Roles of protein kinase A and adenylate cyclase in light-modulated cellulase regulation in Trichoderma reesei

Applied and Environmental Microbiology

Volumn 78, Issue 7, 2012, Pages 2168-2178

  Schuster, André ^a   Tisch, Doris ^a   Seidl Seiboth, Verena ^a   Kubicek, Christian P ^a   Schmoll, Monika ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CATALYTIC SUBUNITS; CELLULASE GENES; COMPLEX FORMATIONS; CRUCIAL FUNCTIONS; CYCLIC AMP (CAMP); DAMPENING EFFECTS; HYPOCREA; MUTANT STRAIN; PROTEIN KINASE A; SEXUAL DEVELOPMENT; SIGNALING CASCADES; T. REESEI; TRANSCRIPT LEVEL; TRICHODERMA REESEI; VEGETATIVE GROWTH; WILD TYPES;

ENZYMES; GENE EXPRESSION; PROTEINS; SUGARS;

LIGHT MODULATION;

ADENYLATE CYCLASE; CELLULASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL PROTEIN; LACTOSE;

CATALYSIS; DEVELOPMENTAL BIOLOGY; ENZYME ACTIVITY; FUNGUS; GENE EXPRESSION; PROTEIN;

ARTICLE; CULTURE MEDIUM; DARKNESS; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MUTATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRICHODERMA;

ADENYLATE CYCLASE; CELLULASE; CULTURE MEDIA; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DARKNESS; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; LACTOSE; LIGHT; MUTATION; SIGNAL TRANSDUCTION; TRICHODERMA;

HYPOCREA JECORINA;

EID: 84861150708     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06959-11     Document Type: Article

References (76)

1. Alspaugh JA, et al. 2002. Adenylyl cyclase functions downstream of the Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot. Cell 1:75-84.
2. Aro N, Ilmen M, Saloheimo A, Penttila M. 2003. ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl. Environ. Microbiol. 69:56-65.
3. Aro N, Saloheimo A, Ilmen M, Penttila 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. Atoui A, et al. 2010. Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet. Biol. 47:962-972.
5. Baker DA, Kelly JM. 2004. Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol. Microbiol. 52:1229-1242.
6. Banno S, et al. 2005. A catalytic subunit of cyclic AMP-dependent protein kinase, PKAC-1, regulates asexual differentiation in Neurospora crassa. Genes Genet. Syst. 80:25-34.
7. Bölker M. 1998. Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet. Biol. 25:143-156.
8. Carlile MJ. 1965. The photobiology of fungi. Annu. Rev. Plant Physiol. 16:175-202.
9. Casas-Flores S, et al. 2006. Cross talk between a fungal blue-light perception system and the cyclic AMP signaling pathway. Eukaryot. Cell 5:499-506.
10. Castellanos F, et al. 2010. Crucial factors of the light perception machinery and their impact on growth and cellulase gene transcription in Trichoderma reesei. Fungal Genet. Biol. 47:468-476.
11. Choi W, Dean RA. 1997. The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973-1983.
12. D'Souza CA, Heitman J. 2001. Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol. Rev. 25:349-364.
13. Fillinger S, Chaveroche MK, Shimizu K, Keller N, d'Enfert C. 2002. cAMP and ras signalling independently control spore germination in the filamentous fungus Aspergillus nidulans. Mol. Microbiol. 44:1001-1016.
14. Friedl MA, Kubicek CP, Druzhinina IS. 2008. Carbon source dependence and photostimulation of conidiation in Hypocrea atroviridis. Appl. Environ. Microbiol. 74:245-250.
15. Friedl MA, Schmoll M, Kubicek CP, Druzhinina IS. 2008. Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress. Microbiology 154:1229-1241.
16. Froehlich A, Noh B, Vierstra R, Loros J, Dunlap J. 2005. Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot. Cell 4:2140-2152.
17. Griffioen G, Thevelein JM. 2002. Molecular mechanisms controlling the localisation of protein kinase A. Curr. Genet. 41:199-207.
18. Gruber F, Visser J, Kubicek CP, de Graaff LH. 1990. The development of a heterologous transformation system for the cellulolytic fungus Trichoderma reesei based on a pyrG-negative mutant strain. Curr. Genet. 18:71-76.
19. Hickey PC, Jacobson DJ, Read ND, Louise Glass N. 2002. Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet. Biol. 37:109-119.
20. Huang G, et al. 2007. Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop. Genes Dev. 21:3283-3295.
21. Ivey FD, Kays AM, Borkovich KA. 2002. Shared and independent roles for a Galpha(i) protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryot. Cell 1:634-642.
22. Kamerewerd J, Jansson M, Nowrousian M, Poggeler S, Kuck U. 2008. Three alpha-subunits of heterotrimericGproteins and an adenylyl cyclase have distinct roles in fruiting body development in the homothallic fungus Sordaria macrospora. Genetics 180:191-206.
23. Kolarova N, Haplová J, Greík M. 1992. Light-activated adenyl cyclase from Trichoderma viride. FEMS Microbiol. Lett. 93:275-278.
24. 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.
25. Larkin M, et al. 2007. ClustalWand Clustal X version 2.0. Bioinformatics 23:2947-2948.
26. Lee K, Dunlap JC, Loros JJ. 2003. Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 163: 103-114.
27. Lee N, D'Souza C, Kronstad J. 2003. Of smuts, blasts, mildews, and blights: cAMP signaling in phytopathogenic fungi. Annu. Rev. Phytopathol 41:399-427.
28. Lengeler KB, et al. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746-785.
29. Liebmann B, Gattung S, Jahn B, Brakhage AA. 2003. cAMP signaling in Aspergillus fumigatus is involved in the regulation of the virulence gene pksP and in defense against killing by macrophages. Mol. Genet. Genomics 269:420-435.
30. Mach RL, Schindler M, Kubicek CP. 1994. Transformation of Trichoderma reesei based on hygromycin B resistance using homologous expression signals. Curr. Genet. 25:567-570.
31. Mach-Aigner A, et al. 2008. Transcriptional regulation of xyr1, encoding the main regulator of the xylanolytic and cellulolytic enzyme system in Hypocrea jecorina. Appl. Environ. Microbiol. 74:6554.
32. Mandels M, Andreotti RE. 1978. Problems and challenges in the cellulose to cellulase fermentation. Proc. Biochem. 13:6-13.
33. Mandels M, Reese ET. 1960. Induction of cellulase in fungi by cellobiose. J. Bacteriol. 79:816-826.
34. Mandels M, Reese ET. 1957. Induction of cellulase in Trichoderma viride as influenced by carbon sources and metals. J. Bacteriol. 73:269-278.
35. Marchler-Bauer A, et al. 2009. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37:D205-D210.
36. Margolles-Clark E, Ihnen M, Penttilä M. 1997. Expression patterns of ten hemicellulase genes of the filamentous fungus Trichoderma reesei on various carbon sources. J. Biotechnol. 57:167-179.
37. Martinez D, et al. 2008. Genome sequencing and analysis of the biomassdegrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 26:553-560.
38. Mehra A, Baker CL, Loros JJ, Dunlap JC. 2009. Post-translational modifications in circadian rhythms. Trends Biochem. Sci. 34:483-490.
39. Mukherjee M, Mukherjee PK, Kale SP. 2007. cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153:1734-1742.
40. Nowrousian M, Duffield G, Loros J, Dunlap J. 2003. The frequency gene is required for temperature-dependent regulation of many clock-controlled genes in Neurospora crassa. Genetics 164:923-933.
41. Pall ML. 1981. Adenosine 3',5'-phosphate in fungi. Microbiol. Rev. 45: 462-480.
42. Park G, et al. 2011. Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Eukaryot. Cell 10:1553-1564.
43. Portnoy T, et al. 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.
44. Rauscher R, et al. 2006. Transcriptional regulation of xyn1, encoding xylanase I, in Hypocrea jecorina. Eukaryot. Cell 5:447-456.
45. Rocha CR, et al. 2001. Signaling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans. Mol. Biol. Cell 12:3631-3643.
46. Roelfsema WA, Kuster BFM, Heslinga MC, Pluim H, Verhage M. 2000. Lactose and derivatives. In Ullmann's encyclopedia of industrial chemistry. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
47. Saloheimo A, Aro N, Ilmen M, Penttila 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.
48. Sands WA, Palmer TM. 2008. Regulating gene transcription in response to cyclic AMP elevation. Cell Signal. 20:460-466.
49. Schmoll M. 2008. The information highways of a biotechnological workhorse-signal transduction in Hypocrea jecorina. BMC Genomics 9:430.
50. Schmoll M, Esquivel-Naranjo EU, Herrera-Estrella A. 2010. Trichoderma in the light of day-physiology and development. Fungal Genet. Biol. 47:909-916.
51. Schmoll M, Franchi L, Kubicek CP. 2005. Envoy, a PAS/LOV domain protein of Hypocrea jecorina (Anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot. Cell 4:1998-2007.
52. Schmoll M, Kubicek CP. 2003. Regulation of Trichoderma cellulase formation: lessons in molecular biology from an industrial fungus. A review. Acta Microbiol. Immunol. Hung. 50:125-145.
53. 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.
54. Schuster A, et al. 2012. A versatile toolkit for high throughput functional genomics with Trichoderma reesei. Biotechnol. Biofuels. 5:1.
55. Schuster A, Kubicek CP, Friedl MA, Druzhinina IS, Schmoll M. 2007. Impact of light on Hypocrea jecorina and the multiple cellular roles of ENVOY in this process. BMC Genomics 8:449.
56. Schuster A, Kubicek CP, Schmoll M. 2011. Dehydrogenase GRD1 represents a novel component of the cellulase regulon in Trichoderma reesei (Hypocrea jecorina). Appl. Environ. Microbiol. 77:4553-4563.
57. Schuster A, Schmoll M. 2009. Heterotrimeric G-protein signaling and light response: two signaling pathways coordinated for optimal adjustment to nature. Commun. Integr. Biol. 2:308-310.
58. Seibel C, Gremel G, Rdo Nascimento Silva Schuster A, Kubicek CP, Schmoll M. 2009. Light-dependent roles of the G-protein alpha subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei). BMC Biol. 7:58.
59. Seiboth B, Pakdaman BS, Hartl L, Kubicek CP. 2007. Lactose metabolism in filamentous fungi: how to deal with an unknown substrate. Fungal Biol. Rev. 21:42-48.
60. Seidl V, Seibel C, Kubicek CP, Schmoll M. 2009. Sexual development in the industrial workhorse Trichoderma reesei. Proc. Natl. Acad. Sci. U. S. A. 106:13909-13914.
61. 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.
62. Stricker AR, Grosstessner-Hain K, Wurleitner 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.
63. Stricker AR, Mach RL, de Graaff LH. 2008. Regulation of transcription of cellulases- and hemicellulases-encoding genes in Aspergillus niger and Hypocrea jecorina (Trichoderma reesei). Appl. Microbiol. Biotechnol. 78: 211-220.
64. Stricker AR, Steiger MG, Mach RL. 2007. Xyr1 receives the lactose induction signal and regulates lactose metabolism in Hypocrea jecorina. FEBS Lett. 581:3915-3920.
65. 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.
66. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
67. Taylor SS, et al. 2005. Dynamics of signaling by PKA. Biochim. Biophys. Acta 1754:25-37.
68. 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.
69. Tisch D, Kubicek CP, Schmoll M. 2011. New insights into the mechanism of light modulated signaling by heterotrimeric G-proteins: ENVOY acts on gna1 and gna3 and adjusts cAMP levels in Trichoderma reesei (Hypocrea jecorina). Fungal Genet. Biol. 48:631-640.
70. Tisch D, Kubicek CP, Schmoll M. 2011. The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei. BMC Genomics 12:613.
71. Tisch D, Schmoll M. 2011. Novel approaches to improve cellulase biosynthesis for biofuel production-adjusting signal transduction pathways in the biotechnological workhorse Trichoderma reesei, p 199-224. In dos Santos Bernardes MA (ed), Biofuel production-recent developments and prospects. Intech, Rijeka, Croatia.
72. Trinci APJ. 1984. Regulation of hyphal branching and hyphal orientation, p 23-52. In Jennings DH, Rayner AD (ed), The ecology and physiology of the fungal mycelium. Cambridge University Press, Cambridge, United Kingdom.
73. Wilkie T, Yokoyama S. 1994. Evolution of the G protein alpha subunit multigene family. Soc. Gen. Physiol. Ser. 49:249-270.
74. Yanisch-Perron C, Vieira J, Messing J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
75. Zeilinger S, Mach RL, Kubicek CP. 1998. Two adjacent protein binding motifs in the cbh2 (cellobiohydrolase II-encoding) promoter of the fungus Hypocrea jecorina (Trichoderma reesei) cooperate in the induction by cellulose. J. Biol. Chem. 273:34463-34471.
76. Zhao W, et al. 2006. Deletion of the regulatory subunit of protein kinase A inAspergillus fumigatus alters morphology, sensitivity to oxidative damage, and virulence. Infect. Immun. 74:4865-4874.