Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL

Abstract Although chromatin organizations in plants have been dissected at the scales of compartments and topologically associating domain (TAD)-like domains, there remains a gap in resolving fine-scale structures. Here, we use Micro-C-XL, a high-throughput chromosome conformation capture (Hi-C)-bas...

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Main Authors: Linhua Sun, Jingru Zhou, Xiao Xu, Yi Liu, Ni Ma, Yutong Liu, Wenchao Nie, Ling Zou, Xing Wang Deng, Hang He
Format: Article
Language:English
Published: Nature Portfolio 2024-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-44347-z
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author Linhua Sun
Jingru Zhou
Xiao Xu
Yi Liu
Ni Ma
Yutong Liu
Wenchao Nie
Ling Zou
Xing Wang Deng
Hang He
author_facet Linhua Sun
Jingru Zhou
Xiao Xu
Yi Liu
Ni Ma
Yutong Liu
Wenchao Nie
Ling Zou
Xing Wang Deng
Hang He
author_sort Linhua Sun
collection DOAJ
description Abstract Although chromatin organizations in plants have been dissected at the scales of compartments and topologically associating domain (TAD)-like domains, there remains a gap in resolving fine-scale structures. Here, we use Micro-C-XL, a high-throughput chromosome conformation capture (Hi-C)-based technology that involves micrococcal nuclease (instead of restriction enzymes) and long cross-linkers, to dissect single nucleosome-resolution chromatin organization in Arabidopsis. Insulation analysis reveals more than 14,000 boundaries, which mostly include chromatin accessibility, epigenetic modifications, and transcription factors. Micro-C-XL reveals associations between RNA Pols and local chromatin organizations, suggesting that gene transcription substantially contributes to the establishment of local chromatin domains. By perturbing Pol II both genetically and chemically at the gene level, we confirm its function in regulating chromatin organization. Visible loops and stripes are assigned to super-enhancers and their targeted genes, thus providing direct insights for the identification and mechanistic analysis of distal CREs and their working modes in plants. We further investigate possible factors regulating these chromatin loops. Subsequently, we expand Micro-C-XL to soybean and rice. In summary, we use Micro-C-XL for analyses of plants, which reveal fine-scale chromatin organization and enhancer-promoter loops and provide insights regarding three-dimensional genomes in plants.
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spelling doaj.art-564cf49c667b43f2a62d21c20275c4222024-01-07T12:32:19ZengNature PortfolioNature Communications2041-17232024-01-0115111810.1038/s41467-023-44347-zMapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XLLinhua Sun0Jingru Zhou1Xiao Xu2Yi Liu3Ni Ma4Yutong Liu5Wenchao Nie6Ling Zou7Xing Wang Deng8Hang He9Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangPeking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangPeking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangSchool of Advanced Agriculture Sciences and School of Life Sciences, State Key Laboratory of Protein and Plant Gene Research, Peking UniversityPeking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangPeking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangWuhan Frasergen Bioinformatics Co., Ltd.Wuhan Frasergen Bioinformatics Co., Ltd.Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangPeking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at WeifangAbstract Although chromatin organizations in plants have been dissected at the scales of compartments and topologically associating domain (TAD)-like domains, there remains a gap in resolving fine-scale structures. Here, we use Micro-C-XL, a high-throughput chromosome conformation capture (Hi-C)-based technology that involves micrococcal nuclease (instead of restriction enzymes) and long cross-linkers, to dissect single nucleosome-resolution chromatin organization in Arabidopsis. Insulation analysis reveals more than 14,000 boundaries, which mostly include chromatin accessibility, epigenetic modifications, and transcription factors. Micro-C-XL reveals associations between RNA Pols and local chromatin organizations, suggesting that gene transcription substantially contributes to the establishment of local chromatin domains. By perturbing Pol II both genetically and chemically at the gene level, we confirm its function in regulating chromatin organization. Visible loops and stripes are assigned to super-enhancers and their targeted genes, thus providing direct insights for the identification and mechanistic analysis of distal CREs and their working modes in plants. We further investigate possible factors regulating these chromatin loops. Subsequently, we expand Micro-C-XL to soybean and rice. In summary, we use Micro-C-XL for analyses of plants, which reveal fine-scale chromatin organization and enhancer-promoter loops and provide insights regarding three-dimensional genomes in plants.https://doi.org/10.1038/s41467-023-44347-z
spellingShingle Linhua Sun
Jingru Zhou
Xiao Xu
Yi Liu
Ni Ma
Yutong Liu
Wenchao Nie
Ling Zou
Xing Wang Deng
Hang He
Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL
Nature Communications
title Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL
title_full Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL
title_fullStr Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL
title_full_unstemmed Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL
title_short Mapping nucleosome-resolution chromatin organization and enhancer-promoter loops in plants using Micro-C-XL
title_sort mapping nucleosome resolution chromatin organization and enhancer promoter loops in plants using micro c xl
url https://doi.org/10.1038/s41467-023-44347-z
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