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Fusarium verticillioides and fumonisin contamination in Bt and non-Bt maize cultivated in Brazil

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Abstract

Fusarium verticillioides is one of the main pathogens of maize, causing ear and stalk rots. This fungus is also able to produce high levels of fumonisins, which have been linked to various illnesses in humans and animals. Previous studies have shown that maize hybrids genetically modified with the cry genes from the bacterium Bacillus thuringiensis (Bt) presented lower incidence of F. verticillioides and fumonisin levels, presumably through the reduction of insects, which could act as vectors of fungi. The aim of this study was to assess the incidence of F. verticillioides and the concentration of fumonisins in Bt and isogenic non-Bt hybrids (2B710Hx, 30F35YG, 2B710, and 30F35, respectively). The samples of 2B710Hx and 30F35YG presented lower F. verticillioides frequency than 2B710 and 30F35 samples. However, there was no statistical difference between fumonisin contamination when Bt and non-Bt samples were compared (P > 0.05). The results suggest that other environmental parameters could possibly trigger fumonisin production during plant development in the field; consequently, other management strategies should be applied to aid controlling fumonisin contamination in maize.

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References

  • Almeida AP, Fonseca H, Fancelli AL, Direito GM, Ortega EM, Correa B (2002) Mycoflora and fumonisin contamination in Brazilian corn from sowing to harvest. J Agric Food Chem 50:3877–3882

    Article  CAS  PubMed  Google Scholar 

  • Almeida AP, Sabino M, Fonseca H, Correa B (2005) Milho recém-colhido no Brasil: interação da microbiota fúngica, fatores abióticos e ocorrência de fumonisinas. Rev Inst Adolfo Lutz 64:1–9

    Google Scholar 

  • Berjark P (1984) Report of seed storage committee working group on the effects of storage fungi on seed viability: 1980-1983. Seed Sci and Technol 12:233–253

    Google Scholar 

  • Bock CH, Cotty PJ (1999) The relationship of gin date to aflatoxin contamination of cottonseed in Arizona. Plant Dis 83:279–285

    Article  Google Scholar 

  • Bowers EL, Hellmich RL, Munkvold GP (2013) Vip3Aa and Cry1Ab proteins in maize reduce Fusarium ear rot and fumonisins by deterring kernel injury from multiple Lepidopteran pests. W Mycotoxin J 6:127–135

    Article  Google Scholar 

  • Bussab WO, Morettin PA (2011) Estatística Básica. Saraiva, São Paulo

    Google Scholar 

  • Clements MJ, Campbell KW, Maragos C, Pilcher JM, Headrick JM, Pataky JK, White DG (2003) Influence of Cry1Ab protein and hybrid genotype on fumonisin contamination and Fusarium ear rot of corn. Crop Sci 43:1283–1293

    Article  CAS  Google Scholar 

  • CONAB Companhia Nacional de Abastecimento (2016) Estudos de prospecção de mercado - Safra 2015/2016. www.conab.gov.br. Acessed 15 June 2016

  • Degola F, Berni E, Dall’asta C, Spotti E, Marchelli R, Ferrero I, Restivo FM (2007) A multiplex RT-PCR approach to detect aflatoxigenic strains of Aspergillus flavus. J Appl Microbiol 103:409–441

    Article  CAS  PubMed  Google Scholar 

  • Delp RB, Stewell LJ, Marois JJ (1986) Evaluation of field sampling techniques for estimation of disease incidence. Phytopathol 76:1299–1305

    Article  Google Scholar 

  • Doko MB, Rapior S, Visconti A, Schjoth JE (1995) Incidence and levels of fumonisin contamination in maize genotypes grown in Europe and Africa. J Agric Food Chem 43:429–434

    Article  CAS  Google Scholar 

  • Dowd PF (2000) Indirect reduction of ear molds and associated mycotoxins in Bacillus thuringiensis corn under controlled and open field conditions: utility and limitations. J Econ Entomol 93:1669–1679

    Article  CAS  PubMed  Google Scholar 

  • Duvick J (2001) Prospects for reducing fumonisin contamination of maize through genetic modification. Environ Health Persp 109:337–342

    Article  CAS  Google Scholar 

  • ECR European Commission Regulation (2007) no 1126/2007: setting maximum levels for certain contaminants in foodstuffs as regards Fusarium toxins in maize and maize products. http://eur-lex.europa.eu. Acessed 15 June 2016

  • Fandohan P, Gnonlonfin B, Hell K, Marasas WF, Wingfield MJ (2005) Natural occurrence of Fusarium and subsequent fumonisin contamination in preharvest and stored maize in Benin, West Africa. Int J Food Microbiol 99:173–183

    Article  CAS  PubMed  Google Scholar 

  • FAO Food and Agricultural Organization of the United States (2016) Food outlook. Biannual report on global food markets. http://www.fao.org/3/a-i5703e.pdf. Accessed 12 Sept 2016

  • FDA Food and Drug Administration (2001) Background paper in support of fumonisin levels in corn and corn products intended for human consumption. http://vm.cfsan. fda.gov/~dms/fumonbg1.html. Accessed 21 June 2016

  • Frisvad JC, Samson RA (1991) Filamentous fungi in foods and feeds: ecology spoilage and mycotoxins production. In: Arora DK, Mukerji KG, Marth EH (eds) Handbook of applied mycology volume 3: food and feeds. Marcel Dekker, New York, pp 31–69

    Google Scholar 

  • Geiser DM, Jiménez-Gasco MM, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) Fusarium-ID V.1.0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479

    Article  CAS  Google Scholar 

  • Hirooka EY, Yamaguchi MM, Aoyama S, Sugiura Y, Ueno Y (1996) The natural occurrence of fumonisins in Brazilian corn kernels. Food Addit Contam 13:173–183

    Article  CAS  PubMed  Google Scholar 

  • Hurst CJ (2001) Manual of environmental microbiology. American Society for Microbiology, Washington

    Google Scholar 

  • IARC International Agency of Research on Cancer (1993) Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monogr Eval Carcinog Risk Hum 56:445–466

    Google Scholar 

  • JECFA Joint FAO/WHO Expert Committee on Food Additives (2012) Tolerable or acceptable daily intakes, other toxicological information and information on specifications. http://www.fao.org/3/a-at873e.pdf. Accessed 10 Dec 2016

  • Jouany JP (2007) Methods for preventing decontamination and minimizing the toxicity of mycotoxins in feeds. Anim Feed Sci Technol 137:342–362

    Article  CAS  Google Scholar 

  • Kellerman T, Marasas WF, Thiel PG, Gelderblom WC, Cawood M, Coetzer JA (1990) Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1. J Vet Res 57:269–275

    CAS  Google Scholar 

  • Leslie JF, Logrieco A (2014) Mycotoxin reduction in grain chains. John Wiley and Sons, Inc., Iowa

    Book  Google Scholar 

  • Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing, Iowa

    Book  Google Scholar 

  • Marasas WFO, Kriek NPJ, Wiggins VM, Steyn PS, Towers DK, Hastie TJ (1979) Incidence, geographical distribution, and toxicity of Fusarium species in South African corn. Phytopathol 69:181–185

    Article  Google Scholar 

  • Marasas WFO, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-Van Waes J, Missmer SS, Cabrera J, Torres O, Gelderblom WC, Allegood J, Martínez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman AV, Voss KA, Wang E, Merrill AH 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

    CAS  PubMed  Google Scholar 

  • Michelotto MD, Pereira AD, Finoto EL, Freitas RS (2011) Controle de pragas em híbridos de milho geneticamente modificados. Grandes Culturas 145:36–38

    Google Scholar 

  • Miller JD (2001) Factors that affect the occurrence of fumonosin. Environ Health Persp 109:321–324

    Article  CAS  Google Scholar 

  • Miller SS, Reid LM, Harris LJ (2007) Colonization of maize silks by Fusarium graminearum, the causative organism of gibberella ear rot. Can J Bot 85:369–376

    Article  Google Scholar 

  • Mills JT (1989) Ecology of mycotoxigenic Fusarium species on cereal seeds. J Food Protect 52:737–742

    Article  Google Scholar 

  • Missmer SA, Suarez L, Felkner M, Wang E, Merrill AH Jr, Rothman KJ, Hendricks KA (2006) Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border. Environ Health Perspect 114:237–241

    Article  PubMed  Google Scholar 

  • Munkvold GP (2003) Cultural and genetic approaches to managing mycotoxins in maize. Annu Rev Phytopathol 41:99–116

    Article  CAS  PubMed  Google Scholar 

  • Munkvold GP, Hellmich RL, Rice LG (1999) Comparison of fumonisin concentration in kernels of transgenic Bt maize hybrids and nontransgenic hybrids. Plant Dis 83:130–138

    Article  Google Scholar 

  • Orsi RB, Correa B, Pozzi CR, Schammass EA, Nogueira JR, Dias SMC, Malozzi MAB (2000) Mycoflora and occurrence of fumonisins in freshly harvest and stored hybrid maize. J Stored Prod Res 36:75–87

    Article  CAS  Google Scholar 

  • Ostry V, Ovesna J, Skarkova J, Pouchova V, Ruprich J (2010) A review on comparative data concerning Fusarium mycotoxins in Bt maize and non-Bt isogenic maize. Mycotoxin Res 26:141–145

    Article  CAS  PubMed  Google Scholar 

  • Papst C, Utz HF, Melchinger AE, Eder J, Magg T, Klein D, Bohn M (2005) Mycotoxins produced by Fusarium spp. in isogenic Bt vs. non Bt maize hybrids under European corn borer pressure. Agron J 97:219–224

    CAS  Google Scholar 

  • Pitt JI, Hocking AD (2009) Fungi and food spoilage. Aspen Pub Inc, Gaithersburg

    Book  Google Scholar 

  • Pomeranz Y (1982) Biochemical, functional and nutritional changes during storage. In: Christensen CM (ed) Storage of cereal grains and their products. American Association of Cereal Chemists, St. Paul, pp 56–114

    Google Scholar 

  • Pozzi CR, Correa B, Gambale W, Paula CR, Chacon-Reche NO, Meirelles MC (1995) Post-harvest and stored corn in Brazil: mycoflora interaction, abiotc factors and mycotoxins occurrence. Food Addit Contam 12:313–319

    Article  CAS  PubMed  Google Scholar 

  • Ranum P, Peña-Rosas JP, Garcia-Casal MN (2014) Global maize production, utilization, and consumption. Ann N Y Acad Sci 1312:105–112

    Article  PubMed  Google Scholar 

  • Rocha LO, Nakai VK, Braghini R, Reis TA, Kobashigawa E, Correa B (2009) Mycoflora and co-occurrence of fumonisins and aflatoxins in freshly harvested corn in different regions of Brazil. Int J Mol Sci 10:5090–5193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha LO, Barroso VM, Andrade LJ, Pereira GHA, Ferreira-Castro FL, Duarte AP, Michelotto MD, Correa B (2016) FUM gene expression profile and fumonisin production by Fusarium verticillioides inoculated in Bt and non-Bt maize. Front in Microbiol. doi:10.3389/fmicb.2015.01503

    Google Scholar 

  • Saxena D, Sottzky G (2000) Insecticidal toxin from Bacillus thuringiensis released from roots of transgenic Bt corn in vitro and in situ. FEMS Microbiol Ecol 33:35–39

    Article  CAS  PubMed  Google Scholar 

  • Schaafsma AW, Hooker DC (2007) Climatic models to predict occurrence of Fusarium toxins in wheat and maize. Int J Food Microbiol 119:116–125

    Article  CAS  PubMed  Google Scholar 

  • Shelby RA, White DG, Burke EM (1994) Differential fumonisin production in maize hybrids. Plant Dis 78:582–584

    Article  CAS  Google Scholar 

  • Shephard GS, Thiel PG, Stockenstrom S, Sydenham EW (1996) Worldwide survey of fumonisin contamination of corn and corn-based products. J AOAC Int 79:671–687

    CAS  PubMed  Google Scholar 

  • Visconti A (1996) Fumonisins in maize genotypes grown in various geographic areas. Adv Exp Med Biol 392:193–204

    Article  CAS  PubMed  Google Scholar 

  • Visconti A, Solfrizzo M, Girolamo A (2001) Determination of fumonisins B1 and B2 in corn and corn flakes by liquid chromatography with immunoaffinity column clean up: collaborative study. Food Chem Contam 84:1828–1837

    CAS  Google Scholar 

  • Wu F (2006) Mycotoxin reduction in Bt corn: potential economic, health, and regulatory impacts. Transgenic Res 15:277–289

    Article  PubMed  Google Scholar 

  • Wu F, Miller JD, Casman EA (2004) Bt corn and mycotoxin reduction: economic impacts in the United States and the developing world. J Toxicol - Toxin Rev 23:397–424

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Microbiology Department, Institute of Biomedical Sciences, University of Sao Paulo, Avenue Prof. Lineu Prestes, 1374, Laboratory 249, Sao Paulo, SP, 05508-000, Brazil

    Vinícius M. Barroso, Liliana O. Rocha, Tatiana A. Reis, Gabriela M. Reis & Benedito Correa

  2. Centre of Grains and Fibres, Agronomic Institute of Campinas, Agro-Business Agency of Sao Paulo (Agência Paulista de Tecnologia dos Agronegócios (APTA)), Avenue Theodureto de Almeida Camargo, 1500, Campinas, SP, 13075-630, Brazil

    Aildson P. Duarte & Marcos D. Michelotto

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  1. Vinícius M. Barroso
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  2. Liliana O. Rocha
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  3. Tatiana A. Reis
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  4. Gabriela M. Reis
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  6. Marcos D. Michelotto
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  7. Benedito Correa
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Correspondence to Benedito Correa.

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This investigation was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Brazil.

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Barroso, V.M., Rocha, L.O., Reis, T.A. et al. Fusarium verticillioides and fumonisin contamination in Bt and non-Bt maize cultivated in Brazil. Mycotoxin Res 33, 121–127 (2017). https://doi.org/10.1007/s12550-017-0271-4

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  • DOI: https://doi.org/10.1007/s12550-017-0271-4

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