Mohammad Anwar HossainShabir Hussain WaniSoumen BhattacharjeeDavid J. BurrittLam-Son Phan Tran Editors

Drought Stress Tolerance in Plants, Volume 2Molecular and Genetic Perspectives

Drought Stress Tolerance in Plants, Vol 2

Mohammad Anwar HossainShabir Hussain WaniSoumen BhattacharjeeDavid J. BurrittLam-Son Phan TranEditors

Drought Stress Tolerancein Plants, Vol 2Molecular and Genetic Perspectives

123

EditorsMohammad Anwar HossainDepartment of Genetics and Plant BreedingBangladesh Agricultural UniversityMymensinghBangladesh

Soumen BhattacharjeeDepartment of BotanyUniversity of BurdwanBurdwan, West BengalIndia

Lam-Son Phan TranRIKEN Center for SustainableResource ScienceYokohamaJapan

Shabir Hussain WaniDivision of Genetics and Plant BreedingFaculty of Agriculture, WaduraSher-e-Kashmir University of AgriculturalSciences and Technology of KashmirSrinagar, Jammu and KashmirIndia

David J. BurrittDepartment of BotanyUniversity of OtagoDunedin, OtagoNew Zealand

ISBN 978-3-319-32421-0 ISBN 978-3-319-32423-4 (eBook)DOI 10.1007/978-3-319-32423-4

Library of Congress Control Number: 2016936434

© Springer International Publishing Switzerland 2016This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or partof 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 transmissionor information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilarmethodology now known or hereafter developed.The use of general descriptive names, registered names, trademarks, service marks, etc. in thispublication does not imply, even in the absence of a specific statement, that such names are exempt fromthe 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 thisbook are believed to be true and accurate at the date of publication. Neither the publisher nor theauthors or the editors give a warranty, express or implied, with respect to the material contained herein orfor any errors or omissions that may have been made.

Printed on acid-free paper

This Springer imprint is published by Springer NatureThe registered company is Springer International Publishing AG Switzerland

Preface

In nature, plants are frequently exposed to various abiotic stresses such as drought,extreme temperatures, submergence, high salt levels, heavy metals, mineral defi-ciency, and toxicity. Plants are seldom exposed to a single abiotic stress, but aremore frequently exposed to multiple stressors. For instance, high temperatures anddrought are commonly encountered together, and the impact of these two stressorson plants can be aggravated by mineral toxicities. It has been projected that abioticstressors may adversely affect yields in up to 70 % of staple food crops. Among thevarious abiotic stresses, drought is the most common and lethal for plants, partic-ularly in critical growth stages, and may result in the complete failure of crops.Conventional breeding approaches, such as selection, hybridization, hybrid breed-ing, wide hybridization, and ideotype breeding, have been used in the past and haveresulted in the development of abiotic stress-tolerant crop varieties. However, giventhe increasing demand of food due to an increasing world population, particularly inAsia, the pace of conventionally bred varieties is very slow. Drought is a complextrait and is governed by a number of genes with complex interactions and lowheritability, and thus is hard to investigate. Additionally, the utilization of wildrelatives for the development of drought-tolerant crop varieties has been slow due tocross incompatibility, the complex genetic nature of drought resistance, and cum-bersome breeding and phenotypic procedures. Advances in molecular genetics haverevealed complex cascades of events at the cellular level that control the adaptationof crop plants to drought, and that numerous genes are involved in the initiation ofabiotic stress-related defenses. These genes can be divided into three major cate-gories. The first group consists of genes concerned with direct protection of essentialproteins and membranes, such as osmoprotectants, free radical scavengers, lateembryogenesis abundant (LEA) proteins, heat shock proteins, and chaperones. Thesecond group comprises membrane transporters and ion channels, involved in waterand ion uptake. The third group consists of regulatory proteins, including kinasesand transcription factors that are involved in transcriptional regulation ofstress-related genes. These transcription factors are distributed in several families,such as the MYB, bHLH, bZIP, NAC, and AP2/EREBP families.

v

In the past few years, considerable effort has gone into deciphering the mech-anisms underlying plant responses to water deficit with the aim to develop cropplants resilient to drought stress. In this book Drought Tolerance in Plants, Vol 2:Molecular and Genetic Perspectives we present a collection of 21 chapters writtenby experts in the field of drought tolerance in plants. It is a timely contribution to atopic that is of great importance for future food security. Chapter 1 describes ourcurrent understanding of plant drought responses from the gene to the whole plant.In this chapter, the authors review, in depth, morphological, physiological, bio-chemical, and molecular mechanisms associated with drought responses andadaptations of crop plants. Chapter 2 describes the genetic basis of cellular anddevelopmental mechanisms and traits conferring drought stress tolerance. Chapter 3aims to uncover the process of drought signal perception, amplification, andtransduction, and to help readers understand the convergent signaling networks inplants exposed to multiple stressors. Chapter 4 deals with the molecular adaptationstrategies of plants under drought stress. The authors discuss signaling molecules,transcription factors, drought-responsive genes, and the regulation of geneexpression associated with the modulation of drought stress tolerance. Chapter 5unravels the recent advances in decoding the ABA signaling pathways in plant cellsthat are involved in drought tolerance. Chapter 6 provides a comprehensive over-view of plant responses to drought at the genetic level. The authors critically discussplant transcriptomic studies investigating drought responses in model plants andhow transcriptomic data can be used to evaluate drought tolerance in plants.Chapter 7 provides an in-depth overview of metabolomic studies related to droughtresponses, discussing preparation techniques for metabolomics, analytical advan-ces, metabolic responses to drought stress, and metabolic engineering of compatiblesolutes for drought tolerance in plants, as well as the future of metabolomics as atool to study drought tolerance. Chapter 8 summarizes the importance ofmicroRNAs, including drought-responsive miRNAs and their targets, and thestrategies to use miRNAs to enhance plant drought tolerance. Chapter 9 deals withthe chloroplastic proteomics of plants in response to drought, salinity, heat, light,and ozone stress. The authors critically discuss the importance of alteration ofprotein structure under various abiotic stresses. Chapter 10 is concerned with themetabolic responses of plants under drought and other abiotic stress conditions andconcentrates on the importance of stress duration and intensity, as well as theimportance of developmental stage. Chapter 11 provides an overview of the variousdefinitions of drought, basic principles of plant water relations, and the similaritiesand differences of drought responses and tolerance in wheat and barley genotypes atdifferent developmental stages, at physiological, biochemical, and molecular levels.In this chapter, the authors provide a brief account of breeding strategies and thepotential of molecular approaches to enhance drought tolerance in wheat andbarley. Chapter 12 discusses common stress-responsive transcription factors, theirinteraction networks and epigenetic control, bioinformatics studies, and themolecular modification of transcription factors involved in abiotic stress tolerance.Chapter 13 addresses the historical development of mutation breeding, mutationbreeding strategies for various plant species, including tilling and eco-tilling, the

vi Preface

application of mutation breeding for the improvement of quantitative traits,breeding strategies for developing drought-tolerant crop plants, and future per-spectives for mutation breeding. Chapter 14 describes various methods to identifycandidate genes for drought responses and tolerance, and provides a list of candi-date genes from model to cultivated crop plants, which might be used for theimprovement of drought tolerance by genetic engineering. Chapter 15 deals withthe principles of microarray, gene expression profiling, and gene ontologyenrichment analysis under drought stress and the future applications of thesetechniques. Chapter 16 deals with system biology approaches for drought stresstolerance, which include transcriptome reprogramming under drought, proteomicinsights, the crucial roles of metabolomics and transcriptomics, and the quest forsystems biology approaches that can be used to understand plant adaptation todrought. Chapter 17 represents a comprehensive overview of oxidative stress andreactive oxygen species (ROS), ROS signal transduction pathways, the effects ofROS on plant growth and metabolism, transgenic plants with higher enzymatic andnonenzymatic defense systems, and their tolerance to drought stress and futureperspectives. Chapter 18 investigates the potential for engineering glycine betaine(GB) metabolism for drought tolerance. In this chapter, the authors summarize thebiosynthesis of GB, genetically engineered biosynthesis of GB for drought toler-ance, the roles of GB in drought tolerance, and GB-induced expression of genesassociated with drought tolerance. Chapters 19 and 20 overviews the transgenicapproach to produce drought-tolerant plants, including past achievements, chal-lenges, and perspectives. In these chapters, the authors discuss the examples ofgenetically engineered crops for drought tolerance, including the environmental andfood safety assessment of genetically modified crops. Chapter 21 discusses chro-matin and drought tolerance. In this chapter, the authors present a comprehensivediscussion of chromatin, transcriptional control of drought stress via chromatinmodifying genes, and future strategies for chromatin control of sustainable droughttolerance in crop plants.

We hope that this volume will be helpful in building approaches to combatdrought stress in plants. This volume will, it is hoped, serve as a key source ofinformation and knowledge to graduate and postgraduate students, teachers, andabiotic stress researchers around the globe. We also believe that it will be of interestto a wide range of plant scientists, including plant breeders, biotechnologists,molecular biologists, agronomists, and physiologists who are interested in droughtresponses and tolerance of crop plants. This book would not have been possiblewithout the contributions of the experts who were eager to share their knowledge inmolecular and genetic perspectives in drought stress, and our heartiest gratitude toall of them. We would like to extend thanks to Dr. Kenneth Teng, the editorial staffof Springer, New York in enabling this book project. Finally, our special thanks toall of the staff members of Springer, Switzerland who are directly or indirectly

Preface vii

associated with us in the book project for their steady support and efforts for thetimely publication of this volume. We strongly believe that the information coveredin this book will make a sound contribution to this fascinating area of research.

Mymensingh, Bangladesh Mohammad Anwar HossainSrinagar, Kashmir, India Shabir Hussain WaniWest Bengal, India Soumen BhattacharjeeDunedin, New Zealand David J. BurrittYokohama, Japan Lam-Son Phan Tran

viii Preface

Contents

1 Understanding How Plants Respond to Drought Stressat the Molecular and Whole Plant Levels . . . . . . . . . . . . . . . . . . . 1Nezar H. Samarah

2 Genetics of Drought Stress Tolerance in Crop Plants. . . . . . . . . . . 39Michael James Van Oosten, Antonello Costa, Paola Punzo,Simone Landi, Alessandra Ruggiero, Giorgia Batelliand Stefania Grillo

3 Tolerance to Drought Stress in Plants: Unravellingthe Signaling Networks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71Karaba Nalkur Nataraja and Madathil Sreekumar Parvathi

4 Plant Molecular Adaptations and Strategies UnderDrought Stress. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91Sávio Pinho dos Reis, Deyvid Novaes Marques, Aline Medeiros Limaand Cláudia Regina Batista de Souza

5 The Role of Abscisic Acid in Drought Stress: How ABAHelps Plants to Cope with Drought Stress . . . . . . . . . . . . . . . . . . . 123Agata Daszkowska-Golec

6 Drought Stress Tolerance in Plants: Insights fromTranscriptomic Studies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153Éderson Akio Kido, José Ribamar Costa Ferreira-Neto,Valesca Pandolfi, Amanda Cordeiro de Melo Souzaand Ana Maria Benko-Iseppon

7 Drought Stress Tolerance in Plants: Insightsfrom Metabolomics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187Ana T. Mata, Tiago F. Jorge, Marcel V. Pires and Carla Antonio

ix

8 MicroRNAs: A Potential Resource and Tool in EnhancingPlant Tolerance to Drought . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217Bu-Jun Shi

9 The Response of Chloroplast Proteome to Abiotic Stress . . . . . . . . 237Fen Ning and Wei Wang

10 Metabolomics on Combined Abiotic Stress Effectsin Crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251Karin Köhl

11 Drought Stress Response in Common Wheat, Durum Wheat,and Barley: Transcriptomics, Proteomics, Metabolomics,Physiology, and Breeding for an Enhanced DroughtTolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277Klára Kosová, Milan Oldřich Urban, Pavel Vítámvásand Ilja Tom Prášil

12 Transcription Factors Involved in Plant DroughtTolerance Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315Lidiane L. Barbosa Amorim, João Pacífico Bezerra-Neto,Rômulo da Fonseca do Santos, José Ribamar Costa Ferreira Neto,Ederson Akio Kido, Mitalle Matos and Ana Maria Benko-Iseppon

13 Mutation Breeding and Drought Stress Tolerance in Plants . . . . . . 359Mohammad Taher Hallajian

14 Identification of Candidate Genes for DroughtStress Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385Amal Harb

15 Analyses of Drought-Tolerance Mechanism of Rice Basedon the Transcriptome and Gene Ontology Data. . . . . . . . . . . . . . . 415Ali Moumeni and Shoshi Kikuchi

16 Systems Biology Approaches to Improve Drought StressTolerance in Plants: State of the Art andFuture Challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 433José Ricardo Parreira, Diana Branco, André M. Almeida,Anna Czubacka, Monika Agacka-Mołdoch, Jorge A.P. Paiva,Filipe Tavares-Cadete and Susana de Sousa Araújo

17 Transgenic Plants for Higher Antioxidant Contentand Drought Stress Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . 473Chandrama Prakash Upadhyaya and Mohammad Anwar Hossain

18 Engineering Glycinebetaine Metabolism for EnhancedDrought Stress Tolerance in Plants . . . . . . . . . . . . . . . . . . . . . . . . 513Weijuan Fan, Hongxia Wang and Peng Zhang

x Contents

19 Genetically Modified Crops with Drought Tolerance:Achievements, Challenges, and Perspectives . . . . . . . . . . . . . . . . . 531Chanjuan Liang

20 Present Status and Future Prospects of Transgenic Approachesfor Drought Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549Yan Xue, Shiu-Cheung Lung and Mee-Len Chye

21 Drought Stress and Chromatin: An Epigenetic Perspective . . . . . . 571Asif Khan and Gaurav Zinta

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 587

Contents xi

Contributors

Monika Agacka-Mołdoch Department of Plant Breeding and Biotechnology,Institute of Soil Science and Plant Cultivation—State Research Institute, Puławy,Poland

André M. Almeida Ross University School of Veterinary Medicine, Basseterre,Saint Kitts and Nevis

Carla Antonio Plant Metabolomics Laboratory, Instituto de Tecnologia QuímicaE Biológica António Xavier-Universidade Nova de Lisboa (ITQB NOVA), Oeiras,Portugal

Susana de Sousa Araújo Plant Cell Biotechnology Laboratory, Instituto deTecnologia Química e Biológica (ITQB NOVA) - Universidade Nova de Lisboa,Oeiras, Portugal; Plant Biotechnology Laboratory, Department of Biology andBiotechnology ‘L. Spallanzani’, Università Degli Studi Di Pavia, Pavia, Italy

Lidiane L. Barbosa Amorim Department of Genetics, Laboratory of PlantGenetics and Biotechnology, Universidade Federal de Pernambuco, Recife, PE,Brazil; Federal Institute of Education, Science and Technology of Piauí, Oeiras, PI,Brazil

Giorgia Batelli National Research Council of Italy, Institute of Biosciences andBioresources, Research Division Portici (CNR-IBBR), Portici, NA, Italy

Ana Maria Benko-Iseppon Department of Genetics, Laboratory of Plant Geneticsand Biotechnology, Federal University of Pernambuco, Recife, PE, Brazil

João Pacífico Bezerra-Neto Department of Genetics, Laboratory of PlantGenetics and Biotechnology, Universidade Federal de Pernambuco, Recife, PE,Brazil

Diana Branco Plant Cell Biotechnology Laboratory, Instituto de TecnologiaQuímica e Biológica (ITQB NOVA)—Universidade Nova de Lisboa, Oeiras,Portugal

xiii

Mee-Len Chye School of Biological Sciences, The University of Hong Kong,Pokfulam, Hong Kong, China

Antonello Costa National Research Council of Italy, Institute of Biosciences andBioresources, Research Division Portici (CNR-IBBR), Portici, NA, Italy

Anna Czubacka Department of Plant Breeding and Biotechnology, Institute ofSoil Science and Plant Cultivation—State Research Institute, Puławy, Poland

José Ribamar Costa da Ferreira Neto Department of Genetics, Laboratory ofPlant Genetics and Biotechnology, Universidade Federal de Pernambuco, Recife,PE, Brazil

Rômulo da Fonseca do Santos Department of Genetics, Laboratory of PlantGenetics and Biotechnology, Universidade Federal de Pernambuco, Recife, PE,Brazil

Agata Daszkowska-Golec Department of Genetics, Faculty of Biology andEnvironmental Protection, University of Silesia, Katowice, Poland

Amanda Cordeiro de Melo Souza Department of Genetics, Federal University ofPernambuco, Recife, PE, Brazil

Cláudia Regina Batista de Souza Instituto de Ciências Biológicas, UniversidadeFederal do Pará, Belém, PA, Brazil

Sávio Pinho dos Reis Instituto de Ciências Biológicas, Universidade Federal doPará, Belém, PA, Brazil; Universidade do Estado do Pará, Marabá, PA, Brazil

Weijuan Fan National Key Laboratory of Plant Molecular Genetics, CAS Centerfor Excellence in Molecular Plant Sciences, Institute of Plant Physiology andEcology, Shanghai Institutes for Biological Sciences, Chinese Academy ofSciences, Shanghai, China

Stefania Grillo National Research Council of Italy, Institute of Biosciences andBioresources, Research Division Portici (CNR-IBBR), Portici, NA, Italy

Mohammad Taher Hallajian Nuclear Agriculture Research School, NuclearScience and Technology Research Institute, Karaj, Iran

Amal Harb Department of Biological Sciences, Yarmouk University, Irbid,Jordan

Mohammad Anwar Hossain Department of Genetics and Plant Breeding,Bangladesh Agricultural University, Mymensingh, Bangladesh

Tiago F. Jorge Plant Metabolomics Laboratory, Instituto de Tecnologia QuímicaE Biológica António Xavier-Universidade Nova de Lisboa (ITQB NOVA), Oeiras,Portugal

Asif Khan Germline Biology Group, Centre for Organismal Studies(COS) Heidelberg, University of Heidelberg, Heidelberg, Germany

xiv Contributors

Éderson Akio Kido Department of Genetics, Laboratory of Plant Genetics andBiotechnology, Universidade Federal de Pernambuco, Recife, PE, Brazil

Shoshi Kikuchi Plant Genome Research Unit, Agrogenomics Research Center,National Institute of Agrobiological Sciences (NIAS), Tsukuba, Ibaraki, Japan

Klára Kosová Laboratory of Plant Stress Biology and Biotechnology, Division ofCrop Genetics and Breeding, Crop Research Institute, Ruzyně, Czech Republic

Karin Köhl Max Planck Institute of Molecular Plant Physiology, Potsdam,Germany

Simone Landi National Research Council of Italy, Institute of Biosciences andBioresources, Research Division Portici (CNR-IBBR), Portici, NA, Italy

Chanjuan Liang Jiangsu Key Laboratory of Anaerobic Biotechnology, School ofEnvironmental and Civil Engineering, Jiangnan University, Wuxi, China

Aline Medeiros Lima Instituto de Ciências Biológicas, Universidade Federal doPará, Belém, PA, Brazil; Programa de Pós-Graduação em Agronomia, UniversidadeFederal Rural da Amazônia, Belém, PA, Brazil

Shiu-Cheung Lung School of Biological Sciences, The University of Hong Kong,Pokfulam, Hong Kong, China

Deyvid Novaes Marques Instituto de Ciências Biológicas, Universidade Federaldo Pará, Belém, PA, Brazil; Programa de Pós-Graduação em Genética e BiologiaMolecular, Universidade Federal do Pará, Belém, PA, Brazil

Ana T. Mata Plant Metabolomics Laboratory, Instituto de Tecnologia Química EBiológica António Xavier-Universidade Nova de Lisboa (ITQB NOVA), Oeiras,Portugal

Mitalle Matos Department of Genetics, Laboratory of Plant Genetics andBiotechnology, Universidade Federal de Pernambuco, Recife, PE, Brazil

Ali Moumeni Rice Research Institute of Iran, Mazandaran Branch, AgriculturalResearch, Education and Extension Organization (AREEO), Amol, Mazandaran,Iran

Karaba Nalkur Nataraja Department of Crop Physiology, University ofAgricultural Sciences, Gandhi Krishi Vigyan Kendra, Bengaluru, India

Fen Ning State Key Laboratory of Wheat and Maize Crop Science, CollaborativeInnovation Center of Henan Grain Crops, College of Life Science, HenanAgricultural University, Zhengzhou, China

Jorge A.P. Paiva Department of Integrative Plant Biology, Institute of PlantGenetics, Polish Academy of Sciences, Poznan, Poland

Valesca Pandolfi Department of Genetics, Federal University of Pernambuco,Recife, PE, Brazil

Contributors xv

José Ricardo Parreira Plant Cell Biotechnology Laboratory, Instituto deTecnologia Química e Biológica (ITQB NOVA) - Universidade Nova de Lisboa,Oeiras, Portugal

Madathil Sreekumar Parvathi Department of Crop Physiology, University ofAgricultural Sciences, Gandhi Krishi Vigyan Kendra, Bengaluru, India

Marcel V. Pires Plant Metabolomics Laboratory, Instituto de Tecnologia QuímicaE Biológica António Xavier-Universidade Nova de Lisboa (ITQB NOVA), Oeiras,Portugal

Ilja Tom Prášil Laboratory of Plant Stress Biology and Biotechnology, Divisionof Crop Genetics and Breeding, Crop Research Institute, Ruzyně, Czech Republic

Paola Punzo National Research Council of Italy, Institute of Biosciences andBioresources, Research Division Portici (CNR-IBBR), Portici, NA, Italy

Alessandra Ruggiero National Research Council of Italy, Institute of Biosciencesand Bioresources, Research Division Portici (CNR-IBBR), Portici, NA, Italy

Nezar H. Samarah Department of Plant Production, Jordan University of Scienceand Technology, Irbid, Jordan

Bu-Jun Shi School of Agriculture, Food and Wine, The University of Adelaide,Urrbrae, SA, Australia

Filipe Tavares-Cadete Okinawa Institute of Science and Technology GraduateUniversity, Onna, Okinawa, Japan

Chandrama Prakash Upadhyaya Department of Biotechnology, DR HarisinghGour Central University, Sagar, Madhya Pradesh, India

Michael James Van Oosten Department of Agriculture, University of Naples“Federico II”, Portici, NA, Italy

Milan Oldřich Urban Laboratory of Plant Stress Biology and Biotechnology,Division of Crop Genetics and Breeding, Crop Research Institute, Ruzyně, CzechRepublic

Pavel Vítámvás Laboratory of Plant Stress Biology and Biotechnology, Divisionof Crop Genetics and Breeding, Crop Research Institute, Ruzyně, Czech Republic

Hongxia Wang National Key Laboratory of Plant Molecular Genetics, CASCenter for Excellence in Molecular Plant Sciences, Institute of Plant Physiologyand Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy ofSciences, Shanghai, China

Wei Wang State Key Laboratory of Wheat and Maize Crop Science, CollaborativeInnovation Center of Henan Grain Crops, College of Life Science, HenanAgricultural University, Zhengzhou, China

xvi Contributors

Yan Xue School of Biological Sciences, The University of Hong Kong, Pokfulam,Hong Kong, China

Peng Zhang National Key Laboratory of Plant Molecular Genetics, CAS Centerfor Excellence in Molecular Plant Sciences, Institute of Plant Physiology andEcology, Shanghai Institutes for Biological Sciences, Chinese Academy ofSciences, Shanghai, China

Gaurav Zinta Department of Biology, University of Antwerp, Wilrijk, Belgium;Shanghai Centre for Plant Stress Biology, Shanghai Institutes of BiologicalSciences, Shanghai, China

Contributors xvii

About the Editors

Dr. Mohammad Anwar Hossain is a professor in the Department of Genetics andPlant Breeding, Bangladesh Agricultural University, Mymensingh-2202,Bangladesh. He received his B.Sc. in agriculture and M.S. in genetics and plantbreeding from Bangladesh Agricultural University, Bangladesh. He also received anM.Sc. in agriculture from Kagawa University, Japan, in 2008 and a Ph.D. in abioticstress physiology and molecular biology from Ehime University, Japan, in 2011. InNovember 2015 he moved to Tokyo University, Japan, as a JSPS postdoctoralscientist to work on isolating low phosphorus stress tolerant genes/QTLs from rice.He has published 25 research articles, 15 book chapters, and 5 review articles onimportant aspects of plant physiology and breeding, plant stress responses and tol-erance mechanisms, and exogenous chemical priming-induced abiotic stress toler-ance. Recently, he edited a book entitled Managing Salt Tolerance in Plants:Molecular and Genomic Perspectives published by CRC press, Taylor and FrancisGroup, USA. He has attended several international and national conferences forpresenting his research findings. He is a professional member of the BangladeshSociety of Genetics and Plant Breeding, Bangladesh Association for Plant TissueCulture and Biotechnology, and the Seed Science Society of Bangladesh.

xix

Dr. Shabir Hussain Wani is an assistant professor in the Division of Genetics andPlant Breeding, Faculty of Agriculture, Wadura, Sher-e-Kashmir University ofAgricultural Sciences and Technology of Kashmir, India. He received his B.Sc. inagriculture from BhimRao Agricultural University Agra, India, and M.Sc. ingenetics and plant breeding from Central Agricultural University, Manipur, India,and Ph.D. in plant breeding and genetics on “transgenic rice for abiotic stresstolerance” from the Punjab Agricultural University Ludhiana, India. After obtaininghis Ph.D. he worked as research associate in the Biotechnology Laboratory, CentralInstitute of Temperate Horticulture (ICAR), Rangreth, Srinagar, India, for 2 years,up to October 2011. In November 2011 he joined the Krishi Vigyan Kendra (FarmScience Centre) as program coordinator (i/c) at Senapati, Manipur, India. He tea-ches courses related to plant breeding, seed science and technology, and stressbreeding and has published more than 80 papers/chapters in journals and books ofinternational and national repute. He has also edited several books on current topicsin crop improvement including Managing Salt Tolerance in Plants: Molecular andGenomic Perspectives published by CRC press, Taylor and Francis Group, USA, in2015. His Ph.D. research won first prize in the North Zone Competition, at nationallevel, in India. He was awarded a Young Scientist Award from the Society forPromotion of Plant Sciences, Jaipur, India, in 2009. He is a fellow of the Society forPlant Research, India. Recently he also received Young Scientist Award(Agriculture) 2015 from Society for Plant Research, Meerut, India. He has beenselected for one year University Grants Commission funded RAMAN fellowshipfor Post Doc Research in Michigan State University USA for the year 2016-17. Hehas attended several international and national conferences, presenting his research.

xx About the Editors

Dr. Soumen Bhattacharjee is presently professor and head of UGC Centre forAdvanced Studies, Department of Botany, the University of Burdwan, WestBengal. He completed his master’s in botany and Ph.D. on the abiotic stressphysiology of plants at the University of Burdwan, West Bengal, India. Later, hestarted his teaching career as a faculty member in the Department of Botany inDelhi University Constituent College. After serving almost two and a half years, hejoined the West Bengal Education Service and worked mainly in the Post GraduateDepartment of Botany, Hooghly Mohsin College, West Bengal, as lecturer, reader,and associate professor. In 2007, Dr. Bhattacharjee was selected by the IndianCouncil of Agricultural Research (ICAR) as a senior scientist and joined theVivekananda Institute of Hill Agriculture, Almora, India. In 2013 he joined theUniversity of Burdwan as associate professor. His research interests center aroundplant redox biology, particularly understanding the relationship between oxidativestress and plant growth, and the role of ROS signaling in stress acclimation,characterization of redox-regulatory mechanisms during germination of rice underabiotic stress, and understanding the physiological basis of antioxidant accumula-tion in underutilized medicinal plants. He has published 34 research papers ininternational peer-reviewed journals, 12 review articles in various national andinternational journals, and 14 book chapters and has 6 edited books and journalvolumes. He is also a member of several professional research bodies and is a guesteditor and reviewer for several international peer-reviewed journals.

About the Editors xxi

Dr. David J. Burritt is an associate professor in the Department of Botany, theUniversity of Otago, Dunedin, New Zealand. He received his B.Sc. and M.Sc.(Hons.) in botany and his Ph.D. in plant biotechnology from the University ofCanterbury, Christchurch, New Zealand. His research interests include oxidativestress and redox biology, plant-based foods and bioactive molecules, plant breedingand biotechnology, cryopreservation of germplasm, and the stress biology of plants,animals, and algae. He has over 90 peer-reviewed publications.

Dr. Lam-Son Phan Tran is head of the Signaling Pathway Research Unit atRIKEN Center for Sustainable Resource Science, Japan. He obtained his M.Sc. inbiotechnology in 1994 and Ph.D. in biological sciences in 1997, from Szent IstvanUniversity, Hungary. After doing his postdoctoral research at the National FoodResearch Institute (1999–2000) and the Nara Institute of Science and Technologyof Japan (2001), in October 2001, he joined the Japan International Research Centerfor Agricultural Sciences to work on the functional analysis of transcription factorsand osmosensors in Arabidopsis plants under stress. In August 2007, he moved tothe University of Missouri–Columbia, USA, as a senior research scientist tocoordinate a research team working to discover soybean genes to be used for

xxii About the Editors

genetic engineering of drought-tolerant soybean plants. His current research inter-ests are elucidation of the roles of phytohormones and their interactions in abioticstress responses, as well as translational genomics of legume crops with the aim toenhance crop productivity under adverse environmental conditions. He has pub-lished over 90 peer-reviewed papers with more than 70 research and 20 reviewarticles, contributed 7 book chapters to various book editions published bySpringer, Wiley-Blackwell, American Society of Agronomy, Crop Science Societyof America, and Soil Science Society of America. He has also edited 5 bookvolumes for Springer, including this one.

About the Editors xxiii

Chapter 1Understanding How Plants Respondto Drought Stress at the Molecularand Whole Plant Levels

Nezar H. Samarah

Abbreviations

A Photosynthetic rateABA Abscisic acidABFs ABRE- binding factorsABRE ABA-responsive elementACC 1-aminocyclopropane-1-carboxylic acidAP2 APETALA 2APX Ascorbate peroxidaseAREB ABRE-binding proteinAsA Reduced ascorbateASH Ascorbic acidbZIP Two basic leucine zipper transcription factorsCAT CatalaseCBF CRT binding factorCRT C-repeatDA Drought avoidanceDAG-PP Diacylglycerol-pyrophosphateDE Drought escapeDehydrin Dehydration-inducedDHAR Dehydroascorbate reductaseDRE Dehydration-responsive elementDREB DRE-binding proteinDT Drought toleranceE Transpiration rateERF Ethylene-responsive element binding factorETC Electron transport chainEUW Effective use of waterGOPX Guaicol peroxidase

N.H. Samarah (&)Department of Plant Production, Jordan University of Science and Technology,P.O. Box 3030, Irbid 22110, Jordane-mail: nsamarah@just.edu.jo

© Springer International Publishing Switzerland 2016M.A. Hossain et al. (eds.), Drought Stress Tolerance in Plants, Vol 2,DOI 10.1007/978-3-319-32423-4_1

1

GPX Glutathione peroxidaseGR Glutathione reductaseGSH GlutathioneGST Glutathione-S- transferaseH2O2 Hydrogen peroxideHI Harvest indexLEA Late embryogenesis proteinsLOX1 Lipoxygenase 1LWP Leaf water potentialMAPK Mitogen-activated protein kinaseMDA MalondialdehydeMDAR Monodehydroascorbate reductaseMDHAR Monodehydroascorbate reductaseNAC NAM, ATAF, CUCNACR NAC recognition sequenceNO Nitric oxideO2�− Superoxide anion

1O2 Singlet oxygenOA Osmotic adjustment.OH Hydroxyl radicalsP5CS Delta (1)-pyrroline-5-carboxylate synthetasePA Phosphatidic acidPCK Phosphoenolpyruvate carboxylasePEG Polyethylene glycolPLD Phospholipase DPOD PeroxidasePP2C 2C-type protein phosphatasePPDK Pyruvate orthophosphate dikinasePSI Photosystem IPSII Photosystem IIPYL Pyrabactin-resistance likePYR Pyrabactin resistanceQTL Quantitative trait locusRAB Response to ABARCAB Regulatory component of ABA receptorROS Reactive oxygen speciesRubisco Ribulose 1,5 bisphosphate carboxylase/oxygenaseRuBP Ribulose 1,5 bisphosphateSnRK2 Sucrose non-fermenting 1-related protein kinaseSOD Superoxide dismutaseWUE Water use efficiency

2 N.H. Samarah

1.1 Introduction

With climate change and abnormal weather events, more frequent drought and otherstresses such as heat and salinity are likely to occur all over the world [169, 185,229]. Drought stress reduces plant growth and crop production [40, 90].

Drought stress induces a range of morphological, physiological, biochemical,and molecular changes in plants [178]. Plant growth (leaf expansion and size, leafarea index, plant height, plant branching, and plant tiller numbers) has been reducedwhen drought stress was imposed on plants during vegetative growth stages [92].Under severe drought stress, plants senesce their leaves to reduce transpiration rateand water consumption [8, 165]. Drought has been reported to enhance plantgrowth and development, shorten the duration of the seed filling period, andremobilize the reserves in plant parts to growing seeds, resulting in a great reductionin the duration of the photosynthetic capacity of plants and lowering seed yield[34, 77, 198].

At the physiological and biochemical level, drought stress induces stomatalclosure and consequently decreases photosynthetic rate, stomatal conductance, andtranspiration rate [54, 121, 154]. Drought also inhibits the biochemistry of photo-synthesis [141, 214]. Soluble solutes accumulate in plants under drought stress tomaintain plant turgor pressure at a lower leaf water potential (LWP) in a processknown as an osmotic adjustment (OA) [56, 208]. Production of reactive oxygenspecies (ROS) under drought stress can cause oxidative damages to lipids, cellnucleic acid, and proteins [22, 106]. Plants respond to the increase in ROS byproducing nonenzymatic antioxidants or enzymatic defense (detoxification andscavenging enzymes) to prevent or reduce the oxidative damages of the ROS underdrought stress [10, 106, 122, 132, 161, 240]. Protein synthesis is also changed inresponse to drought. Dehydrin proteins (Class II of LEA proteins) are induced inresponse to drought stress and have been shown to function in drought tolerance(DT) [38, 94, 123].

Plants also respond to drought at the molecular level. Drought stress induces theaccumulation of ABA [131]. Drought stress and ABA induce drought-responsiveand ABA-responsive genes mediated through ABA-independent andABA-dependent regulatory pathways [23, 41, 211]. Other important signalingtransduction pathways mediate drought-related gene expression such as strigolac-tone hormone [118], ROS [15, 113], lipid derived signaling [113, 167], solublesugars, and others [55, 99]. Transcription factors such as ABREB/ABF,DREB1/CBF, DREB2, and NAC play an important role in the regulatory networkof drought-related genes [169]. The drought-inducible genes include genesencoding important functional and regulatory proteins [189, 211, 212]. Geneticallyengineering plants to express the drought-inducible genes has shown drought stresstolerance and can be a promising tool to improve DT in plants [138, 229, 238].

Development of crops for enhanced drought resistance requires knowledge ofmorphological and physiological responses and genetic control of the contributingtraits at different plant developmental stages [92]. This chapter summarizes

1 Understanding How Plants Respond to Drought Stress … 3

whole plant growth and yield performance under drought to understand plant DTat the physiological and molecular levels. Understanding plant responses to droughtat the morphological, physiological, and molecular levels and how these changesameliorate the effect of drought stress on plant productivity is needed to improveplant stress tolerance using biotechnology, while maintaining the yield and qualityof crop [28, 178]. Using a genetic engineering approach to produce transgenicplants by transferring a specific drought-related gene can improve DT in plants.

1.2 Drought Resistance and Adaptation Mechanisms

Drought resistance is a broad term applied to both wild species and crop plants withadapted traits that enable them to cope with water shortage [19]. Drought resistancemechanisms in plants have been classified into: (1) drought escape (DE) (the abilityof plants to complete their life cycle in the presence of water before the onset ofdrought stress); (2) drought avoidance (DA) (the ability of plants to maintain tissuehydrated; DT at high water potential); (3) DT (the ability of plants to function whiledehydrated; DT at low water potential; desiccation tolerance) [90, 220]. Plants thatescape drought, such as desert ephemerals, annual crops, and pasture plants, exhibitearlier flowering, shorter plant life cycle, and developmental plasticity [20, 210].Brassica rapa plants escape drought through early flowering rather than avoiddrought through increased water-use efficiency [100]. B. rapa plants grown fromseeds collected from natural populations after five consecutive years of drought hadan evolutionary shift to a DE mechanism in which plants had an earlier flowering[100]. This mechanism of DE was related to lower water-use efficiency (hightranspiration and inefficient water use), leading to rapid development and shortenedgrowing season [100]. With respect to the DA mechanism, plants have twoimportant strategies: enhancing water uptake from soil (roots traits); and reducingwater loss from plants (stomatal characteristics and morph-anatomical traits such asleaf rolling, dense leaf pubescence, thick cuticle and epicuticular wax layer, heavilylignified tissue, smaller mesophyll cell and less intercellular spaces, reduced plantgrowth, and leaf senescence) [20]. Root growth rate, root volume, root depth, androot dry weight are traits related to DA [237]. In the third mechanism of plantresistance to drought (DT), plants can tolerate drought through OA, antioxidantdefense mechanisms, dehydrins and late embryogenesis abundant (LEA) proteins,ABA response, desiccation tolerance [237], and water-use efficiency [measured asphotosynthetic carbon gain (A) over transpiration water loss (stomatal conductance,g)] [20, 100]. Two water use strategies may be employed by woody plants: prodigalwater use behavior (beneficial in a short interruption of water supply), and con-servative water use behavior (beneficial in a long-term drought) [20]. In the firststrategy (prodigal water use), plants had a high stomatal conductance, high carbonexchange rate, low water use efficiency, and plants grow faster [20]. In the sec-ond strategy (conservative water use), plants have higher water use efficiency,high capacity for drought resistance, and slow growth rate [20]. Thus higher

4 N.H. Samarah

drought resistance is sometimes linked to even or lower water use efficiency;however, in other cases, higher drought resistance is associated with high water useefficiency, indicating that drought resistance and water use efficiency are not syn-onymous terms [20]. It is impossible to assess the relative contributions of DE, DA,and DT to overall drought resistance at the whole-plant level in rice [237]. DT andDA traits had a distinct genetic basis [237]. The genetic variation in DE andavoidance in natural herbaceous populations is complex and controlled by manyquantitative trait loci (QTL) of small effect, and gene � environment interactions,indicating genetic constraints limit the concurrent evolution of both DE andavoidance strategies [136].

In arid and semiarid regions where rainfall occurs during winter and spring andno rainfall during summer (dry condition), plants use different drought resistantmechanisms to cope with drought stress in these regions. In the DE mechanism,rapid phenological development of plants ensures that flowering and grain fillingoccur before the onset of water shortage and high temperature, which prematurelyterminate the plant life cycle and reduce yield. Improved reproductive success byDE also includes better partitioning of assimilates and stored reserves from stemand root to developing fruits and seeds [20]. The acceleration of maturity (phe-nological adjustment), coupled with a high seed filling rate (shoot biomass distri-bution), reduced the negative effect of drought stress in the drought-resistantcommon bean cultivars (Phaseolus vulgaris L.) [196]. Despite the advantage of DEduring the water shortage seasons, DE limits yield in years with plentiful rainfall.Other drought resistant mechanisms in arid and semiarid regions including an earlyvigor, a greater number of fertile flowers, a longer duration of seed growth, anincreased harvest index (HI), an OA, a high assimilate transfer to the seed, a rapidgrain growth, and high water-use efficiency have been shown to improve cerealyield in these water-limited regions [16, 19]. The ability of plants to save water andretain some residual soil moisture to the end of the season may also contribute tobetter yield [19]. In a Mediterranean legume crop such as lupine (Lupinus luteusL.), contrasting adaptive strategies to terminal drought-stress have been reported.Long-season, high-rainfall habitats select for traits (competitive traits) that arerelated to delayed phenology, high biomass, and productivity, leading to high wateruse and early stress onset, whereas terminal drought-prone environments select forthe opposite traits (ruderal traits) that facilitate DE/avoidance but limit reproductivepotential [30].

In subhumid regions where rainfall occurs during summer, the ability of summercrops to develop a rapid growth and flowering over an extended period (indeter-minate growth habit) may reduce their vulnerability to drought stress compared withcrops that set their flowering at a specific period (determinate growth habit).Indeterminate cultivars of soybean were better able to recover from water stressimposed preflowering and during early pod development and had greater seed yieldafter recovery from stress treatment than were determinate ones [228]. This increasein the yield of the indeterminate cultivars was associated with more pods per noderather than with other yield components, or with leaf area index or leaf area durationdifferences [228]. The indeterminate cultivars of cotton (Gossypium hirsutum L.)

1 Understanding How Plants Respond to Drought Stress … 5

had higher lint yields and irrigation water-use efficiency than did the determinatecultivars at the intermediate moisture level, suggesting that cotton cultivars withrelatively indeterminate growth habit are better adapted to environments with limitedsoil moisture than cotton cultivars with relatively determinate growth habit [188].

1.2.1 Morphological Adaptation

An early response to drought stress is a reduction in plant growth. Plant growth isan irreversible process including cell division, cell elongation, and differentiation.Leaf elongation occurs as a balance among cell turgor pressure, cell wall threshold,and cell wall extensibility [220]. Under drought stress, cell turgor is less than cellwall threshold, which results in a reduction in leaf elongation and size and aretardation of plant growth [220]. Drought stress reduces leaf size, stem extension,and root proliferation [92]. Impaired enzyme activities, loss of turgor, anddecreased energy supply under drought stress results in a reduction in both celldivision and elongation [93, 220]. Loss of turgor under drought decreased growthand productivity of sunflower (Heliantus annuus L.) due to reductions in LWP, rateof cell division, and elongation [129]. Drought significantly reduced shoot and rootdry weights in Asian red sage (Salvia miltiorrhiza L.), but the shoots were moreaffected than roots [147]. Although severe drought stress terminated root growthearlier and significantly decreased the rate of root growth as a result of inhibition ofboth cell elongation and cell production in a Sonoran desert cactus (Pachycereuspringlei, Cactaceae), the total number of lateral roots and primordia was the sameunder severe and well-watered conditions [81]. These results indicated that lateralroot formation is a stable developmental process resistant to severe water stress andthat water stress accelerates the determinate developmental program of the primaryroot, which are two important features for successful seedling establishment in adesert [81].

Another plant response to drought stress is leaf senescence and abscission [8]which is also an important factor in determining seed yield. Leaf senescence,mediated by enhancing the synthesis of endogenous plant hormone ethylene underdrought stress [9, 12], determines the duration of photosynthesis and the seed fillingperiod [13]. When drought stress occurred during late reproductive growth, leafsenescence was accelerated [67, 165]. Although leaf senescence under drought canbe an adaptive mechanism to drought by reducing plant water consumption, leafsenescence reduces plant yield under drought.

Pandey et al. [182] reported that the increase in drought intensity decreasedgrowth parameters such as leaf area index, leaf area duration, crop growth rate, andshoot dry matter of grain legumes. The reduction in leaf area under drought was dueto the loss of turgor and reduced leaf number [91]. Seed yield of grain legumes waspositively correlated with leaf area index, leaf area duration, crop growth rate, andshoot dry matter [182]. Black bean (Phaseolus vulgaris L.) exposed to water stressduring vegetative growth had lower plant height and leaf area index than did

6 N.H. Samarah

well-watered plants [173]. Dry conditions resulted in 68 % reduction in leaf areaindex of soybean plants compared to irrigated conditions [70]. Drought decreasedleaf expansion, tiller formation, and leaf area due to early senescence [129, 137,175]. This reduction in leaf expansion and growth can be a way to adapt to droughtby reducing plant water consumption (plant survival), but the reduction in plantgrowth under drought is related to the reduction in seed yield.

Drought stress has been reported to reduce seed yield and yield components andthe intensity of this reduction depends on the growth stage at which drought occurs,showing that plants are most susceptible to water stress at the reproductive growthstage [198]. Drought stress imposed on soybean during vegetative growthdecreased internode length and plant height [76]. When drought occurred duringvegetative stages of rice, drought had only a small effect on subsequent plantdevelopment and grain yield, resulting in up to 30 % reduction in yield due toreduced panicle number per unit area or reduced number of spikelets per panicle[34]. Drought stress early during the reproductive stage can delay or inhibit flow-ering. In most studied species, the most stress-sensitive reproductive stage is thestage of meiosis [198]. In the mitotic stage of flowering, drought causes pollensterility and only affects female fertility when stress is severe [14, 198]. Whendrought stress was imposed during the reproductive growth stage of wheat, pollenfertility was most affected [187]. The most sensitive stage of wheat yield to droughtstress is in the early spikelet development (5 d after jointing) [187]. The rice andmaize plants are highly susceptible to drought during flowering (anthesis) and earlygrain initiation, causing pollen sterility, failure of pollination, spikelet death, andzygotic abortion due to changes in carbohydrate availability and metabolism [172,198]. Drought stress conditions modify source-sink relations by inducing prematuresenescence in the photosynthetic source tissues of the plant, by reducing the numberand growth of the harvestable sink organs, and by affecting the transport and use ofassimilates, thereby influencing plant growth, adaptive responses, and consequentlycrop yield [12, 13]. Drought stress strongly reduced the cell wall invertases (cwInv)activities, key metabolic enzymes regulating sink activity through the hydrolyticcleavage of sucrose into hexose monomers [12]. The most sensitive stage todrought in rice was observed when stress occurred during panicle development [34,187], resulting in delayed anthesis, reduced number of spikelets per panicle,decreased percentage of filled grains, and consequently reducing grain yield to lessthan 20 % of the control (irrigated plants) [34]. Drought stress during podlengthening (R3–R5) of soybean decreased the number of pods per vegetative drymatter unit [76]. Drought stress during grain development and filling shortened thegrain filling period (prematurely terminated) and reduced seed size and weight[198]. Drought stress during early seed-fill of soybean [Glycine max (L.) Merr.]reduced the number of seeds per pod, whereas late stress during the seed fillingperiod (after the abortion limit stage) decreased seed weight [76]. Drought stressduring grain filling of rice hastened the plant maturity and reduced the percentage offilled grain and individual grain weight [34]. Genetic control of yield underreproductive-stage drought stress in rice showed that a QTL (qtl12.1) had a largeeffect on grain yield under stress, increased HI, biomass yield, and plant height

1 Understanding How Plants Respond to Drought Stress … 7

while reducing the number of days to flowering [31]. In barley, drought stressduring the grain filling period enhanced the grain growth rate, shortened the grainfilling duration, decreased grain yield by reducing the number of tillers, spikes, andgrains per plant, and individual grain weight, indicating that postanthesis droughtstress was detrimental to grain yield regardless of the stress severity [201, 202,205]. Late-terminal drought stress (rainfed) shortened reproductive growth durationand fastened maturity of chickpea plants, resulting in a decrease in seed yield by49–54 % compared with irrigated plants, indicating that drought during thereproductive growth stage was detrimental to all genotypes studied (desi andkabuli) [206]. Other researchers have shown that desi chickpea genotypes (smaller,dark seeds) were generally more drought and heat tolerant than kabuli chickpeagenotypes (larger, pale seeds) [44]. In muskmelon (Cucumis melo var. reticulatus)plants grown under three irrigation levels [0.5, 0.75, 1.0 actual evapotranspiration(AET)], decreasing the irrigation level decreased the length, diameter, weight, Brix,flesh firmness, seeds, and fertile seeds of melon fruit [11]. The best irrigation levelfor getting the highest total fruit yield was at 0.75 AET [11]. Drought stress duringreproductive stages reduces photosynthetic rate, assimilates partitioning toexpanding cells, which increases flower and pod abortion and decreases vegetativegrowth, duration of the seed filling stage, seed number, seed size, and consequentlydecreases total seed yield [127].

1.2.2 Physiological and Biochemical Adaptation

1.2.2.1 Controlling Guard Cell Behavior and Leaf Water Status

An early response of plants to drought stress is the closure of their stomata to preventtranspiration water loss and leaf dehydration [52, 54, 154], affecting all plant waterrelations. The stomata closure under drought stress can result from a decrease in leafturgor and water potential [152] or from low relative humidity of the atmosphere[156]. Under drought stress, stomata closure is considered as a first step to adapt todrought by maintaining cell turgor to continue plant metabolism [146] and to preventthe risk of losing its water transport capacity [133]. Drought stress decreased therelative leaf water content, the LWP, and the transpiration rate and concomitantlyincreased the leaf temperature in wheat and rice [92, 213]. Drought stress alsoreduced the relative leaf water content and transpiration rate in other crop speciessuch as barley, soybean, and triticale [146, 195]. The stomatal closure and thedecrease in stomatal conductance and transpiration rate under drought stress havebeen related to higher water-use efficiency (the ratio of dry matter produced to waterconsumed) in wheat [1], clover (Trifolium alexandrium) [143]), and alfalfa(Medicago sativa) [142]. Drought tolerant species improve the water-use efficiencyby controlling the stomatal function to allow carbon fixation at stress and reduce thewater loss [92, 236]. However, in the case of severe drought stress where plantgrowth and biomass accumulation are greatly diminished, the water-use efficiency is

8 N.H. Samarah

also reduced [69]. Most plants tend to show an increase in water-use efficiency whendrought stress is mild [54]. Although water-use efficiency is often considered animportant determinant of yield under stress and even as a component of crop droughtresistance, selection for high WUE in breeding for water-limited conditions mostlikely leads, under most conditions, to reduced yield and reduced drought resistance[33]. Because biomass production is closely linked to transpiration, breeding foreffective use of water (EUW; implies maximal soil moisture capture for transpira-tion, reduced nonstomatal transpiration, and minimal water loss by soil evaporation)is the most important target for yield improvement under drought stress byimproving plant water status and sustaining assimilate partitions and reproductivesuccess (HI) [33].

Stomatal closure is mediated by the plant hormone ABA [73, 163]. Biosynthesisof ABA is triggered by a decrease in soil water content and plant turgor [78].During soil drying, ABA is synthesized in the roots and transported by the xylem tothe shoot to inhibit leaf expansion and induce stomatal closure before the change inleaf water status [78, 114, 209]. ABA abundance in the xylem sap of field-growngrapevines was correlated with stomatal conductance [218]. The expression ofgenes associated with ABA synthesis (the 9-cis-epoxycarotenoid dioxygenase),NCED1 and NCED2, was higher in the roots than in the leaves, especially whensoil moisture declined and vapor pressure deficit increased [218]. Their expressionin roots was correlated with ABA abundance in the roots, xylem sap, and leaves[218]. The results provide evidence that ABA plays an important role in linkingstomatal response to soil moisture status [218].

Other hormones in addition to ABA are involved in the regulation of stomatalclosure. Increased cytokinin concentration in the xylem promoted stomatal openingby decreasing the stomatal sensitivity to ABA [230], whereas the decrease in theroot cytokinins was concomitant with the increase in xylem ABA and the reductionin stomatal conductance [219]. Plant hormones such as ABA, auxin, cytokinins,ethylene, and gibberellins have been shown to be involved in plant response todifferent environmental stresses [78, 209].

A hydraulic signaling also contributes to plant response to drought stress.Stomata respond to the rate of water loss from the leaf (evaporation demand), thechange in the rate of water supply from soil, the change in xylem conductance, andto the change in leaf turgor, which can be translated to a signal to regulate stomatalaperture [43, 59, 156, 170]. The decline in root water uptake and then waterpotential and turgor in the leaves can lead to stomatal closure and a decrease in leafelongation [43, 59].

1.2.2.2 Modulation of Photosynthetic Behavior Under Drought

Photosynthesis is another primary process to be inhibited by drought stress [52].The reduction in photosynthesis under drought can result directly from stomatal andnonstomatal limitation of photosynthesis, and/or indirectly as a result of oxidativestress [53, 105, 155] (Fig. 1.1). Studies have shown that stomatal limitations could

1 Understanding How Plants Respond to Drought Stress … 9