Why genes persist in organelle genomes

The sequencing of both organelle and nuclear genomes from phylogenetically diverse species will help us to infer how these genomes have evolved and the forces that have shaped them. Recent findings of high rates of transfer of organelle DNA to the nucleus [1], and of high rates of functional gene transfer from organelles to the nucleus [2-5], demonstrate that the endosymbiotic origin of organelles was a major determinant in defining eukaryotic nuclear genomes and was probably a defining event for the formation of the eukaryotic cell [1,6]. Clearly there is an evolutionary pressure to centralize genetic information in the nucleus, but the forces behind this transfer are not obvious. Muller's ratchet - the unidirectional process of building up mutations in an asexually reproducing population - is one commonly suggested hypothesis to account for this centralization, but is limited in its ability to explain more 'recent' gene transfer events (reviewed in [5]). But despite a wealth of information, it is still not clear from genome sequencing why some genes remain encoded in organelles such as mitochondria and chloroplasts.A recent study in yeast [7] indicated that an astonishing 25% of the mitochondrial proteome (around 185 proteins) is required for the maintenance and expression of the eight polypeptides encoded by the mitochondrial genome. Analysis of the Arabidopsis mitochondrial and chloroplast proteomes indicates that a similar amount of cellular effort is required to maintain and express organelle genomes in plants [8,9]. In this article we address the perplexing question of why some genes in the small organelle genomes have been maintained when the majority have been relocated to the nucleus. Figure 1 shows the steps needed for a gene to transfer from the nucleus to the mitochondrion. Historical arguments to explain the retention of a core set of organellar genes fall into two broad categories: either the genes have been 'trapped' in the organelle, or they have be