Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery

Abstract

The nuclear space is not a homogeneous biochemical environment. Many studies have demonstrated that the transcriptional activity of a gene is linked to its positioning within the nuclear space. Following the discovery of lamin-associated domains (LADs), which are transcriptionally repressed chromatin regions, the nonrandom positioning of chromatin at the nuclear periphery and its biological relevance have been studied extensively in animals. However, it remains unknown whether comparable chromatin organizations exist in plants. Here, using a strategy using restriction enzyme-mediated chromatin immunoprecipitation, we present genome-wide identification of nonrandom domain organization of chromatin at the peripheral zone of Arabidopsis thaliana nuclei. We show that in various tissues, 10%-20% of the regions on the chromosome arms are anchored at the nuclear periphery, and these regions largely overlap between different tissues. Unlike LADs in animals, the identified domains in plants are not gene-poor or A/T-rich. These domains are enriched with silenced protein-coding genes, transposable element genes, and heterochromatic marks, which collectively define a repressed environment. In addition, these domains strongly correlate with our genome-wide chromatin interaction data set (Hi-C) by largely explaining the patterns of chromatin compartments, revealed on Hi-C maps. Moreover, our results reveal a spatial compartment of different DNA methylation pathways that regulate silencing of transposable elements, where the CHH methylation of transposable elements located at the nuclear periphery and in the interior are preferentially mediated by CMT2 and DRM methyltransferases, respectively. Taken together, the results demonstrate functional partitioning of the Arabidopsis genome in the nuclear space.

Probing the 3D architecture of the plant nucleus with microscopy approaches: challenges and solutions

“…This raises intriguing questions regarding the evolution of the structure and function of the nuclear periphery in plant and animal cells [1,14]. Nevertheless, peripheral chromatin regions called Plant Lamina-Associated Domains (PLADs) were identified first as chromatin regions associated with NUP1/136, a component of the nuclear pore complex [15] and more recently with CRWN1, a component of the nucleoskeleton [16]. Like in animal cells, the nucleoskeleton of the plant nucleus may function to tether chromatin domainsas seen by ChIP and chromosome painting-that carry repressive features [15,16].…”

“…Nevertheless, peripheral chromatin regions called Plant Lamina-Associated Domains (PLADs) were identified first as chromatin regions associated with NUP1/136, a component of the nuclear pore complex [15] and more recently with CRWN1, a component of the nucleoskeleton [16]. Like in animal cells, the nucleoskeleton of the plant nucleus may function to tether chromatin domainsas seen by ChIP and chromosome painting-that carry repressive features [15,16]. Peripheral localisation of these domains seems dependent upon non-CG methylation [16], a DNA modification unique to plants, hence representing plant-specific novelties in LAD regulation and function.…”

“…Currently, SRM imaging of plant nuclear structures is in its infancy, but is eminently positioned to validate a functional model of the plant cell nucleus at the nanoscale level. Some key goals include:-imaging functional domains -LADs, NADs, knots and KEES, small-packaging units equivalent to animal TADs that are hypothesised by probabilistic models of interaction frequencies [5,15,18,111]; imaging the molecular connections between the chromatin, the nuclear periphery (matrix and envelope) and their supposed continuity with cytoplasmic domains [1]; and capturing fine-scale dynamics of nuclear architecture (e.g. spatial movements of gene loci, transcription complexes or nuclear bodies) in response to environmental signals or developmental cues [3,10,13,64].…”

The Chromatin-Associated Protein PWO1 Interacts with Plant Nuclear Lamin-like Components to Regulate Nuclear Size

“…LADs have not yet been identified in plants. A recent analysis identified the association of a plant nuclear pore component, with DNA/chromatin (Bi et al, 2017) but the extent of LADs in this data set is unclear and will require mapping of core-lamina-like associated proteins. Plants were long believed not to contain lamin homologs.…”

Meeting report – INDEPTH kick-off meeting

“…Chang Liu (University of Tübingen, Germany) showed how he compared results obtained with a restriction enzyme (RE)-mediated ChIP protocol and Hi-C data to obtain a better understanding of chromatin organisation at the nuclear periphery (Bi et al, 2017). He further showed unpublished data that was obtained using different fluorescence in situ hybridisation (FISH) probes to show altered chromatin organisation in plants lacking CRWN components of the nuclear lamina.…”