Plant Abiotic Stress || Frontmatter

Plant Abiotic Stress

Biological Sciences Series

A series which provides an accessible source of information at research and professionallevel in chosen sectors of the biological sciences.

Series Editor:Professor J. A. Roberts, Plant Science Division, School of Biosciences, University ofNottingham, UK.

Titles in the series:

Biology of Farmed Fish

Edited by K.D. Black and A.D. Pickering

Stress Physiology in Animals

Edited by P.H.M. Balm

Seed Technology and its Biological Basis

Edited by M. Black and J.D. Bewley

Leaf Development and Canopy Growth

Edited by B. Marshall and J.A. Roberts

Environmental Impacts of Aquaculture

Edited by K.D. Black

Herbicides and their Mechanisms of Action

Edited by A.H. Cobb and R.C. Kirkwood

The Plant Cell Cycle and its Interfaces

Edited by D. Francis

Meristematic Tissues in Plant Growth and Development

Edited by M.T. McManus and B.E. Veit

Fruit Quality and its Biological Basis

Edited by M. Knee

Pectins and their Manipulation

Edited by G. B. Seymour and J. P. Knox

Wood Quality and its Biological Basis

Edited by J.R. Barnett and G. Jeronimidis

Plant Molecular Breeding

Edited by H.J. Newbury

Biogeochemistry of Marine Systems

Edited by K.D. Black and G. Shimmield

Programmed Cell Death in Plants

Edited by J. Gray

Water Use Efficiency in Plant Biology

Edited by M.A. Bacon

Plant Lipids – Biology, Utilisation and Manipulation

Edited by D.J. Murphy

Plant Nutritional Genomics

Edited by M.R. Broadley and P.J. White


Edited by M.A. Jenks and P.M. Hasegawa


Edited by

MATTHEW A. JENKS

Center for Plant Environmental Stress PhysiologyPurdue UniversityIndiana, USA

and

PAUL M. HASEGAWA

Center for Plant Environmental Stress PhysiologyPurdue UniversityIndiana, USA

� 2005 by Blackwell Publishing Ltd

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First published 2005 by Blackwell Publishing Ltd

Library of Congress Cataloging-in-Publication Data

Plant abiotic stress / edited by Matthew A. Jenks and Paul M. Hasegawa.–1st ed.

p. cm.

Includes bibliographical references and index.

ISBN-10: 1-4051-2238-2 (hardback : alk. paper)

ISBN-13: 978-1-4051-2238-2 (hardback : alk. paper)

1. Crops–Effect of stress on. 2. Crops–Physiology. I. Jenks, Matthew A. II. Hasegawa, Paul M.

SB112.5.P5 2005

632’.1–dc222004025753

ISBN-10: 1-4051-2238-2

ISBN-13: 978-14051-2238-2

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Contents

Contributors xi

Preface xvi

1 Eco-physiological adaptations to limited water environments 1

ANDREW J. WOOD

1.1 Introduction 1

1.2 Limited water environments 2

1.2.1 Arid and semiarid regions of the world 2

1.2.2 Plant strategies for water economy 4

1.2.3 Ability to survive in water-limited environments 5

1.2.4 Surviving water-deficit (drought) and severe

water-deficit (desiccation) 6

1.3 Adaptation to limited water environments 7

1.3.1 Evolution of land plants 7

1.3.2 Tolerance to desiccation 10

1.4 Refresher of the world – how to create more drought-tolerant

crops 10

2 Plant cuticle function as a barrier to water loss 14

S. MARK GOODWIN and MATTHEW A. JENKS

2.1 Introduction 14

2.2 Cuticle structure and composition 14

2.3 Cuticle function as a barrier to plant water loss 18

2.4 Genetics of cuticle permeability 24

2.5 Conclusions 31

3 Plant adaptive responses to salinity stress 37

MIGUEL A. BOTELLA, ABEL ROSADO, RAY A. BRESSAN

and PAUL M. HASEGAWA

3.1 Salt stress effects on plant survival, growth and development 37

3.1.1 NaCl causes both ionic and osmotic stresses 38

3.1.2 Secondary effects of salt stress 38

3.2 Plant genetic models for dissection of salt tolerance

mechanisms and determinant function 39

3.2.1 Arabidopsis thaliana as a model for glycophyte

responses to salt stress 40

3.2.2 Thellungiella halophila (salt cress) – a halophyte

molecular genetic model 40

3.3 Plant adaptations to NaCl stress 41

3.3.1 Intracellular ion homeostatic processes 41

3.3.1.1 Naþ influx and efflux across the plasma

membrane 42

3.3.1.2 Naþ and Cl� compartmentalization into the

vacuole 42

3.3.1.3 Kþ=Naþ selective accumulation 44

3.3.2 Regulation of Naþ homeostasis in roots and shoots 44

3.3.3 Sensing and regulatory pathways that control ion

homeostasis 45

3.3.4 Osmotic homeostasis: compatible osmolytes 46

3.3.5 Damage response and antioxidant protection 46

3.4 Plant salt tolerance determinants identified by functional

genetic approaches 47

3.4.1 Effector genes 52

3.4.1.1 Naþ homeostasis 52

3.4.1.2 Genes involved in osmotic homeostasis:

synthesis of compatible solutes 54

3.4.1.3 Genes involved in ROS scavenging 54

3.4.1.4 Genes involved in protection of cell integrity 56

3.4.2 Regulatory genes 56

3.4.2.1 Kinases 56

3.4.2.2 Transcription factors 57

3.4.2.3 Other salt tolerance determinants 58

3.5 Global analysis of transcriptional activation of salt-responsive

genes 58

4 The CBF cold-response pathway 71

SARAH FOWLER, DANIEL COOK and

MICHAEL F. THOMASHOW

4.1 Introduction 71

4.2 Arabidopsis CBF cold-response pathway 72

4.2.1 Discovery and overview 72

4.2.2 CBF proteins 75

4.2.2.1 General properties 75

4.2.2.2 Mechanism of action 76

vi CONTENTS

4.2.3 Function of the CBF cold-response pathway 78

4.2.3.1 Cryoprotective proteins 79

4.2.3.2 Regulatory proteins 81

4.2.3.3 Biosynthetic proteins 82

4.2.4 Regulation of CBF gene expression in response

to low temperature 83

4.2.4.1 DNA regulatory elements controlling CBF

expression 84

4.2.4.2 Proteins with positive roles in CBF

expression 84

4.2.4.3 Proteins with negative roles in CBF expression 85

4.2.4.4 Other potential CBF regulatory proteins 87

4.2.4.5 Light and circadian rhythms 87

4.2.4.6 Role of calcium 88

4.2.4.7 Role of ABA 89

4.3 Conservation of the CBF cold-response pathway 89

4.3.1 Brassica napus 89

4.3.2 Tomato 90

4.3.3 Rice 92

4.4 Concluding remarks 93

5 Plant responses to high temperature 100

JANE LARKINDALE, MICHAEL MISHKIND and

ELIZABETH VIERLING

5.1 Introduction 100

5.2 Physiological responses to high temperature 101

5.2.1 High temperature limits to optimal plant performance 101

5.2.2 Heat sensitivity of photosynthesis 102

5.2.3 Heat sensitivity of reproduction 104

5.3 Cellular acquired thermotolerance 104

5.4 Heat shock proteins/molecular chaperones 105

5.4.1 Hsp100/ClpB 106

5.4.2 Hsp90 110

5.4.3 Hsp70/DnaK 111

5.4.4 Hsp60/GroE 111

5.4.5 The sHSP family of proteins 112

5.5 Other components of the response to heat 114

5.5.1 Antioxidant production 115

5.5.2 Other heat-stress regulated genes 118

5.5.3 Other heat-protective responses 120

5.5.4 Mutants defective in heat tolerance 121

5.5.5 Transgenic plants with altered heat tolerance 122

CONTENTS vii

5.6 Signaling pathways involved in response to heat 125

5.6.1 Heat shock transcription factors 125

5.6.2 Other signaling pathways 126

5.6.3 Abscisic acid 126

5.6.4 Salicylic acid 127

5.6.5 Calcium 127

5.6.6 Active oxygen species 128

5.6.7 Ethylene 128

5.6.8 Signaling lipids 129

5.6.9 Kinases and phosphatases 129

5.7 Genetic variation in heat tolerance 131

5.7.1 Agricultural/horticultural plants 131

5.7.2 Natural variation in heat tolerance 132

5.8 Summary 132

6 Adaptive responses in plants to nonoptimal soil pH 145

V. RAMIREZ-RODRIGUEZ, J. LOPEZ-BUCIO and

L. HERRERA-ESTRELLA


6.2 Soil pH 146

6.3 Soil acidification 146

6.4 Acid soils 147

6.5 Calcareous soils 148

6.6 Plant responses to soil stress 149

6.7 Plant responses to heavy metals 150

6.8 Aluminum tolerance by exclusion 150

6.9 Aluminum tolerance by internal accumulation 152

6.10 Metal hyperaccumulators 153

6.11 Plant responses to mineral deficiency 155

6.11.1 Phosphorus deficiency 155

6.11.2 Improving P efficiency in transgenic plants 156

6.11.3 Plant responses to iron deficiency 158

6.12 Morphological responses to mineral deficiency 161

6.12.1 Effects of iron availability on transfer cell formation 161

6.12.2 Effects of nutrient availability on root hair formation 162

6.12.3 Effects of nutrient availability on root branching 162

6.13 Functional genomics for the discovery of genes involved in

mineral nutrition 163

6.14 Application of functional genomics to iron and phosphorus

nutrition 164

viii CONTENTS

7 Plant response to herbicides 171

WILLIAM E. DYER and STEPHEN C. WELLER


7.2 Photosynthetic inhibitors 174

7.2.1 Resistance 176

7.3 Biosynthetic inhibitors 177

7.3.1 Branched-chain amino acid synthesis inhibitors 177

7.3.1.1 Resistance 179

7.3.2 Aromatic amino acid synthesis inhibitors 181


7.3.3 Fatty acid synthesis and elongation inhibitors 186


7.3.4 Cellulose synthesis inhibitors 190


7.3.5 Folic acid synthesis inhibitors 190


7.3.6 Nitrogen metabolism inhibitors 191


7.3.7 Quinone synthesis inhibitors 192


7.3.8 Carotenoid biosynthesis inhibitors 193


7.4 Induction of herbicide metabolism 194


7.5 Protoporphyrinogen oxidase inhibitors 196


7.6 Mitotic disruptors 197


7.7 Hormone disruptors 198


7.8 Genome effects 201

7.9 Summary and future prospects 202

8 Integration of abiotic stress signaling pathways 215

MANU AGARWAL and JIAN-KANG ZHU


8.1.1 Sensors 216

8.1.2 ROS 218

8.1.3 Calcium 220

8.1.4 Phospholipids 221

CONTENTS ix

8.1.5 SOS pathway 224

8.1.6 SOS3-like Ca2þ-binding proteins and SOS2-like

protein kinases 227

8.1.7 CDPKs 228

8.1.8 MAPKs 229

8.1.9 ICE1 pathway for cold regulation 230

8.2 Regulation of gene expression by ABA 234

8.3 Conclusions and perspectives 237

8.4 Summary 237

9 Genomic Analysis of Stress Response 248

MOTOAKI SEKI, JUNKO ISHIDA, MAIKO NAKAJIMA,

AKIKO ENJU, KEI IIDA, MASAKAZU SATOU,

MIKI FUJITA, YOSHIHIRO NARUSAKA, MARI NARUSAKA,

TETSUYA SAKURAI, KENJI AKIYAMA, YOUKO OONO,

AYAKO KAMEI, TAISHI UMEZAWA, SAHO MIZUKADO,

KYONOSHIN MARUYAMA, KAZUKO

YAMAGUCHI-SHINOZAKI and KAZUO SHINOZAKI


9.2 Expression profiling under stress conditions by cDNA

microarray analysis 248

9.3 DNA Microarrays are an excellent tool for identifying

genes regulated by various stresses 249

9.4 DNA microarrays are a useful tool for identifying the target

genes of the stress-related transcription factors 250

9.5 Expression profiling in various stress-related mutants 253

9.6 Rehydration- or proline-inducible genes and functions of

their gene products identified by RAFL cDNA microarray 254

9.7 Abiotic stress-inducible genes identified using microarrays

in monocots 255

9.8 Many stress- or hormone-inducible transcription factor genes

have been identified by the transcriptome analysis 256

9.8.1 7K RAFL cDNA microarray analysis 256

9.8.2 GeneChip analysis 257

9.9 Application of full-length cDNAs to structural and functional

analysis of plant proteins 258

9.10 Conclusions and perspectives 259

9.11 Summary 260

Index 266

x CONTENTS

Contributors

Manu Agarwal Department of Botany and Plant Sciences, 2150

Batchelor Hall, Institute for Integrative Genome

Biology, University of California, Riverside,

California 92521, USA

Kenji Akiyama Plant Mutation Exploration Team and Genomic

Knowledge Base Research Team, RIKEN Genomic

Sciences Center, Riken Yokohama Institute, 1-7-22

Suehiro-cho, Tsurumi-ku, Yokohama 230-0045,

Japan

Miguel A. Botella Dep. Biologıa Molecular y Bioquımica, Facultad de

Ciencias, Universidad de Malaga, Campus de

Teatinos s/n, Malaga, 29071 Spain

Ray A. Bressan Center for Plant Environmental Stress Physiology,

625 Agriculture Mall Drive, Purdue University, West

Lafayette, Indiana 47907–2010, USA

Daniel Cook MSU-DOE Plant Research Laboratory, Michigan

State University, East Lansing, MI 48824-1312, USA

William E. Dyer Department of Plant Sciences, Montana State

University, Bozeman, Montana 59717, USA

Akiko Enju Plant Mutation Exploration Team, Plant Functional

Genomics Research Group, RIKEN Genomic

Sciences Center (GSC), RIKEN Yokohama Institute,

1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama,

Kanagawa 230-0045, Japan

Sarah Fowler MSU-DOE Plant Research Laboratory, Michigan

State University, East Lansing, MI 48824-1312, USA

Miki Fujita CREST, Japan Science and Technology Corporation

(JST), Japan

S. Mark Goodwin Center for Plant Environmental Stress Physiology,



Paul M. Hasegawa Center for Plant Environmental Stress Physiology,



Luis Herrera-Estrella Director, Plant Biotechnology Unit, Centro de

Investigacion y Estudios Avanzados, Km 9.6 Carretera

Irapuato-Leon, 36500 Irapuato, Guanajuato, Mexico

Kei Iida Plant Mutation Exploration Team and Genomic

Knowledge Base Research Team RIKEN Genomic


Suehiro-cho, Tsurumi-ku, Yokohama 230-0045,

Japan

Ishida Ishida Plant Mutation Exploration Team, Plant Functional



1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama

230-0045, Japan

Junko Ishida Plant Mutation Exploration Team, Plant Functional





Matthew A. Jenks Center for Plant Environmental Stress Physiology,



Ayako Kamei Plant Mutation Exploration Team, Plant Functional




Kanagawa, 230-0045, Japan

xii CONTRIBUTORS

Jane Larkindale Life Sciences South Building, Room 352, University

of Arizona, P.O. Box 210106, Tucson, AZ 85721,

USA

J. Lopez-Bucio Plant Biotechnology Unit, Centro de Investigacion y

Estudios Avanzados, Km 9.6 Carretera Irapuato-Leon

36500, Irapuato, Guanajuato, Mexico

Nakajima Maiko Plant Mutation Exploration Team, Plant Functional





Kyonoshin Maruyama Biological Sciences Division, Japan International

Research Center for Agricultural Sciences (JIRCAS),

Ministry of Agriculture, Forestry and Fisheries, 2-1

Ohwashi, Tsukuba 305-0074, Japan

Michael Mishkind Life Sciences South Building, Room 352, University

of Arizona, P.O. Box 210106, Tucson, AZ 85721,

USA

Saho Mizukado CREST, Japan Science and Technology Corporation

(JST), Japan

Mari Narusaka Plant Mutation Exploration Team, Plant Functional





Youko Oono Laboratory of Plant Molecular Biology, RIKEN

Tsukuba Institute, 3-1-1 Koyadai, Tsukuba 305-0074,

Japan; Master’s Program in Biosystem Studies,

University of Tsukuba, Tennoudai, Tsukuba, Ibaraki,

305-0074, Japan

V. Ramırez-Rodrıguez Plant Biotechnology Unit, Centro de Investigacion y

Estudios Avanzados, Km 9.6 Carretera Irapuato-Leon

36500, Irapuato, Guanajuato, Mexico

CONTRIBUTORS xiii

Abel Rosado Dep. Biologıa Molecular y Bioquımica, Facultad de

Ciencias, Universidad de Malaga, Campus de

Teatinos s/n, Malaga, 29071 Spain

Tetsuya Sakurai Plant Mutation Exploration Team and Genomic



Suchiro-cho, Tsurumi-ku, Yokohama 230-0045, Japan

Masakazu Satou Plant Mutation Exploration Team and Genomic



Suchiro-cho, Tsurumi-ku, Yokohama 230-0045,

Japan

Motoaki Seki Plant Mutation Exploration Team, Plant Functional





Laboratory of Plant Molecular Biology, RIKEN

Tsukuba Institute, 3-1-1 Koyadai, Tsukuba Ibaraki

305-0074, Japan

Kazuo Shinozaki Plant Mutation Exploration Team, RIKEN Genomic


Suchiro-cho, Tsurumi-ku, Yokohama 230-0045,

Japan; Laboratory of Plant Molecular Biology,

RIKEN Tsukuba Institute, 3-1-1 Koyadai, Tsukuba

305-0074, Japan; CREST, Japan Science and

Technology Corporation (JST), Japan

Michael F. Thomashow MSU-DOE Plant Research Lab, 310 Plant Biology

Building, Michigan State University, East Lansing,

Michigan, USA

Taishi Umezawa Laboratory of Plant Molecular Biology, RIKEN

Tsukuba Institute, 3-1-1 Koyadai, Tsukuba 305-0074,

Japan

Elizabeth Vierling Department of Biochemistry & Molecular

Biophysics, University of Arizona, 1007 E. Lowell

Street, Tucson, Arizona 85721, USA

xiv CONTRIBUTORS

Stephen C. Weller Center for Plant Environmental Stress Physiology,


Lafayette, Indiana 47907-2010, USA

Andrew J. Wood Department of Plant Biology, Southern Illinois

University-Carbondale, Carbondale, IL 62901-6509,

USA

Kazuko

Yamaguchi-Shinozaki

CREST, Japan Science and Technology Corporation

(JST), Japan; Biological Sciences Division, Japan

International Research Center for Agricultural

Sciences (JIRCAS), Ministry of Agriculture, Forestry

and Fisheries, 2-1 Ohwashi, Tsukuba 305-0074, Japan

Jian-Kang Zhu Department of Botany and Plant Sciences, 2150

Batchelor Hall, Institute for Integrative Genome

Biology, University of California, Riverside, CA

92521, USA

CONTRIBUTORS xv

Preface

Over the past decade, our understanding of plant adaptation to environmentalstress, including both constitutive and inducible determinants, has grown con-siderably. This book focuses on stress caused by the inanimate components ofthe environment associated with climatic, edaphic and physiographic factorsthat substantially limit plant growth and survival. Categorically these are abioticstresses, which include drought, salinity, non-optimal temperatures and poorsoil nutrition. Another stress, herbicides, is covered in this book to highlighthow plants are impacted by abiotic stress originating from anthropogenicsources. Indeed, it is an important consideration that, to some degree, the impactof abiotic stress is influenced by human activities. The book also addresses thehigh degree to which plant responses to quite diverse forms of environmentalstress are interconnected. Thus the final two chapters uniquely describe theways in which the plant utilizes and integrates many common signals andsubsequent pathways to cope with less favorable conditions. The many linkagesbetween the diverse stress responses provide ample evidence that the environ-ment impacts plant growth and development in a very fundamental way.

The unquestionable importance of abiotic stress to world agriculture isdemonstrated by the fact that altogether abiotic factors provide the majorlimitation to crop production worldwide. For instance, Bray et al. (2000)estimates that 51–82% of the potential yield of annual crops is lost due toabiotic stress. Another example is the increasing use of aquifer-based irriga-tion by farmers worldwide, which poses a serious threat to the long-termsustainability of world agricultural systems. Over-utilization of these dwin-dling water supplies is leading to an ever-enlarging area in which productivefarming itself has ceased or is threatened. With increasing irrigation world-wide comes the threat of increased salinization of field soils and, just asaquifer loss is shrinking crop yield, so soil salinization due to irrigation has,and will increasingly, reduce crop production in many parts of the world.Another major limitation to expansion of the production of traditional fieldcrops is the problem of non-optimal temperatures, with conditions being eithertoo cold for efficient crop production in the far northern and southern regionsof the globe, or too warm in the more equatorial regions. Degradation of thesoil by various factors (including anthropogenic) is also increasingly limitingcrop yield, and so use of new crops with enhanced resistance to drought,

salinity, sub- and supra-optimal temperatures, poor soil nutrient status andanthropogenic factors would benefit agriculture globally by reducing the useof groundwater resources and expanding the productivity of crops on existingand new lands.

The advent of new technologies for the efficient identification of geneticdeterminants involved in plant stress adaptation, fostered especially by the useof molecular genetics and high throughput transcriptome, proteome, metabo-lome and ionome profiling methods, has opened a door to exciting newapproaches and applications for understanding the mechanisms by whichplants adapt to abiotic stress, and should ultimately result in the productionof new and improved stress-tolerant crops. This book seeks to summarize thelarge body of current knowledge about cellular and organismal mechanisms oftolerance to stress. Nine chapters written by leading scientists involved in plantabiotic stress research worldwide provide comprehensive coverage of themajor factors impacting world crop production. While modifications to theenvironment (like increasing use of irrigation, agrichemicals or cultivation) orthe expansion of farming into undisturbed lands poses an obvious risk tonatural ecosystems, simple genetic changes to crops offer a relatively safemeans of increasing yield at a minimal cost to the environment and the farmer.The material presented in this book emphasizes fundamental genetic, physio-logical, biochemical, and ecological knowledge of plant abiotic stress, whichmay lead to both traditional and biotechnological applications that result inimproved crop performance in stressful environments.

We, the editors, would like to give a special thanks to the authors for theiroutstanding and timely work in producing such fine chapters. We wouldalso like to thank Becky Fagan for her clerical assistance, and BlackwellPublishing’s Graeme MacKintosh and David McDade for their advice andencouragement during the development of this important book.

Matthew A. Jenks and Paul M. Hasegawa

Cited above: Bray, E.A., Bailey-Serres, J. and Weretilnyk, E. (2000) Re-sponses to abiotic stresses. In Biochemistry and Molecular Biology of Plants,B. Buchanan, W. Gruissem and R. Jones (eds), p 1160, American Society ofPlant Physiologists.

PREFACE xvii

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Plant Abiotic Stress || Frontmatter