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

Abstract

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.

Different molecular markers to identify the fertility of sugar beet monogerm germplasm resources

“…Nucleoplasmic interaction-based studies of sugar beet fertility have provided good insight into the causes of sugar beet failure, which are inextricably linked to the Oma1 gene, a gene encoding a yeast protease (Kaser, et al 2003) that plays various roles in mitochondrial quality control (Guo, et al 2020;Migdal, et al 2017). In sugar beet, a duplicated copy of Oma1 evolved into Rf1 (Arakawa, et al 2020). The sugar beet Rf1 locus is actually a complex locus with multiple Oma1-like genes involved in fertility restoration, but Rf1 does not necessarily correspond to a single open reading frame (Arakawa, et al 2020), which adds to the di culty of testing sugar beet fertility by means of molecular markers.…”

“…In sugar beet, a duplicated copy of Oma1 evolved into Rf1 (Arakawa, et al 2020). The sugar beet Rf1 locus is actually a complex locus with multiple Oma1-like genes involved in fertility restoration, but Rf1 does not necessarily correspond to a single open reading frame (Arakawa, et al 2020), which adds to the di culty of testing sugar beet fertility by means of molecular markers. In addition, another Rf2 gene in sugar beet that is associated with fertility restoration is a locus of uncertain action size.…”

Selection of Nuclear Genotypes Associated with the Thermo-inducibility of Owen-type Cytoplasmic Male Sterility in Sugar Beet (Beta vulgaris L.)

“…The Rf1 locus is highly polymorphic in the number of clustered Rf1-Oma1 copies and their nucleotide sequences (Arakawa et al 2020a). The molecular diversity of the Rf1 locus is associated with the variety of its alleles: dominant, semi-dominant, hypomorphic and recessive alleles with very different types of gene organization are known.…”

Migration Restores Hybrid Incompatibility Driven By Mitochondrial-Nuclear Sexual Conflict

“…The accumulation of male-harming mutations places selective pressure on the nuclear genome to evolve variants that restore male fitness, termed "restorers", at least partially counteracting the cost of these Mother's Curse variants. The rapid generation and fixation of such nuclear restorer mutations has been thoroughly documented in plants (38)(39)(40).…”