the chlorophyll-carotenoid proteins of oxygenic ... - Annual Reviews

Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996. 47:685–714 Copyright © 1996 by Annual Reviews Inc. All rights reserved

THE CHLOROPHYLL-CAROTENOID PROTEINS OF OXYGENIC PHOTOSYNTHESIS B. R. Green Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4

D. G. Durnford Department of Applied Science, Brookhaven National Laboratory, Upton, Long Island, New York 11973 KEY WORDS:

Chl a/b (CAB) proteins, fucoxanthin–Chl a/c proteins (FCP), Chl a–peridinen proteins, light-harvesting antenna, algae

ABSTRACT The chlorophyll-carotenoid binding proteins responsible for absorption and conversion of light energy in oxygen-evolving photosynthetic organisms belong to two extended families: the Chl a binding core complexes common to cyanobacteria and all chloroplasts, and the nuclear-encoded light-harvesting antenna complexes of eukaryotic photosynthesizers (Chl a/b, Chl a/c, and Chl a proteins). There is a general consensus on polypeptide and pigment composition for higher plant pigment proteins. These are reviewed and compared with pigment proteins of chlorophyte, rhodophyte, and chromophyte algae. Major advances have been the determination of the structures of LHCII (major Chl a/b complex of higher plants), cyanobacterial Photosystem I, and the peridinen–Chl a protein of dinoflagellates to atomic resolution. Better isolation methods, improved transformation procedures, and the availability of molecular structure models are starting to provide insights into the pathways of energy transfer and the macromolecular organization of thylakoid membranes.

CONTENTS INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . PIGMENT PROTEINS OF THE CORE COMPLEXES. . . . . . . . . . . . . . . . . . . . . . . . . Photosystem II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Combined Reaction Center and Internal Antenna in PSI . . . . . . . . . . . . . . . . . . . . . CP43¢ (CPVI-4 or CPIIIb) and the Prokaryotic Chl a/b Antenna . . . . . . . . . . . . . . .

686 687 687 689 689

685

1040-2519/96/0601-0685$08.00

686

GREEN & DURNFORD

CHL a/b PROTEINS OF HIGHER PLANTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . “What Green Band That Is…”. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Chl a/b (CAB) Polypeptides of PSII . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

691 691 692

THE ATOMIC STRUCTURE OF LHCII . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

693

THE LIGHT-HARVESTING PROTEINS OF ALGAE . . . . . . . . . . . . . . . . . . . . . . . . . Chlorophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Rhodophytes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chromophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dinoflagellates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . EARLY LIGHT-INDUCIBLE PROTEINS AND THEIR PROKARYOTIC RELATIVES ......................................................... EVOLUTIONARY RELATIONSHIPS IN THE CAB/FCP/ELIP/HLIP FAMILY . . . . . . MACROMOLECULAR ORGANIZATION IN THE PHOTOSYNTHETIC MEMBRANE. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lateral Heterogeneity of the Thylakoid Membrane System . . . . . . . . . . . . . . . . . . . . LHCII Trimers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Photosystem I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Photosystem II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ENERGY TRANSFER AND THE PIGMENT-PROTEIN COMPLEXES . . . . . . . . . . . . FOR THE FUTURE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

696 697 699 700 700

701 702 703 703 703 704 704 705 706

INTRODUCTION The pigment proteins of photosynthesis are responsible for the absorption of light energy and the primary steps in its conversion to other forms of energy. All of the pigment proteins bind both chlorophylls (Chl) and carotenoids. The Chls do most of the light harvesting whereas carotenoids protect against excess light energy (185). In some marine organisms, the latter also contribute significantly to light harvesting (78). Both Chls and carotenoids are essential for correct folding of the proteins that bind them (135). Although the pigment proteins tend to be called simply “Chl proteins” or “Chl protein complexes” when discussed as holoproteins, they are more correctly called “Chl-carotenoid proteins.” This review considers the two major types of Chl-carotenoid proteins: the Chl a proteins of cyanobacteria and eukaryotic chloroplasts, and the nuclear-encoded light-harvesting antenna proteins of eukaryotes, which bind a variety of other Chls as well as Chl a. Considerable progress in understanding the molecular makeup of eukaryotic and cyanobacterial photosynthetic membranes has been made since the publication of several comprehensive reviews on chlorophyll-carotenoid proteins (14, 27, 35, 64, 163). Both chloroplast-encoded (Chl a binding) and nuclearencoded (Chl a/b binding) polypeptides of the two photosystems have now been identified by peptide sequencing, and their genes have been cloned. It is now clear that the peripheral light-harvesting antennae (Chl a/b and Chl a/c proteins) of all eukaryotes are encoded by a large gene family that also includes a group of eukaryotic stress-response genes and related prokaryotic genes (42,

PHOTOSYNTHETIC PIGMENT PROTEINS

687

69). The structures of two pigment-protein complexes have been solved to atomic resolution: the major Chl a/b light-harvesting antenna complex (LHCII) of higher plants (105) and the entire Photosystem I complex of cyanobacteria (100). This review focuses on the structural and evolutionary aspects of photosynthetic pigment proteins. Complementary viewpoints and additional information are found in other recent reviews (70, 84, 90, 119, 125, 135) and in a book dedicated to developmental aspects of Chl proteins (161). The roles of Chl a/b proteins in regulation of light harvesting are considered in this volume by Horton et al (85).

PIGMENT PROTEINS OF THE CORE COMPLEXES The core complexes of the two photosystems include all the cofactors necessary for charge separation and electron transfer, as well as proximal (Chl a) light-harvesting antennae. The pigment proteins bind only Chl a and β-carotene and are chloroplast encoded in all eukaryotes. The organization and composition of the core complexes are highly conserved among green plants, cyanobacteria, and all classes of eukaryotic algae (Table 1). The degree of protein sequence conservation is on the order of 70–75% identity between cyanobacteria and chloroplasts, or higher if conservative substitutions are considered, which provides further evidence that all chloroplasts originated from a cyanobacterium-like ancestor that established an endosymbiotic relationship with a nonphotosynthetic eukaryote host (33, 63).

Photosystem II The core complex of PSII includes all the proteins, pigments, and cofactors necessary for light-driven movement of electrons from water to reduced plastoquinone (57). It contains three Chl-protein complexes: the reaction center (RC), where the initial charge separation occurs, and two internal Chl a lightharvesting antennae, CP47 and CP43 (Table 1). The reaction center, strictly defined, contains four to six Chl a's, two pheophytins, and two quinones involved in the initial charge separation, bound by a pair of hydrophobic polypeptides, D1 (psbA) and D2 (psbD) (149, 155). Whether there are four or six Chl a molecules per Reacton Center (RC) is the subject of lively debate. Spectroscopic similarities and conservation of chromophore-binding residues suggest that PSII-RC and the purple bacterial reaction center have a common ancestor (120). A number of hypothetical PSII models built on the bacterial template (e.g. 147, 174) have been useful in designing site-directed mutants in D1 and D2 (40, 173, 177). In

PSII REACTION CENTER (PSII-RC)

688

GREEN & DURNFORD

Table 1 Chlorophyll a complexes of cyanobacteria and chloroplasts. Figures not cited in the text are consensus values from a number of sources. Polypeptides are listed under their most commonly used names Pigments/cofactors Photosystem I

Core complex (CPI)

Photosystem II

Reaction center (RC)

CP47 (CPa-1) CP43 (CPa-2) Other

CP43′ (CPVI-4)

75–100 Chl a 12–15 β-carotene phylloquinone 4Fe-4S cluster 4–6 Chl a 2 pheophytin a 2 plastoquinone 1 nonheme Fe 1–2 β-carotene 20–22 Chl a 2–4 β-carotene 20 Chl a 5 β-carotene Chl a unidentified carotenoid

Polypeptides (encoded by) PsaA or PSI-A (psaA) PsaB or PSI-B (psaB)

D1 or PsbA (psbA) D2 or PsbD (psbD) cytochrome b559 (psbE,psbF) PsbI protein (psbI) PsbW protein (psbW) PsbB (psbB) PsbC (psbC) IsiA (isiA) (cyanobacteria only)

addition to D1 and D2, PSII-RC preparations contain three small proteins: cytochrome b559, PsbI, and PsbW (89, 149, 155), none of which is thought to bind Chl. CP47 and CP43 (also known as CPa-1 and CPa-2) are the internal light-harvesting proteins of PSII (22). The polypeptides of 52 and 48 kDa, encoded by psbB and psbC genes, are very hydrophobic and are predicted to form six transmembrane helices, with both amino and carboxyl termini on the stromal surface (22, 150). The best available data (Table 1) show about 20 Chl a and four to five β-carotene molecules per polypeptide chain, determined using amino acid analysis (3), in agreement with earlier work based on radiolabeling (41). CP47 and CP43 were reported to contain a small amount of lutein in addition to β-carotene (13). In addition to their role as antennae, these polypeptides may also contribute to the protein environment of the water-splitting apparatus. Both CP47 and CP43 polypeptides have a large loop between the fifth and sixth helices, exposed on the lumenal (interior) surface (22). In CP47, this loop is in contact with the 33-kDa polypeptide (psbO gene product) and may be involved in stabilizing the tetramanganese cluster (22, 52, 76). Mutants lacking CP43 cannot evolve O2, but this could be an indirect effect because all PSII polypeptides are depleted (173, 177).

CP47 AND CP43


689

Combined Reaction Center and Internal Antenna in PSI In PSI, the reaction center and internal antenna are combined in a single Chlprotein complex that accepts electrons from plastocyanin or a cytochrome and delivers them to a small ferredoxin-like molecule, encoded by the psaC gene (23, 36, 60, 61). This Chl-carotenoid protein consists of two hydrophobic polypeptides of about 82 kDa (psaA and psaB gene products) that bind the Chl a dimer (P700) and the initial electron acceptors A0 (Chl a), A1 (phylloquinone), and A2 (a 4Fe-4S center). The two polypeptides together bind 75–100 additional Chl a and 12–15 β-carotene molecules. These additional Chl molecules are the “built-in” Chl a antenna, filling the same role as the separate antenna complexes CP47 and CP43 in PSII. The structure of a trimeric cyanobacterial PSI complex has recently been determined to 4.0–4.5 Å resolution by X-ray crystallography (100, 154). The central part of the structure has some striking similarities to the bacterial RC, which had been predicted earlier on the basis of spectroscopic similarities (61, 126). The RC chlorophylls and quinones are organized in pairs around a twofold axis, with the single 4Fe-4S cluster (A2) above them, surrounded by five transmembrane helices from each of the PsaA and PsaB polypeptides. There are a total of 11 transmembrane helices in each of PsaA and PsaB (100, 154), plus two large surface helices lying parallel to the membrane plane (154). The 65 antenna Chl a molecules resolved in the X-ray structure appear to be hung on the outside of the central protein mass at various levels in the (presumed) lipid bilayer, but they are all oriented approximately perpendicular to the membrane axis (154).

CP43¢ (CPVI-4 or CPIIIb) and the Prokaryotic Chl a/b Antennae A novel Chl a protein related to CP43 (referred to as CP43′, CPVI-4, or CPIIIb) is made by certain cyanobacteria in response to iron starvation (158). Its 35kDa polypeptide, encoded by the isiA gene (158), differs from the CP43 polypeptide in having a much shorter lumenal loop between (predicted) helices V and VI. Because phycobilisomes are rapidly degraded under nutrient deprivation (74), CP43′ could maintain some of the cell's light-harvesting capacity or act as a Chl reservoir to speed recovery from iron limitation (28). A new light has been cast on this story with the discovery that the Chl a/b antenna polypeptides of prochlorophytes are encoded by homologues of the isiA genes (109, 171). Prochlorophytes are cyanobacteria-like prokaryotes that have both Chl a and Chl b and lack phycobilisomes (117, 139). When they were first discovered, it was thought that they could be directly related to the ancestral endosymbiont from which green chloroplasts are descended (117). However, molecular phylogeny unequivocally groups prochlorophytes with

690

GREEN & DURNFORD

Figure 1 Biosynthetic pathways connecting the chlorophylls, adapted from Reference 92a. Pigments known to be involved in light harvesting are boxed. Dotted lines indicate plausible biosynthetic relationships. Conversion of Chl a to Chl b requires oxidation of a methyl to a formyl group (176), Chl a to Chl d the oxidation of a vinyl to a formyl group (150).

cyanobacteria rather than chloroplasts and furthermore shows that the three known genera (Prochloron, Prochlorothrix, and Prochlorococcus) are not closely related to one another (62, 129, 139, 167). The Chl a/b protein sequences from all three prochlorophytes are remarkably similar, both to one another and to the CP43′ (isiA) proteins of several cyanobacteria (109, 171). The fact that very closely related proteins can bind either Chl a and Chl b or Chl a alone shows that it is possible for proteins to evolve the capacity to bind different accessory pigments with fairly minor sequence changes. In fact, the three prochlorophytes have rather different pigment compositions (117). Prochlorococcus has divinyl Chls a and b, and the Prochloron antenna contains the Chl c-like pigment MgDVP (Mg-2,4-divinyl phaeoporphyrin a5 monomethyl ester or divinyl protochlorophyllide) as well as Chls a and b (Figure 1; 107, 117). The addition of chlorophylls other than Chl a to the ancestral CP43′ protein may have improved its absorption characteristics and light-harvesting efficiency compared with that of the modern cyanobacterial CP43′, which is not an efficient antenna (28). One possible evolutionary scenario is that the common ancestor of all cyanobacteria may have been able to make and use a whole range of chlorophylls as light-harvesting pigments in addition to phycobiliproteins, and that different de-


691

scendants lost the ability to use one or more of them (24, 68). Alternatively, the ancestor could have made only Chl a, and the ability to synthesize Chl b might have arisen independently several times. Conversion of Chl a to Chl b requires only the conversion of a methyl to a formyl group, which could be accomplished by a monoxygenase recruited from another metabolic pathway. MgDVP is a precursor of all the Chls and is only one step removed from Chl c (Figure 1). Both scenarios are consistent with the variety of pigments found in the three known prochlorophytes, and both predict that photosynthetic prokaryotes with other pigment complements will be discovered.

Chl a/b PROTEINS OF HIGHER PLANTS “What Green Band That Is…” In the past few years, a general consensus has been reached about the polypeptide and pigment compositions of the higher plant Chl a/b–carotenoid complexes (92). The DNA sequences of the genes are available and have been matched to the proteins they encode by peptide sequencing (reviewed in 68, 71, 88, 90). This has resolved most of the confusion in protein identification that resulted from different methods of separation and the fact that pigment proteins, by their very nature, are labile in the presence of detergents but cannot be isolated without them. We can now answer the question “Just what green band is that?”—the subtitle of an earlier review (64). A standard nomenclature for the genes (and thus the polypeptides) has been codified (92), although different names for the pigment-protein complexes themselves are still in use (Table 2). To summarize, there are 10 Chl a/b (CAB) proteins, which with their associated carotenoids make up the six main separable pigment-protein complexes (Table 2). The major light-harvesting complex LHCII is probably organized into trimeric particles that transfer much of their excitation energy to PSII but that under certain conditions dissociate from it and migrate independently between stacked and unstacked regions of the thylakoid membrane. CP29 and CP26 are closely associated with the PSII core (6, 29, 65, 136), although they can be removed from it without affecting PSII activity. CP24 is removed from PSII along with LHCII (29). The two LHCI complexes associated with PSI are called LHCI-680 and LHCI-730 after their fluorescence emission maxima (15, 131). The former can be split into two pigmented subcomplexes, LHCI-680A and LHCI-680B, each enriched for a single polypeptide (99, 164). The 730-nm fluorescence may be associated with the Lhca4 polypeptide (164). It is generally agreed that the Chl a/b ratio of LHCII is 1.3–1.4 (105, 128), but there is a wide range of reported values for the other Chl a/b proteins (Ta-

692 Table 2

GREEN & DURNFORD

Chlorophyll a/b proteins of green plants

Pigment-protein complex Name in text Other names

Chl a/b ratio (Ref.)

LHCI-680A LHCI-680B LHCI-730

LHCIa

1.4 (140), 1.9 (164), 3.1 (131)

LHCIb

2.3 (140), 2.9 (164), 3.2 (131)

LHCII

LHCIIb

1.4 (38), 1.33 (137)

CP29 CP26 CP24 CP22

LHCIIa,CP29-Type II LHCIIc, CP29-Type I LHCIId intrinsic 22-kDa protein of PSII

2.3 (137), 2.8 (38), 3.1 (77) 1.8 (137), 2.2 (38), 3.3 (170) 0.9 (137), 1.6 (38) 6 (53)

Proteins encoded by

LHCI/LHCII polypeptide type

Lhca3 Lhca2 Lhca1 Lhca4 Lhcb1 Lhcb2 Lhcb3 Lhcb4 Lhcb5 Lhcb6 psbS

III II I IV I II III

ble 2). In general, the values approach 3 for the LHCI and minor PSII complexes, with the exception of CP24, which always has a very low Chl a/b ratio. The PSII-associated complexes are reported to differ in their Chl-toprotein ratios, with values of 12, 8, 9, and 5 for LHCII, CP29, CP26, and CP24, respectively (38). This means that the different Chl a/b ratios could result from all the proteins binding the same amount of Chl a but different amounts of Chl b. All the CABs bind lutein, as well as the xanthophylls neoxanthin and violaxanthin. The latter are enriched in CP29, CP26, and CP24 compared with LHCII (13, 110, 146). The role of the Chl a/b proteins in the xanthophyll cycle and nonphotochemical quenching is discussed in Horton et al (85). CP22 is a recent addition to the Chl a/b family (54, 55). Its 22-kDa polypeptide is encoded by the psbS gene, and it is predicted to form four transmembrane helices rather than three (98, 178). It has a Chl a/b ratio of about 6 and appears to have about half as much Chl/polypeptide as LHCII (55). It is stable in the absence of Chl, which suggests that it may have a role as a Chl reservoir or carrier rather than as a light-harvesting complex (53). Alternatively, it may act as a linker between LHCII and the PSII core (97).

The Chl a/b (CAB) Polypeptides of PSII LHCII preparations contain three closely related polypeptides (Types I, II, and III encoded by Lhcb1, Lhcb2, and Lhcb3, respectively) in ratios that vary from 10:3:1 to 20:3:1 depending on plant growth conditions and the preparative


693

method (116). All three of them can only be resolved simultaneously on certain gel systems (71, 116, 157) or by HPLC (39). All plants have multiple Lhcb1 genes encoding almost identical polypeptides (27, 35). Type II and Type III polypeptides are encoded by smaller numbers of genes (35, 71). Single amino acid differences among the population of Type I polypeptides or posttranslational modifications such as phosphorylation (4, 5) could explain the resolution of multiple Type I bands on the novel denaturing gel systems used by Staehelin and coworkers (6, 49, 157). Type I and II but not Type III LHCII polypeptides are phosphorylated (5, 6, 8, 85). The Type III polypeptide is present early in development and under conditions where Chl b is limiting (45, 75, 180), which leads to the suggestion that it might act as a linker between LHCII trimers and PSII core (75, 90). CP29 as originally defined had two polypeptides (29), which were shown to be the products of two different genes by peptide sequencing (138). Unfortunately, when improved isolation methods allowed the separation of the original CP29 complex into two Chl a/b complexes each containing a single polypeptide (38, 49, 77, 136), one of them was called CP29 and the other CP26. Although this is a violation of standard nomenclature rules [the “new” CP29 could have been called CP28 (66)], it does satisfy the “easy-recognition” criterion (64) and has been generally adopted (Table 2; 49, 92). The controversies about the number and composition of Chl a/b proteins (64, 90, 162) result from the fact that the PSII antenna proteins are all related in sequence and associated with one another in vivo, which makes them difficult to distinguish by all available methods. The only way to be sure a new polypeptide is unique is by partial peptide sequencing, preferably accompanied by the sequencing of the corresponding gene. For example, a second polypeptide in CP26 has been identified by protein sequencing (121). When the gene sequence is available it will be possible to tell whether it is a variant of the same Type or should be called Lhcb7. At present, there is no evidence for allelic variants at CAB gene loci. The evidence for and against several putative CAB polypeptides in plants is discussed by Jansson (90). More information about individual CAB polypeptides and genes can be found in References 68, 88, 99, 135, and 163.

THE ATOMIC STRUCTURE OF LHCII Probably the most significant recent achievement in the field of Chl-carotenoid proteins is the determination of the structure of purified pea LHCII to 3.4-Å resolution by electron crystallography (105). This structure is not only important because of the dominant role of LHCII in light harvesting but also because it provides a general model for the overall folding of all the Chl a/b proteins, as all Chl a/b proteins have substantial regions of sequence conservation (69, 104,

694

GREEN & DURNFORD

Figure 2 Structure of pea LHCII as determined by electron crystallography (105). α-helices are represented by ribbons, and the edge of the lipid bilayer is represented by shading. Chl molecules are represented by generic porphyrin rings, with proposed Chl a molecules shaded darker. Helices are denoted by letters as in Reference 105; B, C, and A are the first, second, and third transmembrane helices, respectively (cf Figure 3). Drawing courtesy of W Kühlbrandt.


695

105, 163). In fact, all members of the extended family of proteins, which also includes the fucoxanthin–Chl a/c proteins (FCP) and early light-inducible proteins (ELIP), are predicted to have the same overall fold (67, 105). The LHCII polypeptide folds into three membrane-spanning helices, with an additional small amphipathic helix near the C-terminal end (Figure 2; 105). The first (B) and third (A) helices (already known from sequence analysis to be related to each other) cross each other at an angle of about 30° to the membrane normal and are held together by reciprocal ion pairs involving an Arg on one helix and a Glu on the other. If the flattened helices in Figure 3 could be imagined in three dimensions, the side-chain of Arg 70 on helix 1 would be oriented almost straight up and as forming an ion pair with Glu 180 on Helix 3, while Arg 185 on Helix 3 would also be pointing straight up and bonding with Glu 65 on Helix 1. The two helices and the loops at their Nterminal ends are related by a twofold symmetry axis, along with two carotenoid molecules that connect the loops on either end of each helix, and four pairs of Chl molecules (Figure 2). Seven of the 12 Chl molecules visible in the structure were provisionally identified as Chl as because of their close proximity to one of the carotenoid molecules, which allows efficient energy transfer; the other five Chls, including three bound by the middle helix, were assigned to Chl b (105). Three of the Chl Mg atoms are ligated in a novel way, by the carbonyl groups of Glu residues involved in Glu-Arg ion pairs. Two of the symmetrical Chls (a1 and a4) are bound to the carbonyls of the Glu residues cross-linking Helices 1 and 3, and Chl b5 is ligated by the carbonyl of another Glu-Arg pair formed between adjacent turns of the second transmembrane helix (Figures 2 and 3). Another symmetrical pair of Chl a molecules (a2 and a5) are ligated by His and Asn side-chains in Helix 1 and Helix 3, respectively (Figure 3); Chl a3 is bound by a Gln in Helix 1; and Chl b3 by His in Helix 4(D). No ligands could be assigned to the other Chls. The residues binding the four symmetrical Chls are conserved in all members of the extended family (67). In terms of protein structure, the CAB proteins differ from one another in the surface-exposed loops that connect the helices and probably mediate proteinprotein interactions, and to a lesser extent in the middle transmembrane helix that binds Chl b (Figure 3). There are several conserved motifs in these exposed regions, however, that appear to shield the carotenoid head groups and Chl a molecules (67). Only one of these motifs is universally conserved in Chl a/c proteins (67). Now that it is possible to reconstitute LHCII from proteins expressed in vitro and to obtain trimers and two-dimensional crystals from them (81, 82), it should be possible to determine more precisely the roles of specific motifs and individual residues in the CAB polypeptides. The structure of LHCII differs markedly from the light-harvesting antennae of purple bacteria (96, 118). The latter are oligomeric proteins forming large

696

GREEN & DURNFORD

Figure 3 Model of LHCII showing amino acid sequence of pea Type I, with shading according to degree of conservation among CABs and FCPs/iPCPs (see legend). Helices are lettered (105) and numbered (68); hatching indicates edge of lipid bilayer.

rings of overlapping bacteriochlorophyll molecules. By analogy with an accelerator storage ring, the excitation energy could be very rapidly delocalized over the ring, enabling transfer of energy to any neighboring reaction center or antenna complex regardless of its orientation (118). The bacterial and eukaryotic antenna structures are clearly two independently derived structural solutions to the light-harvesting problem. Other unique three-dimensional solutions are found in the soluble membrane-extrinsic antennas: the phycobilisomes (51), the Prosthecochloris Chl a (FMO) protein (165), and the dinoflagellate peridinen Chl a protein (E Hofmann, F Sharples, P Wrench, R Hiller, W Welte & K Diederichs, personal communication).

THE LIGHT-HARVESTING PROTEINS OF ALGAE Photosynthetic eukaryotes are traditionally divided into three major groups largely on the basis of their light-harvesting pigments (142). The Chlorophytes (green algae and higher plants) have Chl a/b antennae, the Chromophytes have Chl a/c antennas, and the Rhodophytes (red algae) have only Chl a and use


697

phycobilisomes (extrinsic phycobilin-containing structures) as the major PSII antenna. A taxonomic difficulty arises in some groups whose pigment compositions do not put them into the same taxa as classification based on the number of membranes around the chloroplast, flagellar structure, or other anatomical features (Table 3). The Eustigmatophytes have only Chl a but do not have phycobilisomes, the Prasinophytes have the Chl c-like pigment MgDVP as well as Chls a and b, and the Cryptophytes have Chls a and c as well as phycobilins located in the lumen of the thylakoid. The Dinophyta (dinoflagellates) and Euglenophyta are the only taxa with three chloroplast envelope membranes, but their antenna pigments and the sequences of their antenna proteins group them with the Chromophytes and Chlorophytes, respectively. In spite of different pigment compositions, immunological and sequence data (where available) show that all the antenna polypeptides are structurally related to one another (68). Structures of all the Chls known to be bound by members of this extended family are boxed in Figure 1. Information on algal Chl proteins up to 1990 was thoroughly reviewed by Hiller et al (78).

Chlorophytes The green algae have about the same number and complexity of Chl proteins as the higher plants (7, 16, 17), but only a few chlorophyte CAB gene sequences have been reported (68, 90). These genes can be assigned to LHCI or LHCII but not to Types within them (Table 3, Figure 4). There may be additional members of the CAB family in Chlamydomonas that are not found in higher plants (16, 17, 56). Some marine siphonous green algae contain the carotenoids siphonoxanthin and siphonein, which increase blue light–harvesting capacity (78).

CHLOROPHYTA

PRASINOPHYTA The LHC complexes from the prasinophyte Mantoniella have at least two polypeptides of 20–21 kDa (78, 94, 144, 152) arranged into larger oligomeric complexes (144). The presence of a Chl c-like pigment suggested they might be related to the Chl a/c proteins, but gene and protein sequencing showed them to be more related to Chl a/b proteins (Figure 4; 94, 145, 152). There is some evidence that a unique PSI-associated antenna may not exist in Mantoniella and that the same protein complex excites both photosystems (153).

Euglena is generally included with the chlorophytes because of its Chl a/b antenna. Its LHCI and LHCII polypeptides are definitely related to those of green algae (Figure 4; 86, 123). The presence of a third membrane surrounding the Euglena chloroplast suggests that it may have evolved from a eukaryotic rather than a prokaryotic endosymbiont (58). The

EUGLENOPHYTA

698

GREEN & DURNFORD


699

Figure 4 Parsimony tree showing the phylogenetic relationships between amino acid sequences of the main types of light-harvesting proteins, calculated with the PHYLIP package (50). Proteins labeled by gene type and organism name (see Tables 2 and 3). Numbers on branches are bootstrap values (100 replicates) and give an estimate of branch stability. Variable regions that could not be aligned across all sequences were omitted from the analysis.

only remaining traces of the endosymbiont would be the chloroplast surrounded by a membrane originating from the phagocytic host (58, 59). In support of this idea, phylogenetic studies on 18S rRNA show that the “host” is unrelated to the green algae or any other photosynthetic eukaryote (34). The LHCII and LHCI proteins are synthesized as polyproteins that are cleaved after import into the chloroplast (86, 123). It has now been shown convincingly that the polyprotein precursor is cotranslationally inserted into the ER membrane and passed to the Golgi before arriving in the chloroplast by an unknown mechanism (160).

Rhodophytes The rhodophyte plastid genome carries many more genes than the higher plant plastid genome, including most of the genes encoding photosynthetic proteins (143). Along with the presence of phycobilisomes, this suggests the red algal chloroplast is more recently evolved from an endosymbiotic cyanobacterial ancestor. It has now been discovered that the red algae have a PSI-associated antenna complex with four to five polypeptides immunologically related to Chl a/b and Chl a/c antenna proteins, even though the polypeptides bind only Chl a

700

GREEN & DURNFORD

(181, 182). These polypeptides are similar enough to higher plant CABs that they can be assigned to one of the four LHCI Types. The Porphyridium cruentum Lhca1 gene encodes a polypeptide having about 30% identity with higher plant Lhca1 (E Gantt & S Tan, personal communication). These findings are very significant, because they suggest that all the eukaryotic nuclear-encoded light-harvesting antenna proteins are descended from a common ancestral protein (181) and call into question classification schemes that put the red algae on a completely separate branch from chlorophyte and chromophyte algae.

Chromophytes The chromophytes have a smaller number (1–3) of fucoxanthin–Chl a/c polypeptides (FCP) with a typical size range of 17–22 kDa compared with 20–30 kDa for the chlorophyte CABs (Table 3; 78). As biochemical methods improve, the number of FCP polypeptides increases: The raphidophyte Heterosigma now has at least eight immunologically distinguishable polypeptides (47). The Chl a/c ratios of the major chromophyte LHCs are varied, ranging from 1 to 5.6 (78, 79). In general, they have a higher carotenoid:Chl ratio than the higher plant LHCs, and those carotenoids, especially fucoxanthin, make a significant contribution to spectral coverage in the green region of the spectrum (78). The xanthophyte Pleurochloris is the only chromophyte where a PSIassociated antenna with a fluoresence emission different from the main LHC has been reported (25). There is no evidence for specific antenna polypeptides associated with PSI or PSII in other chromophytes. Gene sequences for the major Chl a/c polypeptides of two diatoms (73, 102), two phaeophytes (10, 30), a raphidophyte (48), a chrysophyte (132), and a haptophyte (108) are now available. Sequence comparisons demonstrate that the Chl a/c proteins are indeed related to the Chl a/b proteins (Figure 3), although the relationship is distant (Figure 4). Southern blots indicate the presence of multigene families in several groups (10, 19, 48). The FCPs are all nuclear encoded and synthesized on cytoplasmic ribosomes. The presence of four membranes around the chromophyte chloroplast suggests that chromophytes originated from a secondary endosymbiosis between a photosynthetic eukaryote and a nonphotosynthetic host (33, 44, 59). Very little is known about how the Chl a/c polypeptides make their way from cytoplasm to thylakoid across four membranes, but there is evidence that they are cotranslationally inserted into the endoplasmic reticulum (18), which provides a possible explanation for how they cross the outermost membrane.

Dinoflagellates The dinoflagellates are not considered true chromophytes because they have peridinin rather than fucoxanthin as their major carotenoid and three mem-


701

branes rather than four around the chloroplast. They have two types of lightharvesting complex: a membrane-intrinsic peridinin–Chl a/c complex (iPCP) and a water-soluble peridinin–Chl a complex (sPCP) (78). The sequences of the iPCP polypeptides are related to those of chromophyte FCPs (79, 87) and clearly belong to the FCP branch of the CAB/FCP family (Figure 4). The Amphidinium iPCP polypeptides are translated as a polyprotein (80) that is posttranslationally cleaved to as many as 10 individual but closely related polypeptides (79, 80). Because the dinoflagellate chloroplast is similar to the Euglena chloroplast in being surrounded by three membranes and importing light-harvesting complex proteins as polyproteins, a similar transport mechanism (160) may be involved. The polypeptide(s) of the sPCPs are also nuclear encoded but are not synthesized as polyproteins, although some species have a 35-kDa polypeptide that contains two repeats of the same sequence whereas others have a homodimer of two 15-kDa polypeptides (127). The gene sequence shows no similarity to any other pigment protein (127). The three-dimensional structure of the Amphidinium sPCP has been solved by X-ray crystallography (E Hofmann, F Sharples, P Wrench, R Hiller, W Welte & K Diederich, personal communication). It is quite unlike any other light-harvesting protein: The eight peridinens and two Chl as float in a “boat” made of 16 α-helices. This is the first solved structure of an antenna protein having carotenoids as the major light-absorbing pigment.

EARLY LIGHT-INDUCIBLE PROTEINS AND THEIR PROKARYOTIC RELATIVES The early light-inducible proteins (ELIP) are included with the light-harvesting complexes because their proteins are predicted to have three transmembrane helices and because they share conserved sequences with the Chl a/b proteins (68, 69). They are part of a complex gene family, like the CAB gene family. They are induced primarily by high light stress (111, 112). It has been suggested that ELIPs act as Chl scavengers after light-induced breakdown of Chl proteins (2). Their association with massive β-carotene accumulation in Dunaliella led to the suggestion that this ELIP could have a carotenoid-binding role (111). ELIPs have been proposed to bind xanthophyll cycle pigments in intermittent light-grown plants, which do not accumulate Chl a/b proteins, and to act as sinks for excitation energy under high light (101). The isolation of a single ELIP polypeptide binding lutein and a small amount of Chl has recently been reported (1). ELIPs have not been reported in chromophyte or rhodophyte algae. However, a gene for a one-helix protein (HLIP) expressed under high light stress conditions and related to the ELIPs has been found in cyanobacteria (42).

702

GREEN & DURNFORD

HLIP-like genes have also been found on the plastid genomes of two rhodophyte algae (42; M Reith, personal communication) and on the cyanelle genome of the glaucophyte Cyanophora paradoxa (VL Stirewalt & DA Bryant, personal communication). Because these one-helix proteins are related to both first and third helices of the higher plant ELIPs, and because two transmembrane helices are required to make the reciprocal ion pairs and bind Chl, it has been suggested that they form homodimers (42, 67). To date, there is no evidence that HLIPs of cyanobacteria or red algal chloroplasts bind Chl.

EVOLUTIONARY RELATIONSHIPS IN THE CAB/FCP/ELIP/HLIP FAMILY All the Chl a/b, Chl a/c, and Chl a/a light-harvesting antenna proteins are part of an extended gene family that also includes the ELIPs (68, 69, 90). Conserved residues in the first and third helices of all these proteins include those ligating the four core Chl a molecules, the ionic cross-bridges, and the pattern of small residues (G,A,S,C) that allow the helices to pack together efficiently (67, 105). The discovery of the cyanobacterial HLIP gene, clearly sharing the same conserved residues, supports the idea that prokaryotic HLIPs and eukaryotic antenna proteins had a common ancestor. Because the CAB family includes a four-helix member (CP22 or PsbS) that clearly originated from the duplication of a two-helix protein (98, 178), it has been proposed that a similar gene duplication followed by deletion of the fourth helix gave rise to the three-helix CABs/FCPs/ELIPs (68). The second helix of the two-helix ancestor would have been acquired by a previous fusion of an HLIP-like gene with the gene for another one-helix protein (67). However, there is no obvious relatedness between the second helix of the eukaryotic ELIPs and that of the CABs, so it is possible the middle helices were acquired independently. A phylogenetic tree (Figure 4) generated using the parsimony method (50) shows the FCPs on a separate branch from the CABs. LHCII and LHCI CABs diverged before the green alga/higher plant split, because the Chlamydomonas sequences group with one or the other, but the three LHCII Types (Lhcb1, Lhcb2, and Lhcb3) diverged later. In all the trees, Lhcb5 groups with LHCII, and Lhcb4 and Lhcb6 group together, sometimes closer to the LHCII group and sometimes to the LHCI group (90; DG Durnford, unpublished data). Three of the LHCI sequences cluster together, but all four of them are more divergent from one another than the three LHCII types (DG Durnford, unpublished manuscript). Considering that rhodophyte algae have LHCI but not LHCII and that the LHCI genes appear to have been diverging from one another longer than the LHCII genes, it is possible that LHCII originated from LHCI.


703

MACROMOLECULAR ORGANIZATION IN THE PHOTOSYNTHETIC MEMBRANE Lateral Heterogeneity of the Thylakoid Membrane System Although the thylakoid membrane system is continuous, two distinct regions can be differentiated in higher plants: single unappressed thylakoids (stroma lamellae) and grana stacks consisting of a number of appressed thylakoids. Most of PSII is segregated in the granal regions, and most of PSI is segregated in the stromal regions (8). Furthermore, the PSII units found in stromal regions (PSIIβ) have smaller antenna sizes than the PSIIα units of the grana regions, and at least part of the population is photochemically inactive, i.e. unable to reduce Qb (8, 119). PSI is also heterogeneous: PSIα found in the margins of the granal stacks has a larger antenna size than PSIβ in the stromal regions because of association with LHCII (9, 183). Although detergent fractionation is used in many cases to separate granal and stromal fractions, work from the laboratory of Albertsson (9, 183) involves mechanical fragmentation followed by twophase separation, which argues against fortuitous associations provoked by detergent solubilization. LHCII is found in both regions of the thylakoid membrane system and can transfer excitation energy to PSI as well as PSII. A subpopulation of LHCII can move from granal to stromal regions depending on light quality, redox potential, and phosphorylation (reviewed in 4, 5, 8). This implies that LHCII trimers are not strongly attached to PSII and are able to move independently in the thylakoid membrane system. There are different ratios of the three LHCII polypeptides in stromal, granal, and granal margin fractions (9). There is little or no evidence for lateral heterogeneity of the thylakoid membrane in chromophytes (113, 141, 175). The one possible exception is found in the xanthophyte Pleurochloris, where examination of freeze-fracture specimens by electron microscopy does show some evidence for lateral heterogeneity within the thylakoid membranes, and there appear to be small but significant changes in particle distribution on dark-light adaptation (26).

LHCII Trimers There is good evidence that LHCII exists as a trimer in vivo (reviewed in 90, 104). The LHCII trimers used for molecular structure determination by X-ray crystallography contained both Type I and Type II polypeptides, which have only minor differences in amino acid sequence outside of the first 20 residues (104, 128). It is not known whether LHCII in the plant is present as homo- or heterotrimers, although homotrimers of Type I LHCII have been isolated by chromatography (128). Developmental studies suggest that LHCII is first organized in monomers and only becomes trimeric when the thylakoid mem-

704

GREEN & DURNFORD

brane structure is approaching its mature state (45). A WYGPDR motif conserved in LHCII and CP26 but not in CP29, CP24, or LHCI (68) is essential for the formation of trimers in vitro (81). Phosphatidylglycerol is also involved in trimer stabilization (128).

Photosystem I Both monomeric and trimeric forms of the PSI holocomplex can be isolated from cyanobacteria; the trimer is probably the native form (reviewed in 103). It is generally agreed that higher plant PSI is monomeric and that LHCI remains associated with the PSI core under all physiological conditions (e.g. 9, 21, 183). It has been estimated that there are two copies of each of the four LHCI Chl proteins in each PSI holocomplex, which are possibly arranged in a single layer around the PSI core (21, 90). Cross-linking studies suggest that Lhca2 and Lhca3 form homodimers, but Lhca1 and Lhca4 may form heterodimers (91). However, developmental studies have been interpreted in favor of trimers (46). Several models for the arrangement of Chl proteins in higher plant PSI have been proposed (46, 90, 91, 99).

Photosystem II There is an ongoing debate about whether PSII is a dimer (12, 20, 38, 115, 137, 148) or a monomer (83), with the weight of evidence currently favoring the dimer. The clearest picture comes from negatively stained cyanobacterial PSII particles and spinach PSII cores (without Chl a/b antennas), subjected to sophisticated image analysis (20). These particles clearly have an axis of twofold symmetry bisecting their largest dimension (Figure 5). Molecular weight estimates and the presence of two separate 33-kDa (PsbO) polypeptides per particle support the idea that they are dimeric. Images supporting the dimer concept have also been obtained by atomic force microscopy (156) and from twodimensional crystals of PSII depleted in LHCII (115). On the other hand, images of ordered arrays of particles in PSII membranes containing the full complement of CAB proteins have been interpreted as having a monomeric PSII core (83). Spinach PSII particles containing the Chl a/b antenna complexes have two symmetrical appendages peripheral to the core dimer (Figure 5; 20). A trimer of LHCII fits snugly into each corner, leaving several small regions of electron density unaccounted for. There is not yet enough evidence to localize the minor CAB proteins (CP29, CP26, CP24, CP22). A number of imaginative PSII models have been proposed on the basis of Chl proteins co-isolated after mild detergent solubilization and electrophoresis (90).


705

Figure 5 Model of PSII dimer (top view). Drawn from Reference 20. The unlabeled ovals are regions of electron density that cannot be assigned but probably represent the minor CAB complexes CP29, CP26, CP24, and CP22.

ENERGY TRANSFER AND THE PIGMENT-PROTEIN COMPLEXES There are now many well-defined active preparations of PSII and PSI holocomplexes, core complexes, reaction centers, and antenna complexes. These improved biochemical preparations have yielded higher quality biophysical data for studying the detailed mechanisms of exciton and electron transfer (172). These studies (briefly summarized) have shown that: 1. Excitation energy is rapidly equilibrated throughout the PSI and PSII pigment beds within a few tens of picoseconds (166, 172). All types of particles, including isolated Chl a/b antennae (106, 124, 130, 131, 166), have several fast fluorescence decay components, probably resulting from competing energy transfer processes. 2. Within isolated trimeric LHCII, excitation energy equilibrates in less than 10 ps, but the dominant fluorescence lifetime is several ns, giving maximum opportunity for excitation to be transferred to reaction centers (106, 130). 3. The absorption and fluorescence maxima of all the PSII complexes, both Chl a and Chl a/b–binding, are rather similar, i.e. there are no differences in energy that would funnel excitation energy downhill toward the reaction center (93). The absorption of each isolated Chl protein or complex can be resolved into a number of Gaussian curves (93, 186). These may represent

706

GREEN & DURNFORD

Chl molecules in different protein environments, but they could also reflect collective excitation of groups of pigments close enough together for excitonic coupling (170). 4. Long wavelength fluorescence is not the sole property of LHCI-730: PSI cores from cyanobacteria and higher plants have several “red” Chls close to the reaction center (168, 179, 184). These low-energy Chls are believed to act as a “sink” for accumulation of excitation energy prior to its transfer to the reaction center. Considering that there are Chls in many different orientations and environments within each Chl a/b protein (see the LHCII structure) to say nothing of the Chls on PsaA/B, CP47, and CP43, it is not surprising that we are far from understanding the contributions of any one Chl protein or its interactions with the others. Readers interested in pursuing these questions will find an entry to the literature in the cited references.

FOR THE FUTURE The protein-binding proteins of the oxygenic photosynthetic apparatus and the genes encoding them are close to being sorted out. In contrast, our knowledge of how these components are assembled into an exquisitely engineered energy transfer apparatus is still primitive. It is a mystery why there should be such a variety of different light-harvesting proteins, especially in higher plants that are more likely to suffer from too much rather than too little light absorption. Developing techniques for targeted mutagenesis of nuclear genes in Chlamydomonas reinhardtii may soon make it possible to study the effects of deleting one or more CAB proteins. In vitro reconstitution and electron/X-ray crystallography should give a better idea of how the pigments are bound and the degree of adaptability among pigment-binding proteins. Better three-dimensional structures will provide a framework for understanding the mechanisms of energy transfer, which are far from being rigorously described at the quantum mechanical level. ACKNOWLEDGMENTS We thank all our colleagues who sent reprints and unpublished information, supplied missing references, and provided clarification. We particularly thank W. Kühlbrandt for Figure 2, M. Rögner for help with Figure 5, M. RoobalBoza for reading the manuscript, and L. Balakshin for manuscript preparation. B. R. Green thanks the Natural Sciences and Engineering Research Council of Canada for continuous support of her research on pigment proteins.


707

Any Annual Review chapter, as well as any article cited in an Annual Review chapter, may be purchased from the Annual Reviews Preprints and Reprints service. 1-800-347-8007; 415-259-5017; email: [email protected]

Literature Cited 1. Adamska I, Kloppstech K. 1995. Light stress proteins (ELIPs); the intriguing relatives of cab gene family. See Ref. 116a, 3:887–92 2. Adamska I, Ohad I, Kloppstech K. 1992. Synthesis of the early lightinducible protein is controlled by blue light and related to light stress. Biochim. Biophys. Acta 89:2610–13 3. Alfonso M, Montoya G, Cases R, Rodriguez R, Picorel R. 1994. Core antenna complexes, CP43 and CP47, of higher plant photosystem II: spectral properties, pigment stoichiometry, and amino acid composition. Biochemistry 33:10494–500 4. Allen JF. 1992. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098:275–335 5. Allen JF. 1995. Thylakoid protein phosphorylation, state 1 state 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression: minireview. Physiol. Planta. 93:196–205 6. Allen KD, Staehelin LA. 1992. Biochemical characterization of photosystem-II antenna polypeptides in grana and stroma membranes of spinach. Plant Physiol. 100:1517–26 7. Allen KD, Staehelin LA. 1994. Polypeptide composition, assembly and phosphorylation patterns of the photosystem II antenna system of Chlamydomonas reinhardtii. Planta 194:42–54 8. Anderson JM, Andersson B. 1988. The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends Biochem. Sci. 13:351–55 9. Andreasson E, Albertsson PA. 1993. Heterogeneity in photosystem-I: the larger antenna of photosystem-I alpha is due to functional connection to a special pool of LHCII. Biochim. Biophys. Acta 1141:175–82 10. Apt KE, Clendennen SK, Powers DA, Grossman AR. 1995. The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera. Mol. Gen. Genet. 246: 455–64 11. Arsalane W, Rousseau B, Thomas JC. 1992. Isolation and characterization of native pigment-protein complexes from

12.

13.

14.

15. 16.

17.

18.

19.

20.

21.

22. 23.

two Eustigmatophyceae. J. Phycol. 28: 32–36 Bassi R, Dainese P. 1992. A supramolecular light-harvesting complex from chloroplast photosystem-II membranes. Eur. J. Biochem. 204:317–26 Bassi R, Pineau B, Dainese P, Marquardt J. 1993. Carotenoid-binding proteins of photosystem II. Eur. J. Biochem. 212:297–303 Bassi R, Rigoni F, Giacometti GM. 1990. Chlorophyll binding proteins with antenna function in higher plants and green algae. Photochem. Photobiol. 52: 1187–206 Bassi R, Simpson D. 1987. Chlorophyllprotein complexes of barley photosystem I. Eur. J. Biochem. 163:221–30 Bassi R, Soen SY, Frank G, Zuber H, Rochaix JD. 1992. Characterization of chlorophyll a/b proteins of photosystem I from Chlamydomonas reinhardtii. J. Biol. Chem. 267:25714–21 Bassi R, Wollman F-A. 1991. The chlorophyll-a/b proteins of photosystem-II in Chlamydomonas reinhardtii: isolation, characterization and immunological cross-reactivity to higher-plant polypeptides. Planta 183:423–33 Bhaya D, Grossman AR. 1991. Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol. Gen. Genet. 229:400–4 Bhaya D, Grossman AR. 1993. Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatom Phaeodactylum tricornutum. Nucleic Acids Res. 21:4458–66 Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, et al. 1995. Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc. Natl. Acad. Sci. USA 92:175–79 Boekema EJ, Wynn RM, Malkin R. 1992. The structure of spinach photosystem I studied by electron microscopy. Biochim. Biophys. Acta 1017:49–56 Bricker TM. 1990. The structure and function of CPa-1 and CPa-2 in photosystem II. Photosynth. Res. 24:1–13 Bryant DA. 1992. Molecular biology of photosystem I. In The Photosystems: Structure, Function and Molecular Bi-

708

24. 24a. 25.

26.

27.

28.

29.

30.

31. 32.

33. 34.

35.

36.

GREEN & DURNFORD ology, ed. J Barber, pp. 501–41. Amsterdam: Elsevier Bryant DA. 1992. Puzzles of chloroplast ancestry. Curr. Biol. 2:240–42 Bryant DA, ed. 1994. The Molecular Biology of Cyanobacteria. Dordrecht: Kluwer Büchel C, Wilhelm C. 1993. Isolation and characterization of a photosystemI–associated antenna (LHC-I) and a photosystem-I core complex from the chlorophyll-c-containing alga Pleurochloris meiringensis (Xanthophyceae). J. Photochem. Photobiol. B 20:87–93 Büchel C, Wilhelm C, Hauswirth N, Wild A. 1992. Evidence for a lateral heterogeneity by patch-work like areas enriched with photosystem I complexes in the three thylakoid lamellae of Pleurochloris meiringensis (Xanthophyceae). Cryptogam. Bot. 2:375–86 Buetow DE, Chen H, Erdös G, Yi LSH. 1988. Regulation and expression of the multigene family coding lightharvesting chlorophyll a/b-binding proteins of photosystem II. Photosynth. Res. 18:61–97 Burnap RL, Troyan T, Sherman LA. 1993. The highly abundant chlorophyllprotein complex of iron-deficient Synechococcus sp PCC7942 (Cp43′) is encoded by the isiA gene. Plant Physiol. 103:893–902 Camm EL, Green BR. 1989. The chlorophyll ab complex, CP29, is associated with the photosystem-II reaction center core. Biochim. Biophys. Acta 974:180–84 Caron L, Douady D, Rousseau B, Quinet-Szely M, Berkaloff C. 1995. Light-harvesting complexes from a brown alga: biochemical and molecular study. See Ref. 116a, 3:223–26 Deleted in proof Caron L, Remy R, Berkaloff C. 1988. Polypeptide composition of lightharvesting complexes from some brown algae and diatoms. FEBS Lett. 229:11–15 Cavalier-Smith T. 1993. The origin, losses and gains of chloroplasts. See Ref. 112a, pp. 291–348 Cavalier-Smith T, Allsopp MTEP, Chao EE. 1994. Chimeric conundra: Are nucleomorphs and chromists monophyletic or polyphyletic? Proc. Natl. Acad. Sci. USA 91:11368–72 Chitnis PR, Thornber JP. 1988. The major light-harvesting complex of photosystem II: aspects of its molecular and cell biology. Photosynth. Res. 16:41–63 Chitnis PR, Xu Q, Chitnis VP, Nechushtai R. 1995. Function and organization

37.

38.

39.

40.

41.

42.

43.

44. 45.

46.

47.

48.

of photosystem I polypeptides. Photosynth. Res. 44:23–40 Cunningham FX, Schiff JA. 1986. Chlorophyll-protein complexes from Eu-glena gracilis and mutants deficient in chlorophyll b. II. Polypeptide composition. Plant Physiol. 80:231–38 Dainese P, Bassi R. 1991. Subunit stoichiometry of the chloroplast photosystem-II antenna system and aggregation state of the component chlorophyll-a/b binding proteins. J. Biol. Chem. 266:8136–42 Damm I, Green BR. 1994. Separation of closely related intrinsic membrane polypeptides of the photosystem-II light-harvesting complex (LHC-II) by reversed-phase high-performance liquid chromatography on a poly (styrene-divinylbenzene) column. J. Chromatogr. 664:33–38 Debus RJ. 1992. The manganese and calcium ions of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1102: 269–352 deVitry C, Wollman F-A, Delepelaire P. 1984. Function of the polypeptides of the photosystem II reaction center in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 767:415–22 Dolganov NAM, Bhaya D, Grossman AR. 1995. Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc. Natl. Acad. Sci. USA. 92:636–40 Douady D, Rousseau B, Caron L. 1994. Fucoxanthin-chlorophyll a/c lightharvesting complexes of Laminaria saccharina: partial amino acid sequences and arrangement in thylakoid membranes. Biochemistry 33:3165–70 Douglas SE. 1994. Chloroplast origins and evolution. See Ref. 24a, pp. 91–118 Dreyfuss BW, Thornber JP. 1994. Assembly of the light-harvesting complexes (LHCs) of photosystem II: monomeric LHC IIb complexes are intermediates in the formation of oligomeric LHC IIb complexes. Plant Physiol. 106:829–39 Dreyfuss BW, Thornber JP. 1994. Organization of the light-harvesting complex of photosystem I and its assembly during plastid development. Plant Physiol. 106:841–48 Durnford DG, Green BR. 1994. Characterization of the light harvesting proteins of the chromophytic alga, Olisthodiscus luteus (Heterosigma carterae). Biochim. Biophys. Acta 1184:118–26 Durnford DG, Green BR. 1995. Characterization of a gene encoding a


49.

50. 51.

52.

53.

54.

55.

56.

57.

58.

59.

60. 61.

fucoxanthin-chlorophyll protein from the chromophytic alga, Heterosigma carterae. See Ref. 116a, 1:963–66 Falbel TG, Staehelin LA. 1992. Speciesrelated differences in the electrophoretic behavior of CP29 and CP26: an immunochemical analysis. Photosynth. Res. 34:249–62 Felsenstein J. 1992. PHYLIP (phylogeny inference package). Univ. Wash., Seattle Ficner R, Lobeck K, Schmidt G, Huber R. 1992. Isolation, crystallization, crystal structure analysis and refinement of β-phycoerythrin from the red alga Porphyridium sordidum at 2.2 Å resolution. J. Mol. Biol. 228:935–50 Frankel LK, Bricker TM. 1995. Interaction of the 33-kDa extrinsic protein with photosystem II: identification of domains on the 33-kDa protein that are shielded from NHS-biotinylation by photosystem II. Biochemistry 34:7492–97 Funk C, Adamska I, Green BR, Andersson B, Renger G. 1995. The nuclearencoded chlorophyll-binding PSII-S protein is stable in the absence of pigments. J. Biol. Chem. 270:30141–47 Funk C, Schröder WP, Green BR, Renger G, Andersson B. 1994. The intrinisic 22-kDa protein is a chlorophyll-binding subunit of photosystem II. FEBS Lett. 342:261–66 Funk C, Schröder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B. 1995. The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry 34:11133–41 Gagné G, Guertin M. 1992. The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol. Biol. 18:429–45 Ghanotakis DF, Yocum CF. 1990. Photosystem II and the oxygen-evolving complex. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:255–76 Gibbs SP. 1978. The chloroplasts of Euglena may have evolved from symbiotic green algae. Can. J. Bot. 56:2883–89 Gibbs SP. 1981. The chloroplast endoplasmic reticulum: structure, function and evolutionary significance. Int. Rev. Cytol. 72:49–99 Golbeck JH. 1992. Structure and function of photosystem I. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 43:293–324 Golbeck JH. 1993. Shared thematic elements in photochemical reaction cen-

62.

63. 64.

65.

66.

67.

68.

69.

70.

71.

72.

73.

709

ters. Proc. Natl. Acad. Sci. USA 90: 1642–46 Golden SS, Morden CW, Greer KL. 1993. Comparison of sequences and organization of photosynthesis genes among the prochlorophyte Prochlorothrix hollandica, cyanobacteria, and chloroplasts. See Ref. 112a, pp. 141–58 Gray MW, Doolittle WF. 1982. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46:1–42 Green BR. 1988. The chlorophyll-protein complexes of higher plant photosynthetic membranes, or Just what green band is that? Photosynth. Res. 15:3–32 Green BR, Camm EL. 1990. Relationship of Chl a/b-binding and related polypeptides in PSII core particles. In Current Research in Photosynthesis, ed. M Baltscheffsky, 1:659–62. Dordrecht: Kluwer Green BR, Durnford DG, Aebersold R, Pichersky E. 1992. Evolution of structure and function in the chlorophyll a/b antenna protein families. In Research in Photosynthesis, ed. N Murata, pp. 195–201. Dordrecht: Kluwer Green BR, Kühlbrandt W. 1995. Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosynth. Res. 44:139–48 Green BR, Pichersky E. 1994. Hypothesis for the evolution of three-helix Chl a/b and Chl a/c light-harvesting antenna proteins from two-helix and four-helix ancestors. Photosynth. Res. 39:149–62 Green BR, Pichersky E, Kloppstech K. 1991. The chlorophyll a/b-binding light-harvesting antennas of green plants: the story of an extended gene family. Trends Biochem. Sci. 16:181–86 Green BR, Salter AH. 1995. Light regulation of nuclear-encoded thylakoid proteins. In Molecular Genetics of Photosynthesis, ed. B Anderson, AH Salter, J Barber, pp. 75–103. Oxford: Oxford Univ. Press Green BR, Shen D, Aebersold R, Pichersky E. 1992. Identification of the poly-peptides of the major lightharvesting complex of photosystem II (LHC II) with their genes in tomato. FEBS Lett. 305:18–22 Grevby C, Sundqvist C. 1992. Characterization of light-harvesting complex in Ochromonas danica (Chrysophyceae). J. Plant Physiol. 140:414–20 Grossman AR, Manodori A, Snyder D. 1990. Light-harvesting proteins of diatoms: the relationship to the chlorophyll a/b binding proteins of higher plants and

710

74.

75.

76.

77.

78.

79.

80.

81.

82.

83.

84.

85.

GREEN & DURNFORD their mode of transport into plastids. Mol. Gen. Genet. 224:91–100 Grossman AR, Schaefer MR, Chiang GG, Collier JL. 1993. The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol. Rev. 57:725–49 Harrison MA, Nemson JA, Melis A. 1993. Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants. Photosynth. Res. 38:141–51 Hayashi H, Fujimura Y, Mohanty PS, Murata N. 1993. The role of CP-47 in the evolution of oxygen and the binding of the extrinsic 33-kDa protein to the core complex of photosystem-II as determined by limited proteolysis. Photosynth. Res. 36:35–42 Henrysson T, Schröder WP, Spangfort M, Akerlund H-E. 1989. Isolation and characterization of the chlorophyll a/b protein complex CP29 from spinach. Biochim. Biophys. Acta 977:301–8 Hiller RG, Anderson JM, Larkum AWD. 1991. The chlorophyll-protein complexes of algae. See Ref. 150a, pp. 529–47 Hiller RG, Wrench PM, Gooley AP, Shoebridge G, Breton J. 1993. The major intrinsic light-harvesting protein of Amphidinium: characterization and relation to other light-harvesting proteins. Photochem. Photobiol. 57:125–31 Hiller RG, Wrench PM, Sharples FP. 1995. The light-harvesting chlorophyll a-c-binding protein of dinoflagellates: a putative polyprotein. FEBS Lett. 363: 175–78 Hobe S, Foster R, Klingler J, Paulsen H. 1995. N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34:10224–28 Hobe S, Prytulla S, Kühlbrandt W, Paulsen H. 1994. Trimerization and crystallization of reconstituted light-harvesting chlorophyll a/b complex. EMBO J. 13: 3423–29 Holzenburg A, Bewley MC, Wilson FH, Nicholson WV, Ford RC. 1993. Threedimensional structure of photosystem II. Nature 363:470–74 Hoober JK, White RA, Marks DB, Gabriel JL. 1994. Biogenesis of thylakoid membranes with emphasis on the process in Chlamydomonas. Photosynth. Res. 39:15–31 Horton P, Ruban AV, Walters RG. 1996. Regulation of light-harvesting in

86.

87.

88. 89.

90. 91.

92.

92a.

93.

94.

95.

96.

97.

green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:655–84 Houlné G, Schantz R. 1988. Characterization of cDNA sequences for LHC I apoproteins in Euglena gracilis: the mRNA encodes a large precursor containing several consecutive divergent polypeptides. Mol. Gen. Genet. 213: 479–86 Iglesias-Prieto R, Govind NS, Trench RK. 1993. Isolation and characterization of 3 membrane-bound chlorophyll protein complexes from 4 dinoflagellate species. Philos. Trans. R. Soc. London Ser. B 340:381–92 Ikeuchi M. 1992. Subunit proteins of photosystem-I: mini review. Plant Cell Physiol. 33:669–76 Irrgang KD, Shi LX, Funk C, Schröder WP. 1995. A nuclear-encoded subunit of the photosystem II reaction center. J. Biol. Chem. 270:17588–93 Jansson S. 1994. The light-harvesting chlorophyll a/b binding proteins. Biochim. Biophys. Acta 1184:1–19 Jansson S, Andersen B, Scheller HV. 1995. Subunit organization of the higher plant photosystem I (PSI) holocomplex. See Ref. 116a, 3:385–88 Jansson S, Pichersky E, Bassi R, Green BR, Ikeuchi M, et al. 1992. A nomenclature for the genes encoding the chlorophyll a/b-binding proteins of higher plants. Plant Mol. Biol. Rep. 10:242–53 Jeffrey SW. 1989. Chlorophyll c pigments and their distribution in the chromophyte algae. In The Chromophyte Algae: Problems and Perspectives, ed. JC Green, BSC Leadbeater, WL Diver, pp. 13–36. Oxford: Clarendon Jennings RC, Garlaschi FM, Bassi R, Zucchelli G, Vianelli A, Dainese P. 1993. A study of photosystem-II fluorescence emission in terms of the antenna chlorophyll-protein complexes. Biochim. Biophys. Acta 1183:194–200 Jiao S, Fawley MW. 1994. A cDNA clone encoding a light-harvesting protein from Mantoniella squamata. Plant Physiol. 104:797–98 Jovine RVM, Johnsen G, Prezelin BB. 1995. Isolation of membrane bound light-harvesting-complexes from the dinoflagellates Heterocapsa pygmaea and Prorocentrum minimum. Photosynth. Res. 44:127–38 Karrasch S, Bullough PA, Ghosh R. 1995. The 8.5– angstrom projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J. 14: 631–38 Kim S, Pichersky E, Yocum CF. 1994.


98.

99.

100.

101.

102.

103.

104.

105.

106.

107.

108.

Topological studies of spinach 22-kDa protein of photosystem II. Biochim. Biophys. Acta 1188:339–48 Kim S, Sandusky P, Bowlby NR, Aebersold R, Green BR, et al. 1992. Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett. 314:67–71 Knoetzel J, Svendsen I, Simpson DJ. 1992. Identification of the photosystem-I antenna polypeptides in barley: isolation of 3 pigment-binding antenna complexes. Eur. J. Biochem. 206:209–15 Krauss N, Hinrichs W, Witt I, Fromme P, Pritzkow W, et al. 1993. 3Dimensional structure of system-I of photosynthesis at 6 angstrom resolution. Nature 361:326–31 Krol M, Spangfort MD, Huner NPA, Oquist G, Gustafsson P, Jansson S. 1995. Chlorophyll a/b-binding proteins, pigment conversions, and early lightinduced proteins in a chlorophyll b-less barley mutant. Plant Physiol. 107:873–83 Kroth-Pancic PG. 1995. Nucleotide sequence of two cDNAs encoding fucoxanthin chlorophyll a/c proteins in the diatom Odontella sinensis. Plant Mol. Biol. 27:825–28 Kruip J, Bald D, Boekema EJ, Rögner M. 1994. Evidence for the existence of trimeric and monomeric Photosystem I complexes in thylakoid membranes from cyanobacteria. Photosynth. Res. 40:279–86 Kühlbrandt W. 1994. Structure and function of the plant light-harvesting complex, LHC-II. Curr. Opin. Struct. Biol. 4:519–28 Kühlbrandt W, Wang DN, Fujiyoshi Y. 1994. Atomic model of plant lightharvesting complex by electron crystallography. Nature 367:614–21 Kwa SLS, Groeneveld FG, Dekker JP, Van Grondelle R, Van Amerongen H, et al. 1992. Steady-state and time-resolved polarized light spectroscopy of the green plant light-harvesting complex-II. Biochim. Biophys. Acta 1101: 143–46 Larkum AWD, Scaramuzzi C, Cox GC, Hiller RG, Turner AG. 1994. Lightharvesting chlorophyll c-like pigment in Prochloron. Proc. Natl. Acad. Sci. USA. 91:679–83 La Roche J, Henry D, Wyman K, Sukenik A, Falkowski P. 1994. Cloning and nucleotide sequence of a cDNA encoding a major fucoxanthin-, chlorophyll a/c–containing protein from the chrysophyte Isochrysis galbana: implications

109.

110.

111.

112.

112a.

113.

114.

115.

116a.

116a. 117.

118.

711

for evolution of the cab gene family. Plant Mol. Biol. 25:355–68 La Roche J, Partensky F, Falkowski P. 1995. The major light-harvesting chl binding protein of Prochlorococcus marinus is similar to CP43′, a chl binding protein induced by iron-depletion in cyanobacteria. See Ref. 116a, 1:171–74 Lee ALC, Thornber JP. 1995. Analysis of the pigment stoichiometry of pigment-protein complexes from barley (Hordeum vulgare): the xanthophyll cycle intermediates occur mainly in the light-harvesting complexes of photosystem I and photosystem II. Plant Physiol. 107:565–74 Lers A, Levy H, Zamir A. 1991. Coregulation of a gene homologous to early light-induced genes in higher plants and beta-carotene biosynthesis in the alga Dunaliella bardawail. J. Biol. Chem. 266:13698–705 Levy H, Gokhman I, Zamir A. 1992. Regulation and light-harvesting complex II association of a Dunaliella protein homologous to early light-induced proteins in higher plants. J. Biol. Chem. 267:18831–36 Lewin RA, ed. 1993. Origins of Plastids: Symbiogenesis, Prochlorophytes, and the Origins of Chloroplasts. New York: Chapman Hall Lichtlé C, McKay RML, Gibbs SP. 1992. Immunogold localization of photosystem I and photosystem II lightharvesting complexes in cryptomonad thylakoids. Biol. Cell 74:187–94 Livne A, Katcoff D, Yacobi YZ, Sukenik A. 1992. Pigment-protein complexes of Nannochloropsis sp. (Eustigmatophyceae): an alga lacking chlorophylls b and c. In Research in Photosynthesis, ed. N Murata, pp. 203–6. Boston: Kluwer Lyon MK, Marr KM, Furcinitti PS. 1993. Formation and characterization of two-dimensional crystals of photosystem II. J. Struct. Biol. 110:133–40 Machold O. 1991. The structure of lightharvesting complex II as deduced from its polypeptide composition and stoichiometry I: studies with Vicia faba. J. Plant Physiol. 38:678–84 Mathis P, ed. 1996. Photosynthesis: From Light to Biosphere. Dordrecht: Kluwer Matthijs HCP, van der Staay GWM, Mur LR. 1994. Prochlorophytes: the `other' cyanobacteria? See Ref. 24a, pp. 49–64 McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, et al. 1995. Crystal structure of an

712

119.

120.

121.

122.

123.

124.

125.

126.

127.

128.

128a. 129.

130.

GREEN & DURNFORD integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–21 Melis A. 1991. Dynamics of photosynthetic membrane composition and function. Biochim. Biophys. Acta 1058: 87–106 Michel H, Deisenhofer J. 1988. Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochemistry 27:1–7 Morishige DT, Thornber JP. 1994. Identification of a novel light-harvesting complex II protein (LHC IIc′). Photosynth. Res. 39:33–38 Morishige DT, Thornber JP. 1992. Identification and analysis of a barley cDNA clone encoding the 31-kilodalton LHC IIa (CP29) apoprotein of the lightharvesting antenna complex of photosystem II. Plant Physiol. 98:238–45 Muchhal US, Schwarzbach SD. 1992. Characterization of a Euglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll-a/b-binding protein of photosystem II. Plant Mol. Biol. 18:287–99 Mukerji I, Sauer K. 1993. Energy transfer dynamics of an isolated light harvesting complex of photosystem-I from spinach: time-resolved fluorescence measurements at 295-K and 77-K. Biochim. Biophys. Acta 1142:311–20 Nechushtai R, Cohen Y, Chitnis PR. 1995. Assembly of the chlorophyllprotein complexes. Photosynth. Res. 44: 165–81 Nitschke N, Rutherford AW. 1991. Photosynthetic reaction centres: variations on a common theme? Trends Biochem. Sci. 16:241–45 Norris BJ, Miller DJ. 1994. Nucleotide sequence of a cDNA clone encoding the precursor of the peridinin-chlorophyll a-binding protein from the dinoflagellate Symbiodinium sp. Plant Mol. Biol. 24:673–77 Nussberger S, Dörr K, Wang DN, Kühlbrandt W. 1993. Lipid-protein interactions in crystals of plant lightharvesting complex. J. Mol. Biol. 234: 347–56 Ort DT, Yocum CF, eds. 1996. Oxygenic Photosynthesis: The Light Reactions. Dordrecht: Kluwer Palenik B, Haselkorn R. 1992. Multiple evolutionary origins of prochlorophytes: the Chl b containing prokaryotes. Nature 355:265–67 Pålsson LO, Spangfort MD, Gulbinas V, Gillbro T. 1994. Ultrafast chlorophyll b chlorophyll a excitation energy transfer

131.

132.

133. 134.

135. 136.

137.

138.

139.

140.

141.

142. 143.

in the isolated light harvesting complex, LHC II, of green plants: implications for the organisation of chlorophylls. FEBS Lett. 339:134–38 Pålsson LO, Tjus SE, Andersson B, Gillbro T. 1995. Ultrafast energy transfer dynamics resolved in isolated spinach light-harvesting complex I and the LHC I-730 subpopulation. Biochim. Biophys. Acta 1230:1–9 Passaquet C, Lichtlé C. 1995. Molecular study of a light-harvesting apoprotein of Giraudyopsis stellifer (Chrysophyceae). Plant Mol. Biol. 29:135–48 Deleted in proof Passaquet C, Thomas JC, Caron L, Hauswirth N, Puel F, Berkaloff C. 1991. Light-harvesting complexes of brown algae: biochemical characterization and immunological relationships. FEBS Lett. 280:21–26 Paulsen H. 1995. Chlorophyll a/b-binding proteins. Photochem. Photobiol. 62: 367–82 Peter GF, Thornber JP. 1991. Biochemical composition and organization of higher plant photosystem-II lightharvesting pigment-proteins. J. Biol. Chem. 266:16745–54 Peter GF, Thornber JP. 1991. Biochemical evidence that the higher plant photosystem II core complex is organized as a dimer. Plant Cell Physiol. 32:1237–50 Pichersky E, Subramaniam R, White MJ, Reid J, Aebersold R, Green BR. 1991. Chlorophyll a/b binding (CAB) polypeptides of CP29, the internal chlorophyll a/b complex of PSII: characterization of the tomato gene encoding the 26-kDA (type I) polypeptide, and evidence for a second CP29 polypeptide. Mol. Gen. Genet. 227:277–84 Post AF, Bullerjahn GS. 1994. The photosynthetic machinery in prochlorophytes: structural properties and ecological significance. FEMS Microbiol. Rev. 13:393–413 Preiss S, Peter GF, Anandan S, Thornber JP. 1993. The multiple pigmentproteins of the photosystem-I antenna. Photochem. Photobiol. 57:152–57 Pyszniak AM, Gibbs SP. 1992. Immunocytochemical localization of photosystem-I and the fucoxanthinchloro- phyll a/c light-harvesting complex in the diatom Phaeodactylum tricornutum. Protoplasma 166:208–17 Raven PH. 1970. A multiple origin for plastids and mitochondria. Science 169: 641–46 Reith M. 1995. Molecular biology of rhodophyte and chromophyte plastids.


144.

145.

146.

147.

148.

149.

150.

150a. 151.

152.

153.

154.

Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:549–75 Rhiel E, Lange W, Mörschel E. 1993. The unusual light-harvesting complex of Mantoniella squamata: supramolecular composition and assembly. Biochim. Biophys. Acta 1143:163–72 Rhiel E, Mörschel E. 1993. The atypical chlorophyll a/b/c light-harvesting complex of Mantoniella squamata: molecular cloning and sequence analysis. Mol. Gen. Genet. 240:403–13 Ruban AV, Horton P. 1992. Mechanism of delta pH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. 1. Spectroscopic analysis of isolated light-harvesting complexes. Biochim. Biophys. Acta 1102:30–38 Ruffle SV, Donnelly D, Blundell TL, Nugent JHA. 1992. A threedimensional model of the photosystem II reaction centre of Pisum sativum. Photosynth. Res. 34:287–300 Santini C, Tidu V, Tognon G, Magaldi AG, Bassi R. 1994. Three-dimensional structure of the higher-plant photosystem II reaction centre and evidence for its dimeric organization in vivo. Eur. J. Biochem. 221:307–15 Satoh K. 1993. Isolation and properties of the photosystem II reaction center. In The Photosynthetic Reaction Center, ed. J Deisenhofer, JR Norris, 1:289–318. San Diego: Academic Sayre RT, Wrobelboerner EA. 1994. Molecular topology of the photosystem II chlorophyll alpha binding protein, CP 43: topology of a thylakoid membrane protein. Photosynth. Res. 40:11–19 Scheer H, ed. 1991. Chlorophylls. Baton Rouge, LA: CRC Press Schelvis JPM, Germano M, Aartsma TJ, Van Gorkom HJ. 1995. Energy transfer and trapping in photosystem II core particles with closed reaction centers. Biochim. Biophys. Acta 1230:165–69 Schmitt A, Frank G, James P, Staudenmann W, Zuber H, Wilhelm C. 1994. Polypeptide sequence of the chlorophyll a/b/c-binding protein of the prasinophycean alga Mantoniella squamata. Photosynth. Res. 40:269–77 Schmitt A, Herold A, Welte C, Wild A, Wilhelm C. 1993. The light-harvesting system of the unicellular alga Mantoniella squamata (Prasinophyceae): evidence for the lack of a photosystem I–specific antenna complex. Photochem. Photobiol. 57:132–38 Schubert WD, Klukas O, Krauss N, Saenger W, Fromme P, Witt HT. 1996. Present state of the crystal structure

155.

156.

157.

158. 159.

160.

161. 162.

163.

164.

165.

166.

713

analysis of photosystem I. See Ref. 116a, 2:3–10 Seibert M. 1993. Biochemical, biophysical, and structural characterization of the isolated photosystem II reaction center complex. In The Photosynthetic Reaction Center, ed. J Deisenhofer, JR Norris, 1:319–56. San Diego: Academic Seibert M. 1995. Reflections on the nature and function of the photosystem II reaction centre. Aust. J. Plant Physiol. 22:161–66 Sigrist M, Staehelin LA. 1994. Appearance of Type 1, 2, and 3 light-harvesting complex II and light-harvesting complex I proteins during light-induced greening of barley (Hordeum vulgare) etioplasts. Plant Physiol. 104:135–45 Straus NA. 1994. Iron deprivation: physiology and gene regulation. See Ref. 24a, pp. 731–50 Sukenik A, Livne A, Neori A, Yacobi YZ, Katcoff D. 1992. Purification and characterization of a light-harvesting chlorophyll-protein complex from the marine Eustigmatophyte Nannochloropsis sp. Plant Cell Physiol. 33:1041–48 Sulli C, Schwartzbach SD. 1995. The polyprotein precursor to the Euglena light-harvesting chlorophyll a/b-binding protein is transported to the Golgi apparatus prior to chloroplast import and polyprotein processing. J. Biol. Chem. 270:13084–90 Sundqvist C, Ryberg M. 1993. PigmentProtein Complexes in Plastids: Synthesis and Assembly. New York: Academic Thornber JP, Morishige DT, Anandan S, Peter GF. 1991. Chlorophyll-carotenoid protein of higher plant thylakoids. See Ref. 150a, pp. 549–85 Thornber JP, Peter GF, Morishige DT, Gomez S, Anandan S, et al. 1993. Light harvesting in photosystem-I and photosystem-II. Biochem. Soc. Trans. 21:15–18 Tjus SE, Roobol-Boza M, Pålsson LO, Andersson B. 1995. Rapid isolation of photosystem I chlorophyll-binding proteins by anion exchange perfusion chromatography. Photosynth. Res. 45:41–49 Tronrud DE, Schmid MF, Matthews BW. 1986. Structure and x-ray amino acid sequence of a bacteriochlorophyll a protein from Prosthecochloris aestuarii refined at 1.9 Å resolution. J. Mol. Biol. 188:443–53 Turconi S, Weber N, Schweitzer G, Strotmann H, Holzwarth AR. 1994. Energy transfer and charge separation kinetics in Photosystem I. 2. Picosecond fluorescence study of various PS I particles and light-harvesting complex iso-