Plasticity and environment-specific relationships between gene expression and fitness in Saccharomyces cerevisiae

The environment influences how an organism's genotype determines its phenotype and how this phenotype affects its fitness. Here, to better understand this dual role of environment in the production and selection of phenotypic variation, we determined genotype-phenotype-fitness relationships for mutant strains of Saccharomyces cerevisiae in four environments. Specifically, we measured how promoter mutations of the metabolic gene TDH3 modified expression level and affected growth for four different carbon sources. In each environment, we observed a clear relationship between TDH3 expression level and fitness, but this relationship differed among environments. Mutations with similar effects on expression in different environments often had different effects on fitness and vice versa. Such environment-specific relationships between phenotype and fitness can shape the evolution of phenotypic plasticity. We also found that mutations disrupting binding sites for transcription factors had more variable effects on expression among environments than those disrupting the TATA box, which is part of the core promoter. However, mutations with the most environmentally variable effects on fitness were located in the TATA box, because of both the lack of plasticity of TATA box mutations and environment-specific fitness functions. This observation suggests that mutations affecting different molecular mechanisms contribute unequally to regulatory sequence evolution in changing environments.

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Publication Details

Journal
Nature Ecology & Evolution
Published
2024-11-13
DOI
https://doi.org/10.1038/s41559-024-02582-7
Citations
9
Primary Topic
Evolution and Genetic Dynamics
Type
article
Field-Weighted Citation Impact
4.95

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article

Plasticity and environment-specific relationships between gene expression and fitness in Saccharomyces cerevisiae

Patricia J. Wittkopp, Mohammad A. Siddiq, Fabien Duveau
9 citations
Nature Ecology & Evolution
Evolution and Genetic Dynamics
4.95
article

Plasticity and environment-specific relationships between gene expression and fitness in Saccharomyces cerevisiae

Patricia J. Wittkopp, Mohammad A. Siddiq, Fabien Duveau
article en
9 citations

Abstract

The environment influences how an organism's genotype determines its phenotype and how this phenotype affects its fitness. Here, to better understand this dual role of environment in the production and selection of phenotypic variation, we determined genotype-phenotype-fitness relationships for mutant strains of Saccharomyces cerevisiae in four environments. Specifically, we measured how promoter mutations of the metabolic gene TDH3 modified expression level and affected growth for four different carbon sources. In each environment, we observed a clear relationship between TDH3 expression level and fitness, but this relationship differed among environments. Mutations with similar effects on expression in different environments often had different effects on fitness and vice versa. Such environment-specific relationships between phenotype and fitness can shape the evolution of phenotypic plasticity. We also found that mutations disrupting binding sites for transcription factors had more variable effects on expression among environments than those disrupting the TATA box, which is part of the core promoter. However, mutations with the most environmentally variable effects on fitness were located in the TATA box, because of both the lack of plasticity of TATA box mutations and environment-specific fitness functions. This observation suggests that mutations affecting different molecular mechanisms contribute unequally to regulatory sequence evolution in changing environments.

Nature Ecology & EvolutionVol. 8(12)
Université Claude Bernard Lyon 1 (FR), École Normale Supérieure de Lyon (FR), Centre National de la Recherche Scientifique (FR), University of Michigan (US)
National Science Foundation, European Molecular Biology Organization, National Institutes of Health
Openalex Percentile: Top 4%
Evolution and Genetic Dynamics
4.95
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