Expansion of the MutS Gene Family in Plants

Abstract

TheMutSgene family is distributed across the tree of life and is involved in recombination, DNA repair, and protein translation. Multiple evolutionary processes have expanded the set ofMutSgenes in plants relative to other eukaryotes. Here, we investigate the origins and functions of these plant-specific genes. Land plants, green algae, red algae, and glaucophytes share cyanobacterial-likeMutS1andMutS2genes that presumably were gained via plastid endosymbiotic gene transfer.MutS1was subsequently lost in some taxa, including seed plants, whereasMutS2was duplicated in Viridiplantae (i.e., land plants and green algae) with widespread retention of both resulting paralogs. Viridiplantae also have two anciently duplicated copies of the eukaryoticMSH6gene (i.e.,MSH6andMSH7) and acquiredMSH1via horizontal gene transfer – potentially from a nucleocytovirus. Despite sharing the same name, “plantMSH1” is not directly related to the gene known asMSH1in some fungi and animals, which may be an ancestral eukaryotic gene acquired via mitochondrial endosymbiosis and subsequently lost in most eukaryotic lineages. There has been substantial progress in understanding the functions ofMSH1andMSH6/MSH7in plants, but the roles of the cyanobacterial-likeMutS1andMutS2genes remain uncharacterized. Known functions of bacterial homologs and predicted protein structures, including fusions to diverse nuclease domains, provide hypotheses about potential molecular mechanisms. Because most plant-specific MutS proteins are targeted to the mitochondria and/or plastids, the expansion of this family appears to have played a large role in shaping plant organelle genetics.One-Sentence SummaryPlants are distinguished from other eukaryotes by a functionally diverse complement of MutS proteins gained via a combination of gene duplication, endosymbiotic gene transfer, and horizontal gene transfer.