Evolution of S-domain receptor-like kinases in land plants and origination of S-locus receptor kinases in Brassicaceae

Background: The S-domain serine/threonine receptor-like kinases (SRLKs) comprise one of the largest and most rapidly expanding subfamilies in the plant receptor-like/Pelle kinase (RLKs) family. The founding member of this subfamily, the S-locus receptor kinase (SRK), functions as the female determinant of specificity in the self-incompatibility (SI) responses of crucifers. Two classes of proteins resembling the extracellular S domain (designated S-domain receptor-like proteins, SRLPs) or the intracellular kinase domain (designated S-domain receptor-like cytoplasmic kinases, SRLCKs) of SRK are also ubiquitous in land plants, indicating that the SRLKs are composite molecules that originated by domain fusion of the two component proteins. Here, we explored the origin and diversification of SRLKs by phylogenomic methods. Results: Based on the distribution patterns of SRLKs and SRLCKs in a reconciled species-domain tree, a maximum parsimony model was then established for simultaneously inferring and dating gene duplication/loss and fusion/fission events in SRLK evolution. Various SRK alleles from crucifer species were then included in our phylogenetic analyses to infer the origination of SRKs by identifying the proper outgroups. Conclusions: Two gene fusion events were inferred and the major gene fusion event occurred in the common ancestor of land plants generated almost all of extant SRLKs. The functional diversification of duplicated SRLKs was illustrated by molecular evolution analyses of SRKs. Our findings support that SRKs originated as two ancient haplotypes derived from a pair of tandem duplicate genes through random regulatory neo-/sub- functionalization in the common ancestor of the Brassicaceae.