New comprehensive biochemistry vol 15 photosynthesis

PHOTOSYNTHESIS New Comprehensive Biochemistry Volume 15 General Editors A NEUBERGER London L.L.M van DEENEN Utrecht ELSEVIER AMSTERDAM * NEW YORK * OXFORD Photosynthesis Editor J AMESZ Leiden 1987 ELSEVIER AMSTERDAM NEW YORK * * OXFORD 01987, Elsevier Science Publishers B.V (Biomedical Division) All rights reserved No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher, Elsevier Science Publishers B.V (Biomedical Division), P.O Box 1527, lo00 BM Amsterdam, The Netherlands Special regulations for readers in the USA: This publication has been registered with the Copyright Clearance Center Inc (CCC), Salem, Massachusetts Information can be obtained from the CCC about conditions under which the photocopying of parts of this publication may be made in the USA All other copyright questions, including photocopying outside the USA, should be referred to the publisher ISBN 0-444-80864-7 (volume) ISBN 0-444-80303-3 (series) Published by: Elsevier Science Publishers B V (Biomedical Division) P.O Box 211 lo00 AE Amsterdam The Netherlands Sole distributors for the USA and Canada: Elsevier Science Publishing Company, Inc 52 Vanderbilt Avenue New York, NY 10017 USA Library of Congress Cataloging-in-PublicationData Main entry under title: Photosynthesis (New comprehensive biochemistry ; v 15) Includes bibliographical references and index Photosynthesis I Amesz, Jan 11 Series QD415.N48 VOI.15 574.19'2 s f581.1'33421 87-9229 [QK882] ISBN 0-444-80864-7 Printed in The Netherlands Introduction In the early 17th century Van Helmont (1577-1644) performed one of the first modern experiments in plant physiology He planted a willow branch in a tub of soil and watered it regularly until it had developed into a reasonably large tree After years Van Helmont terminated the experiment and found that the tree had accumulated a considerable amount of dry material (164 pounds to be precise) whereas the weight of the soil had decreased by only a few ounces during the same period From this he concluded that plants not feed on soil, as postulated by the then prevailing theory, but on the only substance supplied to the tree: water Van Helmont’s experiment was probably the first to show that plants have a special form of metabolism that distinguishes them from animals, but it took approximately one and a half centuries before the discoveries of Priestley , Ingen-Housz and others established the existence of the process we now call photosynthesis Although the importance of this process was immediately realized (the reader should consult Rabinowitch’s monograph* for a vivid description of the early years of photosynthesis research), it took another 150 years before some insight into the molecular mechanisms of photosynthesis began to evolve The post-war years, which showed such a rapid development of biochemical and physical techniques, also witnessed an unprecedented expansion of photosynthesis research, based on the application of these very techniques Due to the work of Calvin, Benson and associates in the forties and fifties it became clear that carbon dioxide fixation, once supposed to be the basic photosynthetic reaction, occurs by an intricate sequence of enzymatic processes that can in principle function in the dark if fueled by the products of photosynthesis Duysens’ studies established the role of pigments in harvesting and transferring the energy of light, and gradually it became clear that the primary energy conversion steps consist of electron transfer reactions that take place in an entity called the reaction center Around 1960 the basic difference between plant and bacterial photosynthesis became known: bacteria have only one type of reaction center, whereas plants have two, one of which produces a strong oxidant able to oxidize water to oxygen During the last five or ten years many important developments have taken place in photosynthesis research The combined efforts of biochemists and (bio)physicists have now provided a picture of the mechanisms of the photosynthetic reactions and of the structure of the various components of the photosynthetic membrane which is vastly more detailed than might have been envisaged a few years ago The application of advanced optical instrumentation, both in the visible region (e.g by laser spectroscopy) and by use of electron spin resonance, has provided a wealth of information concerning the primary reactions of photosynthesis and the inter* E.I Rabinowitch, Photosynthesis and Related Processes, Vol I Interscience Publishers, New York, 1945, 599 pp VI actions between the primary reactants On the other hand, the work of protein chemists and molecular biologists and the recent X-ray analysis of the bacterial reaction center together with optical measurements have given increasingly detailed information on the structure and organization of the protein complexes which are embedded in the photosynthetic membrane and are involved in energy conversion and electron transport Also the mechanism of oxygen evolution and the role of manganese in this reaction, for a long time a ‘black box’ in the gradually emerging picture of the electron transfer scheme, are now beginning to reveal their secrets Although these recent developments have not basically altered our concepts of the mechanism of photosynthesis, they have certainly clarified the picture to a considerable extent, and altogether they signify an important leap forward to a better understanding of the intricacies of the molecular processes of photosynthesis Many points that used to be blurred have now come into focus, and many questions can now be asked with more precision and are now amenable to further experimentation It is hoped that this book conveys some of the excitement of the recent discoveries The first two chapters give’an introduction to photosynthesis in plants and bacteria, while the other chapters give a discussion of more specialized topics in the areas of primary charge separation, electron transport, the secondary products of photosynthesis, structure and genetics of protein complexes, and, finally, evolution Together they should present a comprehensive overview of the current state of knowledge of the molecular processes of photosynthesis, which have fascinated so many investigators of various disciplines and scientific backgrounds during the last decades In a book written by specialists in the various areas of photosynthesis research, there are bound to be some overlaps and some gaps One area that may not have been adequately covered, althovgh its impact can be discerned in various chapters, is the wealth of information regarding energy and electron transfer and structure derived from studies of prompt and delayed fluorescence of chlorophyll and bacteriochlorophyll However, the reader interested in this area should find enough information in this book for further literature on the subject At this point the editor wishes to express his thanks to the authors of this volume, both for their willingness to write a chapter and for the quality of their contributions Due to their efforts to keep to the projected time scheme, this book can be published with minimal delay, and give an up-to-date account of research into the molecular aspects of the most fundamental life process on earth J Amesz Department of Biophysics Huygens Laboratory University of Leiden The Netherlands Contents Introduction, by J Amesz V Non-standard abbreviations used in this volume XV Chapter Energy conversion in higher plants and algae, by G Forti 1 Introduction Electron transport from water to NADP: an overview Photosynthetic phosphorylation Molecular and supramolecular structure of thylakoids 4.1 Lateral heterogeneity, fluorescence and electron transport 4.2 Excitation energy distribution between the photosystems References 11 Chapter Photosynthetic bacteria, by B K Pierson and J M Olson 21 2.1, General characteristics Green sulfur bacteria 3.1 General characteristics 21 23 23 24 26 26 Introduction Heliobacteriurn chlorurn - the gram-positive line 4.1 General characteristics 4.2 Light-harvesting, reaction center and electron transport Purple bacteria I General characteristics 5.2 Light-harvesting, reacti ctron transport Bacteriochlorophyll a-containing non-phototrophic bacteria Phylogeny Halobacteria 28 29 29 32 34 35 31 38 39 Chapter The bacterial reaction center, by W.W Parson 43 Introduction 43 VIII Purification and crystallization of reaction centers Protein structure BChl, BPh and other prosthetic groups Spectroscopic properties and the distinction between BPhL and BPh, Electron transfer kinetics and mechanisms Acknowledgements References 46 47 51 53 55 57 51 Chapter The primary reactions of photosystems I and I1 of algae and higher plants by P Mathis and A W Rutherford 63 Introduction Photosystem 2.1 The primary donor P-700 2.1.1 Basic properties of P-700 2.1.2 P-700: a chlorophyll species 2.1.3 P-700: probaby a dimer of chlorophyll 2.2 Sequence of electron acceptors 2.2.1 Terminal acceptors 2.2.2 Centre X, an intermediate ac 2.2.3 Primary acceptors: Ao, A, 2.2.4 Overview of primary reaction 2.3 Electron donation to P-700 2.4 Structure of the PS I reaction centre 2.4.1 Polypeptides and redox centres 2.4.2 Photosystem I light-harvesting antenna 2.4.3 Organization of the reaction centre in the membrane Photosystem I1 reactions 3.1 Introduction 3.2 PS I1 photochemistry 3.3 The electron acceptor s 3.3.1 The quinone-iron 3.3.2 Pheophytin - the intermediate electron acceptor 3.3.3 Other possible acceptors and heterogeneity 3.4 The electron donor side of PS I1 3.4.1 P-680, the primary donor 3.4.2 Z, the electron donor to P-680+ 3.4.3 D, the component associated with Signal I1 slow 3.4.4 Other electron donors in PS I1 3.5 Photochemical electron transfer in PS I1 - an overview 3.6 Structural aspects References 63 64 65 65 65 66 67 67 69 70 72 72 73 73 74 15 75 75 76 76 76 81 82 84 84 85 86 87 88 89 91 Chapter Electron paramagnetic resonance in photosynthesis by A J Hoff 97 Introduction Magnetic resonance for the layman 97 97 - IX Physics of EPR 3.1 Basic principles 3.2 The EPR spectrum 3.3 Electron nuclear double resonance, ENDOR EPR of primary reactants in photosynthesis 4.1 The primary electron donor 4.1.1 Bacterial photosynthesis 4.1.2 Photosystem I 4.1.3 Photosystem I1 4.2 The primary acceptor 4.2.1 Purple bacteria 4.2.2 Green bacteria 4.2.3 Photosystem I 4.2.4 Photosystem I1 4.3 The intermediary acceptor 4.3.1 Bacterial photosynthesis 4.3.2 Photosystem I 4.3.3 Photosystem I1 The triplet state The oxygen-evolving complex 6.1 Manganese 6.2 Signal I1 Electron spin polarization New techniques: ESE and R Conclusions and prospects Acknowledgements References Chapter The photosynthetic oxygen-evolving process b y G.T Babcock Introduction Oxygen evolution - the minimal unit 2.1 Polypeptide composition and function in the PS II/OEC 2.1.1 Intrinsic polypeptides 2.1.2 Extrinsic polypeptides 2.2 Electron transfer components 2.2.1 P-680 and Z 2.2.2 Manganese 2.3 Cofactor requirements Electron transfer in the oxygen-evolving unit 3.1, Electron transfer in the untreated PS IIiOEC 3.2 Electron transfer in the PS IIlOEC following inhibition Water oxidation in the oxygen-evolving unit 4.1 Substrate and substrate analogue binding 4.2 The occurrence of water chemistry 4.3 Representative models of oxygen evolution Conclusions Acknowledgements References 99 99 102 105 106 107 107 108 108 109 109 110 110 111 111 111 112 113 113 115 115 115 116 117 119 119 120 125 125 126 129 129 131 132 132 134 138 139 139 143 146 147 148 149 151 152 152 342 123 Mathis, P , Sauer, K and Remy, R (1978) FEBS Lett 88, 2575-2578 124 Anderson, J.M (1980) Biochim Biophys Acta 591, 113-126 125 Vierling, E and Alberte, R.S (1983) Plant Physiol 72, 625-633 126 Anderson, J M., Brown, J.S., Lam, E and Malkin, R (1983) Photochem Photobiol 38,205210 127 Lagoutte, B., Setif, P and Duranton, J (1984) FEBS Lett 174, 24-29 128 Bengis, C and Nelson, N (1977) J Biol Chem 252, 4564-4569 129 Evans, P.K and Anderson, J.M (1986) FEBS Lett 199,227-233 130 Fish, L.E., Kuck, U and Bogorad, L (1985) J Biol Chem 260, 1413-1421 131 Westhoff, P., Alt, J., Nelson, N., Bottomley, W., Bunemann, H and Herrmann, R.G (1983) Plant Mol Biol 2, 95-107 132 Smith, A.G and Gray, J.C (1984) Mol Gen Genet 194, 471-476 133 Nechushtai, R and Nelson, N (1985) Plant Mol Biol 4, 377-384 134 Vierling, E and Alberte, R.S (1983) J Cell Biol 97, 1806-1814 135 Mullet, J.E., Burke, J.J and Arntzen, C.J (1980) Plant Physiol 65, 823-827 136 Mullet, J.E., Grossman, A.R and Chua, N.-H (1981) Cold Spring Harbor Symp Quant Biol 46, 979-984 137 Zielinski, R.E and Price, C.A (1980) J Cell Biol 85, 435445 138 Smith, A.G and Gray, J.C (1984) in Advances in Photosynthesis Research, Vol (Sybesma, C., ed.) pp 513-516, Martinus NijhoWDr W Junk, The Hague 139 Obokata, J (1986) Plant Physiol 81, 7805-7807 140 Pick, U and Racker, E (1979) J Biol Chem 254, 2793-2799 141 Moase, E.H and Green, B.R (1981) Eur J Biochem 119, 145-150 142 Westhoff, P., Nelson, N., Bunemann, H and Herrmann, R.G (1981) Curr Genet 4, 109-120 143 Walker, J.E and Tybulewicz, V.L.J (1986) in Molecular Biology of the Photosynthetic Apparatus (Arntzen, C.J., Bogorad, L., Bonitz, S and Steinback, K., eds.) pp 141-153, Cold Spring Harbor, New York 144 Sebald, W and Hoppe, J (1981) Curr Top Bioenerg 12, 1-64 145 Suss, K.-H (1980) FEBS Lett 112, 255-259 146 Westhoff, P., Alt, J., Nelson, N and Herrmann, R.G (1985) Mol Gen Genet 199,290-299 147 Cozens, A.L., Walker, J.E., Phillipps, A.L., Huttly, A.K and Gray, J.C (1986) EMBO, J 5, 217-222 148 Bud, C.R., Koller, B., Auffret, A.D., Huttly, A.K., Howe, C.J., Dyer, T.A and Gray, J.C (1985) EMBO J 4, 1381-1388 149 Howe, C.J., Auffret, A.D., Doherty, A., Bowman, C.M., Dyer, T.A and Gray, J.C (1982) Proc Natl Acad Sci USA 79, 6903-6907 150 Krebbers, E.T., Larrinua, I.M., MacIntosh, L and Bogorad, L (1982) Nucleic Acids Res 10, 498.5-5002 151 Zurawski, G., Bottomley, W and Whitfeld, P.R (1982) Proc Natl Acad Sci USA 79,6260-6264 152 Shinozaki, K., Deno, H., Kato, A and Sugiura, M (1983) Gene 24, 147-155 153 Zurawski, G and Clegg, M (1984) Nucleic Acids Res 12,2549-2559 154 Howe, C.J., Fearnley, I.M., Walker, J.E., Dyer, T.A and Gray, J.C (1985) Plant Mol Biol 4, 333-345 155 Zurawski, G., Bottomley, W and Whitfeld, P.R (1986) Nucleic Acids Res 14, 3974 156 Huttly, A.K and Gray, J.C (1984) Mol Gen Genet 194, 402-409 157 Deno, H., Shinozaki, K and Sugiura, M (1983) Nucleic Acids Res 11, 2185-2191 158 Hennig, J and Herrmann, R.G (1986) Mol Gen Genet 203, 117-128 159 Howe, C.J., Bowman, C.M., Dyer, T.A and Gray, J.C (1983) Mol Gen Genet 190, 51-55 160 A t , J., Winter, P., Sebald, W., Moser, J.G., Schedel, R., Westhoff, P and Herrmann, R.G (1983) Curr Genet 7, 129-138 161 Deno, H., Shinozaki, K and Sugiura, M (1984) Gene 32, 195-201 162 Shinozaki, K., Deno, H., Wakasagi, T and Sugiura, M (1986) Curr Genet 10, 421-423 163 Bouthyette, P.-Y and Jagendorf, A (1978) Plant Cell Physiol 19, 1169-1174 164 Mendiola-Morgenthaler, L.R., Morgenthaler, J.J and Price, C.A (1976) FEBS Lett 62, 96-100 165 Doherty, A and Gray, J.C (1980) Eur J Biochem 108, 131-136 166 Nelson, N., Nelson, H and Schatz, G (1980) Proc Natl Acad Sci USA 77, 1361-1364 167 Biekmann, S and Feierabend, J (1985) Eur J Biochem 152, 529-535 I Amesz (ed.) Photosynthesis 01987 Elsevier Science Publishers B V (Biomedical Division) 343 CHAPTER 15 Evolution of photosynthesis H.J VAN GORKOM Department of Biophysics, Huygens Laboratory of the State University, P Box 9504, 2300 RA Leiden, The Netherlands Introduction Like all complicated biological structures, the photosynthetic apparatus may be expected to bear traces of its history, which may range in importance from the fundamental design of the whole thing to a now meaningless scar that has not had enough time yet to heal A full understanding of the structure and function of the photosynthetic apparatus requires that these traces are recognized as such Although in most, if not all, cases only tentative answers can be expected, evolutionary considerations often answer otherwise enigmatic questions in a very satisfactory and illuminating way On the other hand, to distinguish fact and fiction in evolution theory is not a trivial problem To illustrate the point: now 12 years of intensive research have passed since E Broda in his monograph on ‘the evolution of the bioenergetic processes’ [ 11 accumulated over two thousand references, most of them relevant to the subject of this chapter The average specialist in one of the many fields of photosynthesis research is at best superficially acquainted with the relevant literature and will usually not resort to speculations on evolution except as an afterthought, to polish the last paragraph of his research paper, instead of using them as a source of inspiration for new experiments Written by such a specialist, the present chapter does no justice to the rich literature on the evolution of photosynthesis Its primary purpose is to illustrate the significance of evolutionary concepts in understanding the photosynthetic machinery as it operates today The origin of chloroplasts Although hardly relevant to the evolution of photosynthesis as such, the evolutionary origin of the chloroplast will be discussed first, because it provides a striking example of an evolutionary concept that explains a large number of observations which otherwise seem to make no sense at all Globally speaking, photosynthesis takes place in the chloroplast and respiration takes place in the mitochondrion Both chloroplasts and mitochondria are organelles of eukaryotic cells They look in many respects like cells within the cell and 344 it is now generally accepted that these organelles are descendants of once free-living eubacteria Comprehensive accounts of this theory may be found in Refs and The protozoa are thought to originate from some ‘protoeukaryote’ (perhaps similar to the anaerobic amoeba Pelomyxa palustris [2]) which acquired an efficient energy metabolism by the uptake and tolerance in its cytoplasm of some aerobic respiring eubacterium and the subsequent establisment of a stable symbiotic association with this bacterium by synchronization of their reproductive cycles It appears that all mitochondria may be descendants of the same endosymbiont, related phylogenetically to Agrobacteriurn turnefuciens [4].Later, and probably continuing to this day, various symbiotic associations between protozoa and eubacteria with oxygenic photosynthesis were established, some of which led to the different groups of algae now in existence Some features of the chloroplasts of Cryptomonads even suggest that these are derived from a eukaryotic endosymbiont, most likely a red alga: endosymbiosis and integration as an organelle took place twice in succession in this case [ ] The red algae have chloroplasts which may be derived from cyanobacteria, since they contain similar antenna pigmentprotein complexes; all phycobiliproteins are closely related [6] One oxygen-evolving prokaryote with Chl b as an accessory pigment is known (Prochloron), but shows no special affinity to the chloroplasts of green algae [7] No Chl c-containing prokaryotes have been described Presumably a wider variety, especially with regard to antenna pigments, of prokaryotic oxygen-evolving organisms existed before the eukaryotes took their place as the main primary producers in the biosphere Chloroplasts and mitochondria have their own enclosing membrane, and the lack of protoplasmic continuity between the chloroplast stroma or mitochondrial matrix and the cytosol of the eukaryote almost defines these organelles as separate cells They have their own DNA, RNA and protein synthesis machinery and in all these fundamental cellular properties they resemble the eubacteria much more than the eukaryote host cell Many chloroplast proteins which must have been endogenous to the endosymbiont, because homologous proteins are found in Cyanobacteria, are now encoded by nuclear genes and synthesized in the cytoplasm [8] The genetic integration of the mitochondria is even more extensive Perhaps chloroplasts are in the process of losing all their genetic material to the nucleus, but some genes may be much more resistant to the process than others As a general rule, the intrinsic thylakoid proteins are synthesized in the chloroplast The transport across the chloroplast envelope and subsequent insertion in the thylakoid membrane requires a complex processing machinery and, although it does exist for LHC 11, the main light-harvesting Chl alb protein [9], one can imagine that such a system takes time to evolve In view of the endosymbiotic theory no further explanation is needed for the detailed similarity between mitochondrial respiration and that of some eubacteria, nor for the striking resemblance of chloroplast photosynthesis to that of cyanobacteria 345 The origin of photosynthesis How old is photosynthesis? The present atmospheric oxygen level is determined by the balance between photosynthesis and respiration Geochemical evidence indicates that a stable aerobic environment was established some 1700 million years ago Most likely, this marked the ultimate saturation of a vast supply of oxygen sinks (banded iron formations) after a long period of increasing photosynthetic oxygen evolution, starting more than 2500 million years ago [lo] The widespread occurence of photosynthetic bacteria as early as 3500 million years ago is strongly indicated by fossil evidence (stromatolites) [ll].Since the oldest sediments known are not much older (3800 million years) and highly modified by geochemical processes [12], there is little hope of obtaining hard evidence on the origins of photosynthesis other than that preserved in the genomes of extant organisms The photosynthesizing organisms all belong to the eubacteria, if we consider chloroplasts as eubacteria and disregard the light-dependent proton pump of the Halobacteria (which is totally unrelated to what is normally called ‘photosynthesis’ (Ref 13; and Chapter 2) The different types of photosystem known today belong t o different eubacterial ‘phyla’ which are too distantly related to determine their relative phylogenetic positions by the current methods [141 Thus, bacterial phylogeny does not yet help to decide which type of photosystem may be most similar to the ancestral type and does not even support the general assumption that all photosystems are derived from the same ancestral type On the basis of this assumption it now seems likely that the common ancestor of all eubacteria already had a well-developed photosynthetic apparatus On the other hand, to postulate that photosynthesis is as old as life itself [13] may be taking the point a little bit too far, in view of the absence of photosynthetic eukaryotes without chloroplasts and of photosynthetic archaebacteria It seems simpler to assume that these organisms have not lost photosynthesis but are true relics of pre-photosynthetic ‘progenotes’ , which by some specialization managed to survive the appearance of photosynthetic cells: the surviving archaebacteria may stem from progenotes which escaped in some dark corner; the specialization of the ‘urkaryote’ [15] may have been that by that time it had already begun to feed on other cells or their remains In this picture, photosynthesis was invented by one of the progenotes, which thereby became the ancestor of a successful and rapidly expanding family: the eubacteria At present neither fossil evidence nor the phylogeny of extant bacteria can tell what the ancestral photosystem looked like and what properties predisposed its possessor among the progenotes to the acquisition of photosynthesis Another approach t o these questions is to search the photosynthetic apparatus itself for possible traces of its history Reaction center structure Of one purple bacterium, Rhodopseudornonas viridis, the structure of the reaction 346 Fe CYTOPLASM Menaquinone MEMBRANE BPheo L I) _ - _ _ _ PERIPLASMIC SPACE r- special pair of BChl (PI BChl ‘ Fig Arrangement of the pigments in the reaction center of Rhodopseudornonas viridis, based on the crystallographic data in Ref 16 Upon excitation an electron is transferred from the special pair P to the menaquinone QA (From Ref 18) center has been resolved by X-ray crystallography [16,17] Fig shows the arrangement of the six porphyrins and the permanently bound quinone QA in this reaction center The most striking feature is its almost perfect two-fold rotational symmetry, which is not limited to the arrangement of the chromophores shown in Fig 1, but applies to the apoproteins (L and M subunits) and the binding site for the exchangeable quinone QB relative to that of QA as well Such a symmetry is expected when identical, asymmetrical subunits form dimers Probably the present, structurally minor, differences between the two subunits reflect a specialization afterwards, and the formation of dimers had some advantage when the subunits were still identical One possible advantage might be in the dimeric structure of the primary electron donor, but even if this proves to be essential, it is not clear why a similar ‘special pair’ could not arise in a monomeric reaction center protein In fact the presence of two BChl molecules per subunit may perhaps indicate that a ‘special pair’ was already present when the subunits were still independent reaction centers A more obvious reason for the pairing of reaction centers may have been that the reaction center did not yet have a permanently bound quinone as a secondary electron acceptor The reaction center dimer could, upon excitation, transfer an electron to either side, thereby reducing the risk of wasting a charge separation by lack of an electron acceptor to stabilize it This hypothesis presupposes electronic coupling between the pigments acting as the primary electron donors in each of the two monomeric reaction centers and suggests that the present ‘special pair’ may be regarded as the ultimate result of a tendency to enhance this coupling 347 At some stage gene duplication occurred and differentiation of the two branches of electron transfer in the dimeric reaction center could begin The most obvious change is that on one side the quinone binding site has become permanently occupied by a quinone molecule, QA, which upon reduction is not replaced, but in turn reduces the quinone at the other binding site; QB, when present Thus, the differentiation of the two reaction center subunits, just like their association, was probably selected primarily because it reduced the risk of losing a charge separation by lack of a bound quinone to stabilize it Given the permanent presence of a bound quinone at one branch, it makes sense that the intermediary porphyrins in the other branch have lost their electron transport function Their continued presence, apparently without gross conformational changes, may merely indicate a structural role It may not have been worth while to replace them by a modified protein structure, or such a modification may require an improbably large number of simultaneous mutations in order to maintain activity It should be mentioned that electron transfer to the quinone pool, both by PS I1 and by the reaction centers of purple bacteria, now proceeds via a two-electron gating mechanism: after one electron has arrived at the temporarily bound quinone QB, the semiquinone remains in its unprotonated, negatively charged form and tightly bound to the reaction center; only after a second photoreaction does its full reduction, protonation and release as a quinol take place [19] This procedure may also have played a role in the selection of the dimeric reaction center structure, but its importance most likely has to with the reactivity of semiquinones with molecular oxygen and in that case it probably appeared much later Like QA,other stabilizing secondary electron donors and acceptors in reaction centers may have originated as substrate molecules which have become permanently bound The ferredoxin-reducing reaction centers of green sulfur bacteria and of PS I have iron-sulfur centers as secondary electron acceptors With the exception of PS 11, all reaction centers seem to oxidize a Cyt c and in those that have a permanently bound secondary electron donor, this donor is a c-type cytochrome It seems reasonable to assume that the reaction centers acquired their secondary, stabilizing redox components by increasing the affinity of their binding site for the - mobile - substrate (quinone, ferredoxin or Cyt c) and by development of electron transfer between the bound substrate molecule and its mobile colleagues It should be mentioned that such an electron transfer would automatically become thermodynamically favored it the reaction center succeeded in increasing its affinity for the substrate more than for the product (reduced quinone or ferredoxin, or oxidized Cyt c), since the midpoint potential of the bound form would thereby be shifted relative to that of the free form If this hypothesis is correct, some interesting inferences may be made: no ironsulfur centers have been found in the quinone-reducing systems (PS I1 and the reaction centers of purple bacteria), but there is evidence for the presence of a lowpotential quinone in PS I [20] and in Hefiobacterium chforum [21], and no evidence against its presence in green sulfur bacteria This suggests that ferredoxinreducing systems evolved from quinone-reducing systems, in line with the general view in the evolution literature that linear photosynthetic electron transport came later than photosynthetic energy conversion by cyclic electron flow, which is based on the assumption that a shortage of energy preceded a shortage of reduced carbon compounds A minimal model The simplest cyclic photosystem might require a polypeptide spanning the cytoplasmic membrane, carrying two different chlorophyll-like chromophores (perhaps a special pair plus an electron acceptor) arranged in such a way that excitation would result in electron transfer towards the cytoplasmic side, and the presence of lipophilic quinones, probably menaquinone, in the membrane Quinones are quite unreactive in aprotic media [ 2 ] , and in the absence of specialized binding sites would be expected to react only near the cytoplasmic or near the outside surface of the membrane, where protonation and deprotonation reactions could stabilize the product The directionality of the charge separation must be postulated to ensure that, if an electron transfer to quinone took place, it would be followed by proton uptake from the cytoplasm The positive charge left behind on the pigments should be localized preferentially near the outside surface, where it could lead to quinol oxidation upon proton release towards the outside This reaction sequence is the most likely one, in view of the electrochemical properties of quinones: the oxidation of quinol is normally energetically feasible only after dissociation of a proton and is therefore relatively slow [22] The quantum yield of the light-driven proton pump thus obtained would be dependent largely on the probability that a quinone molecule happened to be in the right position to accept an electron at the moment a photon was absorbed, and subsequent developments to enhance that probability are precisely what the present reaction center structure seems to show A possible objection against the above model is that no contemporary photosystem oxidizes the mobile quinol in the membrane, but in PS I1 two quinol molecules seem to be hound close to the reaction center chlorophyll, P-680, and one of those acts as the secondary electron donor Z [23,24] In this case no deprotonation is observed upon oxidation, but that may be regarded as a specialization of the reaction center protein which took place much later, when the need to oxidize very high-potential exogenous electron donors arose At an earlier stage, the ‘prePS 11’ reaction center most likely had some other reason to bind and oxidize quinol and a cyclic electron transport via the quinone pool, pumping protons out of the cell, seems the most simple explanation With the advent of the Cyt blc complex and the Q-cycle [25], quinol oxidation directly by the reaction center became energetically wasteful and therefore selected against Since it was too slow to contribute to the stabilization of the charge separation, it could disappear without trace The history of the Cyt bic complex itself may be closely related to that of the reaction centers The occurrence of such a complex in photosynthetic and respiratory electron transport chains of chloroplasts, mitochondria and eubacteria sug- 349 gests that all these chains have a common evolutionary origin It appears that the Cyt b of chloroplasts and that of mitochondria show considerable homology [26], in spite of their phylogenetic distance The bound Cyt c and the Rieske Fe-S protein from chloroplasts and those from mitochondria show little homology, but these proteins may have had more freedom and more reason to change; they are largely external to the chloroplast stroma and to the mitochondrial matrix, they have a covalently bound prosthetic group and only one, nearly terminal membrane-spanning sequence, and they are presumably inserted in to the membrane from opposite sides in the two types of organelle (the mitochondrial proteins are synthesized in the cytoplasm) [27] The Cyt b, on the other hand, is endogenous in both organelles, is highly intrinsic and spans the membrane five times [26], just like the L and M subunits of the Rhodopseudomonas viridis reaction center The cytochrome complex has its two Cyt b hemes arranged in such a way as to facilitate electron transfer across the membrane [26], it oxidizes quinol with concomitant proton release on the outside, and it can reduce quinone with concomitant proton uptake from the cytoplasm These properties suggest an evolutionary relationship to the primitive reaction center postulated above Photosynthesis By the simple reaction center-quinone cycle described above a photochemical proton pump would be obtained, initially with little requirement for specificity of the polypeptide involved and without any further proteins or redox components Its components might be of abiotic origin, accumulated in the membrane due to their hydrophobicity The selective advantage of the proton pump, e.g in the uptake of amino acids, would be clear even for the first membrane-enclosed ‘cell’ Only a proton-gradient-driven ATP synthase would be needed to establish a photosynthetic energy metabolism Proton-translocating ATPases are ubiquitous and probably date back to the progenotes [28], and the same applies to cytochromes and iron-sulfur proteins, important building blocks of contemporary photosynthetic electron transport Olson and Pierson [13], emphasizing the possible simplicity of ancestral photosynthesis and the possible abiotic origin of its components, argue that fermentative energy metabolism is in fact much more complicated and unlikely to have preceded photosynthesis as an energy source for the first cells They note that the Embden-Meyerhof-Parnas pathway, shared by most fermentations, is absent in archaebacteria and requires a large number of highly specific enzymes If photosynthesis was invented by organisms with a fermentative energy metabolism, a more simple fermentation mechanism would indeed be expected While this consideration may argue against the idea that photosynthesis originated after the establishment of accessory oxidant-dependent fermentation as we know it now [29], it does not remove the necessity of assuming a central role of carbohydrate metabolism at the earliest stages of evolution [30], perhaps even earlier than the development of a membrane-enclosed cell as required for photophosphorylation Substrate-linked phosphorylations carried out by structures as simple 350 and as available as those required for the most primitive type of photosynthetic energy conversion may be hard to conceive, but, without equally demanding biosyntheses coupled to pyrophosphate bond hydrolysis, photophosphorylation serves no purpose References Broda, E (1975) The Evolution of the Bioenergetic Processes, Pergamon Press, New York Margulis, L (1981) Symbiosis in Cell Evolution, Freeman and Co., San Francisco Cavalier-Smith, T (1981) in Molecular and Cellular Aspects of Microbial Evolution (Carlisle, M.J., Collins, J.F and Moseley, B.E.B., eds.) pp 33-84, Cambridge University Press, Cambridge Yang, Y., Oyaizu, H., Olsen, G.J and Woese, C.R (1985) Proc Natl Acad Sci USA 82, 4443-4447 Gillott, M.A and Gibbs, S.P (1980) J Phycol 16, 558-568 Glazer, A.N (1984) Biochim Biophys Acta 768, 29-51 Lewin, R.A (1984) Phycologia 23, 203-208 Ellis, R.J (1981) Annu Rev Plant Physiol 32, 111-137 Schmidt, G.W., Bartlett, S.G., Grossman, A.R., Cashmore, A.R and Chua, N.-H (1981) J Cell Biol 91, 468-478 10 Walker, J.C.G., Klein, C., Schidlowsh, M., Schopf, J.W., Stevenson, D.J and Walter, M.R (1983) in Earth’s Earliest Biosphere; its Origin and Evolution (Schopf, J.W., ed.) pp 260-290, Princeton University Press, Princeton 11 Schopf, J.W and Walter, M.R (1983) ibid., pp 214-239 12 Hayes, J.M., Kaplan, I.R and Wedeking K.W (1983) ibid, pp 93-134 13 Olson, J.M and Pierson, B.K (1986) Int Rev Cytol., in press 14 Woese, C.R (1985) in Evolution of Prokaryotes (Schleifer, K.H and Stackebrandt, E., eds.) pp 1-30, Academic Press, London 15 Woese, C.R and Fox, G.E (1977) Proc Natl Acad Sci USA 74, 5088-5090 16 Deisenhofer, J., Epp, O., Miki, K., Huber, R and Michel, H (1984) J Mol Biol 180, 385-398 17 Deisenhofer, J., Epp O., Miki, K., Huber, R and Michel, H (1985) Nature (London) 318,618-624 18 Van Gorkom, H.J (1986) Bioelectrochem Bioenerg 16, 77-87 19 Crofts, A.R and Wraight, C.A (1983) Biochim Biophys Acta 726, 149-185 20 Rutherford, A.W and Heathcote, P (1985) Photosynth Res 6, 295-316 21 Brok, M., Vasmel, H., Horikx, J.T.G and Hoff, A.J (1986) FEBS Lett 194, 322-326 22 Rich, P.R (1981) Biochim Biophys Acta 637, 28-33 23 O’Malley, P.J and Babcock, G.T (1984) Biochim Biophys Acta 765, 370-379 24 Dekker, J.P., Van Gorkom, H.J., Brok, M and Ouwehand, L (1984) Biochim Biophys Acta 764, 301-309 25 Slater, E.C (1983) Trends Biochim Sci 8, 239-242 26 Widger, W.R., Cramer, W.A., Herrmann, R.G and Trebst, A (1984) Proc Natl Acad Sci USA 81, 674-678 27 Hauska, G (1985) in Molecular Biology of the Photosynthetic Apparatus, (Steinback, K.E., Bonitz, S., Arntzen, C.J and Bogorad, L., eds.) pp 79-87, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 28 Wilson, T.H and Lin, E.C.C (1980) J Supramol Struct 13, 421-446 29 Gest, H (1980) FEMS Microbiol Lett 7, 73-77 30 Quayle, J.R and Ferenci, T (1978) Microbiol Rev 42, 251-273 35 Subject index Adenylsulfate role in sulfide oxidation, 204 ADRY reagents, 142 Agmenellum quadruplicatum, 257, 314 Allophycocyanin, 249-261 Amaranthus 323 Amine binding to oxygen-evolving complex, 147, 148 effect on oxygen evolution, 145-148 Ammonia as uncoupler, 162 binding to oxygen-evolving complex, 147, 148 effect on oxygen evolution, 145-147 Amytal, 202 Ao, 7&72, 112 A,, 70, 72, 112, 113 Arabidopsis thaliana, 321 322 Aspartate transport, 180, 181 ATP in carbon dioxide assimilation, 176, 177, 182 184 in NAD‘ reduction, 201, 202 synthesis, see photophosporylation ATP synthase, 8, 33, 162, 167-169, 283 biosynthesis, 217 218, 324, 337 338 evolution of, 349, 350 genes for, 336, 337 in Chlorobium, 28 in purple bacteria, 33 polypeptides, 168, 169,216, 218, 335-338 reconstitution, 167-169 structure, 216-218, 324, 335, 336 ATP-P, exchange 162 ATPase, 162, 163 ATPIe; ratio photophosphorylation, 11, 160, 166 Atrazine binding, 323 Atriplex spongiosa, 180, 181 Bacteriochlorophyll distribution in photosynthetic bacteria, 36, 37 spectroscopic properties, 299-301 Bacteriochlorophyll a protein complex, 24, 32, 33, 237-247, 301-306, 308-311 structure, 23 Bacteriochlorophyll b protein complex, 237, 240 structure, 23 Bacteriochlorophyll c as primary electron acceptor, 27, 29, 46, 112 in chlorosomes, 24, 27, 245, 246 protein complex, 24, 27, 245, 246 structure, 23 Bacteriochlorophyll d structure, 23 Bacteriochlorophyll e structure, 23 Bacteriochlorophyll g in Heliobacterium chlorum 28, 29 structure, 38 Bacteriopheophytin as electron acceptor, 33, 4447, 54-56, 111, 112 EPR, 111, 112 Bacteriorhodopsin, 38 Bohr magneton, 100 Bundle sheath cells, 178-181, 192 Calvin-Benson cycle, see reductive pentose phosphate cycle Carbon dioxide assimilation, see reductive pentose phosphate cycle Carotenoid as electron donor, 87 distribution in photosynthetic bacteria, 37 in reaction center, 53 in light-harvesting complex, 238, 242, 243, 276, 294 in photosystem I, 219, 220 in photosystem 11, 223, 224, 263, 280 Ca” effect on oxygen evolution, 131, 138-139, 144146 CF,, see ATP synthase CF, , see ATP synthase Charge transfer, 56, 301, 310 Chlamydomonas, 222, 223, 320, 325 reinhardtii, 262, 287 Chlorella, 176, 183 Chloride binding to oxygen-evolvingcomplex, 145, 146 effect on oxygen evolution, 4, 130, 131, 138-139, 142, 144146 352 Chlorobium, 26-28 limicola, 110, 203, 206, 207 Chloroflexus aurantiacus, 23-26,45,48,52, 110, 200, 201, 203, 236, 240, 245, 246, 313, 314 Chlorophyll protein complex, 219, 220, 223-226, 261-266, 275-277, 306, 307 spectroscopic properties, 299-301 Chlorophyll a as electron acceptor, 70, 112 structure, synthesis, 222 Chlorophyll b structure, Chloroplast DNA, 215-218, 222, 226, 227, 323-336, 344 membrane carriers, 187, 188 origin, 343-345 ribosomes, 215 RNA, 226, 328, 333-335, 344 see also thylakoid Chlorosomes of Chloroflexus aurantiacus, 24, 24Y, 246 of green sulfur bacteria, 27 Chromatium vinosum, 33, 34, 43, 47, 56, 111, 202-208, 239, 244 Chroomonas, 250,259-261 CIDEP, 71 Circular dichroism, 300, 301,303-309, 311-315 Crassulacean acid metabolism, 180-183 regulation, 193-194 Cytochromes in green sulfur bacteria, 27 in purple bacteria, 33 of Chloroflexus aurantiacus, 25, 26 Cytochrome b-559, 4, 77, 87, 88, 90, 130, 133, 145, 285 biosynthesis, 255, 329 polypeptides, 280, 320, 326 Cytochrome b6, 5,226, 277-279,285 biosynthesis, 215, 216, 331-333 polypeptides, 277, 278, 324, 330-333 Cytochrome bc, complex Chloroflexus aurantiacus, 25 mitochondria, 204, 214 purple bacteria, 45, 204 Cytochrome b,-f complex biosynthesis, 215,216,226,285,324,329-332 evolution of, 348 function, 5, 6, 214 genes for, 330-331 polypeptides, 214, 215, 277, 278, 330-332 structure, 214, 215,277-279, 324, 329-332 Cytochrome c2, 49 Cytochrome c-551, 207 Cytochrome c-553, 72, 74 Cytochrome c-555, 33, 43, 207 Cytochrome f , 6, 7, 64, 277-279, 285 biosynthesis, 214, 215, 331-333 polypeptides, 214, 215, 277, 278, 324, 330-333 Cytochrome 0,34 Cytoplasmic membrane bacteria, 24, 27-29 C3 cycle, see reductive pentose phosphate cycle C4 pathway, 178-180 regulation, 191-193 C4 plants, 178-180, 185, 192 DCCD, 162 DCMU, 79, 82, 83, 127, 286, 328 Dihydroxyacetone phosphate formation, 177, 183 regulatory function, 190, 191 transport, 187, 188 Dio-9; 162 DNA chloroplast, 215-218, 222, 226, 227, 323-336, 344 nuclear, 222, 321, 323, 327, 331, 334 Ectothiorhodospira halochlork, 23, 33, 242 EDTA, 218, 335 Electrochromism, 54 Electron spin polarization, 113, 116-117 ENDOR, 105, 107 EPR Signal 11, 86, 115, 134 Erythrobacter longus, 35 ESE, 117-119 Excitation energy distribution, 14-17, 293-294 Exciton effects 299-302 FAD, 204,206 FCCP, 162 Ferredoxin, 6, 67 in photosystem I, 219-221, 330 in purple bacteria, 33 thioredoxin system, 185-187, 192 Ferredoxin-NADP+ reductase, 6, 67, 330 Flavocytochrome c , 205-207 Fluorescence, see photosystem I1 Fluorescence polarization, 306, 313 Free energy electron transport, 44, 53 Fremyella diplosiphon, 250-258 Fructose 1,6-bisphosphate formation, 177 regulatory function, 189-191, 195 353 Galactolipids, 274, 281, 282 Glyceraldehyde 3-phosphate formation, 176, 178 Grana, see thylakoid Linear dichroism, 300, 301, 313 Linker polypeptides, 255, 256 Luminescence, 83, 141, 170 Halobacteria, 21, 36 Heliobacterium chlorum, 28, 29, 39, 110, 112, 347 Hole burning, 56 Hydroxylamine binding to oxygen-evolving complex, 147, 148 effect on oxygen evolution, 137, 147 Magnetic quantum number, 100 Malate formation, 181, 185 transport, 180, 181 Manganese complex model, 150, 151 in oxygen evolution, 4, 115, 131, 134-138 in reaction center purple bacteria, 51 multiline EPR signal, 115, 135, 136, 142, 146, 147 release, 136, 137 UV absorption changes, 135, 141, 149 X-ray absorption spectroscopy, 135 Mpstigocladus laminosus, 249-258, 314 Menaquinone, 25, 28, 41, 45, 52, 110, 111 see also QA, QB Mesophyll cells, 178-181, 192 Mitchell's hypothesis, 8-12, 165-167 Mitochondrion origin, 344 Inside-out vesicles, 13, 275, 284 Interaction dipolar, 100, 101, 109 exchange, 101, 111, 112, 117, 118 exciton, 299-302 hyperfine, 100, 101 Zeeman, 105 Iron non-heme in reaction center, 52, 56, 77, 80, 109 Iron-sulfur centers EPR, 67, 104, 111 evolution of as electron acceptors, 347, 348 in Chloroflexus aurantiacus, 26, 203 in green sulfur bacteria, 27, 46, 110 in Heliobacterium chlorum, 29, 110 photosystem I, 6, 7, 67-70, 104, 111 Rieske, 6,26, 215, 278,279, 331, 332 Lemna, 321, 322 gibba, 263;264 Light-harvesting complex biosynthesis plants, 223-227, 334, 335 B1015 structure, 237, 240 B800-850 structure, 237, 240, 243-244, 301-306 B880 structure, 238-242 cryptomonads, 247 cyanobacteria, 247 energy transfer, 14-17,24, 233-235 exciton calculations, 303-311, 314-315 genes for, 223-227, 321-327, 333, 334 green bacteria, 27, 245-247, 308-31 phosphorylation of, 16, 288-290 photosystem I, 74, 262, 263 photosystem 11, 14, 223-225, 263-266, 276, 277, 279-281, 288-290, 306, 307, 32&328 polypeptides plants, 223-227, 332-335 purple bacteria, 32, 33, 238-245, 314-315 red algae, 247 Light-harvesting protein Prosthecochlork crystal structure, 308-311 NAD+ reduction, 201-203, 207 NADH dehydrogenase, 202, 203 NADP-G3P dehydrogenase, 176, 177 NADP+ reduction, 7, 201-203, 207 NADPH in carbon dioxide assimilation, 176, 177, 182, 184 Nicotiana, 321, 325 Nigericin, 162 Oenothera hookeri, 325, 330 Oxaloacetate metabolism, 179, 181 transamination, 180 Oxygen-evolving complex, 4, 131-151 biosynthesis, 225, 329 EPR, 115, 135 inhibition, 143-1 46 molecular structure, 150, 151 polypeptides, 128-132, 225, 329 see also S states P-680, 4, 84-86, 88, 90, 108, 109, 132, 13%141, 144, 223-225, 288,319-321, 476 electron donors to, 4, 83-87, 132, 13%143 P-700, 14, 64-67, 70, 73-75, 108, 219-221, 281, 283, 288, 290 P-700-protein biosynthesis, 222, 333-335 P-798, 29 P-840, 27 354 P-865, 25 P-870, 33, 4S57, 107, 108 P-960, 33, 54, 67 Panicum maximum, 180, 181 Petunia, 321, 322 Pheophytin as electron acceptor, 4, 81, 111, 113 EPR, 113 Phlorizin, 162 Phosphoenolpyruvate carboxylation, 179, 181, 192-194 in mesophyll cells, 192 production, 182, 192, 194 3-Phosphoglycerate formation, 176, 177 phosphorylation, 176, 177 regulatory function, 190 transport, 187, 188 Photogene, 226, 328 Photophosphorylation acid-base, 164, 169 ATPI2e ratio, 11, 160 coupling sites, 161 cyclic, 7, 27 electric field, 165, 169 energy transfer in relation to, 162 evolution of, 349, 350 H+/ATP ratio, 160 H+/e- ratio, 11, 160, 165 in single turnover flashes, 10 ApH in relation to, 165-167, 169 post-illumination, 164 AVI in relation to, 8-12, 163-167, 170 uncouplers, 162 see also ATP synthase Photorespiration in C4 plants, 179 Photosynthetic bacteria comparative biochemistry, 21-39 ecology, 24, 26, 28, 34, 35 phylogeny, 21, 22, 35-37 taxonomy, 29-32 Phyotosystem I biosynthesis, 222, 334-335 electron acceptors, 6, 64-73, 112, 113, 219-221 genes for, 262, 263, 333-334 location in thylakoid, 283-288 polypeptides, 73,74,219-223,262,263,279, 280, 332-335 reaction center, 6, 65, 73-75 see also P-700 Photosystem I1 alternative electron acceptors and donors, 80, 82, 84, 87, 140 biosynthesis, 225-227, 327-329 core complex, 127, 128, 130 electron acceptors, 5, 75-88, 113 electron donors, 4, 83-87, 132, 139-143 energy transfer, 14-17, 265, 266 fluorescence, 5, 12, 14-17, 75, 76, 80-83 genes for, 223-225, 321-327 heterogeneity, 285, 286 location in thylakoid, 283-288 luminescence, 83, 141, 142, 144, 170 polypeptides, , 89-91, 128-132, 143-146, 223-225, 265266,280, 320, 321 preparations, 126129 reaction center, 5, 8%91, 129, 130 see also P-680 Phycobiliproteins, 247-261 energy transfer, 315 structure, 248-261, 314, 315 Phycobilisomes distribution, 249-255 structure, 248-261 Phycocyanin, 249-261 Phycoerythrin, 249-261 Phycoerythrocyanin, 249-261 Piericidin A, 202 Plastocyanin, 2, 64, 72, 281, 290, 291 Plastoquinone, 5-7, 16, 77, 111, 141, 223, 288, 290 as electron donor to P-680, 86, 134 see also QA,QB Porphyridium cruentum, 253 Prochloron, 344 Prosthecochloris, 26, 27 aestuarii, 46,47, 110,236,246,247,308,309 Purple bacteria primary charge separation, 53-56 taxonomy, 29-31 Pyruvate metabolism, 179, 181 5, 44-57, 76, 80, 109, 111, 140, 169, 170, 275, 320 Qg, 5, 44, 45, 52, 53, 56, 77-80, 111, 275, 286, 320, 328 Quinones distribution in photosynthetic bacteria, 37 evolution of as electron acceptors, 346, 347 QA, Reaction center Chloroflexus aurantiacus, 24,25,48,52,313, 314 exciton calculations, 311-314 see also photosystem I, photosystem 11 355 Reaction center purple bacteria, 21, 32, 33, 4s57 absorption spectra, 53-55 crystal structure, 49-51 electron transport, 32, 33,43,53-56, 10-112 evolution, 345-348 isolation, 46 pigment arrangement, 51, 52 polypeptides, 33, 47-50 structure, 47-51, 311-314 X-ray analysis, 47-51 Reductive pentose phosphate cycle, 176-178 free energy changes, 183 in CAM plants, 181-183 in C4plants, 178-180 regulation, 183-187 Reverse electron transport, 169, 170, 204 Rhodobacter capsulatus, 34, 47, 49, 200, 203, 236-240, 243, 244 Rhodobacter sphaeroides, 31, 33, 34, 43-57, 107, 108, 11C112, 118, 119, 203, 236-240, 243, 244 Rhodocyclus gelatinosus, 31, 47, 238, 239 Rhodopseudornonas, see also Rhodobacter, Rhodocyclus Rhodopseudornonas acidophila, 238, 239, 244, 245 Rhodopseudornonas palustris, 238, 239, 244 Rhodopseudornonas viridis, 23, 33, 45, 47-52, 54-57, 67, 107, 112, 114, 215, 129, 237-242, 299, 303, 305, 311, 313, 345, 349 Rhodospirillum rubrum, 32-34, 43, 47, 67, 77, 107, 201, 203, 236-242, 244 Ribosomes chloroplast, 215 Ribulose 5-phosphate formation, 177 Ribulose-l,5-bisphosphate carboxylase, see rubisco Rieske iron-sulfur protein, see iron-sulfur centers RNA chloroplast, 226, 328, 333-335, 344 Rotenone, 202 Rubisco activation, 184 carboxylation, 178 oxygenase activity, 178, 184, 185 3-PGA formation, 178 RYDMAR 117-119 S states, 3, 85, 88, 125, 140-151 manganese involvement in, 4, 115, 134-138 proton release, 4, 148, 149 UV difference spectra, 135, 141, 149 see also oxygen-evolving complex Scenedesmus, 176 Signal 11, 86, 115, 134 Solanum nigrurn, 323 Spirodela, 328, 334, 335, 338 Stark effect, 54 Stromabolites, 345 Succinate oxidation, 201, 203, 204 Sucrose synthesis, 188-191 Sulfide oxidation, 204 Synechococcus, 256, 337 Synechocystis, 222 Tentoxin, 162 Thermoluminescence, 141, 142, 144 Thioredoxin, 185-187, 192 Thiosulfate oxidation, 207 Three-light reaction scheme for photosynthesis, Th ylakoid appressed and non-appressed regions of, 12, 13, 281-294 heterogeneity, 283-288 permeability, 10, 168 stacking, 292-294 structure, 12, 274-277 Triphenyltin, 162 Triplet state ADMR, 114 EPR 113-115 Ubiquinone, 33, 44, 45 see also QA, QB Vitamin K, as electron acceptor, 72 see also A, X-ray absorption spectroscopy manganese, 135 Zea mays, 179, 181 Zeeman energy, 98, 101 This Page Intentionally Left Blank .. .PHOTOSYNTHESIS New Comprehensive Biochemistry Volume 15 General Editors A NEUBERGER London L.L.M van DEENEN Utrecht ELSEVIER AMSTERDAM * NEW YORK * OXFORD Photosynthesis Editor... Company, Inc 52 Vanderbilt Avenue New York, NY 10017 USA Library of Congress Cataloging-in-PublicationData Main entry under title: Photosynthesis (New comprehensive biochemistry ; v 15) Includes... information concerning the primary reactions of photosynthesis and the inter* E.I Rabinowitch, Photosynthesis and Related Processes, Vol I Interscience Publishers, New York, 1945, 599 pp VI actions between