sherif et al. 2016, 2017). There has been little research done on the use of melatonin as a potential treatment for insect infestations in forest trees and agricultural crop. Further research is needed to assess the efficacy of melatonin and the best application methods for its usage in forest management. Knowing how melatonin and serotonin combine to protect plants against these insects and other biotic stresses will be an exciting future study. Similarly, its potential contribution to viral acquisition and transmission on significant vectors might be studied. Melatonin and other insecticide interactions could be studied in order to control insects with less chemicals overall.

12.4

Melatonin-Mediated Induced (MIR) Resistance Against Pathogen

Melatonin-mediated induced resistance (MIR) against pathogens has been observed in several plant species (Shi et al. 2015). However, the exact mechanisms underlying MIR in plants are still not fully understood. One example of MIR in plants is the induction of resistance against the fungal pathogen Botrytis cinerea in grapes (Li et al. 2022). In current study, the authors observed that treatment with melatonin induced the expression of several defense-related genes, including those encoding for chitinases and PR proteins. Moreover, melatonin treatment also enhanced the production of ROS and phytohormones, both of which are important signaling molecules involved in the plant’s immune response. As a result of these changes, the grapes treated with melatonin exhibited a higher level of resistance against Botrytis cinerea compared to untreated plants. However, not all studies have shown a clear link between melatonin and MIR in plants. For example, a study of tomato plants afflicted with the bacterial pathogen Pseudomonas syringae pv. tomato failed to identify any noteworthy modifications to the expression of

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defense-related genes or the generation of ROS or phytohormones in rebuttal to melatonin treatment (Zhu et al. 2019). So, the exact ways in which MIR works in plants may depend on the pathogen and plant species involved. Moreover, MIR in plants has potential implications for agriculture. For example, MIR could be used to develop crops that are more resistant to specific pathogens, reducing the need for broad-spectrum pesticides (Yin et al. 2013). However, the use of melatonin-based treatments in agriculture may have some limitations. For example, the effects of melatonin on plant growth and development are not well understood, and it is possible that long-term treatment with melatonin could have negative impacts on plant growth and yield. Additionally, the potential effects of melatonin-based treatments on non-target organisms, such as pollinators or beneficial insects, are not well understood.

12.5

Role of Melatonin in Modulating Interactions with Plant-Beneficial Microbes and Non-target Organisms (Pollinator and Biocontrol Agents)

Melatonin is engaged in both plant–pathogen interactions and plant-beneficial microbial interactions (Qu et al. 2020). However, the precise processes behind melatonin’s impacts on plant–microbe interactions are still unexplained. Melatonin’s role in encouraging the growth and development of plant-associated microbes such as rhizobia and mycorrhizal fungi is one example of its effects on plant–microbe interactions (Liu et al. 2021). In a study on soybean plants, the authors found that treatment with melatonin increased the number of nodules formed by rhizobia, which are important for nitrogen fixation in the plant. Moreover, melatonin treatment also enhanced the colonization of roots by mycorrhizal fungi, which are important for nutrient uptake in the plant. These results suggest that melatonin can play a positive role in promoting the establishment and function of plant-associated microbes (Ren et al. 2019). However, the use of melatonin-based treatments in agriculture may have some limitations. For example, the effects of melatonin on plant-beneficial microbe interactions may be dependent on the specific microbe and plant species involved. Therefore, the use of melatonin-based treatments may need to be tailored to the specific crop and environment. Additionally, the potential effects of melatonin-based treatments on non-target organisms, such as pollinators or beneficial insects, are not well understood.

12.6

Factors Affecting Melatonin-Mediated Biotic Stress Management

Melatonin-mediated biotic stress management in plants can be influenced by various factors. These factors can affect the production of melatonin, as well as its activity and effectiveness in combating biotic stressors. Some of the factors affecting melatonin-mediated biotic stress management are:

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Light Intensity and Quality Light is a critical factor that regulates the biosynthesis and activity of melatonin in plants. High light intensity and blue light have been shown to increase the production of melatonin, while red light inhibits its production. The optimal light conditions for melatonin-mediated biotic stress management may vary depending on the plant species and biotic stressor (Tiwari et al. 2021a, b). Temperature Temperature is another critical factor that affects melatonin biosynthesis and activity in plants. Melatonin production is higher at low temperatures, and it has been shown to enhance plant tolerance to cold stress. However, high temperatures can reduce melatonin production, which can compromise its effectiveness in managing biotic stress (Raza et al. 2022). Nutrient Availability Nutrient availability is essential for plant growth and development, and it can also affect melatonin production and activity (Lal et al. 2021, 2022). For example, nitrogen availability has been shown to influence melatonin biosynthesis in plants. Additionally, the application of certain nutrients, such as potassium and calcium, can enhance melatonin-mediated biotic stress management (Tiwari et al. 2021a, b). Plant Developmental Stage The stage of plant growth and development can affect the production and activity of melatonin. For example, melatonin production is higher in young plants, and it decreases as the plant matures (Wang et al. 2022). The timing of melatonin application may need to be adjusted based on the plant’s developmental stage for optimal biotic stress management.

12.7

Melatonin Application Method in Plants

Melatonin is a promising natural compound that can be used to reduce plant biotic stress caused by pathogens, pests, and other harmful organisms (Tiwari et al. 2020). Several studies have demonstrated the potential of melatonin as a tool for improving plant health and reducing damage from biotic stress (Savvides et al. 2016). However, the application method of melatonin can vary depending on the plant species and the type of biotic stress being addressed (Table 12.1). One common method of melatonin application is foliar spray (Yang et al. 2021). Foliar spray involves applying a solution of melatonin directly onto the leaves of the plant. This method is effective for treating biotic stress caused by leaf-dwelling pests and pathogens, such as aphids and powdery mildew. For example, a study on cucumber plants found that foliar application of melatonin reduced the severity of downy mildew infection by increasing the expression of defense-related genes and enzymes (Sun et al. 2019). Similarly, a study on wheat plants found that foliar application of melatonin reduced the damage caused by aphid infestation by increasing the production of secondary metabolites that deter insect feeding (Zhou et al. 2021). Melatonin foliar treatment, however, may not be helpful for all types of biotic stress. Soil-borne diseases, for example, Fusarium and Phytophthora are not immediately exposed to foliar spray

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Table 12.1 Melatonin-mediated biotic stressor interaction and their resultant effect SL. No. 1

Plant species Brinjal

2

Arabidopsis

3

Strawberry

4

Biotic stressor Alfalfa mosaic virus (AMV)

Method of melatonin treatment Foliar application

Pseudomonas syringae Botrytis cinerea

Foliar application Fruit dipping

Wheat

Sitobion avenae

Foliar application

5

Tomato

Pseudomonas syringae pv. tomato

Foliar application

6

Rice

Foliar application

7

Cucumber

Xanthomonas oryzae pv. oryzae Aphis gossypii

8

Apple

Marssonina apple blotch

Foliar application Foliar application

9

Tobacco

Tobacco mosaic virus

Root irrigation

10

Apple

Apple stem grooving virus

To the shoot proliferation medium

Resultant effects Melatonin having antiviral activity against AMV Inhibition of pathogen propagation Reduction of postharvest decay in stored strawberry fruits Melatonin boosting wheat resistance to aphids There are no significant changes in the expression of defenserelated genes or the production of reactive species or phytohormones in response to melatonin treatment Inhibit the proliferation of Xanthomonas Inducing host plant resistance in plant Activities of plant defense-related enzymes Reduction of virus concentration in infected plants Eradication of virus from previously infected shoot tip

References Sofy et al. (2021) Lee et al. (2014) Aghdam and Fard (2017) Zhou et al. (2021) Zhu et al. (2019)

Chen et al. (2018) Liu et al. (2022) MoustafaFarag et al. (2019) Zhao et al. (2019) Chen et al. (2019)

and may be unaffected by this mode of administration. Also, foliar spray may not be effective in alleviating biotic stress that damages the plant’s roots. As a result, seed priming is another route of melatonin delivery. Seed priming entails soaking the seeds in a melatonin solution before sowing. This approach is useful for addressing biotic stress on the plant’s roots, such as root rot and nematode infestation (Zhang et al. 2021a, b). Moreover, seed priming with melatonin has the added advantage of promoting seed germination and seedling growth. For example, a study on rice plants found that seed priming with melatonin increased the germination rate and improved the growth and development of seedlings under salt stress conditions.

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However, the effectiveness of seed priming with melatonin may depend on the concentration and duration of the treatment, as well as the plant species and the type of biotic stress being addressed. Moreover, the potential for seed-borne transmission of melatonin and its effects on non-target organisms need to be further investigated. Furthermore, another method of melatonin application is soil drenching (Ahammed et al. 2020). Soil drenching involves applying a solution of melatonin directly onto the soil around the roots of the plant. This method is effective for treating biotic stress that affects the roots and the soil microbiome, such as soil-borne pathogens and soil-borne pests.

12.8

Potential of Melatonin in Plant to Combat Biotic Stress

Melatonin is a potent antioxidant and signaling molecule that has been shown to have several applications in plants to combat biotic stress (Zhao et al. 2013). Pests and diseases generate biotic stress in plants, which can result in severe yield losses and crop quality degradation (Tan et al. 2012). Melatonin can operate as a signaling molecule to activate plant defense mechanisms against pests and diseases, as well as improve the effectiveness of other pest management measures.

12.9

Use of Melatonin as a Biostimulant

Melatonin has been proved as a biostimulant to boost plant growth and development, as well as crop quality and yield (Sun et al. 2021). It can boost seed germination, root development, photosynthetic efficiency, and the manufacture of secondary metabolites including phenolics and flavonoids (Sharif et al. 2018). It has also been demonstrated to boost plant tolerance to abiotic stress, such as drought and salt stress, by lowering oxidative damage and modulating gene expression. Many studies have indicated that melatonin has a positive influence on crop development and yield as a biostimulant. For example, the application of exogenous melatonin to tomato plants resulted in increased seed germination, root and shoot growth, photosynthetic efficiency, and yield (Siddiqui et al. 2019). Similarly, melatonin treatment of rice plants resulted in increased grain yield and quality, as well as improved tolerance to salt stress (Xie et al. 2020).

12.10 Melatonin in Biological Control Melatonin has also been investigated as a potential biological control agent for managing pests and diseases in plants. Melatonin can stimulate the biosynthesis of secondary metabolites, such as phytoalexins and flavonoids, which have antimicrobial and insecticidal properties (Ben Mrid et al. 2021). In addition, melatonin can induce the expression of genes involved in plant defense against pests and diseases, such as pathogenesis-related (PR) genes (Kaur et al. 2022). Several studies have

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demonstrated the potential of melatonin as a biological control agent for managing pests and diseases in plants. For example, melatonin treatment of cucumber plants infected with the fungal pathogen Fusarium oxysporum resulted in increased expression of defense-related genes and reduced disease severity (Ahammed et al. 2020). Similarly, melatonin treatment of cucumber plants infected with downy mildew resulted in increased resistance to the pathogen and decreased disease severity (Sun et al. 2019).

12.11 Melatonin in Integrated Pest Management (IPM) Insects, like many other animals, depend on the hormone melatonin to keep their circadian cycles in tune. Melatonin is capable of altering the insects’ circadian rhythms, thus diminishes their feeding and reproduction has piqued scientific interest in its potential application as a natural pesticide in recent years. It has been found that melatonin can alter insect feeding behavior. For instance, melatonin has been demonstrated to lessen the feeding activity of crop pests like the brown planthopper (Nilaparvata lugens) (Shi et al. 2021). Melatonin, when given orally to Halyomorpha halys (Heteroptera: Pentatomidae), has been shown to cause the insects to grow smaller, stop eating, remain in the nymphal stage longer, and accumulate more fat than their untreated counterparts. Moreover, this treatment did not influence the occurrence of diapause in females, but it did delay gonadal development in males (Niva and Takeda 2003). While the quantities of antioxidant enzymes (GST, SOD, POD, and CAT) were shown to rise after treatment with melatonin, the survival rate of A. cerana cerana was reported to be negatively impacted in another investigation (Fan et al. 2021). Also, it was shown that the amplitude of free-running cycles was directly correlated with the melatonin concentration (Yamano et al. 2001), suggesting melatonin had a substantial function in controlling the circadian rhythm of insects. In addition, melatonin administration in Spodoptera litura (Lepidoptera: Noctuidae) resulted in an increase in antioxidant activity and an inhibition of GST and AChE in majority of the tissues tested (Karthi and Shivakumar 2015). Melatonin’s direct effects on insect feeding and reproduction, as well as its indirect effects on plant immunity, make it a key component in biological pest control. Exogenous melatonin as an alternative to toxic chemical insecticides has the potential to make pest control more humane and environmentally friendly. Overall, there is mounting evidence that melatonin holds promise as a natural and environmentally acceptable alternative to conventional chemical pesticides, despite the fact that its usage as a pesticide is still in its infancy. Melatonin has been shown to be useful in controlling pests, although further study is needed to determine how exactly this hormone exerts its influence. Thus, melatonin can also be incorporated into integrated pest management (IPM) programs, which involve the use of multiple strategies to manage pests and diseases in an environmentally sustainable manner (Leskey and Nielsen 2018). In IPM, melatonin can be used in combination with other strategies, such as cultural practices, biological control, and chemical control, to manage pest and disease outbreaks.

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12.12 Future Directions for Research on Melatonin-Mediated Biotic Stress Management Research on melatonin-mediated biotic stress management in plants is a rapidly evolving field, and there are several future directions that could advance our understanding of its potential and limitations. Elucidation of Melatonin Signaling Pathways It is well-known that melatonin can protect plants from the damaging effects of biotic stress, but the precise signaling routes by which it does so remain unknown. Melatonin has been shown to have protective effects, although more study is needed to determine the receptors and downstream targets responsible for these effects. Identification of Target Organisms While melatonin has been shown to have a broad spectrum of activity against biotic stressors, it is unclear which organisms are most susceptible to its effects. Further research is needed to identify the specific pests and pathogens that can be effectively controlled with melatonin and to determine the optimal dosage and application methods for these organisms. Integration with Other Management Strategies While melatonin has the potential to be an effective component of integrated pest management programs, more research is needed to understand how it can be used in combination with other management strategies such as chemical control and biological control. Research on the synergistic or antagonistic effects of combining melatonin with other strategies will help to optimize its efficacy and minimize negative impacts. Optimization of Application Methods The efficacy of melatonin is highly dependent on the method of application, and further research is needed to optimize application methods and dosages. Factors such as the timing and frequency of application, the method of application (spray, drip irrigation, etc.), and the formulation of the melatonin product (e.g. liquid, powder, granular) can all influence the efficacy of melatonin in mitigating biotic stress. Evaluation of Long-Term Effects While melatonin has been shown to have shortterm benefits in mitigating biotic stress, there is a lack of research on its long-term effects on plant growth, development, and yield. Further research is needed to determine the potential risks and benefits of long-term use of melatonin in agriculture. Assessment of Environmental Impacts While melatonin is generally considered to be a safe and environmentally friendly alternative to chemical pesticides, more research is needed to assess its potential impacts on non-target organisms and the broader ecosystem. Research on the potential accumulation of melatonin in soil and water, and its effects on soil microbial communities and beneficial insects, will help to inform the development of sustainable agricultural practices.

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Identification of New Sources of Melatonin Currently, most melatonin used in agriculture is synthesized chemically, but there is growing interest in developing plant-based sources of melatonin. Research on the biosynthesis of melatonin in different plant species, and the development of plant varieties with higher melatonin content, could provide a more sustainable and cost-effective source of this biostimulant.

12.13 Conclusion Melatonin is a naturally occurring molecule in plants that has shown great potential for mitigating biotic stress in agriculture. It can act as a biostimulant, inducing plant growth and development, and has been shown to have broad-spectrum activity against pests and pathogens. Its use in integrated pest management strategies can reduce reliance on chemical pesticides and minimize negative impacts on the environment and human health. While there are still limitations and knowledge gaps in our understanding of the mechanisms and applications of melatonin in biotic stress management, continued research in this area could lead to the development of more effective and sustainable agricultural practices. Melatonin has the potential to be an important tool in the fight against biotic stress in crops, helping to ensure food security and sustainability in the face of growing global challenges.

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