Plant Performance Under Environmental Stress: Hormones, Biostimulants and Sustainable Plant Growth Management 3030785203, 9783030785208

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Azamal Husen   Editor

Plant Performance Under Environmental Stress Hormones, Biostimulants and Sustainable Plant Growth Management

Plant Performance Under Environmental Stress

Azamal Husen Editor

Plant Performance Under Environmental Stress Hormones, Biostimulants and Sustainable Plant Growth Management

Editor Azamal Husen Wolaita Sodo University Wolaita, Ethiopia

ISBN 978-3-030-78520-8    ISBN 978-3-030-78521-5 (eBook) https://doi.org/10.1007/978-3-030-78521-5 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 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

To my wife, Shagufta Yasmeen and children Zaara, Mehwish, and Huzaifa, for their inspiration, encouragement, and support.

Preface

Global climate change is bound to create a number of abiotic and biotic stresses in the environment, which would affect the overall growth and productivity of plants. Like other living beings, plants have the ability to protect themselves by evolving various mechanisms against stresses, despite being sessile in nature. They manage to withstand extremes of temperature (hot and cold), extremes of water availability (drought and flooding), salinity, heavy metals, atmospheric pollution, toxic chemicals (fertilizers, pesticides, herbicides), and a variety of living organisms, especially viruses, bacteria, fungi, nematodes, insects, arachnids, weeds, etc. Incidence of abiotic stresses may alter the plant–pest interactions by enhancing susceptibility of plants to pathogenic organisms. These interactions often change plant response to abiotic stresses. Food security for the rapidly growing human population in a sustainable ecosystem is a major concern of the present-day world. Understanding the core developmental, physiological, and molecular aspects that regulate plant performance in terms of growth and productivity under stresses is a pivotal issue to be tackled skillfully by the scientific community dealing with sustainable agricultural and horticultural practices. Plant growth regulators modulate plant responses to biotic and abiotic stresses and regulate their growth and developmental cascades. Also, interaction between biotic and abiotic stresses is controlled by hormone signaling. A number of physiological and molecular processes that act together in a complex regulatory network, further manage these responses. Crosstalk between autophagy and hormones also occurs to develop tolerance in plants towards multiple abiotic stresses. Similarly, biostimulants, in combination with correct agronomic practices, have shown beneficial effects on plant metabolism due to the hormonal activity that stimulates different metabolic pathways. At the same time, they reduce the use of agrochemicals and impart tolerance to biotic and abiotic stress. Further, the use of bio- and nano-fertilizers seem to hold promise to improve the nutrient use efficiency and hence the plant yield under stressful environment. Overall, plant exposure to bio-stimulants or hormones reduces damage caused by stress, improves the defense mechanisms involved, and also helps in disease management and nutrient-­use efficiency. It has also been shown that under a stressful environment, use of bio- and vii

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nano-fertilizers determines plant yield and quality, while seed priming agents impart stress tolerance. Additionally, tolerance or resistance to stress may also be induced by using specific chemical compounds such as polyamines, proline, glycine betaine, hydrogen sulfide, silicon, β-aminobutyric acid, and γ-aminobutyric acid. This book comprises of 22 chapters that cover a wide range of topics, as mentioned above, and discusses the trends and advances in plant performance under stressful conditions. The vast coverage of diverse aspects of the subject reflects well from the table of contents. It must be equally useful for graduate students, teachers, researchers, and scientists related to botanical science, crop science, agriculture, horticulture, and environmental science. I express my sincere thanks to the distinguished authors who have shared their knowledge and contributed chapters for this book. I feel indebted to Mr. Eric Stannard, Senior Editor (Botany) at Springer, and all his associates, for their sustained cooperation. I am also grateful to Professor Muhammad Iqbal (Jamia Hamdard, New Delhi, India); Dr. Mansur Osman (University of Gondar, Gondar, Ethiopia); Dr. Mohammad Babar Ali (University of Kentucky, Lexington, USA); Dr. Sophie Mavrikou (Agricultural University of Athens, Athens, Greece); Dr. Adalberto Benavides-Mendoza (Autonomous Agricultural University Antonio Narro, Saltillo, Mexico), and Dr. Rakesh Kumar Bachheti (Addis Ababa Science and Technology University, Addis Ababa, Ethiopia) for their generous help in reviewing various chapters. I shall be happy receiving comments and criticism, if any, from subject experts and general readers of this book. Wolaita, Ethiopia May, 2021

Azamal Husen

Contents

 Cross Talk Between Autophagy and Hormones for Abiotic Stress Tolerance in Plants��������������������������������������������������������������������������������    1 Azamal Husen  Abscisic Acid and Plant Response Under Adverse Environmental Conditions��������������������������������������������������������������������������������������������������������   17 Jorge Gonzalez-Villagra, Carla Figueroa, Ana Luengo-Escobar, Melanie Morales, Claudio Inostroza-Blancheteau, and Marjorie Reyes-Díaz  Auxins and Plant Response to Adverse Environmental Conditions������������   49 Swati T. Gurme, Pankaj S. Mundada, Mahendra L. Ahire, and Supriya S. Salunkhe  Jasmonic Acid for Sustainable Plant Growth and Production Under Adverse Environmental Conditions����������������������������������������������������   71 Sahil, Adhip Das, Sahil Mehta, K. F. Abdelmotelb, Shivaji Ajinath Lavale, S. K. Aggarwal, Bahadur Singh Jat, Anurag Tripathi, and Surbhi Garg  Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment������������������������������������������������������������������������������   99 Sahil, Radhika Keshan, Sahil Mehta, K. F. Abdelmotelb, S. K. Aggarwal, Shivaji Ajinath Lavale, Bahadur Singh Jat, Anurag Tripathi, and Laxman Singh Rajput  Strigolactones for Sustainable Plant Growth and Production Under Adverse Environmental Conditions����������������������������������������������������  129 Ali Raza, Rida Javed, Zainab Zahid, Rahat Sharif, Muhammad Bilal Hafeez, Muhammad Zubair Ghouri, Muhammad Umar Nawaz, and Manzer H. Siddiqui

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 Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental Conditions����������������������������������������������������  167 Brij Bihari Pandey, Ratnakumar Pasala, Kulasekaran Ramesh, Sumit Kumar Mishra, Nidhi Tyagi, Akankhya Guru, Pappu Lal Bairwa, C. L. N. Manikanta, and Arti Guhey  Plant Performance and Defensive Role of Proline Under Environmental Stress��������������������������������������������������������������������������������������  201 Pankaj S. Mundada, Suchita V. Jadhav, Supriya S. Salunkhe, Swati T. Gurme, Suraj D. Umdale, Tukaram D. Nikam, and Mahendra L. Ahire  Plant Performance and Defensive Role of Glycine Betaine Under Environmental Stress ��������������������������������������������������������������������������  225 Praveen Jain, Brijesh Pandey, Pratibha Singh, Ranjana Singh, Satarudra Prakash Singh, Sashi Sonkar, Rahul Gupta, Saurabh Singh Rathore, and Akhilesh Kumar Singh  Plant Performance and Defensive Role of β-Amino Butyric Acid Under Environmental Stress������������������������������������������������������������������  249 Anuj Choudhary, Antul Kumar, Harmanjot Kaur, A. Balamurugan, Asish Kumar Padhy, and Sahil Mehta  Plant Performance and Defensive Role of γ-Gamma Amino Butyric Acid Under Environmental Stress����������������������������������������������������  277 Antul Kumar, Anuj Choudhary, Harmanjot Kaur, Mohammed Javed, and Sahil Mehta  Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress��������������������������������������������������������������������������������������  301 Pankaj Pandey, Asha Devi Pallujam, S. Leelavathi, Sahil Mehta, Manesh Chander Dagla, Bharat Bhushan, and S. K. Aggarwal  Functions of Hydrogen Sulfide in Plant Regulation and Response to Abiotic Stress������������������������������������������������������������������������������������������������  329 Sashi Sonkar, Akhilesh Kumar Singh, and Azamal Husen  Silicon and Plant Responses Under Adverse Environmental Conditions ��  357 Pankaj S. Mundada, Suchita V. Jadhav, Supriya S. Salunkhe, Swati T. Gurme, Suraj D. Umdale, Rajkumar B. Barmukh, Tukaram D. Nikam, and Mahendra L. Ahire  Nanofertilizers as Tools for Plant Nutrition and Plant Biostimulation Under Adverse Environment������������������������������������������������  387 Misbah Naz and Adalberto Benavides-Mendoza  Biostimulants and Plant Response Under Adverse Environmental Conditions: A Functional Interplay ��������������������������������������������������������������  417 Giacomo Cocetta, Andrea Ertani, Roberta Bulgari, Giulia Franzoni, Silvana Nicola, and Antonio Ferrante

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 Biofertilizers-Mediated Sustainable Plant Growth and Production Under Adverse Environmental Conditions������������������������  437 Swetika Porwal, Akhilesh Kumar Singh, Ashok Kumar Yadav, Sudhir Kumar, and Paras Porwal  Seed Priming: A Cost-effective Strategy to Impart Abiotic Stress Tolerance����������������������������������������������������������������������������������  459 Akhila Sen, Riya Johnson, and Jos T. Puthur  Significance of Cyanobacteria in Soil-Plant System and for Ecological Resilience��������������������������������������������������������������������������  481 Subhra Chakraborti, Abhishek Sen, Kuntal Bera, Puspendu Dutta, Shovik Deb, Satyajit Hembram, and Ashok Choudhury Phytomicrobiome Community: An Agrarian Perspective Towards Resilient Agriculture������������������������������������������������������������������������  493 Mayur Mukut Murlidhar Sharma, Pankaj Sharma, Divya Kapoor, Puneet Beniwal, and Sahil Mehta  Adverse Environment and Pest Management for Sustainable Plant Production����������������������������������������������������������������������������������������������  535 Priyanka Saxena, Akhilesh Kumar Singh, and Rahul Gupta  Eco-friendly Approaches of Using Weeds for Sustainable Plant Growth and Production����������������������������������������������������������������������������������  559 Satish Kumar Ameta and Suresh C. Ameta Index������������������������������������������������������������������������������������������������������������������  593

About the Editor

Azamal Husen  (BSc from Shri Murli Manohar Town Post Graduate College, Ballia, UP; MSc from Hamdard University, New Delhi; and PhD from Forest Research Institute, Dehra Dun, India) is a Foreign Delegate at Wolaita Sodo University, Wolaita, Ethiopia. He has served the University of Gondar, Ethiopia, as a Full Professor of Biology, and also worked as the Coordinator of MSc Program and the Head, Department of Biology. He was a Visiting Faculty of the Forest Research Institute, and the Doon College of Agriculture and Forest at Dehra Dun, India. He has a more than 20 years’ experience of teaching, research and administration. Dr. Husen specializes in biogenic nanomaterials fabrication and their application, plant response to nanomaterials, plant production and adaptation to harsh environments at physiological, biochemical and molecular levels, herbal medicine, and clonal propagation and improvement of tree species. He has conducted several research projects sponsored by various funding agencies, including the World Bank, the Indian Council of Agriculture Research (ICAR), the Indian Council of Forest Research Education (ICFRE); and the Japan Bank for International Cooperation (JBIC), etc. He has published over 100 research papers, review articles and book chapters, edited books of international repute, presented papers in several conferences, and produced over a dozen of manuals and monographs. Husen received four fellowships from India and a recognition award from University of Gondar, Ethiopia, for excellent teaching, research and community service. An active organizer of seminars, and conferences, and an efficient evaluator of research projects and book proposals as he is, Dr. Husen has been on the Editorial board and the panel of reviewers of several reputed journals of Elsevier, Frontiers Media SA, Taylor & Francis, Springer Nature, RSC, Oxford University Press, Sciendo, The Royal Society, CSIRO, PLOS and John Wiley & Sons. He is included in the advisory board of Cambridge Scholars Publishing, UK.  He is a Fellow of the Plantae group of

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American Society of Plant Biologists, and a Member of International Society of Root Research, Asian Council of Science Editors, and INPST, etc. Also, he is Editor-in-Chief of American Journal of Plant Physiology; and a Series Editor of ‘Exploring Medicinal Plants’ published by Taylor & Francis Group, USA.

Cross Talk Between Autophagy and Hormones for Abiotic Stress Tolerance in Plants Azamal Husen

Abbreviations ABA Abscisic acid ACC 1-(Aminocarbonyl)-1cyclopropanecarboxylic acid AOX Alternative oxidase ATGs Autophagy-related genes ATI1 Autophagy interacting protein 1 DRE Drought-responsive elements DSK2 DOMINANT SUPPRESSOR OF KAR 2 ERF5 Ethylene response factor 5 ERF5 Ethylene response factor 5 ET Ethylene HSE Heat-shock elements HsfA1a Heat-shock transcription factor A1a HSPs Heat-shock proteins IAA Indole acetic acid PBR Peripheral-type benzodiazepine receptor PDC Programmed cell death PIP2;7 PLASMA-MEMBRANE INTRINSIC PROTEIN 2;7 RNAi RNA interference SA Salicylic acid TOR Target of rapamycin TSPO Tryptophan-rich sensory protein

A. Husen (*) Wolaita Sodo University, Wolaita, Ethiopia © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_1

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1  Introduction Plants, like other living beings, have the ability to protect themselves by evolving numerous mechanisms against abiotic stresses despite being sessile in nature (Anjum et al. 2012, 2014; Bechtold and Field 2018; He et al. 2018). They manage to withstand harsh environmental conditions such as extreme temperatures (Bita and Gerats 2013; Nahar et al. 2015), water scarcity (Husen et al. 2014; Getnet et al. 2015; Embiale et al. 2016), flooding (Loreti et al. 2016; Zhou et al. 2020), salinity (Yousuf et al. 2016a, b; Hussein et al. 2017), heavy metals (Moinuddin et al. 2004; Ghori et al. 2019; Ding et al. 2020), ionizing radiation (Esnault et al. 2010; Aref et al. 2016; Caplin and Willey 2018), nutrient deficiency (Ahmad et al. 2005; Ganie et al. 2016, 2017; Bagheri et al. 2017), atmospheric pollution (Husen 1997; Husen et al. 1999; Husen and Iqbal 2004; Iqbal et al. 2000, 2010), chemicals (Bashir et al. 2007, 2014; Majid et  al. 2013; Bashir and Iqbal 2014), and so on as mentioned in Fig. 1.

Fig. 1  Biological and nonbiological stress factors

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Of late, environmental adversities have grown more prominent due to rapidly increasing atmospheric pollution and the drastic fluctuations in the global climate conditions. For instance, worldwide drought stress may increase due to prolonged exposure to high temperature in rainfed areas. This may also induce osmotic stress, if water evaporates from soils, leading to elevated salt concentrations. Raftery et al. (2017) have suggested an increase of global average temperature from 2.0 to 4.9 °C by 2100. Thus, in the near future, combination of high temperature, drought, and salt stress may possibly lead to a drastic reduction in plant fitness and their overall productivity at the global level. It has also been projected that about 90% of arable lands are now prone to single or multiple stress conditions (dos Reis et al. 2012). Phytohormones such as auxins, gibberellins, cytokinins, ethylene, abscisic acid, jasmonates, brassinosteroids, and strigolactones play a significant role in saving plants from single or multiple stress conditions, by mediating plant growth and development, nutrient allocation and the source and or sink transitions (Peleg and Blumwald 2011; Colebrook et al. 2014; Kazan 2015; Husen et al. 2016, 2017, 2018, 2019; Siddiqi and Husen 2017a, 2019; Podlešáková et al. 2019). In general, they are responsible for stress signaling in plants. Further, during the process of plant adaptation to stress, cells require to recycle the damaged/unwanted proteins and organelles. In this connection, the term autophagy (i.e., self-eating) evolved. In plant, three kinds of autophagy, namely micro-autophagy, macro-autophagy, and mega-­ autophagy, have been reported. In the first case, the cytoplasmic constituents are sequestered by the tonoplast invagination, which is then released into the vacuolar lumen, producing single-membrane autophagic bodies (Todde et  al. 2009; May et al. 2012; Marshall and Vierstra 2018). In macro-autophagy, on the other hand, the double-membrane-bound organelles, called phagophores, develop in the cytoplasm to engulf cytoplasmic material (Thompson and Vierstra 2005; Bassham et al. 2006), and the resulting double-membrane vesicles, autophagosomes, reach the vacuole. The outer membrane of autophagosome combines with the tonoplast to release an autophagic body into the vacuolar lumen; this autophagic body is degenerated in the vacuole to release its content for recycling (Li and Vierstra 2012). Mega-autophagy (massive autophagy) is an utmost form of autophagy, the final phase of the developmental programmed cell death (PCD). In plant cells, two main types of PDC are noticed. The first one is observed during the normal development and after the abiotic stress (developmental PCD), whereas the second one occurs after pathogen attack (pathogen-related PCD). The mega-autophagy process begins with the permeabilization or rupture of vacuolar membrane, which permits vacuolar hydrolases to release into the cytoplasm. These vacuolar hydrolases totally damage the cytoplasm, and in several cases also the cell walls, finally leading to cell death (Fukuda 1996; Marshall and Vierstra 2018; Locato and De Gara 2018; Papini 2018). Salinity, drought and heat stress, nutrient deficiency, oxidative stress, hypoxia, and pathogen attack has been shown to induce autophagy in different cellular settings (Doelling et al. 2002; Xiong et al. 2007; Liu et al. 2009; Zhou et al. 2014; Chen et al. 2015; Lai et al. 2011; Luo et al. 2017; Hofius et al. 2017). Autophagy has also been noticed to control the growth and development processes in plants (Yang et al. 2019). Autophagy-related genes (ATGs) have been shown to be involved in

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pollen growth, seed development and germination, leaf senescence, and nitrogen use efficiency (Wang et al. 2016; Yu et al. 2019; Zhen et al. 2019; Han et al. 2020; Hanamata et al. 2020). Further, the autophagy regulates hormone synthesis and signaling pathways, whereas hormone signaling regulates autophagy gene expression also (Liao and Bassham 2020). The significance of autophagy has increased after the report of mutagenesis in yeast (Tsukada and Ohsumi 1993; Thumm et al. 1994; Harding et al. 1995), and to date, more than 30 ATGs associated with the autophagy pathway have been recognized (Yoshimoto 2012; Marshall and Vierstra 2018). Recently, Signorelli et  al. (2019) have suggested that the accumulation of γ-aminobutyric acid, proline, and polyamines in a stressful environment may indirectly promote autophagy through different pathways and also facilitate the osmotic adjustment that coordinates the autophagic process to avoid mega-autophagy. On the whole, cross talk between autophagy and hormones under abiotic stress conditions are poorly understood in the plant system. Based on the available information, this article discusses the current understanding of autophagy under abiotic stress, and hormones coordination/modulation in plant growth and development.

2  Autophagy and Abiotic Stresses In general, most of the abiotic stresses exhibit some common responses, though they are controlled in different ways. For instance, salinity differs from drought stress in generating ionic stress in addition to osmotic stress, which leads to membrane disruption and enzyme dysfunction. Salinity, drought, and other stresses including nanoparticles exposure lead to an enhanced production of reactive oxygen species (ROS) which damage cellular membranes, proteins, and nucleic acids (Miller et  al. 2008; Jaspers and Kangasjärvi 2010; Gill and Tuteja 2010; Husen 2010; Siddiqi and Husen 2016, 2017b; Singh and Husen 2019, 2020). Plant system has shown numerous mechanisms to tolerate abiotic stress, for example, regulating the growth rate by altering cell wall biosynthesis, protein synthesis, as well as cell division (Burssens et al. 2000; Le Gall et al. 2015; Kosová et al. 2018). At the cellular level, overproduction of ROS may harm organelles and biomolecules, affecting their functionality (Umar et al. 2018). An interplay between ROS and autophagy is noticed; ROS induce autophagy and autophagy reduces ROS production (Signorelli et al. 2019). Further, several genes have been shown to respond under abiotic stress condition and get involved in mechanisms of stress tolerance (Zhu 2001; Haak et al. 2017; Baillo et al. 2019). In this connection, several potential roles of autophagy in response to abiotic stress have been unraveled in terms of plant resistance. For instance, autophagosome induction was noted under mannitol and salinity effects, and Arabidopsis RNAi-ATG18a plants growing under drought, salt, or osmotic stress displayed enhanced sensitivity to the stress (Liu et  al. 2009). Similarly, Luo et al. (2017) have reported various ATG mutants under salt stress, which had higher oxidized proteins in comparison to wild-type plants. Wang et al. (2017) have suggested that the overexpression of ATG3 homologs from Malus

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domestica in Arabidopsis augmented their resistance to salt and osmotic stress. This study suggested an anticipated autophagy function under drought stress to control quality of protein. In Solanum lycopersicum, silencing heat-shock transcription factor A1a (HsfA1a) led to a higher insoluble protein accumulation, whereas overexpression of HsfA1a decreased the insoluble protein content under drought stress (Wang et  al. 2015). This was supported by the observation of reduced insoluble protein and less oxidation of soluble proteins in ATG18a overexpressing M. domestica (Sun et al. 2018a) (Fig. 2). In this experiment, Sun et al. (2018a) observed that the overexpression of ATG18a from M. domestica in S. lycopersicum as well as in M. domestica enhanced their resistance to drought stress in comparison to wild-type plants. In another study, Zhu et al. (2018) found that mitochondrial alternative oxidase (AOX) regulates autophagy via mitochondrial ROS under drought stress

Fig. 2  Identified regulators of autophagy during drought and heat stress in Solanum lycopersicum. AOX within mitochondria and the transcription factor ERF5 are induced by drought stress, in a process mediated by ethylene. AOX can positively regulate autophagy by balancing the level of ROS; lower ROS levels are thought to activate autophagy, whereas higher ROS levels inhibit autophagy. ERF5 induces the expression of ATG8d and ATG18h by binding to DRE in their promoters. HsfA1a is also induced by drought stress and activates the expression of ATG10 and ATG18f by binding to HSE in their promoters. Under heat stress, the transcription factors WRKY33a and WRKY33b activate the expression of ATG5, ATG7, NBR1a, and NBR1b S. lycopersicum. Autophagy in turn functions to degrade the protein aggregates induced by drought or heat (adopted from Tang and Bassham 2018)

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conditions in S. lycopersicum plants. AOX limits the ROS formation by preventing the over-­reduction of the electron transport chain (Selinski et al. 2018). In S. lycopersicum, AOX-overexpressing plants exhibited augmented drought stress tolerance, whereas AOX-silenced S. lycopersicum revealed hypersensitivity in comparison to wild-type plants, signifying the functions of AOX in terms of drought responses (Zhu et al. 2018) (Fig. 2). Also, the AOX transcript and protein were induced by application of ethylene (ET) precursor 1-(aminocarbonyl)-1cyclopropanecarboxylic acid (ACC). ACC application conferred higher autophagy activity and better drought tolerance to S. lycopersicum plants by either overexpressing or silencing the AOX (Zhu et  al. 2018) (Fig.  2). ATGs were transcriptionally controlled by drought stress in S. lycopersicum. The transcription factor ethylene response factor 5 (ERF5), induced by both drought and ACC application, binds to the promoters of ATG8d and ATG18h, and inducing their expression (Zhu et al. 2018). In heat stress also, autophagy plays a significant role in stress alleviation. Accumulation of autophagosomes in Arabidopsis and L. esculentum plants growing under heat stress has been reported (Zhou et al. 2013, 2014; Yang et al. 2016). In the case of Arabidopsis, ATG5 and ATG7 mutants have shown more sensitivity under heat stress condition in comparison to wild-type plants, as demonstrated by more wilting, higher electrolyte leakage, and decreased rate of photosynthesis. Moreover, ATG7 mutant plants exhibited insoluble protein aggregates accumulation, labeled by ubiquitin (Zhou et  al. 2013). In accordance with this observation, Zhou et  al. (2014) reported a virus-induced gene silencing of ATG5 and ATG7 in L. esculentum plants exposed to heat stress (Zhou et al. 2014). It was suggested that heat stress induces autophagy by provoking endoplasmic reticulum stress. Endoplasmic reticulum stress stems from the unfolded proteins accumulation in endoplasmic reticulum, and formation of protein aggregates (Yang et al. 2016). Some of the studies have suggested that both micro- and macro-autophagy play a key role in the formation of anthocyanin vacuolar inclusions under stressful conditions (Masclaux-­ Daubresse et  al. 2014; Chanoca et  al. 2015; Sun et  al. 2018b). ATG mutant Arabidopsis plants have also shown decreased accumulation of anthocyanin under nitrogen starvation (Masclaux-Daubresse et al. 2014), and ATG18a overexpression in M. domestica encouraged accumulation of anthocyanin under nitrogen starvation (Sun et al. 2018b). It is suggested that the abiotic stress condition activated ROS production (Baxter et al. 2014), and anthocyanin possibly works as an antioxidant and mitigates the damage caused by ROS, and thus facilitates stress tolerance. In mammalian cells, selective autophagy is mediated by a receptor such as Neighbor of BRCA1 (NBR1) (Svenning et al. 2011). In plants, NBR1 homologs have been linked to selective autophagy under stress, but it is uncertain how they influence the selective autophagy under non-stressed situations (Jung et al. 2020). Svenning et al. (2011) reported that NBR1 binds to ubiquitin in Arabidopsis plants, as in the mammalian counterpart. In Arabidopsis plants exposed to heat stress condition, NBR1 expression was upregulated, and GFP-NBR1 puncta gathered in the wild-type plants under heat stress, but not in ATG7 mutants; the representative puncta formation was autophagy-dependent (Zhou et al. 2013). Taken together, it was found that the NBR1 mutants were hypersensitive under heat, oxidative, and salt stress

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conditions in comparison to wild-type plants. Under heat stress, NBR1 mutants exhibited ubiquitin-positive, non-soluble protein aggregates accumulation and the part of NBR1-bound insoluble proteins was augmented in ATG7 mutants (Zhou et al. 2013). Zhou et al. (2014) reported the same in L. esculentum in which NBR1 was silenced by virus-induced gene silencing. They found that silencing of L. esculentum ATG5, ATG7, or NBR1 compromised heat-induced expression of not only the targeted genes but also other autophagy-related genes. In another experiment, Sedaghatmehr et al. (2019) identified autophagy as a key negative regulator of thermomemory and, hence, tolerance to successive heat stresses in Arabidopsis. The authors suggested that autophagy mediates the degradation of specific heat-shock proteins (HSPs) at later stages of the thermorecovery phase, leading to protein-­ aggregates accumulation after the second heat stress and facilitates heat tolerance. Autophagy mutants retained HSPs longer than wild type and concurrently showed better thermomemory. Guillaumot et al. (2009) reported a membrane-spanning protein (Tryptophan-rich sensory protein/peripheral-type benzodiazepine receptor-­ TSPO/MBR), which expressed under salt/osmotic stress and abscisic acid exposure. Vanhee et  al. (2011) reported that TSPO binds free heme and acts as a heme-­ scavenger, and also regulates heme levels in cells. In another study, it was suggested that TSPO binds the plasma membrane aquaporin, PLASMA MEMBRANE INTRINSIC PROTEIN 2;7 (PIP2;7). Expression of both proteins reduced PIP2;7 levels and autophagy inhibition stopped this reduction. Thus, Hachez et al. (2014) suggested that TSPO controls the uptake of water by the cell during the abiotic stress associated with water-deficit conditions. However, TSPO overexpression under salinity showed hypersensitivity, though tspo mutants remained unaffected in comparison to wild-type plants (Guillaumot et al. 2009). Perhaps, it could be due to aquaporins over-degradation and hence damaged regulations of cell water status. Further, Nolan et al. (2017) reported that DOMINANT SUPPRESSOR OF KAR 2 (DSK2—a ubiquitin binding receptor) interacted with ATG8 and BRI1-EMS SUPPRESSOR 1 (BES1), a brassinosteroid (BR) pathway regulator. BES1 levels decreased under drought stress. Also, the DOMINANT SUPPRESSOR OF KAR 2 (DSK2)-RNAi Arabidopsis showed enhanced sensitivity under stress, which was due to augmented BES1 levels in comparison to wild-type plants. This was also reported in ATG7 mutants. This investigation also revealed opposite expression of drought-related genes in the DSK2-RNAi plants. It was suggested that by controlling BES1 levels via autophagic degradation, DSK2 may downregulate BR signals to switch cells from growth to stress mode (Nolan et al. 2017). Thus, this report revealed the cross talk among autophagy and hormonal signaling in plants under stress conditions. Thus far, autophagy was considered a phenomenon of promoting plant survival under various abiotic stress conditions. Nonetheless, Bárány et  al. (2018) have shown that autophagy functions in promoting PCD during microspore embryogenesis in Hordeum vulgare. Formation of autophagosome was observed in microspores as well as PCD on exposure to stress (at 4 °C). Further, autophagy inhibitors treatment reduced the microspore cell death. These observations have revealed the dual role of autophagy under abiotic stress conditions, depending on the type of

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stress, plant organ, and the developmental phase. Further, a recent investigation has shown that BRs act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato plants (Chi et al. 2020). It was noted that cold and BRs induced the stability of BRASSINAZOLE-RESISTANT1 (BZR1), which upregulates ATG2, ATG6, NBR1a, and NBR1b expression by binding to their promoters, thus resulting in increased autophagy and increased levels of NBR1 protein. The upsurge in autophagy and the selective autophagy receptor NBR1 increased photoprotection via greater accumulation of functional proteins (PsbS, VDE, and D1) and encouraged the degradation of stress-damaged ubiquitinated protein aggregates, thus leading to increased tolerance to cold (Fig. 3).

Fig. 3  A proposed model for the induction of cold tolerance by BZR1 through the activation of autophagy in tomato. Both cold and brassinosteroids can induce the stability of BRASSINAZOLE RESISTANT 1 (BZR1), which activates the transcription of the autophagy genes ATG2, ATG6, NBR1a, and NBR1b by directly binding to their promoters, subsequently enhancing autophagy. The increase in autophagy promotes photoprotection via greater accumulation of functional proteins (PsbS, VDE, and D1) and increases the degradation of stress-damaged insoluble ubiquitinated protein aggregates via the selective autophagy receptor NBR1. Arrows denote positive regulation; bar ends denote negative regulation (adopted from Chi et al. 2020)

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3  Hormonal Interaction The cross talk between phytohormones and autophagy under stress conditions has been verified many times, yet the precise molecular mechanism is unknown. Abscisic acid (ABA) work as an endogenous messenger under stressful conditions (Raghavendra et al. 2010). ABA was known to prevent the activity of plant target of rapamycin (TOR), which may facilitate the autophagy induction under stress. However, the exact molecular mechanism is still unclear. The role of ABA under abiotic stress was revealed to affect the TSPO expression (Guillaumot et al. 2009). Further, Honig et  al. (2012) reported that the ATI1/2 knockdown seeds showed reduced germination due to ABA exposure, which suggests an interplay between ABA and autophagy. Yoshimoto et al. (2014) suggested that the early senescence phenotype of ATG mutants was arbitrated by salicylic acid (SA) accumulation, and autophagy was revealed to control SA signaling during senescence and also under biotic stress. Slavikova et al. (2008) have reported that GFP-ATG8f-HA Arabidopsis plants showed a different performance on exposure to cytokinin, in comparison to the wild-type plants, as verified by changes in root architecture and the production and accumulation of anthocyanin, testifying that autophagy could regulate this process. However, no changes were seen between GFP-ATG8f-HA plants and wild-­ type plants under IAA exposure (Slavikova et al. 2008). Auxins function in TOR kinase-dependent autophagy induction under specific abiotic stresses (Pu et  al. 2017). TOR kinase works as a global integrator of metabolic and environmental signals to increase or decrease the growth, and one of its important functions is the negative autophagy regulation (Liu et al. 2012; Rexin et al. 2015). Autophagy also regulates phytohormone synthesis. For instance, Nolan et al. (2017) have shown BR signaling regulated by autophagy. They have suggested that selective autophagy may be involved in the regulation of phytohormone signaling and biosynthesis, thus modulating plant responses under changing/adverse and or abiotic environmental conditions.

4  Conclusion Autophagy, a eukaryotic catabolic mechanism, participates in processes of plant growth and development, and responses to numerous biotic and abiotic stresses. It is important for the degradation of unnecessary and dysfunctional cellular components at some stages of growth/development and under adverse environmental conditions. In recent years, investigation associated with autophagy has been expanded from Arabidopsis to other crop plants. So far, many ATGs associated with the autophagy pathway have been recognized. A better understanding of increased ATGs expression could be beneficial for the agricultural sector. Thus far, the regulatory mechanisms of autophagy and the hormonal cross talk under adverse environmental conditions at the molecular level are poorly understood, and deserve further in-depth exploration.

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References Ahmad A, Khan I, Anjum NA, Diva I, Abdin MZ, Iqbal M (2005) Effect of timing of sulfur fertilizer application on growth and yield of rapeseed. J Plant Nutr 28(6):1049–1059 Anjum NA, Gill SS, Ahmad I, Tuteja N, Soni P, Pareek A, Umar S, Iqbal M, Pacheco M, Duarte AC, Pereira E (2012) Understanding stress-responsive mechanisms in plants: an overview of transcriptomics and proteomics approaches. In: Tuteja N, Tiburcio AF, Singh S et  al (eds) Improving crop resistance to abiotic stress—omics approaches. Wiley-VCH Verlag GmbH & Co, Germany, pp 337–355 Anjum NA, Aref IA, Pereira E, Ahmad A, Iqbal M (2014) Glutathione and proline can coordinately make plants withstand the joint attack of osmotic and metal(loid) stresses. Front Plant Sci 5(662):4. https://doi.org/10.3389/fpls.2014.00662 Aref IM, Khan PR, Al-Sahli AA, Husen A, Ansari MKA, Mahmooduzzafar, Iqbal M (2016) Response of Datura innoxia Linn. to gamma rays and its impact on plant growth and productivity. Proc Nat Acad Sci, India (Biol Sci) 86(3):623–629 Bagheri R, Ahmad J, Bashir H, Iqbal M, Qureshi MI (2017) Changes in rubisco, cysteine-rich proteins and antioxidant system of spinach (Spinacia oleracea L.) due to sulphur deficiency, cadmium stress and their combination. Protoplasma 254:1031–1043 Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes (Basel) 10:771 Bárány I, Berenguer E, Solís MT, Pérez-Pérez Y, Santamaría ME, Crespo JL, Risueño MC, Díaz I, Testillano PS (2018) Autophagy is activated and involved in cell death with participation of cathepsins during stress-induced microspore embryogenesis in barley. J Exp Bot 69:1387–1402 Bashir F, Iqbal M (2014) Lambda-cyhalothrin-induced oxidative stress alters ascorbate-­glutathione cycle in Glycine max (L.) Merr. Trends Biosci 7(9):703–710 Bashir F, Mahmooduzzafar, Siddiqi TO, Iqbal M (2007) The antioxidative response system in Glycine max (L.) Merr. exposed to Deltamethrin, a synthetic pyrethroid insecticide. Environ Pollut 147:94–100 Bashir F, Mahmooduzzafar, Siddiqi TO, Iqbal M (2014) Alphamethrin (a synthetic pyrethroid)induced oxidative stress and antioxidant-defence mechanism in Glycine max (L.) Merr. Int J Agric Sci 5(1):27–41 Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2:2–11 Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240 Bechtold U, Field B (2018) Molecular mechanisms controlling plant growth during abiotic stress. J Exp Bot 69:2753–2758 Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273. https://doi. org/10.3389/fpls.2013.00273 Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, Inzé D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640 Caplin N, Willey N (2018) Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses. Front Plant Sci 9:847. https://doi.org/10.3389/fpls.2018.00847 Chanoca A, Kovinich N, Burkel B, Stecha S, Bohorquez-Restrepo A, Ueda T, Eliceiri KW, Grotewold E, Otegui MS (2015) Anthocyanin vacuolar inclusions form by a microautophagy mechanism. Plant Cell 27:2545–2559 Chen L, Liao B, Qi H, Xie LJ, Huang L, Tan WJ, Zhai N, Yuan LB, Zhou Y, Yu LJ, Chen QF, Shu W, Xiao S (2015) Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana. Autophagy 11:2233–2246

Cross Talk Between Autophagy and Hormones for Abiotic Stress Tolerance in Plants

11

Chi C, Li X, Fang P, Xia X, Shi K, Zhou Y, Zhou J, Yu J (2020) Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato. J Exp Bot 71:1092–1106 Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75 Ding Y, Ding L, Xia Y, Wang F, Zhu C (2020) Emerging roles of microRNAs in plant heavy metal tolerance and homeostasis. J Agric Food Chem 68:1958–1965 Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12-­ activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 277:33105–33114 dos Reis SP, Lima AM, de Souza CRB (2012) Recent molecular advances on downstream plant responses to abiotic stress. Int J Mol Sci 13:8628–8647 Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Esnault M-A, Legue F, Chenal C (2010) Ionizing radiation: advances in plant response. Environ Exp Bot 68(3):231–237 Fukuda H (1996) Xylogenesis: initiation, progression, and cell death. Annu Rev Plant Physiol Plant Mol Biol 47:299–325 Ganie AH, Yousuf PY, Ahad A, Pandey R, Ahmad S, Aref IM, Iqbal M (2016) Quantification of phenolic acids and antioxidant potential of inbred, hybrid and composite cultivars of maize under different nitrogen regimes. J Environ Biol 37(6):1273–1279 Ganie AH, Ahmad A, Yousuf PY, Pandey R, Ahmad S, Aref IM, Iqbal M (2017) Nitrogen-regulated changes in total amino acid profile of maize genotypes having contrasting response to nitrogen deficit. Protoplasma 254(6):2143–2153 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara Regional State, Ethiopia. J Agron 14:188–202 Ghori N, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828 Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930 Guillaumot D, Guillon S, Deplanque T, Vanhee C, Gumy C, Masquelier D, Morsomme P, Batoko H (2009) The Arabidopsis TSPO-related protein is a stress and abscisic acid-regulated, endoplasmic reticulum-Golgi-localized membrane protein. Plant J 60:242–256 Haak DC, Fukao T, Grene R, Hua Z, Ivanov R, Perrella G, Li S (2017) Multilevel regulation of abiotic stress responses in plants. Front Plant Sci 8:1564 Hachez C, Veljanovski V, Reinhardt H, Guillaumot D, Vanhee C, Chaumont F, Batoko H (2014) The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation. Plant Cell 26:4974–4990 Han B, Xu H, Feng Y, Xu W, Cui Q, Liu A (2020) Genomic characterization and expressional profiles of autophagy-related genes (ATGs) in oilseed crop castor bean (Ricinus communis L.). Int J Mol Sci 21:562 Hanamata S, Sawada J, Ono S, Ogawa K, Fukunaga T, Nonomura K-I, Kimura S, Kurusu T, Kuchitsu K (2020) Impact of autophagy on gene expression and tapetal programmed cell death during pollen development in rice. Front Plant Sci 11:172 Harding TM, Morano KA, Scott SV, Klionsky DJ (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131:591–602 He M, He CQ, Ding NZ (2018) Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front Plant Sci 9:1771 Hofius D, Li L, Hafren A, Coll NS (2017) Autophagy as an emerging arena for plant-pathogen interactions. Curr Opin Plant Biol 38:117–123

12

A. Husen

Honig A, Avin-Wittenberg T, Ufaz S, Galili G (2012) A new type of compartment, defined by plant-specific Atg8-interacting proteins, is induced upon exposure of Arabidopsis plants to carbon starvation. Plant Cell 24:288–303 Husen A (1997) Impact of air pollution on the growth and development of Datura innoxia Mill. M.Sc. Dissertation, Jamia Hamdard, Hamdard Nagar, New Delhi, India Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A, Iqbal M (2004) Growth performance of Datura innoxia Mill. under the stress of coal-­ smoke pollution. Ann For 12:182–190 Husen A, Ali ST, Mahmooduzzafar, Iqbal M (1999) Structural, functional and biochemical responses of Datura innoxia Mill. to coal-smoke pollution. Proc Acad Environ Biol 8:61–72 Husen A, Iqbal M, Aref MI (2014) Growth, water status and leaf characteristics of Brassica carinata under drought stress and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186 Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agric Food Secur 7:44 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Iqbal M, Jacob M, Mehta S, Mahmooduzzafar (2000) Plant responses to particulate matters suspended in the air. In: Iqbal M, Srivastava PS, Siddiqi TO (eds) Environmental hazards: plants and people. CBS Publishers, New Delhi, pp 80–112 Iqbal M, Mahmooduzzafar, Nighat F, Khan PR (2010) Photosynthetic, metabolic and growth responses of Triumfetta rhomboidea to coal-smoke pollution at different stages of plant ontogeny. J Plant Interact 5(1):11–19 Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413 Jung H, Lee HN, Marshall RS, Lomax AW, Yoon MJ, Kim J, Kim JH, Vierstra RD, Chung T (2020) Arabidopsis cargo receptor NBR1 mediates selective autophagy of defective proteins. J Exp Bot 71:73–89 Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229 Kosová K, Vítámvás P, Urban MO, Prášil IT, Renaut J (2018) Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front Plant Sci 9:122 Lai ZB, Wang F, Zheng ZY, Fan BF, Chen ZX (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66:953–968 Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants (Basel) 4:112–166 Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–537 Liao CY, Bassham DC (2020) Combating stress: the interplay between hormone signaling and autophagy in plants. J Exp Bot 71:1723–1733 Liu YM, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5:954–963

Cross Talk Between Autophagy and Hormones for Abiotic Stress Tolerance in Plants

13

Liu Y, Burgos JS, Deng Y, Srivastava R, Howell SH, Bassham DC (2012) Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24:4635–4651 Locato V, De Gara L (2018) Programmed cell death in plants: an overview. In: De Gara L, Locato V (eds) Plant programmed cell death. Methods in molecular biology, vol 1743. Humana Press, New York, pp 1–8 Loreti E, van Veen H, Perata P (2016) Plant responses to flooding stress. Curr Opin Plant Biol 33:64–71 Luo L, Zhang P, Zhu R, Fu J, Su J, Zheng J, Wang Z, Wang D, Gong Q (2017) Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci 8:1459 Majid U, Mahmooduzzafar, Siddiqi TO, Aref IM, Iqbal M (2013) Quantitative changes in proteins, pigments and sennosides of Cassia angustifolia Vahl. treated with Mancozeb. Pak J Bot 45(5):1509–1514 Marshall RS, Vierstra RD (2018) Autophagy: the master of bulk and selective recycling. Annu Rev Plant Biol 69:173–208 Masclaux-Daubresse C, Clément G, Anne P, Routaboul JM, Guiboileau A, Soulay F, Shirasu K, Yoshimoto K (2014) Stitching together the multiple dimensions of autophagy using metabolomics and transcriptomics reveals impacts on metabolism, development, and plant responses to the environment in Arabidopsis. Plant Cell 26:1857–1877 May AI, Devenish RJ, Prescott M (2012) The many faces of mitochondrial autophagy: making sense of contrasting observations in recent research. Int J Cell Biol 431684:1–18 Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489 Moinuddin, Umar S, Iqbal M (2004) Plants in relation to excess of heavy metals. In: Hemantaranjan A (ed) Advances in plant physiology. Scientific Publishers, Jodhpur, pp 319–346 Nahar K, Hasanuzzaman M, Ahamed KU, Hakeem KR, Ozturk M, Fujita M (2015) Plant responses and tolerance to high temperature stress: role of exogenous phytoprotectants. In: Hakeem KR (ed) Crop production and global environmental issues. Springer, Cham, pp 385–435 Nolan TM, Brennan B, Yang M, Chen J, Zhang M, Li Z, Wang X, Bassham DC, Walley J, Yin Y (2017) Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev Cell 41:33–46 Papini A (2018) Investigation of morphological features of autophagy during plant programmed cell death. In: De Gara L, Locato V (eds) Plant programmed cell death. Methods in molecular biology, vol 1743. Humana Press, New York, pp 9–19 Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295 Podlešáková K, Ugena L, Spíchal L, Doležal K, De Diego N (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 48:53–65 Pu Y, Luo X, Bassham DC (2017) TOR-dependent and -independent pathways regulate autophagy in Arabidopsis thaliana. Front Plant Sci 8:1204 Raftery AE, Zimmer A, Frierson DMW, Startz R, Liu P (2017) Less than 2°C warming by 2100 unlikely. Nat Clim Chang 7:637 Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401 Rexin D, Meyer C, Robaglia C, Veit B (2015) TOR signalling in plants. Biochem J 470:1–14 Sedaghatmehr M, Thirumalaikumar VP, Kamranfar I, Marmagne A, Masclaux-Daubresse C, Balazadeh S (2019) A regulatory role of autophagy for resetting the memory of heat stress in plants. Plant Cell Environ 42:1054–1064 Selinski J, Scheibe R, Day DA, Whelan J (2018) Alternative oxidase is positive for plant performance. Trends Plant Sci 23:588–597 Siddiqi KS, Husen A (2016) Engineered gold nanoparticles and plant adaptation potential. Nanoscale Res Lett 11:400

14

A. Husen

Siddiqi KS, Husen A (2017a) Plant response to strigolactones: current developments and emerging trends. Appl Soil Ecol 120:247–253 Siddiqi KS, Husen A (2017b) Plant response to engineered metal oxide nanoparticles. Nanoscale Res Lett 12:92 Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Bull Natl Res Cent 43:153 Signorelli S, Tarkowski ŁP, Van den Ende W, Bassham DC (2019) Linking autophagy to abiotic and biotic stress responses. Trends Plant Sci 24:413–430 Singh S, Husen A (2019) Role of nanomaterials in the mitigation of abiotic stress in plants. In: Husen A, Iqbal M (eds) Nanomaterials and plant potential. Springer, Cham, pp 441–471 Singh S, Husen A (2020) Behavior of agricultural crops in relation to nanomaterials under biotic and abiotic stress conditions. In: Husen A, Jawaid M (eds) Nanomaterials for agriculture and forestry applications. Elsevier Inc., 50 Hampshire St., 5th Floor, Cambridge, MA 02139, USA, pp 219–256 Slavikova S, Ufaz S, Avin-Wittenberg T, Levanony H, Galili G (2008) An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J Exp Bot 59:4029–4043 Sun X, Wang P, Jia X, Huo L, Che R, Ma F (2018a) Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnol J 16:545–557 Sun X, Jia X, Huo L, Che R, Gong X, Wang P, Ma F (2018b) MdATG18a overexpression improves tolerance to nitrogen deficiency and regulates anthocyanin accumulation through increased autophagy in transgenic apple. Plant Cell Environ 41:469–480 Svenning S, Lamark T, Krause K, Johansen T (2011) Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7:993–1010 Tang J, Bassham DC (2018) Autophagy in crop plants: what’s new beyond Arabidopsis? Open Biol 8:180162 Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8:165–173 Thumm M, Egner R, Koch B, Schlumpberger M, Straub M, Veenhuis M, Wolf DH (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett 349:275–280 Todde V, Veenhuis M, van der Klei IJ (2009) Autophagy: principles and significance in health and disease. Biochim Biophys Acta 1792:3–13 Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169–174 Umar S, Anjum NA, Ahmad P, Iqbal M (2018) Drought-induced changes in growth, photosynthesis, and yield traits in mungbean: role of potassium and sulfur nutrition. In: Ozturk M, Hakeem KR, Ashraf M, Ahmad MSA (eds) Crop production technologies for sustainable use and conservation: physiological and molecular advances. Apple Academic Press, Waretown, pp 79–89 Vanhee C, Zapotoczny G, Masquelier D, Ghislain M, Batoko H (2011) The Arabidopsis multistress regulator TSPO is a heme binding membrane protein and a potential scavenger of porphyrins via an autophagy-dependent degradation mechanism. Plant Cell 23:785–805 Wang Y, Cai S, Yin L, Shi K, Xia X, Zhou Y, Yu J, Zhou J (2015) Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 11:2033–2047 Wang P, Sun X, Jia X, Wang N, Gong X, Ma F (2016) Characterization of an autophagy-related gene MdATG8i from apple. Front Plant Sci 7:720 Wang P, Sun X, Jia X, Ma F (2017) Apple autophagy-related protein MdATG3s afford tolerance to multiple abiotic stresses. Plant Sci 256:53–64 Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143:291–299

Cross Talk Between Autophagy and Hormones for Abiotic Stress Tolerance in Plants

15

Yang X, Srivastava R, Howell SH, Bassham DC (2016) Activation of autophagy by unfolded proteins during endoplasmic reticulum stress. Plant J 85:83–95 Yang M, Bu F, Huang W, Chen L (2019) Multiple regulatory levels shape autophagy activity in plants. Front Plant Sci 10:532 Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53:1355–1365 Yoshimoto K, Shibata M, Kondo M, Oikawa K, Sato M, Toyooka K, Shirasu K, Nishimura M, Ohsumi Y (2014) Organ-specific quality control of plant peroxisomes is mediated by autophagy. J Cell Sci 127:1161–1168 Yousuf PY, Ahmad A, Aref IM, Ozturk M, Hemant, Ganie AH, Iqbal M (2016a) Salt-stress-­ responsive chloroplast proteins in Brassica juncea genotypes with contrasting salt tolerance and their quantitative PCR analysis. Protoplasma 253:1565–1575 Yousuf PY, Ahmad A, Ganie AH, Iqbal M (2016b) Salt stress-induced modulations in the shoot proteome of Brassica juncea genotypes. Environ Sci Pollut Res 23:2391–2401 Yu J, Zhen X, Li X, Li N, Xu F (2019) Increased autophagy of rice can increase yield and nitrogen use efficiency (NUE). Front Plant Sci 10:584 Zhen X, Li X, Yu J, Xu F (2019) OsATG8c-mediated increased autophagy regulates the yield and nitrogen use efficiency in rice. Int J Mol Sci 20:4956 Zhou J, Wang J, Cheng Y, Chi YJ, Fan B, Yu JQ, Chen Z (2013) NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet 9:e1003196 Zhou J, Wang J, Yu JQ, Chen Z (2014) Role and regulation of autophagy in heat stress responses of tomato plants. Front Plant Sci 5:174 Zhou W, Chen F, Meng Y, Chandrasekaran U, Luo X, Yang W, Shu K (2020) Plant waterlogging/flooding stress responses: from seed germination to maturation. Plant Physiol Biochem 148:228–236 Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406 Zhu T, Zou L, Li Y, Yao X, Xu F, Deng X, Zhang D, Lin H (2018) Mitochondrial alternative oxidase dependent autophagy involved in ethylene mediated drought tolerance in Solanum lycopersicum. Plant Biotechnol J 16:2063–2076

Abscisic Acid and Plant Response Under Adverse Environmental Conditions Jorge Gonzalez-Villagra, Carla Figueroa, Ana Luengo-Escobar, Melanie Morales, Claudio Inostroza-Blancheteau, and Marjorie Reyes-Díaz

Abbreviations A Photosynthetic rate AAO3 Abscisic-aldehyde oxidase AAO3 Aldehyde oxidase 3 ABA Abscisic acid ABCG ATP-Binding Cassette subfamily G ABI1 ABA-insensitive1 ABI2 ABA-insensitive2 J. Gonzalez-Villagra · C. Inostroza-Blancheteau Departamento de Ciencias Agropecuarias y Acuícolas, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile Núcleo de Investigación en Producción Alimentaria, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile C. Figueroa Carrera de Bioquímica, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco, Chile A. Luengo-Escobar Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN-UFRO), Universidad de La Frontera, Temuco, Chile M. Morales Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Spain M. Reyes-Díaz (*) Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN-UFRO), Universidad de La Frontera, Temuco, Chile Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco, Chile e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_2

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AIT1 (ABA)-importing transporter 1 ALMT1 Aluminum-activated malate transporter 1 APX Ascorbate peroxidase BAM1-3 Barely any meristem 3 bZIP Basic leucine zipper CLE Clavata3/embryo-surrounding region-related CPKs Ca2+-dependent protein kinases DREB/CBF Dehydration-responsive element binding/core binding factor DTX Detoxification efflux carriers E Transpiration rate ERF Ethylene responsive factor GPx Glutathione peroxidase GR Glutathione reductase gs Stomatal conductance HAB1 Hypersensitive to ABA1 IRT1 Iron-regulated transporter 1 LCYb Lycopene ß-cyclase LEA Late embryogenesis abundant MATE1 Multidrug and toxin extrusion protein 1 MCSU Molybdenum cofactor sulfurase MDA Malondialdehyde MEP Methylerythritol phosphate NCED3 Nine-cis-epoxycarotenoid dioxygenase 3 NPF Nitrate peptide transporter ORE1 ORESARA1 P5CS Pyrroline-5-carboxylate synthetase PP2Cs 2C Protein phosphatases PYR/PYL/RCAR Pyrabactin resistance/pyrabactin resistance-like/regulatory component of ABA receptors RCAR Regulatory component of ABA receptor ROS Reactive oxygen species SAG12 Senescence associated gene12 SDR/ABA2 Short-chain alcohol dehydrogenase/reductase SnRK2s Sucrose nonfermenting 1-related protein kinase type 2 SOD Superoxide dismutase UFGT UDP-glucose:flavonoid 3-Oglucosyl transferase WOX5 Wuschel related homeobox5 XDH Xanthine dehydrogenase ZEP Zeaxanthin epoxidase

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1  Introduction Climate change impacts have imposed challenges to search tools that allow improving plant growth, development, and crop yield under abiotic stresses (Wani and Kumar 2015; Dar et al. 2017; Sah et al. 2016). Therefore, identifying the mechanisms by which plants respond to the abiotic stresses is one of the critical challenges leading to sustainable agriculture, including the development of climate-smart crops and resilient to climate change (Ma et al. 2015; Sah et al. 2016; Dar et al. 2017). According to several studies, abiotic stresses trigger many physiological, biochemical, and molecular responses, influencing various cellular processes in plants (Wang et al. 2001, 2003; Sah et al. 2016; Dar et al. 2017). To cope abiotic stresses, phytohormones have been proposed as a novel and dynamic engineering approach, which could improve the productivity of plants as they are the key regulators of plant growth and development, mediating environmental stress responses (Sreenivasulu et al. 2012; Sah et al. 2016; Trivedi et al. 2016; Checker et al. 2018). Among phytohormones, abscisic acid (ABA) is the central regulator of abiotic stress resistance in plants, coordinating several functions of plants to cope with different stresses (Finkelstein 2013; Wani and Kumar 2015; Sah et al. 2016; Dar et al. 2017). In addition, ABA also plays important roles in the synthesis of biomolecules, embryogenesis, stomatal closure, leaf senescence, germination, seed development, and root architecture (Zeevaart and Creelman 1988; Trivedi et al. 2016). Under osmotic stress, ABA stimulates short-term responses as stomatal closure, regulating water balance and long-term growth responses, regulating stress-­ responsive genes in plants (Sah et al. 2016; Trivedi et al. 2016; Dar et al. 2017). The ABA level significantly increases via ABA biosynthesis under environmental stress conditions, changing gene expression and physiological responses (Kim et al. 2010; Dar et al. 2017), showing induction in the level of the enzymes associated with ABA biosynthesis and relative induction in mRNA leading to ABA accumulation. On the other hand, the upregulation of expression levels of several ABA synthesis genes like zeaxanthin epoxidase (ZEP), aldehyde oxidase (AAO3), 9-cis-epoxycarotenoid dioxygenase (NCED3), and molybdenum cofactor sulfurase (MCSU) have been studied under stress conditions, which can be expressed either through an ABA-­ dependent or ABA-independent pathway (Dar et al. 2017). The major transcription factor families such as bZIP, MYB, MYC, NAC, ERF, and DREB/CBF further control their regulation (Verma et al. 2016). Thus, the role of ABA in stress response has been extensively studied and reviewed (Hashiguchi and Komatsu 2016; Sah et al. 2016; Verma et al. 2016; Dar et al. 2017); therefore, the chapter attempts to underline the biosynthesis, signaling, and transport of ABA and its role in different physiological, biochemical, and molecular responses of plants under adverse environmental conditions.

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2  Functions of ABA in plants Plant growth and development are regulated by several signals into the cell, as well as by some environmental stimuli. In this context, one of the most important regulators is the sesquiterpenoid abscisic acid (ABA) (Xiong and Zhu 2003). This phytohormone plays a role in several physiological processes like seed development, bud dormancy, seed germination, vegetative growth, cuticular wax accumulation, water shortage, stomatal regulation, osmotic regulation, xylem fiber differentiation, and environmental stress responses, among others (Campbell et al. 2018; Yoshida et al. 2019; Chen et al. 2020). Abscisic acid can be synthesized in plants through indirect ways known as carotenoid pathways. Nonetheless in fungi, ABA is synthesized through the mevalonate pathways, more known as direct ways (Izquerdo-Bueno et al. 2018; Takino et al. 2018; Chen et al. 2020). The assays about ABA functions in plants started many years ago, for example, with studies about the maintenance of bud dormancy in potatoes (Hemberg 1949), followed by substances that controlled the abscission of the cotton fruit (Ohkuma et al. 1963), which more recently has confirmed that ABA provoked leaf senescence and abscission independent of ethylene (Zhao et al. 2016). At the present time, the researches focus on the role of ABA in stomatal regulation. This last process is crucial for gas exchange and transpiration in plants; here ABA has an important function in the closure of stomata by regulating guard cells in association with calcium (Ca2+) levels into the cell (Yoshida et al. 2019; Chen et al. 2020). In addition, ABA-induced stomatal closure regulated ion channels in guard cell membranes, more specifically actuating on a slow-type anion channel SLAC1, which is key for stomatal closure in response to several signaling like ABA and CO2 concentration (Ng et  al. 2014). Otherwise, using reverse genetic analysis with mutant ABA-deficient demonstrated a delayed fiber production, due to the reduced expression of genes associated with fiber formation in aba1 mutant in Arabidopsis, which suggested an essential role for ABA in the regulation of xylem fiber differentiation (Campbell et  al. 2018). In the last years, it has been well documented that ABA is involved in the transcriptional and posttranscriptional regulation of several processes; for example, great advances have been made on the mechanism of high ABA concentration, inhibiting root growth (Sun et  al. 2018). Other molecules as ethylene, ROS, and Ca2+ are involved in the mediate processes, and the functions have been known (Bai et al. 2009; Li et al. 2017). Many evidences have shown that high ABA concentration inhibits the cell division in the apical meristem, as well as represses cell expansion in the elongation zone in roots (Bai et  al. 2009; Takatsuka and Umeda 2014; Yang et  al. 2014). Some receptors of ABA signaling in Arabidopsis have been identified to be involved in this last function, such as PYR/PYL/RCAR (Pyrabactin resistance1/ PYR1-like/Regulatory component ABA receptor) ABA receptors, type 2C protein phosphatases (PP2Cs), ABI1 and ABI2 (ABA-insensitive1 and 2), HAB1

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(Hypersensitive to ABA1), Ca2+-dependent protein kinases (CPKs), G proteins, ROS, Ca2+, and transcriptions factors, among others (Cutler et al. 2010; Sah et al. 2016). In fact, except 14 AtPYR ABA receptors in Arabidopsis, many of them regulate ABA inhibition of primary root formation (Sun et al. 2018). On the other hand, ABA can inhibit root growth affecting the auxin accumulation, transport, and signaling; here the PIN family has eight member in Arabidopsis, where the PIN1 to PIN7 are key in root growth and auxin also downregulated WOX5 (Wuschel Related Homeobox5) expression, crucial in root development in plants (Petricka et al. 2012; Mähönen et al. 2014). Abscisic acid has also an important role in the acceleration of leaf senescence through the transcriptional regulation of Oresara1 (ORE1) and Senescence Associated Gene12 (SAG12); these two genes are induced during senescence, and these are transcriptionally activated by ABA signaling (Zhao et al. 2016). With respect to abiotic stress conditions, such as drought or salinity, ABA can induce genes that codified proteins involved in the stress tolerance using dehydrins which are member of Late Embryogenesis Abundant (LEA) proteins, enzymes that detoxify ROS, and regulatory proteins like transcriptions factor, proteins phosphatases and kinases (Ng et  al. 2014). Otherwise, Lim and Lee (2019) reported the functional characterization of RCAR5/PLY11 in response to cold stress in Arabidopsis; these authors suggested that RCAR5 functions in response to cold stress delaying seed germination through ABA-dependent and rapid induction of stomatal closure by ABAindependent pathways. Finally, ABA phytohormone has a crucial role in the regulations of the plant growth, development, and responses to environmental stress. Currently, significant advances have been discovered related to different elements in pathways, such as new receptors, transcription factors, genes, and proteins, among others. These findings have been allowed to understand the complex networks of function, where are involved abscisic acid in all plants.

3  ABA Biosynthesis, Transport, and Signaling As we mentioned above, ABA is the main phytohormone regulating different plant responses under environmental stresses such as heavy metal, low temperature, high radiation, and drought (Zhang et  al. 2014; Vishwakarma et  al. 2017; Zhou et  al. 2020). Under these conditions, plants quickly accumulate ABA activating several stress responses; on the contrary, when the environmental conditions are optimal, ABA is reduced to the basal levels, promoting optimal growth. The balance between defense responses and growth processes is very important in plants under stressed environments, being the ABA modulation levels in tissues and cells a key and critical factor. Thus, ABA levels are controlled by synthesis and degradation, metabolism, conjugation, and transport at the plant.

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3.1  Biosynthesis ABA is a sesquiterpenoid molecule classified as isoprenoid with fifteen carbon (C-15) in their skeleton, which derivate from isopentyl molecule (Xiong and Zhu 2003; Cutler et al. 2010; Ruiz-Sola and Rodríguez-Concepción 2012; Finkelstein 2013). The ABA is biosynthesized by the methylerythritol phosphate (MEP) pathway or “indirect pathway,” which takes place in plastids (Trivedi et  al. 2016; Dejonghe et al. 2018). The first step in ABA biosynthesis is the production of carotenoids. In fact, ß-carotenoid deficient mutant plants are deficient in ABA biosynthesis, negatively affecting drought tolerance (Maluf et  al. 1997; Du et  al. 2013). Interestingly, Diretto et  al. (2020) showed that manipulation of the Lycopene ß-Cyclase (LCYb) gene (overexpression), which is involved in β-carotene biosynthesis, resulted in higher ABA levels in Solanum lycopersicum plants, which could be used as a tool for improving drought stress tolerance. After the production of carotenoids, two steps of epoxidation occurs catalyzing trans-zeaxanthin to trans-violaxanthin by zeaxanthin epoxidase (ZEP) enzyme (Finkelstein 2013), then trans-violaxanthin is converted into two possible products, cis-violaxanthin or trans-neoxanthin (Trivedi et al. 2016). According to North et al. (2007), Arabidopsis ABA4 could catalyze the conversion of trans-violaxanthin to trans-neoxanthin under drought stress. Then, the production of cis-isomers of violaxanthin and neoxanthin could involve two enzymes, neoxanthin synthase and an isomerase (Vishwakarma et al. 2017); however, isomerases to form 9-cis-isomers of violaxanthin and neoxanthin are still unknown (Dejonghe et al. 2018). Thus, 9-cis-­ neoxanthin could be the substrate for 9-cis-epoxycarotenoid dioxygenase (NCED) (North et al. 2007). The NCED is then cleaved into xanthoxin by the NCED enzyme, which is a key regulatory step for ABA biosynthesis under drought stress (Nambara and Marion-Poll 2005; Finkelstein 2013; Sussmil et al. 2017). In fact, a high correlation between ABA levels and NCED gene expression has been reported when plants are subjected to drought stress (Karppinen et  al. 2013; González-Villagra et al. 2018). Xanthoxin is a fifteen-carbon molecule (C15), which is then transferred to the cytosol to produce abscisic aldehyde, which is catalyzed by the short-chain alcohol dehydrogenase/reductase (SDR/ABA2) (Cheng et  al. 2002; González-­ Guzmán et al. 2002). Finally, the abscisic aldehyde is converted to ABA by abscisic aldehyde oxidase, which is encoded by the ABA3 locus in Arabidopsis and requires a molybdenum (Mo) cofactor for enzyme activity (Finkelstein 2013).

3.2  Transport Plant life cycle (e.g., development) and environmental conditions modulate ABA biosynthesis, changing its levels dramatically. Indeed, and similar to hormones in animals, most phytohormones such as ABA, are mobile, which implies that biosynthesis sites and action are separated in cells and/or tissues. For this reason, the ABA

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transport throughout the whole plant is an essential process for its effective plant signaling. The first step is the coordinated regulation of biosynthesis and transport of ABA within a plant. Recent studies have reported multiple sites of ABA biosynthesis, including root/leaf vascular tissues and guard cells under drought stress (Kuromori et  al. 2018), but also multiple ABA transporters have been identified (Kuromori et al. 2010; Boursiac et al. 2013). ABA transport regulation is not unidirectional, and plants are equipped with a highly sophisticated system to sense and respond to external stimuli under diversely fluctuating environments. Therefore, ABA concentration depends on biosynthesis, degradation, compartmentation, and/or conjugation, but also depends on the stimulus that induces ABA biosynthesis and its translocation to other sites or plant tissues. Here, we focused on its important role during seed development, dormancy, and acclimation to abiotic stresses. Related to the importance of ABA during seed development and dormancy, ABA acts as an essential repressor of seed germination under unfavorable conditions (Holdsworth et al. 2008). In Arabidopsis, it has been shown that the endosperm, a single cell layer surrounding the embryo, synthesizes and continuously releases ABA toward the embryo. Kang et al. (2015a) described that four AtABCG transporters act in concert to deliver ABA from the endosperm to the embryo: AtABCG25 and AtABCG31 export ABA from the endosperm, whereas AtABCG30 and AtABCG40 import ABA into the embryo. On the other hand, ABA is also essential in multiple abiotic/biotic cross talk responses. Under drought and/or salt stresses, ABA is synthetized de novo in leaves protecting against loss of water (Schwartz and Zeevaart 2010). According to the most studies about drought responses, cytosolic ABA increases due to de novo biosynthesis in leaves, redistributing within the mesophyll cell, import from the roots, and recirculation from other leaves. When optimal water conditions are re-­ established levels of ABA decrease because of degradation and export from the leaf, as well as biosynthesis decrease, particularly, ABA synthesized in the roots can also be transported to the shoot via the xylem, and its concentration can range from 15 nM to 3000 nM, under well-watered sunflower plants or water-stressed conditions (Schurr et al. 1992). Root-to-shoot signaling under drought stress suggests that ABA synthesized in roots is released to xylem vessels and transported to shoots. Because ABA is a weak acid containing a carboxyl group (pKa = 4.7), it exists in solution in the protonated or deprotonated form, with the proportion of each determined by the pH. An increase in xylem sap pH in response to soil drying has been observed in many plant species, which could enable ABA to move more freely through extracellular space toward guard cells according to the transpiration stream, because a smaller amount of ABA would be trapped by surrounding cells during transport than under lower pH conditions (Taiz and Zeiger 2006; Jia and Davies 2007; Boursiac et al. 2013). ABA is also transported within cells; the designation of the four typical ABA transporters like AtABCG25, AtABCG40, AtNPF4.6, and AtDTX50 is supported by several lines of evidence (Kuromori et al. 2018). All four proteins are localized to plasma membranes, implying the involvement of ABA transfer between the

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inside and outside of cells. Interestingly, these transporter genes are predominantly expressed in vascular tissues or guard cells, strongly indicating that ABA transport is regulated in a network spanning distant tissues related to the site of biosynthesis and the site of physiological actions. Indeed, other ABA transporters like abscisic acid (ABA)-importing transporter 1 (AIT1) contribute to protect against metal stress mediating the inhibition of Cd accumulation (Pan et al. 2020).

3.3  Signaling A resilient status is described by the capacity to absorb disturbances, keeping their characteristics of structure, dynamics, and functionality practically intact, being able to return to the situation prior to the disturbance when it disappears. In this context, plant responses to be adapted under adverse environments relies on their complex signaling mechanisms develop in response to that external stimulus (disturbances or environmental stressors) surviving plant species that respond best to change. The main stress related-phytohormone, ABA, plays an essential role in harsh environments. For decades, several studies have revealed many physiological responses modulated by ABA during drought conditions that favor the plant potential to survive under adverse environments, but also this phytohormone regulates other physiological processes. First studies using the exogenous application of ABA observed the induction of several genes in plants with other functions than abiotic stress responses (Mundy and Chua 1988). Currently, it is well documented that ABA-signaling pathway is based on the perception of the stimulus and transmission to activate several of the downstream plant processes (Fujii et al. 2009; Park et al. 2009; Rajasheker et al. 2019). It includes three protein classes, namely pyrabactin resistance (PYR)/pyrabactin resistance-like (PYL)/regulatory component of ABA receptor (RCAR), which regulate protein phosphatase 2C (PP2C) negatively, and the positive regulators sucrose nonfermenting 1-related protein kinase type 2 (SnRK2s). Low levels of ABA inactivate SnRK2s by PP2Cs (Umezawa et al. 2010), ABA binds to PYR/PYL/RCAR receptors, and these undergo conformational change that allows the binding of PP2C (Seiler et al. 2014). Therefore, ABA-induced inhibition of PP2Cs leads to phosphorylation of SnRK2 and its activation. SnRK2s then can phosphorylate downstream proteins like ion channels, NADPH oxidases, and others (Sah et  al. 2016). While a Raf-like kinase (B3-MAPKKK) activates SnRK2, a casein kinase 2 phosphorylates SnRK2’s carboxyl-terminal serine residues. This enhances SnRK2-PP2C interaction, and thus ABA can bring about activation of several of the downstream events. This regulation is well described in ABA and drought stress section. In the other hand, several candidates involved in root-to-shoot signaling under drought stress have been proposed. Tension in the vascular system caused by water deficit has been reported to act as a hydraulic signal which induces ABA synthesis in leaves (Christmann et al. 2013), and others such as pH or some chemical agent

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(Kuromori et  al. 2014). But, interestingly, small peptides mediating this abiotic stress signal had been characterized recently (Takahashi et al. 2018; Yoshida and Fernie 2018). They reported a root-derived small Clavata3/Embryo-Surrounding Region-related (CLE) peptide, CLE25, that serves as such a signal. Application of CLE25 to roots was shown to remotely induce foliar expression of the key ABA biosynthetic enzyme gene, NCED3. Consistent with this, both ABA levels and stomatal closure were also enhanced (Takahashi et al. 2018). CLE25 is expressed in root/leaf vascular tissues, but only root expression was enhanced following dehydration. In most cases, CLE peptides are recognized by receptors belonging to subclass XI of the leucine-rich-repeat receptor-like kinases, including CLV1 and BAM1-3 (Deyoung et al. 2006). Takahashi et al. (2018) screened several mutants of receptor-like kinases and found that dehydration-responsive expression of NCED3 was reduced in the bam1-5 bam3-3 double mutant. This double mutant also displayed reduced levels of ABA in leaves after dehydration, as well as decreased tolerance to dehydration. In brief, understanding the complex network between ABA biosynthesis, transport, and signaling allows the management for resilient agriculture improvement and ecosystems conservation under changing climate conditions.

4  A  BA and Its Role Under Adverse Environmental Conditions Abscisic acid has been recognized as part of the abiotic stress phytohormone (Dar et al. 2017), since its level commonly increases, enhancing plant adaptation to various abiotic stresses (Sah et al. 2016). In the following sections, we will discuss the role of ABA under stresses from drought, salinity, and heavy metals.

4.1  ABA and Drought Stress Approximately 67% of crop losses were reported in the USA due to drought stress during the last 50 years (Comas et al. 2013). Drought stress induces stomatal closure in plants, which limits CO2 uptake by the leaves, reducing the potential activity of Calvin-Benson cycle enzymes, particularly ribulose-1,5-­bisphosphatecarboxylase/ oxygenase (Rubisco), due to lack of substrate (Chaves et al. 2003; Morales et al. 2020). Thus, the photosynthesis process is the main physiological target limited by drought stress. However, plants have developed morpho-physiological, phenological, biochemical, and molecular mechanisms to maintain constant cellular water potential and/or relative water content (Basu et al. 2016). In fact, the first mechanism in plants to maintain water status is the stomatal closure, which is crucial for decreasing water loss and plant survival under drought stress conditions (Hajihashemi

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2020). ABA has a significant role in regulating physiological processes, mainly under drought stress, and its synthesis occurs upon signal perception during stress conditions (Hajihashemi 2020). The main physiological process influenced by ABA levels is stomatal closure, reducing water loss, and limiting photosynthesis processes (Ullah et al. 2018). It is known that photosynthesis and transpiration decrease slowly in the field at a similar rate in response to season, duration, and sternness of drought stress. Rowe et al. (2016) reported that ABA regulates root growth under osmotic stress conditions. At low water potential, ABA accumulation is essential for Zea mays root elongation. Several studies indicated that ABA biosynthesis is mainly regulated by the 9-cis-epoxycarotenoid dioxygenase (NCED) gene under drought stress, which encodes a key enzyme involved in its biosynthesis (Luchi et al. 2001; Finkelstein 2013; Jan et al. 2019). Thus, a strong positive correlation between NCED gene expression and ABA accumulation (r  =  0.98) was reported in Aristotelia chilensis subjected to drought stress (González-Villagra et  al. 2018). It has been shown that ABA also modulates downstream ABA-inducible genes, which are involved in drought stress tolerance mechanisms such as synthesis of compatible osmolytes, protectant proteins, and enzymatic antioxidant (Finkelstein 2013). González-Villagra et al. (2019) also reported that ABA is involved in anthocyanins biosynthesis in A. chilensis leaves subjected to drought stress. They showed by molecular studies that de novo ABA biosynthesis triggers high UDP-­ glucose:flavonoid 3-Oglucosyl transferase (UFGT) gene expression, which encodes a key enzyme involved on anthocyanin biosynthesis in A. chilensis subjected to drought stress.

4.2  ABA and Salt Stress Salt stress has become a real concern during the last years because of some agricultural management and process going on due to climate change. It occurs in arid and semiarid regions, increasing soil salinity by around 10% annually because of low precipitation, high surface evaporation, and weathering of native rocks, among other factors (Jamil et al. 2005; Isayenkov and Maathuis 2019). As drought, high salinity stress generates osmotic stress in plant cells and also produce ion toxicity by the excessive uptake of Na+ and Cl− ions, oxidative damage, and therefore inducing a reduction in photosynthesis, respiration, metabolism, and plant growth (Abogadallah 2010; Isayenkov and Maathuis 2019). Stomata play an important role in salt stress tolerance (Rajendran et al. 2009; Rahnama et  al. 2010; Barbieri et  al. 2012). NaCl induces Abscisic Acid (ABA)mediated stomatal closure to reduce water loss (van Zelm et al. 2020). ABA is synthesized in the vasculature and in the guard cells of the vegetative part of the plant to be later transported and sensed (Boursiac et  al. 2013). At the leaf level, ABA influences growth and has been widely described in guard cells, where it closes stomata (Tardieu et al. 2010; Hauser et al. 2011). Under salt, Cucurbita maxima, a tissue-tolerant salt species, rapidly close stomata at early stages of salt stress,

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avoiding water loss, attributed to a high accumulation of ABA in the mesophyll together with a high expression of NCED3 gene. This was then complemented with an exclusion mechanism, were Na+ was sequestrated in the xylem parenchyma and cortex of the leaf vein, and therefore avoiding the income of Na+ to the leaf mesophyll (Niu et al. 2018). Grafting experiments confirm that stomatal closure does not rely on ABA production in the root in tomato under drying soil but to a possible signal from roots leading to change apoplastic ABA (Holbrook et al. 2002). Under salt, grafting cucumber onto pumpkin showed a root-source ABA signal leading to decrease stomata opening and transpiration, showing grafting and control similar ABA synthesis, but under the cucumber onto pumpkin grafting, increased sensitivity to ABA incremented salt tolerance in cucumber (Niu et al. 2019). As mentioned before, ABA is known to be synthesized in the different organs and transported to guard cells for stomatal closure. The principal ABA biosynthetic genes have shown to be upregulated in the roots within 3  h of salt treatments (140 mM NaCl) in Arabidopsis (Geng et al. 2013). Mild salt stress (50 mM NaCl) in pea root cells increases ABA together with lipid transfer proteins, which may participate in stress-induced pea root suberization or transport of lipid molecules in the phloem (Akhiyarova et  al. 2019). The increase of suberin, a waxy substance deposited between the cell wall and the plasma membrane, under salt stress conditions, can regulate the in and out of water and solutes, including Na+. Suberin development is controlled by ABA, which increases depending on endodermal ABA signaling (Barberon et  al. 2016). Furthermore, under high salinity, endodermal ABA root signaling promotes an extended quiescent phase in postemergence lateral roots, suppressing for several days the growth rate before recovering in Arabidopsis seedlings (Duan et al. 2013). So, the importance of reducing the hydraulic conductivity in response to salt could be considered important for plants as much as the stomatal regulation on the leaves, preventing in some point the free import of Na+ or water backflow into the soil (van Zelm et al. 2020). It seems that whether the mechanism is focused on tolerating salinity through the shoot Na+ exclusion or by tissue tolerance excluding Na+ out from the mesophyll, the early mechanism to prevent water loss is directed by ABA closing stomata. Early studies in Arabidopsis plants have shown that among the biosynthetic genes, the most responsive to NaCl is NCED3. The study of ABA-deficient mutants has shown the existence of a NaCl-dependent but ABA-independent pathway for the induction of NCED3, AAO3, and ABA1, being NCED3 predominant. However, the ABA-dependent pathway also induces predominantly NCED3 in Arabidopsis (Barrero et al. 2006). This is because in the ABA biosynthetic pathway, NCED is the rate-limiting enzyme (Huang et al. 2018). Salt stresses can trigger responses from the ABA-signaling pathway inducing de novo ABA biosynthesis (Xiong and Zhu 2003; Ruiz-Sola et al. 2014). It has been found that Salt-Related MYB1 (SRM1) transcription factor coordinates ABA biosynthesis and signaling in Arabidopsis under salt stress (200 mM NaCl) during seed germination and seedling development (Wang et al. 2015). Another transcription factor, PtrSSR1, a salt-stress-regulator in the Populus trichocarpa R2R3 MYB gene family, has shown to increase salt tolerance in Arabidopsis by integrating the regulation of lateral root emergence and ABA

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signaling under salt. Poplar species (Populus spp.) are used as a model to study salt stress mechanisms in trees because of their salt tolerance and fully sequenced genomes. Poplars salinity tolerance has been described from cellular and whole plant level (Chen and Polle 2010; Chen et al. 2014; Zhang et al. 2019). Research with transgenic Poplar plants altered in aldehyde oxidase AO (which catalyze the last step in ABA biosynthesis) and ABA3 (essential for activation of the molybdenum enzymes AO and xanthine dehydrogenase XDH) RNAi knockdown and overexpression has shown that these enzymes catalyze critical steps in ABA synthesis under high salt conditions. However, the initial increase of ABA dropped to basal levels after 40 h of salt stress, which means that the primary issue for plants is to handle with the water loss, but under prolonged stress, plants can acclimate (or adapt) to the stress conditions undergoing long-term stress responses (Hamisch et al. 2016 and references therein). The combination of tissue-specific ABA (e.g., as shown in De Zio et al. 2019) and high-resolution ABA reporters (e.g., synthetic transcriptional reporter by Wu et al. 2018, highlighted by Hayes 2018) could elucidate how ABA moves throughout the plant to determine ABA origin and spatial regulation under salt. Further analysis needs to go in that direction to understand gaps in ABA signaling and regulation to increase salt tolerance in sensitive plant species.

4.3  ABA and Heavy Metal Stress During their existence, plants can be affected by toxic metals that can limit their growth, and in agricultural areas affecting severely crop productivity. Levels of some heavy metals can be high due to human activities in natural and agricultural areas (Chowdhury et al. 2016). Growing evidence has confirmed that phytohormone abscisic acid (ABA) plays a crucial role in the heavy metal alleviation and metalloid stresses in plants (Hu et al. 2020). The abscisic acid concentration in plant tissues increases under heavy metal exposures, such as Cd, Cu, Zn, As, and Al (Shukla et  al. 2017; Vishwakarma et  al. 2017). The relevance of these elements not only relies on their direct detrimental effects on plants, but also into their toxicity, accumulating in the food chain, being a major threat for human since some of them, such as As and Cd, are toxic and carcinogenic (Chary et  al. 2008; Zhao et  al. 2010; Shukla et al. 2017). Commonly, Cd can increase in soil because of mining activities, burning, industries, waste seepage, and fertilization in fields with sewage sludge and phosphate (Kubier et al. 2019). The most important factor in the soil for Cd availability is pH, controlling the uptake in plants, with a low pH favoring Cd accumulation (Kirkham 2006). Endogenous ABA has shown the increase under cadmium (Cd) in several plant species such as of Typha latifolia (Fediuc et al. 2005), Oryza sativa roots and leaves (Hsu and Kao 2003), and Solanum lycopersicum (Pompeu et al. 2017). Cd supply induced the expression of NCED1 and endogenous ABA synthesis on Solanum tuberosum plants. This, in turn, leads to an increased synthesis of

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phytochelatins (which can bind to Cd ions) through induction of the expression of the phytochelatin synthase (PCS) gene. The application of the ABA biosynthesis inhibitor fluridone showed that in the Cd induction of the PCS gene necessarily need a proper endogenous concentration of ABA, suggesting that the Cd-signaling pathway is linked to the ABA-signaling pathway (Stroiński et al. 2013). Another case comparing rice Cd-tolerant (TNG67) and Cd-sensitive (TN1) cultivars shed more light into Cd tolerance. The endogenous ABA in leaves and roots increase rapidly in the tolerant cultivar under Cd treatment, and when ABA was supplied exogenously, the sensitive cultivar decreased Cd content and transpiration, enhancing tolerance. When fluridone was supplied, it reduced the tolerance of the TNG67 cultivar, and this could be reversed by the exogenous supply of ABA (Hsu and Kao 2003). So, the regulation of endogenous ABA levels can reduce Cd uptake in rice seedlings (Hsu and Kao 2008). By comparing Micro-Tom (MT) sitiens ABA-­ deficient tomato mutants (sit) and the wild-type MT, it was confirmed that ABA is part of the Cd stress signaling in tomato. The mutant accumulated more Cd in the roots compared to the wild-type counterpart (Pompeu et al. 2017). A decrease of Cd in the presence of exogenous ABA in Arabidopsis was associated with the inhibition of Iron-Regulated Transporter 1 (IRT1), a divalent cation transporter of broad-­ spectrum in roots (Fan et al. 2014). Copper is a different story since it is a micronutrient; plant needs to ensure adequate amounts of it to ensure a normal growth development. ABA can affect copper uptake to ensure homeostasis of Cu, and this has been well described by Carrió-­ Seguí et al. (2016). However, a slight excess of Cu can be very harmful to the plants (Dey et al. 2014). Seed germination is sensitive to Cu stress. It has been found that Cu suppresses ABA catabolism in rice, by reducing the expression of OsABA8ox2, increasing ABA content in seed (Ye et al. 2014). Under Cu stress, GPX6 form, a redox related gene of glutathione peroxidase encoding cytosolic and mitochondrial isoforms, is shown to be upregulated in Arabidopsis (Milla et al. 2003). The accumulation of proline (an important osmolyte and ROS scavenger) mediated by ABA has been described under abiotic stress (Strizhov et al. 1997; Cao et al. 2020). In detached O. sativa leaves, ABA has been suggested to mediate the accumulation of proline under Cu stress (Chen et al. 2001). Under long-term exposition to Cu stress in Populus deltoides PE19/66 clones, the tolerance strategy (accumulating Cu at the root level) seems to rely on proline accumulation and ABA levels in shoots and roots (Kebert et  al. 2017). More research on the mechanism by which ABA can modulate proline accumulation under Cu stress needs to be investigated. Zinc toxicity is very uncommon stress. However, it has become more frequent due to soil pollution by industrial activities such as mining, coal and steel processing, and other activities such as the application of biosolids and manures (Wuana and Okieimen 2011). Zn toxicity depends on pH, which controls the concentration of zinc in soil solution. Abscisic acid exogenously applied has shown to alleviate zinc toxicity in Vitis vinifera seedlings exposed to excess (10 mM) of Zn by reducing the uptake and accumulation in roots and inducing higher expression of both Zrt and Irt-like protein (ZIP) family transporter genes and detoxification-related genes in root and leaf (Song et al. 2019).

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Aluminum is one of the main metals affecting the growth and productivity of plants worldwide in acid soils. Al3+ is the most toxic form, and it is released to the soil solution when the pH drops below 5 (Panda et al. 2009). Aluminum phytotoxicity affects primarily roots, blocking the mechanism of cell division, inhibiting root growth, and leading to poor ion and water uptake. An increase in ABA biosynthesis is directly related to an increase in toxic Al at low soil pH, showing a concomitant increase in Al doses and endogenous ABA levels in the root apex of Glycine max plants (Hou et  al. 2010; Reyna-Llorens et  al. 2015). Application of fluridone in plants exposed to Al toxicity reduced ABA accumulation and root growth, suggesting that ABA inhibition increased the negative effect at lower Al (30 μM) concentration in G. max roots (Hou et  al. 2010). Therefore, this author concluded that Al toxicity may accelerate ABA transport from roots to leaves, suggesting that ABA could be involved in increasing plant tolerance to Al toxicity. However, the current knowledge about the role of ABA in high Al-stressed plants has to be further investigated. It has been proposed that the increase in ABA accumulation in response to heavy metal stress may increase plant tolerance via two different ways: (1) reduction of metal uptake and translocation from root to shoot, which is due to stomatal closure (Kang et al. 2010), and (2) modification of gene expression, contributing to heavy metal tolerance (Perfus-Barbeoch et al. 2002). It was reported that both Al and ABA induced the expression of FeALS3 gene in Fagopyrum esculentum (Reyna-­ Llorens et al. 2015), which is implicated in Al tolerance, facilitating Al compartmentation. While the ABA role in plant Al-stress response has been well characterized, the relationship between Al stress and ABA signal transduction pathways remains largely unknown. Thus, ABA can be an important factor for increasing plant tolerance to Al toxicity via Al-induced organic acid production and can be a key factor in determining the degree of plant tolerance to Al toxicity (Reyes-Díaz et al. 2016). ABA and indole acetic acid (IAA) could induce AtALMT1 gene expression, relating Al signaling to phytohormone-mediated signal transduction pathways (Kobayashi et al. 2013). Interestingly, an in silico analysis also identified an ABA-­ responsive element in the promoter region of VuMATE1 (Liu et al. 2016). In Vigna umbellata, ABA was positively involved in Al tolerance mechanisms, and it was independent of known Al tolerance mechanisms, including Al-mediated organic acid anions efflux (Fan et al. 2019). Therefore, whether and how this hormone regulates the genes encoding transporters of organic acids under Al toxicity is still unclear.

5  Exogenous ABA Application and Resistance Mechanisms Plants living in stressful environments are subject to oxidative stress damage (Bücker-Neto et al. 2017). ABA increases as a result of osmotic stress and plays a central role in enhancing the efficient use of water and the plant response to drought, salinity, metal, and cold stresses (Aroca et al. 2008; Zhang et al. 2012; Bücker-Neto et al. 2017). In plant under stress, application of ABA could help to reduce damage

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Fig. 1  Impact of ABA on physiological and biochemical responses of plant under stress condition

by stomatal closure, osmotic adjustment, and increasing activities of antioxidant enzymes (Teng et al. 2014; Fig. 1). Exogenous ABA in some studies has been demonstrated to have a relationship with photosynthesis, so it is important to measure chlorophyll content, photosynthetic rate, stomatal conductance, and transpiration rate in order to determine ABA availability to alleviate photosynthetic damage in plants induced by stress (Lei et al. 2007; Shi et al. 2015; Chen et al. 2018; Fig. 1).

5.1  Drought Stress As we mentioned above, ABA is synthetized under different environmental stresses, regulating physiological, biochemical, and molecular responses in plants. Thus, ABA application has been suggested as a tool for improving drought stress tolerance (Fig. 1); however, the mechanism of foliar ABA uptake in plant organs is still unknown (Aroca et al. 2008; Sandhu et al. 2011; Teng et al. 2014; Gai et al. 2020). Although there are two possible ways for ABA uptake in plant organs; some authors have suggested that exogenous ABA could penetrate in leaves through the epidermal cells or throughout stomatal pore into the leaf (Eichert and Burkhardt 2001; Eichert et al. 2006; Wheeler et al. 2009; Sandhu et al. 2011). Thus, ABA could be recognized by ABA receptors inside the cells and activate downstream signaling,

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hence activating drought stress responses. Nevertheless, more studies are needed to have a complete understanding of exogenous ABA uptake for plant organs. ABA application for improving drought stress tolerance is still controversial, and different plants responses are observed (Table 1). Some authors have reported that ABA application improves drought stress tolerance in plants (Table  1). For example, Travaglia et al. (2010) and Hussain et al. (2010) reported that 5 μM of ABA application increased grain yield in T. aestivum and Helianthus annuus plants subjected to drought stress (Fig. 1). Likewise, Du et al. (2013) showed that 10 μM ABA application did not increase grain yield in T. aestivum; however, ABA application increased water-use efficiency for grain yield due to a reduction in water use during plant growth (Fig. 1). Similar results were reported by He et al. (2019), where ABA application (10 μM) did not increase crop yield in G. max subjected to drought stress; however, the authors showed that exogenous ABA induced osmotic adjustment, improving leaf water relations and water use efficiency. In contrast, other authors have reported that ABA application reduces plant growth. For example, Yin et al. (2004) showed that 5 μM ABA application to leaves decreased stomatal conductance, transpiration, as well as photosynthesis, which finally reduced plant growth and total biomass in Poplar kangdingensis and Poplar cathayana plants. Likewise, Pandey et al. (2003) showed that 5 μM ABA application reduced photosynthesis, stomatal conductance, and transpiration in Gossypium hirsutum plants subjected to Table 1  Effects of ABA application in plant species subjected to drought stress

Species Zea mays Capsicum annum

ABA concentration/ tissue Conditions 100 μM applied Greenhouse to roots 1 μM applied to Greenhouse leaves

100 μM applied to roots Solanum 100 μM applied lycopersicum to leaves Triticum aestivum 5 μM applied to leaves Helianthus annuus 5 μM applied to leaves 5 μM applied to Poplar leaves kangdingensis, Poplar cathayana Zea mays

Fragaria x ananassa

Effects Increased relative water content and shoot growth Plant growth inhibition

Greenhouse Not significant changes Greenhouse Enhanced plant growth Greenhouse Increased grain yield Greenhouse Increased grain yield

References Zhang et al. (2012) Leskovar and Cantliffe (1992) Ruiz-Lozano et al. (2009) Aroca et al. (2008) Travaglia et al. (2010) Hussain et al. (2010) Yin et al. (2004)

Greenhouse Reduced photosynthesis, stomatal conductance, transpiration, and plant growth 100 μM applied Field Fruit yield was not affected; Sandhu et al. (2011) to leaves experiment however, phenolic acids, flavonoids, and anthocyanins were increased

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drought stress. In addition, it has been reported that ABA application could inhibit plant or organ growth, resulting in lower crop yields (Li et al. 2010; Sandhu et al. 2011; Ferrara et al. 2013). Therefore, plant responses to ABA application are complex and still controversial, depending on the species and ABA concentration (Table 1). At the physiological level, Li et al. (2020) showed that ABA application decreased stomatal conductance with no changes in CO2 assimilation in Ipomoea batatas plants subjected to drought stress. The authors also showed that ABA application regulated source-sink balance, improving carbon metabolism enzyme activities, mainly sucrose synthase and sucrose phosphate synthase, which regulate the synthesis rates of sucrose and starch, resulting in higher crop yield. Interestingly, Teng et al. (2014) showed that in drought stresses O. sativa plants ABA application significantly enhanced CO2 assimilation due to higher OsPsbD1 and OsPsbD2 gene expression, which encode the D1 and D2 proteins related to photosystem II.  At biochemical level, plants subjected to drought stress synthesize proline, which is an osmolyte that supplies energy for growth and reduces lipid peroxidation (Chun et al. 2018). Thus, Kaur and Asthir (2020) reported that ABA application increased proline levels in drought-stressed T. aestivum plants throughout the glutamate pathway, triggering the high activity of glutamate dehydrogenase and Pyrroline-5-Carboxylate Synthetase (P5CS), conferring drought stress tolerance. In fact, Sripinyowanich et al. (2013) reported that P5CS was overexpressed in drought-stressed O. sativa plants by ABA application. Plants have developed complex mechanisms to tolerate drought stress, such as enzymatic antioxidants and non-enzymatic antioxidant compounds, which counteract the oxidative damage produced by scavenging the reactive oxygen species (ROS) (Zhang et al. 2001; Jansen et al. 2008; Yang et al. 2018). Thus, plants induce enzymatic antioxidant system such as superoxide dismutase and peroxidase enzymes, as well as non-enzymatic antioxidant systems such as phenolic acids, flavonoids, and anthocyanins (Ma et al. 2019). Wang et al. (2010) showed that ABA application improved drought tolerance in Actinidia deliciosa plants by activating antioxidant enzymes such as peroxidase, catalase, superoxide dismutase, ascorbate peroxidase, and glutathione reductase (Fig. 1). Regarding non-­ enzymatic compounds, Gai et al. (2020) reported that flavone, flavonol, isoflavone, kaempferol, and anthocyanins levels, as well as phenylpropanoid pathway genes, were increased after ABA application improving drought stress tolerance in Camellia sinensis plants. Indeed, González-Villagra et al. (2019) reported that ABA is involved in anthocyanin biosynthesis in Aristotelia chilensis plants subjected to drought stress. Interestingly, the authors also showed that ABA application triggered tri-hydroxylated anthocyanin forms, giving a greater antioxidant capacity, which improves the defense mechanism against ROS. Therefore, all these physiological, biochemical, and molecular studies show that ABA application could be used as a strategy to improve drought stress tolerance in plants. However, it is important to be careful with the plant species and ABA concentration for improving drought stress tolerance.

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5.2  Salt Stress Salt stress negatively affects physiological, biochemical, and molecular plant processes, and it is most commonly caused by high concentrations of sodium chloride (NaCl), which alters ion homeostasis (Serrano et al. 1999). ABA accelerates adaptation and improves tolerance to high salinity due to changes in gene expression in stressed tissues and inducing the production of osmoprotectants that can help in cell protection or recovery against salt stress (Amzallag et al. 1990; Aroca et al. 2008; Crizel et al. 2020). Proline is produced as a signaling compound and is considered one of the most important osmoprotectors in plants (Aroca et al. 2008). It has been shown that salt stress induces proline accumulation in different plant species (Table 2), like T. aestivum, Z. mays, and O. sativa, to maintain hydric balance in the cell and helping plant stress adaptation (Aroca et al. 2008; Crizel et al. 2020). In A. thaliana, the accumulation of proline is regulated by P5CS gene, which has been demonstrated to be upregulated by exogenous ABA by increasing transcription of AtP5CS1 and AtP5CS2 that lead to proline accumulation in the plant (Strizhov et al. 1997). In O. sativa subjected to salt stress, this accumulation is increased by the overexpression of OsP5CR, which is produced due to ABA application (Table 2), on a sensitive line (LPT123) and a tolerant line (LPT123-TC171), after 3 and 6 days of Table 2  Effects of ABA application in plant species under salinity stress Species Fragaria x ananassa

ABA dose Conditions 200 μM by foliar Greenhouse spraying

Oryza sativa To the roots at 10 μM

Sorghum bicolor Solanum tuberosum Arabidopsis thaliana Phaseolus vulgaris

8, 40, 160 μM sprayed daily to the leaves 50, 75, 100 μM in the solution

Greenhouse

Greenhouse

Greenhouse

In vitro culture 1 μM added to seed-germination liquid medium 1, 10 μM added Environmental chamber to growth medium

Oryza sativa To the leaves at 100 μM

Greenhouse

Effects Stomata closure, reduction of transpiration and availability of carbon to photosynthesis Affect root growth and development, enhancing root cell viability and water permeability Enhance plant growth and acceleration of adaptation to salinity Increase leaf water content and stomatal conductivity Upregulation of AtP5CS genes which lead to proline accumulation Increase root nodule metabolism improving plant response to salt stress Increase proline accumulation induced by overexpression of OsP5CR genes

References Crizel et al. (2020)

Chen et al. (2006)

Amzallag et al. (1990) Etehadnia et al. (2008) Strizhov et al. (1997) Khadri et al. (2006)

Sripinyowanich et al. (2013)

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the treatment (Sripinyowanich et al. 2013). In the same study, it was shown that in O. sativa P5CS is not clearly upregulated by exogenous ABA, showing that the effect of ABA on proline production induced by gene expression depends on plants species. The photosynthetic machine can be affected by salt stress due to a reduction in chloroplast stroma and photosynthetic pigment loss (Popova et  al. 1995; Crizel et al. 2020). The 200 μM ABA application on Fragaria × ananassa subjected to salt stress also can reduce photosynthetic parameters due to stomatal closure and reduction of CO2 exchange (Crizel et al. 2020). In plants subjected to salt stress, ABA treatment also reduces transpiration, rising xylem water potential, and leaf water content, which improves leaf expansion (Table 2). Application of ABA before exposure to soil salinity can raise water content on leaves and the lateral shoot growth (Fig.  1), through stomatal closure induced by ABA (Etehadnia et  al. 2008). Furthermore, it has been reported that ABA also helps to enhance salt stress tolerance by altering root length and root cortex thickness, and by the formation of root hairs and lateral roots (Chen et al. 2006; Table 1). Increasing water content in leaves and improving root hydraulic conductivity can help to revert the osmotic imbalance caused by high salinity (Etehadnia et al. 2008). Root nodules are symbiotic organs present in legumes that are the result of the interaction between the plant and the soil bacteria and are modulated by phytohormones (Verma et al. 1992). Changes in gene expression induced by ABA content and salt stress affect biomass and enzymatic processes that occurs in nodules (Khadri et al. 2006). In Phaseolus vulgaris root nodules, it has been reported that xanthine dehydrogenase (XDH) and uricase are inhibited by NaCl (100 mM) and ABA (10 μM) added to the growth medium, decreasing purine catabolism (Khadri et al. 2006).

5.3  Metal Stress Metal stress in plants affects the balance of reactive oxygen species (ROS) and causes damage in DNA, proteins, and lipids (Wang et al. 2013; Fan et al. 2014; Lei et al. 2014; Shi et al. 2015; Bücker-Neto et al. 2017; Shen et al. 2017). Application of ABA usually leads to the production of hydrogen peroxide (H2O2) and to expression of certain genes that can activate the antioxidant defense system (Wang et al. 2013). Cadmium (Cd) has been shown to be one of the most toxic metals for plants, animals, and humans (Fan et al. 2014; Shen et al. 2017). Its toxicity is visible as chlorosis in the leaves as a result of the alteration of photosynthetic processes, stomatal function, and electron transport that can generate ROS (Shen et  al. 2017). Some species accumulate Cd in their shoots and roots, mainly in vacuoles chelated with organic acids (Sterckeman and Thomine 2020). Exogenous application of ABA to Cd-stressed plants could increase accumulation in the roots and reduce the

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metal transport from roots to shoots, which prevent damage to photosynthetic organs (Hsu and Kao 2003; Fan et al. 2014; Table 3). Oxidative damage on roots and shoots can be measured in the function of malondialdehyde (MDA) content as a sign of lipid peroxidation and accumulation of H2O2 (Zhao et  al. 2009; Wang et  al. 2013; Shen et  al. 2017). In Atractylodes Table 3  Effects of ABA application in plant species subjected to heavy metal stress Species Brassica campestris

Oryza sativa

Atractylodes macrocephala

Oryza sativa

Populus cathayana

Oryza glaberrima

Populus x canescens

Triticum aestivum

Metal exposition Cadmium (Cd)

ABA dose 5 μM to nutrient solution

Conditions Greenhouse

Effects Enhance Cd accumulation in roots to prevent Cd transportation from roots to shoots Phytotron Reduced transpiration Cd To culture rate and decreased Cd medium at content in shoots 1, 3, 5 μM enhancing tolerance to Cd Lead (Pb) To the Growth Increase level of leaves at 2.5, chamber antioxidant enzymes 5, 10 mg L−1 activity and enhance plant growth, soluble sugars and proteins Pb To the Greenhouse Increase ascorbate nutrient peroxidase and solution at decrease superoxide 0.1, 1, dismutase activity in 10 mg L−1 leaf of plants under Pb stress Greenhouse Protect photosynthetic Manganese 50 μM apparatus by (Mn) sprayed to decreasing manganese leaves transportation from roots to shoots Reduced iron Phytotron Iron (Fe) 200 μM to accumulation in and nutrient shoots and increased greenhouse solution MDA concentration in roots after Fe treatment Decrease SA Climate Zinc (Zn) 10 μM to chamber and concentrations in nutrient leaves and IAA in the greenhouse solution roots and leaves in plants under Zn stress Mercury To nutrient Incubator and Increase activity of greenhouse peroxidase enzyme, (Hg) solution at protecting plant 10 μM against Hg stress

References Shen et al. (2017)

Hsu and Kao (2003)

Wang et al. (2013)

Zhao et al. (2009)

Chen et al. (2018)

Majerus et al. (2009)

Shi et al. (2015)

Kang et al. (2015b)

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macrocephala seedlings, production of MDA and H2O2 was induced by the application of 300 μmol L−1 of Pb (NO3)2 (Wang et al. 2013). Likewise, MDA production was induced in O. sativa under lead (Zhao et al. 2009) and Cd stress (Shen et al. 2017), applying Pb(NO3)2 at 0.25  μmol  L−1 and CdCl2×2.5H2O at 0, 10, 20, 50, 100 μmol L−1. Application of ABA at low concentrations (80% of JA responsive genes have a decline in expression (Xie et  al. 1998; Devoto et  al. 2005). In these mutants, this decline resulted in an increase in susceptibility to necrotrophic pathogens. Similarly, in the case of a jar 1-1mutant, the active enzyme involved in JA biosynthesis is mutated making the mutant plant vulnerable to Pythium irregulare (Staswick et al. 1998, 2002). The plants with constitutive expression of JA conferred resistance against fungal pathogens like Erysiphe cichoracearum (Ellis and Turner 2001). These studies explain the involvement of JAs in providing resistance to plants against plant pathogens. The importance of JA in the regulation of plant response during wounding and insect attack is also reported in tomato. Various studies have revealed that the expression of genes important in wounding and expression of proteinase inhibitors is modulated by exogenous JA (Farmer et al. 1992). The def1 mutant of the tomato plant is found to be defective in the octadecanoid pathway-mediated biosynthesis of wound-induced JA and hence has a lower accumulation of JA (Howe et al. 1996). This mutant also showed reduced resistance to tobacco hornworm, Manduca sexta, which correlates with the decrease in JA accumulation and reduction in proteinase inhibitor gene expression. This demonstrates that the octadecanoid signaling pathway is important for the protection of plants from different types of harmful organisms like chewing insects and harmful fungi. An exogenous application of JA to potato plants resulted in local and systemic defense in those plants against different pathogen attacks (Cohen et al. 1993). JA is found to accumulate in potato infected with Pseudomonas syringae pv. Maculicola, (Landgraf et  al. 2002; Halim et  al. 2004). However, JA accumulation against P. syringae is not observed in susceptible plants (Weber et al. 1999; Gobel et al. 2002) revealing that the cumulation of JA takes place in response to PAMP recognition and nonhost pathogen interaction. Another gene JAV1, JA-associated VQ motif gene 1, negatively regulates the JA-mediated defense against insect and pathogen attack (Hu et al. 2013). JA-COI 1 signaling complex is a part of the degradation system responsible for the

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degradation of this negative regulator, JAV1, through 26S proteasome, thereby contributing to the activation of defense-related genes and protection against pathogens. When there is no such attack by pathogens, active JAV1 is not degraded and interacts with the WRKY transcription factor leading to inactivation of its active functions. Once there is a pathogen attack, JAV1 gets degraded resulting in the activation of a downstream signaling pathway that results in the development of plant defense against these pathogens. This negative regulation by JAV1 helps a damaged plant to mediate their JA-mediated defense response to establish a harmony between growth and defense during stress. Genetically engineered rice plants with AOS2 expression, allene oxide synthase (plays role in JA synthesis), have induced expression of antipathogenic proteins (like PR3, PR5, etc.) and enhanced resistance against pathogenic fungi (Mei et al. 2006). The two rice osjar1 mutants having lower JA Ile (product of JAR 1) production are susceptible to blast fungi in contrast to the nonmutants (Shimizu et  al. 2013), revealing the function of JA Ile in mediating defense mechanisms in rice against blast fungus. Also, the complete silencing of OsCOI 1 enhanced the susceptibility of rice plants against chewing insects that correlated with the downregulation of various genes encoding trypsin protease inhibitor, polyphenol oxidase (converts phenols to toxic quinones), and peroxidase. The exogenous treatment of MeJA to Arachis hypogea has shown to increase the level of antioxidant enzymes, thereby reducing growth and development of Helicoverpa armigera (War et al. 2015), whereas in Vigna mungo, methyl jasmonate (MeJA) is found to protect the plant from Mungbean yellow mosaic India virus through the restoration of membrane stability and maintenance of reactive oxygen species homeostasis (Chakraborty and Basak 2019). In Solanum lycopersicum, external treatment with methyl jasmonate provides tolerance against Helicoverpa zea by inducing defense gene expression (Tian et al. 2014). The external treatment of MeJA to Phaseolus vulgaris and Panax notoginseng provided resistance against Sclerotinia sclerotiorum and Fusarium solani, respectively (Oliveira et al. 2015; Liu et al. 2019b), as shown in Table 1.

3.2  Abiotic Stress JA is a crucial plant-hormone that protects against different stresses like cold stress, heat stress, etc. and its role against various abiotic stresses has been studied already in various crops (Acharya and Assmann 2009; Karpets et  al. 2014; Wasternack 2014; Siddiqi and Husen 2019). The use of exogenous JA can protect the plants from various abiotic stresses.

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Table 1  Review of literature highlighting the role of exogenous JA in both biological and nonbiological stresses S. Stress no type Plant species Abiotic stresses 1 Heat Vitis vinifera L. stress Arabidopsis thaliana (L.) Heynh. 2 Cold Prunus persica stress (L.) Batsch

Exogenous JA concentration 50 μM JA 5 μM MeJA

Plant response

References

Increased activities of antioxidant enzymes Stabilized membrane, induced JA pathway

Chen et al. (2006) Clarke et al. (2009)

1 μM L−1 MeJA Increased activities of phenylalanine ammonia lyase, superoxide dismutase, Polygalacturonase decreased activities of polyphenol oxidase, peroxidase, alleviated chilling injury Punica 0.01 and Increased total phenolics and granatum L. 0.1 mM MeJA anthocyanins, enhanced antioxidant activity, alleviated chilling injury 0.05 mM MeJA Modified arginine catabolism, Solanum improved post-harvest chilling lycopersicum tolerance L. 16 μmol L−1 Eriobotrya Increased antioxidant enzyme japonica MeJA activity, decreased lignin (Thunb.) Lindl. content, mitigated harmful effects of freezing injury Vigna sinensis 0.5, 1, 2, 4, and 1 μM MeJA reduced chilling (L.) Walp. 8 μM MeJA injury, increased malondialdehyde content, chlorophyll, and ascorbic acid, induced antioxidant activity

Jin et al. (2009)

Sayyari et al. (2011)

Zhang et al. (2012) Jin et al. (2014)

Fan et al. (2016)

(continued)

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Table 1 (continued) S. Stress no type 3 Heavy metal stress

4

Salt stress

Plant species Cajanus cajan (L.) Millsp.

Exogenous JA concentration 1 μM, 1 nM, and 1 pM MeJA

Plant response Increased chlorophyll and carotenoids, enhanced antioxidant enzyme activity, mitigates copper (Cu) toxicity Capsicum 0.1–1 mM Increased antioxidant enzyme frutescens L. MeJA activity and enhanced chlorophyll levels 0.01 mM MeJA Reduced Cd content, Kandelia increased ascorbic acid obovata Sheue, content, mitigation of Liu and Yong oxidative damage by increased concentration of antioxidant enzymes 0.01 μM MeJA Reduced Cd toxicity, Solanum nigrum L. decreased malondialdehyde, improved activities of antioxidant enzymes Brassica napus 0.1–1 mM Reduced arsenic stress, L. MeJA increased antioxidants, and secondary metabolites Brassica 10 μM MeJA Increased chlorophyll, relative oleracea L. water content, net photosynthesis rate, and abscisic acid level, induced antioxidant system Matricaria 75 μM MeJA Increased proline content, chamomilla L. enhanced photosynthetic rate, increased K+ concentration and decreased Na+ concentration, induced antioxidant system 100 μM MeJA Increased antioxidant enzyme Robinia activity and decreased levels pseudoacacia of hydrogen peroxide and L. superoxide radicals 50 μM MeJA Enhanced net photosynthetic Vigna rate, increased total soluble unguiculata proteins, sugars, and phenolics (L.) Walp. Brassica napus 100 μM MeJA Increased photosynthetic rate, L. relative water content, and soluble sugar content

References Poonam et al. (2013)

Yan et al. (2013) Chen et al. (2014)

Yan et al. (2015)

Farooq et al. (2016) Wu et al. (2012)

Salimi et al. (2016)

Jiang et al. (2016)

Sadeghipour (2017) Ahmadi et al. (2018) (continued)

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Table 1 (continued) S. Stress no type Plant species 5 Drought Triticum stress aestivum L.

Solanum nigrum L. Triticum aestivum L. Glycine max (L.) Merr.

Satureja hortensis L.

Biotic stresses 6 Insect Arachis feeding hypogaea L.

Solanum lycopersicum L.

7

Viral disease

Vigna mungo L.

Exogenous JA concentration 250 mM MeJA

Plant response Reduced malonaldehyde content, decreased oxidative damage because of enhance antioxidant enzymes, increase of compensation irradiance 0.01 mM MeJA Increased antioxidant enzyme activity, decreased malondialdehyde content 500 mM MeJA Increased grain yield and productivity 200 μM MeJA Increased growth, and photosynthetic pigments, induced antioxidant enzymes, enhanced unsaturated fatty acids, and flavonoids 75 mM MeJA Increased growth parameters, and proline content, enhanced antioxidant activity, and oil content

References Ma et al. (2014)

1 mM JA

War et al. (2015)

Induces the activity of antioxidative enzyme, therefore, reducing growth and development of Helicoverpa armigera 2.5 mM MeJA Exogenous MeJA application found to be effective against Helicoverpa zea through inducing defense gene expression, and increased density of glandular trichome Methyl jasmonate (MeJA) 0.01 mM, 0.1 mM, 1 mM found to be effective for Mungbean yellow mosaic and 10 mM India virus tolerance in Vigna MeJA mungo (L.) through restoration of membrane stability, maintenance of reactive oxygen species homeostasis and by reducing the expression of virus coat-protein encoding genes. 0.1 mM has been found to be most effective dose

Yan et al. (2015) Anjum et al. (2016) Mohamed and Latif (2017)

Miranshahi and Sayyari (2018)

Tian et al. (2014)

Chakraborty and Basak (2019)

(continued)

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Table 1 (continued) S. Stress no type 8 Fungal disease

Plant species Phaseolus vulgaris L.

Panax notoginseng (Burkill) F.H. Chen

Exogenous JA concentration 10 μM MeJA

100 μM MeJA

Plant response Foliar application of MeJA induces systemic defense against Sclerotinia sclerotiorum in dry bean plants by increasing the transcripts level that encode pathogenicity related proteins Resistance of Panax notoginseng found to be triggered by methyl jasmonate (MeJA) against Fusarium solani ultimately helping in disease resistance

References Oliveira et al. (2015)

Liu et al. (2019b)

3.2.1  Salinity Stress Salinity stress contributes to huge crop losses every year (Munns and Tester 2008). Na+ and Cl− are the primary salts contributing to salt stress. The prime sources of accumulation of salts in agricultural lands are irrigation water having relatively high salt contents and chemical pesticides/insecticides used for crop protection (Munns and Tester 2008). Salinity hinders various processes such as uptake of nutrients, chlorophyll degradation, etc., and the evolution of ROS is observed under severe salinity conditions. This in turn leads to oxidative damage to various proteins and DNA as well (Farhangi-Abriz and Torabian 2017). Salt treatment to different plants such as Lycopersicon esculentum, Solanum tuberosum, and Arabidopsis thaliana resulted in enhanced endogenous JA in these plants (Pedranzani et al. 2013; Ellouzi et al. 2013; De Domenico et al. 2019). Sweet potato under salt stress is found to have increased levels of JA as per the transcript profile (Zhang et al. 2017). The immediate increase in JA content is observed in salt-sensitive plants under salt stress whereas this increase is minimal in salt-­tolerant plants (De Domenico et al. 2019). In rice, the accumulation of JA resulted in reducing the negative effects of salt stress on biomass production (Kang et al. 2005). The application of JA to safflower leaves growing under salt stress resulted in enhanced yield, and physiological performance (Ghassemi-Golezani and Hosseinzadeh-­ Mahootchi 2015). The external treatment of JA to salt stress exposed plants has shown better potassium content, lower lipid peroxidation, and higher antioxidant activity (Farhangi-Abriz and Ghassemi-Golezani 2018). The external treatment of JA to different plants like Brassica oleracea, Matricaria chamomilla, Robinia pseudoacacia, Vigna unguiculate, and Brassica napus have shown to increase antioxidant enzyme activity and net photosynthetic rate, thereby alleviating negative effects of salt stress (Wu et  al. 2012; Salimi et  al. 2016; Jiang et  al. 2016; Sadeghipour 2017; Ahmadi et al. 2018).

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3.2.2  Drought Stress Drought stress is responsible for extensive crop losses every year. Various changes in plants are observed during drought, which has serious repercussions on their growth and yield (Pandey et al. 2017). There are various negative impacts of drought stress on different physiological processes of plants including the decrease in turgor pressure, reduction in photosynthetic rates, increase in leaf senescence, and ion toxicity. As compared to the different stresses, there is little information related to the functions of JA in drought stress. Jasmonic acid can regulate the opening and closing of stomata, thereby reducing the rate of water loss during water-deficient conditions (Savchenko et  al. 2014). The endogenous JA levels were increased when different plants such as A. thaliana (Balbi and Devoto 2008) and Citrus spp. (De Ollas et al. 2013) were subjected to water-deficient conditions, but JA concentration was declined to basal level upon prolonged exposure. The different components of JA signaling pathways are involved in making plants tolerant to the shortage of water. The negative regulator or a repressor of the JA signaling pathway termed jasmonate ZIM-domain proteins (JAZ) are found to negatively regulate the rice tolerance to water-deficient conditions (Fu et al. 2017). The external employment of various plant hormones to plants growing under particular stress has proved to be an effective method to reduce harmful outcomes of the stress on plants, the same is with JA and drought stress. This strategy has been found to increase crop production under drought stress by increasing antioxidant enzyme activities. The exogenous application of JA to maize plants growing under drought stress resulted in an escalated amount of antioxidant enzymes that lower the damage done by the increased ROS (Abdelgawad et al. 2014). Also, the lipid peroxidation decreased in peanut grown under water-deficient conditions by the exogenous supply of JA that resulted in decreased oxidative stress because of the increased antioxidant enzyme production (Kumari et al. 2006). It is found that the synthesis of antioxidant enzymes like glutathione peroxidase, catalase, etc. is enhanced upon foliar application of JA in Brassica that in turn leads to an alleviation of damage caused by increased ROS (Alam et al. 2014). The exact mechanism of induction of these antioxidant enzymes by the JA application is still not known very well. Additionally, the external application of MeJA to different plants like Solanum nigrum, Triticum aestivum, Glycine max, and summer savory has shown to increase growth and decrease oxidative stress when subjected to stress conditions (Yan et  al. 2015; Anjum et  al. 2016; Mohamed and Latif 2017; Ma et  al. 2014; Miranshahi and Sayyari 2018). 3.2.3  Heat Stress The changes in temperature above and below the limits of ambient temperature decrease crop productivity drastically (Zandalinas et al. 2018). The overall rise in temperature because of the greenhouse effect is termed as heat stress. This type of

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stress has various adverse effects on plants including the protein denaturation, lowering of enzymatic activity, etc. When exposed to heat stress, plants regulate gene expression, thereby producing essential proteins or controlling signaling pathways. One of the important proteins with excessive production during heat stress is heat-­ shock protein (HSP). HSPs protect different proteins from heat stress along with some major roles in many other processes. Jasmonic acid has many protective functions against stress and can also produce different secondary metabolites as well as heat-shock proteins (Creelman and Mullet 1995; Balfagón et al. 2019). JA signaling functions in providing tolerance to Arabidopsis against heat stress (Clarke et al. 2009). The increased concentration of JA in plants growing under heat stress contributes to plant defense against stressful conditions (Hasanuzzaman et al. 2013). The foliar treatment of JA to barley enhances the production of heat-shock proteins by changes in gene expression (Mueller-Uri et al. 1988; Aghdam et al. 2013). A counterview has been proposed by many other scientists stating that the modification in plant phenolic components was responsible for increased production of HSPs, thereby protecting plants from heat stress (Saltveit 2000). The application of JA results in an increase in abscisic acid which led to the induction of stomatal closure and reduced transpiration for maintaining plant temperature (Lehmann et al. 1995; Creelman and Mullet 1997; Acharya and Assmann 2009). JA also regulates water potential in a plant cell resulting in the preservation of water. 3.2.4  Cold Stress Since a long time, cold stress is considered as harmful for the overall growth of the plant that can be further categorized into freezing stress and chilling stress based on temperature either below 0  °C or above 0  °C, respectively (Huang et  al. 2014; Trischuk et al. 2014; Sharma et al. 2020). The major effects of cold stress in plants include ice crystal formation inside the cells and cellular dehydration. Various other changes like the molecular and the biochemical changes along with physiological changes are observed in plants during cold stress that results in the synthesis of cold stress-induced proteins, essential amino acids, and soluble proteins (Hincha and Zuther 2014; Ritonga and Chen 2020). Different plant hormones are demonstrated to be involved in plant protection against cold stress (Kosova et al. 2012; Wasternack 2014). In plants, during low-­ temperature stress, an increase in the concentration of JA is observed (Kosova et al. 2012). Also, when the Pinus pinaster plants suffered two different stresses, water stress and cold stress, a rise in JA content of leaves is observed (Pedranzani et al. 2007). The transcription of different genes like allene oxide cyclase (AOC), lipoxygenase 2, and allene oxide synthase 1 (AOS) increased as a result of cold stress and all these genes are found to contribute to JA biosynthesis. Jasmonates can alleviate chilling stress by inducing the production of proteinase inhibitors, antioxidants, abscisic acid, cryoprotectants, and polyamines (Cao et al. 2009; Zhao et al. 2013). The JA application to chilled rice in a low dosage enhances their survival ratio (Lee

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et al. 1997). Methyl jasmonate has been used on plants like Prunus persica, Punica granatum Solanum lycopersicum, Eriobotrya japonica, and Vigna sinensis, resulting in enhanced antioxidant enzyme activity, decreased oxidative damage, and mitigation of cold stress (Jin et al. 2009; Sayyari et al. 2011; Zhang et al. 2012; Fan et al. 2016). 3.2.5  Heavy Metal Stress This type of abiotic stress is highly prevalent in agricultural lands because of the usage of chemical fertilizers and pesticides, weathering of rocks, etc. Heavy metal stress has various ill effects on plant growth, which could lead to increased leaf senescence and decreased photosynthetic rates (Maksymiec 2007; Berni et al. 2019). Heavy metal toxicity like cadmium and copper toxicity can increase the concentration of endogenous JA in Arabidopsis thaliana plants (Xiang and Oliver 1998). The exogenous application of JA to Glycine max seedlings before NiCl2 stress increased plant survival in Ni2+ stress (Sirhindi et  al. 2015). Heijari et  al. (2008) determined that the external use of methyl jasmonate in lower doses alleviates the adverse effects of aluminum toxicity by elevating the enzymatic and nonenzymatic antioxidants. JA also reduced lipid peroxidation by enhancing the production of glutathione or ascorbate antioxidants (Noriega et al. 2012). The application of jasmonates to soybean leaves growing under cadmium stress alleviated cadmium stress by lowering lipid peroxidation, ROS, and enhancing antioxidant activity (Keramat et al. 2009). The external employment of jasmonates in low dosage to plants under copper toxicity protected plants by modifying photosynthetic pigments (Poonam et al. 2013). The use of MeJA externally can prevent oxidative damage and mitigate heavy metal stress in various plants including Cajanus cajan, Capsicum frutescens, Kandelia obovate, Solanum nigrum, and Brassica napus (Poonam et al. 2013; Yan et al. 2013, 2015; Chen et al. 2014; Farooq et al. 2016). Hence, it can be known from different observations that jasmonates are involved in the reduction of harmful impacts of heavy metal stress.

4  JA Signaling 4.1  In the Absence of JA The synthesis of JA involves three compartments, chloroplast, peroxisome, and cytosol. JA is then transferred to the cytoplasm/cytosol (Wasternack and Hause 2002; Ruan et al. 2019). In the cytoplasm, JA-Ile was found to be the most bioactive form. In response to different stresses, JA moved to the nucleus and apoplast through a transporter protein known as jasmonic acid transfer protein 1 (JAT1).

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Fig. 3  JA signaling pathway in the absence of JA

Under normal conditions, various transcription factors are unable to activate promoters of jasmonate-responsive genes because of very little concentration of JA-lle. The coronatine insensitive 1 (COI1) and JAZ co-receptors together are a part of the jasmonate receptor. It was reported that the COI1-JAZ co-receptor has >100-fold greater affinity for the ligand than either COI1 or JAZ alone (Sheard et al. 2010). The F-box protein, COI1, associates with Skp/cullin to establish an E3 ubiquitin ligase complex, i.e., SCFCOI1. JAZ proteins are the repressors of jasmonate signaling. JAZ proteins have conserved Jas and ZIM/TIFY domains. Both these domains have different functions like Jas domain interacts with COI1 and MYC2 proteins whereas the ZIM domains cause dimerization and association with JAZ proteins and NINJA (Chung and Howe 2009). The NINJA [having an EAR motif] communicates with TOPLESS (TPL). NINJA, TOPLESS along with JAZ proteins form a complex having a role in the repression of transcription (Fig. 3). Through the participation of histone deacetylase 6 (HDA6) and HDA19, this complex aims at inhibiting the jasmonate-responsive genes expression by the formation of a closed complex from an open one (Pauwels et al. 2010; Causier et al. 2012; Acosta et al. 2013; Chini et al. 2016; Wasternack and Song 2017).

4.2  In the Presence of JA After the plant perceives any kind of abiotic stress, it starts elevating the production of JA-lle and it is recognized by COI1. In the nucleus, JA-lle promotes interaction between JAZ and COI1 (Xie et al. 1998; Zhai et al. 2015; Ali and Baek 2020). This JA-lle, COI1, and JAZ interaction facilitate the ubiquitin-dependent degradation of JAZ proteins by 26S proteasome which serves as a repressor of jasmonate signaling.

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Fig. 4  JA signaling pathway in the presence of JA

Degradation of repressor permits transcriptional activation of different jasmonate-­ responsive genes by the activity of various transcription factors (Fig.  4). In Arabidopsis, Mediator 25 (MED25) (Bäckström et al. 2007) serves as a communicator between the general transcription factors (GTFs), RNA polymerase II, and the gene-specific TFs (Chen et al. 2012).

5  I nteraction of JA with Other Phytohormone Signaling Pathways Under Stress Conditions 5.1  Interaction of JA with Auxins for Root Development Cross talk can be visualized as two distinct pathways not independent of each other which can be negative or positive and can alter synthesis, transport, or signaling pathway of another hormone (Jang et al. 2020). For example, the growth of plant roots is being regulated by different hormonal pathways. Auxin plays a crucial role among them. It has been already reported that PLT genes that encode AP2 (APETALA2) class of TFs plays a crucial part in the patterning of SCN (Galinha et  al. 2007). Auxin signaling pathway was reported by Dharmasiri et  al. (2005), Kepinski and Leyser (2005), and Mockaitis and Estelle (2008), where it was demonstrated that TRANSPORT INHIBITOR RESPONSE1 (TIR1) which is an F-box

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protein serves as auxin receptor. After attachment of auxin with TIR1, it facilitates the association of TIR1 with Aux/IAA substrates which serve as an inhibitor of auxin signaling. TIR1 is a component of SCF ubiquitin ligase complex SCFTIR1 leading to the ubiquitin-dependent proteolysis of Aux/IAA by 26S proteasome (Fig. 5). Degradation of repressor permits transcriptional activation by ARFs that promote the expression of different auxin-responsive genes including PLT1and PLT2. Chen et  al. (2011) observed that the expression levels of PLT1 and PLT2 are downregulated by JA, which is reliant on the MYC2 transcription factor. Dombrecht et al. (2007) have reported that the preferable site of MYC2 binding is 5′-CACATG-3′ motif in the target genes. Chen et al. (2011) also reported the existence of this single motif in P1 region (−1609 to −1614 bp) whereas two motifs in P2 region (−940 to −945 and −1098 to −1103 bp) of PLT 1 promoter and also one same motif in P3 region (+288 to +293) of PLT2 promoter. Their study also revealed MYC2 TFs act upstream of PLT1 and PLT2 TFs in regulating SCN maintenance and root meristem activity. It has already been reported that transcription of PLT1 and PLT2 are being upregulated by auxin. SCN maintenance and meristem activity are also being positively regulated by auxin (Aida et al. 2004). As compared to this, the study of Chen

Fig. 5  Hormonal pathways showing an interplay between JA and auxin resulting in regulation of root meristem activity and root stem cell niche (SCN) maintenance

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et  al. (2011) focused on lowered PLT1 and PLT2 expression by JA and negative regulation of SCN maintenance and meristem activity, therefore, hints at the convergence of different JA and auxin signaling pathways in the modulation of maintenance of root SCN.

5.2  I nteraction of JA with Ethylene in the Regulation of Apical Hook Formation Various epigeal plants have developed an organ known as an apical hook during evolution to protect apical meristem and cotyledons from any sort of damage. It is already reported that formation of ethylene (ET) and gibberellins (GAs) contributes to apical hook formation whereas jasmonate (JA) and brassinosteroids discourage the apical hook formation (Vriezen et  al. 2004; Li et  al. 2004; De Grauwe et  al. 2005). Lehman et al. (1996) reported that HOOKLESS1 (HLS1) is a key regulator of auxin distribution and responses at the time of apical hook formation of Arabidopsis seedlings. HLS1 transcript accumulation is promoted by ET through ETHYLENE INSENSITIVE3 (EIN3) which binds directly to the promoter of HLS1. Several ET receptors like ERS1, ERS2, ETHYLENE TRIPLE RESPONSE (ETR1), ETR2, and ETHYLENE INSENSITIVE4 (EIN4) have already been identified. In the absence of ET, the ET responses are negatively regulated by its receptors. CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) is present downstream of the ET receptors and negatively regulates the ethylene response in the absence of ethylene. The binding of ethylene to its receptors promotes the deactivation of its receptors. EIN2 works downstream of CTR1 which gets inactive in the absence of ET because of ETP1 and ETP2 that are components of the ubiquitin ligase complex that targets EIN2 for proteolysis. In the presence of ethylene, ETP1 and ETP2 get degraded whereas the degradation of EIN2 gets halted leading to the activation of downstream signaling. EIN2 promotes the stabilization of EIN3 and EIL1 that are TFs binding at a particular site on the promoter of ERF1 termed as ethylene binding site (EBS). Another TF is encoded by ERF1 that modulates the transcription of ethylene-responsive genes including HLS1. During the unavailability of ET, EIN3 and EIL1 are degraded via ubiquitin-mediated proteolysis by F-box proteins, EBF1, and EBF2 (Fig. 6). The activity of EIN3/EIL1 is repressed by the JA-activated transcription factor (MYC2) in the modulation of HLS1 expression and hook development (Zhang et al. 2014). There are several pieces of evidence available that support the statement that EIN3/EIL1 degradation is being promoted by JA in a SCFEBF1-dependent manner. It can also be concluded that apical hook development is being governed by the antagonistic action of the JA-ET signaling pathway where these two hormones have opposite effects on the stability of EIN3/EIL1 protein. ET stabilizes the cumulation of EIN3/EIL1 whereas JA is responsible to foster their degradation.

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Fig. 6  Cross talk between ethylene and JA signaling pathway in the formation of the apical hook

5.3  JA and GA Cross talk for Stamen Development Stamen is a male reproductive organ that produces pollen, crucial for the fertility of a plant. Different development stages of stamen development are governed by various environmental factors and hormonal signaling. JA and GA are the master regulators of stamen development. GIBBELELLINE INSENSITIVE DWARF1 (GID1) serves as a receptor in the GA signaling pathway. After binding of bioactive GA to GID1, a conformational switch in the GID1 ensures DELLA binding. This interaction in turn promotes transition in the GRAS domain of the DELLA protein for recognition of SKP, Cullin, and F-box proteins, SCFSLY1/GID2 that results in ubiquitin-mediated proteolysis of DELLA protein. Degradation of DELLA promotes the transcription of different GA responsive genes. GA responses begin and SPINDLY (SPY) encodes an N-acetylglucosamine transferase that adds N-acetylglucosamine to DELLA for its activation and therefore serves as GA signaling repressor. EARLY FLOWERING 1 (EL1), a casein kinase in rice, may also phosphorylate and activate DELLA (Sun 2010; Qin et al. 2011).

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Various studies revealed that JA promotes the transcription of R2R3 MYB TFs MYB21, MYB24, etc. crucial for stamen development (Cheng et  al. 2009; Mandaokar and Browse 2009; Song et al. 2011). JAZ proteins act as a repressor of JA signaling where it inhibits the activity of MYB TFs MYB21, MYB24, etc. (Song et al. 2011). The bHLH-MYB complex formed as a result of an association between lle bHLH and MYB21, MYB24 regulates the stamen development (Qi et al. 2015). At the time plant perceives environmental cues it starts synthesizing JA. Interaction of JA to its co-receptor COI1 and JAZ facilitates JAZ to degrade through 26S proteasome, thereby releasing the bHLH-MYB complex that also modulates the downstream gene expression in mediating stamen development (Fig. 7). It was already reported that DELLA is involved in inhibition of JA biosynthesis gene expression in flowers that lead to altering the process of stamen development. Hong et al. (2012) demonstrated direct interaction of DELLA with MYC2 to repress its activity. Further, it remains an area of investigation to find out whether all the bHLH members (MYC2, MYC3, etc.) and MYB21 and MYB24 are targets of DELLA in inhibiting the transcription function of the bHLH-MYB complex for regulating stamen development.

Fig. 7  Cross talk between JA and GA in the regulation of stamen development

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6  Concluding remarks While growing in nature, the green plants are often subjected to multiple abiotic and biotic stresses either in single or in combination. To tackle challenging conditions and support their growth, plants initiate a fine-tuning in their signaling networks as well as bring changes in the concentration of endogenous plant hormones. This makes it necessary to further investigate the cross talk of natural plant hormones in the balance warfare of growth and defense. One of such important phytohormone is jasmonic acid (JA). Due to the continuous research and parallel advancements in omics in recent years, the crucial roles of JA and its derivatives have been investigated from seed germination to plant’s defense as well as tolerance. During the challenging various stresses, JAs induce antioxidative enzymes and other defensive compounds as well as modulate the nutrition uptake for combating the stresses. At present, it has been deduced that the action mechanism of the core JA signaling pathway varies under every stress due to the diversity of both positive and negative interactions with numerous genes, regulatory TFs, small RNAs, hormones, elicitor, and treatments. However, so far, the data still fail to throw light on the highly complex molecular mechanism of JA signaling with changeable networks of other plant hormones in combinatorial stresses at a time. Furthermore, the identified components of hormone signaling are still very low as compared with the unidentified components. Moreover, there are very high chances of the variability in the data recorded in labs from those that actually occur in the farmer fields. Additionally, there is still no single report available in the literature that embarks the complete temporal analysis of plant hormone signaling networks starting from the seedling stage to senescence. So overall, we have to keep in mind that the current knowledge is limited as compared with a big list of related questions. As a result, in the future, systematic omics research on the interaction of JA signaling with each and every interacting factor will be done for broad application prospect, i.e., super tolerance in plants that do not compromise yield. In the future, the exact molecular mechanisms of both vascular and airborne transmission of the JA signal will also be elucidated. The light will be also given on how various environmental signals initiate the synthesis of JA.

References Abdelgawad ZA, Khalafaallah AA, Abdallah MM (2014) Impact of methyl jasmonate on antioxidant activity and some biochemical aspects of maize plant grown under water stress condition. Agric Sci 5:1077–1088 Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462 Acosta IF, Gasperini D, Chételat A, Stolz S, Santuari L, Farmer EE (2013) Role of NINJA in root jasmonate signaling. Proc Natl Acad Sci 110:15473–15478 Aghdam MS, Sevillano L, Flores FB, Bodbodak S (2013) Heat shock proteins as biochemical markers for postharvest chilling stress in fruits and vegetables. Sci Hortic 160:54–64

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Ahmadi FI, Karimi K, Struik PC (2018) Effect of exogenous application of methyl jasmonate on physiological and biochemical characteristics of Brassica napus L. cv. Talaye under salinity stress. S Afr J Bot 115:5–11 Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120 Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2014) Exogenous jasmonic acid modulates the physiology, antioxidant defense and glyoxalase systems in imparting drought stress tolerance in different Brassica species. Plant Biotechnol Rep 8:279–293 Ali M, Baek KH (2020) Jasmonic acid signaling pathway in response to abiotic stresses in plants. Int J Mol Sci 21:621 Anamika, Mehta S, Singh B, Patra A, Islam MA (2019) Databases: a weapon from the arsenal of bioinformatics for plant abiotic stress research. In: Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 135–169 Anjum SA, Tanveer M, Hussain S, Tung SA, Samad RA, Wang L, Khan I, ur Rehman N, Shah AN, Shahzad B (2016) Exogenously applied methyl jasmonate improves the drought tolerance in wheat imposed at early and late developmental stages. Acta Physiol Plant 38:25 Ashraf M, Akram NA, Arteca RN, Foolad MR (2010) The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Crit Rev Plant Sci 29:162–190 Bäckström S, Elfving N, Nilsson R, Wingsle G, Björklund S (2007) Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol Cell 26:717–729 Balbi V, Devoto A (2008) Jasmonate signalling network in Arabidopsis thaliana. Crucial regulatory nodes and new physiological scenarios. New Phytol 177:301–318 Balfagón D, Sengupta S, Gómez-Cadenas A, Fritschi FB, Azad RK, Mittler R, Zandalinas SI (2019) Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiol 181:1668–1682 Berni R, Luyckx M, Xu X, Legay S, Sergeant K, Hausman JF, Lutts S, Cai G, Guerriero G (2019) Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism. Environ Exp Bot 161:98–106 Bharti J, Sahil, Mehta S, Ahmad S, Singh B, Padhy AK, Srivastava N, Pandey V (2021) Mitogen-­ Activated Protein Kinase, Plants, and Heat Stress. In Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp. 323–354 Cao S, Zheng Y, Wang K, Jin P, Rui H (2009) Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chem 115:1458–1463 Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438 Chakraborty N, Basak J (2019) Exogenous application of methyl jasmonate induces defense response and develops tolerance against mungbean yellow mosaic India virus in Vigna mungo. Funct Plant Biol 46:69–81 Chen PQ, Yu SL, Zhan YN, Kang XL (2006) Effects of jasmonate acid on thermotolerance of grape seedlings. Journal of Shihezi University (Natural Science). J Shihezi Univ (Nat Sci) 24:87–91 Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Li X (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352 Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, Li C (2012) The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24:2898–2916 Chen J, Yan Z, Li X (2014) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf 104:349–356 Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5:e1000440

92

Sahil et al.

Chini A, Gimenez-Ibanez S, Goossens A, Solano R (2016) Redundancy and specificity in jasmonate signalling. Curr Opin Plant Biol 33:147–156 Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145 Clarke SM, Cristescu SM, Miersch O, Harren FJ, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187 Cohen Y, Gisi U, Niderman T (1993) Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic-methylester. Phytopathology 83:1054–1062 Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci 92:4114–4119 Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Biol 48:355–381 Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp Bot 115:49–57 De Domenico S, Taurino M, Gallo A, Poltronieri P, Pastor V, Flors V, Santino A (2019) Oxylipin dynamics in Medicago truncatula in response to salt and wounding stresses. Physiol Plant 165:198–208 De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D (2005) Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol 46:827–836 De Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306 Devoto A, Ellis C, Magusin A, Chang HS, Chilcott C, Zhu T (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497–513 Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445 Dilawari R, Kaur N, Priyadarshi N, Kumar B, Abdelmotelb KF, Lal SK, Singh B, Tripathi A, Aggarwal SK, Jat BS, Mehta S (2021) Genome Editing: A Tool from the Vault of Science for Engineering Climate-Resilient Cereals. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 45–72 Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245 Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13:1025–1033 Ellouzi H, Ben Hamed K, Cela J, Müller M, Abdelly C, Munné-bosch S (2013) Increased sensitivity to salt stress in tocopherol-deficient Arabidopsis mutants growing in a hydroponic system. Plant Signal Behav 8:1–13 Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Fan L, Wang Q, Lv J, Gao L, Zuo J, Shi J (2016) Amelioration of postharvest chilling injury in cowpea (Vigna sinensis) by methyl jasmonate (MeJA) treatments. Sci Hortic 203:95–101 Farhangi-Abriz S, Ghassemi-Golezani K (2018) How can salicylic acid and jasmonic acid mitigate salt toxicity in soybean plants? Ecotoxicol Environ Saf 147:1010–1016 Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicol Environ Saf 137:64–70

Jasmonic Acid for Sustainable Plant Growth and Production Under Adverse…

93

Farmer EE, Johnson RR, Ryan CA (1992) Regulation of proteinase inhibitor gene expression by methyl jasmonate and jasmonic acid. Plant Physiol 98:995–1002 Farooq MA, Gill RA, Islam F, Ali B, Liu H, Xu J (2016) Methyl jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L. Front Plant Sci 7:468–483 Fu J, Wu H, Ma SQ, Xiang DH, Liu RY, Xiong LZ (2017) OsJAZ1 attenuates drought resistance by regulating JA and ABA signaling in Rice. Front Plant Sci 8:1–13 Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202 Ghassemi-Golezani K, Hosseinzadeh-Mahootchi A (2015) Improving physiological performance of safflower under salt stress by application of salicylic acid and jasmonic acid. Walia J 31:104–109 Gobel C, Feussner I, Hamberg M, Rosahl S (2002) Oxylipin profiling in pathogen-infected potato leaves. Biochim Biophys Acta 1584:55–64 Halim VA, Hunger A, Macioszek V, Landgraf P, Nürnberger T, Scheel D, Rosahl S (2004) The oligopeptide elicitor Pep-13 induces salicylic acid-dependent and -independent defense reactions in potato. Physiol Mol Plant Pathol 64:311–318 Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684 Heijari J, Nerg AM, Kainulainen P, Vuorinen M, Holopainen JK (2008) Long term effects of exogenous methyl jasmonate application on Scots pine (Pinus sylvestris) needle chemical defence and diprionid sawfly performance. Entomol Exp Appl 128:162–171 Hincha DK, Zuther E (2014) Introduction: plant cold acclimation and freezing tolerance. Methods Mol Biol 1166:1–6 Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648 Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067–2077 Hu P, Zhou W, Cheng Z, Fan M, Wang L, Xie D (2013) JAV1 controls jasmonate-regulated plant defense. Mol Cell 50:504–515 Huang BR, DaCosta M, Jiang YW (2014) Research advances in mechanisms of turfgrass tolerance to abiotic stresses: from physiology to molecular biology. Crit Rev Plant Sci 33:141–189 Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Isah T (2019) Stress and defense responses in plant secondary metabolites production. Biol Res 52:1–25 Jang G, Yoon Y, Choi YD (2020) Crosstalk with jasmonic acid integrates multiple responses in plant development. Int J Mol Sci 21:305

94

Sahil et al.

Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5:726–734 Jiang M, Xu F, Peng M, Huang F, Meng F (2016) Methyl jasmonate regulated diploid and tetraploid black locust tolerance to salt stress. Acta Physiol Plant 38:106 Jin P, Zheng Y, Tang S, Rui H, Wang CY (2009) A combination of hot air and methyl jasmonate vapor treatment alleviates chilling injury of peach fruit. Postharvest Biol Technol 52:24–29 Jin P, Duan Y, Wang L, Wang J, Zheng Y (2014) Reducing chilling injury of loquat fruit by combined treatment with hot air and methyl jasmonate. Food Bioprocess Technol 7:2259–2266 Kang DJ, Seo YJ, Lee JD, Ishii R, Kim KU, Shin DH, Lee IJ (2005) Jasmonic acid differentially affects growth, ion uptake and abscisic acid concentration in salt-tolerant and salt-sensitive rice cultivars. J Agron Crop Sci 191:273–282 Karpets YV, Kolupaev YE, Lugovaya AA, Oboznyi AI (2014) Effect of jasmonic acid on the pro-/ antioxidant system of wheat coleoptiles as related to hyperthermia tolerance. Russ J Plant Physiol 61:339–346 Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451 Keramat B, Kalantari KM, Arvin MJ (2009) Effects of methyl jasmonate in regulating cadmium induced oxidative stress in soybean plant (Glycine max L.). Afr J Microbiol Res 3:240–244 Kosova K, Prášil IT, Vítámvás P, Dobrev P, Motyka V, Floková K, Novák O, Turečková V, Rolčik J, Pešek B, Trávničková A (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576 Kumari GJ, Reddy AM, Naik ST, Kumar SG, Prasanthi J, Sriranganayakulu G, Reddy PC, Sudhakar C (2006) Jasmonic acid induced changes in protein pattern, antioxidative enzyme activities and peroxidase isozymes in peanut seedlings. Biol Plant 50:219–226 Lal SK, Kumar S, Sheri V, Mehta S, Varakumar P, Ram B, Borphukan B, James D, Fartyal D, Reddy MK (2018) Seed priming: an emerging technology to impart abiotic stress tolerance in crop plants. In: Advances in seed priming. Springer, Singapore, pp 41–50 Landgraf P, Feussner I, Hunger A, Scheel D, Rosahl S (2002) Systemic accumulation of 12-oxo-­ phytodienoic acid in SAR-induced potato plants. Eur J Plant Pathol 108:279–283 Lee TM, Lur HS, Chu C (1997) Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings: II. Modulation of free polyamine levels. Plant Sci 126:1–10 Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194 Lehmann J, Atzorn R, Brückner C, Reinbothe S, Leopold J, Wasternack C, Parthier B (1995) Accumulation of jasmonate, abscisic acid, specific transcripts and proteins in osmotically stressed barley leaf segments. Planta 197:156–162 Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193–204 Li J, Zhang K, Meng Y, Hu J, Ding M, Bian J, Yan M, Han J, Zhou M (2018) Jasmonic acid/ethylene signaling coordinates hydroxycinnamic acid amides biosynthesis through ORA59 transcription factor. Plant J 95:444–457 Liu K, Zou W, Gao X, Wang X, Yu Q, Ge L (2019a) Young seedlings adapt to stress by retaining starch and retarding growth through ABA-Dependent and-independent pathways in Arabidopsis. Biochem Biophys Res Commun 515:699–705 Liu D, Zhao Q, Cui X, Chen R, Li X, Qiu B, Ge F (2019b) A transcriptome analysis uncovers Panax notoginseng resistance to Fusarium solani induced by methyl jasmonate. Genes Genomics 41:1383–1396 Lymperopoulos P, Msanne J, Rabara R (2018) Phytochrome and phytohormones: working in tandem for plant growth and development. Front Plant Sci 9:1–14 Ma C, Wang ZQ, Zhang LT, Sun MM, Lin TB (2014) Photosynthetic responses of wheat (Triticum aestivum L.) to combined effects of drought and exogenous methyl jasmonate. Photosynthetica 52:377–385

Jasmonic Acid for Sustainable Plant Growth and Production Under Adverse…

95

Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29:177–187 Mandaokar A, Browse J (2009) MYB108 acts together with MYB24 to regulate jasmonate-­ mediated stamen maturation in Arabidopsis. Plant Physiol 149:851–862 Mehta S, James D, Reddy MK (2019a) Omics technologies for abiotic stress tolerance in plants: current status and prospects. In: Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 1–34 Mehta S, Singh B, Dhakate P, Rahman M, Islam MA (2019b) Rice, marker-assisted breeding, and disease resistance. In: Disease resistance in crop plants. Springer, Cham, pp 83–111 Mehta S, Lal SK, Sahu KP, Venkatapuram AK, Kumar M, Sheri V, Varakumar P, Vishwakarma C, Yadav R, Jameel MR, Ali M, Achary VMM, Reddy MK (2020) CRISPR/Cas9-Edited Rice: A New Frontier for Sustainable Agriculture. In: New Frontiers in Stress Management for Durable Agriculture. Springer, Singapore, pp 427–458 Mehta S, Singh B, Patra A, Tripathi A, Easwaran M, Choudhary JR, Choudhary M, Aggarwal SK (2020) Maize microbiome: current insights for the sustainable agriculture. In: Microbiomes and Plant Health. Academic Press, Massachusetts, pp 267–297 Mehta S, Chakraborty A, Roy A, Singh IK, Singh A (2021) Fight Hard or Die Trying: Current Status of Lipid Signaling during Plant–Pathogen Interaction. Plants 10:1098 Mehta S, Gogna M, Singh B, Patra A, Singh IK, Singh A (2021) Silicon: a plant nutritional “non-­ entity” for mitigating abiotic stresses. In: Plant stress biology. Springer, Singapore, pp 17–49 Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe Interact 19:1127–1137 Miranshahi B, Sayyari M (2018) Methyl jasmonate mitigates drought stress injuries and affects essential oil of Summer savory. J Agric Sci Technol 18:1635–1645 Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80 Mohamed HI, Latif HH (2017) Improvement of drought tolerance of soybean plants by using methyl jasmonate. Physiol Mol Biol Plants 23:545–556 Mueller-Uri F, Parthier B, Nover L (1988) Jasmonate-induced alteration of gene expression in barley leaf segments analyzed by in-vivo and in-vitro protein synthesis. Planta 176:241–247 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681 Noriega G, Cruz DS, Batlle A, Tomaro M, Balestrasse K (2012) Heme oxygenase is involved in the protection exerted by Jasmonic acid against Cadmium stress in Soybean roots. J Plant Growth Regul 31:79–89 Oliveira MB, Junior ML, Grossi-de-Sá MF, Petrofeza S (2015) Exogenous application of methyl jasmonate induces a defense response and resistance against Sclerotinia sclerotiorum in dry bean plants. J Plant Physiol 182:13–22 Pandey N, Iqbal Z, Pandey B, Sawant SV (2017) Phytohormones and drought stress: plant responses to transcriptional regulation. In: Mechanism of plant hormone signaling under stress. Wiley, New Jersey, pp 477–504 Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, García-Casado G (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791 Pedranzani H, Vigliocco A, Miersch O, Abdala G (2007) Cold and water stresses produce changes in endogenous jasmonates in two populations of Pinus pinaster Ait. Plant Growth Regul 52:111–116 Pedranzani H, Racagni G, Alemano S, Miersch O, Ramírez I, Peña-Cortés H, Taleisnik E, Machado-Domenech E, Abdala G (2013) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41:149–158 Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

96

Sahil et al.

Poonam S, Kaur H, Geetika S (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Millsp. seedlings under copper stress. Am J Plant Sci 4:817–823 Qi T, Huang H, Song S, Xie D (2015) Regulation of jasmonate-mediated stamen development and seed production by a bHLH-MYB complex in Arabidopsis. Plant Cell 27:1620–1633 Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LSP, Fujita Y, Yamaguchi-Shinozaki K (2011) SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol 157:1900–1913 Rahman M, Sultana S, Nath D, Kalita S, Chakravarty D, Mehta S, Wani SH, Islam MA (2019) Molecular breeding approaches for disease resistance in sugarcane. In: Disease Resistance in Crop Plants. Springer, Cham, pp 131–155 Rajput LS, Aggarwal SK, Mehta S, Kumar S, Nataraj V, Shivakumar M, Maheshwari HS, Yadav S, Goswami D (2021) Role of WRKY Transcription Factor Superfamily in Plant Disease Management. In: Plant Stress Biology. Springer, Singapore, pp 335–361 Ritonga FN, Chen S (2020) Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants 9:560 Rosahl S, Feussner I (2004) Oxylipins. In: Plant lipids: biology, utilisation and manipulation. Blackwell, Oxford, pp 329–454 Ruan JJ, Zhou YX, Zhou ML, Yan J, Khurshid M, Weng WF, Cheng JP, Zhang K (2019) Jasmonic acid signaling pathway in plants. Int J Mol Sci 20:2479 Sadeghipour O (2017) Amelioration of salinity tolerance in cowpea plants by seed treatment with methyl jasmonate. Legume Res 40:1100–1106 Sahil, Keshan R, Patra A, Mehta S, Abdelmotelb KF, Lavale SA, Chaudhary M, Aggarwal SK, Chattopadhyay A (2021) Expression and Regulation of Stress-Responsive Genes in Plants Under Harsh Environmental Conditions. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 25–44 Salimi F, Shekari F, Hamzei J (2016) Methyl jasmonate improves salinity resistance in German chamomile (Matricaria chamomilla L.) by increasing activity of antioxidant enzymes. Acta Physiol Plant 38:1–14 Saltveit ME (2000) Wound induced changes in phenolic metabolism and tissue browning are altered by heat shock. Postharvest Biol Technol 21:61–69 Savchenko T, Kolla VA, Wang CQ, Nasafi Z, Hicks DR, Phadungchob B, Chehab WE, Brandizzi F, Froehlich J, Dehesh K (2014) Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. Plant Physiol 164:1151–1160 Sayyari M, Babalar M, Kalantari S, Martínez-Romero D, Guillén F, Serrano M, Valero D (2011) Vapour treatments with methyl salicylate or methyl jasmonate alleviated chilling injury and enhanced antioxidant potential during postharvest storage of pomegranates. Food Chem 124:964–970 Sharma P, Sharma MMM, Patra A, Vashisth M, Mehta S, Singh B, Tiwari M, Pandey V (2020) The role of key transcription factors for cold tolerance in plants. In: Transcription factors for abiotic stress tolerance in plants. Academic, London, pp 123–152 Sharma P, Sharma MMM, Malik A, Vashisth M, Singh D, Kumar R, Singh B, Patra A, Mehta S, Pandey V (2021) Rhizosphere, Rhizosphere Biology, and Rhizospheric Engineering. In: Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management. Springer, Cham, pp 577–624 Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, He SY (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405 Shimizu T, Miyamoto K, Miyamoto K, Minami E, Nishizawa Y, Iino M (2013) OsJAR1 contributes mainly to biosynthesis of the stress induced jasmonoyl-isoleucine involved in defense responses in rice. Biosci Biotechnol Biochem 77:1556–1564 Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Bull Natl Res Cent 43:153

Jasmonic Acid for Sustainable Plant Growth and Production Under Adverse…

97

Singh P, Dave A, Vaistij FE, Worrall D, Holroyd GH, Wells JG, Kaminski F, Graham IA, Roberts MR (2017) Jasmonic acid-dependent regulation of seed dormancy following maternal herbivory in Arabidopsis. New Phytol 214:1702–1711 Singh B, Mehta S, Aggarwal SK, Tiwari M, Bhuyan SI, Bhatia S, Islam MA (2019) Barley, disease resistance, and molecular breeding approaches. In: Disease resistance in crop plants. Springer, Cham, pp 261–299 Sirhindi G, Mir MA, Sharma P, Gill SS, Kaur H, Mushtaq R (2015) Modulatory role of jasmonic acid on photosynthetic pigments, antioxidants and stress markers of Glycine max L. under nickel stress. Physiol Mol Biol Plants 21:559–565 Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Xie D (2011) The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23:1000–1013 Staswick PE, Yuen GY, Lehman CC (1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J 15:747–754 Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415 Sun TP (2010) Gibberellin signal transduction in stem elongation & leaf growth. In: Plant hormones. Springer, Dordrecht, pp 303–328 Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665 Tian D, Peiffer M, De Moraes CM, Felton GW (2014) Roles of ethylene and jasmonic acid in systemic induced defense in tomato (Solanum lycopersicum) against Helicoverpa zea. Planta 239:577–589 Trischuk RG, Schilling BS, Low NH, Gray GR, Gusta LV (2014) Cold acclimation, de-acclimation and re-acclimation of spring canola, winter canola and winter wheat: the role of carbohydrates, cold-induced stress proteins and vernalization. Environ Exp Bot 106:156–163 Viswanath KK, Varakumar P, Pamuru RR, Basha SJ, Mehta S, Rao AD (2020) Plant lipoxygenases and their role in plant physiology. J Plant Biol 63:83–95 Vriezen WH, Achard P, Harberd NP, Van Der Straeten D (2004) Ethylene mediated enhancement of apical hook formation in etiolated Arabidopsis thaliana seedlings is gibberellin dependent. Plant J 37:505–516 War AR, Paulraj MG, Ignacimuthu S, Sharma HC (2015) Induced resistance to Helicoverpa armigera through exogenous application of jasmonic acid and salicylic acid in groundnut, Arachis hypogaea. Pest Manag Sci 71:72–82 Wasternack C (2014) Action of jasmonates in plant stress responses and development applied aspects. Biotechnol Adv 32:31–39 Wasternack C, Hause B (2002) Jasmonates and octadecanoids: signals in plant stress responses and development. Prog Nucleic Acid Res Mol Biol 72:165–221 Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058 Wasternack C, Hause B (2019) The missing link in jasmonic acid biosynthesis. Nat Plants 5:776–777 Wasternack C, Song S (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321 Weber H, Chetelat A, Caldelari D, Farmer EE (1999) Divinyl ether fatty acid synthesis in late blight-diseased potato leaves. Plant Cell 11:485–493 Wu H, Wu X, Li Z, Duan L, Zhang M (2012) Physiological evaluation of drought stress tolerance and recovery in cauliflower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. J Plant Growth Regul 31:113–123

98

Sahil et al.

Wu X, Ding C, Baerson SR, Lian F, Lin X, Zhang L, Wu C, Hwang SY, Zeng R, Song Y (2019) The roles of jasmonate signalling in nitrogen uptake and allocation in rice (Oryza sativa L.). Plant Cell Environ 42:659–672 Wuebbles DJ, Fahey DW, Hibbard KA, DeAngelo B, Doherty S, Hayhoe K, Horton R, Kossin JP, Taylor AM, Weaver CP (2017) Climate science special report: a sustained assessment activity of the US global change research program. In: US global change research program. Washington, DC, p 669 Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550 Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094 Yadav B, Jogawat A, Lal SK, Lakra N, Mehta S, Shabek N, Narayan OP (2021) Plant mineral transport systems and the potential for crop improvement. Planta 253:45 Yan Z, Chen J, Li X (2013) Methyl jasmonate as modulator of cd toxicity in Capsicum frutescens var fasciculatum seedlings. Ecotoxicol Environ Saf 98:203–209 Yan Z, Zhang W, Chen J, Li X (2015) Methyl jasmonate alleviates cadmium toxicity in Solanum nigrum, by regulating metal uptake and antioxidative capacity. Biol Plant 59:373–381 Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12 Zhai Q, Zhang X, Wu F, Feng H, Deng L, Xu L, Li C (2015) Transcriptional mechanism of jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27:2814–2828 Zhang X, Sheng J, Li F, Meng D, Shen L (2012) Methyl jasmonate alters arginine catabolism and improves postharvest chilling tolerance in cherry tomato fruit. Postharvest Biol Technol 64:160–167 Zhang X, Zhu Z, An F, Hao D, Li P, Song J, Guo H (2014) Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell 26:1105–1117 Zhang H, Zhang Q, Zhai H, Li Y, Wang X, Liu Q, He S (2017) Transcript profile analysis reveals important roles of jasmonic acid signalling pathway in the response of sweet potato to salt stress. Sci Rep 7:1–12 Zhao ML, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY, Lu WJ (2013) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51

Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment Sahil, Radhika Keshan, Sahil Mehta, K. F. Abdelmotelb, S. K. Aggarwal, Shivaji Ajinath Lavale, Bahadur Singh Jat, Anurag Tripathi, and Laxman Singh Rajput

Abbreviations BA2H Benzoic acid-2-hydroxylase IC Isochorismate ICS Isochorismate synthase IPL Isochorismate pyruvate lyase MeSA Methyl salicylate MeSAG Methyl salicylate O-β-glucoside PAL Phenylalanine ammonia lyase PAL Phenylalanine ammonia-lyase PR Pathogenesis-related proteins SA Salicylic acid SAG SA O-β-glucoside Sahil · R. Keshan Department of Botany, University of Delhi, New Delhi, India S. Mehta International Centre for Genetic Engineering and Biotechnology, New Delhi, India K. F. Abdelmotelb Department of Genetics and Genetic Engineering, Faculty of Agriculture, Zagazig University, Zagazig, Egypt S. K. Aggarwal (*) · B. S. Jat ICAR-Indian Institute of Maize Research, Ludhiana, Punjab, India S. A. Lavale Centre for Plant Biotechnology and Molecular Biology, Kerala Agricultural University, Thrissur, India A. Tripathi GD Goenka School of Agricultural Sciences, Sohna, Haryana, India L. S. Rajput ICAR-Indian Institute of Soybean Research, Indore, Madhya Pradesh, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_5

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SAGT SA glucosyltransferase SAMT SA methyltransferase SGE Salicyloyl glucose ester

1  Introduction Salicylic acid (SA) is strongly established as a modulator for plant defense against biotrophic pathogens through introduction of pathogenesis-related (PR) proteins (Mehta et al. 2021; Viswanath et al. 2020; Dempsey et al. 2011; Lakhssassi et al. 2020). Along with its importance in biotic stress, its requirement is also seen in growth, flowering, fruit ripening, and abiotic stress responses (Rivas-San Vicente and Plasencia 2011; Hara et  al. 2012; Husen et  al. 2018; Zhang and Li 2019). Chemically, SA is a member of plant phenolic compounds. During the initial years of study, SA from plants was not considered important but it gained its value when Cleland and Ajami (1974) first revealed about its distribution in the phloem for signal translocation. Another study by Raskin et  al. (1990) also confirmed SA as a plant hormone involved in thermogenesis in Sauromatum guttatum. After this, many experiments were performed keeping in mind the importance of SA as a plant hormone. The effect of SA on plants depends on concentration where lower levels lead to enhanced antioxidant production and higher concentration can lead to cell demise (Hara et al. 2012; Zaid et al. 2019). The SA biosynthesis in higher plants occurs through the shikimate-phenylpropanoid pathway (Sticher et al. 1997; Zhang and Li 2019) via two different routes that are Phenylalanine Ammonia Lyase (PAL) pathway and Isochorismate (IC) pathway. The study of genetically engineered plants with altered metabolism and synthesis of SA revealed the function of SA in sensing stress and symptom development as well as responses that are hypersensitive such as cell death (Radojičić et al. 2018). The role of SA in abiotic stress can be understood by studying transgenic plants with either its upregulation or downregulation by either overexpression and genome editing (Mehta et al. 2020; Dilawari et al. 2021). For example, many scientists have used SA-deficient transgenic plants for different experiments; these plants express bacteria like salicylate hydroxylase (like-NahG) which forms catechol from SA (Gaffney et al. 1993). At present, this chapter deals with the different roles of SA in various biotic and abiotic stresses along with the signaling mechanism that takes place during the stress responses induced by these stresses.

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2  Biosynthesis and Metabolism 2.1  Biosynthesis Synthesis of salicylic acid has been a subject of debate for more than three decades. Salicylic acid is produced by two different processes, (1) Phenylalanine Ammonia Lyase (PAL) pathway and (2) Isochorismate (IC) pathway. Initial steps of both these routes require Chorismic acid/Chorismate, formed as the result of the Shikimate pathway in the plastid. The suggested pathways for SA biosynthesis are supported by biochemical and genetic evidence. The first enzyme that regulates the phenylpropanoid pathway is PAL producing cinnamate, from which SA is formed (Maeda and Dudareva 2012; Zhang and Liu 2015; Fig.  1). The PAL pathway begins with the deamination of phenylalanine by PAL enzyme, forming trans-cinnamic acid. The acid produces some phenolic compounds like flavonoids, lignin, benzoyl glucosinolates, and volatile benzenoid esters (Dempsey et  al. 2011; Cheynier et  al. 2013; Shahidi and Ambigaipalan 2015). Hence PAL acts as a regulator in primary as well as secondary metabolisms. Cinnamic acid further produces SA with two probable transitional products benzoic acid or O-coumaric acid. The two independent pathways vary in the order of 𝛽-oxidation and ortho-hydroxylation reactions (Raskin 1992). The formation of SA from benzoic acid is mediated by benzoic acid 2-hydroxylase (BA2-­ H) (Garcion and Métraux 2006). Both these pathways being operational in plants have been established by observations or studies showing cinnamic acid transformation to o-coumaric acid by ortho-hydroxylation, thereafter 𝛽-oxidation of o-­ coumaric acid to SA is accelerated during infection by Agrobacterium tumefaciens in tomato. Whereas, the change of cinnamic acid to benzoic acid then to SA was more active in noninfected plants (Chadha and Brown 1974). In another report, synthesis of hydroxybenzoic acids from hydroxycinnamic acids was seen in many plants, supporting the existence of both the pathways (El-Basyouni et  al. 1964). Synthesis of SA by PAL has been suggested after various biochemical experiments using isotope feeding. The pathway is regulated under abiotic and biotic conditions. The genetic studies demonstrate the production of SA from Iso-Chorismate Synthase (ICS) (Chen et al. 2009). Isochorismate (IC) pathway is reported in plants like tomato, Nicotiana benthamiana, Arabidopsis thaliana, and others. Isochorismate synthase (ICS) translates chorismic acid to IC.  In many plant species like rice, tomato, tobacco, soybean, pepper, grapes, etc. the homologs of ICS have been identified. In Arabidopsis, ICS1/SID2 mutants synthesize only 5–10% SA of the total SA produced in nonmutants showing the importance of the gene (Dewdney et al. 2000). Biotic stresses, as well as abiotic stresses such as drought, UV light, and ozone, upregulates ICS1/SID2 (Kilian et  al. 2007; Yokoo et  al. 2018). Double mutants of ics1/sid2 ics2 in Arabidopsis have low concentrations of SA, but SA is present, hinting for an alternate pathway other than the IC pathway (Garcion et al. 2008). Though this pathway is known in many plant species and is also found to be

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Fig. 1  Schematic representation of biosynthesis and metabolism of SA

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conserved in most, still the mechanism of IC conversion to SA is not very clear and requires more work to confirm the pathway.

2.2  Metabolism In plants, the maximum amount of SA is catalyzed by SA glucosyltransferase (SAGT), a pathogen-inducible enzyme forming SA O-β-glucoside (SAG) (Fig. 1). Two SAGT enzymes are reported in Arabidopsis, producing two different end products. Salicyloyl glucose ester (SGE) is scarce as compared to SAG (Dean and Delaney 2008). Salicylic acid is synthesized in the chloroplast, but as observed in a study on tobacco, the SAGT enzyme accumulates in the cytosol. SAG is transported into vacuole from the cytosol, there it is stored in its inactive form and releases SA whenever it is required (Dean et al. 2005; Vaca et al. 2017). Furthermore, SA is also converted to methyl salicylate (MeSA) in plants. In an in vivo study, methyl salicylate (MeSA) and its glucosylated derivative methyl salicylate O-β-glucoside (MeSAG) were found accumulated in high amounts. In cell suspension cultures of tobacco, the MeSA level was five times lesser than MeSAG and SAG whose level was almost the same after conversion from SA which was radiolabeled (Shulaev et al. 1997; Dean et al. 2005). Similar to SAG, MeSA is biologically inactive (Vlot et al. 2009).

3  Salicylic Acid-Mediated Stress Responses Salicylic acid chemically belongs to the phenolic group and plays a variety of roles in many plant species but the mechanism is not yet understood fully. The concentration of SA differs in plant species; for example, in wheat or maize the concentration of SA is lower than 1μg/g fresh weight (that is below optimum level) whereas the rice leaves generally have a concentration of SA that fluctuates between 30 and 40μg/g fresh weight or even more.

3.1  Salicylic Acid in Abiotic Stress Salicylic acid is known to have different functions during biotic stresses as well. The role of SA in various crop plants against different abiotic stresses is reviewed in Table 1.

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Table 1  Review of literature highlighting the role of salicylic acid in various biological and nonbiological stresses S. no Stress type Biotic stresses 1 Powdery mildew (Ervsiphe pisi)

Plant species Pisum sativum L.

Exogenous JA concentration 15 mM

2

Wilt (Fusarium oxysporum)

Cicer arietinum 200.0μM L.

3

Bacterial spot (Xanthomonas campestris) Powdery mildew (Sphaerotheca fuliginea) Citrus canker (Xanthomonas axonopodis)

Solanum 0.109μM lycopersicum L.

4

Cucumis sativus L.

0.2%

References

Reduced the proportions of germlings infecting successfully to form secondary hyphae Significant reduction in disease and hence increase in production Attenuation of disease

Frfy and Carver (1998)

Appreciable disease reduction

Alkahtani et al. (2011)

Increase in mRNA levels of two pathogenesis-­ related genes, CsCHI and CsPR4 100.0– Attains rust resistance 6 Rust (Uromyces Vicia faba L. 1000.0μM and hence increase in viciae-fabae var. yield viciae-fabae) Oryza sativa L. 50.0 mg Upraise in level of 7 Sheath blight protection, improved (Rhizoctonia rice yield solani) 200.0μM Induce resistance to 8 Turnip mosaic Brassica susceptibility of the virus campestris ssp. virus chinensis L. Solanum 50μM, 250μM Lower severity of leaf 9 Leaf curl curl disease, lower (Begomovirus-­ lycopersicum L. and 500μM disease index (DI) ToLCPV) Abiotic stresses

5

Citrus x sinensis (L.) Osbeck

0.25 mM

Plant response

Saikia et al. (2003) AL-Saleh (2011)

Wang and Liu (2012)

Sillero et al. (2012) Sood et al. (2013) Peng et al. (2013) Ong and Cruz (2016)

(continued)

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Table 1 (continued) S. no Stress type 10 Salt stress

11

12

Plant species Triticum aestivum L.

Arabidopsis thaliana (L.) Heynh. Hordeum vulgare L.

Exogenous JA concentration 0.25 mM, 0.50 mM, 0.75 mM and 1 mM 50μM

50μM

13

Dianthus superbus L.

0.5 mM

14

Vigna radiata 50μM (L.) R. Wilczek

15

Cucumis sativus L.

0.3 mM

Plant response Increased fresh and dry masses of both shoot and root, reduced damage to grain yield Improved fresh, dry weight, and water content Increased height and shoot fresh weight, reduced MDA content, enhanced K+ and decreased Na+ in plants Increased fresh weight and biomass, increased transpiration rate, reduced ROS Increased biomass and plant growth, improved relative water content, promoting chlorophyll a content, decreased oxidative damage Increased plant dry weight, improved plant growth and photosynthetic activity, promoted root growth

References Arfan et al. (2007)

Jayakannan et al. (2013) Fayez and Bazaid (2014)

Ma et al. (2017)

Farheen et al. (2018)

Miao et al. (2020)

(continued)

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Table 1 (continued) S. no Stress type 16 Drought stress

Plant species Triticum aestivum L.

Exogenous JA concentration 200 mg L−1

17

Zea mays L.

1 mM

18

Avena sativa L. 100μM

19

Oryza sativa L. 0.5 and 1 nmol/L

20

Hordeum vulgare L.

0.5 mM

Plant response Increased total soluble protein, increased K+ and reduced Na+ in shoots, improved yield Stabilizes membrane, increased chlorophyll a, increased relative water content Reduced amount of putrescine polyamine and increase amount of spermine polyamine leading to alleviation of drought stress Improved germination, enhanced growth, decreased oxidative damage Increased dry weight, fresh weight, and stem length, enhanced relative water content, reduced ROS

References Noreen et al. (2017)

Bijanzadeh et al. (2019)

Canales et al. (2019)

Sohag et al. (2020)

Abdelaal et al. (2020)

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Table 1 (continued) S. no Stress type 21 Heavy metal stress

Plant species Nymphaea tetragona L.

Exogenous JA concentration 20μM

22

Lemna minor L. 50μM

23

Mentha x piperita L.

0.1 mM

24

Solanum tuberosum L.

600μM

25

Oryza sativa L. 50μM and 100μM

Plant response Stabilizes membrane, increased chlorophyll a and b, enhanced antioxidant enzyme activity, increased proline content, mitigates cadmium (Cd) toxicity Reduced Cd accumulation, decreases ROS that is increased by Cd stress, increased antioxidants Reduced Cd content, decreased Cd-induced chlorophyll degradation, increased total phenol content, mitigation of oxidative damage Reduced Cd toxicity, increased chlorophyll content, enhanced proline production, decreased ROS accumulation, improved activities of antioxidant enzymes Reduced growth inhibition by antimony stress, decreased antimony accumulation, enhanced relative water content, reduced proline content, decreased H202 accumulation

References Gu et al. (2018)

Lu et al. (2018)

Ahmad et al. (2018)

Li et al. (2019)

Luo et al. (2020)

(continued)

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Table 1 (continued) S. no Stress type 26 Heat stress

Exogenous JA Plant species concentration Rhododendron 0.5, 1.0, and ‘Fen Zhen Zhu’ 2.0 mM L.

27

Triticum aestivum L.

28

Solanum 1 mM lycopersicum L.

29

Capsicum annuum L.

0.002, 0.01, 0.05, and 0.25 mM

30

Medicago sativa L.

0.25 mM and 0.5 mM

0.1 mM

Plant response Decreased leaf damage rate, increased activity of antioxidant enzymes, reduced H2O2 content Lowered electrolyte leakage, increased proline and sugar content, enhanced soluble proteins and chlorophyll content Mitigated repercussions of heat stress, increased total chlorophyll, increased stomatal conduction and transpiration rates, enhanced activity of antioxidant enzymes Improved thermotolerance, increased chlorophyll content till 0.1 mM SA, enhanced water content, increased activity of antioxidant enzymes Improved plant height and biomass, stabilizes membrane, enhanced chlorophyll content, increased catalase activity but decreased peroxidase and superoxide dismutase activities

References Shen et al. (2016)

Munir et al. (2018)

Jahan et al. (2019)

Zhang et al. (2019)

Wassie et al. (2020)

(continued)

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Table 1 (continued) S. no Stress type 31 Cold stress

Plant species Hordeum vulgare L.

Exogenous JA concentration 0.1 mM

32

Dendrobium officinale (L.) Sw.

0.5, 1.0, 1.5 and 2.0 mM

33

Spinacia oleracea L.

0.25, 0.5, 1.0 and 2.0 mM

34

Triticum aestivum L.

25–200μM

35

Triticum aestivum L.

100μM

Plant response Decreased MDA content, increased H2O2 content in tolerant plants whereas H2O2 content in sensitive plants, enhanced superoxide dismutase, peroxidase, and catalase activity Alleviated the decline in chlorophyll content, decreased MDA content at lower SA concentration that increase with increase in SA concentration, enhanced net photosynthesis rate Mitigated harmful effects of freezing injury, reduced ROS, increased proline content 100μM SA has more positive effect on cold tolerance, reduced MDA accumulation, increased proline content Enhanced plant height and single stem dry weight, increased grain yield, improved content of free proline and soluble sugars, increased activity of antioxidant enzymes

References Mutlu et al. (2016)

Huang et al. (2016)

Shin et al. (2018)

Ignatenko et al. (2019)

Wang et al. (2021)

3.1.1  Heat Stress With the rise in atmospheric temperature globally, the risk of plants getting exposed and damaged by high temperatures is on a rise  (Bharti et  al. 2021; Mehta et  al. 2021). The stress of high temperature poses a severe menace to the plants as it leads to the production of ROS, loss of membrane integrity, and protein aggregation and inactivation that ultimately leads to death of the cell (Los and Murata 2000; Iba 2002; Ergin et al. 2016; Lal et al. 2018). Heat stress primarily disturbs the photochemical reactions occurring in the thylakoid lamellae inside the chloroplast (Bharti et  al. 2021;  Wise et  al. 2004). To counter this effect of heat, plants maintain the

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photosynthesis continuously. During heat stress, cooling is brought about by reduced transpiration by plants insufficient water condition but when heat stress continues to rise, plants activate various defense mechanisms through increased production of SA, jasmonic acid (JA) and heat-shock proteins (HSPs) (Clarke et al. 2004; Larkindale and Huang 2005; Merret et al. 2017). Salicylic acid regulates thermotolerance in a concentration-dependent manner. For example, Brassica plants sprayed with a low concentration of SA at about 0.01–0.1 mM resulted in enhanced plant protection against heat stress (Dat et al. 1998). Also, treatment of 0.01  mM SA on tobacco improved thermotolerance whereas the treatment with 0.10 mM SA was ineffective (Dat et al. 2000). The use of SA inhibitors reduced the internal SA levels and also lowered the amount of heat tolerance largely which revealed the direct importance of SA biosynthesis for tolerance to heat stress (Pan et al. 2006). In pea leaves, the activity and amount of P-type H+ ATPase are enhanced by heat-inducible SA through heat acclimation pointing to the fact that the P-type H+ ATPase is essential for maintaining membrane integrity during high-temperature stress (Liu et al. 2009). Two types of thermotolerance are studied in plants, viz. basal thermotolerance and acquired thermotolerance. Basal tolerance is the one in which plants can tolerate high temperatures even by avoiding heat acclimation or any type of treatment with chemicals whereas acquired tolerance signifies that the plants when exposed to mild stress can gain tolerance against lethal stress levels (Clarke et al. 2004). It is seen that SA, abscisic acid (ABA), and ROS contribute to the acquired thermotolerance (Larkindale and Huang 2005). The role of SA in basal thermotolerance is also demonstrated by Clarke et al. (2004) where it was not observed in acquired thermotolerance. Another study by Liu et al. (2006) suggests that SA acts downstream to ABA. However, unlike ABA, SA is not required in the making of HSP (Larkindale and Huang 2005; Liu et al. 2006). The positive influence of exogenous employment of SA in the alleviation of heat stress has been reported in several plants, namely Triticum aestivum (Munir et al. 2018), Rhododendron (Shen et al. 2016), Capsicum annuum (Zhang et al. 2019), Solanum lycopersicum (Jahan et al. 2019), and Medicago sativa (Wassie et al. 2020) among many others. Increased chlorophyll content and upregulation of antioxidant enzyme activity were the most prevalent SA-mediated phenotyping responses in these plants. Other responses like lower electrolyte leakage (in Triticum aestivum), increased stomatal conductance and transpiration rate (in Solanum lycopersicum), better thermotolerance (in Capsicum annuum), and enhanced overall yield and biomass were some of the other significant response. 3.1.2  Cold Stress Similar to high-temperature stress, low-temperature stress or cold stress is also hazardous to the plants. The decline in the amount and pace of nutrients along with water uptake is enforced by this type of abiotic stress. Cold stress is divided into freezing stress and chilling stress (Mehta et  al. 2019;  Sharma et  al. 2020). The

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chilling stress is observed when the temperature is below 20 °C whereas freezing stress appears when the temperature is lower than 0 °C. Both these stresses negatively affect plant growth and quality (Kasuga et al. 1999; Lang et al. 2005; Suh et al. 2010; Josine et al. 2011). The freezing stress is an extreme type of cold stress where cells are filled with ice crystals, causing dehydration, and ultimately the death of plants. The collection of free SA and SA glucosyl is enhanced by cold stress in wheat, Arabidopsis, berry, and grape (Scott et  al. 2004; Wan et  al. 2009; Kosova et  al. 2012), indicating the function of SA in response to cold stress. Exogenous application of SA, irrespective of the mode of application, can increase tolerance for cold in plants (Janda et al. 1999, 2000). For example, chilling tolerance in young maize plants was increased after the hydroponic application of SA and other phenolic compounds at 0.50  mM concentration (Horvath et  al. 2002). Along with the increased stress tolerance, there was also an enhancement of guaiacol peroxidase and glutathione reductase activity and a decrease in catalase activity. Another study by Kang and Saltveit (2002) showed that upon hydroponic application of exogenous SA to maize, cucumber, and rice, there was an increase in chilling tolerance only in shoots and not in the roots and the similar enzyme activities. External treatment of SA at 0.10 mM and 0.50 mM induced cold tolerance in potato plants and banana seedling, respectively (Mora-Herrera et al. 2005; Kang et al. 2003). The role of SA in freezing tolerance is ambiguous. Tasgín et al. (2003) suggest that the exogenous application of SA reduced the injury in wheat leaves growing in low-temperature conditions. Another study has shown that chilling tolerance is regulated by the action of ethylene and not that of SA because ethylene was observed to increase antifreeze activity (Yu et al. 2001). SA-mediated mitigation of cold stress has been established in many plants (Table  1). Application of 0.1  mM SA in Hordeum vulgare resulted in enhanced antioxidant activity and decreased MDA content with incremental H2O2 content intolerant plants (Mutlu et al. 2016). Specific amounts of SA application on Triticum aestivum manifested positive effects in terms of overall yield, proline content, cellular content of soluble sugars, and antioxidant enzyme activity (Ignatenko et al. 2019; Wang et al. 2021). The positive influence of SA employment was also registered in Dendrobium officinale (Huang et  al. 2016) and Spinacia oleracea (Shin et al. 2018) with reduced MDA and ROS content, enhanced chlorophyll content, increased photosynthetic rates, and increased proline content. 3.1.3  Salinity and Osmotic Stress Salt stress is responsible not only for sodium toxicity but also for osmotic stress (Anamika et al. 2019). Salinity stress can be harmful in many ways like the adverse impact on the photosynthetic activity of the plant leading to a decline in the biomass production (Munns 2007; Rasool et al. 2013; Abdel Latef and Chaoxing 2014; Husen et al. 2016, 2018, 2019; Hussein et al. 2017) and destruction of ionic homeostasis. The NaCl is a major contributor to salt stress. Plants have developed

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methods to reduce its accumulation and replace it with other nutrients like K+ and NO3− that are present in low concentrations. In Arabidopsis thaliana, SA participates in the symptom generation during salinity and osmotic stress by generating ROS in photosynthetic regions (Borsani et al. 2001). In rice plants, the amount of SA and the activity of benzoic acid 2-­hydroxylase were increased during salinity stress (Sawada et al. 2006). The external application of SA can also improve salt tolerance in many species. For example, in sunflower, oil content, as well as the yield, increased by the use of SA, whereas in wheat, enhanced grain yield is observed as a result of SA application (Noreen and Ashraf 2010; Arfan et al. 2007). In barley, SA treatment resulted in improved protective responses to various photosynthetic pigments together with improvement in membrane integrity and maintenance, thereby enhancing the growth of plants (El Tayeb 2005). In SA-treated maize plants, processes like membrane permeability and lipid peroxidation decreased as the plant matured (Gunes et al. 2007). When added to a hydroponic solution of polyethylene glycol and media in which the wheat seedlings were growing, SA increased tolerance to osmotic stress effects (Marcinska et al. 2013). Many recent reports pertinent to salt stress mitigation by the employment of SA on Triticum aestivum (Arfan et al. 2007), Arabidopsis thaliana (Jayakannan et al. 2013), Hordeum vulgare (Fayez and Bazaid 2014), Dianthus superbus (Ma et al. 2017), Vigna radiata (Farheen et al. 2018), and Cucumis sativus (Miao et al. 2020) have revealed improved growth in terms of biomass, reduced MDA and ROS content, maintenance of K+/Na+ ratio, and improved relative water content, among many others. 3.1.4  Drought Stress Drought stress is one of the most prevalent stresses that cause yield reduction in most of the crops (Sharma et al. 2021; Mehta et al. 2020; Pushpavalli et al. 2015; Husen 2010; Husen et  al. 2014, 2017; Getnet et  al. 2015; Embiale et  al. 2016; Mathobo et al. 2017; Lal et al. 2018). Plants protect themselves from this type of stress by employing two different strategies, drought avoidance and drought tolerance (Blum 2005). In the case of drought avoidance, plants avoid drought stress by maintaining high water levels when there is water scarcity in the root zone. For example, as observed in cactus plants, the roots are deeply seated inside the soil so as to increase water inside the plant by collecting it from deep soil or by closing the stomata so as to reduce transpirational loss as major transpiration occurs through stomata. In the case of drought tolerance, plants keep growing in stressful conditions to yield normally. In general, drought stress tends to incorporate many negative changes in the plants. Some of them are listed below: 1. Alterations in the source-sink relationship by decreasing the translocation of carbohydrates (Liu et al. 2004). 2. Depletion in nutrient uptake because of water scarcity in the soil.

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3. Reduced rate of root growth because of dry soil. Abscisic acid is designated as a crucial phytohormone playing a part in different stresses, majorly the water-deficient conditions. Studies have shown that upon water deprivation, the ABA hormone gets synthesized and distributed inside the plants. This hormone tends to close the stomata through ROS production (Acharya and Assmann 2009). Along with ABA, SA also modulates various drought stress responses. During conditions where the water availability was minimal, the SA concentration was found to have increased by twofolds in barley (Bandurska and Stroinski 2005). Drought stress also activated certain genes such as PR1 and PR2 (Miura et al. 2013). This clearly shows the involvement of SA in drought tolerance but the mechanism is still not known because of the divergent results obtained from studies conducted to know the role of SA in drought tolerance where some show a positive effect whereas others claim a negative effect. Kang et al. (2012) found that a higher amount of SA suppresses both the drought tolerance and growth of wheat seedlings whereas a lower amount of SA promotes the plant growth. The resistance to water-deficient conditions is found in wheat when treated with 100 ppm acetyl SA (Hamada 2001). The treatment of SA to barley caused a reduction in repercussions of water scarcity on the cell membrane of barley leaves along with the increase in ABA and proline (Bandurska and Stroinski 2005) as well as a significant improvement in growth parameters and relative water content (Abdelaal et  al. 2020) Employment of SA, in different molar ratios, to Triticum aestivum (Noreen et al. 2017), Zea mays (Bijanzadeh et al. 2019), Avena sativa (Canales et al. 2019), and Oryza sativa (Sohag et al. 2020) resulted in positive influence over plant growth, manifested in the form of improved K+/Na+ ratios, reduced chlorophyll content, increased amount of spermine, and improved germination, respectively. 3.1.5  Heavy Metal Stress Heavy metal stress in one of the most challenging threats among the abiotic stresses (Nagajyoti et al. 2010; Hassan et al. 2017). All the elements having higher atomic density are called heavy metals, comprising both the essential and nonessential elements. Heavy metals are incorporated in the soil through many sources such as natural sources (rock weathering), industrial sources (chemical industries), burning of fossil fuels, agricultural sources (use of chemical pesticides and insecticides), etc. (Mishra and Tripathi 2008; Asati 2013). The heavy metals are contaminants of the soil that can be very harmful to the plants because of the following reasons: 1. The increasing anthropogenic activities have resulted in the speeding up of the rate of addition of these heavy metals leading to a high concentration in the soil. 2. Presence of bioavailable form of heavy metals that can be readily up-taken by the plants. 3. Random deposition of heavy metals in the environment can result in direct exposure of plants to this stress.

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This type of stress causes oxidative damage through the generation of ROS that damages DNA and protein and also leads to the inactivation of vital enzymes (Das and Jayalekshmy 2015; Lu et al. 2017). Early experiments performed on the impact of SA on heavy metals revealed that harmful effects of Hg2+ and Pb2+ on rice seed sprouting and seedling growth was decreased by SA application (Mishra and Choudhuri 1997). Exogenous employment of SA leads to a decline in Hg2+, Mn2+, Cd2+, and Ni2+ toxicity via the antioxidant system (Shi and Zhu 2008; Zhou et al. 2009; Popova et al. 2009; Wang et al. 2009). In Cd-treated rice, external application of SA increased the accumulation of antioxidants along with the increase in the concentration of glutathione and some nonprotein thiols (Guo et al. 2009) as well reduced antimony accumulation, enhanced relative water content, and decreased H2O2 accumulation (Luo et al. 2020). This increase in the antioxidant system causes a decrease in damage by ROS as revealed by the lower H2O2 and malondialdehyde (product obtained from lipid peroxidation). Crops like pea and maize were shown to accumulate SA when treated with Cd (Popova et al. 2009; Pál et al. 2005; Krantev et al. 2008; Tao et al. 2013). The positive influence of SA application has also been recently reported in several plants, namely Nymphaea tetragona (Gu et al. 2018), Lemna minor (Lu et al. 2018), Mentha piperita (Ahmad et al. 2018), and Solanum tuberosum (Li et  al. 2019), all of which reported reduced cadmium toxicity, improved activity of antioxidant enzymes and, thus, decreased ROS accumulation.

3.2  Salicylic Acid in Biotic Stress Several studies have shown that a plant infected with a particular pathogen activates a defense response that results in increased resistance (Rajput et  al. 2021; Sahil et al. 2021; Wasternack and House 2013). Plants can synthesize certain resistance (R) proteins against different avirulence (Avr) factors produced by the various pathogens. The R-avr interaction initiates a hypersensitive response (HR). This HR mediates cell death at the point of pathogen entry, and increases the accumulation of Reactive Oxygen Species (ROS) (Conrath et al. 2001; Galluzzi et al. 2018; Salguero-­ Linares and Coll 2019), further inducing various pathogenesis-related (PR) genes. After this, Systemic Acquired Resistance (SAR) is developed in plants (Gary and Goodman 2004; Spoel and Dong 2012; Fu and Dong 2013). SAR is a type of induced resistance where the signal travels long distances throughout the plant making it a whole-plant resistance (Vlot et  al. 2009; Singh et  al. 2017; Wendehenne et al. 2014). Salicylic acid accumulation regulates the induction of SAR which correlates with the expression of PR genes (Yalpani et  al. 1991; Durrant and Dong 2004; Sekhon and Sangha 2019). Initial experiments performed by White (1979) revealed that SA is an endogenous signal for resistance response. Malamy et al. (1990) found increased levels of SA post-infection with tobacco mosaic virus in resistant plants and there were no increased levels of SA in susceptible plants. Various other studies revealed a correlation between change in SA concentration and the redox state

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maintenance of cells by regulation of antioxidant gene expressions (Rao and Davis 1999; Vanacker et al. 2000; El-Esawi et al. 2017). During the pathogen attack, there is an increased synthesis of SA that induces redox changes in the cell. Redox changes in cells influence the activity of a transcription factor (TF) named Non-Expressor of Pathogenesis Related gene 1 (NPR1) (Mou et al. 2003; Goodspeed et al. 2012). It is present in an oligomeric state in the cytoplasm that upon redox changes gets converted to a monomeric state, which is an active state, by a reduction in the intermolecular disulfide bond. The NPR1, in an active state, translocates into the nucleus where it enhances the binding of other TFs with the promoters of SA-mediated genes, thereby resulting in expression and regulation of PR genes (Mou et al. 2003; Dong 2004). NPR1 persistence in the monomeric state because of the inhibition of the reduction of NPR1 resulted in a decreased synthesis of PR proteins. Whereas overexpression of NPR1 resulted in constitutive expression of PR genes, even when any activation was absent, showing SAR to be positively regulated by NPR1 (Cao et al. 1994; Mou et al. 2003). Various pathways for SA responses that do not depend on NPR1 have been studied indicating the presence of other unknown proteins important for SA signaling (Robert-Seilaniantz et al. 2011; Halder et al. 2019). The exogenous treatment of SA to plants suffering from various diseases has allowed minimizing the impact of diseases like citrus canker, bacterial spot, leaf mosaic, wilt, etc. which has been depicted in Table 1.

4  Salicylic Acid-Mediated Signaling Pathways Non-expressor of Pathogenesis Related gene 1 (NPR1), also called SAI1 or NIM1, is a transcription factor (TF) that is responsible for downstream signaling mediated by SA. The protein plays a role in the activation of the PR-1 gene in the nucleus and it also takes part in the interaction between JA and SA in the cytosol (Spoel et al. 2003). NPR1 in the cytosol are present in the form of oligomers joined with disulfide bonds, and when there is a change in cellular redox state induced by SA, the protein oligomer converted to monomers reducing (Cys82 and Cys216) two cysteine residues by the action of THIOREDOXIN-H3 (TRX-H3) or TRX-H5 (Mou et al. 2003). Transcription of the defense gene occurs when NPR1 monomers translocate from the cytosol into the nucleus. NPR1 mutants in the nucleus showed permanent high resistance when present in monomeric form. The level of nuclear NPR1 monomers elevates on a mutation of Cys82 or Cys216, confirming the correlation with the increased transcription of PR-1 (Mou et al. 2003). However, these NPR1 mutant plants were unable to show SAR response which was SA dependent due to high NPR1 degradation. These studies could conclude that for the complete functioning of SA-mediated signaling in building up resistance, both the process of NPR1 monomerization and its repeated oligomerization are important (Tada et al. 2008; Fu and Dong 2013). Storage of oligomers of NPR1 occurs in cytoplasm mainly because of two reasons, firstly, to avoid unwanted activation of stress responses in the absence of any

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Fig. 2  Signaling pathway involved in the expression of defense genes and other mechanism mediated by salicylic acid under stress conditions

pathogen; the other is to maintain a static balance of NPR1 protein during stress response mechanism in the nucleus. The NPR1 substratum is potentially a signaling repressor for SA.  NPR1 interacts physically with TGA and NIM1-interacting (NIMIN) proteins. TGAs specifically induce target gene expression, while NIMINs repress expression (Fig. 2). Two different domains are present in NPR1, BTB/POZ domain and motif of ankyrin-repeat, which enables it to bind to Cullin 3 E3 ubiquitin ligase and act as an adaptor protein. Cullin 3 E3 ubiquitin ligase polyubiquitinates NPR1 and results in ubiquitin-mediated proteolysis through 26S proteasome. NPR1 degradation by proteasome occurs before the induction of stress response and also later. The degradation after initiation of a stress response is necessary for the action of the target genes of NPR1 (Zhang et al. 2003).

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5  C  ross talk Between Salicylic Acid and Other Plant Hormones Cross talk of SA with other plant regulators occurs in stressed as well as normal conditions due to the participation of SA in many physiological activities. This is important for maintaining a balance in a plant for its growth and action against the defense. Many studies have reported the relationship of SA with the plant hormones like cytokinin, auxin, gibberellins, brassinosteroids, etc. under stressed conditions to be both synergistic and antagonistic meaning either depends on concentration or are specific to tissues and dynamic (Mur et al. 2006; Kohli et al. 2017). In barley, heavy metal-induced ROS production in roots mediated by auxin is observed, which is restricted by regulation of SA (Tamás et al. 2015). In Maize, SA and indole-3-acetic acid (IAA) played opposite roles. External use of IAA decreased the growth of the primary root while increasing lateral growth, whereas the total biomass of root increased by the use of SA. It clearly shows, SA holds a part in the IAA signaling pathway as found in plants treated with SA showed reverse IAA-­ induced stress responses (Agtuca et al. 2014). During abiotic stresses, induction of ethylene-responsive genes increases the production of ethylene in plants which induces oxidative stress. SA application suppresses the induction of ROS in the process of ethylene biosynthesis (Kovács et al. 2014). Interaction between SA and JA is important for regulation in plant growth during environmental stress. Signaling pathways of SA and JA generally interact antagonistically (Khan and Khan 2013). The antagonistic action between SA and JA cell signaling is conciliated by the Mitogen-activated protein kinase (MAPK) signaling pathway (Petersen et al. 2000). In wheat seedlings, the exogenous use of SA increased ABA levels under stress. In plants, internal ABA controls the regulation mediated by SA demonstrating its protective mechanism (Shakirova et al. 2016). SA and ABA are found to regulate guard cell mechanisms together (Prodhan et al. 2018). Also, the interaction between SA and brassinosteroids is very helpful in alleviating stress. Rice plants are made tolerant against pathogens by brassinosteroids by regulating SA (Pan et al. 2018).

6  Conclusions In many countries like India, the economy hugely relies on agriculture, which in turn depends on both soil fertility and suitable climatic conditions. However, over the past decades, environmental perturbations are posing a huge number of harms to the plants. As a result, a huge emphasis has been given on diving into the phytohormone engineering. This interesting field of research comprises two steps, the former one enhances the knowledge of the hormone-related characteristics (synthesis, signaling, and functions) and latter utilizing the generated knowledge for broader application, i.e., development of stable phytohormone-engineered crops that does

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not compromise on growth, tolerance, and yield. The major reason lies in the involvement of phytohormones in direct or indirect regulation of the expression of multiple stress-responsive genes. One such multidimensional studied hormone under fluctuating environmental conditions is SA that induce the plant’s tolerance and adaptations. This hormone has been reported to be involved from physiological metabolic processes to defense against a variety of stresses by cross talking with other biomolecules. To support the statement, there are bundles of reports already available in the literature that advocate the use of foliar spray or amendment of SA at an appropriate concentration in mitigating detrimental repercussions of various environmental stresses. The effects of SA external employment on plants include increased growth, biomass, fresh and dry weight, chlorophyll content, membrane stability, levels of antioxidants, and reduction in oxidative and osmotic damage. So, the use of SA in particular stress has proven to be helpful for the plant to fight against both biological and nonbiological conditions. However, still, there is a huge list of questions that need to be answered. For example, extensive work has to be performed in understanding the events of signal perception, genes expressivity, and homologs involved in SA biosynthetic pathways in non-model plant species. An in-depth study is also needed to unravel the advanced system of SA-regulated genes under the combinatorial stresses. Furthermore, deploying the robust multi-omics approaches at a time will also unravel the unambiguous, precise nodes and convergence points of SA network with other phytohormones, small RNAs, and protein modifications. Taking all points together, on a long way to the future, the super stress-tolerant crop varieties will be developed that will not show any major yield penalties under challenging conditions.

References Abdel Latef AA, Chaoxing H (2014) Does the inoculation with Glomus mosseae improves salt tolerance in pepper plants? J Plant Growth Regul 33:644–653 Abdelaal KA, Attia KA, Alamery SF, El-Afry MM, Ghazy AI, Tantawy DS, Al-Doss AA, El-Shawy ESE, Abu-Elsaoud AM, Hafez YM (2020) Exogenous application of proline and salicylic acid can mitigate the injurious impacts of drought stress on barley plants associated with physiological and histological characters. Sustainability 12:1736 Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462 Agtuca B, Rieger E, Hilger K, Song L, Robert CA, Erb M, Ferrieri RA (2014) Carbon-11 reveals opposing roles of auxin and salicylic acid in regulating leaf physiology, leaf metabolism, and resource allocation patterns that impact root growth in Zea mays. J Plant Growth Regul 33:328–339 Ahmad B, Jaleel H, Sadiq Y, Khan MMA, Shabbir A (2018) Response of exogenous salicylic acid on cadmium induced photosynthetic damage, antioxidant metabolism and essential oil production in peppermint. Plant Growth Regul 86:273–286 Alkahtani M, Omer SA, El-Naggar MA, Abdel-Kareem EM, Mahmoud MA (2011) Pathogenesis-­ related protein and phytoalexin induction against cucumber powdery mildew by elicitors. Int J Plant Pathol 2:63–71

Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment

119

AL-Saleh MA (2011) Pathogenic variability among five bacterial isolates of Xanthomonas campestris pv. vesicatoria, causing spot disease on tomato and their response to salicylic acid. J Saudi Soc Agric Sci 10:47–51 Anamika, Mehta S, Singh B, Patra A, Islam MA (2019) Databases: a weapon from the arsenal of bioinformatics for plant abiotic stress research. In: Recent approaches in Omics for plant resilience to climate change. Springer, Cham, pp 135–169 Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress. J Plant Physiol 164:685–694 Asati SR (2013) Treatment of waste water from parboiled rice mill unit by coagulation/flocculation. Int J Life Sci Biotechnol Pharm Res 2:264–277 Bandurska H, Stroinski A (2005) The effect of salicylic acid on barley response to water deficit. Acta Physiol Plant 27:379–386 Bharti J, Sahil, Mehta S, Ahmad S, Singh B, Padhy AK, Srivastava N, Pandey V (2021) Mitogen-­ Activated Protein Kinase, Plants, and Heat Stress. In Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp. 323–354 Bijanzadeh E, Naderi R, Egan TP (2019) Exogenous application of humic acid and salicylic acid to alleviate seedling drought stress in two corn (Zea mays L.) hybrids. J Plant Nutr 42:1483–1495 Blum A (2005) Drought resistance, water-use deficiency, and yield potential—are they compatible, dissonant, or mutually exclusive. Aust J Agric Res 56:1159–1168 Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidat2ive damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030 Canales FJ, Montilla-Bascón G, Rispail N, Prats E (2019) Salicylic acid regulates polyamine biosynthesis during drought responses in oat. Plant Signal Behav 14:e1651183 Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 8:1583–1592 Chadha KC, Brown SA (1974) Biosynthesis of phenolic acids in tomato plants infected with Agrobacterium tumefaciens. Can J Bot 52:2041–2047 Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal Behav 4:493–496 Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20 Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447 Cleland CF, Ajami A (1974) Identification of the flower-inducing factor isolated from aphid honeydew as being salicylic acid. Plant Physiol 54:904–906 Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119 Das R, Jayalekshmy VG (2015) Mechanism of heavy metal tolerance and improvement of tolerance in crop plants. J Glob Biosci 4:2678–2698 Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357 Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (2000) Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J Plant Physiol 156:659–665 Dean JV, Delaney SP (2008) Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Plant Physiol 132:417–425 Dean JV, Mohammed LA, Fitzpatrick T (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221:287–296

120

Sahil et al.

Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156 Dewdney J, Reuber TL, Wildermuth MC, Devoto A, Cui J, Stutius LM, Ausubel FM (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24(2):205–218 Dilawari R, Kaur N, Priyadarshi N, Kumar B, Abdelmotelb KF, Lal SK, Singh B, Tripathi A, Aggarwal SK, Jat BS, Mehta S (2021) Genome Editing: A Tool from the Vault of Science for Engineering Climate-Resilient Cereals. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 45–72 Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552 Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209 El Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224 El-Basyouni S, Chen D, Ibrahim RK, Neish AC, Towers GHN (1964) The biosynthesis of hydroxybenzoic acids in higher plants. Phytochemistry 3:485–492 El-Esawi MA, Elansary HO, El-Shanhorey NA, Abdel-Hamid AM, Ali HM, Elshikh MS (2017) Salicylic acid-regulated antioxidant mechanisms and gene expression enhance rosemary performance under saline conditions. Front Physiol 8:716 Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Ergin S, Gülen H, Kesici M, Turhan E, Ipek A, Köksal N (2016) Effects of high temperature stress on enzymatic and nonenzymatic antioxidants and proteins in strawberry plants. Turk J Agric For 40:908–917 Farheen J, Mansoor S, Abideen Z (2018) Exogenously applied salicylic acid improved growth, photosynthetic pigments and oxidative stability in mungbean seedlings (Vigna radiata) at salt stress. Pak J Bot 50:901–912 Fayez KA, Bazaid SA (2014) Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J Saudi Soc Agric Sci 23:45–55 Frfy S, Carver TLW (1998) Induction of systemic resistance in pea to pea powdery mildew by exogenous application of salicylic acid. J Phytopathol 146:239–245 Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863 Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756 Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, Annicchiarico-Petruzzelli M (2018) Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 25:486–541 Garcion C, Métraux JP (2006) FiRe and microarrays: a fast answer to burning questions. Trends Plant Sci 11(7):320–322 Garcion C, Lohmann A, Lamodière E, Catinot J, Buchala A, Doermann P, Métraux JP (2008) Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol 147(3):1279–1287 Gary EV, Goodman RM (2004) Systemic acquired resistance and induce systemic resistance in conventional agriculture. Crop Sci 44:1920–1934 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202 Goodspeed D, Chehab EW, Minvenditti A, Braam J, Covington MF (2012) From the cover: Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci U S A 109:4674–4677

Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment

121

Gu CS, Yang YH, Shao YF, Wu KW, Liu ZL (2018) The effects of exogenous salicylic acid on alleviating cadmium toxicity in Nymphaea tetragona Georgi. S Afr J Bot 114:267–271 Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736 Guo B, Liang Y, Zhue Y (2009) Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice. J Plant Physiol 166:20–31 Halder V, Suliman MN, Kaschani F, Kaiser M (2019) Plant chemical genetics reveals colistin sulphate as a SA and NPR1-independent PR1 inducer functioning via a p38-like kinase pathway. Sci Rep 9:1–12 Hamada AM (2001) Salicylic acid versus salinity-drought-induced stress on wheat seedlings. Rostl Vyroba 47:444–450 Hara M, Furukawa J, Sato A, Mizoguchi T, Miura K (2012) Abiotic stress and role of salicylic acid in plants. In: Abiotic stress responses in plants. Springer, New York, pp 235–251 Hassan TU, Bano A, Naz I (2017) Alleviation of heavy metals toxicity by the application of plant growth promoting rhizobacteria and effects on wheat grown in saline sodic field. Int J Phytoremediation 19:522–529 Horvath E, Janda T, Szalai G, Páldi E (2002) In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Sci 163:1129–1135 Huang C, Wang D, Sun L, Wei L (2016) Effects of exogenous salicylic acid on the physiological characteristics of Dendrobium officinale under chilling stress. Plant Growth Regul 79:199–208 Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186 Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata a. Br.). Agric Food Secur 7:44 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of Niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53:225–245 Ignatenko A, Talanova V, Repkina N, Titov A (2019) Exogenous salicylic acid treatment induces cold tolerance in wheat through promotion of antioxidant enzyme activity and proline accumulation. Acta Physiol Plant 41:80 Jahan MS, Wang Y, Shu S, Zhong M, Chen Z, Wu J, Sun J, Guo S (2019) Exogenous salicylic acid increases the heat tolerance in Tomato (Solanum lycopersicum L) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. Sci Hortic 247:421–429 Janda T, Szalai G, Tari I, Páldi E (1999) Hydroponic treatment with salicylic acid decreases the effect of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

122

Sahil et al.

Janda T, Szalai G, Antunovics ZS, Horvath E, Páldi E (2000) Effect of benzoic acid and aspirin on chilling tolerance and photosynthesis in young maize plants. Maydica 45:29–33 Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2013) Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J Exp Bot 64:2255–2268 Josine TL, Ji J, Wang G, Guan CF (2011) Advances in genetic engineering for plants abiotic stress control. Afr J Biotechnol 10:5402–5413 Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576 Kang GZ, Wang CH, Sun GC, Wang ZX (2003) Salicylic acid changes activities of H2O2-­ metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ Exp Bot 50:9–15 Kang G, Li G, Xu W, Peng X, Han Q, Zhu Y (2012) Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J Proteome Res 11:6066–6079 Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt and freezing tolerance by gene transfer of a single stress inducible transcriptional factor. Nat Biotechnol 17:287–291 Khan MIR, Khan NA (2013) Salicylic acid and jasmonates: approaches in abiotic stress tolerance. J Plant Biochem Physiol 1:4 Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50(2):347–363 Kohli SK, Handa N, Kaur R, Kumar V, Khanna K, Bakshi P, Bhardwaj R (2017) Role of salicylic acid in heavy metal stress tolerance: insight into underlying mechanism. In: Salicylic Acid: A Multifaceted Hormone. Springer, Singapore, pp 123–144 Kosova K, Prasil IT, Vitamvas P, Dobrev P, Motyka V, Flokova K (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576 Kovács V, Gondor OK, Szalai G, Darkó É, Majláth I, Janda T, Pál M (2014) Synthesis and role of salicylic acid in wheat varieties with different levels of cadmium tolerance. J Hazard Mater 280:12–19 Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931 Lakhssassi N, Piya S, Bekal S, Liu S, Zhou Z, Bergounioux C, Miao L, Meksem J, Lakhssassi A, Jones K, Kassem MA (2020) A pathogenesis-related protein GmPR08-Bet VI promotes a molecular interaction between the GmSHMT08 and GmSNAP18 in resistance to Heterodera glycines. Plant Biotechnol J 18:1810–1829 Lal SK, Kumar S, Sheri V, Mehta S, Varakumar P, Ram B, Borphukan B, James D, Fartyal D, Reddy MK (2018) Seed priming: an emerging technology to impart abiotic stress tolerance in crop plants. In: Advances in seed priming. Springer, Singapore, pp 41–50 Lang P, Zhang CK, Ebel RC, Dane F, Dozier WA (2005) Identification of cold acclimated genes in leaves of Citrus unshiu by mRNA differential display. Gene 359:111–118 Larkindale J, Huang BR (2005) Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul 47:17–28 Li Q, Wang G, Wang Y, Yang D, Guan C, Ji J (2019) Foliar application of salicylic acid alleviates the cadmium toxicity by modulation the reactive oxygen species in potato. Ecotoxicol Environ Saf 172:317–325 Liu F, Jensen CR, Andersen MN (2004) Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crops Res 86:1–13

Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment

123

Liu H, Liu Y, Pan Q, Yang H, Zhan J, Huang W (2006) Novel interrelationship between salicylic acid, abscisic acid, and PIP 2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347 Liu Y, Liu H, Pan Q, Yang H, Zhan J, Huang W (2009) The plasma membrane H+ ATPase is related to the development of salicylic acid-induced thermotolerance in pea leaves. Planta 229:1087–1098 Los DA, Murata N (2000) Regulation of enzymatic activity and gene expression by membrane fluidity. Sci Signal 62:pe1 Lu T, Meng Z, Zhang G, Qi M, Sun Z, Liu Y, Li T (2017) Sub-high temperature and high light intensity induced irreversible inhibition on photosynthesis system of tomato plant (Solanum lycopersicum L.). Front Plant Sci 8:365 Lu Q, Zhang T, Zhang W, Su C, Yang Y, Hu D, Xu Q (2018) Alleviation of cadmium toxicity in Lemna minor by exogenous salicylic acid. Ecotoxicol Environ Saf 147:500–508 Luo WT, He L, Li F, Li JK (2020) Exogenous salicylic acid alleviates the antimony (Sb) toxicity in rice (Oryza sativa L.) seedlings. J Plant Growth Regul 40:1327–1340 Ma X, Zheng J, Zhang X, Hu Q, Qian R (2017) Salicylic acid alleviates the adverse effects of salt stress on Dianthus superbus (Caryophyllaceae) by activating photosynthesis, protecting morphological structure, and enhancing the antioxidant system. Front Plant Sci 8:600 Maeda H, Dudareva N (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol 63:73–105 Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004 Marcinska I, Czyczyło-Mysza I, Skrzypek E, Grzesiak M, Janowiak F, Filek M et  al (2013) Alleviation of osmotic stress effects by exogenous application of salicylic or abscisic acid on wheat seedlings. Int J Mol Sci 14:13171–13193 Mathobo R, Marais D, Steyn JM (2017) The effect of drought stress on yield, leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris L.). Agric Water Manag 180:118–125 Mehta S, James D, Reddy MK (2019) Omics technologies for abiotic stress tolerance in plants: current status and prospects. In: Recent Approaches in Omics for Plant Resilience to Climate Change. Springer, Cham, pp 1–34 Mehta S, Lal SK, Sahu KP, Venkatapuram AK, Kumar M, Sheri V, Varakumar P, Vishwakarma C, Yadav R, Jameel MR, Ali M, Achary VMM, Reddy MK (2020) CRISPR/Cas9-Edited Rice: A New Frontier for Sustainable Agriculture. In: New Frontiers in Stress Management for Durable Agriculture. Springer, Singapore, pp 427–458 Mehta S, Singh B, Patra A, Tripathi A, Easwaran M, Choudhary JR, Choudhary M, Aggarwal SK (2020) Maize microbiome: current insights for the sustainable agriculture. In: Microbiomes and Plant Health. Academic Press, Massachusetts, pp 267–297 Mehta S, Chakraborty A, Roy A, Singh IK, Singh A (2021) Fight Hard or Die Trying: Current Status of Lipid Signaling during Plant–Pathogen Interaction. Plants 10:1098 Mehta S, Gogna M, Singh B, Patra A, Singh IK, Singh A (2021) Silicon: a plant nutritional “non-­ entity” for mitigating abiotic stresses. In: Plant stress biology. Springer, Singapore, pp 17–49 Merret R, Carpentier MC, Favory JJ, Picart C, Descombin J, Bousquet-Antonelli C, Tillard P, Lejay L, Deragon JM, Charng YY (2017) Heat shock protein HSP101 affects the release of ribosomal protein mRNAs for recovery after heat shock. Plant Physiol 174:1216–1225 Miao Y, Luo X, Gao X, Wang W, Li B, Hou L (2020) Exogenous salicylic acid alleviates salt stress by improving leaf photosynthesis and root system architecture in cucumber seedlings. Sci Hortic 272:109577 Mishra A, Choudhuri MA (1997) Ameliorating effects of salicylic acid on lead and mercury-­ induced inhibition of germination and early seedling growth of two rice cultivars. Seed Sci Technol 25:263–270

124

Sahil et al.

Mishra A, Tripathi BD (2008) Heavy metal contamination of soil, and bioaccumulation in vegetables irrigated with treated wastewater in the tropical city of Varanasi, India. Toxicol Environ Chem 90:861–871 Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM et al (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-­ induced accumulation of reactive oxygen species in Arabidopsis. Plant J 49:79–90 Mora-Herrera ME, Lopez-Delgado H, Castillo-Morales A, Foyer CH (2005) Salicylic acid and H2O2 function by independent pathways in the induction of freezing tolerance in potato. Physiol Plant 125:430–440 Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944 Munir M, Shabbir G et al (2018) Salicylic acid mediated heat stress tolerance in selected bread wheat genotypes of Pakistan. Pak J Bot 50:2141–2146 Munns R (2007) Prophylactively parking sodium in the plant. New Phytol 176:501–504 Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-­ specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262 Mutlu S, Atıcı Ö, Nalbantoğlu B, Mete E (2016) Exogenous salicylic acid alleviates cold damage by regulating antioxidative system in two barley (Hordeum vulgare L.) cultivars. Front Life Sci 9:99–109 Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216 Noreen S, Ashraf M (2010) Modulation of salt (NaCl)-induced effects on oil composition and fatty acid profile of sunflower (Helianthus annuus L.) by exogenous application of salicylic acid. J Sci Food Agric 90:2608–2616 Noreen S, Fatima K, Athar HUR, Ahmad S, Hussain K (2017) Enhancement of physio-­biochemical parameters of wheat through exogenous application of salicylic acid under drought stress. J Anim Plant Sci 27:153–163 Ong S, Cruz FCS (2016) Effect of exogenous application of salicylic acid on the severity of tomato leaf curl disease. J ISSAAS 22:137–145 Pál M, Horváth E, Janda T, Páldi E, Szalai G (2005) Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants. Physiol Plant 125:356–364 Pan Q, Zhan J, Liu H, Zhang J, Chen J, Wen P, Huang W (2006) Salicylic acid synthesized by benzoic acid 2-hydroxylase participates in the development of thermotolerance in pea plants. Plant Sci 171:226–233 Pan G, Liu Y, Ji L, Zhang X, He J, Huang J, Qiu Z, Liu D, Sun Z, Xu T, Liu L, Wang C, Jiang L, Cheng X, Wan J (2018) Brassinosteroids mediate susceptibility to brown planthopper by integrating with the salicylic acid and jasmonic acid. J Exp Bot 69:4433–4442 Peng H, Li S, Wang L, Li Y, Li Y, Zhang C, Hou X (2013) Turnip mosaic virus induces expression of the LRR II subfamily genes and regulates the salicylic acid signaling pathway in non-­ heading Chinese cabbage. Physiol Mol Plant Pathol 82:64–72 Petersen M, Brodersen P, Næsted H, Andreasson E, Lindhart U, Johansen B, Sharma SB (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120 Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231 Prodhan MY, Munemasa S, Nahar MNEN, Nakamura Y, Murata Y (2018) Guard cell salicylic acid signaling is integrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant Physiol 178:441–450 Pushpavalli R, Zaman-Allah M, Turner NC, Baddam R, Rao MV, Vadez V (2015) Higher flower and seed number leads to higher yield under water stress conditions imposed during reproduction in chickpea. Funct Plant Biol 42:162–174

Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment

125

Radojičić A, Li X, Zhang Y (2018) Salicylic acid: a double-edged sword for programed cell death in plants. Front Plant Sci 9:1133 Rajput LS, Aggarwal SK, Mehta S, Kumar S, Nataraj V, Shivakumar M, Maheshwari HS, Yadav S, Goswami D (2021) Role of WRKY Transcription Factor Superfamily in Plant Disease Management. In: Plant Stress Biology. Springer, Singapore, pp 335–361 Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17:603–614 Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Biol 43:439–463 Raskin I, Skubatz H, Tang W, Meeuse BJ (1990) Salicylic acid levels in thermogenic and non-­ thermogenic plants. Ann Bot 66:369–373 Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050 Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338 Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu Rev Phytopathol 49:317–343 Sahil, Keshan R, Patra A, Mehta S, Abdelmotelb KF, Lavale SA, Chaudhary M, Aggarwal SK, Chattopadhyay A (2021) Expression and Regulation of Stress-Responsive Genes in Plants Under Harsh Environmental Conditions. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 25–44 Saikia R, Singh T, Kumar R, Srivastava J, Srivastava AK, Singh K, Arora DK (2003) Role of salicylic acid in systemic resistance induced by Pseudomonas fluorescens against Fusarium oxysporum f. sp. ciceri in chickpea. Microbiol Res 158:203–213 Salguero-Linares J, Coll NS (2019) Plant proteases in the control of the hypersensitive response. J Exp Bot 70:2087–2095 Sawada H, Shim IS, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis—modulation by salt stress in rice seedlings. Plant Sci 171:263–270 Scott IM, Clarke SM, Wood JE, Mur LA (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040–1049 Sekhon PS, Sangha MK (2019) Influence of different SAR elicitors on induction and expression of PR-proteins in Potato and Muskmelon against Oomycete pathogens. Indian Phytopathol 72:43–51 Shahidi F, Ambigaipalan P (2015) Phenolics and polyphenolics in foods, beverages and spices: antioxidant activity and health effects. A review. J Funct Foods 18:820–897 Shakirova FM, Allagulova CR, Maslennikova DR, Klyuchnikova EO, Avalbaev AM, Bezrukova MV (2016) Salicylic acid-induced protection against cadmium toxicity in wheat plants. Environ Exp Bot 122:19–28 Sharma P, Sharma MMM, Patra A, Vashisth M, Mehta S, Singh B, Tiwari M, Pandey V (2020) The role of key transcription factors for cold tolerance in plants. In: Transcription factors for abiotic stress tolerance in plants. Academic, London, pp 123–152 Sharma P, Sharma MMM, Malik A, Vashisth M, Singh D, Kumar R, Singh B, Patra A, Mehta S, Pandey V (2021) Rhizosphere, Rhizosphere Biology, and Rhizospheric Engineering. In: Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management. Springer, Cham, pp 577–624 Shen H, Zhao B, Xu J, Zheng X, Huang W (2016) Effects of salicylic acid and calcium chloride on heat tolerance in Rhododendron ‘Fen Zhen Zhu’. J Am Soc Hortic Sci 141:363–372 Shi Q, Zhu Z (2008) Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environ Exp Bot 63:317–326 Shin H, Min K, Arora R (2018) Exogenous salicylic acid improves freezing tolerance of spinach (Spinacia oleracea L.) leaves. Cryobiology 81:192–200 Shulaev V, Silverman P, Raskin I (1997) Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718–721

126

Sahil et al.

Sillero JC, Rojas-Molina MM, Avila CM, Rubiales D (2012) Induction of systemic acquired resistance against rust, ascochyta blight and broomrape in faba bean by exogenous application of salicylic acid and benzothiadiazole. Crop Prot 34:65–69 Singh A, Lim GH, Kachroo P (2017) Transport of chemical signals in systemic acquired resistance. J Integr Plant Biol 59:336–344 Sohag AAM, Tahjib-Ul-Arif M, Brestic M, Afrin S, Sakil MA, Hossain MT, Hossain MA (2020) Exogenous salicylic acid and hydrogen peroxide attenuate drought stress in rice. Plant Soil Environ 66:7–13 Sood N, Sohal BS, Lore JS (2013) Foliar application of benzothiadiazole and salicylic acid to combat sheath blight disease of rice. Rice Sci 20:349–355 Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100 Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA et al (2003) NPR1 modulates crosstalk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770 Sticher L, MauchMani B, Metraux JP (1997) Systemic acquired resistance. Annu Rev Plant Pathol 35:235–270 Suh JP, Jeung JU, Lee JI, Choi YH, Yea JD, Virk PS, Mackill DJ, Jena KK (2010) Identification and analysis of QTLs controlling cold tolerance at the reproductive stage and validation of effective QTLs in cold-tolerant genotypes of rice (Oryza sativa L.). Theor Appl Genet 120:985–995 Tada Y, Spoel SH, Pajerowska-Muhktar K, Mou Z, Song J et al (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956 Tamás L, Mistrík I, Alemayehu A, Zelinová V, Bočová B, Huttová J (2015) Salicylic acid alleviates cadmium-induced stress responses through the inhibition of Cd-induced auxin-mediated reactive oxygen species production in barley root tips. J Plant Physiol 173:1–8 Tao S, Sun L, Ma C, Li L, Li G, Hao L (2013) Reducing basal salicylic acid enhances Arabidopsis tolerance to lead and cadmium. Plant Soil 372(1–2):309–318 Tasgín E, Atící Ö, Nalbantoğlu B (2003) Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236 Vaca E, Behrens C, Theccanat T, Choe JY, Dean JV (2017) Mechanistic differences in the uptake of salicylic acid glucose conjugates by vacuolar membrane-enriched vesicles isolated from Arabidopsis thaliana. Plant Physiol 161:322–338 Vanacker H, Carver TLW, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol 123:1289–1300 Viswanath KK, Varakumar P, Pamuru RR, Basha SJ, Mehta S, Rao AD (2020) Plant lipoxygenases and their role in plant physiology. J Plant Biol 63:83–95 Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206 Wan SB, Tian L, Tian RR, Pan QH, Zhan JC, Wen PF et al (2009) Involvement of phospholipase D in the low temperature acclimation induced thermotolerance in grape berry. Plant Physiol Biochem 47:504–510 Wang Y, Liu JH (2012) Exogenous treatment with salicylic acid attenuates occurrence of citrus canker in susceptible navel orange (Citrus sinensis Osbeck). J Plant Physiol 169:1143–1149 Wang H, Feng T, Peng X, Yan M, Tang X (2009) Up-regulation of chloroplastic antioxidant capacity is involved in alleviation of nickel toxicity of Zea mays L. by exogenous salicylic acid. Ecotoxicol Environ Saf 72:1354–1362 Wang W, Wang X, Huang M, Cal J, Zhou Q, Dai T, Jiang D (2021) Alleviation of field low-­ temperature stress in winter wheat by exogenous application of salicylic acid. J Plant Growth Regul 40(2):811–823 Wassie M, Zhang W, Zhang Q, Ji K, Cao L, Chen L (2020) Exogenous salicylic acid ameliorates heat stress-induced damages and improves growth and photosynthetic efficiency in alfalfa (Medicago sativa L.). Ecotoxicol Environ Saf 191:110206

Salicylic Acid for Vigorous Plant Growth and Enhanced Yield Under Harsh Environment

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Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Annals of Botany. Ann Bot 111:1021–1058 Wendehenne D, Gao QM, Kachroo A, Kachroo P (2014) Free radical-mediated systemic immunity in plants. Curr Opin Plant Biol 20:127–134 White RF (1979) Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99:410–412 Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant Cell Environ 25:717–724 Yalpani N, Silverman P, Wilson TM, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3:809–818 Yokoo S, Inoue S, Suzuki N, Amakawa N, Matsui H, Nakagami H, Takahashi A, Arai R, Katou S (2018) Comparative analysis of plant isochorismate synthases reveals structural mechanisms underlying their distinct biochemical properties. Biosci Rep 38:1–13 Yu XM, Griffith M, Wiseman SB (2001) Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol 126:1232–1240 Zaid A, Mohammad F, Wani SH, Siddique KM (2019) Salicylic acid enhances nickel stress tolerance by up-regulating antioxidant defense and glyoxalase systems in mustard plants. Ecotoxicol Environ Saf 180:575–587 Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15:2636–2646 Zhang Y, Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol 50:29–36 Zhang X, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-­ lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27 Zhang Z, Lan M, Han X, Wu J, Wang-Pruski G (2019) Response of ornamental pepper to high-­ temperature stress and role of exogenous salicylic acid in mitigating high temperature. J Plant Growth Regul 39:133–146 Zhou ZS, Guo K, Elbaz AA, Yang ZM (2009) Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ Exp Bot 65:27–34

Strigolactones for Sustainable Plant Growth and Production Under Adverse Environmental Conditions Ali Raza , Rida Javed, Zainab Zahid, Rahat Sharif, Muhammad Bilal Hafeez, Muhammad Zubair Ghouri, Muhammad Umar Nawaz, and Manzer H. Siddiqui

Abbreviations ABA Abscisic acid AM Arbuscular mycorrhizal AR Adventitious root CAT Catalase A. Raza (*) Fujian Provincial Key Laboratory of Crop Molecular and Cell Biology, Fujian Agriculture and Forestry University, Fuzhou, China R. Javed Centre of Agricultural Biochemistry and Biotechnology (CABB), University of Agriculture, Faisalabad, Pakistan Z. Zahid Institute of Environmental Sciences and Engineering (IESE), School of Civil and Environmental Engineering (SCEE), National University of Sciences and Technology (NUST), Islamabad, Pakistan R. Sharif Department of Horticulture, College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, China M. B. Hafeez College of Agronomy, Northwest A&F University, Yangling, China M. Z. Ghouri Center for Advanced Studies in Agriculture and Food Security (CAS-AFS), University of Agriculture, Faisalabad, Pakistan M. U. Nawaz Department of Agronomy, University of Agriculture, Faisalabad, Pakistan M. H. Siddiqui Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi Arabia © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_6

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CCD CAROTENOID CLEAVAGE DIOXYGENASE CKs Cytokinins CL Carlactone CLA Carlactonoic acid CRISPR/Cas9 Clustered regularly interspaced palindromic repeats DMBQ 2,6-dimethoxy-p-benzoquinone DSBs Double-stranded breaks ET Ethylene FHY3 FAR-RED ELONGATED HYPOCOTYL3 GAID1 Gibberellic Acid Insisitive Dwarf 1 GR Glutathione reductase GSH Glutathione H2O2 Hydrogen peroxide HIFs Haustorium inducing factors JA Jasmonic acid KAI2 KAR-insensitive 2 KARs Karrikins LBO LATERAL BRANCHING OXIDOREDUCTASE LJ Lamina joint MeJA Methyl jasmonate N Nitrogen NAA N-acetylaspartate NADPH Nicotinamide adenine dinucleotide phosphate NPA N-1-naphthyphalmic acid P Phosphorus PAT Polar auxin transport PGRs Plant growth regulators POD Peroxidase RBOH RESPIRATOTY BURST OXIDASE HOMOLOG ROS Reactive oxygen species S Sulfates SA Salicylic acid SCF SkpCullin-F-box SLs Strigolactones SOD Superoxide dismutase TALENs Transcription activator-like effector nucleases TF Transcription factors TPL TOPLESS TPR TPL RELATED ZFNs Zinc finger nuclease

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1  Introduction Plants are immobile; they need to maintain their growth and existence under ecological constraints. Plants can support themselves in response to the changing environmental conditions by altering their anatomy, morphology, physiology, as well as molecular biology. In the past few decades, the production of the crops around the globe has been greatly affected by various biotic and abiotic stresses. When plants are subjected to any abiotic or biotic stress such as salinity, drought, temperature, nutrient deficiency, heavy metals, viruses, fungi, microorganisms, etc., they respond to it through signal transduction mechanism and regulate it at the molecular level (Raza et  al. 2019a, b, 2020; Abd-Elmabod et  al. 2020; Sharif et  al. 2020; Raza 2020). Abrupt changes in the environmental conditions may result in severe impacts on the productivity of various crop species due to the direct or indirect effects of biotic or abiotic stresses (Sharif et al. 2018; Raza et al. 2019b; Abd-Elmabod et al. 2020). Under these adverse environmental conditions, the agricultural yield of developing countries has suffered a lot in past decades, and the estimation of environmental variation and effects of climate change on agricultural yield is possible through the number of stress spells, their daily impacts on life, and extent of the farming crop damage (FAO et al. 2018; Abd-Elmabod et al. 2020). Phytohormones or plant growth regulators (PGRs) play a significant role in the regulation of stress responses. Their production has been reported in higher plants as well as in various microorganisms including cyanobacteria, bacteria, fungi, and metazoans (Tsavkelova et al. 2006; Kouzuma and Watanabe 2015; Shi et al. 2017). Optimal concentrations of PGRs are essential for the growth and expansion of plants and once synthesized they either remain at the site of synthesis or are transported to different plant organs. The elaborated signaling networks can be generated via SLs themselves or through interaction with other hormones. These interactions leading to cross talk between hormones is crucial in maintaining the growth and development of plants and for the regulation of tissue differentiation (Wang and Irving 2011; Brewer et al. 2015; Visentin et al. 2016; Sharif et al. 2018; Jing et al. 2020; Bakshi et al. 2019). The mode of action or behavior of plants is determined by PGRs and numerous other signaling molecules such as Ca++ and ROS which help plants to adapt to the hostile environment (Wang and Irving 2011; Nazir et al. 2020; Bakshi et al. 2019; De-la-Peña et al. 2017). Traditionally, the classification of plant hormones has been done as growth promoters and growth inhibitors. Cytokinins (CKs), gibberellins/gibberellic acid (GA), and auxins have been classified as growth promotors, while abscisic acid (ABA) and ethylene (ET) as growth inhibitors (Raza et al. 2019a; Muhammad et al. 2019; Jing et al. 2020). Under the stress conditions, the role of various plant hormones has been demonstrated, including SLs, CKs, ET, GA, ABA, jasmonic acid (JA), and salicylic acid (SA) (Bari and Jones 2009; Santner et al. 2009; Muhammad et al. 2019; Raza et al. 2019a; Jing et al. 2020; Mubarik et al. 2021). In a quest to find plant metabolites that work as phytohormones, SL, a compound derived from carotenoids, has proved to be an emerging candidate (Hossain et al.

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2021). For their exudation, 80% roots of land plants were used, and they are involved with the soil arbuscular mycorrhiza (AM) in a symbiotic relationship (Jia et  al. 2018; Zwanenburg and Blanco-Ania 2018; Cooper et al. 2018). The overall structure of plants, such as structures of plants presents above and below the soil, is controlled by phytohormones of this class (Ruyter-Spira et al. 2011). In genera such as Phelipanche, Striga, Orobanche, and Alectra, seed germination was induced in parasitic root plants (Yoneyama et  al. 2013), and they are dependent on the host because these plants are not able to do photosynthetic assimilations. Although they have some impacts on natural vegetation, they are also involved in agricultural losses due to their activities in lands of agriculture (Parker 2009). Hormones of this class were named after the first candidate who was identified from Striga, hence called strigolactone (Cook et al. 1966). A number of experiments reported that shoot branching was suppressed by SLs (Gomez-Roldan et al. 2008; Umehara et al. 2008; Rasmussen et al. 2012; Shinohara et al. 2013). SLs play a role in molecular cue due to which the communication of plants with their environment becomes possible (Andreo-Jimenez et al. 2015; Mostofa et al. 2018). From recent work, it was reported that regulation of various molecular and physiological processes was carried out by SLs while adapting the abiotic stresses (Andreo-Jimenez et al. 2015; Saeed et al. 2017; Siddiqi and Husen 2017; Banerjee and Roychoudhury 2018; Haider et al. 2018; Luo et al. 2018; Mostofa et al. 2018; Ling et al. 2020). SLs play a positive role in managing the reply of plants to salt and drought stresses through max2 (Van Ha et al. 2014; Wang et al. 2019b; Li and Tran 2015). Different views of SLs have been suggested after prime investigation, such as symbiotic promoter or growth stimulant. SLs also served as a tool related to stress, which is an important role and documented in abiotic and biotic stress. Figure 1 illustrates the possible application of SLs in agriculture. Therefore, in this chapter, we have summarized the biosynthesis, metabolism, and beneficial role of SLs in response to a variety of environmental factors. Further, SLs cross talk has also been illustrated, indicating the importance and interaction of SLs with other PGRs to mitigate the adverse effect of environmental stresses on crop plants.

2  Biosynthesis and Metabolism of SLs Strigolactones belong to a class of compounds which are derived from the carotenoids. Several enzymes located in cytosol and plastid react over the carotenoid and generate SLs in the form of apocarotenoid compounds (Matusova et  al. 2005; Cooper et al. 2018). There are also several other players involved in the biosynthesis of SLs in plants. For instance, the initiation of the isomerization process is carried by β-carotene, which is localized in the plastids. The β-carotene in rice and Arabidopsis is controlled by D27 and AtD27, respectively (Mostofa et  al. 2018). After that, the conversion of β-carotene to carlactone (CL) is regulated by the action of CCD7 and CCD8 (D17 and D10 in rice and max3 and max4 in Arabidopsis), respectively (Alder et  al. 2012) and CL plays a crucial role in the production of

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Fig. 1  Schematic overview of the possible application of SLs in agriculture. Solid lines are indicating the beneficial effect, while dash lines are indicating the possible realization (positive or negative). Adapted from Aliche et al. (2020)

different SLs (Seto et  al. 2014). The cytochrome P450 enzyme, namely max1 in Arabidopsis and CL oxidase (Os01g0700900) and orobanchol synthase (Os01g0701400) in rice further oxidize these CLs compounds into orobanchol (Zhang et al. 2014). Additionally, in Arabidopsis, the CL compound transforms into carlactonoic acid (CLA) through the support of max1 gene, which functions as a CL oxidase (Abe et al. 2014). The CLA is methylated by an unidentified methyl transferase before transforming into an SLs-like compound by the action of LATERAL BRANCHING OXIDOREDUCTASE (LBO) (Brewer et  al. 2016; Mostofa et  al. 2018). The SLs biosynthesis pathway has been illustrated in Fig. 2. The D53 from the rice was identified in an SL-insensitive mutant as the first SL repressor. The mutant displayed a semi-dwarf phenotype and a significantly higher number of tillers due to the suppression activity of D53 (Zhou et  al. 2013). The OsD53 gain of function transgenic plants showed a phenotypic resemblance to the d53 mutant, which confers the role of D53 in influencing the plant phenotype (Zhou et al. 2013). Additionally, the SMXL6, SMXL7, and SMXL8, the three orthologous of D53, also suppressed the SL signaling in Arabidopsis (Soundappan et al. 2015; Wang et al. 2015). Initially, it was proposed that all three orthologous genes of D53 work redundantly; however similar phenotypic characteristics to that of D53 were only observed in the triple mutant smxl6/7/8 (Soundappan et al. 2015; Wang et al. 2015). Therefore, and it is still unknown if these three genes function similarly. The SLs molecule facilitated the interaction of SMXL6, SMXL7, and SMXL8 with the receptor D14. Since these orthologs are localized in the nucleus, they could

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Fig. 2  The depiction of the SLs biosynthesis pathway proposed that the β-carotene isomerized by the action of D27/AtD27 in rice and Arabidopsis, respectively. This β-carotene further converts into Carlactone (CL) with the help of CCD8 gene. In the case of rice, the conversion of CL by CL oxidase (Os01g0700900) and Orobanchol synthase (Os01g0701400) into SL like compounds. In Arabidopsis, the simultaneous action of LBO gene with cytochrome P450 max1 and an unknown enzyme transforms CL into CLA before converting it into SLs like compounds

be an important transcriptional regulator of various processes (Zhou et  al. 2013; Soundappan et al. 2015; Wang et al. 2015). In addition to that, the SL has also been reported to influence the degradation of D53, SMXL6, and SMXL7 by inducing the proteasome activity (Zhou et al. 2013; Soundappan et al. 2015; Wang et al. 2015). However, in d3, d14, and d53 mutants, the degradation of D53 was not observed which confirmed that the presence of D3-D14-D53 is crucial for the degradation of D53 (Wang et  al. 2015). Moreover, the suppressor genes, namely, D53, SMXL6, SMXL7, and SMXL8, interact with another corepressor gene TOPLESS (TPL) and TPL RELATED (TPR) (Jiang et al. 2013; Zhou et al. 2013; Soundappan et al. 2015; Wang et al. 2015; Song et al. 2017). More recently, the RNA sequencing has revealed that the SLs regulate various biological processes such as shoot branching, leaf shape, and anthocyanin accumulation by activating the transcription of BRANCHED 1, TCP DOMAIN PROTEIN 1 and production of anthocyanin pigment 1 genes (Wang et al. 2020). Additionally,

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the SMXL6 transgenic plants targeted 729 different genes, which further repressed the SMXL6, SMXL7, and SMXL8 transcription by binding to the promoter region. This shows that SMXL6 is important for the autoregulation of transcription factors (TF), which later maintained the homeostasis SLs signaling pathway (Wang et al. 2020).

3  P  lant Developmental Responses to Environmental Stresses: A SLs Perspective The application of plant hormones to tackle environmental constraint has been used for decades. The discovery of SLs opened further avenues for research to investigate the response of these biomolecules under stressed conditions (Rasmussen et  al. 2017; Yang et al. 2019). Notably, SLs cooperate with other hormones to modulate plant growth and development at various stages (Fig. 3). Below we discussed the

Fig. 3  Potential role of SLs in plant growth and development. Notably, SLs cooperate with other hormones to modulate plant growth and development at various stages. Red arrows are indicating positive effects/regulation, and green arrows are indicating negative/inhibitory effects/regulation. Abbreviations are explained in the text. Adapted from Yang et al. (2019)

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differential role of SLs in the morphological and physiological development of plants and its production in roots.

3.1  Morphological and Physiological Responses The SLs play a major role in various growth and developmental activities by influencing the morphology and physiology of the plants. They control the plant architecture via transport of different substrates from roots to aerial parts of the plants (Al-Babili and Bouwmeester 2015; Ling et  al. 2020), and therefore their role in roots development has been of particular interest. For example, short primary roots and dense lateral roots were observed in the Arabidopsis SL-insensitive and SL-deficient mutants (Kapulnik et al. 2011; Ruyter-­ Spira et al. 2011). Besides that, the SLs application also positively influenced the root hair in Arabidopsis (Kapulnik et al. 2011) and stimulated the crown root in rice (Arite et al. 2012). On contrary to the above-cited examples, SLs have been found to restrict adventitious root (AR) formation in several plants such as tomato (Rasmussen et al. 2013) and pea (Urquhart et al. 2015). Additionally, the application of GR24, an analog of SL, enhanced the rooting activities by inducing the transcription of root related genes (Ma et al. 2017). The GR24 suppressed the negative effects of salinity stress by regulating the antioxidant enzyme activities (Ma et al. 2017). The rice plants, when subjected to NaCl stress, displayed compromised root length by up to 40% in comparison to non-stressed plants. When added to the Hoagland solution, it resulted in the better root length by restoring the antioxidant enzyme indices in roots and also increased resistant to NaCl stress (Ling et al. 2020). The effects of SLs on shoots have been reported in numerous studies in a variety of different plants. In rice, the crippled biosynthesis of SLs led to the dwarf phenotype in the SL-deficient mutant (d17) (Zou et al. 2019) which was recovered by the exogenous application of GA over the d17 mutant. This suggests the crucial role of SL in the elongation of shoots by modulating the GA activities in rice plants (Zou et  al. 2019). The rapeseed seedlings were subjected to salinity stress (Ma et  al. 2017), and with the application of GR24, the seedling not only showed high resistance to salinity but also improved the shoot growth through the upregulation of different genes (Ma et al. 2017). Similarly, the rice seedlings were also rescued by the application of GR24 under NaCl stress. The application of GR24 triggered the rice seedlings’ shoots photosynthetic activities by many folds (Ling et  al. 2020). Literature showed that salinity stress often increases the generation of reactive oxygen species (ROS). A similar case was observed in Salvia nemorosa. Salvia is an essential medicinal herb; however, due to the continuous climate changes, its production has been hampered. The application of SL at the rate of 0.3 μM to the salt-­ stressed Salvia plants significantly increased the production of essential oil (0.4 g plant−1) in comparison to that of non-treated plants. These beneficial changes could be because of abundant proline accumulation in the leaves of Salvia (Sharifi and Bidabadi 2020). The plant miRNA has been documented extensively for their

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role in growth and stress responses (Khraiwesh et  al. 2012; Barciszewska-Pacak et al. 2015). The relationship between SL and miRNA has been studied recently in the tomato plant (Visentin et al. 2020). The study unfolded that the exogenous foliar application of SLs enhanced the miRNA156 accumulation in leaves, which further controls the stomata opening under prolonged drought stress (Visentin et al. 2020). The study provided important clues for future research regarding the simultaneous role of miRNA and SL in mitigating drought stress (Visentin et al. 2020). In another study, the increased level of endogenous SL suppressed the lamina joint (LJ). LJ is an important morphological trait and crucial for delaying leaf senescence and maintaining plant architecture. The study was confirmed in both SLs mutant and WT plants. The SLs rice mutant plants displayed larger LJ in comparison to the WT, whereas the exogenous application of GR24 significantly restricted the growth of LJ. Additionally, endogenous SL level increases under N deficiency, which also hampered the growth of LJ.  It is indicating that the growth of LJ is responding negatively to the augmented level of endogenous SL (Shindo et  al. 2020). These lines of evidence indicating that SLs could be used for not only increasing the plant physiological and morphological parameters but also for boosting resistance against multiple environmental stresses.

3.2  R  oot Development in Response to Environmental Conditions Strigolactones have been generally documented for their role in root development with or without stress conditions (Fig. 3). For example, the application rac-GR24 over Arabidopsis grown in phosphate sufficient conditions were studied. The study revealed that the rac-GR24 significantly increased the primary root length by regulating the expression of max2 gene (Jain et al. 2007). However, contrasting results were observed when rac-GR24 was applied in high concentration (2.5  μM or above), possibly due to the excessive accumulation of GR24  in roots (Jain et  al. 2007). Similarly, the addition of rac-GR24 to SL biosynthetic mutants (max4, max1) under limited carbon conditions displayed longer primary roots in comparison to that of untreated plants (Ruyter-Spira et al. 2011). The effects of SLs on lateral roots are more pronounced than the primary roots. For instance, the max2, max3, and max4 mutants exhibited more number of lateral roots than the wild type under depleted phosphorus (P) conditions (Claassens and Hills 2018). However, the application of rac-GR24 arrested the growth of lateral roots in all the three mutant lines (Claassens and Hills 2018). This clearly shows that SLs negatively regulate the formation of the lateral roots in plants. The generation of a higher number of AR in mutants deficient in SLs biosynthesis also highlighted the negative role of SLs in AR formation (Rasmussen et al. 2012). The study was confirmed by applying the exogenous rac-GR24 to SLs deficient mutants. The rac-GR24 significantly suppressed the AR formation in mutant lines. As it is known that, AR provides support

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to the plant, particularly under deprived nutrient conditions or waterlogging stress (Claassens and Hills 2018; Guan et al. 2019). The other abiotic stresses, such as drought and salinity, also negatively influence the SL biosynthesis in roots of the plants (Ruiz-Lozano et al. 2016). Such as the PEG mediated drought stress significantly suppressed the expression of SL biosynthetic genes that including LjD27, LjCCD7, and LjCCD8, and LjPDR1 in Japonicus (Liu et  al. 2015). It can be assumed that the downregulation of SL biosynthesis genes suppressed the production of SL in roots, which may affect the root architecture partially (Liu et  al. 2015). Similar results were also observed in the tomato plants where the drought stress negatively affected the expression of SL biosynthesis genes SlCCD7 in the root tissue (Ruiz-Lozano et al. 2016). However, contrasting results were recorded in rice roots under water stress conditions (Haider et al. 2018). Therefore, it can be speculated that the roots of monocot and dicot plants respond differently in the context of SL production under stressful conditions. These differences in SL production also define the fate of root development in different plant species under various environmental stresses. The ABA biosynthetic genes are known for their role in regulating numerous plant developmental activities and also providing timely response to the majority of abiotic stresses (Van Ha et al. 2014; Sah et al. 2016; Visentin et al. 2020). Exogenous application of zaxinone enhanced the transcriptional level of SL and ABA biosynthesis genes in the root tissue of Arabidopsis seedlings (Ablazov et al. 2020). Meanwhile, the zaxinone worked as an SL repressor and thus improved the root formation subsequently (Ablazov et al. 2020). This leads us to assume that zaxinone and SL could work oppositely in different plants under different conditions. Because of its ability to significantly upregulating the expression ABA and SL biosynthetic genes (Ablazov et al. 2020), the role of zaxinone under abiotic stresses is still an open question to address. On the other hand, the exogenous application of zaxinone suppressed the SL activity while promoting the root growth (Wang et al. 2019a). The results were confirmed in the zaxinone loss of function mutant (zas), where the exogenous treatment rescued the plummeted the root growth activity in zas mutant and also enhanced the combating capacity against Striga (Wang et al. 2019a).

3.3  S  hoot Development in Response to Environmental Conditions Important abiotic stresses such as salinity and drought have been the concern of the plant science community as it impairs the growth and productivity of crops. In line with that, the SL-deficient mutant showed increased sensitivity to drought and salinity stress (Van Ha et al. 2014). A significant number of SL-deficient Arabidopsis plants were unable to resist the drought and salinity stress. The phenotypic changes caused by the stresses were observed in shoots rather than roots (Van Ha et  al.

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2014). However, the application of exogenous SLs induced the resistance in SL-deficient mutant plants against the drought and salinity stress. Additionally, the stress affected phenotype was also rescued post the exogenous treatment of SLs (Van Ha et al. 2014). The P status in soil has been reported for its crucial role in maintaining the normal plant architecture. The rice SL-biosynthetic and signaling mutants (d10, d3) displayed inhibited shoot branching phenotype in the presence of P (Umehara et al. 2008, 2010). However, contrasting results were in the absence of P (Umehara et al. 2008, 2010). Similar findings were obtained in the Arabidopsis under P-deficient conditions (Kohlen et al. 2011). Additionally, the expression pattern of PDR1 gene (SL transporter gene) induced significantly in the roots, which triggered the SL accumulation in the xylem of Arabidopsis plants when grown in P-deficient conditions (Kohlen et al. 2011). This suggested that SL move from roots to shoots in a P-dependent manner (Kohlen et al. 2011). It can also be speculated that this P-dependent movement of SL from root to shoot could also alleviate the P-deficiency effects on plant shoots. Moreover, SL cross talk with other phytohormones to regulate the plant architecture, particularly under environmental stresses, is also of great significance importance. For instance, the auxin has been recognized for its involvement in the SL homeostasis. Auxin is a major player in developing the shoot architecture, whereas it also provides resistance to various environmental stresses (Sharma et al. 2015; Pandey et al. 2019). Auxin is vital for shoot branching and breaking auxiliary bud dormancy. Auxin also modulates the expression of SL related genes (Felemban et al. 2019). In Arabidopsis, the SL arrests the polar auxin transport (PAT), which ultimately inhibits the growth or the generation of shoot branching. This compromised PAT activity is because of the SL mediated downregulation of the PIN1 gene (a major auxin transporter gene) (Felemban et al. 2019). PAT, on the other hand, is extremely essential for the sustainable growth of auxiliary bud in Arabidopsis and Pea (Barbier et al. 2019). The induced expression level of auxin biosynthesis genes and transporter could be helpful in the homeostasis of SL during the development of shoot branching under stressful environments. The interaction of SL with sucrose could be of great interest, as sucrose regulates the bud outgrowth by increasing the accumulation of CKs in stem (Barbier et al. 2019). However, according to the best of our knowledge, no such study is available so far. More recently, the rice SL-deficient mutant was reported for increased LJ size under the nitrogen abundance conditions. The LJ also reported regulating shoot branching, as the larger LJ resulted in a higher number of shoot branching. On the contrary, the absence of N suppressed the LJ size by triggering the level of endogenous level, which in return increased plant height with less number of shoots branching (Shindo et al. 2020). Therefore, it can assume the endogenous level negatively regulates that generation of shoot branching.

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4  Role of SLs in the Stressful Environment: Recent Progress Recently, several experiments have verified the numerous roles of SLs in the adaptation and modulation of the plant responses to different biotic and abiotic stresses (Van Ha et  al. 2014; Djennane et  al. 2014; Marzec and Muszynska 2015; Ruiz-­ Lozano et al. 2016; Trabelsi et al. 2017; Cooper et al. 2018; Song et al. 2020; Ling et al. 2020). The discovery of SLs furnished new scenarios during the past decade to discover hormonal modulation of plant developmental processes and adaptation to several environmental cues. These experimental efforts also recognized new examples of hormonal cross talk, contributing to the understanding of general responses in crop plants under stressful environments. In this section, we have explained the possible role of SLs under stress conditions in crop plants.

4.1  Drought and Salinity Among several environmental stresses, drought and salinity have severely impacted the crop productivity globally (Raza et al. 2019a, b, 2020; Abd-Elmabod et al. 2020; Wasaya et al. 2021; Saddiq et al. 2021). Many studies have demonstrated the negative impact of stresses like salinity and drought on the SLs production. Under both conditions, this reduction is dependent on the severity of stress (Aroca et al. 2013; Ruiz-Lozano et al. 2016; Ma et al. 2017). On the other hand, plants have adopted different mechanisms, including hormone production, to improve the tolerance against such stresses and alleviate the plant damage (Ling et al. 2020). The results of germination bioassay showed low germination stimulatory activity of NaCl treated plant extracts suggesting a reduction in SL synthesis in lettuce in response to the saline conditions (Aroca et al. 2013). Later on, it was found that SLs biosynthesis under drought was steadily reduced in non-arbuscular mycorrhizal (AM) lettuce as well as in tomato. At the same time, the effect was more pronounced in tomato plants. These findings corroborated with the quantification of SLs biosynthesis genes (SlCCD7) via qRT-PCR, which appeared to be downregulated in non-AM plant roots under drought conditions (Ruiz-Lozano et al. 2016). SL has been reported to support various physiological processes occurring in plants. Foliar application of a synthesized SL, rac-GR24, on grapevine seedlings increased the drought tolerance by improving resistance against the drought-induced decrease of relative water content, activation of the antioxidant defense system, regulation of stomatal closure, rate of photosynthesis, and low electrolyte leakage (Min et al. 2019). Similarly, the salinity is known to impact the roots and shoots of rapeseed, an important edible oil crop, by inhibiting its growth and production. Ma et al. (2017) found an improvement in growth parameters of rapeseed along with the reduction in the salinity stress in response to SL application. It partially alleviated the salinity induced negative impacts on leaf chlorophyll content and other gas

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exchange parameters, including intercellular CO2 concentration and rate of transpiration. Literature suggests that under mild drought conditions, the stomata do not close, but during severe drought conditions, being mediated by a rise in ABA levels and decrease in the SL production, the water loss is prevented by stomatal closure. The data obtained from the analysis of rice corroborate with these findings and implied that compared to 10-fold induction of SL under mild drought conditions, the longer periods of severe drought caused only a 2–3 fold increase in the production of SL. Additionally, a decline in expression of SL biosynthesis genes was also observed to allow the ABA accumulation in rice shoots (Haider et al. 2018). Moreover, the exogenous application of SL led to an accumulation of a novel SL-miR156 module in tomato leaves, which started after a short period of drought treatment and continued till 24  h. Findings suggest that the SL-miR156 module plays a vital role in increasing sensitivity to ABA by setting a basal sensitivity; however, the endogenous production of SL is required for its induction of this module under stress. Data showed the role of SLs in playing a mediating role in preventing the stomatal re-­ opening after re-watering and acting as a molecular link between drought and miR156 in tomato (Visentin et al. 2020). The SLs influenced the Arabidopsis in ABA-mediated stomal closure to prevent rapid water loss in the max mutants, subjected to dehydration. Under high salinity and presence of ABA, the SL-biosynthesis genes, including max3 and max4, were also upregulated, which triggered activation of SL biosynthesis, leading towards SL signaling (Van Ha et al. 2014). In contrast, the osmotic stress decreased the concentration of SL in the roots of Lotus japonicus independent of the phosphate abundance. This decrease was due to the downregulation of SL biosynthesis genes LjD27, LjCCD7, and LjCCD8 during the early phase of osmotic stress. It was necessary for the adaptive adjustment Lotus japonicus to allow the ABA production (Liu et al. 2015). Implying to the role of SLs in helping plants acclimatize against the drought and salinity stress, max3 and max4 (SL biosynthetic) along with max2 (SL responsive) mutants were reported to be more drought susceptible than wild-­ type plants. Zhang et al. (2018b) supported this argument that Arabidopsis max1 (SL-biosynthetic) mutants exhibit a water deficit hypersensitive response. The effects of SL were concentration-dependent and directly impacted various parameters, including stomatal conductance, intercellular CO2 concentration, the net rate of photosynthesis, and transpiration. Application of GR24 protected the rice seedlings against salt stress, improved growth, and stimulated the enzymatic activity of peroxidase (POD), and superoxide dismutase (SOD). Thus, the optimal dose application of GR24 protected rice seedlings from any oxidative damage and improved the yield by providing better conditions for rice adaptation under saline conditions (Ling et al. 2020). In apple, the improved plant tolerance to drought and salinity was observed as a result of the overexpression of the SL receptor gene, MdD14, which improved the plant’s tolerance to drought and salinity, indicating its active role in stress resistance. Additionally, the verification of MdD14 transcript levels in different plant organs through RT-qPCR analysis demonstrated that in comparison to shoots, the gene was highly expressed in roots since they are organs

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for SLs synthesis. It also increased the uptake of inorganic nutrients in plants resulting in expanded growth of lateral roots and root hairs (Yang et al. 2020). The symbiotic relationship of the plants with AM in soil resulted in high SL production under salinity stressed condition. This increase was also in coherence with the transcriptional activity and resulted in the upregulation of the SL biosynthesis gene SlCCD7 (Aroca et al. 2013; López-Ráez 2016). Analysis of the wild-­ type Solanum Lycopersicum shoots with less SL supply from roots appeared to be under mild stress and had more stomatal hyposensitivity to ABA. Reduced production of SL under water-stressed conditions in roots further added to the hypersensitivity of stressed tomatoes (Visentin et al. 2016). In comparison to the above-cited studies, the drought response and seedling development were investigated, and it was reported that the Arabidopsis seedlings of the max2 mutant showed hypersensitivity to drought and salinity. The detached leaf water loss analysis of different mutants also resulted in a rapid water loss in max2 compared with other types. It supported the argument that drought response is specific to max2 mutant and is sensitive to the SL levels rather than SL biosynthetic pathway controlled by max1, max3, and max4 (Bu et al. 2014). One of the pharmacologically important herbs is Salvia, whose production might be constrained under salt stress. In line with that, Sharifi and Bidabadi (2020) demonstrated a reaction of the plant to salinity when treated S. nemorosa with five levels of SLs (0, 0.1, 0.2, 0.3, 0.4 μM), and four levels of salinity (0, 100, 200, 300 mM NaCl) in the greenhouse. There was a reduction in plant growth due to salinity, while the SLs treated plants prevented or restored the salt stress-induced loss of growth. Besides, it has been reported that due to increased salinity, leaf chlorophyll content significantly reduced. Salvia plants with salt stress, together with the SL levels, displayed a significant decrease in POD, SOD, catalase (CAT), and glutathione reductase (GR) activities. Moreover, SL levels up to 0.3 μM overall resulted in low total phenol content and reduced glutathione (GSH) compare with the control plant exposed to salt stress only. The essential oil yield was high (0.4 g plant−1) upon 100 mM of NaCl and 0.3 μM of SL treatment (Sharifi and Bidabadi 2020). Effects of SL treatment in reducing stress conditions of salinity could be attributed to more proline (non-enzymatic antioxidant) accumulation and decreased antioxidant enzymes, which are vital in improving salt tolerance of Salvia plants (Sharifi and Bidabadi 2020).

4.2  Temperature Plant growth and development depends upon surrounding temperature, and each plant species has a specific range of working temperature, i.e., minimum, maximum, and optimum. The temperature has emerged as a critical regulator, and a plant requires a set of optimum conditions to perform specific biological and physiological activities. Thus, slight fluctuations in temperature may bring plants under stress (Pandey et  al. 2016; Raza et  al. 2019b, 2020, 2021; Sharif et  al. 2020; He et  al.

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2021). Seed germination and optimum temperature conditions are allied in a way that, in high temperature, a seed may fail to germinate (Basbouss-Serhal et al. 2016). The key feature in the seed germination is the expression of plant hormones, such as CKs and GA favors seed germination (Pandey et al. 2016). In contrast, ABA might negatively regulate seed germination (Shuai et al. 2017). SLs have been observed to be effective in seed germination (Lechat et al. 2015). SLs maintain the balance of plant hormones by lowered ABA and increased CK levels, thereby facilitating the seed germination process. Tsuchiya et al. (2010) reported stimulation in the germination of SL defective Arabidopsis mutant plants upon application of GR24 under high temperature. Besides, the GR24 application resulted in a reduction of ABA to GA levels and a slight increase in CK levels. Seed dormancy requires a minimum period of 4 days, followed by stimulation from the host stimulants like SLs in Phelipanche ramose. The germination of the seed is stimulated by the activation of the ABA catabolic gene (PrCYP707A1). Molecular mechanisms regarding conditioning period, i.e., silencing, expression, regulation of germination stimulant response of PrCYP707A1, are still unknown. Lechat et al. (2015) described seed response to SLs, which is controlled by ABA-­ independent DNA methylation in obligate root parasitic plant, Philipanche ramose. They used to investigate modulation and the possible role of DNA methylation in the conditioning period and in PrCYP707A1 response to GR24. They demonstrated that there exists an active DNA demethylation during 4 days conditioning period, and it is also required for activation of PrCYP707A1 by GR24 and seed germination. They concluded that DNA methylation plays a vital role during conditioning period independent of ABA in regulating seed germination by controlling GR24 based PrCYP707A1 expression. In a combined study, Djennane et al. (2014) demonstrated the impact of light and temperature on bud burst along stem and interactions with molecular mechanisms in the control of bud burst in rose cultivars. They reported repression of acrotony when exposed to the cold temperature of 5  °C.  Also, they sequenced MAX-­ homologous SL pathway genes to study their expression in buds and internodes. Results demonstrated that the darkening of the distal part of the shoot is triggered by a substantial increase in RwMAX2 expression in buds and bark phloem samples. In contrast, expression of the RwMAX1 acropetal gradient has been suppressed in stems exposed to light. Overall, cold treatment induces acropetal expression of RwMAX1 in internodes and RwMAX2 in buds of stems (Djennane et al. 2014). Recently, Basbouss-Serhal et al. (2016) investigated changes in the germination potential of Arabidopsis seeds stored in combinations of various temperatures (10, 15, 20, and 25 °C) and relative humidity (1–85%) for 63 weeks of storage. Primary dormant seeds did not germinate in darkness at 25 °C; however, they acquired the potential to germinate within 7 weeks with a relative humidity of 50% in all temperatures. It is concluded that break in primary dormancy and induction of secondary dormancy is somewhat associated with the induction and repression of specific genes which are involved in ABA, GA biosynthesis and signaling pathways. Moreover, high humidity progressively favors loss of viability of seeds and induces seed aging.

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Imbibition of seed is an important feature that integrates certain environmental and endogenous signals to break seed dormancy and initiate seed germination. FUS3 (a B3-domain transcription factor) is a novel and master regulator for the seed maturation process uncovered by Chiu et al. (2016a, b); Wang and Perry (2013). FUS3 is characterized as responsible for delaying in seed germination. Chiu et al. (2016a, b) reported the role of FUS3 at a supra-optimal temperature in seed delaying seed germination. At high temperature in imbibed seed, the FUS3 promoter is reactivated and started synthesizing FUS3 mRNA, followed by protein synthesis. Moreover, genetic analysis has shown that it contributed to delay germination at high temperatures. In contrast to wild type, overexpression of FUS3 during imbibition, the seed becomes more sensitive to high temperature and may not germinate. Furthermore, transcriptome analysis revealed that wild-type seeds imbibed at high temperature might activate many seed-specific genes, ABA biosynthesis genes, and signaling genes, whereas inhibiting germination and growth responsive genes. On the other hand, Cooper et al. (2018) highlighted the role of SLs as a positive regulator of chilling tolerance in Pisum sativum and Arabidopsis. The mutants with defective SLs signaling were used for experimentation. In addition, a greater number of branches were observed in the shoot of pea mutants (rms3, rms4, and rms5) along with elevated chlorophyll content a/b ratio and carotenoid content compared to wild type. However, when exposed to dark, chilling condition, the observed number of leaves were increased in all the lines, whereas a significant decrease in fresh shoot weight was observed. In contrast to wild-type plants, chilling temperature inhibits photosynthetic carbon assimilation in P. sativum mutant lines and even in Arabidopsis (max3-9, max4-1, and max2-1) mutants with defective SL signaling. Moreover, max mutants accumulated less biomass than the wild type. GR24 application resulted in decreased leaf area in wild type, max3-9, and max4-1, while it was not observed in max2-1 (Cooper et al. 2018). SLs has a pivotal role in the regulation of root development already discussed in previous sections. However, there is a greater confusion regarding its impact on root elongation under different temperatures in perennial grass species. Therefore, Hu et al. (2018) explained it in a fascinating aspect. Such as the effects of SL on root elongation and examining combined effects SL and auxin in the development of root elongation under both stress (heat 30–35 °C) and non-stress conditions. They used to treat tall fescue plants with GR24, N-acetylaspartate (NAA), or N-1-­ naphthyphalmic acid (NPA, auxin transport inhibitor) or their combination under heat stress of 30–35 °C and non-stress conditions. Crown root elongation has been observed under normal and heat stress due to SL.  In addition, GR24 application positively enhance root elongation, thereby increasing cell number, upregulation of cell cycle relevant genes and downregulation of auxin transport pertinent genes of tall fescue. They also concluded that SL has a positive impact on the development of crown root elongation in different temperatures, and this might be due to the regulation of cell division and interference in auxin transport genes expression.

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4.3  Reactive Oxygen Species Reactive oxygen species (ROS) are popularly known as signal transducers and play a significant role in plant development and growth. The cell compartments of plants produce ROS during photosynthesis, photorespiration. The plants also produce them in response to certain biotic and abiotic stimuli and during programmed cell death (Xia et al. 2015; Choudhury et al. 2017; Raja et al. 2017). Nicotinamide adenine dinucleotide phosphate (NADPH)-oxidase and apo-plastic peroxidases are sources of ROS production in these stress conditions (Sagi and Fluhr 2006; Bettini et al. 2008; Xia et al. 2015). Thus, ROS act as a signal molecule to modulate gene expression, which helps to overcome these stresses. Plant hormones mainly regulate the production of ROS through NADPH oxidase encoded by RESPIRATOTY BURST OXIDASE HOMOLOG (RBOH) to cope up with plant development and stresses (Sagi and Fluhr 2006; Marino et al. 2012). Strigolactones signaling mechanisms have a secure link with ROS production indirectly, and this link came from a finding that FAR-RED ELONGATED HYPOCOTYL3 (FHY3) is a negative regulator of RBOH genes. FHY3 is a prime component in phytochrome A and the circadian clock, involved in far-red light responses; suppresses root and shoot branching in Arabidopsis Fhy3max2 double mutants (Lin et al. 2007). FHY3 has been characterized as a suppressor of MAX2 as it has shown in a study that its activation leads to increased expression of RBOH, which might suppress branching (Ouyang et al. 2011). Koltai et al. (2011) described that the loss-of-function of FHY3 gives rise to the enhanced look of the RBOH gene, which is accountable for the suppression of shoot splitting. However, RBOH has been revealed to modulate branching in Solanum lycopersicum plants, whereas the expression of RBOH enhanced the shoot branching. Additionally, RBOH has been marked to favor shoot branching, while RBOH antisense expression leads to increased shoot branching in L. esculentum. In a recent study, Xia et  al. (2015) uncovered another link between ROS and SLs in drought and salt stress. Increased sensitivity has shown by max2 mutant plants against these stresses with impaired ABA levels, stomata closure, and expression of stress-responsive genes. SL production is also influenced in response to nutrient depletion, which resulted in increased lateral roots formation. Similar to SLs, nutrient depletion also triggers enhanced ROS production. Nutrient starvation between plant and AM fungi has been studied well by Bonneau et al. (2013). Symbiosis process in AM is greatly stimulated by limiting P, which contributes to P and nitrogen (N) procurement. At the same time, it is still unknown what happens in combined P and N nutrient limitation. Therefore, to investigate this, Bonneau et al. (2013) cultivated Medicago truncatula plants in limited P concentration, limited N concentration or combined N and P conditions compared to control plants with sufficient P and N concentration in presence and absence of Rhizophagus irregularis. It is indicated that AM formation was observed higher in combined limitation of P and N levels, which is linked to activation of systematic signaling by plant nutrient status. Moreover, transcriptome analysis of these plants

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revealed that plants with combined limited P and N levels stimulate NADPH oxidases in roots, which ultimately activated certain plant defense genes and signaling pathways, including SLs. It has been suggested that low P and N levels in plants stimulate a physiological state of plants, which is favorable for AM symbiosis (Bonneau et al. 2013). Striga hermonthica is a parasitic weed responsible for causing damage in sub-­ Saharan Africa; however, its mechanism of action or parasitism is still unknown. A haustorium is a special type of organ that can be used by these parasites to obtain nutrients and water often by host-derived haustorium inducing factors (HIFs). So far, the most active HIF factor reported to date is 2,6-dimethoxy-p-benzoquinone (DMBQ), isolated from sorghum root extracts. DMBQ is reported to be produced by oxidation of its precursor syringic acid, and ROS and peroxidases are involved in this process. ROS roles in haustorium formation are yet to be investigated. Therefore, in a very recent study, the effects of various ROS inhibitors and ROS regulating enzymes on haustorium formation in S. hermonthica have been investigated. During the treatment with DMBQ and syringic acid, NADPH oxidases and peroxidases inhabit haustorium formation. They concluded that ROS production and regulation via NADPH oxidases and peroxidases play a crucial role in haustorium formation (Wada et al. 2019). Salt stress is one of the biggest abiotic challenges in plant growth and development. The symbiosis between plants and arbuscular mycorrhizal fungi can help reduce salt stress by alteration in the SLs level in the plant host. Kong et al. (2017) experimented to find out the answer to the question of whether SLs enhances tolerance to salt stress in AM Sesbania cannabina seedlings? Results revealed that the level of SLs is increased with the increase in the treatment time of NaCl application. NADPH oxidase activity and chemical scavenging of H2O2 inhibition significantly reduce the salt tolerance and SLs levels. The H2O2 induced SLs levels were escorted by enhanced salt tolerance. It has been concluded that increased H2O2 concentration leads to increased activity of NADPH oxidase, which ultimately regulates more salt stress tolerance due to SLs accumulation in AM S. cannabina seedlings.

4.4  Karrikins Karrikins (KARs) belong to the class of smoke-derived butanolide compounds that are beneficial for the promotion of seed germination and control distinct characteristics of the plants development. They influence the early stages of plant development by various mechanisms (Flematti et  al. 2004; Chiwocha et  al. 2009; Soundappan et al. 2015; López-Ráez 2016) and are structurally similar to SLs but could be differentiated on the physiological basis (Zhao et al. 2018). Considering the sources of production, effects on germination of different seedlings, and AM symbiosis, SL and KARs have been found to show distinct individual behavior and have added a lot of uncertainty to their role. Nelson et al. (2011) have linked the signal transduction for SL and KARs while providing insights into expression

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analysis and regulation mechanisms of related genes. The activity of F-box protein max2, which is part of a complex called SkpCullin-F-box (SCF), affects the signaling of SL and KARs (Soundappan et al. 2015). The potential modulators of max2 activity, SL-insensitive Arabidopsis thaliana dwarf 14 (AtD14) and KAR-insensitive 2 (KAI2), are needed to determine the Arabidopsis response to KARs and SLs. Whereas, being activated by SL, the AtD14 regulates the repressed branching in plant shoots, promotes the leaf senescence, and determines the interaction with the F-box protein D3/max2 (D3 is the rice ortholog of Arabidopsis max2) while enhancing plant stress tolerance. Similarly, the KAI2 is activated by KARs, and it interacts with the F-box protein max2. On the contrary to AtD14, it inhibits various physiological functions, including seed germination, elongation of the hypocotyl in seedlings, and introduces changes in leaf and root hair growth (Zhao et al. 2018). KARs was associated with the expansion of cotyledon and SL was found to repress the axillary branching along with repression of smxl 6, 7, 8 max2, and reduction in the branch numbers of a primary rosette. Due to this, the later mentioned was also found to suppress the max2 phenotypes, which are known to result in SL D14-regulated growth (Soundappan et al. 2015). Difference between two different phenotypes, AtD14 and KAI2, in Arabidopsis showed that SL and KARs regulate various aspects of the max2 related development; therefore, max2 reflects a combination of these two compounds. However, the formerly mentioned orthologue determines the normal SL responses in adult plants and seedlings, and later one determines the plant responses to KARs (Waters et al. 2012). The function of negative regulators and suppressors of SL signaling, smxl 6, 7, and 8, under drought conditions, was investigated by Li et al. (2020). Analysis involving the smxl 6, 7, and 8 mutants showed that when compared to wild type, they appeared to have a better tendency to adapt under water-deficient conditions owing to various properties such as less water loss, high leaf surface temperature, and less cuticle permeability. Furthermore, the KAR-specific endogenous KAI2 signaling was suggested to regulate the cuticular water permeability in plants. Since some of the SMXL genes play a role in mediating the signaling of SL and KARs, the investigation of the possible involvement of SL and KAR-independent SMXL proteins was carried out to find their role in Arabidopsis thaliana to regulate the formation of phloem. The smxl 3, 4, and 5 deficiency altered the accumulation of sugar, leading to defects in phloem formation. The diversity of SMXL protein is crucial since proteins function differently to the KARs and SL signaling mediators (Wallner et al. 2017). The presence of many phenotypic variables including seed germination and growth, leaf shape, and petiole orientation is shared by KAI2 and max2 mutants alike and are absent in D14 species implying the presence of an unknown ligand in KAI2. The KAI2 and max2 are also involved in response generation to the non-SL, endogenous signal (Conn and Nelson 2016). The Gibberellic Acid Insensitive Dwarf 1 (GAID1) receptors bind to GA, followed by some conformational changes in the GA signaling mechanism. This stimulates an interaction with GA repressor proteins called DELLAs. These proteins also help plants to respond to the GA. The similarities in their signaling pathways

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have also developed a proposition that the max2 targets are very similar to DELLAs with regard to the roles and regulations. This iterates that all three pathways of SL, KARs, and GA signaling are also very much similar since the involved mechanisms require F-box protein and other similar receptors, including KAI2, D14, and GA receptors (Stanga et al. 2013). At high concentrations, the GR-24 has been found to promote the germination of lettuce seedlings due to its role as highly karrikinolide responsive species. On the contrary, tests with other karrikinolide responsive species like Solanum orbiculatum showed no stimulatory activity. Studies have reported KARs to be active in a range of parasitic seedlings. Besides, the karrikinolide showed mix evidence where they could or could not stimulate the rate of germination in strigol responsive species (Chiwocha et al. 2009). Some previous studies reported that karrikinolide could mimic the physiological function of GA. Later on, the results obtained by experimental setup for germination of light-sensitive lettuce seedlings using smoke substitutes for light showed that the rates of germination were comparable to the results obtained with GA treatment. The seeds germination induced by smoke decreased rapidly upon exposure to a GA biosynthesis inhibitor, paclobutrazol (Gardner et al. 2001; Flematti et al. 2010).

4.5  Nutrients Stressed Environment Nutrients uptake and distribution are important for normal plant functioning, which could maintain plant health by ensuring sufficient growth and development. Various studies have reported a negative impact of the nutrients deficiency on the growth parameters (Yoneyama et al. 2012; Gamir et al. 2020; Salim and Raza 2020). As a response to the nutrients stressed environment, SLs modulate the plant’s response and may impact the root and shoot architecture (Luo et al. 2018). Literature shows that P and N deficiency elevated the SL levels in plants followed by secretion into the soil. This process could promote the symbiotic relation with AM and soil bacteria to help the plants to survive under nutrients starvation and suppresses the shoot growth while stimulating the root length and development (Marzec and Melzer 2018). The expression levels of TaD27 and TaCCD8 genes increased in wheat and were significantly induced under P deficient conditions. Similarly, 1 week of P starvation in tomato resulted in high levels of SLs, orobanchol, and solanacol. Furthermore, the exogenous application of SL analog 2‫׳‬-epi-GR24 in tomato elevated the SL levels regardless of the normal conditions or restricted supply of P, and this increase was dose-dependent (Gamir et al. 2020). In rice, the effect of SL on the growth of roots and shoots was found dependent on the N supply. It was observed that under N deficient conditions, unlike shoot length, the root length continually increased in the mutants as well as in the wild type. In contrast to these wild-type plants, the SLs signaling and biosynthesis mutants showed a reduced plant response under P deficiency in roots, which could not be regulated by the GR24 through its exogenous application (Luo et al. 2018). Yoneyama et al. (2012) reported that tomato plants also promoted the orobanchol,

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solanacol, and didehydro-orobanchol exudation to form AM in the rhizosphere in response to the P starvation but exudate formation of any of these SLs was not affected under N deficient conditions during early phases when compared to the control. The orobanchol exudation was increased by about 100-folds. Data suggested a strong growth inhibition after the 10 days of tomato incubation under N deficient conditions showing a reduction in SL exudation in the plants. Along previously reported N and P deficiencies, a low level of sulfates (S) in plants may result in high levels of SL.  The study of LJ angle along expression of SL biosynthesis genes in rice under macronutrient deficient conditions revealed comparatively larger LJ angle in SL mutants when compared to the wild-type counterparts. These plants were dwarf with excessive shoot branching and showed leaf senescence at later stages of their life cycle. The nutrients (N, P, or S) stressed conditions in wild-type plants and GR24 treatment in the SL mutants significantly reduced the LJ angle (Shindo et al. 2020). A study featuring eight genotypes of Vicia faba showed that the nutrients deficiency caused significant effects on the two genotypes, G5 and G9, which were resistant and susceptible respectively to root holoparasites Orobanche foetida and Orobanche crenata. The N and P deficiency positively regulated the SL exudation to almost similar levels in both genotypes. Still, more SLs were exuded from the plants subjected to high sensitivity to N deficiency. The plants, therefore, showed a significant reduction in the root and shoot fresh weight, shoot length, and the number of nodes (Trabelsi et al. 2017). Similarly, the GR24 application in Arabidopsis thaliana under the limited supply of P showed that it promoted the expression of P transporter genes in roots. Moreover, the SL signaling in roots under the limited P supply was represented by the downregulation of the expression of different genes such as SMXL6 and SMXL8. It was also indicated that SLs could regulate P deficiency by suppressing hormones, which could negatively affect the plant starvation response (Prerostova et al. 2018). The SL application along N deficiency in microalga Monoraphidium could upregulate the JA, GSH, γ-aminobutyric acid, and lipogenic gene expression to promote lipid biosynthesis, alleviate the oxidative damage, improve the photosynthetic performance, and overall growth (Song et al. 2020).

5  S  trigolactones-Mediated Interaction with Other Soil-Biotic Lodging Agents According to the recent studies, it was observed that interaction of plants with other organisms also have involvement of SLs either at community or individual level (Andreo-Jimenez et  al. 2015; Schlemper et  al. 2017; López-Ráez et  al. 2017; Lanfranco et al. 2018). The gene “LOW GERMINATION STIMULANT 1” mutations of allelic deletion were responsible for resistance phenotype and observed profile of SL (Gobena et al. 2017). The CCD8 gene (gene of SL-biosynthesis) was undergone mutation, which was CRISPR/Cas9-targeted, and through this in tobacco, the effect

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and allelic control of biosynthesis of SL have been observed and demonstrated. CCD8 genes that are closely related have two mutant alleles such as “NtCCD8A” and “NtCCD8B.” In root tissues, they showed differential and distinctive levels of gene expression (Gao et al. 2018), whereas, at the community level, the effect of SL on plant-microbe interaction was demonstrated by CCD8 (max 4) gene’s mutant line (Carvalhais et al. 2019). In the rhizosphere, the fungal communities’ composition was influenced by SL.  In root rhizosphere, some members of fungal species/family/taxa such as Penicillium, Herpotrichiellaceae, Epicoccum nigrum, Mycosphaerellaceae, Fibulochlamys chilensis, and Mycosphaerella were found in abundance, whereas in max4 mutants the Pleosporaceae, Fusarium, and Alternaria have recruited abundantly (Carvalhais et al. 2019). Mycosphaerella and Epicoccum nigrum are pathogenic fungi and are greatly attracted towards the SLs. Additionally, care must be taken to deal with taxonomic work. Different species of plants produced different SL profiles, and according to new research, it has been observed that in microbes, the response towards SLs also varies according to the plant species. Plant species have differences among their biosynthetic pathways for CLA conversion, which influence the production of SL profile (Bruno and Al-Babili 2016; Iseki et al. 2018; Carvalhais et al. 2019; Aliche et al. 2020). However, Iseki et al. (2018) reported that CLA is first converted into an intermediate, 5-DS, by Sorghum and then into sorgomol, whereas CLA is converted directly into strigol by moonseed. Moreover, conversion of CLA into orobanchol occurred directly in tomato by the action of an enzyme, which is unknown yet (Zhang et al. 2018a). Recently, it has been proved that CLA is converted to orobanchol through the accomplishment of an unidentified enzyme in cowpea (Wakabayashi et al. 2019). Different steps, such as epoxidation, oxidation, lactonization, and ring cleavage have been hypothesized to form zealactone and SL from CLA (Charnikhova et al. 2017; Aliche et al. 2020). Various studies have mentioned and tried to uncover the mechanisms to understand the relation present between microbial recruitment and SL profile. Moreover, further research is required to understand the mechanisms and interactions of plant-­ microbe, which are based on SLs. Notably, SLs also show some indirect benefits in the soil, such as phytoremediation (Vosátka et al. 2012; Lenoir et al. 2016; Aliche et al. 2020), but much more dedicated work is required to find out the mechanism and its effects.

5.1  Strigolactones as a Defensive Agent Against Biotic Stress Although, the overhead discussion emphasized on the possible benefits of SLs-­ based employment of the soil microorganisms by plants, whereas other helpful agricultural applications of SLs in the soil are the management of parasitic weeds and defense against several soil-borne diseases. Nevertheless, agriculture is mostly

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threatened by parasitic weeds because their seeds are viable for a long time in soil and are easily spread further in the fields (Rubiales and Fernández-Aparicio 2012; Goldwasser and Rodenburg 2013). Various practical applications were reviewed by Screpanti et al. (2016) for the reduction of parasitic weeds. In Sorghum and tobacco, suicidal germination was tested to control S. hermonthica (Lendzemo et al. 2007; Mohemed et al. 2018) and Orobanche ramosa (Zwanenburg et al. 2016; Yanev and Kalinova 2020), respectively. In suicidal germination, parasitic weeds are germinated (SL bases/connected) without a suitable host. In this way, before crop cultivation, weeds are died off (Zwanenburg et  al. 2016). For conferring battle against various plant-biotic diseases, the potential of SL is least understood, and the actual potential role is yet to be determined. ABA plays essential roles together with SA and JA, in improving plant defense against biotic stresses (Großkinsky et al. 2016; Ku et al. 2018). The positive side of SL has been demonstrated in tomato when SL biosynthetic mutants showed the defense against Meloidogyne incognita (root-knot nematode) and fungal pathogens such as Alternaria alternate and Botrytis cinerea due to its cross talk with others (Marzec 2016; Xu et al. 2019). Whereas, in the pea plant, from some studies, it was revealed that there is no SL involvement against resistance to Pythium irregulare and Fusarium oxysporum (Foo et al. 2016). The main component in the response to defense of plants was identified as MAX2, by reverse genetics approach. Stomatal conductance was increased in mutant max2 plants. Due to this, in the apoplast, the entry of pathogen is promoted, and the susceptibility to Pectobacterium carotovorum and Pseudomonas syringae was increased. Besides this, decreased tolerance was showed by plants to hormonal signaling and ROS, which was triggered by pathogens (Piisilä et al. 2015). According to these findings, it has been suggested that the SLs role in defense is specific for a combination of plant-pathogen only. The identification of motifs such as 19 cis-regulatory was led by using the promotor region of four biosynthetic regions of Arabidopsis SL through in-silico analysis. Multiple copies of these motifs that exist in the majority were regulated by SLs. ATHB-1, GATABOX, MYBIAT (drought stress response), SURECOREATSULTRII (nutrient stress response), GTCONSENSUS (light response), and ACGTATERDI are some of the identified motifs. SL is not functionally organized in two motifs, ASFMOTIFACAMV and WBOXATNPRI, which have a fundamental function in biotic stress. These two cis-elements also play their role in SA signaling and have their role in reactions during plant defense, such as action against viruses, bacteria, and fungi. The SLs biosynthesis genes present in rice contain two motifs that were identified as BIHD1OS and WRKY1OS. In rice (D17/HTD1, MAX1) and Arabidopsis SL genes, an additional flood response motif was present that is identified as ANAERO1-3CONSENSUS (Marzec and Muszynska 2015).

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6  E  ngineering SLs Biosynthesis for the Development of Climate-Resilient Plants Strigolactones have been known to play a vital role in primary, lateral and AR formation, root hair development, seed germination, nodulation, photomorphogenesis, secondary growth, and biotic and abiotic stress tolerance. Like many other plant hormones, SL has a primary role in plant growth and development; however, recently, it has been suggested that ABA levels regulate the production of SLs. Therefore, there is a possibility that it could play a crucial role in stress management. It has been reported that nutrient starvation has a strong influence on the biosynthesis of SLs, and its production is pivotal under stress conditions (Marzec and Muszynska 2015; Lechat et al. 2015; Pandey et al. 2016; Ruiz-Lozano et al. 2016; Mishra et al. 2017; Ling et al. 2020; Gamir et al. 2020). Genome engineering is the pioneering field in modern agriculture and the production of climate-resilient plants. It could help to increase the crop productivity manifold, which is not possible with the use of conventional techniques. Genome editing relies on designer nucleases, which can create double-stranded breaks (DSBs), which subsequently can be repaired through non-homologous end joining (NHEJ) or homology-directed repair (HDR) pathways. The most notable genome editing tools in use nowadays are the zinc finger nuclease (ZFNs), transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 system. Among these, a special genome editing tool with many potential benefits is the bacterial adaptive CRISPR system (Razzaq et al. 2019; Sedeek et al. 2019; Bari et al. 2019; Zafar et al. 2020). Genome editing technologies mainly, the CRISPR/Cas system, so far have been applied in genetic improvement of SLs potential. Plant architecture is an essential feature in the growth and development of plants, and SLs are known from times for their crucial role in inhibiting tillering. Butt et al. (2018) used to disrupt the CCD7 gene, which has been known to play a pivotal role in the SLs biosynthesis pathway in Oryza sativa through the CRISPR system. Mutants of CCD7 have shown a remarkable increase in tillering as well as the reduced height that could be rescued by the application of GR24. Phelipanche aegyptiaca and Orobanche spp. are obligate plant parasites responsible for devastating damage to crops. These parasitic seeds relay on many factors and compounds such as SLs from the host plant to germinate. SLs are important carotenoid derivatives, and their pathway involves a gene Carotenoid Cleavage Dioxygenase 8 (CCD8). Until now, there is no specific way to control parasitic weeds (Bari et al. 2019). Therefore, Bari et al. (2019) used genome editing tools to develop resistance in host plants against these parasitic weeds. They used CRISPR/ Cas9 system-based mutagenesis in the CCD8 gene to control Phelipanche aegyptiaca and Orobanche spp. weeds. Single guided (sgRNA) was used to target the second exon of CCD8 gene in Solanum lycopersicum plants. This type of genome editing resulted in numerous CCD8-Cas9 mutants with variable insertions/deletions with no possible off-targets. T1 plants upon genotyping have shown that mutations

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introduced in CCD8 gene are often inherited. Besides, CCD8-mutant plants have shown different morphological changes such as excessive shoot branching, dwarfism, and AR formation than control plants. Moreover, CCD8-mutants with SLs deficiency showed a reduction in parasitic infestation than non-mutant plants. Overall, in CCD8-mutant lines, SLs content, carotenoids levels, and expression of genes were increased compared to control tomato plants (Bari et al. 2019). Based on the available literature, a high number of experiments are needed to be conducted to engineer the SLs biosynthesis to uncover the potential of SLs for the improvement of plant physiological and morphological features, and to develop resistance against a variety of environmental stresses.

7  S  trigolactones-Mediated Interaction and Cross Talk with Other Hormonal Signaling Since the start of SLs research, the collective carotenoid predecessor of SLs and ABA have fascinated the probable cross talk of SLs at several levels of biosynthesis. Even though the early employed theory was that both hormones interrelate with each other at the biosynthetic level, and the introduction of ABA biosynthesis influences SLs development and vice versa by substrate competition. Figure 4 shows the interaction and cross talk of SLs with other hormones.

Fig. 4  Strigolactones-mediated interaction and cross talk with other hormones. Dark blue arrows denote activation of the procedure; red lines with bar denote repression, while green arrows denote moderately explored progression promoted by SLs. Abbreviations are described in the text. Adapted from Saeed et al. (2017)

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7.1  Strigolactone and Auxins For the regulation of plant biological processes, endogenous auxins work with other phytohormones, and they may act in a synergistic or antagonistic manner (Leyser 2018). Various links have been revealed between the signaling of SLs and auxins. Auxins influenced the signaling of SLs through the modulation of the biosynthesis process of SLs. Auxins upregulated the expression of genes encoding CCD7- and CCD8, for controlling the shoot branching (Arite et al. 2007). For the regulation of shoot branching, interference of SLs showed with PAT/distribution (Sun et  al. 2014). In the activation and outgrowth of bud, flux, or canalization of auxin is a prominent and significant factor (Balla et  al. 2016). SLs downregulated PIN-­ FORMED protein expression and the influx and efflux of auxin from cells were carried out by these protein families. The bud development repression was resulted due to polarized localization of these proteins on the plasma membrane, which will result in the dampening of the PAT stream’s sink strength of auxin (Domagalska and Leyser 2011; Koltai 2011, 2014; Hu et  al. 2018). Moreover, according to some reports, the transport of auxins in pea had some inhibitory effects in mutants of SL-deficient on the growth of bud, whereas SLs could inhibit outgrowths of bud in pea plants having reduced transport of auxin (Brewer et al. 2009, 2015).

7.2  Strigolactone and Cytokinin According to physiological processes, the variation occurs between SLs and CKs. During the activation of adventitious bud, both acts antagonistically in Zantedeschia (Manandhar et al. 2018), in adventitious rooting, both act independently in peas and Arabidopsis (Rasmussen et  al. 2012). Whereas in the lateral root developmental regulation, they act synergistically (Jiang et al. 2016). The expression level of biosynthesis genes may also regulate by these hormones (Dun et al. 2012). The interaction of CKs and SLs is directly in bud for the mediating shoot branching/bud activation with action that connects transcriptional regulation of FC1 (Xu et  al. 2015), and BRC1 in rice, Arabidopsis and pea, correspondingly (Braun et al. 2012; Xu et al. 2015). From all those factors which are involved in the homeostasis of CKs and SLs in the bud, will involve in the developmental process of a bud.

7.3  Strigolactone and Abscisic Acid Studies over the last decade have suggested that in mediating the responses of plant and its resilience to biotic and abiotic stresses, there are expectations that, in plants, the interaction of SLs occurs with ABA (directly/indirectly) for regulating adaptive stress responses. The points from which the interactions of SLs and ABA can infer

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are following, such as the responses mediated by ABA was obtained by modulating the signaling of SLs. This view is supported by different observations that in plants deficient of ABA. On the other hand, the expression of genes elaborated in the biosynthesis of SLs and SLs content is lowered significantly (Wang et  al. 2018). However, towards drought stress, the SLs signaling and deficient mutants are hypersensitive, and they showed a reduction in stomatal sensitivity to ABA (Lv et  al. 2018), and also showed less sensitivity towards it in tomato plants (Visentin et al. 2016). In the line of SLs deficient, the induction of increasing levels of ABA was not seen, which was due to water loss and increasing stomatal aperture (Cheng et al. 2017). ABA upregulates the genes which cause production and signaling of SLs in Sesbania cannabina for mediation of tolerance against salt stress (Ren et al. 2018). In fruit ripening and shoot architecture, the interactions of ABA and SLs are antagonistic. The formation of the tiller is enhanced by suppression of expression of genes causing signaling and biosynthesis of SLs, by ABA (Wang et al. 2018).

7.4  Strigolactone and Jasmonate Jasmonates are involved in the mediation of physiological processes during secondary metabolism, vegetative growth, wounding, and interactions of plant-pathogens and plant-insects. The experimental data is limited due to which the nature of cross talk between jasmonate-SLs cannot be described clearly. Whereas, in tolerating disease, the connection between jasmonates and SLs has been reported. Results suggest that in Sl-ccd8, a tomato mutant (SL-deficient), the content of JA and expression of gene PINII (jasmonate-dependent) were reduced to enhance the disease tolerance (Torres-Vera et al. 2014, 2016). Notable, Nt-PDR6 (Nicotiana tabacum PDR6) is an SLs transporter’s gene orthologue and methyl jasmonate (MeJA) is responsible for exerting influence on Nt-PDR6 for the modulation of shoot branching (Xie et al. 2015).

7.5  Strigolactone and Salicylic Acid In the perception of the plant defense mechanism against abiotic stresses and pathogens, SA are prominent features of guard cell SA signaling through the Ca2+/CPK-­ dependent pathway in Arabidopsis (Prodhan et al. 2018). The impact of SA signaling on the production of ROS is the main point of showing control on this aspect (Herrera-Vásquez et al. 2015a, b). The interactions of SA and SLs were observed between the interactions of endophytic fungus and plant, in which GR24 induces the SA accumulation, and the concentration of SA had decreased by max2, a mutant of SL signaling (Rozpądek et  al. 2018). Thus, to infections, responses of plant defense may influence by SLs through the induction of SA signaling.

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7.6  Strigolactone and Ethylene SLs control the ET signaling, which is involved in regulating some developmental and growth processes in plants (Vanstraelen and Benková 2012). Some of these processes include elongation of root hair, hypocotyl growth, germination of the seeds, and leaf senescence. SLs utilize ET for the recruitment of auxin signaling, and thus the implication of cross talk, which is three-way hormonal cross talk occurs for controlling the development of root hair (Yamada et al. 2014). ET and SLs are both involved in the formation of AR.  Previously it was suggested that both act independently but the SLs and 1-aminocyclopropane-1-carboxylic acid (ACC), the precursor of ET, worked antagonistically in 1/3 of the hypocotyl. Thus, regardless of the fact that formation of AR was promoted by ACC, in hypocotyl’s lower part, SLs and ACC were found to inhibit this process (Rasmussen et al. 2017; Lakehal and Bellini 2019). Biosynthesis, as well as the perception of SLs, are now targets of researchers to understand how signaling pathways of SL production are explained in the development of both plants and environmental responses. However, various studies are going on to find the effects of SLs on the adaptation mechanism of plants to a variety of environmental stresses.

8  Conclusions Both biotic (bacteria, fungi, viruses, etc.) and abiotic stresses (drought, salinity, temperature, ROS, nutrient depletion, etc.) adversely affect the plant growth, yield, and development across the globe. They may suppress the production of stress tolerance-­enhancing compounds like SLs, which are needed to counteract the adverse effects on plants under unfavorable conditions. Literature suggests that SLs may also drive various plant responses to environmental stresses, including complex hormonal interactions, enzymes production, activation of antioxidant machinery, and roots symbiotic relationship which may alleviate not only the negative impacts but also boost the crop productivity. Roots act as the first line of defense against the stresses, but the in-depth analysis of the cited studies revealed that along with these responses, SLs also influence the shoot architecture to facilitate and elucidate the adverse effects on plants. The cross talk of SLs with phytohormones provided further insights with regard to changes in the molecular structures, physiological processes, and biochemical mechanisms in plants. Suggesting a need to harness the opportunity to explore the SL-hormonal interactions and get further insights into the plant’s adaptive behavior to various stresses under varying environmental conditions. In present times when the world is urging to adopt agricultural strategies that focus on less use of fertilizers and pesticides, there is a need to utilize the synthetic SLs for the improvement of crops and development of climate change-­ resilient and sustainable agricultural systems. Furthermore, a better understanding

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of diversified structures, SLs biosynthesis pathways, the interaction of plant species, and responses to SLs have a great potential to open avenues for the modern agricultural practices while providing better conditions for plants to acclimatize. Thus, further research is required to access the regulatory networks and potential of SLs to participate in the function of plant adaptation to environmental stresses, while providing further understanding of SLs and diversify its potential for agricultural applications. Additionally, the omics approaches such as transcriptomics, metabolomics, proteomics should be utilized to identify the SLs-associated metabolic pathways and key regulators (genes, proteins, and metabolites) for future research. In addition, the identification of SLs-mediated pathways and regulators can open new windows to decipher the beneficial role of SLs under the harsh environment using genetic engineering approaches.

References Abd-Elmabod SK, Muñoz-Rojas M, Jordán A, Anaya-Romero M, Phillips JD, Laurence J, Zhang Z, Pereira P, Fleskens L, van der Ploeg M (2020) Climate change impacts on agricultural suitability and yield reduction in a Mediterranean region. Geoderma 374:114453 Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci U S A 111:18084–18089 Ablazov A, Mi J, Jamil M, Jia K-P, Wang JY, Feng Q, Al-Babili S (2020) The apocarotenoid zaxinone is a positive regulator of strigolactone and abscisic acid biosynthesis in Arabidopsis roots. Front Plant Sci 11:578 Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186 Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351 Aliche EB, Screpanti C, De Mesmaeker A, Munnik T, Bouwmeester H (2020) Science and application of strigolactones. New Phytol 227(4):1001–1011. https://doi.org/10.1111/nph.16489 Andreo-Jimenez B, Ruyter-Spira C, Bouwmeester HJ, Lopez-Raez JA (2015) Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground. Plant Soil 394:1–19 Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka JJTPJ (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029 Arite T, Kameoka H, Kyozuka J (2012) Strigolactone positively controls crown root elongation in rice. J Plant Growth Regul 31:165–172 Aroca R, Ruiz-Lozano JM, Zamarreño ÁM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55 Bakshi P, Handa N, Gautam V, Kaur P, Sareen S, Mir B, Bhardwaj R (2019) Role and regulation of plant hormones as a signal molecule in response to abiotic stresses. In: Plant signaling molecules. Elsevier, pp 303–317 Balla J, Medveďová Z, Kalousek P, Matiješčuková N, Friml J, Reinöhl V, Procházka S (2016) Auxin flow-mediated competition between axillary buds to restore apical dominance. Sci Rep 6:35955

158

A. Raza et al.

Banerjee A, Roychoudhury A (2018) Strigolactones: multi-level regulation of biosynthesis and diverse responses in plant abiotic stresses. Acta Physiol Plant 40:86 Barbier FF, Dun EA, Kerr SC, Chabikwa TG, Beveridge CA (2019) An update on the signals controlling shoot branching. Trends Plant Sci 24:220–236 Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P, Pacak AM, Vazquez F, Karlowski W, Jarmolowski A (2015) Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Front Plant Sci 6:410 Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488 Bari VK, Nassar JA, Kheredin SM, Gal-On A, Ron M, Britt A, Steele D, Yoder J, Aly R (2019) CRISPR/Cas9-mediated mutagenesis of CAROTENOID CLEAVAGE DIOXYGENASE 8 in tomato provides resistance against the parasitic weed Phelipanche aegyptiaca. Sci Rep 9:1–12 Basbouss-Serhal I, Leymarie J, Bailly C (2016) Fluctuation of Arabidopsis seed dormancy with relative humidity and temperature during dry storage. J Exp Bot 67:119–130 Bettini P, Cosi E, Bindi D, Buiatti M (2008) Reactive oxygen species metabolism in plants: production, detoxification and signaling in stress response. Plant Stress 2:28–39 Bonneau L, Huguet S, Wipf D, Pauly N, Truong HN (2013) Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. New Phytol 199:188–202 Braun N, de Saint Germain A, Pillot J-P, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-­ Grondard A, Le Signor C, Bouteiller N (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol 158:225–238 Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493 Brewer PB, Dun EA, Gui R, Mason MG, Beveridge CA (2015) Strigolactone inhibition of branching independent of polar auxin transport. Plant Physiol 168:1820–1829 Brewer PB, Yoneyama K, Filardo F, Meyers E, Scaffidi A, Frickey T, Akiyama K, Seto Y, Dun EA, Cremer JE (2016) LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 113:6301–6306 Bruno M, Al-Babili S (2016) On the substrate specificity of the rice strigolactone biosynthesis enzyme DWARF27. Planta 243:1429–1440 Bu Q, Lv T, Shen H, Luong P, Wang J, Wang Z, Huang Z, Xiao L, Engineer C, Kim TH (2014) Regulation of drought tolerance by the F-box protein MAX2  in Arabidopsis. Plant Physiol 164:424–439 Butt H, Jamil M, Wang JY, Al-Babili S, Mahfouz M (2018) Engineering plant architecture via CRISPR/Cas9-mediated alteration of strigolactone biosynthesis. BMC Plant Biol 18:1–9 Carvalhais LC, Rincon-Florez VA, Brewer PB, Beveridge CA, Dennis PG, Schenk PM (2019) The ability of plants to produce strigolactones affects rhizosphere community composition of fungi but not bacteria. Rhizosphere 9:18–26 Charnikhova TV, Gaus K, Lumbroso A, Sanders M, Vincken J-P, De Mesmaeker A, Ruyter-Spira CP, Screpanti C, Bouwmeester H (2017) Zealactones. Novel natural strigolactones from maize. Phytochemistry 137:123–131 Cheng X, Floková K, Bouwmeester H, Ruyter-Spira C (2017) The role of endogenous strigolactones and their interaction with ABA during the infection process of the parasitic weed phelipanche ramosa in tomato plants. Front Plant Sci 8:392 Chiu RS, Pan S, Zhao R, Gazzarrini S (2016a) ABA-dependent inhibition of the ubiquitin proteasome system during germination at high temperature in Arabidopsis. Plant J 88:749–761 Chiu RS, Saleh Y, Gazzarrini S (2016b) Inhibition of FUSCA3 degradation at high temperature is dependent on ABA signaling and is regulated by the ABA/GA ratio. Plant Signal Behav 11:e1247137 Chiwocha SD, Dixon KW, Flematti GR, Ghisalberti EL, Merritt DJ, Nelson DC, Riseborough J-AM, Smith SM, Stevens JC (2009) Karrikins: a new family of plant growth regulators in smoke. Plant Sci 177:252–256

Strigolactones for Sustainable Plant Growth and Production Under Adverse…

159

Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867 Claassens AP, Hills PN (2018) Effects of strigolactones on plant roots. In: Root biology. Springer, pp 43–63 Conn CE, Nelson DC (2016) Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front Plant Sci 6:1219 Cook C, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190 Cooper JW, Hu Y, Beyyoudh L, Yildiz Dasgan H, Kunert K, Beveridge CA, Foyer CH (2018) Strigolactones positively regulate chilling tolerance in pea and in Arabidopsis. Plant Cell Environ 41:1298–1310 De-la-Peña C, Nic-Can GI, Avilez-Montalvo J, Cetz-Chel JE, Loyola-Vargas VM (2017) The role of miRNAs in auxin signaling and regulation during plant development. In: Plant epigenetics. Springer, pp 23–48 Djennane S, Hibrand-Saint Oyant L, Kawamura K, Lalanne D, Laffaire M, Thouroude T, Chalain S, Sakr S, Boumaza R, Foucher F (2014) Impacts of light and temperature on shoot branching gradient and expression of strigolactone synthesis and signalling genes in rose. Plant Cell Environ 37:742–757 Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211–221 Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158:487–498 FAO, UNICEF, WFP, WHO (2018) The State of Food Security and Nutrition in the World 2017: Building Resilience for Peace and Food Security; Food and Agriculture Organization of the United Nations (FAO): Rome, Italy Felemban A, Braguy J, Zurbriggen MD, Al-Babili S (2019) Apocarotenoids involved in plant development and stress response. Front Plant Sci 10:1168 Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977–977 Flematti GR, Scaffidi A, Goddard-Borger ED, Heath CH, Nelson DC, Commander LE, Stick RV, Dixon KW, Smith SM, Ghisalberti EL (2010) Structure–activity relationship of karrikin germination stimulants. J Agric Food Chem 58:8612–8617 Foo E, Blake SN, Fisher BJ, Smith JA, Reid JB (2016) The role of strigolactones during plant interactions with the pathogenic fungus Fusarium oxysporum. Planta 243:1387–1396 Gamir J, Torres-Vera R, Rial C, Berrio E, de Souza Campos PM, Varela RM, Macías FA, Pozo MJ, Flors V, López-Ráez JA (2020) Exogenous strigolactones impact metabolic profiles and phosphate starvation signalling in roots. Plant Cell Environ 43(7):1655–1668. https://doi. org/10.1111/pce.13760 Gao J, Zhang T, Xu B, Jia L, Xiao B, Liu H, Liu L, Yan H, Xia Q (2018) CRISPR/Cas9-mediated mutagenesis of carotenoid cleavage dioxygenase 8 (CCD8) in tobacco affects shoot and root architecture. Int J Mol Sci 19:1062 Gardner M, Dalling K, Light M, Jäger A, Van Staden J (2001) Does smoke substitute for red light in the germination of light-sensitive lettuce seeds by affecting gibberellin metabolism? South Afr J Bot 67:636–640 Gobena D, Shimels M, Rich PJ, Ruyter-Spira C, Bouwmeester H, Kanuganti S, Mengiste T, Ejeta G (2017) Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. Proc Natl Acad Sci U S A 114:4471–4476 Goldwasser Y, Rodenburg J (2013) Integrated agronomic management of parasitic weed seed banks. In: Parasitic Orobanchaceae. Springer, pp 393–413 Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194 Großkinsky DK, van der Graaff E, Roitsch T (2016) Regulation of abiotic and biotic stress responses by plant hormones. In: Plant pathogen resistance biotechnology. p 131

160

A. Raza et al.

Guan L, Tayengwa R, Cheng ZM, Peer WA, Murphy AS, Zhao M (2019) Auxin regulates adventitious root formation in tomato cuttings. BMC Plant Biol 19:435 Haider I, Andreo-Jimenez B, Bruno M, Bimbo A, Floková K, Abuauf H, Ntui VO, Guo X, Charnikhova T, Al-Babili S (2018) The interaction of strigolactones with abscisic acid during the drought response in rice. J Exp Bot 69:2403–2414 He, H., Lei, Y., Yi, Z. et al. (2021) Study on the mechanism of exogenous serotonin improving cold tolerance of rapeseed (Brassica napus L.) seedlings. Plant Growth Regul 94:161–170 Herrera-Vásquez A, Carvallo L, Blanco F, Tobar M, Villarroel-Candia E, Vicente-Carbajosa J, Salinas P, Holuigue L (2015a) Transcriptional control of glutaredoxin GRXC9 expression by a salicylic acid-dependent and NPR1-independent pathway in Arabidopsis. Plant Mol Biol Rep 33:624–637 Herrera-Vásquez A, Salinas P, Holuigue L (2015b) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 6:171 Hossain A, Raza A, Maitra S, Asaduzzaman Md et al. (2021) Strigolactones: A Novel Carotenoid-­ Derived Phytohormone – Biosynthesis, Transporters, Signalling, and Mechanisms in Abiotic Stress. In: Aftab T., Hakeem K.R. (Eds). Plant Growth Regulators. Springer, Cham, pp 275–303 Hu Q, Zhang S, Huang B (2018) Strigolactones and interaction with auxin regulating root elongation in tall fescue under different temperature regimes. Plant Sci 271:34–39 Iseki M, Shida K, Kuwabara K, Wakabayashi T, Mizutani M, Takikawa H, Sugimoto Y (2018) Evidence for species-dependent biosynthetic pathways for converting carlactone to strigolactones in plants. J Exp Bot 69:2305–2318 Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-­induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144:232–247 Jia K-P, Baz L, Al-Babili S (2018) From carotenoids to strigolactones. J Exp Bot 69:2189–2204 Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:401–405 Jiang L, Matthys C, Marquez-Garcia B, De Cuyper C, Smet L, De Keyser A, Boyer F-D, Beeckman T, Depuydt S, Goormachtig S (2016) Strigolactones spatially influence lateral root development through the cytokinin signaling network. J Exp Bot 67:379–389 Jing X-Q, Shalmani A, Zhou M-R, Shi P-T, Muhammad I, Shi Y, Sharif R, Li W-Q, Liu W-T, Chen K-M (2020) Genome-wide identification of malectin/malectin-like domain containing protein family genes in rice and their expression regulation under various hormones, abiotic stresses, and heavy metal treatments. J Plant Growth Regul 39:492–506 Kapulnik Y, Delaux P-M, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-­ Delmas N, Combier J-P, Bécard G, Belausov E (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216 Khraiwesh B, Zhu J-K, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148 Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987 Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549 Koltai H (2014) Receptors, repressors, PINs: a playground for strigolactone signaling. Trends Plant Sci 19:727–733 Koltai H, Cohen M, Chesin O, Mayzlish-Gati E, Bécard G, Puech V, Dor BB, Resnick N, Wininger S, Kapulnik Y (2011) Light is a positive regulator of strigolactone levels in tomato roots. J Plant Physiol 168:1993–1996 Kong C-C, Ren C-G, Li R-Z, Xie Z-H, Wang J-P (2017) Hydrogen peroxide and strigolactones signaling are involved in alleviation of salt stress induced by arbuscular mycorrhizal fungus in Sesbania cannabina seedlings. J Plant Growth Regul 36:734–742

Strigolactones for Sustainable Plant Growth and Production Under Adverse…

161

Kouzuma A, Watanabe K (2015) Exploring the potential of algae/bacteria interactions. Curr Opin Biotechnol 33:125–129 Ku Y-S, Sintaha M, Cheung M-Y, Lam H-M (2018) Plant hormone signaling crosstalks between biotic and abiotic stress responses. Int J Mol Sci 19:3206 Lakehal A, Bellini C (2019) Control of adventitious root formation: insights into synergistic and antagonistic hormonal interactions. Physiol Plant 165:90–100 Lanfranco L, Fiorilli V, Venice F, Bonfante P (2018) Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J Exp Bot 69:2175–2188 Lechat M-M, Brun G, Montiel G, Véronési C, Simier P, Thoiron S, Pouvreau J-B, Delavault P (2015) Seed response to strigolactone is controlled by abscisic acid-independent DNA methylation in the obligate root parasitic plant, Phelipanche ramosa L. Pomel. J Exp Bot 66:3129–3140 Lendzemo VW, Kuyper TW, Matusova R, Bouwmeester HJ, Van Ast A (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signal Behav 2:58–62 Lenoir I, Sahraoui ALH, Fontaine J (2016) Arbuscular mycorrhizal fungal-assisted phytoremediation of soil contaminated with persistent organic pollutants: a review. Eur J Soil Sci 67:624–640 Leyser O (2018) Auxin signaling. Plant Physiol 176:465–479 Li W, Tran L-SP (2015) Are karrikins involved in plant abiotic stress responses? Trends Plant Sci 20:535–538 Li W, Nguyen KH, Tran CD, Watanabe Y, Tian C, Yin X, Li K, Yang Y, Guo J, Miao Y (2020) Negative roles of strigolactone-related SMXL6, 7 and 8 proteins in drought resistance in Arabidopsis. Biomolecules 10:607 Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:1302–1305 Ling F, Su Q, Jiang H, Cui J, He X, Wu Z, Zhang Z, Liu J, Zhao Y (2020) Effects of strigolactone on photosynthetic and physiological characteristics in salt-stressed rice seedlings. Sci Rep 10:1–8 Liu J, He H, Vitali M, Visentin I, Charnikhova T, Haider I, Schubert A, Ruyter-Spira C, Bouwmeester HJ, Lovisolo C (2015) Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241:1435–1451 López-Ráez JA (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243:1375–1385 López-Ráez JA, Shirasu K, Foo E (2017) Strigolactones in plant interactions with beneficial and detrimental organisms: the Yin and Yang. Trends Plant Sci 22:527–537 Luo L, Wang H, Liu X, Hu J, Zhu X, Pan S, Qin R, Wang Y, Zhao P, Fan XJPS (2018) Strigolactones affect the translocation of nitrogen in rice. Plant Sci 270:190–197 Lv S, Zhang Y, Li C, Liu Z, Yang N, Pan L, Wu J, Wang J, Yang J, Lv Y (2018) Strigolactone-­ triggered stomatal closure requires hydrogen peroxide synthesis and nitric oxide production in an abscisic acid-independent manner. New Phytol 217:290–304 Ma N, Hu C, Wan L, Hu Q, Xiong J, Zhang C (2017) Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L.) by regulating gene expression. Front Plant Sci 8:1671 Manandhar S, Funnell K, Woolley D, Cooney J (2018) Interaction between strigolactone and cytokinin on axillary and adventitious bud development in Zantedeschia. J Plant Physiol Pathol 6:1 Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15 Marzec M (2016) Strigolactones as part of the plant defence system. Trends Plant Sci 21:900–903 Marzec M, Melzer M (2018) Regulation of root development and architecture by strigolactones under optimal and nutrient deficiency conditions. Int J Mol Sci 19:1887 Marzec M, Muszynska A (2015) In silico analysis of the genes encoding proteins that are involved in the biosynthesis of the RMS/MAX/D pathway revealed new roles of strigolactones in plants. Int J Mol Sci 16:6757–6782

162

A. Raza et al.

Matusova R, Rani K, Verstappen FW, Franssen MC, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934 Min Z, Li R, Chen L, Zhang Y, Li Z, Liu M, Ju Y, Fang Y (2019) Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiol Biochem 135:99–110 Mishra S, Upadhyay S, Shukla RK (2017) The role of strigolactones and their potential cross-talk under hostile ecological conditions in plants. Front Physiol 7:691 Mohemed N, Charnikhova T, Fradin EF, Rienstra J, Babiker AG, Bouwmeester HJ (2018) Genetic variation in Sorghum bicolor strigolactones and their role in resistance against Striga hermonthica. J Exp Bot 69:2415–2430 Mostofa MG, Li W, Nguyen KH, Fujita M, Tran LSP (2018) Strigolactones in plant adaptation to abiotic stresses: an emerging avenue of plant research. Plant Cell Environ 41:2227–2243 Mubarik MS, Khan SH, Sajjad M, Raza A, et al. (2021) A manipulative interplay between positive and negative regulators of phytohormones: A way forward for improving drought tolerance in plants. Physiol Plant 172:1269–1290 Muhammad I, Li W-Q, Jing X-Q, Zhou M-R, Shalmani A, Ali M, Wei X-Y, Sharif R, Liu W-T, Chen K-M (2019) A systematic in silico prediction of Gibberellic acid stimulated GASA family members: a novel small peptide contributes to floral architecture and transcriptomic changes induced by external stimuli in rice. J Plant Physiol 234:117–132 Nazir F, Fariduddin Q, Khan TA (2020) Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 252:126486 Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci U S A 108:8897–8902 Ouyang X, Li J, Li G, Li B, Chen B, Shen H, Huang X, Mo X, Wan X, Lin R (2011) Genome-wide binding site analysis of FAR-RED ELONGATED HYPOCOTYL3 reveals its novel function in Arabidopsis development. Plant Cell 23:2514–2535 Pandey A, Sharma M, Pandey GK (2016) Emerging roles of strigolactones in plant responses to stress and development. Front Plant Sci 7:434 Pandey V, Bhatt ID, Nandi SK (2019) Role and regulation of auxin signaling in abiotic stress tolerance. In: Plant signaling molecules. Elsevier, pp 319–331 Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459 Piisilä M, Keceli MA, Brader G, Jakobson L, Jõesaar I, Sipari N, Kollist H, Palva ET, Kariola T (2015) The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol 15:53 Prerostova S, Kramna B, Dobrev PI, Gaudinova A, Marsik P, Fiala R, Knirsch V, Vanek T, Kuresova G, Vankova R (2018) Organ–specific hormonal cross-talk in phosphate deficiency. Environ Exp Bot 153:198–208 Prodhan MY, Munemasa S, Nahar MN-E-N, Nakamura Y, Murata Y (2018) Guard cell salicylic acid signaling is integrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant Physiol 178:441–450 Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157 Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158:1976–1987 Rasmussen A, Depuydt S, Goormachtig S, Geelen D (2013) Strigolactones fine-tune the root system. Planta 238:615–626 Rasmussen A, Hu Y, Depaepe T, Vandenbussche F, Boyer F-D, Van Der Straeten D, Geelen D (2017) Ethylene controls adventitious root initiation sites in Arabidopsis hypocotyls independently of strigolactones. J Plant Growth Regul 36:897–911

Strigolactones for Sustainable Plant Growth and Production Under Adverse…

163

Raza A, Mehmood SS, Tabassum J, Batool R (2019a) Targeting plant hormones to develop abiotic stress resistance in wheat. In: Wheat production in changing environments. Springer, pp 557–577 Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, Xu J (2019b) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants (Basel) 8:34 Raza A (2020) Eco-physiological and Biochemical Responses of Rapeseed (Brassica napus L.) to Abiotic Stresses: Consequences and Mitigation Strategies. J Plant Growth Regul https://doi. org/10.1007/s00344-020-10231-z Raza A, Ashraf F, Zou X, Zhang X, Tosif H (2020) Plant adaptation and tolerance to environmental stresses: mechanisms and perspectives. In: Plant ecophysiology and adaptation under climate change: mechanisms and perspectives I. Springer, pp 117–145 Raza A, Tabassum J, Kudapa H, Varshney (2021) Can omics deliver temperature resilient ready-to-­ grow crops? Crit Rev Biotechnol https://doi.org/10.1080/07388551.2021.1898332 Razzaq A, Saleem F, Kanwal M, Mustafa G, Yousaf S, Imran Arshad HM, Hameed MK, Khan MS, Joyia FA (2019) Modern trends in plant genome editing: an inclusive review of the CRISPR/ Cas9 toolbox. Int J Mol Sci 20:4045 Ren C-G, Kong C-C, Xie Z-H (2018) Role of abscisic acid in strigolactone-induced salt stress tolerance in arbuscular mycorrhizal Sesbania cannabina seedlings. BMC Plant Biol 18:1–10 Rozpądek P, Domka AM, Nosek M, Ważny R, Jędrzejczyk RJ, Wiciarz M, Turnau K (2018) The role of strigolactone in the cross-talk between Arabidopsis thaliana and the endophytic fungus Mucor sp. Front Microbiol 9:441 Rubiales D, Fernández-Aparicio M (2012) Innovations in parasitic weeds management in legume crops. A review. Agron Sustain Dev 32:433–449 Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, García-Mina JM, Ruyter-Spira C, López-Ráez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39:441–452 Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734 Saddiq MS, Iqbal S, Hafeez MB, Ibrahim AMH, Raza A, Fatima EM, Baloch H, Jahanzaib, Woodrow P, Ciarmiello LF (2021) Effect of Salinity Stress on Physiological Changes in Winter and Spring Wheat. Agronomy 11:1193 Saeed W, Naseem S, Ali Z (2017) Strigolactones biosynthesis and their role in abiotic stress resilience in plants: a critical review. Front Plant Sci 8:1487 Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340 Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571 Salim N, Raza A (2020) Nutrient use efficiency (NUE) for sustainable wheat production: a review. J Plant Nutr 43:297–315 Santner A, Calderon-Villalobos LIA, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307 Schlemper TR, Leite MF, Lucheta AR, Shimels M, Bouwmeester HJ, van Veen JA, Kuramae EE (2017) Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol Ecol 93 Screpanti C, Yoneyama K, Bouwmeester HJ (2016) Strigolactones and parasitic weed management 50 years after the discovery of the first natural strigolactone strigol: status and outlook. Pest Manag Sci 72:2013–2015 Sedeek KE, Mahas A, Mahfouz M (2019) Plant genome engineering for targeted improvement of crop traits. Front Plant Sci 10:114

164

A. Raza et al.

Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci U S A 111:1640–1645 Sharif R, Xie C, Zhang H, Arnao MB, Ali M, Ali Q, Muhammad I, Shalmani A, Nawaz MA, Chen P (2018) Melatonin and its effects on plant systems. Molecules 23:2352 Sharif R, Xie C, Wang J, Cao Z, Zhang H, Chen P, Yuhong L (2020) Genome wide identification, characterization and expression analysis of HD-ZIP gene family in Cucumis sativus L. under biotic and various abiotic stresses. Int J Biol Macromol 158:502–520 Sharifi P, Bidabadi SS (2020) Strigolactone could enhances gas-exchange through augmented antioxidant defense system in Salvia nemorosa L. plants subjected to saline conditions stress. Ind Crop Prod 151:112460 Sharma E, Sharma R, Borah P, Jain M, Khurana JP (2015) Emerging roles of auxin in abiotic stress responses. In: Elucidation of abiotic stress signaling in plants. Springer, pp 299–328 Shi T-Q, Peng H, Zeng S-Y, Ji R-Y, Shi K, Huang H, Ji X-J (2017) Microbial production of plant hormones: opportunities and challenges. Bioengineered 8:124–128 Shindo M, Yamamoto S, Shimomura K, Umehara M (2020) Strigolactones decrease leaf angle in response to nutrient deficiencies in rice. Front Plant Sci 11:135 Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11:e1001474 Shuai H, Meng Y, Luo X, Chen F, Zhou W, Dai Y, Qi Y, Du J, Yang F, Liu J, Yang W (2017) Exogenous auxin represses soybean seed germination through decreasing the gibberellin/ abscisic acid (GA/ABA) ratio. Sci Rep 7:12620 Siddiqi KS, Husen A (2017) Plant response to strigolactones: current developments and emerging trends. Appl Soil Ecol 120:247–253 Song X, Lu Z, Yu H, Shao G, Xiong J, Meng X, Jing Y, Liu G, Xiong G, Duan J (2017) IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res 27:1128–1141 Song X, Zhao Y, Han B, Li T, Zhao P, Xu J-W, Yu X (2020) Strigolactone mediates jasmonic acid-­ induced lipid production in microalga Monoraphidium sp. QLY-1 under nitrogen deficiency conditions. Bioresour Technol 306:123107 Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, Leyser O, Nelson DC (2015) SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27:3143–3159 Stanga JP, Smith SM, Briggs WR, Nelson DC (2013) SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol 163:318–330 Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate-and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot 65:6735–6746 Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15:211–216 Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2016) Expression of molecular markers associated to defense signaling pathways and strigolactone biosynthesis during the early interaction tomato-Phelipanche ramosa. Physiol Mol Plant Pathol 94:100–107 Trabelsi I, Yoneyama K, Abbes Z, Amri M, Xie X, Kisugi T, Kim H, Kharrat M (2017) Characterization of strigolactones produced by Orobanche foetida and Orobanche crenata resistant faba bean (Vicia faba L.) genotypes and effects of phosphorous, nitrogen, and potassium deficiencies on strigolactone production. South Afr J Bot 108:15–22 Tsavkelova E, Klimova SY, Cherdyntseva T, Netrusov A (2006) Hormones and hormone-like substances of microorganisms: a review. Appl Biochem Microbiol 42:229–235

Strigolactones for Sustainable Plant Growth and Production Under Adverse…

165

Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6:741 Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200 Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126 Urquhart S, Foo E, Reid JB (2015) The role of strigolactones in photomorphogenesis of pea is limited to adventitious rooting. Physiol Plant 153:392–402 Van Ha C, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Van Dong N (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci U S A 111:851–856 Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487 Visentin I, Vitali M, Ferrero M, Zhang Y, Ruyter-Spira C, Novák O, Strnad M, Lovisolo C, Schubert A, Cardinale F (2016) Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol 212:954–963 Visentin I, Pagliarani C, Deva E, Caracci A, Turečková V, Novák O, Lovisolo C, Schubert A, Cardinale F (2020) A novel strigolactone-miR156 module controls stomatal behaviour during drought recovery. Plant Cell Environ 43(7):1613–1624. https://doi.org/10.1111/pce.13787 Vosátka M, Látr A, Gianinazzi S, Albrechtová J (2012) Development of arbuscular mycorrhizal biotechnology and industry: current achievements and bottlenecks. Symbiosis 58:29–37 Wada S, Cui S, Yoshida S (2019) Reactive oxygen species (ROS) generation is indispensable for haustorium formation of the root parasitic plant Striga hermonthica. Front Plant Sci 10:328 Wakabayashi T, Hamana M, Mori A, Akiyama R, Ueno K, Osakabe K, Osakabe Y, Suzuki H, Takikawa H, Mizutani M (2019) Direct conversion of carlactonoic acid to orobanchol by cytochrome P450 CYP722C in strigolactone biosynthesis. Sci Adv 5:eaax9067 Wallner E-S, López-Salmerón V, Belevich I, Poschet G, Jung I, Grünwald K, Sevilem I, Jokitalo E, Hell R, Helariutta Y (2017) Strigolactone-and karrikin-independent SMXL proteins are central regulators of phloem formation. Curr Biol 27:1241–1247 Wang YH, Irving HR (2011) Developing a model of plant hormone interactions. Plant Signal Behav 6:494–500 Wang F, Perry SE (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 161:1251–1264 Wang L, Wang B, Jiang L, Liu X, Li X, Lu Z, Meng X, Wang Y, Smith SM, Li J (2015) Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27:3128–3142 Wang H, Chen W, Eggert K, Charnikhova T, Bouwmeester H, Schweizer P, Hajirezaei MR, Seiler C, Sreenivasulu N, von Wirén N (2018) Abscisic acid influences tillering by modulation of strigolactones in barley. J Exp Bot 69:3883–3898 Wang JY, Haider I, Jamil M, Fiorilli V, Saito Y, Mi J, Baz L, Kountche BA, Jia K-P, Guo X (2019a) The apocarotenoid metabolite zaxinone regulates growth and strigolactone biosynthesis in rice. Nat Commun 10:1–9 Wang Q, Ni J, Shah F, Liu W, Wang D, Yao Y, Hu H, Huang S, Hou J, Fu S (2019b) Overexpression of the stress-inducible SsMAX2 promotes drought and salt resistance via the regulation of redox homeostasis in Arabidopsis. Int J Mol Sci 20:837 Wang L, Wang B, Yu H, Guo H, Lin T, Kou L, Wang A, Shao N, Ma H, Xiong G (2020) Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature 583(7815):277–281. https://doi. org/10.1038/s41586-­020-­2382-­x Wasaya A, Manzoor S, Yasir TA, Sarwar N, Mubeen K, Ismail IA, Raza A, Rehman A, Hossain A, EL Sabagh A (2021) Evaluation of Fourteen Bread Wheat (Triticum aestivum L.) Genotypes

166

A. Raza et al.

by Observing Gas Exchange Parameters, Relative Water and Chlorophyll Content, and Yield Attributes under Drought Stress. Sustainability 13:4799 Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139:1285–1295 Xia X-J, Zhou Y-H, Shi K, Zhou J, Foyer CH, Yu J-Q (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856 Xie X, Wang G, Yang L, Cheng T, Gao J, Wu Y, Xia Q (2015) Cloning and characterization of a novel Nicotiana tabacum ABC transporter involved in shoot branching. Physiol Plant 153:299–306 Xu J, Zha M, Li Y, Ding Y, Chen L, Ding C, Wang S (2015) The interaction between nitrogen availability and auxin, cytokinin, and strigolactone in the control of shoot branching in rice (Oryza sativa L.). Plant Cell Rep 34:1647–1662 Xu X, Fang P, Zhang H, Chi C, Song L, Xia X, Shi K, Zhou Y, Zhou J, Yu J (2019) Strigolactones positively regulate defense against root-knot nematodes in tomato. J Exp Bot 70:1325–1337 Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:399–408 Yanev M, Kalinova S (2020) Influence of glyphosate on leaf gas exchange and photosynthetic pigments of broomrape-infested tobacco plants. Bulgarian J Agric Sci 26:435–440 Yang T, Lian Y, Wang C (2019) Comparing and contrasting the multiple roles of butenolide plant growth regulators: strigolactones and karrikins in plant development and adaptation to abiotic stresses. Int J Mol Sci 20:6270 Yang Y-Y, Ren Y-R, Zheng P-F, Zhao L-L, You C-X, Wang X-F, Hao Y-J (2020) Cloning and functional identification of a strigolactone receptor gene MdD14 in apple. Plant Cell Tissue Org Cult 140:197–208 Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207 Yoneyama K, Kisugi T, Xie X, Yoneyama K (2013) Chemistry of strigolactones: why and how do plants produce so many strigolactones. J Mol Microbial Ecol Rhizosphere 1:373–379 Zafar SA, Zaidi SS-e-A, Gaba Y, Singla-Pareek SL, Dhankher OP, Li X, Mansoor S, Pareek A (2020) Engineering abiotic stress tolerance via CRISPR/Cas-mediated genome editing. J Exp Bot 71:470–479 Zhang Y, Van Dijk AD, Scaffidi A, Flematti GR, Hofmann M, Charnikhova T, Verstappen F, Hepworth J, Van Der Krol S, Leyser O (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10:1028–1033 Zhang Y, Cheng X, Wang Y, Díez-Simón C, Flokova K, Bimbo A, Bouwmeester HJ, Ruyter-Spira C (2018a) The tomato MAX1 homolog, SlMAX1, is involved in the biosynthesis of tomato strigolactones from carlactone. New Phytol 219:297–309 Zhang Y, Lv S, Wang G (2018b) Strigolactones are common regulators in induction of stomatal closure in planta. Plant Signal Behav 13:e1444322 Zhao Q-P, Wang X-N, Li N-N, Zhu Z-Y, Mu S-C, Zhao X, Zhang X (2018) Functional analysis of MAX2 in phototropins-mediated cotyledon flattening in Arabidopsis. Front Plant Sci 9:1507 Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L (2013) D14–SCF D3-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410 Zou X, Wang Q, Chen P, Yin C, Lin Y (2019) Strigolactones regulate shoot elongation by mediating gibberellin metabolism and signaling in rice (Oryza sativa L.). J Plant Physiol 237:72–79 Zwanenburg B, Blanco-Ania D (2018) Strigolactones: new plant hormones in the spotlight. J Exp Bot 69:2205–2218 Zwanenburg B, Mwakaboko AS, Kannan C (2016) Suicidal germination for parasitic weed control. Pest Manag Sci 72:2016–2025

Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental Conditions Brij Bihari Pandey, Ratnakumar Pasala, Kulasekaran Ramesh, Sumit Kumar Mishra, Nidhi Tyagi, Akankhya Guru, Pappu Lal Bairwa, C. L. N. Manikanta, and Arti Guhey

Abbreviations ABA ACC ADC AdoMetDC DAO

Abscisic acid Amino cyclopropane carboxylic acid Arginine decarboxylase S-adenosylmethionine decarboxylase Diamine oxidase

B. B. Pandey · C. L. N. Manikanta Division of Crop Production, ICAR-Indian Institute of Oilseeds Research, Hyderabad, Telangana, India Department of Plant Physiology, Indira Gandhi Agriculture University, Raipur, Chhattisgarh, India R. Pasala (*) · K. Ramesh Division of Crop Production, ICAR-Indian Institute of Oilseeds Research, Hyderabad, Telangana, India S. K. Mishra Department of Biotechnology, Indian Institute of Technology Roorkee, Roorkee, India Department of Botany, Daudnagar College, Magadh University, Bodhgaya, India N. Tyagi Department of Vegetable Science, Dr. Y.S. Parmar University of Horticulture and Forestry, Solan, India A. Guru Department of Plant Physiology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India P. L. Bairwa Department of Vegetable Science, IGKV, Raipur, Chhattisgarh, India A. Guhey Department of Plant Physiology, Indira Gandhi Agriculture University, Raipur, Chhattisgarh, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_7

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dcSAM Decarboxylated S-adenosylmethionine DFMA a-difluoromethylarginine DFMO a-difluoromethylornithine FAD Flavin adenine dinucleotide GABA γ-Aminobutyric acid LSD Lysine-specific demethylase NO Nitric oxide ODC Ornithine decarboxylase PAO Polyamine oxidase PEG Polyethylene glycol Put Putrescine ROS Reactive oxygen species SAM S-adenosylmethionine SAMDC S-adenosylmethionine decarboxylase Spd Spermidine SPDS Spermidine synthase Spm Spermine SPMS Spermine synthase TSPMS Thermospermine synthase

1  Introduction Globally, climate change and abiotic stresses are a serious threat to food security. Different abiotic stresses under the climate change scenario have adversely affected plant productivity and threatened food production. The abrupt changes in environmental conditions leads to abiotic stresses like water deficit, temperatures extremes, salt and mineral deficiency, toxicity, and altered oxygen levels. On the other hand, an escalated food requirement to feed the continuously increasing population is another serious global concern for farmers and agriculture scientists. According to the FAO report (2009), it was estimated that almost 70% increment in food production is a requisite globally to feed an additional 2.3 billion population by the year 2050. Among the various stresses, water deficit and salinity severely limit crop growth and food production. Similarly, heat stress also causes severe crop damages to a significant level; altogether these stresses bring huge economic losses to farmers (Lobell et  al. 2011). The abiotic stress responses complex as they are being controlled by several intricate factors and each plant species respond differently. The tolerance to these multiple abiotic stresses is also a complex phenomenon that is achieved by making changes at the morphological, physiological, biochemical, and molecular levels in plants. Upon exposure to harsh environmental conditions, changes at the biochemical level lead to modifications in cellular metabolites and

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their activity. These changes are highly linked with the increase in ability of a plant to tolerate respective stress conditions. Among the different changes, an increase in the concentration of metabolites like organic acids, soluble sugars, amino acids, lipids, and polyamines are commonly noticed (Guy 1990). Amid these metabolites, polyamines (PAs) are such compounds that are related to the growth of plant under optimal as well as stress conditions. The PAs are actively engaged with plant’s developmental phases, i.e., embryogenesis, organogenesis, flower development, fruit development, and senescence along with the foremost function to protect macromolecules (Alcázar et al. 2010). The polyamines, i.e., putrescine (Put), spermidine (Spd), and spermine (Spm), are low molecular weight, polycations, aliphatic in nature and found universally in almost all the organisms (Liu et al. 2017; Mustafavi et al. 2018). These polyamines are now considered as a new group in the family of growth regulators in plants (Xu et al. 2014). The polyamines are known as one of the oldest group of compounds (Galston 1991). In the year 1678, van Leeuwenhoek first discovered the tetramine spermine (Spm) from human spermatozoa, while the diamine putrescine (Put) and cadaverine (Cad) were isolated from putrefying cadavers almost a century ago (Brieger 1885). Similarly, diamine putrescine and triamine spermidine (Spd) which are also the most abundant polyamines in nature were found in the 1920s. The findings of Illingworth et al. (2003) suggested that the polyamine biosynthetic pathway in plants was derived from the ancestral cyano-­bacterial precursor of the chloroplast. The polyamine biosynthetic pathway is an ancient pathway that frequently occurs in almost all present-day organisms (Minguet et al. 2008; Liu et al. 2016, 2017). The detailed study of polyamines structures reveals that these are low molecular weight and nitrogen-containing compounds (Hussain et al. 2011; Vuosku et al. 2018). In a cell, polyamines are evenly distributed in all the compartments including the nucleus and regulate a variety of cellular processes (Alcázar et al. 2006b; Kusano et al. 2008). Upon exposure to different stress conditions polyamines are accumulated to great levels in plants, suggesting the protective role of polyamines. By using genetic engineering techniques, polyamines could be targeted to increase plant tolerance to different kind of abiotic stresses (Agudelo-Romero et al. 2013; Pál et al. 2015; Sequeramutiozabal et al. 2016). Due to these properties of polyamines, the plants could be subjected to genetic manipulations for the altered level of polyamines to further explore their functional-biological roles in the growth and development of plants under optimum as well as stress conditions. In this chapter, we have discussed the potential roles of polyamines in plant system, their biosynthetic pathways, catabolism, conjugates, and their role in various abiotic stress conditions. Along with that, we also looked at how the exogenous application of these polyamines modulates the plant responses to different stress conditions. At last, in the chapter, we focused on the role of polyamines in different abiotic stresses and some of the potential mechanisms of polyamines implicated plant responses under abiotic stresses.

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2  Polyamines 2.1  Biosynthesis The key genes that are engaged with the biosynthesis of PAs were detected while complete genome sequencing of Arabidopsis. Within plants, the polyamines are found in free, soluble conjugated and insoluble bound forms. The endogenous levels of polyamines are controlled by anabolic and catabolic reactions (Xu et al. 2014; Mustafavi et  al. 2018). The conjugation (hydroxycinnamic acids) of polyamines also regulates the level of PAs to some extent within the cell. Among the various polyamines found in organisms, Putrescine (Put), spermidine (Spd), and spermine (Spm), thermospermine (Tspm) (Kim et  al. 2014; Sobieszczuk-Nowicka 2017; Takahashi et  al. 2017b; Mustafavi et  al. 2018), and cadaverine (Cad) (Regla-­ Márquez et al. 2015; Nahar et al. 2016) are most common in higher plants. The use of radioactive ornithine (14C) and arginine (14C) in barley confirms the formation of putrescine from both arginine and ornithine (Coleman and Hegartv 1957; Smith and Richards 1962), suggesting that the polyamine biosynthetic pathway is initiated with diamine putrescine (Lefevre et  al. 2001). These two findings suggested the possibility that two independent pathways exist and both arginine and ornithine are responsible for Put biosynthesis. The experiment conducted on E. coli by using C14-­ N15-­putrescine further suggested that diamine putrescine serves as a precursor for the biosynthesis of tri-amine spermidine and tetra-amine spermine (Tabor et  al. 1958). In mammals and fungi, ornithine serves as the precursor for the biosynthesis of Put and enzyme ornithine decarboxylase (ODC, EC 4.1.1.17) catalyzes the reaction (Docimo et al. 2012; Pegg 2016). However, the genes coding for ODC were characterized and activity of ODC has been also reported in many plant species (Michael et al. 1996; Imanishi et al. 1998). Unlike mammals and fungi, an alternative pathway for biosynthesis of Put was reported where arginine serves as the precursor for the synthesis of Put and enzyme arginine decarboxylase (ADC, EC 4.1.1.19) catalyzed the reaction. Although, the ODC pathway is universally accepted pathway in all living organisms for the biosynthesis of Put. In the biosynthetic pathway enzyme, ADC is recognized as a rate-limiting enzyme for Put biosynthesis and the confirmation came from the findings of Alcázar et al. (2005), based on his work on Arabidopsis. The enzyme ADC is found in chloroplast; however, within the chloroplast location varies as in oats it was found to be associated with the thylakoid membranes (Borrell et  al. 1995), while in tobacco it was nuclear or chloroplast localized (Bortolotti et al. 2004). These reports suggested that the ADC pathway is sub-cellularly compartmentalized in plants. Once Put is synthesized, either from ornithine or arginine it follows two consecutive steps, catalyzed by enzymes, viz., agmatine iminohydrolase (AIH, EC 3.5.3.12) and N-carbamoylputrescine amidohydrolase (CPA, EC 3.5.1.53) in which amino-propyl groups are added to Put (Docimo et al. 2012; Pegg 2016). After the addition of aminopropyl group Put gives rise to

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triamine Spd and tetramine Spm with the help of enzymes Spd synthase (SPDS, EC 2.5.1.16) and Spm synthases (SPMS, EC 2.5.1.16), respectively. In parallel reaction, S-adenosylmethionine (SAM) is decarboxylated, regulated by enzyme SAM decarboxylase (SAMDC, EC 4.1.1.50); acts as a donor of the aminopropyl group; and facilitates the production of Spm and Spd (Wimalasekera et al. 2011a, b; Vuosku et  al. 2018). Another plant hormone ethylene is also synthesized from S-adenosylmethionine and two enzymes, i.e., ACC synthase and ACC oxidase, catalyze the reactions. Ghosh (2000) found that in some of the plant species, methylation of Put is catalyzed by N-methyltransferases (PMT) using SAM as substrate. Among the several genes controlling the polyamine biosynthesis, the genes, i.e., Odc, Adc, and AdoMetDC act as key regulators that control the biosynthesis of polyamines under different conditions (Hummel et  al. 2004). Contrarily, besides Spd and Spm, Put also serves as the precursor for various alkaloids including nicotine and tropane in the solanaceae family (Tiburcio et al. 1990).

2.2  Functions in Plant Systems The mutation studies (loss and gain of functional genes) allow the detection and functional characterization of the genes participating in the metabolism for their putative roles in plant development. The previous findings have suggested the role of polyamines during cell division, cell proliferation, and differentiation, regulation of enzyme activity, and programmed cell death in plants (Kusano et  al. 2008). Besides this, the plant developmental processes such as embryogenesis, organogenesis, shoot elongation, root elongation, leaf growth, development of floral tissues and flowers, ripening of fruits, protein synthesis, and senescence are also actively regulated by polyamines (Su et al. 2006; Kusano et al. 2008; Alcázar et al. 2011; Feng and Ji 2011; Zhang et al. 2011; Wimalasekera et al. 2011a; Alet et al. 2012; Tavladoraki et al. 2012; Xu 2015; Pandey et al. 2017; Deotale and Pandey 2018). Generally, at physiological pH polyamines are positively charged and thereby can interact with negatively charged macromolecules (DNA, RNA, chromatin, proteins, and phospholipids) and protect them from denaturation (Igarashi and Kashiwagi 2015). The increased endogenous polyamines content under harsh environmental conditions along with their protective role has been also reported (Vuosku et  al. 2012; de Oliveira et al. 2016; Reis et al. 2016; Mustafavi et al. 2018). Similarly, it was reported that the endogenous level of polyamines (putrescine) was increased under stress conditions by almost 1.2% of the total dry matter (Galston 1991). In addition to this, the exogenous supplies of polyamines and over-expression of polyamine biosynthetic genes modulates the plant’s responses under adverse climatic conditions (Alcázar et al. 2011; Alet et al. 2012).

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2.3  Conjugates of Polyamines In plants, polyamines are present in all forms, i.e., free, conjugated, and insoluble. Generally, polyamines are found conjugated with derivatives of hydroxy-cinnamic acids and are termed as hydroxycinnamic acid amides (HCCAs) (Gholami et  al. 2013). Among the various derivatives, conjugate caffeoylputrescine was first discovered in the year 1893 and also known as paucine that was largely reported in the seeds of leguminous crops (Tiburcio et al. 1990). Besides this, feruloylputrescine, diferuloylspermidine, diferuloylspermine, feruloyltyramine, coumaroylputrescine, coumaroylagamatine, and dicoumaroylspermidine are some other examples of conjugated polyamines found in different plants (Luo et al. 2009; Martin-Tanguy 2001). In lower buds of Arabidopsis, a combination of unique hydroxycinnamic acid conjugates of Spd was also found (Fellenberg et al. 2009). Various kinds of genes were identified which were involved in the formation of conjugates. The formation of conjugates such as tricoumaroyl-Spd, tricaffeoyl-Spd and triferuloyl-Spd is regulated by Spd hydroxycinnamoyl transferase (SHT) gene and is reported in the tapetum cell of Arabidopsis anthers. Similarly, two distinct acyltransferase genes were also identified which control the synthesis of disinapoyl-Spd and sinapoyl-(glucose)Spd in Arabidopsis seeds (Grienenberger et al. 2009; Luo et al. 2009). Upon exposure to stress situations, these conjugates found to be very crucial role in providing the tolerance to plant against the stress conditions and also help in the regulation of plant growth stages (de Oliveira et  al. 2016, 2018; Mustafavi et  al. 2018). With phenolic acids, these conjugates exert antioxidant properties and promote the plant’s ability to cope with stress conditions. Likewise, conjugates along with cinnamic, ferulic, and coffee acids bind with reactive oxygen species (ROS) generated in stress conditions (Bors et al. 1989) and reduce the damages caused by ROS. These conjugated are more efficient scavengers of ROS in comparison to the free form of polyamines. In addition to this, conjugates with transglutaminases protect the photosynthetic apparatus from protease action by binding with Rubisco (Serafini-Fracassini et al. 1995). Thereby, it is worthy to conclude that polyamines-­ conjugates help in reversing the damage caused by different abiotic stresses to photosynthetic efficiency (Sfakianaki et al. 2006). The flower development as well as compatibility in reproduction is also found to be regulated by PA-transglutaminases (Serafini-Fracassini and Del Duca 2008).

2.4  Catabolism The endogenous levels of polyamines are controlled by both biosynthetic and catabolic reactions. The genes which control these reactions (biosynthetic genes and catabolism genes) modulate the levels of polyamines within the cells. The catabolism of polyamines is regulated by several genes which catalyze the oxidative deamination reaction. The catabolism of polyamines is also called as H2O2 biosynthetic

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pathway; hence, the catabolism reactions result in the production of H2O2 which is later used by plants in the processes like lignification and cell wall maturation (Cona et al. 2006; Su et al. 2006). Along with that, produced H2O2 also serves as an important molecule in signaling pathways during various kind of stress (Freitas et  al. 2017; Mellidou et al. 2017). These developmental processes are helpful against both biotic and abiotic stress conditions in plants (Shi and Chan 2014). Two type of enzymes are responsible for the catabolism of polyamines, (1) amine oxidases, i.e., copper-dependent amine oxidase (DAO; EC 1.4.3.6) and flavin-dependent polyamine oxidase (PAO; EC 1.5.3.11) (Smith 1985; Cona et al. 2006). The DAOs catalyze the oxidation of Put and Cad by removing the primary amino group, whereas PAOs facilitate the catabolism of Spd and Spm at the secondary amino group (Cohen 1998). The removal of a primary amino group from diamines (Put and Cad) yields ammonia, H2O2, and 4-aminobutanal, whereas removal of a secondary amino group from tri and tetramines (Spd and Spm) produces 4-aminobutanal and N-(3-­ aminopropyl)-4-aminobutanal. The production of H2O2 and 1, 3-diaminopropane is common in both the oxidation processes (Cona et al. 2006; Liu et al. 2014). Next to this, produced 4-aminobutanal is inter-converted to Δ1-pyrroline by the action of DAOs spontaneously and further changed in 𝛾-aminobutyric acid (GABA) through the catalytic action of enzyme aminobutyraldehyde dehydrogenase (ABALDH; EC 1.2.1.19) (Cona et al. 2006). The trans-amination and oxidation reactions convert GABA into succinic acid which later takes part in the Kreb cycle (Rea et al. 2004). Besides this, the enzyme PAO is also involved in the production of some other polyamines, viz., caldopentamine, caldohexamine, homocaldopentamine, homocaldohexamine, norspermidine, and norspermine; these PAs were proved to be helpful to organisms under adverse environmental conditions (Phillips and Kuehn 1991). Despite PAs oxidation process, back-conversion mechanism of catabolism, related to spermine, was also observed in plants (Liu et al. 2014; Takahashi et al. 2017a). The gene AtPAO1 isolated from Arabidopsis is responsible for the back conversion of spermine (Fincato et al. 2011; Ono et al. 2012; Liu et al. 2014). The catabolic enzyme DAOs are mainly present in dicots; however, the genes encoding for these DAOs have been characterized in a few species only (Alcázar et  al. 2006b). In Arabidopsis a total of 12 DAOs encoding genes were identified and among them, only one has been (ATAO1) successfully characterized (Moller and McPherson 1998). Unlike DAOs, PAOs are abundantly found in monocots and remain non-­ covalently bound to FAD (Takahashi et al. 2017a; Hao et al. 2018). PAOs are generally divided into two different families according to their nature; either associated with back-conversion or terminal breakdown of polyamines (oxidation) (Liu et al. 2014; Takahashi et al. 2017a). The maize PAO (ZmPAO) is the most characterized PAO, classified under the first class of PAOs, and responsible for the terminal breakdown of Spd and Spm. The enzyme Spm oxidase (SMO, EC 1.5.3.3) governs the back-conversion of Spm to Spd and it has been classified as the second type of PAOs. Moschou et al. (2008) also reported another class of PAOs that carries almost similar domain to PAOs; however, the enzymes belonging to this third family are not involved in the deamination reactions. The enzymes which belong to this

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category are relatives of human lysine-specific demethylase 1 (LSD1), which has similar FAD-dependent activity and amine oxidase domain (Shi et al. 2004). The polyamine metabolic pathway is highly inter-related with several other metabolic pathways, which take part in the synthesis of various important metabolites and signaling molecules that are helpful to plants under stress conditions. The synthesis of both polyamines and ethylene are interconnected to each other through SAM, a common precursor in both the pathways. Although, the antagonistic effect among PAs and ethylene has also been observed during late development phases (fruit ripening and senescence) of plants (Pandey et al. 2000; Wi and Park 2002). The metabolic pathway of PAs also interferes with the formation of Nitric Oxides (NO), as it enhances the synthesis of NO (Yamasaki and Cohen 2006). Under the stress conditions, polyamine-mediated stress and other mediators’ responses are associated with the level of NO (Tun et al. 2006). The H2O2 generated during the catabolism of PAs is found to be highly associated with ABA-induced stomata closing under water-deficit conditions and stress signaling under both abiotic and biotic conditions (Cona et al. 2006; An et al. 2008). The oxidations of PAs also produce g-aminobutyric acid (GABA) and it has been observed that the levels of agmatine (Put precursor), Put, GABA, and some other compounds are increase under water-­ deficit conditions (Alcázar et  al. 2006a; Cona et  al. 2006; Urano et  al. 2009). A collective increase of these compounds under water-deficit conditions indicated a connection among these compounds by some metabolic pathways. From sufficient pieces of evidence, it can be concluded that the PAs metabolic pathway is inter-­ related to several other important hormonal and metabolic pathways that together regulate many plant developmental processes under adverse climatic conditions.

2.5  Transport Once the polyamines are synthesized these are transported to the site of action. The cells have an efficient transportation system to transport both endogenously produced as well as exogenously supplied polyamines. The uptake of exogenously applied polyamines is very rapid and shows a biphasic system of uptake. The polyamines are absorbed very rapidly, within 12 min of application; after the uptake, polyamines are accumulated around the protoplast and vacuoles. The transport of polyamines into the protoplast and vacuole is passive and it occurs through the plasma membrane, whereas efflux from protoplast (cytosol) to organelles is mediated by carriers (Pistocchi et  al. 1988). The transport of PAs into the organelles depends on membrane potential and affected by the application of valinomycin and nigericin (potent inhibitors). This hypothesis was later confirmed by Pistocchi et al. (1990) who showed that the transportation of Spd in the mitochondrial matrix of the tubers of Helianthus tuberosus is highly dependent on membrane potential. The mineral ions, i.e., Mg+2 and K+, are also potent inhibitors as these cations interferers for the same binding sites. On the other hand, transport across the tonoplast is completely carrier-mediated, although very little information is available on

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carrier-mediated transportation of polyamines. In rice, Polyamine Uptake Transporter (PUT1) was recognized that reflect high affinity for Spm. Along with that, five additional genes which code for the transporters were also identified in Arabidopsis (Mulangi et al. 2012a, b). After absorption, the polyamines are allocated to different plant parts via long-distance transport (Pistocchi et al. 1988), and in this regard, the experiment on potato with 14C-Put confirms the long-distance transport of polyamines in the phloem (Feray et al. 1991). The xylem sap also contains a high concentration of polyamines, providing sufficient evidence for long-­ distance transport (Friedman et al. 1986; Shevyakova et al. 2001). The long-distance transport of polyamines indicates non-polar translocation of polyamines similar to some of the growth regulators (Bagni and Pistocchi 1991). In some other crops, viz., Ricinus communis (Antognoni et al. 1998), and rice stem (Yokota et al. 1994) the presence of PAs in phloem exudates was reported. Among the polyamines, the diamines are transported easily compared to tri- and tetra-amines, indicating that increase in the number of amino groups decreases the easiness in phloem transport.

3  M  odulations in Levels of Polyamines Under Stress Conditions Concerning polyamine functions, different plant species show different responses upon exposure to stress. As upon exposure to adverse environmental conditions, some of the species might accumulate the polyamines, while other species maintain either a stable or reduced level of the polyamines. For example, tobacco and alfalfa differ in their thermo-sensitivity and when subjected to heat stress both species showed a varied pattern of polyamines (free or conjugated) accumulation (Königshofer and Lechner 2002). Even though, it was reported that different cultivars belonging to the same species also display differences in endogenous polyamine levels (Vakharia et al. 2003). For example, the findings of Liu et al. (2004) indicated that two wheat cultivars upon exposure to drought stress showed a different pattern of polyamines accumulation, as in case of the tolerant cultivar free Spd and Spm content was increased, while, in the sensitive cultivar, free Put content was enhanced. On the other hand, the duration of stress also modulate the polyamines levels. It was reported by several previous researchers that in response to short-­ duration stress the endogenous level of polyamines increased sharply, while only a small fluctuation was observed when plants were exposed to a longer period of stress conditions (Tonon et al. 2004; Legocka and Kluk 2005). This indicates that the accumulation of polyamines levels majorly depends on the onset of stress conditions. In this regard, 15 min of salt treatment to tomato causes a sharp increase in polyamines levels (Santa-Cruz et al. 1997).

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4  E  ffects of Modulating Endogenous Polyamines on the Plant Stress Response It has already been discussed that exposure to harsh environmental conditions leads to modifications in the level of polyamines; however, these modulations only provided an idea about the possible relation of polyamines to stress and did not provide any pieces of evidence regarding the role of polyamines in preventing the consequences of stress on plants. Hence, an exogenous application of PAs either before or during stress subsequently elevates the endogenous polyamine concentration has been attempted to identify and understand the role of polyamines in protecting the plants from stress-related damages (Navakoudis et  al. 2003; Wang et  al. 2004). Various findings have indicated that the exogenous application of PAs could reverse or minimize the inhibitory effects of stress to a varying degree and thus justify the role of polyamines in mitigation of stress-derived injuries.

4.1  Drought Stress Among the various kinds of stress, drought stress is considered as the most serious condition that affects growth, development, and finally the yield of plants. The plant responses upon exposure to drought conditions are very complex and occur at physiological, biochemical, and molecular levels. At biochemical levels, the modulation in endogenous polyamines content is considered to improve drought tolerance (Davies 2004), and in this regard, work has been done by many researchers (Nayyar et al. 2005; Yang et al. 2007; Yamaguchi et al. 2007; Ebeed et al. 2017). The application of Put to Allium fistulum reduces the flooding-induced oxidative damages as the application of Put enhances the antioxidant properties and reduces the superoxide radicals (Yiu et al. 2009). Furthermore, Put provoke the activity of the antioxidative system, ̇O2 scavenging, a-diphenyl-b-picrylhydrazyl (DPPH)-radical scavenging, and metal chelating properties. These polyamines, especially Put and Spd, also play role in improving tolerance even immediately after the exposure to water-deficit conditions in soybean and chickpea. On the other hand, the use of polyamine biosynthetic inhibitors (DFMA, DFMO, and CHA) leads to severe stress injuries in crops (Nayyar et  al. 2005), suggesting the protective role of polyamines under water-limited conditions. The finding of Yang et al. (2007) showed that free Spd, Spm, and conjugated Put enhanced the water stress tolerance in rice which is mainly due to increased activity of SAMDC and SPDS genes. During the water stress conditions, the increased level of free Put (at early stages) and insoluble conjugated Put (whole stress period) contributed to counteract the stress in plants (Sánchezrodríguez et al. 2016; Mohammadi et al. 2018). In addition to this, damages caused by water stress to Arabidopsis can also be reversed by the application of Spm (1 mM) and thus revealed the role of Spm in promoting water stress tolerance (Yamaguchi et al. 2007). Moreover, the role of Spm in controlling the stomatal movement by

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modulating the cytoplasmic Ca levels (involved in stress signaling pathways) was also well reported (Mahajan and Tuteja 2005).

4.2  Salinity Stress Similar to water stress, soil salinity is also a serious problem which is more frequently observed globally in arid and semi-arid regions and restricts the plant productivity. Under salinity stress, the role of different polyamines in protecting the plants from harmful damages has been reported (Verma and Mishra 2005). Among the polyamines, Spd and Spm are highly associated with salinity tolerance in rice and wheat, and a positive relationship between polyamine concentration and salt tolerance has been observed (Chattopadhayay et al. 2002; Li and He 2012). Under salt stress conditions, in rice, the sensitive cultivars were poorer in the accumulation of Spd and Spm; however these cultivars accumulated a higher amount of Put in shoots (Krishnamurthy and Bhagwat 1989). Along with that, the higher Spm and Spd and lower Put content upon exposure to salt stress was also noticed in some crops, viz., spinach, lettuce, melon, pepper, and tomato (Zapata et al. 2004). It is believed that under salt stress conditions Put serves as the precursor for the synthesis of Spd and Spm and that leads to a higher Spd+Spm/Put ratio thus, indicating the protective role of polyamines in salt stress (Xu et al. 2009). Moreover, the molecular approach such as double knockout also confirmed similar facts. The double knocks out mutants from Arabidopsis (acl5/spms) were unable to synthesize Spm and remained susceptible to salt stress in comparison to wild types. Salt stress-induced injuries could be overcome by exogenous application of Spm, whereas Put was found ineffective (Yamaguchi et al. 2006). Interestingly, the pieces of evidence from Pine and Barley seedlings suggested that Put also have a profound effect in conferring salt tolerance (Zhao and Qin 2004; Tang and Newton 2005). Despite this, the role of Spd and Spm in reducing the electrolyte leakages from shoots and roots, negative effect on photosynthesis by enhancing the metabolism of ROS, is also well documented (Meng et al. 2015; Baniasadi et al. 2018). The salinity stress is generally associated with increased toxicity of sodium and further osmotic disturbances. To encounter the salt stress, plants adopt a strategy of sequester the sodium ions in vacuole with the help of a tonoplast Na/H antiporter and it helps in maintaining a higher [K/Na] ratio. It was reported that polyamines are involved in blocking several type of ion channels and the increased level of Spm restricted the activity of fast vacuolar (FV) channel under high salt stress (Bruggemann et al. 1988). Furthermore, PAs reduces the Na influx and therefore lead to selective absorption of Na to balance the ratio of Na and K (Na/K). Similar reports on restricted Na absorption are available in some other crops such as barley (Zhao et al. 2007) and pea (Shabala et al. 2007). The PAs are also involved in the regulation of stomatal movements, and in the case of Vicia faba guard cells, polyamines (Spm) induced the stomata closure by controlling the KAT1-like voltage-dependent inward K channels (Liu et al. 2000;

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Yamaguchi et al. 2007). All these conclusive evidence suggested that PAs play a very crucial role to overcome the detrimental effects of salt stress on plants.

4.3  Chilling Stress The plants require optimum temperature to perform their functions and different processes normally and any deviations either increase (heat stress) or decrease (chilling stress) may impair the process of plant growth and development. When the temperature is too low for normal growth the chilling stress arises, although the temperature remains above the freezing point. The chilling injuries result in serious damages to plant and lead to yield losses (Taiz and Zeiger 2002). The production of ROS is commonly observed upon exposure to chilling stress in plants and these ROS including hydrogen peroxide, hydroxyl radicals, and superoxides cause peroxidation of membrane lipids (Prasad et al. 1994). The plants that are tolerant to chilling stress have an effective antioxidant system (Walker and Mc-Kersie 1993) and higher endogenous levels of polyamines (Guye et al. 1986). When the cucumber seedlings were subjected to chilling stress, the tolerant seedlings showed an increased Spd level and the increased Spd content was closely associated with a lower rate of ROS production; however, Put and Spm did not relate significantly to the chilling tolerance (Wang 1987; Shen et al. 2000). Furthermore, application of Spd prior to the onset of chilling stress prevents the generation of H2O2 in leaves and also enhances the activity of ROS scavenging enzymes (NADPH oxidases and NADPH-dependent superoxide) (Shen et al. 2000). Collectively, these reports suggested that Spd played a significant role in mitigating the chilling stress by preventing the production of ROS and promoting the activity of ROS scavenging enzymes. On the other hand, in Poplar seedlings the level of Put was increased just after the induction of chilling stress, whereas Spd and Spm accumulated after 4–7  days (Renaut et  al. 2005). Although, the increased Put levels declined later with the appearance of the reproductive stage in chilling exposed plants. In these plants, the endogenous Put reverted the damages (higher electrolyte leakage and lower the respiration rates) which was caused by chilling stress (Nayyar et al. 2005). Put was found primarily responsible for chilling tolerance in the bean, wheat, and rice (Guye et al. 1986; Nadeau et al. 1987; Lee et al. 1997). These reports and facts suggested that Spd and Spm may stabilize the macromolecules and detoxify the harmful ROS, whereas Put may reflect suboptimal growth conditions. The Put also served as useful marker to evaluate and identify the tolerant cultivars and genotypes under chilling stress conditions (Hausman et al. 2000; Larher et al. 2003).

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4.4  Oxidative Stress The disturbance in metabolic reactions, including respiration and photosynthesis, causes oxidative stress, the excessive production of ROS. These ROS interfere with normal plant processes and lead to impaired plant growth and development. The commencement of oxidative stress and subsequent ROS production elicit the accumulation of polyamines (Minocha et al. 2014). Almost all the abiotic stresses along with paraquat toxicity result into the production of ROS and the plants which were resistant to PQ toxicity showed an increased synthesis of polyamines (Ye et  al. 1997). Besides the endogenous PAs levels, the exogenous supply of polyamines is also promotive in improving the tolerance of plants to oxidative stress. Among the different types of polyamine, Spd is the most effective and most of the available literature is focused on the role of Spm under oxidative stress (Groppa et al. 2001). In rice, Spd revoked the cell membrane injury and impaired membrane associated H-ATPase activity caused by oxidative stress (Roy et  al. 2005). The findings of Kasukabe et al. (2004) suggested that Spd serves two major roles in plants, one as a stress signaling regulator and the other as a stress-protecting compound. Furthermore, in barley under water-deficit conditions, the exogenous application of Spd reduced the ROS content and subsequently helped in mitigating the oxidative stress (Kubis 2005). The combination of anion and cation binding properties facilitate the polyamines to act as a radical scavenger. This scavenging property of polyamines facilitates plants to overcome the lipid peroxidation and metal-catalyzed oxidative damages caused by ROS during oxidative stress (Wu et al. 2018). Along with this, in earlier sections of the chapter, it was mentioned that the breakdown of polyamines produces H2O2, which acts as a stress signaling molecule (Freitas et  al. 2017; Mellidou et al. 2017). The produced H2O2 also helps in activating an antioxidant defense system. Therefore, it can be concluded that polyamines act against the oxidative stress and reduce the lipid peroxidation, ROS generation, and also promote the expression of genes that are involved in defense.

4.5  Ultraviolet Radiations The increased anthropogenic activities are continuously raising the concern of the damaging effect of UV radiation on plant growth. Among the different types of UV radiation that exert negative effects, i.e., UV-A, UV-B, and UV-C, the most drastic effects are caused by UV-C. However, limited reports are available on the role of PAs in reversing the harmful effect of UV-C on plants (Ehsanpour and Razavizadeh 2005; Prochazkova and Wilhelmova 2007). The injuries caused by UV radiation have been categorized into two groups: physiological injuries and damages at the DNA level. It was reported that upon the exposure to UV radiation the Put content in fruit tissues of tobacco was initially increased (within 6  h), although it was decreased after 1–2  days, whereas Spd and Spm content remained unchanged

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(Gonzalez-Aguilar et al. 2004; Zacchini and de Agazio 2004). The UV-C irradiation caused severe damage to the cell membrane and also increased the endogenous polyamine contents (free, conjugated, and bound Spm, Spd, and Put) that helped in reducing the damages in Pea and tobacco leaves (Lutz et al. 2005; Katerova and Todorova 2009). Furthermore, the changes in endogenous PAs content due to treatment of UV irradiation have been reported in some other crops including cucumber (An et al. 2004), soybean (Kramer et al. 1992), and Phaseolus vulgaris (Smith et al. 2001). On the other hand, the exposure of P. Vulgaris to UV-B caused severe chlorophyll losses, while in cucumber irradiation caused reduced leaf area and reduction in shoot dry weight and plant height. In both P. Vulgaris and cucumber the damages were correlated with a decrease in total PAs content (Smith et al. 2001; An et al. 2004). However, prolonged exposure to UV rays declined PAs levels but along with that, it promoted the synthesis of other secondary metabolites like carotenoids and flavonoids.

4.6  Heavy Metals Toxicity In the environment, metals such as cadmium, copper, and chromium are increasing substantially due to increased anthropogenic and are detrimental to plant life cycle. These heavy metals enter in the biosphere as the waste product of industries such as chemical, metal processing, and mining and further enter in plant system where they cause severe damage by producing ROS (Ensley 2000; Fornazier et al. 2002). The plants also imitate defense mechanisms including synthesis of polyamines and other metabolites in response to metal toxicity and ROS (Tajti et al. 2018). The role of polyamines as membrane stabilizers and as free radical scavengers has already been well documented (Wang et al. 2004; Sharma and Dietz 2006). The heavy metals such as cadmium and copper are responsible for oxidative damage to wheat leaves by increasing the thiobarbituric acid (a reactive substance TBARS) while reducing the glutathione (antioxidant) and Spm content. Several reports indicated that the exogenous application of Spm to the affected wheat plants reduced the TBARS and H2O2 deposition in the leaves and helped in mitigating the harmful effect through the recovery of glutathione reductase (GR) and superoxide dismutase (SOD) activities (Groppa et al. 2007). Also, the negative effect of Cd+2 and Cu+2 on cell membrane in the form of lipid peroxidation can also be effectively mitigated by the application of polyamines (especially Spm) (Tajti et  al. 2018). Moreover, it was observed that cadmium toxicity led to an increase in the endogenous level of Put, whereas the level of Spd and Spm either remained constant or unchanged in oat and beans (Weinstein et  al. 1986). The increased Put content in Cd affected plant is attributed by enhance activity of enzymes such as ADC and ODC, however; in copper affected plants only ODC activity was responsible for increased Put content. Another reason for increased Put content in response to cadmium and copper toxicity was the reduction in the DAOs activity that is responsible for the degradation of Put and hence resulted in higher accumulation of Put (Groppa et al. 2003). Apart

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from this, the role of Spd in improving the cadmium toxicity by enhancing the activity of antioxidant enzymes in Typha latifolia was also well documented (Tang et al. 2005). These results suggested that polyamines exert antioxidative property in response to heavy metal toxicity and also help in protecting the tissues from the metal-induced oxidative damages.

4.7  Nutrients Deficiency Among the various nutrients, the deficiency of potassium (K) induced the endogenous level of Put in many crops including barley (Richards and Coleman 1952; Young and Galston 1984; Watson and Malmberg 1996) by maintaining a cation-­ anion balance. Upon the K deficiency, the activity of polyamine biosynthetic gene ADC was increased, while the levels of Spd and Spm remained unchanged in Arabidopsis. However, this increased ADC activity was not involved in the synthesis of mRNA and protein, indicating a post-translational regulation mechanism for ADC activation (Watson and Malmberg 1996). Furthermore, in grapes polyamines effectively modulate the K supply (Geny et al. 1987). Although, the role of polyamines in response to K as well as other nutrient deficiency remains unclear and more investigation is required to explore the possible mechanisms and role of polyamines under nutrient deficiency.

5  P  olyamines Mechanisms in Regulation of Different Stress Conditions Many studies indicated the role of polyamines and their involvement in various kinds of stress conditions. However, many biochemical compounds are synthesized in response to abiotic stresses, and how polyamines interact and co-ordinate with these compounds is still a question. In this section of the chapter, we will discuss the mechanisms and interactions of polyamines with other pathways and compounds under adverse climatic conditions.

5.1  Polyamines and ABA in Drought and Salt Stress Using Arabidopsis as a model plant, several studies provide an insight into the functional role of polyamines in the regulation of abiotic stresses (Ferrando et al. 2004; Alcázar et  al. 2006b; Kusano et  al. 2008; Takahashi and Kakehi 2009; Gill and Tuteja 2010). The whole genome sequencing of the Arabidopsis and the transcriptional responses allow to the study the biosynthetic pathways and their role under a particular type of stress. Along with that, the use of qRT-PCR facilitates transcript

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profiling which helps in revealing the expression patterns of genes, i.e., ADC2, SPDS1, and SPMS. The upregulation of these genes was reported in plants upon exposure to water-deficit conditions and ABA treatment (Perez-Amador et al. 2002; Urano et al. 2003; Alcázar et al. 2006a). Furthermore, to get detailed information on how ABA regulates the polyamine pathway, the expression of ADC2, SPDS1, and SPMS were accessed; mutants ABA-deficient (aba2-3) and ABA-insensitive (abi1-1) were subjected to water stress conditions. In water-deficit conditions these genes showed reduced transcriptional induction in mutants (aba2-3 and abi1-1), suggesting the role of ABA at the transcriptional level in controlling the polyamines metabolism by enhancing the expression of targeted genes (ADC2, SPDS1, and SPMS) (Alcázar et al. 2006a). Moreover, the accumulation of Put was also reduced in aba2-3 and abi1-1 mutants under water-limited conditions and these results were strengthened by metabolomic studies. It also indicated the similar responses of polyamines under water stress conditions in nced3 mutants (Urano et  al. 2009). Based on these reports, it could be concluded that under water stress conditions upregulation of polyamines biosynthetic genes is ABA-dependent. Similarly, the expression of ADC2 and SPMS was upregulated due to salt stress conditions and resulted in a subsequent enhancement in Put and Spm levels (Urano et al. 2003). The polyamine metabolism genes responses were also regulated by ABA since drought-responsive element (DRE), low temperature-responsive (LTR), and ABA-­ responsive elements (ABRE and/or ABRE-related motifs) were found in the promoter region of ADC2 and SPMS genes (Alcázar et al. 2006b).

5.2  T  he Interplay Between ABA, Polyamines, and ROS (H2O2), and NO in Stomata Regulation The ABA is a growth hormone that acts as anti-transpirant and also responsible for stomata closure upon exposure to water-limited conditions (Bray 1997). The ABA accumulation in guard cells leads to stomatal closure and the process involved several other components such as different ABA receptors, transcriptional factors, protein kinases, phosphatases, G-protein, reactive oxygen species (ROS), NO, and various secondary messengers (Kuppusamy et  al. 2009). The process of ABA-­ induced stomatal closure is regulated by polyamines; along with that, polyamines also control the ABA biosynthetic pathway under abiotic stress conditions (Liu et al. 2000; An et al. 2008). Besides this, the activity of either nitrate reductase (NR) or nitric oxide synthase (NOS) is responsible for the generation of NO from nitrite, which is an important signaling molecule for plant growth (Agurla et  al. 2017). Therefore, it suggests an important link among the ROS, polyamines, ABA-­ mediated stress responses, and NO (Yamasaki and Cohen 2006). During the catabolism of polyamines, the action of amine oxidase enzyme produces H2O2, and with that, polyamines also promote the synthesis of NO (Tun et al. 2006; Pál et al. 2015). However, the production of NO depends on H2O2 synthesis and together these both compounds regulate the ABA-controlled stomatal movement (Neill et al. 2008). On

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the other hand, the catabolism of Put and subsequent H2O2 production is induced by ABA through activating the DAOs enzymes during stomata closure (Freitas et al. 2017; Mellidou et al. 2017). In guard cell, Put and ABA collectively increase the Ca+2 levels that are impaired by DAOs inhibitors (An et al. 2008). This leads to a conclusion that the Ca+2 ions in guard cell control the effect of H2O2 from DAO-­ catalyzed Put oxidation. Concerning polyamines, Spd and Spm appear to induce the synthesis of NO, whereas Put either had a little or no effect on NO production (Tun et  al. 2006), indicating the role of NO as a potential intermediate of polyamine-­ mediated signaling (Parra-Lobato and Gomez-Jimenez 2011; Wimalasekera et al. 2011a, b; Hussain et al. 2011). However, the search for an enzyme that is responsible for direct conversion of polyamine to NO is still incomplete and it is believed that polyamine mediated stomata closure is regulated by signaling molecules (H2O2 and NO) via different paths (Yamasaki and Cohen 2006). In conclusion, the available literature indicated that polyamines, ROS (H2O2), and NO work altogether in mediating the ABA responses in guard cells. The ROS are produced upon exposure to abiotic stress conditions that are responsible for oxidative stress (Shi et  al. 2013b). Despite this, both CuAOs and PAOs mediated catabolism of polyamines produce H2O2, a by-product of catabolism (Alcázar et al. 2011; Tisi et al. 2011; Wimalasekera et al. 2011a, b; Moschou et al. 2012). Recently, the role of polyamine-derived H2O2 as a signaling molecule in various stress and developmental responses including programmed cell death (PCD) was demonstrated (Tisi et al. 2011; Moschou et al. 2012). Along with that, under water-limited conditions, ABA-regulated stomata closure is also controlled by polyamine derived H2O2 (Alcázar et al. 2011; Tisi et al. 2011; Moschou et al. 2012). However, the role of individual polyamines as an antioxidant by activating the peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT) has already been established by several previous researchers (Wang et al. 2011; Moschou et al. 2012; Tavladoraki et al. 2012; Shi et al. 2013b, c). Besides endogenous levels, the exogenous supply of polyamines enhances the activities of antioxidant enzymes under stress conditions and also reduced the H2O2 and O2• accumulation (Shi et al. 2013a). Furthermore, in this regard, physiological and proteomic analyses showed the involvement of polyamines-induced S-nitrosylation of target proteins and indicated the possibilities of a direct link between these proteins with polyamines in regulating the oxidative stress (Tanou et al. 2014).

5.3  Polyamines and Ion Channels At physiological concentration, polyamines are positively charged molecules which interact with the ion channels in a charge-dependent manner. The polyamines are involved in blocking the fast-activating vacuolar cation channel by electrostatic interaction at both single-channel and whole-cell level (Alcázar et al. 2010). Among the polyamines, Spd and Spm essentially regulate the activity of FV channel, whereas Put does not affect. As discussed in earlier headings, the nutrient deficiency

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(K) cause an increase in the endogenous level of Put, which probably reduce the activity of FV channels, while Spd and Spm remain unchanged. Besides this, salt stress also cause an accumulation of polyamines, especially, Spm levels and thus blocks the FV channel activity (Bruggemann et al. 1988). In barley, the exogenous supply of polyamines to root and epidermal cells restricts the Na+ influx and prevents loss of K+ ions and therefore improves the K+/Na+ homeostasis and tolerance to salt stress (Zhao et al. 2007). The polyamines also regulate the ion channel activity by binding with the channel as well as with associated proteins. Additionally, polyamines modulate the activity of plasma membrane and the tonoplast proton pumps by affecting the interaction between 14-3-3 proteins and H+-ATPase that cause inhibitory effect (Garufi et al. 2007; Rosales et al. 2012). These findings suggested that polyamines actively regulate the several ion channels as well as mediate the stomata closure via different signaling pathways at a certain concentration under abiotic stresses. For example, the micromolar concentrations of polyamines effectively block the influx of Na+ as well as efflux of K+ in pea mesophyll protoplasts and thus helps in adopting the salinity stress (Shabala et al. 2007). The activity of ion channels is controlled by the process of phosphorylation and de-­phosphorylation; the specific binding of polyamines to proteins present in cytoplasm and plasma membrane regulates these processes (Tassoni et  al. 1998, 2002). Therefore, it is concluded that polyamines also regulate the protein kinase and/or phosphatase activities that in turn control the activity of ion channels. Altogether, these studies suggested the direct cross talk between polyamines, ion channels, and stomatal movement under stress conditions and also indicated that polyamines serve as the messenger under abiotic stress conditions (Liu et al. 2000).

5.4  Cross Talk Between Polyamines and Ca+2 Calcium (Ca+2) is an essential ion for plant cell, act as a secondary messenger in various signaling pathways. Under stress conditions, phospholipase C (PLC) gets activated and hydrolysis of PIP2 to IP3 occurs that results in the release of Ca+2 from intracellular stores (Mahajan and Tuteja 2005). The increased cytosolic Ca+2 concentrations lead to the activation of ion channels and in turn, induce the stomatal closure (Blatt et al. 1990; Gilroy et al. 1990). Under stress conditions increased Put levels alter the phospho-inositol pools and enhance the drought tolerance, whereas Spm aids drought and salt tolerance in plants by altering the Ca+2 allocations through regulating Ca+2-permeable channels (Yamaguchi et al. 2006, 2007). In addition, the enhanced cytoplasmic Ca+2 concentrations prevent the influx of Na+/K+ into the cell to increase the influx of Na+/K+ into the vacuole. This regulatory mechanism increases plant tolerance to salt stress (Yamaguchi et al. 2006; Kusano et al. 2007). All these reports suggested existence of a link among stress conditions, polyamines, and Ca+2 homeostasis.

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6  U  tilization of Mutants and in Response to Stress Conditions The mutants are widely used in plant biology to study the role of genes and their particular functions. Concerning polyamines, many mutants which lack in PAs biosynthesis have been identified and these mutants provide sufficient evidence regarding the implication of polyamines in stress tolerance. In this regard, two EMS mutants, i.e., spe-1 and spe-2, of Arabidopsis have been isolated and these showed deficit in ADC activity (Watson et al. 1998). The salt stress led to an accumulation of polyamines in wild types, whereas both mutants, i.e., spe-1 and spe-2, were unable to accumulate polyamines and mutants affected by severe salt injuries, including reduced fresh weight, decreased chlorophyll content, as well as declined photosynthetic rates. Similar to this, the Arabidopsis mutant adc2-1 showed that Put biosynthesis is controlled by gene At-adc2 under stress conditions. Under stress conditions, the Put content was reduced by 25% in adc2-1 mutant in comparison to control plants, although Spd and Spm content remained unaffected (Urano et  al. 2004). Together, these findings suggested that the activity of the ADC gene and level of Put both are crucial for plants to tolerate salt stress. Recently, the PCR-­ based mutant screening techniques have been adopted for the identification of knockouts in gene of interest. It makes mutants more feasible, developed through transposons (Ferrando et al. 2004). Using this technique, a mutant was developed in Arabidopsis, which carry an insertion of En-1 transposable element at the ADC2 locus (Soyka and Heyer 1999). Thereby, from the above reports, it can be concluded that manipulation at genetic level (such as mutant development) especially in the polyamines pathway is helpful to discriminate the role of polyamines in plant responses under abiotic stresses.

7  O  ver-Expression and Engineering of Polyamines Biosynthetic Genes Under Abiotic Stresses The harsh environmental conditions lead to an accumulation of polyamines that imparts the tolerance against abiotic stresses (Ahmad et al. 2012). At the cellular level, biosynthesis of PAs is a complex process and in which several genes and their encoded enzymes are involved. Cloning and characterization of these genes, particularly under stress conditions, could be useful to get the insight of their implication in stress response. The various environmental alterations not only bring the changes at physiological and biochemical levels but also cause changes at transcriptional levels. The available studies suggested that different abiotic stresses modulate the expression of genes that code for functional and regulatory proteins. The ADC gene was first characterized by Bell and Malmberg (1990) in oat and over-­expression of this gene under different abiotic stress revealed the presence of complicated transcriptional profile. The mRNA levels of some polyamine biosynthetic genes were

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upregulated rapidly just after exposure to stress conditions, while some of those were induced only when stress was subjected for a certain period. It indicates that expression and upregulation of polyamine biosynthetic genes are disparately regulated during stress and it depends on various other factors like intensity, duration of stress and plant species (Li and Chen 2000; Hao et al. 2005a, b; Liu et al. 2006). Several genes like ADC, ODC, SAMDC, or SPDS were cloned successfully and genetic manipulation in these genes provided an opportunity to improve the plant tolerance under drought stress conditions (Kakkar and Sawhney 2002; Panicot et al. 2002). Also, several reports are available on transgenic development, using manipulated PAs biosynthetic genes. Two genes ADC and ODC code for key enzymes that are involved in Put biosynthesis and over-expression of these genes enhances plant tolerance to abiotic stresses. In this regard, an ADC gene from oats was introduced in rice under an ABA-inducible promoter and it resulted in a higher level of polyamines and subsequent salt tolerance compared to wild types. Although, Roy and Wu (2001) showed that constitutive expression of this gene limits the development of transgenic plants. To eliminate the effect of impaired growth in transgenics, gene transfer under the control of stress-inducible promoters is an effective approach to improve plant tolerance. In this direction, under the control of a stress-inducible promoter over-expression of cDNA of oat ADC gene in rice plant led to enhanced Put level and subsequent salt tolerance (Roy and Wu 2001). In another example, expressions of the ADC gene from the Datura plant enhanced the level of Put that in turn increased the water stress tolerance in transgenic rice (Capell et  al. 2004). Furthermore, over-expression of the SAMDC gene (involved in Spd and Spm biosynthesis) increases the level of SAM decarboxylase that enhances plant tolerances to abiotic stresses. Apart from polyamines biosynthetic genes, the silencing of ACC synthase and ACC oxidase (responsible for ethylene biosynthesis) genes along with the concomitant increase in Put and Spd ensured higher tolerance to abiotic stresses (Tavladoraki et  al. 2012). Similarly, modification in arginase (an enzyme of N-metabolism) leads to an alteration in Put and Spm levels and it also aids tolerance in plants under adverse environmental conditions (Shi et al. 2013b). Furthermore, introgression of antisense ACC synthase or ACC oxidase genes from carnation to tobacco led to enhanced SAMDC activity along with higher levels of polyamines (Put and Spd) that ultimately conferred the tolerance against salt and oxidative stress (Wi and Park 2002). The researchers also observed that even the introduction of a single gene also increased the tolerance in plants from abiotic stresses. Following this, a SPDS gene from Cucurbita ficifolia to A. thaliana and sweet potato increased the endogenous content of polyamines by 1.6- to 1.8-folds that promote plant tolerance to chilling, drought, salinity, osmosis, freezing, and PQ (Kasukabe et al. 2004, 2006). Therefore, the introduction and over-expression of genes involved in polyamine biosynthesis is an effective approach towards conferring the stress tolerance in plants under changing climatic conditions. Besides this, allelic variation within a species as well as among the species also caused variation in gene expression (differential gene expression) and several reports are available in this regard (Guo et al. 2004; Wang et al. 2011). The differential expression of genes due to environmental conditions leads to variability at the

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nucleotide level that further results in altered gene expression. For example, heterologous expression of genes, i.e., DsAdoMetDC and DsAdc, from Datura stramonium to rice improves the drought tolerance compared to plant having endogenous AdoMetDC and Adc gene (Capell et al. 2004; Peremarti et al. 2009). It showed that variation within the gene sequence controls the level of expression; therefore, the enhancement in the activity and efficiency of the enzyme involved in the biosynthesis of polyamines is possible. Thereby, identification of a suitable variant that can act as a donor through both genetic engineering and molecular breeding methods is of prime importance to improve stress tolerance in targeted plants. With the availability of knowledge from molecular-genetic studies (loss or gain of function mutants) and over-expression studies, it is now possible to use biotechnological approaches to facilitate the screening and identification of natural variants among the different species. Moreover, the inclusion of metabolite profiling using GC-MS, LC-MS, techniques provide knowledge on the complete status of metabolites and also helpful in deciphering the function of genes (Obata and Fernie 2012). Concurrently, genomics tools such as SNPs assay and expression profiling can also elaborate on a relationship between polyamine genes associated with abiotic stress tolerance and metabolomics (Fig. 1).

8  Use of Inhibitors and Stress Response The inhibitors are generally used to inhibit the different steps of biosynthetic pathways and allow the elucidation of different reactions that are involved in synthesis and catabolism of polyamines. Under stress conditions, it is important to understand the mechanism of plant-cell homeostasis (Galston et  al. 1997). Many potential chemical inhibitors were identified and used by investigators to recognize the role of PAs in plant processes as well as their role in modulating the levels of PAs under both optimum and stress conditions (Kaur-Sawhney et  al. 2003). The inhibitors, viz., difluoromethylarginine (DFMA) and difluoromethylornithine (DFMO), are reversible inhibitors of ADC and ODC, respectively, and involved in inhibition of PAs biosynthesis (Grossi et al. 2016; Yamamoto et al. 2016). Along with that, the activity of SAMDC is inhibited by methylglyoxyl-bis guanylhydrazone (MGBG) (Williams-Ashman and Schenone 1972), whereas 1, 4-diamino-butanone (1, 4-DB) and cyclohexylamine (CHA) are potent inhibitors of Put and SPDS (Hibasami et al. 1980). Furthermore, d-arginine inhibits PA biosynthesis and aminoguanidine (AG) acts as an inhibitor for DAOs (Kaur-Sawhney et al. 2003). The application of these inhibitors effectively reduces the plant tolerance to stress conditions; however, this effect can be reversed by a concomitant exogenous supply of PAs (He et al. 2002; Hussain et  al. 2011). For example, the application of DFMA restricts the ADC activity and leads to ozone injuries to barley leaves (Rowland-Bamford et al. 1989). Similar to this, treatment with 1, 4-diaminobutanone (Put inhibitor) decrease the

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Fig. 1 (a) Polyamine biosynthesis in plants. ADC Arginine decarboxylase, AIH Agmatine iminohydrolase, CPA N-carbamoyl putrescine amidohydrolase, SPDS Spermidine synthase, SPMS Spermine synthase, dc SAM decarboxylated S-adenosyl methionine, SAM S-adenosyl methionine, SAMDC S-adenosyl methionine decarboxylase, ODC ornithine decarboxylase. (b) Polyamine degradation pathway. DAO Diamine oxidase, PAO Polyamine oxidase

tolerance of tobacco plants to ozone although, the effects of these inhibitors are variable and depend upon applied dosage of polyamines. Collectively the effect of these inhibitors on polyamines and in reducing the plant tolerance to stress conditions suggested the key role of PAs in abiotic stresses.

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9  Conclusions In the current scenario, PAs are considered as a new group of phyto-hormones. The significant role of polyamines in cell growth and functions are highlighted in many crops. Besides their important biological role in plant growth and development, polyamines are also imparted in plant tolerance under various kinds of environmental stress conditions. The genetic manipulation of the polyamine biosynthetic genes, as well as genes involved in the metabolism of polyamines, is proved to be a promising approach for the development of transgenics that are tolerant to abiotic stresses. Although, cross talk with other growth hormones and implication of polyamines in the stress signaling pathways are still under investigation. Along with that, downstream components of polyamines upon exposure to stress conditions are also still unknown. The omics approaches are proved to be useful in many crops and the application of these approaches opens a new window in revealing the polyamine-­ related signaling pathway and downstream targets.

References Agudelo-Romero P, Bortolloti C, Pais MS, Al E (2013) Study of polyamines during grape ripening indicates an important role of polyamine catabolism. Plant Physiol Biochem 67:105–119 Agurla S, Gayatri G, Raghavendra AS (2017) Polyamines increase nitric oxide and reactive oxygen species in guard cells of Arabidopsis thaliana during stomatal closure. Protoplasma 255:153–162 Ahmad P, Kumar A, Gupta A, Hu X, Azooz MM, Sharma S (2012) Polyamines: role in plants under abiotic stress. In: Crop production for agricultural improvement. Springer, Dordrecht, pp 491–512 Alcázar R, Garcia-Martinez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2  in Arabidopsis induces dwarfism and late–flowering drought GA deficiency. Plant J 43:425–436 Alcázar R, Cuevas JC, Patrón M, Altabella T, Tiburcio AF (2006a) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455 Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006b) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876 Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231(6):1237–1249 Alcázar R, Bitrián M, Bartels D, Koncz C, Altabella T, Tiburcio AF (2011) Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signal Behav 6(2):243–250 Alet AI, Sánchez DH, Cuevas JC, Marina M, Carrasco P, Altabella T, Tiburcio AF, Ruiz OA (2012) New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Science 182:94–100 An LZ, Liu GX, Zhang MX, Chen T, Liu YH, Feng HY, Xu SJ, Qiang WY, Wang XL (2004) Effect of enhanced UV-B radiation on polyamine content and membrane permeability in cucumber leaves. Russ J Plant Physiol 51:658–662 An ZF, Jing W, Liu YL, Zhang WH (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Viciafaba. J Exp Bot 59:815–825

190

B. B. Pandey et al.

Antognoni F, Fornale S, Grimmer C, Komor E, Bagni N (1998) Long-distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants. Planta 204:5207 Bagni N, Pistocchi R (1991) Uptake and transport of polyamine and inhibitors of polyamine metabolism in plants. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants. CRC Press, Inc., Boca Raton, p 10520 Baniasadi F, Saffari VR, Moud AAM (2018) Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress. Sci Hortic 234:312–317 Bell E, Malmberg RT (1990) Analysis of a cDNA encoding arginine decarboxylase from oat reveals similarity to the Escherichia coli arginine decarboxylase and evidence of protein processing. Mol Gen Genet 224:431–436 Blatt MR, Thiel G, Trentham DR (1990) Reversible inactivation of K+ channels of Viciastomatal guard-cells following the photolysis of caged Inositol 1,4,5-trisphosphate. Nature 346:766–769 Borrell A, Culianez-Macia FA, Altabella T, Besford RT, Flores D, Tiburcio AF (1995) Arginine decarboxylase is localized in chloroplasts. Plant Physiol 109:771–776 Bors W, Langebartels C, Michel C, Sandermann H (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28:1589–1595 Bortolotti C, Cordeiro A, Alcazar R, Borrell A, Culiañez-Macià FA, Tiburcio AF, Altabella T (2004) Localization of arginine decarboxylase in tobacco plants. Physiol Plant 120:84–92 Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54 Brieger L (1885) Ueber Spaltungsprodukte der Bacterien, Zweite Mittheilung. Zeitschr Physiol Chem 9:1–7 Bruggemann IL, Pottosin II, Schonknech G (1988) Cytoplasmic polyamines block the fast-­ activating vacuolar cation channel. Plant J 16:10–15 Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci U S A 101(26):9909–9914 Chattopadhayay MK, Tiwari BS, Chattopadhayay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:19–29 Cohen SS (1998) Guide to the polyamines. Oxford University Press, New York Coleman RG, Hegartv MP (1957) Metabolism of dl-ornithine-2-14C in normal and potassium-­ deficient barley. Nature 179(4555):376–377 Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88 Davies PJ (2004) The plant hormones: their nature, occurrence and function. In: Davies PJ (ed) Plant hormones, biosynthesis, signal transduction, action. Kluwer, Dordrecht, p 115 De Oliveira LF, Elbl P, Navarro BV, Al E (2016) Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiol 37:116–130 De Oliveira LF, Navarro BV, Cerruti G, Al E (2018) Polyamines and amino acid related metabolism: the roles of arginine and ornithine are associated with the embryogenic potential. Plant Cell Physiol 59:1084–1098 Deotale RD, Pandey BB (2018) An evaluation of the potentiality of exogenously applied putrescine and IBA on biochemical and yield contributing parameters of maize. Journal of soils and crops 27(2):47–53 Docimo T, Reichelt M, Schneider B, Al E (2012) The first step in the biosynthesis of cocaine in Erythroxylum coca: the characterization of arginine and ornithine decarboxylases. Plant Mol Biol 78:599–615 Ebeed HT, Hassan NM, Aljarani AM (2017) Exogenous applications of Polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes. Plant Physiol Biochem 118:438–448 Ehsanpour AA, Razavizadeh R (2005) Effect of UV-C on drought tolerance of alfalfa (Medicago sativa) callus. Am J Biochem Biotechnol 1:107110 Ensley BD (2000) Rational for use of phytoremediation. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. Wiley, New York, p 312

Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental… 191 FAO (2009) High level expert forum-how to feed the world in 2050. Economic and social development. Food and Agricultural Organization of the United Nations, Rome Fellenberg C, Bottcher C, Vogt T (2009) Phenylpropanoid polyamine conjugate biosynthesis in Arabidopsis thaliana flower buds. Phytochemistry 70:1392–1400 Feng W, Ji P (2011) Enzymes immobilized on carbon nanotubes. Biotechnology advances 29(6):889–895 Feray A, Hourmant A, Beraud J, Braun A, Cann-moisan CJ, Penot M (1991) Influence of polyamines on the long distance transport of K (86Rb) in potato cuttings (Solanum tuberosum cv. Sirtema)-comparative study with some phytohormones. J Exp Bot 43:4038 Ferrando A, Carrasco P, Cuevas JC, Altabella T, Tiburcio AF (2004) Integrated molecular analysis of the polyamine pathway in abiotic stress signaling. In: Amancio S, Stulen I (eds) Nitrogen acquisition and assimilation in higher plants. Kluwer Academic Publishers, London, pp 207–230 Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis KA, Tavladoraki P (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. Journal of Experimental Botany 62(3):1155–1168 Fornazier RF, Ferreira RR, Pereira GJG, Molina SMG, Smith RJ (2002) Cadmium stress in sugar cane callus cultures: effect on antioxidant enzymes. Plant Cell Tissue Org Cult 71:125–131 Freitas VS, Miranda RDS, Costa JH, Al E (2017) Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ Exp Bot 145:75–86 Friedman R, Levin N, Altman A (1986) Presence and identification of polyamines in xylem and phloem exudates of plants. Plant Physiol 86:11547 Galston AW (1991) On the trail of a new regulatory system in plants. Polyomines as modulators of plant development: sponsored by Fundación Juan March, Madrid, Spain. New Biol 3(5):450–453 Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF (1997) Plant polyamines in reproductive activity and response to abiotic stress. Bot Acta 110:197–207 Garufi A, Visconti S, Camoni L, Aducci P (2007) Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. Plant and cell physiology 48(3):434–440 Geny L, Broquedis M, Soyer JP, Bouard J (1987) Effect of potassium nutrition on polyamine content of various organs of fruiting cuttings of Vitis vinifera L. cv. Cabernet Sanvignon. Am J Enol Vitic 48:85–92 Gholami M, Fakhari AR, Ghanati F (2013) Selective regulation of nicotine and polyamines biosynthesis in tobacco cells by enantiomers of ornithine. Chirality 25:22–27 Ghosh B (2000) Polyamines and plant alkaloids. Indian J Exp Biol 38:10 Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant signaling & behavior 5(1):26–33 Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346:769–771 Gonzalez-Aguilar G, Wang CY, Buta GJ (2004) UV-C irradiation reduces breakdown and chilling injury of peaches during cold storage. J Sci Food Agri 84:415–422 Grienenberger E, Besseau S, Geoffroy P, Debayle D, Heintz D, Lapierre C, Pollet B, Heitz T, Legrand M (2009) A BAHD acyl-transferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoylspermidines. Plant J 58:246–259 Groppa MD, Tomaro ML, Benavides MP (2001) Polyamines as protectors against cadmium or copper induced oxidative damage in sunflower leaf discs. Plant Sci 161:4818 Groppa MD, Benavides MP, Tomaro ML (2003) Polyamine metabolism in sunflower and wheat leaf discs under cadmium and copper stress. Plant Science 164:293–299 Groppa MD, Maria L, Tomaro ML, Benavides MP (2007) Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium and copper-treated wheat leaves. BioMetals 20:185–195

192

B. B. Pandey et al.

Grossi M, Phanstiel O, Rippe C, Al E (2016) Inhibition of polyamine uptake potentiates the anti-­ proliferative effect of polyamine synthesis inhibition and preserves the contractile phenotype of vascular smooth muscle cells. J. Cell. Physiol. 231:1334–1342 Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. The Plant Cell 16(7):1707–1716 Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annual review of plant biology 41(1):187–223 Guye MG, Vigh L, Wilson JM (1986) Polyamine titers in relation to chilling sensitivity in Phaseolus sp. J Exp Bot 37:1036–1043 Hao YJ, Kitashiba H, Honda C, Nada K, Moriguchi T (2005a) Expression of arginine decarboxylase and ornithine decarboxylase genes in apple cells and stressed shoots. J Exp Bot 56:1105–1115 Hao YJ, Zhang Z, Kitashiba H, Honda C, Ubi B, Kita M, Moriguchi T (2005b) Molecular cloning and functional characterization of two apple S-adenosylmethionine decarboxylase genes and their different involvement in fruit development, cell growth, and stress responses. Gene 350:41–50 Hao Y, Huang B, Jia D, Al E (2018) Identification of seven polyamine oxidase genes in tomato (Solanum lycopersicum L.) and their expression profiles under physiological and various stress conditions. J Plant Physiol 228:1–11 Hausman JF, Evers D, Thiellement H, Jouve L (2000) Compared responses of poplar cuttings and in vitro raised shoots to short-term chilling treatments. Plant Cell Rep 19:954–960 He L, Nada K, Kasukabe Y, Tachibana S (2002) Enhanced susceptibility of photosynthesis to low temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of spinach (Spinacia oleracea L.). Plant Cell Physiol 43:196–206 Hibasami H, Tanaka M, Nagai J, Ikeda T (1980) Dicyclohexylamine, a potent inhibitor of spermidine synthase in mammalian cells. FEBS Lett 116:99–101 Hummel I, Gouesbet G, El Amrani A, Aïnouche A, Couée I (2004) Characterization of the two arginine decarboxylase (polyamine biosynthesis) paralogues of the endemic subantarctic cruciferous species Pringlea antiscorbutica and analysis of their differential expression during development and response to environmental stress. Gene 342(2):199–209 Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311 Igarashi K, Kashiwagi K (2015) Modulation of protein synthesis by polyamines. IUBMB Life 67:160–169 Illingworth C, Mayer MJ, Elliott K, Hanfrey C, Walton NJ, Michale AJ (2003) The diverse bacterial origins of the Arabidopsis polyamine biosynthetic pathway. FEBS Lett 549:26–30 Imanishi S, Hashizume K, Nakakita M, Kojima H, Matsubayashi Y, Hashimoto T, Sakagami Y, Yamada Y, Nakamura K (1998) Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures. Plant Mol Biol 38:1101–1111 Kakkar RK, Sawhney VK (2002) Polyamine research in plants a changing perspective. Physiol Plant 116:281–292 Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Over-expression of spermidine synthase enhances tolerance to multiple environmental stresses and upregulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722 Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83 Katerova ZI, Todorova D (2009) Endogenous polyamines lessen membrane damages in pea plants provoked by enhanced ultraviolet-C radiation. Plant Growth Regul 57:145–152 Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW (2003) Polyamines in plants: an overview. Journal of Cellular and Molecular Biology 2(1):1–12

Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental… 193 Kim DW, Watanabe K, Murayama C, Al E (2014) Polyamine oxidase regulates Arabidopsis growth through thermospermine oxidase activity. Plant Physiol 165:1575–1590 Königshofer H, Lechner S (2002) Are polyamines involved in the synthesis of heat-shock proteins in cell suspension cultures of tobacco and alfalfa in response to high-temperature stress? Plant Physiol Biochem 40:51–59 Kramer G, Krizek D, Mirecki R (1992) Influence of photosynthetically active radiation and spectral quality on UV-B induced polyamine accumulation in soybean. Phytochemistry 31:1119–1125 Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91:500–504 Kubis J (2005) The effect of exogenous spermidine on superoxide dismutase activity, H2O2 and superoxide radical level in barley leaves under water deficit conditions. Acta Physiol Plant 27:289–295 Kuppusamy K, Walcher C, Nemhauser J (2009) Cross-regulatory mechanisms in hormone signaling. Plant Mol Biol 69:375–381 Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav 2:251–252 Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228(3):367–381 Larher FR, Aziz A, Gibon Y, Trotel-Aziz P, Sulpice R, Bouchereau A (2003) An assessment of the physiological properties of the so-called compatible solutes using in  vitro experiments with leaf discs. Plant Physiol Biochem 41:657–666 Lee TM, Lur HS, Chu C (1997) Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings. 2. Modulation of free polyamine levels. Plant Sci 126:1–10 Lefevre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Science 161:943–952 Legocka J, Kluk A (2005) Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinusluteus seedlings. J Plant Physiol 162:662–668 Li ZY, Chen SY (2000) Isolation and characterization of a salt and drought-inducible gene for S-adenosylmethionine decarboxylase from wheat (Triticum aestivum L.). J Plant Physiol 156:386–393 Li Y, He J (2012) Advance in metabolism and response to stress of polyamines in plant. Acta Agric Boreali Sin 27:240–245 Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326 Liu HP, Dong BH, Zhang YY, Liu ZP, Liu YL (2004) Relationship between osmotic stress and the levels of free, conjugated, and bound polyamines in leaves of wheat seedlings. Plant Sci 166:1261–1267 Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599 Liu T, Kim DW, Niitsu M, Berberich T, Kusano T (2014) Oryza sativa polyamine oxidase back-­converts tetra amines, spermine and thermospermine, to spermidine. Plant Cell Rep 33(1):143–151 Liu Q, Nishibori N, Imai I, Al E (2016) Response of polyamine pools in marine phytoplankton to nutrient limitation and variation in temperature and salinity. Mar. Ecol. Prog 544:93–105 Liu W, Tan M, Zhang C, Al E (2017) Functional characterization of murB-potABCD operon for polyamine uptake and peptidoglycan synthesis in Streptococcus suis. Microbiol Res 207:177–187 Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620 Luo J, Fuell C, Parr A, Hill L, Bailey P, Elliott K, Fairhurst SA, Martin C, Michael AJ (2009) A novel polyamine acyl-transferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21:318–333

194

B. B. Pandey et al.

Lutz C, Navakoudis E, Seidlitz HK, Kotzabasis K (2005) Simulated solar irradiation with enhanced UV-B adjusts plastid and thylakoid-associated polyamine changes for UV-B protection. Biochem Biophys Acta 1710:24–33 Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158 Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34:13548 Mellidou I, Karamanoli K, Beris D, Al E (2017) Under expression of apoplastic polyamine oxidase improves thermotolerance in Nicotiana tabacum. J. Plant Physiol 218:171–174 Meng D, Hou L, Yang S (2015) Exogenous polyamines alleviating salt stress on peanuts (Arachis hypogaea) grown in pots. Chin J Plant Ecol 39:1209–1215 Michael AJ, Furze JM, Rhodes MC, Burtin D (1996) Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA. Biochem J 314:241–248 Minguet EG, VeraSirera F, Marina A, Carbonell J, Blazquez MA (2008) Evolutionary diversification in polyamine biosynthesis. Mol Biol Evol 25:2119–2128 Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175 Mohammadi H, Ghorbanpour M, Brestic M (2018) Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind Crops Prod 122:119–132 Moller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis ATAO1 gene encoding an H2O2 generating diamine oxidase. Plant J 13:781–791 Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20(6):1708–1724 Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. Journal of experimental botany 63(14):5003–5015 Mulangi V, Phuntumart V, Aouida M, Ramotar D, Morris P (2012a) Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235(1):1–11 Mulangi V, Chibucos MC, Phuntumart V, Morris PF (2012b) Kinetic and phylogenetic analysis of plant polyamine uptake transporters. Planta 236(4):1261–1273 Mustafavi SH, Badi HN, Sekara A, Al E (2018) Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiol Plant 40:102 Nadeau P, Delaney S, Chouinard L (1987) Effect of cold hardening on the regulation of polyamine levels in wheat (Triticum aestivum L.) and alfalfa (Medicago sativa L.). Plant Physiol 84:737 Nahar K, Hasanuzzaman M, Rahman A, Al E (2016) Polyamines confer salt tolerance in Mung Bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Front. Plant Sci 7:1104 Navakoudis E, Lutz C, Langerbartels C, Lutz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochim Biophys Acta 1621:160–169 Nayyar H, Kaur S, Singh S, Kumar S, Singh KJ, Dhir KK (2005) Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max (L) Merrill) to water deficit stress. Bot Bull Acad Sin 46:33–38 Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176 Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences 69(19):3225–3243 Ono Y, Kim DW, Watanabe K, Sasaki A, Niitsu M, Berberich T, Kusano T, Takahashi Y (2012) Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino acids 42(2–3):867–876

Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental… 195 Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23 Pandey S, Ranade SA, Nagar PK, Kumar N (2000) Role of polyamines and ethylene as modulators of plant senescence. J Biosci 25:291–299 Pandey BB, Deotale RD, Jayabhaye VR, Chinmalwar YA, Suryawanshi VJ, Davhale PN (2017) Morpho-physiological and yield responses of maize plant to foliar spray of polyamines (Putrescine) and IBA. Journal of soils and crops 27(1):114–119 Panicot M, Masgrau C, Borrell A, Cordeiro A, Tiburcio AF, Altabella T (2002) Effects of putrescine accumulation in tobacco transgenic plants with different expression of oat arginine decarboxylases. Physiol Plant 114:2817 Parra-Lobato MC, Gomez-Jimenez MC (2011) Polyamine-induced modulation of genes involved in ethylene biosynthesis and signalling pathways and nitric oxide production during olive mature fruit abscission. J Exp Bot 62:4447–4465 Pegg AE (2016) Functions of polyamines in mammals. J Biol Chem 291:14904–14912 Peremarti A, Bassie L, Christou P, Capell T (2009) Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant molecular biology 70(3):253–264 Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiology 130:1454–1463 Phillips GC, Kuehn GD (1991) Uncommon polyamines in plants and other organisms. In: Biochemistry and physiology of the polyamines in plants, vol 20. CRC Press, Boca Raton, pp 121–136 Pistocchi R, Keller F, Bagni N, Matile P (1988) Transport and subcellular localization of polyamines in carrot protoplasts and vacuoles. Plant Physiol. 87:5148 Pistocchi R, Antognoni F, Bagni N, Zannoni D (1990) Spermidine uptake by mitochondria of Helianthus tuberosus. Plant Physiol 92:6905 Prasad TK, Anderson MD, Stewart CR (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol 105:619–627 Prochazkova D, Wilhelmova N (2007) The capacity of antioxidant protection during modulated ageing of bean (Phaseolus vulgaris L.) cotyledon: the antioxidant enzyme activities. Cell Biochem Funct 25:87–95 Rea G, de Pinto MC, Tavazza R, Biondi S, Gobbi V, Ferrante P, DeGara L, Federico R, Angelini R, Tavladoraki P (2004) Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant Physiology 134(4):1414–1426 Regla-Márquez CF, Canto-Flick A, Avilés-Viñas SA, Al E (2015) Cadaverine: a common polyamine in zygotic embryos and somatic embryos of the species Capsicum chinense Jacq. PCTOC 124:253–264 Reis RS, Vale EM, Heringer AS, Al E (2016) Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. J Proteomics 130:170–179 Renaut J, Hoffmann L, Hausman JF (2005) Biochemical and physiological mechanisms related to cold acclimation and enhanced freezing tolerance in poplar plantlets. Physiol Plant 125:82–94 Richards FJ, Coleman RG (1952) Occurrence of putrescine in potassium-deficient barley. Nature 170(4324):460 Rosales EP, Iannone MF, Groppa MD, Benavides MP (2012) Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide. Amino Acids 42:857–865 Rowland-Bamford AJ, Borland AM, Lea PJ, Mansfield TA (1989) The role of arginine decarboxylase in modulations the sensitivity of barley to ozone. Environ Pollut 61:95–106 Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875

196

B. B. Pandey et al.

Roy P, Niyogi K, SenGupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci 168:583–591 Sánchezrodríguez E, Romero L, Ruiz JM (2016) Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress. J Plant Physiol 190:72–78 Santa-Cruz A, Estañ MT, Rus A, Bolarin MC, Acosta M (1997) Effects of NaCl and mannitol iso-­ osmotic stresses on the free polyamine levels in leaf discs of tomato species differing in salt tolerance. J Plant Physiol 151:754–758 Sequeramutiozabal MI, Erban A, Kopka J, Al E (2016) Global metabolic profiling of Arabidopsis polyamine oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence. Front Plant Sci 7:173 Serafini-Fracassini D, Del Duca S (2008) Transglutaminases: widespread cross-linking enzymes in plants. Ann Bot 102:145–152 Serafini-Fracassini D, Del Duca S, Beninati S (1995) Plant transglutaminases. Phytochemistry 40:355–365 Sfakianaki M, Sfichi L, Kotzabasis K (2006) The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature. J Photochem Photobiol B Biol 84:1818 Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999 Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726 Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:4319 Shevyakova NI, Rakitin VY, Duong DB, Sadomov NG, Kuznetsov VV (2001) Heat shock-induced cadaverine accumulation and translocation throughout the plant. Plant Science 161:1125–1133 Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. Journal of Integrative Plant Biology 56(2):114–121 Shi YJ, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953 Shi H, Ye T, Chan Z (2013a) Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the bermudagrass (Cynodon dactylon) response to salt and drought stresses. Journal of Proteome Research 12(11):4951–4964 Shi H, Ye T, Chen F, Cheng Z, Wang Y, Yang P, Zhang Y, Chan Z (2013b) Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation. J Exp Bot 64:1367–1379 Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2013c) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922 Smith TA (1985) Polyamines. Annu Rev Plant Physiol 36:11743 Smith TA, Richards FJ (1962) The biosynthesis of putrescine in higher plants and its relation to potassium nutrition. The Biochemical Journal 84:292–294 Smith J, Burrit D, Bannister P (2001) Ultraviolet-B radiation leads to a reduction in free polyamines in Phaseolus vulgaris L. Plant Growth Regul 35:289–294 Sobieszczuk-Nowicka E (2017) Polyamine catabolism adds fuel to leaf senescence. Amino Acids 49:49–56 Soyka S, Heyer AG (1999) Arabidopsis knockout mutation of ADC2 gene reveals inducibility by osmotic stress. FEBS Lett 458:219–223 Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. Journal of Integrative Plant Biology 48(4):426–432

Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental… 197 Tabor H, Rosenthal SM, Tabor CW (1958) The biosynthesis of spermidine and spermine from putrescine and methionine. The Journal of Biological Chemistry 233:907–914 Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinauer Associates, Inc., Publishers, Sunderland Tajti J, Janda T, Majláth I, Szalai G, Pál M (2018) Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicol Environ Safety 148:546–554 Takahashi T, Kakehi JI (2009) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6 Takahashi Y, Ono K, Akamine Y, Asano T, Ezaki M, Mouri I (2017a) Highly-expressed polyamine oxidases catalyze polyamine back conversion in Brachypodium distachyon. J Plant Res 131:341–348 Takahashi Y, Tahara M, Yamada Y, Al E (2017b) Characterization of the polyamine biosynthetic pathways and salt stress response in Brachypodium distachyon. J Plant Growth Regul 37:625–634 Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:3143 Tang CF, Liu YG, Zeng GM, Li X, Xu WH, Li CF, Yuan XZ (2005) Effects of exogenous spermidine on antioxidant system responses of Typha latifolia L. under Cd stress. J Integr Plant Biol 47:428–434 Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Fotopoulos V, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37(4):864–885 Tassoni A, Antognoni F, Battistini ML, Sanvido O, Bagni N (1998) Characterization of spermidine binding to solubilized plasma membrane proteins from zucchini hypocotyls. Plant Physiol 117:971–977 Tassoni A, Napier RM, Franceschetti M, Venis MA, Bagni N (2002) Spermidine-binding proteins: purification and expression analysis in maize. Plant Physiol 128:1303–1312 Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Agostinelli E (2012) Polyamine catabolism: target for anti-proliferative therapies in animals and stress tolerance strategies in plants. Amino acids 42(2–3):411–426 Tiburcio AF, Kaur-Sawhney R, Galston AW (1990) Polyamine metabolism. In: Stumpf PK, Conn EE (eds) The biochemistry of plants. Academic, New York, pp 283–235 Tisi A, Federico R, Moreno S, Lucretti S, Moschou PN, Roubelakis-Angelakis KA (2011) Perturbation of polyamine catabolism can strongly affect root development and xylem differentiation. Plant Physiol 157:200–215 Tonon G, Kevers C, Faivre-Rampant O, Grazianil M, Gaspar T (2004) Effect of NaCl and mannitol iso-osmotic stresses on proline and free polyamine levels in embryogenic Fraxinus angustifolia callus. J Plant Physiol 161:701–708 Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354 Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926 Urano K, Yoshiba Y, Nanjo T, Ito T, YamaguchiShinozaki K, Shinozaki K (2004) Arabidopsis stress inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313:369–375 Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078

198

B. B. Pandey et al.

Vakharia DN, Kukadia AD, Parameswara M (2003) Polyamines in response to artificial water stress in groundnut seedlings. Indian J Plant Physiol 8:383–387 Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677 Vuosku J, Suorsa M, Ruottinen M, Sutela S, Muilu-Mäkelä R, JulkunenTiitto R (2012) Polyamine metabolism during exponential growth transition in Scots pine embryogenic cell culture. Tree Physiol 32:1274–1287 Vuosku J, Karppinen K, Muilu-Mäkelä R, Kusano T, Sagor GHM, Avia K (2018) Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. Ann Bot 121:1243–1256 Walker MA, Mc-Kersie BD (1993) Role of ascorbate glutathione antioxidant system in chilling resistance of tomato. J Plant Physiol 141:223–234 Wang CY (1987) Changes of polyamines and ethylene in cucumber seedlings in response to chilling stress. Physiol Plant 69:25–37 Wang W, Vinocur B, Altman A (2004) Role of plant heat shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252 Wang C, Fan X, Wang G, Niu J, Zhou B (2011) Differential expression of Rubisco in sporophytes and gametophytes of some marine macroalgae. PLoS One 6(1):16351 Watson MB, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) Heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1083 Watson MB, Emor KK, Piatak RM, Malmberg RL (1998) Arginine decarboxylase (polyamine synthesis) mutants of Arabidopsis thaliana exhibit altered root growth. Plant J 13:2319 Weinstein LH, Kaur-Sawney RK, Rajam MV, Wettlanfer SH, Galston AW (1986) Cadmium-­ induced accumulation of putrescine in oat and bean leaves. Plant Physiol 82:6415 Wi SJ, Park KY (2002) Antisense expression of carnation cDNA encoding ACC synthase or ACC oxidase enhances polyamine content and abiotic stress tolerance in transgenic tobacco plants. Mol Cells 13:209–220 Williams-Ashman HG, Schenone A (1972) Methyl-glyoxyl-bis (guanyl hydrazone) as a potent inhibitor of mammalian and yeast S-adenosylmethionine. Biochem Biophys Res Commun 46:288–295 Wimalasekera R, Tebartz F, Scherer GF (2011a) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181(5):593–603 Wimalasekera R, Villar C, Begum T, Scherer GFE (2011b) COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678 Wu J, Shu S, Li C, Sun J, Guo S (2018) Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. Plant Physiol Biochem 128:152–162 Xu L (2015) The effect of polyamineon flower bud differentiation and bud germination of chrysanthemum. Shandong Agric Univ 2:31–36 Xu C, Wu X, Zhang H (2009) Impact of D-Arg on drought resistance and endogenous polyamines in mycorrhizal Pinus massoniana. J Nanjing Forestry Univ 33:019–023 Xu L, Xing ST, Sun X (2014) Effects of polyamines on hormones contents and the relationship with the flower bud differentiation in chrysanthemum. Plant Physiol J 50:1195–1202 Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:67–83 Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:48690 Yamamoto A, Shim IS, Fujihara S (2016) Inhibition of putrescine biosynthesis enhanced salt stress sensitivity and decreased spermidine content in rice seedlings. Biol Plant 61:385–388 Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11:522–524

Polyamines for Sustainable Plant Growth and Production Under Adverse Environmental… 199 Yang JC, Zhang JH, Liu K, Wang ZQ, Liu LJ (2007) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58:1545–1555 Ye B, Muller H, Zhang J, Gressel J (1997) Constitutively elevated levels of putrescine and putrescine-­generating enzymes correlated with oxidant stress resistance in Conzya bonariensis and wheat. Plant Physiol 115:1443–1451 Yiu JC, Juang LD, Fang DYT, Liu CW, Wu SJ (2009) Exogenous putrescine reduces flooding-­ induced oxidative damage by increasing the antioxidant properties of Welsh onion. Sci Hortic 120:306–314 Yokota T, Nakayama M, Haarasawa I, Sato M, Katsuhara M, Kawabe S (1994) Polyamines, indole-3-acetic acid and abscisic acid in rice phloem sap. Plant Growth Regul 15:1258 Young ND, Galston AW (1984) Physiological control of arginine decarboxylase activity in K-deficient oat shoots. Plant Physiol 76:3315 Zacchini M, de Agazio M (2004) Spread of oxidative damage and antioxidative response through cell layers of tobacco callus after UV-C treatment. Plant Physiol Biochem 42:445–450 Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella M (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:7818 Zhang Y, Wu R, Qin G, Chen Z, Gu H, Qu LJ (2011) Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis. J Integr Plant Biol 53:493–506 Zhao FG, Qin P (2004) Protective effect of exogenous polyamines on root tonoplast functions against salt stress in barley seedlings. Plant Growth Regul 42:97–103 Zhao FG, Song CP, He JQ, Zhu H (2007) Polyamines improve homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:106–172

Plant Performance and Defensive Role of Proline Under Environmental Stress Pankaj S. Mundada, Suchita V. Jadhav, Supriya S. Salunkhe, Swati T. Gurme, Suraj D. Umdale, Tukaram D. Nikam, and Mahendra L. Ahire

1  Introduction Plants are in the base of the food chain with their unique abilities to produce raw food material. They are the main source of food for the majority of the world population as well as the source of food for animals. Further, plants represent a renewable resource for raw materials used in industry (Mosa et  al. 2017). Geographic allocation and growth of plants are highly influenced by the environment. Most plant problems are caused by environmental stress either expressly or implicitly. Environmental factors that affect plant growth include several biotic and abiotic factors. It is important to understand how these factors affect plant growth and development. Plants respond via different mechanisms for tolerating the unfavorable environmental conditions in order to minimize their impact. These mechanisms

P. S. Mundada Department of Biotechnology, Yashavantrao Chavan Institute of Science, Satara, Maharashtra, India Department of Botany, Savitribai Phule Pune University, Pune, Maharashtra, India S. V. Jadhav · S. S. Salunkhe · S. T. Gurme Department of Biotechnology, Yashavantrao Chavan Institute of Science, Satara, Maharashtra, India S. D. Umdale Department of Botany, Jaysingpur College (Affiliated to Shivaji University, Kolhapur), Jaysingpur, Maharashtra, India T. D. Nikam Department of Botany, Savitribai Phule Pune University, Pune, Maharashtra, India M. L. Ahire (*) Department of Botany, Yashavantrao Chavan Institute of Science, Satara, Maharashtra, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_8

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include production of reactive oxygen species (ROS), accumulation osmolytes, production of hormones, etc. Under stressful conditions, plants accumulate a group of metabolites along with certain amino acids. Amino acids have conventionally been considered as main constituents of proteins and play an important role in regulating several processes related to gene expression, plant metabolism, and development to increase yield and overall quality of crops. Protein synthesis does not occur in deficiency of amino acids, and due to this, different types of plant diseases may arise. The plants take up amino acid through stoma. It has been observed that amino acids influence the physiological activities of the plant as well as improve the microflora of soil to facilitate nutrients. Most of the data suggests a positive correlation between proline accumulation and plant stress. Proline (Pyrrolidine-2-carboxylic acid) is one of the proteinogenic amino acids and plays a greatly advantageous role in plants exposed to various stress conditions. It contains an α-amino group (NH2+), α-carboxylic group (-COO−), and pyrrolidine side chain. Chemically, proline is classified as a nonpolar, aliphatic amino acid. Proline performs variety of functions in biological systems. In plants, accumulation of proline is a common response under variety of environmental stresses. It acts as an organic osmolytes and accumulates them to tolerate osmotic stresses. Osmolyte accumulation is frequently reported in plants exposed to environmental stresses, and has been correlated with plants capacity to tolerate and adapt to extreme environmental conditions (Errabii et al. 2007; Slama et al. 2008; Ahire et al. 2013). Proline is one of the most important and widely studied osmolytes found in plants and is related with abiotic stress tolerance. Dramatic accumulation of proline due to increased synthesis and decreased degradation under a variety of stress conditions such as salt, drought, and metal has been documented in many plants (Kavi Kishor et al. 2005). Proline is generally assumed to serve as a physiologically compatible solute that increases as needed to maintain a favorable osmotic potential between the cell and its surroundings (Pollard and Wyn Jones 1979). Proline is an important osmoprotectant in plants and can protect the photosynthetic machinery against salt-induced damage (Sivakumar et al. 2002). When exposed to salt stress many plants accumulate high amounts of proline, in some cases several times the sum of all other amino acids (Mansour 2000). Although the regulation and function of proline accumulation are not yet completely understood, the engineering of proline metabolism could lead to new opportunities to improve plant tolerance of environmental stresses.

2  Proline Metabolism The metabolic pathway for l-proline was described by Elijah Adams and Harold Strecker in the mid-1950s (Phang et al. 2001). Concentration of proline in different cell types is regulated by the biosynthesis, catabolism, and transport of proline among different cellular compartments (Szabados and Savouré 2010). Plants are capable of rapid synthesis as well as quick degradation of proline as and when

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required in the cell (Trovato et al. 2008). Proline synthesis in plants is carried out by two pathways: glutamate pathway and/or ornithine pathway. These pathways are essentially carried out in the cell cytoplasm and/or chloroplast with the help of an array of enzymes. Degradation of proline leads to the formation of glutamate in mitochondria by different enzymes. Thus, biosynthesis and degradation of proline can also be denoted as the proline cycle (Meena et al. 2019).

2.1  Proline Synthesis Glutamate and ornithine are the precursors for the synthesis of proline in plants (Fig. 1). Fichman et al. (2015) reviewed the proline biosynthesis pathways in different domains of life. Accumulation of proline under stress conditions is subject to both activation of its synthesis and inhibition of its degradation (Ben Rejeb et al. 2014). For basic cellular functions, plant cell synthesizes proline in the cytosol; as plants signal stress conditions, the production moves to chloroplasts (Székely et al. 2008). The most common and dominating pathway of proline synthesis in higher plants and animals is assisted by bifunctional pyrroline-5-carboxylate synthetase (P5CS). This pathway uses glutamate as the substrate for the proline synthesis. The

Fig. 1 Schematic representation  of proline biosynthesis pathway. P5CDH Δ1-pyrroline-5-­ carboxylate dehydrogenase, GSA glutamic g-semialdehyde, OAT ornithine aminotransferase, P5C 1-pyrroline-5-carboxylic acid, PDH proline dehydrogenase, P5CR Δ1-pyrroline-5-carboxylate reductase, P5CS Δ1-pyrroline-5-carboxylate synthetase

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alternative pathway of proline formation uses ornithine from the initial steps of the arginine biosynthetic pathway. Under osmotic stress conditions, plants prefer glutamate pathway for proline synthesis (Ben Rejeb et al. 2014). 2.1.1  Proline Synthesis from Glutamate The synthesis of proline from glutamate was first reported in bacteria (Leisinger 1987). This is an important pathway in plants under nitrogen-insufficient condition or osmotic stress (Trovato et al. 2008). The synthesis of proline from glutamate is catalyzed mainly by two enzymes, pyrroline-5-carboxylate synthetase (P5CS) and pyrroline-5-carboxylate reductase (P5CR) via an intermediate pyrroline-5-­ carboxylate (P5C) (Sekhar et  al. 2007; Verslues and Sharma 2010). The enzyme P5CS is encoded by two different genes, namely, P5CS1 and P5CS2, whereas enzyme P5CR is encoded by one gene in plants (Armengaud et al. 2004). P5CS1 is expressed mostly in shoot and root in response to abscisic acid (ABA) supplementation or stress condition. The other enzyme P5CS2 is significantly expressed in dividing cells, endosperm, and inflorescence (Székely et al. 2008; Kavi Kishor and Sreenivasulu 2014). The first step in proline synthesis from glutamate is phosphorylation of glutamate to γ-glutamyl phosphate. This γ-glutamyl phosphate is converted to an intermediate compound glutamic semialdehyde (GSA) which is then converted into Δ1-pyrroline-5-carboxlyate (P5C) by P5CS enzyme complex. The P5C is then finally reduced to l-proline by P5CR enzyme in both prokaryotes and eukaryotes. In plants P5CS is a key regulatory enzyme for proline synthesis and acts as a rate-­ limiting step (Kavi Kishor et al. 1995). It is regulated by feedback inhibition and transcriptional regulation (Yoshiba et al. 1995; Zhang et al. 2014). The activity of P5CS is affected positively by light (Hayashi et al. 2000) and nitric oxide (Zhao et al. 2009) whereas brassinosteroids affect negatively (Ábrahám et al. 2003). 2.1.2  Proline Synthesis from Ornithine l-Proline is synthesized by an alternative pathway using ornithine as the precursor under supra-optimal nitrogen condition and seed development stage (Roosens et al. 1998; Armengaud et al. 2004). In this pathway amino group of ornithine is trans-­ aminated leading to formation of P5C by ornithine-Δ-aminotransferase (OAT) via an intermediate product pyrroline-2-carboxylate (Delauney and Verma 1993; Verbruggen and Hermans 2008). Then ornithine cyclodeaminase enzyme reduces or directly converts this P5C to l-proline.

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2.2  Proline Degradation The conversion products of P5C during proline synthesis may lead to generation of reactive oxygen species (ROS). The overaccumulation of ROS leads to cellular apoptosis leading to programmed cell death (Hellmann et al. 2000; Székely et al. 2008). Thus, it is necessary to degrade the excess amount of proline immediately upon alleviation of stress condition. The enzymes required for the proline catabolism, proline dehydrogenase (PDH) and proline oxidase (POX) are located in the mitochondria. These enzymes convert proline to P5C, which is in turn converted back to glutamate by P5C dehydrogenase enzyme (P5CDH) (Szabados and Savouré 2010). The genes for the catabolic enzymes have been identified and isolated from Arabidopsis and Nicotiana tabacum. Two genes encode PDH and one gene encodes P5CDH in them (Kiyosue et al. 1996; Verbruggen et al. 1996; Ribarits et al. 2007).

3  Proline Under Adverse Environmental Conditions Proline is a key amino acid accumulated in plants under adverse environmental conditions. Plants are reported to accumulate substantial amount of proline under stress conditions (Dar et al. 2016; Zanella et al. 2016). Zhang et al. (2013) reported that accumulation of proline improves the DNA methylation suggesting the role of proline in epigenetic control. Furthermore, proline accumulation is reported to act as a signal of stress memory in next generations of plants (Kavi Kishor and Sreenivasulu 2014). The cellular level of proline varies from species to species and depends upon the severity and duration of the stress situation (Delauney and Verma 1993). Contradictory literature is available about the relationship between proline accumulation and stress alleviation (Szepesi and Szőllősi 2018). Under stress condition, the overexpression of genes involved in proline biosynthesis pathway leads to inflation of shoot:root biomass ratio, arrangement of inflorescence, and yield of the plants (Kavi Kishor et al. 1995; Hare and Cress 1997). When plants are exposed to a variety of abiotic stresses, damage is occurring on primary metabolites due to an enhanced production of different reactive oxygen species (ROS) like hydrogen peroxide (H2O2), singlet oxygen (1O2), superoxide anion (O2˙−), and hydroxyl radicals (˙OH) (Signorelli et al. 2015). Plant had two types of defense mechanism against ROS, one by enzymatic and the other by the means of nonenzymatic antioxidant processes. Among them, accumulation of proline is considered as a part of nonenzymatic antioxidant plant defense (Chen and Dickman 2005). Under stressed conditions plants are known to accumulate proline up to 100 times than that of normal conditions (Barnnet and Naylor 1966; Signorelli et al. 2015) (Table 1).

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Table 1  Summary of the proline accumulation under adverse environmental conditions Type of stress Salinity

Drought

Leaves Leaves Seedlings Leaves Leaves Seedlings

Solanum tuberosum (Potato)

Leaves

Spirodela polyrhiza (Duckmeat) Arabidopsis thaliana (Arabidopsis) Artemisia annua (Sweet wormwood) Brassica rapa (Mustard) Eleusine coracana (Finger millet) Hordeum vulgare (Barley)

Whole plant Whole plant Leaf

Nicotiana tabacum (Tobacco)

Water logging stress Low temperature (chilling)

Plant organ studied Leaves Leaves Roots Leaves

Plant Brassica juncea (Mustard) Cucumis sativus (Cucumber) Citrus spp. (Citrus) Mesembryanthemum crystallinum (Crystalline iceplant) Panicum virgatum (Switchgrass) Pisum sativum (Pea) Ricinus communis (Castor bean) Simmondsia chinensis (Jojoba) Solanum lycopersicum (Tomato) Solanum melongena (Eggplant)

Nicotiana tabacum (Tobacco) Saccharum officinarum (Grass) Solanum lycopersicum (Tomato) Vigna radiata (Mung bean) Cucumis sativus (Cucumber)

Cicer arietinum (Chick pea) Phyllostachys praecox (Bamboo) Musa (Banana) High temperature Cicer arietinum (Chickpea) (heat) Citrus spp. (Citrus) Triticum aestivum (Wheat) Vigna aconitifolia (Moth bean)

Reference Iqbal et al. (2015) Fariduddin et al. (2013) Vives-Peris et al. (2017) Shevyakova et al. (2009) Guan et al. (2018) Balal et al. (2016) Wang et al. (2019) Alotaibi et al. (2020) Siddiqui et al. (2019) Ahire and Nikam (2011) Hmida-Sayari et al. (2005) Cheng et al. (2013) Dubey et al. (2019) Soni and Abdin (2017)

Leaves Seedlings Leaves and roots Leaves and roots Leaves Leaves Leaves Seedlings Leaves

La et al. (2019) Mundada et al. (2020) Bandurska et al. (2017)

Cvikrová et al. (2013) Zhang et al. (2020) Mona et al. (2017) Saima et al. (2018) Barickman et al. (2019)

Leaves Shoot Leaves Leaves Roots Leaves Leaves

Kaur et al. (2011) Liu et al. (2016) Chen et al. (2020) Kaushal et al. (2011) Vives-Peris et al. (2017) Mishra et al. (2017) Harsh et al. (2016)

Dobrá et al. (2011)

(continued)

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Table 1 (continued) Type of stress Cu

Zn

Ni

Co Cd

Pb

Al

Herbicide (butachlor) Red rot disease resistance

Plant Cucumis sativus (Cucumber) Solanum nigrum (Black nightshade) Solanum lycopersicum (Tomato)

Plant organ studied Leaves Shoot Shoot

Zea mays (Maize) Solanum nigrum (Black nightshade) Solanum lycopersicum (Tomato)

Shoot

Triticum aestivum (Wheat) Eleusine coracana (Finger millet) Pisum sativum (Pea)

Leaves, root Shoot, root Leaves, root

Sesuvium portulacastrum (Sea purslane) Glycine max (Soyabean) Avicennia marina (Mangrove) Kandelia obovata (Mangrove) Mentha arvensis (Mint) Olea europaea (Olive) Solanum nigrum (Black nightshade) Solanum lycopersicum (Tomato)

In vitro culture Leaves Leaves Leaves Leaves Leaves, root Shoot Shoot

Solanum lycopersicum (Tomato) Glycine max (Soyabean) Sesamum indicum (Sesame)

Fruit pulp Leaves Root

Lycopersicum esculentum (Tomato) Zea mays (Maize)

Leaves

Oryza sativa (Rice) Saccharum officinarum (Sugercane)

Shoot Shoot

Reference Fariduddin et al. (2013) Al Khateeb and Al-Qwasemeh (2014) Al Khateeb and Al-Qwasemeh (2014) Wen et al. (2013) Al Khateeb and Al-Qwasemeh (2014) Al Khateeb and Al-Qwasemeh (2014) Li et al. (2013) Kotapati et al. (2017) Gajewska and Skłodowska (2005) Fourati et al. (2019) Imtiyaz et al. (2014) Dai et al. (2017) Dai et al. (2017) Zaid et al. (2020) Zouari et al. (2016) Al Khateeb and Al-Qwasemeh (2014) Al Khateeb and Al-Qwasemeh (2014) Lima et al. (2019) Imtiyaz et al. (2014) Amooaghaie et al. (2017) Varalakshmi et al. (2014) Khan et al. (2000)

Shoot and root Seedlings

Tripthi et al. (2020)

Leaves

Amna et al. (2020)

3.1  Salinity Stress Among the various environmental stresses, salinity is a major abiotic stress which drastically reduces the crop yield. More than 20% of the total land is affected by the salinity throughout the world and the amount of affected soil is continuously

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increasing due to high evapo-transpiration rate, poor-quality water irrigation, and excess use of chemical fertilizers. On the basis of adaptation of salt, ecologically plants are classified as the halophytes (tolerant to higher salt concentrations) and glycophytes (susceptible to higher salt concentrations). Majority of the crop species are categorized in the second group (Gupta and Huang 2014). Salinity stress affects plants in almost every aspect of physiology (Husen et al. 2016, 2018, 2019; Hussein et al. 2017). It affects the plants at whole-plant level as well as at the cellular levels through osmotic stress in an earlier phase and ionic stress at a later stage (Munns and Tester 2008). Proline is worked as a physiologically compatible solute which maintains the required osmotic potential of cell and its environment (Pollard and Wyn Jones 1979; Ahire and Nikam 2011). In addition, proline acts as a storage sink for carbon and nitrogen and it also performs the function of a free-radical scavenger (Chinnusamy et al. 2005; Flors et al. 2007; Ahire et al. 2013). It also stabilizes subcellular structures (membranes and proteins) and buffers cellular redox potential under stress (Kavi Kishor et  al. 2005). Dramatic accumulation of proline under salinity stress in plants has been documented by number of researchers (Kavi Kishor et al. 2005; Szepesi and Szőllősi 2018). In some, the accumulation of proline was found to be several times higher than the sum of all other amino acids (Mansour 2000).

3.2  Drought Stress Drought is one of the major abiotic stresses associated with a reduction of fertile land and food production throughout the world (Moreno-Galván et al. 2020). It is one in every of the foremost studied abiotic in terms of its economic, social, and environmental impacts, together with its impact on plant growth and development (Mahajan and Tuteja 2005; Husen 2010; Kavamura et al. 2013; Husen et al. 2014; Getnet et al. 2015; Ngumbi and Kloepper 2016; Embiale et al. 2016). Almost all the abiotic stresses together with osmotic stress cause oxidative damage and embrace the assembly of reactive oxygen species (ROS) in plants (Upadhyaya et al. 2013; Siddiqi and Husen 2017, 2019). However, plants evolved a range of tolerance mechanisms to manage the injury caused by these stresses (Mundada et  al. 2020). Activation of antioxidative enzymes and additionally the accumulation of compatible solutes that effectively scavenge ROS are among them (Upadhyaya et al. 2013). Plant cells understand stress stimuli via numerous sensors that successively activate communicating pathways such as secondary messengers, plant hormones, signal transducers, and transcriptional regulators (Cvikrová et  al. 2013; Danquah et  al. 2014; Gilroy et al. 2014). Numerous signals thus unite to manage stress-inducible genes that encode proteins and enzymes directly concerned in stress metabolism, causative to the specificity of the acclimatization response to a given stress stimuli (Casaretto et  al. 2016). The inflection of the antioxidant response under drought stress is a preventive mechanism of plants from damage caused due to the augmented ROS concentration. These ROS levels generate a disparity in the redox homeostasis and affect the growth and development of plants in several ways

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(Moreno-Galván et  al. 2020). Plants utilized numerous mechanisms to reinstate redox homeostasis by producing enzymatic and nonenzymatic antioxidants. The nonenzymatic antioxidants composed of several low weight molecules such as proline, ascorbate, and a few sugars have high reducing power. These molecules are synthesized by the plants to keep up water homeostasis of the cell and to avoid the injury caused by interaction of ROS with crucial biomolecules in plants like DNA, proteins, and lipids (Farooq et al. 2009; Daffonchio et al. 2015). Many researchers reported the enhanced accumulation of proline in leaves of different plants and their varieties under drought stress. The increment in osmolytes accumulation is reported in the leaves of oil palm seedlings (Cao et al. 2011), finger millet (Bhatt et al. 2011; Kotapati et al. 2014; Mundada et al. 2020), and four genotypes of lentils (Muscolo et al. 2014). However, the levels of proline accumulation in the tolerant and sensitive genotypes are found varied as different genotypes have differential abilities to synthesize the proline.

3.3  Temperature Stress Among the different climatic factors temperature is an important factor which significantly alters the different life processes of all living organisms including plants. Plants experienced the temperature stress can be classified in three distinct types: (1) heat stress or high temperature stress (higher temperature than optimum), (2) chilling stress (temperatures below freezing), and (3) freezing stress (temperatures above freezing) (Źróbek-Sokolnik 2012). Every plant requires a specific temperature regime for the proper growth and development. Temperature significantly alters the growth and development of plants. The temperature stress and water scarcity are interrelated. The interrelationships between the results of extreme temperatures and scarcity of tissue water content on the growth and metabolism of the whole plant are difficult to unravel. Supra-optimal temperatures will cause an increase in rate of transpiration which leads to lowering the tissue water content in the leaves. Furthermore, low temperature reduces the accessibility of water within the soil and its movement towards roots of the plants. This results in the reduction in leaf water potential. In these cases, it is complex to segregate the direct impacts of temperature on plant metabolism from those mediate through the associated change in water potential (Chu et al. 1974). It was been suggested that plant resistance to cold, heat, and water stress are interrelated (Levitt 1956), which is easily understood if each is a manifestation of response to an analogous modification in tissue surroundings. On the other hand, a lot of direct metabolic responses to temperature extremes are clearly involved. The metabolic responses of plants to temperature stresses are similar to that of water scarcity. The utmost prominent metabolic response to the lower water potential in many plants is a quick and comprehensive accumulation of the imino acid proline (Singh et  al. 1973; Hayat et  al. 2012; Kavi Kishor and Sreenivasulu 2014).

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3.4  Heavy Metal Stress Anthropogenic activities such as mining, industrial wastes, sewage disposal, and improper agricultural practices (over dosage of chemical fertilizers) significantly increase the contamination of heavy metals in soil and groundwater (Tiwari and Lata 2018; Ghori et al. 2019). This accumulation of heavy metals imposes detrimental effects on soil health, which ultimately lead to loss in crop yield. Heavy metals directly and/or indirectly decline the growth and development of plants by affecting various biochemical, physiological, and molecular processes of plants (Panuccio et al. 2009; Hassan et al. 2017). Among the different heavy metals, some (Zn, Cu, Mo, Mn, Co, and Ni) are required in small quantities for the growth and development of plants (Salla et al. 2011; Shahid et al. 2015). Among various significant heavy metals, four heavy metals (As, Pb, Cd, and Hg) are thought-about the maximum toxic metals (ATSDR 2003), supported their toxicity, frequency of incidence, and most significantly their exposure potential to flora and fauna. Heavy metal stress deactivates or denatures different vital enzymes and proteins, and interferes with substitution reactions of crucial metal ions from biomolecules (Ghori et al. 2019), which in turn disturbs the integrity of biological membranes and alters the basic metabolic processes of plants (Hossain et al. 2012). Based on its recognized properties proline could also be concerned in plant heavy metal stress by diverse mechanisms, i.e., osmo- and redox-regulation, metal chelation, and scavenging of free radicals (Sharma and Dietz 2006). Proline has been delineating to be concerned in neutralizing the free radicals produced on acquaintance to heavy metals; however their role in sequestering the metals has not been seen. It has been studied by Hossain et al. (2010) in mung bean that exogenous proline-induced tolerance against Cd stress stimulates the synthesis of glutathione and glutathione-­ metabolizing enzymes (Ghori et al. 2019).

3.5  Other Stresses Instead of these above stresses, other factors are also inducing oxidative damage such as nutrient deficiency, sugars, pathogens, KCl, CaCl2, etc. where the stress tolerance mechanism of the plants involves the accumulation of proline as an osmoprotectant. Reports are available on higher accumulation of proline under nutrient deficiency (Stewart 1978; Gӧring and Thein 1979; Alia and Saradhi 1991; Heidari and Sarani 2012; Arias-Baldrich et  al. 2015), sugars (Al-Khayri and Al-Bahrany 2002; Jain et al. 2010), KCl and CaCl2 (Ahire et al. 2014), plant-pathogen interactions (Fabro et al. 2004; Takahashi et al. 2008; Verslues and Sharma 2010; Rizzi et  al. 2017), and UV irradiation (Hofmann et  al. 2003; Poulson et  al. 2006; Radyukina et al. 2010).

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4  Overexpression of Proline Synthesis Under Stress When a plant is subjected to abiotic stress, a number of genes are turned on, resulting in increased levels of several metabolites and proteins. Among the several metabolites and proteins, some are responsible for conferring a certain degree of protection against these stresses. Genetic engineering would be a faster way to insert beneficial genes than through conventional or molecular breeding. Genetic engineering allows controlling the timing, tissue-specificity, and expression level of the introduced genes for their optimal function. This is an important consideration if the action of a given gene or transcription factor is desired only at a specific time, in a specific organ, or under specific conditions of stress. Recently, engineering of the genes concerned with the synthesis of low molecular weight metabolites which includes mannitol (Pujni et al. 2007), glycine betaine (Mohanty et al. 2002), and proline (Vendruscolo et al. 2007; Yamchi et al. 2007; Bhatnagar-Mathur et al. 2009) have ended up in improved tolerance to abiotic stress in transgenic plants. Among proline biosynthetic pathway genes, Δ1-pyrroline-5-carboxylate synthetase (P5CS) appears to be widely utilized and its overexpression in transformed plants exhibits improved tolerance to oxidative stress. Several researchers have demonstrated that overexpression of P5CS genes increases proline production and confers salt tolerance in transgenics in a number of crop plants including rice (Anoop and Gupta 2003; Su and Wu 2004; Kumar et al. 2010), wheat (Vendruscolo et al. 2007), potato (Hmida-Sayari et  al. 2005), and tobacco (Kavi Kishor et  al. 1995; Yamchi et  al. 2007). Some other examples of overproduction of proline in genetically modified plants are summarized in Table 2.

5  Proline Other Functions in Plants Proline performs multifunctional role in plant metabolism. Though many researchers focus on the role of proline as an osmoprotectant, some researchers drive the attention towards the developmental role of proline in plant metabolism. Kavi Kishor and Sreenivasulu (2014) summarized the multifaceted functions of proline. Proline is thought to be an essential component in signaling mechanism of flower induction as it is so evidently accumulated in reproductive tissues (Chiang and Dandekar 1995; Schwacke et  al. 1999). Under normal physiological conditions, higher amount of proline was found to be transported towards the reproductive organs (Rentsch et al. 1996; Fischer et al. 1998; Mattioli et al. 2009). About 26% of the proline content was found to be accumulated of the total amino acid pool in reproductive tissues, whereas it was only 1–3% in its vegetative tissue in Arabidopsis thaliana (Chiang and Dandekar 1995; Schwacke et al. 1999). Higher accumulation of proline in reproductive tissues such as pollen grains of petunias and tomatoes (Zhang et al. 1982; Fujita et al. 1998) and the ovules of faba beans (Venekamp and Koot 1984) suggests that proline acts as a potential source of nitrogen and energy

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Table 2  Genetically transformed plant with overproduction of proline S. no. Transgenic plant 1. Nicotiana tabaccum (Tobacco) 2. Oryza sativa (Rice) 3.

Gene Δ1-pyrroline-5-carboxylate synthetase Δ1-pyrroline-5-carboxylate synthetase Osmotin

Stress condition Drought stress Water and salt stress Salt stress

Ornithine-δ-­ aminotransferase P5CS

Osmotic stress Salt stress Salt stress

5.

Nicotiana tabaccum (Tobacco) Nicotiana plumbaginifolia (Tex-Mex tobacco) Triticum aestivum (Wheat)

6.

Oryza sativa (Rice)

7.

Oryza sativa (Rice)

8.

Arabidopsis

Vigna aconitifolia Δ(1)-pyrroline-5-­ carboxylate synthetase Ornithine-δ-­ aminotransferase (At δ-OAT gene) AtP5CS2

9.

Oryza sativa (Rice)

P5CS

4.

P5CS 10. Citrus sinensis Osb. × Poncirus trifoliata L. Raf. (Tetraploid Carrizo citrange rootstock) 11. Solanum tuberosum (Potato) Δ1-pyrroline-5-carboxylate synthetase 12. Petunia hybrida cv. AtP5CS, OsP5CS ‘Mitchell’ (Petunia) 13. Oryza sativa (Rice) OsCOIN upregulates OsP5CS 14. Triticum aestivum (Wheat)

P5CS

15. Nicotiana tabaccum (Tobacco) 16. Morus alba (Mulberry)

P5CS HVA1

17. Cicer arietinum (Chick pea) P5CSF129A

Reference Kavi Kishor et al. (1995) Zhu et al. (1998) Barthakur et al. (2001) Roosens et al. (2002) Sawahel and Hassan (2002) Anoop and Gupta (2003)

Salt and Wu et al. drought stress (2003) Plant-­ pathogen interaction Salt and drought stress Drought stress

Fabro et al. (2004)

Salt stress

Hmida-Sayari et al. (2005) Yamada et al. (2005) Liu et al. (2007)

Drought stress Chilling, salt and drought stress Drought stress Osmotic stress Salinity and water stress Drought stress

18. Oryza sativa (Rice)

P5CSF129A

Salt stress

19. Nicotiana tabaccum cv. Xanthi (Tobaco)

P5CS

Osmotic stress

Su and Wu (2004) Molinari et al. (2004)

Vendruscolo et al. (2007) Yamchi et al. (2007) Lal et al. (2008) Bhatnagar-­ Mathur et al. (2009) Kumar et al. (2010) Rastgar et al. (2011) (continued)

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Table 2 (continued) S. no. Transgenic plant Gene 20. Cicer arietinum (Chick pea) P5CS 21. Nicotiana tabaccum (Tobacco) 22. Oryza sativa (Rice)

Stress condition Salt stress

23. Cajanus cajan (Pigeonpea)

Drought and heat stress Δ1-pyrroline-5-carboxylate Salt stress synthetase P5CSF129A Salt stress

24. Arabidopsis

P5CS

Salt stress

25. Ipomoea batatas (Sweetpotato) 26. Nicotiana plumbaginifolia (Tex-Mex tobacco) 27. Panicum virgatum (switchgrass) 28. Glycine max (Soybean)

IbP5CR

Salt stress

P5CSF129A

Δ1-pyrroline-5-carboxylate Salt stress synthetase PuP5CS Salt stress GmDREB6 overexpression Salt stress in enhancing the transcriptional level of GmP5CS

Reference Ghanti et al. (2011) Pospisilova et al. (2011) Karthikeyan et al. (2011) Surekha et al. (2014) Chen et al. (2013) Liu et al. (2014) Ahmed et al. (2015) Guan et al. (2018) Nguyen et al. (2019)

during pollen tube germination and fertilization (Kavi Kishor and Sreenivasulu 2014). Several authors explain the beneficial role of exogenous application of proline to in vitro cultures to improve the production efficiency for somatic embryos (Armstrong and Green 1985; Trigiano and Conger 1987). Addition of proline in the medium was found effective to induce both the size and number of somatic embryos in cultures. Proline accumulation at the time of seed maturation is associated with the activating the desiccation tolerance in plants. ABA induces proline synthesis in many plant species (Hare et al. 1999) showed that ABA and proline are contributing towards the embryo maturation in the seeds (Kavi Kishor and Sreenivasulu 2014).

6  Conclusions Plants tend to synthesize proline under adverse environmental conditions specially under abiotic stresses. Within abiotic stresses, detailed studies on its metabolism are available under salinity and drought stresses. Little attention was imposed on proline synthesis under biotic stresses. Instead of its role under environmental extremes, its developmental role is also well illustrated by many authors. Studies on genetic transformation using Δ1-pyrroline-5-carboxylate synthetase, ornithine-δ-­ aminotransferase, and mutant type Vigna aconitifolia Δ1-pyrroline-5-carboxylate synthetase and its functional role in overaccumulation of proline under both biotic

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and abiotic stresses are also well demonstrated. In addition to this, researches also emphasize on the exogenous application of proline under stress conditions in plants and found beneficial effects on growth and development of plants. However, there is need to unravel the retaliation mechanisms of proline metabolism. Still, more comprehensive analyses are required to disclose novel and interesting links of proline in adaptation of plants under environmental constraints. Still there is scope to development of genetically enhanced plants which can induce endogenous levels of proline instead of GMOs so that plants can survive under extreme environmental conditions. Acknowledgments  Authors are grateful to Yashavantrao Chavan Institute of Science, Satara, for financial support under DBT-STAR college scheme. Financial assistance to the faculty under self-­ funded project is acknowledged and also for providing facilities. Authors are also thankful for financial assistance to Department of Botany, Savitribai Phule Pune University, Pune, by the University Grants Commission, New Delhi, and Department of Science and Technology (DST), Government of India and DST-PURSE are gratefully acknowledged.

References Ábrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372 Ahire ML, Nikam TD (2011) Differential response of Brinjal (Solanum melongena Linn.) varieties to salinity stress in relation to seed germination and osmolytes accumulation. Seed Sci Biotechnol 5:29–35 Ahire ML, Walunj PR, Kavi Kishor PB, Nikam TD (2013) Effect of sodium chloride induced stress on growth, proline, glycine betaine accumulation, antioxidative defense and bacoside A content in in vitro regenerated shoots of Bacopa monnieri (L.) Pennell. Acta Physiol Plant 35:1943–1953 Ahire ML, Laxmi S, Walunj PR, Kavi Kishor PB, Nikam TD (2014) Effect of potassium chloride and calcium chloride induced stress on in vitro cultures of Bacopa monnieri (L.) Pennell. J Plant Biochem Biotechnol 23:366–378 Ahmed AAM, Roosens N, Dewaele E, Jacobs M, Angenon G (2015) Overexpression of a novel feedback-desensitized Δ1-pyrroline-5-carboxylate synthetase increases proline accumulation and confers salt tolerance in transgenic Nicotiana plumbaginifolia. Plant Cell Tissue Organ Cult 122:383–393 Al Khateeb W, Al-Qwasemeh H (2014) Cadmium, copper and zinc toxicity effects on growth, proline content and genetic stability of Solanum nigrum L., a crop wild relative for tomato; comparative study. Physiol Mol Biol Plants 20:31–39 Alia, Saradhi PP (1991) Proline accumulation under heavy metal stress. J Plant Physiol 138:554–558 Al-Khayri JM, Al-Bahrany AM (2002) Callus growth and proline accumulation in response to sorbitol and sucrose-induced osmotic stress in rice. Biol Plant 45:609–611 Alotaibi SS, Elseehy MM, Aljuaid BS, El-Shehawi AM (2020) Transcriptome analysis of jojoba (Simmondsia chinensis) during seed development and liquid wax ester biosynthesis. Plants 9:588 Amna, Xia Y, Farooq MA, Javed MT, Kamran MA, Mukhtar T, Ali J, Tabassum T, ur-Rehman S, Munis MFH, Sultan T, Chaudharya HJ (2020) Multi-stress tolerant PGPR Bacillus ­xiamenensis

Plant Performance and Defensive Role of Proline Under Environmental Stress

215

PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol Biochem 151:640–649 Amooaghaie R, Zangene-madar F, Enteshari S (2017) Role of two-sided crosstalk between NO and H2S on improvement of mineral homeostasis and antioxidative defense in Sesamum indicum under lead stress. Ecotoxicol Environ Saf 139:210–218 Anoop N, Gupta AK (2003) Transgenic indica rice cv IR-50 overexpressing Vigna aconitifolia δ(1)-pyrroline-5-carboxylate synthetase cDNA shows tolerance to high salt. J Plant Biochem Biotechnol 12:109–116 Arias-Baldrich C, Bosch N, Begines D, Feria AB, Monreal JA, García-Mauriño S (2015) Proline synthesis in barley under iron deficiency and salinity. J Plant Physiol 183:121–129 Armengaud P, Thiery L, Buhot N, Ghislaine GDM, Savouré A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol Plant 120:442–450 Armstrong CL, Green CE (1985) Establishment and maintenance of friable, embryogenic maize callus and the involvement of L-proline. Planta 164:207–214 ATSDR (2003) Agency for toxic substances and disease registry. http://www.atsdr.cdc.gov/ Balal RM, Shahid MA, Javaid MM, Anjum MA, Ali HH, Mattson NS, Garcia-Sanchez F (2016) Foliar treatment with Lolium perenne (Poaceae) leaf extract alleviates salinity and nickel-­ induced growth inhibition in pea. Braz J Bot 39:453–463 Bandurska JN, Pietrowska-Borek M, Nuc K, Chadzinikolau T, Radzikowska D (2017) Regulation of proline biosynthesis and resistance to drought stress in two barley (Hordeum vulgare L.) genotypes of different origin. Plant Physiol Biochem 118:427–437 Barickman TC, Simpson CR, Sams CE (2019) Waterlogging causes early modification in the physiological performance, carotenoids, chlorophylls, proline, and soluble sugars of cucumber plants. Plants 8:160 Barnnet J, Naylor A (1966) Amino acid and protein metabolism in bermuda grass during water stress. Plant Physiol 11:1222–1230 Barthakur S, Babu V, Bansal KC (2001) Over-expression of osmotin induces proline accumulation and confers tolerance to osmotic stress in transgenic tobacco. J Plant Biochem Biotechnol 10:31–37 Ben Rejeb K, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284 Bhatnagar-Mathur P, Vincent V, Devi MJ, Lavanya M, Vani G, Sharma KK (2009) Genetic engineering of chickpea (Cicer arietinum L.) with the P5CSF129A gene for osmoregulation with implications on drought tolerance. Mol Breed 23:591–606 Bhatt D, Negi M, Sharma P, Saxena SC, Dobriyal AK, Arora S (2011) Responses to drought induced oxidative stress in five finger millet varieties differing in their geographical distribution. Physiol Mol Biol Plants 17:347–353 Cao HX, Sun CX, Shao HB, Lei XT (2011) Effects of low temperature and drought on the physiological and growth changes in oil palm seedlings. Afr J Biotechnol 10:2630–2637 Casaretto JA, El-kereamy A, Zeng B, Stiegelmeyer SM, Chen X, Bi YM, Rothstein SJ (2016) Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance. BMC Genomics 17:1–15 Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci U S A 102:3459–3464 Chen JB, Yang JW, Zhang ZY, Feng XF, Wang SM (2013) Two P5CS genes from common bean exhibiting different tolerance to salt stress in transgenic Arabidopsis. J Genet 92:461–469 Chen L, Zhao X, Wu J, He Y, Yang H (2020) Metabolic analysis of salicylic acid-induced chilling tolerance of banana using NMR. Food Res Int 128:108796 Cheng TS, Hung MJ, Cheng YI, Cheng LJ (2013) Calcium-induced proline accumulation contributes to amelioration of NaCl injury and expression of glutamine synthetase in greater duckweed (Spirodela polyrhiza L.). Aquat Toxicol 144–145:265–274

216

P. S. Mundada et al.

Chiang HH, Dandekar AM (1995) Regulation of proline accumulation in Arabidopsis thaliana (L) Heynh during development and in response to desiccation. Plant Cell Environ 18:1280–1290 Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448 Chu TM, Aspinall D, Paleg LG (1974) Stress metabolism. VI.* temperature stress and the accumulation of proline in barley and radish. Aust J Plant Physiol 1:87–97 Cvikrová M, Gemperlová L, Martincová O, Vanková R (2013) Effect of drought and combined drought and heat stress on polyamine metabolism in proline-overproducing tobacco plants. Plant Physiol Biochem 73:7–15 Daffonchio D, Hirt H, Berg G (2015) Plant-microbe interactions and water management in arid and saline soils. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Springer, Cham, pp 265–276 Dai M, Lu H, Liu W, Jia H, Hong H, Liu J, Yan C (2017) Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation. Ecotoxicol Environ Saf 139:272–279 Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52 Dar MI, Naikoo MI, Rehman F, Naushin F, Khan FA (2016) Proline accumulation in plants: roles in stress tolerance and plant development. In: Iqbal N, Nazar R, Khan NA (eds) Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer Nature, India, pp 155–166 Delauney AJ, Verma DPS (1993) Cloning of ornithine δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. Plant J 4:215–223 Dobrá J, Vanková R, Havlová M, Burman AJ, Libus J, Štorchová H (2011) Tobacco leaves and roots differ in the expression of proline metabolism-related genes in the course of drought stress and subsequent recovery. J Plant Physiol 168:1588–1597 Dubey AK, Kumar N, Kumar A, Ansari MA, Ranjan R, Gautam A, Meenakshi, Sahu N, Pandey V, Behera SK, Mallick S, Pande V, Sanyal I (2019) Over-expression of CarMT gene modulates the physiological performance and antioxidant defense system to provide tolerance against drought stress in Arabidopsis thaliana L. Ecotoxicol Environ Saf 171:54–65 Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Errabii T, Gandonou CB, Essalmani H, Abrini J, Idaomor M, Senhaji NS (2007) Effects of NaCl and mannitol induced stress on sugarcane (Saccharum sp.) callus cultures. Acta Physiol Plant 29:95–102 Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez ME (2004) Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant Microbe Interact 17:343–350 Fariduddin Q, Khalil RRAE, Mir BA, Yusuf M, Ahmad A (2013) 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856 Farooq ZR, Iqbal MZ, Kabir M, Shafiq M (2009) Toxic effects of lead and cadmium on germination and seedling growth of Albizia lebbeck (L.) Benth. Pak J Bot 41:27–33 Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka LN (2015) Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol Rev 90:1065–1099 Fischer WN, Andre B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195 Flors V, Paradіs M, Garcia-Andrade J, Cerezo M, González-Bosch C (2007) A tolerant behavior in salt-sensitive tomato plants can be mimicked by chemical stimuli. Plant Signal Behav 2:50–57

Plant Performance and Defensive Role of Proline Under Environmental Stress

217

Fourati E, Vogel-Mikuš K, Bettaieb T, Kavčič A, Kelemen M, Vavpetič P, Pelicon P, Abdelly C, Ghnaya T (2019) Physiological response and mineral elements accumulation pattern in Sesuvium portulacastrum L. subjected in vitro to nickel. Chemosphere 219:463–471 Fujita T, Maggio A, Garcia-Rios M, Bressan RA, Csonka LN (1998) Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for delta1-­ pyrroline-­5-carboxylate synthetase from tomato. Plant Physiol 118:661–674 Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–340 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202 Ghanti SK, Sujata KG, Kumar BV, Karba NN, Janardhan Reddy K, Rao MS, Kavi Kishor PB (2011) Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biol Plant 55:634–640 Ghori NH, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828 Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630 Gӧring H, Thein BH (1979) Influence of nutrient deficiency on proline accumulation in the cytoplasm of Zea mays L. seedlings. Biochem Physiol Pflanz 174:9–16 Guan C, Huang Y, Cui X, Liu SJ, Zhou ZY, Zhang YW (2018) Overexpression of gene encoding the key enzyme involved in proline-biosynthesis (PuP5CS) to improve salt tolerance in switchgrass (Panicum virgatum L.). Plant Cell Rep 37:1187–1199 Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596 Hare P, Cress W (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102 Hare PD, Cress WA, van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434 Harsh A, Sharma YK, Joshi U, Rampuria S, Singh G, Kumar S, Sharma R (2016) Effect of short-­ term heat stress on total sugars, proline and some antioxidant enzymes in moth bean (Vigna aconitifolia). Ann Agric Sci 61:57–64 Hassan TU, Bano A, Naz I (2017) Alleviation of heavy metals toxicity by the application of plant growth promoting rhizobacteria and effects on wheat grown in saline sodic field. Int J Phytoremediation 19:522–529 Hayashi F, Ichino T, Osanai M, Wada K (2000) Oscillation and regulation of proline content by P5CS and ProDH gene expressions in the light/dark cycles in Arabidopsis thaliana L. Plant Cell Physiol 41:1096–1101 Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments. Plant Signal Behav 7:1456–1466 Heidari M, Sarani S (2012) Growth, biochemical components and ion content of Chamomile (Matricaria chamomilla L.) under salinity stress and iron deficiency. J Saudi Soc Agric Sci 11:37–42 Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol 122:357–367 Hmida-Sayari A, Gargouri-Bouzid R, Bidani A, Jaoua L, Savoure A, Jaoua S (2005) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers salt tolerance in transgenic potato plants. Plant Sci 169:746–752 Hofmann RW, Campbell BD, Bloor SJ, Swinny EE, Markham KR, Ryan KG, Fountain DW (2003) Responses to UV-B radiation in Trifolium repens L.—physiological links to plant productivity and water availability. Plant Cell Environ 26:603–612

218

P. S. Mundada et al.

Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycine betaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272 Hossain MA, Piyatida P, Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37 Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agric Food Secur 7:44 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Imtiyaz S, Agnihotri RK, Ahmad S, Sharma R (2014) Effect of cobalt and lead induced heavy metal stress on some physiological parameters in Glycine max. Int J Agric Crop Sci 7:26–34 Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91 Jain M, Tiwary S, Gadre R (2010) Sorbitol-induced changes in various growth and biochemical parameters in maize. Plant Soil Environ 56:263–267 Karthikeyan A, Pandian SK, Ramesh M (2011) Transgenic indica rice cv. ADT 43 expressing a Δ1-pyrroline-5-carboxylate synthetase (P5CS) gene from Vigna aconitifolia demonstrates salt tolerance. Plant Cell Tissue Organ Cult 107:383–395 Kaur G, Kumar S, Thakur P, Malik JA, Bhandari K, Sharma KD, Nayyar H (2011) Involvement of proline in response of chickpea (Cicer arietinum L.) to chilling stress at reproductive stage. Sci Hortic 128:174–181 Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiol Mol Biol Plants 17:203 Kavamura VN, Santos SN, da Silva JL, Parma MM, Ávila LA, Visconti A, Zucchi TD, Taketani RG, Andreote FD, de Melo IS (2013) Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol Res 168:183–191 Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311 Kavi Kishor PB, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394 Kavi Kishor PB, Sangam S, Amrutha RN, Laxmi PS, Naidu NR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438 Khan AA, McNeilly T, Collins JC (2000) Accumulation of amino acids, proline, and carbohydrates in response to aluminum and manganese stress in maize. J Plant Nutr 23:1303–1314 Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335

Plant Performance and Defensive Role of Proline Under Environmental Stress

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Kotapati KV, Palaka BK, Kandukuri A, Pamuru RR, Ampasala DR (2014) Response of antioxidative enzymes and lipoxygenase to drought stress in finger millet leaves (Eleusine coracana (L.) Gaertn). Int J Plant Anim Environ Sci 4:644–653 Kotapati KV, Palaka BK, Ampasala DR (2017) Alleviation of nickel toxicity in finger millet (Eleusine coracana L.) germinating seedlings by exogenous application of salicylic acid and nitric oxide. Crop J 5:240–250 Kumar V, Shriram V, Kavi Kishor PB, Jawali N, Shitole MG (2010) Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over-expressing P5CSF129A gene. Plant Biotechnol Rep 4:37–48 La VH, Lee BR, Zhang Q, Park SH, Islam MT, Kim TH (2019) Salicylic acid improves drought-­ stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Hortic Environ Biotechnol 60:31–40 Lal S, Gulyani V, Khurana P (2008) Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica). Transgenic Res 17:651 Leisinger T (1987) Biosynthesis of proline in Escherichia coli and Salmonella typhimurium. In: Neidhart FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 345–351 Levitt J (1956) The hardiness of plants. Academic, New York Li X, Yang Y, Jia L, Chen H, Wei X (2013) Zinc-induced oxidative damage, antioxidant enzyme response and proline metabolism in roots and leaves of wheat plants. Ecotoxicol Environ Saf 89:150–157 Lima LW, Checchio MV, dos Reis AR, de Cássia Alves R, Tezzoto T, Gratão PL (2019) Selenium restricts cadmium uptake and improve micronutrients and proline concentration in tomato fruits. Biocatal Agric Biotechnol 18:101057 Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016 Liu D, He S, Zhai H, Wang L, Zhao Y, Wang B, Li R, Liu Q (2014) Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato. Plant Cell Tissue Organ Cult 117:1–16 Liu Z, Li L, Luo Z, Zheng F, Jiang L, Tang K (2016) Effect of brassinolide on energy status and proline metabolism in postharvest bamboo shoot during chilling stress. Postharvest Biol Technol 111:240–246 Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158 Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500 Mattioli R, Costantino P, Trovato M (2009) Proline accumulation in plants: not only stress. Plant Signal Behav 4:1016–1018 Meena M, Divyanshu K, Kumar S, Swapnil P, Zehra A, Shukla V, Yadav M, Upadhyay RS (2019) Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon 5:e02952 Mishra D, Shekhar S, Agrawal L, Chakraborty S, Chakraborty N (2017) Cultivar-specific high temperature stress responses in bread wheat (Triticum aestivum L.) associated with physicochemical traits and defense pathways. Food Chem 221:1077–1087 Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002) Transgenic plants of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57 Molinari HC, Marur CJ, Filho JB, Kobayashi AK, Pileggi M, Júnior RL, Vieira LE (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. x Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167:1375–1381 Mona SA, Hashem A, Abd-Allah EF, Alqarawi AA, Soliman DWK, Wirth S, Egamberdieva D (2017) Increased resistance of drought by Trichoderma harzianum fungal treatment correlates with increased secondary metabolites and proline content. J Integr Agric 16:1751–1757

220

P. S. Mundada et al.

Moreno-Galván AE, Cortés-Patiño S, Romero-Perdomo F, Uribe-Vélez D, Bashan Y, Bonilla RR (2020) Proline accumulation and glutathione reductase activity induced by drought-tolerant rhizobacteria as potential mechanisms to alleviate drought stress in Guinea grass. Appl Soil Ecol 147:103367. https://doi.org/10.1016/j.apsoil.2019.103367 Mosa KA, Ismail A, Helmy M (2017) Plant stress tolerance: an integrated omics approach. Springer, Cham Mundada PS, Nikam TD, Anil Kumar S, Umdale SD, Ahire ML (2020) Morpho-physiological and biochemical responses of finger millet (Eleusine coracana (L.) Gaertn.) genotypes to PEG-­ induced osmotic stress. Biocatal Agric Biotechnol 23:101488 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681 Muscolo A, Sidari M, Anastasi U, Santonoceto C, Maggio A (2014) Effect of PEG-induced drought stress on seed germination of four lentil genotypes. J Plant Interact 9:354–363 Ngumbi E, Kloepper J (2016) Bacterial-mediated drought tolerance: current and future prospects. Appl Soil Ecol 105:109–125 Nguyen QH, Vu LTK, Nguyen LTN, Pham NTT, Nguyen YTH, Le SV, Chu MH (2019) Overexpression of the GmDREB6 gene enhances proline accumulation and salt tolerance in genetically modified soybean plants. Sci Rep 9:19663 Panuccio MR, Sorgona A, Rizzo M, Cacco G (2009) Cadmium adsorption on vermiculite, zeolite and pumice: batch experiment studies. J Environ Manag 90:364–374 Phang JM, Hu CA, Valle D (2001) Disorders of proline and hydroxyproline metabolism. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) Metabolic and molecular basis of inherited disease. McGraw-Hill, New York, pp 1821–1838 Pollard A, Wyn Jones RG (1979) Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta 144:291–298 Pospisilova J, Haisel D, Vankova R (2011) Responses of transgenic tobacco plants with increased proline content to drought and/or heat stress. Am J Plant Sci 2:318–324 Poulson ME, Boeger MRT, Donahue RA (2006) Response of photosynthesis to high light and drought for Arabidopsis thaliana grown under a UV-B enhanced light regime. Photosynth Res 90:79 Pujni D, Chaudhary A, Rajam MV (2007) Increased tolerance to salinity and drought in transgenic indica rice by mannitol accumulation. J Plant Biochem Biotechnol 16:1–8 Radyukina NL, Shashukova AV, Mapelli S, Shevyakova NI, Kuznetsov VV (2010) Proline controls the level of polyamines in common sage plants under normal conditions and at UV-B irradiation. Russ J Plant Physiol 57:422–429 Rastgar JF, Yamchi A, Hajirezaei M, Karkhane AA (2011) Analysis of growth and germination stage of T2 generation of P5CS over-expressing tobacco plant Nicotiana tabaccum cv. Xanthi exposed to osmotic stress. Afr J Biotechnol 10:8539–8552 Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446 Ribarits A, Abdullaev A, Tashpulatov A, Richter A, Heberle-Bors E, Touraev A (2007) Two tobacco proline dehydrogenases are differentially regulated and play a role in early plant development. Planta 225:1313–1324 Rizzi YS, Cecchini NM, Fabro G, Alvarez ME (2017) Differential control and function of Arabidopsis ProDH1 and ProDH2 genes on infection with biotrophic and necrotrophic pathogens. Mol Plant Pathol 18:1164–1174 Roosens NHCJ, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the Ornithine-δ-­ Aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271 Roosens NH, Al-Bitar F, Loenders K, Angenon G, Jacobs M (2002) Overexpression of ornithine-­ delta-­aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breed 9:73–80

Plant Performance and Defensive Role of Proline Under Environmental Stress

221

Saima S, Li G, Wu G (2018) Effects of drought stress on hybrids of Vigna radiata at germination stage. Acta Biol Hung 69:481–492 Salla V, Hardaway CJ, Sneddon J (2011) Preliminary investigation of Spartina alterniflora for phytoextraction of selected heavy metals in soils from Southwest Louisiana. Microchem J 97:207–212 Sawahel WA, Hassan AH (2002) Generation of transgenic wheat plants producing high levels of the osmoprotectant proline. Biotechnol Lett 24:721–725 Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11:377–392 Sekhar PN, Amrutha NR, Sangam S, Verma DPS, Kavi Kishor PB (2007) Biochemical characterization, homology modeling and docking studies of ornithine δ-aminotransferase—an important enzyme in proline biosynthesis of plants. J Mol Graph Model 26:709–719 Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2015) Heavy metal stress and crop productivity. In: Hakeem KR (ed) Crop production and global environmental issues. Springer International Publishing, Cham, pp 1–25 Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726 Shevyakova NI, Bakulina EA, Kuznetsov VV (2009) Proline antioxidant role in the common ice plant subjected to salinity and paraquat treatment inducing oxidative stress. Russ J Plant Physiol 56:663–669 Siddiqi KS, Husen A (2017) Plant response to strigolactones: current developments and emerging trends. Appl Soil Ecol 120:247–253 Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Bull Natl Res Cent 43:153 Siddiqui MH, Alamri S, Al-Khaishany MY, Khan MN, Al-Amri A, Ali HM, Alaraidh IA, Alsahli AA (2019) Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int J Mol Sci 20:353 Signorelli S, Dans PD, Coitiño EL, Borsani O, Monza J (2015) Connecting proline and γ-aminobutyric acid in stressed plants through non-enzymatic reactions. PLoS One 10(3):e0115349 Singh TN, Paleg LG, Aspinall D (1973) Stress metabolism I. Nitrogen metabolism and growth in the barley plant during water stress. Aust J Biol Sci 26:45–56 Sivakumar P, Sharmila P, Vikas J, Pardha Sardhi P (2002) Sugars have potential to curtail oxygenase activity of Rubisco. Biochem Biophys Res Commun 298:247–250 Slama I, Ghnaya T, Savourѐ A, Abdelly C (2008) Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum. C R Biol 331:442–451 Soni P, Abdin MZ (2017) Water deficit-induced oxidative stress affects artemisinin content and expression of proline metabolic genes in Artemisia annua L. FEBS Open Bio 7:367–381 Stewart CR (1978) Role of carbohydrates in proline accumulation in wilted barley leaves. Plant Physiol 61:775–778 Su J, Wu R (2004) Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci 166:941–948 Surekha C, Kumari KN, Aruna LV, Suneetha G, Arundhati A, Kavi Kishor PB (2014) Expression of the Vigna aconitifolia P5CSF129A gene in transgenic pigeonpea enhances proline accumulation and salt tolerance. Plant Cell Tissue Organ Cult 116:27–36 Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97 Székely G, Abraham E, Cselo A, Rigo G, Zsigmond L, Csiszar J, Ayaydin F, Strizhov N, Jasik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28 Szepesi A, Szőllősi R (2018) Mechanism of proline biosynthesis and role of proline metabolism enzymes under environmental stress in plants. In: Ahmad P, Ahanger MA, Singh VP, Tripathi

222

P. S. Mundada et al.

DK, Alam P, Alyemeni MN (eds) Plant metabolites and regulation under environmental stress. Academic, Cambridge, pp 337–353 Takahashi H, Matsumura H, Kawai-Yamada M, Uchimiya H (2008) The cell death factor, cell wall elicitor of rice blast fungus (Magnaporthe grisea) causes metabolic alterations including GABA shunt in rice cultured cells. Plant Signal Behav 3:945–953 Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Front Plant Sci 9:452 Trigiano RN, Conger BV (1987) Regulation of growth and somatic embryogenesis by proline and serine in suspension-cultures of Dactylis glomerata. J Plant Physiol 130:49–55 Tripthi DK, Varma RK, Singh S, Sachan M, Guerriero G, Kushwaha BK, Bhardwaj S, Ramawat N, Sharma S, Singh VP, Prasad SM, Chauhan DK, Dubey NK, Sahi S (2020) Silicon tackles butachlor toxicity in rice seedlings by regulating anatomical characteristics, ascorbate-glutathione cycle, proline metabolism and levels of nutrients. Sci Rep 10:14078 Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rend Lincei-Sci Fis 19:325–346 Upadhyaya H, Sahoo L, Panda SK (2013) Molecular physiology of osmotic stress in plants. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer, New York, pp 179–192 Varalakshmi S, Anjaneyulu E, Balaji M (2014) Salicylic acid alleviates aluminum toxicity in tomato seedlings (Lycopersicum esculentum Mill.) through activation of antioxidant defense system and proline biosynthesis. Adv Biosci Biotechnol 5:49320 Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376 Venekamp JH, Koot JTM (1984) The distribution of free amino acids, especially of proline, in the organs of field bean plants, Vicia faba L., during development in the field. J Plant Physiol 116:343–349 Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759 Verbruggen N, Hua XJ, May M, Van Montagu M (1996) Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proc Natl Acad Sci U S A 93:8787–8791 Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant environment interaction. Arabidopsis Book 8:e0140. American Society of Plant Biologists. Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM (2017) Citrus plants exude proline and phytohormones under abiotic stress conditions. Plant Cell Rep 36:1971–1984 Wang Y, Peng X, Salvato F, Wang Y, Yan X, Zhou Z, Lin J (2019) Salt-adaptive strategies in oil seed crop Ricinus communis early seedlings (cotyledon vs. true leaf) revealed from proteomics analysis. Ecotoxicol Environ Saf 171:12–25 Wen JF, Gong M, Liu Y, Hu JL, Deng MH (2013) Effect of hydrogen peroxide on growth and activity of some enzymes involved in proline metabolism of sweet corn seedlings under copper stress. Sci Hortic 164:366–371 Wu L, Fan Z, Guo L, Li Y, Zhang W, Qu LJ, Chen Z (2003) Over-expression of an Arabidopsis δ-OAT gene enhances salt and drought tolerance in transgenic rice. Chin Sci Bull 48:2594–2600 Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975–1981 Yamchi A, Jazii FR, Mousav A, Karkhane AA, Renu (2007) Proline accumulation in transgenic tobacco as a result of expression of Arabidopsis Δ1-pyrroline-5-carboxylate synthetase (p5cs) during osmotic stress. J Plant Biochem Biotechnol 16:9–15 Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchi-Shinozaki K, Wada K, Harada Y, Shinozaki K (1995) Correlation between the induction of a gene for delta(1)pyrroline-­5-­carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J 7:751–760

Plant Performance and Defensive Role of Proline Under Environmental Stress

223

Zaid A, Mohammad F, Fariduddin Q (2020) Plant growth regulators improve growth, photosynthesis, mineral nutrient and antioxidant system under cadmium stress in menthol mint (Mentha arvensis L.). Physiol Mol Biol Plants 26:25–39 Zanella M, Borghi GL, Pirone C, Thalmann M, Pazmino D, Costa A, Santelia D, Trost P, Sparla F (2016) β-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress. J Exp Bot 67:1819–1826 Zhang HQ, Croes AF, Linskens HF (1982) Protein synthesis in germinating pollen of petunia— role of proline. Planta 154:199–203 Zhang C, Wang N, Zhang Y, Feng Q, Yang C, Liu B (2013) DNA methylation involved in proline accumulation in response to osmotic stress in rice (Oryza sativa). Genet Mol Res 12:1269–1277 Zhang M, Huang H, Dai S (2014) Isolation and expression analysis of proline metabolism-related genes in Chrysanthemum lavandulifolium. Gene 537:203–213 Zhang YB, Yang SL, Dao JM, Deng J, Shahzad AN, Fan X, Li RD, Quan YJ, Bukhari SAH, Zheng Z (2020) Drought-induced alterations in photosynthetic, ultrastructural and biochemical traits of contrasting sugarcane genotypes. PLoS One 15(7):e0235845 Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767 Zhu B, Su J, Chang M, Verma DS, Fan YL, Wu R (1998) Overexpression of a Δ1-pyrroline-5-­ carboxylate synthetase gene and analysis of tolerance to water-and salt-stress in transgenic rice. Plant Sci 139:41–48 Zouari M, Ahmed CB, Elloumi N, Bellassoued K, Delmail D, Labrousse V, Abdallah FB, Rouina BB (2016) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Saf 128:195–205 Źróbek-Sokolnik A (2012) Temperature stress and responses of plants. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer Science + Business Media, LLC, New York, pp 113–134

Plant Performance and Defensive Role of Glycine Betaine Under Environmental Stress Praveen Jain, Brijesh Pandey, Pratibha Singh, Ranjana Singh, Satarudra Prakash Singh, Sashi Sonkar, Rahul Gupta, Saurabh Singh Rathore, and Akhilesh Kumar Singh

Abbreviations APX Ascorbate peroxidase BADH Betaine aldehyde dehydrogenase CAT Catalase CMO Choline monooxygenase GB Glycine betaine GR Glutathione reductase GSH Glutathione MDA Malondialdehyde ROS Reactive oxygen species SOD Superoxide dismutase P. Jain Department of Botany, Government Chandulal Chandrakar Arts and Science PG College Patan, Durg, Chhattisgarh, India B. Pandey · S. P. Singh · S. S. Rathore · A. K. Singh (*) Department of Biotechnology, School of Life Sciences, Mahatma Gandhi Central University, East Champaran, Bihar, India e-mail: [email protected] P. Singh Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India R. Singh Govt. Model Degree College, Constituent College of CCS University (Meerut) Arniya, Bulandshahr, Uttar Pradesh, India S. Sonkar Department of Botany, Bankim Sardar College, Tangrakhali, South 24 Parganas, West Bengal, India R. Gupta Amity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow, Uttar Pradesh, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_9

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1  Introduction Adverse conditions like abiotic stresses disrupt the normal functioning of living organisms together with the entire ecosystem. At the same time, adverse environmental conditions cause a system to resist or recover from the impairment triggered due to alteration. Resilience is the ability to retain the intrinsic quality as well as identity, while experiencing adverse environmental conditions like drought, salinity, extreme temperatures, heavy metal toxicity, and so on. Such environments let the plant system to react or acclimatize. Generally, the plant system reaction as a whole is composed of reactions of each cells against the ecological environments like abiotic stresses, etc. The abiotic stresses like drought, high salinity, extreme temperatures, heavy metals, ultraviolet-B radiation, water logging, etc., are found to harshly affect the agricultural plant growth/crop production (Kumar 2013; Getnet et  al. 2015; Embiale et al. 2016; Hussein et al. 2017; Husen et al. 2017, 2018, 2019; Iqbal et al. 2020a, b; Rani et al. 2020; Sonkar et al. 2021a, b; Porwal et al 2021; Misra et al. 2021). However, plants have developed various morphological, physiological, and molecular modifications as well as environmental interactions so as to acclimatize with their surroundings (Husen 2009, 2010, 2013; Husen et  al. 2014, 2016; Surabhi 2018; Zhang et  al. 2019; Siddiqi and Husen 2017, 2019;  Sonkar et  al. 2021c). Overall, the cellular metabolic adjustment is the left option for plant system in order to stay alive in abiotic stresses environments since they cannot change their place. Under such stresses, the plant system get trigger towards the cytoplasmic accumulation of some lower molecular weight organic materials, which are together called “compatible solutes” (Surabhi et al. 2000; Roychoudhury et al. 2015). Such solutes are not only membrane-impermeable tiny organic compounds, but also soluble in water. They can buildup massively having high cytoplasmic concentration (0.2 M) under stress condition (Kurepin et al. 2015). These are osmoprotectants like glycine betaine, proline, trehalose, glycerol, sorbitol, mannitol, and so on, which assist the living system to stay alive under intense osmotic stress. Reactions of osmotic stress comprise a set of cellular biochemical as well as physiological acclimatization like modifications in the composition of plasma membrane and formation of plant hormones together with alteration of osmotic potential (Beales 2004). The osmoprotectants assist significantly towards guarding cells from cell-damaging stress conditions (Rabbani and Choi 2018). These osmoprotectants assist towards balancing the osmotic homeostasis of agricultural plants under diverse abiotic stresses (McCue and Hanson 1990; Kishitani et al. 1994; Surabhi et al. 2000, 2003; Husen 2010; Surabhi 2018; Xu et al. 2018). Among osmoprotectants, glycine betaine is able to execute many roles as nonenzymatic antioxidant. It significantly retains the normal cellular physiological responses in plant systems under adverse environments, thereby offering abiotic stress tolerance in various plant species with improved growth and development together with enhanced yield. The present chapter is an attempt to throw lights on diverse plant reactions in the form of GB synthesis/accumulation under various environmental stress conditions, which result in the development of tolerance mechanism in plant systems. Further, it also emphasizes

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on the probable mechanisms of resilience as well as tolerance at physiological level in plant systems.

2  Glycine Betaine Glycine betaine (GB) is extensively occurring in bacteria, algae, and higher plants including animals (Rhodes and Hanson 1993; Prasad and Pardha-Saradhi 2004). Based on the precursors as well as enzymes, it has been reported that there are many routes involved in the formation of GB (Sakamoto and Murata 2000). However, in higher plant systems, GB is formed through a two-step oxidation of choline by means of lethal betaine aldehyde as intermediate (Cromwell and Rennie 1953). Plant systems capable of forming and accumulating GB are termed as natural accumulators, while those that failed to do so naturally are called as non-accumulators (Chen and Murata 2011). The GB accumulating potentials vary among the different plant systems together with organs (Chen and Murata 2011). The occurrence as well as distribution pattern of GB in diverse halophytes growing on sand humps and swampland including agricultural fields pointed out the promising functions of GB towards overcoming the stress environments (Storey et al. 1977). GB is solvable in quaternary ammonium compound with no toxic effects on cells (McDonnell and Wyn Jones 1988; Cleland et  al. 2004). This is dipolar in nature and found to be electrically neutral at physiological pH (Rhodes and Hanson 1993). It efficiently stabilizes the enzymatic as well as complex protein quaternary structures, acts as safeguards towards different constituents of the photosynthetic apparatus like ribulose-­ 1,5-biphosphate carboxylase/oxygenase (Rubisco) as well as the O2-­ producing photosystem II (PS II) (Murata et al. 1992; Rhodes and Hanson 1993; Lee et al. 1997; McNeil et al. 1999; Nayyar et al. 2005a, b; Shahbaz et al. 2011), preserves the highly well-ordered condition of membranes at nonphysiological temperatures, and alleviates the impairment caused due to oxidative stress (Zhao et al. 1992; Rajashekar et al. 1999; Sakamoto and Murata 2002; Nayyar et al. 2005a, b; Chen and Murata 2011; Fariduddin et al. 2013). Abiotic stress-mediated oxidative stress results into excessive formation of reactive oxygen species (ROS), where GB plays an important role towards alleviating the same oxidative damage in plant systems (Das and Roychoudhury 2014). For instance, the externally treated GB not only substantially diminished the chilling-mediated formation of H2O2, but also decrease the plasma membrane impairment in cotton plants (Su and Wu 2004; Cheng et al. 2018). GB does not mitigate ROS directly, but overcomes its harmful impacts through triggering/stabilizing ROS-overcoming enzymes and/or inhibiting the ROS formation by other mechanisms. Nevertheless, some investigators found the cellular signaling function of ROS at low concentrations, thereby controlling growth as well as development of plant systems including many characteristics resulting in stress adaptation (Ismail et al. 2014). Development of distinctive cellular repair mechanisms is one of the notable characteristics of plant systems, which not only preserve the redox state but also decrease the oxidized macromolecules to

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their earlier reduced conditions in cells (Krishnamurthy and Rathinasabapathi 2013). Such cellular repair mechanisms include antioxidant system consisting of enzymatic as well as nonenzymatic constituents, which either mitigate or detoxify ROS (Hasanuzzaman et al. 2012, 2017). Once appropriate signaling, GB accumulating in plant cells under abiotic stress environments lead to tolerance as well as resiliency. Xu et  al. (2018) conducted one study in which the osmotic stress-­ mediated growth inhibition was overcome through the treatment of exogenous GB. However, the osmotic stress-mediated generation of GB is expected to be regulated through jasmonic acid (JA) signaling. Inhibition of JA formation considerably diminishes the GB biosynthesis. The chloroplasts of younger leaf cells of plant systems are the key location of endogenous GB formation under abiotic stress (Park et al. 2007; Chen and Murata 2011). If we assume osmoregulation of cell as reaction to drought or salinity or some other abiotic stresses, then osmotic hardening with modifications of cytoskeleton are the resilience depicted by the cellular system. Preliminary reaction towards abiotic stresses involves an enhancement towards the formation of any or both of two “stress” hormones, i.e., abscisic acid (ABA) and salicylic acid (SA). Enhancements in the contents of ABA as well as SA result in the decline towards the formation or function of plant growth hormones like gibberellins, auxin, and cytokinins (Kurepin et al. 2017). Plant systems that generate higher GB cause improved interaction among plant hormones and enhanced growth as well as photosynthetic activity and therefore offer enhanced stress adaptation (Kurepin et al. 2017). Ripoll et al. (2009) conducted study concerning memorizing the abiotic stimulus by cellular machinery with potential role of Ca2+ during the process. Likewise, the investigation carried out by Xu et al. (2018) on watermelon cell lines are also important, where it was observed higher formation as well as maintenance of GB contents once cells were subjected to osmotic stress. This is possibly an acclimatization mechanism.

3  Location of GB Inside the Cell and Effectiveness The GB formation as well as its further accumulation is genotype specific. This means that for reaction, the entire plants are not reliant on GB. Usual GB accumulating plant systems are associated with genes responsible for producing precursor either through choline or through glycine (Sakamoto and Murata 2002). There is also report regarding the translocation of GB from old to young leaves as well as leaves and roots to other portions of plants (Chen and Murata 2011). Further, exogenous applications of GB or endogenously produced GB both by naturally or by transferred genes lead to protective responses followed by resilience. Although GB is situated in the cytoplasm, vacuoles, chloroplasts, as well as other sites with diverse concentrations, it is reported to be more operative inside the chloroplast over cytoplasm towards stress responses excluding osmotic/osmoregulatory kind response (Park et al. 2007). The chloroplasts of newer leaf cells of plant systems are the chief location of intracellular GB formation under abiotic stress (Park et  al.

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2007; Hattori et al. 2009; Chen and Murata 2011). The translocation of GB takes place largely through the phloem from the key producing locations such as leaves (Mäkelä et al. 1996; Hattori et al. 2009). An interesting study revealed the greater formation of GB inside the older leaves as compared to newer leaves. However, roots depicted substantially lower production of GB. It was concluded that translocation of GB occurs from older to newer portions of plant systems so as to guard them (Annunziata et al. 2019).

4  GB-Mediated Resilience Mechanisms in Plant System Plant system depicted five kinds of resilience mechanism, i.e., recovery, tolerance, avoidance, escape, and adaptation. It is advocated that GB can provide stability to membranes, act as safeguard to protein molecules together with photosystem II, and alleviate the oxidative damage (Chen and Murata 2011). The enhancement in abiotic stress adaptation facilitates the  plant systems to guard their photosynthetic machinery by chloroplast-generated GB contents (Kurepin et al. 2015). Plant stress hormones trigger the expression of related genes that decrease the formation of normal growth hormones such as auxin, gibberellins, as well as cytokinins. Subsequent growth inhibition can be overcome through the formation/accumulation of GB triggered by JA signaling. Also, the GB was translocated to all organs as a result of treatment of the plant leaves with externally applied GB (Mäkelä et  al. 1996). In GB formation, the synthesis of choline monooxygenase (CMO) and NAD+-dependent betaine aldehyde dehydrogenase (BADH) has been also advocated as abscisic acid-independent (Kalinina et  al. 2012). The formation of GB involves a two-step oxidation from choline and betaine aldehyde, catalyzed by CMO and BADH, correspondingly. Upregulated gene expression of BADH as well as CMO triggered through stress is clearly detected; nevertheless the signal transduction is not well understood. In addition, it was also reported that GB-mediated chilling adaptation of sweet pepper was achieved through increasing antioxidant gene expression as well as enzymatic activity (Wang et al. 2016). Cellular formation as well as accumulation of GB with other osmoprotectants is the reaction that is included in the class of tolerance type response. These involve the following mechanisms (Fig. 1): 1. JA signaling pathway mediated GB accumulation: To react under osmotic stress, the plant hormones like ABA, ethylene (ET), as well as JAs were extensively detected to trigger the expression of stress linked genes with formation of secondary metabolites (Zhou and Memelink 2016). The osmotic stress-mediated growth inhibition might be overcome through exogenous supplemented GB. The osmotic stress-mediated formation/accumulation of GB is possibly regulated by JA signaling. Fabrication, accumulation, as well as signaling were based on SA, JA, ET, and so on (Xu et al. 2018); merely the methyl jasmonate (MeJA) exposure/treatment triggered an equivalent rise in GB level. While other treatments

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Exposure of plants to resilient and or stress environments

Initial Response: Signal transduction by jasmonic acid or methyl jasmonates

Resilience response mechanisms after biosynthesis and accumulation of glycine betaine (GB)

Phytohormones

Osmoprotective

Protein stabilization

ROS damage control: scavenging of ROS

Memory based resilience mechanism

Stress hormone production, reduces growth hormone production

Amelioration of salinity stress, production phytoalexins, etc., fluid homeostasis with increased accumulation of calcium and reduction in sodium levels

Increased activity enzymatic antioxidants; increased regulatory gene transcription

Enzyme stabilization, protection of pigments/ macromolecules stop K+ efflux

Adaptation and drought hardening by maintaining levels of GB after the stress is over

Fig. 1  The GB-mediated resilience mechanisms in plant system under major environmental stress conditions

might merely trigger feebler accumulation. Such results pointed out that the GB formation can be largely facilitated by JA signaling pathway (Xu et al. 2018). 2. GB-mediated ROS scavenging activity: Nearly all types of abiotic stresses lead to an oxidative burst with the formation of ROS. Efficient ROS mitigation by nonenzymatic antioxidants like ascorbate (AsA), glutathione (GSH), etc., and enzymatic antioxidants such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), and so on is essential towards preserving the biological processes under adverse environments (Banerjee and Roychoudhury 2017). Rises in GB content might also be connected to stress acclimatization through improved CAT and SOD activities as well as the decrease of plasma membrane impairment by controlling lipid peroxidation together with ion homeostasis route (Alasvandyari et al. 2017). 3 . GB-mediated osmoprotection/osmoregulation: Accumulation of osmoprotectants like GB and so on results in consequent osmoregulation. The GB biosynthesis and accumulation that trigger upon exposure to salinity lead to protection of plant cells from salt stress through osmoregulation/osmotic adjustment (Gadallah 1999). The GB-mediated osmoprotection is found to take place as a result of improved ion homeostasis (Lutts et al. 1999). These osmoprotectants are accompanying with adaptation or resistance mechanisms that involve the generation of defense-related compounds like phytoalexins and so on. Generally, osmoprotectants are soluble substances occurring inside a cell, which play substantial functions towards retaining the fluid homeostasis (Khan et al. 2017). GB also improved fruit quality through enhancement of protein formation with

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enhanced accumulation of Ca2+ together with decrease in sodium contents in the course of waterlogging environments (Rasheed et al. 2018). 4. GB-mediated stabilization of biological molecules: Several studies advocated that GB was capable to safeguard the biomolecules like nucleic acids, proteins, and lipids that are rich in nitrogen as well as carbon contents to be exploited as energy sources (Umezawa et al. 2006). 5 . Memory based resilience mechanism: The current studies revealed that plant systems associated with memory mechanism that that involves the history of stimuli they were subjected to (Ripoll et al. 2009). For instance, as soon as plant systems expose to osmotic stress for a second time, they can memorize the stored information followed by playing a significant function towards adaptation/tolerance. Remarkably, although osmoprotectants like proline undergo instant reduction once the stress condition is overcome, nevertheless the GB remains stable in plant systems (Ashraf and Foolad 2007). These results provide a new picture towards the function of GB to drought-hardening in which plant can translocate the preexisting GB to newly produced cells and also recall the earlier stress stimuli and therefore keeps GB at higher content in newly produced tissues (Mäkelä et al. 1996; Xu et al. 2018).

5  G  B-Mediated Responses and Resilience Under Diverse Abiotic and Biotic Stresses The GB plays an important role in overcoming the diverse type of stress conditions like waterlogging, salinity low temperature/cold, heavy metal, pathogenic organisms, drought, halogens, high temperature, light stresses, etc., experienced by the plant systems. Table 1 provides a highlight on the aforementioned stresses experienced by different plant species that resulted into enhanced accumulation of GB followed by resilience response. This section involves the resilience responses of various plants under diverse stress conditions, which are as follows:

5.1  Waterlogging Waterlogging/flooding stress imposes severe threat towards plant survival as a result of disturbing the nutritional balance as well as hindering various physiological/biochemical activities of the plants. Such events cause impairment towards the growth and development that eventually lead to loss of yield (Hasanuzzaman et al. 2017). Exploitation of diverse externally applied protectant to overcome the waterlogging/ flooding stress is found to be common in plant science. Nonetheless, the promising exploitation of GB for relieving the impacts of waterlogging/flooding stress in plants is very uncommon. It was observed that exogenous exploitation of GB as

Pathogen

Salinity

Halogen

Salinity

Salinity

Salinity

Heavy metal

Cold/chilling

Osmoregulation, osmoprotection as well as hardening Increased ROS production

Resilience pathway Osmoregulation, osmoprotection as well as hardening Osmoregulation, osmoprotection as well as hardening Overproduction of GB caused improved acclimatization/adaptation of the photosynthetic machine to drought/heat stress up to 40 °C Enhanced temperature tolerates up to 42 °C through GB accumulation Gb mediated improved adaptations to light stress with guard of the photosynthetic apparatus Externally supplemented GB enhanced chilling tolerance Externally supplemented GB resulted into mitigation of cadmium toxicity Externally supplemented GB improved the oil quality

Glycine betaine-mediated tolerance/response GB accumulation improves chilling tolerance

Osmoregulation, osmoprotection as well as hardening Cotton plant Mitigation of physiological/ seedlings photosynthetic/oxidative injuries Sunflower Protecting cellular structures in the course of fatty oil formation and storage Triticum durum Osmotic modification in cells of root Overaccumulation of GB improved the salt tolerance (Wheat) ability Wheat chloroplasts are protected due to accumulation Triticum durum Improve the functioning of thylakoid of GB content (Wheat) membrane (may be by defending protein molecules) Cajanus cajan L. Probably GB defends protein Externally supplemented GB mitigated the sodium molecules/enzymes fluoride stress By stimulating potassium efflux Enhancement in salt tolerance as a result of Triticum durum (Wheat) accumulation of GB content Pennisetum glaucum Inhibited sporangial sporulation, Externally supplemented GB improved the seed L. zoospore release together with motility germination as well as seedling vigor

Saccharum sp. HSF-240 (sugarcane) Transgenic Arabidopsis Peach fruit

Higher temperatures Light

Higher temperatures

Plant sp. type Hybrid maize (Zea mays L.) Triticum durum (Wheat)

Stress type Cold/chilling

Table 1  Summary of GB-mediated plant resilience responses under different stress environments

Lavanya and Amruthesh (2017)

Wei et al. (2017)

Yadu et al. (2017)

Farooq et al. (2016) Bakhoum and Sadak (2016) Annunziata et al. (2017) Tian et al. (2017)

Shan et al. (2016)

Rasheed et al. (2010) Wani et al. (2013)

Key references Farooq et al. (2008) Wang et al. (2010)

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Water logging

Heavy metal

Heavy metal

Cold/chilling

Stress type Drought

Resilience pathway Osmoregulation mediated jasmonate signaling Osmoregulation, osmoprotection as well as hardening Mitigation of oxidative burst and modulation of morphology

Sorghum bicolor (HJ541 and SSG 59-3) Brassica oleracea L. Mitigation of oxidative burst and modulation of morphology Physalis peruviana Improvement in stomatal conductance (Cape Gooseberry)

Plant sp. type Citrullus lanatus (cell line) Cottons seeds

Externally supplemented GB caused mitigation of water logging

Mitigation of chromium toxicity

Glycine betaine-mediated tolerance/response Externally supplemented GB improved the drought tolerance/adaptations GB mediated improved tolerance towards chilling stress Externally applied GB mediated improved chromium toxicity Ahmad et al. (2020) Castro-Duque et al. (2020)

Cheng et al. (2018) Kumar et al. (2019)

Key references Xu et al. (2018)

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foliar spray on cape gooseberry plant increased the adaptation with respect to improved water tolerance coefficient as well as leaf area (Castro-Duque et al. 2020). Rasheed et al. (2018) examined the influence of GB on the growth as well as the physiology of tomato plants under waterlogged conditions. It was found that waterlogging not only increased the malondialdehyde (MDA) level, but also worsened the integrity of membranes including the enhanced concentration of sodium as well as decreased concentrations of potassium and calcium in the different parts of the plant. In contrast, treatment of tomato plants with GB under waterlogged condition was found to diminish the MDA level and enhance the integrity of membrane with nutritional status of the tomato plants that led to waterlogging stress acclimatization/adaptation.

5.2  Salt Stress/Salinity Saline soil can be defined as any soil comprising high soluble salts concentration equal to nearly 40 mM NaCl that can generate 0.2 MPa osmotic pressure. This kind of soil can show impact of salt stress on plant systems through decreasing the plant growth and development including yield (FAO 2008). Globally, the salt stress/salinity is the major stress condition that biosphere has yet to face in all the agricultural fields. Among abiotic stresses that upset crop yields, approximately 20% of world soil is exposed to salinity stress. However, it can further enhance up to 50% of global cultivated land by 2050 (Epstein et al. 1980). It is assessed that salinity is not only upsetting almost 950 million hectares of land globally but also imposing the foremost constraint on food crops (Ashraf 2002). Further, it is evaluated that 8.6 million hectares of land area in India is extremely vulnerable towards salt stress/ salinity (Pathak et al. 1999). Interestingly, intracellular GB formation and accumulation results in relieving the plant system from salt stress. This is supported by the fact that sea salt (sodium chloride) mediated salinity stress in transgenic tobacco depicted improved adaptation as a result of GB accumulation (Lilius et al. 1996). Biosynthesis as well as accumulation of GB improved flower formation in genetically modified Arabidopsis plant exposed to salt stress (Sulpice et  al. 2003). Externally supplemented GB led to increased photosynthetic activity under salt stress in maize plant (Yang et  al. 2005). Sunflower (Helianthus annuus L.) seed supplemented with GB led to improved salt adaptation through enhancing photosynthetic pigments, growth, as well as developmental stages. In addition, the externally supplemented GB enhanced the oil quality of Helianthus annuus L. through guarding cell structures in the course of formation of fatty oil as well as storage (Bakhoum and Sadak 2016). The externally supplemented GB in Oryza sativa exposed to salt stress was found to enhance height, fresh weight, dry weight, total chlorophyll together with proline levels and diminished MDA content (Yao et al. 2016). The Triticum durum (wheat) once exposed to salinity stress, the intracellular GB formation and its accumulation mitigated the same stress through osmotic modification within root cells (Annunziata et al. 2017). Also, excess formation of GB

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led to the improved functioning of thylakoid membrane under salt stress conditions (Tian et al. 2017). The GB was also reported to play an important role for increasing salt acclimatization through triggering potassium efflux (Wei et  al. 2017). Khan et al. (2014) examined the impact of salinity stress in mung bean (Vigna radiata L.) in saline condition (100 mM NaCl), where it was observed that GB level improved by 31.9% in salt-supplemented plants over control plants. Tsutsumi et  al. (2015) exposed Atriplex gmelini plants with NaCl having concentrations of 0, 50, and 250 mM. It was detected that all these salt treatments improved GB level in both bladder hairs and leaf laminae. However, the treatment with high salinity of 250 mM NaCl revealed a substantial enhancement of GB accumulation in bladder hairs over leaf laminae.

5.3  Low Temperature or Cold GB has been considered to be cryoprotectant due to its osmoregulatory function (Cleland et al. 2004). An exogenous application of GB enhances chilling tolerance of peach fruit during cold storage (Shan et al. 2016). Some GB synthesis related genes like codA and betA had been reported to enhance plant tolerance against cold conditions (Sakamoto et al. 2000; Quan et al. 2004). Plants modified with gene betA reported to show significantly higher tolerance to low temperature with improved photosynthetic performance and higher accumulation of total soluble sugar (Quan et al. 2004). Zhang et al. (2010) conducted an experiment to understand the role of GB biosynthesis in developing tolerance in Triticum aestivum under cold stress. They used wild-type cv. Shi 4185, and three transgenic lines—T1, T4, and T6 (expressing the BADH gene isolated from Arabidopsis hortensis L.) for this purpose. They found a significant high level of GB content in all types of plants after 2  days of cold treatment (2/0  °C day/night temperature), but the increment was noticed to be higher in transgenic plants than wild type. Expression of BADH genes in transgenic plants increased the GB content which augments plant tolerance to cold stress. GB accumulation improves chilling tolerance in hybrid maize (Farooq et al. 2008). Application of GB at bud stage in cold-stressed chickpea (Cicer arietinum L.) reported to improve flower functioning in terms of pollen viability, pollens germination (in vitro and in  vivo), growth of pollen tube, pollen receptivity of stigma, and ovule viability. Consequently it improves crop production by increasing floral retention, pod formation, and pod retention by 47%, 38%, and 23%, respectively, in cold-stressed chickpea as compared to wild type (Nayyar et al. 2005a, b). Foliar application of GB efficiently improves plant growth by ameliorating the adverse effects of cold stress in tomato plant (Lycopersicum esculantum Mill. cv. Moneymaker). GB translocated and accumulated in different plant parts with the highest accumulation in meristematic tissues of shoot apices and flower buds. In leaves, it is mainly present in the cytosol and only 0.6–22% of the total GB present in leaf was reported to localize in chloroplasts. GB treatment increased about twofold more accumulation of H2O2 content in tomato plants after 3 days of cold stress

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(Park et al. 2006). Similar to this, GB treatment was applied to make cold-tolerant cotton (Gossypium hirsutum cv. Lumianyan19) plants. GB treatment increases seed germination up to 93%. Higher accumulation of GB in leaves (25.6%) and increase in chlorophyll content help plants to tolerate low temperature by improving other physiological processes like photosynthesis and antioxidative system (Cheng et al. 2018). Resurgence of the cell from chilling/cold stress is entirely observed at membrane trafficking level (Einset et al. 2007).

5.4  Drought A large number of research works have been done to understand the role of GB in ameliorating the adverse effects of drought stress and developing drought tolerance in plant. Exogenous application of GB improved morphological as well as physiological parameters in tomato (Rezaei et  al. 2012). Two cultivars of tobacco (Nicotiana tabacum L.), drought-tolerant (DHJ5210) and drought-sensitive (ZY100), were studied to know the effects of foliar-exposure of GB (80 mM) under well-watered and water-deficit conditions. It was observed that a drought-tolerant cultivar (Cv. DHJ5210) absorbed more GB than Cv. ZY100  in the leaves under stress conditions. GB application favors plant growth by improving water status under drought stress (Ma et al. 2007). An improvement in growth and shoot biomass was observed in GB-exposed tobacco plants (Ma et al. 2007). Similarly, Kurepin et al. (2015) also observed that spray of GB enhanced stress tolerance in drought-­ stressed pot-grown tobacco plants that were related to increased stomatal conductance, an increased efficiency of PSII, higher carboxylation efficiency of CO2 assimilation, and better photosynthesis (Ma et  al. 2007; Kurepin et  al. 2015). Besides, foliar exposure of GB to drought-stressed cotton plant (Gossypium hirsutum L.) improved growth, yield, and quality of cotton as it improved chlorophyll content, photosynthetic potential, transpiration rate, and intercellular CO2 concentration in drought-stressed plant as compared to wild-type plants (Ahmad et  al. 2014). GB application increased shoot dry weight, leaf area, photosynthetic rate, and transpiration rate by 27%, 42%, 30%, and 40%, correspondingly, in seedlings of pepper (Capsicum annuum) under water stress conditions as compared with non-­ GB-­treated plants (Korkmaz et al. 2014). Likewise, exogenous application of GB at flowering stage was found to be more effective in improving crop yield and production of hybrid sunflower (Helianthus annuus L. Hysun-33) than in the vegetative stage under water stress. Foliar exposure of GB at flowering stage increased the head (inflorescence), number and weight of achenes per head that in turn improved oil yield of sunflower plant (Hussain et al. 2008). Foliar application of GB at tillering and anthesis stages in 19 genotypes of wheat (T. aestivum) improved the number of grains per spike and thousand grain weight to a certain extent in most genotypes under drought stress, out of them BW 9183, BW 9097, and PBW 550 reacted extensively to GB treatment (Gupta and Thind 2017). Likewise, seed and foliar treatment of GB at flowering stage has been reported to increase the cumin (Cuminum

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cyminum cv. Mashhad) yield by 24% under drought stress (Armin and Miri 2014). Besides, an increase in GB biosynthesis in plants also improved drought tolerance in plants (Sulian et al. 2007). Pusa Basmati 1 (variety of rice) having codA gene was found to be highly tolerant to salt stress and drought stress (Mohanty et al. 2002; Kathuria et al. 2009). Transgenic potato plant modified with BADH gene of spinach exhibited significantly high tolerance to drought and salt (Zhang et  al. 2011). Drought hardening can play a significant role in developing the drought tolerance and hence improving the survival rate when plants unavoidably encounter various abiotic stresses in their life (Yang et al. 2015). Ibrahim et al. (2018) compared the level of osmolyte accumulation in two cotton genotypes, Zhongmian 23 (stress tolerant) and Zhongmian 41 (sensitive). They observed that the stress-tolerant genotype exhibited more tolerance due to increased level of GB, soluble sugar, and K+ in response to both drought (4% soil moisture) and salinity stress (200  mM NaCl), while Zhongmian 23 exhibited higher activities of antioxidative enzymes like SOD, POD, CAT, APX, and Na+/K+-ATPase.

5.5  Halogen Fluoride present in irrigation water is reported to be very toxic to plants and crops. It persists in environment for long in air, water, and soil. It produces a collective stress on plants by causing chlorosis, inhibition of growth, and competition to mineral absorption. Fluoride exposure induces overproduction of various ROS including hydrogen peroxide, superoxide, and hydroxyl radical which may cause oxidative damage in lipids, proteins, and nucleic acids and result in membrane disruption and abnormal cell functions if not scavenged by intrinsic antioxidant enzymes like SOD, POD, and catalase readily. Abiotic stress imposed by fluoride may also cause mutation in DNA by altering polymerase activity. Pretreatment of seeds with sodium fluoride (NaF, 75 ppm) solution caused 68% reduction in dry weight of Cajanus cajan L. seedlings on fifth day of treatment; however, NaF-induced adverse effects were managed to alleviate by applying 50 μM  GB with NaF, which as a result reported to improve biomass productivity, root length, and seedling vigor (Yadu et al. 2017). Heavy metal cadmium (Cd), as a toxic heavy metal, has been selected to study the impacts of heavy metal stress in the plants. The morphological, physiological, and biochemical responses of various plant species to Cd stress had been widely studied by Farid et al. (2013). GB had been recently found to mitigate heavy metal toxicity by suppressing AOS induced-oxidative stress and by modulating morphological and physiological attributes in variety of plants like cotton and Brassica oleracea L. (Farooq et  al. 2016; Ahmad et  al. 2020) and hence plays a crucial role to impart tolerance to plants against various metals/metalloids (Bhatti et al. 2013). GB has been found to ameliorate (Cr) toxicity in Sorghum (HJ541 and SSG 59-3). GB (100 mM) significantly improved shoot length, root length, chlorophyll content, enzymatic antioxidants (SOD, POD, GR, polyphenol oxidase, etc.), and nonenzymatic antioxidants like ascorbate, proline, and glutathione in Cd-treated

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plants (Kumar et al. 2019). GB treatment reduces the oxidative damage caused by metal stress. Ali et al. (2015) reported a decrease in Cr concentrations in GB-exposed wheat plants. GB application mediates various biochemical processes that help in detoxifying heavy metals. For instance, Islam et al. (2009) exposed CdCl2 (100 mM) treated suspension-cultured cells of Nicotiana tabacum L. to 1 mM and 10 mM GB and observed that GB exposure at 10 mM remarkably decreased the MDA level in Cd-treated cell suspension while GB exposure at 1  mM was unable to decrease MDA content. Moreover, Cd accumulation was reported to decrease in both 1 mM and 10 mM GB-treated cell suspension. Similarly, reduction in MDA content was also observed in Cd-stressed mung bean seedlings on GB application (Hossain et al. 2010). Exposure of GB (0.5, 1, 2, and 5 mM) to Lemna gibba plant treated with different doses of Cd (0.5, 1, and 3  mM CdSO4.7H2O) significantly reduced MDA content only at 0.5 mM GB in all Cd-stressed plants (Duman et al. 2011). Likewise, Bharwana et al. (2014) studied the defensive role of GB in cotton (MNH 886) plant against lead (Pb) stress [50 μM and 100 μM Pb(NO3)2]. They found that application of 1  mM  GB alleviates the adverse effects of Pb stress in cotton plants that was associated with reduction in both excessive electrolyte leakage and MDA production in both leaf and root of the Pb-stressed cotton plants. Nevertheless, excessive transpiration rate and water use efficiency considerably augmented in the Pb-stressed plant due to GB application, which in turn improve plant tolerance to metal stress. Rasheed et al. (2014) in an experiment exposed 2-week-old wheat cultivars, viz., Millat-2011 and Punjab-2011, to Cd stress. They observed that foliar application of GB in 1-week-old Cd-stressed plants improved Cd tolerance as they reported a sharp reduction in MDA content in Cd-treated plants after 2 weeks of metal treatment. In another experiment, Lou et al. (2015) has exposed seedlings of 53-day-old perennial ryegrass (Lolium perenne) to different concentrations of Cd (0–0.5 mM CdCl2) and GB (0, 20, and 50 mM) separately or in combination, hydroponically for 7 days and found that Cd stress significantly decreased the normalized relative transpiration and increased electrolyte leakage and MDA content. Exogenous GB mitigated the adverse effects of Cd stress on perennial ryegrass by increasing normalized relative transpiration and decreasing electrolyte leakage and MDA content in Cd-stressed plants. Besides, 20 mM GB application suppressed the Cd accumulation in both shoots and roots. It was concluded that exogenous application of 20 mM GB is the best strategy to ameliorate the damaging effects of Cd stress on perennial ryegrass. Similar results have also been reported by Farooq et al. (2016) in 4-week-old cotton genotype (MNH 886) treated with different Cd doses (0, 1.0, and 5.0 μM CdCl2) and GB (0 and 1 mM) for 6 weeks where GB application significantly increased transpiration rate and water use efficiency [except (1.0 μM CdCl2 + 1 mM GB) treatments] but decreased the levels of MDA and electrolyte leakage in both leaves and roots in contrast to respective only-Cd treatments. On the other hand, Pennisetum typhoideum seeds having radical were treated with Ni, GB and aspirin separately or in combination. Ni treatment increased the level of MDA and 4-hydroxy-2-nonenal and lipoxygenase (LOX), whereas decreased the membrane stability index (MSI). Application of GB in combination with Ni reversed the abovementioned parameters as it increased MSI by 122% and decreased the level of

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MDA, 4-hydroxy-2-nonenal, and LOX by 37, 17, and 23%, respectively, in Pennisetum typhoideum plants (Xalxo et al. 2017).

5.6  Herbicide In contrast to other stresses like salt, heavy metal, cold stress, high temperature, and so on that almost induced the biosynthesis and accumulation of GB in plants, herbicides suppressed the GB biosynthesis. Salt stress treatment induced the synthesis of GB while auxinic herbicides suppressed its biosynthesis in Kochia scoparia plant (Kern and Dyer 2009).

5.7  High Temperature Similar to cold tolerance, GB treatment improves plant performance under high temperature also. In a study, Vollenweider and Gunthardt-Goerg (2005) observed a significant increase in shoot biomass and rate of net photosynthesis in barley seedlings developed from the seeds pretreated with GB under high temperature, as compared to GB-untreated seeds. Alia et al. (1998) reported an increased tolerance to high temperature in transgenic plant of Arabidopsis modified for production of GB. Overaccumulation of GB enhances the tolerance of the photosynthetic apparatus to drought and heat stress in wheat (Wang et al. 2010), and hence wheat being a winter dwelling plant could tolerate high temperatures up to 40  °C.  Genetically modified tobacco plants had been examined for enhanced high temperatures tolerance after commencement of GB biosynthesis in a natural non-accumulator (Yang et al. 2005). Saccharum sp. (HSF-240) had been reported to tolerate up to 42 °C in contrast to control plants (Rasheed et al. 2010). Sorwong and Sakhonwasee (2015) checked the effects of GB in three marigold cultivars, namely, “Narai Yellow,” “Bali Gold,” and “Columbus Orange,” under heat stress conditions (39  °C/29  °C day/ night temperature). Heat stress conditions caused an increase in endogenous GB content which produced seedlings having a greater shoot biomass and also an increased net photosynthetic rate when germinated under heat stress conditions (Wahid and Shabbir 2005).

5.8  Light Stresses: UV-B and Gamma Radiation GB has been known to be involved in plant protection against various abiotic stresses by inhibiting ROS accumulation and by protecting the photosynthetic machinery from oxidative damages. Besides, it also provokes activation of some stress-related genes and protects quaternary structure of proteins and membranes

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from oxidative damage. Thereby, endogenous synthesis or exogenous application of GB could be implicated in maintaining the enzymes activity of plant defense system and to improve plant tolerance under environmental stresses (Sakamoto and Murata 2002). GB prevents excessive accumulation of AOS either by lowering their accumulation or by detoxifying them using antioxidative defense system, which in turn protect photosynthetic machinery, ion-channel proteins, and cell membranes integrity from the adverse impacts of light stress, alone or in presence of some other environmental stress (Wani et  al. 2013). GB accumulation is reported to be protected by various components of photosynthesis, such as (RUBISCO) ribulose-1, 5-bisphosphate carboxylase/oxygenase, photosystem II and quaternary enzyme and protein complex structures under environmental stresses (Hasanuzzaman et  al. 2019). It is well understood that light stress including radiations like UV-B and Gamma adversely affects the photosynthetic performance of plants by affecting chloroplast machinery. Experiments with transgenic Arabidopsis revealed improved tolerance towards light stress (Alia et al. 1999; Mittler 2002). In a study, Moussa and Jaleel (2010) explored the role of GB in Fenugreek plant under gamma-induced stress. For this, they exposed dry seeds of Fenugreek to different doses of irradiation [(0.0, 25, 50, 100, and 150 Gray (1 Gray = 100 rad)], using a gamma source (strength of 500 Ci; dose rate—0.54 Gy min−1). Then, these seeds were soaked in 50 mM of GB for 24 h and allowed them to grow for 30 days. It was reported that gamma radiation treatment alone reduced the accumulation of reducing, non-reducing, and total soluble sugars. Contrary to this, these sugars were found to be considerably high in plants developed from GB-soaked irradiated seeds, which are indicative for protective role of GB against gamma radiation stress (Moussa and Jaleel 2010). Hence, GB protection was more effective against gamma radiation stress at lower doses.

5.9  Pathogen It has been recently reported that GB treatment improves the host response against the fungal pathogen. GB treatment triggered the host defense responses of pearl millet (Pennisetum glaucum L.) during downy mildew infection caused by Sclerospora graminicola. 30  mg  mL−1 concentration of GB for 6  h significantly increased the seed germination and seedling vigor as well as inhibited sporangial sporulation, zoospore release, and motility of zoospores. Seed treatment with GB was found to be more effective than foliar application to reduce the disease incidence (Lavanya and Amruthesh 2017).

5.10  Symbiosis Symbiotic association of higher plants with fungi opens a new avenue to regulate plant tolerance to abiotic stress. Recently, Ghorbani et al. (2018) reported that symbiotic association of fungus Piriformospora indica with tomato plants improved the

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plant growth under salt stress. Symbiotic association activated the prompt accumulation of GB and proline, which proficiently protected the photosynthetic pigment and therefore helps to maintain enhanced photosynthetic efficiency in plants grown under suboptimal edaphic conditions.

6  Conclusions The genes responsible for encoding GB producing enzymes do not occur in all plant species. It could be transferred to such plant systems through the approach of genetic engineering. In field conditions, external supplementation as well as absorption of GB is attained through foliar spray and roots, correspondingly. Numerous studies pointed towards the formation and accumulation of cellular GB that performs important function in plant system resilience in stress environments. Exogenous use or intracellular formation of GB in transgenic plants substantially relieves the stress-­ induced adverse impacts in plant systems. Plant growth regulators, phytohormones, enzymatic/nonenzymatic antioxidants, as well as signaling molecules reinstate the defense responses that subsequently enhance plant production in stressful environments. Stress tolerance approach of plant through GB formation and accumulation can be exploited in soil conservation as well as land management practices. Further, studies on GB including other related defensive substances will be useful towards increase of understanding about plant reactions with tolerance mechanisms under major stress environments such as drought, salinity, temperature extreme, and so on. GB along with other betaines has been found to alleviate lethal impacts of herbicide once supplemented in combination to other adjuvants/additives. Further studies are also required in this field to save the cost as well as labor in retaining the exogenous supplementation of GB or any other osmolyte. Taxonomic listing and wider survey of natural GB forming plant species together with their resilience levels is needed to provide better data for further research workers.

References Ahmad S, Raza I, Ali H, Shahzad AN, Rehman A, Sarwar N (2014) Response of cotton crop to exogenous application of glycinebetaine under sufficient and scarce water conditions. Braz J Bot 37:407–415 Ahmad R, Ali S, Ghani MA (2020) Glycinebetaine alleviates chromium toxicity in Brassica oleracea L. by suppressing oxidative stress and modulating morphology and photosynthetic attributes. Environ Sci Pollut Res 27:1101–1111 Alasvandyari F, Mahdavi B, Hosseini SM (2017) Glycinebetaine affects the antioxidant system and ion accumulation and reduces salinity induced damage in safflower seedlings. Arch Biol Sci 69(1):139–147 Ali S, Chaudhary A, Rizwan M, Anwar HT, Adrees M, Farid M, Irshad MK, Hayat T, Anjum SK (2015) Alleviation of chromium toxicity by glycinebetaine is related to elevated antioxidant enzymes and suppressed chromium uptake and oxidative stress in wheat (Triticum aestivum L.). Environ Sci Pollut Res 22:10669–10678

242

P. Jain et al.

Alia A, Hayashi H, Sakamoto A, Murata N (1998) Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J 16:155–161 Alia K, Sakamoto A, Nonaka H, Hayashi H, Saradhi PP, Chen THH, Murata N (1999) Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol Biol 40:279–288 Annunziata MG, Ciarmiello LF, Woodrow P, Maximova E, Fuggi A, Carillo P (2017) Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Front Plant Sci 7:2035 Annunziata MG, Ciarmiello LF, Woodrow P, Dell’Aversana E, Carillo P (2019) Spatial and temporal profile of glycinebetaine accumulation in plants under abiotic stresses. Front Plant Sci 10:230 Armin M, Miri HR (2014) Effects of glycinebetaine application on quantitative and qualitative yield of cumin under irrigated and rain-fed cultivation. J Essent Oil Bear Plants 17:708–716 Ashraf M (2002) Salt tolerance of cotton: some new advances. Crit Rev Plant Sci 21(1):1–30 Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216 Bakhoum GSH, Sadak MS (2016) Physiological role of glycine betaine on sunflower (Helianthus annuus L.) plants grown under salinity stress. Int J ChemTech Res 9(3):158–171 Banerjee A, Roychoudhury A (2017) Abiotic stress, generation of reactive oxygen species, and their consequences: an overview. In: Singh VP, Singh S, Tripathi D, Mohan Prasad S, Chauhan DK (eds) Revisiting the role of reactive oxygen species (ROS) in plants: ROS boon or bane for plants? Wiley, Hoboken, pp 23–50 Beales N (2004) Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Compr Rev Food Sci 3:1–20 Bharwana SA, Ali S, Farooq MA, Iqbal N, Hameed A, Abbas F, Aqeel S (2014) Glycine betaine-­ induced lead toxicity tolerance related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. Turk J Bot 38:281–292 Bhatti KH, Anwar S, Nawaz K, Hussain K, Siddiqi E, Usmansharif R, Talat A, Khaleed A (2013) Effect of exogenous application of glycinebetaine on wheat (Triticum aestivum L.) under heavy metal stress. Middle-East J Sci Res 14:130–137 Castro-Duque NE, Chavez-Arias CC, Restrepo-Diaz H (2020) Foliar glycine betaine or hydrogen peroxide sprays ameliorate waterlogging stress in Cape Gooseberry. Plants 9:644 Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20 Cheng C, Pei LM, Yin TT, Zhang KW (2018) Seed treatment with glycine betaine enhances tolerance of cotton to chilling stress. J Agric Sci 156:323–332 Cleland D, Krader P, Mccree C, Tang J, Emerson D (2004) Glycine betaine as a cryoprotectant for prokaryotes. J Microbiol Methods 58:31–38 Cromwell BT, Rennie SD (1953) The biosynthesis and metabolism of betaines in plants. Biochem J 55:189–192 Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2(53):1–13 Duman F, Aksoy A, Aydin Z, Temizgul R (2011) Effects of exogenous glycinebetaine and trehalose on cadmium accumulation and biological responses of an aquatic plant (Lemna gibba L.). Water Air Soil Pollut 217:545–556 Einset J, Nielsen E, Connolly EL, Bones AM, Sparstad T, Winge P, Hu JK (2007) Membrane-­ trafficking RabA4c involved in the effect of glycine betaine on recovery from chilling stress in Arabidopsis. Physiol Plant 130:511–518 Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Epstein E et al (1980) Saline culture of crops: a genetic approach. Science 210(4468):399–404

Plant Performance and Defensive Role of Glycine Betaine Under Environmental Stress

243

FAO (2008) FAO land and plant nutrition management service. http://www.fao.org/land-­water/en/. Accessed 8 Aug 2020 Farid M, Shakoor MB, Ehsan S, Ali S, Zubair M, Hanif MA (2013) Morphological, physiological and biochemical responses of different plant species to Cd stress. Int J Chem Biochem Sci 3:53–60 Fariduddin Q, Varshney P, Yusuf M, Ali A, Ahmad A (2013) Dissecting the role of glycinebetaine in plants under abiotic stress. Plant Stress 7(1):8–81 Farooq M, Aziz T, Hussain M, Rehman H, Jabran K, Khan MB (2008) Glycinebetaine improves chilling tolerance in hybrid maize. J Agron Crop Sci 194:152–160 Farooq MA, Ali S, Hameed A, Bharwana SA, Rizwan M, Ishaque W, Farid M, Mahmood K, Iqbal Z (2016) Cadmium stress in cotton seedlings: physiological, photosynthetic and oxidative damages alleviated by glycinebetaine. South Afr J Bot 104:61–68 Gadallah MAA (1999) Effect of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42:249–257 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202 Ghorbani A, Razavi SM, Ghasemi Omran VO, Pirdashti H (2018) Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on growth, gas exchange and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biol 20:729–736 Gupta N, Thind SK (2017) Grain yield response of drought stressed wheat to foliar application of glycine betaine. Indian J Agric Res 51:287–291 Hasanuzzaman M, Hossain MA, Da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateswarlu B, Shanker AK, Shanker C, Maheswari M (eds) Crop stress and its management: perspectives and strategies. Springer, Dordrecht, pp 261–315 Hasanuzzaman M, Mahmud JA, Nahar K, Anee TI, Inafuku M, Oku H, Fujita M (2017) Responses, adaptation, and ROS metabolism in plants exposed to waterlogging stress. In: Khan M, Khan N (eds) Reactive oxygen species and antioxidant systems in plants: role and regulation under abiotic stress. Springer, Singapore, pp 257–281 Hasanuzzaman M, Banerjee A, BorhannuddinBhuyan MHM, Roychoudhury A, AlMahmud J, Fujita M (2019) Targeting glycinebetaine for abiotic stress tolerance in crop plants: physiological mechanism, molecular interaction and signaling. Phyton Int J Exp Bot 88:185–221 Hattori T, Mitsuya S, Fujiwara T, Jagendorf AT, Takabe T (2009) Tissue specificity of glycinebetaine synthesis in barley. Plant Sci 176:112–118 Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272 Husen A (2009) Growth, chlorophyll fluorescence and biochemical markers in clonal ramets of shisham (Dalbergia sissoo Roxb.) at nursery stage. New For 38:117–129 Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A (2013) Growth characteristics, biomass and chlorophyll fluorescence variation of Garhwal Himalaya’s fodder and fuel wood tree species at the nursery stage. Open J For 3:12–16 Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186

244

P. Jain et al.

Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata a. Br.). Agric Food Secur 7:44 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of Niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Hussain M, Malik MA, Farooq M, Ashraf MA, Cheema M (2008) Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J Agron Crop Sci 194:193–199 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Ibrahim W, Qiu CW, Zhang C, Cao F, Zhu S, Wu F (2018) Comparative physiological analysis in the tolerance to salinity and drought individual and combination in two cotton genotypes with contrasting salt tolerance. Physiol Plant 165:155–168 Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597 Ismail A, Takeda S, Nick P (2014) Life and death under salt stress: same players, different timing? J Exp Bot 65:2963–2979 Iqbal MS, Singh AK, Singh SP, Ansari MI (2020a) Nanoparticles and plant interaction with respect to stress response. In: Bhushan I, Singh V, Tripathi D (eds) Nanomaterials and Environmental Biotechnology. Nanotechnology in the Life Sciences. Springer, Cham, pp 1–15 Iqbal MS, Singh AK, Ansari MI (2020b) Effect of drought stress on crop production. In: Rakshit A, Singh H, Singh A, Singh U, Fraceto L (eds) New Frontiers in Stress Management for Durable Agriculture. Springer, Singapore, pp 35–47 Kalinina EB, Keith BK, Kern AJ, Dyer WE (2012) Salt-and osmotic stress-induced choline monooxygenase expression in Kochia scoparia, is ABA independent. Biol Plant 56:699–704 Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyagi AK (2009) Glycinebetaine-­ induced water-stress tolerance in codA-expressing transgenic indica rice is associated with upregulation of several stress responsive genes. Plant Biotechnol J 7:512–526 Kern AJ, Dyer WE (2009) Glycine betaine biosynthesis is induced by salt stress but repressed by auxinic herbicides in Kochia scoparia. J Plant Growth Regul 23:9–19 Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74 Khan TA, Fariduddin Q, Yusuf M (2017) Low-temperature stress: is phytohormones application a remedy? Environ Sci Pollut Res 24(27):21574–21590 Kishitani S, Watanabe K, Yasuda S, Arakawa K, Takabe T (1994) Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ 17:89–95 Korkmaz A, Deger O, Kocacinar F (2014) Alleviation of water stress effects on pepper seedlings by foliar application of glycinebetaine. New Zealand J Crop Hortic Sci 43(1):18–31 Krishnamurthy A, Rathinasabapathi B (2013) Oxidative stress tolerance in plants: novel interplay between auxin and reactive oxygen species signaling. Plant Signal Behav 8:e25761 Kumar M (2013) Crop plants and abiotic stresses. Biomol Res Ther 3:e125 Kumar P, Tokas J, Singal HR (2019) Amelioration of chromium VI toxicity in Sorghum (Sorghum bicolor L.) using glycine betaine. Sci Rep 9:16020 Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V, Hüner NPA (2015) Stress related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res 126:221–235 Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Hurry V, Hüner NP (2017) Interaction of glycine betaine and plant hormones: protection of the photosynthetic apparatus during abiotic stress.

Plant Performance and Defensive Role of Glycine Betaine Under Environmental Stress

245

In: Photosynthesis: structures, mechanisms, and applications. Springer, Berlin/Heidelberg, pp 185–202 Lavanya SN, Amruthesh KN (2017) Glycine betaine mediated disease resistance against Sclerospora graminicola in pearl millet. J Appl Biol Biotechnol 5(3):45–51 Lee CB, Hayashi H, Moon BY (1997) Stabilization by glycinebetaine of photosynthetic oxygen evolution by thylakoid membranes from Synechococcus PCC7002. Mol Cells 7:296–299 Lilius G, Holmberg N, Bülow L (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Biotechnology 14:177–180 Lou Y, Yang Y, Hu L, Liu H, Xu Q (2015) Exogenous glycinebetaine alleviates the detrimental effect of Cd stress on perennial ryegrass. Ecotoxicology 24:1330–1340 Lutts S, Majerus V, Kinet JM (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105:450–458 Ma XL, Wang YJ, Xie SL, Wang C, Wang W (2007) Glycinebetaine application ameliorates negative effects of drought stress in tobacco. Russ J Plant Physiol 54:472–479 Mäkelä P, Peltonen-Sainio P, Jokinen K, Pehu E, Setälä H, Hinkkanen R, Somersalo S (1996) Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Sci 121:221–230 McCue KF, Hanson AD (1990) Drought and salt tolerance; towards understanding and application. Trends Biotechnol 8:358–362 McDonnell E, Wyn Jones RG (1988) Glycinebetaine biosynthesis and accumulation in unstressed and salt stressed wheat. J Exp Bot 39:421–430 McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmo-protectants targets for metabolic engineering of stress resistance. Plant Physiol 120:945–949 Misra V, Mall AK, Al-Khayri JM, Singh AK, Ansari MI (2021) Involvement of Membrane transporters in drought tolerance. In: Roychoudhury A, Tripathi D, Deshmukh R (eds) Transporters and Plant Osmotic Stress. Elsevier (In Press) Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410 Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002) Transgenics of an elite indica rice variety Pusa Basmati 1 harboring the coda gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57 Moussa HR, Jaleel CA (2010) Physiological effects of glycinebetaine on gamma-irradiated Fenugreek plants. Int J Veg Sci 17:60–74 Murata N, Mohanty PS, Hayashi H, Papageorgiou GC (1992) Glycine betaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett 296:187–189 Nayyar H, Bains T, Kumar S (2005a) Low temperature induced floral abortion in chickpea: relationship with abscisic acid and cryoprotectants in reproductive organs. Environ Exp Bot 53:39–47 Nayyar H, Chander K, Kumar S, Bhains T (2005b) Glycinebetaine mitigates cold stress damage in chickpea. Agron Sustain Dev 25:381–388 Park EJ, Jeknic Z, Chen THH (2006) Exogenous application of glycine betaine increases chilling tolerance in tomato plants. Plant Cell Physiol 47:706–714 Park EJ, Jeknic Z, Pino MT, Murata N, Chen THH (2007) Glycinebetaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 30:994–1005 Pathak H, Joshi HC, Chaudhary A, Chaudhary R, Kalra N, Dwiwedi MK (1999) Soil amendment with distillery effluent for wheat and rice cultivation. Water Air Soil Pollut 113:133–140 Porwal P, Sonkar S, Singh AK (2021) Plant stress enzymes nanobiotechnology. In: Al-Khayri JM, Ansari MI, Singh AK (eds) Nanobiotechnology: Mitigation of Abiotic Stress in Plants. Springer (In Press) Prasad KVS, Pardha-Saradhi P (2004) Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. Plant Sci 166:1197–1212

246

P. Jain et al.

Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci 166:141–149 Rabbani G, Choi I (2018) Roles of osmolytes in protein folding and aggregation in cells and their biotechnological applications. Int J Biol Macromol 109:483–491 Rajashekar CB, Zhou H, Marcum KB, Prakash O (1999) Glycine betaine accumulation and induction of cold tolerance in strawberry (Fragaria Xananassa Duch.) plants. Plant Sci 148:175–183 Rani H, Gupta R, Ansari MI, Singh AK (2020) Impact of bioengineered copper quantum dots on germination, photosynthetic pigment and antioxidant response in Chick-pea under Dark stress environment. Res J Biotech 15:120–130 Rasheed R, Wahid A, Ashraf M, Basra SMA (2010) Role of proline and glycinebetaine in improving chilling stress tolerance in sugarcane buds at sprouting. Int J Agric Biol 12:1–8 Rasheed R, Ashraf MA, Hussain I, Haider MZ, Kanwal U, Iqbal M (2014) Exogenous proline and glycinebetaine mitigate cadmium stress in two genetically different spring wheat (Triticum aestivum L.) cultivars. Braz J Bot 37:399–406 Rasheed R, Iqbal M, Ashraf MA, Hussain I, Shafiq F, Yousaf A, Zaheer A (2018) Glycine betaine counteracts the inhibitory effects of waterlogging on growth, photosynthetic pigments, oxidative defence system, nutrient composition, and fruit quality in tomato. J Hortic Sci Biotechnol 93:385–391 Rezaei MA, Jokar I, Ghorbanli M, Livani BK, Masouleh AK (2012) Morpho-physiological improving effects of exogenous glycine betaine on tomato (Lycopersicum esculentum Mill.) cv. PS under drought stress conditions. Plant Omics J 5:79–86 Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulphonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384 Ripoll C, Sceller LL, Verdus MC, Norris V, Tafforeau M, Thellier M (2009) Memorization of abiotic stimuli in plants: a complex role for calcium. In: Baluška F (ed) Plant-environment interactions, signaling and communication in plants. Springer, Heidelberg, pp 267–283 Roychoudhury A, Banerjee A, Lahiri V (2015) Metabolic and molecular-genetic regulation of proline signaling and its cross-talk with major effectors mediates abiotic stress tolerance in plants. Turk J Bot 39:887–910 Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88 Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171 Sakamoto A, Valverde R, Alia, Chen TH, Murata N (2000) Transformation of Arabidopsis with the codAgene for choline oxidase enhances freezing tolerance of plants. Plant J 22:449–453 Shahbaz M, Masood Y, Perveen S, Ashraf M (2011) Is foliar-applied glycinebetaine effective in mitigating the adverse effects of drought stress on wheat (Triticum aestivum L.). J Appl Bot Food Qual 84:192–199 Shan T, Jin P, Zhang Y, Huang Y, Wang X, Zheng Y (2016) Exogenous glycine betaine treatment enhances chilling tolerance of peach fruit during cold storage. Postharvest Biol Technol 114:104–110 Siddiqi KS, Husen A (2017) Plant response to strigolactones: current developments and emerging trends. Appl Soil Ecol 120:247–253 Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Bull Natl Res Cent 43:153 Sonkar S, Pandey B, Rathore SS, Sharm L, Singh AK (2021a) Applications of nanobiotechnology in overcoming temperature stress. In: Al-Khayri JM, Ansari MI, Singh AK (eds) Nanobiotechnology: Mitigation of Abiotic Stress in Plants. Springer (In Press) Sonkar S, Sharma L, Singh RK, Pandey B, Rathore SS; Singh AK; Porwal P; Singh SP (2021b) Plant stress hormones nanobiotechnology. In: Al-Khayri JM, Ansari MI, Singh AK (eds) Nanobiotechnology: Mitigation of Abiotic Stress in Plants. Springer (In Press) Sonkar S, Singh AK, Husen A (2021c) Functions of hydrogen sulfide in plant regulation and response to abiotic stress. In: Husen A (ed) Plant Performance Under Environmental Stress. Springer (In Press)

Plant Performance and Defensive Role of Glycine Betaine Under Environmental Stress

247

Sorwong A, Sakhonwasee S (2015) Foliar application of glycine betaine mitigates the effect of heat stress in three marigold (Tagetes erecta) cultivars. Hortic J 84:161–171 Storey R, Ahmad N, Wyn Jones RG (1977) Taxonomic and ecological aspects of the distribution of glycinebetaine and related compounds in plants. Oecologia 27:319–332 Su J, Wu R (2004) Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci 166:941–948 Sulian LV, Young A, Zhang K, Wang L, Zhang J (2007) Increase of glycinebetaine synthesis improves drought tolerance in cotton. Mol Breed 20:233–248 Sulpice R, Tsukaya H, Nonaka H, Mustardy L, Chen TH, Murata N (2003) Enhanced formation of flowers in salt-stressed Arabidopsis after genetic engineering of the synthesis of glycine betaine. Plant J 36:165–176 Surabhi GK (2018) Update in root proteomics with special reference to abiotic stresses: achievements and challenges. J Proteins Proteomics 9(1):31–55 Surabhi GK, Madhusudhan KV, Sreenivasulu N, Sudhakar C (2000) Stress responses in two genotypes of mulberry (Morus alba L.) under NaCl salinity. Indian J Exp Biol 38:192–195 Surabhi GK, Reddy AM, Sudhakar C (2003) NaCl effects on proline metabolism in two high yielding genotypes of mulberry (Morus alba L.) with contrasting salt tolerance. Plant Sci 165:1245–1251 Tian F, Wang W, Liang C, Wang X, Wang G, Wang W (2017) Overaccumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. Crop J 5(1):73–82 Tsutsumi K, Yamada N, Cha-um S, Tanaka Y, Takabe T (2015) Differential accumulation of glycinebetaine and choline monooxygenase in bladder hairs and lamina leaves of Atriplex gmelini under high salinity. J Plant Physiol 176:101–107 Umezawa T, Fujita M, Fujita Y, Shinozaki KY, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17(2):113–122 Vollenweider P, Gunthardt-Goerg MS (2005) Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. Environ Pollut 137:455–465 Wahid A, Shabbir A (2005) Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Regul 46:133–141 Wang GP, Li F, Zhang J, Zhao MR, Hui Z, Wang W (2010) Over accumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. Photosynthetica 48:30–41 Wang Q, Ding T, Zuo J, Gao L, Fan L (2016) Amelioration of postharvest chilling injury in sweet pepper by glycine betaine. Postharvest Biol Technol 112:114–120 Wani SH, Singh NB, Athokpam H, Mir JI (2013) Compatible solute engineering in plants for abiotic stress tolerance—role of glycine betaine. Curr Genomics 14(3):157–165 Wei D, Zhang W, Wang C, Meng Q, Li G (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci 257:74–83 Xalxo R, Yadu B, Chakraborty P, Chandrakar V, Sahu K (2017) Modulation of nickel toxicity by glycinebetaine and aspirin in Pennisetum typhoideum. Acta Biol Szeged 61(2):163–171 Xu Z, Sun M, Jiang X, Sun H, Dang X, Cong H, Qiao F (2018) Glycinebetaine biosynthesis in response to osmotic stress depends on jasmonate signaling in watermelon suspension cells. Front Plant Sci 9:1469 Yadu B, Chandrakar V, Meena RK, Sahu K (2017) Glycinebetaine reduces oxidative injury and enhances fluoride stress tolerance via improving antioxidant enzymes, proline and genomic template stability in Cajanus cajan L. South Afr J Bot 111:68–75 Yang X, Liang Z, Lu C (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol 138:2299–2309

248

P. Jain et al.

Yang SL, Chen K, Wang SS, Gong M (2015) Osmoregulation as a key factor in drought hardening-­ induced drought tolerance in Jatropha curcas. Biol Plant 59:529–536 Yao T, Shaharuddin A, Chai H, Mahmood M, Shaharuddin N, Chai Ling H, Maziah M, Teh CY (2016) Application of glycine betaine alleviates salt induced damages more efficiently than ascorbic acid in in vitro rice shoots. Aust J Basic Appl Sci 10:58–65 Zhang XY, Liang C, Wang GP, Luo Y, Wang W (2010) The protection of wheat plasma membrane under cold stress by glycine betaine overproduction. Biol Plant 54:83–88 Zhang N, Si NH, Wen G, Du HH, Liu BL, Wang D (2011) Enhanced drought and salinity tolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol Rep 5:71–77 Zhang T, Liang J, Wang M, Li D, Liu Y, Chen THH, Yang X (2019) Genetic engineering of the biosynthesis of glycinebetaine enhances the fruit development and size of tomato. Plant Sci 280:355–366 Zhao Y, Aspinall D, Paleg LG (1992) Protection of membrane integrity in Medicago sativa L. by glycinebetaine against the effect of freezing. J Plant Physiol 140:541–543 Zhou M, Memelink J (2016) Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnol Adv 34:441–449

Plant Performance and Defensive Role of β-Amino Butyric Acid Under Environmental Stress Anuj Choudhary, Antul Kumar, Harmanjot Kaur, A. Balamurugan, Asish Kumar Padhy, and Sahil Mehta

Abbreviations ABA Abscisic acid BABA β-Aminobutyric acid CAT Catalase GR Glutathione reductase HR Hypersensitive reaction JA Jasmonic acid MAPKs Mitogen activated protein kinase NaCl Sodium chloride NO Nitric oxide POX Peroxidase ppm parts per million PR Pathogenesis-related ROS Reactive oxygen species SA Salicylic acid SOD Super oxide dismutase

A. Choudhary · A. Kumar · H. Kaur Department of Botany, Punjab Agricultural University, Ludhiana, India A. Balamurugan Division of Plant Pathology, ICAR-Indian Agricultural Research Institute, New Delhi, India A. K. Padhy National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India S. Mehta (*) International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_10

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1  Introduction Every life of crop plants initiates from seed germination and completes their life cycle by developing the next generation of seeds (Rahman et al. 2019; Viswanath et al. 2020). In due course, seed germination to till the post-harvest stage is the most critical period for its survival and duplicates its desired set of genetic information in the form of DNA (Choudhary et al. 2019; Mehta et al. 2021). Crop plants need to develop their own physiological and biochemical mechanisms to defense and survive against a wide range of environmental conditions (Husen 1997, 2010; Getnet et al. 2015; Embiale et al. 2016; Mehta et al. 2019a; Singh et al. 2019; Anamika et al. 2019; Yadav et al. 2020). The general exposure of the plant to mild chronic stress triggers the specific stress-induced morphogenic responses (Husen et  al. 2014, 2016, 2017; Sharma et  al. 2020;  Choudhary et  al. 2020; Rajput et  al. 2021; Bharti et al. 2021). The adaptation of the plant to one of the stresses brings a kind of acclimation strategy to redirect subsequent tolerance to the other stresses (Prieto et  al. 2020; Sharma et  al. 2020; Choudhary  et  al. 2021; Mehta et  al. 2021; Bharti et al. 2021; Sahil et al. 2021). Such kind of capability in the crop plants built-up stress imprinting tolerance or defense mechanisms through stress-induced genetic and biochemical modifications (Hussein et  al. 2017; Husen et  al. 2018, 2019; Kumar et al. 2021; Sahil et al. 2021). Upon inoculation/application, several biological/synthetic compounds or biological organisms can induce resistance against numerous biological and nonbiological stresses (Conrath et al. 2015; Lal et al. 2018; Mehta et al. 2019b). As a result of extensive uses in numerous publications during the last 20 years, this has been established as one of a technique, called as “priming” (Cohen 2002; Zimmerli et al. 2007; Jisha and Puthur 2016a; Jisha and Puthur 2016b; Rohiwala et al. 2020). The particular inducer confers the protections against the specific spectrum of probable stresses. The chemical inducer called β-aminobutyric acid (BABA) is known to trigger defense mechanisms against fungal, viral, bacterial, oomycetes, nematodes, arthropods attacks, as well as heat, cold, osmotic, and salt stresses (Balmer et al. 2015; Ma et al. 2020). A β-aminobutyric acid is an isomeric form of amino acid with the chemical formula C4H9NO2 (Fig. 1). It induces the elevation of flavonoids, calcium ions, photosynthetic traits, antioxidant compounds, reactive oxygen species, and other qualitative and quantitative characters in plants (Ma et al. 2020; Abid et al. 2020; Ben et al. 2018). BABA effects remain not only in the growth phases of the plant but also in getting rid of the emerging challenge of post-harvest management of vegetable and fruit crops. However, the BABA-like compound that generates long-lasting

Fig. 1  Chemical structure of β-aminobutyric acid (BABA)

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effect from seedling to fruit storage shows its diverse range of effectiveness (Mohamadi et al. 2017; Abid et al. 2020). Moreover, β-aminobutyric acid is used for seed priming, antioxidant systems, photosynthetic traits, biotic and abiotic stress tolerance, prevention of post-harvest loss without affecting yield, and triggering hormones, as reported by many workers (Xu et al. 2018; Mahmud et al. 2020).

2  BABA: Origin and Biosynthesis The nonprotein amino acid BABA is playing a pivotal role in plant defenses and has been known for more than 50  years back. The ten amino acid compounds were screened in 1963 against the root rot disease of pea plant (caused by Aphanomyces euteiches), where BABA and methyl-β-aspartic acid efficiently reduce the severity of root rot in pea (Papavizas and Davey 1963; Jakab et al. 2001). From literature, it has been established that the first to discover the BABA activity against plant-­ pathogen systems, i.e., root rot disease in pea (Papavizas and Davey 1963). The application of β-aminobutyric acid and γ-aminobutyric acid (GABA) was studied on tobacco plants against the downy mildew disease caused by (Peronospore tabacina) where BABA was proving itself the excellent antifungal nature against tobacco downy mildew and tomato late blight, (Phytophthora infestans) (Cohen 1994). The first observation for BABA-induced systemic and local resistance against the root-knot nematode incited by Meloidogyne incognita was reported by Oka et al. (1999) tomato. The first report of BABA-induced resistance against the insect was reported by Hodge et al. (2005) against pea aphid Acyrthosiphon pisum. Up to the year 2016, there were 147 research studies that have been published, including 5 review articles and 3 patentable works describing the BABA-induced resistance in crop plants (Cohen 2001; Cohen et al. 2004; Luna et al. 2014; Baccelli and Mauch-Mani 2016; Li et al. 2020).

3  Distribution and Transport Mechanism in Plants The natural occurrence of BABA has been mentioned in several reports. For instance, it was observed in the Spanish wines (Barrado et al. 2009) and the root exudates of tomato plants conditioned under solarized soils (Gamliel and Katan 1992). In the tree species such as Acacia dealbata, Acacia melanoxylon, and Eucalyptus regnans, the BABA was observed in the xylem and phloem associated exudates (Pfautsch et al. 2009). Recently, the natural occurrence of BABA has been reported in the moss Physcomitrella patens, Arabidopsis thaliana, maize (Zea mays), teosinte (Zea mays sp. Mexicana), Chinese cabbage (Brassica rapa), and wheat (Triticum aestivum). The detection has been made with the help of liquid chromatography-tandem mass spectrometry analysis technique to detect and quantify the BABA in the plant tissues

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(Thevenet et  al. 2017). Interestingly, the endogenous concentration of BABA rises under the abiotic stresses (such as submergence and salt stress) and necrotrophic, biotrophic, and hemibiotrophic pathogens attacks. The BABA is the water-­soluble compound absorbed by the plants and distributed systemically throughout the plant physiological systems (Slaughter et  al. 2012; Vijayakumari and Puthur 2016). The exact clear-cut transport mechanisms of BABA are still not clearly defined; however, once it has been sprayed over the plant it moves to all the plant parts and induces broad-spectrum resistance in the diverse group of plant diseases (Cohen and Gisi 1994; Jakab et al. 2001). The translocation of BABA is not unidirectional was reported by Jakab et al. (2001) on the Arabidopsis plant. It has been investigated that when a certain amount of radiolabeled BABA is applied in the leaves, then its presence is noted down in the young leaves, shoot tips, and also on the roots of treated plants (Li et al. 2020). It has been believed that BABA and l-glutamine share a common type of transporter because the transport of l-­glutamine competes with the BABA (Wu et al. 2010). The roots are not completely able to absorb BABA because of competition for the same transporter with amino acids and inefficiency of transporters specific to BABA (Cohen and Gisi 1994; Jakab et al. 2005).

4  Mechanism of Action BABA triggers a diverse range of defense mechanisms in crop plants by activating both physical and biochemical reactions against invading phytopathogens. The induced physical barriers resist the stress condition by means of lignin deposition in cell walls and callose deposition. The biochemical barriers indulge the hypersensitive responses (HRs), reactive oxygen species production, secondary metabolites biosynthesis such as anthocyanin, phenols, and phytoalexins, and pathogenesis-­ related proteins (Ali et al. 2018). The pinpoint necrotic spots are induced physical barriers under the BABA’s foliar sprays which were considered to be associated with the systemic acquired resistance. However, the necrotic spots are the hypersensitive reactions that occur in plants which indicates the type of localized arresting of the pathogen infection (Siegrist et al. 2000). The hypersensitive reactions sometimes are not restricted to the single-cell type; however, it has been passed to other surrounding cells or other cells can be responded separately to the effector protein to independently initiate HRs. It triggered under the heavy inoculation so that many cells can interact independently with the pathogen cells, or the trailing necrosis (where necrosis in the surrounding cells of developing infectious bodies) does not prevent the pathogen growth by hypersensitivity, thus allocating the pathogen to move via inter-cellular way and triggered HR in each infected single cell (Balint-Kurti 2019). The pathogen infection can be further reduced by depositing callose, observed in the Arabidopsis when it is inoculated with Peronospora parasitica after the foliar application of BABA. The callose is deposited around the neck region of haustoria and thus prevents the nutrient acquisition by the fungal pathogens (Jakab et al. 2001). It has been

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observed that lignin was build up in the grapes after the Plasmopara viticola inoculation whereas no lignin or callose deposition in tobacco after Peronospora tabacina inoculation (Cohen 1994). The pathosystem specificity is extended to the accumulation of pathogenesis-related proteins (PR). BABA activates the PR proteins accumulation to play role in the antimicrobial activity validated from several studies. Siegrist et al. (2000) studied that in the Arabidopsis and tobacco, the PR proteins were induced by the foliar application of BABA. Once the PR proteins are activated, there will be enhanced reactive oxygen species production, phytoalexins production, and cell wall phenolic secretion, and the defense genes activation occurs by means of induced defense mechanisms. The proteome analysis shows that cell wall enzymes and lignin biosynthesis suppression occurred under BABA treatments (Macarisin et al. 2009). Mitogen-associated protein kinases (MAPKs) are the active biochemical components that translate the extracellular information into the appropriate responses. The impact of BABA on MAPKs has been studied in the grape cells (Dubreuil-Maurizi et al. 2010). However, it has been observed that BABA did not directly induce phosphorylation, did not alter the MAPK global amount, and also did not affect the dynamic of phosphorylation (Dubreuil-Maurizi et al. 2010). BABA also altered the amino acid balance reported in the Arabidopsis. The accumulation of BABA induces stress-responsive amino acids are proline and asparagines on the other l-glutamine is inhibited (Singh et al. 2010). BABA triggered the phytoalexin accumulation in the plants whether directly or indirectly is not still clear. BABA induces capsidiol accumulation (pepper), Furano-coumarins (parsley plant), and stilbene (grapes) (Hong et al. 2001; Cohen 2002; Slaughter et al. 2008). BABA has different kinds of action based on the involvement of hormones such as jasmonic acid, salicylic acid, abscisic acid (ABA), and ethylene (Table 1). BABA induces the accumulation of abscisic acid for adjusting osmotic changes under the water stress conditions by targeting the osmosolutes. For instance, the BABA-­ treated plants show a faster response in stomatal closure in the early hours of drought through abscisic acid signaling (Rajeb et al. 2018). Such kind of response is very efficient in cost-effectiveness because the early closure allows withstanding against the forthcoming stress without the biosynthesis of osmotically active substances. Therefore, abscisic acid biosynthesis proves to be defense-related hormones against the tolerance of salt and drought conditions (Fujita et al. 2011; Sripinyowanich et al. 2013). Salicylic acid (SA) dependent pathways induce the expression of PR1 proteins potentiated in the BABA-treated plants. The SA-triggered defense responses involve trailing necrosis and enhanced callose deposition (Ton et  al. 2005). The jasmonic acid (JA) pathways potentiate the PR-4 and LOX-9 gene expression in the grapevine against the Plasmapara viticola (Hamiduzzaman et al. 2005). The BABA primed seeds are observed to be maintaining the ethylene receptor ETR1 (ethylene signaling negative regulator) on the membrane for a longer period. The inhibition of ethylene-induced signaling for gene expression maintained a longer life and increased tuber yield production (Sós-Hegedűs et al. 2014). Nitric oxide (NO) and reactive oxygen species (ROS) are the key players in the mode of action by integrating themselves in the complex signaling network. These molecules are integrated with the hormonal signaling pathways (Wilson et al. 2008).

PR-1, LOX-9 and PR-4 AtSAC1b and IBS2

IBI1

COI1

JA pathway

Phosphatidylinositol pathway

SA pathway

Octadecanoic pathway Phenylpropanoid biosynthesis

MAK1

RAB18 and RD29A

ABA pathway

Pathways ET pathway

Downstream components (genes) PR-1

s-111 and s-765 ibi1-1

PIIF MDCA

Cicer arietinum L.

eIF2α

pS6K1

Tomato

Hyalopernospora arabidopsidis

Hordeum vulgare L., Vigna unguiculata L.

LOX

1-BuOH

Arabidopsis

Schmitt et al. (2018) Yadav et al. (2020)

Schwarzenbacher et al. (2014)

Kammerer et al. (2006) Ton et al. (2005)

Wang et al. (2002)

Inhibitors References Le-ACS6 Wang et al. (2002)

Plant transgenic species employed Tomato

jar1, etr1 Lettuce, cauliflower

ibs

Mutants ran1

Arabidopsis Aspartyl-tRNA synthetase, induced systemic resistance (ISR) after root colonization by Pseudomonas fluorescens Arabidopsis Upstream wound signals and opr3-1 activate anti-herbivore defense Arabidopsis Reduced fungus virulence ref5, ref2

Plant species Biological function Arabidopsis Regulate Le-ACS2 and Le-ACS4 during fruit ripening Arabidopsis Genes encode hydrophilic proteins and make plant stress tolerant Vitis vinifera Impart resistance to downy L. mildew resistance Oryza sativa Reduce pathogen-induced L. callose deposition

Table 1  Signaling pathways potentiated by application of BABA

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The synthesis of ROS and NO-induced under the spraying of potato plants with the BABA (Floryszak-Wieczorek et al. 2012; Bengtsson et al. 2014). It is reported in the grape plants that primed seeds have higher H2O2 production whereas BABA did not induce directly ROS and NO production (Dubreuil-Maurizi et al. 2010).

5  F  unctional and Defensive Role of BABA in Crops Under Stress Conditions The immobile fixation of the plants by its vital part enforced them to build up the potential mechanism or divert its pathways in the course of the evolutionary timeline to remain to stand up in any kind of exposure and complete its life cycle by producing viable seeds (Li et al. 2020). The exposure may be abiotic stresses such as heat, water scarcity, cold, and oxidative burst, and also it can be biotic stresses such as viral, bacterial, fungal, insect, and nematodes (Fig. 2). The changing climatic condition due to

Fig. 2  Schematic representation elucidating the BABA mechanism of action

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anthropogenic activities may lead to enhanced CO2 emissions which exaggerates the deterioration of cultivated lands due to the rise in temperature (Peters et al. 2011). It results in the intensification of drought periods, evapotranspiration, and soil salinization (Munns and Tester 2008). Numerous studies are available showing that the enhanced and more pronounced pathogen reproductive potential and the geographic expansion leads to rise in the more virulent strains with the climate change (Garrett et al. 2006). Therefore, in the future, the biotic and abiotic stresses are likely to be intense along with their complicated interactions. BABA is now a widely accepted environmentally safer agent (Li et al. 2019). Plants have gained the broad-spectrum ability for disease resistance once the stress indicating signals have been perceived. To avoid the constitutive defense expression cost, the plant can evolve defense priming to fast and stronger expression in the future (Li et al. 2020). The priming can be elicited by internal and external stress stimuli and endogenously by immune signals. BABA is one of the potential metabolites that got much attraction from researchers in recent years. The resistance properties of BABA have been known for a long-time back; however, it was recently only discovered to accumulate within the plant under a stressed condition. All these indicating to acts as promising endogenous stress metabolites (Thevenet et al. 2017; Baccelli and Mauch-Mani 2017).

5.1  Abiotic Stress Tolerance The abiotic stresses have gained prime importance with the day-to-day scenario because the different environmental factors cannot be prevented such as drought, heat, salinity, heavy metal, cold, and air pollution (Anamika et al. 2019; Dhakate et al. 2019). The correct predictions regarding crop manufacturing under the impacts of abiotic stresses are difficult  (Mehta et  al. 2021; Sharma et  al. 2021). Abiotic stresses are complicatedly interrelated and target the plant water status from the deep cellular level to complete the entire plant (Hirayama and Shinozaki 2010). These are inducing the series of molecular, biochemical, physiological, and morphological changes that adversely affect the development and growth of plants (Yadav et al. 2021). Plant responses to abiotic stresses are dynamic as well as complicated with their reversible and irreversible action (Cramer et al. 2011; VenegasMolina et al. 2020; Li et al. 2020). Several reports are showing the positive role of BABA in enhancing the tolerance potential against the major abiotic stresses such as heat (Zimmerli et  al. 2007), osmotic stress (Jisha and Puthur 2016a, b), drought, and salinity (Jakab et al. 2005; Macarisin et al. 2009). The adaptive responses have been enhanced by treating with BABA against the heat stress. For instance, Zimmerli et al. (2007) experimented to study the impact of BABA on Arabidopsis plants under heat stress. They used three isomeric forms of BABA (a, b, and c), out of which b form causes the higher thermotolerance. The author suggested that the application of BABA enhances the adaptive responses only not the basal level tolerance to stress.

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The water status was maintained under the osmotic stress condition observed in apple (Tworkoski et al. 2011), Arabidopsis (Jakab et al. 2005), wheat (Du et al. 2012), and flax (Quéro et  al. 2015) after the pretreatment of BABA.  The seedling of Arabidopsis shows the delayed initiation of wilting under both drought and salinity stresses conditions (Jakab et al. 2005). The soil drenching with BABA increases the potential of Malus pumila seedlings to withstand the drought-stressed condition by enhancing the expression of defense signaling pathways (Macarisin et al. 2009). The apple treated with BABA has decreased rate of transpiration in the early morning under exposure to dehydration. It results in the delaying of stress-induced shoot tips wilting (Tworkoski et  al. 2011). The BABA priming induces the accumulation of ABA in wheat leaves under the drought condition and leads to a decline in the water utility by closing the stomata at inappropriate timing. These plants also have less ROS production; lipid peroxidation tightly links with high antioxidant activity due to CAT, SOD, and GR (Du et al. 2012). The 5 mM BABA treatment to the tobacco seedling enhances the tolerance activity to low potassium condition and also promotes growth (Jiang et al. 2012). The chlorophyll content, primary root length, peroxidase activity, potassium uptake, and proline accumulation were improved in the BABA-treated plant. The water status improvement is based on the faster acquisition of an osmotically stabilized state in most of the plants proven under BABA application studies. The seedling of BABA-treated Brassica napus has higher calcium, flavonoid, anthocyanin, and ascorbate concentration in the drought condition (Rajaei and Mohamadi 2013). In the potato plant, metabolic negative alterations are less in the tubes of BABA-drenched plants (Sós-Hegedűs et  al. 2014). In the flax plant, leaves having higher RWC, higher proline and non-structural carbohydrates, inorganic solutes and reduced osmotic potential maintained in the BABA treated plants in comparison to non-treated plants (Quéro et al. 2015). Under the NaCl and PEG stressed conditions, the photosystem activity and photosynthetic pigment content were found to be higher in the BABA-treated plants of Vigna radiata (Jisha and Puthur 2016a). The peach fruits and tomato plant show the memory response to early treatment with BABA against the cold stress. These plants were having a higher expression of antioxidant genes to prevent oxidative damage and the regulation of ROS signaling (Malekzadeh et  al. 2012;  Baier et  al. 2019; Vijayakumari and Puthur 2016). The combined application of 0.2  mM of BABA with 10  mM of Ca2+ furthermore improves the antioxidant content and activity, reduced cell membrane injury, and less ROS production under the cold stress condition (Ma et al. 2020). Further, the application of BABA was reported for abiotic stress tolerance in many crop plants and summarized in Table 2.

5.2  Biotic Stress Resistance The BABA-induced resistance can be able to counterattack the fungal pathogens as revealed in numerous studies (Table 3). The application of 0.25 mg of BABA on the tomato plant through petiole induced the HR when challenge inoculated with

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Table 2  Recent studies (during 2003–2020) highlighting BABA importance in abiotic stress tolerance Stress type Plant species Drought Malus stress niedzwetzkyana Dieck ex Koehne Heat stress

Arabidopsis thaliana L. Heynh.

Heavy metal

Glycine max L. Merr.

Freezing Triticum aestivum L.

Heavy metal stress

Nicotiana tabaccum L.

Heat stress

Oryza sativa L.

Mode of BABA Effect of BABA Effect of stress application application Soil drench Provide resistance by Effect the ABA-independent photosynthetic pathways and rate and plant increase cell wall growth stiffness Soil drench BABA induces Reduce plant accumulation of growth and anthocyanin and HSP pigment production formation Foliar Protect the cells from Reduction in spray Cd-induced oxidative growth due to stress, enhanced the oxidative stress defense-related protein peroxiredoxin and glycolytic enzymes during cadmium exposure Promote root and Reduce seedling Seedling treatment shoot development of growth and seedlings, enhance cause oxidative activities of damage to plant antioxidant enzymes and decreased MDA content Enhance the defense Deteriorate the Spray plant growth by application mechanism by upregulating oxidative stress antioxidant enzymes activities Seed Prevent membrane Drastically treatment damage, increase affect chlorophyll content chlorophyll and photochemical content and net efficiency, enhance photosynthetic activities of rate enzymatic antioxidants like superoxide dismutase, catalase, and ascorbate peroxidase

References Macarisin et al. (2009)

Wu et al. (2010)

Hossain et al. (2012)

Malekzadeh et al. (2012)

Jiang et al. (2012)

Nayyar et al. (2014)

(continued)

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Table 2 (continued) Mode of BABA Effect of BABA Effect of stress application application Soil drench Delayed the Enhance the expression of oxidative drought-inducible damage in gene StDS2, provide plants resistance against microbial attack Drought Linum Decrease the Soil drench Increased stress usitatissimum L. crop production accumulation proline, non-­ structural carbohydrates and reduce the inorganic solutes Seed Enhance the Salinity Vigna radiate L. Reduction in treatment accumulation of stress net protein, photosynthetic carbohydrates, rate and yield antioxidant enzyme activities Enhancement of the Salt Oryza sativa L. Reduced shoot Seed treatment seedling growth stress length, fresh parameters, increase weight and dry of 38–52% in the weight carotenoid content of seedlings, increases in the activity of nitrate reductase (NR) and maximum increase of superoxide dismutase (SOD) activity Enhancement of the Drought Oryza sativa L. Reduced shoot Seed treatment seedling growth stress length, fresh parameters, increase weight and dry of chlorophyll a and weight b content and increase in the shoot length, fresh and dry weight Seedling Decrease the cell Drought Vicia faba L. Decrease the treatment membrane damage stress plant growth and increase the leaf and yield photosynthetic rate

Stress type Plant species Drought Solanum stress tuberosum L.

References Sós-­ Hegedűs et al. (2014)

Quéro et al. (2015)

Jisha and Puthur 2016b)

Jisha and Puthur 2016a

Jisha and Puthur 2016b

Abid et al. (2020)

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Table 3  Recent studies (during 2003–2021) highlighting BABA importance in biotic stress tolerance

Penicillium digitatum

Vitis vinifera L.

Mode of BABA Effect of stress application Affect rhizome Seed soaking development, enzyme activities of polyphenol oxidase lipoxygenase and PAL Reduction in Soil fruit yield drench

Aphid attack

Pisum sativum L., Vicia faba L., Phaseolus coccineus L. and Medicago sativa L.

Root Reductions in the growth rate drench and yield of pea, broad bean, runner bean and alfalfa

Pseudomonas fluorescens

Brassica oleracea var. italica

Reduction in plant growth and yield

Foliar spray

Meloidogyne javanica

Ananas comosus L. Merr.

Reduction in growth and pineapple yields

Foliar spray

Resistance against Plant species Phythium Vitis vinifera aphanidermatum L.

Effect of BABA application Production of PR proteins, increase resistance in plant and elevates enzyme activities Promote pathogen resistance, inhibit spore germination and germ tube elongation of P. digitatum and enhance PAL activity Increased aphid mortality by decreasing the growth rate of individual insects, no direct toxic effects of BABA against A. pisum and lack phytotoxic effects on aphid performance Inducing systemic resistance and effectively controlled downy mildew Improved shoot root weight and increase crop yield

References Karmakar et al. (2003)

Porat et al. (2003)

Hodge et al. (2005)

Pajot and Silue (2005)

Chinnasri et al. (2006)

(continued)

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Table 3 (continued) Resistance against Fusarium graminearum

Plant species Triticum aestivum L.

Effect of stress Drastically affect plant growth

Botrytis allii

Allium cepa L. Effect plant growth and photosynthesis

Bremia lactucae

Lactuca sativa Effect L. cotyledons of young seedlings, damage leaves Triticum Aphid feeding aestivum L. directly affects growth and indirectly affects carbon dioxide assimilation in leaf

Sitobion avenae attack

Botrytis cinerea

Solanum lycopersicum. L.

Deteriorate the fruit quality and plant growth

Effect of BABA application Induce resistance against Fusarium and enhance plant growth Bulb Promote treatment defensive callose deposition Wound site Induces local and systemic resistance against downy mildew Seedling BABA treatment significantly reduced the weights of S. avenae, suppression of S. avenae growth and aminobutyric acid concentration in phloem sap of BABA-­ treated plants was higher Foliar BABA-induced spray resistance through basal defense responses like lignin formation, callose deposition and accumulation of reactive oxygen species Mode of BABA application Foliar spray

References Zhang et al. (2007)

Polyakovskii et al. (2008)

Cohen et al. (2011)

Cao et al. (2014)

Li et al. (2020)

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P. infestans. The foliar application is more effective than the soil drenching against the late blight in the tomato plants as reported by Cohen (2002) and Eschen-Lippold et al. (2010). The sporulation of Plasmopara viticola was observed to be completely inhibited in the grape plant (Cohen et al. 1999; Cohen 2002). The BABA application will allow the massive lignin accumulation, and similarly it also protects the grapevine from the downy mildew disease by inducing the callose deposition through JA signaling pathways and also reports the accumulation of stilbene phytoalexins synthesis (Slaughter et al. 2008; Venegas-Molina et al. 2020; Li et al. 2020). The BABA application on day before the inoculation of Pseudoperonospora cubensis on the cucumber plant triggered the small-sized chlorotic lesions formations. The suppression of Sporangiophore emergence and sporangial production are directly linking in a dose-dependent manner (Ovadia et al. 2000). The resistance can be achieved through callose deposition around the haustoria. Similarly, the resistance is achieved by lignin accumulation against the downy mildew. The BABA-­ treated lettuce plant shows resistance against the biotrophic Bremialactucae fungal pathogen by restricting the primary and secondary vesicle. The penetration is prevented by heavy deposition of callose; however, there is no effect on germination of spores, the formation of appressoria, and the epidermal penetration of the fungus (Pajot et  al. 2001;  Cohen et  al. 2010). The H2O2 production was observed to be higher due to the higher activity of peroxisomal glycolate oxidase (Vaknin 2016). The pea rust disease caused by Uromyces pisi is overcome by the enhanced production of phytoalexins (Barilli et al. 2015). In the artichoke plants, the soil drenching or foliar spray is effective against the necrotrophic Sclerotinia sclerotiorum fungal induced by BABA (Marcucci et al. 2010). Similarly, in the pot condition, the BABA-­ treated lettuce plant remains protected even after the inoculation of Sclerotium sclerotiorum (Vaknin 2016). BABA is recommended as a commercial fungicide against the apple diseases (Gur et al. 2013). For instance, in the field condition, the apple is protected with the application of BABA against the moldy core decay and the blotch disease due to Alternaria alternata (Reuveni et al. 2003; Gur et al. 2013). Similarly, several reports are showing the antifungal activity against the Botrytis cinerea with the application of BABA (Zimmerli et  al. 2001; Luna et  al. 2016) (Fig.  3). The application of >1000 ppm BABA directly inhibits the Botrytis cinerea observed in the fruits of strawberry. Such fruit has higher fructose, sucrose, and glucose content with a high sensory score and sweetness index (Wang et al. 2016). Additionally, in lab conditions, BABA offers antifungal properties against B. cinerea pathogenic fungus (Fischer et  al. 2009). The direct controls of fungal pathogens by BABA are Penicillium digitatum, P. italicum, P. expansum, Botrytis cinerea, Leptosphaeria maculans, and Sclerotinia sclerotiorum, by interfering with the spore germination and mycelia growth (Tavallali et al. 2008; Fischer et al. 2009; Marcucci et al. 2010; Zhang et al. 2011; Venegas-Molina et al. 2020; Li et al. 2020). The soil drenching and the foliar sprays both are effective against the root-knot nematodes Meloidogyne javanicum and Meloidogyne marylandi in tomato and cucumber and the wheat plants, respectively (Oka and Cohen 2001). The nematode-­ inoculated plant was showing the translocation of 14C-BABA from the leaves to the

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Fig. 3  Functional and defensive role of BABA in imparting stress tolerance against various biological and nonbiological stresses

nematodes-induced galls (Oka et al. 1999). Moreover, the soil drenching of BABA was effective against M. incognita in tomato plants (Anter et al. 2014). Similar in the potato plant, BABA efficacy was higher in the disease complex due to Pectobacterium carotovorum subsp. Brasiliense and Meloidogyne incognita (Mongae and Moleleki 2015). The activation of an antioxidant system such as SOD and POX by BABA was considered to be activated in reducing the level of ROS concentration in tomato against M. javanica (Sahebani and Hadavi 2009). Furthermore, as per the literature, the rice is one of the pre-eminent cereals whose productivity get hampered by both biological and non-biological constraints (Mehta et al. 2020; Dilawari et al. 2021). Considerind the economic importance of rice, the BABA application have been also applied in rice. For example, the BABA application in rice inhibits the penetration or delays the nematode and giant cell development; however, no direct interference against the root-knot nematode (M. graminicola) was observed (Ji et al. 2015). The soil drenching of six legume plants with BABA reduces the activity of the Acyrthosiphon pisum aphid (Oka and Cohen 2001). Similarly, on the plants of the Brassicaceae family, BABA reduces the growth of phloem feeders such as Brevicoryne brassicae and Myzuspersicae, also the chewing-type insects such as Plutella xylostella and Tricho plusiani (Hodge et al. 2006). The apples can be protected from BABA application from the rosy apple aphid Dysahis plantaginea (Robert et al. 2016; Philippe et al. 2016). BABA shows high effectiveness in controlling tomato diseases and nematodes. The study is using the 25 mM application BABA as soil drenching (Prieto et al. 2020). It has been observed to induce resistance against insects (phytophagous type). BABA triggered resistance against several bacterial strains including Pseudomonas syringae and Ralstonia solanacearum in Arabidopsis and tomato,

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respectively (Zimmerli et al. 2000; Hassan and Abo-Elyousr 2013). Interestingly, BABA was shown to induce resistance in citrus against the most destructive yellow dragon disease caused by Citrus huanglongbing (Li et al. 2016). The information regarding the viral resistance mediated by BABA is scarce. However, only a few reports are there showing the resistance against the GLRaV1 in grapevine and the tobacco mosaic virus in tobacco (Csikász-Krizsics et al. 2013).

5.3  Potential Role as “Priming Agent” The priming involves the stimulation of plants in the deficiency of a challenge (Lal et al. 2018). It is considered an intrinsic component of induced resistance. The treatment of BABA to plants triggers the quicker and vigorous defensive responses in exposure to abiotic and biotic stresses. The BABA application enhances the salicylic acid, glycosides, indole-3-acetic acid, and primary metabolites of the tri-­ carboxylic acid cycle (Pastor et al. 2014). The rise in metabolite pool induces the specialized pathways of defense signaling in the post-challenged primed period after the exposure to stress. The 50 mM BABA application to the pearl millet seeds was studied against the downy mildew by Sclerospora graminicola (Shailasree et  al. 2001). It has been observed that 75% of the emerged seedling protected, 90% of the plants remain protected in comparison to control, long-lasting effectiveness from the vegetative and reproductive periods of growths. Shailasree et al. (2007) suggested the BABA induced accumulation of the peroxidases, phenylalanine ammonia-lyase, cell wall hydroxyproline-rich glycoproteins, and β-1,3-glucanases. Sixty-three differentially accumulated proteins related to the energy and metabolism were observed in the BABA primed and S. graminicola inoculated pearl millet plants elucidated by the proteomic approach (Anup et al. 2015). In the Vigna radiata, the BABA seed priming improves the tolerance potential against the salinity and drought stresses (Jisha and Puthur 2016a, b). The BABA primed seed increases the photosynthetic and mitochondrial activities, photosynthetic pigments, reduced malondialdehyde contents in seedlings, proline accumulation, total carbohydrate, total protein, antioxidant enzyme activity, and nitrate reductase activity (Fig.  4). The 8-week BABA primed seeds induce diverse defensive responses against the powdery mildew (causal agent is Oidium neo lycopersici) (Worrall et al. 2012). The 1-week primed tomato seeds triggered resistance against the Botrytis cinereal without affecting the plant growth and arbuscular mycorrhizal fungal colonization (Luna et al. 2016). The pre-socking of barley seed for 24  h with BABA permits the seeds to germinate under the 7 days of salinity condition (Mostek et al. 2016). There is the induction of the catalases, superoxide dismutase and peroxidase (antioxidant enzymes), chitinase and endo-1,3-β-glucosidase (PR proteins), and HSC 70 and cyclophilin (chaperons). In the primed seed of Arabidopsis, the major metabolic shift associated with the BABA-triggered resistance involves pipecolic acid accumulation (critical primed endogenous signal) (Conrath et al. 2015).

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Fig. 4  Molecular dissection of BABA-induced priming changes in plants

BABA postponed the senescence in the sweet cherry fruits by reducing membrane permeability, malondialdehyde content, decreasing activities of pectin methylesterase and polygalacturonase, integrated subepidermal cell structure, and an elevated content of cell wall polysaccharides (Wang et al. 2015). Similarly, the BABA-treated strawberry fruits having higher activities of sucrose synthase, sucrose-6-phosphate phosphatase, and sucrose phosphate synthase leads to the increased fruit sweetness (Wang et al. 2016). The BABA-treated citrus fruit tree has a significant reduction in the iron, phosphorus, magnesium, sulfur, sodium, and zinc and the iron chelates with BABA elucidated in an in vivo study (Tiwari et al. 2013; Koen et al. 2014). It has been considered that the deficiency of Fe response induced by BABA triggered the plant defense in the ready state to actively participate in the plant pathogen resistance. Thus, the activation of detoxification mechanisms and the defense responses strengthen the survival value of plants under stressful environmental conditions.

5.4  Recent Advancement of BABA in Crop Improvement Recently, the functional role of β-aminobutyric acid is not limited to seed priming but shows a wide range in crop improvement via biotic and abiotic stress tolerance, antioxidant systems, photosynthetic traits, preventing post-harvest loss without

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affecting yield, and triggering hormones, as reported by many workers (Xu et al. 2018; Mahmud et al. 2020) (Fig. 4). β-Aminobutyric acid exhibits salinity stress tolerance in Brassica napus by regulating Methylglyoxal Detoxification and ROS (Mahmud et al. 2020). Biosynthesis of certain sphingolipids is upregulated by the application that helps in resistance against necrotrophic like pathogenesis, stimulate signaling molecules responsible for basal defense reported in Brassica cinerea. The exogenous application of β-aminobutyric acid enhances drought tolerance in Vicia faba (Faba bean) (Roylawar and Kamble 2017; Chea et al. 2019; Ma et al. 2020; Abid et al. 2020; Ben et al. 2018). β-Aminobutyric acid provides a new alternative and efficient chemical plant disease management strategies used in horticulture crops. The various stages of fruit development the challenges of quality loss especially in post-harvest periods when no plant defense is activated. Exogenous application of BABA in seedling stages significantly decreases the post-harvest loss in the form of infection. The post-harvest resistance from Botrytis cinerea due to BABA is reported in tomato and shows no impact after harvesting. The fungal resistance in susceptible crops like a tomato without affecting their yield traits. However, traces of BABA residues accumulated in the post-harvest stages of tomatoes partially confirmed the resistance to B. cinerea without declining the fruit qualities (Roylawar and Kamble 2017; Chea et al. 2019; Ma et al. 2020). Molecular studies revealed the dual role of BABA molecule in salinity stress against NaHCO3 as well as in the improvement of plant efficiency in Rhododendron. The BABA affects carbon assimilation through photosynthetic traits and prevents plants from oxidative damage. The BABA application to tobacco at seedlings also provides long-term resistance against cadmium stress (Liu et  al. 2016). BABA maintains the cellular homeostasis and redox potential in tomatoes that confirms its resistance against Alternaria disease (Alternaria alternata). Foliar application of BABA in early growth stages provides promising result in highbush blueberry or blue crop. It helps in adult resistance and decreases the risk of fruit deterioration at post-harvesting as well as during storage in a refrigerated fridge (Chea et al. 2019). Exogenous application of BABA compound under drought or salinity stress that enhances abscisic acid accumulation and responsiveness elevates tolerance level. Microbe-associated Molecular Pattern (MAMP) or Pathogen-Associated Molecular Patterns (PAMP) or Damage-Associated Molecular Pattern (DAMP) shows enhanced ABA concentration and increased callose responses the provide the basal resistance in the plant-pathogen interaction systems. In rapeseed, seed priming with BABA induces the accumulation of antioxidants molecules and maintains ion homeostasis and other reactive oxygen species concentration in roots and leaves under drought stress (Mohamadi et  al. 2017; Abid et  al. 2020). Similarly, In Arabidopsis, the BABA treatment activating ethylene and ABA signaling simultaneously under stress conditions causes the accumulation of various stress tolerance transcripts to help in the activation of defense pathways. The BABA priming shows a defense response against infection of Colletotrichum gloesporioides fungi in mango confirmed through quantitative proteomics (Ben et al. 2018). BABA-induced resistance via seed priming and foliar application causes upregulation of antifungal compounds and defense-associated proteins such as phenolics, pathogenesis-related

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proteins, flavonoids of defense signaling factors mediated by calcium, salicylic acid, HDAC, MLP28, and other posttranscriptional-mediated defense response (Balint-Kurti 2019; Ma et  al. 2020). Moreover, BABA induced resistance during vegetative, reproductive, and post-harvesting stages without the metabolism of primary as well as secondary metabolites biosynthesis and contributes well effectively in crop improvement (Xu et al. 2018; Mahmud et al. 2020).

6  Conclusion The continuous pressure of crop losses under the climate change scenario threatens agriculture activities at the global level with no clue. The unpredictable and unavoidable factors like heat, cold, drought, salinity, fungal, viral, and bacterial also cause severe crop yield losses worldwide. The natural hormones, synthetic regulators, growth promotor agents, and several chemical compounds are looking not enough to cope or no more extensive use with the current scenario. The BABA application provides an advanced picture of the possible role in improving crops under biotic and abiotic stress tolerance. It systemically and locally induces both physical and chemical way of defense mechanisms against various biotic and abiotic attacks. However, the BABA-like compound that generates long-lasting effects from seedling to fruit storage shows its diverse range of effectiveness. However, much research is needed to decipher the molecular role of BABA as a signaling molecule that opens the gate of plant physiology and helps to understand the possibilities in future crop improvement programs. Moreover, priming based on BABA should act as a central key player in the development of several efficient strategies that exploit the defense systems to stress and yield enough food quantity for the fastest growing population. Thus, β-aminobutyric acid is a potential chemical molecule to devise effective stress management tools against various biotic, abiotic, as well as plant-­ growth-­related functions and advanced method to study the physiological, chemical, genetic, or molecular coordination in plants.

References Abid G, Ouertani RN, Jebara SH, Boubakri H, Muhovski Y, Ghouili E, Abdelkarim S, Chaieb O, Hidri Y, Kadri S, El Ayed M (2020) Alleviation of drought stress in faba bean (Vicia faba L.) by exogenous application of β-aminobutyric acid (BABA). Physiol Mol Biol Plants 26:1173–1186 Ali S, Ganai BA, Kamili AN, Bhat AA, Mir ZA, Bhat JA, Tyagi A, Islam ST, Mushtaq M, Yadav P, Rawat S (2018) Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiol Res 212:29–37 Anamika, Mehta S, Singh B, Patra A, Islam MA (2019) Databases: a weapon from the arsenal of bioinformatics for plant abiotic stress research. In: Recent approaches in Omics for plant resilience to climate change. Springer, Cham, pp 135–169

268

A. Choudhary et al.

Anter AA, Amin AW, Ashoub AH, El-Nuby AS (2014) Evaluation of some chemical substances as inducers for tomato resistance against root-knot nematode, Meloidogyne incognita. Egypt J Agronematol 13:124–145 Anup CP, Melvin P, Shilpa N, Gandhi MN, Jadhav M, Ali H, Kini KR (2015) Proteomic analysis of elicitation of downy mildew disease resistance in pearl millet by seed priming with β-aminobutyric acid and Pseudomonas fluorescens. J Proteome 120:58–74 Baccelli I, Mauch-Mani B (2016) β-aminobutyric acid priming of plant defense: the role of ABA and other hormones. Plant Mol Biol 91:703–711 Baccelli I, Mauch-Mani B (2017) When the story proceeds backward: the discovery of endogenous β-aminobutyric acid as the missing link for a potential new plant hormone. Commun Integr Biol 10:e1290019 Baier M, Bittner A, Prescher A, van Buer J (2019) Preparing plants for improved cold tolerance by priming. Plant Cell Environ 42:782–800 Balint-Kurti P (2019) The plant hypersensitive response: concepts, control and consequences. Mol Plant Pathol 20:1163–1178 Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B (2015) The ‘prime-ome’: towards a holistic approach to priming. Trends Plant Sci 20:443–452 Barilli E, Rubiales D, Amalfitano C, Evidente A, Prats E (2015) BTH and BABA induce resistance in pea against rust (Uromyces pisi) involving differential phytoalexin accumulation. Planta 242:1095–1106 Barrado E, Rodriguez JA, Castrillejo Y (2009) Determination of primary amino acids in wines by high performance liquid magneto-chromatography. Planta 78:672–675 Ben RI, Pastor V, Gravel V, Mauch-Mani B (2018) Impact of β-aminobutyric acid on induced resistance in tomato plants exposed to a combination of abiotic and biotic stress. J Agric Sci Bot 2:12–23 Bengtsson T, Holefors A, Witzell J, Andreasson E, Liljeroth E (2014) Activation of defence responses to Phytophthora infestans in potato by BABA. Plant Pathol 63:193–202 Bharti J, Sahil, Mehta S, Ahmad S, Singh B, Padhy AK, Srivastava N, Pandey V (2021) Mitogen-­ activated protein kinase, plants and heat stress. In: Harsh environment and plant resilience. Springer Nature, Switzerland AG, Cham, pp 324–355 Cao HH, Zhang M, Zhao H, Zhang Y, Wang XX, Guo SS, Zhang ZF, Liu TX (2014) Deciphering the mechanism of β-aminobutyric acid-induced resistance in wheat to the grain aphid, Sitobion avenae. PLoS One 9:e91768 Chea S, Yu DJ, Park J, Oh HD, Chung SW, Lee HJ (2019) Preharvest β-aminobutyric acid treatment alleviates postharvest deterioration of ‘Bluecrop’ highbush blueberry fruit during refrigerated storage. Sci Hortic 246:95–103 Chinnasri B, Sipes BS, Schmitt DP (2006) Effects of inducers of systemic acquired resistance on reproduction of Meloidogyne javanica and Rotylenchulus reniformis in pineapple. J Nematol 38:319–325 Choudhary A, Kumar A, Kaur N (2019) ROS and oxidative burst: Roots in plant development. Plant Divers 42:33–43 Choudhary A, Kumar A, Kaur N, Paul A (2020) Plasmodesmata the Nano Bridges in Plant Cell: Are the Answer for All the Developmental Processes? Russ J Plant Physiol 67:785–796 Choudhary A, Kumar A, Kaur N, Kaur H (2021) MiRNA: the taskmaster of plant world. Biologia 76:1551–1567 Cohen Y (1994) 3-Aminobutyric acid induces systemic resistance against Peronospora tabacina. Physiol Mol Plant Pathol 44:273–288 Cohen Y (2001) The BABA story of induced resistance. Phytoparasitica 29:375–378 Cohen Y (2002) β-aminobutyric acid-induced resistance against plant pathogens. Plant Dis 86:448–457 Cohen Y, Gisi U (1994) Systemic translocation of 14C-DL-3-aminobutyric acid in tomato plants against Phytophthora infestans. Physiol Mol Plant Pathol 45:441–446

Plant Performance and Defensive Role of β-Amino Butyric Acid Under Environmental…

269

Cohen Y, Reuveni M, Baider A (1999) Local and systemic activity of BABA (DL-3-aminobutyric acid) against Plasmopara viticola in grapevines. Eur J Plant Pathol 105:351–361 Cohen Y, Korat M, Zvi-Tov D (2004) Method to protect plants from fungal infection. US Patent 6,692,774 B2 Cohen Y, Rubin AE, Kilfin G (2010) Mechanisms of induced resistance in lettuce against Bremia lactucae by DL-β-amino-butyric acid (BABA). Eur J Plant Pathol 126:553–573 Cohen Y, Rubin AE, Vaknin M (2011) Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce. Eur J Plant Pathol 130:13–27 Conrath U, Beckers GJ, Langenbach CJ, Jaskiewicz MR (2015) Priming for enhanced defense. Annu Rev Phytopathol 53:97–119 Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163 Csikász-Krizsics A, Mátai A, Nagy Á, Kovács S, Végh B, Werner J (2013) BABA (β-aminobutyric acid) induced resistance against grey mould and virus infection in grapevine. IOBC-WPRS Bull 89:429–432 Dhakate P, Sharma P, Mehta S, Akter J, Bhatt V, Chandanshive S, Chakravarty D, Rahman M, Islam MA (2019) Beneficial role of metalloids in plants: molecular understanding and applicability. In: Recent Approaches in Omics for Plant Resilience to Climate Change. Springer, Cham, pp 357–387 Dilawari R, Kaur N, Priyadarshi N, Kumar B, Abdelmotelb KF, Lal SK, Singh B, Tripathi A, Aggarwal SK, Jat BS, Mehta S (2021) Genome Editing: A Tool from the Vault of Science for Engineering Climate-Resilient Cereals. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 45–72 Du YL, Wang ZY, Fan JW, Turner NC, Wang T, Li FM (2012) b-Aminobutyric acid increases abscisic acid accumulation and desiccation tolerance and decreases water use but fails to improve grain yield in two spring wheat cultivars under soil drying. J Exp Bot 63:4849–4860 Dubreuil-Maurizi C, Trouvelot S, Frettinger P, Pugin A, Wendehenne D (2010) β-Aminobutyric acid primes an NADPH oxidase-dependent reactive oxygen species production during grapevine-­triggered immunity. Mol Plant Microbe Interact 23:1012–1021 Embiale A, Hussein M, Husen A, Sahile S, Mohammed K (2016) Differential Sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Eschen-Lippold L, Altmann S, Rosahl S (2010) DL-β-aminobutyric acid-induced resistance of potato against Phytophthora infestans requires salicylic acid but not oxylipins. Mol Plant Microbe Interact 23:585–592 Fischer MJ, Farine S, Chong J, Guerlain P, Bertsch C (2009) The direct toxicity of BABA against grapevine ecosystem organisms. Crop Prot 28:710–712 Floryszak-Wieczorek J, Arasimowicz-Jelonek M, Milczarek G, Janus L, Pawlak-Sprada S, Abramowski D, Deckert J, Billert H (2012) Nitric oxide-mediated stress imprint in potato as an effect of exposure to a priming agent. Mol Plant Microbe Interact 25:1469–1477 Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525 Gamliel A, Katan J (1992) Influence of seed and root exudates on fluorescent pseudomonads and fungi in solarized soil. Phytopathology 82:320–327 Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE (2006) Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202 Gur L, Reuveni M, Stern R, Cohen Y (2013) Integrated control of Alternaria blotch on cv. ‘Cripps Pink’ apple fruits. Phytoparasitica 41:458–459

270

A. Choudhary et al.

Hamiduzzaman MM, Jakab G, Barnavon L, Neuhaus JM, Mauch-Mani B (2005) β-aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol Plant Microbe Interact 18:819–829 Hassan MA, Abo-Elyousr KA (2013) Activation of tomato plant defence responses against bacterial wilt caused by Ralstonia solanacearum using DL-3-aminobutyric acid (BABA). Eur J Plant Pathol 136:145–157 Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052 Hodge S, Thompson GA, Powell G (2005) Application of DL-beta-aminobutyric acid (BABA) as a root drench to legumes inhibits the growth and reproduction of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Bull Entomol Res 95:449–455 Hodge S, Pope TW, Holaschke M, Powell G (2006) The effect of b-aminobutyric acid on the growth of herbivorous insects feeding on Brassicaceae. Ann Appl Biol 148:223–229 Hong JK, Hwang BK, Kim CH (2001) Induction of local and systemic resistance to colletotrichum coccodes in pepper plants by Dl-β-Amino-n-Butyric Acid. J Phytopathol 147:193–198 Hossain Z, Makino T, Komatsu S (2012) Proteomic study of β-aminobutyric acid-mediated cadmium stress alleviation in soybean. J Proteome 75:4151–4164 Husen A (1997) Impact of air pollution on the growth and development of Datura innoxia Mill. M.Sc. Dissertation, Jamia Hamdard, New Delhi, India Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186 Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agric Food Secur 7:44 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Jakab G, Cottier V, Toquin V, Rigoli G, Zimmerli L, Métraux JP, Mauch-Mani B (2001) β-Aminobutyric acid-induced resistance in plants. Eur J Plant Pathol 107:29–37 Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274 Ji HL, Kyndt T, He W, Vanholme B, Gheysen G (2015) β-Aminobutyric acid-induced resistance against root-knot nematodes in rice is based on increased basal defense. Mol Plant Microbe Interact 28:519–533 Jiang L, Yang RZ, Lu YF, Cao SQ, Ci LK, Zhang JJ (2012) b-Aminobutyric acid mediated tobacco tolerance to potassium deficiency. Russ J Plant Physiol 59:781–787 Jisha KC, Puthur JS (2016a) Seed priming with beta-amino butyric acid improves abiotic stress tolerance in rice seedlings. Rice Sci 5:242–254 Jisha KC, Puthur JT (2016b) Seed priming with BABA (b-amino butyric acid): a cost-effective method of abiotic stress tolerance in Vigna radiata (L.) Wilczek. Protoplasma 253:227–289 Kammerer D, Claus A, Schieber A, Carle R (2005)  A Novel Process for the Recovery of Polyphenols from Grape (Vitis vinifera L.) Pomace. J Food Sci 70:157–163

Plant Performance and Defensive Role of β-Amino Butyric Acid Under Environmental…

271

Karmakar NC, Ghosh R, Purkayastha RP (2003) Plant defence activators inducing systemic resistance in Zingiber officinale Rosc. against Pythium aphanidermatum (Edson) Fitz. Indian J Biotechnol 2:591–595 Koen E, Trapet P, Brulé D, Kulik A, Klinguer A, Atauri-Miranda L, Meunier-Prest R, Boni G, Glauser G, Mauch-Mani B, Wendehenne D (2014) β-Aminobutyric acid (BABA)-induced resistance in Arabidopsis thaliana: link with iron homeostasis. Mol Plant Microbe Interact 27:1226–1240 Kumar A, Sharma A, Sharma R, Srivastava P, Choudhary A (2021) Exploration of Wheat wild relative diversity from Lahaul Valley –a cold arid desert of Indian Himalayas. Cereal Res Commun 10.1007/s42976-021-00166-w Lal SK, Kumar S, Sheri V, Mehta S, Varakumar P, Ram B, Borphukan B, James D, Fartyal D, Reddy MK (2018) Seed priming: an emerging technology to impart abiotic stress tolerance in crop plants. In: Advances in seed priming. Springer, Singapore, pp 41–50 Li J, Trivedi P, Wang N (2016) Field evaluation of plant defense inducers for the control of citrus huanglongbing. Phytopathology 106:37–46 Li T, Fan P, Yun Z, Jiang G, Zhang Z, Jiang Y (2019) β-aminobutyric acid priming acquisition and defense response of mango fruit to Colletotrichum gloeosporioides infection based on quantitative proteomics. Cells 8:1029 Li R, Sheng J, Shen L (2020) Nitric Oxide plays an important role in β-aminobutyric acid-induced resistance to Botrytis cinerea in tomato plants. Plant Pathol J 36:121–132 Liu S, Xiao X, Liu Z, Lu X, You B, Guo J, He K, Chen X (2016) A preliminary study on BABA-­ induced resistance to cadmium stress of tobacco. Acta Tabac Sin 22:101–108 Luna E, Van Hulten M, Zhang Y, Berkowitz O, López A, Pétriacq P, Sellwood MA, Chen B, Burrell M, Van De Meene A, Pieterse CM (2014) Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol 10:450–456 Luna E, Beardon E, Ravnskov S, Scholes J, Ton J (2016) Optimizing chemically induced resistance in tomato against Botrytis cinerea. Plant Dis 100:704–710 Ma XH, Xu JY, Han D, Huang WX, Dang BJ, Jia W, Xu ZC (2020) Combination of β-aminobutyric acid and Ca2+ alleviates chilling stress in Tobacco (Nicotiana tabacum L.). Front Plant Sci 11:556 Macarisin D, Wisniewski ME, Bassett C, Thannhauser TW (2009) Proteomic analysis of b-­aminobutyric acid priming and abscisic acid–induction of drought resistance in crabapple (Malus pumila): effect on general metabolism, the phenyl propanoid pathway and cell wall enzymes. Plant Cell Environ 32:1612–1631 Mahmud JA, Hasanuzzaman M, Khan MI, Nahar K, Fujita M (2020) β-Aminobutyric Acid pretreatment confers salt stress tolerance in Brassica napus L. by modulating reactive oxygen species metabolism and methylglyoxal detoxification. Plants 9:241 Malekzadeh P, Khara J, Heidari R (2012) Effect of exogenous gama-aminobutyric acid on physiological tolerance of wheat seedlings exposed to chilling stress. Iran J Plant Physiol 3:611–617 Marcucci E, Aleandri MP, Chilosi G, Magro P (2010) Induced resistance by β-Aminobutyric acid in artichoke against white mould caused by Sclerotinia sclerotiorum. J Phytopath 158:659–667 Mehta S, James D, Reddy MK (2019a) Omics technologies for abiotic stress tolerance in plants: current status and prospects. In: Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 1–34 Mehta S, Singh B, Dhakate P, Rahman M, Islam MA (2019b) Rice, marker-assisted breeding, and disease resistance. In: Disease resistance in crop plants. Springer, Cham, pp 83–111 Mehta S, Lal SK, Sahu KP, Venkatapuram AK, Kumar M, Sheri V, Varakumar P, Vishwakarma C, Yadav R, Jameel MR, Ali M, Achary VMM, Reddy MK (2020) CRISPR/Cas9-Edited Rice: A New Frontier for Sustainable Agriculture. In: New Frontiers in Stress Management for Durable Agriculture. Springer, Singapore, pp 427–458

272

A. Choudhary et al.

Mehta S, Gogna M, Singh B, Patra A, Singh IK, Singh A (2021) Silicon: a plant nutritional “non-­ entity” for mitigating abiotic stresses. In: Plant stress biology. Springer, Singapore, pp 17–49 Mehta S, Singh B, Patra A, Tripathi A, Easwaran M, Choudhary JR, Choudhary M, Aggarwal SK (2021) Maize microbiome: current insights for the sustainable agriculture. In: Microbiomes and Plant Health. Academic Press, Massachusetts, pp 267–297 Mehta S, Chakraborty A, Roy A, Singh IK, Singh A (2021) Fight Hard or Die Trying: Current Status of Lipid Signaling during Plant–Pathogen Interaction. Plants 10:1098 Mohamadi N, Baghizadeh A, Saadatmand S, Asrar Z (2017) Alleviation of oxidative stress induced by drought stress through priming by β-aminobutyric acid (BABA) in Rapeseed (Brassica napus L.) plants. Iran J Plant Physiol 7:2203–2210 Mongae A, Moleleki L (2015) The effect of β-aminobutyric acid (BABA) on root knot nematode and soft rot pathogen disease complexes in Solanum tuberosum plants. Eur J Plant Pathol 142:117–124 Mostek A, Borner A, Weidner S (2016) Comparative proteomic analysis of β-aminobutyric acid-­ mediated alleviation of salt stress in barley. Plant Physiol Biochem 99:150–161 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681 Nayyar H, Kaur R, Kaur S, Singh R (2014) γ-Aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul 33:408–419 Oka Y, Cohen Y (2001) Induced resistance to cyst and root-knot nematodes in cereals by DL-b-­ amino-n-butyric acid. Eur J Plant Pathol 107:219–227 Oka Y, Cohen Y, Spiegel Y (1999) Local and systemic induced resistance to the root-knot nematode in tomato by DL-β-amino-n-butyric acid. Phytopathology 89:1138–1143 Ovadia A, Biton R, Cohen Y, Katzir N,  Paris HS (2000) Induced resistance to downy mildew and Fusarium wilt in cucurbits. In Proceedings of CUCURBITACEAE. The 7 th EUCARPIA Meeting on Cucurbit Genetics and Breeding Acta Hortic 55–59 Pajot E, Silue D (2005) Evidence that DL-3-aminobutyric acid and acibenzolar-S-methyl induce resistance against bacterial head rot disease of broccoli. Pest Manag Sci 61:1110–1114 Pajot E, Le Corre D, Silue D (2001) Phytogard and DL-baminobutyric acid (BABA) induce resistance in lettuce (Lactuca sativa L.) against downy mildew (Bremia lactucae). Eur J Plant Pathol 107:861–869 Papavizas GC, Davey CB (1963) Effect of sulfur-containing amino compounds and related substances on Aphanomyces root rot of peas. Phytopathology 53:109–115 Pastor V, Balmer A, Gamir J, Flors V, Mauch-Mani B (2014) Preparing to fight back: generation and storage of priming compounds. Front Plant Sci 5:295 Peters GP, Marland G, Le Quéré C, Boden T, Canadell JG, Raupach MR (2011) Rapid growth of CO2 emission after the 2008–2009 global financial crisis. Nat Clim Chang 2:1–3 Pfautsch S, Gessler A, Adams MA, Rennenberg H (2009) Using amino-nitrogen pools and fluxes to identify contributions of understory Acacia spp. to overstory Eucalyptus regnans and stand nitrogen uptake in temperate Australia. New Phytol 183:1097–1113 Philippe R, Ferreol B, Sophie A, Marie-Noelle B (2016) DL- β -aminobutyric acid application negatively affects reproduction and larval development of the rosy apple aphid, Dysaphis plantaginea, on apple. Entomol Exp Appl 159:46–53 Polyakovskii SA, Kravchuk ZN, Dmitriev AP (2008) Mechanism of action of the plant resistance inducer b-aminobutyric acid in Allium cepa. Cytol Genet 42:369–372 Porat R, Vinokur V, Weiss B, Cohen L, Daus A, Goldschmidt EE, Droby S (2003) Induction of resistance to Penicillium digitatum in grapefruit by b-aminobutyric acid. Eur J Plant Pathol 109:901–907 Prieto JD, Alomar O, Agustí N, Battaglia D, Fanti P, Trotta V, Castañé C (2020) Does the plant defense priming compound β-aminobutyric acid affect the performance of Macrolophus pygmaeus when used to control Bemisia tabaci in tomato? Phytoparasitica 49:195–205

Plant Performance and Defensive Role of β-Amino Butyric Acid Under Environmental…

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Quéro A, Fliniaux O, Elboutachfaiti R, Petit E, Guillot X, Hawkins S, Courtois J, Mesnard F (2015) b-Aminobutyric acid increases drought tolerance and reorganizes solute content and water homeostasis in flax (Linum usitatissimum). Metabolomics 11:1363–1375 Rahman M, Sultana S, Nath D, Kalita S, Chakravarty D, Mehta S, Wani SH, Islam MA (2019) Molecular breeding approaches for disease resistance in sugarcane. In: Disease Resistance in Crop Plants. Springer, Cham, pp 131–155 Rajaei P, Mohamadi N (2013) Effect of beta-aminobutyric acid (BABA) on enzymatic and non-­ enzymatic antioxidants of Brassica napus L. under drought stress. Int J Biosci 3:41–47 Rajput LS, Aggarwal SK, Mehta S, Kumar S, Nataraj V, Shivakumar M, Maheshwari HS, Yadav S, Goswami D (2021) Role of WRKY Transcription Factor Superfamily in Plant Disease Management. In: Plant Stress Biology. Springer, Singapore, pp 335–361 Rejeb IB, Pastor V, Gravel V, Mauch-Mani B (2018) Impact of β-aminobutyric acid on induced resistance in tomato plants exposed to a combination of abiotic and biotic stress. J Agric Sci Bot 2:12–23 Reuveni M, Sheglov D, Cohen Y (2003) Control of moldy-core decay in apple fruits by β-aminobutyric acids and potassium phosphites. Plant Dis 87:933–936 Robert P, Braud F, Aligon S, Brisset MN (2016) DL-β-aminobutyric acid application negatively affects reproduction and larval development of the rosy apple aphid, Dysaphis plantaginea, on apple. Entomol Exp Appl 159:46–53 Rohiwala P, Bharat NK, Negi S, Sharma P, Padiyal A (2020) Priming of radish seeds with plant elicitors like SA, MeJA, BABA and KNO3 improves seed quality, seedling quality and seed health. J Pharmacogn Phytochem 9:2709–2713 Roylawar P, Kamble A (2017) β–amino butyric acid mediated changes in cellular redox homeostasis confers tomato resistance to early blight. Australas Plant Pathol 46:239–249 Sahebani N, Hadavi N (2009) Induction of H2O2 and related enzymes in tomato roots infected with root knot nematode (M. javanica) by several chemical and microbial elicitors. Biocontrol Sci Technol 19:301–313 Sahil, Keshan R, Patra A, Mehta S, Abdelmotelb KF, Lavale SA, Chaudhary M, Aggarwal SK, Chattopadhyay A (2021) Expression and regulation of stress-responsive genes in plants under harsh environmental conditions. In: Harsh environment and plant resilience. Springer Nature, Switzerland AG, Cham, pp 26–45 Schmitt AJ, Roy R, Klinkenberg PM, Jia M, Carter CJ (2018) The octadecanoid pathway, but not coi1, is required for nectar secretion in Arabidopsis thaliana. Front Plant Sci 9:1060 Schwarzenbacher RE, Luna E, Ton J (2014) The discovery of the BABA receptor: scientific implications and application potential. Front Plant Sci 5:304 Shailasree S, Sarosh BR, Vasanthi NS, Shetty HS (2001) Seed treatment with β-aminobutyric acid protects Pennisetum glaucum systemically from Sclerospora graminicola. Pest Manag Sci 57:721–728 Shailasree S, Ramachandra KK, Shetty SH (2007) β-amino butyric acid-induced resistance in pearl millet to downy mildew is associated with accumulation of defence-related proteins. Australas Plant Pathol 36:204–211 Sharma P, Sharma MM, Patra A, Vashisth M, Mehta S, Singh B, Tiwari M, Pandey V (2020) The role of key transcription factors for cold tolerance in plants. In: Transcription factors for abiotic stress tolerance in plants. Academic, Cambridge, pp 123–152 Sharma P, Sharma MMM, Malik A, Vashisth M, Singh D, Kumar R, Singh B, Patra A, Mehta S, Pandey V (2021) Rhizosphere, Rhizosphere Biology, and Rhizospheric Engineering. In: Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management. Springer, Cham, pp 577–624 Siegrist J, Orober M, Buchenauer H (2000) b-Aminobutyric acid mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiol Mol Plant Pathol 56:95–106 Singh PK, Wu CC, Zimmerli L (2010) β-Aminobutyric acid priming by stress imprinting. Plant Signal Behav 5:878–880

274

A. Choudhary et al.

Singh B, Mehta S, Aggarwal SK, Tiwari M, Bhuyan SI, Bhatia S, Islam MA (2019) Barley, disease resistance, and molecular breeding approaches. In: Disease resistance in crop plants. Springer, Cham, pp 261–299 Slaughter AR, Hamiduzzaman MM, Gindro K, Neuhaus JM, Mauch-Mani B (2008) Beta-­ aminobutyric acid induced resistance in grapevine against downy mildew: involvement of pterostilbene. Eur J Plant Pathol 122:185–195 Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B (2012) Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843 Sós-Hegedűs A, Juhász Z, Poór P, Kondrák M, Antal F, Tari I, Mauch-Mani B, Bánfalvi Z (2014) Soil drench treatment with β-aminobutyric acid increases drought tolerance of potato. PLoS One 9:e114297 Sripinyowanich S, Klomsakul P, Boonburapong B, Bangyeekhun T, Asami T, Gu H, Buaboocha T, Chadchawan S (2013) Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): the role of OsP5CS1 and OsP5CR gene expression during salt stress. Environ Exp Bot 86:94–105 Tavallali V, Karimi S, Mohammadi S, Hojati S (2008) Effects of b-aminobutyric acid on the induction of resistance to Penicillium italicum. World Appl Sci J 5:345–351 Thevenet D, Pastor V, Baccelli I, Balmer A, Vallat A, Neier R, Glauser G, Mauch-Mani B (2017) The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol 213:552–559 Tiwari S, Meyer WL, Stelinski LL (2013) Induced resistance against the Asian citrus psyllid, Diaphorina citri, by β-aminobutyric acid in citrus. Bull Entomol Res 103:592–600 Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN, Métraux JP, Mauch-Mani B (2005) Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987–999 Tworkoski T, Wisniewski M, Artlip T (2011) Application of BABA and s-ABA for drought resistance in apple. J Appl Hortic 13:85–90 Vaknin M (2016) Genetic resistance and induced resistance against Bremia lactucae in lettuce: microscopy and mechanism. PhD Thesis submitted to Bar-Ilan University, Israel Venegas-Molina J, Proietti S, Pollier J, Orozco-Freire W, Ramirez-Villacis D, Leon-Reyes A (2020) Induced tolerance to abiotic and biotic stresses of broccoli and Arabidopsis after treatment with elicitor molecules. Sci Rep 10:1–17 Vijayakumari K, Puthur JT (2016) g-Aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Regul 78:57–67 Viswanath KK, Varakumar P, Pamuru RR, Basha SJ, Mehta S, Rao AD (2020) Plant lipoxygenases and their role in plant physiology. J Plant Biol 63:83–95 Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151 Wang L, Jin P, Wang J, Jiang L, Shan T, Zheng Y (2015) Effect of β-aminobutyric acid on cell wall modification and senescence in sweet cherry during storage at 20 degrees C. Food Chem 175:471–477 Wang K, Liao Y, Xiong Q, Kan J, Cao S, Zheng Y (2016) Induction of direct or priming resistance against Botrytis cinerea in strawberries by β-aminobutyric acid and their effects on sucrose metabolism. J Agric Food Chem 64:5855–5865 Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631 Worrall D, Holroyd GH, Moore JP, Glowacz M, Croft P, Taylor JE, Paul ND, Roberts MR (2012) Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytol 193:770–778 Wu CC, Singh P, Chen MC, Zimmerli L (2010) L-Glutamine inhibits b-aminobutyric acid-induced stress resistance and priming in Arabidopsis. J Exp Bot 61:995–1002

Plant Performance and Defensive Role of β-Amino Butyric Acid Under Environmental…

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Xu Q, Li HX, Xian XL, Ling LI, Rui CH, Wei SO, Wei FU, Pan YZ (2018) Effects of BABA on photosynthetic characteristics and antioxidative system in Rhododendron under NaHCO3 Stress. Forest Res 31:133–140 Yadav V, Wang Z, Wei C, Amo A, Ahmed B, Yang X, Zhang X (2020) Phenylpropanoid pathway engineering: an emerging approach towards plant defense. Pathogens 9:312 Yadav B, Jogawat A, Lal SK, Lakra N, Mehta S, Shabek N, Narayan OP (2021) Plant mineral transport systems and the potential for crop improvement. Planta 253:45 Zhang S, Schisler DA, Boehm MJ, Slininger PJ (2007) Utilization of chemical inducers of resistance and Cryptococcus flavescens OH 182.9 to reduce Fusarium head blight under greenhouse conditions. Biol Control 42:308–315 Zhang C, Wang J, Zhang J, Hou C, Wang G (2011) Effects of b-aminobutyric acid on control of postharvest blue mould of apple fruit and its possible mechanisms of action. Postharvest Biol Technol 61:145–151 Zimmerli L, Jakab G, Métraux JP, Mauch-Mani B (2000) Potentiation of pathogen-specific defense mechanisms in Arabidopsis by b-aminobutyric acid. Proc Natl Acad Sci U S A 97:12920–12925 Zimmerli L, Métraux JP, Mauch-Mani B (2001) β-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol 126:517–523 Zimmerli L, Hou BH, Tsai CH, Jakab G, Mauch-Mani B, Somerville S (2007) The xenobiotic b-aminobutyric acid enhances Arabidopsis thermotolerance. Plant J 53:144–156

Plant Performance and Defensive Role of γ-Gamma Amino Butyric Acid Under Environmental Stress Antul Kumar, Anuj Choudhary, Harmanjot Kaur, Mohammed Javed, and Sahil Mehta

1  Introduction Globally, the human population will mark 9.6 billion people, and 2050 will confront severe challenges in which fulfilling food security issues is a predominant concern (Sita and Kumar 2020; Mehta et al. 2021). Even before the advent of COVID-19, 135 million people worldwide were currently experiencing severe food insecurity and the current scenario created a situation of “unpredictable and inevitable crisis within a crisis” (FAO 2020; Ahmad et al. 2021). According to the UN (2019), food security is an essential and prime issue for fulfilling goals of sustainable development and hunger eradication concerns. In the Worldwide Global Nutrition Report (2020), currently, every developing nation is facing the crisis of nutritional deficiencies due to the poor framework of the field to plate and it turns into crucial challenges to policy-makers. The impact of climate change and unregulated environmental factors affect crop production and quality, by imposing deleterious changes in their growing condition (Priya et al. 2019; Sharma et al. 2020; Bharti et al. 2021; Sahil et al. 2021; Rajput et al. 2021). Under natural conditions, plants are often exposed to biotic (pests and weeds) and abiotic (salinity, UV, air, flooding, drought, heat, and chilling temperature) stresses (Mehta et  al. 2019a, b, 2020; Singh et  al. 2019; Rahman et  al. 2019; Choudhary et al. 2020; Kumar et al. 2021; Rajput et al. 2021; Dilawari et al. 2021). Withstand under such conditions needs a well-­tuned and sophisticated defense A. Kumar · A. Choudhary · H. Kaur Department of Botany, Punjab Agricultural University, Ludhiana, India M. Javed Division of Plant Pathology, ICAR-Indian Agriculture Research Institute, New Delhi, India S. Mehta (*) International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_11

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Fig. 1  Molecular structure of gamma-aminobutyric acid (GABA)

system that results in stress avoidance, resistance, and tolerance based on genetic regulations which are ensemble and regulated by plant hormones and that favors the plants to overcome such adverse situation (Priya et al. 2019; Sita and Kumar 2020; Choudhary et al. 2021; Bharti et  al. 2021; Sahil et  al. 2021; Rajput et  al. 2021). Instead of that, plant hormones play a significant role in various biochemical processes, mediating growth and development, and also indulged in signal cascading permitting the plant’s innate immune system to sustain a basal level of resistance (Viswanath et al. 2020). Interestingly, plants manage the sensitivity of their immune response upon eliciting specific synthetic and natural stimuli (Mehta et al. 2021; Thevenet et al. 2017). Recently, several synthetic chemical priming agents are utilized as priming agents as to enhance the plant performance and productivity under adverse conditions (Lal et al. 2018). In this context, the γ-aminobutyric acid (GABA), an emerging nonproteinogenic agent amino acid, owns a special place to its wide range of action (Kaur 2013; AL-Quraan 2015; Mahmud et al. 2017; Takeuchi 2018; Seifikalhor et al. 2019; Hany et al. 2020; Che-Othman et al. 2020; Pelgrom et al. 2020) Fig. 1. It plays a significant role in plant antioxidant defenses and osmoregulation and serves as signaling molecules under stressful conditions (Sita and Kumar 2020). Historically, it is was firstly reported in Solanum tuberosum (storage tissue) but later on several angiosperm species Zea mays (fruits), Cucurbita pepo (fruits), Capsicum frutescence (pericarp), Nicotiana tabacum (leaf root and axillary buds), Daucus carota (vascular tissues), Phaseolus vulgaris (fruits, flowers, and leaves), Lupinus album (leaf stem and root), Pyrus malus (leaf and fruit), Beta vulgaris (storage root), Rheum rhaponticum (petioles), Tulipa gesneriana (bulb and leaf), Lolium perenne (leaf), Pisum sativum (seeds), Mentha piperita (leaf, stem, and root), Lupinus albus (stem, root, and leaf), Cucurbita maxima (seeds and pericarp), and Persea americana (fruit) have confirmed its presence till the present date (Sita and Kumar 2020). GABA acts as endogenous signaling molecules that are significantly involved in growth and development (Kaur 2013; AL-Quraan 2015; Mahmud et al. 2017; Takeuchi 2018; Seifikalhor et al. 2019; Hany et al. 2020; Che-Othman et al. 2020; Pelgrom et al. 2020). As a crucial component of intermediate in amino acid and nitrogen metabolism, it mitigates stresses through upregulation of antioxidant defense systems, therefore promising shelf life due to increase in storage quality and antioxidant system. The concentration of GABA enhanced with elevating seed germination stage but its content fluctuates with growing conditions (Tian et al. 2005; Li et al. 2016). The role of GABA has gained much attention in recent decades following the investigations that extracellular and intracellular GABA content effectively in response to various stress (Tables 1, 2, and 3). However, the concentration of GABA ranges from 0.03 to 2.0 μmolg−1 in fresh tissues of the plant and it gets enhanced several

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Table 1  Potential role of GABA and involvement of molecular pathways in abiotic stress tolerance in crop plants Stress type Crop plant Drought Maize, tomato, muskmelon, faba bean, ryegrass, bentgrass and bread wheat

Pathways Genes regulation involved CDPK26, WRKY75, GABA-shunt pathway MAPK1, ABF3, HSP70, MT1, MYB13,14-3-3

Salinity

POP2-1, THE Tobacco, wheat, maize POP2-5, GAD1,2, SlGAD1, SlGAD3, and tomato SlGAD4

TCA cycle, GABA-shunt pathway

Heavy metal

ZmGAD, ZmGAD2 Tobacco, soybean, rice and beans

GABA shunt pathway

Results Improve shoot and root biomass, leaf area, modulate antioxidative defense system, improved nutrient acquisition, osmolyte accumulation, relative water content and plant growth Activates antioxidant enzymatic activity, enhances plant salt tolerance, increases biomass and crop growth via reducing rate of chlorophyll degradation, altering water potential and maintaining high photosynthetic capacity Promote stomatal conductivity, leaf area index, osmotic regulation and root architecture regulation results in improving yield attributes

References Farooq et al. (2017); Li et al. (2018); Hany et al. (2020)

Cheng et al. (2018); Jin et al. (2019); Wu et al. (2020); Che-­ Othman et al. (2020)

Mahmud et al. (2017); Seifikalhor et al. (2020)

(continued)

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Table 1 (continued) Stress type Heat

Crop plant Rice, cowpea, mungbean, bentgrass, soybean and Arabidopsis

Flooding Soybean and Arabidopsis

Anoxia

Arabidopsis

UV

Rice, Arabidopsis and maize

Cold and Barley, freezing wheat, Litchi, Banana and cucumber

Genes regulation HSFA-6a, HSFA-2c, HSFB-2b, APX3, GmHsp90A2, GmHsp90A4, GmHsp90B1, GmHsp90C1.1, and GmHsp90C2.1

Pathways involved HSF pathways

Results Promote carbon fixation, leaf turgor, and assimilation processes by the alleviating activities of several enzymes; enhances membrane stability and photosynthetic machinery Activating GAD5, AMADH, Polyamine antioxidant GABA-T, SSADH degradation enzymes, pathway, GABA shunt improving photosynthetic rate, inhibit production of ROS and regulating the stomatal opening GAD1, At5g17330; GABA shunt Aid in pollen tube GAD2, At1g65960 pathway growth and guidance, GABA use as an alternative N source when inorganic N is less available HSP90, DHN3, and GABA shunt Maintain cellular homeostasis, MT1 pathway, photosynthesis, TCA respiration, pathway, protein structures ROS and ROS scavenging metabolism pathways Tricarboxylic Enhance the COR, OsCIPK01, content of acid cycle, OsCIPK03, GABA shunt adenosine OsCIPK08, triphosphate and Q9S7E9, OsCIPK12 adenosine and OsCIPK17 diphosphate, improve total plant biomass and crop yield

References Kaur (2013); Priya et al. (2019)

Zhang et al. (2016)

Yo and Allen (2008); Seifikalhor et al. (2019)

AL-Quraan (2015); Seifikalhor et al. (2019)

Sita and Kumar (2020)

Stress type Fungus

Uromyces pisi

Colletotrichum orbiculare

Plasmopara elianthin, Plasmopara halstedii Peronospora parasitica

Bremia lactucae

Fusarium graminearum Sclerospora graminicola

Organism Botrytis allii, Botrytis cinerea

Genes regulation FLG22, SnRK1

Pathways involved Results/application/functional role TCA cycle and GABA Reduce H2O2 accumulation, activate shunt enzyme nitrate reductase, accumulation of glucose and fructose and promote root growth Wheat TRI 101 and GABA shunt Increase contents of glucose, succinate, TRI12 citrate, GABA, glutamine and trehalose Pearl millet PR-1, PR-5 GABA shunt and SA Enhance plant height, fresh weight, leaf biosynthetic pathway area and tillering, and reproductive growth, viz. early flowering, number of productive ear heads and 1000 seed weight Lettuce NPR1/ ABA-dependent Promote plant growth and activate NIM1/SAI1 signaling pathways antioxidant defense enzymes Sunflower PR-1a GABA shunt Decrease chlorosis of leaves and increase plant growth Cauliflower PR-1, PR-2, Salicylic acid pathway Production of pathogenesis-related (PR) PR-5 proteins production and early seedling growth Promote cell membrane integrity, stomatal Cucumber PACC, Jasmonic acid RIM101 (JA)-ethylene mediated conductance and photosynthetic rate systemic resistance pathway Pea GAD1, 2 SA pathway Production of phytoalexins, increase in scopoletin, pisatin and medicarpin contents

Crop plant Onion

Table 2  Potential role of GABA and involvement of molecular pathways in biotic stress tolerance in crop plants

(continued)

Barilli et al. (2010)

Jeun et al. (2004); Harata et al. (2021)

Cohen et al. (2011); Pelgrom et al. (2020) Nandeeshkumar et al. (2009) Silue et al. (2002); Kelsey (2020)

Shailasree et al. (2001); Nandini et al. (2017)

Zhang et al. (2007)

References Polyakovskii et al. (2008); Chinnasri et al. (2006)

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Acyrthosiphon pisum

Myzus persicae

Insects

Virus

Pseudomonas fluorescens

Stress type Organism Bacteria Erwinia amylovora

Table 2 (continued)

White mustard

RDL1, RDL2 Rdl

Atu4243

Broccoli

Beans

Genes regulation PFI

Crop plant Apple

α-DOX1 pathway

GABA shunt

Pathways involved GABA shunt, exopolysaccharide biosynthetic pathway Gac/Rsm pathway Regulating stomatal opening, activates antioxidant enzymes, improving photosynthetic rate, and inhibit the generation of reactive oxygen species (ROS) Promote plant defense systems and photosynthetic rate Enhances photosynthetic rate, reduce chlorophyll degradation and alter water potential

Hodge et al. (2011); Benini (2020) Hodge et al. (2006); Yadav and Rathee (2020)

Pajot and Silue (2005); Takeuchi (2018)

Results/application/functional role References Change levels of phenolics, SOD and POX Hassan and enzymes Buchenauer (2007)

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Mode of applications Seed treatment

Nutrient medium

Foliar spray

Nutrient medium

GABA conc. 1–2 mM/L

2 mM

750 μM/L

1 mM

Oryza sativa L.

Lycopersicon esculentum L.

Piper nigrum L.

Plant Zea mays L.

Biochemical changes Increasing the activity of enzymes, such as superoxide dismutase (SOD), peroxidases (POD), and catalases (CAT) Enhanced ABA Increased root:shoot synthesis, maintain ratio, photosynthetic C:N balance, rate, cell growth and increased regulate stomatal accumulation of closure osmolytes and stress-related proteins Promote the activity Increase seedling of SOD and CAT length, stomatal conductivity and water enzymes, increase proline content potential Improve percent Maintain ion germination, seedling homeostasis, vigor index, predominantly modulating the lowering Na+/K+, activity of H+-ATPase accumulation of compatible solutes and regulating such as proline and stomatal movement starch

Physiological changes Increase plant fresh and dry weight, plant height and promote early growth

Malekzadeh et al. (2014), Gramazio et al. (2020) Increase expression of SlGAD1, OsGAD2 genes

(continued)

Nayyar et al. (2014); Sheteiwy et al. (2019)

Vijayakumari and Puthur (2016); Choy et al. (2020)

Enhance the expression of ATHB-13, ERD6, AP2 and AGL8

Upregulation of OsCIPK12 and OsCIPK17 genes

References Tian et al. (2005); Li et al. (2016)

Molecular changes Upregulate the expression of DHN3, MT1 and HSP90 genes

Table 3  Exogenous application of GABA and its effect on physiological, biochemical, and molecular processes

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10 mM

10 μM/L

Shang et al. (2011); Salvatierra et al. (2016); Gramazio et al. (2020)

Malekzadeh et al. (2012); Zifeng et al. (2020)

References Krishnan et al. (2013)

Upregulate the expression of genes like BnNrt2, CiGAD1 and CiGAD2

Shi et al. (2010); Ji et al. (2017); Wu et al. (2020)

Song et al. (2010); Enhance the gene expression of COR, Razik et al. (2021) OsCIPK01, OsCIPK03, OsCIPK08, Q9S7E9 and OsCIPK12

PpAO1, PpNCED1, PpNCED2, and PpZEP genes activated

Enhance antioxidant enzymes activity in roots, lowers MDA content and reactive oxygen production Higher levels of Along with culture Hordeum vulgare L. Promote the proline, soluble sugar solution photosynthetic rate, stomatal conductance and total protein content; upregulation and quantum of heat-shock proteins efficiency (HSP), dehydrin, osmotin, aquaporin and leaf embryogenesis protein (LEA) Accumulation of Along with culture Caragana Increase the medium intermedia L. germination, stomatal osmolytes, HSPs and conductivity, maintain LEA proteins transpiration and leaf water content

Dipping in GABA solution

Production of heat-shock proteins, osmolyte accumulation

5 mM

Triticum aestivum L. Promote germination, total biomass, membrane integrity and stomatal conductivity Prunus persica L. Increase the chlorophyll content, membrane integrity and total biomass

Foliar spray

500 μM/L

Physiological changes Maintain leaf water content and transpiration rate

Molecular changes Upregulate gene expression of MT1, MYB13, CDPK26, WRKY75, ABF3, HSP70, MAPK1 Increase expression of POP2-1, POP2-5, GAD1,2, SlGAD1 genes

Plant Lolium perenne L.

Biochemical changes Promote antioxidant defense enzymatic activity and nitrate reductase activity

Mode of applications Foliar spray

GABA conc. 70 mM

Table 3 (continued)

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folds under abiotic stress conditions (Shelp et al. 2017; Bhattacharya et al. 2018; Cheng et  al. 2018; Ramos et  al. 2019). Keeping these significant advantages of GABA, this chapter compiles the information on the involvement of GABA in biotic and abiotic stress tolerance.

2  Biosynthesis and Chemical Structure of GABA Chemically, the gamma-aminobutyric acid is abbreviated as GABA with chemical formula C4H9NO2 lying in the category of amino acid but not considered as protein (Fig. 1). The versatile GABA is predominantly indulged in growth and development via the GABA shunt, a sidestep of a tricarboxylic acid cycle (TCA). In plants, GABA is derived from glutamate by irreversible decarboxylation, catalyzed through glutamic acid decarboxylase (GAD) in the cytosolic region (Li et  al. 2021). Consequently, GABA is translocated into the mitochondrial matrix and exposed to transamination to succinic semialdehyde (SSA) through GABA transaminase (GABA-T/POP2). Subsequently, SSA is oxidized to succinate through the activity of a dehydrogenase enzyme SSADH (NAD+-dependent succinate semialdehyde dehydrogenase), and successively succinate feeds into the TCA cycle (Wu et  al. 2020; Li et al. 2021). Ultimately, glutamate and its carbon skeleton enter into the TCA cycle through this GABA shunt and recycles. Alternatively, biosynthesis of GABA is mediated by polyamine metabolic pathway, in which putrescine is obtained from arginine through multistep routes. In the presence of oxygen, polyamine oxidase converts putrescene into either 4-aminobutyraldehyde or spermidine but degrades to 4-aminobutyraldehyde and in turn oxidized to GABA through NAD+-dependent 4-amino-butyraldehyde dehydrogenase. Then synthesized GABA enters into the TCA cycle by the activity of SSADH and GABA-T (Wu et al. 2020; Che-Othman et al. 2020; Li et al. 2021).

3  Regulatory Switch for Mediating Oxidative Machinery Reactive oxygen species (ROS) play a significant role in growth, development, and stress conditions (Choudhary et al. 2019). On GABA applications to stressed plants, the GABA shunt activity enhanced with an endogenous level that increases the photosynthetic capacity and activity of antioxidant enzymes along with malondialdehyde content (MDA) and decreases in ROS production. The enzymes that facilitate through GABA shunt are sensitive to oxidative stress and maintain the membrane integrity under stress conditions (Jia et  al. 2017). Such sensitivity results in low TCAC efficiency which causes the GABA shunt to compensate in a challenging environment. The efficient GABA shunt is essential to regulate ROS production and effectively restricts its production (AL-Quraan 2015). Treatment with γ-vinyl-GABA (inhibitor of GABA-T/POP2) or POP2 gene mutation inhibits the ROS production, improves the growth, and restricts cell death

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in ssadh mutant (Li et al. 2021). The sensitive ssadh mutant shows elevating ROS generation and ultimately cell death when subjected to an abiotic stress environment. Mutant studies on pop2 and pop2-ssadh reviled the hyperaccumulation of GABA as compared to the wild-type tomato. The phenotype of ssadh mutants exhibits several morphological deformations like leaf curling and dwarf size similar to Arabidopsis mutant. SSD (Succinic semialdehyde) can be altered into GHB by SSA reductase activity, and similarly GHB converted into SSA by GHB dehydrogenase activity (Wu et al. 2020; Li et al. 2021). Furthermore, double mutant pop2-­ ssadh exhibits several phenotypes than the wild type, suggesting the increased GABA concentration is independent of the phenotypic of ssadh mutant.

4  Response Strategies of GABA in Abiotic Stress Tolerance The injured part of the plants enhances the GABA accumulation in response to abiotic and biotic stress conditions. Using Agrobacterium tumefaciens, GABA responses stimulate the OC8-HSL N-(3-oxooctanoyl) homoserine lactone and degraded by lactonase AttM which elevates Ti-plasmid conjugated GABA concentrations in tumor suppresses. Eventually, the GABA-accumulated tobacco line was not infected by crown gall disease as compared to wild type (Chevrot et al. 2006). According to Haudecoeur et al. (2009), low GABA-rich tomato lines demonstrate higher T-DNA transfer frequency than control, whereas in Erianthus arundinaceous and Solanum lycopersicum GABA-T activity is mediated by A. tumefaciens to degrade GABA which did not affect the copy number or ploidy level. The finding concluded that GABA restricts T-DNA transfer and that GABA degradation during the co-cultivation acts as an effective approach to enhance T-DNA transfer (Li et al. 2021).

5  Abiotic Stress Tolerance There are several reports on functional aspects of GABA in alleviating unavoidable stress challenges; GABA plays a significant role in the successful pursuit of abiotic stress over the past decade (Fig. 2; Table 1). The information on the potential role of GABA and its applications in crop plants has been summarized in the upcoming sections.

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Fig. 2  Overview of the potential role of GABA as an emerging molecule in agriculture

5.1  Salinity Tolerance In plants, saline conditions activate the Ca2+-mediated GABA shunt via GAD pathway. The concentration of GABA is fluctuated during the growth phases and seems to be increased with salinity stress or either at the advanced stages of growth, e.g., when Nicotiana tabacum plant is exposed with 500 mM of NaCl, the GABA content decreased at first and third day and increased on seventh day of salt treatment (Zhang et al. 2011). Chromium toxicity and their uptake decrease with supplementation of GABA which assist to upregulate the glyoxalase activities (Gly I), catalase (CAT), glutathione reductase (GR), glyoxalase II (Gly II), dehydroascorbate reductase (DHAR), ascorbate peroxidase (APX), glutathione peroxidase (GPX), monodehydroascorbate reductase (MDHAR), and non-enzymatic antioxidants like glutathione and ascorbate which resulted in decreasing the oxidative damages (Mahmud et  al. 2017). Moreover, increased proline content (PC), phytochelatin (PCs), decreased relative water content (RWC) and total chlorophyll content (Chl) ultimately restored the plant growth in Brassica juncea. In muskmelon seedling, exogenous application of GABA improves CaCO3 tolerance by alleviating endogenous GABA concentration and polyamine biosynthesis (PA) which covert free putrescine into bounded-polyamine to prevent the degradation of Polyamine (Jin et al. 2019). However, exogenous application in tomato, white clover, maize, hull-­ less barley, and muskmelon improves the endogenous GABA level to enhance the activities of antioxidant enzymes and increases plant salinity tolerance (Wu et al. 2020; Ma et al. 2019; Wang et al. 2017). In response to salinity, the Na+ exclusion strategy promotes upregulation of GABA content which induces the activation of H+ ATPase and decreases the ROS level, H2O2-induced potassium efflux, and Na+ uptake (Ma et al. 2019). A similar finding was reported in cytoplasmic male sterile (CMS) II line and untreated lines of Nicotiana sylvestris, treated with long- and short-duration saline stress, whereas GABA accumulation is independent of the

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GAD activity (Akcay et al. 2012). In salinity-affected wheat leaves, major metabolic enzymes obligatory for TCA cycle regulation would have been physio-­ chemically restricted by high saline conditions. But the enhanced activity of GABA shunt provides an alternative carbon source to the Krebs cycle for an effective role in mitochondria and overcomes the salinity-sensitive enzymes to mediate the leaf respiration. In durum wheat, accumulation of GABA under high nitrogen could also act as an alternative site of nitrogen source (Carillo 2018). In another study, the resistance of wheat cultivars to osmotic and salinity stress was exhibited to be associated with enhanced GAD expression and accumulation of GABA.  Moreover, wheat seedling shows enhanced tolerance to salinity stress correlated with increased activity of antioxidant enzymes and photosynthetic capacity (Li et al. 2016).

5.2  Heat Tolerance Due to anthropogenic activities coupled with global warming, the heat stress has emerged as one of the detrimental nonbiological stresses worldwide (Anamika et al. 2019; Bharti et  al. 2021). Exogenous supplementation of GABA improves leaf water status, maintains osmolyte concentration and carbon fixation, and resists temperature injuries. According to Nayyar et al. (2014), Oryza sativa seedling shows growth restoration by the stimulation of various antioxidant enzymes under heat stress. It provides partial protection from heat stress impact to rice seedling via upregulating osmoprotectant, enhancing leaf turgor, heat-shock proteins, heat shock factors, tricarboxylic cycle, metabolic homeostasis, and antioxidant activities. In Glycine max, exposure of high temperature to immature seeds shows an elevated concentration of GAD and decreased level of SSADH and GABA-T.  Similarly, heat-treated seeds enhance the GABA concentration more than fivefold (447.5/100 g DW) as compared to untreated seeds (79.6 mg/100 g DW). Consequently, the level of GABA was observed to be enhanced in “Gamy red” (pea-sized grape berries) and ripening grapes upon exposure to heat stress. However, the exogenous application of GABA helps to overcome the challenges of high temperature for morphological and reproductive tissues in the mungbean plants. Moreover, in Arabidopsis roots, an elevated temperature increases the glutamic acid level in the cytoplasm associated with GAD activation through calmodulin, thereby enhancing the level of GABA. In durum wheat, accumulation of GABA under high-light treatment could also serve as an alternative source of nitrogen storage (Carillo 2018).

5.3  Drought Tolerance Drought is a major limiting factor for plant growth and development which constantly affects plant life and positively promotes GABA accumulation (Thompson et al. 1996; Filho et al. 2018; Table 1). The endogenous increase in GABA level

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enhancing through exogenous GABA supplementation improves GABA shunt and alleviates the water-deficient situation in white clover (Yong et al. 2017). Injuries cause an increase in GABA concentration, significantly reported in soybean, bean, sesame, and turnip when exposed to water shock conditions (Bor et al. 2009; Serraj et al. 1998; Raggi 1994). Exogenous application of GABA or increased its content in drought condition significantly delays senescence, overcome the drought-affected cell elongation, improves nitrogen recycling, and prevents photo-oxidation damage to photosystem II (Mekonnen et al. 2016). According to Guo et al. (2009), in barely GABA receptor gene expression was reported to be enhanced in drought-tolerant. In this context, barley flag leaf having SSADH was considered to be a metabolic quantitative trait locus (mQTL) (Templer et al. 2017). In drought tolerance, GABA can bind to membrane transporters channels such as aluminum-activated malate transporter (ALMT) that restrict anion influx or stimulate anion influx at the plasma membrane or tonoplast during the water-deficient condition (Lin et al. 2019). The level of GABA and physiological function of rice proline transporter are significantly varying in different tissues at several stages. For example, the activity of OsPROT1 and OsproT3 was reported higher in leaf sheath, nodes of reproductive tissue, leaf blades, root, nodes, and peduncles, respectively, in rice. The expression of ProT genes is affected by the abiotic stresses in barley, mungbean, and Arabidopsis (Lin et al. 2019). In black cumin, enhanced GABA content was suggested to directly increase the proline level, chlorophyll content, antioxidant enzymes, soluble sugars, and other osmoregulatory components under water-deficient conditions (Rezaei-­ Chiyaneh et al. 2018). Using Arabidopsis thaliana gad1/2 mutant study, the GABA content was observed to be least with distorted stomatal morphology as well as physiology (Mekonnen et al. 2016).

5.4  Chilling Stress Chilling stress is one of the most important limiting stresses which affects the early stage of germination, seedling growth, and fruit quality (Sharma et  al. 2020). According to Malekzadeh et al. (2013), GABA reduces electrolytic leakage, activities of antioxidant enzymes, malonaldehydes, and proline content under chilling stress, while decreases in proline content and higher sugar accumulation were detected in non-treated Lycopersicum esculentum plants. The results suggest that exogenous treatment of GABA improves chilling tolerance via maintaining membrane integrity and reducing MDA, catalase, and peroxidase-like antioxidant enzyme activity (Malekzadeh et  al. 2013). The exogenous GABA application enhances endogenous GABA level and alleviates its metabolism in anthurium cut flowers in response to postharvest chilling temperature (Aghdam et  al. 2016a, b; Soleimani et al. 2016). During cold storage, decreased levels of endogenous GABA or enhanced activity of GAD assists to accumulate glutamic acid in zucchini fruits (Palma et al. 2015). However, GABA and glutamic levels might be declined with supplementation of putrescine in control fruits. In contrast, GABA-T activity was perceived higher after

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14 days of putrescine treatment and probably increases the catabolization of glutamate and various metabolic subproducts to overcome chilling stress in zucchini. The above findings suggest that putrescine induction treatment modulates the GABA shunt during cold storage (Aghdam et al. 2016b). The role of GABA in chilling stress tolerance is explained in various crop plants including wheat, peach, barley, and tomato (Table 1).

6  Biotic Stress Tolerance In addition to variety of non-biological stresses, the biotic stresses also play prominent role in shaping the plant growth, development and productivity (Anamika et al. 2019; Mehta et al. 2020; Sharma et al. 2021; Yadav et al. 2021). Besides a functional role in abiotic stress tolerance, several studies were conducted on the application of GABA in controlling phytopathogens attack (Table 2). There are several modes of enhancing the endogenous GABA through an exogenous application that certainly affects the physiological, biochemical, and molecular machinery of crop plants (Table 3). Interestingly, the level of GABA accumulation in response to biotic entities was observed to be elevated in specific regions, for example, Arabidopsis infected with Fusarium graminearum and Solanum sp. Infected with potato virus Y, the tobacco leaves infiltrated with elicitor (hairpin-­like), lettuce inoculated in mold, Diaphorina citri, and Candidatus liberibactor asiatica can show enhanced cytosolic GABA accumulation in infected plants (Su et al. 2019; Tarkowski et al. 2019; Zaini et al. 2018; Chen et al. 2017; Kogovsek et al. 2016; O’Leary et al. 2016; Dimlioglu et al. 2015). GABA also plays a significant role in plant-pathogen interaction; for example, GABA biosynthesis and methionine cycle (MTC) regulate the expression of genes including GAD2, SSADH1, SAMS2, MS1, and SSHH1 respectively were used in virus-induced gene silencing in tomato. Moreover, silencing of GAD2, MS1, and SAHH1 leads to increased susceptibility to Ralstonia solanacearum. The results concluded that two GABA catabolic genes such as SSADH and GABT were upregulated after infection with R. solanacearum. The accumulation of GABA might regulate the communication during plant-­pathogen interaction and contrarily mediates inhibition of SSADH1 and GAD2 expression via VIGS which confirmed that SSADH1 silencing did not affect inoculation of R. solanacearum (Wang et al. 2019). In tomato mutants, infection of Botrytis cinerea compromising an initial biphasic defense as a localized hypersensitive response at the infection sites causes proper overactivation of GABA shunt. Similarly, before the infection in wild type auxiliary treatment of GABA delays susceptibility and shows similar variation as compared to mutants. Moreover, the infection of B. cinerea causes overactivation of GABA shunt and operated its mechanism in susceptible and wild type (Seifi et al. 2013). The potential role of GABA shunt also provides resistance against fungal pathogens; for instance, GABA concentration endogenously increases along with increasing infection of Colletotrichum fulvum in the tomato plant. In tobacco, petunia GAD overexpression leads to GABA biosynthesis which increases resistance to

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Fig. 3  Diagramatic illustration on GABA application in mitigating abiotic and biotic stress challenges

Meloidogyne hapla. However, pathogen invasion positively correlated with GABAinduced pathogen response that confirmed the role of GABA in suppressing the bacterial invasion and growth (Ramesh et  al. 2017; Park et  al. 2010). In another study, before inoculum induction, exogenous GABA was subjected to pears which provide resistance against fungal pathogens via elevating the production of peroxidases and catalase-like antioxidant enzymes and simultaneously induce cell death (Fu et al. 2017). Increased proline content and their biosynthesis are predominantly related to the expression of pro-­biosynthetic enzyme P5CS; therefore increasing the P5CS expression via a transgenic approach could significantly elevate the biotic stress tolerance in plants (Fig. 3).

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7  S  uccessful Example of GABA Application in Crop Plants as a Protectant Exogenous application of GABA in Solanum lycopersicum increases chlorophyll content and plant height and significantly reduced salt damage index when subjected to NaCl stress. In salinity stress, exogenous GABA decreased Na+ accumulation in roots and leaves by restricting Na+ movement from roots to leaves via regulating the expression of the SIGAD1-3 gene. SIGAD1 directly enhances the GAD activity which increased with high salinity and GABA application. However, GABA alleviates the GAD activity along with glutamate, proline, endogenous GABA accumulation, and eight other amino acids. Similarly, GABA reduces the malondialdehyde level and ROS activity as well as comparatively increases the antioxidant enzyme activity. The finding suggests the protective role of GABA under saline stress conditions (Wu et  al. 2020). Generally, GABA shunt coupled with nitrogen and carbon metabolism upon CdCl2 and NaCl stress (Jia et al. 2020). In white clover, the exogenous application of GABA helps to increase polyethylene glycol (PEG) induced drought resistance which positively regulates polyamines, proline metabolism, and ultimately GABA shunt (Yong et al. 2017). GABA also acts as a thermoprotectant and prevents thermal injuries to reproductive function during temperature stress in mungbean plants (Priya et al. 2019). The treatment of GABA increases tolerance to alkalinity-salinity stress by mediating counterbalance between chlorophyll biosynthesis and redox potential in muskmelon plants (Hu et al. 2015; Jin et al. 2019). Contrarily, GABA also mediates the accumulation of antioxidant system and phenolic compounds in germinated hulless barley during salinity stress (Ma et  al. 2019). In addition to these, stronger and rapid defense responses do not concomitantly initiate metabolically extensive defense mechanisms, the process is known as priming and over the past decade, GABA has been well known as a priming agent (Thevenet et al. 2017).

8  Concluding Remarks The exogenous application significantly enhances the endogenous GABA level and alleviates activities of antioxidant machinery including enzymes and stress-related proteins. The positive regulation of GABA shut and its associated pathways efficiently manage abiotic and biotic stress tolerance. In the past decade, GABA plays a significant role in the modulation of physiological processes; when plants are exposed to harsh environmental conditions changes in GABA concentration could be an efficient method in increasing stress resistance. It revealed that increased GABA content directly fine-tunes or alters the activities of antioxidant systems, signaling cascade, defense reactions, and related pathways. The chapter highlights summarize the information on the positive role of GABA in crop plants with the ability to withstand harsh environmental conditions. This comprehensive document

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about biosynthesis and its role in stress mitigations opens the discussion on GABA to be considered as an important tool to unresolved quantity and quality issues in agricultural applications. However, no significant reports on the tolerance or adaptation to GABA in fungi, insects, and other pathogens or likely to be poorly described.

References Aghdam MS, Naderi R, Jannatizadeh A, Babalar M, Sarcheshmeh MA, Faradonbe MZ (2016a) Impact of exogenous GABA treatments on endogenous GABA metabolism in anthurium cut flowers in response to postharvest chilling temperature. Plant Physiol Biochem 106:11–15 Aghdam MS, Naderi R, Malekzadeh P, Jannatizadeh A (2016b) Contribution of GABA shunt to chilling tolerance in anthurium cut flowers in response to postharvest salicylic acid treatment. Sci Hortic 205:90–96 Ahmad S, Chitkara P, Khan FN, Kishan A, Alok V, Ramlal A, Mehta S (2021) Mobile technology solution for COVID-19: surveillance and prevention. In: Computational intelligence methods in COVID-19: surveillance, prevention, prediction and diagnosis. Springer, Singapore, pp 79–108 Akcay N, Bor M, Karabudak T, Ozdemir F, Turkan I (2012) Contribution of Gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. J Plant Physiol 169:452–458 AL-Quraan NA (2015) GABA shunt deficiencies and accumulation of reactive oxygen species under UV treatments: insight from Arabidopsis thaliana calmodulin mutants. Acta Physiol Plant 37:86 Anamika, Mehta S, Singh B, Patra A, Islam MA (2019) Databases: a weapon from the arsenal of bioinformatics for plant abiotic stress research. In: Recent approaches in Omics for plant resilience to climate change. Springer, Cham, pp 135–169 Barilli E, Sillero JC, Rubiales D (2010) Induction of systemic acquired resistance in pea against rust (Uromyces pisi) by exogenous application of biotic and abiotic inducers. J Phytopathol 158:30–34 Benini S (2020) Structural and functional characterization of proteins from the fire blight pathogen Erwinia amylovora. A review on the state of the art. J Plant Pathol. https://doi.org/10.1007/ s42161-­020-­00682-­4 Bharti J, Sahil, Mehta S, Ahmad S, Singh B, Padhy AK, Srivastava N, Pandey V (2021) Mitogen-­ activated protein kinase, plants and heat stress. In: Harsh environment and plant resilience. Springer Nature, Switzerland AG, Cham, pp 324–355 Bhattacharya S, Khatri A, Swanger SA, DiRaddo JO, Yi F, Hansen KB (2018) Triheteromeric GluN1/GluN2A/GluN2C NMDARs with unique single-channel properties are the dominant receptor population in cerebellar granule cells. Neuron 99:315–328 Bor M, Seckin B, Ozgur R, YiLmaz O, Ozdemir F, Turkan I (2009) Comparative effects of drought, salt, heavy metal and heat stresses on gamma-aminobutyric acid levels of sesame (Sesamum indicum L.). Acta Physiol Plant 31:655–659 Carillo P (2018) GABA shunt in durum wheat. Front Plant Sci 9:100 Chen F, Liu C, Zhang J, Lei H, Li HP, Liao YC, Tang H (2017) Combined metabonomic and quantitative RT-PCR analyses revealed metabolic reprogramming associated with Fusarium graminearum resistance in transgenic Arabidopsis thaliana. Front Plant Sci 8:2177 Cheng B, Li Z, Liang L, Cao Y, Zeng W, Zhang X (2018) The gamma-aminobutyric acid (GABA) alleviates salt stress damage during seeds germination of white clover associated with Na?/K? transportation, dehydrins accumulation, and stress-related gene expression in white clover. Int J Mol Sci 19:2520

294

A. Kumar et al.

Che-Othman MH, Jacoby RP, Millar AH, Taylor NL (2020) Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytol 225:1166–1180 Chevrot R, Rosen R, Haudecoeur E, Cirou A, Shelp BJ, Ron E, Faure D (2006) GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 103:7460–7464 Chinnasri B, Sipes BS, Schmitt DP (2006) Effects of inducers of systemic acquired resistance on reproduction of Meloidogyne javanica and Rotylenchulus reniformis in pineapple. J Nematol 38:319–325 Choudhary A, Kumar A, Kaur N (2019) ROS and oxidative burst: Roots in plant development. Plant Diver 42:33–43 Choudhary A, Kumar A, Kaur A, Paul A (2020) Plasmodesmata the Nano Bridges in Plant Cell: Are the Answer for All the Developmental Processes?. Russ J Plant Physiol 67:785–796 Choudhary A, Kumar A, Kaur H, Kaur H (2021) MiRNA: the taskmaster of plant world. Biologia 76:1551–1567 Choy YK, Jennifer AH, Wei YW, Ee TL, Siaw SH (2020) Transcriptional sequencing and gene expression analysis of various genes in fruit development of three different black pepper (Piper nigrum L.) varieties. Int J Genomics 5:18 Cohen Y, Rubin AE, Vaknin M (2011) Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce. Eur J Plant Pathol 130:13–27 Dilawari R, Kaur N, Priyadarshi N, Kumar B, Abdelmotelb KF, Lal SK, Singh B, Tripathi A, Aggarwal SK, Jat BS, Mehta S (2021) Genome editing: a tool from vault of science for engineering climate resilient cereals. In: Harsh environment and plant resilience. Springer Nature, Switzerland AG, Cham, pp 45–72 Dimlioglu G, Das ZA, Bor M, Ozdemir F, Turkan I (2015) The impact of GABA in harpin-elicited biotic stress responses in Nicotiana tabaccum. J Plant Physiol 188:51–57 FAO (2020) COVID-19: our hungriest, most vulnerable communities face “a crisis within a crisis”. http://www.fao.org/news/story/en/item/1269721/icode Farooq M, Nawaz A, Chaudhry M, Indrasti R, Rehman A (2017) Improving resistance against terminal drought in bread wheat by exogenous application of proline and gamma-aminobutyric acid. J Agron Crop Sci 203:464–472 Filho EGA, Braga LN, Silva LMA, Miranda FR, Silva EO, Canuto KM, Miranda MR, de Brito ES, Zocolo GJ (2018) Physiological changes for drought resistance in different species of Phyllanthus. Sci Rep 8:15141 Fu D, Sun Y, Yu C, Zheng X, Yu T, Lu H (2017) Comparison of the effects of three types of aminobutyric acids on the control of Penicillium expansum infection in pear fruit. J Sci Food Agric 97:1497–1501 Gramazio P, Takayama M, Ezura H (2020) Challenges and prospects of new plant breeding techniques for GABA improvement in crops: tomato as an example. Front Plant Sci 11:1382 Guo P, Baum M, Grando S, Ceccarelli S, Bai G, Li R, von Korff M, Varshney RK, Graner A, Valkoun J (2009) Differentially expressed genes between drought-tolerant and drought-­ sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544 Hany GAD, Soumya M, Reham F, Ola HAE, Mohamed H, Ahmed AEY, Salama AAE, Nesreen H, Amr EK (2020) Exogenous γ-aminobutyric acid (GABA)-induced signaling events and field performance associated with mitigation of drought stress in Phaseolus vulgaris L. Plant Signal Behav 2:1853384 Harata K, Shinonaga H, Nishiyama Y, Okuno T (2021) CoGRIM19 is required for invasive hyphal growth of Colletotrichum orbiculare inside epidermal cells of cucumber cotyledons. Microb Pathog 154:104847 Hassan MAE, Buchenauer H (2007) Induction of resistance to fireblight in apple by acibenzolar-­ S-­methyl and DL-3-aminobutyric acid. J Plant Dis Protect 114:151–158

Plant Performance and Defensive Role of γ-Gamma Amino Butyric Acid…

295

Haudecoeur E, Planamente S, Cirou A, Tannieres M, Shelp BJ, Morera S, Faure D (2009) Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 106:14587–14592 Hodge S, Pope TW, Holaschke M, Powell G (2006) The effect of b-aminobutyric acid on the growth of herbivorous insects feeding on Brassicaceae. Ann Appl Biol 148:223–229 Hodge S, Ward JL, Galster AM, Beale MH, Powell G (2011) The effects of a plant defence priming compound, b-aminobutyric acid, on multitrophic interactions with an insect herbivore and ahymenopterous parasitoid. BioControl 56:699–711 Hu X, Xu Z, Xu W, Li J, Zhao N, Zhou Y (2015) Application of g-aminobutyric acid demonstrates a protective role of polyamine and GABA metabolism in muskmelon seedlings under Ca(NO3)2 stress. Plant Physiol Biochem 92:1e10 Jeun YC, Park EW, Kim CH, Fowler WD, Kloepperc JW (2004) Cytological observations of cucumber plants during induced resistance elicited by rhizobacteria. Biol Control 29:34–42 Ji J, Zheng L, Yue J, Yao X, Chang E, Xie T, Deng N, Chen L, Huang Y, Jiang Z, Shi S (2017) Identification of two CiGADs from Caragana intermedia and their transcriptional responses to abiotic stresses and exogenous abscisic acid. PeerJ 5:e3439 Jia Y, Zou D, Wang J, Sha H, Liu H, Inayat MA, Sun J, Zheng H, Xia N, Zhao H (2017) Effects of γ-aminobutyric acid, glutamic acid, and calcium chloride on rice (Oryza sativa L.) under cold stress during the early vegetative stage. J Plant Growth Regul 36:240–253 Jia J, Shi Z, Xie TT, Zhang XM, Chen W, Du CJ (2020) Responses of GABA shunt coupled with carbon and nitrogen metabolism in poplar under NaCl and CdCl2 stresses. Ecotoxicol Environ Saf 193:110322 Jin X, Liu T, Xu J, Gao Z, Hu X (2019) Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biol 19:48 Kaur S (2013) γ-Aminobutyric Acid (GABA) Imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul 33:408–419 Kelsey G (2020) Early stages of infection on seedlings by Peronospora Parasitica in agricultural. Acta Microsc 29:6 Khan MIR, Syed UJ, Priyanka C, Himanshu C, Antonio F, Nafees AK, Mohammad IA (2021) Role of GABA in plant growth, development and senescence. Plant Gene 58:100283 Kogovsek P, Pompe-Novak M, Petek M, Fragner L, Weckwerth W, Gruden K (2016) Primary metabolism, phenylpropanoids and antioxidant pathways are regulated in potato as a response to Potato virus Y infection. PLoS One 11:e0146135 Krishnan S, Laskowski K, Shukla V, Merewitz EB (2013) Mitigation of drought stress damage by exogenous application of a nonprotein amino Acid c–aminobutyric acid on perennial ryegrass. J Am Soc Hortic Sci 138:358–366 Kumar A, Sharma A, Sharma R, Srivastva P, Choudhary A (2021 ) Exploration of Wheat wild relative diversity from Lahaul Valley –a cold arid desert of Indian Himalayas. Cereal res commun, https://doi.org/10.1007/s42976-021-00166-w Kumari S, Kumar V (2020) Role of Gamma Amino Butyric Acid (GABA) against abiotic stress tolerance in legumes: a review. Plant Physiol Rep 25:654–663 Lal SK, Kumar S, Sheri V, Mehta S, Varakumar P, Ram B, Borphukan B, James D, Fartyal D, Reddy MK (2018) Seed priming: an emerging technology to impart abiotic stress tolerance in crop plants. In: Advances in seed priming. Springer, Singapore, pp 41–50 Li W, Liu J, Ashraf U, Li G, Li Y, Lu W, Hu J (2016) Exogenous γ-aminobutyric acid (GABA) application improved early growth, net photosynthesis, and associated physio-biochemical events in maize. Front Plant Sci 7:919 Li Z, Peng Y, Huang B (2018) Alteration of transcripts of stress-protective genes and transcriptional factors by γ-aminobutyric acid (GABA) associated with improved heat and drought tolerance in creeping bentgrass (Agrostis stolonifera). Int J Mol Sci 19:1623

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A. Kumar et al.

Li Z, Huang T, Tang M, Cheng B, Peng Y, Zhang X (2019) iTRAQ-based proteomics reveals key role of γ-aminobutyric acid (GABA) in regulating drought tolerance in perennial creeping bentgrass (Agrostis stolonifera). Plant Physiol Biochem 145:216–226 Li L, Dou N, Zhang H, Wu C (2021) The versatile GABA in plants. Plant Signal Behav 16:1862565 Lin JH, Xu ZJ, Jia SP, Jing Z, Zhang GB, Jun X, Yi ZX, Zhang JH, Gong JM, Ye NH, Shuan M (2019) OsProT1 and OsProT3 Function to mediate proline- and γ-aminobutyric acid-specific transport in yeast and are differentially expressed in rice (Oryza sativa L.). Rice (N Y) 12:79–89 Ma Y, Wang P, Wang M, Sun M, Gu Z, Yang R (2019) GABA mediates phenolic compounds accumulation and the antioxidant system enhancement in germinated hulless barley under NaCl stress. Food Chem 270:593–601 Mahmud J, Hasanuzzaman M, Nahar K (2017) γ-aminobutyric acid (GABA) confers chromium stress tolerance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology 26:675–690 Malekzadeh P, Khara J, Heidari R (2012) Effect of exogenous gamma-aminobutyric acid on physiological tolerance of wheat seedlings exposed to chilling stress. Iran J Plant Physiol 3:611–617 Malekzadeh P, Khara J, Heydari R (2013) Alleviating effects of exogenous gamma-aminobutyric acid on tomato seedling under chilling stress. Physiol Mol Biol Plants 20:133–137 Mehta S, James D, Reddy MK (2019a) Omics technologies for abiotic stress tolerance in plants: current status and prospects. In: Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 1–34 Mehta S, Singh B, Dhakate P, Rahman M, Islam MA (2019b) Rice, marker-assisted breeding, and disease resistance. In: Disease resistance in crop plants. Springer, Cham, pp 83–111 Mehta S, Lal SK, Sahu KP, Venkatapuram AK, Kumar M, Sheri V, Varakumar P, Vishwakarma C, Yadav R, Jameel MR, Ali M, Achary VMM, Reddy MK (2020) CRISPR/Cas9-Edited Rice: a new frontier for sustainable agriculture. In: New frontiers in stress management for durable agriculture. Springer, Singapore, pp 427–458 Mehta S, Singh B, Patra A, Tripathi A, Easwaran M, Choudhary JR, Choudhary M, Aggarwal SK (2020) Maize microbiome: current insights for the sustainable agriculture. In: Microbiomes and Plant Health. Academic Press, Massachusetts, pp 267–297 Mehta S, Gogna M, Singh B, Patra A, Singh IK, Singh A (2021) Silicon: a plant nutritional “non-­ entity” for mitigating abiotic stresses. In: Plant stress biology. Springer, Singapore, pp 17–49 Mekonnen DW, Flugge UI, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci 245:25–34 Nandeeshkumar P, Sarosh BR, Ramachandra Kini K, Prakash HS, Shekar Shetty H (2009) Elicitation of resistance and defense-related proteins by b-aminobutyric acid in sunflower against downy mildew pathogen Plasmopara halstedii. Arch Phytopathol Plant Protect 42:1020–1032 Nandini B, Hariprasad P, Prakash HS, Shetty HS, Geetha N (2017) Trichogenic-selenium nanoparticles enhance disease suppressive ability of Trichoderma against downy mildew disease caused by Sclerospora graminicola in pearl millet. Sci Rep 7:1–11 Nayyar H, Kaur R, Kaur S, Singh R (2014) c-Aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul 33:408–419 O’Leary BM, Neale HC, Geilfus CM, Jackson RW, Arnold DL, Preston GM (2016) Early changes in apoplast composition associated with defence and disease in interactions between Phaseolus vulgaris and the halo blight pathogen Pseudomonas syringae Pv. phaseolicola. Plant Cell Environ 39:2172–2184 Pajot E, Silue D (2005) Evidence that DL-3-aminobutyric acid and acibenzolar-S-methyl induce resistance against bacterial head rot disease of broccoli. Pest Manag Sci 61:1110–1114 Pal S, Zhao J, Khan A, Yadav NS, Batushansky A, Barak S, Rewald B, Fait A, Lazarovitch N, Rachmilevitch S (2016) Paclobutrazol induces tolerance in tomato to deficit irrigation through diversified effects on plant morphology, physiology and metabolism. Sci Rep 6:39321

Plant Performance and Defensive Role of γ-Gamma Amino Butyric Acid…

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Palma F, Carvajal F, Ramos JM, Jamilena M, Garrido D (2015) Effect of putrescine application on maintenance of zucchini fruit quality during cold storage: contribution of GABA shunt and other related nitrogen metabolites. Postharvest Biol Technol 99:131–140 Park DH, Mirabella R, Bronstein PA, Preston GM, Haring A, Lim CK, Collmer A, Schuurink RC (2010) Mutations in c-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J 64:318–330 Pelgrom AJ, Meisrimler CN, Elberse J, Koorman T, Boxem M, Van AG (2020) Host interactors of effector proteins of the lettuce downy mildew Bremia lactucae obtained by yeast two-hybrid screening. PLoS One 15:e0226540 Polyakovskii SA, Kravchuk ZN, Dmitriev AP (2008) Mechanism of action of the plant resistance inducer b-aminobutyric acid in Allium cepa. Cytol Genet 42:369–372 Priya M, Sharma L, Kaur R, Bindumadhava H, Nair RM, Siddique KHM (2019) GABA (c-­aminobutyric acid) as a thermo-protectant, to improve the reproductive function of heat-­ stressed mungbean plants. Sci Rep 9:1–14 Raggi V (1994) Changes in free amino acids and osmotic adjustment in leaves of water-stressed bean. Physiol Plant 91:427–434 Rahman M, Sultana S, Nath D, Kalita S, Chakravarty D, Mehta S, Wani SH, Islam MA (2019) Molecular breeding approaches for disease resistance in sugarcane. In: Disease resistance in crop plants. Springer, Cham, pp 131–155 Rajput LS, Aggarwal SK, Mehta S, Kumar S, Nataraj V, Shivakumar M, Maheshwari HS, Yadav S, Goswami D (2021) Role of WRKY transcription factor superfamily in plant disease management. In: Plant stress biology. Springer, Singapore, pp 335–361 Ramesh SA, Tyerman SD, Gilliham M, Xu B (2017) c-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74:1577–1603 Ramos RR, Martinez F, Knauf BG (2019) The effects of GABA in plants. Cogent Food Agric 5:1670553 Razik A, Alharbi ES, Pirzadah BM, Alnusairi TB, Soliman GSHM, Hakeem KR (2021) γ-Aminobutyric acid (GABA) mitigates drought and heat stress in sunflower (Helianthus annuus L.) by regulating its physiological, biochemical and molecular pathways. Physiol Plant. https://doi.org/10.1111/ppl.13216 Rezaei-Chiyaneh E, Seyyedi SM, Ebrahimian E, Moghaddam SS, Damalas CA (2018) Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind Crop Prod 112:741–748 Sahil, Keshan R, Patra A, Mehta S, Abdelmotelb KF, Lavale SA, Chaudhary M, Aggarwal SK, Chattopadhyay A (2021) Expression and regulation of stress-responsive genes in plants under harsh environmental conditions. In: Harsh environment and plant resilience. Springer Nature, Switzerland AG, Cham, pp 26–45 Salvatierra A, Pimentel P, Almada R, Hinrichsen P (2016) Exogenous GABA application transiently improves the tolerance to root hypoxia on a sensitive genotype of Prunus rootstock. Environ Exp Bot 125:52–66 Seifi HS, Curvers K, De Vleesschauwer D, Delaere I, Aziz A, Hofte M (2013) Concurrent overactivation of the cytosolic glutamine synthetase and the GABA shunt in the ABA-deficient sitiens mutant of tomato leads to resistance against Botrytis cinerea. New Phytol 199:490–504 Seifikalhor M, Aliniaeifard S, Hassani B (2019) Diverse role of γ-aminobutyric acid in dynamic plant cell responses. Plant Cell Rep 38:847–867 Seifikalhor M, Aliniaeifard S, Bernard F (2020) γ-Aminobutyric acid confers cadmium tolerance in maize plants by concerted regulation of polyamine metabolism and antioxidant defense systems. Sci Rep 10:3356 Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of γ-aminobutyric acid in nodulated soybean in response to drought stress. Physiol Plant 102:79–86 Sharma P, Sharma MMM, Malik A, Vashisth M, Singh D, Kumar R, Singh B, Patra A, Mehta S, Pandey V (2021) Rhizosphere, Rhizosphere Biology, and Rhizospheric Engineering. In: Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management. Springer, Cham, pp 577–624

298

A. Kumar et al.

Shailasree S, Sarosh BR, Vasanthi NS, Shetty HS (2001) Seed treatment with b-aminobutyric acid protects Pennisetum glaucum systemically from Sclerospora graminicola. Pest Manag Sci 57:721–728 Shang H, Cao S, Yang Z, Cai Y, Zheng Y (2011) Effect of exogenous c-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. J Agric Food Chem 59:1264–1268 Sharma P, Sharma MM, Patra A, Vashisth M, Mehta S, Singh B, Tiwari M, Pandey V (2020) The role of key transcription factors for cold tolerance in plants. In: Transcription factors for abiotic stress tolerance in plants. Academic, Cambridge, pp 123–152 Shelp BJ, Bown AW, Zarei A (2017) 4-Aminobutyrate (GABA): a metabolite and signal with practical significance. Botany 95:1015–1032 Sheteiwy MS, Shao H, Qi W, Hamoud YA, Shaghaleh H, Khan NU, Yang R, Tang B (2019) GABA-Alleviated oxidative injury induced by salinity, osmotic stress and their combination by regulating cellular and molecular signals in rice. Int J Mol Sci 20:5709 Shi SQ, Shi Z, Jiang ZP, Qi LW, Sun XM, Li CX, Liu JF, Xiao WF, Zhang SG (2010) Effects of exogenous GABA on gene expression of Caragana intermedia roots under NaCl stress: regulatory roles for H2O2 and ethylene production. Plant Cell Environ 33:149–162 Silue D, Pajot E, Cohen Y (2002) Induction of resistance to downy mildew (Peronospora parasitica) in cauliflower by DL-b-aminon-butanoic acid (BABA). Plant Pathol 51:97–102 Singh A, Roychoudhury A (2020) Role of γ-aminobutyric acid in the mitigation of abiotic stress in plants. In: Protective chemical agents in the amelioration of plant abiotic stress: biochemical and molecular perspectives. Wiley, pp 413–423 Singh B, Mehta S, Aggarwal SK, Tiwari M, Bhuyan SI, Bhatia S, Islam MA (2019) Barley, disease resistance, and molecular breeding approaches. In: Disease resistance in crop plants. Springer, Cham, pp 261–299 Sita K, Kumar V (2020) Role of Gamma Amino Butyric Acid (GABA) against abiotic stress tolerance in legumes: a review. Plant Physiol Rep 25:654–663 Soleimani AM, Naderi R, Malekzadeh P, Jannatizadeh A (2016) Contribution of GABA shunt to chilling tolerance in anthurium cut flowers in response to postharvest salicylic acid treatment. Sci Hortic 205:90–96 Song H, Wang XX, Wang H, Taoa YH (2010) Exogenous c-aminobutyric acid alleviates oxidative damage caused by aluminium and proton stresses on barley seedlings. J Sci Food Agric 90:1410–1416 Su N, Wu Q, Chen J, Shabala L, Mithofer A, Wang H, Qu M, Yu M, Cui J, Shabala S (2019) GABA operates upstream of H+-ATPase and improves salinity tolerance in Arabidopsis by enabling cytosolic K+ retention and Na+ exclusion. J Exp Bot 70:6349–6361 Takeuchi K (2018) GABA, a primary metabolite controlled by the Gac/Rsm regulatory pathway, favors a planktonic over a biofilm lifestyle in Pseudomonas protegens CHA0. Mol Plant Microbe Interact 31:274–282 Tarkowski ŁP, Van de Poel B, Hofte M, Van den EW (2019) Sweet immunity: inulin boosts resistance of lettuce (Lactuca sativa) against grey mold (Botrytis cinerea) in an ethylene-dependent manner. Int J Mol Sci 20:1052 Templer SE, Ammon A, Pscheidt D, Ciobotea O, Schuy C, McCollum C, Sonnewald U, Hanemann A, Forster J, Ordon F (2017) Metabolite profiling of barley flag leaves under drought and combined heat and drought stress reveals metabolic QTLs for metabolites associated with antioxidant defense. J Exp Bot 68:1697–1713 Thevenet D, Pastor V, Baccelli I, Balmer A, Vallat A, Neier R, Glauser G, Mauch-Mani B (2017) The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol 213:552–559 Thompson JF, Stewart CR, Morris CJ (1996) Changes in amino acid content of excised leaves during incubation I. The effect of water content of leaves and atmospheric oxygen level. Plant Physiol 41:1578–1584

Plant Performance and Defensive Role of γ-Gamma Amino Butyric Acid…

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Tian XL, Wu XL, Li Y, Zhang SQ (2005) The effect of gamma-aminobutyric acid in superoxide dismutase, peroxidase and catalase activity response to salt stress in maize seedling. Acta Biol Exp Sin 38:75–79 UN (2019) The sustainable development goals report. https://unstats.un.org/sdgs/report/2019/The-­ Sustainable-­Development-­Goals-­Report-­2019.pdf Vijayakumari K, Puthur JT (2016) c-Aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Regul 78:57–67 Viswanath KK, Varakumar P, Pamuru RR, Basha SJ, Mehta S, Rao AD (2020) Plant lipoxygenases and their role in plant physiology. J Plant Biol 63:83–95 Wang Y, Luo Z, Huang X, Yang K, Gao S, Du R (2014) Effect of exogenous γ-aminobutyric acid (GABA) treatment on chilling injury and antioxidant capacity in banana peel. Sci Hortic 168:132–137 Wang Y, Gu W, Meng Y, Xie T, Li L, Li J, Wei S (2017) γ-Aminobutyric acid imparts partial protection from salt stress injury to maize seedlings by improving photosynthesis and upregulating osmoprotectants and antioxidants. Sci Rep 7:43609 Wang G, Kong J, Dandan C, Hongbo Z, Yu N, Mengyun X, Gaofei J, Yahua Z, Wenyi W (2019) Resistance against Ralstonia solanacearum in tomato depends on the methionine cycle and the c-aminobutyric acid metabolic pathway. Plant J 97:1032–1047 Worldwide Global Nutrition Report (2020). https://globalnutritionreport.org/reports/ global-­nutrition-­report-­2020 Wu X, Jia Q, Ji S, Gong B, Li J, Lu G, Gao H (2020) Gamma-aminobutyric acid (GABA) alleviates salt damage in tomato by modulating Na (+) uptake, the GAD gene, amino acid synthesis and reactive oxygen species metabolism. BMC Plant Biol 20:465 Yadav S, Rathee M (2020) Sucking pests of rapeseed-mustard. In: Sucking pests of crops. Springer, Singapore, pp 187–232 Yadav B, Jogawat A, Lal SK, Lakra N, Mehta S, Shabek N, Narayan OP (2021) Plant mineral transport systems and the potential for crop improvement. Planta 253:45 Yo M, Allen GG (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol 49:92–102 Yong B, Xie H, Li Z, Li YP, Zhang Y, Nie G, Zhang XQ, Ma X, Huang LK, Yan YH, Peng Y (2017) Exogenous application of GABA improves peg-induced drought tolerance positively ­associated with GABA-shunt, polyamines, and proline metabolism in white clover. Front Physiol 8:1107–1115 Zaini PA, Nascimento R, Gouran H, Cantu D, Chakraborty S, Phu M, Goulart LR, Dandekar AM (2018) Molecular profiling of Pierce’s disease outlines the response circuitry of Vitis vinifera to Xylella fastidiosa infection. Front Plant Sci 9:771 Zhang S, Schisler DA, Boehm MJ, Slininger PJ (2007) Utilization of chemical inducers of resistance and Cryptococcus flavescens OH 182.9 to reduce Fusarium head blight under greenhouse conditions. Biol Control 42:308–315 Zhang J, Zhang Y, Du Y, Chen S, Tang H (2011) Dynamic metabolomics responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10:1904–1914 Zhang X, Lin HM, Hu H, Hu X, Hu L (2016) Gamma-aminobutyric acid mediates nicotine biosynthesis in tobacco under flooding stress. Plant Divers 38:53–58 Zhu X, Liao J, Xia X, Xiong F, Li Y, Shen J, Wen B, Ma Y, Wang Y, Fang W (2019) Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature. BMC Plant Biol 19:43 Zifeng G, Wenjun X, Umair A, Yuzhan L, Lin M, Runfei G, Shenggang P, Hua T, Meiyang D, Shuli W, Xiangru T, Zhaowen M (2020) Exogenous γ-aminobutyric acid (GABA) application at different growth stages regulates 2-acetyl-1-pyrroline, yield, quality and antioxidant attributes in fragrant rice. J Plant Interact 15:139–152

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress Pankaj Pandey, Asha Devi Pallujam, S. Leelavathi, Sahil Mehta, Manesh Chander Dagla, Bharat Bhushan, and S. K. Aggarwal

Abbreviations GSH Glutathione GSNO S-Nitroglutathione GSNOR S-Nitroglutathione reductase NO Nitric oxide NR Nitrate reductase PTM Post-translational modification RNS Reactive nitrogen species ROS Reactive oxygen species SNO S-Nitrosothiol SNP Sodium nitroprusside Thr Threonine Trx Thioredoxin

1  Introduction Nitric oxide (NO) is a small gaseous, highly reactive molecule that takes part in the signaling of various biological processes. The presence of NO in plants was first described by Klepper (1979) in herbicide-treated soybean plants but its role in the physiological process was discovered later in the late 1990s (Leshem and Kuiper P. Pandey (*) · S. Leelavathi Plant Transformation Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India A. D. Pallujam Department of Biotechnology, Manipur University, Canchipur, Imphal, India S. Mehta Crop Improvement Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India M. C. Dagla · B. Bhushan · S. K. Aggarwal ICAR-Indian Institute of Maize Research, Ludhiana, Punjab, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_12

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1996; Miller et al. 1996; Delledonne et al. 1998). Since the discovery of NO role in the stress responses and growth of the plant in the last two decades, it has been well established as a signaling molecule that affects a wide aspect of plant physiology like seed germination (Astier et al. 2018), root formation (Kushwaha et al. 2019; Prakash et al. 2020), flower induction (Zhang et al., 2019b), fruit ripening (Palma et al. 2019; González-Gordo et al. 2019), stomata closure (Wang et al. 2015), pollen tube growth (Wong et al. 2020), and adaptation-related signaling in case of environmental stresses (Zhou et al. 2016; Jain et al. 2018; Prakash et al. 2019). NO contains a single free electron in its orbit and depending on its cellular environment it can exist as nitric oxide (•NO), nitrosonium ion (NO+), and nitroyl ion (NO−) (Hancock and Neill 2019). NO reacts with many redox-related molecules to produce secondary reactive species like, it reacts with superoxide anion to generate peroxynitrite (ONOO−), GHS to produce S-nitroglutathione (GSNO), H2O2, H2S, ascorbate (ASC) (Hancock and Neill 2019). In the cell compartment, the concentration of secondary reactive species and NO local concentration along with the redox state of immediate vicinity regulate the NO signaling process (Brouquisse 2019). All these factors in combination make the study of NO signaling pathways a challenging task. Another challenge in the study is technical difficulties in the measurement of exact NO concentration; even with recent advance in measurements and localization techniques, the precise estimation of NO is still not possible (Vishwakarma et al. 2019). As a result, most of the studies related to the estimation of NO concentration are actually indirect ones as they are based on the determination of nitration of proteins, fat, and other biomolecules in a cell (Vishwakarma et al. 2019). NO-dependent post-translation modifications (PTM) of proteins are the most studied and common method of NO signaling. Out of all, S-nitrosation is the most common modification in which reversible addition of nitro group to thiol of cysteine regulates various cellular and stress tolerance-related processes (Begara-Morales et al. 2019; Zhang and Liao 2019). S-nitrosation of GSH produces S-nitrosothiol (GSNO) that functions as NO reservoir and participates in S-nitrosation through trans-nitration reaction (Astier and Lindermayr 2012; Heinrich et al. 2013; Jahnová et al. 2019; Chen et al. 2020). The process of nitration in tyrosine is facilitated by ONOO− along with other pathways is second PTM catalyzed by NO. Nitric oxide can react with most of the transition metals in ionized state and form a metal-­nitrosyl complex (M-NO). Both tyrosine nitration and metal-nitrosyl complex take part in numerous basal physiological and stress-related functions (Astier et  al. 2018). It was also reported that in the cellular environment, NO can react with other biomolecules such as fatty acids, DNA, and RNA; however, its regulatory role is still under investigation (Arasimowicz-Jelonek and Floryszak-Wieczorek 2019). Apart from these regulatory roles of NO, it can generate nitrosative stresses and be toxic to cells at higher concentration; hence, the role of nitric oxide depends on its concentration and location in the cell (Brouquisse 2019). Therefore, the light on recent findings related to nitric oxide production, basic mechanism of NO action, and its function in plant acclimatization in abiotic and biotic stresses will be imparted in the upcoming sections.

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2  Production of Nitric Oxide At present, NO signaling and regulation can be divided between two areas of research where the first one deals with its production and removal from cells. On the other hand, the second one solely deals with studying the signaling mechanism. With the findings of NO as a key facilitator in plant physiology and stress responses, several studies have been proposed for the source of NO in plants. However, the mechanisms underlying NO production in plants are still not fully uncovered and hence remains one of the demanding issues in the field (Astier et al. 2018). The key mechanisms for the synthesis of NO in plants rely on two major routes via reduction of nitrites through enzymatic and nonenzymatic reaction together with the oxidation of animated molecules through nitric oxide synthase (NOS) enzyme similar to the main pathway in mammals (Fig.  1a) (Astier et  al. 2018). Moreover, the production is also believed to enhance by the nitrate-reducing activity that depends on mitochondria (Modolo et al. 2005; Wendehenne et al. 2004; Astier et  al. 2018). Besides, Tun et  al. (2006) suggested the phenomenon of NO biosynthesis from polyamines (PA) in Arabidopsis thaliana (Tun et al. 2006). Nitrate reductase (NR), a crucial enzyme for nitrogen assimilation, can produce NO in plants that have increased attention in the past few years. Several papers have reviewed the production of NO catalyzed by NR through nitrate reduction to nitrite utilizing NAD(P)H as an electron donor (Besson-Bard et  al. 2008; Astier et  al. 2018). Furthermore, this enzyme has been shown to involve in the reduction of nitrite to NO through nitrite: NO reductase activity particularly in roots (Besson-­ Bard et al. 2008). Although, the later reaction constitutes only 1% of its reducing capacity of nitrate in normal condition (Małolepsza 2009) and it appears to exhibit under certain conditions such as acidic environment, low oxygen concentration, high accumulation of nitrite. and plant-pathogen interactions (Thu et  al. 2017). Various studies have shown the involvement of NR to generate NO during the stomatal closure, flowering, and nitrogen-fixing nodules (Hancock 2012). Researchers have shown the involvement of NR in the production of NO through biochemical and genetic approaches. Modolo et al. (2005) investigated NO production in A. thaliana plants with defective NR structural genes (NIA1 and NIA2) showed equivalent production with the wild-type plant in the presence of nitrite (Modolo et al. 2005). Another study demonstrated the inhibition of abscisic acid (ABA) to induce NO generation and stomatal closure when provided with A. thaliana nia1, nia2 defective NR mutant which proved that NR-mediated NO production is a key step in ABA signaling in guard cells (Besson-Bard et  al. 2008). Hancock has reviewed several works on the importance of NR in producing NO and the involvement of both the isoforms with perhaps NR1 significantly more important than NR2 in some cases (Hancock 2012). The production of NO in animals is primarily achieved through the enzymatic activity of nitric oxide synthases (NOS), a group of isoenzymes mainly found in the cytosol or in a membrane-bound form that convert NO and l-citrulline from l-­ arginine (Del Castello et  al. 2019; Wendehenne et  al. 2004). Many kinds of the

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Fig. 1 (a) Graphical representation of various nitric oxide (NO) production pathways. (b) S-nitrosation formation and regulation pathway

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literature suggested that plants also appear to possess NOS activity to generate NO using NADPH and O2 with Ca2+/calmodulin that is different from nitrite-based reduction in the absence of oxygen (Małolepsza 2009). Based on many pharmacological and immunological evidence, it is demonstrated that NOS-like activity is one of the major origins of NO. NOS-derived NO generation is inhibited by chemical analogs of l-arginine, i.e., L-NAME (N (G)-nitro-l-arginine methyl ester). However, there is no evidence of what precisely such inhibitors are playing in higher plants (Hancock 2012; Małolepsza 2009), and no typical plant proteins can be identified that corresponds to the antibodies against mammalian NOS (Wendehenne et al. 2004). In 2010, Foresi et al. identified a NOS-like enzyme from Ostreococcus tauri, a green alga belonging to the plant kingdom. They showed the sequence alignment of O. tauri (OtNOS) with human eNOS (epithelial NOS), iNOS (inducible NOS), and nNOS (neuronal NOS) in which the sequence similarity for eNOS, iNOS, and nNOS are 41.6, 42.7, and 34.3%, respectively (Foresi et  al. 2010). It indicates that the OtNOS activity is dependent on the stages of culture growth in which the exponential growth phase showed optimal activity of the enzyme and also demonstrated its importance in response to photoinhibition intensities of light (Del Castello et al. 2019; Foresi et al. 2010). In another work, expression of OtNOS in A. thaliana resulted in higher levels of NO production compared to siblings with empty vector and was shown to enhance germination rates, root and shoot development under salinity stress, and increased in drought and oxidative stress-tolerant (Foresi et al. 2015). To confirm the existence of NOS in photosynthetic organisms, Jeandroz et al. (2016) investigated the datasets of more than 1000 species of higher plants and algae. No typical NOS homologs were identified in 1087 transcriptomes of land plants; however, they identified 15 NOS-like sequences out of 265 algal species (Jeandroz et  al. 2016). Nejamkin et al. (2020) have recently reported the expression of OtNOS under the control of constitutive 35S (cloned in plasmid pCHF3) in tobacco plants. Transgenic tobacco plants showed higher accumulation and effective production of NO between 25% and 30% in root cells and demonstrated faster growth (Nejamkin et al. 2020). These studies would strengthen further research in understanding the molecular mechanisms by which the NOS enzymes play in higher plants. NO removal action performs mainly by phytoglobins (hemoglobins) through their NO dioxygenase activity (Hill et al. 2016). By modulation of NO concentration phytoglobins also function as a regulator of physiological processes. Studies have reported its regulatory role in the development of embryo, plant’s immunity (Mur et al. 2013; Stasolla et al. 2019), and root nodule formation (Berger et al. 2019).

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3  Mechanism of Nitric Oxide Action 3.1  S-Nitrosation S-Nitrosation is a reversible covalent addition  of nitroso (-N=O) group to Sulfur (S-H) of a specific cysteine residue in protein that leads to formation of S-nitrosothiol (SNO) (Umbreen et al. 2019). S-Nitrosation is redox-driven spontaneous process not mediated by an enzyme; not all cysteine residues undergo the S-nitrosation, only specific residues that show low pKa are susceptible of S-nitrosation modification (Begara-Morales et al. 2016; Umbreen et al. 2019). This modification is shown to regulate protein structure in an allosteric fashion, thus modulating protein activity, localization, and stability (Kim et al. 2002; Begara-Morales et al. 2019). S-Nitrosation involves in regulation of many physiological and biochemical metabolism-related activities required for plant function. Recently, Chen Qiu et al. (2019) have identified 191 S-nitrosated proteins located in various subcellular compartments mainly chloroplast and cytosol in tea (Camellia sinensis L.). Identified proteins involve in various metabolic pathways such as the Calvin cycle, TCA cycle, pyruvate metabolism, and glycolysis. 80 S-nitrosated protein is identified in potato tuber and leaf by Kato et al. (2013). Matamoros et al. (2020) showed protein nitrosation level regulates plant growth, nodulation, and flowering time in Lotus japonica plants. Niu et al. (2019) have showed adventitious root formation is enhanced by the application of exogenous GSNO that enhanced the level of nitrosation and inhibited by the use of NO scavengers. In 2019, Gong and Shi showed 334 endogenously S-nitrosated proteins in a tomato plant and involved in ethylene, MAPK, and Ca2+ signaling, reactive oxygen species (ROS) scavenging, and osmotic regulations. Program cell death (PCD) is induced by senescence, self-incompatibility, in response to metal stress, heat stress, and is regulated by ROS and RNS signaling via S-nitrosation (Jahnová et  al. 2019).  More recently, Ageeva-kieferle et  al.  (2021) have showed NO  modulates histone actylation via HDA6, thus coordinated  gene expression of downstreem stress releted genes. All these studies have shown that S-nitrosation participates in the basal physiological metabolism of plants. The S-nitrosation level increase in plants under stress condition and many studies have shown its role in modulation of plant response in stress conditions (Begara-Morales et al. 2019). Table 1 highlights various identified S-nitrosated proteins and their role in plants.

3.2  Tyrosine Nitration Tyrosine nitration is oxidative post  transcriptional  modification that involves the addition of -NO2 (nitro group) on protein tyrosine residues to form 3-nitrotyrosine (Ferrer-Sueta et al. 2018). The main mechanism proposed for tyrosine nitration is mediated by the formation of tyrosyl radicals and peroxynitrite ion (ONOO−),

NADPH oxidase

APX

APX 1 Glutamine synthetase, GS CaRboh/NADPH oxidase (NOX) GAPDH, TUA, GR

Aldehyde dehydrogenase, ALDH3 NADPH oxidase, NOX

12

13 14 15 16

17 18

Proteins Metacaspase ATMC9 Transcription factor NPR1 Pyruvate dehydrogenase Phosphoinositide-dependent kinase 1 Phosphoenolpyruvate carboxylase Zinc finger transcription factor, SRG1, CBC fructose-1,6-bisphosphatase (fbpase), cfbp1 Monodehydroascorbate reductase SUMO E2 enzyme, SCE1 Peroxisomal catalase

11

8 9 10

S. no. 1 2 3 4 5 6 7

Zinc (Zn) stress Nitrogen metabolic Ripening stages Adventitious root development Redox related Chromium (Cr) stress

Redox related

Redox related

Salt stress Biotic stress/SUMOylation Fruit ripening

Functions Protein cleavage Signaling-plant immunity Cellular sugar metabolism Cell death Salt stress Immunity Calvin-Benson cycle

Inhibition Inhibition

Inhibition Inhibition Inhibition Inhibition

Inhibition

Activation

Inhibition Inhibited Activation

Activation/ inhibition Inhibited Inhibited Inactivation Inhibition Activation Activation Inhibition

A. thaliana Zea mays

Solanum lycopersicum Solanum lycopersicum A. thaliana Medicago truncatula Capsicum annuum Cucumis sativus

Helianthus annuus A. thaliana Capsicum annuum

Plant sp. A. thaliana A. thaliana A. thaliana S. lycopersicum Sorghum bicolor A. thaliana P. sativum

Table 1  Example of S-nitrosated proteins identified in plants, their function, and effect of nitration on its activity

Stiti et al. (2020) Kharbech et al. (2020)

Kolbert et al. (2019) Silva et al. (2019) Chu-Puga et al. (2019) Niu et al. (2019)

Jedelská et al. (2019)

Jain et al. (2018) Skelly et al. (2019) Rodríguez-Ruiz et al. (2019) Jedelská et al. (2019)

References Belenghi et al. (2007) Tada et al. (2008) Zhang et al. (2017) Liu et al. (2017) Baena et al. (2017) Cui et al. (2018) Serrato et al. (2018)

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formed by a reaction between nitrogen monoxide (NO.) and superoxide (O2.−). Apart from peroxynitrite, some other mechanism for 3-nitrotyrosine formation is also proposed; most prominent is by the formation of nitrogen dioxide (.NO2). In vivo nitrogen dioxide (.NO2) is proposed to be formed by the action of heme peroxidase/hydrogen peroxide (H2O2) and/or action of transition metal action center (Radi 2004; Bartesaghi and Radi 2018). Many reports published have shown that Tyrosine nitration takes place at a basic physiological state and enhanced with conditions that increase the level of production of ROS and RNS, such as stress conditions (Feigl et al. 2020). Protein tyrosine nitration affects the protein function possibly through structural change; modified structure may change its activity by either loss- or gain-­ of-­function, may interfere in tyrosine-kinase-dependent pathways, and may cause restriction of protein assembly and polymerization, facilitation of protein degradation (turnover), and participation in the creation of proteasome-resistant protein aggregates (Castro et al. 2011; Kolbert et al. 2017). Table 2 highlights various identified proteins that undergo tyrosine nitration in plants.

Table 2  Example of proteins undergoes tyrosine nitration, its function, and effect of nitration S. no. Proteins 1 S-adenosyl homocysteine hydrolase (SAHH) 2 NADH-dependent hydroxypyruvate reductase 3 Hydroxypyruvate reductase (HPR1) 4 Glutathione reductase 5

Ascorbate peroxidase

6

Leghemoglobin (Lb)

7

MSD1, FSD3

8

PR-1; PR-3; PR-5

9 10

PsbO1, PsbO2, and PsbP1 Cytosolic peroxidase

11

NADP-malic enzyme

12

PYL5 receptor

Functions Metabolism

Activation/ inhibition Inhibition

Plant sp. Helianthus annuus

References Chaki et al. (2009) Corpas and Barroso (2013)

Glyoxylate metabolism

Inhibition

A. thaliana

Metabolism

Inhibition

P. sativum

Stress related

Inhibition

Oxidative stress Nitrosative stress Oxidative stress Immunity-­ related proteins Nitrosative stress Salt stress

Inhibition Inhibition Inhibition Inhibition Inhibition Activation

Low Inhibition temperature ABA signaling Inhibition

Corpas and Barroso (2013) P. sativum Begara-Morales et al. (2015) P. sativum Begara-Morales et al. (2015) Glycine max Sainz et al. (2015) A. thaliana Holzmeister et al. (2015) N. tabacum Takahashi et al. (2016) A. thaliana Takahashi et al. (2017) H. annuus Jain et al. (2018) A. thaliana Begara-Morales et al. (2019) A. thaliana Shukla et al. (2019)

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3.3  Metal Nitrosylation The nitric oxide radical has a free electron that it can donate to a transition metal. NO forms metal-nitrosyl complex with metal-containing proteins. Many proteins have been identified with which NO interacts like iron (Fe) containing Hemoglobin (Hb) lipogenase, aconite catalase in cytosol and mitochondria, ascorbate peroxidase and cytochrome c oxidase (COX) are few examples (Nelson 1987; Clark et al. 2000; Besson-Bard et al. 2008). NO preferentially interacts with iron ion in hemoglobin. Three types of hemoglobins are found in plants and categorized as leghemoglobin (Lb) found in nitrogen-­ fixing root nodules, non-symbiotic Hb classified as class 1 and class 2 with a high and low affinity for oxygen, respectively, and truncated Hb (Dordas et al. 2004). In root nodules, Lb transports oxygen to bacteroid as OxyLb (LbFeIIO2) (Mathieu et al. 1998). Studies have reported the presence of NO nitrosyl-Lb complex (LbFeIINO) in the functional root nodule of alfalfa, cowpea, and soybean (Mathieu et al. 1998). Other forms of Lb, oxyLb, and ferrylLb (LbFeIV) have been shown to interact with NO/ONOO− (Herold and Puppo 2005). These results have suggested that NO scavenging role of Lb is to protect nodules from nitrosative stress. Outside root nodules, class 1 Hb helps in the conversion of NO to nitrate with help of NAD(P)H (Perazzolli et al. 2004). Perazzolli et al. (2004) also demonstrated the overexpression of class 1 Hb in transgenic plants that help intolerance of hypoxia and fighting against an avirulent pathogen. These studies indicate that class-1 Hb plays an important role to protect plants from the deleterious effect of nitrosative stress.

4  Role of Nitric Oxide in Plant Stress Agricultural yield depends upon crop plants and their interaction with environmental factors (Mehta et al. 2020; Sharma et al. 2021; Singh et al. 2018). Adverse environmental conditions are the major contributor to yield loss in crop plants (Singh et al. 2019; Anamika et al. 2019). About 50% of yield loss occurs due to abiotic stress (Boyer 1982; Lal et al. 2018; Zhang and Liao 2019). Plants have adopted various mechanisms to protect themselves against stress (Viswanath et al. 2020; Sahil et al. 2021; Bharti et al. 2021). Common strategies adopted by plants to avoid or tolerate abiotic stresses include increased reactive oxygen scavenging activity, reduction in photosynthesis, stomatal closure, decreased in leaf growth, and enhanced root elongation (Maiti and Satya 2014). These plant responses are controlled by several important genes that encode transcription inducers and repressors that regulate downstream stress-induced genes along with metabolism pathways and signaling (Dilawari et al. 2021; Rajput et al. 2021; Sharma et al. 2020). The gain of knowledge about how plants sense stress and acclimatize to stress conditions will be beneficial for understanding plant physiology and to develop new crop varieties with enhanced tolerance to stress (Yadav et al. 2021; Mehta et al. 2019a). Stress in

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plants enhances the level of RNS and ROS and the high level of RNS is used as a marker for plant stress (Hancock and Veal 2021). In recent years, the role of NO in stress-related signaling is in much focus. Several studies have shown the role of NO signaling in all kinds of stress that plant encounters including drought (Santisree et al. 2015; Begara-Morales et al. 2019), salinity (Begara-Morales et  al. 2015; Zhou et  al. 2016; Nabi et  al. 2019), heat (Parankusam et  al. 2017), metal toxicity (Ortega-­Galisteo et  al. 2012; Wei et  al. 2020), cold (Airaki et al. 2012; Kubienová et al. 2014; Lv et al. 2018), and pathogen (Feechan et al. 2005; Chaki et al. 2009; Janus et al. 2013; Ding et al. 2020). In the next part, we will provide the role and description of NO signaling in various stress conditions. Furthermore, Fig.  2 depicts the nitric oxide action pathway and its impact on plants.

4.1  Drought Drought along with salinity is the most common environmental stress plants come across. Depending on the severity, drought stress could seriously hinder plant growth and productivity (Zhang et al. 2007). Along with global climate change and the need for water-saving in agricultural activity, there is an urgent need for identification of factors involved in plant response against stress and using this knowledge to develop different crop varieties that are tolerant to stress (Mehta et al. 2020; Mehta et al. 2021). To cope with drought stress, plants have evolved various strategies at structural, physiological, as well as gene expression levels (Zhu 2002; Shinozaki et al. 2003; Bohnert et al. 2006; Husen 2010; Husen et al. 2014, 2016, 2017; Zhao et al. 2010; Getnet et al. 2015; Embiale et al. 2016; Begara-Morales et al. 2019). Plant initial response against stress is a reduction in transpiration and increasing water uptake (Stanton and Mickelbart 2014). Plants reduce transpiration loss through the closing of stomatal aperture and reducing the density of stomata (Yu et al. 2013). Stomatal aperture regulation is controlled by various factors like NO, ROX, Ca2+ ion concertation, and ABA (Desikan et al. 2004; Yu et al. 2013; Zhang et al. 2019a). Both NO and H2O2 are essential for ABA-induced stomatal closure; on application of external NO it induces stomatal closure and this effect requires the cGMP and cyclic ADP Rib (cADPR) (Neill et  al. 2002). However, Wang et  al. (2015) have reported that at higher concentration NO induces stomatal opening by S-nitrosation of open stomata 1 (OST1) protein kinases. Thus, the complete mechanism of stomatal movement regulation by NO is not completely identified. Drought stress enhances ROS level that can impair the functions of plant cell proteins, lipids, and carbohydrates, and can induce mutation in DNA (Boogar et al. 2014; Cechin et al. 2015). Increased NO level enhances the functions of antioxidant enzymes such as APX, GR, CAT, SOD, and POD and helps plants to limit oxidative damage (Farooq et al. 2009). NO donors such as SNP and potassium nitrite (PN) and NO scavengers like cPTIO [2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-­ oxyl-3-oxide] are widely used to elucidate molecular and physiological effects of

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress

Fig. 2  Model depicting the nitric oxide action pathway and its impact on plants

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NO in plants (Boyarshinov and Asafova 2011). SNP and PN can be applied in various concentrations on grasses (P. pratensis, L. preme, and Cytonodon) cultivated under drought stress led to an increased level of SOD, POD, CAT, and APX activities (Boogar et al. 2014). In wheat, the application of NO enhanced CAT and APX activity and reduced MDA, generated upon lipid oxidation content (Habib et  al. 2020). Similarly, SNP in 1, 10, 100  μL concentration is used on sunflower (Helianthus annuus) plants growing under drought stress and as a control. Results have shown that plants growing under water stress have a higher level of MDA and proline content and decreased POD activity, while SNP-treated plants showed increased relative water content (RWC) and proline concentration, increased POD activity, and decrease in MDA content (Hao et al. 2008). Overall, NO is a vital molecule during drought state, and several studies have shown that NO is generated in a different part of the tissue. Application of NO donors both endogenously and exogenously can help defend plants against oxidative injuries, protein degradation, the harmful effect on photosynthesis, and also enhance antioxidant mechanisms and maintain the water level in the cell.

4.2  Salinity Evaporation and plant transpiration remove pure water from ground that concentrates salt in the soil, irrigation water also contains some salt depending on the source, these salt from irrigation water are also added to the soil (Munns et al. 2020; Van Zelm et al. 2020). Through these processes after some time soil tend to become saline. Major ions contributing to salinity are Ca2+, Mg2+, and SO24− and NaCl (Hanin et al. 2016). Salt affects the plant in two ways, first due to high salt concentration, osmotic potential of water in soil decreases, decreased water potential reducese water available to plants and plants feel osmotic stress due to high solute concentration in plant cell (Farooq et al. 2013). Second, high concentration of ions accumulated in cells cause ionic imbalance and toxicity, high concentration of Na+/ Cl− ions inhibits photosynthesis, low osmotic potential in cytoplasm slows down plant growth (Munns et  al. 2020). Overall, they influence various morpho-­ physiological and biochemical processes in plants (Husen et al. 2016, 2018, 2019; Hussein et al. 2017). Zhou et al. (2016) have found in Arabidopsis that salt stress increases a level of AtCaM1 and AtCaM4 along with an accumulation of NO and AtCaM1 directly binds to GSNOR and inhibits its activity. Mutant atcam1 and atcam4 showed less accumulation of NO and salt stress-sensitive plant compared to wild-type plants. GSNOR knockdown transgenic plants showed a high accumulation of NO and more tolerance to salinity but inhibited growth (Zhou et al. 2016). With these results, Zhou et  al. (2016) summarized that GSNOR inhabitation by AtCaM 1 and AtCaM4 leads to the accumulation of NO and hence provides salinity tolerance to plants. Jain and Bhatla (2018) have observed that salt stress led to the accumulation of RNS; however level of S-nitrosation was different depending on the tissue. S-nitrosation increased in cotyledons but de-nitrosation increased in

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roots. Upon identification of differentially nitrosated proteins, redox-related proteins like peroxiredoxin, ascorbate peroxidase (APX), Glutathione reductase (GR), and monodehydroascorbate reductase (MDAR) were identified. MDAR function inhibited by nitrosation, Begara-Morales et al. (2015) showed that S-nitrosation of Cys68 is responsible for this inhibition, GR does not show any change in activity on nitrosation. APX is interestingly both activated and inhibited by NO (Lindermayr and Durner 2015). Tyrosine nitration negatively regulates cytosolic APX in contrast S-nitrosation on Cys 32 enhances its function and crucial for salt tolerance (Begara-­ Morales et al. 2014). In Arabidopsis, NO promotes germination and plant growth by the accumulation of ETHYLENE INSENSITIVE 3 (EIN3) and enhancement of its downstream signaling (Li et al. 2016).

4.3  Extreme Temperature Heat stress trigger signaling response that activates heat shock proteins, hormones, ROS, and calcium together to cause an adaptive response (Parankusam et al. 2017). Signaling mediated by RNS, ROS, and H2O2 is proposed to induce heat tolerance in plants through activation of antioxidant enzymes, enhancing the expression of heat shock proteins (Zhao et al. 2009; Hasanuzzaman et al. 2013; Parankusam et al. 2017). Protein tyrosine nitration level increases in 3-week-old pea plant upon heat treatment compared to control plants, a similar effect has been observed upon cold treatment also, it showed that both low- and high-temperature stress enhance tyrosine nitration and hence nitrosative stress (Corpas et  al. 2008). Sunflower hypocotyl upon exposure to heat stress showed a 2.5-fold increase in NO2-tyr content compared to control (Chaki et al. 2011). From same experiment 13 tyrosine nitrosylated protein induced upon heat stress exposure was identified, these proteins are involved in redox metabolism, photosynthesis, and carbohydrate metabolism including Ferredoxin NADP oxidoreductase (FNR) and Carbonic anhydrase (CA) (Chaki et al. 2013). Pre-treatment of NO reduced damage caused by high temperature in rice, wheat, and maize (Uchida et al. 2002). Chaki et al. (2011) showed that upon heat treatment NO production decreased but the level of SNO increased due to inhibition effect on GSNOR activity and protein tyrosine nitration was enhanced. NO activates production of protective proline and antioxidant production to decrease oxidative damage, application of cPTIO (NO scavenger) shown to decrease proline production and plant tolerance (Alamri et  al. 2019) Recently, Mata-Pérez et  al. (2016) reported the presence of nitrolinolenic acid (NO2-Ln), the effect of NO2-Ln on gene expression was analyzed using RNA-seq and shown NO2-Ln actively involved in the induction of heat shock protein expression and chaperon network. Level of NO2-Ln fluctuates during various stress conditions like wounding, salt, heat, etc. and showed that it could be involved in these stresses-related responses. The mechanism of NO2-Ln regulation has not yet been unveiled however; NO2-Ln could act as NO donor that might be its role in signaling.

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4.4  Submergence Flooding is common to the stress faced by crop plants especially in tropical and subtropical regions. Climate change prediction also predicted about an increase in flood incidence in the near future (Hirabayashi et al. 2013). Flooding reduces gas exchange between roots and soil air and thus decreases in oxygen availability (hypoxia) (Dat et al. 2004). A decrease in O2 availability leads to disruption in the mitochondrial electron transport chain, increase pH inside cells, and enhance the generation of ROS and NO (Rhoads and Subbaiah 2007). An increase in ROS leads to higher interaction with ethylene and NO to promote adventitious root formation (Steffens 2014). The exact mechanism of NO production under submergence is not fully understood but it is predicted that mitochondrial electron transport chain, nitrite (NO2−), and ascorbate are involved in its production (Wang and Hargrove 2013). Nitrite (NO2−) under hypoxia is reduced in mitochondria and converted into NO, then move to the cytoplasm where it gets oxidized by HB into nitrate (NO3−) (Limami et al. 2014). NO acts as terminal electron acceptor in mitochondria in the absence of oxygen to generate a small amount of ATP and hence prevents the complete absence of energy (Dordas et al. 2003; Herold and Puppo 2005). Under submerge conditions, ethylene response transcription factor VII (ERF VII) acts as hypoxia indicator and induce tolerance, NO shown to promote N-end rule pathway degradation of ethylene response (ERF VII) transcription factor VII, drop in ERF VII concentration is deleterious for plant survival under hypoxia, ERF VII promote expression of PHYTOGLOBIN1 (PGB1), a NO scavenger (Hartman et al. 2019).

4.5  Heavy Metal An increase in ROS is the first and most common effect of metal accumulation (Kalaivanan and Ganeshamurthy 2016). Collectively, studies showed that NO plays a critical role in heavy metal stress conditions through its antioxidant and ROS scavenger properties. Pre-treatment with SNP showed to reduce ROS levels in plants during metal toxicity (Kopyra and Gwóźdź 2003; Nabi et  al. 2019). SNP application on rice growing under high copper metal condition reduces ROS and protects plants (Yu et al. 2005). Heavy metal stress is known to activate NADPH oxidase and stimulate ROS production in apoplast, chloroplast, and mitochondria (Chmielowska-Bąk et al. 2014). Some heavy metals directly increase NO concentration, for example, Lead (Pb) enhances the activity of cytosolic NR (Yu et  al. 2012). Cadmium causes iron deficiency and thus induces signaling cascade that increases NO synthesis (Besson-Bard et al. 2009). Arsenic enhances NO synthesis and GSNOR activity and thus maintains constant NO concentration (Leterrier et al. 2012). The increase in NO concentration may be due to signaling from increased ROS concentration (Yun et al. 2011).

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At low concentration, NO participates in metal detoxification through various mechanisms like binding metal ions to the cell wall (Singh et al. 2011), promoting metal ions transfer to vacuoles, by phytochemical synthesis (De Michele et  al. 2009), or promoting activity of proton gradient pump to create an electrochemical gradient that promotes metal ion absorption (Cui et al. 2010). NO stimulates synthesis and activity of antioxidants in a plant cell that can limit the toxic effect of oxidative stress generated by metal ions (Andrade et al. 2016). S-nitrosation recalibrates the function of enzymes involved in ROS metabolisms, for example, glycolate oxidase and NADPH Oxidase help plants in maintaining homeostasis (Yun et al. 2011). NO has been shown to reduce MDA and ROS by inducing antioxidant enzyme in rice and mung bean growing under arsenic (As3+) stress (Singh et al. 2009; Jin et al. 2010; Ismail 2012). S-nitrosation is known to reduce CAT activity (Clark et  al. 2000) furthermore; a study showed reduced S-nitrosation of CAT during Cd++ stress (Ortega-Galisteo et al. 2012). Thus, CAT activity increased under metal stress condition and helped in reducing ROS.

4.6  Biotic Stress Plant defense against biotic stresses, caused by other living disturbances including fungi, bacteria, viruses, harmful insects, or parasitic plants (Mehta et  al. 2021; Rahman et al. 2019; Mehta et al. 2019b). This is regulated by communicating different signaling cascades in which NO plays a critical role (Dmitriev 2003; Bot et al. 2019). Plants exhibit their strategies to counteract the pathogen attack using effective defense mechanisms including localized program cell death (PCD) which may associate signaling components similar to animal apoptosis (Bot et al. 2019); however, it is necessary to recognize the potential pathogen for triggering defense responses (Dmitriev 2003). Cell membrane receptors recognize the stress stimulus and result in the formation of signaling molecules that changed the concentration or regulation of the second messengers leading to the triggering of defense responses (Arasimowicz and Floryszak-Wieczorek 2007). Several studies demonstrated the ability of NO to regulate the interactions between plants and various pathogens (Gill et al. 2013; Arasimowicz-Jelonek and Floryszak-Wieczorek 2014) and its accumulation is required to inhibit growth and development of the pathogen (Dmitriev 2003). Several works have proven the genetic evidence that application of NO donors to plants and cell suspension cultures induced the expression of defense-related genes which encodes phenylalanine ammonia-lyase (PAL) and pathogenesis-related 1 (PR1) protein, associated with the biosynthesis of phenylpropanoid and salicylic acid (SA)-mediating signaling (Delledonne et al. 1998; Durner et al. 1998; Hong et al. 2008). The expression of PAL and PR1 also triggered by cGMPand cADPR, the two important molecules that act as a second messenger for NO signaling in mammals (Durner et al. 1998). The occurrence of cGMP in plants has been detected by various mass spectrometry techniques (Durner et al. 1998; Dmitriev 2003; Meier et al. 2010). Tobacco cells are treated with NO-induced rise in the cGMP content

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which indicates its role as a second messenger. After the recognition of stress response, cGMP is synthesized from guanosine 5-triphosphate (GTP) catalyzed by the activation of guanylyl cyclase (GC). An Arabidopsis receptor type wall-­ associated kinase-like (AtWAKL10) molecule, a twin domain, was identified as a GC candidate and the experimental evidence has shown the generation of cGMP in vitro from the intracellular domain of AtWAKL10431-700 (Meier et al. 2010). However, the role of catalytic enzymes GCs is yet to be identified in higher plants (Bot et al. 2019). It was indicated that the kinase activity of AtWAKL10431-700 is relatively comparable with the Ser/Thr kinase activity levels in plants and animals. Moreover, AtWAKL10 is co-expressed with genes that are known for their functional roles in early pathogen responses. This indicates that AtWAKL10 has a functional role in early defense responses that marks it as responsible for the generation of cGMP induced by the pathogen (Meier et al. 2010). Also, AtWAK1 is reported to be associated with systemic acquired resistance (SAR), whole-plant resistance in preventing a wide circle of pathogens (Dmitriev 2003; Bot et al. 2019). Besides, Qiao et al. (2015) demonstrated that hydrogen peroxide (H2O2) and Ca2+ are involved in NO production to trigger the HR (hypersensitive response) cell death during Puccinia triticina infection and hence H2O2, NO, and Ca2+ jointly participate in the signal transduction process of HR (Qiao et al. 2015). In another study, transgenic tobacco plants treated with calmodulin-dependent mammalian nNOS enhanced the regulatory role of NO in salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) dependent pathways that are associated with disease resistance (Chun et al. 2012). Recently, Li et al. (2020) demonstrated the importance of NO in β-Aminobutyric acid (BABA)-induced tolerance to Botrytis cinerea in tomato plants. Plants treated with BABA increased NO accumulation and transcription of both the defense marker genes and defensive enzymes and reduced the signs of infection. However, BABA treatment along with cPTIO significantly decreased NO accumulation as well as increased disease occurrence and lesion area (Li et al. 2020). Similarly, the addition of NO scavenger in 2, 4-epibrassinolide (BL) treated maize plants delay Maize Chlorotic Mottle Virus (MCMV) infection (Cao et al. 2019). Zhu et al. have reviewed the significant role of NO in the upregulation of melatonin content, which in turn induced the mitogen-activated protein kinase (MAPK) signaling cascade and associated defense responses to bacterial pathogens (Zhu et al. 2019). To study the cellular NO production in charcoal rot disease of Corchorus capsularis (jute) plants caused by necrotrophic pathogen Macrophomina phaseolina, the biochemical approach was performed which resulted in raised NO, RNS, and SNOs generation in infected tissues. And it was suggested that the production of NO and RNS may significantly play an important role in necrotrophic host-pathogen interaction (Sarkar et al. 2014). Moreover, NO performed its bioactivity predominantly through S-nitrosylation: a cysteine based post-translational modification (PTM) of important transcription factors and direct modulation of ion channels (Hong et al. 2008). Recently, several studies regarding the physiological functions of NO responses to plant and animal stress through S-nitrosylation mediated PTM has been reviewed (Lu et al. 2020). NO covalently binds to cysteine residue and forms an SNO, which then interacts

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with intracellular molecules containing sulfhydryl group that makes great importance since they are more stable than NO.  For example, S-nitrosoglutathione (GSNO), a mobile reservoir of NO, is a product of S-nitrosylation reaction between both NO with glutathione (GSH) (Bot et al. 2019). One study investigated the effect of exogenous NO, i.e., GSNO and sodium nitroprusside (SNP), on Pisum sativum leaves infested by Acyrthosiphon pisum. It induced sequentially defense reaction against A. pisum and had a hindrance effect on aphid feeding (Woźniak et al. 2017). Feechan et  al. showed that mutations in Arabidopsis thaliana GSNO reductase 1 (AtGSNOR1) influenced cellular SNO level both in basal condition and during pathogen invasion. In the loss of function of AtGSNOR1 (atgsnor1), resistance (R) gene plant defense, basal resistance, and non-host disease resistance (NHR) are all compromised. Most importantly, the gain of function of AtGSNOR1 activity led to the induction of resistance against the wheat powdery mildew ingression (Feechan et al. 2005). Furthermore, disease susceptibility in atgsnor plants showed decreased and delayed expression of SA-associated genes which indicates that AtGSNOR1 mediates the expression of the SA gene in response to microbial pathogens (Feechan et al. 2005). To investigate the roles of NO in response to plant biotic stresses, many researchers have used protein S-nitrosylation assay. For example, in a study, induction of NO production in rice black-streaked dwarf virus (RBSDV) inoculated plants increased S-nitrosylation whereas it was not observed in RBSDV plants without NO induction (Lu et al. 2020). This indicates a lack of NO production. Similarly, endogenous GSNO prevented the spread of mildew disease in resistant cultivars of sunflower and reduced GSNOR levels in transgenic Arabidopsis showed increased resistance against Peronospora parasitica by regulating cellular SNO content (Wimalasekera et al. 2011). Therefore, the functions of NO are not fully controlled at the level of its biosynthesis during plant defense response.

5  Conclusions Since many reports on the physiological role of nitric oxide in plants is published, numerous studies have performed to find out the detailed molecular insights of its production in plants, and downstream signaling mechanisms. Results from these reports have shown that NO is the major regulator of metabolic and signaling processes form embryonic development, root development, growth, flowering, fruit ripening, leaf senescence, and stress response in plants. Numerous ways have been described for the generation of NO in plants, but animal-like NO producing enzyme, NOS, is missing in plants. Studies using NOS inhibitors/activators have shown changes in nitration state but there are no evidence enzymes have found. Plants may contain some similar mechanism that is affected by NOS inhibitors/activators and hence works on the identification of production mechanism is still going on. NO is a highly reactive molecule that participates in nitration and nitrosation of amino acids such as tyrosine, tryptophan, methionine, and cysteine. S-nitrosation of cysteine and tyrosine nitration is appeared to be a major contributor in NO-dependent

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regulations along with metal-nitrosylation. From the recent report of fatty acid nitration (NO-FAs), DNA and RNA nitration, along with NO interaction with redox molecule ROS, H2S opens a new area of research on how NO contributes to plant life. The cellular environment is also regulating NO actions depending on its concentration and the redox state of NO function extensively varies. The development of real-time in vivo NO monitoring system will provide more details in this area. The identification of novel NO producing enzymes and understanding the mechanisms of NO reaction with redox-related molecules and their interactions with proteins, nucleic acids, and carbohydrates as a complete network would be beneficial for further studies in finding the significance of spatial and temporal accumulation of NO in the plant cell.

References Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295 Alamri SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Ali HM, Alakeel KA (2019) Nitric oxide-­ mediated cross-talk of proline and heat shock proteins induce thermotolerance in Vicia faba L. Environ Exp Bot 161:290–302 Alexandra Ageeva-Kieferle, Elisabeth Georgii, Barbro Winkler, Andrea Ghirardo, Andreas Albert, Patrick Hüther, Alexander Mengel, Claude Becker, Jörg-Peter Schnitzler, Jörg Durner, Christian Lindermayr, (2021) Nitric oxide coordinates growth, development, and stress response via histone modification and gene expression. Plant Physiol Anamika, Mehta S, Singh B, Patra A, Islam MA (2019) Databases: a weapon from the arsenal of bioinformatics for plant abiotic stress research. In: Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 135–169 Andrade HM, Oliveira JA, Farnese FS, Ribeiro C, Silva AA, Campos FV, Neto JL (2016) Arsenic toxicity: cell signalling and the attenuating effect of nitric oxide in Eichhornia crassipes. Biol Plant 60:173–180 Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876–887 Arasimowicz-Jelonek M, Floryszak-Wieczorek J (2014) Nitric oxide: an effective weapon of the plant or the pathogen? Mol Plant 15:406–416 Arasimowicz-Jelonek M, Floryszak-Wieczorek J (2019) A physiological perspective on targets of nitration in NO-based signaling networks in plants. J Exp Bot 70:4379–4389 Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. Int J Mol Sci 13:15193–15208 Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411 Baena G, Feria AB, Echevarría C, Monreal JA, García-Mauriño S (2017) Salinity promotes opposite patterns of carbonylation and nitrosylation of C4 phosphoenolpyruvate carboxylase in sorghum leaves. Planta 246:1203–1214 Bartesaghi S, Radi R (2018) Fundamentals on the biochemistry of peroxynitrite and protein tyrosine nitration. Redox Biol 14:618–625 Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress

319

Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996 Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant systems are regulated by nitric oxide-mediated post-­ translational modifications (NO-PTMs). Front Plant Sci 7:152 Begara-Morales JC, Sánchez-calvo B, Gómez-rodríguez MV, Chaki M, Valderrama R, Mata-­ pérez C, López-jaramillo J, Corpas FJ, Barroso JB (2019) Short-term low temperature induces nitro-oxidative stress that deregulates the nadp-malic enzyme function by tyrosine nitration in Arabidopsis thaliana. Antioxidants 8:448 Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem 282:1352–1358 Berger A, Boscari A, Frendo P, Brouquisse R (2019) Nitric oxide signaling, metabolism and toxic nitrogen-fixing symbiosis. J Exp 70:4505–4520 Besson-Bard A, Courtois C, Gauthier A, Dahan J, Dobrowolska G, Jeandroz S, Wendehenne D (2008) Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Mol Plant 1:218–228 Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315 Bharti J, Sahil, Mehta S, Ahmad S, Singh B, Padhy AK, Srivastava N, Pandey V (2021) Mitogen-­ Activated Protein Kinase, Plants, and Heat Stress. In Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 323–354 Bohnert HJ, Gong Q, Li P, Ma S (2006) Unraveling abiotic stress tolerance mechanisms—getting genomics going. Curr Opin Plant Biol 9:180–188 Boogar AR, Salehi H, Jowkar A (2014) Exogenous nitric oxide alleviates oxidative damage in turfgrasses under drought stress. South Afr J Bot 92:78–82 Bot P, Mun BG, Imran QM, Hussain A, Lee SU, Loake G, Yun BW (2019) Differential expression of AtWAKL10 in response to nitric oxide suggests a putative role in biotic and abiotic stress responses. PeerJ 7:7383 Boyarshinov AV, Asafova EV (2011) Stress responses of wheat leaves to dehydration: participation of endogenous NO and effect of sodium nitroprusside. Russ J Plant Physiol 58:1034–1039 Boyer JS (1982) Plant productivity and environment. Science 218:443–448 Brouquisse R (2019) Multifaceted roles of nitric oxide in plants. Oxford University Press, Oxford, pp 4319–4322 Cao N, Zhan B, Zhou X (2019) Nitric oxide as a downstream signaling molecule in brassinosteroid-­ mediated virus susceptibility to maize chlorotic mottle virus in maize. Viruses 11:368 Castro L, Demicheli V, Tórtora V, Radi R (2011) Mitochondrial protein tyrosine nitration. Free Radic Res 45:37–52 Cechin I, Cardoso GS, de Fátima Fumis T, Corniani N (2015) Nitric oxide reduces oxidative damage induced by water stress in sunflower plants. Bragantia 74:200–206 Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, López-Jaramillo J, Luque F, Palma JM, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Gómez-Rodríguez MV, Corpas FJ, Barroso JB (2009) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 60:4221–4234 Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-­ Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ 34:1803–1818

320

P. Pandey et al.

Chaki M, Carreras A, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Valderrama R, Corpas FJ, Barroso JB (2013) Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress. Nitric Oxide 29:30–33 Chen L, Wu R, Feng J, Feng T, Wang C, Hu J, Zhan N, Li Y, Ma X, Ren B, Zhang J, Song CP, Li J, Zhou JM, Zuo J (2020) Transnitrosylation mediated by the non-canonical catalase ROG1 regulates nitric oxide signaling in plants. Dev Cell 53:444–457.e5 Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:245 Chun HJ, Park HC, Koo SC, Lee JH, Park CY, Choi MS, Chung WS (2012) Constitutive expression of mammalian nitric oxide synthase in tobacco plants triggers disease resistance to pathogens. Mol Cells 34:463–471 Chu-Puga Á, González-Gordo S, Rodríguez-Ruiz M, Palma JM, Corpas FJ (2019) NADPH oxidase (Rboh) activity is up regulated during sweet pepper (capsicum annuum L.) fruit ripening. Antioxidants 8:9 Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact 13:1380–1384 Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol 199:633–635 Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, Del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722 Cui XM, Zhang YK, Wu XB, Liu CS (2010) The investigation of the alleviated effect of copper toxicity by exogenous nitric oxide in tomato plants. Plant Soil 56:274–281 Cui B, Pan Q, Clarke D, Villarreal MO, Umbreen S, Yuan B, Shan W, Jiang J, Loake GJ (2018) S-nitrosylation of the zinc finger protein SRG1 regulates plant immunity. Nat Commun 9:1–12 Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42:273–282 De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Di Toppi LS, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in arabidopsis suspension cultures. Plant Physiol 150:217–228 Del Castello F, Nejamkin A, Cassia R, Correa-Aragunde N, Fernández B, Foresi N, Lombardo C, Ramirez L, Lamattina L (2019) The era of nitric oxide in plant biology: twenty years tying up loose ends. Nitric Oxide 85:17–27 Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588 Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212 Dilawari R, Kaur N, Priyadarshi N, Kumar B, Abdelmotelb KF, Lal SK, Singh B, Tripathi A, Aggarwal SK, Jat BS, Mehta S (2021) Genome Editing: A Tool from the Vault of Science for Engineering Climate-Resilient Cereals. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 45–72 Ding Y, Gardiner DM, Xiao D, Kazan K (2020) Regulators of nitric oxide signaling triggered by host perception in a plant pathogen. Proc Natl Acad Sci U S A 117:11147–11157 Dmitriev AP (2003) Signal molecules for plant defense responses to biotic stress. Russ J Plant 50:417–425 Dordas C, Rivoal J, Hill RD (2003) Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot 91:173–178 Dordas C, Hasinoff BB, Rivoal J, Hill RD (2004) Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219:66–72 Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci U S A 95:10328–10333

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress

321

Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Farooq M, Basra SMA, Wahid A, Rehman H (2009) Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 195:254–261 Farooq M, Siddique KH, Schubert S (2013) Role of nitric oxide in improving plant resistance against salt stress. In: Ecophysiology and responses of plants under salt. Springer, New York, pp 413–424 Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci U S A 102:8054–8059 Feigl G, Czifra Á, Molnár Á, Bodor A, Kovács E, Perei K, Jebet V, Kolbert Z (2020) Reorganization of protein tyrosine nitration pattern indicates the relative tolerance of Brassica napus (L.) over Helianthus annuus (L.) to combined heavy metal treatment. Plants 9:902 Ferrer-Sueta G, Campolo N, Trujillo M, Bartesaghi S, Carballal S, Romero N, Alvarez B, Radi R (2018) Biochemistry of peroxynitrite and protein tyrosine nitration. Chem Rev 118:1338–1408 Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830 Foresi N, Mayta ML, Lodeyro AF, Scuffi D, Correa-Aragunde N, García-Mata C, Casalongué C, Carrillo N, Lamattina L (2015) Expression of the tetrahydrofolate-dependent nitric oxide synthase from the green alga Ostreococcus tauri increases tolerance to abiotic stresses and influences stomatal development in Arabidopsis. Plant J 82:806–821 Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties—a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202 Gill, S. S., Hasanuzzaman, M., Nahar, K., Macovei, A., & Tuteja, N. (2013). Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261 Gong B, Shi Q (2019) Identifying S-nitrosylated proteins and unraveling S-nitrosoglutathione reductase-modulated sodic alkaline stress tolerance in Solanum lycopersicum L. Plant Physiol Biochem 142:84–93 González-Gordo S, Bautista R, Claros MG, Cañas A, Palma JM, Corpas FJ (2019) Nitric oxide-­ dependent regulation of sweet pepper fruit ripening. J Exp 70:4557–4570 Habib N, Ali Q, Ali S, Javed MT, Zulqurnain Haider M, Perveen R, Shahid MR, Rizwan M, Abdel-­ Daim MM, Elkelish A, Bin-Jumah M (2020) Use of nitric oxide and hydrogen peroxide for better yield of wheat (Triticum aestivum L.) under water deficit conditions: growth, osmoregulation, and antioxidative defense mechanism. Plants 9:285 Hancock JT (2012) No synthase? generation of nitric oxide in plants. Period Biol 114:19–24 Hancock JT, Neill SJ (2019) Nitric oxide: its generation and interactions with other reactive signaling compounds. Plants 8(2):41 Hancock JT, Veal D (2021) Nitric oxide, other reactive signalling compounds, redox and reductive stress. J Exp Bot 72(3):819–829 Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787 Hao, G. P., Xing, Y., & Zhang, J. H. (2008). Role of nitric oxide dependence on nitric oxide synthase‐ like activity in the water stress signaling of maize seedling. J Integr Plant Biol  50(4):435–442 Hartman S, Liu Z, van Veen H, Vicente J, Reinen E, Martopawiro S, Zhang H, van Dongen N, Bosman F, Bassel GW, Visser EJW, Bailey-Serres J, Theodoulou FL, Hebelstrup KH, Gibbs DJ, Holdsworth MJ, Sasidharan R, Voesenek LACJ (2019) Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nat Commun 10:1–9 Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684

322

P. Pandey et al.

Heinrich TA, Da Silva RS, Miranda KM, Switzer CH, Wink DA, Fukuto JM (2013) Biological nitric oxide signalling: chemistry and terminology. Br J Pharmacol 169:1417–1429 Herold S, Puppo A (2005) Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules? J Biol Inorg Chem 10:935–945 Hill R, Hargrove M, Arredondo-Peter R (2016) Phytoglobin: a novel nomenclature for plant globins accepted by the globin community at the 2014 XVIII conference on Oxygen-Binding and Sensing Proteins. F1000Res 5:212 Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kim H, Kanae S (2013) Global flood risk under climate change. Nat Clim Chang 3:816–821 Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999 Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K, Chu C, Wang Y, Loake GJ (2008) Nitric oxide function and signalling in plant disease resistance. J Exp Bot 59:147–154 Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Genet 59:124–136 Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429 Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186 Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agric Food Secur 7:44 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Ismail GSM (2012) Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303–1311 Jahnová J, Luhová L, Petřivalský M (2019) S-nitrosoglutathione reductase-the master regulator of protein S-nitrosation in plant NO signaling. Plants 8:48 Jain P, Bhatla SC (2018) Tyrosine nitration of cytosolic peroxidase is probably triggered as a long distance signaling response in sunflower seedling cotyledons subjected to salt stress. PLoS One 13:e0197132 Jain P, von Toerne C, Lindermayr C, Bhatla SC (2018) S-nitrosylation/denitrosylation as a regulatory mechanism of salt stress sensing in sunflower seedlings. Physiol Plant 162:49–72 Janus Ł, Milczarek G, Arasimowicz-Jelonek M, Abramowski D, Billert H, Floryszak-Wieczorek J (2013) Normoergic NO-dependent changes, triggered by a SAR inducer in potato, create more potent defense responses to Phytophthora infestans. Plant Sci 211:23–34 Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GKS, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci Signal 9:re2 Jedelská T, Kraiczová VŠ, Bercíková L, Cincalová L, Luhová L, Petrivalský M (2019) Tomato root growth inhibition by salinity and cadmium is mediated by S-nitrosative modifications of ROS metabolic enzymes controlled by s-nitrosoglutathione reductase. Biomolecules 9:393 Jin JW, Xu YF, Huang YF (2010) Protective effect of nitric oxide against arsenic-induced oxidative damage in tall fescue leaves. Afr J Biotechnol 9:1619–1627

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress

323

Kalaivanan D, Ganeshamurthy AN (2016) Mechanisms of heavy metal toxicity in plants. In: Abiotic stress physiology of horticultural crops. Springer, pp 85–102 Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant 148:371–386 Kharbech O, Ben Massoud M, Sakouhi L, Djebali W, Jose Mur LA, Chaoui A (2020) Exogenous application of hydrogen sulfide reduces chromium toxicity in maize seedlings by suppressing NADPH oxidase activities and methylglyoxal accumulation. Plant Physiol Biochem 154:646–656 Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T, DeAngelo J, Hausladen A, Stamler JS (2002) OxyR: a molecular code for redox-related signaling. Cell 109:383–396 Klepper L (1979) Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Environ 13:537–542 Kolbert Z, Feigl G, Bordé Á, Molnár Á, Erdei L (2017) Protein tyrosine nitration in plants: present knowledge, computational prediction and future perspectives. Plant Physiol Biochem 113:56–63 Kolbert Z, Molnr A, Olh D, Feigl G, Horvth E, Erdei L, Ardg A, Rudolf E, Barth T, Lindermayr C (2019) S-nitrosothiol signaling is involved in regulating hydrogen peroxide metabolism of zinc-stressed Arabidopsis. Plant Cell Physiol 60:2449–2463 Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017 Kubienová L, Tichá T, Jahnová J, Luhová L, Mieslerová B, Petřivalský M (2014) Effect of abiotic stress stimuli on S-nitrosoglutathione reductase in plants. Planta 239:139–146 Kushwaha BK, Singh S, Tripathi DK, Sharma S, Prasad SM, Chauhan DK, Kumar V, Singh VP (2019) New adventitious root formation and primary root biomass accumulation are regulated by nitric oxide and reactive oxygen species in rice seedlings under arsenate stress. J Hazard Mater 361:134–140 Lal SK, Kumar S, Sheri V, Mehta S, Varakumar P, Ram B, Borphukan B, James D, Fartyal D, Reddy MK (2018) Seed priming: an emerging technology to impart abiotic stress tolerance in crop plants. In: Advances in seed priming. Springer, Singapore, pp 41–50 Leshem YY, Kuiper PJC (1996) Is there a GAS (general adaptation syndrome) response to various types of environmental stress? Biol Plant 38:1–18 Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143 Li X, Pan Y, Chang B, Wang Y, Tang Z (2016) NO promotes seed germination and seedling growth under high salt may depend on EIN3 protein in Arabidopsis. Front Plant Sci 6:1203 Li R, Sheng J, Shen L (2020) Nitric oxide plays an important role in β-aminobutyric acid-induced resistance to Botrytis cinerea in tomato plants. Plant Pathol J 36:121–132 Limami AM, Diab H, Lothier J (2014) Nitrogen metabolism in plants under low oxygen stress. Planta 239:531–541 Lindermayr C, Durner J (2015) Interplay of reactive oxygen species and nitric oxide: nitric oxide coordinates reactive oxygen species homeostasis. Plant Physiol 167:1209–1210 Liu JZ, Duan J, Ni M, Liu Z, Qiu WL, Whitham SA, Qian WJ (2017) S-Nitrosylation inhibits the kinase activity of tomato phosphoinositide-dependent kinase 1 (PDK1). J Biol Chem 292:19743–19751 Lu R, Liu Z, Shao Y, Su J, Li X, Sun F, Zhang Y, Li S, Zhang Y, Cui J, Zhou Y, Shen W, Zhou T (2020) Nitric oxide enhances rice resistance to rice black-streaked dwarf virus infection. Rice 13:1–13 Lv X, Li H, Chen X, Xiang X, Guo Z, Yu J, Zhou Y (2018) The role of calcium-dependent protein kinase in hydrogen peroxide, nitric oxide and ABA-dependent cold acclimation. J Exp Bot 69:4127–4139

324

P. Pandey et al.

Maiti RK, Satya P (2014) Research advances in major cereal crops for adaptation to abiotic stresses. GM Crops Food 5:259–279 Małolepsza U (2009) Nitric oxide production in plants. Postepy Biochem 53:263–271 Matamoros MA, Cutrona MC, Wienkoop S, Begara-Morales JC, Sandal N, Orera I, Barroso JB, Stougaard J, Becana M (2020) Altered plant and nodule development and protein s-­nitrosylation in lotus japonicus mutants deficient in s-nitrosoglutathione reductases. Plant Cell Physiol 61:105–117 Mata-Pérez C, Sánchez-Calvo B, Begara-Morales JC, Carreras A, Padilla MN, Melguizo M, Valderrama R, Corpas FJ, Barroso JB (2016) Nitro-linolenic acid is a nitric oxide donor. Nitric Oxide 57:57–63 Mathieu C, Moreau S, Frendo P, Puppo A, Davies MJ (1998) Direct detection of radicals in intact soybean nodules: presence of nitric oxide-leghemoglobin complexes. Free Radic Biol Med 24:1242–1249 Mehta S, James D, Reddy MK (2019a) Omics technologies for abiotic stress tolerance in plants: current status and prospects. In: Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 1–34 Mehta S, Singh B, Dhakate P, Rahman M, Islam MA (2019b) Rice, marker-assisted breeding, and disease resistance. In: Disease resistance in crop plants. Springer, Cham, pp 83–111 Mehta S, Lal SK, Sahu KP, Venkatapuram AK, Kumar M, Sheri V, Varakumar P, Vishwakarma C, Yadav R, Jameel MR, Ali M, Achary VMM, Reddy MK (2020) CRISPR/Cas9-Edited Rice: A New Frontier for Sustainable Agriculture. In: New Frontiers in Stress Management for Durable Agriculture. Springer, Singapore, pp 427–458 Mehta S, Singh B, Patra A, Tripathi A, Easwaran M, Choudhary JR, Choudhary M, Aggarwal SK (2020) Maize microbiome: current insights for the sustainable agriculture. In: Microbiomes and Plant Health. Academic Press, Massachusetts, pp 267–297 Mehta S, Chakraborty A, Roy A, Singh IK, Singh A (2021) Fight Hard or Die Trying: Current Status of Lipid Signaling during Plant–Pathogen Interaction. Plants 10:1098 Mehta S, Gogna M, Singh B, Patra A, Singh IK, Singh A (2021) Silicon: a plant nutritional “non-­ entity” for mitigating abiotic stresses. In: Plant stress biology. Springer, Singapore, pp 17–49 Meier S, Ruzvidzo O, Morse M, Donaldson L, Kwezi L, Gehring C (2010) The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. PLoS One 5:e8904 Miller YI, Smith A, Morgan WT, Shaklai N (1996) Role of hemopexin in protection of low-density lipoprotein against hemoglobin-induced oxidation. Biochemistry 35:13112–13117 Modolo LV, Augusto O, Almeida IMG, Magalhaes JR, Salgado I (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett 579:3814–3820 Munns R, Passioura JB, Colmer TD, Byrt CS (2020) Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol 225:1091–1096 Mur, L. A., Prats, E., Pierre, S., Hall, M. A., & Hebelstrup, K. H. (2013). Integrating nitric oxide into salicylic acid and jasmonic acid/ ethylene plant defense pathways. Front Plant Sci 4:215 Nabi RBS, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun BG, Yun BW (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ Exp Bot 161:120–133 Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247 Nejamkin A, Foresi N, Mayta ML, Lodeyro AF, Del Castello F, Correa-Aragunde N, Carrillo N, Lamattina L (2020) Nitrogen depletion blocks growth stimulation driven by the expression of nitric oxide synthase in tobacco. Front Plant Sci 11:312 Nelson MJ (1987) The nitric oxide complex of ferrous soybean lipoxygenase-1. Substrate, pH, and ethanol effects on the active-site iron. J Biol Chem 262:12137–12142

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress

325

Niu L, Yu J, Liao W, Wu Y, Xie J, Yu J, Lv J, Xiao X, Hu L (2019) Proteomic investigation of S-nitrosylated proteins during NO-induced adventitious rooting of cucumber. Int J Mol Sci 20:5363 Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-­ Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103 Palma JM, Freschi L, Rodríguez-Ruiz M, González-Gordo S, Corpas FJ (2019) Nitric oxide in the physiology and quality of fleshy fruits. J Exp Bot 70:4405–4417 Parankusam S, Adimulam SS, Bhatnagar-Mathur P, Sharma KK (2017) Nitric oxide (NO) in plant heat stress tolerance: current knowledge and perspectives. Front Plant Sci 8:1582 Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–2794 Prakash V, Singh VP, Tripathi DK, Sharma S, Corpas FJ (2019) Crosstalk between nitric oxide (NO) and abscisic acid (ABA) signalling molecules in higher plants. Environ Exp Bot 161:41–49 Prakash V, Vishwakarma K, Singh VP, Rai P, Ramawat N, Tripathi DK, Sharma S (2020) NO and ROS implications in the organization of root system architecture. Physiol Plant 168:473–489 Qiao M, Sun J, Liu N, Sun T, Liu G, Han S, Hou C, Wang D (2015) Changes of nitric oxide and its relationship with H2O2 and Ca2+ in defense interactions between wheat and Puccinia triticina. PLoS One 10:e0132265 Qiu C, Sun J, Wang Y, Sun L, Xie H, Ding Y, Qian W, Ding Z (2019) First nitrosoproteomic profiling deciphers the cysteine S-nitrosylation involved in multiple metabolic pathways of tea leaves. Sci Rep 9:1–9 Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci U S A 101:4003–4008 Rahman M, Sultana S, Nath D, Kalita S, Chakravarty D, Mehta S, Wani SH, Islam MA (2019) Molecular breeding approaches for disease resistance in sugarcane. In: Disease resistance in crop plants. Springer, Cham, pp 131–155 Rajput LS, Aggarwal SK, Mehta S, Kumar S, Nataraj V, Shivakumar M, Maheshwari HS, Yadav S, Goswami D (2021) Role of WRKY Transcription Factor Superfamily in Plant Disease Management. In: Plant Stress Biology. Springer, Singapore, pp 335–361 Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7:177–194 Rodríguez-Ruiz M, González-Gordo S, Cañas A, Campos MJ, Paradela A, Corpas FJ, Palma JM (2019) Sweet pepper (Capsicum annuum L.) fruits contain an atypical peroxisomal catalase that is modulated by reactive oxygen and nitrogen species. Antioxidants 8:374 Sahil, Keshan R, Patra A, Mehta S, Abdelmotelb KF, Lavale SA, Chaudhary M, Aggarwal SK, Chattopadhyay A (2021) Expression and Regulation of Stress-Responsive Genes in Plants Under Harsh Environmental Conditions. In: Harsh Environment and Plant Resilience: Molecular and Functional Aspects. Springer Nature, Switzerland AG, pp 25–44 Sainz M, Calvo-Begueria L, Pérez-Rontomé C, Wienkoop S, Abián J, Staudinger C, Bartesaghi S, Radi R, Becana M (2015) Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. Plant J 81:723–735 Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers? Plant Sci 239:44–55 Sarkar TS, Biswas P, Ghosh SK, Ghosh S (2014) Nitric oxide production by necrotrophic pathogen Macrophomina phaseolina and the host plant in charcoal rot disease of jute: complexity of the interplay between necrotroph-host plant interactions. PLoS One 9:e107348 Serrato AJ, Romero-Puertas MC, Lázaro-Payo A, Sahrawy M (2018) Regulation by S-nitrosylation of the Calvin-Benson cycle fructose-1,6-bisphosphatase in Pisum sativum. Redox Biol 14:409–416

326

P. Pandey et al.

Sharma P, Sharma MMM, Patra A, Vashisth M, Mehta S, Singh B, Tiwari M, Pandey V (2020) The role of key transcription factors for cold tolerance in plants. In: Transcription factors for abiotic stress tolerance in plants. Academic, London, pp 123–152 Sharma P, Sharma MMM, Malik A, Vashisth M, Singh D, Kumar R, Singh B, Patra A, Mehta S, Pandey V (2021) Rhizosphere, Rhizosphere Biology, and Rhizospheric Engineering. In: Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management. Springer, Cham, pp 577–624 Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417 Shukla S, Zhao C, Shukla D (2019) Dewetting controls plant hormone perception and initiation of drought resistance signaling. Structure 27:692–702.e3 Silva LS, Alves MQ, Seabra AR, Carvalho HG (2019) Characterization of plant glutamine synthetase S-nitrosation. Nitric Oxide 88:73–86 Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297 Singh RK, Anandhan S, Singh S, Patade VY, Ahmed Z, Pande V (2011) Metallothionein-like gene from Cicer microphyllum is regulated by multiple abiotic stresses. Protoplasma 248:839–847 Singh B, Mehta S, Tiwari M, Bhatia S (2018) Legume breeding for fungal resistance: a lesson to learn. In: Molecular approaches for plant improvement. Kalpaz Publication, New Delhi, pp 159–180 Singh B, Mehta S, Aggarwal SK, Tiwari M, Bhuyan SI, Bhatia S, Islam MA (2019) Barley, disease resistance, and molecular breeding approaches. In: Disease resistance in crop plants. Springer, Cham, pp 261–299 Skelly MJ, Malik SI, Le Bihan T, Bo Y, Jiang J, Spoel SH, Loake GJ (2019) A role for S-nitrosylation of the SUMO-conjugating enzyme SCE1 in plant immunity. Proc Natl Acad Sci U S A 116:17090–17095 Stanton K, Mickelbart M (2014) Maintenance of water uptake and reduced water loss contribute to water stress tolerance of Spiraea alba Du Roi and Spiraea tomentosa L. Hortic Res 1:14033 Stasolla C, Huang S, Hill RD, Igamberdiev AU, Brouquisse R (2019) Spatio-temporal expression of phytoglobin: a determining factor in the NO specification of cell fate. J Exp Bot 70:4365–4377 Steffens B (2014) The role of ethylene and ROS in salinity, heavy metal, and flooding responses in rice. Front Plant Sci 5:685 Stiti N, Podgórska KA, Bartels D (2020) S-Nitrosation impairs activity of stress-inducible aldehyde dehydrogenases from Arabidopsis thaliana. Plant Sci 292:110389 Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956 Takahashi M, Shigeto J, Izumi S, Yoshizato K, Morikawa H (2016) Nitration is exclusive to defense-­ related PR-1, PR-3 and PR-5 proteins in tobacco leaves. Plant Signal Behav 11:e1197464 Takahashi M, Shigeto J, Sakamoto A, Morikawa H (2017) Selective nitration of PsbO1, PsbO2, and PsbP1 decreases PSII oxygen evolution and photochemical efficiency in intact leaves of Arabidopsis. Plant Signal Behav 12:1376157 Thu NBA, Hoang XLT, Truc MT, Sulieman S, Thao NP, Tran LP. (2017). Cytokinin signaling in plant response to abiotic stresses. In: Pandey GK, ed. Mechanism of plant hormone signaling under stress. Hoboken, NJ: John Wiley & Sons, 71–100 Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Segal Floh EI, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354 Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523 Umbreen S, Lubega J, Loake GJ, Kopriva S (2019) Sulfur: the heart of nitric oxide-dependent redox signalling. J Exp Bot 70:4279–4286

Nitric Oxide: A Key Modulator of Plant Responses Under Environmental Stress

327

Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433 Vishwakarma A, Wany A, Pandey S, Bulle M, Kumari A, Kishorekumar R, Igamberdiev AU, Mur LAJ, Gupta KJ, Brouquisse R (2019) Current approaches to measure nitric oxide in plants. J Exp Bot 70:4333–4343 Viswanath KK, Varakumar P, Pamuru RR, Basha SJ, Mehta S, Rao AD (2020) Plant lipoxygenases and their role in plant physiology. J Plant Biol 63:83–95 Wang X, Hargrove MS (2013) Nitric oxide in plants: the roles of ascorbate and hemoglobin. PLoS One 8:e82611 Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112:613–618 Wei L, Zhang M, Wei S, Zhang J, Wang C, Liao W (2020) Roles of nitric oxide in heavy metal stress in plants: cross-talk with phytohormones and protein S-nitrosylation. Environ Pollut 259:113943 Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signalling and defence responses. Curr Opin Plant 7:449–455 Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603 Wong A, Donaldson L, Portes MT, Eppinger J, Feijó JA, Gehring C (2020) Arabidopsis DIACYLGLYCEROL KINASE4 is involved in nitric oxide-dependent pollen tube guidance and fertilization. Development 147:dev183715 Woźniak A, Formela M, Bilman P, Grześkiewicz K, Bednarski W, Marczak Ł, Narożna D, Dancewicz K, Mai VC, Borowiak-Sobkowiak B, Floryszak-Wieczorek J, Gabryś B, Morkunas I (2017) The dynamics of the defense strategy of pea induced by exogenous nitric oxide in response to aphid infestation. Int J Mol Sci 18:329 Yadav B, Jogawat A, Lal SK, Lakra N, Mehta S, Shabek N, Narayan OP (2021) Plant mineral transport systems and the potential for crop improvement. Planta 253:45 Yu CC, Hung KT, Kao CH (2005) Nitric oxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. J Plant 162:1319–1330 Yu Q, Sun L, Jin H, Chen Q, Chen Z, Xu M (2012) Lead-induced nitric oxide generation plays a critical role in lead uptake by pogonatherum crinitum root cells. Plant Cell Physiol 53:1728–1736 Yu L, Chen X, Wang Z, Wang S, Wang Y, Zhu Q, Li S, Xiang C (2013) Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162:1378–1391 Yun BW, Feechan A, Yin M, Saidi NBB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268 Zhang J, Liao W (2019) Protein S-nitrosylation in plant abiotic stresses. Funct Plant Biol 47:1–10 Zhang LX, Li SX, Zhang H, Liang ZS (2007) Nitrogen rates and water stress effects on production, lipid peroxidation and antioxidative enzyme activities in two maize (Zea mays L.) genotypes. J Agron Crop Sci 193:387–397 Zhang ZW, Luo S, Zhang GC, Feng LY, Zheng C, Zhou YH, Du JB, Yuan M, Chen YE, Wang CQ, Liu WJ, Xu XC, Hu Y, Bai SL, Kong DD, Yuan S, He YK (2017) Nitric oxide induces monosaccharide accumulation through enzyme S-nitrosylation. Plant Cell Environ 40:1834–1848 Zhang L, Shi X, Zhang Y, Wang J, Yang J, Ishida T, Jiang W, Han X, Kang J, Wang X, Pan L, Lv S, Cao B, Zhang Y, Wu J, Han H, Hu Z, Cui L, Sawa S, He J, Wang G (2019a) CLE9 peptide-­ induced stomatal closure is mediated by abscisic acid, hydrogen peroxide, and nitric oxide in Arabidopsis thaliana. Plant Cell Environ 42:1033–1044 Zhang ZW, Fu YF, Zhou YH, Wang CQ, Lan T, Chen GD, Zeng J, Chen YE, Yuan M, Yuan S, Hu JY (2019b) Nitrogen and nitric oxide regulate Arabidopsis flowering differently. Plant Sci 284:177–184

328

P. Pandey et al.

Zhao FY, Liu W, Zhang SY (2009) Different responses of plant growth and antioxidant system to the combination of cadmium and heat stress in transgenic and non-transgenic rice. J Integr Plant Biol 51:942–950 Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li AQ, Li MJ, Li CS, Zhang BH, Wang XJ (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3 Zhou S, Jia L, Chu H, Wu D, Peng X, Liu X, Zhang J, Zhao J, Chen K, Zhao L (2016) Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S-nitrosoglutathione reductase via direct binding. PLoS Genet 12:e1006255 Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273 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 20:6200

Functions of Hydrogen Sulfide in Plant Regulation and Response to Abiotic Stress Sashi Sonkar, Akhilesh Kumar Singh, and Azamal Husen

Abbreviations H2S Hydrogen sulfide OS Oxidative stress ROS Reactive oxygen species

1  Introduction In the epoch of global warming and climate change, numerous unprecedented challenges were faced by the agricultural systems globally. Agriculture is the most effective division as it provides resources for food and feed industries (Prasad et al. 2017). The adverse environment such as abiotic stress (UV-B radiation, flooding, heavy metals, heat, drought, salinity, and so on) is accountable for the enormous loss of agricultural crop production throughout the world and disturbs overall growth and physiological and biochemical processes (Bray et al. 2000; Wang et al. 2003; Husen 2010; Husen et  al. 2018, 2019; Embiale et  al. 2016; Hussein et  al. 2017; Singh and Husen 2019, 2020; Iqbal et al. 2020a, b; Sonkar et al. 2021a, b; Porwal et al. 2021; Misra et al. 2021). In response to the adverse environment, reactive oxygen species (ROS) are produced and accumulates, which cause an oxidative burst in plants including algae (Singh et al. 2004; Rani et al. 2020. In plants, ROS include free radicals of lipid peroxidation, singlet oxygen, H2O2, and so on that increase cell toxicity and reduce plant growth (Mittler 2002; Khan et  al. 2016). Consequently, to alleviate the influence of oxidative stress (OS), the plants have S. Sonkar Department of Botany, Bankim Sardar College, Tangrakhali, South 24 Parganas, West Bengal, India A. K. Singh (*) Department of Biotechnology, School of Life Sciences, Mahatma Gandhi Central University, East Champaran, Bihar, India A. Husen Wolaita Sodo University, Wolaita, Ethiopia © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_13

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developed the antioxidant system by producing antioxidant enzymes (like glutathione reductase, catalase, and so on) as well as antioxidants, viz. tocopherol, ascorbate, and glutathione, which scavenge ROS (Mittler 2002; Khan and Khan 2017; Jain et  al. 2021). On the other hand, the hydrogen sulfide (H2S) is a colorless, small, lipophilic, and endogenously produced gaseous signaling molecule in plants. It is regarded as the third signaling unit in addition to carbon monoxide and nitric oxide in plants (Wang 2012). Interestingly, the cytotoxic concept of H2S at higher concentration has been changed as at a lower concentration, it acts as the important compound, where it affects various vital physiological processes in the plants (Olas 2014). Overall, the present chapter is an attempt to summarize the functions of H2S in plant regulation and responses under adverse environment (abiotic stress conditions).

2  Physiological Roles of H2S in Plants The H2S belongs to the group of related molecules called reactive sulfur species, which execute several tasks in the functioning of plants (Corpas 2019). The important physiological role of H2S in plants includes photosynthesis (Chen et al. 2011), fruit maturation (Dooley et al. 2013), stomatal movement (Jin and Pei 2016), leaf senescence (Álvarez et al. 2010), flowering (Zhang et al. 2011), root elongation or development (Zhang et al. 2009), seed germination (Zhang et al. 2008) as well as promotes nodulation and nitrogenase activity (Zou et al. 2019) (Fig. 1). It also controls the autophagy (Álvarez et al. 2012) and cell viability (Álvarez et al. 2010).

3  H2S and Plant Responses Under Adverse Environment Apart from the diverse physiological roles, the H2S facilitates protection and tolerance against various adverse environments, including heavy metals, drought, cold, heat, salt, flood, and UV-B radiation. Figure  2 summarizes the role of hydrogen sulfide towards the mitigation of adverse environment in plants (Table 1).

4  Synthesis of H2S in Plant Cell The metabolism of H2S comprises both biogenesis and its decomposition in plant cells. There are five enzymatic pathways occurring in plant cell for the biogenesis of H2S, viz. cysteine synthase, β-cyanoalanine synthase, sulfite reductase, D-cysteine desulfhydrase, and l-cysteine desulfhydrase pathway (Li 2015a, b; Rausch and Wachter 2005). l-Cysteine desulfhydrase is a cytoplasmic enzyme accountable for the conversion of l-cysteine into pyruvate with the generation of NH4+ and H2S

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Fig. 1  Different roles played by hydrogen sulfide in plants

using cofactor like pyridoxal phosphate (Calderwood and Kopriva 2014; Li 2015a, b). However, D-cysteine desulfhydrase is accountable towards the formation of H2S in the plant cell utilizing substrate D-cysteine in the mitochondria. d-Cysteine desulfhydrase and l-cysteine desulfhydrase were not correlated to each other though having similar functions with different cysteine enantiomers (da-Silva and Modolo 2017). In the mitochondria and cytoplasm of plant cells, the enzyme β-cyanoalanine synthase helps in the production of H2S as well as cyanuric acid in the course of the conversion of l-cysteine to cyanide (He et al. 2018; Li 2015a, b). It helps to maintain the cellular level of cyanide during ethylene synthesis since cyanide acts as an inhibitor of the mitochondrial respiratory chain (da-Silva and Modolo 2017). A chloroplast enzyme, sulfite reductase reduces sulfite ion to produce H2S in the presence of ferredoxin as an electron donor (da-Silva and Modolo 2017; He et al. 2018; Li 2015a, b). In chloroplasts, mitochondria, and cytosol, cysteine synthase accelerates the reversible reaction concerning l-cysteine and acetate to produce H2S and O-acetylserine (da-Silva and Modolo 2017; Li 2015a, b). In the presence of cysteine synthase, excessive H2S is reduced to cysteine or polypeptide comprising cysteine excluding gas emission. In higher plants, H2S liberating and cysteine degrading enzymes have been categorized (He et al. 2018; Papenbrock et al. 2007). The variations in the concentration of cellular H2S in plants under abiotic stress depend upon the tissues, genotypes, and species of plants as well as various stress, magnitude of stress, and the duration of stress (He et al. 2018). The double function of H2S as protective (at low concentration) or cytotoxin (at high concentration) is based upon its location and concentration in plant cells (He et  al. 2018). Moreover, H2S

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Fig. 2  Hydrogen sulfide facilitated mitigation of abiotic stress response in plants

homeostasis is very essential for the elimination of various stresses and executes its physiological functions in plant cells (Li et al. 2016a).

5  H  ydrogen Sulfide Mediated Mitigation of Plant Abiotic Stresses The hydrogen sulfide significantly assists in the mitigation of plant abiotic stresses, which are categorized under following subheadings.

5.1  H2S Alleviates UV-B Stress The decrease of the ozone layer in the atmosphere often allows the UV radiation (280-315 nm) to reach on the earth’s surface and cause harmful effects on biological systems together with plants (Rostami et al. 2019; Ulm and Nagy 2005). Various investigations have shown that exposure of the plant to UV-B light considerably alters the biochemical, physiological, and morphological processes (Kataria et al. 2014; Rostami et al. 2019). Usually, ROS produced upon exposure of the plants to

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Table 1  The diverse role of hydrogen sulfide in plants under adverse environment Type of stress UV-B radiation

Plant Barley (Hordeum vulgare) Borago (Borago officinalis L.)

Flooding

Pea (Pisum sativum L.)

Maize (Zea mays L.)

Low Grape (Vitis temperature vinifera L.)

Banana (Musa sp.)

Blueberry (Vaccinium angustifolium)

Source of hydrogen sulfide Stress response 1 mM sodium Increases the accumulation of hydrosulfide UV-B protective compounds such as anthocyanins and flavonoids. Redox homeostasis was maintained Eliminate the damages caused by 120μM UV-B radiation through the sodium improvement of reduced hydrosulfide glutathione content and antioxidative enzyme activities Eliminates root tip death due to 0.1 mM hypoxia by defending root tip cell sodium membranes from the damage hydrosulfide caused by reactive oxygen species as well as inhibiting the production of ethylene 1 mM sodium Stimulates the level of Ca2+ and hydrosulfide alcohol dehydrogenase activity. Improves the antioxidant defense activity High activity of superoxide 0.1 mM dismutase and enhanced expression sodium of VvICE1 and VvCBF3 genes. hydrosulfide The cell membrane permeability, malondialdehyde content, and superoxide anion radicals were found to be low Maintain the greater values of 0.5 mM lightness and peel firmness as well sodium as decrease the accretion of hydrosulfide malondialdehyde. The antioxidant capacity, total phenolics content, and phenylalanine ammonia-lyase activity were promoted. Hydrogen peroxide as well as superoxide anion accumulation was decreased. Activities of glutathione reductase, ascorbate peroxidase, catalase, superoxide dismutase, and guaiacol peroxidase were upregulated 0.5 mmol L−1 Alleviate the degradation of carotenoids and chlorophyll content sodium in leaves caused by the cold stress hydrosulfide as well as decrease the photoinhibition of photosystem II and I

References Li et al. (2016b)

Rostami et al. (2019)

Cheng et al. (2013)

Peng et al. (2016)

Fu et al. (2013)

Luo et al. (2015)

Tang et al. (2020)

(continued)

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Table 1 (continued) Type of stress Heat

Plant Tobacco (Nicotiana tabaccum L.)

Maize (Zea mays L.)

Strawberry (Fragaria × ananassa cv. “Camarosa”)

Maize (Zea mays L.)

Tobacco (Nicotiana tabaccum L.)

Tobacco (Nicotiana tabaccum L.)

Source of hydrogen sulfide Stress response 50μM sodium The decrease in malondialdehyde hydrosulfide accumulation, elimination of increment in electrolyte leakage, and alleviation of reduction in cell vitality 1.5μM sodium Enhanced the survival rate of hydrosulfide seedlings and germination seeds. A reduction in the accretion of malondialdehyde in coleoptile and decrement in tissue vitality as well as the elimination of increment in the electrolyte leakage of roots. The activity of proline dehydrogenase was decreased which allow the accretion of proline endogenously whereas the activity of ∆1-pyrroline-5-carboxylate synthetase was increased Activates the gene expression 100μM encoding for aquaporins, heat-­ sodium shock proteins (such as HSP70, hydrosulfide HSP80, HSP90), and antioxidant enzymes (such as cytosolic ascorbate peroxidase, catalase, manganese superoxide dismutase, and glutathione reductase) Sodium Salicylic acid-induced hydrogen hydrosulfide sulfide accumulation. Enhanced tissue vitality, seed germination, and survival percentage 50μM sodium Decrease in malondialdehyde hydrosulfide accumulation and alleviation of reduction in cells vitality. Increase the regrowth ability and survival rate of cells. Increases in l-cysteine desulfhydrase activity which accumulates hydrogen sulfide endogenously 50μM sodium Application of abscisic acid hydrosulfide increases the l-cysteine desulfhydrase enzyme activity, which in turn helps in the accretion of hydrogen sulfide. Decrease in malondialdehyde accumulation, elimination of an increase in electrolyte leakage, and alleviation of reduction in cell vitality as well as improved the regrowth ability and survival percentage

References Li et al. (2012b)

Li et al. (2013a, b)

Christou et al. (2014)

Li (2015a, b)

Li and Gu (2016)

Li and Jin (2016)

(continued)

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Table 1 (continued) Type of stress

Salt

Plant Poplar (Populus trichocarpa)

Source of hydrogen sulfide –

Maize (Zea mays L.)

500μM sodium hydrosulfide

Arabidopsis (Arabidopsis thaliana)

100μM sodium hydrosulfide or 10μM GYY4137

Wheat (Triticum aestivum L.) Alfalfa (Medicago sativa L.)

0.13 mM sodium hydrosulfide 100μM sodium hydrosulfide

Stress response Stimulates enzymes activity involves in hydrogen sulfide production. Modulation of S-nitrosoglutathione reductase and nitric oxide signaling by preventing the damage in plants caused by reactive oxygen species and reactive nitrogen species Improved fresh weight, root length, sprout length, and germination percentage. Increases the activities of antioxidant enzymes (such as catalase, superoxide dismutase, guaiacol peroxidase, glutathione reductase, and ascorbate peroxidase) and non-enzymatic water-soluble antioxidants (such as glutathione and ascorbic acid) contents as well as the ratio of reduced antioxidant to oxidized antioxidant Improved CONSTITUTIVE PHOTOMORPHOGENESIS 1 in the nucleus, which in turn decreases the expression of ABA-­ INSENSITIVE 5 and improves the degradation of HYPCOTYL 5 which stimulates the germination of seed under heat stress Upsurge the germination rate and growth of seedlings

References Cheng et al. (2018)

Zhou et al. (2018)

Chen et al. (2019)

Bao et al. (2011)

Wang et al. Alleviates the inhibition of seed (2012) germination and inhibition of seedling growth. The alleviation of oxidative damage occurs due to the increased activities of ascorbate peroxidase, guaiacol peroxidase, catalase, and superoxide dismutase (continued)

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Table 1 (continued) Type of stress

Plant Arabidopsis (Arabidopsis thaliana)

Maize (Zea mays L.)

Rice (Oryza sativa L.)

Wheat (Triticum aestivum L.)

Source of hydrogen sulfide 800μM sodium hydrosulfide

Stress response Sustaining a lower Na+/K+ ratio. The root growth inhibition was removed. The production of hydrogen peroxide is promoted which in turn regulates the activities of plasma membrane NADPH oxidase and glucose-6-­ phosphate dehydrogenase. Increase the genes expression and the phosphorylation level of H + -ATPase and Na+/H+ antiporter protein level. Ion hemostasis was maintained in a hydrogen peroxide dependent manner Maintain the redox conditions of 0.6 mM glutathione and ascorbate by sodium upregulating the glutathione and hydrosulfide ascorbate metabolism. Monodehydroascorbate reductase activity reduced and considerably decreases the electrolyte leakage and malondialdehyde content 50μM sodium Increase of soluble protein, hydrosulfide carotenoid, and chlorophyll contents as well as repressed the accretion of reactive oxygen species. Increased level of redox states, glutathione, and ascorbic acid as well as increases the activities of methylglyoxal and reactive oxygen species detoxifying enzymes. Decreases the uptake of Na+ and the Na+/K+ ratio Elimination of growth inhibition. 0.5 mM Decreases the Na+ efflux ratio, the sodium hydrosulfide selective absorption capacity for K+ over Na+, Na+/K+ ratio, and Na+ concentration as well as improved the selective transportability for K+ over Na+ under salinity stress

References Li et al. (2014)

Shan et al. (2014)

Mostofa et al. (2015)

Deng et al. (2016)

(continued)

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Table 1 (continued) Type of stress

Plant Cucumber (Cucumis sativus L.)

Mangrove plant (Kandelia obovata)

Drought

Broad bean (Vicia faba L.) Arabidopsis (Arabidopsis thaliana L. Heynh.) Impatiens (Impatiens walleriana Hook. f.) Soyabean (Glycine max L.)

Source of hydrogen sulfide Stress response 20μM sodium Alleviates growth inhibition, hydrosulfide eliminate the decrement of stomatal factors, chlorophyll fluorescence, and photosynthetic characteristics. The activity of β-cyanoalanine synthase and d/l-cysteine desulfhydrase was increased. Maintained K+ and Na+ homeostasis and alleviates salinity-induced oxidative stress as shown by the lowered the reactive oxygen species accretion and lipid peroxidation Improved lipid membrane stability 200μM and quantum efficiency of sodium photosystem II. Improved carbon hydrosulfide fixation, chlorophyll biosynthesis, and photosynthetic electron transfer rate. Ascorbate-glutathione cycle, triosephosphate isomerase, phosphoglycerate kinase, glutamine synthetase, chaperonin family protein, heat-shock protein, pancreatic and duodenal homeobox 1, copper/zinc superoxide dismutase, and ascorbic acid peroxidase were increased Encourages stomatal closure and 500μM improved leaf relative water content sodium hydrosulfide

0.1 mmol−1 sodium hydrosulfide

References Jiang et al. (2019)

Liu et al. (2019)

García-­ Mata and Lamattina (2010)

Zhang Increase the biomass of both root et al. and leaf. The decrease in (2010) chlorophyll content. Activities of catalase and superoxide dismutase increases. Lipoxygenases activity was decreased. Accumulation of superoxide anion, hydrogen peroxide, and malondialdehyde was delayed

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Table 1 (continued) Type of stress

Copper

Plant Strawberry (Fragaria × ananassa Duch.) Wheat (Triticum aestivum L.)

500μM sodium hydrosulfide

Wheat (Triticum aestivum L.) Alfalfa (Medicago sativa L.)

400μM sodium hydrosulfide Nitric oxide and hydrogen sulfide (NOSH) liberating compounds (100μM)

Wheat (Triticum aestivum L.)

Wheat (Triticum aestivum L.)

Cadmium

Source of hydrogen sulfide 100μM sodium hydrosulfide

Alfafa (Medicago sativa L.)

Desert poplar (Populus euphratica Olivier)

Stress response Increased leaf relative water, content, stomatal conductance, and leaf chlorophyll fluorescence as well as lower lipid peroxidation levels Improves the leaf relative water content and the height of plant seedlings. Increases the activities of antioxidant enzymes and decreases the hydrogen peroxide and malondialdehyde contents in both roots and leaves Stimulation of genes that code for antioxidant enzymes

Enhanced the recovery ensuing re-watering due to altered reactive oxygen species and nitrogen species metabolism and signaling, as well as reduction of cellular damage, as demonstrated by improved lipid peroxidation and proline accretion levels Low levels of malondialdehyde and 1400μM hydrogen peroxide contents in sodium germinating seeds. Upsurges hydrosulfide catalase and superoxide dismutase activities as well as reduces lipoxygenase 0.8μM sodium Protection against copper-induced hydrosulfide oxidative stress; enhanced capacity of antioxidants, improved stability of cellular membranes, Regulation of ascorbate-glutathione cycle; alleviation of oxidative stress Decreases the accretion of 100μM malondialdehyde and hydrogen sodium peroxide. Increase the content of hydrosulfide reduced glutathione and the activities of antioxidant enzymes such as peroxidase, catalase, and superoxide dismutase Enhanced the capacity of 200μM antioxidants such as glutathione sodium reductase, catalase, and ascorbate hydrosulfide peroxidase. Decrease the accumulation of lipid peroxidation and hydrogen peroxide accretion. Limiting cadmium accretion

References Christou et al. (2013)

Ma et al. (2016)

Li et al. (2017) Antoniou et al. (2010)

Zhang et al. (2008)

Shan et al. (2012)

Li et al. (2012a)

Sun et al. (2013)

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Table 1 (continued) Type of stress

Plant Bermudagrass (Cynodon dactylon L. Pers.)

Barley (Hordeum vulgare L.)

Wheat (Triticum aestivum L.)

Aluminum

Arabidopsis (Arabidopsis thaliana L. Heynh.) Rice (Oryza sativa L.)

Soybean (Glycine max L.)

Source of hydrogen sulfide 500μM sodium hydrosulfide

Stress response Alleviates reactive oxygen species burst, cell damage, and growth inhibition by modulating non-­ enzymatic and enzymatic antioxidants. Induces the production of hydrogen sulfide and nitric oxide Alleviation of decrement in 200μM chlorophyll content and growth sodium inhibition. Depressed the accretion hydrosulfide of malondialdehyde in leaves. Raised the superoxide dismutase in roots and leaves as well as a decrease in leaf ascorbate, catalase, and peroxidase activities. Accretion of superoxide ions and hydrogen peroxide in roots Increases the activities of 200μM antioxidant enzymes. Reduce sodium proline content and oxidative stress. hydrosulfide Increases plant dry matter, chlorophyll a and b contents Overexpression of d-CYSTEINE Endogenous DESULFHYDRASE decreases hydrogen cadmium and reactive oxygen sulfide species contents 2μM sodium Alleviates root elongation hydrosulfide inhibition triggered by aluminum toxicity. Reduction of -ve charge in cell walls by reducing the hemicellulose and pectin concentration as well as decreasing the activity of pectin methylesterase in roots. Antioxidant enzymes such as peroxidase, catalase, ascorbate peroxidase, and superoxide dismutase activities were increases. Reduces the malondialdehyde and hydrogen peroxide content in roots 50μM sodium The citrate transporter genes such hydrosulfide as GmMATE47 and GmMATE13 were characterized and identified in soybean plants which in turn. Mediated citrate secretion and enhanced aluminum resistance. Alleviates aluminum influenced inhibition of root elongation

References Shi et al. (2014)

Fu et al. (2019)

Kaya et al. (2020)

Zhang et al. (2020) Zhu et al. (2018)

Wang et al. (2019)

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Table 1 (continued) Type of stress Arsenic

Plant Pea (Pisum sativum L.)

Source of hydrogen sulfide 100μM sodium hydrosulfide

Iron deficiency

Strawberry (Fragaria × ananassa Duch.)

0.2 mM sodium hydrosulfide

Zinc

Pepper (Capsicum annuum L.)

200μM sodium hydrosulfide

Chromium

Arabidopsis (Arabidopsis thaliana L.Heynh.) Caulifower (Brassica oleracea L.)

Hydrogen sulfide fumigation 200μM sodium hydrosulfide

Cucumber (Cucumis sativus L.)

200μM sodium hydrosulfide

Boron

Stress response Increase nitric oxide and hydrogen sulfide. Decrease the concentration of reactive oxygen species and injury to membranes, proteins, and lipids. Increases the activity of the ascorbate-glutathione cycle Reduces hydrogen peroxide, malondialdehyde, and electrolyte leakage. Improved Fe uptake. Upregulate activities of antioxidant enzymes Improved the levels of proline and hydrogen sulfide, water status, fruit yield, and plant growth as well as the activities of different antioxidant enzymes, though it considerably repressed electrolyte leakage, malondialdehyde, and hydrogen peroxide contents Increased hydrogen sulfide accumulation and cysteine as well as improved seed germination Decreases chromium content as well as malondialdehyde, hydrogen peroxide, and electrolyte leakage contents. Increases the activity of antioxidant enzymes Reduced root growth inhibition; decrease in pectin methylesterase activity

References Singh et al. (2015)

Kaya and Ashraf (2019)

Kaya et al. (2018)

Fang et al. (2016)

Ahmad et al. (2020)

Wang et al. (2010)

UV-B radiation led to damage to metabolic pathways and cause oxidative stress (OS) (Nawkar et al. 2013; Rostami et al. 2019). The irreversible or reversible alterations of lipids, carbohydrates, polynucleic acids, and proteins were caused by OS (Gill and Tuteja 2010; Rostami et al. 2019). However, plants develop their defense to eliminate the damage caused by the exposure to UV-B radiation, which includes DNA repair by DNA photolyase as well as the accumulation of UV-absorbing phenolic compounds (Jenkins 2009; Rostami et al. 2019). Plants have also evolved a complex antioxidant defense mechanism comprising numerous metabolites as well as enzymes, to eliminate surplus ROS formed because of UV-B radiation (Hasanuzzaman et al. 2012; Rostami et al. 2019).

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In the aforementioned context, the investigation has been conducted in seedlings of barley plants, where upon exposure of UV-B induces the generation of H2S in the leaves. The maximum concentration of H2S recorded in the leaves was 230 nmol g−1 fresh weight after 12 h of exposure and increases the accumulation of UV-B protective compounds like anthocyanins and flavonoids. The accumulation of these secondary metabolites helps the plant to overcome the detrimental effects of UV-B radiations. The deterioration of ROS by these secondary metabolites may signify a usual approach for avoiding injury under UV-B radiation (Li et  al. 2016b). In another study, the sodium hydrosulfide was utilized by the Rostami et al. (2019) as a H2S donor for the elimination of impairment occurs due to the exposure of borage (Borago officinalis L.) to UV-B light. H2O2 content, protein oxidation, and lipid peroxidation were augmented in plants due to their exposure to UV-B radiation. Moreover, the activities of enzymatic systems like catalase, guaiacol peroxidase, and ascorbate peroxidase including reduced glutathione do not alter considerably in stressed plant systems over the control. However, the concentration of flavonoids was increased significantly. The treatment of plants with sodium hydrosulfide (120μM) before the exposure of the borage plant to UV-B radiation reduces the H2O2, carbonyl groups, and malondialdehyde content considerably. However, the guaiacol peroxidase and ascorbate peroxidase activities were increased and catalase activity was decreased. Moreover, in leaves, the concentration of reduced glutathione was increased. The exploration of flavonoids by HPLC revealed that pretreatment of the borage plant with sodium hydrosulfide caused a decrease in the concentration of flavonoids. This study advocates that H2S eliminates the damages caused by the exposure of borage seedlings to UV-B radiation via the improvement of reduced glutathione content and antioxidative enzyme activities.

5.2  H2S Alleviates Flooding Stress Flooding of lands causes stress in plants due to hypoxic conditions at roots which considerably reduces or decreases the land use and crop production (Bailey-Serres and Voesenek 2008). Tips of the plant root are very sensitive to hypoxia and perish within a few hours (Gladish et al. 2006) owing to the accretion of ROS/OS, acceleration of protein degradation, inhibition of protein synthesis, cytoplasmic pH drop, injury to plasma membranes, alterations in the fermentation of sugars, and deactivation of enzymes present in cytoplasm (Blokhina et  al. 2001; Kreuzwieser and Rennenberg 2014; Sauter 2013). To manage these deleterious consequences triggered by the waterlogging mediated hypoxic condition, plants can alter their metabolic pathways to prevent or metabolize the development of harmful end products to alter the process of fermentation to improve intracellular antioxidant capacity, produce stress tolerance proteins as well as repair of the cell membrane (Kennedy et al. 1992; Lakshmanan et al. 2013; Li et al. 2013a, b; Singaki-wells et al. 2014). The aforementioned context is supported by various studies/ investigations. For instance, Cheng et al. (2013) explored the impacts of H2S on the death of root tip in

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pea (Pisum sativum L.) plant due to the waterlogging induced hypoxic condition via examination of endogenous ROS and H2S concentration. The pretreatment of the plant by exogenous H2S (0.1 mM sodium hydrosulfide) eliminates root tip death due to hypoxia by defending root tip plasma membranes from the injury caused by ROS along with preventing the formation of ethylene and thus improves the acclimatization of the plant to hypoxic stress. Peng et al. (2016) investigated the effects of H2S on nitric oxide-mediated alleviation of hypoxia in maize (Zea mays L.) plants. The treatment of sodium nitroprusside as a source of nitric oxide increases the survival frequency of flooded roots of maize plants via the induced accretion of H2S endogenously. The H2S stimulates the level of Ca2+ and alcohol dehydrogenase activity, which improves the antioxidant defense activity results in the better adaptation of maize seedling to the hypoxic environment. The main enzymes accountable towards the formation of H2S in plants such as β-cyanoalanine synthase, O-acetyl-l-serine (thiol) lyase, and l-cysteine desulfhydrases were stimulated by nitric oxide. The tolerance of hypoxic conditions by sodium nitroprusside was improved by the treatment with 1 mM sodium hydrosulfide, but eliminated by the inhibitor of H2S such as hydroxylamine and H2S scavenger hypotaurine. This investigation advocates the nitric oxide-mediated alleviation of hypoxia in maize seedlings.

5.3  H2S Alleviates Temperature Stress Temperature is one of the vital ecological factors, which account for the progress as well as the growth of crops (Ashraf et al. 2010; Monjardino et al. 2005). The crops were exposed to the temperature stress once the nearby temperature is beyond (heat or high-temperature stress) or under (low-temperature or cold stress) the optimal values for growth. Both are unfavorable towards the growth and development of plants as they adjusted to grow in a narrow array of temperatures (Singh and Grover 2008). Moreover, man-made activities played an essential part in accelerating climate change and global warming effects by increasing CO2 together with other greenhouse gas levels in the atmosphere. This unfavorably affects cultivation through its indirect and direct consequences on crop productivity (Grover et al. 2013). Some investigations have been performed concerning the role of H2S in plants under temperature stress. For example, Fu et al. 2013 examined the role of H2S in the alleviation of cold stress in Vitis vinifera L. The result revealed the increment in the level of hydrogen sulfide, l- and d-cysteine desulfhydrase enzyme activities including the expression of l- and d-cysteine desulfhydrase gene. However, to examine the effects of exogenously applied hydrogen sulfide, the seedlings were treated at 4 °C with sodium hydrosulfide and hypotaurine. The results depicted the activity of superoxide dismutase and the expression of VvICE1 and VvCBF3 genes that were increased significantly. Nevertheless, the plasma membrane permeability, malondialdehyde content, and superoxide anion radicals were found to be low after

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the exposure of seedlings to sodium hydrosulfide. Moreover, the treatment with hypotaurine exhibited the opposite effect under cold stress. Likewise, Luo et  al. (2015) examined the impact of H2S exposure as a result of the treatment of banana fruit with 0.5  mM sodium hydrosulfide (donor of hydrogen sulfide) during cold storage. The results confirmed to maintain the greater values of lightness and peel firmness as well as decreased the accretion of malondialdehyde. Moreover, the antioxidant capacity, total phenolics content, and phenylalanine ammonia-lyase activity were stimulated. However, H2O2 and superoxide anion accumulation were decreased by H2S with the improved responses of glutathione reductase, ascorbate peroxidase, catalase, superoxide dismutase, and guaiacol peroxidase. Recently, Tang et  al. (2020) explored the influences of externally supplemented H2S by spraying leaves of blueberry with sodium hydrosulfide (0.5 mmol L−1) under low-temperature stress (4–6 °C). The carotenoid and chlorophyll content as well as photosystem I and II were suppressed under cold stress. The major consequences of cold stress include the membrane peroxidation owing to the accretion of H2O2 in the leaves. The exposure of blueberry to sodium hydrosulfide as a donor of hydrogen sulfide eliminates the degradation of carotenoids and chlorophyll content in leaves caused by the cold stress as well as decreases the photoinhibition of photosystem II and I. The possible explanation for the improvement of photochemical activities of photosystem II was the exogenously applied H2S stimulated the transfer of an electron from QA to QB in photosystem II acceptor under cold stress. The suspension-cultured cells of tobacco were pretreated with sodium hydrosulfide, which resulted in decreased malondialdehyde accumulation, elimination of increment in electrolyte leakage, and alleviation of reduction in cell vitality under temperature stress. Furthermore, the supplementation of externally Ca2+ together with its ionophore A23187 markedly increased the sodium hydrosulfide-induced temperature tolerance endurance in tobacco suspension-cultured cells (Li et al. 2012b). Li et al. (2013a, b) showed that the pretreatment of sodium hydrosulfide enhanced the survival rate of seedlings and germination rate of maize seeds during temperature stress. A reduction in the accretion of malondialdehyde in coleoptile and decrement in tissue vitality including the elimination of increment in the electrolyte leakage of roots were reported in heat stress exposed maize seedlings because of the pretreatment with sodium hydrosulfide. Furthermore, the activity of proline dehydrogenase was decreased, which allows the accretion of proline endogenously. On the other hand, the activity of ∆1-pyrroline-5-carboxylate synthetase was increased as a result of the pretreatment of sodium hydrosulfide, which resulted in the alleviation of heat stress. Christou et  al. (2014) found that the pretreatment of strawberry plant roots with sodium hydrosulfide (H2S donor) stimulated a synchronized network associated at a transcriptional level with heat-shock defense-related pathways and systematically defends the strawberry plants from thermo stress-induced damages. Further, the pretreatment of strawberry roots with sodium hydrosulfide activated the gene expression encoding for aquaporins, heat-shock proteins (such as HSP70, HSP80,

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and HSP90), and antioxidant enzymes (like cytosolic ascorbate peroxidase, catalase, manganese superoxide dismutase, and glutathione reductase). Li (2015a, b) examines the treatment of maize seedlings with sodium hydrosulfide as a H2S donor, which enhanced the salicylic acid (plant hormone) induced tolerance to heat stress. Moreover, the application of salicylic acid increased the l-cysteine desulfhydrase enzyme activity, which in turn helps in the accretion of H2S and enhanced the tolerance of maize seedlings to heat stress. The suspension-cultured cells of tobacco were pretreated with hematin (carbon monoxide donor), which resulted into a decrease of malondialdehyde accumulation and alleviation of reduction in cell vitality under temperature stress as well as an increase in the regrowth ability and survival rate of cells under heat stress. Furthermore, the application of exogenous hematin markedly increased l-cysteine desulfhydrase activity that accumulates H2S endogenously in tobacco cells. However, the application of sodium hydrosulfide as a H2S markedly increased the hematin-induced heat tolerance in tobacco suspension-­ cultured cells (Li and Gu 2016). The suspension-cultured cells of tobacco were pretreated with abscisic acid, which resulted into a decrease of malondialdehyde accumulation, elimination of enhancement in electrolyte leakage as well as alleviation of reduction in cell vitality as well as improved the regrowth ability and survival percentage under temperature stress. Moreover, the application of abscisic acid improved the l-cysteine desulfhydrase enzyme activity that helps in the accretion of H2S and improved the tolerance of tobacco cells under heat stress. However, the application of sodium hydrosulfide as a H2S markedly enhanced the abscisic acid-induced heat tolerance in tobacco suspension-cultured cells (Jin and Pei 2016). Cheng et al. (2018) found that heat stress mediated production of H2S in a poplar tree, which in turn stimulated the enzyme activity involved in H2S production. H2S alleviated the heat stress in the poplar tree by modulating the S-nitrosoglutathione reductase and nitric oxide signaling by preventing the damage in plants caused by ROS and reactive nitrogen species. Zhou et al. (2018) studied the pre-soaked seeds of maize with sodium hydrosulfide in which improved fresh weight, root length, sprout length, and germination percentage were observed over control. Furthermore, pre-soaked seeds of maize with sodium hydrosulfide improved the activities of antioxidant enzymes (such as catalase, superoxide dismutase, and so on) and non-­ enzymatic water-soluble antioxidants (such as glutathione and ascorbic acid) contents including the ratio of reduced antioxidant to oxidized antioxidant. Chen et al. (2019) investigated the Arabidopsis seeds germination rate under heat stress in which the H2S increases seed germination under thermo-stress. Besides, thermo-­ stress speeds up the efflux of the E3 ligase CONSTITUTIVE PHOTOMORPHOGENESIS 1 from the nucleus to the cytoplasm, which in turn increases nuclear accretion of ELONG HYPCOTYL 5 to trigger the activation of ABA-INSENSITIVE 5 and thus suppresses the germination of seed. Conversely, the H2S signal inverted the thermo-stress consequence, as categorized by improved CONSTITUTIVE PHOTOMORPHOGENESIS 1  in the nucleus, which in turn decreased the expression of ABA-INSENSITIVE 5 and improved the degradation of HYPCOTYL 5 that stimulates the germination of seed under heat stress.

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5.4  H2S Alleviates Salinity Stress Salinity stress is one of the chief ecological causes that unfavorably upset plant survival, productivity, as well as growth (Shan et al. 2014). Salinity stress generally encourages the excess formation of ROS in plant cells. Plants can defend themselves from the salinity stress-mediated damage caused by OS by ROS-foraging systems (Mittler 2002). Various investigations have been carried out pertaining to the abovementioned facts, where Bao et al. (2011) explored the impact of salt stress (100 mM NaCl) in wheat seedlings. In salt stress, the wheat seeding was treated with 0.13 mM sodium hydrosulfide for 12 h, which in turn improved the germination rate together with the growth of seedlings. Likewise, Wang et al. (2012) examined the treatment of salt (100 mM NaCl), sodium nitroprusside (100μM) as nitric oxide donor, and sodium hydrosulfide (100μM) as H2S donor alleviated the prevention of seed germination of alfalfa and inhibition of seedling growth. The alleviation of oxidative damage occurred due to the increased activities of ascorbate peroxidase, catalase, and so on. The protective roles of H2S could be due to the initiation of endogenous nitric oxide production. Li et  al. (2014) studied the exposure of sodium hydrosulfide in Arabidopsis root, which in turn eliminated the salinity stress by sustaining a lower Na+/K+ ratio. The root growth inhibition was removed by H2S under salinity stress. The production of H2O2 was promoted by the application of H2S that regulated the activities of plasma membrane NADPH oxidase and glucose-6-phosphate dehydrogenase. H2S also stimulated the gene expression and the phosphorylation level of H+-ATPase and Na+/H+ antiporter protein levels. Moreover, ion hemostasis was maintained in H2O2 dependent manner. Shan et al. (2014) explored the treatment of maize leaves with exogenous H2S on the redox situations of glutathione and ascorbate under salinity stress (100  mM NaCl). Salt stress improved the functions of l-galactono-1,4-lactone dehydrogenase, γ-glutamylcysteine synthetase, dehydroascorbate reductase, ascorbate monodehydroascorbate reductase, glutathione reductase, and peroxidase as well as electrolyte leakage and malondialdehyde content, and decreased the ratios of reduced and oxidized forms of glutathione and ascorbate over control. The pretreatment with sodium hydrosulfide promoted the functions of the mentioned enzymes excluding monodehydroascorbate reductase and considerably diminished the electrolyte leakage together with malondialdehyde content persuaded by the salinity stress. Mostofa et al. (2015) investigated rice (Oryza sativa L. cv. BRRI dhan52) upon pretreatment with H2S resulted in the increment of soluble protein, carotenoid, and chlorophyll contents as well as repressed the accretion of ROS that protect the plants from oxidative damages. The defense mechanism associated with H2S was connected with an enhanced level of redox states, glutathione, and ascorbic acid and increased the activities of methylglyoxal and ROS detoxifying enzymes. It also decreased the uptake of Na+ as well as the Na+/K+ ratio, thereby indicating a part of H2S in ion homeostasis under salinity stress. The outcome of the exogenous application of sodium hydrosulfide (0.05 mM) as a donor of H2S on the growth of Triticum aestivum L. (LM 15) seedling as well as K+ and Na+

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concentration and Na+ transportation under salinity (100  mM NaCl) stress were examined by Deng et al. (2016). The results showed the elimination of growth inhibition under salinity stress. Moreover, the pretreatment of sodium hydrosulfide decreased the Na+ efflux ratio, the selective absorption capacity for K+ over Na+, Na+/K+ ratio, and Na+ concentration, as well as improved the selective transportability for K+ over Na+ under salinity stress. Jiang et al. (2019) showed the adaptation of the cucumber plant to the salinity stress owing to H2S production endogenously, which alleviated salinity-induced growth inhibition and eliminated the decrement of stomatal factors, chlorophyll fluorescence, and photosynthetic characteristics. The activities of β-cyanoalanine synthase and d/l-cysteine desulfhydrase were increased under salinity stress that increased the production of H2S endogenously. Moreover, H2S maintained the K+ and Na+ homeostasis and alleviated salinity-induced OS as shown by the lower ROS accretion and lipid peroxidation. Liu et al. (2019) studied the influence of sodium hydrosulfide application on the alleviation of salinity stress in the mangrove species, Kandelia obovate, where decrease in photosynthesis triggered by 400 mM of NaCl was recuperated by the sodium hydrosulfide (200μM) application. Moreover, the treatment of H2S improved the lipid membrane stability and quantum efficiency of photosystem II, suggesting that H2S was advantageous to the persistence of mangrove species seedlings under high salt stress. The H2S improved the carbon fixation, chlorophyll biosynthesis, and photosynthetic electron transfer rate. Additionally, ascorbate-glutathione cycle, triosephosphate isomerase, phosphoglycerate kinase, glutamine synthetase, chaperonin family protein, heat-shock protein, pancreatic and duodenal homeobox 1, copper/zinc superoxide dismutase, and ascorbic acid peroxidase were increased by H2S under salt stress.

5.5  H2S Alleviates Drought Stress Drought stress is one of numerous ecological elements significantly accountable for restraining the distribution of plant and production of crops worldwide (Boyer 1982). Throughout drought stress, disturbance of cellular homeostasis is attended by the production of ROS, and the amount of drought stress-mediated injury can be diminished by the activation of the antioxidant systems of plant cells, comprising glutathione, ascorbate, and enzymes accountable for scavenging ROS (Zhang et al. 2010). In the aforementioned context, García-Mata and Lamattina (2010) investigated the ability of H2S to improve the plants (Impatiens walleriana, Arabidopsis thaliana, and Vicia faba) tolerance under drought stress conditions. The exposure of the plants (epidermal strips) to 500μM of sodium hydrosulfide as a donor of H2S encouraged stomatal closure and improved the leaf relative water content and defends the plants from drought stress. Zhang et al. (2010) examined the exposure of soybean (Glycine max L.) seedlings with sodium hydrosulfide, which increased the biomass of both root and leaf over the control under water-deficient condition. The decrement of chlorophyll content due to drought stress was alleviated by the

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exposure of H2S as a result of the increased activities of catalase and superoxide dismutase. However, the lipoxygenase activity was declined. Moreover, the accretion of superoxide anion, H2O2, and malondialdehyde was delayed. These results advocated that H2S could escalate the drought tolerance in Glycine max seedlings via performing as an antioxidant signal molecule. Christou et al. (2013) investigated the pretreatment of strawberry (Fragaria × ananassa cv. Camarosa) roots with a sodium hydrosulfide (100μM for 48  h) and exposure to 10% (w/v) polyethylene glycol-6000 for 7  days. H2S pretreatment of roots caused increased leaf relative water content, stomatal conductance, and leaf chlorophyll fluorescence as well as lower lipid peroxidation levels as compared to the plants exposed to non-ionic osmotic stress. Hence, this suggests an alleviating consequence of H2S pretreatment to cellular injury due to drought stress. Ma et al. (2016) studied the exogenous treatment of sodium hydrosulfide on wheat. This study showed considerable improvement towards the leaf relative water content with the height of plant seedlings under water scarcity stress. It also improved the activities of antioxidant enzyme and decreased the H2O2 and malondialdehyde contents in both roots and leaves of common wheat (Triticum aestivum L.) cultivar “Yumai49-198.” Moreover, the pretreatment of sodium hydrosulfide increased the abscisic acid production level and abscisic acid reactivation genes in leaves; however, the expression levels of abscisic acid production and catabolism genes were upregulated in roots. Therefore, the results indicated that the production of abscisic acid by H2S contributes to drought stress alleviation. Li et al. (2017) depicted that the H2S eliminates the injury caused by drought stress in wheat possibly associated with amino acids and fatty acids metabolism, protein processing pathway, plant hormones signal transduction, and transport systems. Recently, Antoniou et al. (2010) investigated the possible synergistic consequence of nitric oxide and H2S (NOSH) liberating compounds in Medicago sativa under drought stress. Plants were initially pretreated via foliar spraying with NOSH and NOSH-aspirin and then exposed to a moderate water deficit condition. The results depicted the adaptation of the plant to drought stress and enhanced the recovery, resulting in re-watering due to altered ROS and nitrogen species metabolism and signaling, as well as reduction of cell injury, as demonstrated by improved lipid peroxidation as well as proline accretion levels.

5.6  H2S Alleviates Metal Stress Soil pollution is one of the severe issues that the global agriculture industries are facing, which in turn causes metal stress in plants and therefore reduces their productivity. The main activity responsible for polluting the soil includes the usage of metal products mining, sewage irrigation, and exhaust emissions. Due to man-made activities, the concentration of the metals in the environment is much above the normal range, ensuing the worsening of ecosystem health and ecological feature. Generally apprehensive metals include lead, chromium, arsenic, aluminum, cadmium, zinc, and copper. Surplus acquaintance to metals constrains seed germination and seedling growth, damages membrane and antioxidant enzymes system, and

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prompt chromosome aberration, which are in turn accountable for plant death. Moreover, metal ions also hinder plant metabolic pathways by encouraging secondary stress such as oxidative stress, a large number of free radicals, and nutrient imbalance. The features of metallic stress are root damage and accretion toxicity. Because of the diversity of metals, the consequences of metal stress are connected with the duration of treatment, metal types, injured tissue, and plant species. The features of soil such as redox potential, organic matter, clay, and pH control the bioavailability, mobility, and solubility of metals. The harmfulness of metal impurities to plants conveys ecological jeopardies (Hooda 2010; Huyi et al. 2018). Considering the abovementioned facts, Zhu et al. (2018) investigated the role of pretreatment of rice (Oryza sativa L.) with sodium hydrosulfide (2μM) as a H2S donor, which relieved the root elongation prevention triggered by aluminum toxicity in roots. This happened due to the reduction of negative charge on cell walls by diminishing the hemicellulosic as well as pectin concentration as well as decreasing the activity of pectin methylesterase in rice roots. Besides, antioxidant enzymes like responses of peroxidase, catalase, etc., were enhanced with the pretreatment of sodium hydrosulfide that considerably reduces the malondialdehyde and H2O2 concentration in rice roots, thus decreasing the injury of aluminum toxicity on membrane integrity in rice. However, H2S displayed cross talk with nitric oxide pertaining to aluminum toxicity, as well as by decreasing the nitric oxide concentration in root tips to relieve aluminum toxicity. In separate investigations, Wang et  al. (2019) proved that H2S was a potent signaling molecule involved in plant adaptation to different stresses. The citrate transporter genes such as GmMATE47 and GmMATE13 were characterized and identified in soybean plants. Functional analysis of transgenic Arabidopsis revealed that GmMATE47 and GmMATE13 arbitrated citrate secretion and enhanced aluminum resistance. Aluminum exposure initiated H2S production and citrate exudation in the roots of soybean. The pretreatment with 50μM sodium hydrosulfide considerably raised aluminum prompted citrate secretion, decreased aluminum accretion in root tips, and alleviated aluminum-persuaded inhibition of root elongation. Singh et  al. (2015) explored the role of H2S in the alleviation of arsenate toxicity in pea (Pisum sativum L.) seedling. The arsenate stress in plants causes a reduction in nitrogen content, photosynthesis, and growth as well as decreases the cysteine nitrate reductase and desulfhydrase activities and contents of nitric oxide and hydrogen sulfide. Conversely, exposure of 100μM sodium hydrosulfide alleviated arsenate toxicity in pea seedlings, which was associated with the increment in the concentration of nitric oxide and hydrogen sulfide. H2S alleviated the causes of the damage by arsenate toxicity by decreasing the concentration of ROS and injury to membranes, proteins, and lipids. Moreover, H2S increased the activity of the ascorbate-glutathione cycle in pea seedling. Kaya and Ashraf (2019) investigated the effects of sodium hydrosulfide as a contributor of H2S on strawberry seedlings under iron deficiency. The sodium hydrosulfide was applied exogenously by spraying sodium hydrosulfide solution (0.2 mM) to plant leaves. Strawberry plants displayed leaf interveinal chlorosis under iron deficiency. However, such symptoms were overcome by foliar use of sodium hydrosulfide.

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Sodium hydrosulfide improved chlorophyll contents, accessible iron as well as iron enhancement in young leaves. The levels of H2O2, malondialdehyde, and electrolyte leakage increased in plant leaves under iron deficiency. Exogenously applied sodium hydrosulfide decreased the accumulation of H2O2, malondialdehyde, and electrolyte leakage and upregulated the activities of key antioxidant enzymes. Therefore, sodium hydrosulfide demonstrated to be operative in overcoming chlorosis triggered by the iron deficit. Kaya et al. (2018) explored the effect of H2S on growth, main oxidants like H2O2, mineral elements as well as antioxidative defense in pepper plants exposed to the high content of zinc. The high concentration of zinc resulted in decreased relative water content, leaf maximum fluorescence, fruit yield, chlorophyll pigments, and dry mass, but improved endogenous hydrogen sulfide, electrolyte leakage, malondialdehyde, free proline, and H2O2 as well as the responses of superoxide dismutase, catalase, and peroxidase. Exogenously added sodium hydrosulfide considerably improved the levels of proline and hydrogen sulfide, water status, fruit yield, and plant growth as well as the responses of diverse antioxidant enzymes. Though it considerably repressed electrolyte leakage, malondialdehyde, and H2O2 concentrations in the pepper plants getting low-level zinc. High zinc establishment led to increasing intrinsic zinc levels in the roots and leaves; nevertheless, it depressed leaf iron, phosphorus, and nitrogen concentrations. However, sodium hydrosulfide reduced the zinc concentration and enhanced the nitrogen and iron contents in leaf and root organs. It can be established that sodium hydrosulfide could alleviate the damaging effects of zinc on plant growth mainly by sinking the content of zinc, H2O2, electrolyte leakage, and malondialdehyde, and improving the responses of enzymatic antioxidants with levels of important nutrients in pepper plants. Fang et al. (2016) investigated the effects of H2S fumigation in Arabidopsis thaliana under chromium stress, which resulted in increased cysteine and H2S accumulation as well as improved seed germination. Recently, Ahmad et al. (2020) studied the physiological and biochemical mechanisms through which externally supplemented sodium hydrosulfide mitigates chromium stress in cauliflower. The exposure of chromium reduced gas exchange parameters and enzymatic antioxidants, chlorophyll contents, growth, and biomass. Chromium stress improved the production of malondialdehyde, H2O2, and electrolyte leakage contents, and increased chromium content in the flowers, leaf, stem, and roots. Externally supplemented H2S improved the biochemical and physiological features of chromium-­ stressed cauliflower. H2S decreased chromium content in different parts of chromium-stressed plants, although it augmented the gas exchange attributes and chlorophyll contents. H2S decreases the malondialdehyde, H2O2, and electrolyte leakage contents, improving the antioxidant enzyme activities in chromium-stressed leaves and roots over the chromium treatments alone, suggesting hydrogen as a possible applicant in decreasing chromium toxicity in cauliflower and other crops. Boron is a vital micro-nutrient for plants, which when present in excess in the growth medium, turns out to be toxic to plant systems. Rapid prevention of root elongation is one of the utmost distinctive symptoms of boron toxicity. In this context, Wang et al. (2010) examined the role of H2S in boron toxicity in cucumber

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(Cucumis sativus) seedlings. The inhibitory effect of boron on root elongation was considerably relieved by the usage of sodium hydrosulfide. This caused a reduction in root growth inhibition, as well as a decreased in pectin methylesterase activity.

6  Conclusions H2S is associated with the metabolism of sulfur in plants whose function based on redox interactions, particularly the protein post-translational modification persulfidation. The pretreatment of sodium hydrosulfide as a H2S donor, comprising a signaling apparatus, which in turn increases several components associated with the antioxidant system at both protein and gene levels  in plants. However, both the mechanisms (molecular and biochemical) involved in these progressions are requisite to be further explored in the upcoming investigation. Nevertheless, the exposure of different species of plants with H2S exogenously has an advantageous outcome, particularly those of significant agronomic concern under hostile ecological situations. The usage of H2S alone and/or in combination with different substances (i.e., calcium, chitosan, silicon, thiourea, melatonin, and nitric oxide) appeared to have beneficial impact on crop plants. Therefore, it is essential to explore the same in the light of climatic change. Further, the supplementary investigation is essential to interpret the other aspects of H2S and its association with the metabolism of ROS and reactive nitrogen and sulfur species during functional and unfavorable environmental conditions, i.e., adverse environments along with the inventions of biotechnological approaches to alleviate environmental stresses.

References Ahmad R, Ali S, Rizwan M, Dawood M, Farid M, Hussain A, Wijaya L, Alyemeni MN, Ahmad P (2020) Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiol Plant 168:289–300 Álvarez C, Calo L, Romero LC, Garcıá I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669 Álvarez C, García I, Moreno I, Pérez-Pérez ME, Crespo JL, Romero LC, Gotor C (2012) Cysteine-­ generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634 Antoniou C, Xenofontos R, Chatzimichail G, Christou A, Kashfi K, Fotopoulos V (2010) Exploring the potential of nitric oxide and hydrogen sulfide (NOSH)-releasing synthetic compounds as novel priming agents against drought stress in Medicago sativa plants. Biomol Ther 10:E120 Ashraf M, Afzal M, Ahmad R, Maqsood MA, Shahzad SM, Aziz A, Akhtar N (2010) Silicon management for mitigating abiotic stress effects in plants. Plant Stress 4:104–114 Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol:313–339 Bao J, Ding TL, Jia WJ, Wang LY, Wang BS (2011) Effect of exogenous hydrogen sulfide on wheat seed germination under salt stress. Mod Agric Sci Technol 20:40–42

Functions of Hydrogen Sulfide in Plant Regulation and Response to Abiotic Stress

351

Blokhina OB, Chirkova TV, Fagerstedt KV (2001) Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot 52:1179–1190 Boyer JS (1982) Plant productivity and environment. Science 218:443–448 Bray AB, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stress. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiol, Rockville, pp 1158–1203 Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41:72–78 Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493 Chen Z, Huang Y, Yang W, Chang G, Li P, Wei J, Yuan X, Huang J, Hu X (2019) The hydrogen sulfide signal enhances seed germination tolerance to high temperatures by retaining nuclear COP1 for HY5 degradation. Plant Sci 285:34–43 Cheng T, Shi J, Dong Y, Ma Y, Peng Y, Hu X, Chen J (2018) Hydrogen sulfide enhances poplar tolerance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen damage. Plant Growth Regul 84:11–23 Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286 Christou A, Filippou P, Manganaris GA, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14:42 Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966 Corpas FJ (2019) Nitric oxide and hydrogen sulfide in higher plants under physiological and stress conditions. Antioxidants 8:457 da-Silva CJ, Modolo LV (2017) Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity. Acta Botanica Brasilica 32:150–160 Deng YQ, Bao J, Yuan F, Liang X, Feng ZT, Wang BS (2016) Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content. Plant Growth Regul 79:391–399 Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8:e62048 Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: Changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57 Fang HH, Liu ZQ, Jin Z, Zhang LP, Liu DM, Pei YX (2016) An emphasis of hydrogen sulfide-­ cysteine cycle on enhancing the tolerance to chromium stress in Arabidopsis. Environ Pollut 213:870–877 Fu MM, Dawood M, Wang NH, Wu F (2019) Exogenous hydrogen sulfide reduces cadmium uptake and alleviates cadmium toxicity in barley. Plant Growth Regul 89:227–237 Fu P, Wang W, Hou L, Liu X (2013) Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc Bot Pol 82:295 García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984 Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930 Gladish DK, Xu JP, Niki T (2006) Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Ann Bot 97:895–902

352

S. Sonkar et al.

Grover A, Mittal D, Negi M, Lavania D (2013) Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci 205–206:38–47 Hasanuzzaman M, Hossain MA, da Silva J, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress, antioxidant defense is a key factor. In: Venkateswarlu B, Shanker AK, Shanker C, Maheswari M (eds) Crop stress and its management, perspectives and strategies. Springer, Rijeka, pp 261–315 He H, Li Y, He LF (2018) The central role of hydrogen sulfide in plant responses to toxic metal stress. Ecotoxicol Environ Safety 157:403–408 Hooda PS (2010) Assessing bioavailability of soil trace elements. In: Hooda PS (ed) Trace elements in soils. Wiley, UK, pp 229–265 Husen A (2010) Growth characteristics, physiological and metabolic responses of teak (Tectona grandis Linn. f.) clones differing in rejuvenation capacity subjected to drought stress. Silva Gene 59:124–136 Husen A, Iqbal M, Khanum N, Aref IM, Sohrab SS, Meshresa G (2019) Modulation of salt-stress tolerance of niger (Guizotia abyssinica), an oilseed plant, by application of salicylic acid. J Environ Biol 40:94–104 Husen A, Iqbal M, Sohrab SS, Ansari MKA (2018) Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.). Agri Food Secur 7:44 Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49:867–877 Huyi H, Yingqiu L, Long-Fei H (2018) The central role of hydrogen sulfide in plant responses to toxic metal stress. Ecotoxicol Environ Safety 157:403–408 Iqbal MS, Singh AK, Ansari MI (2020a) Effect of drought stress on crop production. In: Rakshit A, Singh H, Singh A, Singh U, Fraceto L (eds) . Springer, New frontiers in stress management for durable agriculture, pp 35–47 Iqbal MS, Singh AK, Singh SP, Ansari MI (2020b) Nanoparticles and plant interaction with respect to stress response. In: Singh VK, Tripathi DK (eds) Bhushan I. Springer, Nanomaterials and environmental biotechnology, pp 1–15 Jain P, Pandey B, Singh P, Singh R, Singh SP, Sonkar S, Gupta R, Rathore SS; Singh AK (2021) Plant Performance and Defensive Role of Glycine Betaine Under Environmental Stress. In: Husen A (ed) Plant Performance Under Environmental Stress. Springer (In Press) Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431 Jiang JL, Tian Y, Li L, Yu M, Hou RP, Ren XM (2019) H2S alleviates salinity stress in cucumber by maintaining the Na+/K+ balance and regulating H2S metabolism and oxidative stress response. Front Plant Sci 10:678 Jin ZP, Pei YX (2016) Hydrogen sulfide: the shutter button of stomata in plants. Sci China Life Sci 59:1187–1188 Kataria S, Jajoo A, Guruprasad KN (2014) Impact of increasing Ultraviolet-B (UV-B) radiation on photosynthetic processes. J Photochem Photobiol B: Biol 137:55–66 Kaya C, Ashraf M (2019) The mechanism of hydrogen sulfide mitigation of iron deficiency-­ induced chlorosis in strawberry (Fragaria × ananassa) plants. Protoplasma 256:371–382 Kaya C, Ashraf M, Akram NA (2018) Hydrogen sulfide regulates the levels of key metabolites and antioxidant defense system to counteract oxidative stress in pepper (Capsicum annuum L.) plants exposed to high zinc regime. Environ Sci Pollut Res Int 25:12612–12618 Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol Plant 168:345–360 Kennedy RA, Rumpho ME, Fox TC (1992) Anaerobic metabolism in plants. Plant Physiol 100:1–6 Khan MIR, Khan N (2017) Reactive oxygen species and antioxidant system in plants: role and regulation under abiotic stress. Springer Nature, New York

Functions of Hydrogen Sulfide in Plant Regulation and Response to Abiotic Stress

353

Khan MIR, Khan NA, Masood A, Per TS, Asgher M (2016) Hydrogen peroxide alleviates nickel-­ inhibited photosynthetic responses through increase in use-efficiency of nitrogen and sulfur, and glutathione production in mustard. Front Plant Sci 7:44 Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259 Lakshmanan M, Zhang Z, Mohanty B, Kwon JY, Choi HY, Nam HJ, Kim DI, Lee DY (2013) Elucidating rice cell metabolism under flooding and drought stresses using flux-based modeling and analysis. Plant Physiol 162:2140–2150 Li H, Li M, Wei X, Zhang X, Xue R, Zhao Y, Zhao H (2017) Transcriptome analysis of drought-­ responsive genes regulated by hydrogen sulfide in wheat (Triticum aestivum L.) leaves. Mol Gen Genomics 292:1091–1110 Li J, Jia H, Wang J, Cao Q, Wen Z (2014) Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-­ dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251:899–912 Li L, Wang Y, Shen W (2012a) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631 Li Q, Wang Z, Zhao Y, Zhang X, Zhang S, Bo L, Wang Y, Ding Y, An L (2016b) Putrescine protects hulless barley from damage due to UV-B stress via H2S- and H2O2-mediated signaling pathways. Plant Cell Rep 35:1155–1168 Li ZG (2015a) Analysis of some enzymes activities of hydrogen sulfide metabolism in plants. Methods Enzymol 555:253–269 Li ZG (2015b) Synergistic effect of antioxidant system and osmolyte in hydrogen sulfide and salicylic acid crosstalk-induced heat tolerance in maize (Zea mays L.) seedlings. Plant Signal Behav 10:e1051278 Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747 Li ZG, Gong M, Xie H, Yang L, Li J (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 18:185–189 Li ZG, Gu SP (2016) Hydrogen sulfide as a signal molecule in hematin-induced heat tolerance of tobacco cell suspension. Biol Plant 60:595–600 Li ZG, Jin JZ (2016) Hydrogen sulfide partly mediates abscisic acid-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells. Plant Cell Tiss Org 125:207–214 Li Z-G, Min X, Zhou Z-H (2016a) Hydrogen sulfide: a signal molecule in plant cross-adaptation. Front Plant Sci 7:1621 Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572 Liu YL, Shen ZJ, Simon M, Li H, Ma DN, Zhu XY, Zheng HL (2019) Comparative proteomic analysis reveals the regulatory effects of H2S on salt tolerance of mangrove plant Kandelia obovata. Int J Mol Sci 21:E118 Luo Z, Li D, Du R, Mou W (2015) Hydrogen sulfide alleviates chilling injury of banana fruit by enhanced antioxidant system and proline content. Sci Hort 183:144–151 Ma D, Ding H, Wang C, Qin H, Han Q, Hou J, Lu H, Xie Y, Guo T (2016) Alleviation of drought stress by hydrogen sulfide is partially related to the abscisic acid signaling pathway in wheat. PLoS One 11:e0163082 Misra V, Mall AK, Al-Khayri JM, Singh AK, Ansari MI (2021) Involvement of Membrane transporters in drought tolerance. In: Roychoudhury A, Tripathi D, Deshmukh R (eds) Transporters and Plant Osmotic Stress. Elsevier (In Press) Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410 Monjardino P, Smith AG, Jones RJ (2005) Heat stress effects on protein accumulation of maize endosperm. Crop Sci 45:1203–1210

354

S. Sonkar et al.

Mostofa MG, Saegusa D, Fujita M, Tran LS (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na(+)/K(+) balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:1055 Nawkar GM, Maibam P, Park JH, Sahi VP, Lee SY, Kang CH (2013) UV induced cell death in plants. Int J Mol Sci 14:1608–1628 Olas B (2014) Hydrogen sulfide in signaling pathways. Clin Chim Acta 15:212–218 Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants - from the field to the test tube and back. Plant Biol 9:582–588 Peng R, Bian Z, Zhou L, Chen W, Hai N, Yang C, Yang T, Wang X, Wang C (2016) Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.). Plant Cell Rep 35:2325–2340 Porwal P, Sonkar S, Singh AK (2021) Plant Stress Enzymes Nanobiotechnology. In: Al-Khayri JM, Ansari MI, Singh AK (eds) Nanobiotechnology: Mitigation of Abiotic Stress in Plants. Springer (In Press) Prasad R, Bhattacharyya A, Nguyen QD (2017) Nanotechnology in sustainable agriculture: recent developments, challenges, and perspectives. Front Microbiol 8:1014 Rani H, Gupta R, Ansari MI, Singh AK (2020) Impact of Bioengineered Copper Quantum Dots on Germination, Photosynthetic Pigment and Antioxidant Response in Chick-pea under Dark Stress Environment. Res J Biotech 15:120–130 Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509 Rostami F, Nasibi F, Kalantari KM (2019) Alleviation of UV-B radiation damages by sodium hydrosulfide (H2S donor) pre-treatment in Borage seedlings. J Plant Interact 14:519–524 Sauter M (2013) Root responses to flooding. Curr Opin Plant Biol 16:282–286 Shan C, Dai H, Sun Y (2012) Hydrogen sulfide protects wheat seedlings against copper stress by regulating the ascorbate and glutathione metabolism in leaves. Aust J Crop Sci 6:248 Shan C, Liu H, Zhao L, Wang X (2014) Effects of exogenous hydrogen sulfide on the redox states of ascorbate and glutathione in maize leaves under salt stress. Biol Plant 58:169–173 Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107 Singaki-Wells R, Millar AH, Whelan J, Narsai R (2014) What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation. Plant Cell Environ 37:2260–2277 Singh A, Grover A (2008) Genetic engineering for heat tolerance in plants. Physiol Mol Biol Plants 14:155–166 Singh AK, Sharma L, Mallick N (2004) Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga, Chlorella. Ecotoxicol Environ Saf 59:223–227 Singh S, Husen A (2019) Role of nanomaterials in the mitigation of abiotic stress in plants. In: Husen A, Iqbal M (eds) Nanomaterials and plant potential. Springer, Cham, pp 441–471 Singh S, Husen A (2020) Behavior of agricultural crops in relation to nanomaterials under adverse environmental conditions. In: Husen A, Jawaid M (eds) Nanomaterials for agriculture and forestry applications. Elsevier Inc., Cambridge, MA, pp 219–256 Singh VP, Singh S, Kumar J, Prasad SM (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate glutathione cycle: Possible involvement of nitric oxide. J Plant Physiol 181:20–29 Sonkar S, Pandey B, Rathore SS, Sharm L, Singh AK (2021a) Applications of Nanobiotechnology in Overcoming Temperature Stress. In: Al-Khayri JM, Ansari MI, Singh AK (eds) Nanobiotechnology: Mitigation of Abiotic Stress in Plants. Springer (In Press) Sonkar S, Sharma L, Singh RK, Pandey B, Rathore SS; Singh AK; Porwal P; Singh SP (2021b) Plant Stress Hormones Nanobiotechnology. In: Al-Khayri JM, Ansari MI, Singh AK (eds) Nanobiotechnology: Mitigation of Abiotic Stress in Plants. Springer (In Press)

Functions of Hydrogen Sulfide in Plant Regulation and Response to Abiotic Stress

355

Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74 Tang X, An B, Cao D, Xu R, Wang S, Zhang Z, Liu X, Sun X (2020) Improving photosynthetic capacity, alleviating photosynthetic inhibition and oxidative stress under low temperature stress with exogenous hydrogen sulfide in blueberry seedlings. Front Plant Sci 11:108 Ulm R, Nagy F (2005) Signalling and gene regulation in response to ultraviolet light. Curr Opin Plant Biol 8:477–482 Wang B-L, Shi L, Li Y-X, Zhang W-H (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231:1301–1309 Wang H, Ji F, Zhang Y, Hou J, Liu W, Huang J, Liang W (2019) Interactions between hydrogen sulphide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminium toxicity. Plant Cell Environ 42:2340–2356 Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896 Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14 Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119 Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529 Zhang H, Hu SL, Zhang ZJ, Hu LY, Jiang CX, Wei ZJ, Wei ZJ, Liu J, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257 Zhang H, Jiao H, Jiang CX, Wei ZJ, Luo JP, Jones RL (2010) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32:849–857 Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094 Zhang Q, Cai W, Ji TT, Ye L, Lu YT, Yuan TT (2020) WRKY13 enhances cadmium tolerance by promoting D-CYSTEINE DESULFHYDRASE and hydrogen sulfide production. Plant Physiol 183:345–357 Zhou ZH, Wang Y, Ye XY, Li ZG (2018) Signaling molecule hydrogen sulfide improves seed germination and seedling growth of maize (Zea mays L.) under high temperature by inducing antioxidant system and osmolyte biosynthesis. Front Plant Sci 9:1288 Zhu CQ, Zhang JH, Sun LM, Zhu LF, Abliz B, Hu WJ, Zhong C, Bai ZG, Sajid H, Cao XC, Jin QY (2018) Hydrogen sulfide alleviates aluminum toxicity via decreasing apoplast and symplast al contents in rice. Front Plant Sci 9:294 Zou H, Zhang NN, Pan Q, Zhang JH, Chen J, Wei GH (2019) Hydrogen sulfide promotes nodulation and nitrogen fixation in soybean-rhizobia symbiotic system. Mol Plant-Microbe Interact 32:972–985

Silicon and Plant Responses Under Adverse Environmental Conditions Pankaj S. Mundada, Suchita V. Jadhav, Supriya S. Salunkhe, Swati T. Gurme, Suraj D. Umdale, Rajkumar B. Barmukh, Tukaram D. Nikam, and Mahendra L. Ahire

1  Introduction Food security is the most important fundamental need of society. The wide-ranging increase in environmental damage and the pressure of ever-increasing human population have adversely affected global food production (Etesami and Jeong 2018). The world population today is estimated to be about 7 billion and projected to reach between 7.5 to 10.5 billion by 2050 (Godfray et al. 2010). Such an enormous rise in the population would demand higher agricultural productivity per unit area from already degraded lands. Moreover, climate change has aggravated the occurrence and intensities of various biotic and abiotic stresses (Etesami and Jeong 2018). Such P. S. Mundada Department of Botany, Savitribai Phule Pune University, Pune, Maharashtra, India Department of Biotechnology, Yashavantrao Chavan Institute of Science (Autonomous), Satara, Maharashtra, India S. V. Jadhav · S. S. Salunkhe · S. T. Gurme Department of Biotechnology, Yashavantrao Chavan Institute of Science (Autonomous), Satara, Maharashtra, India S. D. Umdale Department of Botany, Jaysingpur College (Affiliated to Shivaji University), Jaysingpur, Maharashtra, India R. B. Barmukh Post Graduate Research Centre, Department of Botany, Modern College of Arts, Science and Commerce (Autonomous), Shivajinagar, Pune, Maharashtra, India T. D. Nikam Department of Botany, Savitribai Phule Pune University, Pune, Maharashtra, India M. L. Ahire (*) Department of Botany, Yashavantrao Chavan Institute of Science (Autonomous), Satara, Maharashtra, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. Husen (ed.), Plant Performance Under Environmental Stress, https://doi.org/10.1007/978-3-030-78521-5_14

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conditions would compel farmers to cultivate marginal lands and poor soils (Glick 2014). Stress affects the growth and development of the plants, thereby leading to more significant losses in agricultural productivity. However, plants have adopted numerous mechanisms to tolerate stress and survive stress-induced conditions. Healthy plants are capable of combating stress, and plant nutrients are vital to maintaining healthy plant growth. The microelements or micronutrients are known to give stress tolerance to plants (Vanderschuren et al. 2013; Bradáčová et al. 2016). Though the roles of several macro- and micronutrients in plants have been well documented, few of the nutrient elements have remained neglected. This chapter focuses on the role of silicon, one of the neglected plant nutrients, and its role in plants suffering from adverse environmental conditions.

2  Adverse Environmental Conditions 2.1  Biotic Stress Throughout their life, plants get exposed to a multitude of stresses that modify plant growth and development. Organisms like fungi, bacteria, mycoplasma, insets, nematodes, weeds, and parasitic plants induce biotic stress. The viruses and viroids, though nonliving, also contribute to the biotic stress. These agents affect the plant growth and development by depriving nutrients leading to reduced plant vigor and death of plants in extreme cases (Das and Rakshit 2016). The severity of biotic stress depends on the environmental factors, cropping systems, types of crops, cultivars, and resistance levels of plants. Hot and humid conditions and poor crop management practices are the two leading causes of biotic stresses (Pantazi et al. 2020). Early recognition of biotic stress is the key to control it via integrated pest management and the use of pesticides. Plants do not have an adaptive immune system like vertebrates. They can neither adapt to new diseases nor memorize the previous infections. However, plants have developed several mechanisms to combat biotic stresses. They rely on various physical and chemical barriers that confer strength and rigidity to survive under biological stress.

2.2  Abiotic Stress The nonliving factors imposing adverse effects on healthy growth and development of the plants are called abiotic stresses. These include drought, salinity, heavy metals, too low or too high temperatures, and other environmental extremes. These factors can reduce the crop yield by 51–82% (Bray et al. 2000). Plants combat these

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stresses at various levels like morphological, physiological, biochemical, and molecular levels (Husen 2010; Getnet et al. 2015; Embiale et al. 2016; Husen et al. 2016, 2018, 2019; Hussein et al. 2017; Siddiqi and Husen 2017, 2019; Zeng et al. 2020; Kar and Öztürk 2020). Over the past few decades, advances in plant physiology, genetics, and molecular biology have greatly upgraded our understanding in terms of crops respond to stress conditions. These responses depend not only on their duration and severity but on the age and the developmental stage of the plant as well (He et al. 2018).

3  Is Silicon Essential to Plants? Silicon (Si) is the eighth-most abundant element in the universe. In earth’s crust, its abundance ranks only second to oxygen. The lithosphere contains about 27.7% silicon (Epstein 1999). It rarely occurs in its pure form, and more than 90% of the Si in the earth’s crust exists as silicates (Mitra 2015). Biological systems also contain significant amounts of silicon, as amorphous silica (SiO2·nH2O), and its soluble form, silicic acid (Si(OH)4). The first indication of in vivo formation of organosilicates, their distribution, and physiological importance was discovered in a diatom Navicula pelliculosa (Kinrade et al. 2002). Plants also contain significant amounts of Si that can range from 0.1 to 10% on the dry weight basis (Epstein 1994; Ma and Takahashi 2002; Hodson et al. 2005; Ma et al. 2006). Differences in the levels of silicon in different plants could be due to the differential ability of roots to absorb Si (Takahashi et  al. 1990). Despite its high amounts in plants, Si is looked upon as a quasi-essential element since most of the plant species can live their entire life in the absence of silicon (Arnon and Stout 1939). Nonavailability of Si-free environment due to its contamination in purified water, chemicals, and dust might be the reasons for considering Si as nonessential for higher plants (Liang et al. 2015). Therefore, adhering to the definition of essentiality proposed by Epstein and Bloom (2005), Si is a quasi-essential element in plants. Interestingly, there are several reports on the positive roles of Si in the plant growth (Eneji et  al. 2008; Soundararajan et  al. 2014; Zhang et  al. 2015), yield (Epstein 1999), structural toughness (Epstein 1994), nutrient management (Tripathi et al. 2012), and absorption of light (Li et al. 2004). Its role in accelerating the tolerance to biotic and abiotic stresses in plants has also been explained (Ma 2004; Cookson et al. 2007; Liang et al. 2007; Muneer et al. 2014; Soundararajan et al. 2014). How Si alleviates biotic and abiotic stresses has become a booming topic of interest. In the past 15 years, several researchers have reported and reviewed the positive effects of Si under biotic and abiotic stresses (Fig. 1a, b). However, studies on Si in conjunction with abiotic stress were significantly more than those with biotic stress (Fig. 1b). This chapter summarizes how plants use silicon and respond to Si availability during adverse environmental conditions.

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Fig. 1 (a) Silicon-related publications in the plant sciences from 2005 to 2020 (Till June) (Based on PubMed search with the keywords “silicon” and “abiotic stress”). (b) Silicon-related publications in the plant sciences from 2005 to 2020 (Till June) (based on PubMed search with the keywords “silicon” and “biotic stress”)

4  U  ptake of Si in Plants Under Adverse Environmental Conditions In plants, roots take up more than 90% of Si and translocate it to shoots (Ma and Takahashi 2002). Roots absorb Si in the form of silicic acid at pH