Hostname: page-component-77c89778f8-gq7q9 Total loading time: 0 Render date: 2024-07-19T08:24:13.810Z Has data issue: false hasContentIssue false
  • English
  • Français

Gene expression of detoxification enzymes in insecticide-resistant and insecticide-susceptible Bemisia tabaci strains after diafenthiuron exposure

Published online by Cambridge University Press:  04 March 2016

B.-Z. ZHANG ,
F.-C. KONG ,
R.-K. CUI  and
X.-N. ZENG
B.-Z. ZHANG
Affiliation:
Key Laboratory of Natural Pesticide and Chemical Biology, Ministry of Education, South China Agricultural University, Guangzhou 510642, People's Republic of China College of Natural Resources and Environment, Henan Institute of Science and Technology, Xinxiang 453000, People's Republic of China
F.-C. KONG
Affiliation:
Key Laboratory of Natural Pesticide and Chemical Biology, Ministry of Education, South China Agricultural University, Guangzhou 510642, People's Republic of China
R.-K. CUI
Affiliation:
Key Laboratory of Natural Pesticide and Chemical Biology, Ministry of Education, South China Agricultural University, Guangzhou 510642, People's Republic of China
X.-N. ZENG*
Affiliation:
Key Laboratory of Natural Pesticide and Chemical Biology, Ministry of Education, South China Agricultural University, Guangzhou 510642, People's Republic of China
*
*To whom all correspondence should be addressed. Email: zengxn@scau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Summary

The B-biotype of Bemisia tabaci (Homoptera: Aleyrodidae) has become extremely resistant to commonly used insecticides in China. To further explore the mechanisms of resistance to diafenthiuron, the diafenthiuron induction profiles of carboxylesterase (COE1), glutathione S-transferase (GST) and seven cytochrome P450 genes in both resistant (R-DfWf) and susceptible (S-Lab) strains were characterized. The detoxification genes GST, CYP6CX4, CYP6DW3, CYP6DZ6 and CYP9F, which are known to be constitutively over-expressed in the R-DfWf strain, were significantly upregulated in R-DfWf and S-Lab strains exposed to diafenthiuron at LC50 compared with their levels in strains treated with distilled water (controls); however, CYP6CX1, another detoxification gene, was not upregulated. The upregulation was more pronounced in the R-DfWf strain than in the S-Lab strain exposed to different concentrations of diafenthiuron (LC10 or LC50). Interestingly, COE1, CYP6CM1 and CYP6A, which are not constitutively over-expressed in the R-DfWf strain, were all significantly upregulated after exposure to diafenthiuron. Similarly, significant differences in the expression of these detoxification genes, with the exception of CYP6CM1 in the S-Lab strain, were also observed after exposure to diafenthiuron. However, the induction of CYP6A and COE1 was more pronounced in the S-Lab strain than in the R-DfWf strain after treatment with diafenthiuron at both concentrations, indicating that diafenthiuron induction of CYP6CM1 is specific to the R-DfWf strain, while diafenthiuron induction of the other genes is common to both the R-DfWf and S-Lab strains. These results demonstrate that multiple detoxification genes are co-upregulated in the R-DfWf strain through both constitutive over-expression and induction mechanisms. This knowledge will be useful for rational selection of insecticides for use in resistance management and control of this species.

Type
Animal Research Papers
Information
The Journal of Agricultural Science , Volume 154 , Issue 4 , May 2016 , pp. 742 - 753
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

REFERENCES

Alon, M., Alon, F., Nauen, R. & Morin, S. (2008). Organophosphates’ resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and over-expression of carboxylesterase. Insect Biochemistry and Molecular Biology 38, 940–949.Google Scholar
Bass, C., Puinean, A. M., Andrews, M., Cutler, P., Daniels, M., Elias, J., Paul, V. L., Crossthwaitte, A. J., Denholm, I., Field, L. M., Foster, S. P., Lind, P., Williamson, M. S. & Slater, R. (2011). Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neuroscience 12, 51. doi:10.1186/1471-2202-12-51.Google Scholar
Brandt, A., Scharf, M., Pedra, J. H. F., Holmes, G., Dean, A., Kreitman, M. & Pittendrigh, B. R. (2002). Differential expression and induction of two Drosophila cytochrome P450 genes near the Rst (2) DDT locus. Insect Molecular Biology 11, 337–341.CrossRefGoogle ScholarPubMed
Brown, J. K., Frohlich, D. R. & Rosell, R. C. (1995). The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annual Review of Entomology 40, 511–534.CrossRefGoogle Scholar
Cahill, M., Gorman, K., Day, S., Denholm, I., Elbert, A. & Nauen, R. (1996). Baseline determination and detection of resistance to imidacloprid in Bemisia tabaci (Homoptera: Aleyrodidae). Bulletin of Entomological Research 86, 343–349.CrossRefGoogle Scholar
De Barro, P. J., Liu, S. S., Boykin, L. M. & Dinsdale, A. B. (2011). Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.CrossRefGoogle ScholarPubMed
Delbeke, F., Vercruysse, P., Tirry, L., De Clercq, P. & Degheele, D. (1997). Toxicity of diflubenzuron, pyriproxyfen, imidacloprid and diafenthiuron to the predatory bug Orius laevigatus (Het.: Anthocoridae). Entomophaga 42, 349–358.Google Scholar
Dinsdale, A., Cook, L., Riginos, C., Buckley, Y. M. & De Barro, P. (2010). Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196–208.Google Scholar
Feng, Q. L., Davey, K. G., Pang, A. S. D., Ladd, T. R., Retnakaran, A., Tomkins, B. L. & Palli, S. R. (2001). Developmental expression and stress induction of glutathione S-transferase in the spruce budworm, Choristoneura fumiferana. Journal of Insect Physiology 47, 1–10.CrossRefGoogle ScholarPubMed
Feng, Y., Wu, Q., Wang, S., Chang, X., Xie, W., Xu, B. & Zhang, Y. (2010). Cross-resistance study and biochemical mechanisms of thiamethoxam resistance in B-biotype Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 66, 313–318.Google Scholar
Feng, Y. T., Wu, Q. J., Xu, B. Y., Wang, S. L., Chang, X. L., Xie, W. & Zhang, Y. J. (2009). Fitness costs and morphological change of laboratory-selected thiamethoxam resistance in the B-type Bemisia tabaci (Hemiptera: Aleyrodidae). Journal of Applied Entomology 133, 466–472.CrossRefGoogle Scholar
Gong, Y., Li, T., Zhang, L., Gao, X. & Liu, N. (2013). Permethrin induction of multiple cytochrome P450 genes in insecticide resistant mosquitoes, Culex quinquefasciatus. International Journal of Biological Sciences 9, 863–871.Google Scholar
Hameed, A., Aziz, M. A. & Aheer, G. M. (2010). Susceptibility of Bemisia tabaci Gen. (Homoptera: Aleyrodidae) to selected insecticides. Pakistan Journal of Zoology 42, 295–300.Google Scholar
Horowitz, A. R., Kontsedalov, S. & Ishaaya, I. (2004). Dynamics of resistance to the neonicotinoids acetamiprid and thiamethoxam in Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology 97, 2051–2056.CrossRefGoogle Scholar
Huang, H. S., Hu, N. T., Yao, Y. E., Wu, C. Y., Chiang, S. W. & Sun, C. N. (1998). Molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the diamondback moth, Plutella xylostella. Insect Biochemistry and Molecular Biology 28, 651–658.Google Scholar
Ismail, S. M. M. (1997). Selectivity and joint action of Melia azedarach L. fruit extracts with certain acaricides to Tetranychus urticae Kock and Stethorus gilvifrons Mulsant. Annals of Agricultural Science, Moshtohor 35, 605–618.Google Scholar
Jones, C. M., Daniels, M., Andrews, M., Slater, R., Lind, R. J., Gorman, K., Williamson, M. S. & Denholm, I. (2011). Age-specific expression of a P450 monooxygenase (CYP6CM1) correlates with neonicotinoid resistance in Bemisia tabaci. Pesticide Biochemistry and Physiology 101, 53–58.CrossRefGoogle Scholar
Karunker, I., Benting, J., Lueke, B., Ponge, T., Nauen, R., Roditakis, E., Vontas, J., Gorman, K., Denholm, I. & Morin, S. (2008). Over-expression of cytochrome P450 CYP6CM1 is associated with high resistance to imidacloprid in the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochemistry and Molecular Biology 38, 634–644.CrossRefGoogle Scholar
Karunker, I., Morou, E., Nikou, D., Nauen, R., Sertchook, R., Stevenson, B. J., Paine, M. J., Morin, S. & Vontas, J. (2009). Structural model and functional characterization of the Bemisia tabaci CYP6CM1vQ, a cytochrome P450 associated with high levels of imidacloprid resistance. Insect Biochemistry and Molecular Biology 39, 697–706.Google Scholar
Li, X., Schuler, M. A. & Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231–253.Google Scholar
Lindroth, R. L. & Weisbrod, A. V. (1991). Genetic variation in response of the gypsy moth to aspen phenolic glycosides. Biochemical Systematics and Ecology 19, 97–103.Google Scholar
Liu, N. & Scott, J. G. (1998). Increased transcription of CYP6D1 causes cytochrome P450-mediated insecticide resistance in house fly. Insect Biochemistry and Molecular Biology 28, 531–535.Google Scholar
Liu, N., Li, T., Reid, W. R., Yang, T. & Zhang, L. (2011). Multiple cytochrome P450 genes: their constitutive over-expression and permethrin induction in insecticide resistant mosquitoes, Culex quinquefasciatus. PLoS ONE 6, e23403. doi:10.1371/journal.pone.0023403.Google Scholar
Low, W. Y., Ng, H. L., Morton, C. J., Parker, M. W., Batterham, P. & Robin, C. (2007). Molecular evolution of glutathione S-transferases in the genus Drosophila. Genetics 177, 1363–1375.CrossRefGoogle ScholarPubMed
Nauen, R. & Denholm, I. (2005). Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Archives of Insect Biochemistry and Physiology 58, 200–215.Google Scholar
Nauen, R., Stumpf, N. & Elbert, A. (2002). Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 58, 868–875.Google Scholar
Pavek, P. & Dvorak, Z. (2008). Xenobiotic-induced transcriptional regulation of xenobiotic metabolizing enzymes of the cytochrome P450 superfamily in human extrahepatic tissues. Current Drug Metabolism 9, 129–143.Google Scholar
Perring, T. M. (2001). The Bemisia tabaci species complex. Crop Protection 20, 725–737.Google Scholar
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45. doi:10.1093/nar/29.9.e45.Google Scholar
Puinean, A. M., Foster, S. P., Oliphant, L., Denholm, I., Field, L. M., Millar, N. S., Williamson, M. S. & Bass, C. (2010). Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genetics 6, e1000999. doi:10.1371/journal.pgen.1000999.Google Scholar
Qiu, B. L., Liu, L., Li, X. X., Mathur, V., Qin, Z. Q. & Ren, S. X. (2009). Genetic mutations associated with chemical resistance in the cytochrome P450 genes of invasive and native Bemisia tabaci (Hemiptera: Aleyrodidae) populations in China. Insect Science 16, 237–245.Google Scholar
Ranson, H., Rossiter, L., Ortelli, F., Jensen, B., Wang, X., Roth, C. W., Collins, F. H. & Hemingway, J. (2001). Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochemical Journal 359, 295–304.Google Scholar
Rauch, N. & Nauen, R. (2003). Identification of biochemical markers linked to neonicotinoid cross resistance in Bemisia tabaci (Hemiptera: Aleyrodidae). Archives of Insect Biochemistry and Physiology 54, 165–176.Google Scholar
Schuler, M. A. (2011). P450s in plant–insect interactions. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1814, 36–45.Google Scholar
Scott, J. G. (2008). Insect cytochrome P450s: thinking beyond detoxification. In Recent Advances in Insect Physiology, Toxicology and Molecular Biology (Ed. Liu, N.), pp. 117–124. Kerala, India: Research Signpost.Google Scholar
Shi, Z. & Liu, S. (1998). Toxicity of insecticides commonly used in vegetable fields to the diamondback moth, Plutella xylostella, and its parasite, Cotesia plutellae. Chinese Journal of Biological Control 14, 53–57.Google Scholar
Sun, D. B., Xu, J., Luan, J. B. & Liu, S. S. (2011). Reproductive incompatibility between the B and Q biotypes of the whitefly Bemisia tabaci in China: genetic and behavioural evidence. Bulletin of Entomological Research 101, 211–220.CrossRefGoogle Scholar
Torres, J. B., Silva-Torres, C. S. A., Silva, M. R. & Ferreira, J. F. (2002). Compatibility of insecticides and acaricides to the predatory stinkbug Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) on cotton. Neotropical Entomology 31, 311–317.Google Scholar
Vontas, J. G., Small, G. J. & Hemingway, J. (2001). Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal 357, 65–72.CrossRefGoogle ScholarPubMed
Wang, L. & Wu, Y. (2007). Cross-resistance and biochemical mechanisms of abamectin resistance in the B-type Bemisia tabaci. Journal of Applied Entomology 131, 98–103.Google Scholar
Wang, Z., Yan, H., Yang, Y. & Wu, Y. (2010). Biotype and insecticide resistance status of the whitefly Bemisia tabaci from China. Pest Management Science 66, 1360–1366.Google Scholar
Xie, W., Wang, S., Wu, Q., Feng, Y., Pan, H., Jiao, X., Zhou, L., Yang, X., Fu, W., Teng, H., Xu, B. & Zhang, Y. (2011). Induction effects of host plants on insecticide susceptibility and detoxification enzymes of Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 67, 87–93.Google Scholar
Yang, N., Xie, W., Jones, C. M., Bass, C., Jiao, X., Yang, X., Liu, B., Li, R. & Zhang, Y. (2013). Transcriptome profiling of the whitefly Bemisia tabaci reveals stage-specific gene expression signatures for thiamethoxam resistance. Insect Molecular Biology 22, 485–496.CrossRefGoogle ScholarPubMed
Yoo, S. S. & Kim, S. S. (2000). Comparative toxicity of some pesticides to the predatory mite, Phytoseiulus persimilis (Acarina: Phytoseiidae) and the twospotted spider mite, Tetranychus urticae (Acarina: Tetranychidae). Korean Journal of Entomology 30, 235–241.Google Scholar
Yoshiyama, M. & Shukle, R. H. (2004). Molecular cloning and characterization of a Glutathione S-transferase gene from Hessian fly (Diptera: Cecidomyiidae). Annals of the Entomological Society of America 97, 1285–1293.CrossRefGoogle Scholar
Zhang, B. Z., Kong, F. C., Wang, H. T., Gao, X. W., Zeng, X. N. & Shi, X. Y. (2015 a). Insecticide induction of o-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren). Journal of Integrative Agriculture 15. doi:10.1016/S2095-3119(15)61072-3.Google Scholar
Zhang, B. Z., Kong, F. C. & Zeng, X. N. (2015 b). Detoxification enzyme activity and gene expression in diafenthiuron resistant whitefly, Bemisia tabaci. Journal of Agricultural Science (Canada) 7, 66–76.Google Scholar
Zhu, F., Li, T., Zhang, L. & Liu, N. (2008). Co-up-regulation of three P450 genes in response to permethrin exposure in permethrin resistant house flies, Musca domestica. BMC Physiology 8, 18. doi:10.1186/1472-6793-8-18.Google Scholar
Zhuang, H. M., Wang, K. F., Zheng, L., Wu, Z. J., Miyata, T. & Wu, G. (2011). Identification and characterization of a cytochrome P450 CYP6CX1 putatively associated with insecticide resistance in Bemisia tabaci. Insect Science 18, 484–494.Google Scholar