An Integrative Evolutionary–Genomic Analysis Reveals the Factors That Shape the Sexual Diversity and Molecular Specificity of Gametophytic Self-Incompatibility in Prunus Species

Background: Gametophytic self-incompatibility (GSI) controlled by a multi-allelic S-locus, is inferred to have evolved before the spilt of the Rosidae and Asteridae. In Rosaceae, molecular characterisation of the genera Prunus and Malus reveals that different numbers of genes determine GSI specificity. In Prunus, one pistil-expressed (female) gene and one pollen (male) gene encode a series of stylar RNase (S-RNase) alleles and series of S-haplotype-specific F-box (SFB) alleles, respectively, thereby determining the female and male specificity. In contrast, in Malus, GSI specificity is controlled by one pistil gene and multiple pollen genes, known as SFB-brothers (SFBBs), which encode a series of S-RNase and SFBB alleles, respectively, within the S-locus, to determine female and male specificity. Despite these advances, the molecular mechanisms of these two genera remain largely unknown, and it is still uncertain how GSI originated or which factors shape the orientation, evolution, and function of the S-locus. Methods: Therefore, in this study, we applied a holistic integrative approach combining analyses of gene distribution, phylogenetic inference, biogeographic history, selective pressures, co-evolution, and protein interaction networks across three Prunus genomes (P. dulcis, P. persica, and P. avium) to elucidate the evolutionary forces driving sexual diversity and molecular specificity of GSI within the Rosaceae. Results: Our results indicated that rapid diversification of the Prunus S-locus was due to the repeated duplication events in the SFB, SLF, and S-RNase genes producing both functional and non-functional duplicates. Conclusions: In Rosaceae, diversity of S-locus mechanisms is shaped by lineage-specific selection, functional divergence, co-evolution of pistil- and pollen-expressed components, dynamic protein-interaction networks, geological history and climatic change.