Insertional polymorphisms of Inverted-Repeated sequences near coding genes shape chromatin topology and phenotypic traits in plants

Transposons are mobile elements in the eukaryotic genomes that are commonly silenced to protect genome integrity. In plants, transposable elements (TEs) can be reactivated during stress conditions, inserted into gene-rich regions, and trigger adaptative changes. TE-derived inverted repeated (IR) sequences are commonly detected near genes in plants, affect hosting gene expression and were proposed as essential elements during adaptation. However, the molecular mechanisms by which these IRs control gene expression is unclear in most cases. Here, we identified hundreds of IR near genes in the Arabidopsis thaliana genome that the RNAPII transcribes to produce 24 nt small RNAs that trigger the methylation of the IR coding region. The expression of these IR is associated with drastic changes in the local 3D chromatin organization, which alter the expression pattern of the hosting genes. We found numerous insertional polymorphisms within the identified IRs between Arabidopsis ecotypes. Capture-C sequencing experiments revealed that such variation in the IR content produces changes in short-range chromatin interaction that translate into specific gene expression patterns. Furthermore, CRISPR/CAS9-mediated disruption of IR not only leads to a switch in the genome topology and gene expression but also impacts the plants' phenotype. Altogether our data demonstrate that the insertion of an IR near a gene during evolution provides an anchor point for chromatin interactions that profoundly impact the hosting loci activity. This turn IRs into powerful elements with the potential to produce quick and drastic adaptative changes.