Gasotransmitters Signaling in Plant Abiotic Stress: Gasotransmitters in Adaptation of Plants to Abiotic Stress 3031308573, 9783031308574

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Signaling and Communication in Plants

Mehar Fatma Zebus Sehar Nafees A. Khan   Editors

Gasotransmitters Signaling in Plant Abiotic Stress Gasotransmitters in Adaptation of Plants to Abiotic Stress

Signaling and Communication in Plants Series Editor František Baluška, IZMB, Department of Plant Cell Biology, University of Bonn, Bonn, Nordrhein-Westfalen, Germany

This book series will be devoted to diverse aspects of signaling and communication at all levels of plant organization, starting from single molecules and ending at ecological communities. The individual volumes will interlink molecular biology with plant physiology and the behavior of individual organisms, right up to the system analysis of whole plant communities and ecosystems. Plants have developed a robust signaling apparatus with both chemical and physical communication pathways. The chemical communication is based either on vesicular trafficking pathways or accomplished directly through cell-cell channels known as plasmodesmata. Moreover, there are numerous signal molecules generated within cell walls and also diffusible signals, such as nitric oxide, reactive oxygen species and ethylene, penetrating cells from exocellular space. Physical communication on the other hand is based on electrical, hydraulic, and mechanical signals. The integrative view of this book series will foster our understanding of plant communication throughout the individual plant and with other communicative systems such as fungi, nematodes, bacteria, viruses, insects, other plants, and predatory animals.

Mehar Fatma · Zebus Sehar · Nafees A. Khan Editors

Gasotransmitters Signaling in Plant Abiotic Stress Gasotransmitters in Adaptation of Plants to Abiotic Stress

Editors Mehar Fatma Department of Botany Aligarh Muslim University Aligarh, India

Zebus Sehar Department of Botany Aligarh Muslim University Aligarh, India

Nafees A. Khan Department of Botany Aligarh Muslim University Aligarh, India

ISSN 1867-9048 ISSN 1867-9056 (electronic) Signaling and Communication in Plants ISBN 978-3-031-30857-4 ISBN 978-3-031-30858-1 (eBook) https://doi.org/10.1007/978-3-031-30858-1 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Foreword

Gasotransmitters are the gaseous signaling molecules such as nitric oxide (NO), ethylene, carbon monoxide (CO), hydrogen sulfide (H2 S), and carbon dioxide (CO2 ) that influence cellular redox potential through certain physiological, biochemical, or metabolic changes in plant cells. Maintenance of redox homeostasis strengthens the potentiality of plants to resist abiotic stress conditions through the enhanced antioxidant system and the subsequent impact on other signaling molecules. Gasotransmitters have been viewed as the key integrator of information from cellular metabolism and the plant-environment relationship. This book aims at presenting novel outcomes and implications in plant biology concerning the study of different types of gasotransmitters signaling in the regulation of redox reactions for the adaptation of plants to diverse abiotic stresses. The book will deal with gasotransmitters’ relevance to plant functions and adaptations to abiotic stresses, integration of physiological, biochemical, and molecular studies on the various aspects of the redox homeostasis in plants with gaseous molecules, the influence of gasotransmitters on cellular or whole plant physiology for abiotic stress tolerance, recent progress and new perspective in gasotransmitters, the influence of gasotransmitters on omics for abiotic stress tolerance, and the emerging role of gasotransmitters in regulating redox homeostasis for plant stress management. Mehar Fatma Zebus Sehar Nafees A. Khan Department of Botany Aligarh Muslim University Aligarh, India

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Preface

Gasotransmitters are the gaseous signaling molecules such as nitric oxide (NO), ethylene, carbon monoxide (CO), hydrogen sulfide (H2 S), and carbon dioxide (CO2 ) that influence cellular redox potential through certain physiological, biochemical, or metabolic changes in plant cells. Maintenance of redox homeostasis strengthens the potentiality of plants to resist abiotic stress conditions through the enhanced antioxidant system and the subsequent impact on other signaling molecules. Gasotransmitters have been viewed as the key integrator of information from cellular metabolism and the plant-environment relationship. This book aims at presenting novel outcomes and implications in plant biology concerning the study of different types of gasotransmitters signaling in the regulation of redox reactions for the adaptation of plants to diverse abiotic stresses. Plants are confronted with a variety of abiotic stresses such as heat, drought, chilling, and salinity which are all key constraints impacting crop yields in modern agriculture. In plants exposed to various abiotic stresses such as photosynthesis, antioxidant metabolism is affected. Abiotic stress-induced generation of reactive oxygen species (ROS) is highly deleterious for plants. These environmental factors are responsible for stimulating the generation of ROS including superoxide anion radical (O2 − ) and hydrogen peroxide (H2 O2 ) resulting in oxidative stress that causes an imbalance between ROS production and the available antioxidant defense. This abiotic stress causes alterations in photosynthesis and respiration, resulting in a shorter life cycle and lower plant productivity. Under excess ROS generation, the antioxidant system plays a significant role in reducing the deleterious effect of stressinduced ROS. The antioxidants have the capacity to hold stability in order to avoid disruption due to environmental disturbances. This book deals with the gasotransmitters signaling in the regulation of cellular metabolism of redox reactions and homeostasis for adaptation of plants to unfavorable abiotic stress environments. Abiotic stress negatively impacts the metabolism, growth, development, and productivity of crop plants. It alters the metabolism at the cellular or whole plant level and disturbs the mineral nutrients homeostasis, osmoregulation, functionality of enzymes, and membrane damage, and changes the levels of several signaling molecules in the cell. Plants growing under natural abiotic stress vii

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conditions have an inherent capacity to withstand harsh conditions and their influence on cellular functions. It is thus necessary to understand physiological processes and molecular mechanisms that are operating in plants growing under naturally occurring abiotic environments for accomplishing the adaptation of plants to stress. Chapters are focused on the role of gasotransmitters signaling in plants under abiotic stress and their role in amplifying redox homeostasis for plant adaptation to abiotic stress. The study of gasotransmitters in plants has attracted much attention, especially for abiotic stress. This book is different from the others as the knowledge of gasotransmitters regulation and redox homeostasis under abiotic stress in plants is not available at one place. Our book will be the first comprehensive book covering all aspects of the gasotransmitters in redox homeostasis conferring different abiotic stress tolerance. The resent book could provide an excellent material for professors and lecturers teaching in wide area of plant physiology, environmental science, agriculture, cellular metabolism, abiotic stress tolerance mechanisms, etc., university students at the grade of senior undergraduate, master or Ph.D. level, senior researchers, researchers, or postdoctoral fellows. Aligarh, India

Mehar Fatma Zebus Sehar Nafees A. Khan

Contents

Gasotransmitters Signaling in Plants Under Abiotic Stress: An Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nidhi Verma and Sheo Mohan Prasad

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Influence of Gasotransmitters on the Physiology of Plants with Respect to Abiotic Stress Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Samina Mazahar and Ruchi Raina

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Gasotransmitters and Omics for Abiotic Stress Tolerance in Plants . . . . . Vipul Mishra, Pooja Singh, Mohd. Asif, Samiksha Singh, Shraddha Singh, Dharmendra Singh, Durgesh Kumar Tripathi, and Vijay Pratap Singh Advancement in the Biology of Gasotransmitters: H2 S, NO and Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ekhlaque A. Khan, Akhtar Parwez, Roushan Kumari, and Hamdino M. I. Ahmed Hydrogen Sulfide: An Evolving Gasotransmitter Regulating Salinity and Drought Stress Response in Plants . . . . . . . . . . . . . . . . . . . . . . . Shilalipi Samantaray and Kanchan Kumari Ethylene Synthesis and Redox Homeostasis in Plants: Recent Advancement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Manas Mathur, Ekhlaque A. Khan, Rakesh K. Prajapat, Hamdino M. I. Ahmed, Megha Sharma, and Deepak Sharma

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Nitric Oxide and Cellular Redox Homeostasis in Plants . . . . . . . . . . . . . . . 109 Tanashvi Seth, Sejal Asija, Shahid Umar, and Noushina Iqbal The Function of Hydrogen Sulfide in Plant Responses to Salinity and Drought: New Insights . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143 Harsha Gautam, Sheen Khan, Ameena Fatima Alvi, and Nafees A. Khan

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Hydrogen Peroxide and Its Role in Abiotic Stress Tolerance in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 Syed Nazar ul Islam, Mohd Asgher, and Nafees A. Khan Interaction of Ethylene and H2 S in Plant Stress Management . . . . . . . . . . 197 Humaira, Saba Wani, Nargis Bashir, Najeeb-ul-tarfeen, Zulaykha Khurshid Dijoo, and Khair-ul-nisa

Editors and Contributors

About the Editors Dr. Mehar Fatma is an Assistant Professor in the Department of Botany, Aligarh Muslim University, Aligarh. She did her M.Phil. and Ph.D. from Aligarh Muslim University, Aligarh, and then, she completed her Post-doc as Principal Investigator from Jawaharlal Nehru University, New Delhi (NPDF-SERB, DST-New Delhi and DSKPDF, UGC-New Delhi). During her Ph.D., she received the INSPIRE Fellowship from DST-New Delhi for the first rank holder and bagged the University Gold medal. She also got the prestigious MANF National Fellowship from UGC-New Delhi during her M.Phil. and Merit Scholarship in masters as a meritorious student. She has more than 34 peer-reviewed international publications and has attended conferences and seminars. She also visited Edinburgh, Scotland, and presented her research paper. Her research papers have lots of citations and have a high impact factor. She is also a life member of the Indian Society for Plant Physiology and the Indian Botanical Society and reviews editor for the Journal of Frontiers in Agronomy. Dr. Zebus Sehar did her Masters’s and Ph.D. from Aligarh Muslim University, Aligarh, and then, she worked as a Senior Research Fellow in a CSIR-funded research project with Prof. Nafees A. Khan in the Department of Botany, Aligarh Muslim University, Aligarh. During her Ph.D., she received the fellowships for meritorious students. She has several research publications in high Impact Factor peer-reviewed international journals. She is also a life member of the National Environmental Science Academy (NESA) and a recipient of the Junior Scientist Award of NESA. Prof. Nafees A. Khan is a Professor in the Department of Botany, Aligarh Muslim University, Aligarh. He did his Ph.D. and D.Sc. from Aligarh Muslim University, Aligarh. He has about 30 years of teaching experience and has successfully guided 37+ M.Sc. dissertations and supervised 20 PhD theses. He has been recognized as a Highly Cited Researcher from 2019–2022, Eminent Scientist Award 2019 by Samagra Vikas Welfare Society, Lucknow, UGC Research Award 2005, and UGC

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Mid-Career Award 2018, and many more. He is fellow of National Academy of Sciences. He is also a Fellow of the Linnean Society of London, the Indian Society of Plant Physiology, and the Indian Botanical Society. He has successfully completed or ongoing 9 research projects as Principal Investigator mainly involving gasotransmitters and has published more than 164 papers in peer-reviewed international journals. He is an editorial member in several peer-reviewed journals. He has edited several books published by Springer, Elsevier, NOVA, CRC Press, and others.

Contributors Hamdino M. I. Ahmed Horticulture Research Institute (HRI), Agricultural Research Center (ARC), Giza, Egypt Ameena Fatima Alvi Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, India Mohd Asgher Plant Physiology and Biochemistry Laboratory, Department of Botany, School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Jammu and Kashmir, Rajouri, India Mohd. Asif Plant Physiology Laboratory, Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India Sejal Asija Department of Botany, School of Chemical and Life Sciences, Jamia Hamdard, New Delhi, India Nargis Bashir Department of Botany, University of Kashmir, Srinagar, Jammu and Kashmir, India Zulaykha Khurshid Dijoo Department of Earth and Environmental Sciences, University of Kashmir, Srinagar, Jammu and Kashmir, India Harsha Gautam Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, India Humaira Centre of Research for Development, University of Kashmir, Srinagar, Jammu and Kashmir, India Noushina Iqbal Department of Botany, School of Chemical and Life Sciences, Jamia Hamdard, New Delhi, India Khair-ul-nisa Department of Earth and Environmental Sciences, University of Kashmir, Srinagar, Jammu and Kashmir, India Ekhlaque A. Khan Department of Biotechnology, Chaudhary Bansi Lal University, Bhiwani, Haryana, India

Editors and Contributors

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Nafees A. Khan Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, India Sheen Khan Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, India Kanchan Kumari Department of Botany, A.N College Patna, Patliputra University, Patna, India Roushan Kumari P.G. Department of Biotechnology, Magadh University BodhGaya, Bihar, India Manas Mathur School of Agriculture, Suresh Gyan Vihar University, Jagatpura, India Samina Mazahar Department of Botany, Dyal Singh College, University of Delhi, Delhi, India Vipul Mishra Plant Physiology Laboratory, Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India Najeeb-ul-tarfeen Centre of Research for Development, University of Kashmir, Srinagar, Jammu and Kashmir, India Akhtar Parwez P.G. Department of Biotechnology, Magadh University BodhGaya, Bihar, India Rakesh K. Prajapat School of Agriculture, Suresh Gyan Vihar University, Jagatpura, India Sheo Mohan Prasad Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Ruchi Raina Department of Botany, Dyal Singh College, University of Delhi, Delhi, India Shilalipi Samantaray Department of Biotechnology, MITS Institute of Professional Studies, Affiliated to Berhampur University, Rayagada, India Tanashvi Seth Department of Botany, School of Chemical and Life Sciences, Jamia Hamdard, New Delhi, India Deepak Sharma School of Agricultural Sciences, Jaipur National University, Jaipur, India Megha Sharma Department of Botany, University of Rajasthan, Jaipur, India Dharmendra Singh Department of Zoology, Goswami Tulsidas Government P.G. College, Karwi, Chitrakoot, India

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Pooja Singh Plant Physiology Laboratory, Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India Samiksha Singh Department of Botany, S.N. Sen B.V. P.G. College, Chhatrapati Shahu Ji Maharaj University, Kanpur, India Shraddha Singh Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, India; Homi Bhabha National Institute, Mumbai, India Vijay Pratap Singh Plant Physiology Laboratory, Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India Durgesh Kumar Tripathi Crop Nanobiology and Molecular Stress Physiology Lab, Amity Institute of Organic Agriculture (AIOA), Amity University Uttar Pradesh, Noida, India Syed Nazar ul Islam Plant Physiology and Biochemistry Laboratory, Department of Botany, School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Jammu and Kashmir, Rajouri, India Shahid Umar Department of Botany, School of Chemical and Life Sciences, Jamia Hamdard, New Delhi, India Nidhi Verma Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India; B K Birla Institute of Higher Education, Pilani, Rajasthan, India Saba Wani Department of Biochemistry, University of Kashmir, Srinagar, Jammu and Kashmir, India

Gasotransmitters Signaling in Plants Under Abiotic Stress: An Overview Nidhi Verma and Sheo Mohan Prasad

Abstract Plant systems are allowed to face many stressful experiences throughout their life cycle and during this struggling time plant’s own defence machinery works to stabilize internal metabolic activities. Gasotransmitter molecules, viz. nitric oxide (NO), ethylene, carbon monoxide (CO), hydrogen sulphide (H2 S), and carbon dioxide (CO2 ) constitute a powerful internal defence system in plants, which are endogenously synthesised in plant cells in specific cellular compartments (Fig. 1). During biotic or abiotic stress situations these gaseous signaling molecules possess certain defence related activities like governing cellular redox homeostasis, ROS balancing, boosting-up the defence machinery, regulating genetic modifications to attain stress tolerance in plants. In addition, exogenous applications of these gasotransmitters to plants appear to avail additional protection against stressful conditions, like salinity, drought, high temperatures and heavy metals, mainly through inducing antioxidant machinery, in order to combat oxidative cellular damage. Gasotransmitters also appear to be involved in crosstalk with other signaling molecules and plant hormones which constitute a complex strategic pathway. To understand these complex strategies of gasotransmitters are challenging in plant research.

1 Introduction to Plant Gasotransmitters Changing environment day by day coerce the plants to face several abiotic stresses. These abiotic stresses may worsen their impact on plant growth and regulation. To face several challenging environmental issues plants have their own support system, inbuilt by several gasotransmitters, signaling molecules and several plant hormones, N. Verma · S. M. Prasad (B) Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj 211002, India e-mail: [email protected] N. Verma B K Birla Institute of Higher Education, Pilani, Rajasthan 333031, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_1

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etc. (Dinant and Suarez-Lopez 2012). Among these defensive support systems gasotransmitters have more prominent and promising potential to cope up with negative impacts induced by abiotic stresses. Nitric oxide (NO), ethylene, carbon monoxide (CO), hydrogen sulphide (H2 S), and carbon dioxide (CO2 ) are the well-known gasotransmitters in plant body. Individually these gasotransmitters play an important role in each and every step of plant growth and developmental processes. However, these gasotransmitter molecules sometimes show strategic crosstalk together (Li et al. 2015; da-Silva and Modolo 2018). Previous studies reported the involvement of gasotransmitters in various post translational modifications during challenging abiotic stresses. Because of gaseous nature of these signaling molecules they are prone to interact other secondary metabolites like calcium ions (Ca2+ ), ROS like H2 O2 and O2 •− , other signaling molecules and phytohormones (Verma et al. 2020) (Fig. 1). Accordingly, these gasotransmitter molecules are linked together and they show a crosstalk among them. In previous researches it was explored that gasotransmitters are participating in each and every step of plant growth, and development and their signaling strategies are not so linear (Li et al. 2015; Verma et al. 2020). But to understand the complex multidimensional strategies of gasotransmitter molecules more researches are required. Thus, the main objective of this chapter to collect information about gasotransmitters’ interactive behaviour during acquisition of abiotic stress tolerance.

1.1 Nitric Oxide (NO) Among all other gasotransmitters nitric oxide is a highly potential multitasking molecule clearly depicted by Domingos et al. (2015). In the present scenario, on going researches proved its protective role at each and every developmental stage of the plant (Verma and Prasad 2021a). Its protective role is not limited to higher plants, the lower plants also get benefited to its protective strategies. In this queue, Qian et al. (2009) and Tiwari et al. (2019) reported that exogenously supplied NO in the form of SNP is able to cope up the organisms Chlorella, and Anabaena PCC 7120 from the damaging effect of herbicide and aluminium metal toxicity respectively. The NO has the capacity to interact with different other signaling molecules and also with several phytohormones, that’s why involvement of NO is found at every developmental stages of plants (Delledonne 2005). NO is also found modulated by secondary messengers, i.e. cGMP, cyclic ADP-ribose (cADPR) and Ca2+ . In the guard cells of Vicia faba, it has been reported that NO promoted the levels of cytosolic Ca2+ (Garcia-Mata et al. 2003). NO regulates this function through cGMP and cADPR which activates intracellular Ca2+ -permeable channels. NO can also elevate free cytosolic Ca2+ from tobacco cells that process has been considered under cryptogein or hyperosmotic stress response (Lamotte et al. 2004; Verma et al. 2020).

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Plant Gasotrans mitters Ethylene

Fig. 1 Multidimensional roles of Gasotransmitters

1.2 Ethylene A potential gaseous plant hormone, ethylene has the ability to govern different aspects of plant developmental processes by interacting with other potential plant hormones. Previous study of Vandenbussche and Straeten (2012) reported that ethylene biosynthesis is modulated during biotic stress condition, and also during several regulatory processes in plants like fruit ripening, flowering, and senescence, nodule formation at the time of N-fixation and also in plasticity regulation to overcome with the changing environmental conditions. Previous studies also found the involvement of ethylene to control peroxidase activity in many plants. For instance, the exogenous application of ethrel which is an ethylene-releasing compound controls the peroxidase activity in Picea abies plant (Ingemarsson 1995; Vandenbussche and Straeten 2012).

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1.3 Carbon Monoxide (CO) In recent years researches found the gasotransmitter role of carbon monoxide due to its ability to govern several physiological processes in plants. CO molecule shows its positive involvement in root growth and development, stomatal conductance as well as in seed germination in plants (Wang and Liao 2016). A researcher Xie et al. (2014) have noticed the role of CO molecule not only in developmental processes of the plant but also in regulation of different abiotic environmental stresses by interacting with phytohormones and other signaling molecules. Moreover, this kind of interaction of CO with other gaseous signaling molecules like NO, H2 S, H2 , CH4 shows its complex signaling pathway to mediate abiotic stresses in plants (Lin et al. 2012).

1.4 Hydrogen Sulphide (H2 S) There are several plants found that are able to release H2 S from their leaves, cut branches, leaf discs as well as detached parts of the plants. This phenomenon shows that H2 S is an informative signaling molecule like NO (Zhang et al. 2010). Researchers revealed that L-cysteine desulfhydrases enzyme is mainly responsible for H2 S release and activity of this enzyme was found more enhanced during pathogen attack that shows the defensive role of H2 S inside the plant cell (Romero-Puertas et al. 2013). Multidimensional responses of H2 S in plant defence mechanism like metal stress tolerance, osmotic stress tolerance and freezing tolerance etc. in different plants, are described by Zhang et al. (2010) that justified the involvement of H2 S in plant resistance. Shi et al. (2014) reported that cadmium toxicity is ameliorated from Cynodon dactylon plant by using NaHS as H2 S donor. Finding of da-Silva and Modolo (2018) revealed the involvement of H2 S for balancing of ROS by enhancing the antioxidant system under stress situation. Studies regarding metal stress alleviation in plants by applying exogenous NaHS as H2 S donor are very helpful to understand H2 S signaling inside the cell (Pereira et al. 2010).

1.5 Carbon Dioxide (CO2 ) In previous findings CO2 was also found as a gasotransmitter molecule which has the ability to diffuse across the cell membrane. Studies also found the active participation of aquaporins in trans-membrane passage of CO2 during photosynthesis (Flexas et al. 2006; Kim et al. 2010). In plants the amount of CO2 influx is governed by stomatal conductance in turn during drought condition, intercellular CO2 in leaves mediates the stomatal closure to protect a plant from drastic water loss (Hu et al. 2010). A previous study of Lopes et al. (2011) has described the positive role of intercellular CO2 in acquisition of drought stress tolerance in C3 and C4 plants.

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There are several unravelling areas are left regarding these gasotransmitter molecules in abiotic stress management which need more focus to reveal. Thus, the focus of this study to collect all necessary information to explore the importance and interactions of gasotransmitters in attaining the abiotic stress tolerance in plants.

2 Biosynthesis of Gasotransmitters in Plants 2.1 Sources of NO in Plant Cell Groß et al. (2013) has described the localization of NO inside the different cellular compartments like chloroplast, peroxisome, mitochondria, cytoplasm and apoplast in higher plants. The two pathways of NO synthesis, i.e. oxidative and reductive were demonstrated by Verma et al. (2020) these pathways are arginine or hydroxylamine and nitrate dependent respectively. GTPase implied AtNOA1-gene is involved in NO synthesis from L-arginine in mitochondrial biogenesis (Zemojtel et al. 2006). Recent studies of Verma and Prasad (2021a, b) have experimentally proved the active participation of nitric oxide synthase (NOS) enzyme in maintaining endogenous basal level of NO in cyanobacteria. Likewise, Singh et al. (2021) have also proved the role of NOS enzyme in NO synthesis in soybean plants.

2.2 Sources of Ethylene in Plant Cell There are three major steps involved in biosynthesis of ethylene in plants and these steps are sequentially governed by three major enzymes. The first step involves the formation of S-adenosyl-methionine (SAM) from methionine substrate in the presence of SAM synthetases enzyme. Second step involves the conversion of SAM to1-aminocyclopropane-1-carboxylic acid (ACC) in the presence of ACC synthase enzyme (Chen et al. 2022). The last and final step involves the production of ethylene through ACC in the presence of ACC oxidase. Researches further proved that the production of ethylene is accelerated under abiotic stress responses or in case of specific plant development processes (Xu and Zhang 2015; Chen et al. 2022).

2.3 Sources of CO in Plant Cell In plants heme oxygenase (HOs) enzyme is known as a main enzymatic route of CO formation. Study of Muramoto et al. (2002) has noticed the in vitro synthesis of CO in the presence of a recombinant protein namely plastid heme oxygenase (AtHO1) as represented in Fig. 2. Additionally, Wang and Liao (2016) have observed a release

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Heme Biliverdin +

Fe2+

+

H2O2 or AsA

Heme methylene

Photoproduction Lipid Peroxidation

Ureide Metabolism

Fig. 2 Biosynthesis of CO in plants

of CO on exogenous supplementation of H2 O2 or AsA (ascorbic acid) through the splitting of heme methylene bonds. The biosynthesis of CO is a complex process which still needs more focused researches to explore accurate process in plants.

2.4 Sources of H2 S in Plant Cell Li et al. (2015) have observed an active participation of synthetase L_cysteine desulfhydrase (L_DES) enzyme in H2 S biosynthesis and maintenance of basal level of H2 S inside the cells of maize plant. Few recent studies reported the active involvement of some other H2 S synthesizing enzymes like cysteine synthase (CS), βcyanoalanine synthase (CAS), D-cysteine desulfhydrase (DCD), and sulfite reductase (SiR) in important plant cell organelles (Wang et al. 2021; Huang et al. 2021). L_DES and DCD-H2 S biosynthesizing enzymes were found activated inside the cytosol where cysteine (Cys) worked as a substrate to produce H2 S whereas in mitochondria CAS enzyme was found as an active participant of H2 S production through the reaction of cyanide detoxification. Moreover, in chloroplast H2 S production induced by the photosynthetic sulfate-assimilatory pathway catalysed by SiR enzyme (Takahashi et al. 2011; Singh et al. 2019). Endogenous level of H2 S might show variation in its concentration depending on the developmental state and stress situations (Huang et al. 2021).

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2.5 Sources of CO2 in Plant Cell Increasing atmospheric CO2 can enhance the plant growth and development by providing additional carbon which overall contributes to acquisition of abiotic stress tolerance in plants (AbdElgawad et al. 2016). The atmospheric carbon dioxide (CO2 ) can easily enter the plant through stomatal pores. Further, the Rubisco enzyme actively participates to fix the CO2 molecule for metabolic processes. Previous researches identified the Rubicsco enzyme, as a main carbon fixing enzyme as well as controller of carbon fixation (Xu et al. 2015).

3 Plant Gasotransmitters Under Abiotic Stress Abiotic stresses are the leading concerns that reduce crop production at global level. Upon facing these stresses, there is a huge change in the metabolism and cell signaling pathways in plants that limit crop productivity (Verma et al. 2020). Gasotrasmitters are the molecules which are known to govern several responses against different abiotic stresses.

3.1 Defensive Role of NO in Plants Under Abiotic Stress Among all gasotransmitters NO is an advanced multiplayer signaling molecule having a vital role in plant metabolic activities. Protective role of exogenous supplementation of NO in the form of SNP under the stresses of salinity (Chen et al. 2015), drought (Chakraborty and Acharya 2017), UV-B (Santa-Cruz et al. 2014), heavy metal (Jhanji et al. 2012; Ye et al. 2013), high and low temperature (Neill et al. 2008; Karpets et al. 2012) and wound (Poltronieri et al. 2014) have been noticed in various plants. NO shows a major role in all plant survival activities so that it is designated as ‘plant signaling hormone’ in scientific world. Under various abiotic stresses it regulates certain mechanisms like helps in maintaining K+ /Na+ equilibrium in cell, redox balancing, boosting antioxidants and triggering stress-tolerance genes (Verma et al. 2020). Freschi (2013) described that exogenous supplementation of plant harmones can alter the level of NO that clearly proved the interactive role of NO with phytoharmones. A study of Xu et al. (2010) demonstrated that in cadmium treated Medicago truncatula seedlings NO can enhance the root indole-3-aceticacid (IAA) by reducing its degradation via IAA oxidase activity to ameliorate Cd toxicity. The SnRK2 kinase regulated by ABA in Arabidopsis notified as draught resistant factor for plants by the up-regulation of DREB1A/CBF3 genes that modulate transcription factor genes under stressed situation (Umezawa et al. 2004). Guo et al. (2003) also observed that stomatal opening governed by low light and resistivity towards drought in Arabidopsis was due to mutant nitrate transporter Chl1gene. Moreover, Groß et al. (2013) have

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described that during pathogen attack in wild type Arabidopsis plant, high accumulation of SA, JA and ethylene is due to the response mediated by endogenously accumulated NO inside the plant cell which finally suppress the Hb1-coding gene GLB1 to resist the plant against pathogen attack. Regulation of opening and closing of stomata under stressed environmental conditions are governed by signaling cascade of different plant hormones GA, JA, ET, CK, and AUX, and NO serve as second messenger in this signaling cascade (Saito et al. 2009; Liu et al. 2010). Cross talk among NO, SA and ABA was noticed to cure chilling injury in Zea mays seedlings by enhancing the activities of antioxidants (CAT, SOD, POX) (Esim and Atici 2014). Considering above facts it is clear that NO is a key molecule to govern about all the phytohormones. Moreover, studies are still scant about the interplay between phytohormones with other signaling molecules that make an interesting area for further researches.

3.2 Protective Role of Ethylene in Plants Under Abiotic Stress Ethylene, a protective phytohormone is found to control several plant abiotic stresses like drought, hypoxia, heavy metal, heat, cold, osmotic and salt stresses by regulating several post translational modifications (Chen et al. 2022). Ethylene positively up-regulates the abiotic stress tolerance in plants by triggering some physiological and biochemical attributes including stomatal closure, leaf senescence, ROS scavenging, Na+ /K+ homeostasis and photosynthetic protection (Chandler 2018; Chen et al. 2022).

3.3 Protective Role of CO in Plants Under Abiotic Stress In the natural environment, plants are adapted to induce certain defence mechanism to survive under biotic and abiotic pressures, thereby triggering a wide variety of defensive signaling molecules and plant hormones to unlock the defence-related regulatory systems. CO, a gasotransmitter is also synthesized against oxidative damage inside the cells exposed to abiotic stress, such as water deficit, salinity stress, and heavy metal stress (Liu et al. 2010; Meng et al. 2011; Wang and Liao 2016). Along with the signaling strength CO molecule has also been involved in crosstalk with other plant hormones and signaling molecules to modulate defence-related strategies (Lin et al. 2014; Xie et al. 2014).

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9

3.4 Defensive Role of H2 S in Plants Under Abiotic Stress Chen et al. (2015) have found a promising role of H2 S in salt stress tolerance in barley seedlings through a positive crosstalk with NO. Study stated that H2 S can induce the expression of HvAKT1 gene thereby actively assimilated the K+ in salt treated barley roots (Table 1). Previous studies have suggested the role of H2 S against pathogen attack (Zhang et al. 2008), Al stress alleviation in wheat seedlings (Zhang et al. 2010) and zinc (Zn) stress alleviation in Solanum nigrum (Liu et al. 2016). Interestingly, H2 S can activate the redox balancing inside the stressed cells thereby up-regulating the antioxidant defence system (Singh et al. 2015).

3.5 Defensive Role of CO2 in Plants Under Abiotic Stress Xu et al. (2015) have concluded that CO2 enriched fertilization can contribute to provide tolerance against various environmental stresses, like high temperature, salinity, drought and O3 pollution, Observing these aspects of stress mitigation it was determined that CO2 enrichment promoted the plant’s individual growth (Xu et al. 2014), enhanced the rate of photosynthesis (Zinta et al. 2014), optimized the chlorophyll a fluorescence kinetics (Xu et al. 2015), boosted the membraneprotecting enzymes to enhance antioxidant defence metabolism thereby decreasing the endogenous H2 O2 production (Zinta et al. 2014). Apart from modifications in activities of antioxidants and photorespiration, previous study of AbdElgawad et al. (2016) directs that mitochondrial and chloroplastic ROS production is reduced under high CO2 level, thereby reducing the NADPH oxidase activity. A finding of Kumari et al. (2013) has demonstrated that elevated CO2 can reduce the lipid peroxidation (MDA accumulation), in ozone stressed Beta vulgaris L. plants by boosting the activities of cellular antioxidants.

4 Participation of Gasotransmitters in Gene Regulation In the present scenario it is finally accepted that NO plays a strategic role in plant’s overall growth and developmental processes, including seed development, photomorphogenesis, root and shoot organogenesis, flowering, and fertilization, senescence and stress tolerance management (Domingos et al. 2015; Verma et al. 2020) (Fig. 1). Early studies showed that the regulation of proteins essential for cell construction, metabolic processes, and signaling mechanisms are governed through NO attempting post translational modifications by S-nitrosylation. Moreover, NO is also known to regulate the expressions of several defensive genes like in barley aleurone and in tobacco through activation of cyclic pathways of cGMP and cyclic ADP ribose (cADPR) (Domingos et al. 2015). Similar to NO, H2 S also governs some genetic

Arabidopsis thaliana

Camellia sinensis

Metal (Cd)

Cold

Arabidopsis

Phaseolus vulgaris

UV-B

Metal (Cd)

Wheat

Drought

Ethylene

Barley

Salinity

NO

Plant

Stress

Effective Gasotransmitter

Boosted activities of SOD, APX, CAT

Increased ethylene synthesis boosting up the leaf biomass

Regulation of pollen tube growth and germination, proline accumulation by cGMP signaling pathway

ACS2 and ACS6 transcripts

–

Mediation of Triggered the programmed cell death Mitogen-Activated Protein Kinase (MAPK)

Block the ion leakage and chlorophyll loss

Enhanced activities of SOD, APX, CAT

HvAKT1 and HvHAK4

Regulation of K+ /Na+ equilibrium Reduction of malondialdehyde (MDA) and H2 O2 content

Involved enzymes or specific genes

Response against abiotic stress

Table 1 Responses of gasotransmitters against various abiotic stresses and involvement of signaling molecules

Chakraborty and Acharya (2017)

Chen et al. (2015)

References

–

NOS-like enzyme

–

(continued)

Schellingen et al. (2014)

Wang et al. (2012)

Ye et al. (2013)

upregulation of Santa-Cruz et al. hemeoxygenase (HO-1) (2014) isozyme

Enhanced abscisic acid (ABA) production indicates the direct relation with stomatal closing

H2 S

Involvement of other signaling molecules or phytohormones

10 N. Verma and S. M. Prasad

alfalfa

soybean

Cd stress

UV-B stress

CO

Beta vulgaris L

Zea mays L.)

Heat Stress

Ozone stress

Barley

Arabidopsis

Salt stress

Salt stress

Plant

Stress

CO2

H2 S

Effective Gasotransmitter

Table 1 (continued)

Ethylene Overproducer 1 (ETO1) activated

Involved enzymes or specific genes

restore the GSH: GSSG ratio

Boosting the activities of antioxidants

–

–

Increasing the H2 O2 and NO activity of L-cysteine desulfhydrase (L-DES)

NO

–

Involvement of other signaling molecules or phytohormones

Acquisition of NO Triggered the NO during CO producing UV-B-induced HO-1 heme oxygenase (HO) transcription enzymes signalling pathway

Reduced the cellular oxidative damage

Elevated CO2 reduces the lipid peroxidation (MDA accumulation)

Reducing endogenous accumulation of ROS

Modulation of K+ /Na+ Gene regarding balance by decreasing inward-rectifying potassium channel the net K+ efflux (HvAKT1)

ROS production increased, accompanied with Na+/K+ homeostasis

Response against abiotic stress

Santa-Cruz et al. (2014)

Wang and Liao (2016)

Kumari et al. (2013)

Li et al. (2015)

Chen et al. (2015)

Yang et al. (2017)

References

Gasotransmitters Signaling in Plants Under Abiotic Stress: An Overview 11

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modifications to protect plants from abiotic stresses as mentioned in Table 1. For instance, in heat stressed Zea mays plant H2 S collaborated with NO to reduce cellular oxidative damage (Li et al. 2015). Another gasotransmitters also govern some defence genes like Chen et al. (2015) have reported that H2 S can potentially up-regulate the genetic expression of an inward-rectifying potassium channel (HvAKT1) to modulate the balance of K+ /Na+ in salt stressed barley seedlings (Table 1). Another gasotransmitter CO2 is found involved in various plant developmental processes. Its participation in sugar feedback mechanism was described in which it was depicted that overproduced photosynthate in chloroplasts under elevated CO2 may be responsible for down-regulation of Rubisco enzyme by triggering the sugar signal network (Hexokinase, HXK, a flux sensor) (Xu et al. 2015) (Table 1). Likewise, studies also reported about the positive role of CO in effective alleviation of Cd-induced oxidative damage in alfalfa by modulating cellular glutathione metabolism, which potentially restore the GSH: GSSG ratio by enhancing the conversion of oxidized glutathione (GSSG) to glutathione (GSH) thereby decreasing the cellular oxidative damage (Han et al. 2008; Wang and Liao 2016) (Table 1).

5 Signaling Crosstalk Between Gasotransmitters and ROS Evidences clearly stated that plant gasotransmitters play a vital role in cytoprotection normalizing the redox status of a cell (Chakraborty and Acharya 2017; Verma et al. 2020). NO and H2 S are found to involve in several cellular defence processes like ROS genesis and degradation, enhancing the expressions of ROS scavenging enzymes, transforming the O2 − to H2 O2 and O2 molecules and contributing in cell death. Further, NO and H2 S are considered as active signaling molecule possessing transcriptional changes and signal transduction to cope with abiotic stresses (Li et al. 2015; Verma et al. 2020). In case of CO She and Song (2008) illustrated that H2 O2 signaling pathway is probably involved behind the CO-induced stomatal closure in Vicia faba. Thus, gasotransmitters pursue complex strategic pathways because of their gaseous properties. They show some strategic interactions with other signaling molecules and plant hormones and strongly avail abiotic stress tolerance in plants.

6 Conclusion and Future Perspective Present study summarizes several key points. (1) Plant gasotransmitters are found to involve in a number of positive responses in every step of plant growth and development thereby changing several physiological and biochemical attributes in plant metabolism. (2) Their gaseous nature builds a complex signaling pathway because of their multidirectional interference with other signaling molecules and plant hormones. (3) These gasotransmitter molecules are found to trigger several genes by participating in post translational modifications and ultimately they can

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avail biotic and abiotic stress tolerance in plans. Moreover, studies are very limited to understand all aspects of gasotransmitters in plants. Thus, in the future, researchers might emphasis on several crucial research aspects: (1) to further elucidate the core mechanisms of the plant response to all gasotransmitters participated in key biological processes, including cellular respiration and photosynthesis, cellular redox balancing and antioxidant activities. (2) to unravel and link the diverse responses of gasotransmitter molecules in plants, exposed under different kind of environmental stresses. (3) to find out the cellular crosstalk among these gasotransmitters, and other signaling molecules, plant hormones, ROS, and RNS (reactive nitrogen species).

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Influence of Gasotransmitters on the Physiology of Plants with Respect to Abiotic Stress Tolerance Samina Mazahar and Ruchi Raina

Abstract Abiotic stress is one of the major issue that have negative impacts on the plant growth and development. Plant alteration to stress leads to complex physiological, biochemical and molecular mechanism so as to maintain homeostasis. Gasotransmitters (GTs) are the gaseous signaling molecule and are well known for their active role in plants and maintains plant resilence under stress. GTs include hydrogen sulfide (H2 S), nitric oxide (NO), carbon monoxide (CO), hydrogen gas (H2 ), methane (CH4 ) and the gaseous phytohormone ethylene (ET). They are endogenously synthesized in plants in response to abiotic stress and regulates various plants developmental processes and stress responses. Different GTs work in an interactive way in response to different abiotic stresses. Hence the present chapter provides an insight about the influence of different GTs on plants, their production, site of action and cross-talks in plants in response to abiotic stress tolerance.

Abbreviations ABA Al AsA–GSH APX Cd CAT GSH GR HO HO-1 H2

Abscisic acid Aluminum Ascorbate–glutathione Ascorbate peroxidase Cadmium Catalase Glutathione Glutathione reductase Heme oxygenase Heme oxygenase-1 Hydrogen gas

S. Mazahar (B) · R. Raina Department of Botany, Dyal Singh College, University of Delhi, Delhi, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_2

17

18

H2 S MAPK POD ROS SOD

S. Mazahar and R. Raina

Hydrogen sulfide Mitogen-activated protein kinase Peroxidase Reactive oxygen species Superoxide dismutase

1 Introduction The gasotransmitters (GT) are dynamic signaling molecule generated endogenously and is responsible for various stress response mechanism in plants and are helpful in transmitting biological signals. The GTs can freely penetrate the cellular membranes without requiring any receptors or transporters and has high lipid solubility (Yang et al. 2016). The gasotransmitters regulates various biological functions and includes a group of small gaseous molecules such as carbon monoxide (CO), hydrogen sulfide (H2 S), nitric oxide along with CH4 and H2 (Yao et al. 2019a, b). Ethylene is the only gaseous phytohormone serving as GTs due to its regulatory role in plant growth and development along with stress response (Karle et al. 2021). Various studies suggest the application of GTs exogenously on plants under simulated abiotic stress conditions. Under abiotic stress plants are affected variously in their morphological features such as morphology of the leaf, height and also stomatal opening and closing. This is due to abiotic stressors involving extreme climatic conditions such as high or low temperature regimes, ultraviolet irradiations, salt, heavy metals, osmotic pressure, drought, flodding or waterlogging etc. (Ali et al. 2017; Jin et al. 2017a, b; Shen et al. 2011). These abiotic stresses are serving as a major threat to sustainable crop production (Hasanuzzaman et al. 2020). Several studies suggests that plants usually produce these GTs in response to abiotic stress and hence the release of these endogenous GTs helps in understanding of their function and signaling pathway (Abdulmajeed et al. 2017; Cui et al. 2017; Jia et al. 2018). Various physiological phenomenons are regulated by GTs such as seed germination, gaseous exchange via the guard cells, adventitious and lateral root development, stomatal opening and closure, symbiotic interactions, de-etiolation etc. (Kolupaev et al. 2019). The GTs is also known to increase the accumulation of some antioxidant and regulate their activities and also keep a check on the harmful activities of reactive oxygen species (ROS) (Karle et al. 2021). Various salt stress response is regulated by GTs and the salinity stress response have been studied in different plant species such as rice, wheat, chickpea, pea, cucumber, broadbean, mustard, Arabidopsis, Jatropa, alfalfa etc. (Karle et al. 2021). Activation of different protective mechanism in plants in response to salt stress is due to various factors such as the expression of stress responsive genes, regulation of ion channels via the redox homeostasis, osmolytes and its function in regulating the membrane damage, gaseous exchange, stomatal conductance, root development etc. (Karle et al. 2021). Salt stress and

Influence of Gasotransmitters on the Physiology of Plants with Respect …

19

GTs involves cross-talk with specific signaling components such as polyamines, antioxidant enzymes, osmolytes, ROS, mitogen-activated protein kinases (MAPKs), G-proteins, Ca2+ etc. Hence GTs is playing a major role in enhancing the plant tolerance to various environmental stresses; opening up new challenges in plant research and in the field of agriculture to better understands its function in the ever-changing environment and improve the plant resilence under different abiotic stressors.

2 Relationship Between Plants and Gasotransmitters There is a strong relationship between plants and GTs as they are generated in the plant cell and play a remarkable role in various biological processes. Hence its production and action are important and regulates several plant metabolic processes under stress.

2.1 Production of Gasotransmitters Gasotransmitters (GTs) are a very unique class of signaling molecules that have indispensable role in wide range of biological processes. Most classical transmitters studied so far are usually stored in vesicles but GTs are the family of molecules that are synthesized in response to some stimulus and released in organism soon after their synthesis. The biological action of these signaling molecules can be mediated by either modification of target proteins or by activation of metallo-enzymes (Mustafa et al. 2009). Nitric oxide (NO) was probably the first identified GT, however, through recent studies, carbon monoxide (CO), hydrogen gas (H2 ) hydrogen sulfide (H2 S) and methane have also been established as physiologically relevant GTs (Donald 2021). Over last two decades, the role of different signaling molecules has been extensively studied for their biological roles. Their production has always become very fascinating among scientists and researchers. Yandong Yao et al. studied the production and roles of GTs in plants under abiotic stress (Yao et al. 2019a, b).

2.1.1

Hydrogen Gas

Stephenson and Stickland (1931) were the first to observe emission of hydrogen gas in bacteria due to the hydrogenase enzyme. Various studies also confirmed the production of hydrogen gas by green algae and higher plants (Sanadze 1961). H2 gas emission was also studied in lettuce plant when kept under bright light during seed germination (Renwick et al. 1964). Some Recent studies on rice and alfalfa discovered the production of endogenous H2 gas under abiotic stresses (Xu et al. 2013; Xie et al. 2012; Xu et al. 2017a, b). Xu et al. (2017a, b) reported the production

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of H2 gas when germinating rice seeds were exposed to Al, followed by inhibition of GA/ABA ratio leads to inhibition in seed germination. Ethylene, ABA, Jasmonic acid and other abiotic stresses were also found to induce the production of H2 gas in plants (Zeng et al. 2013).

2.1.2

Hydrogen Sulfide (H2 S)

Once considered a toxic molecule for the biological systems and dangerous to the environment, its role as a signaling molecule for different physiological functions and plant adaptations in adverse conditions has been established (Aroca et al. 2021). H2 S production takes place during cysteine metabolism in mammals and in plants by different enzymes as well as through photosynthetic sulfate assimilation pathway in chloroplast (Gotor et al. 2019). Like hydrogen gas it is also produced in response to drought in Arabadopsis thaliana and wheat (Jin et al. 2011; Ma et al. 2016). Temperature stresses are also responsible for endogenous production of gas in grapes, cucumber and poplars. Production of H2 S is also induced by exposure to some heavy metals like cadmium (Cd), nickel (Ni) and lead (Pb) in bermuda grass, zucchini and cauliflower respectively.

2.1.3

Nitric Oxide (NO)

In plant cells the production of NO takes place endogenously but it can also be incorporated in plants from environment where it is generated by the action of some soil microorganism. In higher plants, NO production takes place by enzymatic and non-enzymatic reactions during oxidative and reductive mechanism depending upon substrate involved. Moreover, research on production of NO in plants has advanced in last few years. However, different sources like stress conditions, substrate availability, heavy metal stress are responsible for production of NO (Galatro et al. 2020). NO was shown to produce in tobacco and Arabadopsis during salt stress, whereas, endogenous level of NO is increased by application of exogenous NO and arginine in wheat during drought condition. Metal toxicity like Cd, Ni and Al are also known to induce the production of NO in peanut, wheat and Arabadopsis (Faria-Lopes et al. 2019; He et al. 2018; Han et al. 2014). Recent studies have also shown to increase the level of NO in roots as well as in shoots during phosphorus deficiency (Galatro et al. 2020).

2.1.4

Carbon Monoxide (CO)

In plants, biosynthesis of CO was first reported by Wilks (1959). Subsequently, the production of CO was observed in lima beans when exposed to sunlight. Like other GTs CO is also found to induce during abiotic stresses. CO production was also reported in Medicago sativa during the presence of heavy metal like Cd. Lipid

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peroxidation, hydrogen peroxide and ureides metabolism could also be considered as potential source of CO in plants (Jin et al. 2017a, b).

2.1.5

Methane (CH4 )

It is well known that methane, a greenhouse gas, is produced by some microorganisms in the intestines of cows, or in rice fields in aerobic condition. Moreover, methane was found to produce under ultraviolet light in citrus where UV reacts with its photosensitizer to produce hydroxy radicals (_OH), which causes the pectin methyl group to form CH4 . However, low light intensities and blue light were also found to be responsible for methane production in different plant species. Some evidences have also indicated the production of methane under salt stress. Polyethylene glycol was also found to elicit the production of CH4 in maize. Heavy metal stress could also be one of the reason for production of CH4 in different plant species (Yao et al. 2019a, b).

2.2 Role of GTs in Plants GTs are small gaseous signaling molecules produced by the organism and transmits signals. Research is in progress to elucidate the potential role of these signaling molecules in the field of biology. Some past studies have proved the pivotal role of GTs in enhancing plant tolerance (Jin et al. 2017a, b). A GT typically has high lipid solubility and can easily penetrate in cell membranes due to have high lipid solubility. Moreover, they do not require any specific receptor or transporter. GTs are also produced endogenously by certain enzymes and perform various functions which are of physiological relevance. Huyi He et al. (2018) demonstrated the role of H2 S in plant growth development and stress responses. Plant hormones mediate the production of H2 S and HS also affects the biosynthesis and transport of plant hormones. NO also proved to enhance the antioxidant defence system of plants and improve the IAA flow towards roots. NO also enhances the heavy metal resistance in plants by regulating the balance of Reactive Oxygen Species (ROS) and improves the changes in mineral nutrition content and metabolites (Kováˇcik et al. 2019). The role of NO in increasing the photosynthetic performance of leaf under drought conditions has already been demonstrated. Moreover, it also improved the quality of wheat grain during heat stress. The exogenous applications of low concentration CO escalates the seed germination and alleviates the damaging effect of seeding leaves in salt stress condition in different plants as well as protect nodule nitrogen fixation and assimilation in soybean (Zilli et al. 2014). CH4 , like other GTs, strengthen plant resistance against heavy metal toxicity and helps in elucidating its role in phytoremediation process.

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3 Gasotransmitters Interaction Under Abiotic Stress The crosstalk among GTs was initially known in animals and in recent years this crosstalk was found in plants under abiotic stress (Yao et al. 2019a, b). These multiple signal molecule regulates the plants response to abiotic stress. The determining factor regulating the plant physiological factor are various environmental stressors such as heat, cold, flood, drought, nutrient deficiencies, salt, excess light etc. (Kolbert et al. 2019). Figure 1 shows the schematic representation of different abiotic stresses on plants and the role of different GTs in combating the stressors and regulating various vital plant functions.

3.1 Crosstalk Between NO and ET Among the various regulatory signals both NO and ET promotes many plants developmental processes. Studies suggests that these gaseous signals interact to regulates significant biological processes in every phase of plant life from early vegetative stage to leaf senescence stage (Kolbert et al. 2019). Detailed discussion of the same is done below.

Regulates H2 signaling pathway, Reduces Al toxicity, ROS and membrane peroxidase production

Involved in salt, temperature & heavy metal stress, reduces As accumulation and activates AsA-GSH cycle ROS, SOD, APX, SOD, GR, CAT, NR activity, Na+/k+ balance, Cd stress, Stomatal closure

Fig. 1 Diagram representing the interactive effect of different Gasotransmitters (GTs) in regulating different abiotic stresses on the overall plant physiology

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Salt Stress

Salt stress is one of the most detrimental environmental stresses known to harm the plants’ cellular structure and physiological function and hence cause yield loss, reduced fertility, premature senescence, growth disturbance by inducing ionic, osmotic and nitro-oxidative stress (Peleg and Blumwald 2011; Zhu 2016). The signalling molecules (NO and ET) helps in improving the salt stress tolerance through their defense response in many ways (Per et al. 2017). The interaction between NO and ET depends on the intensity and duration of salt stress and also on the plant cell types and organs which are under salinity stress (Poór et al. 2014). The ET– NO interaction under salt stress was for the first time studied in Arabidopsis callus (Wang et al. 2009) and also in roots of tomato and mutant Never ripe plants where stronger nitro-oxidative stress caused degradation of DNA and protein, loss of cell viability and decrease in K+ /Na+ ratio (Poór et al. 2015). Both NO and ET regulates various developmental processes along with cell death under salt stress (Kolbert et al. 2019). Studies in wheat leaves suggests the increase in salt stress by the application of SNP under salt stress by decreasing the stress ET to optimal level and reducing the glucose sensitivity which promoted various photosynthetic activities (such as net photosynthetic assimilation, maximum quantum yield of PSII and rubisco activity), stomatal closure, NR activity, proline synthesis and antioxidant metabolism (such as APX, CAT, GR, SOD, glutathione reductase) (Sehar et al. 2019).

3.1.2

Drought Stress

Drought stress causes loss of turgidity in plant cells and disturbs the osmotic homeostasis. NO is known to improve the antioxidant defence system and osmoprotectants and hence play a major role in drought stress tolerance (Zhu 2016). Studies in Arabidopsis show that the emission of ET and NO were extremely reduced after 4day long drought stress (Nabi et al. 2019). NR activity was also found reduced under drought stress. Studies suggests that the interaction of ET and NO are involved in defence response and apoptosis (cell death) under abiotic stress (Kolbert et al. 2019). The drought tolerance of potato was improved after treating with non-protein amino acid β-aminobutyric acid and this led to the down-regulated ETR1 expression along with the production of transient NO and ROS (Haque et al. 2014). Other phytohormone also play an important role in regulating the role of ET and NO as high concentration of ABA enhances NO production in stomata and limits ET production (Sós-Hegedus et al. 2014). Hence the interaction of different GTs depends upon difference in the physiology, cell type and organs in different plants.

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Nutrient Stress

Insufficient availability of essential nutrients has a negative impact on plant development, growth and yield. Studies suggest that ET up-regulates the genes responsible for iron (Fe) acquisition such as AtFRO2, AtFIT, AtIRT etc. (Lucena et al. 2006). Further these genes were found responsive to NO treatment (Romera et al. 2011) hence showing interaction between these gasotransmitters in Fe deficiency in Arabidopsis. In Arabidopsis and cucumber, NO is known to promote the expression of genes (e.g., AtACO1, CsACS2, CsACO2, AtACS6, AtSAM1) in the ethylene synthesis and NO level in the roots were enhanced due to ethylene (García et al. 2010). Hence NO and ET regulates each other level in an equally positive way. Another study in phosphorous (P) deficient rice roots showed fast NO generation followed by a slower ET emission. NO was further found acting upstream of ET in P deficiency signalling response (Zhu et al. 2017). Increased NO and ET production was observed during the root hair development in Arabidopsis stimulated by Mg deficiency (Liu et al. 2017). Although Pharmacological studies suggests prevention of root hair morphogenesis in Mg starved Arabidopsis (Liu et al. 2017). Ethylene promotes the synthesis of NO by enhancing the enzyme activities of NR and NOS. Hence both ET and NO are involved in plant response to nutrient deficiency (Kolbert et al. 2019).

3.1.4

Temperature Stress

Plant growth and development is significantly affected by both low temperature and heat stress. Studies suggests that plant have developed altered molecular, physiological and biochemical mechanism to withstand the temperature stress, where ET and NO are the main GTs (Parankusam et al. 2017). In various parts of the world heat stress is a serious issue affecting the vital processes such as photosynthesis, respiration, membrane stability and water relations and hence limiting the agricultural yield (Kolbert et al. 2019). Heat stress also affects the plants metabolism, rearrangements of cytoskeleton, accumulation of unfolded proteins and influences the production of various phytohormones along with ET, NO and ROS (Wahid et al. 2007). ET and NO are closely related in regulating the cold stress in fruits (Leshem and Pinchasov 2000). In mango the interactive effect of both NO and ET are found reducing the chilling injury, softening and ripening in cold stored mangoes and also causing delaying of the fruit colour development (Zaharah and Singh 2011).

3.1.5

Heavy Metal Stress

Heavy metals (HM) are causing a great harm to agricultural productivity. It causes tissue damage, various morpho-physiological changes in plants, oxidative stress, disturbs the redox homeostasis of cells (Kolbert et al. 2019). Both NO and ET influence plant response under heavy metal stress and their interaction has been studied

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under Cd stress. In pea plant the effect of Cd on the metabolism of NO and ROS was very similar to those of ET, JA and SA (Rodríguez-Serrano et al. 2009). Under Cd stress significant production of ROS, JA, SA and ET was observed and the level of NO was found low (Kolbert et al. 2019). Hence it can be concluded that both NO and ET shows antagonistic effect in different plant parts such as roots and leaves under Cd stress as Cd is known to decrease the NO levels, cause nutritional imbalance and results in protein nitrosation which leads to ET synthesis (Rodríguez-Serrano et al. 2009). However in young soyabean seedlings the short term treatment with Cd enhanced the expression of genes encoding protein involved in ET and NO synthesis (Chmielowska-Bak et al. 2013).

3.2 Interaction Between CO and H2 The interaction of CO and H2 is serving as a messenger in plant and promoting various activities such as APX activities, increase the level of SOD peroxidase, enhances the GSH content and hence improve the antioxidant system in alfalfa under stress (Jin et al. 2013). Also, the interactive effect of CO and H2 is well known for limiting the oxidative damage caused to the plants (Yao et al. 2019a, b). Various biochemical and physiological studies in alfalfa seedling suggests the role of H2 O2 and HO-1 in the H2 signalling pathway under osmotic stress (Jin et al. 2016).

3.3 Crosstalk Between NO and H2 S Both NO and H2 S is involved in different stress response such as salt, temperature and heavy metal (Hancock 2019). The signal transduction pathway of H2 S works in association with NO and exhibit various downstream signalling pathways and have many similar functions (Yao et al. 2019a, b). NO is an essential signalling molecule during abiotic stress as it regulates various processes such as reduces the As accumulation and activates the upregulation of AsA-GSH cycle to overcome and balance the ROS related harm to macromolecules, NO also improves the oxidative damage of plants via signal transduction (Singh et al. 2015). H2 S and NO regulates several signaling pathways and play a significant role in the plants physiology and biochemistry (Corpas 2019). Hence the crosstalk between NO and H2 S play an important role in regulating abiotic stress.

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3.4 Crosstalk Between NO and H2 The GTs NO and H2 improves plant tolerance under abiotic stress. NO somewhere regulates the downstream process in the H2 signaling pathway in response to abiotic stress such as drought stress (Su et al. 2018) and heavy metal stress (Chen et al. 2014). According to Su et al. (2018) the action of both these GTs promotes the antioxidant defence system by upregulating certain antioxidant enzyme activities, reducing ROS production and membrane peroxidase in stressed plants. The interaction of NO and H2 is also known to improve the Al toxicity symptoms (Chen et al. 2014). In cucumber explants the content of NO increases due to the upregulation of nitrate reductase activity by H2 (Zhu et al. 2016a). The interactive effect of NO and H2 is quite complex and needs more research in combating the abiotic stress.

3.5 Interaction Between NO and CO NO and CO are known to play a significant role in signal transduction and in promoting plant growth under abiotic stress. Under several stress condition NO is found to improve the destructive nature of ROS along with the CO molecule and control the antioxidant enzyme system (Yao et al. 2019a, b). Interaction of CO and NO is known to balance the ion homeostasis, improve the antioxidant system in wheat and promote an enhanced tolerance to salt stress (Yao et al. 2019a, b). NO is known to fulfil many functions related to abiotic stress. NO regulates the HO/NO system and the activity of HO was found enhanced by NO (Yao et al. 2019a, b). NO also regulates the UV-B signaling pathway (Santa Cruz et al. 2010) and various other functions.

3.6 Crosstalk of CH4 with NO, CO and HO-1 The CH4 signaling pathway in mung beans is regulated by NO which counterchecks the sugar breakdown, ion balance and limits the ROS production (Zhang et al. 2018). In the adventitious root formation in cucumber the HO-1/CO along with Ca+ are regarded as downstream signals induced by CH4 (Cui et al. 2015). In alfalfa seeds under salt stress the activities of various antioxidant enzymes such as SOD, POD and APX are enhanced by CH4 and HO-1 which is known to upregulate the expression of HO-1 gene (Zhu et al. 2016b). Hence CH4 is known to upregulate HO-1 gene under abiotic stress (Yao et al. 2019a, b) although much studies are needed to understand the interaction of CH4 with other GTs.

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4 Conclusion and Future Perspective The most important global issue in current scenario is abiotic stress that reduces the plant productivity and development. Over the years H2 S, CO, NO and CH4 have received much attention as potential GTs particularly for abiotic stress. In recent past, researchers have proved the generation of these GTs under adverse conditions in plants. These signalling molecules are produced endogenously in an organism or received from outside environment and are responsible for different physiological and biochemical changes in organism, tissue or cell. Moreover, under different environmental conditions GTs escalates the plant tolerance. Hence learning about its production, action and interactions makes GTs a universal signalling molecule in plants. Though significant research has been done so far in the field of GTs, more piece of research is required for the molecular studies in different pathways related to the production of GTs in plants. Moreover, future research should also focus on their role in agriculture in terms of quality and yield of crops.

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Gasotransmitters and Omics for Abiotic Stress Tolerance in Plants Vipul Mishra, Pooja Singh, Mohd. Asif, Samiksha Singh, Shraddha Singh, Dharmendra Singh, Durgesh Kumar Tripathi, and Vijay Pratap Singh

Abstract Anthropogenic activities have exposed the plants to diverse types of abiotic stressors. These stressors restrict the plant growth and their productivity. Recent advances report of gasotransmitters such as nitric oxide and hydrogen sulfide to play alleviatory role against these stressors and restore the physiological normalcy in plants. Techniques such as transcriptomics, proteomics and metabolomics further help in identifying the regulatory elements involved with these gasotransmitters. Moreover, data fetched through these techniques assists in deciphering role of gasotransmitters and encompassing better strategies against abiotic stress tolerance conferred to plants.

V. Mishra · P. Singh · Mohd. Asif · V. P. Singh (B) Plant Physiology Laboratory, Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj 211002, India e-mail: [email protected] S. Singh Department of Botany, S.N. Sen B.V. P.G. College, Chhatrapati Shahu Ji Maharaj University, Kanpur 208012, India S. Singh Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre, Trombay, Mumbai 400 085, India Homi Bhabha National Institute, Mumbai 400 085, India D. Singh Department of Zoology, Goswami Tulsidas Government P.G. College, Karwi, Chitrakoot 210205, India D. K. Tripathi Crop Nanobiology and Molecular Stress Physiology Lab, Amity Institute of Organic Agriculture (AIOA), Amity University Uttar Pradesh, Noida, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_3

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1 Introduction In the past three decades, the world has witnessed progress more than it did in a millennium. As a result of reduced mortality, the world has witnessed a population blast and increase in pollution, causing a huge constraint for global food security, and plant and human lives. The anthropogenic revolution accompanied rampant increase in major abiotic stress factors. Abiotic factors such as water, air, temperature, light, minerals are nonliving essential factors of an environment that support and regulate life of all living organisms. But when any abiotic factor attains its concentration beyond the optimum range then it behaves like an abiotic stress, which includes, water deficit, flooding, chilling, high light, high temperature, salinity, and exposure to heavy metals (Pandey and Gautam 2020). Abiotic stress exposure enhances reactive oxygen species (ROS) generation which significantly restricts plant’s metabolic, biophysical response, and biomass yield worldwide (Zhang et al. 2021a). Plants are continuously faced with stressful conditions and withstand by their potential of evolving adaptations and regulatory properties in environment. Moreover, plant have an intrinsic defense system of enzymatic antioxidants such as catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), glutathione peroxidase (GPX) and ascorbate peroxidase (APX) and non-enzymatic compounds involved in biosynthesis of secondary metabolites like phenolic compound, terpenoids, flavanol, ascorbic acids, carotenoids and others (Lau et al. 2021). Extreme light, low rainfall, and high temperature all collectively cause drought stress, due to which plant-water interaction is influenced and plant life is also affected (Yanık et al. 2020). At physiological level, drought sensitivity in guard cells mainly increases transpiration rate, alters the K+ , anions and Ca2+ channels. While ABA-mediated drought signaling checks water loss and maintains stomatal conductance as well as reduction of CO2 assimilation in photosynthetic mechanism (Silveria et al. 2017). Biochemically, it increases oxidative ROS bursting, peroxidation of membrane lipid (Verma et al. 2019), drought-mediated DNA fragmentation, increasing genotoxic alteration at molecular level (Sahay et al. 2020). For the normal growth and development plants require some essential micronutrients like Zn, Ni, and Co. But some nonessential metals such as Cr, Cd, As, Hg, Pb, Al even under low concentration cause heavy metal toxicity, contaminating air, water and soil thereby negatively impacting plants and humans’ life (Pandey et al. 2019). Metal toxicity causes oxidative damage, disrupting antioxidant system (Kharbech et al. 2017). Moreover, it interferes with different metabolic and enzymatic pathways, resulting in protein modification and DNA damage. Biosynthesis of plants associated various metal detoxicants like phytochelatins, ligands, peptide and metallothionines is followed by the omics-mediated mechanisms (Parihar et al. 2019). Nearly 1/5th of the world’s arable lands and half of the world’s irrigated lands are affected by salt stress. At the current scenario overabundance of salt in soil and water causes salinity stress which is most devastating stress for agricultural production. When in excess, salt content leads to cellular dehydration, hyper osmotic condition, and ultimately restricted physiological response of plants (Ayub et al. 2020). Plant

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maintains the movement of ions, mainly Na+ / H+ and K+ , and their concentrations in the cells, activity of protein channels and expression of plasma membrane under salt stress (Chakraborty et al. 2016). Shahzad et al. (2019) elucidated on the necessary export of Na+ ions from the cell which compete with cytoplasmic K+ and reduces its uptake under salinity condition. While K+ is key regulator of turgor pressure of cells and provide resistance to plants from salinity effect. However, plants show stress-adaptation against abiotic stresses and respond via various signaling mechanisms, physiological, biochemical, and molecular level processes, and initiate production of gasotransmitters in acclimation against these damaging influences. These gasotransmitters are nitric oxide (NO), hydrogen sulfide (H2 S), carbon monoxide (CO), methane (CH4 ), and the only gaseous phytohormone ethylene (C2 H4 ) (Karle et al. 2021). Of these, NO and H2 S have recently gained momentum as they play vital role either in a coordinative manner or independently for physio-biochemical development processes providing stress acclimation to plants (Alamri et al. 2020; Antoniou et al. 2020; Bhat et al. 2021). Hydrogen peroxide (H2 O2 ) and nitric oxide (NO) are two of the central signal transduction pathway elements leading to activation of plant defense against biotic or abiotic stress. The gaseous NO and H2 S easily diffuse across cell membrane as free radical signaling molecules (Huang et al. 2021). These molecules interact with other intracellular secondary signaling molecules like H2 O2 , Ca2+ -dependent pathways, and G-protein-linked signaling phytohormones. Further, they utilize various omics mediated regulations such as, genomic, transcriptomic, proteomic and metabolomic performing molecular mechanisms under stressful conditions, varying with the species (Thakur and Anand 2021; Mishra et al. 2021). Several reports have documented the diverse contribution of endogenous as well as exogenous cellular context of NO and H2 S and their roles in positive as well as negative regulation of abiotic stress. This book chapter highlights about gasotransmitters omics in regulating abiotic stress acclimation in crop plants (Fig. 1).

2 NO in Stress Regulation From half a century, researchers have well documented crucial behavior NO displays in abiotic stress mitigation in plants. NO functions as a cytoprotectant through its property to regulate antioxidant defense mechanism and manage ion redox homeostasis. Generally, production of NO is not clearly known but in this regard two routes one is NOS like (L -arginine mediated) oxidative mechanism and other nitrate reductase (NR) mediated reductive pathway is involved in generation of NO (BegaraMorales et al. 2020). Interestingly, NO acts as savior only under optimum concentrations beyond which it turns toxic. It possesses the ability to interact and modulate different target sites (specially thiol groups) in plant under several adverse conditions (Farnese et al. 2016). According to Silveira et al. (2017), drought signaling enhances the intracellular and extracellular content of NO in root tissues tending to promote root formation in sugarcane (Saccharum spp.), improving uptake of water. Furthermore, NO regulates ROS/NO redox homeostasis and transcription of

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Heat

Salinity

Drought Heavy Metals

Cold

Oxidative damage; Electrolytic leakage; Membrane damage; Protein misfolding etc.

Exogenous SNP

Endogenous NOS/NR

Glycinebetaine, PAL, TAL, Polyamines etc.

METABOLOMICS

Lea, HSP, Kinases, Actin, Photosynthetic proteins etc.

PROTEOMICS

bZIP, WRKY, MYB, ERF, NAC, DREB/CBF, HSF etc.

Endogenous L-Des/D-Des

Exogenous NaHS

TRANSCRIPTOMICS

NO H2S

Fig. 1 Endogenous and Exogenous NO and H2 S mitigate the damage caused by varying abiotic stressors in plants, functioning their mechanisms through the intricate network and interplay of diverse transcriptomes, proteomes and metabolomes. Abbreviations bZIP (Basic leucine zipper domain); DREB/CBF (dehydration-responsive element/C-repeat binding factors); ERF (ethylene responsive factor); HSF (heat shock factors); L-Des/D-Des (L -cysteine desulfhydrase/D cysteine desulfhydrase); Lea (late embryogenesis abundant); MYB (myeloblastoma); NAC (no apical meristem [NAM], Arabidopsis thaliana activating factor [ATAF 1–2], cup-shaped cotyledon [CUC2]); NaHS (sodium hydrosulfide, a donor of H2 S); PAL (phenylalanine ammonia lyase); SNP (sodium nitroprusside, a donor of NO); TAL (tyrosine ammonia lyase)

genes such as gsnor1/hot5 and nox1/cue1 that provide resistance from heat stress (Parankusam et al. 2017). In its defense against heat stress, plant generates low molecular compounds such as polyamines, L -Arginine, GSNO S-nitrosoglutathione, GSNOR, S-nitrosoglutathione reductase and nitrite resulting in endogenous enrichment of NO. It further indulges in crosstalk with downstream H2 O2 , and mostly phytohormones. NO and H2 S are also involved in activation of Ca2+ -CaM dependent protein phosphatases, CDPK, calcium dependent protein kinases; GSNO, MAPK (mitogen activated protein kinase) regulate gene expression along with additional factors to provoke aggregation of HSPs in response to HSFs (heat shock factors) associating with DNA. Analysis by Cantrel et al. (2011) shows NO to participate in modulation of cold stress controlled by gene expression and negative regulation of two phosphorylated sphingolipids in A. thaliana. Exogenously applied SA and NO counteracts salt stress damage in Vigna angularis by enhancing enzymatic and non-enzymatic antioxidative activities (Ahanger et al. 2019). While in maize, NO mediates proteomic modulation against salt sensitivity (Bai et al. 2011). Through S-nitrosylation and tyrosine nitration, NO-mediated post-translational modifications (Fancy et al. 2017) remarkably maintain cellular and metabolic homeostasis. All the above cumulated information about NO against stress tolerance has been recognized as the defensive mechanism to plants.

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3 H2 S in Stress Regulation H2 S is the third important thiol group reactive, multifunctional gasotransmitter. It tends to carry out its functional aspects through persulfidation reaction of certain target groups of proteins. H2 S mediated modulation of protein targets via posttranscriptional modification (PTM) through persulfidation is redox modification of thiol (–SH) and cysteine (Cys) into a specific persulfide group (–SSH) which controls biological implications (Ju et al. 2017; Corpas et al. 2019). Furthermore, new research has demonstratedthat the opposite of persulfidation is S-desulfurization covalent modified protein in Garlic (Allium sativum L) (Zhu et al. 2021). In response to drought stress implications of exogenously applied NaHS (a donor of H2 S) results in the accumulation of osmoprotectants like polyamine, glycine and sugar and reduces membrane damaging content via enhanced antioxidative defense response (Thakur and Anand 2021). NaHS further prevents water loss via ABA-mediated stomatal closure signaling in Arabidopsis thaliana (García-Mata and Lamattina 2010) and maintains cellular integrity in Oryza sativa (Zhou et al. 2020). Moreover NOSH, another synthetic donor of NO and H2 S significantly ameliorates the deleterious effects of drought condition in Medicago sativa (Antoniou et al. 2020). Experimental revelations by Siddiqui et al. (2021) indicate that the exogenous potassium (K+ ) and endogenous H2 S synergistically function in tomato (Solanum lycopersicum L. Mill.) seedlings to regulate redox homoeostasis alongside H+ -ATPase flux and carbohydrate metabolism under drought stress. NO and H2 S interaction prevents damaging impact of salinity (Goyal et al. 2021; Karle et al. 2021). Moreover, induced melatonin (Sun et al. 2021) in cucumber also reports H2 S to regulate transcriptomic and proteomic response to salinity (Jiang et al. 2020). NO and H2 S together or alone tend to provide plant acclimation from metal stress tolerance as well (Rather et al. 2020), implicating their multi-faceted role in abiotic stress tolerance. Furthermore, the super inductive protecting mechanism of gasotransmitters NO and H2 S protects plants from unpredictable abiotic stresses.

4 Omics of Abiotic Stress Regulation by Gasotransmitters 4.1 Transcriptional Regulation Under Abiotic Stress Transcriptional regulation is the functional aspect of the field of transcriptomics. Discovered during the 1990s, it involves the analysis of RNA transcripts generated in response to varying inter/intra cellular stimuli (Liang 2013). It further reports the functional and non-functional transcripts i.e. mRNAs which have been translated into proteins and those which have not. Study of transcriptomics under stress helps in identifying the central genetics players and the signalling pathways involved in the stress mitigation. This knowledge may further be used to develop more resistant crop varieties. Microarray and high-throughput sequencing (RNA-Seq) are the two popular

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techniques used to study transcriptomes (Liang 2013). Analysis through these techniques implicate different types of stressors trigger different set of transcripts, as elaborated in the subsequent paragraphs.

4.1.1

Drought

Erratic weather patterns have caused drought to become a major abiotic stress factor and an agricultural tragedy worldwide. Drought impedes the plant growth and appears in the form of wilting due to turgidity loss under water deficit conditions. To resolve this, microarray analysis and comparative RNA-sequencing methods have enabled scientists to identify various transcripts and genetic signals that plants utilize in response to acclimatize towards drought stress (El-Esawi 2020). These factors move cellular response from sensing to sensitizing the plant through ABA—dependent and ABA—independent pathways. Regulatory TFs that activate stress inducible response genes involve Basic Leucine Zipper (bZIP), WRKY, Homeodomain-Leucine Zipper (HD-Zip), Myeloblastoma (MYB) and Apetala2 (AP2)/Ethylene Responsive Factor (ERF) possessing subfamily members such as Dehydration responsive element binding protein (DREB)/C-Repeat Binding Factor (CBF), Shine (SHN), and Wax Production-Like (WXPL) Transcription Factors (Hrmova and Hussain 2021). Interestingly, activities of members of these TF families have been reported to be in interplay with gasotransmitters such as nitric oxide (NO) and hydrogen sulfide (H2 S) in alleviating drought stress. NO has been known to play a pivotal role in plant growth regulation under both, normal and stressed environments. Water deficit causes endogenous NO to transcriptionally modulate AtPYL4 and AtPYL5 through in-vivo activation of rat neuronal NO synthase (nNOS) in Arabidopsis thaliana. While, nNOS overexpressed Oryza sativa seedlings RT-PCR analysis reports of the OsDREB (2A and 2B), OsSNAC (1 & 2), OsLEA3 and OsRD29A transcripts during drought stress (Singh et al. 2020). Moreover, NO in crosstalk with AtHVA22H, WRKY ABO3, and AtWRKY62 TFs indicates towards transcriptional regulation of drought by NO through the modulation of stress-response ABA genes (Lau et al. 2021). H2 S protects plants from drought through its ability to express transcription factors that integrate with the antioxidative machinery and growth regulation (Corpas 2019). Water-deficit facing Arabidopsis thaliana is rescued by H2 S, modulating expression of growth genes targeting transcripts such as miR167, miR393, miR396 and miR398 and up-regulating stress response elements DREB (2A & 2B), RD29A and CBF4 (Shen et al. 2013). While in wheat, H2 S manages drought stress machinery upregulating the TaERF1 and TaMYB30 as well as Orphans, bHLH, bZIP TFs, molecular switches of survival genes and high proline levels (Li et al. 2017, 2021). In rice, NCED transcripts especially NCED2 gets accumulated on introduction of H2 S while drought response ABA regulated TFs AREB1, AREB8, bZIP23, and LEA3 expression enhances (Zhou et al. 2020).

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Conclusively, under NO and H2 S drought stress is managed by these TFs, by stomatal regulation utilizing various signalling pathways involving phosphorylation by kinases and Ca2+ dependent signalling along with ABA and hormonal interactions (Corpas 2019).

4.1.2

Cold

Cold stress severs the plants growth at all levels. It appears morphologically in the form of chlorosis of leaf and necrosis of tissues. It limits the growth potential of a plant by damaging its metabolomic profile and genetic integrity (Yadav 2010). Cold stress stimulates intracellular Ca2+ ion fluxes to trigger desensitizing mechanisms. These mechanisms either activate calmodulin signalling pathway triggering CAMTA TFs or multiple circadian clock-related TFs. Both ultimately induce the expression of DREB1/CBF TFs also known to be the master regulators of the cold stress, responsible for activation of osmoprotectant genes (El-Esawi 2020; Kidokoro 2022). NO and H2 S are versatile gasotransmitters regulating various abiotic stresses. The available studies suggest that under chilling stress, Ca2+ ions trigger NO generation which activates protection mechanism by up-regulating the CBF1 and CBF3 TFs along with P5CS1 and the down-regulation of ProDH, accompanied by accumulation of cellular protectant Proline (Baudouin and Jeandroz 2015). H2 S utilizes MPK4 to positively stimulate cold resisting TFs, such as CBF3, COLD REGULATED 15A and 15B (COR15A and 15B) to regulate stomatal closure (Zhang et al. 2021a, 2021b, 2021c). However, it triggers another signalling complex auxin response factors (ARF)—DREB3 helping develop resistance to cold stress in cucumber (Zhang et al. 2021a, 2021b, 2021c). Conclusively, actions of NO and H2 S as specific TFs’ triggers under low temperatures have been studied, yet repertoires of regulons and entire mechanisms remain elusive.

4.1.3

Salinity

Among the various abiotic stresses, salt stress affects the global agricultural biomass production the most. Plant cells perform optimally when its signalling components are in sync with the ion homeostasis of both inter and intra cellular space. Salinity fatally damages the cellular integrity of the plants. It causes oxidative damages, extreme ion imbalance (Na+ /K+ pump) resulting in fragmented signalling machinery appearing in the form of stunted growth (Ayub et al. 2020). To counter this, plant perceives and generates committed TFs which trigger counter signals at the genomic level. Solute stress is transcriptionally managed by the members of the WRKY, MYB, bZIP, NAC, and AP2/ERF families as testified by the studies involving up and down regulation of their specific sub members (Kumar et al. 2017). These TFs bind to specific domains of the DNA resulting in the relative activation of stress responsive genes (Chaudhry et al. 2021).

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Much has been discovered about the protective and signalling role of NO, despite that exact transcript functioning under solute stress remains elusive. It is established that NO plays a protective role in salt stressed plants through K+ and Na+ homeostasis regulation and enhanced synthesis of polyamines (Rai et al. 2021). It also activates the antioxidant machinery. Selective studies report of salinity tolerance as in rat neuronal NOS (nNOS) overexpressed Oryza plants (Cai et al. 2015) implicated by enhanced expression of Os-CAT, POX, LEA3, RD29A and SNAC1 transcripts. While, enhancing endogenous NO in overexpressing AtCaM (1 and 4) transgenic Arabidopsis thaliana mitigated salinity effects, confirming NO’s role as suppressor of salt stress (Zhou et al. 2016). H2 S plays an integral part in the salinity stress amelioration through its ability to regulate ion homeostasis and redox state management. It’s reported to involve with JIN1/MYC2 TF to maintain physiological balance in salinity stressed Arabidopsis (Yastreb et al. 2020). However, it activates DREB2B alongside salt overly sensitive (SOS) against salt stress as seen in wheat and strawberry (Christou et al. 2013; Ding et al. 2019). But in grapes, exposure to H2 S up-regulates the expression of VvWRKY30 in order to desensitize the plant to high salinity (Zhu et al. 2019). While in barley H2 S adapts NO mediated pathway, transcriptionally regulating Na+ /H+ antiporter (HvVNHX2) along with H+ -ATPase’s β subunit (HvVHA-β), hence maintaining the ion homeostasis (Chen et al. 2015). Data on salinity stress amelioration by H2 S interplaying with NO is well documented. But the exact transcriptional pathway and participants remains to be found out (Srivastava et al. 2022).

4.1.4

Heavy Metal

Heavy metals (HMs) are the transition group elements, and a cause for imbalance in the physiological functioning of plants. Its toxic effects can be observed in the form of erratic growth patterns (Singh et al. 2020). Being sessile, plants adapt to various strategies to counter these effects such as vacuolar sequestration and antioxidant (enzymatic and non-enzymatic) machinery up-regulation. All these actions require intervention of the genetic segments, regulated by the various transcription factors and differentially expressed genes (DEGs) (El-Esawi 2020). Tracking of a master regulator which functions in heavy metal stress tolerance has been tricky. Arabidopsis plants exposed to arsenic (As) regulate the HM by expressing the SLIM1TF which functions by managing the sulfur (Jamla et al. 2021). Cadmium (Cd) stress, follows another pathway, and is alleviated by the activity of MYB4 TFs. MYB4 attaches itself to promoter region of metallothionein 1C (MT1C) and phytochelatin synthase1 (PCS1) providing oxidative protection (Jamla et al. 2021). Lead (Pb) has been reported to be managed by the action of bZIP TFs. While studies on multiple studies report of the members of the WRKY family to be functioning under Cd and Pb stress (Jamla et al. 2021). Furthermore, FER-like Deficiency Induced Transcription Factor (FIT) and subgroups of bHLH along with IRT1 regulates the uptake of

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Ferrous (Fe) in cells. Additionally, IRT1 also function in regulating the uptake of Zn, Mn, Co, Ni, and Cd (Singh et al. 2016b). NO is also reported to help in amelioration of toxic heavy metal stress and regulation of essential heavy metal transport in plants (Terrón-Camero et al. 2019). Cellularly, S-nitrosoglutathione (GSNO), nitrosylated form of glutathione acts as a pool of NO and hence regulates the activation of stress responsive TFs WRKY and MYB against stress (Singh et al. 2017). It is also responsible for improving the expression of transcripts of iron transporters in rice (Singh et al. 2016a). While in Arabidopsis, it also upregulated transcripts of phytochelatin synthase (PCS1-AT5G44070) responsible for regulating the heavy metal stress (Hussain et al. 2016). Upon AsIII exposure, NO-mediated transcriptional modification in rice root was noted; Sodium nitroprusside (SNP) addition showed clear signs of reduced cell death as well as diminishing ROS and As accumulation. It further modulated various stress related genes (CytP450, GSTs, GRXs), TFs, metal transporters ie., ABC, NIP, iron transporters, and NRAMP, along with amino acids, hormone(s), signaling and secondary metabolism genes involved in As detoxification (Singh et al. 2017). H2 S is integrated as one of the central players in the heavy metal stress amelioration in plants. It utilizes various signalling pathways; as gaseous molecule is involved in cross talks with hormones (ABA, IAA, GA, JA) and molecules like H2 O2 , NO, CO and the master signalling component Ca2+ (González-Morales et al. 2021; He et al. 2018). Further, it regulates antioxidative enzymes and various stress triggered transcripts and metal transport proteins (MTs/MTPs). Notably, H2 S manages mercury (Hg) stress in rice through bZIP60 and OsMT-1 transcripts (Chen et al. 2017). While, in foxtail millet it regulates Cd stress through elevated expressions of ZIP4, Ca2+ /H+ exchanger antiporter (CAX2), and MTP1/12along with suppressed action of natural resistance associated macrophage protein (NRAMP1/NRAMP6) (He et al. 2018). H2 S mediated Mn stress alleviation also reports of AtNramp1 suppression and AtCAX2, AtECA1 and AtMTP11 up-regulation (Hou et al. 2022). In response to chromium (Cr) accumulation H2 S activates transcripts of MTs (MT2A, MT3A), phytochelatins (PCs, PCS1, PCS2,) and Ca2+ -mediated signalling (He et al. 2018). H2 S reportedly mitigates Cr and As stress in vegetable crops as well involving glutathione and antioxidant enzymes (Kushwaha and Singh 2020; Singh et al. 2015). Furthermore, it evidently administers against amelioration of various other heavy metals like zinc, aluminium, copper and lead but the microarray and miRNA studies remain to be reported (He et al. 2018; González-Morales et al. 2021).

4.1.5

Heat

Heat stress encompasses agricultural economy as a major abiotic threat. Not only it reduces the crop productivity, it equally damages the global flora on a cellular level. Heat stress is cellularly alleviated by the heat shock proteins (HSPs) such as small HSPs (sHSPs), HSP—60, 70, 90 and 100 and the antioxidant enzymatic systems (Ohama et al. 2017; Li et al. 2018). Though, transcriptionally the central mediator is reported to be HEAT SHOCK TRANSCRIPTION FACTOR A1s (HsfA1s). HsfA1s

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further controls the stress responsive TFs (DREB2A), HsfA2, HsfA7a, HsfBs, and MULTIPROTEIN BRIDGING FACTOR 1C (MBF1C) (Ohama et al. 2017). All these TFs are supposedly regulated by endogenous gasotransmitters such as NO and H2 S (Li et al. 2018; Rai et al. 2020). The available literature reports of NO and H2 S both to modulate plants against heat stress but the molecular mechanisms remain obscure (Li et al. 2018; Rai et al. 2020). They either, directly perform nitrosylation or sulfhydration or get activated through Ca2+ triggers further activating the MAPK transcripts or antioxidant system (Kolupaev et al. 2017; Prakash et al. 2021). Downstream of MAPK, through unknow intermediaries MAPK modulated HSPs and the master heat shock regulator HSFA1, rendering the plant resistance to high temperatures (Li et al. 2018).

4.2 Proteomics Responses Under Abiotic Stress Given the recent disrupted environmental scenario, plant proteomics has become an increasing popular and sophisticated technique. It aids in analysing and differentiating the effect of stressors on cellular proteins in sensitive and insensitive plant species. This is helpful in determining the protein degenerates along with the stress resistant/responsive proteins which may help in producing varieties that effectively combat stress (Patole and Bindschedler 2019). Various techniques used in proteomic are classified into conventional techniques (e.g. Chromatography based techniques, ELISA), advanced techniques (microarray analysis, Two-dimensional difference gel electrophoresis (2D DIGE)), quantitative techniques (iTRAQ, ICAT) and high throughput techniques (X-Ray crystallography and NMR-spectroscopy) (Aslam et al. 2017). Here a list of proteomic responses involved in diverse abiotic stresses has been elucidated on.

4.2.1

Drought

Drought stress degenerates cell membrane, cellular organelles, and proteins. To tackle this, plants activate a variety of proteins which function as cytoprotectants. These proteins are of regulatory and functional nature. However, regulatory proteins encompass various kinases (MAPK, CDPKs, SnRK2) (Feki and Brini 2016). In transgenic rice aquaporins TdPIP2;1 enhanced drought tolerance. The Lea proteins (2 Lea, 3 Lea, 4 Lea) specifically 2 Lea ameliorate drought damage on wheat LDH (lactate dehydrogenase) and β-glucosidase enzymes. Four classes of heat shock proteins viz. HSP70, HSP60, HSP90, and HSP100. Detoxifying enzymes along with various osmolytes such as proline cycle especially perform drought protectant functions (Feki and Brini 2016). Actin plays an incredible role in providing mechanical endurance to plant under water deficit. S-adenosylmethionine synthetase methylates lignin monomer (Singh et al. 2022). Furthermore, proteins such as elongation factor-1, dihydro-lipoyl

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lysine residue succinyl transferase, aminoacylase-1, cysteine synthase, homocysteine methyltransferase, cinnamoyl-CoA reductase, chalcone-flavanone isomerase, 26S proteasome regulatory subunit 6A homologue and protein disulphide isomerase-like provide protection against drought stress in chickpea (Singh et al. 2022). While in rice experiencing drought, accumulation of putative thiamine biosynthesis protein, putative elongation factor-2, putative beta-alanine synthase, alpha-tubulin, and cysteine synthase is reported (Singh et al. 2022).

4.2.2

Cold

Cold stress in plants is caused due to the fall of temperature below an optimum thermotolerance range. Problem starts to arise when the temperature starts to go subzero or below it. This results in the tissue damage as well as proteomic degeneration due to crystallization of internal fluids of plants. Plants regulate various proteins and metabolic enzymes to adapt to these conditions. Of various pathways, cold triggers Ca2+ signaling network, activating MAPK and/or CDPK phosphorylating and calling for further cold acclimatizing responses as seen in rice, the activity of OsCDPK7 (Janmohammadi et al. 2015). Ca2+ signaling associated with membrane binding annexins and members of hypersensitive-induced response (HIR) protein family control and regulate osmotic homeostasis hence maintaining the intracellular ion concentrations (Ghosh and Xu 2014).Stress management demands of high energy to meet which carbohydrate metabolic enzymes are up-regulated, such as phosphoglycerate kinase (PGK), phosphogluconate dehydrogenase, NADP-specific isocitrate dehydrogenase, fructokinase, GAPDH, triose phosphate isomerase (TPI), and cytoplasmic malate dehydrogenase (Ghosh and Xu 2014). Along with these, accumulation of adenylate kinase suggests enhanced ATP generation, signifying functioning of various stress-busting machinery (Ghosh and Xu 2014). Heat Shock Proteins (HSPs), known to function under heat stress, tend to provide protection against low-temperature stress as well, as seen in HSP70 (wheat, rice, barley, maize, pea and sunflower) and Brassica napus (HSP90) (Rasool et al. 2014; Gharechahi et al. 2016). HSP essentially function in the correct folding of the newly synthesized proteins. As cold stress causes misfolding of proteins, HSP regulate these accumulates either restructuring them or discarding them, especially HSP60 and HSC70 (a member of HSP70), are involved in the assembly of proteins synthesized in chloroplast and folding of non-native proteins, respectively. Furthermore, ER located luminal binding protein (BiP) also aids protein structuring during the cold stress, while, enhanced synthesis of Clp protease, aspartic protease suggests active removal of proteins degraded (Rasool et al. 2014; Gharechahi et al. 2016). LEA/COR proteins have been reported to show antifreeze properties; hence, proteomic studies also implicate of their accumulation under cold stress. Especially dehydrins, belonging to the 2 Lea family, such as WCOR410 and WCS120 serve as cold resistance providers (Gharechahi et al. 2016). Other antifreeze proteins such as b-1,3-glucanase, chitinase, PR-4, thaumatin-like protein, have also been

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reported to accumulate in wheat during winters. Along with these, ROS—antioxidative enzymes and enzymes involved in metabolite regulations such as Glutathione S-transferase (GST), glyoxalase I, thioredoxins (Trxs), germin E and oxalate oxidase show up-regulation and cytoprotective roles (Gharechahi et al. 2016).

4.2.3

Salinity

The disturbed flow of ions caused due to the salinity stress is a major degradative source in plants at the omics level. It further results an imbalance in the generation and uptake of variable proteins. Plants regulate varying degree of proteins in response to this. Candidates that were detected using techniques such a 2-DE and iTRAQ labelling belonged mostly to the photosynthetic system, carbohydrate metabolism and oxidative stress response pathway (Aghaei and Komatsu 2013). In rice triose phosphate isomerase, RuBisCo activase, ATP synthase, beta-1,3glucanase, class III peroxidase and 2-cys peroxiredoxin, dehydroascorbate reductase from leaf were reported (Witzel and Mock 2016). Plant leaves possessing cyclophilin were reported to be more tolerant. While root accumulated proteins associated with protein production and polyamines generation and also, reported of a LRR (leucine rich-repeat) type receptor-like protein kinase OsRPK1 (Witzel and Mock 2016). Results of differential gel electrophoresis (DIGE) and iTRAQ, elucidate on 106 and 521 proteins activity, respectively, of which only 58 overlapped in both. 18 differentially expressed proteins associated with anther/pollen wall remodelling and carbohydrate metabolism were further reported (Witzel and Mock 2016). Interestingly, only 65 proteins in wheat regulated under salinity, which functioned during photosynthesis and ROS detoxification. While in barley, differential 2DE features were identified under salinity, 20 and 21 in the root and leaf proteome, respectively. Maize roots display accumulation of cysteine protease, xyloglucan endotransglycosylase and a alichenase-2 precursor in response to salinity (Witzel and Mock 2016). Carrots accumulate Ornithine decarboxylase responsible for Proline biosynthesis, which provides protection against varying stresses (Aghaei and Komatsu 2013). Ca2+ -CaM-Annexin interplay mediating osmotic stress, reportedly display elevated levels under salt-exposure. Furthermore, members of the Rab family of guanosine triphosphate-binding proteins (GTPase) involved in endocytosis and vesicle trafficking, display functioning under salt stress, and implicated in enhanced protein generation as stress response (Parihar et al. 2015). Ferredoxin NADPH reductase such as FtsH like protein showed upregulation in the maize chloroplast. Accumulation of CP47 protein shows salinity defence through D1 photosynthetic protein protection (Parihar et al. 2015). Another enzyme, mitochondrial alternative oxidase (AOX), functioning during cyanide stress response, is also found to be active under salinity stress. Other proteins reported under salinity stress are germinlike proteins (GLPs), cytochrome P450 monooxygenase, glutathione-S-transferase (GST), thioredoxin h (Trx h), and lectins along with the antioxidative enzymes (Parihar et al. 2015).

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Pre-treatments with H2 S and NO significantly alleviated the detrimental effects induced by salinity in ctrus. The proteomic analysis revealed significant alterations in 85 leaf proteins in salinity exposed plants, however they were unobservable in saltstressed plants pre-treated with either H2 O2 or sodium nitroprusside (SNP; a ˙NOreleasing chemical). This study suggests that H2 O2 - and ˙NO-signaling pathways overlap in response to salinity stress and also inferred that leaf proteins oxidation and S-nitrosylation patterns of citrus plant increase in response to stress (Tanou et al. 2009).

4.2.4

Heavy Metal

Heavy metals (HMs) pose as a serious threat to the agriculture world due to their interference with various groups present in enzymes and proteins through chelation. But plants use this to their advantage by associating these HMs with enzymes and proteins (e.g. phytochelatins, metallothioneins, and ferritins) of protective function and sequestering them to vacuoles through ATP-binding-cassette and V-ATPase transporter (ABCC1/2). Enzymes such as ATPases (or CPx-type, P1B-type), cation diffusion facilitator (CDF) family proteins, natural resistance-associated macrophage proteins (Nramp), zinc–iron permease (ZIP) family proteins, and MATE (Multidrug and Toxin Efflux) tend to uptake of HMs (Singh et al. 2016). Under Cd stress, glutamine synthetase (GS) shows enhanced expression profiles, which later forms GSH before forming PC (Hossain and Komatsu 2013). Along with 2,3-bisphosphoglycerate-independent phosphoglycerate mutase, enolase, formyltetrahydrofolate synthetase, NADH-ubiquinone oxidoreductase, putative vacuolar proton-ATPase (Parihar et al. 2019). A quantitative proteomics approach assisted in elucidating differentially regulated proteins from the rice plasma membrane after Cd or Cd-NO exposure making the role of NO during Cd exposure more explicable. Sixty-six differentially expressed proteins were identified, however, the level of phospholipase D (PLD) was significantly changed after Cd or Cd-NO treatment (Yang et al. 2016). While under Cu exposure, proteins of PS II, HSP70 and putative cytochrome and metallothionein proteins were reported to act in defence. In response to As and Hg stress, glycolysis regulating proteins, proteins of pentose phosphate pathway, and of calvin cycle upregulated meeting the extra energy demand (Parihar et al. 2019). Under Zn stress, plants respond with FRO2 (a ferric-chelate reductase), IRT (an iron and zinc transporter), and V-ATPase. Apart from these proteins of S assimilation are also upregulated as also seen in the case of Ni. Exposure to Cr reports accumulation of nitrate reductase, adenine phospho ribosyl transferase, formate, and IMPase alongside photosynthetic and amino acid metabolism enzymes (Parihar et al. 2019). While under Mn, plants respond with differential synthesis and control of inorganic pyrophosphatase, a probenazole-inducible protein (PBZ1), a chloroplast translational elongation factor (Tu), and ribosomal protein (Parihar et al. 2019). Plants also show enhanced expression of protective proteins such as thioredoxin (Trx), Trx-dependent

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peroxidase, NADP(H)-oxido-reductase and glyoxylase I (Gly I) under HM exposure (Hossain and Komatsu 2013). Along with these, the entire family of antioxidative proteins is active under HM stress but is differentially regulated.

4.2.5

Heat

The mildest of fluctuations in the temperature towards higher degrees are known to denature proteins rendering them as dysfunctional. Plant’s sessility restricts them from physical protective measures but, they protect themselves by regulating cellular proteins. Most of these belong to the photosynthetic and oxygen evolving machinery such as RuBisCO, ATP synthase, GAPDH to avoid photoinhibition (Sharma et al. 2019). HSP proteins regulated by HSF transcription factors form the major proteomic response in response to heat (Haider et al. 2022). Analysis on wheat shows upregulation of Harpin binding protein, glycine decarboxylase, ATP synthase, 2-Cys peroxiredoxin BAS1, ribonuclease TUDOR-1, HSP20, HSP 70 and HSC70 (submember of HSP70 family) (Wang et al. 2015; Kumar et al. 2019). While rice displays elevated levels of HSP16.9A, HSP17.4, HSP17.9A, HSP23.2, and HSP26.7, and along with the RING finger ubiquitin E3 ligases (OsHIRP1, OsHTAS and OsHCI1) and ubiquitin-specific protease, OsUBP21 necessary for rescue from accumulated misfolded proteins (Zhou et al. 2019; Xu et al. 2021). Similarly, in radish (Raphanus sativus L.) taproot iTRAQ (Isobaric Tag for Relative and Absolute Quantification) analysis reports high expression profiles of annexin, ubiquitin-conjugating enzyme, ATP synthase (Wang et al. 2018). Studies on Spinach report of the increased antioxidative activities of SOD, GOX, CAT, GR and GST, endomembrane trafficking proteins and lea protein, aldo/keto reductase, jasmonate-induced proteins, lectin, lactoylglutathione lyase, and aldehyde dehydrogenase as heat stress response (Zhao et al. 2018; Li et al. 2019). The proteins associated with heat stress signify the impact it has on the molecular machinery of the plants. Enhanced functioning of the photosynthetic, photorespiration and ubiquitin-associated enzymes signify the protection from photoinhibition, increased energy demand needed to dissipate excessive heat, and removal of degenerant proteins.

4.3 Metabolomics Regulation Under Abiotic Stress Metabolomics is an emerging technique which is being used for qualitative and quantitative analysis of all low-molecular-weight metabolites. Currently, it is has developed into a significant element of systems biology and is being used in disease diagnosis, toxicology, identification of plant metabolites under varying states and other fields.

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Drought

Drought or water deficit is among serious environmental abiotic stresses. It considerably increases oxidative stress, H2 O2 , malondialdehyde, aldehyde content in plant cells that affects physiological performance. However, drought sensitive show increased survival which naturally entail a series of metabolic reactions such as increases synthesis and accumulation of antioxidant enzyme, ROS detoxification, osmolytes (glycinebetaine and proline), carbohydrates, sugars, secondary metabolites synthesis (Shafiq et al. 2014). According to Akram et al. (2018) exogenously supplied NO and plant growth regulator 5-aminolevulinic acid (5-ALA) even at low concentrations, significantly up-regulated biosynthesis, and accumulation of carbohydrates, and osmolytes such as proline and glycinebetaine in canola (Brassica napus L.) plant against drought. Furthermore, NO prominently alleviate drought impact in soybean (Glycine max) plant by the stimulation of tyrosine ammonia-lyase (TAL), and phenylalanine ammonia-lyase (PAL), and enzymes involved in endogenous phenolic compounds synthesis, lipoxygenase (LOX) activity and reduced ion leakage (Rezayian et al. 2020). Altogether NO and polyamines share their beneficial mitigation property reported in Arabidopsis, all through drought stress (Tun et al. 2006). Chen et al. (2016) reported that H2 S is positively involved in modification of most prominent metabolites such as organic amines-polyamines (arginine, ornithine, putrescine, spermidine and spermine) and sugars (glucose, trehalose, fructose, sucrose, etc.) reported in Spinacia oleracea which improved growth and development under water stress. Exogenous H2 S supplement in crosstalk with ABA improves biosynthesis and metabolic expression as drought combat strategy in wheat (Triticum aestivum L) (Ma et al. 2016). The super inductive protecting mechanism of gassotransmitter NO and H2 S assist plants from unpredictable effects of drought stresses.

4.3.2

Salinity

Over few decades salinity stress accounted as major drawback for agricultural production. Bhardwaj et al. (2021) say that under saline condition NO acts through various crosstalk signal transduction networks (H2 S, phytohormones such as ABA, auxin (AUX), jasmonic acid (JA), ethylene (ET), brassinosteroids (BR), salicylic acid (SA) and polyamines) to support various developmental processes (Sami et al. 2018). Fan et al. (2012) reported that NO and ABA synergistically increased proline accumulation in salt tolerance. Furthermore, NO increases accumulation of Na+ ions in Zea mays as a result it exhibits salinity induced ROS overproduction (Kaya et al. 2015). Exogenous H2 S potentially shield rice (Oryza sativa L) plants from salt destruction and consequentially maintain Na+ /K+ ions content in root and leaves respectively. It further increases uptake of K+ and restrain excessive Na+ movement, reestablishing essential minerals, protecting photosynthesis pigment and water-soluble proteins.

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Additionally, H2 S enhance ascorbic acid and GSH at cellular level resulting in lower oxidative metabolism (Mostofa et al. 2015). Similarly, Jiang et al. (2019) examine Na+ /K+ ion balancing through H2 S in cucumber (Cucumis. sativus L). In a mangrove plant Kandelia obovata Liu et al. (2019) examine H2 S to improve ascorbate–glutathione (AsA–GSH) cycle, heat-shock proteins, and chaperonins, nitrogen metabolism, glycolysis process and protract cellular homeostasis against salt tolerance. Furthermore, exogenous melatonin communicates with endogenous H2 S and modulates LCD activity in salt stressed tomato (Solanum lycopersicum L) (Mukherjee and Bhatla 2021).

4.3.3

Heavy Metal

Excessive introduction of metals in the environment such as Cr, Hg, Pb, As, Al act as limiting factors of vegetative growth. Moreover, heavy metals may stimulate cellular injury, impair redox homeostasis, and cause metabolic arrest. Plants combat excess HMs through complex antioxidant mechanisms, functional inhibition by chelation, and regionalization of HM ions. In tolerance to metal stress, plant immunity triggers the synthesis and accumulation of some low-molecular weight metabolites such as amino acids, phenolic compounds, glutathione and organic acids. Notably combined studies of metallic and saline stress reviewed by Anjum et al. (2014) helped to know the glutathione (sulfur rich peptide) and proline (nitrogenous amino acid) had ability to alleviate metallic stress and protect plant cells by maintaining cellular metabolic mechanisms. NO is an important regulator that transduce heavy metal stress interaction. Metal stress-induces NO generation, which results in inactivation of catalase activity in response to Pb stress (Corpas and Barroso 2017) and S-nitrosylation mediated repression of glycolate oxidase by in Cd stress tolerance in pea plant (OrtegaGalisteo et al. 2012). Moreover, NO amend ROS metabolism to copper (Cu) tolerance in Arabidopsis plants (Pet˝o et al. 2013). Recent researches provide evidence that H2 S potentially ameliorated metalloid stress in plants. Exogenous H2 S application triggered antioxidant system, enhanced photosynthetic machinery as well as up-regulated ATPase activity toward alleviating Al-induced effects in barley (Dawood et al. 2012; Chen et al. 2013). Moreover, H2 S is also involved with Ca2+ ions mediated signaling and activate AsA-GSH cycle regulation in response to Cr toxicity in Setaria italica (Fang et al. 2014). According to Kharbech et al. (2017), H2 S application induces antioxidant production and results in reduced Cr accumulation in maize. Singh et al. (2015) reported that H2 S along with partial involvement of NO suppressed As-induced toxic effects through AsA-GST activity in pea.

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Heat

Increasing temperature or heat is a serious climatic condition. Extreme heat has the ability to damage membranes, lipid peroxidation, ROS bursting, pigment destruction, enzyme alteration and reduction of photosynthetic efficiency (Parankusam et al. 2017; Hu et al. 2020). Researches explored about exogenous application of gasotransmitters, phytohormones, and osmoregulants and their beneficial effects to plants against the heat-stress impacts (Chen et al. 2015). Recent study, Iqbal et al. (2022) deduced that during high temperature stress NO dependent ABA-mediated synergistic interactions minimize degradation of photosynthetic pigment, reduces thiobarbituric acid reactive substances (TBARS) level, and development in wheat (Triticum aestivum L.) plants, but at the same time NO/ABA also induced antioxidant metabolism and osmolytes (proline, GB, trehalose and total soluble sugar) accumulation. Similarly, Li et al. (2014) suggested that H2 S enhance trehalose (non-reducing disaccharide) accumulation in maize (Zea mays L.) which protects plant to cope from heat stress. Furthermore, H2 S mediated ABA signaling up regulates physiological response in A. thaliana, Vicia faba (García-Mata and Lamattina 2010) and in tobacco (Nicotiana tabacum) (Li and Jin 2016) during heat tolerance. Both H2 S and pleiotropic signaling molecule melatonin synergistically upgrade photosynthetic mechanism and comprises metabolism of carbohydrate, amino acids and fatty acids that ameliorated heat stress in wheat (Iqbal et al. 2021). Collectively NO and H2 S decrease heat stress mediated glucose sensitivity, oxidative damage via ascorbate–glutathione and up-regulate photosynthesis in wheat (Iqbal et al. 2021).

5 Conclusions Abiotic stress in plants disturbs the ergonomically designed network of energy flow of the entire ecosystem. This proves equally fatal to health and economy. The reports of the studies insinuate gasotransmitters to mitigate the deleterious effect of these stressors at physio-morphological level and also improving growth (Fig. 1). Recent evolving “omics” technologies have helped in identifying few key players involved with these gasotranmitters at genomic, metabolomic, and proteomic levels which take part in abiotic stress tolerance. But more elaborated studies are required to realize the full potential of these gasotransmitters at various levels and the omic players involved for designing more tolerant crop plants. Acknowledgements Dr. Vijay Pratap Singh is thankful to the Science and Engineering Research Board, New Delhi (EMR/2017/000518) for providing financial assistance to carry out this work.

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Advancement in the Biology of Gasotransmitters: H2 S, NO and Ethylene Ekhlaque A. Khan, Akhtar Parwez, Roushan Kumari, and Hamdino M. I. Ahmed

Abstract Recently, there has been a lot of interest in the research of gasotransmitters in plants. In the past two decades, the idea of the “gasotransmitter,” or gaseous signalling molecule, has advanced. It has applications in the regulation of animal and plant physiological processes. Nitric oxide, hydrogen sulphide, ethylene, carbon monoxide, methane, and, more recently, hydrogen gas have all been discovered as important and essential gasotransmitters in a variety of biological processes. Of them, NO has received the most research attention, while hydrogen sulphide and ethylene have received less. The activity of many antioxidant enzymes can be increased, ROS toxicity can be reduced, and plant tolerance to various stresses can all be improved by these gasotransmitters. The link between H2 S, NO, and ethylene gasotransmitters is examined in this chapter in light of their biochemical origins and uses. We also covered how gasotransmitters interact with one another in different plant environments. Gasotransmitters will likely be used in agriculture due to their great potential. The relative significance and interactions between the three primary gasotransmitters also call for further study.

Ekhlaque A. Khan and Akhtar Parwez have contributed equally. E. A. Khan (B) Department of Biotechnology, Chaudhary Bansi Lal University, Bhiwani, Haryana, India e-mail: [email protected] A. Parwez · R. Kumari P.G. Department of Biotechnology, Magadh University Bodh-Gaya, Bihar, India H. M. I. Ahmed Horticulture Research Institute (HRI), Agricultural Research Center (ARC), Giza 12619, Egypt © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_4

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1 Introduction Numbers of studies shown the appreciable application of gasotrasmitters in medicine and biological sciences. The word “gasotrasmitter was firstly coined by Wang in 2002 and furthermore defined in 2012 and 2014 to for small gaseous molecules comprising carbon monoxide (CO), hydrogen sulphide (H2 S), nitric oxide (NO) and other gases (Wang 2002, 2012, 2014). A gasotrasmitter has high solubility in lipid and can passes across cell membrane without a need of precise receptor and transporter. Endogenous gasotransmitters are produced by specialized enzymes and can perform a variety of tasks at physiologically appropriate quantities by interacting with specific cellular and molecular targets. Irregular production and metabolism of gasotrasmitters have been confirmed to be associated with assorted biological process like as immune function, vascular biology, metabolism, cellular survival, durability, growth and stress resistance. Gasotransmitter has well recognized function by regulating vascular dilation in the vascular system and contraction in both Nitric oxide (NO) and hydrogen sulphide (H2 S) as endothelial derived endothelium-derived relaxing factors or hyperpolarizing factors (Wang et al. 2009). A study confirmed that gasotransmitter action in maturation of oocytes and development of early embryonic in many animal species including mammalian models, Xenopus and sea urchin pointing to the important gasotransmitters role in beginning of life (Nevoral et al. 2016). They advised that gametogenesis of gasotransmitter can happen through modification of cysteine residue of target protein, with development of persulfides and nitrosothiols. Recently suggested that CO, H2 S, NO and SO2 (Sulphide dioxide) has to be a potential gasotransmiter. A study detailed to investigation into SO2 role in vascular structural remodelling (Liu et al. 2016). SO2 can regulate remodelling through affecting smooth muscle, apoptosis and proliferation, balance among tissue inhibitors enzyme metalloproteinase and matrix metalloproteinase, the TGF beta1/Smad2/3 pathway, oxidative stress, and after this, all of which are associated with hypertension pathogenesis. The study also suggested that more clinical evidence or data is required to support the possible healing target for Sulphur dioxide in cardio vascular disease. Since the past twenty years, gasotrasmitters drawn extensive attention because it controls the stomatal closure and boost innate immunity response against biotic and abiotic stress (Scuffi et al. 2016; Yao et al. 2019). Nitric oxide, carbon oxide and hydrogen sulphide are some examples that stimulate stomatal closure. Some important characteristics of gasotrasmitters are small size, freely across the membrane no requirement of receptors. It performs its function at physiological relevant concentration, produce endogenously and enzymatically. It may or may not effected by secondary messenger but have specific cellular and molecular targets (Wang 2002). This article presents an account of gasotrasmitters operating in plants, with an emphasis on NO, H2 S, and Ethylene. In addition, note the interactions of gasotransmitters with each other, and with other signaling molecules. To conclude, remarks are also made to highlight the need for further research on this fascinating topic.

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2 Gasotransmitters: An Overview In 1977, NO the first gasotransmitter was discovered. After 25 years, the gasotransmitter was conceptualized. It took about another 15 years for the gasotransmitter family to expanded to include NH3, NO, H2 S and CO. High production of various atmospheric gases from anthropogenic activities natural resources, cause major environmental problems that have a negative impact on health. H2 S, NO, and CO are pollutant gases. Many studies advocated that gases like H2 S, CO and NO are generated in the human body and also play significant physiological roles. These precise gases share and act similar in their production and function in many respects but carry on their task in unique which different from classic signaling molecules in human. The family of gasotransmitters, made up of the words “gas” and “transmitter,” these are endogenous gas molecules or gaseous signalling molecules. Cellular function are significantly impacted by the control of ions channels by gasotransmitters, whether directly through chemical modifications of ion channel protein or indirectly through second messengers. H2 S, NO, and Co may directly interact with ion channel proteins through the processes of S-nitrosylation, carboxylation, and sulfuration, respectively. For intercellular communication, vehicles are electrical signaling through chemical substances or electrical signaling. The category is made up of transmitters autocoids and hormones. Hormones are released from endocrine cells in to blood stream. Endocrines cells are produce hormone in the blood. When hormones reach to several distant cells and organs, their concentration is diluted to a comparatively steady level. When transmitters are released, they often operate on postsynaptic cells that are nearby. This is a distinction between the endocrine and paracrine actions of transmitters. Autocoids generally (like platelet-activating factor, adenosine and prostaglandins) effect on the identical cells from which they are produced. The biological effects of autocoids still require cognate membrane receptors, much as the effects of hormones and transmitters. Therefore, modifying the plant’s redox homeostasis is a crucial component of resistance to abiotic stress. Plants have develops mechanism for perceiving external signals and enacting adaptive response with the appropriate physiological and morphological changes in order to adjust to such challenges (Liu et al. 2010). Gasotransmitters are tiny gas molecules that are made by organisms and used to communicate biological signals. With the rapid advancement of gasotransmitter research, we are learning more about their potential uses in biology and medicine (Wang 2014). Gasotransmitters that control specific biological processes include nitric oxide (NO), hydrogen gas (H2 ), hydrogen sulphide (H2 S), carbon monoxide (CO), and methane (CH4 ). Over the past couple of decades, a great deal of research has been done on the biological applications of these signalling molecules’ functions.We currently have a better grasp of new gasotransmitter signalling pathways mainly to the extensive study and analysis of endogenous gasotransmitter emissions in plants. According to earlier research, plants typically create these gasotransmitters in response to abiotic

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stresses (Abdulmajeed et al. 2017; Cui et al. 2017; Jia et al. 2018). Additionally, there is now a lot of proof that gasotransmitters can be crucial in improving plant tolerance (Abdulmajeed et al. 2017; Maryan et al. 2019; Xu et al. 2017). Therefore, biological gases from intricate extracellular and intracellular pathways and gas mediators may negatively or positively influence a variety of functions.

3 Advancement in H2 S Synthesis and Its Applications H2 S act as a signaling molecules that focused on capacity to act together with –SH (thiol) group found in protein cysteine residues by PTM (post translational modification) persulfidation (Corpas et al. 2019; Aroca et al. 2018). H2 S competes through additional molecules, like as fatty acids, cyanide, nitric oxide (NO) and glutathione (GSH), which generate the PTMs S-nitrosation (Corpas et al. 2019; Astier et al. 2012), S-cyanylation (García et al. 2019), S-glutathionylation (Zaffagnini et al. 2012; Diaz-Vivancos et al. 2015) and S-acylation (Li and Qi 2017; Zheng et al. 2019) respectively. Experimental evidence shows that the use of H2 S at different developmental phases can mitigate the effects of abiotic stress and improve physiological aspects for instance root growth, seed germination, and vegetable post-harvesting prevention to many plant species (Corpas et al. 2019). In grapevine (Vitis vinifera L.) plants, exogenous application of H2 S causes gene expression involved in the creation of secondary metabolites besides a number of defensive chemicals that boost plant development and abiotic resistance (Ma and Yang 2018). Additionally, 5349 genes were found to be up-regulated and 5536 genes to be down-regulated in tomato plants supplemented with NaHS, according to microarray analysis of differentially expressed genes (Guo et al. 2018). The precise biochemistry of endogenous H2 S in plant cells, along with the locations and procedures involved in its creation and interactions with other molecules in metabolism, is still a relatively new field of study. Numerous enzymes involved in cysteine metabolism are present in subcellular spaces in higher plants, including the chloroplasts, peroxisomes, mitochondria, and cytosol, where H2 S is produced (Corpas et al. 2019). These enzyme comprises cyano alanine synthase (CAS) and L-cysteine desulfhydrase (L-DES), L-cysteine desulfhydrase 1 (DES1), previously known as Cys synthase like (CS-LIKE) in mitochondria; and sulfite reductase (SiR) in chloroplast (Filipovic and Jovanovic 2017; Liu et al. 2019a). Although, H2 S can easily spread all over the lipid bilayer of cell membranes due to its high lipophilicity (Cuevasanta et al. 2017). Some data revealed by what means events like as cysteine desulfhydrase in few of these enzymes are down regulated by blue and white light and up regulated under red light (Liu et al. 2019b). However, exogenous application has been done utilising substances that can provide H2 S. Different chemical families that have the ability to gently release H2 S into cells have been produced for use in biomedical applications in animal research.

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As a result, water-soluble compounds such as the family of cysteine-activated H2 S donors have been created and (p-methoxyphenyl) morpholino phosphinodithioic acid (Zhao et al. 2011). In some plant research, chemicals that are comparatively more expensive to generate than common chemicals like sodium hydrosulfide (NaHS) and inorganic sodium polysulfides (Na2 Sn) like Na2 S4 , Na2 S2 , and Na2 S3 have been utilised (Yamasaki et al. 2019). These polysulfides’ ability to transport H2 S in aqueous solution is therefore dependent on the medium’s pH and related pKa (Gun et al. 2004), less expensive exogenous additions of NaHS are made to hydroponic solutions, in vivo growth media, or plants themselves. NaHS is a temporary donor that can be used in a range of concentrations, but it cannot mimic the in vivo process of H2 S creation, which is constant and progressive. A recent study found that after 4.5 weeks of treatment, the H2 S-releasing substance dialkyldithiophosphate can enhance maize plant weight by up to 39 (Carter et al. 2019). Another chemical that can simultaneously release NO and H2 S is used in pharmaceutical anti-inflammatory therapies (Kashfi et al. 2015). It is generally recognised that a variety of unfavourable factors have a detrimental impact on plant development, production, and growth (Mantri et al. 2012). According to the type of stress and the implicated plant species, plants have created a variety of techniques to mitigate these effects. Numerous times, these stresses are caused by an excessive amount of reactive oxygen and nitrogen species (ROS/RNS) being produced uncontrollably. This can result in nitro-oxidative stress, which is characterised by an increase in important variables like protein tyrosine nitration, lipid peroxidation, and oxidative damage to proteins and nucleic acids (Corpas and Barroso 2013). There is very little information known about endogenous H2 S metabolism in fruits and vegetables. Endogenous H2 S levels have recently been observed to increase in non-climacteric sweet pepper (Capsicum annumm L.) fruits as they age from green immature to red ripe (Muñoz-Vargas et al. 2018). Although, Studies studying the financial impacts of biotechnological H2 S applications on fruit ripening and postharvest storage, which reduce the loss of fresh product due to virus, bacteria, and fungi and low temperatures used to keep vegetables and fruits, have increased over the past ten years. Exogenous administration of H2 S would extend the shelf life of numerous types of fruits, vegetables, and flowers (Ge et al. 2017; Muñoz-Vargas et al. 2018). Another typical reaction to exogenous H2 S treatment is an increase in the antioxidant system, which avoids ROS overproduction and subsequently oxidative damage. A significant source of nitrogen-fixation in both natural ecosystems and agriculture occurs during the creation of nodules during the interaction between plants and rhizobia (Mahmud et al. 2020). H2 S appears to play a variety of roles in this process as well as the NO, which was seen to be active in the rhizobium-legume symbiotic interactio (Puppo et al. 2013; Hichri et al. 2015; Berger et al. 2020). Recently reports indicate that exogenous H2 S stimulates growth of plants, activity of nitrogenase and nodulation in the functional

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symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii) plants (Zou et al. 2019). Furthermore, by controlling linked enzymes at various levels (gene expression, activity, and protein), as well as a senescence-related gene that was controlled, rhizobia and soybeans were able to improve their nitrogen contents (Zhang et al. 2020). Additionally, recent findings from the Mesorhizobium-Lotus symbiosis suggest that the relationship is controlled by the cross-talk between H2 S and other signalling molecules, such as ROS and NO (Fukudome et al. 2020).

4 Advancement in NO Synthesis and Its Applications Animals have a well-known regulated NO production and signalling mechanism. Despite the discovery of nitric oxide synthase (NOS)-like activity in numerous plant species, fundamental questions about NO production in plants remain unanswered (Weisslocker-Schaetzel et al. 2017). For the first time in plants, confirmed nitric oxide synthase synthase (NOS)-like activity. After that, enzymes have consistently been promoted as plant inputs that contribute to nitric oxide generation. As an illustration, there have been reports of the nitric oxide synthase enzyme being active in the peroxisomes of various plant and algal species, such as Ostreococcus tauri and Ostreococus lucimarinus. Nitric Oxide Associated 1 (AtNOA1), which encodes a GTpase and was discovered to be indirectly implicated in nitric oxide synthesis in Arabidopsis thaliana (Fancy et al. 2017). It is questionable whether higher plants have nitric oxide synthase-like activity, hence coordinated efforts are required to find the enzyme homologs of nitric oxide synthase in plants. Currently, nitric oxide generation in plants has been confirmed by both reductive and oxidative pathways because there hasn’t been any experiment or proof demonstrating the direct participation of the nitric oxide synthetase enzyme in plants. Well-known reductive mechanisms for NO generation include nitric reductase (NR) routes and mitochondrial or plasma membranes connected to proteins. However, there are already established oxidative mechanisms for nitric oxide generation, including L-arginine or polyamine and hydroxylamine mediated routes. Nitric oxide is produced through a reductive pathway that is dependent on the presence of nitrites as the primary source. NR catalysed the reduction of NO3 – (nitrate) to NO2 – nitrite and then to NO (Sakihama et al. 2002; Rockel et al. 2002). As a result, it is typically assumed that the activity of the nitric reductase enzyme directly correlates with the rate of nitric oxide generation. However, nitric oxide synthesis from plants with no NR activity has also been documented (Lozano-Juste and Leon 2010) demonstrating the existence of NR-independent mechanisms. The processes including nitrate reductase are well understood routes through which NO is produced in plants. The enzyme NR is responsible for reducing nitrate to nitrite. In Arabidopsis, the NIA1 and NIA2 genes encode a nitrate reductase that is capable of converting nitrite to nitric oxide (Gupta et al. 2011).

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Depending on the endogenous mechanism, nitric oxide can be produced using only 1% of the nitrate reductase capacity that is active in vivo. The relevance of these nitric reductase enzyme-mediated pathways was brought to light in the double knockout nicotiana benthamiana (tobacco) mutant lacking nitrate reductase, which resulted in lower levels of nitrate oxide and nitrite and substantially hampered plant development (Planchet et al. 2005). Nitric oxide is a crucial second messenger that is known to control a number of activities including physiological and developmental responses in plants. It regulates how plants react to a variety of abiotic factors, including heavy metal stress, excessive salinity, extremely high or low temperatures, osmotic stress, light and UV-B exposure, and oxidative damage. Studying the potential for crosstalk between these chemicals was motivated by advances in our understanding of the interactions between secondary messengers like H2 S and NO in the plant’s system and their equivalent roles in the animal system. Numerous investigations have noted the connection between H2 S and NO. NaHS (100 m) and NaCl (100 mM) treatment of alfalfa seeds raises the levels of nitric oxide by 30%. This included an increase in the Na+ /K+ ratio, transcript levels for the genes encoding catalase, guaiacol peroxidase, super oxidase dismutase, and APX, as well as a decrease in the reduction of lipid peroxides. Nitric oxide scavenger therapy reversed the effects of NaH2 on alfalfa, demonstrating how H2 S donor affects endogenous nitric oxide levels (Wang 2012). Recently, it has been discovered that gaseous signalling molecules like H2 S and nitric oxide play a crucial part in the development of stress tolerance. H2 S and nitric oxide can diffuse quickly because they are gaseous and tiny enough to pass through cellular membranes and reach intracellular destinations without the aid of carriers or transporters. However, it’s possible that the cellular signalling system between cells originated before the appearance of recently recognised cellular receptors (Domingos et al. 2015). Depending on their respective concentrations in the plant, nitric oxide and H2 S both have antagonistic or cooperative effects. Studies on various tissues, species, or levels of stress conditions supported the idea that H2 S and NO have complex biological relationships and may be engaged in a variety of processes (Corpas et al. 2019). Persulfidation and S-nitrosation are two examples of post-translational modifications (PTMs) that are known to involve both H2 S and NO (Aroca et al. 2018). In the end, research done to understand the function of S-nitrosation suggested that NO-mediated protein persulfidation might be directly engaged to give a fortification against over-oxidation (Aroca et al. 2018; Filipovic 2015). An extensive investigation in Arabidopsis revealed that 612 proteins combine both PTMs, while 929 proteins experience S-nitrosation and 2330 proteins suffer persulfidation (Aroca et al. 2017; Hu et al. 2015). Over the past few years, evidence of heavy metal stressors among the abiotic variables influencing plants has grown. Any relatively high-density metallic element that is toxic or poisonous to cells even at low concentrations is referred to be a heavy metal. The plant has implemented defence mechanisms such chelation, sequestration, enhancing the antioxidant system, and regulation of metal intake by transporters in order to endure the stress caused by heavy metals. Numerous investigations have separately confirmed that the exogenous use of NO and H2 S donors can reduce metal stress. Crosstalk between NO and H2 S in metal stress tolerance has been discussed

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in recent works. Different plant species’ endogenous nitric oxide concentrations are reported to rise, fall, or remain unchanged after being exposed to aluminium (Al). These variations suggest that various plant species may exhibit different types of Al-induced signalling. Treatment with NO donor (SNP) reduced oxidative stress and enhanced Al toxicity in wheat, soybean, kidney bean, Cassia tora, and other plants (Wang et al. 2019). H2 S works by reducing the activity of rice PMEs, which reduces the negative charge in the root cell walls. Similarly lowers pectin and hemicellulose levels as well as PME activity in roots. Additionally, this action reduced Al binding by boosting citrate secretion and triggering the expression of OsFRDL4, clogged Al-binding sites in the root cell walls, and elevated the expression of OsSATR1 and OsSTAR2 in roots. Cadmium stimulates the expression of the H2 S biosynthesis genes LCD and DES1 in Arabidopsis thaliana, raising the amount of H2 S.Through stimulation of cysteine synthesis in conjunction with the genes SAT1 and OASA1, H2 S increases the quantity of cysteine. The cycle of cysteine and H2 S boosts antioxidant activity, activates PC and MT gene expression, and prevents Cd2+ toxicity (Jia et al. 2018). When Cd is exposed in alfalfa, LCD and DCD expression are promoted as first reactions, which afterwards cause roots to have higher H2 S levels (Cui et al. 2014). By inhibiting the activity of the enzymes NR and DES, respectively, arsenate (AsV) supplementation lowers the levels of NO and H2 S. According to hydroponic tests, AsV decreased photosynthesis, growth, and nitrogen content in pea seeds. The ascorbate glutathione cycle’s activity is impacted by the AsV treatment. Due to the increased level of ROS, it also caused damage to proteins, lipids, and membranes. Exogenous NaHS administration enhanced NO and H2 S levels, restored glutathione and ascorbate’s redox status, decreased ROS-induced damage, and decreased AsV poisonousness in pea seeding (Singh et al. 2015).

5 Advancement in Ethylene Synthesis and Its Application Ethylene gas is a plant hormone that is crucial for plant development and stress reactions throughout the plant life cycle. It is a simple hydrocarbon that is very important in agriculture, particularly in the climacteric ripening of fruit. Additionally, it is the most widely manufactured hydrocarbon in the world and is recycled to make a variety of goods, including rubber, paint, detergent, and toys. Through the entire plant life cycle, it arbitrates a variety of complex aspects of a plant’s growth, development, and existence, including seed germination, shoot and root growth, adventitious root formation, abscission of leaves and fruits, flowering, sex determination, and senescence of flowers and leaves (Filipovic and Jovanovic 2017; Ge et al. 2017). Additionally, ethylene supports adaptive responses to a variety of stressors, including pathogen assault, excessive salinity, drought, and flooding (Hou et al. 2013).

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Fig. 1 Ethylene biosynthesis pathway

6 Ethylene Synthesis Pathway Ethylene is a gaseous and volatile plant hormone that effects plant growth and expansion, and also help to cope various type of stress and infection (Xu and Zhang 2015). Its biosynthetic process is very straightforward, involving only two specific enzyme activities (Fig. 1). The enzyme ACC synthase transforms the substrate Sadenosyl-L-methionine (SAM) into ACC and 5' methylthioadenosine (MTA) in the first step (ACS). The enzyme ACC oxidase (ACO) transforms ACC into ethylene, CO2 , and cyanide in the second step (Hamilton et al. 1991). A group of -cyanoalanine synthases quickly increase the toxicity of the cyanide by-product with the version of -cyanoalanine (Hatzfeld et al. 2000). ACC homeostasis, which includes ACC biosynthesis, transport, and conjugation, controls ethylene production (Pattyn et al. 2021).

7 Ethylene and its Application The major application of ethylene is as follows:

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7.1 Leaf Senescence The most important hormone for controlling leaf senescence among all other plant hormones is ethylene, which plays a crucial role in the process. Senescence can be triggered by it, especially in sensitive species. Its concentration rises during the first stage of leaf development, falls until the leaf is fully extended, and then rises once again during the first stage of senescence start. Only senescing leaves exhibit an increase in ACC content, which follows the same pattern of ethylene synthesis (Bakshi et al. 2015).

7.2 Flower Development The ethylene concentration affects the genetic programming that participates in several signalling pathways, which affects flower timing. By comparing the growth of the ethylene-related mutants eto1, etr1, ein2-1, and ein3-1 to that of the wild-type (WT), it was possible to determine how ethylene regulates the change from vegetative to reproductive growth in Arabidopsis (Ogawara et al. 2003).

7.3 Fruit Senescence One crucial trait is the fruit’s ability to soften. Cell wall breakdown is triggered by several enzymes that work together to activate this process, which leads to cell wall breakdown. The pectin methyl esterase, cellulose, galactosidases, pectate lyase (PL), xyloglucan transglucosylase/hydrolases, and expansins are among these enzymes. These enzymes are almost all controlled by the multi-gene family, which regulates the spatial–temporal stimulation of these enzymes. During ripening and senescence, ethylene regulates these genes and enzymes in a crucial manner (Qin et al. 2019).

7.4 The Interplay Between H2 S, NO, and Ethylene Plant growth is impacted by the several abiotic stresses (heat, drought, cold, and salinity) that are present in the field. Methionine is created through the S-assimilation reaction, and S-adenosyl methionine uses it as a precursor to create ethylene (SAM). Plant cells also produce hydrogen sulphide (H2 S) as a byproduct of the assimilatory sulphate process. In the plastid, the process of reduction converts active sulphate to sulphite, which is then reduced into H2 S by sulphite reductase. O-acetylserin thiol lyase catalyses the reaction in which O-acetylserin (OAS) and H2 S are joined to create cysteine

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(OASTL). It is possible for cysteine to break down into H2 S and OAS in this reversible process (Filipovic and Jovanovic 2017). Cystine is a methionine precursor chemical that finally converted to ethylene through SAM. As a result, there may be connections between the tolerance mechanisms brought on by sulphur, H2 S, and ethylene under heat stress. Fascinatingly, it has also been found that the emerging gasotransmitter H2 S plays important roles in abiotic stress tolerance; additionally, it appears to typically work through influencing the activity of ethylene (Hou et al. 2013; Liu et al. 2019a, b). The effect of ethylene on banana ripening has been proven to be reduced by H2 S (Ge et al. 2017), and ethylene combined with H2 S has recently been discovered to potentially reduce hexavalent chromium toxicity in two pulse crops (Husain et al. 2022). Currently, Liu et al. showed that ethylene-induced stomatal closure, nitrate reductase (NR) activity, and nitric oxide synthase (NOS) inhibitor L-NAME had negligible effects on ethylene-induced NO generation are all part of H2 O2 -regulated nitric oxide (NO) production (Liu et al. 2009). It has been demonstrated that transient changes in calcium and cytoplasmic alkalinity enhanced NO production in ethylene-induced stomatal closure (Liu et al. 2010; Liu and Xue 2021). L-alanine and elemental sulphur, or H2 S, are produced from L-cysteine through the catalytic action of cysteine desulfhydrase. Two possible mechanisms for this process exist: enzymatic release of elemental sulphur from L-cysteine and nonenzymatic reduction of L-cysteine or dithiothreitol to sulphide. A recent review study noted that increasing plants’ production of the gas H2 S has been found to reduce the damage caused by disease attacks (Liu et al. 2010). The role of H2 S as a signal molecule during regulated stomatal movement is still up for debate. NO signals may have assisted in the production of adventitious roots caused by H2 S, and H2 S may act upstream of NO signal pathways (Zhang et al. 2020). By interacting with ROS and other signalling molecules like NO, micro levels of H2 S can play a signalling role during abiotic stress adaption, growth and development, and crucial plant physiological activities. Numerous studies suggest that NO is an important messenger in plants and that it interacts with H2 O2 in the signalling network of guard cells (Jannat et al. 2020; Wang et al. 2019). A pharmacological strategy was utilised by Garc´ıa-Mata and Lamattina (2001) to demonstrate that NO donors promote stomatal closure in both monocots and dicots. It was confirmed that NO and H2 S both contribute to the ABA-induced stomatal closure process, with NO acting downstream of H2 S (Scuffi et al. 2016). The improvement in nitrate reductase and glyoxalase I and II activities as well as the suppression of S-nitrosoglutathione reductase activity by H2 S may be the causes of the increase in NO (and total Snitrosothiols) (Cheng et al. 2018; Janicka et al. 2018; Che et al. 2015).

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8 Conclusion Gasotransmitters, such as H2 , H2 S, NO, CO, ethylene, and CH4 , have gained for importance in the study of stress throughout time, and significant research has been done in this field. According to the reports that are currently accessible, these gasotransmitters are emitted in plants under various unfavourable circumstances. Importantly, these gasotransmitters increase the ability of plants to withstand a range of environmental stimuli. They do this primarily by controlling the activity of antioxidant enzymes, reducing oxidative stress and lipid peroxidation, maintaining ion homeostasis, and restoring GSH homeostasis. Additionally, in challenging conditions, interactions between gasotransmitters have been demonstrated in plants. Future research on the biosynthesis of these gasotransmitters should concentrate on the molecular specifics of their production pathways in plants, despite the fact that a growing body of evidence suggests that plants may synthesise gasotransmitters under stress. The complex mechanisms underlying their reactions to abiotic stimuli continue to be of significant interest. Because of this, future research on gasotransmitters in plants should focus on their molecular mechanisms and how they interact with one another when they are exposed to abiotic stress. What are these gasotransmitter receptors in plants is a further unanswered topic. Proteomics research has so far demonstrated that NO causes the target protein to undergo three post-translational modifications: metal nitration, tyrosine nitration, and S-nitrosation. Additionally, H2 S may directly alter the thiol groups in proteins, and these groups have an impact on how cells function. Other gasotransmitters’ targets proteins, however, are still unknown. Additionally, as these gasotransmitters are crucial for plant resilience, additional study should be done in the field, with the goal of improving agriculture’s productivity and quality.

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Hydrogen Sulfide: An Evolving Gasotransmitter Regulating Salinity and Drought Stress Response in Plants Shilalipi Samantaray and Kanchan Kumari

Abstract Hydrogen sulphide (H2 S) is a reactive signaling molecule that plays significant activities in biological and physiological processes that occur over the course of a plant lifecycle. Numerous successes have been reported regarding H2 S’s ability to activate a cascade of biochemical events that reduce environmental stress when combined with other signal molecules. Plants can naturally create and emit H2 S, specifically when exposed to exogenous cysteine, sulphate or sulfite. This is true despite the gas’s toxicity. This is assumed to be a method for dissipating excess sulfur, although some unfavorable environmental factors, such as salinity and drought, can also increase the endogenously produced rates of H2 S emissions. As an illustration, the regulation of reactive oxygen species (ROS), the activation of the antioxidant system, the accretion of osmoprotectants in the cytoplasm, the orientation of Na+ cell extrusion and K+ uptake and vacuolar compartmentation are all H2 S-stimulated metabolic reactions that takes place in plants in response to drought and extreme salinity. Overall, the study suggested that H2 S has versatile functions in plant as signal molecule, can ameliorate environmental restrictions through the coordinated control of different defense components, offering up novel paths in the area of biochemical priming study toward the application of target-selected chemicals for stress tolerance augmentation.

S. Samantaray Department of Biotechnology, MITS Institute of Professional Studies, Affiliated to Berhampur University, Rayagada, India K. Kumari (B) Department of Botany, A.N College Patna, Patliputra University, Patna, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_5

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1 Introduction Hydrogen sulfide (H2 S) is well-thought-out as third member of the budding family of gas transmitters after nitric oxide and carbon monoxide. Once regarded as a noxious molecule by asset of its disagreeable smell of rotten eggs (Zhang et al. 2011). One of the eminent mechanisms for H2 S toxicity includes inhibition of a crucial enzyme in the mitochondrial respiratory chain, cytochrome c oxidase. This poisonous chalcogen-hydride gas is predominantly present in the atmosphere and metabolized by bacteria and archaea. In aqueous solution, it may be ionized to produce H+ , HS− , and S2− . Though, HS− is unable to pass through the cell membrane, H2 S is readily soluble in lipophilic solvents and can infuse freely into the lipid membrane; but it cannot travel long distance due to poor water solubility. However, SO4 2− and sulfur compounds are valued for endogenous H2 S metabolism by long distance transport through xylem in plant cells. Now, significant evidence shows that H2 S and its crosstalk with other molecules play a critical functions in several aspects of physiological and metabolic process in plant (Raja et al. 2020; Chen et al. 2015). A appraisal of relevant literature finds a wide variety, spanning melatonin and water (i.e., hydropriming), reactive oxygen–nitrogen–sulfur species (RONSS), salicylic acid, hormones, and even amino acids like proline, reactive oxygen species, such as H2 O2 , reactive nitrogen species, such as NO, and reactive sulphur species, such as H2 S, are of special relevance because they are crucial molecules engaged in cellular signaling mechanisms and gene regulation throughout stress, and they play an important role in plant stress acclimatization (Mostofa et al. 2015; Iqbal et al. 2021). In plants, multiple enzymatic systems assist in the synthesis of H2 S, which primarily occurs in the chloroplast and partially cytosol and mitochondria.

2 H2 S Function in Plant The function of H2 S in plants has been highlighted in Fig. 1, numerous reports related to diverse physiological process and metabolism of plant includes germination of seed, organogenesis of root, and stomatal shutting/aperture (Papanatsiou et al. 2015), fruit ripening (Mukherjee and Corpas 2020), controlling in photosynthetic apparatus (Chen et al. 2011), and autophagy regulation (Laureano-Marin et al. 2016), altering gene expression and enzyme activities. H2 S production is stimulated by biotic and abiotic stress to give protection against pressures such as oxidative challenges (Fang et al. 2016), drought tolerance (Li et al. 2012; Shen et al. 2013), osmotic and saline stresses, and is even obliging for protection against diseases. Furthermore, amply of attainments have been proclaimed regarding H2 S utilization in combinuation with additional signal molecules including nitric oxide (NO), abscisic acid (ABA), calcium ion (Ca2+ ), hydrogen peroxide (H2 O2 ) to mitigate environmental damage (Mukherjee and Corpas 2020).

Hydrogen Sulfide: An Evolving Gasotransmitter Regulating Salinity …

Physiological Functions in Plants

Response to abiotic stress

Seed Germination Root organogenesis Photosynthesis Stomatal movement Fruit ripening Nodulation and Nitrogen fixation Leaf senescence

Low temperature stress Heat stress Drought Osmotic stress Salt stress Hypoxia stress Heavy metal stress (Al, Cd, Cr, Pb, Co, As, Ni)

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Crosstalk between other molecules NO (nitric oxide) ABA (abscisic acid) SA (salicylic acid) JA (jasmonic acid)

Ca2+ (calcium ion) Pro (proline)

H2O2 (hydrogen peroxide) MT (melatonin)

Fig. 1 An overview of the key pathways involved in H2 S biosynthesis in higher plants

Since 1978, the emission of H2 S was discovered in the leaves of cucumber, maize and soybean (Wilson et al. 1978). The concentration of H2 S is more in older plant leaves than younger plants. This study was proved by gradual elevated mRNA levels of enzymes Cys desulfhydrases (CDes) in development stage (Rennenberg and Filner 1983). H2 S helps in the adventitious root’s formation (Mukherjee and Corpas 2020). In soil, H2 S generated by microorganisms is poorly absorbed by roots due to its low solubility in water. So, the maximum H2 S accumulates due to endogenous synthesis in root cells. In a study it was found that low concentration i.e., ≤ 40 μmol L−1 of H2 S support formation of adventitious root in cucumber and growth of radicles in pea and high endogenous concentration of H2 S (≥200 μM) have an inhibitory impact on primary root growth due to extreme ROS production (Zhang et al. 2017). Li et al. presented that using H2 S inhibitor or scavanger; Propargylglicine (PAG) and Hypotaurine (HT) significantly reduced the number of lateral root (Li et al. 2014b). H2 S also plays pivotal roles in photosynthetic efficiency of plant. It increases the leaf chlorophyll content for example spinach, by changing the chloroplast structure through regulating rubisco activity and redox alteration of sulfhydryl compound (Chen et al. 2011), H2 S has the ability to disrupt disulfide connections in photosystem proteins in leaves of yellow bean and formerly reverse the process (Hu et al. 2015). A study in Spinacia oleracea seedlings demonstrated that photosynthesis could be promoted by H2 S through, biogenesis of chloroplasts, thiol redox modification, and expression of photosynthetic enzymes (Chen et al. 2016). H2 S signaling regulated stomatal movement in response to stress conditions. Recent reports have conveyed that H2 S is accountable for closure of specialized guard cell in A. thaliana under drought stress relief. Similarly, these remarks are constant with a preceding study in both Vicia faba and Impatiens walleriana (Gotor et al. 2010). Contrary to above finding, a group of scientists reported stomatal opening in A. thaliana and Capsicum annuum induced by H2 S through decreasing the NO buildup in guard cells (Lisjak et al. 2011).

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3 H2 S Biosynthesis in Plants Hydrogen sulfide, gaseous signaling molecule is recognized as versatile regulator in several plant physiological roles such as photosynthesis, stomatal conductance, adventitious root organogenesis and germination (Duan et al. 2015; Jin and Pei 2015). De Cormis in 1968 was first to observe H2 S emission in plants (Rennenberg 1989). Wilson and co-workers reported H2 S emission in plants; including corn, pumpkin, cantaloupe, cucumber and soyabean on exposure to heat (Wilson et al. 1978). Plants absorb S elements via two different pathways., first specifically, by the root uptake and second by stomata through gas exchange (Notni et al. 2007) (Fig. 2). In agricultural ecosystems, sulfate fertilizer is widely applied source of sulfur in soil and plants absorb the majority of the S from the soil as SO4 2− (Wainwright 1984; Rennenberg 1989). Several types of proton/sulfate transporters, for example SULTRs (H+ /SO4 2− co-transporters) have LAST (Low affinity transport proteins), HAST (High affinity transport proteins), and multigene family expresses them in root epidermal cells (Buchner et al. 2004). Then, the SO4 2− is encumbered into the xylem vessels and disseminated into the whole plant (Leustek et al. 2000). Current studies show that intracellular synthesis of H2 S through in plant cells are cytoplasm, mitochondria, vacuole and chloroplast (Fig. 3). H2 S production in plants, occurs via the sulfur assimilation pathway. In chloroplast, H2 S is generated as an intermediary in the sulphur absorption route and perform as a signaling particle in plants to influence cellular metabolism. Whereas, in mitochondria it performs as an effective pollutant that primarily marks respiration (Birke et al. 2015). The concentration of H2 S is approx. 55 μM in cytosol, which is comparatively lower as compared to chloroplasts (125 μM). H2 S present inside organelles is alkaline in nature due to its ionized form.

O-acetylserine (OAS) Cysteine O-acetylserine (thiol) lyase (OAS-TL) D-cys

L-cys

Sulfite APS reductase (APR)

DCD 1

Rdred

Sulfite reductase (SiR)

NH3 Pyruvate

NSF1 DES 1 NSF2

Sulfide Rdox

Adenosine 5’- phosphosulfate (APS) ATP Sulfurylase (ATPS) SO42Soil SO4 Root absorption

SO42-

2-

DCD 1: D-cysteine desulfhydrase 1 DES 1: L-cysteine desulfhydrase 1 NSF1 and NSF2: L-cysteine desulfurases (nitrogen fixation 1 and 2 homologs)

SO42-

Fig. 2 Schematic illustration of the pathways involved assimilatory sulphate reduction in plants

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Fig. 3 Potential biotechnological applications of exogenously applied H2 S

Thus, it cannot permit through the membranes to the cytoplasm (Krueger et al. 2009; Kabil and Banerjee 2010). In chloroplast, sulphate gets activated by adenylation using ATP hydrolysis catalyzed enzyme ATP sulfurylase (ATPS) to form adenosine 5' -phosphosulfate (APS). Following this, reduction reaction takes place by the APS reductase (APR) enzyme, Ferredoxin reliant sulfite reductase (SiR) converts APS to sulfite, which is then reduced to sulphide. The next step is to combine it with O-acetylserine (OAS) to create cysteine. Serine acetyltransferase (SAT) is involved in the inclusion of OAS into the process, generating the cysteine synthase complex (CSC) through the collaboration of SAT and Oacetylserine (thiol) lyase (OAS-TL). Sulfide stabilizes the CSC complex, while OAS dissociates from the CSC complex, resulting in cysteine synthesis. The DES1 and DCD1 enzymes converts cysteine to H2 S (Garcia et al. 2015; Feldman-Salit et al. 2012). SAT is the crucial enzyme for cysteine synthesis, formation of cysteine act as a feedback inhibitor. Thus, development of CSC complex reduces SAT’s susceptibility to feedback inhibitors and promotes its activity for formation of OAS. Thereby, an increase in the OAS-TL-catalyzed reaction for reduction of sulphur to cysteine (Feldman-Salit et al. 2009; Wirtz et al. 2010). H2 S synthesis in the cytosol depends on the L-Cys desulfhydrase (DES1) enzyme, in the desulfhydration pathway from cysteine (L-Cys) following the synthesis of pyruvate and ammonia as byproducts, leading to end product H2 S (Alvarez et al. 2010; Gotor et al. 2010). Another analogous enzyme, D-cysteine desulfhydrase (DCD1) has been noted in the mitochondria which decomposes D-Cys into pyruvate, NH3 and H2 S (Wegele et al. 2004). OAS and cysteine synthesis occurs in the cytosol, chloroplasts, and mitochondria due to the presence of SAT and OAS-TL

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isoforms in all three sections. The cytoplasm contains SAT5 and OAS-TL A, chloroplasts contain SAT1 and OAS-TL B, and mitochondria contain SAT3 and OAS-TL C (Birke et al. 2013; Watanabe et al. 2008). The three SAT and OAS-TL isoforms appear to be somewhat redundant according to research in reverse genetics, which suggests that sulphide, OAS, and cysteine are exchanged between these three cell sections (Lee et al. 2014; Watanabe et al. 2008). Isoforms have distinct actions in different sections. OAS-TL C regulates the action of SAT3 in mitochondria, which produces a considerable amount of OAS, whereas OAS-TL A in the cytoplasm is essential for cysteine production (Birke et al. 2013; Haas et al. 2008; Wirtz et al. 2012).

4 Role of H2 S Signaling in Plants in Response to Drought Stress Climate change is substantial factor that affect growth, development, and physiological processes in plant and as a result of which productivity is reduced. Plants exposed to environmental stress response mostly by increasing the production and generation of superoxide ions and reactive oxygen species (ROS) in cells, including high hydrogen peroxide production (Suzuki et al. 2012). Water scarcity is one of the key factors contributing to reduced water absorption by plant roots and excessive transpiration (Blum 1996). Drought stress wields many lethal effects on plants counting to loss of cell veracity, oxidative and osmotic stress, impairment to PS II and so on. Drought also induced reduction in leaf area and leaf turgor cell, which eventually origins a limit in the enlargement of cells and therefore decreasing the photosynthetic rate (Raja et al. 2020). The disparity between light capture and usage imposed by drought leads to disorganization of thylakoid membranes and in the accumulation of ROS in the chloroplast (Kosar et al. 2020). H2 S can have signaling that causes several adaptations in the cells of plant in response to drought stress (Fig. 4). Many research published have revealed that H2 S play significant role in developing drought stress tolerance in diverse plant types (Table 1). It has been reported that exogenous application of an H2 S donor (NaHS) boosted plants to grow faster and survived longer as compared to non-treated plants exposed to drought stress. H2 S appears to be involved in different ways to this condition. Studies have proposed that H2 S contributes to drought tolerance/resistance in plants by boosting antioxidant enzyme activity, ABA signalling to induce stomatal shutting, and up-regulating the transcriptional genes that participates in the ascorbic acid—glutathione cycle (Lisjak et al. 2011; Zhang et al. 2010a). H2 S could be centrally involved in abscisic acid signal pathway (ABA) was founded by Ma et al. (2016), whereas Shan et al. (2018) discovered that H2 S regulated the AsA–GSH cycle in the leaves enhancing drought resistance in wheat seedling. Drought stress experiments on wheat seedlings revealed that H2 S signalling stimulates ABA production, which resulted in enhanced

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Drought Stress

Exogenous application of H2S Donor

Osmotic stress, Oxidative stress (ROS), Destroy cell integrity, Water deficient within cell, Damage to PS II

Imbalanced antioxidant system

Reduced Osmotic Pressure

Stomata Closure via ABA signaling

Activation of antioxidant system

Accumulation of osmolytes

Overproduction of ROS in Chloroplast

Osmotic Stress

Reduced transpiration rate

Scavenging of ROS

Maintenance of osmotic stress

Oxidative Stress

Reduced water uptake

Reduced oxidative stress

Increase osmotic pressure

Damage biomolecules, Peroxidation of lipid membrane

Separation of biochemical and physiological process

PS II repair, Improve integrity of thylakoid membrane

Increased water uptake

Plant Death

Plant Survival

Fig. 4 Overview of the physiological and biochemical changes in plants on application of H2 S donor to respond the adverse effects of drought stress

plant height, relative water content of leaves, and antioxidant enzyme activity (Ma et al. 2016). Application of NaHS in wheat plants resulted in declined accumulation of MDA and H2 O2 contents in plant parts such as leaves and roots. Upregulation of genes encoding ABA production has been identified in wheat roots, whilst comparable elevation of transcription levels of genes encoding ABA receptors (TaRCAR and TaCHLH) has been seen in wheat leaves in drought stress resistance. GarcíaMata and Lamattina (2010) observed that in Arabidopsis thaliana and Vicia faba, NaHS regulated closing of stomata and upgraded leaf relative water content (RWC) is used to improve drought resistance. Moreover, inhibiting or scavenging H2 S biosynthesis partly blocked stomatal closure (ABA-dependent) through amendable cassette of ATP-binding transporters. Recently, Zhou et al. (2020) affirm by activation and improving ABA biosynthesis, reducing lipid peroxidation and sustaining antioxidant system improve rice’s tolerance to drought stress. Jin et al. (2013) studied in lcd mutant plant with enlarged stomatal aperture causing a drought sensitive phenotype, where ABA-related mutants aba3 and abi1 lcd gene expression where down regulated along with H2 S production. The administration of NaHS exogenously promoted stomatal closure in these mutants. Hence, under drought stress, H2 S may limit stomatal aperture in an ABA-dependent manner, whereas ABA may increase H2 S production. Simultaneously, alternative report deliberated that drought tolerance/resistance plants may accumulate osmoprotectants of low molecular weight, such as proline, sugars, sugar alcohols, and glycine betaine (GB) (Garcia-Mata and Lamattina 2001; Rivero et al. 2014). The content and composition of osmoprotectants differ significantly depending upon the environmental condition and plant species (Rivero et al.

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Table 1 The effect of the exogenous application of H2 S donor on plants exposed to drought stress Plant species

Main effect

Reference

Carthamus tinctorius Reduced oxidative damage due to improved accumulation of secondary metabolites; supported antioxidant capacity and conservation of ion homeostasis

Amir et al. (2020)

Helianthus annuus

Enlarged leaf water potential and POD activity

Almeida et al. (2020)

Medicago sativa

Better physiological performance; reactive oxygen/nitrogen species homeostasis and defence-related pathways regulated transcriptionally

Antoniou et al. (2020)

Oryza sativa

Upkeep of the redox balance by increasing antioxidant capacity; ABA biosynthesis increased and stimulation of downstream genes related to drought

Zhou et al. (2020)

Setaria italica

Improved osmotic stress tolerance by facilitating DNA methylation

Hao et al. (2020)

Triticum aestivum

Enhanced seed germination; improved activities of enzymes such as amylase, esterase, catalase and ascorbate peroxidase; decreased activity of lipoxygenase

Zhang et al. (2010a, b)

Improved activities of ascorbate peroxidase, glutathione reductase, dehydroascorbate reductase, and γ-glutamylcysteine synthetase; Maximum contents of total ascorbate and glutathione

Shan et al. (2011)

Reduction in oxidative stress by Li et al. (2015) boosted activities of SOD and CAT; hastening of PS II repair cycle; enhancing D1 protein phosphorylation, degradation, and synthesis leading to increased D1 protein turnover Boosted antioxidant enzyme Ma et al. (2016) activities; declined MDA and H2 O2 contents; improved ABA biosynthesis Initiation of ribosome biogenesis, protein processing in endoplasmic reticulum, fatty acid degradation and cyan amino acid metabolism

Li et al. (2017)

(continued)

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Table 1 (continued) Plant species

Fragaria ananassa

Main effect

Reference

ascorbate–glutathione cycle upregulated

Shan et al. (2018)

In leaves diminished accumulation of H2 O2 and malondialdehyde; preeminent concentration of proline, anthocyanins, and flavonoids; improved activities of SOD, CAT, and POD

Kolupaev et al. (2019)

Relative water content and stomatal Christou et al. (2013) conductance Increased

Impatiens walleriana Reduced water loss due to closure of stomata

Garcia-Mata and Lamattina (2010)

Vicia faba

Increased relative water content

Garcia-Mata and Lamattina (2010)

Arabidopsis thaliana Increased. Stomatal closure and survival rate,

Garcia-Mata and Lamattina (2010)

Advanced survival of seedlings; Jin et al. (2011) significant reduction in the size of stomatal opening; increased expression of drought related genes such as DREB2A, DREB2B, CBF4, and RD29A Glycine max

Developed superoxide dismutase Zhang et al. (2010a, b) (SOD) and catalase (CAT) activities; lesser lipoxygenase activity; excessive accumulation of MDA, H2 O2 , and superoxide anion (• O2 ) delayed Upregulation of antioxidant enzyme activity; accumulation of soluble sugars, free amino acids, and proline

Batista et al. (2020)

Ipomea batatas

Increased activities of antioxidant Zhang et al. (2009) enzymes; improved stability of cell membranes

Spinacia oleracea

Increased glutathione accumulation Kok et al. (1985) Increased water and osmotic potential of leaves; reduced MDA; increased levels of soluble sugars and PAs; upregulation of genes such as choline monooxygenase (SoCMO), betaine aldehyde dehydrogenase (SoBADH), aquaporin (SoPIP1;2) as well as genes related to the biosynthesis of PAs and soluble sugars

Chen et al. (2016)

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2014). In addition to these compounds, drought tolerance is aided by the manufacture of polyamines, including putrescine, spermidine, and spermine (Takahashi and Kakehi 2010). Mohammadi et al. (2018) studied in Thymus vulgaris that exogenous supplementation of 20 mg L−1 putrescine reduced cell injury and increased water content in leaf, laterally with upregulated antioxidant enzyme actions and accumulation of essential oil under drought stress conditions. Chen et al. (2016) detected that H2 S play a significant part in biosynthesis of sugars and polyamines (PA) in Spinacia oleracea seedlings exposed to drought stress. In the experiment it was observed that the gene expression; ornithine decarboxylase (ODC), N-carbamoylputrescine amidohydrolase (CPA), and arginine decarboxylase (ADC) were upregulated, whereas S-adenosyl-Metdecarboxylase (SAMDC) gene expression were downregulated resulting in preeminent polyamine amounts in drought tolerant Spinacia oleracea seedlings. Similarly, sugar biosynthesis genes encoding fructose-1,6-bisphosphatase (FBPase), trehalose-6-phosphate synthase (T6PS), and sucrose phosphate synthase (SPS1) were found to be increased, which resulted in higher fructose and trehalose concentrations in plant tissue. The over-expression of polyamines-related genes caused higher polyamines content leading to enhancement in tolerance under drought stress (Alcazar et al. 2010; Capell et al. 2004). Concurrently, proteomic analysis report revealed that Mitogen-activated protein kinases (MAPKs) are members of the signaling family that modulates plant responses to stress. Du et al. (2019) conducted experiments on A. thaliana and proposed that under drought stress MAPKs gene expression and H2 S production was stimulated, further in mutant lcd and des1 the induced MAPK expression was stopped and ABA-dependent stomatal movement was impaired. Accordingly, H2 S- MAPK4 a signal cascade is implicated in the improvement of drought stress by ABAstimulated stomatal closure. A previous report proclaimed that H2 S could trigger S-type anion channel via SLAC1 promotes stomatal closure under drought stress (Wang et al. 2016). Drought-induced H2 S protects against oxidative and osmotic damage by modulating the activities of antioxidant enzymes as SOD, CAT, GPOX, APX, GR, dehydroascorbate reductase (DHAR), and monodehydroascorbate reductase (MDHAR). Enhancing the antioxidant activities of enzymes leads to reduced transpiration rate by modifiable stomatal conductance,

5 Role of H2 S Signaling in Plants in Response to Salt Stress Soil salinization is a critical environmental element that causes severe reductions in plant development and productivity, resulting in a large loss of plant output (Krasensky and Jonak 2012). Salt stress exert their malicious effects due to excess ionic and nutrient disorder, and by the accumulation of reactive chemicals leading to oxidative stress in plants (Munns and Tester 2008), It adversely damages several cellular compartments generating excessive reactive oxygen species (ROS) and lipid peroxidation Thus, leading to reduced photosynthetic efficiency and premature leaf senescence (Smirnof 2006). It is well documented that salt stress outcomes in the

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excessive buildup of Na+ in plant cells which will straight abolish the membrane potential homeostasis of the cell membrane on both sides, which inhibit the K+ uptake, thus resulting to K+ deficiency (Zhu 2003; Munns and Tester 2008). Adaptation to salinity, the plants evolve variable mechanisms, such as reducing Na+ influx into the root, vacuoles Na+ compartmentation within cells and leaf Na+ secretion (Cui et al. 2011; Kronzucker and Britto 2011). Na+ reclamation from the xylem and recirculated in the phloem. To boost agricultural plant salt tolerance, the best method is to limit the input of Na+ into the root system. Thus, limiting Na+ accumulation in plants. Under salt stress tolerance, the salt excessively sensitive pathway (SOS) might maintain cytoplasmic ion homeostasis (Zhu 2002). SOS genes such as (Zhu 2002). The SOS pathway is regulated by SOS genes including SOS1, SOS2, SOS3. SOS2like, SOS3-like, and SOS4 (Christou et al. 2013). Under salt stress, SOS1 plays a vital role in the Na+ /H+ antiporter in the plasma membrane is capable of eliminating excess Na+ from A. thaliana and is controlled by two additional SOS genes (Feki et al. 2014). Plants produce a significant quantity of ROS under salt stress, including O2 •− , OH, 1 O2 , and H2 O2 ; to overcome its excessive accumulation plants have developed protective strategies by activating enzymatic and non-enzymatic antioxidants (Ascorbic acid and Glutathione) (Superoxide dismutase, Catalase, Peroxidase, Glutathione peroxidase, Ascorbate peroxidase, and Glutathione reductase) (Yin et al. 2016). Plants can regulate the redox states of ascorbic acid and glutathione in the cell by controlling their production (Kocsy et al. 2001). Evidence from several salt-tolerant plants indicates that H2 S plays a significant part in the signaling system. There have been few studies on the general morphological changes, photosynthetic machinery, stomatal respones, ROS buildup, and the relationship among alterations after exogenous H2 S treatment in the leaves and roots in different plant species (Fig. 5). These investigations, however, are typically focused on one feature, such as Na+ /K + equilibrium for example, or antioxidation mechanisms in roots or leaves. Additionally, the fundamental processes through which H2 S controls salt tolerance, particularly the alterations in H2 S homeostasis, remain obscure and call for in-depth examination at the physiological and biochemical levels. As experimental in various plants, including rice, wheat, strawberry, tomato, Medicago sativa, Arabidopsis, Spartina alterniflora, Malus hupehensis, Populus euphratica and Populus popularis (Table 2). H2 S regulated the exosmosis of intracellular K+ and kept a lower intracellular Na+ buildup and the Na+ /K+ ratio (Ding et al. 2019; Guo et al. 2018; Lai et al. 2014; Li et al. 2020a, b; Mostofa et al. 2015; Wei et al. 2019; Zhao et al. 2018). Notably, H2 S upheld low levels of Na+ in cells by enhancing Na+ compartmentation in vacuoles and boosting transcription of plasma membrane H+ ATPase, H+ -ATPase subunit, and vacuolar Na+ /H+ antiporter genes (Chen et al. 2015). NaHS was found to be responsible for preserving the K+ /Na+ equilibrium in Alfalfa treated with salt by preventing K+ efflux, which was probably brought on by a decrease in the expression of the genes for K+ outward-rectifying channels resembling shakers (Lai et al. 2014). Parallel outcomes were observed in the salt-treated barley seedlings roots when NaHS was present (Chen et al. 2015). In this work, salt stress resulted in down-regulation of TaSOS1 and TaSOS3 and an increase in TaSOS2 in wheat seedling leaves. This suggests that salt content and

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S. Samantaray and K. Kumari Salt Stress Exogenous application of H2S Donor

Ionic Stress

Osmotic Stress

Disruption of ion homeostasis, Nutrient imbalance

Shortage of water

Damage photosynthesis, generate excess ROS, effect antioxidant defense system

Osmotic adjustment Cell wall modification ROS Detoxification Vesicle trafficking K+NO3- homeostasis Vacuole compartmentation Compatible solutes

Osmotic adjustment

Signal transduction Activation of Salinity tolerance genes

Growth reduction, cell death

Plant Death

Salt tolerance

Functional and structural modification

Plant Survival

Fig. 5 Overview of the physiological and biochemical changes in plants on application of H2 S donor to respond the adverse effects of salt stress

cultivar traits may be linked to the distinct responses of these three genes. Increased K+ /Na+ ratio was seen in treated wheat seedlings with 50 M NaHS and then exposed to 100 mM NaCl. The preferential nonselective cation channels transport K+ over Na+ , and SOS1, a plasma membrane Na+ /H+ antiporter, increased in tandem (Deng et al. 2016). In high salinity strawberry plants, NaHS induced the expression of Na+ /H+ antiporter genes in the plasma membrane (such as SOS2-like, SOS3-like, and SOS4), signifying a function for H2 S in K+ absorption (Christou et al. 2013). According to Wang et al. (2012), H2 S can improve Medicago sativa’s tolerance to salt via the NO pathway, as Chen et al. (2015) have verified in barley seedlings. H2 S also increases endogenous NO and total S-nitrosothiols (SNOs) levels in plants during salt-alkali stress (Christou et al. 2013; Ziogas et al. 2015), but it also boosts NR, glyoxalase I and II activity and inhibits S-nitrosoglutathione reductase activity (GSNOR). Treatment with NO can also increase H2 S levels and the activity of H2 S-producing enzymes. Similarly, exogenous NaHS and SNP can activate enzyme activity, allowing them to quickly synthesize themselves from inside (Ziogas et al. 2015). The modulation of the defence response gene enhanced salt tolerance in transgenic rice plants overexpressing OsMPK5 (Xiong and Yang 2003). Additionally, overexpression of SKORs and NSCCs as well as the activation of the MPK pathway help plants recover from salt stress when H2 S is present. Systematic research can aid in an improved comprehension of the signal and mechanism that follows underlying the H2 S-induced reduction of salt-alkali stress. Under salt stress, H2 S may promote the transfer of photosynthetic electrons, chlorophyll synthesis, and carbon fixation in the leaves of Kandelia obovata and cucumber (Jiang et al. 2020; Li et al. 2020a). Furthermore, the number of additional proteins

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Table 2 The effects of the exogenous application of H2 S donor on plants exposed to salt stress Plant species

Main effect

Reference

Rice Oryza sativa L)

Decreases the uptake of Na+ and the Na+ K+ ratio; Activation of antioxidant system; protection of photosynthetic apparatus; induction of osmoregulators accumulation

Mostofa et al. (2015)

Wheat (Triticum aestivum L.)

Suppresses ROS accumulation by increasing antioxidant defence

Deng et al. (2016)

Activation of antioxidant system

Khan et al. (2017)

Keeps Na+ and K+ homeostasis by the gene expression of plasma membrane Na+ / H+ antiporter (SOS1). Decrease lipid peroxidation content and ROS generation. Increases activity of antioxidant system

Jiang et al. (2019)

Stimulation of seed germination and plant growth, Induction of osmoregulators accumulation

Sun and Luo (2014)

Activation of antioxidant system

Yu et al. (2013)

Cucumber Cucumis sativus L

Mangrove plant (Kandelia obovata)

Enhances the quantum efficiency of Liu et al. (2019) photosystem II (PSII) and the membrane lipid stability

Medicago sativa

Activation of antioxidant system, Increase of K+ /Na+ ratio

Lai et al. (2014)

Activation of antioxidant system, stimulation of seed germination and plant growth

Wang et al. (2012)

Cynodon dactylon

Activation of antioxidant system, stimulation of seed germination and plant growth, induction of osmoregulators accumulation

Shi et al. (2013)

Fragaria × ananassa

Activation of antioxidant system, increase of K+ /Na+ ratio, protection of photosynthetic apparatus

Christou et al. (2013)

Arabidopsis thaliana

Stimulation of seed germination and plant growth

Li et al. (2014)

Hordeum vulgare

Increase of K+ /Na+ ratio

Chen et al. (2015)

Zea mays

Activation of antioxidant system

Shan et al. (2014)

involved in metabolic pathways, including Heat-shock protein, glutamine synthetase 1 and 2 involved in nitrogen metabolism, and cysteine synthase 1 are aided in protein synthesis and several increased antioxidants including Cu/Zn superoxide dismutase, APX, pancreatic and duodenal homeobox 1 (Jiang et al. 2020; Li et al. 2020b). H2 S boosted the AsA-GSH cycle (glutathione S-transferase in high saline conditions. H2 S affects such large proteins, but the exact method by which it does so is still unknown (Guo et al. 2018; Li et al. 2014a). Current research has shown that under salt-alkali stress, the transcription factors VvWRKY30 and JIN1/MYC2 trigger the H2 S signal (Yastreb et al. 2020; Zhu et al. 2019).

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Stomata can typically close as a result of salt stress. Nevertheless, the H2 S scavengers such as H2 O2 , ascorbic acid (AsA), hydroxylamine (NH2 OH), potassium pyruvate (C3 H3 KO3 ), ammonia (NH3 ), CAT, and diphenyl iodide (DPI) inhibited stomata shutting in V. faba L. indicating that under salt stress, both H2 S and H2 O2 might control stomatal motility. Furthermore, salt treatment enhanced endogenous H2 S and H2 O2 buildup as well as the activities of L-cysteine desulfhydrase and Dcysteine desulfhydrase in guard cells (Liu et al. 2012). Therefore, H2 S may operate as the downstream of salt stress that has been reduced by H2 O2 . In response to adverse environmental circumstances, plants utilize MAPK cascades as functional signaling mediators. MAPK cascades regulate plant growth and development and contribute to plant stress tolerance through modulating MAPK, MAPKK, and MAPKKK at the transcriptional level (Rodriguez et al. 2010). TaMPK1 was down-regulated in this study when compared to the CK, but TaMPK4 was upregulated at 1 DAS, showing differing salt stress response patterns. Wen et al. (2015) reported similar findings, noting an increase in TaMPK4 expression at 6 h following salt stress and a decrease in TaMPK1 expression at 3 h. Additionally, under salt stress, TaMPK4 activation was seen in seedling leaves, controlling the amount of K+ and osmolytes in the plant (Hao et al. 2015). In this work, treatment with NaHS+ NaCl significantly increased TaMPK4 expression from 1 to 5 DAS compared to control conditions, which may indicate that H2 S administration controls osmolytes via enhancing TaMPK4 expression. According to Du et al. (2017), exogenous supplementation of H2 S reduced alleviated cold stress in Arabidopsis thaliana by promoting the expression of the MPK4 gene and taking part in MPK4-induced stomatal movement. Jin et al. (2011), In Arabidopsis, NaHS fumigation increased DREB2 expression. In this study, NaHS + NaCl treatment enhanced TaDREB2 expression in wheat seedlings compared to salt stress alone, demonstrating that NaHS pretreatment boosted TaDREB2 expression in response to salt stress. These studies suggest that exogenous NaHS therapy appears to reduce salt damage in plants by improving photosynthesis, antioxidant capacity, and the AsA-GSH cycle. Furthermore, it was shown that the SOS and MAPK pathways have a role in H2 S-induced salt stress relief at the transcriptional level.

6 Conclusion and Future Perspectives The action of the gasotransmitter H2 S on plants is paradoxical, since although high levels of H2 S inhibit plant growth and development, low levels of H2 S can work as a dynamic regulator to help plants survive. The bulk of H2 S is created in the cytoplasm of plant cells by the desulfhydration of L-cysteine, which results in the production of pyruvate and ammonia as byproducts in a process catalyzed by the enzyme Lcysteine dedesulfhydrase. H2 S function as a signaling molecule to control a variety of physiological plant activities, including seed germination, root formation, stomatal openings/closing, floral senescence, and pathogen assault. In this signaling route, H2 S has most recently become a new player, regulating the metabolic processes that

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enable plants to tolerate high salt and drought stress. This most likely entails the induction of stomatal closure, the activation of antioxidant defenses, K+ uptake over Na+ , production of semiprojective molecules and the increased gene expression of resistance-associated enzymes. Additionally, H2 S interacts with NO, H2 O2 , Ca2+ , ABA, GA, ethylene, and polyamines in crosstalk, resulting in a complex signaling network all of which are crucial for plants to respond to drought and salt stress. Concentrated in the following categories, there are many unsolved questions and crucial topics that require more study. (1) The regulation of H2 S generation and its target sites in the different organelles are not well understood. A deeper understanding of the intracellular H2 S generation can be achieved by using pharmacological methods for the discovery of specific enzyme inhibitors of the H2 S metabolic pathway. (2) Future study should focus on determining the biochemical and molecular mechanisms underlying these actions. The creation of a highly effective method for H2 S detection must be prioritized in research, and this will require making extensive use of various omics-mediated methodologies to screen out H2 S-related loci in huge scale. (3) Several types of study must be undertaken in abiotic stress circumstances, investigate the point-to-point process within the crosstalk between H2 S and a single signal transducer. It is still unknown how H2 S and NO react with one another and how these reactions interact with protein including persulfidation, S-nitrosylation and S-sulfhydration. It is necessary to find and identify more post-translational modification proteins that are activated by H2 S in ABA- or NO-reliant signal pathways during stressful situations. In order to understand how H2 S interacts with the metabolism of ROS and RNS under stressful and physiological circumstances, more research is required. Lastly, new signal transmitters associated with H2 S activity are still undiscovered. Although H2 S has a short lifetime, it is a very active molecule. It’s also crucial to understand how H2 S and the other chemicals involved in signalling work. Therefore, it is evident that understanding the H2 S complex signalling network is a top research priority.

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Ethylene Synthesis and Redox Homeostasis in Plants: Recent Advancement Manas Mathur, Ekhlaque A. Khan, Rakesh K. Prajapat, Hamdino M. I. Ahmed, Megha Sharma, and Deepak Sharma

Abstract The life cycle of plants is regulated by ethylene in numerous ways, including adaptations to biotic and abiotic stimuli, flower growth, fruit ripening, senescence, and seed germination. As a result, it is crucial for interactions to the environment that directly affect a plant’s capacity for adaptability and reproduction. Major progress has been made in recent years in our knowledge of the molecular mechanisms controlling the synthesis and activity of ethylene. The gaseous plant hormone ethylene is produced via a straightforward two-step biosynthesis process. Despite the simplicity of this route, current molecular and genetic investigations have shown that ethylene production regulation is far more complex and takes place at various layers. The homeostasis of ethylene’s general precursor S-adenosyl-Lmethionine (SAM), which is subject to transcriptional and post translational control of its synthesizing enzymes (SAM synthetase), as well as the metabolic flux through the nearby Yang cycle, are closely related to each other. Two specific enzymes, 1 aminocyclopropane-1-carboxylic (ACS) synthase and ACC oxidase, continue ethylene production from SAM (ACO). In order for plant electron transport cascades to function effectively, both the oxidized and reduced forms of electron carriers must be present simultaneously. This requirement is known as redox positioning, which Manas Mathur and Ekhlaque A. Khan are contributed equally. M. Mathur · R. K. Prajapat School of Agriculture, Suresh Gyan Vihar University, Mahal Road, Jagatpura, India E. A. Khan (B) Department of Biotechnology, Chaudhary Bansi Lal University, Bhiwani, Haryana, India e-mail: [email protected] H. M. I. Ahmed Horticulture Research Institute (HRI), Agricultural Research Center (ARC), Giza 12619, Egypt M. Sharma Department of Botany, University of Rajasthan, Jaipur, India D. Sharma School of Agricultural Sciences, Jaipur National University, Jaipur, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_6

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entails the transfer of electrons to molecular oxygen from various places in the respiratory and photosynthetic electron transport chains. During the course of a plant’s lifetime, adverse environmental conditions like drought, high or low temperature, heavy metal stress, etc., cause the development of superoxide, which in turn gives rise to additional reactive oxygen species (ROS). Ascorbate, a further hydrophilic redox buffer produced by plant cells, shields the plants from oxidative stress. The redox homeostasis is also governed by sizable pools of antioxidants. Additionally, tocopherol is an effective scavenger of ROS like singlet oxygen because it is a liposoluble redox buffer. Additionally, proteinaceous thiol members, including the electron transporters and energy metabolism mediators phosphorylated (NADP) and nonphosphorylated (NAD+) coenzyme forms, interact with ROS, metabolize, and maintain redox homeostasis. Examples include thioredoxin, peroxiredoxin, and glutaredoxin. ACC synthase (ACS), ACC oxidase, and aminocyclopropane-1-carboxylic (ACC) synthase (ACO).This review focuses on important new findings and incorporates knowledge of ethylene production and redox homeostasis in several plant species.

1 Introduction Ethylene is thought to have a significant role in the ripening of fruit and has a variety of physiological functions in higher plants despite its simple fundamental structure. Chemically, it is a nonpolar moiety and an unstable olefin with two carbon (C) atoms. The diffusion ratio in vacuum to water is thousands of times greater than this, and it is more soluble in fatty acids, which have polarity 14 times that of water (Vandenbussche et al. 2012; Chang 2016). These characteristics confer their various biological functions, such as controlling cell destiny, seed germination, sex differentiation, root and shoot growth, stress tolerance, cell death, abscission, and responsiveness to gravity and photoperiod etc. (Poel et al. 2015; Wang et al. 2021). These characteristics confer their various biological functions, such as controlling cell destiny, seed germination, sex differentiation, root and shoot growth, stress tolerance, cell death, abscission, and responsiveness to gravity and photoperiod. This study highlights a critical regulation process of ethylene deposition during root development in soil. The steps for ethylene metabolism and its receptor ligand binding have been explored in Arabidopsis and Oryza sativa (Merchante et al. 2013; Yang et al. 2015a, b). Additionally, a precise physiological pathway for its interaction with other signals has also recently been examined (Poel et al. 2015; Wen 2015). These findings provide a scientific basis for further investigation into the metabolic functions and physiological processes in plants. Numerous studies have also demonstrated its critical role in the creation of cell walls (Chandler 2018; Dubois et al. 2018). Although ethylene aids in various other physiological mechanisms, such as cell wall production, cell wall rigidity maintenance, and cytoskeleton flexibility maintenance, the fundamental functional process is still not fully understood (Qin and Zhu 2011). As a result, more research is needed into

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the transcriptomic level involvement of genes in the ethylene pathway. Additionally, it promotes the girth of the rice coleoptiles flowering portions of R. palustris and aids in the formation of epidermal hairs in Arabidopsis, providing sufficient evidence for the causative machinery of ethylene. In addition, it plays a critical role in stress tolerance, psychological problems, and the synthesis of organelles in plants. The primary source of determining whether a flower is female or male in cucurbits is ethylene, which triggers the development of the ovaries, anthers, and their ratio from a floral bud that contains both sexes (Manzano et al. 2013, 2014). This was demonstrated by preventing the growth of stamens and carpels (Bai et al. 2004). In Cucumis and Cucurbita, ethylene increases the ratio of female to male flowers (Manzano et al. 2013), while opposite results have been seen in Citrullus plants. Cucumis and Cucurbita produce fewer ovules per plant when ethylene production is inhibited, and these ovules become hermaphrodites. Similar observations were made in Citrullus, proving the urge to inhibit stamen growth in female flowers (Manzano et al. 2014). Since several other plant growth regulators, such as GA3, auxins, and brassinosteroids, play important roles in cucurbit sex determination, a few of these physiological roles are aided by ethylene (Papadopoulou et al. 2005; Manzano et al. 2011; Zhang et al. 2014, 2017). Growth, physiological development, and senescence of its basic components such as leaves, flowers, and fruits are all part of the tedious maturity transition. They have many molecular mechanisms in which ethylene plays an important role, interacting with several plant growth regulators and creating an environment suitable for phase succession, reproducibility, and organ lifeless. Variation in concentration, discernment, and hormonal integration all play a role in controlling plant growth and development. Furthermore, there is a strong desire to focus on the molecular mechanisms of ethylene regulation that are responsible during development and physiological death, as well as encourage future experimentation with the goal of obtaining better varieties and traits in specific crops. Ethylene regulates plant development and physiological death (Masood et al. 2012; Nazar et al. 2014). It has been suggested as a multifunctional phytohormone that regulates both growth and senescence. It either initiates or resists growth and senescence mechanisms depending on the amount, time of application, and crop variety.

2 Biosynthesis and Regulation in Ethylene Few genes in Arabidopsis regulate the synthesis of this hormone via a series of biochemical reactions. S-adenosylmethionine synthase, also known as methionineadenosyl transferase, converts methionine to structural form, which is then metabolized by 1-aminocyclopropane-1-carboxylate synthase and 1-aminocyclopropane1-carboxylic acid oxidase (ACO) to produce this plant growth regulator (Lin et al. 2009). However, approximately 82% of methionine is converted to SAM via the Yang cycle. However, some of the molecules discovered in the Arabidopsis genome play no role in ethylene synthesis, with the majority of SAM involved in polyamine

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and methylation (Roje 2006). This transformation follows the initial path, and ACSs are considered key enzymes, but their presence in nature is limited (Wen 2015). Arabidopsis has 12 genes (ACS1-12), of which ACS3 is a pseudogene and ACS10/12 regulates aminotransferases (Yamagami et al. 2003). ACSs also denotes time-consuming and defines transcriptional and posttranscriptional regulation. In addition, unlike other plant growth regulators or stress initiating molecules, ACSs exhibit a wide range of spatiotemporal expression (Lin et al. 2009; Wen 2015). Furthermore, mutations in ACSs or ETO1 increase the stability of ACSs but not enzymatic reactions, stimulating ethylene accumulation in ethylene overproducing mutant’s eto1/2/3 (Wang et al. 2004). ACSs can be classified as homodimers or heterodimers (Tsuchisaka and Theologis 2004). As a result, we conclude that ACSs act as a competitive inhibitor of aminoethoxyvinylglycine (AVG), which inhibits ethylene synthesis (Wenzel et al. 2008). However, ACC, which does not exist as conjugates, can be diffused from the initial active position through permanent plant tissues for further role (Poel and Straeten 2014). Finally, ACC has several other critical roles in plant physiological growth, as it has been reported that it acts as a novel signal compound in important pollination phenomena that do not rely on the ethylene signal pathway (Mou et al. 2020). It also aids in the final pathway where it converts to ethylene, producing O2 and ascorbate as byproducts (Lin et al. 2009). It has been reported that the molecular mechanisms of ACSs and ACOs are controlled by methylation of nucleic acids, indicating epigenetic control (Lang et al. 2017). It has been proposed that sex-determining genes are found during biosynthesis, signaling, or as transcriptional factors, inducing ethylene synthesis. The gene that controls the death of embryonic stamens that initiate female flower development also plays an important role in this regulation (Boualem et al. 2016).

3 Signal Transduction Pathways During Ethylene Synthesis Ethylene is the most basic olefin gaseous multifunctional plant growth regulator and the first of its kind to exist in a gaseous state. It is biosynthesized by plants and regulates plant developmental processes such as growth, seed development, fruit maturation, cell death, abscission, and stress tolerance such as flooding, increased salinity, soil compaction, and parasite infection. The concentration of ethylene, the time of application, and the plant species all influence growth and senescence processes. When dicotyledonous germinates were cultured in the absence of light, they showed decreased root and hypocotyl growth, an embroidered warp of the apical hook, and radial swelling of the hypocotyls. Once biosynthesized in the entire plant, ethylene diffuses and amalgates with its receptors, stimulating its responses. Specifically, research on Arabidopsis thaliana led to an understanding and representation of ethylene signaling, elucidating the role of specific and unique components that are exclusive to ethylene only. Some scientific reports on molecular mechanisms reported some aspects that were unknown to the scientific community, such as its signaling, which includes receptors such as CTR1 protein kinase; EIN2, a transmembrane protein

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Fig. 1 Mechanism of ethylene signaling via canonical and non-canonical pathway

whose physiological role is unknown, as well as transcription genes such as EIN3, EILs, and ERFs. In the absence of ethylene, the receptors stimulate CTR1, which uncomfortably controls the penultimate pathways of synthesis signaling (Fig. 1). Ethylene plays an important physiological role in inhibiting its receptors, resulting in CTR1 inhibition and ethylene signaling (Hall et al. 1999). These reports provide a significant foundation for future research, which will necessitate the binding of these receptors in several signaling pathways, including understanding how the process of signal perception at the ER membrane affects transcription in the nucleus, and many other physiological roles of EIN2. This leads to scientific communities better understanding the basic mechanism of various ways to control ethylene signaling. The majority of genes are working to resist ethylene responses, which play an important role in post-harvest technology (Khatami et al. 2020).

4 Ethylene Signaling Assisted Genes and the Proposed Signaling Pathway Mechanism The ethylene has been attributed to transmembrane molecules found on the ER membrane that are homologous to cyanobacterium (phytochromes and cytokinin receptors). This establishes a universal foundation for the ethylene-binding domain, from which chloroplasts evolved (Schaller et al. 2011; Hérivaux et al. 2017). Signaling occurs via autophosphorylation of histidine residues, followed by phosphate transfer to aspartate in the recipient domain of response regulator protein (Gao and Stock 2009). Arabidopsis thaliana has five isoforms: ETR1, ethylene response sensor 1 (ERS1), ETR2, ERS2, and ethylene insensitive 4 EIN4 (Hua et al. 1995). So, based on phylogenetic studies and gene sequencing, these receptors are broadly classify as ETR1 and ERS1 and ETR2, ERS2, and EIN4 (Wang et al. 2006; Chen et al. 2010, 2020). SlETR1-7 are the names given to seven different types of ethylene receptors found in Solanum lycopersicum (Chen et al. 2020). Receptor mutations have been shown to resist ethylene binding, resulting in ethylene-insensitive plants (Harkey et al. 2018; Khan et al. 2022). Although the

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key role is played by the transmembrane domain, which also amalgates with ethylene using Cu+2 as a cofactor and is assisted by transmembrane protein responsive-toantagonist 1 (RAN1) via antioxidant protein 1 (ATX1) (Hoppen et al. 2019). Because the active form of these receptors was observed during dimerization, only one Cu+ binds to activated dimeric receptors. Only one dimeric receptor detects a single ethylene molecule. The ion’s binding site is Cys-65 in helix 2, and a mutation in this site prevents copper and ethylene binding (Binder 2020). Physiological receptors have the same sphere structural design, with a short Nterminal domain, three transmembrane -helices at the N terminus, and an ethylenebinding domain and a GAF domain (cGMP-specific phosphodiesterases, adenylyl cyclases, and FhlA). Signal motifs in the C-terminal where ETR1 has histidine kinase potential play no role in ethylene signaling, whereas ETR2, ERS2, and EIN4 have serine/threonine kinase potential, with ERS1 having dual in nature (Moussatche and Klee 2004). At the N-terminus, receptor homodimers form and are stabilised by two disulfide bonds forming a cysteine-cysteine interaction (Chen et al. 2010).

5 Activated Signal Transduction Pathways Most signal transduction pathways are activated when a ligand binds to their specific receptors, but in the case of ethylene signaling, ethylene acts as an inhibitor of its receptor, negatively regulating ethylene responses. In other words, in the absence of ethylene, the receptor is stimulated. It communicates with receptors via two critical components: constitutive triple response 1 (CTR1) and ethylene insensitive 2 (EIN2) (EIN2). CTR1 is a mitogen-activated protein kinase (MAPK) kinase with serine/threonine protein kinase activity that functions as a downstream regulator of ethylene signaling. EIN2 has a large N-terminal region with several transmembrane domains (EIN2-N) embedded in the ER membrane, as well as a cytosolic C-terminus (EIN2-C). CTR1 mutations that interfere with receptor-CTR1 binding render it inactive (Huang et al. 2003), and inhibiting binding between ETR1 and EIN2 causes ethylene insensitivity (Bisson and Groth 2015). Other proteins, such as reversion to ethylene sensitivity 1 (RTE1), a highly conserved protein, cytochrome b5, and tetratricopeptide repeat protein 1 (TRP1), which resemble transmembrane and coiled-coil protein 1 (TCC1) in animals and competes with Raf-1 for Ras interaction, play important roles in ethylene signaling. On ethylene amalgation with its receptor, phosphorylation of EIN2 is physiologically inactivated. There is no specific variation in the structure of the receptor-CTR1-EIN2 binding that stops or reduces phosphorylation of EIN2 as amalgation of ethylene to its receptors causes conformational changes that decrease the binding between CTR1 and EIN2, resulting in only a few EIN2 phosphorylations. EIN2 is active in this state and is further fragmented to produce EIN2-C from the membrane-embedded EIN2-N part.EIN2-C is the primary signaling molecule that acts as a go-between signaling molecule in the cell via specific pathways: binding of EIN2-C to the mRNAs encoding EIN3-binding F-box proteins, EBF1 and EBF2, results in their breakdown. Second, EIN2-C enters the nucleus and

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binds to EIN2 nuclear compacted protein 1 (ENAP1), which regulates the molecular activity of EIN3 and the associated EIL1 transcription factor, leading to signaling. According to molecular experiments, less EIN2 phosphorylation leads to less EIN2 ubiquitination, which leads to more EIN2 and further fragmentation of EIN2 by an unidentified protease to produce the C-terminal portion of EIN2 (EIN2-C) from the membrane-embedded N-terminal portion (EIN2-N) (Ju et al. 2012).

6 Redox Homeostasis and Its Understanding The single pathway involved in plant developmental processes and stress resistance against environmental fluctuations generates a variety of ROS through cell metabolism. The natural oxidant present on the earth’s surface is oxygen gas (O2 , which accounts for approximately 20.8% of the atmosphere) in ground state, which catalyses various redox reactions in cells. Oxygen is produced during oxygenic photosynthesis by photosynthetic organisms such as cyanobacteria, green algae, and plants splitting water (H2 O) in the presence of light (Foyer 2018). During photosynthesis, a cascade of redox reactions occurs in plants as electrons pass between a donor and an acceptor, resulting in the production of reactive oxygen species (ROS). During low or no photosynthesis in roots and fruits, the ETS system in mitochondria produced ROS as well as energy in tissues (Schertl and Braun 2014). ROS can cause cell damage by producing toxic byproducts of aerobic metabolism and can influence plant responses (Mittler 2017; Foyer 2018). However, chloroplasts, peroxisomes, and mitochondria are major sites of ROS production in plant cells, which can cause oxidative stress and damage cell membranes through lipid peroxidation and other biomolecules under environmental stress. Plant cells have an inherent ROS-scavenging system that protects them from the negative effects of increased ROS accumulation. This system can remove ROS via enzymatic or non-enzymatic pathways. In the cell, superoxide dismutase (SOD), catalase (CAT), glutathione reductase (GR), monodehydroascorbate reductase (MDAR), dihydroascorbate reductase (DHAR), and glutathione peroxidase (GP) were involved in the enzymatic pathways. Non-enzymatic pathways included ascorbic acid, prolines, glutathione, tocopherols, flavonoids, and carotenoids, as well as some signaling molecules (calcium ions, cAMP, nitrogen oxide). Plant hormones (ABA, ethylene, salicylic acid), osmolytes (amino acids, sugar alcohols, tertiary amines), and other metabolites are also required by the cell in ROS-scavenging mechanisms (Kreslavski et al. 2012). Plants coordinate photosynthesis, respiration, and photorespiration by maintaining an equilibrium between ATP production and consumption during cell signaling. (Suzuki et al. 2012). Cellular homeostasis is primarily maintained by active call metabolism and cell redox potential. During salt stress, ethylene, an important phytohormone, plays

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an important role in salt tolerance via ROS homeostasis. Under suitable physiological conditions, cells maintain redox equilibrium by producing and eliminating ROS/reactive nitrogen species (RNS) (Trachootham et al. 2008). According to Chen et al. (2012), the function of H2 O2 during signaling mimics that of ethephon under abiotic stress conditions.

7 Ethylene’s Influence on ROS Homeostasis and Salt Stress in Plants When ethylene signaling was blocked in Arabidopsis, salt tolerance was reduced, indicating a way to modulate response in salt stress (Achard et al. 2006; Peng et al. 2014). Ethylene signaling-related mutants (ein3 and ein1) were more sensitive to salt stress. Ethylene has also been shown to play a negative role in the rice signaling pathway (Yang et al. 2015a, b). Transgenic plants of Oryza sativa with OsEIL1 and OsEIL2 RNAi showed increased salt tolerance. ROS production in Arabidopsis ethylene Overproducer 1 (ETO1) mutants results in a positive response to salt stress and also modulates NaC/KC homeostasis. In rice, the negative regulator of salt stress SALT INTOLERANCE 1 (SIT1) QTLs, which are controlled by MITOGEN-ACTIVATED PROTEIN KINASE 3/6, controls the production of ethylene and ROS (MPK3/6). Thus, the different mechanisms that operate in monocots and dicots plants in ethylene-directed salt response warrant further investigation. ROS homeostasis is required for the ethylene-dependent regulation of plant development and stress response (Zhong et al. 2014; Yang et al. 2017). During salt stress, ROS act as important signal molecules, activating downstream metabolic pathways. During ROS burst, NaC/KC homeostasis is regulated by RESPIRATORY BURST OXIDASE HOMOLOG D (RbohD) and RbohF (Ma et al. 2012), and transcriptional regulation of AtRbohF ensures increased salt tolerance in mutant eto 1 (Jiang et al. 2013). However, ethylene-signaling components such as EIN3/EIL1 activate ROSscavenging gene expression to avoid excess ROS with increased salt tolerance (Peng et al. 2014). Similarly, the effect of ethylene signaling on ROS is incompatible at various stages of stress. ERF74 promotes ROS burst by regulating RbohD gene expression and inducing ROS-scavenging-related genes (Yao et al. 2017). Reduced ROS content can improve plant stress tolerance in the case of ethylene inducible factor (TERF1) (Zhang et al. 2016). As a result, the above experiments demonstrated that fine-tuning of ethylene biosynthesis and signaling on ROS homeostasis are critical for salt tolerance response. ETHYLENE AND SALT INDUCIBLE ERF GENE 1 (ESE1) is an EIN3 direct target gene that positively regulates salt tolerance and collaborates with EIN3 to stimulate downstream salt-related gene expression (Zhang et al. 2011). Another ethyleneinduced gene, JERF3 in tomato, improves salt tolerance by altering the expression pattern of SUPEROXIDE DISMUTASE (SOD) and CARBONIC ANHYDRASE

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(CA), leading to drought and osmotic stress tolerance in transgenic rice (Wu et al. 2008; Zhang et al. 2010). More ethylene signaling downstream regulators must be identified under salt stress to reveal the regulation of ethylene on ROS and salt stress response in ROS homeostasis.

8 Ascorbic Acid (AsA) Function in ROS Homeostasis: Contributes to Salt Tolerance Ascorbic acid (vitamin C) is an important antioxidant that functions as a component of non-enzymatic ROS scavenging during normal plant growth and stress tolerance (Akram et al. 2017). Increased salt tolerance observed in rice, potato, tomato, and citrus due to increased AsA production (Qin et al. 2016). In plants, AsA is primarily synthesised via the L-galactose pathway, and the majority of the genes involved in this pathway have already been identified (Bulley and Laing 2016). ROS accumulation in response to salt stress is determined by the activities of AsA biosynthesis enzymes and their transcriptional and translational regulation (Laing et al. 2015) by activating Ca2C signaling under salt stress (Choi et al. 2014; Liu et al. 2018). QUASIMODO1 (QUA1) is a chloroplast protein that functions upstream of a thylakoid-localized Ca2C sensor (CAS) by mediating Ca2C signaling under salt stress (Zheng et al. 2017). Furthermore, during salt responses in Arabidopsis, AsA could cause an increase in cytosolic Ca2+ as a signaling molecule (Makavitskaya et al. 2018). Factor induced by ethylene When AtERF98 binds to the promoter of a key enzyme in AsA biosynthesis encoding gene VTC1, it improves salt tolerance (Zhang et al. 2012). The posttranscriptional regulation of COP9 SIGNALOSOME SUBUNIT 5B (CSN5B) on VTC1 explains how light/dark effects on AsA concentration work (Wang et al. 2013; Li et al. 2016). Csn5b, a loss-of-function mutant, produced more AsA and a lower ROS pool, resulting in improved salt tolerance and demonstrating the positive regulation of AsA on salt response. SIZF3, a salt-induced zinc-finger protein that regulates the interaction between CSN5B and VTC1, increases AsA accumulation and improves salt tolerance (Li et al. 2018). Thus, increasing AsA content is a potential approach for improving plant salt tolerance. As a result, ethylene and AsA could have a positive effect on salt tolerance by regulating ROS homeostasis. The non-enzymatic ROS scavenging pathway, also known as the salt response, relies on non-enzymatic antioxidants rather than enzymes (Zhang et al. 2012). Experiments in Arabidopsis revealed the role of ABAINSENSITIVE 4 (ABI4) in mediating AsAsynchronized plant growth and ethylene production via transcriptional repression of ACS (Kerchev et al. 2011; Dong et al. 2016). Ethylene appears to interact with ABA to modulate AsA production (Fig. 1). However, the mechanisms underlying these modulations remain unknown.

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9 Conclusion The equilibrium between the buildup of reactive oxygen species (ROS), the operation of the antioxidant enzyme system, and antioxidants with low molecular weight results in the formation of plant cell redox homeostasis. Under stressful circumstances, plants experience a number of complex alterations that frequently result in intracellular and tissue functional problems. The ability of the homeostasis-maintaining mechanisms to work under these circumstances is crucial to survival. One of the most critical concerns that will help to address the issue of improving plant resistance to stressors is understanding the molecular processes of resistance creation to adverse environmental conditions. Numerous defence mechanisms allow plants to maintain cellular homeostasis under the effect of numerous environmental stimuli. For plants to compete and survive, timing of flowering, flower growth, and seed dissemination must be coordinated with the environment. It is crucial to regulate the appropriate responses to biotic and abiotic environmental stimuli. In all of these activities, ethylene plays a crucial regulatory and signaling role that increases a plant’s capacity for survival. Our understanding of the ethylene production and signaling pathways, their regulation, and interactions with other hormones has been made possible by ethylene mutants, epistasis studies, and biochemical characterization. Finally, it may be said that ethylene supports plant cellular homeostasis under a variety of stress conditions.

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Nitric Oxide and Cellular Redox Homeostasis in Plants Tanashvi Seth, Sejal Asija, Shahid Umar, and Noushina Iqbal

Abstract Attributing to the diverse abiotic stresses and climate fluctuations, the agriculture sector is experiencing some serious misfortunes. This largely influenced the growth, yield, and functioning of crops and have further imposed constraints on food security worldwide. Plants confront various abiotic stresses that leads to the generation of reactive oxygen species (ROS) in different cell compartments and disturb the redox homeostasis of the cells. The ROS when produced at high levels, they are considered harmful to cells and cause cellular damage whereas, at significant levels, they act as signaling molecules to provide defense responses to plants. Under stress, the accumulation of ROS within the cell tends to create an imbalance between the generation of ROS and the production of antioxidant enzymes which sets off a disproportion in the amount of ROS that builds up oxidative stress and ultimately leads to damaging effects on the cell. To combat such conditions, nitric oxide (NO) being a small, bioactive, gaseous signaling molecule employed by plants to mitigate the effects of abiotic stresses. NO is a redox molecule that assist in the scavenging of excessive ROS by promoting the activities of antioxidant enzymes and osmolytes, interacting with sulfur-assimilation pathway, upregulating the ascorbate–glutathione cycle, and utilizing nitrogen metabolism for its synthesis and therefore regulates the growth, development, and functioning of plants. In this chapter, we have documented the recent advancements indicating the harmful nature of ROS that cause oxidative damage and how it alters the cellular homeostasis within plants along with highlighting the crucial strategies utilized by NO to manage the ROS levels to establish a toxic-free environment and aid in the improvement of plant defense responses.

Tanashvi Seth and Sejal Asija are contributed equally. T. Seth · S. Asija · S. Umar (B) · N. Iqbal (B) Department of Botany, School of Chemical and Life Sciences, Jamia Hamdard, New Delhi, India e-mail: [email protected] N. Iqbal e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_7

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1 Introduction Nitric oxide (NO) is a small gaseous signalling molecule, that serves as a critical component of defence related signalling in plants under the impact of varied abiotic stressors (Goyal et al. 2021). This relatively stable free radicle was identified much earlier in mammalian systems as compared to plants, however subsequent to a series of pivotal works during the last decade of the twentieth century, NO is now firmly placed in the pantheon of plant signaling molecules (Singhal et al. 2021). The multitudinous functions of NO in safeguarding physiological processes under varied abiotic stresses has paved a way for its utilization as a bioprotectant in plant systems (Nabi et al. 2019). Extensive data on NO production in plants, suggests coexistence of multiple pathways and substrates for NO synthesis in plants including enzymatic and non-enzymatic routes likely functioning in diverse subcellular locations (Asgher et al. 2017). Reductive pathways which utilize nitrite as a substrate are catalyzed by enzymes including nitrate reductase (NR), nitric oxide forming-nitrite reductase (NOFNiR), and molybdenum containing enzymes which make use of mitochondrial electron transport chain (mETC), on the other hand, oxidative pathways oxidize reduced N containing compounds such as arginine to synthesize NO (Verma et al. 2020). Moreover, in the atmosphere nitrification and denitrification cycles produce NO as a byproduct of N2 O oxidation (Hancock et al. 2019). Under abiotic stress, cellular redox homeostasis is majorly disrupted which leads to the oxidative damage induced by reactive oxygen species (ROS) which are produced in subcellular locations including mitochondria, chloroplast, peroxisomes and nucleus (Czarnocka and Karpi´nski 2018). ROS includes free radicals such as superoxide (O− 2 ), hydroxyl (OH), perhydroxyl (HO2 − ) and alkoxy (RO) and non-radicals like, hydrogen peroxide (H2 O2 ) and singlet oxygen (1 O2 ) which rapidly reacts with cellular structures (Hasanuzzaman et al. 2020). Interestingly, ROS have dual roles in plants, at low endogenous concentrations, ROS act as signalling molecules and elicit positive response to modulate redox homeostasis, however at concentrations, ROS become toxic and provoke degradation and disruption of essential metabolic processes in plants including photosynthesis (Foyer 2018), N and sulfur metabolism (Gautam et al. 2021) and seed germination (Bailly 2019). In response to oxidative damage, NO acts as a chief detoxifier which is believed to act in two ways either by directly scavenging ROS, such as O− 2 , to form peroxynitrite (ONOO− ), which is considerably less toxic than peroxides or its acts as a signaling molecule thereby altering gene expression. Alleviation of oxidative stress mediated by supplementation with NO or via stimulation of endogenous NO biosynthesis in plants is by modulation of a multitude of parameters including antioxidant metabolism (Kaya et al. 2019a), nitrogen and sulfur assimilation (Gautam et al. 2021), regulation of ascorbate–glutathione cycle (Kaya et al. 2020c) and by inducing accumulation of compatible solutes (Ahmad et al. 2016). NO elicits activity of both enzymatic antioxidants including catalase (CAT), peroxidase (POD), superoxide dismutase (SOD), glutathione reductase (GR), ascorbate peroxidase (APX) and non-enzymatic antioxidants including glutathione

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(GSH) and ascorbate (AS A) which further scavenge ROS and stabilize altered redox balance (Christou et al. 2014). Furthermore, correlation between accumulation of GSH and enhanced sulfur assimilation in plants subsequent to supplementation with NO has been reported (Per et al. 2017). Similarly activation of the AsA-GSH cycle by NO in order to combat oxidative stress both separately and under the influence of other signaling molecules such as H2 S and salicylic acid has been documented (Prakash et al. 2021; Mfarrej et al. 2022). Moreover, current reports suggest that NO-mediates osmolyte accumulation in plants which is effective in mitigating ROSinduced oxidative damage, and the correlation between N assimilation and proline, glutamate, and polyamine levels has also been assessed in the presence of NO. This chapter emphasizes on the sources of NO, mechanism of generation of ROS and its impact on essential metabolic functions of plants. An in-depth understanding of the critical role of NO in amelioration of oxidative stress via modulation of antioxidants, induction of osmolyte synthesis, regulation of ascorbate glutathione cycle, nitrogen and sulfur assimilation under various environmental stresses would help to confer biotechnological applications to protect plants against abiotic stresses and to improve crop productivity.

2 Nitric Oxide Synthesis in Plants Nitric oxide can be synthesized from diverse routes and substrates in plants (Astier et al. 2018). Originally, two major routes for NO biosynthesis in plants have been envisioned, the first one is the reductive pathway comprising both enzymatic and non-enzymatic reduction of nitrite (NO− 2 ) to produce NO and the second one is the oxidative pathway which relies on the oxidation of aminated molecules such as amino acid L-arginine or hydroxylamine (León and Costa-Broseta 2020). The prime sites for NO synthesis are protoplasts, chloroplasts, mitochondria, and the peroxisomes in plants. However, in vascular plants, cell membrane, cytoplasm, apoplast, and endoplasmic reticulum are also reported as subcellular locations for NO generation (Gupta et al. 2021).

2.1 Enzymatic Mechanism of NO Biosynthesis in Plants 1. Nitrate reductase (NR): Nitrate reductase is a cytosolic multifunctional catalytic protein involved in the assimilation and metabolism of nitrogen in plants (Liu et al. 2022a). It is a 200 KDa dimeric metalloflavoprotein, attributing to the presence of three prosthetic groups in each subunit of this enzyme i.e. flavin adenine dinucleotide (FAD), heme (cyt b557), and a molybdenum-containing organic molecule known as pterin (Kishorekumar et al. 2020). Besides its major catalytic action in converting nitrate (NO− 3 ) to NO− 2 by utilizing NADH as an electron

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donor, its ability to reductively generate NO from NO− 2 has been well characterized in green algae and vascular plants (Wilson et al. 2008). However, a large proportion of NO− 2 generated by NR activity is further reduced to form ammonium by plastidial nitrite reductase (NiR). NO− 2 /NO reductase activity (Ni-NR activity) denotes only 1% of NR activity under normal conditions, ascribing to 10 folds higher NRkm for NO− 2 than for NO− 3 , which makes NO− 2 a limiting factor for NO production (Frukh et al. 2022). Despite the low efficacy of NRmediated NO production, its significance has been demonstrated several times, for example, in a study on Arabidopsis wherein NR is encoded by two genes NIA1 and NIA2, NR-mutants nia1, nia2, and double mutants nia1/nia2 revealed that a plethora of physiological processes including gravitropic responses (Vazquez et al. 2019), stomatal movements (Desikan et al. 2002), responses to phytohormones (Zhao et al. 2016), cold (Zhao et al. 2009), and osmotic stress (Kolbert et al. 2010) were perturbed in the absence of NO. Another mechanism of NR-induced NO production was reported in Chlamydomonas reinhardtii, where NR interacts with an associated protein, nitric oxideforming nitrite reductase (NOFNiR) to synthesize NO from NO− 2 , it is speculated that similar interaction occurs in higher plants as well during NO generation (Calatrava et al. 2017). Post-translational modification of NR in plants has also been correlated to NO production. Recently it was reported that mutation in the phosphorylation site of NR prevents the inactivation of this catalytic protein which causes NO− 2 accumulation and enhanced NO production in Oryza sativa (rice) (Han et al. 2022). In addition to NR present in cytosol, another nitrite reductase localized in the plasma membrane (PM) identified in the roots of tobacco plants, is reported to be involved in the synthesis of NO by utilizing NADH as an electron donor under anaerobic conditions (Stöhr et al. 2001). Furthermore, the coordinated catalytic action of cytosolic NR and PM-bound Ni-NOR in converting NO− 3 to NO− 2 by utilizing succinate as an electron donor was observed in the root apoplast (Reda et al. 2018). NO− 2 accumulation and subsequent NO production in plants have an advantageous role in reducing cytoplasmic acidosis caused by hypoxic conditions. Evidence suggests that hypoxia causes inhibition of NiR resulting in the accumulation of NO− 2 and subsequent NO production, ranging from 2 nmol gFW−1 h−1 to 200 nmol gFW−1 h−1 in vivo (Rockel et al. 2002; Meyer et al. 2005). Wany et al. (2018) reported that Arabidopsis NR double mutants nia 1,2 showed higher ROS accumulation under hypoxic conditions as compared to wild-type plants when treated with NO scavenger cPTIO, suggesting the significant role of NO in enhancing tolerance to hypoxic conditions (Wany et al. 2018). Moreover, NR-mediated NO production has been reported to be involved in ABAinduced stomatal closure, wherein NO supplementation to epidermal peels of Arabidopsis plants induced NO biosynthesis and stomatal closure (Sun et al. 2019) in the induction of antioxidant metabolism in response to various abiotic stresses (Sang et al. 2008), in improving tolerance to cadmium stress in Piper nigrum (pepper) (Kaya et al. 2020b), salinity tolerance in Glycine max (soybean)

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(Kataria et al. 2020), and iron deficiency in Fragaria annassa (strawberry) by regulating ascorbate glutathione cycle (Kaya et al. 2020a). 2. Nitric oxide synthase (NOS): Besides the NR-mediated NO biosynthesis route, several other pathways for NO generation have been discovered so far. In mammalian systems, NO is generated predominantly via the catalytic action of NOS which is a homodimeric protein comprising two distinct monomers, an N-terminal oxygenase domain with a haem-thiolate protein, and a C-terminal reductase domain, which resembles P450 reductase and contains binding sites for NADPH and FAD (Santolini et al. 2017). NOS generates NO and citrulline from L-arginine, entailing multiple co-factors such as NADPH, FAD, FMN, Ca2+ , calmodulin, and tetrahydrobiopterin (BH4 ) vital for its catalytic action (Corpas et al. 2009). This reaction involves the transfer of five electrons from NADPH to the final acceptor molecule heme via FAD and FMN. Early experiments in plants detected NOS-like activity in peroxisomes, root, stem, and leaves of Pisum sativum (pea plant), soybean, and Nicotiana tabacum (tobacco). Presently NO burst via catalytic action of NOS was reported to be involved in alleviating water stress-induced oxidative damage in rice (Cao et al. 2019) and chilling injury in walnut plants (Dong et al. 2018). Three isoforms of NOS are primarily involved in NO biosynthesis in animals, neuronal NOS (nNOS or NOS1), inducible NOS (nNOS or NOS2), and epithelial NOS (eNOS or NOS3) (Kumar and Pathak 2018). A protein isolated from Arabidopsis, AtNOS1, was speculated to have mammalian NOS-like activity, however, this protein is dependent only on three co-factors including NADPH, Ca2+ , and calmodulin indicating partial similarity with mammalian NOS (Hussain et al. 2022). Additionally, 45% similarity with human NOS was exhibited by a NOS-like protein present in green algae Osteroccocus tauri in terms of its Km for L-arginine (Weisslocker-Schaetzel et al. 2017). Even though NOS-like activities have been detected in several plant extracts which are also inhibited by mammalian NOS inhibitors, concurrent data indicates that, instead of producing NO via evolutionarily conserved NOS enzymes, higher plants have developed finely regulated nitrate assimilation and reduction processes to produce NO through mechanisms distinct from those present in animals. 3. Mitochondrial electron transport chain (mETC): Nearly all complexes of the mitochondrial ETC are capable of interacting with NO, either as a source or as a target of NO (Gupta et al. 2018). For instance, complex I and rotenone-resistant NADPH dehydrogenases are involved in the regulation of NO production under hypoxic conditions. Complex III and IV are major sites for the formation of NO, which later participates in the phytoglobin-NO cycle and results in redox homeostasis. Moreover, NO induces alternative oxidase (AOX) which in turn regulates mitochondrial NO production. Complex II is a target site for NO wherein, NO inhibits Fe-S centres and regulates ROS production. Since, mETC- dependent NO− 2 reduction to form NO is highly sensitive to oxygen, the contribution of this pathway towards NO production under normoxic still remains unclear and required further investigation (Alber et al. 2017).

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4. Xanthine oxidoreductase (XOR): Xanthine oxidoreductase is a molybdenumcontaining anaerobic enzyme that has the ability to reduce organic and inorganic nitrates along with nitrites to produce NO (Allagulova et al. 2022). XOR exists in two convertible forms superoxide-producing xanthine oxidase and NO− producing xanthine dehydrogenase (Khan et al. 2015). Xanthine oxidoreductase was identified in leaf peroxisomes of pea (Pisum sativum) plants, wherein 70% of the enzyme exists as xanthine oxidase, while 30% exists as xanthine dehydrogenase. In the presence of oxygen, superoxide formation occurs, which further reacts with NO to form peroxynitrite, however in its absence NO is produced.

2.2 Non-Enzymatic Mechanism of NO Biosynthesis in Plants N2 O oxidation results in the production of NO as a by-product via nitrification/denitrification cycles in the atmosphere. Non-enzymatic reduction of NO− 2 leads to the production of NO at acidic pH, where nitrite dismutates to produce NO− 3 and NO. Ascorbic acid can also reduce NO− 2 to produce dehydroascorbic acid and NO at a pH range of 3–6 in the apoplastic space or in the cytosol of the plant cell. Inside the aleurone cells of Barley plants, ascorbate reductively generates NO at an acidic pH (Igamberdiev et al. 2006). Similarly, in Vicia faba (broad beans), salicylic acid and H2 O2 -induced reduction of NO− 2 was observed which led to the production of NO in companion cells of phloem tissue (Zou et al. 2012). Another pathway of NO production involves the light-mediated conversion of NO− 2 to NO facilitated by carotenoids. Moreover, NO generation was observed subsequent to hydroxylamine application in tobacco cell cultures which were insufficient in nitrate reductase (Kaiser et al. 2018). Figure 1 represents the route for NO synthesis in plants.

3 Reactive Oxygen Species and Their Mechanism for Causing Oxidative Stress in Plants Reactive oxygen species are natural by-products of cellular metabolism in plants confronting different types of stresses which play dual functions in the cell based on their concentration in plants. The high levels of ROS are toxic to the cell and lead to cellular damage whereas at appreciable amounts it acts as a signalling molecule that transduces signals to provide plant defense responses against a variety of stresses (Nadarajah 2020). ROS comprises hydroxyl radicals (OH• ), singlet oxygen (1 O2 ), hydrogen peroxide (H2 O2 ), and superoxide radicals which results from the oxidation of oxygen molecules and occurs in various subcellular compartments (Nouman et al. 2014). The lifespan of these ROS species ranges in nanoseconds whereas that of H2 O2 and O2 −• ranges slightly longer (milliseconds to seconds), depending mostly on the ROS scavengers present in the surrounding (Mattila et al. 2015). Production

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Fig. 1 Reductive and oxidative routes for biosynthesis of NO in plants. Ca2+ , calcium ion; FAD, flavin adenine dinucleotide; FMN, flavin mononucleotide; H2 O, water; PMNR, plasma membrane nitrate reductase; PM-NiNOR, plasma membrane bound: NO reductase; mETC, mitochondrial electron transport chain; NADP, nicotinamide adenine dinucleotide phosphate; NADPH, nicotinamide adenine dinucleotide phosphate; NO2 − , nitrite; NO3 − , nitrate; NOS, nitric oxide synthase; NR, nitrate reductase; XOR, xanthine oxidoreductase

of ROS is additionally and continually connected with key metabolic exercises in various cell compartments, particularly peroxisomes, mitochondria, and chloroplasts (Couée et al. 2006). It has now long been established an interrelation between ROS and osmotic stress, that various stressors contribute towards the increment of ROS within the cell that ultimately leads to the development of oxidative stress in plants. Oxidative stress could be inferred as a state of imbalance between oxidants and antioxidants that disrupts redox homeostasis which causes faulty redox signaling and triggers cell damage in plants (Dumanovi´c et al. 2021). ROS at basal level is kept up with above cytostatic or beneath cytotoxic level, is, subsequently, key for legitimate ROS or redox motioning in cells, and this level is kept up by maintaining an equilibrium between ROS production and scavenging (Hasanuzzaman et al. 2019). In any case, any aggravation in the balance of ROS production and scavenging of ROS by antioxidants prompts overaccumulation of ROS bringing about oxidative stress on exposure to different types of abiotic stress conditions (Hasanuzzaman et al. 2019). The production and scavenging of ROS should be completely controlled to circumvent the deleterious effects of oxidative stress under abiotic stresses. However, an extreme increase in the ROS concentrations within the cells becomes a principal contributor to oxidative stress. Oxidative stress in plants often results in oxidation of DNA, degradation, and modification of RNA, lipid peroxidation, destruction of proteins, and ion leakage that drastically affect the growth and yield of various crops (Maurya 2020). Excessive accumulation of ROS within the cells causes deleterious effects on organelles as well as tissues of plants (Munns and Gilliham 2015).

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ROS levels above the threshold are the chief reason to cause lipid peroxidation of membranes under stressful conditions (Mishra et al. 2011). The peroxidation of polyunsaturated unsaturated fatty acids by ROS can prompt chain breakage and, accordingly, assist in increased membrane permeability (Sharma et al. 2012). ROS also involved in the oxidation of proteins wherein they trigger protein denaturation (Hasanuzzaman et al. 2020). Generation of ROS often leads to electrolyte leakage (EL) which occurs as a result of electron transport from different compartments like mitochondria, chloroplasts, and plasma membranes or occurs via various metabolic processes within the cell (Kao 2017). It is again well documented that ROS has also shown its negative consequences on DNA by oxidizing its sugar residues, influencing molecular processes like replication and transcription (Banerjee and Roychoudhury 2018). Alongside, oxidative stress-mediated modification of amino acids is also very common, with the most susceptible amino acids being g cysteine (Cys), histidine (His), methionine (Met), tyrosine (Tyr), and tryptophan (Trp) (Farooq et al. 2019) and also affect post-translational modifications like proteome-wide analysis in Arabidopsis has shown 500 Met oxidation sites which are prone to oxidative stress in about 400 proteins that are involved in ROS-mediated reverse post-translational modifications (Jacques et al. 2015). The imbalance between electron transport and the carbon reduction cycle becomes a crucial agent to affect the normal functioning of the photosynthesis process by inducing ROS accumulation within cells (Bhattacharjee 2019). Overproduction of ROS leads to disruption of membrane integrity, high MDA levels, increase in the number of plastoglobules in affected chloroplasts which induces disintegration of the thylakoid membrane and reduced photosynthesis and ultimately leads to programmed cell death in Oryza sativa (rice) varieties, Swarna and Swarna Sub1 under submergence-induced oxidative stress (Basu et al. 2021). Similarly, salinity-induced oxidative stress causes a decrease in physiological boundaries and consequently the photosynthesis of the plants, for example, photosynthetic rate, stomatal conductance, natural CO2 fixation, happening rate, relative chlorophyll items, and relative water contents (RWC) in Brassica napus (canola) (Naveed et al. 2020). In another study, it is reported that accumulation of both abscisic acid (ABA) and ROS, can tremendously hinder seed germination and development in rice exposed to heat and drought stresses together (Liu et al. 2019). Taken together, these studies indicate that ROS works based on its concentration, mostly if occurs in excessive amounts, it leads to several deleterious effects in plants and promotes the development of oxidative stress which is toxic to the cell environment and contributes toward producing damaging effects in plants under abiotic stresses.

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4 Redox Homeostasis: Essentiality for Plant’s Metabolic Functions Metabolic processes play a crucial role in the lives of all aerobic organisms to accomplish the demand for energy for their sustenance. However, the accumulation of unavoidable by-products often disturbs the redox homeostasis and is responsible for causing deleterious effects in the cell. A study conducted on Solanum lycopersicum (tomato), unveils the negative impacts of zinc starvation on the redox state which affects biomass, the integrity of cells, and chlorophyll content and disturbs the overall photosynthesis in plants (Kabir et al. 2021). Likewise, submergence in rice accumulates ROS that affects redox balance and further induces lipid peroxidation of membranes, electrolyte leakage, lower the number of phospholipids, depletes starch content under hypoxic conditions, disintegrates thylakoid membrane and thereby chlorophyll content and photosynthesis (Basu et al. 2021). Similarly, copper (Cu) stress in Hordeum vulgare (barley) inhibits the growth and photosynthetic efficiency (photosynthetic pigments and maximum photosystem II efficiency) of seedlings which is consistent with the increase in the ROS along with the reduction in the glutathione (GSH) and ascorbate (AsA) (Ben Massoud et al. 2022). In addition, it is reported that salinity affects growth rate, nitrogen metabolism, the content of nonenzymatic antioxidant enzymes, and photosynthetic pigments because of disturbance in the ionic balance as it creates a redox imbalance and resulting in significant growth and productivity of wheat plants (Saad-Allah and Ragab 2020). To counteract such conditions, plants have developed fine machinery to modulate the redox homeostasis needed to maintain an equilibrium state within the plants under both normal and stressed circumstances. Nitric oxide, a small reactive gaseous molecule, acts in concentration and redox dependent manner to combat oxidativestress induced by various abiotic factors, either via acting as an antioxidant and directly scavenging ROS such as superoxide anions (O2 − *) to generate peroxynitrite (ONOO− ), or by acting as a signalling molecule in order to maintain redox homeostasis in plants and thereby safeguard a plethora of metabolic functions from oxidative damage. For instance, SNP supplementation in arsenic-stressed tomato plants revealed NO mediated protective effects on chlorophyll and in modulating proline metabolism (Ghorbani et al. 2021), enhancing photosynthetic efficiency in rice plants under high temperature stress (Gautam et al. 2022), improving photosynthetic nitrogen use efficiency, together with enhancing sulfur metabolism in mustard plants under salinity stress (Jahan et al. 2020). Furthermore, high rates of respiration generate ROS, which delays germination in plants, however, treatment with NO donor SNAP, reduced respiration in chickpea variety Kabuli, which decreased ROS levels, and alleviated ROS induced suppression on germination (Pandey et al. 2019), similarly, in magneto primed soyabean seeds subjected to salinity stress, germination was demonstrated to be induced by NO via modulation of ROS homeostasis, its interaction with ABA,GA and IAA, and lowering Na+ /K+ ratio. Contemporary reports imply a significant defensive role of NO in scavenging ROS and simultaneously modulating various essential metabolic processes in plants including photosynthesis, sulfur and

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Fig. 2 Schematic representation of nitric oxide- mediated defense responses to maintain the cellular homeostasis within plants under various environmental cues. APX, ascorbate peroxidase; CAT, catalase; GPX, glutathione peroxidase; GR, glutathione reductase; GSH, glutathione; GSSG, glutathione disulfide; GST, glutathione s-transferase; H2 O, water; H2 O2 , hydrogen peroxide; NR, nitrate reductase; NO, nitric oxide; NO3 − , nitrate NOS, nitric oxide synthase; OH− , hydroxide ion; 1 O2 , singlet oxygen; O2 − , superoxide anion; PUT, putrescine; ROS, reactive oxygen species; SOD, superoxide dismutase; SPD, spermidine; SPM, spermine; TPC, total phenolic content

nitrogen metabolism, and respiration under fluctuating environmental conditions. Figure 2 shows the regulation of redox homeostasis by NO.

5 Nitric Oxide in Maintaining Redox Homeostasis Under Abiotic Stress 5.1 Role of Nitric Oxide in Enhancing Antioxidative Enzymes Nitric oxide (NO) is notable for further developing plant protection from numerous stresses by regulating the activities of several antioxidant enzymes and thereby improving tolerance for the same. NO has a huge part in detoxification which assist in providing constitutive resistance in plants under unfavourable conditions. There are enormous studies connected with the augmentation of antioxidant enzyme activities and adjusting their amount in response to the treatment of NO donors in plants like exogenously applied NO donor, sodium nitroprusside (SNP) is identified to improve arsenic (As) tolerance which has a tendency to hyper accumulate in Isatis cappadocica by stimulating the activity of superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione reductase (GR), glutathione S-transferase (GST), glutathione

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(GSH), in a way affirming the useful role of NO in expanding As resilience (Souri et al. 2020). Rice at the germination stage, were exposed to chilling stress (5.0 ± 1.0 °C for 8 h day−1 ) showed an increase in oxidative parameters like enhancing the levels of superoxide, H2 O2 , MDA, decrease in antioxidants and osmolytes. However, seeds were then pre-treated with 100 μM SNP is shown to positively enhance enzymatic antioxidants APX and catalase (CAT) by 28.40% and 31.80%, respectively whereas a decrease in the CAT activity was observed compared to chilling-stressed rice seedlings along with stimulating the activity of non-enzymatic antioxidants like ascorbate content (AsA), carotenoids, and total phenolic compounds (TPC) by 20.31%, 84.37%, and 72.94%, respectively which was supported by PCA which further assist in highlighting the relation between NO and antioxidants (Sohag et al. 2020). Application of NO has proved effective in inducing the enzymatic antioxidants (SOD, CAT, APX, peroxidase [POX], and SOD) during low drought conditions by about 5% whereas an increment in the non-enzymatic antioxidants (total phenol, flavonol, and tocopherol) was also shown depending on the severity of stress in Glycine max (soybean) exposed to drought stress (Rezayian et al. 2020). Similarly, in salt-stressed mangrove species Kandelia obovata, SNP treatment assists in enhancing SOD that aids in the transformation of O2 •− to H2 O2 and O2 along with increasing the content of enzymes APX, GPX, GST, and AsA, which allow excessive scavenging of ROS to detoxify the system and make the plants salt-tolerant for the same (Hasanuzzaman et al. 2021). Likewise, treatment of SNP (0.1 mM) to Capsicum annuum (pepper) plants imposed to either cadmium (0.1 mM CdCl2 ) or lead (0.1 mM PbCl2 ) stress or in a combination of both stresses, resulted in the rise in the activities of enzymatic antioxidants of leaf-like POX, SOD, CAT, lipoxygenase accompanied by an increase in the non-enzymatic enzymes ascorbate and glutathione (Kaya et al. 2019a). In another related report, the most optimum concentration of SNP is 100 μM, which is viewed as powerful in the evacuation of ROS by reinforcing the antioxidant system like a surge in APX and GR activities together with the synthesis of AsA and GSH which are vital for the transport of electrons to oxygen in chloroplasts and therefore aid in improving the photosynthetic rate in the nickel (Ni)-induced oxidative stress in Solanum melongena (eggplant) (Soliman et al. 2019). Similarly, Cyclocarya paliurus a common plant used to treat diabetes, is majorly affected by salinity stress (Liu et al. 2022c). So, to ensure its longevity without affecting its productivity, its seedlings are pre-treated with NO donors (S-nitroso-N-acetylpenicillamine, SNAP and S-nitrosoglutathione, GSNO and sodium nitroprusside, SNP) which resulted in enhancing both enzymatic and non-enzymatic antioxidant activities like APX, POD, and GSH owing to various types of post-translational modifications (PTMs) which are also efficient to minimize H2 O2 and alleviate the negative impacts of salt stress in plants (Liu et al. 2022b). Moreover, there have been bits of evidence suggesting that endogenous NO is viewed as a putative molecule that can keep up in regulating antioxidant levels in plants. It is reported that the endogenous NO levels are known to activate the HY5 transcription factor which upregulates the expression of chalcone synthase (CHS) and chalcone isomerase (CHI) and assists in a further increase in flavonoid and anthocyanin content which are considered crucial for absorbing UV-B radiation and

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simultaneously eliminates ROS from plants (Cassia et al. 2019). There is an indirect connection that is built between phytohormones and NO that assist in maintaining endogenous levels of NO and further enrich the defense system in plants like foliar application of 24-epibrassinolide (1.0 μM) which induced synthesis of endogenous NO which is involved in influencing antioxidant enzymes like CAT, POD and assist in lowering H2 O2 and MDA to increase tolerance to water-stressed pepper plants (Kaya et al. 2019b). These results were confirmed by the application of NO scavenger cPTIO, which considerably reduced endogenous NO and reversed the key responses which occurred because of EB-induced NO levels in pepper plants, confirming its role as a crucial downstream signaling molecule (Kaya et al. 2019b). Likewise, two wheat species (Triticum aestivum L. cv. Pandas and Triticum durum cv. Altıntoprak 98) were grown under boron toxicity (0.2 mM) and later subjected to a weekly foliar spray of thiourea (TU) (200 or 400 mg L−1 ) led to the increment in the endogenous NO levels in leaves which aid in promoting the activities of antioxidants POX, SOD, CAT, and lipoxygenase. On the contrary, the content of soluble sugars (SS), soluble proteins, and phenols content are observed in lowered amounts in the plants (Kaya et al. 2019c). Rice seedlings exposed to drought stress leads to reduced root N uptake rate, depress the photosynthetic rate, and further aid in increasing NO burst due to water-stressed conditions. However, these problems were relieved after the treatment of seedling with NH4 + supplementation which helped in producing early NO burst mediated by nitric oxide synthase (NOS), which facilitated upregulation of antioxidant enzymes, and indorse downregulation of ROS deposits in rice roots exposed to aluminium (Al) stress. These results were further confirmed by using NO scavenger which led to reduced activity of SOD and CAT in NH4 + -treated roots of the rice plants (Cao et al. 2019). Consequently, jointly the above studies feature the key role of NO which is either produced endogenously or applied exogenously and aids in intervening in the ascent of both enzymatic as well as non-enzymatic antioxidants in plants to restrict the number of harmful oxygen radicals and play critical roles in alleviating oxidative damage induced by a variety of abiotic stressors in plants in light of the fact that NO can itself act an antioxidant molecule.

5.2 Nitric Oxide, Sulfur Assimilation, and Glutathione: A Way for Reducing Reactive Oxygen Species Cellular metabolism continuously produces ROS at basal levels in different locations within the cell and therefore it is important for the cell to constantly eliminate excessive ROS so that it does not harm the internal cell environment and cause any further damage to the cells and plants thereof. It is thus crucial for the plants to maintain a steady equilibrium state between ROS generation and ROS scavenging so that it does not disrupt redox homeostasis and cause extensive injuries to the cell. Therefore, evolution has furnished plants with a more extensive scope of protection which incorporate changes at the morphological, metabolic, and hereditary level to adjust

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to unusual circumstances (Das and Roychoudhury 2014). There are different ways wherein the plants employ strategies to maintain the levels of ROS so that it does not interfere with the proper functioning of various metabolic processes occurring in the plants. One of the most crucial responses is the utilization of nitric oxide (NO), both as an antioxidant as well as a signalling molecule that aims to neutralize the toxic environment of the cell that is under the influence of several stressors. NO is known to be a multifunctional molecule that has the potential to regulate several cellular processes under various types of abiotic stresses. Higher plants impacted with As stress often creates an imbalance in ROS concentration which commonly leads to the production of nitro-oxidative stress in plants which is known to be relieved by exogenous NO application that stimulates several antioxidant enzymes, increase the expression of transport and stress-related genes, induce the synthesis of sulfur compounds like phytochelatins (PCs), and amend modifications for cell wall composition of roots in plants (Bhat et al. 2021). Similarly, Brassica juncea (Indian mustard) exposed to cadmium (Cd) stress (100 μM) considerably increases the ROS and MDA levels. So, treatment with SNP (NO donor) to such plants triggered the antioxidant levels to re-establish the redox status in these plants and help them to detoxify excessive Cd, increase the photosynthesis process, and overall improve the plant growth (Khator et al. 2021). Mostly, NO and ROS are generated at the same time within the cell and both are therefore involved in a common reaction wherein NO reacts with superoxide anion (O2 ·− ) to give peroxynitrite (ONOO− ), so that radicals and NO are eliminated from the cell environment to maintain stable homeostasis and also assists peroxynitrite to itself act as a signalling molecule which aids in the production of stress-buster responses because of the mutual action of both NO and ROS signalling (Hancock and Neill 2019). NO aids to control ROS in a cell by reacting with O2 − to produce NO3 − which limits the accumulation of excessive H2 O2 (Mittler et al. 2012; Katano et al. 2018). In addition, NO mediates reduction in O2 − by lowering MDA levels, scavenging superoxide anions, limiting lipid peroxidation, increasing the activity of SOD isoforms, and overall inhibiting ROS accumulation because of salinity-induced oxidative stress in maize leaves (Klein et al. 2018). NO is well-known to maintain ROS concentration by equalizing a balance among ROS, GSH, GSNO, and AS, when ROS levels are increased beyond the limit, NO induces transcription of SOD, APX, and CAT genes (Cassia et al. 2018). Therefore, NO can act as a central player in promoting tolerance in plants against ROS-induced oxidative stress to preserve the cellular redox homeostasis in plants. Another detoxification strategy employed by plants is to limit the production of excessive ROS from cells by increasing the process of sulfur (S)-assimilation which promotes the synthesis of S compounds that act as a response against abiotic stresses in plants. Sulfur and its derivatives stimulate the antioxidant system as well as help to eliminate excessive ROS under various abiotic stresses (Hasanuzzaman et al. 2018). Sulfur applied to soil is known to relieve the adverse consequence of Cd on S-assimilation, and photosynthetic capabilities, by lowering lipid peroxidation, electrolyte spillage, and receptive oxygen species like ROS, and H2 O2 , O2 •− in mustard (Mir et al. 2021). In addition, an interaction between salt stress and S metabolism has been examined concerning the adaptation of Olea europaea L. (olive) shoots by

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utilizing S assimilation to invigorate the activity of antioxidants, thereby reducing the excessive ROS accumulation to satisfy and fulfil the high demand for sulfur in the plants (Bashir et al. 2021). There are several pieces of evidence suggesting that NO interacts with the process of S-assimilation to combat the deteriorating effects caused due to the generation of oxidative stress. It is reported that NO and S are well known to impart salt tolerance in plants by modulating GSH synthesis, inducing the formation of S compounds, and regulating the antioxidant defense system (Fatma et al. 2016a). In related research conducted on Brassica juncea (mustard) under salinity stress, combinatorial application of NO (100 μM) and S (200 mg S kg−1 soil) result in a reduced levels of superoxide radicals and other ROS along with augment the amount of cysteine (Cys), lowered glutathione (GSH) which aids in the activation of the antioxidant defense system, thereby improve S-assimilation process (Fatma et al. 2016b). Likewise, treatment with 100 μM SNP (NO donor) significantly combat the consequences of oxidative damage caused by Cd (50 μM) stress in mustard plants. SNP enhanced the accumulation of ROS-scavenging compounds like APX, SOD, GSG, and GR along with modulating S-assimilation, increasing photosynthesis, and chlorophyll content, and inhibiting the excessive accumulation of H2 O2 and thiobarbituric acid reactive substance (TBARS) content (Per et al. 2017). Similarly, in drought-tolerant (NK8711) and drought-sensitive (P1574) maize seedlings, an exogenous foliar treatment of SNP doses (0, 50, 100, 150, and 200 μM) was performed under normal and drought stress conditions to observe its effect on regulating the S-assimilation pathway enzymes. The optimum concentration was 100 μM at which NO facilitated the upregulation of S-assimilation enzymes such as glutathione reductase, glutathione S-transferase, and guaiacol peroxidase. However, 150 and 200 μM resulted in a negative impact of SNP especially in P1574 than NK8711, and ultimately results in the reduction in biomass under drought conditions (Majeed et al. 2018). In another research conducted on tomato seedlings, it is observed that under S deficiency, NO has shown to play a crucial role in lowering the ROS levels in roots and leaves, mitigates low S-induced lipid peroxidation, NOmediated rise in the production of H2 S, which assist in improving S-assimilating enzymes (ATP sulfurylase, adenosine 5-phosphosulfate reductase, sulfide reductase, and O-acetylserine (thiol) lyase), assists in inhibition of ROS along with overall recovering the S-uptake and S acquisition (Siddiqui et al. 2020). Also, treatment of tomato seedlings with 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy l3-oxide (an NO scavenger) repressed the functions performed by NO which leads to the generation of low S-conditions that results in the promotion of S-induced oxidative stress (Siddiqui et al. 2020). This way interaction between NO and S-assimilation is important for activating the defense responses as both of them have the potential to hinder the negative impacts caused by ROS under different types of abiotic stresses in crops. A small thiol molecule, glutathione (GSH; γ-glutamyl-cysteinyl-glycine) is considered a strong non-enzymatic antioxidant enzyme that has a remarkable role to detoxify ROS and also in its redox state, it triggers the transduction of signals (Hasanuzzaman et al. 2017). Due to the presence of a highly reactive group in GSH, it has the potential to scavenge cellular H2 O2 , singlet oxygen, superoxide, and hydroxyl

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radicals along with reprograming of the cellular homeostasis by activating the antioxidant system efficiently (Banerjee and Roychoudhury 2019). In a cellular environment, GSH acts as a redox buffer that changes itself either to GSH (reduced) or to GSSG (oxidized) state under control conditions. The calibration of the GSH/GSSG ratio decides all-inclusive redox homeostasis in plants and advances plant endurance during sub-ideal conditions (Banerjee and Roychoudhury 2019). Glutathione reductase (GR) maintains a high GSH/GSSG ratio which helps to balance ROS efficiently and also has a role in improving photosynthesis in plants (Müller-Schüssele et al. 2020). Recently, in a related study, the effect of GSH was assessed in soybean under arsenate (AsV) and arsenite (AsIII) stress by treating the plants with an inhibitor of GSH, i.e., BSO (L-buthionine-sulfoximine). This BSO treatment resulted in a significant reduction of GSH in roots and leaves, a decrease in the content of phytochelatins (PCs) synthesis, membrane damage due to a reduction in the levels of antioxidant enzymes, and an increase in the deleterious effects of As on gas exchange and PSII yield which indicate that GSH modulates As levels by altering its accumulation pattern which assists in promoting As stress tolerance in plants (Vezza et al. 2019). Similarly, in another related report, it is observed that overexpression of soybean’s transcription factor GmNAC085 functions to maintain GSH levels by regulating GSH-induced ROS elimination, upregulating the expression of GSH-biosynthetic genes (GSH1 and GSH2), assists in removing excessive methylglyoxal (MG) by stimulating the activities glyoxalase (Gly I and Gly II) to improve drought tolerance in Arabidopsis (Nguyen et al. 2019). In a recent study, the application of exogenous GSH on rice seedlings under arsenic (As) stress resulted in a significant improvement in the As-induced oxidative stress by maintaining a stable redox environment which further stimulate the ascorbate (AsA) redox ratio by inducing the AsA-GSH cycle (Jung et al. 2019). Likewise, exogenous foliar application of glutathione (GSH; 0, 0.4, and 0.8 mM) was investigated on Capsicum frutescence (chili peppers) under salt and drought stress. This led to the accumulation of osmoprotectants, glutathione, capsaicin, and phenolic contents, improved water use efficiency (WUE), and maintain a stable K+ /Na+ ratio which recover the overall growth and yield of the plants. It was found that 0.8 mM GSH was considered the optimum concentration for satisfactory growth and yield results under deficit irrigation water (DiW) at 80% soil field capacity (FC) and salinity (6.74 dS m–1 ) (Al-Elwany et al. 2020). These instances indicate the effect of GSH on inducing abiotic stress tolerance in plants. The utilization of genetic engineering for GSH-related genes could pave way for upregulation of their expression to maintain high intracellular GSH levels within the cell that will aid in the elimination of cellular ROS and stimulate the antioxidant system to generate crops that exhibit multiple stress-tolerant phenotypes.

5.3 Nitric Oxide in Regulating Ascorbate–Glutathione Cycle The ascorbate–glutathione cycle also known as Foyer–Halliwell–Asada cycle acts as a vital pathway for detoxifying H2 O2 in multiple cellular compartments including

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mitochondria, chloroplast, peroxisomes, and cytosol (Hossain et al. 2017). These non-enzymatic antioxidants i.e., AsA and GSH are utilized in a series of reactions catalyzed by four antioxidant enzymes identified in peroxisomes of Pisum sativum (pea) plants including ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and glutathione reductase (GR) (Jimenez et al. 1997). Due to the high redox states of AsA and GSH, they are capable of interacting with multiple components and pathways in order to retain their reduced state (Hasanuzzaman et al. 2019). Attributing to the presence of APX in the majority of the cellular compartments and its high affinity towards H2 O2 , it effectively converts H2 O2 into water via utilizing AsA as an electron donor, which further forms monodehydroascorbate (MDHA), however some of it is disproportionately converted back to form AsA and dehydroascorbate (DHA). MDHAR re-reduces the remaining MDHA to produce AsA. Subsequently, DHA is further catalytically reduced to AsA using GSH as an electron donor, via catalytic action of DHAR, converting GSH to disulfide GSSG. Gamma-glutamyl transpeptidase (GT) converts GSH to form GSH derivatives and induces other antioxidant enzymes to eliminate peroxides produced by oxidative stress. NO has the potential to enhance the reducing ability of AsA-GSH cycle and effectively scavenge ROS radicals that cause oxidative stress in the plant, for instance, treatment with 10 μL of NO enhanced the activities of DHAR, APX, GT, and GR, together with a decrease in the contents malondialdehyde content (MDA) and sustenance of high level of DPPH radical scavenging activity in (Prunus persica) peach fruit, thereby delaying senescence and maintain high antioxidant capacity during storage (Ma et al. 2019). Accumulating evidence suggests that NO plays a central role in the improvement of redox homeostasis via modulation of the AsA-GSH cycle under various abiotic stresses, such as in heat-stressed Oryza sativa (Rice) plants, 100 μM SNP (NO donor) stimulated photosynthetic nitrogen use efficiency (NUE), SUE, AsA-GSH cycle via improving enzymatic action of APX, GR together with increasing content of GSH, and accumulation of proline which lowered oxidative damage induced by high-temperature stress (Gautam et al. 2021). Similarly, in a recent study on arsenic stress in Glycine max (soybean) roots, NG-nitro-L-arginine methyl ester (L-name) treatment which is a NOS inhibitor (500 μM), led to downregulation of AsA-GSH cycle, however exogenous application of NO (SNP, 50 μM) and H2 O2 (1 μM) triggered AsA-GSH cycle components including APX, DHAR, MDHAR, and GR (Ma et al. 2019). Rendering to recent studies, possible crosstalk between salicylic acid and NO has also played an important role in reducing H2 O2 content in plants via up-regulation of AsA- GSH metabolism. Kaya et al. (2020c) reported that pre-treatment of Capsicum annuum (pepper) plants with salicylic acid (0.5 mM) under salinity stress (100 mM NaCl), effectively up-regulated the activities of enzymes involved in AsA-GSH cycle including APX, GR, DHAR, and MDHAR, however, on supplementation with cPTIO, scavenger of NO, the increase in enzymatic activities was reversed, suggesting that SA triggers endogenous NO, which in turn enhances AsA-GSH cycle mediated alleviation of oxidative stress (Kaya et al. 2020c). Correspondingly, in salt-stressed Vigna angularis, co-application of 100 μM NO and 1 mM SA proved

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beneficial in improving the activities of APX, DHAR, GR, SOD, and CAT suggesting that NO along with SA is a highly efficient strategy for reliving salinity stress in plants (Ahanger et al. 2019). A similar interaction between two gasotransmitters, H2 S and NO has also been reported to enhance antioxidant defence, for example, application of H2 S donor, NaHS (100 μM) stimulated nitrate reductase (NR) activity which further induced NO production in pea seedlings subjected to arsenic stress (50 μM), wherein endogenous NO successfully maintained redox balance by improving the ratios of AsA/DHA and GSH/GSSG which deteriorated under toxicity induced by high arsenic levels in the plant, moreover both NO and H2 S were reported to be involved in reducing As levels and enhancing AsA-GSH cycle (Singh et al. 2015). A succeeding study on exogenous application of NO and H2 S in heat-stressed Triticum aestivum (wheat) plants, showed reversal of repression of photosynthesis caused by the accumulation of glucose due to high temperature (40 °C) via improving AsA-GSH metabolism, which further reduced H2 O2 and thiobarbituric acid reactive substance (TBARS) content (Iqbal et al. 2021). Moreover, scavenging of H2 S by hypotaurine (HT) revealed a reduction in endogenous NO synthesis which confirmed the downstream action of H2 S in stimulating NO-mediated heat tolerance. Besides heat stress, SNP application was also reported to regulate toxicity caused by ZnOPs (100–200 μM) in Triticum aestivum (wheat) seedlings, wherein ZnOPs inhibited the activities of APX, GR, MDHAR, and DHAR activities which resulted in highly reduced ratios of AsA/DHA and GSH/GSSG, conversely, SNP application reversed the inhibition of enzymes involved in AsA-GSH cycle, lowered the accumulation of Zn in xylem and phloem saps, thereby lowering oxidative stress, reflected by reduced the amounts of MDA (Tripathi et al. 2017). In summary, the present findings suggest that NO activates the AsA-GSH cycle in order to combat oxidative stress both separately and under the influence of other signaling molecules such as H2 S and salicylic acid, and has a remarkable role in delaying senescence, improving tolerance to salinity, heat stress, and heavy metal stress by scavenging ROS and dealing with oxidative damage in plants.

5.4 Nitric Oxide, Nitrogen Metabolism, and Osmolytes in ROS Reduction It is well established that NO production in plants is closely linked to nitrogen assimilation and metabolism due to its synthesis from organic and inorganic nitrogen sources, on the other hand, accumulating evidence suggests that NO has a major impact nitrogen metabolism of plants, moreover, osmolytes such as proline and polyamines which are up-regulated by application of NO under oxidative stress act as sinks of N-assimilation. Hence, their cumulative role in maintaining the redox balance in plants has been examined over the years. NO is generated either by the reduction of inorganic nitrogen by NO− 2 dependent pathway involving cytosolic NR which leads to NO production under conditions involving NO− 2 accumulation in the

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cell or oxidation of organic nitrogen by the arginine-dependent pathway culminates in the generation of NO. NO deficient mutants of Arabidopsis nia1 and nia2 subjected to transcriptomic analysis revealed an increase in RBOHD, a ROS synthesis gene suggesting accumulation of ROS in absence of NR mediated NO biosynthesis, which led to altered leaf phenotypes, and impaired photosynthetic parameters in the plant (Pan et al. 2019). Recently, the involvement of NR-mediated NO production was reported in multi-walled carbon nanotube-induced salt stress tolerance in Brassica napus (rapeseed) via re-establishment of redox and ion imbalance, reduction of ROS, decrease in thiobarbituric acid reactive substances production, and lowering the Na+ /K+ ratio (Zhao et al. 2019). Furthermore, alleviation of copper stress in Hordeum vulgare (barley) plants via NO was examined by utilizing NR and NOS inhibitors i.e., tungstate and L-NAME, wherein tungstate effectively suppressed NO-mediated copper stress tolerance (Hu et al. 2015). Numerous reports have also indicated the role of NO in modulating N uptake, metabolism, and remobilization in plants for instance, NO upregulated gene expression of ammonium transporters AMT1:1 and AMT1:2, increased the activity of glutamate dehydrogenase (GDH), enhanced N content in leaves, improved osmotic regulation and ROS scavenging by enhancing enzymatic activities of peroxidases (POD), sucrose phosphate synthases, and sucrose synthases under salinity stress in rice plants (Huang et al. 2020). Similarly, an increase in activities of NR and GS, accompanied by an upsurge in NR-dependent NO production and stimulation of GDH activity upon GABA application was reported in Agrostis stolonifera (creeping bentgrass) (Tang et al. 2020) suggesting that enzymes involved in nitrogen metabolism directly influence NO production. Additionally, NO and nitrogen metabolism are simultaneously interrelated to the accumulation of osmolytes in plants, an increase in proline, total soluble sugar, and chlorophyll content together with an increase in enzymatic action of NR and NiR was observed subsequent to molybdenum application in arsenicstressed wheat seedlings which were reversed upon application of 100 μM NO inhibitor cPTIO, suggesting NO-mediated arsenic stress alleviation via regulation of ROS accumulation (Alamri et al. 2022). Similarly, SNP supplementation (100 and 150 μM) strengthened the elimination of ROS, enhanced proline and glycine betaine content by 31.85 and 15.81% as compared to the control, increased N uptake, improved RWC and antioxidant defense in Solanum melongena (eggplant) subjected to nickel stress (Soliman et al. 2019). Consequently, under NaCl-induced salinity stress (100 mM) in Cicer arietinum (chickpea), treatment with 50 μM S-nitroso-N-acetylpenicillamine (SNAP) exhibited a similar increment in the contents of proline, glycine betaine, and total soluble sugars (Ahmad et al. 2016) and supplementation with 15 mg L−1 of nano-titanium dioxide (nTiO2 ) to Vicia faba (fava bean) under drought stress, elicited NR-mediated NO biosynthesis which enhanced the enzymatic and non-enzymatic defense system of the stressed plants, suppressed the formation of H2 O2 and O2 − content, leakage of electrolytes, lipid peroxidation attributing to a rapid increase in the accumulation of compatible solutes such as proline, glycine betaine which increased the hydration levels of the plants (Khan et al. 2020). Polyamines form a major sink of nitrogen metabolism while its catabolism leads to the generation of GABA, a

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recent report denoted that treatment of tea roots with NO donor, enhanced tolerance of the plant to chilling stress via up-regulating enzymatic action of arginine decarboxylase, ornithine decarboxylase, glutamate decarboxylase, GABA transaminase, and 1-pyrroline-5-carboxylate synthetase suggesting enhanced levels of polyamines, proline and an acceleration in consumption of GABA (Wang et al. 2020). Conversely, treatment with polyamines in plants has often been correlated with the regulation of ROS and NO homeostasis, for instance in tobacco plants, 10 μM and 50 μM of putrescine, spermidine, and spermine were effective in enhancing pollen germination via regulating ROS and NO levels, similarly, application of putrescine, spermine, and spermidine in Arabidopsis induced stomatal closure via enhancing NO levels (Agrula et al. 2018). Contemporary reports reveal that NO-mediated osmolyte accumulation in plants is effective in mitigating ROS-induced oxidative damage, moreover, the correlation between N assimilation and proline, glutamate, and polyamine levels has also been assessed in the presence of NO (Liu et al. 2022a). Table 1 shows the NO-intervened responses in plants to overcome abiotic stress situations.

6 Conclusion and Future Prospects Accumulating research has provided several shreds of evidence regarding the negative impacts portrayed by various abiotic stresses on crop growth and productivity. Abiotic stresses are estimated to be the major contributor to the generation of ROS and are considered an unavoidable by-product of aerobic metabolism in plants. Overproduction of ROS causes extensive damage to lipids, proteins, and DNA disturbing the overall cellular homeostasis that cause serious oxidative harm and ultimately leads to the death of plants. ROS works according to its concentration, if it is produced in excessive amounts, it creates a toxic environment in cell and therefore fabricate deleterious effects in plants and limit the crop yield expansively. However, with evolution plants have inculcated several defense measures that include modifications at the morphological, metabolic, and genetic levels which help the plants to adapt better under adverse climate fluctuations. One most significantly sound defense strategy involves the use of a crucial gaseous, bioactive signaling molecule nitric oxide (NO), which is well-known to confer resistance against abiotic stressors. NO has cytoprotective properties which are attributed to it by upregulating the antioxidant defense system, stimulating the process of sulfur-assimilation, escalating the ascorbate–glutathione cycle, enhancing the production of osmolytes, and interacting with nitrogen metabolism for its synthesis. Further, significant knowledge regarding NO-mediated metabolic processes will give a better understanding of its mode of action and its working in plants. Apart from that, proteomic and genomic approaches will highlight NO interaction with other genes, molecules, proteins and will influence the overall functioning in plants that could help in the production of climate-resistant plants. Also, investigation at the molecular level on these aspects will explain how several stress-related genes interplay with NO to amend how NO

The enzymatic activity of CAT, guaiacol Khator and Shekhawat (2019) peroxidase, and nitrate reductase was enhanced by treatment with NO whereas APX activity was downregulated which resulted in overall detoxifying the negative consequences of salt stress which helps to maintain stable cellular homeostasis Application of SNP increased in the Piacentini et al. (2020) levels of intracellular NO in roots alleviate cadmium (Cd) stress like it inhibited later root formation, limit the elongation of the adventitious root, reduce lignin content of roots, lowered Cd uptake, and reduce ROS as NO reacts with ROS to form peroxynitrite

SNP, 100 μM (Exogenous)

SNP, 50 μM (Exogenous and Endogenous)

Indian mustard (Brassica juncea)

Rice (Oryza sativa)

(continued)

Pre-treatment of quinoa seeds with SNP, Hajihashemi et al. (2020) H2 O2 , and CaCl2 aims to mitigate salt stress by promoting germination rate, and germination index, reducing the amount of α-amylase and β amylase in seeds along with increasing the protein and amino acid content of seeds

Li et al. (2018)

SNP (0, 0.1 and 0.2 mM) (Pre-treatment of seedlings) (Exogenous)

References

Quinoa (Chenopodium quinoa)

NO lowers H2 O2 and MDA levels inhibit electrolyte leakage and activate SOD and POD enzyme activities which resulted in higher photosynthetic rate and yield under ozone pollution

SNP, 200 mM (Foliar application) (Exogenous)

Wheat (Triticum aestivum)

Responses

NO (donor and concentration)

Crops

Table 1 NO-intervened responses in crops to detoxify ROS and maintain stable cellular homeostasis

128 T. Seth et al.

Treatment of maize seedlings with SNP and sodium hydrosulfide (NaHS; H2 S donor) improved the endogenous levels of both the signaling molecules that aid in the reduction of oxidative stress by suppression of lipoxygenase activity, reducing methylglyoxal activity, and overall inducing the antioxidant system to strengthen the integrity of membrane against chromium (Cr)-induced stress

SNP resulted in a significant reduction in Gautam et al. (2021) temperature stress as it enhances photosynthetic-NUE and SUE, Rubisco, and PSII activity, promotes GSH activity and activates enzymes of the ascorbate–glutathione cycle to inhibit the ROS content to hinder oxidative damage

SNP, 500 μM (Pre-treatment on seedlings) (Exogenous)

SNP, 100 μM (Foliar application) (Exogenous)

Maize (Zea mays)

Rice (Oryza sativa)

(continued)

Kharbech et al. (2020)

SNP helps in limiting lipid peroxidation, Alp et al. (2022) reducing H2 O2 levels, enhancing chlorophyll content, lower guaiacol peroxidase, and SOD activity. The proteomic analysis showed NO role in the regulation of metabolic processes like carbohydrate metabolism, protein metabolism, energy metabolism, stress defense, and signal transduction

SNP, 100 μM (Exogenous)

Barley (Hordeum valgare)

References

Responses

NO (donor and concentration)

Crops

Table 1 (continued)

Nitric Oxide and Cellular Redox Homeostasis in Plants 129

Combined application of arsenic Praveen et al. (2019) (AsIII;150 μM) and SNP resulted in inhibition of As accumulation, improved chlorophyll, protein, and mineral content by detoxification of ROS, reduction in N-metabolism, inducing the expression of auxin transporter (PIN) genes which facilitate improvement in crop productivity by alleviation of arsenic (As) stress in mustard seedlings Treatment of seeds with NO and SPM Basit et al. (2022) (0.01 mM) is known to relieve the chromium (Cr)-induced stress in rice by lowering Cr levels, increasing photosynthetic pigments, and germination indices, maintaining nutrient balance, increasing total soluble sugar along with impeding the amount of O2 .− , H2 O2 , and MDA in roots and leaves which helps to minimize the toxic effects of Cr stress

SNP, 100 μM (Exogenous)

SNP, 100 μM (Seed priming) (Exogenous)

Indian mustard (Brassica juncea)

Rice (Oryza sativa)

References

Responses

NO (donor and concentration)

Crops

Table 1 (continued)

(continued)

130 T. Seth et al.

Improved fresh weight, shoot and root elongation and decreased EL and MDA, elevated AsA-GSH cycle, regulated Na+ /K+ homeostasis under salt stress

Reduced high temperature induced Gautam et al. (2021) H2 O2 and TBARS content and improved accumulation of proline and activity of AsA-GSH cycle

SNP (30–70 μM) (Exogenous)

SNP (100 μM)

Nitraria tangutorum

Rice (Oryza sativa)

Gao et al. (2022)

(continued)

Under salinity stress, up-regulated AsA-GSH cycle, activity of antioxidant enzymes including SOD, CAT, APX, DHAR, and GR, and synthesis of proline, GB, and sugars

SNP (100 μM), SA (1 mM) (Exogenous)

Adzuki beans (Vigna angularis)

Ahanger et al. (2019)

Both male and female seedlings T. Liu et al. (2022a, b, c) grandis were exposed to salinity stress (100 mM NaCl) and later treated with SNP to understand the role of gender differences between the two and how they are regulated by NO. The female plants showed better tolerance due to higher photochemical activities of PSII, enhancement in pigment content, improved RWC along with an increase in NO content whereas male plants mitigated salt stress by limiting lipid peroxidation, augmenting antioxidant enzymes, and enhanced GSH and proline accumulation

SNP, 0.05 Mm (Exogenous)

Chinese nutmeg yew (Torreya grandis)

References

Responses

NO (donor and concentration)

Crops

Table 1 (continued)

Nitric Oxide and Cellular Redox Homeostasis in Plants 131

Under chromium (Cr) toxicity, enhanced Kushwaha et al. (2020) contents and redox couple of AsA and GSH, sequestered chromium into vacuoles, stimulated phytochelatins Enhanced sucrose and proline levels, which reduced H2 O2 and MDA by 34% and 54%, respectively, improved photosynthetic rate, stomatal conductance, intercellular CO2 concentration, transpiration rate, and uptake of Zn, Fe, B, K, Ca and Mg Enhanced proline content by 113.3%, GB content by 56.2%, trehalose content by 90%, total soluble sugar content by 40.2%, up-regulation SOD, CAT, APX, GR, and APX and GR in heat-stressed plants Established osmotic adjustments and antioxidant adjustments increased chlorophyll synthesis, total phenol content, and activity of glyoxalase I and II under copper phytotoxicity

(SNP, 50 μM)

(SNP,150 μM) Foliar application (Exogenous)

(SNP and ABA 100 μM each) (Exogenous)

SNP 50 μM and Acetyl SA 100 μM

Tomato (Solanum lycopersicum)

Pepper (Capsicum annuum)

Wheat (Triticum aestivum)

Mung bean (Vigna radiata)

(continued)

Abdulmajeed et al. (2021)

Iqbal et al. (2022)

Shams et al. (2019)

Iqbal et al. (2021)

Suppressed glucose-mediated photosynthetic inhibition by elevating AsA-GSH metabolism and activity of SOD, CAT, GPX, which ameliorated oxidative damage caused by heat stress and lowered H2 O2 and TBARS content

SNP (100 μM), NaHS (200 μM) (Exogenous)

Wheat (Triticum aestivum)

References

Responses

NO (donor and concentration)

Crops

Table 1 (continued)

132 T. Seth et al.

PSKα stimulated endogenous biosynthesis of NO by inducing NOS activity and increased the contents of PUT, SPD, SPM by up-regulating activities of ADC, and ODC to ameliorate chilling injury

150 nM PSKα induced NO biosynthesis (Endogenous)

(Endogenous NO)

Banana (Musa)

Rice (Oryza sativa) Enhanced gene expression of AMT1:1 and AMT1:2, increased the activity of GDH, enhanced N content in leaves, improved osmotic regulation and ROS scavenging by enhancing enzymatic activities of POD, SPS, and SS under salinity stress

Responses

NO (donor and concentration)

Crops

Table 1 (continued)

Huang et al. (2020)

Wang et al. (2022)

References

Nitric Oxide and Cellular Redox Homeostasis in Plants 133

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regulates growth and development in plants under inevitable environmental cues. Methods for determining precise quantities of NO produced in different locations and at different time intervals must be accurate, quick, and efficient to comprehend this multi-functional molecule and its targets to scavenge excessive ROS from the cell environment. Post-translational modifications are crucial to be investigated as they will provide insights regarding NO influencing cellular processes and initiating cross-tolerance in plants. Therefore, there are enormous challenges related to NO in maintaining cellular homeostasis in plants and a rich area persists for future exploration.

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The Function of Hydrogen Sulfide in Plant Responses to Salinity and Drought: New Insights Harsha Gautam, Sheen Khan, Ameena Fatima Alvi, and Nafees A. Khan

Abstract Abiotic stresses are major concerns for agriculture all over the world as they can reduce crop production and quality, as well as agricultural sustainability. Salinity promotes plant toxicity, which slows down the entire growth and development of crop plants. Drought stress affects yield through altering critical plant metabolic processes, accounting for over 70% of potential crop yield and productivity losses globally. Approaching crop plants for more rapid and effective activation of defense mechanisms provides a technique of effectively mitigating the severe implications generated by such extreme environmental conditions. Recently, it has been discovered that hydrogen sulfide (H2 S) is a key priming factor regulating a variety of physiological processes involved in plant growth and development. H2 S has enormous agricultural potential and participates in abiotic stress response against salinity and drought. We give a brief description of recent literature on H2 S sources, biosynthesis, and regulation inside the plant cell in this chapter. Additionally, the role of H2 S in enhancing plant tolerance to salinity and drought is emphasized. The main effects of H2 S on plants have been discussed, including how they affect photosynthesis, the antioxidant defense system, and plant productivity in water-scarce and salinity conditions. We reviewed the roles and underlying mechanisms of H2 S-mediated modulation of salinity and drought stress in this chapter.

1 Introduction Abiotic stress, such as exposure to salinity, drought, extreme temperatures, and heavy metals is typically brought on by changes in environmental factors. Plants are naturally sessile, which makes them susceptible to a variety of abiotic stresses. About 20% of irrigated land worldwide suffers from soil salinity, which significantly lowers H. Gautam (B) · S. Khan · A. F. Alvi · N. A. Khan (B) Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh 202002, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_8

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crop yields (Qadir et al. 2014). Poor irrigation techniques, climate change, and deterioration of the natural environment all contribute to problems with soil salinity (Park et al. 2016; Ziska et al. 2012). Salinity is a condition caused by a high concentration of soluble salts, and soil is regarded to be saline when the ECe value is 4 dS/m−1 or higher. Salts in the soil that are concentrated in high levels make it difficult for roots to access water, and salts in plants that are concentrated in high levels can be toxic. Direct effects of salt on cell growth and expansion are seen in plant roots. Salt concentrations that are toxic build up gradually before affecting the plant (Munns and Tester 2008). It lowers water potential, results in ion imbalance, disturbances in ion homeostasis, and increases toxicity; this altered water status causes a reduction in initial growth and a restriction on plant productivity. All the major processes, including germination, growth, photosynthetic pigments and photosynthesis, water relation, nutrient imbalance, oxidative stress, and yield are influenced by salt stress. The negative impact of salt stress is seen as plant death or a decline in productivity (Parihar et al. 2015). Drought is the greatest risk to global food security due to the scarcity of water resources. The previous major famines were triggered by it. Due to the limited water supply in the world, demands from a fast expanding population are anticipated to make drought conditions worsen in the future (Somerville and Briscoe 2001). Water is a key component of many physiological processes, including many aspects of plant growth, development, and metabolism, makes up about 80–95% of the fresh biomass of the plant body. A variety of plant responses are triggered by drought (Shakeel et al. 2011). Changes in the architecture of the individual plants, affects plant growth, resulting in changed reproductive cycles, reduced fruit production, decreased height, and altered leaf size and number. Drought stress exposure may cause changes in photo-biological processes and restrict the amount of carbon dioxide that may enter the plant through the stomata. The effectiveness of photosynthesis is compromised by the loss of water vapor, restrictions on non-stomatal components, damage to the reaction centers of photosystems I and II (Angelopoulos et al. 1996). The level of drought stress has a linear relationship with the formation of reactive oxygen species, which increases the peroxidation of membrane lipids and the breakdown of nucleic acids as well as structural and functional proteins. Reactive oxygen species created under drought stress are located in a number of organelles, including chloroplasts, mitochondria, and peroxisomes. These organelles are also their primary targets (Farooq et al. 2009). In comparison to a wheat genotype that was more vulnerable to drought, the drought-tolerant wheat genotype had higher ascorbate peroxidase (APX) and catalase (CAT) activity, higher ascorbate content, and lower levels of hydrogen peroxide (H2 O2 ) and malondialdehyde (MDA) (Sairam et al. 1998). Drought causes plants to produce more abscisic acid (ABA), a phytohormone, either at the root or leaf level. This causes stomatal closure and lower transpiration losses, which in turn triggers the expression of several genes related to drought, including up- and down-regulation of many gene transcripts (Bashir et al. 2021).

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Most commonly, hydrogen sulfide (H2 S) has been described as a hazardous gas and environmental risk. But in the last ten years, it has become a new gaseous signaling molecule that is as significant as other signaling molecules in animal and plant cells (Garc´ıa-Mata and Lamattina 2010; Kimura 2014). H2 S has been demonstrated to play crucial roles in a variety of activities of the life cycle of plants such as plant growth, development, and biotic and abiotic stress responses, in contrast to its activity as a phytotoxin at high concentrations (Gautam et al. 2022; Sehar et al. 2022). Furthermore, H2 S has been shown to have protective effects against a variety of abiotic stresses, including osmotic stress, metal stress, drought, salt, and high temperatures (Wang et al. 2010; Li et al. 2012; Shen et al. 2013; Shi et al. 2013; Fang et al. 2016). However, plants were also shown to produce H2 S, and because their physiological effects are comparable to those of nitric oxide (NO), a potential crosstalk with NO has been suggested (Kolluru et al. 2015). According to Li et al. (2021), H2 S reduced the effects of salinity stress via controlling the expression of microRNAs by altering the root architecture of Malus hupehensis. Plants ability to withstand heat was influenced by H2 S, and wheat seedlings pretreatment with sodium hydrosulfide (NaHS), an H2 S donor, reduced oxidative stress by enhancing the activity and gene expression of antioxidant enzymes (Min et al. 2016). H2 S increases chloroplast biogenesis in Spinacia oleracea seedlings to enhance photosynthesis, the expression of photosynthetic enzymes, and thiol redox modification (Chen et al. 2011).

2 H2 S: Source and Synthesis in Plants H2 S is a gas that is poisonous, combustible, corrosive, and colourless (Vikrant et al. 2018). Recent discoveries in the fields of biology and medicine have demonstrated that H2 S controls a wide range of physiological processes, including neurotransmission, anti-inflammation, and blood pressure (Vikrant et al. 2018). Since 1975, when it was only recognized as a factor in plant growth and development, its endogenous production in plants as a signalling molecule and its direct and indirect roles in stress tolerance and protection against diseases have been recognized (Ahmed et al. 2021). H2 S is released in the environment from both anthropogenic and natural sources (Ahmed et al. 2021). Anthropogenic activities include the burning of oil, petroleum, catalytic inverters of cars, in addition, wastewater treatment plant, natural gas processing plants, geothermal industries, anaerobic digestion plants, and agricultural activities also produce H2 S (Ahmed et al. 2021; Kailasa et al. 2020; Vikrant et al. 2018). Among natural sources, volcanoes are considered a primary source of H2 S (Ahmed et al. 2021). Additionally, it releases from coastal sediments, anoxic soils, groundwater, and marshes and as a by-product of the sulfite metabolism in some plants (Kailasa et al. 2020). Hydrogen sulfide (H2 S) is a gaseous secondary signalling molecule, which involves various physiological and developmental responses of plants. Various reports shows the application of H2 S plays a crucial role in alleviating abiotic stresses like salinity, drought, high temperature, and heavy metal stress (Huang et al. 2021).

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It is a small, lipophilic molecule that can easily navigate through a simple diffusion process and thus does not require any transporter. Endogenous synthesis of H2 S in plants primarily takes place in the chloroplast and partly in mitochondria, and cytosol Aroca et al. (2018) also, H2 S production in Arabidopsis peroxisomes was recently demonstrated by Corpas et al. (2019), although it is unknown whether synthesis mechanism is endogenous or derived from other organelles. Multiple enzyme systems contribute significantly to the biosynthesis of H2 S in plants. Figure 1 depicts the H2 S biosynthesis pathway. In the cytosol, H2 S synthesis occurs by the activity of L-cysteine desulfhydrase (LCD), L-cysteine desulfahydrase 1 (DES1), D-cysteine desulfahydrase 1/2 (DCD) (Fig. 1). Out of them, the most common enzymes in plants are LCD and DES1 which catalyzes L-cysteine into H2 S accompanied by the formation of pyruvate and ammonia (Liu et al. 2021). Similarly, DCD catalyzes H2 S production using D-cysteine (Riemenschneider et al. 2005). Pyridoxal phosphate (PLP) is used as a cofactor in this reaction (Shivaraj et al. 2020; Liu et al. 2021). Higher plants use the enzyme β-cyanoalanine synthase (CAS), which is pyridoxal phosphate dependent, to catalyse the reaction between L-cysteine and HCN to produce H2 S and β-cyanoalanine in the mitochondria to detoxify cyanide (Hatzfeld et al. 2000). Three genes CYS-C1, CYS-D1 and CYS-D2, encode CAS in Arabidopsis. Thus, it confirms, that CAS catalyzed H2 S generation from L-cysteine and HCN (Jost et al. 2000). Yamaguchi et al. (2000) found that during β-cyanoalanine synthesis enzyme cyanoalanine synthase cI (CAS-CI) also generates hydrogen sulfide in the mitochondria. Due to the chloroplastic localization of sulfite reductase (SiR), which catalyzes the conversion of SO4 2− to H2 S during the sulfate absorption route, the chloroplast serves as the major sulfide production source among the other plant cellular organelles (Arif et al. 2021). To catalyze this reaction SO4 2− (from soil or SO2 from the atmosphere) is first activated by the enzyme ATP sulfurylase (ATPS) through the adenylation process to form adenosine 5' phosphosulfate (APS). The APS is reduced to sulfite (SO3 2− ) by the APS reductase (APR) enzyme present in the plastid. Sulfite is further reduced by ferredoxin-dependent (SiR) enzyme to H2 S (Ahmed et al. 2021) Furthermore, OAS-TL (O-acetylserine thiol lyase/ also known as cysteine synthase) catalyses the conversion of H2 S and O-acetyl serine (OAS) to cysteine, the reversal of this reaction produce H2 S (Li 2015). Also, AtNFS1 and AtNFS2 genes encode nitrogenase Fe-S cluster (Nifs) like protein cysteine desulfurases, required for catalysis of cysteine to form H2 S (Léon et al. 2002). These enzymes are consequently engaged in regulating the synthesis of H2 S throughout distinct cellular compartments of the plant due to their variable expression. Exogenous application of H2 S donors increases the endogenous H2 S content in plants (Li et al. 2013; Huang et al. 2021). Many H2 S donors are identified and synthesized for research studies, for instance sodium hydrosulfide (NaHS), morpholin-4-ium 4-methoxyphenyl phosphinodithioate (GYY4137), diallyl trisulfide (DATS), NOSH-aspirin etc. Among them, NaHS and GYY4137 is used widely in plant research, because they maintain equilibrium between H2 S, HS− and S2− ions immediately after dissolving in water (Huang et al. 2021).

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Fig. 1 Biosynthesis pathway of H2 S in plant cell: CAS (β-cyanoalanine synthase), OAS-TL (Oacetylserine thiol lyase/also known as cysteine synthase), DCD 1/2 (D-cysteine desulfahydrase 1/2), LCD (L-cysteine desulfhydrase), DES (L-cysteine desulfahydrase 1)

3 Impacts of Salinity and Drought on Plants Plant kingdom through photosynthesis supports all the life-forms on earth. Notwithstanding the responsibility, plants have to undergo range of fluctuations in their surroundings. Shortage of water availability, salinity, excess light, high/low temperatures and nutrient deficiencies are some of the extremes that lead to impairment of plant performance (Verslues et al. 2006). Amongst these limiting abiotic factors, drought (or water deficit) stress is extensively studied given that it is likely the main constraint for crop productivity in many arid and semi-arid areas worldwide. About 80–95% of the fresh biomass of the plant body is comprised of water, which plays a vital role in various physiological processes including many aspects of plant growth, development, and metabolism (Brodersen et al. 2019; Abbasi and Abbasi 2010). Water deficit in plants shows visible symptoms when there is imbalance between water transpired and water uptake by roots. These imbalances are major consequences of inadequate precipitation, decreased ground water level or the retention of water by soil particles (Lambers et al. 2008; Salehi-Lisar and Bakhshayeshan 2016). The other major abiotic stress recovered is salinity stress. It is also equally hampering crop quality and yield. According to Szabolcs there are two types of soil responsible for salt stress. Saline soils—the soluble salts are chiefly NaCl and Na2 SO4 and sometimes also contain appreciable quantities of Cl− and SO4− of Ca2+

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and Mg2+ and sodic soils—these soils contain Na+ salts capable of alkaline hydrolysis, mainly Na2 CO3 . During drought as well as salinity rhizospheric zones are negatively affected which in turn reduces growth and productivity through creating an imbalance in the cytoplasmic ion homeostasis and thereby impacting metabolic dysfunction and other major biochemical and physiological processes (Khanna et al. 2021; Chokshi et al. 2017). Here are the list of parameters drastically affected by drought and salinity in plants.

4 Seed Germination Seed germination governs plant growth and survival. However, salinity and drought stress have been found to be detrimental to seed germination in plethora of plant species. The prominent changes in growth parameters are recorded in plant like maize, sorghum, rice, neptune grass, wheat in case of drought as well as salt exposure (Queiroz et al. 2019; Sengupta and Majumder 2009; Fernández-Torquemada and Sánchez-Lizaso 2013; Akbarimoghaddam et al. 2011). The stress drastically hamper morphological and physiological characteristic during seed germination and seedling development. These stresses reduce the process of imbibition due to reduction in osmotic potential. The water deficit and salinity tend to increase cell toxicity which leads to enzymes denaturation, nucleic acid damage, imbalance in protein and nutrient metabolism (Brito et al. 2019; Dantas et al. 2007). Reduced germination rate index, percentage germination, seedling vigor index, radical and plumule length, root and shoot dry mass are some of the growth indicators negatively regulated under salinity and drought stress. The extent of damage in seeds also depends upon the stress duration and salt concentration.

5 Plant Growth Plants need optimal temperature, water and mineral availability for profuse development and crop yield. Drought and salinity exposed plants experience water or osmotic deficit due to reduced soil moisture and imbalance to the transpiration streams (Munns 1993, 2005). In Lathyrus sativus shoot or stem length is comparatively reduced under drought stress. Moreover, water deficit equally hits leaves and root system in plants. In order to overcome the water loss, plants acquire stronger root architecture by increasing root length, root hair elongation, spread, and lateral root development. The outcome is visibly reported in many plants like Crocus sativus (Maleki et al. 2011). The altered root system like this helps in soil water retention, nutrient accumulation, plant biomass production and better symbiotic association in legumes (Smith and De Smet 2012). Under drought stress the plant root to shoot system improves but it substantially reduces plant biomass (Akhtar and Nazir 2013). Reduction in leaf area, lower turgor pressure, stomatal closure and premature leaf senescence

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are common symptoms in drought exposed plants (Deka et al. 2018; Farooq et al. 2009). Likewise under salinity stress, plant experiences reduction plant height, tiller numbers, leaf area index in case of rice (Hasanuzzaman et al. 2009). Na+ and Cl− ion toxicity causes reduction in plant height and diameter in Suesda salsa and Glycine max. In case of Foeniculum vulgare, growth parameters including plant height, fresh weight, yield, and biomass were affected significantly by irrigation water salinities at 0.01 probability levels (Semiz et al. 2012).

6 Photosynthesis The suppression in photosynthetic activity in presence of drought and salinity are due to reduced leaf area, stomatal closure, and reduced water potential (Zare et al. 2011; Bhargava and Sawant 2013; Zhang et al. 2005). Declined activity of photosynthesis is triggered by the loss of CO2 Deepak et al. (2019) uptake, whose drop has been shown to affect Rubisco activity and decrease the function of nitrate reductase and sucrose phosphate synthase and the ability for ribulose bisphosphate (RuBP) production. Reduction in photosynthetic pigments like chlorophyll a and b, carotenoids and xanthophylls have been reported Vigna radiata (Saha et al. 2010). The fall in chlorophyll content has been reported in soybean and O. sativa (Chutipaijit et al. 2011; Chowdhury et al. 2017). The decline in pigment levels, has led to 16% loss of the intensity of chlorophyll fluorescence on average (Mane et al. 2010). Decrease in the efficiency of PSII, electron transport chain (ETC), and assimilation rate of CO2 under the influence of salinity and drought has been noticed (Piotr and Grazyna 2005). The other factor that causes reduced photosynthesis are dehydration of cell membranes which reduce their permeability to carbon dioxide, salt toxicity, enhanced senescence, changes in enzyme activity induced by alterations in cytoplasmic structure, and negative feedback by reduced sink activity (Iyengar and Reddy 1996).

7 Mineral Nutrition Drought situation results in reduced soil nutrient accessibility, root translocation, ion imbalance in various plant tissues. Potassium (K), Nitrogen (N) and Phosphorus (P) are the prominent mineral deficiency reported under drought stress. Genes encoding K transporters were inhibited by water deficit (Li et al. 2009) and inner K channels are stimulated by a protein kinase, CIPK23, which in turn cooperates with calcineurin B-like calcium sensors. This K channel was inhibited in roots but activated in leaves of grapevine (Cuéllar et al. 2010). Reduction in N was considered as the main responsible factor for photosynthesis decline and leaf senescence (Da Silva et al. 2011). There was a significant reduction in leaf P amount in Ocimum gratissimum (Osuagwu et al. 2010). Drought-stress conditions increased the accumulation of manganese (Mn), molybdenum (Mo), P, K, copper (Cu), calcium (Ca) and zinc

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(Zn) in soybean (Samarah et al. 2014). The relationship between mineral nutrition and salinity is bit complex as compare to drought. The availability of nutrient in saline soil depends upon soil pH, redox potential of the soil, mineral solubility in soil, and the nature of binding site on the organic and inorganic particle surface all the results in competitive uptake, improper distributions and transport in the plant tissues. Under salinity conditions the NO3 – has to compete with Cl– reducing water uptake, growth and yield of the plant (Rozeff 1995) and low phosphate content is reported in pants growing under saline conditions. As per recent studies an imbalance in K, Ca and Mg has been reported in response to NaCl salinity (Hussin et al. 2013).

8 Oxidative Stress With the onset of drought and salinity, generation of reactive oxygen species (ROS) is a common phenomenon. The presence of ROS proves detrimental to plant tissues in terms of membrane damage, protein degradation, lipid peroxidation, DNA damage and many more. There are many instances reported where lipid peroxidation, H2 O2 content, superoxide generation are considerably higher under stressful conditions than control. In order to maintain cellular homeostasis and minimize cell damage plant adopts efficient antioxidant defense system which could be enzymatic or non-enzymatic detoxification moieties. These strategies helps in ROS scavenging, decrease in electrolyte leakage and lipid peroxidation thereby maintaining vitality and integrity of organelles and cell membrane (Gharibi et al. 2016). Both enzymatic (SOD, CAT and APX) and non-enzymatic (ascorbic acid, reduced glutathione and tocopherol) antioxidants are involved in drought as well as salinity stress responses such as in Vicia faba Abid et al. (2017), Vigna mungo Gurumurthy et al. (2019) and in many crops like tomato, citrus, pea etc. (Mittova et al. 2004; Ahmad et al. 2009, 2010).

9 H2 S: A Crucial Component in Plant Salinity Responses High accumulation of Na+ , Cl− , HCO3 − , CO3 − and SO4 2− ions in soil exert salinity stress on plants, affecting their normal growth and development (Jahan et al. 2021). One of the major consequences of salinity is osmotic imbalance affecting water absorption ability by roots, generating hyper-osmotic conditions (Riyazuddin et al. 2020). Salinity stress causes excessive accumulation of ROS, causing oxidation of proteins, membranes, and DNA (Fichman et al. 2019; Jahan et al. 2021). Through the opening of the outward rectifying potassium (K+ ) channels and the consequent loss of K+ , salt stress results in membrane depolarization, affecting the ionic balance of the plant (Jahan et al. 2021). By degrading chlorophyll content, and reducing stomatal conductance, PSII activity, and Rubisco activity, it affects the overall photosynthesis and growth of the plant (Sehar et al. 2021; Jahan et al. 2021). To alleviate the negative

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outcome of salinity, plants develop many mechanisms, such as compartmentalization (ion-homeostasis), accumulation of compatible solute (proline, glycine betaine), and enhancing antioxidant defense system (reducing oxidative stress) (Goyal et al. 2021). By maintaining the Na+ /K+ ratio, producing osmolytes, and protecting the photosynthetic apparatus, evidence suggests that the application of H2 S aids in reducing salinity (Goyal et al. 2021). It has been observed that salt-induced oxidative stress is relieved by H2 S by enhancing the activity of enzymatic antioxidants SOD, POD, CAT, and non-enzymatic antioxidants glutathione, in many plants such as Malus hupehensis (Wei et al. 2019), eggplant and tomato seedlings (Raju and Prasad 2021), (Da Silva et al. 2017, Capsicum annum (Kaya et al. 2020), Oryza sativa (Wei et al. 2021) under salinity stress. It has been recorded that NaHS (H2 S donor) application to Triticum aestivum enhances the AsA-GSH cycle enzyme gene expression (TaDHAR and TaGS), transcription factor TaDREB2, MAPK pathway (TaMPK4) (Ding et al. 2019). Oxidative and nitrification stress in strawberry (Fragaria × ananassa) plants is minimized by exogenous H2 S application under salt or osmotic stress by preserving the high redox state of ascorbic acid and glutathione (Christou et al. 2013). The activity of CAT, APX, and POD has been reported to be regulated by the per-sulfidation mediated by H2 S, supporting the response to oxidative stress (Li et al. 2020). On the other hand, salt also stimulates endogenous H2 S synthesis, which improves the antioxidant system and controls ROS (Srivastava et al. 2022). Exogenous H2 S reduced growth inhibition by increasing Na+ secretion and decreasing its absorption through the regulation of NSCCs (non-selective cation channels) and SOS1 (salt overly sensitive 1) pathways in T. aestivum (Deng et al. 2016). However, a report on Medicago sativa shows that H2 S maintains the content of the K+ in roots and have no discernible impact on the Na+ ion content, thus preventing NaCl-induced K+ -efflux and alleviating salinity effects (Lai et al. 2014). In a study on Hordeum vulgare, H2 S has been reported to maintain the Na+ /K+ ratio by improving the expression of K+ channels, maintaining Na+ ion by increasing the transcriptional level of Na+ /H+ antiporter and H+ -ATPase (Chen et al. 2015). Similar results are found in Arabidopsis thaliana NaHS application regulates the Na+ /H+ antiporter system in an H2 O2 -dependent manner and maintains ion homeostasis, thus enhancing salinity tolerance (Li et al. 2014). Proteomics investigation of NaHS (H2 S donor) treated O. sativa under salt stress recovered and regulated the genes for the light reaction proteins, Calvin cycle, and chlorophyll biosynthesis. Also, cell structure-related proteins are up-regulated by H2 S in rice under salt stress, thus repairing photosynthetic activity, augmentation of primary energy metabolism, improvement of protein metabolism, and preservation of cell structure (Wei et al. 2021). Similar results are observed in a study by Chen et al. (2011) H2 S by stimulating chloroplast biosynthesis, promoting expression of the photosynthetic enzyme, and regulating the thiol-based redox system in Spinacia oleracea enhance the photosynthesis capacity of plants. Exogenous H2 S treatment on eggplant under salt stress mitigate the negative effect of salinity by improving gaseous exchange parameters, promoting the accumulation of proline and sugars, and enhancing antioxidant enzyme activity (Ekinci et al. 2021). H2 S regulates the stomatal aperture and density thus modulating gas exchange in cucumbers under salt

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stress. Also improve chlorophyll fluorescence and content, thus improving photosynthesis (Jiang et al. 2019). A number of investigations have revealed promising functions for H2 S in plant salinity tolerance can be found in (Table 1).

10 Role of H2 S in Overcoming Drought Drought stress exerts various detrimental effects on plants involving osmotic stress, oxidative stress damage to photosystems, loss of cell integrity many more. All these factors hamper overall growth and development of plant. H2 S, however, can help in diminishing these effects in number of ways and help in increase plant resilience. (Table 2) illustrates the role of H2 S in alleviating drought stress in plants. The drought induced water deficit and osmotic stress can be overcome by building up compatible low molecular weight osmoprotectants like soluble sugars, sugar alcohol, proline and glycine betaine (GB) (Garc´ıa-Mata and Lamattina 2001; Rivero et al. 2014). These protectants vary significantly in their compositions well as component depending upon species. Higher seedling survival and lessened stomatal closure are caused by the exogenous application of H2 S in drought-stressed plants like Arabidopsis and Impatiens walleriana, which helps to prevent excessive water loss through stomatal closure (Garc´ıa-Mata and Lamattina 2010). Increased expression of drought associated genes DREB2A, DREB2B, CBF4 and RD29A are also reported (Jin et al. 2011). H2 S also helps in increasing relative water content and stomatal conductance. Upregulation of antioxidant enzymes is discovered in various species like Arabidopsis, Glycine max, and Triticum asetivum. H2 S can mediate the redox homeostasis by enhancing SOD, CAT and APX activity (Zhang et al. 2010a, b; Li et al. 2015; Shen et al. 2013). It also delayed excessive accumulation of MDA, H2 O2 and superoxide anion. The drought damage is seen to be controlled after H2 S application in Carthamus tinctorius in terms of reduced oxidative damage, increased secondary metabolites, and maintenance of ion homeostasis (Amir et al. 2020). H2 S can also lower down drought stress response through transcriptional regulation, mediating DNA methylation and increased ABA biosynthesis and activation of downstream drought related genes in Medicago sativa, Setaria italic and Oryza sativa respectively (Antoniou et al. 2020; Hao et al. 2020; Zhou et al. 2020). Drought stress causes damage to cell integrity, PSII, and water deficit within plant cells. Exogenous NaHS application reduces the content of MDA, lowers lipoxygenase activity to maintain the cell integrity; causes ABA-mediated stomatal closure to prevent water loss through transpiration and increases the turnover of D1 protein, and accelerates PSII repair cycle. Increased activity of antioxidant enzymes like SOD, CAT, and peroxidase, as well as polyamine, soluble sugar, and GB accumulation caused on by H2 S (Chen et al. 2016; Zhang et al. 2010a, b). These are basic drought stress adaptation primarily responsible for maintaining homeostasis in the stressed plants.

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Table 1 Examples of studies examining the role of hydrogen sulfide in the mechanism of response to salinity stress Plant species

H2 S NaCl Observed effects concentration concentration and donor and duration

Cynodon dactylon

500 μM NaHS

300 mM for 28 days

Alleviate the Shi et al. salinity-induced oxidative (2013) stress by modulating enzymatic and non-enzymatic antioxidant pool as well as increased the osmolytes accumulation (proline, sucrose, and soluble sugars)

Cucumis sativus

400 μM NaHS

100 mM for 48 h

Improve salt tolerance by adjusting the antioxidant system and amylase activity

Fragaria × ananassa cv. 100 μM Camarosa NaHS

100 mM for 7 days

reduced oxidative and Christou nitrosative cellular damage et al. (2013) via regulation of SOS pathway and improved antioxidant system

Medicago sativus

100 μM NaHS

100 mM for 4 days

Improved activity of SOD, Wang et al. POD, CAT, and APX thus (2012) reducing oxidative damage. K+ /Na+ ratio increased in roots

Arabidopsis thaliana

200 μM NaHS

100 mM for 48 h

Promote plant tolerance by Li et al. regulating the plasma (2014) membrane Na+ /H+ antiporter system to maintain ion homeostasis in an H2 O2 -dependent manner. In addition lowers the Na+ /K+ ratio

Medicago sativa

100 μM NaHS

175 mM for 24 h

Modulate the antioxidant defence system and maintain K+ /Na+ equilibrium to increase tolerance capacity

Zea mays

600 μM NaHS

100 mM for 48 h

Increased the activity of Shan et al. antioxidant enzymes APX, (2014) GR and reduced the ratio of AsA/DHA and GSH/GSSG

References

Yu et al. (2013)

Lai et al. (2014)

(continued)

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Table 1 (continued) Plant species

H2 S NaCl Observed effects concentration concentration and donor and duration

Hordeum vulgare

50 and 100 μM NaHS

Oryza sativa

50 μM NaHS 150 mM for 4 days

Salinity tolerance Mostofa increased by decreasing et al. (2015) Na+ /K+ ratio and reducing oxidative stress by improving level of glutathione, ascorbic acid and ROS and methylglyoxal-detoxifying enzymes

Triticum aestivum

1200 μM NaHS

Improve antioxidant defense system to reduce oxidative damage and maintain plasma membrane integrity

Triticum aestivum

50 μM NaHS 100 mM for 4 days

Through the regulation of Deng et al. NSCCs (non-selective (2016) cation channels) and SOS1 (salt overly sensitive 1) pathways, H2 S reduced growth inhibition by maintaining a lower Na+ content in seedlings during NaCl stress

Populus euphratica (salt resistant) P. popularis (salt-sensitive)

50 μM NaHS 100 mM for 24 h and 50 mM for 5 days

Maintain Na+ /K+ ratio by Zhao et al. improved regulation of the (2018) Na+ /H+ antiport system

Solanum lycopersicum

20 μM NaHS 100 mM

Enhanced antioxidant defense system protect plant from salinity

Da-Silva et al. (2018)

Malus hupehensis

50 μM NaHS 85 mM for 24, 48 and 72 h

Enhance tolerance via controlling the stability of the plasma membrane, the antioxidant defence system, and the H2 O2 formation

Wei et al. (2019)

150 mM for 48 h

160 mM for 48 h

Improve the K+ uptake by enhancing expression of potassium channel. Maintain the Na+ ion content by increasing transcriptional level of H+ -ATPase and Na+ /H+ antiporter

References

Chen et al. (2015)

Ye et al. (2015)

(continued)

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Table 1 (continued) Plant species

H2 S NaCl Observed effects concentration concentration and donor and duration

Triticum aestivum

50 μM NaHS 160 mM for 5 days

H2 S enhanced the Ding et al. expression of antioxidant (2019) enzymes, SOS and MAPK pathways

Capsicum annum

200 μM NaHS

100 mM for 3 weeks

Reduced the oxidative stress and increased salt tolerance in plants by regulating the levels of osmolytes, the AsA-GSH enzymes, and other associated enzymes

Kaya et al. (2020)

Oryza sativa

100 μM NaHS

100 mM for 3 days

Mitigate oxidative stress by improving antioxidant enzymes, restoration of photosynthetic activity, enhancement of primary and energy metabolism, strengthening of protein metabolism, and consolidation of cell structure

Wei et al. (2021)

Malus hupehensis

500 μM NaHS

150 mM

Reduce alkaline salt stress by modulating the expression of microRNAs

Li et al. (2021)

Fragaria × ananassa (Strawberry)

200 and 500 μM NaHS

15 and 30 mM for 50 days

Reduction in ROS by Bahmanbiglo improving antioxidant and Eshghi defense system and (2021) recovery of photosynthetic activity of plant

Solanum melongena and 40 μM NaHS 20 mM for S. lycopersicum 7 days

Modulate antioxidant activity and increase photosynthetic activity to help the plant adapt to stress

References

Raju and Prasad (2021)

11 Conclusion and Future Prospective The recent effects of climate change have made the problem of drought worsen globally. Agriculture experiences significant economic losses due to drought stress, and crop plants that are subjected to it generate low yields or even perish under extreme drought conditions. Plants growth and development are negatively impacted by salinity, but they have developed regulatory mechanisms that allow them to withstand these harmful conditions. It may be possible to create strategies to reduce the detrimental effects of salinity on crop yields and ultimately advance agricultural growth by identifying the salinity stress signaling pathway and describing the

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Table 2 Several representative studies on the role of hydrogen sulfide in regulating plant tolerance to drought stress Plant species

H2 S concentration and donor

Drought level and duration

Observed effect

References

Arabidopsis NaHS (80 μM) thaliana

Withholding Higher survival of seedlings, Jin et al. water for significant decrease in the size (2011) 14 days of stomatal aperture increased expression of drought associated genes such as DREB2A, DREB2B, CBF4, and RD29A

Carthamus tinctorius

NaHS (0.5 and 1.0 mM)

70 and 50% Diminished drought induced field oxidative damage due to capacity increased accumulation of secondary metabolites, strengthened antioxidant capacity and maintenance of ion homeostasis

Amir et al. (2020)

Fragaria ananassa

NaHS (100 μM)

10% (w/v) PEG-6000 for 7 days

Increased relative water content and stomatal conductance

Christou et al. (2013)

Glycine max

NaHS (50–100 μmol L–1 )

0, 7, 14, 21 days continuous drought with 80–0% humidity range

Higher SOD and CAT activities, lower lipoxygenase activity, delayed excessive accumulation of MDA, H2 O2 , and superoxide anion

Zhang et al. (2009)

Glycine max

NaHS (0.66 dose c.p. ha–1 )

100 and 50% water holding capacity

Up-regulation of antioxidant enzyme activity, accumulation of soluble sugars, free amino acids, and proline

Batista et al. (2020)

Helianthus annuus

NaHS (1.2 g ha–1 )

100 and Increased leaf water potential 30% of field and POD activity capacity

Impatiens walleriana

NaHS (500 μM)

Ipomea batatas

NaHS (800 μM)

Almeida et al. (2020)

Reduced water loss due to Garc´ıa-Mata induction of closure of stomata and Lamattina (2010) 15% PEG 6000 (w/v)

Increased activities of antioxidant enzymes and improved stability of cell membranes

Zhang et al. (2009)

(continued)

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Table 2 (continued) Plant species

H2 S concentration and donor

Drought level and duration

Medicago sativa

NOSH (100 μM)

Withholding Improved physiological watering for performance, reactive 6 days oxygen/nitrogen species homeostasis and transcriptional regulation of defense-related pathways

Antoniou et al. (2020)

Setaria italic

H2 S (50 μM)

30% PEG 8000

Hao et al. (2020)

Oryza sativa

NaHS (100 μM)

Withholding Maintenance of the redox water for balance via increased 10 days antioxidant capacity, increased ABA biosynthesis and activation of downstream drought-related genes

Spinacia oleracea

H2 S (250 ppb/380 μg m–3 )

Spinacia oleracea

NaHS (100 μM)

Withholding Increased water and osmotic water for potential of leaves, reduced 8 days MDA, increased levels of soluble sugars and PAs, up-regulation of genes such as choline monooxygenase (SoCMO), betaine aldehyde dehydrogenase (SoBADH), aquaporin (SoPIP1;2) as well as genes related to the biosynthesis of PAs and soluble sugars

Triticum aestivum

NaHS (200–1000 μM)

25% PEG for 48 h

Improved seed germination, Zhang et al. increased activities of amylase, (2010a, b) esterase, catalase, and ascorbate peroxidase; decreased lipoxygenase activity

Triticum aestivum

NaHS (1 mM)

15% (w/v) PEG for 24 hours

Increased activities of Shan et al. ascorbate peroxidase, (2011) glutathione reductase, dehydroascorbate reductase, γ-glutamylcysteine synthetase, higher contents of reduced ascorbic acid, reduced glutathione, total ascorbate, and total glutathione

Observed effect

H2 S signals improved osmotic stress tolerance by mediating DNA methylation

Increased glutathione accumulation

References

Zhou et al. (2020)

Kok et al. (1985) Chen et al. (2016)

(continued)

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Table 2 (continued) Plant species

H2 S concentration and donor

Drought level and duration

Observed effect

Triticum aestivum

NaHS (400 μM)

20% PEG 6000 (w/v) for 0–24 hours

Reduction in oxidative stress Li et al. by enhanced activities of SOD (2015) and CAT, acceleration of PSII repair cycle, increased turnover of D1 protein by enhancing D1 protein phosphorylation, degradation, and synthesis

Triticum aestivum

NaHS (500 μM)

20% PEG for 7 days

Enhanced antioxidant enzyme Ma et al. activities, decreased MDA and (2016) H2 O2 contents, increased ABA biosynthesis

Triticum aestivum

NaHS (400 μM)

20% PEG 6000 (w/v) for 24 hours or 3 days

Induction of ribosome biogenesis in eukaryotes, protein processing in endoplasmic reticulum, fatty acid degradation and cyanoamino acid metabolism under drought stress

Triticum aestivum

NaHS (300 μM)

10% PEG Up-regulation of ascorbate for 48 hours glutathione cycle

Shan et al. (2018)

Triticum aestivum

NaHS (100–500 μM)

25–30% of soil total moisture capacity

Decreased accumulation of H2 O2 and malondialdehyde in leaves, increased activities of SOD, CAT and POD, elevated concentration of proline, anthocyanins and flavonoids

Kolupaev et al. (2019)

Vicia faba

NaHS (100 μM)

Increased relative water content

Garc´ıa-Mata and Lamattina (2010)

References

Li et al. (2017)

upstream salt stress receptors. Plants adapt biochemical, physiological, and metabolic changes to cope with drought and salinity stress. At low concentrations, H2 S functions as a signaling molecule to control a variety of physiological plant activities, including stomatal apertures, seed germination, pathogen attack, root development, and flower senescence.

References Abbasi T, Abbasi SA (2010) Biomass energy and the environmental impacts associated with its production and utilization. Renew Sustain Energy Rev 14(3):919–937

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Hydrogen Peroxide and Its Role in Abiotic Stress Tolerance in Plants Syed Nazar ul Islam, Mohd Asgher, and Nafees A. Khan

Abstract Plants are continuously subjected to numerous abiotic stresses such as heavy metal, salinity, drought, high temperature, cold and ozone etc. which alters the normal functioning and development thus reduce the productivity globally. As a result, give rise to cellular toxicity by disruption of redox balance in the form of ROS, which eventually transforms into hydrogen peroxide (H2 O2 ). Hydrogen peroxide being a toxicant is now considered as a regulatory molecule because of its dual role. At low concentrations H2 O2 acts as a signalling molecule for expression of multiple pathways of antioxidant system and at higher concentration it causes cell burst and ultimately cell death. Moreover, these multiple abiotic stresses result in alteration of normal homeostasis of formation and scavenging of cellular ROS. To withstand these abiotic stressful conditions, plants have evolved efficient regulatory mechanism by developing anti-oxidative defense system. In this paper, we summarise the various aspects related to H2 O2 function, metabolism and describe multiple abiotic stress, their acclimation and scavenging system. At the end we examine the role of phytohormones and H2 O2 in abiotic stress acclimation and resilience. Thus H2 O2 crosstalk with phytohormones plays a pivotal role in developing strategies for the mitigation of abiotic stress to a great extent.

S. N. ul Islam · M. Asgher (B) Plant Physiology and Biochemistry Laboratory, Department of Botany, School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Jammu and Kashmir, Rajouri 185234, India e-mail: [email protected] N. A. Khan Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh 202002, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_9

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1 Introduction Hydrogen peroxide (H2 O2 ) is the divalent reduction derived from oxygen through a univalent intermediate superoxide anion. In ground state the molecular oxygen has got two unpaired electrons in its outer shell (Halliwell et al. 2000). The role of H2 O2 in plant biochemistry and physiology is of great importance (Ku´zniak and Urbanek 2000). Hydrogen peroxide plays pivotal role in acclimation, cell wall reinforcement, and lignification (Gill and Tuteja 2010), germination and seedling development (Wahid et al. 2008). Apart from that it also plays vital role in photosynthesis (Khan et al. 2015), senescence (Jajic et al. 2015), stomatal movement, cell growth and development (Deng et al. 2012). The contrasting regulation of stomatal functions by H2 O2 could be attributed to the varying impacts of distinct H2 O2 concentrations on both the development and movement of stomata. This suggests that H2 O2 may play a critical role in the intricate processes governing stomatal activity (Shi et al. 2022). The oxygen evolved from the cellular metabolic setup as by-product often results in reduction and brings about the genesis of reactive oxygen species (ROS) such as superoxide radical (O2 − ), H2 O2 , and hydroxyl radical (HO· ), which lays foundation for the malfunctioning of normal cellular phenomenon and eventually causes cell death (Dat et al. 2000; Bartosz 1997; Halliwell 2006). Numerous abiotic stressors, such as heavy metals, salinity, drought, heat, cold, ozone trigger the generation of ROS in plants (Ali et al. 2022). Hydrogen peroxide is non-radical ROS mediates intracellular signaling pathways and correlates with various plant responses (Waszczak et al. 2018). H2 O2 interferes with stress defence regulation and secondary metabolic activities in plants (Ellouzi et al. 2017). H2 O2 could significantly control the morphophysiological and biochemical responses in plants by dampening the proteome model (Khan et al. 2019). H2 O2 , previously thought to be a harmful ROS capable of destroying a variety of cellular structures, now is increasingly being recognised as a possible signalling molecule with many biological functions (Petrov and Van Breusegem 2012; Nazir et al. 2020; Asgher et al. 2021). It is now being recognised as a possible signalling molecule engaged in multiple physiological functions. Thus H2 O2 can minimise or improve plant stress reactivity by acting as a stress transducer (Nazir et al. 2019b; Asgher et al. 2021). In the biological world, the reduction of molecular oxygen generates the highly unstable superoxide anion radical, which acts as a precursor molecule for ROS. Which later undergoes dismutation to form H2 O2 catalysed by an enzyme superoxide dismutase (Liochev and Fridovich 1999). Comparatively among ROS species H2 O2 is regarded as more stable, long life and can easily cross membrane due to its smaller size (Noctor et al. 2014). Overproduction of ROS in plants results in oxidative burst when exposed to various biotic (herbivory, viral and fungal attack) and abiotic stressful conditions like chemicals, flood, drought, cold, heat, salinity, severe light intensity and various pollutants (Wojtaszek 1997). Thus plant growth and reproductive potential are greatly affected by environmental factors, including these various biotic and abiotic stresses. One of the consequences of stress is an increase in the

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cellular concentration of ROS. During evolution, plants have developed strategies to adapt various environmental stresses to function efficiently. Being as the member of ROS family H2 O2 plays dual role, at higher concentration promotes PCD and in lower concentration modulates ROS detoxification by regulating various gene expression pathway. Maintaining the nontoxic orbit between H2 O2 production and scavenging, the H2 O2 plays a key role in signal transduction to induce defence response to diverse biotic, abiotic stresses (Hossain et al. 2015). Thus the proper execution of H2 O2 could be convenient method to amplify stress tolerance and enhancing productivity of crop plants subjected to various stresses. Thus H2 O2 is a dynamic molecule that plays a role in a variety of biological functions, both in stressful and non-stressed situations. Exogenous administration of H2 O2 has a key function in improving plant metabolism amid stress circumstances, resulting in increased growth, photosynthetic capability, and antioxidant protection (Khan et al. 2018). Thus H2 O2 concentration could be used as a reliable indicator of the severity of environmental stress (Asaeda et al. 2022).

2 Biosynthesis In plants H2 O2 formation takes place by aerobic metabolism as a by-product via numerous routes. ROS can be generated in various cellular compartments, including mitochondria, chloroplasts, plasma membranes, peroxisomes, endoplasmic reticulum, and cell walls, under both basal and stress conditions. ROS are predominantly produced by peroxisomes and chloroplasts in the presence of light, while mitochondria are the major sites of ROS production in the absence of light (Khan et al. 2023). Majority of cellular compartments produces ROS either enzymatic or non-enzymatic processes (Mittler 2002). Enzymatic H2 O2 production include cell wall peroxidises (Francoz et al. 2015) amine oxidases and flavin-containing enzymes (Cona et al. 2006), NADPH oxidases, superoxide dismutase (Brewer et al. 2015). Moreover, some other oxidases like glucose oxidases, glycolate oxidases (Chang and Tang 2014) and sulphite oxidases also found in oxidising their respective cellular contents to give rise the formation of H2 O2 (Brychkova et al. 2012). The response of plants to abiotic stressors can involve the modulation of endogenous H2 O2 content or the regulation of expression levels of genes related to H2 O2 production (Dikilitas et al. 2020).. Various non-enzymatic reactions also take place in several cellular processes. There activities involved in photosynthesis and respiration are responsible for H2 O2 generation, through electron transport system occur in mitochondria and chloroplast (Niu and Liao 2016). H2 O2 is formed under favourable as well as in stressful environment in numerous cellular organelles like mitochondria, peroxisomes, chloroplasts, ER, plasma membranes and the cell wall. During light, chloroplasts and peroxisomes are the main sources of ROS formation, whereas mitochondria plays the leading role in production of ROS in dark conditions (Choudhury et al. 2013). In chloroplasts, oversaturation of electron transport system of photosystem I by exposed to high intensity of light, electrons are transmitted to oxygen molecules results in production of H2 O2 (Dietz et al. 2016). Apart from that H2 O2 also forms at the manganese

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containing domain of photosystem II as well as by reduction of ETC component like plastoquionol to singlet oxygen or superoxide anions (Khorobrykh et al. 2015). Peroxisome is the major site of photorespiration in plant cell. Glycolate generated in chloroplasts is transformed to glyoxylate by glycolate oxidase in peroxisomes, accounts for nearly 70% of total H2 O2 generation in a plant cell (Bauwe et al. 2010). Mitochondria also plays a role in endogenous production of H2 O2 in plant cell it takes place in ETC during aerobic respiration of complexes I and II, which then converted to H2 O2 by enzyme superoxide dismutase (Dickinson and Chang 2011). Oxidative catabolism of amines and polyamines results in production of H2 O2 as end product which is considered important source of its formation in plants (Yoda et al. 2003). Respiratory burst oxidase homologs (RBOHs), which are NADPH oxidases localized on the plasma membrane, have been identified as the source of H2 O2 that plays a pivotal role in ROS signaling cascades, particularly those activated by external stimuli (Sun et al. 2021). NADPH oxidase is also major group of H2 O2 -producing transmembrane enzymes also called respiratory burst oxidase homologs (RBOHs) due to homology with mammalian phagocytic defence system. NADPH oxidase oxidises cytosolic NADPH to reduce oxygen to superoxide which then immediately dismutated to H2 O2 (Segal 2016). The production of ROS under stressful environment, specifically H2 O2 , resulting from the activity of diverse cellular organelles such as mitochondria, chloroplasts, peroxisomes, cell-wall-bound peroxidases (PER), and RBOHs, facilitates the mediation of intercellular signaling pathways. The presence of Fe2+ ions, for instance, can induce cellular oxidative stress by promoting the production of hydroxyl radicals. Maintaining a delicate balance between these processes is critical for redox biology as they play a vital role in regulating cellular functions and metabolism (Mansoor et al. 2022). ROS formation takes place at multiple sites under both usual and stressful conditions as in (Fig. 1). Under ideal conditions, antioxidant defense machinery restricts ROS to cross the barrier that can cause oxidative damage. This homeostasis is perturbed by various abiotic stressors like heavy metals, salinity, drought, heat, cold, ozone etc. These changes in equilibrium induce an abrupt rise in cellular ROS levels, which targets and can severely damage biological molecules. The highly reactive and toxic ROS, which include 1 O2 , H2 O2 , O2 •− and OH• disrupt cellular functions as protein oxidation, disruption of nucleic acids and triggers lipid peroxidation, which eventually induce apoptosis (Fig. 1).

3 Metabolism Reactive oxygen species are constantly produced during numerous metabolic processes in, mitochondria, peroxisomes, chloroplast and cytoplasm which disrupts normal metabolism when produced in abundance (Ahmad et al. 2010). H2 O2 is created via electron transport in chloroplasts and mitochondria, peroxisomal oxidases, plasma membrane NADPH oxidases, type III peroxidases, and other apoplastic oxidases, as well as superoxide and superoxide dismutase. Aquaporins

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Fig. 1 Abiotic stress induced changes in plants

facilitate intracellular transport, and peroxiredoxin, catalase, glutathione peroxidaselike enzymes, and ascorbate peroxidise (APX), all of which have cell compartmentspecific isoforms to eliminate H2 O2 (Smirnoff and Arnaud 2019). Various abiotic stress factors results in overproduction and accumulation of ROS (H2 O2 , superoxide anion, and hydroxyl radicals) generating oxidative stress (Das and Roychoudhury 2014; Mostofa et al. 2014; Nahar et al. 2015). Activation of the antioxidant system is one of the methods that plants use to overcome oxidative stress. Plants have evolved a variety of antioxidant mechanisms, both enzymatic and non-enzymatic systems, that regulate and prevent plants from oxidative stress (Foyer and Noctor 2005). H2 O2 scavenging enzymes include SOD, catalase (CAT) (Willekens et al. 1997), APX, glutathione reductase (GR) (Jahan and Anis 2017) glutathione S-transferases (GSTs), peroxidase (POX, and peroxiredoxin (Prx) (Fan and Huang 2012). The nonenzymatic system comprises of glutathione (GSH), ascorbate (AsA), flavonoids and α-tocopherol, which are continuously involved in maintaining the levels of ROS, including homeostasis of H2 O2 (Miller et al. 2010; Kapoor et al. 2015). SOD is a metalloenzyme acts as first line defence system by dismutation catalysed process to quench superoxides to H2 O2 and reducing cellular • OH accumulation to great extent (Gill et al. 2015). CAT is a tetrameric Fe containing enzyme mainly located in peroxisomes which goes under oxidation and dissociates two molecules of H2 O2 into H2 O and O2 (Srivastava et al. 2002). CAT don’t requires any reducing agent for catalysis

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of dismutation process however, in organelles like chloroplasts, cytosol, mitochondria, and peroxisomes APX shows high affinity for H2 O2 and been found that APX was located in the cytosol (Begara-Morales et al. 2014) chloroplasts (Asada 2006) and use ascorbate as electron donor for scavenging of H2 O2 into H2 O (Anjum et al. 2016). H2 O2 decomposed in peroxisome by CAT (Nyathi and Baker 2006). These enzymes are evidently found in several organelles and may effectively lower H2 O2 concentration (Gill and Tuteja 2010). AsA, a major antioxidant for H2 O2 removal, can directly react with H2 O2 . GSH is an important antioxidant that can help restore AsA by rapidly oxidising excess H2 O2 . As a result, GSH plays a role in controlling H2 O2 levels and redox stability in plant cells (Krifka et al. 2012). The oxidase enzymes that produce H2 O2 , including glycolate oxidase, acyl-CoA oxidase, and sulphite oxidase, play a crucial role in various metabolic pathways such as photorespiration, fatty acid β-oxidation, and sulphur metabolism within peroxisomes, resulting in a significant accumulation of H2 O2 in the intracellular environment (Corpas et al. 2020). Infact, H2 O2 homeostasis seems to result in some biological effects on plant cells which may be a signaling in transduction pathway. The α-tocopherol is a lipophilic antioxidants which is the efficient scavengers of ROS and lipid radicals, making them critical for protection and essential component of biological system (Holländer-Czytko et al. 2005). Ascorbate and gultathione are two important metabolites water soluble in water. Among both ascorbate has the tendency to scavenge ROS formed radicals which are involved restoration of other oxidants as as α-tocopherol (Das and Roychoudhury 2014). Besides that it plays a crucial role in AsA-GSH cycle. Using AsA as reducing agent APX detoxifies H2 O2 to H2 O in a very first step. Eventually AsA is converted back to its reduced state coupled with GSH oxidation. Which is finally reduced by the activity of enzyme GR (Cuypers et al. 2016). Production and scavenging of H2 O2 is an integrated network system of plant responsible to function efficiently and regulate cellular homeostasisc (Gechev and Hille 2005; Bhattacharjee 2012; Phua et al. 2021).

4 Effects of H2 O2 on Abiotic Stress 1. Heavy metal In natural environment, plants are exposed to various biotic as well as abiotic stress conditions. Like others stresses, heavy metal (HM) stress plays adverse effects on crop productivity and development. Term HMs is any element which has got high density relatively. It describes the group of metals which has got their atomic density >4 g/cm3 or greater than 5 times to water. Heavy metals comprises of cadmium (Cd), nickel (Ni), chromium (Cr), zinc (Zn), lead (Pb), cobalt (Co), iron (Fe), silver (Ag), arsenic (As) and the platinum group elements. Some of these heavy metals like Cu and Zn act as cofactor and are necessary for enzyme catalysis in metalloproteins (Gill and Author 2014). Heavy metals are categorised into two groups: redox active (Cr, Co, Cu, Fe,) and redox inactive (Ni, Cd, Al, Zn, etc.). The redox activity involved in

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cellular redox reactions directly and gives rise to the formation of O2 •− and eventually forms H2 O2 and finally • OH genesis via the “Haber–Weiss and Fenton reactions” (Schützendübel et al. 2002). When plants are exposed to redox inactive metals results in oxidative stress by indirect process such as interaction with antioxidant mechanism, lipid peroxidation and disrupts ETC. Furthermore, metals have got the tendency to reduce the pool of the crucial antioxidant system like GSH, as a result the ROS equilibrium is disrupted (Lee et al. 2003). Besides that, many metals increase ROS formation by NADPH oxidases bound to plasma membrane (Remans et al. 2012). Thus regulating the delicate range of its formation and scavenging plays signalling pathways that results to plant acclimation to metal stress (Cuypers et al. 2016). Pretreatment of H2 O2 promotes the production of GSH when plant exposed to metal stress. Which regulates detoxification of H2 O2 , therefore decreases the deleterious impact of oxidative stress in plants exposed to heavy metals (Apel and Hirt 2004). Cd stress induces remarkable reduction in biomass of root and shoot development. Pre-treatment of H2 O2 promotes Cd tolerance in Oryza sativa and increases levels of an antioxidant-scavenging actions (CAT, SOD, GPX, GST, and APX). Also non enzymatic antioxidant enzymes GSH and AsA was increased (Hu et al. 2009). GSH acts as precursor molecule for metal phytochelatins (PCs). The sulfhydryl group of GSH plays important role scavenging of metals showing affinity to its sulfhydryl group (Noctor et al. 2012). Accumulation of proline in plants also takes place when subjected to metal stress and has got the ability for protection and maintenance of ROS scavenging enzymes such as peroxidase and CAT (Sharma and Dietz 2006). H2 O2 alleviated Cu and Cd toxicity via metallothionein in Oryza sativa by upregulating the anti-oxidative enzymes to maintain a redox balance, reducing the oxidative burst induced by ROS (Zhang et al. 2017). In the presence of 100 mg kg−1 Cu stress, root dipping treatment with H2 O2 had a substantial impact on growth and yield metrics, as well as leaf water potential, antioxidant system, photosynthetic pigments, stomatal movement, and osmoprotectants H2 O2 (0.1 mM) root dip treatment improves Ni persistence in Solanum lycopersicum by boosting the metabolism of antioxidative enzymes like POX, CAT, and SOD, as well as stomatal movement, morphology of root system, photosynthetic efficiency, growth parameters, and a variety of biochemical characteristics (Nazir et al. 2019a). Exogenously supplied lower concentrations of H2 O2 improved Vigna radiata plant resistance to Cu stress (Fariduddin et al. 2014). In oryza sativa As toxicity reduces the photosynthetic efficiency and yield. Application of H2 O2 acts as signalling molecule to increase PS II activity by protecting psbA and psbB expression, also reduces the oxidative stress by activating antioxidant mechanism (Asgher et al. 2021). H2 O2 modulates activation of the antioxidant as a significant mechanism of Cu-resilience (Nazir et al. 2019b). Activation of the cell cycle through H2 O2 may contribute to Me-JA-promoted adventitious rooting under Cd stress in plants (Feng et al. 2023). When plants are subjected to metal stress, nitric oxide (NO•) is generated. The majority of authors claim that exogenous NO• therapy significantly lowers metal toxicity by activating the anti-oxidant protective mechanism (Xiong et al. 2010). Nickel being an essential element for proper plant growth and functioning but its excessive accumulation give rise to ROS production which can cause cellular injury to protein, lipids and DNA (Asgher et al. 2015).

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Application of H2 O2 reduces the photosynthetic inhibition by increasing sulphur and nitrogen uptake in Ni induced stress in Brassica juncea by modulating Rubisco activity (Khan et al. 2016). 2. Salinity Salinity is the prime abiotic stress which has great negative impact on germination, growth and development in plants. Productivity declines to drastically when soil solution pH exceeds 8.5 or electron conductivity of saturation soil extract crosses above 4 dS m−1 (Sairam et al. 2002). Salinity is caused by the accumulation of extra ions of soluble salts in soil solution like sodium (Na+ ), calcium (Ca2+ ), sulphate (SO4 2− ), chlorine (Cl– ), magnesium (Mg2+) and bicarbonate (HCO3 – ) (Isayenkov 2012). Lowering of osmotic potential takes place when salts get accumulated results in decrease in capacity of free water to the root cells. Salt stress results in reduction of photosynthesis and respiration. Nucleic acid metabolism and translation also gets disrupted. Thus stress results in inhibition of growth and reproductive potential in plant (Sairam et al. 2002). Salinity causes imbalance to the cellular processes by sudden rise in intracellular level of ROS, favouring oxidative stress and promotes the genesis of oxidative reactions in plants. Under ideal conditions there is proper system of the ROS formation and respective scavenging mechanisms. With the result there is the accumulation of ROS that interrupts to get neutralised by its anti-oxidative system. In salt stressed plants ROS formation causes injury by reacting with unsaturated fatty acids. Eventually, results of lipid peroxidation which has key role in membrane assembly. Salinity causes homeostasis interference and photosynthetic catalytic activity is disrupted and also alters the dynamic activity of ROS detoxifying species. Plants have got efficient mechanism to prevent themselves from ROS species by employment of anti-oxidants includes both enzymatic and non-enzymatic system. Under salinity stress anti-oxidant gets activated and imparts protection to cell membranes and cell function (Djanaguiraman and Prasad 2013). Pre-treatment of H2 O2 exogenously improves salt tolerance to trigger those genes that act as transcription factors for scavenging enzymes like sucrose phosphate synthase and pyrroline5-carboxylate synthase (Uchida et al. 2002; Neto et al. 2005). Triticum aestivum seedlings show effective scavenging system when soaked in H2 O2 for 8 h than untreated seedlings under salinity stress. H2 O2 treatment also plays role to maintain turgor, K+ /Na+ balance, lowers ion leakage and thus enhance membrane functions under salt stress (Wahid et al. 2007). Foliar spray of H2 O2 in maize reduce salt stress to great extent and the antioxidant enzyme actions like APX, GPOX, CAT and SOD was seen to be increased. Among these enzymes CAT responds quickly than others and MDA concentration was reduced with catalytic activity of CAT (Gondim et al. 2012). The osmotic water potential drops in a saline conditions due to the high concentration of soluble salts. Plants have evolved acclimated role by formation of inorganic ions to achieve osmotic adjustment include hydrophilic compounds called osmolytes (Peng et al. 2009). Salinity causes biosynthesis of proline and glycine betaine which are found osmoprotectant in nature helps in restoration of cellular osmotic potential and neutralisation ROS by scavenging mechanism (Bohnert and Jensen 1996). Under salt stress, H2 O2 and ethylene may be known to regulate an alternate respiratory

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pathway during salt stress. During salt stress, H2 O2 and ethylene known to be regulate the alternate respiratory pathway (Wang et al. 2010). Plants pretreated with H2 O2 increased photosynthetic efficacy by retaining stacking thylakoids, which prevented salinity-induced energy surplus and ultrastructural damage. Some metabolites, such as arabitol, glucose, asparagine, and tyrosine, were shown to be modulated, which could help maintain osmotic balance and reduce oxidative stress (dos Santos Araújo et al. 2021). 3. Drought Among abiotic stress drought stress is one of the significant stress which produces numerous ROS includes superoxide (O2 − ), hydroxyl radicals (OH), singlet oxygen (1 O2 ), and H2 O2 . ROS formation takes place in those cell organelles which are involved in active ETC mechanism like mitochondria, chloroplast, apoplast and peroxisomes, etc. These organelles produce various anti-oxidative enzymes like GPX, SOD, CAT, APX, etc., having the potential to maintain the homeostasis in plants by neutralizing reactive species produced due to oxidative stress. Apart from that, plants are also developed with the non-enzymatic scavengers such as, tocopherols, GSH, carotenoids, alkaloids, ascorbate and flavonoids. Plants have got efficient antioxidant mechanism to get adapted to adverse conditions including drought stress (Impa et al. 2012). Among ROS, H2 O2 has been used to enhance resistance of plants against various abiotic stresses. Foliar spray and seed priming techniques are excellent procedures for H2 O2 application because of not so costly and simplicity. When wheat is primed with H2 O2 results in increase in growth, uptake of water potential, osmolytes production and accumulation, antioxidant system activity, and seen higher yield under drought stress (Habib et al. 2020). Hydrogen peroxide acts as a key player as a signalling molecule in the plant cellular system, which activates numerous physiological changes that play vital role in tolerance and scavenging mechanism. Seed priming with H2 O2 has direct impact on growth, physiological activities and antioxidant system. Rice seedling subjected under drought stress enhance tolerance when primed with appropriate levels of H2 O2 . Exogenous H2 O2 act as a signalling molecule that activates various defence mechanisms, such as antioxidant activation mechanism, and osmotic adjustment. H2 O2 seed priming enhances antioxidant activities, which plays crucial role to lower oxidative stress (Jira-Anunkul and Pattanagul 2020). Exogenous treatment of H2 O2 at low concentrations activates and enhanced adjustment to drought in wheat (Liheng et al. 2009). In signal pathway, H2 O2 acts as a secondary messenger leads to stress acclimation and tolerance. Exogenous H2 O2 spray under drought stress amplifies foliar membrane stability by decreasing the MDA levels. Pre-treated mustard seedlings have got lower endogenous H2 O2 levels than untreated seedlings under drought stress (Mohammad 2013). Proline accumulation takes place under drought stress which plays a protective role as scavenging of ROS, results in improvement acclimation ability and growth of plants subjected under drought conditions (Türkan and Demiral 2009). Drought stress leads to elevated levels of endogenous abscisic acid (ABA) and salicylic acid (SA), and enhances their signaling along with an increased level of H2 O2 . Under drought conditions,

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proline accumulation is induced and mediated by ABA-dependent MAPK6 activation via OXI1. This ultimately results in the upregulation of ProDH as a hypersensitive response to the elevated H2 O2 level (Lee et al. 2022). During H2 O2 or SA treatment in Oryza sativa shows efficacy in reduction of drought stress and also augments photosynthetic pigments that rise due to oxidative damage, which could aid in the maintenance of normal photosynthesis under drought (Sohag et al. 2020). Under drought stress, the impacts of H2 O2 on agronomic traits in Oryza sativa were studied. Seed priming or foliar treatment of H2 O2 at concentrations of 15, 5, and 1 mmol/L were used. The findings revealed that seed priming and foliar spray of H2 O2 increased various yield components. It was discovered that H2 O2 of concentration 5 mmol/L was the most efficient concentration for reducing drought stress in rice throughout the reproductive stage (Jira-Anunkul and Pattanagul 2020). The role of H2 O2 and sulphur (S) in combination was investigated to protect photosynthetic efficacy of Triticum aestivum subjected to drought stress. H2 O2 improves pigment system (PS) II activity, and growth in the presence of S, also increased S-assimilation capacity, antioxidant enzyme activity, and GSH synthesis under drought stress (Sehar et al. 2021). 4. Heat Heat stress also has negative impact on photosynthesis affects intracellular as well as intercellular membrane components, protein content and antioxidant scavenging machinery, henceforth has substantial impact on crop output (Georgieva 1999). Heat stress gives rise to oxidative free radicals in plants caused by the genesis and the accumulation of O2 − , H2 O2 and OH− , commonly called as ROS. When ROS level increases above the expected threshold causes calcium influx in plasma membrane results in PCD. In response to heat stress electron leakage takes place from ETC when ROS gets accumulated inside cellular compartments (Medina et al. 2021). Higher concentration of H2 O2 under thermal stress give rise to active oxygen species (AOS) (Paolacci et al. 1997). When the Lycopersicon esculentum was cultured at two different temperatures (25 °C, ideal temperature, and 35 °C), the impact of temperature on oxidative metabolism was examined. A higher temperatures over (35 °C) H2 O2 is unable get removed by GSH/AsA mechanism and in turn gets accumulated. This increase in H2 O2 concentration would initially decrease foliar content later goes under PCD. However, plants grown under ideal temperature shows excellent AOS detoxification mechanism and proper growth and development. It has been seen that H2 O2 production significantly rose as 3.5 folds more than when grown on 35 °C, due to higher activity of SOD at 35 °C (Rivero et al. 2004). Plants exposed to high temperature burst of H2 O2 generated as a result of NADPH oxidase activity. This formation promotes the induction of heat responsive genes (HSF) by direct sensing of H2 O2 . HSPs acts as molecular chaperones that safeguard the native structure and function of proteins from denaturation, allowing the plant to withstand to intense heat stress. There are numerous HSPs like HSP101, HSP90, HSP70, HSP23, etc. have been found in many plant and non-plant species (Miller and Mittler 2006). In maize pre-treatment of heat shock induces cross tolerance by formation early transient of endogenous H2 O2 . With the result H2 O2 acts as

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transcription factor for the expression of scavenging enzyme system and induces not only thermotolerance to heat stress but also cross tolerance to other abiotic stresses (Gong et al. 2001). In Solanum tuberosum leaves, sucrose pre-treatment was found to successfully limit heat stress-induced increases in electrolyte leakage and reduce the generation of ROS such as O2 •− and H2 O2 . In heat-stressed potato seedlings, pretreatment with sucrose having concentration100 mM results in endogenous elevation of sucrose and proline content, as well as higher antioxidant enzyme activities like SOD, CAT, APX, and POD, especially when seedlings are subjected to heat stress for 6 to 8 h. During heat stress, there was also a possible decrease in O2 • - and H2 O2 buildup, as well as the preservation of cell membrane integrity (Gong and Chen 2021). Hydrogen peroxide application in Sorghum under drought environment improved germination rate and seedling development by lowering oxidative stress in germination, promoting drought tolerance, and enhancing enzymes that regulate energy metabolism (Song et al. 2023). 5. Cold Freezing is one of major abiotic stress that reduces the crop productivity and distribution of geographically plant species. ROS is induced in freezing stressed plants such as H2 O2 , O2 − and HO· regularly as by-product (Baek and Skinner 2012). Among ROS, H2 O2 is a primary component to play dual role in plant tolerance to freezing stress. Initially it was considered as negative entity for lipid peroxidation and cellular toxicity whereas recent research has provided insight on HS O2 significance as a signalling molecule that trigger acclimatization responses to abiotic stressors (Suzuki et al. 2012; Baxter et al. 2014). Under various stresses, at very low concentrations acts as signal molecules which are involved in acclimatory response, activating the tolerance mechanism against various abiotic stresses whereas at high concentrations it causes oxidative burst and ultimately causes programmed cell death (Asada 2006). H2 O2 gets accumulated during the cold acclimation is relative stable oxygen species so to withstand and cope up the unfavourable stressed conditions of changing environment. H2 O2 has been regarded as to be a signalling molecule in defence response in maize when exposed to chilling stress (Prasad et al. 1994). The impact of H2 O2 in Solanum lycopersicum plant after cold acclimation at 12/10 °C and followed by chilling at 7/4 °C results in increased H2 O2 levels, respiratory burst oxidase homolog 1 gene expression (Rboh1), and NADPH oxidase function, resulting in antioxidant enzyme expression and function being up-regulated. Chilling induced a constant increase in H2 O2 formation, results in MDA production, and oxidises redox state of glutathione in non-acclimated plants. High concentration of H2 O2 reduces the CO2 assimilation rate and the maximal quantum yield of (Fv/Fm) of photosystem II. Whereas in cold-acclimated plants chilling caused photo inhibition, peroxidation of membranes and reduction in CO2 assimilation rate gets depleted. In the apoplast of plant cells, cold acclimation increased NADPH oxidase activity and increased H2 O2 levels. Cold acclimation elevated H2 O2 levels, which moved the GSH/GSSG duo into a more reduced state and drove the transcriptional activation of defence and antioxidant genes, resulting in increased antioxidant enzyme activity that helps to reduce oxidative stress conditions (Zhou et al. 2012). During

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cold acclimation H2 O2 enhances antioxidant capacity by increasing the activities of ROS scavenging enzymes, such as dismutase SOD, APX and CAT. Besides that in many plant species it also promotes high levels of GSH content and activates the GR enzyme, which act as an associate in chilling tolerance. H2 O2 also plays a significant role in modulating cellular GSH content levels when applied exogenously as well as endogenously (Kocsy et al. 2001). Increased H2 O2 and ABA both activate their protective mechanisms, allowing cold-responsive gene expression and antioxidant enzyme activity to be activated, limiting ion leakage and lipid peroxidation, and thus improving photosynthetic efficiency (Fv/Fm and ETR) in wheat exposed plants to cold stress (Wang et al. 2018). At the germination and seedling stages of rice, the effects of H2 O2 priming reduces chilling stress. Treatment of rice seeds with H2 O2 (15,10, and 5 mM H2 O2 ) solution for 24 h and then chilled for 6 or 12 h every 24 h for 7 days. Chilling exposure significantly hinder germination indices, biological properties, total chlorophyll content, and antioxidant capacity CAT and APX, according to the results. Thus H2 O2 priming shows positive physiological effects by boosting antioxidant enzyme activity in chilling stressed rice plant (Afrin et al. 2018). Cold stress induces the formation of MDA, EL, and H2 O2 in plants. MDA, a by-product of lipid membrane peroxidation, serves as an indicator of oxidative stress in plants. The concurrent increase in H2 O2 levels corresponds with elevated MDA rates, thereby characterizing a biochemical indicator for free radical-mediated damage in plants subjected to stress (Ma et al. 2022). 6. Ozone Tropospheric ozone (O3 ) is considered as a secondary pollutant of air which has got the negative impact on plant crop productivity (Ueda et al. 2013). That includes leaf injuries, leaf lesions, potentially reduced growth and crop productivity (Andersen 2003). Ozone makes entry through stomata, results in the formation ROS mainly hydrogen peroxide and superoxide anions in apoplast triggers oxidative burst and degrades cell membrane integrity (Keutgen and Pawelzik 2008). On the other hand ROS accumulation promotes hypersensitivity and induces defence response (Langebartels et al. 2002). ROS accumulation to ozone exposure is not uniformly distributed throughout the leaf, but remains restricted only to periveinal region (Schraudner et al. 1998). Ozone causes formation of (O2 -. ) radical and H2 O2 to form, which cause downstream processes (Kangasjärvi et al. 2005). Under severe ozone stress in rice (Oryza sativa) leaves. Peroxisomal, chloroplastic and mitochondrial, SODs all dramatically reduced their gene expression in response to ozone, although cytosolic SODs had minimal effect. This indicates that organeller SODs are more significant than cytosolic SODs in the ozone responses (Ueda et al. 2013). MDA content increases significantly on elevated concentrations of ozone. Under acute ozone stress there was no change in NADPH oxidase which is prime H2 O2 production site membrane bound transmembrane protein significantly on elevated concentrations of ozone (Dong et al. 2006). Plants have self-protective scavenging system in order withstand H2 O2 accumulation. Antioxidant enzymes like GR, APX, AsA-GSH cycle, AsA-GSH cycle, MDHAR and DHAR. These enzymes provide protective mechanism against the accumulation of ROS concentration but are affected in presence of

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O3 (Lyons et al. 1999). During early phases of ozone stress the enzymatic action of APX, MDHAR, GR and DHAR gets increased which indicates scavenging system enhances antioxidant enzyme activities, however when O3 lasts for longer period, the scavenging anti-oxidant system gets disturbed, thus unable to remove excessive ROS by self-scavenging antioxidant system. ROS accumulation attacks membrane system causes lipid peroxidation and results in plant damage and finally in plant growth (Zhao et al. 2011). Various antioxidants such as CAT, APX, and MDAR in conjunction with AsA, can detoxify H2 O2 , leading to a reduction in H2 O2 formation (Karyotou and Donaldson 2005). The increased AsA concentration in all cells, as well as their potential to detoxify entering ozone, reduces the leaf’s oxidative stress (lower levels of foliar and apoplectic H2 O2 (Peng et al. 2005). Figure 2: Showing mechanism of abiotic stress induced signalling in plants via the induction of antioxidants system.

Fig. 2 Showing mechanism of abiotic stress induced signalling in plants

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5 Role of H2 O2 and Phytohormones in Mitigation of Abiotic Stress In natural environment plants are subjected to multiple abiotic stresses, to cope up these conditions plants owe intrinsic mechanism to perceive signals and showing optimal responses to such external signals. Phytohormones like salicylic acid (SA), abscisic acid (ABA), jasmonic acid (JA), and ethylene (ET) acts in very low concentration regulates various abiotic stress to mediate adaptive response (Bostock 2005; Lorenzo and Solano 2005; Mauch-Mani and Mauch 2005). It is well known that H2 O2 and other ROS are vital molecules that takes part in multiple signalling system in both abiotic and biotic stress responses, often serve as secondary messengers for the expression of defence transcription factors (Foyer and Noctor 2009, 2012). Phytohormones in response to various abiotic stress promotes ROS production among which H2 O2 is involved in complex coordinated signalling and induce stress tolerance to a great extent (Foyer and Noctor 2009; Bartoli et al. 2013). Apart from important plant hormone ABA also regulates abiotic stress response. ABA can cause plant cells to produce ROS, and H2 O2 generation in guard cells is crucial for ABAmediated stomatal closure (Kwak et al. 2003). The application of exogenous ABA was observed to reduce the amount of H2 O2 and relative conductivity in wheat plants exposed to low temperatures ranging from 0°C to -25°C, indicating that ABA can confer protection against the damaging effects of cold stress. Additionally, ABA was found to enhance cold tolerance in both leaves and rhizomes of wheat plants at -10°C and -20°C, by stimulating the production of ROS. These findings suggest that ABA has potential as a protective agent for crops exposed to cold stress in agricultural settings (Jing et al. 2020). Under a variety of environmental stresses, H2 O2 has been shown to interact directly or indirectly with other phytohormones including ethylene, gibberellins, SA, auxins, ABA, and cytokinins, nitric oxide, brassinosteroids and Ca+ (as signalling molecules), to facilitate plant growth and productivity responses to abiotic factors (Nazir et al. 2020). Under salinity and drought stress, it was reported H2 O2 behaves a signal that triggers plasma membrane Ca+ channels causing ABA induced closure of stomata (Kim et al. 2010). Abiotic stress increases the ABA/GA ratio, which boosts DELLA protein expression and alleviates H2 O2 levels (Considine and Foyer 2014). In plants, H2 O2 and ABA crosstalk provide adaptation to water stress (Li et al. 2016). Induced ABA formation also activated H2 O2 generation in pumpkin-grafted cucumber leaves, results in rise of antioxidant defence system and regulation of their gene products. SOD, APX and POD (Shu et al. 2016). In Arabidopsis, salt stress or ABA treatment induces the expression of NADPH oxidase producing genes, as well as the buildup of H2 O2 . An inhibitor (DPI) of NADPH oxidases can diminish H2 O2 accumulation, and DPI-treated plants have lower salt tolerance (Kwak et al. 2003; Leshem et al. 2007). Endogenous SA and H2 O2 levels rise in plant cells when they are under stress. SA therapy, on the other hand, can reduce the amounts of H2 O2 degrading enzymes like CAT and APX (Yuan

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and Lin 2008). Ethylene promotes the ROS formation among H2 O2 induces expression of ET biosynthetic and sensitive genes by inducing ROS production (Vandenabeele et al. 2003). The PCD pathways that occur during leaf abscission are reliant on ET-induced NADPH oxidase-dependent H2 O2 production (Sakamoto et al. 2008). Furthermore, stomatal closure necessitates the combined efforts of H2 O2 and ET. High salinity and drought stress dramatically activate the ETHYLENE RESPONSE FACTOR1 (ERF1) in Arabidopsis (Cheng et al. 2013). MAPK (mitogen activated protein kinase) cascades are modulated by exogenous treatment of H2 O2 , which later on regulated by hormones like JA, SA and ABA (Cristina et al. 2010). H2 O2 triggers the MAPKs (MPK6 and MPK3) in Arabidopsis via the MAPK kinase kinase (MAPKKK) (Kovtun et al. 2000). MKP2 acts as a potent inducer network of MPK3 and MPK6 molecules, which regulates abiotic as well as biotic stress responses (Zhou et al. 2012). It was seen H2 O2 activates photosynthetic genes via BRs, indicating that H2 O2 and EBR regulate calvin cycle and sugar metabolism via redox signalling, enhancing photosynthetic activity and crop yield (Jiang et al. 2012). Jasmonic acid (JA) and methyl jasmonate (MJ) are well-known signal molecules that are excellent inducers of H2 O2 genesis in plant cell cultures and also plays important role in defence system of plants (Wang and Wu 2013). MeJA may possibly have a function in signal transmission in grape cells, controlling NO and H2 O2 levels and increasing the activity of enzymes that takes place in phytoalexin production (Wang et al. 2012). The exogenous treatment of H2 O2 and SA significantly enhance stress tolerance under drought conditions. The positive benefits of H2 O2 or SA treatments could be ascribed to the H2 O2 or SA-mediated reduction of drought-induced ROS over abundance, presumably through increasing antioxidant enzyme activity. Furthermore, application of exogenous H2 O2 or SA was found to be beneficial in osmotic adjustment (Sohag et al. 2020). Application of BR significantly enhances cold tolerance in grape seedlings through the maintenance of higher antioxidase activity, osmoprotectant levels, maximum photosystem II quantum yield, and chlorophyll content, while reducing cell membrane damage and regulating phytohormone levels. Exogenous BR treatment further stimulates upregulation of the VvRBOHa, VvRBOHb, and VvRBOHe gene expression, NADPH oxidase activity, and endogenous H2 O2 levels in grape seedlings exposed to cold stress (Wang et al. 2022). Furthermore, the presence of H2 O2 can alter the signaling pathways involving nitric oxide (NO) and Ca2+ , thereby regulating plant growth, development, and various cellular and physiological responses (Singh et al. 2020). Table 1 showing the effect of combined exogenous treatment of H2 O2 and phytohormones under abiotic stress.

6 Conclusion Abiotic stress is the prime limiting factor which has negative role on plant development and reproductive potential. During abiotic stress ROS formation serve as source for the oxidative burst in plants. H2 O2 only among ROS which has got stability with

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Table 1 Effect of combined exogenous treatment of H2 O2 and phytohormones under abiotic stress Type of stress

H2 O2 dose Conc

Plant name

Phytohormones

Response

Reference(s)

Cold

1.5–2.5 mm/L

Musa acuminata

SA 0.3 0.9 mm/L

Induced stress tolerance by signal transmission and up-regulating various important enzymatic antioxidants

Zhang et al. (2003)

1.0 mM

Cucumis sativus

IAA 75 μM

Improved photosynthesis and reduced lipid oxidation by inducing the expression of genes involved in cold tolerance

Zhang et al. (2021)

200 μM

Vigna radiata

100 μM ABA

Improved chilling tolerance by increasing the levels of GSH, an important antioxidant

Yu et al. (2003)

50 mM

Zea mays

0.5 mM SA

Reduces the Li et al. duration of seed (2017) germination also enhance antioxidant enzyme and α-amylase activity. Endogenous concentration of H2 O2 and SA was also increased

15/20 mM

Brassica juncea

10–8 M 24-EBL

Shows adaptation towards chilling stress by ameliorate

Sirhindi et al. (2009)

10 mM

Zea mays

ABA

H2 O2 priming reduce water loss and increases stress tolerance due to accumulation of soluble solutes

Terzi et al. (2014)

Drought

(continued)

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Table 1 (continued) Type of stress

H2 O2 dose Conc

Plant name

Phytohormones

Response

Reference(s)

5 mmol/L

Oryza sativa

0.5 or 1 mmol/L

Exogenous Sohag et al. treatment of H2 O2 (2020) or SA plays effective role by mitigating oxidative damage to maintain normal cellular homeostasis in rice seedling subjected to droght stress

800 μM

Cucumis sativus

0.5 μM ABA

Promoted adventitious rooting and fresh weight as compared to control under drought stress

Heat

H2 O2 30 ppm

Gossypium hirsutum

SA 50 ppm

Application of SA Sarwar et al. H2 O2 , extract of (2018) moringa leaf, and ASA attempts to mitigate heat related injury by neutralizing excessive ROS by activating antioxidant scavenging system. The parts of cotton like lint yield fiber quality, branching, boll weight seen to be increased by modulating the leaf CAT, SOD activity

Heavy metal

1.0 μM

Rice seadlings

SA 1 mM

Reduces the As toxicity in contrasting cultivars of rice plants that differ in tolerance towards arsenic

Li et al. (2016)

Mallick et al. (n.d.)

(continued)

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Table 1 (continued) Type of stress

Salt stress

H2 O2 dose Conc

Plant name

Phytohormones

Response

Reference(s)

0.1 mM

Solanum lycopersicum L

10− 8 M EBL

Combined suplementation improves seed viability, root morphology, stomatal movement, chloroplast and phptosynthetic efficiencyand also increases resiliance to Solanum lycopersicum plant subjected to Cu stress by transcription of proline and antioxidant enzymes

Nazir et al. (2021)

10 μM

Silybum marianum(milk thistle)

SA 0.25 μM

Enhance the (Nizar et al. growth parameters 2022) like leaf area„root shoot ratio and ratio of dry to fresh weight of both root/shoot. Also enhance the formation of photosynthetic pigments and various secondry metabolites by subpressing the deletarious effect caused by cadmium stress

10 mM

Rice plant

NO (SNP 1 mM)

Induces antioxidant scavenging enzymes as well as synthesis of proline and heat shock proteins when subjected to heat/salt stress Also shows elevation in quantum yield (photosystem II)

Uchida et al. (2002)

(continued)

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Table 1 (continued) Type of stress

H2 O2 dose Conc

Plant name

Phytohormones

Response

Reference(s)

10 mM

Solanum lycopersicum

NO (0.1 Mm)

Maintains cellular water content and membrane stability improves photosynthetic efficiency, also enhance photosynthetic efficiency

Hajivar and Zare-Bavani (2019)

500 μM

Gossypium hirsutuvum

10 μM ABA

H2 O2 enhances the expression of SOS1 gene responsible for Na+ efflux and ABA regulate expression of different aquaporin genes to increase water uptake

Kong et al. (2016)

long life allows to make it capable to mitigate other ROS molecules. During oxidative stress plays as double function in plant cell, on one hand acts as toxic oxidant causing cell damage and ultimately cell death when accumulated in high concentrations. On other side it serves contrarily as a signalling molecule when present in very low concentration triggers antioxidant process to maintain the cellular redox balance. The detoxification is maintained by enzymatic as well as non-enzymatic antioxidant process when plants experience stressful environment. It was found that seedlings treated exogenously with produces an signal that mediates acclimatory response and prevents plants from stressful environment by regulation of cellular redox balance. It was found that H2 O2 plays a crucial role for cellular pathways that boosts tolerance by regulating osmotic adjustment and acclimation to abiotic stresses. H2 O2 protects against the negative effects of abiotic stresses, but there is a pressing need to examine the control of a number of physiological functions mediated by H2 O2 , PGRs like SA, BRs, auxins, ET, JA, GAs ABA and CKs, and Ca2+ , NO as signalling species. H2 O2 is also involved in regulating signalling pathways via MAPKs pathways, which serves as an important strategy to hormone-antioxidant interactions and will aid in growth of plants to withstand to various abiotic stresses. For future research, use of morphological and molecular investigation to gain deeper knowledge for the role of H2 O2 in plants. The interplay between phytohormones and H2 O2 also manage variety of abiotic stress responses for its mitigation and tolerance.

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Interaction of Ethylene and H2 S in Plant Stress Management Humaira, Saba Wani, Nargis Bashir, Najeeb-ul-tarfeen, Zulaykha Khurshid Dijoo, and Khair-ul-nisa

Abstract Hydrogen sulfide (H2 S), merely considered a harmful gas, stays as an intrinsic new gaseous signaling agent that has been broadly researched in plants from seed development to senescence. As global regulatory authorities, phytohormones, which include stimulators (such as auxin: AUX; gibberellin: GA; cytokinin: CTK; and melatonin: MEL) and inhibitors (such as ethylene: ETH; abscisic acid: ABA; salicylic acid: SA; and jasmonic acid: JA), hold an indispensable concern during the progressive stages, advancement, reaction, and adjustment to hostile conditions of plants. Phytohormones are now thought to intend the most important pursuits for increasing plant growth, throughput, and strain resistance, that influence agricultural plant performance and productivity. Exogenous H2 S reduces Ethylene generation in peach seedling roots amid waterlogged conditions, and their interplay adversely impacts Ethylene manufacture during stress caused by osmosis. Ethylene-induced closure of stomata also needs H2 S. The interplay of H2 S and ethylene is critical for reducing hexavalent chromium stress. H2 S collaborates with phytohormones, additional gasotransmitters, and ionic messages like abscisic acid (ABA), ethylene, auxin, CO, and NO in its regulatory roles.

Humaira (B) · Najeeb-ul-tarfeen Centre of Research for Development, University of Kashmir, Srinagar, Jammu and Kashmir, India e-mail: [email protected] S. Wani Department of Biochemistry, University of Kashmir, Srinagar, Jammu and Kashmir, India N. Bashir Department of Botany, University of Kashmir, Srinagar, Jammu and Kashmir, India Z. K. Dijoo · Khair-ul-nisa Department of Earth and Environmental Sciences, University of Kashmir, Srinagar, Jammu and Kashmir, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 M. Fatma et al. (eds.), Gasotransmitters Signaling in Plant Abiotic Stress, Signaling and Communication in Plants, https://doi.org/10.1007/978-3-031-30858-1_10

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Abbreviations ABA ACC ACO ACS APX AUX AVG BR CAT CTK DATS DCD DES1 ETH FMO GA GSH H2 S JA LCD MDA MEL NaHS NPA PCD POD SA SAM SL SOD

Abscisic acid 1-Aminocyclopropane-1-carboxylic acid ACC oxidase ACC synthases Ascorbate peroxidase Auxin Aminoethoxy vinyl glycine Brassinolide Catalase Cytokinin Diallyl thiosulfinate D-cysteine Desulfhydrase L-cysteine desulfhydrase 1 Ethylene Flavin monooxygenase Gibberellin Glutamyl-I-cysteinyl-glycine, Glutathione Hydrogen sulfide Jasmonic acid L-cysteine Desulfhydrase Malondialdehyde Melatonin Sodium hydrosulfide Napthylpthalamic acid Programmed cell death Peroxidase Salicylic acid S-adenosylmethionine Stringolactone Superoxide dismutase

1 Introduction The gaseous transmitter hydrogen sulfide (H2 S), which includes nitric oxide (NO), carbon monoxide (CO), H2 S, ammonia, and ethylene (ETH), From germinating seeds to maturity and withering, is essential to the plant’s entire lifespan (Banerjeea et al. 2018; Corpas and Palma 2020). H2 S has a dosage-related double function, operating as a signaling molecule at trace levels and as a cytotoxin at large concentrations (Jin and Pei 2015; Li et al. 2016b). H2 S is one of a group of tiny proactive chemicals that are recognized to perform a part in plant cell signaling (Hancock 2019).

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According to recent discoveries, H2 S can have a part in stomatal crosstalk and may enhance chloroplast biosynthesis (Garcia Mata and Lamattina 2010; Lisjak et al. 2010). H2 S has an impact on germinating seeds, stomatal motion, and root maturation (Liu et al. 2012; Fang et al. 2014). H2 S enhances plant stress resistance and impacts a range of biological pathways (Zhang et al. 2009a, b; Chen et al. 2018). Several abiotic stressors, for instance, osmotic stress, heavy metal ions, and water deficit can be mitigated by H2 S (Zhu et al. 2018; He et al. 2019; Kaya et al. 2020). It has been revealed that sodium hydrosulfide boosted maize heat tolerance and that proline was involved (Li et al. 2013). It was discovered afresh that H2 S has indeed been substantially engaged in the ecological response to the stress of agronomic and horticultural crops as a signaling molecule (Ali et al. 2020; Zulfqar and Hancock 2020; Ahmed et al. 2021). Furthermore, during everyday biological and stress settings in plants, the role of H2 S as a signaling agent and its subsequent signal transmission modes are unrevealed. In tomatoes and fruit trees like mandarins, it really does seem to promote sensitivity of plants to underwatering distress by raising the antioxidative enzymes (Murshed et al. 2013). H2 S has been demonstrated to promote maize seedling development and reproduction during elevated conditions by triggering antioxidant systems and osmolyte production, according to studies (Zhou et al. 2018). Under some environmental conditions, H2 S can cause alterations in antioxidant capacity (Hancock 2019) (Fig. 1).

2 Highlights About H2 S • H2 S contributors are useful instruments for studying its effects on plant physiological and biochemical processes. • By modulating Na+ /K+ equilibrium and metal ion absorption and transit, H2 S increased saline and metal ions tolerance. • Plants respond to abiotic stressors through the antioxidant defense system, the AsA-GSH cycle, and the H2 S-Cys cycle. • Plant responses to abiotic stressors include interactions between H2 S and NO, phytohormones, and polyamines. • Modification of persulfidation is a promising path for H2 S research. By increasing the photosynthetic rate and decreasing Cr assimilation, H2 S increased barley tolerance to chromium (Cr) stress (Ali et al. 2013a, b). Under salt distress, H2 S boosted photosynthesis and soluble protein levels while inhibiting the escalation of reactive oxygen species (ROS), considerably improving rice sodium resistance (Mostofa et al. 2015). The activity of L-desulfhydrase (L-CDes; EC4.4.1.1) and D-desulfhydrase (D-CDes; EC4.4.1.15) enzymes were up-regulated in Arabidopsis thaliana under drought stress, leading to rising in internal H2 S generation (Jin et al. 2011). Exogenous treatment of H2 S donor chemicals in plants may also raise endogenous H2 S levels. Given the importance of H2 S, numerous investigations have been conducted to learn how it is transferred through cell membranes. According to these

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Nitric oxide (NO)

Abscisc acid

Hydrogen sulfide

Carbon monoxide

(H2S)

Abiotic stress protection

Oxidative stress regulation

Protein persulfidation

Energy metabolism regulation

Post-harvest protection

Fig. 1 Interactive role of H2 S with Phytohormones and some other molecules

investigations, H2 S is transported across the cellular membranes via a simple molecular diffusion that would not require the use of facilitation (Mathai et al. 2009). H2 S figures in chemical signals and assists a wide compass of biological activities, along with numerous protective functions (Figs. 2 and 3). Despite the fact that H2 S gas is an excellent instrument for studying its function in plant vegetation, it must be scarcely employed in studies due to the difficulties in maintaining constant concentration levels throughout the experiment. As a result, substances that can release H2 S in water, light, thiol, a comparable enzyme existence, as well as additional stimulants are frequently used in H2 S functional research (Zhao et al. 2014). Furthermore, the majority of donors’ discharge patterns could not

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Osmotic stress

ACC Oxidase Activity

LeACO1, LeACO2 gene expression

Ethylene

H2S

Stomatal Closure

Water Retention

Fig. 2 Depicting the role of H2 S in numerous plant functions

Ssulfhydration

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Regulation of ABC transporters

Regulation of Antioxidant system

Regulation of stomatal movement

Regulation of senescence

Reduced nutrient imbalance Hydrogen sulfide in plants

Increased biosynthesis of secondary metabolites

Root and shoot development

Increased survival rate

Interaction with other signaling Increased expression of stress-related genes

Accumulation of osmolytes

Modification in protein thiol groups

Fig. 3 Tomato ethylene production is downregulated by ethylene-induced H2 S

be measured, making exact application problematic. H2 S and its donors have been thoroughly researched and applied in medicine to date. Plant investigations have also been recorded, however, most of these are limited to the laboratories.

3 The Donors of H2 S H2 S unleashing agents, commonly known as H2 S donors, are chemicals that emit H2 S gas. The H2 S donors are useful for investigating their functions in regulating several metabolic and biochemical systems. Many H2 S donors were found or manufactured recently, including sodium hydrosulfide (NaHS), calcium sulfide, morpholin-4ium 4-methoxyphenyl(morpholino)phosphinodithioate (GYY4137), dialkyl dithiophosphate, NOSH-aspirin, diallyl trisulfide (DATS), and (10-oxo-10-(4-(3-(AP39). Because of its hydrolyzation, NaHS has been frequently employed in plant research because it establishes balancing between H2 S, HS–, and S2-ions instantly on mixing with water (Powell et al. 2018). Subsequently, H2 S is liberated directly and instantly from NaHS. When calcium sulfide is mixed with water, it produces hydrogen sulfide (H2 S) (Li et al. 2009). However, no evidence of its use as an H2 S donor in plants

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has been found. DATS is a diallyl thiosulfinate breakdown product that is reactive in aqueous systems. In the existence of glutathione, DATS produces the maximum amount of H2 S (Whiteman et al. 2008). Despite this, DATS’s application as H2 S donors is limited due to the chemical structure’s simplicity.

4 Highlights About Ethylene • Ethylene as a phytohormone plays important role in stomatal closure and leaf senescence • It also helps plants cope with environmental stresses by scavenging reactive oxygen species (ROS) • Ethylene improves sodium and metal ions resistance via regulating Na+ /K+ homeostasis • It’s also required for photosynthetic protection and adventitious roots. Cotyledons edema, amplification of the terminal hook bending, and suppression of hypocotyl and root extension are all part of the ethylene-induced triple response in dark-grown pea seedlings. The genetic apparatus essential for ethylene production, sensing, and signaling was identified because of this structural alteration (Merchante and Stepanova 2017). The diagnosis of ethylene mutants was based on this powerful triple response phenotype, which proceeded to the replication and profiling of essential ethylene-related genes (Bleecker and Kende 2000; Binder 2020). Three enzyme-catalyzed stages are involved in ethylene production in plants. SAM synthetases transform methionine to S-adenosylmethionine (SAM), then to 1-aminocyclopropane-1-carboxylic acid (ACC) by ACC synthases (ACS), and lastly to ethylene by ACC oxidases (ACO) (Adams and Yang 1979; Ververidis et al. 1991). Ethylene production is not limited to a single area of the whole plant body, and most, if not all, plant cells are thought to be capable of producing ethylene (Bleecker and Kende 2000). The total amount of ethylene generation is maintained artificially low under favorable growth conditions, although ethylene biosynthesis can be rapidly stimulated throughout specific developmental stages and in reaction to certain environmental stressors (Kende 1993; Xu and Zhang 2015). Consequently, the abundance of ethylene influences plants tolerance to these abiotic stressors at various layers of regulation (Husain et al. 2020). Ethylene, for example, encourages adventitious root production, controls stem and petiole development, and modulates stomatal opening to enhance salinity-induced distress resistance in plants (Druege 2006). In reaction to floodwaters and metal ion stresses, ethylene coordinates with the superoxide anion (ROS) responsive route to adjust metabolic reactions and antioxidant status, increasing plant survivability (Steffens 2014). Furthermore, by balancing photosynthetic and environmental stress reactions, ethylene fine-tunes crop development and health under unfavorable circumstances (Nazar et al. 2014; Sharma et al. 2019). To assist plants in dealing with abiotic stress, ethylene engrosses in complex interactions with heterogeneity of other phytohormones (Zhang et al.

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2021; Ku et al. 2018). It’s not unexpected that varied hormone levels produced by plants have indeed been revealed to participate and collaborate in numerous biological activities, notably abiotic stressors, given the increase in the number of published research relating to the subject of plant science in the previous 3 decades (Devireddy et al. 2020). Some of the hormone interactions occur at the transcriptional level, including the concerted response of a number of hormone controllers. Auxin: AUX; gibberellin: GA; cytokinin: CTK; strigolactone: SL; brassinolide: BR; and melatonin: MEL) are enhancers, while as, (abscisic acid: ABA; ethylene: ETH; salicylic acid: SA; and jasmonic acid: JA) are antagonists (Sytar et al. 2019). Plant progress is mostly stimulated by activator hormones, whereas plant progress is primarily inhibited by inhibitory hormones, which also react to unfavorable conditions. As a result, a combination of stimulators and inhibitory hormones regulates all physiological activities, including cell proliferation, seed germination, seedling formation, plant productivity, progress, and withering, besides reaction and adaptability to stressful conditions (He et al. 2019). Furthermore, phytohormones expertly manage the entire life cycle of plants, affecting not just crop plant output but rather the grade of agricultural goods (Fahad et al. 2015). Phytohormones are hence important in farming, forestry, and agricultural productivity. Phytohormones are widely regarded as the most important objective for increasing plant output and strain resistance (Ciura and Kruk 2018). Phytohormones play a significant act in several cellular passageways in vegetation (Jin and Pei 2015; Xuan et al. 2020), though, their intricate message routes, particularly when dealing with H2 S, are unknown. The core of the current section is to understand the mechanism of H2 S–Ethylene interplay in stressed plants, to encourage the explosive growth of H2 S and Ethylene combined studies in the plant science profession, and to lay the foundation for obtaining genetically altered crops with elevated yield, grade, and diverse stress responses.

5 The Interaction of H2 S with Inhibitor Hormones In so many species of plants, H2 S interacts with both stimulator and inhibitor hormones (such as ABA, ETH, SA, and JA). H2 S-moderated phytohormone signaling and phytohormone-moderated H2 S signaling are both involved in the interaction.

5.1 H2 S–Ethylene Interaction Plant organ development, maturation, senescence, stomatal mobility, and ecological stress reaction and adaptations are all influenced by ethylene, a gaseous phytohormone (Iqbal et al. 2017). As a volatile second messenger, H2 S plays its part in a spectrum of physiological and metabolic processes (Li et al. 2016b; Banerjeea et al. 2018). The aging of the tomato (Solanum lycopersicum L.) petiole and rose (Rosa

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rugosa) flowering apparatus, along with lily Anther dehiscence, was promoted by ethylene (Liu et al. 2020). Brownii lilium. Exogenous H2 S overturned the effects of Ethylene by bringing down the enzymatic activeness engaged in cell wall abatement (cellulase and polygalacturonase) through transcriptional quelling in place of unmediated post-translational alteration (sulfhydration) by H2 S (Liu et al. 2020). H2 S also influenced the expression of SlIAA3, SlIAA4, ILR-L3, and ILR-L4 (all of which are engaged in auxin signaling), preventing petiole abscission in tomato abscission region cells by altering the degree of free auxin (Liu et al. 2020). Flower component aging and Anther dehiscence (bursting) in rose and lily plants produced good findings (Liu et al. 2020). H2 S reacts with Ethylene and auxin during plant organ abscission, according to these studies. Exogenous ETH contributor (ethephon) enhanced the exercises of LCD and DCD in Arabidopsis and Vicia faba plants, ensuing in H2 S yield in guard cells and stomatal constriction. H2 S-synthesis antagonists (PAG) prevented ETH-induced stomatal closure (Liu et al. 2011a, b, 2012; Hou et al. 2013), implying that ETH-induced stomatal closure is facilitated by H2 S. Moreover, Arabidopsis DES1 mutants (with a reduced endogenous H2 S content) showed premature leaf withering, whereas NaHS administration reverted the aging and lengthened the shelf life of flowers by boosting endogenous H2 S contents (Alvarez et al. 2010; Zhang et al. 2011). H2 S-retarded aging has also been spotted in green leafy crops when ETH formation was inhibited (Al Ubeed et al. 2017). These findings imply that ETH enhances stomatal constriction and organ withering in plants by promoting and suppressing endogenous H2 S generation in plants independently. In plants, the enzymes 1-aminocyclopropane 1-carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO) are important for ETH production (Barry et al. 2000). By climacteric respiration (the disintegration of starch, chlorophyll, and cellular contents, along with the agglomeration of carotenoids), ETH could speed up the ripening process in climacteric fruits like tomato, banana (Musa spp.), apple (Malus pumila), and mango (Mangifera indica) (Gray et al. 1992; Johnson and Ecker 1998). Moreover, NaHS therapies inhibited ETH-induced peel discoloration and fruit cushioning in bananas by lowering polygalacturonase function, whereas NaHS and ethephon jointly stimulated the antioxidant status, together with entire phenolics and flavonoids, that lowered ROS levels and hence delayed chlorophyll debasement. Exogenous H2 S therapy reduced chilling-induced damage in banana fruits by decreasing ETH generation, MDA buildup, and ATP hydrolysis, while also stimulating H+ -ATPase, Ca2+ -ATPase, cytochrome c oxidase, and succinate dehydrogenase (Li et al. 2016a). This shows specifically that H2 S, through the downstream ETH signaling pathways, can defer the ripening process and strengthen freezing tolerance.

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6 Under Waterlogging Conditions, Exogenous H2 S Limits Ethylene Production in Peach Seedling Roots Juvenile fruit trees’ development and entering into productivity are hampered by waterlogging stress, while adult trees’ growth, output, and fruit quality are reduced (Penella et al. 2017). In the presence of hypoxia, aerobic respiration in the roots is impeded, and a massive amount of harmful chemicals, including ethanol and lactate, concentrate in the root system (Morard et al. 2000). Secondary stressors like oxygen shortage produced by high moisture content inhibited electrolyte transport in plant cells, and agglomeration of reactive oxygen species (ROS) that impair cellular membrane construction and operation are the major causes of plant damage from protracted poor drainage (Irfan et al. 2010). If plant tissues are subjected to protracted and/or severe moisture stress, a portion of the power delivered by incoming rays may well be rerouted into procedures that encourage the manufacturing of reactive oxygen species (ROS) like hydrogen peroxide (H2 O2 ) and superoxide anion (O2 ), resulting in the production of free radicals and affecting homeostatic mechanisms in cells as well as many other adverse outcomes of poor drainage within the plants. Nonetheless, plants can minimize oxidative damage by activating ROS-scavenging enzymes including superoxide dismutase (SOD) and catalase (CAT) (Tattini et al. 2015). The goal of this research was to see if H2 S could help peach trees recover from water deficit stress by controlling the antioxidative mechanism and ethylene production in their roots, as well as to generate a novel investigation proposal and a logical foundation for decreasing or eliminating waterlogging harm. H2 S pre-treatment has been found to significantly raise the performances of peroxidase (POD), SOD, CAT, and ascorbate peroxidase (APX) and decrease ROS production in plants responding to underwatering distress and cadmium poisoning tension (Sun et al. 2013; Shi et al. 2015). In pea seedlings, H2 S has indeed been demonstrated to decrease ethylene production while reducing oxygen deprivation root tip death (Cheng et al. 2013). Furthermore, H2 S is shown to be implicated in the ETH-triggered stomatal closure activity (Liu et al. 2011a, b). Exogenous H2 S has a favorable effect on physiological indices in herbaceous plants under waterlogging stress, according to these findings. However, the consequences of exogenous H2 S treatments in fruit tree species, particularly peach trees undergoing waterlogging pressure, have received little attention. Phytohormone, ethylene can govern numerous plant cell effective responses during waterlogging exposure, and hypoxia stress can induce its synthesis. As a result, the impact of exogenous H2 S on the amount of ethylene in peach seedling root systems undergoing waterlogging pressure was investigated. Waterlogging stress raised the ethylene biosynthesis rate and enhanced ethylene production in roots. Exogenous H2 S therapy considerably decreased the amount of ethylene in peach saplings’ root systems. The findings showed that exogenous H2 S suppressing ethylene generation in the root system could assist plants to adjust to a stunted oxygenic atmosphere produced by submergence distress.

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7 H2 S Produced by Ethylene Inhibits Ethylene Metabolism Under Osmotic Stress Fruit development, crop production, and environmental adjustments all require ethylene (Lacey and Binder 2014). Dry spells and mechanical damage, for example, cause a spike in ethylene accumulation in plant cells by increasing ethylene formation (Groen and Whiteman 2014). ACC synthases (ACSs) and ACC oxidases are involved in ethylene biosynthesis (ACOs). The rate-limiting enzymes of ethylene production have been recognized as ACOs (Bleecker and Kende 2000). A performance review and other signaling agents govern ethylene production. For instance, auxin has been found to increase ethylene manufacturing in Oryza sativa by decreasing ethylene synthase enzyme performance (Argueso et al. 2007; Zhu et al. 2006). H2 S has been linked to ethylene action regulation afresh. In kiwifruit, H2 S suppresses ethyleneinduced cell withering and reduces the influence of ethylene on banana fruit ripening (Ge et al. 2017). H2 S regulates ethylene biosynthesis, but the mechanism is unknown. Persulfidation, or the post-translational alteration of Cys residues to generate a persulfide group, is the working assumption (cysteine –SH groups are converted to –SSH). Endogenous H2 S persulfidation controls the action of several proteins, like ascorbate peroxidase1 and glyceraldehyde 3-phosphate dehydrogenase, according to new data (Aroca et al. 2015, 2017b). Persulfidation has also been observed in Arabidopsis in vivo, suggesting that AtACO1 may be amongst the numerous peptides that can only be altered through this manner (Aroca et al. 2017a). As a result, tomato ACOs were exposed to H2 S-induced persulfidation in order to figure out how H2 S influences ethylene signaling triggered by osmotic pressure. Tomatoes were used in the research since their osmotic hypersensitivity has been highlighted as a significant obstacle in producing higher effectiveness of this essential crop.

8 Ethylene-Induced Stomatal Sealing Necessitates H2 S H2 S signal frequently engages with phytohormones or signaling molecules to influence a variety of physiological activities (Scuffi et al. 2014; Jin and Pei 2015). H2 S has long been suspected to play a role in Arabidopsis stomatal closure caused by ABA or ETH (Liu et al. 2011a, b). H2 S production can be controlled by ABA or ethylene. Ethylene is found to cause H2 S generation in tomatoes, comparable to what has been reported in Arabidopsis and Vicia faba (Liu et al. 2011a, b, 2012). Notably, stomatal activation in reaction to osmotic stress appears to be dependent on H2 S signaling, as it can be blocked by using an H2 S absorber or inhibitor. When H2 S activity is suppressed, ethylene is inadequate to promote stomatal closure, according to pharmacological research. These results clearly showed that H2 S is a key messenger component in the ethylene signaling, at least in guard cells’ water stress reaction.

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9 Persulfidation of LeACO1 and LeACO2 by H2 S Governs Feedback Monitoring of Ethylene Production The very last, rate-limiting stage of ethylene production is regulated by 1aminocyclopropane-1-carboxylic acid oxidases (Argueso et al. 2007). ACO activity has been found to have a direct impact on endogenous ethylene levels (Groen and Whiteman 2014). Plant signaling chemicals, like nitric oxide, have been shown to influence ACO activity (Tierney et al. 2005; Zhu et al. 2006). H2 S reduces ethylene activity in banana fruit maturation and withering, according to the theory (Ge et al. 2017). As a result, H2 S may be resistant to ETH’s functionality. During osmotic stress, H2 S hindered ETH production, according to the results of an investigation. During osmotic stress, H2 S also was reported to reduce the generation of ethylene likely due to the suppression of ACO functioning. The persulfidation of one particular cysteine residue in the LeACO proteins was discovered to be responsible for this control. The protein tyrosine phosphatase PTP1B (Krishnan et al. 2011) and a phosphodiesterase have both been shown to be negatively regulated by H2 Sinduced persulfidation (Bucci and Cirino 2011). Furthermore, when compared to LeACO1WT, LeACO1C60S was unresponsive to NaHS therapies, implying that the Cys60 is the active plot of H2 S-prompted persulfidation (Fig. 2).

10 Through an Intervening Medium, H2 S Suppresses the Expression of the Ethylene Biosynthetic Pathway The ethylene biosynthesis pathway’s transcriptional regulation has an impact on ethylene signaling. These genes’ transcription can be altered by phytohormones, signaling molecules, and environmental stress, counting ethylene fundamentally (Wang et al. 2002). During osmotic stress, H2 S-treated plants had lower levels of LeACO1 and LeACO2 expression than the untreated plants, which is likely owing to H2 S-instigated suppression of ACO action. This diminishes ethylene concentration and, as a result, the previously documented favorable ethylene biogenesis management (Jakubowicz et al. 2010). Ethylene is a stress hormone that increases plant resistance in reaction to oxidative stress (Bleecker and Kende 2000). Moreover, elevated Ethylene concentration caused cell withering and apoptosis (Lacey and Binder 2014). As a result, the management of ETH biosynthesis is critical for the plants facing stress. H2 S feedback modulates Ethylene production in tomatoes under osmotic stress, according to a new study. Ethylene increases the build-up of H2 S in guard cells, according to the research. In ethylene-induced stomatal closure, H2 S serves a dual role. Ethylene-prompted H2 S is essential for Ethylene-instigated stomatal constriction on the one extreme. The persulfidation of LeACO1 and LeACO2 by ethylene-induced H2 S, on the contrary,

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inhibits ethylene production. H2 S may regulate Ethylene production directly by posttranslational alteration of ACOs. Furthermore, H2 S indirectly suppresses the expression of the Ethylene biosynthetic pathway. Altogether, the work provides concrete proof for the coupling of ethylene and H2 S, and these findings are critical in the bioengineering development of osmotic stress-tolerant tomato plants.

11 H2 S-Ethylene: Vital for Hexavalent Chromium Stress Prevention For plants to operate pharmacologically, chromium metal is not required. The principal source of Cr invading the food supply chain is chromium-contaminated sediments (Rebhi et al. 2019). Hexavalent [Cr (IV)] and trivalent [Cr (III)] Cr (III) Cr (IV) Cr (III) Cr (III) Cr (Cr oxidation states are found in both marine and land habitats (Santos et al. 2009; Joanna et al. 2010), albeit their mobility, bioavailability, and toxicity vary (Panda and Choudhury 2005). The growth of plants, fresh biomass, photosynthetic qualities, and enzyme function are all influenced by Cr stress (Gill et al. 2015). An overabundance of reactive oxygen species (ROS) and their detrimental effect on lipids explain Cr’s phytotoxicity (Ali et al. 2015; Sytar et al. 2018). Harmful impacts of Chromium decrease the availability of micronutrients like salt, iron, manganese, copper, zinc, and calcium, as well as alter metabolic reactions, resulting in significant yield and yield component losses (Zhao et al. 2019). Crops must be protected from Cr stress and toxicity for these purposes. Accelerated ethylene (ETH) production speeds up the activation of ETH-related synthetic pathways, and their transcription rises in reaction to heavy metal stress (Husain et al. 2020; Nguyen et al. 2021; Adrees et al. 2015; Maksymiec and Krupa 2007). Heavy metal exposure is one of several abiotic and biotic stress processes involving ethylene (Khan et al. 2020; Liu et al. 2021). The importance of ethylene in plants is linked to its availability, and it is responsible for better stress resistance (Dubios et al. 2018).

12 Under Cr (VI) Stress, Ethylene and H2 S Significantly Control Growth Characteristics Cr has been found to have a major impact on some crop species, including Oryza sativa (Hussain et al. 2018), Pisum sativum (Rodriguez et al. 2012), Triticum aestivum (Ali et al. 2015), and Brassica napus (Ali et al. 2015; Gill et al. 2015). Since Cr upsets the nutritional status of plants, developmental problems may be connected to nutritional deficiencies (Ali et al. 2013a, b). Abundant Cr engendered histologic remodeling in Brassica napus (Gill et al. 2015) and Oryza sativa (Hussain et al. 2018). It was also found that the incorporation of sulfur and calcium into tomato and brinjal reduced the adverse effects of Cr (VI) (Singh et al. 2020). Both H2 S and

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Ethylene are beneficial to plant growth by reducing Cr (VI) toxicity, according to research into the impact of Cr (VI) toxicity on root and shoot lengths in black beans and mung beans (VI). Since AVG inhibits the production of endogenous Ethylene, it reduced the length of either the shoot or the root in black bean and mung bean in this investigation, showing that Chromium toxicity was enhanced. Additionally, PAG with Ethylene therapy decreased shoot and root lengths in both experimental crops when contrasted with untreated. Regardless of the fact that PAG inhibits endogenous H2 S production, these data show that Ethylene singly cannot ameliorate Cr (VI) lethality in investigational seedlings, showing that both Ethylene and H2 S are needed. In addition, when AVG was mixed with NaHS (an H2 S donor), black bean and mung bean root and shoot growth were reduced compared with the control. This demonstrates that in both pulse crops, H2 S is a downstream signal of ethylene that helps to alleviate Cr (VI) stress (Husain et al. 2021).

13 Ethylene and H2 S During Cr (VI) Stress Regulate Sulfur Absorbing Enzymes and Cysteine Concentration Under abiotic stress, sulfur assimilation is crucial (Fatma et al. 2016). The consequence of sulfur absorption, cysteine, is crucial for the production of antioxidants through abiotic stress (Gill and Tuteja 2011). When contrasted with control, in the leaf and root of black beans and mung beans, Cr (VI) solely increased ATP sulfurylase and O-acetylserine (thiol) lyase performance. Furthermore, after utilizing AVG and PAG, both pulse crops showed a considerable decrease in ATP sulfurylase and O-acetylserine (thiol) lyase function. In the roots and leaves of black bean and mung bean, AVG and PAG possessing Cr (VI) correspondingly inhibited ATP sulfurylase expression. Despite alike circumstances, the activity of oacetylserine (thiol) lyase was lowered in the leaves and roots of black beans and mung beans. ATP sulfurylase and Oacetylserine (thiol) lyase activities were dramatically boosted either by Ethylene or H2 S. Ethylene and PAG, on the other hand, greatly suppressed the efficiency of ATP sulfurylase and O-acetylserine (thiol) lyase in contrast to the untreated. In the dearth of endogenous H2 S, Ethylene cannot effectively treat Cr (VI) toxicity. When contrasted to untreated, H2 S with AVG increased the efficiency of ATP sulfurylase and O-acetylserine (thiol) lyase mostly in leaves and roots of black bean and mung bean, correspondingly. These data suggest that H2 S is essential for Ethylene to function adequately in both pulse crops while reducing Cr (VI) cytotoxicity. The performances of ATP sulfurylase and O-acetylserine (thiol) lyase were identical in the leaves and roots of black bean and mung bean plants (Husain et al. 2021). Salicylic acid modulates the sulfur absorption pathway in mung bean seedlings during salt stress (Nazar et al. 2011).

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14 During Cr (VI) Stress, Ethylene and H2 S Regulate Proline Biosynthesis Management of proline biosynthesis is crucial during abiotic stress adaption (Saibi et al. 2015). Ethylene and H2 S treatment were used to investigate the involvement of proline biosynthesis in Cr (VI) stress resistance, researchers measured proline buildup and activities of metabolizing, such as D1-pyrroline-5-carboxylate synthase and proline dehydrogenase. D1-pyrroline-5-carboxylate synthase activities and proline availability rose marginally in Cr (VI)-distressed crop plants. The incorporation of ethephon to Cr (VI) treatment, together with H2 S, significantly increased D1pyrroline-5-carboxylate synthetase proline material and efficiency. Ethephon and NaHS enhanced the effectiveness of D1-pyrroline-5-carboxylate synthetase in the leaves and roots of black bean and mung bean, correspondingly. The function of D1pyrroline-5-carboxylate synthetase was reduced after administering AVG or PAG with Cr (VI) to the leaves and roots of black bean and mung bean, correspondingly. ET with PAG decreased D1-pyrroline-5-carboxylate synthetase activity in black bean and mung bean leaves and roots, correspondingly, when compared with control. Nevertheless, when H2 S was mixed with AVG, D1-pyrroline-5-carboxylate synthetase activity was dramatically boosted when compared to the control. Although both Ethylene and H2 S influence proline production and D1-pyrroline-5-carboxylate synthase activity, H2 S is necessary. In contrast to proline and D1-pyrroline-5carboxylate synthetase, proline dehydrogenase action was mildly suppressed by Cr (VI) stress. In addition, mixing Ethylene and H2 S with Cr (VI) re-established proline dehydrogenase regulations. Moreover, when AVG or PAG were independently introduced to Cr (VI) treatment, proline dehydrogenase activity was reduced very far (Husain et al. 2021). The findings obtained stipulate that proline dehydrogenase action may be lowered in order to protect against Cr (VI) stress by preserving endogenous proline concentrations. Similar findings were made in mustard seedlings during Ni stress, rice seedlings during herbicide stress, and tomato and aubergine seedlings during Cr (VI) stress (Khan et al. 2020; Tripathi et al. 2020; Singh et al. 2020).

15 During Cr (VI) Stress, Ethylene and H2 S Reduce Oxidative Stress Indicators Toxic metal-mediated ROS generation and oxidative stress are the causes of metal poisoning (Berni et al. 2019). Plants are more susceptible to oxidative stress and lipid peroxidation when exposed to Cr (VI) (Singh et al. 2021). In comparison to controls, Cr (VI) treatment significantly elevated superoxide radical and H2 O2 buildup in the roots and leaves of black bean and mung bean respectively. Moreover, upon using both ethephon (donor of ethylene) and NaHS, superoxide radicals and H2 O2 concentrations in both pulse species reduced dramatically (donor of H2 S).

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When Ethylene was sprayed on the leaves and roots of black bean and mung bean, superoxide radicals and H2 O2 were reduced. The number of superoxide radicals and H2 O2 in both pulse species decreased considerably after NaHS injection, although more than with Ethylene. These data imply that Ethylene and H2 S reduce the levels of ROS among each pulse crop, even during Cr (VI) distress. When compared to Cr (VI), however, AVG and PAG significantly enhanced ROS, suggesting that endogenous Ethylene and H2 S are essential to reduce ROS levels during Cr (VI) stress. Moreover, investigators used Cr (VI) + ET + PAG and Cr (VI) + NaHS + AVG to see if there was any interplay between Ethylene and H2 S in the reduction of Cr (VI) stress. They detected high quantities of superoxide radicals and H2 O2 in both species’ shoots and roots after treatment with Cr (VI) + ETH + PAG. This implies that ethylene is not capable of diminishing ROS concentration in the absence of endogenous H2 S (Husain et al. 2021). Several investigations, including (Ashraf et al. 2021) in okra (Yildiz and Terzi 2021) in mustard (Singh et al. 2021) in tomato and brinjal, and (Singh et al. 2021) in Glycine max, have shown that metal causes the formation of oxidative stress indicators.

16 Crosstalk Between H2 S and Other Phytohormones Phytohormones are essential to plant growth and development enhancers. H2 S interacts strongly with the plant hormone Ethylene as well as ABA, auxin, SA, GA, and JA in the maturing stages of plants during regular and high-stress situations, according to numerous studies.

17 Crosstalk of H2 S with Abscisic Acid Seed dormancy, plant withering, and ABA are all engaged in plant developmental processes, and even drought stress response (Cutler et al. 2010). According to a recent survey, ABA can promote the gene function and enzymatic activity of LCD/DES1, which is involved in the production of H2 S (Jin and Pei 2016). Furthermore, the build-up of H2 S caused by ABA promotes SnRK2.6 activity via S-sulfhydration of SnRK2.6 at Cys131 and Cys137, which improves SnRK2.6-ABF2 interaction. As a result of the S-sulfhydration of SnRK2.6, H2 S has a beneficial function in the control of ABA-elicited stomatal constriction (Chen et al. 2020). The mutants lcd, aba3, and abi1 were examined to determine the intimate link between H2 S and ABA during dry circumstances. Water deficit was more severe in the lcd mutant, and ABA-mediated stomatal constriction was less effective. This was due to a rise in inward-rectifying K+ and anion channel coding genes, as well as a reduction in the stimulation of Ca2+ and outward-rectifying K+ channel coding genes. As LCD transcription and H2 S generation rate reduced, the stomatal aperture was increased in both the aba3 and abi1 mutants. Surprisingly, NaHS administration

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corrects all of the aforementioned abnormalities, suggesting that H2 S is involved in the ABA-regulated stomatal response to water deficit via ion channels (Jin et al. 2013). Furthermore, (Li et al. 2016a, b) discovered that ABA administration boosted LCD performance in nicotine units at elevated temperatures and that NaHS treatment improved ABA-induced thermal dissipation by lowering MDA concentration and electrolyte leakage. The introduction of an H2 S scavenger or a particular blocker of H2 S production decreased the influence of different H2 S or ABA treatments, indicating a synergic activity among H2 S- and ABA-facilitated heat defenses of tobacco suspension-cultured cells (Li et al. 2016a, b). More research has found that H2 S caused the E3 ligase COP1 to concentrate in the nucleus, leading to the disintegration of HY5 and a drop in ABI5 activation, resulting in the reduction of ABA concentration and improved seed germination at intense heat (Chen et al. 2019). Therefore, it’s thought that H2 S may work in tandem with ABA signaling to improve plant resistance to water deficit by stimulating Ca2+ signaling and inward-rectifying K+ channels. By lessening oxidative injury and governing the ABA-related genes in response to temperature exhaustion, H2 S collaborates with ABA signaling to improve seed sprouting and development.

18 H2 S and Auxin Crosstalk Auxin influences a plant’s development and health at varying phases, integrating plant growth and form in reaction to the external environment (Zhao et al. 2009). NaHS treatment significantly increased auxin concentration and boosts the quantity and length of adventitious roots throughout lateral root growth, indicating that H2 S and auxin may have a close relationship (Zhang et al. 2009a, b). Auxin generally suppresses organ abscission, and later research revealed that H2 S frequently upregulates the IAA/auxin family genes (IAA3 and IAA4) (Liu et al. 2020). H2 S is thought to operate as an upstream regulator of NO and IAA, promoting root hair formation or preventing organ abscission (Zhang et al. 2009a, b). Both NAA and NaHS can offset auxin deficiency’s impacts on SlDES1 transcription, DES1 function, and endogenous H2 S levels, as well as the activation of lateral roots caused by auxin depletion (Fang et al. 2014). These findings show that there may be H2 S-auxin feedback regulation during plant growth. During the pathogen response in plants, H2 S suppresses the production of auxin signaling F-box proteins 1 (AFB1), 2 (AFB2), and 3 (AFB3) (Shi et al. 2015). The implementation of NaHS to cucumber seedlings causes the activation of flavin monooxygenase (FMO) and the comparative affirmation of the FMO-like protein YUCCA2, resulting in an increase in intrinsic IAA and enhanced cold tolerance, as evidenced by lessened electrolyte drainage and ROS build-up, as well as increased regulation of gene expression and photosynthetic enzyme activity. IAA or H2 S elimination had no influence on the other particle’s signaling, NPA, an antagonist of IAA polar transport, suppressed H2 S-stimulated chilling resistance and response gene regulation (Zhang et al. 2009a, b). As a downdrift signaling molecule, IAA

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contributes to H2 S-induced stress tolerance in plants, whereas H2 S increases auxin signaling pathways by influencing the activation of auxin-linked genes and the production of auxin, boosting crop resistance to external strains.

19 Crosstalk of H2 S with Gibberellin GA has the ability to control several elements of plant development and growth, including seed sprouting, leaf proliferation, and blooming (Achard and Genschik 2009). GA can help break seed dormancy by stimulating the manufacturing of Amylase and certainly secreted hydrolases during seed germination. H2 S increases the action of amylase and speeds up the sprouting percentage of barley seeds in the presence or in the absence of GA, however, cells without GA have a greater survival rate than those with GA. It’s thought that the stimulation of -amylase by H2 S occurs first, followed by the excitation of -amylase by GA, both of which can subsequently digest starch and give sugar for seedling growth and development (Zhang et al. 2010). GA stimulates PCD in the wheat aleurone layer, and during this time, both LCD action and H2 S manufacturing are reduced (Xie et al. 2014). Intriguingly, NaHS not only suppresses the formation of endogenous H2 S but also reduces the PCD caused by GA. Since NaHS produces an elevation in endogenous GSH amount, and an inhibitor of GSH synthesis eliminates NaHS-mediated PCD, it was hypothesized that this reversal is linked to GSH (Xie et al. 2014). As a result, the interrelation between H2 S and GA is most probably indirect via GSH homeostasis control.

20 Crosstalk of H2 S with Salicylic Acid SA is a phenolic derivative present abundantly in plants that may be transferred through the phloem and has a variety of functions, including disease resistance, water deficit tolerance, and hotness resistance (Raskin 1992). According to researchers, SA administration improves LCD function and leads to the formation of endogenous H2 S throughout maize seedling heat tolerance reactions (Li et al. 2015). The inclusion of NaHS increases the temperature sensitivity caused by SA, while the introduction of an H2 S-metabolism inhibitor (PAG) or scavenger decreases it (HT). Furthermore, critical SA production enzymes and endogenous SA content were unaffected. These findings suggest that H2 S is found downstream of SA and collaborates with it to help plants withstand heat stress.

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21 H2 S and Jasmonate Interactions In higher plants, JA is an essential endogenous modulator that regulates the progressive stages of plants and supports plant shielding reactions to environmental stresses (Devoto and Tuner 2003; Balbi and Devoto 2008). In Arabidopsis, the transcription factors JA and JASMONATE INSENSITIVE (JIN/MYC) are important regulators of stomatal development (Han et al. 2018). In the JA-signaling-deficient myc234 mutant, removing H2 S expanded the number of stomata inhibited by JA, while applying NaHS reduced the stomatal inhibition. H2 S inhibits critical elements of the stomatal signaling pathway, including TOO MANY MOUTHS (TMM), STOMATAL DENSITY AND DISTRIBUTION1 (SDD1), and SPEECHLESS, by reducing the transcription of stomata-correlated genes and blocking essential constituents of the stomatal signaling pathway (SPCH). LCD mutations boosted stomatal density and index values, and an H2 S synthesis inhibitor (HT) hinders JA-induced stomatal density loss (Deng et al. 2020). These findings together show that H2 S is found downstream of JA and works together with it to suppress stomatal growth.

22 Conclusion and Perspective It is obvious that H2 S has a function in stress relief through both endogenous and exogenous generation. According to the literature, the synthesis of H2 S is stimulated by abiotic and biotic stresses, which protect against stress-induced damage and may potentially contribute to disease prevention. H2 S–phytohormone interplay can boost plant tolerance to Cd, boron, salt, and iron under insufficient pressure in stressful conditions. Crosstalk between H2 S and inhibitor hormones like ABA, ETH, SA, and JA can alter stomatal progress and closure, organ maturation and wither (and even abscission), and strain resistance in plants, including high temperatures, cold stress, water stress, and Cd sensitivity, during a natural and stressful experience. As a result, because the processes of H2 S and phytohormones are frequently interconnected by their interplay, the communication of H2 S and phytohormones should be regarded when studying the effects of H2 S and/or plant hormones on metabolic responses under regular and stressed situations. Furthermore, during natural and stressful settings, the interplay of H2 S with some additional plant hormones (such as CTK, SL, and BR) plant hormones interplay (encompassing stimulators and inhibitors) is ambiguous, and more research is needed. Notably, the involvement of H2 S in the charge of hormone signaling through translation and post-translational modifications (such as persulfdation), and hormone metabolism are still unknown. In addition, employing physical, chemical, genomic, molecular, omics, and multiple-omics techniques, the detailed molecular mechanism of H2 S interactions with activator and suppressor plant hormones under natural and stressed circumstances should be addressed in the upcoming especially.

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