Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold.

Chloroplasts and their nonphotosynthetic relatives in the plastid organelle family evolved from a cyanobacterial endosymbiont (for review, see Timmis et al., 2004). The subsequent coevolution of the chloroplast and nuclear genomes produced an organelle that is eubacterial at its core but with extensive chloroplastspecific embellishments. Of the thousands of genes in the cyanobacterial ancestor, only approximately 100 are retained in chloroplast genomes. These genes fall into three categories: those encoding (1) components of the chloroplast gene expression machinery (RNA polymerase, ribosomal proteins, tRNAs, and rRNAs), (2) subunits of photosynthetic enzymes (Rubisco, PSII, the cytochrome b6 f complex, PSI, the ATP synthase, and the NADH dehydrogenase), and (3) proteins involved in other metabolic processes (e.g. ClpP, AccD, Ycf1, and Ycf2). The chloroplast proteome has a complexity of several thousand proteins and is dominated by nuclear gene products that are synthesized in the cytosol and imported into the organelle. Many of these are encoded by genes of cyanobacterial ancestry that were transferred to the nucleus and that have retained their ancestral functions. As a result, the chloroplast gene expression and photosynthesis machineries consist of proteins that are derived from two physically separate genetic systems. Detailed knowledge of chloroplast gene expression and the nucleus-encoded proteins that influence it are prerequisites for understanding nuclear-organellar cross talk and chloroplast evolution, and will aid in optimizing transgene expression in the plastid compartment. The use of genetic and biochemical approaches, together with the ability to manipulate the chloroplast genome in several species, have brought most aspects of chloroplast gene expression out of the “black box” and into the realm of concrete, mechanistic hypotheses. The intent of this contribution is to highlight new perspectives that have resulted from recent observations and instances in which current data warrant the revision of previous paradigms. For more comprehensive information, I refer the reader to recent reviews of chloroplast RNA metabolism (Stern et al., 2010), transcription (Liere and Börner, 2007; Lerbs-Mache, 2010), and translation (PeledZehavi and Danon, 2007). Mechanisms of chloroplast gene expression have been studied primarily in land plants and in the green alga Chlamydomonas reinhardtii. Here, I emphasize findings with land plants, as detailed reviews of chloroplast gene expression in Chlamydomonas have been published in a recent volume (Stern and Harris, 2009).