The influence of Aspergillus niger transcription factors AraR and XlnR in the gene expression during growth in d-xylose, l-arabinose and steam-exploded sugarcane bagasse

Fungal Genetics and Biology

Volumn 60, Issue , 2013, Pages 29-45

  De Souza, Wagner Rodrigo ^a   Maitan Alfenas, Gabriela Piccolo ^b,c   de Gouvêa, Paula Fagundes ^a   Brown, Neil Andrew ^a   Savoldi, Marcela ^a   Battaglia, Evy ^d   Goldman, Maria Helena S ^a   De Vries, Ronald P ^b,d   Goldman, Gustavo Henrique ^a,e  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^c FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^d UTRECHT UNIVERSITY   (Netherlands)

^e BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

Author keywords

AraR; Aspergillus niger; Biofuels; Plant polysaccharide degrading genes; Sugarcane bagasse saccharification; XlnR

Indexed keywords

ARABINOSE; BAGASSE; MONOSACCHARIDE; POLYSACCHARIDE; PROTEIN ARAR; PROTEIN XLNR; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; XYLOSE;

ARTICLE; ASPERGILLUS NIGER; BIOFUEL PRODUCTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEGRADATION; FUNGAL STRAIN; FUNGUS GROWTH; GENE EXPRESSION; GENETIC ENGINEERING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; SUGARCANE; WATER VAPOR;

ASPERGILLUS NIGER; FUNGI;

ARAR; ASPERGILLUS NIGER; BIOFUELS; PLANT POLYSACCHARIDE-DEGRADING GENES; SUGARCANE BAGASSE SACCHARIFICATION; XLNR;

ARABINOSE; ASPERGILLUS NIGER; BIOFUELS; BIOMASS; CELLULOSE; ETHANOL; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; POLYSACCHARIDES; SACCHARUM; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; XYLOSE;

EID: 84887613726     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.07.007     Document Type: Article

References (68)

1. Andersen M.R., Vongsangnak W., Panagiotou G., Salazar M.P., Lehmann L., Nielsen J. A trispecies Aspergillus microarray: comparative transcriptomics of three Aspergillus species. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:4387-4392.
2. Bahn Y.-S., Xue C., Idnurm A., Rutherford J.C., Heitman J., Cardenas M.E. Sensing the environment: lessons from fungi. Nat. Rev. Microbiol. 2007, 5:57-69.
3. Battaglia E., Visser L., Nijssen A., van Veluw G.J., Wosten H.A.B., de Vries R.P. Analysis of regulation of pentose utilization in Aspergillus niger reveals evolutionary adaptations in Eurotiales. Stud. Mycol. 2011, 69:31-38.
4. Battaglia E., Hansen S.F., Leendertse A., Madrid S., Mulder H., Nikolaev I., de Vries R.P. Regulation of pentose utilization by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger. Appl. Microbiol. Biotechnol. 2011, 91:387-397.
5. Billard P., Ménart J., Blaisonneau J., Bolotin-Fukuhara M., Fukuhara H., Wésolowski-Louvel M. Glucose uptake in Kluyveromyces lactis: role of the HGT1 gene in glucose transport. J. Bacteriol. 1996, 178:5860-5866.
6. Blum H., Beier H., Gross H.J. Improved silver staining of plant-proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8:93-99.
7. Brunner K., Lichtenauer A.M., Kratochwill K., Delic M., Mach R.L. Xyr1 regulates xylanase but not cellulase formation in the head blight fungus Fusarium graminearum. Curr. Genet. 2007, 52:213-220.
8. Calero-Nieto F., Di Pietro A., Roncero M.I., Hera C. Role of the trascriptional activator xlnR of Fusarium oxysporum in regulation of xylanase genes and virulence. Mol. Plant Microb. Interact. 2007, 20:977-985.
9. Cantarel B., Rancurel C., Bernard T., Lombard V., Coutinho P.M., Henrissat B. The Carbohydrate-Active EnZymes database: an expert resource for Glycogenomics. Nucleic Acids Res. 2009, 37:D233-D238.
10. Carpita N.C., Gibeaut D.M. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant Journal 1993, 3:1-30.
11. Cardona C.A., Quintero J.A., Paz I.C. Production of bioethanol from sugarcane bagasse: status and perspectives. Bioresour. Technol. 2010, 101:4754.
12. Chow T.H., Sollitti P., Marmur J. Structure of the multigene family of MAL loci in Saccharomices. Mol. Gen. Genet. 1989, 217:60-69.
13. CONAB (National Supply Company), 2011. The Sugarcane Production in Brazil Will Reach a New Record <> (accessed 12.01.11). http://www.conab.gov.br.
14. Coradetti S.T., Craig J.P., Xiong Y., Shock T., Tian C., Glass N.L. Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc. Natl. Acad. Sci. U.S.A. 2012, 8:7397-7402.
15. Coutinho P.M., Anderson M., Kolenova K., vanKuyk P.A., Benoit I., Gruben B.S., Trejo-Aguilar B., Visser H., van Solingen P., Pakula T., Seiboth B., Battaglia E., Aguilar-Osorio G., de Jong J.F., Ohm R.A., Aguilar M., Henrissat B., Nielsen J., Stålbrand H., de Vries R.P. Post-genomic insights into the plant polysaccharide degradation potential of Aspergillus nidulans and comparison to Aspergillus niger and Aspergillus oryzae. Fung. Genet. Biol. 2009, 46:S161-S169.
16. de Groot M.J., van de Vondervoort P.J., de Vries R.P., vanKuyk P.A., Ruijter G.J., Visser J. Isolation and characterization of two specific regulatory Aspergillus niger mutants shows antagonistic regulation of arabinan and xylan metabolism. Microbiology 2003, 149:1183-1191.
17. de Groot M.J., Prathumpai W., Visser J., Ruijter G.J. Metabolic control analysis of Aspergillus niger l-arabinose catabolism. Biotechnol. Prog. 2005, 21:1610-1616.
18. de Groot M.J., Van Den Dool C., Wosten H.A.B., Levisson M., vanKuyk P.A., Ruijter G.J.G., de Vries R.P. Regulation of pentose catabolic pathway genes of Aspergillus niger. Food Technol. Biotechnol. 2007, 45:134-138.
19. de Souza W.R., de Gouvea P.F., Savoldi M., Malavazi I., Bernardes L.A.D., Goldman M.H.S., et al. Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse. Biotechnol. Biofuels 2011, 18:4.
20. de Vries R.P., Visser J. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol. Mol. Biol. Rev. 2001, 65:497-522.
21. de Vries R.P., Visser J., de Graaff L.H. CreA modulates the XlnR induced expression on xylose of Aspergillus niger genes involved in xylan degradation. Res. Microbiol. 1999, 150:281-285.
22. de Vries R.P., van den Broeck H.C., Dekkers E., Manzanares P., de Graaff L.H., Visser J. Differential expression of three alpha-galactosidase genes and a single beta-galactosidase gene from Aspergillus niger. Appl. Environ. Microbiol. 1999, 65:2453-2460.
23. de Vries R.P., van de Vondervoort P.J., Hendriks L., van de Belt M., Visser J. Regulation of the alpha-glucuronidase-encoding gene (aguA) from Aspergillus niger. Mol. Genet. Genomics 2002, 268:96-102.
24. Delmas S., Pullan S.T., Gaddipati S., Kokolski M., Malla S., et al. Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PloS Genet 2012, 8(8):e1002875.
25. Fekete E., Karaffa L., Sándor E., Bánvai I., Seiboth B., Gvémánt G., Sepsi A., Szentirmai A., Kubicek C.P. The alternative d-galactose degrading pathway of Aspergillus nidulans proceeds via l-sorbose. Arch. Microbiol. 2004, 181:35-44.
26. Flipphi M.J.A., Visser J., van der Veen P., de Graaff L.H. Arabinase gene expression in Aspergillus niger: indications for coordinated regulation. Microbiology 1994, 140:2673-2682.
27. Frey P.A. The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. FASEB J. 1996, 10:461-470.
28. Furukawa T., Shida Y., Kitagami N., Ota Y., Adachi M., et al. Identification of the cis-acting elements involved in regulation of xylanase III gene expression in Trichoderma reseei PC-3-7. Fungal Genet. Biol. 2008, 45:1094-1102.
29. Furukawa T., Shida Y., Kitagami N., Mori K., kato M., et al. Identification of specific binding sites for XYR1, a transcriptional activator of cellulolytic and xylanolytic genes in Trichoderma reseei. Fungal Genet. Biol. 2009, 46:564-574.
30. Gielkens M.M., Dekkers E., Visser J., de Graaff L.H. Two cellobiohydrolase-encoding genes from Aspergillus niger require d-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl. Environ. Microbiol. 1996, 65:4340-4345.
31. Gielkens M.M., Dekkers E., Visser J., de Graaff L.H. Two cellobiohydrolase-encoding genes from Aspergillus niger require d-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl. Environ. Microbiol. 1999, 65:4340-4345.
32. Gilsenan J.M., Cooley J., Bowyer P. CADRE: the central aspergillus data REpository 2012. Nucleic Acids Res. 2012, 40:D660-D666.
33. Glanemann C., Loos A., Gorret N., Willis L.B., O'Brien X.M., Lessard P.A., Sinskey A.J. Disparity between changes in mRNA abundance and enzyme activity in Corynebacterium glutamicum: implications for DNA microarray analysis. Appl. Microbiol. Biotechnol. 2003, 61:61-68.
34. Greatrix B.W., van Vuuren H.J. Expression of the HXT13, HXT15 and HXT17 genes in Saccharomyces cerevisiae and stabilization of the HXT1 gene transcript by sugar-induced osmotic stress. Curr. Genet. 2006, 49:205-217.
35. Gruben B.S., Zhou M., de Vries R.P. GalX regulates the d-galactose oxido-reductive pathway in Aspergillus niger. FEBS Lett. 2012, 586:3980-3985.
36. Häkkinen M., Arvas M., Oja M., Aro N., Penttilä M., Saloheimo M., Pakula T.M. Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb. Cell Fact. 2012, 11:134.
37. Hasper A.A., Visser J., de Graaff L.H. 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. 2000, 36:193-200.
38. Hasper A.A., Dekkers E., van Mil M., van de Vondervoort P.J., de Graaff L.H. EglC, a new endoglucanase from Aspergillus niger with major activity towards xyloglucan. Appl. Environ. Microbiol. 2002, 68:1556-1560.
39. Hasper A.A., Trindade L.M., van der Veen D., van Ooyen A.J.J., de Graaff L.H. Functional analysis of the transcri[tional activator XlnR fro Aspergilus niger. Microbiology 2004, 150:1367-1375.
40. Heiland S., Radovanovic N., Höfer M., Winderickx J., Lichtenberg H. Multiple hexose transporters of Schizosaccharomyces pombe. J. Bacteriol. 2000, 182:2153-2162.
41. Henrissat B. A classification of glycosidases based on amino-acid sequence similarities. Biochem. J. 1991, 280:309-316.
42. Koivistoinen O.M., Richard P., Penttila M., Ruohonen L., Mojzita D. Sorbitol dehydrogenase of Aspergillus niger, SdhA, is part of the oxido-reductive d-galactose pathway and essential for d-sorbitol catabolism. FEBS Lett. 2012, 586:378-383.
43. Laemmli U.K. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 1970, 227:680.
44. Marathe D.D., Chandrasekaran E.V., Lau J.T.Y., Matta K.L., Neelamegham S. Systems-level studies of glycosyltransferase gene expression and enzyme activity that are associated with the selectin binding function of human leukocytes. FASEB J. 2008, 22:4154-4167.
45. Miller G.L. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 1959, 31:426-428.
46. Mojzita D., Penttilä M., Richard P. Identification of an l-arabinose reductase gene in Aspergillus niger and its role in l-arabinose catabolism. J. Biol. Chem. 2010, 285:23622-23628.
47. Mojzita D., Vuoristo K., Koivistoinen O.M., Penttilä M., Richard P. The 'true' l-xylulose reductase of filamentous fungi identified in Aspergillus niger. FEBS Lett. 2010, 584:3540-3544.
48. Mojzita D., Koivistoinen O.M., Maaheimo H., Penttila M., Ruohonen L., Richard P. Identification of the galactitol dehydrogenase, LadB, that is part of the oxido-reductive d-galactose catabolic pathway in Aspergillus niger. Fungal Genet. Biol. 2011, 49:152-159.
49. Mojzita D., Herold S., Metz B., Seiboth B., Richard P. L-Xylo-3-hexulose reductase is the missing link in the oxido-reductive pathway for d-galactose catabolism in filamentous fungi. J. Biol. Chem. 2012, 287:26010-26018.
50. Noguchi Y., Sano M., Kanamaru K., Ko T., Takeuchi M., Kato M., Kobayashi T. Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl. Microbiol. Biotechnol. 2009, 85:141-154.
51. Pel H.J., de Winde J.H., Archer D.B., Dyer P.S., Hofmann G., Schaap P.J., Turner G., de Vries R.P., Albang R., Albermann K., et al. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 2007, 25:221-231.
52. Roberts C.F. Enzyme lesions in galactose non-utilising mutants of Aspergillus nidulans. Biochim. Biophys. Acta 1970, 201:267-283.
53. Rocha G.J.M., Martin C., Soares I.B., Souto Maior A.M., Baudel H.M., Moraes C.A. Dilute mixed-acid pretreatment of sugarcane bagasse for the ethanol production. Biomass Bioenergy 2011, 35:663-670.
54. Rocha G.J.M., Martín C., da Silva V.F.N., Gómez E.O., Gonçalves A.R. Mass balance of pilot-scale pretreatment of sugarcane bagasse by steam explosion followed by alkaline delignification. Bioresour. Technol. 2012, 111:447-452.
55. Ruepp A., Zollner A., Maier D., Albermann K., Hani J., Mokrejs M., Tetko I., Güldener U., Mannhaupt G., Münsterkötter M., Mewes H.W. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004, 32:5539-5545.
56. Ruijter G.J.G., Visser J. Carbon repression in aspergilli. FEMS Microbiol. Lett. 1997, 151:103-114.
57. Seiboth B., Hartl L., Pail M., Kubicek C.P. 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, 2:867-875.
58. Seiboth B., Hartl L., Pail M., Fekete E., Karaffa L., Kubicek C.P. The galactokinase of Hypocrea jecorina is essential for cellulase induction by lactose but dispensable for growth on d-galactose. Mol. Microbiol. 2004, 51:1015-1025.
59. Semighini C.P., Marins M., Goldman M.H.S., Goldman G.H. Quantitative analysis of the relative transcript levels of ABC transporter Atr genes in Aspergillus nidulans by real-time reverse transcription-PCR assay. Appl. Environ. Microbiol. 2002, 68:1351-1357.
60. Shida Y., Furukawa T., Ogasawara W., Kato M., Kobayashi T., Okada H., Morikawa Y. Functional analysis of the egl3 upstream region in filamentous fungus Trichoderma ressei. Appl. Microbiol. Biotechnol. 2008, 78:514-524.
61. Stricker A.R., Mach R.L., de Graaff L.H. Regulation of transcription of cellulases- and hemicellulases-encoding genes in Aspergillus niger and Hypocrea jecorina (Trichoderma reesei). Appl. Microbiol. Biotechnol. 2008, 78:211-220.
62. Sun J., Tian C., Diamond S., Glass N.L. Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot. Cell 2012, 11:482-493.
63. van Peij N.N., Visser J., de Graaff L.H. Isolation and analysis of xlnR, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger. Mol. Microbiol. 1998, 27:131-142.
64. van Peij N.N., Gielkens M.M., de Vries R.P., Visser J., de Graaff L.H. The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl. Environ. Microbiol. 1998, 64:3615-3619.
65. vanKuyk P.A., de Groot M.J., Ruijter G.J., de Vries R.P., 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. Eur. J. Biochem. 2001, 268:5414-5423.
66. vankuyk P.A., Diderich J.A., MacCabe A.P., Hererro O., Ruijter G.J., Visser J. Aspergillus niger mstA encodes a high-affinity sugar/H+ symporter which is regulated in response to extracellular pH. Biochem. J. 2004, 379:375-383.
67. Witteveen C.F.B., Busink R., Van de Vondervoort P.J.I., Dijkema C., Swart K., Visser J. l-arabinose and d-xylose catabolism in Aspergillus niger. J. Gen. Microbiol. 1989, 135:2163-2171.
68. Young W.W. Organization of Golgi glycosylransferases in membrane: complexity via complexes. J. Membr. Biol. 2004, 198:1-13.