Encyclopedia of
Plant Physiology
New Series Volume 19
Editors
A. Pirson, Göttingen
M. H. Zimmermann, Harvard
Photosynthesis IQ
Photosynthetic Membranes
and Light Harvesting Systems
Edited by
L. A. Staehelin and C. J. Arntzen
Contributors
J.M.Anderson B.Andersson C.J.Arntzen R.Bachofen
J.Barber J.Barrett R.E.Blankenship RBöger J.Breton
T.M.Bricker R.J.Cogdell J. Deisenhofer R.A.Dilley
B.A.Diner T.J.Donohue P.L.Dutton R.C.Fuller E.Gantt
N. E. Geacintov J. A. Guikema W.Haehnel G.Hauska
J.E.Hearst A.J.Hoff D.Holten A.R.Holzwarth A.Joliot
P.Joliot S.Kaplan K.Keegstra R.S.Knox D.J.Kyle C.Lütz
P.Mathis R.E.McCarty B.A.Melandri H.Michel
D.J.Murphy C.M.Nalin J.R.Norris I.Ohad D.R.Ort
H. B.Pakrasi W.W.Parson R.C.Prince A.Rawyler
I. J.Ryrie G.Sandmann K.Sauer H.Scheer P.Sétif
L.A.Sherman P.A.Siegenthaler D.J.Simpson S.G.Sprague
L. A. Staehelin H.Strotmann J.P.Thornber D.M.Tiede
G. Van Brakel A. R. Varga G. Venturoli J. Whitmarsh
V.Wiemken F.-A.Wollman C.F.Yocum H. Zuber
Springer-Verlag
Berlin Heidelberg New York Tokyo
Professor L . A N D R E W STAEHELIN
Department of Molecular, Cellular,
and Developmental Biology
University of Colorado
Campus Box 347
Boulder, C O 80309
USA
Professor CHARLES J. A R N T Z E N
E.I. du Pont de Nemours & Co.
Central Research and Development Department
Experimental Station
Bldg. 402, Room 3226
Wilmington, D E 19898
USA
With 163 Figures
ISBN 3-540-16140-6 Springer-Verlag Berlin Heidelberg New York Tokyo
ISBN 0-387-16140-6 Springer-Verlag New York Heidelberg Berlin Tokyo
Library of Congress Cataloging-in-Publication Data. (Revised for vol. 3) Main entry under title: Photosynthesis. (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. Photosynthetic 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 0-387-07962-9 (v. 1)
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
© by Springer-Verlag Berlin Heidelberg 1986
Printed in Germany
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.
Typesetting, printing and bookbinding: Universitätsdruckerei H Stürtz AG, Würzburg
2131/3130-543210
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 . PERSON
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 Electron 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 . L A T Z K O , 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 photosynthetic 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 reference source for nonspecialists interested in obtaining an overview of both oxygenic and anoxygenic photosynthesis. This need has been answered by the inclusion 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 biochemical 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 systems.
The specialized chapters in this volume begin with the topic of light harvesting by photosynthetic membranes. The minireviews of Chapter 6 summarize
biochemical and structural studies of light-harvesting assemblages, with emphasis 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-harvesting 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 conversion 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 R C
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 separation that results in reduction of the plastoquinone pool. These studies extend
from detailed understanding of the primary reactions to physiological adaptation of the process to light and chemical (herbicide) stresses.
The reaction centers of prokaryotic and eukaryotic photosynthetic membranes produce high energy electrons which are utilized in electron transport
reactions. The energy released in these reactions is coupled to A T P synthesis.
The membrane components and processes involved in the energy-coupling reactions are the topic of Chapter 10. Minireviews in this section are strongly biochemical 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.
VII
Preface
The last chapter of this volume (Chap. 11) deals with the use of integrative
approaches to study processes associated with control of photosynthetic membrane assembly and maintenance. Chapter 11 includes subject material ranging
from comparative structural analysis of photosynthetic membranes (developmental 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 numerous 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
2 Chloroplast Morphology
2.1 Light Microscopic Observations
2.2 The Chloroplast Envelope
2.2.1 Higher Plants
2.2.1.1 Morphology and Isolation
2.2.1.2 Infoldings of the Inner Envelope Membrane
2.2.2 Algae
2.3 Chloroplast Stroma
2.3.1 Matrix Components
2.3.2 Plastoglobuli
2.3.3 Pyrenoids
2.3.4 Eyespots
2.4 Arrangement of Thylakoids
2.4.1 Thylakoids of Oxygen-Evolving Prokaryotes
2.4.1.1 Cyanobacteria
2.4.1.2 Prochlorons
2.4.2 Higher Plant Thylakoids
2.4.2.1 Three-Dimensional Organization of Grana and Stroma
Thylakoids
2.4.2.2 Normal Development of Grana and Stroma Thylakoids
2.4.2.3 Thylakoid Membrane Nomenclature
2.4.2.4 Naturally and Experimentally Induced Variations in the
Ratio of Stacked to Unstacked Membrane Regions . .
2.4.3 Green Algal Thylakoids
2.4.4 Euglenoid Thylakoids
2.4.5 Red Algal Thylakoids
2.4.6 Chromophytan Thylakoids
2.4.6.1 Cryptophyceae (Cryptomonads)
2.4.6.2 Phaeophyceae (Brown Algae) and Bacillariophyceae
(Diatoms)
2.4.6.3 Chrysophyceae (Golden-Brown-Algae) and
Xanthophyceae (Yellow-Green Algae)
2.4.6.4 Dinophyceae (Dinoflagellates)
3 Supramolecular Organization of Thylakoids
3.1 Freeze-Fracture (-Etch) Electron Microscopy
3.2 Higher Plant and Green Algal Thylakoids
3.2.1 Photosystem II Complexes
3.2.2 Photosystem I Complexes
3.2.3 Cytochrome b / f Complex
6
1
1
1
2
2
2
4
5
10
10
11
11
13
14
16
16
19
19
19
20
22
23
25
25
26
28
28
28
29
29
30
30
32
34
39
40
3.2.4 C F Q - C F ! A T P Synthase
42
3.2.5 Chlorophyll a/b Light-Harvesting Complex
44
X
Contents
3.2.5.1 "Mobile" Versus "Bound" Forms of Chi a/b L H C . .
3.2.5.2 Chi a/b L H C as Membrane Adhesion Factor
3.2.5.3 Reconstitution and Structural Characterization . . . .
3.2.6 Why Do Chloroplasts Need Grana?
3.2.7 Supramolecular Organization of Thylakoids - a Summary . . .
3.3 Prochloron Thylakoids
3.4 Thylakoid Membranes of Cyanobacteria, Red Algae and Cyanelles
3.4.1 Identification of Freeze-Fracture Particles
3.4.2 Relationship Between Phycobilisomes and E F Particles (PS II
Complexes)
3.5 Thylakoid Membranes of Chromophyta
3.5.1 Cryptophyceae
3.5.2 Phaeophyceae and Dinophyceae
4 Experimental Modification of Thylakoid Membrane Structure
4.1. Structural Changes Associated with in Vitro Unstacking and
Restacking of Thylakoids
4.2 State I/State II Transitions - Functional Regulation Mediated by
Structural Rearrangements
4.3 Temperature-Induced Changes in Thylakoid Membrane Organization
4.3.1 Effects of Heat Stress
4.3.2 Chilling Effects
4.3.2.1 Higher Plants
4.3.2.2 Thermophilic Cyanobacteria
4.4 Prothylakoids and Prolamellar Bodies
References
2
44
45
45
47
48
51
53
53
56
58
59
60
61
61
64
66
66
67
67
69
70
72
Photosynthetic Light Reactions - Physical Aspects
K . SAUER (With 5 Figures)
1 Introduction
2 Radiation - Sunlight
3 The Excitation of Pigment Molecules
4 Excitation Transfer
5 Electron Transfer - Charge Separation in the Reaction Center
6 The Reaction Center - Structure and Function
7 Conclusion
References
3
85
86
88
90
92
93
95
96
Biochemical Characterization and Structure of Pigment-Proteins of
Photosynthetic Organism
J.P. THORNBER (With 4 Figures)
1 Introduction
2 Development of the Subject
2.1 Historical Development of Our Understanding of Plant ChlorophyllProteins
2.2 Development of Our Knowledge of Pigment-Proteins of
Photosynthetic Bacteria
3 The State of Knowledge of the Biochemical Organization of
Photosynthetic Pigments in Plants and Bacteria
3.1 Photosystem I of Green Plants
3.1.1 Core Complex I (CC I)
3.1.2 Light-Harvesting Complex I (LHC I)
3.2 Photosystem II
3.2.1 CCU
3.2.2 L H C II
98
100
100
106
107
109
109
Ill
112
112
113
Contents
XI
3.3 Pigment-Protein Complexes of the Algae
3.4 Pigment-Protein Complexes of the Cyanobacteria
3.5 Purple Bacteria
3.5.1 Photochemical Reaction Centers
3.5.2 The Light-Harvesting Pigment-Protein Complexes
3.5.2.1 The B-800-850 Complex
3.5.2.2 The B-890-Protein Complex
3.5.3 Topography of the Antenna and Reaction Center Complexes
3.6 Chlorophyll-Protein Complexes of the Green Bacteria
4 Concluding Remarks
4.1 Isolation of the Pigment-Protein Complexes
4.2 The Structure of the Chlorophyll-Protein Complexes
References
4
Energy Transduction in Oxygenic Photosynthesis: an Overview of
Structure and Mechanism
D.R. ORT (With 7 Figures)
1 Introduction
2 The Chloroplast Thylakoid Membrane
2.1 Thylakoid Membrane Morphology
2.2 Chemical Composition and Physical Properties of the Thylakoid
Membrane
2.2.1 Composition
2.2.1.1 Lipids
2.2.1.2 Polypeptides
2.2.1.3 Carbohydrates
2.2.2 Physical Properties
2.3 Distribution of Thylakoid Membrane Components
2.3.1 Transmembrane Asymmetry
2.3.2 Lateral Asymmetry
3 Photosystem II Complex
3.1 Composition and Structure
3.2 Primary Electron Transfer Events
3.3 The Acceptor-Side Reactions of Photosystem II Electron Transfer . .
3.3.1 The Two-Electron Gate
3.3.2 Mode of Inhibition by Photosystem II Herbicides
3.4 Water Oxidation and Donor-Side Reactions
3.4.1 The Reduction of P -680
3.4.2 Water Oxidation
4 Photosystem I Complex
4.1 Composition and Structure
4.2 Primary Electron Transfer Events
4.3 Electron Donors to Photosystem I
4.4 The Acceptor-Side Components and Reactions of Photosystem I
. .
5 Intersystem Electron Transfer
5.1 Cytochrome b /f Complex
5.1.1 Composition and Structure
5.1.2 Mechanism of the Oxidation of Plastoquinol
5.1.3 Involvement of the Cytochrome b /f Complex in Cyclic Electron
Flow Around Photosystem I
5.2 Mobile Electron Carriers
6 Photophosphorylation
6.1 Mechanism and Energetic Considerations
6.2 "Phosphorylating Unit"
6.2.1 Distribution and Stoichiometry of Components of the
Phosphorylating Unit
+
6
116
117
119
119
123
123
125
125
126
127
128
132
135
143
146
146
149
149
150
152
154
154
156
156
157
158
158
161
162
163
164
165
165
166
168
168
169
170
171
172
173
173
174
6
176
177
179
179
181
181
XII
Contents
6.2.2 Localized vs. Delocalized Coupling
6.3 Coupling Factor Complex
6.3.1 Structure
6.3.2 Regulation of Catalytic Activity
6.3.3 Catalytic Mechanisms
7 Concluding Remarks
References
5
Energy Transduction in Anoxygenic Photosynthesis
P.L.DUTTON (With 1 Figure)
1 Introduction
2 The Photosynthetic Bacterial Membrane
3 Membrane-Associated Energy-Transducing Enzymes
3.1 The Light-Harvesting System
3.2 The Reaction Center
3.3 The Oxido-Reductases
3.3.1 Direct NAD(P) Reduction
3.3.2 Direct Quinone Reduction
3.3.3 The be! Complexes
3.3.4 N A D Reduction Coupled to Aji *
3.3.5 Direct Versus Indirect N A D ( P ) Reduction
3.3.6 The Supply of Electrons from Oxidizable Substrates
3.4 The Reaction Center - Cytochrome c Complex
3.4.1 General Observations
3.4.2 The Rps. viridis Structure
3.4.3 Further Notes on Conformations, States, and Reaction Rates
3.5 Membrane Translocators
3.6 The ATP-Synthase
4 Concluding Remarks
References
+
+
182
184
184
185
186
188
189
197
201
202
203
203
206
206
207
208
2 1 0
H
+
6
Comparative Biochemistry of Light-Harvesting Systems
6.1
Primary Structure and Function of the Light-Harvesting Polypeptides
from Cyanobacteria, Red Algae, and Purple Photosynthetic Bacteria
H. ZUBER (With 4 Figures)
1 Introduction
2 The Polypeptides of the Extra-Membrane Light-Harvesting PigmentProtein Complexes (Phycobiliproteins) of Cyanobacteria and Red Algae
2.1 Structural Organization of the Phycobiliproteins
2.2 Primary Structures of the Phycobiliproteins: Structural and
Functional Implications
3 The Polypeptides of the Intra-Membrane Light-Harvesting PigmentProtein Complexes of Purple Photosynthetic Bacteria
3.1 Types and Molecular Organization of the Antenna Complexes . . .
3.2 Primary Structures and the Structural and Functional Role of the
Light-Harvesting Polypeptides
4 Concluding Remarks
References
6.2
211
212
220
221
224
227
228
229
230
232
238
241
241
242
245
245
246
250
251
Light-Harvesting Complexes in the Purple Photosynthetic Bacteria
R.J. COGDELL (With 4 Figures)
1 Introduction
252
2 The B-890 Class of Light-Harvesting Complexes (LH I Complexes)
. . 253
Contents
The B-800-850 Complex Class of Light-Harvesting Complexes (LH II
Complexes)
4 General Remarks on the Structure of Bacterial Light-Harvesting
Complexes
References
XIII
3
6.3
257
258
Phycobilisomes
E. GANTT (With 4 Figures)
1 Introduction
2 Stability of Phycobilisomes and Isolation
3 Structure and Composition
4 Reconstitution of Phycobilisomes
5 Association with Photosystem II
References
6.4
255
260
261
262
266
266
268
Light-Harvesting Pigment-Protein Complexes of Algae
J . M . ANDERSON and J. BARRETT (With 6 Figures)
1 Introduction
2 Light Environment
3 Distribution of Light-Harvesting Pigments
4 The Structure and Spectra of Light-Harvesting Pigments
5 Pigment-Protein Complexes
6 Core Chi a-Proteins of PS I and PS II
7 Light-Harvesting Complexes of the Chlorophyta
7.1 Siphonales
7.2 Prochlorophyta
8 Light-Harvesting Complexes of the Chromophyta
8.1 Phaeophyta
8.2 Diatoms
8.3 Chrysophyceae and Xanthophyceae
8.4 Cryptophyta
8.5 Peridinin-Chl a-Proteins
8.6 Molecular Topology of Algal Pigment-Protein Complexes
8.7 Structure of Algal Thylakoid Membranes
9 Spatial Organization of PS II and PS I in Algal Thylakoid Membranes
10 Strategies of Light-Harvesting in Algal Groups
11 Conclusions
References
7
Trapping Events in Light-Harvesting Assemblies
7.1
Theory and Modeling of Excitation Derealization and Trapping
269
269
269
270
272
273
274
275
276
276
277
279
279
280
280
281
281
282
282
284
284
R.S. KNOX
1
Introduction
1.1 Excitation Derealization and Trapping: Observations
1.2 Historical Development of Theory and Modeling
2 Derealization and Pairwise Transfer
2.1 States Produced by Light Absorption
2.2 Förster Theory of Pairwise Transfer
2.3 Application : Annihilation of Excitons
2.4 Beyond the Förster Theory : Coherence, Triplets, and the Monopole
Approximation
3 Excitation Flow to Traps
286
286
287
288
288
290
291
292
293
Contents
XIV
7.2
7.3
3.1 Principles : Adaptation of Pairwise Transfer Theory
3.2 Applications to Photosynthesis
4 Conclusions and Prospects
References
293
295
296
297
Excited State Kinetics of Chlorophyll Antenna Pigments
A.R. HOLZWARTH (With 2 Figures)
1 Introduction
2 Instrumentation
3 Room Temperature Fluorescence Kinetics
4 Measurements of Thylakoid Fragments
5 Low Temperature Fluorescence Kinetics
6 Origin of the Long-Lived (Nanosecond) Decay
7 Conclusions and Outlook
References
299
299
301
305
306
306
307
308
Topology and Dimensions of Antenna Pigment Systems Probed by
Exciton Annihilation
N.E. GEACINTOV and J. BRETON (With 1 Figure)
1 Introduction
2 Principles of Annihilation Techniques
3 Exciton Annihilation and Effects of Domain Size
3.1 Small Domains
3.2 Large Domains
4 Annihilation and Capture by Reaction Centers: Topological Effects
5 Mobile Excitons Versus Localized Excitons
6 Conclusions
References
7.4
7.5
310
310
311
311
312
. . 313
315
316
317
Molecular Orientation of the Pigments and the Problem of Energy
Trapping in Photosynthesis
J. BRETON (With 2 Figures)
1 Introduction
2 Orientation of the Absorption Dipoles in Vivo
3 Orientation of the Emission Dipoles in Vivo
4 Assignment and Molecular Origin of the Fluorescence Bands in Vivo
References
319
320
322
324
326
Excitation Transfer in Phycobiliproteins
H . SCHEER (With 2 Figures)
1 Introduction
2 Structure of Phycobiliproteins
3 Photophysics and Photochemistry of the Chromophores
4 The Energy Transfer Chain
5 Dynamics of Energy Transfer
6 Physiological Status
References
327
327
330
331
332
334
336
8
Physical Determinants of Charge Separation Processes
8.1
Primary Electron Transfer Reactions in Photosynthetic Bacteria:
Energetics and Kinetics of Transient States
W.W. PARSON and D. HOLTEN
References
342
Contents
8.2
XV
Redox Center and Secondary Protein Structure Organization in
Bacterial Reaction Centers and the Cytochrome b/c Complex
D . M . TIEDE (With 2 Figures)
1 Introduction
2 Redox Components: Definitions, Abbreviations
2.1 Redox Centers in the Reaction Center
2.2 Redox Centers in the b/cj Complex
3 Reaction Center Structure
3.1 Protein Secondary Structure
3.2 Redox Center Locations in the Membrane Profile
3.3 Redox Center Separations
3.4 Redox Center Orientations with Respect to the Membrane Normal
3.5 Angles Between Donor and Acceptor Molecular Planes
4 Structure of the Cytochrome b/cj Complex
4.1 Location of Redox Centers in the Membrane Profile
4.2 Redox Center Separation: cyt b —Q
4.3 Orientation of Redox Centers
References
t
h
8.3
344
344
344
346
346
346
346
347
348
349
350
350
350
351
351
Energy Trapping in Photosynthesis as Probed by the Magnetic
Properties of Reaction Centers
J.R. NORRIS and G . VAN BRAKEL (With 7 Figures)
1 Introduction
353
2 Mechanistic Aspects of the Photosynthetic Process
353
2.1 Key Features
353
2.2 Primary Photochemistry
353
2.3 Consequences of Blocking Secondary-Tertiary Chemistry
355
3 Components of the Reaction Center
356
3.1 Protein
356
3.2 Primary Donor
357
3.3 Acceptors
358
3.3.1 Bridging Intermediate and Primary Acceptor
358
3.3.2 Acceptor Complex Q — Fe — Q
358
4 Probing of Chemical Trapping by Magnetic Resonance Techniques
. . 359
4.1 Introduction
359
4.2 ENDOR
360
4.3 EPR of Single Crystals
361
4.4 Optically Detected Magnetic Resonance (ODMR)
362
4.4.1 Introduction
362
4.4.2 O D M R of the Photosynthetic Triplet State, P
363
4.4.3 Reaction Yield Detected Magnetic Resonance ( R Y D M R ) of
the Primary Radical Pair State, P
364
5 Summary
367
References
367
A
B
R
F
8.4
X-Ray Diffraction Studies on a Crystalline Bacterial Photosynthetic
Reaction Center: A Progress Report and Conclusions on the Structure
of Photosystem II Reaction Centers
H . MICHEL and J. DEISENHOFER (With 3 Figures)
1 Introduction
2 Results and Discussion
2.1 The Electron Density Map and Its Interpretation
2.1.1 General Description
371
373
373
373
Contents
XVI
2.1.2 The Pigments and Their Arrangement
2.1.3 The Protein Part
2.2 Functional Aspects
2.3 Evolutionary Aspects
2.4 Implications on the Structure of PS II Reaction Center
References
8.5
Primary Structure and Function of the Reaction Center Polypeptides
of Rhodopseudomonas capsulata - the Structural and Functional
Analogies with the Photosystem II Polypeptides of Plants
J.E. HEARST (With 2 Figures)
References
8.6
374
376
377
378
379
380
388
Membrane Topology and Photochemistry of the Green Photosynthetic
Bacterium Chloroflexus aurantiacus
R.E. BLANKENSHIP and R.C. FULLER (With 4 Figures)
1 Introduction
2 The Chlorosome
3 Cytoplasmic Membrane
4 Reaction Center and Electron Transport Pathway
5 Reaction Center Pigment and Protein Composition
References
8.7
390
391
393
394
396
398
Optically Detected Magnetic Resonance (ODMR) of Triplet States
in Vivo
A. J. HOFF (With 7 Figures)
1 Introduction
2 Electron Spin Resonance of the Triplet State in Zero Magnetic Field . .
3 O D M R Techniques
4 Zero Field Splitting Parameters and Decay Rates
5 Relative Orientation of Optical Transition Moments and Spin Axes . .
6 Microwave-Induced Fluorescence (MIF) Spectra
7 Triplet-Minus-Singlet Absorbance Difference Spectra of Bacterial
Reaction Centers
8 Linear Dichroic Triplet-Minus-Singlet Absorbance Difference Spectra of
Bacterial Reaction Centers
9 Triplet-Minus-Singlet Spectra of the Green Plant Photosystems . . . .
10 Conclusions and Prospects
References
9
Photosystems I and II: Structure, Proteins, and Cofactors
9.1
The Reaction Center of Photosystem II
B. A . DINER (With 1 Figure)
1 Introduction
2 Primary Reactants
2.1 Transmembrane Charge Separation
2.2 P-680 (also called Chi a„)
2.3 Pheophytin (Ph, also called I)
2.4 Q (also called Q, X-320, Q , Q i , A , )
2.5 Fluorescence
2.6 Redox Potentials
A
H
400
400
402
403
404
407
408
413
418
418
419
422
422
422
423
424
424
425
426
Contents
XVII
3
Secondary Reactions, Donor Side
3.1 Reduction Kinetics of P-680 +
3.2 Signal II
3.3 Identity of Z (also called D Y )
3.4 Other Donors
3.4.1 Carotenoid
3.4.2 Cytochrome b-559
4 Alternate Acceptors
4.1 Low Potential Acceptor, Q
4.2 Q
(also called A , R and Q )
4.3 a- and ^-Centers
4.4 Still More Heterogeneity
5 Polypeptides
References
427
427
428
428
430
430
430
431
431
432
433
433
433
434
1 ?
L
4 0 0
9.2
H
2
Electron Transfer on the Oxidizing Side of Photosystem II:
Components and Mechanism
CF.
YOCUM
1 Enzymatic Oxidation of H 0 by PS II
2 Components of the Oxygen-Evolving Complex
3 Factors Influencing the Sequential Oxidation of H 0
4 Summary and Conclusions
References
437
438
442
443
445
2
2
9.3
Proteins Participating in Photosynthetic Water Oxidation
B. ANDERSSON (With 1 Figure)
1
2
Introduction
Extrinsic Proteins of Water Oxidation
2.1 The 33, 23, and 16 kDa Proteins. Identification and Connection with
Water Oxidation
2.2 Properties, Biogenesis and Organization in the Thylakoids . . . .
2.3 Specific Functions in Water Oxidation
2.4 A I O kDa Polypeptide
3 Intrinsic Proteins of Water Oxidation
4 Hypothetical Architecture of the Water Oxidation Complex
References
9.4
447
447
447
450
452
453
453
454
455
Photosystem II Reaction Center: Polypeptide Subunits and Functional
Cofactors
C. J. ARNTZEN and H.B. PAKRASI (With 1 Figure)
1
2
Introduction
Polypeptides of the PS II Core Complex
2.1 51 kDa Polypeptide
2.2 45 kDa Polypeptide
2.3 Q (32 kDa) Protein
2.3.1 Quinone-Herbicide Interactions at the Q Site
2.3.2 Photoaffinity Tags of the Q Site
2.3.3 Mutations Affecting Quinone and Herbicide Binding at the Q
Site
2.4 The 34 kDa D2 Protein
2.5 10 kDa Protein
3 Photosystem II : A Membrane-Protein Complex
References
457
457
459
459
460
461
461
B
B
B
B
462
462
463
464
466
Contents
XVIII
9.5
The Mechanism of Photoinhibition in Higher Plants and Green Algae
D.J. KYLE and I. OHAD (With 1 Figure)
1 Introduction
2 Phenomenology of Photoinhibition
2.1 Higher Plants
2.2 Algal Cells
2.3 Photoinhibition in Chloroplasts
3 Mechanism of Photoinhibition
4 Recovery from Photoinhibition Damage
5 Synergism Between Light and Other Stresses
6 Conclusion
References
9.6
468
468
468
469
470
470
471
472
474
474
Photosystem I Reaction Center and Its Primary Electron Transfer
Reactions
P. SÉTIF and P. MATHIS (With 2 Figures)
1 Introduction
2 The Primary Donor P-700
2.1 Basic Properties of P-700
2.2 Chemical Nature of P-700
2.2.1 Two Chlorophyll Molecules
2.2.2 One Chlorophyll Molecule
3 Photosystem I Electron Acceptors
3.1 Terminal Acceptors: F and F
3.2 F and A
3.3 More Primary Electron Acceptors: A , A ,
4 Structural Aspects
4.1 Electron Carriers and Polypeptides
4.2 Geometrical Aspects
4.3 Functional Accessibility
5 Conclusion
References
A
x
476
477
477
477
479
479
480
481
482
482
483
483
484
484
484
485
B
2
0
9.7
Photosystem I Proteins
F. -A. WOLLMAN
1
2
3
4
5
Introduction
The R C I Protein Complex
The L H C I Protein Complex
Architecture of the PS I Protein Complexes
Site of Synthesis and Assembly of Subunits of the PS I Protein
Complexes
References
10
487
488
489
492
492
494
Energy Transfer and Energy-Coupling Processes
10.1 Composition and Structure of Cytochrome be, and b f Complexes
G. HAUSKA (With 2 Figures)
6
1 Introduction
2 Composition
2.1 Redox Components
2.1.1 Cytochrome b
2.1.2 Cytochrome C! or f
2.1.3 The Rieske FeS Center
2.1.4 Quinone
2.2 Polypeptides
496
497
497
497
498
498
499
500
Contents
XIX
3
502
503
504
506
Structure
3.1 Genes and Primary Structures
3.2 A Topographical Model
References
10.2
10.3
Mobile Electron Carries in Thylakoids
J. WHITMARSH (With 2 Figures)
1 Introduction
2 Diffusion in Two Dimensions - Definitions
3 Topology and Composition of the Thylakoid Membrane
4 Lateral Diffusion Between Appressed and Stroma-Exposed Membrane
Regions
5 Lateral Diffusion Within a Localized Region
6 Concluding Remarks
References
508
509
513
519
521
524
525
Cytochrome b /f Complex - Quinol Interactions
6
P. JOLIOT and A . JOLIOT
1 Introduction
2 Slow Electrogenic Phase
3 Proton Translocation Associated with the Intersystem Electron Transfer
4 Reverse Electron Flow
5 Cytochrome b / f Complex
6 Redox Potentials of the Carriers Involved in the Cytochrome b / f
Complex and in the Slow Electrogenic Phase
7 Models
References
6
528
528
529
530
530
6
10.4
533
534
538
Light-Driven Electron and Proton Transfer in the Cytochrome bei
Complex
R.C. PRINCE (With 2 Figures)
1 Introduction
539
2 Components of the Cytochrome bc Complex
539
2.1 Cytochrome C!
539
2.2 Cytochromes b
540
2.3 The Rieske Iron-Sulfur Protein
540
2.4 Quinones
540
3 Stoichiometrics and Interactions in the bc Complex
541
4 Pathways of Electron Flow Within the bc Complex
542
5 Electrogenic Events in the be. Complex
544
6 Electron Flow in the bc Complex of Other Photosynthetic Bacteria
545
7 Light-Induced Electron Flow in the Mitochondrial bc Complex . . . 545
References
546
x
t
{
{
L
10.5
Plastocyanin
W. HAEHNEL (With 1 Figure)
1 Introduction
2 Synthesis
3 Structure
3.1 Refined Crystal Structure
3.2 Chemical Modification
4 Reduction of P-700
4.1 Surface Charges
547
547
548
548
550
552
552
XX
Contents
4.2 Kinetics
4.3 Subunit III of PS I
5 Oxidation of Cytochrome f
6 Reactions in Situ
6.1 Organization of Electron Transport
6.2 Diffusion Coefficient
6.3 Kinetics in Situ
References
10.6
552
553
554
555
555
556
556
557
Local and Delocalized Interactions in Energy Coupling
B.A. MELANDRI and G . VENTUROLI
1 Introduction
2 Steady-State Coupling in Chloroplasts
3 Steady-State Coupling in Bacterial Chromatophores
4 Transient Coupling Phenomena in Chloroplasts
5 Transient Coupling Phenomena in Chromatophores
6 ATP Synthesis Driven by Artificial Ion Gradients
7 Interpretation of the Phenomena of Localized Coupling
References
10.7
560
560
562
563
564
565
566
568
Proton-Membrane Interactions in Chloroplast Thylakoids
R.A. DlLLEY
1 Introduction
2 Proton Uptake and Endogenous Buffering
3 Chemical Probes for Detecting Membrane Proton-Binding Groups
4 Sequestered Proton-Buffering Domains
5 Sequestered Proton Pools and Energy Coupling
References
10.8
570
570
. . 571
572
574
575
Structure, Mechanism, and Regulation of the Chloroplast
H -ATPase ( C F , - C F )
+
0
R.E. MCCARTY and C M . NALIN (With 1 Figure)
1 Introduction
2
576
Structure of C F I - C F Q
577
2.1 Subunit Stoichiometry
577
2.2 Organization of C F ^ C F Q
2.3 Roles of the Subunits
3 Mechanism and Regulation
3.1 Substrates
3.2 H / A T P Stoichiometry
3.3 Regulation of Activity
3.4 Cooperativity During Catalysis
4 Genetic Analysis of C F , - C F
5 Future Directions
References
+
0
10.9
577
578
579
579
579
579
580
581
581
582
Evaluation of Results on Nucleotide-Binding Sites of the ATPase
Complex
H. STROTMANN (With 1 Figure)
1
2
3
4
Introduction
Definitions
The Number of Nucleotide-Binding Sites
Localization of Nucleotide-Binding Sites
584
584
585
587
Contents
XXI
5 Catalytic Mechanism
6 Roles of Tightly Bound Nucleotides
7 Conclusion
References
587
589
592
592
10.10 Sites of Herbicide Inhibition at the Photosynthetic Apparatus
G. SANDMANN and P. BÖGER (With 2 Figures)
1 Introduction
595
2 Bioenergetic Reactions
596
2.1 Inhibition of Electron Transport Between the Two Photosystems 596
2.2 Inhibition of ATP Formation
597
3 Pigment Formation
597
3.1 Carotenoid Biosynthesis
597
3.2 Chlorophyll Biosynthesis
598
4 Peroxidation of Chloroplast Components
599
5 Conclusions
601
6 List of Herbicides Mentioned in the Text
601
References
602
11
Topography, Composition, and Assembly of Photosynthetic
Membranes
11.1 Membrane Architecture of Anoxygenie Photosynthetic Bacteria
S.G. SPRAGUE and A . R . VARGA (With 11 Figures)
1 Introduction
2 Green Bacteria
2.1 Morphology
2.2 Adaptation of the Photosynthetic Apparatus to Different
Environmental Conditions
3
Heliobacterium chlorum
4
Purple Bacteria
4.1 Morphology
4.2 Development of I C M Structure
4.3 Additional Factors Influencing Membrane Structure
5 Summary
References
603
605
605
609
610
610
611
613
616
617
618
11.2 Topology of the Chromatophore Membranes of Purple Bacteria
R. BACHOFEN and V . WIEMKEN (With 1 Figure)
1 Introduction
2 Topology of Pigment-Protein Complexes
3 Topology of Electron Carriers
3.1 Topology of the ATP Synthase, some Dehydrogenases and the
Hydrogenase
4 Topology of Membrane Lipids
5 Conclusions
References
11.3
620
621
626
627
627
628
629
Synthesis and Assembly of Bacterial Photosynthetic Membranes
T.J. DONOHUE and S. KAPLAN
1 Introduction
2 Assembly of the I C M in Steady-State Cells
632
633
XXII
Contents
3 Induction of ICM Synthesis
4 Inhibition of ICM Synthesis
5 Repression/Derepression of ICM Synthesis
6 Future Prospects
References
11.4
Proteins of Cyanobacterial Thylakoids
T.M.
BRICKER, J.A. GUIKEMA, H . B . PAKRASI, and L . A . SHERMAN
1 Introduction
2 Protein Composition of Cyanobacterial Thylakoids
3 Chlorophyll-Protein Complexes
4 Photosystem II
5 Cytochrome b / f Complex
6 Photosystem I
7 F and F F
8 Discussion
References
6
x
11.5
r
0
Introduction
Surface Charge Densities
2.1 Particle Electrophoresis
2.2 Differential Doppler Micro Electrophoresis
2.3 Fluorescence Probe Techniques
2.4 Indirect Methods
2.5 Summary of Surface Charge Properties
3 Control of Photosynthetic Processes by Surface Charge
4 A n Explanation of the Phosphorylation-Induced-Control of Energy
Transfer in Terms of Electrostatics
5 Conclusion
References
653
654
654
655
655
656
656
657
660
662
663
Freeze-Fracture Studies of Mutant Barley Chloroplast Membranes
D.J. SIMPSON (With 10 Figures)
1 Introduction
2 Location of Chlorophyll a/b Proteins
3 Location of the Photosystem I Reaction Center
4 Location of the Photosystem II Reaction Center
5 Reconstitution Studies
6 Effects of Single Gene Mutations on Functional Complexes
7 Concluding Remarks
References
11.7
640
641
641
644
649
649
650
651
651
Surface Electrical Charges and Protein Phosphorylation
J. BARBER (With 1 Figure)
1
2
11.6
634
636
637
638
639
Reconstitution of Thylakoid Components into Artificial Membranes
I.J. RYRIE (With 1 Figure)
1 Introduction
2 Membrane Reconstitution - Overview, Techniques and Some
Drawbacks
3 Reconstitutions with Thylakoid Proteins
3.1 Dicyclohexylcarbodiimide-Sensitive C F ^ F Q ATP Synthetase
Complex
665
666
669
671
672
672
673
674
675
675
676
676
Contents
XXIII
3.2 The Light-Harvesting Complex of Photosystem II, L H C II
3.3 Photosystem I
3.4 Cytochrome b /f
3.5 Binary Protein Systems
4 Conclusions
References
. . .
6
11.8
11.9
Prolamellar Bodies
C. LÜTZ (With 5 Figures)
1 Introduction
2 Formation of Prolamellar Bodies
3 Composition of Prolamellar Bodies
4 The Role of Lipids in Prolamellar Body Formation
5 Prolamellar Bodies and Membrane Formation — A n Outlook
References
. . . .
677
679
679
680
681
681
683
684
686
688
689
690
Acyl Lipids in Thylakoid Membranes: Distribution and Involvement
in Photosynthetic Functions
P.A. SlEGENTHALER and A . R A WYLER
1 Introduction
693
2 Aging of Thylakoids in Vitro
693
3 Extraction of Membrane Lipids by Organic Solvents
694
4 Modulation of Fatty Acid Composition .
694
5 Lipid Composition of Thylakoids and Subchloroplast Fractions
. . . 695
6 Modification of the Lipid : Protein Ratio in Thylakoid Membranes . . 697
7 Immunological Studies
699
8 Lipolytic Treatments
699
9 Biogenesis Studies
702
10 Conclusions
702
References
703
11.10 Biosynthesis of Chloroplast Membrane Lipids
K . KEEGSTRA
1 Introduction
2 Structure of Chloroplast Membrane Lipids
3 Biosynthesis of Galactolipids
3.1 Synthesis of Prokaryotic Galactolipids
3.2 Synthesis of Eukaryotic Galactolipids
4 Biosynthesis of Other Chloroplast Lipids
5 Summary
References
11.11 Structural Properties and Molecular Organization of the Acyl Lipids
of Photosynthetic Membranes
D.J. MURPHY (With 5 Figures)
1 Introduction
2 Composition
3 Structures
3.1 Chemical Structures
3.2 Physical Structures
3.2.1 Diacylgalactosylglycerol
3.2.2 Diacyldigalactosylglycerol
3.2.3 Diacylsulfoquinovosylglycerol
706
706
707
709
710
711
712
712
713
713
714
714
716
716
718
718
Contents
XXIV
3.2.4 Phospholipids
3.2.5 Thylakoid Lipid Mixtures
3.3 Physiological Significance of Lipid Structures
4 Asymmetric Distribution
4.1 Transverse Asymmetry
4.1.1 Antibody Studies
4.1.2 Lipolytic Studies
4.2 Lateral Heterogeneity
4.3 Extent and Functions of Lateral and Transverse Asymmetries
5 Lipid-Protein Interactions
5.1 Galactolipids
5.2 Phospholipids
References
718
718
719
719
719
720
720
720
. . 721
722
722
722
725
Author Index
727
Subject Index
791
List of Contributors
JAN M . ANDERSON
CSIRO
Division of Plant Industry
P.O. Box 1600
Canberra City
A C T 2601/Australia
B. ANDERSSON
Department of Biochemistry
University of Lund
P.O. Box 124
S-22100 Lund/Sweden
C. J. ARNTZEN
E.I. du Pont de Nemours & Co.
Central Research and Development
Department
Experimental Station
Bldg. 402, Room 3226
Wilmington, D E 19898/USA
P. BÖGER
Lehrstuhl für Physiology
und Biochemie der Pflanzen
Universität Konstanz
Postfach 5560
D-7750 Konstanz/FRG
J. BRETON
Service de Biophysique
Département de Biologie
C.E.N. de Saclay
F-91191 Gif-sur-Yvette Cedex/France
T . M . BRICKER
Department of Chemistry
The University of Southern Mississippi
Hattiesburg, M S 39406-5043/USA
R.J. COGDELL
Department of Botany
University of Glasgow
Glasgow G12 8QQ/United Kingdom
R. BACHOFEN
Institut für Pflanzenbiologie
der Universität
Zollikerstraße 107
CH-8008 Zürich/Switzerland
J. DEISENHOFER
Max-Planck-Institut für Biochemie
Abt. Strukturforschung II
Am Klopferspitz
D-8033 Martinsried/FRG
J. BARBER
Department of Pure and
Applied Biology
Imperial College
Prince Consort Road
London SW7 2BB/United Kingdom
R A . DILLEY
Department of Biological Sciences
Purdue University
West Lafayette, IN 47907/USA
B A . DINER
J. BARRETT
Rockefeller University
1230 York Avenue
New York, N Y 10021/USA
Institut de Biologie
Physico-Chimique
13, rue Pierre et Marie Curie
F-75005 Paris, France
T.J. DONOHUE
R.E. BLANKENSHIP
Department of Chemistry
Arizona State University
Tempe, A Z 85287/USA
Department of Bacteriology
University of Wisconsin
1550 Linden Drive
Madison, WI 53706/USA
XXVI
P.L. DUTTON
607 Goddard Laboratories
Department of Biochemistry
and Biophysics
37th & Hamilton Walk
Philadelphia, PA 19104/USA
R.C. FULLER
Department of Biochemistry
University of Massachusetts
Amherst, M A 01003/USA
List of Contributors
A.R. HOLZWARTH
Max-Planck-Institut
für Strahlenchemie
Stiftstraße 34-36
D-4330 Mühlheim/Ruhr/FRG
A . JOLIOT
Institut de Biologie
Physico-Chimique
13, rue Pierre et Marie Curie
F-75005 Paris/France
E. GANTT
Smithsonian Environmental
Research Center
12441 Parklawn Drive
Rockville, M D 20852/USA
N . E . GEACINTOV
Chemistry Department
New York University
New York, N Y 10003/USA
J.A. GUIKEMA
Division of Biology
Kansas State University
Ackert Hall
Manhattan, KS 66506/USA
P. JOLIOT
Institut de Biologie
Physico-Chimique
13, rue Pierre et Marie Curie
F-75005 Paris/France
S. KAPLAN
Department of Microbiology
University of Illinois
at Urbana-Champaign
407 South Goodwin Avenue
Urbana, IL 61801/USA
K . KEEGSTRA
W. HAEHNEL
Westf. Wilhelms-Universität
Münster
Lehrstuhl für Biochemie
der Pflanzen
Hindenburgplatz 55
D-4400 Münster/FRG
G . HAUSKA
Institut für Botanik
Universität Regensburg
Universitätsstr. 31
D-8400 Regensburg/FRG
J.E. HEARST
Department of Chemistry
430 Latimer Hall
University of California
Berkeley, C A 94720/USA
A.J. HOFF
Department of Biophysics
Huygens Laboratory
of the State University
NL-2300 R A Leiden/The Netherlands
D. HOLTEN
Department of Chemistry
Box 1134
Washington University
St. Louis, M O 63130/USA
Department of Botany
University of Wisconsin
Madison, WI 53706/USA
R.S. KNOX
Department of Physics
and Astronomy
University of Rochester
Rochester, N Y 14627/USA
D J . KYLE
Martek Corporation
9115 Guilford Rd.
Columbia, M D 21046/USA
C. LÜTZ
Botanisches Institut
der Universität Köln
1. Lehrstuhl
Gyrhofstraße 15
D-5000 Köln 41
P. MATHIS
Service de Biophysique
Département de Biologie
C.E.N. de Saclay
F-91191 Gif-sur-Yvette Cedex/
France
XXVII
List of Contributors
R.E. MCCARTY
Section of Biochemistry
Molecular and Cell Biology
Cornell University
Ithaca, N Y 14853/USA
W.W.
PARSON
Department of Biochemistry SJ-70
University of Washington
Seattle, W A 98195/USA
R.C. PRINCE
B.A. MELANDRI
University of Bologna
Institute of Botany
Via Irnerio 42
1-40126 Bologna/Italy
H . MICHEL
Max-Planck-Institut
für Biochemie
Abteilung Membranbiochemie
Am Klopferspitz
D-8033 Martinsried/FRG
D J . MURPHY
Department of Botany
University of Durham
Durham, DH1 3LE/United Kingdom
C M . NALIN
Department of Cell Biology
Roche Institute of
Molecular Biology
Roche Research Center
Nutley, N J 07110/USA
J.R.
NORRIS
Chemistry Division
Argonne National Laboratory
Argonne, IL 60439/USA
I. OHAD
Department of
Biological Chemistry
Institute of Life Sciences
The Hebrew University
of Jerusalem
91904 Jerusalem, Israel
D.R. ORT
Department of Plant Biology
289 Morrill Hall
University of Illinois
505 S. Goodwin Ave.
Urbana, IL 61801/USA
Exxon Research
and Engineering Co.
Annandale, N J 08801/USA
A . RA WYLER
Laboratoire de
Physiologie végétale
Université de Neuchâtel
Ch. de Chantemerle 20
CH-2000 Neuchâtel/Switzerland
I J . RYRIE
Department of Applied
Mathematics
Research School of
Physical Sciences
Australian National University
Canberra 2601/Australia
G . SANDMANN
Lehrstuhl für Physiologie
und Biochemie der Pflanzen
Universität Konstanz
Postfach 5560
D-7750 Konstanz/FRG
K . SAUER
Chemistry Department
University of California
Berkeley, C A 94720/USA
H . SCHEER
Botanisches Institut
der Universität
Menzinger Straße 38
D-8000 München 19/FRG
P. SÉTIF
Service de Biophysique
Département de Biologie
C.E.N. de Saclay
F-91191 Gif-sur-Yvette Cedex/
France
H.B. PAKRASI
Central Research and
Development Department
E.I. du Pont de
Nemours & Co.
Wilmington, D E 19898/USA
L . A . SHERMAN
Division of
Biological Sciences
University of Missouri-Columbia
Columbia, M O 65211/USA
List of Contributors
XXVIII
P.A. SlEGENTHALER
Laboratoire de Physiologie
végétale
Université de Neuchâtel
Ch. de Chantemerle 20
CH-2000 Neuchâtel/Switzerland
D.J. SIMPSON
Department of Physiology
Carlsberg Laboratory
G l . Carlsbergvej 10
DK-2500 Copenhagen Valby/
Denmark
S.G.
SPRAGUE
West Virginia University
School of Medicine
Department of Biochemistry
Morgantown, WV 26506/USA
L . A . STAEHELIN
Department of Molecular
Cellular and Developmental
Biology
University of Colorado
Campus Box 347
Boulder, CO 80309/USA
G . VAN BRAKEL
Biokemi
Odense Universitet
Campusvej 55
DK-5230 Odense M/Denmark
A.R. VARGA
University of Illinois
at Urbana-Champaign
Department of Microbiology
Urbana, IL 61801/USA
G . VENTUROLI
University of Bologna
Institute of Botany
Via Irnerio 42
1-40126 Bologna/Italy
J. WHITMARSH
Department of Plant Biology
289 Morrill Hall
University of Illinois
505 S. Goodwin Ave.
Urbana, IL 61801/USA
V. WlEMKEN
Department of Botany
University
Hebelstraße 1
CH-4056 Basel/Switzerland
H . STROTMANN
Botanisches Institut
der Universität Düsseldorf
Universitätsstraße 1
D-4000 Düsseldorf/FRG
J.P. THORNBER
Department of Biology
University of California
405 Hilgard Ave.
Los Angeles, C A 90024
USA
F.-A. WOLLMAN
Service de Photosynthese
Institut de Biologie
Physico-Chimique
13, rue Pierre et Marie Curie
F-75005 Paris/France
CF.
YOCUM
Division of Biological Sciences
The University of Michigan
Ann Arbor, MI 48109-1048/USA
H . ZUBER
D . M . TlEDE
Chemistry Division
Argonne National Laboratory
Argonne, IL 60439/USA
Institut für Molekularbiologie
und Biophysik
ETH-Hönggerberg - H P M
CH-8093 Zürich/Switzerland
7.5 Excitation Transfer in Phycobiliproteins
H . SCHEER
1 Introduction
One of the major strategies in the competition of photosynthetic organisms
for light is qualitative and quantitative adaptation in their light-harvesting apparatus (THORNBER, Chap. 3 ; STAEHELIN, Chap. 1 ; ANDERSON, Chap. 6.4, all this
Vol.). This includes, in particular, the usage of pigments which harvest light
efficiently in the spectral regions not covered by the chlorophylls a and b present
in higher plants, e.g., the bacteriochlorophylls absorbing well beyond 700 nm
(COGDELL, Chap. 6.2, this Vol.), and the phycobiliproteins and carotenoids
absorbing in the "chlorophyll trough" between 470 and 630 nm (GANTT, Chap.
6.3, this Vol.). Among these, the phycobiliproteins are to date probably the
best understood. They are not only the major light-harvesting pigments of cyanobacteria, red algae, and cryptophytes (see STAEHELIN, Chap. 1, this Vol., for
a general characterization of these species), microorganisms which are responsible for a large fraction of the net photosynthetic production on earth, but
they are also readily accessible and pleasing to the eye. Different aspects of
phycobiliprotein research (GANTT 1979, 1981; G L A Z E R 1980, 1983; M A C C O L L
1982; RÜDIGER 1979; SCHEER 1981, 1982; WEHRMEYER 1983; ZUBER 1978) and
related topics (BRASLAVSKY et al. 1983; PRATT 1978, 1982; RÜDIGER 1980; R Ü -
DIGER and SCHEER 1983) have been reviewed in the past 5 years. In this volume,
G A N T T (Chap. 6.3) describes the structure and function of phycobilisomes and
Zu BER (Chap. 6.1) the primary structure of phycobiliproteins. This chapter provides a brief overview of the energy transfer in biliproteins. Due to space limitations, only few citations could be incorporated. They are a biased selection
from a large body of work, and should be used as a source for further references.
2 Structure of Phycobiliproteins
Most phycobiliproteins contain one or both of the chromophores, phycocyanobilin (Fig. 1 a) or phycoerythrobilin (Fig. 1 b), but additional chromophores of
yet unknown structure are present, for example, in red algae, phycoerythrins
("phycourobilin"), in phycoerythrocyanins, and in particular in biliproteins
from cryptophytes. Both chromophores are linked to their apoproteins via one,
and in some cases two (RAPOPORT and G L A Z E R 1984) stable thioether bond(s)
328
H . SCHEER:
R
Fig. 1. Chromophores of phycobiliproteins. Molecular structures of a phycocyanobilin,
the chromophore of PC and APC, b phycoerythrobilin, the main chromophore of phycoerythrins. A hypothetical conformation of the native phycocyanobilin in PC is shown
in c (see SCHIRMER et al., 1985, for three dimensional structures of PC chromophores)
at rings A or D to cystein residues, as has been inferred from several independent
lines of evidence (RÜDIGER 1979; LAGARIAS et al. 1979; ZUBER 1978; KÖST-REYES
and KÖST 1979; FREIDENREICH et al. 1978), including a recent X-ray structure
(SCHIRMER et al. 1985). Additional, more labile bonds have been postulated
to exist based on conflicting results (see SCHEER 1982). Studies with a new,
mild chromophore cleavage method have recently shown the absence of a second
bond in two phycocyanins (KUFER et al. 1983).
The properties of the native biliprotein chromophores are profoundly influenced by noncovalent interactions with the protein (see SCHEER 1982). Both
the intense visible absorption and fluorescence of the phycobiliproteins, which
are crucial for their functions, are caused by these interactions, and are absent
in the denatured pigments and in free chromophores (see below). The phycobiliproteins thus present a good example of "molecular ecology", e.g., the optimization of cofactors to specific functional needs by interactions with the apoproteins
(SCHEER 1982).
All biliproteins are composed of two to three chromophore-bearing subunits.
To date, the primary structures are known for more than ten different subunits,
329
7.5 Excitation Transfer in Phycobiliproteins
including the a- and /J-subunits of all biliproteins from the cyanobacterium,
Mastigocladus laminosus e.g. allophycocyanin (APC), phyocyanin (PC) and
phycoerythrocyanin (PEC) (FÜGLISTALLER et al. 1983), and the red (?) alga,
Cyanidium caldarium (APC and PC) (OFFNER and TROXLER 1983; see also
ZUBER, Chap. 6.1, this Vol.). In the pigments from cyanobacteria and red alga,
the a-subunit (%17kDa) bearing 1-2 chromophores and a slightly larger ßsubunit carrying 1-4 chromophores, are always present in a 1:1 molar ratio.
Additional chromophore-carrying y subunits of generally much larger size are
known in some APC's and in red algal PE's (phycoerythrin) in (<xß) y stoichiometry (n = 3 or 6) (see G L A Z E R 1983 and SCHEER 1982). The fundamental structural
n
units, e.g., cca'ß (GANTT 1979; MÖRSCHEL and WEHRMEYER 1975) of the crypto-
phyte biliproteins have a different composition.
The chromophore composition is most simple in the cyanobacterial biliproteins, which carry only one type of chromophore on any given subunit. Subunits
bearing two different chromophores are common in the more highly evolved
eukaryotic red algae and cryptophytes. The chromophore-binding sequences
are known for many phycobiliproteins (see above). Together with immunochemical studies and the complete peptide sequences cited above, an evolutionary
family tree has been constructed which relates all phycobiliprotein polypeptides
to a common ancestral gene (see ZUBER Chapter 6.1, G L A Z E R 1980; WEHRMEYER
1983).
Isolated biliproteins of cyanobacteria and red algae have a strong tendency
to aggregation. Trimers ( = heterohexamers) (otß) or hexamers ( = heterodode3
camers) (a/?) are generally observed (see M A C O L L and BERNS 1981; SCHEER
6
1982). The former seem to be the largest aggregates in the absence of linkers.
In vivo, they are organized within complex structures, the phycobilisomes
(PB'somes) (GANTT and CONTI 1966). A single PB'some can bear up to 2700
chromophores of different types (GANTT Chap. 6.3, this Vol.) and represents
the functional antenna unit of these organisms. In addition to the chromophorebearing biliproteins, PB'somes contain several, generally colorless, "linker" peptides, which play a crucial role in their organization and their attachment to
the membrane (see G L A Z E R 1983). Much of the basic PB'some structure with
an A P C core and outer rods containing PC and PE (see Fig. 2 in G A N T T ,
Chap. 6.3, this Vol. for a diagram of the different types of PB'somes) has
been obtained by combining high-resolution electron microscopy with biochemical methods (MÖRSCHEL et al. 1980;
G L A Z E R et al. 1979;
SIEGELMAN and K Y C I A
1982; WANNER and KÖST 1980). PB'somes are located on the outer surface
of the thylakoid membrane in a dense packing, but apparently without cooperation between different PB'somes.
Very little is known about the quaternary structure of the cryptophyte biliproteins. Cryptophytes do not have PB'somes; instead their biliproteins are
located on the inner surface of the thylakoids and reveal virtually no substructure in the electron microscope (see Figs. 3 and 19 in STAEHELIN Chap. 1, this
Vol.). This is paralleled by a decreased tendency of the isolated pigments to
aggregate (see G A N T T 1979; M A C C O L L and GUARD-FRIAR
1983). Preliminary
X-ray results have recently been published (MORISSET et al. 1984).
330
H . SCHEER:
3 Photophysics and Photochemistry of the Chromophores
Denatured biliproteins, in which the chromophores are uncoupled from the
protein, as well as free bile pigments of similar structures, have flexible chromophores which are predominantly present in solution in a cyclic-helical conformation (SCHEER 1982; BRASLAVSKY et al. 1983). These conformers have absorptions
of moderate intensity in the visible range (eœ 17,000 M
c m at neutral pH)
-
1
- 1
3
(see BRANDLMEIER et al. 1981 ), low fluorescence yields (0 < 10 " see BRASLAVSKY
et al. 1983) with corresponding fast excitation decays (SCHNEIDER, unpublished)
and low phosphorescence intensities (LAND 1979). The deexcitation is governed
by internal conversion, which is promoted by one or more of the following
mechanisms: proton transfer ( F A L K and NEUFINGERL 1979;
FRIEDRICH et al.
1981), vibrations, or rotations around single bonds (KUFER et al. 1983), and
by photoreactions, e.g., to the labile 10 E isomers (BRASLAVSKY et al. 1983).
This deactivation is only hindered if the above mechanisms are blocked, e.g.,
by a rigid fixation (KUFER et al. 1983), distortion of the chromophores (FALK
and THIRRING 1980), or (photo)selection of more rigid and extended conformers
(BRASLAVSKY et al. 1983). In these cases, the lifetimes of the excited states are
increased to allow high yields of fluorescence, or photochemical reactions to
products like the 4 E - or 15 E isomers which are stable at ambient temperatures.
In the biliproteins, such conformers are predominant. The chromophores
are probably rigidly fixed in an extended and twisted conformation near the
surface of the protein (SCHEER 1982). This rather general picture has been detailed recently by the current X-ray analysis of a PC (SCHIRMER et al. 1985).
The energetically unfavorable conformations must be stabilized by noncovalent
interactions with the polypeptide chains (SCHEER 1982). The absorption in the
visible range is thus increased by a factor of ^5, and fluorescence by several
orders of magnitude to & >0.5 (see GRABOWSKI and G A N T T 1978 a). The phycobiliproteins are photochemically stable at ambient temperatures. It is, however,
of interest to note that the photoreactive, light-sensing plant pigment phytochrome has a chromophore structure and protein interaction that resembles
PC, and that partial denaturation renders phycobiliproteins to a certain extent
photoreactive by partial uncoupling from the protein (BJÖRN 1979; BRASLAVSKY
et al. 1983).
In spite of the large number of chromophores present in phycobiliproteins,
there are generally only moderate interchromophore interactions. Strong coupling between chromophores has been established for the pigments in cryptophytes (HOLZWARTH et al. 1983;
J U N G et al. 1980;
KOBAYASHI et al. 1979), and
may also be present in some of the cyanobacterial and red algal ones, but
many of the isolated phycobiliproteins do not show good evidence of such
coupling as judged from their C D spectra. However, aggregation is often paralleled by the rise of S-shaped C D signals which are indicative of strong coupling.
Since the chromophores are probably located at or near the surface of the
native biliproteins, this would mean that the nearest neighbors in situ may
not be the chromophores on the same subunits or heterodimers, but rather
on different ones [see STAEHELIN, Chap. 1, this Vol. for a discussion of phycobilisome packing in vivo and the recent x-ray results of SCHIRMER et al. (1985)].
7.5 Excitation Transfer in Phycobiliproteins
331
4 The Energy Transfer Chain
The participation of phycobiliproteins in photosynthesis and, in particular, their
association with photosystem II was originally recognized by action spectroscopy (EMERSON 1958). Energy transfer from biliproteins to chlorophylls has
also been demonstrated in solution (FRACKOWIAK et al. 1979; KRASNOVSKII and
EROKHINA 1969). The discovery of PB'somes ( G A N T T and CONTI 1966) marks
the beginning of an understanding of phycobiliprotein function in cyanobacteria
and red alga on a molecular basis. PB'somes collect light efficiently in the
wavelength range between 480 and 630 nm, but their fluorescence is emitted
almost exclusively (>95%) by a small fraction of a minor constituent, e.g.,
A P C (A , absorption « 6 6 5 nm, 2 , emission « 6 8 0 nm). If attached to the
photosynthetic membrane, the energy is transferred further to the chlorophyllcontaining reaction centers in the membrane, preferentially to PS II (GANTT
1981).
In the original PB'some model derived from electron microscopic and biochemical studies of the red alga, Porphyridium cruentum, a phycobilisome somewhat resembles an onion cut in half: a core, made up of A P C , is surrounded
by layers of PC and, further out, PE. Although this model has been considerably
refined by applying improved techniques and working with organisms having
less complex phycobilisomes (see above), the basic elements have remained unchanged : there is a morphological ordering from PE to PC to A P C when going
from the periphery to the center of the PB'some (see Fig. 2 in G A N T T , Chap.
6.3, this Vol.).
This sequence corresponds perfectly to the decrease in excitation energy
among the three pigments, which can thus form an energy transfer chain in
which the fluorescence of any preceding member overlaps reasonably well with
the absorption of the next one (Fig. 2). This model was refined by fluorescence
polarization experiments first undertaken by TEALE and D A L E (1970), which
suggested part of an energy transfer chain to be present already within each
individual biliprotein. The absorptions of PC's and PE's can be resolved into
components of slightly different energies. These are assigned to individual chromophores of often the same molecular structure, but with slightly different
absorption energies due to different interactions with the protein. The ones
absorbing at shorter wavelengths act as sensitizers (s) to the ones absorbing
and fluorescing at longer wavelengths (f chromophores), which provides an
efficient fine-tuning of the energy transfer.
In cyanobacteria, each individual pigment represents only a rather short
fragment of such an energy transfer chain. PC has, for example, one s chromophore on the /?- and one f chromophore on both the a- and /?-subunits. The
full transfer chain is completed by the aggregation with A P C and PE in the
PB'some. The cryptophytes represent the other extreme. They do not have
PB'somes, instead they have biliproteins which carry sufficiently different types
of chromophores to establish an energy transfer over the full absorption spectrum of biliproteins. The red algae, finally, use a combination of both. They
have PB'somes in which the major biliproteins already span a wide absorption
range.
max
max
332
H . SCHEER:
Chromophore
Type *
3
Absorption
Fluorescence
*inax
\ax
500
—
2 (s)
545
^
560
2 (f)
570
—
585
1 (s)
590
—
605
1 (0
620
^
635
515
/
Chlorophyll a j
650
—
686
-h»
Photooxidation
665
CD
Fig. 2. Energy transfer scheme of a phycobilisome. Righi a diagramatic representation
of a PB'some with only one outer rod containing B-PE (top double disk) and C-PC
(lower double disk). Vertical arrows correspond to longitudinal energy transfer, with the
downward direction strongly favored due to a larger overlap integral; horizontal arrows
to transversal energy transfer within the disks. Left approximate absorption and fluorescence maxima of the chromophores. *: 1 = phycocyanobilin, 2 = phycoerythrobilin, 3 =
phycourobilin
The energy transfer chain is completed by the transfer to the chlorophylls
within the photosynthetic membrane. Both the final donor in the PB'some and
the acceptor in the membrane have not yet been firmly established. At present,
the best candidates seem to be a large chromopeptide of the A P C core
(GINGRICH et al. 1983; REDLINGER and G A N T T 1982; RUSCHKOWSKI and ZILINS-
KAS 1982) and a chlorophyll protein close to or even identical with P-680,
respectively (CLEMENT-METRAL and G A N T T 1983, see also G A N T T , Chap. 6.3,
this Vol.).
5 Dynamics of Energy Transfer
A large fraction of the energy transfer in phycobiliproteins proceeds probably
via a FÖRSTER type process (see SAUER, Chap. 2; K N O X , Chap. 7.1, both this
Vol.). This has been deduced from the efficiency of the energy transfer on
one hand, and the low occurrence of strong couplings on the other. GRABOWSKI
and G A N T T (1978 a, b) have critically investigated a series of biliproteins and
calculated FÖRSTER'S critical distances, which are mostly in the range of 40-60 Â ,
333
7.5 Excitation Transfer in Phycobiliproteins
well beyond the diameter of the phycobiliprotein subunits ( « 3 0 Â). The formalism of FÖRSTER (1949) has been developed for a randomly ordered and fluctuating system with high acceptor and low donor concentrations. Since probably
none of these criteria applies to the phycobiliproteins (see above), a concise
theoretical treatment of the process is not yet possible (BLUMEN and M A N Z
1979; PEARLSTEIN 1982), but the critical radius is expected to be even larger
based on still incomplete data on the chromophore orientations (see e.g.,
ZICKENDRAHT et al. 1980; SCHIRMER et al. 1985; GILLBRO et al. 1983). The sec-
ond critical factor, i.e., the overlap integral between the donor fluorescence
and the acceptor absorption, is also fine-tuned in the biliproteins (see above).
Recent applications of picosecond time-resolved techniques to the energy
transfer process in biliproteins have principally verified this concept. The first
detailed investigations by SEARLE et al. (1978) established in Porphyridium omentum a sequential flow of excitation energy from PE via PC and APC to chlorophyll. The observed rates of excitation energy transfer could be fit by the
exp(t~ ) decay law characteristic for the classical FÖRSTER tansfer. Although
the actual kinetics can befitwell with a concise set of rise and decay times
for the PB'somes of this organism (WENDLER et al. 1984), the physical laws
governing the decay have been questioned. The better signal-to-noise ratios
of the current experiments still do not allow an unequivocal discrimination
between multi-exponential £ A e x p ( k t ) ] and non-exponential decay laws, but
generally favor the former. This is in particular supported by the observation
of corresponding decay and rise time constants in pairs of donors and acceptors,
respectively (WENDLER et al. 1984).
Qualitatively similar results have been obtained with entire PB'somes, as
well as with isolated phycobiliproteins and their subunits from several cyanobacteria and red algae (HEFFERLE et al. 1984a, b; HOLZWARTH et al. 1982; Ko1/2
BAYASHi et al. 1979; PELLEGRINO et al. 1981 ; SUTER et al. 1984; SWITALSKI and
SAUER 1984; W O N G et al. 1981 ; Y A M A Z A K I et al. 1984).
Photosynthetic antenna systems are optimized for high absorption crosssections and cooperativity. They thus present a problem for the interpretation
of time-resolved measurements, because *S— S annihilation can compete effil
ciently with energy transfer (see BRETON and GEACINTOV 1980; GEACINTOV and
BRETON, Chapter 7.4). This process has been demonstrated in phycobiliproteins
and investigated in detail by ALFANO'S group (ALFANO 1982; PELLEGRINO et al.
1981; W O N G et al. 1981). It can be distinguished from conventional excitation
energy transfer ( S —°S) by its dependence on the intensity of the exciting light.
More recent studies have thus focused on techniques which use only low photon
fluxes, e.g., repetitive streak cameras (HEFFERLE et al. 1984a, b) or single-photon
!
timing (HOLZWARTH et al. 1982; WENDLER et al. 1984; Y A M A Z A K I et al. 1984;
HOLZWARTH, Chap. 7.3, this Vol.). An advantage of the former is the ready
availability of polarized data, whereas the latter has an exceptionally high dynamic range and can thus detect even minor contributions.
Several criteria have been used to identify energy transfer in biliprotein
antenna systems. The first is the analysis of time-resolved depolarization. Due
to their rigid binding to proteins, rotational depolarization is generally thought
to be absent on the subnanosecond time scale, and depolarization is thus be-
334
H . SCHEER:
lieved to be due to energy transfer among chromophores (GILLBRO et al. 1983;
HEFFERLE et al. 1983, 1984a, b). It should be noted, however, that segmental
movements of the chromophores (HEFFERLE et al. 1984 b) and nonparallel excitation and emission dipoles (SWITALSKI and SAUER 1984) have been implicated
to rationalize the kinetics of some isolated biliproteins and their subunits. It
is also not trivial to obtain energy transfer time from the raw data (HEFFERLE
et al. 1984 a). The second criterion is the correspondence of decay time constants
in the donors with rise time constants in the acceptors, which are separated
by wavelength selective excitation and emission (HOLZWARTH et al. 1982;
WENDLER et al. 1984;
Y A M A Z A K I et al. 1984).
The following conclusions can be drawn from the results obtained until
now: the energy transfer from PE to the terminal APC chromophore proceeds
at a time scale <100ps (e.g., 60-70 ps in Porphyridium cruentum, WENDLER
et al. 1984; YAMAZAKI et al. 1984). It follows the pigment sequence expected
from their energetic and morphological ordering within the PB'somes. The energy transfer from PE to PC appears to be faster than that from PC to the
APC core (SUTER et al. 1984). In isolated biliproteins, the transfer times increase
with decreasing aggregation, e.g., from 70 ps in the trimer (ccß) to %500ps
in monomeric (ay?)! PC from Mastigocladus laminosus (HEFFERLE et al. 1984b).
The transfer times are also dependent on the species, the isolation procedure
and temperature. An intriguing conclusion might be drawn from the comparison
of isolated biliproteins with phycobilisomes, e.g., that the physiologically important longitudinal energy transfer toward the APC core is faster than the potentially wasteful transversal transfer within the platelets of the phycobilisome.
Currently, kinetic data are only available for a single cryptophytan pigment,
i.e., PC-645 from Chroomonas sp. (HOLZWARTH et al. 1983; KOBAYASHI et al.
1979). The findings support again a somewhat different behavior of the cryptophytan pigments compared to the PB'some-forming biliproteins. Differences
between the absorption and fluorescence excitation spectra have been discussed
in terms of a heterogeneous population of f chromophores, albeit with the
same decay kinetics, and the results support the presence of strongly coupled
chromophores (JUNG et al. 1980).
3
6 Physiological Status
Photosynthetic organisms are dynamic systems with the capacity to react to
environmental changes. These changes include the structure of the phycobilisomes, and their light-harvesting and energy-transfer capacities. The best investigated feature is the chromatic adaptation of many cyanobacteria, which involves changes in the composition and structure of the phycobilisomes in response to changes in the qualitity of light (BJÖRN 1979; G A N T T 1981;
GLAZER
1983). Other important factors are the nutritional and developmental status
of the organisms (CSATORDAY 1978). Considerably less is known about the
changes in the energy transfer kinetics in these systems. Using fluorescence
spectroscopy CSATORDAY (1978) has followed the repigmentation of Anacystis
7.5 Excitation Transfer in Phycobiliproteins
335
nidulans cells after nitrogen starvation. This approach allows for the detection
of particular biliproteins before they have been incorporated into the antenna
system. HARNISCHFEGER and CODD (1978) have observed a decrease in biliprotein
fluorescence after illumination of dark-adapted cells of the same organism,
which was correlated with an increased chlorophyll fluorescence. Changes of
the fluorescence yields (FORK et al. 1982) and kinetics (KARUKSTIS and SAUER
1984) upon treatment of algal cells with D C M U or desiccation, indicate the
involvement of different chlorophyll containing antennas, and possibly also
different P S II populations. This changed coupling between phycobilisomes and
membrane-bound pigments probably contributes to the chromatic transients
in cyanobacteria as well. These few examples have been chosen to illustrate
that the physiological status of the cells (as well as the isolation procedures
of PB'somes and their components) may produce significant changes in energy
transfer reactions, which must be considered in the interpretation of the physicochemical data.
Acknowledgements. The cited work of the author was supported by the Deutsche Forschungsgemeinschaft. I thank Drs. A . R . HOLZWARTH and S. SCHNEIDER for critically
reading the manuscript.
Notes Added in Proof: The field has been advancing rapidly after finishing the manuscript
for this mini review. Important aspects should be referenced.
The crystal structure has been determined for a second phycocyanin, viz. from Agmenellum quadruplicatum, which is hexameric instead of trimeric, but otherwise very similar
to that of M. laminosus (T. SCHIRMER, W. BODE, M . SCHNEIDER, W. BODE, M . MILLER,
M.L. HACKERT, J . M o l . Biol., in press). The details of chromophore structures and
the linkage to the apoprotein have been determined by chemical methods, including
the high-resolution N M R of bilipeptides (J.O. NAGY, J.E. BISHOP, A . V . KLOTZ, A . N .
GLAZER, H . RAPOPORT, J . Biol. Chem. 260, 4864-4868 (1985)), milder degradation methods (W. KUFER, G . SCHMIDT, O. SCHMID, H . SCHEER, Z . Naturforsch., in press) and
sequencing studies (W. SIDLER, B. KUMPF, H . ZUBER, W. RÜDIGER, Abstr. Vth. Int.
Symp. on Photosynthetic Procaryotes (ed. H . ZUBER, p. 303, 1985, E T H Zürich). The
results include the structure of the phycourobilin chromophore in R-PE and the characterization of singly and doubly bound chromophores, depending on the species and the
chromophore attachment site.
An assignment of spectrally distinct chromophores to the different chromophore
sites of PC from M. laminosus has been suggested on the basis of fluorescence polarization,
circular dichroism and photochemical reactivities (M. MIMURO, P. FÜGLISTALLER, R.
RÜMBELI, H . ZUBER, Abstr. Vth. Int. Symp. on Photosynthetic Procaryotes (ed. H . ZUBER,
1985, p. 276, E T H Zürich; W. JOHN, R. FISCHER, S. SIEBZEHNRÜBL, H . SCHEER, in Anten-
nas and Reaction Centers of Photosynthetic Bacteria - Structure, Interactions and Dynamics (eds. M . E . MICHEL-BEYERLE, H . SCHEER, S. FISCHER, Springer, Berlin - Heidelberg
- New York, in press).
Several new results have been presented on the excited state dynamics in biliproteins.
Fast (7-10 ps) decay times of the short-wavelength fluorescence and a corresponding
rise-term of the longer wavelength fluorescence has been demonstrated for PC 612 from
the cryptophyte, Hemiselmis virescens ( C A . HANZLIK, L . E . HANCOCK, R.S. KNOX, D .
GUARD-FRIAR, R. MACCOLL, J. Luminescence 34,99-106 (1985). All groups have adopted
the multi-exponential decay analysis, at least as a phenomenological approach, requiring
up to 5 components depending on the system and on the signal-to-noise ratios of the
data. The physical correctness of this approach has been supported by a global analysis
of data sets obtained at different excitation and emission wavelengths with a single set
of components (A.R. HOLZWARTH, in Antennas and Reaction Centers of Photosynthetic
Bacteria - Structure, Interactions and Dynamics (eds. M . E . MICHEL-BEYERLE, H . SCHEER,
336
H. SCHEER:
S. SCHNEIDER), Springer Verlag, Heidelberg, Berlin, New York, 1985, in press). This
method allows at the same time the extraction of time-resolved spectral information.
First data on the influence of linker peptides have shown only relatively small changes
in the excited state dynamics of an R- and a C-PC (S. SWITALSKI, K . SAUER, pers.
communication, J . WENDLER, W . JOHN, H . SCHEER, A . R . HOLZWARTH, unpublished re-
sults). The spectra of the individual components contributing to the emission have been
studied in a chromatically adapting cyanobacterium, Fremyella diplosiphon (M. MIMURO,
I. YAMAZAKI, T. YAMAZAKI, Y . FUJITA, Photochem. Photobiol. 41, 597-603 (1985). Partic-
ular attention has been paid to the relative importance of lateral and vertical energy
transfer, with the latter being favored in green-light adapted cells containing PE, PC
and APC. The uncoupling of phycobilisomes from the PSII-related chlorophylls has
been induced by heat stress in Anacystis nidulans (P. MOHANTY, S. HOSHINA, D.C. FORK,
Photochem. Photobiol. 41, 589-596 (1985). In an interesting application, tandem phycobiliprotein conjugates have been used as immunofluorescent probes with an unusually
large Stoke's shift due to the energy transfer from PE to APC (A.N. GLAZER, J. STRYER,
Biophys. J. 43, 383-386 (1983)).
References
Alfano R R (ed) (1982) Biological events probed by ultrafast laser spectroscopy. Academic
Press, London New York (See in particular chaps 6: Breton J, Geacintov N ; 17:
Doukas et al.; 18: Shank and Greene)
Björn LO (1979) Q Rev Biophys 12:1-25
Blumen A, Manz J (1979) J Chem Phys 71:46-94
Brandlmeier T, Scheer H , Rüdiger W (1981) Z Naturforsch 36c:431-439
Braslavsky SE, Holzwarth A R , Schaffner K (1983) Angew Chem 22:670-689, Angew
Chem Int Ed 20:656-674
Breton J, Geacintov N E (1980) Biochim Biophys Acta 594:1-32
Bryant D A (1982) J Gen Microbiol 128:835-844
Clement-Metrai JD, Gantt E (1983) FEBS Lett 156:185-188
Csatorday K (1978) Biochim Biophys Acta 504:341-343
Emerson R (1958) Annu Rev Plant Physiol 9:1-24
Falk H , Neufingerl F (1979) Monatsh Chem 110:987-1001
Falk H , Thirring K (1980) Z Naturforsch 35b:376-380
Förster T (1949) Z Naturforsch 4A:321-327
Fork DC, Öquist G , Hoch G E (1982) Plant Sei Lett 24:249-254
Frackowiak D, Erokhina L G , Fiksinski K (1979) Photosynthetica 13:245-253
Freidenreich P, Apell GS, Glazer A N (1978) J Biol Chem 253:212-219
Friedrich J, Scheer H , Zickendraht-Wendelstadt B, Haarer D (1981) J Am Chem Soc
103:1030-1035
Füglistaller P, Suter F, Zuber H (1983) Hoppe-Seyler's Z Physiol Chem 364:691-712
Gantt E (1979) Biochem Physiol Protozoa 1:121-137
Gantt E (1981) Annu Rev Plant Physiol 32:327-347
Gantt E, Conti SF (1966) J Cell Biol 29:423-434
Gillbro T, Sundström A, Sundström V, Holzwarth A R (1983) FEBS Lett 162:64^68
Gingrich JC, Lundell DJ, Glazer A N (1983) J Cell Biochem 22:1-14
Glazer A N (1980) In: Sigman D, Brazier M A B (eds) The evolution of protein structure
and function. Academic Press, London New York, pp 221-244
Glazer A N (1983) Annu Rev Biochem 52:125-157
Glazer A N , Williams R C , Yamanaka G , Schachman H K (1979) Proc Natl Acad Sci
USA 76:6162-6166
Grabowski J, Gantt E (1978 a) Photochem Photobiol 28:39-45
Grabowski J, Gantt E (1978b) Photochem Photobiol 28:47-54
Harnischfeger G , Codd G A (1978) Biochim Biophys Acta 502:507-513
7.5 Excitation Transfer in Phycobiliproteins
337
Hefferle P, Nies M , Wehrmeyer W, Schneider S (1983) Photobiochem Photobiophys
5:325-334
Hefferle P, John W, Scheer H , Schneider S (1984a) Photochem Photobiol 39:221-232
Hefferle P, Geiselhart P, Mindl T, Schneider S, John W, Scheer H (1984b) Z Naturforsch
39c:606-616
Holzwarth AR, Wendler W, Wehrmeyer W (1982) Photochem Photobiol 36:479-487
Holzwarth AR, Wendler W, Wehrmeyer W (1983) Biochim Biophys Acta 724:388-395
Jung J, Song PS, Paxton RJ, Edelstein MS, Swanson R, Hazen Jr EE (1980) Biochemistry
19:24^32
Karukstis K K , Sauer K (1984) Biochim Biophys Acta 766:141-147
Kobayashi T, Degenkolb EO, Behrson R, Rentzepis P M , MacColl R, Berns DS (1979)
Biochemistry 18:5073-5078
Köst-Reyes E, Köst H P (1979) Eur J Biochem 102:83-91
Krasnovskii A A , Erokhina L G (1969) Dokl Acad Nauk SSSR 186:957-960
Kufer W, Scheer H , Holzwarth A R (1983) Isr J Chem 23:233-240
Lagarias JC, Glazer A N , Rapoport H (1979) J Am Chem Soc 101:5030-5037
Land EJ (1979) Photochem Photobiol 29:483-487
MacColl R (1982) Photochem Photobiol 35:899-904
MacColl R, Berns DS (1981) Isr J Chem 21:296-300
MacColl R, Guard-Friar D (1983) Biochemistry 22:5568-5572
Mörschel E, Wehrmeyer W (1975) Arch Microbiol 105:153-158
Mörschel E, Koller K , Wehrmeyer W (1980) Arch Microbiol 125:43-51
Morisset W, Wehrmeyer W, Schirmer T, Bode W (1984) Arch Microbiol 140:202-205
Offner GD, Troxler R F (1983) J Biol Chem 258:9931-9940
Pearlstein R M (1982) Photochem Photobiol 35:835-844
Pellegrino F, Wong D , Alfano RR, Zilinskas B (1981) Photochem Photobiol 34:691-696
Pratt L H (1978) Photochem Photobiol 27:81-105
Pratt L H (1982) Annu Rev Plant 33:557-582
Rapoport H , Glazer A N (1984) In: Blauer G , Sund H (eds) Optical properties and
structure of tetrapyrroles. De Gruyter, Berlin, pp 411-423
Redlinger T, Gantt E (1982) Proc Natl Acad Sci USA 79:5542-5546
Rüdiger W (1979) Ber Dtsch Bot Ges 92:414^426
Rüdiger W (1980) Struct Bond 40:101-140
Rüdiger W, Scheer H (1983) In: Shropshire W, Möhr H (eds) Photomorphogenesis.
Encyclopedia of Plant Physiology Vol 16. Springer, Berlin Heidelberg New York,
pp 119-151
Rusckowski M , Zilinskas BA (1982) Plant Physiol 70:1055-1059
Scheer H (1981) Angew Chem 93:230-250, Angew Chem Int Ed 20:241-261
Scheer H (1982) In: Fong F K (ed) Light reaction path of photosynthesis. Springer,
Berlin Heidelberg New York, pp 7-45
Schirmer T, Bode W, Huber R, Sidler W, Zuber H (1985) J Mol Biol 184:257-277
Searle GFW, Barber J, Porter G, Tredwell CJ (1978) Biochim Biophys Acta 501:246-256
Siegelman HW, Kycia H (1982) Plant Physiol 70: 887-897
Suter GW, Mazzola P, Wendler J, Holzwarth A R (1984) Biochim Biophys Acta
766:269-276
Switalski SC, Sauer K (1984) Photochem Photobiol 40:423-427
Teale FWJ, Dale R E (1970) Biochem J 116:161-169
Wanner G, Köst H P (1980) Protoplasma 102:97-109
Wehrmeyer W (1983) In: Jensen U , Fairbrothers D E (eds) Proteins and nucleic acids
in plant systematics. Springer, Berlin Heidelberg New York, pp 143-167
Wendler J, Holzwarth A R , Wehrmeyer W (1984) Biochim Biophys Acta 765:58-67
Wong D, Pellegrino F, Alfano R R , Zilinskas BA (1981) Photochem Photobiol
33:651-662
Yamazaki I, Mimuro M , Murao T, Yamazaki K , Yoshihara K , Fujita Y (1984) Photochem Photobiol 39:233-240
Zickendraht-Wendelstadt B, Friedrich J, Rüdiger W (1980) Photochem Photobiol
31:367-376
Zuber H (1978) Ber Dtsch Bot Ges 91:459-474
Subject Index
A(F ) 481
A
482
absorbance spectra of bacteria 99
of bacterial reaction centers 120
of siphonaxanthin-Chl a/b-proteins 275
absorption, band broadening 90
cross-section 88
determining factors 319
magnetic resonance 401
acclimation, low temperature 37
Acetabularia 2
acyl lipids 693-703
chlorophyll-protein complexes 696-705, 713
lateral heterogeneity 697, 703
thylakoid membrane 693-705, 713
transverse distribution 699, 706
unsaturation 695
adenylate sulfate 217
A D M R 363, 401, 409, 410
A D P sulfurase 217
A D R Y reagent 430
aging of thylakoids 393
algae, chloroplast membrane organization 6,
53-61
Chromophyta 58-61
eukaryotic, systematic organization 599
evolution 8
green 299
pigment-protein complexes 116
red 26,53,241,327
thylakoid membranes 281
allophycocyanin 241
Alocasia 24
alternating site hypothesis 187
Amaranthus 25, 597
amino acid sequence 132, 231, 243
9-aminoacridine 655
amphipathic protein 150
Anabaena 53, 173, 263, 496
Anacystis 261, 335, 649
annihilation, of excitons 291
antenna (see also light harvesting complexes)
89, 98-135
^-apoproteins 258
^-carotene 13
A
2
chlorophyll a 325
complex, bacterial 252, 257
isolation 245
effect 287
L H I 252, 257
L H II 252, 257
mobile 48
photosystem I 152, 170
photosystem II 264
pigments 299
anthracene-tetracene model system 287
antibodies, cytochrome b / f 42
cytochrome C
626
H , L , M subunits 622
lipid 699, 720
Nostoc 265
oxygen-evolving system 451
antioxidant 470
appressed membrane regions 720
asymmetry, lipid 719
A T P synthase 42-44, 229-230, 650
activation 584
binding 588, 590
coupling 229
inactive-active transition 567
phosphoryl transfer 588
stereochemistry 588
stoichiometry 229
structure 229
topology 627
A T P synthesis 564, 576
artificial ion gradients 565
flashing light 564
inhibition 597
lag 574
ATPase (see A T P synthase)
ATP-binding (see nucleotide binding)
atrazine 24, 597
A triplex 25
azidoatrazine 379, 461
6
2
B(Bulk)-820, nomenclature
B-790 392
B-790, chlorosome 392
252
792
B-800-820, antennae 125, 245, 257
protein 107, 124
spectral analysis 99
B-800-850, antennae 107, 123, 125, 245
nomenclature 252
protein structure 133
spectral analysis 99
B-800-850 protein comparison 124
B-850-protein 123
B-875-890, antennae 246
B-875-protein 123, 125
B-890-spectral analysis 99
B-890-protein 107, 123, 124, 125, 132
structure 133
b-cycle 176
Bacillariophyceae 6
bacteria, green 197-232, 371, 390-399, 605-610
chlorophyll-complexes 126
bacteria, purple, alpha-apoproteins 258
photosynthetic membranes 197-232, 604,
610-617, 620-630, 632-638
reaction centers 113, 119-125, 457, 458
bacteriochlorophyll a, antennae 246
bacteriochlorophyll a-protein, green bacteria
102, 126, 132, 133
bacteriochlorophyll a, purple bacteria 119-125
bacteriochlorophyll anion 354
bacteriochlorophyll b, absorbance 102
bacteriochlorophyll, B-890 253
fluorescence 624
photon absorbtion 338
reaction center 93
special pair 94
bacteriochlorophyll binding 382
bacteriochlorophyll-binding proteins 633, 638
bacteriochlorophyll c 126, 392
bacteriochlorophyll cation 354
bacteriochlorophyll d 126
bacteriochlorophyll e 126
bacteriopheophytin, green bacteria 119, 121
purple bacteria 119,121
reaction center 338
barley 665
be, complex 208, 209
BChl (see bacteriochlorophyll) bilayer, fluidity
155
integral membrane proteins 150, 152
lipids 149, 157, 716
bentazon 23
/?-carotene 269, 273
antennae 272
orientation 484
photosystem I 109, 110, 273
photosystem II 273
biliprotein organization 329
biliprotein, transfer time 334
Subject Index
biliproteins, aggregation 329
binding site, chromophore 244, 249
bipyridyliums 595
blue light, prolamellar body 690
bridging intermediates 355
brown algae 58-61,270-273,276-282
buried domain, lumen pH 572
C pathway 4
C thylakoid morphology 25
calcium 438, 452, 453
calmodulin antagonists of photosystem II 649
carbanilates 595
carotenes, green bacteria 126
carotenoid-Chl a/c-protein 277
carotenoids 101, 106
algae 116
B-890-protein 99
bacteria 119, 122, 253, 398
biosynthesis 597-598
etioplasts 586-598
mutants 625
catalytic hydrogénation, fatty acyl chains 694
catalytic mechanism 587-589
Caulerpa 10
C C I (see also chlorophyll protein complexes)
105, 108-111, 116, 118, 119, 130, 135
C C II (see also chlorophyll protein complexes)
105, 108, 112, 113, 116, 118, 130
CF (see coupling factor and A T P synthase)
C F (see coupling factor and A T P synthase)
charge recombination, fluorescence 306
Klimov mechanism 302
model 325
pheophytin 307
charge separation 93, 94
annihilation 354
radical pair 353
charge transfer, reaction center 412
transitions 340
zero field splitting 403
chemiosomotic theory 179,180,181
chilling injury 67, 718
Chi a-P2 130
Chla-P3 130
chi a/b L H C (see also light harvesting complex) 31,35,44-47
chla/b-Pl 130
chi a/c 277, 278
chi d 271
c h l c 271,280
Chlamydomonas 8, 13, 161, 471, 490, 668
chloramphenicol 472
Chlorella 2, 304, 305, 313
chloride, 0 evolution 438, 452
Chlor obiaceae, reaction center 208, 390-398,
604-610
4
4
{
0
2
2
Subject Index
Chlorobium 127, 390-398, 496, 604-610, 545
chlorobium vesicles (see chlorosomes)
Chloroßexacae
119, 121, 122, 126, 127, 150,
390-398, 604-610
Chlorophyceae 6
chlorophyll 104
reaction center 93
chlorophyll a 100
in algae 269, 273
in reaction center I 110, 273
in reaction center II 273-274
orientation 319
P-700 477
special pair 374
surrounding chlorophyll b 114
chlorophyll a/b ratio 101, 114
chlorophyll b 100, 276
linear dichroism 321
chlorophyll biosynthesis 598, 702
chlorophyll c 58, 116
chlorophyll Cj 271
chlorophyll c
271
chlorophyll proteins (see reaction center and
light-harveating complexes)
Chlorophyta 270, 274, 281, 282, 284
chloroplast, D N A 11
envelope 2-10, 706
evolution (see evolution)
membrane components 35
morphology 1, 665
stroma 10-14
survival after isolation 10
chlorosomes 126, 390, 391-393, 605, 606, 609
assembly 610
baseplate 607
core 618
envelope 607
rod elements 607
chromatic adaptation 18, 264, 334
chromatic transients 335
Chromatium 122, 124, 256, 545
chromatophores 88, 201, 245, 328, 562-565
chromophyta 58-61, 270, 276-282
Chroomonas 334
Chrysophyceae 6, 279-280
circular dichroism, biliproteins 330
B-890 254
P-700 479
C0 -fixation 468
Codium 10, 275
coherence 292
conformational changes of protein complexes
571, 590
conformers 330
cooperativity in A T P synthase 586
copper binding 548
core complex I (see CCI)
2
2
793
counter ions 653
coupling factor (see also A T P synthase) 42,
152, 160, 187
chlorophyll ratio 580, 581
cooperativity 580, 581
distribution 42, 50
genetic analysis 581
light activation 186
lipid requirement 152
localization 158, 181
molecular weight 586
nucleotide interactions 584
of photosynthetic bacteria 185
organization 577
per chlorophyll 152, 153, 182
PFu particles 43
proton translocation 183, 576
reconstituted 43, 676
regulation 579
roles of subunits 578
structure 576, 577
substrates 579
subunit stoichiometry 577
CP (see also chlorophyll proteins)
CP1 109
CP 29 44, 108, 113, 130
CP 43 108, 112, 433, 459
amino acid sequence 460
CP 47 108, 112, 433, 459
amino acid sequence 459
CP I 40, 103, 130, 483, 488, 493, 642
C P I * 110
CP la 110
C P U 44, 103, 108, 130, 642
C P U * 44
CP III 104, 108, 130, 433, 642
CP IV 104, 108, 112, 130, 433, 642
C P V 642
CPa 108, 130
CPO 40, 112
Cr
551
cross-linkers, chemical 622
Cryptomonads 277
Cryptomonas 59
Cryptophyceae 6, 280, 282, 327
crystals of reaction centers 372, 625
cyanelles 28
Cyanidium 53, 57, 329
cyanobacteria 15, 53, 116, 143, 270
genes 640
lipid composition 150
pigment-protein complexes 117-119
photosystem I 169, 170
photosystem II 459
phycobilisomes 241, 327
structure 15, 17, 281, 282, 284
thermophilic 69
3 +
794
Subject Index
Cyanophora 26, 53, 268
cyclic-helical conformation 330
cytochrome b 540
cytochrome b-559 159, 160, 383, 444, 453, 458
cytochrome b gene 503
cytochrome bc complex 496, 497
components 539
electron flow 539-546
mitochondria 496, 545
stoichiometrics 541-542
topology 626
cytochrome b / f complex 40-42, 50, 145, 152,
160, 177, 178, 181, 496, 516-524, 528, 640,
649
electron transport 172
freeze-fracture 174
hydropathy plots 189
localization 158, 532
proteins 152
proton translocator 679
Q-cycle 175, 176
reconstitution 42, 679
cytochrome b / f complex ratio with photosystems 182
cytochrome c 220-228, 373, 378
heme structure 224, 225
high-low potential forms 220, 227
cytochrome c-552 228, 394, 548, 650
cytochrome c 539-540
gene 503
cytochrome c
626
cytochrome f 160, 173, 174, 531, 533,
554-555, 649
cytochrome f topology 627
cytochrome f reaction with plastocyanin 555
cytochrome oxidase 444
t
6
6
{
2
D-l protein (see also Q protein) 385, 460
D-2 protein 372, 379, 385, 460, 462
DBMIB 174, 177, 595
DCCD-binding protein 627
D C M U 596
decay laws 333
decay rates 403, 405
decay time constants 334
delayed fluorescence 340
derealization 286, 288, 292
depolarization 334
Deriphat 160, 105, 130
desaturase complex 598
development 702
D G D G (see digalactosyldiacylglycerol)
diacyl lipids 149, 677
diffusion 177
diacylglycerol synthesis 708, 709
diacylsulfoquinovosylglycerol 150, 151, 157,
686, 696-699, 702, 713
B
diatoms 277, 279
diffuse layer 653
diffusion coefficients 177, 178, 510, 512, 513
constant of exciton 294
Fick's laws 510
Stokes-Einstein equation 510, 511
difunon 595
digalactosyldiacylglycerol 696, 697, 699, 700,
702, 713
in prolamellar bodies 72, 687, 688
in thylakoids 150-158, 178
structure 151,713-725
dimer of P-700 478
dinoflagellates 280
Dinophyceae 6
diphenyl ethers 595
diphenylamines 595
dipole-dipole interaction tensor 400, 402
diuron 164
DNP-INT 595
Doppler shift 655
double resonant 403
DTP 595
D T T 590
edge particles 609
E F particles 30-72, 665-673
EFs particles 32, 44, 668
EFu particles 32, 44, 668
electric field 85, 95
electrochemical potential 183
electrochromic band shift 176
electron acceptors 93, 338, 339, 480-483
electron donors 93, 165-174
electron flow, reverse 211
electron microscopy, freeze-fracture 1-72,
665-674, 718
electron spin resonance 400-402
electron transfer 161-162, 169-170, 200
electron transport 87, 92-93, 161-167,
172-179
electrical responses 347
in bacteria 198-200, 338-342
in cytochrome be complexes 496
in photosystem I 476-485
in photosystem II 447
inhibition 596-597
long range 555
electron tunneling 344, 349, 350.
electrophoresis 98-135, 641
emission 303, 319
E N D O R 360-361,479
endosymbiotic 5-10, 19, 143
energetics 338
energy conversion 87
energy distribution, PS I and PS II 64-66, 657,
660
Subject Index
energy transfer 238, 250, 331
dynamics 332
1S-1S annihilation 333
energy trapping 319-325
energy-linked binding change mechanism 588
envelope membranes 2-10,708-711
EPR 224,438,479
ethylenediamine 551
etioplasts 70-72, 683-691
Euglenophyceae 6
evolution 8, 197, 238-251, 265, 329, 371-380,
382-388
exchange energy 400
excitation derealization 286-297
excitation energy transfer 47, 48, 86, 90, 267,
668
excited state 88
exciton 90, 294, 412, 413
annihilation 310, 315
coupling 250, 410
delocalized 90
lifetimes 313
splitting 289
theory 479
trapping 325
eyespots 13-14
f chromophores 331,334
F-685 322
F-695 322
F (see coupling factor and A T P synthase)
F i subunits 651
fast component 302
fatty acids 24, 693, 700, 708, 710, 713
FDMIR 407
F D M R 401, 410
Fe(II) binding 382
Fe-S center 536
Fe-S protein 533, 537
feedback mechanism, phosphorylation 66
ferredoxin N A D P oxidoreductase 160, 168,
171, 172, 176, 177, 476, 650
flavodoxin 650
fluidity of thylakoid membrane 67, 662, 694,
695, 697, 698
fluometuron 23
fluorescence 299,311,313,340
decay 301, 313-316
detected magnetic resonance 401
of chlorophyll 299,301,641
of photosystem I 305, 425-426
of photosystem II 425-426
of phycobilisomes 331
photosynthetic capacity 468
polarization 289, 331
quenchers 286, 315
spectra 320
t
795
surface charge 656
yield 302
F (see coupling factor and A T P synthase)
Forster transfer 92, 290, 332, 333
F R A P 511
freeze-fracture 1-72
nomenclature 30
of bacterial membranes 605-617
of envelope membranes 9, 10
of prolammellar bodies 71, 72
of thylakoid membrane 20, 21, 30-72,
665-674
Fremyella 266
fucoxanthin 116, 271, 272
fucoxanthin-Chl a-proteins 116, 277-279
Fucus 60
F
482
0
x
g=4.1 EPR signal 438
galactolipid synthesis (see also mono- and digalactosyldiacylglycerol) 707-711
galactose 715
galactosyl transferase 708
gel phase 716
Glaucocystis 28
Gloeobacter 19, 55, 263
glycolipid (see mono- and digalactosyldiacylglycerol)
glycoproteins 154
Gonyaulax 61
Gouy-Chapman theory 653
grana, formation 47
grana membranes 38, 114, 147-149, 155-157,
177, 653-663, 665
greening 493, 684, 702
Griffithsia 26, 261
group transfer reaction 184, 187
+
H / A T P stoichiometry 579
H / P ratio 561
H-ATPase (see also proton) 576
H-subunit 121, 356, 376, 382-388, 397, 615,
629
H 0 as a reduced substrate 213
H S as a reduced substrate 213
heat stress 66-67
Heliobacterium 605, 610
Helmholtz layer 654
Hemiselmis 29
herbicide list 601
herbicide resistance 165, 695
herbicides 23, 164, 165, 379, 461, 686
electron transport 24, 462
sites of inhibition 465, 595-602
heterocyst 53
hexagonal II phase 689, 713-724
19' hexanoylfucoxanthin 279
+
2
2
796
Subject Index
HgCl
550
histidine 623, 625
homology in reaction center 385
hydrogen bonding chains 571
hydropathy indexes 660
hydrophobic markers 622
hydrophobic proteins 384
hydrophobicity plots 134
hyperfine coupling 479
2
ICM (intracytoplasmic membrane), aerobic
growth 637
formation 613-615, 617, 636
function and structure 634
induction 615, 635
0 and light control 632, 635
protein insertion 634
synthesis 637
Ilf 440
Ilvf 440
immunological techniques (see antibodies)
induction, anaerobic 613, 615
membrane 618
inner bulk phases 574
interchromophore interactions 330
intermittent light 303
internal conversion 330
intersystem crossing 402
intracytoplasmic membrane (see ICM)
inverted micelles 689, 722
iodination 641
IPI 474
iron-sulfur centers, PS I 171, 180, 181, 481
iron-sulfur cluster, cyt b / f complex 673
iron-sulfur proteins 643
isoelectronic 653
2
6
K C N 550
kinetics of electron transfer reactions
kinetics, single turnover 221
Klimov mechanism 301, 307
338
L-subunit 376
lake model 312
lasers 310
lateral asymmetry 157, 158
lateral heterogeneity 35, 49, 177, 282, 720-721
lateral migration of membrane components
61-64, 660, 661
lateral separation of membrane proteins 182,
662, 673
lauryl dimethylamine oxide 106
L D 319-321,424
LDS-Page 641
L H I 616,633
L H II 636
L H C (see also light harvesting complex)
L H C , chi a/b-protein 31, 35, 44^47, 108
L H C I 40, 50, 108-112, 116, 130, 274, 276
absorption spectra 490
electrophoretic mobility 497
nomenclature 105
subunits 490, 497
L H C II 108, 113-116, 130, 133, 135, 21A-216
excitation transfer 680
fluorescence 303, 304
nomenclature 105
reconstitution studies 677
structure 134
L H C P (see also light harvesting complexes)
108
L H C P 1 130
L H C P 2 130
L H C P 3 130
L H P 621
lifetimes 302
light activation 186
light-harvesting apparatus, adaptation 327
light-harvesting complex 98-135, 641-644
bound 35
chi a 325
chla/b 19,44,320
chi c-protein 277
development 100
freeze-fractured 46
intermittent light 135, 303
isolation 128-131
lipid association 696-702, 724
membrane adhesion factor 45
mobile 31, 35, 44, 50, 64, 65
of algae 269-684
of bacteria 117,124, 238-250, 252-258, 618,
621
particles 66
PFs particles 668
polypeptides 161
protein 105
reconstituted 45
three-dimensional map 47
topology 621-626
light-harvesting, long term modulation
283
light-harvesting pigment proteins 238, 246,
250
light-harvesting pigments, accessory 14
light-harvesting polypeptides, alpha and beta
250
evolution 240
light-harvesting strategies 282
light-harvesting systems, accessory 16
linear dichroic triplet-minus-singlet absorption
413-417
linear dichroism 319-321, 424
Subject Index
linolenic acid 24, 662, 698, 701
lipid, boundary 152
lipid enrichment of thylakoid membranes 698
lipid extraction 694
lipid pools 703
lipid-protein interactions 693-705, 722
lipid to protein ratio 697-699
lipid transfer 710
lipids (see also acyl lipids and mono- and digalactosyldiacylglycerols), eukaryotic 707
prokaryotic 707
surface charge 656
lipolytic treatment of thylakoid membranes
699-702
lipophilic anions 443
liposomes 42, 38, 672
liquid-crystalline phase 716
lithium dodecyl sulfate 104
localized domains 570
Lolium 20
low oxygen tension 613
L-subunit 121, 356, 376, 383-388, 397, 626,
629
luminescence 425
lutein 272
lutein-chl a/b proteins 274
lysine-specific protease 465
+
M
438
m-phehoxybenzamides 595
M-subunit 121, 356, 376, 383-388, 397, 626,
629
macromolecules, assembly 638
magnesium ions, proton gradient 229
magnetic fields 340, 341
magnetic resonance technique 356, 400
magnetophotoselection 402, 405
manganese 438, 450, 668
Master Equation 294
Mastigocladus 57, 242, 329, 334
melittin 699
membrane, adhesion factor 45
architecture 603
asymmetry, lipid 719
attachment site, chlorosomes 608, 609
fluidity 155
fracture faces, nomenclature 30
kinase 659
labeling 621
lipids, phase transitions 67, 155
morphology 69
phosphatase 659
position of redox center 350
protein, amphipathic 150
reconstitution 34-50, 675
stacking 45, 63, 146, 148, 149, 154, 155,
656, 697
797
membranes, appressed 63, 656, 697
cytoplasmic 390, 393
electrical properties 202
envelope 2-10, 706, 710
extra-chloroplastic 5
fluid mosaic model 620
inner envelopes 4
intracytoplasmic 390
lateral heterogeneity 35, 49, 177, 282, 720,
721
non-appressed 14-25, 656, 697
menaquinone 372, 375, 394
metastable buffered proton pool 572
metastable proton pool 572
methabenthiazuron 23
M G D G (see monogalactosyldiacylglycerol)
Micrasterias 2
microsecond laser pulse 310
microwave induced fluorescence spectra
407-408
microwave selection 413
M I F 407,408
migration of exitation 286
mitochondrial bc complex 496
mitochondrial electron transfer 200
mitochondrial evolution and symbiosis 197
MK-616 595
modification, chemical 571
molecular ecology 328
molecular excitation, localized 90
molecular triplet PR 367
monogalactolipid (see monogalactosyldiacylglycerol)
monogalactosyldiacylglycerol, biogenesis 702
degree of unsaturation 696
in prolamellar bodies 72, 683-692
in thylakoid membranes 150-158, 696-700
structure 713-725
monolayer 721
monopole approximation 292, 293
morphological organization of phycobilisomes
331
morphology of bacterial reaction center 420
Mossbauer spectroscopy 481
multigene family of L H C II 114
multiline signal 439
mutants, chlorophyll b-less 37, 45, 103,
666-669
carotenoid 481
herbicide resistance 462, 595-597
PS I 39,669
PS II 34, 35, 668
ultrastructure 665-674, 689
water oxidation 450
x
+
N A D reduction 206, 210
N A D P reduction 206, 212
+
798
Subject Index
nearest neighbor analysis of water-splitting enzymes 451
Neoghardiella 267
Nerium 67
neutron diffraction 624
N H groups 574
N H O H 437
NH
437
nitrofen 595
non-heme iron 375
nonappressed regions 720
norflurazon 595
Nostoc 263
nucleotide-binding sites 585-587
nucleotides, exchangeable 586
tightly bound 586, 591
2
2
3
O-phenanthroline 376
Ochromonas 1
octyl glucoside 129, 591
O D M R 362-367,400
ohmic components 567
one-electron intermediate 382
optical absorption cross-section 314, 316
optical transition dipole moments 348, 349
orientation of optical transition moments
404-406
of pigment molecules 319-325, 484
overlap integral of biliproteins 333
oxadiazon 595
oxidation rate 222
oxidizing potentials of reaction centers 214
oxygen-evolving complex, 10 kDa protein 453
16 kDa protein 447
23 kDa protein 447
32 kDa protein 447
oxygen-evolving systems 231, 437-445,
447-456
oxygen radicals 470
oxygen regulation 635
P-430 171,481
P-680 112, 160, 162, 165, 170, 321
dimer vs. monomer 423
P-680 reduction kinetics 427
P-700 145,160,169-172,321,476-485,
487-494, 669
of cyanobacteria 118,647,649,650
P-700 reduction kinetics 172, 175, 553,
556-557
P-700, apoprotein 127
chlorophyll a-protein 103, 108, 109
reduction by plastoxyanin 552-554
P-870 121, 122
primary donor complex 357
P-960 121, 122
P/2e ratio 561
+
+
pairwise transfer 288-293
particle electrophoresis 654, 655
particle size histograms 33, 666
particles, intramembrane 34, 62, 665-674
PC (phycocyanin) 330
PChl(ide) 686
PCR 689
perforated lamellae 689
peridinin 271, 272
peridinin-Chl a-protein 117, 280, 281
peripheral reticulum 4
permeability of thylakoid membranes 156
peroxidation 599-601
herbicide induced 600
pF 339
radical pair 354
PF particles 30-72, 665-673
pH in lumen 570, 572
pH-clamp 572
pH-gradient 186, 560
pH-indicating dye 573
Phaeophyceae 6
Phaeophyta 277
phase transitions (see also lipids) 67-70, 155
phehylhydrozones 595
pheophytin 93, 159, 162, 424-427
phonon wing 412
Phormidium 118
phosphate group transfer 180, 187
phosphate-water-oxygen exchange 589
phosphatidylcholine 150, 151, 155, 696-703,
713
phosphatidylethanolamine 714
phosphatidylglycerol 150, 151, 157, 694-702, 711
phospholipase A
701
phospholipase C 701
phospholipase D 701
phospholipid (see also lipids) 628, 686, 688,
716, 677
insertion into ICM 616, 634
phosphorescence 401
phosphoryl group transfer 144, 145
phosphorylating units 181, 182
phosphorylation, external electric field 565
fluorescence 304
in Porphyridium 267
kinetic analysis 565
maximal affinity 562
onset lag 574
rate 567
phosphorylation/dephosphorylation of proteins 64, 115, 659
photoaffinity herbicides 461
photobleaching 470
photochemical reaction centers 106
photoinhibition 461, 468-474
photon absorption 85
2
Subject Index
photon correlation length 289
photophosphorylation 179-189, 560, 561, 651
photorespiration 469
photoselection 349, 413
photosynthetic bacteria 15, 98, 102, 106, 107,
197-232, 252-258, 338-342, 344-351,
371-380, 382-388, 390-398, 603-619,
620-630
photosynthetic electron transport 31, 145
photosynthetic membrane biogenesis 632-639,
702
photosynthetic membrane morphology 1-72,
146-158, 603-618, 620-630
photosynthetic unit 288, 633
photosynthetic water oxidation 437-445,
447-455
photosystem I (see also P-700), assembly 492,
493
chlorophyll-proteins 101, 103, 108, 111, 275
complexes 39, 40, 109-112, 160, 168-172,
492
core complex 40, 169
cyanobacteria 118, 640, 647, 649, 650
digitonin particles 553
energy conversion 87
fluorescence quenching 313
L D peak 321
lipolytic hydrolase effects 724
localization on fracture faces 39, 40, 492,
669
localization in thylakoids 35, 39, 40, 517,
669-671
mobility 521
of algae 273
of Prochloron 276
reaction center electron transfer 476-485,
553
reconstitution 39, 679
relationship to phycobilisomes 266
similarities with bacterial reaction centers
208, 371
siphoxanthin-chl a/b proteins 276
subunit III 553-554
surface charge 552
Triton X-100 particles 553
photosystem II 87
antennae 112-115, 264
bound antennae 44
carotenoid oxidation 430
charge separation 422
chlorophyll a-proteins 273
chlorophyll-proteins 101, 103, 108
C l ~ requirement 573
cofactors 457
composition 112-115,158-168, 457-467
core complex 35, 458
cytochrome b-559 430
799
distance to nearest neighbor 516, 518
E F particles 34-38, 48, 671-672
electrogenic reaction 423
fluorescence 426
fluorescence quenching 313
freeze-fracture particles 32-63, 48, 55
gene sequences 458
in cyanobacteria 640, 644-649
isolation 102
L D spectrum 321
lipolytic hydrolase effects 724
localization in thylakoids 31, 34-38, 517,
671-672
mobility 521
mutants 34, 671-672
oxygen-evolving preparations 38
oxygen evolving system 437-445, 447-455
polypeptides 433, 434
populations 335
primary reactants 422
Q protein 380, 457-463, 468-474
reaction center 422-435, 457
reaction centers, bacteria vs. plants
371-380, 383, 457
reconstituted complexes 38
redox potentials 426, 427
relationship to phycobilisomes 56-58, 226,
331
siphonaxanthin-chl a/b proteins 275
subunits 457, 458
photosystem II to photosystem I ratio 53, 517
photosystem II, 34 kDa protein 453
47 kDa protein 380, 453, 596
a-centers 37, 38, 304, 433
a-ß heterogeneity 308
photosystem II, ^-centers 37, 38
phycobilin 244
phycobiliproteins (see also phycobilisomes)
117, 118, 241, 260-268, 327
heterodimers 250
phycobilisomes 260-268
association with photosystem II 56-58,
266-269, 644
compared to chlorosomes 393
emission 262
hemispherical type 26
isolation 261
light regulation 18
linker peptides 329
molecular ecology 328
polypeptides 241, 331
reconstitution 266
structure 18, 53, 262-266, 329
phycocyanin 241, 280
phycocyanobilin 327
phycoerythrin 241, 280
phycoerythrobilin 327
B
800
phycourobilin 327
phylogenetic relationship of pigment proteins
244, 248
phytochrome 330
phytoplankton 469
phytyl side chains 375
phytylation 690
picosecond fluorescence decays 299
picosecond laser pulse 310
picosecond time-resolved techniques 333
pigment arrangement 374
terminal 264
pigment-proteins (see also light-harvesting complexes), spectral analysis 99
synthesis 611
pigments, distribution among algae 16, 269
Pisum 385
plants, shade 24
plastocyanin 145, 160, 168-179, 512, 518,
547-559
binding site at PS I 554
chemical modification 550
electron transfer site 550, 551
inhibitors 550
isoelectric point (pi) 552
mobility 179, 518-524, 556
molecular structure 171, 548, 549
rate constants 552, 553
reaction with cytochrome f 555
synthesis 547
plastocyanin to P-700 ratio 557
plastoglobuli 1
plastohydroquinone 441, 724
plastoquinol 145, 173-176
plastoquinone (see also quinone) 153-156,
172, 177, 518, 531
and cytochrome b6/f 174
and photosystem II 158-164
mobility 178, 179, 521-522, 695, 724
plastosemiquinone 165, 429, 471
polarized emission 322
polypeptides, primary sequence of light-harvesting 382, 240
Porphyridium 2, 26, 261, 331, 333, 334
Portulacca 5
post-translationally imported proteins 451
potential, transmembrane 566
primary acceptor, of bacteria 354
of photosystem I 477
of photosystem II 324
primary donor, exciton trapping 325
of photosystem I 477
primary reactions in bacteria 338
primary structure 248
Prochloron 15, 19, 143, 276
Prochlorophyta 276
prolamellar bodies 70-72, 683-692
Subject Index
Prosthecochloris 127
protease digestion of L and M subunits 622
protein acid-base dissociation groups 570
protein synthesis associated with photoinhibition 473, 474
protein targeting 638
prothylakoids 70, 686, 687
protochlorophyllide reductase 687
proton buffering domains 571
proton channel forming proteins 574
proton currents, intramembrane 567
proton gradient 573
formation kinetics 563
proton pump 536, 537
proton translocation 184, 185, 529, 530, 544,
560, 570
protonic circuits 567
protonmotive force 180, 184, 185
PS I (see photosystem I)
PS II (see photosystem II)
PS II 37, 49, 304, 308, 433
PS ll
37, 49, 308
psbA gene for D l (Q ) protein 385, 463
psbD gene for D2 protein 463
Pseudoanabaena 264
puddle model 312
pyrenoids 11-13
a
ß
B
Qpool 218,541
Q-cycle 1 7 4 - 1 7 6 , 5 3 4 - 5 3 7 , 5 4 2
Q
432
2
Q400
432
Q
A
228,424,425,427
Q
B
379,433,457-462,471
Qß-protein
162-165, 468-474, 596,
597
herbicides 460
mutations 462, 465
turnover 461, 468-474
Qc 541
QL
431
quantum efficiency 162
quantum yield 338
quinol-cytochrome c oxidoreductases 208, 496
quinone (see also plastoquinone) 121, 122,
540, 541
quinone binding 2 0 9 , 2 3 1 , 3 8 2 , 6 2 5
quinone radical 471
quinone-iron complex 358
Q
Z
541
radical formation 595
radical pair 339, 341
RC-H polypeptide 636
RC-L, organization of structural gene 633
R C - M , organization of structural gene 633
Subject Index
reaction center, biochemistry 127
cytochrome c 220
four types 371
general reaction scheme 205
lake model 313
electron transfer events 144,161
generated membrane potential 203, 206
organization 85
to phycobilisome ratio 56-58, 267
topography 124, 125
reactions centers of bacteria 107, 205, 218,
354, 357, 371-380, 382, 621
of green bacteria 371, 394,
reaction center I complex 488, 489
reaction center I composition 152, 487-494
reaction center I organization 168-170,
476-485
reaction center II composition 152, 457-466
reaction center II, charge separation 162,
422-434
manganese depletion 35, 167
reaction center-bCi complex cycle 211
reaction center-phycobilisome coupling 56-58,
267
reconstitution of membrane complexes 38, 39,
613, 672, 675-681, 722
redox center orientation in bacterial membranes 346-348, 351
redox centers in reaction centers of bacteria
344
redox chain control 561
redox potentials, theory and conventions 204
reducing equivalents 219
reducing power sources 212
relocalization 286
repair of photodamage 474
repetitive streak cameras 333
resonance energy transfer 92
respiration in mitochondria 496
reverse electron flow 164, 530
Rhodeila 26
Rhodophyceae 6
Rhodophyta 143,270,281,282,284
Rhodopseudomonas 118, 119, 121, 123, 125,
197-232, 246, 254, 256, 313, 344, 355, 371381, 383-389, 497, 539, 545, 604, 605, 610-618
Rhodospirillum 99, 125, 219, 246, 253, 313,
471, 610-618
ribulose bisphosphate carboxylase 11
Rieske FeS center 173, 174, 498, 499
Rieske FeS protein 127, 500-502, 540, 649
gene 503
structure 504-605
rise time of fluorescence 306, 334
rod elements of chlorosomes 610, 618
rotary shadowed replicas 666
R Y D M R 364-367
801
S-states 166-168, 437
SAN-9785 24
Sargassum 60
Scenedesmus 685, 689
secondary electron transfer 355
secondary quinone acceptor 354
semi-aerobic induction 609
sensitizers 331
sequence homology 248
signal II 165,166,170,428
single site catalysis 589
single turnover resolution 564
single-photon timing 299, 333
siphonaxanthin-chl a/b proteins 275
siphonoxanthin 271, 272
slow component lifetimes 302
slow electrogenic phase 528-529
sodium dodecyl sulfate 104, 129
space charge density 654
special pair 360
Spermothamnion 26, 53
spillover 303
spin axes 402, 406
spin polarization 483
spin-probes 724
spinach 59, 153, 173, 183
spirilloxanthin 125
Spirodela 684
staining, tetramethylbenzidine 641
State I-State II transitions 64-66, 115, 657,
658
steady-state coupling 560-561
Stern layer 654
stress 472, 473
stroma 10-14, 665
membranes 20-24, 147, 305
strong coupling 292, 333
structure analysis, x-ray 328, 372
structure, bacterial reaction center 345
cyt b/Ci complex 345
primary 240, 242, 328, 348
secondary 346, 351
three dimensional of proteins 240, 244
topographical 504
subchloroplast fractions 696
surface charge of thylakoids 154-158,
653-664, 698, 700
sulfide, electron transport to reaction center
215, 216
sulfide oxidation 217
sulfolipids (see diacylsulfoquinovosylglycerol)
sulfur compounds, reduced 215
transport 220
sulfur-oxidizing enzymes 218
sulphoquinovosyldiacylglycerol (see diacylsulfoquinovosylglycerol)
sunlight 86
802
Subject Index
superexchanges 358
supramolecular organization of thylakoids
1-7, 603-618, 675-681
model 49
surface potential 653
Synechococcus 17
Synechocystis 263
systematic organization of algae 5
T A D M R 401,410
temperature dependence of fluorescence 307
temperature-induced changes in membranes
66-70
terminal polypeptide antibodies 265
tertiary electron transfer 355
tetranitromethane 551
tetraphenyl boron 431
Thiocapsa 122
thioether bonds 327
thioredoxin 186, 590
thiosulfate oxidation 217
thylakoid, architecture 1-72, 513-516,
603-618, 665-673
arrangement in chloroplasts 6, 14-30
fragments 299, 305, 306
frets 515
freeze-fractured 1-72, 603-618, 665-673
freshly prepared 573
frozen and thawed 573
lipids 683-691, 693-704, 706-711, 713-724
location of cyt b / f 40
marginal regions 152, 722
nomenclature 2, 22-23
of chromophytan algae 28-30
of Chrysophyceae 29
of cryptomonads 28
of cyanelles 53-58
of cyanobacteria 53-58
of diatoms 28-29
of dinoflagellates 29-30
of euglenoids 25
of green algae 25
of oxygen-evolving prokaryotes 16-19
of Prochloron 51-52
of red algae 53-58
of Xanthophyceae 29
supramolecular organization 30-61,
603-618, 665-673
protein density 516-518
thylakoids, brown algae 28-29
endogenous buffering capacity 563
girdle 26
grana development 20-22
grana three dimensional organization 19-22,
146-149
stacking, light intensity 23
stroma development 20-22
stroma three dimensional organization
19-20, 63
surface, inner 451
tightly-bound nucleotides 589-592
time-resolved spectrum 305
tobacco 3
Tolypothrix 263
topology of antenna pigments 317
topology of membranes 281, 620-630
transient coupling 563-564
transient states 338, 342
transmembrane electrochemical potential 145,
170, 176, 180, 181, 184, 187
transport, M g control 229
trapping of excitation energy 286, 293
triazines 164, 165, 595
triplet states 292, 293, 310, 340, 356, 363, 395,
400-421, 482
triplet-minus-singlet absorbance difference
402, 409-412
triplet-minus-singlet spectra 417-418
Tris, alkaline release of proteins 448
Triton X-100 106, 129
tunneling of electrons 95
turnover of Q protein 471, 472
two electron gate 163, 174
++
B
ubiquinone 119, 178, 372
unstacking in vitro 61-63, 149, 660, 616
urea 595
6
van der Waals attractive forces 657
variable fluorescence yield 306
vesicles, inside-out 305, 448
right-side-out 448
violaxanthin-chl a/cl/c2-protein 277
violaxanthin-chl a/chl cl/c2 complex 278
violaxanlhin-chlorophyll a/cl +c2-complex
116
vitamin C 601
water oxidation site 453
water stres effects on photoinhibition 468
water-splitting enzymes 37, 447-455
X-ray analysis of proteins
X
432
330, 357, 371, 624
a
Z 428,429
Z
165,429,440
Z-scheme 144, 145
Zea 23
zero field splitting parameters 403, 404
zeta-potential 655
+