Table Of ContentEncyclopedia of
Plant Physiology
New Series Volume 19
Editors
A. Pirson, Gottingen
M. H. Zimmermann, Harvard
Photosynthesis ill
Photosynthetic Membranes
and Light Harvesting Systems
Edited by
L.A. Staehelin and C. J. Arntzen
Contributors
1. M. Anderson B. Andersson C. 1. Arntzen R. Bachofen
1. Barber 1. Barrett R. E. Blankenship P. Boger 1. Breton
T. M. Bricker R. 1. Cogdell 1. Deisenhofer R.A. Dilley
B. A. Diner T. 1. Donohue P. L. Dutton R. C. Fuller E. Gantt
N. E. Geacintov 1. A. Guikema W. Haehnel G. Hauska
1. E. Hearst A. 1. Hoff D. Holten A. R. Holzwarth A. 1oliot
P. 1oliot S. Kaplan K. Keegstra R. S. Knox D. 1. Kyle C. Lutz
P. Mathis R. E. McCarty B. A. Melandri H. Michel
D. 1. Murphy C. M. Nalin 1. R. Norris I. Ohad D. R. Ort
H. B. Pakrasi W. W. Parson R. C. Prince A. Rawyler
I. 1. Ryrie G. Sandmann K. Sauer H .. Scheer P. Setif
L.A. Sherman P. A. Siegenthaler D. J. Simpson S. G. Sprague
L.A. Staehelin H. Stratmann 1. P. Thornber D. M. Tiede
G. Van Brakel A. R. Varga G. Venturoli 1. Whitmarsh
V. Wiemken F.-A. Wollman C. F. Yocum H. Zuber
Springer-Verlag Berlin Heidelberg GmbH
Professor L. ANDREW STAEHELIN
Department of Molecular, Cellular,
and Developmental Biology
University of Colorado
Campus Box 347
Boulder, CO 80309
USA
Professor CHARLES J. ARNTZEN
E.I. du Pont de Nemours & Co.
Central Research and Development Department
Experimental Station
Bldg. 402, Room 3226
Wilmington, DE 19898
USA
With 163 Figures
ISBN 978-3-642-70938-8 ISBN 978-3-642-70936-4 (eBook)
DOI 10.1007/978-3-642-70936-4
Library of Congress Cataloging-in-Publication Data. (Revised for voL 3) Main entry under title: Photosyn
thesis. (Encyclopedia of plant physiology; new ser., v. 5-6, 19) Includes bibliographies and indexes. Contents:
1. Photosynthetic electron transport and photophosphorylation, edited by A. Trebst and M. Avron. 2.
Photosynthetic carbon metabolism and related processes, edited by M. Gibbs and E. Latzko. 3. Photosyn
thetic membranes and light harvesting systems, edited by L.A. Staehelin and C.J. Arntzen. 1. Photosynthesis
-Collected works. I. Trebst, Achim. II. Alberte, R.S. III. Series. QK711.2.E5 voL 5-6 581.1s [581.1'3342]
76-30357 [QK882] ISBN 978-3-642-70938-8
This work is subjected to copyright. All rights are reserved, whether the whole or part of the material is concerned,
specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying
machine or similar means, and storage in data banks.
Under §54 of the German Copyright Law where copies are made for other than private use, a fee is payable
to ,Verwertungsgesellschaft Wort" Munich
©Springer-Verlag Berlin Heidelberg 1986
Originally published by Springer-Verlag Berlin Heidelberg New York Tokyo 1986
Softcover reprint of the hardcover I st edition 1986
The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific
statement, that such names are exempt from the relevant protective laws and regulations and therefore free for
general use.
Preface
The Encyclopedia of Plant Physiology series has turned several times to the
topic of photosynthesis. In the original series, two volumes edited by A. PIRSON
and published in 1960 provided a broad overview of the entire field. Although
the New Series has devoted three volumes to the same topic, the overall breadth
of the coverage has had to be restricted to allow for greater in-depth treatment
of three major areas of modern photosynthesis research: I. Photosynthetic Elec
tron Transport and Photophosphorylation (Volume 5 edited by A. TREBST and
M. AvRON, and published in 1977); II. Photosynthetic Carbon Metabolism
and Related Processes (Volume 6 edited by M. GIBBS and E. LATZKO, and
published in 1979); and III. Photosynthetic Membranes and Light-Harvesting
Systems (this volume).
As we approached the organization of the current volume, we chose a set
of topics for coverage that would complement the earlier volumes, as well as
provide updates of areas that have seen major advances in recent years. In
addition, we wanted to emphasize the following changes in the study of photo
synthetic systems which have become increasingly important since 1977: the
trend toward increased integration of biochemical and biophysical approaches
to study photosynthetic membranes and light-harvesting systems, and a renewed
appreciation of the structural parameters of membrane organization.
Due to the increased complexity of the field, we also decided to try a new
format for our volume to better serve the following two purposes. First, we
believe a review volume on photosynthetic membranes should serve as a refer
ence source for nonspecialists interested in obtaining an overview of both oxy
genic and anoxygenic photosynthesis. This need has been answered by the inclu
sion of five introductory chapters which summarize the main broad topic areas
of the volume. We also recognize that a review volume should provide insight
to the "state of the art" in specific research areas which have seen major recent
advances. To this end, Chapters 6 through 11 have been organized such that
each consists of a number of minireviews related to a common theme. All
of the 43 minireviews are authored by highly regarded specialists, and focus
on recent research highlights and interpretations of significant new findings.
Great emphasis has been placed on the integration of the materials covered
in the introductory chapters and in the minireviews. Extensive cross-referencing
has been used to allow easy transitions by the reader from a general to a
specialized coverage of a topic. Similarly, all minireviews contain references
to the appropriate introductory chapters, as well as to other minireviews.
VI Preface
With students in mind, the authors of the introductory chapters have stressed
integrative and comparative aspects of their topics. This type of approach is
becoming more and more relevant in photosynthesis research, thanks to the
convergence of information coming from structural, biophysical, and biochemi
cal studies. Indeed, it is truly exciting to witness the progress being made toward
the goal of a molecular understanding of the diverse biophysical and biochemical
reactions associated with photosynthetic membranes and light-harvesting sys
tems.
The specialized chapters in this volume begin with the topic of light harvest
ing by photosynthetic membranes. The minireviews of Chapter 6 summarize
biochemical and structural studies of light-harvesting assemblages, with empha
sis on the light-harvesting components of bacteria and algae, since higher plant
chloroplast components are extensively reviewed in Chapter 3. Whereas Chapter
6 emphasizes the biochemical diversity in light-harvesting systems, Chapter 7
consists of minireviews which discuss unifying concepts governing light-harvest
ing events. All authors in this section are concerned with photon absorption
and structural parameters of the pigment bed that determine the efficiency of
excitation energy transfer to reaction centers.
The most fundamental result of photosynthetic light reactions is the conver
sion of excitation energy, derived from absorbed light, into stable chemical
form. This occurs in the reaction center (RC). In the last 5 years there have
been major advancements in the understanding of these processes - especially
by those groups who have focused their work on photosynthetic bacteria. The
identity of the cofactors (chlorophyll, pheophytin, quinones, etc.) involved in
the initial charge separations and the events involved in charge stabilization
are now highly defined. The minireviews of Chapter 8 present various aspects
of this rapidly moving field, ranging from energetic considerations of the RC
to discussions of similarities and differences among the different types of protein
which comprise different reaction centers.
Chapter 9 makes a transition from the highly defined bacterial reaction
centers into the less well understood photosystems I and II of green plants.
The inclusion of several minireviews devoted to the complexity of reactions
in photosystem II, for example, reflects the wide diversity in studies of a system
capable of extracting electrons from water and catalyzing a stable charge separa
tion that results in reduction of the plastoquinone pool. These studies extend
from detailed understanding of the primary reactions to physiological adapta
tion of the process to light and chemical (herbicide) stresses.
The reaction centers of prokaryotic and eukaryotic photosynthetic mem
branes produce high energy electrons which are utilized in electron transport
reactions. The energy released in these reactions is coupled to A TP synthesis.
The membrane components and processes involved in the energy-coupling reac
tions are the topic of Chapter 10. Minireviews in this section are strongly bio
chemical in emphasis, with special reference to the structural organization of
membranes and the protein complexes which mediate proton translocation and
ATP biosynthesis. Specific enzymes involved in electron transport and inhibitors
which affect them are reviewed in light of information obtained since 1977.
Preface VII
The last chapter of this volume (Chap. 11) deals with the use of integrative
approaches to study processes associated with control of photosynthetic mem
brane assembly and maintenance. Chapter 11 includes subject material ranging
from comparative structural analysis of photosynthetic membranes (develop
mental diversity) to the use of physical analysis of membranes or simulated
membrane systems to characterize functional components. The minireviews of
this chapter will be of increasing value as the field of membrane biosynthesis
and assembly matures to use more information about physical and biochemical
features of the photosynthetic membranes. We can anticipate the advent of
use of genetic engineering tools to manipulate photosynthetic membranes, and
the rapid expansion of knowledge in this area.
In summary, this volume is a selection of both overview chapters and numer
ous topical speciality reviews. It should be useful as a reference source and
as a teaching aid for individuals interested in the rapidly expanding field of
photosynthetic membranes.
Boulder and Wilmington, Spring 1986 L.A. STAEHELIN
C.J. ARNTZEN
Contents
1 Chloroplast Structure and Supramolecular Organization of
Photosynthetic Membranes
L.A. STAEHELIN (With 45 Figures)
1 Introduction . . . . . . . . 1
2 Chloroplast Morphology . . . 1
2.1 Light Microscopic Observations 1
2.2 The Chloroplast Envelope 2
2.2.1 Higher Plants . . . . . 2
2.2.1.1 Morphology and Isolation 2
2.2.1.2 Infoldings of the Inner Envelope Membrane 4
2.2.2 Algae . . . . . . 5
2.3 Chloroplast Stroma . . . 10
2.3.1 Matrix Components 10
2.3.2 Plastoglobuli 11
2.3.3 Pyrenoids . . . . . 11
2.3.4 Eyespots . . . . . 13
2.4 Arrangement of Thylakoids 14
2.4.1 Thylakoids of Oxygen-Evolving Prokaryotes 16
2.4.1.1 Cyanobacteria . . . . . . . . . 16
2.4.1.2 Prochlorons . . . . . . . . . . 19
2.4.2 Higher Plant Thylakoids . . . . . . . . 19
2.4.2.1 Three-Dimensional Organization of Grana and Stroma
Thylakoids . . . . . . . . . . . . . . . . . . . 19
2.4.2.2 Normal Development of Grana and Stroma Thylakoids 20
2.4.2.3 Thylakoid Membrane Nomenclature . . . . . . . . . 22
2.4.2.4 Naturally and Experimentally Induced Variations in the
Ratio of Stacked to Unstacked Membrane Regions 23
2.4.3 Green Algal Thylakoids 25
2.4.4 Euglenoid Thylakoids . . . . . . . 25
2.4.5 Red Algal Thylakoids . . . . . . . 26
2.4.6 Chromophytan Thylakoids . . . . . 28
2.4.6.1 Cryptophyceae (Cryptomonads) 28
2.4.6.2 Phaeophyceae (Brown Algae) and Bacillariophyceae
(Diatoms) . . . . . . . . . . . . . . 28
2.4.6.3 Chrysophyceae (Golden-Brown-Algae) and
Xanthophyceae (Yellow-Green Algae) 29
2.4.6.4 Dinophyceae (Dinoflagellates) 29
3 Supramolecular Organization of Thylakoids 30
3.1 Freeze-Fracture (-Etch) Electron Microscopy 30
3.2 Higher Plant and Green Algal Thylakoids 32
3.2.1 Photosystem II Complexes 34
3.2.2 Photosystem I Complexes . . . . . 39
3.2.3 Cytochrome b /f Complex 40
6
3.2.4 CF -CF ATP Synthase . . . . . 42
0 1
3.2.5 Chlorophyll ajb Light-Harvesting Complex 44
X Contents
3.2.5.1 "Mobile" Versus "Bound" Forms of Chi ajb LHC 44
3.2.5.2 Chi ajb LHC as Membrane Adhesion Factor . . 45
3.2.5.3 Reconstitution and Structural Characterization 45
3.2.6 Why Do Chloroplasts Need Grana? . . . . . . . . . 47
3.2.7 Supramolecular Organization of Thylakoids-a Summary 48
3.3 Prochloron Thylakoids . . . . . . . . . . . . . . . . . . 51
3.4 Thylakoid Membranes of Cyanobacteria, Red Algae and Cyanelles 53
3.4.1 Identification of Freeze-Fracture Particles . . . . . . . . . 53
3.4.2 Relationship Between Phycobilisomes and EF Particles (PS II
Complexes) . . . . . . . . . . 56
3.5 Thylakoid Membranes of Chromophyta 58
3.5.1 Cryptophyceae . . . . . . . . 59
3.5.2 Phaeophyceae and Dinophyceae . 60
4 Experimental Modification of Thylakoid Membrane Structure 61
4.1. Structural Changes Associated with in Vitro Unstacking and
Restacking of Thylakoids . . . . . . . . . . . . . . . 61
4.2 State I/State II Transitions - Functional Regulation Mediated by
Structural Rearrangements . . . . . . . . . . . . . . . . . 64
4.3 Temperature-Induced Changes in Thylakoid Membrane Organization 66
4.3.1 Effects of Heat Stress 66
4.3.2 Chilling Effects . . . . . . . . . 67
4.3.2.1 Higher Plants . . . . . . 67
4.3.2.2 Thermophilic Cyanobacteria 69
4.4 Prothylakoids and Prolamellar Bodies 70
References . . . . . . . . . . . . . . . . . 72
2 Photosynthetic Light Reactions - Physical Aspects
K. SAUER (With 5 Figures)
1 Introduction . . . . . . . . . . . 85
2 Radiation - Sunlight . . . . . . . 86
3 The Excitation of Pigment Molecules 88
4 Excitation Transfer . . . . . . . . 90
5 Electron Transfer - Charge Separation in the Reaction Center 92
6 The Reaction Center - Structure and Function 93
7 Conclusion 95
References . . . . . . . . . . . . . . . . . 96
3 Biochemical Characterization and Structure of Pigment-Proteins of
Photosynthetic Organism
J.P. THORNBER (With 4 Figures)
1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . 98
2 Development of the Subject . . . . . . . . . . . . . . . . . . . 100
2.1 Historical Development of Our Understanding of Plant Chlorophyll-
Proteins . . . . . . . . . . . . . . . . . . . . . 100
2.2 Development of Our Knowledge of Pigment-Proteins of
Photosynthetic Bacteria . . . . . . . . . . . . . . 106
3 The State of Knowledge of the Biochemical Organization of
Photosynthetic Pigments in Plants and Bacteria 107
3.1 Photosystem I of Green Plants . . . . . 109
3.1.1 Core Complex I (CCI) . . . . . . 109
3.1.2 Light-Harvesting Complex I (LHC I) 111
3.2 Photosystem II 112
3.2.1 CCII 112
3.2.2 LHC II . 113
Contents XI
3.3 Pigment-Protein Complexes of the Algae . . . . 116
3.4 Pigment-Protein Complexes of the Cyanobacteria 117
3.5 Purple Bacteria . . . . . . . . . . . . . . . 119
3.5.1 Photochemical Reaction Centers . . . . . 119
3.5.2 The Light-Harvesting Pigment-Protein Complexes 123
3.5.2.1 The B-800-850 Complex . . . . . . . . 123
3.5.2.2 The B-890-Protein Complex . . . . . . 125
3.5.3 Topography of the Antenna and Reaction Center Complexes 125
3.6 Chlorophyll-Protein Complexes of the Green Bacteria 126
4 Concluding Remarks . . . . . . . . . . . . . . . 127
4.1 Isolation of the Pigment-Protein Complexes 128
4.2 The Structure of the Chlorophyll-Protein Complexes 132
References . . . . . . . . . . . . . . . . . . . . . 135
4 Energy Transduction in Oxygenic Photosynthesis: an Overview of
Structure and Mechanism
D.R. ORT (With 7 Figures)
1 Introduction . . . . . . . . . . . . 143
2 The Chloroplast Thylakoid Membrane . 146
2.1 Thylakoid Membrane Morphology 146
2.2 Chemical Composition and Physical Properties of the Thylakoid
Membrane . . . . 149
2.2.1 Composition 149
2.2.1.1 Lipids 150
2.2.1.2 Polypeptides 152
2.2.1.3 Carbohydrates 154
2.2.2 Physical Properties . . 154
2.3 Distribution of Thylakoid Membrane Components 156
2.3.1 Transmembrane Asymmetry 156
2.3.2 Lateral Asymmetry 157
3 Photosystem II Complex . . . . . . 158
3.1 Composition and Structure . . . 158
3.2 Primary Electron Transfer Events 161
3.3 The Acceptor-Side Reactions of Photosystem II Electron Transfer 162
3.3.1 The Two-Electron Gate . . . . . . . . . . . . 163
3.3.2 Mode of Inhibition by Photosystem II Herbicides 164
3.4 Water Oxidation and Donor-Side Reactions 165
3.4.1 The Reduction of p+ -680 165
3.4.2 Water Oxidation . . 166
4 Photosystem I Complex . . . . . 168
4.1 Composition and Structure . . 168
4.2 Primary Electron Transfer Events 169
4.3 Electron Donors to Photosystem I 170
4.4 The Acceptor-Side Components and Reactions of Photo system I 171
5 Intersystem Electron Transfer 172
5.1 Cytochrome b /f Complex . . . . . . . . . . 173
6
5.1.1 Composition and Structure . . . . . . . 173
5.1.2 Mechanism of the Oxidation of Plastoquinol 174
5.1.3 Involvement of the Cytochrome b /f Complex in Cyclic Electron
6
Flow Around Photosystem I 176
5.2 Mobile Electron Carriers . . . . . . . 177
6 Photophosphorylation . . . . . . . . . . . . . . . . . . 179
6.1 Mechanism and Energetic Considerations . . . . . . . 179
6.2 "Phosphorylating Unit" . . . . . . . . . . . . . . . 181
6.2.1 Distribution and Stoichiometry of Components of the
Phosphorylating Unit . . . . . . . . . . . . . 181
