Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism

Transcription

1 Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism

2 Advances in Photosynthesis and Respiration VOLUME 12 Series Editor: GOVINDJEE University of Illinois, Urabna, Illinois, U.S.A. Consulting Editors: Christine FOYER, Harpenden, U.K. Elisabeth GANTT, College Park, Maryland, U.S.A. John H. GOLBECK, University Park, Pennsylvania, U.S.A. Susan S. GOLDEN, College Station, Texas, U.S.A. Wolfgang JUNGE, Osnabrück, Germany Hartmut MICHEL, Frankfurt am Main, Germany Kirmiyuki SATOH, Okayama, Japan James Siedow, Durham, North Carolina, U.S.A. The scope of our series, beginning with volume 11, reflects the concept that photosynthesis and respiration are intertwined with respect to both the protein complexes involved and to the entire bioenergetic machinery of all life. Advances in Photosynthesis and Respiration is a book series that provides a comprehensive and state-of-the-art account of research in photosynthesis and respiration. Photosynthesis is the process by which higher plants, algae, and certain species of bacteria transform and store solar energy in the form of energy-rich organic molecules. These compounds are in turn used as the energy source for all growth and reproduction in these and almost all other organisms. As such, virtually all life on the planet ultimately depends on photosynthetic energy conversion. Respiration, which occurs in mitochondrial and bacterial membranes, utilizes energy present in organic molecules to fuel a wide range of metabolic reactions critical for cell growth and development. In addition, many photosynthetic organisms engage in energetically wasteful photorespiration that begins in the chloroplast with an oxygenation reaction catalyzed by the same enzyme responsible for capturing carbon dioxide in photosynthesis. This series of books spans topics from physics to agronomy and medicine, from femtosecond processes to season long production, from the photophysics of reaction centers, through the electrochemistry of intermediate electron transfer, to the physiology of whole orgamisms, and from X-ray christallography of proteins to the morphology or organelles and intact organisms. The goal of the series is to offer beginning researchers, advanced undergraduate students, graduate students, and even research specialists, a comprehensive, up-to-date picture of the remarkable advances across the full scope of research on photosynthesis, respiration and related processes.

3 Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism Edited by Christine H. Foyer Crop Performance and Improvement Division, IACR-Rothamsted, Harpenden, U.K. and Graham Noctor Université Denis Diderot Paris VII, Institut de la Biotechnologie des Plantes, Orsay, France KLUWER ACADEMIC PUBLISHERS NEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW

4 ebook ISBN: Print ISBN: Kluwer Academic Publishers New York, Boston, Dordrecht, London, Moscow Print 2002 Kluwer Academic Publishers Dordrecht All rights reserved No part of this ebook may be reproduced or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Kluwer Online at: and Kluwer's ebookstore at:

5 Editorial Advance in Photosynsthesis and Respiration It gives me great pleasure to announce the publication of Volume 12, Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism, edited by Christine H. Foyer and Graham Noctor in our Series. This volume is the second one to appear under the new title of Advances in Photosynthesis and Respiration. Further, a new beginning has already been made with the appointment of new members of the Board of Consulting Editors. They are: Christine Foyer, UK; Elisabeth Gantt, USA; John H. Golbeck, USA; Susan Golden, USA; Wolfgang Junge, Germany; Hartmut Michel, Germany; and Kimiyuki Satoh, Japan. James Siedow, USA, has joined our Board to provide leadership and strength in the area of respiration in this Series. Several volumes on respiration (both plant and bacterial) are already in production or being contracted. Published Volumes The present volume is a sequel to the following eleven volumes in the Advances in Photosynthesis and Respiration (AIPH) series. (1) (2) (3) (4) (5) (6) (7) Molecular Biology of Cyanobacteria (D.A. Bryant, editor, 1994); Anoxygenic Photosynthetic Bacteria (R.E. Blankenship, M.T. Madigan and C.E. Bauer, editors, 1995); Biophysical Techniques in Photosynthesis (J. Amesz and A.J. Hoff, editors, 1996); Oxygenic Photosynthesis: The Light Reactions (D.R. Ort and C.F. Yocum, editors, 1996); Photosynthesis and the Environment (N.R. Baker, editor, 1996); Lipids in Photosynthesis: Structure, Function and Genetics (P.-A. Siegenthaler and N. Murata, editors, 1998); The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas (J.-D. Rochaix, M. Goldschmidt-Clermont and S. Merchant, editors, 1998); (8) (9) (10) (11) The Photochemistry of Carotenoids (H.A. Frank, A.J. Young, G. Britton and R.J. Cogdell, editors, 1999); Photosynthesis: Physiology and Metabolism (R.C. Leegood, T.D. Sharkey and S. von Caemmerer, editors, 2000); Photosynthesis: Photobiochemistry and Photobiophysics (B. Ke, author, 2001); Regulation of Photosynthesis (E-M. Aro and B. Andersson, editors, 2001). See for further information and to order these books. Please note that the members of the International Society of Photosynthesis Research (ISPR) ( receive special discounts. Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism, edited by Christine H. Foyer and Graham Noctor, Volume 12 in our series, is a great book that bridges the basics of photosynthesis and respiration with ecology and agriculture. Plant growth and biomass production require the assimilation of nitrogen into organic compounds using energy and carbon skeletons produced by photosynthesis and respiration. Placing nitrogen assimilation firmly at the heart of photosynthesis, this volume provides an original and innovative appraisal of the metabolic co-operation that is required. Unique perspectives are presented in sixteen key areas of current research, each discussing the latest data and critically examining the most important developing concepts. Key themes are the underlying cooperation between organelles (chloroplasts and mitochondria) and pathways (photosynthesis and respiration), as well as the extensive metabolic crosstalk that dictates appropriate gene expression. This book is essential reading for those seeking to understand the details of carbon-nitrogen interactions and the importance of these relationships in determining photosynthetic biomass production. v

6 Future Books The readers of the current series are encouraged to watch for the publication of the forthcoming books: (1) (2) (3) (4) (5) (6) Light-harvesting Antennas in Photosynthesis (Editors: B.R. Green and W.W. Parson); Photosynthesis in Algae (Editors: A.W.D. Larkum, S. Douglas, and J.A. Raven); Respiration in Archaea and Bacteria, 2 volumes (Editor: D. Zannoni); Biochemistry and Biophysics of Chlorophylls (Editors: B. Grimm, R. Porra, W. Rüdiger, and H. Scheer). Chlorophyll Fluorescence (Editors: G. Papageorgiou and Govindjee); Photosystem II: The Water/Plastoquinone Oxido-reductase in Photosynthesis (Editors: T. Wydrzynski and K. Satoh); In addition to these contracted books, invitations are out for several books. Topics planned are: Plant Respiration; Protein Complexes of Photosynthesis and Respiration; Photoinhibition and Photoprotection; Photosystem I; Protonation and ATP Synthesis; Global Aspects of Photosynthesis; Functional Genomics; History of Photosynthesis; The Cytochromes; The Chloroplast; Laboratory Methods for Studying Leaves and Whole Plants. In view of the interdisciplinary character of research in photosynthesis and respiration, it is my earnest hope that this series of books will be used in educating students and researchers not only in Plant Sciences, Molecular and Cell Biology, Integrated Biology, Biotechnology, Agricultural Sciences, Microbiology, Biochemistry, and Biophysics, but also in Bioengineering, Chemistry, and Physics. I take this opportunity to thank Christine Foyer and Graham Noctor; all the authors of volume 12; Larry Orr; Jacco Flipsen, Lanette Setkoski; and my wife Rajni Govindjee for their valuable help and support that made the publication of Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism possible. Readers are requested to send their suggestions for future volumes, authors or editors to me by E- mail (gov@uiuc.edu) or fax ( ). Govindjee Series Editor Advances in Photosynthesis and Respiration University of Illinois at Urbana-Champaign Departments of Biochemistry and Plant Biology And Center of Biophysics and Computational Biology 265 Morrill Hall, 505 South Goodwin Avenue Urbana, IL , USA URL: vi

7 Govindjee The Series Editor of Advances in Photosynthesis and Respiration, Govindjee, uses one name only. He has been Professor Emeritus of Biophysics, Biochemistry and Plant Biology, at the University of Illinois at Urbana-Champaign (UIUC), since He was born in the city of Allahabad (Uttar Pradesh, India) in Govindjee graduated from the University of Allahabad, India in 1952 with a B.Sc. degree in Chemistry, Botany and Zoology, and obtained his M.Sc. (also from the University of Allahabad) in Botany (specializing in Plant Physiology) under Professor Shri Ranjan, in He subsequently served as a lecturer in Botany, at the same university, from Govindjee came to the United States of America in 1956, to pursue his doctoral studies at UIUC. He worked, first with Robert Emerson, then with Jan B. Thomas and Eugene Rabinowitch, and obtained his Ph.D. in 1960, in Biophysics. After postdoctoral research on a US Public Health Service Award, he was appointed as Assistant Professor of Botany at UIUC in 1961; in 1965, he became an Associate Professor, and then in 1969, a Professor of Biophysics and Plant Biology, at the same institution. Govindjee is co-author of Photosynthesis (John Wiley and Sons, New York, 1969), and co-editor of eight volumes on photosynthesis including (1) Concepts in Photobiology: Photosynthesis and Photomorphogenesis (Narosa Publishers, New Delhi/ Kluwer Academic Publishers, Dordrecht, 1999), (2) Molecular Biology of Photosynthesis (Kluwer Academic Publishers, Dordrecht, 1988), and (3) Light Emission by Plants and Bacteria (Academic Press, NY, 1986). Govindjee has edited (1) Photosynthesis Vol. 1: Energy Conversion by Plants and Bacteria; and Photosynthesis Vol. 2: Development, Carbon Metabolism, and Plant Productivity (Academic Press, NY, Russian Version, 1987), and (2) Bioenergetics of Photosynthesis (Academic Press, NY. 1975). In collaboration with others, Govindjee s early research established the participation of a shortwavelength form of chlorophyll a in Photosystem II (PS II), that the two-light effect of Robert Emerson was in photosynthesis, not in respiration, and that it could be studied through chlorophyll fluorescence and delayed fluorescence. Over the years, his research, again with many collaborators, has focused on the mechanisms of PS II, including the first studies on its primary charge separation; the specific role of bicarbonate on the acceptor side of PS II, the demonstration that excess light indeed quenches the lifetime of PS II chlorophyll fluorescence (and thus diminishes the quantum yield of fluorescence); and on the theory for the mechanism of thermoluminescence in plants. Currently, however, he focuses on the history of photosynthesis research, and is equally concerned with photosynthesis education (see / vii

8 Contents Editorial Contents Preface Color Plates 1 Photosynthetic Nitrogen Assimilation: Inter-Pathway Control and Signaling Christine H. Foyer and Graham Noctor II. Control of Leaf Amino Acid Contents III. Integration and Control of Nitrogen and Carbon Metabolism IV. The Carbon-Nitrogen Signal Transduction Network: Interactions Between Nitrate, Sugars and Abscisic Acid V. Conclusions and Perspectives 2 Photosynthesis and Nitrogen-Use Efficiency P. Ananda Kumar, Martin A. J. Parry, Rowan A. C. Mitchell, Altaf Ahmad and Yash P. Abrol II. Nitrogen in the Photosynthetic Apparatus III. Optimization of Amounts of Photosynthetic Components for Different Environments Role of Regulation of Rubisco Activity Approaches to Improving Nitrogen-Use Efficiency in Crops IV. V. 3 Molecular Control of Nitrate Reductase and Other Enzymes Involved in Nitrate Assimilation Wilbur H. Campbell II. Transcriptional Control of Nitrate Reductase and Other Nitrogen Metabolism Genes III. Post-Translational Control of Nitrogen Metabolism Enzymes v viii xiii CP viii

9 IV. Protein Kinases and Control of Carbon and Nitrogen Metabolism V. Future Prospects for the Control of Nitrogen Metabolism Acknowledgment 4 Soluble and Plasma Membrane-bound Enzymes Involved in Nitrate and Nitrite Metabolism Christian Meyer and Christine Stöhr II. Nitrate Reduction at the Plasma Membrane III. Nitrite Transport and Reduction IV. Conclusions 5 What Limits Nitrate Reduction in Leaves? Werner M. Kaiser, Maria Stoimenova and Hui-Min Man II. Nitrate Reduction and Nitrate Reductase Activity in Photosynthesizing Leaves III. Nitrate Reduction after Artificial Activation of Nitrate Reductase IV. Is Cytosolic Nitrate Concentration Rate-Limiting? V. Is Nitrate Reduction Limited by NAD(P)H? VI. Conclusions 6 The Biochemistry, Molecular Biology, and Genetic Manipulation of Primary Ammonia Assimilation Bertrand Hirel and Peter J. Lea I. II. III. IV. Introduction: Glutamine Synthetase and Glutamate Synthase, Two Enzymes at the Crossroads Between Carbon and Nitrogen Metabolism Glutamine Synthetase Glutamate Synthase Glutamate Dehydrogenase Regulation of Ammonium Assimilation in Cyanobacteria Francisco J. Florencio and José C. Reyes II. Ammonium Uptake III. The Glutamine Synthetase/Glutamate Synthase Pathway ix

10 IV. Regulation of Ammonium Assimilation V. Future Perspectives Photorespiratory Carbon and Nitrogen Cycling: Evidence from Studies of Mutant and Transgenic Plants Alfred J. Keys and Richard C. Leegood II. Entry of Carbon into the Photorespiratory Pathway III. Recycling of Carbon to the Reductive Pentose Phosphate Pathway IV. Recycling of Nitrogen Associated with Photorespiration V. Feedback from Photorespiration on Other Processes VI. Role of Photorespiration During Stress Conclusions 9 The Regulation of Plant Phosphoenolpyruvate Carboxylase by Reversible Phosphorylation Jean Vidal, Nadia Bakrim and Michael Hodges II. Properties of Phosphoenolpyruvate Carboxylase III. The Enzyme s Physiological Context IV. Reversible Modulation in vivo by a Regulatory Phosphorylation Cycle V. Significance of Regulatory Phosphorylation of the Photosynthetic Isoform VI. Regulatory Phosphorylation of the Form: Importance in Anaplerosis VII. Conclusions and Perspectives Mitochondrial Functions in the Light and Significance to Carbon-Nitrogen Interactions Per Gardeström, Abir U. Igamberdiev and A. S. Raghavendra II. Export of Photosynthate from the Chloroplast III. Mitochondrial Products of Photorespiration IV. Products of Glycolysis in the Light V. Operation of the Tricarboxylic Acid Cycle VI. Electron Transport and Redox Levels in Plant Mitochondria VII. Participation of Mitochondria in the Regulation of Metabolism during Transitions between Light and Darkness VIII. Mitochondrial Respiration and Photoinhibition IX. The Role of Mitochondria in Photosynthesis x

11 X. Glycolate Metabolism in Algal Mitochondria XI. Concluding Remarks Alternative Oxidase: Integrating Carbon Metabolism and Electron Transport in Plant Respiration Greg C. Vanlerberghe and Sandi H. Ordog I. II. III. IV. Integration in Plant Respiration The Alternative Oxidase in Plant Mitochondrial Electron Transport Regulation of Alternative Oxidase Physiological Function of Alternative Oxidase Nitric Oxide Synthesis by Plants and its Potential Impact on Nitrogen and Respiratory Metabolism A. Harvey Millar, David A. Day and Christel Mathieu I. Nitric Oxide as a Biological Messenger Molecule II. Evidence of Nitric Oxide Synthesis and Accumulation in Plants III. Evidence of Nitric Oxide Modulation of Plant Signaling, Metabolism and Development IV. So What is the Role of Nitric Oxide in Plants? Nitrogen and Signaling Anne Krapp, Sylvie Ferrario-Méry and Bruno Touraine II. Processes Regulated by Nitrate and Reduced Nitrogen-Compounds III. Molecular Mechanisms of Nitrogen Signal Perception and Transduction IV. Concluding Remarks Regulation of Carbon and Nitrogen Assimilation Through Gene Expression Tatsuo Sugiyama and Hitoshi Sakakibara II. Physiological and Biochemical Nature of Plant Response to Nitrogen xi

12 III. IV. V. Regulation of Nitrogen-Responsive Genes for Carbon Assimilation Regulation of Nitrogen-Responsive Genes for Assimilation and Subsequent Metabolism of Nitrogen Regulation of Partitioning of Nitrogen into Proteins: A Model for Sensing and Signaling 15 Intracellular And Intercellular Transport Of Nitrogen And Carbon Gertrud Lohaus and Karsten Fischer I. II. III. IV. Introduction Transport Processes of Plastids Transport Processes Involved in Phloem Loading Concluding Remarks Optimizing Carbon-Nitrogen Budgets: Perspectives for Crop Improvement John A. Raven, Linda L. Handley and Mitchell Andrews II. The Nature of Crops III. What Are We Seeking to Optimize in Carbon-Nitrogen Budgets? IV. How Can We Change Carbon-Nitrogen Budgets? V. What are the Outcomes of Changing Carbon-Nitrogen Budgets? VI. Prospects and Conclusions Index 275 xii

13 Preface According to many textbooks, carbohydrates are the unique final products of plant photosynthesis. However, the photoautotrophic production of organic nitrogenous compounds may be just as old, in evolutionary terms, as carbohydrate synthesis. In the algae and plants of today, the light-driven assimilation of nitrogen remains a key function, operating alongside and intermeshing with photosynthesis and respiration. Photosynthetic production of reduced carbon and its reoxidation in respiration are necessary to produce both the energy and the carbon skeletons required for the incorporation of inorganic nitrogen into amino acids. Conversely, nitrogen assimilation is required to sustain the output of organic carbon and nitrogen. Together, the sugars and amino acids produced by the pigments and enzymes of the photosynthetic apparatus form the building blocks for plant development, growth, and biomass production. Complex interactions between photosynthetic carbon and nitrogen metabolism must, therefore, have evolved long ago and can be regarded as the expression of a truly ancient principle. Perhaps more than any other major physiological process, nitrogen assimilation weds together photosynthesis and respiration into a unified network of interdependent processes. In plants especially, this network is further complicated by the concomitant operation of photorespiratory metabolism. The numerous interactions between carbon and nitrogen metabolism have been intensively studied at multiple levels of complexity and plant anatomy. Within the cell, extensive co-operation is required between different compartments, including chloroplasts, peroxisomes, cytosol, and mitochondria, while changes in carbon and nitrogen status influence organ physiology and root/shoot relationships. Ultimately, carbon/nitrogen relationships are whole plant phenomena but many of the primary interactions of key importance occur in the photosynthetic heart of green cells, the chloroplast, in co-operation with the mitochondrion. A multitude of interconnections are required between chloroplasts and mitochondria that function to achieve optimal energy balance and partitioning of assimilate, and hence avoid undue perturbation of cellular redox balance. Rates of photosynthesis and mitochondrial respiration fluctuate in a circadian manner in almost every organism studied. In addition, external triggers and environmental influences necessitate precise and appropriate re-adjustment of relative flux rates, to prevent excessive swings in energy/resource provision and use. This requires integrated control of the expression and activity of numerous key enzymes in photosynthetic and respiratory pathways, in order to co-ordinate carbon partioning and nitrogen assimilation. This volume has two principal aims. The first is to provide a comprehensive account of the very latest developments in our understanding of how green cells reductively incorporate nitrate and ammonium into the organic compounds required for growth. From the partitioning of organic nitrogen within the photosynthetic apparatus, through the primary processes of nitrate reduction and ammonia assimilation and cycling in photorespiration, to the intracellular and intercellular transport of carbon and nitrogen, the processes involved in photosynthetic nitrogen assimilation are described and exciting new developments such as nitric oxide production evaluated. The second aim is to provide a comprehensive account of the mechanisms of crosstalk between carbon and nitrogen metabolism. A key theme of this volume is the close co-ordination of photosynthetic and respiratory processes in nitrogen assimilation. Emerging concepts of the interdependence of chloroplasts and mitochondria are described, and essential communication, transport and signaling processes are highlighted. We are becoming more aware that photosynthesis uses light and changes in redox state, as well as carbon and nitrogen metabolites, not only to drive assimilatory metabolism but also to signal current status at the level of control of gene expression. Recent data on carbon/nitrogen interactions suggest that, from the capture of light to the synthesis of amino acids and export of carbon and nitrogen, numerous substrates, intermediates and products are monitored by the cell and the information transduced into regulation at the levels of gene expression and enzyme activity. Effective regulation ultimately determines the fate xiii

14 of the photosynthetic system, as loss of metabolic balance can trigger precocious senescence. These considerations must lead us to consider the term homeostasis, rarely considered in relation to photosynthesis. This term does not imply a static situation but rather describes a dynamic equilibrium between the provision and use of energy within the regulated limits of carbon and nitrogen assimilation capacity. To ensure homeostasis, several key molecules play major roles in signaling appropriate changes in gene expression. This is the first comprehensive treatise that places nitrogen assimilation firmly within the context of photosynthesis. Volume 7 of this series covered the molecular biology of chloroplasts and mitochondria in algae while Volume 9 provided a comprehensive overview of photosynthetic carbon metabolism in plants. The content of the present book reflects our view that we are at the beginning of an era in which new genomic and related profiling techniques will allow metabolism to be examined more holistically than previously. The present volume therefore reviews the new developments that are uncovering the significance of nitrogen metabolism in photosynthesis and the importance of carbon metabolism for nitrogen assimilation. For the first time in this series, equal emphasis is placed on photosynthetic and respiratory metabolism. A major theme of the book is the intricate relationship between metabolic processes that requires researchers to take a broader view than ever before in examining the enormous complexity of plant metabolism. Written by a multinational team of experts, this work will be an invaluable tool for students at final-year undergraduate and graduate level, as well as essential and engaging reading for all those whose enthusiasm is fired by the intricate metabolic networks that support the growth of photosynthetic organisms on earth. As editors of this volume, we wish to acknowledge the considerable efforts of all involved in the production of this work. In particular, we wish to thank the authors, who have made the most important contribution of all in providing their unique insights and personal perspectives. We are also deeply indebted to Govindjee and Larry Orr for their invaluable advice, patience and good humor, without which this volume could not have been assembled. Christine H. Foyer Rothamsted Research, UK christine.foyer@bbsrc.ac.uk Graham Noctor Institut de Biotechnologie des Plantes, France graham.noctor@ibp.u-psud.fr xiv

15 Christine Foyer is a visiting Professor at the University of Newcastle, U.K. and the head of the Stress Biology Programme in the Crop Productivity and Improvement Division at Rothamsted Research, Harpenden, Hertfordshire, U.K. She was born in the town of Gainsborough (UK) in She graduated from the University of Portsmouth, UK in 1974 with a B.Sc. degree in Biology (Hons), and obtained her Ph.D. in 1977 from Kings College, University of London, U.K., working with Barry Halliwell. After postdoctoral research at King s College (with David Hall), she moved to the Research Institute for Photosynthesis, University of Sheffield, U.K. In 1988, she became a Directeur de Recherche at the Laboratoire du Métabolisme et de la Nutrition des Plantes, at INRA (Institut National de la Recherche Agronomique), Versailles, France. In 1994, she became Head of the Environmental Biology Department at the Institute of Grassland and Environmental Research, Aberystwyth, Wales. In 1998 she moved to her present position at the Institute of Arable Crops Research, Rothamsted, U.K., where she was Head of the Biochemistry and Physiology Department until She is author of Photosynthesis, Bittar E. E. series ed., Cell Biology: A Series of Monographs, John Wiley and Sons, New York, 219 pp, 1984, and co-editor of Causes of Photooxidative Stress in Plants and Amelioration of Defense Systems, 1994, CRC Press, 416 pp; and A molecular Approach to Primary Metabolism in Plants, Taylor and Francis, London, UK, 347 pp, Christine s current research interests concern the regulation of primary and intermediary metabolism in optimal and stress conditions. She is particularly interested in the metabolic crosstalk that controls assimilate partitioning between sucrose and amino acid biosynthesis in leaves. Moreover, she is a specialist in the field of oxidative stress in plants having published extensively on plant antioxidant metabolism and its role in stress signaling xv

16 Graham Noctor is a Professor at the Institut de Biotechnologie des Plantes, Paris, France. He was born in Manchester, UK in He obtained his first degree (B.Sc.) from the University of Essex, UK and his Ph.D from the University of Keele, UK in 1988, for work with John Mills on the control of photosynthetic metabolism by thiol-regulation. Then followed post-doctoral research in Peter Horton s laboratory at the University of Sheffield, UK, on relationships between photosynthetic light-harvesting efficiency and metabolism, focusing particularly on the mechanisms that underlie non-photochemical quenching of chlorophyll fluorescence. It was while at Sheffield that he became involved in work on carbon-nitrogen interactions, during two visits in 1990 and 1991 to Christine Foyer s laboratory at the Institut National de la Recherche Agronomique (INRA), Versailles, France. He subsequently returned to INRA Versailles, where he worked for four years on the control of the synthesis of the tripeptide, glutathione. From 1998 to 2001, he was a research scientist at the Institut of Arable Crops Research (Rothamsted, UK), where he was involved in several projects, notably investigating the role of mitochondria in photosynthesis and in carbon/nitrogen interactions, and in the relationship between oxidant production and antioxidant metabolism in leaves. He continues to explore these themes in his present post, which he took up in xvi

17 Color Plates Christine H. Foyer and Graham Noctor (eds): Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism pp. CP-1 CP Kluwer Academic Publishers. Printed in The Netherlands.

18 CP-2 Color Plates

19 Color Plates CP-3