Plastids, Genomes, and the Probability of Gene Transfer

Abstract

In a snowball fight, the amount of snow that sticks to your coat depends on the number and size of snowballs that hit you and the stickiness of your coat. Much the same goes for the bombardment of nuclear genomes by organellar genes, according to genome sequence data published in GBE this week (Smith et al. 2011). The new findings suggest that organisms with more plastids per cell have a higher probability of undergoing plastid-to-nucleus DNA transfer than organisms with only one or a few plastids per cell. The report is consistent with the ‘‘limited transfer window’’ hypothesis for organelle-to-nucleus gene transfer, but the ramifications extend more generally to the processes that fashion eukaryotic chromosomes. The limited transfer window hypothesis was proposed by Barbrook et al. (2006) to explain why plastids in nonphotosynthetic organisms almost always retain a small genome. Both mitochondria and chloroplasts have lost the vast majority of their genes, through gene transfer to the nucleus, and by simple loss, retaining only those needed for the local control of chemiosmotic electron and proton transfer, according to the Colocation for Redox Regulation (CoRR) hypothesis (Allen 2003; Puthiyaveetil et al. 2008), recently backed by compelling evidence in chloroplasts (Shimizu et al. 2010). But although redox regulation is both necessary and sufficient to account for genes in chloroplasts and mitochondria, it cannot explain why plastids in nonphotosynthetic organisms retain genes. Specific biochemical reasons, such as heme synthesis and even protein synthesis for nearby mitochondria, may explain the retention of plastid DNA in particular cases (Barbrook et al. 2006), but do not offer a general explanation. The limited transfer window hypothesis does. Many protists, including the apicomplexan parasites such as Plasmodium (the malarial parasite) and algae such as Chlamydomonas, retain a single plastid. This makes gene loss much more difficult: lysis of the single plastid is likely to be lethal to the host cell as well as the plastid. The retention of plastid genes might therefore not reflect a need so much as ‘‘an inability to get them out,’’ as Barbrook et al. (2006) put it. This inability should be reflected not only in the retention of genes in plastids but also in a low rate of transfer of plastid genes to the nucleus—the fate of at least someDNA relinquished from lysed organelles. Although limited genomic evidence in 2006 was consistent with this prediction, Smith et al. (2011) report on 30 newly available genome sequences in diverse monoplastidic and polyplastidic species. These genome sequences unequivocally support the limited transfer window hypothesis. The findings are not inherently surprising, but the scale of the differences is striking and fits into a larger picture of genome bombardment. Species with multiple plastids have an average of 80 times more plastid sequences incorporated into the nuclear genome (nupts or nuclear plastid sequences) than monoplastidic species. Not only the number but the mean length of nuclear inserts is greater in polyplastidic species. The same goes for nuclear mitochondrial sequences (numts), as reported for some species by Smith et al. (2011) and in a larger study of numts by Hazkani-Covo et al. (2010). The content of nupts and numts therefore depends in part on what amounts to the number of snowballs thrown at the target. Two recent studies show how high this rate can be. numts, for example, accumulate within a single lifetime. In rats, real-time polymerase chain reaction quantification and fluorescence in situ hybridization demonstrate up to four times as many nuclear chromosomal insertions of two mitochondrial genes (COX III and 16S rRNA) in old versus young rats (Caro et al. 2010). This bombardment of mitochondrial genes may play a role in ageing, as seems to be the case in yeast. In Saccharomyces cerevisiae, the migration This article is linked to evr001