Oxygenic Photosynthesis: The Light Reactions Advances in Photosynthesis VOLUME 4 Series Editor: GOVINDJEE Department of Plant Biology University of Illinois, Urbana, Illinois, U.S.A. Consulting Editors: Jan AMESZ, Leiden, The Netherlands Eva-Mari ARO, Turku, Finland James BARBER, London, United Kingdom Robert E. BLANKENSHIP, Tempe, Arizona, U.S.A. Norio MURATA, Okazaki, Japan Donald R. ORT, Urbana, Illinois, U.S.A. Advances in Photosynthesis is an ambitious new book series seeking to provide a comprehensive and state-of-the-art account of photosynthesis research. 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 organisms. As such, virtually all life on the planet ultimately depends on photosynthetic energy conversion. This series of multiauthored books spans topics from physics to agronomy, from femtosecond reactions to season long production, from the photophysics of reaction centers to the physiology of whole organisms, and from X-ray crystallography of proteins to the morphology of intact plants. The intent of this new series of publications is to offer beginning researchers, graduate students, and even research specialists a comprehensive current picture of the remarkable advances across the full scope of photosynthesis research. The titles to be published in this series are listed on the backcover of this volume. Oxygenic Photosynthesis: The Light Reactions Edited by Donald R. Ort USDA/ARS, Photosynthesis Research Unit, University of Illinois, Urbana, Illinois, U.S.A. and Charles F. Yocum Department of Biology/Chemistry, University of Michigan, Ann Arbor, Michigan, U.S.A. Assistant Editor Iris F. Heichel University of Illinois KLUWER ACADEMIC PUBLISHERS NEW YORK,BOSTON, DORDRECHT, LONDON, MOSCOW eBookISBN: 0-306-48127-8 Print ISBN: 0-7923-3683-6 ©2004 Kluwer Academic Publishers NewYork, Boston, Dordrecht, London, Moscow Print ©1996 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 eBookstore at: http://ebooks.kluweronline.com Contents Preface xv Introduction 1 Electron Transfer and Energy Transduction in Photosynthesis: An Overview 1–9 D. R. Ort and C. F. Yocum Summary 1 I. Introduction 2 II. Thylakoid Membranes: Energy Trapping and Electron Transfer Reactions 2 III. Energy Conservation In Thylakoid Membranes 6 IV. Molecular Biology of Thylakoids 7 Acknowledgments 9 References 9 Thylakoid Membranes: Structure 2 Structure, Composition, Functional Organization and Dynamic Properties of Thylakoid Membranes 11–30 L. Andrew Staehelin and Georg W. M. van der Staay Summary 11 I. Structural Organization and Compartmentalization of Chloroplasts 12 II. Composition and Distribution of AcylLipids in Thylakoid Membranes 13 III. The Photosynthetic Electron Transport Chain: Components and Functional Organization 16 IV. Composition of the Five Complexes of the Thylakoid Membrane 18 V. Lateral Distribution of Protein Complexes Between Grana and Stroma Membrane Regions 18 VI. Macromolecular Organization of Thylakoid Membranes: Correlative Freeze-fracture, Freeze-etch and Biochemical Studies 19 VII. Why do Thylakoid Membranes Form Grana Stacks? 25 VIII. Alteration in Thylakoid Membrane Composition and Organization in Response to Changes in the Light Environment 25 Acknowledgments 27 References 27 3 Evolution of Thylakoid Structure 31–40 Gregory R. Wolfe and J. Kenneth Hoober Summary 31 I. Introduction 31 II. Photosystems 31 III. Light-Harvesting Complexes 35 IV. ThylakoidMorphology 36 V. Conclusions 37 References 38 Thylakoid Membranes: Synthesis and Assembly of Thylakoid Membranes 4 Control ofThylakoid Membrane Development and Assembly 41–58 AndrewN.Webberand Neil R.Baker Summary 41 I. Introduction 42 II. Multimeric Protein Complexes 42 III. PhotochemicalActivities 50 IV. Environmental Influences 52 V. Concluding Remarks 53 Acknowledgments 53 References 53 5 Development of Thylakoid Membrane Stacking 59–68 LászlóMustárdy Summary 59 I. Introduction 60 II. ReconstitutionofThree-dimensional ThylakoidArrangement 60 III. OntogeneticAssembly ofThylakoidsViewedin Three-dimensions 63 IV. PossibleFunctionalRoleofHelicalArrangement 66 References 67 6 Biosynthesis ofThylakoid Membrane Lipids 69–101 Roland DouceandJacquesJoyard Summary 69 I. Introduction 70 II. Characterization and Biosynthesis ofChloroplastGlycerolipids 70 III. Characterization and Biosynthesis ofChloroplast Prenyllipids 82 IV. Transfer of LipidConstituentsbetween Envelopeand Thylakoids 92 V. Future Prospects 94 Acknowledgments 95 References 95 7 Targeting of Proteins Into and Across theThylakoid Membrane 103–112 Colin Robinson Summary 103 I. Introduction 104 II. SitesofSynthesisofThylakoid Proteins 104 III. Insertionof Proteinsinto theThylakoid Membrane 104 IV. Translocation ofLumenal ProteinsAcrosstheThylakoid Membrane 107 V. Concluding Remarks 110 References 111 vi The Photosynthetic Apparatus: Oxygen Evolution 8 Introduction to Oxygen Evolution and the Oxygen-Evolving Complex 113–136 Terry M. Bricker and Demetrios F. Ghanotakis Summary 113 I. Introduction 114 II. Photosystem II Preparations 115 III. The Proteins of Photosystem II 116 III. Inorganic Cofactors of Photosystem II 125 IV. The Mechanism of WaterOxidation 128 V. Conclusions 129 Acknowledgments 129 References 129 9 Oxygen Evolution 137–164 R. David Britt Summary 137 I. Introduction and Overview 138 II. Kinetics and Thermodynamics of Oxygen Evolution 139 III. Structural Studies 141 IV. Manganese Cluster Ligation 148 V. Water Oxidation Mechanisms 154 Acknowledgments 159 References 159 10 Protons and Charge Indicators in Oxygen Evolution 165–192 Michael Haumann and Wolfgang Junge Summary 165 I. Introduction 166 II. Materials and Techniques 167 III. Extents and Rates of Proton Release During the Redox Transitions 174 IV. Structural and Mechanistic Considerations 184 Acknowledgments 187 References 187 The Photosynthetic Apparatus: Photosystem II 11 Introduction tothe Photosystem II Reaction Center—Isolation and Biochemical and Biophysical Characterization 193–211 Kimiyuki Satoh Summary 193 I. Introduction 194 II. Isolation 195 III. Chemical Composition and Polypeptide Sequence 196 IV. Functional Aspects of PS II RC Organization—Energy and Electron TransferProcesses 200 vii V. Structural Aspects of Organization—Structure of the Primary Donor (P680) 203 VI. Perspectives 207 References 207 12 Structure, Dynamics, and Energy Conversion Efficiency in Photosystem II 213–247 Bruce A. Diner and Gerald T. Babcock Summary 214 I. Introduction 214 II. Biochemical and Pigment Organization of Photosystem II 218 III. Absorption Characteristics and Organization of Pigments in Photosystem II 218 IV. Primary Photochemistry 222 V. Secondary Electron Transfer 226 Acknowledgments 240 References 240 13 Form and Function of Cytochrome b-559 249–264 John Whitmarsh and Himadri B. Pakrasi Summary 249 I. Introduction 250 II. Cytochrome b-559 Structure 250 III. Cytochrome b-559 Forms in Photosystem II 252 IV. Cytochrome b-559 Function 257 Acknowledgments 260 References 260 14 Photosystem II Heterogeneity 265–287 Jérôme Lavergne and Jean-Marie Briantais Summary 265 I. Introduction 266 II. Static Heterogeneities: Basic Data 267 III. Possible Correlations 274 IV. Dynamic Heterogeneities 276 VI. Conclusions 281 Acknowledgments 281 References 282 The Photosynthetic Apparatus: Photosystem I 15 Introduction to Photosystem I: Reaction Center Function, Composition and Structure 289–311 Rachel Nechushtai, Amir Eden, Yuval Cohen and Judith Klein Summary 290 I. Introduction 290 II. The Composition and Function of PS I Components 292 III. The Organization and Structure of Photosystem I 298 Acknowledgments 306 References 306 viii 16 Photosystem I Electron Transfer Reactions—Components and Kinetics 313–332 Richard Malkin Summary 313 I. Introduction 314 II. Electron Carriers in PS I 314 III. Kinetics of PS I Electron Transfer Reactions 321 IV. Cyclic Electron Transfer and Cyclic Phosphorylation 327 Acknowledgments 329 References 329 17 Ferredoxin and Ferredoxin-Dependent Enzymes 333–361 David B. Knaff Summary 333 I. Introduction 334 II. Ferredoxin 334 III. Ferredoxin:NADP+ Oxidoreductase (FNR) 339 IV. Nitrite Reductase 346 V. Glutamate Synthase 349 VI. Thioredoxin Reductase 351 VII. Conclusion 353 Acknowledgments 353 References 354 18 Structure Analysis of Single Crystals of Photosystem I by X-Ray, EPR and ENDOR: A Short Status Report 363–375 H. T. Witt Summary 363 I. Introduction 364 II. The PS I Complex of Cyanobacterium Synechococcuselongatus 364 III. Crystallization of the Trimer of PS I 365 IV. X-Ray Structure Analysis of Single Crystals of PS I at 4.5 Å Resolution 365 V. EPR Structure Analysis of P700 and the Fe-S clusters in PS I Complexes and Single Crystals at Low Temperature 370 VI. ENDOR Structure Analysis of P700 in Single Crystals of PS I at Low Temperature 371 Acknowledgments 374 References 374 The Photosynthetic Apparatus: Components of Intersystem Elec- tronTransfer 19 The Cytochrome Complex—Composition, Structure and Function 377–398 Günter Hauska, Michael Schütz and Michael Büttner Summary 377 I. Introduction 378 II. Occurrence 378 III. Isolation 380 ix IV. Components and Structure 380 V. Function 387 VI. Regulation 391 VIII. Conclusions and Open Questions 392 Acknowledgments 393 Note in Proof 394 References 394 20 Basic Aspects of Electron and Proton Transfer Reactions with Applications to Photosynthesis 399–411 Lev I. Krishtalik and William A. Cramer Summary 399 I. Introduction 400 II. Medium Reorganization in Electron Transfer 400 III. Transition Probability 402 IV. Proteins As Polar Media 402 V. Proteins As an Intervening Medium in Electron Transfer 403 VI. Pathways of Proton Transfer in Energy-Transducing Membranes 407 Acknowledgments 409 References 409 21 Plastocyanin: Structure, Location, Diffusion and Electron Transfer Mechanisms 413–429 Elizabeth L. Gross Summary 413 I. Introduction 414 II. Structure 414 III. The Interaction of Plastocyanin with Cytochrome f 420 IV. The Interaction of Plastocyanin with P700 423 V. The Function of Plastocyanin in the Lumen of the Thylakoid at Acid pH 425 VI. Conclusions 426 Acknowledgments 426 References 426 22 Some Consequences of the High Resolution X-Ray Structure Analysis of Cytochrome f 431–437 S. E. Martinez, D. Huang, J. L. Smith and W. A. Cramer Summary 431 I. Introduction 431 II. Preparation and Crystallization of TruncatedCytochrome f 432 III. Unprecedented Aspects of the Structure 434 IV. Other Major Properties of the Structure 434 V. Orientation of Cytochrome f Relative to the Membrane Plane 436 VI. Evolutionary Relation between Cytochromes f and 436 VII. Electron Transferfrom Cyt f to Plastocyanin 436 Acknowledgments 437 References 437 Summary 439 x