Centrophilic retrotransposon integration via targeting CENH3 chromatin in Arabidopsis

In organisms ranging from vertebrates to plants, major components of centromeres are rapidly-evolving repeat sequences, such as tandem repeats (TRs) and transposable elements (TEs). These repeats harbor centromere-specific histone H3 (CENH3), which also evolves rapidly. Complete centromere structures recently determined in human and Arabidopsis suggest frequent integration and purging of retrotransposons within the TR regions of centromeres. Despite the high impact of "centrophilic" retrotransposons on the paradox of rapid centromere evolution, the mechanisms involved in centromere targeting remain poorly understood in any organism. Here we show that both Ty3 and Ty1 LTR retrotransposons rapidly turnover within the centromeric TRs of Arabidopsis species. We demonstrate that the Ty1/Copia element Tal1 (Transposon of Arabidopsis lyrata 1) integrates de novo into regions occupied by CENH3 in A. thaliana, and that ectopic expansion of the CENH3 region results in spread of Tal1 integration regions. The integration spectra of chimeric TEs reveal the key structural variations responsible for contrasting chromatin-targeting specificities to centromeres versus gene-rich regions, which have recurrently converted during the evolution of these TEs. Our findings reveal the impact of centromeric chromatin on TE-mediated rapid centromere evolution, with relevance across eukaryotic genomes.