How did a duplicated gene copy evolve into arestorer-of-fertilitygene in a plant? The case ofOma1

Abstract

Restorer-of-fertility (Rf) is a suppressor of cytoplasmic male sterility (CMS), a mitochondrion-encoded trait that has been reported in many plant species. The occurrence of CMS is considered to be independent in each lineage; hence, the question of how Rf evolved was raised. Sugar beet Rf resembles Oma1, a gene for quality control of the mitochondrial inner membrane. Oma1 homologues comprise a small gene family in the sugar beet genome, unlike Arabidopsis and other eukaryotes. The sugar beet sequence that best matched Arabidopsis atOma1 was named bvOma1; sugar beet Rf (RF1-Oma1) was another member. During anther development, atOma1 mRNA was detected from the tetrad to the microspore stages, whereas bvOma1 mRNA was detected at the microspore stage and RF1-Oma1 mRNA was detected during the meiosis and tetrad stages. A transgenic study revealed that, whereas RF1-Oma1 can bind to a CMS-specific protein and alter the higher-order structure of the CMS-specific protein complex, neither bvOma1 nor atOma1 show such activity. We favour the hypothesis that an ancestral Oma1 gene duplicated to form a small gene family, and that one of the copies evolved and acquired a novel expression pattern and protein function as an Rf, i.e. RF1-Oma1 evolved via neofunctionalization.

What Does the Molecular Genetics of Different Types of Restorer-of-Fertility Genes Imply?

“…Sugar beet Rf1 is a duplicated gene of Oma1 [41,56]. Oma1 (named after overlapping activity with m-AAA protease) is known to be involved in quality control of mitochondria and mitochondrial dynamics in yeast and mammals [57][58][59].…”

“…CNV within a non-PPR Rf locus has rarely been reported to date. An exceptional case is the sugar beet Rf1 locus, in which Rf1-like genes are tandemly clustered [56], reminiscent of the PPR Rf locus. In fact, CNV is seen in the Rf1 locus of sugar beet and other Beta vulgaris genetic resources (e.g., Arakawa et al [72]), suggesting that a similar evolutionary mechanism to that of PPR Rf may be involved (i.e., interallelic recombination with unequal crossing over).…”

“…The clustered genes in the sugar beet Rf1 locus were designated RF1-Oma1 [56]. From the sugar beet genome, another Oma1 homologue that is more similar to Arabidopsis Oma1 (atOma1) was found and named bvOma1.…”

“…In yeast, a Zn 2+ -binding motif in the peptidase M48 domain was shown to be critical for Oma1 function [57]. The peptidase M48 domain with a functional Zn 2+ -binding motif was predicted from the translation products of atOma1 and bvOma1 but not from RF1-Oma1 due to a critical amino acid substitution [56]. The occurrence of multiple Oma1 homologues in the sugar beet genome contrasts with Arabidopsis and rice, both of which have a single Oma1 copy as is also the case for yeast and humans [41].…”

“…An Arabidopsis plant with a defect in atOma1 is viable but has malfunctioning oxidative phosphorylation [75]. A comparison of the proteins' ability to bind with preSATP6 and the expression pattern among RF1-Oma1, bvOma1 and atOma1 is summarized in Table 2; neither bvOma1 nor atOma1 had binding activity with preSATP6 protein [56]. The expression pattern during anther development was different among the three genes, of which only RF1-Oma1 was expressed at the meiosis stage [56].…”