Targets of light signalling in Trichoderma reesei

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Tisch, Doris ^a   Schmoll, Monika ^b  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^b AIT AUSTRIAN INSTITUTE OF TECHNOLOGY   (Austria)

Author keywords

BLR1; BLR2; D galactose; ENVOY; Glycoside hydrolases; Hypocrea jecorina; L arabinose; Light response; Trichoderma reesei

Indexed keywords

GALACTOSE; GLYCOSIDASE; HEMICELLULOSE; MANNITOL DEHYDROGENASE; PENTOSE; TRANSCRIPTOME; CELLULASE; FUNGAL PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GENE; CARBOHYDRATE METABOLISM; CARBON METABOLISM; CARBON SOURCE; CELL WALL; CONTROLLED STUDY; DARKNESS; FUNGAL STRAIN; GENE CLUSTER; GENE CONTROL; GENE NUMBER; GENETIC TRANSCRIPTION; HYPOCREA JECORINA; LIGHT; NEUROSPORA CRASSA; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT; PHOTORECEPTOR; PHOTOTRANSDUCTION; PLANT CELL; TRANSCRIPTION REGULATION; DNA MICROARRAY; ENZYME INDUCTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TRICHODERMA;

FUNGI; HYPOCREA JECORINA;

CARBOHYDRATE METABOLISM; CELLULASE; ENZYME INDUCTION; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GLYCOSIDE HYDROLASES; LIGHT; MULTIGENE FAMILY; NEUROSPORA CRASSA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TRICHODERMA;

EID: 84885037488     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-657     Document Type: Article

References (66)

1. Schmoll M, Seiboth B, Druzhinina I, Kubicek CP. Genomics analysis of biocontrol species and industrial enzyme producers from the genus Trichoderma. MYCOTA XIII, Fungal Genomics 2013, Berlin, Heidelberg: Springer, Nowrousian M, in press.
2. Schuster A, Schmoll M. Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 2010, 87(3):787-799. 10.1007/s00253-010-2632-1, 2886115, 20461510.
3. Wilson DB. Cellulases and biofuels. Curr Opin Biotechnol 2009, 20(3):295-299. 10.1016/j.copbio.2009.05.007, 19502046.
4. Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B. Metabolic engineering strategies for improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2009, 2(1):19. 10.1186/1754-6834-2-19, 2749017, 19723296.
5. Benitez T, Rincon AM, Limon MC, Codon AC. Biocontrol mechanisms of Trichoderma strains. Int Microbiol Offic J Spanish Soc Microbiol 2004, 7(4):249-260.
6. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 2008, 26(5):553-560. 10.1038/nbt1403, 18454138.
7. Hakkinen M, Arvas M, Oja M, Aro N, Penttila M, Saloheimo M, Pakula TM. Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microbial Cell Factories 2012, 11:134. 10.1186/1475-2859-11-134, 3526510, 23035824.
8. Tisch D, Schmoll M. Novel approaches to improve cellulase biosynthesis for biofuel production - Adjusting signal transduction pathways in the biotechnological workhorse Trichoderma reesei. Biofuel Production - Recent developments and prospects 2011, 199-224. Rijeka, Croatia: Intech, dos Santos Bernardes MA.
9. Schmoll M. Assessing the relevance of light for fungi implications and insights into the network of signal transmission. Adv Appl Microbiol 2011, 76:27-78.
10. Tisch D, Kubicek CP, Schmoll M. The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei. BMC Genom 2011, 12:613.
11. Brunner M, Kaldi K. Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol Microbiol 2008, 68(2):255-262. 10.1111/j.1365-2958.2008.06148.x, 18312266.
12. Chen CH, Dunlap JC, Loros JJ. Neurospora illuminates fungal photoreception. Fungal Genet Biol 2010, 47(11):922-929. 10.1016/j.fgb.2010.07.005, 3649881, 20637887.
13. Castellanos F, Schmoll M, Martinez P, Tisch D, Kubicek CP, Herrera-Estrella A, Esquivel-Naranjo EU. Crucial factors of the light perception machinery and their impact on growth and cellulase gene transcription in Trichoderma reesei. Fungal Genet Biol 2010, 47(5):468-476. 10.1016/j.fgb.2010.02.001, 20144726.
14. Gyalai-Korpos M, Nagy G, Mareczky Z, Schuster A, Reczey K, Schmoll M. Relevance of the light signaling machinery for cellulase expression in Trichoderma reesei (Hypocrea jecorina). BMC Res Notes 2010, 3:330. 10.1186/1756-0500-3-330, 3016267, 21138554.
15. Seibel C, Tisch D, Kubicek CP, Schmoll M. ENVOY is a major determinant in regulation of sexual development in Hypocrea jecorina (Trichoderma reesei). Eukaryot Cell 2012, 11(7):885-895. 10.1128/EC.05321-11, 3416498, 22581525.
16. Heintzen C, Loros JJ, Dunlap JC. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 2001, 104(3):453-464. 10.1016/S0092-8674(01)00232-X, 11239402.
17. Chen CH, DeMay BS, Gladfelter AS, Dunlap JC, Loros JJ. Physical interaction between VIVID and white collar complex regulates photoadaptation in Neurospora. Proc Natl Acad Sci USA 2010, 107(38):16715-16720. 10.1073/pnas.1011190107, 2944764, 20733070.
18. Chen CH, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ. Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J 2009, 28(8):1029-1042. 10.1038/emboj.2009.54, 2683703, 19262566.
19. Gin E, Diernfellner AC, Brunner M, Höfer T. The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation. Mol Syst Biol 2013, 9:667.
20. Hunt SM, Thompson S, Elvin M, Heintzen C. VIVID interacts with the WHITE COLLAR complex and FREQUENCY-interacting RNA helicase to alter light and clock responses in Neurospora. Proc Natl Acad Sci USA 2010, 107(38):16709-16714. 10.1073/pnas.1009474107, 2944716, 20807745.
21. Malzahn E, Ciprianidis S, Kaldi K, Schafmeier T, Brunner M. Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 2010, 142(5):762-772. 10.1016/j.cell.2010.08.010, 20813262.
22. Schmoll M, Franchi L, Kubicek CP. Envoy, a PAS/LOV domain protein of Hypocrea jecorina (anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot cell 2005, 4(12):1998-2007. 10.1128/EC.4.12.1998-2007.2005, 1317494, 16339718.
23. Schuster A, Kubicek CP, Friedl MA, Druzhinina IS, Schmoll M. Impact of light on Hypocrea jecorina and the multiple cellular roles of ENVOY in this process. BMC Genom 2007, 8(1):449.
24. Tisch D, Kubicek CP, Schmoll M. 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 2011, 48(6):631-640. 10.1016/j.fgb.2010.12.009, 3082050, 21220037.
25. Schmoll M, Tian C, Sun J, Tisch D, Glass NL. Unravelling the molecular basis for light modulated cellulase gene expression - the role of photoreceptors in Neurospora crassa. BMC Genom 2012, 13:127.
26. Schuster A, Kubicek CP, Schmoll M. Dehydrogenase GRD1 represents a novel component of the cellulase regulon in Trichoderma reesei (Hypocrea jecorina). Appl Environ Microbiol 2011, 77(13):4553-4563. 10.1128/AEM.00513-11, 3127732, 21602376.
27. Seiboth B, Metz B. Fungal arabinan and L-arabinose metabolism. Appl Microbiol Biotechnol 2011, 89(6):1665-1673. 10.1007/s00253-010-3071-8, 3044236, 21212945.
28. Seiboth B, Pakdaman SB, Hartl L, Kubicek CP. Lactose metabolism in filamentous fungi: how to deal with an unknown substrate. Fungal Biol Rev 2007, 21(1):42-48.
29. Holden HM, Rayment I, Thoden JB. Structure and function of enzymes of the Leloir pathway for galactose metabolism. J Biol Chem 2003, 278(45):43885-43888. 10.1074/jbc.R300025200, 12923184.
30. Mojzita D, Herold S, Metz B, Seiboth B, Richard P. L-xylo-3-hexulose reductase is the missing link in the oxidoreductive pathway for D-galactose catabolism in filamentous fungi. J Biol Chem 2012, 287(31):26010-26018. 10.1074/jbc.M112.372755, 3406684, 22654107.
31. Casas-Flores S, Rios-Momberg M, Bibbins M, Ponce-Noyola P, Herrera-Estrella A. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiology 2004, 150(Pt 11):3561-3569.
32. Rosales-Saavedra T, Esquivel-Naranjo EU, Casas-Flores S, Martinez-Hernandez P, Ibarra-Laclette E, Cortes-Penagos C, Herrera-Estrella A. Novel light-regulated genes in Trichoderma atroviride: a dissection by cDNA microarrays. Microbiology 2006, 152(Pt 11):3305-3317.
33. Sanchez-Arreguin A, Perez-Martinez AS, Herrera-Estrella A. Proteomic analysis of Trichoderma atroviride reveals independent roles for transcription factors BLR-1 and BLR-2 in light and darkness. Eukaryot Cell 2012, 11(1):30-41. 10.1128/EC.05263-11, 3255938, 22058143.
34. Gremel G, Dorrer M, Schmoll M. Sulphur metabolism and cellulase gene expression are connected processes in the filamentous fungus Hypocrea jecorina (anamorph Trichoderma reesei). BMC Microbiol 2008, 8(1):174. 10.1186/1471-2180-8-174, 2584116, 18842142.
35. Seibel C, Gremel G, Silva RD, Schuster A, Kubicek CP, Schmoll M. Light-dependent roles of the G-protein subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei). BMC Biol 2009, 7(1):58. 10.1186/1741-7007-7-58, 2749820, 19728862.
36. Baker SE, Perrone G, Richardson NM, Gallo A, Kubicek CP. Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma. Microbiology 2012, 158(Pt 1):147-154.
37. Zeilinger S, Ebner A, Marosits T, Mach R, Kubicek CP. 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 Genom: MGG 2001, 266(1):56-63.
38. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95(25):14863-14868. 10.1073/pnas.95.25.14863, 24541, 9843981.
39. Kasuga T, Townsend JP, Tian C, Gilbert LB, Mannhaupt G, Taylor JW, Glass NL. Long-oligomer microarray profiling in Neurospora crassa reveals the transcriptional program underlying biochemical and physiological events of conidial germination. Nucleic Acids Res 2005, 33(20):6469-6485. 10.1093/nar/gki953, 1283539, 16287898.
40. Kim SK, Lund J, Kiraly M, Duke K, Jiang M, Stuart JM, Eizinger A, Wylie BN, Davidson GS. A gene expression map for Caenorhabditis elegans. Sci (New York, NY 2001, 293(5537):2087-2092.
41. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssonen E, Bhatia A, Ward M, Penttila M. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem/FEBS 2002, 269(17):4202-4211.
42. Aro N, Pakula T, Penttila M. Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 2005, 29(4):719-739. 10.1016/j.femsre.2004.11.006, 16102600.
43. Foreman PK, Brown D, Dankmeyer L, Dean R, Diener S, Dunn-Coleman NS, Goedegebuur F, Houfek TD, England GJ, Kelley AS, et al. Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei. J Biol Chem 2003, 278(34):31988-31997. 10.1074/jbc.M304750200, 12788920.
44. Derntl C, Gudynaite-Savitch L, Calixte S, White T, Mach RL, Mach-Aigner AR. Mutation of the Xylanase regulator 1 causes a glucose blind hydrolase expressing phenotype in industrially used Trichoderma strains. Biotechnol Biofuels 2013, 6(1):62. 10.1186/1754-6834-6-62, 3654998, 23638967.
45. Stricker AR, Grosstessner-Hain K, Wurleitner E, Mach RL. Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-Xylose metabolism in Hypocrea jecorina. Eukaryot Cell 2006, 5(12):2128-2137. 10.1128/EC.00211-06, 1694815, 17056741.
46. Schuster A, Tisch D, Seidl-Seiboth V, Kubicek CP, Schmoll M. Roles of protein kinase A and adenylate cyclase in light-modulated cellulase regulation in Trichoderma reesei. Appl Environ Microbiol 2012, 78(7):2168-2178. 10.1128/AEM.06959-11, 3302631, 22286997.
47. Herold S, Bischof R, Metz B, Seiboth B, Kubicek CP. Xylanase gene transcription in Trichoderma reesei is triggered by different inducers representing different hemicellulosic pentose polymers. Eukaryot cell 2013, 12(3):390-398. 10.1128/EC.00182-12, 3629775, 23291620.
48. Schmoll M. Regulation of cellulase expression and signal transduction in the filamentous fungus Hypocrea jecorina (Trichoderma reesei) 2003, TU Vienna: Ph D Thesis.
49. Pail M, Peterbauer T, Seiboth B, Hametner C, Druzhinina I, Kubicek CP. The metabolic role and evolution of L-arabinitol 4-dehydrogenase of Hypocrea jecorina. Eur J Biochem/FEBS 2004, 271(10):1864-1872.
50. Seiboth B, Hartl L, Pail M, Kubicek CP. 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 2003, 2(5):867-875. 10.1128/EC.2.5.867-875.2003, 219359, 14555469.
51. vanKuyk PA, de Groot MJ, Ruijter GJ, de Vries RP, Visser J. The Aspergillus niger D-xylulose kinase gene is co-expressed with genes encoding arabinan degrading enzymes, and is essential for growth on D-xylose and L-arabinose. Europ J Biochem/FEBS 2001, 268(20):5414-5423.
52. Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, Tag AG, Sancar C, Bredeweg EL, Priest HD, McCormick RF, et al. Transcription factors in light and circadian clock signaling networks revealed by genome wide mapping of direct targets for Neurospora white collar complex. Eukaryot Cell 2010, 9(10):1549-1556. 10.1128/EC.00154-10, 2950426, 20675579.
53. Seiboth B, Gamauf C, Pail M, Hartl L, Kubicek CP. 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 2007, 66(4):890-900. 10.1111/j.1365-2958.2007.05953.x, 17924946.
54. Richard P, Putkonen M, Vaananen R, Londesborough J, Penttila M. The missing link in the fungal L-arabinose catabolic pathway, identification of the L-xylulose reductase gene. Biochemistry 2002, 41(20):6432-6437. 10.1021/bi025529i, 12009906.
55. Metz B, de Vries RP, Polak S, Seidl V, Seiboth B. The Hypocrea jecorina (syn. Trichoderma reesei) lxr1 gene encodes a D-mannitol dehydrogenase and is not involved in L-arabinose catabolism. FEBS Lett 2009, 583(8):1309-1313. 10.1016/j.febslet.2009.03.027, 19303876.
56. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 2006, 103(27):10352-10357. 10.1073/pnas.0601456103, 1482798, 16801547.
57. Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, Cate JH, Glass NL. Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci USA 2009, 106(52):22157-22162. 10.1073/pnas.0906810106, 2794032, 20018766.
58. Olmedo M, Ruger-Herreros C, Luque EM, Corrochano LM. Regulation of transcription by light in Neurospora crassa: A model for fungal photobiology?. Fungal Biol Rev 2013, 27:10-18.
59. Sahar S, Sassone-Corsi P. The epigenetic language of circadian clocks. Handbook Exp Pharmacol 2013, 217:29-44.
60. Coradetti ST, Craig JP, Xiong Y, Shock T, Tian C, Glass NL. Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc Natl Acad Sci USA 2012, 109(19):7397-7402. 10.1073/pnas.1200785109, 3358856, 22532664.
61. Seidl V, Gamauf C, Druzhinina IS, Seiboth B, Hartl L, Kubicek CP. The Hypocrea jecorina (Trichoderma reesei) hypercellulolytic mutant RUT C30 lacks a 85 kb (29 gene-encoding) region of the wild-type genome. BMC Genom 2008, 9:327.
62. Mandels M, Andreotti R. Problems and challenges in the cellulose to cellulase fermentation. Proc Biochem 1978, 13:6-13.
63. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):e36. 10.1093/nar/30.9.e36, 113859, 11972351.
64. Seo J, Gordish-Dressman H, Hoffman EP. An interactive power analysis tool for microarray hypothesis testing and generation. Bioinformatics 2006, 22(7):808-814. 10.1093/bioinformatics/btk052, 16418236.
65. Coppe A, Danieli GA, Bortoluzzi S. REEF: searching REgionally Enriched Features in genomes. BMC Bioinformatics 2006, 7:453. 10.1186/1471-2105-7-453, 1624853, 17042935.
66. Metz B, Seidl-Seiboth V, Haarmann T, Kopchinskiy A, Lorenz P, Seiboth B, Kubicek CP. Expression of biomass-degrading enzymes is a major event during conidium development in Trichoderma reesei. Eukaryot Cell 2011, 10(11):1527-1535. 10.1128/EC.05014-11, 3209057, 21890820.