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Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae)
BACKGROUND: Analysis of the relationship between chromosomal structural variation (synteny breaks) and 3D-chromatin architectural changes among closely related species has the potential to reveal causes and correlates between chromosomal change and chromatin remodeling. Of note, contrary to extensiv...
Autores principales: | , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10029228/ https://www.ncbi.nlm.nih.gov/pubmed/36941615 http://dx.doi.org/10.1186/s12915-023-01560-y |
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author | Li, Xiaochong Wang, Jinbin Yu, Yanan Li, Guo Wang, Jinpeng Li, Changping Zeng, Zixian Li, Ning Zhang, Zhibin Dong, Qianli Yu, Yiyang Wang, Xiaofei Wang, Tianya Grover, Corrinne E. Wang, Bin Liu, Bao Wendel, Jonathan F. Gong, Lei |
author_facet | Li, Xiaochong Wang, Jinbin Yu, Yanan Li, Guo Wang, Jinpeng Li, Changping Zeng, Zixian Li, Ning Zhang, Zhibin Dong, Qianli Yu, Yiyang Wang, Xiaofei Wang, Tianya Grover, Corrinne E. Wang, Bin Liu, Bao Wendel, Jonathan F. Gong, Lei |
author_sort | Li, Xiaochong |
collection | PubMed |
description | BACKGROUND: Analysis of the relationship between chromosomal structural variation (synteny breaks) and 3D-chromatin architectural changes among closely related species has the potential to reveal causes and correlates between chromosomal change and chromatin remodeling. Of note, contrary to extensive studies in animal species, the pace and pattern of chromatin architectural changes following the speciation of plants remain unexplored; moreover, there is little exploration of the occurrence of synteny breaks in the context of multiple genome topological hierarchies within the same model species. RESULTS: Here we used Hi-C and epigenomic analyses to characterize and compare the profiles of hierarchical chromatin architectural features in representative species of the cotton tribe (Gossypieae), including Gossypium arboreum, Gossypium raimondii, and Gossypioides kirkii, which differ with respect to chromosome rearrangements. We found that (i) overall chromatin architectural territories were preserved in Gossypioides and Gossypium, which was reflected in their similar intra-chromosomal contact patterns and spatial chromosomal distributions; (ii) the non-random preferential occurrence of synteny breaks in A compartment significantly associate with the B-to-A compartment switch in syntenic blocks flanking synteny breaks; (iii) synteny changes co-localize with open-chromatin boundaries of topologically associating domains, while TAD stabilization has a greater influence on regulating orthologous expression divergence than do rearrangements; and (iv) rearranged chromosome segments largely maintain ancestral in-cis interactions. CONCLUSIONS: Our findings provide insights into the non-random occurrence of epigenomic remodeling relative to the genomic landscape and its evolutionary and functional connections to alterations of hierarchical chromatin architecture, on a known evolutionary timescale. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01560-y. |
format | Online Article Text |
id | pubmed-10029228 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-100292282023-03-22 Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) Li, Xiaochong Wang, Jinbin Yu, Yanan Li, Guo Wang, Jinpeng Li, Changping Zeng, Zixian Li, Ning Zhang, Zhibin Dong, Qianli Yu, Yiyang Wang, Xiaofei Wang, Tianya Grover, Corrinne E. Wang, Bin Liu, Bao Wendel, Jonathan F. Gong, Lei BMC Biol Research Article BACKGROUND: Analysis of the relationship between chromosomal structural variation (synteny breaks) and 3D-chromatin architectural changes among closely related species has the potential to reveal causes and correlates between chromosomal change and chromatin remodeling. Of note, contrary to extensive studies in animal species, the pace and pattern of chromatin architectural changes following the speciation of plants remain unexplored; moreover, there is little exploration of the occurrence of synteny breaks in the context of multiple genome topological hierarchies within the same model species. RESULTS: Here we used Hi-C and epigenomic analyses to characterize and compare the profiles of hierarchical chromatin architectural features in representative species of the cotton tribe (Gossypieae), including Gossypium arboreum, Gossypium raimondii, and Gossypioides kirkii, which differ with respect to chromosome rearrangements. We found that (i) overall chromatin architectural territories were preserved in Gossypioides and Gossypium, which was reflected in their similar intra-chromosomal contact patterns and spatial chromosomal distributions; (ii) the non-random preferential occurrence of synteny breaks in A compartment significantly associate with the B-to-A compartment switch in syntenic blocks flanking synteny breaks; (iii) synteny changes co-localize with open-chromatin boundaries of topologically associating domains, while TAD stabilization has a greater influence on regulating orthologous expression divergence than do rearrangements; and (iv) rearranged chromosome segments largely maintain ancestral in-cis interactions. CONCLUSIONS: Our findings provide insights into the non-random occurrence of epigenomic remodeling relative to the genomic landscape and its evolutionary and functional connections to alterations of hierarchical chromatin architecture, on a known evolutionary timescale. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01560-y. BioMed Central 2023-03-20 /pmc/articles/PMC10029228/ /pubmed/36941615 http://dx.doi.org/10.1186/s12915-023-01560-y Text en © The Author(s) 2023 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 Article Li, Xiaochong Wang, Jinbin Yu, Yanan Li, Guo Wang, Jinpeng Li, Changping Zeng, Zixian Li, Ning Zhang, Zhibin Dong, Qianli Yu, Yiyang Wang, Xiaofei Wang, Tianya Grover, Corrinne E. Wang, Bin Liu, Bao Wendel, Jonathan F. Gong, Lei Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) |
title | Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) |
title_full | Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) |
title_fullStr | Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) |
title_full_unstemmed | Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) |
title_short | Genomic rearrangements and evolutionary changes in 3D chromatin topologies in the cotton tribe (Gossypieae) |
title_sort | genomic rearrangements and evolutionary changes in 3d chromatin topologies in the cotton tribe (gossypieae) |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10029228/ https://www.ncbi.nlm.nih.gov/pubmed/36941615 http://dx.doi.org/10.1186/s12915-023-01560-y |
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