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Improved use of a public good selects for the evolution of undifferentiated multicellularity

We do not know how or why multicellularity evolved. We used the budding yeast, Saccharomyces cerevisiae, to ask whether nutrients that must be digested extracellularly select for the evolution of undifferentiated multicellularity. Because yeast use invertase to hydrolyze sucrose extracellularly and...

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Detalles Bibliográficos
Autores principales: Koschwanez, John H, Foster, Kevin R, Murray, Andrew W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3614033/
https://www.ncbi.nlm.nih.gov/pubmed/23577233
http://dx.doi.org/10.7554/eLife.00367
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author Koschwanez, John H
Foster, Kevin R
Murray, Andrew W
author_facet Koschwanez, John H
Foster, Kevin R
Murray, Andrew W
author_sort Koschwanez, John H
collection PubMed
description We do not know how or why multicellularity evolved. We used the budding yeast, Saccharomyces cerevisiae, to ask whether nutrients that must be digested extracellularly select for the evolution of undifferentiated multicellularity. Because yeast use invertase to hydrolyze sucrose extracellularly and import the resulting monosaccharides, single cells cannot grow at low cell and sucrose concentrations. Three engineered strategies overcame this problem: forming multicellular clumps, importing sucrose before hydrolysis, and increasing invertase expression. We evolved populations in low sucrose to ask which strategy they would adopt. Of 12 successful clones, 11 formed multicellular clumps through incomplete cell separation, 10 increased invertase expression, none imported sucrose, and 11 increased hexose transporter expression, a strategy we had not engineered. Identifying causal mutations revealed genes and pathways, which frequently contributed to the evolved phenotype. Our study shows that combining rational design with experimental evolution can help evaluate hypotheses about evolutionary strategies. DOI: http://dx.doi.org/10.7554/eLife.00367.001
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spelling pubmed-36140332013-04-10 Improved use of a public good selects for the evolution of undifferentiated multicellularity Koschwanez, John H Foster, Kevin R Murray, Andrew W eLife Genomics and Evolutionary Biology We do not know how or why multicellularity evolved. We used the budding yeast, Saccharomyces cerevisiae, to ask whether nutrients that must be digested extracellularly select for the evolution of undifferentiated multicellularity. Because yeast use invertase to hydrolyze sucrose extracellularly and import the resulting monosaccharides, single cells cannot grow at low cell and sucrose concentrations. Three engineered strategies overcame this problem: forming multicellular clumps, importing sucrose before hydrolysis, and increasing invertase expression. We evolved populations in low sucrose to ask which strategy they would adopt. Of 12 successful clones, 11 formed multicellular clumps through incomplete cell separation, 10 increased invertase expression, none imported sucrose, and 11 increased hexose transporter expression, a strategy we had not engineered. Identifying causal mutations revealed genes and pathways, which frequently contributed to the evolved phenotype. Our study shows that combining rational design with experimental evolution can help evaluate hypotheses about evolutionary strategies. DOI: http://dx.doi.org/10.7554/eLife.00367.001 eLife Sciences Publications, Ltd 2013-04-02 /pmc/articles/PMC3614033/ /pubmed/23577233 http://dx.doi.org/10.7554/eLife.00367 Text en Copyright © 2013, Koschwanez et al http://creativecommons.org/licenses/by/3.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Genomics and Evolutionary Biology
Koschwanez, John H
Foster, Kevin R
Murray, Andrew W
Improved use of a public good selects for the evolution of undifferentiated multicellularity
title Improved use of a public good selects for the evolution of undifferentiated multicellularity
title_full Improved use of a public good selects for the evolution of undifferentiated multicellularity
title_fullStr Improved use of a public good selects for the evolution of undifferentiated multicellularity
title_full_unstemmed Improved use of a public good selects for the evolution of undifferentiated multicellularity
title_short Improved use of a public good selects for the evolution of undifferentiated multicellularity
title_sort improved use of a public good selects for the evolution of undifferentiated multicellularity
topic Genomics and Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3614033/
https://www.ncbi.nlm.nih.gov/pubmed/23577233
http://dx.doi.org/10.7554/eLife.00367
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