An ancestral T2 RNase provides insights into the origin and evolution of self-incompatible S-RNase

With the evolution of true floral structures, angiosperms have become the most diverse and successful plant group, a success largely attributed to the genetic diversity generated by self-incompatibility. The canonical S-RNase (class III T2 RNase)/F-boxes locus that mediates gametophytic self-incompatibility is present across multiple lineages of core eudicots, and its origin has been traced back to the last common ancestor of core eudicots. However, because class III T2 RNases are completely absent from non-eudicot taxa, the origin of this S-RNase/F-boxes locus remains elusive. Here, we identify a rare class TI T2 RNase (EVM0017713)/F-boxes locus in the basal eudicot Akebia trifoliata as a candidate S-locus for late-acting self-incompatibility, sharing molecular features with the S-RNase/F-boxes locus. The class TI T2 RNase subfamily exhibits a continuous gradient transition from class I to class III T2 RNase subfamilies in terms of phylogenetic distribution, molecular structural characteristics, physicochemical properties, and gene structure. Crucially, the class TI EVM0017713/F-boxes locus is ancient and collinear with the S-RNase/F-boxes loci. These results suggest that the class TI T2 RNase/F-box locus may represent an ancestral form of the S-RNase/F-box system, offering new insights into the origin and evolution of plant self-incompatibility.