Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution

Abstract

Eukaryotic cells have harbored mitochondria for at least 1.5 billion years in an apparently mutually beneficial symbiosis. Studies on the agronomically important crop trait cytoplasmic male sterility (CMS) have suggested the semblance of a host-parasite relationship between the nuclear and mitochondrial genomes, but molecular evidence for this is lacking. Key players in CMS systems are the fertility restorer (Rf) genes required for the development of a functional male gametophyte in plants carrying a mitochondrial CMS gene. In the majority of cases, Rf genes encode pentatricopeptide repeat (PPR) proteins. We show that most angiosperms for which extensive genomic sequence data exist contain multiple PPR genes related to Rf genes. These Rf-like genes show a number of characteristic features compared with other PPR genes, including chromosomal clustering and unique patterns of evolution, notably high rates of nonsynonymous to synonymous substitutions, suggesting diversifying selection. The highest probabilities of diversifying selection were seen for amino acid residues 1, 3, and 6 within the PPR motif. PPR proteins are involved in RNA processing, and mapping the selection data to a predicted consensus structure of an array of PPR motifs suggests that these residues are likely to form base-specific contacts to the RNA ligand. We suggest that the selection patterns on Rf-like genes reveal a molecular "arms-race" between the nuclear and mitochondrial genomes that has persisted throughout most of the evolutionary history of angiosperms.