Abstract
Darwin's studies on heterostyly in Primula described two floral morphs, pin and thrum, with reciprocal anther and stigma heights that promote insect-mediated cross-pollination. This key innovation evolved independently in several angiosperm families. Subsequent studies on heterostyly in Primula contributed to the foundation of modern genetic theory and the neo-Darwinian synthesis. The established genetic model for Primula heterostyly involves a diallelic S locus comprising several genes, with rare recombination events that result in self-fertile homostyle flowers with anthers and stigma at the same height. Here we reveal the S locus supergene as a tightly linked cluster of thrum-specific genes that are absent in pins. We show that thrums are hemizygous not heterozygous for the S locus, which suggests that homostyles do not arise by recombination between S locus haplotypes as previously proposed. Duplication of a floral homeotic gene 51.7 million years (Myr) ago, followed by its neofunctionalization, created the current S locus assemblage which led to floral heteromorphy in Primula. Our findings provide new insights into the structure, function and evolution of this archetypal supergene.
Highlights
Evolved independently in at least 28 families of animal-pollinated angiosperms[1]
The s haplotype lacks a 278 kb sequence containing five thrumspecific genes present in thrum and homostyles; thrums are hemizygous not heterozygous for the S locus. We demonstrate that this 278 kb region is the only thrum-specific genomic region transcribed in flowers, and by genetic and natural population analyses demonstrate complete linkage to the S locus; our data indicate that homostyles cannot occur by recombination as proposed
Haplotype does not contain any additional genes compared to the long homostyle SLH1 haplotype. These analyses revealed 391 gene models that are uniquely expressed in thrums, and 270 gene models that are uniquely expressed in pins, but present in both pin and thrum genomes; these are candidates for direct or indirect targets of the S locus genes that control pin and thrum flower development
Summary
Darwin’s studies on heterostyly in Primula described two floral morphs, pin and thrum, with reciprocal anther and stigma heights that promote insect-mediated cross-pollination. This key innovation evolved independently in several angiosperm families. Established genetic model for Primula heterostyly involves a diallelic S locus comprising several genes, with rare recombination events that result in self-fertile homostyle flowers with anthers and stigma at the same height. We reveal the S locus supergene as a tightly-linked cluster of thrum-specific genes that are absent in pins. Duplication of a floral homeotic gene 51.7 MYA, followed by its neofunctionalisation, created the current S locus assemblage which led to floral heteromorphy in Primula. Our findings provide new insights into the structure, function and evolution of this archetypal supergene
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