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Mechanisms of ethanol tolerance in Saccharomyces cerevisiae

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Abstract

Saccharomyces cerevisiae is a superb ethanol producer, yet is also sensitive to higher ethanol concentrations especially under high gravity or very high gravity fermentation conditions. Ethanol tolerance is associated with interplay of complex networks at the genome level. Although significant efforts have been made to study ethanol stress response in past decades, mechanisms of ethanol tolerance are not well known. With developments of genome sequencing and genomic technologies, our understanding of yeast biology has been revolutionarily advanced. More evidence of mechanisms of ethanol tolerance have been discovered involving multiple loci, multi-stress, and complex interactions as well as signal transduction pathways and regulatory networks. Transcription dynamics and profiling studies of key gene sets including heat shock proteins provided insight into tolerance mechanisms. A transient gene expression response or a stress response to ethanol does not necessarily lead to ethanol tolerance in yeast. Reprogrammed pathways and interactions of cofactor regeneration and redox balance observed from studies of tolerant yeast demonstrated the significant importance of a time-course study for ethanol tolerance. In this review, we focus on current advances of our understanding for ethanol-tolerance mechanisms of S. cerevisiae including gene expression responses, pathway-based analysis, signal transduction and regulatory networks. A prototype of global system model for mechanisms of ethanol tolerance is presented.

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References

  • Aguilera F, Peinado RA, Millán C, Ortega JM, Mauricio JC (2006) Relationship between ethanol tolerance, H+-ATPase activity and the lipid composition of the plasma membrane in different wine yeast strains. Int J Food Microbiol 110:34–42

    CAS  Google Scholar 

  • Alexandre H, Rousseaux I, Charpentier C (1994) Relationship between ethanol tolerance, lipid composition and plasma membrane fluidity in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiol Lett 124:17–22

    CAS  Google Scholar 

  • Alexandre H, Ansanay-Galeote V, Dequin S, Blondin S (2001) Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Lett 498:98–103

    CAS  Google Scholar 

  • Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314:1565–1568

    CAS  Google Scholar 

  • Auesukaree C, Damnernsawad A, Kruatrachue M, Pokethitiyook P, Boonchird C, Kaneko Y, Harashima S (2009) Genome-wide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. J Appl Genet 50:301–310

    CAS  Google Scholar 

  • Baerends RJS, Qiu JL, Rasmussen S, Nielsen HB, Brandt A (2009) Impaired uptake and/or utilization of leucine by Saccharomyces cerevisiae is suppressed by the SPT15-300 allele of the TATA-binding protein gene. Appl Environ Microbiol 75:6055–6061

    CAS  Google Scholar 

  • Bai FW, Chen LJ, Zhang Z, Anderson WA, Moo-Young M (2004) Continuous ethanol production and evaluation of yeast cell lysis and viability loss under very high gravity medium conditions. J Biotechnol 110:287–293

    CAS  Google Scholar 

  • Betz C, Schlenstedt G, Bailer SM (2004) Asr1p, a novel yeast ring/PHD finger protein, signals alcohol stress to the nucleus. J Biol Chem 279:28174–28181

    CAS  Google Scholar 

  • Blazquez MA, Lagunas R, Gancedo C, Gancedo JM (1993) Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinase. FEBS Lett 329:51–54

    CAS  Google Scholar 

  • Bonner JJ, Ballou C, Fackenthal DL (1994) Interactions between DNA-bound trimers of the yeast heat shock factor. Mol Cell Biol 14:501–508

    CAS  Google Scholar 

  • Bruinenberg PM, Van Dijken JP, Scheffers WA (1983) A theoretical analysis of NADPH production and consumption in yeasts. J Gen Microbiol 129:953–964

    CAS  Google Scholar 

  • Cakar ZP, Seker UO, Tamerler C, Sonderegger M, Sauer U (2005) Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res 5:569–578

    CAS  Google Scholar 

  • Cardona F, Carrasco P, Pérez-Ortín JE, del Olmo M, Aranda A (2007) A novel approach for the improvement of stress resistance in wine yeasts. Int J Food Microbiol 114:83–91

    CAS  Google Scholar 

  • Cartwright CP, Veazey FJ, Rose AH (1987) Effect of ethanol on activity of the plasma-membrane ATPase in, and accumulation of glycine by, Saccharomyces cerevisiae. J Gen Microbiol 133:857–865

    CAS  Google Scholar 

  • Casey GP, Ingledew WM (1986) Ethanol tolerance in yeasts. Crit Rev Microbial 13:219–280

    CAS  Google Scholar 

  • Chandler M, Stanley GA, Rogers P, Chambers P (2004) A genomic approach to defining the ethanol stress response in the yeast Saccharomyces cerevisiae. Ann Microbiol 54:427–454

    CAS  Google Scholar 

  • Chi Z, Arneborg N (1999) Relationship between lipid composition, frequency of ethanol-induced respiratory deficient mutants, and ethanol tolerance in Saccharomyces cerevisiae. J Appl Microbiol 86:1047–1052

    CAS  Google Scholar 

  • Colombo S, Ma P, Cauwenberg L, Winderickx J, Crauwels M, Teunissen A, Nauwelaers D, de Winde JH, Gorwa MF, Colavizza D, Thevelein JM (1998) Involvement of distinct G-proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J 17:3326–3341

    CAS  Google Scholar 

  • Costa V, Moradas-Ferreira P (2001) Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol Aspects Med 22:217–246

    CAS  Google Scholar 

  • Costa V, Amorim MA, Reis E, Quintanilha A, Moradas-Ferreira P (1997) Mitochondrial superoxide dismutase is essential for ethanol tolerance of Saccharomyces cerevisiae in the post-diauxic phase. Microbiol 143:1649–1656

    CAS  Google Scholar 

  • D’Amore T, Stewart GG (1987) Ethanol tolerance of yeast. Enzyme Microb Technol 9:322–330

    Google Scholar 

  • D’Amore T, Panchal CJ, Stewart GG (1990) A study of ethanol tolerance in yeast. Crit Rev Biotechnol 9:287–304

    Google Scholar 

  • Daulny A, Geng F, Muratani M, Geisinger JM, Salghetti SE, Tansey WP (2008) Modulation of RNA polymerase II subunit composition by ubiquitylation. Proc Natl Acad Sci USA 105:19649–19654

    CAS  Google Scholar 

  • del Castillo AL (1992) Lipid content of Saccharomyces cerevisiae strains with different degrees of ethanol tolerance. Appl Microbiol Biotechnol 37:647–651

    Google Scholar 

  • Ding J, Huang X, Zhang L, Zhao N, Yang D, Zhang K (2009) Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 85:253–263

    CAS  Google Scholar 

  • Dinh TN, Nagahisa K, Hirasawa T, Furusawa C, Shimizu H (2008) Adaptation of Saccharomyces cerevisiae cells to high ethanol concentration and changes in fatty acid composition of membrane and cell size. PLoS ONE 3:e2623

    Google Scholar 

  • Dinh TN, Nagahisa K, Yoshikawa K, Hirasawa T, Furusawa C, Shimizu H (2009) Analysis of adaptation to high ethanol concentration in Saccharomyces cerevisiae using DNA microarray. Bioprocess Biosyst Eng 32:681–688

    CAS  Google Scholar 

  • Du X, Takagi H (2007) N-Acetyltransferase Mpr1 confers ethanol tolerance on Saccharomyces cerevisiae by reducing reactive oxygen species. Appl Microbiol Biotechnol 75:1343–1351

    CAS  Google Scholar 

  • Durchschlag E, Reiter W, Ammerer G, Schuller C (2004) Nuclear localization destabilizes the stress-regulated transcription factor Msn2. J Biol Chem 279:55425–55432

    CAS  Google Scholar 

  • Eastmond DL, Nelson HC (2006) Genome-wide analysis reveals new roles for the activation domains of the Saccharomyces cerevisiae heat shock transcription factor (Hsf1) during the transient heat shock response. J Biol Chem 281:32909–32921

    CAS  Google Scholar 

  • Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24:469–486

    CAS  Google Scholar 

  • Fernandes L, Rodrigues-Pousada C, Struhl K (1997) Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol Cell Biol 17:6982–6993

    CAS  Google Scholar 

  • Forgac M (1998) Structure, function and regulation of the vacuolar (H+)-ATPases. FEBS Lett 440:258–263

    CAS  Google Scholar 

  • Francois J, Parrou JL (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25:125–145

    CAS  Google Scholar 

  • Fujita K, Matsuyama A, Kobayashi Y, Iwahashi H (2006) The genome-wide screening of yeast deletion mutants to identify the genes required for tolerance to ethanol and other alcohols. FEMS Yeast Res 6:744–750

    CAS  Google Scholar 

  • 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 11:4241–4257

    CAS  Google Scholar 

  • Geymonat M, Wang L, Garreau H, Jacquet M (1998) Ssa1p chaperone interacts with the guanine nucleotide exchange factor of Ras Cdc25p and controls the cAMP pathway in Saccharomyces cerevisiae. Mol Microbiol 30:855–864

    CAS  Google Scholar 

  • Gibson BR, Lawrence SJ, Leclaire JP, Powell CD, Smart KA (2007) Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol Rev 31:535–569

    CAS  Google Scholar 

  • Gong Y, Kakihara Y, Krogan N, Greenblatt J, Emili A, Zhang Z, Houry WA (2009) An atlas of chaperone-protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Mol Syst Biol 5:275

    Google Scholar 

  • Hahn JS, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24:5249–5256

    CAS  Google Scholar 

  • Hahn S (2004) Structure and mechanism of the RNA polymerase II transcription machinery. Nat Struct Mol Biol 11:394–403

    CAS  Google Scholar 

  • Hara S, Sasaki M, Obata T, Noshiro K (1976a) Isolation of ethanol tolerant mutants from sake yeast Kyotai no. 7. J Brew Soc Jpn 71:301–304

    CAS  Google Scholar 

  • Hara S, Yamamoto N, Fukuda Y, Obata T, Noshiro K (1976b) Comparison of physiological characteristics between sake yeast Kyokai no. 7 and its ethanol tolerant mutant. J Brew Soc Jpn 71:564–568

    CAS  Google Scholar 

  • Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne JB, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431:99–104

    CAS  Google Scholar 

  • Hartley AD, Ward MP, Garrett S (1994) The Yak1 protein kinase of Saccharomyces cerevisiae moderates thermotolerance and inhibits growth by an Sch9 protein kinase-independent mechanism. Genetics 136:465–474

    CAS  Google Scholar 

  • Hashikawa N, Mizukami Y, Imazu H, Sakurai H (2006) Mutated yeast heat shock transcription factor activates transcription independently of hyperphosphorylation. J Biol Chem 281:3936–3942

    CAS  Google Scholar 

  • Herman PK (2002) Stationary phase in yeast. Curr Opin Microbiol 5:602–607

    CAS  Google Scholar 

  • Hirasawa T, Yoshikawa K, Nakakura Y, Nagahisa K, Furusawa C, Katakura Y, Shimizu H, Shioya S (2007) Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J Biotechnol 131:34–44

    CAS  Google Scholar 

  • Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372

    CAS  Google Scholar 

  • Hou J, Lages NF, Oldiges M, Vemuri GN (2009) Metabolic impact of redox cofactor perturbations in Saccharomyces cerevisiae. Metab Eng 11:253–261

    CAS  Google Scholar 

  • Hu XH, Wang MH, Tan T, Li JR, Yang H, Leach L, Zhang RM, Luo ZW (2007) Genetic dissection of ethanol tolerance in the budding yeast Saccharomyces cerevisiae. Genetics 175:1479–1487

    CAS  Google Scholar 

  • Inoue T, Wang Y, Jefferies K, Qi J, Hinton A, Forgac M (2005) Structure and regulation of the V-ATPases. J Bioenerg Biomembr 37:393–398

    CAS  Google Scholar 

  • Izawa S, Ikeda K, Kita T, Inoue Y (2006) Asr1, an alcohol-responsive factor of Saccharomyces cerevisiae, is dispensable for alcoholic fermentation. Appl Microbiol Biotechnol 72:560–565

    CAS  Google Scholar 

  • Kaino T, Takagi H (2008) Gene expression profiles and intracellular contents of stress protectants in Saccharomyces cerevisiae under ethanol and sorbitol stresses. Appl Microbiol Biotechnol 79:273–283

    CAS  Google Scholar 

  • Kobayashi N, McEntee K (1993) Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13:248–256

    CAS  Google Scholar 

  • Kubota S, Takeo I, Kume K, Kanai M, Shitamukai A, Mizunuma M, Miyakawa T, Shimoi H, Iefuji H, Hirata D (2004) Effect of ethanol on cell growth of budding yeast: genes that are important for cell growth in the presence of ethanol. Biosci Biotechnol Biochem 68:968–972

    CAS  Google Scholar 

  • Lee S, Carlson T, Christian N, Lea K, Kedzie J, Reilly JP, Bonner JJ (2000) The yeast heat shock transcription factor changes conformation in response to superoxide and temperature. Mol Biol Cell 11:1753–1764

    CAS  Google Scholar 

  • Lin Y, Tanaka S (2006) Ethanol fermentation from biomass resources: current state and prospects. Appl Microbiol Biotechnol 69:627–642

    CAS  Google Scholar 

  • Liu ZL (2006) Genomic adaptation of ethanologenic yeast to biomass conversion inhibitors. Appl Microbiol Biotechnol 73:27–36

    CAS  Google Scholar 

  • Liu ZL, Saha BC, Slininger PJ (2008) Lignocellulosic biomass conversion to ethanol by Saccharomyces. In: Wall J, Harwood C, Demain A (eds) Bioenergy. ASM, Washington, DC, pp 17–36

    Google Scholar 

  • Liu ZL, Ma M, Song M (2009) Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Mol Genet Genomics 282:233–244

    Google Scholar 

  • Lockshon D, Surface LE, Kerr EO, Kaeberlein M, Kennedy BK (2007) The sensitivity of yeast mutants to oleic acid implicates the peroxisome and other processes in membrane function. Genetics 175:7–91

    Google Scholar 

  • Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction. Plant J 31:699–712

    CAS  Google Scholar 

  • Mansure JJC, Panek AD, Crowe LM, Crowe JH (1994) Trehalose inhibits ethanol effects on intact yeast cells and liposomes. Biochim Biophys Acta 1191:309–316

    CAS  Google Scholar 

  • Marchler G, Schuller C, Adam G, Ruis H (1993) A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 12:1997–2003

    CAS  Google Scholar 

  • Marks VD, Ho Sui SJ, Erasmus D, van der Merwe GK, Brumm J, Wasserman WW, Bryan J, van Vuuren HJ (2008) Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 8:35–52

    CAS  Google Scholar 

  • Martin CE, Oh CS, Jiang Y (2007) Regulation of long chain unsaturated fatty acid synthesis in yeast. Biochim Biophys Acta 1771:271–285

    CAS  Google Scholar 

  • Martínez-Pastor MT, Marchler G, Schuller C, Marchler-Bauer A, Ruis H, Estruch F (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15:2227–2235

    Google Scholar 

  • McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, Frydman J (2007) Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 131:121–135

    CAS  Google Scholar 

  • Millar DG, Griffiths-Smith K, Algar E, Scopes RK (1982) Activity and stability of glycolytic enzymes in the presence of ethanol. Biotechnol Lett 9:601–606

    Google Scholar 

  • Moskvina E, Schuller C, Maurer CT, Mager WH, Ruis H (1998) A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast 14:1041–1050

    CAS  Google Scholar 

  • Moukadiri I, Zueco J (2001) Evidence for the attachment of Hsp150/Pir2 to the cell wall of Saccharomyces cerevisiae through disulfide bridges. FEMS Yeast Res 1:241–245

    CAS  Google Scholar 

  • Müller D, Exler S, Aguilera-Vázquez L, Guerrero-Martín E, Reuss M (2003) Cyclic AMP mediates the cell cycle dynamics of energy metabolism in Saccharomyces cerevisiae. Yeast 20:351–367

    Google Scholar 

  • Nevoigt E (2008) Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 72:379–412

    CAS  Google Scholar 

  • Nguyên DT, Alarco AM, Raymond M (2001) Multiple Yap1p-binding sites mediate induction of the yeast major facilitator FLR1 gene in response to drugs, oxidants, and alkylating agents. J Biol Chem 276:1138–1145

    Google Scholar 

  • Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJ (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9:44

    Google Scholar 

  • Ogawa Y, Nitta A, Uchiyama H, Imamura T, Shiomoi H, Ito K (2000) Tolerance mechanism of the ethanol-tolerant mutant of sake yeast. J Biosci Bioeng 90:313–320

    CAS  Google Scholar 

  • Outlaw J, Collins KJ, Duffield JA (2005) Agriculture as a producer and consumer of energy. CABI, Oxfordshire

    Google Scholar 

  • Parsell DA, Kowal AS, Singer MA, Lindquist S (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372:475–478

    CAS  Google Scholar 

  • Pascual C, Alonso A, García I, Romay C (1988) Effect of ethanol on glucose transport, key glycolitic enzymes and proton extrusion in Saccharomyces cerevisiae. Biotechnol Bioeng 32:374–378

    CAS  Google Scholar 

  • Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648

    CAS  Google Scholar 

  • Pina C, António J, Hogg T (2004) Inferring ethanol tolerance of Saccharomyces and non-Saccharomyces yeasts by progressive inactivation. Biotechnol Lett 26:1521–1527

    CAS  Google Scholar 

  • Piper PW (1995) The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol Lett 134:121–127

    CAS  Google Scholar 

  • Piper PW, Talreja K, Panaretou B, Moradas-Ferreira P, Byrne K, Praekelt UM, Meacock P, Récnacq M, Boucherie H (1994) Induction of major heat-shock proteins of Saccharomyces cerevisiae, including plasma membrane Hsp30, by ethanol levels above a critical threshold. Microbiology 140:3031–3038

    CAS  Google Scholar 

  • Piper PW, Ortiz-Calderon C, Holyoak C, Coote P, Cole M (1997) Hsp30, the integral plasma membrane heat shock protein of Saccharomyces cerevisiae, is a stress-inducible regulator of plasma membrane H+-ATPase. Cell Stress Chaperones 2:12–24

    CAS  Google Scholar 

  • Prodromou C, Pearl LH (2003) Structure and functional relationships of Hsp90. Curr Cancer Drug Targets 3:301–323

    CAS  Google Scholar 

  • Puig S, Pérez-Ortín JE (2000) Stress response and expression patterns in wine fermentations of yeast genes induced at the diauxic shift. Yeast 16:139–148

    CAS  Google Scholar 

  • Reinders A, Burckert N, Boller T, Wiemken A, De Virgilio C (1998) Saccharomyces cerevisiae cAMP dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev 12:2943–2955

    CAS  Google Scholar 

  • Rep M, Krantz M, Thevelein JM, Hohmann S (2000) The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275:8290–8300

    CAS  Google Scholar 

  • Rosa MF, Sá-Correia I (1996) Intracellular acidification does not account for inhibition of Saccharomyces cerevisiae growth in the presence of ethanol. FEMS Microbiol Lett 135:271–274

    CAS  Google Scholar 

  • Rudolph AS, Crowe JH (1985) Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology 22:367–377

    CAS  Google Scholar 

  • Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545

    CAS  Google Scholar 

  • Sajbidor J, Ciesarova Z, Smogrovicova D (1995) Influence of ethanol on the lipid content and fatty acid composition of Saccharomyces cerevisiae. Folia Microbiol 40:508–510

    CAS  Google Scholar 

  • Salgueiro SP, Sá-Correia I, Novais JM (1988) Ethanol induced-leakage in Saccharomyces cerevisiae: kinetics and relationship to yeast ethanol tolerance and alcohol fermentation productivity. Appl Environ Microbiol 54:903–909

    CAS  Google Scholar 

  • Samuel D, Kumar TKS, Ganesh G, Jayaraman G, Yang PW, Chang MM, Trivedi VD, Wang SL, Hwang KC, Chang DK, Yu C (2000) Proline inhibits aggregation during protein refolding. Protein Sci 9:344–352

    CAS  Google Scholar 

  • Sanchez OJ, Cardona CA (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour Technol 99:5270–5295

    CAS  Google Scholar 

  • Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 73:129–169

    CAS  Google Scholar 

  • Schrader M, Fahimi HD (2004) Mammalian peroxisomes and reactive oxygen species. Histochem Cell Biol 122:383–393

    CAS  Google Scholar 

  • Schuller C, Brewster JL, Alexander MR, Gustin MC, Ruis H (1994) The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J 13:4382–4389

    CAS  Google Scholar 

  • Sebollela A, Louzada PR, Sola-Penna M, Sarrone-Williams V, Coelho-Sampaio T, Ferreira ST (2004) Inhibition of yeast glutathione reductase by trehalose: possible implications in yeast survival and recovery from stress. Int J Biochem Cell Biol 36:900–908

    CAS  Google Scholar 

  • Singer MA, Lindquist S (1998) Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1:639–648

    CAS  Google Scholar 

  • Stukey JE, McDonough VM, Martin CE (1989) Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae. J Biol Chem 264:16537–16544

    CAS  Google Scholar 

  • Stukey JE, McDonough VM, Martin CE (1990) The OLE1 gene of Saccharomyces cerevisiae encodes the Δ9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. J Biol Chem 265:20144–20149

    CAS  Google Scholar 

  • Takagi H (2008) Proline as a stress protectant in yeast: physiological functions, metabolic regulations and biotechnological applications. Appl Microbiol Biotechnol 81:211–223

    CAS  Google Scholar 

  • Takagi H, Takaoka M, Kawaguchi A, Kubo Y (2005) Effect of L-proline on sake brewing and ethanol stress in Saccharomyces cerevisiae. Appl Environ Microbiol 71:8656–8662

    CAS  Google Scholar 

  • Takagi H, Matsui F, Kawaguchi A, Wu H, Shimoi H, Kubo Y (2007) Construction and analysis of self-cloning sake yeasts that accumulate proline. J Biosci Bioeng 103:377–380

    CAS  Google Scholar 

  • Takemori Y, Sakaguchi A, Matsuda S, Mizukami Y, Sakurai H (2006) Stress-induced transcription of the endoplasmic reticulum oxidoreductin gene ERO1 in the yeast Saccharomyces cerevisiae. Mol Genet Genomics 275:89–96

    CAS  Google Scholar 

  • Teixeira MC, Monteiro P, Jain P, Tenreiro S, Fernandes AR, Mira NP, Alenquer M, Freitas AT, Oliveira AL, Sá-Correia I (2006) The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucl Acids Res 34:D446–D451

    CAS  Google Scholar 

  • Teixeira MC, Raposo LR, Mira NP, Lourenço AB, Sá-Correia I (2009) Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Appl Environ Microbiol 75:5761–5772

    CAS  Google Scholar 

  • Thevelein JM (1991) Fermentable sugars and intracellular acidification as specific activators of the RAS-adenylate cyclase signaling pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol 5:1301–1307

    CAS  Google Scholar 

  • Thevelein JM, de Winde JH (1999) Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33:904–918

    CAS  Google Scholar 

  • Van Uden N (1985) Ethanol toxicity and ethanol tolerance in yeasts. Ann Rep Ferment Process 8:11–58

    Google Scholar 

  • Van Voorst F, Houghton-Larsen J, Jønson L, Kielland-Brandt MC, Brandt A (2006) Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under ethanol stress. Yeast 23:351–359

    Google Scholar 

  • Vertes A, Qureshi N, Yukawa H, Blaschek H (2010) Biomass to biofuels. Wiley, West Sussex

    Google Scholar 

  • Wall J, Harwood C, Demain A (2008) Bioenergy. ASM, Washington

    Google Scholar 

  • Watanabe M, Tamura K, Magbanua JP, Takano K, Kitamoto K, Kitagaki H, Akao T, Shimoi H (2007) Elevated expression of genes under the control of stress response element (STRE) and Msn2p in an ethanol-tolerance sake yeast Kyokai no. 11. J Biosci Bioeng 104:163–170

    CAS  Google Scholar 

  • Watanabe M, Watanabe D, Akao T, Shimoi H (2009) Overexpression of MSN2 in a sake yeast strain promotes ethanol tolerance and increases ethanol production in sake brewing. J Biosci Bioeng 107:516–518

    CAS  Google Scholar 

  • Wei P, Li Z, Lin Y, He P, Jiang N (2007) Improvement of the multiple-stress tolerance of an ethanologenic Saccharomyces cerevisiae strain by freeze-thaw treatment. Biotechnol Lett 29:1501–1508

    CAS  Google Scholar 

  • Wilson WA, St Amour CV, Collins JL, Ringe D, Petsko GA (2004) The 1.8-A resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: a member of the DJ-1/ThiJ/PfpI superfamily. Pro Natl Acad Sci USA 101:1531–1536

    CAS  Google Scholar 

  • Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T, Shimizu H (2009) Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res 9:32–44

    CAS  Google Scholar 

  • You KM, Rosenfield CL, Knipple DC (2003) Ethanol tolerance in the yeast Saccharomyces cerevisiae is dependent on cellular oleic acid content. Appl Environ Microbiol 69:1499–1503

    CAS  Google Scholar 

  • Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5:781–791

    CAS  Google Scholar 

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Acknowledgments

The authors thank Michael A. Cotta for critically reading the manuscript and helpful suggestions. This study was supported in part by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2006-35504-17359.

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Authors and Affiliations

  1. U.S. Department of Agriculture, ARS, Bioenergy Research, National Center for Agricultural Utilization Research, 1815 N University St., Peoria, IL, 61604, USA

    Menggen Ma & Z. Lewis Liu

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  1. Menggen Ma
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  2. Z. Lewis Liu
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Correspondence to Z. Lewis Liu.

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Ma, M., Liu, Z.L. Mechanisms of ethanol tolerance in Saccharomyces cerevisiae . Appl Microbiol Biotechnol 87, 829–845 (2010). https://doi.org/10.1007/s00253-010-2594-3

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  • DOI: https://doi.org/10.1007/s00253-010-2594-3

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