Skip to main content
SpringerLink
Log in

Occurrence of Cercospora beticola Sacc populations resistant to benzimidazole, demethylation-inhibiting, and quinone outside inhibitors fungicides in Morocco

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

Abstract

The sugar beet crop is essential for the production of refined sugar in Morocco. It is cultivated in four large areas (Gharb, Tadla, Doukalla, and Moulouya). A reported reduction in efficacy for fungicide treatments led to an in vitro sensitivity study of isolates collected in 2017 and 2018 from sugar beet areas. After authentication of the pathogen by specific primers amplifying 959 pb of the actin gene of Cercospora beticola Sacc, the inhibition tests on a modified medium by different fungicide molecules belonging to three groups (benzimidazole, demethylation inhibitors, and quinone outside inhibitors) were carried out. Measurement of inhibition allowed the calculation of EC50, which showed that resistance is present in isolates collected for the three fungicide groups with different levels by group and year. All isolates were resistant to thiophanate methyl (EC50 > 5 ppm) in 2017 and 2018. At least 70% of the isolates (in 2018) were resistant to azoxystrobin (EC50 > 10 ppm) and at least 68% of the isolates (in 2018) were resistant to difenoconazole (EC50 > 0.01 ppm). In parallel, in vivo tests on three sites in the Gharb area were conducted during 2017 and 2018 to monitor the severity of Cercospora beticola on the host under different fungicide treatments (thiophanate methyl, chlorothalonil, tetraconazole, epoxiconazole, difenoconazole, penthiopyrad, azoxystrobin, trifloxystrobin, and Pythium oligandrum) by measuring the area under the disease progress curve. The fungicide molecules all had better efficacy in preventive treatment, with the best results for trifloxystrobin, difenoconazole, and epoxiconazole. In curative treatment, three molecules stood out: trifloxystrobin, difenoconazole, and penthiopyrad.

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

Data availability

All data are available.

References

  • Anesiadis, T., Karaoglanidis, G. S., & Tzavella-Klonari, K. (2003). Protective, curative and eradicant activity of the strobilurin fungicide azoxystrobin against Cercospora beticola and Erysiphe betae. Journal of Phytopathology, 151, 647–651.

    Article  CAS  Google Scholar 

  • Balau, A. M., & Faretra, F. (2010). Molecular method for detection of Cercospora beticola Sacc. Lucrăriştiinţifice (Seria Agronomie), 53(1), 1–3.

    Google Scholar 

  • Bolton, M., Birla, K., Rivera-Varas, V., Rudolph, K. D., & Secor, G. A. (2012). Characterization of CbCyp51 from field isolates of Cercospora beticola. Phytopathology, 102, 298–305.

    Article  CAS  Google Scholar 

  • Dafang, H., & Shuzhi, W. X. Z. (1982). Studies on resistance of Cercospora beticola to benzimidazole fungicides. Journal of Plant Protection, 2, 11.

    Google Scholar 

  • Délye, C., & Corio-Costet, M. F. (1998). Origin of primary infections of grape powdery mildew Uncinula necator : RAPD analysis discriminates two biotypes. Mycological Research, 102, 283–288.

    Article  Google Scholar 

  • Doyle, J. J., & Doyle, J. L. (1990). Isolation of plant DNA from fresh tissue. Focus, 12, 13–15.

    Google Scholar 

  • El Housni, Z., Ezrari, S., Tahiri, A., & Ouijja, A. (2020). Resistance of Cercospora beticola Sacc isolates to thiophanate methyl (benzimidazole), demethylation inhibitors and quinone outside inhibitors in Morocco. EPPO Bulletin, 50(2), 350–357.

    Article  Google Scholar 

  • Ezrari, S., Lahlali, R., Radouane, N., Tahiri, A., Asfers, A., Boughalleb-M’Hamdi, N., ... & Lazraq, A. (2021). Characterization of Fusarium species causing dry root rot disease of citrus trees in Morocco. Journal of Plant Diseases and Protection, 128(2), 431–447. https://doi.org/10.1007/s41348-020-00392-0

  • Ezzahiri, B. (2013). Guide de protection phytosanitaire de la betterave à sucre au Maroc. AMPP, 1ère édition.

  • Franc, G. D. (2010). Ecology and epidemiology of Cercospora beticola. In R. T. Lartey et al. (Eds.), Cercospora leaf spot of sugar beet and related species (pp. 7–19). The American Phytopathological Society.

    Google Scholar 

  • Franc, G. D., Harveson, R. M., Kerr, E. D., & Jacobsen, B. J. (2001). Disease management. In Sugarbeet Production Guide. University of Nebraska Cooperative Extension EC01–156 (pp. 131–160). University of Nebraska.

  • Georgopoulos, S., & Dovas, C. (1973). A serious outbreak of strains of Cercospora beticola resistant to benzimidazole fungicides in northern Greece. Plant Disease Report, 57, 321–324.

    Google Scholar 

  • Harveson, R. M. (2013). Cercospora leaf spot of sugar beet. NebGuide.

  • Holtschulte, B. (2000). Cercospora beticola worldwide distribution and incidence. In M. J. C. Asher, B. Holtschulte, R. Molard, F. Rosso, G. Steinruecken, & R. Beckers (Eds.), Advances in sugar beet research: Cercospora beticola Sacc. Biology, agronomic influence and control measures in sugar beet (Vol. 2, pp. 5–16).

    Google Scholar 

  • Jacobsen, B. J. (2010). Integrated management of Cercospora leaf spot. In R. T. Lartey, J. J. Weiland, L. Panella, P. W. Crous, & C. E. Windels (Eds.), Cercospora leaf spot of sugar beet and related species (pp. 275–284). The American Phytopathological Society.

    Google Scholar 

  • Jacobsen, B. J., & Franc, G. D. (2009). Cercospora leaf spot. In R. M. Harveson, L. E. Hanson, & G. L. Hein (Eds.), Compendium of beet diseases and pests (2nd ed.).

    Google Scholar 

  • Karadimos, D. A., & Karaoglanidis, G. S. (2006). Comparative efficacy, selection of effective partners, and application time of strobilurin fungicides for control of cercospora leaf spot of sugar beet. Plant Disease, 90(6), 820–825.

    Article  CAS  Google Scholar 

  • Karaoglanidis, G. S., & Bardas, G. (2006). Control of benzimidazole-and DMI-resistant strains of Cercospora beticola with strobilurin fungicides. Plant Disease, 90(4), 419–424.

    Article  CAS  Google Scholar 

  • Karaoglanidis, G. S., Ioannidis, P. M., & Thanassoulopoulos, C. C. (2000). Reduced sensitivity of Cercospora beticola to sterol-demethylation inhibiting fungicides. Plant Pathology, 49, 567–572.

    Article  CAS  Google Scholar 

  • Karaoglanidis, G. S., Ioannidis, P. M., & Thanassoulopoulos, C. C. (2001). Influence of fungicide spray schedules on the sensitivity of Cercospora beticola to the sterol demethylation-inhibiting fungicide flutriafol. Crop Protection, 20(10), 941–947.

    Article  Google Scholar 

  • Karaoglanidis, G. S., Karadimos, D. A., Ioannidis, P. M., & Ioannidis, P. I. (2003). Sensitivity of Cercospora beticola populations to fentin-acetate, benomyl and flutriafol in Greece. Crop Protection, 22(5), 735–740.

    Article  CAS  Google Scholar 

  • Kayamori, M., Shimizu, M., Yamana, T., Komatsu, T., Minako, S., Shinmura, A., ... & Yasuoka, S. (2020). First report of QoI resistance in Cercospora beticola in sugar beet in Japan. Journal of General Plant Pathology, 86(2), 149–153.

  • Kerr, E. D., & Weiss, A. (1990). Fungicide efficacy and yield responses to fungicide treatments based on predictions of Cercospora leaf spot of sugar beet. Journal of Sugar Beet Research, 27, 58–71.

    Article  Google Scholar 

  • Khan, M. F. (2015). Sugar beet diseases: Cercospora leaf spot. In Fungicide Resistance in Plant Pathogens (pp. 379–387). Springer.

  • Khan, J., Del Río, L. E., Nelson, R., & Khan, M. F. R. (2007). Improving the Cercospora leaf spot management model for sugar beet in Minnesota and North Dakota. Plant Disease, 91(9), 1105–1108.

    Article  CAS  Google Scholar 

  • Lartey, R. T., Weiland, J. J., & Bucklin-Comiskey, S. (2003). A PCR protocol for rapid detection of Cercospora beticola in sugarbeet tissues. Journal of Sugar Beet Research, 40(1/2), 1–10.

    Article  Google Scholar 

  • Meriggi, P., Rosso, F., Ioannides, P. M., & Ayala Garcia, J. (2000). Fungicide treatments against Cercospora leaf spot in sugar beet (Beta vulgaris L.). Advances in Sugar Beet Research IIRB, 2, 77–102.

    Google Scholar 

  • Muellender, M. M., Mahlein, A. K., Stammler, G., & Varrelmann, M. (2020). Evidence for the association of target-site resistance in cyp51 with reduced DMI sensitivity in European Cercospora beticola field isolates. Pest Management Science, 77(4), 1765–1774.

    Article  Google Scholar 

  • ONSSA. (n.d.). Office National de Securité Sanitaire des Produits Alimentaires. http://eservice.onssa.gov.ma/IndPesticide.aspx

  • Pethybridge, S. J., Vaghefi, N., & Kikkert, J. R. (2017). Management of Cercospora leaf spot in conventional and organic table beet production. Plant Disease, 101(9), 1642–1651.

    Article  CAS  Google Scholar 

  • Piszczek, J., Pieczul, K., & Kiniec, A. (2018). First report of G143A strobilurin resistance in Cercospora beticola in sugarbeet (Beta vulgaris) in Poland. Journal of Plant Diseases and Protection, 125(1), 99–101. https://doi.org/10.1007/s41348-017-0119-3

  • Pool, V. W., & McKay, M. B. (1916). Climatic conditions as related to Cercospora beticola Sacc. Journal of Agricultural Research, 6, 21–60.

    Google Scholar 

  • Rossi, V., Meriggi, P., Biancardi, E., & Rosso, F. (2000). Effect of Cercospora leaf spot on sugar beet growth, yield and quality. In M. J. C. Asher, B. Holtschulte, M. Richard Molard, F. Rosso, G. Steinruecken, & R. Beckers (Eds.), Advances in sugar beet research Vol. 2:Cercospora beticola Sacc. Biology, agronomic influence and control measures in sugar beet (pp. 49–76). International Institute for Beet Research.

    Google Scholar 

  • Ruppel, E. G. (1986). Cercospora leaf spot. In E. D. Whitney & J. E. Duffus (Eds.), Compendium of beet diseases and insects (pp. 8–9). American Phytopathological Society.

    Google Scholar 

  • Ruppel, E., & Scott, P. (1974). Strains of Cercospora beticola resistant to benomyl in the USA. Plant Disease Report, 58, 434–436.

    Google Scholar 

  • Schnabel, G., Amiri, A., & Brannen, P. M. (2012). Field kit-and internet-supported fungicide resistance monitoring. In T. S. Thind (Ed.), Fungicide Resistance in Crop Protection Risk and Management (pp. 116–132). CAB International.

    Chapter  Google Scholar 

  • Secor, G. A., Rivera, V. V., Khan, M. F. R., & Gudmestad, N. C. (2010). Monitoring fungicide sensitivity of Cercospora beticola of sugar beet for disease management decisions. Plant Disease, 94(11), 1272–1282.

    Article  Google Scholar 

  • Smith, G. A., & Martin, S. S. (1978). Differential response of sugar beet cultivars to Cercospora leaf spot disease. Crop Science, 18, 39–41.

    Article  CAS  Google Scholar 

  • Smith, G. A., & Ruppel, E. G. (1973). Association of Cercospora leaf spot, gross sucrose, percentage sucrose, and root weight in sugar beet. Canadian Journal of Plant Science, 53, 695–696.

    Article  CAS  Google Scholar 

  • Sombardier, A., Dufour, M. C., Blancard, D., & Corio-Costet, M. F. (2010). Sensitivity of Podosphaera aphanis isolates to DMIs fungicides: Distribution and reduced cross-resistance. Pest Management Science, 66, 35–43.

    Article  CAS  Google Scholar 

  • Takenaka, S., & Tamagake, H. (2009). Foliar spray of a cell wall protein fraction from the biocontrol agent Pythium oligandrum induces defence-related genes and increases resistance against leaf spot in sugar beet. Journal of General Plant Pathology, 75(5), 340–348.

    Article  Google Scholar 

  • Trkulja, N., Ivanovic, Ž., Pfaf-Dolovac, E., Dolovac, N., Mitrovic, M., Toševski, I., & Jovic, J. (2013). Characterisation of benzimidazole resistance of Cercospora beticola Sacc in Serbia using PCR-based detection of resistance-associated mutations of the ß-tubulin gene. European Journal of Plant Pathology, 135, 889–902. https://doi.org/10.1007/s10658-012-0135-x

    Article  CAS  Google Scholar 

  • Trkulja, N., Milosavljević, A., Stanisavljević, R., Mitrović, M., Jović, J., Toševski, I., & Bošković, J. (2015). Occurrence of Cercospora beticola populations resistant to benzimidazoles and demethylation-inhibiting fungicides in Serbia and their impact on disease management. Crop Protection, 75, 80–87.

    Article  CAS  Google Scholar 

  • Trueman, C. L., & Burlakoti, R. R. (2014). Evaluation of products for management of Cercospora leaf spot in sugarbeet, 2014. Plant Dis Manag Rep., 9, FC009.

    Google Scholar 

  • Trueman, C., Hanson, L., Somohano, P., & Rosenzweig, N. (2017). First report of DMI-insensitive Cercospora beticola on sugar beet in Ontario, Canada. New Disease Reports, 36, 20.

    Article  Google Scholar 

  • Verreet, J. A., Wolf, P., & Weis, F. J. (1996). Bekämpfungsschwellen als Grundlage für eine integrierte Bekämpfung von Cercospora beticola–Das IPS-Modell Zuckerrübe. Proceedings of the IIRB, 59, 55–69.

  • Weiland, J., & Koch, G. (2004). Sugarbeet leaf spot disease (Cercospora beticola Sacc.). Molecular Plant Pathology, 5(3), 157–166.

  • Wolf, P. F. J., & Verreet, J. A. (2002). An integrated pest management system in Germany for the control of fungal leaf diseases in sugar beet: The IPM sugar beet model. Plant Disease, 86(4), 336–344.

    Article  CAS  Google Scholar 

  • Wolf, P. F. J., & Verreet, J. A. (2005). Factors affecting the onset of Cercospora leaf spot epidemics in sugar beet and establishment of disease-monitoring thresholds. Phytopathology, 95, 269274.

    Article  Google Scholar 

  • Wong, F. P., & Wilcox, W. F. (2000). Distribution of baseline sensitivities to azoxystrobin among isolates of Plasmopara viticola. Plant Disease, 84, 275–281.

    Article  CAS  Google Scholar 

  • Wong, F. P., & Wilcox, W. F. (2002). Sensitivity to azoxystrobin among isolates of Uncinula necator : Baseline distribution and relationship to myclobutanil sensitivity. Plant Disease, 86, 394–404.

    Article  CAS  Google Scholar 

Download references

Code availability

We have the code for our statistical software.

Author information

Authors and Affiliations

  1. Meknes Faculty of Sciences, Laboratory of Biotechnology and Molecular Biology, Department of Biology, Moulay Ismail University, PO Box 11201, Zitoune, Meknès, Morocco

    Zakariae El Housni & Abderrahman Ouijja

  2. Phytopathology Unit, Department of Plant Protection, Ecole Nationale d’Agriculture de Meknès, BPS 40, Meknès, Morocco

    Zakariae El Housni, Abdessalem Tahiri, Said Ezrari & Nabil Radouane

  3. Laboratory of Functional Ecology and Environment, Sidi Mohamed Ben Abdellah University, PO Box 2202, Route d’Imouzzer, Fez, Morocco

    Said Ezrari & Nabil Radouane

Authors
  1. Zakariae El Housni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abdessalem Tahiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Said Ezrari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nabil Radouane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abderrahman Ouijja
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zakariae El Housni.

Ethics declarations

Financial interests

The authors declare they have no financial interests.

Competing interests

Authors declares that they has no conflict of interest or competing interest.

Ethics approval

Not applicable

Consent to participate

Not applicable.

Consent for publication

Not applicable

Supplementary Information

Table S1

EC50 calculation for 22 isolates of Cercospora beticola in Morocco in response for thiophanate methyl (TM), azoxystrobin (AZ), trifloxystrobin (TR), tetraconazole (TT), epoxiconazole (EP), difenoconazole (DF) for 2017. (DOCX 15 kb)

Table S2

EC50 calculation for 20 isolates of Cercospora beticola in Morocco in response for thiophanate methyl (MT), azoxystrobin (AZ), trifloxystrobin (TR), tetraconazole (TT), epoxiconazole (EP), difenoconazole (DF) for 2018. (DOCX 17 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Housni, Z., Tahiri, A., Ezrari, S. et al. Occurrence of Cercospora beticola Sacc populations resistant to benzimidazole, demethylation-inhibiting, and quinone outside inhibitors fungicides in Morocco. Eur J Plant Pathol 165, 73–83 (2023). https://doi.org/10.1007/s10658-022-02589-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-022-02589-5

Keywords

Search

Navigation