Advertisement

European Journal of Plant Pathology

, Volume 152, Issue 3, pp 677–689 | Cite as

Pathogenicity and toxigenicity of Fusarium verticillioides isolates collected from maize roots, stems and ears in South Africa

  • A. Schoeman
  • B. C. Flett
  • B. Janse van Rensburg
  • E. Ncube
  • A. Viljoen
Article
First Online:
  • 133 Downloads

Abstract

Fusarium verticillioides is most frequently associated with maize in South Africa. It colonises maize roots, stems and ears endophytically and causes diseases such as Fusarium ear rot (FER) and stalk rot. Fusarium verticillioides can produce fumonisins, which are toxic secondary metabolites harmful to humans and animals. It is, however, unknown whether endophytic and pathogenic isolates from distinct maize tissues differ in their ability to cause disease and produce fumonisins. In this study, Fusarium spp. were collected from maize roots, stems and kernels for phylogenetic analysis and the F. verticillioides isolates were subjected to pathogenic and toxigenic comparison. The translation elongation 1-α (TEF1) gene of the isolates was sequenced, and a phylogenetic tree constructed with maximum likelihood (ML) and Bayesian interference (BI) inferred. Fumonisin production of F. verticillioides isolates was determined in vitro and in planta by using high performance liquid chromatography, and virulence of the isolates was determined by silk channel inoculation of maize ears under field conditions. F. verticillioides was the species with the highest number of isolates followed by F. temperatum and then F. subglutinans. Phylogenetic analyses clustered the different Fusarium spp. according to species. Fumonisin production by F. verticillioides isolates varied from 0 to 21.3 mg/kg in vitro, and 0–16.2 mg/kg in planta. All the F. verticillioides isolates produced FER symptoms, including isolates from roots and stems. Fusarium verticillioides isolates in South Africa thus presented a species highly diverse in toxigenicity, but not in virulence. This finding has implications for managing mycotoxins in maize, as visible symptoms might be misleading to the actual toxin level present, for example low level of disease severity might represent high fumonisin levels and vice versa. The high numbers of F. temperatum, also a mycotoxin producer highlights the concern that kernels could be contaminated with more than one mycotoxin. Integrated disease management of not only F. verticillioides but all Fusarium spp. should thus focus strongly on reducing fungal contamination of maize and the detoxification of grain with focus on using regionally adapted maize varieties.

Keywords

Fumonisins Fusarium verticillioides Pathogenicity Phylogeny Toxigenicity 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

The authors wish to thank the Agricultural Research Council – Grain Crops Institute (South Africa) for the use of infrastructure and funding. The National Research Foundation and Maize Trust is also acknowledged for funding.

References

  1. Afolabi, C. G., Ojiambo, P. S., Ekpo, E. J. A., Menkir, A., Bandyopadhyay, R., et al. (2007). Evaluation of maize inbred lines for resistance to Fusarium ear rot and fumonisin accumulation in grain in tropical Africa. Plant Disease, 91, 279–286.CrossRefGoogle Scholar
  2. Alberts, J. F., Gelderblom, W. C. A., Thiel, P. G., Marasas, W. F. O., Van Schalkwyk, D. J., Behrend, Y., et al. (1990). Effects of temperature and incubation period on the production of fumonisin B1 by Fusarium moniliforme. Applied and Environmental Microbiology, 56, 1729–1733.PubMedPubMedCentralGoogle Scholar
  3. Bacon, C. W., & Hinton, D. M. (1996). Symptomless endophytic colonization of maize by Fusarium moniliforme. Canadian Journal of Botany, 74, 1195–1202.CrossRefGoogle Scholar
  4. Bacon, C. W., Yates, I. E., Hinton, D. M., Meredith, F., et al. (2001). Biological control of Fusarium moniliforme in maize. Environmental Health Perspectives, 109, 325–332.PubMedPubMedCentralGoogle Scholar
  5. Boutigny, A.-L., Beukes, I., Small, I., Zühlke, S., Spiteller, M., Janse van Rensburg, B., Flett, B. C., Viljoen, A., et al. (2012). Quantitative detection of Fusarium pathogens and their mycotoxins in South African maize. Plant Pathology, 61, 522–531.CrossRefGoogle Scholar
  6. Britz, H., Steenkamp, E. T., Countinho, T. A., Wingfield, B. D., Marasas, W. F. O., Wingfield, M. J., et al. (2002). Two new species of Fusarium section Liseola associated with mango malformation. Mycologia, 94, 722–730.CrossRefPubMedGoogle Scholar
  7. Burger, H.-M., Lombard, M. J., Shephard, G. S., Rheeder, J. R., van der Westhuizen, L., Gelderblom, W. C. A., et al. (2010). Dietary fumonisin exposure in a rural population of South Africa. Food and Chemical Toxicology, 48, 2103–2108.CrossRefPubMedGoogle Scholar
  8. Burgess, L. W., & Trimboli, D. (1986). Characterization and distribution of Fusarium nygamai sp. nov. Mycologia, 78, 223–229.CrossRefGoogle Scholar
  9. Bush, B. J., Carson, M. L., Cubeta, M. A., Hagler, W. M., Payne, G. A., et al. (2004). Infection and fumonisin production by Fusarium verticillioides in developing maize kernels. Phytopathology, 94, 88–93.CrossRefPubMedGoogle Scholar
  10. Butler, E. J., & Khan, A. H. (1913). Some new sugarcane diseases. Memoirs of the Department of Agriculture in India: Botanical Series, 6, 185–190.Google Scholar
  11. Chu, F. S., & Li, G. Y. (1994). Simultaneous occurrence of fumonisin B1 and other mycotoxins in mouldy corn collected from the People’s Republic of China in regions with high oesophageal cancer. Applied and Environmental Microbiology, 60, 847–852.PubMedPubMedCentralGoogle Scholar
  12. Clements, M. J., Maragos, C. A., Pataky, J. K., White, D. G., et al. (2004). Sources of resistance to fumonisin accumulation in grain and Fusarium ear and kernel rot of corn. Phytopathology, 94, 251–260.CrossRefPubMedGoogle Scholar
  13. Cumagun, C. J. R., Ramos, J. S., Dimaano, A. O., Munaut, F., Van Hove, F., et al. (2009). Genetic characteristics of Fusarium verticillioides from corn in the Philippines. Journal of General Plant Pathology, 75, 405–412.CrossRefGoogle Scholar
  14. De Oliveira Rocha, L., Reis, G. M., Nascimento da Silva, V., Braghini, R., Teixeira, M. M. G., Corrêa, B., et al. (2011). Molecular characterization and fumonisin production by Fusarium verticillioides isolated from corn grains of different geographic origins in Brazil. International Journal of Food Microbiology, 145, 9–21.CrossRefPubMedGoogle Scholar
  15. Desjardins, A. E., & Plattner, R. D. (2000). Fumonisin B1-nonproducing strains of Fusarium verticillioides cause maize (Zea mays) ear infection and ear rot. Journal of Agricultural Food Chemistry, 48, 5773–5780.CrossRefPubMedGoogle Scholar
  16. Desjardins, A. E., Plattner, R. D., Nelsen, T. C., Leslie, J. F., et al. (1995). Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Applied and Environmental Microbiology, 61, 79–86.PubMedPubMedCentralGoogle Scholar
  17. Desjardins, A. E., Plattner, R. D., & Gordon, T. R. (2000). Gibberella fujikuroi mating population A and Fusarium subglutinans from teosinte species and maize from Mexico and Central America. Mycological Research, 104, 865–872.CrossRefGoogle Scholar
  18. Foley, D. C. (1962). Systemic infection of corn by Fusarium monilifome. Phytopathology, 52, 870–872.Google Scholar
  19. Geiser, D. M., Jiménez-Gasco, M. M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., Zhang, N., Kuldau, G. A., O’Donnell, K., et al. (2004). Fusarium-ID v 1.0: A DNA sequence database for identifying Fusarium. European Journal of Plant Pathology, 110, 473–479.CrossRefGoogle Scholar
  20. Gelderblom, W. C. A., Kriek, N. P. J., Marasas, W. F. O., Thiel, P. G., et al. (1991). Toxicity and carcinogenicity of the Fusarium moniliforme metabolite fumonisin B1 in rats. Carcinogenesis, 12, 1247–1251.CrossRefPubMedGoogle Scholar
  21. Goertz, A., Zuehlke, S., Spiteller, M., Steiner, U., Dehne, H. W., Waalwijk, C., de Vries, I., Oerke, E. C., et al. (2010). Fusarium species and mycotoxin profiles on commercial maize hybrids in Germany. European Journal of Plant Pathology, 28, 101–111.CrossRefGoogle Scholar
  22. Guidon, S., & Gascuel, O. (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 5, 696–704.CrossRefGoogle Scholar
  23. Harrison, L. R., Colvin, B. M., Green, J. T., Newman, L. E., Cole, J. R., et al. (1990). Pulmonary edema and hydrothorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. Journal of Veterinary Diagnostic Investigation, 2, 217–221.CrossRefPubMedGoogle Scholar
  24. Heulsenbeck, J. P., Ronquist, F., Nielsen, R., Bollack, J. P., et al. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.CrossRefGoogle Scholar
  25. Hirata, T., Kimishima, E., Aoki, T., Nirenberg, H. I., O’Donnell, K., et al. (2001). Morphological and molecular characterization of Fusarium verticillioides from rotten banana imported into Japan. Mycoscience, 42, 155–166.CrossRefGoogle Scholar
  26. Janse van Rensburg, B. (2012). Modelling the incidence of Fusarium and Aspergillus toxin producing species in maize and sorghum in South Africa. PhD. University of the Free State, South Africa. 150 pp.Google Scholar
  27. Jardine, D. J., & Leslie, J. F. (1999). Aggressiveness to mature maize plants of Fusarium strains differing in ability to produce fumonisin. Plant Disease, 83, 690–693.CrossRefGoogle Scholar
  28. Jiménez, M., Mateo, J. J., Hinojo, M. J., Mateo, R., et al. (2003). Sugars and amino acids as factors affecting the synthesis of fumonisins in liquid cultures by isolates of the Gibberella fujikuroi complex. International Journal of Microbiology, 89, 185–193.CrossRefGoogle Scholar
  29. Kedera, C. J., Leslie, J. F., Claflin, L. E., et al. (1994). Genetic diversity of Fusarium section Liseola (Gibberella fujikuroi) in individual maize stalks. Phytopathology, 84, 603–607.CrossRefGoogle Scholar
  30. Kellerman, T. S., Marasas, W. F. O., Thiel, P. G., Gelderblom, W. C. A., Cawood, M., Coetzer, J. A. W., et al. (1990). Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1. Onderstepoort Journal of Veterinary Research, 57, 269–275.PubMedGoogle Scholar
  31. Klaasen, J. A., & Nelson, P. E. (1996). Identification of a mating population, Gibberella nygamai sp. nov., within the Fusarium nygamai anamorph. Mycologia, 88, 965–969.CrossRefGoogle Scholar
  32. Klittich, C. J. R., Leslie, J. F., Nelson, P. E., Marasas, W. F. O., et al. (1997). Fusarium thapsinum (Gibberella thapsina): A new species in section Liseola from sorghum. Mycologia, 89, 643–652.CrossRefGoogle Scholar
  33. Leslie, J. F. (1991). Mating populations in Gibberella fujikuroi (Fusarium section Liseola). Phytopathology, 81, 1058–1060.Google Scholar
  34. Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual (pp. 388). Oxford: Blackwell Publishing Ltd.CrossRefGoogle Scholar
  35. Leslie, J. F., Pearson, C. A. S., Nelson, P. E., Toussoun, T. A., et al. (1990). Fusarium spp. from corn, sorghum and soybean fields in the central and eastern United States. Phytopathology, 80, 343–350.CrossRefGoogle Scholar
  36. Leslie, J. F., Zeller, K. A., Logrieco, A., Mulè, G., Morretti, A., Ritieni, A., et al. (2004). Species diversity and toxin production by strains in the Gibberella fujikuroi species complex isolated from native grasses in Kansas. Applied and Environmental Microbiology, 70, 2254–2262.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Leslie, J. F., Zeller, K. A., Lamprecht, S. C., Rheeder, J. P., Marasas, W. F. O., et al. (2005). Toxicity, pathogenicity, and genetic differentiation of five species of Fusarium from sorghum and millet. Phytopathology, 95, 275–283.CrossRefPubMedGoogle Scholar
  38. López-Errasquín, E., Vásquez, C., Jiménez, M., Gonzàlez-Jaén, M. T., et al. (2007). Real-time RT-PCR assay to quantify the expression of fum1 and fum19 genes from fumonisin-producing Fusarium verticillioides. Journal of Microbiological Methods, 68, 312–317.CrossRefPubMedGoogle Scholar
  39. Marasas, W. F. O. (1996). Fumonisins: history, worldwide occurrence and impact. In L. S. Jackson, J. W. Devries, & L. B. Bullerman (Eds.), Fumonisins in Food (pp. 1–17). New York: Plenum Press.Google Scholar
  40. Marasas, W. F. O., Rheeder, J. P., Lamprecht, S. C., Zeller, K. A., Leslie, J. F., et al. (2001). Fusarium andiyazi sp.nov. a new species from sorghum. Mycologia, 93, 1203–1210.CrossRefGoogle Scholar
  41. 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., Allegood, J., Martinez, C., Maddox, J., Miller, J. D., Starr, L., Sullards, M. C., Roman, A. V., Voss, K. A., Wang, E., Merril Jr., A. H., et al. (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. Journal of Nutrition, 134, 711–716.CrossRefPubMedGoogle Scholar
  42. Melcion, D., Cahagnier, B., Richard-Molard, D., et al. (1997). Study of the biosynthesis of fumonisin B1, B2 and B3 by different strains of Fusarium moniliforme. Letters in Applied Microbiology, 24, 301–305.CrossRefPubMedGoogle Scholar
  43. Miller, J. D. (2001). Factors that affect the occurrence of fumonisin. Environmental Health Perspectives, 109, 321–324.PubMedPubMedCentralGoogle Scholar
  44. Mirete, S., Vázquez, C., Mulé, G., Jurado, M., González-Jaén, M. T., et al. (2004). Differentiation of Fusarium verticillioides from banana fruits by IGS and EF-1 α sequence analysis. European Journal of Plant Pathology, 110, 515–523.CrossRefGoogle Scholar
  45. Missmer, S. A., Suarez, L., Felkner, M., Wang, E., Merrill Jr., A. H., Rothman, K. J., Hendricks, K. A., et al. (2006). Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border. Environmental Health Perspectives, 114, 237–241.CrossRefPubMedGoogle Scholar
  46. Moretti, A., Mulé, G., Ritieni, A., Làday, M., Stubnya, V., Hornok, L., Logrieco, A., et al. (2008). Cryptic subspecies and beauvericin production by Fusarium subglutinans from Europe. International Journal of Food Microbiology, 127, 312–315.CrossRefPubMedGoogle Scholar
  47. Moses, L. M., Marasas, W. F. O., Vismer, H. F., De Vos, L., Rheeder, J. P., Proctor, R. H., Wingfield, B. D., et al. (2010). Molecular characterization of Fusarium globosum strains from South African maize and Japanese wheat. Mycopathologia, 170, 237–249.CrossRefPubMedGoogle Scholar
  48. Munkvold, G. P., & Desjardins, A. E. (1997). Fumonisins in maize: can we reduce their occurrence? Plant Disease, 81, 556–565.CrossRefGoogle Scholar
  49. Ncube, E., Flett, B. C., Waalwijk, C., Viljoen, A., et al. (2011). Fusarium spp. and levels of fumonisins in maize produced by subsistence farmers in South Africa. South African Journal of Science, 107, 1–7.CrossRefGoogle Scholar
  50. Nelson, P. E., Toussoun, T. A., Marasas, W. F. O., et al. (1983). Fusarium Species: An Illustrated Manual for Identification (p. 139). University Park: Pennsylvania State University, University Press.Google Scholar
  51. Nirenberg, H. I., & O’Donnell, K. (1998). New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia, 90, 434–458.CrossRefGoogle Scholar
  52. O’Donnell, K., Kistler, H. C., Cigelnik, E., Ploetz, R. C., et al. (1998). Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from the nuclear and mitochondrial gene genealogies. Proceeding of the National Academy of Science, 95, 2044–2049.CrossRefGoogle Scholar
  53. O’Donnell, K., Nirenberg, H. I., Aoki, T., Cigelnik, E., et al. (2000). A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct species. Mycoscience, 41, 61–78.CrossRefGoogle Scholar
  54. O’Donnell, K., Sarver, B. A. J., Brandt, M., Chang, D. C., Noble-Wang, J., Park, B. J., Sutton, D. A., Benjamin, L., Lindsley, M., Padhye, A., Geiser, D. M., Ward, T. J., et al. (2007). Phylogenetic diversity and microsphere array-based genotyping of human pathogenic Fusaria, including isolates from the multistate contact lens-associated US keratitis outbreaks of 2005 and 2006. Journal of Clinical Microbiology, 45, 2235–2248.CrossRefPubMedPubMedCentralGoogle Scholar
  55. O’Donnell, K., Sutton, D. A., Rinaldi, M. G., Sarver, B. A. J., Balajee, S. A., Schroers, H.-J., Summerell, R. C., Robert, V. A. R. G., Crous, P. W., Zhang, N., Aoki, T., Jung, K., Park, J., Lee, Y.-H., Kang, S., Park, B., Geiser, D. M., et al. (2010). Internet-Accessible DNA sequence database for identifying Fusaria from human and animal infections. Journal of Clinical Microbiology, 48, 3708–3718.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Parsons, M. W., & Munkvold, G. P. (2012). Effects of planting date and environmental factors on fusarium ear rot symptoms and fumonisin B1 accumulation in maize grown in six North America locations. Plant Pathology, 61, 1130–1142.CrossRefGoogle Scholar
  57. Pascale, M., Doko, M.B., Visconti, A., et al. (1995). Determination of fumonisins in polenta by high performance liquid chromatography. In: Proceedings of the 2nd national Congress on Food Chemistry. Giardini-Naxos (pp. 1067–1071). Messina, Italy: La Grafica Editoriale.Google Scholar
  58. Posada, D. (2003). Using MODELTEST and PAUP* to Select a Model of Nucleotide Substitution. In A. D. Baxevanis, D. B. Davison, R. D. M. Page, G. A. Petsko, L. D. Stein, & G. D. Stormo (Eds.), Current Protocols in Bioinformatics (pp. 6.51–6.5.14). New York: Wiley.Google Scholar
  59. Posada, D. (2008). Jmodeltest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Proctor, R. H., Plattner, R. D., Brown, D. W., Seo, J.-A., Lee, Y.-W., et al. (2004). Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycological Research, 108, 815–822.CrossRefPubMedGoogle Scholar
  61. Rayner, A. A. (1969). A first course in Biometry for agriculture students (626 pp). Pietermaritzburg: University of Natal Press.Google Scholar
  62. Rheeder, J. P., Marasas, W. F. O., Thiel, P. G., Sydenham, E. W., Shephard, G. S., van Schalkwyk, D. J., et al. (1992). Fusarium moniliforme and fumonisins in corn in relation to human oesophageal cancer in Transkei. Phytopathology, 82, 353–357.CrossRefGoogle Scholar
  63. Rheeder, J. P., Marasas, W. F. O., Vismer, H. F., et al. (2002). Production of fumonisin analogues by Fusarium species. Applied and Environmental Microbiology, 68, 2101–2105.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sambrooks, J., Fritsch, E. F., Maniatis, T., et al. (1989). Molecular cloning: a laboratory manual, 2 nd ed. Cold Spring Harbour: Cold Spring Harbor Laboratory Press.Google Scholar
  65. SAS Institute, Inc. (1999). SAS/STAT User's Guide, Version 9, 1st printing, Volume 2. SAS Institute Inc, SAS Campus Drive, Cary, North Carolina 27513.Google Scholar
  66. Scauflaire, J., Gourgue, M., Munaut, F., et al. (2011a). Fusarium temperatum sp. nov. from maize, an emergent species closely related to Fusarium subglutinans. Mycologia, 103, 586–597.CrossRefPubMedGoogle Scholar
  67. Scauflaire, J., Mahieu, O., Louvieaux, J., Foucart, G., Renard, F., Munaut, F., et al. (2011b). Biodiversity of Fusarium species in ears and stalks of maize plants in Belgium. European Journal of Plant Pathology, 131, 59–66.CrossRefGoogle Scholar
  68. Seo, J.-A., Proctor, R. H., Plattner, R. D., et al. (2001). Characterization of four clustered and co-regulated genes associated with fumonisin biosynthesis in Fusarium verticillioides. Fungal Genetics and Biology, 34, 155–165.CrossRefPubMedGoogle Scholar
  69. Shephard, G. S., Thiel, P. G., Stockenström, S., Sydenham, E. W., et al. (1996). Worldwide survey of fumonisin contamination of corn and corn-based products. Journal of Association of Official Analytical Chemists International, 79, 671–687.Google Scholar
  70. Small, I. M., Flett, B. C., Marasas, W. F. O., McLeod, A., Viljoen, A., et al. (2012). Resistance in maize inbred lines to Fusarium verticillioides and fumonisin accumulation in South Africa. Plant Disease, 96, 881–888.CrossRefGoogle Scholar
  71. Sydenham, E. W., Shephard, G. S., Thiel, P. G., Stockenström, S., Van Schalkwyk, D. J., et al. (1996). Liquid chromatographic determination of fumonisins B1, B2 and B3 in corn: AOAC-IUPAC collaborative study. Journal of Association of Official Analytical Chemists International, 79, 688–696.Google Scholar
  72. Van der Westhuizen, L., Shephard, G. S., Scussel, V. M., Costa, L. L., Vismer, H. F., Rheeder, J. P., Marasas, W. F., et al. (2003). Fumonisin contamination and Fusarium incidence in corn from Santa Catarina, Brazil. Journal of Agricultural and Food Chemistry, 51, 5574–5578.CrossRefPubMedGoogle Scholar
  73. Van Hove, F., Waalwijk, C., Logrieco, A., Munaut, F., Moretti, A., et al. (2011). Gibberella musae (Fusarium musae) sp. Nov., a recently discovered species from banana is sister to F. verticillioides. Mycologia, 103, 570–585.CrossRefPubMedGoogle Scholar
  74. Van Wyk, P. S., Scholtz, D. J., Los, O., et al. (1986). A selective medium for the isolation of Fusarium spp. from soil debris. Phytophylactica, 18, 67–69.Google Scholar
  75. Vismer, H. F., Snijman, P. W., Marasas, W. F. O., van Schalkwyk, D. J., et al. (2004). Production of fumonisins by Fusarium verticillioides strains on solid and defined liquid medium – Effects of L-methionine and inoculum. Mycopathologia, 158, 99–106.CrossRefPubMedGoogle Scholar
  76. White, D.G. 1999. Compendium of corn diseases. 3rd Ed. APS Press, The American Phytopahtology Society, Minnesota, 128 pp.Google Scholar
  77. World Health Organization. (2002). Evaluation of certain mycotoxins in food. Fifty-sixth report of the Joint FAO/WHO Expert Committee on Food Additives (JECFA). WHO Technical Report, 906, 16–27.Google Scholar
  78. Yates, I. E., Bacon, C. W., Hinton, D. M., et al. (1997). Effects of endophytic infection by Fusarium moniliforme on corn growth and cellular morphology. Plant Disease, 81, 723–728.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • A. Schoeman
    • 1
    • 2
  • B. C. Flett
    • 1
  • B. Janse van Rensburg
    • 1
  • E. Ncube
    • 1
  • A. Viljoen
    • 2
  1. 1.Agricultural Research Council-Grain Crop InstitutePotchefstroomSouth Africa
  2. 2.Department of Plant PathologyStellenbosch UniversityMatielandSouth Africa

Personalised recommendations

Cite article

Buy options