A lineage-specific paralogue of Oma1 evolved into a gene family from which a suppressor of male sterility-inducing mitochondria emerged in plants

Cytoplasmic male sterility in plants is caused by male sterility-inducing mitochondria, which have emerged frequently during plant evolution. Nuclear Restorer-of-fertility (Rf) genes can suppress their cognate male sterility-inducing mitochondria. Whereas many Rfs encode a class of RNA binding protein, the sugar beet (Caryophyllales) Rf encodes a protein resembling Oma1, which is involved in the quality control of mitochondria. In this study we investigated the molecular evolution of Oma1 homologues in plants. We analyzed 37 plant genomes and concluded that a single copy is the ancestral state in Caryophyllales. Among the sugar beet Oma1 homologues, the orthologous copy is located in a syntenic region that is preserved in Arabidopsis thaliana. The sugar beet Rf is a complex locus consisting of a small Oma1 homologue family (RF-Oma1 family) unique to sugar beet. The gene arrangement in the vicinity of the locus is seen in some but not all Caryophyllalean plants and is absent from A. thaliana. This suggests a segmental duplication rather than a whole genome duplication as the mechanism of RF-Oma1 evolution. Among the positively selected codons in RF-Oma1, many are located in predicted transmembrane helices. Phylogenetic network analysis indicated that homologous recombination among the RF-Oma1 members played an important role to generate protein activity related to suppression. Together, our data illustrate how an evolutionarily young Rf has emerged from a lineage-specific paralogue. Interestingly, several evolutionary features are shared with the RNA binding protein type Rfs. Hence, the evolution of the sugar beet Rf is representative of Rf evolution in general.

Keywords: restorer-of-fertility; Cytoplasmic male sterility; nuclear-mitochondrial interaction; plant mitochondria; positive selection; sugar beet.