Yunxiao Liu

S-RNases are essential in the gametophytic self-incompatibility (GSI) system of many flowering plants, where they act as stylar-S determinants. Despite their prominence, the syntenic genomic origin and evolutionary trajectory of S-RNase genes in eudicots have remained largely unclear. Here, we performed large-scale phylogenetic and microsynteny network analyses of T2 RNase genes across 130 angiosperm genomes, encompassing 35 orders and 56 families. S-like RNase genes in Cucurbitaceae species phylogenetically grouped with functionally characterized S-RNases in various species. Additionally, Cucurbitaceae S-like RNase genes showed conserved synteny with Class I T2 RNase genes. From this, we inferred that the well-characterized S-RNase genes (belonging to Class III-A genes) and Class I T2 RNase genes (located on duplicated genomic blocks) likely derived from the gamma triplication event shared by core eudicots. Additionally, we identified frequent lineage-specific gene transpositions of S-RNases and S-like RNases across diverse angiosperm lineages, including Rosaceae, Solanaceae, and Rutaceae families, accompanied by a significant increase in transposable element activity near these genes. Our findings delineate the genomic origin and evolutionary path of eudicot S-RNase genes, enhancing our understanding of the evolution of the S-RNase-based GSI system.

S-RNases are essential in the gametophytic self-incompatibility (GSI) system of many flowering plants, where they act as stylar-S determinants. Despite their significance, the syntenic genomic origin and evolutionary trajectory of S-RNase genes in eudicots have remained largely unclear. Here, we performed large-scale phylogenetic and microsynteny network analyses of RNase T2 genes across 130 angiosperm genomes, encompassing 35 orders and 56 families. Based on the connections observed in the synteny network, particularly the persisting synteny block in none-SI Cucurbitaceae species, we infer that well-characterized S-RNase genes (Class III-A RNase genes) were duplicated and evolved from Class I S-like RNase genes, possibly as a result of the gamma triplication event shared by core eudicots. Additionally, we identified frequent lineage-specific gene transpositions of S-RNase genes across diverse angiosperm lineages, including Rosaceae, Solanaceae, and Rutaceae families, accompanied by a significant increase in transposable element (TE) activity near these genes. Our findings delineate the precise genomic origin and evolutionary path of eudicot S-RNase genes, enhancing our understanding of the evolution of the S-RNase-based GSI system.