Genetic causes and genomic consequences of breakdown of distyly in Linum trigynum

Distyly 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. Here, we aimed to study the genetic causes and genomic consequences of the shift to homostyly in Linum trigynum , which is closely related to distylous Linum tenue. Building on a high-quality genome assembly, we show that L. trigynum harbors a genomic region homologous to the dominant haplotype of the distyly supergene conferring long stamens and short styles in L. tenue , suggesting that loss of distyly first occurred in a short-styled individual. In contrast to homostylous Primula and Fagopyrum , L. trigynum harbors no fixed loss-of-function mutations in coding sequences of S- linked distyly candidate genes. Instead, floral gene expression analyses and controlled crosses suggest that mutations downregulating the S- linked LtWDR-44 candidate gene for male SI and/or anther height could underlie homostyly and self-compatibility (SC) in L. trigynum . Population genomic analyses of 224 whole-genome sequences further demonstrate that L. trigynum is highly self-fertilizing, exhibits significantly lower genetic diversity genome-wide, and is experiencing relaxed purifying selection and less frequent positive selection on nonsynonymous mutations relative to L. tenue . Our analyses shed light on the loss of distyly in L. trigynum , and advance our understanding of a common evolutionary transition in flowering plants. ### Competing Interest Statement The authors have declared no competing interest.