Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. / Vlogiannitis, Spyridon; Mavridis, Konstantinos; Dermauw, Wannes; Snoeck, Simon; Katsavou, Evangelia; Morou, Evangelia; Harizanis, Paschalis; Swevers, Luc; Hemingway, Janet; Feyereisen, René; van Leeuwen, Thomas; Vontas, John.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 118, No. 6, e2020380118, 2021.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Vlogiannitis, S, Mavridis, K, Dermauw, W, Snoeck, S, Katsavou, E, Morou, E, Harizanis, P, Swevers, L, Hemingway, J, Feyereisen, R, van Leeuwen, T & Vontas, J 2021, 'Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 6, e2020380118. https://doi.org/10.1073/pnas.2020380118

APA

Vlogiannitis, S., Mavridis, K., Dermauw, W., Snoeck, S., Katsavou, E., Morou, E., Harizanis, P., Swevers, L., Hemingway, J., Feyereisen, R., van Leeuwen, T., & Vontas, J. (2021). Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. Proceedings of the National Academy of Sciences of the United States of America, 118(6), [e2020380118]. https://doi.org/10.1073/pnas.2020380118

Vancouver

Vlogiannitis S, Mavridis K, Dermauw W, Snoeck S, Katsavou E, Morou E et al. Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. Proceedings of the National Academy of Sciences of the United States of America. 2021;118(6). e2020380118. https://doi.org/10.1073/pnas.2020380118

Author

Vlogiannitis, Spyridon ; Mavridis, Konstantinos ; Dermauw, Wannes ; Snoeck, Simon ; Katsavou, Evangelia ; Morou, Evangelia ; Harizanis, Paschalis ; Swevers, Luc ; Hemingway, Janet ; Feyereisen, René ; van Leeuwen, Thomas ; Vontas, John. / Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. In: Proceedings of the National Academy of Sciences of the United States of America. 2021 ; Vol. 118, No. 6.

Bibtex

@article{e1b6959b5f1b4096a729d58eb8ed32f7,
title = "Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor",
abstract = "Varroa destructor is one of the main problems in modern beekeeping. Highly selective acaricides with low toxicity to bees are used internationally to control this mite. One of the key acaricides is the organophosphorus (OP) proinsecticide coumaphos, that becomes toxic after enzymatic activation inside Varroa. We show here that mites from the island Andros (AN-CR) exhibit high levels of coumaphos resistance. Resistance is not mediated by decreased coumaphos uptake, target-site resistance, or increased detoxification. Reduced proinsecticide activation by a cytochrome P450 enzyme was the main resistance mechanism, a powerful and rarely encountered evolutionary solution to insecticide selection pressure. After treatment with sublethal doses of [14C] coumaphos, susceptible mite extracts had substantial amounts of coroxon, the activated metabolite of coumaphos, while resistant mites had only trace amounts. This indicates a suppression of the P450 (CYP)-mediated activation step in the AN-CR mites. Bioassays with coroxon to bypass the activation step showed that resistance was dramatically reduced. There are 26 CYPs present in the V. destructor genome. Transcriptome analysis revealed overexpression in resistant mites of CYP4DP24 and underexpression of CYP3012A6 and CYP4EP4. RNA interference of CYP4EP4 in the susceptible population, to mimic underexpression seen in the resistant mites, prevented coumaphos activation and decreased coumaphos toxicity.",
keywords = "CYPome, Honey bee, Pesticide, Resistance management, Selectivity",
author = "Spyridon Vlogiannitis and Konstantinos Mavridis and Wannes Dermauw and Simon Snoeck and Evangelia Katsavou and Evangelia Morou and Paschalis Harizanis and Luc Swevers and Janet Hemingway and Ren{\'e} Feyereisen and {van Leeuwen}, Thomas and John Vontas",
year = "2021",
doi = "10.1073/pnas.2020380118",
language = "English",
volume = "118",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "The National Academy of Sciences of the United States of America",
number = "6",

}

RIS

TY - JOUR

T1 - Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor

AU - Vlogiannitis, Spyridon

AU - Mavridis, Konstantinos

AU - Dermauw, Wannes

AU - Snoeck, Simon

AU - Katsavou, Evangelia

AU - Morou, Evangelia

AU - Harizanis, Paschalis

AU - Swevers, Luc

AU - Hemingway, Janet

AU - Feyereisen, René

AU - van Leeuwen, Thomas

AU - Vontas, John

PY - 2021

Y1 - 2021

N2 - Varroa destructor is one of the main problems in modern beekeeping. Highly selective acaricides with low toxicity to bees are used internationally to control this mite. One of the key acaricides is the organophosphorus (OP) proinsecticide coumaphos, that becomes toxic after enzymatic activation inside Varroa. We show here that mites from the island Andros (AN-CR) exhibit high levels of coumaphos resistance. Resistance is not mediated by decreased coumaphos uptake, target-site resistance, or increased detoxification. Reduced proinsecticide activation by a cytochrome P450 enzyme was the main resistance mechanism, a powerful and rarely encountered evolutionary solution to insecticide selection pressure. After treatment with sublethal doses of [14C] coumaphos, susceptible mite extracts had substantial amounts of coroxon, the activated metabolite of coumaphos, while resistant mites had only trace amounts. This indicates a suppression of the P450 (CYP)-mediated activation step in the AN-CR mites. Bioassays with coroxon to bypass the activation step showed that resistance was dramatically reduced. There are 26 CYPs present in the V. destructor genome. Transcriptome analysis revealed overexpression in resistant mites of CYP4DP24 and underexpression of CYP3012A6 and CYP4EP4. RNA interference of CYP4EP4 in the susceptible population, to mimic underexpression seen in the resistant mites, prevented coumaphos activation and decreased coumaphos toxicity.

AB - Varroa destructor is one of the main problems in modern beekeeping. Highly selective acaricides with low toxicity to bees are used internationally to control this mite. One of the key acaricides is the organophosphorus (OP) proinsecticide coumaphos, that becomes toxic after enzymatic activation inside Varroa. We show here that mites from the island Andros (AN-CR) exhibit high levels of coumaphos resistance. Resistance is not mediated by decreased coumaphos uptake, target-site resistance, or increased detoxification. Reduced proinsecticide activation by a cytochrome P450 enzyme was the main resistance mechanism, a powerful and rarely encountered evolutionary solution to insecticide selection pressure. After treatment with sublethal doses of [14C] coumaphos, susceptible mite extracts had substantial amounts of coroxon, the activated metabolite of coumaphos, while resistant mites had only trace amounts. This indicates a suppression of the P450 (CYP)-mediated activation step in the AN-CR mites. Bioassays with coroxon to bypass the activation step showed that resistance was dramatically reduced. There are 26 CYPs present in the V. destructor genome. Transcriptome analysis revealed overexpression in resistant mites of CYP4DP24 and underexpression of CYP3012A6 and CYP4EP4. RNA interference of CYP4EP4 in the susceptible population, to mimic underexpression seen in the resistant mites, prevented coumaphos activation and decreased coumaphos toxicity.

KW - CYPome

KW - Honey bee

KW - Pesticide

KW - Resistance management

KW - Selectivity

U2 - 10.1073/pnas.2020380118

DO - 10.1073/pnas.2020380118

M3 - Journal article

C2 - 33547243

AN - SCOPUS:85100660702

VL - 118

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 6

M1 - e2020380118

ER -

ID: 258083287