Research Faculty of Agriculture, Hokkaido University, Kita-ku, Sapporo, Japan.
Gifu Prefectural Research Institute for Agricultural Technology in Hilly and Mountainous Areas, Nakatsugawa, Gifu, Japan.
Genome Biol Evol. 2020 Dec 6;12(12):2314-2327. doi: 10.1093/gbe/evaa186.
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 cognate MS-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 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 small Oma1 homolog 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 Ar. thaliana. This suggests a segmental duplication rather than a whole-genome duplication as the mechanism of RF-Oma1 evolution. Of thirty-seven positively selected codons in RF-Oma1, twenty-six 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 shared with the RNA-binding protein type Rfs. Hence, the evolution of the sugar beet Rf is representative of Rf evolution in general.
植物细胞质雄性不育（CMS）是由 CMS 诱导的线粒体引起的，这些线粒体在植物进化过程中频繁出现。核育性恢复（Rf）基因可以抑制其同源 CMS 诱导的线粒体。虽然许多 Rf 基因编码一类 RNA 结合蛋白，但甜菜（石竹目）的 Rf 基因编码一种类似于 Oma1 的蛋白质，该蛋白质参与线粒体的质量控制。在这项研究中，我们研究了植物中 Oma1 同源物的分子进化。我们分析了 37 种植物基因组，得出结论认为单拷贝是石竹目的原始状态。在甜菜 Oma1 同源物中，直系同源物位于在拟南芥中保留的同线性区域。甜菜 Rf 是一个复杂的基因座，由一个小的 Oma1 同源家族（RF-Oma1 家族）组成，该家族是甜菜所特有的。该基因座附近的基因排列在一些但不是所有石竹目中的植物中可见，而在拟南芥中不存在。这表明 RF-Oma1 进化的机制是片段复制而不是全基因组复制。在 RF-Oma1 中的三十七个正选择密码子中，有二十六个位于预测的跨膜螺旋中。系统发育网络分析表明，RF-Oma1 成员之间的同源重组在产生与抑制相关的蛋白质活性方面发挥了重要作用。总之，我们的数据说明了一个进化较年轻的 Rf 是如何从一个谱系特异性的旁系同源物中出现的。有趣的是，几种进化特征与 RNA 结合蛋白类型的 Rf 共享。因此，甜菜 Rf 的进化代表了一般 Rf 进化的代表。
