Xue Haoran, Gong Yunchen, Wright Stephen I, Barrett Spencer C H
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario M5S 3B2, Canada.
Institute for Biochemistry and Biology, University of Potsdam, Potsdam-Golm 14476, Germany.
Mol Biol Evol. 2025 Jul 30;42(8). doi: 10.1093/molbev/msaf170.
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.
三型花柱是被子植物的一种性多态现象，其特征是存在三种花形态，通过形态间异交交配导致的负频率依赖选择在种群中得以维持。这些花形态具有由两个上位性相互作用的双等位基因座（S和M）控制的互逆柱头和花药高度。尽管在确定控制相关异型花柱多态现象二型花柱的遗传结构和基因方面已经取得了相当大的进展，但我们对三型花柱遗传基础的这些方面的理解尚未得到研究。在这里，我们通过研究 paniculata（雨久花科）的三型花柱的基因组基础来填补这一知识空白，paniculata是一种一年生蜜蜂传粉的草本植物，原产于新热带地区，主要分布在巴西东北部。通过 paniculata的染色体水平基因组组装，我们在同一条染色体上低重组的一个大区域两侧鉴定出了S和M基因座。S基因座由两种不同的单倍型组成：具有三个S单倍型特异性基因的S单倍型（2.51 Mb）和具有五个s单倍型特异性基因的s单倍型（596 kb）。两个S单倍型特异性基因，LAZY1-S和HRGP-S，分别在花柱和雄蕊中特异性表达，使其成为三型花柱候选基因，并为该基因座作为半合子超基因发挥作用提供了证据。M基因座包含一个与LAZY1-S同源的基因（LAZY1-M），存在于M单倍型中，但在m单倍型中不存在。基因年龄估计和系统发育重建与S基因座比M基因座进化更早的理论预测一致。同一基因重复利用的证据突出了基因复制在上位性多基因座多态性进化中的潜在作用。
