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Tracing the Thread of Plastid Diversity Through the Tapestry of Life

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Tracing the Thread of Plastid Diversity Through the Tapestry of Life vol. 154, supplement the american naturalist october 1999 Tracing the Thread of Plastid Diversity through the Tapestry of Life Charles F. Delwiche* Departments of Cell Biology and Molecular Genetics and Biology, and Zeiger 1991). Hence, the general term ªplastidº is H. J. Patterson Hall, University of Maryland, College Park, more appropriate for the purposes of this article than is Maryland 20742-5815 ªchloroplast,º which refers to photosynthetic plastids, par- ticularly those of green algae and plants. The derivation of plastids from cyanobacteria is not in serious question, although, through force of habit, this is often referred to abstract: Plastids (chloroplasts) are endosymbiotic organelles de- as the endosymbiotic hypothesis. But while the cyanobac- rived from previously free-living cyanobacteria. They are dependent terial origin of plastids is well established (Delwiche et al. on their host cell to the degree that the majority of the proteins 1995), fundamental questions in plastid evolution, in- expressed in the plastid are encoded in the nuclear genome of the host cell, and it is this genetic dependency that distinguishes organ- cluding the number of independent origins of plastids, the elles from obligate endosymbionts. Reduction in the size of the plastid mechanisms by which the plastid was permanently incor- genome has occurred via gene loss, substitution of nuclear genes, porated into the host cell, and the relationships among and gene transfer. The plastids of Chlorophyta and plants, Rhodo- different plastid lineages, remain active areas of study (Del- phyta, and Glaucocystophyta are primary plastids (i.e., derived di- wiche et al. 1995; Gray and Spencer 1996; Van de Peer et rectly from a cyanobacterium). These three lineages may or may not al. 1996; Douglas 1998; Martin et al. 1998; Palmer and be descended from a single endosymbiotic event. All other lineages of plastids have acquired their plastids by secondary (or tertiary) Delwiche 1998). endosymbiosis, in which a eukaryote already equipped with plastids The most dramatic feature distinguishing plastids from is preyed upon by a second eukaryote. Considerable gene transfer free-living cyanobacteria is the tremendous reduction in has occurred among genomes and, at times, between organisms. The the size and gene content of plastid genomes (Martin and eukaryotic crown group Alveolata has a particularly complex history Herrmann 1998; Palmer and Delwiche 1998). While the of plastid acquisition. genome of the cyanobacterium Synechocystis PCC 6803 is Keywords: plastid, chloroplast, endosymbiosis, phylogeny, rubisco, 3,573 kb and contains about 3,200 genes (Kaneko et al. apicomplexa. 1996), that of the plastid of the red alga Porphyra purpurea is only 191 kb and contains roughly 250 genes (Reith and Munholland 1995). The genomes of plastids on the green Photosynthesis in eukaryotes is carried out by plastids, lineage that includes those of land plants are even more which are endosymbiotic organelles derived from cyano- reduced; the liverwort Marchantia polymorpha has a plastid bacteria (Mereschkowsky 1905). The most familiar kind genome of 121 kb and contains 120 recognized open read- of plastid is the plant plastid, but these represent only a ing frames (Ohyama et al. 1986; Shinozaki et al. 1986). tiny portion of the plastid diversity found among other This is comparable toÐor somewhat more complex photosynthetic eukaryotes (see Van den Hoek et al. 1995 thanÐthe plastid genomes of other land plants. It is this for an overview of the algae). A great diversity of algal reduction in the plastid genome, and the concomitant ab- plastids is evident by any measure, including structure, solute dependency of the plastid on the host cell, that pigmentation, gene content, and DNA sequence diver- distinguishes an endosymbiotic organelle from an obligate gence. Plastids are also the site for a number of biochemical endosymbiont (Cavalier-Smith and Lee 1985). The plastid tasks other than photosynthesis, including fatty acid and is not, however, as highly reduced in terms of protein amino acid biosynthesis, and not all are pigmented (Taiz complexity as the reduction in the size of the plastid ge- nome would suggest (Emes and Tobin 1993). Estimates of * E-mail: [email protected]. the number of proteins in plastids range from 500 to Am. Nat. 1999. Vol. 154, pp. S164±S177. q 1999 by The University of 5,000Ðin any case, a number that greatly exceeds the Chicago. 0003-0147/1999/15404S-0006$03.00. All rights reserved. complexity of any known plastid genome (Martin and The Thread of Plastid Diversity S165 Herrmann 1998). Those plastid proteins not encoded in membranes could also represent the two membranes of the plastid genome are encoded in the nuclear genome the gram-negative cyanobacterial cell. This view is bol- and must be targeted to the plastid. stered by the recent determination that Toc75, a key com- Three mechanisms underlie this reduction of the plastid ponent of the plant plastid's protein import apparatus, is genome; gene loss, substitution, and transfer. First, in the homologous to a cyanobacterial secretory protein, both case of gene loss, genes that no longer confer a selective localized to the outer plastid envelope (reported in two advantage in the endosymbiotic environment may be lost papers submitted within 5 d of each other: BoÈlter et al. outright. A probable example of such a loss is that of the 1998; Reuman et al. 1999). It is presumably possible for cyanobacterial cell wall, which is entirely lacking in most changes to occur in the localization of membrane proteins. plastid lineages (but see comments on the plastids in glau- However, the elaborate membrane structures present in cocystophytes in ªThree Lineages of Primary Plastidsº). some algae, particularly those with secondary plastids, im- In the second case, that of gene substitution, a gene plies that such changes do not occur very easily. Thus, the originally resident in the nuclear genome and expressed location of Toc75 may be a clue to the origin of the two in the cytosol may also have its product targeted to the membranes of the primary plastid. Toc75 seems to be an plastid. In such a case, the plastid and cytosolic versions essential protein and is present in all fully sequenced gram- of the protein are closely related and may be identical and negative bacterial genomes to date, which suggests that transcribed from a single locus, and, consequently, they this would be a useful protein to examine in Rhodophyta, are dif®cult to trace individually. For this reason, relatively Glaucocystophyta, and other algal groups. little information is available about this mechanism of gene The precise content of plastid genomes depends on the replacement, but it is likely to have had a signi®cant role lineage. Following the sequencing in the late 1980s of the in plastid evolution (Martin and Schnarrenberger 1997). plastid genomes of Nicotiana tabacum (tobacco) and M. The ®nal mechanism for reduction of the plastid ge- polymorpha (a liverwort), it was widely assumed that all nome is gene transfer. In this case, a plastid gene probably plastids would have roughly the same set of just over 100 ®rst undergoes a duplication event that results in a second genes. This view of plastids as genetically uniform entities copy of the gene resident in the nuclear genome, a process with genomes reduced to a bare minimum of genes has that is in at least some cases RNA mediated (Nugent and been displaced as information about the plastids of diverse Palmer 1991). If the gene product from the nuclear copy algal groups has become available (reviewed in Palmer and is then targeted into the plastid, the result is two redundant Delwiche 1998). The plastids of red algae and those of loci, one in the plastid genome and one in the nuclear glaucocystophytes are substantially larger and encode genome. Because these loci are redundant, selection will genes for a wider range of cellular functions than do those act to maintain one functional copy of the gene, but it is of green algae and plants. Although the genomes of all likely that one of the two will eventually undergo dele- photosynthetic plastids contain key genes involved with terious mutations and ultimately be lost entirely. If this gene expression and photosynthesis, the genomes of green occurs in the plastid genome, the gene has been transferred algal plastids contain few genes that are not involved with from the plastid to the nuclear genome. Note that such one of these processes. By contrast, the red algae, as evi- peripatetic genes are not limited to the nuclear genome; denced by P. purpurea, have plastid genes involved with for example, sequences originally of plastid origin have several biosynthetic pathways, nitrogen assimilation, pro- also been detected in the mitochondrial genome of plants tein transport and processing, and metabolic regulation; (Nugent and Palmer 1988). the Cyanophora paradoxa plastid genome is similarly elab- For a plastid gene to undergo successful transfer from orate and adds to its repertoire genes for biosynthesis of the plastid to the nuclear genome, it is essential that the both NAD1 and the peptidoglycan wall that is distinctive gene product be targeted back to the plastid. This is ef- to glaucocystophyte plastids. Whether there is a functional fected by transit peptides, polypeptide leaders that direct difference between genes encoded in the plastid and those the gene product to the appropriate compartment. Plastids encoded in the nucleus but targeted to the plastid is not and mitochondria have distinct transit peptides, such that known. A useful survey of plastid gene content is presented gene products are selectively targeted to one or the other by Stoebe et al. (1998). endosymbiotic organelle. But, remarkably, the transit pep- tides of both red algal and land plant plastids seem to be Three Lineages of Primary Plastids functionally interchangeable (Apt et al.
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