The treasure trove of algal chloroplast genomes. Surprises in architecture and gene content, and their functional implications.

The completion of the chloroplast genome sequence of the chlorophyte alga Chlamydomonas reinhardtii in our laboratory has been announced recently (J. Maul, J. Lilly, and D.B. Stern, unpublished data; accession no. AF396929). Because C. reinhardtii is the most genetically and biochemically tractable eukaryotic model system for photosynthesis and chloroplast gene expression (for review, see Harris, 2001), it is appropriate to use this opportunity to reflect briefly upon the history of chloroplast genomics—and more importantly, to take a broad and futuristic view as the stage is set for structure/function studies at a level of detail only recently unimaginable. The first phase of chloroplast genomics culminated with the completion of the tobacco (Nicotiana tabacum) and liverwort (Marchantia polymorpha) chloroplast genome sequences in 1986. The present chapter has witnessed the discovery of new plastid-encoded traits, the use of plastids for foreign gene expression, and an appreciation of their diversity, particularly outside the vascular plants. Two major foci have emerged: functional studies, ranging from details of photosynthesis to gene expression and cell biology; and genomics, whose major goal is to obtain evolutionary and comparative information through sequence analysis. At present, complete genome sequences have been obtained from virtually all the major algal lineages, and the C. reinhardtii sequence and the Synechocystis sp. PCC 6803 genome, representing its presumed ancestor, are complete. We now envision a new chapter of chloroplast molecular genetics, where the evolutionary forces and intracellular mechanisms that shape genome architecture, gene expression, and ecological adaptation, are revealed. In this Update, we promote algal plastid genomes as an underutilized resource, particularly the completely sequenced ones, through a discussion of structural and coding diversity. Because the antecedents of land plants are thought to lie within the green algal lineage (Turmel et al., 1999a, 2002; Karol et al., 2001), algal plastid genomics also offers useful experimental guides for Arabidopsis, maize (Zea mays), and other model systems. Importantly, some algal cpDNAs have retained novel or key genes that are absent in land plant cpDNAs, which provides an opportunity to use them to determine gene function, instead of dealing with complex nuclear gene families and technical land mines. This leads us to advocate not only C. reinhardtii, but also other algae as useful and perhaps essential complements to plantbased studies of chloroplast biogenesis and leaf development.