Progress in Plant Protection

Strategie zarządzania odpornością grzybów na substancje czynne fungicydów
Strategies of management resistance fungus to active substances of fungicides

Agnieszka Kiniec, e-mail: a.kiniec@iorpib.poznan.pl

Instytut Ochrony Roślin – Państwowy Instytut Badawczy, Terenowa Stacja Doświadczalna w Toruniu, Pigwowa 16, 87-100 Toruń, Polska
Abstract

Wzrost odporności patogenów na substancje czynne stosowanych fungicydów stanowi poważne wyzwanie dla współczesnej ochrony roślin. Na ogół populacje składają się z osobników o zróżnicowanych poziomach wrażliwości na fungicydy. Intensywne wykorzystywanie preparatów grzybobójczych i wynikająca z tego presja selekcyjna powodują dynamiczny rozwój odporności grzybów na substancje czynne o różnych mechanizmach działania. Strategie zarządzania odpornością opierają się na stosowaniu mieszanin, naprzemiennym aplikowa­niu substancji czynnych oraz używaniu fungicydów w możliwie niskich, ale skutecznych dawkach.

 

The increase in pathogen resistance to the active substances of fungicides used is a serious challenge for modern plant protection. Ingeneral, populations consist of individuals with different levels of sensitivity to fungicides. The intensive use of fungicides and the result­ing selection pressure cause the dynamic development of fungal resistance to active substances with different modes of action. Resis­tance management strategies are based on the use of mixtures, alternating the use of active substances, and the use of fungicides in the lowest possible but effective doses.

Key words
odporność grzybów; rodzaje odporności; strategie zarządzania odpornością; fungicydy; fungus resistance; types of resistance; fungicide resistance management; fungicides
References

Albertini C., Gredt M., Leroux P. 1999. Mutations of the β-tubulin gene associated with different phenotypes of benzimidazole resistance in the cereal eyespot fungi Tapesia yallundae and Tapesia acuformis. Pesticide Biochemistry and Physiology 64 (1): 17–31. DOI: 10.1006/pest.1999.2406

 

Arzanlou M., Mousavi S., Bakhshi M., Khakvar R., Bandehagh A. 2016. Inhibitory effects of antagonistic bacteria inhabiting the rhizosphere of the sugarbeet plants, on Cercospora beticola Sacc., the causal agent of Cercospora leaf spot disease on sugar­beet. Journal of Plant Protection Research 56 (1): 6–14. DOI: 10.1515/jppr-2016-0002

 

Avenot H.F., Solorio C., Morgan D.P., Michailides T.J. 2016. Sensitivity and cross-resistance patterns to demethylation- -inhibiting fungicides in California populations of Alternaria alternata pathogenic on pistachio. Crop Protection 88: 72–78. DOI: 10.1016/j.cropro.2016.05.012

 

Bolton M.D., Birla K., Rivera-Varas V., Rudolph K., Secor G.A. 2012. Characterization of CbCyp51 from field isolates of Cerco­spora beticola. Phytopathology 102 (3): 298–305. DOI: 10.1094/PHYTO-07-11-0212

 

Bolton M.D., Riviera V., Secor G.A. 2013. Identification of the G143A mutation associated with QoI resistance in Cercospora beticola field isolates from Michigan. Pest Management Science 69 (1): 35–39. DOI: 10.1002/ps.3358

 

Brent K.J., Hollmon D.W. 2007. Fungicide Resistance: The Assessment of Risk. FRAC Monograph No. 2, Edition 2nd. Croplife International, Brussels, Belgium, 53 ss.

 

Cioni F., Maines G., Kempl F. 2014. Sensitivity and resistance of Cercospora beticola to different fungicides, new strategies in CLS control in Italy and Austria. Proceedings of 74th International Institute of Sugar Beet Research Congress, Dresden, 01–03.07.2014: 12–23.

 

Çolak Tümbek A., Özeren P., Kaya R., Katircioğlu Y.Z., Maden S. 2011. Sensitivity of Cercospora beticola populations in Tur­key to flutriafol, mancozeb, and fentin acetate. Turkish Journal of Agriculture and Forestry 35 (1): 65–71. DOI: 10.3906/tar- 0910-24

 

Corkley I., Fraaije B., Hawkins N. 2022. Fungicide resistance management: maximizing the effective life of plant protection prod­ucts. Plant Pathology 71 (1): 150–169. DOI: 10.1111/ppa.13467

 

Davidson R.M., Hanson L.E., Franc G.D., Panella L. 2006. Analysis of β-tubulin gene fragments from benzimidazole-sensitive and -tolerant Cercospora beticola. Journal of Phytopathology 154 (6): 321–328. DOI: 10.1111/j.1439 0434.2006.01080.x

 

de Miccolis Angelini R.M., Pollastro S., Faretra F. 2015. Genetics of fungicide resistance. s. 13–34. W: Fungicide Resistance in Plant Pathogens. Principles and a Guide to Practical Management (H. Ishii, D.W. Hollomon, red.). Springer, Tokyo, Japan. DOI: 10.1007/978-4-431-55642-8_2

 

Deising H.B., Reimann S., Pascholati S.F. 2008. Mechanisms and significance of fungicide resistance. Brazilian Journal of Micro­biology 39 (2): 286–295. DOI: 10.1590/S1517-838220080002000017

 

Dooley H., Shaw M.W., Spink J., Kildea S. 2016. The effect of succinate dehydrogenase inhibitor/azole mixtures on selection of Zymoseptoria tritici isolates with reduced sensitivity. Pest Management Science 72 (6): 1150–1159. DOI: 10.1002/ps.4093

 

Elderfield J.A.D., Lopez-Ruiz F.J., van den Bosch F., Cunniffe N.J. 2018. Using epidemiological principles to explain fungicide resistance management tactics: why do mixtures outperform alternations? Phytopathology 108 (7): 803–817. DOI: 10.1094/ PHYTO-08-17-0277-R

 

EPPO 2015. PP 1/213 (4) Resistance risk analysis. Bulletin OEPP/EPPO 45 (3): 371–387. DOI: 10.1111/epp.12246

 

Fernandez-Ortuno D., Tores J.A., de Vicente A., Perez-Garcia A. 2008. Mechanism of resistance to QoI fungicides in phytopatho­genic fungi. International Microbiology 11 (1): 1–9. DOI: 10.2436/20.1501.01.38

 

Fourie P.H., Holz G. 2001. Incomplete cross-resistance to folpet and iprodione in Botrytis cinerea from grapevine in South Africa. South African Journal of Enology and Viticulture 22 (1): 3–7. DOI: 10.21548/22-1-2158

 

FRAC Code List 2024. Fungal control agents sorted by cross resistance pattern and mode of action (including coding for FRAC Groups on product labels). Fungicide Resistance Action Committee.

 

Georgopoulos S.G., Dovas C. 1973. Occurrence of Cercospora beticola strains resistant to benzimidazole fungicides in Northern Greece. The Plant Disease Reporter 57 (4): 321–324.

 

Gleason J., Peng J., Proffer T.J., Slack S.M., Outwater C.A., Rothwell N.L., Sundin G.W. 2021. Resistance to boscalid, fluopyram and fluxapyroxad in Blumeriella jaapii from Michigan (U.S.A.): molecular characterization and assessment of practical resis­tance in commercial cherry orchards. Microorganisms 9 (11): 2198. DOI: 10.3390/microorganisms9112198

 

Heick T.M., Justesen A.F., Jørgensen L.N. 2017. Anti-resistance strategies for fungicides against wheat pathogen Zymoseptoria tritici with focus on DMI fungicides. Crop Protection 99: 108–117. DOI: 10.1016/j.cropro.2017.05.009

 

Hobbelen P.H.F., Paveley N.D., Oliver R.P., van den Bosch F. 2013. The usefulness of fungicide mixtures and alternation for delay­ing the selection for resistance in populations of Mycosphaerella graminicola on winter wheat: a modeling analysis. Phytopa­thology 103 (7): 690–707. DOI: 10.1094/PHYTO-06-12-0142-R

 

Hobbelen P.H.F., Paveley N.D., van den Bosch F. 2014. The emergence of resistance to fungicides. PLoS ONE 9 (3): e91910. DOI: 10.1371/journal.pone.0091910

 

Hollomon D.W. 2015. Fungicide resistance: 40 years on and still a major problem. s. 3–12. W: Fungicide Resistance in Plant Pathogens. Principles and a Guide to Practical Management (H. Ishii, D.W. Hollomon, red.). Springer, Tokyo, Japan. DOI: 10.1007/978-4-431-55642-8_1

 

Hsiang T., Yang L., Barton W. 1997. Baseline sensitivity and cross-resistance to demethylation-inhibiting fungicides in Ontario isolates of Sclerotinia homoeocarpa. European Journal of Plant Pathology 103 (5): 409–416. DOI: 10.1023/a:1008671321231

 

Ishii H., Bryson P.K., Kayamori M., Miyamoto T., Yamaoka Y., Schnabel G. 2021. Cross-resistance to the new fungicide mefen­trifluconazole in DMI-resistant fungal pathogens. Pesticide Biochemistry and Physiology 171 (7): 1–9. DOI: 10.1016/j.pest­bp.2020.104737

 

Jørgensen L.N., Matzen N., Semaskiene R., Korbas M., Danielewicz J., Glazek M., Maumene C., Rodemann B., Weigand S., Hess M., Blake J., Clark B., Kildea S., Bataille C., Ban R. 2017a. Azoles have different trengths and perform diversely across Europe. s. 129–134. W: Modern Fungicides and Antifungal Compounds Vol. VIII (H.B. Deising, B. Fraaije, A. Mehl, E.C. Oerke, red.). Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany. ISBN 978-3-941261-15-0.

 

Jørgensen L.N., van den Bosch F., Oliver R.P., Heick T.M., Paveley N.D. 2017b. Targeting fungicide inputs according to need. Annual Review of Phytopathology 55: 181–203. DOI: 10.1146/annurev-phyto-080516-035357

 

Karaoglanidis G.S., Ioannidis P.M. 2010. Fungicide resistance of Cercospora beticola in Europe. s. 189–211. W: Cercospora Leaf Spot of Sugar Beet and Related Species (R.T. Lartey, J.J. Weiland, L. Panella, P.W. Crous, C.E. Windels, red.). The American Phytopathological Society Press, St. Paul, USA.

 

Karaoglanidis G.S., Ioannidis P.M., Thanassoulopoulos C.C. 2000. Reduced sensitivity of Cercospora beticola isolates to sterol-demethylation-inhibiting fungicides. Plant Pathology 49 (5): 567–572. DOI: 10.1046/j.1365-3059.2000.00488.x

 

Karaoglanidis G.S., Markoglou A.N., Bardas G.A., Doukas E.G., Konstantinou S., Kalampokis J.F. 2011. Sensitivity of Penicil­lium expansum field isolates to tebuconazole, iprodione, fludioxoniland cyprodinil and characterization of fitness parameters and patulin production. International Journal of Food Microbiology 145 (1): 195–204. DOI: 10.1016/j.ijfoodmicro.2010.12.017

 

Karaoglanidis G.S., Thanassoulopoulos C.C. 2003. Cross-resistance patterns among sterol biosynthesis inhibiting fungicides (SBIs) in Cercospora beticola. European Journal of Plant Pathology 109 (9): 929–934. DOI: 10.1023/B:EJPP.0000003672.36076.8a

 

Karaoglanidis G.S., Thanassoulopoulos C.C., Ioannidis P.M. 2001. Fitness of Cercospora beticola field isolates resistant and sensitive to demethylation inhibitor fungicides. European Journal of Plant Pathology 107 (3): 337–347. DOI: 10.1023/A:1011219514343

 

Khan J., del Rio L.E., Nelson R., Rivera-Varas V., Secor G.A. 2008. Survival, dispersal, and primary infection site for Cercospora beticola in sugar beet. Plant Disease 92 (5): 741–745. DOI: 10.1094/PDIS-92-5-0741

 

Kiniec A., Piszczek J. 2023. Występowanie izolatów odpornych grzyba Cercospora beticola na mefentriflukonazol – nowo wprowadzoną substancję czynną. [Occurrence of resistant isolates of the fungus Cercospora beticola to mefentrifluconazole, a newly introduced active substance]. Konferencja Ochrony Roślin 63. Sesja Naukowa IOR – PIB, Streszczenia, s. 134.

 

Kiniec A., Piszczek J., Miziniak W., Sitarski A. 2020. Impact of the variety and severity of Cercospora beticola infection on the qualitative and quantitative parameters of sugar beet yields. Polish Journal of Agronomy 41 (41): 29–37. DOI: 10.26114/pja. iung.410.2020.41.04

 

Kukawka R., Spychalski M., Grzempa B., Smiglak M., Górski D., Gaj R., Kiniec A. 2024. The use of a new ionic derivative of salicylic acid in ugar beet cultivation. Agronomy 14 (4): 827. DOI: 10.3390/agronomy14040827

 

Leroux P., Chapeland F., Arnold A., Gredt M. 2000. New cases of negative cross resistance between fungicides, including sterol biosynthesis inhibitors. Journal of General Plant Pathology 66 (1): 75–81. DOI: 10.1007/PL00012925

 

Ma Z., Yoshimura M., Michailides T.J. 2003. Identification and characterization of benzimidazole resistance in Monilinia fruc­ticola from stone fruit orchards in California. Applied and Environmental Microbiology 69 (12): 7145–7152. DOI: 10.1128/ AEM.69.12.71457152.2003

 

Malandrakis A.A., Apostolidou Z.A., Markoglou A., Flouri F. 2015. Fitness and cross-resistance of Alternaria alternata field iso­lates with specific or multiple resistance to single site inhibitors and mancozeb. European Journal of Plant Pathology 142 (3): 489–499. DOI: 10.1007/s10658-015-0628-5

 

Markoglou A.N., Doukas E.G., Malandrakis A.A. 2011. Effect of anilinopyrimidine resistance on aflatoxin production and fitness parameters in Aspergillus parasiticus Speare. International Journal of Food Microbiology 146 (2): 130–136. DOI: 10.1016/j. ijfoodmicro.2011.02.009

 

Moretti M., Arnold A., D’Agostina A., Farina G., Gozzo F. 2003. Characterization of field-isolates and derived DMI-resistant strains of Cercospora beticola. Mycological Research 107 (10): 1178–1188. DOI: 10.1017/S0953756203008396

 

Mostafanezhad H., Edin E., Grenville‑Briggs L.J., Lankinen A., Liljeroth E. 2022. Rapid emergence of boscalid resistance in Swedish populations of Alternaria solani revealed by a combination of field and laboratory experiments. European Journal of Plant Pathology 162 (2): 289–303. DOI: 10.1007/s10658-021-02403-8

 

Müllender M.M., Mahlein A.K., Stammler G., Varrelmann M. 2021. 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. DOI: 10.1002/ps.6197

 

Nikou D., Malandrakis M., Konstantakaki M., Vontas J., Markoglou A., Ziogas B. 2009. Molecular characterization and detection of overexpressed C-14 alpha demethylase-based DMI resistance in Cercospora beticola field isolates. Pesticide Biochemistry and Physiology 95 (1): 18–27. DOI: 10.1016/j.pestbp.2009.04.014

 

Oxley S.J.P., Burnett F., Hunter E.A., Fraaije B.A., Cooke L.R., Mercer P.C., Gilchrist A. 2008. Understanding fungicide mixtures to control Rhynchosporium in barley and minimise resistance shifts. Project Report HGCA No. 436.

 

Pavely N., Fraaije B., van den Bosch F., Kildea S., Burnett F., Clark W., Gosling P., Boor T., Corkley I., Young C. 2020. Managing resistance evolving concurrently against two modes of action. s. 141–146. W: Modern Fungicides and Antifungal Compounds Vol. IX (H.B. Deising, B. Fraaije, A. Mehl, E.C. Oerke, H. Sierotzki, G. Stammler, red.). Deutsche Phytomedizinische Gesell­schaft, Braunschweig, Germany. ISBN 978-3-941261-16-7.

 

Peever T.L., Milgroom M.G. 1993. Genetic correlations in resistance to sterol biosynthesis-inhibiting fungicides in Pyrenophora teres. Phytopathology 83 (10): 1076–1082. DOI: 10.1094/phyto-83-1076

 

Pieczul K. 2015. Przyczyny odporności na fungicydy grzybów patogenicznych dla roślin. Zagadnienia Doradztwa Rolniczego 1 (79): 83–93.

 

Pieczul K., Łacka A. 2016. Analiza odporności krzyżowej Cercospora beticola na fungicydy triazolowe (DMI). Progress in Plant Protection 56 (1): 79–84. DOI: 10.14199/ppp-2016-014

 

Piñeros-Guerrero N., Neves D.L., Bradley C.A., Telenko D.E.P. 2023. Determining the distribution of QoI fungicide-resistant Cer­cospora sojina on soybean from Indiana. Plant Disease 107 (4): 1012–1021. DOI: 10.1094/PDIS-08-22-1744-SR

 

Piszczek J., Czekalska A. 2006. Oporność chwościka buraka – grzyba Cercospora beticola Sacc. na fungicydy stosowane do jego zwalczania w Polsce. Progress in Plant Protection 46 (1): 375–379.

 

Piszczek J., Strażyński P., Mrówczyński M. (red.). 2018. Metodyka integrowanej ochrony buraka cukrowego i pastewnego dla doradców. Instytut Ochrony Roślin – Państwowy Instytut Badawczy, Poznań, 123 ss.

 

Rachitha P., Krupashree K., Jayashree G.V., Gopalan N., Khanum F. 2017. Growth inhibition and morphological alteration of Fusar­ium sporotrichioides by Mentha piperita essential oil. Pharmacognosy Research 9 (1): 74–79. DOI: 10.4103/0974-8490.199771

 

Raveau R., Fontaine J., Sahraoui A.L.-H. 2020. Essential oils as potential alternative biocontrol products against plant pathogens and weeds: a review. Foods 9 (3): 365. DOI: 10.3390/foods9030365

 

Secor G.A., Rivera V.V., Bolton M.D. 2020. Sensitivity of Cercospora beticola to foliar fungicides in 2019. s. 170–177. W: Sugar­beet Research and Extension Reports. North Dakota State University, Fargo, USA.

 

Steinberg G. 2015. Cell biology of Zymoseptoria tritici: Pathogen cell organization and wheat infection. Fungal Genetics and Biology 79: 17–23. DOI: 10.1016/j.fgb.2015.04.002

 

Taylor N.P., Cunniffe N.J. 2023. Modelling quantitative fungicide resistance and breakdown of resistant cultivars: designing in­tegrated disease management strategies for Septoria of winter wheat. PLoS Computational Biology 19 (3): e1010969. DOI: 10.1371/journal.pcbi.1010969

 

Thomas A., Langston D.B., Stevenson K.L. 2012. Baseline sensitivity and cross resistance to succinate-dehydrogenase-inhibiting and demethylation-inhibiting fungicides in Didymella bryoniae. Plant Disease 96 (7): 979–984. DOI: 10.1094/PDIS-09-11- 0744-RE

 

Trkulja N., Ivanović Ž., Pfaf-Dolovac E., Dolovac N., Mitrović M., Toševski I., Jović J. 2013. Characterisation of benzimidazole resistance of Cercospora beticola in Serbia using PCR-based detection of resistance-associated mutations of the β-tubulin gene. European Journal of Plant Pathology 135 (4): 889–902. DOI: 10.1007/s10658-012-0135-x

 

Trkulja N.R., Milosavljević A.G., Milana S., Mitrović M.S., Jović J.B., Toševski I.T., Khan M.F.R., Secor G.A. 2017. Molecular and experimental evidence of multi-resistance of Cercospora beticola field populations to MBC, DMI and QoI fungicides. European Journal of Plant Pathology 149 (4): 895–910. DOI: 10.1007/s10658-017-1239-0

 

van den Berg F., van den Bosch F., Paveley N. 2013. Optimal fungicide application timings for disease control are also an effec­tive anti-resistance strategy: a case study for Zymoseptoria tritici (Mycosphaerella graminicola) on wheat. Phytopathology 103 (12): 1209–1219. DOI: 10.1094/PHYTO-03-13-0061-R

Progress in Plant Protection (2025) : 0-0
First published on-line: 2025-09-25 12:18:15
http://dx.doi.org/10.14199/ppp-2025-019
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