FLO1 Is a Variable Green Beard Gene that Drives Biofilm-like Cooperation in Budding Yeast

Scott Smukalla; Marina Caldara; Nathalie Pochet; Anne Beauvais; Stephanie Guadagnini; Chen Yan; Marcelo D. Vinces; An Jansen; Marie Christine Prevost; Jean Paul Latgé; Gerald R. Fink; Kevin R. Foster; Kevin J. Verstrepen

doi:10.1016/j.cell.2008.09.037

FLO1 Is a Variable Green Beard Gene that Drives Biofilm-like Cooperation in Budding Yeast

Scott Smukalla, Marina Caldara, Nathalie Pochet, Anne Beauvais, Stephanie Guadagnini, Chen Yan, Marcelo D. Vinces, An Jansen, Marie Christine Prevost, Jean Paul Latgé, Gerald R. Fink, Kevin R. Foster, Kevin J. Verstrepen^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

371 Scopus citations

Abstract

The budding yeast, Saccharomyces cerevisiae, has emerged as an archetype of eukaryotic cell biology. Here we show that S. cerevisiae is also a model for the evolution of cooperative behavior by revisiting flocculation, a self-adherence phenotype lacking in most laboratory strains. Expression of the gene FLO1 in the laboratory strain S288C restores flocculation, an altered physiological state, reminiscent of bacterial biofilms. Flocculation protects the FLO1 expressing cells from multiple stresses, including antimicrobials and ethanol. Furthermore, FLO1⁺ cells avoid exploitation by nonexpressing flo1 cells by self/non-self recognition: FLO1⁺ cells preferentially stick to one another, regardless of genetic relatedness across the rest of the genome. Flocculation, therefore, is driven by one of a few known "green beard genes," which direct cooperation toward other carriers of the same gene. Moreover, FLO1 is highly variable among strains both in expression and in sequence, suggesting that flocculation in S. cerevisiae is a dynamic, rapidly evolving social trait.

Original language	English (US)
Pages (from-to)	726-737
Number of pages	12
Journal	Cell
Volume	135
Issue number	4
DOIs	https://doi.org/10.1016/j.cell.2008.09.037
State	Published - Nov 14 2008
Externally published	Yes

Funding

We apologize for the omission of relevant references due to space restrictions. We thank three reviewers and B. Stern, B. Aertsen, S. Alonzo, M. Legendre, A. Schier, A. Regev, R. Losick, and A. Murray for their suggestions. K.J.V. and K.R.F. are supported by NIH NIGMS grant 5P50GM068763, and K.J.V. also by the Human Frontier Science Program Award HFSP RGY79/2007, an Odysseus fellowship of the Flemish Fund for Scientific Research (FWO), and VIB. J.-P.L. is supported by contract LSHB-CT-2004-511952 FUNGWALL. G.R.F. is supported by NIH grant GM40266. N.P. is a fellow of the Belgian American Educational Foundation (B.A.E.F.). M.D.V. is a fellow of the Ford Foundation and the B.A.E.F. S.S. and C.Y. thank the Harvard College Research Program, PRISE, and the Bauer Internship Program.

Keywords

CELLBIO
EVO_ECOL
MICROBIO

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2008.09.037

Cite this

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title = "FLO1 Is a Variable Green Beard Gene that Drives Biofilm-like Cooperation in Budding Yeast",

abstract = "The budding yeast, Saccharomyces cerevisiae, has emerged as an archetype of eukaryotic cell biology. Here we show that S. cerevisiae is also a model for the evolution of cooperative behavior by revisiting flocculation, a self-adherence phenotype lacking in most laboratory strains. Expression of the gene FLO1 in the laboratory strain S288C restores flocculation, an altered physiological state, reminiscent of bacterial biofilms. Flocculation protects the FLO1 expressing cells from multiple stresses, including antimicrobials and ethanol. Furthermore, FLO1+ cells avoid exploitation by nonexpressing flo1 cells by self/non-self recognition: FLO1+ cells preferentially stick to one another, regardless of genetic relatedness across the rest of the genome. Flocculation, therefore, is driven by one of a few known {"}green beard genes,{"} which direct cooperation toward other carriers of the same gene. Moreover, FLO1 is highly variable among strains both in expression and in sequence, suggesting that flocculation in S. cerevisiae is a dynamic, rapidly evolving social trait.",

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author = "Scott Smukalla and Marina Caldara and Nathalie Pochet and Anne Beauvais and Stephanie Guadagnini and Chen Yan and Vinces, {Marcelo D.} and An Jansen and Prevost, {Marie Christine} and Latg{\'e}, {Jean Paul} and Fink, {Gerald R.} and Foster, {Kevin R.} and Verstrepen, {Kevin J.}",

note = "Funding Information: We apologize for the omission of relevant references due to space restrictions. We thank three reviewers and B. Stern, B. Aertsen, S. Alonzo, M. Legendre, A. Schier, A. Regev, R. Losick, and A. Murray for their suggestions. K.J.V. and K.R.F. are supported by NIH NIGMS grant 5P50GM068763, and K.J.V. also by the Human Frontier Science Program Award HFSP RGY79/2007, an Odysseus fellowship of the Flemish Fund for Scientific Research (FWO), and VIB. J.-P.L. is supported by contract LSHB-CT-2004-511952 FUNGWALL. G.R.F. is supported by NIH grant GM40266. N.P. is a fellow of the Belgian American Educational Foundation (B.A.E.F.). M.D.V. is a fellow of the Ford Foundation and the B.A.E.F. S.S. and C.Y. thank the Harvard College Research Program, PRISE, and the Bauer Internship Program. ",

year = "2008",

month = nov,

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doi = "10.1016/j.cell.2008.09.037",

language = "English (US)",

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AU - Caldara, Marina

AU - Pochet, Nathalie

AU - Beauvais, Anne

AU - Guadagnini, Stephanie

AU - Yan, Chen

AU - Vinces, Marcelo D.

AU - Jansen, An

AU - Prevost, Marie Christine

AU - Latgé, Jean Paul

AU - Fink, Gerald R.

AU - Foster, Kevin R.

AU - Verstrepen, Kevin J.

N1 - Funding Information: We apologize for the omission of relevant references due to space restrictions. We thank three reviewers and B. Stern, B. Aertsen, S. Alonzo, M. Legendre, A. Schier, A. Regev, R. Losick, and A. Murray for their suggestions. K.J.V. and K.R.F. are supported by NIH NIGMS grant 5P50GM068763, and K.J.V. also by the Human Frontier Science Program Award HFSP RGY79/2007, an Odysseus fellowship of the Flemish Fund for Scientific Research (FWO), and VIB. J.-P.L. is supported by contract LSHB-CT-2004-511952 FUNGWALL. G.R.F. is supported by NIH grant GM40266. N.P. is a fellow of the Belgian American Educational Foundation (B.A.E.F.). M.D.V. is a fellow of the Ford Foundation and the B.A.E.F. S.S. and C.Y. thank the Harvard College Research Program, PRISE, and the Bauer Internship Program.

PY - 2008/11/14

Y1 - 2008/11/14

N2 - The budding yeast, Saccharomyces cerevisiae, has emerged as an archetype of eukaryotic cell biology. Here we show that S. cerevisiae is also a model for the evolution of cooperative behavior by revisiting flocculation, a self-adherence phenotype lacking in most laboratory strains. Expression of the gene FLO1 in the laboratory strain S288C restores flocculation, an altered physiological state, reminiscent of bacterial biofilms. Flocculation protects the FLO1 expressing cells from multiple stresses, including antimicrobials and ethanol. Furthermore, FLO1+ cells avoid exploitation by nonexpressing flo1 cells by self/non-self recognition: FLO1+ cells preferentially stick to one another, regardless of genetic relatedness across the rest of the genome. Flocculation, therefore, is driven by one of a few known "green beard genes," which direct cooperation toward other carriers of the same gene. Moreover, FLO1 is highly variable among strains both in expression and in sequence, suggesting that flocculation in S. cerevisiae is a dynamic, rapidly evolving social trait.

AB - The budding yeast, Saccharomyces cerevisiae, has emerged as an archetype of eukaryotic cell biology. Here we show that S. cerevisiae is also a model for the evolution of cooperative behavior by revisiting flocculation, a self-adherence phenotype lacking in most laboratory strains. Expression of the gene FLO1 in the laboratory strain S288C restores flocculation, an altered physiological state, reminiscent of bacterial biofilms. Flocculation protects the FLO1 expressing cells from multiple stresses, including antimicrobials and ethanol. Furthermore, FLO1+ cells avoid exploitation by nonexpressing flo1 cells by self/non-self recognition: FLO1+ cells preferentially stick to one another, regardless of genetic relatedness across the rest of the genome. Flocculation, therefore, is driven by one of a few known "green beard genes," which direct cooperation toward other carriers of the same gene. Moreover, FLO1 is highly variable among strains both in expression and in sequence, suggesting that flocculation in S. cerevisiae is a dynamic, rapidly evolving social trait.

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KW - EVO_ECOL

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JO - Cell

JF - Cell

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ER -

FLO1 Is a Variable Green Beard Gene that Drives Biofilm-like Cooperation in Budding Yeast

Abstract

Funding

Keywords

ASJC Scopus subject areas

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