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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...

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Autores principales: Pei, Liuling, Huang, Xianhui, Liu, Zhenping, Tian, Xuehan, You, Jiaqi, Li, Jianying, Fang, David D., Lindsey, Keith, Zhu, Longfu, Zhang, Xianlong, Wang, Maojun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
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.
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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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