Metabolic engineering of inducer formation for cellulase and hemicellulase gene expression in Trichoderma reesei

Sub-Cellular Biochemistry

Volumn 64, Issue , 2012, Pages 367-390

  Seiboth, Bernhard ^a   Herold, Silvia ^a   Kubicek, Christian P ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Biore fineries; Cellulase production; Gene regulation; Lactose metabolism; Trichoderma

Indexed keywords

FUNGI; HYPOCREA JECORINA; TRICHODERMA;

CELLULASE; GLYCOSIDASE; HEMICELLULASE;

ENZYME INDUCTION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HYDROLYSIS; METABOLIC ENGINEERING; METABOLISM; METHODOLOGY; REGULATOR GENE; REVIEW; TRICHODERMA;

CELLULASE; ENZYME INDUCTION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GENES, REGULATOR; GLYCOSIDE HYDROLASES; HYDROLYSIS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; TRICHODERMA;

EID: 84874551191     PISSN: 03060225     EISSN: None     Source Type: Journal    
DOI: 10.1007/978-94-007-5055-5_18     Document Type: Article

References (91)

1. Akel E, Metz B, Seiboth B, Kubicek CP (2009) Molecular regulation of arabinan and L-arabinose metabolism in Hypocrea jecorina (Trichoderma reesei). Eukaryot Cell 8: 1837-1844.
2. Andreotti RE, Medeiros JE, Roche C, Mandels M (1980) Effects of strain and substrate on production of cellulases by Trichoderma reesei mutants. In: Ghose TK (ed) Bioconversion and bioengineering symposium. BERC, IIT, New Delhi, pp 353-371.
3. Aro N, Saloheimo A, Ilmen M, Penttilä M (2001) ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J Biol Chem 276: 24309-24314.
4. Aro N, Ilmen M, Saloheimo A, Penttilä M (2003) ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl Environ Microbiol 69: 56-65.
5. Aro N, Pakula T, Penttilä M (2005) Transcriptional regulation of plant cell wall degradation byfilamentous fungi. FEMS Microbiol Rev 29: 719-739.
6. Bhat PJ, Murthy TV (2001) Transcriptional control of the GAL/MEL regulon of yeast Saccharomyces cerevisiae: mechanism of galactose-mediated signal transduction. Mol Microbiol 40: 1059-1066.
7. Bouffard GG, Rudd KE, Adhya SL (1994) Dependence of lactose metabolism upon mutarotase encoded in the gal operon in Escherichia coli. J Mol Biol 244: 269-278.
8. Bouws H, Wattenberg A, Zorn H (2008) Fungal secretomes-nature's toolbox for white biotechnology. Appl Microbiol Biotechnol 80: 381-388.
9. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrateactive enZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37: D233-D238.
10. Carle-Urioste JC, Escobar-Vera J, El-Gogary S, Henrique-Silva F, Torigoi E, Crivellaro O, Herrera-Estrella A, El-Dorry H (1997) Cellulase induction in Trichoderma reesei by cellulose requires its own basal expression. J Biol Chem 272: 10169-10174.
11. Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60: 165-182.
12. Cherry JR, Fidantsef AL (2003) Directed evolution of industrial enzymes: an update. Curr Opin Biotechnol 14: 438-443.
13. Chilton IJ, Delaney CE, Barham-Morris J, Fincham DA, Hooley P, Whitehead MP (2008) The Aspergillus nidulans stress response transcription factor StzA is ascomycete-specific and shows species-specific polymorphisms in the C-terminal region. Mycol Res 112: 1435-1446.
14. Cziferszky A, Mach RL, Kubicek CP (2002) Phosphorylation positively regulates DNA binding of the carbon catabolite repressor Cre1 of Hypocrea jecorina (Trichoderma reesei). J Biol Chem 277: 14688-14694.
15. Denton JA, Kelly JM (2011) Disruption of Trichoderma reesei cre2, encoding an ubiquitin C-terminal hydrolase, results in increased cellulase activity. BMC Biotechnol 11: 103.
16. Divne C, Ståhlberg J, Reinikainen T, Ruohonen L, Pettersson G, Knowles JK, Teeri TT, Jones TA (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265: 524-528.
17. Durand H, Clanet H, Tiraby G (1988) Genetic improvement of Trichoderma reesei for large scale cellulase production. Enzyme Microbiol Technol 10: 341-346.
18. El-Gogary S, Leite A, Crivellaro O, Eveleigh DE, el-Dorry H (1989) Mechanism by which cellulose triggers cellobiohydrolase I gene expression in Trichoderma reesei. Proc Natl Acad Sci USA 86: 6138-6141.
19. Fekete E, Karaffa L, Sandor E, Banyai I, Seiboth B, Gyemant G, Sepsi A, Szentirmai A, Kubicek CP (2004) The alternative D-galactose degrading pathway of Aspergillus nidulans proceeds via L-sorbose. Arch Microbiol 181: 35-44.
20. Fekete E, Karaffa L, Kubicek CP, Szentirmai A, Seiboth B (2007) Induction of extracellular β-galactosidase (Bga1) formation by D-galactose in Hypocrea jecorina is mediated by galactitol. Microbiology 153: 507-512.
21. Fekete E, Seiboth B, Kubicek CP, Szentirmai A, Karaffa L (2008) Lack of aldose 1-epimerase in Hypocrea jecorina (anamorph Trichoderma reesei): a key to cellulase gene expression on lactose. Proc Natl Acad Sci USA 105: 7141-7146.
22. Fekete E, Karaffa L, Seiboth B, Fekete E, Kubicek CP, Flipphi M (2012) Identification of a permease gene involved in lactose utilisation in Aspergillus nidulans. Fungal Genet Biol 49(6): 415-425.
23. Flipphi M, van de Vondervoort PJ, Ruijter GJ, Visser J, Arst HN Jr, Felenbok B (2003) Onset of carbon catabolite repression in Aspergillus nidulans. Parallel involvement of hexokinase and glucokinase in sugar signaling. J Biol Chem 278: 11849-11857.
24. Foreman PK, Brown D, Dankmeyer L, Dean R, Diener S, Dunn-Coleman NS, Goedegebuur F, Houfek TD, England GJ, Kelley AS, Meerman HJ, Mitchell T, Mitchinson C, Olivares HA, Teunissen PJ, Yao J, Ward M (2003) Transcriptional regulation of biomass-degrading enzymes in thefilamentous fungus Trichoderma reesei. J Biol Chem 278: 31988-31997.
25. Fowler T, Brown RD Jr (1992) The bgl1 gene encoding extracellular β-glucosidase from Trichoderma reesei is required for rapid induction of the cellulase complex. Mol Microbiol 6: 3225-3235.
26. Frey PA (1996) The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. FASEB J 10: 461-470.
27. Fritscher C, Messner R, Kubicek CP (1990) Cellobiose metabolism and cellobiohydrolase I biosynthesis by Trichoderma reesei. Exp Mycol 14: 451-461.
28. Furukawa T, Shida Y, Kitagami N, Mori K, Kato M, Kobayashi T, Okada H, Ogasawara W, Morikawa Y (2009) Identification of specific binding sites for XYR1, a transcriptional activator of cellulolytic and xylanolytic genes in Trichoderma reesei. Fungal Genet Biol 46: 564-574.
29. Gremel G, Dorrer M, Schmoll M (2008) Sulphur metabolism and cellulase gene expression are connected processes in thefilamentous fungus Hypocrea jecorina (anamorph Trichoderma reesei). BMC Microbiol 8: 174.
30. Harman GE, Kubicek CP (1998) Trichoderma and Gliocladium, enzymes, biological control and commercial applications, vol 2. Taylor & Francis Ltd., London.
31. Hartl L, Kubicek CP, Seiboth B (2007) Induction of the gal pathway and cellulase genes involves no transcriptional inducer function of the galactokinase in Hypocrea jecorina. J Biol Chem 282: 18654-18659.
32. Holden HM, Rayment I, Thoden JB (2003) Structure and function of enzymes of the Leloir pathway for galactose metabolism. J Biol Chem 278: 43885-43888.
33. Ilmen M, Thrane C, Penttilä M (1996) The glucose repressor gene cre1 of Trichoderma: isolation and expression of a full-length and a truncated mutant form. Mol Gen Genet 251: 451-460.
34. Ilmen M, Saloheimo A, Onnela ML, Penttilä ME (1997) Regulation of cellulase gene expression in thefilamentous fungus Trichoderma reesei. Appl Environ Microbiol 63: 1298-1306.
35. Karaffa L, Fekete E, Gamauf C, Szentirmai A, Kubicek CP, Seiboth B (2006) D-Galactose induces cellulase gene expression in Hypocrea jecorina at low growth rates. Microbiology 152: 1507-1514.
36. Koivistoinen OM, Richard P, Penttila M, Ruohonen L, Mojzita D (2012) Sorbitol dehydrogenase of Aspergillus niger, SdhA, is part of the oxido-reductive D-galactose pathway and essential for D-sorbitol catabolism. FEBS Lett 586: 378-383.
37. Kubicek CP (1987) Involvement of a conidial endoglucanase and a plasma-membrane-bound betaglucosidase in the induction of endoglucanase synthesis by cellulose in Trichoderma reesei. J Gen Microbiol 133: 1481-1487.
38. Kubicek CP (2012) Systems biological approaches towards understanding cellulase production by Trichoderma reesei. J Biotechnol Jun 29. [Epub ahead of print].
39. Kubicek CP, Harman GE (eds) (1998) Trichoderma and gliocladium, vol 1 and 2. Taylor & Francis Ltd., London.
40. Kubicek CP, Mühlbauer G, Grotz M, John E, Kubicek-Pranz EM (1988) Properties of a conidial bound cellulase enzyme system from Trichoderma reesei. J Gen Microbiol 134: 1215-1222.
41. Kubicek CP, Messner R, Gruber F, Mandels M, Kubicek-Pranz EM (1993) Triggering of cellulase biosynthesis by cellulose in Trichoderma reesei. Involvement of a constitutive, sophoroseinducible, glucose-inhibited β-diglucoside permease. J Biol Chem 268: 19364-19368.
42. Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B (2009) Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2: 19.
43. Kumar R, Singh S, Singh OV (2008) Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J Ind Microbiol Biotechnol 35: 377-391.
44. Limon MC, Pakula T, Saloheimo M, Penttilä M (2011) The effects of disruption of phosphoglucose isomerase gene on carbon utilisation and cellulase production in Trichoderma reesei Rut-C30. Microbl Cell Fact 10: 40.
45. Mach-Aigner AR, Pucher ME, Steiger MG, Bauer GE, Preis SJ, Mach RL (2008) Transcriptional regulation of xyr1, encoding the main regulator of the xylanolytic and cellulolytic enzyme system in Hypocrea jecorina. Appl Environ Microbiol 74: 6554-6562.
46. Mach-Aigner AR, Grosstessner-Hain K, Pocas-Fonseca MJ, Mechtler K, Mach RL (2010) From an electrophoretic mobility shift assay to isolated transcription factors: a fast genomicproteomic approach. BMC Genomics 11: 644.
47. Mach-Aigner AR, Gudynaite-Savitch L, Mach RL (2011) L-Arabitol is the actual inducer of xylanase expression in Hypocrea jecorina (Trichoderma reesei). Appl Environ Microbiol 77: 5988-5994.
48. Mandels M, Parrish FW, Reese ET (1962) Sophorose as an inducer of cellulase in Trichoderma viride. J Bacteriol 83: 400-408.
49. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, de Leon AL, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A, Schoch CL, Yao J, Barabote R, Nelson MA, Detter C, Bruce D, Kuske CR, Xie G, Richardson P, Rokhsar DS, Lucas SM, Rubin EM, Dunn-Coleman N, Ward M, Brettin TS (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: 553-560.
50. Merino ST, Cherry J (2007) Progress and challenges in enzyme development for biomass utilization. Adv Biochem Eng Biotechnol 108: 95-120.
51. Messner R, Kubicek-Pranz EM, Gsur A, Kubicek CP (1991) Cellobiohydrolase II is the main conidial-bound cellulase in Trichoderma reesei and other Trichoderma strains. Arch Microbiol 155: 601-606.
52. Metz B, de Vries RP, Polak S, Seidl V, Seiboth B (2009) The Hypocrea jecorina (syn. Trichoderma reesei) lxr1 gene encodes a D-mannitol dehydrogenase and is not involved in L-arabinose catabolism. FEBS Lett 17: 1309-1313.
53. Metz B, Seidl-Seiboth V, Haarmann T, Kopchinskiy A, Lorenz P, Seiboth B, Kubicek CP (2011) Expression of biomass-degrading enzymes is a major event during conidium development in Trichoderma reesei. Eukaryot Cell 10: 1527-1535.
54. Mishra P, Singh A (1993) Microbial pentose utilization. Adv Appl Microbiol 39: 91-152.
55. Mojzita D, Penttilä M, Richard P (2010) Identification of an L-arabinose reductase gene in Aspergillus niger and its role in L-arabinose catabolism. J Biol Chem 285: 23622-23628.
56. Mojzita D, Koivistoinen OM, Maaheimo H, Penttila M, Ruohonen L, Richard P (2012) Identification of the galactitol dehydrogenase, LadB, that is part of the oxido-reductive D-galactose catabolic pathway in Aspergillus niger. Fungal Genet Biol 49: 152-159.
57. Nakari-Setälä T, Paloheimo M, Kallio J, Vehmaanperä J, Penttilä M, Saloheimo M (2009) Genetic modification of carbon catabolite repression in Trichoderma reesei for improved protein production. Appl Environ Microbiol 75: 4853-4860.
58. Noguchi Y, Tanaka H, Kanamaru K, Kato M, Kobayashi T (2011) Xylose triggers reversible phosphorylation of XlnR, the fungal transcriptional activator of xylanolytic and cellulolytic genes in Aspergillus oryzae. Biosci Biotechnol Biochem 75(5): 953-959.
59. Pail M, Peterbauer T, Seiboth B, Hametner C, Druzhinina I, Kubicek CP (2004) The metabolic role and evolution of L-arabinitol 4-dehydrogenase of Hypocrea jecorina. Eur J Biochem 271: 1864-1872.
60. Pakula TM, Salonen K, Uusitalo J, Penttilä M (2005) The effect of specific growth rate on protein synthesis and secretion in thefilamentous fungus Trichoderma reesei. Microbiology 151: 135-143.
61. Penttilä M, Limon C, Nevalainen H (2004) Molecular biology of Trichoderma and biotechnological applications. In: Arora DK (ed) Handbook of fungal biotechnology, vol 20, 2nd edn. Marcel Dekker, New York, pp 413-427.
62. Pettersson H, Pettersson G (2001) Kinetics of the coupled reaction catalysed by a fusion protein of β-galactosidase and galactose dehydrogenase. Biochim Biophys Acta 1549: 155-160.
63. Portnoy T, Margeot A, Seidl-Seiboth V, Le Crom S, Ben Chaabane F, Linke R, Seiboth B, Kubicek CP (2011) Differential regulation of the cellulase transcription factors XYR1, ACE2, and ACE1 in Trichoderma reesei strains producing high and low levels of cellulase. Eukaryot Cell 10: 262-271.
64. Reyes-Dominguez Y, Bok JW, Berger H, Shwab EK, Basheer A, Gallmetzer A, Scazzocchio C, Keller N, Strauss J (2010) Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Mol Microbiol 76: 1376-1386.
65. Richard P, Putkonen M, Väänänen R, Londesborough J, Penttilä M (2002) The missing link in the fungal L-arabinose catabolic pathway, identification of the L-xylulose reductase gene. Biochemistry. 41(20): 6432-6437.
66. Roberts CF (1970) Enzyme lesions in galactose non-utilizing mutants of Aspergillus nidulans. Biochim Biophys Acta 201: 267-283.
67. Rubio-Texeira M (2005) A comparative analysis of the GAL genetic switch between not-so-distant cousins: Saccharomyces cerevisiae versus Kluyveromyces lactis. FEMS Yeast Res 5: 1115-1128.
68. Saloheimo A, Aro N, Ilmen M, Penttilä M (2000) Isolation of the ace1 gene encoding a Cys(2)-His(2) transcription factor involved in regulation of activity of the cellulase promoter cbh1 of Trichoderma reesei. J Biol Chem 275: 5817-5825.
69. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263-289.
70. Schmoll M, Schuster A, Silva Rdo N, Kubicek CP (2009) The G-alpha protein GNA3 of Hypocrea jecorina (Anamorph Trichoderma reesei) regulates cellulase gene expression in the presence of light. Eukaryot Cell 8: 410-420.
71. Schuster A, Tisch D, Seidl-Seiboth V, Kubicek CP, Schmoll M (2012) Roles of protein kinase A and adenylate cyclase in light-modulated cellulase regulation in Trichoderma reesei. Appl Environ Microbiol 78: 2168-2178.
72. Seibel C, Gremel G, do Nascimento SR, Schuster A, Kubicek CP, Schmoll M (2009) Lightdependent roles of the G-protein alpha subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei). BMC Biol 7: 58.
73. Seiboth B, Hakola S, Mach RL, Suominen PL, Kubicek CP (1997) Role of four major cellulases in triggering of cellulase gene expression by cellulose in Trichoderma reesei. J Bacteriol 179: 5318-5320.
74. Seiboth B, Hofmann G, Kubicek CP (2002a) Lactose metabolism and cellulase production in Hypocrea jecorina: the gal7 gene, encoding galactose-1-phosphate uridylyltransferase, is essential for growth on galactose but not for cellulase induction. Mol Genet Genomics 267: 124-132.
75. Seiboth B, Karaffa L, Sandor E, Kubicek C (2002b) The Hypocrea jecorina gal10 (uridine 5'-diphosphate-glucose 4-epimerase-encoding) gene differs from yeast homologues in structure, genomic organization and expression. Gene 295: 143-149.
76. Seiboth B, Hartl L, Pail M, Kubicek CP (2003) D-xylose metabolism in Hypocrea jecorina: loss of the xylitol dehydrogenase step can be partially compensated for by lad1-encoded L-arabinitol-4-dehydrogenase. Eukaryot Cell 2: 867-875.
77. Seiboth B, Hartl L, Pail M, Fekete E, Karaffa L, Kubicek CP (2004) The galactokinase of Hypocrea jecorina is essential for cellulase induction by lactose but dispensable for growth on D-galactose. Mol Microbiol 51: 1015-1025.
78. Seiboth B, Hartl L, Salovuori N, Lanthaler K, Robson GD, Vehmaanperä J, Penttilä ME, Kubicek CP (2005) Role of the bga1-encoded extracellular b-galactosidase of Hypocrea jecorina in cellulase induction by lactose. Appl Environ Microbiol 71: 851-857.
79. Seiboth B, Gamauf C, Pail M, Hartl L, Kubicek CP (2007) The D-xylose reductase of Hypocrea jecorina is the major aldose reductase in pentose and D-galactose catabolism and necessary for beta-galactosidase and cellulase induction by lactose. Mol Microbiol 66: 890-900.
80. Seiboth B, Aghcheh RK, Phatale PA, Linke R, Hartl L, Sauer DG, Smith KM, Baker SE, Freitag M, Kubicek CP (2012) The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol 84(6): 1150-1164.
81. Seidl V, Gamauf C, Druzhinina IS, Seiboth B, Hartl L, Kubicek CP (2008) The Hypocrea jecorina (Trichoderma reesei) hypercellulolytic mutant RUT C30 lacks a 85 kb (29 gene-encoding) region of the wild-type genome. BMC Genomics 9: 327.
82. Sellick CA, Campbell RN, Reece RJ (2008) Galactose metabolism in yeast-structure and regulation of the Leloir pathway enzymes and the genes encoding them. Int Rev Cell Mol Biol 269: 111-150.
83. Sestak S, Farkas V (1993) Metabolic regulation of endoglucanase synthesis in Trichoderma reesei: participation of cyclic AMP and glucose-6-phosphate. Can J Microbiol 39: 342-347.
84. Sternberg D, Mandels GR (1979) Induction of cellulolytic enzymes in Trichoderma reesei by sophorose. J Bacteriol 139: 761-769.
85. Strauss J, Horvath HK, Abdallah BM, Kindermann J, Mach RL, Kubicek CP (1999) The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol Microbiol 32: 169-178.
86. Stricker AR, Grosstessner-Hain K, Würleitner E, Mach RL (2006) Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot Cell 5: 2128-2137.
87. Stricker AR, Mach RL, de Graaff LH (2008a) Regulation of transcription of cellulases-and hemicellulases-encoding genes in Aspergillus niger and Hypocrea jecorina (Trichoderma reesei). Appl Microbiol Biotechnol 78: 211-220.
88. Stricker AR, Trefflinger P, Aro N, Penttilä M, Mach RL (2008b) Role of Ace2 (Activator of Cellulases 2) within the xyn2 transcriptosome of Hypocrea jecorina. Fungal Genet Biol 45: 436-445.
89. Vaheri M, Leisola M, Kaupinnen V (1979) Transglycosylation products of the cellulase system of Trichoderma reesei. Biotechnol Lett 1: 41-46.
90. Wilson DB (2009) Cellulases and biofuels. Curr Opin Biotechnol 20: 295-299.
91. Zeilinger S, Ebner A, Marosits T, Mach R, Kubicek CP (2001) The Hypocrea jecorina HAP 2/3/5 protein complex binds to the inverted CCAAT-box (ATTGG) within the cbh2 (cellobiohydrolase II-gene) activating element. Mol Genet Genomics 266: 56-63.