1887

Abstract

Living organisms display large differences in stress resistance throughout their life cycles. To study the coordinated regulation of development and stress responses in exponentially growing yeast, mutants that displayed elevated heat-shock resistance at this stage were screened for. Here, two new mutant alleles of in , and , are described. During exponential growth in glucose at 25 °C, these mutants are resistant to heat, oxidative, osmotic and ionic shock, accumulate stress-protein transcripts, show slow growth rates, thick cell walls and glycogen hyperaccumulation and lack cAMP signalling in response to glucose. Genetic and cellular analyses revealed that the stationary-phase phenotypes of and mutants are not due to entrance to a G state during exponential growth, but are the result of a prolonged G phase. It was found that, in the W303 background, is dispensable for growth in glucose media. However, is essential for growth in galactose, in non-fermentable carbon sources and under continuous incubation at 38 °C. In conclusion, the function of the catalytic, C-terminal domain of Cdc25p is not only important for fermentative growth, but also for growth in non-fermentable carbon sources and to trigger galactose derepression.

Keyword(s): PKA, protein kinase A
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2004-09-01
2020-04-09
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References

  1. Albertyn J., Hohmann S., Thevelein J. M., Prior B. A. 1994; GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol14:4135–4144
    [Google Scholar]
  2. Boeke J. D., LaCroute F., Fink G. R. 1984; A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet197:345–346[CrossRef]
    [Google Scholar]
  3. Boy-Marcotte E., Ikonomi P., Jacquet M. 1996; SDC25, a dispensable Ras guanine nucleotide exchange factor of Saccharomyces cerevisiae differs from CDC25 by its regulation. Mol Biol Cell7:529–539[CrossRef]
    [Google Scholar]
  4. Breeden L., Nasmyth K. 1985; Regulation of the yeast HO gene. Cold Spring Harb Symp Quant Biol50:643–650[CrossRef]
    [Google Scholar]
  5. Broek D., Toda T., Michaeli T., Levin L., Birchmeier C., Zoller M., Powers S., Wigler M. 1987; The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell48:789–799[CrossRef]
    [Google Scholar]
  6. Camus C., Geymonat M., Garreau H., Baudet-Nessler S., Jacquet M. 1997; Dimerization of Cdc25p, the guanine-nucleotide exchange factor for Ras from Saccharomyces cerevisiae, and its interaction with Sdc25p. Eur J Biochem247:703–708[CrossRef]
    [Google Scholar]
  7. Chen R. A., Michaeli T., Van Aelst L., Ballester R. 2000; A role for the noncatalytic N terminus in the function of Cdc25, a Saccharomyces cerevisiae Ras-guanine nucleotide exchange factor. Genetics154:1473–1484
    [Google Scholar]
  8. Collart M. A., Oliviero S. 1993; Preparation of yeast RNA. In Current Protocols in Molecular Biology 2 pp.13–12 Edited by Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K.. New York: Wiley;
    [Google Scholar]
  9. Corkidi G., Diaz-Uribe R., Folch-Mallol J. L., Nieto-Sotelo J. 1998; COVASIAM: an image analysis method that allows detection of confluent microbial colonies and colonies of various sizes for automated counting. Appl Environ Microbiol64:1400–1404
    [Google Scholar]
  10. Damak F., Boy-Marcotte E., Le-Roscouet D., Guilbaud R., Jacquet M. 1991; SDC25, a CDC25-like gene which contains a RAS-activating domain and is a dispensable gene of Saccharomyces cerevisiae. Mol Cell Biol11:202–212
    [Google Scholar]
  11. Draper N. R., Smith H.. (editors) 1981; Applied Regression Analysis, 2nd edn. New York: Wiley-Interscience;
    [Google Scholar]
  12. Drebot M. A., Johnston G. C., Singer R. A. 1987; A yeast mutant conditionally defective only for reentry into the mitotic cell cycle from stationary phase. Proc Natl Acad Sci U S A84:7948–7952[CrossRef]
    [Google Scholar]
  13. Drebot M. A., Barnes C. A., Singer R. A., Johnston G. C. 1990; Genetic assessment of stationary phase for cells of the yeast Saccharomyces cerevisiae. J Bacteriol172:3584–3589
    [Google Scholar]
  14. Fedor-Chaiken M., Deschenes R. J., Broach J. R. 1990; SVR2, a gene required for RAS activation of adenylate cyclase in yeast. Cell61:329–340[CrossRef]
    [Google Scholar]
  15. Gasch A. P., Spellman P. T., Kao C. M., Carmel-Harel O., Eisen M. B., Storz G., Botstein D., Brown P. O. 2000; Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell11:4241–4257[CrossRef]
    [Google Scholar]
  16. Gietz R. D., Woods R. A. 2002; Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol350:87–96
    [Google Scholar]
  17. Güldener U., Heck S., Fiedler T., Beinhauer J., Hegemann J. H. 1996; A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res24:2519–2524[CrossRef]
    [Google Scholar]
  18. Guthrie C., Fink G. R.. (editors) 1991; Guide to Yeast Genetics and Molecular Biology New York: Academic Press;
    [Google Scholar]
  19. Hazell B. W., Nevalainen H., Attfield P. V. 1995; Evidence that the Saccharomyces cerevisiae CIF1 (GGS1/TPS1) gene modulates heat shock response positively. FEBS Lett377:457–460[CrossRef]
    [Google Scholar]
  20. Iida H. 1988; Multistress resistance of Saccharomyces cerevisiae is generated by insertion of retrotransposon Ty into the 5′ coding region of the adenylate cyclase gene. Mol Cell Biol8:5555–5560
    [Google Scholar]
  21. Iida H., Yahara I. 1984; A heat shock-resistant mutant of Saccharomyces cerevisiae shows constitutive synthesis of two heat shock proteins and altered growth. J Cell Biol99:1441–1450[CrossRef]
    [Google Scholar]
  22. Lai C.-C., Boguski M., Broek D., Powers S. 1993; Influence of guanine nucleotides on complex formation between Ras and CDC25 proteins. Mol Cell Biol13:1345–1352
    [Google Scholar]
  23. Lawrence C. W. 1991; Classical mutagenesis techniques. In Guide to Yeast Genetics and Molecular Biology pp.273–281 Edited by Guthrie C., Fink G. R.. New York: Academic Press;
    [Google Scholar]
  24. Lindquist S., Kim G. 1996; Heat-shock protein 104 expression is sufficient for thermotolerance in yeast. Proc Natl Acad Sci U S A93:5301–5306[CrossRef]
    [Google Scholar]
  25. Ma P., Wera S., Van Dijck P., Thevelein J. M. 1999; The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell10:91–104[CrossRef]
    [Google Scholar]
  26. Martegani E., Vanoni M., Baroni M. 1984; Macromolecular synthesis in the cell cycle mutant cdc25 of budding yeast. Eur J Biochem144:205–210[CrossRef]
    [Google Scholar]
  27. Munder T., Mink M., Küntzel H. 1988; Domains of the Sacchromyces cerevisiae CDC25 gene controlling mitosis and meiosis. Mol Gen Genet214:271–277[CrossRef]
    [Google Scholar]
  28. Nicolet C. M., Craig E. A. 1991; Inducing and assaying heat-shock response in Saccharomyces cerevisiae. In Guide to Yeast Genetics and Molecular Biology pp.710–717 Edited by Guthrie C., Fink G. R.. New York: Academic Press;
    [Google Scholar]
  29. Palomares L. A., Ramírez O. T. 1996; The effect of dissolved oxygen tension and the utility of oxygen uptake rate in insect cell culture. Cytotechnology22:225–237[CrossRef]
    [Google Scholar]
  30. Petitjean A., Hilger F., Tatchell K. 1990; Comparison of thermosensitive alleles of the CDC25 gene involved in the cAMP metabolism ofSaccharomyces cerevisiae. Genetics124:797–806
    [Google Scholar]
  31. Plesset J., Ludwig J. R., Cox B. S., McLaughlin C. S. 1987; Effect of cell cycle position on thermotolerance in Saccharomyces cerevisiae. J Bacteriol169:779–784
    [Google Scholar]
  32. Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. 1987; A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing vector. Gene60:237–243[CrossRef]
    [Google Scholar]
  33. Rothstein R. 1991; Targeting, disruption, replacement and allele rescue: integrative DNA transformation in yeast. In Guide to Yeast Genetics and Molecular Biology pp.710–717 Edited by Guthrie C., Fink G. R.. New York: Academic Press;
    [Google Scholar]
  34. Rudoni S., Mauri I., Ceriani M., Coccetti P., Martegani E. 2000; The overexpression of the CDC25 gene ofSaccharomyces cerevisiae causes a derepression of GAL system and an increase of GAL4 transcription. Int J Biochem Cell Biol32:215–224[CrossRef]
    [Google Scholar]
  35. Sambrook J., Fritsch E. F., Maniatis T.. (editors) 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. Sikorski R. S., Hieter P. 1989; A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics122:19–27
    [Google Scholar]
  37. Tatchell K. 1986; RAS genes and growth control in Saccharomyces cerevisiae. J Bacteriol166:364–367
    [Google Scholar]
  38. Tatchell K. 1993; RAS genes in the budding yeast Saccharomyces cerevisiae. In Signal Transduction: Prokaryotic and Simple Eukaryotic Systems pp.147–188 Edited by Kurjan J., Taylor B. L.. San Diego, CA: Academic Press;
    [Google Scholar]
  39. Thevelein J. M. 1992; The RAS-adenylate cyclase pathway and cell cycle control in Saccharomyces cerevisiae. Antonie van Leeuwenhoek62:109–130[CrossRef]
    [Google Scholar]
  40. 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[CrossRef]
    [Google Scholar]
  41. Thevelein J. M., Cauwenberg L., Colombo S.. 13 other authors 2000; Nutrient-induced signal transduction through the protein kinase A pathway and its role in the control of metabolism, stress resistance, and growth in yeast. Enzyme Microb Technol26:819–825[CrossRef]
    [Google Scholar]
  42. Toda T., Uno I., Ishikawa T.. 7 other authors 1985; In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell40:27–36[CrossRef]
    [Google Scholar]
  43. Toda T., Cameron S., Sass P., Zoller M., Scott J. D., McMullen B., Hurwitz M., Krebs E. G., Wigler M. 1987a; Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol Cell Biol7:1371–1377
    [Google Scholar]
  44. Toda T., Cameron S., Sass P., Zoller M., Wigler M. 1987b; Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell50:277–287[CrossRef]
    [Google Scholar]
  45. Tortora G. J., Funke B. R., Case C. L.. (editors) 1986; Microbiology, 2nd edn. Menlo Park, CA: Benjamin/Cummings;
    [Google Scholar]
  46. Van Aelst L., Boy-Marcotte E., Camonis J. H., Thevelein J. M., Jacquet M. 1990; The C-terminal part of the CDC25 gene product plays a key role in signal transduction in the glucose-induced modulation of cAMP level in Saccharomyces cerevisiae. Eur J Biochem193:675–680[CrossRef]
    [Google Scholar]
  47. Van Aelst L., Jans A. W. H., Thevelein J. M. 1991; Involvement of the CDC25 gene product in the signal transmission pathway of the glucose-induced Ras-mediated cAMP signal in the yeast Saccharomyces cerevisiae. J Gen Microbiol137:341–349[CrossRef]
    [Google Scholar]
  48. Van Dijck P., Colavizza D., Smet P., Thevelein J. M. 1995; Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells. Appl Environ Microbiol61:109–115
    [Google Scholar]
  49. Wang X., Hoekstra M. F., DeMaggio A. J., Dhillon N., Vancura A., Kuret J., Johnston G. C., Singer R. A. 1996; Prenylated isoforms of yeast casein kinase I, including the novel Yck3p, suppress the gcs1 blockage of cell proliferation from stationary phase. Mol Cell Biol16:5375–5385
    [Google Scholar]
  50. Werner-Washburne M., Braun E., Johnston G. C., Singer R. A. 1993; Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev57:383–401
    [Google Scholar]
  51. Wieser R., Adam G., Wagner A., Schüller C., Marchler G., Ruis H., Krawiec Z., Bilinski T. 1991; Heat shock factor-independent heat control of transcription of the CTT1 gene encoding the cytosolic catalase T ofSaccharomyces cerevisiae. J Biol Chem266:12406–12411
    [Google Scholar]
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