The Mitochondrial Genome Evolution of the Geranium Family: Elevated Substitution Rates Decrease Genomic Complexity

The nucleotide substitution rate of plant mitochondrial DNA (mtDNA) is generally very low compared to the nuclear genome or its plastid counterpart. Mitochondrial sequences from taxa of the geranium family, however, have an exceptional increase in their substitution rate. To further analyze this unusual finding, we used next-generation sequencing to obtain complete mtDNAs of seven representative Geraniales taxa. Our results show that the elevated substitution rates co-occur with an exceptional increase in mitochondrial genome size. This increase in size is coupled with a radical reduction of complexity reflected by a massive loss of genes, introns, and RNA editing sites. Of particular note was the loss of three nad1 introns, including a trans-spliced intron that re-established continuity of nad1 gene transcription. In parallel, the maturase matR (usually encoded within a nad1 intron) evolved to be a free-standing mitochondrial gene in most Geraniaceae genera. In Pelargonium (which has the fastest evolving mtDNA), the matR gene is transferred into the nuclear genome where it acquired target signals for protein re-import into the mitochondria. The mtDNA of Pelargonium has lost its matR gene copy together with most ribosomal protein and all succinate dehydrogenase genes leading to a highly reduced gene content. Additionally, the transcripts of the remaining mitochondrial genes lost most RNA editing sites--only a total of three mitochondrial editing positions remain in Pelargonium. This unique correlation of elevated substitution rates with increased genome sizes and decreased genomic complexity in the geranium family represent yet another pathway of mtDNA evolution.