Plant Hormones and Climate Change 9811949409, 9789811949401

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Golam Jalal Ahammed Jingquan Yu Editors

Plant Hormones and Climate Change

Plant Hormones and Climate Change

Golam Jalal Ahammed • Jingquan Yu Editors

Plant Hormones and Climate Change

Editors Golam Jalal Ahammed Department of Horticulture, College of Horticulture and Plant Protection Henan University of Science and Technology Luoyang, Henan, China

Jingquan Yu Department of Horticulture Zhejiang University Hangzhou, China

ISBN 978-981-19-4940-1 ISBN 978-981-19-4941-8 https://doi.org/10.1007/978-981-19-4941-8

(eBook)

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

“I dedicate this book to the memory of my late father Golam Rosul, who passed away recently in August 2021.” -Golam Jalal Ahammed

Preface

Drought, heat, cold, salinity, flooding, nutrient deficiency, and greenhouse gas emissions are all being exacerbated with the unprecedented climate change, leaving global food security at risk. Phytohormones are endogenous messenger molecules that play a crucial role in plant growth, development, and stress response throughout their life cycle. Extensive research on phytohormones with groundbreaking discoveries has provided a better understanding of how these hormones work physiologically and molecularly, although the precise biological mechanisms and many biochemical, physiological, and molecular pathways that contribute to greater stress tolerance are still unknown. Over the past decades, major components of most hormone signaling pathways have been identified and characterized. There is mounting evidence that certain hormone-signaling components serve as a critical convergence point of crosstalk between endogenous and environmental signals. Nonetheless, plant hormone signal crosstalk is more complex than previously thought, and thus more research efforts are needed to address many unresolved puzzles. In light of the fact that exogenous application or genetic manipulation of phytohormones can improve crop yield under favorable and/or unfavorable climatic conditions, the use of plant hormones and growth regulators is very important for sustainable crop production in the era of climate change. Since the publication of our first book on plant hormones and stress response in 2016 by Springer, related literature has been supplemented by a wealth of empirical data in the context of climate change. Thus a new book is needed to address a wide audience of plant science, including researchers and advanced university students, in order to cover the most current advances in plant hormone research on growth regulation and stress response. This book aims to give readers with a current account of plant hormonemediated responses to abiotic stressors, which could have potential implications in ensuring food security in the face of climate change. The present book is composed of 14 chapters on various aspects of plant growth, development, and stress response. There are individual chapters dedicated to addressing specific climate change drivers or associated factors including high CO2, O3, high temperature, cold, drought, vii

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flooding, soil acidity, acid rain, nutrient deficiency, and heavy metal stress in plants. The book provides new insights into our understanding of the mechanisms of phytohormone-mediated growth regulation and stress tolerance covering the most recent biochemical, physiological, genetic, and molecular studies. Despite a few minor emendations, the authors' entire premise was preserved in every chapter. However, it is indeed possible that there are still some flaws in the book, so any input from readers would be greatly appreciated for future editions. We would like to thank all the authors who contributed to this book. Thank you to Springer, especially the in-house editors and production staff involved in this book project, for your gracious assistance in completing this project! Luoyang, Henan, China Hangzhou, China

Golam Jalal Ahammed Jingquan Yu

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant numbers 31950410555, 31550110201); Ministry of Science and Technology of the People’s Republic of China (grant numbers DL2022026004L, QNJ2021026001, QNJ20200226001); and Henan University of Science and Technology Research Start-up Funds for New Faculty (grant numbers 13480058, 13480070).

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Contents

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Introduction to Plant Hormones and Climate Change . . . . . . . . . . . Golam Jalal Ahammed, Xin Li, and Jingquan Yu

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The Complex Interaction Between Elevated CO2 and Hormones on the Control of Plant Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . Karla Gasparini, Fred A. L. Brito, Lázaro E. P. Peres, Dimas M. Ribeiro, and Agustin Zsögön

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Role of Plant Hormones in Plant Response to Elevated CO2 Concentrations: Above- and Below-ground Interactions . . . . . . . . . Estibaliz Leibar-Porcel and Ian C. Dodd

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The Intriguous Roles of Phytohormones in Plant Response to Ozone Interacting with Other Major Climate Change Stressors . . . Alessandra Marchica and Elisa Pellegrini

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Role of Phytohormones in Plant Responses to Acid Rain . . . . . . . . . Biswojit Debnath, Masuma Zahan Akhi, Md. Mahfuzur Rob, Ashim Sikder, Md. Masudur Rahman, Md. Shahidul Islam, Animesh Chandra Das, Manna Salwa, Delara Akhter, Xin Li, and Golam Jalal Ahammed

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The Role of Plant Hormones in Fruit Response to Photooxidative and Heat Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 Carolina A. Torres and Carlos R. Figueroa

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Phytochrome and Hormone Signaling Crosstalk in Response to Abiotic Stresses in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145 Marina Alves Gavassi, Frederico Rocha Rodrigues Alves, and Rogério Falleiros Carvalho

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Phytohormone-Mediated Regulation of Heat Stress Response in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 Sylva Prerostova and Radomira Vankova

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Phytohormones and Cold Stress Tolerance . . . . . . . . . . . . . . . . . . . 207 Joanna Lado, Florencia Rey, and Matías Manzi

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Drought Stress: Involvement of Plant Hormones in Perception, Signaling, and Response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227 Sasan Aliniaeifard, Maryam Rezayian, and Seyed Hasan Mousavi

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Involvement of Phytohormones in Flooding Stress Tolerance in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251 Xiaohua Qi, Zhongyuan Hu, Xuehao Chen, Mingfang Zhang, and Mikio Nakazono

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Roles of Long-Distance Signals in Nitrogen, Phosphorus, and Sulfur Uptake and Sensing in Plants . . . . . . . . . . . . . . . . . . . . 273 Masato Shindo and Mikihisa Umehara

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Phytohormone Involvement in Plant Responses to Soil Acidity . . . . 301 Marjorie Reyes-Díaz, Jorge González-Villagra, Elizabeth Maria Ulloa-Inostroza, Mabel Delgado, Claudio Inostroza-Blancheteau, and Alexander Gueorguiev Ivanov

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Plant Response to Toxic Metals: Emerging Sources, Phytohormone Role, and Tolerance Responses . . . . . . . . . . . . . . . . 325 Marina Alves Gavassi, Brenda Mistral de Oliveira Carvalho, Anna Carolina Gressler Bressan, and Gustavo Habermann

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369

Editor and Contributors

About the Editors Golam Jalal Ahammed is an Associate Professor at the Department of Horticulture, College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang, China. He obtained his B.Sc. in Agriculture in 2004 and M.S. in Horticulture in 2006 from Bangladesh Agricultural University, Mymensingh, Bangladesh. Dr. Ahammed received a Ph.D. in Olericulture with a major focus on Plant Stress Physiology and Hormonal Regulation in 2012 from Zhejiang University, China. Afterward, he completed two consecutive postdoctoral programs at the Institute of Pesticide and Environmental Toxicology and the Institute of Crop Science of Zhejiang University. His major research interests include plant stress physiology, phytohormones, climate change effects on plants, and environmental pollution. Dr. Ahammed authored over 150 papers in peer-reviewed journals. He is a Senior Editorial Board Member of Scientific Reports and an Associate Editor of AoB Plants, BMC Plant Biology, and Journal of Plant Growth Regulation. Dr. Ahammed was awarded several research grants by the National Natural Science Foundation of China, the Ministry of Science and Technology of China, and the China Postdoctoral Science Foundation.

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Jingquan Yu is an Academician of the Chinese Academy of Engineering, a Professor of Horticulture at Zhejiang University, Hangzhou, China, and the Director of the Key Laboratory of Horticultural Plants Growth, Development, and Quality Improvement, Agricultural Ministry of China. He completed his M.Sc. in Agrochemistry in 1991 from Shimane University, Japan, and Ph.D. in Bio-resource Chemistry in 1994 from Tottori University, Japan. Afterward, he worked as a postdoc scientist at Shimane University. In 1995, he returned to China and joined Zhejiang University. His fields of specialization include plant hormones, systemic signaling, plant growth regulation, allelopathy, and monocropping obstacle. Prof. Yu is one of the leading scientists in the area of vegetable research. He was awarded a number of honors such as Excellent Youth Instructor, Yangtze River Scholar, National Natural Science Award, Science and Technology Advancement Award, Science and Technology Advancement Award of Zhejiang Province, National Outstanding Youth Scholar, and so on. He has been serving as an editor for several domestic and international journals. He authored more than 200 articles in peer-reviewed journals. Prof Yu is one of the highly cited researchers in 2020 and 2021 (Clarivate-Web of Science).

Contributors Golam Jalal Ahammed Department of Horticulture, College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang, Henan, China Masuma Zahan Akhi Department of Horticulture, Sylhet Agricultural University, Sylhet, Bangladesh Delara Akhter Department of Genetics and Plant Breeding, Sylhet Agricultural University, Sylhet, Bangladesh Sasan Aliniaeifard Photosynthesis Laboratory, Department of Horticulture, Aburaihan Campus, University of Tehran, Tehran, Iran Frederico Rocha Rodrigues Alves Department of Botany, Federal University of Goiás (UFG), Campus Goiânia, Goiânia, GO, Brazil

Editor and Contributors

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Anna Carolina Gressler Bressan Department of Biodiversity, Biosciences Institute, São Paulo State University, Rio Claro, São Paulo, Brazil Fred A. L. Brito Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, Brazil Brenda Mistral de O. Carvalho Department of Biodiversity, Biosciences Institute, São Paulo State University, Rio Claro, São Paulo, Brazil Rogério Falleiros Carvalho Biology Applied to Agriculture Department, São Paulo State University (FCAV/UNESP), Campus Jaboticabal, Jaboticabal, SP, Brazil Xuehao Chen Department of Horticulture, School of Horticulture and Plant Protection, Yangzhou University, Yangzhou, Jiangsu, People’s Republic of China Animesh Chandra Das Department of Horticulture, Sylhet Agricultural University, Sylhet, Bangladesh Biswojit Debnath Department of Horticulture, Sylhet Agricultural University, Sylhet, Bangladesh Mabel Delgado Laboratory of Molecular and Functional Ecophysiology of Plants, Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco, Chile Ian C. Dodd Lancaster Environment Centre, Lancaster University, Lancaster, UK Carlos R. Figueroa Millennium Nucleus for the Development of Super Adaptable Plants (MN-SAP), Santiago, Chile Karla Gasparini Laboratory of Plant Developmental Genetics, Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, SP, Brazil Marina Alves Gavassi Department of Biodiversity, Biosciences Institute, São Paulo State University (IB/UNESP), Rio Claro, SP, Brazil Jorge González-Villagra Departamento de Ciencias Agropecuarias y Acuícolas, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile Gustavo Habermann Department of Biodiversity, Biosciences Institute, São Paulo State University, Rio Claro, São Paulo, Brazil Zhongyuan Hu Laboratory of Germplasm Innovation and Molecular Breeding, Institute of Vegetable Science, Zhejiang University, Hangzhou, People’s Republic of China Claudio Inostroza-Blancheteau Departamento de Ciencias Agropecuarias y Acuícolas, Facultad de Recursos Naturales, Universidad Católica de Temuco, Temuco, Chile

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Md. Shahidul Islam Department of Horticulture, Sylhet Agricultural University, Sylhet, Bangladesh Alexander Gueorguiev Ivanov Department of Biology and The Biotron Centre for Experimental Climate Change Research, Western University, London, ON, Canada Joanna Lado Instituto Nacional de Investigación Agropecuaria (INIA), Salto, Uruguay Estibaliz Leibar-Porcel Lancaster Environment Centre, Lancaster University, Lancaster, UK Xin Li Key Laboratory of Tea Quality and Safety Control, Ministry of Agriculture and Rural Affairs, Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, People’s Republic of China Matías Manzi Fertilidad de Suelos, Estación Experimental Facultad de Agronomía Salto (EEFAS), Facultad de Agronomía, Universidad de la República, Salto, Uruguay Alessandra Marchica Department of Agriculture, Food and Environment, University of Pisa, Pisa, Italy Seyed Hasan Mousavi Vegetable Research Center, Horticultural Sciences Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran Mikio Nakazono Graduate School of Bioagricultural Science, Nagoya University, Nagoya, Japan Elisa Pellegrini Department of Agriculture, Food and Environment, University of Pisa, Pisa, Italy Lázaro E. P. Peres Laboratory of Plant Developmental Genetics, Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, SP, Brazil Sylva Prerostova Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany, Czech Academy of Sciences, Prague, Czech Republic Xiaohua Qi Department of Horticulture, School of Horticulture and Plant Protection, Yangzhou University, Yangzhou, Jiangsu, People’s Republic of China Md. Masudur Rahman Department of Crop Botany and Tea Production Technology, Sylhet Agricultural University, Sylhet, Bangladesh Marjorie Reyes-Díaz Laboratory of Molecular and Functional Ecophysiology of Plants, Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco, Chile Florencia Rey Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC), Valencia, Spain

Editor and Contributors

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Maryam Rezayian Department of Plant Biology, School of Biology, College of Science, University of Tehran, Tehran, Iran Dimas M. Ribeiro Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, Brazil Md. Mahfuzur Rob Department of Horticulture, Sylhet Agricultural University, Sylhet, Bangladesh Manna Salwa Department of Horticulture, Sylhet Agricultural University, Sylhet, Bangladesh Masato Shindo Graduate School of Life Sciences, Toyo University, Itakura-machi, Ora-gun, Gunma, Japan Ashim Sikder Department of Agroforestry and Environmental Science, Sylhet Agricultural University, Sylhet, Bangladesh Carolina A. Torres Horticulture Department, Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA, USA Elizabeth Maria Ulloa-Inostroza Laboratorio de Fisiología Vegetal Aplicada, Universidad de Aysén, Coyhaique, Aysén, Chile Departamento de Ciencias Naturales y Tecnología, Universidad de Aysén, Coyhaique, Aysén, Chile Mikihisa Umehara Graduate School of Life Sciences, Toyo University, Itakuramachi, Ora-gun, Gunma, Japan Radomira Vankova Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany, Czech Academy of Sciences, Prague, Czech Republic Jingquan Yu Department of Horticulture, Zhejiang University, Hangzhou, China Mingfang Zhang Laboratory of Germplasm Innovation and Molecular Breeding, Institute of Vegetable Science, Zhejiang University, Hangzhou, People’s Republic of China Agustin Zsögön Laboratory of Plant Developmental Genetics, Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, SP, Brazil

Chapter 1

Introduction to Plant Hormones and Climate Change Golam Jalal Ahammed, Xin Li, and Jingquan Yu

1 Introduction Climate change is a naturally occurring phenomenon that includes unusual features of the environment caused by changes in natural factors such as solar energy, volcanic activities, shifts in the Earth’s orbit, and the interaction of the oceans and the atmosphere (Baluska & Mancuso, 2020; Gullino, 2021). It is believed that humans have greatly contributed to climate change in recent centuries by anthropogenic activities that affect the mean values and time lag between atmospheric phenomena, which can be reflected by the changes in the composition of the atmosphere as well as temperature regimes (Ahad & Reshi, 2015; Gullino, 2021). Climate change is one of the most widely discussed environmental topics in the twenty-first century, and it continues to be so (IPCC, 2021). Human civilization and the natural environment are both affected by climate change, and thus present and future generations face an existential risk from climate change (Baluska & Mancuso, 2020; Castroverde & Dina, 2021). Global food security is negatively impacted by climate change since climatic variabilities, such as high temperatures, fluctuating

G. J. Ahammed (*) Department of Horticulture, College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang, Henan, China e-mail: [email protected] X. Li Key Laboratory of Tea Quality and Safety Control, Ministry of Agriculture and Rural Affairs, Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, People’s Republic of China e-mail: [email protected] J. Yu Department of Horticulture, Zhejiang University, Hangzhou, China e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_1

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rainfall patterns, and other environmental conditions including biotic factors affect plant growth, development, and productivity (Mishra, 2021; Zandalinas et al., 2021). Agricultural sectors are particularly vulnerable to global warming and high temperatures (Castroverde & Dina, 2021; Sharma et al., 2020). In tropical and subtropical locations, a 1 °C rise in seasonal temperature is projected to result in a loss of 2.5–16% in staple crop yields (Li et al., 2020). During the previous four decades, there has been a significant rise (approx. 20%) in atmospheric CO2 concentrations, reaching the current level of 415 μmol mol-1 from 340 μmol mol-1 in the early 1980s (Foyer & Noctor, 2020). Such changes in CO2 concentrations have a significant impact on plant growth and development, as well as the composition of plant communities (Zandalinas et al., 2021). As autotrophs, plants perform photosynthesis to convert inorganic carbon into sugars using solar energy, which they can then use to meet their own energy needs and the energy needs of other heterotrophs including humans. Moreover, plant roots sequester carbon in the soil, and thus it is possible that plants are also able to actively influence climate (Baluska & Mancuso, 2020). Nonetheless, the impact of climate change on plants eventually affects humans owing to the climate-associated challenges to agriculture. Plant hormones, also known as phytohormones, are tiny signaling compounds that play a critical role in plant growth and development (Cutler & Nelson, 2017). Studies on plant hormones mainly started in the previous century which have found several connections between internal and external cues that control plant growth and adaptation (Alves et al., 2021; Yu et al., 2020). According to a number of studies, each plant hormone does not have a single biological function in plants, but rather it performs multiple highly specialized tasks at various stages, in different tissues, or under varying environmental circumstances (Ahammed et al., 2020; Alves et al., 2021; Blazquez et al., 2020; Chanclud & Lacombe, 2017; Li et al., 2020; Yu et al., 2020; Zhang et al., 2020). When it comes to agriculture and food security, understanding how unfavorable environments affect vital plant biological processes leading to yield penalties is a crucial scientific subject of elucidation. Exogenous stress signals and endogenous developmental cues are integrated by plants to maximize the balance of growth and stress responses in order to survive under unfavorable conditions (Zhang et al., 2020). In addition to regulating plant growth and development under normal conditions, increasing evidence suggests that phytohormones mediate a variety of stress responses and govern plant growth adaptability (Castroverde & Dina, 2021; Shimotohno et al., 2021; Yu et al., 2020). Moreover, some phytohormones have also been identified to act as interorganismal signals (MacLean et al., 2017). Thus, plant hormone research is important for understanding plant growth, developmental physiology, and interactions with the environment. But the signaling pathways of phytohormones are generally complicated, which involve numerous functionally redundant genes and spontaneous interactions with other signals.

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Fig. 1.1 The number of articles published and relevant citations on plant hormones and climate change from the year 2010 to 2021. Information was retrieved from the web of science with the keywords “Plant hormone” and “Climate change”

Plants are affected by climate change from the molecules to the ecosystem level (Altındal & Altındal, 2021; Mishra, 2021). Abiotic stresses including drought, salt, cold, and heat severely restrict plant development and geographic dispersion (Saddhe et al., 2021). As climate change threatens plant growth and development, elucidation of the response of plants becomes crucial in establishing strategies for coping with the climate change-related risks. Scientists have been working hard to understand how environmental and developmental signals converge at the cellular or organelle level in order to accomplish optimal and adaptable organogenesis in a changing environment. A wide range of studies have been conducted to examine the responses of plants to various environmental stimuli (Ge et al., 2022; Li et al., 2021a; Zhang et al., 2020). In particular, the number of research examining how plant hormones respond to climate change factors is increasing rapidly (Fig. 1.1). To expand our existing understanding of the effect of climate change on plants, multiple chapters focusing on the impact of various climate change-associated factors on plants in relation to hormone metabolism and signaling have been complied in this book. In several parts of this book, the authors demonstrate how phytohormones mediate diverse stress signals in order to govern plant growth adaptability and development. The authors also discuss how plants develop a defensive mechanism in response to stress by coordinating the biosynthesis, signaling, and metabolism of numerous hormones via a network of interconnected pathways. Our focus in this chapter is to introduce the most common plant hormones and outline their functions in plant growth, development, and stress responses.

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2 Plant Hormones Hormones are chemical messengers in multicellular organisms that essentially function to coordinate internal processes. In 1937, Frits Went and Kenneth Thimann coined the term “phytohormones” to distinguish “plant hormones” from “animal hormones” (Williams, 2010). Plant hormones are organic molecules smaller than 500 Da, and they readily move between plant cells (Cutler & Nelson, 2017). One of the distinctive features of plant hormones is that they are physiologically active at low concentrations (nanomolar to micromolar ranges). In response to environmental or developmental signals, phytohormones are synthesized, and they can function far from where they are synthesized. In general, phytohormones are transported across the plant system by active transport through influx and efflux carrier proteins found in cellular membranes (Felemban et al., 2019; VanWallendael et al., 2019). In addition to environmental and developmental factors, the (inter)actions of other phytohormones impact the accumulation and effects of each phytohormone (Jewaria et al., 2021; Li et al., 2021b; Schaller et al., 2015). In contrast to animal hormones, phytohormones are fewer in number. Early to mid-twentieth century, scientists discovered the five classical plant hormones, such as auxins, cytokinins (CKs), ethylene (ET), gibberellins (GAs), and abscisic acid (ABA) (Williams, 2010). Later, in the past half century or more, brassinosteroids (BRs), jasmonates (JAs), salicylates (SAs), and strigolactones (SLs), these four novel hormones were discovered (Ahammed et al., 2020; Ding & Ding, 2020; Felemban et al., 2019; Peng et al., 2021). Among these nine well-studied plant hormones, ABA, ET, salicylic acid (SA), and jasmonic acid (JA) are generally classified as stress response hormones, whereas the rest five hormones such as auxin, GAs, CKs, BRs, and SLs are categorized as growth promotion hormones (Cutler & Nelson, 2017; Felemban et al., 2019; Williams, 2010). However, this classification is often debated as the latter group also participates in stress response or vice versa. Although plant hormones have a wide range of functions, they all have a significant impact on growth and development (Alves et al., 2021; Blazquez et al., 2020; Zhao et al., 2021a). Phytohormones play critical roles in all phases of the life cycle of plants including seed germination, seedling growth, branching, flowering, fertilization, embryogenesis, seed dormancy, fruit formation, fruit ripening, and senescence as well as their interaction with biotic and abiotic factors occurring in the environment (Fig. 1.2). Unraveling the role of plant hormones and signaling pathways has been a major challenge in plant biology and remains one of the most active areas of study.

Introduction to Plant Hormones and Climate Change

Fig. 1.2 Nine principal plant hormones and their involvement in growth, development, and stress response. Modified and redrawn from Williams (2010). Created with BioRender.com

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3 General Concepts of Phytohormone Synthesis, Perception, and Signaling Hormone production is closely controlled, with positive or negative feedback regulation depending on the context and cross talk from other hormones and environmental inputs. Hormones regulate the functions of target cells via binding to receptor proteins, which can be transmembrane or intracellular receptors (Hakoshima, 2018). Binding of hormones (e.g., ET, CKs, and BRs) to transmembrane receptors initiates information relays, which frequently involve activation of receptor kinase activity, whereas binding of hormones (e.g., auxin, GAs, ABA, JA) to intracellular receptors changes the receptor's binding affinity for other proteins and mediates the binding domain interaction (Blazquez et al., 2020). Soluble receptors are more common in plant hormone signaling pathways than transmembrane receptors (Cutler & Nelson, 2017). Hormonal signaling has a variety of downstream consequences, including changes in gene expression patterns and, in some circumstances, nongenomic responses. As a result of hormone signaling, gene expression patterns can be altered or even completely reversed (Castroverde & Dina, 2021; Howe et al., 2018; Peng et al., 2021). The recruitment of RNA polymerase II to the core promoter is controlled by gene-specific transcription factors which often act as an “on-off switch” for transcription. The stages between hormone binding to receptor and activation of transcription factor might be simple or complex. In general, a phosphorelay system or the ubiquitin 26S proteolysis system is induced upon hormone binding to receptors leading to activation of transcription factors (Williams, 2010). Ubiquitin is a tiny protein that uses a ubiquitin ligase complex to covalently attach to other proteins (Hakoshima, 2018). After ubiquitination, the tagged protein is transported to the massive 26S proteasome complex, which particularly destroys ubiquitinated proteins (Ahammed et al., 2021b). Several hormonal signaling pathways, including auxin, GA, and JA, rely on the proteolytic breakdown of inhibiting proteins (Blazquez et al., 2020; Hakoshima, 2018). Upon hormone perception, the signal transduction in the GA, auxins, JA, and SL pathways all rely on the degradation of the negative regulator proteins, such as DELLAs, INDOLE-3-ACETIC ACID INDUCIBLEs (Aux/IAAs), JASMONATE ZIM-DOMAIN PROTEINS (JAZs), and DWARF53like SMAX1-LIKES (SMXLs), respectively, via the ubiquitination proteasome system-dependent protein degradation (Blazquez et al., 2020; Das et al., 2021; Howe et al., 2018; Schaller et al., 2015). The positive signaling components of the ET pathway ethylene insensitive2 (EIN2) and EIN3 are degraded when the ET is absent (Ahammed et al., 2021a; Cutler & Nelson, 2017). Again, BRI1-EMS SUPPRESSOR1 (BES1) and BIN2 which are positive and negative regulators in BR signaling are degraded with the deficiency and availability of BRs, respectively (Ahammed et al., 2020; Li et al., 2021b). In plants, the control of gene expression is not restricted to transcriptional regulation alone; posttranscriptional regulation is just as important (Zhao et al., 2021a). Ethylene has been found to block the translation of certain genes in Arabidopsis

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(Merchante et al., 2015). Gene-specific translational regulation in response to plant hormones other than ethylene is largely unknown at this time (Zhao et al., 2021a).

4 Phytohormones in Plant Growth, Development, and Stress Response Auxin, CKs, SLs, GAs, and BRs work together to control vegetative growth patterns (Williams, 2010). Furthermore, several hormones have been shown to have a role in the normal development and functioning of reproductive organs. For example, JAs aid pollen viability and anther filament elongation, and GAs and ET aid in the determination of flower sex in certain plants (Howe et al., 2018). Hormones play an important role during fruit growth and maturation (Fenn & Giovannoni, 2021). Pollination and seed formation cause an increase in the production of auxin and GAs, which stimulate cell proliferation and growth in the ovary, leading to an increase in fruit size (Schaller et al., 2015). Thus, GAs are frequently sprayed to improve the size of commercially grown fruits (Cutler & Nelson, 2017). In the following paragraphs, we briefly introduce the abovementioned nine plant hormones along with their well-known roles.

4.1

Auxins

The name “Auxin” is derived from the Greek word “auxein,” which means “to grow” (Shimotohno et al., 2021). Auxins refer to a group of closely similar chemicals that promote plant growth by cell elongation and also shape plant architecture (Schaller et al., 2015). Indole-3-acetic acid (IAA) is the most common naturally occurring auxin. The amino acid tryptophan is the starting point for the enzymatic pathways that lead to IAA synthesis (Cutler & Nelson, 2017). Auxin plays crucial roles in the formation of embryonic patterning, the promotion and specification of the sites of vascular tissues, the establishment of leaf and secondary roots, and the maintenance of stem cell populations (Schaller et al., 2015). Many cell cycle regulators are under the control of auxin. Auxin deficiency induces cell cycle arrest at the G1 phase in plant cell suspension cultures, while a reduction in auxin concentration increases the cell population arrested at G2, and reapplication of auxin allows cell cycle progression to resume (Shimotohno et al., 2021). Many other plant biological processes are mediated by auxins, including apical dominance as well as responses to light and gravity (Fernandez-Milmanda & Ballare, 2021). Extensibility and turgor pressure are critical for cell wall development; auxins influence both of these. Differential apical hook growth is controlled by feedback between the cell wall and auxin response (Jewaria et al., 2021). The development of some reproductive organs is also linked to auxin (Schaller et al., 2015).

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Cytokinins

Cytokinins (CKs) are a group of similar chemicals endogenously generated from the amino acid adenine in plants (Williams, 2010). Other hormones and inorganic nutrients have a big role in CK biosynthesis and catabolism. Plants produce numerous CKs, each of which interacts with CK receptors in a distinct way, allowing for more precise control of CK signaling (Hakoshima, 2018). “Kinetin” is the first known CK, and “Trans-zeatin” is the main endogenous CK (Cutler & Nelson, 2017). In plants, cell proliferation and organogenesis depend heavily on CKs and auxins. In many cases, CKs work in opposition to auxin (Schaller et al., 2015). For instance, auxin stimulates the initiation of lateral organs at the shoot apex, while CK keeps the stem cells undifferentiated. Auxin maintains the stem cell population at the root apex, while CK stimulates differentiation. As a result, cell division and differentiation are maintained in sync by the two hormones in two mutually exclusive zones. CK counteracts auxin's actions and thus increasing bud development, whereas auxin from the apex represses CK production at the bud (Schaller et al., 2015). The third hormone that represses bud development is SLs (Fichtner et al., 2021). Cytokinins also influence the formation of nitrogen-fixing root nodules, the architecture of roots and shoots, nutrient uptake, seed yields, and leaf senescence (Ikeuchi et al., 2019; Schaller et al., 2015). Moreover, CKs play a critical role in drought resistance and post-drought compensatory growth (Wang et al., 2020a; Zhang et al., 2020). Thus genetic manipulation of CK biosynthetic gene can be used as an effective tool for improving plant growth under a deficit water supply.

4.3

Gibberellins

Gibberellins (GAs) are named after the plant pathogenic fungus Gibberella fujikuroi, which causes “bakane” disease (stupid seedling) in rice with the typical phenotype of extensive plant growth due to fungus-produced GAs (Williams, 2010). In the 1960s, Norman Borlaug developed high-yielding semi-dwarf wheat cultivars that were less sensitive to GAs, which led to the “Green Revolution” and greatly contributed to global food security. Stem elongation, seed germination, flowering, developmental transitions (from juvenile to adult), and flower sex determination are mediated by GAs (Sharma et al., 2020). More than 100 GAs have been identified so far. But only a few members of the gibberellin family have biological activity in plants. GA1, GA3, GA4, and GA7 are the main bioactive forms, while gibberellic acid (GA3) is the most bioactive form of GAs (Cutler & Nelson, 2017). DELLA proteins, the negative regulator of GA signaling, are degraded in response to GAs (Casal & Balasubramanian, 2019). A lower ABA/GA ratio in the seed is necessary to alleviate dormancy and allow germination, which is determined by the balance between ABA and GA levels in the seed (Reed et al., 2022). Each of these hormones has an antagonistic effect on the metabolism of the other. Recent studies suggest that

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GAs mediate plant response to abiotic stresses including heat stress (Sharma et al., 2020).

4.4

Abscisic Acid

ABA is a ß-carotene-derived essential hormone in terrestrial plants, controlling transpiration via stomatal closure, hence reducing water loss (Li et al., 2021b; Yu et al., 2020). ABA biosynthesis is tightly regulated by 9-cis epoxycarotenoid dioxygenases (NCEDs), whose transcripts are highly expressed in response to a variety of abiotic stresses (Saddhe et al., 2021). Additionally, ABA plays a vital role in establishing and maintaining physiological seed dormancy, which prevents the germination of seeds under unfavorable conditions or periods (Reed et al., 2022). ABA is also involved in bud dormancy and stomatal development (Feitosa-Araujo et al., 2022). It reduces elongation growth and hastens senescence. The application of high concentrations of ABA induces ET production, leading to organ abscission in plants (Cutler & Nelson, 2017). As one of the main abiotic stress-responsive hormones, ABA confers tolerance to drought, salinity, heat and cold stress (Saddhe et al., 2021; Yu et al., 2020). An important role of ABA is to slow the rate of plant growth in order to let the plant cope with and adapt to adverse environmental circumstances (Li et al., 2021b; Zhang et al., 2020). ABA and ET interact with the sugar signaling pathway to mediate response to such abiotic stress (Saddhe et al., 2021). ABA synthesis and signaling are affected by cytosolic nicotinamide adenine dinucleotide (NAD, a ubiquitous metabolic coenzyme) levels, which in turn affects the response of plants to biotic and abiotic stresses (Feitosa-Araujo et al., 2022). On the contrary, ABA also affects NAD biosynthesis through transcriptional regulation, and NAD contributes to the formation of reactive oxygen species (ROS) in response to ABA, thereby playing a critical role in stress response. Plant growth responses to salt stress are controlled by complex signaling cross talk between ABA, ROS, and Ca2+ (Yu et al., 2020).

4.5

Ethylene

Ethylene (ET) is a small gaseous hormone molecule in plants (Zhao et al., 2021b). The amino acid methionine serves as a starting point for the biosynthesis of ET; nonetheless, 1-aminocyclopropane-1-carboxylic acid (ACC) is the crucial intermediate substance in ET biosynthesis. In a dark-grown eudicot seedling, ET exerts a triple response characterized by a shorter hypocotyl and root, a thickening of the hypocotyl and an exaggerated apical hook (Binder, 2020). It is often referred to as the “ripening hormone” since it is essential for the onset of fruit senescence and other physiological and metabolic processes during ripening (Fenn & Giovannoni, 2021).

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Tomatoes are an example of ET-ripened fruits (also known as climacteric fruits), in which a quick rise in ET production promotes fruit ripening (Gao et al., 2020). Ethylene has a wide range of other functions, including responses to (a)biotic stress, suppression or promotion of organ elongation and blooming, acceleration of foliar and floral senescence, and determination of the sex of flowers in some species (Fenn & Giovannoni, 2021). Ethylene production is triggered by wounding, pathogen invasion, and various abiotic stressors (Kazan & Lyons, 2014). In particular, the rapid production of ET under flooding stress leads to the fast growth of deep-water rice. In fact, ET and GA function together in hypoxia to regulate a variety of downstream targets (Saddhe et al., 2021). Most often, ET and JA work together synergistically in response to biotic stressors (Kazan & Lyons, 2014).

4.6

Salicylates

Salicylic acid (SA) is a crucial plant hormone that basically functions in mounting resistance to a variety of plant pathogens (Peng et al., 2021). Salicylates include SA and its metabolites. SA is mostly synthesized from chorismate through the secondary metabolic pathways (Peng et al., 2021). SA is an important hormone in plant innate immunity, which includes resistance to biotic attacks, hypersensitive response, and cell death (Karasov et al., 2017; Kim et al., 2021). Being an important hormone in plant innate immunity, SA mediates resistance to both local and systemic tissue (Ding & Ding, 2020; Kim et al., 2021). Plant defenses against biotrophic pathogens largely rely on SA signaling pathways (Kazan & Lyons, 2014). Systemic acquired resistance (SAR) is another key element of plant innate immunity mediated by SA (Peng et al., 2021). Plants that are unable to synthesize SA are very vulnerable to a wide range of disease-causing plant pathogens. Upon recognition of the pathogens, plants trigger SA production, which causes the activation of numerous genes involved in pathogen defenses, including pathogenesis-related proteins with antimicrobial activities (Kazan & Lyons, 2014). Nonetheless, extensive cross talk between the SA and ET/JA signaling pathways fine-tunes plant defense response to different plant pathogens (Howe et al., 2018; Mermigka et al., 2020).

4.7

Jasmonates

Jasmonates (JAs) are a broad term for the family of hormones comprising jasmonic acid (JA) and its derivatives (Howe et al., 2018). JA is synthesized from membrane lipids in the chloroplast and peroxisome (Williams, 2010). However, JA cannot act as a bioactive hormone unless it is conjugated to various amino acids (most often isoleucine) in the cytoplasm to produce jasmonyl-Ile (JA-Ile) (Howe et al., 2018). In addition to the defensive function, JAs have a role in vegetative and reproductive

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development (Fenn & Giovannoni, 2021; Li et al., 2021a; Varshney & Majee, 2021). For instance, JA is involved in tuber formation, pollen fertility establishment, mechanosensing, and responses to biotic and abiotic stress (Cutler & Nelson, 2017). JA and ET act synergistically to mediate plant responses to necrotrophic phytopathogens and various herbivores. Sometimes, the JA/ET pathway dampens the SA pathway and vice versa (Ding & Ding, 2020).

4.8

Brassinosteroids

The steroid hormone brassinosteroids (BRs) regulate many biological processes related to plant growth, development, and response to stress (Planas-Riverola et al., 2019). Cell elongation was first assumed to be the cause of BR-induced growth enhancement; later cell division has also been shown to be linked to the function of BR. In addition to cell elongation and cell division, BRs govern a variety of other processes of growth and development, including xylem differentiation, photomorphogenesis, plant reproduction, and responses to abiotic and biotic challenges (Ahammed et al., 2020; Nolan et al., 2017; Planas-Riverola et al., 2019). BR biosynthesis is supposed to occur solely in the endoplasmic reticulum (Nolan et al., 2020). The plasma membrane-localized BRASSINOSTEROID INSENSITIVE1 (BRI1) and homologous receptors sense BRs, leading to the activation of the key transcription factor BRASSINAZOLE-RESISTANT1 (BZR1), which regulates the transcription of BR-responsive genes in the nucleus (Nolan et al., 2017). Under suboptimal conditions, BRs boost photosynthetic efficiency and thereby promote growth and biomass accumulation. BR deficiency leads to dwarfism, dark de-etiolation, blossom delay, reduced male fertility, and senescence (Clouse, 2015). But overexpressing the BR biosynthetic gene leads to an increase in crop yield and an improvement in stress tolerance (Nolan et al., 2017; Ramirez & Poppenberger, 2020). RESPIRATORY BURST OXIDASE HOMOLOG 1 (RBOH1)-dependent ROS signaling plays a critical role in BR-induced stress tolerance (Ahammed et al., 2020). ABA and BR signaling pathways have long been known to interact antagonistically. However, recent research showed that the synergistic mechanism of ABA and BR is triggered in a short period of time to govern plant growth and adaptability under moderate stress in rice (Li et al., 2021b).

4.9

Strigolactones

Strigolactones (SLs) are carotenoid-derived plant secondary metabolites that function as a novel class of plant hormones in a variety of aspects of plant growth and development as well as rhizospheric communication with symbiotic microorganisms (Bürger, 2021; Mashiguchi et al., 2021; Wang et al., 2020b). SLs have been shown to be a root-derived, upwardly mobile signal that inhibits the branching of

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shoots (Mashiguchi et al., 2021). SLs are also involved in shaping root architecture, senescence, and secondary growth (Fichtner et al., 2021). SLs secreted from the host plant roots increase the germination, hyphal branching, and chitin oligomer synthesis of arbuscular mycorrhizal fungi (AMF) hyphae, thereby facilitating AMF symbiosis (MacLean et al., 2017). Auxin from the shoot to the root promotes the production of SLs, which are then translocated into the shoot to inhibit bud outgrowth (Aliche et al., 2020; Fichtner et al., 2021). When nutrients are scarce, SLs promote root growth and mycorrhizal symbiosis to facilitate nutrient acquisition while inhibiting shoot development (Ge et al., 2022). Besides, elevated atmospheric CO2 and specific light quality have been shown to modulate SL production and signaling (Ge et al., 2022; Zhou et al., 2019).

5 Conclusions and Future Perspectives In the field, crop plants are constantly subjected to a variety of environmental challenges. Thus, in-depth knowledge of plant hormones is essential for gaining insight into plant growth, physiology, and interactions with their environments. In this chapter, we provide a short overview of nine well-known plant hormones and discuss their involvement in plant growth, development, and stress tolerance under changing climatic conditions. Notably, these hormones do not always affect plant growth, development, or defense in a linear manner. Stress response in plants is finely coordinated by the interaction and communication between several hormones. By the middle of this century, the world’s population is expected to reach about 10 billion. High-yielding crops that can sustain under more varied environmental conditions will be required in the next decades to keep up with the rising global population and to meet their demand for food. Given that rising temperature threatens plant growth and productivity worldwide, a more pressing need is to investigate the thermal-responsive hormone signal transduction pathway and sophisticated cross talk between different signaling pathways in order to clarify phytohormone functions in plant stress response. Recent advances in genetics and genomics are making it possible to improve important agricultural traits that affect crop yield and quality. Such research will continue to discover critical candidate genes related to yield and stress tolerance, and following studies that target these genes for alteration will help unveil their usefulness for enhancing agricultural productivity. Extending the multi-gene regulatory circuits will help us learn more about the regulation of endogenous hormones and develop ever-more complex hormonetriggered biological processes in plants. The development of novel plant hormones, on the other hand, continues to be a hot topic in plant research. Polyamines, melatonin, and plant peptide signals systemin and phytosulfokines are some interesting plant growth regulators that might be new candidate plant hormones. To address climate change-related issues in crop production, we must embrace new technologies and unravel mechanisms of stress perception, signaling, and response in plants. CRISPR/CAS-mediated genome editing has recently been adopted in plant

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science, which provides exciting instances of effective applications in plant hormone research, thus opening new avenues in this promising field of plant science. Genomic technologies and their applications in plant hormone research have also emerged recently, opening the path for a new generation of scientists to pursue this lucrative field of phytohormone research. Aside from this new viewpoint on plant hormone function, synthetic biology has the potential to inspire the development of new biotechnologies. The area of plant hormone biology needs to use a variety of techniques to examine the functions of individual hormone signaling components, hence revealing information on particular signaling events or the relationships between linked pathways. Acknowledgments Research in the authors’ laboratories was supported by the National Natural Science Foundation of China (grant numbers 31950410555, 31550110201); Ministry of Science and Technology of the People’s Republic of China (grant numbers DL2022026004L, QNJ2021026001); Zhejiang Provincial Natural Science Foundation of China (grant number LR22C160002); and Henan University of Science and Technology Research Start-up Funds for New Faculty (grant numbers 13480058, 13480070). Declaration of Competing Interest The authors declare that they have no conflict of interest.

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Peng, Y., Yang, J., Li, X., & Zhang, Y. (2021). Salicylic acid: Biosynthesis and signaling. Annual Review of Plant Biology, 72, 761–791. https://doi.org/10.1146/annurev-arplant-081320-092855 Planas-Riverola, A., Gupta, A., Betegon-Putze, I., Bosch, N., Ibanes, M., & Cano-Delgado, A. I. (2019). Brassinosteroid signaling in plant development and adaptation to stress. Development, 146(5), 15894. https://doi.org/10.1242/dev.151894 Ramirez, V. E., & Poppenberger, B. (2020). Modes of brassinosteroid activity in cold stress tolerance. Frontiers in Plant Science, 11, 583666. https://doi.org/10.3389/fpls.2020.583666 Reed, R. C., Bradford, K. J., & Khanday, I. (2022). Seed germination and vigor: Ensuring crop sustainability in a changing climate. Heredity. https://doi.org/10.1038/s41437-022-00497-2 Saddhe, A. A., Manuka, R., & Penna, S. (2021). Plant sugars: Homeostasis and transport under abiotic stress in plants. Physiologia Plantarum, 171(4), 739–755. https://doi.org/10.1111/ppl. 13283 Schaller, G. E., Bishopp, A., & Kieber, J. J. (2015). The yin-yang of hormones: Cytokinin and auxin interactions in plant development. Plant Cell, 27(1), 44–63. https://doi.org/10.1105/tpc.114. 133595 Sharma, L., Priya, M., Kaushal, N., Bhandhari, K., Chaudhary, S., Dhankher, O. P., Prasad, P. V. V., Siddique, K. H. M., & Nayyar, H. (2020). Plant growth-regulating molecules as thermoprotectants: Functional relevance and prospects for improving heat tolerance in food crops. Journal of Experimental Botany, 71(2), 569–594. https://doi.org/10.1093/jxb/erz333 Shimotohno, A., Aki, S. S., Takahashi, N., & Umeda, M. (2021). Regulation of the plant cell cycle in response to hormones and the environment. Annual Review of Plant Biology, 72, 273–296. https://doi.org/10.1146/annurev-arplant-080720-103739 VanWallendael, A., Soltani, A., Emery, N. C., Peixoto, M. M., Olsen, J., & Lowry, D. B. (2019). A molecular view of plant local adaptation: Incorporating stress-response networks. Annual Review of Plant Biology, 70, 559–583. https://doi.org/10.1146/annurev-arplant-050718-100114 Varshney, V., & Majee, M. (2021). JA shakes hands with ABA to delay seed germination. Trends in Plant Science, 26(8), 764–766. https://doi.org/10.1016/j.tplants.2021.05.002 Wang, X.-L., Duan, P.-L., Yang, S.-J., Liu, Y.-H., Qi, L., Shi, J., Li, X.-L., Song, P., & Zhang, L.-X. (2020a). Corn compensatory growth upon post-drought rewatering based on the effects of rhizosphere soil nitrification on cytokinin. Agricultural Water Management, 241, 106436. https://doi.org/10.1016/j.agwat.2020.106436 Wang, L., Wang, B., Yu, H., Guo, H., Lin, T., Kou, L., Wang, A., Shao, N., Ma, H., Xiong, G., Li, X., Yang, J., Chu, J., & Li, J. (2020b). Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature, 583(7815), 277–281. https://doi.org/10.1038/s41586-020-2382-x Williams, M. E. (2010). Introduction to phytohormones. The Plant Cell, 22(3), 1–10. https://doi. org/10.1105/tpc.110.tt0310 Yu, Z., Duan, X., Luo, L., Dai, S., Ding, Z., & Xia, G. (2020). How plant hormones mediate salt stress responses. Trends in Plant Science, 25(11), 1117–1130. https://doi.org/10.1016/j.tplants. 2020.06.008 Zandalinas, S. I., Fritschi, F. B., & Mittler, R. (2021). Global warming, climate change, and environmental pollution: Recipe for a multifactorial stress combination disaster. Trends in Plant Science, 26(6), 588–599. https://doi.org/10.1016/j.tplants.2021.02.011 Zhang, H., Zhao, Y., & Zhu, J. K. (2020). Thriving under stress: How plants balance growth and the stress response. Developmental Cell, 55(5), 529–543. https://doi.org/10.1016/j.devcel.2020. 10.012 Zhao, C., Yaschenko, A., Alonso, J. M., & Stepanova, A. N. (2021a). Leveraging synthetic biology approaches in plant hormone research. Current Opinion in Plant Biology, 60, 101998. https:// doi.org/10.1016/j.pbi.2020.101998 Zhao, H., Yin, C. C., Ma, B., Chen, S. Y., & Zhang, J. S. (2021b). Ethylene signaling in rice and Arabidopsis: New regulators and mechanisms. Journal of Integrative Plant Biology, 63(1), 102– 125. https://doi.org/10.1111/jipb.13028 Zhou, Y., Ge, S., Jin, L., Yao, K., Wang, Y., Wu, X., Zhou, J., Xia, X., Shi, K., Foyer, C. H., & Yu, J. (2019). A novel CO2-responsive systemic signaling pathway controlling plant mycorrhizal symbiosis. The New Phytologist, 224(1), 106–116. https://doi.org/10.1111/nph.15917

Chapter 2

The Complex Interaction Between Elevated CO2 and Hormones on the Control of Plant Growth Karla Gasparini, Fred A. L. Brito, Lázaro E. P. Peres, Dimas M. Ribeiro, and Agustin Zsögön

1 Introduction Half a century has passed since the publication of the Study of Man’s Impact on the Climate (SMIC): Inadvertent Climate Modification (SMIC, 1971). This white paper was written by a panel of renowned scientists who, for the first time, called the attention of the world to a global problem of unprecedented scope. It presented evidence that carbon dioxide (CO2), methane (CH4), nitrous oxide (N2O), and fluorinated gases produced by human activities lead to global warming by absorbing infrared radiation emitted from the Earth’s surface and trapping it in the atmosphere. This soon became popularized in the media as the “greenhouse effect.” The evidence of human impact on climate was convincing enough to convene the first UN Conference on the Human Environment (Stockholm, 1972—known today as “Earth Summits”) and to create the UN Environmental Program, headquartered in Nairobi, Kenya. The mission of these institutions was to implement measures to reduce the emission of greenhouse gases, with especial focus on the CO2 derived from the use of fossil fuels. Unfortunately, an international mechanism with enforcement authority was not established for another 25 years, when the Kyoto Protocol was adopted (Bazerman, 2006). The effectiveness of the Kyoto Protocol in mitigating climate change is still a matter of debate, with evidence for (Maamoun, 2019) and against (Almer & Winkler, 2017) a discernible positive impact. The sixth periodical report of the Intergovernmental Panel on Climate Change (IPCC) has

K. Gasparini · L. E. P. Peres · A. Zsögön (*) Laboratory of Plant Developmental Genetics, Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, SP, Brazil e-mail: [email protected] F. A. L. Brito · D. M. Ribeiro Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, Brazil © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_2

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shown that global mean temperature has increased faster since 1970 than in any other 50-year period over the last two millennia, most likely due to greenhouse gases: atmospheric CO2 concentration ([CO2]) was higher in 2019 than at any time during the last two million years, and concentrations of CH4 and N2O were higher than at any time in at least 800,000 years (IPCC, 2021). Plants supply humankind with foods, nutritional and medicinal chemicals, fibers for paper and clothes, and fuel as firewood or biodiesel. Primary productivity on the planet depends on the fixation of CO2 by aquatic and terrestrial photosynthetic organisms, so changes in atmospheric [CO2] are expected to have a profound impact in trophic chains. At face value, changing climate and increased [CO2] could be beneficial for agriculture by allowing increased yields at higher latitudes (Butler et al., 2018; Parent et al., 2018), by mitigating drought stress (Wang et al., 2018) or by increasing yield (Nakano et al., 2017). However, the suite of changes in crop physiology driven by the combination of higher atmospheric [CO2] and fluctuating temperature and rainfall patterns is bound to be more complex (Zsögön et al., 2022). A deeper understanding of the effects of elevated [CO2] on plant growth is urgently needed. Considerable research effort has been devoted to unveiling the effects of elevated [CO2] on the development and dynamics of stomata, the pores controlling the exchange of CO2 and water vapor in the epidermis of plant organs. We begin by considering the first tool that plants have in their repertoire of mechanisms to cope with fluctuating conditions, namely, stomatal aperture and closure, and how changing atmospheric [CO2] may alter their dynamics.

2 Elevated CO2 and Abscisic Acid Interaction in the Control of Stomatal Dynamics Throughout their life cycle, plants experience fluctuation in environmental CO2 concentration due to diurnal and seasonal variation driven by CO2 fluxes associated with vegetation itself (Imasu & Tanabe, 2018). In addition, plants need to acclimate to the particular environmental conditions within the canopy and the resistance to CO2 flux along the diffusion pathway within of leaves (Buchmann et al., 1996; Evans et al., 2009). Plants have therefore developed complex physiological and morphological mechanisms to sense and respond to variations in [CO2]. The epidermis represents a highly impermeable barrier to water and CO2 fluxes, due to the presence of a hydrophobic cuticle (Woodward, 1998). However, gas exchange is possible due to the presence of specialized cell pairs (guard cells) that surround a pore (stomatal pore) which the guard cells can open or close via changes in their turgidity (Buckley, 2019). Plants perceive changes in [CO2] in cells of the mesophyll rather than at the leaf surface (Engineer et al., 2016). The development and dynamics of stomata are essential to balance CO2 uptake and water loss in a changing environment (Hetherington & Woodward, 2003). Thus, the effects of elevated CO2 on plant

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growth and development are, to a large extent, a consequence of changes in stomatal conductance and their effect on CO2 assimilation. In general, elevated [CO2] induces two types of responses along the temporal scale. In the short term, it reduces leaf stomatal aperture, and in the long term, it alters stomatal density via changes in developmental patterning (Qi & Torii, 2018). At elevated [CO2], stomata short-term behavior is linked to cell guard depolarization via CO2 activation of anion channels (Brearley et al., 1997; Raschke et al., 2003). This response is controlled by increased activity of outward rectifying K+ channels and decreased activity of inward rectifying K+ channels, increased activation of S-type anion channels, and stimulation of Cl- release from guard cells as well as decrease in guard cell concentrations of zeaxanthin (Brearley et al., 1997; Hanstein & Felle, 2002; Webb et al., 1996; Zhu et al., 1998). The stomata response to elevated [CO2] is also associated with increased Ca2+ in the guard cells (Webb et al., 1996). In addition, variations of cytosolic Ca2+ ([Ca2+]cyt) transient have been associated with changes in [CO2] after initial Ca2+-independent stomatal movement and CO2-regulated [Ca2+]cyt transients impair CO2-induced stomatal movement (Young et al., 2006). Although a vast list of potential messengers in stomatal response to [CO2] has been described (e.g., ion channel activity, calcium, abscisic acid—ABA-, malate, zeaxanthin), little is known about the components which act on the earliest signaling pathway that controls stomatal aperture in response to elevated [CO2]. Carbonic anhydrases, the protein kinase NtMPK4, and the HIGH LEAF TEMPERATURE 1 kinase (HT1) have been identified as early players in stomatal closure at elevated [CO2] (Hashimoto et al., 2006; Hu et al., 2010; Marten et al., 2008). The former two control stomatal conductance by [CO2] independently of ABA response, while HT1 shows a functional response to ABA. ABA is the key hormone regulating stomatal closure in plants, yet the mechanism of ABA and CO2 interaction and its role of stomatal closure remains unclear. Early research indicated a positive correlation between ABA content and CO2 sensitivity in Xanthium strumarium L. (Raschke, 1975; Raschke et al., 1976). In agreement with these results more recent work (Chater et al., 2015), using mutants of the PYR/RCAR family ABA receptors (pyr1pyl1pyl4 and pyr1pyl1pyl2pyl4) and ABA biosynthesis (neced3 and nced5) showed that both are required for stomatal closure at elevated [CO2] in Arabidopsis thaliana. However, some studies have suggested that the stomatal response to elevated [CO2] is ABA-independent (Hsu et al., 2018a, 2018b; Merilo et al., 2013, 2015; Webb & Hetherington, 1997). ABA-deficient mutants (aba1, aba1-1, and aba3-1), which have low endogenous levels of ABA, displayed reduction in stomatal aperture in response to CO2 in a similar way to the corresponding wild-type counterparts (Merilo et al., 2013, 2015; Webb & Hetherington, 1997). A combination of genetic, physiological, and biochemical approaches to evaluate the relationship between elevated [CO2], ABA, and stomatal closure recently shed new light on this point (Dubeaux et al., 2021). In contrast to the findings in previous studies, strong ABA biosynthesis mutants (nced3/nced5 and aba2-1) and the PYR/RCAR ABA receptor mutant retained the ability to respond to elevated [CO2]. However, nced3/nced5 and aba2-1 showed an attenuated long-term

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response, and ABA receptor mutants exhibited delayed response to elevated [CO2] (Hsu et al., 2018a, 2018b). These results suggest that stomatal closure responses to elevated [CO2] are not only caused by altered ABA levels, but that ABA is essential to facilitate, maintain, and accelerate the stomatal response to CO2 elevation (Hsu et al., 2018a, 2018b). In addition, a basal level of ABA seems to be necessary for the stomatal response to CO2, since even drastic mutants in ABA biosynthesis retain a minimum level of ABA and respond to CO2 changes (Hsu et al., 2018a, 2018b). Another potential convergence point of the ABA and CO2 signaling pathways in the promotion of stomatal closure is the OPEN STOMATA 1 (OST1) protein (Merilo et al., 2013; Xue et al., 2011). OST1 is a Ser/Thr kinase that appears to play a key role in ABA signaling and CO2-induced stomatal closure. The activation of slow (S-type) anion channels (encoded by SLOW ANION CHANNEL-ASSOCIATED1; SLAC1) via phosphorylation by OST1 is essential to stimulate anion efflux in guard cells and stomatal closure (Brandt et al., 2012; Geiger et al., 2009; Lee et al., 2009). Thus, mutations in OST1 affect both ABA signaling and CO2-induced stomatal closure (Merilo et al., 2013; Xue et al., 2011). New evidence suggests that although elevated CO2 induces stomatal closure via an ABA-independent pathway, basal ABA levels and OST1 activity are required to amplify and accelerate stomatal closure triggered by elevated CO2 (Hsu et al., 2018a, 2018b). In addition, ABA and CO2 synergistically induce stomatal closure downstream of OST1, and not upstream as suggested previously (Hsu et al., 2018a, 2018b). However, ABA is not the only plant hormone involved in stomatal control. We next turn our attention to the effect of other hormones and their interaction with CO2 in the control of stomatal opening and closure.

3 Convergence of Elevated CO2 and Hormone Signaling in the Control of Stomatal Dynamics Plant hormones are small molecules that can be transported over the plant body to act as integrators of growth and physiological responses. Their effects are mediated by a balance between metabolism (synthesis and degradation or inactivation), transport, and perception (Davies, 2010). The hormone families, besides ABA, are auxins, cytokinins (CKs), gibberellins (GAs), ethylene, brassinosteroids (BRs), strigolactones, jasmonic acid (JA), and salicylic acid (SA). Elevated [CO2] induces significant increases in auxin and cytokinin levels in leaves (Teng et al., 2006). Notably, it has also been observed that under elevated [CO2], the transcripts of genes encoding selective transporters of both auxins and CKs are decreased (Wei et al., 2013). The spatial distribution of hormones is crucial to their function, so this effect deserves to be explored in more detail (Anfang & Shani, 2021). Auxins have ambiguous functions in stomatal movement. On the one hand, they play a positive role in stomatal opening in physiological concentrations, but at higher concentrations auxin can induce stomatal closure (Lohse & Hedrich, 1992). Early work

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showed an antagonistic effect of CKs on both ABA- and CO2-induced stomatal closure (Blackman & Davies, 1983, 1984). It was subsequently shown that this effect was mediated by ethylene (Tanaka et al., 2006). However, contradictory evidence later showed that manipulation of CK levels did not affect stomatal movement or ABA-induced stomatal closure (Farber et al., 2016). Ethylene and JA have been associated to the regulation of stomatal movement at elevated [CO2]. JA is well-known for its role in abiotic stress (Raza et al., 2021). In response to abiotic stress, genes related to JA signaling are upregulated, and, in turn, JA regulates the expression of numerous genes related to stress response promoting protective mechanisms (Ali & Baek, 2020). Methyl jasmonate (MeJa) induces stomatal closure by changes in free cytosolic calcium concentration in guard cells. CPK6 (Ca2+-dependent protein kinase 6) is required for ABA signaling and for activation of nonselective Ca2+-permeable cation channels and S-type anion channels in MeJA signaling in the guard cells (Munemasa, Hossain, et al., 2011). Many other common signaling components involved in ABA and MeJA crosstalk have been described (reviewed in Munemasa, Mori, & Murata, 2011), which reinforces the participation of MeJa in the regulation of stomatal aperture. Studies of the association between elevated [CO2], JA, and stomatal movement are still scarce. However, metabolomic analysis in Brassica napus exposed to elevated [CO2] showed significant changes in the JA biosynthesis pathway (Geng et al., 2016). This result led the authors to explore the relationship of JA with stomatal closure at elevated [CO2]. JA biosynthesis and signaling mutants showed compromised CO2 response under elevated [CO2] (Geng et al., 2016). However, more recent work described only minor effects of JA and SA on stomatal closure in response to CO2 (Zamora et al., 2021). As described above for auxins and CKs, the mode of action of ethylene is ambiguous, as it can promote both stomatal opening and closure (Desikan et al., 2006; Tanaka et al., 2005, 2006). The incubation of Arabidopsis leaves in ethylene gas, ethephon, or the ethylene precursor ACC (1-aminocyclo-propane-1-carboxylic acid) induced stomatal closure in a dose-dependent manner (Desikan et al., 2006). Stomatal closure was dependent on hydrogen peroxide (H2O2) production in guard cells generated by NADPH oxidase AtrbohF, and H2O2 is a key signaling molecule in ABA-induced stomatal closure (Desikan et al., 2006). In contrast, ethylene and ACC suppressed ABA induction of stomatal closure (Tanaka et al., 2005). Thus, both of these hormones could induce stomatal closure independently, but when applied simultaneously, they do not trigger the complete closure of the stomata (Beguerisse-Diaz et al., 2012; Tanaka et al., 2005). Increased expression of ACC OXIDASE 1 (ACO1) and CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1) was observed in Arabidopsis Col-0 plants growing at elevated [CO2] (Smet et al., 2020). Interestingly, these genes have divergent functions in the ethylene pathway, whereby ACO1 is involved in ethylene biosynthesis, and CTR1 is a negative regulator of the ethylene response pathway. In ethylene insensitive 2-5 (ein2-5), a mutant insensitive to ethylene, genes involved in stomatal movement were upregulated, some of them involved in the regulation of stomatal movement via

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ABA (e.g., PP2CA), and others not directly involved in ABA signaling (e.g., TPC1) (Islam et al., 2010; Smet et al., 2020). Recent work has shown that regulation of GA signaling via the transcriptional repressor PROCERA (Nir et al., 2017) and the GA receptor protein GID1 (Sukiran et al., 2020) can also influence stomatal aperture. Brassinolide (BL), the main BR active molecule, promotes stomatal closure in an ABA-independent manner in Arabidopsis (Ha et al., 2016) and tomato (Solanum lycopersicum) (Xia et al., 2014). Recently, SA and SA signaling were described as important components of elevated [CO2]-induced stomatal closure by reactive oxygen species (ROS) production (He et al., 2020). SA-deficient mutant and SA signaling mutants did not show significant reduction in stomatal aperture at elevated [CO2], compared to WT. Moreover, ROS accumulation, an important signal involved in the regulation of stomatal closure, was completely abolished in these mutants (He et al., 2020). Further investigation should elucidate if atmospheric CO2 has an effect on these signaling modules of GA, BR, and SA in the control of stomatal function. The conflicting results described here in relation to hormones and stomatal movement suggest that different pathways may regulate stomatal movement at elevated [CO2], and disruption of one pathway may favor an alternative one (Lawson & Matthews, 2020). Furthermore, in the face of the extensive hormonal crosstalk (Aerts et al., 2021), it is not possible to exclude the possibility of convergence and interaction between pathways or sharing of signaling molecules to control stomatal movement. The numerous possibilities between hormonal crosstalk, concentrationdependent hormonal function, and organ-dependent hormonal function, associated with nonlinear hormonal response to increasing [CO2], make it difficult to understand the regulatory pathways of stomatal movement. However, the availability of hormone biosynthesis, signaling, and perception mutants (loss-of-function and gainof-function mutants, overexpression lines, knockdown lines) (Carvalho et al., 2011) in combination with new technologies for the analysis of transcripts, metabolites, and epigenetics provides new possibilities to better understand the connections between hormones, stomatal movement, and environmental changes. Another factor that can influence stomatal conductance is stomatal density and patterning, which are controlled by differentiation of meristematic cells in the epidermis in response to endogenous and exogenous factors.

4 Elevated CO2 and Hormones Control Stomatal Development Like stomatal aperture, stomatal development is also regulated by a combination of environmental cues mediated by plant hormones (Qi & Torii, 2018). The canonical long-term response to growth under elevated [CO2] is a decrease in stomatal density (SD, the number of stomata per unit leaf area) mediated by changes in stomatal index (SI, the ratio of stomatal guard cells to epidermal pavement cells) (Woodward &

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Kelly, 1995). The study of plants growing at different altitudes provides an interesting setting for powerful “natural experiments” to explore and confirm the effect of [CO2] in stomatal development. The volume percentage (mole fraction) of CO2 in the air remains almost constant with increasing elevation, but its partial pressure or concentration (mass per volume) decreases as the barometric pressure falls with increasing altitude. SD responded to the reduced partial pressure of CO2 in a simulation of high altitude (3000 m), when the CO2 mole fraction was unchanged (Woodward & Bazzaz, 1988). SD has thus been shown to change along environmental gradients of CO2 (Hovenden & Brodribb, 2000; Kouwenberg et al., 2018; Pato & Obeso, 2012). In addition, the reciprocal approach has also been used: the analysis of fossil and herbaria plant records has established a correlation between SD and palaeo-CO2 levels (McElwain & Chaloner, 1995; Rivera et al., 2014; Woodward, 1987). Leaves of temperate tree species collected over the last 200 years and preserved in herbaria showed a 40% decrease in SD occurring over time (Woodward, 1987). The decreased SD observed in the herbarium specimens was confirmed for some of the species when they were grown under a [CO2] increased from 280 μmol mol-1 to 340 μmol mol-1 (Woodward, 1987). The analysis of Buxus epidermis fragment found in coprolites revealed significant increases in SD and SI compared to those found in the extant species Buxus balearica and Buxus sempervirens (Rivera et al., 2014). Although decreased SD and SI are a common response triggered by growth under elevated [CO2], divergent responses such as increased SD and SI have also been reported in Free Air CO2 Enrichment (FACE) experiments (Reid et al., 2003; Tricker et al., 2005). In addition, meta-analyses compiling data from multiple assays demonstrated only 5% of decrease in SD (Ainsworth & Rogers, 2007). Since stomatal development is influenced by internal and external signals, the intensity of SD and SI response could depend on species/genotypes, plant age, experimental duration, and environmental conditions (e.g., light intensity and type, water availability, CO2 concentration, and exposure time of CO2) (Xu et al., 2016). For example Tricker et al. (2005) reported decreases in SI and SD in the first and second year, respectively, in leaves of poplar trees exposed to 550 μmol mol-1 of CO2. However in the third, fourth and fifth years after elevated CO2 treatment, no significant changes were observed in SD and SI (Tricker et al., 2005). These results could be related to CO2 access to the canopy. In the first 2 years of treatment, the canopy is more open, which allows more CO2 contact with the leaves. With canopy growth, CO2 dissipation in the canopy could be reduced, and thus the effect of CO2 on stomatal development is altered. Another important point to be considered regarding the influence of CO2 on SD is the combination of environmental factors and genotype-specific response. Col-0 and Ws Arabidopsis thaliana accessions showed different SD response when grown in elevated [CO2] and either well-watered or drought treatments (Woodward et al., 2002). Col-0 had a slight reduction in SD at well-watered x elevated [CO2] but exhibited greatly reduction in SD in drought x elevated [CO2]. Ws, on the other hand, showed significant reduction in SD in both treatments, well-watered ×

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elevated [CO2] and drought × elevated [CO2]. Since different environmental factors affect stomatal density (CO2, light, abiotic stress), caution is required when SD is directly associated with [CO2] (Xu et al., 2016). The pattern of stomatal development is determined by the environment of the mature leaves, that appear to detect and transmit the external cues in a systemic manner to newly emerged leaves (Lake et al., 2001). However, the perception and signal transduction pathways underlying this phenomenon are still poorly known. The Arabidopsis gene HIC (High Carbon Dioxide) was shown to link CO2 perception to stomatal development (Gray et al., 2000). The HIC gene, in which encodes a putative 3-keto acyl coenzyme A synthase, is negative regulator of stomatal development that responds to CO2. hic mutants showed a 42% increase in SD in response to a doubling [CO2]. Interestingly, HIC is involved in wax biosynthesis, and usually mutants with altered wax profile, such as cer1 and cer6, also exhibit increases in stomatal indices (Gray et al., 2000). Since modifications in wax profile could alter CO2 permeability, it is possible that cuticular wax influences stomatal development pattern (Casson & Gray, 2008). Although mutations in genes such as TOO MANY MOUTHS (TMM) and FOUR LIPS (FLP) also alter stomatal density, these mutants exhibit stomatal cluster formation, a pattern not observed in hic mutants (Torii, 2021). These results suggest different mechanism that control SD by environmental and cell-to-cell mechanisms (Lake et al., 2002). Engineer et al. (2014) identified key players in the control of stomatal development by CO2: the β carbonic anhydrase genes CA1 and CA4, the extracellular pro-peptide-encoding gene epidermal patterning factor 2 (EPF2), and CO2 response secreted protease (CRSP). EPF2 is essential for CO2 control of stomatal development, and the transcription of this gene is only induced in wild-type but not in ca1 ca4 mutants at elevated [CO2]. Thus, both mutants, ca1 ca4 and epf2, exhibited increase in SI at elevated [CO2]. Additionally, the authors demonstrated that CRSP cleaves and activates EPF2, repressing stomatal development at elevated [CO2] (Engineer et al., 2014). As integrators of environmental signals in plant growth and development, plant hormones play a key role in stomatal development (Qi & Torii, 2018). The main classes of hormones are involved in determining the fate of the guard cell lineage and guiding stomatal development, including auxin (Zhang et al., 2014), CKs (Vatén et al., 2018), BRs (Kim et al., 2012), and ethylene (Gong et al., 2021). However, the role of hormones and pathways linking hormones, stomatal development, and elevated [CO2] is still poorly explored. It should be noticed that alterations in SD could be caused by differential growth responses (either cell division, cell expansion, or both) of the epidermal pavement cells caused by environmental conditions. Modifications in SD in response to environmental signals, including CO2 and humidity, were initially correlated with changes in whole-plant transpiration and leaf ABA concentration (Lake & Woodward, 2008). ABA plays a role in inhibiting initiation of stomatal development (Tanaka et al., 2013), and ABA-deficient mutants exhibit increased stomatal density compared to their controls (Chater et al., 2015; Hsu et al., 2018a, 2018b; Merilo et al., 2018; Tanaka et al., 2013). ABA receptor and biosynthesis mutants maintain stomatal density at elevated [CO2] indicating that

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ABA is required to reduced stomatal density or that ABA presence modulates the sensitivity of stomatal development to [CO2] (Chater et al., 2015). Ethylene signaling has also been implicated in stomatal patterning (Serna & Fenoll, 1997; Serna & Noll, 1995). The use of loss-of-function ein2 mutants, completely insensitive to ethylene, indicates that ethylene signaling affects epidermal cell number and that ethylene is required for stomatal response on the abaxial leaf surface, when mature leaf was submitted to elevated [CO2] (Lake et al., 2002). More recent work has shown a role for CTR1, a negative regulator of ethylene signaling on the self-renewing capacity of stomatal lineage stem cells (Gong et al., 2021). Although few studies have reported on the involvement of hormones in the regulation of stomatal development via CO2, most plant hormones are involved in the control and patterning of stomatal development, and the signaling pathways in which they participate and/or which they regulate are slowly being unraveled (recently reviewed by Wei, Fang, et al., 2021). ABA, BR, auxin, and JA generally repress stomata development, while CK, ethylene, and GAs promote stomatal differentiation (Wei, Jing, et al., 2021). However, the action of each hormone in stomatal development is largely subject to influence by the organ, hormone concentration, and interaction between hormones (Daszkowska-Golec & Szarejko, 2013; Wei, Fang, et al., 2021). For instance, BR shows opposite effects on development of stomata in cotyledon and hypocotyls (Fuentes et al., 2012; Gudesblat et al., 2012; Kim et al., 2012). Application of exogenous BR decreases stomatal density, while the addition of BR biosynthesis inhibitors stimulates the formation of stomatal clusters in cotyledons (Kim et al., 2012). In contrast, mutants defective in BR biosynthesis, perception, and signaling show reduced stomata in the hypocotyl (Fuentes et al., 2012; Gudesblat et al., 2012). Given the important role of hormones in stomatal development and movement, the knowledge of the hormonal pathways that control these processes, as well as their interaction, is of great importance for understanding the response of plants to environmental changes as well as for production of more efficient and climate resilient crops (Gasparini et al., 2021). Further work should elucidate the effect of elevated [CO2] on stomatal development in conjunction with hormonal biosynthesis, signaling, or transport mutants.

5 Sugar Signaling Controls Plant Hormones at Elevated CO2 Photosynthetic assimilation of CO2 is essential for plant metabolism, growth, and development (Orr et al., 2017). Plants take up CO2 from the atmosphere through the stomata and fix it into carbohydrates, providing a source of energy and organic building blocks for growth, biomass production, and substrates for metabolism (Hartmann & Trumbore, 2016; Osorio et al., 2014). Sugar content reflects a plant’s

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energy status, and the ability to sense sugar levels ensures plant adaptation and survival to environmental variations and stress conditions (Lastdrager et al., 2014). Thus, plants have evolved complex systems to sense sugar levels and modify their development and function accordingly (Li & Sheen, 2016). Atmospheric [CO2] is rising and is predicted to reach between 730 and 1020 ppm by 2100, which may in turn increase photosynthetic rate in C3 species resulting in increased carbohydrate production. Photosynthesis and carbon metabolism are under feedback control and a prime target of sugar signaling (Rolland et al., 2006). Additionally, regulatory interactions with plant hormones are an essential part of the sugar sensing and signaling network (Rolland et al., 2006). Thus, carbon availability has been identified as the key regulator of growth and development of plants submitted to elevated [CO2] (Huang et al., 2017; Teng et al., 2006). Sugars may trigger biosynthesis, degradation, transport, and signaling of most plant hormones, and hormones can act on pathways of sugar metabolism (Ćosić et al., 2021; Liu et al., 2015; Mishra et al., 2009; Perata et al., 1997; Wang & Ruan, 2013; Zhang & He, 2015). Thus, the crosstalk between sugars and hormones is important for controlling processes involved in plant growth and development, such as cell cycle, seed germination, hypocotyl elongation, seedling development, root growth, and phase transition (Gibson, 2004; Li, Ma, et al., 2016; Matsoukas, 2014). Elevated [CO2] can influence the same processes regulated by hormones and sugar, which suggests a close relationship between them. The carbon availability in plants grown at elevated [CO2] has been associated with cell division and expansion (Masle, 2000), flowering time (reviewed by Jagadish et al., 2016), and root architecture (reviewed by Thompson et al., 2017). Given that it is a biological event directly associated with hormones, the relationship between elevated [CO2], carbohydrate availability, and hormones has been become more evident (Fig. 2.1). Auxins play an important role in plant growth and development by regulating cell division, cell expansion, cell differentiation, lateral root formation, and flowering (Davies, 2010; Silva et al., 2018). At elevated [CO2], the increase in auxin, coupled with higher carbohydrate production, has been associated with shoot and root growth in Arabidopsis thaliana (Hachiya et al., 2014; Teng et al., 2006) and tomato seedlings (Wang et al., 2009). Auxin is also associated with root development at elevated [CO2]. Elevated [CO2] enhance root hair development via auxin signaling and transport that modulate root hair initiation and the expression of specific genes, such as CPC (CAPRICE) and TRY (TRIPTYCHON) (Niu, Jin, Chai, et al., 2011). Therefore, auxin-response mutants and auxin transport mutants do not show an increase in root hair development (Niu, Jin, Jin, et al., 2011). The elongation of root hairs is also associated with another plant hormone, ethylene (Pitts et al., 1998). In tomato, root growth and root hair development and elongation were associated with an increase in ethylene production and indolacetic acid (IAA) content at elevated [CO2] (Wang et al., 2009). The effect of ethylene on root growth is mediated by regulation of auxin biosynthesis and by modulating auxin transport machinery (Růzicka et al., 2007). A recent study showed that auxin acts downstream of ethylene and nitric oxide (NO) to regulate magnesium (Mg) deficiency-induced root hair morphogenesis (Liu et al., 2018). As well as Mg deficiency, elevated [CO2]

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Fig. 2.1 Schematic overview of the effects of elevated [CO2] on plant growth. Elevated [CO2] influences stomatal dynamics and stomatal development, which in turn modulates photosynthetic carbon assimilation. Photosynthetic production of carbohydrates is correlated with growth stimulation. Sugar availability is involved in the regulation of biosynthesis, conjugation, and/or transport of plant hormones, such as auxin, cytokinins (CKs), gibberellins (GAs), and brassinosteroids (BR)

could induce NO accumulation (Du et al., 2016; Jin et al., 2009), suggesting that the same pathway can be adopted to control root development under both conditions. However, some research has suggested that NO may act downstream in the auxin, ethylene, and CO2 (Correa-Aragunde et al., 2004; Lombardo et al., 2006; Niu, Jin, Chai, et al., 2011). In view of this, future research is needed to investigate the interaction between CO2, NO, auxin, and ethylene and their position in the pathway that regulates root development at elevated CO2. Elevated [CO2] generally results in plant growth acceleration (Jitla et al., 1997; Teng et al., 2006), which is associated with changes in development at the shoot apex (Jitla et al., 1997). CKs have been associated with growth acceleration due to their positive role in shoot meristem function and by promoting cell expansion and increasing the size of the meristem (Kiba et al., 2019; Werner et al., 2001). Elevated [CO2] significantly increased CK content in Arabidopsis (Teng et al., 2006). In cotton (Gossypium hirsutum), the increase in CK levels was detected in xylem sap, indicating that CK acts as a root-to-shoot signal under elevated [CO2] (Yong et al., 2000). The increase in CK at elevated [CO2] is directly associated with the availability of sugars generated by photosynthesis (Kiba et al., 2019). Thus, the increase in the availability of carbon induces de novo cytokinin biosynthesis for growth regulation at elevated [CO2]. As discussed earlier in this chapter, the relationship between ABA and elevated CO2 is still unclear due to contradictory results shown by some studies (Chater et al., 2015; Hsu et al., 2018a, 2018b; Merilo et al., 2013). Changes in carbohydrate

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availability have been suggested as a pathways in which ABA content is increased at elevated [CO2] (Chater et al., 2014, 2015). Thus, ABA could control stomatal development and movement under elevated [CO2] (Chater et al., 2015). However, soluble sugars are not positively correlated with ABA in winter wheat (Triticum aestivum) under elevated [CO2] (Huang et al., 2017). Besides, elevated [CO2] did not affect ABA levels in Arabidopsis (Kiba et al., 2019; Teng et al., 2006). Variation in hormone signaling may be linked to variation in plant responses to herbivores and pathogens under elevated [CO2] (Sun et al., 2013; Zhang et al., 2020). JA and SA mediate induced plant defense responses and are mutually antagonistic (Wei et al., 2014). In general, elevated [CO2] enhances SA acidmediated defenses and suppresses JA-mediated defense (Casteel et al., 2012; Li et al., 2013; Sun et al., 2013; Zhang et al., 2020). In soybean (Glycine max), elevated [CO2] increased the concentration of SA-regulated phenolics but decreased the concentration of JA-regulated cystein protease inhibitors (CysPI) (Zavala et al., 2009). As a main anti-herbivore mechanism, CysPI acts in soybean defense against insect herbivores, and its suppression, combined with an increase in leaf carbohydrates, potentially increases the susceptibility to chewing insects under elevated [CO2] (DeLucia et al., 2012). Although elevated [CO2] increases SA-mediate defense, it is not always able to suppress herbivores when JA-mediate defense is reduced (Sun et al., 2013). Plants can integrate photo-assimilate status with GA biosynthesis. This enables plant growth to be compatible with the environmental conditions and energy status (Paparelli et al., 2013; Prasetyaningrum et al., 2021). The synthesis of active GAs is reduced in mutants defective in starch synthesis or degradation that show dwarf phenotypes (Paparelli et al., 2013). A low amount of starch at night or the inability to use it results in reduced GA synthesis. This is due to downregulation of genes involved in GA biosynthesis, such as COPALYL DIPHOSPHATE SYNTHASE (CPS), ent-KAURENE OXIDASE (KO), and ent-KAURENE SYNTHASE (KS) (Paparelli et al., 2013). The exogenous application of GA can restore the growth of these plants; however, they show signs of sugar starvation. These results highlight the relationship between plant growth and starch metabolism, taken as an integrator of photosynthesis activity. Thus, under elevated [CO2], the increase in photosynthetic rates stimulates the production of non-structural carbohydrates in leaves which can lead to greater starch reserves, increased GA biosynthesis, and consequently plant growth. At elevated [CO2], an increase in GA concentrations was reported in Arabidopsis (Teng et al., 2006), Ginkgo biloba L. (Li et al., 2011), and Populus (Liu et al., 2014). However, the increase in growth induced by elevated [CO2] may be partially uncoupled from the effects of GA (Gasparini et al., 2019; Ribeiro et al., 2012). The reduction in growth of Arabidopsis treated with paclobutrazol (PAC, an inhibitor of GA synthesis) was reversed when the plants were exposed to elevated [CO2] (Ribeiro et al., 2012). In tomato, GA-deficient mutants restore growth after being transferred to elevated [CO2] at 21 days after germination (Gasparini et al., 2019). At elevated [CO2], changes in the expression of GA-related genes were negligible when compared with the ambient [CO2] (Ribeiro et al., 2012). Furthermore, elevated

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[CO2] did not affect the level of GA precursor (GA24) (Kiba et al., 2019). These results suggest that elevated [CO2] stimulates plant growth, at least in part in a GA-independent manner, and that GA may be required in the integration of carbon metabolism and plant growth only at ambient [CO2] (Ribeiro et al., 2012). In addition, other hormones or crosstalk between them can compensate for the lack of GA and thus stimulate growth: especially due to the overlapping functions (cellular activities and developmental process) and sharing of common signaling components between some plant hormones (Jaillais & Chory, 2010). BR and GA promote similar developmental response in plants. Mutants deficient in BR and GA show similar phenotypes, such as dwarfing, reduced seed germination, de-etiolation in the dark, and delayed flowering (Alabadí et al., 2004; Jianming et al., 1996; Steber & McCourt, 2001; Szekeres et al., 1996). GA-deficient mutants, GA-insensitive mutants, and plants treated with PAC are responsive to BR and partially recovered growth (Bai et al., 2012). In addition, BR rescues the germination phenotype of GA biosynthetic mutants and of the GA-insensitive mutant (Steber & McCourt, 2001). This suggests that BRs act downstream of GAs (GallegoBartolomé et al., 2012) and that BR can control growth and development in absence or reduced content of GA. Plant growth associated with BR is dependent on sugar availability (Zhang & He, 2015). Sugars regulate positively the transcription and stability of BRASSINOZALE-RESISTANT 1 (BZR1) transcription factors, which control BR-responsive gene expression (Zhang & He, 2015), and the relation between sugar availability and BR possibly is responsible for controlling the expression of BR-related genes at elevated [CO2] (Ribeiro et al., 2013; Rizi, 2014). In Arabidopsis thaliana, elevated [CO2] affect the BR-related gene expression in low and high GA plants (Ribeiro et al., 2013). Although GA is essential for growth at ambient [CO2], the plant capacity to regulate and adjust multiple hormonal signal pathways by carbon availability at elevated [CO2] can compensate the low levels of GA and stimulate plant growth. This highlights the remarkable hormonal flexibility in response to elevated [CO2] and how hormone sensing and signaling permit the fine-tuning of plant growth to changes in carbohydrate availability (Ribeiro et al., 2013).

6 The Effect of Elevated [CO2] on Plant Growth Is Growth Habit and Age Dependent The rise in atmospheric [CO2] could potentially fuel increased photosynthetic rates, which lead to growth acceleration, increase in biomass and productivity by higher carbohydrate availability, metabolic modifications, and flexibility in hormonal responses (Gasparini et al., 2019; Li et al., 2008; Ribeiro et al., 2012, 2013; Teng et al., 2006). In this way, elevated [CO2] can act as a natural fertilizer and benefit growth and yield of many crop species. Although biomass is generally increased in C3 plants under elevated [CO2], the effect of CO2 fertilization on plant growth has a

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Fig. 2.2 Factors affecting plants’ response to elevated [CO2]. The effect of elevated [CO2] on plant growth is dependent on time of exposure to CO2, plant age, and growth habit, as well as the combination of these factors. Long-term exposure to high CO2 may lead to acclimation of photosynthesis, especially in plants with determinate growth habit, which show reduced sink strength due to limited growth. Juvenile plants are more responsive to elevated [CO2] due to the greater ability of cells to divide, proliferate, and expand at this stage of development

large variation among different species. For example, fast-growing herbaceous C3 species respond more to elevated [CO2] than slow-growing C3 herbs or C4 plants, whereas CAM species and woody species show intermediate responses (Poorter & Navas, 2003). The most obvious reason for the variations in plant responses to elevated CO2 concentration is related to physiological differences in photosynthesis, such as CO2 concentrating mechanisms that increases the [CO2] at the Rubisco site in C4 plants. However, factors such as exposure time to CO2 (short- or long-term effects), plant age and growth habit are also involved in the response of plants to elevated [CO2] (Ainsworth et al., 2004; Christian et al., 2005; Gasparini et al., 2019; Reich et al., 2018) (Fig. 2.2).

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Although it is consensus that C3 species are more responsive to elevated [CO2], some studies have shown that not all C4 species are unresponsive to elevated [CO2] (Hager et al., 2016; Reich et al., 2018; Wand et al., 1999; Ziska & Bunce, 1997). Ten different C4 species were evaluated with respect to biomass accumulation and photosynthetic rate (Ziska & Bunce, 1997). Eight of them showed a significant increase in photosynthesis at elevated [CO2], and higher biomass accumulation was also observed for four C4 weeds (Ziska & Bunce, 1997). Meta-analysis study of C3 and C4 response to elevated [CO2] in Poaceae reported biomass increase of 44% and 33% in C3 and C4, respectively, in response to elevated [CO2], suggesting that responses to [CO2] are not necessarily related to the photosynthetic mechanism (Wand et al., 1999). A recent study showed that long-term exposure to elevated [CO2] can reverse the pattern of biomass response between C3 and C4 grasses over a period of 20 years (Reich et al., 2018). As expected, over the first 12 years at elevated [CO2], biomass was only increased in C3 plants, but during the subsequent 8 years, the pattern reversed and biomass was increased in C4 but not in C3 plants (Reich et al., 2018). Thus, time of exposure to CO2 can modulate in different way or time the plant response to elevated [CO2]. As most of studies are conducted under shortterm perspective, the plant’s response to CO2 may not be detected in some of them, especially in plants with a long life cycle. Plant growth depends on factors controlled by the stage of development, which limits growth to specific periods (Sloan et al., 2009). Cell expansion, an important cellular process for plant growth, is a result of turgor pressure and irreversible cell wall extension. Addition of new extracellular polymers and remodeling of existing components in the primary cell walls mark the exponential phase of cell expansion. This is followed by cell wall thickening and rigidification to create secondary cell walls that enhance structural integrity, but reduce cell wall extension (Hall & Ellis, 2013). The transition from the juvenile to the adult phase, which is preceded by a change in the competence of the shoot to respond to stimuli, can determine plant architecture and growth (Poethig, 2013). The changes in meristem identity during phase transition are accompanied by genetic reprogramming that may trigger changes in leaf and stem morphology, as well as alteration in growth rate (Poethig, 2013). Mature deciduous forest trees showed no increase in stem growth and leaf production when exposed to elevated [CO2] (Christian et al., 2005). A recent study showed that the effects of elevated [CO2] on plant growth may be age-dependent (Gasparini et al., 2019). Tomato plants deficient in GA have their reduced growth restored when exposed to elevated [CO2] at 21 days after germination (DAG). However, restoration of growth was not observed when the same plants were subjected to elevated [CO2] at 35 DAG (Gasparini et al., 2019). In Arabidopsis, the most pronounced growth under elevated [CO2] was observed during the vegetative stage (Watanabe et al., 2014). This suggests that the stimulation of growth by elevated [CO2] is possibly associated with the stage of plant development. The source-sink ratio is another factor influencing plant response to elevated [CO2], specially photosynthesis (Ainsworth et al., 2004; Arp, 1991). Although studies have shown that elevated [CO2] generally stimulated photosynthetic rate, other studies reported reduction in photosynthesis when plants are exposed to long-

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term elevated [CO2] (Adam et al., 2004; Ainsworth et al., 2004; Zheng et al., 2019). The downregulation of photosynthesis at elevated [CO2] is usually associated with leaf carbohydrate accumulation, which acts as a signal to repress genes related to photosynthesis (Drake et al., 1997; Moore et al., 1999). Thus, carbohydrate utilization by metabolic activity and/or storage sink activity is the key to sustaining photosynthetic activity at elevated [CO2] (Clough & Peet, 1981). The plant growth habit (determinate or indeterminate) has been associated with variation in growth responses of Glycine max under elevated [CO2] (Ainsworth et al., 2002, 2004). Significant acclimation of photosynthesis was only observed in non-nodulating and determinate soybean cultivars, named Williams-NN and Williams-dt1, respectively (Ainsworth et al., 2004). These traits may limit the size of the sink for carbon and thus contribute to the downregulation of photosynthesis. Although the soybean Elf cultivar also shows determined growth, no loss in photosynthetic capacity was observed at elevated [CO2]. This contrasting result between two cultivars of determinate growth is due to the capacity of Elf to produce many pods on branches and in the main stem, which avoids sink limitation and downregulation of photosynthesis (Ainsworth et al., 2004).

7 Hormonal Responses of Plants to Biotic and Abiotic Stresses Under Elevated [CO2] Plants have mechanisms for adjusting to environmental conditions that range from short-term responses like stomatal closure to long-term changes in metabolism and gene expression. These changes are mediated by hormones, which therefore play a fundamental role in plants’ response to stress conditions (Devireddy et al., 2021; Huang et al., 2018; Wani et al., 2016) (Fig. 2.3). As a rule, elevated [CO2] is believed to mitigate the severity of many abiotic and biotic stresses. Among the former, there is an increase in plant tolerance to water deficit and salinity and protection against high temperatures and against nutritional deficiency (Brito et al., 2020; Jin et al., 2009; Li et al., 2015; Li, Kristiansen, et al., 2019). The interaction between biotic factors and elevated [CO2], on the other hand, seems to be more ambiguous. Elevated [CO2] can either stimulate defense mechanisms of plants against pathogens (Mathur et al., 2018; Zhang et al., 2015; Zhou et al., 2019), increase the incidence of disease and insects attack (Guo et al., 2012; Sun et al., 2013; Zhang et al., 2015), or have no discernible effect (Hall et al., 2020; Zhou et al., 2019). As explained in previous sections, elevated [CO2] stimulates plant growth, alters metabolite flow and energy balance (Li et al., 2018; Zhuang et al., 2019), increases antioxidant system defenses, and induces cell damage decline (AbdElgawad et al., 2015; Martins et al., 2016; Pérez-López et al., 2009), modifies water relations of roots and shoots (Fang et al., 2019; Liu et al., 2020), increases photosynthesis (Hussin et al., 2017; Zaghdoud et al., 2016), and induces stomatal closure (Yi et al., 2015; Yu et al.,

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Fig. 2.3 Schematic summary of known hormonal responses to abiotic and biotic stress under elevated [CO2]. Although some hormonal patterns are similar, the stress response is dependent on the plant species and the intensity and type of stress. In general, under some abiotic stress, ABA synthesis increases rapidly. However, at elevated [CO2], tomato plants maintain growth under salt stress via reduced concentration of abscisic acid (ABA) as well as reduced content of the ethylene (ET) precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), in leaves and roots (Brito et al., 2020). Regarding biotic stress, in general, elevated [CO2] increases salicylic acid (SA) biosynthesis and reduces jasmonic acid (JA) and ethylene levels and their respective signalling pathways

2014). All these effects, alone or in combination, may affect a plant’s response to biotic stressors. Drought and soil salinity are among the abiotic factors with the greatest impact on plant growth and crop yield. Elevated [CO2] triggers significant morphophysiological changes that may ensure drought mitigation (Hebbar et al., 2020; Wei, Fang, et al., 2021; Zaghdoud et al., 2016). In general, ABA plays a central role in controlling tolerance responses to reduced water availability, from triggering stomatal closure to altering gene expression patterns. The reduction of water vapour loss by ABA-induced stomatal closure occurs through a signaling cascade involving ABA receptors of the PYR/PYL/SCAR family and protein kinases of the OST1/ SnRK2 family (Cotelle & Leonhardt, 2019). The stomata are also sensitive to high levels of CO2, and elevated [CO2]-induced stomatal closure signaling pathways involves ABA biosynthesis, as well as ABA-independent mechanisms through carbonic anhydrases, a signaling cascade (MPK4, HT1, RHC1) and an increase in ROS (Hsu et al., 2018a, 2018b; Ma & Bai, 2021; Zhang et al., 2018). Under drought and salinity, elevated [CO2] can enhance stomatal responses, increasing water use efficiency—WUE (Li, Zhang, et al., 2019; Wang et al., 2018). However, the

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mechanisms that involve stomatal adjustments as a function of elevated [CO2] and ABA concentration are notoriously species-specific and are dependent on growth condition and the intensity of stress.

8 Elevated [CO2] and Hormonal Responses of Plant Abiotic Stresses: Drought, Heat, and Soil Salinity When studying the effect of progressive drought on soils, Wei et al. (2020) reported that elevated [CO2] can increase ABA in the shoot of barley (Hordeum vulgare) and tomato plants under progressive soil dehydration, which would lead to a more effective reduction in stomatal conductance. On the other hand, in response to progressive drought, tomato plants had delayed photosynthesis and stomatal responses when subjected to elevated [CO2] in relation to plants in ambient [CO2] (Liu et al., 2019). In addition, the results of this study also indicate that under elevated [CO2], plant responses to moderate drought are independent of ABA (Liu et al., 2019). By contrast, in soybean plants grown under water deficit, elevated [CO2] improves WUE mediated by ABA-induced reduction in stomatal conductance, but not sufficiently to promote gains in net photosynthesis (Li et al., 2020). Furthermore, the evaluation of ABA-deficient mutant plants ( flacca in tomato and Az34 in barley) demonstrated that ABA is essential for increasing WUE and nitrogen use efficiency (NUE) under drought stress, regardless of the [CO2] condition (Wei, Fang, et al., 2021). Another recent publication suggests that elevated [CO2] can reduce the concentration of ABA and ACC (1-aminocyclopropane-1-carboxylate, the ethylene precursor) in leaves of tomato plants under conditions of progressive salinity in soils (Brito et al., 2020). Plants subjected to elevated [CO2] were able to keep their stomata open under variable conditions of temperature, irradiance, and relative humidity (Brito et al., 2020). Consistent with this, Shokat and collaborators observed less pronounced decreases in stomatal conductance and transpiration in water-deficient wheat plants under elevated [CO2] compared to ambient [CO2], suggesting that plants under elevated [CO2] may support a certain level of physiological activity (Shokat et al., 2021). In addition to the stomatal effect, there is a threshold under the endogenous ABA concentration that promotes vegetative growth and biomass breakdown (Humplík et al., 2017; Thompson et al., 2007). ABA can, to some extent, stimulate plant growth, but under high concentrations it inhibits growth (Luo et al., 2014; Thompson et al., 2007). On the other hand, the effect of elevated [CO2]-induced growth seems to be not only related to the control of ABA biosynthesis, but directly related to the energy input of carbon under stress conditions. In water deficit, coffee (Coffea arabica) plants show better use of carbon due to elevated [CO2], which stimulates root growth, even under high levels of ABA (Avila et al., 2020). Nevertheless, the reduction of ABA levels in tomato tissues under salt stress was associated with increases in total biomass when subjected to elevated [CO2] (Brito et al.,

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2020). In line with this, Piñero et al. (2014) reported that an increase in [CO2] favored the reduction of ABA levels in sweet pepper (Capsicum annuum) roots grown in saline nutrient solution, accompanied by an increase in the concentration of auxins. There was also a significant increase in the concentration of total CKs in the roots under elevated [CO2], which is related to better N uptake by the roots under salinity conditions (Piñero et al., 2014). Elevated [CO2] not only regulates the maintenance of lower ABA levels under water deficit, but favors increases in CKs and JA in creeping bentgrass (Agrostis stolonifera L.), which was associated with improved performance of tillers and stolons (Burgess et al., 2019). Under drought and ambient [CO2] conditions, growth inhibition of Kentucky bluegrass rhizomes (Poa pratensis L.) and A. stolonifera L. tillers seems to be linked to high auxin concentration (Burgess et al., 2019; Chapman et al., 2020). However, under elevated [CO2], the growth of these organs is larger and was associated with lower levels of auxins (Burgess et al., 2019; Chapman et al., 2020). In cucumber (Cucumis sativus) seedlings, CO2 enrichment regulated an increase in root growth, which may have been affected by the reduction of ABA levels in moderate drought, to the detriment of the increase in GAs, a growth stimulator (Li, Feng, et al., 2020). In this study, regardless of CO2 concentration, auxin and CK levels were reduced under moderate drought, indicating that the stimulation of cell growth and division controlled by these hormones was affected (Li, Li, et al., 2020). Furthermore, CKs are related to the induction of plant growth, since elevated [CO2] mediates the high production of sugars from photosynthesis, thus stimulating the de novo synthesis of CKs (Kiba et al., 2019). Forecasts indicate that by 2050 there will be an irreversible increase in average global surface temperature of 1.5 °C above pre-industrial levels (IPCC, 2021). Higher temperatures can induce heat stress in plants, which results in crop growth and productivity reductions by limiting photosynthetic capacity (Gray & Brady, 2016; Song et al., 2014; Tan et al., 2011). Studies demonstrate that elevated [CO2] modulates acclimatizing responses to high temperature stress by inducing hormonal changes (Li et al., 2015; Pan et al., 2019). Li et al. (2015) highlight that in tomato plants, a minimal concentration of ABA is essential to reduce the impacts of heat stress; however, the induction of thermotolerance by elevated [CO2] occurs through the mitigation of oxidative stress and reduction of damage caused to the photosynthetic apparatus in ABA-independent pathways (Li et al., 2015). Likewise, Li, Kristiansen, et al. (2019) analyzed wheat genotypes with contrasting tolerance to high temperatures and found that elevated [CO2] does not control ABA levels in any of the genotypes under high temperature (Li, Zhang, et al., 2019). Elevated [CO2] also alleviates the effects of heat stress by modulating guard cell movement in tomato leaves (Zhang et al., 2019). Under elevated [CO2], tomato plants showed high gene expression of RBOH1 (RESPIRATORY BURST OXIDASE 1), which, by promoting the production of apoplastic H2O2, induces stomatal closure and therefore controls water loss through excess transpiration (Zhang et al., 2019). In addition to the stomatal factor, the acclimatization responses of tomato plants to heat under elevated [CO2] are strongly related to the increase in ethylene biosynthesis and signaling (Pan et al., 2019). Ethylene production is able to regulate the expression of

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chaperones such as heat shock proteins (HSP) relieving heat damage (Pan et al., 2019). Abo Gamar et al. (2019) carried out a robust study in Arabidopsis using WT and ABA-insensitive mutant (abi1-1) plants, where the effects of elevated [CO2] and high temperature and water deficit were evaluated combined and in isolation. They found that biomass gain and plant growth in response to elevated [CO2] were higher in WT plants than in abi1-1 mutants. In addition, elevated [CO2] helped plants under heat and water deficit by reducing oxidative damage and improving water status. Interestingly, ethylene biosynthesis was upregulated under elevated [CO2], highlighting its involvement in mitigating water and heat stresses (Abo Gamar et al., 2019). On the other hand, CKs also seem to be related to better performance of wheat plants under heat stress when subjected to elevated [CO2], which may be associated with an increase in antioxidant capacity, defense against oxidative stress, and improvement in photosynthetic rates (Shokat et al., 2021). Under low pH condition and low N in the soil, the rise of [CO2] induces the development of lateral roots (LR) by regulating the levels of auxins and CKs (Hachiya et al., 2014). At low pH, plants accumulate carbon from photosynthesis due to elevated [CO2], which stimulates the biosynthesis and transport of auxins from the shoot to the roots and represses the inhibition of lateral root growth by CKs (Hachiya et al., 2014). Furthermore, low N availability induces preferential root growth increases and LR growth under elevated [CO2] due to high N depletion, which may be associated with the auxins/CKs balance (Hachiya et al., 2014). In response to elevated [CO2] and low N availability, the biosynthesis and distribution of CKs via xylem is essential to control the development of shoots and roots of cotton plants in this type of stress (Yong et al., 2000). In contrast, studies show that elevated [CO2] mitigates the effects of ammonium (NH4+) toxicity by the coordinated increase of transcripts related to ethylene biosynthesis and signaling (ACC synthase and ACC oxidase), as well as the increase of auxin-responsive genes (Vega-Mas et al., 2017).

9 Elevated [CO2] and Hormonal Responses of Plant Biotic Stresses: Pathogens and Insects As much as 5% of all annual terrestrial primary production is consumed by herbivores (Turcotte et al., 2014), and rates of herbivory are higher in croplands than in the wild (Welter & Steggall, 1993). The induction of defenses against pathogens and insect herbivory depends on SA-, JA-, and MeJA-dependent responses, as well as involving ABA and ethylene (Kazan, 2018; Zhou et al., 2017). Studies have reported diverse effects in relation to plant resistance to biotic attacks on plants under elevated [CO2], which have a strong influence on hormone levels (Roy & Mathur, 2021; Zavala et al., 2013). There is a consensus, although dependent on species and environmental factors, that elevated [CO2] controls increased SA biosynthesis and defense signaling depends on SA in contrast to the reduction of JA/ethylene levels

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and their respective signal pathways (Casteel et al., 2012; Guo et al., 2012; Hall et al., 2020) (Fig. 2.3). The endogenous elevation of SA under elevated [CO2] can reduce the incidence and severity of Tomato yellow leaf curl virus (TYLCV) in tomato plants (Huang et al., 2012). However, although SA and JA usually display antagonistic responses, it has been observed that, under elevated [CO2], control of TYLCV infection is highly regulated by both SA and JA (Huang et al., 2012). In this same context, elevated [CO2] increases the constitutive and induced defenses against the fungal pathogen Alteria brassicae in Brassica juncea plants, through the joint regulation of SA and JA (Mathur et al., 2018). The role of SA in defense responses to plant pathogens in elevated [CO2] is related to the activation of the phenylpropanoid pathway, regulated by phenylalanine ammonia-lyase (PAL) activity, which is responsible for the increase of phenolics and flavonoids (defense compounds) (Li, Kristiansen, et al., 2019; Mathur et al., 2018; Matros et al., 2006). It was observed that in Arabidopsis, common beans (Phaseolus vulgaris), barley, and wheat total SA was stimulated in elevated [CO2] and resulted in improved resistance to inoculation of bacteria and fungi (Mhamdi & Noctor, 2016). In addition, elevated [CO2]-dependent responses have been linked to effective signaling of cellular redox status (e.g., variations in oxidized and reduced forms of glutathione, NAD(P)H) (Mhamdi & Noctor, 2016). In contrast to the accumulation of SA, the reduction of JA induced by elevated [CO2] leads plants of Camellia oleifera to increase susceptibility to anthracnose caused by Colletotrichum gloeosporioides (Li, Ahammed, et al., 2016). In this work, Li, Ma, et al. (2016) demonstrated that caffeine, an alkaloid involved in defense responses against C. gloeosporioides, is reduced in conditions of elevated [CO2] and inhibits the biosynthesis of JA. In maize (Zea mays) under elevated [CO2], the increase in SA was accompanied by suppression of JA biosynthesis and lipoxygenase defense genes (Vaughan et al., 2014). Interestingly, plant-induced defense responses are variable, depending on the growth habits of pathogens, for instance, biotrophs, (hemi)biotrophs, and viruses increase SA-induced signaling, while necrotrophs increase JA/ethylene-mediated responses (Zhang et al., 2015; Zhou et al., 2019). Tomato plants show decreased incidence and severity of Tobacco mosaic virus (TMV) and (hemi)biotrophic Pseudomonas syringae infection under elevated [CO2], associated with increased expression of genes related to SA signaling (Zhang et al., 2015). The repression of elevated [CO2]-mediated JA biosynthesis and signaling may increase the susceptibility of tomato plants to the necrotrophic pathogen Botrytis cinerea (Zhang et al., 2015). However, this joint response of resistance to pathogenic habit under elevated [CO2] may vary according to plant species. For example, in Arabidopsis the defense response to P. syringae was reduced in elevated [CO2], where a reduction of SA-dependent defense marker gene transcripts was observed, while elevated [CO2] induced increased responses to B. cinerea, which was accompanied by an increase in JA-responsive resistance marker genes (Zhou et al., 2019). P. syringae infection in A. thaliana is increased in elevated [CO2] due to increases in ABA after infection (Zhou et al., 2017). ABA signaling triggers coronatin responses and allows post-infection reopening of the stomata (Zhou et al., 2017).

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Under elevated [CO2], inhibition of JA and its responsive genes may reduce plant resistance to attack by insect herbivory (Guo et al., 2012; Hall et al., 2020). Zavala et al. (2008) report that elevated [CO2] favors the attack of Diabrotica virgifera and Popillia japonica by the attenuated effects of LOX and ACC synthase gene expression. Furthermore, Sun et al. (2013) found that elevated [CO2] increases the level of infective responses against aphids through increased biosynthesis and SA signalling and repression of JA and ethylene signaling. The relationship between plant susceptibility to aphids under elevated [CO2] is coordinated by the suppression of ethylene biosynthesis and signalling (ACC synthase and ethylene response transcription factors, ERF) as well as its positive relationship with nitrogen assimilation by plants (Guo, Sun, Li, Liu, Zhang, & Ge, 2014b). Legume species like Medicago truncatula, poorly responsive to ethylene and with high nodulation activity, are more susceptible to aphids mainly in elevated [CO2] (Guo, Sun, Li, Liu, Zhang, & Ge, 2014b). Similarly, elevated [CO2] increased the growth rate of aphids in infestation of M. truncatula plants while increasing the SA response and reducing the effective defense responses induced by JA and ethylene (Guo, Sun, Li, Liu, Wang, et al., 2014a).

10

Conclusions

Elevated atmospheric [CO2] induces multiple changes in plant growth that are mediated by several hormones, including ABA, auxin, CK, ethylene, GA, JA, and SA. Elevated [CO2], for instance, induces stomatal closure through changes in ABA levels. Moreover, ABA levels are essential to facilitate, maintain, and accelerate the stomatal response to CO2 elevation; however, other hormone signaling pathways and their interactions with atmospheric [CO2] deserve to be further explored. Elevated [CO2] plays an important role in plant defense response, modulating SAand JA-mediated defenses. In addition, elevated [CO2] increases auxin levels and the photosynthetic carbon gain of plants and can thus enhance shoot and root growth. Both elevated [CO2] and sugars affect the biosynthesis of CK and GA, which may regulate plant growth. Factors such as plant age and growth habit are also involved in the response of plants to elevated [CO2]. Further research on molecular and physiological aspects of plant growth is needed to improve our understanding of how elevated [CO2] affects hormone signaling pathways, carbon allocation, source-sink relations, and ultimately crop yield. This improved understanding may inform crop breeding for future levels of elevated [CO2] and, thus, contribute to food security over the course of this century.

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Chapter 3

Role of Plant Hormones in Plant Response to Elevated CO2 Concentrations: Above- and Below-ground Interactions Estibaliz Leibar-Porcel and Ian C. Dodd

1 Introduction Many countries have committed to increase resilience to climate risks through adaptation and mitigation policies in the agriculture sector. By growing selected food crops in a semi-controlled environment that regulates aerial environmental conditions, protected horticulture can to some extent mitigate the climate change effects on food production. This sector is growing in value, and it is estimated that there are around 173,561 ha of greenhouses in Northern Europe (Hickman, 2018). In winter when low radiation conditions prevail, canopy photosynthesis of these densely packed crops can result in critically low aerial CO2 concentrations (Singh et al., 2020). Therefore, many greenhouses supplement the air with carbon dioxide to increase photosynthesis, thereby increasing crop production. Based on the species and crop growth stage, and also growth conditions such as light intensity, temperature and vent position, CO2 levels are generally maintained at 700–1000 ppm CO2 but can be elevated up to 1500 ppm CO2 (Dunn & Poudel, 2017). These greenhouses periodically open their vents, to prevent excessive humidity accumulating (which provides favourable conditions for foliar disease development) and supra-optimal temperatures under high radiation conditions, thereby releasing CO2 to the atmosphere (Körner & Challa, 2003). Thus routine greenhouse operation (a climate mitigation strategy) may therefore actually contribute to climate change. Hence it is essential to maximise the efficiency of CO2 enrichment in greenhouse production systems. Maximum CO2 emission levels have been set by governments for various industrial sectors, including the greenhouse sector (Defra., 2012). Boiler, combined heat and power (CHP) and furnace exhaust gases, flue gases of

E. Leibar-Porcel · I. C. Dodd (*) Lancaster Environment Centre, Lancaster University, Lancaster, UK e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_3

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conventional gas boilers and liquefied pure gas are all sources of CO2 for enrichment (Adams et al., 2009). All these CO2 sources have quite a high energy cost that can reach up to £200,000 per year for a 5-hectare glasshouse (Pratt, 2011). While summer time coincides with high light intensities potentially allowing plants to make the best use of additional CO2, periods of high ventilation are often required to prevent excessive greenhouse temperatures. Thus, CO2 enrichment can be expensive and inefficient as a result of CO2 losses to the environment (De Zwart, 2012). This is likely to become more prominent when the frequency of necessary ventilation increases due to the predicted rise in heat waves (Bisbis et al., 2018a, 2018b). Maintaining CO2 concentrations inside the greenhouse can be challenging if the vents are continuously and completely open, since CO2 escapes through the vent. Despite technical improvements by growers to minimise spending and maximise production, further opportunities may exist by better understanding how CO2 regulates plant growth and development and evaluating alternatives to conventional aerial CO2 enrichment. Irrespective of which part of the plant is exposed to elevated CO2, plant hormone concentrations and their interactions with other signalling pathways (such as sugar and nitrogen) seem important in adjusting plant growth to prevailing environmental conditions. Within this book chapter, we firstly examine the impacts of high aerial CO2 concentrations on plant hormone status and its relationship to shoot development and physiology. In some cases, parallel measurements of shoot and root hormone concentrations have established conserved hormonal responses. Nevertheless, it is important to also understand pathways of CO2 transport in planta, as a prelude to determining the viability and effects of CO2 enrichment in root zone (RZ), which may offer a more targeted solution. While we preferentially focus on examples from commercial greenhouse crops (e.g. cucumber, lettuce, pepper, tomato), studies with arable crops (e.g. rice, wheat) and model species (e.g. Arabidopsis) are included to expand the literature, especially when using model species substantially enhances our understanding of the responses of plants to elevated CO2.

2 Elevated Atmospheric CO2 Effects on Phytohormones High aerial CO2 has variable effects on plant growth and performance, even in the same species (Hasegawa et al., 2013). If plants become nutrient-limited (Igarasahi et al., 2021) or root-restricted (Schaz et al., 2014), CO2-accelerated growth rates may not be sustained. Some phytohormones are vital in regulating stomatal aperture, and plant growth as well as development and their in vivo concentrations have been measured in some investigations in response to aerial CO2 enrichment. Elevated CO2 (eCO2) can enhance total leaf area by promoting leaf expansion (Ferris et al., 2001; Taylor et al., 1994), and phytohormones seem to be involved in such growth responses. The concentrations of some phytohormones including leaf indole-3acetic acid (IAA), gibberellic acid (GA3), trans-zeatin (ZR), dihydrozeatin

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Fig. 3.1 Changes in leaf hormone concentration of Arabidopsis thaliana in response to elevated CO2 (eCO2). Phytohormone concentrations of plants grown with elevated CO2 are divided by hormone concentrations of plants grown with ambient CO2, so values greater than 0 mean that eCO2 increases hormone concentrations, while values less than 0 mean that eCO2 decreases hormone concentrations. Data are from Teng et al. (2006)

(DHZR), isopentenyl adenine (iPA) (Fig. 3.1) and ethylene (Seneweera et al., 2003; Teng et al., 2006; Wang et al., 2009) increased under eCO2; alternatively, in vivo concentrations of the “stress hormones” abscisic acid (ABA) and jasmonic acid (JA) decreased (Guo et al., 2012; Li et al., 2006). Nevertheless, relatively few of these studies have considered whether changes in phytohormone concentrations regulate plant growth, in part because fully expanded leaves were often sampled. While recognising that individual plant hormones can exert effects on the biosynthesis and signalling of other hormone groups, it is instructive to first review the changes that occur.

2.1

Auxins and CO2

Different processes such as stem cell maintenance, embryo development, shoot and root architecture, and tropic growth responses are all regulated by IAA, the key auxin in plants (Davies, 2010). Total leaf area per plant often expands in response to eCO2, by stimulating both leaf thickness and individual leaf area (Pritchard et al., 1999). IAA mediates multiple processes that determine leaf growth, including leaf primordia initiation (Reinhardt et al., 2000), vascular differentiation (Sieburth, 1999) and leaf expansion during both the cell division (Ljung et al., 2001) and cell expansion of leaf growth phase (Braun et al., 2008).

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Root to shoot ratios usually increase under eCO2 as a result of unequal organ growth (Ainsworth & Long, 2005). Foliar sugar accumulation under elevated CO2 stimulates shoot IAA biosynthesis, with long-distance IAA signalling from shoot to roots (Lilley et al., 2012; Sairanen et al., 2012) stimulating not only root growth but also root hair development in tomato (Solanum lycopersicum L.) and Arabidopsis thaliana (Hachiya et al., 2014; Niu et al., 2011) seedlings (Wang et al., 2009). Conversely, IAA decreased almost fivefold in roots of sweet pepper (Capsicum annuum L.) subjected to increased (800 ppm) CO2 (Piñero et al., 2014), highlighting the variability in hormonal response.

2.2

Cytokinins and CO2

Cytokinins (CKs) increase cell division and are involved in the development of embryos, vascular tissue and root architecture and also regulate responses to light (Kieber & Schaller, 2014). Meristematic regions (young leaves, roots, seeds and developing fruits) have the highest CK concentrations (Shani et al., 2006; Taiz & Zeiger, 2010). While total root cytokinin concentration (Z, tZR, DHZ, cZR, DHZR, iP and iPR) did not differ between sweet pepper plants grown and 400 and 800 ppm CO2, total leaf cytokinin concentration decreased threefold (Piñero et al., 2014). In contrast, leaves of A. thaliana grown at eCO2 (700 ppm) had significantly higher levels of ZR, DHZR and iPA-type CK concentrations (by 16%, 56% and 75%, respectively) than those grown at ambient CO2 (370 ppm) (Teng et al., 2006). Within 2 days of exposure, eCO2 (780 ppm) doubled shoot concentrations of iP-type CK precursors and increased the concentrations of tZ-type CK precursors by 50%, compared to A. thaliana plants grown at pre-industrial CO2 concentrations (280 ppm), when plants were grown in soil (Kiba et al., 2019). Shoot cytokinin accumulation was even more rapid (within 6 h) when plants were grown on agar plates, although cytokinin biosynthesis genes (IPTs) were not upregulated during this time (Kiba et al., 2019), focusing attention on the roots. Roots exposed to eCO2 also accumulated CKs to a similar (iP-type CK precursors) or greater (tZ-type CK precursors) level than the shoots, in this case coincident with the upregulation of two genes (AtIPT3 and CYP735A2) responsible for de novo CK synthesis (Kiba et al., 2019). This upregulation was abolished by darkness or adding photosynthetic inhibitors and could be mimicked by adding sugars to the roots, suggesting that sugars generated in the shoots by photosynthesis (and subsequently transported to the roots) regulated root gene expression (Kiba et al., 2019). While these results imply that sugar-mediated cytokinin biosynthesis is more sensitive in the roots, they also have implications for root-to-shoot CK signalling. Compared to plants grown at ambient CO2, elevated CO2 enhanced tZ-type CK transport to cotton leaves to a greater extent at low (2 mM) than at high (12 mM) nitrogen supply (Yong et al., 2000), with soil N availability also upregulating root expression of CK biosynthesis genes (Sakakibara, 2021). Similarly, root-to-shoot CK delivery was greater under high (700 ppm) CO2 than plants

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grown under control conditions (Schaz et al., 2014). Thus root CK biosynthesis integrates both local (N availability) and systemic (assimilate transport from the shoots) signals, to modulate shoot growth responses.

2.3

Gibberellins (GAs) and CO2

Elongation of leaves, stems and reproductive organs is a primary role of the gibberellins (Colebrook et al., 2014), with increased wall extensibility that promotes cell expansion (Cosgrove & Sovonick-Dunford, 1989). Moreover, both cell division (number) and cell expansion (length) increased under eCO2 (Luomala et al., 2005; Taylor et al., 2003) consistent with the known effect of GAs (Yang et al., 1996). Foliar gibberellic acid (GA3) concentrations of rice were maximal at 600 ppm CO2, with lower concentrations at 400 and 800 ppm CO2 (Qi et al., 2021). Elevated CO2 (700 ppm) increased foliar GA3 concentrations in the model plant Arabidopsis by 55%, associated with 29% higher growth rate than at ambient (350 ppm) CO2 (Teng et al., 2006). Elevated CO2 effects on the growth of plants seem partly associated with the gibberellin effects, with paclobutrazol (GA biosynthesis inhibitor)-mediated growth inhibition partially reverted under high (750 ppm) CO2 (Ribeiro et al., 2012). Furthermore, eCO2 (750 ppm) partially reverted the phenotype of the dwarf gib-1 tomato mutant when applied 21 days after germination, but had no effect in older (35 days after germination) plants (Gasparini et al., 2019), possibly linked to phenological changes in hormone sensitivity as the latter plants flowered. Proteomic studies indicated that rice leaves could perceive GA3 and transduce a signal that activates cell growth and division (Wang et al., 2013), but it is unknown if eCO2 can also stimulate this signal.

2.4

Jasmonic Acid (JA) and CO2

Jasmonates (whose biosynthesis is described in Wasternack & Hause, 2013) play an important role in regulating plant defence responses against herbivory. Tomato and rice plants with mutations in genes involved in JA biosynthesis or signalling are less resistant to herbivory (Wang et al., 2013; Wasternack & Hause, 2013). Synthesis of jasmonates is in part regulated by intercellular CO2 levels (Zavala et al., 2013), with elevated CO2 generally repressing the JA pathway at the whole plant level. Soybean leaves grown under eCO2 (550 ppm) were less able to produce JA (Zavala et al., 2008), although there was substantial variation between different cultivars with some maintaining their constitutive JA levels (Casteel et al., 2012). Very high CO2 concentrations (5000 ppm) had no statistically significant effect on wheat shoot JA concentrations (Jiang et al., 2017), while foliar JA concentrations increased with aerial CO2 concentrations (400–800 ppm CO2) in rice (Qi et al., 2021). Guard cells of Brassica napus and A. thaliana grown under eCO2 (800 ppm) had elevated

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levels of JA biosynthesis pathway metabolites, with JA-Ile (JA-isoleucine) and JA signalling assumed to induce stomatal closure under eCO2 (Geng et al., 2016). In roots, eCO2 (680 ppm) enhanced the concentrations of JA-Ile and JA in winter wheat throughout early vegetative development (Huang et al., 2017). Nevertheless, Arabidopsis grown at a range of CO2 concentrations (150, 400, 800 ppm) showed no differences in sensitivity to the soil fungal pathogens Fusarium oxysporum f sp. raphani and Rhizoctonia solani, despite eCO2 increasing expression of PDF1.2 for JA-dependent defences (Zhou et al., 2019). The spatial location of this increased gene expression was not clear, possibly explaining why eCO2 did not affect the disease phenotype. These interactions warrant further experiments, since eCO2 can enhance susceptibility to soilborne diseases such as Fusarium (Melloy et al., 2014).

2.5

Salicylic Acid and CO2

Salicylic acid (SA) is a secondary metabolite (phenylpropanoid derivative) and mainly functions as a signal molecule to mediate plant-biotic interactions (Mhamdi & Noctor, 2016). Exposing plants to eCO2 markedly promotes SA concentrations in several plant species including A. thaliana, tomato (S. lycopersicum) and soybean (Glycine max) (Casteel et al., 2012; Mhamdi & Noctor, 2016; Zhang et al., 2015). On the contrary, SA concentrations did not increase in barley (Hordeum vulgare) and tobacco (Nicotiana tabacum) when grown under eCO2 (Matros et al., 2006; Mhamdi & Noctor, 2016). Wheat plants maintained at a suboptimal CO2 concentration (170 ppm) had a higher foliar SA concentration than their counterparts grown at 390 or 680 ppm CO2, but there was no consistent effect of CO2 levels on stem or root SA concentrations. Whether these changes affect interactions with pest and diseases is best addressed using mutants in SA biosynthesis. While endogenous SA and SA signalling are essential for eCO2-promoted stomatal closure, this hormone is not required for eCO2-inhibited stomatal opening (He et al., 2020).

2.6

Abscisic Acid and CO2

Abscisic acid (ABA), derived from carotenoid pigments, is synthesised when plants are exposed to (atmospheric and soil) water deficits. ABA biosynthesis and catabolism in different tissues, and transport between roots and shoots, regulate tissue ABA concentrations in vivo (Jiang et al., 2010). Endogenous ABA concentrations show variable responses to elevated CO2, according to the plant species, tissue analysed and whether additional stresses such as soil drying are imposed. Root ABA concentrations of cucumber (Li et al., 2020) and pepper (Piñero et al., 2014) plants were not changed in response to elevated (800 ppm) CO2. Whereas pepper leaf ABA concentrations were similarly unresponsive to elevated CO2 (Piñero et al.,

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2014), rice leaf ABA concentrations progressively decreased with increasing CO2 concentrations between 400 and 800 ppm CO2 as the stomata closed (Qi et al., 2021). Elevated CO2-induced stomatal closure is often associated with increased leaf water potential, which might explain instances where leaf ABA concentrations decline with elevated CO2. Such changes in ABA status may be physiologically significant when plants are concurrently exposed to drying soil. A series of papers evaluated tomato water relations and ABA status in response to factorial experiments that varied atmospheric CO2 concentration and soil moisture (Li et al., 2021; Liu et al., 2019; Wei et al., 2020). In well-watered soil, typically there were no differences in leaf ABA concentrations or root xylem sap ABA concentrations, but with progressive soil drying, elevated CO2 consistently enhanced root ABA export (Li et al., 2021; Liu et al., 2019) but either stimulated (Wei et al., 2020) or attenuated (Liu et al., 2019) foliar ABA accumulation (Fig. 3.2). Enhanced ABA signalling is somewhat surprising since elevated CO2 had no effect on root water potential, Ψroot (Li et al., 2021), when root ABA concentration typically increases as Ψroot declines (Puértolas et al., 2013). Furthermore, tomato leaves are expected to have higher turgor when grown with elevated CO2 (since leaf water potential did not change but greater osmotic adjustment occurred—Li et al., 2021), yet turgor loss is regarded as a trigger for ABA synthesis (Pierce & Raschke, 1981). Possibly the impact of enhanced root-toshoot ABA signalling on leaf ABA accumulation is modulated by changes in foliar ABA metabolism. Irrespective of changes in endogenous ABA concentrations, elevated CO2 may alter stomatal sensitivity to ABA. In elevated CO2, stomatal conductance (gs) was lower at a given leaf ABA concentration, with lower stomatal sensitivity (less relative change in gs per unit change of ABA) to ABA (Liu et al., 2019). Stomatal sensitivity to xylem ABA did not change, despite lower gs in plants exposed to elevated CO2. Possible variation in stomatal sensitivity to ABA seems important in regulating responses to drying soil, as plants exposed to elevated CO2 continue to transpire normally (albeit at lower rates) until the soil is much drier (Li et al., 2021; Liu et al., 2019). Such a response to soil moisture depletion was conserved in both wild-type and ABA-deficient mutants and thus independent of foliar ABA status (Li et al., 2021). While this might suggest hydraulic regulation of stomatal response, declining leaf and root hydraulic conductance in response to drying soil also occurred at similar soil moisture values independent of genotype (ABA status) and eCO2 (Li et al., 2021). Thus, variations in stomatal sensitivity to ABA may be involved in modulating plant responses to drying soil. Elevated CO2 has well-documented effects on stomatal morphology, with stomatal development regulated by both ABA and CO2. Plants grown at eCO2, or with exogenous ABA treatment, usually have lower stomatal density. eCO2-induced regulation of stomatal density (and aperture) requires increased reactive oxygen species (ROS) levels and the involvement of ABA receptors and ABA itself (Chater et al., 2015). However, shoot ABA levels did not differ between wild-type Arabidopsis plants when grown at ambient CO2 and eCO2, suggesting that stomatal sensitivity to ABA, rather than the bulk foliar ABA levels, modulates stomatal density under eCO2.

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Fig. 3.2 Changes in xylem ABA concentration (top panel) and leaf ABA concentration (bottom panel) as a function of soil drying (expressed as fraction of transpirable soil water) in different studies of tomato plants grown under elevated CO2 (eCO2). ABA concentrations of plants grown with ambient CO2 are subtracted from ABA concentrations of plants grown with elevated CO2, so values of 0 mean no effect of atmospheric CO2 concentration on ABA concentration, positive values mean higher ABA concentrations in eCO2-exposed plants, and negative values mean lower ABA concentrations in e-CO2-exposed plants

Moreover, expression of ABA-responsive genes increased when Arabidopsis was grown at high (550 ppm) CO2 (Li et al., 2006). In addition, eCO2-mediated stomatal closure was ABA-independent, by modulating OST1/OST2 kinases (Hsu et al., 2018).

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Therefore, the convergence point between ABA and CO2 signalling is contentious, and there is a continued need to explore how eCO2 modulates stomatal responses.

2.7

Ethylene and CO2

When oxygen is present, almost all plant tissues synthesise the gaseous phytohormone ethylene (ET) (Lin et al., 2010). High CO2 concentrations can antagonise ethylene-induced fruit ripening (Ahammed & Li, 2022). Ethylene can promote or inhibit growth as well as senescence based on the dose, time of application and also the species of plant (Pierik et al., 2006; Reid, 1995). Chemical inhibitors of ethylene synthesis or action, and the phenotypes of mutants perturbed in ethylene biosynthesis or ethylene sensitivity, have confirmed ethylene’s role in restraining leaf growth and development (Bleecker et al., 1988; Oh et al., 1997). The enzymes 1-aminocyclopropane-1- carboxylic acid (ACC) synthase (ACS) and ACC oxidase (ACO) catalyse biosynthesis reactions from S-adenosylmethionine to the precursor ACC and from ACC to ethylene, respectively. High CO2 levels may inhibit the synthesis of ethylene from ACC in fruits (Rothan & Nicolas, 1994), as CO2 is a required cofactor for ACC oxidase (Dong et al., 1992). Decreased plant height, leaf epinasty, premature leaf senescence and sterility are all symptoms of elevated ET levels in closed environments (Abeles et al., 1992; Morison & Gifford, 1984). High leaf glucose concentrations occurring in rice growing under eCO2 has been associated with ethylene-mediated growth promotion (Seneweera et al., 2003). However, soil ethylene accumulation inhibits root growth of many plants, but promotes root hair development (Pierik et al., 1999; Visser et al., 1997). In hydroponic tomato, eCO2 (800 ppm) increased leaf IAA concentration and ethylene evolution to a greater extent than qualitatively similar changes in the roots (Wang et al., 2009). These hormonal changes were associated with root growth promotion and altered root architecture, with increased root length and diameter (20%), surface area (45%) and more than double the number of root tips (Wang et al., 2009). In contrast, eCO2 (750 ppm) did not affect root ACC concentrations of substrate-grown tomato in spite of similar root growth promotion, as expected from observations of limited alterations in the expression of ET biosynthesis genes ACS and ACO (Brito et al., 2019). Thus root ethylene responses to eCO2 may be highly dependent on growing substrate.

3 CO2 Movement in Plant Roots and Rhizosphere Typical soil CO2 levels are higher than atmospheric levels (Van Veen et al., 1991), which at the time of writing is 419 ppm (NASA, 2022). The “rhizosphere” represents the soil volume influenced by plant roots, a highly dynamic region that supports a diverse and dense microorganism population which are affected by the root released

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chemicals (Hartmann et al., 2008). The bulk soil and the rhizosphere can be readily distinguished by their contrasting physical, chemical and biological properties (Hinsinger et al., 2009). During the early growth of plant roots, the rhizosphere develops its own pore structure which influences the dynamics of water uptake, nutrient acquisition and gas flows surrounding the roots (Helliwell et al., 2017). Rhizosphere processes play a critical role in the carbon and nutrient cycles of soil (Coleman et al., 1992; Van Veen et al., 1991). Soil CO2 efflux is driven by variations of root respiration and microbial respiration, along with the soil organic material decomposition (Kuzyakov, 2006). Soil depth, soil water content, soil type and time of the year all alter soil CO2 concentrations (Bouma et al., 1997; Duenas et al., 1995; Johnson et al., 1994), which typically range from 2000 to 5000 ppm, but with poor aeration may reach 20% (De Jong & Schappert, 1972; Norstadt & Porter, 1984). Stomata in leaves are the primary route of gas exchange including CO2 intake in higher plants. The CO2 that is not fixed in the shoot and is translocated to the roots can be respired, assimilated or exuded and used by microorganisms (Warembourg & Paul, 1973). Unlike aquatic plants that can absorb and translocate CO2 captured from sediments and respiration from the roots to the shoots, terrestrial plants absorb minimal CO2 amounts through their roots (Brix, 1990; Colmer, 2003). Nonetheless, the land plant Stylites andicola is an exception because most of its CO2 fixation occurs via its roots, since it lacks stomata (Keeley et al., 1984). Old experiments indicate that roots are able to capture CO2 and translocate it to the shoot (Ruben & Kamen, 1940; Stolwijk & Thimann, 1957), with numerous subsequent studies confirming this hypothesis. Although grasslands represent about 40% of land surface (Adams et al., 1990; White et al., 2000), most knowledge of carbon fluxes at the root-soil interface comes from research of forest ecosystems, with ecosystem photosynthesis and respiration dominating carbon balances. Ecosystem respiration is the sum of autotrophic (root, leaves and stems) and heterotrophic (bacteria, fungi and animals) respiration (Hanson et al., 2000). When plant respiration occurs, the CO2 produced moves from inside the roots into the pore space of the soil. Thus plants can be major contributors to the CO2 flux. When the CO2 dissolves in the soil, it generates dissolved inorganic carbon (DIC), according to the partial pressure of CO2, temperature and pH (Clark & Fritz, 1997). CO2 dissolves in water to form DIC according to the following reaction: Soil CO2 ðgÞ = CO2 ðaqÞ þ H2 O = H2 CO3 $ Hþ þ HCO3 $ 2Hþ þ CO3 2 -

ð3:1Þ

Total system DIC sums dissolved CO2 gas (CO2), carbonic acid (H2CO3), bicarbonate (HCO3-) and carbonate (CO32-) (Karberg et al., 2005).   ½DIC = ½CO2 ðaqÞ þ ½H2 CO3  þ ½HCO3 -  þ CO3 2 thus:

ð3:2Þ

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Role of Plant Hormones in Plant Response to Elevated CO2 Concentrations:. . .

½H2 CO3  = ½H2 CO3  þ ½CO2 ðaqÞ

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ð3:3Þ

Gas (CO2), liquid (HCO3- and CO3- in solution) and solid (carbonate) phases comprise the soil inorganic carbon. As a weak acid, CO2 is capable of dissolving basic minerals including CaCO3. Simultaneously with CO2 dissolving in water, hydrolysis of HCO3- results in the formation of carbonates of other salts, typically with Mg2+ and Ca2+ (Bai et al., 2017). The pathway of the reaction is driven by the pH of the solution which determines the fraction of the carbonate species existing in the solution. At pH 5, a proportion of DIC occurs as HCO3- and CO32-, and CO2 solubility increases thereafter (Golterman & Clymo, 1969). At pH ≤6.36, H2CO3 prevails. At pHs between 6.36 and 10.33, HCO3- prevails, while at higher pHs, CO32- predominates (Lindsay, 1979). Interestingly, part of the CO2 respired by cottonwood tree roots was dissolved in the xylem sap and internally transported throughout the tree (Bloemen et al., 2013). Whether this significantly contributes to shoot carbon gain is not known. With this context, it is perhaps not surprising that many investigators have sought to establish the impact of rootzone CO2 enrichment or dissolved inorganic carbon on shoot growth. Elevated RZ CO2 markedly augmented mean biomass by 2.9% in a review of 358 experiments (Enoch & Olesen, 1993). Nevertheless, some studies demonstrate more substantial effects, with RZ CO2 enrichment possibly a more sustainable and economic alternative to atmospheric CO2 enrichment. Supply of 5000 ppm CO2 to a hydroponic solution enhanced tomato (S. lycopersicum) biomass in both control and salt stress (100 mM NaCl) compared to the plants not supplemented with RZ CO2 (0 ppm). This only happened when plants were grown at high light irradiance (1500 μmol m-2 s-1) and high aerial temperatures (37/19 °C (day/night)) at pH 5.8 of hydroponic nutrient solution, resulting in a 40% higher effect than on control plants (Cramer & Richards, 1999). When irradiances are lower (45  C in fruit skin), defense mechanisms involving antioxidant metabolites and enzymes are triggered during tissue acclimation to these conditions throughout the growing season. Antioxidant molecules, such as ASC and GSH, decrease initially, but antioxidant-related enzymatic activities and transcripts increase (Ma & Cheng, 2003; Torres et al., 2006). Carotenoids and phenylpropanoids, such flavonol glycosides (Racsko & Schrader, 2012), lignin/ monolignols, hydroxycinnamoyl esters, and biosynthetic enzymes and their transcripts increase as photoprotective mechanisms in apple (Torres et al., 2020). If fruit tissues are unable to acclimate to these environmental stress, they ultimately suffer oxidation of macromolecules leading to invisible and visible sunburn symptoms. Some of these are as follows: peel discoloration, increase in soluble solids, increase in flesh firmness, increase in soluble pectin, reduction in titratable acidity, and

 ⁄ Fig. 6.2 (continued) photoprotective, characterized by an increase of phenylpropanoids, specifically flavonol glycosides, lignin and monolignols, hydroxycinnamoyl esters, and their biosynthetic pathway’s enzymes such as phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), flavanone-3-hydroxylase (F3H), O-methyltransferase 1 (COMT1), and cinnamyl alcohol dehydrogenase (CAD), and an increase in carotenoids, particularly β-carotene, xanthophylls, and lutein, as well as increase in antioxidant system components such as ascorbate (ASC), glutathione (GSH), antioxidant enzymes (ascorbate peroxidase, APX; monodehydroascorbate reductase, MDHR; dehydroascorbate reductase, DHAR). Symptoms on the sun-exposed side of the fruit (peel and flesh) include the following: peel discoloration, increase in soluble solids and flesh firmness, increase in soluble pectin, decrease in titratable acidity, and changes in tissue morphology

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changes in tissue morphology (Racsko & Schrader, 2012; Torres et al., 2013) (Fig. 6.2).

5 Conclusions The combined effect of HL and high temperature causing POS and HS on fruit will be an increasing problem in several agricultural areas worldwide with climate change. ABA and JAs arise as the main phytohormones controlling the antioxidant response against POS in plants, and ethylene and salicylates may perhaps play important roles in fruit too. Biotechnological approaches have been used to decrease deleterious effects from oxidative stress in fruit, frequently by overexpressing ROS-scavenging enzymes but also by increasing total antioxidants through applications of plant regulator applications. Potential breeding targets to improve plant/fruit antioxidant status include key transcriptional regulators, as those related with JA signaling. Also, engineered fruit crops with high levels of antioxidants could provide advantages in other quality traits including appearance (color) and nutritional value. Future applications to face HL and HS associated to climate change will demand the regulation of hormonal balance focusing on redox homeostasis during fruit development and ripening. Acknowledgements We would like to acknowledge the support of the USDA National Institute of Food and Agriculture Hatch project 1014919, titled “Crop Improvement and Sustainable Production Systems” (WSU reference 00011), and the Hatch Multistate funding, Project NE-1836, from the USDA National Institute of Food and Agriculture to C.A Torres, and ANID—Millennium Science Initiative Program—NCN2021_010 and FONDECYT/Regular 1210941 to C. R. Figueroa.

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Chapter 7

Phytochrome and Hormone Signaling Crosstalk in Response to Abiotic Stresses in Plants Marina Alves Gavassi, Frederico Rocha Rodrigues Alves, and Rogério Falleiros Carvalho

1 Introduction Plants live in dynamic and ever-changing environments, constantly challenging them to cope with stressful conditions in order to survive. External signals, such as light, temperature, and water availability, are perceived by specialized plant receptors and converted to internal biological signals, triggering growth, and developmental differential responses to adapt accordingly to the surrounding environment (Anwar et al., 2021; Lamers et al., 2020). Phytochromes (PHYs) are red/far-red light receptors characterized as photoreversible chromoproteins. The biologically inactive PHYr form absorbs red light (wavelengths around 660 nm) and converts itself in the active PHYfr form. PHYfr inactivation occurs upon far-red light absorption (wavelengths around 730 nm) or through thermal reversion, a temperature-dependent process (Legris et al., 2016; Rockwell et al., 2006). PHYs are coded by a small multigenic family in plants, being functionally diverse due to differences concerning protein structure and corresponding photochemical properties (Li et al., 2011). PHYs are classified as light-labile, usually associated with very low fluence responses, represented in Arabidopsis by PHYA, and light-stable, related to red high irradiance responses,

M. A. Gavassi (*) Department of Biodiversity, Biosciences Institute, São Paulo State University (IB/UNESP), Rio Claro, SP, Brazil e-mail: [email protected] F. R. R. Alves Department of Botany, Federal University of Goiás (UFG), Campus Goiânia, Goiânia, GO, Brazil R. F. Carvalho Department of Biology, São Paulo State University (FCAV/UNESP), Jaboticabal, SP, Brazil © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_7

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represented by PHYB, PHYC, PHYD, and PHYE (Legris et al., 2019). Therefore, PHY-dependent responses are determined by the balance between PHYr and PHYfr forms according to environmental light quality, quantity, and temperature. In summary, PHY-dependent light signaling initiates with PHY photoactivation, followed by translocation into the nucleus, interaction with other proteins, and consequent transcriptional control of photoresponsive genes (Xu et al., 2015). In the nucleus, PHYfr inhibits the action of ubiquitin E3 ligases, such as the CONSTITUTIVE PHOTOMORPHOGENESIS (COP) and SUPPRESSOR OF PHYA (SPA) complex that mediates ubiquitin-dependent degradation of light signalingrelated factors, such as ELONGATED HYPOCOTYL 5(HY5) (Podolec & Ulm, 2018). Active PHYs also repress PHYTOCHROME INTERACTING FACTORS (PIFs), important transcription factors that promote expression of numerous development-related genes (Leivar & Quail, 2011). As transductors of environmental stimuli into differential gene expression modulation, PHYs are directly related to important morphophysiological responses to abiotic stresses, crosstalking with hormone signaling pathways to cope and survive through challenging situations (Carvalho et al., 2011; Li, Euring, et al., 2021; Lymperopoulos et al., 2018; Silva Junior et al., 2021). A detailed introduction to the regulation of plant hormone metabolism by light has been reviewed by Alves et al. (2021). In this chapter, some of the most significant links between PHY- and hormone signaling crosstalk in response to common abiotic stresses will be presented and discussed.

2 Heat Stress Climate change is among the main challenges for plant productivity of recent times, so that temperature extremes have been registered in agricultural regions worldwide with varying frequency, intensity, and duration (Augspurger, 2013; Sinha et al., 2021). Plants usually live in thermodynamic environments and their tissue temperature depends on solar radiation, temperature of surrounding air and soil, fluorescence emission capacity, and evapotranspiration (Casal & Balasubramanian, 2019). Prolonged exposure to high temperatures may cause impairments to plant growth, development, and productivity, characterizing heat stress (Lippmann et al., 2019; Mishra et al., 2021). Inside plant cells, temperature is a main factor driving homeostasis, directly affecting the rate of enzymatic reactions and viscosity of cytoplasm and within organelles. Temperatures above an optimal level destabilize protein structures (leading to denaturation) and membrane properties. The heat-caused disturbance on membrane fluidity, for instance, dismantles thylakoid structure and grana stacking within chloroplasts, disrupting the photosynthetic machinery. Key photosynthetic enzymatic steps are also temperature-dependent, such as the activation of RuBisCO, which is impaired as temperature increases. The loss of photosynthetic efficiency

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also leads to accumulation of ROS and other toxic compounds, driving to oxidative stress (Surabhi & Seth, 2020; Zhao et al., 2021). The deleterious effects of heat on photosynthesis, coupled with scorching and sunburn of plant tissues, ultimately lead to leaf senescence, alterations in organ size and weight, and severe reductions in plant yield (Hemmati et al., 2015). Indeed, climate change models indicate global average yield losses of 6.0% for wheat, 3.2% for rice, 7.4% for maize, and 3.1% for soybean per each degree-Celsius increase in global mean temperature (Zhao et al., 2017). Plants can cope with heat stress by temperature-dependent modulation of plant morphology (thermomorphogenesis), synthesis of heat-shock proteins (HSPs), and antioxidants. Warm temperature morphoresponses include greater hypocotyl and petiole length, moving the sensitive apical meristems away from soil hot surface; hyponasty, reducing the direct incidence of solar radiation especially at midday to avoid overheating and enhancing ventilation; elongated leaf shape and lower stomatal index, preventing excessive loss of water by transpiration; and early flowering (Casal & Balasubramanian, 2019; Park et al., 2021). HSPs are essential to maintain cell homeostasis during high temperature stress by binding to structurally unstable proteins, preventing protein denaturation and protecting synthesis machineries, in a chaperon-like function (Haq et al., 2019; Hemmati et al., 2015). The heat stressdriven oxidative stress and accumulation of ROS are also signals for the synthesis of HSPs and antioxidant enzymes (Hemmati et al., 2015; Volkov et al., 2006). High temperature modulates the plant phytohormone levels, which, in turn, mediates very complex stress-adaptive crosstalk and signaling cascades across plant organs (Devireddy et al., 2021). However, phytochromes are also plant thermal sensors; thus, many light-dependent signaling factors also interact with phytohormone signaling pathways to convey primary responses to achieve tolerance to detrimental effects of high temperatures (Li, Euring, et al., 2021; Song et al., 2017). Thermomorphogenic responses are controlled by PIF levels, acting as central signaling hubs integrating environmental signals, such as light and temperature, and hormonal responses (Fig. 7.1) (Balcerowicz, 2020). Under warmer temperatures, transcription of PIFs is increased as well as their protein levels, due to lower rates of PHY-dependent PIF degradation, once PHYB deactivation rate via thermal reversion is increased, and PIF stabilization by other transcriptional activators such as HEMERA (HMR) and SPA1 (Hahm et al., 2020; Lee et al., 2021; Qiu et al., 2019). PIF expression and stability are also regulated by hormonal signaling to coordinate thermomorphogenic responses. Gibberellin (GA) biosynthetic genes are upregulated under elevated temperature, while catabolic genes are down-regulated (Stavang et al., 2009). GA prevents repressive DELLA proteins to inhibit PIF action (De Lucas & Prat, 2014); therefore, increased GA levels may contribute to heatdependent higher PIF activity in plant tissues. Brassinosteroid (BR), that also plays critical roles in the control of cell division and elongation, has biosynthetic genes positively regulated by PIF4 and they are also upregulated under high temperatures (Martínez et al., 2018). In a feed-forward positive loop, BRASSINAZOLERESISTANT 1 (BZR1), a downstream BR signaling factor, accumulates in the

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Fig. 7.1 Phytochrome (PHY) and Hormone Signaling Crosstalk in Response to Heat Stress. Upon red light absorption, inactive PHYr converts into active PHYfr form, eventually photoreverted to inactive form by far-red light absorption or under warm temperatures. PHYfr suppresses the action of phytochrome interacting factors (PIFs), central signaling hubs that induce the accumulation of many hormones related to heat tolerance responses. PIFs are positively related to accumulation of ABA and cytokinins (CKs), which induce the synthesis of antioxidants and heat-shock proteins (HSPs) to cope with heat stress. PIFs also induce the synthesis of auxins, which are related to thermomorphogenic responses, such as elongation of stems and petioles under heat stress. Other transcription factors, such as LONGIFOLIA (LNG), senescence-related genes, and SPEECHLESS (SPCH), are also related to thermomorphogenic responses. Under warm temperatures, gibberellin (GA) levels increase, inhibiting the repression of della proteins over PIFs, resulting in heatdependent early flowering due to promotion of FLOWERING LOCUS T (FT) expression by PIFs. Brassinosteroid (BRs) synthesis is also induced by PIFs and, in a positive feedback loop, BRASSINAZOLE-RESISTANT 1 (BZR1), a downstream BR signaling factor, promotes PIF expression

nucleus in a warmth-dependent manner and induces PIF4 expression, amplifying the activation of growth-responsive genes (Ibañez et al., 2018). When it comes to shoot growth, temperature-dependent growth of stems and petioles is caused by increased levels of auxin in aerial organs, due to enhanced binding of PIFs to the promoters of auxin-biosynthetic genes YUCCA8 (YUC8) and TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) (Franklin et al., 2011; Sun et al., 2012), and other auxin-responsive genes such as AUXIN/ INDOLE-3-ACETIC ACID 19 (IAA19) and IAA29 (Sun et al., 2013). PIF4 also increases LONGIFOLIA (LNG) protein levels, related to elongation of leaf blade, petiole, and hypocotyl (Hwang et al., 2017). The lower stomata index registered in plants grown under warmer temperatures occurs due to an accumulation of PIFs in stomata precursors, suppressing the expression of SPEECHLESS (SPCH), a master transcription factor driving stomata initiation and development (Lau et al., 2018). Heat stress-induced leaf senescence is also under transcriptional control of both PIF4 and PIF5, enhancing the levels of senescence-related genes (Li, Bo, et al., 2021).

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Such refined response could prevent excessive water loss through transpiration; however, further manners to dissipate excess energy should be adopted. Acceleration of floral transition is another developmental response to warmer temperatures. Flowering depends on the expression modulation of many floral pathway integrators (Bao et al., 2020). PIF4 binds to the promoter of FLOWERING LOCUS T (FT), inducing the expression of this important floral transition trigger (Kumar et al., 2012). Once lower levels of GA delay flowering under warm temperatures (Balasubramanian et al., 2006), it has been proposed that increased biosynthesis of GA due to higher temperatures would elicit flowering by inhibiting DELLA-mediated repression over PIFs, allowing FT transcription (Kumar et al., 2012). However, elucidating the crosstalk between GA and PIFs in mediating temperature-dependent flower initiation has been proven to be complex, depending on photoperiod, cell specificity, epigenetic modulation, and recruitment of other flowering factors (Bao et al., 2020; Fernández et al., 2016; Galvão et al., 2015; Jin & Ahn, 2021). To cope with heat stress-driven increasing levels of ROS and oxidative consequences, plants coordinate the synthesis of antioxidants via light- and hormonalsignaling crosstalk. Heat-induced synthesis of HSPs and antioxidant enzymes is associated with increased levels of ABA and CK in plant tissues or exogenous application of these hormones (Cortleven et al., 2019; Ding et al., 2010; Hönig et al., 2018; Larkindale & Knight, 2002; Zandalinas et al., 2016). ABA concentration and signaling are also under phytochrome control in many species (Boggs et al., 2010; Gil et al., 2018; Kraepiel et al., 1994; Sawada et al., 2008). PIFs promote ABA accumulation in plant tissues via upregulation of ABA-biosynthetic genes and repression of ABA-catabolic genes (Kim et al., 2008; Oh et al., 2007, 2009). As for the PHY-dependent modulation of CK levels and signaling, evidences point out that CK induces the accumulation of HY5 proteins (Vandenbussche et al., 2007), and the promoters of CYTOKININ OXIDASE (CKX) catabolic genes possess PIF-binding motifs (Hornitschek et al., 2012), although experimental links of PHY- and CK-signaling crosstalk remain elusive. Nevertheless, it is inevitable to relate PIF regulation and hormonal signaling as one of the main features guaranteeing plant survival to heat.

3 Low-Temperature Stress Low-temperature (LT) stress causes detrimental effects on plant growth and development, being an important environmental impact factor over productivity and yield, leading to huge economic losses and threatening global food security (FAO, 2020; Mehrotra et al., 2020). LT stress is categorized as chilling stress (environmental temperature below 20 °C) and freezing stress (temperature below 0 °C) (Ritonga & Chen, 2020). Chilling stress notably inhibits water uptake, initiates cellular dehydration, which lowers membrane fluidity, and directly affects conformation of nucleic acids and specific proteins (Jouyban et al., 2013; Nievola et al., 2017).

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Thus, when a plant undergoes this stress, several physiological alterations occur, impairing processes in the plant cell, including photosynthesis, respiration, water and mineral uptake, and other metabolic activities. The extent of damage caused to the plants is proportional to the intensity and duration of exposure to LT. The ability of plants to tolerate LT stress without damages is referred to as cold tolerance. Temperature sensibility is an important determining factor of the geographical distribution of plants (Liu & Zhou, 2018; Shi et al., 2018). Tropical and subtropical crops such as rice, corn, soybean, potato, cotton, and tomato are especially sensitive to chilling stress, lacking cold tolerance. On the other hand, plants from temperate environments can tolerate seasonal freezing temperatures (Chinnusamy et al., 2007), such as barley, wheat, and rye (Mehrotra et al., 2020; Zhang et al., 2011). These temperate plants acquire freezing tolerance upon previous and seasonal exposure to low temperatures (but nonlethal), a process called cold acclimation that is achieved by activation of a set of COLD-REGULATED (COR) genes, related to the synthesis of cryoprotective proteins and important freezing-related osmolytes (Ding et al., 2019; Shi et al., 2018). Other LT-related responses include the release of Ca2+, reduced water content (Thakur & Nayyar, 2013), ROS scavenging (Gurunani et al., 2015), and carbon metabolic adjustments (Ruelland & Zachowski, 2010). Light and temperature signaling pathways are reported to be tightly connected, because in natural conditions, dark periods are accompanied by cooler temperatures. During winter and fall seasons, plants experience lower temperatures, shorter days, decreased red to far-red ratios (R/FR) of light, and longer twilight durations (Franklin & Whitelam, 2007). These environmental changes are usually associated with decreased plant growth rates and improved cold tolerance as temperatures decrease along the start of the fall season. Biochemically, the cold acclimation process occurs due to transcript reprogramming and regulation of plant hormone levels such as ABA and GA, leading to growth impairment or dormancy, subsequently conferring freezing tolerance to plants (Wisniewski et al., 2011). As for the crosstalk between light and hormone signaling during cold stress, LT induces the transcription of PHYA and accumulation of HY5 in tomato plants. HY5 directly binds and induces the transcription of GIBBERELLIN 2-OXIDASE 4 (GAox4) and 9-CISEPOXYCAROTENOID DIOXYGENASE 6 (NCED6), encoding a GA-inactivation enzyme and an ABA-biosynthetic enzyme, respectively. Thus, PHYA-dependent HY5 accumulation leads to sensitive alterations in the plant hormone homeostasis, resulting in higher levels of ABA and lower levels of GA, restricting plant growth, and inducing cold-related morphophysiological responses (Wang et al., 2019). Furthermore, silencing of NCED6 compromises the light-dependent tomato resistance to cold stress. These results highlight the evidence that photoperiod and light quality regulate the acquisition of efficient cold hardiness tolerance through PHYs and hormonal balance (Fig. 7.2) (Eremina et al., 2016; Franklin & Whitelam, 2007; Lee & Thomashow, 2012). As previously pointed out, many regulatory genes, particularly transcription factors (TFs), work synergistically to improve cold tolerance, playing essential roles in plant stress response. These regulators include antifreeze proteins and osmoregulators, whereas indirect regulators as chaperones, functional proteins, and

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Fig. 7.2 Phytochrome (PHY) and Hormone Signaling Crosstalk in Response to Low-Temperature Stress. Evidences point out that low temperatures stabilize PHYs. PHYA induces the expression of ELONGATED HYPOCOTYL 5 (HY5), which, in turn, controls the balance between gibberellin (GA) and abscisic acid (ABA) levels inside plant cells. A high ABA:GA ratio confers cold hardiness to plants. PHYB-mediated inhibition of PIFs and subsequent impact over cold tolerance via expression of C-REPEAT-BINDING FACTOR (CBFs) seems to be regulated differentially according to the species

kinases (Mehrotra et al., 2020; Thomashow, 1999). In plants, the identification of the C-REPEAT BINDING FACTOR/DEHYDRATION-RESPONSIVE ELEMENT BINDING FACTOR (CBF/DREB) transcription factors associated with COR signaling pathway led to significant progress in unraveling the molecular mechanisms behind LT-dependent responses (Liu, Dang, et al., 2019; Liu, Schlappi, et al., 2019). The CBF/DREB-related transcriptional cascade has been extensively characterized in several plant species and it is considered a major pathway controlling cold signaling and acclimation. The transcription of many cold-responsive genes is tightly regulated by interaction between PHY-signaling elements, especially PIFs, and hormone signaling pathway elements (Fig. 7.2); however, the mechanisms of control and crosstalk between the pathways seem to occur differently in a species-specific manner. In Arabidopsis, cold causes rapid transcription of CBF genes and subsequential promotion of CBF-targeted genes related to freezing tolerance (Lee & Thomashow, 2012). PIFs, namely PIF3, PIF4, and PIF7, act as repressors of the CBF genes under low temperatures by directly binding to their promoters (Jiang et al., 2017; Kidokoro et al., 2009; Lee & Thomashow, 2012; Lin et al., 2018). In the other hand, cold stabilizes PHYB, promoting the degradation of PIFs and consequently mediating the expression of CBFs and freezing tolerance in Arabidopsis (Jiang et al., 2020). Divergently, in tomato, knocking out PIF4 increases cold susceptibility, and the overexpression of PIF4 improves cold tolerance responses in tomato plants (Wang

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et al., 2020). Under LT stressful conditions, tomato PIF4 activates the expression of CBFs via binding to their promoters, regulates plant hormone biosynthesis and signaling, including ABA and GA, and directly induces GA-INSENSITIVE 4 (GAI4) expression, a plethora of biochemical and molecular alterations which enhances cold tolerance. Distinct PIFs also respond differentially to ABA levels and cold stress according to the species. For instance, Arabidopsis PIF1 and Brassica napus PIF7 expression is upregulated by cold and repressed by ABA, while Arabidopsis PIF6 is upregulated by ABA (Li, Liu, et al., 2021). ABA-responsive genes are potential targets of PIFs, including stress-induced protein kin1, which functions as an antifreeze protein (Liang et al., 2020; Soitamo et al., 2008). These results reveal that light and temperature signals are integrated by plants through entangled hormone signaling pathways to better cope with cold stress; however, there seems to be a complex species-specific crosstalk between the elements, which requires detailed experimentations toward a comprehensive understanding of plant growth and development in environments facing low temperatures.

4 Drought Stress Water is an essential resource for plant survival and limitations in water availability heavily restrains plant growth and productivity worldwide, causing more annual loss in crop yield than all pathogens combined (Gupta et al., 2020). When exposed to drought conditions, plants strive to keep water balance mainly by stomata closure, preventing water loss via transpiration at the expense of CO2 uptake, and osmotic adjustments (Kapoor et al., 2020; Rodrigues et al., 2019). Drought stress also leads to accumulation of ROS and consequent oxidative stress, requiring synthesis of enzymatic antioxidants and other stress-protectant metabolites (Ahmad et al., 2014; Laxa et al., 2019). LATE EMBRYOGENESIS ABUNDANT (LEA) proteins are hydrophilic metabolites that also accumulate in plant tissues in response to drought and other associated stresses, performing osmotic adjustments, ROS scavenging and membrane stabilization, acting as chaperones (Riyazuddin et al., 2021). ABA is the main drought stress-responsive phytohormone in plants. Under water shortage in the soil, ABA biosynthesis is induced in the roots and then transported through the vascular systems to the leaves, ultimately leading to the drought tolerance responses (Shinozaki & Yamaguchi-Shinozaki, 2007; Takahashi et al., 2020; Ullah et al., 2018). Briefly, under low ABA levels, TYPE 2C PROTEIN PHOSPHATASES (PP2Cs) prevent activation of SNF1-RELATED PROTEIN KINASES (SnRK2s). SnRK2s are responsible for the phosphorylation of target proteins such as transcription factors and ion channels directly involved in ABA responses. In the presence of ABA, PYRABACTIN RESISTANCE 1/PYRABACTIN RESISTANCE 1-LIKE/ REGULATORY COMPONENT OF ABA RECEPTOR (PYR/PYL/RCAR) receptors bind to the hormone and to PP2Cs proteins, inhibiting its functions and allowing

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the accumulation of phosphorylated SnRK2s, leading to ABA-dependent stress responses (Cutler et al., 2010; Ng et al., 2014; Soma et al., 2021). There is a correlation between high light irradiance, heat, and drought stress in nature. Strong solar irradiance accelerates water evaporation from both soil and plant body, promoting water deficit stress (Farooq et al., 2012). Excessive light exposure also induces ABA and ROS accumulation in leaves and consequent stomata closure (Devireddy et al., 2018). Therefore, it is not surprising that plant responses to drought would be also associated with light signaling (Kim et al., 2021). PHYs are related to many morphological and physiological responses that impact water uptake, transport, and loss, reflecting upon carbon gain, especially concerning stomata opening and development. PHYs diminish the repression of PIFs and COP/SPA complex over the transcription of stomata development-related genes (Wei et al., 2020). Manipulation of PHY and consequent impact over stomata density and index can, therefore, affect crop performance accordingly. Heterologous Arabidopsis PHYB overexpression increased stomatal conductance, transpiration, and photosynthetic rates in potato plants in field conditions (Boccalandro et al., 2003). In rice, loss-of-function phyB mutants presented reduced stomatal density and size, conferring drought tolerance attributed to decreased transpiration rates (Liu et al., 2012). Many PHY-dependent signaling elements can regulate endogenous ABA levels and ABA signaling, which, in turn, can influence plant adaptation to drought stress (Fig. 7.3). PIFs can also interact physically with ABA receptors to control the expression of ABA-INSENSITIVE 5 (ABI5) transcription factor (Kim et al., 2016; Qi et al., 2020), considered a convergence hub between light and ABA signaling (Xu et al., 2014). The positive regulators of the PHYA signaling pathway FAR-RED ELONGATED HYPOCOTYL 3 (FHY3) and FAR-RED IMPAIRED RESPONSE 1 (FAR1) as well as the central light-responsive transcription factor HY5 are also promoters of ABI5 expression (Chen et al., 2008; Tang et al., 2013). ABI5 is directly related to abiotic stress adaptations such as the promotion of synthesis of LEA proteins (Skubacz et al., 2016) and stomata aperture control (Kang et al., 2018). The characterization and knowledge of the complex light-ABA signaling pathway can indicate promising strategies for crop improvement. Heterologous overexpression of maize PIF1 and PIF3 enhances tolerance to drought stress in rice. Transgenic rice presented water saving by decreasing stomatal aperture and transpiration rate due to increased sensitivity to ABA and also presented increased grain yield (Gao et al., 2015; Gao, Wu, Zhang, Jiang, Liang, et al., 2018; Gao, Wu, Zhang, Jiang, Ren, et al., 2018). Overexpression of apple PIF3 also improved drought tolerance in apple callus and transgenic Arabidopsis lines (Zheng et al., 2021), indicating that PIFs are interesting candidates for biotechnological manipulation aiming to develop drought-resistant plants. Auxin signaling elements also induce drought tolerance in tight control by PIFs (Fig. 7.3). AUXIN/INDOLE-3-ACETIC ACID (IAA) proteins, downstream transcriptional repressors of the auxin signaling pathway, are required in stress tolerance response in plants (Shani et al., 2016). In Arabidopsis, IAA19 is positively associated with the synthesis of glucosinolates, aliphatic compounds that confer drought

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Fig. 7.3 Phytochrome (PHY) and hormone signaling crosstalk in response to drought and salinity stresses. Abscisic acid (ABA) levels are induced by phytochrome-interacting factor (PIF) activity, increasing the synthesis of osmoprotectants and antioxidants in response to drought and salinity stresses. ABA-INSENSITIVE 5 (ABI5), an important ABA signaling element, is induced by ELONGATED HYPOCOTYL 5 (HY5), leading to accumulation of LATE EMBRYOGENESIS ABUNDANT (LEA) proteins and stomata control to cope drought stress. PIFs are also related to the induction of AUXIN/INDOLE-3-ACETIC ACID 19 (IAA19) transcription, which promotes the synthesis of glucosinolate osmoregulators. High salinity impairs PIF-mediated repression over gibberellin (GA) accumulation, allowing DELLA proteins to inhibit seedling elongation

tolerance and are also important in stomata aperture control (Salehin et al., 2019). PIFs bind to IAA19 promoters, activating its expression (Sun et al., 2013), providing an interesting link to be explored concerning a crosstalk between PHY and auxin signaling pathways to mediate drought tolerance besides the classic association in photomorphogenic responses.

5 Salt Stress Conditions of high salinity in the soil are characterized by an estimated soluble salt concentration of 4 dS/m or more, approximately equivalent to 40mM NaCl, corresponding to an osmotic pressure around 0.2 MPa (Munns & Tester, 2008). Normally, the osmotic pressure in plant cells is found to be greater than that in soil solution, creating a differential water potential driving water and essential mineral nutrients uptake from the soil solution to the root cells. On the other hand, salinity increases the osmotic pressure in the soil solution, diminishing the ability of a plant

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to absorb water and nutrients. Once cations such as Na+ and Cl- are largely taken up by roots, both cations can impair metabolic processes and negatively affect photosynthetic efficiency (Kader & Lindberg, 2010; Kumari et al., 2019). Salt stress is considered a major abiotic stress causing osmotic stress and ion poisoning, resulting in oxidative stress, cell membrane damage, inhibition of mitosis, loss of chloroplast activity and then decreasing efficiency of photosynthesis (Munns, 2002), limiting plant growth, and productivity around the world. Soil salinity levels also increase due to heavy irrigation with saline water, poor water management irrigation practices, regular use of chemical fertilizers, and climate change, being the later responsible for sea levels rising and increased evaporation during drought periods (Kumari et al., 2016; Van Zelm et al., 2020). Many physiological and biochemical mechanisms are employed by plants in order to thrive in soils presenting high salt concentration such as ion homeostasis and compartmentalization (Flowers et al., 2015), ion transport and uptake (Sun et al., 2009), biosynthesis of osmoprotectants and osmoregulators (Slama et al., 2015), synthesis of antioxidant compounds and activation of the corresponding antioxidant enzymatic defense system (Donaldson et al., 2004; Miller et al., 2010), synthesis of polyamines (Zepeda-Jazo et al., 2011), generation of nitric oxide (NO) (Liu et al., 2015), and hormone modulation (Barrero et al., 2006; Kim et al., 2012; Thalmann et al., 2016). A comprehensive understanding of physiological, biochemical, and molecular mechanisms on how plants respond to salt stress at different levels according to light quality and hormone modulation is imperative to enable plant breeders to produce tolerant plants suitable for salt-affected areas in the future. Salt stress negatively affects plant growth and development via hormonal balance, especially during germination and seedling establishment (Park et al., 2016). GA signaling controls plant growth by regulation of the growth-repressing DELLA proteins (Achard et al., 2006). High light intensity has been pointed out as an important interfering factor with the inhibitory effect of DELLA on seed germination under salt stress in Arabidopsis (Arain et al., 2021). Following germination, shoot elongation and penetration through the soil are decisive for successful plant establishment at early developmental stages, particularly in saline soils. During salt stress, energy partition aims to biosynthesize osmolytes and proteins involved in osmotic adjustment and metabolism homeostasis, so that hypocotyl elongation is not the seedling priority. Consistently, studies in rice revealed that overexpressing PIFLIKE14 or loss of function of the DELLA protein SLENDER RICE 1 (SLR1) induces elongation in the dark during seedling emergence from soil and decreased the sensitivity to NaCl-mediated seedling growth inhibition (Mo et al., 2020). In fact, salt stress promoted PIF-LIKE14 degradation but SLR1 accumulation. Rice PIF-LIKE14 directly regulates the expression of genes related to mesocotyl elongation and SLR1 negatively regulates this process by physically interacting with PIF-LIKE14, hindering its normal transcriptional activity. Thus, the PIF-LIKE14SLR1 interaction in rice integrates light and GA signals to adjust and determine seedling growth under salt stress (Fig. 7.3) (Mo et al., 2020). After reaching the soil surface, the ability to respond to shade is another factor determining plant growth. In this matter, soil salinity strongly seems to negatively

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affect the plant response to shade. In Arabidopsis, the transcripts of SAG29, an ABA-responsive gene (Song et al., 2016), accumulated in high levels in +NaCl/+FR conditions while this accumulation was not registered in plants lacking four ABA-responsive transcription factors (referred as arebQ) (Yoshida et al., 2015). Whereas plants lacking ABI5 still presented a significant NaCl-mediated repression over hypocotyl elongation under +FR light, arebQ plants grown in the presence and absence of NaCl displayed similar heights in both treatments. These evidences suggest that the effect of NaCl on +FR-induced elongation depends upon increased ABA synthesis or signaling (Hayes et al., 2019). Finally, important evidence of light-hormone modulation of salt stress tolerance was obtained in heterologous overexpression of resurrection plants PIFs on Arabidopsis. Resurrection plants can keep themselves alive without experiencing any permanent injuries, tolerating dissection, even under massive dehydration. Numerous diverse transcription factors were involved in desiccation tolerance in Myrothamnus flabellifolia, a distinctive wooden resurrection plant from southern Africa (Moore et al., 2007), and among them, PIF1 is upregulated immediately at the early stage of dehydration (Ma et al., 2015). Heterologous overexpression of M. flabellifolia PIF1 (MfPIF1) conferred enhanced drought and salinity tolerance to Arabidopsis transgenic lines, related to higher levels of chlorophyll, proline, antioxidant enzymes, and lower reactive oxygen species accumulation. Lower water loss rate was also associated with lesser stomatal aperture after drought and ABA treatment (Qiu et al., 2020). Thus, PIFs from halophyte plants should be considered as important tools for future studies for genetic improvement, especially if we consider their evident relationship with hormonal balance.

6 Concluding Remarks Abiotic stresses, represented in this chapter by heat, low temperature, drought, and salinity, cause a plethora of morphophysiological, biochemical and gene expression changes in plants, challenging them to cope with stressful conditions to survive. These adverse effects eventually impact plant growth and development, consequently diminishing productivity and yield. Therefore, the increasing number of climatological extremes and the predicted negative effect over crop production impose new challenges to mankind to grant future global food security. Elucidating the complex mechanistic links and crosstalks between light and hormone signaling pathways that allow plants to sustain its growth and development under abiotic stress can highlight possibilities of biotechnological manipulation aiming to develop stress-tolerant cultivars. Central signaling hubs capable of integrating environmental signals, such as light and temperature, and hormonal responses, such as PIFs, are interesting candidates toward this goal. Manipulation of PIFs has led to significant and improved tolerance to abiotic stresses associated with altered hormonal balance in different crops, such as maize, rice, and tomato, as pointed out throughout this chapter. However, as we move away from studies solely

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based upon plant models such as Arabidopsis, we begin to unravel different speciesspecific mechanisms, emphasizing the need for diversification of studies in distinct species, aiming to develop generalized models. Research efforts aiming to understand the molecular basis of abiotic stress tolerance are fundamental to design new plant biotechnological solutions to face challenging socioenvironmental scenarios.

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Chapter 8

Phytohormone-Mediated Regulation of Heat Stress Response in Plants Sylva Prerostova and Radomira Vankova

1 Introduction Environmental factors play essential role in regulation of plant growth and development. Temperature, light, water, nutrients, atmospheric carbon dioxide as well as the presence of toxic compounds create a range of signals that can individually or collectively positively affect plant growth, or contrarily cause plant damage as abiotic stress. Among those various environmental factors, temperature is of great significance in the regulation of plant development (Casal & Balasubramanian, 2019). Plants have the “physiological temperature optimum” which depends on the species but also on plant developmental stage (Niu & Xiang, 2018; Quint et al., 2016). Slightly higher temperatures, “warmth” (generally up to 30 °C), can even support plant growth (Romero-Montepaone et al., 2021). Exceeding this interval disturbs normal growth and development of a plant and is generally considered as “heat stress.” This stress is one of the most severe in nature because it can rapidly lead to subsequent lethal irreversible damages, like changes in stability of proteins, nucleic acids, membranes and cytoskeletal structures (Asthir, 2015). Climatic changes coming within last decades bring some serious problems associated with temperature. Firstly, fluctuation of temperature during a year has begun to increase, causing long periods of extremely high temperatures usually combined with drought, alternating with much lower temperatures or above-average rainy weather. Interestingly, plants are able to tolerate wider range of low temperatures than those of high temperatures (Lancaster & Humphreys, 2020). Secondly, the mean year temperature is increasing. Both factors dramatically affect plant

S. Prerostova (*) · R. Vankova Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany, Czech Academy of Sciences, Prague, Czech Republic e-mail: [email protected]; [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_8

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production, causing significant losses in yield of many important crops. The increase of seasonal temperature by about 1 °C can cause 9–10% reduction in cereal yields (Lesk et al., 2016). Thus, rising temperature represents severe risk of food insecurity. It is also anticipated that increasing heat stress will cause complete extinction of many species (Field et al., 2014; Lynas, 2020). It is obvious that stresses, with a few exceptions, do not act in nature alone but they affect the environment in combination. For example, heat stress is in nature mostly connected with drought, salinity and/or higher irradiance. It is very important to study these combinations, but firstly, we need to better understand plant responses to each stress alone. Responses to some stresses show overlap (e.g. Mizoi et al., 2019; Yao et al., 2018). It indicates that the combination of these specific stresses could not exhaust plants so much as a combination of stresses with different responses. Moreover, the exposure of a plant to one stress could be beneficial for defence to a potential subsequent stress, causing so-called cross-tolerance (Hossain et al., 2018). There are several studies on combined stresses, but this research could be more efficient when understanding well responses to individual stresses. For example, new data have pointed out beneficial effect of light (both intensity and quality) on response to temperature stresses, which is based on cross-talk between both signalling pathways (Janda et al., 2021; Romero-Montepaone et al., 2021). The detail description of individual stress responses could also highlight new potential ways of breeding, genetic manipulation and application of protectants. The other issue is the effect of pre-treatment with the same, but weaker stress—“acclimation” or “priming” (Hilker & Schmülling, 2019; Hossain et al., 2018). Acclimation to heat stress can significantly increase plant tolerance, even a shortterm acclimation event (minutes, a few hours) can be effective (Olas et al., 2021; Oyoshi et al., 2020; Sun et al., 2019). The enhanced tolerance of plants caused by previous acclimation is called “acquired thermotolerance.” By contrast, “basal thermotolerance” means the heat–stress tolerance without previous acclimation and plants with high basal thermotolerance belong to stress-resistant species (Larkindale et al., 2005). It is important to distinguish the acclimation made by stepwise increase of temperature or gradual heating. The effect of acclimation may differ when heat shock follows immediately or after some gap. The optimal length of gap depends on the “stress memory” (“thermomemory” in the case of heat stress) (Hilker & Schmülling, 2019; Olas et al., 2021). Stress memory is a set of changes caused by stress (or acclimation), which persists also after stress release. Different molecules exhibit specific dynamics; they may stay elevated for hours, days, weeks, but also longer. The stress tolerance achieved by endured stress can be even transferred to next generations, which is called “transgenerational memory.” This phenomenon is highly important for breeding and can be utilized by planting stocks from the places with similar climatic conditions. The transgenerational memory has been described also in heat stress-treated plants (Liu et al., 2015). Heat shock can sometimes reach extremely high temperatures. For instance, plants exposed half of a day to direct sunshine can fight with temperatures exceeding 45 °C at the canopy surface, a temperature that is bound to cause denaturation. There are plants, however, that are still able to survive, acclimation having a beneficial

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effect in the adaptation. The processes standing behind that extreme tolerance could reveal key points in the battle with climatic temperature fluctuation and the attention should be focused also on these very high temperatures, which are behind limits of commonly used climate chambers. In the case of heat stress, it is necessary to highlight the role of air humidity which dramatically influences plant heat sensitivity (Zheng et al., 2020). Relative air humidity related to temperature can be expressed as vapour pressure deficit (VPD) (Grossiord et al., 2020). Soil moisture in relation to VPD must be considered when plant abiotic stress is evaluated, because drought in combination with dry air and high temperature induces stomata closure and subsequent overheating of plants (Zhang et al., 2021). By contrast, VPD can be the reason why Arabidopsis plants grown on plates with 100% relative humidity die even at relatively low temperatures (Silva-Correia et al., 2014). It can be related to the comparison of temperature and humidity in a sauna and a steam bath. High water potential of air diminishes water transpiration efficiency and condensed liquid water in stomata can even plug the aperture. The impact of humidity is often ignored in studies, despite its critical role in plant heat–stress tolerance. Plants as sessile organisms are not able to escape from unfavourable conditions. They must adapt to long-term or periodical stress and tolerate or acclimate to shortterm stress in order to survive. The stress response is generally connected with changes in growth and morphology and it highly depends on developmental stage (Quint et al., 2016). As these processes are regulated by phytohormones, their role in stress responses is intensively studied (see Li, Euring, et al., 2021). This chapter summarizes changes in phytohormone pools and signal transduction associated with heat stress responses and suggests future ways of their study and application.

2 Sensing Thermal Stimuli by Plants Due to severity of heat stress with a risk of protein degradation, perception of temperature is highly evolutionary conserved among different organisms. However, temperature receptors in plants are still covered by uncertainty. Theoretically, a precise modelling of changes of 3D structures of the receptors caused by heat could clarify the primary impulse of heat sensing. The study of naturally heatadapted species could also bring some breakthrough about evolution of heat sensing as well as new possibilities of heat protection applicable in genetic manipulation. Despite the fact that many researchers have searched for the primary molecule activating the stress signalling responses (heat sensor), the truth is that the sensor is not unique and several molecules have been identified as sensors, which influence each other in an intensive cross-talk (Hayes et al., 2021). At the same level of importance as sensors, the role of physical changes in molecular structures caused by heat stress needs to be taken into account in activation of signalling pathways. Additionally, faster/diminished enzymatic reactions due

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to different temperature optimum can dramatically redirect pathways to branches, which are normally in minority. It affects sensing and influences nutrient and energy consumption as well as production of ROS (Lantz et al., 2019). The other highly important and mostly neglected topic includes non-enzymatic reactions, which definitely occur during heat stress (Keller et al., 2015). The variability of heat stress perception is unavoidable due to severity and speed of heat stress and a high risk of damage by this harsh condition if there was only one potential sensor. It explains also the interconnection of the regulatory pathways and multiple feedback loops and cross-talk among sensors, which lead to steady activation of the correct stress response. Moreover, temperature changes are not only stress-related, but they have diurnal and seasonal variations and these temperature oscillations are also sensed by plants (Bahuguna & Jagadish, 2015). All these signals vary with different onset, dynamics and temperature sensitivity, which probably fine-tune the sensing of even small temperature changes (Hayes et al., 2021). The precise timing and temperature dependence of individual interactions make the model of heat–stress responses very complicated, and only spatiotemporal modelling could shed light on the hierarchy of involved molecules. Nevertheless, the knowledge of individual processes has become wider during last decades when the web of interactions could be created. In this subchapter, the main temperature sensors are summarized.

2.1

Calcium

Heat stress activates cyclic nucleotide gated channels (CNGCs) causing Ca2+ import into cells (Finka et al., 2012). The channels are regulated by cyclic adenosine monophosphate (cAMP), which is synthesized from adenosine triphosphate (ATP) by adenylyl cyclase (AC) during the first minute of heat stress, suggesting that AC is thermosensitive (Gao et al., 2012). Downregulation of cAMP to control level occurs within 4 minutes. The cAMP binding site of CNGC was identified to be competitive with Ca2+ and calmodulin, indicating negative feedback (Hua et al., 2003). Nevertheless, Ca2+ could be transported into cytosol not only by CNGCs, but also by other cation channels, and some of them can be activated by change in membrane fluidity (Niu & Xiang, 2018) or by thermal changes in microtubules (Hayes et al., 2021). The precise mechanisms should be uncovered by modelling of the channel structure. Ca2+ rapidly activates signalling pathways based on phosphorylation of proteins, like mitogen-activated protein kinases (MAPKs) or calcium-dependent protein kinases (CDPKs); and via calmodulin it regulates other processes by calmodulinprotein kinases (CaMKs) (Hayes et al., 2021). The other important signalling cascades include transcription coactivator multiprotein bridging factor 1C (MBF1c), and transcription factors WRKY and dehydration-responsive elementbinding (DREB) (Niu & Xiang, 2018). DREB2A is a transcriptional activator that induces heat- and drought-responsive genes and increases tolerance to both heat and

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drought stress. Under control conditions, the protein is phosphorylated and fast degraded, but during stress progression, phosphorylation is inhibited, which stabilizes the protein (Mizoi et al., 2019).

2.2

Hydrogen Peroxide

Hydrogen peroxide (H2O2) is the second key heat–stress signalling molecule, which is universal for many stresses. Its production is enhanced during heat stress by respiratory burst oxidase homolog D (RBOHD) in apoplast (summarized in Hayes et al., 2021). The reaction requires NADPH. RBOHD is localized on plasma membrane and it is activated by cytosolic Ca2+ or phosphatidic acid (PA) released from membrane lipids. H2O2 is transported into the cell through a channel. H2O2 has to work together with Ca2+ in order to activate enzyme phospholipase D delta (PLDδ) as the result of heat stress, MAPKs and MBF1c. H2O2 is accumulated also in chloroplasts and mitochondria. It is a question whether the accumulation in organelles is caused by controlled production of H2O2 or by heat-induced excessive accumulation causing metabolic imbalance.

2.3

Membrane Lipids

Membrane lipids play two main roles in heat–stress signalling. Firstly, high temperature increases fluidity of membranes. Content of saturated lipids increases because of thermolability of fatty acid desaturases (FADs). The lipid bilayer also evidences active movement between the layers and small HSP (sHSP) intercalate into membranes, which both modulate the shape of membranes. Fluidic membrane enables entry of Ca2+ ions through cation channels. It also affects the movement, stability and the content of microdomains (Niu & Xiang, 2018). Simultaneously, phosphatidylinositol (4,5)-bisphosphate (PIP2) and phosphatidic acid (PA) are released from membranes by enzymes phosphatidylinositol phosphate kinase (PIPK) and PLDδ. PIP2 and PA serve as signalling molecules regulating multiple pathways in cells. Inositol 1,4,5-trisphosphate (IP3) is produced together with diacylglycerol (DAG) by PLC, and diacylglycerol kinase (DGK) transforms DAG to PA. IP3 is phosphorylated into IP6, which serves as a second messenger and regulates also Ca2+ intracellular stores. An IP6 receptor is not known (Niu & Xiang, 2018). Moreover, DAG was found to play a role in the connection of endoplasmic reticulum with plasma membrane. PLDδ itself can affect depolymerization of microtubules (Hayes et al., 2021).

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Light Receptors

Phytochrome B (PHYB) has been suggested as another potential temperature sensor, because its conversion from the active Pfr form to the inactive Pr one can be performed not only by far-red light but also by high temperature (Legris et al., 2016). This inactivating conversion stabilizes the transcription factor phytochrome interacting factor 4 (PIF4), which regulates many processes associated with heat stress as well as light responses (Janda et al., 2021). The activated PHYB under light conditions can cause phosphorylation of PIF4 and subsequent degradation in proteasome (Quint et al., 2016). PHYB can also sense small temperature deviations through disassembly from its nuclear compartments called photobodies (Hahm et al., 2020). The potential link between photobodies and the thermosensitive clock regulator early flowering 3 (ELF3), which creates liquid droplets under high temperatures, was highlighted in the review of Hayes et al. (2021). As far as light sensors are concerned, the possible role of the blue-light sensor phototropin has to be mentioned, too. Its active form is deactivated by high temperatures (Fujii et al., 2017). A few studies indicate the potential influence of increased temperature on other light sensors (cryptochromes, UV-B sensing UVR8, zeitlupes), but intensive research has to be done to elucidate how light signalling is involved in temperature sensing (Hayes et al., 2021; Janda et al., 2021).

2.5

Histones and Stability of Nucleic Acids

Heat stress influences DNA and RNA conformation and accessibility of regulatory elements. Some inactive genes start to be translated because of less coiled chromatin. Uncovering of unused DNA parts releases also transposons. In the case of DNA, modification of histones plays the critical role in chromatin remodelling (Kumar & Wigge, 2010). Namely, histone H2A.Z has been shown to regulate heat–stress responses as a sensor. It intercalates into nucleosomes, and after temperature increase, it is released, which enables the access of heat shock factor 1 (HSF1) (Cortijo et al., 2017). The composition of different nucleosomes containing H2A.Z and related chromatin condensation give high flexibility of heat sensing regulation, which means that this system is highly sensitive even to small temperature changes by 1 °C (Kumar & Wigge, 2010). Unfortunately, the effect of very small temperature changes is difficult to study because of temperature deviation in climate chambers and technical limits of sampling. Histone H3K4 was identified as one of the compounds inducing heat–stress memory, when it is triple methylated (H3K4me3) (Shekhawat et al., 2021). It is the key factor also in transgenerational memory, together with the methylation of DNA (Liu et al., 2015). Triple methylation of H3K36 (H3K36me3) is important for heat-induced flowering. H3K27me3 regulates transcription of heat-induced genes

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probably in connection with H2A.Z. Contrarily, acetylation of H3K9 reduces stress tolerance (Casal & Balasubramanian, 2019). Transcription and translation of genes can be affected also by the stability and shape of RNA. For example, the shape of the hairpin at the 50 -UTR of PIF7 mRNA was found to be affected by high temperatures, which stimulates gene translation (Chung et al., 2020). Furthermore, genes are subjected to alternative splicing leading to changed translation rate, subcellular localization, structure or activity of proteins (Ling et al., 2018). The transcription of microRNAs (miRNA) is noticeable after chromatin remodelling. Moreover, high temperatures reduce stability of RNA, fragments of which can be a source of small interfering RNA (siRNA). Small RNAs are highly produced under high temperatures (Ding et al., 2020; Liu et al., 2015; Singh et al., 2021). miR166 and miR6300 were found to inhibit expression of HSPs (Ding et al., 2020). miR156 is critical for thermomemory and its occurrence is highly evolutionary conserved. It targets squamosa-promoter binding-like (SPL) transcription factors, which regulate proper organ development (Stief et al., 2014). Recently, Pan et al. (2018) found that newly discovered circular RNAs (circRNA), the subgroup of small RNAs, are highly produced under heat stress. Function of these circRNAs includes also abscisic acid, salicylic acid and ethylene signalling. Endoplasmic reticulum has been shown to be critical point in the stress signalling as this is the place of translation and post-translational modifications, as well as maturation of transporters (e.g. Che et al., 2010; Deng et al., 2011; Feraru et al., 2019).

2.6

Heat Shock Proteins

High temperatures affect protein conformation, activity and the rate of dissociation of protein complexes. Chaperons which comprise HSPs significantly increase heat stress tolerance. They are expressed during heat stress (especially HSP70, HSP90 and HSP101), stabilize proteins and membranes and keep them in correct conformation. Small HSPs (sHSP) are generally upregulated by different stresses. They bind to aggregating proteins and enable protein refolding by interaction with high molecular weight HSPs like HSP101. Damaged proteins can be rapidly degraded by associated proteasome (Hayes et al., 2021). sHSP can be presented also during recovery after stress as the stress memory mechanism (Olas et al., 2021; Saksena et al., 2020). HSPs (specifically proved for HSP101) also protect 3D structure and stability of mRNA, which is important for thermomemory and recovery after stress (Merret et al., 2017). Under high temperatures, when the amount of misfolded proteins is beyond the critical point and they are also found in endoplasmic reticulum, the unfolded protein response (UPR) is activated. UPR involves HSP70, which accumulates around misfolded proteins and is released from bZIP17 and bZIP28 transcription factors.

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The bZIP factors are transferred into the nucleus, where they start transcription of stress-related genes, including HSPs (Deng et al., 2011). In the promoter regions of UPR-related genes, bZIP17 and bZIP28 compete with the bZIP repressor elongated hypocotyl 5 (HY5), which positively regulates blue-light signalling. HY5 is then degraded in proteasome via constitutive photomorphogenesis 1 (COP1) (Nawkar et al., 2017). The abundance of HSPs is a good marker of stress severity (e.g. Prerostova, Jarosova, et al., 2021). Isono et al. (2021) showed that strong UPR response can lead to early cell death and that the process is connected with the transport of proteins between endoplasmic reticulum and Golgi apparatus. They described the mechanism on the Arabidopsis mutant sensitive to long-term heat (sloh), which is hypersensitive to long-term heat stress (37 °C, 5 days), but not to the short-term one (37 °C 60 min). It has a defect in MAG2-interacting protein 3 (MIP3), a member of the tethering complex MAIGO 2 (MAG2) on endoplasmic reticulum, which enhance protein transport to Golgi. The mutant showed strongly enhanced UPR response of endoplasmic reticulum and died early. This indicates that the strong stress response could result in tissue senescence and that the process of cell death can be regulated or even reverted by fine-tuning of the signalling also under severe stress conditions. Chaperons can be activated by HSFs, transcription factors influencing expression of many stress-related genes. Transcription of HSFs is activated by Ca2+ signalling cascade (Hayes et al., 2021). HSFA1 is the key heat–stress transcription factor. It activates HSFA2, which can methylate histone H3K4 (H3K4me3) and by that induce a heat–stress memory (Shekhawat et al., 2021). The expression of HSPs and HSFs is fast (starting within 5 min) (Oyoshi et al., 2020).

2.7

Methyl Erythritol Cyclodiphosphate

An interesting potential powerful connection of heat sensing, light perception and phytohormones lies in the molecule 2-C-methyl-D-erythritol 2,4-cyclodiphosphate (MEcPP or MEcDP). MEcPP is an intermediate of the methyl erythritol 4-phosphate (MEP) pathway, which is besides mevalonate pathway the source of isoprenoids in plants. Isoprenoids are a large group of molecules participating in vital processes including photosynthesis, respiration, growth regulation, membrane permeability, antioxidant protection and volatile signalling (reviewed in Jiang & Dehesh, 2021). MEP pathway is plastidic, being more important in roots, which could be one of the main reasons why roots react faster, stronger and differently to heat stress than shoots. The first steps [enzymes 1-deoxy-d-xylulose 5-phosphate synthase (DXS) and 1-deoxy-d-xylulose 5-phosphate reducto-isomerase (DXR)] are induced by high temperatures. The intermediate MEcPP is processed by reductase GcpE, which is sensitive to oxygen, ROS (produced also during wounding), light and cadmium, and this enzyme is the rate limiting of the whole MEP pathway (Mongélard et al., 2011). In summary, high temperature increases MEP pathway, but the limiting

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stress-sensitive enzyme GcpE causes the accumulation of MEcPP and inhibition of the production of isoprenoids (Bjornson et al., 2017). MEcPP can activate the general stress regulators like calmodulin-binding transcriptional activator CAMTA3 (Jiang & Dehesh, 2021). It also upregulates the content of Pfr form of PHYB probably by inhibition of PIF4, which negatively affects the expression of auxin and ethylene biosynthetic genes (Jiang et al., 2020). Another possible way of the PHYB regulation could lead through B-BOX domain protein 19 (BBX19), which promotes turnover of ELF3 and creation of photobodies (Jones, 2019). All the mentioned regulatory pathways as well as the reduced synthesis of isoprenoids (including cytokinins, abscisic acid and gibberellins) explain the negative effect of MEcPP on plant growth and cell elongation. Mutant ceh1 (in hydroperoxide lyase 1), which accumulates MEcPP, has constitutive synthesis of salicylic acid. The synthesis of salicylic acid seems to be enhanced due to upregulated enzyme isochorismate synthase 1 (ICS1) by calmodulin-binding protein CBP60g, systemic acquired resistance deficient 1 (SARD1) and the transcription factor WRKY28. Double mutant ceh1/eds16 (mutation in ICS1) shows surprisingly similar regulatory mechanisms, which indicates tight connection of MEcPP and salicylic acid synthesis (Bjornson et al., 2017). The authors found that MEcPP stimulation is associated with upregulation of proteins related to endoplasmic reticulum, correction of protein folding, proteasome and transport, which correlates well with stress responses. Jasmonic acid was upregulated in specific organs and transcription of genes connected with pathogen interactions and glutathione metabolism was upregulated. Downregulated proteins were connected with photosynthesis and carbon metabolism, which can be associated with the decrease of isoprenoid synthesis (chlorophylls, carotenoids).

2.8

Volatile Compounds

The production of volatile compounds during heat stress treatment has been poorly characterized. Some small molecules exhibit transition to gaseous state by higher temperature; other volatile compounds can be released after oxidation/reduction or cleavage of side chains. The conversion to gas absorbs energy, by which the leaves can be cooled, but it is disputable if this conversion consumes enough energy to justify the release of organic carbon (Lantz et al., 2019). Isoprene was found to be produced during heat stress, improving plant tolerance (review in Lantz et al., 2019). It is produced by MEP pathway from dimethylallyl diphosphate and its optimal emission rate is about 45 °C. It is caused by isoprene synthase (ISPS) having an optimum of 42–45 °C, but the dimethylallyl diphosphate concentration peaks at 30–35 °C. It indicates that isoprene has important role also in the rapidly fluctuating temperatures (e.g. during partly cloudy weather). Isoprene content positively correlates with the content of carotenoids and chlorophyll indicating that the synthetic pathway is not diverted. Isoprene alters expression of genes related to synthesis and signalling of jasmonic acid, cytokinins, gibberellins,

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ethylene, auxin and salicylic acid (Zuo et al., 2019). Isoprene also negatively regulates the first enzyme of MEP pathway DXS (Lantz et al., 2019), which suggests a dampening of MEcPP production. Some mono- and sesquiterpenes were found to be rapidly released from tomato leaves under heat stress, being downregulated soon, but their abundance increased during recovery phase (Pazouki et al., 2016). The signalling of terpenoids in long distance goes probably through transient receptor potential (TRP) ion channels (Nguyen et al., 2021). However, the precise mode of action is still unknown. Dong et al. (2016) found that 2,3-butanediol, which is produced by bacteria, increases heat tolerance of plants by upregulation of genes related to cell elongation, metabolism and stress responses. It stimulates growth and affects sugar metabolism, cytokinins and jasmonic acid. This is an example of the potential beneficial signalization between microbes and plants. Some phytohormones are volatile and they can serve also as signal molecules, like methyl jasmonate and ethylene. Their roles in heat stress responses are described in detail in Sect. 4.

2.9

Photosynthesis

Photosynthesis is very sensitive to high temperature. Heat stress causes downregulation of its activity mainly due to manganese ion release from the cluster of the photosystem II, production of ROS and damage of protein complexes (especially D1 protein) (Niu & Xiang, 2018). Interestingly, heat stress induces synthesis of tocopherol from tyrosine in chloroplasts. Tocopherol enhances accumulation of 30 -phosphoadenosine 50 -phosphate (PAP), which is translocated into nucleus, where it inhibits exoribonucleases and by that protects mRNA from degradation (Fang et al., 2019).

2.10

Tissue-Specific Heat–Stress Responses

The experiments with organ-targeted heat stress showed that the sensing of heat stress is localized in the affected organs but the signal is transferred also into the non-exposed parts of plants (Macková et al., 2013; Prerostova, Jarosova, et al., 2021). All the mentioned studies highlighted different patterns of hormonal responses in roots in comparison with leaves, which are tightly connected with different roles of these tissues. In leaves, regulation of photosynthesis, transpiration, sugar production and nutrient utilization are the key processes affecting stress tolerance as well as subsequent recovery. In roots, nutrient and water uptake, and primary metabolism of nutrients seem to be the main regulatory mechanisms. Moreover, it seems that root tissues of rice as well as Arabidopsis react stronger to heat stress than leaves and are also more affected by acclimation (Bellstaedt et al.,

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2019; Prerostova, Jarosova, et al., 2021). The differences in responses are probably connected with the fact that root and shoot meristematic tissues are critical for plant survival, while leaves can be sacrificed (going to early senescence). It was observed in monocot rice as well as in dicot Arabidopsis (Prerostova et al., 2020; Prerostova, Jarosova, et al., 2021). Similarly, the production of antioxidant secondary metabolites was enhanced in roots of Panax quinquefolius, while leaves went to senescence (Jochum et al., 2007). The other explanation could be associated with the primary location of the synthesis of phytohormones—cytokinins and abscisic acid in roots, auxins in shoot meristematic tissue (Hwang et al., 2012; Matthes et al., 2019; Vishwakarma et al., 2017). The spatial differences in stress responses are also evident in the case of the protection of meristematic tissue (Prerostova et al., 2020). It seems that heat stress blocks stem cell identity causing delay of leaf formation and that this process is regulated by HSFA2 (Olas et al., 2021). Moreover, the authors showed the importance of the carbon source for heat stress tolerance and plant survival, especially in connection with fructose bisphosphate aldolase 6 (FBA6). Sharma et al. (2019) found that thermotolerance and thermomemory are dependent on glucose, which activates target of rapamycin (TOR)-mediated upregulation of HSPs. TOR also promotes trimethylation of histone H3K4 (H3K4me3) in regulatory regions of heat stress-related genes, which increases thermomemory.

3 Thermomorphogenesis Heat–stress signalling affects many processes in plants, which results in dramatic changes in regulation of plant growth and development, leading to thermomorphogenesis and adaptation. Heat stress responses can significantly differ in dependence on the actual temperature used. It is necessary to differentiate between a temperature promoting growth (warmth) and a temperature causing growth inhibition and even dying of tissues. The boundary between these two consequences can be fragile, as was shown in the case of sloh mutant (Isono et al., 2021), which gives an opportunity to revert the lethal stress progression by modulation of the signalling. Quint et al. (2016) summarized thermomorphogenic changes connected with specific temperature range in Arabidopsis. Warmth induces hypocotyl elongation of seedlings in order to escape from heat soil. Leaves move up in order to enhance cooling by wind and diminish sunlight. They have long petioles and short rounded blades. Roots are longer and curled. The morphological changes in other species have been reviewed by Casal and Balasubramanian (2019). In the case of monocots, growth is also supported and the number of leaves increases, while the leaf shape is not significantly changed. However, it depends on species, carbon metabolism and temperature optimum. The key regulator of thermomorphogenesis is PIF4, which coordinates the morphological changes with daytime in order to balance the source of water, nutrients and carbon assimilation. Recently, Kim, Hwang, et al. (2020) showed that the PIF4

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response to high temperatures is predominant in epidermis and to lower extent also in mesophyll cells, but not in vasculature tissue. Consequently, the synthesis and signalling of auxins and gibberellins happen predominantly in epidermis, affecting plant morphology. Li, Bo, et al. (2021) showed that PIF4 and PIF5 can promote also leaf senescence during heat stress and that this process includes cross-talk among many phytohormones (mainly abscisic acid, ethylene and jasmonic acid). The regulation goes through induction of the expression of transcription factors NAC domain containing protein 019 (NAC019), senescence-associated gene 113 (SAG113) and C-repeat/ DRE binding factor 2 (CBF2), as well as suppression of auxin/indole-3-acetic acid 29 (Aux/IAA29) transcription. Under heat stress conditions, the primary response is the opening of stomata, which supports transpiration and cooling of a plant. However, water consumption is high and the dependence on water supply is critical, leading to wilting in the combination with drought. Stomata closure is driven by ABA, while their opening is antagonistically directed by cytokinins (Macková et al., 2013). In response to long-term elevated temperature, leaves are thinner and have fewer stomata. PIF4 directly suppresses expression of speechless (SPCH) transcription factor, which serves as the master regulator of stomatal initiation, resulting in fewer stomata. Vice versa, SPCH negatively regulates PIF4 transcription in a feedback loop (Lau et al., 2018). Phosphorylation of MAPK cascade, including the kinase YODA, which leads to phosphorylation of SPCH and inhibition of its function, is stabilized by HSP90 (Samakovli et al., 2020). Cytoskeleton structures can modify particle movement in cells and stability of cytoskeleton, which leads to morphological changes (Hayes et al., 2021). Flowering is probably influenced by alternative splicing of the transcription factor flowering locus M (FLM), which represses flowering locus T (FT) (Bao et al., 2020). The warm temperature-induced modification of transcription, which is still not clearly explained, causes earlier flowering. PIF4 can directly bind to FT promoter inducing flowering. Nevertheless, study of double mutant flm pif4 revealed that the flowering is regulated by other processes, too (Casal & Balasubramanian, 2019). The role of phytohormones during flowering and grain production in rice in the relation to heat stress was summarized in Wu et al. (2019). Surprisingly, UV-B as well as long day diminishes thermomorphogenesis despite the fact that heat stress endangers plants mostly in summer days (Casal & Balasubramanian, 2019). Casal and Balasubramanian (2019) assumed that this effect may be connected with shade avoidance response. But this hypothesis is in contradiction with van der Woude et al. (2019), who described distinct regulatory pathways of thermomorphogenesis and shade avoidance. Another option is that responses induced by high summer temperatures may be so intensive (as in Isono et al., 2021) that the signalling caused by UV-B radiation or long day can in fact suppress the overreaction to the heat, resulting in overall better conditions of the plants. The correct cross-talk is yet to be discovered.

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4 Phytohormones Involved in Heat Stress Responses Phytohormones regulate plant growth and development and they are also involved in the stress responses. They affect fast physiological processes, morphological adaptations as well as production of protective compounds (reviewed in Li, Euring, et al., 2021). Characterization of the role of individual phytohormones is complicated by their intensive cross-talk (Sharma et al., 2020). Auxin and cytokinin cross-talk can be driven by synergistic on auxin and cytokinin 1 (SYAC1), expression of which is in roots tied up with pathways of both hormones (Hurný et al., 2020). Concentrations of auxins, gibberellins and brassinosteroids are positively affected by PIFs. Important regulatory mechanisms target the MEP pathway of isoprenoid biosynthesis, which is common for several phytohormones, namely abscisic acid, strigolactones, gibberellins and cytokinins (Quint et al., 2016). Phytohormones, especially abscisic acid and auxins, are influenced by melatonin, which seems to have a regulatory role in heat stress responses (summarized in Wang et al., 2018). The other important regulator of phytohormones involved in stress responses (including heat stress) is the receptor-like protein kinase feronia (FER). FER mediates the cross-talk among auxins, brassinosteroids, abscisic acid, ethylene, gibberellins and H2O2. It is involved in root hair formation. The precise mechanisms of FER mode of action need to be uncovered (Liao et al., 2017). It is necessary to keep in mind the dynamics of phytohormone levels during the progression of the stress responses. For example, transient upregulation of cytokinins associated with stimulation of transpiration at the early phase of heat stress response is followed by their decrease, while cytokinin drop upon cold shock is followed by their increase during acclimation. The responses differ among the individual organs. In the case of severe stress, plants protect preferentially the tissues most important for plant fitness and survival, predominantly root and shoot meristematic tissues (Prerostova et al., 2020; Prerostova, Jarosova, et al., 2021). It can be associated with the site of phytohormone production. Besides the active forms of phytohormones, also the levels of their conjugates seem to be important in stress responses, too. They may provide important information about preceding plant reactions. Some conjugations convert hormones to inactive deactivation products which are subsequently metabolized (e.g. auxin conjugates with amino acids, cytokinin N-glucosides). Other modifications can reversibly deactivate a hormone. The resulting conjugate can be stored and reutilized when necessary or transported to long distance (e.g. abscisic acid-glucosyl ester, cytokinin O-glucosides or ribosides), saving energy and nutrients necessary for de novo synthesis. This strategy is often used by highly tolerant species or it can be observed after acclimation (Prerostova, Zupkova, et al., 2021). Some conjugations can be crucial for the activity of a hormone (for example jasmonoyl-isoleucine; Wasternack & Song, 2017), or create a volatile compounds which can represent a rapid signal to unstressed tissues (like methyl jasmonate; Su et al., 2021). It is also necessary to take

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into account the non-enzymatic reactions, which can (de)activate phytohormones in different ways (Keller et al., 2015). The effect of phytohormones was summarized, e.g. in Islam et al. (2018), Sharma et al. (2020), and Jha et al. (2021).

4.1

Abscisic Acid

Abscisic acid belongs to isoprenoid phytohormones. It is a key regulator of abiotic stress responses. Its short-term effects include stomata closure, the longer-term ones stimulation of production of protective compounds (Vishwakarma et al., 2017). It also enhances antioxidant capacity. The role of abscisic acid in high temperature responses was summarized by Islam et al. (2018). Abscisic acid induces sHSPs and HSP70 under heat stress (Islam et al., 2018). The transcription factor ABA-responsive element binding protein (AREB) binds directly to cis-regulatory elements of HSFA genes, activating their expression; and oppositely, HSFAs induce abscisic acid synthesis (Wang et al., 2017). Abscisic acid also upregulates RBOHD expression and by that the production of H2O2 (Li, Euring, et al., 2021). During heat stress, photosynthesis is diminished and Mg-protoporphyrin IX activates genome uncoupled 1 (GUN1) protein, which is transported to nucleus, where it supports the bZIP transcription factor abscisic acid insensitive 4 (ABI4). Similarly, heat-induced damages of the respiratory electron-transport chain in mitochondria and the accumulation of ROS release signalling molecules into nucleus, also activating ABI4. ABI4 is a central regulator of many signalling pathways related to environmental cues, plant growth and developmental changes (Niu & Xiang, 2018). ABI4 also stimulates metabolism of starch through activation of the transcription factor NAC60. Sugar-related genes affected by abscisic acid include sucrose transporter (SUT), sucrose synthase (SUS) and invertase (INV), suggesting promotion of energy for the synthesis of protective compounds as well as release of the signalling sugar molecules (sucrose, glucose and fructose) (Islam et al., 2018). The starch catabolism seems to be the limiting factor in the phase of seed production. Together with low levels of cytokinins and gibberellins, which support source-sink transport of nutrients to developing seeds, the higher levels of abscisic acid yield smaller seeds and low yield (Asthir, 2015). The regulation of stomata opening is dependent predominantly on the ratio cytokinins/abscisic acid. When plants have upregulated cytokinin content, the ratio increases leading to stomata opening and decrease of endogenous temperature (Dobrá et al., 2015; Macková et al., 2013). The ratio seems to be important also in other processes during whole ontogenesis (Vishwakarma et al., 2017). When plants are exposed to long-term heat stress, their morphological adaptation evidences lower amount of stomata (Quint et al., 2016). Decrease of stomata establishment is

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supported by abscisic acid, jasmonic acid and brassinosteroids and the whole process is regulated in cross-talk with other phytohormones (Wei et al., 2021). Abscisic acid is upregulated under high temperatures also in seeds, inhibiting germination through transcription factor ABI5. Chen et al. (2019) showed that the ABI5 transcription is activated by HY5, which is not degraded because of sequestration of COP1 ubiquitin ligase from nucleus. They also found that hydrogen sulphide H2S can reverse COP1 transport, keeping high level of COP1 in the nucleus, degradation of HY5 and block of ABI5 transcription, which leads to increased thermotolerance of seed germination. However, as mentioned in Sect. 2.6, HY5 is the negative regulator of heat–stress responses because of blocking of UPR-related genes. It means that the regulation of these heat–stress responses will be more complicated. Abscisic acid promotes biosynthesis of salicylic acid and vice versa. Both hormones together with H2O2 are involved in stress memory (Islam et al., 2018). Abscisic acid attenuates brassinosteroid signalling; however, brassinosteroids support the content of abscisic acid under heat stress, which responses are probably driven by H2O2 (Zhou et al., 2014). The influence of abscisic acid on auxin and gibberellins is variable during heat stress and probably tissue- and developmental stage-specific (Islam et al., 2018). The levels of abscisic acid are tightly connected with drought stress and the study of heat stress in soil conditions can be affected by soil moisture and relative air humidity. In the case of plants grown in well-watered conditions, hydroponics or on plates, in which drought stress is excluded, the changes in abscisic acid levels caused by heat stress are not so high as in combination with drought and the dynamic is different. Recovery after heat stress may be connected with increase of abscisic acid content, probably associated with the synthesis of protective compounds and stress memory (Islam et al., 2018; Prerostova et al., 2020). Contrarily, recovery after heat stress combined with drought caused downregulation of much higher levels of abscisic acid (Macková et al., 2013). Abscisic acid has been shown to serve as a universal priming hormone, which can induce tolerance to variety of abiotic stresses when it is applied before the stress (Li, Euring, et al., 2021).

4.2

Salicylic Acid

Salicylic acid is a phenolic phytohormone involved in stress responses in general, playing a crucial role after biotroph attack. It is synthesized by the shikimate pathway in chloroplasts. The signalling pathway includes the release of the transcriptional activator nonexpressor of pathogenesis-related genes 1 (NPR1) monomers from oligomers in cytoplasm and their transport into nucleus. Binding of NPR1 to TGA transcription factors activates the expression of salicylic acid-inducible genes, including pathogenesis-related (PR) genes. Salicylic acid activates antioxidant system in order to scavenge ROS and protect photosynthetic apparatus. It

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induces systemic resistance to pathogens (Khan et al., 2015). Previous studies showed that exogenous salicylic acid can improve heat stress tolerance (Li, Euring, et al., 2021). Clarke et al. (2004) described that salicylic acid is involved in the basal thermotolerance (i.e. the tolerance without previous acclimation), because the constitutive overexpresser of PR genes, cpr, exhibited high thermotolerance. Nevertheless, the tolerance was maintained during recovery phase. Salicylic acid upregulated HSP21 chaperone in tomato chloroplasts, which could be linked to stress memory (Wang et al., 2010). Prerostova et al. (2020) found higher levels of salicylic acid only in roots of 5-week-old Arabidopsis plants acclimated to heat stress, which also suggests connection of salicylic acid with thermomemory and better stress tolerance, as well as with the root protection. The thermomemory is probably associated with the protection of D1 protein against degradation and with stabilization of the active state of the complex ribulose-1,5-bisphosphate carboxylase/oxygenase (RUBISCO), supporting photosynthesis (Wang et al., 2010; Zhao et al., 2011). Typically, salicylic acid induces under heat stress synthesis of proline (Sharma et al., 2020), which seems to be an important component of heat stress memory. Its upregulated levels, however, rather negatively correlated with basal thermotolerance of several species (Hu et al., 2015). Huot et al. (2017) showed that higher temperature as well as the pathogen Pseudomonas syringae can downregulate biosynthetic enzyme isochorismate synthase 1 (ICS1) and cause low levels of salicylic acid. Similarly, PIF4 enhanced by high temperatures was found to repress immunity causing suppression of defence-related genes such as PR1 and PR5 (Casal & Balasubramanian, 2019). The results demonstrate that combination of heat and biotic stresses can have antagonistic responses, balance of which is directed by salicylic acid. Possible regulation of salicylic acid pathways could be mediated by the interaction with other phytohormones, but the cross-talk is not well described. Gibberellins regulate salicylic acid during seed germination and seedling growth in order to increase thermotolerance (Sharma et al., 2020). Abscisic acid could probably stimulate salicylic acid synthesis (Islam et al., 2018). The interaction between salicylic and jasmonic acid during heat stress is probably mediated by the transcription factor WRKY39, which activates signalling pathways of both hormones (Li et al., 2010). WRKY39 possibly acts upstream of PR1 and downstream of MBF1c.

4.3

Jasmonic Acid

Jasmonic acid is a fatty acid-derivate, which is synthetized in chloroplasts from α-linolenic acid, which arises from DAG produced by PLD. Linolenic acid is metabolized to 12-oxo-phytodienoic acid (OPDA), which is transferred to peroxisomes. Biosynthetic pathway is finished by a series of oxidations. Jasmonic acid is conjugated with isoleucine and resulting jasmonate-isoleucine binds to the receptor F-box protein coronatine insensitive 1 (COI1), which then directs transcriptional

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repressor jasmonate-ZIM domain proteins (JAZ) to proteasome, activating transcription of jasmonic acid-inducible genes (Wasternack & Song, 2017). Jasmonic acid (as well as its isoleucine conjugate) is accumulated during heat stress and it can have beneficial impact on plants. It is a part of basal thermotolerance (Clarke et al., 2009), but it is probably not involved in acquired thermotolerance (Muench et al., 2016). It stabilizes membranes. It protects also photosystems, as its limitation causes chlorosis. Jasmonic acid effect could be the result of the stabilized membranes (Li, Euring, et al., 2021). Interestingly, jasmonic acid as well as its methyl derivative supresses stomata development in control conditions, but the process is not clear in the relation to heat stress (Wei et al., 2021). It is possible that the stomata reduction is connected with long-term stress or with heat stress combined with drought. High temperature increases levels of OPDA, a precursor of jasmonic acid (Sharma et al., 2020). Jasmonic acid synthesis in chloroplasts is upregulated by MEcPP, while the continuation of the biosynthetic pathway in peroxisomes is not significantly affected (Bjornson et al., 2017). Some members of the group of the biosynthetic enzymes lipoxygenases (LOXs) were found to be regulated specifically under high temperatures in tomato—namely SlLOX5 was upregulated and SlLOX1 and SlLOX3 were downregulated (Upadhyay et al., 2019). HSP90 makes complex with HSP70, co-chaperone required for MLA12 resistance 1 (RAR1) and its interactor suppressor of the G2 allele of SKP1 (SGT1). SGT1 specifically binds to F-box protein COI1 and stabilizes it. In summary, HSP90 and HSP70 boost the degradation of JAZ repressors and transcription of jasmonic acidinducible genes. This kind of interaction is different from, e.g. the HSP90-induced brassinosteroid signalling pathway (Zhang et al., 2015). MEcPP probably also affects COI1 (Bjornson et al., 2017), but the pathway could go through HSP90 regulation. This hypothesis needs to be proved. In a positive feedback loop, jasmonic acid promotes the accumulation of several HSPs (including HSP101) by activation of HSFA1 transcription (Muench et al., 2016). This pathway goes via several WRKY transcription factors (WRKY25, WRKY26, WRKY33 and WRKY39) induced by jasmonic acid (Li, Euring, et al., 2021). They stimulate also synthesis of antioxidants (Sharma et al., 2020). The same WRKY transcription factors connect the pathway with abscisic acid and ethylene. However, ethylene works antagonistically during heat stress responses (Li, Euring, 2021). Despite the fact that jasmonic acid increases heat stress tolerance, jasmonic acid induced by wounding or insect herbivory was shown to block heat–stress changes like closing stomata and leaf hyponasty, probably due to its overaccumulation. The stress combination led to susceptibility of plants to the damage caused by herbivores as well as by overheating because of closed stomata (Havko et al., 2020). OPDA in wounded plants did not activate HSP expression (Muench et al., 2016). Jasmonic acid can be transported over long distance within a plant, but its volatile methyl derivative spreads the signal much faster to upper leaves as well as to the neighbour vegetation. Methyl jasmonate formation is catalysed by jasmonic acid carboxyl methyltransferase (JMT) and it can be reversibly converted back to

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jasmonic acid by methyl jasmonate-specific methyl esterase (MJE) (Yu et al., 2019). No evidence has been found of methyl jasmonate effect on the expression of HSPs and thermotolerance (Sharma et al., 2020). However, methyl jasmonate causes protection of proteins involved in photosynthesis, and in this way, it may increase recovery rate after heat stress (Fatma et al., 2021). It also stimulates production of anthocyanins and other antioxidants (Thakur et al., 2019). The analysis of promoters with potential binding sites for methyl jasmonate revealed that it could stimulate expression of some jasmonic acid-induced genes, genes for synthesis of flavonoids and terpenoids (Sadeghnezhad et al., 2019).

4.4

Ethylene

Ethylene is a simple alkene, as a gas it can rapidly influence distant parts of a plant or neighbouring plants. Its synthesis includes the Yang cycle, in which methionine is converted to S-adenosylmethionine (SAM). SAM is converted to aminocyclopropane-1-carboxylic acid (ACC) by ACC synthase (ACS). ACC can be metabolized to a range of compounds, which have different functions, connecting, for example, the pathway of jasmonic acid or polyamines. ACC is the direct precursor of ethylene, which is synthetized by ACC oxidase (ACO) (Poór et al., 2021). As the ethylene level is usually determined as ACC level (assuming correlation), the role of the other pathways proceeded from ACC under heat stress conditions is not known. Ethylene (as well as ACC) increases heat stress tolerance and its biosynthesis is probably promoted by ROS via MAPK MPK6 (Müller & Munné-Bosch, 2015). Ethylene is accumulated in high temperatures, especially in the shoot apical meristem (Poór et al., 2021; Prerostova et al., 2020). However, the responses seem to be dependent on developmental stages, species specificity and severity of the stress. Ethylene upregulation under heat stress can be probably connected with two distinct effects. Firstly, ethylene in lower concentrations can activate stress-related proteins that are involved in maintaining stability of plant cells due to the reduction of oxidative stress by enhancement of antioxidant enzyme activity and maintaining chlorophyll content. It increases plant stress tolerance. Secondly, ethylene in higher concentrations induces senescence, which negatively affects fertility and seed production, and leads to leaf death (Poór et al., 2021). The boundary concentration between these two ethylene effects and the knowledge how to modify it could bring new possibilities of elevation of stress tolerance in crop plants. Interestingly, the beneficial effect of lower ethylene concentrations is also inhibition of fruit ripening during heat stress, which can be reversed during recovery phase. The restoration of fruit senescence and ripening is caused by de novo produced ACS and ACO enzymes, not by their activation (Biggs et al., 1988). In Arabidopsis, ACS6, ACS7, ACS8, ACS10, ACS11, ACS12, ACO2 and ACO4 were found to be strongly induced under heat stress, whereas ACS2, ACS4, ACS5, ACO1, ACO3 and ACO4 were negatively regulated (Poór et al.,

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2021). Ethylene synthesis through ACS4, ACS5 and ACS8 was negatively affected also by MEcPP, which downregulates PIF4, repressing ACS transcription (Jiang et al., 2020). ACS7 probably suppresses thermotolerance due to inhibition of abscisic acid synthesis and signalling (Dong et al., 2011). Stability of N-terminal ACS7 sequence is enhanced by senescence (by phosphorylation), while fast turnover is mediated by direct interaction with protein phosphatases of the type PP2C ABI1, ABI2 and hypersensitive to ABA 1 (HAB1) (Marczak et al., 2020; Sun et al., 2017). Temperature-related signalling of ethylene is connected with the upregulation of receptors ethylene receptor (ETR1 and ETR2) and enhancer of shoot regeneration 2 (ERS2), (Poór et al., 2021). The crucial component of ethylene signalling is ethylene insensitive 2 (EIN2), which blocks degradation of transcription factors EIN3 and ethylene insensitive 3-like (EILs) and is suppressed by constitutive triple response (CTR1). EIN2 is also affected by high temperatures (Poór et al., 2021). EIN2 was reported to be a repressor of thermotolerance, because ein2 mutant displayed better resistance (Clarke et al., 2009). However, Larkindale et al. (2005) described reduced basal (not acquired) thermotolerance of ein2 and etr1 mutants, which is in contradiction. The difference could be given by different stress duration, because Clarke et al. (2009) used 38 °C for 16 h, while Larkindale et al. (2005) exposed younger plants to 45 °C for 1 h. EIN2 could be one of the factors influencing stress response direction to senescence. It could be interesting to uncover the other regulatory pathways influencing EIN2. Yu et al. (2021) highlighted that the transcription factor WRKY71, which is activated by ethylene, induces senescence. Moreover, WRKY71 supports transcription of ACS2 and by that the synthesis of ethylene in a positive feedback loop. WRKY71 stimulates EIN2 signalling and also the EIN2-downstream transcription factor from NAC family ORESA 1 (ORE1). Interestingly, ORE1 can be upregulated also by PIF4 or abscisic acid inducing cell death (Kim, Kim, et al., 2020). These genes (especially WRKY71) could reveal the boundary between senescence and thermotolerance. Transcription factors EIN1 and EIN3 seem to positively react to high temperatures, while EIN4, EIN5, EIN6, EIL1, EIL2 and EIL3 exhibited downregulation. In addition, EIN3 was upregulated also during recovery (Poór et al., 2021). EIN3 can activate HSFA2 factor directly, not through HSFA1. EIN3 expression can be affected by beneficial endophytes (Shekhawat et al., 2021). This link gives new opportunities for elevation of heat–stress tolerance in the field. Transcription factors ethylene response factors (ERF) from the group VII were found to enhance stress tolerance to different abiotic stresses including heat stress. They bind to dehydration-responsive elements (DREs) in promoters of stressresponsive genes, which induces their expression and enhances heat tolerance (Müller & Munné-Bosch, 2015). ERF1 stimulates the production of HSFA3, HSP70, HSP101 and proline under heat stress conditions. It positively links pathways of ethylene and jasmonic acid as well as the signalling of heat, salt and drought stresses, but it is negatively regulated by abscisic acid (Cheng et al., 2013; Müller & Munné-Bosch, 2015). ERF53 expression is activated by heat, drought and salt stresses and it positively regulates transcription of stress-related genes (like HSPs)

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and genes related to abscisic acid and proline synthesis (Hsieh et al., 2013). ERF47 (and to a lesser extent also ERF75) activates transcription of RBOHD genes, leading to production of H2O2 on plasma membrane. H2O2 activates synthesis of heatresponsive genes, but also the expression of antioxidant enzymes, which balance the content of H2O2. The transcription of antioxidant enzymes is, however, delayed (Yao et al., 2018). Transcription factor ethylene-responsive element binding protein (EBP) was found to be downregulated during heat stress (Poór et al., 2021). ETR1 can link the pathway of cytokinins; EIN2 links the jasmonic acid pathway (Binder, 2020). The response of ethylene and jasmonic acid is late (ca 2 h after the beginning of the stress) in comparison with abscisic and salicylic acid increase during the first hour (Pistelli et al., 2019). The possible influence of abscisic acid pathway was shown on ACS7 or ERF53 (Dong et al., 2011; Hsieh et al., 2013). Salicylic acid is able to reduce ethylene synthesis, which strengthens the accumulation of protective proline (Khan et al., 2013). However, ethylene signalling through ERFs can be induced by salicylic acid (Poór et al., 2021). High temperature inhibits the apical hook formation of seedlings treated by ethylene in dark. It seems that the inhibition is not the result of disrupted ethylene signalling through transcription factor EIN3, but of auxin downregulation (Jin et al., 2018).

4.5

Auxins

Auxins belong to indole-type phytohormones regulating growth and cell elongation (Matthes et al., 2019). Auxins are one of the main regulators of thermomorphogenetic changes under warm temperature. Upward leaf movement, hypocotyl and petiole elongation and root curling are characteristic for thermomorphogenesis as well as for the shade avoidance. However, van der Woude et al. (2019) found that the heat–stress response is driven by specific pathway containing the chromatin-modifying enzyme histone deacetylase 9 (HDA9), which is stabilized only under higher temperatures and which mediates histone deacetylation at the YUCCA 8 (YUC8) gene locus eliminating the presence of repressing histone H2A.Z. This chromatin remodelling enables PIF4 transcription factor to bind to auxin biosynthetic genes YUC8, cytochrome P450 (CYP79B2) and tryptophan aminotransferase of arabidopsis 1 (TAA1) and signalling genes transport inhibitor 1 (TIR1), Aux/IAA19 and Aux/IAA29. Interestingly, the synthetic auxin-responsive promoter DR5 is also heat-sensitive (Casal & Balasubramanian, 2019; Quint et al., 2016). Similarly, as in the case of jasmonic acid, HSP90 directly interacts with the auxin receptor TIR1 (F-box protein), together with co-chaperone RAR1 and its interactor SGT1. The interaction promotes TIR1 stability, which stimulates root and shoot elongation at warm temperatures (Wang et al., 2016). Kim, Hwang, et al. (2020) found that the heat responses of PIF4 as well as of auxins are predominantly localized in epidermis and partially also in mesophyll cells, which affects thermomorphogenesis.

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Synthesis of auxin indole-3-acetic acid (IAA) from the precursor indole-3pyruvic acid (IPyA) can be upregulated during high temperatures by YUC8 enzyme. Simultaneously, IPyA may be glucosylated by UDP-glycosyltransferase 76F1 (UGT76F1). Glucosylation occurs often under light conditions, resulting in IAA synthesis inhibition, but heat stress induced PIF4 directly blocks the expression of UGT76F1 (Chen et al., 2020). YUC2 and YUC6 were found to be downregulated by heat stress causing male sterility due to local auxin limitation. The exogenous application of auxin restored the fertility (Bielach et al., 2017). The enzymes conjugating IAA with amino acids, gretchen hagen 3 (GH3), can be upregulated by high temperature resulting in deactivation of auxins, having inhibitory effect on high auxin levels caused by the heat stress (Bielach et al., 2017). miR160 and miR167 were found to block expression of auxin response factor ARF10, ARF16 and ARF17, increasing plant thermotolerance, because the auxinrelated transcription factors inhibit HSPs transcription (Lin et al., 2018). PIF4 upregulates also small auxin up RNA (SAUR19-24 and SAUR61-68), which interact with auxin and induce H+-ATPase on plasma membrane. Protons acidify apoplast and stimulate cell elongation and cell wall production. Under normal conditions, SAURs are directly inhibited by protein phosphatases type 2C belonging to the D subfamily (PP2C.D), but warm temperature probably blocks this interaction through post-translational modifications of PP2C.D. Nevertheless, PP2C. D can be activated after a delay also by high temperatures indicating negative feedback loop preventing overgrowth (Quint et al., 2016; Ren et al., 2018). PIF4 activates auxin transporter pin-formed 1 (PIN1). MEcPP through inhibition of PIF4 and upregulation of the active PHYB form negatively affects the expression of auxin biosynthetic gene YUC8 and the distribution of PIN1 transporter (Jiang et al., 2020). Feraru et al. (2019) showed that PIN-likes 6 (PILS6) auxin transporter is temperature-sensitive. It is localized on the membrane of endoplasmic reticulum and removes auxin from cytosol under control conditions. PILS6 is degraded under heat stress, which promotes auxin accumulation in the cytosol. This response is characteristic for roots. Auxin transport is regulated also by HSP90, which interacts with twisted dwarf 1 (TWD1), the membrane-associated protein localized at the endoplasmic reticulum, plasma and vacuolar membranes. TWD1 seems to control the maturation and positioning of ABCB auxin transporters on the plasma membrane (di Donato & Geisler, 2019). Cell elongation under warm temperatures, positively affected by auxins, seems to be dependent on other phytohormones. Gibberellin synthesis and signalling are also directly regulated by PIF4. Moreover, DELLA repressors of gibberellin signalling, which are degraded under high temperatures, supress transcription of the auxin signalling component ARF6 (Quint et al., 2016). Auxin in shoot apical meristem supports stem elongation through brassinosteroids and their signalling pathway (Bellstaedt et al., 2019). Interestingly, PIF4 can be also activated by cytokinins through type-B response regulators ARR1 and ARR12, which can connect auxin and cytokinin pathways (Di et al., 2016). This finding brings new possibilities of the regulation of thermomorphogenesis. Another potential cross-talk might occur via SYAC1, a

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regulator of secretory pathway connected with both auxins and cytokinins, enhanced activity of which interferes with cell wall deposition and organ growth (Hurný et al., 2020). High temperature causes the inhibition of the apical hook formation of seedlings induced by ethylene in dark. This phenomenon is caused by low local levels of auxin as a result of downregulated YUC genes and auxin transporters, not by ethylene signalling. The precise mechanism is not known but the hook formation is not influenced by PIF4, which means that heat stress response of seedlings in dark has to be connected with other sensors (Jin et al., 2018). Severe heat stress causing growth inhibition results in decrease of auxin levels in roots, which can be explained by the suppression of auxin polar transport (Bielach et al., 2017; Prerostova et al., 2020). Exogenous application of auxin alleviates the negative effects of stress (Sharma et al., 2018). Sheldrake (2021) hypothesizes that auxin IAA biosynthesis enhanced during stresses may be connected also with intensive protein degradation, which would increase the levels of the IAA precursor tryptophan.

4.6

Cytokinins

Cytokinins are adenine derivatives with isoprenoid or aromatic side chain at N6 position. The most studied cytokinins have an isoprenoid side chain: isopentenyladenine (iP), trans-zeatin (tZ), cis-zeatin (cZ) and dihydrozeatin (DHZ). The role of aromatic ones is much less known, because of their limited occurrence in plants. Nevertheless, they are often used in in vitro cultivation because they are stable, poorly degraded by cytokinin oxidase/dehydrogenase (CKX) enzymes, while they show strong cytokinin effect (Hluska et al., 2021). Cytokinins are indispensable for cell division, growth and development (especially trans-zeatin and isopentenyladenine). They induce also stomata opening, stabilize photosynthesis machinery and delay senescence (Hwang et al., 2012). Černý et al. (2014) described the proteomes of differently treated plants and they found that cytokinin response is highly similar to heat stress response, which indicates the involvement of cytokinins in the heat stress reaction. Early heat stress response is associated with transient elevation of stomata opening in order to promote transpiration, the main cooling mechanism in plants. Stomata opening is regulated by the ratio cytokinins/abscisic acid (Hwang et al., 2012). Cytokinins lead opening and abscisic acid closing of stomata (the ratio cytokinins/abscisic acid decreases during closure). This ratio is crucial also in other processes in plants and it seems to be more important than actual hormone concentrations. Cytokinins exhibit dynamic changes during heat stress response. The early response to heat shock (ca about 30 min) is connected with opening of stomata aperture and elevation of the cytokinin content. This cooling mechanism allows plants to keep the leaf temperature cooler than the environment before the defence

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mechanisms can be activated. Long-term cytokinin impact is associated with the protection of photosynthetic apparatus, carbon accumulation, production of antioxidants and senescence inhibition (Dobrá et al., 2015; Macková et al., 2013; Skalák et al., 2016). Enhancement of source–sink transport is also directed by cytokinins (Lubovská et al., 2014). Černý et al. (2014) emphasized that the role of cytokinins in heat–stress responses is tightly linked with chloroplasts, the organelles involved in above-mentioned processes. Positive effects of cytokinins have been observed during long-term warmth (e.g. Xu et al., 2009). Some studies focused on the recovery after stress indicate that cytokinins support growth restoration (e.g. Prerostova et al., 2020). The actual cytokinin effects depend on the individual active cytokinin form. The most physiologically active cytokinin in stimulation of cell division, trans-zeatin, is downregulated by heat stress in the later stages and its levels increase much later again. Isopentenyladenine is downregulated by heat stress, too, but it seems to be important for restoration of cytokinesis during recovery phase (Prerostova et al., 2020). Dihydrozeatin has low activity; it is present in minor levels and not degraded by CKX enzymes (Hluska et al., 2021). High dihydrozeatin levels are probably connected with severe stress (Prerostova et al., 2017). No significant changes in dihydrozeatin content have been detected under heat stress. All the mentioned cytokinins are produced in plastids by MEP pathway, which is affected by high temperatures; nevertheless, the precise mechanism of regulation of cytokinin levels by heat stress is unknown. More and more studies show that cytokinin cis-zeatin (and its riboside), the stereoisomer of the highly active trans-zeatin, is upregulated in stresses conditions. cis-zeatin could be connected with cytokinin-related processes in stress, like elongation of roots and root hairs, as was mentioned in the case of phosphate starvation (Silva-Navas et al., 2019). It has a role in maintaining of basal cytokinin functions (except strong stimulation of cell division), e.g. accumulation of antioxidants (Prerostova, Jarosova, et al., 2021). This type of cytokinins is synthesized in cytosol by mevalonate (MVA) pathway, which could be affected by heat stress (Balti et al., 2020). At least partial biosynthesis through tRNA degradation indicates connection of cis-zeatin with tRNA stability (Kamínek, 2015). Nevertheless, the role of ciszeatin and its riboside in different stress responses and the link with stress tolerance should be elucidated in detail (e.g. Prerostova, Zupkova, et al., 2021). cis-zeatin-type cytokinins represent predominant cytokinin forms in some monocot species, e.g., maize (Gajdošová et al., 2011). The possibility of the conversion between cis and trans form is limited; a non-enzymatic mechanism was proposed (Keller et al., 2015). But this topic requires further research. Isoprene synthesis has the same pathway as cytokinins. Černý et al. (2014) hypothesized that upregulation of MEP pathway by heat stress leads to intensive production of isoprene in order to balance cytokinin homeostasis, among other things. But the regulation could be connected with other isoprenoid phytohormones present in much higher concentrations, like abscisic acid. One of the significant stress responses is the accumulation of cytokinin ribosides. It could indicate not only sequestration of the active form to inactive storage

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conjugates, but also stimulated transport from roots to shoots, probably in order to enhance sink and protect photosynthetic apparatus (Prerostova et al., 2020; Prerostova, Jarosova, et al., 2021). Nomoto et al. (2012) pointed out the possible link between the regulators of circadian clock and CKX5, which could be involved also in heat stress responses. Cytokinins are able to activate PIF4 under high temperatures by signalling via arabidopsis histidine kinase 3 (AHK3) receptor and type-B response regulators (ARR1 and ARR12), and they are involved in thermomorphogenesis (Černý et al., 2014; Di et al., 2016). Cytokinin response factor 6 (CRF6) is upregulated by heat stress, probably in the link with ROS signalling (Bielach et al., 2017). However, severe heat stress downregulates cytokinin signalling pathway (AHKs and ARRs) in leaves (Skalák et al., 2016) and it could be connected with lethal damage of leaves and starting senescence. The existence of functional cytokinin receptors on plasma membrane and membrane of endoplasmic reticulum (Hluska et al., 2021) leads to an idea that the receptors on endoplasmic reticulum could be specifically involved in stress responses. However, this hypothesis needs to be verified. The data indicate that cytokinins can enhance stress tolerance, especially when upregulated during the stress progression, and they are important in recovery after stress. However, cytokinin impact depends on developmental stage, tissue and stress severity. For example, cytokinin overaccumulation coinciding immediately with heat shock has negative impact on plants (Prerostova et al., 2020). Li, Euring, et al. (2021) highlighted that cytokinins protect flowering and seed production. It should be, however, taken into consideration that cytokinins upregulated in leaves delay seed maturation, because seed sink strength is rather low in comparison with vigorously growing leaves, which results in diminished transport and accumulation of nutrients into seeds (Sýkorová et al., 2008). Yang et al. (2016) showed necessity of the downregulation of zeatin riboside production in wheat kernels after heat stress treatment, and oppositely elevation of auxins, gibberellins and abscisic acid in order to accelerate seed production. This needs to be kept in mind in case of potential cytokinin application in the field.

4.7

Gibberellins

Gibberellins are isoprenoid phytohormones involved in vegetative growth, flowering induction, seed germination and fruit development (Hedden & Thomas, 2012). They were found to be involved in stress responses, especially in the connection with seed germination and seed development, which subsequently affects yield of crop plants. Gibberellins have a great potential in the increasing of tolerance and seed production under different stresses, including heat stress (AlonsoRamírez et al., 2009). However, as it was shown in the case of cytokinins, it strongly depends on the developmental stage. For example, Sobol et al. (2014) reported negative impact of gibberellins on flowering, causing earlier flower abortion during heat stress. It could be reversed by cytokinins. By contrast, the seed production

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requires cytokinin downregulation in leaves and increase of gibberellin content (Yang et al., 2016). It is obvious that the complex response to high temperatures is precisely regulated with respect to actual conditions. Biosynthesis of gibberellins takes place in chloroplast; then, the intermediate entkauren is transported to endoplasmic reticulum; and after oxidative conversions, the synthesis is finished in cytosol (Hedden & Thomas, 2012). Elevated temperatures stimulate synthesis of gibberellin-biosynthetic enzymes gibberellin oxidase GA20ox1 and GA3ox1 and downregulates the production of the catabolic enzyme GA2ox1. It is probably driven by PIF4 (Quint et al., 2016). It is obvious that gibberellins are tightly connected with endoplasmic reticulum, the organelle involved in heat stress responses, as well as with the MEP pathway in chloroplasts. However, the connection of, e.g. HSP proteins with gibberellin synthetic enzymes on endoplasmic reticulum, like ent-kauren oxidase (KAO) or GA13ox, is not known. Similarly, almost nothing is known about the targeting of heat-modified MEP pathway on the synthesis of gibberellins. Only the positive effect of isoprene on the expression of genes related to synthesis and signalling of gibberellins was described (Zuo et al., 2019). As gibberellin synthesis and metabolism is based on oxidative reactions by oxidases, it is a question if some conversions can be made also non-enzymatically using ROS produced by heat stress as a trigger (Keller et al., 2015). Gibberellin signalling pathway is suppressed by DELLA proteins, which block transcription of the gibberellin-inducible genes as well as transcription of PIFs under light conditions. It suggests similar regulation of PIF4 under heat stress. However, heat-induced PIF4 and high gibberellin levels degrade DELLA repressors, activating gibberellin signalling and the expression of gibberellin-responsive genes, leading to growth stimulation (Quint et al., 2016). PIF4 also binds to the promoter of FT gene, which is facilitated by H2A.Z nucleosomes, inducing flowering (Bahuguna & Jagadish, 2015). One of the gibberellin-inducible genes is MYB transcription factor. MYB activates the expression of many other genes and it is well known in the regulation of flowering (Bao et al., 2020). Under high temperatures, the expression of MYB factor is downregulated by miR159. The miR159 overexpressing lines with low levels of MYB are more sensitive to heat stress and they show delayed flowering and male sterility (Ding et al., 2020). Gibberellins were found to stimulate expression of ICS1 and NPR1, leading to increase of salicylic acid and its signalling, which can be associated with stress memory (Sharma et al., 2020). DELLA proteins downregulate the transcription of auxin signalling gene ARF6 and brassinosteroid signalling-related gene brassinazole-resistant 1 (BZR1). It means that heat-induced gibberellins enhance auxin and brassinosteroid signalling, and they together direct thermomorphogenesis (Quint et al., 2016).

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Brassinosteroids

Brassinosteroids are steroid hormones, which direct growth, development and stress responses of plants (Nolan et al., 2020). The role of brassinosteroids in heat stress is dual probably depending on the tissue. Increased temperatures lead to accumulation of brassinosteroid-responsive transcription factors BRI1-EMS-suppressor 1 (BES1) and BZR1 through the PIF4 signalling pathway involving auxin-stimulated synthesis of brassinosteroids (Ibañez et al., 2018). BZR1 is expressed also after repression of DELLA proteins (Quint et al., 2016). Interestingly, BZR1 can activate transcription of PIF4, which indicates positive regulatory loop. HSP90 was found to bind directly to BES1 and BZR1, stabilizing their structure and keeping them in the dephosphorylated (active) state. Moreover, HSP90.3 maintains the brassinosteroid repressor brassinosteroid insensitive 2 (BIN2), which phosphorylates BES1 and BZR1, in the dephosphorylated form. HSP90.1 and HSP90.3 actively transport BIN2 out of the nucleus (Shigeta et al., 2015). BES1 production can be enhanced by bZIP17 and bZIP28 transcription factors involved in the UPR response connected with endoplasmic reticulum (Che et al., 2010). By contrast, Martins et al. (2017) showed that warm temperatures can inhibit brassinosteroid signalling by degradation of the receptor brassinosteroid insensitive 1 (BRI1), which results in enhanced root growth. It seems that the brassinosteroid impact during stress is shoot/root-specific, because other studies showed that BRI1 receptor function was enhanced through structural stabilization by TWD1 (and so by HSP90) (di Donato & Geisler, 2019). Interestingly, TWD1 connects together auxin transport and brassinosteroid signalling. Exogenous application of 24-epibrassinolide increased tolerance of tomato plants to heat stress by enhanced net photosynthetic rate, stomatal conductance, maximal carboxylation rate of RUBISCO and maximal potential rate of electron transport, which contributed to ribulose-1,5-bisphosphate formation (Ogweno et al., 2008). In addition, antioxidant enzyme activity was induced, protecting cells from accumulated ROS. Brassinosteroids can upregulate H2O2 signalling through activation of RBOH (Zhou et al., 2014). Brassinosteroids activate via BZR1 one of the main regulators of development, hormonal cross-talk and stress responses, receptor-like protein kinase FER. In tomato, the connection between brassinosteroids and the heat stress responses was found only for FER2 and FER3 (Yin et al., 2018).

4.9

Strigolactones

Strigolactones belong to recently discovered phytohormones. They have been shown to regulate responses to different abiotic stresses (Kramna et al., 2019).

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Despite the fact that their roles in cold stress responses have been intensively studied, their involvement in heat stress response is almost unknown. In contrast, strigolactone-related compounds karrikins were found associated with high temperature responses. They are active after exposure of plant seeds to smoke and burning of plant material, stimulating germination (De Cuyper et al., 2017). However, their role was mostly studied in relation to seed germination and burning than the heat stress itself. The synthesis of strigolactones was found to be enhanced by increased temperature, probably mediated by ABA (Wang et al., 2013). Strigolactones can probably alleviate physiological changes caused by high temperature. Exogenous application of synthetic strigolactone analogue GR24 mitigated stress-induced inhibition of leaf and root growth in grass Festuca arundinacea, supported cell division and operated oppositely in comparison with auxin (Hu et al., 2018, 2019). Similarly, Omoarelojie et al. (2020) highlighted positive role of strigolactones in high temperatures during seed germination and seedling development. Nevertheless, the authors pointed out the independence of signalling on D14 protein. Moreover, all above-mentioned studies used racemic mixture of synthetic GR24, which has been found to influence both strigol and karrikin pathways (Kramna et al., 2019). The absence of the involvement of D14 protein indicates that the heat tolerance effects are probably activated through karrikin pathway. However, this theory has to be studied in detail using transgenic lines, correct enantiomers of GR24 and tracking strigolactone signalling components.

5 Conclusion This chapter provides a survey of the interactions between heat sensors and plant hormones during warm temperatures and severe heat stress. The heat stress responses are tightly connected with light signalling (PIF4), oxidative stress response (ROS, H2O2) and water deficiency (abscisic acid, HSPs). Phytohormones, as the main regulators of plant growth and development, play key roles in stress response amplification, stress tolerance, thermomorphogenesis and senescence. They react on heat stress sensors, but they are also able to support the sensor production in feedback loops. Upon high temperatures, all main phytohormones can have a protective role and are able to work in synergistic relationship. In the case of ethylene and cytokinins, the results indicate the importance of their ratio with other hormones, especially abscisic acid. The actual effect of phytohormones is dependent on the temperature level, stress duration and developmental stage of a plant. The cross-talk of phytohormones under warm temperatures in leaves is shown in Fig. 8.1. These interactions seem to be important for heat tolerance. As Isono et al. (2021) showed, the opportunity to reverse the lethal progression of severe heat stress could lie in the finetuning of the signalling network approaching warmth signalling network.

Fig. 8.1 The known molecular mechanisms of intensive cross-talk among phytohormones during the responses to high temperatures in plant leaves are visualized in the scheme. High temperature stimulates synthesis of PIF4 (PHYTOCHROME INTERACTING FACTOR 4), the key regulator of heat stress responses, which expression can be regulated by phytohormones. Heat itself affects activities of MBF1c transcription factor and protein phosphatase PP2C.D, chromatin modulation through histones modification (H2A.Z), stimulates production of microRNAs, causes damage of chloroplasts and mitochondria leading to

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production of reactive oxygen species (ROS) and increases hydrogen peroxide (H2O2) levels in cytosol through activation of RBOHD (RESPIRATORY BURST OXIDASE HOMOLOG D). High temperatures induce synthesis of plant hormone jasmonic acid (JA) by LOX (LIPOXYGENASEs), upregulating also the level of precursor diacylglycerol (DAG). The production of volatile methyl jasmonate (MeJA) can radically influence long-distance signalling. JA signalling [COI1 (CORONATINE INSENSITIVE 1), JAZ (JASMONATE-ZIM DOMAIN PROTEIN)] can be affected by other hormones and influences salicylic acid (SA) signalling by WRKY transcription factors. SA synthesis through ICS1 (ISOCHORISMATE SYNTHASE 1) can be directed by heat stress or indirectly activated by gibberellins (GA). GA stimulates also SA signalling (upregulating NPR1 transcription activator and TGA transcription factor). GA-signalling repressors DELLA play key regulatory role in thermomorphogenesis regulating signals of auxins (IAA, indole-3-acetic acid) and brassinosteroids (BR) through ARF6 (AUXIN RESPONSE FACTOR) and BZR1 (BRASSINAZOLE-RESISTANT 1) transcription factors. GA synthesis and degradation are regulated by PIF4 [GA oxidases and KAO (ENT-KAUREN OXIDASE)], and high temperature itself can modulate content of GA precursors by MEP (methyl erythritol 4-phosphate) and MVA (mevalonate) pathways. Both pathways are important for synthesis of other heat-inducible molecules like isoprene, MEcPP (methyl erythritol cyclodiphosphate), abscisic acid (ABA) and cytokinins [CK; including tZ (trans-zeatin), iP (isopentenyladenine) and cZ (cis-zeatin)]. Diverse effect of heat stress on cZ and tZ with iP might be important in stress responses. CK signalling through receptor AHK3 and transcription factors ARR (RESPONSE REGULATOR) and CRF6 (CYTOKININ RESPONSE FACTOR 6) preserves chloroplast function as well as supports sugar production and starch accumulation. Sugar production by starch degradation [enzymes INV (INVERTASE) and SUS (SUCROSE SYNTHASE)] and sugar transport (SUT, SUCROSE TRANSPORTER) are enhanced by ABA. ABA concentrates signalling of other phytohormones as well as heat–stress signals, like ROS, upregulation of HSF (HEAT-SHOCK FACTORs) and HSP (HEAT-SHOCK PROTEINs). ABA blocks expression of BR transcription factor BES1 and ethylene (ET) transcription factors ERFs. ABA signalling through transcription factors ABI affects also ET biosynthesis [ACS, AMINOCYCLOPROPANE-1CARBOXYLIC ACID (ACC) SYNTHASE]. Balance of ET, ABA and PIF4 signalling pathways is important for the expression of ORE1 (ORESA 1), a transcription factor inducing cell death. HSP can make a complex with co-chaperone RAR1 and its interactor SGT1 and they can stabilize COI1 and auxin receptor TIR1, which enhances JA and auxin signalling, respectively. IAA synthesis [YUC8 (YUCCA 8), TAA1 (TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1), CYP79B2 (CYTOCHROME P450)], deactivation [GH3 (GRETCHEN HAGEN 3), UGT76F1 (UDP-GLYCOSYLTRANSFERASE 76F1)], transport [PIN1 (PIN-FORMED 1), PILS6 (PIN-LIKES 6), TWD1 (TWISTED DWARF 1)] and signalling (ARFs, Aux/IAA (AUXIN/INDOLE-3ACETIC ACID)] are modulated directly by high temperatures or indirectly by PIF4, microRNAs and histone modifications. PIF4 upregulates expression of SAUR (SMALL AUXIN UP RNA), which interacts with auxin and induces H+-ATPase on plasma membrane, leading to cell growth stimulation. Hypothetical connections (dotted lines) and question marks indicate described influence of molecules with ambiguity of the precise functional mechanisms. Dashed lines point out multistep pathways containing several enzymes and intermediates, which might be potentially affected by heat stress. These interactions seem to be important for heat tolerance of plants (created with BioRender.com)

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The heat tolerance can be successfully modulated by heat acclimation or other pre-treatments. Plants exhibit stress memory, which includes methylation of histones, glucose and H2O2 signalling, accumulation of sHSP, abscisic acid-induced synthesis of protective compounds and accumulation of proline caused by salicylic acid. Recovery after stress is connected with cytokinins (trans-zeatin and isopentenyladenine), ethylene (through EIN3 signalling) and MeJA, but the other phytohormones may be important for growth restoration. Moreover, the importance of roots as well as the protection of meristematic tissues in the heat stress responses should be taken into account. With the increasing global temperature, it is highly important to extend the spectrum of crops and introduce more tolerant species. Targeted breeding, genetic modifications and application of growth regulators should utilize the knowledge of complex cross-talk because the positive impact in one developmental stage (e.g. in vegetative stage) can negatively affect the other one (e.g. flowering or seed production). The usage of the tissue-specific or developmental stage-specific promoters has great potential in fine regulation of the stress responses. Acknowledgements Research in the authors’ laboratory is supported by funding from the Ministry of Education, Youth and Sports of CR: Inter-Excellence project No. LTAUSA17081 and from European Regional Development Fund-Project “Centre for Experimental Plant Biology,” grant number CZ.02.1.01/0.0/0.0/16_019/0000738 and by the Czech Science Foundation, grant number 20-22875S.

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Chapter 9

Phytohormones and Cold Stress Tolerance Joanna Lado, Florencia Rey, and Matías Manzi

1 Introduction Abiotic stress is an important constraint for food production in temperate regions such as Latin-America, Africa, and Northern and Central Europe (Ray et al., 2012). Still, low temperatures can be experienced at night even in tropical countries, particularly if crops are cultivated at high altitudes. The extension of tropical and subtropical crops to other regions, favored by global climatic changes, represents an additional challenge for cold stress adaptation. Due to global warming, ecologists revealed a paradoxical connection between plant growth and climatic changes, confirming an upsurge of cold injury in warmer regions (Hassan et al., 2021). The rise in temperatures results in extended growing periods and delays cold hardening process during fall, fastening de-hardening in spring, and increasing the risk of damage due to early or late frosts (Ramirez & Poppenberger, 2020; Zhang, Zhao, et al., 2021). Persistent extreme cold temperatures have been registered during the past decade in different agricultural regions, varying in frequency, duration, and intensity (Hassan et al., 2021). These conditions cause an inhibition of photosynthesis and growth with its inherently negative impact on crop yield (Raza et al., 2021). Cold stress causes a delayed emergence and poor stand of different crops, culminating in stunted growth, leaf chlorosis, lower root-shoot surface area, flower

J. Lado (*) Instituto Nacional de Investigación Agropecuaria (INIA), Salto, Uruguay e-mail: [email protected] F. Rey Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC), Valencia, Spain M. Manzi Fertilidad de Suelos, Estación Experimental Facultad de Agronomía Salto (EEFAS), Facultad de Agronomía, Universidad de la República, Salto, Uruguay © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_9

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Fig. 9.1 Schematic representation of hormones signaling through transcriptional regulation and main physiological changes in response to cold stress. ABI5 ABA-INSENSITIVE 5, ARF Auxin response factors, AuxRE auxin response DNA elements, BES1 BRI1-EMS-suppressor 1, BZR1 BRASSINOSTEROLE-RESISTANT; CBFs, consecutive triple response1, D14 α/β hydrolases DWARF14, EIN ethylene insensitive, ERFs ethylene response factors, ICE inducer of CBF expression, MAX2 MORE AXILLARY GROWTH 2, JAZ JASMONATE ZIM-DOMAIN

shedding, infertility, incomplete/poor fruit setting, and disturbed water-nutrient relations, which has a negative impact on crop yield and quality (Hassan et al., 2021). For some crops, chilling events determine important losses such as in rice, where chilling injury during the reproductive stage causes yield reductions of 0.68–3.0 ton/ha in Australia and California, respectively (Zhang, Zhao, et al., 2021). Plants face temperature changes activating tightly coordinated mechanisms that involve changes at different developmental stages, physiological and biochemical processes, transcriptional regulation, and modifications in key metabolites and proteins. The role of phytohormones in these responses is crucial, and new approaches revealed new clues and roles towards plant cold adaptation. Cold-tolerance mechanisms are usually characterized by an accumulation of soluble solids, signaling molecules, and transcriptional changes, all governed by internal signals (Hassan et al., 2021; Raza et al., 2021). This chapter highlights recent knowledge on hormonal roles and their interaction towards cold stress adaptation and survival (Fig. 9.1). Cold stress is associated with

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low temperatures (usually below 10 °C but non-freezing) (Gusta et al., 2005; Zhou et al., 2011). These processes are mostly governed by a cross-regulation among “stress-related” phytohormones: jasmonic acid (JA), abscisic acid (ABA), and ethylene (ET). In addition, cold responses also involve other phytohormones such as brassinosteroids (BRs), strigolactones (SLs), auxins (AUXs), and gibberellins (GAs), among signaling molecules (Hassan et al., 2021; Peleg & Blumwald, 2011; Raza et al., 2021; Shi et al., 2015).

2 New Players: SLs and BRs Role in Cold Tolerance SLs and BRs contribution to plant stress adaptation has been explored in recent years, revealing a positive role towards plant survival under chilling stress and a possible hub for integrating plant responses in different organs reducing crop yield trade-off (Ahammed et al., 2020; Bhoi et al., 2021; Ramirez & Poppenberger, 2020). SLs are sesquiterpene metabolites derived from carotenoids, mostly β-carotene catabolism, which display emerging roles in plant stress adaptation (Bhoi et al., 2021). A contribution of SLs to plant adaptation to a combination of dark and chilling was proposed recently in pea and Arabidopsis seedlings under cold stress (Cooper et al., 2018). SLs were described to promote stomatal closure by stimulating production of hydrogen peroxide (H2O2) and nitric oxide, being both metabolites related to SL signaling under adverse conditions (Lv et al., 2018). In addition, SL signaling may contribute to plant adaptation to low temperature environment by regulating leaf growth (Figs. 9.1 and 9.2). A reduction in leaf area has been observed following dark and chilling treatment in the presence of GR24, a synthetic SL (Cooper et al., 2018).

Fig. 9.2 Stimulation or repression of key physiological processes mediated mostly by SLs and BRs in response to cold stress in different plant organs (canopy and roots)

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Recently, SLs applied exogenously to mungbean (Vigna radiata L.) promoted cold (7 ± 2 °C) tolerance via enhancing superoxide dismutase (SOD)-scavenging and soluble sugars content, reducing malondialdehyde (MDA) and H2O2 accumulation, and inducing lipoxygenase (LOX), phenylalanine ammonia lyase (PAL), and tyrosine ammonia lyase (TAL) activities under cold exposure (Omoarelojie et al., 2021). Cold stress rapidly (6 h at 4 °C) induces solanacol biosynthesis in the roots of tomato, favored by an induction of CCD7, CCD8, and MAX1 genes involved in SL biosynthesis (Chi et al., 2021). Moreover, exogenous application of GR24 enhanced cold-induced expression changes in C-REPEAT BINDING FACTOR 1 (CBF1) gene in tomato together with stimulating antioxidant system responses and reducing the presence of H2O2 (Chi et al., 2021) (Fig. 9.1). Similarly, SLs analogue application in Brassica rapa under cold stress substantially favored cold survival through maintaining photosynthesis and cell viability, increasing soluble protein and proline content, inhibiting the production of ROS and favoring expression of cold-related genes such as MAPKs, NADPH oxidase or antioxidant enzymes (Zhang et al., 2020). SL sensing was recently explored and is linked to an F-box (MAX2/D3/ RMS4) and α/β-hydrolase (D14/AtD14/DAD2) proteins (Fig. 9.1). SLs are sensed by the α/β-fold hydrolase that further delivers the signal to a leucine (Leu)-richrepeat F-box protein (MAX2 in Arabidopsis; D3 in Oryza sativa (Bhoi et al., 2021). BRs are steroid phytohormones that have been also studied as possible players in favoring plant cold tolerance (Krishna et al., 2017; Ramirez & Poppenberger, 2020). Arabidopsis seedlings overproducing BRs enhanced cold tolerance through stimulation of certain cold-regulated genes (COR), triggering the expression of stress-related genes, mantaining photosynthetic activity, antioxidant enzymes, accumulation of osmoprotectants, and inducing other hormonal changes (Divi & Krishna, 2010). It was recently described in Arabidopsis that BRS1 (brassinosteroid-insensitive 1 suppressor 1), a serine carboxypeptidase that mediates BRs signaling, has a role in enhancing cold stress response through CBF1, CBF2, and CBF3 (Fig. 9.1) and other cold-related genes such as RD29A, COR413, and KIN2 (Zhang, Ming, et al., 2021). A direct role of this protein in improving redox homeostasis and reducing oxidative stress was recently demonstrated (Zhang, Guo, et al., 2021). Exposure of tomato plants to cold stress favors BR synthesis and the accumulation of BRASSINAZOLE-RESISTANT1 (BZR1), which stimulates the expression of CBF1, CBF3, and RESPIRATORY BURST OXIDASE HOMOLOG 1 (RBOH1) genes by binding directly to their promoter, which finally favors cold tolerance by influencing glutathione homeostasis (Fang et al., 2021). Authors demonstrated that crosstalk between BZR1 and ROS mediates cold- and BR-activated CBF expression, leading to cold tolerance in tomato. BRs enhance chilling tolerance of crops when applied exogenously (Dou et al., 2021; Ramirez & Poppenberger, 2020). BRs provoke/trigger transcriptional changes of the CBF-dependent and independent way through BZR1 and WRKY6 transcription factors (TFs) mediation (Li et al., 2017), finally mitigating cold-induced oxidative stress through the activation of the cellular antioxidant systems (Sun et al., 2020; Zhang et al., 2020). Studies carried out in Brassica rapa revealed that several BZRs could be involved in the activation of CBF-mediated cold response (Fig. 9.1), being

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also upregulated in response to exogenous ABA (Saha et al., 2015), suggesting a complex interplay between phytohormones. In cotton seedlings, application of 24-Epibrassinolide (EBR), a BR analog, reduced MDA content and electrolyte leakage, and downregulated transcriptional changes associated with ABA (PYL and PP2C) and ET (ETR, EIN and ERFs) signaling (Dou et al., 2021). Authors suggest that it should be also involved the biosynthesis of key metabolites, especially gossypol and glutathione as both are related to cold tolerance in cotton. In citrus rootstocks, BR signaling appears to play a dominant role in cold perception and transduction, triggering dephosphorylation and activation of BZR1 homolog protein (Cs2g09750) which was upregulated upon cold stress (Peng et al., 2021). It has been also described that exogenous application of BRs improves CO2 assimilation, alleviating photoinhibition and favoring the recovery of the photosynthetic apparatus mediated by the action of the ascorbic acid (AsA)-glutathione cycle and redox homeostasis (Chen et al., 2019). Transcriptome data revealed that BRs increase the expression of genes related to chlorophyll biosynthesis and photosynthesis (Zhao et al., 2019), revealing a relevant role of these phytohormones in photosynthesis maintenance through photoprotection under cold stress (Fig. 9.2). Other possible function of BRs relies on improving cell membrane fluidity during cold stress, highlighted while studying BR-deficient barley mutants (Sadura et al., 2021). Membranes are proposed to function as thermal sensors, being the primary cause of other physiological changes within cells and tissues. Alteration in membrane fluidity during cold stress is connected with changes in unsaturated fatty acids and phospholipids, affecting membrane properties (Sadura et al., 2021). A different fatty acid membrane composition in BR-deficient mutants resulted in altered membrane properties and a more rigid chloroplast membrane upon cold stress compared to wild-type barley plants (Sadura et al., 2021). In this line, exogenous application of EBR (0.3 μM) reduced membrane lipid peroxidation by activating the antioxidant system in grapevine, favoring cold tolerance (Xi et al., 2013). The former suggests a possible role of BRs in regulating/interacting in cell and chloroplast membrane responses to cold. Membrane fluidity maintenance properties were also demonstrated in detached fruit, where post-harvest chilling injury was ameliorated in mango (Li et al., 2012), tomato (Aghdam & Mohammadkhani, 2014), orange (Habibi et al., 2021), and eggplant (Gao et al., 2015) after BRs analog application at 6–10 μM concentration. This protection was linked to an increased unsaturation of the fatty acids in the plasma membrane, a reduced phase transition temperature and a lower phospholipase D (PLD) and LOX activities, providing evidence that BR plays an important role in regulating cold stress tolerance even in detached fruit (Aghdam & Mohammadkhani, 2014; Gao et al., 2015; Habibi et al., 2021; Li et al., 2012). A reduction in the activity of browning-related enzymes such as polyphenol oxidase (PPO) or PAL and peroxidase (POD) in eggplant after EBR treatment was behind the browning and chilling damage control by BRs during eggplant storage (Gao et al., 2015). Similarly, in cold-sensitive banana fruit, exogenous application of EBR reduced the MDA content and electrolyte leakage but increased total soluble solids and

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chlorophyll fluorescence, reducing chilling injury during post-harvest cold storage (Li, de Ollas, & Dodd, 2018). Energy biosynthesis, stress response, and cell wall modification processes were up-regulated in response to EBR treatment (40 μM), whereas protein degradation and energy consumption were down-regulated. These results suggest that EBR treatment favors defense while maintaining a desired energy status in banana (Li, de Ollas, & Dodd, 2018). Similarly, in table grape, BRs application (1.5 ppm) provided an enhanced tolerance to chilling injury disorder during post-harvest storage (Pakkish et al., 2019) and in blood oranges, application of a BRs analog (10 μM) reduced chilling injury symptoms together with an increment in sugars, polyphenols, mainly anthocyanins and therefore antioxidant capacity of the pulp tissue (Habibi et al., 2021). It is worth mentioning that much higher BR analog concentration is needed in detached fruit (6–40 μM) than in other plant organs (0.3–1.0 μM) in order to prevent cold damage (Ahammed et al., 2020).

3 Key Function of Old Players ABA and JA in Cold Tolerance ABA is one of the main phytohormones involved in the acclimation and tolerance to cold stress in plants including seeds and above- and below-ground tissues (Pan et al., 2021). ABA is essential to prevent seed germination and vegetative tissues sprouting such as buds and rhizomes during the adverse cold season, but also in the promotion of organ senescence, which finally results in a pre-acclimation period needed to reach cold tolerance (Caselles et al., 2021). Furthermore, ABA can be transported via phloem from stress-sensing and high ABA-accumulating organs such as leaves to other organs such as roots and rhizomes, where ABA finally acts as a signaling molecule (Caselles et al., 2021; Li, Yun, et al., 2018; Manzi et al., 2015). JA as well as other jasmonate-related compounds have been linked to cold tolerance and alleviation of chilling damage in several plant species (Hu et al., 2017). Low-temperature induces JA biosynthetic genes favoring its accumulation (Hu et al., 2013), while JA-defective Arabidopsis mutants showed a higher cold damage (Hu et al., 2013). Evidence of the effect of exogenous JA and methyljasmonate (MJ) confirms that there is a stimulation of the antioxidant system and ROS scavenging ability (SOD, CAT, POD, GSH, and AsA antioxidants accumulation) on a great diversity of crops. Thus, jasmonates restrict oxidative damage and help to maintain the integrity of cell membrane and organelles (Mustafa et al., 2018; Rodrigues et al., 2020; Wang, Jiang, et al., 2021). It is worth noting that the response to the JA exogenous treatment is suggested to be dose-dependent, with low concentrations (0.01–0.1 μM) inducing a desired and protective effect but higher concentrations (10–100 μM) can promote lipid peroxidation and consequently, chilling damage (Kamińska et al., 2018; Rodrigues et al., 2020). However, these or even higher concentrations (500–2000 μM) may induce tolerance to drought or salt

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stresses in other plant species, suggesting a species-specific and dose-dependent response to JA towards different stress conditions (Rodrigues et al., 2020). ABA and JA play a crucial role individually in triggering responses to cold stress, but they act also co-ordinately by precisely modulating these changes. It was recently demonstrated in apple that the APETALA2/ET responsive factor (AP2/ERF) family protein MdABI4 mediates in the ABA response to low temperatures by upregulating the INDUCER OF CBF EXPRESSION 1 (ICE1) MdICE1, which codifies for a key regulatory protein involved in the cold stress response. On plants subjected to low temperatures MdICE1 regulates downstream target gene MdCBF1 (An, Wang, et al., 2021). To do this, a B-box (BBX) protein MdBBX37, a class of zinc-finger TFs, bounds to the MdICE1 and also the MdICE4 promoters to activate their transcription (An, Wang, et al., 2021). Conversely, MdABI4 protein is negatively modulated by the jasmonate-ZIM domain (JAZ) proteins MdJAZ1 and MdJAZ2, by interfering with the interaction between the MdABI4 and MdICE1 proteins (An, Xu, et al., 2021). Therefore, the MdABI4 is a key protein integrating the ABA and JA signals to display the low-temperature tolerance (An, Xu, et al., 2021). In addition, it was demonstrated that JAZ physically interact with ABI3 and ABI5 under normal growth conditions but once that JA increases after stress exposure, JAZ proteins are degraded to allow ABI3 and ABI5 to activate the ABA response (Pan et al., 2020). In the same line, how JA signaling could regulate cold stress adaptation was explored. JAZ repressors (JAZ1 and JAZ4) have been described as possible regulators which directly bound and suppress transcription of ICE1 and ICE2, avoiding cold stress responses (Hu et al., 2013). JA levels are induced by cold, stimulating COI1-mediated degradation of JAZs, which further release ICEs from repression and favor CBF-mediated responses (Hu et al., 2013; extensively reviewed in Kamińska et al., 2018; Fig. 9.1). Whereas JAZ1 and JAZ4 acts as signaling repressors of cold tolerance, MYC2, a master regulator of JA signaling, positively regulates cold tolerance by forming a complex with ICE1 as has been reported in banana (An, Wang, et al., 2021). In this mechanism, a B-box protein MdBBX37 forms a JAZ-BBX37-ICE1-CBF regulatory cascade which finally improves plant cold tolerance mediated by JA (An, Wang, et al., 2021). It was also demonstrated that MYC2 could induce the expression of ADC1, which codifies to the major putrescine biosynthetic gene. This polyamine is accumulated during the exposure to low temperatures and could alleviate cold damage in plants (Ding et al., 2021). Some of the BBX proteins (SlBBX7, SlBBX9, and SlBBX20) were demonstrated to be involved in the response of tomato to cold stress. In SlBBX7, SlBBX9, and SlBBX20-silenced plants, low temperatures caused an increase in the photoinhibition of PSI and PSII photosystems, suggesting that those proteins integrate both cold and light signaling processes (Bu et al., 2021). In this sense, light and cold stress appears to work dependently during leaf senescence. In light of recent evidence, it was proposed that the JAZ-ABI4-ICE1-CBF signaling cascade integrates the ABA- and JA-signaling pathways. In the presence of ABA, ABI4 interacts with ICE1 which results in an upregulation of the expression of CBF1, and thus, in a final promotion of cold tolerance. ABA could also act

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co-operatively by degrading the JAZ proteins. However, under low-ABA availability, JAZ proteins are bound to the ABI4 protein, avoiding the interaction between ABI4 and ICE1, and restricting cold tolerance response (An, Xu, et al., 2021). It was previously reported that the expression of OsJAZ1 is strongly upregulated by exogenous JA in rice, but only shows moderate or delayed changes after ABA or cold treatment (Fu et al., 2017).

4 ET: A Well-Known Stress-Responsive Player ET is a gaseous plant hormone that participates in diverse physiological processes and has been associated to plant’s tolerance to different biotic and abiotic stresses. Although an increase in ET endougenous levels is a common response of plants to cold stress, ET implication in the regulation of cold or freezing tolerance is not clear and studies have shed contradictory results, with a positive or negative role appearing to be dependent on the species, and also on growing conditions or plant tissue. A negative effect of ET on cold tolerance has been observed in Arabidopsis seedlings grown in vitro, in which treatments with the ET precursor 1-aminocyclopropane-1-carboxylic acid (ACC) showed a reduced freezing tolerance, whereas the application of an inhibitor of ACC biosynthesis, aminoethoxyvinylglycine (AVG), increased the freezing tolerance of these plants (Shi et al., 2012). Moreover, these authors found an enhanced freezing tolerance in the ET insensitive mutans etr1-1, ein4-1, ein2-5, and ein3-1, and a hypersensitive phenotype in mutants overexpressing the gene EIN3, reinforcing the notion that ET plays a negative role in cold tolerance. Similar results have been obtained in other species, such as the legume Medicago truncatula, in which plants grown in vitro and treated with the ET releaser ethephon or ACC were hypersenstive to freezing, while the application of AVG improved it (Zhao et al., 2014). In addition, an ET-insensitive mutant of Medicago truncatula, Mtskl1 (orthologue of AtEIN2), was more tolerant to cold in comparison to their wild-type plants, further supporting the negative effect of ET in the cold tolerance of this species (Zhao et al., 2014). Although the direct effect of ET was not assessed, a higher expression of ET-related genes, specifically ACC oxidase (ACO) and ethylene-responsive transcription factor (ERF), was found in roots of a cold-senstive rice genotype in comparison to the cold tolerant one, suggesting ET levels may have a negative effect in the tolerance of rice roots to cold (Rativa et al., 2020). By contrast, evidence supporting a positive role of ET in the regulation of cold tolerance has been obtained in Arabidopsis and other plant species. Catalá et al. (2014) found a positive effect of ET in conferring cold tolerance in Arabidopsis plants, as the application of ACC to soil-grown seedlings enhanced freezing tolerance, and a similar effect was detected in Arabidopsis mutant plants overproducing ET (eto-1 overexpressing line) (Catalá & Salinas, 2015). Similarly, other authors detected a decreased tolerance to cold in Arabidopsis mutant plants that are impaired

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in perceiving and transducing the ET signal (ET-insensitive mutans etr1-1 and ein21) (Popov et al., 2019; Sin’kevich et al., 2020). These mutant plants proved to be very sensitive to freezing, and although cold acclimatation was capable of improving their tolerance, stress damage was still higher than in wild-type plants (Sin’kevich et al., 2020). Interestingly, the decrease in freezing tolerance in the etr1-1 and ein2-1 mutants was associated to a lower activity of antioxidant enzymes SOD and catalase (CAT), suggesting ET improvement of cold-tolerance is linked to a more efficient capacity to scavenge reactive oxygen species (ROS). These results in Arabidopsis contradict the negative effect of ET on cold-tolerance described by Shi et al. (2012) and suggest that growing environment can also influence the effect of ET on cold tolerance. In line with this, a negative effect was found in Arabidopsis seedlings cultured in vitro (Shi et al., 2012), whereas a positive effect was detected in soilgrown seedlings (Catalá et al., 2014; Sin’kevich et al., 2020). Similarly, in contrast to what was detected by Rativa et al. (2020) in rice roots, a positive relationship between ET and cold tolerance was proposed in rice leaves, related to the expression of the ET receptor gene OsETR4 (Jiang et al., 2020). Rice seedlings overexpressing OsETR4 showed higher cold tolerance than wild-type plants, which was linked to a differential expression of genes involved in ET biosynthesis and signaling, and also of kinases involved in protein phosphorilation (Jiang et al., 2020). Furthermore, a positive effect of ET on cold tolerance has been detected in grape (Sun et al., 2016; Sun, Zhang, et al., 2019; Sun, Zhu, et al., 2019), trifoliata orange (Wang et al., 2019; Zhang, Zhao, et al., 2021), apple (Han et al., 2020; Han et al., 2021; Wang, Liu, et al., 2021), bermudagrass (Hu et al., 2020), tomato, and tobacco (Zhang et al., 2009; Zhang & Huang, 2010), related to the expression of specific ERF genes, whose expression seems dependent on ET synthesis. ERF genes belong to the APETALA2/ERF (AP2/ERF) superfamily of TFs, which participate in the transduction of stress signals by modulating the expression of downstream target genes, and have been implicated in the response to abiotic stress, including cold stress (Hu et al., 2020) (Fig. 9.1). In grape, a positive effect of ET on cold tolerance has been reported as application of ACC to whole plants of two grape cultivars with differrent cold tolerance, coldhardy Vitis amurensis and cold-sensitive Vitis vinifera, increased their freezing tolerance, whereas treatment with AVG-reduced ET production during cold exposure and increased cold sensitivity (Sun et al., 2016). Moreover, the analysis of the expression patterns of different ERF genes that were significantly up-regulated by cold stress (VvERF057, VaERF057, VaERF080, VaERF087, and VaERF092) revealed that the application of ACC induced their expression, while treatment with AVG inhibited the induction by cold detected in these genes, indicating that ET is essential for their induction under cold stress conditions (Sun et al., 2016; Sun, Zhang, et al., 2019; Sun, Zhu, et al., 2019). Furthermore, the independent overexpression of these TFs in transgenic Arabidopsis lines led to an enhanced cold tolerance and survival rate in comparison to wild-type plants. Transgenic plants showed lower signs of lipid peroxidation (MDA levels) and higher activity of antioxidant enzymes, such as SOD, CAT, and POD, suggesting that the increase in cold tolerance was, at least in part, associated to a higher capacity to eliminate

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ROS and preventing damage to cellular membranes and components (Sun et al., 2016; Sun, Zhang, et al., 2019; Sun, Zhu, et al., 2019). ET also plays a positive role in the cold tolerance of the cold-hardy species Poncirus trifoliata (trifoliate orange), which has also been linked to the activation of different ERF genes and the ability to maintain ROS homeostasis (Wang et al., 2019; Zhang, Zhao, et al., 2021). Under cold exposure, freezing tolerance was higher in trifoliate seedlings treated with ACC than in AVG-treated seedlings, which exhibited more severe damage and higher signs of oxidative stress (Zhang, Zhao, et al., 2021). Moreover, two ERF genes were identified in this species that were significantly induced by cold and whose up-regulation was also dependent on ET synthesis: PtrERF9 and PtrERF109 (Wang et al., 2019; Zhang, Zhao, et al., 2021). Expression of PtrERF9 was induced by the exogenous application of the ET precursor ACC and, on the other hand, the application of AVG was capable of repressing its induction by cold (Zhang, Zhao, et al., 2021), whereas PtrERF109 was up-regulated by the application of ethephon (ET releaser) (Wang et al., 2019). The role of these ERF genes as positive regulators of cold tolerance was further corroborated by silencing PtrERF9 and PtrERF109, which resulted in an increase in their cold sensitivity (Wang et al., 2019; Zhang, Zhao, et al., 2021). Furthermore, the overexpression of these ERF genes in transgenic lines of tobacco and lemon, which is a very cold-sensitive Citrus species, proved to be effective in improving their cold tolerance (Zhang, Zhao, et al., 2021). Similar results were obtained in Cynodon dactylon bermudagrass, where the CdERF1 gene is up-regulated by cold and by the application of ACC, and its overexpression in Arabidopsis mutant plants confers enhanced cold tolerance (Hu et al., 2020). Interestingly, genes involved in the synthesis of antioxidant enzymes were identified among the downstream target genes of these two ERF, suggesting that the positive role of these TFs in cold tolerance is associated to the modulation of ROS homeostasis. In particular, PtrERF9 was found to interact with the promoter of PtrGSTU17 (Zhang, Zhao, et al., 2021), a gene encoding the enzyme gluthatione S-tranferase (GST), whereas PtrERF109 targets the POD encoding gene PtrPrx1 (Wang et al., 2019). In both tobacco and lemon lines overexpressing PtrERF9 and PtrERF109, a higher GST and POD activity, respectively, and lower accumulation of ROS and oxidative stress sensitivity was detected, while the opposite effect was observed in Poncirus trifoliata plants in which these ERF genes were silenced. Additionally, Zhang, Guo, et al. (2021) found that PtrERF9 is also able to bind with the promoter of ACC synthase1 (PtrACS1), positively regulating its expression and, therefore, ET production. This was corrobotated in plants in which PtrERF9 was silenced, as a decreased in the expression of PtrACS1, ACS activity and ACC content, was detected. These results indicated an ET regulation feedback underlying the coldstress response, in which ET modulates the expression of PtrERF9 and, in turns, PtrERF9 regulates ET biosynthesis by interacting with the promoter of PtrACS1. Exposure to cold of seedlings of Malus domestica apple induced the production of ET and the expression of MdERF1B TFs (Wang, Liu, et al., 2021). MdERF1B proved to positively regulate cold tolerance, as overexpression of MdERF1B in apple and Arabidopsis seedlings enhanced their freezing tolerance. Interestingly, and

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similarly to what was detected with the PtrERF9 in trifoliate orange (Zhang, Zhao, et al., 2021), MdERF1B is capable of interacting with the promoters of two genes involved in ET biosynthesis, MdACO1 and MdERF3, positively regulating ET production. In addition, two ERF genes have been identified in the low-temperature resistant Malus bacatta apple: MbERF11 and MbERF12. MbERF11 and MbERF12 were up-regulated by cold and other abiotic stresses in leaves and roots of soil-grown seedlings, and its stress-induction seemed to be dependent on ET biosynthesis in both tissues (Han et al., 2020; Han et al., 2021). Morevoer, overexpression of MbERF11 in transgenic Arabidopsis enhanced its cold tolerance, associated to an increase in SOD, CAT, and POD activities and the capacity to eliminate ROS (Han et al., 2020; Han et al., 2021). In some plant species, it has been suggested that the regulation of the cold stress response by ET is, at least partially, through the transcriptional control of coldregulated CBFs (Fig. 9.1). In line with this, in the ET-overproducing Arabidopsis plants eto1-3, higher accumulation of CBF1-3 transcripts was detected, which explains the tolerant phenotype of these mutants (Catalá & Salinas, 2015). Although Shi et al. (2012) reported the opposite effect of ET on cold tolerance, the tolerant phenotype found in the double mutant ein3 eil1 was also associated to a higher expression of CBF1-3 and downstream CBF target genes such as COR genes. These authors found that EIN3 negatively regulates the expression of CBFs genes by binding to their promoters. An up-regulation of CBF1 and 2 and downstream genes such as COR15A and COR47, was detected in grape and Arabidopsis plants overexpressing the ERF genes, which were tolerant to cold conditions (Sun et al., 2016; Sun, Zhang, et al., 2019; Sun, Zhu, et al., 2019). Similarly, the cold tolerance of Arabidopsis plants overexpressing CdERF1 was also associated to an activation of stress-related genes such as CBF2 (Hu et al., 2020), and it has been indicated that the gene MdERF1B upregulates the expression of the cold-responsive gene MdCBF1 in apple seedlings (Wang, Liu, et al., 2021). All these results support that the relevance of ET in plants response to low temperature is by mediating the CBF-dependent signaling pathway (Fig. 9.1).

5 Cold Responses Mediated by Growth-Promoting Phytohormones Growth-regulating phytohormones such as GAs and AUXs also display a relevant function in plant response to cold stress. Growth reduction in response to cold is associated with a down-regulation of GA and AUX metabolism (Rahman, 2013; Vanková et al., 2014). Cold-treated wheat plants decreased GA4 content in all organs (Vanková et al., 2014), whereas citrus trees exposed to cold stress showed a decrease in GA1, GA3, GA4, and GA7 endogenous levels, which was finally associated with an enhanced cold tolerance (Peng et al., 2021).

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Cold stress in citrus increases CBFs, GA oxidase and DELLA expression levels together with a reduction in GAs availability, suggesting that DELLA-dependent growth repression stimulated by CBF pathway could be part of cold tolerance strategy (Peng et al., 2021). A higher endogenous level of GA3 during tomato cold storage was associated with an enhancement of cold tolerance and lower chilling injuries (Zhu et al., 2016). Furthermore, it is suggested that the CBF pathway mediated GA-induced chilling tolerance in tomato fruit by modulating GA catabolism. AUXs possible implication in cold stress signaling is limited. AUX signaling genes, which play a relevant role in determining a small leaf petiole angle, could be impacting in rapeseed cold adaptation, providing insights into possible molecular mechanisms behind environmental adaptation of Brassica napus (Hu et al., 2021). These findings provide clues regarding the molecular mechanism behind environmental adaptation at the seedling stage and present valuable information for facilitating marker-based breeding in this crop. In pumpkin (Cucurbita maxima) exposed to cold stress, a total of 53 genes related to AUX signaling pathway were differentially expressed, mostly down-regulated, indicating that this process is inhibited, including 20 AUX-IAA, 21 small Auxin-Up RNAs (SAURs), six AUX1s, four Gretchen Hagen 3s (GH3s), and one auxin response factor (ARF), all involved in AUX-induced signal transduction (Li, Lu, et al., 2021).

6 Phytohormones Interplay Towards Cold Tolerance Relevant research during recent years analyzed the concerted interaction among phytohormones that finally conduct (or not) to cold stress survival. Transcriptomic analysis revealed that plant hormone signal transduction (mostly JA, ABA, AUX, and ET) and glycerophospholipid metabolism are two of the most modified metabolic processes in response to chilling stress in mangrove apple (Sonneratia caseolaris) seedlings, indicating a tight connection of phytohormones with fatty acid metabolism that respond coordinately to low temperature (Yang et al., 2021). In pumpkin (Cucurbita maxima), a total of 148 gene expression changes under cold stress were associated with auxin (AUX/IAA), cytokinin (CK), GA, ABA, ET, BR, JA, and SA-mediated pathways. Moreover, changes in other possible messengers such as H2O2, Ca2+ or sugars, have been proposed as crucial during cold stress response (Li, Lu, et al., 2021). Under low temperatures, several biological processes and molecules are affected amino acids, re-distribution of intracellular calcium ions as well as alterations in protoplasmic streaming and electron flow (Hassan et al., 2021). In this context, maintenance of membrane integrity or cuticle properties under cold storage should be crucial to avoid the imbalance of membrane fluid content and derived changes in permeability that severely affect biochemical processes. BRs were described to regulate and favor membrane fluidity and, hence, enhancing plant and fruit tolerance to cold stress (Ahammed et al., 2020; Sadura et al., 2021).

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BRs were described to alleviate cold injury, reducing membrane damage by lipid peroxidation, alleviating ROS burst and improving antioxidant capacity and photosynthetic efficiency when applied exogenously (Li, Sun, et al., 2021). BR and ABAs were described to interplay in favoring cold tolerance, since application of both phytohormones enhanced antioxidant defense slowing ROS accumulation under chilling temperatures. However, fluridone (an ABA inhibitor) application blocked BR protective effect, suggesting that ABA is mediating this process (Liu et al., 2011). It was also proposed that Ca2+ signaling is involved in both ABA- and BR-induced cold tolerance (Hassan et al., 2021; Li, Sun, et al., 2021). BR function appears to be mediated by other phytohormones since exogenous brassinolide application in maize seedlings promoted cold tolerance by inducing slightly higher levels of endogenous IAA and GA3, while decreasing internal ABA content (Sun et al., 2020). An interaction between BRs and ET was also evidenced in Arabidopsis mutants since overexpression of BRS1 gene derived in a higher expression of ET synthesis-related genes (ACS4, ACO3) and resulted in an enhanced cold tolerance (Zhang, Guo, et al., 2021). BRs analogs application in cotton seedling revealed an interaction with both ABA and ET, causing an inhibition of signal transduction and an induction of cold tolerance (Dou et al., 2021). Leaf senescence was promoted under dark (senescence) and cold conditions (yellowing), favored by a balanced action of ABA and BR. Pathway analysis demonstrated that cold-induced senescence is favored by ABA pathway but prevented by BR genes (Panigrahy et al., 2021). EBR application favors GA3 and IAA accumulation in tomato plants where coldsensitive species showed an altered response. BR and ABA also act synergically favoring cold tolerance through antioxidants regulation, photosynthesis and expression of stress-related genes such as ERFs and ICE1 in this crop (Heidari et al., 2021). Authors revealed that the EBR treatment decrease the ROS damage by stimulating antioxidant enzymes, improving the growth rate of the tomato by favoring AUX and GAs endogenous content (Heidari et al., 2021). The crosstalk of SLs with other phytohormones such as AUX, ABA, CK and GAs, in response to abiotic stresses, indicates that SLs are part of the mechanisms that favor stress adaptation (Bhoi et al., 2021). A higher cold tolerance after SL GR24 application (which induced LOX activity) suggests a crosstalk between oxylipins and jasmonates in SL-mediated chilling tolerance and brings the phenylpropanoid pathway into consideration (Omoarelojie et al., 2021). Endogenous ABA in tomato increased in response to SL exogenous application, suggesting that SLs positively regulate tomato cold tolerance at least partially by the induction of CBF-mediated and the antioxidant response in an ABA-dependent manner (Chi et al., 2021). Recent reports in citrus trees revealed that there are many changes in gene expression between cold tolerant and cold-sensitive rootstocks involved in ABA, BR, and GA metabolism, being the first two up-regulated while the last downregulated in cold-tolerant genotype (Peng et al., 2021). Authors propose that the ABA and BR pathways may work cooperatively in cold response of the low-temperature resistant Chongyi wild mandarin to cold stress (Peng et al., 2021).

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7 Perspectives and Future Challenges Recent information suggest that BR-response cascade probably plays a relevant role in cold response regulation, with an emergent function of BR-favoring membrane properties to cope with cold-favored rigidness and lipid protection. A first level of regulation that involves a wide range of TFs is crucial, being both CBF-dependent and -independent pathways activated, leading to physiological changes mainly related to osmoprotectans accumulation and activation of ROS scavengers (Peng et al., 2021). Many other osmolytes (such as glycine betaine, sugars, amino acids) and other plant hormones are involved in this tightly connected network finally resulting in plant cold adaptation. The diversity of processes and mechanisms involved requires a multi-disciplinary approach to reveal new clues and paths involved in this cold stress challenge (Hassan et al., 2021). Complementary approaches have proved to success in favoring freeze and cold tolerance including the application of traditional breeding techniques and new biotechnological tools (Gusta & Wisniewski, 2013; Wisniewski & Gusta, 2014). The improvement of cold stress tolerance by breeding (mostly still unsuccessful) may help to minimize the negative effects in growth and yield reduction in a changing climate context (Ramirez & Poppenberger, 2020). New key targets for breeding are being discovered helping to design cold tolerance improvement strategies that aim to minimize trade-offs on crop yield. Under worldwide climate change scenario, how plants may survive under such emerging environments? Is cold tolerance compatible with an accepted crop growth and yield? How global temperature rise will impact in cold adaptation and the contribution of phytohormones to this balance should be elucidated. New players such as BRs and SLs appear to contribute to cold tolerance and plant adaptation, together with amelliorating loses in crop growth and yield, and constitute possible targets for further cold-tolerance improvement (Fig. 9.2). ABA is a key cold stress response hormone usually, which was numerously linked with cold tolerance in plants. A rising challenge relies on the highly species-specific or tissue-specific responses where the ratio and cross-talk with other phytohomones could determine the success or failure during cold stress adaptation. The scenario is even more complex since it is worth noting that cold tolerance should be pursued in coordination with other environmental challenges such as salinity, nutrient starvation, water scarcity, darkness or high-light stress that often occur simultaneously. In this context, new emerging technologies and techniques integrated to different disciplines should be crucial for the complete understanding of physiological responses under cold stress.

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Chapter 10

Drought Stress: Involvement of Plant Hormones in Perception, Signaling, and Response Sasan Aliniaeifard, Maryam Rezayian, and Seyed Hasan Mousavi

1 Putative Roles of ABA in Drought Stress Response Abscisic acid (ABA) is a sesquiterpenoid (C15H20O4) containing a 15-carbon ring, which acts as a chief regulator for the enhancement of abiotic stress tolerance in plants (Cutler et al., 2010; Hauser et al., 2011). This phytohormone regulates different processes in order to enable plants to cope with various stresses (Chater et al., 2014; Montillet et al., 2013). When environmental conditions are unfavorable such as the lack of enough moisture in the surrounding environments (both root and shoot environments) of the plants, the ABA level enhances (Aliniaeifard et al., 2014a; Aliniaeifard & van Meeteren, 2013, 2014; Hu et al., 2005; Pantin et al., 2013) through three main pathways including (Fig. 10.1): • Promotion of its biosynthesis (Finkelstein, 2013; Wani & Kumar, 2015) • Slowing down or retardation of its degradation (Kondo et al., 2012; Okamoto et al., 2009) • Conversion of its inactive form (ABA-glucose ester) to active form (Lee et al., 2006)

S. Aliniaeifard (*) Photosynthesis Laboratory, Department of Horticulture, Aburaihan Campus, University of Tehran, Tehran, Iran e-mail: [email protected] M. Rezayian Department of Plant Biology, School of Biology, College of Science, University of Tehran, Tehran, Iran S. H. Mousavi Vegetable Research Center, Horticultural Sciences Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_10

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Fig. 10.1 ABA accumulation as a result of plant exposure to water deficit condition. Water vapor deficit in the surrounding air, moisture deficit, and osmotic stress in the rhizosphere would result in ABA accumulation in plant organs (e.g., leaf and root) through three mechanisms: promotion of ABA biosynthesis, slow down or retardation of its degradation, and conversion of its storage and inactive form [ABA-glucose ester (ABA-GE)]

Close relationship between drought tolerance and ABA accumulation is reinforced by the evidence that exogenous application of ABA could improve drought tolerance (Liting et al., 2015; Zeinali et al., 2014). Accumulation of endogenous ABA have been reported in diverse plant species such as maize and wheat in response to drought stress (Guóth et al., 2009). The 9-cis-epoxycartenoid dioxygenase (NCEDs) functions as the main rate-limiting factors for ABA synthesis. NCED genes were detected to be upregulated in bean and cowpea under drought condition (Malcheska et al., 2017). The ABA can have both slow and rapid responses to drought stress. The slow response of ABA comprises alteration in expression of drought-induced genes, whereas the rapid response is intermediated by the involvement of ion channels (Song et al., 2016). There is an interrelationship between the effects of drought and salt stresses on plant (Shomali et al., 2021; Shomali & Aliniaeifard, 2020). Drought can impose osmotic stress on the plant cells. ABA plays a vital role in the osmotic stress tolerance of plants (Zhang et al., 2006). Osmotic stress induced by drought causes dehydration and prevention of water uptake in plants. ABA changes ion transport of guard cells under both drought and saline conditions, which induces closure of stomata and inhibits their opening (Kim et al., 2010), in order to control excessive water loss from the plant (Aliniaeifard, Hajilou, and Tabatabaei 2016; Aliniaeifard, Hajilou, Tabatabaei, and Sifi-Kalhor 2016; Aliniaeifard & Van Meeteren, 2016; Lastochkina et al., 2021; Seifikalhor, Aliniaeifard, Shomali, et al., 2019). ABA prompts the expression of various transcription factors and genes that are involved in encoding of the enzymes having roles in the synthesis of compatible osmolytes (Daszkowska-Golec & Szarejko, 2013). LEA-like proteins and dehydrins act as cellular chaperones that maintain macromolecules and membranes in the cells. LEA-like proteins are synthesized by both ABA-dependent and ABA-independent pathways under drought stress (Bhattacharjee & Saha, 2014; Shinozaki & Yamaguchi-Shinozaki, 2007). Apart from the effects of ABA on osmotic regulation and gas exchange responses of plants under water deficit conditions, ABA stimulates gene transcription and

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activities related to the antioxidant enzymes that have a role in the detoxification of reactive oxygen species (Jiang & Zhang, 2003). It has also been reported that ABA improves carbon metabolism, protein transport, and expression of resistance proteins to enhance plant tolerance to drought (Zhou et al., 2014).

2 ABA-Dependent and ABA-Independent Signaling Pathways Under Drought Stress Stomatal aperture are modulated through both ABA-dependent and ABA-independent pathways in response to drought conditions (Planchet et al., 2011; Seo et al., 2012). Drought stress promotes stomatal closure through two main pathways: first, close the stomata through the participation of ABA signaling and second, close the stomata through the induction of an osmotic stress. Stomatal closure through elevated levels of ABA is a slow response to water deficit conditions, while induction of a hyperosmotic shock generates a fast-acting signal promoting closure of the stomata (Luan, 2002). Therefore, in general in response to water scarcity, both ABA and hyperosmotic signals promote stomatal closure, and in this way, a closure response of the stomata to water stress would be prompt. The ABA perception by ABA receptors starts the ABA-induced signaling cascades. The early part for the onset of perception and signaling of ABA comprises its receptor protein including PYrabactin Resistance (PYR)/PYrabactin Resistance-like (PYL)/Regulatory Component of the ABA Receptor (RCAR) family. When ABA level due to water deficit increases and this signal is perceived by ABA receptors, a series of events occur (Aliniaeifard et al., 2014b, 2020; Aliniaeifard & van Meeteren, 2013; Shomali & Aliniaeifard, 2020) (Fig. 10.2). The signaling pathway of ABA that finally result in the plant responses (e.g., stomatal closure or seed dormancy) is comprised of positive and negative regulators: SNF1-related kinases (SnRK2) are positive regulators, and Protein Phosphatase 2Cs (PP2Cs) function as negative regulators of ABA signaling (Umezawa et al., 2010). The expression level of various genes is up- or downregulated by ABA-dependent and independent pathways under drought conditions. ABA-responsive element (ABRE) and ABRE-binding protein/ABRE-binding factors (AREB/ABFs) play key roles in gene expression on an ABA-dependent path. Dehydration-responsive element/C-repeat (DRE/CRT) and DRE-/CRT-binding protein 2 (DREB2) transcription factors have main functions in gene expression in an ABA-independent way during exposure to water deficit conditions. AREBs/ABFs are members of the bZIP (basic leucine zipper) subfamily of transcription factor. AREB1/ABF2, AREB2/ABF4, and ABF3 act as positive modulators of the ABA-dependent signaling pathways under water deficit conditions (Fujita et al., 2005). Similarly, some other transcription factors such as AREB/ABF are stimulated in a pathway with the participation of ABA via phosphorylation of their preserved domains through SnRK2s (Furihata et al., 2006).

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Fig. 10.2 Water deficit-induced ABA signal transduction in guard cells of stomata. Under water deficit conditions, ABA accumulate in the guard cell symplast through three sources: (1) delivery of ABA from the root and vascular system (AtABCG25 transporter in the vascular system and function of guard cell importers; AtABCG22 & 40) into the guard cell, (2) Conversion of ABA-GE (storage and inactive form of ABA) to ABA, and 3. inhibition of ABA-hydroxylases (CYP707A1 & 3) that catabolize ABA in the vascular system and guard cell. Following ABA accumulation in the guard cells and its perception by receptors PYR/PYL/RCAR, it is able to block the negative regulators (ABI1 & 2/PP2C); as a result its positive regulators (SnRK2/OST1 protein kinase) will be activated, which block KAT1 ion channels (K+ importer) and activate SLAC1 (Cl-); consequently stomatal closure occurs. Red lines show blockage and black arrows indicate activation [modified from (Aliniaeifard & van Meeteren, 2013)]

The SnRK2s phosphorylate downstream proteins, including ion channels, enzymes, and transcription factors, thereby prompt ABA responses. SnRK2 OPEN STOMATA 1 (OST1) is an important protein kinase during ABA signaling, which participates in modulating the stomatal closure through adjustment of guard cell swellings. Under drought stress, ABA activates OST1 and inhibits water loss. Thus, SnRK2/OST1 functions as a positive regulator during ABA-mediated closure of stomata (Sirichandra et al., 2009). SnRK2/OST1 activates SLOW ANION CHANNEL ASSOCIATED 1 (SLAC1), an S-type anion channel, which involves ABA-induced closure of stomata (Brandt et al., 2012). H+-ATPase in guard cells

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has an important role in modulating stomatal opening and closure. H+-ATPase activity is blocked by ABA through a regulatory mechanism involving OST1 (Merlot et al., 2007). DREB2 proteins belong to the AP2/ERF family of plant-specific transcription factors. DREB2 has a preserved AP2/ERF domain that initiate expression of some stress-tolerance-related genes through binding to DRE/CRT cis-acting element, thus augmenting tolerance to stress in plants (Shinozaki & Yamaguchi-Shinozaki, 2000). Among eight DREB2s in Arabidopsis, DREB2A and DREB2B are noticeably prompted by water deficit stress. DREB2A acts as the main transcription factor for the modulation of gene expression in an ABA-independent pathway during drought exposure. The protein level of DREB2A is strongly controlled by ubiquitin E3 ligases such as DREB2A-INTERACTING PROTEIN1 (DRIP1) and DRIP2. Furthermore, expression of DREB2A is suppressed by GROWTH-REGULATING FACTOR7 (GRF7) under normal conditions. Through targeting DREB2A to 26S proteasome proteolysis, DRIP1 and DRIP2 negatively adjust gene expression in response to drought (Sakuma et al., 2006).

3 Putative Roles of Auxin in Drought Stress Response Among the main plant growth regulators, auxin plays different roles in plant growth and development. Indole-3-acetic acid (IAA) is the chief auxin that synthesized by both tryptophan-dependent and independent pathways (Zhao, 2010). Auxin transport, biosynthesis, and conjugation with sugar and amino acids are regulated by environmental cues (Shibasaki et al., 2009). Several studies suggested a relation between drought stress and auxin responses (Rellán-Álvarez et al., 2016). Auxin contributes in the positive adjustment of drought stress tolerance, at least through the control of root architecture. Auxin increases root growth and branching, which might enhance water uptake efficiency and, therefore, help drought stress tolerance (Shi et al., 2014). Enhanced auxin content and better drought stress tolerance are associated with reduction in ROS level and leaf senescence in plants (Ke et al., 2015). Auxin also facilitates the accumulation of compatible solutes such as sugar alcohols and sugars. Also, auxin boosted the activity of four antioxidant enzymes which include superoxide dismutase (SOD), peroxidase (POX), catalase (CAT), and glutathione reductase (GR) under drought conditions, thus enhancing ROS detoxification (Sharma et al., 2015; Shi et al., 2014). Induction of shoot growth, formation of root hair, and reduction of water loss have been perceived in potato plants overexpressing the Arabidopsis YUCCA6 gene (gene of auxin biosynthesis) under drought stress (Im Kim et al., 2013). Glucosinolate (GLS) levels are controlled by the auxin-sensitive Aux/IAA repressors (IAA5, IAA6, and IAA19). Decline of IAA5/6/19 caused reduction in GLS level and drought tolerance, which is associated with a weakness in stomatal adjustment. Thus, auxin acts independently of ABA to control stomatal aperture by its impact on GLS level (Salehin et al., 2019). Auxin could improve drought

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resistance by controlling ROS metabolism and ABA-responsive genes expression (Schopfer et al., 2002).

4 Role of Auxin Responsive Genes in Drought Stress Response Transcriptomic studies discovered that the expression of some auxin-related genes is changed under abiotic stresses (Song et al., 2009). AUX/IAAs, small auxinupregulated RNAs (SAURs), and GRETCHEN HAGEN3s (GH3s) are auxinresponsive genes that are induced by auxin within a few minutes of receiving the signal. Auxin-intermediated transcriptional adjustments are dependent on the roles of Aux/IAA (Naser & Shani, 2016). Aux/IAA group of transcriptional repressors with corepressor proteins, such as TOPLESS, repress the target genes by auxin response factors (ARFs) at low auxin level. ARFs directly bind with DNA and may stimulate or suppress transcription of genes. Aux/IAA proteins are degraded by the 26S proteasome, causing de-suppression of ARFs and stimulation of transcriptional responses at high auxin level (Chapman & Estelle, 2009). IAA3, IAA14, and IAA18 play a regulatory role in lateral root formation by cooperating with ARF7 and ARF19 (Guseman et al., 2015). It has been reported that AUX/IAA12 (BDL) and AUX/IAA17 (AXR3) are involved in stomatal closure (Balcerowicz & Hoecker, 2014). Zhang et al. (2021) presented that OsIAA20 plays a significant role in drought response in rice plants, by regulating stomatal closure, proline content, and chlorophyll content. SAURs are the largest class of early auxin-responsive genes and numerous SAURs participate in the adjustment of drought-tolerance responses (Spartz et al., 2014). SAUR proteins play a common role in cell elongation and prompt plant growth by controlling cell wall acidification and adjust growth in response to environmental factors (Stortenbeker & Bemer, 2019). AtSAUR32 overexpression improved drought tolerance in Arabidopsis. AtSAUR32 possibly controls drought tolerance by drought-responsive parameters and ABA-independent pathways (He et al., 2021). Overexpression of TaSAUR75 augmented tolerance in Arabidopsis under drought. Transgenic plants under drought stress revealed upper root length and survival than the control plants. Higher expression of several stressresponsive genes and lower H2O2 content have been reported in transgenic plants under drought stress. TaSAUR75 decreased H2O2 content through triggering stresstolerance genes such as AtRD 26, which repress ROS accumulation (Guo et al., 2018) and help plant to cope with drought stress. GH3 genes, which encode auxin-conjugating enzymes (IAA-amido synthetases), also took role in plant responses to drought stress. OsGH3.13 promotes the transcript level of LEA (late embryogenesis abundant), which improve tolerance in rice seedlings exposed to drought condition (Zhang et al., 2009). Knockdown of GH3.5 is extremely assisted in tolerance of cotton plants to drought stress by the

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induction of antioxidant enzyme activities such as SOD, reduction of malondialdehyde (MDA) content, and accumulation of proline (Kirungu et al., 2019).

5 Involvement of Auxin Carriers in Drought Stress Response Auxin transport occurs by two distinct pathways in plants including active intercellular transport and passive transport through phloem. Influx and efflux carriers support the intercellular transport of auxin (Finet & Jaillais, 2012). Biosynthesis of auxin and its polar transport (PAT) play a significant role in the promotion of auxin production and are necessary for plant responses to stress conditions. The coordination and modulation of influx and efflux of auxin carriers create a flexible system for plant reaction to alteration in environmental cues. The AUX/LAX, PIN, PIN-LIKES (PILS), and glycoproteins (PGP) are auxin transporter in plants (Grones & Friml, 2015). Among them, AUX1/LAX influx, PIN, and ABC/PGP efflux carriers are the main groups of transporters that are involved in PAT. Carrier abundance at plasma membrane, capacity of transport auxin, and polarity influence the rate and directionality of intercellular auxin movement and thereby determine the pattern of auxin distribution (Adamowski & Friml, 2015). PGP proteins involve in the cellular and long-distance transport of auxin and are members of ATP-dependent ATP-binding cassette (ABC) transporter subfamily (Geisler & Murphy, 2006). AUX1/LAX transporters belong to the auxin amino acid permease (AAAP) family of proton-driven transporters (Bennett et al., 1996). The polarity and flexible subcellular localization of AUX1 across roots permits quick regulation of auxin flow and thus control of root growth in response to environmental factors (Swarup et al., 2001). Also, AUX1 is involved in acropetal auxin transport and lateral root primordial formation (Laskowski et al., 2008). It has been shown that AUX1 plays a significant role in adjusting plant responses to abiotic stresses (Swarup & Bhosale, 2019). The PIN carriers contribute to auxin transport at intracellular and intercellular levels in plants. PINs have specific functions in the developmental processes such as embryogenesis, positioning, initiation, and new organ formation (Blilou et al., 2005). Shen et al. (2010) showed that the expression of SbPIN4, SbPIN5, SbPIN8, SbPIN9, and SbPIN 11 was extremely enhanced in Sorghum bicolor under drought condition. It has been proposed that the PAT pathway is involved in the regulation of the response to drought stress in rice plants (Zhang et al., 2012) as the OsPIN3t participates in auxin transport and the drought stress responses of rice plant.

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6 Putative Roles of Gibberellin in Drought Stress Response Gibberellins (GAs) belong to tetracyclic diterpenoid carboxylic acid class and play important roles in plant responses including leaf expansion, seed germination, flowering time, stem and root growth, and development of fruit (Sun & Gubler, 2004). GA has two opposite roles in plant tolerance to drought stress. Low GA level is associated with enhancement of plant tolerance to abiotic stresses, including drought and salt (Nir et al., 2017). The plants need to keep GA level low in order to be able to restrict excessive water loss under drought conditions (Nir et al., 2014). Low GA levels are also associated with osmolyte accumulations (Omena-Garcia et al., 2019), stimulation of stress-related genes, and ROS suppressing enzymes (Achard et al., 2008), which all result in the improvement of drought tolerance. On the other hand, GAs are contributed in plant responses to abiotic stresses, which is described by supporting plant growth and development under stress conditions (Colebrook et al., 2014). GAs have a vital role in the control of sourcesink transfer under various growth conditions (Iqbal et al., 2011). Despite of the indicated negative effects of high GA level on drought stress tolerance, it has been reported that GA application could induce plant growth, maintain photosynthetic functionality, and reduce oxidative damage under stress conditions (Akter et al., 2014). Furthermore, amplification of GA signal from root-to-shoot can facilitate the balance between water use and growth during drought stress exposure (Gaion et al., 2018).

7 Role of GA on Stomata Movement and Other Physiological Responses GA3 stimulates division of epidermal cells and development of stomata in Arabidopsis. GA is a positive regulator of stomatal opening (Göring et al., 1990). Plant responses to GA are blocked by a famous nuclear proteins introduced as DELLAs, which cooperate with several other transcription factors (Locascio et al., 2013). GA has indirect impacts on transpiration by reduced plant size (Magome et al., 2008). In tomato, overexpression of GA METHYLTRANSFERASE1 reduces the GA levels, which leads to improved water deficit tolerance. Due to reduced transpiration, the transgenic plants are capable to preserve more leaf water content for a longer duration than the wild-type plants under drought stress. However, it has been reported that the declined transpiration was related to the generation of slighter leaves, leading to closure of stomata in transgenic plants. This is indicative of regulatory role of GA on water loss of plants through the modulation of stomatal aperture (Nir et al., 2014). Low stomatal conductance, limited transpiration, and sustained relative water content were observed in tomato plants exposed to drought

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and treated with GA. This reveals a significant role of GA to prompt stomatal closure during drought conditions (Gaion & Carvalho, 2021). GA is able to suppress ROS under drought stress, and it helps plants with their more negative water potential, thus conserving photochemical operation of photosystem II (Aktas et al., 2008). Pan et al. (2013) showed that GA can remove ROS similar to the function of antioxidant enzymes. Furthermore, GA aids to reduce lipid peroxidation and induce POX and SOD activity. It is also reported that GA improves photosynthetic functionality, postpones leaf senescence, and enhances seed-set under drought conditions (Li et al., 2010). GA boosts the chlorophyll content of leaf and uptake of mineral nutrients under drought stress (Hasanuzzaman et al., 2018), which alleviate the negative impacts of drought on plants.

8 Role of GA in Leaf Senescence and Drought Stress Signaling GA has inhibitory impact on senescence, but its active form degrades as the plant ages (van der Graaff et al., 2006). GA influences leaf senescence through DELLA proteins which are negative regulators of its signaling pathway (Jan et al., 2019). It has been shown that GA signaling acts upstream of ethylene, SA, and JA pathways during leaf senescence (Chen et al., 2014). In Paris polyphylla, exogenous application of GA inhibited leaf senescence, although paclobutrazol, a deterrent of GA biosynthesis, enhanced senescence. In P. polyphylla, GA inhibits leaf senescence by inhibiting impacts on ABA. Thus, ABA and GA cross talk shows a significant role in adjusting leaf senescence (Yu et al., 2009). GA response to abiotic stresses includes alteration in its biosynthesis, inactivation, perception, and signal transduction (Colebrook et al., 2014). The dioxygenases include GA 2-oxidases (GA2ox), GA 3-oxidase (GA3ox), and GA 20-oxidase (GA20ox), causing inactivation of GA (O’Neill et al., 2010). The biosynthetic pathway of GA has been detected in response to environmental factors (Hedden & Kamiya, 1997). As an example, downregulation of GA 2-oxidase, the GA inactivation-associated enzyme, has been detected in wheat roots under drought stress (Krugman et al., 2011). There are several pivotal components in signaling pathway of GA: GA receptor [GIBBERELLIN INSENSITIVE DWARF1 (GID1)], GA inhibitors (DELLAs), and the F-box proteins SLEEPY1 (SLY1) and SNEEZY (SNZ) (Achard et al., 2008). GA stimulates plant growth by promoting cell elongation through the suppression of DELLA. Induction of GID1L2 in wheat plants showed that GA participates in drought tolerance through its action on the roots (Krugman et al., 2011). Binding of GA to GID1 modulates the association of GID1 with DELLA proteins, following poly-ubiquitination of DELLAs by the E3 ubiquitin-ligase SCFSLY1 and ultimately DELLAs destruction. Besides, non-destructed DELLAs cause reduction of expansion rate and cell proliferation, and increase of DELLA proteins inhibits root

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meristem size (Sun, 2010a). Also, DELLA proteins are used for controlling stomatal aperture in Arabidopsis (Sukiran et al., 2020).

9 Mediation of Cellular Expansion Under Drought Stress Cell elongation is regulated by cell wall expansion through cell wall proteins such as xyloglucan endotransglycosylase (XET) and expansin (Cosgrove, 1998). Expansin facilitates cell wall tension by interrupting the hydrogen bonds connecting cellulose microfibrils to matrix polysaccharides. XETs have vital roles in strengthening and loosening of the cell wall by matrix cleavage without hydrolysis. Some of the XET and expansin genes have various roles in adjusting plant growth and stress tolerance in different plants (Cal et al., 2013; Cosgrove, 1997; Eklöf & Brumer, 2010). For example, TaEXPB23 responds to drought stress in wheat plants (Han et al., 2012). GA regulates cell elongation in different plant organs including leaves, hypocotyls, internodes, and roots (Bultynck & Lambers, 2004; Ubeda-Tomás et al., 2009). GA controls plant growth through the stimulation or suppression of gene expression following downstream impacts on cell division and elongation (Azeez et al., 2010). GA3 upregulates the gene expression of expansins, XET, and cyclindependent protein kinases and increases cell elongation and division (Sun, 2010b). GA could alleviate stress retardation of leaf elongation by assisting cell elongation under osmotic stress. Direct effects of GAs on the cellular expansion are not clear under drought stress so far. GA can also modify cell expansion by stimulating expansion genes comprising EXPA4 and EXPB4 and XET genes under drought stress (Xu, Burgess, et al. 2016; Xu, Liu, et al. 2016). Todaka et al. (2012) recognized that OsPIL1, a GA-responsive transcription factor, downregulates expansin in the internode of plants under drought stress.

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Putative Roles of Cytokinin in Drought Stress Response

Cytokinin (CK) as one of the indispensable phytohormones plays a vital role in the cell cycle, growth, and development of plants. Also, CK delays senescence of plants by preventing decomposition of nucleic acids, chlorophyll, proteins, and other compounds in plants and reorganizing essential amino acids, inorganic salts, hormones, and other constituents to other sections of the plant (Ullah et al., 2018). CK level can be increased or decreased during drought exposure, leading to drought tolerance. Enhancement of drought tolerance through regulation of CK level rely on soil water potential, stress duration, and plant dehydration percentage (Zhang et al., 2018). The rise of CK level may aid drought tolerance via impeding drought-accelerated leaf senescence. It has been revealed that overexpression of isopentyl transferase (IPT), which involves CK biosynthesis, enhances CK levels, and develops drought

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tolerance by boosting metabolite accumulation and antioxidant system activity in plants (Kuppu et al., 2013; Rivero et al., 2009). CK can alleviate the decline in photosynthetic rate under water stress conditions, through controlling chlorophyll biosynthesis and stomatal conductance (Cortleven & Schmülling, 2015). CK influences ROS content by various mechanisms, such as inducing the activity of antioxidant enzymes (SOD and CAT) and inhibiting the activity of ROS-producing enzymes (xanthine oxidase). Reduction of CK level can increase drought tolerance by different physiological responses comprising induction of leaf senescence, stomatal closure, and leaf abscission (Naidoo & Naidoo, 2018). Since CK is a negative controller of root growth, declined CK level causes root expansion and elevated root-to-shoot ratio, resulting in the enhancement of water uptake by the roots. Comparatively restricted shoot growth and leaf area can limit transpiration. Therefore, plant can preserve high water content resulting in the improvement of drought tolerance (Lubovská et al., 2014).

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Leaf Senescence and Drought Stress Signaling

CK is the main phytohormone that impedes senescence and therefore is considered as an important agent for the improvement of crop growth (Zwack & Rashotte, 2013). CK prevents senescence by stimulation of genes that are involved in oxidative stress occurrence, and as a consequence, it avoids chlorophyll catabolism and maintains chloroplast functionality (Lu et al., 2017). Elevated level of CK is described to impede leaf senescence and induce drought tolerance in creeping bentgrass due to increased activity of IPT (Merewitz et al., 2016). CK inhibits senescence by modulating its own biosynthesis via the IPT gene using a promoter senescence-associated gene 12 (SAG12) (Xiao et al., 2017). Transgenic plants where IPT expression is adjusted by the SARK promoter conserve better photorespiration rate and water content and showed delayed leaf senescence and increased stress tolerance under drought conditions (Kuppu et al., 2013). CK signaling is a complex phosphorylation system including histidine kinases (HKs), histidine phosphotransfers (HPs), and response regulators (RRs) and regulates cell division, apical dominance, and leaf senescence (Pils & Heyl, 2009). Furthermore, this complex phosphorylation system takes a role in response to stress signals. CK functions as a signal to trigger the HKs input domain and causes phosphorylation of preserved His residue. The phosphate group is transmitted to preserve Asp in Rec domain and then transported to HPs and RRs downstream components. In this way CK causes a regulatory stream. CK ultimately causes alterations in transcription of genes in the nucleus (Schaller et al., 2008). Changing the CK level by modifying the expression of biosynthetic (IPT) or degradation (CKX) genes could influence the expression of different genes and consequently could improve drought tolerance. Overexpression of CK biosynthesis-associated gene (IPT) in creeping bentgrass caused the expression of

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encoded genes having various functions including RuBisCo large subunit, CAT, Leu-rich repeat (LRR) receptor-like kinase, chloroplast precursor, and oxygenevolving enhancer protein 3-1 (Merewitz et al., 2016). AHK1 is prompted by drought and is a positive manager of drought tolerance, probably performing like an osmosensor (Kumar et al., 2013). AHK1 plays a role in response to drought during the vegetative phase of plant growth and in the adjustment of dehydration processes during seed development (Wohlbach et al., 2008). Drought significantly increased the expression of ARR genes such as ARR5, ARR7, ARR15, and ARR22 (Kang et al., 2012). AHK5 is a negative regulator of drought stress, directly cooperating with AHP1, AHP2, and AHP5 (Pham et al., 2012). Dehydration stress prompts the transcription of type-A ARR5, 6, 7, and 15 (Kang et al., 2012). The roots of transgenic barley overexpressing AtCKX1 gene exhibited a high level of transcripts playing a role in photosynthesis, phenylpropanoid pathway, and drought-responsive transcription factors under drought stress (Vojta et al., 2016).

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Putative Roles of Ethylene in Drought Stress Response

Ethylene is one of the main phytohormones with the molecular formula of C2H4, which acts in a gaseous form. This phytohormone has a diverse role in plants including leaf abscission, floral opening, and fruit ripening. For the biosynthesis of ethylene, first S-adenosyl-L-methionine (SAM or AdoMet) is produced through AdoMet synthetase. AdoMet then through the involvement of ACC synthase converts to 1-aminocyclopropane-1-carboxylic-acid (ACC), which is considered as the precursor of ethylene biosynthesis. This step is the rate-limiting part of the ethylene biosynthetic pathway. On the step, ACC oxidase in the presence of oxygen converts ACC into ethylene (Chen et al., 2010). Ethylene is considered as a stress hormone due to its production and effects under stress and senescence occurrences. Following a 10–30-min lag time, ethylene applies its effects through a sharp increase in its production within several hours (Yang & Hoffman, 1984). The involvement of ethylene in plant drought stress response is a complicated process. When exposure to drought stress is intense and fast, production of both ethylene and its precursor, ACC, would occur. When exposure is gradual, induction of ethylene or ACC accumulation would not occur. There are some indication regarding the involvement of ABA in the induction of ethylene synthesis. For instance, the accumulation of ABA in the roots as a result of water scarcity in the rhizosphere induces ACC synthesis and elevates ethylene production in the leaves. However, it has been shown that the application of ethylene to plants that are exposed to drought stress promotes stomatal opening in wild-type Arabidopsis (Tanaka et al., 2005).

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There are still many questions about the role of ethylene and its signal transduction under drought and salt stress exposure. Since the regulation of stomatal aperture under drought is of vital importance, the role of ethylene in the regulation of stomatal aperture is still controversial. The interaction between ethylene and other phytohormones is widely studied, and many synergistic and antagonistic interactions have been reported. For instance, auxin (at concentrations of 0.01 to 1.0 mM of IAA) and ethylene releasing compound, ethephon (0.3% v/v Ethrel), induce stomata opening when they are applied to the epidermal peels of Vicia faba (Merritt et al. 2001). Despite this synergistic effect of ethylene on stomatal opening, induction of stomatal closure by ethylene has been reported in tomato, carnation, and peanut. On the other hand, in pinto and jelly (Sedum pachyphyllum) bean plant, ethylene has null effects on stomatal opening and closure. Ethylene is involved in the production and accumulation of hydrogen peroxide (H2O2) during the process of programmed cell death. For instance, exogenous application of ethylene elevates camptothecininduced H2O2 production, while by itself alone it is not able to induce H2O2 production (De Jong et al. 2002). Regulation of stomatal closure by the involvement of ethylene has been reported (Tanaka et al., 2005). Investigating the stomatal response of Arabidopsis mutant with disturbed ethylene receptor, ETR1, confirmed the important role of ethylene in the induction of stomatal closure through the mediation of H2O2. In this mutant stomatal closure as the result of H2O2 accumulation is inhibited. This finding supports the interrelation between ethylene and H2O2 for closure response of stomata (Tanaka et al., 2005). Components of ethylene signalling pathways are involved in stomatal responses. Confirming this idea, etr-1 and etr1-3 ethylene receptor mutants are not capable of H2O2 accumulation and as the consequence closure of stomata. Mutations in another component of ethylene signalling pathway, EIN2, would result in H2O2 production when they are exposed to ethylene; however, they are not able to close their stomata in response to H2O2 or ethylene. Mutation in Arabidopsis response regulator 2 (ARR2) also exhibited the same pattern (Desikan et al., 2006). Stomata of other ethylene signalling mutant, etr1-7, was also not responsive to H2O2 application. Desikan et al. (2006) confirmed that H2O2-induced stomatal closure needs the ethylene receptor of ETR1 (Desikan et al., 2006). ETR1 is involved in both ethylene and H2O2 signal transduction; therefore, it may function as the interconnector of these two molecules (Desikan et al., 2005). Therefore, ethylene and H2O2 signalling in guard cell are modulated via ETR1 by the involvement of ARR2 and EIN2 signalling components (Desikan et al., 2006).

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Putative Roles of Polyamines in Drought Stress Response

Polyamines (PAs) are involved in different processes including embryogenic competence, fruit ripening, programmed cell death, biofilm formation, and xylem differentiation. Putrescine (Put), spermine (Spm), and spermidine (Spd) are the three major PAs in plants. PAs are mainly involved in plant responses to abiotic stresses. Their involvements in plant stress responses depend on type of species and stress duration and intensity. Remarkably, drought stress promotes changes in PA content, which is mostly associated with drought tolerance characters (Gill and Tuteja 2010). In transgenic rice, overexpression of the DsADC gene caused more drought tolerance by alteration of Put to Spd and Spm (Do et al. 2014). PAs can mitigate the oxidative stress of the stressed plants by adjustment of antioxidant systems (Seifikalhor et al., 2020), alterations in the ROS generation, and redox status. The PA-induced tolerance to drought stress could be related with the link between Ca2+ and H2O2 for the control of antioxidant systems (Li et al., 2010). Spm can adjust some ABA-associated genes, which in turn regulate stressresponsive gene expression, stomatal closure, and osmolyte accumulation (Fujita et al., 2005). Put performs similar to osmolite and buffering agent, prompting proline accumulation, which causes the preservation of plant water status during stress conditions (Kotakis et al. 2014). Spm application in drought-stressed soybean seedlings enhanced carotenoid, chlorophyll, protein content, SOD, and CAT activity. Furthermore, PAs have been recommended to be involved in the protection of membrane stability under stress conditions (Lu et al., 2017). A protective function for Spm under drought stress has been shown in Arabidopsis, where Spm moderates the activity of ion channels, increases Ca2+ concentration, and as a result prompts stomatal closure (Yamaguchi et al. 2007). Recently, Li et al. (2010) stated that Spm helps plant to sustain water equilibrium under drought conditions by inducing the expression of the Ca2+-dependent AQPs, TrTIP2-1, TrTIP2-2, and TrPIP2-7. Adamipour et al. (2020) showed that endogenous Spm level are enhanced in Rosa damascene seedlings under drought stress and triggered resistance mechanisms to alleviate drought stress. Photosynthetic efficiency (FV/FM) was detected to be greater in Spm-treated plants under drought stress (Krishnan and Merewitz 2017). Therefore, PA functions as osmoticum, antioxidant, stomatal closing agent, and photosynthetic functionality preserver in plants exposed to water deficit condition.

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Hormonal Cross Talk Under Drought Stress

Hormonal regulation of plant processes usually is not a sole function and mainly occurred synergistically or antagonistically with several phytohormone to control a function or process as well as stress responses in plant (Aalifar et al., 2020;

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Aliniaeifard & van Meeteren, 2013; Kalhor et al., 2018; Lastochkina et al., 2021; Seifikalhor, Aliniaeifard, Hassani, et al. 2019; Seifikalhor, Aliniaeifard, Shomali, et al. 2019; Seifikalhor et al. 2020; Shomali et al., 2021; Shomali & Aliniaeifard, 2020; Van Meeteren et al., 2020). For instance, ABA facilitates auxin transport in the root tip under drought conditions, which boosts the proton pumps in the plasma membranes. In the root tip, proton secretion plays a vital role in the growth of primary root and development of root hair under water deficit condition (Xu et al., 2013). Furthermore, it has been shown that in P. polyphylla, GA inhibits leaf senescence by antagonizing ABA. Thus, ABA and GA cross talk shows an important role in the process of leaf senescence (Yu et al., 2009). The interaction between ethylene and ABA for drought stress tolerance through the regulation of stomatal aperture attracted lots of attention (Tanaka et al., 2005). Stomatal response to ethylene depends on the presence or absence of ABA, or vice versa (Desikan et al., 2006; Tanaka et al., 2006). Ethylene or ACC as its precursor can prevent ABA-induced stomatal closure (Tanaka et al., 2005), while under lack or low ABA level, ethylene promotes closure of stomata (Desikan et al., 2006; Tanaka et al., 2006). The interaction between ABA and ethylene occurs in different levels from their production to their signal transduction. The action of ACC synthase, which produces the precursor of ethylene (ACC), can be retarded by ABA, as a result reduces the production of ethylene. It has also been shown that endogenous ABA limits ethylene production in plants under water stress condition (Sharp, 2002). Therefore, the interaction between ABA and ethylene determines plant responses to drought condition (Desikan et al., 2005; Chen et al., 2014). Induction of stomatal closure has been reported for some other phytohormones such as brassinosteriods (BRs), salicylic acid (SA), and jasmonic acid (JA) (Hossain et al., 2011; Khokon et al., 2011; Munemasa et al., 2011), while auxins and CKs inhibit stomatal closure or induce stomatal opening (Tanaka et al., 2006). BRs promote tolerance to drought stress in diverse plant species through the induction of stomatal closure (Acharya & Assmann, 2009). However, in Arabidopsis mutation in BSK5, encoding a brassinosteroid-signaling kinase protein increases sensitivity of stomatal closure response to ABA (Li et al., 2010). SA plays a role in pathogen defense responses, and also it induces stomatal closure when plants are exposed to water stress conditions (Acharya & Assmann, 2009). JA participates in plant defense responses to necrotic pathogens and pests. Similar to SA, JA level is elevated as a result of drought exposure, which induces stomatal closure in plants. JA-induced stomatal closure employs similar signaling components as the ABA has (Acharya & Assmann, 2009). CKs and auxins induce stomatal movements through the function of ethylene. Both of these phytohormones, through antagonistic effects of ethylene on the induction of stomatal closure by ABA, keep the stomata open (Tanaka et al., 2006). As indicated before, stomatal closure response to ethylene occurs when ABA level is low, and in the presence of high level of ABA, it keeps the stomata open (Desikan et al., 2006; Tanaka et al., 2006). Since ethylene application induces stomatal opening under drought condition (Tanaka et al., 2005), it decreases the

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level of stomatal closure by ABA and elevates transpirational water loss over the leaf surface of the plant (Song et al., 2005). Probably ethylene employs a pathway independent of ABA for the induction of stomatal closure. In line with this, it has been proposed that ETR1 contributes in ethylene and H2O2 cross talk for stomatal closure (Desikan et al., 2005).

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Chapter 11

Involvement of Phytohormones in Flooding Stress Tolerance in Plants Xiaohua Qi, Zhongyuan Hu, Xuehao Chen, Mingfang Zhang, and Mikio Nakazono

1 Introduction Based on the climate change and global warming in recent years, it is expected that flood frequency will increase continuously in South and Southeast Asia, Northeast Eurasia, eastern and low-latitude Africa, and South America (Hirabayshi et al., 2021). These climate change will expose crops in these regions to serious flooding stresses. Gas diffusion is much slower in water than that in air (10,000 times, Armstrong, 1979), which will subject submerged plants to reductions in oxygen (O2) and to an increase in ethylene because of its slow diffusion in water (Voesenek & Bailey-Serres, 2015). Consequently, submerged plants experience serious O2 deficiency, which leads to the inhibition of mitochondrial respiration and ATP production (Hartman et al., 2021). To survive under O2 deficiency, plants switch quickly from respiratory to fermentative metabolism. In the absence of respiration, fermentation still regenerates NAD+, thereby allowing glycolysis and ATP generation to continue in a hypoxic environment. However, the efficiency of ATP generation by glycolysis is significantly lower than that of mitochondrial respiration.

X. Qi (*) · X. Chen Department of Horticulture, School of Horticulture and Plant Protection, Yangzhou University, Yangzhou, Jiangsu, People’s Republic of China e-mail: [email protected] Z. Hu · M. Zhang Laboratory of Germplasm Innovation and Molecular Breeding, Institute of Vegetable Science, Zhejiang University, Hangzhou, People’s Republic of China Hainan Institute of Zhejiang University, Yazhou Bay, Sanya, People’s Republic of China Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Hangzhou, People’s Republic of China M. Nakazono Graduate School of Bioagricultural Science, Nagoya University, Nagoya, Japan © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 G. J. Ahammed, J. Yu (eds.), Plant Hormones and Climate Change, https://doi.org/10.1007/978-981-19-4941-8_11

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Therefore, some energy-consuming processes including protein synthesis are decreased under flooding. Moreover, sugar metabolism is also differentially altered in some plant species to balance carbohydrate metabolism and growth of plants (Loreti et al., 2018). To avoid O2 insufficiency under flooding stress, plants have adapted a variety of induced and/or constitutive anatomical traits to enhance the transport of gases between and within the aerial and submerged parts, such as aerenchyma and adventitious root (AR) formation, induction of barriers to radial O2 loss (ROL), and control of shoot elongation (i.e., the elongation of leaves, petioles, and internodes) (Voesenek & Bailey-Serres, 2015; Watanabe et al., 2017). Aerenchyma is the longitudinally interconnected gas spaces, which include primary aerenchyma and secondary aerenchyma (Yamauchi et al., 2013). Primary aerenchyma forms from the primary tissues, while secondary aerenchyma forms from the secondary tissues. Primary aerenchyma can be classified into schizogenous aerenchyma and lysigenous aerenchyma. Schizogenous aerenchyma is formed by cell separation and expansion of existing space, while lysigenous aerenchyma is formed by selective programmed cell death (PCD) in parenchyma tissues (Yamauchi et al., 2013). ARs develop from waterlogged organs such as hypocotyl and stem. Newly formed ARs usually contain more aerenchyma compared with primary roots (Visser and Voesenek, 2004; Steffens et al., 2006). In addition, to restrict O2 leakage, some waterlogging-tolerant plants have evolved their ability to develop ROL barriers in the external cell layers of the root basal zone (Armstrong, 1979). These morphological adaptions are effective for partially submerged conditions; however, they may not work under complete submergence. In some plant species, the shoots could elongate rapidly to keep some parts above the water surface, a strategy that is called low-oxygen escape syndrome (LOES). On the other hand, some plant species suspend growth to avoid energy consumption, which is called low-oxygen quiescence syndrome (LOQS, Colmer & Voesenek, 2009). Ethylene is the first signal to initiate these metabolic and morphological or anatomical responses in plants, whereas other hormones like auxin, gibberellin (GA), and abscisic acid (ABA) and their interactions are also involved in the flooding response. In this chapter, we summarize recent progress in the hormonal regulation of flooding responses in plants.

2 Roles of Ethylene in Flooding Stress Tolerance Ethylene was established to play important roles in most of the morphological, anatomical, and metabolic responses of plants to flooding, although it does not appear to involve in the ROL barrier formation. In the ethylene biosynthesis pathway, 1-aminocyclopropane-1-carboxylic acid (ACC) is firstly converted from S-adenosyl-L-methionine by ACC synthase (ACS) and then is catalyzed by ACC oxidase (ACO) into ethylene. Subsequently, the ethylene signal pathway, including the ethylene insensitive 1, 2, and 3 (EIN1, 2, 3), EIN3-like (EIL), constitutive triple

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response 1 (CTR1), and ethylene response factors (ERFs) govern plant development. Below, we summarized how ethylene biosynthesis and signaling regulate the flooding response in plants.

2.1

Role of Ethylene in Altering Plants to Low-Oxygen Level

Low-oxygen levels are quickly sensed by plants through ethylene signaling. Rapid induction of ethylene signaling was observed in the root tips of Arabidopsis 1 h after submergence, which allows plants to anticipate upcoming hypoxia (Hartman et al., 2019, 2021; Perata, 2020). Group VII ethylene response factors (ERF-VIIs) that act downstream of ethylene were known to play an important role in the activation of the transcriptional response to hypoxia (Gibbs et al., 2011; Licausi et al., 2011). Plant cysteine oxidases (PCOs) were found to oxidize the N-terminal Cys2 residue of ERF-VIIs into cys-sulfinic acid, which leads to the degradation of ERF-VII proteins by the 26S proteasome (Weits et al., 2014; White et al., 2018). Under flooding conditions, PCOs failed to destabilize the ERF-VII transcription factors as the PCO activity is repressed by low oxygen concentrations (