Extensive Loss of RNA Editing Sites in Rapidly Evolving Silene Mitochondrial Genomes: Selection vs. Retroprocessing as the Driving Force

Article excerpt


Theoretical arguments suggest that mutation rates influence the proliferation and maintenance of RNA editing. We identified RNA editing sites in five species within the angiosperm genus Silene that exhibit highly divergent mitochondrial mutation rates. We found that mutational acceleration has been associated with rapid loss of mitochondrial editing sites. In contrast, we did not find a significant difference in the frequency of editing in chloroplast genes, which lack the mutation rate variation observed in the mitochondrial genome. As found in other angiosperms, the rate of substitution at RNA editing sites in Silene greatly exceeds the rate at synonymous sites, a pattern that has previously been interpreted as evidence for selection against RNA editing. Alternatively, we suggest that editing sites may experience higher rates of C-to-T mutation than other portions of the genome. Such a pattern could be caused by gene conversion with reverse-transcribed mRNA (i.e., retroprocessing). If so, the genomic distribution of RNA editing site losses in Silene suggests that such conversions must be occurring at a local scale such that only one or two editing sites are affected at a time. Because preferential substitution at editing sites appears to occur in angiosperms regardless of the mutation rate, we conclude that mitochondrial rate accelerations within Silene have "fast-forwarded" a preexisting pattern but have not fundamentally changed the evolutionary forces acting on RNA editing sites.

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IN the organelle genomes of land plants, a variable but often large number of sites undergo C-to-U RNA editing in which a cytidine is converted to uridine by deamination (Yu and Schuster 1995; Giege and Brennicke 1999). A generally much smaller number of sites undergo "reverse" U-to-C editing (Steinhauser et al. 1999). RNA editing is believed to be essential for organelle gene function in plants. Editing sites are preferentially located in protein genes and, within them, at first and second codon positions (Gray 2003). Editing at these sites generally results in the restoration of phylogenetically conserved (and presumably functionally constrained) amino acids in mitochondrial and chloroplast protein sequences (Gray and Covello 1993; Mower 2005; Yura and Go 2008). Therefore, there are obvious selective pressures for plants to maintain RNA editing in the short term. In contrast, the origin and long-term maintenance of RNA editing pose an evolutionary puzzle, as it is unclear what if any benefit this seemingly cumbersome process confers over direct encoding of the edited sequence in the genomic DNA. This puzzle mirrors broader evolutionary questions about the origin, maintenance, and function of a number of major features of gene and genome architecture (Lynch 2007).

Various adaptive effects of RNA editing have been proposed, including a role in gene regulation (Hirose et al. 1999; Farajollahi and Maas 2010), maintenance of alternative functional protein isoforms (Gott 2003; Farajollahi and Maas 2010), generation of genetic variation (Tillich et al. 2006; Gommans et al. 2009), optimization of genomic GC content (Jobson and Qiu 2008), nuclear control of selfish organelle genes (Burt and Trivers 2006), and mutational buffering (Borner et al. 1997). In humans, there is evidence for divergent functional roles for products of the edited and unedited forms of apolipoprotein B (Powell et al. 1987), but there is little evidence for the aforementioned adaptive mechanisms in plant organelles. Moreover, replacement of edited C's with T's at the genomic level appears to occur readily across lineages with no obvious detrimental effect (Shields andWolfe 1997;Mower 2008). Accordingly, neutral and nonadaptive models for the proliferation of RNA editing have also been proposed (Covello and Gray 1993; Fiebig et al. 2004; Lynch et al. 2006).

C-to-U RNA editing appears to have evolved in a recent common ancestor of land plants, but the frequency of editing varies dramatically across lineages and between genomes (Turmel et al. …