Abstract
BackgroundThe mitochondrial genome of higher plants is unusually dynamic, with recombination and nonhomologous end-joining (NHEJ) activities producing variability in size and organization. Plant mitochondrial DNA also generally displays much lower nucleotide substitution rates than mammalian or yeast systems. Arabidopsis displays these features and expedites characterization of the mitochondrial recombination surveillance gene MSH1 (MutS 1 homolog), lending itself to detailed study of de novo mitochondrial genome activity. In the present study, we investigated the underlying basis for unusual plant features as they contribute to rapid mitochondrial genome evolution.ResultsWe obtained evidence of double-strand break (DSB) repair, including NHEJ, sequence deletions and mitochondrial asymmetric recombination activity in Arabidopsis wild-type and msh1 mutants on the basis of data generated by Illumina deep sequencing and confirmed by DNA gel blot analysis. On a larger scale, with mitochondrial comparisons across 72 Arabidopsis ecotypes, similar evidence of DSB repair activity differentiated ecotypes. Forty-seven repeat pairs were active in DNA exchange in the msh1 mutant. Recombination sites showed asymmetrical DNA exchange within lengths of 50- to 556-bp sharing sequence identity as low as 85%. De novo asymmetrical recombination involved heteroduplex formation, gene conversion and mismatch repair activities. Substoichiometric shifting by asymmetrical exchange created the appearance of rapid sequence gain and loss in association with particular repeat classes.ConclusionsExtensive mitochondrial genomic variation within a single plant species derives largely from DSB activity and its repair. Observed gene conversion and mismatch repair activity contribute to the low nucleotide substitution rates seen in these genomes. On a phenotypic level, these patterns of rearrangement likely contribute to the reproductive versatility of higher plants.
Highlights
The mitochondrial genome of higher plants is unusually dynamic, with recombination and nonhomologous end-joining (NHEJ) activities producing variability in size and organization
While confirming previously identified repeats [21], deep sequencing revealed 14 new repeat pairs ranging from 50 to 250 bp in size, with sequence homology within each pair ranging from 85% to 98% and the smallest repeats displaying the highest identity (Figure 1B)
A more extensive survey of repeats showed no clear pattern of donor or recipient strand cleavage for correction of nucleotide insertions. These results reveal the presence of a mitochondrial mismatch repair mechanism in plants that is independent of MSH1
Summary
The mitochondrial genome of higher plants is unusually dynamic, with recombination and nonhomologous end-joining (NHEJ) activities producing variability in size and organization. Given the linear structure of the genome, this recombination activity is Mitochondrial genome plasticity is evident in extensive DNA polymorphism among closely related lines of a given plant species [6], rapid accumulation of polymorphisms within a line under cell culture conditions [7,8,9] and novel insertions, deletions and sequence chimeras [6]. These types of genomic alterations are causative in cytoplasmic male sterility (CMS) in a wide range of plant species [10], implying an adaptive rationale for the genomic phenomena [11]. The DNA repair mechanisms accounting for unusually low nucleotide substitution rates in plants are not known [14,15]
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