Genomic studies in Linum shed light on the evolution of the distyly supergene and the molecular basis of convergent floral evolution

Abstract

O_LIDistyly, an example of convergent evolution, is governed by a supergene called the S- locus. Recent studies highlight similar genetic architectures of independently evolved S-loci, but whether similar regulatory pathways underlie convergent evolution of distyly remains unclear. C_LIO_LIWe examined the evolution of supergenes and mechanisms underlying distyly in Linum species that diverged [~]33 Mya. Using haplotype-resolved genomes and population genomics, we identified and characterized the S-loci of Linum perenne (distylous) and Linum grandiflorum (style length dimorphic), and compared them to that of Linum tenue (distylous). We then tested for a conserved hormonal mechanism regulating style length polymorphism in Linum. C_LIO_LIHemizygosity in short-styled individuals is a shared feature of the Linum S-locus supergene, though its size, gene content, repeat elements, and extent of recombination suppression vary greatly among species. Two distyly candidate genes, TSS1 (style length) and WDR-44 (anther height/pollen self-incompatibility) are conserved at the C_LIO_LIS-locus. Consistent with a brassinosteroid-dependent role of TSS1, epibrassinolide treatment revealed a conserved, morph-specific effect on style length. C_LIO_LIS-locus genetic architecture, key S-locus genes and mechanisms regulating style length remain conserved >30 Mya in Linum. In combination with findings from other systems, our results suggest that the brassinosteroid pathway frequently contributes to style length polymorphism. C_LI