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Chloroplast Origin and Integration1 Chloroplast Origin and Integration1 Geoffrey I. McFadden* Plant Cell Biology Research Centre, School of Botany, University of Melbourne, Victoria 3010, Australia The origin of oxygenic photosynthesis must rank lope (12, 13). It has subsequently emerged that plants just after the origin of life itself as one of the most (and probably algae) have learned to operate these significant events in the history of life. The early transporters in reverse to “feed” their chloroplasts at photosynthesizers, which Bill Schopf has shown night or in organs underground. Norman Weeden were similar to modern cyanobacteria (32), made then recognized that the endosymbiont, in addition earth a nicer place to live by quietly cranking out to the gift of photosynthesis, was responsible for the oxygen over hundreds of millions of years. Having introgression of several other metabolic pathways established an ozone UV shield, the cyanobacteria into the host (38). Weeden’s insight was the spur for then entered into an extraordinary partnership with the ongoing characterization of the bacterial-type eukaryotic cells: They became chloroplasts. Equipped chloroplast pathways for amino acid biosynthesis, with chloroplasts, the early plants were ready to carotenoid biosynthesis, non-Shemin tetrapyrole bio- colonize the land and green the planet. This review synthesis, non-mevalonate isoprenoid biosynthesis, recounts major leaps in our understanding of chloro- and nitrate and sulfate assimilation. Weeden also plast evolution from the preceding 25 years. recognized that many of the genes for these processes must have undergone intracellular transfer from plastid to nucleus. ENDOSYMBIOSIS TRIUMPHS ONE RING TO RULE THEM...AND IN THE In 1975 the theory of endosymbiosis (which de- DARKNESS BIND THEM scribes the origins of mitochondria and plastids from eubacteria-like cells living within eukaryotic hosts) The advent of Sanger-style DNA sequencing was still hanging in the balance. Major players like opened the way to more ambitious projects. Oyha- Lawrence Bogorad (4) and Tom Cavalier-Smith (7) ma’s team (28) was first to sequence a chloroplast were weighing the merits of the autogenous (nonen- genome determining the 121,024 bp of the liverwort dosymbiotic) alternatives for chloroplasts against the Marchantia polymorpha chloroplast. The Japanese early compelling scenarios of Mereschkowsky and group’s work inspired numerous other chloroplast later Lynn Margulis. However, in the same year, an genome sequencing projects from which various pat- innovative paper from Linda Bonen and Ford terns, and a few surprises, have emerged. The March- Doolittle (5; which provided the first quantitative antia genome has proven to be a good general model. measure of similarities between T1 rRNA catalogues Typical chloroplast DNAs, including those of plants of cyanobacteria and chloroplasts) is now recogniz- and most algae, are circular with genes organized in able as the first ripple in a tidal wave of chloroplast operons. Plastid gene content varies from about 70 in molecular data that swept the autogenous origin hy- some non-photosynthetic plastids such as that of the pothesis away. malaria parasite (39) up to about 200 in red algae (30); Hans Ko¨ssel was one of the first to apply the re- plants typically have around 100 genes in the chlo- cently developed Maxan/Gilbert DNA sequencing roplast. Dinoflagellate algal chloroplasts are the only technology to chloroplasts. Primary and secondary example that so far seriously defy this trend, having structure of maize chloroplast rRNA was revealed to single gene mini-circles that encode only a handful of be more closely related to the bacterium Escherichia genes (40). One ring no longer binds them. coli than to equivalent genes in the nuclei of eu- The next major leap in the application of sequenc- karyotes (the yeast sequence only became available ing was the complete genome of the cyanobacterium to Ko¨ssel at the proof stage!), corroborating the en- of Synechocystis (20). The Japanese team identified dosymbiotic hypothesis (34). 3,229 genes, which provided a reference point for the Flu¨ gge and Heldt recognized that integration of the gene content of the chloroplast endosymbiont at the endosymbiont required a transporter for export of outset of endosymbiosis. For the first time we held a photosynthate and characterized a family of phos- list of genes with which the endosymbiont probably phate translocators located in the chloroplast enve- started. Comparisons of this list with the present content of plastid genomes issues some weighty 1 G.I.M. is supported by the Australian Research Council and is challenges. an International Scholar of the Howard Hughes Medical Institute. The genome sequences also provided an opportu- * E-mail [email protected]; fax 61–3–9347–1071. nity to compare gene synteny between chloroplasts 50 Plant Physiology, January 2001, Vol. 125, pp. 50–53, www.plantphysiol.org © 2001 American Society of Plant Physiologists Chloroplast Origin and Integration and bacteria. Conservation of large operons proved within the chloroplast prior to assembly of the ho- that chloroplast DNAs are reduced bacterial ge- loenzyme. Gregory Schmidt and colleagues (31) de- nomes (28). In a converse manner, unique gene as- termined the leader sequence and the site of process- semblages shared among all chloroplasts suggest that ing. Chua and Schmidt (9) and Highfield and Ellis all chloroplasts arose from a single primary endo- (19) subsequently demonstrated that the transloca- symbiosis (30), as first argued by Tom Cavalier-Smith tion into the chloroplast occurs post-translationally. (8). Many other studies now concur, but the idea is These experiments were important for two key rea- not universally accepted (23). Large amounts of se- sons: first, they showed that chloroplast targeting quence data have also allowed meta-analyses in was different to the “signal hypothesis” for cotrans- which multiple genes are used in determining more lational insertion into the endomembrane system, robust phylogenies (25). These trees are consistent and second, they were the germ of a system to dissect with the belief that the glaucophyte alga Cyanophora, the import process. By using in vitro translated pre- which has a blue-green chloroplast with a pepti- cursors in conjunction with isolated plastids it has doglycan wall, is one of the earliest diverging lines to been possible to manipulate the system experimen- contain a chloroplast. Meta-analysis also confirms tally to identify conditions required for transport and morphological clues suggesting that the prasino- components of the transport machinery. Mishkind et phyte Mesostigma is the closest living relative to the al. (27) demonstrated that the transit peptide was unicellular alga from which the land plants are de- sufficient and necessary for import of proteins. scended (22). Schrier et al. (33) and van den Broek et al. (37) estab- lished the use of transit peptides to direct foreign proteins into chloroplasts in transgenic plants, which INTRACELLULAR GENE TRANSFER AND paved the way for targeting of reporter proteins such PROTEIN TARGETING as the jellyfish green fluorescent protein. A key development in understanding the mecha- An important outcome of comparing the gene con- nisms of import was the identification of ATP as the tent of a cyanobacterium with that of chloroplasts is essential requirement for transport (16). This depen- the detailed reconstruction of genome reduction. dence was exploited to interrupt transfer, which en- When it was first established that nuclear genes en- abled the partially transferred precursor to be used as code some types of chloroplast proteins it became a tag (often through innovative use of cross linkers or clear that chloroplasts were genetically only semi- autonomous and had relinquished genes to their affinity motifs attached to the targeted protein) to hosts. The genome maps in conjunction with the recover components of the transport apparatus. Ap- phylogeny tell us that this process occurred in a proaches based on this strategy have identified nu- somewhat ad hoc manner, although certain classes of merous transport-related proteins (known as Tocs genes are apparently less amenable to transfer (25). and Tics) located in the inner and outer chloroplast Two intriguing questions are how many nuclear membranes such as the receptors (36) and the chan- genes service the chloroplast and are they all derived nel protein (24). from the endosymbiont cyanobacterium. The Arabi- The targeting of proteins within the confines of the dopsis genome project is beginning to allow us to chloroplast was first studied by Smeekens et al. (35). address these questions; early surveys indicate that They demonstrated that plastocyanin was targeted as many as 2,000 nuclear genes encode proteins with into the chloroplast stroma by a typical transit pep- plastid functions (1). The tagged mutagenesis pro- tide, but that a second signal, this time homologous gram also provides a means to assay the functions of to bacterial secretion peptides, directed the protein those genes whose products are predicted to be chlo- across the thylakoid membranes. In other words, the roplast targeted, but for which no obvious function is original bacterial mechanisms for targeting proteins apparent. across the inner membrane have been retained in The transfer of genes from chloroplast to nucleus chloroplasts, a phenomenon now termed “conserva- typically requires return passage of the gene product
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