Genes for Plant Abiotic Stress

Genes for Plant Abiotic Stress Editors Matthew A. Jenks and Andrew J. Wood© 2010 Blackwell Publishing ISBN: 978-0-813-81502-2

Genes for Plant Abiotic Stress

EditorsMATTHEW A. JENKS

ProfessorHorticulture and Landscape Architecture

Center for Plant Environmental Stress PhysiologyPurdue University

ANDREW J. WOODProfessor

Stress Physiology and Molecular BiologyDepartment of Plant BiologySouthern Illinois University

A John Wiley & Sons, Inc., Publication

Edition fi rst published 2010© 2010 Blackwell Publishing

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Library of Congress Cataloging-in-Publication Data

Genes for plant abiotic stress / editors, Matthew A. Jenks, Andrew J. Wood. p. cm. Includes bibliographical references and index. ISBN 978-0-8138-1502-2 (hardback : alk. paper) 1. Crops–Effect of stress on. 2. Crop improvement. 3. Crops and climate. 4. Crops–Physiology. 5. Crops–Development. I. Jenks, Matthew A. II. Wood, Andrew J. SB112.5G46 2009 632′.1–dc22 2009031844

A catalog record for this book is available from the U.S. Library of Congress.

Set in 10.5 on 12 pt Times by SNP Best-set Typesetter Ltd., Hong KongPrinted in the Singapore

1 2010

Contents

Contributors ixPreface xiii

Section 1 Genetic Determinants of Plant Adaptation under Water Stress 3

Chapter 1 Genetic Determinants of Stomatal Function 5 SONG LI and SARAH M. ASSMANN

Introduction 5 Arabidopsis as a Model System 7 How Do Stomates Sense Drought Stress? 7 Signaling Events inside Guard Cells in Response to Drought 11 Cell Signaling Mutants with Altered Stomatal Responses 15 Transcriptional Regulation in Stomatal Drought Response 22 Summary 24 References 25

Chapter 2 Pathways and Genetic Determinants for Cell Wall–based Osmotic Stress Tolerance in the Arabidopsis thaliana Root System 35 HISASHI KOIWA

Introduction 35 Genes That Affect the Cell Wall and Plant Stress Tolerance 35 Genes and Proteins in Cellulose Biosynthesis 36 Pathways Involved in N-glycosylation and N-glycan Modifi cations 38 Dolichol Biosynthesis 38 Sugar-nucleotide Biosynthesis 39 Assembly of Core Oligosaccharide 40 Oligosaccharyltransferase 40 Processing of Core Oligosaccharides in the ER 42 Unfolded Protein Response and Osmotic Stress Signaling 42 N-glycan Re-glycosylation and ER-associated Protein Degradation 44 N-glycan Modifi cation in the Golgi Apparatus 44 Ascorbate as an Interface between the N-glycosylation Pathway and Oxidative Stress Response 46 Biosynthesis of GPI Anchor 46 Microtubules 47

v

vi CONTENTS

Conclusion 48 References 49

Chapter 3 Transcription and Signaling Factors in the Drought Response Regulatory Network 55 MATTHEW GEISLER

Introduction 55 Drought Stress Perception 55 Systems Biology Approaches 56 Transcriptomic Studies of Drought Stress 63 The DREB/CBF Regulon 66 ABA Signaling 71 Reactive Oxygen Signaling 72 Integration of Stress Regulatory Networks 72 Assembling the Known Pathways and Expanding Using Gene Expression Networks’ Predicted Protein Interactions 74 Acknowledgments 75 References 75

Section 2 Genes for Crop Adaptation to Poor Soil 81

Chapter 4 Genetic Determinants of Salinity Tolerance in Crop Plants 83 DARREN PLETT, BETTINA BERGER, and MARK TESTER

Introduction 83 Salinity Tolerance 85 Conclusion 100 References 100

Chapter 5 Unraveling the Mechanisms Underlying Aluminum-dependent Root Growth Inhibition 113 PAUL B. LARSEN

Introduction 113 Mechanisms of Aluminum Toxicity 114 Aluminum Resistance Mechanisms 117 Aluminum Tolerance Mechanisms 120 Arabidopsis as a Model System for Aluminum Resistance, Tolerance, and Toxicity 121 Aluminum-sensitive Arabidopsis Mutants 121 The Role of ALS3 in A1 Tolerance 122 ALS1 Encodes a Half-type ABC Transporter Required for Aluminum Tolerance 126 Other Arabidopsis Factors Required for Aluminum Resistance/Tolerance 128 Identifi cation of Aluminum-tolerant Mutants in Arabidopsis 129 The Nature of the alt1 Mutations 132 Conclusions 138 References 138

CONTENTS vii

Chapter 6 Genetic Determinants of Phosphate Use Effi ciency in Crops 143 FULGENCIO ALATORRE-COBOS, DAMAR LÓPEZ-ARREDONDO, and LUIS HERRERA-ESTRELLA

Introduction 143 Why Improve Crop Nutrition and the Relationship with World Food Security? 143 Phosphorus and Crops: Phosphorus as an Essential Nutrient and Its Supply as a Key Component to Crop Yield 144 Phosphorus and Plant Metabolism: Regulatory and Structural Functions 145 Phosphate Starvation: Adaptations to Phosphate Starvation and Current Knowledge about Phosphate Sensing and Signaling Networks during Phosphate Stress 146 Nutrient Use Effi ciency 150 Genetic Determinants for the Phosphate Acquisition 150 Genetic Determinants for Pi Acquisition by Modulating Root System Architecture 153 Genetic Determinants Involved with Phosphorus Utilization Effi ciency 155 Genetic Engineering to Improve the Phosphate Use Effi ciency 156 Conclusions 158 References 158

Color Plate Section

Chapter 7 Genes for Use in Improving Nitrate Use Effi ciency in Crops 167 DAVID A. LIGHTFOOT

Introduction 167 The Two Forms of NUE: Regulation of Nitrogen Partitioning and Yield in Crops 169 Mutants as Tools to Isolate Important Plant Genes 169 Transcript Analysis 174 Metanomic Tools for Extending Functional Genomics 174 Transgenics Lacking A Priori Evidence for NUE 175 Microbial Activity 176 Nodule Effects and Mycorrhizal Effects 178 Water Effects 178 Conclusions 178 References 179

Section 3 Genes for Plant Tolerance to Temperature Extremes 183

Chapter 8 Genes and Gene Regulation for Low-temperature Tolerance 185 MANTAS SURVILA, PEKKA HEINO, and E. TAPIO PALVA

Introduction 185 Protective Mechanisms Induced during Cold Acclimation 188 Regulation of Gene Expression 192 Cross Talk between Abiotic and Biotic Stress Responses 207

viii CONTENTS

Conclusions and Future Perspectives 207 Acknowledgments 209 References 209

Chapter 9 Genetic Approaches toward Improving Heat Tolerance in Plants 221 MAMATHA HANUMAPPA and HENRY T. NGUYEN

Introduction 221 Thermotolerance 221 High Temperature Impact and Plant Response to Heat Stress 223 Mechanism of Heat Tolerance in Plants 230 Genetic Approaches to Improve Heat Tolerance in Crops 235 The Effect of Stress Combination 244 Evolving Techniques 246 Conclusion and Perspectives 247 References 247

Section 4 Integrating Plant Abiotic Stress Responses 261

Chapter 10 Genetic Networks Underlying Plant Abiotic Stress Responses 263 ARJUN KRISHNAN, MADANA M.R. AMBAVARAM, AMAL HARB, UTLWANG BATLANG, PETER E. WITTICH, and ANDY PEREIRA

Introduction 263 Plant Responses to Environmental Stresses 264 Transcriptome Analysis of Abiotic Stress Responses 270 Gene Network of Universal Abiotic Stress Response 274 Conclusions 276 References 276

Chapter 11 Discovering Genes for Abiotic Stress Tolerance in Crop Plants 281 MICHAEL POPELKA, MITCHELL TUINSTRA, and CLIFFORD F. WEIL

Introduction 281 Salt Stress 286 Heat Stress 287 Oxidative Stress 288 Nutrient/Mineral Stress 289 Plant Architecture and Morphology 290 Evolutionary Conservation and Gene Discovery 291 Conclusion 292 References 292

Index 303

ix

Contributors

Fulgencio Alatorre - Cobos Laboratorio Nacional de Gen ó mica para la Biodiversidad, Centro de Investigaci ó n y Estudios Avanzados del Instituto Polit é cnico Nacional Campus Guanajuato 36821 Irapuato, Guanajuato, M é xico falatorre@ira.cinvestav.mx

Madana M.R. Ambavaram Virginia Bioinformatics Institute Virginia Tech Washington Street Blacksburg, VA 24061 USA

Sarah M. Assmann Biology Department Penn State University 208 Mueller Laboratory University Park, PA 16802 USA

Utlwang Batlang Virginia Bioinformatics Institute Virginia Tech Washington Street Blacksburg, VA 24061 USA

Bettina Berger Australian Centre for Plant Functional Genomics and University of Adelaide, PMB1 Glen Osmond, SA Australia, 5064

Matthew Geisler Southern Illinois University Department of Plant Biology 403 Life Science II Building 1125 Lincoln Drive Carbondale, IL 62901 USA

x CONTRIBUTORS

Mamatha Hanumappa Division of Plant Sciences and National Center for Soybean Biotechnology University of Missouri Columbia, MO 65211 USA

Amal Harb Virginia Bioinformatics Institute Virginia Tech Washington Street Blacksburg, VA 24061 USA

Pekka Heino Department of Biological and Environmental Sciences Division of Genetics University of Helsinki P.O. Box 56, FIN - 00014 Helsinki Finland

Luis Herrera - Estrella Laboratorio Nacional de Gen ó mica para la Biodiversidad, Centro de Investigaci ó n y Estudios Avanzados del Instituto Polit é cnico Nacional Campus Guanajuato 36821 Irapuato Guanajuato, M é xico lherrera@ira.cinvestav.mx

Hisashi Koiwa Department of Horticultural Sciences 2133 Texas A & M University College Station, TX 77843 - 2133 USA

Arjun Krishnan Virginia Bioinformatics Institute Virginia Tech Washington Street Blacksburg, VA 24061 USA

Paul B. Larsen Department of Biochemistry University of California Riverside, CA 92521 USA 951 - 827 - 2026 paul.larsen@ucr.edu

CONTRIBUTORS xi

Song Li Biology Department Penn State University 208 Mueller Laboratory University Park, PA 16802 USA

David A. Lightfoot Department of Plant Soil and Agricultural Systems Southern Illinois University Carbondale, IL 62901 USA

Damar L ó pez - Arredondo Laboratorio Nacional de Gen ó mica para la Biodiversidad, Centro de Investigaci ó n y Estudios Avanzados del Instituto Polit é cnico Nacional Campus Guanajuato 36821 Irapuato Guanajuato, M é xico dlopez@ira.cinvestav.mx

Henry T. Nguyen Division of Plant Sciences and National Center for Soybean Biotechnology University of Missouri Columbia, MO 65211 USA

E. Tapio Palva Department of Biological and Environmental Sciences Division of Genetics, University of Helsinki P.O. Box 56, FIN - 00014 Helsinki Finland

Andy Pereira Virginia Bioinformatics Institute Virginia Tech Washington Street Blacksburg, VA 24061 USA pereiraa@vbi.vt.edu , 540 - 231 - 3784

Darren Plett Australian Centre for Plant Functional Genomics and University of Adelaide, PMB1 Glen Osmond, SA Australia, 5064

xii CONTRIBUTORS

Michael Popelka Agronomy Department Purdue University 915 West State Street West Lafayette, IN 47907 USA

Mantas Survila Department of Biological and Environmental Sciences Division of Genetics, University of Helsinki P.O. Box 56, FIN - 00014 Helsinki Finland

Mark Tester Australian Centre for Plant Functional Genomics and University of Adelaide, PMB1 Glen Osmond, SA Australia, 5064

Mitchell Tuinstra Agronomy Department Purdue University 915 West State Street West Lafayette, IN 47907 USA

Clifford F. Weil Agronomy Department Purdue University 915 West State Street West Lafayette, IN 47907 USA

Peter E. Wittich Virginia Bioinformatics Institute Virginia Tech Washington Street Blacksburg, VA 24061 USA

xiii

Preface

Conventional crop - breeding strategies have made limited progress in enhancing harvest indices in regions commonly beset by abiotic environmental stresses, such as those caused by drought, salin-ity, toxic metals, cold, heat, and nutrient - limiting soils. Worldwide, crop yield losses to abiotic stress range from minor to total, with actual losses being infl uenced by the timing, intensity, and duration of the stress. A major constraint to improving yield under abiotic stress is our limited understanding of the diverse genes and their alleles that underlie stress tolerance, as well as the diffi culties faced by breeders and biotechnologists seeking to combine favorable alleles to create the desired stress - adapted high - yielding genotypes. Moreover, crop domestication has narrowed the genetic diversity for stress adaptation available within crops, and thus, limited options for traditional crop breeding. Consequently, a better understanding of gene function in plant - stress adaptation and the means to use these genes to enhance crop performance are needed if we are to realize the full potential of our efforts in crop improvement.

Recent studies of gene function have revealed highly complex and surprisingly integrated genetic and metabolic networks for plant response to abiotic stress. These fi ndings are revealing a new paradigm for effective crop improvement, one that adapts a systems - based approach that closely integrates new discoveries in fundamental biology with newly developed methods in plant breeding and biotechnology.

This book integrates a broad cross - section of scientifi c knowledge and expertise around the key genetic determinants of plant abiotic stress adaptation, with gene function discussed in a way that bridges the physiological, biochemical, developmental, and molecular levels, and gives special consideration to the importance of signaling networks. New and creative approaches for manipulat-ing these determinants for germplasm improvement are also discussed. Information presented in this book will be especially useful to agronomists and horticulturists, crop breeders, biotechnolo-gists, and molecular geneticists, and serve as an important scholarly text for researchers, educators, and post - graduate students.

Matthew A. Jenks and Andrew J. Wood