Abstract
Zymoseptoria tritici is a dominant pathogen in wheat causing Septoria leaf blotch (SLB), and sterol 14α-demethylation inhibitors fungicides (DMI) are commonly used for control in Northern Europe. In 14 winter wheat trials carried out in Denmark, Lithuania, and Sweden in the years 2011 to 2013, fungicides containing DMIs were investigated for their efficacy and impact on CYP51 mutations in Z. tritici populations. All fungicide treatments were applied twice – each time using 50 % of the standard rate, applied at GS 37 & 55. The single-agent DMIs, epoxiconazole and prothioconazole and a mixture of difenoconazole + propiconazole gave similar control and crop yields. The best solution varied among localities. Adding prochloraz to prothioconazole as well as using co-formulations of DMIs + SDHIs generally improved control compared with using DMIs alone. Yield responses were significant from all treatments, but co-formulations of DMIs plus SDHIs increased yield the most. Specific CYP51 mutations in Z. tritici were analysed by pyrosequencing and qPCR. Their frequency varied across sites and countries. The amount of I381V was high in all trials whereas the amount of A379G was moderate. Levels of D134G, V136C, and S524T were low to moderate across all sites. DMIs and mixtures of DMIs + SDHI selected differently for CYP51 mutations. Prochloraz increased selection for D134G and V136A and decreased selection for A379G and I381V. The lowest selection pressure towards D134G and V136A/C was recorded in the presence of the mixture difenoconazole and propioconazole. Mixtures of DMIs and SDHI tended to lower the frequency of V136A/C compared to DMIs used alone but had no measurable impact on the frequency of I381V and A379G. No responses were seen in relation to S524T, which only occurred at a very low level.
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References
Anonymous (2014). http://www.hgca.com/media/547811/Fungicide-performance-in-wheat-2014-V2.pdf.
Buitrago, C., Frey, R., Wullschleger, J., & Sierotzki, H. (2013). An update on the genetic changes in the CYP51 gene of Mycosphaerella graminicola and their relationship to DMI fungicide sensitivity. In H. W. Dehne, Deising H.B., Fraaije B., U. Gisi, Hermann D., Mehl A., et al. (Eds.), 17th International Reinhardsbrunn Symposium, Friedrichroda, Germany, 21–23 April 2013 (pp. 103–110). Braunschweig: DPG Verlag
Chassot, C., Hugelshofer, U., Sierotzki, H., & Gisi, U. (2008). Sensitivity of CYP51 genotypes to DMI fungicides in Mycosphaerella graminicola. In Deising H. B., Dehne H. W., Gisi U., Kuck K. H., Russell P. E., Stammler G., et al. (Eds.), 15th International Reinhardsbrunn Symposium, Friedrichroda, Germany, 2008 (pp. 129–136). Braunschweig: DPG Verlag
Clark, W. S. Septoria tritici and azole performance. In Bryson R.J., Burnett F.J., Foster V., Fraaije B.A., & K. R. (Eds.), Aspects of Applied Biology. Fungicide resistance: Are we winning the battle but losing the war?, Edinburgh, 2006 (Vol. 78, pp. 127–132): Warwick HRI
Cools, H. J., & Fraaije, B. A. (2012). Resistance to azole fungicides in Mycophaerella graminicola: Mechanisms and management. In T. S. Thind (Ed.), Fungicide resistance in crop protection: Risk and management (pp. 64–75). Wallingford: U.K.: CAB International.
Cools, H. J., & Fraaije, B. A. (2013). Update on mechanisms of azole resistance in Mycosphaerella graminicola and implications for future control. Pest Management Science, 69(2), 150–155. doi:10.1002/ps.3348.
Cools, H. J., Mullins, J. G. L., Fraaije, B. A., Parker, J. E., Kelly, D. E., Lucas, J. A., et al. (2011). Impact of recently emerged sterol 14 alpha-demethylase (CYP51) variants of mycosphaerella graminicola on azole fungicide sensitivity. Applied and Environmental Microbiology, 77(11), 3830–3837. doi:10.1128/aem.00027-11.
Fraaije, B. A., Cools, H. J., Fountaine, J., Lovell, D. J., Motteram, J., West, J. S., et al. (2005). Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology, 95(8), 933–941. doi:10.1094/phyto-95-0933.
Fraaije, B. A., Cools, H. J., Kim, S. H., Motteram, J., Clark, W. S., & Lucas, J. A. (2007). A novel substitution I381V in the sterol 14 alpha-demethylase (CYP51) of Mycosphaerella graminicola is differentially selected by azole fungicides. Molecular Plant Pathology, 8(3), 245–254. doi:10.1111/j.1364-3703.2007.00388.X.
Fraaije, B. A., Bayon, C., Atkins, S., Cools, H. J., Lucas, J. A., & Fraaije, M. W. (2012). Risk assessment studies on succinate dehydrogenase inhibitors, the new weapons in the battle to control Septoria leaf blotch in wheat. Molecular Plant Pathology, 13(3), 263–275. doi:10.1111/j.1364-3703.2011.00746.x.
Germer, S., Holland, M. J., & Higuchi, R. (2000). High-throughput SNP allele-frequency determination in pooled DNA samples by kinetic PCR. Genome Research, 10(2), 258–266. doi:10.1101/gr.10.2.258.
Gigot, C., Saint-Jean, S., Huber, L., Maumene, C., Leconte, M., Kerhornou, B., et al. (2013). Protective effects of a wheat cultivar mixture against splash-dispersed septoria tritici blotch epidemics. Plant Pathology, 62(5), 1011–1019. doi:10.1111/ppa.12012.
Gisi, U., Pavic, L., Stanger, C., Hugelshofer, U., & Sierotzki, H. Dynamics of Mycosphaerella graminicola populations in response to selection by different fungicides. In Dehne H.W., Gisi U., Kuck K.H., Russell P.E., & L. H. (Eds.), 14th International Reinhardsbrunn Symposium, Alton, United Kingdom, 2005 (pp. 89–101): BCPC
Gladders, P., Paveley, N. D., Barrie, I. A., Hardwick, N. V., Hims, M. J., Langton, S., et al. (2001). Agronomic and meteorological factors affecting the severity of leaf blotch caused by Mycosphaerella graminicola in commercial wheat crops in England. Annals of Applied Biology, 138(3), 301–311. doi:10.1111/j.1744-7348.2001.tb00115.x.
Griffin, M. J., & Fisher, N. (1985). Laboratory studies on benzimidazole resistance in Septoria tritici. EPPO Bulletin, 15(4), 505–511. doi:10.1111/j.1365-2338.1985.tb00262.x.
Hobbelen, P. H. F., Paveley, N. D., & van den Bosch, F. (2014). The emergence of resistance to fungicides. Plos One, 9(3), 14. doi:10.1371/journal.pone.0091910.
Jørgensen, L. N., Hovmøller, M. S., Hansen, J. G., Lassen, P., Clark, B., Bayles, R., et al. (2014). IPM Strategies and Their Dilemmas Including an Introduction to www.eurowheat.org. [Review]. Journal of Integrative Agriculture, 13(2), 265–281, doi:10.1016/s2095-3119(13)60646-2.
Kildea, S., Mehenni-Ciz, J., Spink, J., & O’Sullivan, E. (2014). Changes in the frequency of Irish Mycophaerella graminicola CYP51 variants 2006–2011. In Dehne H W, Deising H B, Fraaije B, Gisi U, Hermann D, Mehl A, et al. (Eds.), 17th International Reinhardsbrunn Symposium, Friedrichroda, Germany, 2014 (pp. 143–144). Braunschweig, Germany: DPG Verlag
Kudsk, P. (2010). Norbarag (nordic baltic resistance action group) – A new resistance action group covering Denmark, Estonia, Finland, Latvia, Lithuania, Norway and Sweden. Outlooks on Pest Management, 21(5), 223–224. doi:10.1564/21oct06.
Leroux, P., & Walker, A. S. (2011). Multiple mechanisms account for resistance to sterol 14 alpha-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Management Science, 67(1), 44–59. doi:10.1002/ps.2028.
Leroux, P., Walker, A. S., Albertini, C., & Gredt, M. (2006). Resistance to fungicides in French populations of Septoria tritici, the causal agent of wheat leaf blotch. In Bryson R.J., Burnett F.J., Foster V., Fraaije B.A., & K. R. (Eds.), Aspects of Applied Biology. Fungicide Resistance: Are we winning the battle but losing the war?, Edinburgh, 2006 (Vol. 78, pp. 153–162). Warwick: Warwick HRI
Leroux, P., Albertini, C., Gautier, A., Gredt, M., & Walker, A. S. (2007). Mutations in the CYP51 gene correlated with changes in sensitivity to sterol 14 alpha-demethylation inhibitors in field isolates of Mycosphaerelia graminicola. Pest Management Science, 63(7), 688–698. doi:10.1002/ps.1390.
Paveley, N. D., Lockley, D., Vaughan, T. B., Thomas, J., & Schmidt, K. (2000). Predicting effective fungicide doses through observation of leaf emergence. Plant Pathology, 49(6), 748–766. doi:10.1046/j.1365-3059.2000.00518.x.
RCoreTeam (2014). R: A Language and Environment for Statistical Computing. Vienna, Austria
Stammler, G., & Semar, M. (2011). Sensitivity of Mycosphaerella graminicola (anamorph: Septoria tritici) to DMI fungicides across Europe and impact on field performance. EPPO Bulletin, 48(2), 149–155. doi:10.1111/j.1365-2338.2011.02454.x.
Stammler, G., Carstensen, M., Koch, A., Semar, M., Strobel, D., & Schlehuber, S. (2008). Frequency of different CYP51-haplotypes of Mycosphaerella graminicola and their impact on epoxiconazole-sensitivity and -field efficacy. Crop Protection, 27(11), 1448–1456. doi:10.1016/j.cropro.2008.07.007.
Stammler, G., Taher, K., Koch, A., Haber, J., Liebmann, B., Bouagila, A., et al. (2012). Sensitivity of Mycosphaerella graminicola isolates from Tunisia to epoxiconazole and pyraclostrobin. Crop Protection, 34, 32–36. doi:10.1016/j.cropro.2011.11.007.
Thygesen, K., Jørgensen, L. N., Jensen, K. S., & Munk, L. (2009). Spatial and temporal impact of fungicide spray strategies on fungicide sensitivity of Mycosphaerella graminicola in winter wheat. European Journal of Plant Pathology, 123(4), 435–447. doi:10.1007/s10658-008-9381-3.
van den Bosch, F., Paveley, N., Shaw, M., Hobbelen, P., & Oliver, R. (2011). The dose rate debate: does the risk of fungicide resistance increase or decrease with dose? Plant Pathology, 60(4), 597–606. doi:10.1111/j.1365-3059.2011.02439.x.
van den Bosch, F., Paveley, N., van den Berg, F., Hobbelen, P., & Oliver, R. (2014). Mixtures as a fungicide resistance management tactic. Phytopathology, 104(12), 1264–1273. doi:10.1094/phyto-04-14-0121-rvw.
Zadoks, J. C., Chang, C. C., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14(6), 415–421. doi:10.1111/j.1365-3180.1974.tb01084.x.
Acknowledgments
The authors would like to acknowledge the technicians at Aarhus University, Flakkebjerg (DK), Hushållningssällskapet, Malmöhus (SWE) and Institute for Agriculture, Dotnuva (LT) for carrying out the practical part of the field trials. We also like to thank BASF SE, Bayer CropScience, and Syngenta Crop Protection for financial support of the trials and for their involvement in CYP51 characterisation.
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Wieczorek, T.M., Berg, G., Semaškienė, R. et al. Impact of DMI and SDHI fungicides on disease control and CYP51 mutations in populations of Zymoseptoria tritici from Northern Europe. Eur J Plant Pathol 143, 861–871 (2015). https://doi.org/10.1007/s10658-015-0737-1
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DOI: https://doi.org/10.1007/s10658-015-0737-1