Rapid establishment of genetic incompatibility through natural epigenetic variation

Epigenetic variation is currently being investigated with the aim of deciphering its importance in both adaptation and evolution [1]. In plants, epimutations can underlie heritable phenotypic diversity [2-4], and epigenetic mechanisms might contribute to reproductive barriers between [5] or within species [6]. The extent of epigenetic variation begins to be appreciated in Arabidopsis [7], but the origin of natural epialleles and their impact in the wild remain largely unknown. Here we show that a genetic incompatibility among Arabidopsis thaliana strains is related to the epigenetic control of a pair of duplicate genes involved in fitness: a transposition event results in a rearranged paralogous structure that causes DNA methylation and transcriptional silencing of the other copy. We further show that this natural, strain-specific epiallele is stable over numerous generations even after removal of the duplicated, rearranged gene copy through crosses. Finally, we provide evidence that the rearranged gene copy triggers de novo DNA methylation and silencing of the unlinked native gene by RNA-directed DNA methylation. Our findings suggest an important role of naturally occurring epialleles originating from structural variation in rapidly establishing genetic incompatibilities following gene duplication events.