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Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues

The ability of cells to translate different extracellular cues into different intracellular responses is vital for their survival in unpredictable environments. In Saccharomyces cerevisiae, cell polarity is modulated in response to environmental signals which allows cells to adopt varying morphologi...

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Autores principales: Kingma, Enzo, Diepeveen, Eveline T., Iñigo de la Cruz, Leila, Laan, Liedewij
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10382278/
https://www.ncbi.nlm.nih.gov/pubmed/37520345
http://dx.doi.org/10.3389/fmicb.2023.1076570
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author Kingma, Enzo
Diepeveen, Eveline T.
Iñigo de la Cruz, Leila
Laan, Liedewij
author_facet Kingma, Enzo
Diepeveen, Eveline T.
Iñigo de la Cruz, Leila
Laan, Liedewij
author_sort Kingma, Enzo
collection PubMed
description The ability of cells to translate different extracellular cues into different intracellular responses is vital for their survival in unpredictable environments. In Saccharomyces cerevisiae, cell polarity is modulated in response to environmental signals which allows cells to adopt varying morphologies in different external conditions. The responsiveness of cell polarity to extracellular cues depends on the integration of the molecular network that regulates polarity establishment with networks that signal environmental changes. The coupling of molecular networks often leads to pleiotropic interactions that can make it difficult to determine whether the ability to respond to external signals emerges as an evolutionary response to environmental challenges or as a result of pleiotropic interactions between traits. Here, we study how the propensity of the polarity network of S. cerevisiae to evolve toward a state that is responsive to extracellular cues depends on the complexity of the environment. We show that the deletion of two genes, BEM3 and NRP1, disrupts the ability of the polarity network to respond to cues that signal the onset of the diauxic shift. By combining experimental evolution with whole-genome sequencing, we find that the restoration of the responsiveness to these cues correlates with mutations in genes involved in the sphingolipid synthesis pathway and that these mutations frequently settle in evolving populations irrespective of the complexity of the selective environment. We conclude that pleiotropic interactions make a significant contribution to the evolution of networks that are responsive to extracellular cues.
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spelling pubmed-103822782023-07-30 Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues Kingma, Enzo Diepeveen, Eveline T. Iñigo de la Cruz, Leila Laan, Liedewij Front Microbiol Microbiology The ability of cells to translate different extracellular cues into different intracellular responses is vital for their survival in unpredictable environments. In Saccharomyces cerevisiae, cell polarity is modulated in response to environmental signals which allows cells to adopt varying morphologies in different external conditions. The responsiveness of cell polarity to extracellular cues depends on the integration of the molecular network that regulates polarity establishment with networks that signal environmental changes. The coupling of molecular networks often leads to pleiotropic interactions that can make it difficult to determine whether the ability to respond to external signals emerges as an evolutionary response to environmental challenges or as a result of pleiotropic interactions between traits. Here, we study how the propensity of the polarity network of S. cerevisiae to evolve toward a state that is responsive to extracellular cues depends on the complexity of the environment. We show that the deletion of two genes, BEM3 and NRP1, disrupts the ability of the polarity network to respond to cues that signal the onset of the diauxic shift. By combining experimental evolution with whole-genome sequencing, we find that the restoration of the responsiveness to these cues correlates with mutations in genes involved in the sphingolipid synthesis pathway and that these mutations frequently settle in evolving populations irrespective of the complexity of the selective environment. We conclude that pleiotropic interactions make a significant contribution to the evolution of networks that are responsive to extracellular cues. Frontiers Media S.A. 2023-07-14 /pmc/articles/PMC10382278/ /pubmed/37520345 http://dx.doi.org/10.3389/fmicb.2023.1076570 Text en Copyright © 2023 Kingma, Diepeveen, Iñigo de la Cruz and Laan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Kingma, Enzo
Diepeveen, Eveline T.
Iñigo de la Cruz, Leila
Laan, Liedewij
Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
title Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
title_full Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
title_fullStr Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
title_full_unstemmed Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
title_short Pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
title_sort pleiotropy drives evolutionary repair of the responsiveness of polarized cell growth to environmental cues
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10382278/
https://www.ncbi.nlm.nih.gov/pubmed/37520345
http://dx.doi.org/10.3389/fmicb.2023.1076570
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