Skip to main content

Advertisement

Log in

Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Pretreatment of lignocellulose biomass for biofuel production generates inhibitory compounds that interfere with microbial growth and subsequent fermentation. Remediation of the inhibitors by current physical, chemical, and biological abatement means is economically impractical, and overcoming the inhibitory effects of lignocellulose hydrolysate poses a significant technical challenge for lower-cost cellulosic ethanol production. Development of tolerant ethanologenic yeast strains has demonstrated the potential of in situ detoxification for numerous aldehyde inhibitors derived from lignocellulose biomass pretreatment and conversion. In the last decade, significant progress has been made in understanding mechanisms of yeast tolerance for tolerant strain development. Enriched genetic backgrounds, enhanced expression, interplays, and global integration of many key genes enable yeast tolerance. Reprogrammed pathways support yeast functions to withstand the inhibitor stress, detoxify the toxic compounds, maintain energy and redox balance, and complete active metabolism for ethanol fermentation. Complex gene interactions and regulatory networks as well as co-regulation are well recognized as involved in yeast adaptation and tolerance. This review presents our current knowledge on mechanisms of the inhibitor detoxification based on molecular studies and genomic-based approaches. Our improved understanding of yeast tolerance and in situ detoxification provide insight into phenotype-genotype relationships, dissection of tolerance mechanisms, and strategies for more tolerant strain development for biofuels applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alenquer M, Tenreiro S, Sá-Correia I (2006) Adaptive response to the antimalarial drug artesunate in yeast involves Pdr1p/Pdr3p-mediated transcriptional activation of the resistance determinants TPO1and PDR5. FEMS Yeast Res 6:1130–1139

    Article  CAS  PubMed  Google Scholar 

  • Almeida JRM, Roder A, Modig T, Laadan B, Liden G, Gorwa-Grauslund M (2008) NADH - vs NADPH-coupled reduction of 5-hydroxymethylfurfural (HMF) and its implications on product distribution in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 78:939–945

    Article  CAS  PubMed  Google Scholar 

  • Alriksson B, Horváth IS, Jönsson LJ (2010) Overexpression of Saccharomyces cerevisiae transcription factor and multidrug resistance genes conveys enhanced resistance to lignocellulose-derived fermentation inhibitors. Process Biochem 45:264–271

    Article  CAS  Google Scholar 

  • Bowman MJ, Jordan DB, Vermillion KE, Braker JD, Moon J, Liu ZL (2010) Stereochemistry of furfural reduction by an aldehyde reductase from Saccharomyces cerevisiae that contributes to in situ furfural detoxification. Appl Envir Microbiol 76:4926–4932

    Article  CAS  Google Scholar 

  • Burnie JP, Carter TL, Hodgetts SJ, Matthews RC (2006) Fungal heat-shock proteins in human disease. FEMS Microbiol Rev 30:53–88

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Derfler B, Samson L (1990) Saccharomyces cerevisiae 3-methyladenine DNA glycosylase has homology to the AlkA glycosylase of E. coli and is induced in response to DNA alkylation damage. EMBO J 9:4569–4575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke DJ, Mondesert G, Segal M, Bertolaet BL, Jensen S, Wolff M, Henze M, Reed SI (2001) Dosage suppressors of pds1 implicate ubiquitin-associated domains in checkpoint control. Mol Cell Biol 21:1997–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Rijcke M, Seneca S, Punyammalee B, Glansdorff N, Crabeel M (1992) Characterization of the DNA target site for the yeast ARGR regulatory complex, a sequence able to mediate repression or induction by arginine. Mol Cell Biol 12:68–81

    Article  PubMed  PubMed Central  Google Scholar 

  • De Risi J, van den Hazel B, Marc P, Balzi E, Brown P, Jacq C, Goffeau A (2000) Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants. FEBS Lett 470:156–160

    Article  Google Scholar 

  • Delahodde A, Delaveau T, Jacq C (1995) Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance. Mol Cell Biol 15:4043–4051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubacq C, Chevalier A, Courbeyrette R, Petat C, Gidrol X, Mann C (2006) Role of the iron mobilization and oxidative stress regulons in the genomic response of yeast to hydroxyurea. Mol Genet Genomics 275:114–124

    Article  CAS  PubMed  Google Scholar 

  • Ferguson SB, Anderson ES, Harshaw RB, Thate T, Craig NL, Nelson HC (2005) Protein kinase A regulates constitutive expression of small heat-shock genes in an Msn2/4p-independent and Hsf1p-dependent manner in Saccharomyces cerevisiae. Genetics 169:1203–1214

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisk DG, Ball CA, Dolinski K, Engel SR, Hong EL, Issel-Tarver L, Schwartz K, Sethuraman A, Botstein D, Cherry JM (2006) Saccharomyces cerevisiae S288C genome annotation: a working hypothesis. Yeast 23:857–865

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Pastushok L, Xiao W (2008) DNA damage-induced gene expression in Saccharomyces cerevisiae. FEMS Microbiol Rev 32:908–926

    Article  CAS  PubMed  Google Scholar 

  • Gasch AP, Werner-Washburne M (2002) The genomics of yeast responses to environmental stress and starvation. Funct Integr Genomics 2:181–192

    Article  CAS  PubMed  Google Scholar 

  • Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression program in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh AK, Ramakrishnan G, Rajasekharan R (2008) YLR099C (ICT1) encodes a soluble Acyl-CoA-dependent lysophosphatidic acid acyltransferase responsible for enhanced phospholipid synthesis on organic solvent stress in Saccharomyces cerevisiae. J Biol Chem 283:9768–9775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg AL (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426:895–899

    Article  CAS  PubMed  Google Scholar 

  • Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD (2006) Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 71:339–349

    Article  CAS  PubMed  Google Scholar 

  • Glickman MH, Ciechanover A (2002) The ubiquitin proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428

    Article  CAS  PubMed  Google Scholar 

  • Hahn JS, Neef DW, Thiele DJ (2006) A stress regulatory network for co-ordinated activation of proteasome expression mediated by yeast heat shock transcription factor. Mol Microbiol 60:240–251

    Article  CAS  PubMed  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 31:99–104

    Article  CAS  Google Scholar 

  • Haugen AC, Kelley R, Collins JB, Tucker CJ, Deng C, Afshari CA, Brown JM, Ideker T, Van Houten B (2004) Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol 5:R95

    Article  PubMed  PubMed Central  Google Scholar 

  • Heer D, Heine D, Sauer U (2009) Resistance of Saccharomyces cerevisiae to high concentrations of furfural is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol 75:7631–7638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellauer K, Rochon MH, Turcotte B (1996) A novel DNA binding motif for yeast zinc cluster proteins: the Leu3p and Pdr3p transcriptional activators recognize everted repeats. Mol Cell Biol 16:6096–6102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrero E, Ros J, Belli G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biotechnica Biophysica Acta 1780:1217–1235

    Article  CAS  Google Scholar 

  • Jungwirth H, Kuchler K (2006) Yeast ABC transporters – a tale of sex, stress, drugs, and aging. FEBS Lett 580:1131–1138

    Article  CAS  PubMed  Google Scholar 

  • Katzmann DJ, Hallstrom TC, Voet M, Wysock W, Golin J, Volckaert G, Moyle-Rowley WS (1995) Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol Cell Biol 15:6875–6883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kihara A, Igarashi Y (2004) Cross talk between sphingolipids and glycerophospholipids in the establishment of plasma membrane asymmetry. Mol Biol Cell 15:4949–4959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66:10–26

    Article  CAS  PubMed  Google Scholar 

  • Kuyper M, Toirkens MJ, Diderich JA, Winkler AA, van Dijken JP, Pronk JT (2005) Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain. FEMS Yeast Res 5:925–934

    Article  CAS  PubMed  Google Scholar 

  • Laadan B, Almeida JRM, Radstrom P, Hahn-Hagerdal B, Gorwa-Grauslund M (2008) Identification of an NADH-dependent 5-hydroxymethylfurfural-reducing alcohol dehydrogenase in Saccharomyces cerevisiae. Yeast 25:191–198

    Article  CAS  PubMed  Google Scholar 

  • Larochelle M, Drouin S, Robert F, Turcotte B (2006) Oxidative stress-activated zinc cluster protein Stb5 has dual activator/repressor functions required for pentose phosphate pathway regulation and NADPH production. Mol Cell Biol 26:6690–6701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larroy C, Fernadez MR, Gonzalez E, Pares X, Biosca JA (2002a) Characterization of the Saccharomyces cerevisiae YMR318C (ADH6) gene product as a broad specificity NADPH-dependent alcohol dehydrogenase: relevance in aldehyde reduction. Biochem J 361:163–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larroy C, Pares X, Biosca JA (2002b) Characterization of a Saccharomyces cerevisiae NADP(H)-dependent alcohol dehydrogenase (ADHVII), a member of the cinnamyl alcohol dehydrogenase family. Eur J Biochem 269:5738–5745

    Article  CAS  PubMed  Google Scholar 

  • Larroy C, Rosario FM, Gonzalez E, Pares X, Biosca JA (2003) Properties and functional significance of Saccharomyces cerevisiae ADHVI. Chem Biol Interact 143–144:229–238

    Article  CAS  PubMed  Google Scholar 

  • Larsson S, Palmqvist E, Hahn-Hägerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant N (1999) The generation of fermentation inhibitors during dilute acid hydrolysis of softwood. Enzy Micro Technol 24:151–159

    Article  CAS  Google Scholar 

  • Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, Gerber GK, Hannett NM, Harbison CT, Thompson CM, Simon I, Zeitlinger J, Jennings EG, Murray HL, Gordon DB, Ren B, Wyrick JJ, Tagne JB, Volkert TL, Fraenkel E, Gifford DK, Young RA (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298:799–804

    Article  CAS  PubMed  Google Scholar 

  • Li Bz, Yuan Yj (2010) Transcriptome shifts in response to furfural and acetic acid in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 86:1915–1924

    Article  CAS  PubMed  Google Scholar 

  • Lin FM, Qiao B, Yuan YJ (2009a) Comparative proteomic analysis for tolerance and adaptation of ethanologenic Saccharomyces cerevisiae to furfural, a lignocellulosic inhibitory compound. Appl Environ Microbiol 75:3765–3776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin FM, Tan Y, Yuan YJ (2009b) Temporal quantitative proteomics of Saccharomyces cerevisiae in response to a nonlethal concentration of furfural. Proteomics 9:5471–5483

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu, Z.L., B.J. Andersh, and P.J. Slininger, (2007). Mechanisms of in situ detoxification of furfural and HMF by ethanologenic yeast Saccharomyces cerevisiae. 29th Symposium of Biofuels and Chemicals. Abs. 85.

  • Liu ZL, Blaschek HP (2010) Lignocellulosic biomass conversion to ethanol by Saccharomyces. In: Vertes A, Qureshi N, Yukawa H, Blaschek H (eds) Biomass to biofuels: strategies for global industries. John Wiley & Sons, Ltd, West Sussex, UK, pp 17–36

    Google Scholar 

  • Liu ZL, Moon J (2009) A novel NADPH-dependent aldehyde reductase gene from Saccharomyces cerevisiae NRRL Y-12632 involved in the detoxification of aldehyde inhibitors derived from lignocellulosic biomass conversion. Gene 446:1–10

    Article  CAS  PubMed  Google Scholar 

  • Liu ZL, Slininger PJ (2005) Development of genetically engineered stress tolerant ethanologenic yeasts using integrated functional genomics for effective biomass conversion to ethanol. In: Outlaw J, Collins K, Duffield J (eds) Agriculture as a producer and consumer of energy CAB International. Wallingford, UK, pp 283–294

    Chapter  Google Scholar 

  • Liu ZL, Slininger PJ (2006) Transcriptome dynamics of ethanologenic yeast in response to 5-hydroxymethylfurfural stress related to biomass conversion to ethanol. In: Recent research developments in multidisciplinary applied microbiology: understanding and exploiting microbes and their interactions-biological, physical, chemical and engineering aspects (Mendez-Vilas A Ed) Wiley-VCH, pp679-684

  • Liu ZL, Slininger PJ, Dien BS, Berhow MA, Kurtzman CP, Gorsich SW (2004) Adaptive response of yeasts to furfural and 5-hydroxymethylfurfural and new chemical evidence for HMF conversion to 2, 5-bis-hydroxymethylfuran. J Ind Microbiol Biotechnol 31:345–352

    Article  CAS  PubMed  Google Scholar 

  • Liu ZL, Slininger PJ, Gorsich SW (2005) Enhanced biotransformation of furfural and 5-hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 121–124:451–460

    Article  PubMed  Google Scholar 

  • Liu ZL, Moon J, Andersh AJ, Slininger PJ, Weber S (2008a) Multiple gene mediated NAD(P)H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and HMF by ethanologenic yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 81:743–753

    Article  CAS  PubMed  Google Scholar 

  • Liu ZL, Saha BC, Slininger PJ (2008b) Lignocellulosic biomass conversion to ethanol by Saccharomyces. In: Wall J, Harwood C, Demain A (eds) Bioenergy. ASM Press, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma M, Liu ZL (2010) Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae. BMC Genomics 11:660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70:583–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahé Y, Lemoine Y, Kuchler K (1996) The ATP binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in vivo. J Biol Chem 271:25167–25172

    Article  PubMed  Google Scholar 

  • Mamnun YM, Pandjaitan R, Mahé Y, Delahodde A, Kuchler K (2002) The yeast zinc finger regulators Pdr1p and Pdr3p control pleiotropic drug resistance (PDR) as homo- and heterodimers in vivo. Mol Microbiol 46:1429–1440

    Article  CAS  PubMed  Google Scholar 

  • Mannhaupt G, Schnall R, Karpov V, Vetter I, and Feldmann (1999) Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett 450:27–34

  • Martin C, Marcelo M, Almazan O, Jonsson LJ (2007) Adaptation of a recombinant xylose-utilizing Saccharomyces cerevisiae strain to a sugarcane bagasse hydrolysate with high content of fermentation inhibitors. Bioresour Technol 98:1767–1773

    Article  CAS  PubMed  Google Scholar 

  • Miura S, Zou W, Ueda M, Tanaka A (2000) Screening of genes involved in isooctane tolerance in Saccharomyces cerevisiae by using mRNA differential display. Appl Environ Microbiol 66:4883–4889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon J, Liu ZL (2011) Protein engineering of GRE2 from Saccharomyces cerevisiae for enhanced detoxification of 5-hydroxymethylfurfural. (submitted)

  • Morimoto S, Murakami M (1967) Studies on fermentation products from aldehyde by microorganisms: the fermentative production of furfural alcohol from furfural by yeasts (part I). J Ferment Technol 45:442–446

    CAS  Google Scholar 

  • Moye-Rowley WS (2003) Transcriptional control of multidrug resistance in the yeast Saccharomyces. Prog Nucleic Acid Res Mol Biol 73:251–279

    Article  CAS  PubMed  Google Scholar 

  • Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, Marton MJ (2001) Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol 21:4347–4368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemirovskii V, Gusarova L, Rakhmilevich Y, Sizov A, Kostenko V (1989) Pathways of furfurol and oxymethyl furfurol conversion in the process of fodder yeast cultivation. Biotekhnologiya 5:285–289

    CAS  Google Scholar 

  • Nichols NN, Dien BS, Cotta MA (2010) Fermentation of bioenergy crops into ethanol using biological abatement for removal of inhibitors. Bioresour Technol 101(19):7545–7550

    Article  CAS  PubMed  Google Scholar 

  • Nilsson A, Gorwa-Grauslund MF, Hahn-Hagerdal B, Liden G (2005) Cofactor dependence in furan reduction by Saccharomyces cerevisiae in fermentation of acid-hydrolyzed lignocellulose. App Environ Microbiol 71:7866–7871

    Article  CAS  Google Scholar 

  • Onda M, Ota K, Chiba T, Sakaki Y, Ito T (2004) Analysis of gene network regulating yeast multidrug resistance by artificial activation of transcription factors: involvement of Pdr3 in salt tolerance. Gene 332:51–59

    Article  CAS  PubMed  Google Scholar 

  • Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33

    Article  CAS  Google Scholar 

  • Petersson A, Almeida JR, Modig T, Karhumma K, Hahn-Hägerdal B, Gorwa-Grauslund MF (2006) A 5-hydroxymethylfurfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23:455–464

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues-Pousada C, Menezes RA, Pimentel C (2010) The Yap family and its role in stress response. Yeast 27:245–258

    Article  CAS  PubMed  Google Scholar 

  • Salin H, Fardeau V, Piccini E, Lelandais G, Tanty V, Lemoine S, Jacq C, Devaux F (2008) Structure and properties of transcriptional networks driving selenite stress response in yeasts. BMC Genomics 9:333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song M, Liu ZL (2007) A linear discrete dynamic system model for temporal gene interaction and regulatory network influence in response to bioethanol conversion inhibitor HMF for ethanologenic yeast. Lect Notes Bioinfomatics 4532:77–95

    Google Scholar 

  • Song M, Ouyang Z, Liu ZL (2009) Discrete dynamic system modeling for gene regulatory networks of HMF tolerance for ethanologenic yeast. IET Syst Biol 3:203–218

    Article  CAS  PubMed  Google Scholar 

  • Sundstrom L, Larsson S, Jonsson LJ (2010) Identification of Saccharomyces cerevisiae genes involved in the resistance to phenolic fermentation inhibitors. Appl Biochem Biotechnol 161:106–115

    Article  CAS  PubMed  Google Scholar 

  • Taherzadeh MJ, Gustafsson L, Niklasson C, Liden G (2000) Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 53:701–708

    Article  CAS  PubMed  Google Scholar 

  • Talebnia F, Taherzadeh MJ (2006) In situ detoxification and continuous cultivation of dilute-acid hydrolysate to ethanol by encapsulated S. cerevisiae. J Biotechnol 125:377–384

    Article  CAS  PubMed  Google Scholar 

  • Teixeira MC, Sá-Correia I (2002) Saccharomyces cerevisiae resistance to chlorinated phenoxyacetic acid herbicides involves Pdr1p-mediated transcriptional activation of TPO1 and PDR5 genes. Biochem Biophys Res Commun 292:530–537

    Article  CAS  PubMed  Google Scholar 

  • Tomitori H, Kashiwagi K, Asakawa T, Kakinuma Y, Michael AJ, Igarashi K (2001) Multiple polyamine transport systems on the vacuolar membrane in yeast. Biochem J 353:681–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Träff KL, Otero Cordero RR, van Zyl WH, Hahn-Hägerdal B (2001) Deletion of the GRE3 aldose reductase gene and its influence on xylose metabolism in recombinant strains of Saccharomyces cerevisiae expression the xylA and XKSI genes. Appl Environ Microbiol 67:5668–5674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villa GP, Bartroli R, Lopez R, Guerra M, Enrique M, Penas M, Rodriquez E, Redondo D, Jglesias I, Diaz M (1992) Microbial transformation of furfural to furfuryl alcohol by Saccharomyces cerevisiae. Acta Biotechnol 12:509–512

    Article  CAS  Google Scholar 

  • Wahlbom CF, Hahn-Hägerdal B (2002) Furfural, 5-hydroxymethylfurfrual, and acetone act as external electron acceptors during anaerobic fermentation of xylose in recombinant Saccharomyces cerevisiae. Biotechnol Bioeng 78:172–178

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Xu H, Ju D, Xie Y (2008) Disruption of Rpn4-induced proteasome expression in Saccharomyces cerevisiae reduces cell viability under stressed conditions. Genetics 180:1945–1953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Xu H, Ha SW, Ju D, Xie Y (2010) Proteasomal degradation of Rpn4 in Saccharomyces cerevisiae is critical for cell viability under stressed conditions. Genetics 184:335–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfger H, Mahé Y, Parle-McDermott A, Delahodde A, Kuchler K (1997) The yeast ATP binding cassette (ABC) proteins PDR10 and PDR15 are novel targets for the Pdr1 and Pdr3 transcriptional regulators. FEBS Lett 418:269–274

    Article  CAS  PubMed  Google Scholar 

  • Workman CT, Mak HC, McCuine S, Tagne JB, Agarwal M, Ozier O, Begley TJ, Samson LD, Ideker T (2006) A systems approach to mapping DNA damage response pathways. Science 312:1054–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Y, Varshavsky A (2001) RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc Natl Acad Sci USA 98:3056–3061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Xiao W (2004) Pdr3 is required for DNA damage induction of MAG1 and DDI1 via a bi-directional promoter element. Nucl Acids Res 32:5066–5075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the National Research Initiative of the USDA National Institute of Food and Agriculture grant number 2006-35504-17359. The author is grateful to Michael A. Cotta for critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Z. Lewis Liu.

Additional information

The mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal-opportunity provider and employer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Z.L. Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl Microbiol Biotechnol 90, 809–825 (2011). https://doi.org/10.1007/s00253-011-3167-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3167-9

Keywords

Navigation