Cocultivation of phytopathogenic Fusarium and Alternaria strains affects fungal growth and mycotoxin production

Journal of Applied Microbiology

Volumn 113, Issue 4, 2012, Pages 874-887

  Muller M E H ^a   Steier, I ^b   Koppen R ^c   Siegel, D ^c   Proske, M ^c   Korn, U ^a   Koch, M ^c  

^a LEIBNIZ CENTRE FOR AGRICULTURAL LANDSCAPE RESEARCH ZALF   (Germany)

^b TECHNICAL UNIVERSITY OF APPLIED SCIENCES WILDAU   (Germany)

^c BAM FEDERAL INSTITUTE FOR MATERIALS RESEARCH AND TESTING   (Germany)

Author keywords

Alternaria; Cocultivation; Ergosterol; Fusarium; Interfungal competition; Multimycotoxin analysis

Indexed keywords

ALCOHOLS; BIOMASS; ECOLOGY; GRAIN (AGRICULTURAL PRODUCT); METABOLITES; TOXICITY;

ALTERNARIA; CO-CULTIVATION; ERGOSTEROL; FUNGAL BIOMASS; FUNGAL GROWTH; FUSARIUM; INTERFUNGAL COMPETITION; LABORATORY STUDIES; MULTIMYCOTOXIN ANALYSE; TOXIGENIC;

MYCOTOXINS;

ALTENEUN; ALTERNARIOL; ALTERNARIOL METHYL ETHER; ERGOSTEROL; MYCOTOXIN; NIVALENOL; UNCLASSIFIED DRUG; VOMITOXIN; ZEARALENONE;

BIOGENIC MATERIAL; BIOMASS; CULTIVATION; ERGOSTEROL; FUNGUS; GROWTH RATE; INTERSPECIFIC COMPETITION; LABORATORY METHOD; PATHOGEN; TOXIN; WHEAT;

ALTERNARIA; ARTICLE; BACTERIUM ISOLATE; CLINICAL EVALUATION; COCULTURE; CONTROLLED STUDY; FUNGAL BIOMASS; FUNGAL STRAIN; FUNGUS GROWTH; FUSARIUM; FUSARIUM CULMORUM; FUSARIUM GRAMINEARUM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; LABORATORY TEST; MASS SPECTROMETRY; MEDICAL DECISION MAKING; NONHUMAN;

ALTERNARIA; ALTERNARIA TENUISSIMA; FUNGI; FUSARIUM; FUSARIUM CULMORUM; GIBBERELLA ZEAE; TRITICUM AESTIVUM;

EID: 84866342614     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2012.05388.x     Document Type: Article

References (67)

1. Andersen, B., Thrane, U., Svendsen, A. and Rasmussen, I.A. (1996) Associated field mycobiota on malt barley. Can J Bot 74, 854-858.
2. Azcarate, M.P., Patriarca, A., Terminiello, L. and Fernandez Pinto, V. (2008) Alternaria toxins in wheat during the 2004 to 2005 Argentinean harvest. J Food Prot 71, 1262-1265.
3. Bateman, G.L. (2005) The contribution of ground-level inoculum of Fusarium culmorum to ear blight of winter wheat. Plant Pathol 54, 299-307.
4. Bottalico, A. (1998) Fusarium diseases of cereals: species complex and related mycotoxin profiles in Europe. J Plant Pathol 80, 85-102.
5. Bottalico, A. and Logrieco, A. (1998) Toxigenic Alternaria species of economic importance. In: Mycotoxins in Agriculture and Food Safety ed. Sinha, K.K. and Bhatnagar, D. pp. 65-108. New York: Marcel Dekker, Inc.
6. Bottalico, A. and Perrone, G. (2002) Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur J Plant Pathol 108, 611-624.
7. Burgess, L.W., Nelson, P.E., Toussoun, T.A. and Forbes, G.A. (1988) Distribution of Fusarium species in sections Roseum, Arthrosporiella, Gibbosum, and Discolor recovered from grassland, pasture and pine nursery soils of eastern Australia. Mycologia 80, 815-824.
8. Champeil, A., Doré, T. and Fourbet, J.F. (2004) Fusarium head blight: epidemiological origin of the effects of cultural practices on head blight attacks and the production of mycotoxins by Fusarium in wheat grains. Plant Sci 166, 1389-1415.
9. Chelkowski, J. and Visconti, A. (eds) (1992) Alternaria - Biology, Plant Diseases and Metabolites. Topics in Secondary Metabolism vol 3, Amsterdam-London-New York-Tokyo: Elsevier.
10. Commission Regulation (EC)No. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs - consolidated version 01.04.2012 (online). http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2006R1881: 20120401:EN:PDF.
11. Cooney, J.M., Lauren, D.R. and di Menna, M.E. (2001) Impact of competitive fungi on trichothecene production by Fusarium graminearum. J Agric Food Chem 49, 522-526.
12. Dawood, M. (1982) Seed-borne fungi, especially pathogens of spring wheat. Acta Mycol 18, 83-112.
13. Dawson, W.A.J.M., Jestoi, M., Rizzo, A., Nicholson, P. and Bateman, G.L. (2004) Field evaluation of fungal competitors of Fusarium culmorum and F. graminearum, causal agents of ear blight of winter wheat, for the control of mycotoxin production in grain. Biocontrol Sci Technol 14, 783-799.
14. Desmond, O.J., Manners, J.M., Stephens, A.E., Maclean, D.J., Schenk, P.M., Gardiner, D.M., Munn, A.L. and Kazan, K. (2008) The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defense responses in wheat. Mol Plant Pathol 9, 435-445.
15. Diamond, H. and Cooke, B.M. (2003) Preliminary studies on biological control of the Fusarium ear blight complex of wheat. Crop Prot 22, 99-107.
16. Dill-Macky, R. and Jones, R.K. (2000) The effect of previous crop residues and tillage on Fusarium head blight of wheat. Plant Dis 4, 71-75.
17. D'Mello, J.P.F., MacDonald, A.M.C. and Cochrane, M.P. (1993) A preliminary study of the potential for mycotoxin production in barley grain. Aspects Appl Biol 36, 375-382.
18. EC 2002/657Commission Decision of 12 August 2002 implementing Council Directive 96/23/EC concerning the performance of analytical methods and the interpretation of results, Official J. L221, 8-36.
19. EC 2006/401Commission decision of 23 February 2006 laying down the methods of sampling and analysis for the official control of the levels of mycotoxins in foodstuffs. Official J. L70/12, 20-23.
20. EFSA (European Food Safety Authority) (2004) Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to deoxynivalenol (DON) as undesirable substance in animal feed (Question No. EFSA-Q-2003-036) adopted on 2 June 2004. EFSA J 73, 1-42.
21. Fitt, B.D.L., Huang, J.Y., Van den Bosch, F. and West, J.S. (2006) Coexistence of related pathogen species on arable crops in space and time. Annu Rev Phytopathol 44, 163-182.
22. González, H.H.L., Martínez, E.J., Pacin, A. and Resnik, S.L. (1999) Relationship between Fusarium graminearum and Alternaria alternata contamination and deoxynivalenol occurrence on Argentinian durum wheat. Mycopathologia 144, 97-102.
23. Harman, G.E. (2000) Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis 84, 377-393.
24. He, J., Boland, G.J. and Zhou, T. (2009) Concurrent selection for microbial suppression of Fusarium graminearum, Fusarium head blight and deoxynivalenol in wheat. J Appl Microbiol 106, 1805-1817.
25. Holz, K. (2010) Pflanzliche Reaktionen auf eine Infektion mit Pilzen der Gattung Alternaria. Diploma thesis. University of Applied Sciences Zittau/Görlitz, Registrier-Nr. NO 06-08.
26. Hooker, D.C., Schaafsma, A.W. and Tamburic-Ilincic, L. (2002) Using weather variables pre- and postheading to predict deoxynivalenol content in winter wheat. Plant Dis 86, 611-619.
27. Jones, D.R., Jenkinson, P., Clement, J.A., Turner, J.E., Jennings, P. and Gladders, P. (1997) Epidemiology and control of Fusarium ear blight. HGCA Project Report No 143, pp 66.
28. King, A.D. Jr and Schade, J.E. (1984) Alternaria toxins and their importance in food. J Food Prot 47, 886-901.
29. Korn, U., Müller, T., Ulrich, A. and Müller, M.E.H. (2011) Impact of aggressiveness of Fusarium graminearum and F. culmorum isolates on yield parameters and mycotoxin production in wheat. Mycotox Res 27, 195-206.
30. Kosiak, B., Torp, M., Skjerve, E. and Andersen, B. (2004) Alternaria and Fusarium in Norwegian grains of reduced quality - a matched pair sample study. Int J Food Microbiol 93, 51-62.
31. Laitila, A., Alakomi, H.-L., Raaska, L., Mattila-Sandholm, T. and Haikara, A. (2002) Antifungal activities of two Lactobacillus plantarum strains against Fusarium moulds in vitro and in malting of barley. J Appl Microbiol 93, 566-576.
32. Li, F. and Yoshizawa, T. (2000) Alternaria mycotoxins in weathered wheat in China. J Agr Food Chem 48, 2920-2924.
33. Liggitt, J., Jenkinson, P. and Parry, D.W. (1997) The role of saprophytic microflora in the development of Fusarium ear blight of winter wheat caused by Fusarium culmorum. Crop Prot 16, 679-685.
34. Logrieco, A., Moretti, A. and Solfrizzo, M. (2009) Alternaria toxins and plant diseases: an overview of origin, occurrence and risks. World Mycotox J 2, 129-140.
35. Luongo, L., Galli, M., Corazza, L., Meekes, E., De Haas, L., van der Plas, C.L. and Köhl, J. (2005) Potential of fungal antagonists for biocontrol of Fusarium spp. in wheat and maize through competition in crop debris. Biocontrol Sci Technol 15, 229-242.
36. Maiorano, A., Blandino, M., Reyneri, A. and Vanara, F. (2008) Effects of maize residues on the Fusarium spp. infection and deoxynivalenol (DON) contamination of wheat grain. Crop Prot 27, 182-188.
37. Miedaner, T., Cumagun, C.J.R. and Chakraborty, S. (2008) Population genetics of three important head blight pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum. J Phytopathol 156, 129-139.
38. Miller, J.D. and Trenholm, H.L. (eds) (1994) Mycotoxins in Grain. Compounds Other than Aflatoxin. St. Paul Minnesota, USA:Eagan Press.
39. Müller, M., von der Waydbrink, G., Peters, M., Umann, K. and Seyfarth, W. (2002) Belastung von Winterweizen mit Alternaria-Mykotoxinen im Land Brandenburg. Mycotox Res 18A, 217-220.
40. Müller, M.E.H., Brenning, A., Verch, G., Koszinski, S. and Sommer, M. (2010) Multifactorial spatial analysis of mycotoxin contamination of winter wheat at the field and landscape scale. Agric Ecosyst Environ 139, 245-254.
41. Naef, A., Senatore, M. and Défago, G. (2006) A microsatellite based method for quantification of fungi in decomposing plant material elucidates the role of Fusarium graminearum DON production in the saprophytic competition with Trichoderma atroviride in maize tissue microcosms. FEMS Microbiol Ecol 55, 211-220.
42. Nirenberg, H.I. (1976) Untersuchungen über die morphologische und biologische Differenzierung in der Fusarium Sektion Liseola. Mitt Biol Bundesanst Land- u Forstwirtsch 169, 1-117.
43. Ostry, V. (2008) Alternaria mycotoxins: an overview of chemical characterization, producers, toxicity, analysis and occurrence in foodstuffs. World Mycotox J 1, 175-188.
44. Parry, D.W., Jenkinson, P. and McLeod, L. (1995) Fusarium ear blight (scab) in small grain cereals - a review. Plant Pathol 44, 207-238.
45. Patriarca, A., Azcarate, M.P., Terminiello, L. and Fernandez Pinto, V. (2007) Mycotoxin production by Alternaria strains isolated from Argentinean wheat. Int J Food Microbiol 119, 219-222.
46. Prelusky, D.B., Rotter, B.A. and Rotter, R.G. (1994) Toxicology of mycotoxins. In Mycotoxins in Grain: Compounds other than Aflatoxins. ed. Miller, D. and Trenholm, D.L., pp 359-403. Saint Paul: APS Press.
47. Riungu, G.M., Muthomi, J.W. and Narla, R.D. (2007) Effect of antagonistic microorganisms on severity of Fusarium head blight of wheat and grain yield. Afr Crop Sci Conference Proceed 8, 827-832.
48. Rotter, B., Prelusky, D.B. and Pestka, J.J. (1996) Toxicology of deoxynivalenol (vomitoxin). J Toxicol Environ Health 48, 1-34.
49. Sanzani, S.M., Reverberi, M., Punelli, M., Ippolito, A. and Fanelli, C. (2012) Study on the role of patulin on pathogenicity and virulence of Penicillium expansum. Int J Food Microbiol 153, 323-331.
50. Saß, V., Milles, J., Krämer, J. and Prange, A. (2007) Competitive interactions of Fusarium graminearum and Alternaria alternata in vitro in relation to deoxynivalenol and zearalenone production. J Food Agric Environ 5, 257-261.
51. Schaafsma, A.W. and Hooker, D.C. (2007) Climatic models to predict occurrence of Fusarium toxins in wheat and maize. Int J Food Microbiol 119, 116-125.
52. Scherm, B., Orrù, M., Balmas, V., Spanu, F., Azara, E., Delogu, G., Hammond, T.M., Keller, N.P. et al. (2011) Altered trichothecene biosynthesis in TRI6-silenced transformants of Fusarium culmorum influences the severity of crown and foot rot on durum wheat seedlings. Mol Plant Pathol 12, 759-771.
53. Siebert, S. (2011) Effekt von Trichoderma harzianum auf das Wachstum und die Mykotoxinbildung von Fusarien. Thesis Bachelor of Science, Freie Universität Berlin, pp 38.
54. Siegel, D., Rasenko, T., Koch, M. and Nehls, I. (2009) Determination of the Alternaria mycotoxin tenuazonic acid in cereals by high-performance liquid chromatography/electrospray ionization-multistage mass spectrometry after derivatization with 2, 4-dinitrophenylhydrazine. J Chromatogr A 1216, 4582-4588.
55. Simmons, E.G. (1992) Alternaria taxonomy: current status, viewpoints, challenge. In Alternaria Biology, Plant Diseases and Metabolites. ed. Chelkowski, J. and Visconti, A. pp 1-36, Amsterdam: Elsevier.
56. Simpson, D.R., Thomsett, M.A. and Nicholson, P. (2004) Competitive interactions between Microdochium nivale var. majus, M. nivale var. nivale and Fusarium culmorum in planta and in vitro. Environ Microbiol 6, 79-87.
57. Singh Lakhesar, D.P., Backhouse, D. and Kristiansen, P. (2010) Nutritional constraints on displacement of Fusarium pseudograminearum from cereal straw by antagonists. Biol Control 55, 241-247.
58. Strandberg, J.O. (1992) Alternaria species that attack vegetable crops: Biology and options for disease management. In Alternaria - Biology, Plant Diseases and Metabolites. ed Chelkowski, J. and Visconti, A. pp. 175-205. Amsterdam-London-New York-Tokyo: Elsevier.
59. Utermark, J. and Karlovsky, P. (2007) Role of zearalenone lactonase in protection of Gliocladium roseum from fungitoxic effects of the mycotoxin zearalenone. Appl Environ Microbiol 73, 637-642.
60. Visconti, A. and Sibilia, A. (1994) Alternaria toxins. In Mycotoxins in Grain: Compounds other than Aflatoxins ed Miller, D. and Trenholm, H.L. pp. 315-336, Saint Paul: APS Press.
61. Visconti, A., Minervini, F., Solfrizzo, M., Bottalico, C. and Lucivero, G. (1992) Toxicity of some Fusarium section Sporotrichiella strains in relation to mycotoxin production. Appl Environ Microbiol 58, 769-772.
62. Webley, D.J., Jackson, K.L., Mullins, J.D., Hocking, A.D. and Pitt, J.I. (1997) Alternaria toxins in weather-damaged wheat and sorghum in the 1995-1996 Australian harvest. Aust J Agric Res 48, 1249-1255.
63. Windels, C.E. (2000) Economic and social impacts of Fusarium head blight: changing farms and rural communities in the northern Great Plains. Phytopathology 90, 17-21.
64. Wu, F. (2004) Mycotoxin risk assessment for the purpose of setting international regulatory standards. Environ Sci Technol 38, 4049-4055.
65. Xu, X.M. and Nicholson, P. (2009) Community ecology of fungal pathogens causing wheat head blight. Annu Rev Phytopathol 47, 83-103.
66. Xu, X.M., Monger, W., Ritieni, A. and Nicholson, P. (2007) Effect of temperature and duration of wetness during initial infection periods on disease development, fungal biomass and mycotoxin concentrations on wheat inoculated with single, or combination of, Fusarium species. Plant Pathol 56, 943-956.
67. Zhang, H., Wolf-Hall, C. and Hall, C. (2008) Modified microwave-assistent extraction of ergosterol for measuring fungal biomass in grain cultures. J Agr Food Chem 56, 11077-11080.