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Annu. Rev. Plant Biol. 2002. 53:50321 DOI: 10.1146/annurev.arplant.53.100301.135212 Copyright c 2002 by Annual Reviews.
All rights reserved
COMPLEX EVOLUTION OF PHOTOSYNTHESIS

Jin Xiong
Department of Biology, Texas A&M University, College Station, Texas 77843; e-mail: jxiong@mail.bio.tamu.edu
Annu. Rev. Plant Biol. 2002.53:503-521. Downloaded from arjournals.annualreviews.org by Universidad Nacional de Colombia on 03/20/09. For personal use only.
Carl E. Bauer
Department of Biology, Indiana University, Bloomington, Indiana 47405; e-mail: cbauer@bio.indiana.edu
Key Words phylogeny, bacteriochlorophyll, photosynthetic reaction center I Abstract The origin of photosynthesis is a fundamental biological question that has eluded researchers for decades. The complexity of the origin and evolution of photosynthesis is a result of multiple photosynthetic components having independent evolutionary pathways. Indeed, evolutionary scenarios have been established for only a few photosynthetic components. Phylogenetic analysis of Mg-tetrapyrrole biosynthesis genes indicates that most anoxygenic photosynthetic organisms are ancestral to oxygenevolving cyanobacteria and that the purple bacterial lineage may contain the most ancestral form of this pigment biosynthesis pathway. The evolutionary path of type I and type II reaction center apoproteins is still unresolved owing to the fact that a unied evolutionary tree cannot be generated for these divergent reaction center subunits. However, evidence for a cytochrome b origin for the type II reaction center apoproteins is emerging. Based on the combined information for both photopigments and reaction centers, a unied theory for the evolution of reaction center holoproteins is provided. Further insight into the evolution of photosynthesis will have to rely on additional broader sampling of photosynthesis genes from divergent photosynthetic bacteria. CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . GEOCHEMICAL EVIDENCE AND THEORIES FOR THE ORIGIN OF PHOTOSYNTHESIS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . EVOLUTION OF NONPHOTOSYNTHESIS-RELATED MOLECULAR MARKERS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . EVOLUTION OF MG-TETRAPYRROLE BIOSYNTHESIS . . . . . . . . . . . . . . . . . . . ORIGIN OF PHOTOSYNTHETIC REACTION CENTER APOPROTEINS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . EVOLUTIONARY PATHWAY OF REACTION CENTER APOPROTEINS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . UNIFIED MODEL FOR THE ORIGIN AND EVOLUTION OF REACTION CENTERS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . EVOLUTION OF OXYGENIC PHOTOSYNTHESIS . . . . . . . . . . . . . . . . . . . . . . . . . 1040-2519/02/0601-0503$14.00 504 505 507 508 511 513 515 516
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EVOLUTION OF THE CYTOCHROME BC COMPLEX . . . . . . . . . . . . . . . . . . . . . 517 EVOLUTION OF CAROTENOID BIOSYNTHESIS GENES . . . . . . . . . . . . . . . . . . 517 CONCLUDING REMARKS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 518
INTRODUCTION
Photosynthesis is a biological process that harvests solar energy for the formation of chemical bonds. The advent of photosynthesis, especially oxygenic photosynthesis, has fundamentally changed the landscape of Earth. Oxygen-evolving photosynthesis has generated most of the atmospheric oxygen that is used for respiration as well as formation of an ozone layer to shield Earth from UV radiation (1). Thus, the process of photosynthesis is arguably the most important chemical reaction on Earth that has led to the development of advanced life forms. There are two major speculations regarding the origin of photosynthesis (29, 30). One suggests that photosynthesis originated in a prebiotic environment on Earth and was coupled with the origin of life. The second, which is based on more recent molecular phylogenetic analyses, suggests that photosynthesis evolved after chemolithotrophy-based life was developed in the last common ancestor. However, the evolutionary history of how multiple biochemical components were incorporated in the photosynthetic process has long remained murky. The questions that remain in debate are: What is the earliest ancestor for photosynthetic organisms, what is its closest living descendent, and how did photosynthesis evolve into diverse lineages? Photosynthesis has been widely accepted as a bacterially derived process given that there are no Archaeal species that synthesize Mg-tetrapyrrole-based photosystems and that the photosynthetic properties of eukaryotes were acquired from cyanobacteria through endosymbiosis. Because photosynthesis evolved from bacteria, an understanding of the origin and evolution of photosynthesis requires detailed phylogenetic analysis of photosynthesis genes from the known bacterial branches that synthesize photosystems. These branches include (a) purple bacteria that synthesize a simplied, nonoxygen-evolving type II photosystem; (b) green nonsulfur bacteria that also synthesize a nonoxygen-evolving type II photosystem; (c) green sulfur bacteria that synthesize a type I photosystem with a homodimeric reaction center; (d ) the gram-positive heliobacteria that synthesize a similar homodimeric type I reaction center; and (e) cyanobacteria that contain both a type I photosystem and a more complex oxygen-evolving type II photosystem, both of which contain a heterodimeric reaction center core. This review covers recent evolutionary analyses of these ve photosynthetic lineages containing either one or two photosystem types. The goal is to reveal the complexity of the evolutionary pathway of photosynthesis, in which no simple linear branching scheme can be drawn to account for distribution of various photosynthetic components in diverse photosynthetic organisms. With a focus on Mg-tetrapyrrole biosynthesis enzymes and photosynthetic reaction center apoproteins, we discuss various scenarios derived from the use of advanced molecular phylogenetic methods for the early evolutionary history of the reaction centers.
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GEOCHEMICAL EVIDENCE AND THEORIES FOR THE ORIGIN OF PHOTOSYNTHESIS

Earth is over 4.5 giga-years (Gyrs) old (1 Gyr = 1 109 years) (26). During the rst 0.5 Gyr (Hadean stage), Earths environment was characterized by frequent and massive meteorite bombardment. Some of the impacts are thought to have been capable of evaporating the entire ocean. The Archean stage is characterized by the end of the bombardment and the beginning of life, probably starting approximately 3.8 to 4.0 Gyrs ago. The earliest Archean fossil stromatolites that contain evidence for biological carbon xation (38) are dated at 3.8 Gyrs old. The earliest cyanobacteria-like cellular microfossils are 3.5 Gyrs old (39, 40), only 0.3 Gyr after the rst record of life. However, Earth was beginning to be dominated by cyanobacteria starting 2.7 Gyrs ago, coinciding with the early rise of oxygen on Earth (9). Within approximately 1 Gyr, cyanobacteria increased the O2 level to approximately one fourth of the current level. The success of cyanobacteria was suggested to be due to not only the energetic advantage of photosynthesis, but also the inhibition of competitors through the creation of the potentially toxic agent O2 (27). The rst emergence of eukaryotes was 1.8 Gyrs ago. It took almost another 0.60.8 Gyr for photosynthetic cyanobacteria to be incorporated into eukaryotes as chloroplasts. Algae subsequently lifted the atmospheric oxygen to the current level. The descedents of algae, land plants, appeared on Earth 0.5 Gyrs ago, creating the landscape that we know today. Some of the major historical landmarks on Earth are depicted in Figure 1, with schematic representation of the rise of oxygen levels in atmosphere due to oxygenic photosynthesis. Because the origin of oxygenic photosynthesis is key to understanding the early evolution of photosynthesis, it is necessary to mention the current debate regarding the 3.5-Gyr-old cellular fossil record, which was determined to be of lamentous cyanobacterial origin. Based on this nding, it has been suggested that photosynthetic organisms were the earliest cellular organisms on Earth and that oxygenic photosynthesis started in the early Archean (30, 35). However, molecular analyses have suggested that the earliest forms of life may not be phototrophic, despite the energetic advantages of photosynthesis. In addition, the identication of the microfossils, which is based mainly on morphological resemblance to current microorganisms, presents its own challenges. Pierson (34) pointed out that the same morphological characteristics can be easily attributed to other lamentous nonoxygen-evolving phototrophs such as green nonsulfur bacteria, including Chloroexus, that are microscopically indistinguishable from many cyanobacteria. Controversies surrounding the biogenicity of certain specic microfossils and stromatolites also exist (5). Another problem with linking the microfossils to cyanobacteria is that it is impossible to determine whether the organisms in question really contained photosynthesis-related genes, especially in light of the pervasive lateral gene transfers that had occurred during early evolution of prokaryotes. (The mosaic and dynamic nature of bacterial genomes are discussed in detail below.) Because no denite geochemical evidence exists, tracing the origin of the biochemical process of photosynthesis using geological evidence alone will be difcult.
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Figure 1 Schematic representation of the rise of oxygen level on Earth during the early history of life [modied from (27)]. Major evolutionary landmarks are indicated by arrows on the lower x-axis, and major geological periods are indicated by brackets on the upper x-axis. Putative stages of early divergence of photosynthetic prokaryotes are indicated by brackets above the lower x-axis: one assumes 33.8 Gyrs and the other 3.53.8 Gyrs, depending on what date is accepted as the starting point for oxygenic photosynthesis.
There are many geologically oriented hypotheses regarding the origin of photosynthesis. The overall consensus appears to be that primitive photosynthetic pigments rst evolved from chemoautotrophic organisms living in an environment where local chemical disequilibrium can be easily exploited, leading to a capability of cells to use pigments to exploit light as an additional source of energy. Fulledged photosynthesis would develop later to allow cells to use sunlight as their sole energy source (26). A hypothesis was proposed by Nisbet et al. (25) suggesting that anoxygenic photosynthesis could have evolved from purple bacteria that used infrared phototaxis as an intermediate step. Based on a close match of the emission spectra of geothermal light and the absorption spectra of bacteriochlorophylls a and b, the authors suggested that photosynthesis arose from bacteriochlorophyll a- or b-containing organisms near oceanic hydrothermal vents where weak infrared radiation could be detected. They proposed that the organisms initially used the bacteriochlorophyll pigments to sense infrared light, which guided them in their phototaxis behavior. The bacteria capable of detecting geothermal light and phototaxis could preferentially occupy an optimum habitat, which may render
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them with evolutionary advantages in the competition for nutrient resources. Rudimentary photosynthesis would have subsequently evolved as a supplement to chemotrophy, giving the organisms an added selective advantage. Through further adaptation of a primitive photosystem, the organisms would start making use of the near-infrared part of sunlight when moving to shallow water. Eventually, chlorophylls would be developed to make use of higher energy (visible) light to split water. The hypothesis appears to be supported by the observation that purple bacteria are indeed capable of infrared phototaxis behavior (36). Furthermore, the amount of energy emitted from the geothermal light appears to be sufcient to drive photochemical reactions (45). The hypothesis also received support from our phylogenetic analysis (detailed below), suggesting that purple photosynthetic bacteria may indeed represent the rst group of organisms to evolve photosynthesis.
EVOLUTION OF NONPHOTOSYNTHESIS-RELATED MOLECULAR MARKERS

Owing to the difculty of using geochemical markers to trace the origin of photosynthesis, another approach to reconstruct the evolutionary history of photosynthesis is to use phylogenetic methods to analyze molecular sequence information. Before sequence information for a large number of photosynthesis genes was available, most phylogenetic analysis relied on the characterization of nonphotosynthesis genes. The most-often used phylogenetic marker is small subunit ribosomal rRNA (SS rRNA or 16S rRNA for prokaryotes). Several versions, with minor variations, of SS rRNA trees exist; all of which consistently place green nonsulfur bacteria as the earliest photosynthetic lineage (28, 32, 47), with heliobacteria branching off as the second photosynthetic lineage, followed by green sulfur bacteria, cyanobacteria, and then purple bacteria (proteobacteria). Gruber & Bryant (13) constructed phylogenetic trees using sigma 70 factor sequences within a large number of bacterial groups. They found that heliobacteria (Firmicutes) branch closer to proteobacteria than to cyanobacteria, which was very different from the branching patterns observed with 16S rRNA. Gupta et al. (14) used heat shock proteins (Hsp60 and Hsp70) as markers and concluded that the earliest evolving photosynthetic lineage is the heliobacterial group that subsequently diverged to green nonsulfur bacteria and then to cyanobacteria, green sulfur bacteria, and nally purple bacteria. The above controversies [see (50)] with the use of these nonphotosynthesis gene markers signicantly hindered the development of a clear picture of the evolutionary history of photosynthesis. These controversies also reinforced recent suggestions by various authors that lateral gene transfers played a major role in prokaryotic evolution (10, 17, 20). Thus, attempts to extrapolate the evolution of photosynthesis, which is a very ancient event, from the characterization of nonphotosynthesis genes may be a futile endeavor [for details see (50)].
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EVOLUTION OF MG-TETRAPYRROLE BIOSYNTHESIS

Genes and enzymes involved in (bacterio)chlorophyll biosynthesis are intimately involved in the evolutionary process of photosynthesis. Because these pigments are an integral part of the reaction centers, they are ideal molecular indicators for a wide-scale phylogenetic comparison of photosynthetic complexes. The biosynthetic enzymes are relatively conserved in sequence, structure, and function throughout all types of photosynthetic organisms and therefore readily reveal the ancient evolutionary history of the pigment biosynthesis. Recently, Xiong et al. (50, 51) conducted comprehensive sequence analysis of many pigment biosynthesis genes and enzymes from a variety of diverse photosynthetic bacteria in an effort to understand the molecular evolution of photosynthesis. Nine different bacteriochlorophyll biosynthesis genes and enzymes, one concatenated set of genes and enzymes of all prokaryotic photosynthetic groups, and several algal and plant taxa were analyzed (50). Phylogenetic trees were constructed using three major phylogenetic methods, i.e., distance neighbor joining (NJ), maximum parsimony (MP), and maximum likelihood (ML). The direction of evolution was resolved by rooting the trees with properly selected outgroup sequences. [An outgroup is a sequence that is homologous to the sequences under consideration but is found only in distantly related proteins or organisms and/or has diverged to a different function within the same organism (2).] For example, the nitrogenase complex was used as an outgroup for the light-independent protochlorophyllide reductase complex. In addition to sequence similarities, the two types of protein complexes have been experimentally veried as carrying out different but related enzymatic activities (11). For the Mg-chelatase complex, cobalt chelatase and putative nickel chelatase were used as an outgroup. All of these enzymes have related but modied functions in similar but distinct metabolic pathways. Using the rooted phylogenetic approach (mentioned above), Xiong et al. (50) observed that most bacteriochlorophyll-synthesizing anoxygenic photosynthetic bacterial groups evolved earlier than chlorophyll-synthesizing oxygenic photosynthetic groups. This implies that anoxygenic photosynthesis evolved prior to oxygenic photosynthesis. This conclusion is also supported by the ferrous iron oxidation experiment that shows that purple nonsulfur bacteria can naturally oxidize colorless Fe2+ to brown Fe3+ and reduce CO2 to cell material, implying that the Precambrian banded iron formations may be of anoxygenic origin (46). One surprise nding from the rooted phylogenetic analysis is that the purple photosynthetic group emerges as the earliest branching taxon. Another surprising nding is that green sulfur bacteria and green nonsulfur bacteria are sister groups that together form the second-earliest branching order on the phylogenetic tree. This result is striking in that these different green bacterial lineages contain vastly different photosystems, with green sulfur bacteria containing a type I photosystem and green nonsulfur bacteria containing a type II photosystem. Except for the fact that the two groups of organisms synthesize a common antenna pigment, bacteriochlorophyll
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c, and share a similar light-harvesting complex, the chlorosome, they are otherwise unrelated in many aspects of cellular metabolism (2). Xiong et al. (50, 51) also observed that heliobacteria form a sister group with cyanobacteria and the rest of the oxygenic photosynthetic taxa. The conclusion is equally striking in that, according to biochemical analyses, heliobacteria contain a far more primitive photosynthetic apparatus than any other known photosynthetic organisms (2). The heliobacterial reaction center contains a single pigment in a homodimer protein complex without any peripheral antenna complexes. Moreover, this sister relationship between heliobacteria and cyanobacteria is supported by other recent analysis on ribosomal protein genes (15) and cytochrome b proteins (41, 51). One of the major implications of these results is a reversal of the often-cited Granick hypothesis (12), which states that pigment biosynthesis recapitulates the evolutionary appearance of the pigment itself. As chlorophyll biosynthesis is one of the intermediate steps in bacteriochlorophyll a biosynthesis [see review in (43)], the Granick hypothesis of pigment biosynthesis can be interpreted to mean that chlorophyll-containing oxygenic photosynthetic organisms predate bacteriochlorophyll-containing anoxygenic photosynthetic organisms. However, molecular phylogeny clearly indicates that bacteriochlorophyll a is indeed a more ancient pigment. This implies that the chlorophyll acontaining cyanobacterial reaction centers are a more recent evolutionary product and that the evolution of pigment biosynthesis from bacteriochlorophylls to chlorophylls may have involved gene loss and shortening of the pathway, rather than stepwise additions. By comparing bacteriochlorophyll biosynthesis gene-based phylogeny with 16S rRNAbased phylogeny (32), it is clear that the evolutionary pathways of the two sets of genes are drastically different. This incongruence may be attributed to lateral gene transfer events for bacteriochlorophyll biosynthesis genes. With more and more prokaryotic genomes being sequenced, the chimeric or mosaic nature of their genomes is being recognized. In fact, lateral gene transfers may have so pervasively occurred among ancient prokaryotes that they may be the driving force of prokaryotic evolution (20). This supports the notion that a gene phylogeny in prokaryotes maximally reects the evolution of a metabolic process rather than the whole genome (50). As Doolittle (10) recently pointed out, the evolutionary history of life should be best represented by a mangrove-like network with many crossovers between branches, rather than by the well-known universal tree. Although directions of lateral gene transfers are often difcult to resolve, there are methods to address this issue. As further analysis of the evolution of (bacterio)chlorophyll biosynthesis genes, Xiong & Bauer (48) recently carried out a Baysian analysis (52) to infer ancestral sequences of (bacterio)chlorophyll biosynthesis genes at internal nodes of phylogenetic trees. The Baysian analysis (Figure 2) shows that the ancestral sequence for all in-group sequences indeed belongs to purple bacteria. The ancestral sequence at the node before the divergence of green bacteria and cyanobacteria/heliobacteria groups is the green sulfur bacterial lineage, whereas the nodal sequence before green sulfur and green nonsulfur is also
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Figure 2 Phylogenetic tree of BchL (top) with ancestral sequence (middle) at the common internal node (solid circle) inferred by Baysian analysis. Direction of lateral gene transfer is indicated below the sequence (bottom).
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green sulfur. The sequence before the divergence of cyanobacteria and heliobacteria indicates a closer relationship to cyanobacterial sequences. Thus, a more accurate route for the bacteriochlorophyll biosynthesis gene transfer is obtained (shown in Figure 2). The resolution of the direction of evolution by the Baysian analysis is largely consistent with the phylogenetic interpretation by Xiong et al. (50). The one surprising exception is that bacteriochlorophyll g synthesized by heliobacteria may have evolved from chlorophyll a of cyanobacteria. This is an interesting observation given that the two pigments have highly related structures, with the only difference between bacteriochlorophyll g and chlorophyll a being an isomerization of the double bond at ring II, which occurs spontaneously in bacteriochlorophyll g upon exposure to air. With the illustration of signicant lateral gene transfer events among prokaryotic genomes and the phylogenetic consensus that purple bacteria are the earliest photosynthetic group, a rethinking of the signicance of the 3.5-Gyr-old cyanobacterialike microfossils is warranted. Indeed, linking microfossil morphology with no information about the metabolic nature of the object is problematic. This is because genomes from ancient cyanobacteria-like fossils may not have encoded any photosynthesis genes at the 3.5-Gyr period.
ORIGIN OF PHOTOSYNTHETIC REACTION CENTER APOPROTEINS

In addition to Mg tetrapyrroles, another key part of the photosynthetic apparatus is the photosynthetic reaction center apoproteins. The origin and evolutionary pathway of the photosynthetic reaction center apoproteins has long been the subject of debate. This is mainly owing to the lack of obvious sequence similarity between type I and type II reaction center apoproteins. Based on similarity in photochemical charge separation of both types of reaction centers, it was proposed that both reaction centers may have derived from a common origin (1, 22). More-rened structural analysis of the two types of reaction centers supported the proposal that both types I and II of reaction centers are homologous. Schubert et al. (42) have shown that both reaction centers have a common structural motif with similar topology for transmembrane helices and cofactor arrangement. The most-recent high-resolution crystal structures of both type I and type II reaction centers conrmed signicant conservation in the topology of transmembrane helices as well as of the positions of the core Mg-tetrapyrrole photopigments (18, 53). The structural data have often been interpreted as evidence that these two reaction centers most likely evolved from a common origin. However, despite signicant structural conservation, the lack of primary sequence conservation between the type I and type II reaction center apopolypeptides still calls into question the possibility of convergent evolution (51). In addition, the nature of the common ancestor for the reaction center apoproteins remains unresolved.
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Because a unied reaction center apopolypeptide phylogeny that includes all photosynthetic lineages cannot be generated, there have been several biochemically oriented hypotheses proposed regarding the origin of the reaction centers. Mulkidjanian & Junge (24) suggested that a putative 11-transmembrane helix protein providing a UV protection role may be an ancestor for the reaction centers. Because of the unclear nature of the proposed UV protector, this hypothesis has remained unsupported. Meyer (23) suggested that photosynthetic reaction centers may have originated from the cytochrome b subunit of the cytochrome bc1 complex. This proposal was based on the observation that both types of proteins are membrane spanning, with bound tetrapyrroles and quinones functioning in electron transfers. However, because this hypothesis lacks supporting evidence based on sequence analysis, it has not been broadly accepted. In our own analysis (J. Xiong & C. Bauer, submitted), we discovered that type II reaction center core polypeptides share weak sequence similarity with cytochrome b of the bc1 complex. Further rened analysis revealed a region of high similarity, which includes three contiguous transmembrane helices (B, C, and D) of cytochrome b that bind two hemes and three contiguous transmembrane helices (B, C, and D) of type II reaction centers that bind cofactors such as (bacterio)chlorophylls, (bacterio)pheophytin, quinone, and a nonheme iron. The core regions with 130 residues show a sequence identity of 2030% between the two groups. Furthermore, three of the four heme ligands in cytochrome b are conserved with the cofactor ligands in the reaction center polypeptides [the special pair (bacterio)chlorophyll histidine ligand, the nonheme iron histdine ligand, and the chlorophyllZ ligand (for oxygenic reaction center only)]. In addition, there is relatively strong statistical support from PRSS tests (33) for sequence comparison and DALI search (16) for structural comparison for the two groups of membrane proteins. Recent studies have shown a ubiquitous existence of cytochrome b and the Rieske iron-sulfur protein, essential components of the cytochrome bc complex, in Archaea, Bacteria, and Eukarya (41). Phylogenetic analyses of several electron transfer proteins related to aerobic respiration (7, 8, 41) also indicate that many respiratory components including the cytochrome bc complex and cytochrome c oxidase may have existed in the last common ancestor of Archaea and Bacteria. In contrast, Mg-tetrapyrrole-based photosystems are found in Bacteria only, inclusive of the chloroplast lineage, and are therefore less likely to have existed in the common ancestor of both Archaea and Bacteria. This nding led to the proposal that photosynthetic metabolism must have appeared after the advent of respiratory metabolism (6). Nitschke et al. (27) further proposed that photochemical reaction centers may have evolved by integrating into an existing respiratory electron transport chain. The evidence for the existence of respiratory components prior to photosynthetic ones is contrary to the common belief that oxygenic photosynthesis must precede respiration because the respiratory process requires oxygen as a substrate. However, the primitive form of cytochrome bc complex may have performed either an anaerobic type of respiration for energy conversion or, as
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recently suggested, an aerobic type of respiration in the presence of an extremely low level of oxygen in a primitive Earth environment (19, 37) that was resulted from photolysis of water molecules.
EVOLUTIONARY PATHWAY OF REACTION CENTER APOPROTEINS

Although structural similarities of the type I and type II reaction centers provide a convincing argument for a common evolutionary ancestor, it is impossible to infer phylogenetic relationships between the type I and type II bacterial photosynthetic reaction center apoproteins owing to extensive sequence divergence. Previous analysis on the evolutionary pathways of reaction centers has been thus largely based on subunit composition and functionality. There are three competing models to account for the evolutionary paths of the two types of reaction centers in oxygenic cyanobacteria. One is the selective-loss model by Olson & Pierson (31), which suggests that both types of photosystem were developed from a single cyanobacterial origin. Subsequent loss of one of the photosystem types during evolutionary diversication would give rise to the existing single reaction center types in anoxygenic photosynthetic lineages. Another model is the fusion model (1, 22), which suggests that a primordial homodimeric photosystem would give rise to either type I or type II anoxygenic photosynthetic reaction centers. Subsequent fusion or arrival of these two types of anoxygenic photosystems in a single organism and the development of water-oxidizing capabilities would give rise to the current oxygenic cyanobacterial photosystems. A third model was put forward by Vermaas (44), suggesting that a homodimeric anoxygenic type I reaction center is the common ancestor to all of the current reaction centers. According to this model, the cyanobacterial reaction centers would have been derived from duplication and fragmentation of an ancestral type I reaction center. The purple bacterial reaction center would be the latest development through a subsequent selective loss of the type I photosystem in the cyanobacterial lineage. For this review, we carried out new phylogenetic analysis for both types of reaction center core proteins. To help determine what the rst reaction center was like at the protein sequence level, we calculated the ancestral sequences using Baysian analysis (52). The reconstructed ancestral sequence at the internal node for the type II reaction centers (Figure 3A) is shown to be a purple bacterial L subunit-like protein. Thus, a simplied scenario for the type II reaction center gene ow appears to be a diversication from purple bacteria to both green nonsulfur and cyanobacterial lineages. Similar analysis for type I reaction centers indicates that the ancestral sequence belongs to the heliobacterial type (Figure 3B), suggesting that both green nonsulfur and the cyanobacterial type I reaction center are results of diversication from a primitive heliobacterial reaction center. The analysis result does not come as a complete surprise as the nding that the heliobacterial reaction center, with
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Figure 3 Phylogenetic trees for type II (A) and type I (B) reaction centers (top). Calculated ancestral sequences (middle) at common ancestral nodes (solid circles) are shown below the trees. Only partial ancestral sequence for type II reaction centers was derived using a rened and reliable alignment region for type II reaction center proteins and cytochrome b. Direction of lateral gene transfer for both types of photosynthetic reaction centers are indicated below the sequences (bottom).
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no known antenna complexes (2), is the most primitive photosynthetic apparatus. However, a paradox exists given that heliobacteria also appear to contain the most recently acquired Mg-tetrapyrrole biosynthesis genes. These paradoxal observations underscore the difculty in unraveling photosynthesis evolution, which involves components that contain different evolutionary paths. Our ancestral sequence analysis supports the fusion model as well as a derivative of that model presented by Xiong et al. (51). Our current analysis is clearly in disagreement with the selective-loss model because the two types of cyanobacterial reaction center apoproteins are developed from two different anoxygenic sources. It is also in disagreement with the model by Vermaas because the cyanobacterial type II reaction center is not ancestral to the purple bacterial reaction center. If both types of reaction centers indeed share a common ancestry (18, 42, 53), the type II purple bacterial reaction center may be more ancestral relative to the type I reaction center because the type II reaction center is more closely related to the putative cytochrome b origin. In this scenario, the type I reaction center would be a result of gene fusion for a type II reaction center and ancestral CP43/CP47 proteins. Close sequence similarity of photosystem (PS) II antenna proteins CP43/CP47 with the light-harvesting domain of type I reaction centers has been demonstrated by Vermaas (44) and Xiong et al. (51). Structural similarities between CP43/CP47 and the light-harvesting domain of PSI have been veried by high-resolution crystal structures of both types of photosynthetic reaction centers (18, 53).
UNIFIED MODEL FOR THE ORIGIN AND EVOLUTION OF REACTION CENTERS

In an attempt to reconcile the differences between the evolutionary pathways for Mg tetrapyrroles and for reaction center apoproteins, we further proposed an apoprotein-early hypothesis (J. Xiong & C. Bauer, submitted). The proposal was based on combined analysis results showing that almost all photosynthetic groups independently received pigment biosynthesis genes and reaction center apoprotein genes from at least two different sources. It is almost impossible for both sets of genes to have arrived at a given lineage at the same time. This raises the question of which set of genes, the reaction center genes or Mg-tetrapyrrole genes, would have arrived rst. We propose that Mg-tetrapyrrole biosynthesis genes may have evolved in organisms containing preexisting reaction center apoproteins that may have still functioned as cytochromes. This hypothesis is also augmented by the argument that if Mg tetrapyrroles had arrived alone without polypeptides to bind Mg tetrapyrroles that assist in photochemistry, then there would be a waste of cellular resources for biosynthesis and, more importantly, a generation of damaging free radicals by photoexcitation, which would be highly detrimental to the cells survivala clearly unfavorable and unlikely evolutionary outcome. The combined evolutionary information for both reaction centers and Mg tetrapyrroles allowed us to construct a unied theory for the evolution of reaction
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center holoproteins (Figure 4). In this hypothesis, we propose that an initial gene duplication event for cytochrome b gave rise to a cytochrome that became the precursor of a type II reaction center apoprotein. Once Mg tetrapyrroles evolved, the cytochrome blike primitive form of the reaction center apoprotein would then combine with Mg tetrapyrroles to become a functional reaction center holoprotein. For Mg-tetrapyrrole biosynthesis, the pigment biosynthesis genes may have rst derived from the purple photosynthetic bacterial lineage, making purple bacteria the most ancestral photosynthetic form. The pigment biosynthesis genes would then have been transferred to green sulfur bacteria and then bifurcated to both green nonsulfur bacteria and cyanobacteria and eventually to heliobacteria, making bacteriochlorophyll g the latest development of photosynthetic pigment. Although heliobacteria received the photopigment last, they may have developed the earliest type I reaction center through a gene fusion process of genes for the type II reaction center protein and ancestral CP43/CP47 proteins. For cyanobacteria to perform oxygenic photosynthesis with both types of reaction centers, their type II reaction center apoproteins would have been laterally transferred from the purple bacterial lineage; their type I reaction center apoproteins would have been derived from the heliobacterial lineage. In all cases, the aforementioned reaction center as cytochrome b scenario would apply before the bacterial lineages received Mg tetrapyrroles.
EVOLUTION OF OXYGENIC PHOTOSYNTHESIS

The development of oxygenic photosynthesis was one of the most important events in Earths history as it fundamentally changed the redox balance on Earth and permitted development of aerobic metabolism and more-advanced life forms (2). As discussed above, oxygenic photosynthesis is likely a late event during evolution that was preceded by anoxygenic photosynthesis. The key in developing oxygenic photosynthesis is the development of the manganese complex that is capable of water oxidation. Blankenship & Hartman (3) have proposed that hydrogen peroxide (H2O2) may be a transitional donor to PSII before water was used as an electron donor. This mechanism may have been developed rst as a means to detoxify excess peroxide. The authors (3) also proposed that the proteinaceous portion of PSII involved in binding the manganese cluster may have developed through domain swapping with catalase. This proposal is based on the observation that photosynthetic water oxidation is mechanistically similar to that of catalases involved in breaking down H2O2 to water and oxygen. Specically, they observed that the binuclear Mn center in catalase is similar to one half of the tetranuclear Mn center within the water oxidation complex. Indeed, under certain conditions, the PSII water oxidation complex can act as a catalase. The redox potential for oxidation of H2O2 to O2 is +0.27 V, which is lower than the oxidation of purple bacterial reaction center P870 to P870+ at +0.5 V. Although this theory is interesting, it lacks geochemical support showing that there was indeed a signicant
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amount of H2O2 on Earth (30). There is also no phylogenetic or structural evidence for relatedness between catalase and the water oxidation complex.
EVOLUTION OF THE CYTOCHROME BC COMPLEX

Many types of cytochromes are involved in photochemistry either directly or indirectly. The cytochrome bc complex appears to be conserved among all ve photosynthetic groups and is involved intimately in the photosynthetic process. A recent review on the early evolution of cytochrome bc complexes was provided by Sch utz et al. (41) in which the primary structures, functional characteristics, and phylogenetic positions of subunits of cytochrome bc complexes from diverse bacterial and Archaeal groups were analyzed. Similar comparison was also made by Xiong et al. (51). Both groups observed interesting differences in the physical organization of the structural genes in various organisms. For example, in the cytochrome bc complex of green sulfur bacteria, cytochrome b is a fusion protein of cytochrome b6 and subunit IV, whereas in heliobacteria the two proteins are encoded by two separate but linked open reading frames. In nonphotosynthetic Bacillus subtilis, subunit IV, whose gene is downstream of the cytochrome b gene, is instead fused with cytochrome c. The phylogenetic tree topology from both studies share many similarities, though the work of Sch utz et al. (41) includes more phylogenetic taxa and provides a case of lateral gene transfer of cytochrome b from proteobacteria to Aquifex. The conserved nature of subunits of the cytochrome bc complex and its ubiquitous presence in all photosynthetic lineages appear to t the criteria for them to be used for wide-scale phylogenetic comparisons. However, these molecular markers suffer from not being able to truly represent the photosynthetic process as the cytochrome bc complex is found in most nonphotosynthetic taxa where it is involved in the respiratory electron transport chain. Cytochrome bc genes are thus arguably no more effective than 16S rRNA as a molecular marker for tracing the evolution of photosynthesis.
EVOLUTION OF CAROTENOID BIOSYNTHESIS GENES

Carotenoids are found in reaction centers and light-harvesting complexes where they fulll the light-harvesting and free-radical scavenging roles. However, carotenoids are not unique to photosynthesis and are synthesized ubiquitously in all three domains, Bacteria, Archaea, and Eukarya, serving as retinoid components, hormones, and membrane components. There are few evolutionary studies involving carotenoid biosynthesis genes. Boucher & Doolittle (4) as well as Lange et al. (21) surveyed enzymes for isoprenoid biosynthesis among a large number of eubacterial species. The reconstructed evolutionary history of the enzymes bears
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no resemblance with other known phylogenies. All results have clearly indicated that lateral gene transfer events have contributed to the early distribution of the carotenoid biosynthesis genes across the prokaryotic genomes (4, 21). Although the antiquity and wide distribution of carotenoids may shed light on early cell evolution, owing to their secondary role in photosynthesis, carotenoid biosynthetic enzymes may be of less value in determining the early evolutionary routes in photosynthesis.
CONCLUDING REMARKS
The overall evolution of photosynthesis is a complex process involving distinct origins and pathways of many different components. Consequently, the evolutionary development of photosynthesis cannot be described by a simple, linear branching pathway. Evidence has shown that various photosynthetic components have distinctively different evolutionary histories, indicating that these components may have been recruited or modied from several other preexisting metabolic pathways during different stages of evolutionary development (2). Although photosynthesis as a mosaic process appears to have no single well-dened origin, what is certain is that the emergence of Mg tetrapyrroles and reaction center apoproteins was the key event that led to the advent of photosynthesis (1). The evolution of (bacterio)chlorophyll pigments may be a limiting step in the overall evolution of reaction center holoprotein (48, 50). Thus, the evolutionary pathway of (bacterio)chlorophyll pigments provides a unied view for both oxygenic and anoxygenic photosynthesis. One issue that has been satisfactorily solved with overwhelming support is that anoxygenic photosynthesis evolved prior to oxygenic photosynthesis (48, 50, 51). Despite recent developments, there are still many unresolved key issues within the evolution of photosynthesis, such as the precise nature of the earliest photosystems and how water-oxidizing capability evolved in cyanobacteria. Because of the inherent difculty of studying deep evolution and the presence of highly diversied photosynthetic components, we believe that new molecular insight on evolution of photosynthesis can only be obtained through larger sampling of photosynthesis genes in more diverse phototrophic organisms. With the increased pool of molecular data, in particular for photosynthesis genes, and with the use of more sophisticated phylogenetic analysis tools, a clearer picture of evolutionary history of photosynthesis will continue to emerge.
ACKNOWLEDGMENTS The work is supported by an NIH grant (GM53940) and an Arizona State University NASA astrobiology grant to C.E.B. as well as a faculty startup fund from Texas A&M University to J.X.
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Figure 4 Model of evolutionary pathway of photosynthetic reaction center holoproteins based on combined phylogenetic information for both reaction center apoproteins and Mg-tetrapyrrole biosynthesis enzymes. Green lines indicate the direction of evolution for pigment biosynthesis, yellow lines for reaction center apoproteins.
Annual Review of Plant Biology Volume 53, 2002
CONTENTS
FrontispieceA. A. Benson PAVING THE PATH, A. A. Benson NEW INSIGHTS INTO THE REGULATION AND FUNCTIONAL SIGNIFICANCE OF LYSINE METABOLISM IN PLANTS, Gad Galili SHOOT AND FLORAL MERISTEM MAINTENANCE IN ARABIDOPSIS,
Jennifer C. Fletcher
xii 1 27 45 67 109 131
NONSELECTIVE CATION CHANNELS IN PLANTS, Vadim Demidchik,

Romola Jane Davenport, and Mark Tester
REVEALING THE MOLECULAR SECRETS OF MARINE DIATOMS,

Angela Falciatore and Chris Bowler
ABSCISSION, DEHISCENCE, AND OTHER CELL SEPARATION PROCESSES,

Jeremy A. Roberts, Katherine A. Elliott, and Zinnia H. Gonzalez-Carranza
PHYTOCHELATINS AND METALLOTHIONEINS: ROLES IN HEAVY METAL DETOXIFICATION AND HOMEOSTASIS, Christopher Cobbett
and Peter Goldsbrough 159 183 203
VASCULAR TISSUE DIFFERENTIATION AND PATTERN FORMATION IN PLANTS, Zheng-Hua Ye LOCAL AND LONG-RANGE SIGNALING PATHWAYS REGULATING PLANT RESPONSES TO NITRATE, Brian G. Forde ACCLIMATIVE RESPONSE TO TEMPERATURE STRESS IN HIGHER PLANTS: APPROACHES OF GENE ENGINEERING FOR TEMPERATURE TOLERANCE, Koh Iba SALT AND DROUGHT STRESS SIGNAL TRANDUCTION IN PLANTS,
Jian-Kang Zhu
225 247 275 299
THE LIPOXYGENASE PATHWAY, Ivo Feussner and Claus Wasternack PLANT RESPONSES TO INSECT HERBIVORY: THE EMERGING MOLECULAR ANALYSIS, Andr e Kessler and Ian T. Baldwin PHYTOCHROMES CONTROL PHOTOMORPHOGENESIS BY DIFFERENTIALLY REGULATED, INTERACTING SIGNALING PATHWAYS IN HIGHER PLANTS, Ferenc Nagy and Eberhard Sch afer
329
vi
CONTENTS
vii
THE COMPLEX FATE OF -KETOACIDS, Brian P. Mooney, Jan A. Miernyk,

and Douglas D. Randall
MOLECULAR GENETICS OF AUXIN SIGNALING, Ottoline Leyser RICE AS A MODEL FOR COMPARATIVE GENOMICS OF PLANTS,
Ko Shimamoto and Junko Kyozuka
357 377 399
ROOT GRAVITROPISM: AN EXPERIMENTAL TOOL TO INVESTIGATE BASIC CELLULAR AND MOLECULAR PROCESSES UNDERLYING MECHANOSENSING AND SIGNAL TRANSMISSION IN PLANTS,
K. Boonsirichai, C. Guan, R. Chen, and P. H. Masson
421
RUBISCO: STRUCTURE, REGULATORY INTERACTIONS, AND POSSIBILITIES FOR A BETTER ENZYME, Robert J. Spreitzer
and Michael E. Salvucci 449 477 503 523
A NEW MOSS GENETICS: TARGETED MUTAGENESIS IN PHYSCOMITRELLA PATENS, Didier G. Schaefer COMPLEX EVOLUTION OF PHOTOSYNTHESIS, Jin Xiong and Carl E. Bauer CHLORORESPIRATION, Gilles Peltier and Laurent Cournac STRUCTURE, DYNAMICS, AND ENERGETICS OF THE PRIMARY PHOTOCHEMISTRY OF PHOTOSYSTEM II OF OXYGENIC PHOTOSYNTHESIS, Bruce A. Diner and Fabrice Rappaport INDEXES
Subject Index Cumulative Index of Contributing Authors, Volumes 4353 Cumulative Index of Chapter Titles, Volumes 4353
551
581 611 616
ERRATA
An online log of corrections to Annual Review of Plant Biology chapters (if any, 1997 to the present) may be found at http://plant.annualreviews.org/

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Annu. Rev. Plant Biol. 2002. 53:50321 DOI: 10.1146/annurev.arplant.53.100301.135212 Copyright c 2002 by Annual Reviews.

All rights reserved

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

GEOCHEMICAL EVIDENCE AND THEORIES FOR THE ORIGIN OF PHOTOSYNTHESIS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

EVOLUTION OF NONPHOTOSYNTHESIS-RELATED MOLECULAR MARKERS

EVOLUTION OF MG-TETRAPYRROLE BIOSYNTHESIS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

ORIGIN OF PHOTOSYNTHETIC REACTION CENTER APOPROTEINS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

EVOLUTIONARY PATHWAY OF REACTION CENTER APOPROTEINS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

UNIFIED MODEL FOR THE ORIGIN AND EVOLUTION OF REACTION CENTERS

EVOLUTION OF OXYGENIC PHOTOSYNTHESIS

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

EVOLUTION OF THE CYTOCHROME BC COMPLEX

EVOLUTION OF CAROTENOID BIOSYNTHESIS GENES

COMPLEX EVOLUTION OF PHOTOSYNTHESIS

Visit the Annual Reviews home page at www.annualreviews.org

Annual Review of Plant Biology Volume 53, 2002

xii 1 27 45 67 109 131

NONSELECTIVE CATION CHANNELS IN PLANTS, Vadim Demidchik,

REVEALING THE MOLECULAR SECRETS OF MARINE DIATOMS,

ABSCISSION, DEHISCENCE, AND OTHER CELL SEPARATION PROCESSES,

225 247 275 299

THE COMPLEX FATE OF -KETOACIDS, Brian P. Mooney, Jan A. Miernyk,

357 377 399

K. Boonsirichai, C. Guan, R. Chen, and P. H. Masson

581 611 616

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