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Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation
BACKGROUND: Despite remarkable advances in our knowledge of epigenetically mediated transcriptional programming of cell differentiation in plants, little is known about chromatin topology and its functional implications in this process. RESULTS: To interrogate its significance, we establish the dyna...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812185/ https://www.ncbi.nlm.nih.gov/pubmed/35115029 http://dx.doi.org/10.1186/s13059-022-02616-y |
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author | Pei, Liuling Huang, Xianhui Liu, Zhenping Tian, Xuehan You, Jiaqi Li, Jianying Fang, David D. Lindsey, Keith Zhu, Longfu Zhang, Xianlong Wang, Maojun |
author_facet | Pei, Liuling Huang, Xianhui Liu, Zhenping Tian, Xuehan You, Jiaqi Li, Jianying Fang, David D. Lindsey, Keith Zhu, Longfu Zhang, Xianlong Wang, Maojun |
author_sort | Pei, Liuling |
collection | PubMed |
description | BACKGROUND: Despite remarkable advances in our knowledge of epigenetically mediated transcriptional programming of cell differentiation in plants, little is known about chromatin topology and its functional implications in this process. RESULTS: To interrogate its significance, we establish the dynamic three-dimensional (3D) genome architecture of the allotetraploid cotton fiber, representing a typical single cell undergoing staged development in plants. We show that the subgenome-relayed switching of the chromatin compartment from active to inactive is coupled with the silencing of developmentally repressed genes, pinpointing subgenome-coordinated contribution to fiber development. We identify 10,571 topologically associating domain-like (TAD-like) structures, of which 25.6% are specifically organized in different stages and 75.23% are subject to partition or fusion between two subgenomes. Notably, dissolution of intricate TAD-like structure cliques showing long-range interactions represents a prominent characteristic at the later developmental stage. Dynamic chromatin loops are found to mediate the rewiring of gene regulatory networks that exhibit a significant difference between the two subgenomes, implicating expression bias of homologous genes. CONCLUSIONS: This study sheds light on the spatial-temporal asymmetric chromatin structures of two subgenomes in the cotton fiber and offers a new insight into the regulatory orchestration of cell differentiation in plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02616-y. |
format | Online Article Text |
id | pubmed-8812185 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-88121852022-02-03 Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation Pei, Liuling Huang, Xianhui Liu, Zhenping Tian, Xuehan You, Jiaqi Li, Jianying Fang, David D. Lindsey, Keith Zhu, Longfu Zhang, Xianlong Wang, Maojun Genome Biol Research BACKGROUND: Despite remarkable advances in our knowledge of epigenetically mediated transcriptional programming of cell differentiation in plants, little is known about chromatin topology and its functional implications in this process. RESULTS: To interrogate its significance, we establish the dynamic three-dimensional (3D) genome architecture of the allotetraploid cotton fiber, representing a typical single cell undergoing staged development in plants. We show that the subgenome-relayed switching of the chromatin compartment from active to inactive is coupled with the silencing of developmentally repressed genes, pinpointing subgenome-coordinated contribution to fiber development. We identify 10,571 topologically associating domain-like (TAD-like) structures, of which 25.6% are specifically organized in different stages and 75.23% are subject to partition or fusion between two subgenomes. Notably, dissolution of intricate TAD-like structure cliques showing long-range interactions represents a prominent characteristic at the later developmental stage. Dynamic chromatin loops are found to mediate the rewiring of gene regulatory networks that exhibit a significant difference between the two subgenomes, implicating expression bias of homologous genes. CONCLUSIONS: This study sheds light on the spatial-temporal asymmetric chromatin structures of two subgenomes in the cotton fiber and offers a new insight into the regulatory orchestration of cell differentiation in plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02616-y. BioMed Central 2022-02-03 /pmc/articles/PMC8812185/ /pubmed/35115029 http://dx.doi.org/10.1186/s13059-022-02616-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Pei, Liuling Huang, Xianhui Liu, Zhenping Tian, Xuehan You, Jiaqi Li, Jianying Fang, David D. Lindsey, Keith Zhu, Longfu Zhang, Xianlong Wang, Maojun Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
title | Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
title_full | Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
title_fullStr | Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
title_full_unstemmed | Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
title_short | Dynamic 3D genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
title_sort | dynamic 3d genome architecture of cotton fiber reveals subgenome-coordinated chromatin topology for 4-staged single-cell differentiation |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812185/ https://www.ncbi.nlm.nih.gov/pubmed/35115029 http://dx.doi.org/10.1186/s13059-022-02616-y |
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