Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Keane, Orla M., Toft, Christina, Carretero-Paulet, Lorenzo, Jones, Gary W., Fares, Mario A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2014
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
_version_ 1782342329324011520
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
work_keys_str_mv AT keaneorlam preservationofgeneticandregulatoryrobustnessinancientgeneduplicatesofsaccharomycescerevisiae
AT toftchristina preservationofgeneticandregulatoryrobustnessinancientgeneduplicatesofsaccharomycescerevisiae
AT carreteropauletlorenzo preservationofgeneticandregulatoryrobustnessinancientgeneduplicatesofsaccharomycescerevisiae
AT jonesgaryw preservationofgeneticandregulatoryrobustnessinancientgeneduplicatesofsaccharomycescerevisiae
AT faresmarioa preservationofgeneticandregulatoryrobustnessinancientgeneduplicatesofsaccharomycescerevisiae