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Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery

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 chromati...

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Autores principales: Bi, Xiuli, Cheng, Ying-Juan, Hu, Bo, Ma, Xiaoli, Wu, Rui, Wang, Jia-Wei, Liu, Chang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5495068/
https://www.ncbi.nlm.nih.gov/pubmed/28385710
http://dx.doi.org/10.1101/gr.215186.116
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author Bi, Xiuli
Cheng, Ying-Juan
Hu, Bo
Ma, Xiaoli
Wu, Rui
Wang, Jia-Wei
Liu, Chang
author_facet Bi, Xiuli
Cheng, Ying-Juan
Hu, Bo
Ma, Xiaoli
Wu, Rui
Wang, Jia-Wei
Liu, Chang
author_sort Bi, Xiuli
collection PubMed
description 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.
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spelling pubmed-54950682017-07-18 Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery Bi, Xiuli Cheng, Ying-Juan Hu, Bo Ma, Xiaoli Wu, Rui Wang, Jia-Wei Liu, Chang Genome Res Research 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. Cold Spring Harbor Laboratory Press 2017-07 /pmc/articles/PMC5495068/ /pubmed/28385710 http://dx.doi.org/10.1101/gr.215186.116 Text en © 2017 Bi et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by/4.0/ 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/.
spellingShingle Research
Bi, Xiuli
Cheng, Ying-Juan
Hu, Bo
Ma, Xiaoli
Wu, Rui
Wang, Jia-Wei
Liu, Chang
Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
title Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
title_full Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
title_fullStr Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
title_full_unstemmed Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
title_short Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery
title_sort nonrandom domain organization of the arabidopsis genome at the nuclear periphery
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5495068/
https://www.ncbi.nlm.nih.gov/pubmed/28385710
http://dx.doi.org/10.1101/gr.215186.116
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