ThePrimula edelbergii S-locus is an example of a jumping supergene

Abstract

AbstractResearch on supergenes, non-recombining genomic regions housing tightly linked genes that control complex phenotypes, has gained prominence in genomics, with supergenes having been described in most eukaryotic lineages. Heterostyly, a floral heteromorphism promoting outcrossing in several angiosperm families, is controlled by theS-locus supergene. Historically, theS-locus has been studied primarily in closely relatedPrimulaspecies and, more recently, in other groups that independently evolved heterostyly. However, it remains unknown whether genetic architecture and composition of theS-locus are maintained among species that share a common origin of heterostyly and subsequently diverged across larger time scales. To address this research gap, we present a chromosome-scale genome assembly ofPrimula edelbergii, a species that shares the same origin of heterostyly withPrimula veris(whoseS-locus has been characterized) but diverged from it ca. 18 million years ago. Comparative genomic analyses betweenP. edelbergiiandP. verisallowed us to show, for the first time, that theS-locus can ‘jump’ (i.e. translocate) between chromosomes. Additionally, we found that fourS-locus genes were maintained across time but were reshuffled within the supergene, seemingly without affecting their expression. Furthermore, we confirmed thatS-locus hemizygosity counteracts genetic degeneration, otherwise expected in supergenes. Finally, we investigatedP. edelbergiievolutionary history within Ericales in terms of whole genome duplications and transposable element accumulation. In summary, our work provides a valuable resource for comparative analyses aimed at investigating the genetics of heterostyly and the pivotal role of supergenes in shaping the evolution of complex phenotypes.