Unlike in animal mitochondria, recombination is widespread in plant mtDNA. Recombinant molecules have been detected in various species, and are involved in a number of phenotypic traits, including thermotolerance and male sterility. The nuclear-encoded MSH1 gene, which is the product of fusion between a homologue of the bacterial DNA-repair gene MutS and an endonuclease gene, is involved in the control of plant mtDNA recombination. Using next-generation sequencing technologies, Davila et al. [3] have examined the recombination pattern in wild-type versus MSH1-mutant ecotypes of the Brassicaceae Arabidopsis thaliana model. They report that MSH1 mutants experience mitochondrial recombination at a much higher rate than the wild type, as reflected by the frequent detection of rearranged mitochondrial molecules generated by illegitimate (ectopic) recombination between repeated elements. Interestingly, recombination in MSH1 mutants is shown to be associated with asymmetrical genetic exchanges: in a window of a few hundred bases surrounding the recombination breakpoint, one of the two recombining DNA sequences is copied and pasted onto the other one. This process, known as gene conversion, is mediated by efficient DNA mismatch repair activity, and contributes to sequence homogenization of recombinogenic motifs. An analysis of mitochondrial variations across 72 natural ecotypes of A. thaliana reveals similar patterns, suggesting that the processes described by Davila et al. actually impact on the evolution of plant mtDNA.
This study, therefore, provides us with a proximal explanation for the low substitution rate of plant mtDNA, namely the existence of efficient recombination-associated DNA repair activity. Ectopic recombination is potentially harmful in generating chromosomal rearrangements that disrupt coding frames or impede gene expression regulation. Mechanisms of recombination surveillance and repair of recombination-induced DNA damage, including mismatch repair, appear necessary for plant mtDNA. Animal mtDNA, in contrast, is essentially devoid of repeated elements, so illegitimate recombination is much less an issue in these genomes. Selective pressure for efficient DNA repair might thus be relaxed, leading to an increased mutation rate. We note that, in turn, its elevated mutation rate has been invoked to explain the absence of introns in animal mtDNA-in a highly mutable context, the functional sequences necessary to proper intron excision imply an additional, counter-selected mutation load [4]. The contrast between plant and animal mtDNA behaviour might therefore reflect the two distinct solutions they implement to cope with repeated element threats: either avoiding them, at the cost of a high point mutation rate (animals), or repairing the damage they cause by selecting for efficient DNA repair activity (plants). This response, however, gives rise to another question: what properties of plants and animals, if any, have made them take such distinctive pathways regarding mitochondrial evolution?