1887

Abstract

Transition from growth to the stationary phase in yeast is still poorly understood. Previously, we identified a group of yeast genes that are universally upregulated upon starvation for different macronutrients. Here, we demonstrate that the Gis1 transcription factor and the Rim15 kinase are responsible for the upregulation of many of these genes. In chemostat cultures, or mutant cells are outcompeted by their wild-type parents under conditions resembling the later stages of diauxie (glucose-limiting) and post-diauxie (ethanol as a carbon source). Whilst Gis1p and Rim15p have distinct functions in gene repression, the growth defects of or deletants can be accounted for by the overlapping functions of their protein products in promoting the expression of genes involved in glutamate biosynthesis, the glyoxylate cycle, the pentose phosphate pathway and the stress response. Further, we show that the sets of - and -dependent genes and the degree of their regulation change in response to the identity of the carbon source, suggesting the likely dynamics of gene regulation exerted by Rim15p and Gis1p during different phases of the transition into stationary phase. In particular, Rim15p is required for the expression of genes involved in gluconeogenesis/glycolysis and glycerol biosynthesis only when ethanol is used as the carbon source. In agreement with this, Rim15p is shown to act in parallel with Hog1p to defend cells against osmotic stress.

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2009-05-01
2020-07-12
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References

  1. Amberg D., Burke D. J., Strathern J. N.. 2005; Methods in Yeast Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  2. Avendano A., Riego L., DeLuna A., Aranda C., Romero G., Ishida C., Vazquez-Acevedo M., Rodarte B., Recillas-Targa F.. other authors 2005; Swi/SNF-GCN5-dependent chromatin remodelling determines induced expression of GDH3 , one of the paralogous genes responsible for ammonium assimilation and glutamate biosynthesis in Saccharomyces cerevisiae . Mol Microbiol57:291–305
    [Google Scholar]
  3. Baganz F., Hayes A., Farquhar R., Butler P. R., Gardner D. C. J., Oliver S. G.. 1998; Quantitative analysis of yeast gene function using competition experiments in continuous culture. Yeast14:1417–1427
    [Google Scholar]
  4. Balciunas D., Ronne H.. 1999; Yeast genes GIS1–4 : multicopy suppressors of the Gal phenotype of snf1 mig1 srb8 cells. Mol Gen Genet262:589–599
    [Google Scholar]
  5. Boorstein W. R., Craig E. A.. 1990; Regulation of a yeast HSP70 gene by a cAMP responsive transcriptional control element. EMBO J9:2543–2553
    [Google Scholar]
  6. Brown A. J., Planta R. J., Restuhadi F., Bailey D. A., Butler P. R., Cadahia J. L., Cerdan M. E., De Jonge M., Gardner D. C. J.. other authors 2001; Transcript analysis of 1003 novel yeast genes using high-throughput northern hybridizations. EMBO J20:3177–3186
    [Google Scholar]
  7. Cameroni E., Hulo N., Roosen J., Winderickx J., De Virgilio C.. 2004; The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle3:462–468
    [Google Scholar]
  8. Capaldi A. P., Kaplan T., Liu Y., Habib N., Regev A., Friedman N., O'Shea E. K.. 2008; Structure and function of a transcriptional network activated by the MAPK Hog1. Nat Genet40:1300–1306
    [Google Scholar]
  9. Castrillo J. I., Zeef L. A., Hoyle D. C., Zhang N., Hayes A., Gardner D. C. J., Cornell M. J., Petty J., Hakes L.. other authors 2007; Growth control of the eukaryote cell: a systems biology study in yeast. J Biol6:4
    [Google Scholar]
  10. Costa V., Moradas-Ferreira P.. 2001; Oxidative stress and signal transduction in Saccharomyces cerevisiae : insights into ageing, apoptosis and diseases. Mol Aspects Med22:217–246
    [Google Scholar]
  11. DeRisi J. L., Iyer V. R., Brown P. O.. 1997; Exploring the metabolic and genetic control of gene expression on a genomic scale. Science278:680–686
    [Google Scholar]
  12. Herman P. K.. 2002; Stationary phase in yeast. Curr Opin Microbiol5:602–607
    [Google Scholar]
  13. Inoki K., Ouyang H., Li Y., Guan K. L.. 2005; Signaling by target of rapamycin proteins in cell growth control. Microbiol Mol Biol Rev69:79–100
    [Google Scholar]
  14. Jang Y. K., Wang L., Sancar G. B.. 1999; RPH1 and GIS1 are damage-responsive repressors of PHR1 . Mol Cell Biol19:7630–7638
    [Google Scholar]
  15. Johnston M., Carlson M.. 1992; Regulation of carbon and phosphate utilization. . In The Molecular and Cellular Biology of the Yeast Saccharomyces cerevisiae Gene Expression pp193–281 Edited by Jones E. W., Pringle J. R., Broach J. R. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  16. Maeda T., Wurgler-Murphy S. M., Saito H.. 1994; A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature369:242–245
    [Google Scholar]
  17. Oshiro J., Han G. S., Iwanyshyn W. M., Conover K., Carman G. M.. 2003; Regulation of the yeast DPP1 -encoded diacylglycerol pyrophosphate phosphatase by transcription factor Gis1p. J Biol Chem278:31495–31503
    [Google Scholar]
  18. Pahlman A. K., Granath K., Ansell R., Hohmann S., Adler L.. 2001; The yeast glycerol 3-phosphatases Gpp1p and Gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress. J Biol Chem276:3555–3563
    [Google Scholar]
  19. Pedruzzi I., Burckert N., Egger P., De Virgilio C.. 2000; Saccharomyces cerevisiae Ras/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1. EMBO J19:2569–2579
    [Google Scholar]
  20. Pedruzzi I., Dubouloz F., Cameroni E., Wanke V., Roosen J., Winderickx J., De Virgilio C.. 2003; TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell12:1607–1613
    [Google Scholar]
  21. Roosen J., Engelen K., Marchal K., Mathys J., Griffioen G., Cameroni E., Thevelein J. M., De Virgilio C., De Moor B., Winderickx J.. 2005; PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol Microbiol55:862–880
    [Google Scholar]
  22. Schuller H. J.. 2003; Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae . Curr Genet43:139–160
    [Google Scholar]
  23. Sopko R., Huang D., Preston N., Chua G., Papp B., Kafadar K., Snyder M., Oliver S. G., Cyert M.. other authors 2006; Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell21:319–330
    [Google Scholar]
  24. Swinnen E., Rosseels J., Winderickx J.. 2005; The minimum domain of Pho81 is not sufficient to control the Pho85–Rim15 effector branch involved in phosphate starvation-induced stress responses. Curr Genet48:18–33
    [Google Scholar]
  25. Swinnen E., Wanke V., Roosen J., Smets B., Dubouloz F., Pedruzzi I., Cameroni E., De Virgilio C., Winderickx J.. 2006; Rim15 and the crossroads of nutrient signalling pathways in Saccharomyces cerevisiae . Cell Div1: 3
    [Google Scholar]
  26. Thevelein J. M., de Winde J. H.. 1999; Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae . Mol Microbiol33:904–918
    [Google Scholar]
  27. Urban J., Soulard A., Huber A., Lippman S., Mukhopadhyay D., Deloche O., Wanke V., Anrather D., Ammerer G.. other authors 2007; Sch9 is a major target of TORC1 in Saccharomyces cerevisiae . Mol Cell26:663–674
    [Google Scholar]
  28. Wanke V., Pedruzzi I., Cameroni E., Dubouloz F., De Virgilio C.. 2005; Regulation of G0 entry by the Pho80-Pho85 cyclin-CDK complex. EMBO J24:4271–4278
    [Google Scholar]
  29. Wanke V., Cameroni E., Uotila A., Piccolis M., Urban J., Loewith R., De Virgilio C.. 2008; Caffeine extends yeast lifespan by targeting TORC1. Mol Microbiol69:277–285
    [Google Scholar]
  30. Wilson W. A., Roach P. J.. 2002; Nutrient-regulated protein kinases in budding yeast. Cell111:155–158
    [Google Scholar]
  31. Winzeler E. A., Shoemaker D. D., Astromoff A., Liang H., Anderson K., Andre B., Bangham R., Benito R., Boeke J. D.. other authors 1999; Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science285:901–906
    [Google Scholar]
  32. Wu J., Zhang N., Hayes A., Panoutsopoulou K., Oliver S. G.. 2004; Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth and starvation. Proc Natl Acad Sci U S A101:3148–3153
    [Google Scholar]
  33. Wullschleger S., Loewith R., Hall M. N.. 2006; TOR signaling in growth and metabolism. Cell124:471–484
    [Google Scholar]
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