Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis

Abstract Background Promoters serve as key elements in the regulation of gene transcription. In mammals, loop interactions between promoters and enhancers increase the complexity of the promoter-based regulatory networks. However, the identification of enhancer-promoter or promoter-related loops in...

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Main Authors: Dingyue Wang, Suxin Xiao, Jiayue Shu, Lingxiao Luo, Minqi Yang, Myriam Calonje, Hang He, Baoxing Song, Yue Zhou
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Genome Biology
Online Access:https://doi.org/10.1186/s13059-024-03465-7
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author Dingyue Wang
Suxin Xiao
Jiayue Shu
Lingxiao Luo
Minqi Yang
Myriam Calonje
Hang He
Baoxing Song
Yue Zhou
author_facet Dingyue Wang
Suxin Xiao
Jiayue Shu
Lingxiao Luo
Minqi Yang
Myriam Calonje
Hang He
Baoxing Song
Yue Zhou
author_sort Dingyue Wang
collection DOAJ
description Abstract Background Promoters serve as key elements in the regulation of gene transcription. In mammals, loop interactions between promoters and enhancers increase the complexity of the promoter-based regulatory networks. However, the identification of enhancer-promoter or promoter-related loops in Arabidopsis remains incomplete. Results Here, we use promoter capture Hi-C to identify promoter-related loops in Arabidopsis, which shows that gene body, proximal promoter, and intergenic regions can interact with promoters, potentially functioning as distal regulatory elements or enhancers. We find that promoter-related loops mainly repress gene transcription and are associated with ordered chromatin structures, such as topologically associating domains and fountains-chromatin structures not previously identified in Arabidopsis. Cohesin binds to the center of fountains and is involved in their formation. Moreover, fountain strength is positively correlated with the number of promoter-related loops, and the maintenance of these loops is linked to H3K4me3. In atxr3 mutants, which lack the major H3K4me3 methyltransferases in Arabidopsis, the number of promoter-related loops at fountains is reduced, leading to upregulation of fountain-regulated genes. Conclusions We identify promoter-related loops associated with ordered chromatin structures and reveal the molecular mechanisms involved in fountain formation and maintenance.
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institution Kabale University
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publishDate 2024-12-01
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spelling doaj-art-2093f47d2eae43b8a5dd0f6aed46af8a2025-01-05T12:31:56ZengBMCGenome Biology1474-760X2024-12-0125111810.1186/s13059-024-03465-7Promoter capture Hi-C identifies promoter-related loops and fountain structures in ArabidopsisDingyue Wang0Suxin Xiao1Jiayue Shu2Lingxiao Luo3Minqi Yang4Myriam Calonje5Hang He6Baoxing Song7Yue Zhou8State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityInstitute of Plant Biochemistry and Photosynthesis (IBVF-CSIC)State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityPeking University Institute of Advanced Agricultural SciencesState Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking UniversityAbstract Background Promoters serve as key elements in the regulation of gene transcription. In mammals, loop interactions between promoters and enhancers increase the complexity of the promoter-based regulatory networks. However, the identification of enhancer-promoter or promoter-related loops in Arabidopsis remains incomplete. Results Here, we use promoter capture Hi-C to identify promoter-related loops in Arabidopsis, which shows that gene body, proximal promoter, and intergenic regions can interact with promoters, potentially functioning as distal regulatory elements or enhancers. We find that promoter-related loops mainly repress gene transcription and are associated with ordered chromatin structures, such as topologically associating domains and fountains-chromatin structures not previously identified in Arabidopsis. Cohesin binds to the center of fountains and is involved in their formation. Moreover, fountain strength is positively correlated with the number of promoter-related loops, and the maintenance of these loops is linked to H3K4me3. In atxr3 mutants, which lack the major H3K4me3 methyltransferases in Arabidopsis, the number of promoter-related loops at fountains is reduced, leading to upregulation of fountain-regulated genes. Conclusions We identify promoter-related loops associated with ordered chromatin structures and reveal the molecular mechanisms involved in fountain formation and maintenance.https://doi.org/10.1186/s13059-024-03465-7
spellingShingle Dingyue Wang
Suxin Xiao
Jiayue Shu
Lingxiao Luo
Minqi Yang
Myriam Calonje
Hang He
Baoxing Song
Yue Zhou
Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis
Genome Biology
title Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis
title_full Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis
title_fullStr Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis
title_full_unstemmed Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis
title_short Promoter capture Hi-C identifies promoter-related loops and fountain structures in Arabidopsis
title_sort promoter capture hi c identifies promoter related loops and fountain structures in arabidopsis
url https://doi.org/10.1186/s13059-024-03465-7
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