The genomic basis of the tristylous floral polymorphism - evidence for a role of gene duplications in a region of restricted recombination.

Abstract

Tristyly is an angiosperm sexual polymorphism characterized by three flower morphs maintained in populations by negative frequency-dependent selection resulting from disassortative mating among morphs. The floral morphs possess reciprocal stigma and anther heights controlled by two epistatically interacting diallelic loci (S and M). Although considerable progress has been made on determining the genetic architecture and genes governing the related heterostylous polymorphism distyly, our understanding of these aspects of the genetic basis of tristyly have not been examined. Here, we address this knowledge gap by investigating the genomic basis of tristyly in Eichhornia paniculata (Pontederiaceae), an annual bee-pollinated herb native to the Neotropics, primarily N.E. Brazil. Chromosome-level genome assemblies of E. paniculata identified the S- and M-loci on either side of a large region of low recombination on the same chromosome----. The S-locus consisted of two divergent haplotypes: the S-haplotype (2.51-Mb) with three S-haplotype specific genes and the s-haplotype (596-kb) with five s-haplotype specific genes. Two of the S-haplotype specific genes, LAZY1-S and HRGP-S, were specifically expressed in styles and stamens, respectively, making them candidate tristyly genes and providing evidence for this locus functioning as a hemizygous supergene. The M-locus contained one gene (LAZY1-M), homologous to LAZY1-S, present in the M-haplotype but absent from the m-haplotype. Estimates of gene ages and phylogenetic reconstruction were consistent with the theoretical prediction that the S-locus evolved before the M-locus. Evidence for re-use of the same gene highlights the potential role of gene duplication in the evolution of epistatic multilocus polymorphisms.