The regulatory factor PcRFX1 controls the expression of the three genes of β-lactam biosynthesis in Penicillium chrysogenum

Fungal Genetics and Biology

Volumn 49, Issue 11, 2012, Pages 866-881

  Domínguez Santos, Rebeca ^a   Martín, Juan Francisco ^a   Kosalková, Katarina ^b   Prieto, Carlos ^b   Ullán, Ricardo V ^b   García Estrada, Carlos ^b  

^a UNIVERSITY OF LEÓN   (Spain)

^b Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

Author keywords

Development; Morphology; Penicillin biosynthesis; Regulation; Sporulation; Winged helix transcription factor

Indexed keywords

BETA LACTAM; CPCR1 PROTEIN; PCRFX1 PROTEIN; PENICILLIN G; REGULATOR PROTEIN; RFXA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CEPHALOSPORIUM ACREMONIUM; CONTROLLED STUDY; DNA BINDING; FUNGAL GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SEQUENCE; GENE SILENCING; GENOME ANALYSIS; NONHUMAN; PCBAB GENE; PCBC GENE; PCRFX1 GENE; PENDE GENE; PENICILLIUM CHRYSOGENUM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MOTIF; REPORTER GENE; SPOROGENESIS; TRANSCRIPTION REGULATION;

ACYLTRANSFERASES; BASE SEQUENCE; BETA-LACTAMS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PENICILLIN-BINDING PROTEINS; PENICILLIUM CHRYSOGENUM; PEPTIDE SYNTHASES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

ACREMONIUM CHRYSOGENUM; FUNGI; PENICILLIUM CHRYSOGENUM; PENICILLIUM MARNEFFEI;

EID: 84867910216     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.08.002     Document Type: Article

References (48)

1. Aharonowitz Y., Cohen G., Martín J.F. Penicillin and cephalosporin biosynthetic genes: structure, regulation, and evolution. Annu. Rev. Microbiol. 1992, 46:461-495.
2. Barreiro C., Martín J.F., García-Estrada C. Proteomics shows new faces for the old penicillin producer Penicillium chrysogenum. J. Biomed. Biotechnol. 2012, 2012:105109.
3. Bergh K.T., Litzka O., Brakhage A.A. Identification of a major cis-acting DNA element controlling the bidirectionally transcribed penicillin biosynthesis genes acvA (pcbAB) and ipnA (pcbC) of Aspergillus nidulans. J. Bacteriol. 1996, 178:3908-3916.
4. Bok J.W., Keller N.P. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot. Cell 2004, 3:527-535.
5. Brakhage A.A., Spröte P., Al-Abdallah Q., Gehrke A., Plattner H., Tüncher A. Regulation of penicillin biosynthesis in filamentous fungi. Adv. Biochem. Eng. Biotechnol. 2004, 88:45-90.
6. Bugeja H.E., Hynes M.J., Andrianopoulos A. The RFX protein RfxA is an essential regulator of growth and morphogenesis in Penicillium marneffei. Eukaryot. Cell 2010, 9:578-591.
7. Cantoral J.M., Díez B., Barredo J.L., álvarez E., Martín J.F. High frequency transformation of Penicillium chrysogenum. Bio/Technology 1987, 5:494-497.
8. Cantoral J.M., Gutiérrez S., Fierro F., Gil-Espinosa S., van Liempt H., Martín J.F. Biochemical characterization and molecular genetics of nine mutants of Penicillium chrysogenum impaired in penicillin biosynthesis. J. Biol. Chem. 1993, 268:737-744.
9. Casqueiro J., Bañuelos O., Gutiérrez S., Hijarrubia M.J., Martín J.F. Intrachromosomal recombination between direct repeats in Penicillium chrysogenum: gene conversion and deletion events. Mol. Gen. Genet. 1999, 261:994-1000.
10. Chang L.T., McGrory E.L., Elander R.P. Penicillin production by glucose-derepressed mutants of Penicillium chrysogenum. J. Ind. Microbiol. 1990, 6:165-169.
11. Chu Y.W., Renno D., Saunders G. Detection of a protein which binds specifically to the upstream region of the pcbAB gene in Penicillium chrysogenum. Curr. Genet. 1995, 28:184-186.
12. Dimmer E.C., Huntley R.P., Alam-Faruque Y., Sawford T., O'Donovan C., Martin M.J., Bely B., Browne P., Mun Chan W., Eberhardt R., Gardner M., Laiho K., Legge D., Magrane M., Pichler K., Poggioli D., Sehra H., Auchincloss A., Axelsen K., Blatter M.C., Boutet E., Braconi-Quintaje S., Breuza L., Bridge A., Coudert E., Estreicher A., Famiglietti L., Ferro-Rojas S., Feuermann M., Gos A., Gruaz-Gumowski N., Hinz U., Hulo C., James J., Jimenez S., Jungo F., Keller G., Lemercier P., Lieberherr D., Masson P., Moinat M., Pedruzzi I., Poux S., Rivoire C., Roechert B., Schneider M., Stutz A., Sundaram S., Tognolli M., Bougueleret L., Argoud-Puy G., Cusin I., Duek-Roggli P., Xenarios I., Apweiler R. The UniProt-GO annotation database in 2011. Nucl.Acids Res. 2012, 40(Database issue):D565-D570.
13. Dreyer J., Eichhorn H., Friedlin E., Kürnsteiner H., Kück U. A homologue of the Aspergillus velvet gene regulates both cephalosporin C biosynthesis and hyphal fragmentation in Acremonium chrysogenum. Appl. Environ. Microbiol. 2007, 73:3412-3422.
14. Emery P., Durand B., Mach B., Reith W. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucl. Acids Res. 1996, 24:803-807.
15. Espeso E.A., Tilburn J., Arst H.N., Peñalva M.A. PH regulation is a major determinant in expression of a fungal penicillin biosynthetic gene. EMBO J. 1993, 12:3947-3956.
16. Feng B., Friedlin E., Marzluf G.A. A reporter gene analysis of penicillin biosynthesis gene expression in Penicillium chrysogenum and its regulation by nitrogen and glucose catabolite repression. Appl. Environ. Microbiol. 1994, 60:4432-4439.
17. Feng B., Friedlin E., Marzluf G.A. Nuclear DNA-binding proteins which recognize the intergenic control region of penicillin biosynthetic genes. Curr. Genet. 1995, 27:351-358.
18. Fernández F.J., Cardoza R.E., Montenegro E., Velasco J., Gutiérrez S., Martín J.F. The isopenicillin N acyltransferases of Aspergillus nidulans and Penicillium chrysogenum differ in their ability to maintain the 40-kDa alphabeta heterodimer in an undissociated form. Eur. J. Biochem. 2003, 270:1958-1968.
19. Fierro F., Barredo J.L., Díez B., Gutiérrez S., Fernández F.J., Martín J.F. The penicillin gene cluster is amplified in tandem repeats linked by conserved hexanucleotide sequences. Proc. Natl. Acad. Sci. USA 1995, 92:6200-6204.
20. Fierro F., García-Estrada C., Castillo N.I., Rodríguez R., Velasco-Conde T., Martín J.F. Transcriptional and bioinformatic analysis of the 56.8 kb DNA region amplified in tandem repeats containing the penicillin gene cluster in Penicillium chrysogenum. Fungal Genet. Biol. 2006, 43:618-629.
21. Gajiwala K.S., Chen H., Cornille F., Roques B.P., Reith W., Mach B., Burley S.K. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 2000, 403:916-921.
22. García-Estrada C., Vaca I., Lamas-Maceiras M., Martín J.F. In vivo transport of the intermediates of the penicillin biosynthetic pathway in tailored strains of Penicillium chrysogenum. Appl. Microbiol. Biotechnol. 2007, 76:169-182.
23. García-Estrada C., Ullán R.V., Velasco-Conde T., Godio R.P., Teijeira F., Vaca I., Feltrer R., Kosalková K., Mauriz E., Martín J.F. Post-translational enzyme modification by the phosphopantetheinyl transferase is required for lysine and penicillin biosynthesis but not for roquefortine or fatty acid formation in Penicillium chrysogenum. Biochem. J. 2008, 415:317-324.
24. C103S of the isopenicillin N acyltransferase is transported inside peroxisomes and regulates its self-processing. Fungal Genet. Biol. 2008, 45:1043-1052.
25. Gutiérrez S., Marcos A.T., Casqueiro J., Kosalková K., Fernández F.J., Velasco J., Martín J.F. Transcription of the pcbAB, pcbC and penDE genes of Penicillium chrysogenum AS-P-78 is repressed by glucose and the repression is not reversed by alkaline pHs. Microbiology 1999, 145:317-324.
26. Haas H., Marzluf G.A. NRE, the major nitrogen regulatory protein of Penicillium chrysogenum, binds specifically to elements in the intergenic promoter regions of nitrate assimilation and penicillin biosynthetic gene clusters. Curr. Genet. 1995, 28:177-183.
27. Haas H., Bauer B., Redl B., Stoffler G., Marzluf G.A. Molecular cloning and analysis of nre, the major nitrogen regulatory gene of Penicillium chrysogenum. Curr. Genet. 1995, 27:150-158.
28. Hoff B., Kück U. Use of bimolecular fluorescence complementation to demonstrate transcription factor interaction in nuclei of living cells from the filamentous fungus Acremonium chrysogenum. Curr. Genet. 2005, 47:132-138.
29. Hoff B., Schmitt E.K., Kück U. CPCR1, but not its interacting transcription factor AcFKH1, controls fungal arthrospore formation in Acremonium chrysogenum. Mol. Microbiol. 2005, 56:1220-1233.
30. Hoff B., Kamerewerd J., Sigl C., Mitterbauer R., Zadra I., Kürnsteiner H., Kück U. Two components of a velvet-like complex control hyphal morphogenesis, conidiophore development, and penicillin biosynthesis in Penicillium chrysogenum. Eukaryot. Cell 2010, 9:1236-1250.
31. Jami M.S., Barreiro C., García-Estrada C., Martín J.F. Proteome analysis of the penicillin producer Penicillium chrysogenum: characterization of protein changes during the industrial strain improvement. Mol. Cell. Proteomics 2010, 9:1182-1198.
32. Kosalková K., Marcos A.T., Fierro F., Hernando-Rico V., Gutiérrez S., Martin J.F. A novel heptameric sequence (TTAGTAA) is the binding site for a protein required for high level expression of pcbAB, the first gene of the penicillin biosynthesis in Penicillium chrysogenum. J. Biol. Chem. 2000, 275:2423-2430.
33. Kosalková K., García-Estrada C., Ullán R.V., Godio R.P., Feltrer R., Teijeira F., Mauriz E., Martín J.F. The global regulator LaeA controls penicillin biosynthesis, pigmentation and sporulation, but not roquefortine C synthesis in Penicillium chrysogenum. Biochimie 2009, 91:214-225.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
35. Martín J.F. Molecular control of expression of penicillin biosynthesis genes in fungi: regulatory proteins interact with a bi-directional promoter region. J. Bacteriol. 2000, 182:2355-2362.
36. Martín J.F., Casqueiro J., Kosalková K., Marcos A.T., Gutiérrez S. Penicillin and cephalosporin biosynthesis: mechanism of carbon catabolite regulation of penicillin production. Antonie van Leeuwenhoek 1999, 75:21-31.
37. Martín J.F., Ullán R.V., García-Estrada C. Regulation and compartmentalization of β-lactam biosynthesis. Microb. Biotechnol. 2010, 3:285-299.
38. Raper K.B., Alexander D.F., Coghill R.D. Penicillin. II. Natural variation and penicillin production in Penicillium notatum and allied species. J. Bacteriol. 1944, 48:639-659.
39. Schmitt E.K., Kück U. The fungal CPCR1 protein, which binds specifically to beta-lactam biosynthesis genes, is related to human regulatory factor X transcription factors. J. Biol. Chem. 2000, 275:9348-9357.
40. Schmitt E.K., Hoff B., Kück U. AcFKH1, a novel member of the forkhead family, associates with the RFX transcription factor CPCR1 in the cephalosporin C-producing fungus Acremonium chrysogenum. Gene 2004, 342:269-281.
41. Schmitt E.K., Bunse A., Janus D., Hoff B., Friedlin E., Kürnsteiner H., Kück U. Winged helix transcription factor CPCR1 is involved in regulation of beta-lactam biosynthesis in the fungus Acremonium chrysogenum. Eukaryot. Cell 2004, 3:121-134.
42. Spröte P., Brakhage A.A. The light-dependent regulator velvet A of Aspergillus nidulans acts as a repressor of the penicillin biosynthesis. Arch. Microbiol. 2007, 188:69-79.
43. Suárez T., Peñalva M.A. Characterization of a Penicillium chrysogenum gene encoding a PacC transcription factor and its binding sites in the divergent pcbAB-pcbC promoter of the penicillin biosynthetic cluster. Mol. Microbiol. 1996, 20:529-540.
44. Ullán R.V., Godio R.P., Teijeira F., Vaca I., García-Estrada C., Feltrer R., Kosalkova K., Martín J.F. RNA-silencing in Penicillium chrysogenum and Acremonium chrysogenum: validation studies using beta-lactam genes expression. J. Microbiol. Methods 2008, 75:209-218.
45. van den Berg M.A. Impact of the Penicillium chrysogenum genome on industrial production of metabolites. Appl. Microbiol. Biotechnol. 2011, 92:45-53.
46. van den Berg M.A., Westerlaken I., Leeflang C., Kerkman R., Bovenberg R.A. Functional characterization of the penicillin biosynthetic gene cluster of Penicillium chrysogenum Wisconsin54-1255. Fungal Genet. Biol. 2007, 44:830-844.
47. van den Berg M.A., Albang R., Albermann K., Badger J.H., Daran J.M., Driessen A.J., Garcia-Estrada C., Fedorova N.D., Harris D.M., Heijne W.H., Joardar V., Kiel J.A., Kovalchuk A., Martín J.F., Nierman W.C., Nijland J.G., Pronk J.T., Roubos J.A., van der Klei I.J., van Peij N.N., Veenhuis M., von Döhren H., Wagner C., Wortman J., Bovenberg R.A.L. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nature Biotechnol. 2008, 26:1161-1168.
48. Yan T., Yoo D., Berardini T.Z., Mueller L.A., Weems D.C., Weng S., Cherry J.M., Rhee S.Y. PatMatch: a program for finding patterns in peptide and nucleotide sequences. Nucl.Acids Res. 2005, 33(Web Server issue):W262-W266.