Penicillium decumbens BrlA extensively regulates secondary metabolism and functionally associates with the expression of cellulase genes

Applied Microbiology and Biotechnology

Volumn 97, Issue 24, 2013, Pages 10453-10467

  Qin, Yuqi ^a   Bao, Longfei ^a   Gao, Meirong ^a   Chen, Mei ^a   Lei, Yunfeng ^a   Liu, Guodong ^a   Qu, Yinbo ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Branches; Cellulase; Conidiation; Penicilliumdecumbens; Secondary metabolism

Indexed keywords

BRANCHES; CELLULASE; CONIDIATION; PENICILLIUMDECUMBENS; SECONDARY METABOLISM;

BIOCHEMISTRY; FUNGI; GENE EXPRESSION; METABOLISM; NUTRIENTS; POLYMERASE CHAIN REACTION;

GENE EXPRESSION REGULATION;

ACID PROTEINASE; CELLULASE; CHITIN SYNTHASE; GLYCOSIDASE; MYCOTOXIN;

CELLULOSE; FERMENTATION; FUNGUS; GENE EXPRESSION; GENOME; METABOLISM; PHENOTYPE; SECONDARY METABOLITE; TOXIN;

ARTICLE; BACTERIAL METABOLISM; BIOSYNTHESIS; BRLA GENE; CONTROLLED STUDY; EMERICELLA NIDULANS; ENZYME ACTIVITY; GENE; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; MORPHOLOGY; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PENICILLIUM DECUMBENS; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; SECONDARY METABOLISM; WILD TYPE;

CHINA;

CELLULASE; CHINA; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HYPHAE; MULTIGENE FAMILY; MYCOTOXINS; PENICILLIUM; SECONDARY METABOLISM; SPORES, FUNGAL;

EID: 84892146979     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5273-3     Document Type: Article

References (89)

1. Abad A, Fernández-Molina JV, Bikandi J, Ramírez A, Margareto J, Sendino J, Hernando FL, Pontón J, Garaizar J, Rementeria A (2010) What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol 27:155-182
2. Adams TH, Wieser JK, Yu JH (1998) Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62:35-54
3. Andrianopoulos A, Timberlake WE (1994) The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol Cell Biol 14:2503-2515
4. Arratia-Quijada J, Sánchez O, Scazzocchio C, Aguirre J (2012) FlbD, a Myb transcription factor of Aspergillus nidulans, is uniquely involved in both asexual and sexual differentiation. Eukaryot Cell 11:1132-1142
5. Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986-995
6. Baba S, Kinoshita H, Nihira T (2012) Identification and characterization of Penicillium citrinum VeA and LaeA as global regulators for ML-236B production. Curr Genet 58:1-11
7. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504-1506
8. Busby TM, Miller KY, Miller BL (1996) Suppression and enhancement of the Aspergillus nidulans medusa mutation by altered dosage of the bristle and stunted genes. Genetics 143:155-163
9. Calvo AM, Wilson RA, Bok JW, Keller NP (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66:447-459
10. Chang YC, Timberlake WE (1993) Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 133:29-38
11. Chang MH, Chae KS, Han DM, Jahng KY (2004) The GanB Gα-protein negatively regulates asexual sporulation and plays a positive role in conidial germination in Aspergillus nidulans. Genetics 167:1305-1315
12. Chang PK, Scharfenstein LL, Ehrlich KC, Wei Q, Bhatnagar D, Ingber BF (2012a) Effects of laeA deletion on Aspergillus flavus conidial development and hydrophobicity may contribute to loss of aflatoxin production. Fungal Biol 116:298-307
13. Chang PK, Scharfenstein LL, Mack B, Ehrlich KC (2012b) Deletion of the Aspergillus flavus orthologue of A. nidulans fluG reduces conidiation and promotes production of sclerotia but does not abolish aflatoxin biosynthesis. Appl Environ Microbiol 78:7557-7563
14. Cheng Y, Song X, Qin Y, Qu Y (2009) Genome shuffling improves production of cellulase by Penicillium decumbens JU-A10. J Appl Microbiol 107:1837-1846
15. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676
16. Cooper CR, Vanittanakom N (2008) Insights into the pathogenicity of Penicillium marneffei. Future Microbiol 3:43-55
17. Coutinho PM, Andersen MR, Kolenova K, van Kuyk PA, Benoit I, Gruben BS, Trejo-Aguilar B, Visser H, van Solingen P, Pakula T, Seiboth B, Battaglia E, Aguilar-Osorio G, de Jong JF, Ohm RA, Aguilar M, Henrissat B, Nielsen J, Stålbrand H, de Vries RP (2009) Post-genomic insights into the plant polysaccharide degradation potential of Aspergillus nidulans and comparison to Aspergillus niger and Aspergillus oryzae. Fungal Genet Biol 46:S161-S169
18. Dagenais TR, Giles SS, Aimanianda V, Latgé JP, Hull CM, Keller NP (2010) Aspergillus fumigatus LaeA-mediated phagocytosis is associated with a decreased hydrophobin layer. Infect Immun 78:823-829
19. D'Souza CA, Lee BN, Adams TH (2001) Characterization of the role of the FluG protein in asexual development of Aspergillus nidulans. Genetics 158:1027-1036
20. Emri T, Szilágyi M, LászlóK, M-Hamvas M, Pócsi I (2009) PepJisanew extracellular proteinase of Aspergillus nidulans. Folia Microbiol (Praha) 54:105-109
21. Etxebeste O, Ni M, Garzia A, Kwon NJ, Fischer R, Yu JH, Espeso EA, Ugalde U (2008) Basic-zipper-type transcription factor FlbB controls asexual development in Aspergillus nidulans. Eukaryot Cell 7:38-48
22. Fang X, Yano S, Inoue H, Sawayama S (2009) Strain improvement of Acremonium cellulolyticus for cellulase production by mutation. J Biosci Bioeng 107:256-261
23. Fukuda K, Yamada K, Deoka K, Yamashita S, Ohta A, Horiuchi H (2009) Class III chitin synthase ChsB of Aspergillus nidulans localizes at the sites of polarized cell wall synthesis and is required for conidial development. Eukaryot Cell 8:45-956
24. García-Estrada C, Ullán RV, Albillos SM, Fernández-Bodega MÁ, Durek P, von Döhren H, Martín JF (2011) A single cluster of coregulated genes encodes the biosynthesis of the mycotoxins roquefortine C and meleagrin in Penicillium chrysogenum. Chem Biol 18:1499-1512
25. Girardin H, Paris S, Rault J, Bellon-Fontaine MN, Latgé JP (1999) The role of the rodlet structure on the physicochemical properties of Aspergillus conidia. Lett Appl Microbiol 29:364-369
26. Gutiérrez S, Fierro F, Casqueiro J, Martín JF (1999) Gene organization and plasticity of the β-lactam genes in different filamentous fungi. Antoine van Leeuwenhoek 75:81-94
27. 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 251:451-460
28. Jami MS, García-Estrada C, Barreiro C, Cuadrado AA, Salehi-Najafabadi Z, Martín JF (2010) The Penicillium chrysogenum extracellular proteome. Conversion from a food-rotting strain to a versatile cell factory for white biotechnology. Mol Cell Proteomics 9:2729-2744
29. Jørgensen H, Kristian A, Krogh BR, Olsson L (2005) Production of cellulases and hemicellulases by three Penicillium species: effect of substrate and evaluation of cellulase adsorption by capillary electrophoresis. Enzyme Microb Technol 36:42-48
30. Jørgensen TR, Park J, Arentshorst M, van Welzen AM, Lamers G, Vankuyk PA, Damveld RA, van den Hondel CA, Nielsen KF, Frisvad JC, Ram AF (2011) The molecular and genetic basis of conidial pigmentation in Aspergillus niger. Fungal Genet Biol 48:544-553
31. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND (2010) SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol 47:736-741
32. Knutsen AP, Hutcheson PS, Slavin RG, Kurup VP (2004) IgE antibody to Aspergillus fumigatus recombinant allergens in cystic fibrosis patients with allergic bronchopulmonary aspergillosis. Allergy 59:198-203
33. Koukaki M, Giannoutsou E, Karagouni A, Diallinas G (2003) A novel improved method for Aspergillus nidulans transformation. J Microbiol Methods 55:687-695
34. Krappmann S, Bayram O, Braus GH (2005) Deletion and allelic exchange of the Aspergillus fumigatus veA locus via a novel recyclable marker module. Eukaryot Cell 4:1298-1307
35. 2 transcription factor regulating development in Aspergillus nidulans. Mol Microbiol 77:1203-1219
36. Kwon NJ, Shin KS, Yu JH (2010b) Characterization of the developmental regulator FlbE in Aspergillus fumigatus and Aspergillus nidulans. Fungal Genet Biol 47:981-993
37. Lafond M, Tauzin A, Desseaux V, Bonnin E, Ajandouz E-H, Giardina T (2011) GH10 xylanase D from Penicillium funiculosum: biochemical studies and xylooligosaccharide production. Microb Cell Fact 10:20
38. Lee BN, Adams TH (1996) fluG and flbA function interdependently to initiate conidiophore development in Aspergillus nidulans through brlA β activation. EMBO J 15:299-309
39. Lee JI, Choi JH, Park BC, Park YH, Lee MY, Park HM, Maeng PJ (2004) Differential expression of the chitin synthase genes of Aspergillus nidulans, chsA, chsB, and chsC, in response to developmental status and environmental factors. Fungal Genet Biol 41:635-646
40. Liu G, Zhang L, Wei X, Zou G, Qin Y, Ma L, Li J, Zheng H, Wang S, Wang C, Xun L, Zhao GP, Zhou Z, Qu Y (2013a) Genomic and secretomic analyses reveal unique features of the lignocellulolytic enzyme system of Penicillium decumbens. PLoS ONE 8:e55185
41. Liu G, Zhang L, Qin Y, Zou G, Li Z, Yan X, Wei X, Chen M, Chen L, Zheng K, Zhang J, Ma L, Li J, Liu R, Xu H, Bao X, Fang X, Wang L, Zhong Y, Liu W, Zheng H, Wang S, Wang C, Xun L, Zhao GP, Wang T, Zhou Z, Qu Y (2013b) Long-term strain improvements accumulate mutations in regulatory elements responsible for hyperproduction of cellulolytic enzymes. Sci Rep 3:1569
42. López-Berges MS, Hera C, Sulyok M, Schäfer K, Capilla J, Guarro J, Di Pietro A (2013) The velvet complex governs mycotoxin production and virulence of Fusarium oxysporum on plant and mammalian hosts. Mol Microbiol 87:49-65
43. Masayuki M, Osamu Y, Katsuya G (2008) Genomics of Aspergillus oryzae: learning from the history of Koji mold and exploration of its future. DNA Res 15:173-183
44. Mayorga ME, Timberlake WE (1990) Isolation and molecular characterization of the Aspergillus nidulans wA gene. Genetics 126:73-79
45. McGuire SL, Roe DL, Carter BW, Carter RL, Grace SP, Hays PL, Lang GA, Mamaril JL, McElvaine AT, Payne AM, Schrader MD, Wahrle SE, Young CD (2000) Extragenic suppressors of the nimX2 (cdc2) mutation of Aspergillus nidulans affect nuclear division, septation and conidiation. Genetics 156:1573-1584
46. Melin P, Schnürer J, Wagner EG (2003) Characterization of phiA, a gene essential for phialide development in Aspergillus nidulans. Fungal Genet Biol 40:234-241
47. Mellado E, Aufauvre-Brown A, Gow NA, Holden DW (1996) The Aspergillus fumigatus chsC and chsG genes encode class III chitin synthases with different functions. Mol Microbiol 20:667-679
48. Mellado E, Dubreucq G, Mol P, Sarfati J, Paris S, Diaquin M, Holden DW, Rodriguez-Tudela JL, Latgé JP (2003) Cell wall biogenesis in a double chitin synthase mutant (chsG-/chsE-) of Aspergillus fumigatus. Fungal Genet Biol 38:98-109
49. Meyer V, Mueller D, Strowig T, Stahl U (2003) Comparison of different transformation methods for Aspergillus giganteus. Curr Genet 43:371-377
50. Mirabito PM, Adams TH, Timberlake WE (1989) Interactions of three sequentially expressed genes control temporal and spatial specificity in Aspergillus development. Cell 57:859-868
51. Molnár Z, Mészáros E, Szilágyi Z, Rosén S, Emri T (2004) Influence of fadAG203R and ?flbA mutations onmorphology and physiology of submerged Aspergillus nidulans cultures. Appl Biochem Biotechnol 118:349-360
52. Moralejo FJ, Cardoza RE, Gutierrez S, Lombraña M, Fierro F, Martín JF (2002) Silencing of the aspergillopepsin B (pepB) gene of Aspergillus awamori by antisense RNA expression or protease removal by gene disruption results in a large increase in thaumatin production. Appl Environ Microbiol 68:3550-3559
53. Nakari-Setälä T, Paloheimo M, Kallio J, Vehmaanperä J, Penttilä M, Saloheimo M (2009) Genetic modification of carbon catabolite repression in Trichoderma reesei for improved protein production. Appl Environ Microbiol 75:4853-4860
54. Navarro RE, Stringer MA, Hansberg W, Timberlake WE, Aguirre J (1996) catA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. Curr Genet 29:352-359
55. Ni M, Yu JH (2007) A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS ONE 2:e970
56. Ogawa M, Tokuoka M, Jin FJ, Takahashi T, Koyama Y (2010) Genetic analysis of conidiation regulatory pathways in koji-mold Aspergillus oryzae. Fungal Genet Biol 47:10-18
57. Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, Mallet R, Chabasse D, Symoens F, Bouchara JP (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9:177
58. Polonelli L, Morace G, Rosa R, Castagnola M, Frisvad JC (1987) Antigenic characterization of Penicillium camemberti and related common cheese contaminants. Appl Environ Microbiol 53:872-878
59. Prade RA, Timberlake WE (1993) The Aspergillus nidulans brlA regulatory locus consists of overlapping transcription units that are individually required for conidiophore development. EMBO J 12:2439-2447
60. Ravanal MC, Callegari E, Eyzaguirre J (2010) Novel bifunctional α-L-arabinofuranosidase/xylobiohydrolase (ABF3) from Penicillium purpurogenum. Appl Environ Microbiol 76:5247-5253
61. Sahare P, Singh R, Laxman RS, Rao M (2012) Effect of alkali pretreatment on the structural properties and enzymatic hydrolysis of corn cob. Appl Biochem Biotechnol 168:1806-1819
62. Sarikaya Bayram Ö, Bayram Ö, Valerius O, Park HS, Irniger S, Gerke J, Ni M, Han KH, Yu JH, Braus GH (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6:e1001226
63. Schier N, Liese R, Fischer R (2001) A Pcl-like cyclin of Aspergillus nidulans is transcriptionally activated by developmental regulators and is involved in sporulation. Mol Cell Biol 21:4075-4088
64. Seo JA, Guan Y, Yu JH (2003) Suppressor mutations bypass the requirement of fluG for asexual sporulation and sterigmatocystin production in Aspergillus nidulans. Genetics 165:1083-1093
65. Seo JA, Guan Y, Yu JH (2006) FluG-dependent asexual development in Aspergillus nidulans occurs via derepression. Genetics 172:1535-1544
66. Si H, Rittenour WR, Xu K, Nicksarlian M, Calvo AM, Harris SD (2012) Morphogenetic and developmental functions of the Aspergillus nidulans homologues of the yeast bud site selection proteins Bud4 and Axl2. Mol Microbiol 85:252-270
67. Sigl C, Haas H, Specht T, Pfaller K, Kürnsteiner H, Zadra I (2011) Among developmental regulators, StuA but not BrlA is essential for penicillin V production in Penicillium chrysogenum. Appl Environ Microbiol 77:972-982
68. Singhvi MS, Adsul MG, Gokhale DV (2011) Comparative production of cellulases by mutants of Penicillium janthinellum NCIM 1171 and its application in hydrolysis of Avicel and cellulose. Bioresour Technol 102:6569-6572
69. Soid-Raggi G, Sánchez O, Aguirre J (2006) TmpA, a member of a novel family of putative membrane flavoproteins, regulates asexual development in Aspergillus nidulans. Mol Microbiol 59:854-869
70. Strauss J, Mach RL, Zeilinger S, Hartler G, Stöffler G, Wolschek M, Kubicek CP (1995) Cre1, the carbon catabolite repressor protein from Trichoderma reesei. FEBS Lett 376:103-107
71. Stringer MA, Timberlake WE (1995) dewA encodes a fungal hydrophobin component of the Aspergillus spore wall. Mol Microbiol 16:33-44
72. Sun J, Glass NL (2011) Identification of the CRE-1 cellulolytic regulon in Neurospora crassa. PLoS ONE 6:e25654
73. Sun J, Li JP, Wang AQ, Tang GM, Wang HM (2004) Construction and functional analysis of the pepB gene disruptant in Aspergillus niger. Wei Sheng Wu Xue Bao 44:766-770
74. Sun X, Liu Z, Qu Y, Li X (2008) The effects of wheat bran composition on the production of biomass-hydrolyzing enzymes by Penicillium decumbens. Appl Biochem Biotechnol 146:119-128
75. Szilágyi M, Kwon NJ, Dorogi C, Pócsi I, Yu JH, Emri T (2010) The extracellular β-1, 3-endoglucanase EngA is involved in autolysis of Aspergillus nidulans. J Appl Microbiol 109:1498-1508
76. Szilágyi M, Kwon NJ, Bakti F, M-Hamvas M, Jámbrik K, Park H, Pócsi I, Yu JH, Emri T (2011) Extracellular proteinase formation in carbon starving Aspergillus nidulans cultures - physiological function and regulation. J Basic Microbiol 51:625-634
77. 't Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, de Menezes RX, Boer JM, van Ommen GJ, den Dunnen JT (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36:e141
78. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
79. Tao L, Yu JH (2011) AbaA and WetA govern distinct stages of Aspergillus fumigatus development. Mcrobiology 157:313-326
80. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
81. Todd RB, Greenhalgh JR, Hynes MJ, Andrianopoulos A (2003) TupA, the Penicillium marneffei Tup1p homologue, represses both yeast and spore development. Mol Microbiol 48:85-94
82. Twumasi-Boateng K, Yu Y, Chen D, Gravelat FN, Nierman WC, Sheppard DC (2009) Transcriptional profiling identifies a role for BrlA in the response to nitrogen depletion and for StuA in the regulation of secondary metabolite clusters in Aspergillus fumigatus. Eukaryot Cell 8:104-115
83. van den Hombergh JP, Sollewijn Gelpke MD, van de Vondervoort PJ, Buxton FP, Visser J (1997) Disruption of three acid proteases in Aspergillus niger-effects on protease spectrum, intracellular proteolysis, and degradation of target proteins. Eur J Biochem 247:605-613
84. Wadman MW, de Vries RP, Kalkhove SI, Veldink GA, Vliegenthart JF (2009) Characterization of oxylipins and dioxygenase genes in the asexual fungus Aspergillus niger. BMC Microbiol 9:59
85. Wiebe MC, Robson GD, Trinci A P J (1990) Edifenphos (Hinosan) reduces hyphal extension, hyphal growth unit length and phosphatidylcholine content of Fusarium graminearum A3/5, but has no effect on specific growth rate. J Gen Mcrobiol 136:979-984
86. Wieser J, Lee BN, Fondon JW 3rd, Adams TH (1994) Genetic requirements for initiating asexual development in Aspergillus nidulans. Curr Genet 27:62-69
87. Yamazaki H, Yamazaki D, Takaya N, Takagi M, Ohta A, Horiuchi H (2007) A chitinase gene, chiB, involved in the autolytic process of Aspergillus nidulans. Curr Genet 51:89-98
88. Yang Y, Li L, Li X, Shao Y, Chen F (2012) mrflbA, encoding a putative FlbA, is involved in aerial hyphal development and secondary metabolite production in Monascus ruber M-7. Fungal Biol 116:225-233
89. Yu JH, Rosén S, Adams TH (1999) Extragenic suppressors of loss-offunction mutations in the Aspergillus FlbA regulator of G-protein signaling domain protein. Genetics 151:97-105