Comparative transcriptomics reveals commonalities and differences in the genetic underpinnings of a floral dimorphism

Abstract

Abstract Distyly is a floral dimorphism associated with a heteromorphic self-incompatibility mechanism that prevents inbreeding and promotes outcrossing in 28 angiosperm families. Distyly is controlled by a cluster of genes, i.e. the S-locus supergene, that evolved independently in all distylous species studied to date. Here we present a transcriptome atlas for Primula veris, the main model for studying distyly since Darwin, which helped to elucidate the mechanism through which the S-locus gene CYPT acquired its role in controlling style elongation. We also identified genes that are differentially expressed between the two floral morphs of P. veris and Fagopyrum esculentum, revealing the main molecular mechanisms and hormones underlying the expression of distyly in these two species. Further, we discovered shared homologous genes that likely control distyly in P. veris, F. esculentum and Turnera subulata, suggesting that the convergent evolution of distyly at the phenotypic level is coupled, to some extent, also at the molecular level. Additionally, we provided statistical support to the hypothesis that distyly supergenes of different species evolved by the recruitment of genes related to the phytochrome-interacting factor (PIF) signaling network. Overall, this is the first study to identify homologous genes that underlie the control of distyly in distantly-related taxa.