Modern Fungicides: Mechanisms of Action, Fungal Resistance and Phytotoxic Effects

Main Article Content

Ekaterina V. Baibakova
Elena E. Nefedjeva
Małgorzata Suska-Malawska
Mateusz Wilk
Galina A. Sevriukova
Vladimir F. Zheltobriukhov


The establishment of safe and effective methods for controlling fungal diseases is an urgent issue in agriculture and forestry. Fungicide research has provided a wide range of products with new modes of action. Extensive use of these compounds in agriculture enhances public anxiety due to the harmful potential for the environment and human health. Moreover, the phytotoxic effects of some fungicides are already recognized but still little is known about their influence on the photosynthetic apparatus and plant physiology. This review provides an understanding of the mechanisms of action of fungicides, mechanisms of fungicide resistance development, and the phenomenon of phytotoxicity.

Contact fungicides, systemic fungicides, disease control, resistance

Article Details

How to Cite
Baibakova, E. V., Nefedjeva, E. E., Suska-Malawska, M., Wilk, M., Sevriukova, G. A., & Zheltobriukhov, V. F. (2019). Modern Fungicides: Mechanisms of Action, Fungal Resistance and Phytotoxic Effects. Annual Research & Review in Biology, 32(3), 1-16.
Review Article


Rohr JR, Brown J, Battaglin WA, McMahon TA, Relyea RA. A pesticide paradox: Fungicides indirectly increase fungal infections. Ecological Applications. 2017; 27(8):2290–2302.
DOI: 10.1002/eap.1607

Xia XJ, Huang YY, Wang L, et al. Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L. Pesticide Biochemistry and Physiology. 2006;86(1):42–48.
DOI: 10.1016/J.PESTBP.2006.01.005

Marín S, Ramos AJ, Cano-Sancho G, Sanchis V. Reduction of mycotoxins and toxigenic fungi in the Mediterranean basin maize chain. Phytopathologia Mediterranea. 2012;51(1):93–118.
(Accessed January 10, 2018)

Forrer HR, Musa T, Schwab F, et al. Fusarium head blight control and prevention of mycotoxin contamination in wheat with botanicals and tannic acid. Toxins. 2014;6(3):830–849.
DOI: 10.3390/toxins6030830

Pablo C. García, Rosa M. Rivero, Juan M. Ruiz LR. The role of fungicides in the physiology of higher plants: Implications for defense responses. The Botanical Review. 2003;69(2):162–172.

Report on the pesticide residues monitoring programme: Quarter 1 2017. London; 2017.

Petit AN, Fontaine F, Clement, Christophe; Vaillant-Gaveau N. Photosynthesis limitations of grapevine after treatment with the fungicide fludioxonil. Agriculture and Food Chemistry. 2008;56:6761–6767.
DOI: 10.1021/jf800919u

Vincelli P. QoI (Strobilurin) Fungicides: Benefits and Risks. The Plant Health Instructor; 2002.
DOI: 10.1094/PHI-I-2002-0809-02

Southern AG. Liquid copper fungicide. New Jersey; 2015.

Hahn Matthias. The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. Journal of Chemical Biology. 2014;7(4):133–41.
DOI: 10.1007/s12154-014-0113-1

Lesemann SS, Schimpke S, Dunemann F, Deising HB. Mitochondrial heteroplasmy for the cytochrome b gene Controls the level of strobilurin resistance in the apple powdery mildew fungus Podosphaera leucotricha (Ell. & Ev.) E.S. Salmon. Journal of Plant Diseases and Protection. 2006;113(6):259–266.
DOI: 10.1007/BF03356191

Oliver RP, Hewitt HG. Fungicides in crop protection. 2th Ed. CAB International; 2014.

Aynalem B, Assefa F. Effect of glyphosate and mancozeb on the rhizobia isolated from nodules of Vicia faba L. and on their N 2 -fixation, North Showa, Amhara Regional State, Ethiopia. Advances in Biology. 2017;2017:1–7.
DOI: 10.1155/2017/5864598

Johnson DA, Hamm PB, Miller JS, State W. Fungicide application for management of potato late blight in the Columbia Basin; 2014.
(Accessed December 21, 2017)

González M., Caetano P. SME. Testing systemic fungicides for control of Phytophthora oak root disease. Forest Pathology. 2017;47(4):1–3.
DOI: 10.1111/efp.12343

Dias Maria Celeste. Phytotoxicity: An overview of the physiological responses of plants exposed to fungicides. Journal of Botany. 2012;1–4.
DOI: 10.1155/2012/135479

Borgers Marcel. Mechanism of Action of Antifungal Drugs, with Special Reference to the Imidazole Derivatives [with Discussion]. Reviews of Infectious Diseases. 1980;2:520–534.

Mueller DS. Fungicides: Terminology. Integrated Crop Management. 2006:120–123.
Available: January 10, 2018)

Paul Vincelli, Bruce Clarke GM. Chemical Control of Turfgrass Diseases; 2017.

Lucas JA (John Alexander). Plant pathology and plant pathogens. John Wiley & Sons; 2009.

Deising HB, Reimann S, Pascholati SF. Mechanisms and significance of fungicide resistance. Brazilian Journal of Microbiology. 2008;39(2):286–295.

Miguez M, Reeve C, Wood PM, Hollomon DW. Alternative oxidase reduces the sensitivity ofMycosphaerella graminicola to QOI fungicides. Pest Management Science 2004; 60(1):3–7.
DOI: 10.1002/ps.837

Bernauer O, Gaines-Day H, Steffan S. Colonies of Bumble Bees (Bombus impatiens) produce fewer workers, less bee biomass, and have smaller mother queens following fungicide exposure. Insects. 2015;6(4):478–488.
DOI: 10.3390/insects6020478

Saladin Gaëlle, Magné Christian CC, Clément C. Effects of fludioxonil and pyrimethanil, two fungicides used against Botrytis cinerea, on carbohydrate physiology in Vitis vinifera L. Pest Management Science. 2003;59(10):1083–1092.
DOI: 10.1002/ps.733

McGrath MT. What are Fungicides? The Plant Health Instructor; 2004.
DOI: 10.1094/PHI-I-2004-0825-01

Jørgensen Lise Nistrup, Oliver Richard Peter, Heick Thies Marten. Occurrence and avoidance of fungicide resistance in cereal diseases. 2018;235–259.

Cameron J. Effects of Seed Applied Fungicide on arbuscular mycorrhizal colonization of South Dakota cultivars of Oat, Soybean, and Corn; 2016.

Ganiev MM, Nedorezkov VD. Chemical plant protection products. (A.S. Maksimova, ed). Moscow: Colossus; 2006. Russian.

Paranjape K,‎ Gowariker V,‎ Krishnamurthy VN,‎ Gowariker S,‎ KP. The pesticide encyclopedia. UK ed. Edi. London: CABI; 2014.

Woodward JE, Russell SA, Baring MR, Cason JM, Baughman TA. Effects of Fungicides, Time of Application, and Application Method on Control of Sclerotinia Blight in Peanut. International Journal of Agronomy. 2015;8.
DOI: 10.1155/2015/323465

E. Lee Butler LPT. Method and timing of fungicide applications for control of spring dead spot in hybrid bermudagrass. Plant Health Progress; 2006.
DOI: 10.1094/PHP-2006-0901-01-RS

Hasan MA, Ahmed JU, Tofazzal H, Mian MAK, Haque MM. Evaluation of the physiological quality of wheat seed as influenced by high parent plant growth temperature. Journal of Crop Science and Biotechnology. 2013;16(1):69–74.
DOI: 10.1007/s12892-010-0056-1

Shuping DSS, Eloff JN. The use of plants to protect plants and food against fungal pathogens: A review. African journal of traditional, complementary, and alternative medicines. AJTCAM. 2017;14(4):120–127. DOI: 10.21010/ajtcam.v14i4.14

Clayton A. Hollier, Jeffrey W. Hoy, Christopher A. Clark, Charles Overstreet, Jaspreet Sidhu, Melanie L. Lewis Ivey, Raghuwinder Singh, Trey Price III, Mary Helen Ferguson, G. Boyd Padgett DG. Louisiana Plant Disease Management Guide. Louisiana; 2016.

Kerr Ailen, Keane Philip. Prediction of disease outbreaks. In: Brown JF, Ogle HJ eds., ed. Plant pathogens and diseases. Armidale, NSW: University of England Print. 1997;229–314.

Suffert F, Thompson RN. Some reasons why the latent period should not always be considered constant over the course of a plant disease epidemic. Plant Pathology. 2018;67(9):1831–1840.
DOI: 10.1111/ppa.12894

Ming-wang Shi. Based on time series and RBF network plant disease forecasting. Procedia Engineering. 2011;15:2384–2387.
DOI: 10.1016/J.PROENG.2011.08.447

Benelli Jesse J. Non-target effects of strobilurin fungicide applications on creeping bentgrass putting greens during summer stress; 2013.

Kuna-Broniowski M, Makarski P, Kuna-Broniowska I. Application of electric fields as a method for plant disease forecasting. Agriculture and Agricultural Science Procedia. 2015;7:146–151.
DOI: 10.1016/J.AASPRO.2015.12.009

Donatelli M, Magarey RD, Bregaglio S, Willocquet L, Whish JPM, Savary S. Modelling the impacts of pests and diseases on agricultural systems. Agricultural Systems. 2017;155:213–224. DOI: 10.1016/J.AGSY.2017.01.019

Untiedt R, Blanke MM. Effects of fungicide and insecticide mixtures on apple tree canopy photosynthesis, dark respiration and carbon economy. Crop Protection. 2004;23(10):1001–1006.
DOI: 10.1016/j.cropro.2004.02.012

Kjøhl M, Nielsen A, Stenseth NC. Potential effects of climate change on crop pollination; 2011.

Tom Allen. Not everything is as it seems: Fungicide phytotoxicity and plant diseases | Mississippi Crop Situation. Mississippi Crop Situation; 2013.
(Accessed January 9, 2018)

Cools HJ, Hawkins NJ, Fraaije BA. Constraints on the evolution of azole resistance in plant pathogenic fungi. Plant Pathology. 2013;62:36–42.
DOI: 10.1111/ppa.12128

Kilani J, Fillinger S. Phenylpyrroles: 30 Years, Two Molecules and (Nearly) No Resistance. Frontiers in Microbiology. 2016;7:2014.
DOI: 10.3389/fmicb.2016.02014

Lew RR. Turgor and net ion flux responses to activation of the osmotic MAP kinase cascade by fludioxonil in the filamentous fungus Neurospora crassa. Fungal Genetics and Biology. 2010;47(8):721–726.
DOI: 10.1016/J.FGB.2010.05.007

Ren W, Shao W, Han X, Zhou M, Chen C. Molecular and biochemical characterization of laboratory and field mutants of Botrytis cinerea resistant to fludioxonil. Plant Disease 2016; 100(7):1414–1423.
DOI: 10.1094/PDIS-11-15-1290-RE

Walker AS, Micoud A, Rémuson F, Grosman J, Gredt M, Leroux P. French vineyards provide information that opens ways for effective resistance management of Botrytis cinerea (grey mould). Pest Management Science. 2013;69(6):667–678.
DOI: 10.1002/ps.3506

Leroux P. Recent Developments in the Mode of Action of Fungicides. Pesticide Science. 1996;47(2):191–197.

Ahemad M, Khan MS. Alleviation of fungicide-induced phytotoxicity in greengram [Vigna radiata (L.) Wilczek] using fungicide-tolerant and plant growth promoting Pseudomonas strain. Saudi Journal of Biological Sciences. 2012; 19(4):451–459.
DOI: 10.1016/J.SJBS.2012.06.003

Costa AV, Oliveira MVL de, Pinto RT, et al. Synthesis of novel glycerol-derived 1,2,3-triazoles and evaluation of their fungicide, phytotoxic and cytotoxic activities. Molecules. 2017;22(10):1666.
DOI: 10.3390/molecules22101666.

Balba H. Review of strobilurin fungicide chemicals. Journal of Environmental Science and Health, Part B. 2007; 42(4):441–451.
DOI: 10.1080/03601230701316465

Reddy PP. Strobilurin Fungicides. In: Recent advances in crop protection. New Delhi: Springer India. 2012;185–200.

Wojdyła AT. Influence of strobilurin compounds on the development of Puccinia horiana. Communications in Agricultural and Applied Biological Sciences. 2007; 72(4):961–6.
(Accessed January 23, 2018)

Isaac S. Fungal-plant interactions. 1. ed. London: Chapman & Hall; 1992.

Biol TJ, Jităreanu A, Pădureanu S, Tătărîngă G, Tuchiluș C, Stănescu U. Evaluation of phytotoxic and mutagenic effects of some cinnamic acid derivatives using the Triticum test. Turkish Journal of Biology. 2013:748–756.
DOI: 10.3906/biy-1304-39

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

Barr CM, Neiman M, Taylor DR. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist 2005;168(1):39–50.
DOI: 10.1111/j.1469-8137.2005.01492.x

Nason MA, Farrar J, Bartlett D. Strobilurin fungicides induce changes in photosynthetic gas exchange that do not improve water use efficiency of plants grown under conditions of water stress. Pest Management Science Pest Manag Sci. 2007;63:1191–1200.
DOI: 10.1002/ps.1443

Hunsche M, Damerow L, Schmitz-Eiberger M, Noga G. Mancozeb wash-off from apple seedlings by simulated rainfall as affected by drying time of fungicide deposit and rain characteristics. Crop Protection. 2007; 26(5):768–774.
DOI: 10.1016/j.cropro.2006.07.003

Changjun Chen, Jianxin Wang, Qingquan Luo SY, Mingguo Z. Characterization and fitness of carbendazim-resistant strains ofFusarium graminearum (wheat scab). Pest Management Science. 2007;63(12): 1201–1207.
DOI: 10.1002/ps.1449

Lamberth C. Morpholine fungicides for the treatment of powdery mildew. In: Bioactive Heterocyclic Compound Classes. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA. 2012;119–127.

Kandel YR, Mueller DS, Legleiter T, Johnson WG, Young BG, Wise KA. Impact of fluopyram fungicide and preemergence herbicides on soybean injury, population, sudden death syndrome, and yield. Crop Protection. 2018;106:103–109.
DOI: 10.1016/j.cropro.2017.12.009

Pantazopoulou A, Diallinas G. Fungal nucleobase transporters. FEMS Microbiology Reviews. 2007;31(6):657–675.
DOI: 10.1111/j.1574-6976.2007.00083.x

War AR, Paulraj MG, Ahmad T, et al. Mechanisms of plant defense against insect herbivores. Plant Signaling & Behavior. 2012;7(10):1306–20.
DOI: 10.4161/psb.21663.

Indian Council Of Agricultural research. Handbook of agriculture. 6th ed. New Delhi: Directorate of Information and Publications of Agriculture, Indian Council of Agricultural Research; 2011.

Pérez-de-Luque A, Tille S, Johnson I, Pascual-Pardo D, Ton J, Cameron DD. The interactive effects of arbuscular mycorrhiza and plant growth-promoting rhizobacteria synergistically enhance host plant defences against pathogens. Scientific Reports. 2017;7(1).
DOI: 10.1038/s41598-017-16697-4

He, Xue-Li, Wang P, Ma L, Meng JJ. Effects of three fungicides on arbuscular mycorrhizal fungal infection and growth of Scutellaria baicalensis Georgi. Huan Jing Ke Xue= Huanjing Kexue. 2012; 33(3): 987–91. Available:
(Accessed January 18, 2018)

Doe J. Arbuscular mycorrhizal fungi not inhibited by seed-applied fungicides. CSA News. 2017;62(7):12.
DOI: 10.2134/csa2017.62.0713

Schreiner RP, Bethlenfalvay GJ. Plant and soil response to single and mixed species of arbuscular mycorrhizal fungi under fungicide stress. Applied Soil Ecology. 1997;7:93–102. Available:
(Accessed January 22, 2018)

Hongyan, Germida JJ, Walley FL. Suppressive effects of seed-applied fungicides on arbuscular mycorrhizal fungi (AMF) differ with fungicide mode of action and AMF species. Applied Soil Ecology. 2013;72:22–30.
(Accessed January 22, 2018)

Murillo-Williams A, Pedersen P. Arbuscular mycorrhizal colonization response to three seed-applied fungicides. Agronomy Journal. 2008;100(3):795.
DOI: 10.2134/agronj2007.0142.

Hernández-Dorrego A, Mestre-Parés J. Evaluation of some fungicides on mycorrhizal symbiosis between two Glomus species from commercial inocula and Allium porrum L. seedlings. Spanish Journal of Agricultural Research. 2010; 8(S1):43.
DOI: 10.5424/sjar/201008S1-1222