Comparative Genomics Elucidates the Origin of a Supergene Controlling Floral Heteromorphism

Abstract

Supergenes are non-recombining genomic regions ensuring the co-inheritance of multiple, co-adapted genes. Despite the importance of supergenes in adaptation, little is known on how they originate. A classic example of supergene is the S locus controlling heterostyly, a floral heteromorphism occurring in 28 angiosperm families. In Primula, heterostyly is characterized by the co-occurrence of two complementary, self-incompatible floral morphs and is controlled by 5 genes clustered in the hemizygous, ca. 300-kbp S locus. Here we present the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip). By leveraging the high contiguity of the P. veris assembly and comparative genomic analyses, we demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations. Furthermore, we discovered a new whole-genome duplication in Ericales that is specific to the Primula lineage. We also propose a mechanism for the origin of S-locus hemizygosity via nonhomologous recombination involving the newly discovered two pairs of CFB genes flanking the S locus. Finally, we detected only weak signatures of degeneration in the S locus, as predicted for hemizygous supergenes. The present study provides a useful resource for future research addressing key questions on the evolution of supergenes in general and the S locus in particular: How do supergenes arise? What is the role of genome architecture in the evolution of complex adaptations? Is the molecular architecture of heterostyly supergenes across angiosperms similar to that of Primula?

Genomic analyses of theLinumdistyly supergene reveal convergent evolution at the molecular level

“…At the Linum distyly supergene, we observed an enrichment of TEs, but no signature of relaxed purifying selection on S- linked genes. This result mirrors recent findings in Primula (Cocker et al 2018; Potente et al 2022) and while efficient selection in hemizygous regions could contribute to this pattern, sequence constraints on S- linked genes resulting from their role in distyly could also be involved.…”

“…Taken together, our findings in combination with those of earlier studies indicate remarkable convergence with respect to the genetic architecture, origin and evolution of distyly supergenes in Linum, Primula (Li et al 2016; Cocker et al 2018; Huu et al 2020; Potente et al 2022) and Turnera (Shore et al 2019), and suggest that convergence may extend to the level of molecular pathways controlling distyly. Our chromosome-level genome assembly and detailed characterization of the Linum distyly S- locus augment our knowledge on the evolution of S -loci across distylous lineages and motivate further work to better understand the conditions favoring similar mechanisms and processes for the origin and maintenance of supergenes.…”

“…The finding that the L. tenue S- locus harbors LtTSS1 , an ortholog of the L. grandiflorum thrum-specific and S -linked gene TSS1 (Ushijima et al 2012; Ushijima et al 2015) suggests that presence-absence polymorphism at the S- locus could have been retained for at least 30-40 million years, since the divergence of L. tenue and L. grandiflorum (Ruiz-Martín et al 2018; Maguilla et al 2021). Furthermore, our finding that paralogs of S- linked genes are found in disparate genomic locations both in L. tenue and in outgroups suggests that the S- locus gene set evolved in a stepwise process involving several gene duplications and translocations, similar to the Primula S- locus (Huu et al 2020; Potente et al 2022). These results imply that the presence-absence polymorphism at the Linum distyly S- locus likely did not originate through one large segmental duplication.…”

“…Hemizygosity in thrums could elegantly explain both the lack of recombination and dominance of the thrum S- locus allele, but structural variation could potentially constitute either a cause or a consequence of suppressed recombination. In Primula , the location of the S -locus in a pericentromeric region (Li et al 2015; Kappel et al 2017; Potente et al 2022) might have favored supergene formation if recombination rates were ancestrally low in this region. In contrast, at the Linum distyly supergene, we observed localized recombination suppression largely coinciding with the boundaries of the indel, without broad-scale recombination suppression surrounding the supergene.…”

“…The hemizygous region harbors CYP734A50, a gene that simultaneously controls the position of the style (Huu et al 2016) and female self-incompatibility (Huu et al 2022), and GLO T , which determines anther position (Huu et al 2020). The presence of paralogs of S-linked genes at different genomic locations suggests stepwise assembly of the genes at the S-locus (Huu et al 2020;Potente et al 2022). Subsequently, hemizygosity and S-linked candidate genes for style elongation have also been documented in distylous Turnera (Shore et al 2019;Matzke et al 2021).…”