Maize seedling blight induced by fusarium verticillioides: Accumulation of fumonisin B1 in leaves without colonization of the leaves

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 9, 2014, Pages 2118-2125

  Baldwin, Thomas T ^a,b   Zitomer, Nicholas C ^a   Mitchell, Trevor R ^a   Zimeri, Anne Marie ^c   Bacon, Charles W ^a   Riley, Ronald T ^a   Glenn, Anthony E ^a  

^a RUSSELL RESEARCH CENTER   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

abscisic acid; B73; bulk flow; Silver Queen; Tama Flint; translocation; transpiration; W23

Indexed keywords

ABSCISIC ACID; B73; BULK FLOW; TAMA FLINT; TRANSLOCATION; W23;

FUNGI; TISSUE; TRANSPIRATION;

TISSUE ENGINEERING;

FUMONISIN; FUMONISIN B1;

ARTICLE; CHEMISTRY; FUSARIUM; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT LEAF; SEEDLING;

FUMONISINS; FUSARIUM; PLANT DISEASES; PLANT LEAVES; SEEDLING; ZEA MAYS;

GIBBERELLA MONILIFORMIS; ZEA MAYS;

EID: 84897678131     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf5001106     Document Type: Article

References (38)

1. Kommedahl, T.; Windels, C. E. Root-, stalk-, and ear infection Fusarium species on corn in the USA. Fusarium: Diseases, Biology, and Taxonomy; Pennsylvania State University: University Park, PA, USA, 1981; pp 94-103.
2. Bacon, C. W.; Hinton, D. M. Symptomless endophytic colonization of maize by Fusarium moniliforme Can. J. Bot. 1996, 74, 1195-1202
3. Fotso, J.; Leslie, J. F.; Smith, J. S. Production of beauvericin, moniliformin, fusaproliferin, and fumonisins B1, B2, and B3 by fifteen ex-type strains of Fusarium species Appl. Environ. Microbiol. 2002, 68, 5195-5197
4. Giesbert, S.; Schuerg, T.; Scheele, S.; Tudzynski, P. The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea Mol. Plant Pathol. 2008, 9, 317-327
5. Marasas, W. F. O.; Thiel, P. G.; Rabie, C. J.; Nelson, P. E.; Toussoun, T. A. Moniliformin production in Fusarium section Liseola Mycologia 1986, 78, 242-247
6. Wiebe, L. A.; Bjeldanes, L. F.; Fusarin, C. A mutagen from Fusarium moniliforme grown on corn J. Food Sci. 1981, 46, 1424-1426
7. Marasas, W. F. O. Fumonisins: their implications for human and animal health Nat. Toxins 1995, 3, 193-198
8. Bartok, T.; Tolgyesi, L.; Szekeres, A.; Varga, M.; Bartha, R.; Szecsi, A.; Bartok, M.; Mesterhazy, A. Detection and characterization of twenty-eight isomers of fumonisin B1 (FB1) mycotoxin in a solid ice culture infected with Fusarium verticillioides by reversed-phase high-performance liquid chromatography/electrospray ionization time-of-flight and ion trap mass spectrometry Rapid Commun. Mass Spectrom. 2010, 24, 35-42
9. Marasas, W. F.; Kellerman, T. S.; Gelderblom, W. C.; Coetzer, J. A.; Thiel, P. G.; Van der Lugt, J. J. Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme Onderstepoort J. Vet. Res 1988, 55, 197-203
10. Colvin, B. M.; Harrison, L. R. Fumonisin-induced pulmonary edema and hydrothorax in swine Mycopathologia 1992, 117, 79-82
11. IARC. Fumonisin B1. In IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: Some Traditional Medicines, Some Mycotoxins, Napththalene and Styrene: IARC Press: Lyon, France, 2002; Vol. 82, pp 301-366.
12. 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.; Martinez, C.; Maddox, J.; Miller, J. D.; Starr, L.; Sullards, M. C.; Roman, A. V.; Voss, K. A.; Wang, E.; Merrill, A. H. 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. 2004, 134, 711-716
13. Wang, E.; Norred, W. P.; Bacon, C. W.; Riley, R. T.; Merrill, A. H. Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme J. Biol. Chem. 1991, 266, 14486-14490
14. Abbas, H. K.; Tanaka, T.; Duke, S. O.; Porter, J. K.; Wray, E. M.; Hodges, L.; Sessions, A. E.; Wang, E.; Merrill, A. H.; Riley, R. T. Fumonisin-and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases Plant Physiol. 1994, 106, 1085-1093
15. Brandwagt, B. F.; Mesbah, L. A.; Takken, F. W.; Laurent, P. L.; Kneppers, T. J.; Hille, J.; Nijkamp, H. J. 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. 2000, 97, 4961-4966
16. Spassieva, S. D.; Markham, J. E.; Hille, J. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death Plant J. 2002, 32, 561-572
17. Glenn, A. E.; Zitomer, N. C.; Zimeri, A. M.; Williams, L. D.; Riley, R. T.; Proctor, R. H. 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. 2008, 21, 87-97
18. Sanchez-Rangel, D.; Sanchez-Nieto, S.; Plasencia, J. Fumonisin B1, a toxin produced by Fusarium verticillioides, modulates maize β-1,3-glucanase activities involved in defense response Planta 2012, 235, 965-978
19. Vicente, M.; Larios-Zarate, G.; Plasencia, J. Disruption of sphingolipid biosynthesis in Nicotiana benthamiana activates salicylic acid-dependent responses and compromises resistance to Alternaria alternata f. sp. lycopersici Planta 2013, 237, 121-136
20. Desjardins, A. E.; Munkvold, G. P.; Plattner, R. D.; Proctor, R. H. 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. 2002, 15, 1157-1164
21. Desjardins, A. E.; Plattner, R. D.; Lu, M.; Claflin, L. E. Distribution of fumonisins in maize ears infected with strains of Fusarium moniliforme that differ in fumonisin production Plant Dis. 1998, 82, 953-958
22. Desjardins, A. E.; Busman, M.; Muhitch, M.; Proctor, R. H. Complementary host-pathogen genetic analyses of the role of gumonisins in the Zea mays-Gibberella moniliformis interaction. Physiol Mol. Plant Pathol. 2007, 70, 149-160
23. Williams, L. D.; Glenn, A. E.; Zimeri, A. M.; Bacon, C. W.; Smith, M. A.; Riley, R. T. Fumonisin disruption of ceramide biosynthesis in maize roots and the effects on plant development and Fusarium verticillioides induced seedling disease J. Agric. Food Chem. 2007, 55, 2937-2946
24. Zitomer, N. C.; Glenn, A. E.; Bacon, C. W.; Riley, R. T. A single extraction method for the analysis by liquid chromatography/tandem mass spectrometry of fumonisins and biomarkers of disrupted sphingolipid metabolism in tissues of maize seedlings Anal. Bioanal. Chem. 2008, 391, 2257-2263
25. Zitomer, N. C.; Jones, S.; Bacon, C. W.; Glenn, A. E.; Baldwin, T. T.; Riley, R. T. Translocation of sphingoid bases and their 1-phosphates, but not fumonisins, from roots to aerial tissues of maize seedlings watered with fumonisins J. Agric. Food Chem. 2010, 58, 7476-7481
26. Bohorova, N.; Fenell, S.; McLean, S.; Pellegrineschi, A.; Hoisington, D. Laboratory protocols: CIMMYT applied genetic engineering lab. Mexico D.F.: CIMMYT; 1999, http://repository.cimmyt.org/xmlui/handle/10883/628.
27. Williams, L. D.; Glenn, A. E.; Bacon, C. W.; Smith, M. A.; Riley, R. T. Fumonisin production and bioavailability to maize seedlings grown from seeds inoculated with Fusarium verticillioides and grown in natural soils J. Agric. Food Chem. 2006, 54, 5694-5700
28. Glenn, A. E.; Richardson, E. A.; Bacon, C. W. Genetic and morphological characterization of a Fusarium verticillioides conidiation mutant Mycologia 2004, 96, 968-980
29. Bacon, C. W.; Hinton, D. M.; Richardson, M. D. A corn seedling assay for resistance to Fusarium moniliforme Plant Dis. 1994, 78, 302-305
30. Desjardins, A. E.; Plattner, R. D.; Stessman, R. J.; McCormick, S. P.; Millard, M. J. Identification and heritability of fumonisin insensitivity in Zea mays Phytochemistry 2005, 66, 2474-2480
31. Schroeder, J. I.; Allen, G. J.; Hugouvieux, V.; Kwak, J. M.; Waner, D. Guard cell signal transduction Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 627-658
32. Kang, Z.; Buchenauer, H. Studies on the infection process of Fusarium culmorum in wheat spikes: degradation of host cell wall components and localization of trichothecene toxins in infected tissue Eur. J. Plant Pathol. 2002, 108, 653-660
33. Balasubramanian, V.; Vashisht, D.; Cletus, J.; Sakthivel, N. Plant β-1,3-glucanases: their biological functions and transgenic expression against phytopathogenic fungi. Biotechnol. Lett. 2012, 34, 1983-1990.
34. Gupta, P.; Ravi, I.; Sharma, V. Induction of β-1,3-glucanase and chitinase activity in the defense response of Eruca sativa plants against the fungal pathogen Alternaria brassicicola. J. Plant Interact. 2013, 8, 155-161.
35. Østergaard, L.; Petersen, M.; Mattsson, O.; Mundy, J. An Arabidopsis callose synthase Plant Mol. Biol. 2002, 49, 559-566
36. Greenberg, J. T.; Guo, A. L.; Klessig, D. F.; Ausubel, F. M. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions Cell 1994, 77, 551-563
37. Frey, M.; Chomet, P.; Glawischnig, E.; Stettner, C.; Grun, S.; Winklmair, A.; Eisenreich, W.; Bacher, A.; Meeley, R. B.; Briggs, S. P.; Simcox, K.; Gierl, A. Analysis of a chemical plant defense mechanism in grasses Science 1997, 277, 696-699
38. Wicklow, D. T.; Roth, S.; Deyrup, S. T.; Gloer, J. B. A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides Mycol. Res. 2005, 109, 610-618