Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings

Molecular Plant-Microbe Interactions

Volumn 21, Issue 1, 2008, Pages 87-97

  Glenn, Anthony E ^a   Zitomer, Nicholas C ^a   Zimeri, Anne Marie ^a,b   Williams, Lonnie D ^a,b,d   Riley, Ronald T ^a,b   Proctor, Robert H ^c  

^a RUSSELL RESEARCH CENTER   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

^d Burdock Group   (United States)

Author keywords

Gibberella fujikuroi species complex; Gibberella moniliformis; Zea mays

Indexed keywords

FUMONISIN;

ARTICLE; BANANA; FUNGAL GENE; FUSARIUM; GENE DELETION; GENETIC COMPLEMENTATION; GENETIC TRANSFORMATION; GENETICS; MAIZE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; SEEDLING; SOUTHERN BLOTTING;

BASE SEQUENCE; BLOTTING, SOUTHERN; FUMONISINS; FUSARIUM; GENE DELETION; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUSA; PLANT DISEASES; PLANT LEAVES; SEEDLING; TRANSFORMATION, GENETIC; ZEA MAYS;

ASCOMYCOTA; FUSARIUM; GIBBERELLA; GIBBERELLA FUJIKUROI; GIBBERELLA MONILIFORMIS; MONILIFORMIS; ZEA MAYS;

EID: 37149054321     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-21-1-0087     Document Type: Article

References (57)

1. Abbas, H. K., and Boyette, C. D. 1992. Phytotoxicity of fumonisin B1 on weed and crop species. Weed Technol. 6:548-552.
2. Abbas, H. K., Tanaka, T., Duke, S. O., Porter, J. K., Wray, E. M., Hodges, L., Sessions, A. E., Wang, E., Merrill, A. H., Jr., and Riley, R. T. 1994. Fumonisin- and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases. Plant Physiol. 106:1085-1093.
3. Bacon, C. W., Hinton, D. M., and Richardson, M. D. 1994. A corn seedling assay for resistance to Fusarium moniliforme. Plant Dis. 78:302-305.
4. Brandwagt, B. F., Mesbah, L. A., Takken, F. L., Laurent, P. L., Kneppers, T. J., Hille, J., and Nijkamp, H. J. 2000. A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc. Natl. Acad. Sci. U.S.A. 97:4961-4966.
5. Brown, D. W., Butchko, R. A. E., Busman, M., and Proctor, R. H. 2007. The Fusarium verticillioides FUM gene cluster encodes a Zn(II)2Cys6 protein that affects FUM gene expression and fumonisin production. Eukaryot. Cell 6:1210-1218
6. Chang, P. K., Horn, B. W., and Dorner, J. W. 2005. Sequence breakpoints in the aflatoxin biosynthesis gene cluster and flanking regions in nonaflatoxigenic Aspergillus flavus isolates. Fungal Genet. Biol. 42:914-923.
7. Chen, M., Han, G., Dietrich, C. R., Dunn, T. M., and Cahoon, E. B. 2006. The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell 18:3576-3593.
8. Cheng, J. J., Park, T. S., Fischl, A. S., and Ye, X. S. 2001. Cell cycle progression and cell polarity require sphingolipid biosynthesis in Aspergillus nidulans. Mol. Cell. Biol. 21:6198-6209.
9. Colvin, B. M., and Harrison, L. R.. 1992. Fumonisin-induced pulmonary edema and hydrothorax in swine. Mycopathologia 117:79-82.
10. Desjardins, A. E., and Plattner, R. D. 2000. Fumonisin B(1)-nonproducing strains of Fusarium verticillioides cause maize (Zea mays) ear infection and ear rot. J. Agric. Food Chem. 48:5773-5780.
11. Desjardins, A. E., Plattner, R. D., Shackelford, D. D., Leslie, J. F., and Nelson, P. E. 1992. Heritability of fumonisin B1 production in Gibberella fujikuroi mating population A. Appl. Environ. Microbiol. 58:2799-2805.
12. Desjardins, A. E., Plattner, R. D., Nelsen, T. C., and Leslie, J. F. 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.
13. Desjardins, A. E., Plattner, R. D., and Proctor, R. H. 1996. Linkage among genes responsible for fumonisin biosynthesis in Gibberella fujikuroi mating population A. Appl. Environ. Microbiol. 62:2571-2576.
14. Desjardins, A. E., Plattner, R. D., Lu, M., and Claflin, L. E. 1998. Distribution of fumonisins in maize ears infected with strains of Fusarium moniliforme that differ in fumonisin production. Plant Dis. 82:953-958.
15. Desjardins, A. E., Munkvold, G. P., Plattner, R. D., and Proctor, R. H. 2002. FUM1 - a gene required for fumonisin biosynthesis but not for maize ear rot and ear infection by Gibberella moniliformis in field tests. Mol. Plant-Microbe Interact. 15:1157-1164.
16. Desjardins, A. E., Plattner, R. D., Stessman, R. J., McCormick, S. P., and Millard, M. J. 2005. Identification and heritability of fumonisin insensitivity in Zea mays. Phytochemistry 66:2474-2480.
17. Doehlert, D. C., Knutson, C. A., and Vesonder, R. F. 1994. Phytotoxic effects of fumonisin B1 on maize seedling growth. Mycopathologia 127:117-121.
18. Gilchrist, D. G., Ward, B., Moussato, V., and Mirocha, C. J. 1992. Genetic and physiologic response to fumonisin and AAL-toxin by intact tissue of a higher plant. Mycopathologia 117:57-64.
19. Glenn, A. E. 2006. Natural variation of ascospore and conidial germination by Fusarium verticillioides and other Fusarium species. Mycol. Res. 110:211-219.
20. Glenn, A. E., Hinton, D. M., Yates, I. E., and Bacon, C. W. 2001. Detoxification of corn antimicrobial compounds as the basis for isolating Fusarium verticillioides and some other Fusarium species from corn. Appl. Environ. Microbiol. 67:2973-2981.
21. Glenn, A. E., Gold, S. E., and Bacon, C. W. 2002. Fdb1 and Fdb2, Fusarium verticillioides loci necessary for detoxification of preformed antimicrobials from corn. Mol. Plant-Microbe Interact. 15:91-101.
22. Glenn, A. E., Richardson, E. A., and Bacon, C. W. 2004. Genetic and morphological characterization of a Fusarium verticillioides conidiation mutant. Mycologia 96:968-980.
23. González-Jaén, M. T., Mirete, S., Patiño, B., López-Errasquín, E., and Vázquez, C. 2004. Genetic markers for the analysis of variability and for production of specific diagnostic sequences in fumonisin-producing strains of Fusarium verticillioides. Eur. J. Plant Pathol. 110:525-532.
24. Hirata, T., Kimishima, E., Aoki, T., Nirenberg, H. I., and O'Donnell, K. 2001. Morphological and molecular characterization of Fusarium verticillioides from rotten banana imported into Japan. Mycoscience 42:155-166.
25. 1. Pages 301-366 in: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: Some Traditional Medicines, Some Mycotoxins, Naphthalene and Styrene. IARC Press, Lyon, France.
26. Kommedahl, T., and Windeis, C. E. 1981. Root-, stalk-, and ear-infecting Fusarium species on corn in the USA. Pages 94-103 in: Fusarium: Diseases, Biology and Taxonomy. P. E. Nelson, T. A. Toussoun, and R. J. Cook, eds. The Pennsylvania State University Press, University Park, U.S.A.
27. Lamprecht, S. C., Marasas, W. F. O., Alberts, J. F., Cawood, M. E., Gelderblom, W. C. A., Shephard, G. S., Thiel, P. G., and Calitz, F. J. 1994. Phytotoxicity of fumonisins and TA-toxin to corn and tomato. Phytopathology 84:383-391.
28. Leslie, J. F., and Summereil, B. A. 2006. The Fusarium Laboratory Manual. Blackwell Publishing, Ames, IA, U.S.A.
29. Leslie, J. F., Plattner, R. D., Desjardins, A. E., and Klittich, C. J. R. 1992. Fumonisin B1 production by strains from different mating populations of Gibberella fujikuroi (Fusarium section Liseola). Phytopathology 82:341-345.
30. Logrieco, A., Mulè, G., Moretti, A., and Bottalico, A. 2002. Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. Eur. J. Plant Pathol. 108:597-609.
31. Lynch, D. V., and Dunn, T. M. 2004. An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytol. 161:677-702.
32. Malonek, S., Rojas, M. C., Hedden, P., Hopkins, P., and Tudzynski, B. 2005. Restoration of gibberellin production in Fusarium proliferatum by functional complementation of enzymatic blocks. Appl. Environ. Microbiol. 71:6014-6025.
33. Marasas, W. F. O., Kellerman, T. S., Gelderblom, W. C., Coetzer, J. A., Thiel, P. G., and van der Lugt, J. J. 1988. Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onderstepoort J. Vet. Res. 55:197-203.
34. Marasas, W. F. O., Riley, R. T., Hendricks, K. A., Stevens, V. L., Sadler, T. W., Gelineau-van Waes, J., Missmer, S. A., Cabrera, J., Torres, O., Gelderblom, W. C. A., Allegood, J., Martínez, C., Maddox, J., Miller, J. D., Starr, L., Sullards, M. C., Roman, A. V., Voss, K. A., Wang, E., and Merrill, A. H., Jr. 2004. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: A potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J. Nutr. 134:711-716.
35. Merrill, A. H., Jr., Sullards, M. C., Wang, E., Voss, K. A., and Riley, R. T. 2001. Sphingolipid metabolism: Roles in signal transduction and disruption by fumonisins. Environ. Health Perspect. 109 (Suppl. 2):283-289.
36. Mirete, S., Vázquez, C., Mulè, G., Jurado, M., and González-Jaén, M. T. 2004. Differentiation of Fusarium verticillioides from banana fruits by IGS and EF-1α sequence analyses. Eur. J. Plant Pathol. 110:515-523.
37. Moretti, A., Mulè, G., Susca, A., González-Jaén, M. T., and Logrieco, A. 2004. Toxin profile, fertility and AFLP analysis of Fusarium verticillioides from banana fruits. Eur. J. Plant Pathol. 110:601-609.
38. O'Donnell, K., Cigelnik, E., and Nirenberg, H. I. 1998. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465-493.
39. Oren, L., Ezrati, S., Cohen, D., and Sharon, A. 2003. Early events in the Fusarium verticillioides-maize interaction characterized by using a green fluorescent protein-expressing transgenic isolate. Appl. Environ. Microbiol. 69:1695-1701.
40. Proctor, R. H., Desjardins, A. E., Plattner, R. D., and Hohn, T. M. 1999. A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet. Biol. 27:100-112.
41. Proctor, R. H., Brown, D. W., Plattner, R. D., and Desjardins, A. E. 2003. Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet. Biol. 38:237-249.
42. Proctor, R. H., Plattner, R. D., Brown, D. W., Seo, J. A., and Lee, Y. W. 2004. Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycol. Res. 108:815-822.
43. Proctor, R. H., Plattner, R. D., Desjardins, A. E., Busman, M., and Butchko, R. A. E. 2006. Fumonisin production in the maize pathogen Fusarium verticillioides: Genetic basis of naturally occurring chemical variation. J. Agric. Food Chem. 54:2424-2430.
44. Revilla, P., and Tracy, W. F. 1995. Isozyme variation and phylogenetic relationships among open-pollinated sweet corn cultivars. Crop Sci. 35:219-227.
45. Riley, R. T., Wang, E., Schroeder, J. J., Smith, E. R., Plattner, R. D., Abbas, H., Yoo, H. S., and Merrill, A. H., Jr. 1996. Evidence for disruption of sphingolipid metabolism as a contributing factor in the toxicity and carcinogenicity of fumonisins. Nat. Toxins 4:3-15.
46. Riley, R. T., Enongene, E., Voss, K. A., Norred, W. P., Meredith, F. I., Sharma, R. P., Spitsbergen, J., Williams, D. E., Carlson, D. B., and Merrill, A. H., Jr. 2001. Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis. Environ. Health Perspect. 109 (Suppl. 2):301-308.
47. Ross, P. F., Nelson, P. E., Richard, J. L., Osweiler, G. D., Rice, L. G., Plattner, R. D., and Wilson, T. M. 1990. Production of fumonisins by Fusarium moniliforme and Fusarium proliferatum isolates associated with equine leukoencephalomalacia and a pulmonary edema syndrome in swine. Appl. Environ. Microbiol. 56:3225-3226.
48. Spassieva, S. D., Markham, J. E., and Hille, J. 2002. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J. 32:561-572.
49. van Asch, M. A. J., Rijkenberg, F. H. J., and Coutinho, T. A. 1992. Phytotoxicity of fumonisin B1, moniliformin, and T-2 toxin to corn callus cultures. Phytopathology 82:1330-1332.
50. Waalwijk, C., van der Lee, T., de Vries, I., Hesselink, T., Arts, J., and Kema, G. 2004. Synteny in toxigenic Fusarium species: The fumonisin gene cluster and the mating type region as examples. Eur. J. Plant Pathol. 110:533-544.
51. Wang, E., Norred, W. P., Bacon, C. W., Riley, R. T., and Merrill, A. H., Jr. 1991. Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. J. Biol. Chem. 266:14486-14490.
52. White, D. G. 1999. Compendium of Corn Diseases. American Phytopathological Society Press, St. Paul, MN, U.S.A.
53. Williams, L. D., Bacon, C. W., Meredith, F. I., Franzluebbers, A. J., Wyatt, R. D., Smith, M. A., and Riley, R. T. 2003. Leaching and binding of fumonisins in soil microcosms. J. Agric. Food Chem. 51:685-690.
54. Williams, L. D., Glenn, A. E., Bacon, C. W., Smith, M. A., and Riley, R. T. 2006. Fumonisin production and bioavailability to maize seedlings grown from seeds inoculated with Fusarium verticillioides and grown in natural soils. J. Agric. Food Chem. 54:5694-5700.
55. Williams, L. D., Glenn, A. E., Zimeri, A. M., Bacon, C. W., Smith, M. A., and Riley, R. T. 2007. Fumonisin disruption of ceramide biosynthesis in maize roots and the effects on plant development and Fusarium verticillioides-induced seedling disease. J. Agric. Food Chem. 55:2937-2946.
56. Xu, J.-R., and Leslie, J. F. 1996. A genetic map of Gibberella fujikuroi mating population A (Fusarium moniliforme). Genetics 143:175-189.
57. Dana-Farber Cancer Institute: compbio.dfci.harvard.edu/tgi/fungi.html