Dissecting the Heterostyly Supergene in Primula (primrose)

Heterostyly is a wide-spread floral adaptation to promote outbreeding, yet its genetic basis and evolutionary origin remain poorly understood. In Primula (primroses), heterostyly is controlled by the S-locus supergene that determines the reciprocal arrangement of reproductive organs and incompatibility between the two morphs. The S-locus supergene comprises at least three, more likely five individual causal genes controlling the different traits that are held together in tight linkage by suppressed recombination. While one S-locus haplotype carries dominant alleles at all of these loci, the other only has recessive alleles. The long-styled L-morph is homozygous for the recessive S-locus haplotype, while the short-styled S-morph is heterozygous; the system thus resembles XX/XY-based sex determination in animals. The two haplotypes are thus under long-term balancing selection, and the dominant one is not recombining, making it subject to Muller’s ratchet. However, testing population-genetic and evolutionary predictions about the S-locus is hampered by our lack of knowledge about the component causal genes. We have recently identified the Primula CYP734A50 gene, encoding a putative brassinosteroid-degrading enzyme, as the G locus that determines the style-length dimorphism. CYP734A50 is only present on the short-styled S-morph haplotype, it is specifically expressed in S-morph styles, and its loss or inactivation leads to long styles. The gene arose by a duplication specific to the Primulaceae lineage and shows an accelerated rate of molecular evolution. Additional genes with analogous characteristics, such as being present only on the dominant S-morph haplotype, have been identified, representing candidates for other causal heterostyly genes. Their functional characterization is ongoing. Thus, our results provide a mechanistic explanation for the Primula style-length dimorphism and begin to shed light on the evolution of the S-locus as a prime model for a complex plant supergene.