Mutation Rate Variation and Organelle Genome Evolution in the Angiosperm Genus Silene

The defining challenge to the field of molecular evolution in the genomic era is to identify the evolutionary forces that have shaped the striking diversity in genome size, structure, and organization across the tree oflife. The mutational burden hypothesis offers a potentially unifying framework for explaining much of this diversity based on variation in the intensity and efficacy of selection associated with mutational processes. One key prediction from this hypothesis is that high mutation environments should select against large and complex genomes, because they are more susceptible to being altered or disrupted by mutation. For example, it has been argued that the abnormally large and complex mitochondrial genomes found in angiosperms reflect a history of relaxed selection resulting from the extremely low point mutation rates in these genomes. This dissertation establishes the angiosperm genus Silene (Caryophyllaceae) as an ideal system for testing this prediction. The genus Silene is shown to harbor dramatic variation in mitochondrial substitution rates both among genes and among evolutionary lineages. Several Silene species exhibit genome-wide accelerations of approximately 100-fold in mitochondrial substitution rates, which appear to reflect changes in underlying mutation rates. A comparative analysis of complete organelle genome sequences from four Silene species with highly divergent mitochondrial mutation rates shows that mutational acceleration has been associated with dramatic changes in mitochondrial genome architecture as well as some correlated differences in the rate of sequence and structural evolution in plastid genomes. However, many of the observed changes iii run counter to the predictions of the mutational burden hypothesis. In particular, rather than showing evidence of streamlining, the fast-evolving mitochondrial genomes have experienced a massive proliferation in non-coding content, resulting in the largest mitochondrial genomes ever identified. The specific mechanisms underlying the observed differences in mutation rate and genome architecture remain unknown, but evidence for changes in recombinational processes within these genomes motivate the hypothesis that disruptions in the nuclear-encoded organelle recombination machinery may be responsible. Further unraveling the process of rapid extreme change in Silene organelles genomes should provide new insights into the evolutionary forces responsible for the tremendous variation in eukaryotic genome size and complexity.

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