Genome-wide analysis of the Zn(II)2Cys6 zinc cluster-encoding gene family in Aspergillus flavus

Applied Microbiology and Biotechnology

Volumn 97, Issue 10, 2013, Pages 4289-4300

  Chang, Perng Kuang ^a   Ehrlich, Kenneth C ^a  

^a SOUTHERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

Aspergillus flavus; DUF3468; Gene cluster; Genome; Secondary metabolite; Zinc cluster protein

Indexed keywords

ASPERGILLUS FLAVUS; ASPERGILLUS NIDULANS; DUF3468; GENE CLUSTERS; INVASIVE ASPERGILLOSIS; SECONDARY METABOLITES; SEXUAL DIFFERENTIATIONS; ZINC FINGER PROTEIN;

AMINO ACIDS; ASPERGILLUS; BIOINFORMATICS; METABOLITES; TRANSCRIPTION FACTORS; YEAST; ZINC; ZINC COMPOUNDS;

GENES;

ARABINOXYLAN; CARBON; CELLULOSE; CYSTEINE; DIMETHYLALLYL TRYPTOPHAN SYNTHASE; DNA BINDING PROTEIN; ENTEROBACTIN ESTERASE; FARNESYL TRANS TRANSFERASE; FUNGAL PROTEIN; ISOPENICILLIN N SYNTHETASE; NITROGEN; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG; ZINC CLUSTER PROTEIN; ZINC DERIVATIVE;

DATABASE; FUNGUS; GENOME; PROTEIN; SECONDARY METABOLITE; SPACING; YEAST; ZINC;

AMINO ACID SEQUENCE; ASEXUAL REPRODUCTION; ASPERGILLUS FLAVUS; ASPERGILLUS NIGER; CARBON UTILIZATION; FUNGAL GENETICS; GENE CLUSTER; NITROGEN UTILIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; REVIEW; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT;

AMINO ACID SEQUENCE; ASPERGILLUS FLAVUS; CYSTEINE; DATABASES, GENETIC; FUNGAL PROTEINS; GENOME, FUNGAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NITROGEN; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

ASPERGILLUS FLAVUS; CANDIDA ALBICANS; EMERICELLA NIDULANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 84877787096     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-4865-2     Document Type: Review

References (77)

1. Abe Y, Ono C, Hosobuchi M, Yoshikawa H (2002) Functional analysis of mlcR, a regulatory gene for ML-236B (compactin) biosynthesis in Penicillium citrinum. Mol Genet Genomics 268:352-361 (Pubitemid 35352135)
2. Akache B, Wu K, Turcotte B (2001) Phenotypic analysis of genes encoding yeast zinc cluster proteins. Nucleic Acids Res 29:2181-2190 (Pubitemid 32472089)
3. Andrianopoulos A, Hynes MJ (1990) Sequence and functional analysis of the positively acting regulatory gene amdR from Aspergillus nidulans. Mol Cell Biol 10:3194-3203
4. Baum JA, Geever R, Giles NH (1987) Expression of qa-1F activator protein: identification of upstream binding sites in the qa gene cluster and localization of the DNA-binding domain. Mol Cell Biol 7:1256-1266 (Pubitemid 17017449)
5. 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 (Pubitemid 351929431)
6. Bergmann S, Schumann J, Scherlach K, Lange C, Brakhage AA, Hertweck C (2007) Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat Chem Biol 3:213-217 (Pubitemid 46440540)
7. Beri RK, Whittington H, Roberts CF, Hawkins AR (1987) Isolation and characterization of the positively acting regulatory gene QUTA from Aspergillus nidulans. Nucleic Acids Res 15:7991-8001
8. Bibbins M, Crepin VF, Cummings NJ, Mizote T, Baker K, Mellits KH, Connerton IF (2002) A regulator gene for acetate utilisation from Neurospora crassa. Mol Genet Genomics 267:498-505 (Pubitemid 34671344)
9. Bluhm BH, Kim H, Butchko RA, Woloshuk CP (2008) Involvement of ZFR1 of Fusarium verticillioides in kernel colonization and the regulation of FST1, a putative sugar transporter gene required for fumonisin biosynthesis on maize kernels. Mol Plant Pathol 9:203-211 (Pubitemid 351281002)
10. Bok JW, Chung D, Balajee SA, Marr KA, Andes D, Nielsen KF, Frisvad JC, Kirby KA, Keller NP (2006) GliZ, a transcriptional regulator of gliotoxin biosynthesis, contributes to Aspergillus fumigatus virulence. Infect Immun 74:6761-6768 (Pubitemid 44913150)
11. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ (2011) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7:e1001287
12. Brakhage AA (2012) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21-32
13. 6 protein that affects FUM gene expression and fumonisin production. Eukaryot Cell 6:1210-1218 (Pubitemid 47077172)
14. Brown DW, Yu JH, Kelkar HS, Fernandes M, Nesbitt TC, Keller NP, Adams TH, Leonard TJ (1996) Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc Natl Acad Sci U S A 93:1418-1422 (Pubitemid 26075137)
15. Burger G, Strauss J, Scazzocchio C, Lang BF (1991) nirA, the pathway-specific regulatory gene of nitrate assimilation in Aspergillus nidulans, encodes a putative GAL4-type zinc finger protein and contains four introns in highly conserved regions. Mol Cell Biol 11:5746-5755 (Pubitemid 21895342)
16. Chang P-K, Ehrlich KC, Yu J, Bhatnagar D, Cleveland TE (1995) Increased expression of Aspergillus parasiticus aflR, encoding a sequence-specific DNA-binding protein, relieves nitrate inhibition of aflatoxin biosynthesis. Appl Environ Microbiol 61:2372-2377
17. Chang P-K, Horn BW, Dorner JW (2009) Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus. Fungal Genet Biol 46:176-182
18. Chang P-K, Scharfenstein LL, Mack B, Ehrlich KC (2012) 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
19. Chang P-K, Scharfenstein LL, Wei Q, Bhatnagar D (2010) Development and refinement of a high-efficiency gene-targeting system for Aspergillus flavus. J Microbiol Methods 81:240-246
20. Chen H, Lee MH, Daub ME, Chung KR (2007) Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae. Mol Microbiol 64:755-770 (Pubitemid 46653212)
21. Chen YP, Yuan GF, Hsieh SY, Lin YS, Wang WY, Liaw LL, Tseng CP (2010) Identification of the mokH gene encoding transcription factor for the upregulation of monacolin K biosynthesis in Monascus pilosus. J Agric Food Chem 58:287-293
22. Chiang YM, Szewczyk E, Davidson AD, Entwistle R, Keller NP, Wang CC, Oakley BR (2010) Characterization of the Aspergillus nidulans monodictyphenone gene cluster. Appl Environ Microbiol 76:2067-2074
23. Chiang YM, Szewczyk E, Davidson AD, Keller N, Oakley BR, Wang CC (2009) A gene cluster containing two fungal polyketide synthases encodes the biosynthetic pathway for a polyketide, asperfuranone, in Aspergillus nidulans. J Am Chem Soc 131:2965-2970
24. 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 (Pubitemid 32667089)
25. 6 zinc cluster DNA-binding motif, derived from the basidiomycete Lentinus edodes. Gene 139:117-121 (Pubitemid 24086749)
26. Felenbok B, Sequeval D, Mathieu M, Sibley S, Gwynne DI, Davies RW (1988) The ethanol regulon in Aspergillus nidulans: characterization and sequence of the positive regulatory gene alcR. Gene 73:385-396 (Pubitemid 19043271)
27. 6 DNA binding protein regulates the sirodesmin PL biosynthetic gene cluster in Leptosphaeria maculans. Fungal Genet Biol 45:671-682 (Pubitemid 351484257)
28. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D'Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Penalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105-1115 (Pubitemid 41831674)
29. Gardner KH, Pan T, Narula S, Rivera E, Coleman JE (1991) Structure of the binuclear metal-binding site in the GAL4 transcription factor. Biochemistry 30:11292-11302
30. Georgianna DR, Fedorova ND, Burroughs JL, Dolezal AL, Bok JW, Horowitz-Brown S, Woloshuk CP, Yu J, Keller NP, Payne GA (2010) Beyond aflatoxin: four distinct expression patterns and functional roles associated with Aspergillus flavus secondary metabolism gene clusters. Mol Plant Pathol 11:213-226
31. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274:563-567 (Pubitemid 26360429)
32. Gomi K, Akeno T, Minetoki T, Ozeki K, Kumagai C, Okazaki N, Iimura Y (2000) Molecular cloning and characterization of a transcriptional activator gene, amyR, involved in the amylolytic gene expression in Aspergillus oryzae. Biosci Biotechnol Biochem 64:816-827
33. Hidalgo P, Ansari AZ, Schmidt P, Hare B, Simkovich N, Farrell S, Shin EJ, Ptashne M, Wagner G (2001) Recruitment of the transcriptional machinery through GAL11P: structure and interactions of the GAL4 dimerization domain. Genes Dev 15:1007-1020 (Pubitemid 32323550)
34. Hong M, Fitzgerald MX, Harper S, Luo C, Speicher DW, Marmorstein R (2008) Structural basis for dimerization in DNA recognition by Gal4. Structure 16:1019-1026 (Pubitemid 351899283)
35. Horn BW, Moore GG, Carbone I (2009) Sexual reproduction in Aspergillus flavus. Mycologia 101:423-429
36. Huang X, Li HM (2009) Cloning and bioinformatic analysis of lovastatin biosynthesis regulatory gene lovE. Chin Med J (Engl) 122:1800-1805
37. 6-type transcription regulator, controls plant infection of the vascular wilt fungus Fusarium oxysporum. Mol Microbiol 63:737-753 (Pubitemid 46105899)
38. Johnston M (1987) A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol Rev 51:458-476
39. Keegan L, Gill G, Ptashne M (1986) Separation of DNA binding from the transcription-activating function of a eukaryotic regulatory protein. Science 231:699-704 (Pubitemid 16104039)
40. Keller S, Macheleidt J, Scherlach K, Schmaler-Ripcke J, Jacobsen ID, Heinekamp T, Brakhage AA (2011) Pyomelanin formation in Aspergillus fumigatus requires HmgX and the transcriptional activator HmgR but is dispensable for virulence. PLoS One 6:e26604
41. 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
42. Kihara J, Moriwaki A, Tanaka N, Tanaka C, Ueno M, Arase S (2008) Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett 281:221-227 (Pubitemid 351422947)
43. Kim JE, Jin J, Kim H, Kim JC, Yun SH, Lee YW (2006) GIP2, a putative transcription factor that regulates the aurofusarin biosynthetic gene cluster in Gibberella zeae. Appl Environ Microbiol 72:1645-1652 (Pubitemid 43271281)
44. Lee BN, Adams TH (1996) fluG and flbA function interdependently to initiate conidiophore development in Aspergillus nidulans through brlAβ activation. EMBO J 15:299-309
45. Lee BY, Han SY, Choi HG, Kim JH, Han KH, Han DM (2005) Screening of growth- or development-related genes by using genomic library with inducible promoter in Aspergillus nidulans. J Microbiol 43:523-528
46. Liu TD, Marzluf GA (2004) Characterization of pco-1, a newly identified gene which regulates purine catabolism in Neurospora. Curr Genet 46:213-227 (Pubitemid 39462390)
47. Ma J, Ptashne M (1987a) The carboxy-terminal 30 amino acids of GAL4 are recognized by GAL80. Cell 50:137-142
48. Ma J, Ptashne M (1987b) Deletion analysis of GAL4 defines two transcriptional activating segments. Cell 48:847-853
49. MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70:583-604 (Pubitemid 44484686)
50. 6 binuclear cluster DNA-binding domains in Candida albicans. Comp Funct Genomics 6:345-356 (Pubitemid 43336578)
51. Marmorstein R, Carey M, Ptashne M, Harrison SC (1992) DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356:408-414
52. Nakazawa T, Ishiuchi K, Praseuth A, Noguchi H, Hotta K, Watanabe K (2012) Overexpressing transcriptional regulator in Aspergillus oryzae activates a silent biosynthetic pathway to produce a novel polyketide. ChemBioChem 13:855-861
53. Nicholson MJ, Koulman A, Monahan BJ, Pritchard BL, Payne GA, Scott B (2009) Identification of two aflatrem biosynthesis gene loci in Aspergillus flavus and metabolic engineering of Penicillium paxilli to elucidate their function. Appl Environ Microbiol 75:7469-7481
54. Noguchi Y, Sano M, Kanamaru K, Ko T, Takeuchi M, Kato M, Kobayashi T (2009) Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl Microbiol Biotechnol 85:141-154
55. 6 transcriptional activator, controls the beta-mannan utilization system in Aspergillus oryzae. Fungal Genet Biol 49:987-995
56. 6 binuclear cluster. Proc Natl Acad Sci U S A 87:2077-2081
57. Payne GA, Nierman WC, Wortman JR, Pritchard BL, Brown D, Dean RA, Bhatnagar D, Cleveland TE, Machida M, Yu J (2006) Whole genome comparison of Aspergillus flavus and A. oryzae. Med Mycol 44(Suppl):9-11 (Pubitemid 44524078)
58. Payne GA, Nystrom GJ, Bhatnagar D, Cleveland TE, Woloshuk CP (1993) Cloning of the afl-2 gene involved in aflatoxin biosynthesis from Aspergillus flavus. Appl Environ Microbiol 59:156-162 (Pubitemid 23028384)
59. Pildain MB, Frisvad JC, Vaamonde G, Cabral D, Varga J, Samson RA (2008) Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. Int J Syst Evol Microbiol 58:725-735
60. Reece RJ, Ptashne M (1993) Determinants of binding-site specificity among yeast C6 zinc cluster proteins. Science 261:909-911 (Pubitemid 23275805)
61. Sato A, Oshima K, Noguchi H, Ogawa M, Takahashi T, Oguma T, Koyama Y, Itoh T, Hattori M, Hanya Y (2011) Draft genome sequencing and comparative analysis of Aspergillus sojae NBRC4239. DNA Res 18:165-176
62. Scazzocchio C (1994) The proline utilisation pathway, history and beyond. Prog Ind Microbiol 29:259-277
63. Seo JA, Guan Y, Yu JH (2006) FluG-dependent asexual development in Aspergillus nidulans occurs via derepression. Genetics 172:1535-1544
64. Shimizu T, Kinoshita H, Nihira T (2007) Identification and in vivo functional analysis by gene disruption of ctnA, an activator gene involved in citrinin biosynthesis in Monascus purpureus. Appl Environ Microbiol 73:5097-5103 (Pubitemid 47326638)
65. Suarez T, de Queiroz MV, Oestreicher N, Scazzocchio C (1995) The sequence and binding specificity of UaY, the specific regulator of the purine utilization pathway in Aspergillus nidulans, suggest an evolutionary relationship with the PPR1 protein of Saccharomyces cerevisiae. EMBO J 14:1453-1467
66. 6 binuclear cluster DNA binding motif. Fungal Genet Biol 21:388-405 (Pubitemid 27453328)
67. 6 transcriptional activator. Mol Gen Genet 254:495-504 (Pubitemid 27246468)
68. 6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 38:940-954 (Pubitemid 32009671)
69. 6 putative transcription factor NosA controls fruiting body formation in Aspergillus nidulans. Mol Microbiol 61:544-554 (Pubitemid 44356582)
70. 6 putative Aspergillus nidulans transcription factor repressor of sexual development inhibits sexual development under low-carbon conditions and in submersed culture. Genetics 169:619-630 (Pubitemid 40404299)
71. Wiemann P, Willmann A, Straeten M, Kleigrewe K, Beyer M, Humpf HU, Tudzynski B (2009) Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Mol Microbiol 72:931-946
72. Wight WD, Kim KH, Lawrence CB, Walton JD (2009) Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. Mol Plant Microbe Interact 22:1258-1267
73. Young C, McMillan L, Telfer E, Scott B (2001) Molecular cloning and genetic analysis of an indole-diterpene gene cluster from Penicillium paxilli. Mol Microbiol 39:754-764 (Pubitemid 32158153)
74. Yu J, Chang P-K, Ehrlich KC, Cary JW, Bhatnagar D, Cleveland TE, Payne GA, Linz JE, Woloshuk CP, Bennett JW (2004) Clustered pathway genes in aflatoxin biosynthesis. Appl Environ Microbiol 70:1253-1262 (Pubitemid 38365101)
75. Yuan GF, Fu YH, Marzluf GA (1991) nit-4, a pathway-specific regulatory gene of Neurospora crassa, encodes a protein with a putative binuclear zinc DNA-binding domain. Mol Cell Biol 11:5735-5745 (Pubitemid 21895341)
76. 6 transcriptional activator involved in the regulation of inulinolytic genes in Aspergillus niger. Mol Genet Genomics 279:11-26 (Pubitemid 350243858)
77. Zhang S, Monahan BJ, Tkacz JS, Scott B (2004) Indole-diterpene gene cluster from Aspergillus flavus. Appl Environ Microbiol 70:6875-6883 (Pubitemid 39518601)