Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity

Molecular Plant-Microbe Interactions

Volumn 13, Issue 7, 2000, Pages 742-753

  Johnson, R D ^a,d   Johnson, L ^a   Itoh, Y ^c   Kodama, M ^a   Otani, H ^b   Kohmoto, K ^a  

^a TOTTORI UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c SHINSHU UNIVERSITY   (Japan)

^d WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APPLE; FUNGAL GENE; GENE DISRUPTION; GENETIC SCREENING; GENETIC SUSCEPTIBILITY; GENETIC TRANSFORMATION; GENOME LIBRARY; MUTANT; MYCOTOXIN; PATHOTYPE; PEPTIDE SYNTHASE; POLYMERASE CHAIN REACTION; VIRULENCE; WILD RELATIVE;

ALTERNARIA; ALTERNARIA ALTERNATA; ALTERNATA ALTERNATA; EMBRYOPHYTA; FUNGI; MALUS X DOMESTICA;

EID: 0034041314     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2000.13.7.742     Document Type: Article

References (61)

1. Ahn, J. H., and Walton, J. D. 1996. Chromosomal organization of TOX2, a complex locus controlling host-selective toxin biosynthesis in Cochliobolus carbonum. Plant Cell 8:887-897.
2. Ann, J. H., and Walton, J. D. 1997. A fatty acid synthase gene in Cochliobolus carbonum required for production of HC-toxin, cyclo(D- prolyl-L-alanyl-D-alanyl-L-2-amino-9,10-epoxi-8-oxodecanoyl). Mol. Plant-Microbe Interact. 10:207-214.
3. Ahn, J. H., and Walton, J. D. 1998. Regulation of cyclic peptide biosynthesis and pathogenicity in Cochliobolus carbonum by TOXEp, a novel protein with a bZIP basic DNA-binding motif and four ankyrin repeats. Mol. Gen. Genet. 260:462-469.
4. Akamatsu, H., Itoh, Y., Kodama, M., Otani, H., and Kohmoto, K. 1997. AAL-toxin-deficient mutants of Alternaria alternata tomato pathotype by restriction enzyme-mediated integration. Phytopathology 87: 967-972.
5. Akamatsu, H., Taga, M., Kodama, M., Johnson, R., Otani, H., and Kohmoto, K. 1999. Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxins. Curr. Genet. 35:647-656.
6. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
7. Annis, S. L., and Panaccione, D. G. 1998. Presence of peptide synthetase gene transcripts and accumulation of ergopeptines in Claviceps purpurea and Neotyphodium coenophialum. Can. J. Microbiol. 44:80-86.
8. Bailey, A. M., Kershaw, M. J., Hunt, B. A., Paterson, I. C., Charnley, K., Reynolds, S. E., and Clarkson, J. M. 1996. Cloning and sequence analysis of an intron-containing domain from a peptide synthetase-encoding gene of the entomopathogenic fungus Metarhizium anisopliae. Gene 173:195-197.
9. Ballance, D. J. 1991. Pages 1-29 in: Molecular Industrial Mycology. S. A. Leong and R. M. Berka, eds. Marcel Dekker, New York.
10. Bruchez, J. J. P., Eberle, J., and Russo, V. E. A. 1993. Regulatory sequences involved in the translation of Neurospora crassa mRNA: Kozak sequences and stop codons. Fungal Genet. Newsl. 40:85-88.
11. Diez, B., Gutierrez, S., Barredo, J. L., van Solingen, P., van der Voort, L. H., and Martin, J. F. 1990. The cluster of penicillin biosynthetic genes. Identification and characterization of the pcbAB gene encoding the alpha-aminoadipyl-cysteinyl-valine synthetase and linkage to the pcbC and penDE genes. J. Biol. Chem. 265:16358-16365.
12. Etchegaray, A., Dieckmann, R., Engel, P. C., Turner, G., and von Dohren, H. 1998. Group specific antibodies against the putative AMP-binding domain signature SGTTGXPKG in peptide synthetases and related enzymes. Biochem. Mol. Biol. Int. 44:235-243.
13. Filajdić, N., and Sutton, T. B. 1991. Identification and distribution of Alternaria mali on apples in North Carolina and susceptibility of different varieties of apples to Alternaria blotch. Plant Dis. 75:1045-1048.
14. Gocht, M., and Marahiel, M. A. 1994. Analysis of core sequences in the D-Phe activating domain of the multifunctional peptide synthetase TycA by site directed mutagenesis. J. Bacteriol. 176:2654-2662.
15. Gutiérrez, S., Diez, B., Montenegro, E., and Martin, J. F. 1991. Characterization of the Cephalosporium acremonium pcbAB gene encoding alpha-aminoadipyl-cysteinyl-valine synthetase, a large multidomain peptide synthetase: linkage to the pcbC gene as a cluster of early cephalosporin biosynthetic genes and evidence of multiple functional domains. J. Bacteriol. 173:2354-2365.
16. Haese, A., Schubert, M., Herrmann, M., and Zocher, R. 1993. Molecular characterization of the enniatin synthetase gene encoding a multifunctional enzyme catalysing N-methyldepsipeptide formation in Fusarium scirpi. Mol. Microbiol. 7:905-914.
17. Hayami, C., Otani, H., Nishimura, S., and Kohmoto, K. 1982. Induced resistance in pear leaves by spore germination fluids of nonpathogens to Alternaria alternata Japanese pear pathotype and suppression of the induction by AK-toxin. J. Fac. Agric. Tottori Univ. 17:9.
18. Keller N. P., and Hohn, T. M. 1997. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet. Biol. 21:17-29.
19. Kleinkauf, H., and von Dohren, H. 1987. Biosynthesis of peptide antibiotics. Annu. Rev. Microbiol. 41:259-289.
20. Kleinkauf, H., and von Dohren, H. 1990. Nonribosomal biosynthesis of peptide antibiotics. Eur. J. Biochem. 236:335-351.
21. Kohmoto, K., and Otani, H. 1991. Host recognition by toxigenic plant pathogens. Experientia 47:755-764.
22. Kohmoto, K., Taniguchi, T., and Nishimura, S. 1974. Correlation between the susceptibility of apple cultivars to Alternaria mali and their sensitivity to AM-toxin I. Ann. Phytopathol. Soc. Jpn. 43:65-66.
23. Kozak, M. 1991. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266:19867-19870.
24. Kuninaga, S., and Yokosawa, R. 1987. Studies on the taxonomy of plant pathogenic fungi by a comparison of DNA homology. I. Genetic relatedness among species in the genus Alternaria. (In Japanese). Ann. Phytopathol. Soc. Jpn. 53:368-369.
25. Kusaba, M., and Tsuge, T. 1994. Nuclear ribosomal DNA variation and pathogenic specialization in Alternaria fungi known to produce host-specific toxins. Appl. Environ. Microbiol. 60:3055-3062.
26. Kusaba, M., and Tsuge, T. 1995. Phylogeny of Alternaria fungi known to produce host-specific toxins on the basis of variation in internal transcribed spacers of ribosomal DNA. Curr. Genet. 28:491-498.
27. Marahiel, M. A. 1992. Multidomain enzymes involved in peptide synthesis. FEBS Lett. 307:40-43.
28. Nikolskaya, A. N., Panaccione, D. G., and Walton, J. D. 1995. Identification of peptide synthetase-encoding genes from filamentous fungi producing host-selective phytotoxins or analogs. Gene 165:207-211.
29. Nishimura, S., and Kohmoto, K. 1983. Host-specific toxins and chemical structures from Alternaria species. Annu. Rev. Phytopathol. 21: 87-116.
30. Okuno, T., Ishita, Y., Sawai, K., and Matsumoto, T. 1974. Characterization of alternariolide, a host-specific toxin produced by Alternaria mali Roberts. Chem. Lett. 1974:635-638.
31. Otani, H., Kohmoto, K., and Kodama, M. 1995. Alternaria toxins and their effects on host plants. Can. J. Bot. 73(Suppl. 1):S453-S458.
32. Panaccione, D. G. 1996. Multiple families of peptide synthetase genes from ergopeptine-producing fungi. Mycol. Res. 100:429-436.
33. Park, P., Nishimura, S., Kohmoto, K., Otani, H., and Tsujimoto, K. 1981. Two action sites of AM-toxin I produced by apple pathotype of Alternaria alternata in host cells: an ultrastructural study. Can. J. Bot. 59: 301-310.
34. Park, P., Tsuda, M., Hayashi, Y., and Ueno, T. 1977. Effect of a host-specific toxin (AM-toxin I) produced by Alternaria mali, an apple pathogen, on the ultrastructure of plasma membrane of cells in apple and Japanese pear leaves. Can. J. Bot. 55:2383-2393.
35. Pope, M. R., Ciuffetti, L. M., Knoche, H. W., McCrery, D. A., and Tomer, K. B. 1985. Structure of an amino acid analog of the host-specific toxin from Helminthosporium carbonum. Biochemistry 22: 3502.
36. Pringle, R. B., and Scheffer, R. P. 1964. Host-specific plant toxins. Annu. Rev. Phytopathol. 2:133-156.
37. Punt, P. J., Oliver, R. P., Dingemanse, M. A., Pouwels, P. H., and van den Hondel, C. A. M. J. J. 1987. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56:117-124.
38. Reed, K. C., and Mann, D. A. 1985. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res. 13:7207-7221.
39. Sambrook, J., Fritsch, E. F., and Maniatis, T. A. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
40. Sawamura, K. 1966. Studies on spotted disease of apples. 6. On the host-specific toxin of Alternaria mali Roberts. Bull. Hortic. Res. Stn. Japan, Ser. C. 4:43-59.
41. Scheffer, R. P., and Livingston, R. S. 1984. Host-selective toxins and their role in plant diseases. Science 223:415-419.
42. Scott-Craig, J. S., Panaccione, D. G., Pocard, J. A. and Walton, J. D. 1992. The cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungus Cochliobolus carbonum is encoded by a 15.7-kilobase open reading frame. J. Biol. Chem. 267:26044-26049.
43. Smith, D. J., Earl, A. J., and Turner, G. 1990. The multifunctional peptide synthetase performing the first step of penicillin biosynthesis in Penicillium chrysogenum is a 421073 protein similar to Bacillus brevis peptide antibiotic synthetases. EMBO J. 9:2743-2750.
44. Stachelhaus, T., and Marahiel, M. A. 1995a. Modular structure of genes encoding multifunctional peptide synthetases required for non-ribosomal peptide synthesis. FEMS Microbiol. Lett. 125:3-14.
45. Stachelhaus, T., and Marahiel, M. A. 1995b. Modular structure of peptide synthetases revealed by dissection of the multifunctional enzyme GrsA. J. Biol. Chem. 270:6163-6169.
46. Stachelhaus, T., Mootz, H. D., and Marahiel, M. A. 1999. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6:493-505.
47. Tanaka, A., Shiotani, H., Yamamoto, M., and Tsuge, T. 1999. Insertional mutagenesis and cloning of the genes required for biosynthesis of the host-specific AK-toxin in the Japanese pear pathotype of Alternaria alternata. Mol. Plant-Microbe Interact 12:691-702.
48. Thompson, J. D., Higgins, D. G., and Gibson, T. J. 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.
49. Tudzynski, P., Holter, K., Correia, T., Arntz, C., Grammel, N., and Keller, U. 1999. Evidence for an ergot alkaloid gene cluster in Claviceps purpurea. Mol. Gen. Genet. 261:133-141.
50. Turgay, K., Krause, M., and Marahiel, M. A. 1992. Four homologous domains in the primary structure of GrsB are related to domains in a super-family of adenylate-forming enzymes. Mol. Microbiol. 6:529-546.
51. Turgay, K., and Marahiel, M. A. 1994. A general approach for identifying and cloning peptide synthetase genes. Peptide Res. 7:238-241.
52. Ueno, T., Nakashima, T., Uemoto, M., Fukami, H., Lee, S. N., and Izumiya, N. 1977. Mass spectrometry of Alternaria mali toxins and related cyclodepsipeptides. Biomed. Mass Spectrom. 4:134-142.
53. van Kan, J. A. L., van den Ackerveken, G. F. J. M., and de Wit, P. J. G. M. 1991. Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol. Plant-Microbe Interact. 4:52-59.
54. Walton, J. D. 1996. Host-selective toxins: Agents of compatibility. Plant Cell 8:1723-1733.
55. Walton, J. D., Earle, E. D., and Gibson, D. W. 1982. Purification and structure of the host-specific toxin from Helminthosporium carbonum race 1. Biochem. Biophys. Res. Commun. 107:785.
56. Walton, J. D., and Panaccione, D. G. 1993. Host-selective toxins and disease specificity: Perspective and progress. Annu. Rev. Phytopathol. 31:275-303.
57. Weber, G., Schörgendorfer, K., Schneider-Scherzer, E., and Leitner, E. 1994. The peptide synthetase catalyzing cyclosporine production in Tolypocladium niveum is encoded by a giant 45.8-kilobase open reading frame. Curr. Genet, 26:120-125.
58. Wolpert, T. J., Macko, V., Acklin, W., Jaun, B., Seibl, J., Meili, J., and Arigoni, D. 1985. Structure of victorin C, the major host-selective toxin from Cochliobolus victoriae. Experientia 41:1524.
59. Yang, G., Rose, M. S., Turgeon, B. G., and Yoder, O. C. 1996. A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Cell 8:2139-2150.
60. Yoder, O. C. 1980. Toxins in pathogenesis. Annu. Rev. Phytopathol. 18: 103-29.
61. Yoder, O. C., 1998. A mechanistic view of the fungal/plant interaction based on host-specific toxin studies. Pages 3-15 in: Molecular Genetics of Host-Specific Toxins in Plant Disease. K. Kohmoto and O. C. Yoder, eds. Kluwer Academic Pub., Dordrecht, The Netherlands.