Flipping the switch on some of the slowest mutating genomes: Direct measurements of plant mitochondrial and plastid mutation rates inmsh1mutants

Plant mitochondrial and plastid genomes have exceptionally slow rates of sequence evolution, and recent work has identified an unusual member of theMutSgene family (“plantMSH1”) as being instrumental in preventing point mutations in these genomes. However, the eXects of disruptingMSH1-mediated DNA repair on “germline” mutation rates have not been quantified. Here, we usedArabidopsis thalianamutation accumulation (MA) lines to measure mutation rates inmsh1mutants and matched wild type (WT) controls. We detected 124 single nucleotide variants (SNVs: 49 mitochondrial and 75 plastid) and 668 small insertions and deletions (indels: 258 mitochondrial and 410 plastid) inmsh1MA lines. In striking contrast, we did not find any organelle mutations in the WT MA lines, and reanalysis of data from a much larger WT MA experiment also failed to detect any variants. The observed number of SNVs in themsh1MA lines corresponds to estimated mutation rates of 6.1ξ10^-7and 3.2 ξ10^-6per bp per generation in mitochondrial and plastid genomes, respectively. These rates exceed those of species known to have very high mitochondrial mutation rates (e.g., nematodes and fruit flies) by an order of magnitude or more and are on par with estimated rates in humans despite the generation times ofA. thalianabeing nearly 100-fold shorter. Therefore, disruption of a single plant-specific genetic factor inA. thalianais suXicient to erase or even reverse the enormous diXerence in organelle mutation rates between plants and animals.