Skip to main content Accessibility help
×
Home
Hostname: page-component-cf9d5c678-cnwzk Total loading time: 0.243 Render date: 2021-07-29T20:51:35.752Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Mechanisms of resistance to three mite growth inhibitors of Tetranychus urticae in hops

Published online by Cambridge University Press:  03 May 2017

A.W. Adesanya
Affiliation:
Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA 99350, USA Department of Entomology, College of Agricultural, Human, and Natural Resource Sciences, Washington State University, Pullman, WA 99164, USA
M.A Morales
Affiliation:
Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA 99350, USA Department of Entomology, College of Agricultural, Human, and Natural Resource Sciences, Washington State University, Pullman, WA 99164, USA
D.B. Walsh
Affiliation:
Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA 99350, USA
L.C. Lavine
Affiliation:
Department of Entomology, College of Agricultural, Human, and Natural Resource Sciences, Washington State University, Pullman, WA 99164, USA
M.D. Lavine
Affiliation:
Department of Entomology, College of Agricultural, Human, and Natural Resource Sciences, Washington State University, Pullman, WA 99164, USA
F. Zhu
Affiliation:
Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA 99350, USA Department of Entomology, College of Agricultural, Human, and Natural Resource Sciences, Washington State University, Pullman, WA 99164, USA
Corresponding
E-mail address:

Abstract

Mite growth inhibitors (MGIs), such as etoxazole and hexythiazox, are valuable IPM tools for Tetranychus urticae control in hops due to their unique mode of action and selectivity. Hence, it is necessary to standardize bioassay methods to evaluate the efficacy of MGIs, monitor resistance, and identify mechanisms underlying MGI resistance in the field. Here, we developed a three-tiered approach for evaluating ovicidal toxicity of MGIs to T. urticae, which simulated different MGI exposure scenarios in the field. The most effective bioassay method was direct exposure of T. urticae eggs to MGIs. With this method, four field-collected T. urticae populations showed low-to-moderate resistance to MGIs. Cross-resistance among MGIs and from MGIs to bifenazate and bifenthrin was detected. Besides target site insensitivity, enhanced cytochrome P450 and esterase activities also contribute to the MGI resistance in hop yard-collected T. urticae populations. Low-to-moderate MGI resistance in T. urticae populations may be mediated by multiple mechanisms. Positive selection pressure on the I1017F mutation is moderate in field-collected T. urticae populations. Further studies are required to identify metabolic detoxification genes that confer resistance to MGIs for precise resistance monitoring.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265267.CrossRefGoogle Scholar
Abraham, C.M., Braman, S.K., Oetting, R.D. & Hinkle, N.C. (2013) Pesticide compatibility with natural enemies for pest management in greenhouse gerbera daisies. Journal of Economic Entomology 106, 15901601.CrossRefGoogle ScholarPubMed
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). Journal of Economic Entomology 101, 17041710.CrossRefGoogle Scholar
Aveyard, C.S., Peregrine, D.J. & Bryan, K.M.G. (1986) Biological activity of clofentezine against egg and motile stages of tetranychid mites. Experimental and Applied Acarology 2, 223229.CrossRefGoogle Scholar
Ay, R. & Kara, F.E. (2011) Toxicity, inheritance and biochemistry of clofentezine resistance in Tetranychus urticae . Insect Science 18, 503511.CrossRefGoogle Scholar
Bi, J.L., Niu, Z.M., Yu, L. & Toscano, N.C. (2016) Resistance status of the carmine spider mite, Tetranychus cinnabarinus and the twospotted spider mite, Tetranychus urticae to selected acaricides on strawberries. Insect Science 23, 8893.CrossRefGoogle ScholarPubMed
Chapman, R.B. & Marris, J.W.M. (1986) The sterilizing effect of clofentezine adn hexythiazox on female twospotted mites. pp. 237240 in Proceedings of the 39th New Zealand Weed and Pest Control Conference. Canterbury, New Zealand.Google Scholar
Chouaibou, M., Zivanovic, G.B., Knox, T.B., Jamet, H.P. & Bonfoh, B. (2014) Synergist bioassays: a simple method for initial metabolic resistance investigation of field Anopheles gambiae s.l. populations. Acta Tropica 130, 108111.CrossRefGoogle ScholarPubMed
Cranham, J.E. (1985) Control of Tetranychidae in Hop. pp. 367–369 in Helle, W. and Sabelis, M.W. (Eds) World Crop Pests: Spider Mites their Biology, Natural Enemies and Control. Amsterdam, Elsevier Press.Google Scholar
Dekeyser, M.A. (2005) Acaricide mode of action. Pest Management Science 61, 103110.CrossRefGoogle ScholarPubMed
Demaeght, P., Dermauw, W., Tsakireli, D., Khajehali, J., Nauen, R., Tirry, L., Vontas, J., Lummen, 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 Biochemistry and Molecular Biology 43, 544554.CrossRefGoogle Scholar
Demaeght, P., Osborne, E.J., Odman-Naresh, J., Grbic, M., Nauen, R., Merzendorfer, H., Clark, R.M. & Van Leeuwen, T. (2014) High resolution genetic mapping uncovers chitin synthase-1 as the target-site of the structurally diverse mite growth inhibitors clofentezine, hexythiazox and etoxazole in Tetranychus urticae . Insect Biochemistry and Molecular Biology 51, 5261.CrossRefGoogle ScholarPubMed
Dermauw, W., Wybouw, N., Rombauts, S., Menten, B., Vontas, J., Grbic, M., Clark, R.M., Feyereisen, R. & Van Leeuwen, T. (2013) A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae . Proceedings of the National Academy of Sciences of the United States of America 110, E113E122.CrossRefGoogle ScholarPubMed
Feyereisen, R. (2012) Insect CYP genes and P450 enzymes. pp. 236316 in Gilbert, L.I. (Ed) Insect Molecular Biology and Biochemistry. Cambridge, Massachusetts, Elisevier Academic Press.CrossRefGoogle Scholar
Grbic, M., Van Leeuwen, T., Clark, R.M., Rombauts, S., Rouze, P., Grbic, V., Osborne, E.J., Dermauw, W., Ngoc, P.C., Ortego, F., Hernandez-Crespo, P., Diaz, I., Martinez, M., Navajas, M., Sucena, E., Magalhaes, S., Nagy, L., Pace, R.M., Djuranovic, S., Smagghe, G., Iga, M., Christiaens, O., Veenstra, J.A., Ewer, J., Villalobos, R.M., Hutter, J.L., Hudson, S.D., Velez, M., Yi, S.V., Zeng, J., Pires-daSilva, A., Roch, F., Cazaux, M., Navarro, M., Zhurov, V., Acevedo, G., Bjelica, A., Fawcett, J.A., Bonnet, E., Martens, C., Baele, G., Wissler, L., Sanchez-Rodriguez, A., Tirry, L., Blais, C., Demeestere, K., Henz, S.R., Gregory, T.R., Mathieu, J., Verdon, L., Farinelli, L., Schmutz, J., Lindquist, E., Feyereisen, R. & Van de Peer, Y. (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479, 487492.CrossRefGoogle ScholarPubMed
Herron, G., Edge, V. & Rophail, J. (1993) Clofentezine and hexythiazox resistance in Tetranychus urticae Koch in Austrilia. Experimental and Applied Acarology 17, 433440.CrossRefGoogle Scholar
Hoy, M.A. & Ouyang, Y.L. (1986) Selectivity of the acaricides clofentezine and hexythiazox to the predator Metaseiulus occidentalis (Acari: Phytoseiidae). Journal of Economic Entomology 79, 13771380.CrossRefGoogle Scholar
Ilias, A., Vontas, J. & Tsagkarakou, A. (2014) Global distribution and origin of target site insecticide resistance mutations in Tetranychus urticae . Insect Biochemistry and Molecular Biology 48, 1728.CrossRefGoogle ScholarPubMed
Knight, A.L., Beers, E.H., Hoyt, S.C. & Riedl, H. (1990) Acaricide bioassay with spider mites (Acari: Tetranychidae) on pome fruits: evaluation of methods and selection of discriminating concentrations for resistance monitoring. Journal of Economic Entomology 83, 17521760.CrossRefGoogle Scholar
Liu, N. & Yue, X. (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). Journal of Economic Entomology 93, 12691275.CrossRefGoogle Scholar
Liu, N. & Zhu, F. (2011) House fly cytochrome P450s: their role in insecticide resistance and strategies in the isolation and characterization. pp. 246257 in Liu, T. and Kang, L. (Eds) Recent Advances in Entomological Research. Beijing and Verlag Berlin Heidelberg, Higher Education Press and Springer.CrossRefGoogle Scholar
Liu, N., Zhu, F., Xu, Q., Pridgeon, J.W. & Gao, X.W. (2006) Behavioral change, physiological modification, and metabolic detoxification: mechanisms of insecticide resistance. Acta Entomologica Sinica 49, 671679.Google Scholar
Marcic, D. (2003) The effects of clofentezine on life-table parameters in two-spotted spider mite Tetranychus urticae . Experimental and Applied Acarology 30, 249263.CrossRefGoogle ScholarPubMed
Marris, J.W.M. (1988) The toxicity of hexythiazox to twospotted spider mite (Tetranychus urncae Koch) adults and eggs. MS thesis, University of Canterbury.Google Scholar
Merzendorfer, H. (2006) Insect chitin synthases: a review. Journal of Comparative Physiology B 176, 115.CrossRefGoogle ScholarPubMed
Morales, M.A., Mendoza, B.M., Lavine, L.C., Lavine, M.D., Walsh, D.B. & Zhu, F. (2016) Selection of reference genes for expression studies of xenobiotic adaptation in Tetranychus urticae . International Journal of Biological Sciences 12, 11291139.CrossRefGoogle ScholarPubMed
Nauen, R. (2007) Insecticide resistance in disease vectors of public health importance. Pest Management Science 63, 628633.CrossRefGoogle ScholarPubMed
Nauen, R. & Smagghe, G. (2006) Mode of action of etoxazole. Pest Management Science 62, 379382.CrossRefGoogle ScholarPubMed
O'Neal, S.D., Walsh, D.B., Gent, D.H., Barbour, J.D., Boydston, R.A., George, A.E., James, D.G. & Sirrine, J.R. (2015) Field Guide for Integrated Pest Management in Hops. Pullman, WA, U.S. Hop Industry Plant Protection Committee.Google Scholar
Piraneo, T.G., Bull, J., Morales, M.A., Lavine, L.C., Walsh, D.B. & Zhu, F. (2015) Molecular mechanisms of Tetranychus urticae chemical adaptation in hop fields. Scientific Reports 5, 17090.CrossRefGoogle ScholarPubMed
Pree, D.J., Bittner, L.A. & Whitty, K.J. (2002) Characterization of resistance to clofentezine in populations of European red mite from orchards in Ontario. Experimental and Applied Acarology 27, 181193.CrossRefGoogle ScholarPubMed
Rathman, R.J., Beers, E.H., Flexner, J.L., Riedl, H., Hoyt, S.C., Westigard, P.H. & Knight, A.L. (1990) Baseline bioassays with hexythiazox and clofentezine of three mite species (Acari: Tetranychidae) occurring on Washington and Oregon tree fruits. Journal of Economic Entomology 83, 17111714.CrossRefGoogle Scholar
Riga, M., Tsakireli, D., Ilias, A., Morou, E., Myridakis, A., Stephanou, E.G., Nauen, R., Dermauw, W., Van Leeuwen, T., Paine, M. & Vontas, J. (2014) Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae . Insect Biochemistry and Molecular Biology 46, 4353.CrossRefGoogle ScholarPubMed
Riga, M., Myridakis, A., Tsakireli, D., Morou, E., Stephanou, E.G., Nauen, R., Van Leeuwen, T., Douris, V. & Vontas, J. (2015) Functional characterization of the Tetranychus urticae CYP392A11, a cytochrome P450 that hydroxylates the METI acaricides cyenopyrafen and fenpyroximate. Insect Biochemistry and Molecular Biology 65, 9199.CrossRefGoogle ScholarPubMed
Saenz-de-Cabezon Irigaray, F.J. & Zalom, F.G. (2012) Transovarial biotransference of etoxazole through a terrestrial trophic web. Pest Management Science 68, 14671470.CrossRefGoogle ScholarPubMed
Sparks, T.C. & Nauen, R. (2015) IRAC: mode of action classification and insecticide resistance management. Pesticide Biochemistry and Physiology 121, 122128.CrossRefGoogle ScholarPubMed
Suzuki, J., Ishida, T., Kikuchi, Y., Ito, Y., Morikawa, C., Tsukidate, Y., Tanji, I., Ota, Y. & Toda, K. (2002) Synthesis and activity of novel acaricidal/insecticidal 2,4-diphenyl-1,3-oxazolines. Journal of Pesticide Science 27, 18.CrossRefGoogle Scholar
Thwaite, W.G. (1991) Resistance to clofentezine and hexythiazox in Panonychus ulmi from apples in Australia. Experimental and Applied Acarology 11, 7380.CrossRefGoogle Scholar
Uesugi, R., Goka, K. & Osakabe, M. (2002) Genetic basis of resistances to chlorfenapyr and etoxazole in the two-spotted spider mite (Acari: Tetranychidae). Journal of Economic Entomology 95, 12671274.CrossRefGoogle Scholar
USDA-NASS (2015) Available online at http://www.nass.usda.gov/Statistics_by_Subject (accessed 8 December 2016).Google Scholar
Van Leeuwen, T. & Dermauw, W. (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annual Review of Entomology 61, 475498.CrossRefGoogle ScholarPubMed
Van Leeuwen, T. & Tirry, L. (2007) Esterase-mediated bifenthrin resistance in a multiresistant strain of the two-spotted spider mite, Tetranychus urticae . Pest Management Science 63, 150156.CrossRefGoogle Scholar
Van Leeuwen, T., Demaeght, P., Osborne, E.J., Dermauw, W., Gohlke, S., Nauen, R., Grbic, M., Tirry, L., Merzendorfer, H. & Clark, R.M. (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proceedings of the National Academy of Sciences of the United States of America 109, 44074412.CrossRefGoogle ScholarPubMed
Van Pottelberge, S., Van Leeuwen, T., Khajehali, J. & Tirry, L. (2009) Genetic and biochemical analysis of a laboratory-selected spirodiclofen-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Pest Management Science 65, 358366.CrossRefGoogle Scholar
Yamamoto, A., Yoneda, H., Hatano, R. & Asada, M. (1995) Laboratory selections of populations in the citrus red mite, Panonchus citri (McGregor), with hexythiazox and their cross-resistance spectrum. Journal of Pesticide Science 20, 493501.CrossRefGoogle Scholar
Yorulmaz Salman, S., Aydinli, F. & Ay, R. (2015) Etoxazole resistance in predatory mite Phytoseiulus persimilis A.-H. (Acari: Phytoseiidae): cross-resistance, inheritance and biochemical resistance mechanisms. Pesticide Biochemistry and Physiology 122, 96102.CrossRefGoogle ScholarPubMed
Zhang, N.N., Liu, C.F., Yang, F., Dong, S.L. & Han, Z.J. (2012) Resistance mechanisms to chlorpyrifos and F392W mutation frequencies in the acetylcholine esterase ace1 allele of field populations of the tobacco whitefly, Bemisia tabaci in China. Journal of Insect Science 12, 41.CrossRefGoogle Scholar
Zhu, F., Parthasarathy, R., Bai, H., Woithe, K., Kaussmann, M., Nauen, R., Harrison, D.A. & Palli, S.R. (2010) A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum . Proceedings of the National Academy of Sciences of the United States of America 107, 85578562.CrossRefGoogle ScholarPubMed
Zhu, F., Moural, T.W., Shah, K. & Palli, S.R. (2013 a) Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle, Tribolium castaneum . BMC Genomics 14, 174.CrossRefGoogle ScholarPubMed
Zhu, F., Gujar, H., Gordon, J.R., Haynes, K.F., Potter, M.F. & Palli, S.R. (2013 b) Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Scientific Reports 3, 1456.CrossRefGoogle ScholarPubMed
Zhu, F., Cui, Y., Lavine, L.C. & Walsh, D.B. (2014) Application of RNAi toward insecticide resistance management. pp. 595619 in Chandrasekar, R., Tyagi, B.K., Gui, Z. and Reeck, G.R. (Eds) Short Views on Insect Biochemistry and Molecular Biology. Manhattan, Academic Publisher.Google Scholar
Zhu, F., Moural, T.W., Nelson, D.R. & Palli, S.R. (2016 a) A specialist herbivore pest adaptation to xenobiotics through up-regulation of multiple Cytochrome P450s. Scientific Reports 6, 20421.CrossRefGoogle ScholarPubMed
Zhu, K.Y., Merzendorfer, H., Zhang, W., Zhang, J. & Muthukrishnan, S. (2016 b) Biosynthesis, turnover, and functions of chitin in insects. Annual Review of Entomology 61, 177196.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Adesanya supplementary material

Figure S1 and Tables S1-S4

Download Adesanya supplementary material(PDF)
PDF 187 KB
Supplementary material: File

Adesanya supplementary material

Adesanya supplementary material 1

Download Adesanya supplementary material(File)
File 24 KB
14
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Mechanisms of resistance to three mite growth inhibitors of Tetranychus urticae in hops
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Mechanisms of resistance to three mite growth inhibitors of Tetranychus urticae in hops
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Mechanisms of resistance to three mite growth inhibitors of Tetranychus urticae in hops
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *