Extremophiles

, Volume 10, Issue 2, pp 117–128

Genome-wide expression analysis of yeast response during exposure to 4°C

  • Yoshinori Murata
  • Takayuki Homma
  • Emiko Kitagawa
  • Yuko Momose
  • Masanori S. Sato
  • Mine Odani
  • Hisayo Shimizu
  • Mika Hasegawa-Mizusawa
  • Rena Matsumoto
  • Satomi Mizukami
  • Katsuhide Fujita
  • Meher Parveen
  • Yasuhiko Komatsu
  • Hitoshi Iwahashi
Original Paper

Abstract

Adaptation to temperature fluctuation is essential for the survival of all living organisms. Although extensive research has been done on heat and cold shock responses, there have been no reports on global responses to cold shock below 10°C or near-freezing. We examined the genome-wide expression in Saccharomyces cerevisiae, following exposure to 4°C. Hierarchical cluster analysis showed that the gene expression profile following 4°C exposure from 6 to 48 h was different from that at continuous 4°C culture. Under 4°C exposure, the genes involved in trehalose and glycogen synthesis were induced, suggesting that biosynthesis and accumulation of those reserve carbohydrates might be necessary for cold tolerance and energy preservation. The observed increased expression of phospholipids, mannoproteins, and cold shock proteins (e.g., TIP1) is consistent with membrane maintenance and increased permeability of the cell wall at 4°C. The induction of heat shock proteins and glutathione at 4°C may be required for revitalization of enzyme activity, and for detoxification of active oxygen species, respectively. The genes with these functions may provide the ability of cold tolerance and adaptation to yeast cells.

Keywords

Yeast DNA microarray Hierarchical cluster Gene expression profiling Cold shock protein Trehalose Glycogen Membrane maintenance 

References

  1. Abramova N, Sertil O, Mehta S, Lowry CV (2001). Reciprocal regulation of anaerobic and aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J Bacteriol 183:2881–2887CrossRefPubMedGoogle Scholar
  2. Aguilar PS, Lopez P, de Mendoza D (1999) Transcriptional control of the low-temperature-inducible des gene, encoding the delta5 desaturase of Bacillus subtilis. J Bacteriol 181:7028–7033PubMedGoogle Scholar
  3. Avery AM, Avery SV (2001) Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases. J Biol Chem 276:33730–33735CrossRefPubMedGoogle Scholar
  4. Bell W, Sun W, Hohmann S, Wera S, Reinders A, De Virgilio C, Wiemken A, Thevelein JM (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273:33311–33319CrossRefPubMedGoogle Scholar
  5. Carman GM, Zeimetz GM (1996) Regulation of phospholipid biosynthesis in the yeast Saccharomyces cerevisiae. J Biol Chem 271:13293–13296CrossRefPubMedGoogle Scholar
  6. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12:323–337PubMedGoogle Scholar
  7. Choi JH, Lou W, Vancura A (1998) A novel membrane-bound glutathione S-transferase functions in the stationary phase of the yeast Saccharomyces cerevisiae. J Biol Chem 273:29915–29922CrossRefPubMedGoogle Scholar
  8. Collinson EJ, Grant CM (2003) Role of yeast glutaredoxins as glutathione S-transferases. J Biol Chem 278:22492–22497 (Epub 2003 April 8)CrossRefPubMedGoogle Scholar
  9. Delneri D, Gardner DC, Oliver SG (1999) Analysis of the seven-member AAD gene set demonstrates that genetic redundancy in yeast may be more apparent than real. Genetics 153:1591–1600PubMedGoogle Scholar
  10. Fang L, Hou Y, Inouye M (1998) Role of the cold-box region in the 5′ untranslated region of the cspA mRNA in its transient expression at low temperature in Escherichia coli. J Bacteriol 180:90–95PubMedGoogle Scholar
  11. Francois J, Parrou JL (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25:125–145CrossRefPubMedGoogle Scholar
  12. Fujita K, Matsuyama A, Kobayashi Y, Iwahashi H (2004) Comprehensive gene expression analysis of the response to straight-chain alcohols in Saccharomyces cerevisiae using cDNA microarray. J Appl Microbiol 97:57–67CrossRefPubMedGoogle Scholar
  13. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257PubMedGoogle Scholar
  14. Godon C, Lagniel G, Lee J, Buhler JM, Kieffer S, Perrot M, Boucherie H, Toledano MB, Labarre J (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273:22480–22489CrossRefPubMedGoogle Scholar
  15. Guy C (1999) Molecular responses of plants to cold shock and cold acclimation. J Mol Microbiol Biotechnol 1:231–242PubMedGoogle Scholar
  16. Homma T, Iwahashi H, Komatsu Y (2003) Yeast gene expression during growth at low temperature. Cryobiology 46:230–237CrossRefPubMedGoogle Scholar
  17. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H, Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191–12198CrossRefPubMedGoogle Scholar
  18. Iwahashi H, Nwaka S, Obuchi K, Komatsu Y (1998) Evidence for the interplay between trehalose metabolism and Hsp104 in yeast. Appl Environ Microbiol 64:4614–4617PubMedGoogle Scholar
  19. Iwahashi H, Nwaka S, Obuchi K (2000) Evidence for contribution of neutral trehalase in barotolerance of Saccharomyces cerevisiae. Appl Environ Microbiol 66:5182–5185CrossRefPubMedGoogle Scholar
  20. Jones PG, Inouye M (1996) RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol Microbiol 21:1207–1218CrossRefPubMedGoogle Scholar
  21. Kandror O, Goldberg AL (1997) Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc Natl Acad Sci USA 94:4978–4981CrossRefPubMedGoogle Scholar
  22. Kandror O, DeLeon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732 (Epub 2002 July 8)CrossRefPubMedGoogle Scholar
  23. Kandror O, Bretschneider N, Kreydin E, Cavalieri D, Goldberg AL (2004). Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 13:771–781CrossRefPubMedGoogle Scholar
  24. Kitagawa E, Takahashi J, Momose Y, Iwahashi H (2002) Effects of the pesticide thiuram: genome-wide screening of indicator genes by yeast DNA microarray. Environ Sci Technol 36:3908–3915CrossRefPubMedGoogle Scholar
  25. Kondo K, Inouye M (1991) TIP 1, a cold shock-inducible gene of Saccharomyces cerevisiae. J Biol Chem 266:17537–17544PubMedGoogle Scholar
  26. Kondo K, Inouye M (1992) Yeast NSR1 protein that has structural similarity to mammalian nucleolin is involved in pre-rRNA processing. J Biol Chem 267:16252–16258PubMedGoogle Scholar
  27. Kowalski LR, Kondo K, Inouye M (1995) Cold-shock induction of a family of TIP1-related proteins associated with the membrane in Saccharomyces cerevisiae. Mol Microbiol 15:341–353PubMedGoogle Scholar
  28. Lashkari DA, DeRisi JL, McCusker JH, Namath AF, Gentile C, Hwang SY, Brown PO, Davis RW (1997) Yeast microarrays for genome wide parallel genetic and gene expression analysis. Proc Natl Acad Sci USA 94:13057–13062CrossRefPubMedGoogle Scholar
  29. Lillie SH, Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143:1384–1394PubMedGoogle Scholar
  30. Mizukami S, Suzuki Y, Kitagawa E, Iwahashi H (2004) Standardization of cDNA microarray technology for toxicogenomics; essential data for initiating cDNA microarray studies. Chem BioInformatics J 4:38–55CrossRefGoogle Scholar
  31. Moskovitz J, Berlett BS, Poston JM, Stadtman ER (1997) The yeast peptide–methionine sulfoxide reductase functions as an antioxidant in vivo. Proc Natl Acad Sci USA 94:9585–9589CrossRefPubMedGoogle Scholar
  32. Mountain HA, Bystrom AS, Larsen JT, Korch C (1991) Four major transcriptional responses in the methionine/threonine biosynthetic pathway of Saccharomyces cerevisiae. Yeast 7:781–803CrossRefPubMedGoogle Scholar
  33. Murata Y, Momose Y, Hasegawa M, Iwahasi H, Komatsu Y (2002) Cluster analysis and display of genome-wide expression profiles in dimethyl sulfoxide treatment. Chem BioInformatics J 2:18–31CrossRefGoogle Scholar
  34. Murata Y, Watanabe T, Sato M, Momose Y, Nakahara T, Oka S, Iwahashi H (2003) Dimethyl sulfoxide exposure facilitates phospholipid biosynthesis and cellular membrane proliferation in yeast cells. J Biol Chem 278:33185–33193 (Epub 2003 May 27)CrossRefPubMedGoogle Scholar
  35. Nakagawa Y, Sugioka S, Kaneko Y, Harashima S (2001) O2R, a novel regulatory element mediating Rox1p-independent O(2) and unsaturated fatty acid repression of OLE1 in Saccharomyces cerevisiae. J Bacteriol 183:745–751CrossRefPubMedGoogle Scholar
  36. Nakagawa Y, Sakumoto N, Kaneko Y, Harashima S (2002) Mga2p is a putative sensor for low temperature and oxygen to induce OLE1 transcription in Saccharomyces cerevisiae. Biochem Biophys Res Commun 291:707–713CrossRefPubMedGoogle Scholar
  37. Odani M, Komatsu Y, Oka S, Iwahashi H (2003) Screening of genes that respond to cryopreservation stress using yeast DNA microarray. Cryobiology 47:155–164CrossRefPubMedGoogle Scholar
  38. Parrou JL, Teste MA, Francois J (1997) Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology 143:1891–1900PubMedGoogle Scholar
  39. Pedrajas JR, Kosmidou E, Miranda-Vizuete A, Gustafsson JA, Wright AP, Spyrou G (1999) Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J Biol Chem 274:6366–6373CrossRefPubMedGoogle Scholar
  40. Phadtare S, Inouye M, Severinov K (2004) The mechanism of nucleic acid melting by a CspA family protein. J Mol Biol 337:147–155CrossRefPubMedGoogle Scholar
  41. Rachidi N, Martinez MJ, Barre P, Blondin B (2000) Saccharomyces cerevisiae PAU genes are induced by anaerobiosis. Mol Microbiol 35:1421–1430CrossRefPubMedGoogle Scholar
  42. Sahara T, Goda T, Ohgiya S (2002) Comprehensive expression analysis of time-dependent genetic responses in yeast cells to low temperature. J Biol Chem 277:50015–50021CrossRefPubMedGoogle Scholar
  43. Singer MA, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16:460–468CrossRefPubMedGoogle Scholar
  44. Stolc V, Katz A, Altman S (1998) Rpp2, an essential protein subunit of nuclear RNase P, is required for processing of precursor tRNAs and 35S precursor rRNA in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 95:6716–6721CrossRefPubMedGoogle Scholar
  45. Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244CrossRefPubMedGoogle Scholar
  46. Thieringer HA, Jones PG, Inouye M (1998) Cold shock and adaptation. Bioessays 20:49–57CrossRefPubMedGoogle Scholar
  47. Thomas D, Surdin-Kerjan Y (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61:503–532PubMedGoogle Scholar
  48. Thomas D, Becker A, Surdin-Kerjan Y (2000) Reverse methionine biosynthesis from S-adenosylmethionine in eukaryotic cells. J Biol Chem 275:40718–40724CrossRefPubMedGoogle Scholar
  49. Varela JC, Praekelt UM, Meacock PA, Planta RJ, Mager WH (1995) The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol Cell Biol 15:6232–6245PubMedGoogle Scholar
  50. Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol 133:910–918 (Epub 2003 September 18)CrossRefPubMedGoogle Scholar
  51. Zlotnik H, Fernandez MP, Bowers B, Cabib E (1984) Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity. J Bacteriol 159:1018–1026PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Yoshinori Murata
    • 1
  • Takayuki Homma
    • 1
    • 6
  • Emiko Kitagawa
    • 2
  • Yuko Momose
    • 1
  • Masanori S. Sato
    • 1
  • Mine Odani
    • 1
  • Hisayo Shimizu
    • 1
  • Mika Hasegawa-Mizusawa
    • 1
  • Rena Matsumoto
    • 1
  • Satomi Mizukami
    • 2
  • Katsuhide Fujita
    • 3
  • Meher Parveen
    • 4
  • Yasuhiko Komatsu
    • 5
  • Hitoshi Iwahashi
    • 1
    • 2
  1. 1.International Patent Organism DepositaryNational Institute of Advanced Industrial Science TechnologyTsukubaJapan
  2. 2.Human Stress Signal Research Center (HSS)National Institute of Advanced Industrial Science TechnologyTsukubaJapan
  3. 3.Japan Bioindustry Association (JBA) Daicel Chemical Industries, LtdTsukubaJapan
  4. 4.Research Institute for Biological Resources and FunctionsNational Institute of Advanced Industrial Science and TechnologyTsukubaJapan
  5. 5.National Institute of Technology and EvaluationChibaJapan
  6. 6.Department of Molecular and Cellular Biology, Institute for Frontier Medical ScienceKyoto UniversityKyotoJapan

Personalised recommendations