Primula vulgaris (primrose) genome assembly, annotation and gene expression, with comparative genomics on the heterostyly supergene

Abstract

Primula vulgaris (primrose) exhibits heterostyly: plants produce self-incompatible pin- or thrum-form flowers, with anthers and stigma at reciprocal heights. Darwin concluded that this arrangement promotes insect-mediated cross-pollination; later studies revealed control by a cluster of genes, or supergene, known as the S (Style length) locus. The P. vulgaris S locus is absent from pin plants and hemizygous in thrum plants (thrum-specific); mutation of S locus genes produces self-fertile homostyle flowers with anthers and stigma at equal heights. Here, we present a 411 Mb P. vulgaris genome assembly of a homozygous inbred long homostyle, representing ~87% of the genome. We annotate over 24,000 P. vulgaris genes, and reveal more genes up-regulated in thrum than pin flowers. We show reduced genomic read coverage across the S locus in other Primula species, including P. veris, where we define the conserved structure and expression of the S locus genes in thrum. Further analysis reveals the S locus has elevated repeat content (64%) compared to the wider genome (37%). Our studies suggest conservation of S locus genetic architecture in Primula, and provide a platform for identification and evolutionary analysis of the S locus and downstream targets that regulate heterostyly in diverse heterostylous species.

Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene

“…reside in this 280-kb segment based on its sequence in Primula vulgaris and the closely related Primula veris (25). This architecture of the S locus with a large hemizygous region appears to be conserved in five species belonging to different clades of the genus Primula (25), yet whether all five predicted genes are present at the S locus throughout the different Primula species is unknown.…”

“…Style length and female-compatibility type have never been genetically separated (20,21); by contrast, male compatibility is likely controlled by a locus distinct from A and P (21,22). At the molecular level, the dominant S-locus haplotype represents a roughly 280-kb-long genomic segment that is hemizygous; specifically, it is present only on the chromosome with the S haplotype but missing from the chromosome with the recessive s haplotype (23)(24)(25). Five genes have been predicted to…”

The Genomic Architecture and Evolutionary Fates of Supergenes

“…The extent of divergence in particular determines the suitability of different strategies. For instance, nucleotide divergence and population differentiation can be useful to identify homomorphic supergenes ( Tuttle et al 2016 ; Sun et al 2018 ), whereas repeat content analyses can facilitate detection of heteromorphic supergenes ( Stolle et al 2019 ), and read depth analyses have successfully identified supergenes with hemizygous regions ( Li et al 2016 , 2020 ; Cocker et al 2018 ) (see figure box 1 ). Table 1 summarizes analyses used for the identification and study of several supergenes.…”

Modeling the stepwise extension of recombination suppression on sex chromosomes and other supergenes through deleterious mutation sheltering

“…Sex chromosomes, mating-type chromosomes and supergenes in general are widespread in nature. These structures are defined by extensive regions of recombination suppression encompassing multiple genes, and they control iconic polymorphisms, such as sexual dimorphism or color polymorphism, in many organisms, including humans [1][2][3][4][5] . Supergenes, and sex chromosomes in particular, often display a stepwise extension of non-recombining regions, generating "evolutionary strata" of differentiation 4,[6][7][8][9][10] .…”