Genomic analyses elucidate the causes and consequences of breakdown of distyly inLinum trigynum

Abstract

AbstractDistyly is an iconic floral polymorphism governed by a supergene, which promotes efficient pollen transfer and outcrossing through reciprocal differences in the position of sexual organs in flowers, often coupled with heteromorphic self-incompatibility (SI). Distyly has evolved convergently in multiple flowering plant lineages, but has also broken down repeatedly, often resulting in homostylous, self-compatible populations with elevated rates of self-fertilization relative to their distylous ancestors. Here, we aimed to study the causes and consequences of the shift to homostyly inLinum trigynum, which is closely related to distylousLinum tenue.Building on a high-quality genome assembly, we show thatL. trigynumharbors a genomic region homologous to the dominant haplotype of the distyly supergene inL. tenue, suggesting that loss of distyly first occurred in a short-styled individual. In contrast to homostylousPrimulaandFagopyrum,L. trigynumharbors no fixed loss-of-function mutations in coding sequences ofS-linked distyly candidate genes. Instead, floral gene expression analyses and controlled crosses suggest that mutations downregulating theS-linkedLtWDR-44candidate gene for male SI and/or anther height could underlie homostyly inL. trigynum. Population genomic analyses of 224 whole-genome sequences further demonstrate thatL. trigynumis highly self-fertilizing, exhibits significantly lower genetic diversity genome-wide and is experiencing relaxed purifying selection on nonsynonymous mutations relative toL. tenue, despite the relatively recent split ofL. trigynumandL. tenue. Our analyses elucidate the tempo and mode of loss of distyly inL. trigynum, and advances our understanding of a common evolutionary transition in flowering plants.