Genes and Junk in Plant Mitochondria—Repair Mechanisms and Selection

Abstract

Plant mitochondrial genomes have very low mutation rates. In contrast, they also rearrange and expand frequently. This is easily understood if DNA repair in genes is accomplished by accurate mechanisms, whereas less accurate mechanisms including nonhomologous end joining or break-induced replication are used in nongenes. An important question is how different mechanisms of repair predominate in coding and noncoding DNA, although one possible mechanism is transcription-coupled repair (TCR). This work tests the predictions of TCR and finds no support for it. Examination of the mutation spectra and rates in genes and junk reveals what DNA repair mechanisms are available to plant mitochondria, and what selective forces act on the repair products. A model is proposed that mismatches and other DNA damages are repaired by converting them into double-strand breaks (DSBs). These can then be repaired by any of the DSB repair mechanisms, both accurate and inaccurate. Natural selection will eliminate coding regions repaired by inaccurate mechanisms, accounting for the low mutation rates in genes, whereas mutations, rearrangements, and expansions generated by inaccurate repair in noncoding regions will persist. Support for this model includes the structure of the mitochondrial mutS homolog in plants, which is fused to a double-strand endonuclease. The model proposes that plant mitochondria do not distinguish a damaged or mismatched DNA strand from the undamaged strand, they simply cut both strands and perform homology-based DSB repair. This plant-specific strategy for protecting future generations from mitochondrial DNA damage has the side effect of genome expansions and rearrangements.

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

“…In most angiosperms, the opposite is true (Wolfe et al. 1987), possibly owing to RRR mechanisms that are found in plant mtDNA but absent in animals (Christensen 2014). However, in several independent angiosperm lineages, mutation rates in mitochondrial genomes have undergone an acceleration, shifting the mitonuclear mutation balance to a more animal-like pattern (Mower et al.…”

The mutational hazard hypothesis of organelle genome evolution: 10 years on

“…). By comparing mitochondrial genome sequences of Arabidopsis thaliana ecotypes and other closely related angiosperms, Christensen (, ) showed that intergenic sites have a much higher rate of substitution (including insertions/deletions and rearrangements) than synonymous sites, which is a feature that has largely gone unnoticed in previous work. It is not known why substitution rates differ so significantly between these two kinds of so‐called neutral sites, but Christensen (, ) proposed that there is greater selection on synonymous vs. intergenic sites in land plant mtDNAs, which ultimately impacts how these sites are repaired.…”

“…Short‐, micro‐ or nonhomology‐based repair pathways, such as nonhomologous end‐joining or microhomology‐mediated break‐induced replication, are error prone and can often lead to genomic expansion and rearrangements. Figure based on Christensen (, ).…”

The Roles of Mutation, Selection, and Expression in Determining Relative Rates of Evolution in Mitochondrial versus Nuclear Genomes

“…The mt genomes of angiosperms also fundamentally differ from those of bilaterian animals in that they have much lower rates of nucleotide substitution than the nuclear genome (Wolfe et al 1987), which may be due to mt recombination/repair mechanisms found in plants but not animals (Christensen 2014). However, the slow-plant/fast-animal dichotomy of mt evolution is a gross oversimplification.…”