Antioxidants and Reactive Oxygen Species in Plants

Biological Sciences Series

A series which provides an accessible source of information at research and professional level in chosen sectors of the biological sciences. Series Editor: Professor Jeremy A. Roberts, Plant Science Division, School of Biosciences, University of Nottingham. 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 Graham B. Seymour and J. Paul 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 Plant Abiotic Stress Edited by M.A. Jenks and P.M. Hasegawa Gene Flow from GM Plants Edited by G.M. Poppy and M.J. Wilkinson Antioxidants and Reactive Oxygen Species in Plants Edited by N. Smirnoff

Antioxidants and Reactive Oxygen Species in Plants

Edited by NICHOLAS SMIRNOFF School of Biological and Chemical Sciences University of Exeter UK

 2005 by Blackwell Publishing Ltd Editorial Offices: Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK Tel: 44 (0)1865 776868 Blackwell Publishing Professional, 2121 State Avenue, Ames, Iowa 50014-8300, USA Tel: 1 515 292 0140 Blackwell Publishing Asia, 550 Swanston Street, Carlton, Victoria 3053, Australia Tel: 61 (0)3 8359 1011 The right of the Author to be identified as the Author of this Work has been asserted in accordance with the Copyright, Designs and Patents Act 1988. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. First published 2005 by Blackwell Publishing Ltd Library of Congress Cataloging-in-Publication Data: Antioxidants and reactive oxygen species in plants / edited by Nicholas Smirnoff. p. cm. Includes bibliographical references and index. ISBN-13: 978-1-4051-2529-1 (hardback : alk. paper) ISBN-10: 1-4051-2529-2 (hardback : alk. paper) 1. AntioxidantsPhysiological effect. 2. Active oxygenPhysiological effect. 3. PlantsMetabolism. I. Smirnoff, N. QK898.A57A57 2005 572 .42dc22 2004027446 ISBN-13: 978-1-4051-2529-1 ISBN-10: 1-4051-2529-2 British Library Cataloguing-in-Publication Data A catalogue record for this title is available from the British Library Set in 10/12 pt Times by Newgen Imaging Systems (P) Ltd, Chennai, India Printed and bound in India by Gopsons Papers Ltd, Noida The publishers policy is to use permanent paper from mills that operate a sustainable forestry policy, and which has been manufactured from pulp processed using acid-free and elementary chlorine-free practices. Furthermore, the publisher ensures that the text paper and cover board used have met acceptable environmental accreditation standards. For further information on Blackwell Publishing, visit our website: www.blackwellpublishing.com

Contents

Contributors Preface 1 Glutathione CHRISTINE H. FOYER, LEONARDO D. GOMEZ AND PHILIPPUS D.R. VAN HEERDEN 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 1.9 1.10 2 Introduction The glutathione redox couple and cellular redox potential Glutathione metabolism Biosynthesis and inhibition by L-buthionine-SR-sulphoximine Glutathione and the cell cycle Glutathione in leaves and its relationship to chilling tolerance Glutathione and homoglutathione in the regulation of root and root nodule development Transport and transporters Glutathione and signalling Conclusions and perspectives

xi xiii 1

1 2 2 5 9 10 12 15 16 18 25

Plant thiol enzymes and thiol homeostasis in relation to thiol-dependent redox regulation and oxidative stress KARL-JOSEF DIETZ 2.1 2.2 2.3 2.4 2.5 2.6 Introduction: plant sulfur and thiol contents The redox potential and its relation to the redox proteome Oxidation of thiol groups C-X-X-C and C-X-X-S motifs in redox proteins The principle reactions that maintain thiol-redox homeostasis Enzymes involved in thioldisulfide interconversion 2.6.1 Thioredoxins 2.6.2 Glutaredoxins 2.6.3 Omega and lambda-GSTs 2.6.4 Protein disulfide isomerases Peroxiredoxins, thiol/disulfide proteins in antioxidant defence 2.7.1 1-Cys Prx 2.7.2 2-Cys Prx 2.7.3 Prx Q 2.7.4 Type II Prx

2.7

25 26 28 29 30 32 32 33 35 35 36 37 37 39 40

vi 2.8 2.9 2.10 2.11 2.12 3

CONTENTS

The thiol proteome of plants Thiol homeostasis in subcellular compartments Thiol-dependent redox regulation of gene expression Linking thiol regulation to metabolic and developmental pathways Outlook

41 42 44 46 47

Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions NICHOLAS SMIRNOFF 3.1 3.2 Introduction Ascorbate 3.2.1 Distribution and subcellular localisation 3.2.2 Ascorbate biosynthesis 3.2.3 Ascorbate recycling 3.2.4 Ascorbate and dehydroascorbate transport across membranes 3.2.5 Enzymes involved in ascorbate oxidation 3.2.6 Ascorbate catabolism 3.2.7 Control of ascorbate synthesis and metabolic engineering 3.2.8 The functions of ascorbate 3.3 Vitamin E: tocopherols and tocotrienols 3.3.1 Isoprenoid antioxidants 3.3.2 Structure and antioxidant activity of tocopherols and tocotrienols 3.3.3 Functions of tocopherol 3.3.4 Biosynthesis of tocopherols and tocotrienols 3.3.5 Control and engineering of tocopherol and tocotrienol biosynthesis 3.4 Carotenoids 3.4.1 Carotenoids as antioxidants 3.4.2 Carotenoid biosynthesis and metabolic engineering

53

53 53 53 54 58 60 60 61 61 62 67 67 68 70 73 74 75 75 78 87

Ascorbate peroxidase RON MITTLER AND THOMAS L. POULOS 4.1 4.2 4.3 Enzymatic removal of hydrogen peroxide in plants Functional analysis of APX APX structure 4.3.1 Overall structure 4.3.2 Active site structure 4.3.3 Substrate binding Evolution of APXs Summary

4.4 4.5

87 90 92 92 93 94 94 96

CONTENTS

vii

Catalases in plants: molecular and functional properties and role in stress defence JRGEN FEIERABEND Introduction Biochemistry and molecular structure of catalases 5.2.1 Types of catalases 5.2.2 Molecular structure 5.2.3 Mechanism of the catalytic reaction and kinetic properties 5.3 Occurrence and properties of plant catalases 5.3.1 Sources of H2O2 production in plant cells 5.3.2 Occurrence and subcellular localization of plant catalases 5.3.3 Properties of plant catalases 5.3.4 Multiple forms, gene families and gene evolution 5.4 Biogenesis and control of expression 5.4.1 Biosynthesis and import into peroxisomes 5.4.2 Control of expression of catalase 5.5 Photoinactivation and regulation of turnover 5.6 Physiological significance and role in stress defence 5.6.1 Responses to deficiencies or overexpression of catalase 5.6.2 Low- and high-temperature stress 5.6.3 Salinity stress 5.6.4 Pathogen defence 5.1 5.2

101

101 102 102 103 106 108 108 109 110 111 114 114 116 119 126 126 128 130 130 141

Phenolics as antioxidants STEPHEN C. GRACE 6.1 6.2 6.3 Introduction Biosynthetic aspects of phenolic metabolism Stress-induced phenylpropanoid metabolism 6.3.1 High light 6.3.2 UV radiation 6.3.3 Low temperatures 6.3.4 Pathogens 6.3.5 Ozone Antioxidant properties of phenolic compounds Biological targets of phenolic antioxidants Prooxidant properties of phenolic compounds Anti-herbivore properties of phenolics Conclusions

6.4 6.5 6.6 6.7 6.8

141 142 143 144 146 147 149 151 151 156 157 158 159

viii 7

CONTENTS

Reactive oxygen species as signalling molecules RADHIKA DESIKAN, JOHN HANCOCK AND STEVEN NEILL 7.1 7.2 7.3 Introduction ROS chemistry ROS signalling 7.3.1 Specificity of ROS 7.3.2 Perception and direct effects of ROS Regulators of ROS signalling 7.4.1 ROS, calcium and ion channels 7.4.2 Reversible protein phosphorylation 7.4.3 ROS regulation of gene expression Regulation of ROS production 7.5.1 ROS removal Cross-talk with other signalling molecules/pathways Systemic signalling Conclusion

169

7.4

7.5 7.6 7.7 7.8 8

169 172 174 174 175 179 179 180 182 184 187 187 190 191

Reactive oxygen species in plant development and pathogen defence MARK A. JONES AND NICHOLAS SMIRNOFF 8.1 8.2 8.3 Introduction The roles of ROS in plant development NADPH oxidase and ROS in plant cell morphogenesis 8.3.1 NADPH oxidases in polarised plant cells 8.3.2 NADPH-oxidase-mediated effects on gene expression 8.3.3 The regulatory effect of ROS on calcium channels 8.3.4 The role of calcium in regulating plant NOXs 8.3.5 The role of ROP GTPases in regulating plant NOXs Programmed cell death and senescence ROS and antioxidants in response to pathogens and wounding

197

8.4 8.5 9

197 197 200 200 200 202 202 203 203 207 215

Reactive oxygen species in cell walls ROBERT A.M. VREEBURG AND STEPHEN C. FRY 9.1 9.2 9.3 The cell wall and the apoplast Reactive oxygen species H2O2 in plant cell walls 9.3.1 Evidence for the presence of H2O2 in the wall/apoplast of the living plant cell

215 216 217 217

CONTENTS

ix

External and internal factors that trigger apoplastic H2O2 formation 9.3.3 Proposed roles for apoplastic H2O2 in vivo 9.3.4 Proposed mechanisms of H2O2 formation 9.4 O2 and HO2 in plant cell walls 9.4.1 Properties of O2 and HO2 9.4.2 Detection of O2 9.4.3 Formation of O2 in plant cell walls 9.4.4 Role of O2 in plant cell walls 9.4.5 Regulation of O2 production in plant cell walls 9.4.6 Lifetime and fate of O2 in plant cell walls 9.5 OH in plant cell walls 9.5.1 Properties of OH 9.5.2 Proposed mechanisms of apoplastic OH formation 9.5.3 Evidence for presence of OH in the wall/apoplast of the living plant cell 9.5.4 Factors that trigger formation of apoplastic OH 9.5.5 Proposed roles for apoplastic OH in vivo 9.5.6 Chemical effects and fate of OH in the apoplast 9.6 Concluding remarks 10 Reactive oxygen species and photosynthesis BARRY A. LOGAN Introduction Light absorption and allocation 10.2.1 Triplet-chlorophyll mediated singlet O2 formation 10.2.2 Thermal energy dissipation 10.2.3 Acclimation of the light harvesting complex to the environment 10.3 Singlet O2 generation at photosystem II 10.4 Electron transport and O2 photoreduction 10.4.1 The waterwater cycle 10.4.2 The extent of O2 photoreduction 10.4.3 O2 metabolism and the regulation of PSII excitation pressure 10.4.4 Acclimation of the waterwater cycle to the environment 10.5 Linkages between photosynthesis and extrachloroplastic oxidative metabolism 10.6 Concluding remarks 10.1 10.2

9.3.2

217 219 221 223 223 224 225 226 227 228 228 228 229 231 236 237 240 243 250

250 250 250 251 253 255 256 256 258 259 259 260 262

CONTENTS

11 Plant responses to ozone PINJA JASPERS, HANNES KOLLIST, CHRISTIAN LANGEBARTELS AND JAAKKO KANGASJRVI Introduction 11.1.1 Regulation of O3 flux to leaves 11.1.2 O3 degradation to ROS and removal by antioxidants in the apoplast 11.1.3 Induction of the active oxidative burst and sensing of ROS 11.2 Hormonal control of plant O3 responses 11.2.1 Lesion initiation 11.2.2 Lesion propagation 11.2.3 Lesion containment 11.2.4 Interactions between the hormonal signaling cascades 11.3 Other regulators of plant O3 responses 11.3.1 Induction of plant volatiles 11.3.2 O3 and mitogen-activated protein kinases 11.3.3 G-proteins 11.4 Conclusions Index 11.1

268

268 269 270 273 276 276 278 280 281 282 282 284 285 286 293

Contributors

Dr Radhika Desikan

Centre for Research in Plant Science, University of the West of England, Frenchay Campus, Coldharbour Lane, Bristol BS16 1QY, UK Lehrstuhl fr Biochemie und Physiologie der Pflanzen, Fakultt fr Biologie W5, Universitt Bielefeld, 33501 Bielefeld, Germany Institute of Botany, J.W. Goethe-Universitt, D-60054 Frankfurt/Main, Germany Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK School of Biological Sciences, University of Edinburgh, The Kings Buildings, Mayfield Road, Edinburgh EH9 3JH, UK Centre for Novel Agricultural Products, Department of Biology, University of York, PO Box 373, York YO10 5YW, UK Biology Department, University of Arkansas at Little Rock, 2801 South University Avenue, Little Rock, AR 72204-1099, USA Centre for Research in Plant Science, University of the West of England, Frenchay Campus, Coldharbour Lane, Bristol BS16 1QY, UK Department of Biological and Environmental Sciences, University of Helsinki, FIN-00014 Helsinki, Finland School of Biological and Chemical Sciences, University of Exeter, Washington Singer Laboratories, Perry Road, Exeter EX4 4QG, UK

Professor Karl-Josef Dietz

Professor Jrgen Feierabend

Professor Christine H. Foyer

Professor Stephen C. Fry

Dr Leonardo Gomez

Dr Stephen C. Grace

Dr John Hancock

Ms Pinja Jaspers

Dr Mark A. Jones

xii Professor Jaakko Kangasjrvi

CONTRIBUTORS

Department of Biological and Environmental Sciences, University of Helsinki, FIN-00014 Helsinki, Finland Department of Biological and Environmental Sciences, University of Helsinki, FIN-00014 Helsinki, Finland GSF National Research Center for Environment and Health, Ingolstdter Landstrasse 1, D-85764 Oberschleissheim, Germany Biology Department, Bowdoin College, 6500 College Station, Brunswick ME 04011, USA Department of Biochemistry, University of Nevada, MS 200, 1664 North Virginia Street, Reno, Nevada 89557, USA Centre for Research in Plant Science, University of the West of England, Frenchay Campus, Coldharbour Lane, Bristol BS16 1QY, UK Department of Molecular Biology and Biochemistry, University of California, Irvine, CA 92697-3900, USA School of Biological and Chemical Sciences, University of Exeter, Washington Singer Laboratories, Perry Road, Exeter EX4 4QG, UK School of Environmental Sciences and Development, Section Botany, North-West University, Potchefstroom 2520, South Africa School of Biological Sciences, University of Edinburgh, The Kings Buildings, Mayfield Road, Edinburgh EH9 3JH, UK

Dr Hannes Kollist

Dr Christian Langebartels

Dr Barry A. Logan

Dr Ron Mittler

Professor Steven Neill

Dr Thomas L. Poulos

Dr Nicholas Smirnoff

Dr Philippus D.R. van Heerden

Dr Robert A.M. Vreeburg

Preface

Reactive oxygen species (ROS), which include superoxide, hydrogen peroxide and the hydroxyl radical, are produced during the interaction of metabolism with oxygen. ROS have the potential to cause oxidative damage by reacting with biomolecules. Accordingly, the emphasis of research on ROS has been on the oxidative damage that results from exposure to environmental stresses and on the role of ROS in defence against pathogens. More recently, it has become apparent that ROS have important roles as signalling molecules that contribute to the control of plant development and to the sensing of the external environment. A complex network of enzymatic and small molecule antioxidants control the concentration of ROS and repair oxidative damage. Interest in the function of small molecule antioxidants such as tocopherols (vitamin E), glutathione and ascorbic acid (vitamin C) is increasing, now that the details of their biosynthetic pathways have been uncovered. This research is revealing the complex and subtle interplay between ROS and antioxidants in controlling plant growth, development and response to the environment. The book covers these new developments through a series of in-depth chapters, but it also provides, in one place, an overview of the subject for those outside the research area. The first six chapters cover the synthesis and function of antioxidants (glutathione, proteins involved in thiol homeostasis, ascorbate, tocopherol, carotenoids, phenolic compounds and catalase). Many of these antioxidants are important in the human diet, which provides additional impetus to understand their metabolism in order to manipulate their synthesis more effectively. The next three chapters consider the role of ROS in signalling, developmental processes and cell wall biochemistry. The final two chapters consider photosynthesis, which is a major source of ROS in leaves, and response to ozone, which has provided a useful model system for understanding the complex interplay of responses made by plants to ROS and oxidative stress. The subject matter is generally focussed on the molecular and biochemical details, as these have provided the basis for the large increase in research activity on ROS and antioxidants over the last decade. The antioxidant network is an ideal candidate for investigation on the genome-wide scale, using functional genomics and systems biology tools, and I hope that this volume will provide a background for this endeavour. Nicholas Smirnoff