Skip to main content
SpringerLink
Log in

Detection and characterization of fungicide resistant phenotypes of Botrytis cinerea in lettuce crops in Greece

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

The development of resistance to chemical control agents needs continuous monitoring in Botrytis cinerea. 790 isolates from lettuce and other vegetable crops were collected from six widely separated sites in Greece and tested for their sensitivity to 11 fungicides from nine unrelated chemical groups. 44 of the isolates exhibited multiple resistance to fenhexamid (hydroxyanilides), azoxystrobin and pyraclostrobin (QoI’s), boscalid (SDHI’s), cyprodinil and pyrimethanil (anilinopyrimidines), fludioxonil (phenylpyrroles), carbendazim (benzimidazoles) and iprodione (dicarboximides). Thirty per cent of such phenotypes were detected in an experimental glasshouse with lettuce crops, the third year after commencing fungicide applications. The average resistance factor (Rf) for mycelial growth to fenhexamid, pyraclostrobin, boscalid, cyprodinil and fludioxonil, was over 40, 1,000, 100, 700 and 50, respectively. Some strains with high resistance to anilinopyrimidines (14 %) or moderate to fludioxonil (7 %) were detected even in isolates collected from vegetable crops prior to commercial use of these fungicides in Greece. Isolates with fludioxonil moderate resistance and fenhexamid high resistance, were detected for the first time in Greece. The results suggested the high risk in chemical control of grey mould due to development of resistance to most fungicides with site-specific modes of action. Isolates with resistance to fluazinam (phenylpyridinamines) and to chlorothalonil (phthalonitriles) were not found. The inclusion of appropriate multi-site inhibitors like chlorothalonil in fungicide anti-resistance strategies was indispensable.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

Ani:

anilinopyrimidines

Ben:

benzimidazoles

Bos:

boscalid

Chlo:

chlorothalonil

Dic:

dicarboximides

DMSO:

dimethyl sulfoxide

ED50 :

effective dose inhibiting the 50 % of mycelial growth or spore germination

Flu:

fluazinam

HR:

highly resistant

Hyd:

hydroxyanilides

MEA:

malt extract agar

MIC:

minimal inhibitory concentration

MR:

moderately resistant

PDA:

potato dextrose agar

Phen:

phenylpyrroles

QoI’s:

quinone outside inhibitors, strobilurins

Resistance factor (Rf):

average ED50 of resistant isolates/average ED50 of sensitive (wild type) isolates tested

R:

resistant

S:

sensitive

SDHI’s:

succinate dehydrogenase inhibitors, carboxamides

SHAM:

salicylhydroxamic acid

References

  • Banno, S., Yamashita, K., Fukumori, F., Okada, K., Uekusa, H., & Takagaki, M. (2009). Characterization of QoI resistance in Botrytis cinerea and identification of two types of mitochondrial cytochrome b gene. Plant Pathology, 58, 120–129.

    Article  CAS  Google Scholar 

  • Bardas, G. A., Myresiotis, C. K., & Karaoglanidis, G. S. (2008). Stability and fitness of anilinopyrimidine-resistant strains of Botrytis cinerea. Phytopathology, 98, 443–450.

    Article  PubMed  CAS  Google Scholar 

  • Bardas, G. A., Veloukas, T., Koutita, O., & Karaoglanidis, G. S. (2010). Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest Management Science, 66, 967–973.

    Article  PubMed  CAS  Google 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.

    Article  PubMed  CAS  Google Scholar 

  • Billard, A., Fillinger, S., Leroux, P., Lachaise, H., Beffa, R., & Debieu, D. (2011). Strong resistance to the fungicide fenhexamid entails a fitness cost in Botrytis cinerea as shown by comparisons of isogenic strains. Pest Management Science, 68, 684–691.

    Article  PubMed  Google Scholar 

  • Brent, K. J., & Hollomon, D. W. (Eds.). (2007). Fungicide resistance in crop protection: How can it be managed? FRAC Monograph No 1, second, and revised edition. Brussels: International Croplife.

    Google Scholar 

  • Debieu, D., Bach, J., Hugon, M., Malosse, C., & Leroux, P. (2001). The hydroxyanilide fenhexamid, a new sterol biosynthesis inhibitor fungicide efficient against the plant pathogenic fungus Botryotinia fuckeliana (Botrytis cinerea). Pest Management Science, 57, 1060–1067.

    Article  PubMed  CAS  Google Scholar 

  • Esterio, M., Ramos, C., Walker, A. S., Fillinger, S., Leroux, P., & Auger, J. (2011). Phenotypic and genetic characterization of Chilean isolates of Botrytis cinerea with different levels of sensitivity to fenhexamid. Phytopathologia Mediterranea, 50, 414–420.

    CAS  Google Scholar 

  • Faretra, F., & Pollastro, S. (1993). Isolation, characterization and genetic analysis of laboratory mutants of Botryotinia fuckeliana resistant to the phenylpyrrole fungicide CGA 173506. Mycological Research, 97, 620–624.

    Article  CAS  Google Scholar 

  • Fritz, R., Lanen, C., Colas, V., & Leroux, P. (1997). Inhibition of methionine biosynthesis in Botrytis cinerea by the anilinopyrimidine fungicide pyrimethanil. Pesticide Science, 49, 40–46.

    Article  CAS  Google 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.

    Article  PubMed  CAS  Google Scholar 

  • Guo, Z., Miyoshi, H., Komyoji, T., Haga, T., & Fujita, T. (1991). Uncoupling activity of a newly developed fungicide, fluazinam [3-chloro-N-(3-chloro-2,6-dinitro-4-trifluoromethylphenyl)-5-trifluoromethyl-2-pyridinamine]. Biochimica et Biophysica Acta, 1056, 89–92.

    Article  CAS  Google Scholar 

  • Heaney, S. P., Hall, A. A., Davies, S. A., & Olaya, G. (2000). Resistance to fungicides in the QoI-STAR cross-resistance group: current persectives. In Proceedings of Brighton Crop Protection Conference – Pests and Diseases, Brighton, U. K, November 13–16, 2000, Vol. 2, pp. 755–762. British Crop Protection Council

  • Hilber, U. W., Schuepp, H., & Schwinn, F. J. (1994). Resistance risk evaluation of fludioxonil, a new phenylpyrrole fungicide. In S. Heaney, D. Slawson, D. W. Hollomon, M. Smith, P. E. Russel, & D. W. Parry (Eds.), Fungicide resistance (pp. 397–402). U.K: British Crop Protection Council.

    Google Scholar 

  • Joseph-Horne, T., & Hollomon, D. W. (2000). Functional diversity within the mitochondrial electron transport chain of plant pathogenic fungi. Pest Management Science, 56, 24–30.

    Article  CAS  Google Scholar 

  • Kalamarakis, A. E., Petsikos-Panagiotarou, N., Mavroidis, B., & Ziogas, B. N. (2000). Activity of fluazinam against strains of Botrytis cinerea resistant to benzimidazoles and/or dicarboximides and to a benzimidazole-phenylcarbamate mixture. Journal of Phytopathology, 148, 449–455.

    Article  CAS  Google Scholar 

  • Kim, Y. K., & Xiao, C. L. (2010). Resistance to pyraclostrobin and boscalid in populations of Botrytis cinerea from stored apples in Washington State. Plant Disease, 94, 604–612.

    Article  CAS  Google Scholar 

  • Koike, S. T., Gladders, P., & Paulus, A. O. (Eds.). (2007). Vegetable diseases: A colour handbook. London: Manson Publishing Ltd.

    Google Scholar 

  • Korolev, N., Mamiev, M., Zahavi, T., & Elad, Y. (2011). Screening of Botrytis cinerea isolates from vineyards in Israel for resistance to fungicides. European Journal of Plant Pathology, 129, 591–608.

    Article  CAS  Google Scholar 

  • Leroux, P. (2004). Chemical control of Botrytis and its resistance to chemical fungicides. In Y. Elad, B. Williamson, P. Tudzinski, & N. Delen (Eds.), Botrytis: Biology, pathology and control (pp. 195–222). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  • Leroux, P., Chapeland, F., Desbrosses, D., & Gredt, M. (1999). Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Protection, 18, 687–697.

    Article  CAS  Google Scholar 

  • Leroux, P., Gredt, M., Leroch, M., & Walker, A. S. (2010). Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Applied and Environmental Microbiology, 76, 6615–6630.

    Article  PubMed  CAS  Google Scholar 

  • Mercier, J., Kong, M., & Cook, F. (2010). Fungicide resistance among Botrytis cinerea isolates from California strawberry fields. Plant Health Progress. doi:10.1094/PHP-2010-0806-01-RS.

    Google Scholar 

  • Moyano, C., Gomez, V., & Melgarejo, P. (2004). Resistance to pyrimethanil and other fungicides in Botrytis cinerea populations collected on vegetable crops in Spain. Journal of Phytopathology, 152, 484–490.

    Article  CAS  Google Scholar 

  • Myresiotis, C. K., Karaoglanidis, G. S., & Tzavella-Klonari, K. (2007). Resistance of Botrytis cinerea isolates from vegetable crops to anilinopyrimidine, phenylpyrrole, hydroxyanilide, benzimidazole, and dicarboximide fungicides. Plant Disease, 91, 407–413.

    Article  CAS  Google Scholar 

  • Pappas, A. C. (1997). Evolution of fungicide resistance in Botrytis cinerea in protected crops in Greece. Crop Protection, 16, 257–263.

    Article  CAS  Google Scholar 

  • Rosslenbroich, H. J., & Stuebler, D. (2000). Botrytis cinerea - history of chemical control and novel fungicides for its management. Crop Protection, 19, 557–561.

    Article  CAS  Google Scholar 

  • Stammler, G., Brix, H. D., Nave, B., Gold, R., & Schoelf, U. (2008). Studies on the biological performance of boscalid and its mode of action. In H. W. Dehne, H. B. Deising, U. Gisi, K. H. Kuck, P. E. Russell, & H. Lyr (Eds.), Proceedings of the 15th International Reinhardsbrunn Symposium on modern fungicides and antifungal compounds, Friedrichroda, Germany, May 6–10, 2007, pp. 45–51. Deutsche Phytomedizinische Gesellschaft

  • Tamura, O. (2000). Resistance development of grey mould on beans towards fluazinam and relevant counter-measures. In Proceedings of the 10th Symposium of Research Committee of Fungicides Resistance, Okayama, Japan, April 5, 2000, pp. 7–16. The Phytopathological Society of Japan

  • Veloukas, T., Leroch, M., Hahn, M., & Karaoglanidis, G. S. (2011). Detection and molecular characterization of boscalid-resistant Botrytis cinerea isolates from strawberry. Plant Disease, 95, 1302–1307.

    Article  CAS  Google Scholar 

  • Vignutelli, A., Hilber-Bodmer, M., & Hilber, U. W. (2002). Genetic analysis of resistance to the phenylpyrrole fludioxonil and the dicarboximide vinclozolin in Botryotinia fuckeliana (Botrytis cinerea). Mycological Research, 106, 329–335.

    Article  CAS  Google Scholar 

  • Weber, R. W. S. (2011). Resistance of Botrytis cinerea to multiple fungicides in northern German small-fruit production. Plant Disease, 95, 1263–1269.

    Article  CAS  Google Scholar 

  • Zhang, C. Q., Hu, J. L., Wei, F. L., & Zhu, G. N. (2009). Evolution of resistance to different classes of fungicides in Botrytis cinerea from greenhouse vegetables in Eastern China. Phytoparasitica, 37, 351–359.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agriculture, Crop Production and Rural Environment, Laboratory of Plant Pathology, University of Thessaly, Fitokou str., 384 46 N. Ionia, Volos, Greece

    Michael Chatzidimopoulos, Dimitris Papaevaggelou & Athanassios Christos Pappas

Authors
  1. Michael Chatzidimopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dimitris Papaevaggelou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Athanassios Christos Pappas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Chatzidimopoulos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chatzidimopoulos, M., Papaevaggelou, D. & Pappas, A.C. Detection and characterization of fungicide resistant phenotypes of Botrytis cinerea in lettuce crops in Greece. Eur J Plant Pathol 137, 363–376 (2013). https://doi.org/10.1007/s10658-013-0248-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-013-0248-x

Keywords

Search

Navigation