1887

Abstract

Strains of that exhibit varied capacities for accumulation of trehalose were tested for intrinsic thermotolerance. Yeast that accumulated trehalose rapidly in early respiratory phase showed equally rapid attainment of thermotolerance, whereas a strain unable to accumulate trehalose at this stage of culture showed markedly delayed appearance of thermotolerance. These results were obtained using closely related but non-isogenic diploids and so it is possible that variable factors other than trehalose were responsible for the observed thermotolerance effects. Therefore, a pair of isogenic diploid strains was generated to facilitate further testing of whether trehalose functions in intrinsic stress tolerance. Both isogenic strains inherited a partially reverted phenotype, designated CPR, from the trehalose-deficient progenitor that had been used in construction of the non-isogenic strains. The CPR phenotype permitted growth on glucose but not accumulation of trehalose, indicating that not all -related deficiencies were suppressed in the CPR strains. However, one of the isogenic CPR pair was and failed to accumulate trehalose, whilst the other was and was able to accumulate this sugar. The trehalose-proficient strain showed intrinsic stress tolerance whereas the trehalose-deficient strain was sensitive to heat stress during early respiratory growth. These results suggest that one or more functions of , not operating in the (CPR) strains, are important for intrinsic thermotolerance of yeast in early respiratory phase. When considering these results with those of others whose work has indicated a role for trehalose in protection of proteins and membranes, it is reasonable to hypothesize that the trehalose deficiency associated with (CPR) strains could be a key factor in their intrinsic thermosensitivity. However, if this is the case the importance of trehalose, relative to other stress tolerance factors, appears to vary with growth phase and culture status.

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1994-10-01
2021-10-28
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References

  1. Attfield P.V. Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Lett 1987; 225:259–263
    [Google Scholar]
  2. Attfield P.V., Raman A., Northcott C.J. Construction of Saccharomyces cerevisiae strains that accumulate relatively low concentrations of trehalose, and their application in testing the contribution of the disaccharide to stress tolerance. FEMS Microbiol Lett 1992; 94:271–276
    [Google Scholar]
  3. Bataille N., Regnacq M., Boucherie H. Induction of a heat-shock-type response in Saccharomyces cerevisiae following glucose limitation. Yeast 1991; 7:367–378
    [Google Scholar]
  4. Bell W., Klaassen P., Ohnacker M., Boiler T., Herweijer M., Schoppink P., Van Der Zee P., Wiemken A. Characterisation of the 56 kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur J Biochem 1992; 209:951–959
    [Google Scholar]
  5. Boucherie H. Protein synthesis during transition and stationary phases under glucose limitation in Saccharomyces cerevisiae. J Bacteriol 1985; 161:385–392
    [Google Scholar]
  6. Brown A.D., Mackenzie K.F., Singh K.K. Selected aspects of microbial osmoregulation. FEMS Microbiol Rev 1986; 39:31–36
    [Google Scholar]
  7. Carpenter J.F., Martin B., Loomis S.H., Crowe J.H. Long-term preservation of dried phosphofructokinase by sugars and sugar/zinc mixtures. Cryobiology 1988; 25:372–376
    [Google Scholar]
  8. Cheng L., Kirk N., Piper P. A small influence of HSP90 levels on the trehalose and heat shock element inductions of the yeast heat shock response. Biochem Biophys Res Commun 1993; 195:201–207
    [Google Scholar]
  9. Collinson L.P., Dawes I.W. Inducibility of the response of yeast cells to peroxide stress. J Gen Microbiol 1992; 138:329–335
    [Google Scholar]
  10. Crowe J.H., Crowe L.M., Carpenter J.F., Aurell-Wistrom C. Stabilisation of dry phospholipid bilayers and proteins by sugars. Biocbem J 1987; 242:1–10
    [Google Scholar]
  11. De Virgilio C., Hottiger T., Dominguez J., Boiler T., Wiemken A. The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. Eur J Biocbem 1994; 219:179–186
    [Google Scholar]
  12. De Virgilio C., Simmen U., Hottiger T., Boiler T., Wiemken A. Heat shock induces enzymes of trehalose metabolism, trehalose accumulation, and thermotolerance in Schi^osaccharomyces pombe, even in the presence of cycloheximide. FEBS Lett 1990; 273:107–110
    [Google Scholar]
  13. De Virgilio C., Piper P., Boiler T., Wiemken A. Acquisition of thermotolerance in Saccharomyces cerevisiae without heat shock protein hspl04 and in the absence of protein synthesis. FEBS Lett 1991; 288:86–90
    [Google Scholar]
  14. Gadd G.M., Chalmers K., Reed R.H. The role of trehalose in dehydration resistance of Saccharomyces cerevisiae. FEMS Microbiol Lett 1987; 48:249–254
    [Google Scholar]
  15. Gonzalez M.I., Stucka R., Blazquez M.A., Feldmann H., Gancedo C. Molecular cloning of CIF1, a yeast gene necessary for growth on glucose. Yeast 1992; 8:183–192
    [Google Scholar]
  16. Hohmann S., Neves M.J., De Koning W., Alijo R., Ramos J., Thevelein J.M. The growth and signalling defects of the ggsl (Jdp1 /byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII. Curr Genet 1993; 23:281–289
    [Google Scholar]
  17. Hottiger T., Boiler T., Wiemken A. Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett 1987; 220:113–115
    [Google Scholar]
  18. Hottiger T., Boiler T., Wiemken A. Correlation of trehalose content and heat resistance in yeast mutants altered in the RAS/adenylate cyclase pathways: is trehalose a thermoprotectant. FEBS Lett 1989; 255:431–434
    [Google Scholar]
  19. Hottiger T., De Virgilio C., Bell W., Boiler T., Wiemken A. The 70-kilodalton heat-shock proteins of the SSA subfamily negatively modulate heat-shock-induced accumulation of trehalose and promote recovery from heat stress in the yeast, Saccharomyces cerevisiae. Eur J Biochem 1992; 210:125–132
    [Google Scholar]
  20. Hottiger T., De Virgilio C., Hall M.N., Boiler T., Wiemken A. The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro. Eur J Biochem 1994; 219:187–193
    [Google Scholar]
  21. Lewis J.G., Northcott C.J., Learmonth R.P., Attfield P.V., Watson K. The need for consistent nomenclature and assessment of growth phases in diauxic cultures of Saccharomyces cerevisiae. J Gen Microbiol 1993; 139:835–839
    [Google Scholar]
  22. Lillie S.H., Pringle J.R. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 1980; 143:1384–1394
    [Google Scholar]
  23. Lindquist S., Craig E.A. The heat shock proteins. Annu Rev Genet 1988; 22:631–637
    [Google Scholar]
  24. Mackenzie K.F., Blomberg A., Brown A.D. Water stress plating hypersensitivity of yeasts. J Gen Microbiol 1986; 132:2053–2056
    [Google Scholar]
  25. Mackenzie K.F., Singh K.K., Brown A.D. Water stress plating hypersensitivity of yeasts: protective role of trehalose in Saccharomyces cerevisiae. J Gen Microbiol 1988; 134:1661–1666
    [Google Scholar]
  26. Meyer E.D., Sinclair N.A., Nagy B. Comparison of the survival and metabolic activity of psychrophilic and mesophilic yeasts subjected to freeze-thaw stress. Appl Microbiol 1975; 29:739–744
    [Google Scholar]
  27. Mishra P., Prasad R. Relationship between ethanol tolerance and fatty acyl composition of Saccharomyces cerevisiae. Appl Microbiol Biotechnol 1989; 30:294–298
    [Google Scholar]
  28. Navon G., Shulman R.G., Yamane T., Ecdeshall T.R., Lam K.B., Baronfsky J.J., Marmur J. Phosphorous-31 nuclear magnetic resonance studies of wild type and glycolytic pathway mutants of Saccharomyces cerevisiae. Biochemistry 1979; 18:4487–4499
    [Google Scholar]
  29. Operti M.S., Oliveira D.E., Freitas-Valle A.B., Oestreicher E.G., Mattoon J.R., Panek A.D. Relationships between trehalose metabolism and maltose utilisation in Saccharomyces cerevisiae. Curr Genet 1982; 5:69–76
    [Google Scholar]
  30. Panaretou B., Piper P.W. Plasma-membrane ATPase action affects several stress tolerances of Saccharomyces cerevisiae and Schis^psaccharomyces pombe as well as the extent and duration of the heat shock response. J Gen Microbiol 1990; 136:1763–1770
    [Google Scholar]
  31. Panek A.C., Francois J., Panek A.D. New insights into a mutant of Saccharomyces cerevisiae having impaired sugar uptake metabolism. Curr Genet 1988; 13:15–20
    [Google Scholar]
  32. Panek A.C., Mansure Vania J.J., Paschoalin M.F., Panek A.D. Regulation of trehalose metabolism in Saccharomyces cerevisiae mutants during temperature shifts. Biochimie 1990; 72:77–79
    [Google Scholar]
  33. Panek A.D. Trehalose metabolism and its role in Saccharomyces cerevisiae. J Biotechnol 1985; 3:121–130
    [Google Scholar]
  34. Panek A.D., Bernades E.J. Trehalose: its role in germination of Saccharomyces cerevisiae. Curr Genet 1983; 7:393–397
    [Google Scholar]
  35. Panek A.D., Ferreira R., Panek A.C. Comparative studies between the glucose-induced phosphorylation signal and the heat shock response in mutants of Saccharomyces cerevisiae. Biochimie 1989; 71:313–318
    [Google Scholar]
  36. Parry J.M., Davies P.J., Evans W.E. The effects of & cell age” upon the lethal effects of chemical and physical mutagens in the yeast Saccharomyces cerevisiae. Mol & Gen Genet 1976; 146:27–35
    [Google Scholar]
  37. Parsell D.A., Taulien J., Lindquist S. The role of heat-shock proteins in thermotolerance. Philosoph Trans Roy Soc Lond B 1993; 339:279–286
    [Google Scholar]
  38. Piper P.W. Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 1993; 11:339–356
    [Google Scholar]
  39. Reed R.H., Chudek J.A., Foster R., Gadd G.M. Osmotic significance of glycerol accumulation in exponentially growing yeasts. Appl Environ Microbiol 1987; 53:2119–2123
    [Google Scholar]
  40. Rosa M.F., Sa-Correia I. In vivo activation by ethanol of plasma membrane ATPase of Saccharomyces cerevisiae. Appl Environ Microbiol 1991; 57:830–835
    [Google Scholar]
  41. Rudolph A.S., Crowe J.H. Membrane stabilisation during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology 1985; 22:367–377
    [Google Scholar]
  42. Sanchez Y., Taulien J., Borkovich A., Lindquist S. Hsp 104 is required for tolerance to many forms of stress. EMBO J 1992; 11:2357–2364
    [Google Scholar]
  43. Schenberg-Frascino A., Moustacchi E. Lethal and mutagenic effects of elevated temperature on haploid yeast. Mol & Gen Genet 1972; 115:243–257
    [Google Scholar]
  44. Sherman F., Fink G.R., Hicks J.B. Methods in Yeast Genetics 1981 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  45. Stucka R., Blazquez M.A. The fdp1 and cio1 mutations are caused by different single nucleotide changes in the yeast CIF 1 gene. FEMS Microbiol Lett 1993; 107:251–254
    [Google Scholar]
  46. Thomas S.D., Hossack J.A., Rose A.H. Plasmamembrane lipid composition and ethanol tolerance in Saccharomyces cerevisiae. Arch Microbiol 1978; 117:239–245
    [Google Scholar]
  47. Van Aelst L., Hohmann S., Zimmermann F.K., Jans A.W.H., Thevelein J.M. A yeast homologue of the bovine lens fibre MIP gene family complements the growth defect of a Saccharomyces cerevisiae mutant on fermentable sugars but not its defect in glucose- induced RAS-mediated cAMP signalling. EMBO J 1991; 10:2095–2104
    [Google Scholar]
  48. Van Aelst L., Hohmann S., Bulaya B., De Koning W., Sierkstra L., Neves M.J., Luyten K., Alijo R., Ramos J., Coccetti P., Martegani E., De Magalhäes-Rocha N.M., Brandäo R.L., Van Dijck P., Vanhalewyn M., Durnez P., Jans A.W.H., Thevelein J.M. Molecular cloning of a gene involved in glucose sensing in the yeast Saccharomyces cerevisiae. Mol Microbiol 1993; 8:927–943
    [Google Scholar]
  49. Van De Poll K.W., Schamhart D.H.J. Characterisation of a regulatory mutant of fructose 1,6-bisphosphatase in Saccharomyces carlsbergensis. Mol & Gen Genet 1977; 154:61–66
    [Google Scholar]
  50. Wemer-Washburne M., Becker J., Kosic-Smithers J., Craig E.A. Yeast Hsp70 RNA levels vary in response to the physiological status of the cell. J Bacteriol 1989; 171:2680–2688
    [Google Scholar]
  51. Yun S.-K., Matheson N.K. Estimation of amylose content of starches after precipitation of amylopectin by conconavalin-A. Starch J Starke 1990; 42:302–305
    [Google Scholar]
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