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Resistance to polyoxin AL and other fungicides in Botrytis cinerea collected from sweet basil crops in Israel

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Abstract

A total of 568 B. cinerea isolates were collected from diseased sweet basil plants and the air in 10 sweet basil greenhouses. Mycelial growth tests were used to evaluate the sensitivity of these isolates to benomyl, fenhexamid, iprodione, polyoxin AL and pyrimethanil. EC50 values for polyoxin, the main botryticide on sweet basil in Israel, ranged from 0.4 to 6.5 μg ml−1 and had a bimodal distribution; the EC50 values for sensitive isolates ranged from 0.4 to 1.5 μg ml−1 and the EC50 values for low-level resistant isolates ranged from 4 to 6.5 μg ml−1. Among populations that had not been exposed to polyoxin treatments, 20 to 35 % of the collected isolates were low-level resistant for polyoxin. Polyoxin treatments in an experimental greenhouse shifted the equilibrium in favour of low-level resistant isolates, and the change occurred rapidly: from a frequency of 20 % low-level resistant isolates in the population that had never been treated with polyoxin to a frequency of 72 % after a few treatments over two seasons. Prolonged use of polyoxin in Israeli basil crops (in some sites for more than 10 years) does not appear to have led to the development of high-level resistance, but low-level resistant isolates were found in commercial greenhouses with the frequency of up to 73 %. High-level resistance to benzimidazoles was common (60 to 80 % of isolates) in greenhouses with a history of benzimidazole treatments; whereas 15–25 % of the isolates from greenhouses in which fungicides were not used were resistant. Low-level resistance to dicarboximides was fairly widespread (frequency of 30 to 80 % depending on the greenhouse) and a few cases of moderate resistance to dicarboximides were also noted (frequency of 0 to 9 %). Neither high- nor low-level resistance to anilinopyrimidines was common in sweet basil commercial greenhouses (0 to 7 %). However, 34 % of the isolates were strongly resistant in the experimental greenhouse, following a few treatments with anilinopyrimidine fungicides during the previous season. Before those treatments, the proportion of anilinopyrimidines resistant isolates had been 1 %. About 3 % of the isolates exhibited low-level resistance to fenhexamid and no isolates were found to be strongly resistant to fenhexamid. Low-level resistance to one fungicide was often associated with low-level resistances to other fungicides. Thirty-two phenotypes exhibiting resistance to one or more of the tested fungicides were noted among B. cinerea isolates. Resistant isolates showed similar or reduced fitness parameters in comparison to wild-type isolates.

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References

  • Adachi, Y., Watanabe, H., & Tsuge, T. (1996). Relationships between genetic polymorphisms and fungicide resistance within Alternaria alternata. Phytopathology, 86, 1248–1254.

    Article  CAS  Google Scholar 

  • Baroffio, C. A., Siegfried, W., & Hilber, U. W. (2003). Long-term monitoring for resistance of Botryotinia fuckeliana to anilinopyrimidine, phenylpyrrole, and hydroxyanilide fungicides in Switzerland. Plant Disease, 87, 662–666.

    Article  CAS  Google Scholar 

  • Becker, J., Covert, N., Shenbagamurthi, P., Steinfeld, A., & Naider, F. (1983). Antimicrobial Agents and Chemotherapy, 23, 926–929.

    Article  PubMed  CAS  Google Scholar 

  • Chen, C., & Wong, F. P. (2008). In vitro sensitivity of Waited circinata var. circinata to fludioxonil and polyoxin-D. Phytopathology, 98, S37 (Abstract).

    Google Scholar 

  • Copping, L. G., & Menn, J. J. (2000). Biopesticides: a review of their action, application and efficacy. Pest Management Science, 56, 651–676.

    Article  CAS  Google Scholar 

  • Cui, W., Beever, R. E., Parkes, S. L., & Templeton, M. D. (2004). Evolution of an osmosensing histidine kinase in field strains of Botrytotinia fuckeliana (Botrytis cinerea) in response to dicarboximide fungicide usage. Phytopathology, 94, 1129–1135.

    Article  PubMed  CAS  Google Scholar 

  • De Waard, M. A., Andrade, A. C., Hayashi, K., Schoonbeek, H., Stergiopolus, I., & Zwiers, L. (2006). Impact of fungal drug transporters on fungal sensitivity, multidrug resistance and virulence. Pest Management Science, 62, 195–207.

    Article  PubMed  Google Scholar 

  • Edwards, S. G., & Seddon, B. (2001). Selective media for the specific isolation and enumeration of Botrytis cinerea conidia. Letters in Applied Microbiology, 32, 63–66.

    Article  PubMed  CAS  Google Scholar 

  • Elad, Y., Shabi, E., & Katan, T. (1988). Negative cross-resistance between benzimidazoles and N-phenylcarbamate fungicides and control of Botrytis cinerea on grapes. Plant Pathology, 37, 141–147.

    Article  CAS  Google Scholar 

  • Elad, Y., Yunis, H., & Katan, T. (1992). Multiple resistance to benzimidazoles, dicarboximides and diethophencarb in field isolates of Botrytis cinerea in Israel. Plant Pathology, 41, 41–46.

    Article  CAS  Google Scholar 

  • Esterio, M., Auger, J., & Garcia, H. (2007). First report of fenhexamid resistant isolates of Botrytis cinerea on grapevine in Chile. Plant Disease, 91, 768 (Abstr.).

    Article  Google Scholar 

  • Fillinger, S., Leroux, P., Auclair, C., Barreau, C., Al Hajj, C., & Debieu, D. (2008). Genetic analysis of fenhexamid-resistant field isolates of the phytopathogenic fungus Botrytis cinerea. Antimicrobial Agents and Chemotherapy, 52, 3933–3940.

    Article  PubMed  CAS  Google Scholar 

  • Fillinger, S., Ajouz, S., Nicot, P. C., Leroux, P., Bardin, M. (2012). Functional and structural comparison of pyrrolnitrin- and iprodione-induced modifications in the class III histidine-kinase Bos1 of Botrytis cinerea. PLoS Pathogens, 7, Article e42520. http://www.plospathogens.org. Accessed 7 November 2012.

  • Fidanza, M., & Davis, D. (2009). In vitro screening of fungicides to control artillery fungi. Journal of Environmental Horticulture, 27, 155–158.

    CAS  Google Scholar 

  • Förster, H., Driever, G. F., Thompson, D. C., & Adaskaveg, J. E. (2007). Postharvest decay management for stone fruit crops in California using the “reduced-risk” fungicides fludioxonil and fenhexamid. Plant Disease, 91, 209–215.

    Article  Google Scholar 

  • Gamliel, A., & Yarden, O. (1998). Diversification of diseases affecting herb crops in Israel accompanies the increase in herb crop production. Phytoparasitica, 26, 53–58.

    Article  Google Scholar 

  • Garibaldi, A., Gullino, L., & Minuto, G. (1997). Diseases of basil and their management. Plant Disease, 81, 124–132.

    Article  Google Scholar 

  • Gooday, C. W. (1979). The action of polyoxin on fungi. In H. Lyr & C. Polter (Eds.), Systemfungizide (pp. 159–168). Berlin: Akademie-Verlag.

    Google Scholar 

  • Gullino, M. L., & Shoemaker, R. A. (1994). Social and political implication of managing plant disease with restricted fungicides in Europe. Annual Review of Phytopathology, 32, 559–579.

    Article  PubMed  CAS  Google Scholar 

  • Hilber, U. W., & Hilber-Bodmer, M. (1998). Genetic basis and monitoring of resistance of Botryotinia fuckeliana to anilinopyrimidines. Plant Disease, 82, 496–500.

    Article  CAS  Google Scholar 

  • Hwang, B. K., & Yun, J. H. (1986). Variability in sensitivity to polyoxin B of isolates of Alternaria mali and decreased fitness of polyoxin-resistant isolates. Journal of Phytopathology, 115, 305–312.

    Article  CAS  Google Scholar 

  • Iida, W. (1975). On the tolerance of plant pathogenic fungi and bacteria to fungicides in Japan. Japan Pesticide Information, 23, 13–16.

    CAS  Google Scholar 

  • Kato, T. (1988). Resistance experience in Japan. In C. Delp (Ed.), Fungicide resistance in North America (pp. 16–18). St. Paul: APS Press.

    Google Scholar 

  • Keymanesh, K., Soltani, S., & Sardari, S. (2009). Application of antimicrobial peptides in agriculture and food industry. World Journal of Microbiology and Biotechnology, 25, 933–944.

    Article  Google Scholar 

  • Koh, Y. J., Lee, J. G., Seo, J. K., Moon, D.-K., & Han, H.-R. (1998). Fungicide resistance and genetic diversity of Botrytis cinerea of citrus. Korean Journal of Plant Pathology, 14, 682–688 (in Korean, abstract in English).

    Google Scholar 

  • Köller, W., Wilcox, W., Barnard, J., & Braun, P. (1997). Detection and quantification of resistance of Venturia inaequalis populations to sterol demethylation inhibitors. Phytopathology, 87, 184–190.

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kretschmer, M., Leroch, M., Mosbach, A., Walker, A.-S., Fillinger, S., Mernke, D., et al. (2009, December 5). Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathogens, 5, Article e1000696. http://www.plospathogens.org. Accessed 15 June 2010.

  • Leroch, M., Kretschmer, M., & Hahn, M. (2011). Fungicide resistance phenotypes of Botrytis cinerea isolates from commercial vineyards in south west Germany. Journal of Phytopathology, 159, 63–65.

    Article  CAS  Google Scholar 

  • Leroux, P. (2004). Chemical control of Botrytis and its resistance to chemical fungicides. In Y. Elad, P. 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., Fritz, R., Debieu, D., Albertini, C., Lanen, C., Bach, J., et al. (2002). Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Management Science, 58, 876–888.

    Article  PubMed  CAS  Google Scholar 

  • Lichtnaier, L. (Ed.). (2011). Pesticides for plant protection registered for use and sale in Israel. Bet-Dagan: Ministry of Agriculture and Rural Development, Plant Protection and Inspection Services.

    Google Scholar 

  • Ma, Z., & Michailides, T. J. (2005). Genetic structure of Botrytis cinerea populations from different host plants in California. Plant Disease, 89, 1083–1089.

    Article  CAS  Google Scholar 

  • Morton, V., & Staub, T. (2008). A short history of fungicides. APSnet Feature, March 2008. http://apsnet.org/online/feature/fungi. Accessed 2/2012.

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

    Article  CAS  Google Scholar 

  • Nakajima, M., Suzuki, J., Hosaka, T., Hibi, T., & Akutsu, K. (2001). Functional analysis of an ATP-binding cassette transporter gene in Botrytis cinerea by gene disruption. Journal of General Plant Pathology, 67, 212–214.

    Article  CAS  Google Scholar 

  • Nishimura, S., Kohmoto, K., & Udagawa, H. (1973). Field emergence of fungicide-tolerant strains in Alternaria kikuchiana Tanaka. Reports of Tottori Institute of Mycology (Japan), 10, 677–686.

    Google Scholar 

  • Sakurai, H., & Fujita, S. (1978). The antifungal activity of Polyoxin B and Iprodione against phytopathogenic fungi recently isolated from diseased plants in Japan. Pesticide Science, 9, 207–212.

    Article  CAS  Google Scholar 

  • Sharabani, G., Shtienberg, D., Elad, Y., & Dinoor, A. (1999). Epidemiology of Botrytis cinerea in sweet basil and implications for disease management. Plant Disease, 83, 554–560.

    Article  Google Scholar 

  • Tanaka, C., Shimizu, K., Gafur, A., & Tsuda, M. (2002). Polyoxin resistance of reddish brown laboratory mutants of Cochliobolus heterostrophus. Journal of General Plant Pathology, 68, 141–146.

    Article  CAS  Google Scholar 

  • Woodcock, D. (1977). Structure – activity relationships. In R. W. Marsh (Ed.), Systemic fungicides (pp. 32–84). London: Longman.

    Google Scholar 

  • Yamaguchi, I., & Fujimura, M. (2005). Recent topics on action mechanisms of fungicides. Journal of Pesticide Science, 30, 67–74.

    Article  CAS  Google Scholar 

  • Yermiyahu, U., Shamai, I., Peleg, R., Dudai, N., & Shtienberg, D. (2006). Reduction of Botrytis cinerea sporulation in sweet basil by altering the concentrations of nitrogen and calcium in the irrigation solution. Plant Pathology, 55, 544–552.

    Article  CAS  Google Scholar 

  • Yourman, L. F., & Jeffers, S. N. (1999). Resistance to benzimidazole and dicarboximide fungicides in greenhouse isolates of Botrytis cinerea. Plant Disease, 83, 569–575.

    Article  CAS  Google Scholar 

  • Yourman, L. F., Jeffers, S. N., & Dean, R. A. (2001). Phenotype instability in Botrytis cinerea in the absence of benzimidazole and dicarboximide fungicides. Phytopathology, 91, 307–315.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was partially supported by a fellowship from the Israeli Ministry of Immigration, the research fund of the Herb Growers’ Board and the Chief Scientist of the Israeli Ministry of Agriculture and Rural Development, Project no. 132–1408. Contribution No 509/12 from the ARO, Volcani Center, Institute of Plant Protection.

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  1. Department of Plant Pathology and Weed Research, ARO, The Volcani Center, Bet Dagan, 50250, Israel

    Mukhiddin Mamiev, Nadia Korolev & Yigal Elad

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  1. Mukhiddin Mamiev
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  2. Nadia Korolev
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  3. Yigal Elad
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Correspondence to Nadia Korolev.

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Mamiev, M., Korolev, N. & Elad, Y. Resistance to polyoxin AL and other fungicides in Botrytis cinerea collected from sweet basil crops in Israel. Eur J Plant Pathol 137, 79–91 (2013). https://doi.org/10.1007/s10658-013-0218-3

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