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Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation

Authors

  • Markus J. Tamás,

    1. Laboratorium voor Moleculaire Celbiologie, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Leuven-Heverlee, Flanders, Belgium.,
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  • Kattie Luyten,

    1. Laboratorium voor Moleculaire Celbiologie, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Leuven-Heverlee, Flanders, Belgium.,
    2. Departamento de Microbiología, Escuela Técnica de Ingenieros Agrónomos y de Montes, Universidad de Córdoba, Apartado 3048, E-14080 Córdoba, Spain.,
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    • F. Chris W. Sutherland,

      1. Department of Microbiology and Biochemistry, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa.,
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    • Agustin Hernandez,

      1. Laboratorium voor Moleculaire Celbiologie, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Leuven-Heverlee, Flanders, Belgium.,
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    • Jacobus Albertyn,

      1. Department of Microbiology and Biochemistry, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa.,
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    • Hadi Valadi,

      1. Department of Cell and Molecular Biology/Microbiology, Göteborg University, Box 462, SE-405 30 Göteborg, Sweden.
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    • Hong Li,

      1. Department of Microbiology and Biochemistry, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa.,
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    • Bernard A. Prior,

      1. Department of Microbiology and Biochemistry, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa.,
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      • Stephanus G. Kilian,

        1. Department of Microbiology and Biochemistry, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa.,
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      • José Ramos,

        1. Departamento de Microbiología, Escuela Técnica de Ingenieros Agrónomos y de Montes, Universidad de Córdoba, Apartado 3048, E-14080 Córdoba, Spain.,
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      • Lena Gustafsson,

        1. Department of Cell and Molecular Biology/Microbiology, Göteborg University, Box 462, SE-405 30 Göteborg, Sweden.
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      • Johan M. Thevelein,

        1. Laboratorium voor Moleculaire Celbiologie, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Leuven-Heverlee, Flanders, Belgium.,
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      • Stefan Hohmann

        1. Laboratorium voor Moleculaire Celbiologie, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Leuven-Heverlee, Flanders, Belgium.,
        2. Department of Microbiology and Biochemistry, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa.,
        3. Department of Cell and Molecular Biology/Microbiology, Göteborg University, Box 462, SE-405 30 Göteborg, Sweden.
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      Stefan Hohmann. E-mail hohmann@gmm.gu.se; Tel. (+46) 31 773 2595; Fax (+46) 31 773 2599.

      Abstract

      The accumulation of compatible solutes, such as glycerol, in the yeast Saccharomyces cerevisiae, is a ubiquitous mechanism in cellular osmoregulation. Here, we demonstrate that yeast cells control glycerol accumulation in part via a regulated, Fps1p-mediated export of glycerol. Fps1p is a member of the MIP family of channel proteins most closely related to the bacterial glycerol facilitators. The protein is localized in the plasma membrane. The physiological role of Fps1p appears to be glycerol export rather than uptake. Fps1Δ mutants are sensitive to hypo-osmotic shock, demonstrating that osmolyte export is required for recovery from a sudden drop in external osmolarity. In wild-type cells, the glycerol transport rate is decreased by hyperosmotic shock and increased by hypo-osmotic shock on a subminute time scale. This regulation seems to be independent of the known yeast osmosensing HOG and PKC signalling pathways. Mutants lacking the unique hydrophilic N-terminal domain of Fps1p, or certain parts thereof, fail to reduce the glycerol transport rate after a hyperosmotic shock. Yeast cells carrying these constructs constitutively release glycerol and show a dominant hyperosmosensitivity, but compensate for glycerol loss after prolonged incubation by glycerol overproduction. Fps1p may be an example of a more widespread class of regulators of osmoadaptation, which control the cellular content and release of compatible solutes.

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