Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast
The three-dimensional (3D) organization of chromosomes can influence transcription. However, the frequency and magnitude of these effects remain debated. To determine how changes in chromosome positioning affect transcription across thousands of genes with minimal perturbation, we characterized nucl...
| Autores: | , , , , , , , |
|---|---|
| Tipo de recurso: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2020 |
| País: | España |
| Institución: | Universitat Pompeu Fabra |
| Repositorio: | Repositorio Digital de la UPF |
| OAI Identifier: | oai:repositori.upf.edu:10230/43995 |
| Acceso en línea: | http://hdl.handle.net/10230/43995 http://dx.doi.org/10.1534/genetics.119.302978 |
| Access Level: | acceso abierto |
| Palabra clave: | Cromosomes Genomes Expressió gènica Llevats |
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Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| title |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| spellingShingle |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast Di Stefano, Marco Cromosomes Genomes Expressió gènica Llevats |
| title_short |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| title_full |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| title_fullStr |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| title_full_unstemmed |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| title_sort |
Impact of chromosome fusions on 3D genome organization and gene expression in budding yeast |
| dc.creator.none.fl_str_mv |
Di Stefano, Marco Di Giovanni, Francesca, 1985- Pozharskaia, Vasilia Gomar-Alba, Mercè Baù, Davide Carey, Lucas, 1980- Marti-Renom, Marc A. Mendoza, Manuel (Mendoza Palomares) |
| author |
Di Stefano, Marco |
| author_facet |
Di Stefano, Marco Di Giovanni, Francesca, 1985- Pozharskaia, Vasilia Gomar-Alba, Mercè Baù, Davide Carey, Lucas, 1980- Marti-Renom, Marc A. Mendoza, Manuel (Mendoza Palomares) |
| author_role |
author |
| author2 |
Di Giovanni, Francesca, 1985- Pozharskaia, Vasilia Gomar-Alba, Mercè Baù, Davide Carey, Lucas, 1980- Marti-Renom, Marc A. Mendoza, Manuel (Mendoza Palomares) |
| author2_role |
author author author author author author author |
| dc.subject.none.fl_str_mv |
Cromosomes Genomes Expressió gènica Llevats |
| topic |
Cromosomes Genomes Expressió gènica Llevats |
| description |
The three-dimensional (3D) organization of chromosomes can influence transcription. However, the frequency and magnitude of these effects remain debated. To determine how changes in chromosome positioning affect transcription across thousands of genes with minimal perturbation, we characterized nuclear organization and global gene expression in budding yeast containing chromosome fusions. We used computational modeling and single-cell imaging to determine chromosome positions, and integrated these data with genome-wide transcriptional profiles from RNA sequencing. We find that chromosome fusions dramatically alter 3D nuclear organization without leading to strong genome-wide changes in transcription. However, we observe a mild but significant and reproducible increase in the expression of genes displaced away from the periphery. The increase in transcription is inversely proportional to the propensity of a given locus to be at the nuclear periphery; for example, a 10% decrease in the propensity of a gene to reside at the nuclear envelope is accompanied by a 10% increase in gene expression. Modeling suggests that this is due to both deletion of telomeres and to displacement of genes relative to the nuclear periphery. These data suggest that basal transcriptional activity is sensitive to radial changes in gene position, and provide insight into the functional relevance of budding yeast chromosome-level 3D organization in gene expression. |
| publishDate |
2020 |
| dc.date.none.fl_str_mv |
2020 2020 2020 |
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info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion |
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article |
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publishedVersion |
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http://hdl.handle.net/10230/43995 http://dx.doi.org/10.1534/genetics.119.302978 |
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http://hdl.handle.net/10230/43995 http://dx.doi.org/10.1534/genetics.119.302978 |
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Inglés |
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Inglés |
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Genetics. 2020 Mar; 214(3) :651-67 info:eu-repo/grantAgreement/EC/H2020/676556 info:eu-repo/grantAgreement/ES/3PN/BFU2012-37162 info:eu-repo/grantAgreement/ES/1PE/BFU2015-68351-P info:eu-repo/grantAgreement/ES/2PE/BFU2017-85926-P |
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http://creativecommons.org/licenses/by/4.0/ info:eu-repo/semantics/openAccess |
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http://creativecommons.org/licenses/by/4.0/ |
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openAccess |
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application/pdf application/pdf |
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Genetics Society of America |
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Genetics Society of America |
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reponame:Repositorio Digital de la UPF instname:Universitat Pompeu Fabra |
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Universitat Pompeu Fabra |
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Repositorio Digital de la UPF |
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Repositorio Digital de la UPF |
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1869410929207148544 |
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Impact of chromosome fusions on 3D genome organization and gene expression in budding yeastDi Stefano, MarcoDi Giovanni, Francesca, 1985-Pozharskaia, VasiliaGomar-Alba, MercèBaù, DavideCarey, Lucas, 1980-Marti-Renom, Marc A.Mendoza, Manuel (Mendoza Palomares)CromosomesGenomesExpressió gènicaLlevatsThe three-dimensional (3D) organization of chromosomes can influence transcription. However, the frequency and magnitude of these effects remain debated. To determine how changes in chromosome positioning affect transcription across thousands of genes with minimal perturbation, we characterized nuclear organization and global gene expression in budding yeast containing chromosome fusions. We used computational modeling and single-cell imaging to determine chromosome positions, and integrated these data with genome-wide transcriptional profiles from RNA sequencing. We find that chromosome fusions dramatically alter 3D nuclear organization without leading to strong genome-wide changes in transcription. However, we observe a mild but significant and reproducible increase in the expression of genes displaced away from the periphery. The increase in transcription is inversely proportional to the propensity of a given locus to be at the nuclear periphery; for example, a 10% decrease in the propensity of a gene to reside at the nuclear envelope is accompanied by a 10% increase in gene expression. Modeling suggests that this is due to both deletion of telomeres and to displacement of genes relative to the nuclear periphery. These data suggest that basal transcriptional activity is sensitive to radial changes in gene position, and provide insight into the functional relevance of budding yeast chromosome-level 3D organization in gene expression.This project was supported by European Research Council Starting grant 2010-St-20091118 and Spanish Ministry of Economy and Competitiveness grant BFU2012-37162 to M.M., and grant ANR-10-LABX-0030-INRT, which is a French State fund managed by the Agence Nationale de la Recherche under the frame Programme Investissements d’Avenir ANR-10-IDEX-0002-02 to the Institut de Génétique et de Biologie Moléculaire et Cellulaire. L.B.C. was supported by the Agència de Gestió d’Ajuts Universitaris i de Recerca (grant 2014 SGR 0974), and the Spanish Ministerio de Economía y Competitividad and the European Regional Development Fund (FEDER) (grant BFU2015-68351-P). M.A.M.-R. was supported by the European Union’s Horizon 2020 research and innovation programme (grant agreement 676556) and the Spanish Ministry of Economy and Competitiveness (grant BFU2017-85926-P). We also acknowledge the support of the Spanish Ministry of Science and Innovation to the EMBL partnership, the ‘Centro de Excelencia Severo Ochoa 2013-2017’, SEV-2012-0208, the CERCA Programme/Generalitat de Catalunya, Spanish Ministry of Science and Innovation through the Instituto de Salud Carlos III, the Generalitat de Catalunya through Departament de Salut and Departament d’Empresa i Coneixement and the Co-financing by Spanish Ministry of Science and Innovation with funds from the European Regional Development Fund (ERDF) corresponding to the 2014-2020 Smart Growth Operating Program to the CRG. M.G.-A. is a recipient of a Postdoctoral Fellowship (APOSTD/2017/094) from the Generalitat ValencianaGenetics Society of America202020202020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/43995http://dx.doi.org/10.1534/genetics.119.302978reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésGenetics. 2020 Mar; 214(3) :651-67info:eu-repo/grantAgreement/EC/H2020/676556info:eu-repo/grantAgreement/ES/3PN/BFU2012-37162info:eu-repo/grantAgreement/ES/1PE/BFU2015-68351-Pinfo:eu-repo/grantAgreement/ES/2PE/BFU2017-85926-P© 2020 Marco Di Stefano et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly citedhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/439952026-06-12T07:21:37Z |
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15,811543 |