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A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains
The early development of aneuploidy from an accidental chromosome missegregation shows contrasting effects. On the one hand, it is associated with significant cellular stress and decreased fitness. On the other hand, it often carries a beneficial effect and provides a quick (but typically transient)...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104565/ https://www.ncbi.nlm.nih.gov/pubmed/37018197 http://dx.doi.org/10.1073/pnas.2211687120 |
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author | Pompei, Simone Cosentino Lagomarsino, Marco |
author_facet | Pompei, Simone Cosentino Lagomarsino, Marco |
author_sort | Pompei, Simone |
collection | PubMed |
description | The early development of aneuploidy from an accidental chromosome missegregation shows contrasting effects. On the one hand, it is associated with significant cellular stress and decreased fitness. On the other hand, it often carries a beneficial effect and provides a quick (but typically transient) solution to external stress. These apparently controversial trends emerge in several experimental contexts, particularly in the presence of duplicated chromosomes. However, we lack a mathematical evolutionary modeling framework that comprehensively captures these trends from the mutational dynamics and the trade-offs involved in the early stages of aneuploidy. Here, focusing on chromosome gains, we address this point by introducing a fitness model where a fitness cost of chromosome duplications is contrasted by a fitness advantage from the dosage of specific genes. The model successfully captures the experimentally measured probability of emergence of extra chromosomes in a laboratory evolution setup. Additionally, using phenotypic data collected in rich media, we explored the fitness landscape, finding evidence supporting the existence of a per-gene cost of extra chromosomes. Finally, we show that the substitution dynamics of our model, evaluated in the empirical fitness landscape, explains the relative abundance of duplicated chromosomes observed in yeast population genomics data. These findings lay a firm framework for the understanding of the establishment of newly duplicated chromosomes, providing testable quantitative predictions for future observations. |
format | Online Article Text |
id | pubmed-10104565 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-101045652023-10-05 A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains Pompei, Simone Cosentino Lagomarsino, Marco Proc Natl Acad Sci U S A Physical Sciences The early development of aneuploidy from an accidental chromosome missegregation shows contrasting effects. On the one hand, it is associated with significant cellular stress and decreased fitness. On the other hand, it often carries a beneficial effect and provides a quick (but typically transient) solution to external stress. These apparently controversial trends emerge in several experimental contexts, particularly in the presence of duplicated chromosomes. However, we lack a mathematical evolutionary modeling framework that comprehensively captures these trends from the mutational dynamics and the trade-offs involved in the early stages of aneuploidy. Here, focusing on chromosome gains, we address this point by introducing a fitness model where a fitness cost of chromosome duplications is contrasted by a fitness advantage from the dosage of specific genes. The model successfully captures the experimentally measured probability of emergence of extra chromosomes in a laboratory evolution setup. Additionally, using phenotypic data collected in rich media, we explored the fitness landscape, finding evidence supporting the existence of a per-gene cost of extra chromosomes. Finally, we show that the substitution dynamics of our model, evaluated in the empirical fitness landscape, explains the relative abundance of duplicated chromosomes observed in yeast population genomics data. These findings lay a firm framework for the understanding of the establishment of newly duplicated chromosomes, providing testable quantitative predictions for future observations. National Academy of Sciences 2023-04-05 2023-04-11 /pmc/articles/PMC10104565/ /pubmed/37018197 http://dx.doi.org/10.1073/pnas.2211687120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Physical Sciences Pompei, Simone Cosentino Lagomarsino, Marco A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
title | A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
title_full | A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
title_fullStr | A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
title_full_unstemmed | A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
title_short | A fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
title_sort | fitness trade-off explains the early fate of yeast aneuploids with chromosome gains |
topic | Physical Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104565/ https://www.ncbi.nlm.nih.gov/pubmed/37018197 http://dx.doi.org/10.1073/pnas.2211687120 |
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