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 has 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. With chromosome-level genome assemblies of E. paniculata, we dentified 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 reuse of the same gene highlights the potential role of gene duplication in the evolution of epistatic multilocus polymorphisms.