Regulation of Photosynthesis Advances in Photosynthesis and Respiration VOLUME 11 Series Editor: GOVINDJEE University of Illinois, Urbana, Illinois, U.S.A. Consulting Editors: Eva-Mari ARO, Turku, Finland Christine FOYER, Dyfed, 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 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.AdvancesinPhotosynthesis andRespiration is a book series that provides a comprehensive and state-of-the-art account of research in photo- synthesis and respiration. Photosynthesis is the process by which higher plants, algae, and certain species of bacteriatransform 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. The titles published in this series are listed at the end of this volume and those of forthcoming volumes on thebackcover. Regulation of Photosynthesis Edited by Eva-Mari Aro University of Turku, Finland and Bertil Andersson University of Stockholm/Linköping, Sweden KLUWER ACADEMIC PUBLISHERS NEW YORK,BOSTON, DORDRECHT, LONDON, MOSCOW eBookISBN: 0-306-48148-0 Print ISBN: 0-7923-6332-9 ©2004 Kluwer Academic Publishers NewYork, Boston, Dordrecht, London, Moscow Print ©2001 Kluwer Academic Publishers Dordrecht All rights reserved No part of this eBook maybe reproducedor transmitted inanyform or byanymeans,electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Kluwer Online at: http://kluweronline.com and Kluwer's eBookstoreat: http://ebooks.kluweronline.com Editorial Advances in Photosynthesis and Respiration I am proud to announce the publication of Volume 11, (8) The Photochemistry of Carotenoids (H.A. Regulation of Photosynthesis, edited by Eva-Mari Frank, A.J. Young, G. Britton and R.J. Cogdell, Aro and Bertil Andersson, in our Series. This volume editors, 1999); is the first one to appear under the new title of (9) Photosynthesis: Physiology and Metabolism Advances in Photosynthesis and Respiration. Further, (R.C. Leegood, T.D. Sharkey and Susanne von a new beginning is made here with the appointment Caemmerer, editors, 2000); and of new members of the Board of Consulting Editors. (10) Photosynthesis: Photobiochemistry and They are: Christine Foyer, UK; Elisabeth Gantt, Photobiophysics (Bacon Ke, author, 2001) USA; John H. Golbeck, USA; Susan Golden, USA; See <http://www.wkap.nl/series.htm/AIPH> for Wolfgang Junge, Germany; Hartmut Michel, further information and to order these books. Please Germany; and Kimiyuki Satoh, Japan. I take this note that the members of the International Society of opportunity to welcome them and to thank the Photosynthesis Research, ISPR (<http://www. members of the previous Board of Consulting Editors: photosynthesisresearch.org>) receive special Jan Amesz*, the Netherlands, Eva-Mari Aro, Finland; discounts. James Barber, UK; Robert E. Blankenship, USA; Norio Murata, Japan; and Donald R. Ort, USA. Eva- Regulatory Aspects of Photosynthesis Mari has kindly agreed to stay with the Boarduntil Volume 12, after which we will appoint someone This new volume, Volume 11, is devoted to a critical devoted solely to the area of “Respiration.” area of photosynthesis, regulation. Regulation is the key for the optimum functioning of photosynthesis, Published Volumes and for dealing with both the abiotic (temperature, -deficiency, drought, and even light) and biotic The present volume is a sequel to the following ten stresses that are imposed on the plants. Eva-Mari volumes in the Advances in Photosynthesis (AIPH) Aro and Bertil Andersson have provided us with an series. authoritative book that has a broad perspective of the (1) Molecular Biology of Cyanobacteria (D.A. regulatory processes of photosynthesis. I have read Bryant, editor, 1994); the entire book and am impressed with the (2) Anoxygenic Photosynthetic Bacteria (R.E. thoroughness of each chapter; it is a unique book in Blankenship, M.T. Madigan and C.E. Bauer, a rapidly growing field of plant biology. I predict that editors, 1995); this book will remain a major resource in the area of (3) Biophysical Techniques in Photosynthesis ‘regulatory processes’ for decades to come. It provides (J. Amesz and A.J. Hoff, editors, 1996); the genetic and biochemical basis of: regulation of (4) Oxygenic Photosynthesis: The Light Reactions chloroplast gene expression and signal transduction; (D.R. Ort and C.F. Yocum, editors, 1996); how nuclear and chloroplast genomes cooperate; (5) Photosynthesis and the Environment (N.R. how photosynthesis controls its own functions Baker, editor, 1996); through redox regulation and through metabolism of (6) Lipids in Photosynthesis: Structure, Function the end-products; how proteins are correctly placed and Genetics (P.-A. Siegenthaler and N. Murata, in the membranes; biogenesis and assembly of editors, 1998); photosynthetic apparatus; and, how a myriad of (7) The Molecular Biology of Chloroplasts and enzymes, present at low levels, control and regulate Mitochondria in Chlamydomonas (J.-D. many processes in the photosynthetic cells, among Rochaix, M. Goldschmidt-Clermont and other topics. This book is highlysuitable for advanced Sabeeha Merchant, editors, 1998); undergraduate and graduate students, beginning researchers, and even experts in the areas of plant * DeceasedJanuary 29, 2001 biochemistry; plant physiology; plant molecular biology; molecularandcellularbiology; integrative (3) Photosynthetic Nitrogen Assimilation and biology; microbiology; and plant biology. Associated Organic Acid Metabolism (Editors: C.H. Foyer and G. Noctor); The Scope of the Series (4) Chlorophyll a Fluorescence: A Signature of Photosynthesis (Editors: G. Papageorgiou and We expect that the scope of our series, beginning Govindjee); and, with this volume, will reflect the concept that (5) Photosystem II: The Water/Plastoquinone photosynthesis and respiration are intertwined with Oxido-reductase in Photosynthesis (Editors: T. respect to both the protein complexes involved and to Wydrzynski and K. Satoh). the entire bioenergetic machinery of all life. Advances in Photosynthesis andRespiration is a book series In addition to these contracted books, invitations providing a comprehensive and state-of-the-art are out for several books. Topics planned are: Archael, account of research in photosynthesis and respiration. Bacterial and Plant Respiration; Protein Complexes Photosynthesis is the process by which higher plants, of Photosynthesis and Respiration; Photoinhibition algae, and certain species of bacteria transform and and Photoprotection; Photosystem I; Protonation and store solar energy in the form of energy-rich organic ATP Synthesis; Global Aspects of Photosynthesis; molecules. These compounds are in turn used as the Functional Genomics; History of Photosynthesis; energy source for all growth and reproduction in The Chlorophylls; The Cytochromes; The Chloro- these and almost all other organisms. As such, plast; Laboratory Methods for Studying Leaves and virtually all life on the planet ultimately depends on Whole Plants; and C-3 and C-4 Plants. In view of the photosynthetic energy conversion. Respiration, which interdisciplinary character of research in photo- occurs in mitochondrial and bacterial membranes, synthesis and respiration, it is my earnest hope that utilizes energy present in organic molecules to fuel a this series of books will be used in educating students wide range of metabolic reactions critical for cell and researchers not only in Plant Sciences, Molecular growth and development. In addition, many and Cell Biology, Integrative Biology, Biotechnology, photosynthetic organisms engage in energetically Agricultural Sciences,Microbiology,Biochemistry, wasteful photorespiration that begins in the and Biophysics, but also in Bioengineering, chloroplast with an oxygenation reaction catalyzed Chemistry, and Physics. by the same enzyme responsible for capturing carbon I take this opportunity to thank Eva-Mari Aro; dioxide in photosynthesis. This series of books spans Bertil Andersson; all the authors of volume 11; Larry topicsfrom physics to agronomy and medicine, from Orr; Jacco Flipsen, Gloria Verhey; and my wife femtosecond processes to season long production, Rajni Govindjee for their valuable help and support from the photophysics of reaction centers, through that made the publication of Regulatory Aspects of the electrochemistry of intermediate electron transfer, Photosynthesis possible. to the physiology of whole organisms, and from Readers are requested to send their suggestions X-ray crystallography of proteins to the morphology for future volumes, authors or editors to me by of organelles and intactorganisms. The intent of the E-mail ([email protected]) or fax (1-217-244-7246). series is to offer beginning researchers, advanced undergraduatestudents,graduate students, and even May 14, 2001 research specialists, a comprehensive, up-to-date Govindjee picture of the remarkable advances across the full Series Editor, scope of research on bioenergetics and carbon Advances in Photosynthesis and Respiration metabolism. University of Illinois at Urbana-Champaign Department of Plant Biology Future Books 265 Morrill Hall 505 South Goodwin Avenue The readers of the current series are encouraged to Urbana, IL 61801-3707, U.S.A. watch for the publication of the forthcoming books: (1) Light-harvesting Antennas in Photosynthesis Email: [email protected] (Editors:B.R. Green and W.W. Parson); URL: http://www.life.uiuc.edu/govindjee (2) Photosynthesis in Algae (Editors: A.W.D. Larkum, S. Douglas, and J.A. Raven); vi Contents Editorial v Contents vii Preface xvii Color Plates CP-1 Part I: Evolution, Complexity andRegulation ofPhotosynthetic Structures 1 Thylakoid Biogenesis and Dynamics:The Result ofa Complex Phylogenetic Puzzle 1–28 Reinhold. G. Herrmann and Peter Westhoff Summary 1 I. Introduction 2 II. Aspectsof Chloroplast and PlantGenome Evolution—Plant Genome Structure 5 III. Functional Consequences of Genome Rearrangement—Regulatory Levels 11 IV. The Impact of Multicellularity and Terrestrial Life upon Thylakoid Biogenesis 18 V. Maintenance and Acclimation ofThylakoids 19 VI. Outlook—NewApproaches 21 Acknowledgments 23 References 23 Part II: Gene Expression andSignalTransduction 2 Plastid RNA Polymerases in Higher Plants 29–49 Karsten LiereandPalMaliga Summary 29 I. Introduction 30 II. The Plastid-Encoded Plastid RNAPolymerase (PEP) 31 III. The Nuclear-Encoded Plastid RNAPolymerase (NEP) 39 IV. The RoleofNEPand PEP in PlastidGene Expression 43 V. Unsolved Mystery: tRNA Transcription 43 Acknowledgments 44 References 44 vii 3 Phytochrome and Regulation Of Photosynthetic Gene Expression 51–66 Michael Malakhov and Chris Bowler Summary 51 I. Introduction 52 II. Activation of Phytochrome and Other Photoreceptors 52 III. Second Messengers in Phytochrome Signal Transduction 53 IV. Genetic Approaches to Dissect Phytochrome Signaling 54 V. Nuclear-Localized Components of the Light Signaling Machinery 57 VI. Interactions Between Phytochrome and Other Signaling Pathways 61 VII. Concluding Remarks 62 Acknowledgments 62 References 63 4 Regulating Synthesis ofthe Purple Bacterial Photosystem 67–83 Carl E. Bauer Summary 67 I. Introduction 68 II. The Purple Bacterial Photosystem 68 III. The Photosynthesis Gene Cluster 69 IV. Regulating PhotosystemSynthesis 70 V. Concluding Statements 79 Acknowledgment 79 References 79 5 Redox Regulation of Photosynthetic Genes 85–107 Gerhard Link Summary 85 I. Introduction 86 II. Redox Regulation of Nuclear Genes for Photosynthetic Proteins 89 III. Redox Regulation of Gene Expression Inside the Chloroplast 93 IV. Outlook 100 Acknowledgments 102 References 102 6 Sugar Sensing and Regulation of Photosynthetic Carbon Metabolism 109–120 Uwe Sonnewald Summary 109 I. Photosynthetic Carbon Metabolism in Plants 110 II. Sink Regulation of Photosynthesis 112 III. Sugar Regulation of Gene Expression 114 Acknowledgment 118 References 118 viii 7 Editing, Polyadenylation and Degradation of mRNA in the Chloroplast 121–126 Gadi Schuster and Ralph Bock Summary 121 I. Introduction 122 II. RNA Editing in the Chloroplast 122 III. Polyadenylation and Degradation of mRNA in the Chloroplast 126 Acknowledgments 132 References 133 8 Regulation of Chloroplast Translation 137–151 Aravind Somanchi and Stephen P. Mayfield Summary 137 I. Introduction 138 II. Translation in the Chloroplast—An Overview 138 III. Translational Regulation in the Chloroplast 139 IV. Mechanism of Translational Activation 145 V. Conclusions and Perspectives 147 References 148 Part III: Biogenesis, Turnover and Senescence 9 Proteins Involved in Biogenesis of the Thylakoid Membrane 153–175 Klaas Jan van Wijk Summary 153 I. Introduction 154 II. Chloroplast Proteins Involved in Targeting and Insertion into the Thylakoid Membrane 155 III. Peptidases and Proteases Responsible for Processing and Turnover 161 IV. Proteins involved in Folding and Post-translational Modifications 162 V. Proteins Assisting in Protein and Cofactor Transport, Storage and Ligation 163 VI. Vesicles Formation, Low Density Membranes and Tubules 167 VII. Proteomics as a Tool for Identification of Proteins involved in Thylakoid Biogenesis 168 VIII. Conclusions and Perspectives 169 Acknowledgments 170 References 170 10 Peptidyl-Prolyl Isomerases and Regulation of Photosynthetic Functions 177–193 Alexander V. Vener Summary 177 I. Introduction 178 II. Structure and Function of Peptidyl-Prolyl Isomerases (PPIases) 179 III. Plant PPIases 184 ix