A Molecular Evolutionary Framework of Self-Incompatibility in the Angiosperms

SUMMARYThe angiosperms are the largest vascular plant group. However, the mechanisms for their rapid expansions in the Cretaceous and Paleogene remain unclear. Here, we find that self-incompatibility (SI) appears to be one central component contributing to their expansions. SI is a genetic barrier to prevent inbreeding widely found in the angiosperms and controlled by the polymorphic S -locus. So far, five molecular types of S -loci have been identified with the first defined by Lolium perenne domain of unknown function 247 ( LpS-DUF247 ), the second S-RNase and S-locus F-box ( SLF s), the third S-locus cysteine-rich protein ( SCR ) and S-locus receptor kinase ( SRK ), the fourth Papaver rhoeas stigma S ( PrsS ) and Papaver rhoeas pollen S ( PrpS ) and the fifth a hemizygous S -locus supergene of Primula . Phylogenomics and functional analyses showed that SI evolved twice in the Cretaceous and around the Cretaceous-Paleogene boundary, respectively. The first evolution involved the origins of the S genes of types 1 and 2 in the ancestors of Poales and eudicots, respectively. Then, the S -locus of type 2 underwent divergent evolution with losses in several ancestral eudicot lineages. The second involved the S -loci of types 3, 4 and 5 in the ancestors of Brassicaceae, Paperveraceae and Primulaceae, respectively. Interestingly, the times of the two evolutions of SI systems coincided with early angiosperm expansions. Furthermore, we find that neofunctionalization and de novo gene formation contributed to the S gene origins. Taken together, our results reveal a molecular evolutionary framework of SI in the angiosperms and its promoting role in their expansions.