Skip to main content
Log in

Resistance risk assessment of the novel complex II inhibitor pyflubumide in the polyphagous pest Tetranychus urticae

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Pyflubumide is a novel selective carboxanilide acaricide that inhibits mitochondrial complex II of spider mite species such as Tetranychus urticae. We explored the baseline toxicity and potential cross-resistance risk of pyflubumide in a reference panel of T. urticae strains resistant to various acaricides with different modes of action. A cyenopyrafen-resistant strain (JPR) was identified as the only strain with low-to-moderate level of cross-resistance to pyflubumide (LC50 = 49.07 mg/L). In a resistance risk assessment approach, JPR was subsequently selected which led to two highly resistant strains JPR-R1 (RR = 466.7) and JPR-R2 (RR = 614.8). Interestingly, compared to adult females, resistance was much less pronounced in adult males and eggs of the two JPR-R strains. In order to elucidate resistance mechanisms, we first sequenced the complex II subunits in susceptible and resistant strains, but target-site insensitivity could not be detected. In contrast, synergism/antagonism experiments strongly suggested that cytochrome P450 monooxygenases are involved in pyflubumide resistance. We therefore conducted genome-wide gene expression experiments to investigate constitutive and induced expression patterns and documented the overexpression of five cytochrome P450 and four carboxyl/choline esterase genes in the JPR-R strains after pyflubumide exposure. Together, we provide a first resistance risk assessment of a novel complex II inhibitor and provide first evidence for metabolic resistance mediated by cytochrome P450s in T. urticae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Asahara M, Uesugi R, Osakabe M (2008) Linkage between one of the polygenic hexythiazox resistance genes and an etoxazole resistance gene in the twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 101:1704–1710

    Article  CAS  PubMed  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 Prot 29:643–651

    Article  CAS  Google Scholar 

  • Baker BS, Gorman M, Marin I (1994) Dosage compensation in Drosophila. Annu Rev Genet 28:491–521

    Article  CAS  PubMed  Google Scholar 

  • Carrière Y (2003) Haplodiploidy, sex, and the evolution of pesticide resistance. J Econ Entomol 96:1626–1640

    Article  PubMed  Google Scholar 

  • Daly JG, Fitt GP (1990) Monitoring for pyrethroid resistance in relation to body weight in adult Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Econ Entomol 83:705–709

    Article  Google Scholar 

  • Demaeght P, Dermauw W, Tsakireli D, Khajehali J, Nauen R, Tirry L, Vontas J, Lümmen P, Van Leeuwen T (2013) Molecular analysis of resistance to acaricidal spirocyclic tetronic acids in Tetranychus urticae: CYP392E10 metabolizes spirodiclofen, but not its corresponding enol. Insect Biochem Mol Biol 43:544–554

    Article  CAS  PubMed  Google Scholar 

  • Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbic M, Clark RM, Feyereisen R, Van Leeuwen T (2013) A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc Natl Acad Sci USA 110:E113–E122

    Article  CAS  PubMed  Google Scholar 

  • Fotoukkiaii SM, Tan Z, Xue W, Wybouw N, Van Leeuwen T (2019) Identification and characterization of new mutations in mitochondrial cytochrome b that confer resistance to bifenazate and acequinocyl in the spider mite Tetranychus urticae. Pest Manag Sci. https://doi.org/10.1002/ps.5628

    Article  PubMed  Google Scholar 

  • Furuya T, Suwa A, Nakano M, Fujioka S, Yasokawa N, Machiya K (2015) Synthesis and biological activity of a novel acaricide, pyflubumide. J Pestic Sci 40(2):38–43. https://doi.org/10.1584/jpestics.D14-087

    Article  CAS  Google Scholar 

  • Furuya T, Machiya K, Fujioka S, Nakano M, Inagaki K (2017) Development of a novel acaricide, pyflubumide. J Pestic Sci 42:132–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Ngoc PCT, Ortego F (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hahn M (2014) The rising threat of fungicide resistance in plant pathogenic fungi: botrytis as a case study. J Chem Biol 7:133–141

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeppson L, Keifer H, Baker E (1975) Mites injurious to economic plants. University of California Press, Los Angeles

    Google Scholar 

  • Kauffmann A, Gentleman R, Huber W (2008) arrayQualityMetrics—a bioconductor package for quality assessment of microarray data. Bioinformatics 25:415–416

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Khajehali J, Van Leeuwen T, Tirry L (2009) Susceptibility of an organophosphate resistant strain of the two-spotted spider mite (Tetranychus urticae) to mixtures of bifenazate with organophosphate and carbamate insecticides. Exp Appl Acarol 49:185–192

    Article  CAS  PubMed  Google Scholar 

  • Khajehali J, Van Nieuwenhuyse P, Demaeght P, Tirry L, Van Leeuwen T (2011) Acaricide resistance and resistance mechanisms in Tetranychus urticae populations from rose greenhouses in the Netherlands. Pest Manag Sci 67:1424–1433

    Article  CAS  PubMed  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, Bajda S, Osakabe M, Tirry L, Van Leeuwen T (2016) Molecular analysis of cyenopyrafen resistance in the two-spotted spider mite Tetranychus urticae. Pest Manag Sci 72:103–112

    Article  CAS  PubMed  Google Scholar 

  • Kurlovs AH, Snoeck S, Kosterlitz O, Van Leeuwen T, Clark RM (2019) Trait mapping in diverse arthropods by bulked segregant analysis. Curr Opin Insect Sci 36:57–65

    Article  PubMed  Google Scholar 

  • Marín I, Siegal ML, Baker BS (2000) The evolution of dosage-compensation mechanisms. BioEssays 22:1106–1114

    Article  PubMed  Google Scholar 

  • Nakano M, Yasokawa N, Suwa A, Fujioka S, Furuya T, Sakata K (2015) Mode of action of novel acaricide pyflubumide: effects on the mitochondrial respiratory chain. J Pestic Sci 40:19–24

    Article  CAS  Google Scholar 

  • Nauen R, Elbert A, McCaffery A, Slater R, Sparks TC (2012) IRAC: insecticide resistance, and mode of action classification of insecticides. Modern Crop Prot Compd 1:935–955

    Google Scholar 

  • Oliver RP (2014) A reassessment of the risk of rust fungi developing resistance to fungicides. Pest Manag Sci 70:1641–1645

    Article  CAS  PubMed  Google Scholar 

  • Rao S, Padmaja M (1992) Mammalian-type dosage compensation mechanism in an insect—Gryllotalpa fossor (Scudder)—Orthoptera. J Biosci 17:253–273

    Article  Google Scholar 

  • Rathman R, Johnson M, Rosenheim J, Tabashnik B, Purcell M (1992) Sexual differences in insecticide susceptibility and synergism with piperonyl butoxide in the leafminer parasitoid Diglyphus begini (Hymenoptera: Eulophidae). J Econ Entomol 85:15–20

    Article  CAS  Google Scholar 

  • Riga M, Tsakireli D, Ilias A, Morou E, Myridakis A, Stephanou E, Nauen R, Dermauw W, Van Leeuwen T, Paine M (2014) Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae. Insect Biochem Mol Biol 46:43–53

    Article  CAS  PubMed  Google Scholar 

  • Riga M, Bajda S, Themistokleous C, Papadaki S, Palzewicz M, Dermauw W, Vontas J, Van Leeuwen T (2017) The relative contribution of target-site mutations in complex acaricide resistant phenotypes as assessed by marker assisted backcrossing in Tetranychus urticae. Sci Rep 7:9202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23:2700–2707

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Smyth GK, Altman NS (2013) Separate-channel analysis of two-channel microarrays: recovering inter-spot information. BMC Bioinform 14:165

    Article  Google Scholar 

  • Smyth Gordon K (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:1–25

    Google Scholar 

  • Snoeck S, Wybouw N, Van Leeuwen T, Dermauw W (2018) Transcriptomic plasticity in the arthropod generalist Tetranychus urticae upon long-term acclimation to different host plants. G3 (Bethesda) 8:3865–3879

    CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto N, Osakabe M (2014) Cross-resistance between cyenopyrafen and pyridaben in the twospotted spider mite Tetranychus urticae (Acari: Tetranychidae). Pest Manag Sci 70:1090–1096

    Article  CAS  PubMed  Google Scholar 

  • Team RC (2018) R Foundation for Statistical Computing; Vienna. Austria 2014:2013

    Google Scholar 

  • Tibshirani R, Walther G, Hastie T (2001) Estimating the number of clusters in a data set via the gap statistic. J R Stat Soc Ser B (Stat Methodol) 63:411–423

    Article  Google Scholar 

  • Vacante V (2015) The handbook of mites of economic plants: identification, bio-ecology and control. CAB International, London, p 872

    Google Scholar 

  • Van Leeuwen T, Dermauw W (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annu Rev Entomol 61:475–498

    Article  PubMed  CAS  Google Scholar 

  • Van Leeuwen T, Van Pottelberge S, Tirry L (2005) Comparative acaricide susceptibility and detoxifying enzyme activities in field-collected resistant and susceptible strains of Tetranychus urticae. Pest Manag Sci Form Pestic Sci 61:499–507

    Article  CAS  Google Scholar 

  • Van Leeuwen T, Tirry L, Nauen R (2006) Complete maternal inheritance of bifenazate resistance in Tetranychus urticae Koch (Acari: Tetranychidae) and its implications in mode of action considerations. Insect Biochem Mol Biol 36:869–877

    Article  PubMed  CAS  Google Scholar 

  • Van Leeuwen T, Vanholme B, Van Pottelberge S, Van Nieuwenhuyse P, Nauen R, Tirry L, Denholm I (2008) Mitochondrial heteroplasmy and the evolution of insecticide resistance: non-Mendelian inheritance in action. Proc Natl Acad Sci USA 105:5980–5985

    Article  PubMed  CAS  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (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  CAS  Google Scholar 

  • Van Leeuwen T, Demaeght P, Osborne EJ, Dermauw W, Gohlke S, Nauen R, Grbic M, Tirry L, Merzendorfer H, Clark RM (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci USA 109:4407–4412

    Article  PubMed  Google Scholar 

  • Van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (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

    Article  PubMed  CAS  Google Scholar 

  • Van Nieuwenhuyse P, Van Leeuwen T, Khajehali J, Vanholme B, Tirry L (2009) Mutations in the mitochondrial cytochrome b of Tetranychus urticae Koch (Acari: Tetranychidae) confer cross-resistance between bifenazate and acequinocyl. Pest Manag Sci 65:404–412

    Article  PubMed  CAS  Google Scholar 

  • Van Pottelberge S, Van Leeuwen T, Van Amermaet K, Tirry L (2008) Induction of cytochrome P450 monooxygenase activity in the two-spotted spider mite Tetranychus urticae and its influence on acaricide toxicity. Pestic Biochem Physiol 91:128–133

    Article  CAS  Google Scholar 

  • Van Pottelberge S, Van Leeuwen T, Khajehali J, Tirry L (2009a) Genetic and biochemical analysis of a laboratory-selected spirodiclofen-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Pest Manag Sci 65:358–366

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wybouw N, Kosterlitz O, Kurlovs AH, Bajda S, Greenhalgh R, Snoeck S, Bui H, Bryon A, Dermauw W, Van Leeuwen T, Clark RM (2019) Long-term population studies uncover the genome structure and genetic basis of xenobiotic and host plant adaptation in the herbivore Tetranychus urticae. Genetics 211:1409–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z (2003) Mites of greenhouses: identification, biology and control. CABI Publishing, Wallingford, p 244

    Book  Google Scholar 

Download references

Acknowledgements

This work was partially funded by the University of Amsterdam (IBED), and it was supported by the Research Foundation - Flanders (FWO) [Grant G009312N and Grant G053815N] and the Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program [Grant 772026-POLYADAPT and 773902–SUPERPEST]. N.W. was supported by a Research Foundation - Flanders (FWO) postdoctoral fellowship (12T9818N).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Van Leeuwen.

Additional information

Communicated by E. Roditakis.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Supplementary material 2 (XLSX 250 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fotoukkiaii, S.M., Mermans, C., Wybouw, N. et al. Resistance risk assessment of the novel complex II inhibitor pyflubumide in the polyphagous pest Tetranychus urticae. J Pest Sci 93, 1085–1096 (2020). https://doi.org/10.1007/s10340-020-01213-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-020-01213-x

Keywords

Navigation