Melatonin: Role in Plant Signaling, Growth and Stress Tolerance: Phytomelatonin in normal and challenging environments (Plant in Challenging Environments, 4) [1st ed. 2023] 3031401727, 9783031401725

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Plant in Challenging Environments 4

Soumya Mukherjee Francisco J. Corpas   Editors

Melatonin: Role in Plant Signaling, Growth and Stress Tolerance Phytomelatonin in normal and challenging environments

Plant in Challenging Environments Volume 4

Series Editors Dharmendra K. Gupta, Ministry of Environment, Forest and Climate Change of India, New Delhi, India José Manuel Palma, Estación Experimental del Zaidín, Granada, Granada, Spain Francisco J. Corpas, Estación Experimental del Zaidín, Granada, Granada, Spain

This book series provides recent advancements in wide areas related to higher plants and how they adapt / evolve under environmental changes in a scenario of climate change. It investigates plants under the complementary point of views, including agronomy aspects (vegetables and fruits), nutrition and health (food security), “omics,” epigenetics, contamination by heavy metals, environmental stresses (salinity, drought, high and low temperatures), interaction with beneficial or pathogenic microorganisms, and application of exogenous molecules (nitric oxide, melatonin, chitosan, silicon, etc.) to palliate negative effects. It also includes changes due to climatic condition (high/low rainfall) taking into account that the climate change is often the reason why plants evolve in a challenging environment. This book series also covers molecular-/cellular-level responses of plants under different climatic reasons. Families of molecules derived from hydrogen peroxide (H2O2), nitric oxide (NO) and hydrogen sulfide (H2S) designated as reactive oxygen, nitrogen and sulfur species (ROS, RNS and RSS, respectively) are included since, depending on the production level, they function both as signal molecules and as a mechanism of response against adverse/changing environmental conditions that can produce multiple cellular damages, alter the redox state or even trigger cell death. During these ensued metabolic processes, some anti-oxidative/oxidative enzymes are also disturbed or triggered abruptly, but there are adequate mechanisms of regulation/homeostasis in the different subcellular compartments to keep these enzymes under control. In the last decades, the progression in this field has been enormous, but still there is so much in this field to understand the plethora of phenomena behind.

Soumya Mukherjee  •  Francisco J. Corpas Editors

Melatonin: Role in Plant Signaling, Growth and Stress Tolerance Phytomelatonin in normal and challenging environments

Editors Soumya Mukherjee Jangipur College, Department of Botany University of Kalyani Jangipur, India

Francisco J. Corpas CSIC Estación Experimental del Zaidín Granada, Granada, Spain

ISSN 2730-6194     ISSN 2730-6208 (electronic) Plant in Challenging Environments ISBN 978-3-031-40172-5    ISBN 978-3-031-40173-2 (eBook) https://doi.org/10.1007/978-3-031-40173-2 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 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 Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Paper in this product is recyclable.

Preface

Similar to animals, plants have also evolved a unique set of cognitive responses to various environmental stimuli. The fact that plants do possess various animal-based neurotransmitters have lured plant physiologists to investigate their specific roles concerning growth, development, and signaling. Investigations on different aspects of melatonin in plants have undergone a prolific surge in the last decade. In view of such a considerable volume of investigations in melatonin, the proposed new volume will collate its role in different aspects of plants signaling, growth, and metabolism. Plant stress tolerance, phytoremediation, plant hardening, fruit ripening, and post-harvest management of crops have been known to be associated with the physiology of melatonin and its metabolism in plants. Nowadays, melatonin has emerged as a wonder molecule in plants that exhibits crosstalk with various other biomolecules like phytohormones, enzymes, and inorganic ions in plants. In view of the myriad roles of melatonin in higher plants, the new volume shall focus on aspects related to plant–environment interaction about biotic and abiotic stress management, growth modulation, circadian rhythm, fruit ripening, and post-harvest management of crops. The book shall provide a collation of recent advancements in genomic, transcriptomic, and metabolomic approaches to decipher the molecular mechanisms of melatonin signaling and its agronomic importance in plants. In this context, it has been important to understand its function as a stress priming molecule that executes associative synergistic relation with various other plant growth regulators (viz. nitric oxide, hydrogen sulfide, inorganic ions, and enzymes). Thus, crop management under diverse stressful environments can be better achieved by elucidating our current understanding of the role of melatonin and its interplay with various plant metabolites. Jangipur, India

S. Mukherjee

Granada, Spain

F. J. Corpas

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Contents

Part I Melatonin as an Antioxidant 1

Melatonin and the Metabolism of Reactive Oxygen Species (ROS) in Higher Plants��������������������������������������������������������������    3 Jorge Taboada, Russel J. Reiter, José M. Palma, and Francisco J. Corpas

Part II Melatonin, Biosynthesis, Plant Growth, Development and Reproduction 2

Melatonin in Plants: Biosynthesis, Occurrence and Role in plants������������������������������������������������������������������������������������   29 Atanu Bhattacharjee, Subhashis Debnath, Pranabesh Sikdar, Kunal Bhattacharya, and Nongmaithem Randhoni Chanu

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 Abiotic Stress-Induced Modulation of Melatonin Biosynthesis Accompanying Phytohormonal Crosstalk in Plants ����������������������������   45 Mrinalini Kakkar

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Role of Melatonin in Embryo, Seed Development and Germination��������������������������������������������������������������������������������������   73 Kiran Bala

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Melatonin Metabolism in Seeds: Physiological and Nutritive Aspects������������������������������������������������������������������������������   91 Anita Thakur

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 Melatonin in Plant Growth and Signaling��������������������������������������������  105 Gustavo Ravelo-Ortega, Karen M. García-Valle, Ramón Pelagio-Flores, and José López-Bucio

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Functions and Prospects of Melatonin During Pre-fertilization Reproductive Stages in Plants������������������������������������  123 Priyanka Khanduri and Sudip Kumar Roy

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Melatonin and Fruit Ripening Physiology: Crosstalk with Ethylene, Nitric Oxide, Hydrogen Peroxide and Hydrogen Sulphide��������������������������������������������������������������������������  141 Sani Sharif Usman, Atif Khurshid Wani, Abdullahi Ibrahim Uba, Tahir ul Gani Mir, Weda Makarti Mahayu, and Parnidi

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Melatonin and Postharvest Biology of Fruits and Vegetables: Augmenting the Endogenous Molecule by Exogenous Application������������������������������������������������������  155 Abdullahi Ibrahim Uba, Atif Khurshid Wani, and Sani Sharif Usman

10 Melatonin  Language in Postharvest Life of Horticultural Crops ����������������������������������������������������������������������������  173 Morteza Soleimani Aghdam Part III Melatonin and Its Signaling in Biotic and Abiotic Stress 11 Melatonin-Mediated  Regulation of Biotic Stress Responses in Plants����������������������������������������������������������������������������������  219 Swati Singh and Ravi Gupta 12 Emerging  Roles of Melatonin in Mitigating Pathogen Stress��������������  237 Hala B. Khalil, Ahmed M. Kamel, Ammar Y. Mohamed, Deyaa Hesham, Yousef Mahmoud, Roqaia Ibrahim, Nabil Salama, and Mohammed H. Elsayed 13 E  co-Physiological and Morphological Adaptive Mechanisms Induced by Melatonin and Hydrogen Sulphide Under Abiotic Stresses in Plants ������������������������������������������������������������  249 Khadiga Alharbi, Mona H. Soliman, and Abbu Zaid 14 Melatonin  in Plants Under UV Stress Conditions��������������������������������  263 Antonio Cano, Josefa Hernández-Ruiz, and Marino B. Arnao 15 Molecular  Physiology of Melatonin Induced Temperature Stress Tolerance in Plants������������������������������������������������  279 Suman Sharma and Siddhant Pandey 16 Melatonin-Mediated  Salt Stress Tolerance in Plants����������������������������  299 Tanveer Ahmad Khan, Bisma Hilal, Qazi Fariduddin, and Mohd Saleem

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17 Role  of Phytomelatonin in Promoting Ion Homeostasis During Salt Stress������������������������������������������������������������������������������������  313 Ali Mahmoud El-Badri, Maria Batool, Ibrahim A. A. Mohamed, Ramadan Agami, Ibrahim M. Elrewainy, Bo Wang, and Guangsheng Zhou 18 Positive  Regulatory Role of Melatonin in Conferring Drought Resistance to Plants������������������������������������������������������������������  343 Atif Khurshid Wani, Nahid Akhtar, Sani Sharif Usman, Abdullahi Ibrahim Uba, Farida Rahayu, Taufiq Hidayat R. Side, and Mala Murianingrum 19 Potential,  Mechanism and Molecular Insight of Melatonin in Phyto-Remediation ������������������������������������������������������  363 Umair Riaz, Laila Shahzad, Muhammad Athar Shafiq, Muhammad Kamran, Humera Aziz, Muhammad Irfan Sohail, SaifUllah, and Ghulam Murtaza

Part I

Melatonin as an Antioxidant

Chapter 1

Melatonin and the Metabolism of Reactive Oxygen Species (ROS) in Higher Plants Jorge Taboada, Russel J. Reiter, José M. Palma, and Francisco J. Corpas

Abstract  Melatonin, designated in plants as phytomelatonin, is a key biomolecule in both animal and plant cells. This is because, in addition to the detoxifying capacity melatonin has against different reactive oxygen species (ROS), it also has signaling properties that boost certain metabolic pathways and trigger both enzymatic and non-enzymatic antioxidant systems. This review aims to give a wide perspective of melatonin biosynthesis in plant cells and the relevance of this molecule to palliate certain environmental stresses, many of which have been accompanied by oxidative stress. Likewise, it evaluates the data which documents the beneficial effects of melatonin when it is applied exogenously. Keywords  Antioxidant · Abiotic stress · Phytohormone · Nitric oxide · Melatonin · Oxidative stress

1.1 Introduction Since its identification in plants in 1995 (Dubbels et al. 1995; Hattori et al. 1995), the indoleamine melatonin (N-acetyl-5-methoxytriptamine) has attracted the attention of many research groups working in highly diverse aspects of animal and plant systems. This interesting and promising biomolecule derived from tryptophan (Palego et  al. 2016), whose chemical structure is the result of serotonin

J. Taboada · J. M. Palma · F. J. Corpas (*) Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín (Spanish National Research Council, CSIC), Granada, Spain e-mail: [email protected] R. J. Reiter Department of Cell Systems and Anatomy, UT Health San Antonio, Long School of Medicine, San Antonio, TX, USA © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_1

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(5-­hydroxytryptamine) acetylation (Lerner et al. 1959a), is known in plants as phytomelatonin (Blask et al. 2004; Zhao et al. 2021). The discovery and isolation of melatonin in animals initially took place in 1958, more specifically in the pineal gland of cows (Lerner et al. 1958). A year later, it was discovered in humans (Lerner et al. 1959b). In animal systems, numerous physiological roles of melatonin have been documented, including the modulation of circadian rhythms (Vadnie and McClung 2017; Zisapel 2018; Stein et al. 2020), sleep regulation (Zisapel 2018; Stein et al. 2020), control of autophagy (Pan et al. 2018; Xiao et al. 2019), buffering the immune system (Carrillo-Vico et al. 2013) and prevention of oxidative stress (Reiter et al. 2016; Shen et al. 2018; Reiter et al. 2013; Hardeland 2013) and avoiding inflammatory response (Mannino et  al. 2019). In addition, melatonin is currently used for the treatment of jet lag (Herxheimer 2005) and its therapeutic effectiveness is being evaluated both in Alzheimer’s and Parkinson’s disease and in many types of cancer and in recent times in diabetes and SARS-COV-2 (Di Bella et al. 2013; Xie et al. 2017; Alghamdi 2018; Blume et al. 2019; Pandi-Perumal et  al. 2020; Okeke et  al. 2022; Yiang et  al. 2023; Wang et al. 2023a). Melatonin is essential for cellular redox homeostasis in animal and plant systems since it works as a scavenger of different free radicals and therefore it is considered a potent endogenous cellular antioxidant effects (Reiter et  al. 2016; Arnao et  al. 2022). Due to its amphiphilicity and the presence of transporters, melatonin easily passes through the cell membrane and distributes in the cytoplasm from where it enters the nucleus and mitochondria to exert its antioxidant capacity (Reiter et al. 1997). Melatonin defends against oxidative stress and free radicals due to its direct capacity of scavenging reactive oxygen species (ROS) and reactive nitrogen species (RNS), but also it functions as a signaling molecule to enhance the activities of antioxidant enzymes and related enzymes, such as catalase (CAT), superoxide dismutases (SOD) isozymes, ascorbate peroxidases (APX), glutathione S-transferases (GST) and pathogenesis-related proteins (PR), as well as antioxidant molecules including glutathione and ascorbate (Khan et al. 2020; Sun et al. 2020a, b; Siddiqui et al. 2020; Ahmad et al. 2020), and maintaining mitochondrial homeostasis (Zhang and Zhang 2014; Wang et al. 2018). Furthermore, the discovery of the first melatonin receptor in Arabidopsis thaliana in 2018, designated candidate G-protein-­ coupled receptor 2/phytomelatonin receptor (CAND2/PMTR1) (Wei et al. 2018), prompted many workers to identify melatonin as a plant hormone (Hardeland 2014; Ludwig-Müller and Lüthen 2015). PMTR1 has the capacity to specifically bind melatonin and interact with the G protein α subunit 1 (GPA1). GPA1 mediates the production of H2O2 and the influx of calcium ions (Ca2+), resulting in stomatal closure (Wei et al. 2018). Recently it has been questioned whether the CAND2 receptor is located in the plasma membrane or in the cytosol. Also, using mutants deficient in the CAND 2 receptor, the stimulation of mitogen-activated protein kinase (MAPK) mediated by melatonin was not suppressed (Back and Lee 2020). Thus, it is an open question whether the CAND 2 receptor is valid and, if it is, the signaling processes remain unknown. Recently, new data provide evidence that PMTR1

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mediates in the stomata closure induced by melatonin through the control of ROS and nitric oxide generation (Wang et al. 2022a, 2023b). Phytomelatonin can also act as an essential regulator in the mechanism of response to both abiotic and biotic adverse factors (Arnao and Hernández-Ruiz 2019). Regarding the defensive function of melatonin against abiotic stresses, relevant studies show that it protects against cold (Li et  al. 2019), heat (Jahan et  al. 2019), high salinity (Zhan et  al. 2019; Zhang et  al. 2022a, b; Zhu et  al. 2022), drought (Zhang et al. 2013; Li et al. 2019; Jensen et al. 2023), heavy metals (Xu et al. 2020; Ou et al. 2023; Yang et al. 2023) global warming (Back et al. 2021), and bright light (Lee and Back 2018). Moreover, studies on the beneficial role of melatonin against biotic stresses have been published (Zeng et  al. 2022; Sharif et  al. 2018; Moustafa-Farag et al. 2019; Zhao et al. 2021; Tiwari et al. 2021; Reiter et al. 2015; Yin et al. 2013; Lee et al. 2015; Hernández-Ruiz et al. 2023; Li et al. 2023); however, the mechanism of action is not yet clearly elucidated. Phytomelatonin, as in animals a product of tryptophan metabolism, acts coordinately with other phytohormones and plays a pivotal role in regulating plant growth and development (Liu et al. 2022), being involved in different physiological processes such as promoting germination, seedling growth, root development, product yield, stomatal movements, circadian rhythm regulation, deferring leaf senescence, flowering and regulating fruit ripening (Corpas et al. 2021; Lee et al. 2022; Wang et al. 2018; Erdal 2019; Arnao and Hernández-Ruiz 2020; Hong et al. 2018; Arnao and Hernández-Ruiz 2021; Abbas et al. 2021). This chapter provides an overview of the interaction of ROS with melatonin in various physiological processes, e.g., photosynthesis, stomatal aperture, etc., protection against abiotic and biotic adverse conditions, as well as the role of the variou Zhang s phytomelatonin-derived hydroxy metabolites present in plants and their possible future application to the industry for developments in horticulture, agriculture and to obtain greater agro-economic benefits.

1.2 Biosynthesis of Melatonin The animal pathway of the biosynthesis of melatonin has been widely studied and described (Axelrod and Weissbach 1960; Champney et  al. 1984), but with some unexpected variations (Tan et  al. 2016; Mannino et  al. 2021; Tan and Hardeland 2021). In higher plants as revealed using biochemical, molecular biology, and genetic approaches it has been shown that the melatonin biosynthetic pathway is more complex than that in animals since it contains diverse routes and reversible processes that have not been well described in many plant species (Tan and Reiter 2020). Melatonin biosynthesis starts with tryptophan (Trp), an aromatic amino acid produced through the chloroplastic shikimate pathway (Schmid and Amrhein 1995); it is generally agreed upon that the synthesis of melatonin involves four main steps catalyzed by at least six enzymes (Sun et  al. 2021). Figure  1.1 shows a simple

Fig. 1.1  Biosynthesis of melatonin in and formation of hydroxymelatonins. The main enzymes involved in the biosynthesis of melatonin are tryptophan decarboxylase (TDC), tryptamine 5-hydroxylase. (T5H), serotonin N-acetyltransferase (SNAT), N-acetylserotonin methyltransferase (ASMT), N-acetylserotonin deacetylase (ASDAC), caffeic acid O-methyltransferase (COMT). Conversely, the enzyme melatonin 2-hydroxylase (M2H) and melatonin 3-hydroxylase (M3H) mediated the formation of (Lee et al. 2016) of 2-hydroxymelatonin (2-OHM), cyclic 3-hydroxymelatonin (3-OHM), respectively. The 2-OHM can be found in its tautomeric form, 2-acetamidoethyl-5-methoxyindolin-2-one (AMIO). Additionally, indoleamine 2,3-dioxygenase (IDO) catalyzes the formation of N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) which can be oxidized to N-acetyl-5-methoxykynuramine (AMK)

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scheme of the biosynthesis route of melatonin and some of the compounds derived from its oxidation. Tryptophan decarboxylase (TDC) catalyzes the first stage which involves the conversion of tryptophan to tryptamine (Noé et al. 1984; Mérillon et al. 1986; Byeon et al. 2014a; Pang et al. 2018; Lee and Back 2019b; Taboada et al. 2023). In the next stage, tryptamine is converted to 5-hydroxytryptamine (serotonin) by tryptamine 5-hydroxylase (T5H), a cytochrome P450 enzyme found in the endoplasmic reticulum (Fujiwara et  al. 2010; Park et  al. 2013). The third stage involves the serotonin N-acetyltransferase (SNAT) that converts serotonin to N-acetylserotonin (NAS) in chloroplasts and mitochondria. Now, three SNAT genes that have a low sequence homology have been recognized in higher plants, SNAT1, SNAT2, and SNAT3 (Kang et al. 2013; Byeon et al. 2016; Wang et al. 2017). The last stage is the conversion of NAS to melatonin by the enzyme N-acetylserotonin methyltransferase (ASMT) (Kang et al. 2011). In several plant species that lack ASMT homologs, the NAS is converted to melatonin by the action of caffeic acid O-methyltransferase (COMT) (Byeon et  al. 2014b, 2015a; Lee et  al. 2014). Furthermore, it has been reported a reverse pathway which involved the named enzyme N-acetylserotonin deacetylase (ASDAC), which catalyzes the conversion of NAS to serotonin; it is present in the chloroplast as is SNAT (Lee et al. 2018) and its overexpression leads to a lower endogenous melatonin content than that in the wild type (Back et al. 2020). In general, melatonin content in healthy plant tissues/ organs range from picograms to nanograms per gram of fresh weight (Back 2021) but it could rise by several hundred-fold when plants are under diverse types of stresses (Lee et al. 2017). Table 1.1 displays representative examples of the variability in melatonin content in diverse plant species and organs including fruits (climacteric and non-­climacteric), leaves, stems, and different types of edible roots and seeds. This content can range from 10 to 5,300 pmol melatonin g−1 fresh weight (FW). Although the values of melatonin are expressed in fresh weight, it should be noted that the data expressed by dry weight are more reliable since the water content of plant tissue varies widely and depends on many factors such as plant variety, organs (roots, stems, leaves or fruits), climatic conditions, the amount of water available in soils, ripening stage of the fruits, etc. (Riga et al. 2014).

1.3 Reactive Oxygen Species (ROS) and Reactive Nitrogen Species (RNS) Aerobic life is inevitably associated with the generation of both ROS and RNS (del Río 2015; Kohli et al. 2019). Table 1.2 includes some of the main ROS and RNS. In addition, some of these molecules such as H2O2, NO, nitrosoglutathione (GSNO), or nitro-fatty acids (NO2-FAs) have recognized signaling functions in plants in a wide variety of processes involving primary metabolism, growth, and development, response to biotic and abiotic stress, solute transport, autophagy, and programmed

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Table 1.1 Melatonin concentration in different plant species and in the different organs, determined by radioimmunoassay. (Data extracted from Hattori et al. 1995). FW, fresh weight Plant species Climacteric fruits  Kiwi (Actinidia chinensis)  Tomato (Solanum lycopersicum)  Apple (Malus domestica) Non- climacteric fruits  Strawberry (Fragaria magna)  Cucumber (Cucumis sativus)  Pineapple (Ananas comosus)  Red chili pepper (Capsicum annuum) Leaves  Indian spinach (Basella alba)  Cabbage (Brassica oleracea)  Chungiku (Chrysanthemum coronarium)  Japanese ashitaba (Angelica keiskei)  Tall fescue (Festuca arundinacea) Stem  Asparagus (Asparagus officinalis)  Welsh onion (Allium fistulosum) Root  Onion (Allium cepa) bulb  Carrot (Daucus carota) bulb  Ginger (Zingiber officinale) rhizome  Japanese radish (Brassica campestris) Seed  Barley (Hordeum vulgare)  Sweet corn (Zea mays L.)  Rice (Oryza sativa)  Oat (Avena sativa)

Melatonin content (pg g−1 FW) 24.4 32.2 47.6 12.4 24.6 36.2 1190–4480a 38.7 107.4 416.8 623.9 5288.1 9.5 85.7 31.5 55.3 583.7 657.2 378.1 1366.1 1006.0 1796.1

Data obtained from Riga et al. 2014

a

cell death (Corpas et al. 2013; Mata-Pérez et al. 2016, 2017; Turkan 2018; Foyer and Hanke 2022). Moreover, ROS and RNS are also involved in post-translational modification (PTMs) of proteins including S-sulfenylation, nitration, S-nitrosation, nitroalkylation or methylation of histones (Niu et  al. 2015; Mengel et  al. 2017; Aranda-Caño et al. 2019; Corpas et al. 2020a, 2022a). ROS are primarily produced by two chemical routes. The primary way is the electron transfer (between one to three electrons) to oxygen, involving in the production of superoxide anion (O2•−), hydrogen peroxide (H2O2), or hydroxyl radical (•OH). The second of these processes is the transfer of energy to molecular oxygen (O2), leading to the formation of singlet oxygen (1O2) (Halliwell and Gutteridge

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Table 1.2  Main reactive oxygen and nitrogen species (ROS and RNS, respectively) containing inorganic and organic molecules Nonradicals Inorganic molecules  Hydrogen peroxide (H2O2)  Singlet oxygen (1O2)  Nitroxyl anion (NO−) Nitrosonium cation (NO+)  Nitrous acid (HNO2)  Dinitrogen trioxide (N2O3)  Dinitrogen tetroxide (N2O4)  Peroxynitrite (ONOO−)  Peroxynitrous acid (ONOOH) Organic molecules  Nitrotyrosine (Tyr-NO2)  Nitrosoglutathione (GSNO)  Nitrosothiols (SNOs)  Nitro-γ-tocopherol    Nitro-fatty acid (NO2-FA)

Radicals Superoxide anion (O2•−) Hydroxyl radical (•OH) Hydroperoxyl radical (•OOH) Nitric oxide (•NO) Nitrogen dioxide (•NO2)

Lipid peroxyl radicals (LOO•)

1999; Sánchez-Corrionero et  al. 2017; Arnao and Hernández-Ruiz 2019; Lemke et al. 2021). Plant cells generate also reactive nitrogen species (RNS), but unlike ROS, for RNS the production mechanism is not fully resolved. Among the RNS, nitric oxide (•NO), nitrogen dioxide (•NO2), and non-radical species peroxynitrite (ONOO−) and S-nitrosoglutathione (GSNO) are included (Halliwell and Gutteridge 1999; Kohli et al., 2019; Arnao and Hernández-Ruiz 2019). In higher plant cells, the central ROS sources are the electron transport chain present in chloroplasts and mitochondria (Kohli et al. 2019), but there are different enzymes present in the subcellular compartments which can generate ROS such as some metabolic pathways present in peroxisomes such as β-oxidation, photorespiration, purine metabolism, polyamine catabolism or sulfite detoxification pathway (Corpas et  al. 2020a, b), the plasma membrane NADPH oxidase (NOX) is also known as a respiratory burst oxidase homolog (Rboh) (Torres and Dangl 2005; Liu et al. 2020) as well as the family of antioxidant superoxide dismutases (SODs) (del Río et al. 2018). Additionally, other subcellular places of ROS generation are cytosol, plasma membrane, and cell wall (Corpas et al. 2015; Podgórska et al. 2017; Kámán-Tóth et al. 2019). Although the primary enzymatic source of NO in plant cells is still an open question, there are two main candidates an L-arginine-dependent NO synthase-like activity and nitrate reductase (Mohn et  al. 2019; Corpas et  al. 2022a, b). In general, pathogen infections raise the endogenous content of H2O2 and NO, and these reactive species act upstream of melatonin and promote its synthesis (Shi et  al. 2015; Lee and Back 2017), although the mechanism of how this is achieved remains unknown.

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1.4 Interactions Between Phytomelatonin and ROS As previously mentioned, phytomelatonin is a powerful antioxidant, which, due to its lipophilic nature, is capable of crossing biological membranes to act in the different cellular compartments (Reiter et al. 2001b; Sofic et al. 2005; Tan et al. 2007; Galano et al. 2013; Zhang and Zhang 2014). Melatonin can directly scavenge •OH, H2O2, 1O2, NO, ONOO−, and other free radicals (Reiter et al. 2001a; Reiter and Tan 2002; Galano and Reiter 2018). Thus, one molecule of melatonin has the capacity to scavenge two •OH molecules and four H2O2 molecules (Pieri et al. 1995; Reiter et al. 2000; Allegra et al. 2003). In animal systems, it is well-documented that melatonin is converted to 6-­hydroxymelatonin (6-OHM) by P450 enzymes and further conjugated by sulfation into 6-sulfatoxymelatonin (Ma et  al. 2005; Hardeland 2017). Also, while some hydroxymetabolites such as N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) are generated from melatonin by the achievement of several enzymes such as indoleamine 2,3-dioxygenase (IDO) (Hirata et al. 1974; Tan et al. 2001) and cytochrome c (Semak et  al. 2005), other derivative metabolites of melatonin such as N-acetyl-5-methoxykinuramine (AMK), AFMK, 2-hydroxymelatonin (2-OHM), cyclic 3-hydroxymelatonin (3-OHM) and 4-hydroxymelatonin (4-OHM) are generated non-enzymatically by interaction with different oxidants, including ROS and RNS (Hardeland 2017) with all of them exhibiting high antioxidant activity (Reiter et al. 2016) (Fig. 1.1). Melatonin seems not to be an end product in plant cells, however, and the phytomelatonin-­derived hydroxymetabolites are not simple oxidation products of reactions between melatonin and ROS as observed in animals (Mannino et al. 2021). In plant cells, these compounds constitute the main forms of phytomelatonin in terms of endogenous levels (Lee et al. 2016) highlighting the 3-OHM and 2-OHM catalyzed by the enzymatic reactions of melatonin 3-hydroxylase (M3H) (Lee et al. 2016) and melatonin 2-hydroxylase (M2H) (Byeon and Back 2015), respectively. Both M2H and M3H belong to the 2-oxoglutarate-dependent dioxygenase (2-ODD) family proteins (Bugg 2003; Kawai et al. 2014) that are only present in land plants (Lee and Back 2019a) (Fig. 1.1). In healthy leaves of rice, concentrations of 600 ng · g−1 fresh weight (FW) of serotonin, 0.3  ng ·  g−1 FW of melatonin, 100  ng · g−1 FW of 3-OHM and 40 ng · g−1 FW of 2-OHM have been obtained. However, higher levels of these hydroxymetabolites derived from phytomelatonin and serotonin are measured are in higher concentrations than phytomelatonin itself under cadmium stress and senescence (Lee et al. 2017; Choi and Back 2019a, 2019b). According to the example in rice, and taking into account that the catalytic efficiency of the M3H enzyme is 35 times higher than the M2H enzyme, 3-OHM is the most abundant hydroxymetabolite in plants, followed by 2-OHM and then AFMK and AMK (Byeon and Back 2015; Lee et al. 2016). Nevertheless, in plant species such as coffee (Coffea arabica), ginkgo (Ginkgo biloba), spinach (Spinacia

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oleracea) and feverfew (Tanacetum parthenium), 2-OHM concentrations 368 times higher than phytomelatonin have been found, once again indicating its role as a precursor of these hydroxymetabolites (Byeon et al. 2015b).

1.4.1 The Function of 2-hydroymelatonin (2-OHM) As mentioned, 2-hydroxy melatonin is the product of the M2H enzyme and because it has a higher catalytic efficiency than SNAT and COMT enzymes (Back 2021), concentrations of 2-OHM are up to 100 times higher than phytomelatonin (Byeon et al. 2015b). Several plant studies show that 2-OHM participes in the induction of defense genes (Byeon et al. 2015c), tolerance against abiotic stress (Lee and Back 2019a), and cadmium (Shah et al. 2020). In addition, other studies document that 2-OHM can act as a senescence-inducing factor in Arabidopsis thaliana since it has pro-oxidative properties, capable of inducing the ROS production in a respiratory burst NADPH oxidase (RBOH)-dependent manner in senescent leaves (Lee and Back 2021a) and seeds (Lee and Back 2022a). In a recent study, the effects of 2-OHM and phytomelatonin on seed germination concerning ROS production were compared in Arabidopsis thaliana (Lee and Back 2022a). Thus, it was observed that the seed pretreatment with 20 μM melatonin increased, by around 13%, the germination in both dormant and non-dormant seeds, while the treatment with 20  μM 2-OHM increased the germination rate by 80% and 40% in non-dormant and dormant seeds, respectively. Furthermore, this concentration of 2-OHM enhanced the expression of acid gibberellic (GA) biosynthetic genes such as 3-oxidase 2 (GA3ox2) and ent-kaurene synthase (KS) compared with the control. Furthermore, when a GA synthesis inhibitor (paclobutrazol) was applied, the germination was fully abolished, indicating that both GA and 2-OHM are clearly associated with the seed germination. Likewise, genetic approaches using knock-out mutant or overexpression of M2H in embryo tissues during seed germination demonstrate that 2-OHM mediates ROS production in the germination of seeds (Lee and Back 2022a). Similarly, 2-OHM acts rather as a signaling molecule capable of inducing ROS production both in leaf senescence and seed germination. Therefore, the balance between melatonin and 2-OHM is capable of regulating various physiological processes such as seed germination, senescence, and embryogenesis. It should be noted that 2-OHM is in equilibrium with its tautomeric form, 2-acetamidoethyl-5-­ methoxyindolin-2-one (AMIO) (Hardeland 2017, 2019), which in turn has a low antioxidant capacity (Pérez-González et al. 2017), making it difficult to eliminate, and although its exact distribution in plant cells is not known. AMIO is located in lipid droplets or compartments with many membranes such as chloroplasts or mitochondria. It is involved in the activation of MAP kinases against pathogens (Lee and Back 2016a) and protects against abiotic stresses such as low temperatures and drought (Lee and Back 2016b). Therefore, it is in turn an active biomolecule that complements the physiological effects of phytomelatonin.

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1.4.2 Cyclic 3-hydroymelatonin (3-OHM) 3-OHM is a hydroxy metabolite derived from phytomelatonin resulting from the action of M3H activity; it exhibits an antioxidant effect dealing with •OH and hydroperoxyl radical (•OOH) (Tan et  al. 2014; Galano et  al. 2014). This cytoplasmic enzyme shares only a 2-ODD domain with M2H, but it shows a low M2H activity in rice. Owing to the catalytic efficiency of M3H being even higher than M2H, and the endogenous levels of 3-OHM are higher than 2-OHM; thus, phytomelatonin is rapidly transformed into 3-OHM (Lee et al. 2016). In addition, the 3-OHM levels are maximum at night and when overexpressed M3H mutants, the secondary tiller number is increased in rice (Choi and Back 2019a), whereas in Arabidopsis thaliana, M3H knockout (m3h) exhibited less growth and antioxidant activity resulting in a delayed flowering phenotype, due to the suppression of Flowering Locus T gene (FT), indicating that this hydroxymetabolite promotes plant growth and reproduction Furthermore, m3h plants had lower total biomass per plant and are smaller than the wild-type, owing to a lower expression of GA genes, such as KS, GA3ox1, and GA3ox2. Also, since no differences were found in the length of the root in response to saline stress (100 mM NaCl for 3 weeks) or the pathogen (Pseudomonas syringae pv. Tomato DC3000) compared to wild-type, it was concluded that 3-OHM is not involved in the response to infections by pathogens or saline stress (Lee and Back 2022b)

1.5 Phytomelatonin and Antioxidant System Under Physiological and Stress Conditions The exogenous application of melatonin has commonly been used at the experimental level due to its priming effects, protecting the plants against different types of environmental stresses, both of biotic and abiotic origin (Debnath et al. 2018, 2019; Dai et al. 2020; Mohamadi Esboei et al. 2022; Xie et al. 2022a, b. One of the most widespread aspects is that many types of stress lead to a marked increase in the generation of ROS, which usually triggers oxidative damage at the level of membranes as well as certain cellular components (nucleic acid, proteins, and lipids), affecting their functionality (Siddiqui et al. 2020; Ren et al. 2022). Table 1.3 contains some examples in which it is shown how melatonin applied in different ways and diverse plant species causes an increase in the main antioxidant systems, which makes it possible to control the exacerbated production of ROS and, therefore, alleviate its associated damage. Among the most studied are the enzymatic antioxidants including the peroxisomal catalase (CAT), the different superoxide dismutase (SOD) isozymes, components of the ascorbate-glutathione pathway including ascorbate peroxidase (APX), monodehydroascorbate peroxidase (MDAR), dehydroascorbate reductase (DHAR) and glutathione reductase (GR) as well as non-­ enzymatic antioxidant including ascorbate and glutathione (GSH) and the peroxidase

0.050

0.05 and 0.1 0.015

0.02 and 0.1 0.05 and 0.5 0.1

1.0

1.0

0.2

0.1

mM MT 0.1

Main effects of ROS meatbolism Increases of SOD and APX activities. Accumulation of ascorbate. Reduces the content of O2•− and H2O2. Delays postharvest senescence. Increases the activity of SOD, CAT, APX, and GR activity. Decreases the content of O2•−, H2O2 and MDA. Reduces the electrolyte leakage and increases the membrane integrity. Immersion Decreases H2O2 and MDA contents in the exocarp of the fruit, delaying the for 30 min ripening process Immersion Improves antioxidant system in the fruits such as catalase, SOD, APX, AsA, for 30 min polyphenols, flavonoids, and anthocyanins during cold storage and reduces qualitative decay Spray Increases the activity of catalase, SOD, and peroxidase. Reduces ethylene production Keeps apple quality during postharvest storage. Irrigated for Significant improve of cold, drought and salt stress tolerance exhibiting 7 days higher chlorophyll content and survival rate, and lower electrolyte leakage Immersion Improves seed germination and viability against cold stress enhancing SOD for 5 days and GR activity and show a lower H2O2 content Spray Improves resistance against Fusarium oxysporum fungi disease decreasing H2O2 and MDA content and electrolyte leakage Immersion Alleviates the growth inhibition of wheat seedlings under cadmium stress for 7 days (0.2 mM cadmium) Added to the Seed pre-treatment with melatonin protects cotton seedlings from cadmium-­ nutrient induced oxidative injury by increasing the activities of CAT, SOD, APX and solution POD. Added to the Under salt, drought, and heat stresses, melatonin treatment triggers the nutrient enrichment of flavonoids and mediates the reprogramming of biosynthetic solution pathway genes

Method of application Immersion for 10 min Immersion for 5 min

Song et al. (2022)

Khan et al. (2022b)

Ahammed et al. (2020) Ni et al. (2018)

Marta et al. (2015)

Shi et al. (2015)

Onik et al. (2021)

Magri and Petriccione (2022)

Dong et al. (2021)

Wang et al. (2019)

References Gao et al. (2016)

APX ascorbate peroxidase, AsA ascorbate, CAT catalase, GR glutathione reductase, GSH reduced glutathione, MDA malondialdhyde, POD peroxidase, SOD superoxide dismutase

Pigeon pea (Cajanus cajan)

Apple (Malus domestica L. Borkh) Bermudagrass (Cynodon dactylon L. Pers) Cucumber (Cucumis sativus L.) Cucumber (Cucumis sativus L. ‘Jinyou 28’) Wheat (Triticum aestivum) Cotton (Gossypium hirsutum L.)

Mango (Mangifera indica L.) Blueberry (Vaccinium corymbosum L.)

Plant species Peach (Prunus persica L.) Sweet cherry (Prunus avium L.)

Table 1.3  Main effects of exogenous application of melatonin in different plant species

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(POD) family (Mohamadi Esboei et al. 2022). Likewise, melatonin applies exogenously also triggers the biosynthesis of secondary metabolites which possess antioxidant capacities such as phenolic or terpene derivatives, for example, flavonoids, isoflavones, or carotenoids (Sun et al. 2020a, b; Jafari and Shahsavar 2021; Yin et al. 2022a, b; Corpas et al. 2023). The cascade of signals which mediate how melatonin triggers these antioxidant systems including its own biosynthesis is still poorly understood (Khan et al. 2022a). At present, there is a battery of interactions among melatonin and other cellular components which seem to participate including calcium (Siddiqui et al. 2020; Tian et al. 2022), mitogen-activated protein kinase (MAPK) cascades (Lee and Back 2021b; Ma et al. 2022; Maity et al. 2022; Xie et al. 2022b), nitric oxide (Zhao et al. 2018; Feng et al. 2021; Imran et al. 2022; Yin et al. 2022a, b), hydrogen sulfide (Kaya et al. 2022; Wang et al. 2022a), phytohormones such as abscisic acid (Guo et al. 2022), indole3-acetic acid (Zhang et al. 2022a, b), gibberellins (Arabia et al. 2022) or jasmonic acid (Ding et al. 2022; Wang et al. 2022a, b) as well as transcription factors. For example, melatonin treatment of pigeon pea triggers an increase in the expression of flavonoid 3’ hydroxylase (F3´H) family which encodes for enzymes involved in the biosynthesis of luteolin; this may to be a result of the transcription factor Phytoclock1 (PCL1) directly being bonded to the F3´H-5 promoter to enhance its expression that finally promotes an increase resistant to different stresses (Song et al. 2022).

1.6 Concluding Remarks At present, melatonin is recognized as a master molecule in animal and plant systems because in addition to its highly diverse antioxidant properties (Manchester et  al. 2015; Reiter et al. 2016), it has signaling capacities to stimulate a variety of metabolic pathways (Back 2021). Among them, the main enzymatic and non-­enzymatic antioxidant systems are highly implicated since they respond to melatonin allowing it to exert its beneficial effects to palliate the oxidative stress associated with different types of environmental stress. Therefore, melatonin initiates the cascade of signals and exerts its beneficial effects to counteract potential oxidative damage. Melatonin exhibits coordinated activities with a battery of other signaling molecules including calcium, MAP kinase, phytohormones, nitric oxide, or hydrogen sulfide. Figure 1.2 shows a working model where the main effects triggered by melatonin are summarized particularly where they relate to antioxidant systems; these systems have high relevance to the regulation of diverse physiological processes as well as to the mechanism of response to environmental stresses where oxidative metabolism usually is a significant feature. One aspect of melatonin that has attracted the attention of many plant researchers is its biotechnological potential, since the exogenous application of melatonin makes it possible to alleviate oxidative damage in the face of numerous types of stresses, but also due to its application in the horticultural industry since it is involved in maintaining the quality of horticultural products throughout their postharvest storage (Aghdam et al. 2023; Corpas et al. 2022a, b).

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Fig. 1.2  Model of actions of melatonin (phytomelatonin) in higher plants under physiological and stress conditions where the antioxidant systems play a key function. The mechanism of melatonin modulation of the different antioxidant systems seems to be mediated by different signaling molecules including calcium (Ca2+), nitric oxide (NO), hydrogen sulfide (H2S), mitogen-activated protein (MAP) kinase, and phytohormones such as abscisic acid (ABA), indole-3-acetic acid (IAA), gibberellins (GAs) or jasmonic acid (JA)

Acknowledgements  Our research work is supported by a European Regional Development Fund-cofinanced grant from the Ministry of Economy and Competitiveness/Science and Innovation (PID2019-10103924GB-I00), the Plan Andaluz de Investigación, Desarrollo e Innovación (PAIDI 2020) (P18-FR-1359) and Junta de Andalucía (group BIO192), Spain.

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Part II

Melatonin, Biosynthesis, Plant Growth, Development and Reproduction

Chapter 2

Melatonin in Plants: Biosynthesis, Occurrence and Role in plants Atanu Bhattacharjee, Subhashis Debnath, Pranabesh Sikdar, Kunal Bhattacharya, and Nongmaithem Randhoni Chanu

Abstract  Melatonin (N-acetyl-5-methoxytryptamine) is a pineal gland hormone, relatively little research has been done on it in this area up until 1995. It can be found in several plant species in different concentrations. Melatonin has even been proposed as nature’s most adaptable biological signal molecule due to its widespread distribution throughout all kingdoms. Since Hattori first discovered melatonin in plants, Numerous studies have been released, expanding the field of phytomelatonin i.e. melatonin generated from plants. Plants biosynthesize phytomelatonin from the precursor tryptophan. Because of their powerful antioxidant properties, the majority of herbs with high melatonin content have been utilised for centuries to treat neurological problems linked to the production of free radicals. This brief summary aims to give a general understanding of phytomelatonin, including information on its distribution, biosynthesis, potential roles in the regulation and growth, and abiotic stress management of plants. Keywords  Phytomelatonin · Tryptophan · Medicinal plants · Abiotic stress · Antioxidant

A. Bhattacharjee (*) · P. Sikdar Royal School of Pharmacy, The Assam Royal Global University, Guwahati, Assam, India S. Debnath Royal School of Pharmacy, The Assam Royal Global University, Guwahati, Assam, India Bharat Pharmaceutical Technology, Agartala, Tripura, India K. Bhattacharya Royal School of Pharmacy, The Assam Royal Global University, Guwahati, Assam, India Pratiksha Institute of Pharmaceutical Sciences, Guwahati, India N. R. Chanu Pratiksha Institute of Pharmaceutical Sciences, Guwahati, India Faculty of Pharmaceutical Science, Assam Downtown University, Guwahati, Assam, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_2

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2.1 Introduction Melatonin has a long history and is a well-known companion in animal and human physiology, but it is new to plant physiology (Reiter et al. 2011). In 1958, Lerner and colleagues isolated melatonin for the first time from the pineal gland of cattle (Lerner et al. 1958) Melatonin was given that name because it can make the skin of several fish amphibians, and reptiles (Chava and Sirisha 2012). Melatonin is essential for controlling the circadian rhythm in mammals (Sahna et al. 2005). This powerful antioxidant boosts the gene expression of antioxidant enzymes while also protecting mitochondrial homeostasis. (Nitulescu et al. 2009; Carrillo et al. 2013; Fatma et al. 2013; Bhavini et al. 2009). Consequently, it is very helpful in treating neurological diseases like Alzheimer’s, etc. whose pathophysiology is linked to the cytotoxic effects of reactive oxygen species (Russel et al. 2010; Ayushi and Maheep 2007; Hardeland 2005; Jian and Ze 2006; Venkatramanujam 2011). For the first time, melatonin was independently discovered in plants by Dubbels et  al. 1995; Hattori et al. 1995 (Dubbels et al. 1995; Hattori et al. 1995). Since then, research into phytomelatonin generated from plants has become one of the fastest-growing fields in plant physiology. Numerous scientific studies support the presence of melatonin is present in many plant species (Rudiger and Burkhard 2003). Melatonin is regarded as one of nature’s most adaptable biological signals due to its widespread dispersion and multidirectional activity. According to the current study, plants both produce and absorb this conventional indole derivative (Marino and Josefa 2006). The results of the experiments provide the clearest evidence for phytomelatonin’s functions as an antioxidant, free radical scavenger, and growth promoter (Russel et al. 2014). According to studies, excessive UV radiation increases the formation of indole compounds, which is strong evidence for phytomelatonin’s activity as an antioxidant that protects plants from strain related to oxidation and lessens macromolecule damage in a way that is comparable to that of animals (Katerova et al. 2012). It is essential for controlling plant reproductive physiology and protecting plant cells from apoptosis brought on by unfavorable environmental factors. Phytomelatonin has been identified to have a variety of physiological roles, including a probable role in blooming, regulating circadian rhythms and photoperiodicity, and serving as a growth regulator. Melatonin content varies by plant organ or tissue, with leaves and fragrant plants having higher levels than seeds (Dun 2015). It has auxin-like activity and regulates root, shoot, and explant growth. It also promotes seed germination and rhizogenesis, slows the start of induced leaf senescence, and regulates explant growth (Krystyna and Małgorzata 2013). Recently, a potential function in lupin rhizogenesis has also been suggested (Katarzyna et al. 2014). Melatonin production in plants is well established and relatively little is known about its existence in organisms other than angiosperms. This is mostly owing to insufficient detection techniques and a lack of experimental protocols to look into

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phytomelatonin’s molecular and biochemical properties. To get quick, accurate results on phytomelatonin content, however, certain methodological protocols had been designed successfully. Tryptophan was discovered to be a common precursor for serotonin, melatonin, and indole-3-acetic acid (IAA) in investigations using radioisotope tracer techniques (Hernandez et al. 2004; Marino 2014; Russel et al. 2007). The whole biosynthetic pathways of phytomelatonin synthesis are yet to be explored vividly. According to certain accounts, plants may be able to absorb melatonin from the soil in which they are grown. According to the research, melatonin is also involved in the maintenance of chlorophyll and the promotion of photosynthesis (Van Tassel et  al. 1995; Kolar and Machackova 2005). High-melatonin transgenic plants may significantly contribute to raising food yields and enhancing human health in general (Amit and Vinod 2014). This article’s goals include deepening our comprehension of the various physiological functions of phytomelatonin as well as discussing intriguing data about the substance.

2.2 Biosynthesis of phytomelatonin The precursor tryptophan has a phylogenetic widespread distribution and is the source of melatonin. It was long believed that only vertebrates’ pineal glands could produce this neuro-hormone (Ebels and Tommel 1972). Later, a new area of study on this substance was created when melatonin was discovered in photosynthesizing organisms. Animals cannot synthesis the necessary amino acid tryptophan, hence they must get it from other natural sources since it cannot be produced by them (Marino and Hernandez 2007). In addition to the hormone auxin, phytoalexins, glucosinolates, alkaloids, and indoleamines, tryptophan also serves as a precursor for phytomelatonin (Bandurski et al. 1995). In angiosperms, the rate of melatonin production varies rhythmically, peaking at night and seasonally during the flowering period (Katri et al. 2012). Chorismate and anthranilate are used in the shikimic acid pathway to biosynthesize tryptophan. The conversion of tryptophan to 5-­ hydroxytryptophan to serotonin is regulated by tryptophan hydroxylase. Arylalkylamine N-acetyl Transferase (AANAT) converts serotonin into N-acetyl serotonin, from which hydroxyindole-O-methyltransferase (HIOMT) produces melatonin. It should be emphasized that AANAT is yet to be identified, although plants can still produce melatonin on their own. As a result, the genetic features of the serotonin N-acetylating enzyme in plants may differ from those of animal AANAT.  Tryptophan decarboxylase is the only enzyme in plants that makes indole-­3-acetic acid (IAA) from tryptophan (Yeo et  al. 2007; Bruno et  al. 2005; Marcello et al. 2006) (Fig. 2.1).

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O-

O

O-

O

OH

P

O

O

HO

O

CH2

OH

HO

HO

OH

C00-

OH

OH

SHIKIMATE

ERYTHROSE-4-PHOSPHATE

CHORISMATE O

H N

H 2N

Tryptophan decar boxvlase

H 2N

OH

-O

NH2 N H TRYPTOPHAN

TRYPTAMINE

O ANTHRANILATE

Tryptophanhydroxylse

HO

HO

NH2

CHO

N H

HN

NH3 N H

5-HYDROXYTRYPTOPHAN

INDOLE-3-ACETALDEHYDE

SERATONIN

Serotonin Nacetylating enzyme O

HO OH

N H

INDOLE-3-ACETIC ACID (LAA) In plant

H3C O

HIOMT HN HN

CH3

HN O

MELATONIN

CH3

HN O

N-ACETYL SEROTONIN

Fig. 2.1  The biosynthetic pathway of melatonin

2.3 Melatonin in Edible Plants Humans have discovered the presence of melatonin in more than 140 distinct fragrant, medicinal, and food plants (Jan and Ivana 2005). To find melatonin in plant tissues, several advanced analytical methods were created. The most trustworthy sources among these include radioimmuno assays (RIA), enzyme-linked immunoadsorbent assays (ELISA), high-performance liquid chromatography (HPLC), and gas chromatography-mass spectrophotometry (GC-MS) (John et  al. 2011; Kolar

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2003; Marcello et  al. 2012). According to reports, cereals from the family of Graminae, such as rice, barley, sweet corn, and oats, contain significant amounts of melatonin (Dun et al. 2007). Melatonin was found in bananas in a concentration of 0.655 ng/g, according to GC-MS analysis, but HPLC-MS suggested higher melatonin content (1 ng/g of plant tissue) (Badria 2002). In many fruits like berries, kiwis, etc., melatonin contents were reported. Both white and black mustard seeds contained melatonin (189 ng/g of plant tissue and 123 ng/g of plant tissue, respectively through RIA analysis) (Burkhardt et al. 2001; Manchester et al. 2000). Both green and roasted beans contained melatonin, with concentrations of 5.8 g/g dry weight and 8.0 g/g dry weight, respectively (Akula et al. 2012) (Table 2.1). Table 2.1  Phytomelatonin occurrence Common name Kiwi fruit Beet root Taro Asparagus Feverfew Barren wort Indian spinach white radish Pineapple Cucumber fruit Alfalfa seed Saint John’s wort

Walnut Poppy seed Burmese grape

Taxonomy Actinidia deliciosa Liang-Ferg (Actinidiaceae) Beta vulgaris L. (Amaranthaceae) Colocasia esculenta L. (Araceae) Asparagus officinalis L. (Asparagaceae) Tanacetum parthenium L. (Asteraceae) Epimedium brevicornum M. (Berberidaceae) Basella alba L. (Basellaceae) Raphanus sativus L. (Brassicaceae) Ananas comosus L. (Bromeliaceae) Cucumis sativus L. (Cucurbitaceae) Medicago sativa L. (Fabaceae) Hypericum perforatum L. (Hypericaceae) Juglans regia L. (Juglandaceae) Papaver somniferum L. (Papaveraceae) Baccaurea ramiflora (Phyllanthaceae)

Detection method ELISA

Amount (pg/g) 24.4

ELISA

2

ELISA

54.6

ELISA

9.5

HPLC-UV ELISA

1300– 7000 ng/g 1105 ng/g

ELISA

38.7

ELISA

657.2

ELISA

36.2

HPLC

24.6

HPLC-UV

16,000

Leaf Flower ELISA

1750 ng/g 2400– 4000 ng/g 3500

RIA

6000

ELISA HPLC-UV

76.7 43.2

Reference Hattori et al. (1995) Dubbels et al. (1995) Hattori et al. (1995) Hattori et al. (1995) Pandi et al. (2006) Hardeland et al. (2011) Hattori et al. (1995) Hattori et al. (1995) Hattori et al. (1995) Hattori et al. (1995) Manchester et al. (2000) Tan et al. (2007)

Kolar (2003) Manchester et al. (2000) Hardeland (1997) (continued)

A. Bhattacharjee et al.

34 Table 2.1 (continued) Common name Rice seed

Taxonomy Oryza sativa L. (Poaceae)

Welsh onion

Allium fistulosum L. (Liliaceae) Punica granatum L. (Lythraceae) Morus alba M. (Moraceae)

Pomegranate White mulberry Banana Olive oil Chinese rhubarb Chinese goldthread Almond seed Gambir Vine Amur cork tree Silver leaf nightshade fruit Devil’s trumpet flower Anise seed Coriander seed Fennel seed Sunflower seed Grapevine Cardamom seed Curcuma

Detection method ELISA

Amount (pg/g) 1006

RIA

85.7

HPLC-MS

540–5500

0.46

Reference Hattori et al. (1995) Hattori et al. (1995) Hardeland et al. (2011) Sergio et al. (2009) Marino (2014)

ELISA

50–119 pg/ mL 1078 ng/g

Xiaoyuan et al. (2014) Marino (2014)

ELISA

1008 ng/g

Marino (2014)

ELISA

Marino (2014)

ELISA

1400– 11,260 2460 ng/g

Marino (2014)

ELISA

1235 ng/g

Marino (2014)

HPLC

7895

HPLC

1500

ELISA

7000

ELISA

7000

ELISA

28,000

ELISA

29,000

ELISA

5965

HPLC-MS

15,000

Hattori et al. (1995) Pandi et al. (2006) Pandi et al. (2006) Pandi et al. (2006) Pandi et al. (2006) Manchester et al. (2000) Manchester et al. (2000) Marino (2014)

GC-MS

120,000

Marino (2014)

1510 ng/g

Musa acuminata Colla GC-MS (Musacea) Olea europaea L. (Oleracea) ELISA Rheum palmatum L. (Polygonaceae) Coptis chinensis F. (Ranunculaceae) Prunus amygdalus Batsch. (Rosaceae) Uncaria rhynchophylla (Rubiaceae) Phellodendron amurense (Rutaceae) Solanum elaeagnifolium Cav. (Solanaceae) Datura metel L. (Solanaceae) Pimpinella anisum L. (Umbelliferae) Coriandrum sativum L. (Umbelliferae) Foeniculum vulgare L. (Umbelliferae) Helianthus annuus L. (Umbelliferae) Vitis vinifera L. (Vitaceae) Elettaria cardamomum L. (Zingiberaceae) Curcuma aeruginosa Roxb. (Zingiberaceae)

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2.4 Role of phytomelatonin 2.4.1 Circadian Rhythm Melatonin regulates the circadian rhythm in animals, peaking during the scotophase and remaining constant during the photoperiod (Kazutaka et al. 2013). Consequently, phytomelatonin was assumed to serve a similar purpose in plants. It produces a diurnal oscillation that increases at night and decreases during the day (Shiddamallayya et al. 2010). This showed how the photoperiod affects melatonin’s involvement in regulating circadian rhythm. Circadian alterations in melatonin levels have been seen in algae and dinoflagellates in addition to higher plants (Amod et al. 2005; Parvin et al. 2011; Atanu et al. 2014). Researchers looked at how exogenous melatonin treatment affected Chenopodium rubrum flowering. In comparison to the control plants, the data did not indicate any harmful effects or changes in the form, colour, or quantity of leaves. Thus, the role of melatonin in flowering remains unclear (Ackermann et al. 2006; Pasquale et al. 2003). Figure 2.2 elaborates on the multi-directional role of melatonin in plants.

Fig. 2.2  The summary of multi directional actions of melatonin in plant growth, metabolism and redox balance (Bhattacharjee and Kumar 2018)

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2.4.2 Antioxidant and Free Radical Scavenger Melatonin is a well-known antioxidant in mammals (Russel 2001). This prompted the scientists to speculate that the indole molecule would behave similarly in plants. According to reports, Lycopersicon esculentum Mill. (cultivated tomato) melatonin concentration is five times higher than that of Lycopersicon pimpinellifolium Mill. (wild tomato), making the first one more tolerant in higher ozone levels. Melatonin protects against photography (Fuhrberg et al. 1996). Large amounts of free radicals, reactive nitrogen species (RNS), are evolved during photosynthesis. Additionally, as photophase exposure to light increases, the violaxanthin cycle becomes hindered, resulting in reduced plastidial photo-protection. Eichhornia crassipes had a perfect diurnal rhythm, with melatonin metabolites peaking in the late-night section of the light-dark cycle. This suggested melatonin metabolites may protect against harmful ROS and RNS damages (Balzer and Hardeland 1991). Additionally, it has been suggested higher plants and algae can benefit from melatonin’s photoprotective actions against UV radiation (Wolf et al. 2001). Alpine and Mediterranean plants subjected to high UV levels in their native habitat contain more melatonin than the same species exposed to lower UV levels, lending support to this notion. (Tettamanti et al. 2000).

2.4.3 Growth Promoter Melatonin and IAA, a powerful plant growth stimulant, are structurally similar. Melatonin is thus recommended to imitate auxin and promote vegetative development in a wide range of plant species (Kolar et al. 2003). Changes in endogenous melatonin levels, according to research, impeded auxin and cytokinin-induced root and shoot organogenesis respectively. This demonstrates the role of melatonin as a plant growth regulator (Russel and Manchester 2005). Later, Hernandez-Ruiz et al., incubated etiolated hypocotyls from Lupinus albus L. to further explore the function of melatonin with various melatonin and IAA concentrations (Hernandez and Arnao 2008). Both chemicals were scattered in plant tissues along a concentration gradient, with lower concentrations stimulating growth and higher concentrations inhibiting growth in both intact and de-rooted plant tissues. Melatonin produced the most roots and hypocotyls in this study, with values for root length that were nearly identical to those of the IAA concentrations studied (Hernandez et al. 2005). Further, the growth-promoting effects of melatonin were demonstrated in various monocots, including oat, wheat, canary grass, and barley. Studies showed that melatonin, as opposed to IAA, stimulated development in coleoptiles by about 10, 20, 31, and 55%, respectively (Dubbels et al. 1995).

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2.4.4 Defense Against Herbivores Melatonin possesses a bitter and unpleasant palate, and offers defense against herbivores (Kolar and Machackova 2001). Additionally, because melatonin tends to accumulate in animal bodies, ingestion of plants like walnut (3.5–1.0 ng/g) that contain high levels of the hormone can disrupt the physiology of herbivores. According to studies, feeding rats a diet high in melatonin elevated their blood levels from 11.51.9 pg/ml to 38.04.3 pg/ml (Rudiger 2015). This finding might be relevant to how plants defend themselves from herbivores. White fly reproduction in tobacco is reduced by tryptophan decarboxylase overexpression, an enzyme that converts 5-hydroxytryptophan to 5-hydroxytryptamine (Thomas et al. 1995). Melatonin inhibits white fly reproduction, but the exact mechanism by which it does so is still unknown.

2.4.5 Abiotic Stress Tolerance The use of melatonin can help to mitigate the detrimental consequences of abiotic stressors. The manufacture of phytomelatonin, which generally occurs within chloroplasts, and the accompanying metabolic processes have been widely researched. Melatonin controls stress responses by reducing ROS and RNS species buildup and modulating stress response pathways. Phytomelatonin role in abiotic stress is mentioned below. 2.4.5.1 Drought Stress Drought inhibits plant growth and development. Drought aggravates ROS and RNS species via activation of stress signalling pathways. Drought stress activates transcription factors such as NACs, MYBs, AP2/EREBPs, bZIPs, HDs, and bHLHs (Zhang et al. 2014). Melatonin production is often stimulated by a lack of water (Shi et al. 2015). Endogenous melatonin levels alter when melatonin biosynthesis genes (e.g., TDC, ASMT, COMT, and SNAT) are activated during a water shortage. Drought also stimulates melatonin generation in Graminae species. (Moustafa et al. 2020). Increased melatonin levels improve the stability of drought-stressed plants (Meng et al. 2014; Ding et al. 2018). Melatonin treatment can promote seed germination and lateral root formation, process (Hosseini et al. 2021; Sun et al. 2021). Melatonin also suppresses ROS-induced oxidative damage and increases antioxidative enzyme levels during drought in plants (Li et al. 2015; Antoniou et al. 2017; Alharby and Fahad 2020; Sadak and Bakry 2020).

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2.4.5.2 Waterlogging Stress Crop survival, growth, and productivity can all be harmed by waterlogging. This checks gas diffusion, resulting in hypoxic stress in the roots, and promotes ROS accumulation (Zhang et al. 2019; Gu et al. 2020; Wu et al. 2021). Waterlogging causes a rise in endogenous melatonin levels (Moustafa et al. 2020). Exogenous melatonin treatment significantly improves the seedling vitality of many plants (Zheng et al. 2017; Zhang et al. 2019; Gu et al. 2020). It reduces stomatal closure, chlorophyll and photosynthesis reduction, and leaf senescence (Zhang et al. 2019; Gu et al. 2020; Zheng et al. 2017). Melatonin treatment also reduces the oxidative damage caused by waterlogging. To maintain redox homeostasis under waterlogging stress, melatonin activates antioxidant enzymes and minimized H2O2 levels in both leaves and roots of peach seedlings (Gu et al. 2020). 2.4.5.3 Salt Stress Melatonin improves salt tolerance in many plants such as maize, wheat, etc. (Liang et al. 2015; Zhou et al. 2016; Chen et al. 2018; Ke et al. 2018; Zhang et  al. 2021). Salt stress alters the expression of essential biosynthetic enzyme patterns resulting increase in endogenous melatonin levels (Arnao and Hernández 2009). Furthermore, overexpression of SNAT can improve plant salt tolerance considerably (Wu et  al. 2021). SNAT inhibition, on the other hand, lowers endogenous melatonin levels, making rice more sensitive to salt stress (Byeon and Back 2016). Exogenous melatonin protects plants from salt stress by regulating antioxidant enzyme expression (Zhan et al. 2019) resulting in suppression of ROS and H2O2 caused level by salinity. Furthermore, melatonin-NO crosstalk regulates redox equilibrium via differential expression of copper/zinc-SOD and manganese-SOD under salt stress (Arora and Bhatla 2017; Kaya et al. 2020). 2.4.5.4 Cold Stress Melatonin protects plants from cold-induced stress. Plant cold tolerance can be improved by increasing endogenous melatonin levels. SNAT transgenic rice showed better stability than wild-variety (Kang et al. 2010). Melatonin improves cold tolerance in grafted watermelons (Tan et al. 2007; Li et al. 2021a). 2.4.5.5 Heat Stress Heat stress has physiological, transcriptional, post-transcriptional, and epigenetic effects on plants (Zhao et al. 2020). Melatonin improves thermal tolerance in plants. COMT1 and TDC silencing in tomatoes resulted in a decline in melatonin biosynthesis causing temperature-induced stress (Ahammed et al. 2019).

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Tolerance to potassium deficiency is a critical issue in crop production. Melatonin increases potassium levels in Malus and wheat (Li et al. 2016, Li 2021a). TaNAC71-­ regulated TaHAK1 is a vital factor to cope with MT-mediated potassium deficiency in wheat (Li et al. 2021b). Furthermore, melatonin reduces nano-plastic uptake by roots and translocation to shoots by regulating the expression of aquaporin-related genes (TIP2-9, PIP2, PIP3, PIP1-5, and PIP1.2) (Li et al. 2021c).

2.5 Conclusion & Future Aspects Melatonin regulates various physiological functions in plants, including the circadian rhythm, cytoprotection and growth promotion, antioxidant defence, and free radical scavenging (Xiaoyuan et al. 2014). Additionally, it encourages rhizogenesis, cellular growth, and protects from environmental stress conditions (Chandana et al. 2014). Uses of phytomelatonin in agriculture; and humans have gained momentum at present. The first, exogenous melatonin administration to plants promotes improved growth and development as well as greater response to a variety of environmental stressors, including radiation, heat, cold, and drought. Additionally, melatonin speeds up plant germination, development, and productivity. It slows the senescence of leaves brought on by stress. These cumulative findings suggest that treating farmed plants with exogenous melatonin or overproducing plants with greater melatonin levels may aid crops in more readily resisting various harmful environmental situations that they typically experience throughout their growth (Pandi et al. 2006). The latter parts deal with the potential introduction of melatonin-rich plant foods or dietary supplements because of the enormous health benefits it offers, especially in the fight against neurodegenerative diseases like Alzheimer’s. According to studies, persons who take up to 1 gram of melatonin orally each day experience no negative side effects. Melatonin is additionally quickly absorbed through the digestive system. As a result, the use of melatonin as a nutraceutical appears to have a bright future in promoting a better lifestyle (Charanjit et al. 2008; Jemima et al. 2011). Acknowledgements  We sincerely acknowledge The Assam Royal Global University, Guwahati, Pratiksha Institute of Pharmaceutical Sciences, Guwahati and Assam Downtown University, Guwahati for providing necessary infrastructure to prepare the manuscript. Conflict of interest  The author declares there is no conflict of interest.

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Chapter 3

Abiotic Stress-Induced Modulation of Melatonin Biosynthesis Accompanying Phytohormonal Crosstalk in Plants Mrinalini Kakkar

Abstract  Initially identified as a potent regulator in animals, melatonin is a multifunctional molecule that regulates versatile physiological and developmental processes in both plants and animals. The biosynthesis of melatonin is not restricted but shares multiple locations in both plants and animals. Moreover, the levels too are critically regulated depending upon the type and time where they are produced. Melatonin production is induced under several abiotic and biotic stress conditions, and therefore, its multiple signalling and secondary plant metabolic processes. Therefore, this chapter summarises the comparative understanding of melatonin biosynthesis in plant and animal systems, along with the biosynthetic regulation under normal and challenging conditions and cross-talk of melatonin with other plant regulators for optimal growth and development. Keywords  Melatonin · Plant growth · Tryptophan · Biosynthetic regulation · Stressors · Hormonal crosstalk

3.1 Introduction: Discovery and Functional Attributes More than 50 years ago, melatonin was first extracted from the bovine pineal gland and then structurally characterised (discovered in 1958), Melatonin (MT, N-acetyl-5-­ methoxytryptamine) as an indole compound derived from tryptophan (Lerner et al. 1958, 1959; Fig. 3.1). It was coined as melatonin due to its ability to lighten the skin color in certain fishes, reptiles, and amphibians (Carlson 1994). Known and well-­ characterized as an essential neurohormone in animals, it was first discovered in the cow’s pineal gland and plays a critical role in many biological processes. (Aaron et al. 1958). In humans, melatonin is functionally associated with the regulation of M. Kakkar (*) Department of Plant Molecular Biology, University of Delhi, South Campus, New Delhi, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_3

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Fig. 3.1  Structure of melatonin showing 5-methoxy group and 3-amide groups, the two ROS quenching sites, responsible for antioxidant activity

physiological functions such as improving sleep, sexual reproduction, temperature homeostasis, retina physiology, behaviour, mood, anxiety, regulating jetlag issues (Cardinali et al. 2012), dietary supplement (due to its perceived antioxidant activity), regulate the circadian clock, delay aging, alleviating allergic symptoms, and regulating the immune system. Thereby, it is commercially used in healthcare products and medicines (Lerner et al. 1958; Shi et al. 2015a). Initially believed to only exist and serve certain purposes in the animal kingdom, three separate studies found that melatonin is naturally dispersed in the plant kingdom as well (Dubbels et al. 1995; Hattori et al. 1995; Koláˇr and Macháˇcková 2005). In the past decade, melatonin was found to regulate diverse biological and physiological plant processes, such as plant growth and development, circadian rhythms and photoperiodic responses, antioxidation, abiotic stress responses (heat, salt, cold, salinity), and biotic stresses (bacterial and fungal infections) (Hernández-Ruiz et  al. 2004, Shi et al. 2015b; Yu et al. 2019; Arnao and Hernández-Ruiz 2015; Turk et al. 2014; Zhao et al. 2021a). Functions thoroughly in coleoptile growth, melatonin regulates fruit ripening (Mansouri et al. 2021), root architecture and morphogenesis (Yang et al. 2021a; Sarropoulou et al. 2012), flowering processes (Byeon and Back 2014), leaf senescence (Wang et al. 2013), and, chlorophyll, proline and carbohydrate content in leaves and fruits (Shi et al. 2016), acting as a signaling molecule, mediating the plant defense response to pathogen attacks through the mitogen-activated protein

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kinase (MAPK) pathway (Lee et  al. 2014, 2016; Shi et  al. 2016), melatonin is a multifactorial component in plants. Melatonin is a pleiotropic signalling molecule that is involved in many abiotic stress reactions, such as oxidative (Li et al. 2016a), heavy metal (Lee et  al. 2017), high temperature (Xu et  al. 2016), cold (Li et  al. 2016b), senescence (Liang et al. 2015), drought (Wei et al. 2015), aluminum (Zhang et al. 2017), and salt stresses (Kostopoulou et al. 2015), its involvement is highly appreciated. Melatonin modulates seed germination, promotes lateral root development, manages flowering time, and delays leaf senescence under normal circumstances (Arnao and Hernández-Ruiz 2019a, 2020). Melatonin functions as a direct scavenger of reactive oxygen and nitrogen species in unfavourable settings (Arnao and Hernández-Ruiz 2019b). It also indirectly regulates the expression via regulating the expression of stress-responsive transcription factors. It functions as an auxin-­like regulator by acting upstream to the auxin pathway and changing the expression profiles of numerous auxin-related transcription factors (WRKY, NAC, MYB, bHLH, and HD-ZIP), mimicking the activity of auxin (Liang et al. 2017). Not only auxin, but melatonin also interacts with several other plant hormones, including gibberellic acid (GA), cytokinin (CK), abscisic acid (ABA), ethylene (ET), salicylic acid (SA), jasmonic acid (JA), brassinosteroid (BR), strigolactones, and polyamines (Arnao and Hernández-Ruiz 2020) where it plays a pivotal role in plant growth and development. Moreover, the exogenous application of melatonin can modulate the biosynthesis of endogenous melatonin and the activity of antioxidative enzymes, it enhances plant tolerance towards various stresses (e.g., drought, salt, heat, cold, waterlogging, and heavy metal toxicity) (Weeda et  al. 2014; Mukherjee et al. 2014; Zhang et al. 2015; Mukherjee 2019; Moustafa-Farag et al. 2020; Sun et al. 2021). Owing to these essential characteristics, in 2004 the term ‘phytomelatonin’ was proposed (Murch and Erland 2021), and the need to learn more about the biological processes, biosynthesis routes, and control of melatonin in the plant kingdom drove scientists to pursue their research in this field. Distributed ubiquitously throughout the evolution apart from higher plants and animals (Hattori et al. 1995; Dubbels et al. 1995), melatonin is also found in a unicellular alga (Balzer and Hardeland 1991), amphibians, and birds. As identified in lower organisms, the origin of melatonin is estimated to be almost 2.5–3.5 billion years ago when the transition from anaerobic to aerobic metabolism occurred to acquire the ability to produce melatonin to mitigate oxidative stress damage (Kurland and Andersson 2000; Muller et al. 2012) Henceforth, melatonin was identified in the primitive nitrogen-fixing bacterium as Rhodospirillum rubrum (Manchester et  al. 1995; Tilden et  al. 1997), primitive photosynthetic bacteria including cyanobacteria, dinoflagellate Lingulodinium polyedrum (Balzer and Hardeland 1991, Poeggeler et  al. 1991), blue-green algae Arthrospira platensis (syn. Spirulina platensis) (Majima et al. 1999, Hattori et al. 1995, kelp Pterygophora californica (Fuhrberg et al. 1996) and non-metazoans (Hardeland 1999). The fact that this indolamine molecule has been widely distributed and preserved throughout the evolution of all creatures points to its importance and functional relevance in plant and animal kingdoms. (Manchester et  al. 2015; Pshenichnyuk et  al. 2017). Its widespread use and active participation in many regulatory and

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developmental processes have drawn a lot of study interest recently. The basic knowledge of melatonin in plants has advanced significantly during the last 10 years.

3.2 Structural Features of Melatonin Melatonin, an indolamine also known by its chemical name N-acetyl-5-­ methoxytriptamine, was discovered and initially identified as a small molecule with a molecular weight of 232 Daltons. (Lerner et  al. 1959). Pure melatonin has a molecular weight of 232.28 g/mol, a density of 1.175 g/cm3, and an off-white powdery appearance and texture, according to the results of the physio-chemical analysis. Between 116.5 °C and 118 °C, it melts, and 512.8 °C is the temperature at which it boils. (Mannino et al. 2021). Melatonin has the chemical formula C13H16N2O2 and is functionalized with a 3-amide group and a 5-alkoxy group on the indole chemical scaffold (Fig. 3.1). This molecule is amphiphilic by nature due to the hydrophobic 3-amide group and hydrophilic 5-alkoxy group. Due to its ability to cross any biological membrane and enter any cellular or subcellular compartment, it enables a varied subcellular distribution that is simple throughout the cell (Omer et al. 2021). It is also categorised as an indolamine molecule since tryptophan is its precursor (Omer et al. 2021), and the electron-rich indole moiety exhibits strong resonance mesomerism and electro reactivity, making it a potent free radical scavenger (Poeggeler et al. 1996; Omer et al. 2021).

3.3 Comparative Insight into Melatonin Biosynthesis in Plant and Animal System The aromatic amino acid tryptophan is the sole precursor for melatonin biosynthesis in both plants and animals. Melatonin biosynthesis occurs from tryptophan was experimentally validated almost two decades ago by isotope tracer studies using 14C-tryptophan, which demonstrated rapid conversion to melatonin within an hour in the in vitro grown in Hypericum perforatum (L.) plantlets (Murch et al. 2000). Clearly, melatonin biosynthesis in both plants and animals can be divided into two parts; (A) Synthesis of an intermediate (tryptophan to serotonin), and (B) Synthesis of the final product (melatonin from serotonin). Four enzymes work together to produce melatonin in animals. Tryptophan hydroxylase (TPH) converts tryptophan into 5-hydroxytryptophan, which is then decarboxylated by aromatic amino acid decarboxylase (AADC) to produce serotonin, which is then acetylated by arylalkylamine N-acetyltransferase (AANAT), also known as serotonin N-acetyl (or N-acetylserotonin). Finally, N-acetyl-5-­ hydroxytryptamine is O-methylated by hydroxyl indole-O-methyltransferase (HIOMT), also known as N-acetylserotonin methyltransferase (ASMT), to produce melatonin (Axelrod and Weissbach 1960; Weissbach et al. 1960; Tan et al. 2016). In

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contrast, the melatonin production route in plants consists of four key stages and six enzymes (Back et  al. 2016). Four pathways for melatonin biosynthesis in plants have been proposed based on the enzyme kinetics: (1) the tryptophan/tryptamine/ serotonin/N-acetylserotonin/melatonin pathway (which occurs under normal environmental conditions); (2) tryptophan/tryptamine/serotonin/5- methoxy tryptamine/ melatonin pathway (which may occur under stress conditions, or when plant produces high levels of serotonin; Back et al. 2016); (3) tryptophan/5-­hydroxytryptophan/ serotonin/N-acetylserotonin/melatonin pathway, and (4) tryptophan/5-­ hydroxytryptophan/serotonin/5-methoxytryptamine/melatonin pathway. The six enzymes that are involved in the synthesis of melatonin from tryptophan are: (a) L-tryptophan decarboxylase (TDC), (b) Tryptamine 5-hydroxylase (T5H), (c) Serotonin N-acetyltransferase (SNAT), (d) Acetyl-serotonin O-methyltransferase (ASMT), (e) Caffeic acid 3-O-methyltransferase (COMT), and (f) a putative tryptophan hydroxylase (TPH); yet to be identified in plants. The first two steps of animal biosynthesis are reversed in plants. Tryptophan is decarboxylated by tryptophan decarboxylase (TDC) into tryptamine in the cytoplasm, which is then hydroxylated by tryptamine-5-hydroxylase (T5H) into serotonin in the endoplasmic reticulum. The latter steps of biosynthesis are catalysed by the SNAT (serotonin-N-­ acetyltransferase), ASMT (acetyl-serotonin methyl transferase), and COMT (caffeic acid O-methyltransferase). The serotonin is acetylated by SNAT enzyme, which converts serotonin into N-acetyl serotonin, which further upon methylation either by ASMT or COMT forms melatonin in the cytoplasm (Referred as Pathway I; Fig.  3.2). Serotonin in the presence of either ASMT or COMT is converted into 5-­methoxyltryptamine in the cytoplasm and finally by the activity of SNAT, converted into melatonin in the chloroplast (Pathway II; Fig. 3.2). However, similar to animals, tryptophan 5-hydroxylase (TPH) converts tryptophan into 5-­hydroxytryptophan, which is converted into serotonin by tryptophan decarboxylase (TDC) in the cytoplasm. Further serotonin in the cytoplasm is converted into N-acetylserotonin by SNAT activity, and further by the activity of ASMT/COMT into the final product melatonin (pathway III; Fig. 3.2). Whereas, serotonin formed via 5-hydroxytryptophan intermediate, from cytoplasm can also be converted into 5-methoxytrpamine by ASMT/COMT activity, which further is converted into melatonin by SNAT in the chloroplast (Pathway IV; Fig. 3.2) (Tan et al. 2016; Back et al. 2016). Depending on the surrounding conditions, the order of the enzyme’s action changes (Byeon et al. 2015). Different ASMT isoforms are expressed when there is adversity or stress, which causes serotonin to be first O-methylated by ASMT to produce 5-methoxytryptamine and then acetylated to produce melatonin (Ye et al. 2018; Tan and Reiter 2020). In contrast, the predominant process under normal circumstances is the acetylation of serotonin to create N-acetyl-5-hydroxytryptamine, which is then O-methylated to create melatonin (Ye et al. 2018; Fig. 3.2). Mammals utilize animal-specific transferases to catalyse acetylation and methylation reactions. Mammalian serotonin N-acetyltransferase (SNAT) and N-acetyl serotonin methyltransferase (ASMT), known as arylalkylamine N-acetyltransferase (AANAT), and hydroxyl indole-O-methyltransferase (HIOMT), respectively.

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Fig. 3.2  Schematic representation of biosynthesis of indode-3-acetic acid (IAA), salicylic acid (SA), and melatonin sharing common precursor chorismite from shikimate pathway. Dashed arrows represent pathways other than melatonin biosynthesis. The multiple pathways of melatonin biosynthesis are represented based on the intermediated and corresponding enzymes. The details of the four pathways are mentioned in coloured boxes. Green, blue, and red boxes correspond to plastids, cytoplasm, and endoplasmic reticulum, respectively. The dashed line in the lower half of the figure depicts the feedback loop as mentioned in the literature. The right side of the figure represents the melatonin biosynthesis pathway in animals. TDC, tryptophan decarboxylase; TPH, tryptophan hydroxylase; T5H, tryptamine 5-hydroxylase; SNAT, serotonin N-acetyltransferase; ASMT, N-acetylserotonin methyltransferase; COMT, caffeic acid O-methyltransferase; ASDAC, N-acetylserotonin deacetylase; AANAT, arylalkylamine N-acetyltransferase; HIOMY, hydroxyindole-O-methyltransferase

Crystallographic studies have shown that plant and animal SNATs are distinct from one another because plant SNATs can make dimers in solution, which is a characteristic that distinguishes them from animal SNAT/AANAT (Liao et al. 2021). This implies that there is no genetic conservation between the SNAT genes of plants and animals. As the biosynthetic capability of tryptophan to melatonin conversion exceeds the conversion of serotonin to melatonin, a low level of melatonin is always being synthesised in plants. Of all the variable biosynthesis pathways for melatonin production, serotonin is a necessary intermediate, suggesting that serotonin is an essential intermediate for melatonin synthesis. Beginning with an aromatic amino acid tryptophan is the precursor produced from the shikimate pathway in plants and attained through the dietary components in the animals, is first transformed to tryptamine through a decarboxylation process catalysed by tryptophan decarboxylase (TDC) (Zhou et al. 2020). The mechanism of the conversion of tryptophan to tryptamine using TDC is not conserved throughout evolution among plants, as certain ecotypes of Arabidopsis fail to show the presence of the TDC gene, along with some ecotypes responding differently to melatonin exposure (Zia et al. 2019). TDC serves as a bottleneck in regulating melatonin biosynthesis. The TDC gene has been cloned from several different species, including rice (Kang et al. 2007a, b), pepper (Park et al. 2009), Catharanthus roseus (De Luca et al. 1989), and tobacco (Di Fiore et al. 2002), although its expression is very low or nonexistent in these species. Five

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genes expressing TDC proteins and 14 genes encoding ASMT proteins were found in the tomato genome by in silico analyses (Liu et al. 2017; Pang et al. 2018). Using the already reported TDC probe, in the genus Citrus, the first putative TDC protein sequence was experimentally proven De Masi et al. 2017). Apart from competition for tryptamine, the conversion of tryptamine to serotonin by TDC also exhibits feedback regulation because it serves as a precursor for numerous secondary metabolic pathways and one of the many pathways for IAA biosynthesis (tryptamine transforms into indole-3-acetaldehyde and then into IAA) (Kang et  al. 2007a; Erland et al. 2018; Fig. 3.2, upper part). As a result, it has been postulated that the first enzyme in the melatonin pathway that is kinetics dependent and the rate-­ limiting enzyme is the tryptophan by TDC activity is converted to tryptamine (Kang et al. 2007a). TDC was first only found in the Apocynaceae family (De Luca et al. 1989), but it has since been thoroughly characterised in rice, sweet cherry, and cassava plant systems (Byeon et al. 2014a, b, 2016; Zhao et al. 2019; Wei et al. 2018b). However, an intermediate step; 5-hydroxytryptophan formation from tryptophan occurs in animals, regulated by TPH, which is the first enzyme in the melatonin biosynthesis pathway in animals (Fitzpatrick 1999; Slominski et  al. 2002). The cloning of the TPH coding genes and determination of the corresponding TPH enzyme has yet not been reported in plants. However, recently 5- hydroxytryptophan product has been detected in hickory, suggesting that some gene encoding an enzyme or performing a similar function to TPH as in animals is present, suggesting though not true homologs, TPH-like genes may exist in plants (Chen et al. 2021). Also, in the seeds of Griffonia simplicifolia high levels of 5-hydroxytryptophan were detected (Bell and Fellows 1966; Lemaire and Adosraku 2002). An enzyme similar to TPH was found in rice roots as well, probably catalysing the conversion of tryptophan to 5-hydroxytryptophan, however, serotonin is produced in the cytoplasm in rice (Kang et  al. 2007a, b; Back et  al. 2016). The production of 5-­hydroxytryptophan in mammals, where tryptophan is first transformed by TPH activity to 5-hydroxytryptophan, which is subsequently catalysed by AADC to generate serotonin, is undoubtedly an important step in this process. In plants, this aspect of the system is less well understood. In plants, the C-5 position of tryptamine is then hydroxylated to create serotonin (5-hydroxytryptamine), which is the main intermediate step of the melatonin production pathway, after the action of the cytochrome P450 enzyme, tryptamine 5-hydroxylase (T5H) (Fujiwara et al. 2010; Kang et al. 2007a). T5H has been studied in several plant species, including rice, where Fujiwara et al. (2010) used map-based cloning to identify it in rice sekiguchi lesion (sl) mutants. Plants that grow rice (Oryza sativa) are healthy and express T5H by default (Kang et al. 2007b). In the second part of the pathway; biosynthesis of melatonin from serotonin occurs via two intermediates; (a) N-acetylserotonin (NAS), and b) 5-­ methoxytryptamine (5-MT), the reaction catalyzed by serotonin N-acetyltransferase (SNAT; Kang et al. 2013) and by a caffeic acid-O-methyltransferase (COMT; Lee et al. 2014), respectively. Plants exhibit dual pathways for the conversion to melatonin, where a) acetylation is followed by methylation, or (b) methylation is followed by acetylation. However, animal cells successively use

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mammalian-­specific acetylases and methylases; AANAT and HIOMT, respectively. The serotonin is converted into N-acetyl-serotonin by the activity of N-acetyltransferase (SNAT) or arylalkylamine N-acetyltransferase (AANAT), in plants and animals, respectively (Kang et al. 2013). Afterward, N-acetyl-serotonin is converted into melatonin by ASMT (Park et al. 2013), or COMT (Byeon et al. 2014a) and HIOMT (Zuo et al. 2014) in plants and animals, respectively. In parallel to this reaction, serotonin is also converted by ASMT or COMT and HIOMT into the 5-methoxytryptamine, which in turn is converted by SNAT into the final product, melatonin (Lee et al. 2014; Tan et al. 2016). Furthermore, recently a reverse reaction of serotonin acetylation has also been found in plant cells using N-acetylserotonin deacetylase (ASDAC) (Lee et al. 2017; Back 2021; Wei et al. 2021; Liao et al. 2021) converting N-acetyl-­serotonin to serotonin, or melatonin to 5-methoxytryptophan; allowing the probability of regulating the melatonin levels in specific cellular compartments (Lee et al. 2019; Fig. 3.2). ASMT and COMT were likely to be evolved in the land plants. COMT was identified in bryophytes as well, and COMT is presumed to have evolved from ASMT, as in higher plants an increased activity of COMT than ASMT has been found. Moreover, in higher plants, COMT is also involved in the lignin biosynthesis pathway (Zhao et al. 2021b). SNAT is also a key rate-limiting enzyme (Liao et al. 2021). The knockouts of SNAT enzymes exhibit changed phenotypes and show enhanced sensitivity to abiotic stress conditions (Lee et al. 2019). The SNAT enzyme was found to be regulated by feedback inhibition in rice (Back et al. 2016).

3.4 Biosynthetic Regulation of Melatonin in Normal and Challenging Environments In plant cells, the various enzymes involved in the production of melatonin are distributed differently. In practically every plant organ, including the leaves, roots, stems, petals, flower buds, fruits, and seeds, melatonin is found in varying degrees. In numerous plant systems, including fruit trees, herbs, and crops, melatonin expression has thoroughly been researched (Byeon et al. 2012). However, plant species, organs, and growth stages all exhibit significant variations in expression (Hernández-­ Ruiz et al. 2004). In pepper fruits, two TDC genes, PepTDC1 (LOC107877290) and PepTDC2 (LOC107842494), have been identified. The expression of the former is elevated in pepper fruits that have been contaminated with fungus or treated with ethylene, and it is significantly expressed in unripe green fruit but not in mature red fruit. In contrast, the latter is constitutively low expressed in all the tissues (Park et al. 2009). Seasons and circadian cycles can affect the levels of melatonin production (Beilby et al. 2015). For instance, in morning glory, its concentration skyrockets as the plant matures (Van Tassel et al. 2001). The melatonin biosynthetic enzymes exhibit modulation under particular light/dark regimes. In comparison to plants grown in darkness, grapevine plants grown in the light had higher amounts of

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melatonin (Boccalandro et  al. 2011). In rice, the expression of some genes was induced in the light phase (OsTDC1, for OsASMT4/6 and OsASMT13), some in dark conditions (OsTDC2, OsSNAT1, and OsSNAT2), and some are independent of light and dark fluctuations (OsTDC3 and OsTDC4). Consequently, light/dark conditions change the expression levels of genes encoding enzymes for melatonin production, exhibiting a cyclical/ rhythmic pattern (Bhowal et  al. 2021). So, to generalise the melatonin levels under the day/night cycle need to be studied in more plant species. Melatonin concentration is also affected by environmental conditions, the levels are significantly higher in field-grown rice compared to those in the growth chamber grown (Byeon et  al. 2012). Two microRNAs, miR6249a and miR-1846e, were recently found to modulate the expression of the melatonin biosynthesis genes OsTDC5 and OsASMT18 under light and stress, respectively (Bhowal et al. 2021). The melatonin content varies with the age of the plant, higher in reproductive tissues (young parts), while the decline in senescence tissues as observed in two-day-­ old seedlings of Pharbitis nil (L.) compared with older seedlings (Van Tassel et al. 2001). Moreover, the expression of key melatonin biosynthesis genes is also affected by hormone pathways. For instance; in hickory, the ethylene-insensitive protein 3 (CcEIN3) stimulates the production of CcTDC and CcASMT1 (Chen et al. 2021). OsTDC2, OsT5H1, and OsSNAT2 transcripts were shown to be downregulated in rice during salt stress, but only OsSNAT2 expression was found to be elevated in rice under heat stress. However, rice treated for drought stress showed an upregulation of the majority of the biosynthetic genes (Bhowal et al. 2021). Besides flowering and morphogenesis, melatonin biosynthesis is induced during senescence (Park et al. 2012; Lee et al. 2017; Byeon et al. 2012). Enhanced accumulation of serotonin and TDC levels were identified in rice leaves undergoing senescence (Kang et al. 2009b). Both AtTDC1 (comparatively high levels) and AtTDC2 genes and AtASMT13 and AtASMT14 expressions were induced under senescence (Bhowal et al. 2021). Therefore, melatonin biosynthesis in plants is dependent upon many factors, like light/dark cycles, environmental conditions, reactive oxygen species, photoreceptors (e.g., phytochromes and cryptochromes), age of the plant, etc. (Lee et al. 2017; Hwang et al. 2020; Hwang and Back 2021). Literature has shown that the genes involved in melatonin biosynthesis also have huge variability in the number of genes corresponding to each enzyme in different plants. For example; in Hickory plants, there are 9 TDC, 11 T5H, 1 SNAT, 7 COMT, and 1 ASMT genes encoding the melatonin biosynthetic pathway enzymes, and no gene encoding TPH was identified (Chen et al. 2021). Table 3.1 shows the number of genes corresponding to melatonin biosynthesis enzymes, as identified in some of the monocot and dicot plants. The cellular compartments in plants with the greatest melatonin levels are the mitochondria and chloroplasts., therefore are the important sites of melatonin biosynthesis (Tan and Reiter 2020; Kanwar et  al. 2018). In Catharanthus roseus and Tabernaemontana divaricata, the first enzyme that is involved in melatonin biosynthesis, TDC is localized in the cytoplasm (De Luca and Cutler 1987; Stevens et al. 1993), whereas the T5H is localized in the endoplasmic

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Table 3.1  Number of melatonin biosynthesis genes identified in various monocot and dicot plants Plant system TDC T5H SNAT ASMT References Arabidospis 2 1 1 17 Bhowal et al. (2021); Byeon et al. (2016) Rice (Oryza sativa) 7 1 2 19 Bhowal et al. (2021); Ahn et al. (2021); Byeon et al. (2014a, b); Kang et al. (2011, 2013); Fujiwara et al. (2010); Kang et al. (2007a, b) Tomato (Solanum 5 6 2 14 Bhowal et al. (2021); Liu et al. (2017) lycopersicum) Sorghum (Sorghum 9 1 1 28 Bhowal et al. (2021) bicolor) Hickory (Carya 9 11 1 1 Chen et al. (2021) cathayensis) Barley (Hordeum 13 1 2 1 Yang et al. (2022) vulgare) Wheat (Triticum ~39 4 6 3 Yang et al. (2022) aestivum) Maize (Zea mays) 5 2 2 0 Yang et al. (2022) Cassava 2 1 1 3 Wei et al. (2016) Capsicum annuum 16 Pan et al. (2019) Morus alba 20 Zheng et al. (2021) Apple 37 Wang et al. (2022) Walnut 46 Ma et al. (2022)

reticulum (ER), and similar localization of these enzymes is in rice (Back 2021; Kang et al. 2007a; Fujiwara et al. 2010). The SNAT from both rice and Arabidopsis were found in chloroplasts; studied after merging with chlorophyll fluorescence (Lee et al. 2014; Kang et al. 2013; Byeon et al. 2014a, b, 2016). ASMTs from rice are cytoplasmic localized (Byeon et  al. 2014b). Due to the absence of leader or transit sequences, both COMT proteins from Arabidopsis, rice, and are localised in the cytoplasm (Byeon et al. 2014a, 2015). Transient expression in tobacco leaves was used to study the localization of the cassava enzymes MeTDC2, MeASMT2, and MeASMT3, which localized in both the cytoplasm and nucleus (Wei et  al. 2016). At particular developmental stages, the bulk of the genes that code for the enzymes involved in melatonin production has varying transcript abundances. For instance, AtTDC1 levels are maximum at the seed germination stage in Arabidopsis, SlT5H6 levels are highest at the fruit ripening stage in tomato and OsTDC1 levels boost during the rice heading stage, and SbASMT14 is especially increased at the sorghum booting stage (Bhowal et al. 2021). SNAT, a crucial melatonin synthetase, is mostly found in the chloroplasts of rice, cotton, cucumber, and tomato (Byeon et al. 2014b; Zhang et al. 2022). Apple’s MzSNAT5, which is located in the mitochondria rather than the chloroplast, resembles animal SNAT more than MzSNAT9 or other SNATs found in other species (Wang et al. 2017; Tan and Reiter 2020). Significant chloroplast expression of COMT and ASMT leads to increased melatonin synthesis when they are overexpressed (Choi et  al. 2017). When considered collectively, these data point to the chloroplast as the primary location for melatonin

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production. Several bacterial species, including cyanobacteria and -proteobacteria, generate melatonin. Melatonin is found in both of these organisms, and it is generally known that mitochondria evolved from ingesting -proteobacteria and chloroplasts from photosynthetic cyanobacteria. According to Zhao et  al. (2019), both subcellular locations are the sites for melatonin production because both organelles most likely kept their capacity to generate melatonin throughout evolution. Recent evidence from plants also suggests that, under normal circumstances, plants preferentially perform melatonin biosynthesis in chloroplasts; however, under stressful circumstances, the chloroplast pathway is blocked, and mitochondria are the preferred site for melatonin biosynthesis (Tan and Reiter 2020). Although the mitochondria and chloroplast of roots and leaves are the primary sites of melatonin production, its transfer to meristems, flowers, and fruits stimulates the addition of its numerous activities in plants (De la Puerta et al. 2007; Wang et al. 2016a; Arnao and Hernández-Ruiz 2017). Melatonin expression and location vary widely in some plant species, where it is transported as a long-distance signal from roots to shoots (Mukherjee et al. 2014). Therefore, from different studies, it can be concluded that TDC, ASMT, T5H, and SNAT, are localised in the cytoplasm, ER, and chloroplast, respectively, with a few exceptions. Additionally, because the melatonin intermediates are dispersed throughout several subcellular spaces, including the cytoplasm, endoplasmic reticulum, and chloroplast, the enzymatic regulation either facilitates or impedes biosynthesis. Henceforth, the cytoplasm or chloroplasts can be the ultimate subcellular locations of melatonin synthesis, which has an impact on how melatonin affects plant growth and development.

3.5 Melatonin and Phytohormone Crosstalk To control stress tolerance, melatonin interacts with several plant hormones including indoleacetic acid (IAA), gibberellic acid (GA), cytokinin (CK), abscisic acid (ABA), ethylene (ET), salicylic acid (SA), jasmonic acid (JA), brassinosteroid (BR), strigolactones, and polyamines. According to several studies (Kaur et  al. 2015; Mukherjee et  al. 2014; Shi et  al. 2016; Arnao and Hernández-Ruiz 2006; Mukherjee 2019), melatonin modulates abiotic stress tolerance in plants by altering hormonal metabolic processes produced by stress signals. Among the major plant hormones, indole-3-acetic acid (IAA) shares structural similarity with melatonin (Baluška and Mancuso 2013; Arnao and Hernández-Ruiz 2014) such that regulates endogenous NO levels, which further regulates transcription factors, and helps to maintain redox homeostasis and tolerance during stress conditions (Zhu et al. 2019). Serotonin, a tryptophan-derived conserved signalling molecule, intermediate of melatonin biosynthetic pathway, regulates gene expression associated with auxinresponsive pathways. Auxin, a very well-studied plant hormone, controls the polarity, growth, and gravitropism of plant tissues through its distinctive spatial-temporal distribution. NaCl stress also alters auxin efflux and threshold levels (Sun et  al.

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2008; Zolla et al. 2010). Therefore, the abiotic stress-induced inhibition of auxin biosynthesis shifts the metabolic process towards serotonin accumulation, which further enhances melatonin levels in plant tissues, mainly roots, major sites for serotonin and auxin biosynthesis, reported in growing sunflower seedlings (Mukherjee et al. 2014). However, in both rice and Arabidopsis, auxin had no discernible effects on the expression of the genes that code for the enzymes that produce melatonin. While prolonged auxin exposure in tomato suppressed the expression of SlASMTs (Bhowal et al. 2021). Although endogenous auxin production and transportation are necessary for melatonin to have an impact on plant growth and development, the underlying processes are yet unknown. Similar to IAA, melatonin works by promoting root elongation at low concentrations while inhibiting root development at higher concentrations. In the case of IAA, for instance, low melatonin concentrations encourage root elongation while high melatonin concentrations limit root growth. Melatonin and IAA do not have the same working concentration, hence they cannot be placed in the same category. IAA at 0.1–1 nM (low) and melatonin at 10–1000 nM (high) both stimulate root development in Arabidopsis, and IAA at 1  nM (low) and melatonin at 1000  nM (high) both moderately correlate with changed expression of auxin-responsive genes (Yang et al. 2021a). Additionally, in Brassica, the exogenous injection of melatonin (at 0.1 M) boosted root elongation because the root’s endogenous IAA levels were elevated, whereas treatment with 100 M (high) inhibited root development but did not affect t on the level of endogenous IAA (Chen et al. 2009). High levels of exogenous melatonin may prevent the synthesis of endogenous melatonin, causing tryptophan to become freely available and the metabolic process to switch to auxin biosynthesis. It is generally established that auxin controls two opposing routes in roots that result in cell expansion (Li et al. 2021b). What is less clear is how melatonin acts in relation to this process of cell expansion, specifically whether it facilitates auxin’s binding to TMK1 or TIR1/ AFBs needs to be explored. Melatonin acts as an auxin-like regulator and increases the expression of auxin signalling and efflux genes (PIN1, PIN3, and PIN7) in tomato plants as well as the development of adventitious roots (Wen et al. 2016). Melatonin mimics auxin action by acting upstream of the auxin pathway to change the expression patterns of different auxin-related transcription factors, including those from the WRKY, NAC, MYB, bHLH, and HD-ZIP families (Liang et  al. 2017; Tan and Reiter 2020). Moreover, the concentration of melatonin in plants is strongly correlated with the availability of its precursor (Byeon et  al. 2015), and that’s why there is always a competition between melatonin and auxin biosynthesis. While there is a wealth of information regarding the interactions between melatonin and other plant hormones, it is still necessary to understand the internal crosstalk that controls these interactions. Moreover, how this cross-networking helps to relieve stress conditions also needs to be evaluated. Melatonin and serotonin function similarly to auxins and cytokinins because of their strong biosynthetic relationships, which is analogous to the equilibrium that exists for auxin and cytokinin. Together, these chemicals are incriminating their function in plant growth and development, organogenesis, and morphogenesis (Erland et  al. 2019). Melatonin impacts the production and catabolism of ABA genes under various abiotic

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stressors, including drought, salinity, heat, and cold (Fu et al. 2017; Li et al. 2015, 2017; Arnao and Hernández-Ruiz 2017). Melatonin was investigated in alfalfa to affect ethylene and polyamine biosynthesis and metabolism to increase waterlogging tolerance (Zhang et al. 2019; Gu et al. 2020). Melatonin enhances the levels of polyamine by increasing the metabolic flow from arginine and methionine to polyamines and reducing the salt-induced degradation of polyamines (Ke et al. 2018). Melatonin is reported to upregulate the expression of genes in GA biosynthesis, whereas downregulates crucial genes in ABA biosynthesis. The essential gene for GA production, ent-kaurene synthase (KS), and flowering time were both delayed in Arabidopsis thaliana’s melatonin biosynthesis enzyme knockout mutants (snat1 and snat2) (Lee et al. 2019, 2021). Additionally, melatonin therapy raised the GA content in various plant species, such as cucumber, cotton, rapeseed, apple, and pear (Arnao and Hernández-Ruiz 2021). The involvement of melatonin during ABA biosynthesis is a little opposing. In barley seedlings, under drought priming and cold stress conditions, melatonin promoted ABA biosynthesis (Li et al. 2016a, b), whereas it inhibits ABA accumulation in Chinese cabbage by activating the transcription factor ABF (Tan et  al. 2019). Melatonin also reduced the amount of ABA in apple plants by lowering the expression of the ABA synthesis gene (MdNCED3) and raising the levels of ABA catabolic genes (MdCYP707A1 and MdCYP707A2), which in turn blocked stomatal closure (Li et al. 2015). In response to various abiotic stress conditions like salt, drought, heat, and cold, melatonin biosynthesis also affects the biosynthesis and catabolism of ABA-responsive genes, possibly by acting upstream of the ABA pathway (Li et  al. 2015, 2017; Fu et  al. 2017; Arnao and Hernández-Ruiz 2018). Melatonin may function similarly to ABA while seed germination. During seed maturation, accumulation of ABA induces seed dormancy, and high phytomelatonin levels were detected in dry seeds, and decreased during germination. This fact was proved in Arabidopsis, where the exogenous application of melatonin affects endogenous hormone levels during seed germination, and low melatonin concentrations (0–100 μM) do not affect on seed germination, whereas enhanced concentrations reduced the germination rates (Lv et al. 2021). Melatonin inhibits seed germination by crosstalk with abscisic acid, gibberellin, and auxin in Arabidopsis. Therefore, the collaborative action of ABA and melatonin occurs to inhibit seed germination. Melatonin increases innate immunity against infections by regulating the biosynthesis of salicylic acid (SA), jasmonic acid (JA), cytokinin, and brassinosteroid under biotic stress conditions (Weeda et al. 2014; Jibran et al. 2013; Zhang et al. 2017). This may be accomplished by modulating SA and JA signalling cascades (Li et al. 2015; Weeda et al. 2014; Jibran et al. 2013). Melatonin can lessen the harm done by heavy metals and dehydration by sharing a route with SA (through the shikimate pathway; Fig. 3.2) (Wang et al. 2017). Exogenous melatonin increases the expression of genes involved in the SA and JA signalling pathways in Arabidopsis, whereas mutant plants with SA signalling defects showed reduced effects of melatonin administration (Li et al. 2015; Weeda et al. 2014, Jibran et al. 2013). Melatonin may therefore alter the SA and JA pathways to improve innate immunity to pathogen assault. The process still needs to be clarified, though. Melatonin induces the

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production of marker genes that code for pathogenesis-related (PR) proteins through the SA signalling pathway (Jibran et al. 2013). A similar hypothesis has also been proposed during stress tolerance in Hordeum (Yang et al. 2021a, b). Additionally, melatonin changes the metabolism of ET and polyamines to increase alfalfa’s resistance to waterlogging. (Zhang et al. 2019; Gu et al. 2020). Melatonin and ethylene crosstalk is also reported in banana fruits, where ethylene regulates fruit ripening of fruits, and melatonin application could delay by repressing ethylene biosynthesis (Hu et al. 2017). Exogenous application of melatonin can alter the ethylene biosynthesis and signalling genes, where the expression ethylene biosynthesis gene, ACS4, and ethylene signaling-related genes (NR, ETR4, EIL1, EIL3, and ERF2) were enhanced and thereby promoting fruit ripening (Sun et  al. 2015). During normal plant growth and development, the endogenous melatonin levels are extremely low (found in rice, Arabidopsis, and cassava as 0.5 ng/g fresh weight (FW) 0.05 and 0.006 ng/g FW, respectively) (Ye et al. 2017; Wei et al. 2018a, b; Wang et al. 2021), Melatonin is induced in response to external stress conditions (Shi et  al. 2015b; Moustafa-Farag et al. 2020), for instance; melatonin levels rise from 0.5 to 225 ng/g FW in rice leaves upon cadmium treatment (Lee et  al. 2017). Though melatonin affects almost all plant hormones, including auxin, GA, cytokinins, abscisic acid (ABA), ethylene, salicylic acid, jasmonates, and BR under normal conditions and various stresses (Arnao and Hernández-Ruiz 2021); despite being various studies the clear mechanisms underlying the crosstalk between plant hormones and melatonin synthesis is poorly understood. So, probably there must be some complex regulatory networks linking melatonin and plant hormones. Despite mounting evidence of interactions between melatonin and other plant hormones, little is known about the specifics of these processes. As each plant hormone involves the cascade of genes orchestrion in a particular fashion to regulate the biosynthesis and functionality, deciphering the clear signalling, and crosstalk networks from the complicated metabolic processes is a complex process.

3.6 Melatonin in Combating Stress Conditions in the Plants Plants being sessile organisms encounter various environmental stresses throughout their lives. Stress conditions have a negative impact on a plant’s physiological, molecular, and metabolic processes as well as its ability to absorb nutrients and water. They can also disrupt cellular machinery, create membrane disorganization, and diminish photosynthetic efficiency, all of which lead to poor output. Therefore, cells utilize multiple response mechanisms and regulatory responses to mitigate adverse environmental conditions, ensuring their successful survival and reproduction. Along with several well-known bio-stimulants, secondary metabolites, or other defence mechanisms serving to mitigate stress, recently the emphasis on the role of melatonin in executing indispensable responses in stress management came into the picture. Its exogenous application showed to reduce the harmful effects of abiotic stresses. Melatonin controls plant stress responses by either directly limiting the

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formation of reactive oxygen and nitrogen species or by influencing stress-­ responsive pathways because it is a multifunctional molecule that is ubiquitously present in living organisms. Numerous reactive oxygen and nitrogen species, such as the hydroxyl radical, hydrogen peroxide, singlet oxygen, nitric oxide, and peroxynitrite anion, are scavenged by melatonin. By interacting with oxidants, the indole moiety of the melatonin molecule makes it a powerful free radical scavenger. When structurally comparable moieties like benzofurane and naphthalene are substituted, the antioxidant activity of these substances is diminished in comparison to melatonin (Gozzo et al. 1999). Along with this, its exogenous application critically helps to acquire tolerance in plants under varied stress conditions (e.g., to drought, salt, heat, cold, waterlogging, and heavy metal toxicity) by regulating downstream processes (Weeda et al. 2014; Zhang et al. 2015; Moustafa-Farag et al. 2020; Sun et al. 2021). To increase resistance to drought stress, melatonin acts as a priming agent by modulating an essential antioxidant system (the AsA-GSH cycle) by activation of particularly associated genes (APX, MDHAR, and DHAR) (Cui et al. 2017; Tiwari et  al. 2021). MAPKs and transcription factors are also impacted by the administration of melatonin, which increases drought tolerance, in addition to being the key molecules in modifying nitro-oxidative and osmoprotective homeostasis to withstand drought stress in Medicago plants (Sun et al. 2021; Tiwari et al. 2021). Being an excellent scavenger, it interacts with ROS and reduces ROS production under stress conditions, and therefore aids in combating the harmful effects of stress conditions (Arnao and Hernández-Ruiz 2019a). The increased ROS production is likely to be linked with an increase in melatonin synthesis under stress conditions (Arnao and Hernández-Ruiz 2019b). In grapevine and barley under stress conditions, an enhanced concentration of melatonin was detected, which further increased with stress intensity (Arnao and Hernández-Ruiz 2009). High melatonin levels were detected under heat stress in the rice seedlings (Byeon and Back 2016). Under high-temperature conditions, the levels of rice SNAT and ASMT also increased (Byeon and Back 2016). As there is a considerable increase in melatonin biosynthesis on exposure to heat stress, it highlights that melatonin plays an imperative role in escaping these damaging conditions (Hardeland 2016). Moreover, the expression levels of melatonin biosynthesis enzymes were found to be upregulated under heavy metal stress conditions. For instance, in rice seedlings grown under cadmium stress, the gene expression of TDC and T5H was significantly increased (Byeon et al. 2015). Melatonin levels rise in tomato cultivars under cadmium stress due to the direct binding of a transcription factor (HsfA1a) to the promoter of the caffeic acid O-methyltransferase 1 (COMT1) gene (Cai et al. 2017). The transgenic rice seedlings’ high melatonin levels during periods of cold stress indicated increased chlorophyll production, which improves cold stress tolerance (Kang et al. 2011). Moreover, during cold and drought stress, a higher level of 2-hydroxymelatonin indicates its role in plant resistance and stress tolerance (Lee and Back 2016). A variety of biotic and abiotic challenges cause significant ROS generation, which is countered by either directly scavenging ROS or by stimulating a variety of antioxidant enzymes (such as superoxide dismutase, ascorbate peroxidase, and glutathione S-transferase). Melatonin is produced in response to these

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stresses (Zhao et al. 2021a, b; Arnao et al. 2019; Back 2021). For example, high light causes the acceleration of melatonin levels by 38-fold in St. John’s wort (Murch et al. 2000). In response to 10 mM hydrogen peroxide treatment, a sixfold increase in melatonin synthesis was observed in barley roots (Arnao and Hernández-­ Ruiz 2009). Furthermore, bacterial and fungal infections too can induce melatonin synthesis, as proved in Arabidopsis (Shi et al. 2015a, b) and cotton (Li et al. 2019) respectively. In Brassica juncea (L.), low exogenous application (0.1 mM) enhances root growth, while higher melatonin concentration (100  mM) showed inhibitory effects (Chen et al. 2009). Also, low concentration (0.1–0.5 μM) was found to promote the regrowth of the frozen shoots of American elm (Uchendu et  al. 2013). Improved germination of Cucumis sativus (L.) seeds was observed after100 μM melatonin treatment (Zhang et  al. 2013). Exogenous melatonin administration under cold stress alters the expression patterns of a critical gene involved in JA biosynthesis, ClAOC1, and IAA production, ClAMI1 (Chang et  al. 2021; Li et  al. 2021a, b). These enhanced JA and IAA contents help to improve photosynthesis and redox homeostasis (Chang et  al. 2021). As melatonin is well characterised to be involved in normal growth and development processes along with combating stress conditions by defense responses against many biotic and abiotic factors (Arnao and Hernández-Ruiz 2021; Sun et  al. 2021), this participation of melatonin in varied biological processes points towards the fact that similar to animals, plants also possess melatonin receptors and, recently Cand2 has been proposed as a phytomelatonin receptor (Zhao et al. 2019; Wei et al. 2018a, b), however, the clear role is still debated (Lee and Back 2020). Table 3.2 summarizes a few functionally characterised melatonin biosynthesis genes in different plant species under specific stress conditions.

3.7 Conclusion Plants being sessile organisms encounter various environmental stresses throughout their lives. In addition to harming a plant’s physiological, molecular, and biochemical processes, stress conditions can impair nutrient and water intake, cause cellular membrane disorganization, disturb cellular machinery, and lower photosynthetic efficiency, all of which lead to poor yield. Therefore, cells utilize multiple response mechanisms and regulatory responses to mitigate adverse environmental conditions, ensuring their successful survival and reproduction. Along with several well-­ known bio-stimulants, secondary metabolites, or other defence mechanisms serving to mitigate stress, recently the emphasis on the role of melatonin in executing indispensable responses in stress management is evident. Multiple plant species have been used to characterise the essential melatonin biosynthesis enzymes and the complete biosynthetic pathway. It has been demonstrated to modulate gene expression in difficult environments and to ameliorate redox imbalance. Therefore, transgenic studies on melatonin biosynthesis may be useful to improve stress resistance in plants given the significance of melatonin in abiotic stress tolerance in plants.

Malus zumi Mats

Arabidopsis

Hypericum perforatum Cotton (Gossypium)

Solanum lycopersicum

Organism Catharanthus roseus Oryza sativa

MzASMT1 (KJ123721)

GhSNAT5D, GhSNAT11D, GhSNAT13A, GhSNAT2D GhSNAT1D and GhSNAT2A GhSNAT9D, GhSNAT13D, GhSNAT12A GhSNAT1A, GhSNAT3D, GhSNAT6A, GhSNAT7A, GhSNAT7D, GhSNAT1A and GhSNAT3D GhSNAT7A, GhSNAT7D, GhSNAT10D, GhSNAT23D, and GhSNAT25D SNAT2 (AT1G26220)

Reduced melatonin levels in the SNAT2 knockout mutant (snat2) delayed flowering and slowed development. Overexpression of MzASMT1- enhances salt tolerance in transgenic tobacco Overexpression enhances drought tolerance in transgenic Arabidopsis thaliana

Down regulated by melatonin under salt stress Up regulated by melatonin under salt stress

Down regulated by exogeneous melatonin application

Highly expressed in stem and petals Highly expressed in torus

Increased serotonin levels First T5H gene cloned from rice Expresses during the development of tomato fruit Detected in the leaves of the tomato Detected in every tissue tested, indicating a crucial part in the growth and development of tomato plants. Arabidopsis mutant snat displayed salt and drought tolerance after overexpressing HpSNAT1 and HpSNAT2. Highly expressed in leaf

TDC (AK069031) T5H (AK071599) SlTDC1 (Solyc07g054860) SlTDC2 (Solyc07g054280) SlTDC3 (Solyc09g064430)

HpSNAT1 and HPSNAT2

Function/importance First TDC gene cloned from plants

Gene name/GenBank accession no. TDC (J04521)

Table 3.2  A glimpse of some characterised and functionally important melatonin biosynthesis genes in different plant systems

(continued)

Zuo et al. (2014)

Zhuang et al. (2020)

Lee et al. (2019)

Zhang et al. (2022)

Zhou et al. (2020)

Kang et al. (2007a, b) Fujiwara et al. (2010) Pang et al. (2018)

Reference De Luca et al. (1989)

3  Abiotic Stress-Induced Modulation of Melatonin Biosynthesis Accompanying… 61

VvSNAT1

OsASMT1 (AK072740), OsASMT2 (AK069308), OsASMT3

MdASMT1

Vitis vinifera

Oryza sativa

Apple

AtASMT1 (At4g35160)

ASMT

SlASMT

MeASMT2, MeASMT3

OsASMT1 (AK072740)

Arabidospsis thaliana

Strawberry

Tomato

Cassava

Rice

MdASMT11 and MdASMT14

Gene name/GenBank accession no. AeVTDC1

Organism Aegilops variabilis

Table 3.2 (continued) Function/importance Positive role at the early stage of plant resistance to CCN (cereal cyst nematode) infection Overexpression of AeVTDC1 in tobacco led to reduced susceptibility to RKN (root knot nematode) Improvements in salt tolerance and a reduction in oxidative damage were seen in Arabidopsis overexpressed lines. Increased rice ASMT enzyme activity and better drought stress tolerance were achieved by independent overexpression of OsASMT1, OsASMT2, and OsASMT3. Under drought stress, elevated MdASMT1 expression improved stomatal function and water content. MdASMT11 and MdASMT14 probably regulate rootstocks to abiotic stresses AtASMT caused massive melatonin accumulation and synergized with the phytohormone abscisic acid (ABA) to inhibit seed germination in Arabidopsis Exogenous melatonin induced the strawberry ASMT expression and accelerated the ripening of strawberry fruits through the ABA pathway The heat shock protein (HSP) profile and the expression of genes linked to autophagy were both elevated in tomatoes by the overexpression of SlASMT genes. In cassava, MeASMT2 and MeASMT3 work together to bioactivate melatonin and interact with genes involved in autophagy to positively drive dynamic changes in cassava autophagic activity. The first ASMT gene discovered and cloned from recombinant Escherichia coli was rice OsASMT1, whose expression level was increased with ageing and exhibited a strong correlation with melatonin levels. Kang et al. (2011)

Wei et al. (2021)

Xu et al. (2016)

Mansouri et al. (2021)

Lv et al. (2021)

Wang et al. (2022)

Park et al. (2013)

Wu et al. (2021)

Reference Huang et al. (2018)

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Tan XL, Fan ZQ, Kuang JF, Lu WJ, Reiter RJ, Lakshmanan P, Su XG, Zhou J, Chen JY, Shan W (2019) Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-­ mediated abscisic acid biosynthesis and chlorophyll degradation. J Pineal Res 67(1):e12570 Tilden AR, Becker MA, Amma LL, Arciniega J, McGaw AK (1997) Melatonin production in an aerobic photosynthetic bacterium: an evolutionarily early association with darkness. J Pineal Res 22(2):102–106 Tiwari RK, Lal MK, Kumar R, Chourasia KN, Naga KC, Kumar D, Das SK, Zinta G (2021) Mechanistic insights on melatonin-mediated drought stress mitigation in plants. Physiol Plant 172(2):1212–1226 Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152 Uchendu EE, Shukla MR, Reed BM, Saxena PK (2013) Melatonin enhances the recovery of cryopreserved shoot tips of American elm (Ulmus americana L.). J Pineal Res 55(4):435–442 Van Tassel DL, Roberts N, Lewy A, O'Neill SD (2001) Melatonin in plant organs. J Pineal Res 31(1):8–15 Wang P, Sun X, Li C, Wei Z, Liang D, Ma F (2013) Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. J Pineal Res 54(3):292–302 Wang H, Wang H, Shao H, Tang X (2016a) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67 Wang R, Yang X, Xu H, Li T (2016b) Research progress of melatonin biosynthesis and metabolism in higher plants. Plant Physiol J 52:615–627 Wang L, Feng C, Zheng X, Guo Y, Zhou F, Shan D, Liu X, Kong J (2017) Plant mitochondria synthesize melatonin and enhance the tolerance of plants to drought stress. J Pineal Res 63(3):e12429 Wang LF, Li TT, Zhang Y, Guo JX, Lu KK, Liu WC (2021) CAND2/PMTR1 is required for melatonin-conferred osmotic stress tolerance in Arabidopsis. Int J Mol Sci 22:4014 Wang H, Song C, Fang S, Wang Z, Song S, Jiao J, Wang M, Zheng X, Bai T (2022) Genome-wide identification and expression analysis of the ASMT gene family reveals their role in abiotic stress tolerance in apple. Sci Hortic 293:110683 Weeda S, Zhang N, Zhao X, Ndip G, Guo Y, Buck GA, Fu C, Ren S (2014) Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS One 9(3):e93462 Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66(3):695–707 Wei Y, Hu W, Wang Q, Liu W, Wu C, Zeng H, Yan Y, Li X, He C, Shi H (2016) Comprehensive transcriptional and functional analyses of melatonin synthesis genes in cassava reveal their novel role in hypersensitive-like cell death. Sci Rep 6:35029 Wei J, Li DX, Zhang JR, Shan C, Rengel Z, Song ZB, Chen Q (2018a) Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J Pineal Res 65(2):e12500 Wei Y, Liu G, Chang Y, Lin D, Reiter RJ, He C, Shi H (2018b) Melatonin biosynthesis enzymes recruit WRKY transcription factors to regulate melatonin accumulation and transcriptional activity on W-box in cassava. J Pineal Res 65:e12487 Wei Y, Bai Y, Cheng X, Reiter RJ, Yin X, Shi H (2021) Lighting the way: advances in transcriptional regulation and integrative crosstalk of melatonin biosynthetic enzymes in cassava. J Exp Bot 72(2):161–166 Weissbach H, Redfield BG, Axelrod J (1960) Biosynthesis of melatonin: enzymic conversion of serotonin to N-acetylserotonin. Biochim Biophys Acta 43:352–353 Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, Yang F, Li Y, Shi Q (2016) Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front Plant Sci 7:718

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Wu Y, Fan X, Zhang Y, Jiang J, Sun L, Rahman FU, Liu C (2021) VvSNAT1 overexpression enhances melatonin production and salt tolerance in transgenic Arabidopsis. Plant Physiol Biochem 166:485–494 Xu W, Cai SY, Zhang Y, Wang Y, Ahammed GJ, Xia XJ, Shi K, Zhou YH, Yu JQ, Reiter RJ, Zhou J (2016) Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J Pineal Res 61(4):457–469 Yang L, You J, Li J, Wang Y, Chan Z (2021a) Melatonin promotes Arabidopsis primary root growth in an IAA-dependent manner. J Exp Bot 72(15):5599–5611 Yang SJ, Huang B, Zhao YQ, Hu D, Chen T, Ding CB, Chen YE, Yuan S, Yuan M (2021b) Melatonin enhanced the tolerance of Arabidopsis thaliana to high light through improving anti-­ oxidative system and photosynthesis. Front Plant Sci 12:752584 Yang X, Chen J, Ma Y, Huang M, Qiu T, Bian H, Han N, Wang J (2022) Function, mechanism, and application of plant melatonin: an update with a focus on the cereal crop, barley (Hordeum vulgare L.). Antioxidants (Basel, Switzerland) 11(4):634 Ye T, Hao YH, Yu L, Shi H, Reiter RJ, Feng YQ (2017) A simple, rapid method for determination of melatonin in plant tissues by UPLC coupled with high resolution Orbitrap mass spectrometry. Front Plant Sci 8:64 Ye T, Yin X, Yu L, Zheng SJ, Cai WJ, Wu Y, Feng YQ (2018) Metabolic analysis of the melatonin biosynthesis pathway using chemical labelling coupled with liquid chromatography-mass spectrometry. J Pineal Res 66(1):e12531 Yu Y, Bian L, Jiao Z, Yu K, Wan Y, Zhang G, Guo D (2019) Molecular cloning and characterization of a grapevine (Vitis vinifera L.) serotonin N-acetyltransferase (VvSNAT2) gene involved in plant defense. BMC Genomics 20:880 Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo YD (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54(1):15–23 Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo YD (2015) Roles of melatonin in abiotic stress resistance in plants. J Exp Bot 66(3):647–656 Zhang J, Zeng B, Mao Y, Kong X, Wang X, Yang Y, Zhang J, Xu J, Rengel Z, Chen Q (2017) Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean. Funct Plant Biol 44(10):961–968 Zhang Q, Liu X, Zhang Z, Liu N, Li D, Hu L (2019) Melatonin improved waterlogging tolerance in alfalfa (Medicago sativa) by reprogramming polyamine and ethylene metabolism. Front Plant Sci 10:44 Zhang Y, Rui C, Fan Y, Xu N, Zhang H, Wang J, Sun L, Dai M, Ni K, Chen X, Lu X, Wang D, Wang J, Wang S, Guo L, Zhao L, Feng X, Chen C, Ye W (2022) Identification of SNAT family genes suggests GhSNAT3D functional Reponse to melatonin synthesis under salinity stress in cotton. Front Mol Biosci 9:843814 Zhao D, Yu Y, Shen Y, Liu Q, Zhao Z, Sharma R, Reiter RJ (2019) Melatonin synthesis and function: evolutionary history in animals and plants. Front Endocrinol (Lausanne) 10:249 Zhao D, Wang H, Chen S, Yu D, Reiter RJ (2021a) Phytomelatonin: an emerging regulator of plant biotic stress resistance. Trends Plant Sci 26(1):70–82 Zhao D, Yao Z, Zhang J, Zhang R, Mou Z, Zhang X, Li Z, Feng X, Chen S, Reiter RJ (2021b) Melatonin synthesis genes N-acetylserotonin methyltransferases evolved into caffeic acid O-methyltransferases and both assisted in plant terrestrialization. J Pineal Res 71(3):e12737 Zheng S, Zhu Y, Liu C, Zhang S, Yu M, Xiang Z, Fan W, Wang S, Zhao A (2021) Molecular mechanisms underlying the biosynthesis of melatonin and its isomer in mulberry. Front Plant Sci 12:708752 Zhou Y, Liao L, Liu X, Liu B, Chen X, Guo Y, Huang C, Zhao Y, Zeng Z (2020) Crystal structure of Oryza sativa TDC reveals the substrate specificity for TDC-mediated melatonin biosynthesis. J Adv Res 24:501–511 Zhu Y, Gao H, Lu M, Hao C, Pu Z, Guo M, Hou D, Chen LY, Huang X (2019) Melatonin-nitric oxide crosstalk and their roles in the redox network in plants. Int J Mol Sci 20(24):6200

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Zhuang W, Liu T, Shu X, Wang H, Wang Z, Wang T, Zhang F, Qu S (2020) Overexpression of MzASMT 1, a gene from Malus zumi Mats, enhances salt tolerance in transgenic tobacco. Front Plant Sci 11:561903 Zia SF, Berkowitz O, Bedon F, Whelan J, Franks AE, Plummer KM (2019) Direct comparison of Arabidopsis gene expression reveals different responses to melatonin versus auxin. BMC Plant Biol 19(1):567 Zolla G, Heimer YM, Barak S (2010) Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J Exp Bot 61(1):211–224 Zuo B, Zheng X, He P, Wang L, Lei Q, Feng C, Zhou J, Li Q, Han Z, Kong J (2014) Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants. J Pineal Res 57(4):408–417

Chapter 4

Role of Melatonin in Embryo, Seed Development and Germination Kiran Bala

Abstract  Germination and seedling development are regarded as important steps in the successful growth of a new plant. It is a method of reproductive adaptation in terrestrial plants that help to spread their progeny, which can then survive in a dormant state until favorable environmental conditions for further growth of the next generation. Many hormones participate in the whole process. The presence of melatonin in plants is now confirmed. Melatonin (N-acetyl-5-methoxytryptamine) is a signaling molecule with many functions, universally reported in different plant parts and known to play an important role in several physiological mechanisms during unfavourable conditions. Many studies have suggested that melatonin participates in many physiological processes like detoxification of free radicals, signaling molecules, chlorophyll preservation, photosynthesis enhancement, increased root development, and environmental protection. However, as of now, there is no known specific role for melatonin in embryo and seed development. However, few papers address its role in seed germination. The current chapter’s recent advancements in the role of melatonin research in embryos are discussed. Keywords  Melatonin · Seed development · Melatonin and seed germination · N-acetyl-5-methoxytryptamine · Indoleamines · Metabolic regulator · Plant growth regulators · Antioxidants · Photo regulation

4.1 Introduction Embryo development and seed formation have important functions in the life cycle of angiosperm that start with the double fertilization process which leads to the formation of the embryo and endosperm. A seed consists of an embryo and stored food that is used for initial growth after germination. The embryo is surrounded by K. Bala (*) Department of Botany, Swami Shraddhanand College, University of Delhi, Delhi, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_4

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a protective coat in a test known as a testa. Several functions are associated with embryo development in seeds like multiplications, perennation, and dormancy. This process of seed and embryo development occurs in an insulated environment, therefore different from vegetative growth (de Vries and Weijers 2017). The constant undertaking of regulatory mechanisms results in changes like morphogenesis, cell enlargement, accumulation of the reserve food, and finally dehydration with dormancy (Sonia et al. 2011). In higher plants, these events are controlled by interrelated metabolic, cellular, and biochemical events in the life of plants. Several physical and metabolic changes occur during embryo development as well as during seed formation. After fertilization, the zygote undergoes substantial cell division as well as differentiation. It leads to differentiation which further results in the formation of a miniature plant with a root and shoot axis with three major types of tissue vasculature, dermal and ground tissue is formed (West and Harada 1993). Endosperm development is another event that takes place during embryonic development. Nutrient reserve present in endosperm further assists in the development of the embryo. It remains preserved in mature seed or gets consumed in the last phase of seed development depending upon the species (Liu et  al. 2015). Seed undergoes maturation in the last phase of development. After detachment from the mother plants embryo and seed get ready to survive further. During the last stage, reserve material is stored in the seed that helps for survival during germination. Accumulation of reserve either occurs in embryo and endosperm or both. The immature embryo undergoes a change from cell division to cell enlargement because of the accumulation of the reserves. Finally, seeds undergo water loss to achieve a period of dormancy (Finkelstein 2015). Dehydration up to tolerance permits survival with less water (almost 10%). Dormancy varies from species to species. Some species require specific environmental factors such as light or chilling for sprouting whereas, in certain cases, it needs only water to resume growth (Wolny et al. 2018). Another important factor is the germination of the embryo. Metabolic activities are resumed during the germination process. Meristematic activity is restored in embryonic tissues. Embryonic tissue mobilizes the stored food by redifferentiation. During this stage desiccation tolerance is lost and growth for the next generation gets started. So it results in a transition from seed to seedling. Many environmental factors such as illumination, temperature, and moisture influence this activity (Gilbert and Sunderland 2000). This stage is influenced by several external factors like the outer environment and interval of stress sensitivity and ability to survive under adverse conditions (Bensmihen et  al. 2002). Seed germination is one side considered as starting point of plant life on the other side it is the initial phase of plant life’s response towards the external environment. It directly influences the extension and final submission of seedlings. Therefore, seed germination has its own importance. Response to environmental signals is mediated by or interacted with signaling via one or many hormones. However non-hormonal regulation is also there (Shu Kao et al. 2016). Melatonin (N-acetyl-5-methoxytryptamine, MT) is one of the well-known animal hormones also known to be present in the plant system. Melatonin was first discovered in 1958 in the pineal gland (Khadija et al. 2021). The role of melatonin in humans is studied in detail and many functions associated

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with them are elaborated. In humans, it is responsible for the antioxidative activity, circadian rhythms regulation, and control of many metastatic diseases (Grivas and Savvidou 2007; Balabusta et al. 2016). Melatonin was first recognized in 1995 in plants (Wang et al. 2016b). Earlier it was thought that it was synthesized in chloroplasts and mitochondria of plants. Later it was detected in many parts like seeds, roots, and leaves of the plant (Bose and Howlader 2020). In the last few years, it was found in many plant species (Shi et al. 2017). It is attracted by many researchers due to its multiple functions in plants and much information is accumulating about them. So now it is the center of interest to know its possible physiological role in plants. Melatonin has an efficient antioxidative against reactive oxygen and nitrogen species (ROS and RNS, respectively) activity (Murch et  al. 2001a). It protects biomolecules from oxidative stress. Melatonin scavenges H2O2 and OH− and indirectly regulates free radical stealing by increasing the activities of antioxidant enzymes, such as SOD, CAT, POD, and glutathione peroxidase (GPX) (Han et al. 2017). Melatonin involves in root growth (Ren et  al. 2019), photosynthesis (Katarzyna et al. 2017), abiotic stress tolerance (Khan et al. 2020), and fruit ripening (Arnao and Ruix 2018). As a multiple role in animals and plants, MT is also known as an efficient growth regulator in plants (Khadija et al. 2021). It is responsible for energizing several metabolic responses against adverse conditions in various stress systems (Debnath et  al. 2019). Melatonin provides the first line of defense and acts as an internal sensor of oxidative stress in plants. For instance, when we provide Melatonin externally it increases photosynthetic C uptake and improves plant antioxidant activity of organelles under unfavourable conditions (Zhiyo et al. 2017). Several studies have shown that melatonin triggers many responses in plants that help to enhance growth carbon fixation, rooting, seed germination, and defense against several biotic and abiotic stressors. Melatonin can also be known to enhance the starch metabolism and energy used as a result of damage caused by environmental stressors from heavy metals and temperature fluctuations (Maria et  al. 2018). It also works as an important regulator of plant hormone genes such as in the metabolism of indole-3-acetic acid, cytokinin, ethylene, gibberellins, and auxin carrier proteins (Khadija et al. 2021). Many other stress-specific genes are regulated and antipathogenic as well as antioxidative activity making it a more versatile molecule. Studies have shown that melatonin also participates in food ripening (Arnao and Hernandz-Ruiz 2020). Because of the multiple actions of melatonin as its role in plant development, physiological action, and gene expression, it is considered a master regulator. However, information about the effects of Melatonin in embryo, and seed development is limited. The role of melatonin in seed germination under the stress condition in plants is well elaborated in many studies (Xiao et al. 2019; Yu et al. 2021; Cao et al. 2019). Several studies on its physiological and genetic effects on plants have increased interest in them in the past last decade. Studies have demonstrated that a lower concentration of melatonin can enhance the maize plant growth and the germination of cucumber seeds during the cold. In cucumbers, the addition of melatonin to seed results in lateral root formation and seed sprouting under water-stress

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conditions (Cao et  al. 2019). Thus seed along with melatonin improved in seed germination could be due to an enhanced antioxidant system and increased starch metabolism. The hypothesis given by Balzer and Hardeland (1996) suggests the role of melatonin in plants may be similar to its function in mammals as a chemical messenger or an oxidant. Therefore, the objective of this chapter is to study the role of melatonin in embryo and seed development along with seed germination. Additionally, identification of new forms where melatonin may have many possible roles in seed development and maturation in plants.

4.2 Melatonin Production in the Plants Compare to animals it is observed that melatonin reduction in plants is different from production in animals. In plants, melatonin is mainly biosynthesized in mitochondria and chloroplasts (Arnao and Hernandz-Ruiz 2014). A separate group of enzymes is involved in the synthesis of melatonin via different procedures (Bose and Howlader 2020). Melatonin synthesis regulation is enhanced by many external factors such as light, environmental stresses such as ultraviolet-B, drought, cold, and heat (Arnao and Hernandez-Ruiz 2015). Tryptophan is one of the amino acids which is known to precursor of melatonin and biosynthesis of it requires four enzymatic reactions (Zhao 2012). The production of melatonin is a two-way method, so if the melatonin production is blocked in mitochondria it will start in chloroplasts. In plants, it is produced by a specific enzyme M3H (Rock and Quatrano 1995). The reaction starts with tryptophan which gets changed into tryptamine by the enzyme tryptophan decarboxylase (TDC). Further tryptamine is converted into 5-hydroxytryptamine (serotonin) by another enzyme tryptamine 5-hydroxylase (T5H) (Back et al. 2016, Fig.  4.1). This pathway is considered one of the principal biogenesis pathways. In another pathway of synthesis, tryptophan changes into 5-hydroxytryptophan in the presence of tryptophan 5-hydroxylase (TPH) enzyme, and further 5-­hydroxytryptophan changes into serotonin by aromatic-L-amino-acid decarboxylase (TDC/AADC) (Murch et al. 2000). N-acetyl serotonin is generated from serotonin in the presence of serotonin N-acetyltransferase (SNAT) enzyme or arylalkylamine N-acetyltransferase (AANAT) (Shi et al. 2017). N-acetyl serotonin produces melatonin using enzymes N-acetyl-serotonin methyltransferase (ASMT) or hydroxy indole-O-methyltransferase (HIOMT). In addition, N-acetyl-­tryptamine is the catalytic product of tryptamine catalyzed by SNAT but, T5H cannot further convert N-acetyl tryptamine into N-acetyl-serotonin (Fan et al. 2018). By another alternate pathway serotonin is converted into 5-methoxy-tryptamine using the enzyme HIOMT and finally, 5-methoxy-tryptamine is converted to melatonin by catalytic reaction of SNAT enzyme (Arnao and Ruix 2018). Also, a reverse reaction for melatonin biosynthesis was observed, in which N-acetyl-serotonin is catalyzed by N-acetyl-serotonin deacetylase (ASD) to produce serotonin (Lee et  al. 2018). Interestingly, both melatonin and indole-3 acetic acid (IAA) are generated from the

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Fig. 4.1  Biosynthesis pathway of melatonin in plants. The enzyme of the different stages are TDC Tryptophan decarboxylase, T5H Tryptophan-5-hydroxylase, SNAT Serotonin N-acetyl transferase, AANT Arylalkylamine N-acetyltransferase, ASMT N-acetylserotonin methyltrans Ferase, HIOMT Hydroxyindole-O-methyltransferase, AADC Aromatic-Lamino-acid decarboxyl Ase, HIOMT- hydroxyindole-O-methyltransferase

same precursor, tryptophan is catalyzed into tryptamine and IAA produce by indole3-acetaldehyde, which may be participated in multifunctional activities of melatonin in plants (Arnao and Hernandz-Ruiz 2014). A schematic presentation of the melatonin production cycle is explained in Fig. 4.1.

4.3 Melatonin in the Plants The existence of melatonin in plants was first notified in 1995 (Rock and Quatrano 1995). Many studies have shown their presence in edible monocots and dicots plant families (Dubbels et al. 1995; Van Tassel et al. 1995). The presence of melatonin is shown in many plant organs such as stems, leaves, roots, flowers, fruits, and seeds (Arnao et al. 1917; Van Tassel et al. 2001). Intriguingly, compare to animals a high amount of melatonin, has been reported in plants (Nawaz et al. 2016). The endogenous concentration of melatonin is varying in herbs, vegetables, and fruit plants (Cheng et al. 2021; Meng et al. 2017; Tanit et al. 2014). It may be from pictograms to micrograms per gram. Generally, it is high in seeds and leaves whereas in fruits it is the lowest (Burkhardt et al. 2001; Van Tassel et al. 2001). Variations of endogenous melatonin content among different plant species suggest the diversified function of Melatonin from plant to plant (Ying et al. 2021). Many reports have shown that melatonin is present in different horticultural crops and different varieties of foods like grapes, strawberries, tomato (Jibiao et  al. 2018; Sturtz et  al. 2011), banana, bitter gourd, mango, papaya, broccoli, pineapple, black pepper, and cabbage (Arnao and Hernandez-Ruiz 2006). Melatonin extracted from plants is used as a sleep modulator and antidepressant. Some herbs contain a high level of

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melatonin such as (Hypericum perforatum, Tanacetum parthnium (feverfew) and some Chinese medicinal herbs (Simopoulos et al. 2005). Table 4.1 summarises the melatonin identified in different stages of seed embryo development and seed germination. Reports suggest that Melatonin acts as a signaling molecule during seed germination under adverse conditions, however, the underlying basic regulatory mechanisms are largely unknown. Significantly, melatonin concentration is high in

Table 4.1  Studies on melatonin and embryonic studies in the plants Plant seeds Zoysia japonica Stued Maize

Gossypium hirsutum L. Cucumber Zea mays Soybean Arabidopsis thaliana Cotton

Maize Medicago sativa Vicia faba

Function Increase antioxidative capacity in the seed Increase regulatory pathway related to anti-oxidative activity and hormonal activity Decrease CK,ABA,GA Increase germination energy and percentage, seedling strenth index, lent of shoot and root, fresh and dry weights in seedling, K+ content, relative water content, proline and total phenolic contents, superoxide dismutase, catalase and phenylalanine ammonia lyase activities; and significantly decreased mean emergence time, Na + content, Increased hypocotyls length, α-amylase, β-galactosidase, Abscisic acid, GA, Up regulation of the gene of ABA, GA, embryo root development, seed germination in salt stress plant. Increase GSH, Glutathione reductase, protection from oxidative stress induced by chilling stress Increase proteome Photosynthetic rate, 100-seed mass, and total seed mass per plant under water stress Seed viability increase in heat stress. Stimulate root growth at low dose Decrease leaf area at high dose Promote seed germination MDA level decrease Antioxidative enzyme activity increased Reduce ABA content Increase germination potential, root radical, hypocotyl length, antioxidative defence, starch metabolism Enhance seed germination and seed growth Increase plant growth and tolerance

Soybean

Increase plant growth

Wheat

Put out the adverse effect of drought ie germination percentage, index, and potential. –Reduce the negative effect of water stress on germination ie increase radical length, radicle no and plumule length. –Increase lysine content.

References Dong et al. (2021)

Jiang (2016)

Chen et al. (2021) Balabusta et al. (2016) Kołodziejczyk et al. (2016) Zou et al. (2019) Hernandez et al. (2015) Xiao et al. (2019)

Cao et al. (2019) Ruonan Yu et al. (2021) Dawoof and Sadak (2014) Wei et al. (2015) Zhang et al. (2019)

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ripe tomatoes than in unripe ones (Van Tassel et al. 2001; Van Tassel and O’Neil 2001), and melatonin concentrations varied in the seeds of several edible plants (Manchester et al. 2000).

4.4 Early Embryogenesis Two major incidents in the starting of embryogenesis help to initiate the body plan and potentiality of the developing embryo. After double fertilization, the zygote undergoes an asymmetric division indicating its already established polarity (Robert B Goldberg et al. 1994, Souter and Lindsey 2000). The smaller last cell (opposite to the micropyle) produces the maximum part of the embryo and the rudimental cell gives rise to the root apical meristem, a small file of cells that attaches the embryo with maternal tissue and has a nutritive role for the early embryo (Fig. 4.2). The different destinies of embryo and suspensor cells are highly regulated processes (Yuan et al. 2015). Simultaneously with early embryo division, endosperm starts to develop (Berger 2003; West and Harada 1993). The endosperm is the main part of DNA amplification and takes control of the suspensor and acts as a source of nutrients for germinating embryos. The endosperm may continue and accumulate starch, protein, and lipids as reserve food. Studies have shown that concentrations of cytokinin, IAA, and GA increase transiently (Bewley and Black 1994; Rock and Quatrano 1995). Manipulating hormone levels or genetic response and tissue culture studies have shown that cytokinin and GAs are nutritive whereas Auxin has a main role in pattern formation (Schaller and Bishop 2015). In general, the redirection of plant growth is initiated by changes in the relative ratio of plant growth regulators, viz. auxins and cytokinins (Skoog and Miller 1957).

Fig. 4.2  Pattern formation during Arabidopsis embryogenesis. Left to right: 2-cell, octant, heart stage embryos, and seedling. Thick lines: divisions separating apical (a), central (c), and basal (b) embryo regions. HY, hypophysis. The suspensor is a cell file beneath hypophysis. Cell groups that give rise to seedling structures are indicated in the heart-stage embryo. SAM shoot apical meristem, COT cotyledons, H hypocotyl, ER embryonic root, RM root meristem, RMI root meristem initials, QC quiescent center, COL Columella root cap

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Usually, auxins are responsible for polarized growth whereas cytokinins work the opposite of auxin (Saiko Yoshida et al. 2013). A high ratio of auxin to cytokinin stimulates the regeneration of long, thin tissues such as adventitious roots (Jing and Strader 2019), whereas a low auxin to cytokinin ratio enhances the regeneration of the thicker and more isodiametric tissue forms that are affiliated with the shoot (Su et al. 2015). Over the past 45 years, there have been numerous reports of other compounds that modulate the auxin: cytokinin responses (Jasmina et  al. 2018). Thus, various plant responses to auxin hormones are responses to auxin-derived or stimulated biomolecules. Another possible role for melatonin may be in seed development may be associated with auxin. Although research into the role of melatonin in seed development is in its beginning, there are many promising results and interesting new directions which can be perused further. Studies have shown that melatonin performs almost the same functions as auxin i.e. it initiates growth at low concentrations whereas at high concentrations it works opposite of it (Chen et al. 2009). Melatonin not only increases the antioxidant capacity of crops but also promotes growth under adverse conditions (Hardeland 2016; Marta et al. 2016). Very few studies indicate that melatonin promotes seed development and helps to increase yield through a variety of regulatory functions. Melatonin treatment under drought stress improved restored seed growth and yield (Zou et al. 2019; Wei et al. 2015). Exogenous application of melatonin in Arabidopsis prolonged the seed viability under heat stress conditions (Hernandez et al. 2015). Therefore, there are chances that melatonin may be involved either in addition to indole-3-acetic acid, synergistically or antagonistically. Further studies are needed a re-consideration of the traditional systems of plant physiology may provide give some new clues to the part of melatonin that may be independent of other growth regulators, may mediate in coordination with other plant hormones, or may be involved in some other metabolic activities. Observation from the mammalian system may be useful for the further investigation of melatonin in the plant kingdom. In a signal transduction system, a biomolecule binds and stimulates a receptor that is associated with G protein-coupled with an effector protein, therefore stimulating an intracellular secondary messenger cascade resulting in different cellular responses and opening of an ion channel. Hardeland (2016) suggested that melatonin in plants sticks to an intracellular receptor protein along with a GTP binding protein present on the membrane of the acidic vacuole, resulting in increased proton flux. Studies have shown that metabolically melatonin is linked to cAMP and the Ca2+ signal transduction pathways (New et al. 2003). Furthermore, biosynthesis of both melatonin and auxin occurs from common predecessors such as tryptophan and tryptamine (Arnao and Ruix 2018). Melatonin induces growth in the aerial pas well in roots of Triticum, Hordeum, Avena, Oryza, Lupinus, arabidopsis, Brassica, Helianthus, Prunus, Cucumis, and Punica, but also in tomato, soybean, and maize plants (Arnao and Hernández-Ruiz 2017). Melatonin is also known to induce a slight increase in endogenous IAA whereas in untreated plants concentration of IAA is low in Brassica juncea (Chen et al. 2009) and tomato plants (Wen et  al. 2016). Recently studies carried out on melatonin have shown

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altered sixteen auxin-related genes (Shuxin et  al. 2019; Arnao and Ruix 2018). Many of these genes encode important auxin transports and are responsible for the inhibition of root growth and hypocotyl elongation. Increased lateral root development by melatonin could be due to synergistic effects along with Auxin. Another study (Yan et  al. 2021) has shown that melatonin inhibits seed germination in Arabidopsis when the concentration of the same is increased. Further, RNA sequencing studies also support that melatonin-regulated seed germination corresponds to many phytohormones like gibberellin (GA) abscisic acid (ABA), and auxin (IAA). Both ABA and melatonin together decrease seed germination, while GA and auxin opposed the inhibitory effect of seed germination by melatonin. In plants, it appears that melatonin acts as a multi-regulatory molecule, as found in animals. However further studies are needed to understand the mechanism.

4.5 Growth Promotion by GA and CK and Possible Role of Melatonin Cells in suspension are among those cells which remain large and vacuolated (Schwartx et al. 1997). In some cases, cells adjacent to pre-embryo have invaginated with walls that help to increase area and help in the transfer of the material. This property of the suspensor has an important role in the nutrition of early embryos. Studies in culture mediums have shown that gibberellins (GA) replace the function of removed suspensors and promote embryo growth (Finkelstein 2010). It indicates that the suspensor provides GA along with nutrients. Few studies have shown that melatonin is responsible for the upregulation of GA biosynthesis in seedling germination under stress conditions (Han et al. 2017; Katarzyna et al. 2017; Zhang et al. 2014a, b). In Arabidopsis, melatonin acts as a plant growth regulator at low concentrations and maintains seed credibility at high concentrations (Hernandez et  al. 2015). Several studies have confirmed the role of plant melatonin in morphogenesis (Murch et al. 2001b). Another study is shown that ABA catabolism genes are regulated by melatonin treatment and one of the enzymes which are responsible for the down-regulation of NCE, the down-­regulation of synthesis of ABA results in decreased ABA levels during seed germination in salt stress condition (Zhang et al. 2014a). Cytokinin has been involved in promoting suspensor function but may have a significant role in endosperm growth (Bewley and Black 1994). Cytokinin participates in pattern formation as a pattern-forming gene required for pattern formation of vascular tissue encodes a cytokinin receptor. When inhibitors of the transformation from serotonin to melatonin are used, cytokinin-induced organogenesis in the shoot is increased (Murch and Erland 2021). It suggests some unexplored interrelation between them. The inhibitor of serotonin, i.e. p-chlorophenyl alanine, when given to mammal’s system, is responsible to decrease serum serotonin concentration (Yamada et  al. 1999) and when given to plant system decrease the root

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formation in vitro cultures (Murch et al. 2001a, b). Several studies have confirmed the role of melatonin in root formation (Pelagio-Flores et  al. 2012; Liang et  al. 2017; Ren et  al. 2019). Melatonin modulates the function of genes of almost all hormones such as carrier proteins of auxin and has a role in the metabolism of auxins (IAA), cytokinin, abscisic acid, gibberellins, and ethylene (Arnao and HernandezRuiz 2015; Arnao and Ruix 2018). The effect of melatonin on GA and cytokine in seed development needs to be investigated further.

4.6 Pattern Formation and Melatonin Plant hormones are known to participate actively in embryo development. They work in a coordinated manner during the process. Several studies have shown the direct role of Auxin in pattern formation in the developing embryo. In plants, melatonin is known to influence organ development (Arnao and Hernandz-Ruiz 2014, 2015). It is also believed to promote vascular development, the establishment of polarity, and root apical meristem formation (Van Tassel et al. 2001). Since melatonin shares its biosynthetic precursor tryptophan with the hormone auxin. Chemically, melatonin is an indolic compound, and the plant hormone auxin belongs to the indole group (Zhao 2012; Rock and Quatrano 1995). As both are similar chemically as well as in their biosynthetic pathway so it may be possible that they have some potential linkage. Both are synthesized by some common precursors such as tryptophan and tryptamine. IAA synthesis pathway is largely shown by radioactive and biochemical assay but, very less is known about melatonin biosynthesis in plants. But several studies on the melatonin biosynthesis pathway show the interrelation between melatonin and IAA metabolic pathway (Arnao and Hernandez-Ruiz 2006). Studies have shown that melatonin in high concentration suppresses the root meristem by adjusting both syntheses of auxin and polar transport of auxin in Arabidopsis (Wang et al. 2014). It is confirmed in the studies that melatonin is responsible for root formation in embryo and lateral root through the transformation of auxin response in rice (Liang et al. 2015). The measure of endogenous hormone concentration has shown that CK, GA, and IAA are all transiently high during this phase. By regulating ABA and GA, melatonin also increases salt tolerance in cotton seeds by influencing the expression of hormone-related genes in the plant hormone signal transduction system (Chen et  al. 2019). The role of endogenous and exogenous auxin in the regulation of plant morphogenesis but little attention has been paid to alternative pathways of auxin and tryptophan metabolism. Therefore less information is available on regulatory mechanisms during seed development. Both auxin and melatonin promote lateral and adventitious roots and therefore behave the same. Melatonin also influences the expression of IAA response genes (Dong et al. 2021; Murch et al. 2002).

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4.7 Embryo Maturation When developing embryos cease the growth result in seed maturation with an increase in ABA content. During this stage, ABA induces ICK1 resulting in cell cycle arrest during the G1/S transition (Faiza Ali et al. 2021). At the center stage of seed development, there is cell enlargement with an accumulation of lipid bodies (Rodrigo et  al. 2006; Fan et  al. 2018). Further, it leads to the formation of the enlarged cell due to protein and lipid bodies accumulation (Shao et al. 2019; Shibata et al. 2020) at this stage water content decreased. ABA expression is at the peak level when the seed gains maximum weight. Finally, the embryo becomes desiccation tolerant and it loses both water and ABA and becomes inactive. They do not germinate until they get any signal further. Slowly with development, they acquire autonomy and if embryos are removed from the seed are capable of ‘precocious germination’ and even germinate in a simple nutrient medium. With development, their chances for persistence for seedling formation get better. Later food accumulation and other events are important for their generative success. However, their precocious germination suggests some factors are suppressing them and the final stage is not necessary for the germination. Usually, mangroves (Rhizopora mangle) show an interesting pattern of growth. Here they skip normal development. As they are tropical aquatic plants, therefore, water and temperature are favorable to their growth. They germinate while still attached to the maternal plant (vivipary). Many regulators responsible for embryo maturation are studied and tested for their physiological role. ABA and limited water are among the regulators which are responsible for embryo maturation (Mikko et al. 2018). From studies, it’s now clear that ABA concentration gets increased at that age and it is responsible for suppressing germination in mature seeds. ABA deficiency often results in vivipary. During seed maturation, water content gets reduced whereas germination requires water uptake. During the development event of signal transduction goes which is not easy to quantify and manipulate.

4.8 Melatonin and Seed Germination Germination is the process where an embryo starts developing and it usually occurs when conditions favor the growth of the next generation. For this purpose, water is needed, and stored substances within seeds are utilized. Many other events like seed respiration, transcription (mRNA), mitochondrial repair, and multiplication take place during this process (Wolny et al. 2018; Zhang et al. 2014a, b). Many physiological and metabolic processes are needed. In inactive seeds, water hydration is needed to permit germination (Bewley 1997). Dormant seeds are usually inhibited

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due to the hard seed coat which acts as a barrier to uptake and gas exchange and loss of chemicals like ABA (Nonogaki 2017). The specific requirement to break the dormancy varies among species. It is observed that applied GAs can be replaced for light and light appears to increase both GA synthesis and GA sensitivity (Seo et al. 2009; Jiang 2016). Hormones like GA and ABA are involved in seed regulation. At the same time, when melatonin is applied externally, is responsible for the ABA content in the cotton seeds which show a first rise than falling at the germination stage (Chen et  al. 2021). Many studies have shown that exogenous melatonin enhances seed germination (Xiao et al. 2019; Kołodziejczyk et al. 2016; Li et al. 2016; Shuang et al. 2019; Susan et al. 2021). The concentration of ABA increases in the starting and later decreased thereby involved in the seed dormancy. Later germination is promoted by melatonin (Zou et al. 2019). ABA and GA are two plant hormones with inimical effects on seed germination (Chen et  al. 2019). During germination, Melatonin treatment increases GA with seed germination. Therefore, seed germination was accelerated by melatonin (Cao et  al. 2019; Hernandez et al. 2015).

4.9 Conclusion Seed germination is a fundamental process by which species grow from a single seed into a plant that includes the movement of the reserve food material. It is one of the analytical stages in the initiation of the plant life cycle. During germination, it is sensitive to external factors (Weitbrecht et al. 2011). Melatonin is responsible for the promotion of root growth but further studies are needed to investigate its role in the development and seed germination of the seed. Since few reports have been published showing interactions between melatonin and seed development, maturation, and germination. Similarly, very less is known about the effect of melatonin on embryo development. However, melatonin is known to be present in all plants, but how it is synthesized is not very clear. Studies have shown that melatonin resembles auxin in terms of function. Many studies favour it, whereas some are against it. Melatonin has many benefits for plants, especially in stressful conditions. Even exogenous melatonin can reduce the adverse effect of drought on the chlorophyll content of cucumber and maize and increase the photosynthetic rate (Wang et al. 2016a, b: Ye et al. 2016). Under drought conditions, melatonin also increases the chlorophyll content in soybean leaves during different stages of seed development (Zou et al. 2019). In the same conditions, melatonin maintains the photosynthetic gas exchange parameters and high photosynthetic levels. As a result of it, photosynthetic electron transport and assimilatory capability are maintained at a high level (Liu et al. 2015). More detailed investigations should be done regarding the feasible roles of melatonin in seed development and its interaction with other hormones during seed germination.

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Ren S, Rutto L, Katuuramu D (2019) Melatonin acts synergistically with auxin to promote lateral root development through fine tuning auxin transport in Arabidopsis thaliana. PLoS one 14(8):e0221687. https://doi.org/10.1371/journal.pone.0221687 Rock C, Quatrano R (1995) The role of hormone during seed development. In: Davies PJ (ed) Plant hormones; physiology, biochemistry and molecular biology, 2nd edn. Kluwer Academic Publishers, Norwell, pp 671–697 Rodrigo MP, Siloto KF, Lopez-Villalobos A, Edward C, Nykiforuk C (2006) The accumulation of Olosins determines the size of seed oil bodies in Arabidopsis. Plant Cell 18:1962–1974 Schaller E, Bishop A, Kieber JJ (2015) The yon yan of hormones-Cytokinin and Auxin interactions in plant development. Plant Cell 27:1. https://doi.org/10.1105/tpc.114,133595 Schwartx B, Vernon D, Dw M (1997) Development of the suspensor, differentiation, communication and programmed cell death during plant embryogenesis. In: Larkins BA, Vasil IK (eds) Cellular and molecular biology of plant seed development. Kluwer Academic Publishers, Dordrecht Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone in germinating seed. Plant Mol Biol 69:4,63–4,72 Shao Q, Liu X, Su T, Ma C, Wang P (2019) New insights into the role of seed oil body protein in metabolism and plant development. Front Plant Sci 10:1568 Shi H, John L, Wei H (2017) Melatonin in plants. Front Plant Sci 8:1666 Shibata M, Coelho CMM, Steiner N, Block JM, Maraschin M (2020) Lipid protein and carbohydrate during seed development. Cerne 26:2–309 Shuang X, Liantao LD, Wang H, Li D et al (2019) Exogenous melatonin accelerates seed germination in cotton (Gossypium hirsutum L.). PLoS One. https://doi.org/10.3371/jounal. pone.0216575 Shuxin R, Laban R, Dennis K (2019) Melatonin acts synergistically with auxin to promote lateral root development through fine tuning auxin transport in Arabidopsis Thaliana. PLoS One. https://doi.org/10.1371/jounal.pone.0221687 Simopoulos AP, Tan DX, Manchestor LC, Reiter RJ, Purslane (2005) A plant source of omega-3 fatty acid and melatonin. J Pineal Res 39:331–332 Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symp Soc Exp Biol 11:118–130 Sonia B, Steffen K, Laux T (2011) Embryonic development in Arabidopsis thaliana; from the zygote division to the shoot meristem. Front Plant Sci 07 Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51:971–983 Sturtz M, Cerezo AB, Cantos-Villar E, Garcia-Parrilla MC (2011) Determination of the melatonin content of different varieties of tomatoes (Lycopersicon esculentum) and strawberries (Fragaris ananassa). Food Chem 127:1329–1334 Su YH, Liu YB, Bai B, Zhang XS (2015) Establishment of embryonic shoot root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front Plant Sci 5:792 Susan MJ, Lauren A, Erland E (2021) A systematic review of melatonin in plants; an example of evolution of literature. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.683047 Tanit P, Jeffrey J, Autcharaporn S, Suppachai T (2014) Determination of melatonin content in traditional Thai herbal remedies used as sleeping aids. J Pharm Sci 22:6 Van Tassel DL, O’Neill SD (2001) Putative regulatory molecules in plants: evaluating melatonin. J Pineal Res 31:1–7 Van Tassel DL, Roberts NJ, O’Neill SD (1995) Melatonin from higher plants; isolation and identification of N-acetyl-5-methoxytryptamine. Plant Physiol 108S:101–819 Van Tassel DL, Roberts N, Lewy A, Sd ON (2001) Melatonin in plants organ. J Pineal Res 31(1):8–15 Wang P, Sun X, Xie Y, Li M, Chen W, Zhangs et al (2014) Melatonin regulates proteomic changes during leaf senescence in Malus hupenhens. J Pineal Res 57, 291–307. https://doi.org/10.1111/ jpi.12169 Wang LY, Liu JL, Wang WX, Sun Y (2016a) Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 54:19–27

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Wang R, Yang X, Xu H, Li T (2016b) Research progress of melatonin biosynthesis and metabolism in higher plants. Plant Physiol 52:615–627 Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH et al (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707 Weitbrecht K, Muller K, Leunbner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62(10):3289–3309 Wen D, Gong B, Sun S et al (2016) Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signalling. Front Plant Sci 7:718 West MAL, Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell 5:1361–1369. https://doi.org/10.2307/3869788 Wolny E, Betekhtin A, Rojek M, Braszewska Zalewska A, Lusinska J, Hastrock R (2018) Germination and the early stages of seedling development in Brachypodium distachyon. Int J Mol Sci. 19(10):2916 Xiao S, Liu L, Wang H, Li D, Bai Z, Zhang Y et al (2019) Exogenous melatonin accelerates seed germination in cotton (Gossypium hirusutum L). PLoS 14(6):e0216575 Yamada S, Harano M, Annoh N, Nakamura K, Tanaka M (1999) Involvement of serotonin 2A receptors in phencyclidine-induced disruption of prepulse inhibition of the acoustic startle in rats. Bio Psychiatry 46(6):832–838 Yan F, Wei H, Ding Y, Li W, Chen L, Ding C et al (2021) Melatonin enhances Na+/K+ homeostasis in rice seedlings under salt stress through increasing the root h+/− pump activity and Na+/K+ transporters senstivity to ROS/RNS. Environ Exp Bot 182:104328. https://doi.org/10.1016/J. envexpbot.2020.10430 Ye J, Wang SW, Deng XP et al (2016) Melatonin increased maize (Zea mays L.) seedling drought tolerance by alleviating drought-induced photosynthetic inhibition and oxidative damage. Acta Physiol Plant 38:48 Ying Z, Guo MJ, Song JB, Zhang SY, Guo R, Hou DR, Hao CY, An HL, Huang X (2021) Roles of endogenous melatonin in resistance to Botrytis cinerea infection in an Arabidopsis Model. Front Plant Sci Yoshida S, Saiga S, Wieners D (2013) Auxin regulation of embryonic root formation. Plant Cell Biol 54(3):325–332 Yu R, Zuo T, Diao P, Jiabin F, Fan Y, Wang Y, Zhao Q, Ma X, Lu W, Li A, Wang R, Yan F, Li P, Niu Y, Wuriyanghan H (2021) Melatonin enhances seed germination and seedling growth of Medicago sativa under salinity via a putative melatonin receptor. Plant Sci 12:702875. https:// doi.org/10.3389/fpls.2021.702875 Yuan L, Li X, Zhao J, Tang X, Tian S, Chen J, Shi C, Wang W, Zhang L, Feng X, Sun M-X (2015) Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis. PNAS 112(40):12432–12437 Zhang HJ, Zhang N, Yang RC et  al (2014a) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res 57:269–279 Zhang N, Zhang HJ, Zhao B et al (2014b) The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. J Pineal Res 56:39–50 Zhang Z, Guo L, Sun H, Jinhua W, Liu L, Wang J, Wang B, Wang Q, Sun Z, Li D (2019) Melatonin increases drought resistance through regulating the fine root and root hair morphology of wheat revealed with RjizoPot. Agronomy 13(7). https://doi.org/10.3390/agronomy13071881 Zhao YD (2012) Auxin biosynthesis-a simpler two step pathway converts tryptophan to indole-­3-­ Acetic acid in plants. Mol Plant 5:334–338 Zhiyo Z, Luying S, Tianyu W, Mi P, Xiancan Z, Shengqun L, Fengbin S, Hanping M, Li X (2017) Melaton improves the photosynthetic carbon assimilation and antioxidative capacity in wheat exposed to nano-ZnO stress. Molecule 22:10–21 Zou JN, Jin XJ, Zhang YZ, Ren MC, Wang MX (2019) Effects of melatonin on photosynthesis and soybean seed growth during grain filling under drought stress. Photosynthetica 57(2):512–520

Chapter 5

Melatonin Metabolism in Seeds: Physiological and Nutritive Aspects Anita Thakur

Abstract   Melatonin plays an important role in various physiological responses as a possible plant master regulator. It was first discovered in animal tissues but was later on identified in plants and named phytomelatonin. Melatonin is involved in mediating responses to many different biotic and abiotic stresses by reducing the negative impacts of the stressors. It also improves the plant responses by increasing their stress tolerance to these stresses. Melatonin has been identified in the leaves, flowers, and seeds of the plants. Seeds are the progenitors of the next generation. Melatonin is involved in playing an important role in modulating various physiological and biochemical processes during seed development and germination. The physiological concentrations of melatonin in the seeds studied in various plants range from 2 to 200 ng/g dry weight. White and black mustard seeds reported the highest concentrations of melatonin. This level of physiological concentrations of melatonin is much higher than the known concentrations in the blood of many vertebrates. Melatonin presence in seeds may be essential in protecting germ and reproductive tissues of plants from oxidative damage due to ultraviolet light, drought, extremes in temperature, and environmental chemical pollutants as the seed is highly susceptible to oxidative stress and damage. This establishes the role of melatonin as a free radical scavenger and an important component of the antioxidant defense system. Consumption of melatonin-rich foods increases blood melatonin concentrations, thereby increasing the antioxidative capacity of this blood as reflected by augmentation of Trolox equivalent antioxidant capacity and ferric-­ reducing ability of serum values. A search for melatonin as a health-related phytochemical is finding a new arena for research as a possibility of modulating blood melatonin levels in mammals through the ingestion of plant-derived foods. Keywords  Melatonin · Orthodox seeds · Trolox equivalent antioxidant capacity · Ferric-reducing ability of serum

A. Thakur (*) Department of Botany, Acharya Narendra Dev College, New Delhi, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_5

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5.1 Introduction: Melatonin and Seed Development Melatonin (N-acetyl-5-methoxytriptamine) is an indolamine primarily discovered in 1958 in extracts from the bovine pineal gland. It was first isolated and identified in 1960 by Lerner (Lerner et al. 1960). Melatonin was dubbed as such for its capacity to consolidate melanin pigment in the chromatophores of frog and fish skin. Plants produce melatonin in different anatomical districts. The term phytomelatonin was proposed in 2004 to discriminate plant melatonin from melatonin produced by other organisms (Murch and Erland 2021). Tryptophan is the precursor of melatonin biosynthesis. It is synthesized in plants via the shikimate pathway. All aromatic amino acids in plants are synthesized through this pathway (Mannino et al. 2021). There are six enzymes known to be biosynthesizing melatonin tryptophan. This indicates the presence of multiple biosynthetic pathways for the synthesis of melatonin in plants (Mannino et al. 2021). Seed development is a process involving events from ovule fertilization to physiological maturity. This process can be divided into four phases according to Phases I and II comprising cell division and expansion. In Phase III, reserve accumulation occurs and there is a rapid increase in seed dry mass. Phase III is followed by Phase IV which is marked by the intensified moisture loss from the seed. Following fertilization, the seed structure is formed by the process of cell division, expansion, and differentiation. The process results in the formation of seed structure primordia. At this point, future embryo parts can be visualized. The embryonic cells receive assimilates from the parent resulting in a significant increase in seed size (Bareke 2018). Seeds’ moisture content remains constant and high though out this period of growth. As the seed approaches maturity, the seed witnesses a significant decrease in seed moisture content. The seed also experiences changes in cell membrane structure organization and an increase in enzyme synthesis to prepare for successful germination. Maternal and filial tissue systems that are highly organized and heterogenous result in developing seeds. Embryo development is marked by the differentiation of filial tissue from the meristem. For both monocots and dicots, the ovule moisture content at the time of fertilization is roughly 80% (fresh weight basis). Water serves as the medium for transferring nutrients from the parent plant to the growing seeds, so it stays relatively high for the majority of the maturation period. However, this value rapidly decreases during maturation in both monocots and dicots. Until the hygroscopic equilibrium is attained, the decrease in moisture content continues. Initially, due to slow dehydration, the dry weight of the seed is less and it starts accelerating till it reaches maturity; at that time, seeds possess 35–55% moisture content for orthodox monocot and dicot seeds, respectively, produced in orthodox fruits. However, the moisture content of seeds produced in recalcitrant fleshy fruits decreases less slowly than seeds produced in conventional fruits. Recalcitrant seeds, which typically have moisture contents of over 60% (fresh weight basis), do not exhibit noticeable

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changes in desiccation or an increase in the dry weight of the seed at the end of maturation (Baroux et al. 2002). After gametic fusion, the developing seeds show an increase in weight owing to nutrient accumulation and water uptake. Because cell division and elongation are occurring frequently at this stage, seed filling is initially slow. Soon after, seeds begin to accumulate more dry mass until they reach their highest dry weight. For both monocots and dicots, the ovule moisture content at the time of fertilization is around 80% (fresh weight basis). Water is the means through which nutrients are transported from the parent plant to the developing seeds, therefore although its value declines during maturation, it stays quite high for the majority of the duration. This indicates that the initial phase of dehydration is slow, and is accelerated as the seed approaches maturity. For orthodox monocot and dicot seeds, the moisture content ranges from 35% to 55% at that time, respectively. A decrease in moisture and an increase in the dry weight of the seed content proceed until hygroscopic equilibrium is attained. Moisture content changes from this point on are associated with variations in relative humidity. In comparison to its final seed size, the fertilized ovule is a minuscule structure. Low illumination is less of an issue for big-seeded plant life due to their richer vitality resources including protein and fatty substances, alongside evolutionary superiority. Large seeds, however, typically result in fewer seeds per bloom or fruit. Additionally, due to the weight of the seed, large seeds cannot be physically carried by small plants, which may help partially explain the correlation between plant and seed size. Following sexual fusion, nutrient buildup, and water intake lead to an increase in seed filling. Because cell division and elongation are taking place at this stage, seed fill initially moves slowly. Maximum molecular and biochemical activity is shown during the seed-filling stage, with improved protein synthesis and increased enzymatic activity. It is marked by high metabolic activity, synthesis, and accumulation of nitrogenous and carbon storage compounds which are important for the initial phase of seed germination and seedling growth. Various plant species exhibit a wide range in the relative proportion of storage elements in seeds. For example, Glycine max seeds contain approximately 40% protein and 20% oil. In contrast, seeds of Brassica napus contain approximately 15% protein and 40% oil. Soon after, seeds begin to accumulate more dry mass until they reach their highest dry weight. When desiccating during the maturation phase, “Orthodox seeds” have many oil bodies with smaller diameters than “recalcitrant seeds,” which have more and smaller oil bodies. Lipid bodies are primarily found in the seeds and embryo axis of exalbuminous seeds (such as sunflower seeds) (Thakur and Bhatla 2015). Recalcitrant seeds typically lack this maturation during the germination transition period. Oilseed plants have a large concentration of lipid reserves in their seeds, which protect them from lipid oxidation and hydrolysis until seed germination. In conclusion, cell division, cell expansion, and accumulation of storage products all occur sequentially and gradually during the process of seed development.

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5.2 Melatonin Content in Seeds Melatonin is an indole derivative of tryptophan which was considered unique to the pineal gland. The brain releases this hormone in response to darkness. It helps with the timing of your circadian rhythms. Much of the research on melatonin has centered around its presence in vertebrates (Lerner et al. 1958). However, melatonin has been identified in a variety of other tissues (Huether 1993) and every kingdom including Monera (Rhodospirillum rubrum), Protista (Gonyaulax polyedra), Fungi (Saccharomyces cerevisiae), and Plantae (Manchester et al. 2000). The discovery of large amounts of melatonin in two so-called medicinal herbs, feverfew and St. John’s wort has heightened the interest in the presence of melatonin in plants (Murch and Simmons 1997). High-performance liquid chromatography (HPLC) has helped in identifying melatonin in several edible plants, including tomatoes, rice, oranges, apples, banana, and cabbage (Hattori et  al. 1995). These initial discoveries have led scientists to concern themselves with the extent of the distribution of melatonin in plants. The physiological concentrations of melatonin were observed in different seeds per gram of dry weight (Table 5.1) and the highest concentrations of melatonin were observed in white and black mustard seeds (Manchester et al. 2000). These melatonin concentrations are much higher than the known physiological concentrations in the blood of many vertebrates. Melatonin is an important component of the antioxidant defense system owing to its free radical scavenging nature (Reiter 1998) Therefore, higher levels of melatonin in seeds may be a sign that it is crucial for preventing oxidative damage to plant reproductive and germ tissues brought on by a variety of factors such as drought, temperature extremes, and environmental chemical pollutants. Table 5.1  Melatonin contents reported in seeds of different edible plants. (Manchester et al. 2000) Plant name Silybum marianum Papaver somniferum Pimpinela anisum Coriandrum sativum Apium graveolens Linum usitatissimum Elettaria cardamomum Medicago sativum Foeniculum vulgare Helianthus annus Prunus amygdalus Trigonella foenum-graceum Lycium barbarum Brassica nigra Brassica hirta

Melatonin content (ng/g dry seed) 2 6 7 7 7 12 15 16 28 29 39 43 103 129 189

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Fig. 5.1  Figure illustrating the biosynthesis of melatonin in plants from its precursor and subsequent physiological roles of melatonin in plants. L-tryptophan is a precursor for the synthesis of melatonin. Serotonin is formed by a two-step conversion of l-tryptophan. First, l-tryptophan is hydroxylated to 5-hydroxy serotonin by tryptophan hydroxylase (TPH), which in turn is carboxylated by tryptophan decarboxylase (TDC) to yield serotonin. Melatonin is produced by a two-step enzymatic conversion of serotonin. Serotonin is first converted by N-acetyltransferase, which replaces its hydrogen at the C3 position with N-acetyl-2-aminoethyl. Subsequently, it is methylated at the hydroxy position Melatonin is involved in modulating and regulating many physiological responses in plants ranging from seed germination and seed developmental aspects to seed dormancy. It also confers defense against several biotic and abiotic stresses by regulating the levels of ROS and ROS-scavenging enzymes in plants. Melatonin is a spotlight biomolecule in perceiving circadian rhythms and acting as a flowering and fruit ripening regulator by regulating various elements related to the redox network or interfering with other phytohormones

The primary function of melatonin in plants may involve scavenging free radicals and defending reproductive and germ tissues from biological and chemical assaults (Fig. 5.1). Therefore, it may be necessary for melatonin to be present in seeds, fruits, and flowers in high concentrations to counteract the harm caused by the production of free radicals as a result of reactive intermediates, toxins, and pollutants.

5.3 Melatonin Accumulation During Seed Dormancy and Germination Two major physiological processes that have a significant impact on how seed plants adapt and survive are seed dormancy and seed germination (Yan and Chen 2020). Seed habit is a landmark event for flowering plants as they can disperse their progeny by producing seeds. Regarding the higher plant’s ability to survive as a

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species, the seed stage is crucial. Orthodox seeds develop desiccation tolerance during seed production as an adaptive defense mechanism, and they remain in a dormant, dehydrated state for a certain amount of time until the environment is favorable for the growth of the next generation (Finkelstein 2010). This arrested state of seeds is referred to as seed dormancy. Seed dormancy is defined as a quiescent or resting phase of a viable seed that is unable to germinate under favorable conditions (Finch-­ Savage and Leubner-Metzger 2006). Seed dormancy is instrumental in preventing preharvest sprouting and optimizing seedling establishment. Seed maturation results in the establishment of seed dormancy (Chahtane et al. 2017). The dormancy level gradually rises and reaches a maximum in newly matured seeds during this phase (Karssen et al. 1983). After additional dry storage, seeds gradually lose their dormancy, allowing them to control when to germinate by sensing and integrating a variety of environmental cues (Donohue et al. 2005). Breaking seed dormancy determines the timing of seed germination. The mother plant’s most important environmental cues are humidity and temperature, which have a significant impact on how deeply seeds are dormant. Seed germination happens when dormant seeds are imbibed in a favorable environment. Another significant developmental stage in a plant’s life cycle is seed germination, which determines whether the plant will survive afterward (Finch-Savage and Leubner-Metzger 2006). Seed germination results in the conversion of static seeds into actively growing seedlings. Seed germination can be divided into three major phases: Phase I of seed germination is characterized by rapid water uptake; Phase II by a plateau in water uptake; and Phase III by a restart of water uptake accompanied by radicle protrusion (Bewley 1997). Phases I and II are considered to be germination strictly speaking, while Phase III is considered to be post germination. The resumption of vital processes like transcription, translation, and DNA repair are the first indicators of germination. Cell elongation and eventually cell division are shown when the radicle protrudes (Barroco et  al. 2005; Masubelele et al. 2005). Physically, germination is a two-step process that starts with testa rupture and ends with endosperm rupture. Germination is complete when the emerging radicle ruptures the micropylar endosperm. To accurately forecast seasonal information, seeds must sense and integrate a variety of environmental signals to ripen at the proper time. (Bewley 1997). Numerous internal factors and environmental cues collectively affect seed dormancy and germination potential. The environment influences whether seeds remain dormant or begin to germinate by acting as a signal input. These factors include water content, light intensity, ambient temperature, and nitrogen availability. The three most important environmental variables that have a significant impact on seed dormancy and germination are light, temperature, and nitrogen availability. Melatonin is an indoleamine (N-acetyl-5-methoxytryptamine) occurring in evolutionarily distant organisms which reflects the conservative nature of this molecule (Hernández-Ruiz and Arnao 2008). It has been found across various groups of bacteria, algae, vascular plants, invertebrates, and vertebrates (Murch and Saxena 2002a, b; Hardeland and Poeggeler 2003). In 1958, Lerner et  al. determined the chemical structure of melatonin and discovered that it shared structural similarities

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with other significant compounds like tryptophan, serotonin, and indole-3-acetic acid (IAA). Since that time, melatonin biosynthesis and decomposition in vertebrates have been extensively researched and well-documented. Melatonin in the plant kingdom was first detected in the photosynthesizing alga Gonyaulax polyedra and then in vascular plants. The occurrence of this indoleamine till now has been widely reported in many edible plants and herbs (Hernández-Ruiz and Arnao 2008). The amount of melatonin per gram of fresh fruits, plants, and food products varies from nanograms to picograms (Table  5.1) (Reiter 1998; Hernández-Ruiz 2006; Hernández-Ruiz and Arnao 2008; Posmyk et al. 2009a, b). Additionally, melatonin was found and measured in a variety of plant organs, including roots, shoots, leaves, flowers, fruits, and seeds. Melatonin (N-acetyl 5-methoxytryptamine) plays a very potent regulatory role in plant growth and reproduction. Growing evidence suggests that melatonin is important for plant growth and development by increasing resiliency to biotic and abiotic stresses and doing so by controlling a variety of biological functions (Li et al. 2019). As a non-toxic substance of natural origin that can enhance and stimulate plant health (Kołodziejczyk and Posmyk 2016; Janas and Posmyk 2013) melatonin is regarded as a stimulator. The endogenous melatonin content of plants varies not only across the species but also among varieties of the same species. Through genetic modification, these endogenous levels can be altered (Byeon and Back 2014). The highest concentrations of this compound were found in reproductive organs, especially seeds, which may be related to its function in the process of seed germination, according to an analysis of the endogenous melatonin contents in various plant organs and seeds (Hernández-Ruiz and Arnao 2008). Zea mays, Cucumis sativus, Brassica oleracea, and Vigna radiata seeds were treated with melatonin to encourage seed germination and seedling growth in stressful environments (Kołodziejczyk et al. 2015; Janas et al. 2009; Szafrańska et al. 2014; Posmyk et al. 2009a, b). Investigations have proved that MT also plays a promoting role in seed germination in normal as well as stress conditions (Jiang 2015). Zhang in 2016, reported the significant stimulation of germination of cucumber seeds by external MT treatment. It can enhance the germination of cucumber seeds by promoting ABA catabolism and GA synthesis, reducing the inhibition of seed germination by various substances, promoting the metabolism of storage materials (globulin) in seeds, and the production of the cytoskeleton (microtubules and filaggrin), promoting cell division and elongation, and finally promoting seed germination. According to experiments, melatonin may help break the dormancy of kiwi seeds and encourage germination (Shen et al. 2019). Picograms to micrograms of melatonin per gram of plant material are found in various plant organs. In general, melatonin levels are highest in seeds and leaves and lowest in fruits. The highest concentrations of melatonin have been reported in reproductive organs, particularly in seeds. Sunflower seeds’ melatonin levels have previously been found to rise as they sprout (Cho et al. 2008). Melatonin in seeds may function as a significant antioxidant and efficient free radical scavenger because the germ tissue is highly susceptible to oxidative injuries. Melatonin may therefore be crucial for preventing oxidative damage to plant reproductive and germ tissues (Tan 1993).

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5.4 Melatonin in Survival and ROS Scavenging in Plants Multiple investigations on the role of melatonin in plants have proposed that melatonin plays different physiological roles in plants (Table 5.2). For example, some studies have demonstrated the role of melatonin as a growth promoter, in a similar way to the plant hormone indole-3-acetic acid (IAA) (Arnao and Hernández-Ruiz 2013). Melatonin also functions as a rooting agent in various plant species like cucumber, cherry, and rice (Zhang et al. 2013; Sarropoulou et al. 2012; Park and Back 2012) where it not only shows some similarities with IAA but also has important peculiarities in its action (Pelagio-Flores et al. 2012). Due to its useful properties as a scavenger of free radicals, particularly reactive oxygen and nitrogen species, many studies have concentrated on the role of melatonin as a cytoprotective and abiotic stress protector (Galano et al. 2011; Tan et al. 2000). In this regard, some noteworthy instances include the apoptotic prevention provided by melatonin in cultured carrot cells, the delay in senescence brought about by melatonin in barley, rice, and apple leaves, and its obvious protective role against chemical stresses. Several articles have reported the cellular protective role of exogenous melatonin. For example, the reduction in copper toxicity by melatonin has been described in red cabbage (Brassica oleracea rubrum) (Posmyk et al. 2008). Also, Tan et al. (2007) demonstrated that melatonin added to soil enhanced the tolerance and survival of pea plants (Pisum sativum L.) against copper contamination, indicating that the presence of melatonin in plants can be used for phytoremediation purposes. The role of melatonin in traditional medicinal practices dates back a long time. Melatonin in medicinal herbs has been used not only as a sleep modulator to correct human sleeping disorders but also as an anti-depressant or to combat jet lag. As is the case with Hypericum perforatum (St. John’s wort), Tanacetum parthenium (feverfew), Table 5.2  Various physiological effects of Melatonin observed in different plants Plant studied Triticum aestivum

Observed effect of melatonin on the plant Reference Melatonin as growth promoter in coleoptiles Hernandez-Ruiz et al. (2005) Avena sativa Melatonin as growth inhibitor in roots Hernandez-Ruiz et al. (2005) Hordeum vulgare Melatonin as growth inhibitor in roots Hernandez-Ruiz et al. (2005) Phalaris canariensis Melatonin as growth inhibitor in roots Hernandez-Ruiz et al. (2005) Lupinus albus Melatonin as growth promoter Hernandez-Ruiz et al. (2004) Daucus carota Effect of exogenous melatonin as protector Lei et al. (2004) Hypericum Melatonin in flower development Murch and Saxena perforatum (2002a, b) Pharbitis nil Melatonin in different photoperiods Van Tassel et al. (2001) Chenopodium Effect of exogenous applied melatonin in Kolar et al. (2003) rubrum flowering

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and some Chinese medicinal herbs, some herbs—whether medicinal or not—present high levels of melatonin, in the order of g/g dry weight (Arnao and Hernández-­ Ruiz 2006). Melatonin’s ability to neutralize biological free radicals like reactive oxygen (hydroxyl radical, singlet oxygen, peroxyl radical, and hydrogen peroxide) and nitrogen species (peroxy nitrite anion and nitric oxide) through its antioxidant activity is a crucial physiological property. Not only does the melatonin molecule have anti-oxidative properties, but its intermediate products also do (Van Tassel et  al. 2001; Reiter et  al. 2001). These products also have significant synergistic effects with other antioxidants like ascorbic acid and glutathione. Melatonin stimulates the expression of RbOHs, which produce O2•−, as well as SOD, which raises the levels of H2O2.

5.5 Melatonin Mediated Modulation of Biochemical Constituents/Nutritive Value in Seeds The primary defense mechanism against internal and external oxidative stressors in plants is melatonin. Popular drinks like coffee, tea, wine, and beer, as well as crops like corn, rice, wheat, barley, and oats, have been found to contain startlingly high levels of melatonin (Tan et al. 2012). Plant foods such as nuts are with the highest content of melatonin. Melatonin can also be found in small amounts in some types of mushrooms, cereals, and seeds or legumes that have been germinated. These products are regularly consumed by billions of people worldwide. It is important to take into account the melatonin’s positive effects on human health that result from consuming these products. The ability of melatonin to boost crop production is also supported by evidence. Melatonin’s functions in photosynthesis, root development stimulation, and chlorophyll preservation may be part of the mechanisms. Increased melatonin levels in transgenic plants may result in innovations that boost agricultural crop production and enhance human health in general. In a study, it was documented that increased melatonin levels in the blood after walnut consumption positively correlates with an increased total antioxidant capacity of the serum as reflected by an increase in TEAC and FRAP (Reiter et al. 2005a, b). Therefore, it has been demonstrated that changes in blood melatonin concentrations in mammals, including humans, strongly correlate with changes in the blood’s capacity to eliminate harmful free radicals and related reactants (Benot et al. 1998, 1999). Along with direct protective actions against oxidative damage to the cardiovascular system, melatonin has been shown to synergize with other antioxidants, e.g., vitamin E, which are found in walnuts (Morreale and Livrea 1997; Gitto et al. 2001; López-Burillo et al. 2003). Along with melatonin’s beneficial actions on the heart, it is also involved in decreasing the initiation of cancer by limiting oxidative damage of DNA (Qi et al. 2000). Melatonin further curtails the growth of tumors once they are established. Melatonin achieves these actions by several means including inhibiting the uptake of growth factors such as ω-6 fatty acids by cancer cells (Reiter 2004). Additionally, phytomelatonin, such as that found in walnuts, has been

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suggested as a potential way to slow the growth of tumors that have already developed (Blask et al. 2004). It has been shown that eating melatonin-rich foods significantly increases the concentration of melatonin in human serum. Since melatonin from plant foods is absorbed from the gastrointestinal tract and incorporated into the bloodstream, studies should be concentrated on measuring its levels and its possible implications in human food. Through food, it is incorporated into the human body and is bound to cross the blood-brain barrier and the placenta. At the subcellular level, it is incorporated in the most important cellular organelles, the nucleus, and mitochondria. Consumption of fruits that contain melatonin has been reported to increase serum melatonin concentrations (Sae-Teaw et al. 2013). Because there may be a way to influence the blood levels of melatonin in mammals and birds through the consumption of plant-derived foods, research into melatonin as a phytochemical with potential health benefits is entering a new phase. Because of its antioxidant properties and influence on photoperiodic (circadian) rhythms, melatonin is occasionally taken as a food supplement.

5.6 Conclusion Seed development observes enhanced protein synthesis and high enzymatic activity during the filling stage. It is also marked by increased synthesis and accumulation of nitrogenous and carbon storage compounds which are necessary for early seed germination and seedling growth. Melatonin is a non-toxic substance of natural origin that acts as a stimulator and is instrumental in improving and stimulating plant health (Kołodziejczyk and Posmyk 2016; Janas and Posmyk 2013). Its primary role in plants may be related to protecting the germ and reproductive tissues from biological and chemical assaults by improving tolerance to abiotic and biotic stresses by scavenging free radicals and regulating biological processes (Li et al. 2019). The highest concentrations of melatonin have been reported in reproductive organs, particularly in seeds (Cho et  al. 2008). Melatonin has been traditionally used not only as a sleep modulator to correct human sleeping disorders, but also as an anti-depressant or to combat jet lag (Arnao and Hernández-Ruiz 2006). The digestive tract absorbs and incorporates melatonin from plant foods into the bloodstream. Through food, melatonin is incorporated into the human body and is bound to cross the blood-brain barrier and the placenta. At the subcellular level, it is incorporated in the most important cellular organelles, the nucleus, and mitochondria. Consumption of fruits that contain melatonin has been reported to increase serum melatonin concentrations (Sae-Teaw et al. 2013). Investigations have reported that the endogenous levels of melatonin in plants can be modulated through genetic transformation (Byeon and Back 2014). The need of searching for melatonin as a health-related phytochemical is finding a new arena for research because there could be a possibility of modulating blood melatonin levels in mammals. Because of its antioxidant properties and influence on photoperiodic (circadian) rhythms, melatonin is occasionally taken as a food supplement.

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Chapter 6

Melatonin in Plant Growth and Signaling Gustavo Ravelo-Ortega, Karen M. García-Valle, Ramón Pelagio-Flores, and José López-Bucio

Abstract  In recent years, knowledge has been gained into the mechanisms of action of melatonin in plants and its regulation of morphogenesis. Melatonin accumulates in several organs, such as the root, stem, and leaves, and can be transported from the major site of synthesis in leaves to distant tissues through the vascular bundles, where it affects cell signaling in crosstalk with major phytohormones. The structural similarity of melatonin with indole-3-acetic acid (IAA) led some authors to suggest a potential auxinic effect in plant signal transduction, particularly root branching and stem elongation. However, its physiological roles throughout the life cycle of plants did not support an auxinic role, but in contrast suggest independent mechanisms of action for each molecule, in agreement with the recent discovery of the melatonin receptor CAND2 that differs from the auxin receptors. This chapter describes the recent roles of melatonin in seed germination, root architecture, shoot development, reproduction, and senescence, and the genes and proteins targeted by melatonin signaling. The function of melatonin in these processes goes beyond its function as an antioxidant, and their possible applications represent a valuable input to optimize plant productivity and confer protection against stressing growth conditions. Keywords  Melatonin · Germination · Root architecture · Fruit ripening · Senescence · Signaling

G. Ravelo-Ortega · K. M. García-Valle · J. López-Bucio (*) Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Edificio B3, Ciudad Universitaria, Morelia, Michoacán, Mexico e-mail: [email protected] R. Pelagio-Flores Facultad de Químico Farmacobiología, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, Mexico © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_6

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6.1 Introduction Melatonin (N-acetyl-5-methoxytryptamine) is a ubiquitous indoleamine present across all kingdoms of life, best known for its role as a mammal neurotransmitter, where it was initially discovered in the bovine pineal gland. In animals, melatonin influences several physiological processes, including temperature, appetite, mood, sexual behavior, circadian rhythms and sleep, and reinforces the immune system (Brenner et al. 2006). The research of plant melatonin spread upon its identification in edible and wild species of angiosperms, distributed in more than 94 families (Dubbels et al. 1995; Hattori et al. 1995; Banerjee and Sharma 2021). Melatonin acts as a multifunctional molecule in promoting germination, root branching, flowering, and fruit ripening by regulating ethylene signaling, delaying senescence, and mediating stress responses (Arnao and Hernández-Ruiz 2009, 2017; Imran et al. 2021). More recently, its role in photosynthesis, photorespiration, stomatal opening, and water use efficiency has been uncovered (Teng et al. 2022), and protective mechanisms through biosynthesis of flavonoids, anthocyanins and carotenoids, among other secondary metabolites opened new biotechnological potential (Khan et al. 2020). The signal transduction pathways in plant cells for melatonin perception have just begun to be characterized. In this sense, the first putative melatonin receptor CAND2/PMRT1 was described in Arabidopsis thaliana (Wei et  al. 2018). This receptor is localized in the plasma membrane and interacts with the G protein α subunit (GPA1). Upon binding to melatonin, CAND2/PMRT1 drives the closure of stomata via H2O2 production and Ca2+ influx. Increasing efforts are devoted to the elucidation of the molecular components for decoding the melatonin message into plant cells through genetic and “omics” approaches.

6.2 Melatonin: A Ubiquitous Molecule Melatonin can be found in bacteria, yeasts, fungi, animals, and plants. As a such ubiquitous molecule, its paramount role as an antioxidant enables organisms to adapt and resist Reactive Oxygen Species (ROS) burst, thus improving the stability of macromolecules such as DNA, RNA, and proteins. Moreover, additional detoxification properties may be related to the production of the antioxidant enzymes superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) (Arnao and Hernández-Ruiz 2019; Fichman and Mittler 2020). Coincidentally, melatonin is synthesized in chloroplast and mitochondria, the main sources of ROS in plants, thus mitigating their potentially toxic effects (Zheng et al. 2017; Wang et al. 2017). The endogenous content of melatonin in plants varies among species, growth conditions, and plant organs. It protects the functioning of photosystems, particularly under environmental stress, such as heat, cold, soil pollution, or pathogen challenge (Takahashi and Murata 2008; Arnao and Hernández-Ruiz 2013). The highest

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content of melatonin is found in flowers, seeds, and leaves in species from the families Vitaceae, Rosaceae, Brassicaceae, Apiaceae, and Poaceae, but also in roots of Scutellaria biacalensis (Lamiaceae) (Reiter and Tan 2002; Altaf et  al. 2021; Mannino et al. 2021). The spatiotemporal, tissue-specific, and developmental regulation of melatonin biosynthesis is an important trait for the management of its endogenous levels in crops.

6.2.1 Biosynthesis Recent efforts have been made toward elucidating the pathway for melatonin biosynthesis in angiosperms. The corresponding enzymes involve tryptophan decarboxylase (TDC), tryptamine 5-hydroxylase (T5H), tryptophan hydroxylase (TPH), serotonin N-acetyltransferase (SNAT), N-acetylserotonin methyltransferase (ASMT) and caffeic acid O-methyltransferase (COMT), which are located in different cellular compartments, including the cytoplasm, the endoplasmic reticulum and the chloroplast (Back et al. 2016). The first precursor is the amino acid tryptophan, which is decarboxylated by TDC, then T5H-catalyzes a hydroxylation step forming serotonin. Even though T5H is essential for serotonin biosynthesis, T5H-deficient plants showed higher levels of melatonin, suggesting that melatonin and serotonin levels within plants are not equally distributed (Park et al. 2012). Serotonin acetylation occurs via SNAT (or AANAT in animals), resulting in N-acetylserotonin (Back et al. 2016). A SNAT isoform (MzSNAT5) was located in the mitochondria (Tan and Reiter 2020), whereas the last step of melatonin biosynthesis, namely the O-methylation of N-acetylserotonin by ASMT occurs in the chloroplast (Tan and Reiter 2020). The subcellular location of their biosynthetic enzymes suggests the importance of melatonin in the evolution of eukaryotic cells from their prokaryotic ancestors. Melatonin can be degraded either via an enzymatic pathway or through a non-­ enzymatic one. The enzymatic route involves hydroxylation producing cyclic 3-hydroxymelatonin, and 6-hydroxymelatonin, while its nitrosation leads to N-nitrosomelatonin or, alternatively, its deacetylation leads to 5-­methoxytryptamine (5-MT). The non-enzymatic reactions may occur under free radical stress or photocatalytic changes driven by UV light (Blanchard et al. 2000; Hardeland 2015; Lee and Back 2019).

6.2.2 Distribution Melatonin has been found in several plant organs, such as the root, stem, and leaves, and can be transported from the major sites of synthesis in leaves to distant tissues through the vascular bundles (Arnao and Hernández-Ruiz 2006). Its application to roots also enriched its content in leaves of water hyacinth and watermelon, which

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contributed to cold tolerance (Li et al. 2017; Tan et al. 2007), and alleviated photo-­ oxidative stress in cucumber (Li et al. 2016a). These data indicate the existence of transporting systems for the spread of melatonin, whose distribution could be related to enhanced production of antioxidant enzymes (SOD, CAT, and POD) (Qari et al. 2022). In lupin and barley roots, a melatonin gradient acts coordinately with auxin to drive growth and development (Hernández-Ruiz et  al. 2004; Hernández-Ruiz and Arnao 2008).

6.3 Plant Developmental Responses to Melatonin The structural similarity of melatonin with auxin led some authors to suggest a potential auxinic effect in plant signal transduction. To date, several physiological roles throughout the life cycle, from seed germination to senescence have been uncovered, which, however, did not support its auxinic role, but in contrast, suggest specific mechanisms of action for this indoleamine as described below.

6.3.1 Germination Seed germination is a critical event for survival and plant establishment in a given environment. During this process, the absorption of water by the seed and the subsequent rupture of external tissue layers enable the emergence of the radicle (Han and Yang 2015). Melatonin accumulates in seeds of cucumber, maize, and alfalfa, where it may act to protect germ tissue, particularly under stress conditions (Manchester et al. 2000; Paredes et al. 2009). In red cabbage (Brassica oleracea) treated with toxic copper concentrations (0.5 and 1 mM), which were associated with reduced germination, low melatonin concentrations (1 and 10 μM) improved germination. In contrast, a high melatonin concentration (100 μM) had the opposite effect, reducing seed germination (Posmyk et  al. 2008). The concentration-­ dependent effect of melatonin was also observed in cotton (Xiao et  al. 2019). Melatonin enhanced seed germination of Limonium bicolor under salt stress up-­ regulating or down-regulating genes related to gibberellic acid (GA) or abscisic acid biosynthesis, respectively, which leads to enhanced ABA content (Li et al. 2019). Comparable effects under different stress conditions were documented in cucumber, alfalfa, and maize (Cao et al. 2019; Yu et al. 2021; Zhang et al. 2014) (Fig. 6.1). In Arabidopsis, Lv et al. (2021) documented a strong repressing effect of melatonin in germination. They also found that the Arabidopsis mutants or overexpression lines of AMST, a gene for melatonin biosynthesis, had a higher and lower germination percentage than WT seeds, respectively. This process is apparently independent of the melatonin receptor CAND2/PMTR because the germination in the Arabidopsis mutant cand2–1 was equally inhibited as in the WT (Lv et al. 2021). Early repression of plant growth after germination could be attributed to increasing

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Fig. 6.1  Melatonin bioactivity at early stages of plant development. Melatonin promotes germination through negative and positive regulation of gibberellic acid (GA) and abscisic acid (ABA) biosynthesis, respectively. The primary root growth and the development of lateral or adventitious roots are altered by melatonin in a manner dependent or not on the synthesis, transport, and signaling of auxin (AUX). Foliage growth can be repressed or stimulated by melatonin. Arrows and blunt arrows represent positive or negative regulation, respectively

ABA levels in melatonin-treated Arabidopsis seedlings that were PMTR1-dependent (Yin et al. 2022). These reports show the interaction between melatonin and plant hormones such as GA and ABA to regulate germination and early post-germination events that depend on the concentration of the molecule applied and its internal levels.

6.3.2 Root Growth and Development Auxins are the most representative plant hormones for the regulation of root growth and development because they are critical players in the initiation of lateral and adventitious roots, elongation of root branches, and root hair development (Saini et al. 2013; Enders and Strader 2015). Melatonin has a chemical structure similar to the auxin indole-3-acetic acid (IAA), as such many studies have been focused on elucidating its potential auxin-activity (Murch and Erland 2021).

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The first study about the role of melatonin in plants, from which it was suggested that this molecule acts like an auxin was conducted in Hypericum perforatum testing its root formation capacity (Murch et al. 2001). Subsequent research of plant responses commonly attributed to auxin, concluded that melatonin and auxin activities were comparable (Arnao and Hernández-Ruiz 2007, 2019). Instead, Pelagio-­ Flores et al. (2012) indicated that despite melatonin and IAA could promote lateral and adventitious root formation in Arabidopsis, the phenotype of the auxin-­signaling mutants and expression of auxin-inducible genes did not support an auxinic mechanism for melatonin in this model plant. Coincidentally, other reports evidenced not only the lack of auxin bioactivity for the indoleamine through examining classical auxin tests over the phenotype of plants (Kim et al. 2016) but also documented a suppressing effect on both the synthesis and transport of auxin (Wang et al. 2016), that were further confirmed at the transcriptional response (Zhang et al. 2014; Zia et al. 2019). The existence of melatonin-IAA crosstalk is obvious since both compounds are biosynthesized from a common precursor, tryptophan. The auxin levels and the polar auxin transport mediated by the PIN transporters are influenced negatively by melatonin, which accounts for the regulation of the primary and lateral root development processes (Ren et al. 2019; Wang et al. 2016). In contrast, auxin content and transport have been positively regulated by melatonin and associated with primary and adventitious root development (Wen et al. 2016), and on primary roots, a proper IAA biosynthesis and distribution is required for cellular responses to melatonin (Wang et al. 2022; Yang et al. 2021). Melatonin levels increased after auxin application, suggesting a regulation loop for melatonin and IAA (Erland and Saxena 2019). In rice plants, the melatonin effect on root growth and lateral root formation is associated with transcriptional activation of auxin signaling (Liang et  al. 2017). Although data about auxin-like or auxin-independent functions of melatonin remain still challenging, the available information points to the importance of the plant species, growth conditions, plant organ, and concentrations applied when regarding the auxin-melatonin crosstalk (Fig. 6.1).

6.3.3 Shoot Growth Melatonin shows a concentration-dependent effect in etiolated hypocotyls of Lupinus albus, promoting its growth at micromolar concentrations and repressing it at higher concentrations (Hernández-Ruiz et al. 2004; Yang et al. 2019; Zhao et al. 2015). Comparable results were observed in coleoptiles of the monocots canary grass, wheat, barley, and oat (Hernández-Ruiz et  al. 2005). Several subsequent reports also documented its promoting properties under standard or stress growth conditions in several plant species. For instance, treating seeds of Zea mays, Cucumis sativus, Vigna radiata, Glycine max, and Triticum aestivum with melatonin or its foliar application in broccoli improved growth parameters (Gul et al. 2022; Janas and Posmyk 2013; Qiao et al. 2019; Wei et al. 2015).

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The opposite responses have also been reported. The growth of maize and apple plants was strongly inhibited by melatonin concentrations ranging from 100–5000 μM, in both cases, the inhibitory effect on plant growth was related to impaired sugar metabolism, transport, or photosynthesis, and in maize, the inhibitory effect is associated with photosynthetic alterations and downregulation of sucrose transport genes SUT1 and SUT2, whereas in apple were associated with increased levels of fructose, glucose, and sucrose in leaves, and downregulation of MdFRK2 (Yang et al. 2019; Zhao et al. 2015). Plant growth induction or inhibition by melatonin is concentration-dependent, being the biostimulation by far the most interesting trait towards agricultural improvement. In this sense, the natural role of melatonin as a plant growth promoter could be supported by a reduced growth or semi-dwarf phenotype in Oryza sativa and Arabidopsis thaliana mutants, which exhibit decreased endogenous melatonin levels (Back 2021). Consistently, an Arabidopsis mutant defective in the putative melatonin receptor cand2 has reduced growth (Wei et al. 2018). Together, these findings provide strong genetic evidence of the natural role of melatonin in plants as a positive growth regulator.

6.3.4 Flowering Plants develop flowers and fruits upon the activation of shoot apical meristems at maturity. Although the photoperiod is apparently the main stimulus that regulates flowering, other factors such as temperature, drought, herbivory, nutrient scarcity, and phytopathogen challenges can accelerate flowering and affect plant yield, since stressed plants cannot reach appropriate biomass to support productivity (Cho et al. 2017). In rice plants, melatonin levels increase at the flowering and post-flowering stages. Likewise, melatonin biosynthesis genes such as TDC, T5H, SNAT, and ASMT, were up-regulated during the pre-flowering stage (Park et al. 2013). Mutants affected by genes encoding these enzymes show delayed senescence and lower melatonin content, but the contrary occurs in over-expressing lines (Huang et  al. 2017; Lee et al. 2019). Key genes encoding flowering control proteins such as FLOWERING LOCUS T1 (FT1), APETALA 3, (AP3)-like gene (APL3), SUPPRESSION OF OVEREXPRESSION OF CONSTANS1 (SOC1)-like gene (SL1), FLOWERING PROMOTING FACTOR 3-like gene (FLP3) and MADS-Box gene (MADS15, MADS6), were up-regulated in the over-expressing lines of melatonin biosynthesis genes (Huang et al. 2017). These findings suggest that melatonin biosynthesis is essential to promote flowering (Fig. 6.2). However, the melatonin effect may vary depending on several factors. Concentrations greater than 500  μM melatonin delayed flowering in Arabidopsis thaliana and Chenopodium rubrum (Kolář and Macháčková 2005; Shi et al. 2016). Also, apple trees exhibited higher flowering percentages by spraying low melatonin concentrations (20 and 200 μM) and a lesser percentage at high concentrations (1000 μM) (Zhang et al. 2019a). This molecule is important for plant reproduction as it intensifies the

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Fig. 6.2  Melatonin and plant developmental transitions. Melatonin promotes the transition from vegetative into reproductive stage and raises fruit growth and weight in different species. Depicted are the proteins and major hormonal pathways influenced by melatonin at each developmental stage. FLOWERING LOCUS C (FLC), suppresses the activity of transcription factors that induce flowering transition by up-regulating the expression of genes encoding SUPPRESSION OF OVEREXPRESSION OF CONSTANS1 (SOC1) and FLOWERING LOCUS T (FT). Reactive oxygen species, which enhance senescence, are diminished by melatonin via improving the activity of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD), increasing the content of solutes and suppressing the expression of Senescence Associated Genes (SAG). Arrows and blunt arrows represent positive or negative regulation, respectively

biosynthesis of volatile organic compounds (VOCs) that act as pollinator attractants in Hedychium coronarium flowers and mitigates the male fertility damage caused by drought in Gossypium hirsutum (Abbas et al. 2021; Hu et al. 2020). Therefore, melatonin not only regulates the flowering time but also protects plants from environmental stress. Different pathways can activate flowering including the phytohormone gibberellic acid (GA). The interaction of GA to its receptor GA INSENSITIVE DWARF 1 (GID1) provokes the degradation via the 26S proteasome of protein repressors named DELLAs, which repress the activity of transcriptional factors that promote flowering (Bao et al. 2020). Besides, DELLAs work as co-repressors by binding to FLOWERING LOCUS C (FLC), which inhibits vernalization-dependent flowering affecting the SOC1 and FT expression (Li et al. 2016b). Shi et al. (2016) exposed Arabidopsis plants to 500 and 1000 μM melatonin, which were delayed in flowering and manifested a high expression of FLC. The mutants in DELLA genes previously treated with melatonin did not show increased transcription of FLC. Hence, the melatonin regulation in Arabidopsis flowering involves the FLC expression

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activated by DELLAs. It was recently reported that strigolactones could stimulate flowering by reducing melatonin content through FLC expression (Screpanti et al. 2016; Zhang et al. 2019b).

6.3.5 Fruit Development and Ripening The fruits are organs that protect and disperse the seed for subsequent generations (Fenn and Giovannoni 2021). Nevertheless, for humans, fruits are an important food resource that supports the economy of many countries. The physiological and molecular processes responsible for regulating fruit development and ripening have been explored for many years to improve yield and resistance to environmental stress (Quinet et al. 2019). Fruit development begins from the ovary formation until it completes its maturation, which implies a genetic regulation that controls the events of cell division and growth to give an adequate shape and size (Handa et al. 2012). The high content of melatonin in various fruits such as tomatoes, apples, and cherries, suggested its participation in fruit development (Tijero et al. 2019; Verde et al. 2022; Li et al. 2021). In pepper fruits, the highest concentration of melatonin was found in stage I, precisely on the sixth day after flowering (Korkmaz et  al. 2014), whereas in cherry it occurs at stage II (Zhao et al. 2013). The genes encoding for melatonin biosynthesis enzymes (TDC, T5H, NAT, and ASMT) were up-­regulated in the early stages of apple fruit development, which coincided with the highest melatonin content (Lei et al. 2013). It appears that the accumulation of melatonin in fruits may be related to its antioxidant function, preventing oxidative damage caused by ROS derived from the rapid cell division and elongation that enables fruit biomass augmentation (Fig. 6.2). Melatonin-treated pear trees showed bigger fruits, increasing by 47.85% the weight, and these fruits also accumulated more sugars (Liu et al. 2019b). The production of lycopene, a carotenoid responsible for the red pigmentation of tomatoes, increased five-fold in response to 50 μM melatonin. This treatment promoted the expression of synthase1 (PSY1) and carotenoid isomerase (CRTISO) genes, which encode for two lycopene biosynthesis enzymes, stimulated fruit softening through up-regulation of cell-wall degrading enzymes, and ameliorated the flavor by increasing the sugar content (Sun et al. 2015). However, the opposite effect was observed in mangoes or sweet cherries, where melatonin delayed their ripening (Liu et al. 2020a; Tijero et al. 2019). The phytohormone ethylene is responsible for inducing ripening by controlling the expression of genes that mediate pigment biosynthesis, cell wall remodeling, sugar metabolism, and production of aromas (Liu et  al. 2020b). Two enzymatic steps mediate ethylene biosynthesis: First, 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) converts S-adenosyl-methionine (SAM) into ACC, which is then transformed to ethylene by ACC oxidase (ACO). In the absence of ethylene, the ethylene receptor (ETR) keeps active the CONSTITUTIVE TRIPLE

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RESPONSE1 (CTR1) protein, which inhibits ETHYLENE INSENSITIVE2 (EIN2) regulator. When the ethylene level is optimal, CTR is inactivated and EIN2 is activated, allowing the expression of genes regulated by ethylene-response transcription factors such as EIN3 and ETHYLENE INSENSITIVE3-LIKE (EIL) proteins (Arraes et al. 2015). Melatonin treatments increased the ethylene level in tomatoes during postharvest and improved the pigmentation and sugar content. Furthermore, ethylene signaling genes such as ETR4 and EIL1/3 were up-regulated by melatonin (Sun et al. 2015). In apple fruits during the ripening process, melatonin content rises coincidentally with the emission of ethylene, indicating hormonal crosstalk (Verde et al. 2022). Mangoes in storage and treated with melatonin had a delayed ripening. This result was associated with a decrease in ABA levels, which was suggested to be caused by a decline in NCED enzymatic activity (Liu et al. 2020a). These data open the way for using melatonin to improve fruit production and quality as well as in postharvest management.

6.3.6 Senescence Plant cells may enter into a process of age-regulated deterioration that affects mitotic activity and physiological processes, which may also occur during stress exposure. This process, also known as senescence, mainly occurs in leaves and flowers, and its purpose is to remobilize nutrients or biomolecules from old to new organs (Guo et al. 2021). In addition to age, environmental factors such as temperature, light, water status, and nutrient availability influence senescence, affecting the growth and yield of crops (Woo et al. 2019). When plants are exposed to unfavorable environmental conditions, a ROS burst is generated to induce stress tolerance mechanisms. But if ROS levels continue rising and are not effectively removed by antioxidant systems, the membranes can collapse, and therefore, premature senescence occurs due to the degradation of proteins, DNA, and the collapse of organelles (Kumar et al. 2019). In different studies, melatonin delayed senescence via an improved antioxidant status (Ahmad et  al. 2020; Sharafi et al. 2021). The activity of antioxidant enzymes such as SOD, POD, and CAT, and the chlorophyll content decline while progressing the senescence in leaves (Liang et al. 2018). However, plants under senescence-stimulating conditions and treated with melatonin had better SOD, POD, and CAT activity (Chen et  al. 2021; Sharafi et al. 2021). Also, chlorophyll degradation became slower through the regulation of genes encoding for pigment-catalytic enzymes, which delays senescence (Ahmad et al. 2020; Chen et al. 2021; Tan et al. 2020). Knock-out mutants in genes of methyltransferases that participate in melatonin biosynthesis showed fast chlorophyll loss and premature senescence, confirming the importance of this molecule for controlling age, and stress-dependent processes (Hong et al. 2018; Huangfu et al. 2022). Additionally, melatonin slows leaf senescence by down-regulating the expression of Senescence Associated Genes (SAGs) such as SAG12, SAG13, and SEN4 (Chen et  al. 2021; Shi et  al. 2019; Tan et  al. 2020). Other non-enzymatic

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antioxidant mechanisms such as the AsA-GSH (ascorbate-glutathione) cycle, where ascorbic acid acts as an electron donor to reduce H2O2 to water, and solutes that diminish the oxidative stress reacting with free radicals, increased in response to melatonin (Liang et al. 2018; Tan et al. 2020; Wang et al. 2019a). The control of senescence in response to abiotic or biotic signals involves the participation of molecular mechanisms regulated by different phytohormones (Guo et al. 2021). Auxin and cytokinin are two important phytohormones that antagonistically mediate root and shoot meristem activity and coordinate several development processes (Kurepa et  al. 2019). Both phytohormones may inhibit leaf senescence through parallel pathways. AUXIN RESISTANT3 (AXR3)/INDOLE-3-­ ACETIC ACID INDUCIBLE17 (IAA17), which belongs to the repressor family that disrupts the auxin signaling by interacting with auxin response factors, was up-regulated in Arabidopsis by melatonin application (Shi et al. 2015). The mutants (iia17–1 and iia17–2) and overexpressing lines (IAA17OX-1 and IAA17OX-2) of IAA17 showed delayed or premature senescence, respectively. iia17–1 and iia17–2 mutants had lower SAG12 and SEN14 expression than wild-type plants, and the opposite result was recorded in the over-expressing lines, which confirmed that melatonin blocks auxin signaling to delay senescence through decreasing IAA17 expression. Otherwise, melatonin may interact with cytokinin to delay leaf senescence. For example, melatonin treatments repressed heat-induced leaf senescence in perennial ryegrass (Lolium perenne) and increased the expression of signaling and biosynthesis genes of the cytokinin pathway (Zhang et al. 2017). Transgenic lines of creeping bentgrass (Agrostis stolonifera) that over-express a cytokinin biosynthesis enzyme (isopentenyl transferase) exhibited higher melatonin content than the WT under both drought-induced senescence and melatonin treatment. In the same conditions, the over-expressing lines showed greater resistance to senescence as the expression of chlorophyll catalase genes and the degradation of this pigment were reduced (Ma et al. 2018). The ripening and senescence of climacteric fruits require a high production of ethylene that induces the activation of enzymes responsible for fruit softening and sugar production (Liu et  al. 2020a). In postharvest pears, melatonin application reduces ethylene levels by promoting nitric oxide synthesis, which decreases the senescence process. This protective effect was suppressed using an inhibitor for this reactive nitrogen specie (Liu et al. 2019a). Several transcription factors activated by the phytohormone ABA (BF1, BF4, and ABI5) are responsible for expressing chlorophyll catabolic and ABA biosynthetic genes, which accelerate senescence. These genes and the ABA content were down-regulated and senescence tolerance was enhanced by melatonin (Tan et al. 2019). Melatonin alleviates heat-induced senescence by decreasing the expression of ABA biosynthesis (NCED1 and ZEP) and signaling genes (ABI3 and ABI5) (Zhang et al. 2017). Gibberellins can induce leaf senescence by activating the degradation of DELLA proteins that repress the activity of transcription factors WRKY6 and WRKY45 (Chen et  al. 2017; Zhang et  al. 2018). In tomato plants, melatonin increased tolerance to heat-induced senescence interacting oppositely with the GA and ABA pathways, since it up-regulated GA and down-regulated ABA at the

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signaling and biosynthetic level (Jahan et  al. 2021). Another phytohormone that induces leaf senescence and whose effect can be lessened by melatonin is jasmonic acid. Wang et  al. (2019b) observed that melatonin diminished the senescence of tomato leaves exposed to methyl jasmonate, reducing lipoperoxidation, ROS content, and pigment degradation.

6.4 Conclusions The occurrence and wide distribution of melatonin in plants are explained by its important role in growth, development, and metabolism acting not only as an antioxidant but also as a phytohormone-like compound. The alteration of genes related to melatonin synthesis and signaling in Arabidopsis and economically relevant species via mutational and transgenic approaches yielded clear phenotypes, indicating that correct perception of this indoleamine is crucial for biomass production, root development, flowering, and ripening (Back 2021; Teng et al. 2022; Wei et al. 2018). Moreover, the application of melatonin to roots and shoots helps plants to contend with soil, heat, and water stress that normally compromises productivity (Jahan et al. 2021). The discovery of the melatonin receptor CAND2 as well as transcriptomic and proteomic approaches unveiled molecular mechanisms to deliver the melatonin message into plant cells, for which many genes change its expression being these either up-regulated or down-regulated depending upon the tissue-­ specific or environmental context (Zia et al. 2019). Finally, crosstalk with classical phytohormones including auxins, cytokinins, ABA, but also ethylene and jasmonic acid, these later comprising important defense sentinels, opens the possibility of using melatonin to protect plants from predators and pests (Yin et al. 2022; Wang et al. 2019b). Although understanding the mechanisms of action of indoleamines in plants is still in its infancy, the myriad of possible applications represents a valuable input in the search for more sustainable agriculture to ensure food security. Acknowledgments  The authors appreciate the support of the Consejo Nacional de Ciencia y Tecnología (CONACYT), México (grant A1-S-34768) for their research on melatonin signaling in plants.

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Chapter 7

Functions and Prospects of Melatonin During Pre-fertilization Reproductive Stages in Plants Priyanka Khanduri and Sudip Kumar Roy

Abstract  In the last two decades, an exhaustive amount of research has shown that melatonin is a critical pleiotropic molecule, controlling several developmental and stress-related responses in plants. In this chapter, we discuss the current and potential uses of melatonin during pre-fertilization reproductive stages, with particular emphasis on its involvement in regulating flowering and flower development as well as adaptation of reproductive stages to environmental stresses. Recent evidence indicates that melatonin delays the transition of floral meristem and, thereby, flowering time. It has been proposed that it plays a protective role during the development of flowers particularly male gametophyte development through its antioxidant activity. Recent studies also show that melatonin functions in the production of volatiles in flowers and the induction of parthenocarpy through cooperation with other phytohormones. Finally, melatonin can alleviate the effects of various abiotic stresses during flowering, including high temperature, chilling, and drought. The encouraging results obtained from the various studies point towards diverse roles of melatonin during pre-fertilization reproductive stages and also highlight the enormous potential of melatonin in improving plant performance under stressful environmental conditions. Keywords  Melatonin · Flowering · Floral transition · Floral volatiles · Parthenocarpy · Stress tolerance

P. Khanduri (*) Department of Botany, Vidyasagar Metropolitan College, University of Calcutta, Calcutta, India S. K. Roy Department of Botany, Charuchandra College, University of Calcutta, Calcutta, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_7

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7.1 Introduction Melatonin is an indoleamine (N-acetyl-5-methoxytryptamine) that was for the very first time isolated from the bovine pineal gland (Lerner et al. 1958). The exclusivity of the animal origin of melatonin changed after its discovery in the unicellular dinoflagellate Gonyaulax polyedra (Poeggeler et al. 1991). Soon, in 1995 the first reports of the presence of melatonin in plants came simultaneously from two independent groups (Dubbels et al. 1995; Hattori et al. 1995). Since then, melatonin has been shown to have pleiotropic effects on several aspects of plant growth. Melatonin regulates circadian rhythms, promotes cell enlargement and root development, delays flowering, delays senescence and improves crop quality, and increases fruit yield (Arnao and Hernandez-Ruiz 2015, 2020, 2021; Back 2021; Sun et al. 2021; Ahn et al. 2021). Melatonin is well-known to have antioxidative effects as it directly or indirectly scavenges reactive oxygen species (ROS) and reactive nitrogen species (RNS) and attenuates oxidative stress in cells, tissues, and organisms (Zhang et al. 2015). Several studies have confirmed that melatonin helps plants in alleviating the negative effects of various kinds of biotic and abiotic stress (Zhang et al. 2014, 2015; Arnao and Hernandez-Ruiz 2014, 2015, 2018; Li et  al. 2015, 2021; Nawaz et al. 2015; Chen and Li 2017; Cao et al. 2018; Ahammed et al. 2019; Huang et al. 2019; Siddiqui et al. 2020). Recently, the first putative plant melatonin receptor was identified in Arabidopsis indicating that melatonin could be a phytohormone (Arnao and Hernandez-Ruiz 2020). Reproduction is the basis for sustenance of any species. In higher plants, the flower is the basic unit of sexual reproduction. The initiation of flowering, growth, and development of sex organs in a flower, interaction between gametophytes, and fertilization are all regulated by complex signaling networks. It is a well-established fact that phytohormones regulate reproductive processes. In recent years, there are growing pieces of evidence that phytohormones like auxin, and gibberellins are indispensable for the development of sex organs. For instance, Gibberellins regulate early stamen development while auxin plays a role in anther dehiscence, pollen maturation, and filament elongation (Song et al. 2013). Multiple studies in the last two decades have shown that melatonin exhibits many hormone-like activities. Although its roles in various plant biological processes are known for a long time, information on its involvement in reproductive development has been quite recent. In this chapter, we explore the myriad roles of melatonin during flowering, pre-­ fertilization reproductive processes, stress tolerance during reproductive stages, and the molecular mechanisms behind its many functions.

7.2 Physiological Roles of Melatonin During Pre-fertilization Reproductive Stages An increasing repository of work has shown that phytomelatonin plays a crucial role in the regulation of various aspects of plant growth and development. Several important roles have been attributed to phytomelatonin like enhancement of plant

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antioxidant enzyme activity, improvement of plant tolerance to various biotic and abiotic stresses, synchronization of plant resistance, and improving fruit yield and crop quality (Zhang et al. 2015; Li et al. 2015, 2021; Cao et al. 2018; Arnao and Hernandez-Ruiz 2018, 2020, 2021; Huang et  al. 2019; Mohamed et  al. 2020; Siddiqui et al. 2020; Sun et al. 2021). However, the number of studies on the roles of phytomelatonin on reproductive development is considerably fewer but equally exciting. The present section gives a brief account of the role of melatonin during plant reproductive development.

7.2.1 Flowering Time An environmentally coordinated circadian clock is important for the growth and development of plants. The well-synchronized flowering rhythm ensures adequate pollination and normal seed/fruit development. Studies have shown that the transition from the vegetative phase to flowering in plants is under the control of environmental (photoperiod and temperature), physiological (phytohormones and nutritional status), and genetic factors (gene regulation and developmental stage) (Cao et al. 2021). The role of melatonin in controlling circadian rhythms in animals is well known. Taking cues from that, initial studies indicating a possible role of melatonin as a chrono-regulator of circadian rhythms in plants were done on short-­ day plant Chenopodium rubrum (Kolar et al. 1997; Wolf et al. 2001). These studies showed that during the light period, melatonin concentration remained low or undetectable. As the dark period ensues the melatonin concentration starts to increase reaching a maximum at 4–6  hours of the dark period before decreasing rapidly. Similar fluctuating levels of melatonin in a 24-hr cycle have been seen in various other plant species, such as Eichhornia crassipes, Vitis vinifera, Prunus avium, and Hordeum vulgare (Tan et al. 2007; Boccalandro et al. 2011; Zhao et al. 2013; Arnao and Hernandez-Ruiz 2015). The effect of melatonin on flowering rhythm was also studied for the first time in C. rubrum and it was shown that melatonin interferes in the photoperiod induction of flowering (Machackova and Krekule 2002; Kolar et  al. 2003; Kolář and Macháčková 2005). In C. rubrum, flower induction was shown to be inhibited by an average of 40–50% when high concentrations of melatonin is applied 2 h before and after the beginning of the inductive dark period. However, melatonin treatment had no effect per se on the duration of flowering which suggests that it controls some process related to floral transition (Kolář and Macháčková 2005). Also, in transgenic rice plants which were rich in melatonin flowering was seen to be delayed by 1  week indicating some role of melatonin in regulating flowering time. Delayed flowering resulted in a reduction of grain yields by an average of 33% in the melatonin-­rich transgenic lines (Byeon and Back 2014). More direct evidence for the restrictive role of melatonin in flowering was provided by Shi et al. (2016). The authors showed that exogenous application of melatonin retards flowering in Arabidopsis. In this study, Arabidopsis plants which were treated with 500 μM melatonin exhibited delayed flowering by 5 days and plants

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had more rosette leaves as compared to the untreated plants. The study also demonstrated the novel involvement of DELLAs and flowering Locus C (FLC) in melatonin-­mediated flowering in Arabidopsis. However, recently Lee et al. (2019) have presented contradictory results in snat2 knockout mutants of Arabidopsis. Serotonin N-acetyltransferase (SNAT) catalyzes the formation of N-acetylserotonin (NAS) from serotonin and is known to play important roles both in melatonin biosynthesis and function (Zheng and Cole 2002). snat2 mutants produce less melatonin than the wild type. Interestingly, it was discovered that the snat2 seedlings showed delayed flowering despite having a lower concentration of melatonin (Lee et al. 2019). According to the authors, exogenously applied melatonin cannot translate the effects of endogenous melatonin on flowering and hence their results were in contradiction with the results of Shi et  al. (2016) Also, high-dose melatonin (500 μM, as used by Shi et al. 2016) probably retarded the growth of Arabidopsis seedlings. This contradictory report warrants more attention as most of the studies to date have pointed to delayed flowering in the presence of high concentrations of melatonin. Another interesting study was done in Arabidopsis mutants for strigolactone (SL) synthesis or signaling, a carotenoid-derived compound involved in regulating flowering in plants (Zhang et al. 2019). It was shown that the flowering time of Arabidopsis is delayed if the tissue content of melatonin is higher than ~8 ng/g F.W, or accelerated if it falls below ~0.9 ng/g. Authors proposed that melatonin acts downstream of SL, and if its concentration is not within a certain range it can cause a delay in flowering. Another recent study that has shown a suppressive effect of melatonin on flowering if present in high concentrations was done in apples by Zhang et al. (2018). The authors monitored apple trees for two consecutive years and reported a significant reduction in endogenous melatonin content in apple trees before flowering. Apple trees were also subjected to different concentrations (0, 20, 200, and 1000 μM) of exogenous melatonin through spraying. It was found that in comparison to the control plants, 20- and 200-μM melatonin treatments delayed apple bloom by 2 days, and 1000-μM melatonin treatment delayed flowering by 3 days (Zhang et al. 2018). Hence, the application of melatonin in a dose-dependent manner before flowering could delay the flowering in apple trees (Zhang et al. 2018). Thus, based on the current evidence, melatonin can be assumed to be a chrono-­ regulator of flowering time and the concentration of melatonin likely decreases just before flowering. However, this notion should be thoroughly investigated in other plant species for conclusive evidence.

7.2.2 Floral Meristem Formation The development of a flower is a highly coordinated multistep procedure that involves floral induction, floral meristem formation, and floral organ development. All these steps are under the strict control of a network of interacting genes and their protein products known as the Gene Regulatory Network (GRN) (Kinoshita and

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Richter 2020). After reaching the right developmental stage and perceiving the right environmental cues, flowering-time genes are triggered resulting in the conversion of the vegetative shoot apical meristem (SAM) into an inflorescence meristem (IM) (Liu et al. 2009). In the model plant, A. thaliana, several regulators which are involved in the flowering induction are recognized. These regulators facilitate the transition of vegetative meristem to the reproductive meristem by integrating the gene interactions and resultant signal transduction pathways (Liu et al. 2015b). The main flowering genes recognized in A. thaliana include FLOWERING LOCUS C (FLC), FLOWERING LOCUS T (FT), SUPPRESSSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), APETALA1 (AP1), CONSTANS (CO), LEAFY (LFY), and TARGET OF EAT1 (TOE1). Out of these, FLC is a MADS-box transcription factor which is a negative regulator of floral transition as it represses the transcription of some floral genes like SOC1 and FT by binding to their promoter regions (Li et  al. 2016). Phytohormone Gibberellic Acid (GA) also plays an important role in the formation of floral meristem in A. thaliana (Sun and Gubler 2004). GA promotes the ubiquitin-­ mediated degradation of DELLA proteins which mediate different genetic pathways that repress plant flowering (Wigge et al. 2005; Searle et al. 2006). DELLAs also affect the transcriptional activity of FLC leading to late flowering (Li et al. 2016). The role of melatonin in the transition from the vegetative to the reproductive phase was first described in Arabidopsis by Shi et  al. (2016). According to this study, melatonin mediates the stabilization of DELLA proteins which activates FLC and represses the transcription of FT resulting in delayed flowering (Fig.  7.1). Authors treated plants with exogenous melatonin and it was proposed that stabilization of DELLAs by melatonin is without regulation of transcription of DELLAs and endogenous GA level. Notably, floral transition in della mutants was not influenced by exogenous melatonin as there was a decrease in melatonin-induced FLC transcripts in della mutants. Thus, results suggested that melatonin mediated flowering in Arabidopsis through DELLAs-activated FLC. According to Mukherjee (2019), melatonin induces endogenous nitric oxide (NO) levels and it has been speculated that NO may play some role in melatonin-mediated DELLA stabilization and consequently delayed flowering (Shi et al. 2016). A study by Zhang et al. (2019) revealed the interaction between melatonin and other signaling molecules in regulating floral transition. As mentioned in the previous 3.1, this study was done in Arabidopsis mutants for SL synthesis or signaling. SL is a carotenoid-derived compound involved in regulating various developmental pathways in plants including flowering. The authors suggested that floral transition in Arabidopsis is mediated by a combination of melatonin and SL. The study proposed that whenever the melatonin content exceeds a certain threshold, SL acts upstream of melatonin to delay flowering due to the activation of FLC. The above-mentioned studies unravel the role of melatonin in a key developmental event of the transition of vegetative meristem to reproductive meristem (Fig. 7.1). However, exactly how SL regulates melatonin and melatonin regulates the transcription of FLC needs more investigation. Table 7.1 summarizes the effect of melatonin on the expression of various genes involved in flowering.

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Fig. 7.1  Proposed role of melatonin in floral transition. Melatonin upregulates the expression of DELLAs and FLC, consequently delaying the transition of SAM to IM (Shi et al. 2016). During this process, SL acts upstream of melatonin to delay flowering (Zhang et al. 2019). SL strigolactone, FLC flowering locus C, FT flowering locus T, SOC1 suppressor of overexpression of CONSTANS1, API1 Apetala-1, SAM shoot apical meristem, IM inflorescence meristem

7.2.3 Flower Development Flowers harbor the reproductive organs of a plant which in turn store the male and female gametophytes i.e., the pollen grains and the embryo sac respectively. The gametophytes are the most vulnerable and vital tissues produced in the life cycle of a plant having a direct role in plant reproduction. It is well known that the development of reproductive tissues is highly sensitive to potential environmental damage which may induce the generation of oxidants like ROS and RNS. These oxidants need to be in a redox balance, or else, they may cause oxidative damage to reproductive tissues and hamper the reproductive success of plants. In the initial years of research, phytomelatonin was reported from a wide variety of tissues like roots, stems, leaves, fruits, and seeds except flowers (Murch et al. 1997; Chen et al. 2003; Cao et al. 2006; Arnao and Hernandez-Ruiz 2006). In the subsequent years, one of the roles attributed to melatonin in plants was protecting from oxidative damage through direct radical scavenging (Hardeland 2005; Tan et  al. 2007; Schaefer and Hardeland 2009). The hypothesis that melatonin may serve as an antioxidant served as the basis for the detection of melatonin in flowers. The first study to determine the presence of melatonin during flower development was done in Hypericum perforatum (Murch and Saxena 2002). It was reported that during the uninucleate stage of microsporogenesis, concentrations of the indole were highest and at the elevated concentration of melatonin the regenerative potential of isolated anthers was also maximum. Thus, the authors proposed that

+ +

Arabidopsis Pyrus communis

GIBBERELIC ACID 2 OXIDASE (GA20ox) Pyrus communis

Hedychium coronarium

Solanum lycopersicum

Solanum lycopersicum

Solanum lycopersicum

Solanum lycopersicum

Solanum lycopersicum

Solanum lycopersicum

Solanum lycopersicum

HcMYB genes

CATALASE 1 (CAT 1)

ASCORBATE PEROXIDASE (APX)

GUAIACOL PEROXIDASE (G-POD)

SUPEROXIDE DISMUTASE (SOD)

HEAT SHOCK PROTEIN 21 (HSP21)

HEAT SHOCK PROTEIN 70 (HSP70)

AUTOPHAGY-RELATED GENEs (ATG6, ATG8c, ATG12 and ATG18h)

+

+

+

+

+

+

+

+ –

Plant Species Arabidopsis Arabidopsis Arabidopsis

Gene FLOWERING LOCUS C (FLC) FLOWERING LOCUS T (FT) SUPPRESSSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) DELLA genes GIBBERELIC ACID 2 OXIDASE (GA2ox)

Upregulation (+) or downregulation (−) of genes + – + Delays flowering GA biosynthesis related to parthenocarpy GA biosynthesis to induce parthenocarpy MYB transcription factors putatively involved in floral aroma biosynthesis Alleviating high temperature-induced ROS production Alleviating high temperature-induced ROS production Alleviating high temperature-induced ROS production Alleviating high temperature-induced ROS production Putative role in restoring the stability of tapetum upon exposure to high-temperature Putative role in restoring the stability of tapetum upon exposure to high-temperature Induction of autophagy in response to high-temperature stress

Effect Delays flowering Delays flowering Delays flowering

Table 7.1  Summary of effect of melatonin treatment on expression of genes involved in flowering and related processes

Qi et al. (2018)

Qi et al. (2018)

Qi et al. (2018)

Qi et al. (2018)

Qi et al. (2018)

Qi et al. (2018)

Qi et al. (2018)

Abbas et al. (2021)

Liu et al. (2018)

Shi et al. (2016) Liu et al. (2018)

Reference Shi et al. (2016) Shi et al. (2016) Shi et al. (2016)

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melatonin may play a significant role in the regulation of the reproductive physiology and flower development of H. perforatum. Authors also speculated a similar pattern of melatonin accumulation in flowers of other species. High levels of melatonin were also reported in the floral tissues of Datura metel (Murch et al. 2009). It was found that melatonin levels were high in the developing flower buds and ovules of D. metel and which progressively declined in fruits. Authors proposed that melatonin in D. metel acts as an antioxidant in protecting the early stages of reproductive tissues. The hypothesis was further supported by the observation of elevated levels of melatonin in flower buds exposed to cold stress. Accumulation of melatonin during flower development was also shown in rice (Park et al. 2013). In the study, melatonin content was estimated during reproductive stages (pre-flowering, flowering, and post-flowering) and it was demonstrated that the melatonin contents were sixfold higher in the flowering stage than the pre-­ flowering stage. Authors also reported induction of melatonin biosynthesis was marked by the induction of required proteins such as tryptophan decarboxylase, tryptamine 5-­ hydroxylase, and N-acetylserotonin methyltransferase. In Prunus avium, melatonin levels were reported to increase later in the season by Zhao et al. (2013), which authors attributed to defense against high light stress and increased ROS load in the tissues. In the herbaceous ornamental plant Paeonia lactiflora, the melatonin content has been studied in different color series and developmental stages of flowers viz. flower-bud stage (Stage 1, S1), initiating bloom stage (Stage 2, S2), bloom stage (Stage 3, S3) and wither stage (Stage 4, S4) (Zhao et al. 2018). It has been reported that peony flowers are rich in melatonin, however, the color series vary in melatonin content. The highest amount of melatonin was found in the white series, followed by the ink series, the red series, and then the pink series. Also, during flower development, the melatonin content first increases in the S1 stage and then decreases in S2 before peaking in the bloom stage (S3). The melatonin content again decreases in the S4 stage but was still higher than the content in S2. Zhao et al. (2018) also studied the effect of different parts of the light spectrum on the melatonin content during flowering. They demonstrated that sun exposure and blue light induce melatonin production whereas shade conditions, and white and green lights lower melatonin production. Also, “dual peaks” of melatonin were reported at 2  p.m. and 2 a.m. in a 24-h light/dark cycle. Authors linked this fluctuation in the melatonin content during different stages, at different times, and in different light conditions to a matching expression pattern of the tryptophan decarboxylase gene (TDC). Melatonin has been reported from flowers of many other plants like Malus domestica, Tanacetum parthenium, Tripleurospermum disciforme, Viola odorata, Oryza sativa, Solanum lycopersicum, and Capsicum annum (Okazaki and Ezura 2009; Ansari et al. 2010; Park et al. 2013; Lei et al. 2013; Korkmazab 2014). All these studies show that the induction of melatonin occurs during flower development and that melatonin may have a protective role during flower development. However, how, where and at which stage of flower development exactly melatonin functions are still a matter of investigation. Also, more direct evidence of its function during flower development will be more revealing of its role.

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7.2.4 Floral Volatiles The majority of flowering plants rely on biotic pollination for reproductive success (Ollerton et al. 2011). To cause this effect plants develop a variety of contrivances to attract potential pollinators. Floral volatiles are one of the key floral attractants for pollinators which other than that also defend the plants from floral antagonists (Schiestl et al. 2014; Junker and Parachnowitsch 2015). Other than its role in flower reproduction, floral volatiles also have immense economical value in perfumes, cosmetics, flavorings, and therapeutic industries. Chemically floral volatiles can range from terpenoids to benzenoids, fatty acid derivatives, nitrogen-containing compounds, amino acid derivatives, and sulfur-containing compounds (Farré-Armengol et al. 2020). Floral volatiles is synthesized through complex biochemical pathways which are regulated by various internal and external stimuli (Dudareva and Pichersky 2008; Abbas et al. 2017). A recent study by Abbas et al. (2021) in Hedychium coronarium has proposed a putative regulatory role of melatonin floral scent production. Flowers of H. coronarium are known to release abundant amounts of volatiles during the blooming period. The major volatiles found in the scent are terpenoids (monoterpenes and sesquiterpenes) and benzenoids/phenylpropanoids. Through integrated metabolomic and transcriptomic approaches, authors analyzed the changes triggered by melatonin exposure during the half bloom (HS), full bloom (FB), and fade stage (FS) of flower development in H. coronarium. The study revealed that volatile organic compound emission was significantly enhanced at all the stages of flowering after exposure to melatonin. The metabolomic analysis led to the identification of 15 volatile compounds whose concentration was enhanced by the melatonin treatments. According to the transcriptomic analysis, around seventy-six genes and some transcription factors, such as MYB/bHLH, were found to be significantly upregulated and were speculated to be directly involved in the biosynthesis of floral aromatic compounds. Thus, the authors suggested that melatonin mediates the expression of certain genes involved in the biosynthesis of volatile compounds and enhances the production of aroma in H. coronarium flowers (Abbas et al. 2021).

7.2.5 Parthenocarpy Parthenocarpy is the production of fruits without the fertilization of ovules such that fruits are seedless. It is of common occurrence in the horticultural varieties of banana, pineapple, cucumber, tomatoes, figs, oranges, grapes, kiwi, blackberry, pepper, etc. One of the main advantages of parthenocarpy is that the fruit set is not dependent on pollination and fertilization. Therefore, it ensures reproduction even in environmental conditions that are not conducive to pollination. Moreover, the absence of seeds increases the palatability of fruits and in turn their commercial viability.

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Parthenocarpy is a genetically inherited trait and the potential to form parthenocarpic fruit is dependent on the genetic makeup of the cultivar. Parthenocarpy can also be induced artificially by exogenous applications of plant hormones. For instance, indole-3-acetic acid (IAA) is used to induce parthenocarpy in many horticultural plants, such as tomatoes, cucumbers, and zucchini (Martinelli et al. 2009; Pomares-Viciana et al. 2017). Also, the treatment of certain cultivars of oranges, tomatoes, blueberries, garden peas, and Arabidopsis by GA3 (or GA1) causes parthenocarpic fruit development (Cano-Medrano and Darnell 1997). The similarity between the functions of melatonin and IAA in plants, the fact they share a common precursor, tryptophan, and the already-known role of melatonin in the GA pathway of flowering led Liu et al. (2018) to explore the involvement of melatonin in inducing parthenocarpy. Authors used ‘Starkrimson’ pear for their study and found that the exogenous application of melatonin promoted the development of ovaries in the absence of pollination same as pollinated ovaries. Melatonin-­ treated ovaries led to the development of fruits without seeds. Investigation into the changes of related hormones in the ovaries led to the revelation of a significant increase in the contents of the gibberellins (GAs) GA3 and GA4. The authors also studied the relationship between melatonin and GA using paclobutrazol (PAC), a GA-biosynthesis inhibitor. It was seen if a prior treatment of PAC was given, neither GA content increased nor parthenocarpic fruit development happened even after spraying with melatonin. Also, transcriptome analysis has shown that melatonin can cause significant upregulation of PbGA20ox (GA 20-oxidase) and downregulation of PbGA2ox (GA 2-oxidase), enzymes involved in the biosynthesis of GA. Thus, it has been suggested that melatonin induces parthenocarpy in pears by promoting the biosynthesis of GA biosynthesis.

7.3 Role of Melatonin During Stress Tolerance in Reproductive Tissues Over the past decade, huge amounts of evidence have amassed which suggests that melatonin protects plants against biotic stress (Arnao and Hernandez-Ruiz 2014, 2015, 2018; Chen and Li 2017) and abiotic stress (Zhang et al. 2014; Arnao and Hernandez-Ruiz 2015; Zhang et al. 2015; Li et al. 2015, 2021; Nawaz et al. 2015; Cao et al. 2018; Ahammed et al. 2019; Huang et al. 2019; Siddiqui et al. 2020). Currently, several review articles discuss the protective effects of melatonin in improving plant tolerance and the role of melatonin in regulating epigenetic and transcriptional changes in plants under stress. Most of these studies have focussed on the role of melatonin in response to abiotic stresses in vegetative tissues. Although melatonin is known to accumulate in high quantities during flower development, very limited literature is available on the role of melatonin in stress tolerance in reproductive organs. Nevertheless, the few studies conducted on the aspect have put forward some very interesting findings and helped in understanding the functions of melatonin in plant reproductive development.

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The study by Qi et al. (2018) through exhaustive data reported that melatonin protects pollen activity in Solanum lycopersicum under high-temperature stress. Authors reported that irrigation treatment with 20 μM of melatonin can alleviate high temperature-induced pollen abortion. Under high temperature, both pollen viability and the mean germination ratio of pollen grains was found to be significantly higher in plants treated with melatonin as compared to untreated plants. It was also shown that melatonin alleviates high temperature-induced ROS accumulation in tomato anthers as there was a decrease in H2O2 content by 35.3% after 3 h of high-temperature stress in the plants treated with melatonin. The gene expression analysis has shed light on the genes which might be upregulated after melatonin pre-treatment. Transcript levels of antioxidant-related genes like CAT1, APX1, DAHR, and Fe-SOD are known to be accentuated by melatonin under oxidative stress. All these findings suggest that melatonin helps in the protection of anthers from oxidative stress as triggered by high temperature by either directly scavenging the ROS or indirectly stimulating the expression of antioxidative enzymes (Qi et  al. 2018). The study also revealed the ultrastructural changes specifically, premature degeneration of the tapetum cells which lead to pollen abortion in response to high temperature can be assuaged by melatonin. Pre-treatment with melatonin also enhances the expression of heat shock protein genes HSP21 and HSP70 which help in refolding the unfolded proteins. Autophagy is a degradation system employed by cells to destroy dysfunctional proteins and organelles by delivering them to lysosomes. It is involved in numerous biological processes of plants including responses to biotic and abiotic stress (Qi et al. 2021). Investigating if melatonin can enhance the occurrence of autophagy in heatstressed anthers of tomato revealed that the expression of the autophagy-related (ATG) genes was greater in melatonin-pre-­treated anthers. This results in the manifestation of autophagy upon high-­temperature stress. Drought stress during flowering can significantly reduce the yield of plants by damaging the reproductive organs (Fang et  al. 2010). Numerous studies have reported drought-induced yield loss due to low male sterility (Fang et al. 2010; Fu et al. 2011). The role of melatonin in overcoming the drought-induced suppression of seed germination and root elongation is known in many plants (Zhang et al. 2014; Li et al. 2015; Liu et al. 2015a; Wei et al. 2015). However, the first study to explore the role of melatonin in drought tolerance in male reproductive organs was attempted by Hu et al. (2020). The authors studied the effects of exogenous melatonin (100, 200, and 1000  μM) on male fertility and related carbohydrate metabolism in drought-stressed anthers of cotton cultivar Yuzaomian 9110. Results showed that exogenous melatonin can enhance the concentration of endogenous melatonin in drought-stressed anthers and also improve the water status by 1.4–14.2 folds. Also, melatonin application significantly improves the translocation of carbon assimilates to drought-stressed anthers which otherwise is inhibited by drought. Drought lowers male fertility in plants by modifying carbohydrate metabolism. Under the conditions of drought, pollen viability and germination are restricted due to a decline either in the deposition of starch or the hydrolysis of sucrose into hexoses, or the generation of adenosine triphosphate (ATP) in anthers. Hu et  al. (2020) reported that exogenous melatonin can improve male fertility under drought conditions by

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regulating the carbohydrate metabolism. In their study, the application of exogenous melatonin in drought-stressed anthers led to enhancement in the activities of ADP-glucose pyrophosphorylase and soluble starch synthases which in turn increases the starch accumulation. Exogenous melatonin was also reported to generate more ATP for reproductive activities and also accelerate the hydrolysis of sucrose by increasing the activities of sucrose synthase and acid and alkaline invertases. Cut flowers suffer from a short life span post-harvest. To meet the demands for high-quality freshly cut flowers, preservation of cut flowers is essential. Low-­ temperature storage is one of the most important post-harvest handling procedures for cut flowers. However, flowers develop chilling injuries during this time which decreases their quality and negatively affects consumer preferences. Many compounds are used as protective and preservative factors in the cut flowers industry like γ-aminobutyric acid (GABA), putrescine, spermidine, etc. The role of melatonin in abating chilling injury in cut flowers was studied for the first time in cut anthurium flowers (Aghdam et al. 2019). It was shown that exogenous melatonin at 1, 10, 100, and 1000 μM can ameliorate chilling injury in cut anthurium flowers during storage at 4 °C for 21 d by 11, 29, 51 and 31%, respectively, compared with that of untreated flowers, (Aghdam et al. 2019). Flowers treated with 100 μM melatonin show lower electrolyte leakage and malondialdehyde concentration during cold storage and authors speculated that high NADPH oxidase activity may be responsible for signaling H2O2 concentration in treated flowers. Authors also reported higher alternative oxidase gene expression which was accompanied by higher activities of catalase, superoxide dismutase, ascorbate peroxidase, and glutathione reductase, and higher concentrations of ascorbate and glutathione. It was linked to protection from the damaging effects of H2O2 at 4 °C. A recent study on a similar aspect in carnations also shows the efficacy of melatonin in prolonging the vase life of a cut flower (Lezoul et al. 2022). The authors evaluated the effect of different concentrations of melatonin (0.01, 0.1, and 1  mM) on the vase life of cut carnations flowers cv. Baltico. It was observed that melatonin at 0.1 mM concentration increases the vase life of cut carnations by up to 10 days. The results obtained from the above studies underline the potential role of melatonin in improving reproductive performance, thereby yield of crop plants under unfavorable environmental conditions, and also as a tool for post-harvest management of horticultural crops.

7.4 Conclusions and Future Perspectives Melatonin acts at various levels of flowering and flower development. High amounts of melatonin before flowering leads to a delay in flowering. Molecular mechanisms show that melatonin delays flowering by upregulating the transcription of FLC and consequently inhibiting the meristem transition. Melatonin also increases the stabilization of DELLA proteins which induce a late-flowering effect. It is speculated that melatonin-mediated stabilization of DELLAs and consequently delayed

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flowering may involve NO. Another aspect of melatonin-mediated control of flowering is the suppression of melatonin signaling and/or biosynthesis by SL which induces earlier flowering. Although downregulation of melatonin is required before flowering, it is the opposite during flower development. Melatonin concentrations are highest in the initial stages of flower development and decrease progressively till fruit development. Melatonin is required for the development and protection of male gametophytes and is probably involved in the scavenging of ROS in general. Melatonin also has a putative regulatory role in floral aroma enhancement and inducing parthenocarpy. It is involved in enhancing stress tolerance during male gametophyte development through ROS scavenging and carbohydrate metabolism under heat stress and drought stress respectively. Accumulation of enormous data on the functions of melatonin clearly shows that it is a regulator of multiple aspects of plant growth and development. So much so, that the possibility of melatonin as a phytohormone has also been raised after the identification of the putative melatonin receptor CAND2/PMTR1 in plants. However, there are several aspects especially ones related to flowering that need to be deciphered and could be the aim of future studies. In-depth investigations are required to understand the exact role of melatonin in delaying flowering. Future studies should explore how melatonin signaling is switched off or downgraded before flowering. Also, the precise cross-talk between SL and melatonin in flowering is an area of further investigation. The data generated can be of immense value to horticultural species. The involvement of NO in many of the responses mediated by melatonin has been the subject of many studies. Investigation into the genetic regulation of NO and melatonin can increase our knowledge of the effects of melatonin on flowering. Understanding of the functions of melatonin during flower development is largely limited. Investigations in the area will help clarify how melatonin is involved in so many cellular and physiological activities during flower development. The effect of melatonin on female gametophyte development and stress tolerance is completely untouched. Likewise, investigation of melatonin during the progamic phase in plants will be interesting as it is a very important phase for successful reproduction. Concerted interactions occur between pollen and pistil during the progamic phase. Carbohydrates in the pistil are essential for normal pollen tube growth. However, heat stress results in substantial changes in the carbohydrate balance of pollen and pistil. Future studies can explore applications of exogenous melatonin to rescue plants from the ill-effects of heat stress during the progamic phase. Given the diverse roles of melatonin in plants, it will be beneficial to convert these findings into commercial outputs.

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Chapter 8

Melatonin and Fruit Ripening Physiology: Crosstalk with Ethylene, Nitric Oxide, Hydrogen Peroxide and Hydrogen Sulphide Sani Sharif Usman, Atif Khurshid Wani, Abdullahi Ibrahim Uba, Tahir ul Gani Mir, Weda Makarti Mahayu, and Parnidi

Abstract Ripening of fruit is a complex physiological process comprising a sequence of events that precipitates the signaling molecules, especially hydrogen peroxide (H2O2), ethylene, melatonin, nitric oxide (NO), auxin, hydrogen sulfide (H2S), and brassinosteroids at different levels of gene and protein expression to initiate activation and/or deactivation of various signaling pathways that ultimately lead to the ripening of the fruit. Although ethylene has been documented as a potent molecule capable of regulating fruit ripening, molecules such as phytomelatonin, NO, H2O2, and H2S have the potential of regulating fruit ripening. However, the interaction of ethylene and these new emerging signaling molecules particularly phytomelatonin, NO, H2O2, and H2S is not fully understood. Therefore, harnessing the phytohormonal functions of phytomelatonin in fruit ripening physiology via crosstalk with ethylene and NO as well as H2O2 and H2S is of biological importance in revealing the free radical scavenging role of phytomelatonin. In this chapter, the

S. S. Usman Department of Molecular Biology and Genetic Engineering, School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India Department of Biological Sciences, Faculty of Science, Federal University of Kashere, Kashere, Gombe, Nigeria A. K. Wani (*) · T. u. G. Mir School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India A. I. Uba Department of Molecular Biology and Genetics, Istanbul AREL University, Istanbul, Türkiye W. M. Mahayu · Parnidi Research Centre for Horticulture and Plantation, National Research Innovation Agency, Bogor, Indonesia © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_8

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interaction of melatonin in fruit ripening in an ethylene-NO- H2O2-H2S -dependent manner via the various signaling pathways will be highlighted and presented. Keywords  Ethylene · Fruit · Nitric oxide · Ripening · Melatonin · Phytomelatonin · Signaling pathways · Hydrogen peroxide · Hydrogen sulphide

8.1 Introduction Melatonin is ubiquitously distributed in various parts of plants such as the shoots, the leaves, the seeds, and the fruits with poly functions in varying concentrations and involved in various aspects of plant development, biotic and abiotic stress stimuli (Reiter 2003; Hardeland 2009; Arnao 2014; Arnao and Hernández-Ruiz 2019; Liu et al. 2020, 2022; Moustafa-Farag et al. 2020; Sun et al. 2020; Khanna et al. 2021; Mannino et al. 2021; Corpas et al. 2022; LOSADA et al. 2022). The myriad roles of phytomelatonin are known to be achieved either via its direct metabolic pathway or through its indirect signaling routes (Arnao 2014; Corpas et al. 2022; Liu et al. 2022). Although the light and dark cycle appears to be the principal regulator of melatonin formation (Reiter 2003), the pineal gland in animals produces melatonin in large amounts only in darkness at night (Hardeland et al. 1995, 2006; Hardeland 2009). However, phytomelatonin production is not influenced by the pineal gland because plants are devoid of the pineal gland (Hardeland 2009; Arnao 2014). Following the identification of melatonin in 1958 by Lerner et al., the carefully identified compound appeared to be N-acetyl-5-methoxytryptamine capable of activating melanin aggregation and illuminating virtually all amphibians, however, the melatonin identified in 1958 in humans, N-acetyl-5-methoxytryptamine, was not capable of illuminating the skin of mammals (Lerner et al. 1958; Reiter 2003; Hardeland 2009; Mannino et al. 2021). The presence of melatonin in various birds, amphibians, and fishes, was reported in the 1960s and 70 s (Vivien-Roels and Pévet 1993; Mannino et al. 2021). In the 1980s, invertebrates were found to be the embodiment of melatonin (Vivien-Roels and Pévet 1993). Interestingly, phytomelatonin was endogenously investigated in tomato fruits and Convolvulaceae ivy morning glory by Tassel and O’Neill in 1993 using radioimmunoassay (RIA) and gas chromatography coupled with mass spectrometry (GC-MS) followed by publishing the outcomes of their research in 1995 (Vivien-Roels and Pévet 1993; Liu et al. 2022). Dubbels et al. revealed the phytomelatonin concentrations in extracts of nearly five edible plants as well as Nicotiana tabacum using RIA and HPLC-MS (high-­performance liquid chromatography with mass spectrometry) (Dubbels et  al. 1995). Hardeland et  al. reported the phytomelatonin levels in photoautotrophs which appeared to be an indicator of extraction efficiency (Hardeland et al. 1995, 2006; Hardeland 2009).

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Phytomelatonin has been by far identified for nearly three decades as having auxin activity, anticancer activity, and antioxidant property that surpasses the standard antioxidants such as ascorbic acid and trolox, thereby protecting and conferring the plants exposed to stressors including salinity, pollutants, extreme pH and temperature, drought, irradiation, among others, with the potentiality to be used as a biostimulant for managing the field crops (Pöggeler et  al. 1991; Reiter 2003; Arnao 2014; Turk et al. 2014; Arnao and Hernández-Ruiz 2019; Liu et al. 2022). Although phytomelatonin is widely distributed in all plants species so far examined, aromatic plants such as rosemary, oregano, laurel, fennel, thyme, parsley, basil, mint, lander, dill, among others aromatic plants, were reported to be the reservoir of phytomelatonin. Plants metabolites including flavonoids (anthocyanins, flavonols, and flavanones), organic acids, phenolic acids, tocopherols, and carotenoids have been documented and reported to have antioxidant activities as well as anticancer activities since antiquity (Arnao 2014; Liu et al. 2020, 2022; Sun et al. 2020; Corpas et al. 2022). In the same manner, the indolic compounds comprising IAA (indolyl-­3-­ acetic acid), IM (indole-3-methanol), IPA (indole-3- propionic acid), and IBA (indole-3-butyric acid) whose precursor appears to be an aromatic amino acid, tryptophan (W), are highly diverse and enormous in plants species (Arnao 2014; Basheer and Rai 2016; Khanna et al. 2021; Corpas et al. 2022; Liu et al. 2022). These secondary metabolites in plants were reported to have antioxidant activities, thus conferring protective effects on human well-being. Ethylene, being a plant hormone, is known to get involved in signaling pathways together with endogenous phytomelatonin that ultimately lead to control of plant development and fruit ripening as well senescence (Umeh 2017; Khanna et  al. 2021; Corpas et  al. 2022; Steelheart et al. 2022). Although the antioxidant activities of signaling molecules namely: phytomelatonin and ethylene in abrogating the pro-oxidant activities of signaling molecules particularly hydrogen peroxide (H2O2), nitric oxide (NO), hydrogen sulfide (H2S) are not fully understood, the way and manner these signaling molecules interact with one another has been deciphered to induce ripening of fruits (Adams-Phillips et al. 2004; Sun et al. 2015; Umeh 2017; Mukherjee 2019; Moustafa-Farag et al. 2020; Pardo-Hernández et  al. 2020; Khanna et  al. 2021; Corpas et  al. 2022; Steelheart et al. 2022; Usman et al. 2015). Therefore, harnessing the phytohormonal functions of melatonin in fruit ripening physiology via crosstalk with ethylene and NO as well as H2O2 is of biological importance in revealing the free radical scavenging role of phytomelatonin. In this chapter, the interaction of signaling molecules such as phytomelatonin and ethylene with those of signaling molecules particularly H2O2 and NO towards enhancing the fruits ripening and/or adjusting postharvest shelf life to prevent the deterioration of the fruit most notably tomatoes, grapes, bananas, mangoes, pawpaws, red bell peppers, lettuce, cabbage, among other fruits will be carefully evaluated and discussed.

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8.2 Physiology of Fruit Ripening Ethylene, phytomelatonin, NO, H2O2, and H2S have been by far known as the major players during various plant cellular and physiological processes particularly during fruit ripening and are currently at the forefront of fruit ripening physiology from different researchers worldwide (Adams-Phillips et al. 2004; Mukherjee 2019; Liu et al. 2020; Sun et al. 2020; Khanna et al. 2021; Corpas et al. 2022; LOSADA et al. 2022; Steelheart et al. 2022). Fruit ripening, being the final phase of plant development, involves a complex physiological process consisting of a series of events that precipitates the signaling molecules, especially H2O2, salicylic acid, NO, ethylene, abscisic acid, auxin, H2S, brassinosteroids, and jasmonic acid at different levels of gene and protein expression to initiate activation and/or deactivation of various signaling pathways that ultimately lead to the ripening of the fruits (Umeh 2017; Mukherjee 2019; Moustafa-Farag et al. 2020; Pardo-Hernández et al. 2020; Khanna et al. 2021; Corpas et al. 2022; Liu et al. 2022; Steelheart et al. 2022). Except for abscisic acid and strigolactones having phytomelatonin effect with synergistic inhibition on seed germination and antagonism of flowering respectively, virtually the effects of phytomelatonin on all signaling molecules including H2O2, H2S, salicylic acid, NO, ethylene, auxin, cytokinin, brassinosteroids, polyamines, and jasmonic acid, are involved in synergistic promotion of plants growth and development particularly the fruit ripening (Sun et al. 2020; Khanna et al. 2021; Corpas et al. 2022; Liu et al. 2022; Steelheart et al. 2022). Fruits are the embodiment of micronutrients especially vitamins, minerals, and fibers, even though fruits appeared to have a drastically shortest life span that ultimately leads to the loss of micronutrients that the fruits more often than not are meant to supplement (Liu et al. 2020; Sun et al. 2020; Corpas et al. 2022). Previously, substances including chemicals, waxes, plastic films, and adjuvants were used to mitigate the loss of micronutrients, thereby increasing the postharvest shelf life of fruits by delaying the ripening of the fruits (Vivien-Roels and Pévet 1993; Hardeland et al. 1995; Sun et al. 2015; Umeh 2017; Rodríguez-Ruiz et al. 2019; Liu et al. 2020; Corpas et al. 2022). However, these chemicals as well as adjuvants and plastic films used for delaying the fruit ripening are carcinogenic (Giovannoni 2007; Steelheart et al. 2022). With the advent of phytomelatonin which is a naturally occurring compound with wider acceptability globally, the life span of fruits was reported to dramatically get extended (Giovannoni 2007; Sun et al. 2015; Rodríguez-Ruiz et al. 2019; Liu et al. 2020). The physiological rationale behind the dramatic increase in the life span of fruits by phytomelatonin is not yet unveiled, however, it was observed that exogenous phytomelatonin was responsible for suppressing the function of the principal molecule (ethylene) for ripening of fruits through mitogen-activating protein kinases (MAPKs) pathway (Arnao 2014; Umeh 2017; Liu et al. 2022; LOSADA et al. 2022). Ethylene exposure to plants brings about their ripening instantly, suggesting that ethylene is the most potent molecule for fruit ripening. The series of the complex physiology of fruit ripening involving NO, H2S, and H2O2 signaling molecules appears to regulate not only the ripening of fruits by promoting the gene expression of enzymes involved in the direct metabolic pathway of

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H N

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H CO 2 melatonin

BR IAA + JA

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HN

CH O

NO2H2O2 and H2S

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Fig. 8.1 Concept of fruit ripening in NO-H2O2-H2S-melatonin-ethylene-dependent fashion. + activation, BR brassinosteroid, IAA indole-3-acetic acid, JA jasmonic acid

phytomelatonin biosynthesis thereby enhancing the formation of ethylene but also positively regulating the plant developmental stages including modification of cell wall, growth of root, germination of seed, differentiation of xylem and closure of stomata (Pardo-Hernández et al. 2020; Khanna et al. 2021; Corpas et al. 2022; Liu et al. 2022; Steelheart et al. 2022). Therefore, phytomelatonin interacts with many signaling molecules such as antioxidants particularly ethylene, auxin (IAA), and brassinosteroids as well as prooxidants including NO, H2O2, and H2S to precipitate a complex physiological reaction that ultimately leads to ripening of the fruits as depicted in Fig. 8.1.

8.2.1 Microbial Genesis of Fruit Spoilage and Its Inhibition by Phytomelatonin, and Other Biomolecules During Fruit Ripening Microorganisms adapt to various conditions through the cascade of genetic pathways (Wani et al. 2022a; Akhtar et al. 2022). They produce several molecules and toxins beneficial in drug formulation, but harmful in inducing food spoilage (Abdel-­Mohsein et al. 2010; Wani et al. 2021). Microbial contaminants account for nearly 20% of fruits and vegetables spoilage harvested for human consumption worldwide (Arnao 2014; Sun et  al. 2015; Umeh 2017; Rodríguez-Ruiz et  al. 2019; Moustafa-­Farag et  al. 2020). However, phytomelatonin appears to defend the plants against microbial attacks by positively regulating the activities of salicylic acid, ethylene, abscisic acid, auxin, brassinosteroids, jasmonic acid, among other phytohormones(Rodríguez-Ruiz et  al. 2019;

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Corpas et al. 2022; Liu et al. 2022). Phytomelatonin has been by far reported to have phyto-antimicrobial activities against both Gram-positive and Gram-negative bacteria including multi-drug-­resistant (MDR) bacteria; viruses including tobacco mosaic virus, fungi including Botrytis cinerea (Arnao 2014; Umeh 2017; Moustafa-Farag et al. 2020). Microbial contaminants were reported to be associated with the spoilage of fruits (Umeh 2017; Moustafa-Farag et al. 2020). This provides evidence that phytomelatonin is capable of delaying fruit ripening (Sun et al. 2015; Rodríguez-Ruiz et al. 2019; Corpas et al. 2022; Liu et al. 2022). In the same manner, ethylene, NO, H2O2, and H2S are ubiquitously considered gaseous transmitters or signaling molecules in plants. They are devoted to regulating either positively or negatively, or both, of plant developmental processes including germination, senescence, defense, and maturation thereby promoting fruit ripening along with the quality of fruits (Turk et  al. 2014; Umeh 2017; Rodríguez-Ruiz et al. 2019; Moustafa-Farag et al. 2020; Pardo-Hernández et al. 2020; Khanna et al. 2021; Corpas et al. 2022; Steelheart et al. 2022). By being in a gaseous state, they are capable of diffusing from one region of plants to another thereby crosstalking with phytomelatonin that is ubiquitously distributed in various parts of plants such as the shoots, the leaves, the seeds, and the fruits to bring ripening of fruits about that ultimately associated with maintaining the quality features of fruits(Giovannoni 2004; Sun et al. 2015, 2020; Umeh 2017; Liu et al. 2020; Moustafa-Farag et al. 2020; Corpas et al. 2022; Steelheart et al. 2022). Equally, as ethylene, NO, H2O2, and H2S are moving from one region to another throughout the plant system, the pathogens encountered along the way are completely aborted probably by counterbalancing the pro-­ oxidant/antioxidant pools as well as post-­ translationally modifying the microbes’ architecture to be attractive to ubiquitination that ultimately leads to proteasomal degradation of microbial contaminants(Umeh 2017; Moustafa-Farag et  al. 2020; PardoHernández et al. 2020; Khanna et al. 2021; Corpas et al. 2022; Steelheart et al. 2022). This, in turn, activates the plant tolerance to not only the microbes but also adverse conditions by regulation of the system, oxidative stress signaling, antioxidative defense, homeostasis, and metal transport, among others (Arnao 2014; Arnao and HernándezRuiz 2019; Pardo-Hernández et al. 2020; Corpas et al. 2022) to cause fruits ripening with superb quality features of the fruits as depicted in Fig. 8.2.

8.2.2 Biochemical Basis of Fruit Ripening Mediated by Interaction of Melatonin, Ethylene, NO, H2O2 and H2S Although phytomelatonin has potent antioxidant activity, it causes the production of stress-induced ROS (reactive oxygen species) and RNS (reactive nitrogen species) through mainly its direct metabolic pathway (Mukherjee 2019; Rodríguez-Ruiz et al. 2019; Corpas et al. 2022; Liu et al. 2022). The generation of H2O2 and NO via stress-induced ROS and RNS respectively by phytomelatonin through its direct metabolic pathway dramatically induces the ripening of fruits especially tomato in an ethylene-dependent fashion (Mukherjee 2019; Rodríguez-Ruiz et al. 2019; Liu et al. 2022; Steelheart et al. 2022). However, induction of NO and/or hydrogen sulfide (H2S) synthesis by phytomelatonin direct metabolic pathway during the

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Microbial Contaminants

ge ila po it s Fru +

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Fig. 8.2  Concept of inhibition of fruits spoilage by microbial contaminants with a concomitant ripening that maintained the quality features of the fruits. + activation, – inhibition

ripening of fruits is not so understood as that of H2O2 (Turk et al. 2014; Mukherjee 2019; Khanna et al. 2021; Corpas et al. 2022; Steelheart et al. 2022). Regulation of fruit ripening by phytohormones including brassinosteroids, melatonin, abscisic acid, auxin, jasmonic acid, and salicylic acid is of significant importance in the maintenance of the quality traits as well as minimizing postharvest damage (Černý et al. 2018; Liu et al. 2020; Sun et al. 2020; Khanna et al. 2021; Corpas et al. 2022). The indolic compounds comprising IAA, IM, IPA, and IBA whose precursor appears to be tryptophan (W), an aromatic amino acid, being highly distributed in plants species were reported to influence the ripening of fruits (Černý et al. 2018; Mukherjee 2019; Khanna et al. 2021; Liu et al. 2022). Fruit ripening cannot take place without ethylene because its deficiency and/or drastic decrease in its sensitivity has been reported to abrogate fruit ripening (Rodríguez-Ruiz et al. 2019; Corpas et al. 2022; Steelheart et al. 2022). This is likely by dint of deficiency of the two committed steps enzymes devoted to the biosynthesis of ethylene namely: (1) ACS (Aminocyclopropane Carboxylate Synthase); (2) ACO (Aminocyclopropane Carboxylate Oxidase); capable of involving in system 1 and system 2 as well as stress-induced ethylene synthesis (Sun et al. 2015; Houben and Van de Poel 2019; Liu et al. 2020; Liu et al. 2022). However, ACS and ACO activities were reported to be significantly (27.1%) induced by phytomelatonin thereby dramatically activating the formation of ethylene (Liu et al. 2022). Therefore, the effect of phytomelatonin in fruit ripening physiology from the biochemical point of view involves the activation of the two committed steps enzymes of ethylene biosynthesis namely ACS and ACO.

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8.2.3 Molecular Fundamentals of Fruit Ripening and Genetic Regulation of Melatonin, Thylene, NO, H2O2 and H2S Synthesis Molecular biology methods for fruit ripening depicted the downregulation of genes encoding the enzymes responsible for ethylene biosynthesis, particularly the downregulation of genes devoted to encoding ACS and ACO enzymes, the two committed steps enzymes of ethylene biosynthesis, as reported elsewhere would delay the fruit ripening (Giovannoni 2007; Houben and Van de Poel 2019; Liu et  al. 2020, 2022). However, the application of ethylene exogenously to such genetically engineered fruits using molecular approaches resulted in their ripening. This implies that ethylene is the principal catalyst of fruit ripening(AdamsPhillips et  al. 2004; Giovannoni 2004, 2007; Liu et  al. 2022). Importantly, however, exogenous application of phytomelatonin in mango fruit appears to halt the ripening of the mango fruits probably by negatively regulating ACS and ACO genes as well as pectin-­modifying enzymes (Liu et al. 2020, 2022). Conversely, exogenous application of phytomelatonin in tomato appears to downregulate DNA methylation of CpG islands in SlACS10 and SlERF-A1 genes but DNA methylation of CpG islands in SlCRT1 is upregulated thereby activating the expression of SlACS10, SlEIN3, SlERF-A1, SlACO, SlACS, and SlERT10 genes while deactivating the expression of SlCT1 gene, which all together bring about the induced biosynthesis of ethylene with dramatic improvement in the quality of tomato (Adams-Phillips et  al. 2004; Giovannoni 2004; Giovannoni 2007; Mukherjee 2019; Liu et al. 2020, 2022). Therefore, DNA methylation appears to regulate numerous pathways of genetic material stability, gene expression, and histone modification particularly during plant growth and development (Giovannoni 2004; Liu et al. 2022). Incorporation of NO, H2O2, and H2S as transcriptional factors followed by their interactions with the promoter region of genes of phytomelatonin and/or ethylene particularly in the CpG islands is reported to abrogate the DNA methylation and by so doing promote the expression of phytomelatonin and ethylene (Liu et al. 2022). Therefore, DNA methylation is associated with a decrease in gene expression in contrast to DNA hypomethylation/demethylation which is associated with an increase in gene expression.

8.3 Crosstalk of Melatonin, and Other Relevant Signaling Molecules During Fruit Ripening Proper understanding of the crosstalk of phytomelatonin with ethylene and NO as well as other signaling molecules particularly H2O2 and H2S during fruit ripening would greatly widen the horizon of postharvest biologists to carefully take into cognizance the way and manner to prevent the deterioration of the fruit most

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notably tomatoes, grapes, bananas, mangoes, pawpaws, red bell peppers, lettuce, cabbage, among others. The crosstalk between phytomelatonin and ethylene, NO, H2O2, and H2S as well as other phytohormones including salicylic acid, auxin, brassinosteroids, jasmonic acid is discussed as follows: Although the interaction between phytomelatonin, ethylene, NO, H2O2, and H2S is not fully understood, it is evident that abiotic stress stimuli (salinity, pollutants, extreme pH and temperature, drought, irradiation) interact with a stressinduced receptor (SIR) which causes the imbalance between pro-oxidant and antioxidants (Arnao 2014; Turk et  al. 2014; Arnao and Hernández-Ruiz 2019; Mukherjee 2019; Rodríguez-Ruiz et al. 2019; Khanna et al. 2021; Corpas et al. 2022; Liu et  al. 2022; Steelheart et  al. 2022). The phytohormonal functions of melatonin in fruit ripening physiology via crosstalk with these new emerging signaling molecules particularly ethylene, NO, H2O2, and H2S is of biological importance in revealing the free radical scavenging role of phytomelatonin. NO and H2O2 and H2S are considered to be the end-products of reactive nitrogen species (RNS) and reactive oxygen species (ROS) respectively, capable of disturbing the balance between pro-oxidants (such as malondialdehyde, NO, H2O2, H2S, hydrogen radical, hydroxyl radical and superoxide anion radical) and antioxidants (nonenzymatic such as glutathione reduced form, melatonin, ascorbic acid, trolox and ethylene; enzymatic including catalase, superoxide dismutase, glutathione peroxidase and glutathione reductase) (Arnao 2014; Mukherjee 2019; Sharif Usman et al. 2019; Liu et al. 2020, 2022; Corpas et al. 2022). NO, H2O2, and H2S, being the end-products of highly-branched biochemical pathways, remain the most suitable form of pro-oxidants in both plants and animals. However, their conversion into either NO● (nitric oxide radical), ●OH (hydroxyl radical), or H● (hydrogen radical) appears to be dangerous, especially ●OH which is by far the most catastrophic free radicals ever identified (Turk et al. 2014; Sharif Usman et al. 2019; Pardo-Hernández et  al. 2020; Khanna et  al. 2021; Steelheart et  al. 2022). Importantly, enzymatic and/or non-enzymatic antioxidants including catalase, superoxide dismutase, peroxidase, glutathione reductase, and/or glutathione reduced form, melatonin, ascorbic acid, trolox and ethylene, among other antioxidants, counterbalance the effect of NO, H2O2, and H2S (Mukherjee 2019; Sharif Usman et  al. 2019; Khanna et  al. 2021; Corpas et  al. 2022; Liu et  al. 2022; Steelheart et al. 2022). Furthermore, phytomelatonin is capable of positively regulating glutathione reduced form, ascorbic acid, trolox, and ethylene; catalase, superoxide dismutase, peroxidase, glutathione reductase, among other antioxidant defense systems against different abiotic stresses including salinity, pollutants, extreme pH and temperature, drought, irradiation, among others (Arnao 2014; Arnao and Hernández-Ruiz 2019; Mukherjee 2019; Sharif Usman et  al. 2019). Therefore, nitro-oxidative stress can be prevented in the presence of antioxidants, thereby restoring the balance between pro-oxidants and antioxidants to normal. It is abundantly clear that NO generates S-nitrosation proteins by covalently getting attached to cysteine residues of proteins or peptides as well as H2S, henceforth, proteins or peptides rich in cysteine residues are the embodiment of NO owing to the covalent attachment of NO in an S-nitrosation-dependent

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Fig. 8.3  Crosstalk between phytomelatonin and signaling molecules via SIR and PMTR1/ CAND2. ACS aminocyclopropane carboxylate synthase, ACO aminocyclopropane carboxylate oxidase, BR brassinosteroid, CK cytokinin, IAA indole-3-acetic acid, JA jasmonic acid, MAPKs mitogen-activating protein kinases, PMTR1/CAND2 phytomelatonin receptor, SA salicylic acid, SIR stress-induced receptor, + activation, – inhibition

manner (Umeh 2017; Liu et al. 2020, 2022; Usman et al.). This crosstalk of H2S, NO, and H2O2 with just mentioned signaling molecules favors H2S-Cys-cycle during abiotic stressed conditions that consequently mediates the S-nitrosation proteins and peptides as well. Interactions of H2S, NO, and H2O2 with phytohormones including melatonin, ethylene, abscisic acid, salicylic acid, auxin, brassinosteroids, jasmonic acid, among others, have been well documented and reported (Mukherjee 2019; Liu et  al. 2022). The crosstalk between phytomelatonin and ethylene, NO, H2O2, and H2S as well as other phytohormones including salicylic acid, auxin, brassinosteroids, and jasmonic acid is depicted in Fig. 8.3.

8.4 Conclusion and Future Perspectives Taken together, the crosstalk between phytomelatonin and signaling molecules particularly ethylene, NO, H2O2, and H2S, as well as other phytohormones including abscisic acid, salicylic acid, auxin, brassinosteroids, and jasmonic acid, involve activation of inactive stress-induced receptors especially by biotic and abiotic stressors such as salinity, pollutants, extreme pH and temperature, drought, irradiation which causes the imbalance between pro-oxidants and antioxidants in favor of elevation of

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ROS and RNS which consequently leads to induction of NO, H2O2, and H2S that ultimately brings about upregulation of phytomelatonin direct pathway genes. The upregulation of phytomelatonin direct pathway genes causes the activation of endogenous phytomelatonin biosynthesis which in turn not only feedback inhibits the production of ROS and RNS but also activates the production of both enzymatic antioxidants including catalase, superoxide dismutase, glutathione peroxidase, and glutathione reductase; and non-enzymatic antioxidants such as glutathione reduced form, melatonin, ascorbic acid, trolox, and ethylene. In addition, endogenous phytomelatonin induces the activities of ACS and ACO, the two committed steps enzymes devoted to the biosynthesis of ethylene, which lead to a marked elevation of ethylene synthesis. Both endogenously synthesized phytomelatonin and ethylene are potent inhibitors of senescence and at the same time the powerful activator of fruit ripening. Exogenous phytomelatonin application binds to PMTR1/CAND2 which is intrinsically capable of activating MAPKs pathway with a concomitant delay in fruit ripening. Incorporation of molecular biology tools including genomics, metagenomics, epigenetics, and CRISPR/Cas9 engineering approaches would open up new perspectives to decipher the complex network of crosstalk (Wani et al. 2022c, b; Mir et al. 2022). Phytomelatonin and new emerging signaling molecules such as H2S, NO, H2O2, and ethylene as well as regulatory elements that downregulate DNA methylation at the promoter region, especially in the CpG islands of the genes encoding the biosynthesis of ethylene and phytomelatonin could be the key to understanding the fruit-ripening physiology.

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Chapter 9

Melatonin and Postharvest Biology of Fruits and Vegetables: Augmenting the Endogenous Molecule by Exogenous Application Abdullahi Ibrahim Uba, Atif Khurshid Wani, and Sani Sharif Usman Abstract  The physiological process of ripening occurs rapidly when fruits and vegetables become mature, and beyond a specific stage after the harvest, they to undergo rapid deterioration in quality. Melatonin, a nontoxic biological molecule with significant antioxidant capacity, plays several roles, including delaying senescence, alleviating chilling injury, enhancing resistance to diseases, and tolerance to stress conditions during postharvest preservation of fruits and vegetables. Interestingly, the application of exogenous melatonin to prolong the shelf life of fruits and vegetables augment the endogenous molecule, thereby promoting these functions. There is crosstalk among different physiological and biochemical processes involved in melatonin action, which remain largely elusive. This chapter provides insights into those mechanisms and discusses several case studies demonstrating the promising effects of melatonin treatment on the postharvest preservation of fruits and vegetables. Keywords  Melatonin · Postharvest biology · Fruits and vegetables · Crosstalk, melatonin augmentation

A. I. Uba (*) Department of Molecular Biology and Genetics, Istanbul AREL University, Istanbul, Türkiye e-mail: [email protected] A. K. Wani Department of Biotechnology, School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India S. S. Usman Department of Molecular Biology and Genetic Engineering, School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India Department of Biological Sciences, Faculty of Science, Federal University of Kashere, Kashere, Gombe, Nigeria © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_9

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9.1 Introduction Melatonin (N-acetyl-5-methoxytryptamine) is a neurohormone discovered in the bovine pineal gland in 1965 (Lerner et  al. 2002; Reiter 1991). It is a ubiquitous molecule released primarily by the pineal gland in the brain in response to darkness, usually at night—hence functions to regulate circadian rhythms, thereby synchronizing the sleep/wake cycle (Auld et al. 2017). Until the identification and quantification of melatonin in plants in 1995 (Dubbels et al. 1995), it was thought to be produced primarily by animals. It is now common knowledge that several organisms, ranging from microbes (including bacteria and fungi) to higher animals and plants produce melatonin. It performs several physiological functions in plants, which include maintenance of the integrity of cell structure, protection of DNA from damage (Arnao and Hernández-Ruiz 2014), and removal of free radicals to reduce lipid peroxidation (Zheng et al. 2019). Having been extracted from different parts of the plants studied so far (Setyaningsih et  al. 2012), melatonin has been shown to play vital roles including seed germination (Hardeland 2016), delaying leaf senescence (Liang et al. 2015; Wang et al. 2012, 2013), root development and architecture (Liang et al. 2017; Zhang et al. 2014). Also, melatonin enhances plant tolerance to biotic and abiotic stress (Debnath et al. 2019; Wang et al. 2012, 2013; Zhang et  al. 2014). Enhancement of plant tolerance to stressors including heavy metal stress, drought conditions, and high salinity is important for proper growth (Akhtar et  al. 2022). Increased melatonin production is observed in transgenic plants. For instance, transgenic Arabidopsis was found to have elevated melatonin levels, which in turn is associated with drought tolerance enhancement (Zuo et al. 2014; Yang et  al. 2019b). SNAT gene-overexpressing alfalfa exhibited increased tolerance to cadmium compared with the wild-type (Gu et  al. 2017). In another instance, the upregulation of ovine HIOMT and AANAT genes in switch grass is associated with increased salt tolerance (Huang et al. 2017). During fruit ripening, there are changes in physiological and biochemical processes, resulting in various development of various features. After pollination and fertilization, the size of the fruits becomes bigger triggering the ripening process, resulting in the development of organoleptic features (Rekhy and McConchie 2014). A significant portion of harvested fruit and vegetables get wasted due to postharvest decay (Romanazzi et  al. 2016; Feliziani and Romanazzi 2016; Rajestary et  al. 2020), which occurs as a result of continuous utilization of own nutrients via respiration, which in turn causes destruction of chlorophyll, softening of the cell wall, and membrane penetration (Barrett and Lloyd 2012). Also, the effects of changes in temperature, humidity, and air composition continuously reduce the nutritional value of fruits and vegetables (Zainalabidin et al. 2019). Therefore, to prolong the preservation period, methods including controlled atmosphere storage (Caleb et al. 2012), edible coatings (Gol et al. 2013) ventilation storage, and refrigeration (Lal Basediya et al. 2011), and application of chemicals such as Hydrogen sulfide (H2S), Sulfur dioxide (SO2) (Sivakumar et  al. 2010; Cantín et  al. 2012), short water

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brushing treatment and more, have been employed (Molinett et  al. 2021; Mayer et al. 2018; Porat et al. 2000; Mahajan et al. 2014). Interestingly, melatonin serves as a nontoxic substance that functions as an environmentally friendly chemical to control the postharvest decay of fruits and vegetables. For instance, exogenous melatonin was demonstrated to have tolerance enhancement effects on abiotic stress in crops, vegetables, and fruits by activating a series of downstream signaling (Zhan et al. 2019). These prominent effects include tolerance to salt stress demonstrated by strawberries (Fragaria × ananassa Duch.) (Nimbolkar et al. 2020), tolerance to high-temperature displayed by cucumber seedlings (Hu et al. 2010; Yu et al. 2018), and low-temperature stress tolerance of tea plant (Li et al. 2018) and tomato (Qi et al. 2018). Also, tolerance to heavy metals has been reported; like in the case of cadmium tolerance of tomatoes (Hasan et al. 2015) and vanadium tolerance of watermelon seedlings (Nawaz et al. 2018) (Fig. 9.1). Moreover, melatonin induces the biosynthesis of other plant hormones like salicylic acid (SA) and jasmonic acid (JA), initiating cascades that trigger pathogen-­ induced responses in postharvest fruits and vegetables (Lee and Back 2016). The

Fig. 9.1  Functions of melatonin in fruit plant: root development and architecture, germination, and development of leaf, delaying leaf senescence, enhancing disease resistance, and alleviating chilling injury in postharvest fruits

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details of the interaction of melatonin with reactive oxygen and nitrogen species such as hydrogen peroxide (H2O2), nitric oxide (NO), and hydrogen sulfide (H2S) have been discussed elsewhere (Aghdam et al. 2021). Melatonin also interacts with the gaseous hormone ethylene, which promotes ripening in fruits such as apples (Verde et al. 2022). For instance, immersion treatment of bananas with melatonin (0.05 to 0.5  mM) reduced ethylene biosynthesis, thereby delaying ripening (Hu et al. 2017). Immersion melatonin treatment (0.1 Mm) delayed the ripening of pear fruit by suppressing the expression of PcACS1, PcACO1, and PcPG (Zhai et  al. 2018). In another study, ethylene climacteric was induced following treatment with exogenous melatonin (Sun et  al. 2015). Melatonin protects fruits and vegetables against pathogens (Shi et al. 2015; Liu et al. 2019a). Other functions of melatonin include but are not limited to the alleviation of chilling injury mainly via exhibiting remarkable antioxidant effects (Bhardwaj et al. 2022). Both inductions of endogenous melatonin and application of exogenous melatonin are effective in regulating the postharvest quality of produce. Interestingly, the endogenous melatonin is augmented by the exogenous application. The modulatory roles of melatonin in several physiological and biochemical processes point to the crosstalk with different players involved, and the mechanisms largely remain unclear. In this chapter, those mechanisms were elucidated based on specific roles of melatonin relevant to the postharvest prolongation of shelf life and quality of fruits and vegetables. Moreover, several case studies that demonstrated promising effects of melatonin treatment on postharvest preservation of fruits and vegetables are discussed.

9.2 Postharvest Biology of Fruits and Vegetables Fruits and vegetables have become important dietary choices, primarily because of their several health benefits due to their enriched biochemical composition and nutritional properties. They have evolved features such as attractive colors, pleasant scent, and taste, that allow them to attract vectors for seed dispersal (Yahia 2019). While fruits generally develop from the ovary, pome fruits like apples and nashi grow from the thalamus. Cherries, and peaches, which are the typical example of dupe fruits, develop into a seed. Tomato and grape, which belong to berry fruits, have their seed within a very jellylike pectinaceous matrix, and their fleshy part is developed from the ovary wall. Citrus fruits belong to the category referred to as hesperidium, with a protective structure enclosing the edible part of the fruits called juice-filled locules. The seed can also be located outside the fruit, with the ovary receptacle developing into the edible part as exemplified by the case of strawberry. Vegetables are mainly of leaf and flower origin, and typical examples are cabbage and broccoli, which belong to the Cruciferae family. Roots, and tubers such as potatoes and yams belong to Dioscoreaceae and Araceae family while eggplant is classified as Solanaceae (Liu 2013).

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Postharvest preservation is a longstanding practice in human history. Postharvest science is a field of study that deals with the physiology of preserving the quality of horticultural crops. Over the last two decades, the use of molecular tools in addressing postharvest issues has remarkably increased. Postharvest decay poses a serious threat to farmers and has therefore become an important issue worldwide. Postharvest losses are minimal in those parts of the globe where advanced technology is used to preserve produce. Early harvest of fruits used as vegetables are necessary before ripening. As soon as the fruit becomes mature, the process of ripening proceeds, which is followed by deterioration postharvest. Therefore, on reaching optimal maturity, fruits are harvested and suitable storage procedures are used to preserve their shelf life and quality (Ziv and Fallik 2021). However, some fruits such as avocados are not allowed to ripen fully, instead, are harvested as soon as they display acceptable quality characteristics before the attainment of physiological maturity (Moirangthem and Tucker 2018). Regardless of the properties of the product, various technologies like cold storage (Zhang et al. 2017b), controlled atmosphere storage (Caleb et al. 2012), and alteration of biochemical processes (Pérez-Llorca et al. 2019) are used to produce quality products with prolonged shelf life enough to allow for marketing, and subsequently, consumption. During ripening, several metabolic processes occur, including ethylene production. Based on the response to the indigenous production of ethylene and its exogenous application, fruits are generally classified as ‘climacteric’ and ‘non-climacteric’ ones. Those fruits that evolve high concentrations of ethylene, which occurs with an increase in respiration during ripening, are termed respiratory climacteric. For example, in climacteric fruits like apples and tomatoes, ethylene can evolve up to 30–500 ppm/(kg h) (El-Ramady et al. 2015). In contrast, the evolution of ethylene in non-climacteric fruits such as strawberries and citrus during ripening is considerably low (Pérez-Llorca et al. 2019).

9.3 Melatonin Exhibits High Antioxidant Effects and Delays Senescence Several plants metabolites have been shown to have significant antioxidant capacity which is attributed to their chemical structures (Uba et al. 2022; Świątek et al. 2022; Zengin et al. 2022b; Kurt-Celep et al. 2022; Zengin et al. 2022a). Similarly, melatonin functions as a hydroxyl radical scavenger; this is directly attributed to its chemical structure (Poeggeler et  al. 1993; Poeggeler et  al. 1999; Reiter et  al. 2000; Poeggeler et  al. 2006; Purushothaman et  al. 2020). Cyclic-3-hydroxy melatonin (c3OHM) is a melatonin metabolite produced by melatonin photodegradation and functions to protect against oxidative damage. Exogenous melatonin treatment delays postharvest senescence in apples (Wang et al. 2013) and in peach fruits (Gao et  al. 2016). These effects were attributed to the reduction of ROS levels and

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enhancement of the activities of APX, dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDAR), and glutathione reductase (GR) (Wang et al. 2012, 2013). During senescence, there is a significant accumulation of reactive oxygen species (ROS) and reactive nitrogen species (RNS) increased membrane lipid peroxidation, which in turn leads to an increase in cell membrane permeability. ROS accumulation induces senescence in fruits and vegetables (Shewfelt and del Rosario 2000). As demonstrated very recently, ROS and hydrogen peroxide (H2O2) levels gradually increased with fruit ripening but then got lowered significantly after melatonin treatment (Fan et al. 2022). Similarly, melatonin lowers the level of O2− throughout the storage period of guava fruit. The authors also revealed that the total antioxidant capacity (T-AOC) of guava fruits, which is known to decrease gradually over time storage, retained an increased capacity during the first week of storage following the exogenous application of melatonin. Furthermore, Malondialdehyde (MDA), which is an indicator of lipid peroxidation (Sharif Usman et al. 2019), and whose content is usually high as the fruit ripens, was reported to have reduced after exogenous melatonin administration, indicating reduced peroxidation in the fruits (Fan et al. 2022). Melatonin exhibits antioxidant roles by promoting the expressions and enhancing the activity of antioxidant enzymes: catalase, superoxide dismutase, glutathione reductase, and ascorbate peroxidase (Ma et al. 2021). This property allows melatonin to alleviate the postharvest decay of wax apples (Chen et al. 2020). Postharvest treatment with melatonin delayed cassava root deterioration by lowering the accumulation of H2O2 (Zhang et al. 2016). Melatonin also caused senescence delay in pitaya fruits (Ba et al. 2022) through inhibition of ethylene production (Hu et al. 2017). Similarly, the antioxidant function of melatonin in preventing the postharvest decay of strawberry fruit (Ma et al. 2016) and jujube fruit (Zhang et al. 2022). An increase in the ascorbic acid production and enhanced activities of superoxide dismutase were observed in a fruit following melatonin treatment (Zhang et al. 2022). Melatonin treatment delayed senescence and reduced the production of MDA, O2·-, and H2O2 in peaches (Gao et al. 2016). Melatonin induces the accumulation of phenolic compounds. The phenolics content of nectarine fruits increased during the first 10 days of storage but started to decrease at about 40 days due to an increase in polyphenol oxidase activity. The rate at which this decrease occurs is lowered by melatonin by suppressing the activity of this enzyme (Rastegar et al. 2020). A significant increase in phenolic acid content was observed in sweet cherries following melatonin treatment. Phenolic acid is a strong non-enzymatic antioxidant responsible for the several health benefits of cherry fruit (Gonçalves et  al. 2018). It was shown that the nutritional quality of sweet cherries depends on both preharvest and postharvest melatonin treatments (Michailidis et  al. 2019; Michailidis et  al. 2020). Furthermore, UPLC–MS/MS analysis revealed a total of 28 phenolic compounds in “Ferrovia” cherries whose content remarkably increased during cold storage. Interestingly, procyanidin B1, procyanidin B2 + B4, ferulic acid, vanillin, and cyanidin-3-O-sambubioside) were found to increase at harvest; 11 phenolic compounds: rutin neochlorogenic acid, chlorogenic acid, epicatechin, procyanidin B1, procyanidin B2  +  B4,

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cyanidin-3-O-glucoside, cyanidin-3-O-galactoside, cyanidin-3-O-rutinoside, phloridzin, and quercetin-3,4-O-diglucoside, were induced melatonin treatment after cold (Michailidis et al. 2021). Consistently, postharvest melatonin treatment promoted the expression of genes involved in anthocyanin biosynthesis (Miranda et al. 2020). Finally, a comprehensive analysis of data from 36 articles using 24 indicator parameters relating to the antioxidant properties and postharvest quality of fruits shows that endogenous melatonin production is augmented by the application of the exogenous one (Madebo et al. 2022). That exogenous melatonin increased endogenous melatonin levels by up-regulating the expression of SlTDC, SlSNAT, and SlASMT genes in fruit postharvest (Li et al. 2022a). Figure 9.2 describes the mechanisms of melatonin-mediated post-harvest physiological signaling.

Fig. 9.2  Postharvest treatment of melatonin and working mechanism. Melatonin, acting upstream of the defense gene signaling pathway, induces the expression of nitric oxide (NO)- and salicylic acid (SA), jasmonic acid (JA), and ethylene-related genes, which in turn work to increase resistance to pathogens. Melatonin exhibits antioxidant roles by enhancing the activity and promoting the expressions of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), glutathione reductase, and ascorbate acid peroxidase (APX), and non-enzymatic antioxidants such as phenol, flavonoid, anthocyanin. Melatonin has been shown to improve the GABA shunt pathway by increasing the activity of the GABA transaminase (GABA-T) enzyme. Together, these mechanisms promote the postharvest preservation of fruits and vegetables

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9.3.1 Melatonin Alleviates Chilling Injury Some sensitive species of fruits and vegetables often undergo a variety of physiological/biochemical changes during postharvest cold storage in response to exposure to low temperatures, resulting in weakened tissues. Eventually, these alterations lead to the development of chilling injury, whose symptoms include failure to ripen, discoloration, loss of flavor, wilting, and decay (Wang 1989). The strategies used to prevent the deterioration of fruits include the application of chemicals including methyl jasmonate (González-Aguilar et al. 2000), salicylic acid (Ding et al. 2007), nitric oxide (Zaharah and Singh 2011), 2,4-dichlorophenoxyacetic acid (Wang et al. 2008), ether (Nair et  al. 2015), oxalic acid and low-temperature conditioning (Zahedi et  al. 2019), and chitosan and polyamine coating (Zhang et  al. 2017b). Although these methods have remarkably assisted in alleviating chilling injury in fruits, there are negative effects. For instance, excessive 2,4-dichlorophenoxyacetic acid is associated with toxicity in humans (Wang et al. 2008). Elevated levels of nitric oxide and polyamine coating reduce fruit respiration and ethylene production in mangoes, thereby causing poor coloration (Zaharah and Singh 2011; Zahedi et al. 2019). Melatonin treatment is promising for alleviating chilling stress by influencing the expression of the enzyme involved in the biosynthesis of melatonin, resulting in an increase in the levels of endogenous melatonin (Liu et al. 2011). This effect has been demonstrated in the form of cucumber alleviation of chilling injury in cucumber seedlings (Zhang et al. 2021), tomatoes (Jannatizadeh et al. 2019), and litchi fruits (Wang et  al. 2020). The biochemical changes occurring during these processes include the promotion of intracellular ATP supply by elevating the activity of HC-ATPase, and other enzymes. Similarly, melatonin treatment alleviated the chilling effects in two mango cultivars (Bhardwaj et  al. 2022). During cold storage, melatonin enhances energy metabolism to maintain the integrity of the cell membrane, releasing energy into the membrane (Sondergaard et al. 2004). Ca2+-ATPase pumps Ca2+ ion across the membrane, releasing the energy from ATP hydrolysis that regulates the level of Ca2+ ion in the extracellular matrix, causing adjustment in the physiological processes, enabling the postharvest fruits to resist stress (Zhang et al. 2017a).

9.3.2 Melatonin and GABA Shunt Pathway γ-Aminobutyric Acid (GABA) is a non-proteinogenic amino acid yielded by the GABA shunt of the citric acid cycle pathway (Bown and Shelp 1997). The activity of this pathway is crucial in preserving the quality of fruits and vegetables during postharvest cold storage (Han et al. 2018). The pathway can reduce sensitivity to environmental stress in some mutant plants (Bouché et al. 2003; Bouché and Fromm 2004). Melatonin can increase the activity of the GABA transaminase (GABA-T)

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enzyme, enabling fruits and vegetables to produce more ATP used in the removal of excess ROS (Carvajal et al. 2015). GABA shunt pathway reduced the postharvest deterioration of strawberry fruits (Aghdam and Fard 2017). Exogenous application of melatonin stimulates the production of endogenous melatonin (Szafrańska et al. 2016) and GABA (Wang et al. 2016). GABA shunt pathway promotes stress tolerance via osmoregulation (Kinnersley and Turano 2010; Barbosa et  al. 2010; Shi et al. 2010). GABA shunt pathway activity associated with increased glutamate decarboxylase (GAD), GABA-T, and SSADH enzymes activities in tomato fruits following treatment with melatonin, may be due to an increase in cytosolic Ca2+ upon melatonin detection on the cell membrane by PMTR1 receptor. PAL enzyme activity supplies sufficient NH4+ ion—vital for generating the glutamate via GS/GOGAT cycle that is used in the GABA shunt pathway (Aghdam and Fard 2017). The increased activity of the GABA shunt pathway following melatonin treatment is associated with the amelioration of fungal deterioration in strawberry fruits. Therefore, melatonin treatment of fruits is associated with extended postharvest shelf life in low-­ temperature (4 °C) storage, which is attributed to the increased GABA content, fatty acid ratios, and higher ATP generation and maintenance in fruits (Gao et al. 2018; Cao et al. 2018).

9.3.3 Postharvest Melatonin Treatment Induces Disease Resistance Pathogen infection is usually accompanied by the postharvest decay of fruits and vegetables. Melatonin inhibits a wide range of pathogenic infections by modulating immune and inflammatory processes (Yin et al. 2013). Therefore, the antimicrobial activities of melatonin against different fruit pathogens have been reported (Liu et  al. 2019a; Shi et  al. 2015). Melatonin enhanced resistance against B. cinerea infection in cherry tomato fruit during postharvest storage (Li et  al. 2022a). Melatonin treatment increased banana resistance to the pathogen Fusarium oxysporum (Wei et al. 2017), promoted downy mildew resistance demonstrated by cucumber plants (Sun et  al. 2019; Mandal et  al. 2018), and resistance to Malus in Marssonina apple blotch by modulating the levels of pathogenesis-related proteins, including chitinase (CHI) and β − 1,3-glucanase (GLU) (Yin et al. 2013). Melatonin contributed to enhanced resistance against Fusarium oxysporum f. sp. niveum (FON) infection in watermelon and played a role in defense response against Phytophthora crown rot due to Phytophtora capsici infection in the fruit (Mandal et  al. 2018). Postharvest application of melatonin reduced disease severity by increasing the levels of enzymatic and non-enzymatic antioxidants (Li et al. 2022b). Melatonin, acting upstream of the defense gene signaling pathway, induces the expression of NO, SA, and JA-related genes, which in turn work to increase resistance to pathogens (Arnao and Hernández-Ruiz 2018) (Fig. 9.3). The implication of

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Fig. 9.3  Proposed mechanism for enhancement of disease resistance by melatonin in postharvest fruits. Pathogen attack increases melatonin and NO levels through a rise in the level of ROS. Both melatonin and NO can induce JA biosynthesis, resulting in the activation of pathogenesis-related gene expression. Also, melatonin inhibits ethylene biosynthesis and activates SA signaling, which triggers a pathogen-induced response

melatonin and NO on the biosynthesis of ethylene and postharvest management of fruits has been comprehensively discussed (Mukherjee 2019). For example, melatonin delayed postharvest senescence in pears via the regulation of NO (Liu et  al. 2019b). Melatonin inhibits ethylene production by downregulating the genes involved in the biosynthesis of ethylene (Martínez-Lorente et al. 2022), resulting in delayed senescence in banana fruit (Hu et al. 2017). However, during the ripening of tomato fruit, melatonin was demonstrated to induce ethylene biosynthesis through 1-aminocyclypropane-carboxylate synthase 4 (ACS4) (Sun et al. 2015). JA and ethylene interact in a cooperative or antagonistic manner in downstream signaling pathways (Zhu and Lee 2014). Although direct biochemical interaction with hormone signaling molecules has not been fully established, genetic analysis suggests that JA and ethylene interact at ERF1 and ORA59 nodes (Zhu and Lee 2014). Interestingly, since EIN3 directly targets the ERF1 gene (Solano et al. 1998), EIN3 is proposed to be the link to ethylene-JA synergistic interactions. While JA promotes lycopene synthesis in tomatoes, exogenous ethylene triggers and initiates ripening in climacteric fruits (Liu et  al. 2012). Interestingly, ethylene not only affects the biochemical components, but also speeds up the rate of respiration in

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fruits and vegetables (Prasanna et al. 2007). The effects of melatonin treatment on berries of grapes were also observed, and there were attributed to ethylene signaling (Hu et al. 2018). Similar effects contributed to the attractive aroma, color, and higher quality of postharvest tomatoes (Sun et al. 2015). Both melatonin and NO can induce biosynthesis the biosynthesis of JA and increase the levels of glucose, fructose, sucrose, and glycerol, thereby consequently increasing the expression of pathogenesis-related genes (Yang et  al. 2019a). By induction, the expression of key genes in sugar metabolism, melatonin regulates the levels of carbohydrates in apple fruit (Yang et al. 2019a). The same study found that when melatonin concentration increased, transcript levels of MdFRK2 and fructokinase (FRK) decreased. These findings suggest a strong relationship between melatonin levels and responses during the postharvest processes, preventing deterioration of fruits and vegetables.

9.4 Concluding Remarks The influence of abiotic stress-causing forces (temperature, humidity, and air composition) continuously reduces the quality of fruits and vegetables. Postharvest preservation is a challenging endeavor that requires multiple approaches, mostly used in combination to prevent the deterioration of produce. Some of these approaches are costly due to the requirement of advanced technology, which is not readily available everywhere around the globe. Fortunately, melatonin, a nontoxic substance endogenously produced by plants, can also be applied exogenously to control the postharvest decay of fruits and vegetables. The application of melatonin exogenously augments the function of the endogenous molecules through a complex interplay among multiple physiological and biochemical pathways, resulting in the enhancement of abiotic stress tolerance in fruits and vegetables. Examples of such effects include salt stress tolerance of apple fruit, high-temperature stress tolerance of cucumber seedlings, low-temperature stress tolerance of tea plants and tomatoes, and heavy metal tolerance, like cadmium tolerance of tomato and vanadium tolerance of watermelon seedlings. Demonstrating high antioxidant capacity, melatonin delays senescence exhibits antimicrobial activity, and alleviates chilling injury in fruits and vegetables. Melatonin is also associated with the extension of the shelf life of harvested fruits and vegetables through influence on the GABA shunt pathway, which supplies intracellular ATP and increases the biosynthesis of PAL enzyme, resulting in the accumulation of non-enzymatic antioxidants such as phenols and anthocyanins. Moreover, the complex relationship between melatonin and several downstream pathways has been demonstrated. For instance, via regulation of NO, JA, and SA biosynthesis, melatonin induces the expression of pathogenesis-­ related genes, resulting in enhanced drug resistance. Melatonin, via regulation of the NO level, decreased the production of ethylene to enhance disease resistance in fruits. However, melatonin can induce or inhibit ethylene synthesis. These effects have been demonstrated in terms of an increase in the production of ethylene in

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tomatoes while its levels decreased in bananas and pears. Taken together, these tremendous effects of melatonin on the postharvest biology of fruits and vegetables point out the need for enhanced exogenous application of the molecules toward improved preservation. Acknowledgements  AIU would like to thank Professor Gökhan Zengin of Department of Biology, Selcuk University for guidance and support.

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Chapter 10

Melatonin Language in Postharvest Life of Horticultural Crops Morteza Soleimani Aghdam

Abstract  During postharvest life, fresh horticultural crops suffer from sensory and nutritional quality deterioration accompanied by fungal decay incidence. Low-­ temperature storage has been employed for delaying senescence and attenuating fungal decay while maintaining the sensory and nutritional quality of fresh horticultural crops. However, a chilling injury occurring confines low-temperature storage employed for economically important horticultural crops. Therefore, worthy attempts have been done by researchers for introducing procedures for alleviating chilling injury and fungal decay accompanied by maintaining sensory and nutritional quality in fresh horticultural crops during low-temperature storage. In recent years, melatonin gains great attention for employment as a safe eco-friendly procedure for improving the marketability of horticultural crops. By tryptophan supplying from the shikimate pathway, TDC, T5H, SNAT, and ASMT expression and enzyme activities are responsible for melatonin biosynthesis in the cytosol, chloroplasts, and mitochondria. By exogenous melatonin treatment or promoting endogenous melatonin accumulation by triggering TDC, T5H, SNAT, and ASMT expression or suppressing M2H and M3H expression, CAND2/PMTR1 is responsible for triggering melatonin signaling by employing NADPH oxidase-dependent ROS and Ca2+/CaM secondary messengers while promoting CDPK and MAPK signaling pathway. By melatonin signaling, MYB, NAC, bHLH, bZIP, WRKY, HSF, and ERF transcription factors activation could be responsible for marketability-responsive gene expression. In addition to transcription regulation, epigenetic DNA methylation, and histone protein posttranslational modifications (PTMs) accompanied by post-transcriptionally microRNAs (miRNAs) employed by melatonin could be responsible for marketability responsive gene expression. In addition to genes expression regulation, PTMs such as phosphorylation, ubiquitination, SUMOylation, nitrosation, and persulfidation could be employed by melatonin for regulating marketability-­responsive metabolic pathways. In addition to signaling function, M. S. Aghdam (*) Department of Horticultural Science, Imam Khomeini International University, Qazvin, Iran e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_10

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melatonin serves as an amphiphilic molecule with higher intracellular dynamism exhibiting ROS/RNS scavenging cascade. In addition to direct marketability responsive gene expression, melatonin exhibited overlapping with ethylene, cytokinin, abscisic acid, jasmonic acid, salicylic acid, nitric oxide, hydrogen sulfide, strigolactone, brassinosteroids, phytosulfokine α, and extracellular ATP signaling pathways. Keywords  Postharvest life · Melatonin · Chilling injury · Sensory and nutritional quality · Marketability · Fungal decay · ROS scavenging capacity

10.1 Phytomelatonin Biosynthesis and Its Intracellular Homeostasis In plants, tryptophan decarboxylase (TDC), tryptamine 5-hydroxylase (T5H), serotonin N-acetyltransferase (SNAT), N-acetylserotonin methyltransferase (ASMT) or caffeic acid O-methyltransferase (COMT) enzymes are responsible for melatonin biosynthesis from tryptophan in the cytosol, chloroplast and mitochondria by decarboxylation, hydroxylation, N-acetylation, and O-methylation (Fig. 10.1) (Aghdam et al. 2022). TDC is responsible for the decarboxylation of tryptophan to tryptamine or 5-hydroxytryptophan to serotonin in the cytosol. Tomato was transformed with tryptophan decarboxylase (SlTDC1) by Tsunoda et al. (2021) to discover the possibility of molecular breeding of serotonin-rich tomato fruits. Transgenic tomato overexpressing SlTDC1 exhibited higher serotonin and tryptamine accumulation accompanied by lower tryptophan accumulation in fruits, which could result from higher SlTDC1 expression demonstrating the efficiency of SlTDC1 gene overexpressing in producing serotonin-rich tomato fruits. Hence, the TDC gene would signify a potential candidate for molecular breeding of serotonin-rich fruits and vegetables by promoting endogenous serotonin accumulation as a promising bioactive functional molecule exhibiting anti-obesity capacity (Tsunoda et al. 2021). T5H acts as a cytochrome P450 monooxygenase (CYPs) enzyme for the hydroxylation of tryptamine to serotonin in the endoplasmic reticulum (Fujiwara et  al. 2010). Higher tryptamine accumulation in transgenic rice suppressing OsT5H could be responsible for triggering OsTDC1 expression through tryptamine oxidation by monoamine oxidase activity, which by promoting signaling H2O2 accumulation could be responsible for triggering OsTDC1 expression for serotonin biosynthesis from 5-hydroxytryptophan (5-OH-Trp). By suppressing OsT5H, cytosolic 5-OH-Trp synthase or tryptophan hydroxylase may be responsible for 5-OH-Trp biosynthesis from tryptophan, accelerating endogenous melatonin accumulation by TDC, SNAT, and ASMT activities (Park et al. 2013). In addition, higher endogenous melatonin accumulation in transgenic rice suppressing OsT5H could be ascribed to the promotion of mitochondrial melatonin biosynthesis by 5-OH-Trp production (Park et al. 2013). In Sekiguchi rice lacking functional tryptamine 5-hydroxylase (T5H)

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Fig. 10.1  Intracellular melatonin biosynthesis in plants. TDC, T5H, SNAT, ASMT or COMT enzymes are responsible for melatonin biosynthesis from tryptophan in the cytosol, chloroplast and mitochondria by decarboxylation, hydroxylation, N-acetylation, and O-methylation

activity, TDC activity could be responsible for serotonin biosynthesis from 5-OH-Trp during senescence. In addition, higher N-acetyltryptamine accumulation by SNAT activity could be responsible for suppressing endogenous melatonin accumulation in Sekiguchi rice during senescence by inhibiting ASMT activity (Park et al. 2012). SNAT is responsible for the acetylation of serotonin to N-acetylserotonin or 5-methoxytryptamine to melatonin in chloroplast and mitochondria (Wang et  al. 2017; Lee et al. 2014b). Apple MzSNAT5 is responsible for catalyzing serotonin to N-acetylserotonin in mitochondria, and higher drought stress tolerance in transgenic Arabidopsis ectopically expressing apple MzSNAT5 could be ascribed to promoting mitochondrial melatonin biosynthesis and attenuating oxidative stress (Wang et al. 2017). Pyruvate dehydrogenase (PDH) serves as a supplier of acetyl-­ CoA for SNAT activity in chloroplast and mitochondria (Tovar-Méndez et al. 2003). Sufficient acetyl-CoA provision by PDH confers efficient potential for melatonin biosynthesis in chloroplasts and mitochondria, which are premier intracellular ROS-generating organelles during senescence and stresses (Tan and Reiter 2020). By suppressing AtSNAT1 expression, Lee and Back (2021) reported that chloroplastic melatonin biosynthesis by SNAT activity is crucial for chloroplast protein quality control (CPQC) which could be ascribed to mitogen-activated protein kinase

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(MPK3/6) function (Lee and Back 2021). Lee et  al. (2018) reported that plants possess two genes encoding SNAT and ASDAC proteins to regulate endogenous melatonin accumulation during senescence and stress. Histone deacetylase genes in rice (OsHDAC10) and arabidopsis (AtHDAC14) encoded the ASDAC enzyme responsible for the deacetylation of NAS into serotonin in the chloroplast. Therefore, reversible acetylation and deacetylation by SNAT and HDAC expression and enzyme activities in chloroplast may be crucial for preserving intracellular melatonin homeostasis. OsHDAC10 and AtHDAC14 genes encoding ASDAC enzymes responsible for serotonin biosynthesis from N-acetylserotonin in the chloroplast. So, SNAT and HDAC expression and activities in chloroplast may be crucial for governing melatonin accumulation (Lee et al. 2018). ASMT and COMT are responsible for the O-methylation of N-acetylserotonin to melatonin or serotonin to 5-methoxytryptamine in cytosol and chloroplast or mitochondria. ATP-dependent S-adenosyl methionine (SAM) synthetase (SAMS) activity supplies SAM in the cytoplasm, whereas SAM can be transferred into the chloroplast and mitochondrial by SAM carrier 1 (SAMC1) or chloroplast by SAM carrier 2 (SAMC2) for serving as a methyl donor for ASMT and COMT activities (Palmieri et al. 2006; Ravanel et al. 2004). Zhao et al. (2021) provided evidence that COMT evolved from ASMT by gene duplication during plant terrestrialization, COMT prominently exhibits not only higher ASMT activity for higher melatonin biosynthesis for reactive oxygen and nitrogen species (ROS/RNS) scavenging but also acquires a new function in monolignol biosyntheses such as p-coumaryl alcohol and coniferyl alcohol for UV-protective lignin molecules biosynthesis during sessile lifestyle plants acclimation to land environmental challenges. During plant terrestrialization, whole-genome duplication (WGDs) imposed COMT evolving from ASMT by gene duplication and divergence, ASMT/COMT is crucial for acclimation to environmental biotic/abiotic challenges of plant terrestrialization by melatonin and lignin biosynthesis. Transgenic tomato plants overexpressing the indoleamine 2,3-dioxygenase (OsIDO) gene exhibited lower endogenous melatonin accumulation by promoting cytosolic AFMK production (Okazaki et  al. 2010). In addition, melatonin 2-­hydroxylase (M2H) and melatonin 3-hydroxylase (M3H) expression and enzyme activities are responsible for the production of 2-hydroxymelatonin (2OHM) and cyclic 3-hydroxymelatonin (c3OHM) in cytosol and chloroplast from melatonin and they could be responsible for maintenance of intracellular melatonin homeostasis. 2OHM and c3OHM in cytosol and chloroplast may serve as signaling molecules for triggering defense response, in addition to exhibiting ROS scavenging activity (Byeon and Back 2015; Byeon et al. 2015; Choi and Back 2019; Lee et al. 2016). RNAi suppressing OsM2H expression, promoting chloroplastic melatonin accumulation conferred cadmium, salinity, and oxidative stress tolerance in rice plants. Without stresses, suppressing OsM2H expression repressed endogenous melatonin accumulation, which could be ascribed to promoting cyclic 3-hydroxymelatonin (c3OHM) accumulation, demonstrating feedback regulation between melatonin, 2OHM, and c3OHM (Choi and Back 2019). In addition to OsM2H, RNAi-­ suppressing N-acetylserotonin deacetylase (OsASDAC) expression promoted

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chloroplastic melatonin accumulation, which could be beneficial for conferring environmental stress in rice plants (Lee et al. 2020).

10.2 Phytomelatonin Biosynthesis Regulation by Transcription Factors As ROS-responsive transcription factors, MeRAV1 and MeRAV2 are beneficial for conferring resistance versus cassava bacterial blight by promoting endogenous melatonin accumulation (Wei et al. 2018b). By chromatin immunoprecipitation (ChIP), and electrophoretic mobility shift analysis (EMSA) assays, Wei et  al. (2018b) reported that MeRAV1 and MeRAV2 are transcriptional activators of melatonin biosynthesis genes through directly binding to the CAACA motif in the promoters of MeTDC2, MeT5H, and MeASMT1, activating their expression and promoting endogenous melatonin accumulation (Wei et al. 2018b). In tomato plants, heat-shock factor A1a (HsfA1a) transcription factor expression conferred cadmium (Cd) stress tolerance by promoting endogenous melatonin accumulation and triggering HSP20, HSP21, HSP70, and HSP90 expression (Cai et  al. 2017). By ChIP and EMSA assays, Cai et  al. (2017) reported that HsfA1a binding to the heat shock elements (HSE, GAANNTTC) in the promoter of COMT1 activated its expression and melatonin accumulation which enhanced Cd tolerance by participating in HSPs expression. Exogenous melatonin treatment or endogenous melatonin accumulation by SlSNAT gene overexpression conferred heat stress in tomato plants, which was associated with higher ribulose bisphosphate carboxylase oxygenase (RuBisCO) and RuBisCO activase proteins accumulation, lower O2•and H2O2 accumulation, and higher heat shock proteins (SlHSPs) expression. By yeast two-hybrid and BiFC assays, Wang et al. (2020c) reported that HSP40 interaction with SlSNAT in chloroplasts preserves SNAT enzyme stability and activity as a molecular chaperone for promoting endogenous melatonin accumulation during heat stress. By heat stress perception, higher heat shock transcription factors (HSFs) expression could be responsible not only for triggering HSPs expression but also can trigger SlSNAT expression by directly binding to the heat shock elements (HSE, GAANNTTC) in the promoter of SlHSP40 and SlSNAT genes. By serving as a molecular chaperon, HSP40 could be responsible for protecting SNAT protein stability and enzymatic activity versus oxidative stress, which supports endogenous melatonin accumulation and improves ROS scavenging capacity (Wang et al. 2020c). By cassava bacterial blight, MeWRKY79 and MeHsf20 transcription factors expression could be responsible for conferring disease resistance by promoting endogenous melatonin accumulation. By LUC, ChIP, and EMSA assays, Wei et al. (2017) reported that MeWRKY79 and MeHsf20 directly bound to W-box elements (TTGACC/T) and heat shock elements (HSE, GAANNTTC) in the promoter of MeASMT2 activated its expression conferring resistance versus cassava bacterial blight by promoting endogenous melatonin accumulation (Wei et  al. 2017). In

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addition, higher MeHSP90.9 expression could be ascribed to higher MeHsf8 transcription factor expression during cassava bacterial blight. By Y2H, pull-down, and BiFC analysis, Wei et  al. (2021) reported that MeHSP90.9 interacts with MeWRKY20, and MeHSP90.9 promotes the transcriptional activation of MeWRKY20 on MeASMT2 by binding to W-box elements (TTGACC/T) in the promoter of MeASMT2 as evidenced by LUC, ChIP, and EMSA assays, which activates MeASMT2 expression conferring resistance versus cassava bacterial blight by promoting endogenous melatonin accumulation or suppressing auxin (indole-­3-­ acetic acid, IAA) accumulation. During hickory fruit ripening, ethylene-responsive CcEIN3 and ABA-responsive CcAZF2 transcription factors could be responsible for promoting endogenous melatonin accumulation. Evidenced by yeast one-hybrid (Y1H) and LUC assays, Chen et al. (2021) reported that the CcEIN3 transcription factor directly binding to EIN3-­ binding sites (ATGTAT, ATACAT, CTACAT, or ATGTAC) in the promoter of CcTDC1 while CcAZF2 transcription factor directly binding to A(G/C)T-box in the promoter of CcASMT1, activated CcTDC1 and CcASMT1 expression promoting endogenous melatonin accumulation (Chen et al. 2021). During heat stress, nuclear PlTOE3 as an APETALA2/ethylene-responsive element-­binding factor (AP2/ERF) transcription factor, directly binds to the promoter and activates the expression of tryptophan decarboxylase (PlTDC), as evidenced by pull-down, Y1H and LUC assays, which is responsible for conferring heat tolerance in herbaceous peony by promoting endogenous melatonin accumulation, which not only serves as an endogenous ROS/RNS scavenger but also functions as a signaling molecule for promoting H2O2 scavenging SOD−CAT pathway, and ultimately improve heat stress tolerance in herbaceous peony (Zhang et al. 2022b).

10.3 Phytomelatonin Signaling Illumination by Discovering Receptors In Arabidopsis, the candidate G protein-coupled receptor (AtCAND2) gene encoded a membrane-localized protein serving as phytomelatonin receptor 1 (PMTR1). By binding to CAND2, melatonin as an extracellular signaling molecule promotes direct interaction of CAND2 with heterotrimeric G protein α subunit (GPA1) as evidenced by bimolecular fluorescence complementation (BiFC) and yeast mating-­ based split ubiquitin system (SUS) analysis, which promotes signaling ROS production by activation of NADPH oxidase for enhancing Ca2+ influx facilitating stomatal closure (Wei et al. 2018a). Recently, Wang et al. (2021b) discovered phytomelatonin receptor 1 (ZmPMTR1) as Arabidopsis AtCAND2/AtPMTR1 homologous gene in maize plants by homology searching. By microscale thermophoresis (MST) analysis, ZmPMTR1 exhibited a strong binding capacity to melatonin which revealed plasma membrane ZmPMTR1 function as a melatonin receptor in maize

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plants. As well as Arabidopsis AtPMTR1, ZmPMTR1 expression induced by exogenous melatonin, osmotic stress, and ABA application in maize root and shoot. By transgenic wild type and cand2–1 mutant of Arabidopsis overexpressing ZmPMTR1 and transgenic maize silencing ZmPMTR1, Wang et al. (2021b) reported that conferring osmotic and drought stress could be ascribed to higher ROS scavenging system activity accompanying by promoting stomatal closure. Li et al. (2020a) reported that daily rhythmicity in melatonin biosynthesis and signaling is beneficial for conferring drought tolerance by minimizing water loss and improving water-use efficiency in Arabidopsis. Higher melatonin biosynthesis by higher AtSNAT1, AtCOMT1, and AtASMT expression was associated with higher melatonin signaling by higher AtPMTR1 expression during the daytime, which could be responsible for preserving ROS dynamics through suppressing ROS generation NADPH oxidase (AtRBOHA) expression along with promoting ROS scavenging catalase (AtCAT), superoxide dismutase (AtSOD), alternative oxidase (AtAOX) and peroxiredoxin (AtPRX) expression. Therefore, ROS signaling arising from melatonin signaling by PMTR1 function during the daytime could be responsible for darkness signals transduction for triggering stomatal closure during nighttime. By melatonin treatment or Pst DC3000 bacterial infection, triggering AtSNAT1 and AtCOMT1 expression was associated with higher AtPMTR1 expression in Arabidopsis. By triggering AtPMTR1 expression, MAPK cascade and G protein independent signaling pathways serve as plant PTI response for triggering stomatal immunity. By melatonin signaling through AtPMTR1, triggering MKK4/5 and MPK3/6 expression following MPK3/6 phosphorylation is responsible for triggering stomatal immunity (Yang et al. 2021b). MPK3/MPK6 signaling cascade could be responsible for promoting organic acids malate/citrate metabolism by triggering NADP-malic enzyme (NADP-ME2/3) and NAD-isocitrate dehydrogenase (NAD-­ IDH1/2/5) expression and activities leading to stomatal closure by lower malate/ citrate accumulation (Su et  al. 2017). In addition to organic acid metabolism, MPK3/6 are responsible for Arabidopsis actin-bundling protein villin 3 (VLN3) phosphorylation at Serine 779, which is crucial for stomatal immunity by facilitating Ca2+ dependent actin cytoskeletal rearrangement in guard cells (Zou et al. 2021; Singh and Verma 2022). In addition to MPK3/MPK6 signaling cascade, PMTR1 interaction with GPA1, evidenced by co-immunoprecipitation (Co-IP) and western blot analyses, is responsible for stomatal closure by triggering ROS production by NADPH oxidase activity promoting Ca2+ signaling, independent from MAPK signaling pathway (Yang et al. 2021a). By rhythmic melatonin signaling via PMTR1/ MAPKs, triggering stomatal closure could be responsible for avoiding water loss and preventing bacterial invasion at nighttime. Hence, genetic manipulation of melatonin signaling responsive PMTR1 gene would be a beneficial approach for improving crop stress tolerance (Li et al. 2022c). Lee and Back (2018) reported that the endogenous melatonin accumulation by melatonin treatment and AtSNAT1 gene overexpression attenuated ER stress in Arabidopsis plants challenged with tunicamycin (Tm) by employing bZIP60 transcription factor for triggering ER chaperones luminal binding protein (BIP2/3) and

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calnexin (CNX1) expression. MAPK3/6 cascades signaling is responsible for ER stress sensor inositol-requiring enzyme 1 (IRE1) activation, which by RNase function facilitated ER membrane-associated bZIP60 mRNAs splicing, promotes its nuclear translocation for chaperone expression. By melatonin signaling via ­PMTR1/ CAND2, ER chaperone activities could be responsible for perfect folding and plasma membrane localization of ER secretory proteins BRI1 and FLS2 during ER stress. In addition, higher BRI1 protein accumulation could be ascribed to preserving ER network structure and improving ER protein folding capacity by melatonin during ER stress (Lee and Back 2018). Wang et al. (2021d) report that endogenous melatonin accumulation by triggering AtSNAT1, AtCOMT1, and AtASMT1 expression could be responsible for conferring osmotic stress tolerance in Arabidopsis by enhancing catalase (AtCAT1, AtCAT2, AtCAT3) and superoxide dismutase (AtSOD1) expression and activities giving rise to lower H2O2 accumulation. By endogenous melatonin accumulation, AtCAND2/AtPMTR1 expression could be responsible for endogenous melatonin signaling for triggering ROS scavenging expression. By employing AtCAND2/PMTR1 and AtGPA1 silencing, Bychkov et al. (2022) reported that the conferring photooxidative stress in Arabidopsis by melatonin treatment was dependent on CAND2/PMTR1-GPA1 signaling pathway. By melatonin treatment, triggering AtSNAT1, AtASMT, and AtCOMT expression promoted endogenous melatonin accumulation and triggering CAND2/PMTR1-GPA1 signaling pathway, which could be responsible for suppressing early light-inducible protein 1 (ELIP1) gene and protein expression accompanying by promoting nuclear-encoded RNA polymerase (NEPs) targeted into chloroplasts (RPOTp) or chloroplasts and mitochondria (RPOTmp) expression, promoting plastid-encoded plastid RNA polymerase (PEPs, RpoA and RpoB) expression, enhancing nuclear-encoded light-harvesting antenna protein of PSII (LHCB2) and chloroplast-encoded structural proteins of PSI (PsaA), PSII (PsbA, PsbD), ATP synthase subunit beta (AtpB) and acetyl-CoA carboxylase subunit beta (accD) genes and proteins expression, mitochondrial encoded alternative respiratory alternative oxidase (AOX1a) expression and activity, and electron transport chain NADH dehydrogenase (Nad3 and Nad6), cytochrome c reductase (Cob), cytochrome c oxidase (Cox1) and ATP synthase (Atp6–1), and cytochrome c biogenesis (CcmC and CcmFC) expression (Bychkov et al. 2022). By melatonin treatment and PMTR1 gene overexpression or silencing by CRISPR/Cas9 system, Yin et  al. (2022) reported that the melatonin signaling by PMTR1/CAND2 is responsible for orchestrating seed development and germination in Arabidopsis by regulating ABA biosynthesis AtNCED2/3/5/9 expression along with ABA signaling AtABF1/2/3/4 and AtABI5 expression. As a potent long-­ distance signal, rhizospheric melatonin application conferred systemic cold tolerance in watermelon leaves. By melatonin treatment, endogenous melatonin signaling by PMTR1-GPA1 interaction could be responsible for promoting phospholipase C (PLC) activity for phosphatidylinositol (4,5) bisphosphate (PIP2) hydrolyzing giving rise to inositol-trisphosphate (InsP3) and diacylglycerol (DAG) accumulation. As a second messenger, InsP3 promotes intracellular Ca2+ store mobilization and cytosolic Ca2+ signaling, which activates NADPH oxidase (ClRBOH) and signaling

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ROS accumulation. By PLC/IP3/Ca2+-ROS signaling cascade, calcium-dependent protein kinase (ClCDPK18) and mitogen-activated protein kinase (ClMAPK16) activation could be responsible for transcriptional activity of ERFs, bZIPs, bHLHs, WRKYs, MYBs, and HSFs for triggering cold-responsive protective heat shock proteins (ClHSPs), jasmonic acid generating lipoxygenase (ClLOX), and ROS scavenging peroxidase (ClPOD) expression (Li et al. 2017). By VIGS GhCOMT gene silencing and melatonin treatment, Zhang et al. (2021a) reported that endogenous melatonin signaling by PMTR1/GPA1 could be responsible for phosphatidylinositol signaling system activity by promoting phosphatidylinositol 4,5-bisphosphate dependent phospholipase C (GhPLC2) and heavy metal-associated isoprenylated plant protein 02 (GhHIPP02) expression for inositol 1,4,5-triphosphate (InsP3) and inositol hexaphosphate (InsP6) supplying for intracellular Ca2+ stores mobilization. By endogenous melatonin signaling, enhancing NADPH oxidase activity along with promoting second messengers IP3, DAG, IP6, and Ca2+ accumulation could be responsible for triggering CDPK/MAPK signaling pathway employing bZIP, MYB, WRKY, and ERF transcription factors for triggering stress responsive auxin, ABA, ethylene, brassinosteroids, and jasmonic acid biosynthesis and signaling along with triggering ROS scavenging expression and activities (Zhang et al. 2021a). Gong et al. (2017) reported that the higher endogenous melatonin accumulation arising from melatonin treatment could be responsible for suppressing endogenous NO and SNOs accumulation. As evidenced by biotin-switch assay and western blot analysis, lower S-nitrosylation promoted NADPH oxidase activity leading to signaling H2O2 accumulation. By promoting H2O2 signaling, triggering SlCDPK1/2 and SlMAPK1/4 expression could be responsible for improving drought, heat, and cold stress tolerance in tomato plants by triggering SlERF1/4, SlWRKY30/65, SlMYB86, and SlbHLH93 transcription factors and corresponding SlPAO5, SlGRF3, SlPIN6, SlERD15, and SlHSP80 expression and SOD, APX and CAT activities (Gong et al. 2017). By RNAi silencing OsTDC, OsT5H, OsSNAT2, and OsCOMT expression, lower endogenous melatonin accumulation was concomitant with lower endogenous BR accumulation arising from lower OsDWARF4 expression. Melatonin treatment promoted endogenous BR accumulation in rice seedlings by triggering OsDWARF4 expression (Hwang and Back 2018; Lee and Back 2019). Fu et al. (2022) reported that melatonin treatment conferred cold and drought stress tolerance in perennial ryegrass by triggering endogenous melatonin accumulation arising from higher LpASMT1/3 and LpCOMT2 expression. By endogenous melatonin signaling, triggering NADPH oxidase (LpRBOHB/C) expression promoted signaling H2O2 accumulation, which could be responsible for promoting endogenous brassinosteroids (BRs) biosynthesis (LpDWF4 and LpCYPs) and signaling (LpBRI1, LpIWS1, LpSERK1, and LpBZR1) expression. By employing propiconazole (PPZ) as a BRs biosynthesis inhibitor, endogenous BRs biosynthesis and signaling is crucial for cold and drought stress tolerance conferred by melatonin treatment. By melatonin-­ BRs-­H2O2 signaling networks activation, promoting MAPK signaling cascade along with triggering DREB1A, ERF1/109, MYB4/108, WRKY30/53, bZIP73, and

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ZAT6 transcription factors expression could be responsible for triggering cold stress-responsive genes expression (Fu et al. 2022). By pathogens infection, promoting H2O2 and NO could be responsible for triggering endogenous melatonin accumulation in Arabidopsis. By endogenous melatonin accumulation arising from pathogen infection or melatonin treatment, PMTR1 function activates the MPK3/6 signaling cascade. In addition, PMTR1 interaction with GPA1 triggers ROS production by NADPH oxidase activity. In addition to direct MPK3/6 activation by PMTR1, oxidative burst response, serine/threonine oxidative signal-inducible 1 (OXI1) kinase could be responsible for phosphorylation and activation of MPK3/6 signaling cascade. By MPK3/6 signaling cascade, promoting endogenous salicylic acid accumulation by triggering isochorismate synthase 1 (ICS1) expression promoted NPR1/TGA signaling and chitinase (CHI) and β-1,3-glucanase (GLU) expression and activities (Yin et al. 2013; Lee et al. 2015; Lee and Back 2016, 2017; Lee et al. 2014a). In addition to NADPH oxidase produces ROS activates OXI1 kinase, phosphatidic acid (PA) produced by PLD promotes phosphoinositide-dependent protein kinase 1 (PDK1) for phosphorylation and activation of OXI1 kinase (Anthony et al. 2006). In addition to ICS1/SA signaling, promoting glycerol accumulation by endogenous melatonin accumulation could be responsible for AzA signal transduction by G3P biosynthesis for activating SAR (Qian et al. 2015). Mandal et al. (2018) reported that the melatonin treatment or overexpressing SNAT gene attenuates powdery mildew caused by Podosphaera xanthii in watermelon and cucumber leaves and Phytophthora decay caused by Phytophthora capsici in watermelon and cucumber fruits. By endogenous melatonin accumulation, triggering shikimic acid pathway activity could be responsible for sufficient phenylalanine and tryptophan supplying for phenylpropanoid pathway and tryptophan-melatonin pathways, respectively, which both are beneficial for triggering PRs expression. By melatonin treatment, conferring resistance of lilium to leaf blight caused by Botrytis elliptica could be ascribed to endogenous melatonin signaling by triggering respiratory burst oxidase (RBOH) expression which could be responsible for triggering the Ca2+ signaling pathway by calcium-dependent protein kinase (CDPK) expression. In addition, by triggering Ca2+ signaling, promoting nitric-oxide synthase (NOS) expression could be responsible for triggering the NO signaling pathway. By promoting MAP kinase signaling pathway as shown by triggering MPK3/6 expression, employing WRKYs transcription factor may be responsible for promoting salicylic acid (higher NPR1) and jasmonic acid (higher COI1 and JAZ) signaling, triggering HSP90 expression and enhancing phenylpropanoid pathway activity as shown by higher phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), 4-coumarate: CoA ligase (4CL), and cinnamate 4-hydroxylase (C4H) (Xie et al. 2022). By manipulating endogenous melatonin accumulation by overexpression or silencing of AtSNAT and AtASMT genes, Zhu et  al. (2021b) reported that triggering jasmonic acid (JA) accumulation and signaling as shown by suppressing JAZ1 and MYC2 expression could be responsible for Botrytis cinerea resistance in Arabidopsis by triggering PR1 and PR5 expression. Also, triggering WRKY33 transcription factor expression could be responsible for conferring Botrytis cinerea resistance in Arabidopsis by promoting antimicrobial phytoalexin

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camalexin accumulation from chorismate-tryptophan-IAOx-IAN pathway (Zhu et  al. 2021b). By endogenous melatonin signaling, pathogen-responsive MPK3/6 signaling cascade could be responsible for phosphorylation and activation of WRKY33 transcription factor for directly binding to the promoter and enhancing expression of camalexin biosynthetic AtPAD3 gene (Mao et al. 2011).

10.4 Phytomelatonin Language in Postharvest Life of Fruits and Vegetables 10.4.1 Phytomelatonin Palliates Chilling Injury By melatonin treatment, triggering signaling H2O2 accumulation arising from promoting NADPH oxidase expression and activity (Sharafi et  al. 2019; Cao et  al. 2018b; Aghdam et al. 2019a), enhancing endogenous melatonin accumulation arising from triggering TDC, T5H, SNAT, and ASMT expression (Sharafi et al. 2019; Liu et al. 2021), promoting cysteine 2/histidine 2 (C2H2) zinc finger (SlZAT2/6/12) transcription factors expression giving rise to activating C-repeat/dehydration-­ responsive element (CRT/DRE) binding factors (CBF1) expression (Aghdam et al. 2019c), activating arginine pathway as shown by higher arginase (ARG1/2) expression (Aghdam et al. 2019c), promoting endogenous polyamines accumulation arising from higher ornithine decarboxylase (ODC) and arginine decarboxylase (ADC) expression and activities (Aghdam et al. 2019c; Cao et al. 2016; Bhardwaj et al. 2022c; Madebo et al. 2021), enhancing endogenous proline accumulation arising from higher 1-pyrroline-5-carboxylate synthase (P5CS) and ornithine δ-aminotransferase (OAT) expression and activities accompanying by lower proline dehydrogenase (ProDH) expression and activity (Aghdam et al. 2019c; Cao et al. 2016; Liu et al. 2020a; Bhardwaj et al. 2021; Aghdam et al. 2019a; Sun et al. 2020a; Madebo et al. 2021), enhancing endogenous nitric oxide (NO) accumulation arising from higher nitric oxide synthase (NOS) expression and activity (Aghdam et  al. 2019c), higher γ-aminobutyric acid (GABA) shunt pathway activity demonstrating by higher glutamate decarboxylase (GAD), GABA transaminase (GABA-T) and succinate semialdehyde dehydrogenase (SSADH) activities (Sharafi et  al. 2019; Cao et  al. 2016; Bhardwaj et  al. 2022c; Madebo et  al. 2021), higher phenylpropanoid pathway activity demonstrating by higher higher phenylalanine ammonia-­ lyase (PAL), cinnamic acid 4-hydroxylase (C4H), 4-coumarate: CoA ligase (4CL) and chalcone synthase (CHS) along with lower polyphenol oxidase (PPO) expression and activity giving rise to higher phenols, flavonoids and anthocyanins accumulation and higher DPPH scavenging capacity (Sharafi et  al. 2019; Gao et  al. 2018; Liu et  al. 2021; Bhardwaj et  al. 2022b; Jannatizadeh 2019; Aghdam et  al. 2019a, 2020; Sun et  al. 2020a), triggering miR528 expression for suppressing miR528 targets PPOs expression (Wang et al. 2021e), sufficient intracellular ATP supplying arising from higher H+-ATPase, Ca2+-ATPase, cytochrome c oxidase

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(CCO), and succinate dehydrogenase (SDH) expression and activities (Jannatizadeh et al. 2019; Liu et al. 2020a; Bhardwaj et al. 2022a; Xu et al. 2022), higher unsaturated/saturated fatty acids (unSFA/SFA) accumulation as shown by higher linoleic and linolenic acids accumulation coincides with lower palmitic, stearic and oleic acids accumulation (Jannatizadeh et al. 2019; Gao et al. 2018; Wang et al. 2022b; Bhardwaj et al. 2022a; Kong et al. 2020) arising from higher fatty acid desaturases (FADs) expression (Jannatizadeh et al. 2019; Wang et al. 2022b) along with lower phospholipase D (PLD) and lipoxygenase (LOX) expression and activities (Jannatizadeh et al. 2019; Gao et al. 2018; Wang et al. 2022b; Bhardwaj et al. 2022a; Jannatizadeh 2019; Kong et  al. 2020; Mirshekari and Madani 2022; Mirshekari et al. 2020), protective membrane integrity as shown by lower electrolyte leakage and malondialdehyde (MDA) accumulation (Aghdam et al. 2019c; Gao et al. 2018; Cao et al. 2018b; Liu et al. 2020a; Bhardwaj et al. 2022c; Kong et al. 2020), triggering SUMO E3 ligase (SIZ1) expression (Shao et  al. 2016), promoting oxidative pentose phosphate pathway (OxPPP) activity representing by higher glucose-­6-­ phosphate dehydrogenase (G6PDH) and 6-phosphogluconate dehydrogenase (6PGDH) activities (Gao et al. 2018; Aghdam et al. 2020; Sun et al. 2020a), promoting shikimate pathway activity representing by higher shikimate dehydrogenase (SKDH) activity (Gao et al. 2018; Sun et al. 2020a), promoting endogenous salicylic acid (SA) accumulation (Gao et al. 2018), enhancing ROS scavenging superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), and dehydroascorbate reductase (DHAR) expression and activities giving rise to lower O2•- and H2O2 accumulation (Cao et al. 2018b; Wang et al. 2021e, 2022b; Liu et al. 2021; Bhardwaj et  al. 2022b; Jannatizadeh 2019; Kong et  al. 2020; Aghdam et  al. 2019a, 2020; Mirshekari et  al. 2020), triggering ascorbic acid biosynthesis responsive genes mannose-­ 1-phosphate guanylyl transferase (GMPH), GDP-D-mannose-3′,5′epimerase (GME), GDP-L-galactose guanylyl transferase (GGGT), L-galactose-1-­ phosphate phosphatase (GPP), L-galactose-1-dehydrogenase (GDH), and L-galactono-1,4-lactone dehydrogenase (GLDH) expression (Cao et  al. 2018b), promoting protein oxidative repairing methionine sulfoxide reductase (MsrA1, MsrA2, MsrB1, and MsB2) expression (Liu et al. 2021), promoting non-covalently binding spermidine (Spd3+) and spermine (Spm4+) accumulation arising from higher SAM decarboxylase (SAMDC) activity along with promoting covalently binding putrescine (Put2+) and Spd3+ accumulation arising from higher transglutaminase (TGase) activity (Dong et  al. 2022b; Du et  al. 2021), triggering ROS avoidance alternative oxidase (AOX) expression (Aghdam et  al. 2019a, 2020), suppressing ascorbic acid oxidation responsible ascorbic acid oxidase (AAO) activity (Aghdam et al. 2020), inhibiting lignification by suppressing NACs and MYBs transcription factors expression giving rise to suppressing PAL, cinnamyl alcohol dehydrogenase (CAD), and peroxidase (POD) expression and activities (Li et al. 2019a; Yang et al. 2022; Wang et al. 2021a; Jiao et al. 2022) (Fig. 10.2) could be responsible for palliating chilling injury in tomato fruits (Aghdam et  al. 2019c; Jannatizadeh et  al. 2019; Sharafi et al. 2019), peach fruits (Cao et al. 2016, 2018a, b; Gao et al. 2018; Shao et al. 2016), banana fruits (Wang et al. 2021e, 2022b), litchi fruits (Liu et al.

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Fig. 10.2  Hypothetical model representing mechanisms employed by exogenous melatonin application and endogenous melatonin signaling for palliating chilling injury and fungal decay in horticultural crops during postharvest life

2020a, 2021), mango fruits (Bhardwaj et al. 2021, 2022a, b, c), apple fruits (Dong et  al. 2022b), plum fruits (Du et  al. 2021; Xu et  al. 2022), pomegranate fruits (Jannatizadeh 2019; Molla et al. 2022; Aghdam et al. 2020), pepper fruits (Kong et al. 2020), cut anthurium flowers (Aghdam et al. 2019a), pear fruits (Sun et al. 2020a), cucumber fruits (Madebo et  al. 2021), guava fruits (Chen et  al. 2022; Mirshekari and Madani 2022), sapota fruits (Mirshekari et al. 2020), bamboo shoots (Li et al. 2019a; Yang et al. 2022), loquat fruits (Wang et al. 2021a) and kiwifruits (Jiao et al. 2022).

10.4.2 Phytomelatonin Attenuates Fungal and Bacterial Decay Endogenous melatonin accumulation by melatonin treatment attenuated grey mold decay caused by Botrytis cinerea and promoted flavonoids accumulation in ‘Merlot’ and ‘Shine Muscat’ grape berries. Melatonin and DNA methylation inhibitor 5́-azacytidine (5́-Aza) application triggered expression while decreased DNA methylation of VvPAL1 (phenols accumulation), stilbene synthase 1 (VvSTS1, resveratrol accumulation), enhanced disease susceptibility 1 (VvEDS1, salicylic acid accumulation) and calcium-binding protein (VvCML41, Ca2+ signaling). Lower DNA (cytosine-­5)-methyltransferase 1 (MET1) and SAM-dependent methyltransferase (SAM-MTase) expression could be responsible for decreased DNA methylation. Melatonin treatment triggered defense responses VvPAL1, VvSTS1, VvEDS1, and

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VvCML41 expression by lowering promoter methylation validated by single-base DNA methylation bisulfite sequencing (BS-Seq) and bisulfite-RT-PCR (BS-PCR) and thereby attenuated grey mold decay caused by Botrytis cinerea and promoted flavonoids accumulation in ‘Merlot’ and ‘Shine Muscat’ grape berries (Gao et al. 2020). Microbial antagonist Meyerozyma guilliermondii Y-1 attenuated gray mold caused by Botrytis cinerea in ‘Fuji’ apple fruits by promoting endogenous melatonin accumulation arising from higher MdSNAT1 and MdASMT1 expression. Melatonin treatment improved the biocontrol efficacy of Meyerozyma guilliermondii Y-1 for attenuated gray mold caused by Botrytis cinerea in ‘Fuji’ apple fruits by promoting population growth and colonization of Meyerozyma guilliermondii Y-1 in apple fruits accompanying by triggering jasmonic acid (JA) signaling pathway (MdPDF1.2 and MdCOI1) expression, enhancing ROS scavenging SOD and CAT activities and intracellular antioxidant capacity, promoting phenols and lignin accumulation by promoting PAL and PPO activities, and triggering MdPR1, MdPR5, MdGLU, and MdCHI expression (Sun et al. 2021a). Melatonin treatment suppresses the growth of food-borne Bacillus cereus, Bacillus licheniformis and Bacillus subtilis in tomato fruits by antibacterial activity of melatonin on Bacillus cereus, Bacillus licheniformis and Bacillus subtilis. By melatonin treatment, lower FtsZ, FtsA, and divIB expression participating in bacterial cell division, lower FlgB expression participating in bacterial flagellum formation, lower CybB and AtpI expression exhibiting NADPH oxidase and ATP synthase activity, and lower YikB and YukE expression participating in ATP-dependent transportation and secretion processes could be responsible for inhibiting swimming motility and biofilm formation by Bacillus cereus, Bacillus licheniformis and Bacillus subtilis (Zhu et  al. 2021a). In addition, melatonin treatment triggers ethylene biosynthesis and signaling ACC oxidase (ACO1) and ethylene response factor (ERF6) expression promoting nitric oxide biosynthesis and signaling NOS and E3 ubiquitin-protein ligase CSU1 expression, suppressing ROS accumulation by enhancing POD18 and SOD1 expression, promoting phenols and flavonoids accumulation and ABTS scavenging capacity and promoting PRs expression conferring resistance to the non-­necrotrophic bacterium in tomato fruits (Zhu et al. 2021a). By melatonin treatment, triggering signaling O2•- and H2O2 accumulation arising from higher NADPH oxidase expression and activity (Li et al. 2019b, c, 2022a, b; Fan et al. 2022a), triggering CDPKs expression responsible for Ca2+ signaling pathway (Li et al. 2022a), triggering MAPKs expression responsible for ROS signaling pathway (Li et al. 2019c), promoting endogenous salicylic acid accumulation arising from triggering PAL and isochorismate synthase (ICS) expression along with enhancing PAL and benzoic acid 2-hydroxylase (BA2H) activities (Li et al. 2019b, 2022a, b; Chen et al. 2020), activating endogenous salicylic acid signaling pathway by triggering WRKY70, NPR1, and TGAs expression (Li et  al. 2019b, 2022a, b), triggering GLU and CHI expression and activities (Li et  al. 2019b, 2022a; Zang et  al. 2022; Qu et  al. 2022b; Huang et  al. 2021; Fan et  al. 2022a, b), promoting phenylpropanoid pathway activity for phenols and lignin accumulation by triggering PAL, C4H, 4CL and CHS expression and activities giving rise to higher phenols,

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flavonoids and anthocyanins accumulation (Li et al. 2019b, 2022a; Zang et al. 2022; Yan et al. 2022b; Qu et al. 2022b; Huang et al. 2021; Zhang et al. 2021c; Fan et al. 2022a, b; Jannatizadeh et al. 2021), improving ROS scavenging SOD, CAT, APX and GR expression and activities responsible for higher ascorbate and glutathione accumulation along with lower O2•- and H2O2 accumulation (Zang et al. 2022; Liu et al. 2019a; Yan et al. 2022a; Chen et al. 2020; Zhang et al. 2022a; Fan et al. 2022a, b; Jannatizadeh et al. 2021), promoting endogenous melatonin accumulation arising from triggering TDC, T5H, SNAT and ASMT expression (Yan et al. 2022a; Li et al. 2019b, 2022b), promoting endogenous jasmonic acid (JA) and methyl jasmonate (MeJA) accumulation and signaling arising from triggering lipoxygenase (LOX), allene oxide synthase (AOS) and allene oxide cyclase (AOC) expression along with suppressing MYC2 and JAZ1 expression (Liu et  al. 2019a; Chen et  al. 2020; Qu et al. 2022b; Arabia et al. 2022), protective membrane integrity as shown by lower electrolyte leakage and MDA accumulation (Yan et al. 2022a; Chen et al. 2020), suppressing endogenous nitric oxide accumulation arising from inhibiting NOS expression and activity (Li et al. 2022b), promoting GABA shunt pathway activity by triggering GAD, GABA-T, and SSADH expression and activities (Chen et  al. 2020), inhibiting membrane deteriorating PLD and LOX activities (Fan et al. 2022a, b), promoting OxPPP activity representing by higher G6PDH and 6PGDH activities giving rise to sufficient intracellular NADPH supplying (Zhang et al. 2021c), promoting H+-ATPase, Ca2+-ATPase, SDH and CCO activities giving rise to sufficient intracellular ATP supplying (Zhang et al. 2021c), triggering phosphoinositide phospholipase C (PI-PLC4) expression beneficial for triggering signaling molecule inositol 1,4,5-triphosphate (InsP3) accumulation (Li et al. 2019c), triggering heat shock transcription factors (HSFs) expression for promoting heat shock proteins (HSPs) expression (Li et al. 2019c), promoting cuticular wax and cutin biosynthesis by triggering 3-ketoacyl-CoA synthase (KCSs) and lipid transfer protein (LTPs) expression, respectively, and promoting MYBs transcription factor expression for governing cuticular cutin and wax biosynthesis (Li et al. 2019c), and suppressing carcinogenic aflatoxin B1 (ABF1) accumulation (Jannatizadeh et al. 2021) (Fig. 10.2) could be responsible for attenuating fungal decay in tomato fruits (Zang et al. 2022; Li et al. 2019b, 2022a, b; Liu et al. 2019a; Sheng et al. 2020; Yan et al. 2022a), wax apple fruits (Chen et al. 2020), plum fruits (Yan et al. 2022b), blueberry fruits (Qu et al. 2022b), ginger rhizomes (Huang et al. 2021), pistachio fruits (Jannatizadeh et al. 2021), guava fruits (Fan et al. 2022b), litchi fruits (Zhang et al. 2021c), jujube fruits (Zhang et al. 2022a) and papaya fruits (Fan et al. 2022a).

10.4.3 Phytomelatonin Delays Senescence Zhang et  al. (2021b) employed weighted gene co-expression network analysis (WGCNA) and degradome technology (miRNA target RNA identification) to investigate the molecular mechanisms activated by melatonin treatment for delaying the

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senescence of litchi fruit. Melatonin treatment delayed litchi fruit senescence manifesting by lower pericarp browning and higher chromaticity L*, a*, and b* values. By melatonin treatment, endogenous melatonin accumulation was accompanied by lower endogenous ABA accumulation. Lower endogenous ABA accumulation accompanied by higher PUB protein, RING-H2 finger protein, phosphatase 2C, and F-box expression in litchi fruit treated with melatonin represents a lower ABA signaling pathway, which could be responsible for delaying senescence in litchi fruits. In addition, lower transcription factor bHLHs expression by melatonin treatment could be ascribed to suppressing ABA signaling, which contributes to delaying litchi fruit senescence (Zhang et al. 2021b). By melatonin treatment, suppressing miR858 expression could be responsible for triggering MYB251 and TT2 transcription factors expression which binds to promoters and triggers LcPAL, Lc4CL, LcCHS, LcCHI, LcDFR, LcDFR, LcANS, and LcUFGT expression and anthocyanins accumulation. In addition, suppressing miR160 expression could be responsible for triggering auxin response factor (LcARF) transcription factor expression which binds to promoters and repressing cell wall architecture LcXTH, LcEGase, and LcEXP expression and keeps cell wall strength (Zhang et al. 2021b). Therefore, miR858b and its target gene (miRNA-mRNA pairs) serve as crucial downstream regulators of melatonin signaling to promote anthocyanins biosynthesis, contributing to the delay of pericarp browning and discoloration in litchi fruit. Melatonin treatment suppresses LcVIN3 expression, highlighting histone methylation contribution in delaying the senescence of litchi fruits by melatonin application (Zhang et al. 2021b). VIN3 family proteins accelerate senescence by promoting H3K4me3 accumulation, which refers to tri-methylation at the fourth lysine residue of the histone H3 protein for epigenetic regulation of expression. H3K4 trimethylation regulates expression by chromatin remodeling (Li et al. 2020b). Melatonin treatment promotes zinc finger protein 10 (LcZAT10) and dehydration-responsive element-­binding protein 1 (LcDREB1) expression for delaying the senescence of litchi fruits by maintaining redox homeostasis. In addition, MAPK signaling pathway activation by exogenous melatonin could be beneficial for countering oxidative stress and delaying the senescence of litchi fruits. In addition to the MAPK signaling pathway, triggering NAC transcription factor expression could be responsible for avoiding ROS accumulation and delaying the senescence of litchi fruits by triggering LcAOX expression. In litchi fruits, lower DUFs expression as negative regulation of AA biosynthesis along with lower LcAAO expression as positive regulation of ascorbic acid degradation by melatonin treatment could be beneficial for higher ascorbic acid accumulation and maintaining redox homeostasis (Zhang et  al. 2021b). Melatonin treatment promotes BON association protein 1 (LcBAP1) expression acting as a negative regulator of PCD while suppressing accelerated cell death 6 (LcACD6) and formin protein 18 (LcFH18) expression acting as a positive regulator of programmed cell death (PCD). Therefore, exogenous melatonin delayed the senescence of litchi fruits by suppressing PCD (Zhang et al. 2021b). Melatonin treatment promotes E3 ubiquitin-protein ligase expression and E3-ligase-dependent protein turnover pathway delayed senescence of litchi fruits by

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suppressing PCD (Zhang et al. 2021b). Melatonin treatment promotes phospholipase A (PLA1) and MYC2 for triggering jasmonic acid biosynthesis and signaling, mitochondrial uncoupling protein 5 (LcUCP5) for avoiding ROS accumulation, H+ATPase, Ca2+-ATPase, and pyruvate kinase for ATP supplying and NADP-malic enzyme (NADP-ME) for NADPH supplying, and 3-ketoacyl-CoA synthase (KCS) for fatty acids biosynthesis (Zhang et  al. 2021b). Melatonin treatment promotes LcGAD1, LcCaM, and LcCMLs expression in litchi fruits. Owing to Ca2+/CaM being responsible for GAD enzyme activation, promoting GABA biosynthesis by melatonin treatment in litchi fruits could serve as an antisenescence mechanism by activating GABA shunt and energy providing (Zhang et al. 2021b). By tandem mass tags (TMT)-based quantitative proteomic analysis, Wang et al. (2022a) showed that melatonin treatment promotes pyruvate dehydrogenase, citrate synthase, isocitrate dehydrogenase, NADH dehydrogenase proteins expression in mitochondrial tricarboxylic acid (TCA) cycle, and electron transport system activity, concomitant promotes enoyl-CoA hydratase and acyl-CoA acetyltransferase proteins expression in peroxisome fatty acids β-oxidation pathway activity for ensuring sufficient intracellular energy supplying, promotes 3-dehydroquinate dehydratase, chorismate synthase and chorismate mutase proteins expression in chloroplast shikimate pathway activity for ensuring sufficient intracellular phenylalanine and tryptophan supplying in ‘Kyoho’ grape berry by melatonin treatment (Wang et al. 2022a). Triggering VvODC, VvADC, N-carbamoylputrescine amidase (VvNCA), and spermidine synthase (VvSPDS) expression concomitant with N-carbamoylputrescine amidase (NCA) protein expression could be responsible for promoting endogenous polyamines Put2+, Spd3+, and Spm4+ accumulation, whereas, triggering copper amine oxidases (VvCuAO) expression along with NAD+-amino aldehyde dehydrogenase (AMADH) protein expression could be responsible for promoting endogenous GABA accumulation in ‘Kyoho’ grape berry by melatonin treatment (Wang et  al. 2022a). Accordingly, higher endogenous polyamines and GABA accumulation by melatonin treatment could be beneficial for attenuating oxidative stress in ‘Kyoho’ grape berries as shown by lower electrolyte leakage and MDA accumulation, and delaying quality deterioration as shown by lower berries abscission and decay during cold storage (Wang et al. 2022a). By melatonin treatment, inhibiting ethylene production via suppressing ACC synthase (ACS) and ACC oxidase (ACO) expression and activities (Hu et al. 2022; Zhai et  al. 2018; Liu et  al. 2019c), diminishing chlorophyll degradation via suppressing chlorophyll b reductase (CBR), chlorophyllase (Chlase), Mg-dechelatase (MDC), pheophytinase (PPH), pheophorbide a oxygenase (PaO) and red chlorophyll catabolite reductase (RCCR) expression and activities (Hu et  al. 2022; Wu et al. 2021; Tan et al. 2019, 2020), sufficient intracellular energy supplying arising from higher H+-ATPase, Ca2+-ATPase, SDH, and CCO expression and activities (Tan et al. 2021b; Wang et al. 2020b; Luo et al. 2020; Sun et al. 2022a; Dong et al. 2022a; Li et al. 2021a; Shekari et al. 2021; Lin et al. 2022), sufficient intracellular NADPH supplying arising from higher G6PDH and 6PGDH expression and activities (Tan et  al. 2021b), sufficient intracellular NADP+ supplying by promoting

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nicotinamide adenine dinucleotide kinase (NADK) activity (Tan et al. 2021b), promoting ROS scavenging SOD, CAT, APX, GR, DHAR and MDHAR expression and activities giving rise to higher AA/DHA and GSH/GSSG accumulation accompanying by lower O2•- and H2O2 accumulation (Dong et al. 2022a; Tan et al. 2019, 2020; Ma et al. 2021a; Hu et al. 2018; Zhang et al. 2018; Luo et al. 2020; Liu et al. 2018; Shang et al. 2021; Li et al. 2022d; Wang et al. 2019a; Miranda et al. 2020; Boonsiriwit et al. 2021; Lin et al. 2022; Gao et al. 2016; Zhai et al. 2018; Tang et al. 2020; Magri and Petriccione 2022; Luo et al. 2021; Wei et al. 2022), protective membrane integrity as shown by lower electrolyte leakage and MDA accumulation (Tan et al. 2019, 2020; Ma et al. 2021a; Hu et al. 2018; Zhang et al. 2018; Luo et al. 2020; Liu et al. 2018; Shang et al. 2021; Li et al. 2022d; Dong et al. 2022a), promoting endogenous melatonin accumulation by triggering TDC, T5H, SNAT and ASMT expression (Tan et al. 2019; Liu et al. 2018; Sharafi et al. 2021; Wang et al. 2020b, 2021c; Li et al. 2021a; Shekari et  al. 2021; Lin et  al. 2022; Aghdam et  al. 2019b), suppressing endogenous ABA accumulation via inhibiting 9-cis-epoxycarotenoid dioxygenase (NCEDs) expression (Tan et al. 2019), promoting phenylpropanoid pathway activity representing by higher PAL, C4H, 4CL, and CHS expression and activities along with lower PPO expression and activity giving rise to higher phenols, flavonoids and anthocyanins accumulation along with higher DPPH, FRAP, and ABTS scavenging capacity (Yang et al. 2020; Wang et al. 2019b; Zhang et al. 2018; Liu et al. 2018; Pang et al. 2020; Sharafi et al. 2021; Miranda et al. 2020; Wang et al. 2019a, 2021c; Shang et al. 2021; Magri and Petriccione 2022; Qu et al. 2022a; Li et al. 2021a, 2022d; Boonsiriwit et al. 2021; Wei et al. 2022; Shekari et al. 2021; Lin et al. 2022), preserving firmness arising from suppressing cell wall degrading polygalacturonase (PG), pectin methyl esterase (PME), β-galactosidase (β-Gal), cellulase (Cel) and β-glucosidase (β-Glu) expression and activities (Cao et al. 2022a; Zhai et al. 2018; Liu et al. 2019c; Sun et al. 2022b; Tang et al. 2020; Qu et al. 2022a), lower PLD and LOX expression and activities giving rise to higher phosphatidylcholines accumulation along with lower phosphatidic acid accumulation, higher unSFA/SFA accumulation arising from higher oleic, linoleic and linolenic acids accumulation along with lower palmitic and stearic acids accumulation (Wang et al. 2020b; Luo et al. 2020; Aghdam and Fard 2017; Sharafi et al. 2021), higher protein oxidative repairing methionine sulfoxide reductase (MsrA1, MsrA2, MsrB1, and MsB2) expression (Zhang et  al. 2018), higher intracellular NO accumulation by promoting NOS expression and activity (Sun et al. 2022a; Liu et al. 2019c), promoting signaling H2O2 accumulation arising from higher SOD activity, associated with CAT and APX activities (Aghdam and Fard 2017), promoting GABA shunt pathway activity as shown by higher GAD and GABA-T activities (Aghdam and Fard 2017), promoting endogenous hydrogen sulfide (H2S) accumulation arising from higher l-cysteine desulfhydrase (LCD) and d-cysteine desulfhydrase (DCD) expression and activities (Sharafi et al. 2021), improving cuticle integrity via triggering eceriferum 1 (CER1) and glycerol-3-phosphate acyltransferase 4/8 (GPAT4/8) expression for wax and cutin biosynthesis (Miranda et al. 2020; Cao et al. 2022b), confining intracellular water outflow by suppressing plasma membrane intrinsic

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protein aquaporin (PIP1;4 and PIP2;7) expression and promoting endogenous ABA accumulation by triggering 9-cis-epoxycarotenoid dioxygenase (NCED1) expression (Miranda et al. 2020), enhancing endogenous glutathione (GSH) accumulation along with promoting glutathione S-transferase (GST) activity for endogenous pesticides chlorothalonil, malathion, and glyphosate detoxification (Deng et  al. 2021), and higher ascorbic acid accumulation arising from higher ascorbic acid biosynthesis GDP-d-mannose-3,5-epimerase (GME), GDP-l-galactose guanyltransferase (GGP), GDP-d-mannose pyrophosphorylase (GMP), and l-galactono-­1,4lactone dehydrogenase (GalDH) expression (Dong et al. 2022a) (Fig. 10.3) could be responsible for delaying senescence in broccoli florets (Hu et al. 2022; Wu et al. 2021; Luo et al. 2018; Miao et al. 2020), cabbage leaves (Tan et al. 2019, 2020, 2021a), orange fruits (Ma et al. 2021a), grape berry fruits (Sun et al. 2020c; Yang et al. 2020), kiwifruits (Cheng et al. 2022; Wang et al. 2019b; Cao et al. 2022a; Hu et al. 2018), litchi fruits (Wang et al. 2020b; Zhang et al. 2018, 2021b), lotus seeds (Luo et al. 2020; Sun et al. 2022a), peach fruits (Gao et al. 2016), pear fruits (Zhai et al. 2018; Liu et al. 2019c), strawberry fruits (Aghdam and Fard 2017; Liu et al. 2018; Pang et al. 2020), sweet cherry fruits (Sharafi et al. 2021; Wang et al. 2019a; Miranda et al. 2020), jujube fruits (Deng et al. 2021; Sun et al. 2022b; Tang et al. 2020; Wang et al. 2021c), blueberry fruits (Cao et al. 2022b; Magri and Petriccione 2022; Qu et al. 2022a; Shang et al. 2021), sweetpotato roots (Li et al. 2022d), and white bottom mushrooms (Li et al. 2021a; Lin et al. 2022; Shekari et al. 2021).

Fig. 10.3  Hypothetical model representing mechanisms employed by exogenous melatonin application and endogenous melatonin signaling for delaying senescence and preserving sensory and nutritional quality in horticultural crops during postharvest life

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10.4.4 Phytomelatonin Preserves the Sensory and Nutritional Quality In cut herbaceous peony flowers, higher endogenous melatonin accumulation by higher PlTDC and PlCOMT1 expression could be responsible for lower stem bending due to higher stem strength by promoting lignin accumulation providing mechanical support to cut herbaceous peony flower stems (Zhao et al. 2022). By melatonin treatment, promoting endogenous melatonin accumulation arising from triggering cytoplasmic PlTDC and PlCOMT1 expression could be responsible for enhancing cut herbaceous peony flower stems strength. By employing FTIR spectroscopy and 2D-HSQC analysis, higher S-lignin and G-lignin accumulation (higher S/G lignin accumulation in secondary cell walls) by melatonin treatment could be responsible for enhancing cut herbaceous peony flower stems strength by improving secondary cell walls thickness. By RNA-seq analysis, Zhao et al. (2022) reported that triggering PlPAL, PlCCR, PlCAD, PlCOMT and PlPOD expression by melatonin treatment could be responsible for promoting lignin accumulation while enhancing cut herbaceous peony flower stems strength by improving secondary cell walls thickness. By PlTDC and PlCOMT1 overexpression in tobacco and virus-induced gene silencing (VIGS) in herbaceous peony, endogenous melatonin could be responsible for promoting lignin accumulation while enhancing cut herbaceous peony flower stems strength by improving secondary cell walls thickness (Zhao et al. 2019, 2022). By melatonin treatment, endogenous melatonin accumulation in Merlot grape berry was accompanied by higher ethylene biosynthesis arising from higher VvACS1 expression and higher resveratrol and gallic acid accumulation arising from higher stilbene synthases (VvSTS1), flavonoid 3′-hydroxylase (VvF3′H), leucoanthocyanidin reductase (VvLAR2) and dihydroflavonol-4-reductase (VvDFR) expression (Ma et al. 2021b). By yeast one-hybrid (Y1H) assays and electrophoretic mobility shift (EMS) assays, higher VvMYB14 expression triggers transcriptionally activating VvACS1 by binding to the promoter of VvACS1 and activates its transcription, therefore, higher ethylene biosynthesis could be responsible for promoting phenols, flavonoids, stilbenes, and flavonols accumulation in Merlot grape berry by melatonin treatment (Ma et  al. 2021b). By melatonin treatment concomitant with ethylene action inhibitor, 1-methylcyclopropene (1-MCP) employing, Xu et  al. (2017) reported that the endogenous ethylene biosynthesis and signaling contribute to promoting phenols, flavonoids, and anthocyanins such as chlorogenic acid, gallic acid, epicatechin and malvidin-3,5-glucose accumulation along with improving DPPH, ABTS, and FRAP scavenging capacity by triggering VvSTS, and VvPAL expression in ‘Moldova’ grape berry by melatonin treatment and endogenous melatonin accumulation (Xu et al. 2017). By melatonin treatment, promoting endogenous melatonin accumulation arising from triggering TDC, T5H, SNAT, and ASMT expression (Onik et al. 2021; Zhao et  al. 2022; Wang et  al. 2020a), higher sucrose synthase synthesis (SuSy) and

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sucrose phosphate synthase (SPS) activities along with lower acid/neutral invertase (AIV and NIV) and sucrose synthase cleavage (SuSy) activities (Fan et al. 2022c; Xia et al. 2021), suppressing ethylene production and signaling arising from lower ACSs and ACOs and ERFs expression (Onik et al. 2021), promoting ROS scavenging SOD, CAT, APX, GR, DHAR, and MDHAR expression and activities giving rise to higher ascorbic acid (AA) and glutathione (GSH) accumulation along with lower O2− and H2O2 accumulation (Onik et al. 2021; Wei et al. 2020a), higher heat shock protein (HSPs) expression (Onik et al. 2021), promoting phenylpropanoid pathway activity representing by higher PAL, 4CL, C4H, and CHS expression and activities along with lower PPO expression and activity giving rise to higher phenols, flavonoids and anthocyanins accumulation and higher DPPH, FRAP and ABTS scavenging capacity (Onik et al. 2021; Zhao et al. 2022; Wei et al. 2020a; Wang et al. 2020a; Xia et al. 2021; Zheng et al. 2019; Di et al. 2022), improving anticarcinogenic glucosinolates accumulation by triggering glucosinolates biosynthetic genes (CYP79F1, CYP79B2) and their regulating transcription factors (MYB28, MYB34) expression (Miao et al. 2020; Di et al. 2022), promoting glucoraphanin-sulforaphane system activity by triggering myrosinase activity and its encoding MYO expression accompanied by suppressing AOP expression (Wei et  al. 2020b), promotes alternative electron transporting system activity and sufficient intracellular ATP supplying (Zhu et al. 2018) (Fig. 10.3) could be responsible for prserving sensory and nutritional quality in apple fruits (Fan et al. 2022c; Onik et al. 2021), grape berry fruits (Meng et al. 2019; Sun et al. 2020c; Wang et al. 2020a; Xia et al. 2021; Xu et al. 2017; Yang et al. 2020), broccoli florets (Miao et al. 2020; Wei et al. 2020a, b), and pear fruits (Liu et al. 2019b; Sun et al. 2020a; Zheng et al. 2019).

10.4.5 Phytomelatonin Regulates Fruit Ripening In sweet cherry fruits, preharvest melatonin spraying suppressed respiration at harvest but postharvest melatonin dipping promoted respiration following cold storage, demonstrating that the anti-ripening function of melatonin is reversible by cold temperature. In addition, higher pyruvate dehydrogenase (PaPDH), fumarase (PaFUM), isocitrate dehydrogenase (PaIDH1), oxoglutarate dehydrogenase (PaOGDH), and succinyl CoA ligase (PaSCL) expression was concomitant with higher shikimate kinase (PaSK), Pa4CL1, PaC4H, PaPAL, and PaDFR expression by melatonin treatment by preharvest spraying and postharvest dipping promoted phenols accumulation such as neochlorogenic acid, chlorogenic acid, epicatechin, procyanidins, cyanidin-3-O-galactoside, and cyanidin-3-O-rutinoside in Ferrovia sweet cherry fruits (Michailidis et al. 2021). During banana fruit ripening, higher endogenous melatonin accumulation was concomitant with higher endogenous ethylene production and can be considered as an endogenous pointer for climacteric banana fruit ripening. However, melatonin

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treatment promotes endogenous melatonin accumulation and delays banana fruit ripening by interfering with climacteric ethylene biosynthesis. By suppressing MaACS1 and MaACO1 expression, lower climacteric ethylene production represses starch degradation giving rise to firmer fruits with higher starch accumulation (Hu et al. 2017). By cluster bagging, grape berry cultivar Cabernet Sauvignon exhibited higher serotonin, tryptamine, N-acetylserotonin, and melatonin accumulation at the veraison stage which was associated with higher VvTDC1, VvT5H, and VvSNAT1 expression concomitant lower VvM3H expression, whereas, grape berry cultivar Carignan exhibited higher L-tryptophan, serotonin, and N-acetylserotonin and melatonin accumulation along with lower 5-methoxytryptamine accumulation at veraison stage which was associated with higher VvTDC1, and VvSNAT1 expression concomitant lower VvM3H expression. By cluster bagging, delaying berry ripening represented by lower berry pigmentation could be ascribed to higher endogenous melatonin accumulation in Cabernet Sauvignon and Carignan grape berries (Guo et  al. 2020). Endogenous 5-methoxytryptamine accumulation only in Carignan grape berry during ripening under cluster bagging demonstrates that in Cabernet Sauvignon grape berry tryptophan to tryptamine to serotonin to N-acetylserotonin to melatonin pathway is responsible for melatonin biosynthesis, but in Carignan grape berry, in addition to tryptophan to tryptamine to serotonin to N-acetylserotonin to melatonin pathway, tryptophan to tryptamine to serotonin to 5-­methoxytryptamine to melatonin pathway also contributes in endogenous melatonin accumulation (Guo et  al. 2020). In ‘Niagara Rosada’ table grapes, preharvest salicylic acid spraying extends shelf life by attenuating berry drop and decay. Higher chlorogenic acid, gallic acid, rutin, cyanidin-3,5-diglucoside, and 3-O-glycosidic delphinidin accumulation by preharvest salicylic acid spraying was concomitant with higher tryptophan, 5-hydroxytryptophan, tryptamine, serotonin, and melatonin accumulation, which synergistically contributes in higher berries DPPH, FRAP, and ABTS scavenging capacity (Gomes et al. 2021). By fluoridone (Flu; an inhibitor of ABA biosynthesis), diphenylene iodonium (DPI; an inhibitor of H2O2 biosynthesis), and 1-methylcyclopropene (1-MCP; an inhibitor of ethylene action), Xu et al. (2018) suggested that melatonin treatment promoted “Moldova” grape berry ripening indicated by higher total soluble solids and anthocyanins accumulation along with lower titratable acid accumulation through signaling molecules ABA, ethylene, and H2O2 accumulation. Endogenous melatonin accumulation gives rise to endogenous ABA and H2O2 accumulation which is crucial for triggering ethylene production and signaling which promotes anthocyanins biosynthesis VvMYB1 and VvUFGT expression (Xu et al. 2018). By exogenous melatonin application, delaying Keitt mango fruit ripening was associated with higher firmness, chlorophyll accumulation and lower respiration rate, a* and b* chromaticity, and carotenoid accumulation. By lipidomic analysis, Keitt mango fruits treated with melatonin exhibited higher phosphatidylglycerol and phosphatidylinositol accumulation, along with lower phosphatidylserine and

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phosphatidic acid accumulation, demonstrating protective chloroplast membrane integrity delaying fruit ripening (Dong et al. 2021). In addition, lower lauric, myristic, palmitic, and stearic acids accumulation along with higher oleic, linoleic, and linolenic acids accumulation could be ascribed to lower H2O2 accumulation which preserves membrane integrity as shown by lower MDA accumulation. Consequently, melatonin treatment promotes unSFA/SFA accumulation by remodeling fatty acids for preserving plasma membrane fluidity and integrity which have benefits in delaying the ripening of Keitt mango fruits (Dong et al. 2021). Exogenous melatonin application delays ‘Guifei’ mango fruits ripening by suppressing pulp yellowing as indicated by lower chromaticity b* and β-carotene accumulation, which could be ascribed to delaying climacteric ethylene production arising from lower 1-aminocyclopropane-1-carboxylic acid (ACC) accumulation and ACS and ACO activities, delaying endogenous ABA accumulation arising from lower NCED activity. Lower ethylene and ABA biosynthesis and signaling in ‘Guifei’ mango fruits treated with melatonin could be responsible for preserving firmness by preventing PG, β-Gal, and PME activities (Liu et al. 2020b). By preharvest melatonin application, higher red color development in pear fruits could be ascribed to higher endogenous melatonin accumulation arising from higher PuTDC, PuT5H, PuSNAT, and PuASMT expression giving rise to higher anthocyanins accumulation by triggering anthocyanins biosynthesis regulatory MBW (MYB–bHLH–WD40) protein transcription factors MYB10, MYB114, bHLH, and WD40 and anthocyanins biosynthesis structural PuPAL, PuCHS, PuCHI, PuF3H, PuDFR, PuANS, PuUFGT, PuFLS, and PuLAR expression (Sun et al. 2021b). In pear fruits, NADPH oxidase (PuRBOHF) overexpression promotes anthocyanins accumulation whereas PuRBOHF silencing suppresses anthocyanins accumulation by regulating signaling H2O2 accumulation and anthocyanin biosynthesis PuMYB10, PuPAL, PuCHS, PuCHI, PuDFR, PuANS, and PuUFGT expression. Melatonin treatment promotes signaling H2O2 accumulation arising from triggering plasma membrane NADPH oxidase (respiratory burst oxidase homologs; PuRBOHF) expression. By signaling H2O2 accumulation, dual-luciferase (LUC) reporter assay and GUS staining and activity analysis revealed that PuRBOHF enhances PuMYB10 expression which not only is responsible for PuUFGT promoter activation but also activates PuRBOHF expression and promotes anthocyanin accumulation in pear fruits (Sun et al. 2021c). In the pear cultivar ‘Korla’, melatonin application inhibited hydroperoxide lyase (HPL) activity and suppressed PbHPL expression, whereas in the pear cultivar ‘Abbé Fetel’, melatonin application inhibited LOX activity, suppressed PbLOX1 and PbLOX2 expression, and promoted alcohol dehydrogenase (ADH) and alcohol acyltransferase (AAT) activity, both suppressed hexanal and (E)-hex-2-enal production along with promoted propyl acetate, and hexyl acetate accumulation. Melatonin treatment suppressed ethylene production, promoted ADH and AAT activities, and increased C6 esters production from C6 alcohols in pear fruits (Liu et al. 2019b).

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Melatonin treatment promoting strawberry fruits ripening could be ascribed to promoting endogenous melatonin accumulation resulting from higher FaTDC, FaSNAT, FaT5H, and FaASMT expressions giving rise to signaling H2O2 accumulation by triggering FaRHOB1 expression. By signaling H2O2 accumulation, triggering FaGAMYB expression along with suppressing FaSnRK2.6 expression promotes endogenous ABA accumulation by triggering FaNCED1, FaNCED2, FaNCED3, and FaNCED4 expression and enhancing anthocyanin accumulation by higher FaPAL and FaCHS expressions (Mansouri et al. 2021). During sweet cherry development, lower endocarp lignification accompanied by water seeds higher ROS accumulation was associated with higher MDA accumulation, which triggers PaTDC1 expression and endogenous melatonin accumulation in the exocarp and mesocarp. Endogenous melatonin diffuses from the mesocarp into the endocarp for rescuing watery seeds from oxidative damage by exhibiting ROS scavenging activity. By seed desiccation and endocarp lignification, lower ROS accumulation was associated with lower PaTDC1 expression and lower endogenous melatonin accumulation. In addition to lower ROS accumulation, higher IAA accumulation in sweet cherry fruits during seed desiccation and endocarp lignification could be responsible for tryptophan consumption from melatonin to IAA biosynthesis. Also, daily rhythmic endogenous melatonin accumulation during sweet cherry fruit ripening could be ascribed to high temperature and high light intensity which promotes ROS accumulation giving rise to triggering PaTDC1 expression for protecting fruits from oxidative stress during ripening (Zhao et al. 2013). Tijero et al. (2019) reported that lower endogenous melatonin, salicylic acid, and jasmonic acid accumulation was concomitant with higher endogenous ABA accumulation during Prime Giant sweet cherry fruit ripening, demonstrating an inhibitory regulating mechanism of sweet cherry ripening by endogenous melatonin accumulation. These authors observed that delaying sweet cherry fruit ripening through melatonin treatment could be ascribed to the promotion of endogenous melatonin and cytokinin accumulation including trans-zeatin (Z), trans-zeatin riboside (ZR), and isopentenyl adenosine (IPA), giving rise to lower anthocyanins accumulation. As melatonin is a safe bioactive molecule, this set of results offers an opportunity for its use in the agri-food biotechnology area to govern fruit ripening by regulating hormonal cross-talk (Tijero et al. 2019). Li et al. (2021b) reported that the endogenous melatonin decline during tomato fruit ripening, whereas, monochromatic Red light at a wavelength of 657 nm promotes endogenous melatonin accumulation but monochromatic Blue light at a wavelength of 457 nm suppresses endogenous melatonin accumulation. By double chromatic Red/Blue light (3:1, 75% R light at a wavelength of 657 nm and 25% B light at a wavelength of 457 nm), promoting endogenous melatonin accumulation accelerates tomato fruit ripening. By double chromatic Red/Blue light, phytochromes (Phy) and cryptochrome (Cry) synergistically operation by COP1-HY5/ PIFs signaling pathway could be responsible for promoting endogenous melatonin accumulation by triggering TDC, T5H, SNAT, and ASMT expression, which promoting ethylene biosynthesis by triggering SlACS2, SlACS4 and SlACO1 expression

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accompanying promoting lycopene accumulation by triggering carotenoid biosynthetic genes phytoene synthase 1 (SlPSY1) and carotene isomerase (SlCRTISO) expression (Li et al. 2021b). By double chromatic Red/Blue light, higher H2O2 and MDA accumulation in tomato fruits were accompanied by higher endogenous melatonin accumulation, suggesting that melatonin provides a ROS scavenging mechanism for delaying senescence, in addition to accelerating ripening in tomato fruits (Li et al. 2021b). In addition to endogenous melatonin accumulation, accelerating tomato fruit ripening by melatonin treatment has been reported by Sun et al. (2020b), by triggering SlRIN, SlCNR, and SlNOR transcription factors expression as a positive regulator of fruit ripening concomitant suppressing SlAP2a transcription factors expression as a negative regulator of fruit ripening. By regulating the ripening regulatory transcription factors network, promoting ethylene biosynthesis by triggering SlACS2, SlACS4, SlACO1, and SlACO3 expression along with triggering ethylene signaling SlETR1, SlETR3, SlETR4, and SlETR6 expression could be responsible for lycopene and αand β-carotene accumulation by triggering 1-deoxy-D-xylulose-5-phosphate synthase (SlDXS), 1-deoxy-D-xylulose 5-phosphate reductoisomerase (SlDXR), geranylgeranyl diphosphate synthase (SlGGPS2), phytoene synthase (SlPSY1), phytoene desaturase (SlPDS), ζ-carotene desaturase (SlZDS), carotene isomerase (SlCRTISO), and lycopene β-cyclase (Slβ-LCY1/2) expression in tomato fruits during ripening (Sun et  al. 2020b). In addition, melatonin treatment was unable to promote lycopene accumulation in the ethylene-insensitive mutant, Never ripe (Nr) fruits, suggesting melatonin promotes carotenoid synthesis in tomato fruit through ethylene receptor NR (Sun et al. 2020b). By melatonin treatment and endogenous melatonin accumulation, accelerating tomato fruit ripening was accompanied by promoting lycopene accumulation by SlPSY1 and SlSlCRTISO expression, fruit softening by cell wall degrading SlPG2, SlPE1, SlTBG4, and SlEXP1 expression, ethylene biosynthesis by SlACS2, SlACS4, and SlACO1 expression and ethylene signaling by NR, SlETR4, SlEIL1, SlEIL3, and SlERF2 expression, aroma hexanal biosynthesis by SlLOXC, SlADH2, and SlAAT expression, and water loss by aquaporin SlPIP12, SlPIP21, and SlPIP22 expression (Sun et al. 2015). In addition, higher RIN, FUL1, and lower AP2 proteins expression, higher ethylene biosynthesis ACO1 protein expression, higher carotenoids accumulation CRTISO protein expression, higher cell wall degradation PG protein expression, higher amino acids biosynthesis CM2, AlaAT2, HisC proteins expression, higher aroma flavor biosynthesis PDC1 proteins expression, higher intracellular water outflow (water loss) by lower VHP, V-ATPase, and CCO2 proteins expression, higher anthocyanin accumulation by PAL, CHS1, CHS2, F3H, F3′H, FLS, DFR, 3GT, GST, and ANS genes and proteins expression, cell apoptosis inhibitor (API5) protein expression, POD7/9/12 and CAT3 proteins expression indicated melatonin treatment accelerates ripening but delays senescence by attenuating ROS accumulation in tomato fruits (Sun et al. 2016). Recently, Shan et al. (2022) reported that accelerating tomato fruit ripening by melatonin treatment could be ascribed to regulating DNA methylation of CpG islands of ethylene biosynthesis and

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signaling genes. By melatonin treatment, the DNA methylation levels of the CpG island of SlACS10 and SlERF1 were decreased, and the DNA methylation level of the CpG island of SlCTR1 was increased. In addition, melatonin treatment increased SlACS10 and SlERF1 expression and inhibited SlCTR1 expression (Shan et al. 2022).

10.5 Conclusion During postharvest life, fresh horticultural crops suffer from sensory and nutritional quality deterioration accompanied by fungal decay incidence. Low-temperature storage has been employed for delaying senescence and attenuating fungal decay while maintaining the sensory and nutritional quality of fresh horticultural crops. However, chilling injury occurring confines low-temperature storage employed for economically important horticultural crops. Therefore, worthy attempts have been done by researchers for introducing procedures for alleviating chilling injury and fungal decay accompanied by maintaining sensory and nutritional quality in fresh horticultural crops during low temperature storage. In recent years, melatonin gains great attention for employment as a safe eco-friendly procedure for improving the marketability of horticultural crops (Table. 10.1). By tryptophan supplying from the shikimate pathway, TDC, T5H, SNAT, and ASMT expression and activities are responsible for melatonin biosynthesis in the cytosol, chloroplasts, and mitochondria. By melatonin treatment or promoting endogenous melatonin accumulation by triggering TDC, T5H, SNAT, and ASMT expression or suppressing M2H and M3H expression, CAND2/PMTR1 is responsible for triggering melatonin signaling by employing NADPH oxidase-dependent ROS and Ca2+/CaM secondary messengers while promoting CDPK and MAPK signaling pathway. By melatonin signaling, MYB, NAC, bHLH, bZIP, WRKY, HSF, and ERF transcription factors activation could be responsible for marketability responsive genes expression. In addition to transcription regulation, epigenetic DNA methylation, and histone PTMs accompanied by post-transcriptionally microRNAs (miRNAs) employed by melatonin could be responsible for marketability-responsive genes expression. In addition to gene expression regulation, protein PTMs such as phosphorylation, ubiquitination, SUMOylation, nitrosation, and persulfidation could be employed by melatonin for regulating marketability-responsive metabolic pathways. In addition to signaling function, melatonin serves as an amphiphilic molecule with higher intracellular dynamism exhibiting ROS/RNS scavenging cascade. In addition to direct marketability responsive gene expression, melatonin exhibited overlapping with ethylene, cytokinin, abscisic acid, jasmonic acid, salicylic acid, nitric oxide, hydrogen sulfide, strigolactone, brassinosteroids, phytosulfokine α, and extracellular ATP signaling pathways.

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Table 10.1  Exogenous melatonin application for chilling injury and fungal decay, delaying senescence, and preserving sensory and nutritional quality in horticultural crops during postharvest life Horticultural crops Melatonin effects Chilling injury Peach fruit Signaling H2O2 accumulation, Higher AA biosynthesis, Higher GMPH, GGGT, GME, GPP, GDH and GalLDH expression, Higher SOD, APX, CAT and GR expression, Lower O2− and H2O2 accumulation, Higher membrane integrity, Lower MDA accumulation. Higher NADPH oxidase activity, signaling H2O2 accumulation, Cut anthurium Higher AOX expression, Higher SOD, APX, CAT and GR flower activities, Higher AA/DHA and GSH/GSSG, Higher endogenous proline accumulation, Higher OAT and P5CS activities, Lower PDH activity, Higher phenols accumulation and DPPH scavenging capacity, Higher PAL/PPO activities, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation. Peach fruit Higher SUMO E3 ligase SIZ1 expression, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation. Tomato fruit Higher FAD3 and FAD7 expression, Lower PLD and LOX expression and activities, Higher membrane unsaturation, Lower palmitic, stearic and oleic acids accumulation, Higher linoleic and linolenic acids accumulation, keeping membrane integrity, Lower electrolyte leakage and MDA accumulation. Pomegranate Higher SOD, APX, CAT and GR activities, Lower H2O2 fruit accumulation, Lower PLD and LOX activities, Higher phenols accumulation and DPPH scavenging capacity, Higher PAL/PPO activities, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation. Peach fruit Higher membrane unsaturation, Lower palmitic, stearic and oleic acids accumulation, Higher linoleic and linolenic acids accumulation, Lower LOX activity, Higher OPP pathway activity, Higher G6PDH activity, Higher SKDH activity, Higher endogenous salicylic acid (SA) accumulation, Higher phenols accumulation, Higher PAL/PPO activities. Keeping membrane integrity, Lower MDA accumulation. Tomato fruit Triggering ZAT2/6/12 transcription activity, Higher arginase expression and activities, Higher CBF1 expression, Higher endogenous polyamines accumulation, Higher ADC and ODC expression and activities, Higher endogenous proline accumulation, Higher P5CS and OAT expression and activities, Lower PDH expression and activity, Higher endogenous NO accumulation, Higher NOS expression and activity. Peach fruit Higher PME expression, Lower PG expression, Harmonizing PME and PG expression. Mango fruit Delaying softening, Lower PG and PME activities, Lower ethylene production, Lower ACS and ACO activities, Lower endogenous ABA accumulation, Lower NCED activity.

References Cao et al. (2018b)

Aghdam et al. (2019a)

Shao et al. (2016) Jannatizadeh et al. (2019)

Jannatizadeh et al. (2019)

Gao et al. (2018)

Aghdam et al. (2019c)

Cao et al. (2018a) Liu et al. (2020b) (continued)

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Table 10.1 (continued) Horticultural crops Melatonin effects Litchi fruit Lower electrolyte leakage and MDA accumulation, Higher intracellular ATP supplying, Higher H+-ATPase, Ca2+-ATPase, SDH and CCO activities, Higher endogenous proline accumulation, Higher P5CS and OAT activities along with Lower PDH activity Lotus poods Higher endogenous melatonin accumulation, Higher intracellular and seed ATP supplying, Higher SDH, CCO, H+-ATPase and Ca2+-ATPase activities, Lower O2− and H2O2 accumulation, Lower PLD and LOX activities, Higher oleic, linoleic and linolenic acids accumulation, Lower palmitic and stearic acids accumulation, Lower electrolyte leakage and MDA accumulation. Fungal decay Tomato fruit Higher chitinase, β-1,3-glucanase, PPO and PAL activities, Lower H2O2 accumulation, Higher SOD and APX activities, Higher endogenous MeJA accumulation, Higher LOX and AOC expression, Lower JAZ1 and MYC2 expression. Banana fruit Higher ACO and ERFs expression, Higher IAA amido synthetase expression, Higher endogenous IAA accumulation, Higher NADPH oxidase expression, signaling H2O2 accumulation, Triggering MAPK signaling pathway, Higher ERFs, bZIPs, WRKYs, HSFs and MYBs transcription factors expression, Higher pectin and cellulose accumulation, Higher xyloglucan endotransglucosylase and cellulose synthase expression, Higher 3-ketoacyl-CoA synthase and lipid transfer proteins and MYBs expression, Higher PAL, CHS, 4CL and COMT expression, Higher PLC expression, Higher sHSPs accumulation, Higher HSFs expression. Strawberry Signaling H2O2 accumulation, Higher SOD activity, Lower CAT fruit and APX activities, Higher PAL activity, Higher phenols and anthocyanins accumulation and Higher DPPH scavenging capacity, Higher GAD and GABA-T activity, Higher membrane unsaturation, Lower palmitic, stearic and oleic acids accumulation, Higher linoleic and linolenic acids accumulation, Higher intracellular ATP and ADP and Lower intracellular AMP accumulation. Senescence Peach fruit Higher membrane integrity, Lower MDA accumulation, Lower LOX activity, Higher SOD, CAT and APX activities, Lower O2− and H2O2 accumulation, Higher ascorbic acid accumulation. Cucumber Higher SOD, CAT and APX activities, Lower O2− and H2O2 fruit accumulation, Higher AA and chlorophyll accumulation, Lower respiration rate and ethylene production, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation. Pear fruit Lower ACS and ACO expression, Lower PG and Cel expression, Lower LOX expression, Higher SOD and DHAR activities.

References Liu et al. (2020a)

Luo et al. (2020)

Liu et al. (2019a)

Li et al. (2019c)

Aghdam and Fard (2017)

Gao et al. (2016) Xin et al. (2017)

Zhai et al. (2018) (continued)

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Table 10.1 (continued) Horticultural crops Melatonin effects Pear fruit Higher endogenous NO accumulation, Higher NOS expression and activity, Lower ACS and ACO expression, Lower PG and Cel expression. Strawberry Higher endogenous melatonin accumulation, Higher TDC, T5H, fruit SNAT, and ASMT expression, Higher phenols and flavonoids accumulation and Higher DPPH and ABTS scavenging capacity, Higher membrane integrity, Lower MDA accumulation. Litchi fruit Higher endogenous melatonin accumulation, Higher MSR expression, Higher SOD, CAT, APX and GR activities, Lower O2− and H2O2 accumulation, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation, Higher L*a*b*, Higher phenols, flavonoids and anthocyanins accumulation, Lower PPO activity. Sweet cherry Higher endogenous melatonin accumulation, Higher SOD, CAT, fruit APX and GR activities, Higher ascorbic acid and reduced glutathione accumulation, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation, Lower O2− and H2O2 accumulation. Cut gardenia Higher endogenous melatonin accumulation, Higher TDC flower expression, Higher chlorophyll accumulation, Lower O2− and H2O2 accumulation, Higher SOD, CAT, APX and GR activities, Higher membrane integrity, Lower electrolyte leakage and MDA accumulation. Cabbage leaf Lower SAGs expression, Higher endogenous melatonin accumulation, Higher TDC, T5H, SNAT and ASMT expression, Lower ABF2, ABF4 and ABI5 expression, Lower endogenous ABA accumulation, Lower NCED and AAO expression, Higher chlorophyll accumulation, Lower CBR, PPH, PAO, RCCR, and SGR expression, Higher membrane integrity, Lower electrolyte leakage. Mushroom Signaling H2O2 accumulation, Higher NADPH oxidase activity, Higher SKDH activity, endogenous melatonin accumulation, Lower H2O2 accumulation, Higher AOX expression, Higher PAL/ PPO activities, Higher phenols accumulation and Higher DPPH scavenging capacity, Higher membrane integrity, Lower MDA accumulation. Cassava root Higher endogenous Ca2+ accumulation, Higher endogenous melatonin accumulation, Higher TDC, T5H, SNAT and ASMT expression, Higher ascorbic acid and starch accumulation. Cassava root Higher endogenous melatonin accumulation, Higher TDC, T5H, SNAT and ASMT expression, Lower O2− and H2O2 accumulation, Higher CAT, SOD, APX, and GR expression and activities, Higher ascorbic acid and anthocyanins accumulation, Higher ABTS scavenging capacity, Higher endogenous ethylene accumulation.

References Liu et al. (2019c) Liu et al. (2018)

Zhang et al. (2018)

Wang et al. (2019a)

Zhao et al. (2017)

Tan et al. (2019)

Aghdam et al. (2019b)

Hu et al. (2018) Liu et al. (2019c)

(continued)

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Table 10.1 (continued) Horticultural crops Melatonin effects Cassava root Higher endogenous melatonin accumulation, Higher TDC, T5H, SNAT and ASMT expression, Lower O2− and H2O2 accumulation, Higher CAT, SOD, APX, and GR expression and activities, Higher ascorbic acid and carotenoids accumulation, Higher ABTS scavenging capacity, Higher endogenous gibberellic acid accumulation. Broccoli Higher intracellular ATP supplying, Higher AOX pathway floret activity, Higher SOD and CAT activities, Lower O2− and H2O2 accumulation, Higher chlorophyll accumulation. Grape berry Higher phenols and flavonoids accumulation, Higher CHS, 4CL, fruits F3H, LAR, ANR and DFR expression. Litchi fruit Lower electrolyte leakage, Higher intracellular ATP supplying, Higher H+-ATPase, Ca2+-ATPase, SDH and CCO activities, Lower PLD and LOX activities, Lower palmitic and stearic acids accumulation, Higher oleic, linoleic and linolenic acids accumulation, Lower phosphatidic acid accumulation, Higher phosphatidylcholine accumulation. Sweet cherry Delaying water and weight loss, Improving cuticle integrity, fruit Higher CER1 and GPAT4/8 expression, Lower AQPs expression, Higher NCED1 expression, Higher endogenous ABA accumulation, Lower respiration and ethylene production, Lower pedicle browning, Higher SOD, CAT, APX, DHAR and GR expression, Lower MDA accumulation, Higher anthocyanins accumulation, Higher DFR and UFGT expression. Jujube fruits Higher APX and GR activities, Higher ascorbic acid and reduced glutathione accumulation, Lower PG and PME activities, keeping firmness Nutritional quality Cabbage Higher anthocyanins accumulation, Higher PAL, CHS, CHI, C4H, F3H, F3′H, and DFR expression, Higher SOD, CAT and APX activities, Lower O2−, OH− and H2O2 accumulation, Higher membrane integrity, Lower MDA accumulation. Grape berry Higher endogenous melatonin accumulation, Higher phenols fruit chlorogenic, gallic, caffeic, cinnamic and coumaric acids accumulation, Higher flavonoids epicatechin, catechin accumulation, Higher anthocyanins malvidin-3-glucoside, cyanidin-3-glucoside, pelargonidin-3-glucoside and delphinidin-­ 3-­glucoside accumulation, Higher PAL and CHS expression, Higher resveratrol accumulation, Higher STS expression, Higher DPPH, FRAP and ABTS scavenging capacity, Higher ethylene biosynthesis, Higher ACS and ACO expression, Higher ethylene signaling, Higher ERFs expression. Fresh-cut Higher membrane integrity, Lower MDA accumulation, Lower pear fruit LOX gene expressing, Lower H2O2 accumulation, Higher ascorbic acid accumulation, Higher PAL and CHS expression and activities, Lower PPO expression and activities, Higher phenols accumulation and Higher DPPH and ABTS scavenging capacity.

References Liu et al. (2019b)

Zhu et al. (2018) Yang et al. (2020) Wang et al. (2020b)

Miranda et al. (2020)

Tang et al. (2020)

Zhang et al. (2016)

Xu et al. (2017)

Zheng et al. (2019)

(continued)

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Table 10.1 (continued) Horticultural crops Melatonin effects Plum fruit Higher phenols, anthocyanins and ascorbic acid accumulation, Higher DPPH scavenging capacity. Pear fruit Higher C6 aroma esters biosynthesis, Higher ADH and AAT expression and activities, Lower LOX and HPL expression and activities, Higher linoleic acid accumulation. Pomegranate Higher NADPH accumulation, Higher G6PDH and 6PGDH fruit activities, Higher AOX expression, Higher PAL activity, Higher phenols and anthocyanins accumulation and DPPH scavenging capacity, Higher ascorbic acid and reduced glutathione accumulation, Higher APX and GR activities, Lower AAO activity. Mango fruit Higher phenols, flavonoids and ascorbic acid accumulation, Higher CAT activity, Lower PPO activity, Higher DPPH scavenging capacity. Higher phenols and ascorbic acid accumulation, Higher SOD and Broccoli floret CAT activities, Higher FRAP scavenging capacity, Higher glucosinolates glucoraphanin accumulation, Higher CYPs and MYBs expression. Sweet cherry Higher phenols, flavonoids, anthocyanins and ascorbic acid fruit accumulation, Higher DPPH, ABTS and FRAP scavenging capacity. Strawberry Higher firmness, Higher phenols and ascorbic acid accumulation, fruit Higher DPPH scavenging capacity. Grape berry Higher endogenous tryptophan accumulation, Higher endogenous fruit melatonin accumulation, Higher TDC, T5H, SNAT and ASMT expression, Higher endogenous phenylalanine accumulation, Higher phenols, flavonoids and anthocyanins accumulation, Higher PAL, 4CL, CHS, F3H, DFR, LAR and ANR expression.

References Bal (2019) Liu et al. (2019c) Aghdam et al. (2020)

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Zheng H, Liu W, Liu S, Liu C, Zheng L (2019) Effects of melatonin treatment on the enzymatic browning and nutritional quality of fresh-cut pear fruit. Food Chem 299:125116. https://doi. org/10.1016/j.foodchem.2019.125116 Zhu L, Hu H, Luo S, Wu Z, Li P (2018) Melatonin delaying senescence of postharvest broccoli by regulating respiratory metabolism and antioxidant activity. Nongye Gongcheng Xuebao/Trans Chin Soc Agric Eng 34(3):300–308. https://doi.org/10.11975/j.issn.1002-­6819.2018.03.040 Zhu G-Y, Sha P-F, Zhu X-X, Shi X-C, Shahriar M, Zhou Y-D, Wang S-Y, Laborda P (2021a) Application of melatonin for the control of food-borne Bacillus species in cherry tomatoes. Postharvest Biol Technol 181:111656. https://doi.org/10.1016/j.postharvbio.2021.111656 Zhu Y, Guo M-J, Song J-B, Zhang S-Y, Guo R, Hou D-R, Hao C-Y, An H-L, Huang X (2021b) Roles of endogenous melatonin in resistance to Botrytis cinerea infection in an Arabidopsis model. Front Plant Sci 12:1031 Zou M, Guo M, Zhou Z, Wang B, Pan Q, Li J, Zhou J-M, Li J (2021) MPK3-and MPK6-mediated VLN3 phosphorylation regulates actin dynamics during stomatal immunity in Arabidopsis. Nat Commun 12(1):1–14

Part III

Melatonin and Its Signaling in Biotic and Abiotic Stress

Chapter 11

Melatonin-Mediated Regulation of Biotic Stress Responses in Plants Swati Singh and Ravi Gupta

Abstract  Crop productivity is largely dependent on the severity of biotic stresses that not only reduce the plant performance but also limit the yield significantly. The severity of these stresses depends on various factors including causal organisms and environmental conditions which eventually result in crop loss. Plants use a sophisticated immune system, tightly regulated by various phytohormones and signaling molecules, of which the role of melatonin is recently gained attention. Plants exposed to biotic stresses show a rapid increase in melatonin concentration, suggesting a potential role of melatonin in plant defense. Alternatively, plants supplied with exogenous melatonin exhibit improved resistance against invading pathogens. In this chapter, we discuss the role of melatonin in mediating biotic stress in plants and how melatonin helps in plant defense against various pathogens including bacteria, viruses, and fungi. Keywords  Melatonin · Plant immunity · Biotic stress · Signaling · Anti-microbial

11.1 Introduction Biotic stress is described as damage caused to crops by living organisms including pests and pathogens such as fungi, bacteria, viruses, parasitic nematodes, insects, weeds, and other indigenous or grown plants. The direct yield loss caused by biotic stress accounts for 20–40% of global agricultural productivity (Oerke 2006; Moustafa-Farag et al. 2020). On the advent of any form of biotic stress, plants utilize preformed and induced immune responses that include both physical and chemical defenses such as cuticles, waxes, trichomes, and chemical compounds to protect S. Singh TERI School of Advanced Studies, Department of Biotechnology, New Delhi, India R. Gupta (*) College of General Education, Kookmin University, Seoul, South Korea © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_11

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themselves against herbivores and pathogens (Iqbal et al. 2021). If the pathogen is able to evade this first line of defense, the physical barriers such as cell wall, bark, and waxy cuticle, the second line of defense is activated in plants by recognition of the pathogen-associated molecular patterns (PAMPs) such as flagellin, bacterial lipopolysaccharides, fungal chitin, and peptidoglycans, to activate the PAMPtriggered immunity (PTI) (Gupta et  al. 2015). However, these PTI responses are often feeble and thus pathogens are able to suppress the PTI responses by secreting effector proteins inside the host cells. These effector proteins (Avr proteins) are identified by resistance (R) proteins of plants to activate a relatively stronger immune response, known as effector-triggered immunity (ETI) which often culminates into hypersensitive responses (HR) (Meng et al. 2019). These plant immune responses are tightly regulated by the interplay of several phytohormones such as salicylic acid (SA), jasmonic acid (JA), and ethylene (ET). Moreover, recent investigations have suggested a crucial role of other plant growth regulators such as polyamines (Asija et  al. 2022) and gasotransmitters such as nitric oxide (NO) and hydrogen sulfide (H2S) in plant defense response against biotic stresses (Choudhary et al. 2022). In addition, a growing body of evidence also suggests the role of other chemicals such as melatonin in plant immune responses. Melatonin (N-acetyl-5-methoxytryptamine) was first identified in animals and was isolated from the pineal gland of beef long back in 1958 (Lerner et al. 1958). The primary function of melatonin in animals is to provide darkness signals to the brain and peripheral organs to induce endogenous sleep-wake cycles, seasonal reproduction, and endocrine release cycles (Arnao and Hernández-Ruiz 2014). Owing to the numerous physiological roles performed by melatonin in animals, it is one of the best-studied biological molecules across different groups of the animal kingdom (Carrillo-Vico et al. 2013). Although melatonin was identified in animals in the early 90s, it took 30 years for scientists to detect melatonin in plants with the first report in 1991 where it was identified in unicellular dinoflagellate Gonyaulax polyedra (Poeggeler and Hardeland 1994), followed by Japanese morning glory (Pharbitis nil) (Van Tassel et al. 2001). Subsequently, melatonin was identified in several species of domesticated and wild plants including tomato, banana, cucumber, beetroot, potato, and tobacco (Dubbels et al. 1995; Arnao et al. 2006; Arnao and Hernández-Ruiz 2014). In plants, melatonin exhibits several physiological functions such as growth regulation, activation of rhizogenesis, and delaying induced leaf senescence, among several others (Arnao and Hernández-Ruiz 2014). In addition, some of recent investigations have also suggested a potential role of melatonin in the regulation of biotic stress tolerance in plants (Gupta 2023). In this chapter, we present evidence in support of the role of melatonin in plant immune responses.

11.2 Biosynthesis of Melatonin Melatonin (N-acetyl-5-methoxytryptamine) is an indolic compound that is hypothesized to be synthesized in mitochondria and chloroplasts (Tan et al. 2013; Tan and Reiter 2020). Although melatonin is found both in animals and plants,

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its biosynthetic pathway differs significantly (Back et  al. 2016; Tan et  al. 2016) (Fig.  11.1). In animals, melatonin synthesis begins with tryptophan as a starting material, whereas it is not necessarily in plants. Plants are capable of de novo synthesis of tryptophan using carbon dioxide as substrate via the shikimic acid pathway (Tan et al. 2016) (Fig. 11.1). The biosynthesis of melatonin has four basic steps: (1) hydroxylation/decarboxylation of tryptophan (2) formation of 5-hydroxy tryptamine, commonly known as serotonin (3) N-acetylation of serotonin, and (4) hydroxy methylation of N-acetyl serotonin to result in the formation of melatonin. The initial steps in the biosynthesis of melatonin in animals result in the hydroxylation of tryptophan to 5-hydroxy tryptophan catalyzed by tryptophan 5-hydroylase, however in the case of plants tryptophan is decarboxylated to tryptamine and this step is catalyzed by tryptophan decarboxylase. The tryptamine thus formed in plants is either converted into indole-3-aldehyde and finally to Indole acetic acid (IAA) by the action of indole aldehyde dehydrogenase or can result in the formation of serotonin. In the animal system, serotonin is formed directly from 5-hydroxy tryptophan catalyzed by aromatic amino acid decarboxylase (AADC). Thereafter, the conversion of serotonin to N-acetyl-5-hydroxy tryptamine (N-acetyl serotonin) is catalyzed by alkyl amine- acetyltransferase (AANAT) in animals. However, in plants, alternate pathways for serotonin conversion are reported wherein serotonin is either converted to N-acetyl serotonin catalyzed by N-acetyltransferase (SNAT) or to 5-­methoxytryptamine catalyzed by ASMT (N- acetyl serotonin-O-methyl transferase). The methoxytryptamine thus formed results in the formation of melatonin by

Fig. 11.1  Biosynthetic routes of melatonin in plant and its comparison with the animal cells

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the action of the SNAT enzyme. The conversion of N-acetyl serotonin to melatonin, the final step of melatonin biosynthesis, is catalyzed by hydroxyindole-O-methyl transferase (HIOMT) enzyme in both animals as well as plants (Fig. 11.1) (Arnao and Hernández-Ruiz 2014; Tan and Reiter 2020).

11.3 The Physiological Role of Melatonin in Plants Early work on the physiological role of melatonin production in plants has ascertained its role as a potent antioxidant. Melatonin is capable of neutralizing (1) reactive oxygen species (ROS) such as superoxide anion, hydroxyl radical, and hydrogen peroxide, (2) reactive nitrogen species (RNS) such as nitric oxide, peroxynitrite, and nitrogen dioxide, and (3) various other harmful compounds including toxins, medicines, and insecticides, among others (Corpus et  al. 2022; Arnao and Hernández-Ruiz 2019). Melatonin has been shown to have a strong scavenging capacity against hydroxyl radicals, nitric oxide, peroxynitrite, and nitrogen dioxide. To achieve an acceptable cellular redox equilibrium, melatonin regulates ROS and RNS levels through a direct chemical interaction or by modulating the expression of a large number of genes including FaHSFA3, FaAWPM, FaCYTC2, SAD, CAT, APX, MAPK, bZIP60, BIP2, BIP3, CNX1, CDPK1, MAPK1, TSPMS, ERF4, HSP80, and ERD15, among others (Arnao and Hernández-Ruiz 2019; Zhao et al. 2017; Alam et al. 2018; Lee and Back 2018). Melatonin has been characterized to bear key physiological functions in two major categories: (i) melatonin as a plant growth stimulator; and (ii) melatonin as a regulator of flowering and fruit ripening. Owing to its chemical similarity to Indole acetic acid, melatonin is presumed to either mimic the activity of the plant hormone auxin or act on the auxin upstream pathway to increase its action (Arnao and Hernández-Ruiz 2018, 2019). However, according to a recent study, melatonin and auxin function in separate pathways and have little in common in terms of biological functions (Zia et al., 2019). Reports of melatonin as a plant growth stimulator in promoting different aspects of plant growth have been well documented (Arnao and Hernández-Ruiz 2019, 2020). Melatonin has been found to promote seed germination in wheat, Stevia rebaudiana, cotton, and Limonium bicolor (Simlat et al. 2018; Li et al. 2019a, b; Nabavi et al. 2019). It is also been found to promote lateral root generation in rice, Arabidopsis, and tomato (Liang et al. 2017; Chen et al. 2018a, c; Ren et al. 2019), to enhance photosynthetic efficiency in tomato and maize, (Chen et al. 2018b; Debnath et al. 2018; Ahmad et al. 2019), to increases the biomass in Lupinus albus, cherry and Prunella vulgaris (Hernández-Ruiz et  al. 2004; Sarropoulou et al. 2012; Fazal et al. 2018), and to elevate the yield in soybean and wheat (Qiao et al. 2019). In reference to its function as a regulator of flowering and fruit ripening, melatonin has been reported to delay flowering in rice, apple, Chenopodium rubrum (Zhang et al. 1991, 2019; Kolář et al. 2003; Korkmaz et al. 2014). On the contrary, when a melatonin synthetic enzyme (Serotonin N-acetyltransferase) was knocked

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out in Arabidopsis, it resulted in a reduction of melatonin levels, and eventually, flowering was delayed (Lee et al. 2014). Melatonin has been reported to improve fruit ripening and improve fruit quality during post-harvest in tomato, grape, Capsicum annuum, (Sun et al. 2015; Xu et al. 2018; Tan and Reiter 2020) while an antagonistic effect has been seen on fruit ripening in cherry (Tijero et al. 2019; Tan and Reiter 2020). Tan et al. (2012) proposed that the biological role of melatonin in plants is to protect them from environmental stressors and the hypothesis tested true when researchers started ascertaining the amount of melatonin in stress induced plants and relating the same with better adaptability of plants towards stress. Exogenously provided or endogenously produced melatonin allows plants to survive and thrive under conditions of hot, cold, drought, waterlogging, salinity, cadmium or other metals, and chemical pollutions (Zheng et al. 2017; Qi et al. 2018; Li et al. 2019a; Liu et al. 2019; Naghizadeh et al. 2019; Zhang et al. 2019). In addition, a growing body of evidence also shows that melatonin can improve plant resistance to the virus, pathogenic bacterium, and fungal diseases (Yin et al. 2013; Chen et al. 2018a; Zhang et al. 2018a, b; Liu et al. 2019).

11.4 Melatonin in Plant Defense Against Biotic Stress To withstand the influence of environmental changes throughout plant growth and development, the plant can adapt to diverse biotic (Mandal et al. 2018; Zhao et al. 2021) and abiotic (Chen et  al. 2017) stresses. Melatonin’s physiological role in plants’ tolerance toward stress has been well documented (Fan et al. 2018). Many signaling molecules, such as ROS (Pardo-Hernández et al. 2020) and NO (Zhu et al. 2019) are required for the immunological response of melatonin in plants to send both intracellular and intercellular messages. Melatonin has been shown to have immunomodulatory, antioxidant, anti-inflammatory, and neuroprotective properties in animals (Regodón et  al. 2005; Carrillo-Vico et  al. 2013; Vielma et  al. 2014; Nabavi et al. 2019), suggesting that it could be used as a therapeutic alternative for microbes. On the other hand, numerous recent studies have demonstrated the positive effects of melatonin in plant-pathogen interactions (Fig. 11.2) (Moustafa-Farag et al. 2020). Under a variety of abiotic and biotic conditions, melatonin acts as a strong antioxidant and has been shown to directly scavenge ROS improving plant stress resistance (Reiter et al. 2018). Melatonin also alters the roles of key components related to stress tolerance, fungal infection, and commonly used chemical fungicides, all of which are hazardous to most living organisms, indicating less lethality even under high concentrations upon comparison with its chemical counterparts. Thus, on a global scale, scientists are systematically and methodically probing the potential of melatonin in synthetic applications for biotic and abiotic stress management (Tripathi et al. 2021). Zhao and his coworkers (2021) found that biotic stressors such as pathogen attacks or any other microbial infection in the plants trigger the synthesis of endogenous melatonin, ROS, and RNS. Furthermore,

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Fig. 11.2  An overview of melatonin induced disease resistance in plants. Melatonin triggers PAMP-mediated immune response accompanied by modulation of JA and SA signalling which in turn cascades the expression of defence proteins. Furthermore, melatonin-induced defense response is also mediated by changes in the accumulation of secondary metabolites and antioxidative defence

cellular responses may occur under stressful situations as a result of the interaction between extracellular signals and plasma membrane receptors (Tripathi et al. 2021). This could disrupt the cellular homeostasis mechanism, resulting in an overabundance of ROS and RNS, as well as other ions. These are some of the potential causes of oxidative stress and, ultimately, cell death (Zhao et  al. 2021). Because of the above reasons, there is a possibility of developing a transgenic potato crop that can supply more melatonin and create sRNA by modifying the important genes controlling melatonin biogenesis in potato and amino acid metabolism in P. infestans (Tripathi et al. 2021).

11.5 Role of Melatonin as an Antibacterial Agent In microbes, melatonin was first discovered in Escherichia coli, which is a type of intestinal bacteria (Luo et  al. 2020). In combination with the uptake of a-­proteobacteria and cyanobacteria as ancestors of mitochondria and plastids, bacteria are even considered to be the evolutionary source of melatonin in eukaryotes (Tan et al. 2013; Hardeland 2019). Because many bacteria generate melatonin or dwell close proximity to melatonin-producing microbes, low concentrations of melatonin, to which these organisms are exposed anyway under physiological conditions, are unlikely to have antibacterial effects (Table 11.1). This does not, however, prevent bacteriostatic effects at high concentrations or the protection of hosts from bacterial harm or inflammatory responses generated by bacterial challenges (He et al. 2021). Melatonin has been proven to bear excellent antibacterial properties, including protection against bacterial infections of pathogenic gram-­positive and gram-negative bacteria such as Pseudomonas aeruginosa, Acinetobacter

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Table 11.1  Physiological roles of melatonin in different plant diseases Pathogen Botrytis cinerea

Disease Gray mold disease

Plant Arabidopsis thaliana

Physiological role Increased melatonin reduces cell membrane damage, also enhances Superoxide dismutase and Peroxidase activity, allowing scavenging of excess ROS Plasmodiophora Clubroot Arabidopsis Increased melatonin resulted brassicae disease thaliana in high expression of the JA-responsive PR3 and PR4 genes Sclerotinia Sclerotinia Brassica rapa Melatonin treatment in infected leaves resulted in sclerotiorum stem rot ssp. increased thiamine synthesis, pekinensis ribosomal synthesis-related proteins, amino acid metabolism, adenosine-­ triphosphate (ATP) content and the activity of antioxidant enzymes in B. rapa infected leaves. Colletotrichum Anthracnose Capsicum Melatonin mitigates the gloeosporioides annuum infection by modulating the CHITINASE gene and enhancing the antioxidant activity Podosphaera xanthii Powdery Citrullus Melatonin treatment resulted mildew lanatus in upregulatation of 27 genes that were associated in both PAMP (pathogen-associated molecular pattern) and ETI (effector- triggered immunity) mediated plant defenses Penicillium Green mold Citrus Melatonin reduces resistance digitatum disease reticulata to Penicillium digitatum- by scavenging defense-related ROS in diseased fruits Fusarium oxysporum Fusarium Cucumis Exogenous melatonin wilt sativus application resulted in an increased rate of AMF (arbuscular mycorrhizal fungi) colonization resulted in reduced levels of malondialdehyde, H2O2, and electrolyte leakage

Reference Zhu et al. (2021)

Chang et al. (2018) Teng et al. (2021)

Ali et al. (2021)

Mandal et al. (2018)

Lin et al. (2019)

Ahammed et al. (2020)

(continued)

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Table 11.1 (continued) Pathogen Pseudoperonospora cubensis

Disease Downy mildew

Plant Cucumis sativus

Diplocarpon mali

Marssonina apple blotch

Malus prunifolia

Phytophthora, Rhizoctonia spp., soil microbes

Apple replant disease

Malus domestica

Fusarium oxysporum Fusarium f. sp. cubense wilt

Musa acuminata

Phytophthora infestans

Potato late blight

Solanum tuberosum

Botrytis cinerea

Gray mold disease

Solanum lycopersicum

Physiological role Increased melatonin enhances Superoxide dismutase, Peroxidase activity and catalase activity, allowing scavenging of excess ROS Melatonin treatment resulted in boosting chitinase gene expression, controlling hydrogen peroxide (H2O2), and regulating the expression of pathogenesis-related (PR) proteins Exogenous supplementation of melatonin resulted in elevating K levels and stimulating photosynthesis. Melatonin treatment resulted in production of defense-­ related plant hormones such as Indole acetic acid (IAA), salicylic acid (SA), Jasmonic acid (JA), ethylene. Foliar spray of exogenous melatonin resulted in (i) reducing mycelial development, (ii) modifying cell ultrastructure, (iii) decreasing virulence Melatonin inhibits H2O2 production and increases the expression of methyl ester, allene oxide cyclase, lipoxygenase, proteinase inhibitor II, involved in the jasmonic acid signaling mechanism

Reference Sun et al. (2019)

Yin et al. (2013)

Li et al. (2018)

Wei et al. (2017)

Zhang et al. (2017)

Liu et al. (2019)

baumannii, and Staphylococcus aureus (Tekbas et  al. 2008). Melatonin has also been shown to significantly reduce the symptoms in mice infected with S. aureus and E. coli (Bishayi et al. 2016). Melatonin has also been shown to limit the growth of Mycobacterium tuberculosis, albeit the specific mechanism is unknown (Wiid et al. 1999). Antimicrobial resistance among gram-positive bacteria (most notably S. aureus, Enterococcus faecium, Enterococcus faecalis, and Streptococcus pneumoniae) has become a major public health concern, prompting the development of new anti-infection drugs and promoting melatonin as a promising candidate (Abbas et al. 2017). A. baumannii is a conditional pathogen that causes pneumonia, meningitis, and bacteremia (Amaya-Villar and Garnacho-Montero 2019). It frequently causes hospital infection (110) and is often resistant to several antimicrobial drugs

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(Fernández-García et  al. 2018), making clinical treatment difficult. Melatonin, effectively inhibits the growth of A. baumannii (Tekbas et al. 2008), suggesting that it could be used as an additional medication in the treatment of hospital infections. Melatonin has also been shown to protect Arabidopsis and tobacco from Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) infection (Lee et  al. 2014). Promising data on the impact of stress-related genes and phytohormones on defense against bacterial infections in plants has been obtained, but more research is needed (He et al. 2021).

11.6 Role of Melatonin in the Viral Infections Melatonin’s antiviral action in animals has been established in numerous studies (Table 11.1). Melatonin treatment, for example, reduced the harmful effects of reactive oxygen species (ROS) implicated in the spread of the Venezuelan equine encephalomyelitis (VEE) virus. In comparison to infected control mice, melatonin treatment drastically reduced blood and brain viruses (Vielma et al. 2014). Melatonin and the antiviral medicine ribavirin were combined in another investigation to dramatically boost the survival rate of influenza-virus-infected mice compared to ribavirin treatment alone (Huang et al. 2019). Melatonin, with its great antioxidation efficacy and ability to lower endoplasmic reticulum stress, may be able to regulate autophagy during some viral infections (Boga et al. 2019). Until now only a few studies have looked into melatonin’s antiviral properties in plants. In Nicotiana glutinosa and Solanum lycopersicum seedlings infected with Tobacco mosaic virus (TMV) viral RNA, the virus concentration was reduced after treatment with exogenous melatonin (100 mM, twice). This beneficial effect of melatonin was ascribed to an increase in Salicylic acid (SA) levels in the Nitric oxide (NO)-dependent pathway (Zhao et al. 2019). Melatonin also effectively eradicated apple stem grooving virus (ASGV) from virus-infected apple shoots of “Gala” in-vitro, suggesting that it could be a helpful tool for producing virus-free plants (Chen et al. 2019).

11.7 Role of Melatonin as an Antifungal Agent Melatonin is implicated in plant resistance to a variety of fungi in the realm of biotic stress (Table 11.1) (Moustafa-Farag et al. 2020). Several theories have been offered to explain the protective action of melatonin against plant fungal infections. Melatonin’s ability to maintain H2O2 cellular concentration and the regulation of antioxidant enzyme activities has been attributed to its defense mechanism (Aghdam and Fard 2017). According to RNA sequencing results in Arabidopsis, 6 stress receptors (TolB related protein, Description TolB related protein Disease resistance protein (TIR-NBS class), Toll-Interleukin-Resistance domain family protein TIR-­ NBS-­LRR, TIR-NBS-LRR class disease resistance protein, Receptor like protein 22 and Leucine rich repeat transmembrane protein) exhibited a change in transcript

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levels of at least two fold in response to melatonin (Weeda et al. 2014). In watermelon, transcriptome analysis through RNA sequencing for assessing the role of melatonin in multiple disease resistant (MDR) to powdery mildew and Phytophthora fruit rot revealed 27 upregulated genes that were associated with constitutive defense as well as initial priming of the melatonin-induced plant resistance response (Mandal et al. 2018). The identified 27 genes were primarily associated with the activated defense pathway in response to an external biotic stimulus such as 5 genes involved in defense response to the bacterial pathogen Pseudomonas syringae pv tomato DC3000 and 4 genes associated with defense against plant pathogenic fungi such as P. infestans and Blumeria graminis f.sp. hordei (powdery mildew). Therefore, melatonin buildup in plants increases resistance to foliar diseases such as powdery mildew and soil-borne oomycetes in watermelon and other cucurbits by altering the expression of defense-responsive genes involved in ETI- and PAMP-­ mediated defenses (Mandal et  al. 2018). Foliar spray of exogenous melatonin in varying concentrations (1, 3, 6, 8, 10  mM) was reported to limit Phytophthora infestans-­caused potato late blight infections by (i) reducing mycelial development, (ii) modifying cell ultrastructure, (iii) decreasing virulence, and (iv) reducing the ability of stress tolerance of P. infestans (Zhang et al. 2017). In Potato plants, the synergistic inhibitory impact caused by co-treatment with melatonin and a well-­ known fungicide “Infinito” composed of Fluopicolide and Propamocab was also discovered, and it was observed that melatonin reduced the dosage and efficacy of chemical fungicides in potato late blight fungus management. According to RNA-­ sequencing studies, melatonin appears to be able to limit the growth of P. infestans by modifying the homeostasis of amino acid metabolisms in fungus (Zhang et al. 2017). Zhang et al. (2018b) found that combining melatonin with ethylicin (1- ethylsulfonylsulfanylethane; a biological fungicide) has a synergistic effect that suppresses Phytophthora nicotianae development in-vitro and in-vivo by disrupting the fungus’ amino acid metabolic equilibrium which eventually reduced the advent of tobacco black shank disease. Exogenous melatonin treatment either at 0.1 or 0.5 mM concentration enhanced apple (Malus prunifolia) resistance to Marssonina apple blotch (Diplocarpon mali) by boosting chitinase gene expression, controlling hydrogen peroxide (H2O2), and regulating the expression of pathogenesis-related (PR) proteins such as phenylalanine ammonia-lyase (PAL; EC 4.1.3.5), and b-1,3-glucanase (EC 3.2.1.39) (Yin et al. 2013). Foliar spray of 100 μM melatonin treatment stimulated the production of defense-related plant hormones [Indole acetic acid (IAA), salicylic acid (SA), Jasmonic acid (JA), ethylene] in banana (Musa acuminata) through modulation of MaHSP90 expression, hence improving resistance to Fusarium wilt (Wei et  al. 2017). Exogenous supplementation of 200 μM melatonin in replant soil alleviates apple replant disease (ARD) symptoms by promoting apple seedling growth, elevating K levels, and stimulating photosynthesis (Li et al. 2018). In stored apple juice, the addition of 250 mg/L and 500 mg/L melatonin suppressed total microorganisms including mold, yeast, and bacteria to around 72% and 81% upon comparison with control, during the storage period (4–12  hours)(Zhang et  al. 2018a). Unlike the other research, melatonin was found to diminish resistance to Penicillium digitatum-­ caused green mold disease on citrus fruit by scavenging defense-related ROS in

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diseased fruits (Lin et al. 2019). Foliar spray of 50 μM melatonin on tomato fruits promoted tomato fruit resistance to Botrytis cinerea by inhibiting H2O2 production and increasing the expression of methyl ester (MeJA), AOC (allene oxide cyclase), LoxD (lipoxygenase), PI II (proteinase inhibitor II), involved in the jasmonic acid signaling mechanism (Liu et al. 2019). However, two genes JAZ1 (JASMONATE ZIM DOMAIN 1) and MYC2, identified as a negative regulators of pathogen-­ responsive genes in the JA signaling pathway resulted in significant inhibition upon 50  μM melatonin spray on tomato fruits. Furthermore, in Arabidopsis thaliana, transgenic lines overexpressing N-acetylserotonin methyltransferase, one of the main enzymes in the melatonin biosynthetic pathway resulted in elevated melatonin levels as compared to silenced or control plants. This increased melatonin reduces cell membrane damage, thus increasing resistance to Botrytis cinerea and relieving biotic stress (Zhu et  al. 2021). Increased endogenous melatonin also enhances superoxide dismutase (SOD) and peroxidase (POD) activity, allowing the scavenging of excess ROS and, as a result, improved plant defense against B. cinerea (Zhu et al. 2021). In Arabidopsis, both, the incidence of Plasmodiophora brassicae infection and the number of pathogen sporangia were reduced after exogenous application of 10 μmol/L melatonin, and this reduction was ascribed to the high expression of the JA-responsive PR3 and PR4 genes (Chang et al. 2018). Powdery mildew on cucumber seedlings pre-treated with 100 mM melatonin was dramatically reduced by increasing the enzyme activity of antioxidant enzymes such as catalase (CAT), APX, POD and SOD. This pretreatment of melatonin on cucumber seedlings also lowered the illness index by nearly 43% upon comparison with control seedlings (Sun et al. 2019). Exogenous foliar spray of 10 μM and 100 μM of Brassica rapa ssp. pekinensis infected with Sclerotinia sclerotiorum showed increased amounts of adenosine triphosphate (ATP), antioxidant enzymes such as SOD, POD, CAT, and glutathione reductase (GR), sulfur metabolism enzymes such as cysteine synthase, cysteine desulfurase, and succinate dehydrogenase [ubiquinone] flavoprotein subunit (SDHA). In response to S. sclerotiorum infection, many important enzymes and metabolites in thiamine biosynthesis, such as asparagine synthetase [glutaminehydrolyzing] (ASNA), tryptophan synthase (TRPs), S-adenosylmethionine synthase (SAMs), cysteine desulfurase, pyruvate, leucine, methylmalonate, and lysine, were upregulated leading to an increased accumulation of thiamine in Arabidopsis. However, in response to melatonin treatment, thiamine formation was inhibited while glutathione (GSH) was promoted, inferring the transfer of sulfur from thiamine synthesis to GSH in order to protect against S. sclerotiorum infection in B. rapa leaves (Teng et al. 2021). In a recent study by Ali et al. 2021, melatonin mitigates the infection of Colletotrichum gloeosporioides by modulating the CHITINASE gene and enhancing the antioxidant activity in Capsicum annuum L. (Ali et al. 2021). Melatonin has also been studied to lower the damage caused by increased ROS production such as reduced photosynthesis levels, enhanced metabolite biosynthesis, decreased antioxidant capacity of plants, and greater oxidative stress in cells, tissues, or whole organisms caused by penicillin fungal infections on citrus fruits, by eliminating reactive oxygen species (ROS) (Zhu et  al. 2021). Exogenous melatonin application (100 μM melatonin) on the foliage of cucumber

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seedlings infected with Fusarium oxysporum resulted in an increased rate of AMF (arbuscular mycorrhizal fungi) colonization in cucumber roots, possibly suppressing Fusarium wilt. In Fusarium-infected plants, both melatonin and AMF significantly reduced the levels of malondialdehyde, H2O2, and electrolyte leakage, and their combination treatment resulted in an even greater reduction. The findings imply that melatonin and AMF work together to improve cucumber plant resistance to Fusarium wilt (Ahammed et al. 2020). Owing to its significant role in mediating antifungal response in plants, melatonin can be potentially utilized to reduce the use of chemical fungicides as a potential synergist. It is said to improve the efficacy of chemical fungicides, thereby limiting their higher dose application on plants, and eventually reducing crop protection requirements (Zhang et al. 2017; Madigan et al. 2019).

11.8 Conclusions With a global increase in greenhouse gases, the frequency and severity of diseases are increasing in the crops and thus loss of crop yield is imminent in the coming few decades. The need of the hour is to protect our crops and eventually increase their yield to bridge the supply chain. In this process, the identification of natural compounds with an ability to provide tolerance toward stress is the most crucial part of the research. Thus, identifying the potential of melatonin to strengthen plants subjected to multiple abiotic/biotic stressors has opened up an interesting area of study. Being a natural substance with less lethal consequences and better resistance to phytopathogens, it has become a sought-after compound to be utilized especially for crop improvement and pathogen protection. With the advent of next-generation sequencing, proteomics, and transcriptomics, the role of melatonin in regulating the genes/proteins underlying providing resistance to stress can be elucidated and utilized in a synchronized way for crop improvement. Acknowledgments  SS is grateful to the Council of Scientific & Industrial Research; Industrial Research (CSIR), Govt. of India for the award of the RA Fellowship. This work was supported by a  grant  from the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science, and Technology (grant no. RS-2023-00248352).

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Chapter 12

Emerging Roles of Melatonin in Mitigating Pathogen Stress Hala B. Khalil, Ahmed M. Kamel, Ammar Y. Mohamed, Deyaa Hesham, Yousef Mahmoud, Roqaia Ibrahim, Nabil Salama, and Mohammed H. Elsayed Abstract  Melatonin has gained substantial interest in agriculture. This multi-­ functional molecule has unique aspects in plant growth, development, and resistance. Melatonin is an environmental-friendly compound that can be used as an alternative strategy for empowering plants to cope with stress conditions. In that respect, there have been white hands to elucidate the impact of melatonin on plants. Furthermore, shreds of evidence have been presented to highlight the role of melatonin on various plants infected by bacteria, fungi, viruses, and nematodes. However, it is necessary to investigate in detail the role of melatonin on plant defense. Till now, the direct function of melatonin in stimulating plant pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) is vague. However, the capability of melatonin to enhance plant immunity and trigger defense-related genes has been proven in several investigations. In light of these studies, melatonin counteracted pathogens by reprogramming plant cellular responses and activating defense-related genes. Recently, the phytomelatonin receptor has been discovered in Arabidopsis named phytomelatonin receptor 1 (PMTR1). This finding has emerged speculations of melatonin function as a plant hormone. Although components of the melatonin signaling pathway remain to be discovered, this chapter offers insights for understanding melatonin’s subsequent pathways. Here, we explain how melatonin alleviates pathogen responses by uncovering aspects of the signaling pathway associated H. B. Khalil (*) Department of Biological Sciences, College of Science, King Faisal University, Al-Ahsa, Saudi Arabia Department of Genetics, Faculty of Agriculture, Ain Shams University, Cairo, Egypt e-mail: [email protected] A. M. Kamel · R. Ibrahim · N. Salama · M. H. Elsayed Department of Genetics, Faculty of Agriculture, Ain Shams University, Cairo, Egypt A. Y. Mohamed · Y. Mahmoud Department of Biotechnology, Faculty of Agriculture, Cairo University, Cairo, Egypt D. Hesham Faculty of Pharmacy, Ain Shams University, Cairo, Egypt © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_12

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with melatonin-induced stomatal immunity and the crosstalk among hormones for plant defense. Keywords  Phytomelatonin · Pattern-triggered immunity · Effector-triggered immunity · Phytomelatonin receptor 1 · Stomata closure, signal transduction · Plant hormones · Defense-related genes · Pathogenesis-related proteins

12.1 Introduction The emerging plant hormone phytomelatonin is a ubiquitous molecule that regulates various biological and physiological processes such as photosynthesis, germination, rooting, fruit ripening, and circadian rhythms (Arnao and Hernández-Ruiz 2018a, 2018b, 2019). Melatonin levels range from undetectable to high concentrations in plants (Hardeland 2016). It has been detected by many techniques including enzyme-linked immunosorbent assay (ELISA), radioimmunoassay (RIA), gas chromatography-­mass spectrometry (GS-MS), and high-performance liquid chromatography (HPLC) (Nawaz et al. 2016). During harsh environmental conditions (biotic and/or abiotic stress), plants accumulate a large amount of phytomelatonin (Arnao 2014). In addition, plants tend to produce accumulated amounts of melatonin intermediates like serotonin, tryptophan, and tryptamine. Melatonin has significant antioxidant potential and scavenges reactive oxygen species (ROS) and reactive nitrogen species (RNS) (Arnao and Hernández-Ruiz 2015). It is also involved in regulating downstream signaling transduction pathways in plants challenged by harsh conditions (Wang et al. 2018). Interestingly, exogenous melatonin application elevates the expression of genes-­ controlled endogenous melatonin biosynthesis pathways. All exogenous melatonin treatments have been carried out under laboratory-scale conditions. Therefore, field studies are required to determine the effects of melatonin treatment on final crop yield under standard and harsh environmental conditions. In this respect, melatonin can be an alternative candidate to current agricultural practices. Thus, the application of melatonin to plants could benefit the environment compared to other synthetic chemicals used for protection against different stress conditions (Agathokleous et al. 2021). Melatonin may also play an important role in combating simultaneously combined stresses in crops which are a real challenge these days. Plants develop strategies to counteract pathogens. They have a sophisticated immune system in two organized layers. First, they detect microbial tags or pathogen-­associated molecular patterns (MAMPs/ PAMPs) by pattern recognition receptors (Jones and Dangl 2006; Dodds and Rathjen 2010). The second layer involves plant resistance (R) proteins for pathogen specific effector recognition and activation of effector-triggered immunity (ETI, a branch of the plant immune system activated by the recognition of secreted microbial effectors and recognized by intracellular receptors to induce strong, specific and localized immune reactions) (Nimchuk et al. 2003; Jones and Dangl 2006). Reports explained the activation of

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pattern-triggered immunity (PTI, a branch of the plant immune system induced when membrane receptors perceive generic molecules from microorganisms and provided basal immunity against entire classes of pathogens) and ETI responses by phytohormones and signaling molecules during pathogen infection (Moustafa-­ Farag et al. 2020; Tiwari et al. 2020). Till now, the direct role of melatonin in stimulating PTI and ETI is unknown and needs hands in research. To our knowledge, progress has been made in plant melatonin studies as a stimulator for plant immunity but the exact molecular mechanism is still elusive to researchers. Several investigations demonstrate the capability of melatonin to counteract pathogens by activating the expression of defense-related genes against microbes (Mandal et al. 2018; Sharma and Zheng 2019; Zhan et al. 2019; Moustafa-­ Farag et al. 2020), The outcomes of these indicated the functions of melatonin in reprogramming cellular responses (Mandal et al. 2018; Sun et al. 2016; Liu et al. 2019; Ali et al. 2021), elevating the endogenous melatonin level in plants (Zhang et al. 2015; Moustafa-Farag et al. 2020), and activating stress-response genes, and increasing resistance (Aghdam and Fard 2017; Tiwari et al. 2020). In this chapter, we highlighted the direct roles of melatonin in plants towards direct inhibition of pathogens by demonstrating putative plant melatonin receptors, explaining the role of melatonin in stomatal closure for defending pathogens, elucidating the signal transductions switched on by melatonin applications, demonstrating the crosstalk with other plant hormones, and finally presenting genes regulated explicitly by melatonin for increasing plant pathogen defense.

12.2 Melatonin Receptor Candidates Regulate Plant Defense Response Melatonin receptor has been recently identified in plants as a G-protein coupled receptor (GPCR, a cell surface receptor acts like an inbox for messages or connives information sent by other cells). For Arabidopsis, candidate G-protein coupled receptor 2/ Phytomelatonin receptor 1 (CAND2/ PMTR1) has been characterized as a melatonin receptor based on several lines of evidence. First, an investigation on a mutant of Arabidopsis, cand2, was found to be insensitive to melatonin-induced stomatal closure (Wei et  al. 2018). Moreover, an Arabidopsis thaliana PMTR1 mutant, cand2–1, altered the daily rhythm of stomatal closure and ROS production (Li et al. 2020). Another study by Yang et al. (2021) demonstrated the capability of PMTR1, the plasma membrane protein, to transduce signals from the flagellin sensing 2/ Brassinosteroid 1 complex (FLS2/BAK1) to the mitogen-activated protein kinase (MAPK) signaling cascade by upregulating the expression of MAPK3 and MAPK6 genes and to the heterotrimeric G-protein signaling pathway by directly interacting to the Gα, GPA1, protein (Fig. 12.1c and d). Both studies emphasized the role of melatonin AtPMTR1-dependent mechanism on stomatal closure to prevent pathogen invasion.

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Fig. 12.1  Melatonin and PMTR1 regulate the stomatal closure during pathogen infection. (a) The chemical formula and model of the melatonin molecule. (b) The human GPR175 receptor protein was the closest to the Arabidopsis PMTR1 protein, with ~15% sequence similarity. (c) PMTR1 activates heterotrimeric G-protein assembly by direct interaction with the Gα. (d) PMTR1 transduces signals from the flg22 peptide and FLS2/BAK1 receptor complex to the MAPK signaling cascade and the Gα of the heterotrimeric G-protein

Unlike plants, human cells stimulate and regulate the perception of melatonin through four G-protein coupled receptor candidates (MT1, MT2, GPR50, and GPR175). The conservation of melatonin receptor protein sequences of AtPMTR1 and human MT1, MT2, and GPR50 is poor, but all have seven predicted transmembrane domains and are known as membrane proteins (Fig. 12.1b). Of the four human receptor candidates, the GPR175 receptor protein was the closest to the AtPMTR1 protein, with about 15% sequence similarity, (Wei et  al. 2018). In humans, the

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function of GPR50 proteins counteracted the heterodimerization of MT1 and MT2 formation, therefore PMTR1 maybe not be an authentic plant melatonin receptor but it is essential in mediating melatonin signaling (Levoye et al. 2006). Besides Arabidopsis PMTR1, plasma membrane melatonin receptors were identified by a homology-based search in Nicotiana and maize. A couple of putative transmembrane receptors, trP47363 and trP13076, in Nicotiana benthamiana have been reported to recognize melatonin and melatonin homologs, 5-­methoxytryptamine and 5-methoxyindole (Kong et al. 2021). Both receptors appear to be involved in the induced immunity response in N. benthamiana through their silencing that altered the induction of stomatal closure, pathogenesis-related protein 1 (PR1) gene expression, and SA accumulation by melatonin and its homologs. In addition, trP47363 and trP13076 were most likely to recognize melatonin through the in silico molecular docking analyses. Both Nicotiana members, trP47363 and trP13076, revealed lower protein sequence similarity to AtPMTR1. On the contrary, the other members, trP49122 and trP40966, revealed unpromising results to melatonin docking results were the closest to AtPMTR1. On the other hand, Zea mays PMTR1 was identified as a potential phytomelatonin receptor that revealed strong binding activity to melatonin (Wang et  al. 2021). The overexpressing ZmPMTR1 also largely rescued defects in melatonin-induced stomatal closure in the cand2–1 mutant. In response to plant-microbe interaction, Receptor-like kinases (RLKs) may act as alternative melatonin receptor candidates. During the invasion, pathogens have a specific type of protein effector called flagellin peptide 22 (flg22) that has a special binding to plant FLS2/BAK1 receptors (Fig. 12.1d). This interaction may trigger the perception of melatonin by its receptor. As a result, Ca+2 influx, ROS process, MAPK cascade, and stomatal closure mechanisms are activated to counteract microbial invasion (Yang et  al. 2022). In Arabidopsis, FLS2 is an RLK protein involved in plant innate immunity that perceives flg22 which then activates the MAPK cascade and the WRKY transcription factors that activate the expression of several defense-related genes including glutathione S-transferase 1 (GST1), PR1 and PR5 (Back et al. 2016). One or more of the 600 RLKs could act as a plant melatonin receptor. This is still an open question and such quality investigations are required to assign RLK involved in melatonin perception in plant cells.

12.3 Closing ‘Doors’ for Pathogen Invasion via PMTR1 and Phytomelatonin Signaling in Circadian Stomatal Closure Like humans, plants transduce signals to perceive the transition from day to night. These signals regulate metabolisms for circadian stomatal rhythms. For Arabidopsis, the stomatal opening is regulated by the circadian transcription-translation feedback loops during downtime (Hassidim et  al. 2017). Meanwhile, the expression of defense genes peaks in the early morning. On the other hand, endogenous phytomelatonin elevates in the morning to regulate the expression of PMTR1.

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Phytomelatonin acts as darkness signaling in daily stomatal closure for preventing the entry of pathogens. In the afternoon, the expression of PMTR1 peaks to initiate a transient ROS burst resulting in stomata closure late in the day and remaining closed at night (Fig. 12.2a). ROS burst occurred due to the interaction between phytomelatonin and PMTR1 that activates NADPH oxidase-dependent ROS production, both leading to an increase in the production of ROS. All of these result in boosting Ca2+ influx and K+ efflux. At midnight, the stomata are closed to avert the entry of pathogens when the expression of defense genes is downregulated. Stomata are doors for pathogen invasion. In some cases, pathogens have a specific type of protein sequence called flg22 peptide with a special affinity to some plant receptors such as FLS2/BAK1. This particular affinity triggers the activation of GPA1 and MAPK cascades resulting in a ROS burst, Ca2+ influx, K+ efflux, and stomatal closure. As a result, ROS and the stomatal closure mechanism are initiated and will occur and be considered as a physical barrier that inhibits microbial invasion (Fig. 12.2b). In addition, activation of PMTR1 via phytomelatonin and flg22 signals are integrated via PMTR1for initiating the plant’s innate immune responses (Yang et al. 2021).

12.4 Melatonin-Mediated Signaling Response for Disease Resistance Signal transduction secondary messengers including calcium, MAPK cascade, and hydrogen peroxide (H2O2) connect upstream receptors to activate downstream responsive genes. Melatonin has been known as a signaling molecule in plants during pathogen invasion. Under biotic stress, melatonin unregulated the expression of genes involved in the activation of receptors/ kinases/ Ca+ ions that help in stress signal perception in plants (Weeda et  al. 2014). Once the signal gets perceived, melatonin interacts with transcription factors, such as C-repeat binding factors (CBF), dehydration-responsive element-binding protein (DREB), ethylene-­ responsive transcription factors (ERF), NAC, MYB, and WRKY (Shi et al. 2015; Fan et al., 2018). This interaction will elevate the expression of stress-responsive genes that will benefit the plant in overcoming microbes (Fig. 12.3). Another essential signaling pathway that plays a vital role in melatonin-induced signaling is MAPKs. Inoculating Arabidopsis by flg22 peptides activated various MAPK3 and MAPK6 which activated the flg22 signal transduction network with MAPKKK1-MKK4/5-MPK3/6 (Lee and Back 2016). The stimulation of various MAPKs was detected by exogenous melatonin in response to the pathogen and triggered plant innate defense in both Arabidopsis and tobacco plants. In Arabidopsis, pathogen attack-induced melatonin biosynthesis promotes MAPK kinases cascade involved in different MAPKs such as oxidative signal-induced kinase 1 (OXI1), followed by the MAPK kinase 4/5/7/9 and MAPK3/6 cascades (Fig. 12.3). Melatonin-­ mediated MAPK activation causes the SA receptor to translocate into the nucleus and interact with multiple transcription factors for PR1 and isochorismate synthase

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Fig. 12.2  Circadian rhythm of phytomelatonin modulates stomatal closure in Arabidopsis. (a) the stomatal opening is regulated by the circadian rhythm; the expression of defense-related genes peaks in the early morning; endogenous phytomelatonin elevates the expression of PMTR1; the expression of PMTR1 peaks to initiate a transient ROS burst resulting in stomata closure late in the day and remaining closed at night. (b) The interaction between phytomelatonin and PMTR1 activates NADPH oxidase-dependent ROS production. All of these result in boosting Ca2+ influx and K+ efflux

1 (ICS1) leading to pathogen resistance (Lee and Back 2016). In addition, MPK6 stimulates ET production by activating the 1-aminocyclopropane-1-carboxylate synthase 6 enzyme (ACS6). Melatonin can act as an elicitor for activating MPK3 and MPK6 in response to infection (like flg22) (Lee and Back 2021). This increases the expression of several defense genes such as PR1, ICS1, GST1, and ascorbate peroxidase 1 (APX1) (Lee et al. 2015; Lee and Back 2017).

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Fig. 12.3  Exogenous melatonin-mediated regulation in response to pathogen invasion. Melatonin upregulates the expression of genes involved in the activation of receptors/ kinases/ Ca+2 ions that help in stress signal perception in plants. Exogenous melatonin application induces changes in gene expression in different pathways resulting in defense-related gene induction. The expression of MAPK, ICS1, APX1, PR1, PR5, ACS6, and GST1 activates by various melatonin treatments. Melatonin crosstalk with phytohormone signaling for biotic resistance. Melatonin is an essential regulator of genes involved in the SA, ET, and JA pathways

12.5 Melatonin Crosstalk with Phytohormone Signaling for Biotic Resistance Plants develop defense responses to protect the intact tissues from pathogen attack by accumulating ET, JA, and SA (Zulfiqar and Ashraf 2021). The three hormones act as signaling molecules in various effective defense mechanisms. The systemic acquired resistance (SAR) is accompanied by accumulating SA and defensive genes encoding PR proteins that hold antimicrobial or antifungal properties (Lee et  al. 2014), while the induced systemic resistance (ISR) is activated by ET and JA (Bari and Jones 2009). In a detailed transcriptomic study, melatonin considerably elevated the expression of genes involved in the production of ABA, SA, JA, and ET and their associated downstream stress-responsive genes (Weeda et  al. 2014). In plants, innate immunity induced by melatonin is suppressed in mutants defective in SA and ET signaling (Lee and Back 2017). Both SA and melatonin are thought to have positive impacts on plant-pathogen responses (Arnao and Hernández-Ruiz 2018a, 2018b).

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Recently, findings have reported the indirect impact of melatonin on plant-­ pathogen inhibition by inducing SAR (Zhao et al. 2019; Chen et al. 2019; Moustafa-­ Farag et al. 2020). Studies on Arabidopsis inoculated with virulent bacteria explained that exogenous melatonin application increased SA-mediated induced defense in plants (Shi et  al. 2015; Zhao et  al. 2015). Serotonin N-acetyltransferase (SNAT) knockout Arabidopsis mutants displayed decreased SA levels, increased susceptibility to P. syringae, and upregulated various defense-related genes (Lee et al. 2015). In a similar study, exogenous melatonin increased the transcript expression of the ICS1 gene resulting in an increase of SA production (Lee et al. 2014). Another study involving various host-pathogen combinations suggested melatonin as a secondary messenger in the plant’s immunity through the SA-dependent pathways (Zhao et al. 2019). Moreover, the three-way interaction of melatonin with ET and SA has been observed through studies obtained from npr1, ein2, and mpk6 Arabidopsis mutants resulting in reduced bacterial multiplication (Lee et al. 2014). Melatonin is an essential regulator of genes involved in the JA pathway. For instance, melatonin treatment minimizes the post-harvest decay in tomatoes caused by Botrytis cineraria due to JA signaling pathway activation (Liu et  al. 2019). Melatonin treatment increased methyl jasmonate gene expression and the expression of JA biosynthesis-related genes allene oxide cyclase (AOC), lipoxygenase (LoxD), and proteinase inhibitor II (PI II). For Arabidopsis, most JA-related genes were induced by adding melatonin when screened in a high-throughput transcriptome analysis (Ren et  al. 2019). Moreover, knockout of tomato MAPK3 reduced resistance of tomato plants against B. cinerea where MAPK3 mutant showed down-­ regulation of JA-signaling pathway-related genes (Zhang et al. 2018).

12.6 Melatonin Regulates the Defense-Related Genes Several defense-related genes are upregulated by melatonin. Several reports revealed the relationship between melatonin and defense-related genes. During fungal infection, the expression of defense-related genes such as chitinase (CHI), glucanase (GLU), polyphenol oxidase (PPO), and phenyl ammonialyase (PAL) was activated by melatonin when treated with Capsicum annuum (Ali et al. 2021). Both CHI and GLU enzymes play essential roles in destroying fungal cell walls. In addition, the PPO enzyme catalyzes the oxidation of phenolic chemicals to generate quinines, which have antibacterial and cytotoxic properties against microorganisms (Tiwari et al. 2020). PAL is also an important enzyme in the phenylpropanoid pathway and, by extension, in plant disease resistance (Aghdam and Fard 2017). Sun et al. (2016) speculated how the expression of genes for PAL and PPO increased by melatonin pretreatment. Moreover, watermelon plants transformed with the melatonin biosynthetic gene SNAT were more resistant to powdery mildew disease caused by Podosphaera xanthii (Mandal et al. 2018). Cucumber plants infected by powdery mildew were healed when 100 mM melatonin was applied. Moreover, melatonin pretreatment reduced the illness index by activating antioxidant-related genes,

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(Zhang et al.,2018). For bacterial invasion, PR1 and PR5 were also activated due to melatonin-induced antibacterial mechanisms against phytopathogenic bacteria. Furthermore, sucrose and glycerol are implicated in melatonin-related protection against (Pst) DC3000  in Arabidopsis SA- and NO-dependent pathways Zhao et al. (2015). Finally, melatonin is a master regulator phytohormone in plants. The potential role of melatonin in helping plants to defend against pathogen attacks could be a novel path. Under laboratory-scale conditions, treatments by melatonin have been applied. However, large-scale applications of melatonin are rarely performed. Therefore, field treatments are essential to know the impact of melatonin on final crop yield and quality under regular and environmental stress conditions. Furthermore, the combined impacts of melatonin and traditional technologies are required to be evaluated for potential applications in agriculture.

12.7 Conclusion Melatonin is a multifunctional compound that can be used as an alternative strategy for enhancing plants to tolerate stress conditions. Evidences highlighted the role of melatonin on plants infected by pathogens. Melatonin can be an alternative candidate to current agricultural practices. Thus, the application of melatonin to plants could benefit the environment compared to other synthetic chemicals used for protection against different stress conditions. Melatonin may also play an important role in combating simultaneously combined stresses in crops which are a real challenge these days. Aknowledgement  The authors express their gratitude to the Deanship of Scientific Research at King Faisal University, KSA, for their generous financial support with Grant No. 3731. They also acknowledge the Biological Sciences Department at King Faisal University for providing the graet atmosphere to finalize this chapter. Funding  This work was supported by Deanship of Scientific Research at King Faisal University, KSA with Grant No. 3731.

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Chapter 13

Eco-Physiological and Morphological Adaptive Mechanisms Induced by Melatonin and Hydrogen Sulphide Under Abiotic Stresses in Plants Khadiga Alharbi, Mona H. Soliman

, and Abbu Zaid

Abstract  Under the present era of changing climate, non-biotic pressures such as low or high temperature stress, constant heat waves, ultra-violet (UV) radiations, oxidizing agents, heavy metal and metalloids and salinity are continuously increasing and pose significant retardations in plants’ physiological processes to a great extent. Plants are equipped with adaptive mechanisms which enable them to withstand these induced effects. However, in today’s era, when the global temperature is increasing at an alarming rate, these mechanisms are not sufficient to protect plants from stress-induced growth and photosynthetic inhibitions. The application of plant growth regulators (PGRs) has gained an interesting insight in this regard. The melatonin (Mel) and hydrogen sulphide (H2S) are emerging plant elicitors which impart abiotic stress tolerance in diverse crop plants. The ameliorative role of these PGRs under various abiotic pressures in controlling diverse adaptive mechanisms in diverse crop plants is a topic that is still in infancy stage. Therefore, in the present chapter, the role played by Mel and H2S in regulating complex physiological and morphological adaptive mechanisms under myriads of abiotic pressures is apprehensively discussed. Keywords  Abiotic pressures · Eco-physiology · Morphology · Melatonin · Hydrogen sulphide K. Alharbi Department of Biology, College of Science, Princess Nourah Bint Abdulrahman University, Riyadh, Saudi Arabia e-mail: [email protected] M. H. Soliman Botany and Microbiology Department, Faculty of Science, Cairo University, Giza, Egypt Biology Department, Faculty of Science, Taibah University, Yanbu, Saudi Arabia e-mail: [email protected]; [email protected] A. Zaid (*) Department of Botany, Government Degree College Doda, Jammu and Kashmir, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_13

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13.1 Introduction There is a significant threat to the global production of crop plants due to the current status of changing climate. Under changing climate, plants are simultaneously exposed to biotic and abiotic pressures. As they are sessile in nature and have to perform their normal metabolism continuously under various environmental stresses, including extreme temperatures, high salt ions, heavy metals and metalloids, water-logging, drought, ultraviolet (UV) radiation, deficit soil nutrient availability, pest and pathogen attack. These stress factors hinder plant growth and performance, alter the plant-soil ecosystem, and finally result in significant losses to productivity of crop plants (He et al. 2018; Sharma et al. 2019; Zaid et al. 2021, 2022). Waqas et al. (2019) estimated that about 90% approximate of global arable land is under threat to one or more environmental stress factors, which results in the loss of 70% yield in crop plans. Nevertheless, between 1980 and 2012 in USA, heat and drought stress caused $200 billion losses in major crop plant production (Suzuki et al. 2014). In general, abiotic stress factors pose significant negative impacts on principal plant developmental processes through alterations in physiological and biochemical processes that impact various signalling mechanisms that are directly related with the plant growth and productivity (Ritonga and Chen 2020; Johnson and Puthur 2021; Moon and Ali 2022). There are myriads of negative effects of abiotic stress factors (salinity, heat, drought, cold, water-logging, and heavy metal and metalloids) on the growth, development, and yield of crop plants. Nonetheless, there are present millions of microorganisms (viruses, archaea, protozoa, fungi, and bacteria) that live in the soil environment, and the interactive effects of plants and microbes are crucial for sustainable agricultural productivity. Abiotic stress factors greatly affect the diversity of soil microbes, alter the structure of the microbial flora thereby directly and indirectly influence plants’ optimal performance. Excess generation of diverse reactive oxygen species (ROS) in organisms (plants and animals) is called as oxidative stress, which damages various biomolecules-lipids, proteins, DNA and RNA, thus leading to injury and death of cells (Zaid and Wani 2019; Sachdev et al. 2021; Mittler et al. 2022). Plants are bestowed with efficient antioxidant gadgets which scavenge excess ROS, thus maintain a balance between ROS generation and production. However, an imbalance between oxidants and antioxidant molecules results in oxidative stress under the effects of abiotic stress, thus damaging biomolecules and interrupt the redox signalling in crop plants (Zaid and Wani 2019; Hasanuzzaman et al. 2020; Mansoor et al. 2022). To palliate such abiotic stress-induced oxidative stress, plants have evolved numerous signalling pathways that help trigger various adaptive morphological and physiological responses. Phytohormones are chemical signalling elicitors that modulate various adaptive responses under myriads of biotic and abiotic stress in plants. Nevertheless, the external supplements of desired doses of various plant growth regulators (PGRs) have yielded promising results in the era of changing climate. Melatonin (Mel) and hydrogen sulphide (H2S) are two potent signalling elicitors that modulate plants’

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growth and development under normal or stressful environmental conditions. Both help regulate numerous vital processes, such as stabilization of proteins and enzymes, respiration, metabolic energy storing and shifting, photosynthate synthesis and partitioning, osmoregulation, chelation of metal/metalloid ions, and signal transduction mechanisms. But their individual and/or combined dose dependent response in modulating various adaptive responses in diverse crop plants receives less attention. Therefore, in this present chapter, we tend to shed light on the effects of these two elicitors in modulation various responses under myriad of abiotic pressures.

13.2 Melatonin and Hydrogen Sulphide: An Introduction Under Drought Stress Conditions Melatonin is a pleiotropic signalling molecule that exerts multiple functions in diverse crop plants. Since its discovery in plants, numerous evidences have yielded insights into its biosynthesis, catabolism, and physiological and biochemical adaptive functions under abiotic and biotic stress situations (Nawaz et al. 2020; Reviewed by Arnao and Hernández-Ruiz 2021). Plant Mel is primarily an antioxidant molecule which exerts important actions in controlling the production of various ROS and reactive nitrogen species (RNS), and other lethal oxidants present in plant cells. For the first time in 1995, two groups engaged in vascular plant research identified the presence of Mel (N-acetyl-5-methox-ytrytamine) in plants (Hattori et al. 1995; Dubbels et al. 1995). In addition, in case of animal tissues, Mel was reported to act as an antioxidant molecule to control ROS production and lipid peroxidation (Reiter et al. 2014). However, the fascinating role of Mel as an antioxidant in a wide range of organisms, such as fish, birds, and animals was discovered earlier (Fenwick 1970; Vivien-Roels and Pévet 1993). Melatonin was also identified in plants and algae (Fuhrberg et al. 1996; Pape and Lüning 2006). The biosynthesis of Mel in plants is different from animals and its synthesis is affected by many factors in plants; whilst light being a principal factor. The mitochondria and chloroplasts are two sites of Mel biosynthesis in plants. There are various groups of enzymes present in these organelles to catalyse its synthesis via synthetic procedures. The Mel production is a two-way process, that is, if its synthesis is blocked in mitochondria, it will start in chloroplasts. In plants, Mel is produced by a specific enzyme M3H (Li et al. 2019). Under drought stress conditions, phytomelatonin shows modulatory role in conferring biotic and abiotic stress tolerance. Dai et al. (2020) applied Mel (100 μM) to enhance drought stress resistance in two contrasting rapeseed (Brassica napus L.) genotypes (Qinyou 8; drought-sensitive and Q2; drought-tolerant). The result showed that rate of photosynthesis (Pn), stomatal conductance (gs), water use efficiency (WUE) and chlorophyll content were decreased under drought for Qinyou 8, whereas, drought only decreased Pn and chlorophyll content in Q2. In Qinyou 8, the drought exposure decreased actual photochemical efficiency in saturated light (Fv′/ Fm′), actual photochemical efficiency (PhiPSII), quenching of photochemical

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efficiency (qL) and electron transport rate (ETR) but in case of Q2 genotypes, it was found that exposure to drought stress only decreased Fv′/Fm′ and qL. In contrast, drought boosted the contents of malondialdehyde (MDA) and hydrogen peroxide (H2O2) in the roots of both genotypes. Application of Mel enhanced catalase (CAT) activity, promoted taproot and lateral root growth, stomatal opening under drought stress that resulted in an increment in the rate of photosynthesis in both genotypes. Ye et al. (2016) showed that foliar Mel (100 μmol/L) increased Zea mays L. drought-­ stress tolerance by palliating the drought-induced photosynthetic inhibition and oxidative damage. When plants were exposed to drought stress, H2O2 and MDA were increased. The Mel applied plants showed recovered Pn, Gs and transpiration rates and maintenance of high turgor potential and relative water content (RWC) and enhanced enzymatic and non-enzymatic antioxidant activity. Liu et al. (2015) investigated the efficacy of exogenously applied Mel to improve seedling health index and drought-stress tolerance in tomato plants. Drought stress decreased chlorophyll contents, Pn and the kinetics of chlorophyll fluorescence. The pre-treatment of Mel (0.1 mM) significantly allayed these negative impacts and enhanced root vigor, PSII reaction centers efficiency and the antioxidant defense system. In the last few decades, there has been an increasing interest on the effect of H2S on the integrative plant physiology. A plethora of reports from the last 3 decades (e.g. Thompson and Kats 1978) suggest that it can have profound effect on the growth of crop plants, but according to recent work published suggests that it is a fundamental signalling molecule biosynthesised in plants that control basic plant functions (Zhang et  al. 2010). Hydrogen sulphide is a colorless, low molecular weight soluble gas having bad odor and possess phytotoxic effects. According to Watts (2000) out of the total natural sulfur emission (i.e., 52 Tg), H2S represents only 8.5% (i.e., 4.4 Tg). Hydrogen sulphide is present in atmosphere and is contributed by volcanos, wetlands, geothermal vents, salt marshes, livestock, industries and factories, biomass and fossil fuels combustion, and anaerobic respiration from bacteria. From atmosphere, H2S is taken up by plants through foliage via stomata which alters the normal metabolism of sulphate (Ausma and De Kok 2019). In most of the investigations on H2S involving growth and physiological traits, sodium hydrosulfide (NaHS) has been used as a donor molecule (Ahmed et  al. 2021). However, sodium sulfide (Na2S) is also used as a potent donor of H2S (Ziogas et al. 2018). In plants, H2S functions as a gaseous signalling molecule under non-biotic stress conditions that shows a regulatory interplay with other PGRs, signalling molecules, and ROS. There are several enzymes in plant systems that are capable of generating H2S, which is part of the metabolism of cysteine (Cys). These enzymes consist of L-and D-cysteine desulfhydrase (L-DES/D-DES), sulfite reductase (SiR), cyano alanine synthase (CAS) and cysteine synthase (CS) (Calderwood and Kopriva 2014; Zhang 2016; Corpas et al. 2019). These enzymes are present in different compartments of a cell, viz- cytosol, chloroplasts and mitochondria (Hancock and Whiteman 2016; Singh et al. 2020). It is now being applied in diverse crop plants for protection against drought stress conditions. Hosseini et al. (2021) studied Mel mediated effects on drought impacts on growth and essential oil (EO) yield of lemon verbena (Lippia citriodora) plants. Four levels of drought stress were applied by

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maintaining soil water level at 100% field capacity (FC) (control), 75% FC (mild drought), 50% FC (moderate drought) and 25% FC (severe drought) for 45 days. Melatonin (100 or 200 μM) was applied once a week (5 sprays in total during the entire growth period under drought treatments). Two levels of drought-stress impositions caused a significant reduction in plant height, biomass and mineral balance. Exogenous Mel prevented oxidative damages by enhancing the SOD, APX and CAT activities and increased levels of total phenolic compounds, chicoric acid, caffeic acid and chlorogenic acid, ascorbate and total antioxidant capacity. Nevertheless, Mel treatment improved the concentrations and yield of EO in the leaves of the tested plants in all drought treatments. Xia et al. (2020) studied the Mel mediated non-enzymatic and enzymatic antioxidative underlying mechanisms in kiwifruit under drought stress by the transcriptomes method. The transcriptomes of tested plants were evaluated under control (CN), DS (drought stress), and DSM (drought + Mel) treatments. The differential gene expression between DS and DSM were found. It was also found that the content and gene expression of ascorbic acid (AsA), glutathione (GSH), and carotenoid were higher in the DSM treatments as compared to others. In addition, the activity and mRNA expression levels of CAT, POD and SOD, were also high under DSM. Finally, it was concluded that exogenous Mel induced the ascorbic acid-glutathione (AsA-GSH) cycle, carotenoid biosynthesis, and protective enzyme system to improve seedling growth under drought stress regimes.

13.3 Melatonin and Hydrogen Sulphide Under Metal/ Metallloid Stress As plants are sessile and require unprecedented improvements to avoid themselves from the harsh surroundings like other living organisms. The disturbances caused by anthropogenic emissions, climate change, improper use of pesticides, fertilizers and environmental cues, the concentration of metal/metalloid (metal/s) in increasing at an alarming rate. Both Mel and H2S showed palliating role in reducing the harmful effects of ions of metal/s stress. It has been reported by various researches that elevated levels of metals induced the endogenous biosynthesis of Mel in barley (Arnao and Hernández-Ruiz 2009), tomato (Li et al. 2016; Cai et al. 2017), soybean (Imran et  al. 2022), lupin (Arnao and Hernández-Ruiz 2013), tobacco (Lee and Back 2017), Arabidopsis thaliana (Byeon et al. 2016) and wheat (Kaya et al. 2019). Nabaei and Amooaghaie (2020) studied the integrative effects of Mel and nitric oxide (NO) under Cd stress in Catharanthus roseus (L.) G. Don. The various doses (0, 50, 100, and 200 mg Cd kg−1 soil) of Cd were used by using CdSO4. The results revealed that 50 mg kg−1 Cd had no significant effect on the fresh and dry weight of roots and shoots and contents of chlorophyll a and b, but the higher levels of Cd (100 and 200 mg kg−1) significantly reduced these traits and induced an increase in EL and altered nutrient dynamics. The CAT and POD activities were increased under low Cd doses (50 and 100 mg kg−1) but showed a decrement under 200 mg kg−1

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Cd. The application of Mel and NO to the foliage of plants increased shoot biomass, contents of Chl a and b, boosted activities of POD and CAT, but lowered down the values of EL, and increased the contents of essential cations. Both Mel and NO under Cd stress of C. roseus increased Cd phytoremediation efficiency. Mir et al. (2020) applied Mel to analyse the modulation in photosynthesis capacity, redox status, and elemental composition in Brassica juncea cv. Varuna under natural environmental conditions in the net house of the Department of Botany, Aligarh Muslim University, Aligarh, India. The screening experiment consisted of five different doses (10, 20, 30, 40, or 50 μM) of Mel as foliar spray to the leaf of tested plants at 25 days after sowing (DAS). The sampling of the plants was done at 30, 45, and 60 DAS. The obtained results indicated that 40 μM Mel proved to the best in improving most of the parameters, i.e., growth, photosynthetic, nutrients, and enzyme activities at the same time reduced the ROS accumulation by enhancing the antioxidant enzyme activities. The 40  μM Mel increased the stomatal aperture maximally. Okant and Kaya (2019) studied the role of endogenous NO in Mel-improved tolerance to Pb toxicity in maize plants. In the experimentation, a solution of 0.05-or 0.10 mM Mel was sprayed for a period of 10 days to maize plants grown under Pb stress (0.1-mM PbCl2). It was observed that Pb toxicity significantly caused reductions in plant biomass (both fresh and dry), Fv/Fm, total chlorophyll, leaf potassium (K), calcium (Ca), and leaf water potential, but increased levels of proline, H2O2, MDA, EL, endogenous NO and leaf Pb content. In another experiment, the role of NO in mitigation of Pb toxicity by Mel using NO scavenger (cPTIO) was affirmed. It was observed that the effect of Mel-induced Pb toxicity tolerance was totally eliminated in presence of cPTIO by inhibiting the NO. It was confirmed that Mel acts as an upstream signalling molecule to NO in conferring Pb toxicity tolerance in tested plants. Hydrogen sulphide has also been applied in diverse cop plants to alleviate the harmful effects of metal/s. Kaya et al. (2018) applied H2S to regulate the level of metabolites and antioxidants to palliate the Zn-induced oxidative stress in Capsicum annuum L. plants in a factorial experiment. The two Zn levels (0.05 and 0.5 mM) and 0.2 mM H2S in the form of sodium hydrosulfide (NaHS) was applied through the roots. It was found that Zn levels caused significant reductions in plant dry mass, chlorophyll pigments, fruit yield, chlorophyll fluorescence, and RWC, but boosted EL, H2O2, proline, MDA, endogenous H2S, and activities of CAT, POD, and SOD enzyme activities. The high Zn-exposed plants increased endogenous Zn content in the leaves and roots of tested plants, but lowered the leaf N, P, and Fe contents. The application of NaHS enhanced plant growth, fruit yield, water status, H2S level, proline and antioxidant enzyme activities, but significantly lowered down the EL, MDA, and H2O2 levels under low Zn grown plants. The NaHS application also reduced the Zn levels and enhanced root and leaf Fe and N contents in pepper plants. In Arabidopsis thaliana ecotypes, Jia et  al. (2016) worked out the role of H2S-­ cysteine (Cys) cycle system under Cd-induced oxidative stress. It was observed that within 3  h of Cd2+ exposure, the expression of synthetic genes of H2S-LCD and DES1 and Cys synthesis-related genes SAT1 and OASA1 were induced. The H2S inhibited the ROS burst by inducing alternative respiration capacity (AP) and

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antioxidase activity and induced the expression of metallothionein (MTs) genes. In turn, Cys promoted accumulation of gluthathione (GSH) and inhibited the excess ROS. The study got further confirmation when lcddes1-1 and oasa1 mutants were used in which the Cd2+ tolerance ability was found to be weakened when the cycle system was blocked. In Medicago sativa, Cui et al. (2014) found that production of H2S by Cd is engaged in alleviation of Cd-toxicity by re-establishing the redox state of GSH and ROS detoxification. Singh et  al. (2015) in a hydroponic experiment applied H2S (in the form of NaHS) and found that it alleviates the toxic effects of As-stress in pea seedlings via the up-regulation of the ascorbate–glutathione (AsA-­ GSH) cycle via-a-vis crosstalk with NO.  The decrement in growth, chlorophyll fluorescence and contents of H2S and N, the activities of cysteine desulfhydrase and nitrate reductase and NO and the enzymes of AsA-GSH was observed under As stress. The NaHS addition ameliorated As toxicity by increasing the contents of H2S and NO, reducing the content of ROS and by the conspicuous increment in AsA-­ GSH cycle. In yet another study, Alsahli et al. (2021) applied H2S donor, i.e., NaHS (200  μM) under 20  μM sodium arsenite (NaAsO2) in Pisum sativum L. plants. Moreover, in order to find out the role of endogenously synthesized H2S, its scavenger hypotaurine (HT) was used. As causes significant decrease in root length, shoot length, dry biomass, photosynthetic pigments and gas exchange characteristics, but increased AsA, GSH and methylglyoxal (MG) levels and As content in roots and shoot tissues, H2O2, MDA and EL. The supplementation of H2S to As-stresses plants significantly decreased accumulation of As in root and shoot tissues, H2O2, MDA and EL, and accelerated the activities of antioxidants and also the AsA-GSH cycle. In a recent study, Zhu et al. (2022) unearthed the alleviatory underlying mechanisms of H2S pre-treatment (2 μM applied as H2S donor NaHS) under Al toxicity (30 μM Al as AlCl3·6H2O) in rice. The 30 μM Al-stress significantly inhibited root growth but increased the Al content in apoplasm and cytoplasm. The pre-treatment H2S donor reversed the Al induced negative effects by significantly increasing the energy production, contents of ATP as well as non-structural carbohydrates, reducing the stress ethylene levels, stimulation of the AsA-GSH cycle and regained the Al-inhibited pectin synthesis and increased the pectin methylation degree. The positive effect of H2S was also ascribed to the tolerance trade-off of H2S with PGRs like indole-3-acetic and brassinolide. In yet another recent study, the putative role of H2S and mechanism(s) lying behind the amelioration of hexavalent chromium (Cr(VI) toxicity in wheat and rice seedlings were unearthed by studying the nutrient assimilation and role of AsA-GSH cycle (Kumar et  al. 2022). The Cr toxicity reduced length of wheat and rice seedlings, down-regulated the AsA-GSH cycle and increased the oxidation of proteins. This disturbed state was recovered by the application NaHS (a donor of H2S) which caused an enhancement in sulfur assimilation, AsA-SH cycle and reduced the protein oxidation. A pot study with three replicates in complete randomized design was performed in Ayub Agriculture Research Institute, Faisalabad Pakistan to study the effects of four (0, 10, 100, 200 μM) different levels of K2Cr2O7 and the possible ameliorative role of sodium hydrosulfide (200 μM; H2S donor) in cauliflower plants was studied (Ahmad et al. 2020). The Cr exposed plants exhibited reduced growth, biomass, chlorophylls content, gas

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exchange parameters, and enzymatic antioxidants but enhanced EL, H2O2, MDA and Cr contents in roots, stem, leaf, and flowers. Nevertheless, the supplement of H2S improved these physiological and biochemical attributes by decreasing the Cr contents in different parts, reducing the EL, H2O2, and MDA concentrations and enhancing the antioxidant enzymes activities in roots and leaves of tested plants. In barley, a two-factorial design with six replicates hydroponic experiment to examine the role of three (0 μM, 100 μM, and 200 μM) levels of H2S in alleviating Cr (0 μM and 100 μM) stress was explored (Ali et  al. 2013). The results showed that Cr-induced growth retardation was palliated by NaHS addition by enhancing the plant growth and photosynthesis. The higher levels of NaHS exhibited more pronounced effects in roots, shoots, and leaves. The Cr stress caused an increase in number of plastoglobuli, disintegration, and disappearance of thylakoid membranes and visualization of starch granules as revealed by ultrastructural examination. Moreover, the alleviation of cell disorders in root and leaf with H2S application were also indicated by ultrastructural examination of plant cells.

13.4 Melatonin and Hydrogen Sulphide: Ameliorating Role Under Salt Stress Salt stress is adversely affecting plant growth and development and causes considerable losses in yield of several important crop plants. The ions of salinity invoke osmotic, ionic and oxidative stress in plants (Fariduddin et al. 2019; Dawood et al. 2022). The plant salinity-stress tolerance mechanisms are complex, imparted by the interplay of various signalling compounds expressed in various morpho-­biochemical and physiological activities (Mangal et  al. 2022; Kumar et  al. 2022; Raza et  al. 2022). Excess amounts of salt-ions cause a state of oxidative stress by excess generation of various ROS, thus decreasing growth and yield of crop plants. Both Mel and H2S showed palliating role in lowering down the salt-induced negative changes in diverse crop plants. In the following compiled literature from doctorate thesis, scientific research journals and online literature, some relevant aspects on the role of Mel and H2S will be critically analysed. Li et al. (2017) in Citrullus lanatus L., applied Mel to confer salt stress tolerance. The watermelon seedlings at the three-­ leaf stage were given 0, 50, 150, or 500 μM Mel (80 mL per plant) for 6 days. The plants were irrigated with 300 mM NaCl (80 mL per plant). The NaCl stress significantly inhibited photosynthesis and increased accumulation of ROS and membrane damage in leaves of tested plant. Nonetheless, pre-treatment with Mel palliated the NaCl-induced oxidative stress and photosynthesis capacity inhibition in a dose-­ dependent manner. The Mel application prevented inhibition of stomatal closure and improved light energy absorption efficiency and electron transport rate in PSII on one hand and the reduction of NaCl-oxidative stress was attributed to the regained redox homeostasis along with boosted antioxidant enzymes. Ke et  al. (2018) in wheat ecotype Xinong 9871, supplemented 1  μM Mel to study the mitigative changes imposed by salt stress. The plants were grown under 100 mM NaCl stress

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for 16 days with three biological replicates. The Mel pre-treatment partially mitigated the salt-induced inhibitions as evidenced from improved shoot dry weight, IAA content, Pn, maximum photochemistry efficiency of PSII, and chlorophyll content. The Mel mediated mitigation was observed by its effect on lowering the H2O2 accumulation and increased the expression of TaSNAT transcript, which encodes a key enzyme in its biosynthetic pathway. Conclusively, Mel mediated functional crosstalk with polyamine was responsible for salt-stress mitigation in tested plants. Zhang et al. (2020) in cucumber plants showed the alleviative effects of exogenous Mel under salt stress. The results showed that under salt stress, Mel improved cell viability and photosynthesis, increased antioxidant enzyme activity, inhibited the explosion of active oxygen and reduced MDA content and relative conductivity. The study got further confirmation by gene expression analysis that showed under salt stress, Mel mediated increased expression of antioxidant enzyme gene, nicotinamide adenine dinucleotide phosphate (NADPH) oxidase genes, mitogen-­activated protein kinase (MAPK) genes (MAPK3, MAPK4, MAPK6) and salt overly sensitive (SOS) genes (SOS1, SOS2, SOS3). Moreover, the confirmed results about the biosynthesis of Mel in chloroplast responsible for protection of plants from salt-stress came from the efforts of Zheng et  al. (2017). Liang et  al. (2015) studied the involvement of Mel in delaying leaf senescence and improving salt stress resistance in rice seedlings in a hydroponic culture with three biological replicates. The Mel treatments significantly reduced chlorophyll degradation, suppressed the transcripts of senescence-associated genes, delayed the leaf senescence, and enhanced salt stress tolerance. It was found by genome-wide expression profiling by RNA that Mel acted as a free radical scavenging molecule that enhanced antioxidant protection. By using a leaf cell death in noe1, a mutant which overproduced H2O2, it was found that this mutant can be reversed by Mel exogenous application. Altaf et al. (2020) applied various concentrations of Mel (0, 1, 50, 100, 150, and 200 μM) for 12 days under irrigation with 150 mM NaCl stress with three replicates in tomato. It was found that the application of 100 μM Mel proved to be the best in compensating the growth inhibitory effects under salt-stress as an increased fresh and dry masses of shoots and roots, regained relative chlorophyll content (SPAD index), root characteristics, and leaf gas exchange was observed with minimized accumulation of ROS and improved activities of antioxidative enzymes in tomato plants. Yan et  al. (2021) exposed rice seedlings to study the salt-stress changes in the presence of Mel in improving leaf photosynthesis. The results showed that Mel increased RWC, sucrose and starch content, Pn, and boosted the capacity of absorption and transmission of light energy. The Mel under salt stress conditions maintained low ROS status, improved total antioxidant capacity, promoted the xanthophyll cycle and increased the xanthophyll pool and also the activities of key photosynthetic enzymes. Chen et  al. (2020) under salt stress (150  mM NaCl) in Gossypium hirsutum L. applied Mel (10, 20 and 50 μM) to promote the seed germination and osmotic regulation. The Mel content was the lowest at day 6, while the germination rate of cotton peaked at day 6. The salt stress increased EL, H2O2, MDA, organic solutes (proline and soluble sugars) and inorganic nutrients (Na+ and Cl−) but decreased the endogenous contents of Mel, soluble proteins, and K+ as well as

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the K+/Na+ balance and damaged cellular membranes. The Mel treatment alleviated the adverse effects of salt stress by reducing EL, contents of H2O2, MDA, Na+, and Cl− and promoted Mel, soluble sugar and proteins, proline, and K+ /Na+ contents under salt stress treatments. The 20 μM Mel treatment was found to be the most effective treatment in promoting seed germination and improving salt stress resistance in cotton plants. Thus, the collected literature clearly suggests that Mel exert a protective role under salt challenged environments.

13.5 Conclusion From the above collected literature, it in inferred that an appreciable progress has been made in understanding the underlying mechanisms on the role of Mel and H2S in countering drought, metal/metalloid and salt stress in various crop plants. An environmental stress has been found to generally increase the level of endogenous Mel and H2S, which is believed to play important roles in stress resistance. Moreover, the exogenous application of Mel and/or H2S ameliorates the deleterious effects of a stress. As multifunctional signalling factor, both Mel and/or H2S can regulate plant growth and stress resistance by modulating adaptive mechanisms in crop plants. A schematic chart to visually understand the mechanisms is given in Fig. 13.1.

, ht ug ro al/ s d lt, et oid Sa m tall e m

Receptors

Receptors

Receptors

Adaptive Mechanisms

Signal transduction Adaptive Mechanisms

Antioxidants

Endogenous Mel and H2S

ROS

Signalling Pathway s

Grow Photos th ynthe Minera sis ls

Receptors

Rece

ptors

Exogenous Melatonin/ hydrogen sulphide

Fig. 13.1  Overview of various plant stress responses to exogenous Mel and/or H2S treatment under stress conditions. Both Mel and/or H2S promote plant growth, regulate photosynthesis, maintain ion homeostasis, and alter the expression of stress-related genes

13  Eco-Physiological and Morphological Adaptive Mechanisms Induced by Melatonin… 259 Acknowledgments  The authors extend their appreciation to Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2022R188), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia. Funding  This research was funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2022R188), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

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Chapter 14

Melatonin in Plants Under UV Stress Conditions Antonio Cano, Josefa Hernández-Ruiz, and Marino B. Arnao

Abstract  Melatonin (N-acetyl-5-methoxytryptamine), an indolic molecule with interesting regulatory properties in plants, is being widely used lately for physiological and molecular studies. Germination, plant growth, photosynthesis, senescence, parthenocarpy, flowering, ripening, and metabolic pathways are some of the processes and topics where melatonin has presented interesting results. To highlight its role as a biostimulator and protector against different stressors, both abiotic and biotic, through regulating redox network, in this chapter, studies on the role of melatonin in plants subjected to UV radiation are summarized and analyzed with the aim of presenting a model or scheme on the UV-melatonin interaction. Keywords  Biostimulator · Melatonin · Phytomelatonin · Plant abiotic stress · UV-B radiation

Abbreviations ANS leucoanthocyanidin dioxygenase AOX alternative oxidase ASMT acetyl serotonin methyl transferase BES1 positive brassinosteroid-signaling transcription factor BIM1 positive brassinosteroid-signaling transcription factor BRs brassinosteroids CAT catalases CCA1 circadian clock associated1 Chls chlorophylls

A. Cano · J. Hernández-Ruiz · M. B. Arnao (*) Phytohormones & Plant Development Lab, Department of Plant Biology (Plant Physiology), Faculty of Biology, University of Murcia, Murcia, Spain e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_14

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chalcone synthase caffeoyl-O-methyl transferase E3 ubiquitin-protein ligase, repressor of photomorphogenesis COP1-SPA-DDB1-CUL4 E3 ubiquitin ligase complex CRY3 cryptochrome DASH (reparation of UV radiation-­ induced DNA damage) D11 cytochrome P450 (724B1) involved in BR biosynthesis D2 cytochrome P450 (90D2) involved in BR biosynthesis DFR dihydroflavonol 4-reductase DWARF4 cytochrome P450 (90B2) involved in BR biosynthesis ELIP1 early light-induced protein1 F3H flavanone 3-hydroxylase FLS flavonol synthase/flavanone 3-hydroxylase GPX glutathione peroxidase HY5 elongated hypocotyl5 HYH HY5 homolog LAR leucoanthocyanidin 4-reductase LHY late elongated hypocotyl MDA malondialdehyde MEL melatonin PAL phenylalanine ammonia-lyase PHR1 deoxyribodipyrimidine photo-lyase (reparation of UV radiation-induced DNA damage) PMTR1 phytomelatonin receptor1 POD peroxidases RAVL transcription factor involved in BR biosynthesis control RNS reactive nitrogen species ROS reactive oxygen species RUPs repressors of UV-B photomorphogenesis (rup1,2) SNAT serotonin N-acetyl transferase SOD superoxide dismutases SPA repressor of photomorphogenesis TOC1 timing of CAB expression1 UVR3 DNA photolyase (reparation of UV radiation-induced DNA damage) UVR8 UV-B receptor (UV RESISTANCE LOCUS8) WRKY36 transcription factor interacts specifically with the W box

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14.1 Plant Stress The development of plants is an adaptive process to the environment and subject to the multiple factors that determine it. Among them are abiotic and biotic factors as elements of great influence on the plant development. The sudden onset or continuous persistence of such factors in the plant environment can lead to stressful situations that require different responses by the plant (Kranner et  al. 2010; Shabala 2017; Hasanuzzaman et  al. 2020). Eustress and distress are two types of stress caused by plant stressors. Although most studies on stress in plants focus on responses to simple stress, in real situations, the environment subject’s plants to situations of multiple stress, generated by various stressors that synergize or antagonize their stressful action on the plants (Zandalinas and Mittler 2022). The term eustress refers to a mild or low intensity stress, which is usually beneficial for the plant, since it actives its defenses without suffering serious damage (Sies 2017; 2021). On the other hand, the term distress refers to situations of high stress or very persistent stress that usually provokes damage at the cellular level. In the case of distress, if the plant does not adequately activate its responses or they are overwhelmed by the stressor, then significant oxidative damage and degradation effects will appear, which if made irreversible will cause cell, tissue, or total death. The thresholds of eustress and distress are usually different for each plant according to its degree adaptive to the stressor. The jump from eustress to distress is usually established by the homeostatic capacity of the plant in the face of different stressors (Potters et al. 2009; 2010; Zhu 2016; Toyota et al. 2018).

14.2 Melatonin in Abiotic Stress The redox network is a powerful tool that plants use to control redox homeostasis in cells. This redox network is an antioxidant machinery made up of enzymatic elements such as superoxide dismutases, catalases, peroxidases, transferases, etc., and no-enzymatic, antioxidant metabolites such as ascorbate, glutathione, tocopherols, phenolic compounds, and others. All these elements, together with oxidative stress signaling and response factors, form a fundamental protective system for aerobic cells, where reactive oxygen species (ROS) and nitrogen (RNS) are usually generated in their metabolism. The control of ROS and RNS levels within the margins of eustress (redox homeostasis) is essential so that the cells do not enter into distress, causing damage to cellular elements such as proteins, lipids, and nucleic acids; therefore, the excess of ROS and RNS must be detoxified (Ahmad et  al. 2010; Sandalio and Romero-Puertas 2015; Zhu 2016; Nieves-Cordones et  al. 2019). Interestingly, some of the ROS and RNS can act as stress signals inducing gene expression, so their control by the redox network requires fine molecular adjustments (Mittler 2017; Fichman et al. 2019; Fichman and Mittler 2020; Devireddy et al. 2020). Also, different biological processes related to cellular differentiation,

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Fig. 14.1  Relationship of the triad: core biological clock, phytomelatonin and redox network (Arnao and Hernández-Ruiz 2020). CCA1, circadian clock associated1; LHY, late elongated hypocotyl; PMTR1, phytomelatonin receptor1; RNS, reactive nitrogen species; ROS, reactive oxygen species; TOC1, timing of CAB expression1

growth, and immune/pathogen responses are also attributed to ROS-induced redox signaling (Dangl and Jones 2001; Decros et al. 2019; Hasanuzzaman et al. 2020). Melatonin (N-acetyl-5-methoxytryptamine) is a universal component of biological systems that presents interesting antioxidative and regulatory properties (Arnao and Hernández-Ruiz 2015). In plants, melatonin, called phytomelatonin, is considered a new phytohormone with a primary role in the response to stressful situations (Arnao and Hernández-Ruiz 2014; 2019b). Melatonin controls the redox network by regulating the antioxidative response of enzymes and antioxidants, through the biosynthesis of ROS and RNS and their inactivation. In addition, melatonin controls the responses of other plant hormones to stress, all coordinated with the rhythmic-­ circadian responses of its biosynthesis enzymes and its PMTR1 receptor (see Fig.  14.1) (Arnao and Hernández-Ruiz 2020). Also, melatonin is involved in the responses to different stressors both abiotic (drought, high and low temperatures, salinity, alkalinity, radiation, chemical contaminants, etc.) and biotic (bacteria, fungi and viruses), regulating the different transcription factors and specific response elements such as dehydrins, SOS-transporters, heat-shock proteins, cold-responsive factors, phytochelatins, etc. (Arnao and Hernández-Ruiz 2019a; c; Buttar et  al. 2020; Moustafa-Farag et al. 2020a, b, c; Altaf et al. 2021; Arnao and Hernández-­ Ruiz 2022; Menhas et al. 2022).

14.3 Melatonin in UV Stress In natural environments, the plants receive, in addition to the radiation necessary for photosynthesis, other photonic stimuli, including UV radiation. UV radiation is divided into three wavelength ranges: UV-A (315–400 nm), UV-B (280–315 nm) and UV-C (100–280  nm). UV-C, the most energetic of the three, is completely

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absorbed by the ozone layer. UV-A is not attenuated by ozone, but it is the least damaging and would act as a photomorphogenic signal. About 5% of UV-B radiation reaches the Earth’s surface and, depending on the quantity, can act as a plant stressor, provoking important damage in proteins, lipids, and nucleic acids, leading to the accumulation of ROS (Björn 2015). Terrestrial plants have developed throughout evolution a set of acclimatization strategies to the UV-B radiation inherent in the environment, both to avoid excess UV-B radiation and to minimize the negative consequences of inevitable exposure. Because the incidence of UV-B radiation in plants implies oxidative stress (Hideg et al. 2013; Yao et al. 2015), in recent years some works applying melatonin have appeared, which are presented in Table 14.1. Table 14.1  Different studies of UV radiation and melatonin effects on several plant species and culture cells UV radiation UV-B

UV-B

UV-B

Plant specie Glycyrrhiza uralensis Chinese liquorice roots Nicotiana sylvestris Tobacco transgenic plants Malus halupensis Apple plants

UV-B

Malus halupensis Transgenic apple plants

UV-B

Arabidopsis thaliana

Melatonin treatment Observed effects – ↑ UV-B tolerance ↑ melatonin accumulation Ectopic overproduction

↑ UV-B tolerance ↑ melatonin accumulation ↓ DNA damage (tail-DNA)

↑ UV-B tolerance ↑ plant growth, ↑ Chls, photosynthesis, stomatic exchange ↑ flavonoids, phenolic acids, antioxidants ↑ melatonin biosynthesis enzymes ↓ ROS, MDA ↑ UV-B tolerance Ectopic overproduction ↑ photosynthesis, stomatal density, leaf area ↑ flavonoids, phenolic acids ↑ melatonin biosynthesis ↓ ROS, MDA 100 μM and ectopic ↑ UV-B tolerance overproduction ↑ hypocotyl growth ↑ melatonin biosynthesis transcripts ↑ antioxidative enzymes ↑↓ UV-B-signaling elements (UVR8, COP1, HY5, HYH, RUP1, RUP2) ↑ UV-B-induced DNA repair transcripts (CRY3, PHR1) ↓ ROS, MDA 1 μM

Reference Afreen et al. (2006)

Zhang et al. (2012)

Wei et al. (2019)

Liu et al. (2021)

Yao et al. (2021)

(continued)

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Table 14.1 (continued) UV radiation UV-B

UV-C

UV-C

Plant specie Arabidopsis thaliana

Lepidium sativum Gardencress calli Ocimum basilicum Purple basil calli

Melatonin treatment Observed effects 10 μM ↑ UV-B tolerance ↑ photosynthesis ↑ redox protection (GPX2,7) ↑ UV-B absorbing compounds ↓ MDA, oxidative stress ↓ alternative oxidases (AOX) 20 μM ↑ UV-C tolerance ↑ accumulation of flavonoids, antioxidants, and antidiabetic metabolites 0.1–5 mg/L ↑ flavonoids, phenolic acids ↑ antioxidant activity ↓ ROS, RNS, oxidative stress

Reference Haskirli et al. (2021)

Ullah et al. (2019)

Nazir et al. (2020)

Glycyrrhiza uralensis studies were the first in which a relationship between the phytomelatonin content in roots and UV-B treatments was observed, multiplying 5-times the endogenous levels of phytomelatonin. A proposal for phytomelatonin as a protective molecule against UV-B was postulated (Afreen et al. 2006). The use of plants genetically transformed with ectopic enzymes for the melatonin biosynthesis has allowed great advances (Arnao and Hernández-Ruiz 2018). Thus, ectopic woodland tobacco plants over-producing melatonin had a greater tolerance to UV-B radiation and less damage to their DNA, measured through tail-­ DNA, demonstrating the protective role of phytomelatonin (Zhang et al. 2012). Also using ectopic expression, melatonin-overproducing apple plants had a greater tolerance to UV-B, improving their photosynthetic parameters and the content of protective phenolic compounds, which had an impact on lower levels of ROS and membrane lipid peroxidation compared to unmodified plants with low levels of melatonin (Wei et al. 2019; Liu et al. 2021). Also, UV-B promoted the generation of pheophorbide-a oxygenase, a chlorophyll-degrading enzyme, and melatonin repressed it, resulting in a higher content of active chlorophylls. Both UV-B radiation and melatonin treatments upregulated enzyme transcripts of the biosynthetic pathways of phenolic acids, flavonoids, and anthocyanins such as CHS, F3H, ANS, UFGT, LAR and FLS (Wei et al. 2019; Arnao et al. 2022). Also, UV-B increases color and nutritional quality in several fruits and herbs, and is also applied in post-­ harvest to prevent plant diseases (Hideg et al. 2013; Mditshwa et al. 2017; Tohge et al. 2017; Yadav et al. 2020; Apoorva et al. 2021; Sen et al. 2021; Yoon et al. 2021; Takeda 2021; Meyer et  al. 2021; Ferreyra et  al. 2021; Mandal et  al. 2022; Yin et al. 2022). The discovery of the UV-B photoreceptor, UVR8 (UV RESISTANCE LOCUS8), from a mutant of Arabidopsis thaliana with a low flavonoid content, and therefore hypersensitive to UV-B radiation has allowed important advances in this field (Kliebenstein et al. 2002; Tossi et al. 2019; Takeda 2021). In an interesting work in

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A. thaliana, melatonin regulated UV-B signaling and changed gene expression, affecting to antioxidant network in response to UV-B exposure, improving tolerance. Using several mutant plants, the authors demonstrated that exogenous melatonin, also in ectopic melatonin-overproducing transgenic plants, up−/downregulated several key elements of UV-B signaling such as COP1, HY5, HYH and RUPs. Three genes of the melatonin biosynthesis pathway (SNAT, COMT and ASMT) showed increased expression relative to control following UV-B treatment. Also, endogenous melatonin content had a peak after to UV-B treatment. In addition, an overexpression cell line of SNAT improved UV-B stress resistance and reduced DNA damage and lipid peroxidation by ROS.  Finally, the expression of genes involved in DNA repair (CRY3 and PHR1) was anticipated in melatonin treatments, indicating a preparation of cellular defenses to UV-B damage (Yao et al. 2021). Also in Arabidopsis, 10 μM melatonin treatments improved redox protection through the upregulation of glutathione peroxidases (GPX) and UV-B absorbing compounds (possibly flavonoids), all by reducing oxidative stress and improving tolerance to UV-B radiation (Haskirli et al. 2021). Also, in the in vitro cell cultures of some plant species, UV-C treatments together with melatonin have been used to induce the biosynthesis of interesting secondary metabolites (Table  14.1). In general, several strategies using UV radiation, and other abiotic stressors, for the intensification of interesting metabolite production have been applied (Espinosa-Leal et  al. 2022). As an example, gardencress (Lepidium sativum) is an edible Brassicaceae with interesting therapeutic properties in lung dysfunctions, such as cough, asthma, and bronchitis, confirming its potential applications as a bronchodilator and antirheumatic; also, in hemorrhoids, leucorrhea, diarrhea, scurvy, and skin illness, among others. Its pharmaceutical possibilities are due to being a plant material rich in phytochemicals, such as phenolics, flavonoids, terpenoids and carotenoids, which have therapeutic potential to protect cells from oxidative stress that is the causative agent of some of the main metabolic diseases (Diwakar et al. 2008; Rehman et al. 2012; Attia et al. 2019; Ahmad et al. 2021; Painuli et al. 2022). Calli of L. sativum treated with UV-C radiation for different time intervals and various concentrations of melatonin showed several secondary metabolites were enhanced versus untreated material. Also, antioxidant, antidiabetic, and enzymatic activities of callus cultures were significantly enhanced, with maximum antidiabetic activities (57% α-glucosidase and 62% α-amylase) recorded in 20 μM melatonin treatment. The authors proposed that melatonin can be an excellent elicitor to improve yield plant cell cultures (Ullah et al. 2019). We can find multiple examples of the elicitor capacity of melatonin in cell culture for various secondary metabolites (Arnao et al. 2022). In callus cultures of purple basil (Ocimum basilicum L. var purpurascens), melatonin and UV-C treatments (either alone or in combination, although individual melatonin treatments were more effective), showed that rosmarinic acid, chichoric acid, and the anthocyanins, cyanidin and peonidin were accumulated in higher degree than in the control callus. Antioxidant activity was also enhanced with UV-C and melatonin treatments, demonstrating that these elicitors were very effective in the polyphenol biosynthesis promotion in plant cell culture (Nazir et al. 2020).

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In general, melatonin exerts a protective effect against UV radiation, minimizing morphological and metabolic damage and increasing growth and photosynthetic rates. Moreover, it also enhances the presence of diverse phenols such as phenolic acids, flavonoids, and anthocyanins, which help in the protective effect against UV radiation (Arnao et  al. 2022). Although molecular data on this are very few, the action of melatonin could be mediated by several photomorphogenic transcription factors that determine the response to UV-B. Thus, taking the studies of Yao et al. (2021) in A. thaliana, we can propose a general model of interaction between melatonin and UV-B radiation (Fig. 14.2). UVR8 (UV RESISTANCE LOCUS 8) protein, localized in both the cytoplasm and the nucleus, regulates UV-B signal transduction and tolerance (Kliebenstein et al. 2002). UVR8 regulates its own signaling elements and also regulates the biosynthesis of anthocyanin and brassinosteroid response elements, among others (Tossi et al. 2019; Takeda 2021) (Fig. 14.2). UV-B radiation changes UVR8 quaternary structure from dimeric to active monomeric, inducing the nuclear accumulation of UVR8, where it is functional (Rizzini et al. 2011; Christie et al. 2012). In presence of UV-B radiation, the UVR8 monomer interacts with COP1, that uncouples COP1-SPA from the E3 ubiquitin ligase

Fig. 14.2  Proposed model of melatonin action in UV-B responses. ASMT, acetyl serotonin methyl transferase; BES1, positive brassinosteroid-signaling transcription factor; BIM1, positive brassinosteroid-­signaling transcription factor; BR, brassinosteroids; COMT, caffeoyl-O-methyl transferase; COP1, E3 ubiquitin-protein ligase (repressor of photomorphogenesis); COP1-SPA-­ DDB1-CUL4, E3 ubiquitin ligase complex; D11, cytochrome P450 (724B1) involved in BR biosynthesis; DFR, dihydroflavonol 4-reductase; DWARF4, cytochrome P450 (90B2) involved in BR biosynthesis; ELIP1, early light-induced protein1; F3H, flavanone 3-hydroxylase; FLS, flavonol synthase/flavanone 3-hydroxylase; HY5, elongated hypocotyl5; HYH, HY5 homolog; LAR, leucoanthocyanidin 4-reductase; MEL, melatonin; PAL, phenylalanine ammonia-lyase; RAVL, transcription factor involved in BR biosynthesis control; RUPs, repressors of UV-B photomorphogenesis (rup1,2); SNAT, serotonin N-acetyl transferase; SPA, repressor of photomorphogenesis; UV-B, ultraviolet B radiation; UVR3, DNA photolyase (reparation of UV radiation-induced DNA damage); UVR8, UV-B receptor (UV RESISTANCE LOCUS8); WRKY36, transcription factor interacts specifically with the W box

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complex (COP1-SPA-DDB1-CUL4), avoiding ubiquitination and subsequent degradation of the transcriptional factors HY5 and HYH (Lau and Deng 2012; Huang et al. 2014). The UVR8-COP1-SPA complex is transported to nucleus, stabilizing HY5/HYH which induces several UV-B responsive genes, including its own expression, COP1 and RUPs genes. The latter encoding for RUP proteins that regulate by negative feedback the formation of UVR8-COP1-SPA complex, binding to UVR8 and promoting its re-dimerization (Brown et  al. 2005; Favory et  al. 2009; Cloix et al. 2012; Heijde and Ulm 2013; Binkert et al. 2014). In photoperiodical conditions, UVR8 reaches a dimer/monomer equilibrium in which RUP protein action is crucial (Findlay and Jenkins 2016). Other proteins also regulate the action and level of UVR8 and its interactions with the E3 ubiquitin ligase complex (Tossi et  al. 2019). HY5/HYH are blocked by the transcription factor WRKY36, which can interact with the UVR8 monomer, allowing the action of HY5/HYH (Yang et al. 2018). On the other hand, UVR8 monomer is capable of interacting with BES1 and BIM1 elements. BES1/BIM1 are brassinosteroid response factors that induce the growth of hypocotyls, so the response to UV-B radiation results in an inhibition of plant growth (Yin et al. 2005; Vert and Chory 2006; Belkhadir and Jaillais 2015; Liang et al. 2018). Melatonin level was increased in UV-B treatments through the upregulation of biosynthesis enzyme transcripts SNAT, ASMT and COMT. Also, UV-B treatments provoked relevant increased in oxidative markers such as ROS and MDA. Melatonin and UV-B co-treatments enhanced antioxidative defenses such as SOD, CAT, POD, decreasing oxidative stress (Yao et  al. 2021). Melatonin improved the action of COP1, either favoring the formation of URV8-COP1-SPA complex and/or its input and stability in the nucleus, making the action of HY5/HYH more efficient. In addition, melatonin seems to delay the appearance of the RUP inhibitors, getting more URV8 protein in its monomeric form (Fig. 14.2). Studies with transgenic Arabidopsis plants that overproduced or decreased their endogenous melatonin levels indicated that a higher level of expression of melatonin biosynthesis correlated with a greater effectivity of HY5/HYH, and vice versa; for example in snat mutants, where low melatonin levels correlated with low expression of URV8 signaling elements (Yao et al. 2021). In darkness, melatonin at very low concentrations was able to activate the growth of diverse seedlings (Hernández-Ruiz et al. 2004; Hernández-Ruiz et al. 2005). The growth-inhibiting action of UV-B radiation is clearly related to one of the most novel roles attributed to melatonin, its action as a regulatory hormone for skotomorphogenesis. The rice SNAT2 RNAi lines exhibited a dwarf phenotype with erect leaves reminiscent of brassinosteroid-deficient phenotype, indicating that melatonin takes part in determining BR levels in plants. In darkness, exogenous melatonin treatment induced the transcription factor RAVL1 and several BR biosynthetic genes, including DWARF4, D2 and, D11 (Hwang and Back 2018). This melatonin-­ mediated dark growth response is opposite to that of UV-B radiation, where the induction of hypocotyl growth mediated by melatonin was affected in the mutant arabidopsis cop1 under UV-B conditions (Yao et al. 2021), suggesting COP1 might

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be a signaling component of phytomelatonin in hypocotyl growth (Tossi et al. 2019; Chen et al. 2022) (Fig. 14.2).

14.4 Concluding Remarks Melatonin is a widely applied molecule in order to increase the tolerance of plants to abiotic stressors. Although it is known that UV-B radiation induces melatonin biosynthesis in plants, studies on tolerance to UV radiation and melatonin are very scarce, so there is a wide lack of knowledge in many aspects. However, some conclusions can be drawn from the current data: 1. Melatonin increases tolerance to UV-B radiation thanks to the activation of its biosynthesis in treated tissues. 2. Melatonin activates the defense mechanisms through the redox network, controlling oxidative stress in the eustress zone. 3. Melatonin counteracts the harmful effects of UV-B radiation on growth and photosynthesis, both physiologically and morphologically. 4. Melatonin, together with UV-B, increases the biosynthesis of phenolic compounds, especially simple phenols, flavonoids, and anthocyanins, which protect the plant from UV radiation. 5. Quite a few elements of the co-acting mechanism of melatonin and UVR8 are known, working in the regulation of UVR8 signaling elements through COP1, such as anthocyanin biosynthesis, and brassinosteroid responses. 6. Melatonin and UV-C radiation have been used to optimize yields in the biosynthesis of interesting secondary metabolites using plant cell cultures. Acknowledgements  This work has been supported by the grant PID2020-113029RB-I00 from Ministerio de Ciencia e Innovación/ Agencia Estatal de Investigación (MCIN/AEI/ 10.13039/501100011033), Spain.

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Chapter 15

Molecular Physiology of Melatonin Induced Temperature Stress Tolerance in Plants Suman Sharma and Siddhant Pandey

Abstract  Plants being immobile are exposed to several abiotic stress in nature out of which temperature is the most significant one. Temperature stress affects many growth and development processes in plants like nutrient and water uptake, organization of cellular membranes, seed germination, pollen viability, photosynthesis, leaf senescence, starch metabolism, biomass production and root growth. Understanding the molecular and biochemical mechanism of abiotic stress tolerance in plants is of great concern as it can contribute significantly to enhancing plant productivity. Recently a lot of data has been accumulated on the regulation of temperature stress in plants by melatonin. Melatonin is an indoleamine-based signaling molecule present ubiquitously in plants, showing pleiotropic responses. It possesses antioxidant properties which are highly beneficial in stress tolerance. Melatonin can regulates stress responses in plants either directly by inhibiting the accumulation of reactive nitrogen and oxygen species or indirectly by inducing alterations in the stress response pathways. In this chapter we have reviewed the mechanism of melatonin–mediated temperature stress tolerance in plants by understanding its biosynthesis, signaling pathways, the role of endo and exogenous melatonin in regulating the inhibitory effects of heat and cold stress, melatonin interplay with other phytohormones and signaling molecules, up and down-regulation of temperature stress-­ related genes in presence of melatonin. Keywords  Abiotic stress · Indoleamine · Melatonin · Signaling molecule · Antioxidant · Reactive oxygen

S. Sharma (*) · S. Pandey Department of Botany, Ramjas College, University of Delhi, Delhi, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_15

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Abbreviations ASMT N-acetyl-serotonin methyltransferase MAPK Mitogen-activated protein kinase MT Melatonin NO Nitric oxide ROS Reactive oxygen species SA Salicylic acid SNAT Serotonin N-acetyltransferase T5H Tryptamine 5-hydroxylase TDC Tryptophan decarboxylase TPH Tryptophan 5-hydroxylase

15.1 Introduction Melatonin (N -acetyl 5 methoxy tryptamine) is a natural signaling molecule that regulates several physiological responses in diverse organism including plants, animals and humans as well (Arnao 2014; Erland et  al. 2015). Melatonin was first isolated from pineal gland of bovine in the year 1958 (Lerner et al. 1958) and was named so due to its ability to lighten skin pigmentation in animals and humans. Earlier it was known to be present only in animals but later it was also identified in many lower as well as higher plants like unicellular dinoflagellate Lingulodinium polyedrum (syn. Gonyaulux polyedra) (Balzer and Hardeland 1991) ivy morning glory (Pharbitis nil L. syn. Ipomoea nil L.) fruits of Solanum lycopersicum (Van Tassel and O’Neill 1993; van Tassel et al. 1995) in Chenopodium rubrum (Kolář et al. 2003) Nicotiana tabacum (Dubbels et al. 1995; Hattori et al. 1995). At present melatonin is reported in more than 300 plant species most of which are angiosperm (Paredes et al. 2009; Simlat et al. 2018; Yan et al. 2020). Melatonin is ubiquitously present in almost all plant tissues including stem, leaves, roots, flowers, fruits, seeds, and bulbs (Nawaz et al. 2016) but its concentration varies in different parts of a plant, usually a relatively high levels is maintained in leaves and seeds in contrast to a low level in fruits (Arnao 2014). Several factors like the genotype of a plant, temperature, photoperiod and developmental stage of a plant determine the endogenous concentration of melatonin. The endogenous level of melatonin is also enhanced significantly upon being exposed to biotic and abiotic stress (Reiter et al. 2015). The primary site for melatonin production is located in usually in chloroplasts, mitochondria of root and leaf tissue and from their it is then transported to the meristem, flowers and fruits of plants (Wang et al. 2016). Melatonin is known to have strong antioxidant properties (Tan et al. 2015) and also scavenges free radicals like reactive oxygen (ROS) and nitrogen species (RNS) generated by several metabolic processes occurring in plants. Melatonin plays a significant role in protecting plants from various abiotic and biotic stresses (Mukherjee et al. 2014; Bajwa et al. 2014; Lei et al. 2004; Arnao 2014; Shi et al.

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2015b; Pelagio-Flores et al. 2016). These factors stimulates accumulation of melatonin in the endogenous tissues of plants which thus evoking genetic responses by activating or de- repressing the stress related transcription factors and antioxidant genes.

15.2 Biosynthesis of Melatonin Melatonin biosynthesis in plants occur mainly in roots through a common biosynthetic pathway functioning in chloroplasts and mitochondria (Tan et al. 2013). The biosynthesis of melatonin is regulated by various plant growth and developmentrelated process (Van Tassel et al. 2001; Okazaki and Ezura 2009; Shi et al. 2015a, b, c, d, e, f) and a few environmental factors (Afreen et al. 2006; Arnao and HernándezRuiz 2013; Byeon and Back 2014). In the majority of plant species, tryptophan acts as a precursor for the biosynthesis of melatonin and is converted to tryptamine by the enzyme tryptophan decarboxylase (TDC). Tryptamine is further converted to serotonin by tryptamine 5-hydroxylase (T5H) and finally to converted to melatonin through a two-step process. In an alternate pathway as observed in Hypericum perforatum, tryptophan is first catalyzed into 5-hydroxytryptophan by an enzyme tryptophan 5-hydroxylase (TPH), followed by its conversion to serotonin by enzymes TDC or AADC (aromatic-L-­amino-acid decarboxylase) (Murch et al. 2000). The serotonin is then converted to N-acetyl-serotonin by the enzyme serotonin N-acetyltransferase (SNAT) or arylalkylamine N-acetyltransferase (AANAT). Finally, N-acetyl-serotonin is converted into melatonin by either N-acetyl-serotonin methyltransferase (ASMT) or hydroxyindole-­ O-methyltransferase (HIOMT). However, sometimes tryptamine can be converted into N-acetyl-tryptamine, a reaction catalysed by SNAT, but the pathway to convert N-acetyl-tryptamine into N-acetyl-serotonin is not known (Fig.  15.1). In yet another pathway serotonin is converted into 5-methoxy-­tryptamine by HIOMT and, finally to melatonin by SNAT (Tan et al. 2016; Choi et al. 2017) (Fig. 15.1).

15.3 Signaling of Melatonin in Plants Under Stress Melatonin plays a significant role in the metabolism of ROS and the upregulation of antioxidants, which induces stress resistance properties in plants (Zhang et al. 2015; Sun et  al. 2015). Candidate-protein-coupled receptor 2/phytomelatonin receptor 1(CAND2/PMTR1), the first putative receptor protein for melatonin was identified in A. thaliana. It has seven transmembrane helixes located on the plasma membrane, where they directly bind to melatonin and regulates stomatal closure by activating Ca+2 channels and enhancing the Ca+2 and K+ influx. (Wei et al. 2018; Wen et  al. 2016). Unlike other phytohormones, melatonin can also act as a signaling molecule under stress by regulating the transcription of stress-responsive genes and

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Fig. 15.1  Possible pathways of Melatonin (MT) biosynthesis. The enzymes participating are: Tryptophan decarboxylase (TDC), Tryptophan hydroxylase (TPH), Tryptamine 5-hydroxylase (T5H), Serotonin N-acetyltransferase (SNAT), N-acetylserotonin methyltransferase (ASMT), and caffeic acid O-methyltransferase (COMT), Hydroxyindole-O-methyltransferase (HIOMT), N-acetylserotonin deacetylase (ASDAC), Aralkylamine N-acetyltransferase (AANAT), Aromatic l-amino acid decarboxylase (AADC)

developing crosstalk between other signaling pathways (Arnao and Hernández-­ Ruiz 2015; Shi et al. 2015a, b, c, d, e, f; Zhang et al. 2015; Sun et al. 2015). Four transcription factors have been identified in A. thaliana to show melatonin-mediated stress response, Zinc Finger Protein 6 (ZAT6), which regulates melatonin-mediated low temperature stress response, Auxin Resistant 3 (AXR3)/IAA inducible 17, regulates leaf senescence, class A1 Heat Shock Factors, which show melatonin-­ mediated high temperature tolerance and C-repeat-Binding Factors (CBFs)/Drought Response Element Binding 1 factors (DREB1s), which is involved melatonin – mediated stress response by accumulating high sugar levels (Mir et  al. 2020). Exogenous melatonin treatment in plants provide immunity against bacterial pathogens via SA –NO mediated pathways due to increase in endogenous levels of nitric oxide (NO) (Qian et al. 2015; Shi et al. 2016). Furthermore, Lee and Back (2016)

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reported that melatonin also establishes innate immunity in plants via mitogen-­ activated protein kinase (MAPK) signaling cascades.

15.4 Temperature-Mediated Abiotic Stress Among all other abiotic stress factors, temperature is one of the most significant factors as it affect almost all aspects of growth, development and productivity in plants (Palit et al. 2020). Production of reactive oxygen species increases in plant on being exposed to environmental stress and these are required for signal transduction during biotic and abiotic stress (Sewelam et al. 2016). The temperature stress can disrupt the cellular redox status, thus leading to decreased biomass production and hence the cell death (Czarnocka and Karpiński 2018).

15.4.1 Melatonin Role in Cold (Chilling) Stress Cold stress can effectively reduce the growth and productivity of plants via ROS-­ mediated redox imbalance. Under extremely low temperatures, plants accumulate melatonin to protect them against fatal injuries. Tolerance to cold stress can be improved in plants by enhancing the endogenous level of melatonin which can be achieved by regulating melatonin biosynthesis genes for example rice plants with SNAT transgene are less sensitive to cold stress than their wild counterparts (Kang 2011). The quality of fruits and vegetables can be effectively managed under cold storage through exogenous treatment with melatonin. Pre-treatment with melatonin can reduces the amount of lignin and increases the accumulation of phenolic compounds in loquat fruit, thereby enhancing the flavour and nutrition qualities that are otherwise compromised in cold storage (Wang et  al. 2021). In cut flowers upon treatment with melatonin, the concentration of H2O2 decreases while the scavenging capacity of 2,2-diphenyl-1- picrylhydrazyl (DPPH) is enhanced significantly in comparison to untreated flowers helping them to increase their shelf life (Aghdam et al. 2019). In bermuda grass, the exogenous application of melatonin can improve the concentration of certain primary and secondary metabolites like carbohydrates, amino acids, organic acids, thereby enhancing cold tolerance (Hu et al. 2016). Some metabolites of melatonin like 2-hydroxymelatonin, may also enhance tolerance to cold stress in plants like tomato, tobacco and cucumber (Lee and Back 2019). Exogenous application of melatonin can also minimize the extent of cold induced damage by activating antioxidant enzymes which inhibiting degradation of chlorophyll pigments and also by reducing the accumulation of ROS and peroxidation of lipids (Hu et al. 2016; Wang et al. 2017). In tomato, response to chilling stress is enhanced via arginine-dependent NO accumulation following melatonin treatment. Lei et al. (2004) observed in carrots the exogenous application of melatonin at a very low concentration could stabilize the cell membrane structure and hence improve cell viability by inhibiting the degradation of DNA through apoptosis.

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Cold-induced decrease in photosynthetic yield can be enhanced by the exogenous application of melatonin in plants (Ding et al. 2017; Liu et al. 2019). Germination of cucumber seeds under cold stress is directly related to an increase in endogenous melatonin concentration (Posmyk et al. 2009a, b). Germinating cucumber seedlings are highly sensitive to oxidative stress caused by extremely low temperatures. Pre-­ treating the seeds with melatonin results in H2O2 scavenging and also increases the GSH/GSSG ratio which helps the seedling to tolerate chilling stress. The activity of glutathione reductase (GR) is found to be two-fold higher in the melatonin-treated seeds in comparison to the non-treated ones. It indicates that a high and effective GSH pool is created in the melatonin pre- treated seeds which helps them to tolerate cold stress. In wheat, it has been observed that both the seed pre-soaking as well as treatment of the parents with melatonin can effectively enhance seed germination, seedling establishment and improved tolerance under low-temperature stress. Both methods resulted in a high seed germination rate, enhanced antioxidant properties and increased degradation of starch under low temperatures (Zhang et  al. 2021). Similar observations were also made by Cao et al. (2019) in waxy maize seed germination when they are primed with different concentrations of melatonin before being exposed to chilling stress. Pre-treatment with melatonin can minimize the severe injury of cryopreserved callus and ensure a hundred percent germination in dormant shoot tips or winter buds (Zhao et  al. 2011a, b; Uchendu et  al. 2013). Cold stress can cause several physiological as well as morphological changes in plants like reduction in leaf area, decreased water content and photosynthetic pigments in the leaf, and peroxidation of membrane lipids in wheat seedlings. Twelve-hour induction of such cold stressed wheat seedlings with 1 mM melatonin resulted in enhanced activity of ascorbate peroxidase, glutathione reductase, superoxide dismutase and antioxidant enzymes which overcome oxidative stress and enhance plant growth. Some metabolites like sugar, organic acids, amino acid and alcohol also increase in plants on exogenous application of melatonin (Vigentini et al. 2015). Melatonin-induced accumulation of methyl jasmonate and H2O2 in the grafted rootstock of watermelon and other horticultural crops helps them to overcome cold stress (Li et al. 2021). A study done in Citrullus lanatus L. by Li et al. (2017), revealed that exogenous melatonin can induce cold tolerance in the plant through long-distance signaling. Melatonin applied on roots or shoots of the plant not only induces cold tolerance at the site where it is applied rather it can systemically induce tolerance to cold tress even in the distantly located untreated parts of the plant. This long-distance signaling is the result of enhanced antioxidant activity together with a few cold related defensive genes transcribed in presence of melatonin. Similarly, melatonin-­mediated long-distance transport under cold stress is observed in grafted watermelons (Tan et al. 2007; Li et al. 2021). To understand the role of melatonin in cold acclimatization, a wild species of Bermuda grass is pre-treated with 100 μM melatonin; these are then incubated for 8 hours, with and without cold-stress conditions of −5 °C. Results obtained when compared with melatonin untreated plants under cold stress clearly indicated a low amount of malondialdehyde (MDA) and electrolyte leakage (EL) and higher levels of chlorophyll, activities’of enzymes superoxide dismutase and peroxidase in the

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melatonin treated than in the non - treated plants (Fan et al. 2015). About 46 metabolites in melatonin-treated Bermuda grass showed alterations in concentration. The concentration of five sugars (arabinose, glucopyranose, mannose, turanose, and maltose) and propanoic acid showed a significant increase while the concentration of valine and threonic acid was highly reduced (Fan et al. 2015). Cold stress may induce chlorosis in leaves, wilting leading to necrosis and stunted growth (Janowiak et al. 2002), low and delayed seed germination in wheat (Jame and Cutforth 2004). It also affects root growth and root proliferation, resulting in poor nutrient and water uptake (Hussain et al. 2018; Kul et al. 2020). The reproductive phase of plant is also prone to cold stress (Thakur et al. 2010) as cold stress can result in premature abscission of flowers, aberrant pollen tube growth (Chakrabarti et al. 2011), pollen sterility (Ji et al. 2017), poor grain development (Barton et al. 2014), resulting in decreased final productivity of the plant (Hussain et  al. 2018). A lower temperature may also interfere with rhizosphere microbial activities resulting in poor nutrient availability (Massenssini et al. 2015). Moreover, cold stress also damages the structure and enzymatic processes occurring in mitochondria, hence reducing the rate of respiration (Ikkonen et al. 2020).

15.4.2 MT Crosstalk with Other Phytohormones Under Cold Stress Interplay of melatonin with abscisic acid (ABA) in cold stress was thoroughly investigated in two genotypes, a cold-tolerant Damxung (DX) and the cold-sensitive Gannan (GN) of Elymus nutans Griseb. Pre-treatment with both, melatonin and ABA can effectively overcome the inhibitory effect of cold stress. The endogenous level of melatonin, as well as ABA, was significantly increased in both the genotypes under cold stress. Further exogenous application of melatonin resulted in increased ABA production, while application of an ABA biosynthesis inhibitor fluridone, suppressed melatonin-induced ABA accumulation. However, pre-treatment with ABA and fluridone failed to alter the endogenous melatonin concentration. Observations were also made for up-regulation of the expression of cold-responsive genes in an ABA-independent manner on being treated exogenously with melatonin. Hence conclusion can be drawn that both ABA-dependent and independent pathways together may contribute towards melatonin-induced cold tolerance in E. nutans (Fu et al. 2017).

15.4.3 Melatonin-Induced Gene Regulation in Cold Stress Expression of certain genes involved in stress response pathways such as calmodulin binding transcription activator 1 (CAMTA1), C-repeat binding factor/ dehydration-­responsive element binding protein (CBF/DREB), cold regulated 15a (COR15a) and zinc finger transcription factors 10 and 12 may be upregulated in

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presence of melatonin (ZAT 10 and ZAT 12; Zhao et  al. 2017; Guo et  al. 2018; Wang et  al. 2018). In hulless barley seedlings a few genes involved in circadian clock are also altered by melatonin application helping the seedlings to regulate their growth and also to enhance cold tolerance (Chang et al. 2021). In addition to this, the expression patterns of some genes regulating phytohormone biosynthesis are also altered by exogenous melatonin treatment. For example, the expression of genes (ClAOC1) and (ClAMI1), involved in the biosynthesis of JA and IAA respectively are upregulated in watermelon leaves on being treated with melatonin under cold stress (Chang et al. 2020; Li et al. 2021) scaling up photosynthesis and redox homeostasis to enhance production (Chang et al. 2021). Overexpression of a few melatonin biosynthesis enzymes like TDC, ASMT, AANAT, and HIOMT in various crops resulted in boosting the level of endogenous melatonin (Meng et al. 2015; Zhao et al. 2015; Zhang et al. 2019a, b) as observed in a few tomato lines with the overexpression the ASMT gene. Additionally, some heat shock proteins are also generated in response to exogenous melatonin which provides cellular protection through refolding the denatured proteins that trigger heat resistance. Overall, both the exogenous applications as well as endogenous boosting of melatonin levels influenced plant growth, morphological and physiological changes, photosynthetic ability and activity of antioxidant enzymes in several plants like tomato, pea seedlings, and rice. Exogenous melatonin can also induce the expression of a few transcription factors (CBFs, DREBs, COR15a, CAMTA1, and ZATs) involved in many low-temperature specific responses (Bajwa et  al. 2014), indicating that the response shown by melatonin in cold stress is regulated at the transcriptional level. (Fig. 15.2). Li et al. (2016a) identified that in watermelon when treated with melatonin, the expression of a few miRNAs (miR159-5p, miR858, miR8029-3p, and novel-­ m0048-­3p) was downregulated. The downregulation is directly correlated with the upregulation of some targeted signal transduction genes like CDPK, BHLH, WRKY, MYB, and DREB and protection/detoxification genes (LEA and MDAR) under cold stress suggesting that negative regulation of target mRNAs by miRNA is a melatonin–mediated cold tolerance response.

15.4.4 Role of Melatonin in Heat Stress High temperatures stress may severely affect fluidity of cell membrane and the activity of enzymes. It can bring about morphological, physiological, transcriptional, post-transcriptional, and epigenetic changes in plants. Thermo-tolerance of plants is naturally enhanced in plants by increased endogenous synthesis of melatonin (Byeon and Back 2014). Ahammed et al. 2019 reported that in tomato, silencing the genes COMT1 and TDC, which are involved in the endogenous biosynthesis of melatonin, temperature-induced oxidative damage gets aggravated and at the same time there is overexpression of ASMT and SNAT to improve thermos-tolerance by increasing endogenous melatonin (Xu et al. 2016a; Wang et al. 2020).

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Fig. 15.2  Schematic representation of Melatonin induced cold-stress tolerance in plants. The enzymes involved are: Mitogen-activated protein kinase (MAPK), Calcium-dependent protein kinase (CDPK), Gamma-aminobutyric acid (GABA), l-arginine decarboxylase (ADC), l-ornithine decarboxylase (ODC), Pyrroline-5-carboxylate synthase (P5CS), Ornithine aminotransferase (OAT), glutamic acid decarboxylase (GAD), succinate dehydrogenase (SDH), cytochrome c oxidase (CCO), Lipoxygenases (LOX), Phospholipase D (PLD), catalase (CAT), Superoxide dismutase (SOD), Peroxidase (POD), Ascorbate peroxidase (APX), 2,2-diphenyl-1-picrylhydrazyl

Plant antioxidant defense mechanism can be enhanced by the exogenous application of melatonin during heat stress, which is attained by the accumulation of ROS and also by enhancing the proline metabolism pathway. Melatonin-mediated polyamines and nitric oxide biosynthesis also promote thermos-tolerance and redox homeostasis in tomato seedlings (Jahan et al. 2019). Melatonin interacts with hydrogen sulfide under heat stress to alleviate photosynthetic potential in wheat (Iqbal et al. 2021). Exogenous application of melatonin enhances the activity of heat shock proteins (HSFs) under heat stress as in Arabidopsis and tomato. Melatonin-mediated thermo-tolerance is due to upregulation of a few heat shock proteins, HSFA2, HSA32, HSP90, and HSP101 which later repair the denatured and damaged proteins (Shi et al. 2015b; Xu et al. 2016a, b). Exogenous melatonin treatment can also significantly improve the expression of heat shock factors (HSFA1s and HSFA2s) along

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with a few heat shock protein (HSP90 and HSP101) in Arabidopsis and can enhance stress tolerance in Raphanus sativus L. var. radculus pers, which resulted in a manifold increase in biomass, soluble protein antioxidant enzymes, especially for POD (Shi et al. 2015a, b, c, d, e, f; Jia et al. 2020). (Table 15.1). A heat shock protein HSP40 interacts with SlSNAT a melatonin biosynthesis enzyme and promotes thermo tolerance by stabilizing the activity of the enzyme Rubisco under heat stress (Wang et al. 2020). Melatonin treatment not only enhances cell membrane stability but also the expression of metabolic genes and hence mitigating the damage caused to the antioxidant mediated defense system through heat stress (Shi et al. 2015a, b, c, d, e, f). Application of melatonin in Triticum aestivum L. and Cucumber alleviated structural changes caused by heat stress by enhancing the activity of antioxidant enzymes, transcription of stress-responsive genes, and stabilizing the photosynthetic machinery (Arnao and Hernández-Ruiz 2009). Festuca arundinacae (turf grass) seedlings when pre-treated with melatonin and 24-epibrassinolide, showed an effective reduction in ROS, malondialdehyde and electrolyte leakage, at the same time amount of total protein, chlorophyll content and antioxidant enzyme activities also get enhanced under heat stress, resulting in improved growth of plant. Transcriptome analysis has shown that near about 4311 and 8395 unigenes showed significant change after 2 and 12 hours of heat treatments respectively, which includes genes related to heat stress response, redox reactions, nucleic acids and protein degradation, production of energy and metabolism of hormone. A few genes including FaHSFA3, FaAWPM and FaCYTC2 were upregulated by both melatonin and 24- epibrassinolide treatments, indicating that these genes are putative target genes of both hormones (Alam et al. 2018). Three different methods of exogenous melatonin application namely, seed soaking, root immersion, and foliar spraying were used at varying concentrations of melatonin in rice plants to understand the effect of melatonin in cold stress. Investigation showed that seed soaking and root immersion both methods when applied at higher doses could significantly relieve the stress-induced inhibitions in photosynthesis enhancing thereby the activity of enzymatic as well as non-enzymatic antioxidant levels (Han et al. 2017). Heat stress-mediated inhibition of pollen germination can be altered by treating plants with melatonin. In tomato (Qi et  al. 2018), exogenous application of melatonin-­enhanced expression of some heat shock proteins and autophagosomes to refold the unfolded or misfolded proteins and degrade the denatured proteins respectively, which are responsible for heat-induced degradation of organelles in pollen grains, leading to increased pollen germination. Heat-induced damage was reduced In kiwifruit (Actinidia deliciosa) (Dong et al. 2018) by exogenous melatonin which resulted in decreased H2O2 content, elevated levels of of amino acids proline, ascorbic acid, enhanced activity of antioxidant enzymes, dehydroascorbate reductase (DHAR), glutathione reductase (GR) and glutathione S-transferase (GST), superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR). Tomato seedlings when treated with 100 μM melatonin for 7 days followed by exposure to high-temperature stress for twenty-four hours, showed effective reduction in the

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Table 15.1  Effect of melatonin treatment on physiology, growth and antioxidant property of plants under temperature stress Abiotic Stress Cold

Melatonin treatment Plant species (μM) Arabidopsis 10–30

Chilling

Cucumber

50–500

Chilling

0.1

Chilling

Rhodiola crenulate American elm Watermelon

Chilling

Wheat

1000 (1 mM)

Chilling

Cabbage

10–1000

Chilling/ salinity/ drought

Bermuda grass

20–100

Chilling/ salinity/ drought Chilling/ drought

Arabidopsis

50

Barley

1000 (1 mM)

Chilling

Tomato

100

Heat

Phacelia

0.3–90

Heat

Arabidopsis

5–20

Heat

Tomato

10

Chilling

0.1–0.5 150

Effect/observation Marked increase in shoot height, fresh weight and development of primary roots, thereby increasing survival rate survival Marked increase in GSH pool and a decrease in ROS (reactive oxygen species) burst Increased NR activity and NO content Cryopreservation of callus observed

Reference Bajwa et al. (2014) Shi and Chan (2014) Zhao et al. (2017)

Zhao et al. (2011a) Regrowth induced in frozen shoots Uchendu et al. (2013) Enhanced photosynthesis and Li et al. decrease in cold-related microRNA (2016a, b) Turk et al. Redox balance is increased, (2014) chlorophyll content increased, enhanced osmoregulation, decrease in ROS burst Zhang et al. Increase in the amount of (2016) anthocyanins, proline, increase in redox balance, decrease in ROS burst Increase in fresh weight, enhanced Shi et al. (2015a, b, c, d, osmoregulation, decrease in ROS e, f) burst, reduced cell damage Fan et al. (2015) Increase in sucrose content; Shi et al. enhanced survival rate (2015a, b, c, d, e, f) Li et al. Enhanced photosynthesis (2016a, b) efficiency, decrease in ABA and water content, reduced ROS burst Jannatizadeh Enhanced cytochrome oxidase, H-ATPase and Ca-ATPase enzyme et al. (2019) activity Germination promoted Tiryaki and Keles (2012) Enhanced thermotolerance Shi et al. (2015a, b, c, d, e, f) Enhanced thermotolerance and cell Xu et al. protection (2016a, b) (continued)

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Table 15.1 (continued) Abiotic Stress Heat

Melatonin treatment Plant species (μM) Triticum 100 aestivum

Heat

Glycine max 100

Heat

Actinidia deliciosa Lolium perenne

Heat

200 20

Effect/observation Protection against inhibition of photosynthesis during heat-stress via cross-talk with Hydrogen sulphide. Increase in phenolic and flavonoid content, enhanced biosynthesis of PA and SA, decreased ABA content, reduced ROS burst Enhancement in antioxidant enzyme activities Increased content of t-ZR by regulating CK biosynthesis

Reference Iqbal et al. (2021)

Imran et al. (2021)

Liang et al. (2018) Zhang et al. (2017a)

oxidative stress by scaling up their antioxidant defense mechanism, activating the ascorbate–glutathione cycle, and reprogramming the metabolic pathway for biosynthesis of polyamines and NO. All of these alterations contributed for better scavenging of excessive ROS and hence enhanced the cellular membrane integrity to mitigate oxidative stress induced by high temperature (Jahan et al. 2019) (Table 15.1). In wheat seedlings exogenous application of MT significantly improved their heat tolerance by modulating their antioxidant defense system by ascorbate peroxidase (APX) mediated activation of the ascorbate–glutathione (AsA–GSH) cycle, increasing the activities of glutathione reductase (GR) and stabilizing the photosynthesis process by increasing the content of chlorophyll. Exogenous application of MT under heat stress also leads to enhancement in the endogenous MT concentration in comparison to the untreated controls. Further, some genes related to reactive oxygen species (ROS)(TaSOD, TaPOD, and TaCAT), and genes responsive to anti-­ stress such as TaMYB80, TaWRKY26, and TaWRKY39, were also induced in MT-treated wheat seedlings (Buttar et al. 2020).

15.4.5 MT Crosstalk with Other Phytohormones Under Heat Stress Melatonin is involved in crosstalk with several other phytohormones and in doing that it suppresses heat-induced leaf senescence by interacting and regulating signalling and biosynthesis pathways for ABA and CK (Zhang et al. 2017b) (Fig. 15.3). Exogenously applied melatonin upregulates SA and downregulates ABA levels in soybean seedlings to overcome heat-induced damage (Imran et al. 2021) in tomato.

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Fig. 15.3 Schematic representation of Melatonin induced heat-stress tolerance in plants. Hormones involved: Abscisic acid (ABA), Gibberellic acid (GA). Enzymes involved: Tryptophan decarboxylase (TDC), Tryptamine 5-hydroxylase (T5H), N-acetylserotonin methyltransferase (ASMT), serotonin N-acetyltransferase (SNAT)

In order to understand the mechanism behind the interaction melatonin with GA and ABA in heat-induced leaf senescence (Jahan et al. 2021), tomato seedlings were pre-treated with 100 mM melatonin (MT) and water and were exposed to high temperature stress for 5  days. Results clearly showed reduced yellowing of leaf, increased Fv/Fm ratio and reduced ROS production indicating thereby that melatonin treatment can significantly overcame heat-induced leaf senescence. The expression certain genes like Rbohs gene, chlorophyll catabolic genes and genes associated with senescence was significantly suppressed by melatonin treatment. In addition to this exogenous application of MT, elevated the endogenous level of MT and GA but at the same time reduced the ABA content under high-temperature stress. The expression of the suppressor of GA signaling and GA catabolic gene was inhibited, while the expression of the ABA catabolic gene was upregulated by melatonin application (Fig. 15.3) (Table 15.1).

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15.5 Conclusions and Future Perspectives Melatonin plays a significant role in alleviating damage caused by temperature stress in plants. Melatonin enhances tolerance to temperature stress in plant through three pathways, (1) Improves antioxidant property by scavenging the ROS and RNS (2) regulating the expression of genes involved in stress related responses, production of antioxidant and a few phytohormones (ABA, GA, SA, JA, and ET) biosynthesis pathways by acting as a signaling molecule (3) Maintain antioxidant potential during abiotic stress by regulating redox homeostasis through interaction with NO . Although melatonin is endogenously synthesized in plants under biotic and abiotic stress, at the same time, its exogenous application can significantly modulate plant growth and impart temperature stress tolerance in plants. The exogenous MT application improves several aspects of plant growth like the synthesis of photosynthetic pigments, rate of photosynthesis, stability of membranes, maintenance of osmotic balance by osmolytes, plant water relations, uptake of water and nutrients, root growth, leaf senescence, under temperature stress. Moreover, exogenous MT also overcomes the deleterious effects induced by cold-stress in plants by increasing the expression of several defensive genes responsible for the higher antioxidant activities. Although research has demonstrated the strong effects of exogenous melatonin in enhancements of plant stress tolerance, however the precise mechanism of melatonin signaling, transcription of genes, and epigenetics is still very obscure and requires more investigation. Melatonin can affect the biosynthesis, signaling, and functioning of other phytohormones, but the exact mechanisms by which melatonin crosstalk with these phytohormones need to be explored further. Transfer of the information derived from melatonin–mediated temperature stress tolerance to a wide variety of crops and raising transgenics in this area are the future perspectives for its potential application in crop improvement.

References Afreen F, Zobayed S, Kozai T (2006) Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation. J Pineal Res 41(2):108–115 Aghdam MS, Jannatizadeh A, Nojadeh MS, Ebrahimzadeh A (2019) Exogenous melatonin ameliorates chilling injury in cut anthurium flowers during low temperature storage. J Post Harv Bio 148:184–191 Ahammed GJ, Xu W, Liu A, Chen S (2019) Endogenous melatonin deficiency aggravates high temperature-induced oxidative stress in Solanum lycopersicum L.  Environ Exp Bot 161(2019):303–311 Alam MN, Zhang L, Yang L, Islam M, Liu Y, Luo H, Yang P, Wang Q, Chan Z (2018) Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide. BMC Genomics 19(1):1–14 Arnao MB (2014) Phytomelatonin: discovery, content, and role in plants. Adv Bot 2014:815769

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Chapter 16

Melatonin-Mediated Salt Stress Tolerance in Plants Tanveer Ahmad Khan, Bisma Hilal, Qazi Fariduddin, and Mohd Saleem

Abstract  Among the abiotic stresses, salt stress could become more severe for sustainable agricultural practices and limit crop production. It affects plant growth performances and limits both the yield and quality of crop plants by disturbing the optimum physiology and metabolism of the plants. Melatonin (Mel) is a multifaceted signaling molecule and is involved in a wide range of physiological processes in plants such as improvement in growth, germination of seeds, adventitious rooting, photosynthetic processes, and osmoregulation. Importantly, Mel acts as an antioxidant with a significant role in the regulation of cellular redox homeostasis by scavenging excessive accumulation of toxic reactive oxygen species (ROS) as well as reactive nitrogen species (RNS) and also enhances the antioxidant system in the plants under stress conditions, including salt stress. Recently, Mel has been implicated in combating salt-induced toxicities by regulating multiple plant processes such as enhancing the level of osmoregulatory substances, up-regulating Na+ exclusion and sequestration, increasing the K+/Na+ ratio, protecting photosynthetic pigment system and biomolecules, regulating stomatal movements and gene expression of salt stress-associated genes. In this compiled work, we have comprehensively discussed the regulatory role of Mel in augmenting salt stress tolerance in plants. Keywords  Melatonin · Salt stress · Signaling molecule · ROS and RNS · Salt tolerance

T. A. Khan · B. Hilal · Q. Fariduddin (*) · M. Saleem Plant Physiology and Biochemistry Section, Department of Botany, Faculty of Life Sciences, Aligarh Muslim University, Aligarh, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_16

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16.1 Introduction Increasing salinity is a serious global challenge, as it limits plant growth performances and adversely affects crop production. Apart from naturally occurring soil salinity, its level in the soil has enhanced and is expected to increase further due to a number of reasons such as poor irrigation practices, mismanagement of wastewater, and climate change (Khan et  al. 2022b). Climate change acts through either enhanced evaporation and thus induces drought stress or a rise in the sea level (Rengasamy 2006). The toxic effect of salt stress on agricultural plants is caused by both decline in soil moisture content, and sodium as well chloride ion toxicities (Munns and Tester 2008; Khan et al. 2022b). On the contrary side, halophytes are plants that are well adapted to salinity environments. They have special mechanisms to deal with high salinized conditions (Flowers et al. 2015) and could be used as candidates to understand the salt resilience in plants. High salinity stress triggers osmotic as well as ion toxicity in plants and negatively affects plant growth processes and induces developmental as well as metabolic changes (Flowers et  al. 2015). Furthermore, accumulation of high salt concentration leads to more catastrophic events such as enzyme inhibition, disorganization of the membrane, disturbance in membrane potential, hyper-accumulation of ROS, downregulation of photosynthesis, and decline in nutrient acquisition (Greenway and Munns 1980; Yeo 1998; Hasegawa et  al. 2000). However, agriculturally important plants are mostly glycophytes (salt-sensitive) and thus there is a dire need to develop sustainable approaches in order to optimize plant production on salinized agricultural land. Plant growth regulators (PGRs) are used to alleviate salt stress and among them, the application of Mel could prove a novel strategy for combating salt-induced toxicities. Chemically Mel is known as N-acetyl-5-methoxytryptamine which is a multi-­ regulatory signaling bioactive compound present in plants as well as in animals. Lerner et al. (1958) first detected Mel in the bovine pineal gland and then researchers extensively studied the functions of Mel in animals, particularly its functions as a neurohormone (Reiter et al. 2010). Mel regulates a wide range of processes like circadian rhythms, sleep, and acts as a potent antioxidant molecule (Pieri et  al. 1994; Khan et al. 2020). The existence of Mel was confirmed in higher plants by two research groups Hattori et al. (1995) and Dubbels et al. (1995). The studies in plants revealed that Mel is a potential antioxidant molecule that neutralizes oxidative stress and also acts as a key molecule in maintaining membrane structure, particularly chloroplast and mitochondrial membranes (Galano et  al. 2011; García et al. 2014; Khan et al. 2022a). The protective functions of Mel against multiple stress conditions in plants have now been established (Arnao and Hernández-Ruiz 2019; Khan et al. 2020, 2022a, b). Furthermore, the structural similarity of Mel to auxin (IAA) infused researchers to carry out studies regarding its interactive roles with other PGRs. It has been well-studied in plants that Mel acts as a potential antioxidant molecule and also regulates a number of physio-biochemical processes (Arnao and Hernández-Ruiz 2019; Khan et al. 2020, 2022a, b). Additionally, the

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first receptor of Mel namely CAND2/PMRT has recently been identified in Arabidopsis and also confirmed in cotton plants (Wei et al. 2018; Yu et al. 2021). Thus, considering the diverse role of Mel in plants, it is now considered a potent master regulator in plants. Therefore, the pleiotropic functions governed by Mel in plants, particularly its functions in the mitigation of salt-induced negative effects in plants are discussed in this chapter.

16.2 Biosynthesis of Mel in Plants in Relation to Salinity Stress It has been widely experimented that exogenous application of Mel significantly enhanced plant stress tolerance including salinity stress (Khan et  al. 2020; Khan et al. 2022a, b), and plant biologists are now focusing to modulate the endogenous level of Mel in plants via genetic transformation. Mel biosynthesis in plants shares a common precursor molecule, tryptophan with auxin. Briefly, biosynthesis of Mel starts with the processes of decarboxylation of amino acid tryptophan forming tryptamine; secondly, hydroxylation of tryptamine leads to the formation of serotonin; thirdly, serotonin N-acetyltransferase (SNAT) enzyme regulates the formation of N-acetyl serotonin from serotonin, and then, Mel is synthesized from N-acetyl serotonin through catalyzation of two types of enzymes known as ASMT or COMT (acetyl serotonin methyl transferase or caffeic acid O-methyltransferase) (Byeon et al. 2014a; Wang et al. 2014; Khan et al. 2020, 2022b). It has also been reported that the enzyme activity of COMT in rice was higher by 700-fold to that of ASMT during Mel biosynthesis, and the COMT overexpression increases the level of endogenous Mel and therefore promotes salinity stress resilience in plants (Byeon et al. 2014b). Usually under normal growth conditions, a constant level of Mel is maintained in plants but its level is strongly affected by environmental stresses such as salt, water stress, and oxidative damage (Arnao and Hernández-Ruiz 2019; Khan et al. 2022b). For example, seedlings of barley and lupine when exposed to chemical compounds like NaCl, ZnSO4, and H2O2 had an enhanced concentration of Mel (Arnao and Hernández-Ruiz 2009). The activities of Mel biosynthetic enzymes seem to be strongly regulated in response to stress stimuli. For instance, HIOMT enzyme activity was elevated in cotyledons of sunflower plants under salinity, which results in the production of Mel (Mukherjee et al. 2014). Moreover, overexpression of Mel biosynthetic genes such as AANAT or HIOMT in tomato plants enhanced the levels of Mel and thereby improved drought stress resilience (Wang et al. 2014). In another study, it was found that overexpression of Mel biosynthetic genes was associated with improved internal water balance in Malus hupehensis plants under drought stress (Li et al. 2015).

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16.3 Involvement of Mel in Conferring Tolerance to Salt Stress Plants being sessile in nature regulate their cellular physiology to alleviate adverse stress conditions including salt stress. Under stressed conditions, swift and tremendous changes occur in plant cells for survival. Mel is a multifaceted signaling bioactive compound that governs a wide array of plant processes. One important feature of Mel is that it has amphipathic property and thus diffuses easily through the membrane system into the cytosol and moves through cellular organelles. Further, its receptor has been recently identified and characterized in Arabidopsis namely CAND2/PMTR1 (Wei et al. 2018) and is also confirmed in cotton plants (Yu et al. 2021). The phytomelatonin receptor is localized on the cell membrane and has a topology like receptor, Mel stimulates its expression and then it binds with the α-subunit (GPA1) of G-protein. Phytomelatonin–receptor interaction induces the separation of Gγb and Gα subunits, which stimulates H2O2 production by NADPH oxidase-dependent H2O2 production (RBOH), upsurges Ca2+ ion influx and improves K+ efflux and these processes trigger the closure of stomata. Therefore, phytomelatonin could be a new plant hormone that regulates stomatal closure via the phytomelatonin i.e., CAND2/PMTR1-facilitated signaling cascade and H2O2-mediated signaling (Wei et al. 2018). Salt stress negatively affects agricultural production, therefore imposing a great challenge to sustainable agriculture. It adversely affects plant growth by inducing physiological drought conditions and ion toxicity which then collectively inhibits growth of the plant or even causes death at higher levels by distorting enzyme activity, redox balance, and membrane fluidity. Additionally, it could be toxic to biomolecules, like proteins, nucleic acids (DNA, RNA) and, triggers ROS and causes oxidative burst (Zhu 2001; Khan et al. 2020, 2022a). It is now well-studied that Mel promotes tolerance to salt stress in a number of plants such as Zea mayz, Triticum aestivum, cucumber, Solanum lycopersicum, and Oryza sativa (Chen et al. 2018; Ke et al. 2018; Zhou et al. 2016; Liang et al. 2015). The results of these studies further reiterate that Mel is a potential antioxidant molecule that inhibits peroxidative metabolism in plants under abiotic stress. The role of Mel under drought conditions has been evaluated. Deficit water conditions during the seedlings growth of lupin trigger an upsurge in endogenous Mel level that was 4-fold more than that detected in well-watered plants, signifying that Mel is a vital signaling player (Arnao and Hernández-Ruiz 2013). A similar study also revealed that Mel treatment to drought-­ stressed cucumber plants had an increased root growth and germination of seeds by regulating redox balance and increasing the photosynthetic efficiency, demonstrating that the supplementation of Mel limits the inhibitory effects of drought stress (Zhang et  al. 2013). The protective effect of Mel has been evaluated in waterstressed apple plants. Root dipping application of Mel significantly reduced the leaf senescence, enhanced photosynthetic attributes like PS-II efficiency, and improved

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the antioxidative system, which infuses the researchers to recommend the usage of Mel as a beneficial molecule for agricultural production (Wang et al. 2013; Weeda et al. 2014; Wang et al. 2012). In vitro culture of shoot tip explants of cherry maintained in a medium augmented with Mel resulted in a significant increase in proline levels suggesting that Mel may be the indicator of stress tolerance (Sarropoulou et  al. 2012). Another study highlights the tolerance in transgenic tomato lines through overexpressing Mel biosynthesis genes such as AANAT and HIOMT under drought stress. The transgenic tomato plants recovered fully following re-watering, while the wild-type (which do not overexpress Mel biosynthetic genes) plants did not recover (Wang et al. 2014).

16.3.1 Regulation of Ion Homeostasis by Mel Under Salt Stress Regulating K+ and Na+ ion homeostasis is very crucial in response to salinity stress conditions. Two vital ion channels (NHX1 and AKT1) are important in maintaining ion homeostasis and were significantly up-regulated in plants by the application of Mel under salt stress (Li et  al. 2012) thereby promoting salt stress tolerance. Application of Mel decreased the Na+ and Cl− accumulation in rice seedlings and increased the transcription of SOS signaling genes such as OsSOS1, OsCLC1, and OsCLC2, (Li et al. 2017a, b). Mel treatment mediates K+/Na+ homeostasis which could be due to increased breakdown of triacylglycerol, β-oxidation of fatty acid, and energy turnover in order to sustain the plasma membrane H+-ATPase activity, thereby sustaining K+/ Na+ homeostasis (Li et al. 2017b). Moreover, these studies further corroborate the findings of another report which revealed that Mel treatment mitigated the impact of salinity stress by improving energy production in cucumber plants under salt stress (Zhang et al. 2017a). Mel promotes resistance to salinity by facilitating K+ maintenance and stimulates RBOHF which produces ROS as signaling molecules thereby inducing stress-responsive genes and up-regulating K+ uptake transporters in rice. In another report, it has been revealed that the application of Mel increased salt stress tolerance by improving K+/Na+ ratio in potato plants, enhancing K+ and reducing Na+ and Cl− contents (Yu et al. 2018b). Mel significantly improved salt resilience in tomato by improving the photosynthetic efficiency and maintaining the balance between ROS and the antioxidants (Khan et  al. 2022a). Thus, it seems that Mel plays an important role in promoting salt stress tolerance, regulates different mechanisms, and functions in a number of ways to modify these processes. Based on the current study, the regulatory functions of Mel in response to salt stress have been comprehensively summarized in Fig. 16.1.

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Fig. 16.1  Illustrates the effects of salinity-induced toxicities and the regulatory role of Mel in alleviating salt stress. The red-colored text boxes show the salt-induced toxicities in the plants while the green-colored text boxes show the different regulatory mechanisms governed by melatonin under salt stress

16.3.2 Mel-Mediated Antioxidative Defense Under Salt Stress Abiotic environmental constraints, like drought, salinity, heavy metal stress and extreme temperature, can negatively affect plant functions like electron transport chain, thereby inducing photo-oxidation and a progressive decrease in photosynthetic efficacy in plants (MaGururani and Tran 2015; Almeida et al. 2017; Alvi et al. 2022). Notably, above mentioned, abiotic stresses also trigger ultrastructural alterations in leaf chloroplasts and mitochondria structures, leading to excessive formation of ROS like H2O2 or O2▪ ─ (Debnath et al. 2018; Khan et al. 2020; Hilal et al. 2023). The photosynthetic efficacy is dependent on chlorophyll content which in turn is important for growth and development of plants and enhanced ROS levels due to salt stress decreases chlorophyll content in plants (Tan et al. 2012). However, at optimal physiological conditions, ROS are maintained at lower concentrations and act as essential secondary messengers in various plant signaling and physiological functions (Yu et al. 2018a; Khan et al. 2022b). High salt stress generated ROS bursts and induces oxidative stress in plant tissues. Interestingly, Mel, a potent antioxidant molecule and can directly scavenge excessive ROS more efficiently than the classical antioxidants compounds, like Ascorbic acid, NADH and glutathione (GSH) (Reiter et  al. 2016; Tan et  al. 2012; Khan et  al. 2020). Moreover, one

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molecule of Mel can neutralize numerous toxic free radicals. Additionally, AMK, AFMK, and nitosomelatonin, which are the metabolites of Mel can also neutralize ROS (Tan et al. 2012, 2016; Reiter et al. 2014; Reiter et al. 2015). It is now well established that Mel mitigates stress-stimulated oxidative injuries in plants and acts as a powerful antioxidant, improving the overall antioxidant system and regulating the stress-responsive genes to promote tolerance in plants against diverse range of environmental stresses such as salt stress (Shi et al. 2015; Zuo et al. 2017). Mel treatment markedly enhanced plant growth by boosting carbon assimilation, as well as providing protection to cellular proteins (Xu et al. 2016; Zhang et al. 2017b). Additionally, numerous related studies also confirmed the involvement of Mel in promoting the photochemical efficacy of PSII (Xin et al. 2013; Meng et al. 2014; Ye et al. 2016; Zuo et al. 2017). Application of Mel to plants treated with ZnO nanoparticles significantly improved the Fv/Fm signifying the bio-stimulatory role of Mel (Xin et al. 2013). Stomatal movements play an important part in the processes of photosynthesis and respiration. Exogenously Mel treatment improves stomatal conductance in different plants such as grape and apple plants (Li et al. 2015; Meng et al. 2014). Moreover, pretreatment of Mel enhanced the stomatal dimensions (length and width), regulated its movements in plants under stress conditions, and substantially increased the photosynthetic efficiency (Meng et al. 2014; Khan et al. 2022a). In rice plants, the application of Mel causes a considerable decrease in the chlorophyll damage, as well as down-regulates the senescence-associated genes (Liang et al. 2015). Therefore, Mel seems to be important for conferring resilience to environmental stresses in plants. Metabolites of Mel such as N1-acetyl-N2-formyl-5-methoxyknuramine (AFMK), 2-hydroxymelatonin, or cyclic-3-hydroxymelatonin can also function as antioxidants and neutralize ROS directly (Tan et  al. 2012; Tan et  al. 2016; Khan et al. 2020). Notably, Mel also increases the activities of antioxidant enzymes (SOD, CAT, GSH, and ASA), thereby neutralizing ROS indirectly (Reiter et  al. 2014; Reiter et al. 2015). Interestingly, Mel in crosstalk with other signaling compounds like nitric oxide regulates cellular homeostasis. For instance, it has been studied that Mel modulates NO and improves GSH levels and activity of GR under salt stress in sunflower seeds (Kaur and Bhatla 2016). Recently, it has been also revealed that Mel protects the membrane integrity by decreasing the TBARS content, regulating the AsA-GSH as well as enhancing the activities of antioxidant enzymes in rice plants (Yan et  al. 2021). Also, chlorophyll damage and ROS accumulation were significantly reduced under salinity stress in rubber tree seedlings by Mel treatment which was mainly by modulating the Mel biosynthesis, photosynthetic processes, ROS metabolism and flavonoid genes (Yang et al. 2020). Similarly, recent findings of Li et al. (2022) evaluated that Mel up-regulated the genes associated with photosynthesis, ROS scavenging and MAPK in Limonium bicolor plant in response to salinity stress.

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16.3.3 Mel-Mediated Plant Growth and Development Under Salt Stress Salinity stress negatively affects plant functions like the growth of the plants, seed germination, photosynthetic activity, and ultimately limits agricultural production (Yu et al. 2018b). Apart from salinity-induced osmotic as well as ion toxicity, high salt stress may also lead to nutritional disorders and deficiencies along with oxidative damage (Parida and Das 2005; Gao et al. 2008; Acosta-Motos et al. 2017; Khan et al. 2022a, b). Thus, salt stress affects plants in complex manure and disturbs plant physiology and metabolism. However, the beneficial effects of Mel to promote tolerance to salt stress in plants have been exploited by two methods: exogenous supplementation of Mel and/or overexpression of the Mel biosynthetic genes (Kanwar et  al. 2018). Findings of recent studies revealed that exogenous Mel treatment enhanced growth, chlorophyll content, photosynthetic processes, and antioxidant system, but reduced the ROS content and finally oxidative stress under salt stress in cucumber and tomato plants (Wang et al. 2016; Khan et al. 2022a). The direct involvement of Mel in regulating plant growth processes was primarily studied in coleoptiles of different plants such as Hordeum vulgare, Phalaris canariensis, Triticum aestivum, and Avena sativa, and findings disclosed that the growth of coleoptiles of these plants was improved when treated with Mel (Hernandez-Ruiz et al. 2005). The application of Mel also promoted the growth of other plants like Cucumis sativus, Arabidopsis and tomato (Posmyk et al. 2009; Wei et al. 2015; Khan et al. 2022a). In Arabidopsis and rice, suppression of Mel biosynthetic enzymes, SNAT1 or SNAT2 led to the development of plants with stunted growth (Hwang and Back 2018; Lee and Back 2019). Overexpression of rice IDO gene in transgenic tomato plants had reduced endogenous Mel concentration and decreased plant biomass, which suggests that increasing the production of Mel can improve plant growth (Okazaki et al. 2010). A structural resemblance between Mel and indol-amine hormone IAA, infuses the researchers to investigate the influence of Mel on growth and development in the root system of plants and this area of research has gathered ample consideration. In the last two decades, a number of reports highlighted the possible role of Mel in promoting growth of roots (Pelagio-­ Flores et al. 2012; Arnao and Hernández-Ruiz 2015; Wen et al. 2016; Chen et al. 2019). Exogenous Mel treatment stimulated root organogenesis, like adventitious or lateral root development, in numerous plant species, such as Arabidopsis, Oryza sativa and Lupinus albus, (Arnao and Hernández-Ruiz 2007; Pelagio-Flores et al. 2012; Zhang et al. 2014b; Chen et al. 2019). Pelagio-Flores et al. (2012) found that exogenous application of Mel enhanced adventitious or lateral roots growth in Arabidopsis by up to two-fold. Dawood and El-Awadi (2015) revealed that faba bean plants treated with Mel had decreased uptake of ions of sodium chloride and improved cellular water level, enhanced phenolic content, improved photosynthetic efficacy, enhanced nutrient uptake, and plant biomass under salt stress conditions. In another study, treatment of Mel to Cucumis sativus improved the growth, and nitrogen metabolism under salinity conditions (Zhang et al. 2017b). Likewise, Jiang

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et al. (2016) revealed that exogenous application of Mel alleviated the salt-induced negative effects and improved plant growth by promoting photosynthetic processes, enhancing antioxidant efficiency, and homeostasis. It has also been observed that relative to control, Mel contents in roots enhanced significantly under salt stress conditions (Zheng et al. 2017) which suggest that it could play a crucial role in mitigating stress conditions. Also, seed soaking or Mel pre-treatment enhanced salt stress tolerance through up-regulation of cell division gene expression (BUBR1, CDH1, CYCA, and CYCB genes), photosynthesis genes (Psa (A, F, G, H, K, and O) in PS I, and Psb (E, O, P, Q, Y, Z, and 28) in PS II), VTC4, which regulates carbohydrate metabolism, and UDP-glucuronosidase genes in soybean (Wei et al. 2015).

16.3.4 Crosstalk of Mel with Plant Growth Regulators Phytohormones, also known as plant hormones, are low molecular bioactive compounds active in minute levels in plants and play a crucial role in their growth and development. These phytohormones also have a central effect on the regulation of stress responses and therefore act as potent players against environmental stresses. Mel is a newly introduced plant growth regulator and is involved in regulating a wide array of plant processes (Khan et al. 2020, 2022b). For instance, Mel boosts the rate of photosynthetic efficiency (Khan et  al. 2022a), promotes adventitious rooting (Chen et  al. 2019), delays senescence (Wang et  al. 2013), and predominantly regulates stress responses under environmental cues (Arnao and Hernández-­ Ruiz 2019; Khan et al. 2022b). Mel also interacts with principal hormones like IAA, BR, GA, and ABA in modulating various plant responses including redox network (Arnao and Hernández-Ruiz 2018; Tan and Reiter 2020). Mel as a growth promoter has been investigated in a number of plants e.g., Arabidopsis, rice, Lupinus albus and tomato (Arnao and Hernández-Ruiz 2007; Pelagio-Flores et  al. 2012; Chen et al. 2019; Khan et al. 2022a). Mel promotes lateral root growth via IAA independent pathway, as Mel neither stimulates expression of DR5: GUS, which is an auxin-stimulated gene marker nor downregulates HS: AXR3NT-GUS (Pelagio-­ Flores et al. 2012; Koyama et al. 2013). Sarropoulou et al. (2012) also evaluated that Mel has a similar action to that of IAA in promoting the rhizogenesis in tomato and mustard and also exogenous applied Mel elevated the IAA and IBA levels (Wen et al. 2016; Chen et al. 2009). Low levels of Mel (50 μM) application increased the gene expression of auxin signaling-pathway (IAA-19; 24) and auxin efflux genes (PIN-1, 3, 7) as well as lateral root promotion in tomato seedlings (Wen et al. 2016). Under salt stress, Mel enhanced the expression levels of auxin-responsive genes OsIAA8, OsARF5, OsARF6, OsGH3–1, OsGH3–2, and OsSAUR10 and brassinosteroids-­responsive genes (OsBLE3 and OsDWARF) in rice (Xie et  al. 2021). Mel can modulate ABA levels e.g., in cucumber pre-treatment of Mel (1 μM) suppressed biosynthesis gene of ABA (NCED2) and induces ABA catabolism genes like CYP707-A1; A2, which results in a significant reduction in ABA content under salinity stress (Zhang et al. 2014a). Additionally, it has been studied that drought

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stress up-surges phytohormones such as ABA, JA and BRs, and suppresses CKs and GAs, however, Mel enhanced levels of GAs, BRs, CKs and JA and decreases ABA contents (Moustafa-Farag et al. 2020). In another experimental study, Mel declined the ABA level in drought-treated apple plants by up-regulating MdCYP707A1 and MdCYP707A2 and down-regulating MdNCED3 gene (Li et  al. 2015). Therefore, Mel also interacts with phytohormones and regulates a wide array of growth and developmental processes.

16.4 Conclusion Salinity stress is one of the serious abiotic stresses that negatively affects the productivity of crops throughout the globe. There are various approaches used to alleviate salinity stress and among them, supplementation of Mel could be a potentially sustainable approach to mitigate the salt stress in crop plants. Mel demonstrates promising results for enhancing salt resilience in crop plants by modulating the physiology and metabolism of plants. Interestingly, Mel protects the photosynthetic machinery and enhances the chlorophyll content under salt stress, thereby boosting photosynthetic efficacy and fundamentally promoting the growth of the plants. In addition, Mel application increases osmoregulatory compounds and regulates the genetic expression of defensive genes activated in response to salinity stress. Notably, under salinity stress, treatment of Mel reduced the accumulation of ROS through different mechanisms such as enhancing the antioxidant system and modifying stress-responsive genes and thus regulating redox homeostasis. Therefore, application of Mel could be a novel sustainable method for conferring salt stress resilience in crop plants.

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Chapter 17

Role of Phytomelatonin in Promoting Ion Homeostasis During Salt Stress Ali Mahmoud El-Badri, Maria Batool, Ibrahim A. A. Mohamed, Ramadan Agami, Ibrahim M. Elrewainy, Bo Wang, and Guangsheng Zhou

Abstract  Salinity is one of the major abiotic factors limiting plant growth and agricultural productivity. Salt stress disrupts the ion compartmentalization and leaf water status, resulting in an ionic imbalance and impairing mineral uptake and ion homeostasis. Plants cope with ion toxicity through various mechanisms, including ionic balance which is one of the important stress responses against salt stress. Notably, melatonin holds a crucial function in plant’s responses to salinity stress through its ample potential in regulating the signaling related to stress-mediated pathways in various plants. In this context, the role of melatonin in promoting ion homeostasis under salinity stress by mediating various physiological and molecular mechanisms has been described in detail. As a master regulator in plants, melatonin can improve plant defense response to salt stress conditions by directly regulating A. M. El-Badri MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China Field Crops Research Institute, Agricultural Research Center (ARC), Giza, Egypt M. Batool · B. Wang · G. Zhou (*) MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China e-mail: [email protected] I. A. A. Mohamed MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China Botany Department, Faculty of Agriculture, Fayoum University, Fayoum, Egypt R. Agami Botany Department, Faculty of Agriculture, Fayoum University, Fayoum, Egypt I. M. Elrewainy Field Crops Research Institute, Agricultural Research Center (ARC), Giza, Egypt © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_17

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ROS and RNS or indirectly regulating Ca2+ levels and K+/Na+ homeostasis. Exogenously applied melatonin regulates calcium signaling-related genes such as PLC2, HIPP02, CML10, CML45, and Na+/H+ antiporter-related genes (SOS1, SOS2, and SOS3); besides increasing Ca2+-ATPase activity for ATP synthesis, which improves plant development under stresses. Moreover, it has a significant contribution to K+ signaling by increasing RBOHF-dependent ROS signaling that improves the K+ level under salt stress, indicating that melatonin may improve plant stress response through regulating NADPH function in the K+ transporters pathway and K+ transporter genes such as AKT1, GORK, SOS1, HAK1, HAK5, and HAK21. In conclusion, melatonin enhances K+/Na+ and Ca2+/Na+ levels by increasing the influx and distribution of K+ and Ca2+ with decreasing Na+ levels under salt stress conditions to maintain ion hemostasis, thus plant stress tolerance. The comprehensive knowledge of the versatile role of melatonin in anti-stress regulation will help decipher its mode of action and signaling cascade in plants that aid in understanding the roles of melatonin-mediated ion homeostasis under salinity stress conditions. Keywords  Melatonin · Ion homeostasis · Signaling · Nitric oxide · Calcium · Potassium · Salt stress

17.1 Introduction Salinity is one of the detrimental abiotic factors that seriously threaten global agricultural crop production and cause yield loss. Globally, salinity affects about 20% of cultivated land and 33% of irrigated agricultural land; consequently, 1.5 million hectares have not been cultivated due to higher salinity conditions, which contributes to an annual loss of $27.3 billion in agriculture and posing a great threat to food security (El-Badri et al. 2021b). Salt stress limits plant growth by producing osmotic and ionic stress that impairs water uptake and causes nutritional imbalance. Moreover, sodium ions (Na+) can disturb the metabolic processes by replacing ions, especially potassium ions (K+), during enzymatic reactions, ultimately impairing enzymatic function (El-Badri et al. 2021a; Mohamed et al. 2020a). Salinity causes disturbance in the ion compartmentalization and leaf water status, which leads to ionic imbalance and impairs mineral uptake and ion homeostasis (Ashrafi and Nejad 2018). A maintained cytosolic K+/Na+ ratio is vital for plant survival, while high salinity levels lead to an imbalance of ions (Na+, K+ and Ca2+) (Chinnusamy et al. 2005). Plant copes with Na+ toxicity through vacuolar compartmentalization of excessive ions and/or effluxes it at the root-soil interface (Tester and Davenport 2003), by using Na+/H+ antiporters on plasma and vacuolar membranes. Besides, plants maintained H+ gradients and improved H+-pumps functioning to control membrane depolarization and facilitate Na+/H+ transport in the vacuolar membrane (Apse et al. 1999). Lower Na+ and higher cytosolic K+/Na+ levels are helpful for cell metabolic processes as well as better growth and salt stress responses (El-Badri et al. 2021a, 2022a).

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Excessive Na+ and Cl− ions lead to different physiochemical disturbances such as osmotic stress, ionic toxicity, mineral imbalance, disrupted stomatal movement, and gradual leaf death due to the higher solubility of Na+ and Cl−; thus, cellular ions begin to compete with harmful Na+ ions (Ayub et al. 2020). Moreover, Na+ has a competition with K+ for main binding sites in different processes, mainly enzyme activity, biosynthesis of protein, and ribosome functions, due to the resemblance in their physio-biochemical characteristics such as radius and hydration energy of both ions (Shabala and Munns 2017). The aforementioned knowledge has demonstrated that higher Na+ reduces the availability of vital minerals for plants that negatively affect ions transporter, i.e., NSCC and HKT, due to the higher competition to occupy the uptake sites between Na+ and other important cations (K+ and Mg2+), causing membrane depolarization that led to essential mineral ions in-flow passively and decreased the anions influx (NO3− and PO4−3) due to decreasing H+-ATPase activity, as ATP level is reduced due to imbalance osmoprotectants synthesis under salt stress (Ashraf 2009; Shabala and Cuin 2008). Extensive accumulation of sodium (Na+) and chloride (Cl−) ions adversely affect various cellular processes since a higher Na+ level impairs the action of transporter protein related to mineral absorption, thereby alleviating the nitrogen (N) and K+ contents in the tissues (El-Badri et al. 2021c). In addition, excessive salt accumulation leads to ionic imbalance, hence disrupting ionic homeostasis; therefore, the re-establishment of ion homeostasis is a necessary process that enables the plant to improve salt tolerance (D’Amelia et al. 2018). Higher salinity levels cause massive K+ loss that negatively affects plant growth due to the high participation of K+ in various physiochemical processes (EL Sabagh et  al. 2021); besides, the higher influx of Na+ into the cytoplasm results in membrane depolarization, and thus an efflux of K+ from cells resulting in a higher Na+/K+ ratio in the cytosol. Hence, the ability of cells to avoid membrane depolarization by maintaining intracellular K+ homeostasis is a key mechanism for salt tolerance (Shabala and Munns 2017). Furthermore, as signaling molecules, H2O2 and Ca2+ control the ion transport system, thus balancing the Na+/K+ level (Sun et al. 2010). On the other hand, under salt stress conditions, plants are characterized by adapting different strategies, including transportation, homeostasis and compartmentalization of ions, and osmotic protection by operating the antioxidant system and producing polyamine molecules that are capable of mediating the adverse effects of salinity (de Freitas et al. 2019). To adapt salt stress, plants control the influx of Na+ into root tissues and migration into leaf tissues to maintain the Na+/K+ level (Liu et al. 2021; Wang et al. 2019), induce NO synthesis (Zhao et al. 2019), activate ion channels and transporters (Wu et al. 2018), compartmentalization of Na+ from the cytosol to the vacuole (Wu 2018), and/or exclusion of Na+ to roots (Munns and Tester 2008). Nitric oxide (NO) participates in various physiological processes in plants. Moreover, NO-derived molecules, known as reactive nitrogen species (RNS), cause nitrosative stress, whereas reactive oxygen species (ROS) are involved in oxidative stress. Initially, the attention was on the deleterious effects of these molecules and their related counteracting mechanisms under stress conditions; later on, they are

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considered essential participants in signaling networks to trigger the defense responses in plants (Turkan 2017). Recently, it was found that two species (ROS and RNS) showed a metabolic interplay to regulate nitro-oxidative stress response in plants; however, under a stressful environment, excessive production of these molecules can impair cell integrity (Corpas and Barroso 2013). Despite the damaging effects, a proportion of the same molecules may also involve in stress signals to lessen the damage. ROS, especially hydrogen peroxide (H2O2) and RNS, especially NO, as signaling molecules, regulate the ionic balance of Na+/K+ (Qiao et al. 2014). The regulatory role of ROS and RNS against ionic stress of salinity is a fascinating and emerging field of research (Zhao et al. 2018b). Higher salinity levels adversely affect the ionic balance and cell structure leading to cell death, while melatonin application modulates the Na+/K+ level in plant cells due to alleviated K+ loss (Li et al. 2017a). Interestingly, melatonin has not significantly affected the Na+ level in roots; while it reduced the Na+ with increasing K+ levels in seedlings shoot, suggesting its role in restricting Na+ loading in root xylem and/or increasing Na+ retrieval from shoots rather than modulating Na+ uptake in maize roots (Jiang et al. 2016). Melatonin is a pleiotropic molecule with multiple regulatory mechanisms and stress tolerance roles (Huangfu et al. 2021; Jiang et al. 2021). As a master regulator in plants, melatonin application can improve the plant’s defense response to counteract the salt stress condition by regulating nitric oxide (NO) (Fancy et al. 2017), Ca2+ level, and K+/Na+ homeostasis (Sun et  al. 2021; Yu et  al. 2018). Moreover, elevated endogenous melatonin levels under salt stress with exogenously applied melatonin enhanced stress tolerance in Oryza sativa plants (Yan et al. 2020). Salt stress led to an increase in K+ efflux through NSCCs and KORC channels (Demidchik and Maathuis 2007) due to increased cell membrane depolarization (Shabala et al. 2003). However, membrane repolarization occurs by increasing the activity of the H+-ATPase that maintains the level of K+ in the cell (Shabala et al. 2016). Melatonin works to regulate the activity of H+-pump and ATP levels by elevating NO content, which positively affects ionic uptake and homeostasis (Arnao and Hernández-­ Ruiz 2013). However, the application of cPTIO (NO scavenger) negatively affected the melatonin- mediated H+-pump activity and indicated that melatonin and NO relationships regulate H+-pump is helpful to maintain the H+ gradient of vacuolar membrane and polarization of plasma membrane (Chinnusamy et  al. 2005; Shabala and Pottosin 2014). Melatonin participates in the redox network of ROS and RNS regulation via mediating H2O2 and NO signaling in a feedback loop (Gong et al. 2017; Reiter et al. 2016; Shi et al. 2015a). The regulatory functions of melatonin, ROS, and RNS are controlled by NO biosynthesis enzymes (NOS-like and NR), key enzymes (RBOH), and melatonin synthesis genes (TDC, T5H, SNAT, COMT, and ASMT) (Chen et al. 2018b; Molassiotis et al. 2016). Researchers have recently identified melatonin signaling associated with K+ influx in the cell through regulating the transcription level of RBOHF-dependent ROS-related genes and K+ transporters genes, indicating that melatonin has a vital role in ionic homeostasis under salt stress, which enhances plant tolerance (Arnao

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and Hernández-Ruiz 2015). Furthermore, under salinity stress conditions, maintaining Na+, K+ and Ca2+ homeostasis is a hallmark to reduce plant stress damage; therefore, melatonin treatment maintains cellular ion balance through triggering fatty acid β-oxidation triacylglycerol breakdown, and plasma membrane H+-ATPase activity (Shafi et  al. 2021). Exogenously applied melatonin reduces Na+ and Cl− contents by increasing the expression level of SOS1 (Salt Overly Sensitive) in rice root tissues as well as CLC1 and CLC2 in rice root and leaf tissues (Li et al. 2017b). Additionally, melatonin enhances ATP synthesis and regulates NHX1 and AKT1 genes related to ion channels, conferring ion homeostasis, and thus improving the plant’s salt tolerance (Li et al. 2019). Likewise, melatonin plays a significant role in ionic transport by controlling Ca2+ signaling and membrane permeability (Wei et al. 2015). Moreover, it is involved in the induction of NADPH oxidase-dependent H2O2 synthesis (RBOH) and enhancement of Ca2+ and K+ uptake by inducing the separation of Gγb and Gα by melatonin-receptor linkage; thereby, it controls the stomatal movement (Arnao and Hernández-Ruiz 2019). In recent years, melatonin has been at the core of attention; what makes the study of melatonin important in plants is its diverse participation in plant growth and defense system under the adverse environment. Melatonin acts as a potential bio-­ stimulator molecule in plants, and considerable success has been attained to explore the involvement of melatonin in ion homeostasis under salt stress conditions. A comprehensive review of previous findings is necessary to disclose in detail to better understand the role of melatonin in ion homeostasis; therefore, an effort has been made to summarize the dynamic aspects of melatonin in ionic equilibrium under salt stress conditions. This context will summarize the melatonin-mediated regulation of ion homeostasis and the interaction between melatonin and ion signaling (NO, K+ and Ca2+) to confront salt stress in plants.

17.2 Roles of Ion Homeostasis in Plants Under Salt Stress Conditions Environmental adversities, especially salt stress, severely affect agricultural production; moreover, higher salt concentration leads to an excessive increase in sodium ions, which causes cellular ionic imbalance (Doungous et al. 2022). The intracellular ionic (Na+/K+) balance/ homeostasis is vital for normal physiological processes, salt tolerance, and plant development (Zhang et al. 2022a). Maintaining an appropriate ionic flux is essential to avoid ion toxicity; therefore, plants employ different mechanisms to keep ion homeostasis, including ion transport regulated by H+ pumps, ion transporters, and channels (Zhao et al. 2021). Moreover, a balanced transporters and/or channels activity for Na+ and K+, and stabilizing the cytosolic K+/Na+ ratio has become a key mechanism of salt tolerance due to its stabilizing role in a variety of metabolic processes (Mohamed et al. 2022). Under salinity stress, the ion balance becomes even more crucial; hence, regulatory mechanisms related to ion homeostasis can be a source of understanding the complex interactions and

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pathways involved in ion transport; therefore, knowledge regarding plant responses under Na+ toxicity to avoid ionic stress becomes significantly important (Zhang et al. 2022b). In addition, since K+ is involved in a myriad of physiological and molecular functions in different plant cells, a high external Na+ level often competitively inhibits K+ uptake, resulting in a deficiency of K+ that diminished growth under high salt stress conditions (Assaha et al. 2017; El-Badri et al. 2022b; Ketehouli et al. 2019). Under low or medium levels of salt stress, Na+ can promote plant development; this beneficial effect may be due to the role of Na+ in substituting K+ in the vacuole, making more K+ available to the cytosol (Almeida et al. 2017; Wu 2018). Calcium is a promising mediator that senses stress signals and triggers the signaling mechanisms under stress conditions (An et al. 2020). Under salt stress, various Ca2+ sensors, such as calmodulin, calcineurin B-like protein (CBL) and Ca2+-dependent protein kinase (CPK), decode Ca2+ resulting in the release of free Ca2+ cascade in the cell cytosol (Vafadar et al. 2020). Salt Overly Sensitive (SOS) signaling pathway consists of a complex of three genes (SOS3, SOS2, and SOS1) is considered a significant contributor to cellular signal transduction under salinity stress for ionic homeostasis (Ji et al. 2013). Excessive Na+ accumulation leads to elevated Ca2+ signaling by SOS3 (Ca2+-binding proteins) that trigger SOS2 (Ser/Thr kinase) (Yang and Guo 2018), SOS2 further triggers SOS1 (codes for Na+/H+ antiporter in the plasma membrane), which leads to cellular Na+ extrusion out of the cell (Quintero et al. 2011), as shown in Fig. 17.1. Furthermore, P-type ATPases (P-ATPases) are localized at the plasma membrane and become more active to counteract Na+-induced depolarization; moreover, proton pumps (H+-ATPase) play an essential role in transporting ions (activate secondary transport) at the cellular level (Zelm et al. 2020). Na+/H+ exchangers (NHXs) are

Fig. 17.1  Roles of ion homeostasis in plants under salt stress conditions

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versatile transporter in vacuolar membranes, and it is important for cellular ion homeostasis by balancing Na+/K+ ions through transporting them in exchange for H+ in cells under excessive Na+ contents (Nawaz et  al. 2017). The NHX1 genes encoding NHX transporters balanced the cellular Na+/K+ ratio by Na+ extrusion to develop a steady state under salt stress conditions (Liu et  al. 2017). Moreover, P-ATPase has a role in mediating the Na+/proton antiporter SOS1/NHX7 to exclude Na+ ions from the root (Cui et al. 2020). In Arabidopsis thaliana, overexpression of NHX1 increases salt resistance and improves Na+ accumulation in shoot parts during the salt stress by sequestering Na+ in the vacuole (Gong et al. 2020). Transgenic B. napus plants that overexpressed NHX1 (a vacuolar Na+/H+ antiport from A. thaliana) could grow and produce seeds in the presence of 200 mM NaCl (Zhang et al. 2001). It was found that NHX1s were the highest up-regulated genes under salt stress among all NHXs that showed higher expression in rapeseed shoots than roots (Cui et al. 2020), as shown in Fig. 17.1. Similarly, vacuolar H+-ATPase (V-ATPase) plays an important role in stress response in plants. The V-ATPase subunit H (VHA-H) is required for the formation of a stable and efficient V-ATPase; whereas, a total of 22 VHA-H genes have been identified from 11 plants representing major crops, and shared exon-intron structures similar to those of A. thaliana (Kang et al. 2019). Table 17.1 and Fig. 17.1 provide examples of gene families involved in ion hemostasis that promote the salt tolerance of plants. The K+ transporter (HAK) is the high-affinity K+ transporter family, which plays key roles in K+ homeostasis, root and embryo development, and stress resistance. Recently, Zhou et  al. (2020) identified 40 putative HAK genes divided into four groups based on phylogenetic analysis, eight of which are significantly upregulated under K+-deficiency treatment.

17.3 Melatonin Regulates Ion Homeostasis Under Osmotic Stress Ion homeostasis refers to a plant’s ability to maintain proper ionic balance under stress conditions; moreover, under higher salinity levels, plants absorb more Na+, which affects the activity of enzymes in the cytosol, thereby the homeostasis of Na+, Ca2+, K+ and H+ is a vital cellular process (Shabala and Munns 2017), via increasing Na+ leakage and K+ influx into the cytosol, which protects plant cell under salt stress conditions (Wangsawang et al. 2018). Furthermore, melatonin treatment maintains ion balance through decreasing Na+ uptake and enhancing K+ uptake to maintain the K+/Na+ ratio under sodic alkaline conditions in Solanum lycopersicum leaves (Liu et al. 2015b), as well as it reduced Cl− content in Citrus aurantium leaves under salt stress conditions (Kostopoulou et  al. 2015). Melatonin applications had various vital roles in modulating ion hemostasis in different plants under salinity stress conditions, as mentioned in Table 17.2. The NHX1 gene encodes a vacuolar Na+/H+ exchanger, and the AKT1 gene encodes a Shaker-type K+ channel protein that plays a role in K+ uptake by roots

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Table 17.1  Examples of gene families involved in ionic hemostasis to enhance salt tolerance of plants Cellular localization Plasma membrane

Gene family Na+/H+ antiporter (NHX1)

Member Na+/H+ antiporter (NHX1)

Vacuolar Na+/H+ antiporter (NHX1)

Vacuolar Na+/H+ antiporter (NHX1)

Plasma membrane

Vacuolar H+-ATPase (V-ATPase)

Vacuolar H+-ATPase (V-ATPase)

Tonoplast and various components

High-affinity K+ transporter (HAK) KT/HAK/ High-affinity KUP family K+ transporter 5 (HAK5) HAKs

Plasma membrane

Cell surface membrane

KT/HAK/ Arabidopsis Plasma KUP family K+ membrane transporter 1 (AKT1) KT/HAK/ K+ Plasma KUP family transporter 1 membrane (HKT1)

Function during salt stress Enhances salt tolerance with increased Na+ accumulation in leaves and maintenances of seed and oil quality under high salinity in saline soils. Vacuolar Improves tolerance sequestration to salinity-induced of Na+ and K+ oxidative stress by improving intracellular ion homeostasis, transpiration rate, osmoregulation and reduced cell membrane damage. Tonoplast V-ATPase acts as a membrane stress-responsive enzyme that undergoes moderate changes in the expression of subunits and modulations of enzymatic structures. Potassium Improvement of K+ (K+) utilization efficiency transporter of plants under salt stress conditions. A symporter It is activated under a for protons low K+ level. and the K+ ion Up-regulation of HAK5 transporter genes that are associated with salt tolerance. It mediates K+ Up-regulation of uptake by AKT1 transporter plant roots in genes that correlates response to with salt tolerance in low K+ level plants. Mediate the Increased the balance expression level of between Na+ HKT1 transporter and K+ ions genes associated with salt tolerance. Function Vacuolar sequestration of Na+ and K+

Reference Zhang et al. (2001)

Rajagopal et al. (2007)

Kang et al. (2019)

Zhou et al. (2020)

Chakraborty et al. (2016)

Chakraborty et al. (2016)

Chakraborty et al. (2016)

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Table 17.2  Role of melatonin in modulating ion hemostasis in different plants under salinity stress Melatonin application Application concentration method Crop 100 μM 1/2 Tomato Hoagland’s (Solanum solution lycopersicum L.)

Rapeseed (Brassica napus L.)

25, 50 and 100 μM

Seed priming

Melon (Cucumis melo L.)

100 μmol L−1 Nutrient solution

Maize (Zea mays L.)

20 and 100 μM

1/2 Hoagland’s solution

Salt stress concentration Melatonin roles 150 mM NaCl Maintains the integrity of the cell membrane through decreasing Na+ translocation from underground to upperparts with an effective elevation of K+ level, which enhances root architecture and then the growth and development of plants. 100 mM NaCl Melatonin reduces ion toxicity by enhancing the levels of K+/Na+ and Ca2+/Na+ that is positively correlated with growth and yield-related traits, which maintain ionic balance under salt stress conditions. 100 mmol⋅L−1 Significantly reduced Na+ level and markedly elevated Ca2+ level in melon seedlings. 150 mM NaCl Melatonin has altered the phenomenon of stressed roots and leaves of plants, which significantly reduced the content of Na+ and resulted in an obvious elevated content of K+.

Reference Altaf et al. (2021)

Mohamed et al. (2020b)

Wu et al. (2019)

Chen et al. (2018a)

(continued)

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322 Table 17.2 (continued)

Crop Wheat (Triticum aestivum L.)

Melatonin application Application concentration method 300 μmol L−1 1/2 Hoagland’s solution

Rice (Oryza sativa L.)

25, 50, 100, 200, 300 and 400 μM

Foliar spraying

Maize (Zea mays L.)

1 μM

1/2 Hoagland’s solution

Cotton (Gossypium hirsutum L.)

1 μM

1/2 Hoagland’s solution

Salt stress concentration Melatonin roles 100 mM NaCl It modulates the K+/Na+ ratio and increases the Ca2+ level, which maintains a higher water potential and lowers H2O2 accumulation in wheat plants. 50 and Reduced Na+ 100 mM NaCl influx and upward flow with enhanced K+ and Ca2+ that maintain the ionic equilibrium of K+/ Na+ and Ca2+/Na+ in rice leaf tissues. 100 mM NaCl In stressed plants, melatonin reduces Na+ level, meanwhile enhancing K+ levels that maintain K+/Na+ level in upper ground parts of maize. 100 mM NaCl Melatonin regulated the transcription level of AKT1 (K+ channel) and NHX1 and SOS1 (Na+/H+ antiporter genes), leading to modulation of Na+/ K+ level in tonoplast to protect plant cells from salt-induced damage and ionic imbalance.

Reference Zhang et al. (2022d)

Wei et al. (2021)

Jiang et al. (2016)

Shen et al. (2021)

(continued)

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Table 17.2 (continued)

Crop Rapeseed (Brassica napus L.)

Sweet potato (Ipomoea batatas L.)

Melatonin application Application concentration method 1 μM 1/2 Hoagland’s solution

0.1, 0.5, and 1 μM 50, 100, and 200 μM

Alfalfa (Medicago sativa L.)

50 μM

Citrus (Citrus 1 μΜ aurantium L.)

Strawberry (Fragaria × ananassa Duch.)

100 and 200 μM

Irrigated to treated roots. Foliar spraying to treated leaves Foliar spraying

Irrigated three times per week (300 mL each time)

Foliar spraying

Salt stress concentration Melatonin roles 100 mM NaCl Significantly elevated the Ca2+ and K+ levels, decreasing Na+ and Cl− levels in both roots and leaves of treated plants under salt stress conditions. 150 mM NaCl Melatonin induced ATP and H+ATPase activity in the plasma membrane, as well as modulated Na+/ K+ balance. 250 mM NaCl Modulating the level of Na+/K+ in upper parts resulted from decreasing the Na+ level. 100 mM NaCl It mitigated the levels of Na+ and Cl− by regulating the expression levels of stress-­ responsive genes SLAH1 (anion channels) and MYB73 (transcription factor correlated to ionic stress), which improve ion homeostasis in citrus plants. 40 and 80 mM Melatonin reduced NaCl Na+ content with increasing P, K+, Mg2+ and Ca2+ in leaves versus untreated plants.

Reference Javeed et al. (2021)

Yu et al. (2018)

Cen et al. (2020)

Kostopoulou et al. (2015)

Zahedi et al. (2020)

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from the soil (Shafi et al. 2021). In addition, it has been shown that up-regulation of NHX1, SOS1, and AKT1 genes enhances K+ content and reduces Na+ content in the plant cell (Sun et al. 2021). On the other hand, the application of melatonin reduced the deleterious effect of salt stress by elevating the transcription level of Na+ and K+ transporters-related genes (NHX1 and AKT1) to re-establish ionic homeostasis via transporting Na+ into the vacuole and maintaining a higher K+, thus balanced K+/ Na+ ratio (Li et al. 2012), indicating that exogenous melatonin plays a significant role in regulating ionic homeostasis to counteract salinity stress. Furthermore, Ca+2 signaling has a key role in plants exposed to environmental adversity which is enhanced by melatonin application that is an essential adaptive mechanism to reduce salt-induced damage and ameliorate plant growth and development (Abdelrahman et al. 2020). Foliar application of melatonin reduced the Na+ concentration and enhanced the K+ concentration, resulting in balancing the Na+/K+ ratio and increasing Ca+2 uptake in Olea europaea plants treated under salinity conditions (Zahedi et al. 2021). Previous investigations have shown that different applications of melatonin under stress conditions could regulate the ionic balance and maintain an appropriate Na+/K+ ratio in plant cells in Oryza sativa (Liu et al. 2020), Zea mays (Chen et  al. 2018a; Jiang et  al. 2016), and Gossypium hirsutum (Shen et  al. 2021), which explained the function of melatonin to restrict Na+ uptake, induced Na+ leak and/or translocated Na+ into the vacuole to protect the cell from the deleterious salt effects and Na+ sequestration in different tissues, besides increasing K+ influx in the plant cell. Taken into knowledge, K+ content is vital for enzyme activity, stomatal opening, and closure, as well as conservation of energy, thus raising the plant’s ability for proper development under salinity stress conditions (Shabala and Pottosin 2014). Moreover, exogenous melatonin application protects plant cells from the deleterious impacts of salt by modulating the efflux and influx of ions (Na+ and K+), thus maintaining a better proportion of K+/Na+ in Gossypium hirsutum (Chen et al. 2020) and Oryza sativa (Li et al. 2017b). In the same line, melatonin decreased the Na+ level in rice shoots and reduced the translocation factor of sodium ions by restricting the Na+ loading or/and raising Na+ recovery in rice shoots (Yan et al. 2021). Under melatonin treatment, increasing the selective absorption (SA), increased SA of potassium ions higher than that of sodium ions while increasing the selective transport (ST), increased the transport of potassium ions and decreased the transport of sodium ions from plant root to shoot, suggesting the higher capacity of roots for ST, indicating that melatonin enhanced the root’s ability for higher K+ uptake and lower Na+ uptake under salinity stress conditions in rice plants (Wang et  al. 2005). In wheat, melatonin elevated Na+ and Na+/K+ levels in the upper parts (stem and leaves) while reduced Na+ and Na+/K+ levels in the underground part (roots), indicating that melatonin might be regulated Na+ content firstly in roots and then in shoots, which interpret why Na+ level is higher in upper parts due to nutrient solution uptake and translocate in shoots (Zhang et al. 2022d).

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To maintain ionic balance, plants activate Na+ leakage to the apoplast or outer environment from the root as a vital mechanism under salinity stress conditions (Tester and Davenport 2003) by increasing the transcription level of SOS1 (Na+/H+ antiporter-related genes in the plasma membrane) (Shi et al. 2000). In the same way, melatonin raised the expression level of the SOS1 gene in root tissues, which led to Na+ transfer from the underground part to the upper part of rice plants (Li et  al. 2017b). Furthermore, melatonin increased the transcription level of NHX1 and SOS2 genes in Brassica napus seedlings, which maintain the Na+/K+ ratio in rapeseed roots (Zhao et al. 2018a). In A. thaliana, melatonin promotes massive Na+ loss, particularly in the meristem zone, by increasing the expression level of SOS genes in the root apex under saline conditions (Shi et al. 2002). Vacuolar sequestration is a vital mechanism for protecting the cell by suppressing Na+ content in the cytosol and elevating Na+ exclusion that is stimulated by electrochemical H+ gradients generated by plasma membrane H+-ATPase or vacuolar membrane H+-ATPase and H+-PPase (Munns and Tester 2008). In saline conditions, plant cells activate H+-ATPase and H+-PPase as essential ways to protect various cells from excessive Na+ in several plants (Chen et al. 2007; Liang et al. 2005). Moreover, exogenous melatonin elevated H+-pump activity in rice seedlings (Yan et al. 2021) and regulated the transcription level of NHX (a vacuolar Na+/H+ antiporter), indicating that melatonin can enhance the vacuolar sequestration of excessive sodium ions in apple and canola plants under salinity conditions (Li et al. 2012; Tester and Davenport 2003). Maintaining the level of K+ in the cell is an important process that helps the plant to grow under salinity conditions, as K+ is considered an important element in plant metabolism (Yu et al. 2016). Tolerant plants have a higher K+ concentration due to the regulation of ion transport through high H+-ATPase activity in the plasma membrane (Chen et  al. 2007). A previous study investigated that melatonin treatment enhanced K+ contents that are associated with a higher transcription level of AKT in Malus hupehensis (Li et al. 2012); also, melatonin increased H+-ATPase activity and ATP level to maintain plasma membrane polarization that facilitates K+ influx via K+ transporter in rice roots (Yan et al. 2021), which proved the significant role of melatonin in modulating K+ uptake under salt stress conditions. Similarly, melatonin participates in regulating different proteins involved in ATP synthesis, including glycosylate, glycolysis, and citric acid cycles; thus, it improves ion homeostasis (Na+/K+) under salinity stress in cucumber seedlings (Zhang et al. 2017). Additionally, 500 mM of melatonin treatment decreased Na+ and Cl− ions in Vicia faba (Dawood and El-Awadi 2015) and Oryza sativa (Li et al. 2017b). On the other hand, the transcription level of NHX1 was regulated by ABA and NaCl, which might be dependent on the signaling and biosynthesis of ABA via ABA-insensitive pathway1 under salinity stress (Shi and Zhu 2002; Yuan et al. 2014). Meanwhile, exogenously applied melatonin affected ABA decomposition and ABA biosynthesis, suggesting that melatonin may mediate ion homeostasis through ABA signal transduction by increasing the expression level of NHX1 and AKT1 genes (Li et al. 2012).

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17.4 Melatonin Mediates Signaling Pathways 17.4.1 Melatonin and Nitric Oxide Signaling Nitric oxide (NO) is an essential signaling agent involved in various plant stress responses to counteract environmental adversities (Arora and Bhatla 2017; Kaur and Bhatla 2016; Zhan et al. 2019). ROS (H2O2) and RNS (NO) work as important signaling molecules in plant cells; however, adverse external stimuli cause an imbalance in the production and degeneration of these molecules (Yan et al. 2021). NO synthase (NOS) is responsible for NO production in animal cells (Lozano-Juste and Leon 2009), while it was not evident in plant cells, whereas Helga and Josef in 1996 identified NOS-like proteins in the Mucuna hassjoo plants (Ninnemann and Maier 1996). Earlier, NOA1 was described as a NOS-like gene in Arabidopsis thaliana, while recently, it has been characterized the same as GTPases function that participates in binding RNA/ribosomes (Corpas et al. 2009). At present, seven different pathways of NO biosynthesis have been identified; according to NO function in plant cells, these are classified into two pathways, oxidative or reductive ones, involving arginine and nitrite as substrates, respectively (Gupta et al. 2011). In living organisms, NO signaling has been explained through the interaction of NO and S-nitrosation (Feng et al. 2019; Gupta 2011); moreover, S-nitrosothiol was produced as a result of S-nitrosation in which NO binds to its target proteins via cysteine residues (Astier et  al. 2011). Increased S-nitrosothiol content led to NO activation and reduced the hypersensitive response, which reduced ROS accumulation (Yun et al. 2011). Moreover, melatonin mediates plant growth under various environmental stresses byregulating NO-mediated protein S-­nitrosation (Chen et al. 2018b). The complex redox network was built as a result of the interaction of melatonin, ROS and/or RNS; in addition, melatonin acts as a significant antioxidative regulator that can modulate ROS and RNS signaling (Arnao and Hernández-Ruiz 2019). Exoand endogenous melatonin can significantly promote plant development through interfering with salinity-induced NO signaling (Shafi et  al. 2021). Under salinity stress conditions, endogenous melatonin level was enhanced in response to NaCl stress, while NO acts as a signaling molecule in signal transduction in A. thaliana (Lindermayr et al. 2005). Additionally, melatonin elevated S-nitrosation under salt stress conditions as well as promoting the expression level of BnNHX1 and BnSOS2, while these genes were downregulated by NO removal, indicating that melatonin and NO interaction play a vital role to keep ion homeostasis in the cell under stress conditions (Zhao et al. 2018a). Furthermore, NO is an integral part of signal transduction in plant cells, regulating different physiochemical processes; additionally, the interactions of melatonin and NO have a promising role in stress tolerance to fine-tune the plant response against salinity stress (Arnao and Hernández-Ruiz 2019). Overwhelming evidence has reported that different signaling pathways mediated by stress messengers, including Ca2+, H2O2 and NO, contribute significantly to melatonin-modulated

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stress tolerance in plants (Zhang et  al. 2022c). Likewise, melatonin application increased salt tolerance by mediating NO in rice plants (Yan et al. 2020); moreover, it elevated NO content under alkaline stress, whereas NO acts as a downstream signal for melatonin-mediated stress tolerance in tomato seedlings (Liu et al. 2015a). In the same trend in tomato seedlings, exogenously applied melatonin decreased the transcription level of GSNOR (S-nitroglutathione reductase), which increased the level of endogenous NO; ultimately, melatonin promotes seedling growth under saline conditions (Wen et al. 2016). In addition, NO is an important participant in the antioxidative response induced by melatonin (Lindermayr et al. 2005), and melatonin-­NO mediated signal transduction could promote plant development as well as mediate the oxidative homeostasis by mitigating excessive RNS and ROS in sunflower (Helianthus annuus) (Arora and Bhatla 2017). Melatonin has different promising functions in biological kingdoms as it is a multi-directional molecule, including under various environmental stresses (Zhang et al. 2019). Furthermore, melatonin biosynthesis is correlated with an exposure level of salinity and the genotype of plant species as sensitive or tolerant under stress conditions (Back et al. 2016). In Arabidopsis  thaliana, H2O2 and Ca2+ signaling are regulated by CAND2/ PMTR1-mediated melatonin signaling; thus, melatonin might be controlled the stomatal movement (Wei et al. 2018). Recently, various investigations in the biological kingdom revealed that melatonin is an effective protector against a wide range of adverse stresses and is instrumental in counteracting reactive species (ROS and RNS) in a receptor-independent manner (Zhang et al. 2022c). For instance, the roles of melatonin have been reported in previous research that shows its direct participation in the removal of excessive ROS and/or activation of antioxidant enzymes, which alleviates the stress-induced damage in plant cells under saline conditions (Altaf et al. 2021; Jahan et al. 2020). Melatonin has a vital role in NO signaling to maintain redox balance; for instance, the melatonin-NO relationship works to regulate glutathione content and activity; it also efficiently participates in modulating cellular NO accumulation in sunflower plants under saline conditions (Kaur and Bhatla 2016). Formerly researchers found that exogenous melatonin raises NO levels, leading to better root growth and development in tomato seedlings under NaCl stress conditions (Arnao and Hernández-Ruiz 2017); besides, NO application increased endogenous melatonin levels indicating a possible feedback loop in tomato plants (Wen et al. 2016). Exogenously applied melatonin mediates the NO synthesis and signal transduction to reduce the deleterious effect of salt stress in rice (Liang et al. 2015; Yan et al. 2020) and cucumber plants (Zhang et  al. 2014). Moreover, melatonin showed a similarity in function with indole-3 acetic acid and enhanced the endogenous NO level that regulates transcription factors and mediates redox balance related to salinity tolerance (Rehaman et al. 2021). Melatonin elevated the biosynthesis of NO in tomato and Arabidopsis under abiotic stresses (Liu et al. 2015a; Zhang et al. 2019), indicating that melatonin improves NO transporters activity under salt stress, thus regulating NO signaling in rice plants (Yan et al. 2021). Additionally, NO regulated the H+-pump and H+ translocation (Zhang et al. 2006) by modulating H2O2 (Siddiqui et  al. 2011), hence increasing salt tolerance in plants. Besides, melatonin-­treated

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plants showed a higher K+ uptake, suggesting that melatonin treatment improves the K+ transporter’s responses to ROS signals, indicating that melatonin raised the transcription level of transporter genes related to K+ uptake and improved H+-pump activity (Li et al. 2019).

17.4.2 Melatonin and Calcium Signaling Calcium (Ca2+) plays a vital role in the plant’s adaptive response to counteract the external stress stimuli and is considered a second messenger in regulating the proper growth and development of plants. Moreover, Ca2+ sensors are categorized into three main families: calcineurin B-like proteins, Ca2+-dependent protein kinases (CDPKs), and calmodulin (Bouché et  al. 2005; Kashyap et  al. 2020). Under an adverse environment, the plants rapidly respond through an upsurge of Ca2+ contents in the cytosol using Ca2+ pumps and transporters; therefore, Ca2+ signaling works as an essential regulator to respond to different biotic and abiotic stresses (Krishnamurthy et al. 2017). On the other hand, as signaling molecules, H2O2 and Ca2+ controlled the ionic transport system, hence balancing the Na+/K+ level (Sun et al. 2010). Glucuronosyltransferase is a Na+ sensor that turns on Ca2+ channels, which in turn activates Ca2+ uptake into the cell (Zhang et al. 2022d). Ca2+/CaM complex is formed as a result of Ca2+ in-flow from outside of the cell through Ca2+ channels in the plasma membrane that is helpful in the plant’s response against salt stress, indicating that melatonin positively affects the plant stress response through Ca2+ signaling under salinity conditions (Vafadar et al. 2020). Furthermore, as a versatile messenger, Ca2+ participates in regulating various metabolite syntheses stimulated by salicylic, abscisic, and jasmonic acid under various stresses (Guo et al. 2015; Lee-Parsons and Ertürk 2005; Vighi et al. 2019). To protect the cell from excessive Na+, plants elevate the Ca2+ level in the cytosol that stimulating Ca2+-binding proteins with the increased expression level of Na+/H+ antiporter-related genes under salinity conditions (Jiang et al. 2019). Melatonin regulates calcium signaling-related genes in plants (Zhang et  al. 2022c); besides, melatonin and Ca2+ calmodulin interactions are involved in Ca2+ signal transduction in animals (Posmyk and Janas 2008). Moreover, in Cynodon dactylon, melatonin application regulates the expression level of calcium-dependent protein kinase (CDPK) under oxidative stress (Shi et al. 2015b). CAND2/PMTR1 is a melatonin receptor in plants, whereas melatonin controls stomatal closure through the CAND2/PMTR1-mediated H2O2 and Ca2+ signaling pathways in A. thaliana (Wei et al. 2018). Inositol-1,4,5-triphosphate (InsP3) is one of the signaling molecules generated from phosphatidylinositol 4,5-bisphosphate hydrolysis by phospholipase C (PLC) under stress conditions (Hung et  al. 2014; Testerink and Munnik 2011). Inositol hexaphosphate (InsP6) is produced from InsP3 phosphorylation that mobilizes Ca2+ in plant cells (Krinke et  al. 2006). Stress conditions cause an increase in the

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intracellular Ca2+ levels that stimulate several calcium-binding proteins, such as Ca2+ sensors/decoders, protein kinases and transcription factors (Seifikalhor et al. 2019). Melatonin regulates the expression level of calcium-dependent signalingrelated genes in the phosphatidylinositol signaling pathway, suggesting that melatonin plays a vital role in salt tolerance by activating phosphoinositide metabolism (Weeda et al. 2014). Moreover, HIPP02 participates in the catalysis of IP6 synthesis (the storage form of phosphate), which modulates the mobilization of Ca2+ in plant cells (Krinke et al. 2006; Munnik and Vermeer 2010). Furthermore, the expression level of PLC2 and HIPP02 decreased under salinity conditions, while it increased with melatonin treatment; also, melatonin regulated the transcription level of InsP3 and InsP6 synthesis-­related genes, which enhancing intracellular Ca2+ as well as increased InsP3 and InsP6 synthesis; besides, through modulating the phosphatidylinositol signal pathway, melatonin might mediate the releasing of calcium ions in cotton plants (Zhang et al. 2021). On the other side, CML10 and CML45 negatively affected plant growth under salt stress, which caused massive Ca2+ leakage (Srivastava et al. 2013), whereas melatonin reduced the expression levels of CML10 and CML45 under salinity stress conditions, which increases the stress tolerance in plants (Zhang et al. 2021). Under higher salinity levels, plant cells work to exclude Na+ from the cytosol via activating the plasma membrane Na+/H+ antiporter (SOS1, SOS2, and SOS3), which transport and compartmentalize Na+ ions into vacuoles (Peng et al. 2014; Srivastava et al. 2013). On the other hand, Ca2+ level was increased in cell cytoplasm under saline conditions leading to trigger the CBL/CIPKs in the SOS signaling pathway to mediate ionic transport (Na+) in plants (Nikalje et al. 2017); besides, Ca2+ regulates SOS3/SOS2 complex that maintains Na+ balance through phosphorylation and upregulation of SOS1 gene (Zhang et al. 2022a). Former investigation showed that melatonin treatment increased the expression level of SOS1, which is directly related to Na+ ions transport from plant root to stem tissues which protect photosynthetic tissues from excessive Na+ (Ren et al. 2020). Also, melatonin-mediated ion hemostasis might be through regulating SOS-mediated Na+ leak and NO signaling during salinity stress conditions (Zhao et al. 2018a); moreover, it increased the transcription level of AKT1 and HKT1 genes (transporter genes of K+) in apple plants (Li et al. 2016). Taken into knowledge, H2O2 and Ca2+ signaling are essential contributors to ionic transport systems, especially Na+/K+ homeostasis (Michard and Simon 2020). On the other hand, melatonin treatment elevated K+ and Ca2+ contents and modulated H2O2 (Kaya et al. 2019), as well as increased Ca2+-ATPase activity for ATP synthesis, which improves the plant development under different stresses (Sun et al. 2018). In wheat plants, melatonin reduced H2O2 and enhanced Ca2+ levels in the cytosol; thus, Ca2+ activated RBOH that enhanced H2O2 production (Zhang et al. 2022d). Moreover, in melon seedlings, melatonin treatment (100 μM) enhanced the Ca2+/ Na+ level by increasing the influx and distribution of Ca2+ with decreasing Na+ levels under salt stress conditions (Wu et al. 2019).

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Fig. 17.2  Roles of melatonin in promoting ion homeostasis through regulating calcium signaling

To sum up, plants raise the Ca2+ level in the cytosol that stimulates Ca2+-binding proteins by increasing the expression level of Na+/H+ antiporter-related genes under salinity stress conditions to protect the cell from excessive Na+. However, melatonin plays a vital role in the regulation of Ca2+ signaling under salinity stress conditions by increasing the phosphatidylinositol to regulate the Ca2+ signaling in the plant cell. Moreover, melatonin regulates calcium signaling-related genes in plants such as PLC2, HIPP02, CML10, CML45, and Na+/H+ antiporter (SOS1, SOS2, and SOS3), and increases Ca2+-ATPase activity for ATP synthesis, which improves the plant development under salt stress. Furthermore, melatonin enhanced Ca2+/Na+ levels by increasing the influx and distribution of Ca2+ with decreasing Na+ levels under salt stress conditions that maintained ion hemostasis, thereby plant stress tolerance (Fig. 17.2).

17.4.3 Melatonin and Potassium Signaling An essential nutrient, potassium (K+) is a dominant cellular osmoticum and it is one of the co-factors that participates in the activity of several enzymes. K+ plays an essential role in various processes, including maintaining cytosolic pH, protein biosynthesis, and ionic balance (Gong et al. 2020). Moreover, K+ transporters are of great significance for ion homeostasis in cells under salt stress (Kashyap et  al. 2020). Under salt stress conditions, Na+ influx leads to excessive K+ efflux; therefore, an appropriate K+/Na+ level facilitates the physiological and metabolic processes, and it is an important marker for tolerance against salt stress (Almeida et al. 2017). In plant cells, K+ homeostasis is one of the key processes that enable plants to withstand stress by inhibiting cell membrane depolarization (Gao et al. 2021).

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Higher salinity level leads to a significant massive K+ loss, which causes ionic imbalance, particularly K+/Na+ in the cell, which might be due to different pathways using ROS-activated K+ channels (Shabala and Pottosin 2014) or GORK channels (Srivastava et al. 2013), which reduces the cellular K+ content. Melatonin treatments significantly decreased the massive K+ loss from root epidermis and leaf mesophyll cells in Ipomoea batatas (Yu et al. 2018), indicating that melatonin plays an essential role in maintaining ionic homeostasis by elevating the transcription level of ion transporter related genes in Malus hupehensis plants under salinity stress conditions (Li et al. 2010). On the other hand, exogenous melatonin promotes plant growth under stress conditions by elevating K+ influx due to melatonin’s unique structure, which gives it the ability to provide an election to ROS, thus reducing excessive ROS through a free radical scavenging cascade, hence reducing electrolytic leakage and maintaining appropriate K+/Na+ ratio, ultimately alleviating the plant cells damage caused by salinity induced stress in Oryza sativa (Yan et  al. 2020). Melatonin application enhanced the K+ content by elevating the expression level of transporter genes related to K+ in different tissues of Cynodon dactylon under potassium deficiency (Chen et al. 2017a). Similarly, the differential expression level of the transporter and channel-related genes for K+ uptake indicates that melatonin increases the stress-­ responsive signaling of the aforementioned genes, suggesting that melatonin treatment has a role in reducing the massive K+ loss induced by salt stress in Oryza sativa plants (Michard and Simon 2020). Moreover, H2O2 plays a crucial role in regulating the K+ signaling related to transporters and proteins; on the other side, melatonin plays a significant role in protecting the plant cells from excessive ROS, especially lesser H2O2 removal than •OH, which leads to a distinct H2O2-dependent signaling pathway that increases the plant ability to tolerate the salinity stress (Zhang et al. 2022a). Additionally, K+ influx was enhanced under saline conditions by activating NADPH oxidase-­dependent H2O2 signaling in Cucumis sativus, Cucurbita moschata (Huang et al. 2019) and A. thaliana plants (Ma et al. 2011). Previous reports have documented that exogenous melatonin improves plant stress response through regulating NADPH oxidase-dependent ROS signal transduction in Arabidopsis thaliana (Chen et al. 2017b) and Solanum lycopersicum (Gong et al. 2017), indicating that melatonin might be improved plant stress response by regulating NADPH function in the K+ transporters pathway. Respiratory burst oxidase homolog (RBOH) is an NADPH oxidase that is a source of ROS generation in apoplast; thus, it is associated with melatonin-activated K+ regulation under salt stress conditions (Michard and Simon 2020); however, AtrbohF mutant plants have exhibited lower salt tolerance and ionic imbalance as compared to wild type of A. thaliana plants (Ma et al. 2011). On the other side, melatonin application regulates the transcription level of K+ transporters-related genes by activating RBOHF-dependent ROS signaling then improving the K+ level in rice roots (Liu et al. 2020). Inward-rectifying K+ (AKT1) and high-affinity K+ (HAK1, HAK5, and HAK21) have been identified as important K+ channels and transporters-related genes, respectively (Gong et al. 2020). In the same line, GORK, AKT1 and HAK1, HAK5,

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and HAK21 were up-regulated with melatonin treatment in rice plants under salt stress (Liu et al. 2020). Moreover, in Arabidopsis under salinity conditions, HKT1;1 and SOS1 were associated with Na+ and K+ homeostasis (Gao et al. 2021); however, melatonin regulates AKT1 and HKT1 genes via the CBL1-CIPK23 pathway to maintain K+ ion balance (Li et al. 2016). Additionally, under salinity conditions, it has been reported that the increased level of endogenous melatonin works to up-­ regulate HAK5 and AKT1 (transporter-related genes), thereby maintaining ion K+ homeostasis in the cytosol of the plant cells (Liu et al. 2020). HAK5 plays a critical role in keeping ion balance (Na+ and K+) in plants, which is downregulated under higher salinity levels, while it was upregulated in A. thaliana plants treated with melatonin under NaCl solution (Shukla et al. 2021). Conclusively, a higher salinity level leads to massive K+ loss, which causes ionic imbalance due to different pathways using ROS-activated K+ channels or GORK channels, thus reducing cellular K+ content. On the other side, melatonin has a significant contribution to K+ signaling by increasing RBOHF-dependent ROS signaling that ameliorates K+ levels under salt stress conditions, suggesting that melatonin improves plant stress response through regulating NADPH function in the K+ transporters pathway. Moreover, melatonin plays an essential role in maintaining ionic homeostasis by elevating the transcription level of K+ transporter genes such as AKT1, GORK, SOS1, HAK1, HAK5, and HAK21 (Fig. 17.3). Fig. 17.3  Roles of melatonin in promoting ion homeostasis through regulating potassium signaling

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17.5 Concluding Remarks Under salinity stress conditions, intracellular ionic homeostasis is vital for normal physiological processes, stress tolerance and plant development. The balanced transporter and/or channel activity of Na+ and K+, and stabilizing the cytosolic K+/ Na+ ratio became a major mechanism of salt tolerance due to its stabilizing role in various metabolic processes. Melatonin is an omnidirectional molecule with ­multiple regulatory mechanisms and emphasizes stress tolerance. As a master regulator in plants, it improves plant defense response against salt stress conditions directly through regulating ROS and RNS or indirectly through regulating Ca2+ level and K+/Na+ homeostasis. Melatonin regulates Na+/K+ transport and K+ selective absorption ratio and stronger Na+ efflux and K+ influx by modulating the H+pump activity and ATP level, besides modulating Na+/K+ transporters in response to ROS/RNS (Fig. 17.4). Moreover, the interactions of ROS, RNS, and melatonin have described that melatonin has a vital role in the redox network; thus, melatonin can control various physio-biochemical and molecular responses to improve plant salt tolerance. Exogenously applied melatonin demonstrated remarkable adaptive mechanisms against salt stress through regulating NO, K+, and Ca+2 signaling-related genes as well as ion transporters and channel-related genes; besides modulating ROS and RNS scavenging systems (Fig.  17.4). Recently, a lot of research has been done, which shows the huge potential of melatonin in ionic homeostasis to improve salt

Fig. 17.4  The simplified schematic diagram shows the roles of melatonin-mediated ion homeostasis under salinity stress conditions

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stress tolerance in plants. However, significant gaps in melatonin regulatory pathways that could be used further must be explored to understand the roles of melatonin under salt stress.

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Chapter 18

Positive Regulatory Role of Melatonin in Conferring Drought Resistance to Plants Atif Khurshid Wani, Nahid Akhtar, Sani Sharif Usman, Abdullahi Ibrahim Uba, Farida Rahayu, Taufiq Hidayat R. Side, and Mala Murianingrum Abstract  Drought stress negatively affects the physiology, biochemistry, and morphology of plants. This leads to leaf rolling, leaf scorching, stunning plants, and permanent wilting. Plants adapt different strategies to build stress tolerance by enhancing the production of certain phytohormones. Melatonin is synthesized in plants in response to biotic and abiotic stresses, performing an important role as a plant growth regulator under environmental stresses Melatonin, a natural hormone, is widely found in animals, plants, protists, bacteria, and fungi. It is present in the roots, stems, leaves, fruits, and seeds of the plant in varying concentrations. The presence of melatonin has been revealed in coffee, corn, rice, barley, wheat, and oats. The role of melatonin in plant growth, development, and photosynthesis is well known. Melatonin potentially gives protection to the plants by improving reactive oxygen species (ROS) scavenging efficiency thereby safeguarding photosynthetic apparatus from drought led oxidative stress. In this chapter, the role of melatonin in plant stress tolerance during drought through the cascade of physiological and molecular mechanisms will be discussed. A. K. Wani (*) · N. Akhtar School of Bioengineering and Biosciences, Lovely Professional University, Phagwara, Punjab, India S. Sharif Usman School of Bioengineering and Biosciences, Lovely Professional University, Punjab, India Department of Biological Sciences, Faculty of Science, Federal University of Kashere, Pindiga, Gombe State, Nigeria A. I. Uba Department of Molecular Biology and Genetics, Istanbul AREL University, Istanbul, Türkiye F. Rahayu Research Center for Applied Microbiology, National Research and Innovation Agency, Bogor, Indonesia T. H. R. Side · M. Murianingrum Research Center for Horticulture and Plantation, National Research and Innovation Agency, Bogor, Indonesia © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_18

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Keywords  Melatonin · Plants · Drought · ROS · Photosynthesis

18.1 Introduction Melatonin or N-[2-(5-methoxy-1H-indol-3-yl) ethyl] acetamide or 5-methoxy-N-­ acetyltryptamine is found in plants and animals naturally. Since its discovery in 1958 several biological functions have been studied in relation to it (Chowdhury et al. 2008). Melatonin is secreted by the pineal gland in animals and regulates the sleeping pattern through hormonal action. Besides playing an active role in synchronizing circadian rhythms, it controls seasonal rhythmicity such as hibernation, molting, fattening, and reproduction. Because of its role in regulating blood pressure and sleeping pattern in animals, it is as a medication and dietary supplement for treating insomnia and sleeping disorders. Until 1987 melatonin was only known as a neurohormone in animals (Reiter 1995; Karasek 1999; Stein et al. 2020). In 1970, melatonin was found in coffee extracts, but it was supposed to be a byproduct of the extraction process (Ramakrishna et al. 2012). Subsequently, melatonin presence has been established in most of the plants. It is present in roots (Liang et  al. 2017), stems, leaves, seeds, and fruits (Zhang and Zhang 2021) in different concentrations. The concentration of melatonin varies between plant varieties of the same species depending on the growth conditions. The concentration ranges from picograms to micrograms (Arnao and Hernández-Ruiz 2009). A high concentration of melatonin has been reported in tea, coffee, corn, barley, and oats (Çalişkan et  al. 2017). Melatonin has been reported as a very potent antimicrobial, anticancer, and antioxidant agents like other plants and plant derivatives (Kostoglou-Athanassiou 2013; Sharif Usman et al. 2019; Mir et al. 2022a). When it is applied in synergy with other plant metabolites or drugs, there is a marked increase in its therapeutic function (Fan et  al. 2010; Wani et  al. 2022b). The biosynthetic pathways of melatonin in plants and animals show substantial relatedness. In both animals and plants, the precursor molecule of melatonin synthesis is tryptophan, producing serotonin as an intermediate. However, the enzymes in operation for the conversion of tryptophan to serotonin are different in animals and plants. In animals, the process is catalyzed by tryptophan hydroxylase and decarboxylase, however in plants tryptophan decarboxylase and tryptamine 5-hydroxylase are in action. In animals, tryptophan besides being present in dietary sources is produced in both mitochondria and cytoplasm, whereas in plants tryptophan is synthesized in chloroplasts (Chattoraj et al. 2009; Arnao and Hernández-Ruiz 2015a, b; Back et al. 2016; Zhao et al. 2019; Tan and Reiter 2020). The role of melatonin as an essential plant hormone remains obscure, however, its function in photosynthesis and growth is well established. The melatonin-­induced morphogenetic effects have been reviewed comprehensively over the years (Caniato et al. 2003; Posmyk and Janas 2009; Arnao and Hernández-­ Ruiz 2015a, b). The studies have been done in various plant systems, such as Triticum (Zafar et  al. 2019), Avena (Varghese et  al. 2019), Prunella (Fazal et  al. 2018), and Hordeum (Chang et al. 2022). The effects of melatonin are considerably

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similar to that of the auxin-induced effects (Hu et al. 2021). It is also presumed that indole acetic acid and melatonin show affinity towards the same binding sites (Chen et al. 2009). Being versatile in nature, it regulates functions like seed germination, flowering time, leaf senescence, biomass production, and root architecture (Altaf et al. 2021). Another important property associated with melatonin is the scavenging capacity against reactive nitrogen and oxygen species, including peroxyl radical, single oxygen, nitric oxide, and hydrogen peroxide (Jahan et al. 2019). Off late, metabolomic, transcriptomic, and proteomic studies conducted on Cynodon dactylon, Malus hupehensis, and Arabidopsis thaliana have shown marked melatonin-­ induced changes in mRNA and protein expressions (Weeda et al. 2014; Hu et al. 2020). Melatonin’s role in the complex biotic and abiotic stress protector, wound healing, senescence, and defense represent an emerging field (Sun et al. 2021). In this chapter, the brief account of the melatonin role in phytomicrobiome homeostasis and metabolism during drought conditions will be briefly delineated, besides highlighting its role in regulating drought stress tolerance.

18.2 Plant Adaptations Under Drought Stress The two major outcomes of climate change are an increase in temperature and a reduction in annual precipitation. Despite the development and advancement of weather forecasting models continues to be a major challenge. Thus, it is imperative to identify the biochemical, molecular, and physiological basis of plants to respond and adapt during drought conditions. Plants generally avoid dehydration by efficient water uptake system, increasing the cross-section of vessels, reducing transport distances by forming short internodes, closing stomata for limit transpiration, developing trichome leaf cover, shedding leaves, and reducing the number and size of leaves (Hura et al. 2022). Figure 18.1 gives an illustration of drought-induced stress and the response of the plant. Some plants withstand extreme dehydration by anabiosis, i.e., ceasing the metabolic activity (Zhang and Bartels 2018; Abd El-Gawad et al. 2021). Some plants when exposed to water stress conditions synthesize dehydrins or carbohydrates for stabilizing the cell membrane phospholipids (Eriksson and Harryson 2011). Plants perceive water deficiency in roots and coalesce this information with other plant parts. Vitis vinifera, and lycophytes respond to water scarcity by stomatal closure in ABA- independent and ABA-dependent manner respectively (Christen et  al. 2007; Takahashi et  al. 2020). The hydraulic stress also activates ABA synthesis in leaves (Finkelstein 2013). ABA increases Ca2+ currents leading to H2O2 activation, which is the principal component of guard cells. The H2O2-induced Ca2+ increase is now regarded as a sensor system for H2O2 in guard cells (Pei et al. 2000). Arabidopsis histidine kinase 1 (AHK1) also acts as an osmotic stress sensor. The loss and gain of AHK1 function are indicative of drought stress resistance and response through ABA accumulation and expression of drought-stress-induced genes (Wohlbach et  al. 2008). However, some T-DNA mutants of AHK1 didn’t show much difference in the accumulation of ABA as compared to control plants

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Fig. 18.1  Drought induced effects on plant’s germination, photosynthesis, shoot mass, nutrient uptake, and plant response to mitigate water deficit stress through leaf expansion, stomatal closure, ROS scavenging, and ABA production

under drought stress conditions- instead showed higher stomata density (Kumar et al. 2013). Legumes respond to hydraulic stress by reducing the nodulation rate, and biological nitrogen fixation (Islam et al. 2021). Drought stress increases soluble sugars and reduces solute potential in nodule cells that maintain the turgor at a reduced water potential (Laxa et al. 2019). The lesser amount of water in the upper soil ensures deeper root penetration for gaining access to moisture, while excess water reduces the root penetration. Thus, increased root length and deeper penetration are among the adaptation strategies of plants during drought (Kim et al. 2020). Studies have shown that jasmonic acid and its derivatives regulate stomatal dynamics (de Ollas et al. 2013; Zhang and Huang 2013; Wang et al. 2020). Various strategies and bioactive agents are being adopted and explored globally for improving drought tolerancein a plant for better crop production, one such biological is melatonin.

18.3 Plant Microbiome Under Drought Stress Owing to the adaptable nature of microorganisms, they are present everywhere (Wani et al. 2022c). Plants tissues also dwell in bacterial, archaeal, and fungal communities. The plant-microbe association mediates plant health, and productivity (Wani et al. 2022d). The plant microbial consortia potentially respond to both biotic as well as abiotic stresses. Hence alterations in microbial communities present in different plant parts act as potential markers in sensing different

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environment-­induced stresses (Berard et al. 2015; Naylor and Coleman-Derr 2018; Schimel 2018). Xie et al. (2021) reported that hydraulic stress triggers a shift in the microbiome of the rhizosphere and changes functional categories in the gene pool. Drought stress that causes metabolism perturbations in plants also results in phytomicrobiome alterations with consequences for host fitness (Seleiman et al. 2021). Rhizosphere which is rich in microbial diversity experiences the impact of its microbiome with the reduction in soil moisture. Studies have shown the impact of drought on the rhizosphere microbiome (Xu et al. 2021; Song and Haney 2021). The endophytic bacteria recruited from the soil assist rhizosphere to tolerate drought stress by increasing the production of ABA, indole-acetic-acid, and aminocyclopropane-­ 1-carboxylic acid (ACC) deaminase (Akhtar et  al. 2022). Microbial communities help to withstand hydraulic stress by promoting nutrient uptake, increasing nitrogen fixation, and improving soil properties (Rashid et  al. 2016). Paenibacillus polymyxa has been studied to increase drought tolerance in A. thaliana by regulating ERD15 (Early response to dehydration 15) expression (Timmusk and Wagner 1999). Several studies have also suggested that the synergistic application of multispecies also helps in mitigating drought-induced negative effects through the formation of biofilms (Burmølle et al. 2014; Berendsen et al. 2018; Yang et al. 2021a). Since all the plant microbes are not culturable in the labs, it is always difficult to study the functional aspect of the plant-microbe association during different stress conditions. Metagenomics being a culture-independent tool for accessing bacterial diversity is emerging as a method of choice to study the underlying molecular mechanisms of gene functions in relation to plants (Handelsman 2004; Wani et al. 2022a, 2022f).

18.4 Melatonin and Its Role in Plants Under Normal Conditions Melatonin is a well-known plant growth regulator. It regulates seed germination and other developmental processes showing effects like auxins (Sun et al. 2021). The co-regulatory action of melatonin and auxin is also believed to play role in several physiological processes (Sharma and Zheng 2019). The varying concentrations of melatonin act as a rate-limiting step in the control of plant processes (Arnao and Hernández-Ruiz 2006). At high concentrations, it shows inhibitory effects whereas, at low concentrations, it acts as a growth promoter. Melatonin regulates rhizogenesis, caulogenesis, and morphogenesis (Debnath et al. 2019). Studies have reported that melatonin induces root primordia formation from pericycle cells (Chen et al. 2018). In another transcriptomic study, melatonin was reported to upregulate 121 genes of cucumber roots while downregulating 196 genes (Reiter et  al. 2015). Melatonin positively affects carbon assimilation, photochemical efficiency of photosystem II, accumulation of RuBisCO, protein content, catabolism of chlorophyll, senescence, glutathione (GSH) accumulation, and fruit ripening (Zuo et al. 2017).

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18.5 Melatonin Mediated Drought Stress Tolerance 18.5.1 Regulation of Oxidative Stress Melatonin guards plants from the adverse effects of water stress by increasing ROS scavenging efficiency (Kaur et al. 2015; Sharma and Zheng 2019). The process of ROS scavenging is attributed to melatonin triggered antioxidative defense mechanism of plants during drought (del Río et al. 2006; Khan et al. 2020). The drought-­ induced synthesis of superoxide anions is regulated by melatonin by increasing the scavenging or controlling the generation of superoxide anions (Huang et al. 2022). Figure 18.2 gives an overview of the melatonin-induced stress response. The scavenging ability of H2O2 is also improved by melatonin in plants under drought stress. This leads to enhanced detoxification of hydroxyl radials and aldehydes responsible for inducing oxidative stress (Cruz de Carvalho 2008). Melatonin-driven ROS scavenging also ensures plant cell wall protection under water deficit conditions. This is due to a reduction in electrolyte leakage and malondialdehyde levels (Aghdam et al. 2021; Ahmad et al. 2021). Plants under drought stress experience enhanced ABA biosynthesis which leads to more ABA accumulation than normal. This favors ROS generation causing electrolyte leakage, chlorophyll breakdown, and lipid peroxidation (Campos et  al. 2019). The proteomic studies have revealed that melatonin-­ treated plants in water-deficit environments exhibit a decline in ABA accumulation besides ROS reduction. This is attributed to the fact that melatonin down-regulates ABA biosynthetic genes while upregulating genes are responsible for ABA catabolism (Su et  al. 2019). Melatonin mediates the ROS generation via cytokinin and

Fig. 18.2  Melatonin induced drought stress response through ROS scavenging, antioxidative, and photosynthetic systems

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both function synergistically to mediate oxidative stress induced by drought. Table  18.1 highlights the impact of melatonin on plants during the drought. Overexpression of MzASMT gene (melatonin biosynthetic gene) in Arabidopsis ensures better drought tolerance and scavenging (Zuo et al. 2014). This is also supported by another research in which TaCOMT gene was overexpressed for improving drought tolerance (Yang et al. 2019). Table 18.1  Regulation of oxidative stress, antioxidative defense system, photosynthesis by melatonin in different plants during drought stress Plant Concentration Application Triticum aestivum 100 μM Increase in GSH accumulation, total GSH, and total ascorbic acid (AsA) Triticale 20 μM Increase in stomatal conductance, leaf hexaploide L. area, decrease in ROS, and malonaldehyde content Malus domestica 100 μM Reduction in chlorophyll degradation and suppression of senescence-­ associated gene 12 (SAG12) Camellia sinensis 0.4 mM Increase in stomatal conductance, L. intercellular CO2 concentration, and transpiration rate. Decrease in stomatal density Zea mays L. 100 μM Increase in photosynthetic efficiency by sustaining stomatal opening Zea mays L. 150 μM Reduced biomass accumulation, enhances ROS, and relative water content Agrostis 20 μM Down regulation of chlorophyllase stolonifera gene and maintenance of photochemical efficiency Pisum sativum 200 μM Increase in chlorophyllase activity and 5-aminolevulinic contents Brassica napus 50 μM Promotion of APX and CAT activity Avena nuda 100 μM Reduction in H202 and superoxode anions Vitis vinifera 100 nM Increase in the activity of SOD and POD Coffea arabica 300 μM Promotion of CAT and APX activity. No change in SOD activity Cucumis sativus 100 μM Reduction in hydroxyl radical, membrane lipid peroxidation, and H202 Lippia citriodra 200 μM Enhances super mutase, APX, and catalase activities. Protects photosynthetic pigments Solanum 100 μM Restoration of chlorophyll content, root lycopersicum L. architecture, and mitigation of antioxidant enzymes like APX, SOD, and POD

Reference Cui et al. (2017) Guo et al. (2022)

Wang et al. (2013)

Yang et al. (2022b)

Zhao et al. (2021) Ahmad et al. (2021) Ma et al. (2018)

Szafrańska et al. (2017) Gao et al. (2018) Zhang et al. (2022) Meng et al. (2014) Campos et al. (2019) Zhang et al. (2013) Hosseini et al. (2021) Altaf et al. (2022)

(continued)

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Table 18.1 (continued) Plant Gossypium herbaceum Solanum tuberosum Glycine max S. lycopersicum

Citrus latifolia, and C. aurantifolia Lolium perenne and Medicago sativa Oryza sativa L.

Concentration Application 100 μM Increase in osmotic substances by decreasing H202, MDA, and superoxide anion. 0.1 mM Decrease in MDA, ABA, SOD, APX and methylglyoxal 100 μM Reduction in ROS accumulation, and MDA 50 μM Down regulation of linoleic catabolic genes 150 μM

Reference Bai et al. (2020)

El-Yazied et al. (2022) Imran et al. (2021)

Mukherjee and Bhatla 2021; Yang et al. (2022a) Increase in total phenolic and flavonoid Jafari and content Shahsavar (2021)

100 μM

Increase in nitrogen and phosphorus content in leaves and roots

Wang et al. (2022)

300 μM

Enhances soluble sugar, proline, relative water and chlorophyll content

Silalert and Pattanagul (2021)

18.5.2 Regulation of Antioxidative Defense System The ROS level in plants during drought stress is regulated by stimulating the defense system of plants (Huang et al. 2019). Melatonin is known to trigger the plant defense system which mediates ROS scavenging thus reducing oxidative stress (Gu et al. 2022). As a multifunctional antioxidant, melatonin is a receptor-less free radical scavenger acting as an initiator of enzymatic anti-oxidative defense system (Tan et al. 2000; Siddiqui et al. 2021; Corpas et al. 2022). It has been reported that melatonin enhances the functioning of ABA degrading and H2O2 scavenging enzymes like chloramphenicol acetyltransferase (CAT), ascorbate peroxidase (APX), and peroxidase (horseradish roots)/POD (Zhang et al. 2016). The increase in the activity of these enzymes leads to H202 decline in guard cells, thus making the role of melatonin in H202 scavenging very clear (Moniruzzaman et al. 2018). Melatonin has also been reported to promote the activity of other anti-oxidative enzymes like glutathione reductase (GR), glutathione peroxidase (GPx), dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), and superoxide dismutase (SOD) (Palma et al. 2002; Begara-Morales et al. 2014; Talaat and Todorova 2022).

18.5.3 Regulation of Photosynthetic System Melatonin treatment to plants besides promoting plant growth also enhances chlorophyll content and relative water content for efficient photosynthesis during drought. It protects photosynthetic apparatus from the adverse effects of drought by

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preventing chlorophyll degradation thus ensuring smooth stomatal conductance, and transpiration (Khan et al. 2020). Pheophytinase, chlorophyllase, pheophorbide-­ a-­ oxygenase, and chlorophyll degrading peroxidase are the commonly known enzymes that mediate chlorophyll degradation (Yamauchi et al. 2004). Melatonin has been reported to down-regulate genes encoding these enzymes (Yang et  al. 2021b). Melatonin also helps in recovering photosynthetic performance in drought-­ stressed plants by recovering accessory pigments and by enhancement of non-­ photochemical quenching (Ding et al. 2017). The expansion of leaf surface area in melatonin-treated plants is another application associated with melatonin (Muhammad et al. 2022). The applicability of melatonin in enhancing photosynthesis during water deficit conditions is due to the protective role of melatonin in the chloroplast that prevents oxidative damage in leaves. Generally, drought stress causes a decrease in chloroplasts, damaging stroma lamellae, thylakoids, grana, and membranes. Melatonin is known to prevent plants from these adverse effects (Sharma et al. 2020). Melatonin has been studied to regulate carbon fixation, which helps in recovering photosynthetic performance during drought (Jahan et al. 2021). Melatonin upregulates essential enzymes of carbon fixation such as phosphoglycerate kinase, RuBisCO, phosphoribulokinase, and fructose bisphosphate aldolase (Huang et al. 2022). Table 18.1 gives an overview of the melatonin applications in mitigating drought-induced stress through photosynthetic components.

18.6 Melatonin Crosstalk with Other Plant Hormones During Drought Stress The endogenous synthesis of melatonin in transgenic A. thaliana improved drought tolerance by alleviating the oxidative stress-induced damage caused by the increased production of ROS due to drought stress (Wang et al. 2017b). Apart from the endogenous production of melatonin under drought stress, the exogenous application can also confer drought tolerance to plants. The prolonged exogenous application of melatonin in soil has been reported to delay leaf senescence, and alleviate oxidative damage and photosynthesis inhibition caused by drought stress in apples under long-term drought stress (Wang et al. 2013). Furthermore, melatonin can mediate the expression of different genes encoding enzymes and transcription factors related to the synthesis and catabolism of several plant hormones like IAA, gibberellic acid, brassinosteroids, jasmonic acid, cytokinin, and abscisic acid under drought conditions; thus implying potential crosstalk among melatonin and plant hormones under drought stress (Tiwari et al. 2021; Zeng et al. 2022). The modulation of the various plant hormones during drought stress by melatonin in plants could help in overcoming drought stress. Normally, drought stress increases abscisic content but melatonin decreases the abscisic acid content (Moustafa-Farag et al. 2020). Melatonin has been reported to decrease the abscisic acid concentration in drought-stressed Malus species to maintain stomatal function by down-regulating the gene involved in the abscisic acid synthesis and upregulating the gene involved in its catabolism (Li et al.

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2015). Similarly, in another study, the exogenous melatonin treatment of maize by soil drenching method under drought stress reduced abscisic acid content which has antagonistic to maize plants under drought stress by elevating abscisic acid catabolism (Ahmad et al. 2022). Another study also reported the exogenous treatment of maize seedlings via foliar spray under polyethylene glycol-mediated drought stress downregulated NCED1 gene (associated with abscisic acid synthesis) and upregulated genes such as ABA8ox1 and ABA8ox3 which are involved in abscisic acid catabolism thus decreasing abscisic acid content and promoting stomatal reopening (Li et al. 2021). The transcriptomic study of A. nuda under drought stress revealed that the melatonin treatment affected the genes that encode proteins such as Type 2C protein phosphatase, SnRK2, and PYL protein which are involved in abscisic acid signal transduction pathway (Zhang et  al. 2022). The transcriptomic study also reported that the melatonin treatment of A. nuda under drought stress induced the IAA (Indole-3-acetic acid) expression which can promote lateral root growth and help plants to absorb more water under drought stress (Zhang et al. 2022). Drought stress decreases IAA content but the foliar treatment of Moringa oleifera under drought stress with 100 mM melatonin increase IAA content in comparison to the drought-stressed plants untreated with melatonin (Sadak et al. 2020). Another transcriptomic study revealed that the melatonin upregulated the genes involved in auxin signal transduction and brassinosteroid biosynthesis pathway in Davidia involucrata seedlings under drought stress (Liu et al. 2021). 24-epibrassinolide, a brassinosteroid that helps plants to tolerate abiotic stress including drought stress was upregulated in Carya cathayensis plants exogenously treated with melatonin under drought stress (Sharma et al. 2020). Sharma et al, reported that the exogenous treatment of Carya cathayensis with melatonin conferred drought resistance by inducing crosstalk between melatonin and plant hormones where zeatin, gibberellin A14, and jasmonic acid were positively regulated, and abscisic acid was negatively regulated (Sharma et al. 2020). The exogenous application of melatonin to the transgenic Agrostis stolonifera expressing isopentenyl transferase gene under drought conditions upregulated the genes such as histidine phosphotransferase and histidine kinases which are associated with cytokinin synthesis and signalling (Ma et  al. 2018). Moreover, a possible synergistic association between melatonin and cytokinin has been also suggested in ameliorating drought stress-caused leaf senescence in Agrostis stolonifera (Ma et al. 2018). The exogenous melatonin application to the rhizosphere of soybean seedlings under drought conditions reduced abscisic acid content and increased jasmonic acid and salicylic acid accumulation which play important role in abiotic stress tolerance (Imran et  al. 2021). The pre-soaking of Gossypium hirsutum seeds with melatonin under drought stress increased the gibberellin acid content 4 days after germination in comparison to untreated seeds under drought stress suggesting gibberellin acid biosynthesis as a mechanism by which melatonin treatment could alleviate drought stress (Bai et al. 2020). The studies discussed in this section show that the crosstalk between melatonin and plant hormones plays an important role in conferring drought resistance to plants. The crosstalk provides drought resistance decreasing the abscisic acid content to

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promote stomata reopening and increasing the biosynthesis of gibberellin, jasmonic acid, salicylic acid, brassinosteroids, cytokinin, and IAA.

18.7 Conclusion and Future Perspective Drought poses a strong food security threat by adversely affecting plant growth, development, yield, and biomass. To combat these effects, different phytohormones play their role. These molecules play an essential role in building tolerance levels in plants growing under heavy metal, temperature, and drought stress. Melatonin safeguards plants from drought stress by enhancing ROS scavenging. This protects plant cells from oxidative damage by assisting in the recovery of chloroplast structure that improves photosynthetic efficiency. Melatonin-mediated-drought stress protection is regulated and stimulated by various metabolic pathways, but its exact mechanism of action is still obscure. Genome editing can emerge as a method of choice for researchers to build stress tolerance in plants. The identification and characterization of key drought stress-related genes can open new gateway towards sustainability. Conventional molecular breeding strategies in combination with genetic engineering have been effective in developing drought tolerance in plants, these methods are time-consuming and cumbersome. Plant breeders are shifting focus toward genome-editing technology for improving important traits. The advent of site-specific nucleases facilitates precise genome modification for resisting fluctuating environments (Wolter et al. 2019). Owing to the complexity of genome editing technology, there have been limited studies highlighting their contribution to developing drought stress-tolerant plants. CRISPR/Cas9 system has been successfully applied to animals and plants for inducing functional loss of specific genes (Jaganathan et al. 2018; Wani et al. 2022e). In Arabidopsis the CRISPR/Cas9 system was used to knock out open stomata gene 2 which leads to drought stress tolerance (Joshi et al. 2020). Similarly, mitogen-activated protein kinase (SIMAPK), and OsSAPK2 gene function loss were induced in tomato and rice for building drought resistance through ABA signaling using the CRISPR/Cas9 system (Lou et al. 2017; Wang et al. 2017a). It is known through genomic studies that variation in elite traits is mostly attributed to polymorphism or single-base modifications. For example, 77 single nucleotide polymorphisms (SNPs) are associated with at least 10 drought-­ responsive transcription factors (Villordo-Pineda et al. 2015). Since it is difficult to induce single base modification using CRISPR/Cas because the efficiency of the template DNA- dependent homology-directed repair method is lower than template-­ free non-homologous end joining in plants (Vu et al. 2020). Engineering plant for building drought tolerance involves the manipulation of several genes involved in different pathways. Thus, it is essential to target and modify genes concurrently. Multiple single guide RNA driven by independent promoters have been multiplexed into a single expression vector of CRISPR/Cas9 using the Gibson assembly method or Golden gate cloning (Zuckermann et al. 2018). The inefficient regeneration property of edited plants, off-target activities, and ethical issues are some of the major

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issues associated with CRISPR technology (Modrzejewski et al. 2020; Mir et al. 2022b). These challenges can be mitigated by the use of immature embryos, edited pollens, and strict guidelines. CRISPR will continue to transform agriculture by mediating the development of climate-resilient crops.

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Chapter 19

Potential, Mechanism and Molecular Insight of Melatonin in Phyto-Remediation Umair Riaz, Laila Shahzad, Muhammad Athar Shafiq, Muhammad Kamran, Humera Aziz, Muhammad Irfan Sohail, SaifUllah, and Ghulam Murtaza

Abstract  Melatonin act as a plant growth stimulator under plant stress condition. Various factors induce stress on plants like heavy metals accumulation, salt uptake, and environmental factors. Regarding environmental degradations, biosynthesis of melatonin causes remarkable indirect (stimulate plant metabolism by the anti-­ oxidation system) and direct (chelating heavy metals, scavenging free radicals) impacts in enhancing phytoremediation treatment. Melatonin has the ability to improve plant metabolism and produce resistance/tolerance in contradiction of stresses. Furthermore, studies gap still exit about the uptake, translocation, and gene pathways of melatonin during phytoremediation. This chapter covers all the aspects to understand the application of melatonin to achieve sustainability and more accuracy in phytoremediation against stresses. U. Riaz (*) Department of Soil and Environmental Sciences, MNS-University of Agriculture, Multan, Pakistan e-mail: [email protected] L. Shahzad Sustainable Development Study Center, GC University, Lahore, Pakistan M. A. Shafiq Department of Botany, Faculty of Life Sciences, University of Okara, Okara, Pakistan M. Kamran Department of Agronomy, University of Agriculture, Faisalabad, Pakistan H. Aziz Department of Environmental Sciences and Engineering, Government College University Faisalabad, Faisalabad, Pakistan M. I. Sohail Department of Environmental Sciences, Faculty of Life Sciences, University of Okara, Okara, Pakistan SaifUllah · G. Murtaza Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, Pakistan © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 S. Mukherjee, F. J. Corpas (eds.), Melatonin: Role in Plant Signaling, Growth and Stress Tolerance, Plant in Challenging Environments 4, https://doi.org/10.1007/978-3-031-40173-2_19

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Keywords  Stress resistance · Molecular changes · Abiotic · Cell biology · Metal extraction

19.1 Introduction and Background History In mammals, reptiles, fish, and plants, melatonin is a hormone that regulates sleep (Hardeland et al. 2011). Plants generate Melatonin, which regulates the body’s biological clock. A healthy immune system and protection from cell damage caused by free radicals are just a few of the benefits of taking this supplement daily (Calvo et al. 2013; Hardeland et al. 2012). Amphiphilicin has been shown in studies by (Byeon and Back 2013; Galano et al. 2013) to penetrate cell membranes and reach subcellular locations. As the plant matures and changes genotype, temperature, and stage, the quantity of melatonin it produces will also change. Melatonin stimulates both SNAT and HIOMAT/ASMT (Byeon and Back 2014a). Melatonin has the potential to impact a variety of biological processes, including flowering, chlorophyll synthesis, root regeneration, and the withering of leaves (Wei et al. 2015; Zhang and Zhang 2014). Melatonin, also known as N-acetyl-5-methoxytryptamine, is produced from the amino acid tryptophan and functions as a potent antioxidant in plants. In reaction to abiotic stressors, such as heavy metals and metalloids, it activates the defense systems of plants. Melatonin is generated from the amino acid tryptophan (Sami et al. 2020; Xu et al. 2020). In plant tissues, melatonin functions as a reactive oxygen species (ROS) scavenger, an anti-stress mediator, and an anti-­oxidant, thereby preventing tissue damage. (Sharma et al. 2020). Several writers have published studies into M’s defense mechanisms in brassica plants (Ayyaz et al. 2020, 2021; Farooq et al. 2022; Banerjee and Roychoudhury 2019). Figure 19.1 represents the general mechanism of heavy metal uptake and its translocation in plants. Melatonin lowers nickel toxicity in tomato plants by regulating its sequestration in vacuoles and conversion to secondary metabolites (Jahan et al. 2020). Farooq et al. (2022) and Siddiqui et al. (2020) employed Se-M nanoparticles and M-sulfur synergy to protect rape and tomato plants from the detrimental effects of lanthanum and arsenic. Exogenous melatonin enhanced the development of heavy metal-­ stressed plants e.g., Galinsoga parviflora, Cyphomandra betacea, and Malva parviflora. There were increases in biomass, photosynthetic activity, and antioxidant capacity (Tang et  al. 2018a, 2020; Xiang et  al. 2019). Some plant species exposed to melatonin had chronically elevated levels of melatonin synthesis, stress-­responsive genes, and redox network regulator genes (Ahn et  al. 2021; Debnath et al. 2020). Chemically melatonin is a member of acetamides, it is formed by replacing the Hydrogen ion of acetamide nitrogen with 2(−5-­methoxy-­1H-­indole-­3-­­yl) ethyl group. Thus, melatonin is chemically N-Acetyl-5-methoxytryptamine, N-[2-(5-Methoxy-1H-indol-3-yl) ethyl] acetamide, formulae are C13H16N2O2 and molecular weight is 232.28. Primary role of the melatonin is to decontaminate the ROS and reactive nitrogen species (RNS) generated from oxidative metabolism (Galano et al. 2018; Manchester

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Detoxification Glutathione reductase Chloroplast of O-1 and -Tocopherol, Melatonin

Detoxification Antioxidant defense Mitochondria by Glutathione and of ROS Melatonin

Signal transduction

Vacuole

Compartmentalization of heavy metal ions

Heavy metal sequestration

Up-regulation ROS scavenging

Nucleus of Defence genes

Root

Acidification Chelation Redox reaction

Phytoremediation

Heavy metal up take

Fig. 19.1  The schematic representation of HMs uptake as well as translocation in plant stream, along with plant responses to mitigate the stress (Feng et al. 2021)

et al. 2015) along with this melatonin also behave as pleiotropic molecule and also influence biological rhythms and suppress inflammations (Tamtaji et al. 2019). The pineal glands of cows were the first to be shown to contain melatonin in 1958. It is the ancestor of the melanophores seen in fish and other animals (Lerner et al. 1958). Melatonin was shown to be prevalent in plants in 1995 (Dubbels et al. 1995; Hattori et al. 1995). In 2003, melatonin was found in 108 distinct Chinese medicines. Plant tissue contains hundreds of milligrams of melatonin per gram, ranging from nano-­ gram levels (Chen et al. 2003). These differences imply that melatonin has a distinct purpose in plants compared to mammals.

19.2 Metabolism of Melatonin Tryptophan is the first substrate used in the four enzymatic steps that create melatonin (Back et al. 2016). Some key proteins implicated are (TPH, TDC, T5H, SNAT, ASMT, and COMT). Five enzymatic transcripts, excluding TPH, have been identified (Kang et al. 2011; Byeon et al. 2013; Fujiwara et al. 2010). TDC first decarboxylases tryptophan in the cytoplasm to yield tryptamine, which is then hydroxylated by T5H in the endoplasmic reticulum to produce serotonin (Kang et  al. 2007). Tryptophan may be hydroxylases in the cytoplasm by one TPH (unidentified) to make 5-hydroxytryptophan, which is subsequently decarboxylase with TDC to produce serotonin (Park et  al. 2009). Serotonin in the chloroplast is changed by the enzymes SNAT and ASMT into N-acetyl-serotonin as well as 5-methoxytryptamine inside the cytosol. Melatonin is synthesized in the cytoplasm and chloroplasts by

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Tryptophan (chloroplast)

TDC

ROS Detoxification

Tryptamine

Compartmentalization

Sertonin

AC-CoA

5-methoxytryptamine

CoA

Signal Transduction

Melatonin-mediated response

TSH

ASMT/COMT

PCs Chelation

Melatonin

Fig. 19.2  Melatonin synthesis pathway, signal transduction and biological response to detoxify the deleterious effects of heavy metals ions in plant. The enzymes which catalyze the reactions are T5H (tryptamine-5-hydroxylase), TDC (tryptophan decarboxylase), ASMT (N-acetyl serotonin methyltransferase), ASMT (N-acetyl serotonin methyltransferase), COMT (acetyl serotonin O-methyltransferase), COMT (acetyl serotonin O-methyltransferase) and SNAT (serotonin N-acetyltransferase)

enzymes known as ASMT and SNAT (Park et al. 2013; Kang et al. 2013). ASMT and COMT are both enzymes required for plants to produce phyto-melatonin in their cytoplasm (Byeon et  al. 2014). Figure  19.2 depicts the routes of melatonin biosynthesis in plants.

19.3 Stress-Related Melatonin Accumulation Bioactive melatonin enzyme levels rise in response to temperature, cold, dryness, salt, oxidative damage, heavy metals, or pathogenic microbes (Hardeland 2016; Shi et al. 2016). When a plant is stressed, gene expression and enzyme activity of melatonin synthesis and catabolism candidates are directly linked. This increases phyto-­ melatonin. Melatonin synthetases (TDC, T5H, and ASMT) are activated by cadmium in rice (Byeon et al. 2015). Higher temperatures boost SNAT and ASMT activity, which increases melatonin synthesis in rice (Byeon et al. 2013). How melatonin predicts stress is unknown. HsfA1a and COMT1 interactions enhance tomato melatonin during Cd stress (Cai et al. 2017). Molecular compositions make precursors more accessible (Hardeland 2016). ASMT/COMT and SNAT had less catalytic

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effectiveness than TDC and T5H, hence increasing serotonin in the melatonin synthesis pathway did not enhance melatonin levels, despite what some researchers expected. Past research employed plants or HIOMT, the animal analogue of ASMT, with low activity of the stress-tolerant SNAT/ASMT gene to determine whether phyto-melatonin provides stress tolerance in plants. Serotonin helps low-­temperature rice resist stress (Kang et al. 2010). Cold and drought may have enhanced rice’s stress-resistance (Byeon et al. 2015; Lee et al. 2016). Bioactive melatonin promotes enzyme synthesis in response to cold, frost, drought, salt, oxidative damage, heavy metals, or pathogenic microbial invasion (Hardeland 2016; Shi et al. 2016). Enzymes help manage stress. Strong links exist between melatonin synthesis and catabolism during stress, as well as gene expression and enzyme activity. Melatonin synthetases (TDC, T5H, and ASMT) are involved in cadmium-induced melatonin synthesis in rice (Byeon et  al. 2015). Temperature increases stimulated rice’s melatonin synthesis through modifying SNAT and ASMT enzyme activity (Byeon et  al. 2013). How melatonin predicts stress is unknown. HsfA1a and COMT1 interactions enhance tomato melatonin during Cd stress (Cai et  al. 2017). Molecular compositions make precursors more accessible (Hardeland 2016). Contrary to expectations, increasing serotonin in the melatonin pathway does not enhance melatonin levels. ASMT/COMT and SNAT are less catalytic than TDC and T5H (2012). In prior investigations, phyto-stress-­ relieving melatonin’s effects were examined. Melatonin increases plant stress tolerance via altering SNAT/ASMT in plants or HIOMT in animals. Serotonin helps low-temperature rice resist stress (Kang et al. 2010). Cold and drought may have enhanced rice’s stressresistance (Byeon et al. 2015; Lee et al. 2016).

19.4 Melatonin Modulated Signal Transduction to Induce Stress Tolerance Recently, Arabidopsis G-protein component GPA1 was shown to be linked to melatonin receptors in the plant. The CAND2/PMTR1 signal transduction pathway modulates stomatal closure, which in turn affects the generation of H2O2 (Arnao and Hernandez-Ruiz 2019a). It also controls PIN1, PIN3, and PIN7, all of which are auxin transporters. Melatonin has an impact on the ASC-GSC cycle, fatty acid metabolism, the TCA cycle, and the production of myo-inositol (Zhang et al. 2017a; Turk and Genisel 2020). IAA and melatonin have the same metabolic process (Arnao and Hernandez-Ruiz 2019a, b). A study by Farouk and Al-Amri (2019) discovered that melatonin supplementation lowered the expression of the genes CLH1, HXK1, and PAO (a critical gene for chlorophyll breakdown) in As-treated rosemary plants. An increase in EO production and plant biomass production were both stimulated by auxin receptor interaction as a result, melatonin makes HM-treated plants feel less stressed (Farouk and Al-Amri 2019). There has been researched linking plants’ response to heavy metals (HMs) stress to hormones and signaling molecules

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for example brassinosteroids, axing (IAA), abscisic acid (ABA), and others (Menhas et al. 2021; Khalid et al. 2017; Gu et al. 2021). Melatonin-mediated processes are metal remediation, ROS scavenging and redox metabolism and sequestration at the root level, modulation of electron transport flow, alteration of endogenous antioxidants and hormonal balance, boosting proline thresholds and regulating carotenoids. The observed variances in plant response caused by melatonin support its metal tolerance capacity in situations of multi-metal stress. Endogenous regulators of physiological and molecular responses to HM stressors such as phytohormones have been identified as significant players (Hasan et al. 2018; Lee et al. 2017). The genetic development of plant tolerance to HMs depends on a clear understanding of the molecular processes that underlie hormonal homeostasis and their stress signaling network. The cellular and physiological roles of melatonin, a signal molecule found in both animal and plant kingdoms, are diverse. (Debnath et al. 2018; Kanwar et al. 2020).

19.5 Melatonin Turns Up Genes for Defense Oxidative damage, protein kinase activation, and hormonal signaling are all promoted by HMs (Kumar and Trivedi 2016; Dubey et al. 2014). Signal transduction genes are impacted by melatonin. Gene expression or antioxidant enzyme activity may be boosted by HM stress (Zhao et al. 2017; Zhang et al. 2017a, b). Treatment of watermelon seedlings with melatonin and vanadium (V) stress resulted in an increased SOD/APX/GPX expression (Nawaz et al. 2018). Plant HM toxicity may be reduced by increasing the synthesis of metal-binding peptides (PCs, phytochelatins) (Pál et al. 2018). Melatonin and GSH both increased the proportion of PC in safflower seedlings that were subjected to zinc deficiency, which may be explained by the fact that melatonin has a role in initiating the production of PC-encoding genes transcripts (Goodarzi et al. 2020). Cd transporters were made more active by melatonin. Transporters of cadmium include YSL2, ZIP12, HMA4, and YSL7 (yellow stripe-like transporter 7). Additionally, melatonin enhanced the ATP-dependent expression of the CAX4 gene, which encodes the vacuolar cation/proton exchanger 4. The efficiency of photosynthesis is increased as a result of melatonin’s ability to promote gene expression for chlorophyll production. In the presence of Ni stress, seedlings that had been treated with melatonin expressed the genes CHLG, POR, and CAO (Jahan et al. 2020). During times of V stress, melatonin causes a rise in the quantity of chloride (Chl) in watermelon by causing a change in the amount of mRNA that is produced by the Chl biosynthetic gene (Nawaz et al. 2018). Since these transcripts are required for stress signaling in HM in the presence of melatonin, it’s safe to assume that the two function in harmony together. This is because the HM stress response depends on these specific genes.

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19.6 Melatonin-Induced Differentially Expressed Genes (DEGs) Stress enhances endogenous melatonin by increasing biosynthetic enzyme transcripts (COMT, SNAT, TDC, and ASMT genes). Arnao and colleagues (Arnao and Hernandez-Ruiz 2013) studied lupin, tomato, and barley melatonin levels. Cherry fruits (Zhao et  al. 2017), water hyacinth (Tan et  al. 2007), grape berry skin (Boccalandro et al. 2011), and showed it initially. Salinity, cold, drought, and heavy metals promote melatonin biosynthesis. Pathogens produce melatonin. This stress response upregulates stress genes and strengthens the redox network against ROS and RNS.  This boosts plant growth, photosynthesis, water use, and metabolism while lowering stress-related inhibition (Arnao and Hernandez-Ruiz 2019a, b). Using plants that are resistant to poisons and biomass to clean. Melatonin’s effects on biomass and antioxidant defenses are enhanced by strong primary and secondary metabolism and plant hormone stress responses. Melatonin sustains and/or accelerates photosynthesis by activating photosystems, electron transporters, and ATPase genes. Melatonin enhances CO2 availability by changing dehydrins and guard cell anion channels. Carbohydrate inter-conversion is influenced by Melatonin. Myo-­ inositol, ASC-GSH, and TCA synthesis are all affected by melatonin. Carbohydrates, amino acids, and organic acids are all enhanced in melatonin-treated plants. Blood sugar, lipids, protein and nitrogen, phosphorus, and sulfur metabolism are all affected by stress and flavonoids and anthocyanins are influenced by melatonin (Liang et al. 2018a). It affects gibberellins, auxin and cytokinines as well as ABA and jasmonic acid (SA), and brassinosteroid (Arnao and Hernandez-Ruiz 2018).

19.7 Melatonin Mediated Antioxidant Defense System Hydrogen peroxide (H2O2), and free oxygen radicals i.e., O2•-, and •NO are formed in plants as a result of HM stress (Savvides et al. 2016; Chan and Shi 2015). Cell membranes, RCS (MDA), and lipid peroxidation are all affected by HM free radicals (Kaciene et al. 2017; Wang et al. 2010). Oxidative stress is reduced by melatonin, according to studies. Tweaking plant antioxidant capacity and protein production (Cu/Zn-SOD, POX, GPx) lower the toxicity of hydrogen peroxide in plants (Nabaei and Amooaghaie 2019). Ni stress elevated PAL, CHS, POR, CAO, and CHL, chlorophyll synthesis genes, and melatonin biosynthesis genes ASMT, TDC, SNAT, and T5H in melatonin-treated tomato seedlings. Anti-oxidative enzyme activity to eliminate excessive ROS was improved by positive regulation of the chlorophyll and melatonin genes (Nawaz et  al. 2018; Gong et al. 2017). When exposed to Cu, Al, Pb, Fe, V, Cd, and Zn, watermelon, cucumber, wheat, tomato, and mustard have improved anti-oxidative activity (Sami et al. 2020). When plants are under stress, their production and removal of ROS are affected. Antioxidants protect plants against harm and the formation of ROS (Mittler

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2017; Li et al. 2018a). Plants are better able to withstand stress when ROS levels are reduced by melatonin (Reiter et al. 2016). By increasing POD and SOD activity and gene transcription levels, melatonin may boost the antioxidant system in plants that scavenges ROS and decreases oxidative stress in cucumbers when there is a lack of Fe (Ahammed et al. 2020). For example, (Ni et al. 2018; Wu et al. 2021; and (melatonin improved ROS scavenging)) (Cao et al. 2019). Anthocyanins and GSH are also boosted by the addition of exogenous melatonin. Tocopherols and thiols are also increased (Shi et al. 2019; Zhao et al. 2017). Scavenging ROS from HM boosts melatonin’s ability to withstand stress.

19.8 Heavy Metal Stress and Enzymatic Antioxidants When exposed to metal stress, plants utilize antioxidant enzymes to detoxify free radicals. The majority of antioxidants give electrons and produce benign compounds the antioxidant enzyme’s active site attracts free radicals, which then create water and molecular oxygen. Superoxide radicals are dismutase by SOD and converted to H2O2 (Abbas et al. 2017). An extremely dangerous ROS that swiftly diffuses through macromolecule membranes and harms biological components is hydrogen peroxide (Rafique et al. 2018). Plants contain Cu, Zn-SOD in the cytosol or chloroplast, and peroxisome, Fe-SOD in the chloroplast, and Mn-SOD in the mitochondria and peroxisomes (see note). H2O2 created by SOD is catalyzed by CAT and APX.  H2O2 is changed by catalase into water and oxygen. Ascorbate is used by APX to change H2O2 into water and molecule oxygen. APX is a maintenance protein found in the cytosol and chloroplast. APX is fed by ascorbate. Ascorbate is converted to dehydro-ascorbate by MDHAR and NADPH. A variety of studies have discovered changes in antioxidant enzymes brought on by heavy metals.

19.9 Mitigation of Heavy Metal Stress by Exogenous Melatonin Melatonin may increase plant growth indices by mitigating the harmful effects of HM stress. Exogenous melatonin therapies have been found in studies to be effective in reducing the harmful effects of a variety of HMs, including cadmium, zinc, arsenic, iron, copper, lead, aluminum, and nickel. Exogenous melatonin improves plant systemic resistance to heavy metals by improving photosynthetic efficiency antioxidant enzymes, and metabolite concentration. This is accomplished by scavenging ROS. Maintaining the photosynthesis system of Chinese cabbage in the face of Al stress was enhanced by using melatonin (Tang et al. 2017).

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Melatonin reduces the negative effects of Al on soybean plants. Soybean roots were treated with melatonin, which boosted citrate and malate exudation and decreased Al-induced H2O2 concentration (Zhang et al. 2017a, b). By boosting non-­ protein thiols and phyto-chelating (PCs), foliar melatonin increased hydration status, plant growth, and As stress tolerance in rosemary under As stress (Farouk and Al-Amri 2019). Melatonin boosted rice seedling biomass in both the underground and the aboveground regions. When rice plants were exposed to Cd stress, SOD and POD levels increased while MDA levels declined (Lv et  al. 2019). Melatonin reduced Cd accumulation and restored ROS equilibrium in alfalfa seedlings when subjected to Cd stress (Gu et al. 2017). Tobacco plants become more resistant to Cd by reducing Cd deposition, growth inhibition, and photoinhibition using melatonin (Wang et al. 2019). In tobacco plants, oxidative damage was minimized by melatonin because it directly scavenged ROS (Wang et  al. 2019). When melatonin was administered to Cd-stressed plants, apple rootstalk growth, photosynthesis, enzyme activity, and the generation of ROS and MDA all increased. Exogenous melatonin influenced the expression of PM H+ HA7-ATPases 7/NRAMP3/NRAMP1 HMA4/ plant Cd resistance protein 2 / nicotiana mine synthetase 1 / metallothionein 2 / and ATP-binding cassette transporter. These findings imply that melatonin is involved in controlling the mechanism in plants responsible for heavy metal transport. Cucumber seedlings were given melatonin therapy, which enhanced leaf area, decreased growth inhibition, and reduced severe Cd toxicity, as well as other photosynthetic process-related parameters (He et al. 2020).

19.10 Melatonin Bioassay The genes transcribe the enzymes that potentially catalyze different biosynthetic routes of mechanism are engaged to control the melatonin synthesis by separating the active sites of subcellular localize reactions (Sun et al. 2016; Zhang et al. 2021a). In plants, mitochondria and chloroplast provide a reaction system to convert L-tryptophan into melatonin synthesis (Zhao et al. 2021) under normal as well as stressful environments (Agathokleous et  al. 2019). Under normal circumstances, L-tryptophan is carboxylated into tryptamine in presence of L-tryptophan decarboxylase in the cytoplasm furthermore, tryptamine transformed in serotonin catalyzed by tryptamine-5-hydoxylase on the endoplasmic reticulum. The third step is the transformation of serotonin in N-acetyl serotonin by serotonin N-acetyltransferase (SNAT) in the chloroplast. Consequently, N-Acetyl serotonin methyltransferase (ASMT) concludes the final step and converts N-acetyl-serotonin into melatonin inside the cytoplasm. Besides, during an episode of heavy metal stress, the plant instantly accumulates serotonin in cell and introduce ASMT to transform it into methyexytryptamine, which is further converted to melatonin by SNAT (32). The last step of the reaction is accomplished by the formation of S-adenosyl-L-­ homocysteine (SAH) from S-adenosyl-L-methionine (SAM; Ma et al. 2017).

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19.11 Signal Transduction Afterward, melatonin involves in signal transduction as well as an antioxidant defense system in ensuring stress tolerant plant species from germination to maturity (ElSayed et al. 2015) by up-regulating stress-responsive genes which encode and run an antioxidant defense system to scavenge ROS under abiotic stresses. Overexpression of MzASMT9 gene increases melatonin biosynthesis and the interaction of Ca2+ and melatonin is intricate to overcome ionic, osmotic, and oxidative imbalances in plants by long- distance signal transduction to activate stress-tolerant mechanisms (Vafadar et al. 2020; Zheng et al. 2017). The onset of abiotic stress, triggers the interaction of Ca and melatonin (CaM) which transduce long-distance signaling and activate tolerance mechanism to overcome heavy metal toxicity, sodium toxicity, osmotic injury, and cellular membrane damage in the plant (Vafadar et al. 2020). Zheng et al. (2017) observed high expression of the MzASMT9 gene which elevates melatonin levels in Arabidopsis. Furthermore, the higher level of melatonin triggers the plant’s defense system against stress by detoxifying ROS, arresting lipid peroxidation, and continuing photosynthesis (Zheng et al. 2017).

19.12 Phytoremediation Potential of Melatonin Biotic or abiotic stressors are toxic in biological systems and phytoremediation is the vastly used technology against stresses for treatment because of plant’s take up, low biomass, eco-friendly and cost-effective properties. Hyper-accumulators are plants most effectively used for this purpose as they have the property to accumulate metals and other stressors in their shoot, then leaves, roots, etc. They are up to 1000 times more effective in the uptake of zinc (Zn), copper (Cu), lead (Pb), nickle (Ni), cobalt (Co), manganese (Mn), etc. than non-hyperaccumulator (Sheoran et  al. 2011). Phytoremediation works with different mechanisms like concentration, translocation, accumulation, distribution, exclusion, and osmoregulation by various processes like, phyto-filtration, phyto-desalination, phyto-volatilization, phyto-­ stabilization, rhizofiltration, phyto-degradation, phyto-extraction (Bhargava et  al. 2012; Marques et al. 2009). Melatonin (MEL) was initially detected and isolated only in animals but in the early 1990s, scientists explore the presence of Gonyaulax polyedra also known as Lingulodinium polyedrum in dinoflagellate and in mid-­1990s the scientist detected MEL in mono-cotyledon and di-cotyledon plants groups (Janas and Posmyk 2013). Tryptophan, tryptamine, and melatonin are structurally indoleamine that is indole-3acetic acid (IAA), as important in plant physiology as auxin (Nawaz et al. 2016). In plants, under stress, the resilience mechanism activates, tryptophan decarboxylase (TDC) converts the amino acid tryptophan into tryptamine which is the precursor of melatonin N-acetyl-5-methoxytryptamine (MEL) (Zhao et al. 2018). Under stress conditions, MEL behaves as a free radical to hunt reactive molecules. It readily scavenges reactive nitrogen species (RNS) and

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reactive oxygen species (ROS) such as peroxynitrite, hydroxyl radical, hydrogen peroxide, peroxynitrous acid, nitric acid, hypochlorous acid, etc. (Romero et  al. 2014) This depicts MEL an in-vivo anti-oxidant compound, four to six times stronger than vitamin E and C (Arnao 2014). Another feature of melatonin is it is an amphiphilic (Arnao and Hernandez-Ruiz 2015, 2019a, b) compound, allowing it to pass through the cell membrane and crosses morphophysiological barriers (Tarocco et al. 2019). Melatonin also has the capability to change the expressions of major genes that take part in physiological behavior (Waeeda et  al. 2014). Table  19.1 shows the endogenous and exogenous-based melatonin resistance in different stress

Table 19.1  Oxidative damages induced by different HMs on plant and strategies of plants to mitigate HM stress by biochemical and physiological alteration Heavy metal Oxidative damage Cd Oxidative damage, chlorosis and stunted growth Pb

Chloroplast disruption, Electron transport and Calvin cycle inhibition, impaired enzymes and lowered essential elements uptake, for instance; Mg, Fe, and deficiency of CO2 resulting from stomatal closure

As

Decreased ratio of reducing and non-­ reducing sugars in rice shoots, suppressed sucrose synthesis concerned with available hexose monophosphate up regulated activities of sucrose-hydrolyzing enzymes for example, acid invertase and sucrose synthase

Biochemical alterations Inhibition of photosystem II due to ceased electron transfer Photosynthetic inhibition, ceased mineral nutrition, reduced water balance and enzymatic activities ATP inhibition, lipid peroxidation, ROS related DNA damage. Inhibits seed germination, radicle elongation, seedling development, transpiration, plant growth, chlorophyll production, and H2O and protein content. ROS generation such as SOD radical (O2−), hydroxyl radical (OH), and hydrogen peroxide (H2O2), lipid peroxidation

Physiological damage Reduced photosynthesis and stomatal density

Reference Shaw et al. (2004)

Rapid root inhibition Pourrut and growth, et al. (2011) underdeveloped plant growth, root blackening and chlorosis

Reduction in root and shoot length, chlorophyll degradation, restricted stomatal conductance and nutrient uptake, limited biomass and yield

Abbas et al. (2018)

(continued)

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Table 19.1 (continued) Heavy metal Oxidative damage Ni ROS generation High MDA content

Hg

Cu

Cr

Al

Cell membrane permeability changes, reactions of sulfhydryl (-SH) groups with cations, Phosphate affinity with phosphate groups and active groups of ADP or ATP Less photosynthetic carotene pigments

Biochemical alterations Oxidative damage, Suppression of growth, nutrient uptake, antioxidant enzymes activity, and translocation Effect on aquaporin proteins and disturbs the water relations

Physiological damage Reference Inhibition of growth, Amjad et al. induction of (2019) chlorosis, necrosis and wilting

evokes extreme phytotoxicity and impaired numerous metabolic processes including nutrient uptake, water status, and photosynthesis

Chen and Yang (2012)

The inhibition of PSII and photosynthetic light reactions as well as oxidative stress Enhanced production of ROS, decreased seed germination, decreased leaf area

Nutritional imbalances and constraints to plants growth increased ROS generation and oxidative stress, as well as suppression of pigment formation and alteration of nearly all cellular components

Feil et al. (2020)

Low carotenoids and anthocyanins, disruption of chloroplast ultrastructure, suppression of chlorophyll synthesis, inhibition of photosynthetic electron transport, and release of magnesium ions from the molecule of chlorophyll Stimulation of nitrate Nutrient uptake reductase and a rise in NO3- absorption and buildup of P in plant roots and leaves

Stambulska et al. (2018)

limits root Bojórquez-­ elongation and has a Quintal negative impact on et al. (2017) plant growth

conditions. During phytoremediation, melatonin not only behaves as an anti-­ oxidative agent but also as a redox regulator (Zhou et al. 2016). Under environmental stress conditions, like, waterlogging, higher temperatures, bacteria, viruses, alkalinity, fungi, salinity, metal presence, mineral excess, mineral deficiency, toxicity, etc., melatonin behave as a biostimulator and help to resist extreme condition and promote growth (Huang et al. 2019). During phytoremediation, the application of exogenous melatonin activates the antioxidative mechanism, produces tolerance against stressors, and reduces the inimical affects produced by the formation of ROS and RNS in plants (Tang et al. 2018). MEL also has the potential to mobilize toxic metals by phytochelatins, form chelates reducemetal-induced toxicity, and enhance the plant resistance against toxic metallic components (Hoque et al. 2021).

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Fig. 19.3  Melatonin potential of phytoremediation

Not only this, but melatonin also works effectively in stress conditions and improves cell metabolism by boosting the uptake of sulfur, phosphorus, and nitrogen. As a natural response, endogenous stress-induced melatonin is produced in hyperaccumulators to enhance the activity of phytoremediation by plants, however, the exogenous MEL also improves the activity of phytoremediation to clear toxicity from the environment (Fig. 19.3) (Asif et al. 2019).

19.13 Biosynthetic Pathways of Melatonin Under Metal Stress Condition A certain concentration of heavy metals is the need for the plant to grow, like iron (Fe) used in photosynthesis, zinc (Zn) used in plant growth regulation, copper (Cu) used in activating enzyme systems, etc. However, some heavy metals like cadmium (Cd), lead (Pb), arsenic (As), etc. are not necessary for any plant process, in fact, they are hazardous to the plant processes (Riaz et al. 2021; Arif et al. 2016). If the limit exceeds a certain level, it will create a hindrance in plant metabolism (Chibuike and Obiora 2014). The primary action after the intensification of heavy metals is the production of ROS in mitochondria, peroxisomes, and chloroplasts (Yu et al. 2018).

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Fig. 19.4  Phyto-melatonin activation, synthesis, and mediation against heavy metals

It enhances the oxidative stressors; it causes toxicity of heavy metals in plants. In effect, the stomata closure happened, ROS increases, the photorespiratory phenomenon triggers and the anti-oxidant system interjects, ultimately obstructing plant metabolism and the electron transport chain (Rucińska-Sobkowiak 2016). Not only this, but the heavy metal-induced ROS also causes lipid peroxidation which causes the degradation of the cell membrane, hence hindering the function and integrity of the membrane (Janicka-Russak et al. 2008). Heavy metals not only disrupt the normal cycles of plants but also affect the plant growth processes from germination to final production. On exposure to heavy metals, the roots are the first element to confront stress, primarily disturbs nutrient absorption and transportation, and causes the decline in the chlorophyll of leaves, hence a decrease in CO2 assimilation rate. This inhibits the absorption of light, disturbs ETC, and the opening and closing of stomata. The stomatal closure system thus disturbs by blocking ion and water channels, restricts guard cells and affect the movement of stomata. The whole process disturbs the redox homeostasis of the cell and starts producing ROS and RNS, damaging the cell biomolecules and start causing cell death (Ghori et  al. 2019). Figure  19.4 depicted the factors that start activating melatonin production and melatonin-­mediated actions against heavy metals (Tables 19.2 and 19.3). Under heavy metal stress toxicity, the production of phyto-melatonin as an anti-­ oxidant defense mechanism activates, depicting the function of MEL as a stress response. This biosynthesis of MEL after exposure of metals occurs in four enzymatic steps. Tryptophan and six enzymes, TPH (tryptophan hydroxylase), TDC (tryptophan decarboxylase), T5H (tryptamine 5-hydroxylase), SNAT (serotonin N-acetyltransferase), ASMT (N-acetylserotonin methyltransferase), COMT

Table 19.2  Melatonin-mediated physiochemical responses in plant cells to alleviate stress induced by different types of heavy metals Heavy metal Gene up regulation Cd COMT (caffeic acid O-methyltransferase) Overexpressing crops having sulfate transporter (SUT)1 and SUT2 gene suppression, Pb Pb_50MT and Pb200

As Ni Hg

Cu Cr

Al

Biochemical changes Decreased Sulfur accumulation and aggravated Cd phytotoxicity

Physiological changes Improve plant growth and Cd tolerance

Highest genome-­ wide methylation level

Lead sequestration into vacuoles via complex formation; lead binding via phytochelatins, glutathione, and amino acids; and osmolyte synthesis Genes responsible for Increased Increased seed and plant antioxidants encoding antioxidant activity growth Genes responsible for Increased Increased seed and plant antioxidants encoding antioxidant activity growth auxin-related Scavenging ROS In addition, activation of transcription factors (e.g., and RNS various antioxidants to WRKY, NAC, MYB, combat increased bHLH, and HD-ZIP production of lead-­ induced ROS constitutes a secondary defense system. P transporter genes (i.e., Nullify oxidative Optimal growth as well CsPT1.4 and CsPT1.9) damages as development in plants ROS scavenger induced senescence Increased primary responsible genes showed improved photochemistry (qP) and efficiency of PSII decreased non-­ with decrease in photochemical energy dissipation quenching as heat (ΦD) ROS and RNS scavenger Scavenging ROS Increased seed and plant responsible genes and RNS growth

Reference Hasan et al. (2018)

Pourrut et al. (2011); Zeng et al. (2022)

Zhang et al. (2015a) Zhang et al. (2015a) Pourrut et al. (2011)

Feil et al. (2020) Feil et al. (2020)

Zhang et al. (2015a)

Table 19.3  Melatonin-based stress resistance in different plant species Stress conditions Heat Cold stress

Pathogen Salt Heavy metal

Plant species Solanum lycopersicum chrysanthemum seeds Camellia sinensis L., Bermuda grass Rice leaves Arabidopsis thaliana Rice plant Crimson seedless grape vine Triticum aestivum L. Oil seed crops Solanum lycopersicum

Melatonin application Endogenous Exogenous Exogenous Endogenous Endogenous Exogenous Endogenous Exogenous Exogenous Endogenous

Reference Ahmmad et al. (2019) Xing et al. (2021) Li et al. (2018a, b); Hu et al. (2016) Byeon et al. (2015) Zhu et al. (2021) Chen et al. (2020) Xu et al. (2019) Zhang et al. (2022) Menhas et al. (2021) Umapathi et al. (2018)

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Fig. 19.5  Biosynthetic pathway of melatonin in plants

(caffeic acid O-methyltransferase) are involved. In the start, TDC starts catalyzing the decarboxylation of tryptophan and produces tryptamine in the cytoplasm, succeeding the hydroxylation by T5H and start producing serotonin in ER. Serotonin is also produced by the hydroxylation of tryptophan by TPH/T5H generating 5-hydroxytryptophan (Yu et al. 2021). After serotonin production two intermediates are produced, ASMT through methylation produces 5-methoxytryptamine in the cytoplasm and SNAT by acetylation produces acetylserotonin in the chloroplast. The methylation of serotonin is also carried out by COMT in plants. Afterward, SNAT and ASMT start converting serotonin intermediates into a compound known as melatonin, a warrior against metal stress (Zhu et al. 2021). The biosynthesis of melatonin follows the schematic pathway in a manner (Fig. 19.5).

19.14 Conclusion and Future Perspectives Melatonin act as a plant growth stimulator under heavy metal stresses. Concerning environmental degradations, biosynthesis of melatonin causes remarkable indirect (stimulate plant metabolism by the anti-oxidative system) and direct (chelating heavy metals, scavenging free radicals) impacts in enhancing phytoremediation treatment. MEL will enhance the plant metabolism and produce tolerance against stresses. Moreover, studies gap still exits about the uptake, translocation, and genes pathways of MEL actions. More studies are required to understand the application of MEL to achieve sustainability and more accuracy in phytoremediation against stresses. The interaction of the plant with the environment during the episode of heavy metal stress induces resistance against heavy metal stress developed resilience in various plant species in a long evolutionary process. During this interaction, plants updated internal physiological, biochemical and genetic mutations to develop adaptation under stressful environments. In the future, additional transgenic crops should be produced focusing on the alteration of melatonin levels about develop a homeostatic balance between stress and tolerance. Similarly, the importance of melatonin as a stress tonic for humans as well, future research will be based on the production of vegetables and fruits with a higher level of melatonin. Moreover, the melatonin-mediated tolerance mechanisms in crops against biotic stress like

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pathogens and insects should also be decoded which will help to enhance the capability of phytoremediation in a plant. It has been documented globally that melatonin promotes root growth but its impact on nutrient uptake is yet to be investigated. Moreover, the most efficient method for melatonin application, absorption to induce tolerance in sensitive species needs further exploration.

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