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Assessing white maize resistance to fumonisin contamination

European Journal of Plant Pathology volume 138, pages 283–292 (2014)Cite this article

Abstract

Genetic improvement is an emerging method to reduce the levels of fumonisin (FB) contamination in maize, but breeding advances depend on the development of suitable methods to accurately assess the performance of different cultivars. Our study focused on characterizing a local isolate of Fusarium verticillioides; comparing artificial inoculation techniques with this isolate (injection into kernels and down the silk channel); and assessing white maize resistance under artificial vs. natural inoculation. The fungal growth rate significantly increased with temperature and water activity a w. The optimum growth rate, corresponding with the shortest phase of initial growth, occurred at 25–30 °C and 0.99 a w. Under silk inoculation with this isolate, the hybrid EP10 × EC22 accumulated significantly less FBs than the other hybrids, whereas, under kernel inoculation, differences among hybrids were not significant (P ≤ 0.05). The local isolate of F. verticillioides produced FBs and responded to the usual environmental conditions during maize kernel ripening in northwestern Spain. Inoculation with this isolate is recommended because it is aggressive, toxigenic, and adapted to the local environment. Silk inoculation was the only method that allowed a clear distinction among genotypes based on differences in resistance to FB accumulation. Resistance to natural and artificial inoculations was confirmed for the hybrid EP10 × EC22.

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References

  • Avantaggiato, G., Quaranta, F., Desiderio, E., & Visconti, A. (2003). Fumonisin contamination of maize hybrids visibly damaged by Sesamia. Journal of the Science of Food and Agriculture, 83, 13–18.

    Article  CAS  Google Scholar 

  • Baranyi, J., & Roberts, T. A. (1994). A dynamic approach to predicting bacterial growth in food. International Journal of Food Microbiology, 23, 277–294.

    Article  CAS  PubMed  Google Scholar 

  • Bennett, J. W., & Klich, M. (2003). Mycotoxins. Clinical Microbiology Reviews, 16, 497–516.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bragulat, M. R., Abarca, M. L., & Cabanes, F. J. (2001). An easy screening method for fungi producing ochratoxin A in pure culture. International Journal of Food Microbiology, 71, 139–144.

    Article  CAS  PubMed  Google Scholar 

  • Bush, B. J. (2001). Fusarium verticillioides infection, fumonisin contamination and resistance evaluation in North Carolina maize. Raleigh: Master’s thesis. North Carolina State Univ.

    Google Scholar 

  • Butrón, A., Santiago, R., Mansilla, P., Pintos-Varela, C., Ordas, A., & Malvar, R. A. (2006). Maize (Zea mays L.) genetic factors for preventing fumonisin contamination. Journal of Agricultural and Food Chemistry, 54, 6113–6117.

    Article  PubMed  Google Scholar 

  • Butrón, A., Revilla, P., Sandoya, G., Ordás, A., & Malvar, R. A. (2009). Resistance to reduce corn borer damage in maize for bread. Crop Protection, 28, 134–138.

    Article  Google Scholar 

  • CAST. (2003). Mycotoxins—risks in plant, animal and human systems, task force report, No. 139 (pp. 1–191). Ames: Council for Agricultural Science and Technology.

    Google Scholar 

  • Clements, M. J., Kleinschmidt, C. E., Maragos, C. M., Pataky, J. K., & White, D. G. (2003). Evaluation of inoculation techniques for fusarium ear rot and fumonisin contamination of corn. Plant Disease, 87, 147–153.

    Article  CAS  Google Scholar 

  • Duncan, K. E., & Howard, R. J. (2010). Biology of Maize Kernel Infection by Fusarium verticillioides. Molecular Plant-Microbe Interactions, 23, 6–16.

    Article  CAS  PubMed  Google Scholar 

  • Eller, M. S., Holland, J. B., & Payne, G. A. (2008). Breeding for improved resistance to fumonisin contamination in maize. Toxin Reviews, 27, 371–389.

    Article  CAS  Google Scholar 

  • García, D., Barros, G., Chulze, S., Ramos, A. J., Sanchis, V., & Marin, S. (2012). Impact of cycling temperatures on Fusarium verticillioides and Fusarium graminearum growth and mycotoxins production in soybean. Journal of the Science of Food and Agriculture, 92, 2952–2959.

    Article  PubMed  Google Scholar 

  • Indira, S., & Muthusubramanian, V. (2004). Influence of weather parameters on spore production in major mold pathogens of sorghum in relation to mold severity in the field. Indian Journal of Plant Protection, 32, 75–79.

    Google Scholar 

  • Jurado, M., Marin, P., Magan, N., & Gonzalez-Jaen, M. T. (2008). Relationship between solute and matric potential stress, temperature, growth, and FUM1 gene expression in two Fusarium verticillioides strains from Spain. Applied and Environmental Microbiology, 74, 2032–2036.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Löffler, M., Miedaner, T., Kessel, B., & Ouzunova, M. (2010). Mycotoxin accumulation and corresponding ear rot rating in three maturity groups of European maize inoculated by two Fusarium species. Euphytica, 174, 153–164.

    Article  Google Scholar 

  • Logrieco, A., Bottalico, A., Mule, G., Moretti, A., & Perrone, G. (2003). Epidemiology of toxigenic fungi and their associated mycotoxins for some Mediterranean crops. European Journal of Plant Pathology, 109, 645–667.

    Article  CAS  Google Scholar 

  • Marin, S., Sanchís, V., & Magan, N. (1995). Water activity, temperature, and pH effects on growth of Fusarium moniliforme and Fusarium proliferatum isolates from maize. Canadian Journal of Microbiology, 41, 1063–1070.

    Article  CAS  PubMed  Google Scholar 

  • Marin, S., Homedes, V., Sanchis, V., Ramos, A. J., & Magan, N. (1999). Impact of Fusarium moniliforme and F. proliferatum colonisation of maize on calorific losses and fumonisin production under different environmental conditions. Journal of Stored Products Research, 35, 15–26.

    Article  Google Scholar 

  • Marin, S., Magan, N., Ramos, A. J., & Sanchis, V. (2004). Fumonisin-producing strains of Fusarium: a review of their ecophysiology. Journal of Food Protection, 67, 1792–1805.

    CAS  PubMed  Google Scholar 

  • Marin, P., Magan, N., Vazquez, C., & Gonzalez-Jaen, M. T. (2010). Differential effect of environmental conditions on the growth and regulation of the fumonisin biosynthetic gene FUM1 in the maize pathogens and fumonisin producers Fusarium verticillioides and Fusarium proliferatum. FEMS Microbiology Ecology, 73, 303–311.

    CAS  PubMed  Google Scholar 

  • Mesterhazy, A., Lemmens, M., & Reid, L. M. (2012). Breeding for resistance to ear rots caused by Fusarium spp. in maize—a review. Plant Breeding, 131, 1–19.

    Article  Google Scholar 

  • Miedaner, T., Bolduan, C., & Melchinger, A. E. (2010). Aggressiveness and mycotoxin production of eight isolates each of Fusarium graminearum and Fusarium verticillioides for ear rot on susceptible and resistant early maize inbred lines. European Journal of Plant Pathology, 127, 113–123.

    Article  CAS  Google Scholar 

  • Miller, S. S., Reid, L. M., & Harris, L. J. (2007). Colonization of maize silks by Fusarium graminearum, the causative organism of gibberella ear rot. Canadian Journal of Botany, 85, 369–376.

    Article  Google Scholar 

  • Munkvold, G. P., Mcgee, D. C., & Carlton, W. M. (1997). Importance of different pathways for maize kernel infection by Fusarium moniliforme. Phytopathology, 87, 209–217.

    Article  CAS  PubMed  Google Scholar 

  • Pildain, M. B., Vaamonde, G., & Cabral, D. (2004). Analysis of population structure of Aspergillus flavus from peanut based on vegetative compatibility, geographic origin, mycotoxin and sclerotia production. International Journal of Food Microbiology, 93, 31–40.

    Article  CAS  PubMed  Google Scholar 

  • Reid, L. M., Spaner, D., Mather, D. E., Bolton, A. T., & Hamilton, R. I. (1993). Resistance of maize hybrids and inbreds following silk inoculationwith three isolates of Fusarium graminearum. Plant Disease, 77, 1248–1251.

    Article  Google Scholar 

  • Reid, L. M., Hamilton, R. E., & Mather, D. E. (1996). Screening maize for resistance to gibberella ear rot (p. 62). Ottawa: Agriculture and Agri-Food Canada: Technical Bulletin.

    Google Scholar 

  • Reid, L. M., Nicol, R. W., Ouellet, T., Savard, M., Miller, J. D., Young, J. C., et al. (1999). Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology, 89, 1028–1037.

    Article  CAS  PubMed  Google Scholar 

  • Robertson, L. A., Kleinschmidt, C. E., White, D. G., Payne, G. A., Maragos, C. M., & Holland, J. B. (2006). Heritabilities and correlations of fusarium ear rot resistance and fumonisin contamination resistance in two maize populations. Crop Science, 46, 353–361.

    Article  CAS  Google Scholar 

  • Ryu, D., Munimbazi, C., & Bullerman, L. B. (1999). Fumonisin B-1 production by Fusarium moniliforme and Fusarium proliferatum as affected by cycling temperatures. Journal of Food Protection, 62, 1456–1460.

    CAS  PubMed  Google Scholar 

  • Samapundo, S., Devlieghere, F., De Meulenaer, B., & Debevere, J. (2005). Effect of water activity and temperature on growth and the relationship between fumonisin production and the radial growth of Fusarium verticillioides and Fusarium proliferatum on corn. Journal of Food Protection, 68, 1054–1059.

    CAS  PubMed  Google Scholar 

  • Santiago, R., Cao, A., Malvar, R. A., Reid, L. M., & Butron, A. (2013). Assessment of corn resistance to fumonisin accumulation in a broad collection of inbred lines. Field Crops Research, 149, 193–202.

    Article  Google Scholar 

  • SAS Institute Inc. (2008), Cary, NC, USA.

  • Schaafsma, A. W., Miller, J. D., Savard, M. E., & Ewing, R. J. (1993). Ear rot development and mycotoxin production in corn in relation to inoculation method, corn hybrid, and species of Fusarium. Canadian Journal of Plant Pathology, 15, 185–192.

    Article  CAS  Google Scholar 

  • Schaafsma, A. W., Tamburic-Illincic, L., & Reid, L. M. (2006). Fumonisin B-1 accumulation and severity of fusarium ear rot and gibberella ear rot in food-grade corn hybrids in Ontario after inoculation according to two methods. Canadian Journal of Plant Pathology, 28, 548–557.

    Article  CAS  Google Scholar 

  • Shephard, G. S., Sydenham, E. W., Thiel, P. G., & Gelderblom, W. C. A. (1990). Quantitative determination of fumonisin B1 and fumonisin B2 by high performance liquid chromatography with fluorescence detection. Journal of Liquid Chromatography, 13, 2077–2087.

    Article  CAS  Google Scholar 

  • Stepien, L., Koczyk, G., & Waskiewicz, A. (2011). Genetic and phenotypic variation of Fusarium proliferatum isolates from different host species. Journal of Applied Genetics, 52, 487–496.

    Article  PubMed Central  PubMed  Google Scholar 

  • Velasco, P., Revilla, P., Butron, A., Ordas, B., Ordas, A., & Malvar, R. A. (2002). Ear damage of sweet corn inbreds and their hybrids under multiple corn borer infestation. Crop Science, 42, 724–729.

    Article  Google Scholar 

  • Velasco, P., Revilla, P., Monetti, L., Butron, A., Ordas, A., & Malvar, R. A. (2007). Corn borers (Lepidoptera : Noctuidae; Crambidae) in Northwestern Spain: population dynamics and distribution. Maydica, 52, 195–203.

    Google Scholar 

  • Venturini, G., Assante, G., & Vercesi, A. (2011). Fusarium verticillioides contamination patterns in Northern Italian maize during the growing season. Phytopathologia Mediterranea, 50, 110–120.

    Google Scholar 

  • Voss, K. A., Smith, G. W., & Haschek, W. M. (2007). Fumonisins: toxicokinetics, mechanism of action and toxicity. Animal Feed Science and Technology, 137, 299–325.

    Article  CAS  Google Scholar 

  • Wiseman, B. R., & Isenhour, D. J. (1992). Relationship of planting dates and corn-earworm developmental parameters and injury to selected maize entries. Maydica, 37, 149–156.

    Google Scholar 

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Acknowledgments

This research was supported by the National Plan for Research and Development of Spain (AGL2009-12770), the Autonomous Government of Galicia (PGIDIT06TAL40301PR) and the Excma. Diputación Provincial de Pontevedra. A. Cao acknowledges funding from the JAE Program of the Spanish Council of Research. R. Santiago acknowledges postdoctoral contract “Isidro Parga Pondal” supported by the Autonomous Government of Galicia and the European Social Fund.

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Authors and Affiliations

  1. Misión Biológica de Galicia (CSIC), Apdo. 28, 36080, Pontevedra, Spain

    Ana Cao, Ana Butrón & Rogelio Santiago

  2. Escuela Técnica Superior de Ingeniería Agraria (ETSEA), Universidad de Lleida, XaRTA- UTPV- Agrotecnio, Avda Rovira Roure 191, 25198, Lleida, Spain

    Antonio J. Ramos & Sonia Marín

  3. E.U.E.T. Forestal, Universidad de Vigo, Campus Universitario Pontevedra, 36005, Pontevedra, Spain

    Carlos Souto

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  1. Ana Cao
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  2. Ana Butrón
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Correspondence to Rogelio Santiago.

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Cao, A., Butrón, A., Ramos, A.J. et al. Assessing white maize resistance to fumonisin contamination. Eur J Plant Pathol 138, 283–292 (2014). https://doi.org/10.1007/s10658-013-0328-y

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Keywords

  • Fusarium verticillioides
  • Fumonisin
  • Artificial inoculation
  • Maize silks