Email this article 
Hide
Show all
Apple Scab in Morocco: Resistance to Chemical Fungicides and Perspectives of Control: A Review
Abstract
Apple scab, caused by the ascomycete fungus Venturia inaequalis (Cooke) G. Winter (1875), is one of the most devastating diseases of apple (Malus × domestica) worldwide, including in Morocco, where apple cultivation plays an important role in the arboriculture sector. This disease can spread widely under favorable environmental conditions and in the absence of effective preventive and curative measures, leading to severe economic losses due to fruit damage, reduced yields, and increased costs associated with fungicide applications. Moreover, the intensive and repeated use of chemical fungicides has contributed to the emergence of V. inaequalis strains that are resistant to several active substances. In Morocco, thirteen active fungicidal compounds are currently used to control this disease. This review presents all the active ingredients authorized for use in Morocco against apple scab and evaluates their efficacy. It also discusses the development of resistance to systemic fungicides by Venturia inaequalis at both the national and global levels and assesses their future prospects. Finally, this article highlights alternative approaches to chemical control, including biological and genetic interventions in the management of apple scab, with an emphasis on the potential of these strategies to guide and support future research efforts.
Keywords
References
Adeli, I., H. MohammadSadeghi and B. Bameri. 2023. Captan, In: Encyclopedia of toxicology, 4th ed. Elsevier. https://doi.org/10.1016/B978-0-12-824315-2.00331-6
Avenot, H. F. and T. J. Michailides. 2010. Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Protection, 29: 643–651. https://doi.org/10.1016/j.cropro.2010.02.019
Ayer, K. M., D. A. Strickland, M. Choi and K. D. Cox. 2021. Optimizing the integration of a biopesticide (Bacillus subtilis QST 713) with a single-site fungicide (benzovindiflupyr) to reduce reliance on synthetic multisite fungicides (captan and mancozeb) for management of apple scab. Plant Disease, 105: 3545–3553. https://doi.org/10.1094/PDIS-02-21-0426-RE
Ayer, K. M., M. W. Choi, S. T. Smart, K. D. Cox and A. E. Moffett. 2020. The effects of succinate dehydrogenase inhibitor fungicide dose and mixture on development of resistance in Venturia inaequalis. Applied and Environmental Microbiology, 86. https://doi.org/10.1128/AEM.01196-20
Bahouq, M., H. Bahouq and A. Soulaymani. 2021. Bibliographic review of phytopharmacovigilance actions and measures on plant protection products in Morocco. E3S Web of Conferences, 319. https://doi.org/10.1051/e3sconf/202131901034
Bartlett, D. W., J. M. Clough, J. R. Godwin, A. A. Hall, M. Hamer and B. Parr-Dobrzanski. 2002. The strobilurin fungicides. Pest Management Science, 58: 649–662. https://doi.org/10.1002/ps.520
Beata, M., A. Broniarek-Niemiec and A. Bielenin. 2008. Resistance of Venturia inaequalis to strobilurin and dodine fungicides in Polish apple orchards. Phytopathologica Polonica, 57–61.
Bhaik, A., M. K. Mboup and J. L. Genet. 2022. Fungicide resistance: threats and management approaches, In: Sustainable management of potato pests and diseases. Springer, Singapore, pp. 59–81. https://doi.org/10.1007/978-981-16-7695-6_3
Bhat, M. A., Z. A. Bhat, G. H. Mir, S. Banday and T. Ahmad. 2021. Kresoxim methyl SC-a quinone outside inhibitor against major fungal foliar diseases of apple. Pesticide Research Journal, 33: 65–74. https://doi.org/10.5958/2249-524X.2021.00040.6
Brent, K. J. and D. W. Hollomon. 2007. Fungicide resistance in crop pathogens: how can it be managed? FRAC Monograph No. 1. Fungicide Resistance Action Committee.
Carbone, M. J., S. Alaniz, O. Bentancur and P. Mondino. 2021. Sensitivity of Venturia inaequalis to dodine in Uruguay. Tropical Plant Pathology, 46: 643–650. https://doi.org/10.1007/s40858-021-00467-9
Carmona, M., M. R. E. and S. Francisco. 2018. Fungal resistance to fungicides in field crops: a growing problem worldwide, In: Fungicides: perspectives, resistance management and risk assessment, pp. 149–192.
Chapman, K. S., G. W. Sundin and J. L. Beckerman. 2011. Identification of resistance to multiple fungicides in field populations of Venturia inaequalis. Plant Disease, 95: 921–926. https://doi.org/10.1094/PDIS-12-10-0899
Chatzidimopoulos, M., F. Lioliopoulou, E. Vellios and A. Zambounis. 2022. Detection of Venturia inaequalis isolates with multiple resistance in Greece. Microorganisms, 10. https://doi.org/10.3390/microorganisms10122354
Chatzidimopoulos, M., F. Lioliopoulou, T. Sotiropoulos and E. Vellios. 2020. Efficient control of apple scab with targeted spray applications. Agronomy, 10. https://doi.org/10.3390/agronomy10020217
De Artur Teixeira, A., P. Longhi, P. Ritschel, R. Gava, R. M. V. Sanhueza and K. Cox. 2015. Use of RFLP-PCR method to detect kresoxim methyl-resistant Venturia inaequalis isolates from the south of Brazil. Summa Phytopathologica, 41: 224–226. https://doi.org/10.1590/0100-5405/2085
Fontaine, S., F. Remuson, L. Fraissinet-Tachet, A. Micoud, R. Marmeisse and D. Melayah. 2009. Monitoring of Venturia inaequalis harbouring the QoI resistance G143A mutation in French orchards as revealed by PCR assays. Pest Management Science, 65: 74–81. https://doi.org/10.1002/ps.1649
FRAC. 2022. Group U12 (guanidines) dodine recommendations. Fungicide Resistance Action Committee. https://www.frac.info/media/525fag4z/group-u12-guanidines-dodine-recommendations-20th-october-2022.pdf
FRAC. 2025. FRAC code list 2025: fungal control agents sorted by cross-resistance pattern and mode of action (including coding for FRAC groups on product labels). Fungicide Resistance Action Committee. https://www.frac.info/media/ljsi3qrv/frac-code-list2025.pdf
Frederick, Z. A., S. M. Villani and K. D. Cox. 2015. The effect of delayed-dormant chemical treatments on demethylation inhibitor (DMI) sensitivity in a DMI-resistant population of Venturia inaequalis. Plant Disease, 99: 1751–1756. https://doi.org/10.1094/PDIS-12-14-1253-RE
Frederick, Z. A., S. M. Villani, D. R. Cooley, A. R. Biggs, J. J. Raes and K. D. Cox. 2014. Prevalence and stability of qualitative QoI resistance in populations of Venturia inaequalis in the northeastern United States. Plant Disease, 98: 1122–1130. https://doi.org/10.1094/PDIS-10-13-1042-RE
Gisi, U., U. Müller and S. Hall. 2019. Fungicides acting on amino acids and protein synthesis, In: Modern crop protection compounds. Wiley, pp. (chapter reference). https://doi.org/10.1002/9783527699261.ch16
Gouit, S., I. Chair, Z. Belabess, I. Legrifi, K. Goura, A. Tahiri, A. Lazraq and R. Lahlali. 2024. Harnessing Trichoderma spp.: a promising approach to control apple scab disease. Pathogens, 13. https://doi.org/10.3390/pathogens13090752
Gouit, S., M. Radi, I. Chair, Z. Belabess, A. Farhaoui, A. Tahiri, A. Lazraq and R. Lahlali. 2025. Potential of bacterial isolates for the biological control of apple scab (Venturia inaequalis). Journal of Natural Pesticide Research, 14: 100165. https://doi.org/10.1016/j.napere.2025.100165
Gouit, S., S. Chiadmi, K. Goura, I. Legrifi, M. El Jarroudi, Z. Belabess, A. Tahiri, A. Lazraq, M. Baala and R. Lahlali. 2025. Assessing Venturia inaequalis response to common fungicides in Morocco. Journal of Fungi, 11: 493. https://doi.org/10.3390/jof11070493
Guérin, F. and B. Le Cam. 2004. Breakdown of the scab resistance gene Vf in apple leads to a founder effect in populations of the fungal pathogen Venturia inaequalis. Phytopathology, 94: 364–369. https://doi.org/10.1094/PHYTO.2004.94.4.364
Hassold, E. and T. Backhaus. 2009. Chronic toxicity of five structurally diverse demethylase-inhibiting fungicides to the crustacean Daphnia magna: a comparative assessment. Environmental Toxicology and Chemistry, 28: 1218–1226. https://doi.org/10.1897/08-339.1
Hauke, K., P. Creemers, W. Brugmans and S. Van Laer. 2004. Signum, a new fungicide with interesting properties in resistance management of fungal diseases in strawberries. Communications in Agricultural and Applied Biological Sciences, 69: 743–755.
Herce, H. D., A. E. Garcia and M. C. Cardoso. 2014. Fundamental molecular mechanism for the cellular uptake of guanidinium-rich molecules. Journal of the American Chemical Society, 136: 17459–17467. https://doi.org/10.1021/ja507790z
Hermann, D. and K. Stenzel. 2019. FRAC mode-of-action classification and resistance risk of fungicides, In: Modern crop protection compounds. Wiley, pp. (chapter reference). https://doi.org/10.1002/9783527699261.ch14
Hirayama, K. 2022. Curative effects of fungicides against Venturia inaequalis causing apple scab. Journal of General Plant Pathology, 88: 264–269. https://doi.org/10.1007/s10327-022-01071-8
Hoffmeister, M., P. Scheu, A. Glaab, R. Zito and G. Stammler. 2024. Sensitivity evolution in Venturia inaequalis towards SDHIs in comparison to other modes of action. European Journal of Plant Pathology, 168: 763–773. https://doi.org/10.1007/s10658-023-02798-6
Hoffmeister, M., R. Zito, J. Böhm and G. Stammler. 2021. Mutations in Cyp51 of Venturia inaequalis and their effects on DMI sensitivity. Journal of Plant Diseases and Protection, 128: 1467–1478. https://doi.org/10.1007/s41348-021-00516-0
Jha, G., K. Thakur and P. Thakur. 2009. The Venturia apple pathosystem: pathogenicity mechanisms and plant defense responses. Journal of Biomedicine and Biotechnology, 2009. https://doi.org/10.1155/2009/680160
Jobin, T. and O. Carisse. 2007. Incidence of myclobutanil- and kresoxim-methyl-insensitive isolates of Venturia inaequalis in Quebec orchards. Plant Disease, 91: 1351–1358. https://doi.org/10.1094/PDIS-91-10-1351
Jørgensen, L. N., F. van den Bosch, R. P. Oliver, T. M. Heick and N. D. Paveley. 2017. Targeting fungicide inputs according to need. Annual Review of Phytopathology, 55: 181–203. https://doi.org/10.1146/annurev-phyto-080516-035357
Karkach, I., N. Eloutassi, H. El Yacoubi and A. Rochdi. 2025. Perceptions and practices of peach producers in Fez-Meknes region and evaluation of environmental impacts using an environmental indicator of pesticide pressure. Environment, Development and Sustainability. https://doi.org/10.1007/s10668-025-06065-y
Kolattukudy, P. E. 1985. Enzymatic penetration of the plant cuticle by fungal pathogens. Annual Review of Phytopathology, 23: 223–250. https://doi.org/10.1146/annurev.py.23.090185.001255
Köller, W. 1991. Role of cutinase in the penetration of apple leaves by Venturia inaequalis. Phytopathology, 81: 1375. https://doi.org/10.1094/Phyto-81-1375
Köller, W. and W. F. Wilcox. 2001. Evidence for the predisposition of fungicide-resistant isolates of Venturia inaequalis to a preferential selection for resistance to other fungicides. Phytopathology, 91: 776–781. https://doi.org/10.1094/PHYTO.2001.91.8.776
Köller, W., D. Parker, W. Turechek, D. Rosenberger, W. Wilcox, J. Carroll, A. Agnello and H. Reissig. 2005. Fungicide resistance of apple scab: status quo and management options. New York Fruit Quarterly, 13: 9–17.
Köller, W., W. F. Wilcox and A. L. Jones. 1999. Quantification, persistence and status of dodine resistance in New York and Michigan orchard populations of Venturia inaequalis. Plant Disease, 83: 66–70. https://doi.org/10.1094/PDIS.1999.83.1.66
Köller, W., W. F. Wilcox and D. M. Parker. 2005. Sensitivity of Venturia inaequalis populations to anilinopyrimidine fungicides and their contribution to scab management in New York. Plant Disease, 89: 357–365. https://doi.org/10.1094/PD-89-0357
Kucheryava, N., J. K. Bowen, P. W. Sutherland, J. J. Conolly, C. H. Mesarich, E. H. A. Rikkerink, E. Kemen, M. Plummer, K. M. Hahn and M. D. Templeton. 2008. Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane. Fungal Genetics and Biology, 45: 1329–1339. https://doi.org/10.1016/j.fgb.2008.07.010
Lahlali, R., A. Moinina, S. Ezrari, D. Maclean and M. Boulif. 2019. Apple scab disease severity in the Sais region of Morocco and its sensitivity to three commercial fungicides. Notulae Scientia Biologicae, 11: 249–257. https://doi.org/10.15835/nsb11210434
Lahlali, R., M. Boulif and A. Moinina. 2021. Pratiques phytosanitaires des pomiculteurs: cas de la région Fès-Meknès. Revue Marocaine des Sciences Agronomiques et Vétérinaires, 9: 151–157.
Leroux, P. and A. S. Walker. 2011. Multiple mechanisms account for resistance to sterol 14α-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Management Science, 67: 44–59. https://doi.org/10.1002/ps.2028
Leroux, P., R. Fritz, D. Debieu, C. Albertini, C. Lanen, J. Bach, M. Gredt and F. Chapeland. 2002. Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Management Science, 58: 876–888. https://doi.org/10.1002/ps.566
Lesniak, K. E., T. J. Proffer, J. L. Beckerman and G. W. Sundin. 2011. Occurrence of QoI resistance and detection of the G143A mutation in Michigan populations of Venturia inaequalis. Plant Disease, 95: 927–934. https://doi.org/10.1094/PDIS-12-10-0898
Li, X., H. Li, Z. Yu, L. Gao and J. Yang. 2021. Investigating the sensitivity of Venturia inaequalis isolates to difenoconazole and pyraclostrobin in apple orchards in China. European Journal of Plant Pathology, 161: 207–217. https://doi.org/10.1007/s10658-021-02316-6
Masny, S. 2017. Occurrence of Venturia inaequalis races in Poland able to overcome specific apple scab resistance genes. European Journal of Plant Pathology, 147: 313–323. https://doi.org/10.1007/s10658-016-1003-x
Megadi, V. B., P. N. Tallur, S. I. Mulla and H. Z. Ninnekar. 2010. Bacterial degradation of fungicide captan. Journal of Agricultural and Food Chemistry, 58: 12863–12868. https://doi.org/10.1021/jf1030339
Moinina, A., R. Lahlali, D. Maclean and M. Boulif. 2018. Farmers’ knowledge, perception and practices in apple pest management and climate change in the Fès-Meknès region, Morocco. Horticulturae, 4. https://doi.org/10.3390/horticulturae4040042
Morais, C. 2014. Advances in drug resistance research, In: Advances in drug resistance research.
Nabi, A., M. Ahmad, M. D. Shah, B. A. Padder, M. S. Dar and S. Banday. 2023. First report of myclobutanil resistance and shift in sensitivity to difenoconazole and flusilazole in north-western Himalayan Venturia inaequalis populations. Australasian Plant Pathology, 52: 13–22. https://doi.org/10.1007/s13313-022-00894-5
Nasonov, A. I., G. V. Yakuba and E. V. Lobodina. 2022. The long-term resistance to carbendazim in Venturia inaequalis in the Krasnodar region (Russia). Mikologiya i Fitopatologiya, 56: 374–378. https://doi.org/10.31857/S0026364822050087
Nasonov, A. I., G. V. Yakuba, I. L. Astapchuk and N. A. Marchenko. 2024. Sensitivity baseline and orchard populations of Venturia inaequalis to the succinate dehydrogenase inhibitor fungicides (SDHI). Siberian Journal of Life Sciences and Agriculture, 16: 189–210. https://doi.org/10.12731/2658-6649-2024-16-1-707
Nasonov, A., G. Yakuba, N. Marchenko, E. Lobodina and I. Astapchuk. 2022. Evaluation of sensitivity of apple scab pathogen to difenoconazole using the discriminatory dose technique. BIO Web of Conferences, 47. https://doi.org/10.1051/bioconf/20224710002
ONSSA. 2025. Office national de sécurité sanitaire des produits alimentaires. https://eservice.onssa.gov.ma/IndPesticide.aspx
Özkılınç, H., B. T. Fidanoğlu, S. Öncel, E. Kurtuluş and İ. E. Kadıoğlu. 2025. Resistance evolution and local adaptation of Venturia inaequalis to old and new generation SDHI fungicides. Fungal Biology, 129: 101543. https://doi.org/10.1016/j.funbio.2025.101543
Padder, B. A., T. A. Sofi, M. Ahmad, M. U. D. Shah, A. Hamid, S. Saleem and F. A. Ahanger. 2013. Virulence and molecular diversity of Venturia inaequalis in commercial apple growing regions in Kashmir. Journal of Phytopathology, 161: 271–279. https://doi.org/10.1111/jph.12061
Padder, S. A., S. Mansoor, S. A. Bhat, T. R. Baba, R. A. Rather, S. M. Wani, S. M. Popescu, S. Sofi, M. A. Aziz, D. I. Hefft, O. M. Alzahrani, A. Noureldeen and H. Darwish. 2021. Bacterial endophyte community dynamics in apple (Malus domestica Borkh.) germplasm and their evaluation for scab management strategies. Journal of Fungi, 7: 923. https://doi.org/10.3390/jof7110923
Percival, G. C. and S. Graham. 2021. Evaluation of inducing agents and synthetic fungicide combinations for management of foliar pathogens of urban trees. Arboriculture and Urban Forestry, 47: 85–95. https://doi.org/10.48044/jauf.2021.008
Pikunova, A. V. and E. N. Sedov. 2019. The racial composition of Venturia inaequalis in environments of the Oryol region. Mikologiya i Fitopatologiya, 53: 293–300. https://doi.org/10.1134/S0026364819050040
Polat, Z. and H. Bayraktar. 2021. Resistance of Venturia inaequalis to multiple fungicides in Turkish apple orchards. Journal of Phytopathology, 169: 360–368. https://doi.org/10.1111/jph.12990
Quello, K. L., K. S. Chapman and J. L. Beckerman. 2010. In situ detection of benzimidazole resistance in field isolates of Venturia inaequalis in Indiana. Plant Disease, 94: 744–750. https://doi.org/10.1094/PDIS-94-6-0744
Rekanović, E., M. Stepanović, I. Potočnik, S. Milijašević-Marčić, B. Todorović and M. Stević. 2012. Some experiences in control of apple scab in Serbia. Acta Horticulturae.
Rocafort, M., V. Srivastava, J. K. Bowen, S. M. Díaz-Moreno, Y. Guo, V. Bulone, K. M. Plummer, P. W. Sutherland, M. A. Anderson, R. E. Bradshaw and C. H. Mesarich. 2023. Cell wall carbohydrate dynamics during the differentiation of infection structures by the apple scab fungus Venturia inaequalis. Microbiology Spectrum, 11. https://doi.org/10.1128/spectrum.04219-22
Schumacher, C. F. A., U. Steiner, H. W. Dehne and E. C. Oerke. 2008. Localized adhesion of nongerminated Venturia inaequalis conidia to leaves and artificial surfaces. Phytopathology, 98: 760–768. https://doi.org/10.1094/PHYTO-98-7-0760
Shaik, S., J. H. Lee, Y. G. Kim and J. Lee. 2024. Antifungal, anti-biofilm and anti-hyphal properties of N-substituted phthalimide derivatives against Candida species. Frontiers in Cellular and Infection Microbiology, 14. https://doi.org/10.3389/fcimb.2024.1414618
Sokolova, O. and I. Moročko-Bičevska. 2022. Evaluation of apple scab and occurrence of Venturia inaequalis races on differential Malus genotypes in Latvia. Proceedings of the Latvian Academy of Sciences, Section B: Natural, Exact and Applied Sciences, 76: 488–494. https://doi.org/10.2478/prolas-2022-0075
Song, X. 2014. Captan, In: Encyclopedia of toxicology, 3rd ed. Elsevier. https://doi.org/10.1016/B978-0-12-386454-3.00105-6
Steiner, U. and E. C. Oerke. 2023. A melanin-deficient isolate of Venturia inaequalis reveals various roles of melanin in pathogen life cycle and fitness. Journal of Fungi, 9. https://doi.org/10.3390/jof9010035
Stewart, K., T. Passey, C. Verheecke-Vaessen, Z. Kevei and X. Xu. 2023. Is it feasible to use mixed orchards to manage apple scab? Fruit Research, 3. https://doi.org/10.48130/FruRes-2023-0028
Torriani, S. F. F., P. C. Brunner, B. A. McDonald and H. Sierotzki. 2009. QoI resistance emerged independently at least four times in European populations of Mycosphaerella graminicola. Pest Management Science, 65: 155–162. https://doi.org/10.1002/ps.1662
Viljanen-Rollinson, S. L. H., S. M. Thompson, S. Keenan, S. R. Bulman, P. J. Wright, P. N. Wood, N. M. Park and R. M. Beresford. 2013. Resistance of Venturia inaequalis to quinone outside inhibitor (QoI) fungicides in New Zealand apple orchards. New Zealand Plant Protection, 66: 284–292. https://doi.org/10.30843/nzpp.2013.66.5659
Villani, S. M. and K. D. Cox. 2014. Heteroplasmy of the cytochrome b gene in Venturia inaequalis and its involvement in quantitative and practical resistance to trifloxystrobin. Phytopathology, 104: 945–953. https://doi.org/10.1094/PHYTO-06-13-0158-R
Villani, S. M., A. R. Biggs, D. R. Cooley, J. J. Raes and K. D. Cox. 2015. Prevalence of myclobutanil resistance and difenoconazole insensitivity in populations of Venturia inaequalis. Plant Disease, 99: 1526–1536. https://doi.org/10.1094/PDIS-01-15-0002-RE
Weber, R. W. S., R. Busch and J. Wesche. 2025. Spatial and temporal aspects of fungicide resistance in Venturia inaequalis (apple scab) populations in northern Germany. BioTech, 14: 44. https://doi.org/10.3390/biotech14020044
Xu, X., J. Yang, V. Thakur, A. Roberts and D. J. Barbara. 2008. Population variation of apple scab (Venturia inaequalis) isolates from Asia and Europe. Plant Disease, 92: 247–252. https://doi.org/10.1094/PDIS-92-2-0247
DOI: 10.33687/phytopath.014.03.5787
Refbacks
- There are currently no refbacks.
Copyright (c) 2026 HICHAM ZITOUN, Adil Laaziz, Rajae Belkhou, Abdelouahed Hajjaji
This work is licensed under a Creative Commons Attribution 4.0 International License.
