Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates

A pair of species within the genus Silene have evolved the largest known mitochondrial genomes, coinciding with extreme changes in mutation rate, recombination activity, and genome structure.
Genome size and complexity vary tremendously among eukaryotic species and their organelles. Comparisons across deeply divergent eukaryotic lineages have suggested that variation in mutation rates may explain this diversity, with increased mutational burdens favoring reduced genome size and complexity. The discovery that mitochondrial mutation rates can differ by orders of magnitude among closely related angiosperm species presents a unique opportunity to test this hypothesis. We sequenced the mitochondrial genomes from two species in the angiosperm genus Silene with recent and dramatic accelerations in their mitochondrial mutation rates. Contrary to theoretical predictions, these genomes have experienced a massive proliferation of noncoding content. At 6.7 and 11.3 Mb, they are by far the largest known mitochondrial genomes, larger than most bacterial genomes and even some nuclear genomes. In contrast, two slowly evolving Silene mitochondrial genomes are smaller than average for angiosperms. Consequently, this genus captures approximately 98% of known variation in organelle genome size. The expanded genomes reveal several architectural changes, including the evolution of complex multichromosomal structures (with 59 and 128 circular-mapping chromosomes, ranging in size from 44 to 192 kb). They also exhibit a substantial reduction in recombination and gene conversion activity as measured by the relative frequency of alternative genome conformations and the level of sequence divergence between repeat copies. The evolution of mutation rate, genome size, and chromosome structure can therefore be extremely rapid and interrelated in ways not predicted by current evolutionary theories. Our results raise the hypothesis that changes in recombinational processes, including gene conversion, may be a central force driving the evolution of both mutation rate and genome structure.
Author Summary A fundamental challenge in evolutionary biology is to explain why organisms exhibit dramatic variation in genome size and complexity. One hypothesis predicts that high rates of mutation in DNA sequence create selection against large and complex genomes, which are more susceptible to mutational disruption. Species of flowering plants in the genus Silene vary by approximately 100-fold in the rates of mutation in their mitochondrial DNA, providing an excellent opportunity to test the predicted effects of high mutation rates on genome evolution. Contrary to expectation, Silene species with elevated mutation rates have experienced dramatic expansions in mitochondrial genome size compared to their slowly evolving relatives, resulting in the largest known mitochondrial genomes. In addition to the increases in size and mutation rate, these genomes also reveal a history of rapid change in genome structure. They have been fragmented into dozens of chromosomes and appear to have experienced major reductions in recombination activity. All of these changes have occurred in just the past few million years. This mitochondrial genome diversity within the genus Silene provides a striking example of rapid genomic change and raises new hypotheses regarding the relationship between mutation rate and genome evolution.