European Journal of Plant Pathology

, Volume 118, Issue 2, pp 165–172 | Cite as

Pathogenicity and mycotoxin production by Fusarium proliferatum isolated from onion and garlic in Serbia

  • S.  Stankovic
  • J. Levic
  • T. Petrovic
  • A. Logrieco
  • A. Moretti
Full Research Paper


Fusarium proliferatum can occur on a wide range of economically important vegetable plants but its role in disease is not always well established. In 2000 and 2001, from forty-one field samples of wilting onion and garlic plants in Serbia, F. proliferatum as the predominant fungal species was isolated from root and bulbs. Seventy isolates were firstly characterized for their sexual fertility and were shown to be mostly members of Gibberella intermedia (sixty-seven of seventy isolates, the remaining three isolates were unfertile), the sexual stage of F. proliferatum (syn. mating population D of G. fujikuroi complex). A selected set of eleven F. proliferatum isolates from both hosts were also tested for their pathogenicity and toxigenicity. Although onion and garlic plants were susceptible to all isolates, onion plants showed a significantly higher disease severity index. Six of the eleven isolates of F. proliferatum produced fumonisin B1 from 25 to 3000 μg g−1, and beauvericin from 400 to 550 μg g−1; ten isolates produced fusaric acid from 80 to 950 μg g−1 and moniliformin from 50 to 520 μg g−1. Finally, all isolates produced fusaproliferin up to 400 μg g−1. These results confirm F. proliferatum as an important pathogen of garlic and onion in Europe and that there is a potential mycotoxin accumulation risk in contaminated plants of both garlic and onion.


Gibberella intermedia Mating type Phytotoxicity Fumonisin B1 Moniliformin 



The authors would like to thank J.F. Leslie, Kansas State, University, Manhattan, KS, for providing mating population tester strains and Vincenzo Ricci for valuable technical assistance.


  1. Abdalla, M. Y., Al-Rokibah, A., Moretti, A., & Mulè, G. (2000). Pathogenicity of toxigenic Fusarium proliferatum from date palm in Saudi Arabia. Plant Disease, 84, 321–324.Google Scholar
  2. Armengol, J., Moretti, A., Perrone, G., Vicent, A., Bengoechea, J. A., & Garcia-Jemenez, J. (2005). Identification, incidence and characterization of Fusarium proliferatum on ornamental palms in Spain. European Journal of Plant Pathology, 112, 123–131.CrossRefGoogle Scholar
  3. Bacon, C. W., Porter, J. K., Norred, W. P., & Leslie, J. F. (1996). Production of fusaric acid by Fusarium. Applied and Environmental Microbiology, 62, 4039–4043.PubMedGoogle Scholar
  4. Bottalico, A., Visconti, A., & Solfrizzo, M. (1982). Production of Moniliformin by Fusarium species in Italy. Phytopathologia Mediterranea, 21, 105–106.Google Scholar
  5. Chulze, S. N., Ramirez, M. L., Pascale, M., & Visconti, A. (1998). Fumonisin production by, and mating populations of, Fusarium section Liseola isolates from maize in Argentina. Mycological Research, 102, 141–144.CrossRefGoogle Scholar
  6. Cole, R. J., Kirskey, J. W., Cutler, H. G., Doupnik, B. L., & Peckam, J. C. (1973). Toxin from Fusarium moniliforme: Effects on plants and animals. Science, 179, 1324–1326.CrossRefPubMedGoogle Scholar
  7. Desjardins, A. E., Plattner, R. D., & Nelson, P. E. (1997). Production of fumonisin B1 and moniliformin by Gibberella fujikuroi from rice from various geographic areas. Applied and Environmental Microbiology, 63, 1838–1842.PubMedGoogle Scholar
  8. Dugan, F. M, Hellier, B. C, & Lupien, S. L (2003). First report of Fusarium proliferatum causing rot of garlic bulbs in North America. Plant Pathology, 52, 426.CrossRefGoogle Scholar
  9. du-Toit, J. L., & Inglis, D. A. (2003). Fusarium proliferatum pathogenic on onion bulbs in Washington. Plant Disease, 87, 750.Google Scholar
  10. Elmer, W. H. (1990). Fusarium proliferatum, as casual agent in Fusarium crown and root rot of asparagus. Plant Disease, 74, 938.Google Scholar
  11. Elmer, W. H. (1995). A single mating population of Gibberella fujikuroi (Fusarium proliferatum) predominates in asparagus fields in Connecticut, Massachussets, and Michigan. Mycologia, 87, 68–71.CrossRefGoogle Scholar
  12. Gaeumann, E. (1957). Fusaric acid as a wilt toxin. Phytopathology, 47, 342–357.Google Scholar
  13. Klittich, C. J. R., & Leslie, J. F. (1988). Nitrate reduction mutants of Fusarium moniliforme (Gibberella fujikuroi). Genetics, 118, 417–423.PubMedGoogle Scholar
  14. Lacy, M. L., & Roberts, D. L. (1982). Yields of onion cultivars in midwestern organic soils infested with Fusarium oxysporum f. sp. cepae and Pyrenochaeta terrestris. Plant Disease, 66, 1003–1006.CrossRefGoogle Scholar
  15. Lamprecht, S. C., Marasas, W. F. O., Alberts, J. F., Cawood, M. E., Gelderblom, W. C. A., Shephard, G. S., Thiel, P. G., & Calitz, F. J. (1994). Phytotoxicity of fumonisins and TA toxin to corn and tomato. Phytopathology, 84, 383–391.CrossRefGoogle Scholar
  16. Ledoux, D. R., Bermudez, A. J., & Rottinghaus, G. E. (1995). Effects of feeding Fusarium fujikuroi culture material, containing known levels of moniliformin, in young broiler chicks. Poultry Science, 74, 297–305.PubMedGoogle Scholar
  17. Lerda, D., Bistoni, M. B., Peralta, N., Ychari, S., Vazquez, M., & Bosio, G. (2005). Fumonisins in foods from Cordoba (Argentina), presence and genotoxicity. Food and Chemical Toxicity, 43, 691–698.CrossRefGoogle Scholar
  18. Leslie, J. F. (1995). Gibberella fujikuroi: available populations and variable traits. Canadian Journal of Botany, 73(Suppl. 1), S282–S291.Google Scholar
  19. Leslie, J. F., & Klein, K. K. (1996). Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics, 144, 557–567.PubMedGoogle Scholar
  20. Leslie, J. F., Marasas, W. F. O., Shephard, G. S., Sydenham, E. W., Stockenstrom, S., & Thiel, P. G. (1996). Duckling toxicity and the production of fumonisin and moniliformin by isolates in the A and F mating populations of Gibberella fujikuroi (Fusarium moniliforme). Applied Environmental Microbiology, 62, 1182–1187.Google Scholar
  21. Leslie, J. F., Pearson, C. A. S., Nelson, P. E., & Toussoun, T. A. (1990). Fusarium spp. from corn, sorghum, and soybean fields in the central and eastern United States. Phytopathology, 80, 343–350.Google Scholar
  22. Logrieco, A., Moretti, A., Fornelli, F., Fogliano, V., Ritieni, A., Caiaffa, M. F., Randazzo, G., Bottalico, A., & Macchia, L. (1996). Fusaproliferin production by Fusarium subglutinans and its toxicity to Artemia salina, SF-9 insect cells, and human B lymphocytes. Applied and Environmental Microbiology, 62, 3378–3384.PubMedGoogle Scholar
  23. Logrieco, A., Moretti, A., Ritieni, A., Bottalico, A., & Corda, P. (1995). Occurrence and toxigenicity of Fusarium proliferatum from preharvest maize ear rot, and associated mycotoxins, in Italy. Plant Disease, 79, 727–731.CrossRefGoogle Scholar
  24. Logrieco, A., Moretti, A., Ritieni, A., Caiaffa, M. F., & Macchia, L. (2002). Beauvericin: Chemistry, biology, significance. In R. K. Upadhyay (Ed.), Advances in microbial toxin research and its biotechnological exploitation (pp. 23–30). New York: Kluwer Academic.Google Scholar
  25. Logrieco, A., Moretti, A., Ritieni, A., Chelkowski, J., Altomare, C., & Randazzo, G. (1993). Natural occurrence of beauvericin in preharvest Fusarium subglutinans infected corn ears in Poland. Journal of Agricultural and Food Chemistry, 41, 2149–2152.CrossRefGoogle Scholar
  26. Mannerucci, C. F., Cristani, C., Marziano, F., & Gambogi, P. (1987). Specie di Fusarium in seme di Cipolla di produzione nazionale. Phytopathologia Mediterranea, 26, 156–164.Google Scholar
  27. Marasas, W. F. O., Nelson, P. E., & Toussoun, T. A. (1984). Toxigenic Fusarium species: Identity and mycotoxicology. University Park: Pennsylvania State University Press.Google Scholar
  28. Moretti, A., Logrieco, A., Bottalico, A., Ritieni, A., Fogliano, V., & Randazzo, G. (1996). Diversity in beauvericin and fusaproliferin production by different populations of Gibberella fujikuroi (Fusarium section Liseola). Sydowia, 48, 45–56.Google Scholar
  29. Moretti, A., Mulè, G., Perrone, G., & Logrieco, A. (1998). Genetic and toxigenic characterization of Fusarium moniliforme and Fusarium proliferatum from various plants. In Sixth International Mycological Congress (pp. 166). Jerusalem, Israel.Google Scholar
  30. Munkvold, G., Stahr, H. M., Logrieco, A., Moretti, A., & Ritieni, A. (1998). Occurrence of fusaproliferin and beauvericin in Fusarium-contaminated livestock feed in Iowa. Applied and Environmental Microbiology, 64, 3923–3926.PubMedGoogle Scholar
  31. Nelson, P. E., Toussoun, T. A., & Marasas, W. F. O. (1983). Fusarium species. An illustrated manual for identification (pp. 193). University Park and London: The Pennsylvania State University Press.Google Scholar
  32. Nirenberg, H. I., & O’Donnell, K. (1998). New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia, 90, 434–458.CrossRefGoogle Scholar
  33. O’Donnell, K., Cigelnik, E., & Nirenberg, H. I. (1998). Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia, 90, 465–493.CrossRefGoogle Scholar
  34. Paciolla, C., Dipierro, N., Mulè, G., Logrieco, A., & Dipierro, S, (2004). The mycotoxins beauvericin and T-2 induce cell death and alteration to the ascorbate metabolism in tomato protoplasts. Physiological and Molecular Plant Pathology, 65, 49–56.CrossRefGoogle Scholar
  35. Porter, J. K., Bacon, C. W., Wray, E. M., & Hagler, W. M. (1995). Fusaric acid in Fusarium moniliforme cultures, corn, and feeds toxic to livestock and the neurochemical effects in the brain and pineal gland of rats. Natural Toxins, 3, 91–100.PubMedCrossRefGoogle Scholar
  36. Rengwalska, M. M, & Simon, P. W. (1986). Laboratory evaluation of pink root and Fusarium basal rot resistance in garlic. Plant Disease, 70, 670–672.Google Scholar
  37. Rheeder, J. P., Marasas, W. F. O., Thiel, P. G., Sydenham, E. W., Shephard, G. S., & Vanschalkwyk, D. J. (1992). Fusarium moniliforme and fumonisins in corn in relation to human oesophageal cancer in transkei. Phytopathology, 82, 353–357.Google Scholar
  38. Ritieni, A., Fogliano, V., Randazzo, G., Scarallo, A., Logrieco, A., Moretti, A., Mannina, L., & Bottalico, A. (1995). Isolation and characterization of fusaproliferin, a new toxic metabolite from Fusarium proliferatum. Natural Toxins, 3, 17–20.PubMedCrossRefGoogle Scholar
  39. Ritieni, A., Monti, S. M., Randazzo, G., Logrieco, A., Moretti, A., Peluso, G., Ferracane, R., & Fogliano, V. (1997). Teratogenic effects of fusaproliferin on chicken embryos. Journal of Agricultural and Food Chemistry, 45, 3039–3043.CrossRefGoogle Scholar
  40. Ross, P. F., Nelson, P. E., Richard, J. L., Osweiler, G. D., Rice, L. G., Plattner, R. D., & Wilson, T. M. (1990). Production of fumonisins by Fusarium moniliforme and Fusarium proliferatum isolates associated with equine leukoencephalomalacia and pulmonary edema syndrome in swine. Applied and Environmental Microbiology, 56, 3225–3226.PubMedGoogle Scholar
  41. Schwartz, H. F., & Mohan, S. K. (1995). Compendium of onion and garlic diseases (pp. 54) APS Press.Google Scholar
  42. Seefelder, W., Gossmann, M., & Humpf, H. U. (2002). Analysis of fumonisin B1 in Fusarium proliferatum––infected asparagus spears and garlic bulbs from Germany by liquid chromatography––electrospray ionization mass spectrometry. Journal of Agricultural and Food Chemistry, 50, 2778–2781.PubMedCrossRefGoogle Scholar
  43. Simey, E. I. (1990). Garlic rot caused by Fusarium proliferatum (Matsushima) Nirenberg var. minus Nirenber in Hungary. Novenyvedehem, 26, 397–399.Google Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  • S.  Stankovic
    • 1
  • J. Levic
    • 1
  • T. Petrovic
    • 1
  • A. Logrieco
    • 2
  • A. Moretti
    • 2
  1. 1.Maize Research Institute “Zemun Polje”Belgrade-ZemunSerbia and Montenegro
  2. 2.Institute of Sciences of Food ProductionNational Council of ResearchBariItaly

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