Mitochondrial genomes have undergone massive reductions in size and gene content since their endosymbiotic origin. Furthermore, compared with the genomes of their bacterial ancestors, most mitochondrial DNA lineages evolve rapidly in sequence. Land plants are apparently the one exception to this, but we have very recently identified two independent lineages of plants (Pelargonium and Plantago) whose substitution rates for four mitochondrial protein and two rRNA genes are at least 5-30 times higher than those of typical, slowly-evolving plant mitochondrial genomes. Hypotheses for the mechanisms underlying these major and recent increases in mitochondrial DNA mutation rate include: 1) deficient DNA repair, 2) error-prone DNA replication, and 3) error-prone retroprocessing. Although virtually all plant mitochondrial mRNAs are subject to extensive RNA editing, our data indicate that mitochondrial RNA editing does not occur in either Pelargonium or Plantago, that in fact their genomes are already edited as a consequence of unusually extensive retroprocessing. These data support the hypothesis of intense, error-prone retroprocessing, i.e., mutagenic reverse transcription followed by recombination back into the genome. Experiments are proposed to test among the various hypotheses and to determine the mechanisms responsible for the observed acceleration in mitochondrial DNA evolution in Pelargonium and Plantago.
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