Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
- 1Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen 72076, Germany;
- 2National Key Laboratory of Plant Molecular Genetics (NKLPMG), CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology (SIPPE), Shanghai Institutes for Biological Sciences (SIBS), Shanghai 200032, People's Republic of China;
- 3University of Chinese Academy of Sciences, Shanghai 200032, People's Republic of China;
- 4Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen 72076, Germany
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↵5 These authors contributed equally to this work.
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.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.215186.116.
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Freely available online through the Genome Research Open Access option.
- Received August 28, 2016.
- Accepted April 5, 2017.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.