Abstract
Novel strategies that address vitamin A deficiency have been developed, such as high-carotenoid maize, a biofortified transgenic maize line rich in carotenoids generated by genetic transformation. The South African white maize inbred (M37W), which is devoid of carotenoids, was engineered to accumulate high levels of β-carotene (provitamin A), lutein, and zeaxanthin. Maize seeds contaminated with fumonisins and other mycotoxins pose a serious threat to both humans and livestock. During three consecutive harvests, the fungal incidence and the fumonisin and aflatoxin content of maize seeds grown in an experimental field in Catalonia (Northeastern Spain) were evaluated. Fungal infection was similar in high-carotenoid maize and its isogenic line, with Fusarium verticillioides being the most prevalent fungus in all the harvests. Neither Aspergillus spp. nor aflatoxin contamination was found. Fumonisin levels were lower in high carotenoid than in its isogenic line, but this reduction was statistically significant in only 2 of the 3 years of study. Our results suggest that high carotenoid content reduces fumonisin levels in maize grains.
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Abbreviations
- AFs:
-
Aflatoxins
- FBs:
-
Fumonisins
- FB1 :
-
Fumonisin B1
- FB2 :
-
Fumonisin B2
- AFB1 :
-
Aflatoxin B1
- AFB2 :
-
Aflatoxin B2
- AFG1 :
-
Aflatoxin G1
- AFG2 :
-
Aflatoxin G2
- HPLC:
-
High-performance liquid chromatography
References
AOAC International (2005) International Method 925.09B. Official methods of analysis, 18th edn. AOAC, Inc., Gaithersburg
Atanasova-Pénichon V, Barreau C, Richard-Forget F (2016) Antioxidant secondary metabolites in cereals: potential involvement in resistance to Fusarium and mycotoxin accumulation. Front Microbiol 7:1–16
Bakan B, Melcion D, Richard-Molard D, Cahagnier B (2002) Fungal growth and Fusarium mycotoxin content in isogenic traditional maize and genetically modified maize grown in France and Spain. J Agric Food Chem 50:728–731
Berman J (2016) Unraveling the molecular bases of carotenoid biosynthesis in maize. Doctoral Thesis, University of Lleida, Lleida, Spain, January 2016
Blandino M, Reyneri A (2007) Comparison between normal and waxy maize hybrids for Fusarium-toxin contamination in NW Italy. Maydica 52:127–134
Bluhm BH, Woloshuk CP (2005) Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels. Mol Plant-Microbe Interact 18:1333–1339
Boutigny AL, Richard-Forget F, Barreau C (2008) Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. Eur J Plant Pathol 121:411–423
Cano-Sancho G, Ramos AJ, Marín S, Sanchis V (2012) Occurrence of fumonisins in Catalonia (Spain) and an exposure assessment of specific population groups. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 29:799–808
Cao A, Santiago R, Ramos AJ, Souto XC, Aguín O, Malvar RA, Butrón A (2014) Critical environmental and genotypic factors for Fusarium verticillioides infection, fungal growth and fumonisin contamination in maize grown in northwestern Spain. Int J Food Microbiol 177:63–71
Delgado RM, Sulyok M, Jirsa O, Spitzer T, Krska R, Polišenská I (2014) Relationship between lutein and mycotoxin content in durum wheat. Food Addit Contam Part A 31:1274–1283
Demeke T, Clear RM, Patrick SK, Gaba D (2005) Species-specific PCR-based assays for the detection of Fusarium species and a comparison with the whole seed agar plate method and trichothecene analysis. Int J Food Microbiol 103:271–284
Desjardins AE (2006) Fusarium mycotoxins : chemistry, genetics and biology. The American Phytopathological Society (APS) Press, St. Paul
European Commission (2006a) Commision Regulation (EC) No. 401/2006 of 23 February 2006 laying down the methods of sampling and analysis for the official control of the levels of mycotoxins in foodstuffs. Off J Eur Union L70:12–34
European Commission (2006b) Commision Regulation (EC) No. 1881/2006, of 19 December 2006, setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union L364:5–24
European Commission (2007) Commision Regulation (EC) No. 1126/2007 of 28 September 2007, amending Regulation (EC) No. 1881/2006, setting maximum levels for certain contaminants in foodstuffs as regards Fusarium toxins in maize and maize products. Off J Eur Union L255:14–17
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330
Harrison LR, Colvin BM, Greene JT, Newman LE, Cole JR (1990) Pulmonary edema and hydrothorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. J Vet Diagnostic Investig 2:217–221
International Agency for Research on Cancer (IARC) (2002) Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monogr. Eval. Carcinog Risks Humans 82:169–366
International Agency for Research on Cancer (IARC) (2012) Aflatoxins. Chemical agents and related occupations. IARC Monogr Eval Carcinog Risks Humans 100 F:226–248
Joint FAO/WHO Expert Committee on Food Additives (JECFA) (2001) Safety evaluation of certain mycotoxins in food. 56th meeting of the JECFA, International Programme on Chemical Safety. WHO, Geneva, WHO Food Additives Series No. 47
Jurado M, Vázquez C, Marín S, Sanchis V, González-Jaén MT (2006) PCR-based strategy to detect contamination with mycotoxigenic Fusarium species in maize. Syst Appl Microbiol 29:681–689
Kellerman TS, Marasas WFO, Thiel PG, Gelderblom WCA, Cawood ME, Coetzer JAW (1990) Leukoencephalomacia in two horses induced by oral dosing of fumonisin B1. Onderstepoort J Vet Res 57:269–275
Marasas WFO (2001) Discovery and occurrence of the fumonisins: a historical perspective. Environ Health Perspect 109:239–243
Marín S, Magan N, Ramos AJ, Sanchis V (2004) Fumonisin-producing strains of Fusarium: a review of their ecophysiology. J Food Prot 67:1792–1805
Marín S, Ramos AJ, Cano-Sancho G, Sanchis V (2012) Reduction of mycotoxins and toxigenic fungi in the mediterranean basin maize chain. Phytopathol Mediterr 51:93–118
Marín S, Ramos AJ, Sanchis V (2013) Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem Toxicol 60:218–237
Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J, Perez Conesa D, Ros G, Sandmann G, Capell T, Christou P (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci U S A 106:7762–7767
Nicholson P, Simpson DR, Weston G, Rezanoor HN, Lees AK, Parry DW, Joyce D (1998) Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiol Mol Plant Pathol 53:17–37
Norton RA (1997) Effect of carotenoids on aflatoxin B1 synthesis by Aspergillus flavus. Phytopathology 87:814–821
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci U S A 95:2044–2049
O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylo Evol 7:103–116
Patiño B, Mirete S, González-Jaén MT, Mulé G, Rodriguez MT, Vázquez C (2004) PCR detection assay of fumonisin-producing Fusarium verticillioides strains. J Food Prot 67:1278–1283
Picot A, Atanasova-Pénichon V, Pons S, Marchegay G, Barreau C, Pinson-Gadais L, Roucolle J, Daveau F, Caron D, Richard-Forget F (2013) Maize kernel antioxidants and their potential involvement in Fusarium ear rot resistance. J Agric Food Chem 61:3389–3395
Picot A, Barreau C, Pinson-Gadais L, Caron D, Lannou C, Richard-Forget F (2010) Factors of the Fusarium verticillioides-maize environment modulating fumonisin production. Crit Rev Microbiol 36:221–231
Picot A, Barreau C, Pinson-Gadais L, Piraux F, Caron D, Lannou C, Richard-Forget F (2011) The dent stage of maize kernels is the most conducive for fumonisin biosynthesis under field conditions. Appl Environ Microbiol 77:8382–8390
Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, Berlin
Reverberi M, Ricelli A, Zjalic S, Fabbri AA, Fanelli C (2010) Natural functions of mycotoxins and control of their biosynthesis in fungi. Appl Microbiol Biotechnol 87:899–911
Santiago R, Cao A, Butrón A (2015) Genetic factors involved in fumonisin accumulation in maize kernels and their implications in maize agronomic management and breeding. Toxins 7:3267–3296
Servei Metereològic de Catalunya http://www.meteo.cat. Accessed 21 June 2016
Shephard GS (2008) Determination of mycotoxins in human foods. Chem Soc Rev 37:2468–2477
Stahl W, Sies H (2003) Antioxidant activity of carotenoids. Mol Asp Med 24:345–351
Sydenham EW, Shephard GS, Thiel PG, Stockenström S, Snijman P (1996) Liquid chromatographic determination of fumonisins B1, B2 and B3 in corn: AOAC-IUPAC collaborative study. J AOAC Int 79:688–696
Velluti A, Marín S, Sanchis V, Ramos AJ (2001) Note. Occurrence of fumonisin B1 in Spanish corn-based foods for animal and human consumption. Food Sci Technol Int 7:433–437
Wang E, Norred WP, Bacon CW, Riley RT, Merril AH (1991) Inhibition of sphingolipids biosynthesis by fumonisins. J Biol Chem 266:14486–14490
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc., New York, pp. 315–322
World Health Organization (WHO) (2009) Global prevalence of vitamin A deficiency in populations at risk 1995–2005. WHO Global database on vitamin A deficiency. WHO, Geneva
Wicklow DT, Norton RA, McAlpin CE (1998) β-Carotene inhibition of aflatoxin biosynthesis among Aspergillus flavus genotypes from Illinois corn. Mycoscience 39:167–172
Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D (2004) Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr 80:1106–1122
Zhu C, Naqvi S, Breitenbach J, Sandmann G, Christou P, Capell T (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci U S A 105:18232–18237
Acknowledgments
The study was supported by La Caixa (Recercaixa project PC084082 VitaMaize: high-quality and safe food through antioxidant fortified maize), the Agrotecnio Center, the Catalonian Government (2014 SGR 1296 Agricultural Biotechnology Research Group and XaRTA Reference Network on Food Technology) and the Spanish Ministry of Economy and Competitiveness (BIO2014-54441-P). J. Díaz-Gómez thanks the University of Lleida for a pre-doctoral grant. The authors would like to thank the Agricultural Biotechnology group of the University of Lleida, Antonio Michelena, and Jaume Lloveras for their work in the experimental field.
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Díaz-Gómez, J., Marín, S., Nogareda, C. et al. The effect of enhanced carotenoid content of transgenic maize grain on fungal colonization and mycotoxin content. Mycotoxin Res 32, 221–228 (2016). https://doi.org/10.1007/s12550-016-0254-x
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DOI: https://doi.org/10.1007/s12550-016-0254-x