Analysis of a conserved cellulase transcriptional regulator reveals inducer-independent production of cellulolytic enzymes in Neurospora crassa

MicrobiologyOpen

Volumn 2, Issue 4, 2013, Pages 595-609

  Coradetti, Samuel T ^a   Xiong, Yi ^a   Glass, N Louise ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aspergillus; Biofuels; Cellulase; Neurospora; Transcriptional regulation

Indexed keywords

CARBON; CELLULASE; MICROCRYSTALLINE CELLULOSE; RNA;

ARTICLE; ASPERGILLUS NIDULANS; BIOMASS; CLR 2 GENE; CLRB GENE; COMPARATIVE STUDY; CONTROLLED STUDY; ECOLOGICAL NICHE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DEGRADATION; ENZYME RELEASE; ENZYME SYNTHESIS; FUNGAL GENE; FUNGUS MUTANT; GENE ACTIVITY; GENE CLUSTER; GENE CONTROL; GENE FUNCTION; GENETIC CONSERVATION; GENETIC MANIPULATION; NEUROSPORA CRASSA; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; REGULON; RNA SEQUENCE; STARVATION; TRANSCRIPTION REGULATION; WILD TYPE;

ASPERGILLUS; BIOFUELS; CELLULASE; NEUROSPORA; TRANSCRIPTIONAL REGULATION;

ASPERGILLUS NIDULANS; CELLULASE; CELLULOSE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; NEUROSPORA CRASSA; TRANSCRIPTION FACTORS;

ASPERGILLUS; EMERICELLA NIDULANS; FUNGI; NEUROSPORA; NEUROSPORA CRASSA;

EID: 84893450996     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.94     Document Type: Article

References (71)

1. Anders, S., and W. Huber . 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106
2. Andersen, M. R., W. Vongsangnak, G. Panagiotou, M. P. Salazar, L. Lehmann, and J. Nielsen . 2008. A trispecies Aspergillus microarray: comparative transcriptomics of three Aspergillus species. Proc. Natl. Acad. Sci. USA 105:4387-4392.
3. Aro, N., A. Saloheimo, M. IImen, and M. Penttila . 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., M. IImen, A. Saloheimo, and M. Penttila . 2003. ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl. Environ. Microbiol. 69:56-65.
5. Aro, N., T. Pakula, and M. Penttila . 2005. Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol. Rev. 29:719-739.
6. Beeson, W. T., A. T. Iavarone, C. D. Hausmann, J. H. Cate, and M. A. Marletta . 2011. Extracellular aldonolactonase from Myceliophthora thermophila. Appl. Environ. Microbiol. 77:650-656.
7. Beeson, W. T., C. M. Phillips, J. H. D. Cate, and M. A. Marletta . 2012. Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J. Am. Chem. Soc. 134:890-892.
8. Berka, R. M., I. V. Grigoriev, R. Otillar, A. Salamov, J. Grimwood, I. Reid, et al. 2011. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat. Biotechnol. 29:922-927.
9. Bey, M., S. M. Zhou, L. Poidevin, B. Henrissat, P. M. Coutinho, J. G. Berrin, et al. 2013. Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl. Environ. Microbiol. 79:488-496.
10. Brunner, K., A. M. Lichtenauer, K. Kratochwill, M. Delic, and R. L. Mach . 2007. Xyr1 regulates xylanase but not cellulase formation in the head blight fungus Fusarium graminearum. Curr. Genet. 52:213-220.
11. Calero-Nieto, F., A. Di Pietro, M. I. G. Roncero, and C. Hera . 2007. Role of the transcriptional activator XInR of Fusarium oxysporum in regulation of xylanase genes and virulence. Mol. Plant Microbe Interact. 20:977-985.
12. Cantarel, B. L., P. M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat . 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37:D233-D238.
13. Colot, H. V., G. Park, G. E. Turner, C. Ringelberg, C. M. Crew, L. Litvinkova, et al. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 103:10352-10357.
14. Coradetti, S. T., J. P. Craig, Y. Xiong, T. Shock, C. G. Tian, and N. L. Glass . 2012. Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc. Natl. Acad. Sci. USA 109:7397-7402.
15. Delmas, S., S. T. Pullan, S. Gaddipati, M. Kokolski, S. Malla, M. J. Blythe, et al. 2012. Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet. 8:e1002875.
16. Du, J., S. Li, and H. Zhao . 2010. Discovery and characterization of novel d-xylose-specific transporters from Neurospora crassa and Pichia stipitis. Mol. BioSyst. 6:2150-2156.
17. Elvin, M., J. J. Loros, J. C. Dunlap, and C. Heintzen . 2005. The PAS/LOV protein VIVID supports a rapidly dampened daytime oscillator that facilitates entrainment of the Neurospora circadian clock. Genes Dev. 19:2593-2605.
18. Espagne, E., O. Lespinet, F. Malagnac, C. Da Silva, O. Jaillon, B. M. Porcel, et al. 2008. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 9:R77.
19. Floudas, D., M. Binder, R. Riley, K. Barry, R. A. Blanchette, B.Henrissat, et al. 2012. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715-1719.
20. Frey, S. D., J. Six, and E. T. Elliott . 2003. Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil-litter interface. Soil Biol. Biochem. 35:1001-1004.
21. Galagan, J. E., S. E. Calvo, K. A. Borkovich, E. U. Selker, N. D. Read, D. Jaffe, et al. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868.
22. Galagan, J. E., S. E. Calvo, C. Cuomo, L. J. Ma, J. R. Wortman, S. Batzoglou, et al. 2005. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105-1115.
23. Galazka, J. M., C. G. Tian, W. T. Beeson, B. Martinez, N. L. Glass, and J. H. D. Cate . 2010. Cellodextrin transport in yeast for improved biofuel production. Science 330:84-86.
24. Gielkens, M. M., E. Dekkers, J. Visser, and L. H. de Graaff . 1999. Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl. Environ. Microbiol. 65:4340-4345.
25. Gusakov, A. V. 2011. Alternatives to Trichoderma reesei in biofuel production. Trends Biotechnol. 29:419-425.
26. Hakkinen, M., M. Arvas, M. Oja, N. Aro, M. Penttila, M. Saloheimo, et al. 2012. Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb. Cell Fact. 11:134.
27. Heimann, M., and M. Reichstein . 2008. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289-292.
28. Hieber, M., and M. O. Gessner . 2002. Contribution of stream detrivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026-1038.
29. de Hoon, M. J., S. Imoto, J. Nolan, and S. Miyano . 2004. Open source clustering software. Bioinformatics 20:1453-1454.
30. Klich, M. A. 2002. Biogeography of Aspergillus species in soil and litter. Mycologia 94:21-27.
31. Kominkova, D., K. A. Kuehn, N. Busing, D. Steiner, and M. O. Gessner . 2000. Microbial biomass, growth, and respiration associated with submerged litter of Phragmites australis decomposing in a littoral reed stand of a large lake. Aquat. Microb. Ecol. 22:271-282.
32. Konno, N., K. Igarashi, N. Habu, M. Samejima, and A. Isogai . 2009. Cloning of the Trichoderma reesei cDNA encoding a glucuronan lyase belonging to a novel polysaccharide lyase family. Appl. Environ. Microbiol. 75:101-107.
33. Kunitake, E., S. Tani, J. I. Sumitani, and T. Kawaguchi . 2012. A novel transcriptional regulator, ClbR, controls the cellobiose- and cellulose-responsive induction of cellulase and xylanase genes regulated by two distinct signaling pathways in Aspergillus aculeatus. Appl. Microbiol. Biotechnol. 97:2017-2028.
34. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg . 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.
35. Li, X., W. T. Beeson, C. M. Phillips, M. A. Marletta, and J. H. Cate . 2012. Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure 20:1051-1061.
36. Liu, G., L. Zhang, Y. Qin, G. Zou, Z. Li, X. Yan, et al. 2013. Long-term strain improvements accumulate mutations in regulatory elements responsible for hyper-production of cellulolytic enzymes. Sci. Rep. 3:1569.
37. Mach, L., and S. Zeilinger . 2003. Regulation of gene expression in industrial fungi: Trichoderma. Appl. Microbiol. Biotechnol. 60:515-522.
38. Mach-Aigner, A. R., M. E. Pucher, M. G. Steiger, G. E. Bauer, and R. L. Mach . 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.
39. Margeot, A., B. Hahn-Hagerdal, M. Edlund, R. Slade, and F. Monot . 2009. New improvements for lignocellulosic ethanol. Curr. Opin. Biotechnol. 20:372-380.
40. McCluskey, K. 2003. The fungal genetics stock center from molds to molecules. Adv. Appl. Microbiol. 52:245-262.
41. Nayak, T., E. Szewczyk, C. E. Oakley, A. Osmani, L. Ukil, S. L. Murray, et al. 2006. A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172:1557-1566.
42. Nitta, M., T. Furukawa, Y. Shida, K. Mori, S. Kuhara, Y. Morikawa, et al. 2012. A new Zn(II)(2)Cys(6)-type transcription factor BglR regulates beta-glucosidase expression in Trichoderma reesei. Fungal Genet. Biol. 49:388-397.
43. Noguchi, Y., M. Sano, K. Kanamaru, T. Ko, M. Takeuchi, M. Kato, et al. 2009. Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl. Microbiol. Biotechnol. 85:141-154.
44. Ogawa, M., T. Kobayashi, and Y. Koyama . 2012. ManR, a novel Zn(II)2Cys6 transcriptional activator, controls the beta-mannan utilization system in Aspergillus oryzae. Fungal Genet. Biol. 49:987-995.
45. Ogawa, M., T. Kobayashi, and Y. Koyama . 2013. ManR, a transcriptional regulator of the beta-mannan utilization system, controls the cellulose utilization system in Aspergillus oryzae. Biosci. Biotechnol. Biochem. 77:426-429.
46. van Peij, N. N. M. E., M. M. C. Gielkens, R. P. de Vries, J. Visser, and L. H. de Graaff . 1998. The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl. Environ. Microbiol. 64:3615-3619.
47. Perkins, D. D., and B. C. Turner . 1988. Neurospora from natural populations: toward the population biology of a haploid eukaryote. Exp. Mycol. 12:91-131.
48. Peterson, R., and H. Nevalainen . 2012. Trichoderma reesei RUT-C30-thirty years of strain improvement. Microbiology 158:58-68.
49. Phillips, C. M., W. T. Beeson, J. H. Cate, and M. A. Marletta . 2011a. Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem. Biol. 6:1399-1406.
50. Phillips, C. M., A. T. Iavarone, and M. A. Marletta . 2011b. Quantitative proteomic approach for cellulose degradation by Neurospora crassa. J. Proteome Res. 10:4177-4185.
51. Porciuncula, J., T. Furukawa, K. Mori, Y. Shida, H. Hirakawa, K. Tashiro, et al. 2013. Single nucleotide polymorphism analysis of a Trichoderma reesei hyper-cellulolytic mutant developed in Japan. Biosci. Biotechnol. Biochem. 77:534-543.
52. Portnoy, T., A. Margeot, R. Linke, L. Atanasova, E. Fekete, E. Sandor, et al. 2011. The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation. BMC Genomics 12:269.
53. Punt, P. J., M. A. Dingemanse, A. Kuyvenhoven, R. D. Soede, P. H. Pouwels, and C. A. van den Hondel . 1990. Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene 93:101-109.
54. Quinlan, R. J., M. D. Sweeney, L. Lo Leggio, H. Otten, J. C. Poulsen, K. S. Johansen, et al. 2011. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc. Natl. Acad. Sci. USA 108:15079-15084.
55. Roberts, A., C. Trapnell, J. Donaghey, J. L. Rinn, and L. Pachter . 2011. Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol. 12:R22.
56. Ruijter, G. J., and J. Visser . 1997. Carbon repression in Aspergilli. FEMS Microbiol. Lett. 151:103-114.
57. Sternberg, D., and G. R. Mandels . 1979. Induction of cellulolytic enzymes in Trichoderma reesei by sophorose. J. Bacteriol. 139:761-769.
58. Stricker, A. R., K. Grosstessner-Hain, E. Wurleitner, and R. L. Mach . 2006. Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot. Cell 5:2128-2137.
59. Stricker, A. R., M. G. Steiger, and R. L. Mach . 2007. Xyr1 receives the lactose induction signal and regulates lactose metabolism in Hypocrea jecorina. FEBS Lett. 581:3915-3920.
60. Sun, J. P., and N. L. Glass . 2011. Identification of the CRE-1 cellulolytic regulon in Neurospora crassa. PLoS ONE 6:e25654.
61. Sun, J. P., C. G. Tian, S. Diamond, and N. L. Glass . 2012. Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot. Cell 11:482-493.
62. Szewczyk, E., T. Nayak, C. E. Oakley, H. Edgerton, Y. Xiong, N. Taheri-Talesh, et al. 2006. Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 1:3111-3120.
63. Tian, C., W. T. Beeson, A. T. Iavarone, J. Sun, M. A. Marletta, J. H. Cate, et al. 2009. Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc. Natl. Acad. Sci. USA 106:22157-22162.
64. Updegraff, D. M. 1969. Semimicro determination of cellulose in biological materials. Anal. Biochem. 32:420-424.
65. Vishniac, W., and M. Santer . 1957. The thiobacilli. Bacteriol. Rev. 21:195-213.
66. Visser, H., V. Vivi, P.J. Punt, A.V. Gusakov, P.T. Olson, R. Joosten, et al. 2011. Development of a mature fungal technology and production platform for industrial enzymes based on a Myceliophthora thermophila isolate, previously known as Chrysosporium lucknowense C1. Ind. Biotechnol. 7:214-223.
67. Vogel, H. 1956. A convenient growth medium for Neurospora (medium N). Microb. Genet. Bull. 13:2-43.
68. Waring, R. B., G. S. May, and N. R. Morris . 1989. Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulin-coding genes. Gene 79:119-130.
69. Yamakawa, Y., Y. Endo, N. Li, M. Yoshizawa, M. Aoyama, A. Watanabe, et al. 2013. Regulation of cellulolytic genes by McmA, the SRF-MADS box protein in Aspergillus nidulans. Biochem. Biophys. Res. Commun. 431:777-782.
70. Zhou, Q., J. Xu, Y. Kou, X. Lv, X. Zhang, G. Zhao, et al. 2012. Differential involvement of beta-glucosidases from Hypocrea jecorina in rapid induction of cellulase genes by cellulose and cellobiose. Eukaryot. Cell 11:1371-1381.
71. Znameroski, E. A., S. T. Coradetti, C. M. Roche, J. C. Tsai, A. T. Iavarone, J. H. D. Cate, et al. 2012. Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc. Natl. Acad. Sci. USA 109:6012-6017.