S-RNase evolution in self-incompatibility: Phylogenomic insights into synteny with Class I T2 RNase genes

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Abstract
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.
Funding Information
  • State Key Research and Development Project
  • Youth Scientist Program (2023YFD1202400)
  • National Natural Science Foundation of China (32102338)
  • Chinese Universities Scientific Fund (2452021133)

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