Field Studies on the Relationship between Fusarium verticillioides and Maize (Zea mays L.): Effect of Biocontrol Agents on Fungal Infection and Toxin Content of Grains at Harvest
Maize (Zea mays L.) is a staple food for the majority of the world's population. Fusarium verticillioides (Sacc.) Nirenberg (Teleomorph: Gibberella moniliformis Wineland; synonym: F. moniliformis) is both a saprophyte and a parasite of maize and can also be found as an endophyte. The presence of this fungus in maize constitutes an imminent risk due to its ability to produce fumonisins, mycotoxins with proven carcinogenic effects. The present work investigated biocontrol activity of Bacillus amyloliquefaciens and Microbacterium oleovorans against F. verticillioides infection and fumonisin B1 production in field-grown maize during four consecutive growing seasons. Treatment with B. amyloliquefaciens consistently reduced F. verticillioides inoculum and fumonisin content of harvested grains. F. verticillioides count and fumonisin levels correlated negatively with rainfall regimes; however, none of these parameters showed significant correlation with yields. Treatment with these biocontrol agents may improve phytosanitary quality of the grains and reduce toxicological risk in the maize agroecosystem. 1. Introduction Maize (Zea mays L.) is a staple food for the majority of the world’s population together with wheat and rice [1]. The maize crop is currently the third most traded cereal with a total production of 817 million tones in over 159 million hectares by 2009 [2]. About 35 to 40% of maize annual production of Argentina is obtained in Córdoba province [3]. Maize is mainly used as a food source but it has become the most important raw material for animal feed and for several industrial processes [4, 5]. An increasing area is now being used to cultivate this crop, not only in temperate agro-ecological zones but also in all sorts of edaphic, altitudinal, and fertility conditions; which explains its global adaptability and its many types of varieties [6]. In spite of this versatility, maize, as well as the rest of the agronomic crops, is not exempt of suffering from different diseases affecting its emergence, growth, development, and yield. Plant diseases cause global losses ranging between 9 and 22% of annual production, depending mainly on the crop and technological development of the country where the crop is [7]. Fusarium verticillioides (Sacc.) Nirenberg (Teleomorph: Gibberella moniliformis Wineland; synonym: F. moniliformis) is both a saprophyte and a parasite of maize; it can be found as a systemic endophyte in a symptomless biotrophic state or as a hemibiotrophic pathogen depending on environmental conditions [8, 9]. Regardless the occurrence of
References
[1]
J. von Braun, The World Food Situation. New Driving Forces and Required Actions, International Food Policy Research Institute (IFPRI), Washington, DC, USA, 2007.
[2]
FAO, Food and Agriculture Organization of the United Nations, “FAOSTAT, crop production statistics, maize,” 2011, http://faostat.fao.org/site/291/default.aspx.
[3]
SAGPyA, Secretaría de Agricultura, Ganadería, Pesca y Alimentos, “Reports on cereals, maize. Reports per crop, Dirección de Coordinación de Información, delegaciones y elaboración de estimaciones agropecuarias,” 2008, http://www.sagpya.gov.ar.
[4]
D. Pimentel and T. W. Patzek, “Ethanol production using corn, switchgrass, and wood; biodiesel production using soybean and sunflower,” Natural Resources Research, vol. 14, no. 1, pp. 65–76, 2005.
[5]
ILSI, Internacional Life Sciences Institute, “Maíz y nutrición. Informe sobre los usos y las propiedades nutricionales del maíz para la alimentación humana y animal,” in Recopilación de ILSI Argentina, vol. 2 of Serie de Informes Especiales, 2006.
[6]
R. K. Osboo, M. Mirabolfathy, and F. Aliakbari, “Natural deoxynivalenol contamination of corn produced in Golestan and Moqan areas in Iran,” Journal of Agricultural Science and Technology, vol. 12, no. 2, pp. 233–239, 2010.
[7]
S. L. Lenardón, “Enfermedades endémicas y emergentes de las plantas cultivadas,” Revista Ciencia Hoy, vol. 13, no. 74, 2003.
[8]
C. W. Bacon and I. E. Yates, “Endophytic root colonization by Fusarium species: histology, plant interactions and toxicity,” in Microbial Root Endophytes, B. J. E. Schulz, C. J. C. Boyle, and T. N. Sieber, Eds., Springer, Heidelberg, Germany, 2006.
[9]
C. W. Bacon, A. E. Glenn, and I. E. Yates, “Fusarium verticillioides: managing the endophytic association with maize for reduced fumonisins accumulation,” Toxin Reviews, vol. 27, no. 3-4, pp. 411–446, 2008.
[10]
IARC, International Agency for Research on Cancer, “Fumonisin B1. Some traditional herbal medicines, some mycotoxins, naphthalene and styrene,” IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 82, pp. 301–366, 2002.
[11]
R. N. Strange and P. R. Scott, “Plant disease: a threat to global food security,” Annual Review of Phytopathology, vol. 43, pp. 83–116, 2005.
[12]
P. Koirala, S. Dhakal, and A. S. Tamrakar, “Pesticide application and food safety issue in Nepal,” The Journal of Agriculture and Environment, vol. 10, pp. 111–114, 2009.
[13]
C. Potera, “Pesticides disrupt nitrogen fixation,” Environmental Health Perspectives, vol. 115, no. 12, p. 579, 2007.
[14]
R. A. Slepecky and H. E. Hemphill, “The genus Bacillus,” in The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K. Schleifer, Eds., p. 4126, Springer, New York, NY, USA, 1992.
[15]
J. G. Holt, N. R. Krieg, P. H. A. Sneath, J. T. Staley, and S. T. Williams, Bergey’s Manual of Determinative Bacteriology, Williams & Wilkins, Baltimore, Md, USA, 9th edition, 1994.
[16]
P. Pereira, A. Nesci, and M. Etcheverry, “Efficacy of bacterial seed treatments for the control of Fusarium verticillioides in maize,” BioControl, vol. 54, no. 1, pp. 103–111, 2009.
[17]
S. W. Ritchie and J. J. Hanway, “How a corn plant develops,” Special Report 48, University of Science and Technology. Cooperative Extension Service, Ames, Iowa, USA, 1982.
[18]
SAGPyA, Secretaría de Agricultura, Ganadería, Pesca y Alimentos, “Norma de comercialización de maíz 1075/94. norma XII,” 1994, http://www.cosechaypostcosecha.org/data/postcosecha/basescomercializacion/basescomercializacionmaiz.pdf.
[19]
P. E. Nelson, T. A. Toussoun, and W. F. O. Marasas, Fusarium Species: An Illustrated Manual for Identification, Pennsylvania State University, University Park, Pa, USA, 1983.
[20]
J. F. Leslie and B. A. Summerell, The Fusarium Laboratory Manual, Blackwell Publishing Professional, Ames, Iowa, USA, 2006.
[21]
G. S. Shephard, E. W. Sydenham, P. G. Thiel, and W. C. A. Gelderblom, “Quantitative determination of fumonisins B1 and B2 by HPLC with fluorescence detection,” Journal of Liquid Chromatography, vol. 13, no. 10, pp. 2077–2087, 1990.
[22]
ADCON Telemetry Field Station, Dependent of Aseagro and Universidad Nacional de Río Cuarto http://www.aseagro.com.ar.
[23]
J. Dobereiner, “Biological nitrogen fixation in the tropics: social and economic contributions,” Soil Biology and Biochemistry, vol. 29, no. 5-6, pp. 771–774, 1997.
[24]
G. Schilling, A. Gransee, A. Deubel, G. Lezovic, and S. Ruppel, “Phosphorus availability, root exudates and microbial activity in the rhizosphere,” Zeitschrift für Pflanzenern？hrung und Bodenkunde, vol. 161, pp. 465–478, 1998.
[25]
J. S？rensen, “The rhizosphere as a habitat for soil microorganisms,” in Modern Soil Microbiology, J. D. van Elsas, J. T. Trevors, and E. M. H. Wellington, Eds., pp. 21–45, Marcel Dekker, New York, NY, USA, 1997.
[26]
J. Kozdrój, J. T. Trevors, and J. D. van Elsas, “Influence of introduced potential biocontrol agents on maize seedling growth and bacterial community structure in the rhizosphere,” Soil Biology and Biochemistry, vol. 36, no. 11, pp. 1775–1784, 2004.
[27]
F. Ciccillo, A. Fiore, A. Bevivino, C. Dalmastri, S. Tabacchioni, and L. Chiarini, “Effects of two different application methods of Burkholderia ambifaria MCI 7 on plant growth and rhizospheric bacterial diversity,” Environmental Microbiology, vol. 4, no. 4, pp. 238–245, 2002.
[28]
D. A. Presello, G. Botta, J. Iglesias, and G. H. Eyhérabide, “Effect of disease severity on yield and grain fumonisin concentration of maize hybrids inoculated with Fusarium verticillioides,” Crop Protection, vol. 27, no. 3–5, pp. 572–576, 2008.
[29]
A. E. Desjardins, R. D. Plattner, M. Lu, and L. E. Claflin, “Distribution of fumonisins in maize ears infected with strains of Fusarium moniliforme that differ in fumonisin production,” Plant Disease, vol. 82, no. 8, pp. 953–958, 1998.
[30]
M. J. Cantalejo, J. M. Carrasco, and E. Hernández, “Incidence and distribution of Fusarium species associated with feeds and seeds from Spain,” Revista Iberoamericana de Micologia, vol. 15, no. 1, pp. 36–39, 1998.
[31]
J. D. Miller, “Factors affecting the occurrence of fumonisin in corn,” in Proceedings of the International Conference on the Toxicology of Fumonisin, Arlington, Va, USA, June, 1999.
[32]
P. Fandohan, K. Hell, W. F. O. Marasas, and M. J. Wingfield, “Infection of maize by Fusarium species and contamination with fumonisin in Africa,” African Journal of Biotechnology, vol. 2, no. 12, pp. 570–579, 2003.
[33]
J. D. Miller, M. E. Savard, A. W. Schaafsma, K. A. Seifert, and L. M. Reid, “Mycotoxin production by Fusarium moniliforme and Fusarium proliferatum from Ontario and occurrence of fumonisin in the 1993 corn crop,” Canadian Journal of Plant Pathology, vol. 17, pp. 233–239, 1995.
[34]
B. J. Bush, M. L. Carson, M. A. Cubeta, W. M. Hagler, and G. A. Payne, “Infection and fumonisin production by Fusarium verticillioides in developing maize kernels,” Phytopathology, vol. 94, no. 1, pp. 88–93, 2004.
[35]
F. G. Rojo, M. M. Reynoso, M. Ferez, S. N. Chulze, and A. M. Torres, “Biological control by Trichoderma species of Fusarium solani causing peanut brown root rot under field conditions,” Crop Protection, vol. 26, no. 4, pp. 549–555, 2007.
[36]
W. C. A. Gelderblom, K. Jaskiewicz, W. F. O. Marasas et al., “Fumonisins—novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme,” Applied and Environmental Microbiology, vol. 54, no. 7, pp. 1806–1811, 1988.
[37]
J. W. Bennett and M. Klich, “Mycotoxins,” Clinical Microbiology Reviews, vol. 16, no. 3, pp. 497–516, 2003.
[38]
B. H. Bluhm and C. P. Woloshuk, “Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels,” Molecular Plant-Microbe Interactions, vol. 18, no. 12, pp. 1333–1339, 2005.
[39]
P. Fandohan, B. Gnonlonfin, K. Hell, W. F. O. Marasas, and M. J. Wingfield, “Natural occurrence of Fusarium and subsequent fumonisin contamination in preharvest and stored maize in Benin, West Africa,” International Journal of Food Microbiology, vol. 99, no. 2, pp. 173–183, 2005.
[40]
P. F. Ross, A. E. Ledet, D. L. Owens et al., “Experimental equine leukoencephalomalacia, toxic hepatosis, and encephalopathy caused by corn naturally contaminated with fumonisins,” Journal of Veterinary Diagnostic Investigation, vol. 5, no. 1, pp. 69–74, 1993.
[41]
P. G. Thiel, G. S. Shephard, E. W. Sydenham, W. F. O. Marasas, P. E. Nelson, and T. M. Wilson, “Levels of fumonisins B1 and B2 in feeds associated with confirmed cases of equine leukoencephalomalacia,” Journal of Agricultural and Food Chemistry, vol. 39, no. 1, pp. 109–111, 1991.
[42]
G. K. Motelin, W. M. Haschek, D. K. Ness et al., “Temporal and dose-response features in swine fed corn screenings contaminated with fumonisin mycotoxins,” Mycopathologia, vol. 126, no. 1, pp. 27–40, 1994.
[43]
J. P. Rheeder, W. F. O. Marasas, P. G. Thiel, E. W. Sydenham, G. S. Shephard, and D. J. Van Schalkwyk, “Fusarium moniliforme and fumonisins in relation to human oesophageal cancer in Transkei,” Phytopathology, vol. 82, pp. 353–357, 1992.
[44]
S. N. Chulze, M. Etcheverry, S. Lecumberry et al., “Fumonisin production on irradiated corn kernels: effect of inoculum size,” Journal of Food Protection, vol. 62, no. 7, pp. 814–817, 1999.
[45]
C. Y. Warfield and D. G. Gilchrist, “Influence of kernel age on fumonisin B1 production in maize by Fusarium moniliforme,” Applied and Environmental Microbiology, vol. 65, no. 7, pp. 2853–2856, 1999.
[46]
P. G. Thiel, W. F. O. Marasas, E. W. Sydenham, G. S. Shephard, and W. C. A. Gelderblom, “The implications of naturally occurring levels of fumonisins in corn for human and animal health,” Mycopathologia, vol. 117, no. 1-2, pp. 3–9, 1992.
[47]
E. W. Sydenham, G. S. Shephard, P. G. Thiel, and W. F. O. Marasas, “Fumonisins in Argentinian field-trial corn,” Journal of Agricultural and Food Chemistry, vol. 41, no. 6, pp. 891–895, 1993.
[48]
M. B. Doko, S. Rapior, A. Visconti, and J. E. Schj？th, “Incidence and levels of fumonisin contamination in maize genotypes grown in Europe and Africa,” Journal of Agricultural and Food Chemistry, vol. 43, no. 2, pp. 429–434, 1995.
[49]
A. B. F. Bittencourt, C. A. F. Oliveira, P. Dilkin, and B. Corrêa, “Mycotoxin occurrence in corn meal and flour traded in S？o Paulo, Brazil,” Food Control, vol. 16, no. 2, pp. 117–120, 2005.
[50]
Official Journal of the European Union, “Commission recommendation of 17 August on the prevention and reduction of Fusarium toxins in cereals and cereal products,” 2006, http://eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:234:0035:0040:EN:PDF.
[51]
FDA, Food and Drug Administration, “Background paper in support of fumonisin levels in corn and corn products intended for human consumption,” Center for Food Safety and Applied Nutrition, 2001, http://www.fda.gov/Food/FoodSafety/FoodContaminantsAdulteration/NaturalToxins/ucm212899.htm.
