Members of the Penicillium chrysogenum velvet complex play functionally opposing roles in the regulation of penicillin biosynthesis and conidiation

Eukaryotic Cell

Volumn 12, Issue 2, 2013, Pages 299-310

  Kopke, Katarina ^a   Hoff, Birgit ^a,b   Bloemendal, Sandra ^a   Katschorowski, Alexandra ^a   Kamerewerd, Jens ^a   Kück, Ulrich ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b BASF SE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MULTIPROTEIN COMPLEX; PENICILLIN DERIVATIVE;

ARTICLE; BIOSYNTHESIS; DNA MICROARRAY; FUNGUS HYPHAE; FUNGUS SPORE; GENE INACTIVATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MICROBIAL VIABILITY; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PENICILLIUM CHRYSOGENUM; PHENOTYPE; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION;

FUNGAL PROTEINS; GENE KNOCKOUT TECHNIQUES; GENE REGULATORY NETWORKS; HYPHAE; MICROBIAL VIABILITY; MULTIPROTEIN COMPLEXES; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PENICILLINS; PENICILLIUM CHRYSOGENUM; PHENOTYPE; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION; SPORES, FUNGAL;

EID: 84873134889     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00272-12     Document Type: Article

References (55)

1. Fleming A. 1929. On the antibacterial action of cultures of a Penicillium, with special reference to their use in the isolation of B. influenzae. Br. J. Exp. Pathol. 10:226-236.
2. Barber MS, Giesecke U, Reichert A, Minas W. 2004. Industrial enzymatic production of cephalosporin-based beta-lactams. Adv. Biochem. Eng. Biotechnol. 88:179-215.
3. van den Berg MA. 2011. Impact of the Penicillium chrysogenum genome on industrial production of metabolites. Appl. Microbiol. Biotechnol. 92: 45-53.
4. Brakhage AA, Spröte P, Al-Abdallah Q, Gehrke A, Plattner H, Tüncher A. 2004. Regulation of penicillin biosynthesis in filamentous fungi. Adv. Biochem. Eng. Biotechnol. 88:45-90.
5. Martín JF, Liras P. 1989. Organization and expression of genes involved in the biosynthesis of antibiotics and other secondary metabolites. Annu. Rev. Microbiol. 43:173-206.
6. Woloshuk CP, Prieto R. 1998. Genetic organization and function of the aflatoxin B1 biosynthetic genes. FEMS Microbiol. Lett. 160:169-176.
7. Yu JH, Keller N. 2005. Regulation of secondary metabolism in filamentous fungi. Annu. Rev. Phytopathol. 43:437-458.
8. Calvo AM, Wilson RA, Bok JW, Keller NP. 2002. Relationship between secondary metabolism and fungal development. Microbiol. Mol. Biol. Rev. 66:447-459.
9. Tag A, Hicks J, Garifullina G, Ake C, Phillips TD, Beremand M, Keller N. 2000. G-protein signalling mediates differential production of toxic secondary metabolites. Mol. Microbiol. 38:658-665.
10. Hicks JK, Yu JH, Keller NP, Adams TH. 1997. Aspergillus sporulation and mycotoxin production both require inactivation of the FadA G alpha protein-dependent signaling pathway. EMBO J. 16:4916-4923.
11. Keller NP, Turner G, Bennett JW. 2005. Fungal secondary metabolism-from biochemistry to genomics. Nat. Rev. Microbiol. 3:937-947.
12. Schmitt EK, Hoff B, Kück U. 2004. AcFKH1, a novel member of the forkhead family, associates with RFX transcription factor CPCR1 in the cephalosporin C-producing fungus Acremonium chrysogenum. Gene 342: 269-281.
13. Hoff B, Kück U. 2005. Use of bimolecular fluorescence complementation to demonstrate transcription factor interaction in nuclei of living cells from the filamentous fungus Acremonium chrysogenum. Curr. Genet. 47: 132-138.
14. Hoff B, Schmitt EK, Kück U. 2005. CPCR1, but not its interacting transcription factor AcFKH1, controls fungal arthrospore formation in Acremonium chrysogenum. Mol. Microbiol. 56:1220-1233.
15. Kato N, Brooks W, Calvo AM. 2003. The expression of sterigmatocystin and penicillin genes in Aspergillus nidulans is controlled by veA, a gene required for sexual development. Eukaryot. Cell 2:1178-1186.
16. Spröte P, Brakhage AA. 2007. The light-dependent regulator velvet A of Aspergillus nidulans acts as a repressor of the penicillin biosynthesis. Arch. Microbiol. 188:69-79.
17. Bayram Ö, 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.
18. Purschwitz J, Müller S, Fischer R. 2009. Mapping the interaction sites of Aspergillus nidulans phytochrome FphA with the global regulator VeA and the White Collar protein LreB. Mol. Genet. Genomics 281:35-42.
19. Calvo AM. 2008. The VeA regulatory system and its role in morphological and chemical development in fungi. Fungal Genet. Biol. 45:1053-1061.
20. Käfer E. 1965. Origins of translocations in Aspergillus nidulans. Genetics 52:217-232.
21. Bok JW, Keller NP. 2004. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot. Cell 3:527-535.
22. Ni M, Yu JH. 2007. A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS One 2:e970. doi:10.1371/journal.pone.0000970.
23. Sarikaya BayramÖ, 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. doi:10.1371/journal.pgen.1001226.
24. Bayram Ö, Braus GH. 2012. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol. Rev. 36:1-24.
25. Myung K, Zitomer NC, Duvall M, Glenn AE, Riley RT, Calvo AM. 2012. The conserved global regulator VeA is necessary for symptom production and mycotoxin synthesis in maize seedlings by Fusarium verticillioides. Plant Pathol. 61:152-160.
26. Hoff B, Kamerewerd J, Sigl C, Mitterbauer R, Zadra I, Kürnsteiner H, Kück U. 2010. Two components of a velvet-like complex control hyphal morphogenesis, conidiophore development, and penicillin biosynthesis in Penicillium chrysogenum. Eukaryot. Cell 9:1236-1250.
27. Sambrook J, Russell DW. 2001. Molecular cloning, a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Habor, NY.
28. Bullock WO, Fernandez JM, Short JM. 1987. XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with α-galactosidase selection. Biotechniques 5:376-378.
29. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U. S. A. 103:10352-10357.
30. Becker DM, Lundblad V. 1994. Introduction of DNA into yeast cells, p 13.17.11-13.17.10. In Ausubel FM, Brent R, Kingston RE, Moore DD, Seidmann JG, Smith JA, Struhl K (ed), Current protocols in molecular biology. John Wiley & Sons, Inc., Hoboken, NJ.
31. Hoff B, Kamerewerd J, Sigl C, Zadra I, Kück U. 2010. Homologous recombination in the antibiotic producer Penicillium chrysogenum: strain α-Pcku70 shows up-regulation of genes from the HOG pathway. Appl. Microbiol. Biotechnol. 85:1081-1094.
32. Kopke K, Hoff B, Kück U. 2010. Application of the Saccharomyces cerevisiae FLP/FRT recombination system in filamentous fungi for marker recycling and construction of knockout strains devoid of heterologous genes. Appl. Environ. Microbiol. 76:4664-4674.
33. Janus D, Hoff B, Kück U. 2009. Evidence for Dicer-dependent RNA interference in the industrial penicillin producer Penicillium chrysogenum. Microbiology 155:3946-3956.
34. Hoff B, Pöggeler S, Kück U. 2008. Eighty years after its discovery, Fleming's Penicillium strain discloses the secret of its sex. Eukaryot. Cell 7:465-470.
35. van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJ, Garcia-Estrada C, Fedorova ND, Harris DM, Heijne WH, Joardar V, Kiel JA, Kovalchuk A, Martín JF, Nierman WC, Nijland JG, Pronk JT, Roubos JA, van der Klei IJ, van Peij NN, Veenhuis M, von Döhren H, Wagner C, Wortman J, Bovenberg RA. 2008. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26:1161-1168.
36. Zadra I, Abt B, Parson W, Haas H. 2000. xylP promoter-based expression system and its use for antisense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl. Environ. Microbiol. 66:4810-4816.
37. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119-122.
38. Jekosch K, Kück U. 2000. Loss of glucose repression in an Acremonium chrysogenum beta-lactam producer strain and its restoration by multiple copies of the cre1 gene. Appl. Microbiol. Biotechnol. 54:556-563.
39. Schmitt EK, Bunse A, Janus D, Hoff B, Friedlin E, Kürnsteiner H, Kück U. 2004. Winged helix transcription factor CPCR1 is involved in regulation of beta-lactam biosynthesis in the fungus Acremonium chrysogenum. Eukaryot. Cell 3:121-134.
40. Bloemendal S, Bernhards Y, Bartho K, Dettmann A, Voigt O, Teichert I, Seiler S, Wolters DA, Pöggeler S, Kück U. 2012. A homologue of the human STRIPAK complex controls sexual development in fungi. Mol. Microbiol. 84:310-323.
41. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35:W585-W587.
42. la Cour T, Kiemer L, Molgaard A, Gupta R, Skriver K, Brunak S. 2004. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17:527-536.
43. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: 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.
44. Nicholas KB, Nicholas HB, Deerfield DW, II. 1997. GeneDoc: analysis and visualization of genetic variation. EMBNEW. News 4:14.
45. Kamerewerd J, Zadra I, Kürnsteiner H, Kück U. 2011. PcchiBI, encoding a class V chitinase, is affected by PcVelA and PcLaeA and responsible for cell wall integrity in Penicillium chrysogenum. Microbiology 157:3036-3048.
46. Stinnett SM, Espeso EA, Cobeno L, Araújo-Bazán L, Calvo AM. 2007. Aspergillus nidulans VeA subcellular localization is dependent on the importin-carrier and on light. Mol. Microbiol. 63:242-255.
47. Webster RH, Sil A. 2008. Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc. Natl. Acad. Sci. U. S. A. 105:14573-14578.
48. Wiemann P, Brown DW, Kleigrewe K, Bok JW, Keller NP, Humpf HU, Tudzynski B. 2010. FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol. Microbiol. 77:972-994.
49. 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.
50. Hortschansky P, Eisendle M, Al-Abdallah Q, Schmidt AD, Bergmann S, Thon M, Kniemeyer O, Abt B, Seeber B, Werner ER, Kato M, Brakhage AA, Haas H. 2007. Interaction of HapX with the CCAAT-binding complex-a novel mechanism of gene regulation by iron. EMBO J. 26:3157-3168.
51. Steidl S, Papagiannopoulos P, Litzka O, Andrianopoulos A, Davis MA, Brakhage AA, Hynes MJ. 1999. AnCF, the CCAAT binding complex of Aspergillus nidulans, contains products of the hapB, hapC, and hapE genes and is required for activation by the pathway-specific regulatory gene amdR. Mol. Cell. Biol. 19:99-106.
52. Caruso ML, Litzka O, Martic G, Lottspeich F, Brakhage AA. 2002. Novel basic-region helix-loop-helix transcription factor (AnBH1) of Aspergillus nidulans counteracts the CCAAT-binding complex AnCF in the promoter of a penicillin biosynthesis gene. J. Mol. Biol. 323:425-439.
53. Li Y, Su C, Mao X, Cao F, Chen J. 2007. Roles of Candida albicans Sfl1 in hyphal development. Eukaryot. Cell 6:2112-2121.
54. Berckmans B, Lammens T, Van Den Daele H, Magyar Z, Bogre L, De Veylder L. 2011. Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol. 157:1440-1451.
55. Iven T, Strathmann A, Bottner S, Zwafink T, Heinekamp T, Guivarc'h A, Roitsch T, Droge-Laser W. 2010. Homo-and heterodimers of tobacco bZIP proteins counteract as positive or negative regulators of transcription during pollen development. Plant J. 63:155-166.