Cargando…
Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by...
Autores principales: | , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2017
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5449599/ https://www.ncbi.nlm.nih.gov/pubmed/28369650 http://dx.doi.org/10.1093/nar/gkx198 |
_version_ | 1783239814206717952 |
---|---|
author | Tsochatzidou, Maria Malliarou, Maria Papanikolaou, Nikolas Roca, Joaquim Nikolaou, Christoforos |
author_facet | Tsochatzidou, Maria Malliarou, Maria Papanikolaou, Nikolas Roca, Joaquim Nikolaou, Christoforos |
author_sort | Tsochatzidou, Maria |
collection | PubMed |
description | The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by the genome through the function of DNA topoisomerases, as has been shown in the concurrent transcriptional activation and suppression of genes upon transient deactivation of topoisomerase II (topoII). By analyzing a genome-wide transcription run-on experiment upon thermal inactivation of topoII in Saccharomyces cerevisiae we were able to define 116 gene clusters of consistent response (either positive or negative) to topological stress. A comprehensive analysis of these topologically co-regulated gene clusters reveals pronounced preferences regarding their functional, regulatory and structural attributes. Genes that negatively respond to topological stress, are positioned in gene-dense pericentromeric regions, are more conserved and associated to essential functions, while upregulated gene clusters are preferentially located in the gene-sparse nuclear periphery, associated with secondary functions and under complex regulatory control. We propose that genome architecture evolves with a core of essential genes occupying a compact genomic ‘old town’, whereas more recently acquired, condition-specific genes tend to be located in a more spacious ‘suburban’ genomic periphery. |
format | Online Article Text |
id | pubmed-5449599 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-54495992017-06-05 Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae Tsochatzidou, Maria Malliarou, Maria Papanikolaou, Nikolas Roca, Joaquim Nikolaou, Christoforos Nucleic Acids Res Gene regulation, Chromatin and Epigenetics The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by the genome through the function of DNA topoisomerases, as has been shown in the concurrent transcriptional activation and suppression of genes upon transient deactivation of topoisomerase II (topoII). By analyzing a genome-wide transcription run-on experiment upon thermal inactivation of topoII in Saccharomyces cerevisiae we were able to define 116 gene clusters of consistent response (either positive or negative) to topological stress. A comprehensive analysis of these topologically co-regulated gene clusters reveals pronounced preferences regarding their functional, regulatory and structural attributes. Genes that negatively respond to topological stress, are positioned in gene-dense pericentromeric regions, are more conserved and associated to essential functions, while upregulated gene clusters are preferentially located in the gene-sparse nuclear periphery, associated with secondary functions and under complex regulatory control. We propose that genome architecture evolves with a core of essential genes occupying a compact genomic ‘old town’, whereas more recently acquired, condition-specific genes tend to be located in a more spacious ‘suburban’ genomic periphery. Oxford University Press 2017-06-02 2017-03-23 /pmc/articles/PMC5449599/ /pubmed/28369650 http://dx.doi.org/10.1093/nar/gkx198 Text en © The Author(s) 2017. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Gene regulation, Chromatin and Epigenetics Tsochatzidou, Maria Malliarou, Maria Papanikolaou, Nikolas Roca, Joaquim Nikolaou, Christoforos Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae |
title | Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae |
title_full | Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae |
title_fullStr | Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae |
title_full_unstemmed | Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae |
title_short | Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae |
title_sort | genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of saccharomyces cerevisiae |
topic | Gene regulation, Chromatin and Epigenetics |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5449599/ https://www.ncbi.nlm.nih.gov/pubmed/28369650 http://dx.doi.org/10.1093/nar/gkx198 |
work_keys_str_mv | AT tsochatzidoumaria genomeurbanizationclustersoftopologicallycoregulatedgenesdelineatefunctionalcompartmentsinthegenomeofsaccharomycescerevisiae AT malliaroumaria genomeurbanizationclustersoftopologicallycoregulatedgenesdelineatefunctionalcompartmentsinthegenomeofsaccharomycescerevisiae AT papanikolaounikolas genomeurbanizationclustersoftopologicallycoregulatedgenesdelineatefunctionalcompartmentsinthegenomeofsaccharomycescerevisiae AT rocajoaquim genomeurbanizationclustersoftopologicallycoregulatedgenesdelineatefunctionalcompartmentsinthegenomeofsaccharomycescerevisiae AT nikolaouchristoforos genomeurbanizationclustersoftopologicallycoregulatedgenesdelineatefunctionalcompartmentsinthegenomeofsaccharomycescerevisiae |