Recent Acceleration of Plastid Sequence and Structural Evolution Coincides with Extreme Mitochondrial Divergence in the Angiosperm Genus Silene

Abstract

The angiosperm genus Silene exhibits some of the most extreme and rapid divergence ever identified in mitochondrial genome architecture and nucleotide substitution rates. These patterns have been considered mitochondrial specific based on the absence of correlated changes in the small number of available nuclear and plastid gene sequences. To better assess the relationship between mitochondrial and plastid evolution, we sequenced the plastid genomes from four Silene species with fully sequenced mitochondrial genomes. We found that two species with fast-evolving mitochondrial genomes, S. noctiflora and S. conica, also exhibit accelerated rates of sequence and structural evolution in their plastid genomes. The nature of these changes, however, is markedly different from those in the mitochondrial genome. For example, in contrast to the mitochondrial pattern, which appears to be genome wide and mutationally driven, the plastid substitution rate accelerations are restricted to a subset of genes and preferentially affect nonsynonymous sites, indicating that altered selection pressures are acting on specific plastid-encoded functions in these species. Indeed, some plastid genes in S. noctiflora and S. conica show strong evidence of positive selection. In contrast, two species with more slowly evolving mitochondrial genomes, S. latifolia and S. vulgaris, have correspondingly low rates of nucleotide substitution in plastid genes as well as a plastid genome structure that has remained essentially unchanged since the origin of angiosperms. These results raise the possibility that common evolutionary forces could be shaping the extreme but distinct patterns of divergence in both organelle genomes within this genus.