Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability

Abstract Living systems may have evolved probabilistic bet hedging strategies that generate cell‐to‐cell phenotypic diversity in anticipation of environmental catastrophes, as opposed to adaptation via a deterministic response to environmental changes. Evolution of bet hedging assumes that genotypes...

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Main Authors: Steffen Fehrmann, Hélène Bottin‐Duplus, Andri Leonidou, Esther Mollereau, Audrey Barthelaix, Wu Wei, Lars M Steinmetz, Gaël Yvert
Format: Article
Language:English
Published: Springer Nature 2013-10-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2013.53
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author Steffen Fehrmann
Hélène Bottin‐Duplus
Andri Leonidou
Esther Mollereau
Audrey Barthelaix
Wu Wei
Lars M Steinmetz
Gaël Yvert
author_facet Steffen Fehrmann
Hélène Bottin‐Duplus
Andri Leonidou
Esther Mollereau
Audrey Barthelaix
Wu Wei
Lars M Steinmetz
Gaël Yvert
author_sort Steffen Fehrmann
collection DOAJ
description Abstract Living systems may have evolved probabilistic bet hedging strategies that generate cell‐to‐cell phenotypic diversity in anticipation of environmental catastrophes, as opposed to adaptation via a deterministic response to environmental changes. Evolution of bet hedging assumes that genotypes segregating in natural populations modulate the level of intraclonal diversity, which so far has largely remained hypothetical. Using a fluorescent Pmet17‐GFP reporter, we mapped four genetic loci conferring to a wild yeast strain an elevated cell‐to‐cell variability in the expression of MET17, a gene regulated by the methionine pathway. A frameshift mutation in the Erc1p transmembrane transporter, probably resulting from a release of laboratory strains from negative selection, reduced Pmet17‐GFP expression variability. At a second locus, cis‐regulatory polymorphisms increased mean expression of the Mup1p methionine permease, causing increased expression variability in trans. These results demonstrate that an expression quantitative trait locus (eQTL) can simultaneously have a deterministic effect in cis and a probabilistic effect in trans. Our observations indicate that the evolution of transmembrane transporter genes can tune intraclonal variation and may therefore be implicated in both reactive and anticipatory strategies of adaptation.
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spelling doaj-art-104fc4ac07de42959bff305b281cbedf2025-08-20T03:46:34ZengSpringer NatureMolecular Systems Biology1744-42922013-10-019111710.1038/msb.2013.53Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variabilitySteffen Fehrmann0Hélène Bottin‐Duplus1Andri Leonidou2Esther Mollereau3Audrey Barthelaix4Wu Wei5Lars M Steinmetz6Gaël Yvert7Laboratoire de Biologie Moléculaire de la Cellule, Ecole Normale Supérieure de Lyon, CNRS, Université Lyon 1Laboratoire de Biologie Moléculaire de la Cellule, Ecole Normale Supérieure de Lyon, CNRS, Université Lyon 1Laboratoire de Biologie Moléculaire de la Cellule, Ecole Normale Supérieure de Lyon, CNRS, Université Lyon 1Laboratoire de Biologie Moléculaire de la Cellule, Ecole Normale Supérieure de Lyon, CNRS, Université Lyon 1Laboratoire de Biologie Moléculaire de la Cellule, Ecole Normale Supérieure de Lyon, CNRS, Université Lyon 1Genome Biology Unit, European Molecular Biology LaboratoryGenome Biology Unit, European Molecular Biology LaboratoryLaboratoire de Biologie Moléculaire de la Cellule, Ecole Normale Supérieure de Lyon, CNRS, Université Lyon 1Abstract Living systems may have evolved probabilistic bet hedging strategies that generate cell‐to‐cell phenotypic diversity in anticipation of environmental catastrophes, as opposed to adaptation via a deterministic response to environmental changes. Evolution of bet hedging assumes that genotypes segregating in natural populations modulate the level of intraclonal diversity, which so far has largely remained hypothetical. Using a fluorescent Pmet17‐GFP reporter, we mapped four genetic loci conferring to a wild yeast strain an elevated cell‐to‐cell variability in the expression of MET17, a gene regulated by the methionine pathway. A frameshift mutation in the Erc1p transmembrane transporter, probably resulting from a release of laboratory strains from negative selection, reduced Pmet17‐GFP expression variability. At a second locus, cis‐regulatory polymorphisms increased mean expression of the Mup1p methionine permease, causing increased expression variability in trans. These results demonstrate that an expression quantitative trait locus (eQTL) can simultaneously have a deterministic effect in cis and a probabilistic effect in trans. Our observations indicate that the evolution of transmembrane transporter genes can tune intraclonal variation and may therefore be implicated in both reactive and anticipatory strategies of adaptation.https://doi.org/10.1038/msb.2013.53bet hedgingcomplex traitmethioninenoise in gene expressionQTL
spellingShingle Steffen Fehrmann
Hélène Bottin‐Duplus
Andri Leonidou
Esther Mollereau
Audrey Barthelaix
Wu Wei
Lars M Steinmetz
Gaël Yvert
Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability
Molecular Systems Biology
bet hedging
complex trait
methionine
noise in gene expression
QTL
title Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability
title_full Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability
title_fullStr Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability
title_full_unstemmed Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability
title_short Natural sequence variants of yeast environmental sensors confer cell‐to‐cell expression variability
title_sort natural sequence variants of yeast environmental sensors confer cell to cell expression variability
topic bet hedging
complex trait
methionine
noise in gene expression
QTL
url https://doi.org/10.1038/msb.2013.53
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