Loss of gibberellin production in Fusarium verticillioides (Gibberella fujikuroi MP-A) is due to a deletion in the gibberellic acid gene cluster

Applied and Environmental Microbiology

Volumn 74, Issue 24, 2008, Pages 7790-7801

  Bömke, Christiane ^a   Rojas, Maria C ^b   Hedden, Peter ^c   Tudzynski, Bettina ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF CHILE   (Chile)

^c ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; ENCODING (SYMBOLS); GENE ENCODING; GENES; GENETIC ALGORITHMS; HORMONES; METABOLITES; PATHOGENS; PROGRAMMING THEORY;

BIOLOGICAL SPECIES; BIOSYNTHESIS GENES; CODING REGIONS; DELETION MUTANTS; DESATURASE; DITERPENOID; FUMONISINS; FUSARIUM; FUSARIUM VERTICILLIOIDES; GENE CLUSTERS; GIBBERELLA FUJIKUROI; GIBBERELLIC ACIDS; GIBBERELLIN PRODUCTIONS; KAURENE; MATING POPULATIONS; PLANT HORMONES; PRODUCTION CAPACITIES; SECONDARY METABOLITES; SEQUENCE IDENTITIES;

GALLIUM ALLOYS;

FUNGAL ENZYME; GIBBERELLIC ACID; GIBBERELLIN;

ENZYME ACTIVITY; FUNGAL DISEASE; FUNGUS; GENE EXPRESSION; HORMONE; PATHOGEN; SECONDARY METABOLITE; SPECIES COMPLEX; TOXIN;

ARTICLE; COSMID; FUNGAL GENE; FUNGUS MUTANT; GENE CLUSTER; GENE DELETION; GIBBERELLA FUJIKUROI; NONHUMAN; NUCLEOTIDE SEQUENCE;

BIOSYNTHETIC PATHWAYS; DNA, FUNGAL; FUNGAL PROTEINS; GENE DELETION; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; GIBBERELLA; GIBBERELLINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; GIBBERELLA FUJIKUROI; GIBBERELLA KONZA; GIBBERELLA MONILIFORMIS; ZEA MAYS;

EID: 57449100652     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01819-08     Document Type: Article

References (65)

1. Bacon, C. W., J. K. Porter, W. P. Norred, and J. F. Leslie. 1996. Production of fusaric acid by Fusarium species. Appl. Environ. Microbiol. 62:4039-4043.
2. Bearder, J. R., J. MacMillan, M. Wels, M. B. Chaffey, and B. O. Phinney. 1974. Position of the metabolic block for gibberellin biosynthesis in mutant B1-41a of Gibberella fujikuroi. Phytochemistry 13:911-917.
3. Bezuidenhout, S. C., W. C. A. Gelderblom, C. P. Gorst-Allman, R. M. Horak, W. F. O. Marasas, G. Spiteller, and R. Vleggaar. 1988. Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme. J. Chem. Soc. 1988:743-745.
4. Bojja, R. S., R. L. Cerny, R. H. Proctor, and L. C. Du. 2004. Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J. Agr. Food Chem. 52:2855-2860.
5. Bok, J. W., and N. P. Keller. 2004. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot. Cell 3:527-535.
6. Bömke, C., M. C. Rojas, F. Gong, P. Hedden, and B. Tudzynski. 2008. Isolation and functional characterization of the gibberellin biosynthetic gene cluster in Sphaceloma manihoticola. Appl. Environ. Microbiol. 74:5325-5339.
7. Chulze, S. N., M. L. Ramirez, M. Pascale, and A. Visconti. 1998. Fumonisin production by, and mating populations of, Fusarium section Liseola isolates from maize in Argentina. Mycol. Res. 102:141-144.
8. Church, G. M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81:1991-1995.
9. Desjardins, A. E. 2003. Gibberella from A (venaceae) to Z (eae). Annu. Rev. Phytopathol. 41:177-198.
10. Desjardins, A. E., and R. D. Plattner. 2000. Fumonisin B-1-nonproducing strains of Fusarium verticillioides cause maize (Zea mays) ear infection and ear rot. J. Agr. Food Chem. 48:5773-5780.
11. Desjardins, A. E., R. D. Plattner, T. C. Nelsen, and J. F. Leslie. 1995. Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Appl. Environ. Microbiol. 61:79-86.
12. Desjardins, A. E., H. K. Manandhar, R. D. Plattner, G. G. Manandhar, S. M. Poling, and C. M. Maragos. 2000. Fusarium species from Nepalese rice and production of mycotoxins and gibberellic acid by selected species. Appl. Environ. Microbiol. 66:1020-1025.
13. Doyle, J. J., and J. L. Doyle. 1990. Isolation of plant DNA from fresh tissue. Focus 12:13-15.
14. Fernández-Martín, R., F. Reyes, C. E. Domenech, E. Cabrera, P. M. Bramley, A. F. Barrero, J. Avalos, and E. Cerdá- Olmedo. 1995. Gibberellin biosynthesis in gib mutants of Gibberella fujikuroi. J. Biol. Chem. 270:14970-14974.
15. Gaskin, P., and J. MacMillan. 1992. GC-MS of the gibberellins and related compounds: methodology and a library of spectra. Cantock's Enterprises, Bristol, United Kingdom.
16. Geissman, T. A., A. J. Verbiscar, B. O. Phinney, and G. Cragg. 1966. Studies on the biosynthesis of gibberellins from (-)-kaurenoic acid in cultures of Gibberella fujikuroi. Phytochemistry 5:933-947.
17. Glenn, A. E., N. C. Zitomer, A. M. Zimeri, L. D. Williams, R. T. Riley, and R. H. Proctor. 2008. Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings. Mol. Plant Microbe Interact. 21:87-97.
18. Jurgenson, J. E., R. L. Bowden, K. A. Zeller, J. F. Leslie, N. J. Alexander, and R. D. Plattner. 2002. A genetic map of Gibberella zeae (Fusarium graminearum). Genetics 160:1451-1460.
19. Kawaide, H. 2006. Biochemical and molecular analyses of gibberellin biosynthesis in fungi. Biosci. Biotechnol. Biochem. 70:583-590.
20. Keller, N. P., and T. M. Hohn. 1997. Metabolic pathway gene cluster in filamentous fungi. Fungal Genet. Biol. 21:17-29.
21. Kerényi, Z., K. Zeller, L. Hornok, and J. F. Leslie. 1999. Standardization of mating type terminology in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 65:4071-4076.
22. Khaldi, N., J. Collemare, M. H. Lebrun, and K. H. Wolfe. 2008. Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol. 9:R18.
23. Krügel, H., G. Fiedler, C. Smithand, and S. Baumberg. 1993. Sequence and transcriptional analysis of the nourseothricin acetyltransferase- encoding gene nat1 from Streptomyces noursei. Gene 127:127-131.
24. Leslie, J. F. 1995. Gibberella fujikuroi: available populations and variable traits. Can. J. Bot. 73:282-291.
25. Leslie, J. F., W. F. O. Marasas, G. S. Shephard, E. W. Sydenham, S. Stockenström, and P. G. Thiel. 1996. Duckling toxicity and the production of fumonisin and moniliformin by isolates in the A and F mating populations of Gibberella fujikuroi (Fusarium moniliforme). Appl. Environ. Microbiol. 62: 1182-1187.
26. Leslie, J. F., K. A. Zeller, A. Logrieco, G. Mule, A. Moretti, and A. Ritieni. 2004. Species diversity of and toxin production by Gibberella fujikuroi species complex strains isolated from native prairie grasses in Kansas. Appl. Environ. Microbiol. 70:2254-2262.
27. Leslie, J. F., K. Zeller, M. Wohler, and B. Summerell. 2004. Interfertility of two mating populations in the Gibberella fujikuroi species complex. Eur. J. Plant Pathol. 110:611-618.
28. Linnemannstöns, P., T. Voß, P. Hedden, P. Gaskin, and B. Tudzynski. 1999. Deletions in the gibberellin biosynthesis gene cluster of Gibberella fujikuroi by restriction enzyme-mediated integration and conventional transformation-mediated mutagenesis. Appl. Environ. Microbiol. 65:2558-2564.
29. Linnemannstöns, P., J. Schulte, M. del Mar Prado, R. H. Proctor, J. Avalos, and B. Tudzynski. 2002. The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet. Biol. 37:134-148.
30. Logrieco, A., A. Moretti, G. Castella, M. Kostecki, P. Golinski, A. Ritieni, and J. Chelkowski. 1998. Beauvericin production by Fusarium species. Appl. Environ. Microbiol. 64:3084-3088.
31. Malonek, S., M. C. Rojas, P. Hedden, P. Gaskin, P. Hopkins, and B. Tudzynski. 2004. The NADPH:cytochrome P450 reductase gene from Gibberella fujikuroi is essential for gibberellin biosynthesis. J. Biol. Chem. 279:25075-25084.
32. Malonek, S., M. C. Rojas, P. Hedden, P. Gaskin, P. Hopkins, and B. Tudzynski. 2005. Functional characterization of two cytochrome P450 monooxygenase genes, P450-1 and P450-4, of the gibberellic acid gene cluster in Fusarium proliferatum (Gibberella fujikuroi MP-D). Appl. Environ. Microbiol. 71:1462-1472.
33. Malonek, S., C. Bömke, E. Bornberg-Bauer, M. C. Rojas, P. Hedden, P. Hopkins, and B. Tudzynski. 2005. Distribution of gibberellin biosynthetic genes and gibberellin production in the Gibberella fujikuroi species complex. Phytochemistry 66:1296-1311.
34. Malonek, S., M. C. Rojas, P. Hedden, P. Hopkins, and B. Tudzynski. 2005. Restoration of gibberellin production in Fusarium proliferatum by functional complementation of enzymatic blocks. Appl. Environ. Microbiol. 71:6014-6025.
35. Malz, S., M. N. Grell, C. Thrane, F. J. Maier, P. Rosager, A. Felk, K. S. Albertsen, S. Salomon, L. Bohn, W. Schäfer, and H. Giese. 2005. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet. Biol. 42:420-443.
36. Maniatis, T., J. Sambrook, and E. F. Fritsch. 1982. Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
37. Marasas, W. F. O. 2001. Discovery and occurrence of the fumonisins: a historical perspective. Environ. Health Perspect. 109:239-243.
38. Marasas, W. F. O., P. G. Thiel, C. J. Rabie, P. E. Nelson, and T. A. Toussoun. 1986. Moniliformin production in Fusarium section Liseola. Mycologia 78:242-247.
39. Marasas, W. F. O., T. S. Kellerman, W. C. A. Gelderblom, J. A. W. Coetzer, P. G. Thiel, and J. J. Vanderlugt. 1988. Leukoencephalomalacia in a horse induced by fumonisin-B1 isolated from Fusarium moniliforme. Onderstepoort J. Vet. Res. 55:197-203.
40. Mihlan, M., V. Homann, T.-W. D. Liu, and B. Tudzynski. 2003. AreA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Mol. Microbiol. 47:975-991.
41. Mirete, S., C. Vázquez, G. Mulè, M. Jurado, and M. T. González-Jaén. 2004. Differentiation of Fusarium verticillioides from banana fruits by IGS and EF-1α sequence analyses. Eur. J. Plant Pathol. 110:515-523.
42. Moretti, A., G. Mulè, A. Susca, M. T. González- Jaén, and A. Logrieco. 2004. Toxin profile, fertility and AFLP analysis of Fusarium verticillioides from banana fruits. Eur. J. Plant Pathol. 110:601-609.
43. Nelson, P. E., A. E. Desjardins, and R. D. Plattner. 1993. Fumonisins, mycotoxins produced by Fusarium species: biology, chemistry, and significance. Annu. Rev. Phytopathol. 31:233-252.
44. Nirenberg, H. I., and K. O'Donnell. 1998. New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia 90:434-458.
45. O'Donnell, K., E. Cigelnik, and H. I. Nirenberg. 1998. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465-493.
46. Pontecorvo, G. V., J. A. Poper, L. M. Hemmonns, K. D. MacDonald, and A. W. J. Buften. 1953. The genetics of Aspergillus nidulans. Adv. Genet. 141:141-238.
47. Proctor, R. H., A. E. Desjardins, and R. D. Plattner. 1999. Biosynthetic and genetic relationships of B-series fumonisins produced by Gibberella fujikuroi mating population A. Nat. Toxins 7:251-258.
48. Proctor, R. H., D. W. Brown, R. D. Plattner, and A. E. Desjardins. 2003. Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet. Biol. 38:237-249.
49. Proctor, R. H., R. D. Plattner, D. W. Brown, J. A. Seo, and Y. W. Lee. 2004. Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycol. Res. 108:815-822.
50. Punt, P. J., R. P. Oliver, M. A. Dingenanse, P. H. Puwels, and C. A. M. J. J. van den Hondel. 1987. Transformation of Aspergillus nidulans based on the hygromycin B resistance marker from Escherichia coli. Gene 56:117-124.
51. Reynoso, M. M., A. M. Torres, and S. N. Chulze. 2004. Fusaproliferin, beauvericin and fumonisin production by different mating populations among the Gibberella fujikuroi complex isolated from maize. Mycol. Res. 108:154-160.
52. Rheeder, J. P., W. F. O. Marasas, and H. F. Vismer. 2002. Production of fumonisin analogs by Fusarium species. Appl. Environ. Microbiol. 68:2101-2105.
53. Rojas, M. C., P. Hedden, P. Gaskin, and B. Tudzynski. 2001. The P450-1 gene of Gibberella fujikuroi encodes a multifunctional enzyme in gibberellin biosynthesis. Proc. Natl. Acad. Sci. USA 98:5838-5843.
54. Tominaga, M., Y. H. Lee, R. Hayashi, Y. Suzuki, O. Yamada, K. Sakamoto, K. Gotoh, and O. Akita. 2006. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains. Appl. Environ. Microbiol. 72:484-490.
55. Torres, A. M., M. M. Reynoso, F. G. Rojo, M. L. Ramirez, and S. N. Chulze. 2001. Fusarium species (section Liseola) and its mycotoxins in maize harvested in northern Argentina. Food Addit. Contam. 18:836-843.
56. Tsavkelova, E. A., C. Bömke, A. I. Netrusov, J. Weiner, and B. Tudzynski. 2008. Production of gibberellic acids by an orchid-associated Fusarium proliferatum strain. Fungal Genet. Biol. 45:1393-1403.
57. Tudzynski, B. 2005. Gibberellin biosynthesis in fungi: genes, enzymes, evolution, and impact on biotechnology. Appl. Microbiol. Biotechnol. 66:597-611.
58. Tudzynski, B., and K. Hölter. 1998. The gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet. Biol. 25:157-170.
59. Tudzynski, B., K. Mende, K.-M. Weltring, S. E. Unkles, and J. R. Kinghorn. 1996. The Gibberella fujikuroi niaD gene encoding nitrate reductase: isolation, sequence, homologous transformation and electrophoretic karyotype location. Microbiology 142:533-539.
60. Tudzynski, B., V. Homann, B. Feng, and G. A. Marzluf. 1999. Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Mol. Gen. Genet. 261:106-114.
61. Tudzynski, B., P. Hedden, E. Carrera, and P. Gaskin. 2001. The P450-4 gene of Gibberella fujikuroi encodes ent-kaurene oxidase in the gibberellin biosynthetic pathway. Appl. Environ. Microbiol. 67:3514-3522.
62. Tudzynski, B., M. C. Rojas, P. Gaskin, and P. Hedden. 2002. The Gibberella fujikuroi gibberellin 20-oxidase is a multifunctional monooxygenase. J. Biol. Chem. 277:21246-21253.
63. 4 desaturase and the 13-hydroxylase, respectively. J. Biol. Chem. 278:28635-28643.
64. Voß, T., J. Schulte, and B. Tudzynski. 2001. A new MFS-transporter gene next to the gibberellin biosynthesis gene cluster of Gibberella fujikuroi is not involved in gibberellin secretion. Curr. Genet. 39:377-383.
65. Zeller, K. A., B. A. Summerell, S. Bullock, and J. F. Leslie. 2003. Gibberella konza (Fusarium konzum) sp. nov. from prairie grasses, a new species in the Gibberella fujikuroi species complex. Mycologia 95:943-954.