Sfp-type 4'-phosphopantetheinyl transferase is indispensable for fungal pathogenicity

Plant Cell

Volumn 21, Issue 10, 2009, Pages 3379-3396

  Horbach, Ralf ^a,b   Graf, Alexander ^a,f   Weihmann, Fabian ^a   Antelo, Luis ^b   Mathea, Sebastian ^c   Liermann, Johannes C ^d   Opatz, Till ^d   Thines, Eckhard ^b   Aguirre, Jesús ^e   Deising, Holger B ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b Institut für Biotechnologie and Wirkstoff Forschung IBWF   (Germany)

^c MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

^d UNIVERSITY OF HAMBURG   (Germany)

^e INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^f NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLETOTRICHUM; FUNGI; GLOMERELLA GRAMINICOLA; MAGNAPORTHE; ZEA MAYS;

EID: 72049128860     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.064188     Document Type: Article

References (77)

1. Antelo, L., Hof, C., Welzel, K., Eisfeld, K., Sterner, O., and Anke, H. (2006). Siderophores produced by Magnaporthe grísea in the presence and absence of iron. Z. Naturforsch. C 61: 461-464.
2. Baker, S.E., Kroken, S., Inderbitzin, P., Asvarak, T., Li, B.Y., Shi, L., Yoder, O.C., and Turgeon, B.G. (2006). Two polyketide synthaseeneoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol. Plant Microbe Interact. 19: 139-149.
3. Bechinger,C.,Giebel,K.-F.,Schnell,M.,Leiderer,P.,Deising,H.B., andBastmeyer,M.(1999). Opticalmeasurementsofinvasiveforcesexertedbyappressoriaofaplantpathogenicfungus. Science285:1896-1899.(Pubitemid129515506)
4. Becker, D.M., and Lundblad, V. (2001). Introduction of DNA into yeast cells. In Current Protocols in Molecular Biology, F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds (New York: John Wiley & Sons), pp. 13.17.11-13.17.10.
5. Bergstrom, G.C., and Nicholson, R.L. (1999). The biology of corn anthracnose. Knowledge to exploit for improved management. Plant Dis. 83: 596-608.
6. Birren, B., Fink, G., and Lander, E. (2002). Fungal Genome Initiative: White Paper Developed by the Fungal Research Community. (Cambridge, MA: Whitehead Institute Center for Genome Research).
7. Brown, T. (1999). Southern blotting. In Current Protocols in Molecular Biology, F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds (New York: John Wiley & Sons), pp. 2.9.1-2.9.15.
8. Chapman, D.J., and Leech, R.M. (1979). Changes in pool sizes of free amino-aeids and amines in leaves and plastids of Zea mays during leaf development. Plant Physiol. 63: 567-572.
9. Chirgwin, J.M., Przybyla, A.E., MacDonald, R.J., and Rutter, W.J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294-5299.
10. Collemare, J., Billard, A., Bohnert, H.U., and Lebrun, M.H. (2008). Biosynthesis of secondary metabolites in the rice blast fungus Magnaporthe grisea: The role of hybrid PKS-NRPS in pathogenicity. Mycol. Res. 112: 207-215.
11. Dean, R.A., et al. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980-986.
12. Deising, H.B., Werner, S., and Wernitz, M. (2000). The role of fungal appressoria in plant infection. Microbes Infect. 2: 1631-1641. (Pubitemid 30943288)
13. De Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997). Glycerol generates turgor In rice blast. Nature 389: 244-245. (Pubitemid 27406629)
14. de Neergaard, E. (1997). Methods in Botanical Histopathology. (Copenhagen, Denmark: Kandrups Bogtrykkeri).
15. Desjardins, A.E., Manandhar, G., Plattner, R.D., Maragos, C.M., Shrestha, K., and McCormick, S.P. (2000). Occurrence of Fusarium species and mycotoxins in nepalese maize and wheat and the effect of traditional processing methods on mycotoxin levels. J. Agrie. Food Chem. 48: 1377-1383.
16. Döbbeling,U.,Böni,R.,Häffner,A.,Dummer,R.,andBurg,G.(1997) .MethodforsimultaneousRNAandDNAisolationfrombiopsymaterial,culturecells, plantsandbacteria.Biotechniques22:88-90.(Pubitemid27036421)
17. Ehmann, D.E., Gehring, A.M., and Walsh, C.T. (1999). Lysine biosynthesis in Saccharomyces cerevisiae: Mechanism of alphaamlnoadipate reductase (Lys2) involves posttranslational phosphopantetheinylation by Lys5. Biochemistry 38: 6171-6177.
18. Eichhorn, H., Lessing, F., Winterberg, B., Schirawski, J., Kämper, J., Müller, P., and Kahmann, R. (2006). A ferroxldation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18: 3332-3345. (Pubitemid 46013294)
19. Fichtischerer, F., Wellein, C., Mittag, M., and Schweizer, E. (2000). A novel function of yeast fatty acid synthase. Subunit alpha is capable of self-pantetheinylation. Eur. J. Biochem. 267: 2666-2671.
20. Fudal, I., Collemare, J., Böhnert, H.U., Melayah, D., and Lebrun, M.H. (2007). Expression of Magnaporthe grisea avirulence gene ACE1 is connected to the Initiation of appressorium-mediated penetration. Eukaryot. Cell 6: 546-554.
21. Fuganti, C., Mendozza, M., Joulain, D., Minut, J., Pedrocchi-Fantoni, G., Piergianni, V., Servi, S., and Zucchi, G. (1996). Biogeneration and biodegradation of raspberry ketone in the fungus Beauveria bassiana. J. Agrie. Food Chem. 44: 3616-3617.
22. Gay, A., Zimmermann, G., Nowara, D., Kumlehn, J., Schweizer, P., and Hensel, G. (2008). Triple RNAi constructs for broad-range resistance against fungal leaf diseases. Book of Abstracts, 9th Inter-national Congress of Plant Pathology 2008, Torino, Italy. J. Plant Pathol. 90 (suppl.), 267-268.
23. Greenshields, D.L., Liu, G., Feng, J., Selvara, J., G., and Wei, Y. (2007). The siderophore biosynthetic gene SID1, but not the ferroxldase gene FET3, is required for full Fusarium graminearum virulence. Mol. Plant Pathol. 8:411-421.
24. Guzmán-de-Peña, D., Aguirre, J-, and Ruiz-Herrera, J. (1998). Cor-relation between the regulation of sterigmatocystin biosynthesis and asexual and sexual sporulation in Emericella nidulans. Antonie Van Leeuwenhoek 73: 199-205. (Pubitemid 28375468)
25. Haas, H., Eisendle, M., and Turgeon, B.G. (2008). Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46: 149-187.
26. Han, Y.-J., and Han, D.-M. (1993). Isolation and characterization of null pigment mutant in Aspergillus nidulans. Korean J. Genet. 15: 1-10.
27. Henson, J.M., Butler, M.J., and Day, A.W. (1999). The dark side of the mycelium: Melanins of phytopathogenic fungi. Annu. Rev. Phytopa-thol. 37: 447-471.
28. Hof, C., Eisfeld, K., Welzel, K., Antelo, L., Foster, A.J., and Anke, H. (2007). Ferricrocin synthesis in Magnaporthe grisea and its role in pathogenicity in rice. Mol. Plant Pathol. 8: 163-172.
29. Howard, R.J., and Ferrari, M.A. (1989). Role of melanin in appresso-rlum function. Exp. Mycol. 13: 403-418.
30. Howard, R.J., Ferrari, M.A., Roach, D.H., and Money, N.P. (1991). Penetration of hard substances by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. USA 88: 11281-11284.
31. Keszenman-Pereyra, D., Lawrence, S., Twfieg, M.E., Price, J., and Turner, G. (2003). The npgA/cfwA gene encodes a putative 4'-phosphopantetheinyl transferase which is essential for penicillin biosynthesis in Aspergillus nidulans. Curr. Genet. 43: 186-190.
32. Kopecká, M., and Gabriel, M. (1995). Actin cortical cytoskeleton and cell wall synthesis in regenerating protoplasts of the Saccharomyces cerevisiea actin mutant DBY 1693. Microbiology 141: 1289-1299.
33. Krijger, J.-J., Horbach, R., Behr, M., Schweizer, P., Deising, H.B., and Wirsel, S.G.R. (2008). The yeast signal sequence trap identifies secreted proteins of the hemibiotrophic corn pathogen Colletotrichum graminicola. Mol. Plant Microbe Interact. 21: 1325-1336.
34. Kroken, S., Glass, N.L., Taylor, J.W., Yoder, O.C., and Turgeon, B.G. (2003). Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc. Natl. Acad. Sci. USA 100: 15670-15675.
35. Küster, S., Ludwig, N., Willers, G., Hoffmann, J., Deising, H.B., and Kiesow, A. (2008). Thin PTFE-like membranes allow characterizing germination and mechanical penetration competence of pathogenic fungi. Acta Biomater. 4: 1809-1818.
36. Langfelder, K., Streibel, M., Jahn, B., Haase, G., and Brakhage, A.A. (2003). Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet. Biol. 38: 143-158.
37. Lee, B.N., Kroken, S., Chou, D.Y., Robbertse, B., Yoder, O.C., and Turgeon, B.G. (2005). Functional analysis of all nonribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryot. Cell 4: 545-555.
38. Liebmann, B., Mühleisen, T.W., Müller, M., Hecht, M., Weidner, G., Braun, A., Brock, M., and Brakhage, A.A. (2004). Deletion of the Aspergillus fumigatus lysine biosynthesis gene lysF encoding homo-aconitase leads to attenuated virulence in a low-dose mouse infection model of invasive aspergillosis. Arch. Microbiol. 181: 378-383.
39. Liu, X., and Baird, W.V. (2001). Rapid amplification of genomic DNA ends by NlaIII partial digestion and polynucleotide tailing. Plant Mol. Biol. Rep. 19: 261-267.
40. Lu, S., Lyngholm, L., Yang, G., Bronson, C., Yoder, O.C., and Turgeon, B.G. (1994). Tagged mutations at the Tox1 locus of Cochliobolus heterostrophus by restriction enzyme-mediated integra-tion. Proc. Natl. Acad. Sci. USA 91: 12649-12653.
41. Manning, V.A., Hardison, L.K., and Ciuffetti, L.M. (2007). Ptr ToxA interacts with a chloroplast-localized protein. Mol. Plant Microbe Interact. 20: 168-177.
42. Marquez-Fernandez, O., Trigos, A., Ramos-Balderas, J.L., Viniegra-Gonzalez, G., Deising, H.B., and Aguirre, J. (2007). Phosphopante-theinyl transferase CfwA/NpgA is required for Aspergillus nidulans secondary metabolism and asexual development. Eukaryot. Cell 6: 710-720.
43. Meister, J., Weber, D., Martino, V., Sterner, O., and Anke, T. (2007). Phomopsidone, a novel depsidone from an endophyte of the medic-inal plant Eupatorium arnottianum. Z. Naturforsch. C 62: 11-15.
44. Mofid, M.R., Finking, R., and Marahiel, M.A. (2002). Recognition of hybrid peptidyl carrier proteins/acyl carrier proteins in nonribosomal peptide synthetase modules by the 4'-phosphopantethelnyl transfer-ases AepS and Sfp. J. Biol. Chem. 277: 17023-17031.
45. Money, N.P., Caesar-TonThat, T.C., Frederick, B., and Henson, J.M. 1998 Melanin synthesis is associated with changes in hyphopodial turgor, permeability, and wall rigidity in Gaeumannomyces graminis var. graminis. Fungal Genet. Biol. 24: 240-251. (Pubitemid 28472950)
46. Mootz, H.D., Schorgendorfer, K., and Marahiel, M.A. (2002). Func-tional characterization of 4'-phosphopantetheinyl transferase genes of bacterial and fungal origin by complementation of Saccharomyces cerevisiae lys5. FEMS Microbiol. Lett. 213: 51-57.
47. Neville, C., Murphy, A., Kavanagh, K., and Doyle, S. (2005). A 4'-phosphopantetheinyl transferase mediates non-rlbosomal peptide synthetase activation in Aspergillus fumigatus. ChemBioChem 6: 679-685.
48. Nosanchuk, J.D., and Casadevall, A. (2003). The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 5: 203-223.
49. Oberegger, H., Eisendle, M., Schrettl, M., Graessle, S., and Haas, H. (2003). 4'-Phosphopantethelnyl transferase-encodlng npgA is essen-tial for siderophore biosynthesis in Aspergillus nidulans. Curr. Genet. 44:211-215.
50. Oide, S., Moeder, W., Krasnoff, S., Gibson, D., Haas, H., Yoshioka, K., and Turgeon, B.G. 2006 NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabo-lism, is a conserved virulence determinant of plant pathogenic asco-mycetes. Plant Cell 18: 2836-2853. (Pubitemid 44749907)
51. 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.
52. Punt, P.J., Oliver, R.P., Dingemanse, M.A., Pouwels, P.H., and van den Hondel, C.A. (1987). Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56: 117-124.
53. Ramakers, C., Ruijter, J.M., Lekanne Deprez, R.H., and Moorman, A.F.M. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339: 62-66.
54. Rasmussen, J.B., and Hanau, R.M. (1989). Exogenous scytalone restores appressorial melanization and pathogenicity in albino mu-tants of Colletotrichum graminicola. Can. J. Plant Pathol. 11:349-352.
55. Rohe, M., Gierlich, A., Hermann, H., Hahn, M., Schmidt, B., Rosahl, S., and Knogge, W. (1995). The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avlrulence on host plants of the Rrs1 resistance genotype. EMBO J. 14: 4168-4177.
56. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Clon-ing: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
57. Sawada, H., Sugihara, M., Takagaki, M., and Nagayama, K. (2004). Monitoring and characterization of Magnaporthe grisea isolates with decreased sensitivity to scytalone dehydratase inhibitors. Pest Manag. Sci. 60: 777-785.
58. Scheffer, J., Chen, C., Heidrich, P., Dickman, M.B., and Tudzynski, P. (2005). A CDC42 homologue in Claviceps purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryot. Cell 4: 1228-1238.
59. Schrettl, M., Bignell, E., Kragl, C., Sabiha, Y., Loss, O., Eisendle, M., Wallner, A., Arst, H.N.J., Haynes, K., and Haas, H. (2007). Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog. 3: 1195-1207.
60. Schweizer, P., Novara, D., and Douchkov, D. (2006). Method for increasing a fungal resistance of transgenic plants by a host-induced suppression of a pathgogenic fungi genetic expression. International Patent Number WO 2006/097465 A2.
61. Smith, D.B., and Corcoran, L.M. (1994). Expression and purification of gluthathion-S-transferase fusion proteins. In Current Protocols in Molecular Biology, F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore,
62. J.G. Seidman, J.A. Smith, and K. Struhl, eds (New York: John Wiley & Sons), pp. 16.17.11.11-16.17.17.
63. Soid-Raggi, G., Sanchez, O., and Aguirre, J. (2006). TmpA, a member of a novel family of putative membrane flavoproteins, regulates asexual development in Aspergillus nidulans. Mol. Microbiol. 59: 854-869.
64. Steiner, U., and Oerke, E.C. (2007). Localized melanization of appres-soria is required for pathogenicity of Venturia inaequalis. Phytopa-thology 97: 1222-1230.
65. Studier, F.W., and Moffatt, B.A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189: 113-130.
66. Sugui, J.A., and Deising, H.B. (2002). Isolation of infection-specific sequence tags expressed during early stages of maize anthracnose disease development. Mol. Plant Pathol. 3: 197-203.
67. Takeshita, N., Yamashita, S., Ohta, A., and Horiuchi, H. (2006). Aspergillus nidulans class V and VI chitin synthases CsmA and CsmB, each with a myosin motor-like domain, perform compensatory func-tions that are essential for hyphal tip growth. Mol. Microbiol. 59:1380-1394.
68. Treco, D.A., and Lundblad, V. (1993). Basic techniques of yeast genetics. In Current Protocols in Molecular Biology, F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds (New York: John Wiley & Sons), pp. 13.11.11-13.11.17.
69. Tsuji, G., Kenmochi, Y., Takano, Y., Sweigard, J., Farrall, L., Furusawa, I., Horino, O., and Kubo, Y. (2000). Novel fungal tran-scriptional activators, Cmrl p of Colletotrichum lagenarium and pigl p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-blnding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol. Microbiol. 38: 940-954.
70. Vernet, T., Dignard, D., and Thomas, D.Y. (1987). A family of yeast expression vectors containing the phage f1 intergenic region. Gene 52: 225-233. (Pubitemid 17090751)
71. Walton, J.D. (2006). HC-toxin. Phytochemistry 67: 1406-1413.
72. Weiergang, I., Dunkle, L.D., Wood, K.V., and Nicholson, R.L. (1996). Morphogenic regulation of pathotoxin synthesis in Cochliobolus carbonum. Fungal Genet. Biol. 20: 74-78.
73. Werner, S., Sugui, J.A., Steinberg, G., and Deising, H.B. (2007). A chitin synthase with a myosln-like motor domain is essential for hyphal growth, appressorium differentiation and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol. Plant Microbe Interact. 20: 1555-1567. (Pubitemid 350136441)
74. Wilson, R.A., and Talbot, N.J. (2009). Under pressure: Investigating the biology of plant infection by Magnaporthe oryzae. Nat. Rev. Microbiol. 7: 185-195.
75. Yin, J., Straight, P.D., McLoughlin, S.M., Zhou, Z., Lin, A.J., Golan, D.E., Kelleher, N.L., Kolter, R., and Walsh, C.T. (2005). Genetically encoded short peptide tag for versatile protein labeling by Sfp phosphopantetheinyl transferase. Proc. Natl. Acad. Sci. USA 102: 15815-15820.
76. Yu, J.H., Hamari, Z., Han, K.H., Seo, J.A., Reyes-Domínguez, Y., and Scazzocchio, C. (2004). Double-joint PCR: A PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41:973-981.
77. Zhbanko, M., Zinchenko, V., Gutensohn, M., Schierhorn, A., and Klösgen, R.B. 2005 Inactivation of a predicted leader peptidase prevents photo autotrophic growth of Synechocystis sp strain PCC 6803. J. Bacteriol. 187: 3071-3078. (Pubitemid 40571600)