Transposon accumulation lines uncover strong chromatin-driven integration bias towards genes

Inherited transposition events are important drivers of genome evolution but because mobilization of transposable elements (TEs) is typically rare, its impact on the creation of genetic variation remains poorly characterized. Here, we used A. thaliana epigenetic recombinant inbred lines (epiRILs) to characterize in depth >8000 de novo insertions that have accumulated for two DNA transposon and one LTR-retrotransposon families also active in nature. Integration was strongly biased towards genes, with evident deleterious effects. Biases were associated with distinct chromatin features for the three TE families and we demonstrate that the preferential integration of COPIA retrotransposons within environmentally responsive genes is promoted as well as guided by the histone variant H2A.Z. Furthermore, we show that H2A.Z-dependent integration of Ty1/Copia retrotransposons is ancestral and evolutionary conserved from yeast to plants. Finally, we uncover an important role for epigenetic silencing in exacerbating or alleviating the effects of new TE insertions on genes. These findings establish chromatin as a major determinant of the spectrum and functional impact of TE-generated mutations, with important implications for adaptation and evolution.