Advertisement

Regulation of transcription of cellulases- and hemicellulases-encoding genes in Aspergillus niger and Hypocrea jecorina (Trichoderma reesei)

  • Astrid R. Stricker
  • Robert L. Mach
  • Leo H. de Graaff
Mini-Review

Abstract

The filamentous fungi Aspergillus niger and Hypocrea jecorina (Trichoderma reesei) have been the subject of many studies investigating the mechanism of transcriptional regulation of hemicellulase- and cellulase-encoding genes. The transcriptional regulator XlnR that was initially identified in A. niger as the transcriptional regulator of xylanase-encoding genes controls the transcription of about 20–30 genes encoding hemicellulases and cellulases. The orthologous xyr1 (xylanase regulator 1-encoding) gene product of H. jecorina has a similar function as XlnR, although at points, the mechanisms seems to be different. Specifically in H. jecorina, the interaction of Xyr1 and the co-regulators Ace1 and Ace2 in the regulation of transcription of xylanases and cellulases has been studied. This paper describes the similarities and differences in the transcriptional regulation of expression of hemicellulases and cellulases in A. niger and H. jecorina.

Keywords

Transcriptional regulation Gene expression Xylanase Cellulase 

Notes

Open Access

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

References

  1. Aro N, Saloheimo A, Ilmén M, Penttilä M (2001) ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J Biol Chem 276:24309–24314CrossRefGoogle Scholar
  2. Aro N, Ilmén M, Saloheimo A, Penttilä M (2003) ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl Environ Microbiol 69:56–65CrossRefGoogle Scholar
  3. Bisaria VS, Mishra S (1989) Regulatory aspects of cellulase biosynthesis and secretion. Crit Rev Biotechnol 9:61–103CrossRefGoogle Scholar
  4. Bourne Y, Hasper AA, Chahinian H, Juin M, De Graaff LH, Marchot P (2004) Aspergillus niger protein EstA defines a new class of fungal esterases within the alpha/beta hydrolase fold superfamily of proteins. Structure 12:677–687CrossRefGoogle Scholar
  5. Brakhage AA, Andrianopoulos A, Kato M, Steidl S, Davis MA, Tsukagoshi N, Hynes MJ (1999) HAP-Like CCAAT-binding complexes in filamentous fungi: implications for biotechnology. Fungal Genet Biol 27:243–252CrossRefGoogle Scholar
  6. Buchert J, Oksanen T, Pere J, Siika-aho M, Suurnäkki A, Viikari L (1998) Applications of Trichoderma reesei enzymes in the pulp and paper industry. In: Harman GE, Kubicek CP (eds) Trichoderma and gliocladium. vol. 2. Taylor & Francis, London, UK, pp 343–357Google Scholar
  7. Bussink H, van den Hombergh J, van den Ijssel P, Visser J (1992) Characterization of polygalacturonase-overproducing Aspergillus niger transformants. Appl Microbiol Biotechnol 37:324–329CrossRefGoogle Scholar
  8. de Graaff LH, Visser J, van den Broeck HC, Strozyk F, Kormelink FJM, Boonman JC (1992) Cloning, expression and use of acetyl xylan esterases from fungal origin. Eur. Patent Application no. 0507369-A/7Google Scholar
  9. de Graaff LH, van den Broeck HC, van Ooijen AJ, Visser J (1994) Regulation of the xylanase-encoding xlnA gene of Aspergillus tubigensis. Mol Microbiol 12:479–490CrossRefGoogle Scholar
  10. de Vries RP, Visser J (1999) Regulation of the feruloyl esterase (faeA) gene from Aspergillus niger. Appl Environ Microbiol 65:5500–5503Google Scholar
  11. de Vries RP, van den Broeck HC, Dekkers E, Manzanares P, de Graaff LH, Visser J (1999a) Differential expression of three alpha-galactosidase genes and a single beta-galactosidase gene from Aspergillus niger. Appl Environ Microbiol 65:2453–2460Google Scholar
  12. de Vries RP, Visser J, de Graaff LH (1999b) CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation. Res Microbiol 150:281–285CrossRefGoogle Scholar
  13. de Vries RP, van de Vondervoort PJ, Hendriks L, van de Belt M, Visser J (2002) Regulation of the alpha-glucuronidase-encoding gene (aguA) from Aspergillus niger. Mol Genet Genomics 268:96–102CrossRefGoogle Scholar
  14. Delgado L, Trejo B, Huitron C, Aguilar G (1992) Pectin lyase from Aspergillus sp. CH-Y-1043. Appl Microbiol Biotechnol 39:515–519CrossRefGoogle Scholar
  15. Fägerstam L, Pettersson G (1980) The b-1,4-glucan cellobiohydrolases of Trichoderma reesei QM9414: a new type of synergism. FEBS Lett 119:97–101CrossRefGoogle Scholar
  16. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251CrossRefGoogle Scholar
  17. Fowler T, Brown RD Jr (1992) The bgl1 gene encoding extracellular beta-glucosidase from Trichoderma reesei is required for rapid induction of the cellulase complex. Mol Microbiol 6:3225–3235CrossRefGoogle Scholar
  18. Galante YM, Monteverdi R, Inama S, Caldini C, De Conti A, Lavelli V, Bonomi F (1993) New applications of enzymes in wine making and olive oil production. Italian Biochem Soc Trans 4:34Google Scholar
  19. Gielkens M (1999) A molecular analysis of (hemi)-cellulose degradation by Aspergilli. Ph.D. thesis, Wageningen University, Wageningen, The NetherlandsGoogle Scholar
  20. Gielkens MM, Visser J, de Graaff LH (1997) Arabinoxylan degradation by fungi: characterization of the arabinoxylan-arabinofuranohydrolase encoding genes from Aspergillus niger and Aspergillus tubingensis. Curr Genet 31:22–29CrossRefGoogle Scholar
  21. Gielkens MM, Dekkers E, Visser J, de Graaff LH (1999) Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl Environ Microbiol 65:4340–4345Google Scholar
  22. Grassin C, Fauquembergue P (1996) Applicationsof pectinases in berverages. In: Visser J, Voragen A (eds) Pectin and pectinases. vol. 14. Elsevier, Amsterdam, The Netherlands, pp 453–462CrossRefGoogle Scholar
  23. Hahn-Hägerdal B, Galbe M, Gorwa-Grauslund MF, Liden G, Zacchi G (2006) Bio-ethanol—the fuel of tomorrow from the residues of today. Trends Biotechnol 24:549–556CrossRefGoogle Scholar
  24. Hasper AA (2003) Function and mode of regulation of the transcriptional activator XlnR from Aspergillus. Ph.D. thesis, Wageningen University, Wageningen, The NetherlandsGoogle Scholar
  25. Hasper AA, Visser J, de Graaff LH (2000) The Aspergillus niger transcriptional activator XlnR, which is involved in the degradation of the polysaccharides xylan and cellulose, also regulates D-xylose reductase gene expression. Mol Microbiol 36:193–200CrossRefGoogle Scholar
  26. Hasper AA, Dekkers E, van Mil M, van de Vondervoort PJ, de Graaff LH (2002) EglC, a new endoglucanase from Aspergillus niger with major activity towards xyloglucan. Appl Environ Microbiol 68:1556–1560CrossRefGoogle Scholar
  27. Hasper AA, Trindade LM, van der Veen D, van Ooyen AJ, de Graaff LH (2004) Functional analysis of the transcriptional activator XlnR from Aspergillus niger. Microbiology 150:1367–1375CrossRefGoogle Scholar
  28. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807CrossRefGoogle Scholar
  29. Hrmova M, Biely P, Vrsanska M (1986) Specificity of cellulase and β-xylanase induction in Trichoderma reesei QM 9414. Arch Microbiol 144:307–311CrossRefGoogle Scholar
  30. Ilmén 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 251:451–460Google Scholar
  31. Ilmén M, Saloheimo A, Onnela ML, Penttilä ME (1997) Regulation of cellulase gene expression in the filamentous fungus Trichoderma reesei. Appl Environ Microbiol 63:1298–306Google Scholar
  32. Irwin D, Spezio M, Walker L, Wilson D (1993) Activity studies of eight purified cellulases: specificity, synergism and binding domain effects. Biotechnol Bioeng 42:1002–1013CrossRefGoogle Scholar
  33. Kinoshita K, Takano M, Koseki T, Ito K, Iwano K (1995) Cloning of the xynNB gene encoding xylanase B from Aspergillus niger and its expression in Aspergillus kawachii. J Ferment Bioeng 79:422–428CrossRefGoogle Scholar
  34. Koo H, Ueda M, Wakida T, Yoshimura Y, Igarashi T (1994) Cellulase treatment of cotton fabrics. Textile Res J 64:70–74CrossRefGoogle Scholar
  35. Kubicek CP (1993) From cellulose to cellulase inducers: facts and fiction. In: Suominen P, Reinikainen T (eds) Proceedings of the 2nd Tricel Symposium on Trichoderma reesei Cellulases and Other Hydrolases, Espoo, Finland. Foundation for Biotechnical and Industrial Fermentation Research, Helsinki, pp 181–188Google Scholar
  36. Kubicek CP, Messner R, Gruber F, Mach RL, Kubicek-Pranz EM (1993) The Trichoderma cellulase regulatory puzzle: from the interior life of a secretory fungus. Enzyme Microb Technol 15:90–99CrossRefGoogle Scholar
  37. Mach RL, Strauss J, Zeilinger S, Schindler M, Kubicek CP (1996) Carbon catabolite repression of xylanase I (xyn1) gene expression in Trichoderma reesei. Mol Microbiol 21:1273–1281CrossRefGoogle Scholar
  38. MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70:583–604CrossRefGoogle Scholar
  39. Mandels M, Reese ET (1960) Induction of cellulase in fungi by cellobiose. J Bacteriol 79:816–826Google Scholar
  40. Mandels M, Parrish FW, Reese ET (1962) Sophorose as an inducer of cellulase in Trichoderma viride. J Bacteriol 83:400–408Google Scholar
  41. Margolles-Clark E, Ilmén M, Penttilä M (1997) Expression patterns of ten hemicellulase genes of the filamentous fungus Trichoderma reesei on various carbon sources. J Biotechnol 57:167–179CrossRefGoogle Scholar
  42. Marmorstein R, Harrison SC (1994) Crystal structure of a PPR1–DNA complex: DNA recognition by proteins containing a Zn2Cys6 binuclear cluster. Genes Dev 8:2504–2512CrossRefGoogle Scholar
  43. Marmorstein R, Carey M, Ptashne M, Harrison SC (1992) DNA recognition by GAL4: structure of a protein–DNA complex. Nature 356:408–414CrossRefGoogle Scholar
  44. Mathieu M, Felenbok B (1994) The Aspergillus nidulans CREA protein mediates glucose repression of the ethanol regulon at various levels through competition with the ALCR-specific transactivator. Embo J 13:4022–4027Google Scholar
  45. Narendja FM, Davis MA, Hynes MJ (1999) AnCF, the CCAAT binding complex of Aspergillus nidulans, is essential for the formation of a DNase I-hypersensitive site in the 5′ region of the amdS gene. Mol Cell Biol 19:6523–6531Google Scholar
  46. Nidetzky B, Steiner W, Hayn M, Claeyssens M (1994) Cellulose hydrolysis by the cellulases from Trichoderma reesei: a new model for synergistic interaction. Biochem J 298:705–710Google Scholar
  47. Noé P, Chevalier J, Mora F, Comtat J (1986) Action of enzymes in chemical pulp and fibers. PartII: enzymatic beating. J Wood Chem Technol 6:167–184CrossRefGoogle Scholar
  48. Parenicová L, Benen JA, Kester HC, Visser J (2000) pgaA and pgaB encode two constitutively expressed endopolygalacturonases of Aspergillus niger. Biochem J 345(Pt 3):637–644CrossRefGoogle Scholar
  49. Pedersen GP, Screws GA, Cereoni DA (1992) Biopolishing of cellulosic fabrics. Can Text J 109:31–35Google Scholar
  50. Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, van den Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, d, Enfert C, Geysens S, Goosen C, Groot GS, de Groot PW, Guillemette T, Henrissat B, Herweijer M, van den Hombergh JP, van den Hondel CA, van der Heijden RT, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, van Kuyk PA, Lauber J, Lu X, van der Maarel MJ, Meulenberg R, Menke H, Mortimer MA, Nielsen J, Oliver SG, Olsthoorn M, Pal K, van Peij NN, Ram AF, Rinas U, Roubos JA, Sagt CM, Schmoll M, Sun J, Ussery D, Varga J, Vervecken W, van de Vondervoort PJ, Wedler H, Wosten HA, Zeng AP, van Ooyen AJ, Visser J, Stam H (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25:221–231CrossRefGoogle Scholar
  51. Poutanen K-J (1997) Enzymes. An important tool in the improvement of the quality of cereal foods. Trends Food Sci Technol 8:300–306CrossRefGoogle Scholar
  52. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489CrossRefGoogle Scholar
  53. Rauscher R, Würleitner E, Wacenovsky C, Aro N, Stricker AR, Zeilinger S, Kubicek CP, Penttilä M, Mach RL (2006) Transcriptional regulation of xyn1, encoding xylanase I, in Hypocrea jecorina. Eukaryot Cell 5:447–456CrossRefGoogle Scholar
  54. Saloheimo A, Aro N, Ilmén 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 275:5817–5825CrossRefGoogle Scholar
  55. Saloheimo M, Kuja-Panula J, Ylosmaki E, Ward M, Penttilä M (2002) Enzymatic properties and intracellular localization of the novel Trichoderma reesei beta-glucosidase BGLII (cel1A). Appl Environ Microbiol 68:4546–53CrossRefGoogle Scholar
  56. Senior DJ, Mayers PR, Saddler JN (1989) Production and purification of xylanases. ACS Symp Ser 309:641–655CrossRefGoogle Scholar
  57. Sternberg D, Mandels GR (1979) Induction of cellulolytic enzymes in Trichoderma reesei by sophorose. J Bacteriol 139:761–769Google Scholar
  58. 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 5:2128–2137CrossRefGoogle Scholar
  59. Stricker AR, Steiger MG, Mach RL (2007a) Xyr1 receives the lactose induction signal and regulates lactose metabolism in Hypocrea jecorina. FEBS Lett 581:3915–3920CrossRefGoogle Scholar
  60. Stricker AR, Trefflinger P, Aro N, Penttilä M, Mach RL (2007b) Role of Ace2 (Activator of Cellulases 2) within the xyn2 transcriptosome of Hypocrea jecorina. Fungal Genet Biol (in press). DOI  10.1016/j.fgb.2007.08.005
  61. van Peij NN, Brinkmann J, Vrsanska M, Visser J, de Graaff LH (1997) beta-Xylosidase activity, encoded by xlnD, is essential for complete hydrolysis of xylan by Aspergillus niger but not for induction of the xylanolytic enzyme spectrum. Eur J Biochem 245:164–173CrossRefGoogle Scholar
  62. van Peij NN, Gielkens MM, de Vries RP, Visser J, de Graaff LH (1998a) The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl Environ Microbiol 64:3615–3619Google Scholar
  63. van Peij NN, Visser J, de Graaff LH (1998b) Isolation and analysis of xlnR, encoding a transcriptional activator co- ordinating xylanolytic expression in Aspergillus niger. Mol Microbiol 27:131–142CrossRefGoogle Scholar
  64. Viikari L, Kantelinen A, Sundquist J, Linko M (1994) Xylanases in bleaching-from an idea to the industry. FEMS Microbio Rev 13:335–350CrossRefGoogle Scholar
  65. Walsh GA, Power RF, Headon DR (1993) Enzymes in the animal-feed industry. Trends Biotechnol 11:424–430CrossRefGoogle Scholar
  66. Wang D, Hu Y, Zheng F, Zhou K, Kohlhaw GB (1997) Evidence that intramolecular interactions are involved in masking the activation domain of transcriptional activator Leu3p. J Biol Chem 272:19383–19392CrossRefGoogle Scholar
  67. Weidner G, Steidl S, Brakhage AA (2001) The Aspergillus nidulans homoaconitase gene lysF is negatively regulated by the multimeric CCAAT-binding complex AnCF and positively regulated by GATA sites. Arch Microbiol 175:122–132CrossRefGoogle Scholar
  68. Wood T, McCrae S (1979) Synergisms between enzymes involved in the solubilization of native cellulose. Adv Chem Ser 181:181–209Google Scholar
  69. Würleitner E, Pera L, Wacenovsky C, Cziferszky A, Zeilinger S, Kubicek CP, Mach RL (2003) Transcriptional regulation of xyn2 in Hypocrea jecorina. Eukaryot Cell 2:150–158CrossRefGoogle Scholar
  70. Zeilinger S, Mach RL (1998) Xylanolytic enzymes of Trichoderma reesei: properties and regulation of expression. Curr Topics Cer Chem 1:27–35Google Scholar
  71. Zeilinger S, Mach RL, Schindler M, Herzog P, Kubicek CP (1996) Different inducibility of expression of the two xylanase genes xyn1 and xyn2 in Trichoderma reesei. J Biol Chem 271:25624–25629CrossRefGoogle Scholar
  72. 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 266:56–63CrossRefGoogle Scholar
  73. Zeilinger S, Schmoll M, Pail M, Mach RL, Kubicek CP (2003) Nucleosome transactions on the Hypocrea jecorina (Trichoderma reesei) cellulase promoter cbh2 associated with cellulase induction. Mol Genet Genomics 270:46–55CrossRefGoogle Scholar

Copyright information

© The Author(s) 2007

Authors and Affiliations

  • Astrid R. Stricker
    • 1
  • Robert L. Mach
    • 1
  • Leo H. de Graaff
    • 2
  1. 1.Gene Technology, Gene Technology and Applied BiochemistryInstitute of Chemical EngineeringWienAustria
  2. 2.Fungal Genomics Group, Laboratory of MicrobiologyWageningen UniversityWageningenThe Netherlands

Personalised recommendations