NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes

Plant Cell

Volumn 18, Issue 10, 2006, Pages 2836-2853

  Oide, Shinichi ^a   Moeder, Wolfgang ^b   Krasnoff, Stuart ^c   Gibson, Donna ^c   Haas, Hubertus ^d   Yoshioka, Keiko ^b   Turgeon, B Gillian ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CROPS; IRON; METABOLISM; PATHOLOGY; VIRUSES;

ALTERNARIA BRASSICICOLA; ARABIDOPSIS THALIANA; COCHLIOBOLUS HETEROSTROPHUS; COCHLIOBOLUS MIYABEANUS;

PROTEINS;

IRON; METABOLISM; PATHOGENS; PROTEINS; RICE; VIRUSES;

ALTERNARIA; ALTERNARIA BRASSICICOLA; ARABIDOPSIS; ARABIDOPSIS THALIANA; ASCOMYCOTA; COCHLIOBOLUS; COCHLIOBOLUS HETEROSTROPHUS; COCHLIOBOLUS MIYABEANUS; GIBBERELLA ZEAE; NEUROSPORA CRASSA; ORYZA SATIVA; TRITICUM AESTIVUM; ZEA MAYS;

EID: 33750981838     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.045633     Document Type: Article

References (66)

1. Armstrong, J.E., and Baalen, V. (1979). Iron transport in microalgae: The isolation and biological activity of a hydroxamate siderophore from the blue-green alga Agmenellum quadruplicatum. J. Gen. Microbiol. 111, 253-262.
2. Bearden, S.W., and Perry, R.D. (1999). The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32, 403-414.
3. Birch, L.E., and Ruddat, M. (2005). Siderophore accumulation and phytopathogenicity in Microbotryum violaceum. Fungal Genet. Biol. 42, 579-589.
4. Bohnert, H.U., Fudal, I., Dioh, W., Tharreau, D., Notteghem, J.L., and Lebrun, M.H. (2004). A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell 16, 2499-2513.
5. Bull, C.T., Carnegie, S.R., and Loper, J.E. (1996). Pathogenicity of mutants of Erwinia carotovora subsp. carofovora deficient in aerobactin and catecholate siderophore production. Phytopathology 86, 260-266.
6. Catlett, N., Lee, B.-N., Yoder, O., and Turgeon, B. (2003). Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet. Newsl. 50, 9-11.
7. Charlang, G., Ng, B., Horowitz, N.H., and Horowitz, R.M. (1981). Cellular and extracellular siderophores of Aspergillus nidulans and Penicillium chrysogenum. Mol. Cell. Biol. 1, 94-100.
8. Chumley, F.G., and Valent, B. (1990). Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Mol. Plant Microbe Interact. 3, 135-143.
9. Cullen, D., Leong, S.A., Wilson, L.J., and Henner, D.J. (1987). Transformation of Aspergillus nidulans with the hygromycin-resistance gene, hph. Gene 57, 21-26.
10. Dellagi, A., Brisset, M.N., Paulin, J.P., and Expert, D. (1998). Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol. Plant Microbe Interact. 11, 734-742.
11. Dellagi, A., Rigault, M., Segond, D., Roux, C., Kraepiel, Y., Cellier, F., Briat, J.-F., Gaymard, F., and Expert, D. (2005). Siderophore-mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J. 43, 262-272.
12. 2 production in Ulmus pumila and Ulmus campestris cell suspension cultures inoculated with Ophiostoma novo-ulmi. Physiol. Plant. 111, 512-518.
13. Diekmann, H., and Krezdorn, E. (1975). Metabolic products of microorganisms. 150. Ferricrocin, triacetylfusigen and other sideramines from fungi of genus Aspergillus, group Fumigatus. (Author's translation.) Arch. Microbiol. 106, 191-194.
14. Edwards, K., Johnstone, C., and Thompson, C. (1991). A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349.
15. Enard, C., Diolez, A., and Expert, D. (1988). Systemic virulence of Erwinia chrysanthemi 3937 requires a functional iron assimilation system. J. Bacteriol. 170, 2419-2426.
16. Ernst, J., and Winkelmann, G. (1977). An attempt to localize iron-chelate binding sites on cytoplasmic membranes of fungi. FEMS Microbiol. Lett. 76, 71-76.
17. Fernandez, V., Winkelmann, G., and Ebert, G. (2004). Iron supply to tobacco plants through foliar application of iron citrate and ferric dimerum acid. Physiol. Plant. 122, 380-385.
18. Franza, T., Mahe, B., and Expert, D. (2005). Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55, 261-275.
19. Guillen, A., Turgeon, B.G., Thorson, P.R., Bronson, C.R., and Yoder, O.C. (1994). Linkage among melanin biosynthetic mutations in Cochliobolus heterostrophus. Fungal Genet. Newsl. 41, 41-42.
20. Haas, H. (2003). Molecular genetics of fungal siderophore biosynthesis and uptake: The role of siderophores in iron uptake and storage. Appl. Microbiol. Biotechnol. 62, 316-330.
21. Haas, H., Schoeser, M., Lesuisse, E., Ernst, J.F., Parson, W., Abt, B., Winkelmann, G., and Oberegger, H. (2003). Characterization of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem. J. 371, 505-513.
22. Hissen, A.H.T., Wan, A.N.C., Warwas, M.L., Pinto, L.J., and 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.
23. Horwitz, B.A., Sharon, A., Lu, S.W., Ritter, V., Sandrock, T.M., Yoder, O.C., and Turgeon, B.G. (1999). A G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation. Fungal Genet. Biol. 26, 19-32.
24. Hossain, M.B., Jalal, M.A.F., Benson, B.A., Barnes, C.L., and Vanderhelm, D. (1987). Structure and conformation of 2 Coprogen-type siderophores- Neocoprogen-1 and Neocoprogen-li. J. Am. Chem. Soc. 109, 4948-4954.
25. Howard, D.H. (1999). Acquisition, transport, and storage of iron by pathogenic fungi. Clin. Microbiol. Rev. 12, 394-404.
26. Howard, D.H. (2004). Iron gathering by zoopathogenic fungi. FEMS Immunol. Med. Microbiol. 40, 95-100.
27. Jalal, M., and van der Helm, D. (1989). Siderophores of highly phytopathogenic Alternaria longipes. Biol. Met. 2, 11-17.
28. Jalal, M.A., Love, S.K., and van der Helm, D. (1988). N alpha-dimethylcoprogens. Three novel trihydroxamate siderophores from pathogenic fungi. Biol. Met. 1, 4-8.
29. Jia, Y., Valent, B., and Lee, F.N. (2003). Determination of host responses to Magnaporthe grisea on detached rice leaves using a spot inoculation method. Plant Dis. 87, 129-133.
30. Johnson, R.D., Johnson, L., Itoh, Y., Kodama, M., Otani, H., and Kohmoto, K. (2000). Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol. Plant Microbe Interact. 13, 742-753.
31. Kawamura, C., Tsujimoto, T., and Tsuge, T. (1999). Targeted disruption of a melanin biosynthesis gene affects conidial development and UV tolerance in the Japanese pear pathotype of Alternaria alternata. Mol. Plant Microbe Interact. 12, 59-63.
32. Kicic, A., Chua, A.C., and Baker, E. (2001). Effect of iron chelators on proliferation and iron uptake in hepatoma cells. Cancer 92, 3093-3110.
33. Konetschny-Rapp, S., Huschka, H.G., Winkelmann, G., and Jung, G. (1988). High-performance liquid chromatography of siderophores from fungi. Biol. Met. 1, 9-17.
34. Kubo, Y., Nakamura, H., Kobayashi, K., Okuno, T., and Furusawa, I. (1991). Cloning of a melanin biosynthetic gene essential for appressorial penetration of Colletotrichum lagenarium. Mol. Plant Microbe Interact. 4, 440-445.
35. Leach, J., Lang, B.R., and Yoder, O.C. (1982). Methods for selection of mutants and in vitro culture of Cochliobolus heterostrophus. J. Gen. Microbiol. 128, 1719-1729.
36. Lee, B.-N., Kroken, S., Chou, D.Y.-T., Robbertse, B., Yoder, O.C., and Turgeon, B.G. (2005). Functional analysis of all non-ribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryot. Cell 4, 545-555.
37. Leong, S.A., and Neilands, J.B. (1981). Relationship of siderophore-mediated iron assimilation to virulence in crown gall disease. J. Bacteriol. 147, 482-491.
38. Lesuisse, E., and Labbe, P. (1994). Reductive iron assimilation in Saccftaromyces cerevisiae. In Metal Ions in Fungi, G. Winkelmann and D.R. Winge, eds (New York: Marcel Dekker), pp. 149-178.
39. Masclaux, C., and Expert, D. (1995). Signalling potential of iron in plant microbe interactions: the pathogenic switch of iron transport in Erwinia chrysanthemi. Plant J. 7, 121-128.
40. Mei, B.G., Budde, A.D., and 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.
41. Moriwaki, A., Kihara, J., Kobayashi, T., Tokunaga, T., Arase, S., and Honda, Y. (2004). Insertional mutagenesis and characterization of a polyketide synthase gene (PKS1) required for melanin biosynthesis in Bipolaris oryzae. FEMS Microbiol. Lett. 238, 1-8.
42. Neema, C., Laulhere, J.P., and Expert, D. (1993). Iron deficiency induced by Chrysobactin in Saintpaulia leaves inoculated with Erwinia chrysanthemi. Plant Physiol. 102, 967-973.
43. Neilands, J.B., and Leong, S.A. (1986). Siderophores in relation to plant growth and disease. Annu. Rev. Plant Physiol. Plant Mol. Biol. 37, 187-208.
44. Neubauer, U., Nowack, B., Furrer, G., and Schulin, R. (2000). Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environ. Sci. Technol. 34, 2749-2755.
45. Oberegger, H., Schoeser, M., Zadra, I., Abt, B., and Haas, H. (2001). SREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans. Mol. Microbiol. 41, 1077-1089.
46. Ochman, H., Gerber, A.S., and Hartl, D.L. (1988). Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621-624.
47. Ohra, J., Morita, K., Tsujino, Y., Tazaki, H., Fujimori, T., Goering, M., Evans, S., and Zorner, P. (1995). Production of the phytotoxic metabolite, ferricrocin, by the fungus Colletotrichum gloeosporioides. Biosci. Biotechnol. Biochem. 59, 113-114.
48. Panaccione, D.G., Scott-Craig, J.S., Pocard, J.A., and Walton, J.D. (1992). A cyclic peptide synthetase gene required for pathogenicity of the fungus Cochliobolus carbonum on maize. Proc. Natl. Acad. Sci. USA 89, 6590-6594.
49. Perpetua, N.S., Kubo, Y., Yasuda, N., Takano, Y., and Furusawa, I. (1996). Cloning and characterization of a melanin biosynthetic THR1 reductase gene essential for appressorial penetration of Colletotrichum lagenarium. Mol. Plant Microbe Interact. 9, 323-329.
50. Pritsch, C., Vance, C.P., Bushnell, W.R., Somers, D.A., Hohn, T.M., and Muehlbauer, G.J. (2001). Systemic expression of defense response genes in wheat spikes as a response to Fusarium graminearum infection. Physiol. Mol. Plant Pathol. 58, 1-12.
51. Renshaw, J., Robson, G., Trinci, P., Wiebe, M., Livens, F., Collison, D., and Taylor, R. (2002). Fungal siderophores: Structures, functions and applications. Mycol. Res. 106, 1123-1142.
52. Schrettl, M., Bignell, E., Kragl, C., Joechl, C., Rogers, T., Arst, H.N., Jr., Haynes, K., and Haas, H. (2004). Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J. Exp. Med. 200, 1213-1219.
53. Simonart, T., Degraef, C., Stordeur, P., Noel, J.C., Mosselmans, R., Van Vooren, J.P., Parent, D., Boelaert, J.R., Heenen, M., and Galand, P. (2001). Iron induces Bcl-2 expression in human dermal microvascular endothelial cells. Free Radic. Res. 34, 221-235.
54. Sokolovsky, V., Kaldenhoff, R., Ricci, M., and Russo, V.E.A. (1990). Fast and reliable mini-prep RNA extraction from Neurospora crassa. Fungal Genet. Newsl. 37, 41.
55. Subramoni, S., and Sonti, R.V. (2005). Growth deficiency of a Xanthomonas oryzae pv. oryzae fur mutant in rice leaves is rescued by ascorbic acid supplementation. Mol. Plant Microbe Interact. 18, 644-651.
56. Takase, H., Nitanai, H., Hoshino, K., and Otani, T. (2000). Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68, 1834-1839.
57. Tzeng, T.H., Lyngholm, L.K., Ford, C.F., and Bronson, C.R. (1992). A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 130, 81-96.
58. 2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiol. 123, 1289-1300.
59. Voigt, C.A., Schafer, W., and Salomon, S. (2005). A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42, 364-375.
60. Walton, J.D. (1996). Host-selective toxins: Agents of compatibility. Plant Cell 8, 1723-1733.
61. Weinberg, E.D. (2000). Modulation of intramacrophage: iron metabolism during microbial cell invasion. Microbes Infect. 2, 85-89.
62. Welzel, K., Eisfeld, K., Antelo, L., Anke, T., and Anke, H. (2005). Characterization of the ferrichrome A biosynthetic gene cluster in the homobasidiomycete Omphalotus olearius. FEMS Microbiol. Lett. 249, 157-163.
63. Winkelmann, G. (1991). Importance of siderophores in fungal growth, sporulation and spore germination. In Frontiers in Mycology, D.L. Hawksworth, ed (Wallingford, UK: CAB International), pp. 49-65.
64. Winkelmann, G., and Huschka, H. (1987). Molecular recognition and transport of siderophores in fungi. In Iron Transport in Microbes, Plants and Animals, G. Winkelmann, D. van der Helm, and J.B. Neilands, eds (Weinheim, Germany: VCH), pp. 317-336.
65. Yamada, O., Na Nan, S., Akao, T., Tominaga, M., Watanabe, H., Satoh, T., Enei, H., and Akita, O. (2003). dffA gene from Aspergillus oryzae encodes L-ornithine N5-oxygenase and is indispensable for deferriferrichrysin biosynthesis. J. Biosci. Bioeng. 95, 82-88.
66. Yuan, W.M., Gentil, G.D., Budde, A.D., and 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.