Invasive DNA elements modify nuclear architecture by KNOT-Linked Silencing in plants

Abstract

BackgroundThe three-dimensional (3D) organization of chromosomes is linked to epigenetic regulation and transcriptional activity. However, only few functional features of 3D chromatin architecture have been described to date. The KNOT is a 3D chromatin structure in Arabidopsis, comprising 10 interacting genomic regions termed KNOT ENGAGED ELEMENTs (KEEs). KEEs are enriched in transposable elements and small RNAs, suggesting a function in transposon biology.\n\nResultsHere, we report the KNOTs involvement in regulating invasive DNA elements. Transgenes can specifically interact with the KNOT, leading to perturbations of 3D nuclear organization, which correlates with the transgenes expression: high KNOT-contact frequencies are associated with transgene silencing. KNOT-Linked Silencing (KLS) cannot readily be connected to canonical silencing mechanisms, such as RNA-directed DNA methylation and post-transcriptional gene silencing, as both cytosine methylation and small RNA abundance do not correlate with KLS. Furthermore, KLS exhibits paramutation-like behavior, as silenced transgenes can lead to the silencing of active transgenes in trans.\n\nConclusionTransgene silencing can be readily connected to a specific feature of Arabidopsis 3D nuclear organization, namely the KNOT. KLS likely acts either independent or prior canonical silencing mechanisms and, hence, its characterization promises to not only contribute to our understanding of chromosome folding but moreover provides valuable insight into how genomes are defended against invasive DNA elements.