CMS

Galtier N 2011 The intriguing evolutionary dynamics of plant mitochondrial DNA. BMC Biol 9:61.

  • 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
  • Davila et al. [3] have examined the recombination pattern in wild-type versus MSH1-mutant ecotypes of the Brassicaceae Arabidopsis thaliana model
  • MSH1 mutants experience mitochondrial recombination at a much higher rate than the wild type
  • recombination in MSH1 mutants is shown to be associated with asymmetrical genetic exchanges
  • 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
  • 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.
  • in turn, its elevated mutation rate has been invoked to explain the absence of introns in animal mtDNA
  • 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 germline bottleneck explains the rapid segregation of mitochondrial variants across generations
  • it is thought to have evolved to decrease heteroplasmy, the co-existence of several mitochondrial haplotypes within the same individual
  • avoiding heteroplasmy is beneficial for the nuclear genome since it reduces the opportunity for selfish mtDNA mutations to increase in frequency in the population
  • a germline bottleneck is not documented in plants, perhaps as a consequence of their delayed differentiation of reproductive cells
  • gene conversion and efficient mismatch repair in plants might therefore be interpreted as mechanisms selected in the nuclear genome to homogenize mtDNA sequences within an individual, thus limiting the spread of selfish mitochondrial variants, in the absence of a germline bottleneck
  • the syndrome of cytoplasmic male sterility, in which mtDNA variants arrest pollen growth, illustrates the major role played by mitochondrial heteroplasmy in the nucleo-cytoplasmic conflict in plants
  • and the potential benefit for the nucleus to control it
  • one could object that nucleo-cytoplasmic conflict arguments should apply to the chloroplast as well
  • although recombination and DNA repair systems are documented in chloroplasts, they do not result in a particularly low nucleotide substitution rate or in a particularly high rearrangement rate in this organelle
  • the very low point mutation rate of mtDNA in plants, sponges and anthozoans apparently reflects a mitochondrion-specific property