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Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae
Biological systems remain robust against certain genetic and environmental challenges. Robustness allows the exploration of ecological adaptations. It is unclear what factors contribute to increasing robustness. Gene duplication has been considered to increase genetic robustness through functional r...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory Press
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4216924/ https://www.ncbi.nlm.nih.gov/pubmed/25149527 http://dx.doi.org/10.1101/gr.176792.114 |
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author | Keane, Orla M. Toft, Christina Carretero-Paulet, Lorenzo Jones, Gary W. Fares, Mario A. |
author_facet | Keane, Orla M. Toft, Christina Carretero-Paulet, Lorenzo Jones, Gary W. Fares, Mario A. |
author_sort | Keane, Orla M. |
collection | PubMed |
description | Biological systems remain robust against certain genetic and environmental challenges. Robustness allows the exploration of ecological adaptations. It is unclear what factors contribute to increasing robustness. Gene duplication has been considered to increase genetic robustness through functional redundancy, accelerating the evolution of novel functions. However, recent findings have questioned the link between duplication and robustness. In particular, it remains elusive whether ancient duplicates still bear potential for innovation through preserved redundancy and robustness. Here we have investigated this question by evolving the yeast Saccharomyces cerevisiae for 2200 generations under conditions allowing the accumulation of deleterious mutations, and we put mechanisms of mutational robustness to a test. S. cerevisiae declined in fitness along the evolution experiment, but this decline decelerated in later passages, suggesting functional compensation of mutated genes. We resequenced 28 genomes from experimentally evolved S. cerevisiae lines and found more mutations in duplicates—mainly small-scale duplicates—than in singletons. Genetically interacting duplicates evolved similarly and fixed more amino acid–replacing mutations than expected. Regulatory robustness of the duplicates was supported by a larger enrichment for mutations at the promoters of duplicates than at those of singletons. Analyses of yeast gene expression conditions showed a larger variation in the duplicates’ expression than that of singletons under a range of stress conditions, sparking the idea that regulatory robustness allowed a wider range of phenotypic responses to environmental stresses, hence faster adaptations. Our data support the persistence of genetic and regulatory robustness in ancient duplicates and its role in adaptations to stresses. |
format | Online Article Text |
id | pubmed-4216924 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | Cold Spring Harbor Laboratory Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-42169242015-05-01 Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae Keane, Orla M. Toft, Christina Carretero-Paulet, Lorenzo Jones, Gary W. Fares, Mario A. Genome Res Research Biological systems remain robust against certain genetic and environmental challenges. Robustness allows the exploration of ecological adaptations. It is unclear what factors contribute to increasing robustness. Gene duplication has been considered to increase genetic robustness through functional redundancy, accelerating the evolution of novel functions. However, recent findings have questioned the link between duplication and robustness. In particular, it remains elusive whether ancient duplicates still bear potential for innovation through preserved redundancy and robustness. Here we have investigated this question by evolving the yeast Saccharomyces cerevisiae for 2200 generations under conditions allowing the accumulation of deleterious mutations, and we put mechanisms of mutational robustness to a test. S. cerevisiae declined in fitness along the evolution experiment, but this decline decelerated in later passages, suggesting functional compensation of mutated genes. We resequenced 28 genomes from experimentally evolved S. cerevisiae lines and found more mutations in duplicates—mainly small-scale duplicates—than in singletons. Genetically interacting duplicates evolved similarly and fixed more amino acid–replacing mutations than expected. Regulatory robustness of the duplicates was supported by a larger enrichment for mutations at the promoters of duplicates than at those of singletons. Analyses of yeast gene expression conditions showed a larger variation in the duplicates’ expression than that of singletons under a range of stress conditions, sparking the idea that regulatory robustness allowed a wider range of phenotypic responses to environmental stresses, hence faster adaptations. Our data support the persistence of genetic and regulatory robustness in ancient duplicates and its role in adaptations to stresses. Cold Spring Harbor Laboratory Press 2014-11 /pmc/articles/PMC4216924/ /pubmed/25149527 http://dx.doi.org/10.1101/gr.176792.114 Text en © 2014 Keane et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/. |
spellingShingle | Research Keane, Orla M. Toft, Christina Carretero-Paulet, Lorenzo Jones, Gary W. Fares, Mario A. Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae |
title | Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae |
title_full | Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae |
title_fullStr | Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae |
title_full_unstemmed | Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae |
title_short | Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae |
title_sort | preservation of genetic and regulatory robustness in ancient gene duplicates of saccharomyces cerevisiae |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4216924/ https://www.ncbi.nlm.nih.gov/pubmed/25149527 http://dx.doi.org/10.1101/gr.176792.114 |
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