Transposable elements are prevalent vectors of transgenerational epigenetic inheritance in nature

Transgenerational epigenetic inheritance (TEI) mediated by transposable elements (TEs) is well established in plants. However, the molecular determinants and functional impact of this additional system of inheritance are poorly characterized. Through comprehensive analyses of severe DNA methylation loss over TEs in an experimental population and in >700 natural strains of Arabidopsis thaliana , we uncovered hundreds of TE epivariants in nature, most of which can be inherited independently of DNA sequence changes and thus are true epialleles. Furthermore, natural epivariants are enriched near genes and we uncovered a novel role for the Paf1 complex as a major facilitator of their prevalence. Conversely, related TE copies limit epiallelic variation, by producing the small RNAs that guide DNA methylation in trans . Crucially, natural epivariants mainly affect stress-responsive genes, making them unique targets for selection. Our findings therefore demonstrate that TEs are important mediators of transgenerational epigenetic variation in nature, with singular properties for plant adaptation.