Evidence for natural resistance towards trifloxystrobin in Fusarium graminearum
- 345 Downloads
- 22 Citations
Abstract
A collection of 55 Fusarium graminearum (Gibberella zeae) strains isolated between 1969 and 2009 in Belgium, Canada, Germany, Italy, Luxembourg, or the USA belonging to the three known chemotypes (3-acetylated deoxynivalenol, 15-acetylated deoxynivalenol and nivalenol) were screened for their sensitivity towards the fungicide trifloxystrobin using a liquid culture assay. None of the isolates was completely inhibited by trifloxystrobin concentrations up to 3 mM. For comparison, prothioconazole completely inhibited fungal growth of a standard isolate at concentrations as low as 0.007 mM. The maximum level of inhibition, which could be obtained by trifloxystrobin, ranged from 14 to 65% among the strains tested and was not significantly affected by the country of origin or by the chemotype. The absence of significant differences in resistance levels between the countries of origin and chemotypes as well as the fact that strains isolated before the market introduction of strobilurins in 1996 also showed a high level of resistance is evidence that this is largely a case of natural resistance and not primarily related to strobilurin use in agriculture.
Keywords
Chemotype Gibberella zeae Fungicide Respiration inhibitionNotes
Acknowledgements
We would like to thank Kerry O’Donnell, Virgilio Balmas and Liane Gale for providing fungal strains, Servane Contal for technical assistance, and the ‘Administration des Services Techniques de l’Agriculture de Luxembourg’ for financial support.
References
- Andrews, S., & Pitt, J. I. (1986). Selective medium for isolation of Fusarium species and dematiaceous hyphomycetes from cereals. Applied and Environmental Microbiology, 51, 1235–1238.PubMedGoogle Scholar
- Anonymous. (2006). Commission Regulation (EC) No 1881/2006 (19 December 2006). Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union, L364, 5–24.Google Scholar
- Audenaert, K., Callewaert, E., Höfte, M., De Saeger, S., & Haesaert, G. (2010). Hydrogen peroxide induced by the fungicide prothioconazole triggers deoxynivalenol (DON) production by Fusarium graminearum. BMC Microbiology, 10, 112.PubMedCrossRefGoogle Scholar
- Bartlett, D. W., Clough, J. M., Godwin, J. R., Hall, A. A., Hamer, M., & Parr-Dobrzanski, B. (2002). The strobilurin fungicides. Pest Management Science, 58, 649–662.PubMedCrossRefGoogle Scholar
- Becher, R., Hettwer, U., Karlovsky, P., Deising, H. B., & Wirsel, G. R. (2010). Adaptation of Fusarium graminearum to tebuconazole yielded descendants diverging for levels of fitness, fungicide resistance, virulence, and mycotoxin production. Phytopathology, 100, 444–453.PubMedCrossRefGoogle Scholar
- Beyer, M., Klix, M. B., Klink, H., & Verreet, J.-A. (2006). Quantifying the effects of previous crop, tillage, cultivar and triazole fungicides on the deoxynivalenol content of wheat grain—a review. Journal of Plant Diseases and Protection, 113, 241–246.Google Scholar
- Beyer, M., Pogoda, F., Hoffmann, L., Dubos, T., & Pasquali, M. (2010). Studies on the sensitivity of Fusarium graminearum towards trifloxystrobin. Julius-Kühn-Archiv, 428, 144–145.Google Scholar
- Brent, K. J., & Hollomon, D. W. (2007). Fungicide resistance in crop pathogens: How can it be managed? FRAC Monograph No. 2 (2nd ed., pp. 1–53). Brussels: Global Crop Protection Federation.Google Scholar
- Dekker, J. (1976). Acquired resistance to fungicides. Annual Review of Phytopathology, 14, 405–428.CrossRefGoogle Scholar
- de Melo Abreua, S., Cabonib, P., Cabrasb, P., Garaub, V. L., & Alves, A. (2006). Validation and global uncertainty of a liquid chromatographic with diode array detection method for the screening of azoxystrobin, kresoxim-methyl, trifloxystrobin, famoxadone, pyraclostrobin and fenamidone in grapes and wine. Analytica Chimica Acta, 573–574, 291–297.Google Scholar
- FCD (2010). Fusarium comparative database. http://www.broadinstitute.org/annotation/genome/fusarium_graminearum/MultiHome.html), Accessed 9 March 2010.
- FRAC (2009). List of plant pathogenic organisms resistant towards disease control agents. http://www.frac.info/frac/work/List%20of%20resistant%20plant%20pathogens_Jan%202009_web.pdf. Accessed 23 March 2010.
- Gale, L. R., Ward, T. J., Balmas, V., & Kistler, H. C. (2007). Population subdivision of Fusarium graminearum sensu stricto in the Upper Midwestern United States. Phytopathology, 97, 1434–1439.PubMedCrossRefGoogle Scholar
- Giraud, F., Pasquali, M., El Jarroudi, M., Vrancken, C., Brochot, C., Cocco, E., et al. (2010). Fusarium head blight and associated mycotoxin occurrence on winter wheat in Luxembourg in 2007/2008. Food Additives & Contaminants Part A, 27, 825–835.CrossRefGoogle Scholar
- Gisi, U., Sierotzki, H., Cook, A., & McCaffery, A. (2002). Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Management Science, 58, 859–867.PubMedCrossRefGoogle Scholar
- Goswami, R. S., & Kistler, H. C. (2005). Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology, 95, 1397–1404.PubMedCrossRefGoogle Scholar
- Gullino, M. L., Minuto, A., Gilardi, G., & Garibaldi, A. (2002). Efficacy of azoxystrobin and other strobilurins against Fusarium wilts of carnation, cyclamen and Paris daisy. Crop Protection, 21, 57–61.CrossRefGoogle Scholar
- Kaneko, I., & Ishii, H. (2009). Effect of azoxystrobin on activities of antioxidant enzymes and alternative oxidase in wheat head blight pathogens Fusarium graminearum and Microdochium nivale. Journal of General Plant Pathology, 75, 388–398.CrossRefGoogle Scholar
- Kim, Y. S., Dixon, E. W., Vincelli, P., & Farman, M. L. (2003). Field resistance to strobilurin (QoI) fungicides in Pyricularia grisea caused by mutations in the mitochondrial cytochrome b gene. Phytopathology, 93, 891–900.PubMedCrossRefGoogle Scholar
- Klix, M. B., Verreet, J.-A., & Beyer, M. (2007). Comparison of the declining triazole sensitivity of Gibberella zeae and increased sensitivity achieved by advances in triazole fungicide development. Crop Protection, 26, 683–690.CrossRefGoogle Scholar
- Liu, X., Jiang, J., Shao, J., Yin, Y., & Ma, Z. (2010). Gene transcription profiling of Fusarium graminearum treated with an azole fungicide tebuconazole. Applied Microbiology and Biotechnology, 85, 1105–1114.PubMedCrossRefGoogle Scholar
- Nirenberg, H. (1976). Untersuchungen über die morphologische und biologische Differenzierung in der Fusarium-Sektion Liseola. Mitteilungen aus der Biologischen Bundesanstalt für Land – und Forstwirtschaft. Berlin – Dahlem, 169, 1–93.Google Scholar
- O’Donnell, K., Kistler, H. C., Cigelnik, E., & Ploetz, R. C. (1998). Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proceedings of the National Academy of Sciences of the USA, 95, 2044–2049.PubMedCrossRefGoogle Scholar
- Parry, D. W., Jenkinson, P., & McLeod, L. (1995). Fusarium ear blight (scab) in small grain cereals—a review. Plant Pathology, 44, 207–238.CrossRefGoogle Scholar
- Pasquali, M., Giraud, F., Brochot, C., Hoffmann, L., & Bohn, T. (2009). First report of the nivalenol chemotype of Fusarium graminearum causing head blight of wheat in the Grand Duchy of Luxembourg. Plant Disease, 93, 1217.CrossRefGoogle Scholar
- Pasquali, M., Giraud, F., Brochot, C., Cocco, E., Hoffmann, L., & Bohn, T. (2010). Genetic Fusarium chemotyping as a useful tool for predicting nivalenol contamination in winter wheat. International Journal of Food Microbiology, 137, 246–253.PubMedCrossRefGoogle Scholar
- Ponts, N., Couedelo, N., Pinson-Gadais, L., Verdal-Bonnin, M.-N., Barreau, C., & Richard-Forget, F. (2009). Fusarium response to oxidative stress by H2O2 is trichothecene chemotype-dependent. FEMS Microbiology Letters, 293, 255–262.PubMedCrossRefGoogle Scholar
- Reuveni, M., & Sheglov, D. (2002). Effects of azoxystrobin, difenoconazole, polyoxin B (polar) and trifloxystrobin on germination and growth of Alternaria alternata and decay in red delicious apple fruit. Crop Protection, 21, 951–955.CrossRefGoogle Scholar
- Reverberi, M., Ricelli, A., Zjalic, S., Fabbri, A. A., & Fanelli, C. (2010). Natural functions of mycotoxins and control of their biosynthesis in fungi. Applied Microbiology and Biotechnology, 87, 899–911.PubMedCrossRefGoogle Scholar
- Russell, P. E. (2005). A century of fungicide evolution. Journal of Agricultural Science, 143, 11–25.CrossRefGoogle Scholar
- Siranidou, E., & Buchenauer, H. (2001). Chemical control of Fusarium head blight on wheat. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz, 108, 231–243.Google Scholar
- Starkey, D. E., Ward, T. J., Aoki, T., Gale, L. R., Kistler, H. C., Geiser, D. M., et al. (2007). Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genetics and Biology, 44, 1191–1204.PubMedCrossRefGoogle Scholar
- Torriani, S. F. F., Brunner, P. C., McDonald, B. A., & Sierotzki, H. (2009). QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Management Science, 65, 155–162.PubMedCrossRefGoogle Scholar
- Vogelgsang, S., Hecker, A., Musa, T., Dorn, B., & Forrer, H. R. (2011). On-farm experiments over five years in a grain maize—winter wheat rotation: effect of maize residue treatments on Fusarium graminearum infection and deoxynivalenol contamination of wheat. Mycotoxin Research. doi: 10.1007/s12550-010-0079-y.
- von der Ohe, C., Gauthier, V., Tamburic-Ilincic, L., Brule-Babel, A., Fernando, W., Clear, R. M., et al. (2010). A comparison of aggressiveness and deoxynivalenol production between Canadian Fusarium graminearum isolates with 3-acetyl and 15-acetyldeoxynivalenol chemotypes in field-grown spring wheat. European Journal of Plant Pathology, 127, 407–417.CrossRefGoogle Scholar
- VZP (2010). Verzeichnis zugelassener Pflanzenschutzmittel. https://portal.bvl.bund.de/psm/jsp/, Accessed 9 June 2010.
- Ward, T. J., Clear, R. M., Rooney, A. P., O’Donnell, K., Gaba, D., Patrick, S., et al. (2008). An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genetics and Biology, 45, 473–484.PubMedCrossRefGoogle Scholar
- Zhang, H., Zhang, Z., van der Lee, T., Chen, W. Q., Xu, J., Xu, J. S., et al. (2010). Population genetic analyses of Fusarium asiaticum populations from barley suggest a recent shift favoring 3ADON producers in southern China. Phytopathology, 100, 328–336.PubMedCrossRefGoogle Scholar