Elucidation of the complete ferrichrome a biosynthetic pathway in Ustilago maydis

Molecular Microbiology

Volumn 75, Issue 5, 2010, Pages 1260-1271

  Winterberg, Britta ^a,c   Uhlmann, Stefanie ^a,b   Linne, Uwe ^b   Lessing, Franziska ^a,d   Marahiel, Mohamed A ^b   Eichhorn, Heiko ^a,e   Kahmann, Regine ^a   Schirawski, Jan ^a,f  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e NOVARTIS PHARMA AG   (Switzerland)

^f UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; ENOYL COENZYME A HYDRATASE; FER3 ENZYME; FER4 ENZYME; FER5 ENZYME; FERRICHROME; HYDROXYMETHYLGLUTARYL COENZYME A SYNTHASE; IRON; PEPTIDE SYNTHASE; SIDEROPHORE; UNCLASSIFIED DRUG; 3-HYDROXY-3-METHYLGLUTARYL-COENZYME A; ACYL COENZYME A; FUNGAL PROTEIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; RECOMBINANT PROTEIN;

ARTICLE; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; USTILAGO MAYDIS; ANALOGS AND DERIVATIVES; BIOLOGICAL MODEL; BIOSYNTHESIS; CHEMICAL STRUCTURE; FUNGAL GENE; GENE DELETION; GENE EXPRESSION; GENE ORDER; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MOLECULAR CLONING; USTILAGO;

USTILAGO MAYDIS;

ACYL COENZYME A; AMIDOHYDROLASES; BIOSYNTHETIC PATHWAYS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLONING, MOLECULAR; ENOYL-COA HYDRATASE; FERRICHROME; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION; GENE ORDER; GENES, FUNGAL; HYDROXYMETHYLGLUTARYL-COA SYNTHASE; MASS SPECTROMETRY; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PEPTIDE SYNTHASES; RECOMBINANT PROTEINS; USTILAGO;

EID: 77349109110     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07048.x     Document Type: Article

References (42)

1. An, Z., Mei, B., Yuan, W.M. Leong, S.A. (1997a) The distal GATA sequences of the sid1 promoter of Ustilago maydis mediate iron repression of siderophore production and interact directly with Urbs1, a GATA family transcription factor. EMBO J 16 : 1742 1750.
2. An, Z., Zhao, Q., McEvoy, J., Yuan, W.M., Markley, J.L. Leong, S.A. (1997b) The second finger of Urbs1 is required for iron-mediated repression of sid1 in Ustilago maydis. Proc Natl Acad Sci USA 94 : 5882 5887.
3. Banuett, F. Herskowitz, I. (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 86 : 5878 5882.
4. Bottin, A., Kämper, J. Kahmann, R. (1996) Isolation of a carbon source-regulated gene from Ustilago maydis. Mol Gen Genet 253 : 342 352.
5. Brachmann, A., König, J., Julius, C. Feldbrügge, M. (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272 : 216 226.
6. Bushley, K.E., Ripoll, D.R. Turgeon, B.G. (2008) Module evolution and substrate specificity of fungal nonribosomal peptide synthetases involved in siderophore biosynthesis. BMC Evol Biol 8 : 328.
7. Eichhorn, H., Lessing, F., Winterberg, B., Schirawski, J., Kämper, J., Müller, P. Kahmann, R. (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18 : 3332 3345.
8. Emery, T.F. (1966) Initial steps in the biosynthesis of ferrichrome. Incorporation of Δ-N-hydroxyornithine and Δ-N-acetyl-Δ-N- hydroxyornithine. Biochem 5 : 3694 3701.
9. Finking, R. Marahiel, M.A. (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 58 : 453 488.
10. Grunler, J., Ericsson, J. Dallner, G. (1994) Branch-point reactions in the biosynthesis of cholesterol, dolichol, ubiquinone and prenylated proteins. Biochim Biophys Acta 1212 : 259 277.
11. Haas, H., Eisendle, M. Turgeon, B. (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46 : 149 187.
12. van der Helm, D. Winkelmann, G. (1994) Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi. In Metal Ions in Fungi. Winkelmann, G. Winge, D. (eds). New York : Marcel Dekker, pp. 39 98.
13. Hissen, A.H., Wan, A.N., Warwas, M.L., Pinto, L.J. Moore, M.M. (2005) The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence. Infect Immun 73 : 5493 5503.
14. Hoffman, C.S. Winston, F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57 : 267 272.
15. Holliday, R. (1974) Ustilago maydis. In Handbook of Genetics, Vol. 1. King, R. (ed.). New York : Plenum Press, pp. 575 595.
16. Kämper, J. (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271 : 103 110.
17. Lankford, C. (1973) Bacterial assimilation of iron. Crit Rev Microbiol 2 : 273 331.
18. Lazardi, K., Urbina, J.A. de Souza, W. (1990) Ultrastructural alterations induced by two ergosterol biosynthesis inhibitors, ketoconazole and terbinafine, on epimastigotes and amastigotes of Trypanosoma (Schizotrypanum) cruzi. Antimicrob Agents Chemother 34 : 2097 2105.
19. Lee, T., Johnson, L., Johnson, R., Koulman, A., Lane, G., Lott, J. Arcus, V. (2009) The structure of a eukaryotic non-ribosomal peptide synthetase adenylation domain which activates a large hydroxamate amino acid in siderophore biosynthesis. J Biol Chem (in press). doi:10.1074/jbc.M109.071324.
20. Lin, Y.-M. Miller, M.J. (1999) Practical synthesis of hydroxamate-derived siderophore components by an indirect oxidation method and syntheses of a DIG-siderophore conjugate and a biotin-siderophore conjugate. J Org Chem 64 : 7451 7458.
21. Mei, B., Budde, A.D. Leong, S.A. (1993) sid1, a gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron, and role in phytopathogenicity. Proc Natl Acad Sci USA 90 : 903 907.
22. Miethke, M. Marahiel, M.A. (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71 : 413 451.
23. Oide, S., Moeder, W., Krasnoff, S., Gibson, D., Haas, H., Yoshioka, K. Turgeon, B.G. (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18 : 2836 2853.
24. Oide, S., Krasnoff, S.B., Gibson, D.M. Turgeon, B.G. (2007) Intracellular siderophores are essential for ascomycete sexual development in heterothallic Cochliobolus heterostrophus and homothallic Gibberella zeae. Eukaryot Cell 6 : 1339 1353.
25. Payne, S.M. (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol 235 : 1634 1642.
26. Reineke, G., Heinze, B., Schirawski, J., Buettner, H., Kahmann, R. Basse, C.W. (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9 : 339 355.
27. Sambrook, J., Frisch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York : Cold Spring Harbor Laboratory Press.
28. Schrettl, M., Bignell, E., Kragl, C., Joechl, C., Rogers, T., Arst, H.N., Jr., et al. (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200 : 1213 1219.
29. Schrettl, M., Bignell, E., Kragl, C., Sabiha, Y., Loss, O., Eisendle, M., et al. (2007) Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PloS Pathog 3 : 1195 1207.
30. Schrettl, M., Kim, H.S., Eisendle, M., Kragl, C., Nierman, W.C., Heinekamp, T., et al. (2008) SreA-mediated iron regulation in Aspergillus fumigatus. Mol Microbiol 70 : 27 43.
31. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., et al. (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60 : 295 306.
32. Schwecke, T., Gottling, K., Durek, P., Duenas, I., Kaufer, N.F., Zock-Emmenthal, S., et al. (2006) Nonribosomal peptide synthesis in Schizosaccharomyces pombe and the architectures of ferrichrome-type siderophore synthetases in fungi. Chembiochem 7 : 612 622.
33. Schwyn, B. Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160 : 47 56.
34. Servouse, M. Karst, F. (1986) Regulation of early enzymes of ergosterol biosynthesis in Saccharomyces cerevisiae. Biochem J 240 : 541 547.
35. Teichmann, B., Linne, U., Hewald, S., Marahiel, M.A. Bölker, M. (2007) A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66 : 525 533.
36. Voisard, C., Wang, J., McEvoy, J.L., Xu, P. Leong, S.A. (1993) urbs1, a gene regulating siderophore biosynthesis in Ustilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. Mol Cell Biol 13 : 7091 7100.
37. Wang, J., Budde, A.D. Leong, S.A. (1989) Analysis of ferrichrome biosynthesis in the phytopathogenic fungus Ustilago maydis: cloning of an ornithine-N5-oxygenase gene. J Bacteriol 171 : 2811 2818.
38. Welzel, K., Eisfeld, K., Antelo, L., Anke, T. Anke, H. (2005) Characterization of the ferrichrome A biosynthetic gene cluster in the homobasidiomycete Omphalotus olearius. FEMS Microbiol Lett 249 : 157 163.
39. Winkelmann, G. (2007) Ecology of siderophores with special reference to the fungi. Biometals 20 : 379 392.
40. Yuan, W.M., Gentil, G.D., Budde, A.D. Leong, S.A. (2001) Characterization of the Ustilago maydis sid2 gene, encoding a multidomain peptide synthetase in the ferrichrome biosynthetic gene cluster. J Bacteriol 183 : 4040 4051.
41. Zdobnov, E.M. Apweiler, R. (2001) InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17 : 847 848.
42. Zuther, K., Mayser, P., Hettwer, U., Wu, W., Spiteller, P., Kindler, B.L., et al. (2008) The tryptophan aminotransferase Tam1 catalyses the single biosynthetic step for tryptophan-dependent pigment synthesis in Ustilago maydis. Mol Microbiol 68 : 152 172.