A Lineage-Specific Paralog of Oma1 Evolved into a Gene Family from Which a Suppressor of Male Sterility-Inducing Mitochondria Emerged in Plants

Cytoplasmic male sterility (MS) in plants is caused by MS-inducing mitochondria, which have emerged frequently during plant evolution. Nuclear restorer-of-fertility (Rf)genes can suppress their cognateMS-inducing mitochondria.Whereas many Rfs encode a class of RNA-binding protein, the sugar beet (Caryophyllales) Rf encodes a protein resemblingOma1,which is involved in the quality control ofmitochondria. In this study, we investigated the molecular evolution of Oma1 homologs in plants.We analyzed 37 plant genomes and concluded that a single copy is the ancestral state in Caryophyllales. Among the sugar beet Oma1 homologs, 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 smallOma1homolog family (RF-Oma1 family) unique to sugar beet. The gene arrangement in the vicinity of the locus is seen in some but not allCaryophyllalean plants and is absent fromAr. thaliana. This suggests a segmental duplication rather than a whole-genome duplication as themechanism of RF-Oma1 evolution.Of thirty-seven positively selected codons in RF-Oma1, twentysix of these sites 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 paralog. Interestingly, several evolutionary features are sharedwith the RNA-binding protein type Rfs.Hence, the evolution of the sugar beet Rf is representative of Rf evolution in general