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Molecular signatures of aneuploidy-driven adaptive evolution

Alteration of normal ploidy (aneuploidy) can have a number of opposing effects, such as unbalancing protein abundances and inhibiting cell growth but also accelerating genetic diversification and rapid adaptation. The interplay of these detrimental and beneficial effects remains puzzling. Here, to u...

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Autores principales: Kaya, Alaattin, Mariotti, Marco, Tyshkovskiy, Alexander, Zhou, Xuming, Hulke, Michelle L., Ma, Siming, Gerashchenko, Maxim V., Koren, Amnon, Gladyshev, Vadim N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6992709/
https://www.ncbi.nlm.nih.gov/pubmed/32001709
http://dx.doi.org/10.1038/s41467-019-13669-2
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author Kaya, Alaattin
Mariotti, Marco
Tyshkovskiy, Alexander
Zhou, Xuming
Hulke, Michelle L.
Ma, Siming
Gerashchenko, Maxim V.
Koren, Amnon
Gladyshev, Vadim N.
author_facet Kaya, Alaattin
Mariotti, Marco
Tyshkovskiy, Alexander
Zhou, Xuming
Hulke, Michelle L.
Ma, Siming
Gerashchenko, Maxim V.
Koren, Amnon
Gladyshev, Vadim N.
author_sort Kaya, Alaattin
collection PubMed
description Alteration of normal ploidy (aneuploidy) can have a number of opposing effects, such as unbalancing protein abundances and inhibiting cell growth but also accelerating genetic diversification and rapid adaptation. The interplay of these detrimental and beneficial effects remains puzzling. Here, to understand how cells develop tolerance to aneuploidy, we subject disomic (i.e. with an extra chromosome copy) strains of yeast to long-term experimental evolution under strong selection, by forcing disomy maintenance and daily population dilution. We characterize mutations, karyotype alterations and gene expression changes, and dissect the associated molecular strategies. Cells with different extra chromosomes accumulated mutations at distinct rates and displayed diverse adaptive events. They tended to evolve towards normal ploidy through chromosomal DNA loss and gene expression changes. We identify genes with recurrent mutations and altered expression in multiple lines, revealing a variant that improves growth under genotoxic stresses. These findings support rapid evolvability of disomic strains that can be used to characterize fitness effects of mutations under different stress conditions.
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spelling pubmed-69927092020-02-03 Molecular signatures of aneuploidy-driven adaptive evolution Kaya, Alaattin Mariotti, Marco Tyshkovskiy, Alexander Zhou, Xuming Hulke, Michelle L. Ma, Siming Gerashchenko, Maxim V. Koren, Amnon Gladyshev, Vadim N. Nat Commun Article Alteration of normal ploidy (aneuploidy) can have a number of opposing effects, such as unbalancing protein abundances and inhibiting cell growth but also accelerating genetic diversification and rapid adaptation. The interplay of these detrimental and beneficial effects remains puzzling. Here, to understand how cells develop tolerance to aneuploidy, we subject disomic (i.e. with an extra chromosome copy) strains of yeast to long-term experimental evolution under strong selection, by forcing disomy maintenance and daily population dilution. We characterize mutations, karyotype alterations and gene expression changes, and dissect the associated molecular strategies. Cells with different extra chromosomes accumulated mutations at distinct rates and displayed diverse adaptive events. They tended to evolve towards normal ploidy through chromosomal DNA loss and gene expression changes. We identify genes with recurrent mutations and altered expression in multiple lines, revealing a variant that improves growth under genotoxic stresses. These findings support rapid evolvability of disomic strains that can be used to characterize fitness effects of mutations under different stress conditions. Nature Publishing Group UK 2020-01-30 /pmc/articles/PMC6992709/ /pubmed/32001709 http://dx.doi.org/10.1038/s41467-019-13669-2 Text en © The Author(s) 2020 Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Kaya, Alaattin
Mariotti, Marco
Tyshkovskiy, Alexander
Zhou, Xuming
Hulke, Michelle L.
Ma, Siming
Gerashchenko, Maxim V.
Koren, Amnon
Gladyshev, Vadim N.
Molecular signatures of aneuploidy-driven adaptive evolution
title Molecular signatures of aneuploidy-driven adaptive evolution
title_full Molecular signatures of aneuploidy-driven adaptive evolution
title_fullStr Molecular signatures of aneuploidy-driven adaptive evolution
title_full_unstemmed Molecular signatures of aneuploidy-driven adaptive evolution
title_short Molecular signatures of aneuploidy-driven adaptive evolution
title_sort molecular signatures of aneuploidy-driven adaptive evolution
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6992709/
https://www.ncbi.nlm.nih.gov/pubmed/32001709
http://dx.doi.org/10.1038/s41467-019-13669-2
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