Avoid common mistakes on your manuscript.
Many cases of fungicide resistance are caused by homologous mutations in the target genes. As the genes differ in length in different pathogen species, the numbering of homologous mutations can cause confusion. We introduced the idea of giving ‘labels’ to homologous mutations based on alignment to an archetype sequence (Mair et al. (2016). Cases of resistance-associated mutation published since the last Reinhardsbrunn meeting are listed in the tables below. In some cases, the archetype gene sequence has been given a new identifier. A complete list is available from the authors. The species abbreviations are given at gd.eppo.int. The alignments were defined using FRAST—a Fungicide Resistance Alignment Sequence Tool—https://www.frast.com.au/ (Tables 1, 2, 3, 4, 5, 6, 7, 8, 9, 10).
References
Adnan M et al (2018) Detection and molecular characterization of resistance to the dicarboximide and benzamide fungicides in Botrytis cinerea from Tomato in Hubei Province, China. Plant Dis 102(7):1299–1306
Assinger T et al (2021) Fungicide strategies and resistance of Ramularia collo-cygni to demethylation and succinate dehydrogenase inhibitors in Austrian winter barley (Hordeum vulgare). J Plant Dis Prot 128:735–748
Assinger T et al (2022) Detection of Ramularia collo-cygni DMI- and SDHI-resistant field populations in Austria and the effect of fungicides on the population and genetic diversity. Eur J Plant Pathol 162(3):575–594
Bittner RJ, Sweigard JA, Mila AL (2017) Assessing the resistance potential of Phytophthora nicotianae, the causal agent of black shank of tobacco, to oxathiopropalin with laboratory mutants. Crop Prot 102:63–71
Cai M et al (2020) Stepwise accumulation of mutations in CesA3 in Phytophthora sojae results in increasing resistance to CAA fungicides. Evol Appl 14:996–1008
Chen W et al (2022) Sterol demethylation inhibitor fungicide resistance in Colletotrichum siamense from chili is caused by mutations in CYP51A and CYP51B. Phytopathol Res 4(1):1–16
Chitolina GM et al (2021) Distribution of Alternaria alternata isolates with resistance to quinone outside inhibitor (QoI) fungicides in Brazilian orchards of tangerines and their hybrids. Crop Prot 141:105493
Chong P et al (2021) A world-wide analysis of reduced sensitivity to DMI fungicides in the banana pathogen Pseudocercospora fijiensis. Pest Manag Sci 77:3273–3288
Claus A, Simões K, May De Mio LL (2022) Sdh C-I86F mutation in Phakopsora pachyrhizi is stable and can be related to fitness penalties. Phytopathology 112(7):1413–1421
Cook, N.M. et al., High frequency of fungicide resistance-associated mutations in the wheat yellow rust pathogen Puccinia striiformis f. sp. tritici. Pest Management Science, 2021. n/a(n/a).
Dooley H et al (2016) Detection of Zymoseptoria tritici SDHI-insensitive field isolates carrying the SdhC-H152R and SdhD-R47W substitutions. Pest Manag Sci 72:2203–2207
Duan Y et al (2019) Benzimidazole- and QoI-resistance in Corynespora cassiicola populations from greenhouse-cultivated cucumber: an emerging problem in China. Pestic Biochem Physiol 153:95–105
Erreguerena IA et al (2022) Characterization of DMI, QoI and SDHI fungicides sensitivity of Ramularia collo-cygni isolates in Argentina. J Plant Dis Prot 129:1343–1353
Fontaine S et al (2019) Investigation of the sensitivity of Plasmopara viticola to amisulbrom and ametoctradin in French vineyards using bioassays and molecular tools. Pest Manag Sci 75(8):2115–2123
Fouché G et al (2021) Directed evolution predicts cytochrome b G37V target site modification as probable adaptive mechanism towards the QiI fungicide fenpicoxamid in Zymoseptoria tritici. Environ Microbiol 24:1117–1132
Fraaije B et al (2020) The multi-fungicide resistance status of Aspergillus fumigatus populations in arable soils and the wider European environment. Front Microbiol 11(3199):599233
FRAC. Succinate Dehydrogenase Inhibitor (SDHI) Working Group 10th Meeting on December 13, 2017. 2018; Available from: http://www.frac.info/.
Gao X et al (2022) Analysis of resistance risk and resistance-related point mutations in Cyt b of QioI fungicide ametoctradin in Phytophthora litchii. Pest Manag Sci 78:2921–2930
Harper LA et al (2021) Fungicide resistance characterized across seven modes of action in Botrytis cinerea isolated from Australian vineyards. Pest Manag Sci. https://doi.org/10.1002/ps.6749
Hu J et al (2018) Thiophanate-methyl resistance in Sclerotinia homoeocarpa from golf courses in China. Pestic Biochem Physiol 152:84–89
Jørgensen KM et al (2021) Dissection of the activity of agricultural fungicides against clinical aspergillus isolates with and without environmentally and medically induced azole resistance. J Fungi 7(3):205
Kiiker R et al (2021) Changes in DMI, SDHI, and QoI fungicide sensitivity in the estonian Zymoseptoria tritici population between 2019 and 2020. Microorganisms 9(4):814
Li HX et al (2019) Differences in fungicide resistance profiles and multiple resistance to a quinone-outside inhibitor (QoI), two succinate dehydrogenase inhibitors (SDHI), and a demethylation inhibitor (DMI) for two Stagonosporopsis species causing gummy stem blight of cucurbits. Pest Manag Sci 75:3093–3101
Li S et al (2021) The research progress in and perspective of potential fungicides: Succinate dehydrogenase inhibitors. Bioorganic Med Chem 50:116476
Li F et al (2022) Synergistic effect of amino acid substitutions in CYP51B for prochloraz resistance in Fusarium fujikuroi. Pestic Biochem Physiol 189:105291
Li Y et al (2022) Resistance risk and resistance-related point mutation in SdhB and SdhC1 of cyclobutrifluram in Fusarium pseudograminearum. J Agric Food Chem. https://doi.org/10.1002/ps.7616
Liu K et al (2022) Biological and molecular characterizations of fluxapyroxad-resistant isolates of Botrytis cinerea. Phytopathol Res 4(1):2
Liu S et al (2022) Functional characterization of MoSdhB in conferring resistance to pydiflumetofen in blast fungus Magnaporthe oryzae. Pest Manag Sci 78:4018–4027
MacKenzie KJ et al (2020) Widespread QoI fungicide resistance revealed among corynespora cassiicola tomato isolates in Florida. Plant Dis 104(3):893–903
Mair W et al (2016) Proposal for a unified nomenclature for target-site mutations associated with resistance to fungicides. Pest Manag Sci 72(8):1449–1459
Malandrakis AA et al (2022) Fungicide resistance frequencies of Botrytis cinerea greenhouse isolates and molecular detection of a novel SDHI resistance mutation. Pestic Biochem Physiol 183:105058
Mathew FM et al (2019) Resistance to Quinone Outside Inhibitor fungicides conferred by the G143A mutation in Cercospora sojina (Causal Agent of Frogeye Leaf Spot) isolates from South Dakota Soybean Fields. Plant Health Prog 20(2):104–105
Mboup MK et al (2022) Genetic mechanism, baseline sensitivity and risk of resistance to oxathiapiprolin in oomycetes. Pest Manag Sci 78:905–913
Mello FED et al (2021) Sensitivity assessment and SDHC-I86F mutation frequency of Phakopsora pachyrhizi populations to benzovindiflupyr and fluxapyroxad fungicides from 2015 to 2019 in Brazil. Pest Manag Sci 77:4331–4339
Mello FED et al (2021) Resistance of Corynespora cassiicola from soybean to QoI and MBC fungicides in Brazil. Plant Pathol. https://doi.org/10.1111/ppa.13474
Miao J et al (2020) Multiple point mutations in PsORP1 gene conferring different resistance levels to oxathiapiprolin confirmed using CRISPR–Cas9 in Phytophthora sojae. Pest Manag Sci 76(7):2434–2440
Miyamoto T et al (2010) Distribution and molecular characterization of Corynespora cassiicola isolates resistant to boscalid. Plant Pathol 59(5):873–881
Müller MA, Stammler G, MayDeMio LL (2021) Multiple resistance to DMI, QoI and SDHI fungicides in field isolates of Phakopsora pachyrhizi. Crop Prot 145:105618
Oiki S et al (2022) Wide distribution of resistance to the fungicides fludioxonil and iprodione in Penicillium species. PLoS ONE 17(1):e0262521
Pearce TL et al (2019) Multiple mutations across the succinate dehydrogenase gene complex are associated with boscalid resistance in Didymella tanaceti in pyrethrum. PLoS ONE 14(6):e0218569
Rodriguez SB et al (2021) Impact of SDH mutations in Alternaria solani on recently developed SDHI fungicides adepidyn and solatenol. Plant Dis 105(10):3015–3024
Salehi Z et al (2023) Clinical epidemiology of pulmonary aspergillosis in hospitalized patients and contribution of Cyp51A, Yap1, and Cdr1B mutations to voriconazole resistance in etiologic Aspergillus species. Eur J Clin Microbiol Infect Dis 42:853–864. https://doi.org/10.1007/s10096-023-04608-7
Shao W et al (2022) Fusarium graminearum FgSdhC1 point mutation A78V confers resistance to the succinate dehydrogenase inhibitor pydiflumetofen. Pest Manag Sci 78(5):1780–1788
Simões K et al (2018) First detection of a SDH variant with reduced SDHI sensitivity in Phakopsora pachyrhizi. J Plant Dis Prot 125(1):21–26
Spanner R et al (2021) Genome-wide association and selective sweep studies reveal the complex genetic architecture of DMI fungicide resistance in Cercospora beticola. Genome Biol Evol 13(9):evab209
Stammler G et al (2015) Respiration inhibitors: complex II. Fungicide Resistance in Plant Pathogens. Springer, pp 105–117
Stergiopoulos I et al (2022) Identification of putative SDHI target site mutations in the SDHB, SDHC, and SDHD subunits of the grape powdery mildew pathogen Erysiphe necator. Plant Dis 106(9):2310–2320
Testempasis SI, Karaoglanidis GS (2023) Resistance of black aspergilli species from grape vineyards to SDHI, QoI, DMI, and phenylpyrrole fungicides. J Fungi 9(2):221
Wang J et al (2014) Novel mutations in CYP51B from Penicillium digitatum involved in prochloraz resistance. J Microbiol 52(9):762–770
Wang Z et al (2022) Activity and point mutation G699V in PcoORP1 confer resistance to oxathiapiprolin in Phytophthora colocasiae field isolates. J Agric Food Chem 70(44):14140–14147
Xu S et al (2019) Molecular characterization of carbendazim resistance of Fusarium species complex that causes sugarcane pokkah boeng disease. BMC Genomics 20(1):115
Xue Z et al (2022) Multiple mutations in SDHB and SDHC2 Subunits confer resistance to the succinate dehydrogenase inhibitor cyclobutrifluram in Fusarium fujikuroi. J Agric Food Chem 71:3694–3704
Xue Z et al (2023) Resistance risk assessment for the new OSBP inhibitor Y18501 in Pseudoperonospora cubensis and point mutations (G705V, L798W, and I812F) in PscORP1 that Confer Resistance. J Agric Food Chem 71(2023):4510–4520
Zhou Y et al (2015) Resistance mechanisms and molecular docking studies of four novel QoI fungicides in Peronophythora litchii. Sci Rep 5(1):1–10
Zhu F et al (2019) Occurrence, distribution, and characteristics of boscalid-resistant corynespora cassiicola in China. Plant Dis 103(1):69–76
Acknowledgements
Research in the CCDM is supported by the Australian Grains Research and Development Corporation and Curtin University.
Funding
The funding was provided by GRDC (Grant No. CUR00023).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Oliver, R., Hane, J., Mair, W. et al. The 2023 update of target site mutations associated with resistance to fungicides and a web-tool to assist label designations. J Plant Dis Prot 131, 1265–1270 (2024). https://doi.org/10.1007/s41348-024-00872-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-024-00872-7