Phylogenetic analysis of S-RNase-like genes from Fragaria provides evidence for ancestral S-RNase duplication in the Rosaceae lineage

Abstract

Self-incompatibility (SI) is associated with cultural and breeding difficulties in rosaceous fruit trees such as cherry, plum, apple, and pear. Many species in Rosaceae, Solanaceae, and Plantaginaceae have S-RNase-based gametophytic SI, with S-RNase and F-box proteins as pistil S and pollen S determinants, respectively. Although the S-RNase-based gametophytic SI system is generally believed to have evolved once in a eudicot ancestor before the divergence of asterids and rosids, we previously found that S-RNase and its homologs were duplicated in the ancestral genome of Rosaceae. Here, we reinvestigated the evolutionary paths of S-RNase-like genes using homologs from the diploid Fragaria species F. nipponica (SI), F. nubicola (SI), and F. iinumae (SI phenotype undetermined). Our phylogenetic analysis and estimation of proxy ages for the establishment of S-RNase and its homologs in rosaceous species supports the previously inferred ancestral S-RNase duplication in the Rosaceae lineage. The divergence of S-RNases in subtribe Malinae and Prunus predated the most recent common ancestor of Rosaceae, which includes genes from three rosaceous species (Fragaria, Prunus, and Malus). The results of the present study strengthen the idea that the genus Prunus and subtribe Malinae have evolved different S-RNases for SI recognition. These results may explain the genus- or subtribe-specific SI recognition mechanism operating in rosaceous fruit trees and will be valuable for artificial SI control and self-compatible breeding.