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 associated small RNAs, suggesting a function in transposon biology.ResultsHere, we report the KNOT’s involvement in regulating invasive DNA elements. Transgenes can specifically interact with the KNOT, leading to perturbations of 3D nuclear organization, which correlates with the transgene’s expression: high KNOT interaction 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.ConclusionTransgene silencing can be connected to a specific feature of Arabidopsis 3D nuclear organization, namely the KNOT. KLS likely acts either independent of or prior to canonical silencing mechanisms, such that its characterization not only contributes to our understanding of chromosome folding but also provides valuable insights into how genomes are defended against invasive DNA elements.
Highlights
The three-dimensional (3D) organization of chromosomes is linked to epigenetic regulation and transcriptional activity
We previously proposed a role of the 3D genome in transposon biology in Arabidopsis [5]: Ten KNOT ENGAGED ELEMENTs (KEEs), transposable element (TE) insertion hotspots enriched in associated small RNAs, contact each other to form a nuclear
We observed an enrichment of interaction frequencies between the TRANSGENE INTEGRATON SITE (TIS) and constitutive heterochromatin of all five Arabidopsis chromosomes (Fig. 1b and Additional file 1: Figure S1A-B)
Summary
The three-dimensional (3D) organization of chromosomes is linked to epigenetic regulation and transcriptional activity. KEEs are enriched in transposable elements and associated small RNAs, suggesting a function in transposon biology. We previously proposed a role of the 3D genome in transposon biology in Arabidopsis [5]: Ten KNOT ENGAGED ELEMENTs (KEEs) (aka IHIs [6]), transposable element (TE) insertion hotspots enriched in associated small RNAs (sRNAs), contact each other to form a nuclear. Plants have evolved a balanced response to these elements, allowing for potential benefits, such as rapid adaptation to environmental challenges through controlled mobility [10]. Their uncontrolled proliferation and expression, which can lead to genome instability and potentially harmful ectopic gene expression, respectively, is counteracted by the silencing of invasive elements. With transgenes, silencing has been observed since the beginning of their use (reviewed in Kooter et al, [11]) and is of concern to both, gene
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