Genomic evidence supports the genetic convergence of a supergene controlling the distylous floral syndrome

Abstract

Summary Heterostyly, a plant sexual polymorphism controlled by the S‐locus supergene, has evolved numerous times among angiosperm lineages and represents a classic example of convergent evolution in form and function. Determining whether underlying molecular convergence occurs could provide insights on constraints to floral evolution. Here, we investigated S‐locus genes in distylous Gelsemium (Gelsemiaceae) to determine whether there is evidence of molecular convergence with unrelated distylous species. We used several approaches, including anatomical measurements of sex‐organ development and transcriptome and whole‐genome sequencing, to identify components of the S‐locus supergene. We also performed evolutionary analysis with candidate S‐locus genes and compared them with those reported in Primula and Turnera. The candidate S‐locus supergene of Gelsemium contained four genes, of which three appear to have originated from gene duplication events within Gelsemiaceae. The style‐length genes GeCYP in Gelsemium and CYP734A50 in Primula likely arose from duplication of the same gene, CYP734A1. Three out of four S‐locus genes in Gelsemium elegans were hemizygous, as previously reported in Primula and Turnera. We provide genomic evidence on the genetic convergence of the supergene underlying distyly among distantly related angiosperm lineages and help to illuminate the genetic architecture involved in the evolution of heterostyly.

Haplotype‐resolved genome assembly provides insights into the evolution of S‐locus supergene in distylous Nymphoides indica

“…More recent molecular studies of several unrelated distylous genera, especially Primula (Nowak et al, 2015;Huu et al, 2016Huu et al, , 2020Huu et al, , 2022J. Li et al, 2016;Cocker et al, 2018;Potente et al, 2022a) and Turnera (Shore et al, 2019;Henning et al, 2020;Matzke et al, 2020), but also Fagopyrum (Yasui et al, 2012(Yasui et al, , 2016Takeshima et al, 2019), Linum (Ushijima et al, 2012;Gutierrez-Valencia et al, 2022), and Gelsemium (Zhao et al, 2023) have advanced understanding of the genetic architecture of the S-locus supergene in distylous plants (reviewed in Kappel et al, 2017;Barrett, 2019).…”

Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly

“…Brassinosteroids play essential roles in nearly all the processes of plant tissue growth and organ development with the important function of promoting organ elongation. To date, nearly all the relevant studies reported that the style-length regulation of distylous plants was dependent on BR-signaling pathways (e.g., Huu et al., 2016 in Primula ; Shore et al., 2019 in Turnera; Zhao et al., 2022 in Gelsemium ). Based on the functional enrichment analysis, we primarily focused on the expressional patterns of BR-related genes.…”

“…CYP734A50 involved in brassinosteroids degradation was the first identified “style-length gene” with experimental support, which has been reported in at least three Primula species ( Huu et al., 2016 ; Li et al., 2016 ; Burrows and McCubbin, 2018 ; Zhao et al., 2019 ). In the most recent study in Gelsemiaceae, we revealed that the style length was also controlled by a gene of the CYP734A subfamily, GeCYP ( Zhao et al., 2022 ).…”

“…To facilitate the sampling of RNA-sequencing materials, flower buds were dissected in the lab, and style length and anther position were measured by a digital caliper (573-S, Mitutoyo, Japan). The sampling method follows Shore et al (2019) and Zhao et al (2022). Three developmental stages were divided based on the elongation process of styles and corolla tubes as well as the relative position of stigma and anthers (see Results).…”

“…TsBAHD was expressed in the S-morph but was absent from the L-morph. Our recent studies in Gelsemium elegans (Gelsemiaceae) revealed that the style-length gene GeCYP and CYP734A50 in Primula may have arisen from duplication of CYP734A1 ( Zhao et al., 2022 ). These findings proposed a genetic convergence of the style-length regulation genes as they were hemizygous with the function of inactivating BRs ( Barrett, 2019 ; Zhao et al., 2022 ).…”