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New chemical fungicides in relation to risk for resistance development

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Abstract

Fungicides have played a key role in crop disease control worldwide. However, resistance development in pathogen populations became a serious concern in as early as 1970s and has increased further in recent years. More stringent pesticide regulation based on precautionary principle has made the introduction of new chemistry challenging. Despite such difficulties, many fungicides have been developed successfully and some of them have novel mode of actions such as the inhibition of DHODH and GWT1. In this paper, the author reviews large numbers of literature on newly developed fungicides in relation to resistance. The approach to mitigate resistance which includes the application of non-fungitoxic disease resistance inducers, crop resistance breeding, and biocontrol is also discussed briefly.

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References

  • Adaskaveg JE, Luo Y, Förster H (2020) Characterization of resistance to five SDHI sub-groups in Alternaria species causing leaf spot of almond in California. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 173-180

  • Agriland (2019) ‘Endocrine disruptor’ fungicide withdrawn in France. https://www.agriland.ie/farming-news/endocrine-disruptor-fungicide-withdrawn-in-france/. Accessed 31 July 2022

  • Amiri A, Heath SM, Peres NA (2014) Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from strawberry. Plant Disease 98:532–539

    Article  CAS  PubMed  Google Scholar 

  • Amiri A, Zuniga AI, Peres NA (2020) Mutations in the membrane-anchored SdhC subunit affect fitness and sensitivity to succinate dehydrogenase inhibitors in Botrytis cinerea populations from multiple hosts. Phytopathology 110:327–335

    Article  CAS  PubMed  Google Scholar 

  • Andes D (2022) New antifungals in development. Presentation at the workshop ‘The role of plant agricultural practices on development of antimicrobial resistant fungi affecting human health’. The National Academies, USA. https://www.nationalacademies.org/our-work/the-role-of-agricultural-practices-on-development-of-antimicrobial-resistant-microbes-affecting-human-health-a-workshop-series. Accessed 31 July 2022

  • Andreassi JL, Gutterridge S, Pember SO, Sweigard JA (2013) Detection and screening method and materials useful in performance thereof. International Patent No. WO2013009971. World Intellectual Property Organization, Geneva, USA

  • Astvad KMT, Jørgensen KM, Hare RK, Datcu R, Arendrup MC (2021) Olorofim susceptibility testing of 1,423 Danish mold isolates obtained in 2018–2019 confirms uniform and broad-spectrum activity. Antimicrobial Agents and Chemotherapy 65:e01527-e1620

    CAS  Google Scholar 

  • Avenot HF, van den Biggelaar H, Morgan DP, Moral J, Joosten M, Michailides TJ (2014) Sensitivities of baseline isolates and boscalid-resistant mutants of Alternaria alternata from pistachio to fluopyram, penthiopyrad, and fluxapyroxad. Plant Disease 98:197–205

    Article  CAS  PubMed  Google Scholar 

  • Avenot HF, Luna M, Michailides TJ (2019) Phenotypic and molecular characterization of resistance to the SDHI fungicide fluopyram in populations of Alternaria alternata from pistachio orchards in California. Crop Protection 124:104838

    Article  CAS  Google Scholar 

  • Avenot HF, Michailides TJ (2010) Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Protection 29:643–651

    Article  CAS  Google Scholar 

  • Avenot HF, Thomas A, Gitaitis RD, Langston Jr DB, Stevenson KL (2012) Molecular characterization of boscalid- and penthiopyrad-resistant isolates of Didymella bryoniae and assessment of their sensitivity to fluopyram. Pest Management Science 68:645–651

  • Avila-Adame C, Wang N, Slanee T, Yao C (2019) In vitro insensitivity of Rhizoctonia solani to the natural product UK-2A associated with L198F variant at the Qi target site of cytochrome b. Phytopathology 105:S2.76 (Abstr.)

  • Ayer KM, Villani SM, Choi M-W, Cox KD (2019) Characterization of the VisdhC and VisdhD genes in Venturia inaequalis, and sensitivity to fluxapyroxad, pydiflumetofen, inpyrfluxam, and benzovindiflupyr. Plant Disease 103:1092–1100

    Article  CAS  PubMed  Google Scholar 

  • Bartholomaeus A, Dahmen P, Desbordes P, Essigmann B, Gary S, Gutbrod O, Kleemann J, Lancashire P, Maue M, Schwarz H-G, Tinwell H (2021) Isoflucypram - the next-generation succinate dehydrogenase inhibitor fungicide. In: Maienfisch P, Mangelinckx S (eds) Recent Highlights in the Discovery and Optimization of Crop Protection Products. Academic Press, London, UK, pp 367–380

    Chapter  Google Scholar 

  • Bittner RJ, Sweigard JA, Mila AL (2017) Assessing the resistance potential of Phytophthora nicotianae, the causal agent of black shank of tobacco, to oxathioprolin with laboratory mutants. Crop Protection 102:63–71

    Article  CAS  Google Scholar 

  • Budde-Rodriguez S, Celoy RM, Mallik I, Pasche JS, Gudmestad NC (2021) Impact of SDH mutations in Alternaria solani on recently developed SDHI fungicides Adepidyn and Solatenol. Plant Disease 105:3015–3024

    Article  CAS  PubMed  Google Scholar 

  • Buil JB, Oliver JD, Law D, Baltussen T, Zoll J, Hokkens MWJ, Tehupeiory-Kooreman M, Melchers WJG, Birth M, Verweij P (2022) Resistance profiling of Aspergillus fumigatus to olorofim indicates absence of intrinsic resistance and unveils the molecular mechanisms of acquired olorofim resistance. Emerging Microbes & Infections 11:703–714

    Article  CAS  Google Scholar 

  • Carraro TAC, Lichtemberg PSF, Michailides TJ, May De Mio LL (2020) Assessing the sensitivity levels of Colletotrichum spp. to multiple chemical fungicide groups with potential use to manage persimmon anthracnose disease in Brazil. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 37-38

  • Castroagudin VL, Ceresini PC, de Oliveira SC, Reges JTA, Maciel JLN, Bonato ALV, Dorigan AF, McDnald BA (2015) Resistance to QoI fungicides is widespread in Brazilian populations of the wheat blast pathogen Magnaporthe oryzae. Phytopathology 105:284–294

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Wei L, Zhao W, Wang B, Zheng H, Zhang P, Lou T, Duan Y, Hou Y, Zhou M, Chen C (2021) Resistance risk assessment for a novel succinate dehydrogenase inhibitor pydiflumetofen in Fusarium asiaticum. Pest Management Science 77:538–547

    Article  CAS  PubMed  Google Scholar 

  • Cherrad S, Hernandez C, Steva H, Vacher S (2018) Resistance de Plamopara viticola aux inhibiteurs du complexe III: un point sur la caracterisation phenotypique et genotypique des souches. Proc. 12th Intr. Conf, Plant Dis.: 449–459 (in French with English abstr.)

  • Claus A, Simões K, May De Mio LL (2022) SdhC-I186F mutation in Phakopsora pachyrhizi is stable and can be related to fitness penalties. Phytopathology 112:1413–1421

    Article  CAS  PubMed  Google Scholar 

  • Cohen Y (2015) The novel oomycide oxathiapiprolin inhibits all stages in the asexual life cycle of Pseudoperonospora cubensis - causal agent of cucurbit downy mildew. PLoS One 10:e0140015

  • Cohen Y, Rubin AE, Galperin M (2018) Oxathiapiprolin-based fungicides provide enhanced control of tomato late blight induced by mefenoxam-insensitive Phytophthora infestans. PLoS ONE 13:e0204523

  • Corkley I, Fraaije B, Hawkins N (2022) Fungicide resistance management: Maximizing the effective life of plant protection products. Plant Pathology 71:150–169

    Article  Google Scholar 

  • Craig IR, Stammler G, Bryson R, Rheinheimer J, Klappach K (2020) Molecular insight into the binding of metyltetraprole: a new QoI fungicide. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 271-276

  • Dekker J, Georgopoulos SG (1982) Fungicide Resistance in Crop Protection. Pudoc, Wageningen, p 273

  • Desbordes P, Essigmann B, Gary S, Gutbrod O, Maue M, Schwarz H-G (2020) Isoflucypram, the first representative of a new succinate dehydrogenase inhibitor fungicide subclass: its chemical discovery and unusual binding mode. Pest Managment Science 76:3340–3347

    Article  CAS  Google Scholar 

  • Doughty KJ, Sierotzki H, Semar M, Goertz A (2021) Selection and amplification of fungicide resistance in Aspergillus fumigatus in relation to DMI fungicide use in agronomic settings: hotspots versus coldspots. Microorganisms 9:2439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Draskau MK, Boberg J, Taxvig C, Pederson M, Frandsen HL, Christiansen S, Svingen T (2019) In vitro and in vivo endocrine disrupting effects of the azole fungicides triticonazole and flusilazole. Environmental Pollution 255:113309

    Article  CAS  PubMed  Google Scholar 

  • Dreinert A, Wolf A, Mentzel T, Meunier B, Fehr M (2018) The cytochrome bc1 complex inhibitor ametoctradin has an unusual binding mode. BBA-Bioenergetics 1859:567–576

    Article  CAS  PubMed  Google Scholar 

  • Duan Y, Xiu Q, Li H, Li T, Wang J, Zhou M (2019) Pharmacological characteristics and control efficacy of a novel SDHI fungicide pydiflumetofen against Sclerotinia sclerotiorum. Plant Disease 103:77–82

    Article  CAS  PubMed  Google Scholar 

  • Elis de Mello F, Mathioni SM, Fantin LH, Rosa DD, Antunes RFD, Filho NRC, Duvaresch DL, Canteri MG (2021) Sensitivity assessment and SDHC-I86F mutation frequency of Phakopsora pachyrhizi populations to benzovindiflupyr and fluxapyroxad fungicides from 2015 to 2019 in Brazil. Pest Management Science 77:4331–4339

    Article  Google Scholar 

  • Escribano P, Gómez A, Reigadas E, Muñoz P, Guinea J (2022) In vitro activity of olorofim against Aspergillus fumigatus sensu lato clinical isolates: activity is retained against isolates showing resistance to azoles and/or amphotericin B. Clinical Microbiology and Infection 28:1291.e7-1291.e10

    Article  CAS  PubMed  Google Scholar 

  • European Food Safety Authority (EFSA) (2018) Peer review of the pesticide risk assessment of the active substance BAS 750F (mefentrifluconazole). EFSA Journal 16:5379

    Google Scholar 

  • European Food Safety Authority (EFSA) (2022) Pesticide evaluations: overview and procedure. https://www.efsa.europa.eu/en/applications/pesticides#endocrine-disruptissng-properties. Accessed 31 July 2022

  • Fehr M, Wolf A, Stammler G (2016) Binding of the respiratory chain inhibitor ametoctradin to the mitochondrial bc1 complex. Pest Management Science 72:591–602

    Article  CAS  PubMed  Google Scholar 

  • Feldmann F, Jehle J, Bradάčovά K, Weinmann M (2022) Biostimulants, soil improvers, bioprotectants: promoters of bio-intensification in plant production. Journal of Plant Diseases and Protection 129:707–713

    Article  Google Scholar 

  • Fisher MC, Alastruey A, Berman J, Bicanic T, Bignell EM, Bowyer P, Bromley M, Brüggemann M, Garber G, Cornely OA, Gurr SJ, Harisson TS, Kuijper E, Rhodes J, Sheppard DC, Warris A, White PL, Xu J, Zwaan B, Verweij PE (2022) Tackling the emerging threat of antifungal resistance to human health. Nature Reviews Microbiology 20:557–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher MC, Hawkins NJ, Sanglard D, Gurr SJ (2018) Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science 360:739–742

    Article  CAS  PubMed  Google Scholar 

  • Fisher N, Meunier B, Biagini GA (2020) The cytochrome bc1 complex as an antipathogenic target. FEBS Letters 594:2935–2952

    Article  CAS  PubMed  Google Scholar 

  • Fontaine S, Remuson F, Caddoux L, Barrès B (2019) Investigation of the sensitivity of Plasmopara viticola to amisulbrom and ametoctradin in French vineyards using bioassays and molecular tools. Pest Management Science 75:2115–2123

    Article  CAS  PubMed  Google Scholar 

  • Fraaije B, Atkins S, Hanley S, Macdonald A, Lucas J (2020) The multi-fungicide resistance status of Aspergillus fumigatus populations in arable soils and the wider European environment. Frontiers in Microbiology 11:599233

    Article  PubMed  PubMed Central  Google Scholar 

  • Fouché G, Debieu D, Young D, Meunier B, Walker A-S, Fillinger S (2020) Assessing the risk of resistance selection towards quinone inside inhibitor fungicides (QiIs) in Zymoseptoria tritici. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 57-62

  • Fouché G, Michel T, Lalève A, Wang NX, Young DH, Meunier B, Debieu D, Fillinger S, Walker A-S (2022) Direct evolution predicts cytochrome b G37V target site modification as probable adaptive mechanism towards the QiI fungicide fenpicoxamid in Zymoseptoria tritici. Environmental Microbiology 24:1117–1132

    Article  PubMed  Google Scholar 

  • Fungicide Resistance Action Committee (FRAC) (2022) https://www.frac.info. Accessed 31 July 2022

  • Gao Y, He L, Zhu J, Cheng J, Li B, Liu F, Mu W (2020) The relationship between features enabling SDHI fungicide binding to the Sc-Sdh complex and its inhibitory activity against Sclerotinia sclerotiorum. Pest Management Science 76:2799–2808

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Liu Y, He L, Zhu J, Wu B, Liu F, Mu W (2021) Activity of the novel fungicide mefentrifluconazole against Colletotrichum scovillei. Plant Disease 105:1522–1530

    Article  CAS  PubMed  Google Scholar 

  • Garavito MF, Narvaez-Ortiz HY, Pulido DC, Löffler M, Judelson HS, Restrepo S, Zimmermann BH (2019) Phytophthora infestans dihydroorotate dehydrogenase is a potential target for chemical control – a comparison with the enzyme from Solanum tuberosum. Frontiers in Microbiology 20:1479

    Article  Google Scholar 

  • Garcia-Bayona L, Garavito MF, Lozano GL, Vasquez JJ, Myers K, Fry WE, Bernal A, Zimmermann BH, Restrepo S (2014) De novo pyrimidine biosynthesis in the oomycete plant pathogen Phytophthora infestans. Gene 537:312–321

    Article  CAS  PubMed  Google Scholar 

  • Gisi U, Sierotzki H (2015) Oomycete fungicides: phenylamides, quinone outside inhibitors, and carboxylic acid amides. In: Ishii H, Hollomon DW (Eds.), Fungicide Resistance in Plant Pathogens - principles and a guide to practical management. Springer Japan, Tokyo, Japan, pp 145–174

  • Godoy CV, Seixas CDS, Soares RM, Marcelino-Guimarães FC, Meyer MC, Costamilan LM (2016) Asian soybean rust in Brazil: past, present, and future. Pesquisa Agropecuária Brasileira 51:407–421

    Article  Google Scholar 

  • Gold RE, Schiffer H, Speakman J, Stammler G, Klappach K, Brix HD, Schlehuber S (2011) Initium® - A new innovative fungicide for the control of Oomycetes in speciality crops. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern Fungicides and Antifungal Compounds. Vol. VI, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 55-61

  • Green R, Sang H, Im J, Jung G (2018) Chlorothalonil biotransformation by cytochrome P450 monooxygenases in Sclerotinia homoeocarpa. FEMS Microbiology Letters 365:1–6

    Article  Google Scholar 

  • Guicherit E, Bartlett D, Dale SM, Haas H-U, Scalliet G, Walter H (2013) Solatenol – the second generation benzonorbornene SDHI carboxamide with outstanding performance against key crop diseases. In: Dehne HW, Deising HB, Fraaije B, Gisi U, Hermann D, Mehl A, Oerke EC, Russell PE, Stammler G, Kuck KH, Lyr H (eds) Modern Fungicides and Antifungal Compounds. Vol. VII, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 67-72

  • Guo S, He F, Song B, Wu J (2021) Future direction of agrochemical development for plant disease in China. Food Energy Security 10:e293

    Article  Google Scholar 

  • Hagerty CH, Klein AM, Reardon CL, Kroese DR, Melle CJ, Graber KR, Mundt CC (2021) Baseline and temporal changes in sensitivity of Zymoseptoria tritici isolates to benzovindiflupyr in Oregon, U.S.A., and cross-sensitivity to other SDHI fungicides. Plant Disease 105:169–174

    Article  CAS  PubMed  Google Scholar 

  • Hagiwara H (2019) Modes of action and biological activities of a novel fungicide tolprocarb. Journal of Pesticide Science 44:186–192

    Article  CAS  Google Scholar 

  • Hagiwara H, Ezaki R, Hamada T, Tsuda M, Ebihara K (2019) Development of a novel fungicide, tolprocarb. Journal of Pesticide Science 44:209–213

    Article  Google Scholar 

  • Hagiwara H, Ogura R, Fukumoto T, Ohara T, Tsuda M, Hiratsuka K (2020) Novel bacterial control agent tolprocarb enhances systemic acquired resistance in Arabidopsis and rice as a second mode of action. Journal of General Plant Pathology 86:39–47

    Article  CAS  Google Scholar 

  • Hatamoto M, Aizawa R, Kobayasshi Y, Fujimura M (2019) A novel fungicide aminopyrifen inhibits GWT-1 protein in glycosylphosphatidylinositol-anchor biosynthesis in Neurospora crassa. Pesticide Biochemistry and Physiology 156:1–8

    Article  CAS  PubMed  Google Scholar 

  • Hatamoto M, Aizawa R, Koda K, Fukuchi T (2021) Aminopyrifen, a novel 2-aminonicotinate fungicide with a unique effect and broad-spectrum activity against plant pathogenic fungi. Journal of Pesticide Science 46:198–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He L, Cui K, Song Y, Li T, Liu N, Mu W, Liu F (2020) Activity of the novel succinate dehydrogenase inhibitor fungicide pydiflumetofen against SDHI-sensitive and SDHI-resistant isolates of Botrytis cinerea and efficacy against gray mold. Plant Disease 104:2168–2173

    Article  CAS  PubMed  Google Scholar 

  • Health Canada (2020) Re-evaluation decision RVD2020–12: mancozeb and its associated end-use products. https://publications.gc.ca/collections/collection_2020/sc-hc/h113-28/H113-28-2020-12-eng. Accessed 31 July 2022

  • Heick TM, Matzen N, Jørgensen LN (2020) Reduced field efficacy and sensitivity of demethylation inhibitors in the Danish and Swedish Zymoseptoria tritici populations. European Journal of Plant Pathology 157:625–636

    Article  CAS  Google Scholar 

  • Heinecke M, Rocha LF, Fakhoury AM, Bond JP (2019) Efficacy of fungicides containing mefentrifluconazole to manage Frogeye leaf spot of soybean. Phytopathology 109:S2.63 (abstr.)

  • Helepciuc F-E, Todor A (2022) EU microbial pest control: a revolution in waiting. Pest Management Science 78:1314–1325

    Article  CAS  PubMed  Google Scholar 

  • Higashimura N, Hamada A, Ohara T, Sakurai S, Ito H, Banba S (2022) The target site of the novel fungicide quinofumelin, Pyricularia oryzae class II dihydroorotate dehydrogenase. Journal of Pesticide Science 47:190–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou Y-P, Chen Y-L, Qu X-P, Wang J-X, Zhou M-G (2018a) Effects of a novel SDHI fungicide pyraziflumid on the biology of the plant pathogenic fungi Bipolaris maydis. Pesticide Biochemistry and Physiology 149:20–25

    Article  CAS  PubMed  Google Scholar 

  • Hou Y-P, Chen Y-L, Wu L-Y, Wang J-X, Chen C-J, Zhou M-G (2018b) Baseline sensitivity of Bipolaris maydis to the novel succinate dehydrogenase inhibitor benzovindiflupyr and its efficacy. Pesticide Biochemistry and Physiology 149:81–88

    Article  CAS  PubMed  Google Scholar 

  • Hou Y-P, Mao X-W, Lin S-P, Song X-S, Duan Y-B, Wang J-X, Zhou M-G (2018c) Activity of a novel succinate dehydrogenase inhibitor pyraziflumid against Sclerotinia sclerotiorum. Pesticide Biochemistry and Physiology 145:22–28

    Article  CAS  PubMed  Google Scholar 

  • Hou Y-P, Mao X-W, Wang J-X, Zhan S-W, Zhou M-G (2017) Sensitivity of Fusarium asiaticum to a novel succinate dehydrogenase inhibitor fungicide pydiflumetofen. Crop Protection 96:237–244

    Article  CAS  Google Scholar 

  • Hu M-J, Fernández-Ortuño D, Schnabel G (2016) Monitoring resistance to SDHI fungicides in Botrytis cinerea from strawberry fields. Plant Disease 100:959–965

    Article  CAS  PubMed  Google Scholar 

  • Irish Examiner (2021) EU bans one of the world's most commonly used fungicides - one year to use up banned mancozeb. https://www.irishexaminer.com//farming/arid-40201155.html. Accessed 31 July 2022

  • Ishii H (2011) Fungicide resistance in rice. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern Fungicides and Antifungal Compounds, vol VI. Deutsche Phytomedizinische Gesellschaft. Braunschweig, Germany, pp 35–40

    Google Scholar 

  • Ishii H (2015) Rice pathogens in Japan. In: Ishii H, Hollomon DW (eds) Fungicide Resistance in Plant Pathogens - principles and a guide to practical management. Springer Japan, Tokyo, Japan, pp 341–354

  • Ishii H, Bryson PK, 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 171:104737

    Article  CAS  PubMed  Google Scholar 

  • Ishii H, Fujiwara M, Nishimura K (2019) Systemic resistance inducer acibenzolar-S-methyl (ASM) and its microencapsulated formulations: their long-lasting control efficacy against cucumber diseases and mitigation of phytotoxicity. Pest Management Science 75:801–808

    Article  CAS  PubMed  Google Scholar 

  • Ishii H, Hollomon DW (2015) Fungicide Resistance in Plant Pathogens - principles and a guide to practical management. Springer Japan, Tokyo, Japan, p 490

  • Ishii H, Miyamoto T, Katayose K (2020) Differential pattern of cross resistance to SDHI fungicides and association with sdh gene mutations in Corynespora cassiicola. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds), Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 157-162

  • Ishii H, Miyamoto T, Ushio S, Kakishima (2011) Lack of cross-resistance to a novel succinate dehydrogenase inhibitor, fluopyram, in highly boscalid-resistant isolates of Corynespora cassiicola and Podosphaera xanthii. Pest Management Science 67:474–482

    Article  CAS  PubMed  Google Scholar 

  • Ishii H, Watanabe H, Yamaoka Y, Schnabel G (2022) Sensitivity to fungicides in isolates of Colletotrichum gloeosporioides and C. acutatum species complexes and efficacy against anthracnose diseases. Pesticide Biochemistry and Physiology 182:105049

  • Ishii H, Zhen F, Hu M, Li X, Schnabel G (2016) Efficacy of SDHI fungicides, including benzovindiflupyr, against Colletotrichum species. Pest Management Science 72:1844–1853

    Article  CAS  PubMed  Google Scholar 

  • Ishizaki K (2008) Breeding and practical application of blast-resistant isogenic lines in rice cultivar Koshihikari in Niigata Prefecture. Gamma Field Symposia 47:33–38

    Google Scholar 

  • Ishizaki K (2010) Breeding and practical application of ‘Koshihikari Niigata BL series’ in Niigata Prefecture. Breeding Research 12:160–164 (in Japanese)

    Article  Google Scholar 

  • Jones JG, Korir RC, Walter TL, Everts KL (2020) Reducing chlorothalonil use in fungicide spray programs for powdery mildew, anthracnose, and gummy stem blight in melons. Plant Disease 104:3213–3220

    Article  CAS  PubMed  Google Scholar 

  • Jørgensen LN (2023) Practical disease management in cereals - a historic view, including hurdles with fungicides resistance and a future with more specific IPM. Abstr. 20th Intr. Reinhardsbrunn Symp. - Modern Fungicides and Antifungal Compounds (Deutsche Phytomedizinische Gesellschaft), 9

  • Jørgensen LN, Heick TM (2021) Azole use in agriculture, horticulture, and wood preservation - is it indispensable? Frontiers in Cellular and Infection Microbiology 11:73029

    Article  Google Scholar 

  • Jørgensen LN, Matzen N, Havis N, Holdgate S, Clark B, Blake J, Glazek M, Korbas M, Danielewicz J, Maumene C, Rodemann B, Weigand S, Kildea S, Bataille C, Brauna-Morˇzevska E, Gulbis K, Ban R, Berg G (2020) Efficacy of common azoles and mefentrifluconazole against septoria, brown rust and yellow rust in wheat across Europe. In: Deising HB, Fraaije B, Mehl A, Oerke E, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 27–34

    Google Scholar 

  • Kang SE, Sumabat LG, Melie T, Mangum B, Momany M, Brewer MT (2022) Evidence for the agricultural origin of resistance to multiple antimicrobials in Aspergillus fumigatus, a fungal pathogen of humans. G3 12:jkab427

  • Kapoor M, Moloney M, Soltow QA, Pillar CM, Shawa KJ (2020) Evaluation of resistance development to the Gwt1 inhibitor manogepix (APX001A) in Candida species. Antimicrobial Agents and Chemotherapy 64:e01387-e1419

    CAS  Google Scholar 

  • Keinath (2022) Reduced sensitivity of Pseudoperonospora cubensis clades 1 and 2 to oxathiapiprolin in South Carolina. Plant Health Progress 23:256–259

    Article  Google Scholar 

  • Kikutake K, Furuya T, Hasebe M, Nagai H, Oda M (2020) Development of a novel fungicide, pyraziflumid. Journal of Pesticide Science 45:184–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kildea S, Hellin P, Heick TM, Hutton F (2022) Baseline sensitivity of European Zymoseptoria tritici populations to the complex III respiration inhibitor fenpicoxamid. Pest Management Science 78:4488–4496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klappach K, Stammler G (2019) Resistance of plant pathogens to succinate dehydrogenase inhibitor (SDHI) fungicides (FRAC code 7). In: Stevenson KL, McGrath MT, Wyenandt CA (eds) Fungicide Resistance in North America, 2nd edn. APS Press, St. Paul, Minnesota, pp 85–95

    Chapter  Google Scholar 

  • Knight SC, Stammler G, Torriani SFF (2020) Review of fungicide resistance management in Asia. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 3-12

  • Kurahashi M (2021) Biological activity of a novel fungicide inpyrfluxam. Abstr. 38th Symp. Res. Com. Bioact. Pestic. (Pestic. Sci. Soc. Jpn.), 5–8 (in Japanese)

  • Kuwahara R, Sato M, Kawasaki T, Saiga T (2022) The mode of action of a novel fungicide, Kinoprol®. Abstr. 47th Ann. Meet. Pestic. Sci. Soc. Jpn.: 79 (in Japanese)

  • Lalève A, Fillinger S, Walker A-S (2014a) Fitness measurement reveals contrasting costs in homologous recombinant mutants of Botrytis cinerea resistant to succinate dehydrogenase inhibitors. Fungal Genetics and Biology 67:24–36

    Article  PubMed  Google Scholar 

  • Lalève A, Gamet S, Walker A-S, Debieu D, Toquin V, Fillinger S (2014b) Site-directed mutagenesis of the P225, N230 and H272 residues of succinate dehydrogenase subunit B from Botrytis cinerea highlights different roles in enzyme activity and inhibitor binding. Environmental Microbiology 16:2253–2266

    Article  PubMed  Google Scholar 

  • Lamberth C, Jeanmart S, Luksch T, Plant A (2013) Current challenges and trends in the discovery of agrochemicals. Science 341:742–746

    Article  PubMed  Google Scholar 

  • Lee J, Elliott MR, Kim M, Yamada T, Jung G (2021a) A rapid molecular detection system for SdhB and SdhC point mutations conferring differential succinate dehydrogenase inhibitor resistance in Clarireedia populations. Plant Disease 105:660–666

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Elliott MR, Kim M, Yamada T, Jung G (2021b) Field assessment of six point-mutations in SDH subunit genes conferring varying resistance levels to SDHIs in Clarireedia spp. Plant Disease 105:1685–1691

    Article  CAS  PubMed  Google Scholar 

  • Li T, Li H, Liu T, Zhu J, Zhang L, Mu W, Liu F (2021) Evaluation of the antifungal and biochemical activities of mefentrifluconazole against Botrytis cinerea. Pesticide Biochemistry and Physiology 173:104784

    Article  CAS  PubMed  Google Scholar 

  • Li C, Liu X, Liu Z, Hu S, Xue Z, Fu Y, Miao J, Liu X (2022a) Resistance risk and novel resistance-related point mutations in target protein PiORP1 of fluoxapiprolin in Phytophthora infestans. Journal of Agricultural and Food Chemistry 70:4881–4888

    Article  CAS  PubMed  Google Scholar 

  • Li X, Gao X, Hu S, Hao X, Li G, Chen Y, Liu Z, Li Y, Miao J, Gu B, Liu X (2022b) Resistance to pydiflumetofen in Botrytis cinerea: risk assessment and detection of point mutations in sdh genes that confer resistance. Pest Management Science 78:1448–1456

    Article  CAS  PubMed  Google Scholar 

  • Li X, Yang J, Jiang Q, Tang L, Xue Z, Wang H, Zhao D, Miao J, Liu X (2022c) Baseline sensitivity and control efficacy of a new QiI fungicide, florylpocoxamid, against Botrytis cinerea. Pest Management Science 78:5184–5190

    Article  CAS  PubMed  Google Scholar 

  • Li J-L, Zhou L-M, Gao M-Q, Huang Z-Q, Liu X-L, Zhu X-L, Yang G-F (2020) Design, synthesis, and fungicidal evaluation of novel oxysterol binding protein inhibitors for combatting resistance associated with oxathiapiprolin. Pesticide Biochemistry and Physiology 169:104673

    Article  CAS  PubMed  Google Scholar 

  • Liang X, Zou L, Lian W, Wang M, Yang Y, Zhang Y (2022) Comparative transcriptome analyses reveal conserved and distinct mechanisms of the SDHI fungicide benzovindiflupyr inhibiting Colletotrichum. Phytopathology 112:1255–1263

    Article  CAS  PubMed  Google Scholar 

  • Lynxee consulting (2019) FRANCE: withdrawal of propiconazole-based products. http://lynxee.consulting/en/france-withdrawal-of-propiconazole-based-products/. Accessed 31 July 2022

  • Machida K, Takimoto H, Miyoshi H, Taniguchi M (1999) UK 2A, B, C and D, novel antifungal antibiotics from Streptomyces sp. 517–02. V. Inhibition mechanism of bovine heart mitochondrial cytochrome bc1 by the novel antibiotic UK 2A. Journal of Antibiotics 52:748–753

    Article  CAS  PubMed  Google Scholar 

  • Madak JT, Bankhead III A, Cuthbertson CR, Showalter HD, Neamati N (2019) Revisiting the role of dihydroorotate dehydrogenase as a therapeutic target for cancer. Pharmacology & Therapeutics 195:111–131

    Article  CAS  Google Scholar 

  • Malandrakis AA, Krasagakis N, Kavroulakis N, Ilias A, Tsagkarakou A, Vontas J, Markakis E (2022) Fungicide resistance frequencies of Botrytis cinerea greenhouse isolates and molecular detection of a novel SDHI resistance mutation. Pesticide Biochemistry and Physiology 183:105058

    Article  CAS  PubMed  Google Scholar 

  • Mallik I, Arabiat S, Pasche JS, Bolton MD, Patel JS, Gudmestad NC (2014) Molecular characterization and detection of mutations associated with resistance to succinate dehydrogenase-inhibiting fungicides in Alternaria solani. Phytopathology 104:40–49

    Article  CAS  PubMed  Google Scholar 

  • Massi F, Torriani SFF, Waldner-Zulauf M, Bianco PA, Coatti M, Borsa P, Borghi L, Toffolatti SL (2023) Characterization of Italian Plasmopara viticola populations for resistance to oxathiapiprolin. Pest Management Science 79:1243–1250

    Article  CAS  PubMed  Google Scholar 

  • Matsumura M (2012) Biological activity of tebufloquin and testing methods for sensitivity of Magnaporthe oryzae. Abstr 22nd Symp. Res. Com. Fungic. Resist. (Phytopathol. Soc. Jpn.): 29–38 (in Japanese with English abstr.)

  • Matsuzaki Y, Iwahashi F (2020) Biological profile of metyltetraprole, a new QoI-fungicide: discovery of the tetrazolinone chemical class and in vitro/in vivo analysis of activity against QoI-resistant fungal strains. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 265-270

  • Matsuzaki Y, Uda Y, Harada T, Iwahashi F (2022) Metyltetraprole activity against plant pathogens with relatively rare cytochrome b haplotypes for azoxystrobin resistance. Journal of General Plant Pathology 88:318–324

    Article  CAS  Google Scholar 

  • Matsuzaki Y, Uda Y, Kurahashi M, Iwahashi F (2021) Microtiter plate test using liquid medium in an alternative method for monitoring metyltetraprole sensitivity in Cercospora beticola. Pest Management Science 77:1226–1234

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki Y, Watanabe S, Harada T, Iwahashi F (2020a) Pyridachlometyl has a novel anti-tubulin mode of action which could be useful in anti-resistance management. Pest Management Science 76:1393–1401

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki Y, Yoshimoto Y, Arimori S, Kiguchi S, Harada T, Iwahashi F (2020b) Discovery of metyltetraprole: Identification of tetrazoline pharmacophore to overcome QoI resistance. Bioorganic and Medicinal Chemistry 28:115211

    Article  CAS  PubMed  Google Scholar 

  • Mboup MK, Sweigard JW, Carroll A, Jaworska G, Genet J-L (2022) Genetic mechanism, baseline sensitivity and risk of resistance to oxathiapiprolin in oomycetes. Pest Management Science 78:905–913

    Article  CAS  PubMed  Google Scholar 

  • McGrath MT (2022) Role of broad-spectrum fungicides in managing vegetable diseases and fungicide resistance. Phytopathology 112:S3.201 (abstr.)

  • Mehl A, Schmitz H, Stenzel K, Bloomberg J (2019) DMI fungicides (FRAC code 3): sensitivity status of key target pathogens, field versus laboratory resistance, and resistance mechanisms. In: Stevenson KL, McGrath MT, Wyenandt CA (eds) Fungicide Resistance in North America, 2nd edn. APS Press, St. Paul, Minnesota, pp 51–68

    Chapter  Google Scholar 

  • Miao J, Cai M, Dong X, Liu L, Lin D, Zhang C, Pang Z, Liu X (2016a) Resistance assessment for oxathiapiprolin in Phytophthora capsici and the detection of a point mutation (G769W) in PcORP1 that confers resistance. Frontiers in Microbiology 7:615

    Article  PubMed  PubMed Central  Google Scholar 

  • Miao J, Chi Y, Lin D, Tyler BM, Liu X (2018) Mutations in ORP1 conferring oxathiapiprolin resistance confirmed by genome editing using CRISPR/Cas9 in Phytophthora capsici and P. sojae. Phytopathology 108:1412–1419

    Article  CAS  PubMed  Google Scholar 

  • Miao J, Dong X, Lin D, Wang Q, Liu P, Chen F, Du Y, Liu X (2016b) Activity of the novel fungicide oxathiapiprolin against plant-pathogenic oomycetes. Pesticide Biochemistry and Physiology 72:1572–1577

    CAS  Google Scholar 

  • Miao J, Li C, Liu X, Zhang X, Li G, Xu W, Zhang C, Liu X (2021) Activity and resistance-related point mutations in target protein PcORP1 of fluoxapiprolin in Phytophthora capsici. Journal of Agricultural and Food Chemistry 69:3827–3835

    Article  CAS  PubMed  Google Scholar 

  • Miao J, Liu X, Du X, Li G, Li C, Zhao D, Liu X (2020a) Sensitivity of Pythium spp. and Phytopythium spp. and tolerance mechanism of Pythium spp. to oxathiapiprolin. Pest Management Science 76:3975–3981

    Article  CAS  PubMed  Google Scholar 

  • Miao J, Liu X, Li G, Du X, Liu X (2020b) Multiple point mutations in PcORP1 gene conferring different resistance levels to oxathiapiprolin confirmed using CRISPR-Cas9 in Phytophthora sojae. Pest Management Science 76:2434–2440

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto T, Hayashi K, Okada R, Wari D, Ogawara T (2020) Resistance to succinate dehydrogenase inhibitors in field isolates of Podosphaera xanthii on cucumber: monitoring, cross-resistance patterns and molecular characterization. Pesticide Biochemistry and Physiology 169:104646

    Article  CAS  PubMed  Google Scholar 

  • Motoyama T, Yun C-S, Osada H (2021) Biosynthesis and biological function of secondary metabolites of the rice blast fungus Pyricularia oryzae. Journal of Industrial Microbiology & Biotechnology 48: PMC8788799

  • Mounkoro P, Michel T, Benhachemi R, Surpateanu G, Iorga BI, Fisher N, Meunier B (2019) Mitochondrial complex III Qi-site inhibitor resistance mutations found in laboratory selected mutants and field isolates. Pest Management Science 75:2107–2114

    Article  CAS  PubMed  Google Scholar 

  • Müller MA, Stammler G, May de Mio LL (2021) Multiple resistance to DMI, QoI and SDHI fungicides in field isolates of Phakopsora pachyrhizi. Crop Protection 145:105618

    Article  Google Scholar 

  • Munier-Lehmann H, Vidalain P-O, Tangy F, Janin YL (2013) On dihydroorotate dehydrogenases and their inhibitors and uses. Journal of Medicinal Chemistry 56:3148–3167

    Article  CAS  PubMed  Google Scholar 

  • Nagata T, Yamawaki D, Kogure A, Kaneko I (2018) Studies on a novel fungicide “Dichlobentiazox” - synthesis and biological activity -. Abstr. 43rd Ann. Meet. Pestic. Sci. Soc. Jpn.: 71 (in Japanese)

  • Neves DL, Bradley CA (2019) Baseline sensitivity of Cercospora zeae-maydis to pydiflumetofen, a new succinate dehydrogenase inhibitor fungicide. Crop Protection 119:177–179

    Article  CAS  Google Scholar 

  • Nishino S, Fujii T, Nishimura S, Ogino T (2022) Studies on a novel fungicide, Kinoprol® (MIGIWA®) (2): efficacies of Kinoprol® on fruit tree diseases. Abstr. Ann. Meet. Phytopathol. Soc. Jpn.: 99 (in Japanese)

  • Nishino S, Kuwahara R, Fujii T, Nishino C, Sano H (2021) Studies on a novel fungicide, Kinoprol® (MIGIWA®) (1): control efficacies of Kinoprol® on apple scab. Japanese Journal of Phytopathology 87:197. (Japanese abstr.)

  • Oliveira MS, Cordova LG, Peres NA (2020) Efficacy and baseline sensitivity of succinate-dehydrogenase-inhibitor fungicides for management of Colletotrichum crown rot of strawberry. Plant Disease 104:2860–2865

    Article  CAS  PubMed  Google Scholar 

  • Oliver JD, Sibley GEM, Beckmann N, Dobb KS, Slater MJ, McEntee L, du Pré S, Livermore J, Bromley MJ, Wiederhold NP, Hope WW, Kennedy AJ, Law D, Birth M (2016) F901318 represents a novel class of antifungal drug that inhibits dihydroorotate dehydrogenase. PNAS 113:12809–12814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olkkonen VM (2013) OSBP-related proteins: liganding by glycerophospholipids opens new insight into their function. Molecules 18:13666–13679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owen WJ, Meyer KG, Slanec TJ, Meyer ST, Wang NX, Fitzpatrick GM, Niyaz NN, Nugent J, Ricks MJ, Rogers RB, Yao C (2020) Synthesis and biological activity of analogs of the antifungal antibiotic UK-2A. III. Impact of modifications to the macrocycle isobutyryl ester position. Pest Management Science 76:277–286

    Article  CAS  PubMed  Google Scholar 

  • Owen WJ, Meyer KG, Slanec TJ, Wang NX, Meyer ST, Niyaz NN, Rogers RB, Bravo-Altamirano K, Herrick JL, Yao C (2019) Synthesis and biological activity of analogs of the antifungal antibiotic UK-2A. I. Impact of picolinamide ring replacement. Pest Management Science 75:413–426

    Article  CAS  PubMed  Google Scholar 

  • Owen WJ, Yao C, Myung K, Kemmitt G, Leader A, Meyer KG, Bowling AJ, Slanec T, Kramer VJ (2017) Biological characterization of fenpicoxamid, a new fungicide with utility in cereals and other crops. Pest Management Science 73:2005–2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panon M-L, Steva H, Debuisson D, Descotes A (2018) Efficacite au vignoble de plusieurs preparations fongicides en presence de differents pourcentages de phenotypes resistants AOX de Plamopara viticola. Proc. 12th Intr. Conf, Plant Dis.: 490–498 (in French with English abstr.)

  • Parker MH, Durst GL, Hannum AC, Henry MJ, Lawler LK, Smith AJ (2001) The identification and optimization of oömycete dihydroorotate dehydrogenase inhibitors as fungicides. Synthesis and Chemistry of Agrochemicals VI (American Chemical Society): pp. 303–313

  • Pasteris RJ, Hanagan MA, Bisaha JJ, Finkelstein BL, Hoffman LE, Gregory V, Andreassi JL, Sweigard JA, Klyashchitsky BA, Henry YT, Berger RA (2016) Discovery of oxathiapiprolin, a new oomycete fungicide that targets an oxysterol binding protein. Bioorganic & Medicinal Chemistry 24:354–361

    Article  CAS  Google Scholar 

  • Perotin B, Pierre S, Shepherd C, Summers B, Salas B, Majeau G (2015) ZorvecTM (oxathiapiplolin), a new fungicide from DuPont de Nemours against Oomycetes. Proc. 11th Intr. Conf, Plant Dis.: 463–472

  • Phillips MWA (2020) Agrochemical industry development, trend in R&D and the impact of regulation. Pest Management Science 76:3348–3356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Portz K, Casanova F, Jordine A, Bohnert S, Mehl A, Portz D, Schaffrath U (2021) Wheat blast caused by Magnaporthe oryzae pathovar Triticum is effectively controlled by the plant defence inducer isotianil. Journal of Plant Diseases and Protection 128:249–259

    Article  CAS  Google Scholar 

  • Purnhagen KP, Clemens S, Eriksson D, Fresco LO, Tosun J, Qaim M, Visser RGF, Weber APM, Wesseler JHH, Zilberman D (2021) Europe’s farm to fork strategy and its commitment to biotechnology and organic farming: conflicting or complementary goals? Trends in Plant Science 26:600–606

    Article  CAS  PubMed  Google Scholar 

  • Sang H, Lee HB (2020) Molecular mechanisms of succinate dehydrogenase inhibitor resistance in phytopathogenic fungi. Research in Plant Disease 26:1–7

    Article  CAS  Google Scholar 

  • Sautua FJ, Carmona MA (2022) Baseline sensitivity of QoI-resistant isolates of Pyrenophora tritici-repentis from Argentina to fenpicoxamid. European Journal of Plant Pathology 164:583–591

    Article  CAS  Google Scholar 

  • Shao W, Sun J, Zhang X, Chen C (2020) Amino acid polymorphism in succinate dehydrogenase subunit C involved in biological fitness of Botrytis cinerea. Molecular Plant-Microbe Interactions 33:580–589

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Sun B, Xie X, Chai A, Li L, Li B (2021) Site-directed mutagenesis of the succinate dehydrogenase subunits B and D from Corynespora cassiicola reveals different fitness costs and sensitivities to succinate dehydrogenase inhibitors. Environmental Microbiology 23:5769–5783

    Article  CAS  PubMed  Google Scholar 

  • Sierotzki H (2015) Respiration inhibitors: complex III. In: Ishii H, Hollomon DW (eds) Fungicide resistance in plant pathogens - principles and a guide to practical management. Springer Japan, Tokyo, Japan, pp 119–143

  • Sierotzki H, Scalliet G (2013) A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology 103:880–887

    Article  CAS  PubMed  Google Scholar 

  • Sierotzki H, Stammler G (2019) Resistance of plant pathogens to QoI fungicides (FRAC Code 11). In: Stevenson KL, McGrath MT, Wyenandt CA (eds) Fungicide Resistance in North America, 2nd edn. APS Press, St. Paul, Minnesota, pp 97–113

    Chapter  Google Scholar 

  • Simões K, Hawlik A, Rehfus A, Gava F, Stammler G (2018) First detection of a SDH variant with reduced SDHI sensitivity in Phakopsora pachyrhizi. Journal of Plant Diseases and Protection 125:21–26

    Article  Google Scholar 

  • Stammler G, Wolf A, Glaettli A, Klappach K (2015) Respiration inhibitors: complex II. In: Ishii H, Hollomon DW (eds) Fungicide Resistance in Plant Pathogens - principles and a guide to practical management. Springer Japan, Tokyo, Japan, pp 105–117

  • Strobel D, Bryson R, Semar M, Stammler G, Kienle M, Smith J (2020) Mefentrifluconazole (REVYSOL®) - the first isopropanol-azole. In: Deising HB; Fraaije B; Mehl A; Oerke EC; Sierotzki H; Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp. 259-264

  • Suemoto H, Matsuzaki Y, Iwahashi F (2019) Metyltetraprole a novel putative complex III inhibitor, targets known QoI-resistant strains of Zymoseptoria tritici and Pyrenophora teres. Pest Management Science 75:1181–1189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun H-Y, Cui J-h, Tian B-h, Cao S-l, Zhang X-x, Chen H-G (2020) Resistance risk assessment for Fusarium graminearum to pydiflumetofen, a new succinate dehydrogenase inhibitor. Pest Management Science 76:1549–1559

    Article  CAS  PubMed  Google Scholar 

  • Takagaki M (2015) Melanin biosynthesis inhibitors. In: Ishii H, Hollomon DW (eds) Fungicide Resistance in Plant Pathogens - principles and a guide to practical management. Springer Japan, Tokyo, Japan, pp 175–180

  • Tao X, Zhao H, Xu H, Li Z, Wang J, Song X, Zhou M, Duan Y (2021) Antifungal activity and biological characteristics of the novel fungicide quinofumelin against Sclerotinia sclerotioum. Plant Disease 105:2567–2574

    Article  CAS  PubMed  Google Scholar 

  • Taxvig C, Hass U, Axelstad M, Dalgaard M, Boberg J, Andeasen HR, Vinggaard AM (2007) Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicological Sciences 100:464–473

    Article  CAS  PubMed  Google Scholar 

  • Taxvig C, Vinggaard AM, Hass U, Axelstad M, Metzdorff S, Nellemann C (2008) Endocrine-disrupting properties in vivo of widely used azole fungicides. International Journal of Andrology 31:170–177

    Article  CAS  PubMed  Google Scholar 

  • Terada M, Kogure A, Kaneko I, Kawai K, Ozaki K (2019) Studies on a novel fungicide Dichlobentiazox (3) - analysis of the mode of action. Japanese Journal of Phytopathology 85:275–276. (Japanese abstr.)

  • Terada M, Kogure A, Kaneko I, Ozaki K (2018) The efficacy of a novel fungicide “Dichlobentiazox” on rice blast. Abstr. 43rd Ann. Meet. Pestic. Sci. Soc. Jpn.: 72 (in Japanese)

  • Tesh SA, Tesh JM, Fegert I, Buesen R, Schneider S, Mentzel T, van Ravenzwaay B, Stinchcombe S (2019) Innovative selection approach for a new antifungal agent mefentrifluconazole (Revysol®) and the impact upon its toxicity profile. Regulatory Toxicology and Phamacology 106:152–168

    Article  CAS  Google Scholar 

  • Thind TS (2012) Fungicide Resistance in Crop Protection - risk and management. CAB International (CABI), Wallingford, UK, p 284

  • Thind TS, Hollomon DW (2018) Thiocarbamate fungicides: reliable tools in resistance management and future outlook. Pest Management Science 74:1547–1551

    Article  CAS  PubMed  Google Scholar 

  • Tsukuda S (2014) Developing trend of SDHI fungicide and studies on a novel fungicide, isofetamid. Japenese Journal of Pesticide Science 39:89–95 ((in Japanese))

    CAS  Google Scholar 

  • Ueki M, Abe K, Hanafi K, Shibata K, Tanaka T, Taniguchi M (1996) UK 2A, B, C and D, a novel antifungal antibiotics from Streptomyces sp, 517–02. I. Fermentation, isolation and biological properties. The Journal of Antibiotics 49:639–643

    Article  CAS  PubMed  Google Scholar 

  • Ueki M, Taniguchi M (1997) The mode of action of UK 2A and UK-3A, novel antifungal antibiotics from Streptomyces sp, 517–02. Journal of Antibiotics 50:1052–1057

    Article  CAS  PubMed  Google Scholar 

  • Umetsu N, Shirai Y (2020) Development of novel pesticides in the 21 century. Journal of Pesticide Science 45:54–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uppala LS, Marrano A, Moyers B (2020) Evaluation of chlorothalonil alternative fungicide regimes for cranberry fruit rot and quality: traditional methods vs high-throughput image analysis. Phytopathology 110:S2.87 (abstr.)

  • Veloukas T, Karaoglanidis GS (2012) Biological activity of the succinate dehydrogenase inhibitor fluopyram against Botrytis cinerea and fungal baseline sensitivity. Pest Management Science 68:858–864

    Article  CAS  PubMed  Google Scholar 

  • Veloukas T, Markoglou AN, Karaoglanidis GS (2013) Differential effect of SdhB gene mutations on the sensitivity to SDHI fungicides in Botrytis cinerea. Plant Disease 97:118–122

    Article  CAS  PubMed  Google Scholar 

  • Verweij PE, Arendrup MC, Alastruey-Izquierdo A, Gold JAW, Lockhart SR, Chiller T, White PL (2022) Dual use of antifungals in medicine and agriculture: how do we help prevent resistance developing in human pathogens. Drug Resistance Updates 65:100885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verweij PE, Lucas JA, Arendrup MC, Bowyer P, Brinkmann AJF, Denning DW, Dyer PS, Fisher MC, Geenen PL, Gisi U, Hermann D, Hoogendijk A, Kiers E, Lagrou K, Melchers WJG, Rhodes J, Rietveld AG, Schoustra SE, Stenzel K, Zwaan BJ, Fraaije BA (2020) The one health problem of azole resistance in Aspergillus fumigatus: current insights and future research agenda. Fungal Biology Reviews 34:202–214

    Article  Google Scholar 

  • Vielba-Fernández A, Polonio Á, Ruiz-Jiménez L, de Vicente A, Pérez-García A, Fernández-Ortuño D (2021) Resistance to the SDHI fungicides boscalid and fluopyram in Podosphaera xanthii populations from commercial cucurbit fields in Spain. Journal of Fungi 7:733

    Article  PubMed  PubMed Central  Google Scholar 

  • Walker A-S, Micoud A, Rémuson F, Grosman J, Gredt M, Leroux P (2013) French vineyards provide information that opens ways for effective resistance management of Botrytis cinerea (grey mould). Pest Management Science 69:667–678

    Article  CAS  PubMed  Google Scholar 

  • Watanabe S (2017) Fungicidal properties and sensitivity analysis of picarbutrazox. Abstr. 27th Symp. Res. Com. Fungic. Resist. (Phytopathol. Soc. Jpn.): 30–37 (in Japanese with English abstr.)

  • Watanabe S, Iwakawa J, Sakai R, Iwahashi F (2020a) Studies on a novel fungicide, inpyrfluxam (1) -biological profile of inpyrfluxam. Japanese Journal of Phytopathology 86:202 (Japanese abstr.)

  • Watanabe S, Matsuzaki Y, Sakaguchi H, Iwahashi F, Kawanaka H, Matsunaga T, Kondo M, Tabuchi M (2020b) Research and development of a novel fungicide, inpyrfluxam. Sumitomo Kagaku (English edition) Report 1, 1–14

  • Weber RWS, Entrop A-P, Coertz A, Mehl A (2015) Status of sensitivity of northern German Botrytis populations to the new SDHI fungicide fluopyram prior to its release as a commercial fungicide. Journal of Plant Diseases and Protection 122:81–90

    Article  Google Scholar 

  • Xiu Q, Bi L, Xu H, Lo T, Zhou Z, Li Z, Wang J, Duan Y, Zhou M (2021) Antifungal activity of quinofumelin against Fusarium graminearum and its inhibitory effect on DON biosynthesis. Toxins 13:348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao C, Meyer KG, Gallup C, Bowling AJ, Hufnagl A, Myung K, Lutz J, Slanec T, Pence HE, Delgado J, Wang NX (2021) Florylpicoxamid, a new picolinamide fungicide with broad spectrum activity. Pest Management Science 77:4483–4496

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto Y, Arimori S (2020) Discovery of Pavecto® - a new QoI fungicide. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 277-278

  • Young D, Kemmitt G, Leader A (2020) Fenpicoxamid provides a new target site for control of Septoria leaf blotch in cereals. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds. Vol. IX, Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 279-284

  • Young DH, Meunier B, Wang NX (2022) Interaction of picolinamide fungicide primary metabolites UK-2A and CAS-649 with the cytochtome bc1 complex Qi site: mutation effects and modelling in Saccharomyces cerevisiae. Pest Management Science 78:2657–2666

    Article  CAS  PubMed  Google Scholar 

  • Young DH, Wang NX, Meyer ST, Avila-Adame C (2018) Characterization of the mechanism of action of the fungicide fenpicoxamid and its metabolite UK-2A. Pest Management Science 74:489–498

    Article  CAS  PubMed  Google Scholar 

  • Zeng L, Luo R, Chen Q, Hao G, Zhu X, Yang G (2022) Discovery of fungicide flubeneteram. Chinese J Pestic Sci 24:895–903 (in Chinese with English abstr.)

    Google Scholar 

  • Zhang C, Imran M, Liu M, Li Z, Gao H, Duan H, Zhou S, Liu X (2020) Two point mutations on CYP51 combined with induced expression of the target gene appeared to mediate pyrisoxazole resistance in Botrytis cinerea. Frontiers in Microbiology 11:1396

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Wu J, Lu F, Bi Q, Yang K, Han X, Wang W (2022) Baseline-sensitivity of Botrytis cinerea to pydiflumetofen and its efficacy on tomato gray mold in Hebei Province, China. Crop Protection 158:105989

    Article  CAS  Google Scholar 

  • Zhou F, Cui YX, Ma YH, Wang JY, Hu HY, Li SW, Zhang FL, Li C-W (2021a) Investigating the potential mechanism of pydiflumetofen resistance in Sclerotinia sclerotiorum. Plant Disease 105:3580–3585

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Tao L, Zhou X, Zuo Z, Gong J, Liu X, Zhou Y, Liu C, Sang N, Liu H, Zou J, Gou K, Yang X, Zhao Y (2021b) DHODH and cancer: promising prospects to be explored. Cancer & Metabolism 9:22

    Article  Google Scholar 

  • Zhu J, Li J, Ma D, Gao Y, Cheng J, Mu W, Li B, Liu F (2022) SDH mutations confer complex cross-resistance patterns to SDHIs in Corynespora cassiicola. Pesticide Biochemistry and Physiology 186:105157

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Li X, Zhang L, Gao Y, Mu W, Liu F (2021) The bioactivity and efficacy of benzovindiflupyr against Corynespora cassiicola, the causal agent of cucumber Corynespora leaf spot. Plant Disease 105:3201–3207

    Article  CAS  PubMed  Google Scholar 

  • Zito R, Meyer L, Aumont C, Fehr M, Stammler G (2020) State of knowledge on molecular mechanisms leading to a reduced sensitivity of P. viticola towards ametoctradin and complex III inhibitors. In: Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (eds) Modern Fungicides and Antifungal Compounds, vol IX. Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 117–118

    Google Scholar 

  • Zuniga AI, Oliveira MS, Rebello CS, Peres NA (2020) Baseline sensitivity of Botrytis cinerea isolates from strawberry to isofetamid compared to other SDHIs. Plant Disease 104:1224–1230

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Hideo Ishii.

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Ishii, H. New chemical fungicides in relation to risk for resistance development. Trop. plant pathol. 49, 18–35 (2024). https://doi.org/10.1007/s40858-023-00596-3

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