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Fenpyroximate resistance in Iranian populations of the European red mite Panonychus ulmi (Acari: Tetranychidae)

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Abstract

The European red mite, Panonychus ulmi (Koch), is one of the most important apple orchard pests worldwide. Fenpyroximate, a mitochondrial electron transport inhibitor of complex I (METI-I), is a commonly used acaricide to control this pest. In this study, we determined fenpyroximate resistance levels for 11 P. ulmi populations from Iran and a spirodiclofen-resistant strain from Germany (PSR-TK). The LC50 values ranged between 121.8 and 5713.9 mg a.i. L−1 and the highest resistance ratio (RR) was 47-fold for the Padena population. PBO, TPP and DEM synergist ratios (SRs) were the highest for the PSR-TK (SR = 6.7), Shahin Dej (SR = 6.1) and Semirom3 (SR = 3.6) populations, respectively. In vitro enzyme activity measurements also showed that there was a higher glutathione S-transferases (GSTs) activity in the PSR-TK and Shahin Dej population compared to the most susceptible populations, whereas the esterase and P450 monooxygenase activity were not significantly higher in the resistant populations. Last, we screened all populations for the presence of two mutations previously associated with METI-I resistance in spider mites but none of these mutations could be detected. To conclude, moderate to high levels of fenpyroximate resistance were observed in P. ulmi populations from Iran, with increased detoxification most likely underlying fenpyroximate resistance.

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References

  • Alavijeh ES, Khajehali J, Snoeck S et al (2020) Molecular and genetic analysis of resistance to METI-I acaricides in Iranian populations of the citrus red mite Panonychus citri. Pestic Biochem Physiol 164:73–84

    Article  CAS  PubMed  Google Scholar 

  • Allocati N, Masulli M, Di Ilio C, Federici L (2018) Glutathione transferases: substrates, inhibitors and pro-drugs in cancer and neurodegenerative diseases. Oncogenesis 7:1–15

    Article  CAS  Google Scholar 

  • Arbabi M, Kamali H, Shahrokhi MR (2004) Evaluating fenazaquin 20% SC new acaricide against Panonychus ulmi Koch in apple orchards of Chenaran of Mashad. Agron Hortic 16:51–56

    Google Scholar 

  • Badieinia F, Khajehali J, Nauen R et al (2020) Metabolic mechanisms of resistance to spirodiclofen and spiromesifen in Iranian populations of Panonychus ulmi. Crop Prot 134:105166. https://doi.org/10.1016/j.cropro.2020.105166

    Article  CAS  Google Scholar 

  • Bajda S, Dermauw W, Panteleri R et al (2017) A mutation in the PSST homologue of complex I (NADH: ubiquinone oxidoreductase) from Tetranychus urticae is associated with resistance to METI acaricides. Insect Biochem Mol Biol 80:79–90. https://doi.org/10.1016/j.ibmb.2016.11.010

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3

    Article  CAS  PubMed  Google Scholar 

  • Devine GJ, Barber M, Denholm I (2001) Incidence and inheritance of resistance to METI-acaricides in European strains of the two‐spotted spider mite (Tetranychus urticae) (Acari: Tetranychidae). Pest Manag Sci 57:443–448. https://doi.org/10.1002/ps.307

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Herron GA, Rophail J (1998) Tebufenpyrad (Pyranica®) resistance detected in two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) from apples in Western Australia. Exp Appl Acarol 22:633–641. https://doi.org/10.1023/A:1006058705429

    Article  CAS  Google Scholar 

  • Hirata K, Kudo M, Igarasgi H (1995) Development of a new acaricide, pyridaben. J Pestic Sci 20:213–221

    Article  Google Scholar 

  • Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, Berkeley

    Google Scholar 

  • Khalighi M, Tirry L, Van Leeuwen T (2014) Cross-resistance risk of the novel complex II inhibitors cyenopyrafen and cyflumetofen in resistant strains of the two‐spotted spider mite Tetranychus urticae. Pest Manag Sci 70:365–368

    Article  CAS  PubMed  Google Scholar 

  • Khalighi M, Dermauw W, Wybouw N et al (2016) Molecular analysis of cyenopyrafen resistance in the two-spotted spider mite Tetranychus urticae. Pest Manag Sci 72:103–112. https://doi.org/10.1002/ps.4071

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Lee S, Lee S, Ahn Y (2004) Fenpyroximate resistance in Tetranychus urticae (Acari: Tetranychidae): cross-resistance and biochemical resistance mechanisms. Pest Manag Sci 60:1001–1006. https://doi.org/10.1002/ps.909

    Article  CAS  PubMed  Google Scholar 

  • Konno T, Kuriyama K, Hamaguchi H (1990) Fenpyroximate (NNI-850), a new acaricide. In: Brighton crop protection conference, pests and diseases-1990, vol 1, pp 71–78

  • Kramer T, Nauen R (2011) Monitoring of spirodiclofen susceptibility in field populations of European red mites, Panonychus ulmi (Koch) (Acari: Tetranychidae), and the cross-resistance pattern of a laboratory‐selected strain. Pest Manag Sci 67:1285–1293

    Article  CAS  PubMed  Google Scholar 

  • Kumral NA, Kovanci B (2007) Susceptibility of female populations of Panonychus ulmi (Koch) (Acari: Tetranychidae) to some acaricides in apple orchards. J Pest Sci (2004) 80:131–137. https://doi.org/10.1007/s10340-007-0163-z

    Article  Google Scholar 

  • Motoba K, Nishizawa H, Suzuki T et al (2000) Species-specific detoxification metabolism of fenpyroximate, a potent acaricide. Pestic Biochem Physiol 67:73–84

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Na N, Guo H, Zhang S et al (2009) In vitro and in vivo acute toxicity of fenpyroximate to flounder Paralichthys olivaceus and its gill cell line FG. Aquat Toxicol 92:76–85

    Article  CAS  PubMed  Google Scholar 

  • Nauen R, Stumpf N, Elbert A et al (2001) Acaricide toxicity and resistance in larvae of different strains of Tetranychus urticae and Panonychus ulmi (Acari: Tetranychidae). Pest Manag Sci 57:253–261. https://doi.org/10.1002/ps.280

    Article  CAS  PubMed  Google Scholar 

  • Nourbakhsh S (2019) List of important pests, diseases and weeds of major agricultural crops, pesticides and recommended methods for their control. Ministry of Jihad-e-Agriculture, Plant Protection Organization, Iran

  • Ozawa A (1994) Acaricides susceptibility of Kanzawa spider mite, Tetranychus kanzawai KISHIDA (Acarina; Tetranychidae) collected from tea fields in Chuuen and Ogasa District in Shizuoka Prefecture. Chagyo Kenkyu Hokoku (Tea Res J) 1994:1–14. https://doi.org/10.5979/cha.1994.1

    Article  Google Scholar 

  • Rameshgar F, Khajehali J, Nauen R et al (2019a) Characterization of abamectin resistance in Iranian populations of European red mite, Panonychus ulmi Koch (Acari: Tetranychidae). Crop Prot 125:104903

    Article  CAS  Google Scholar 

  • Rameshgar F, Khajehali J, Nauen R et al (2019b) Point mutations in the voltage-gated sodium channel gene associated with pyrethroid resistance in Iranian populations of the European red mite Panonychus ulmi. Pestic Biochem Physiol 157:80–87

    Article  CAS  PubMed  Google Scholar 

  • Riga M, Myridakis A, Tsakireli D et al (2015) Functional characterization of the Tetranychus urticae CYP392A11, a cytochrome P450 that hydroxylates the METI acaricides cyenopyrafen and fenpyroximate. Insect Biochem Mol Biol 65:91–99. https://doi.org/10.1016/j.ibmb.2015.09.004

    Article  CAS  PubMed  Google Scholar 

  • Robertson JL, Jones MM, Olguin E, Alberts B (2017) Bioassays with arthropods. CRC Press, Boca Raton

    Book  Google Scholar 

  • Sato ME, Miyata T, Da Silva M et al (2004) Selections for fenpyroximate resistance and susceptibility, and inheritance, cross-resistance and stability of fenpyroximate resistance in Tetranychus urticae Koch (Acari: Tetranychidae). Appl Entomol Zool 39:293–302

    Article  CAS  Google Scholar 

  • Sherer TB, Richardson JR, Testa CM et al (2007) Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson’s disease. J Neurochem 100:1469–1479. https://doi.org/10.1111/j.1471-4159.2006.04333.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snoeck S, Kurlovs AH, Bajda S et al (2019) High-resolution QTL mapping in Tetranychus urticae reveals acaricide-specific responses and common target-site resistance after selection by different METI-I acaricides. Insect Biochem Mol Biol 110:19–33. https://doi.org/10.1016/j.ibmb.2019.04.011

    Article  CAS  PubMed  Google Scholar 

  • Sparks TC, Nauen R (2015) IRAC: mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128

    Article  CAS  PubMed  Google Scholar 

  • Stumpf N, Nauen R (2001) Cross-resistance, inheritance, and biochemistry of mitochondrial electron transport inhibitor-acaricide resistance in Tetranychus urticae (Acari: Tetranychidae). J Econ Entomol 94:1577–1583. https://doi.org/10.1603/0022-0493-94.6.1577

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto N, Osakabe M (2014) Cross-resistance between cyenopyrafen and pyridaben in the two spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Pest Manag Sci 70:1090–1096. https://doi.org/10.1002/ps.3652

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Stillatus V, Tirry L (2004) Genetic analysis and cross-resistance spectrum of a laboratory-selected chlorfenapyr resistant strain of two-spotted spider mite (Acari: Tetranychidae). Exp Appl Acarol 32:249

    Article  PubMed  Google Scholar 

  • Van Leeuwen T, Van Pottelberge S, Tirry L (2006) Biochemical analysis of a chlorfenapyr-selected resistant strain of Tetranychus urticae Koch. Pest Manag Sci 62:425–433

    Article  PubMed  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A et al (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572

    Article  PubMed  Google Scholar 

  • Van Leeuwen T, Dermauw W, Grbic M et al (2013) Spider mite control and resistance management: does a genome help? Pest Manag Sci 69:156–159

    Article  PubMed  Google Scholar 

  • Van Leeuwen T, Tirry L, Yamamoto A et al (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Physiol 121:12–21. https://doi.org/10.1016/j.pestbp.2014.12.009

    Article  CAS  PubMed  Google Scholar 

  • Van Pottelberge S, Van Leeuwen T, Nauen R, Tirry L (2009) Resistance mechanisms to mitochondrial electron transport inhibitors in a field-collected strain of Tetranychus urticae Koch (Acari: Tetranychidae). Bull Entomol Res 99:23–31. https://doi.org/10.1017/S0007485308006081

    Article  CAS  PubMed  Google Scholar 

  • Vontas JG, Small GJ, Hemingway J (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357:65–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • William GB, Janet C (1997) Heme peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. J Am Mosq Control Assoc 13:233–237

    Google Scholar 

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Acknowledgements

The authors are grateful for financial support of this work by the Research Council of Isfahan University of Technology.

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Correspondence to Jahangir Khajehali or Thomas Van Leeuwen.

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Yaghoobi, R., Khajehali, J., Alavijeh, E.S. et al. Fenpyroximate resistance in Iranian populations of the European red mite Panonychus ulmi (Acari: Tetranychidae). Exp Appl Acarol 83, 69–79 (2021). https://doi.org/10.1007/s10493-020-00569-0

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