Synergistic and compensatory effects of two point mutations conferring target-site resistance to fipronil in the insect GABA receptor RDL

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zhang, Yixi ^a   Meng, Xiangkun ^a   Yang, Yuanxue ^a   Li, Hong ^a   Wang, Xin ^a   Yang, Baojun ^b   Zhang, Jianhua ^a   Li, Chunrui ^a   Millar, Neil S ^c   Liu, Zewen ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b CHINA NATIONAL RICE RESEARCH INSTITUTE   (China)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; FIPRONIL; INSECT PROTEIN; INSECTICIDE; PYRAZOLE DERIVATIVE;

AMINO ACID SEQUENCE; ANIMAL; ELECTROPHYSIOLOGY; GENE REPRESSION; GENETICS; HEMIPTERA; INSECTICIDE RESISTANCE; METABOLISM; OOCYTE; PHYSIOLOGY; POINT MUTATION; SEQUENCE HOMOLOGY; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; ELECTROPHYSIOLOGICAL PHENOMENA; HEMIPTERA; INSECT PROTEINS; INSECTICIDE RESISTANCE; INSECTICIDES; OOCYTES; POINT MUTATION; PYRAZOLES; RECEPTORS, GABA; SEQUENCE HOMOLOGY, AMINO ACID; SUPPRESSION, GENETIC; XENOPUS;

EID: 84983750320     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32335     Document Type: Article

References (58)

1. Casida, J. E., Durkin, K. A. Neuroactive Insecticides: Targets, Selectivity, Resistance, and Secondary Effects. Annu. Rev. Entomol. Vol 58 58, 99-117 (2013).
2. Perry, T., Batterham, P., Daborn, P. J. The biology of insecticidal activity and resistance. Insect Biochem. Mol. Biol. 41, 411-422 (2011).
3. Chen, L., Durkin, K. A., Casida, J. E. Structural model for ?-aminobutyric acid receptor noncompetitive antagonist binding: Widely diverse structures fit the same site. Proc. Natl. Acad. Sci. USA 103, 5185-5190 (2006).
4. Kliot, A., Ghanim, M. Fitness costs associated with insecticide resistance. Pest Manag. Sci. 68, 1431-1437 (2012).
5. Berticat, C. et al. Costs and benefits of multiple resistance to insecticides for Culex quinquefasciatus mosquitoes. BMC Evol. Biol. 8 (2008).
6. Berticat, C., Boquien, G., Raymond, M., Chevillon, C. Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet. Res. 79, 41-47 (2002).
7. Agnew, P., Berticat, C., Bedhomme, S., Sidobre, C., Michalakis, Y. Parasitism increases and decreases the costs of insecticide resistance in mosquitoes. Evolution 58, 579-586 (2004).
8. Foster, S. P. et al. Comparative survival of insecticide-susceptible and resistant peach-potato aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in low temperature field trials. Bull. Entomol. Res. 86, 17-27 (1996).
9. Lenormand, T., Guillemaud, T., Bourguet, D., Raymond, M. Appearance and sweep of a gene duplication: Adaptive response and potential for new functions in the mosquito Culex pipiens. Evolution 52, 1705-1712 (1998).
10. Raymond, M., Berticat, C., Weill, M., Pasteur, N., Chevillon, C. Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation ? Genetica 112, 287-296 (2001).
11. Edi, C. V. et al. CYP6 P450 enzymes and ACE-1 duplication produce extreme and multiple insecticide resistance in the malaria mosquito Anopheles gambiae. Plos Genet. 10, e1004236 (2014).
12. D'Hulst, C., Atack, J. R., Kooy, R. F. The complexity of the GABA(A) receptor shapes unique pharmacological profiles. Drug Discov. Today 14, 866-875 (2009).
13. Knipple, D. C., Soderlund, D. M. The ligand-gated chloride channel gene family of Drosophila melanogaster. Pestic. Biochem. Physiol. 97, 140-148 (2010).
14. Casida, J. E., Durkin, K. A. Novel GABA receptor pesticide targets. Pestic. Biochem. Physiol. 121, 22-30 (2015).
15. Casida, J. E., Tomizawa, M. Insecticide interactions with gamma-aminobutyric acid and nicotinic receptors: predictive aspects of structural models. J. Pestic. Sci. 33, 4-8 (2008).
16. Zheng, N. et al. Binding Difference of fipronil with GABAARs in fruitfly and zebrafish: insights from homology modeling, docking, and molecular dynamics simulation studies. J. Agric. Food Chem. 62, 10646-10653 (2014).
17. McGonigle, I., Lummis, S. C. R. RDL receptors. Biochem. Soc. Trans. 37, 1404-1406 (2009).
18. Ffrench-Constant, R. H., Mortlock, D. P., Shaffer, C. D., Macintyre, R. J., Roush, R. T. Molecular-cloning and transformation of cyclodiene resistance in Drosophila-an invertebrate gamma-aminobutyric-acid subtype-a receptor locus. Proc. Natl. Acad. Sci. USA 88, 7209-7213 (1991).
19. Ffrench-Constant, R. H., Rocheleau, T. A. A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363, 449-451 (1993).
20. Buckingham, S. D., Biggin, P. C., Sattelle, B. M., Brown, L. A., Sattelle, D. B. Insect GABA receptors: Splicing, editing, and targeting by antiparasitics and insecticides. Mol. Pharmacol. 68, 942-951 (2005).
21. Zhang, H. G., ffrench-Constant, R. H., Jackson, M. B. A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J. Physiol. 479 (Pt 1), 65-75 (1994).
22. Hosie, A. M., Baylis, H. A., Buckingham, S. D., Sattelle, D. B. Actions of the insecticide fipronil, on dieldrin-sensitive and dieldrinresistant GABA receptors of Drosophila melanogaster.Br. J. Pharmacol. 115, 909-912 (1995).
23. Buckingham, S. D. et al. Wild-type and insecticide-resistant homo-oligomeric GABA receptors of Drosophila melanogaster stably expressed in a Drosophila cell line. Neuropharmacol. 35, 1393-1401 (1996).
24. Maisnier-Patin, S., Andersson, D. I. Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Res. Microbiol. 155, 360-369 (2004).
25. Powles, S. B., Yu, Q. Evolution in action: Plants resistant to herbicides. Annu. Rev. Plant Biol. 61, 317-347 (2010).
26. Boivin, T., Bouvier, J. C., Chadoeuf, J., Beslay, D., Sauphanor, B. Constraints on adaptive mutations in the codling moth Cydia pomonella (L.): measuring fitness trade-offs and natural selection. Heredity (Edinb) 90, 107-113 (2003).
27. Qi, Q., Preston, G. M., MacLean, R. C. Linking system-wide impacts of RNA polymerase mutations to the fitness cost of rifampin resistance in Pseudomonas aeruginosa. Mbio. 5 (2014).
28. Troyer, R. M. et al. Variable fitness impact of HIV-1 escape mutations to cytotoxic t lymphocyte (CTL) response. Plos Pathog. 5 (2009).
29. Vila-Aiub, M. M., Neve, P., Powles, S. B. Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol. 184, 751-767 (2009).
30. Ffrench-Constant, R. H., Pittendrigh, B., Vaughan, A., Anthony, N. Why are there so few resistance-associated mutations in insecticide target genes? Philosophical Transactions Of the Royal Society Of London Series B-Biological Sciences; 1998 Oct 29; 1998. p. 1685-1693.
31. Li, X., Schuler, M. A., Berenbaum, M. R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52, 231-253 (2007).
32. Bjorkman, J., Nagaev, I., Berg, O. G., Hughes, D., Andersson, D. I. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287, 1479-1482 (2000).
33. Levin, B. R., Perrot, V., Walker, N. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154, 985-997 (2000).
34. Kimura, M. Some models of neutral evolution, compensatory evolution, and the shifting balance process. Theor. Popul. Biol. 37, 150-158 (1990).
35. Wright, S. The shifting balance theory and macroevolution. Annu. Rev. Genet. 16, 1-19 (1982).
36. Remnant, E. J. et al. Gene duplication in the major insecticide target site, Rdl, in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 110, 14705-14710 (2013).
37. Wondji, C. S. et al. Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem. Mol. Biol. 41, 484-491 (2011).
38. Le Goff, G., Hamon, A., Berge, J. B., Amichot, M. Resistance to fipronil in Drosophila simulans: influence of two point mutations in the RDL GABA receptor subunit.J. Neurochem. 92, 1295-1305 (2005).
39. Taylor-Wells, J., Brooke, B. D., Bermudez, I., Jones, A. K. The neonicotinoid imidacloprid, and the pyrethroid deltamethrin, are antagonists of the insect Rdl GABA receptor. J. Neurochem. 135, 705-713 (2015).
40. Nakao, T., Hama, M., Kawahara, N., Hirase, K. Fipronil resistance in Sogatella furcifera: Molecular cloning and functional expression of wild-type and mutant RDL GABA receptor subunits. J. Pestic. Sci. 37, 37-44 (2012).
41. Remnant, E. J. et al. The role of Rdl in resistance to phenylpyrazoles in Drosophila melanogaster. Insect Biochem. Mol. Biol. 54, 11-21 (2014).
42. Bloomquist, J. R. GABA and glutamate receptors as biochemical sites for insecticide action. Springer-Verlag GmbH and Co. KG, Heidelberger Platz 3, D-14197, Berlin, Germany, 2001.
43. Gao, J. R. et al. The A302S mutation in Rdl that confers resistance to cyclodienes and limited cross-resistance to fipronil is undetectable in field populations of house flies from the USA. Pestic. Biochem. Physiol. 88, 66-70 (2007).
44. Du, W. et al. Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Mol. Biol. 14, 179-183 (2005).
45. Nakao, T. et al. The A2'N mutation of the RDL gamma-aminobutyric acid receptor conferring fipronil resistance in Laodelphax striatellus (Hemiptera: Delphacidae). J. Econ. Entomol. 104, 646-652 (2011).
46. Nakao, T., Naoi, A., Kawahara, N., Hirase, K. Mutation of the GABA receptor associated with fipronil resistance in the whitebacked planthopper, Sogatella furcifera. Pestic. Biochem. Physiol. 97, 262-266 (2010).
47. Thompson, M., Steichen, J. C., ffrench-Constant, R. H. Conservation of cyclodiene insecticide resistance-associated mutations in insects. Insect Mol. Biol. 2, 149-154 (1993).
48. Jones, C. M. et al. Footprints of positive selection associated with a mutation (N1575Y) in the voltage-gated sodium channel of Anopheles gambiae. Proc. Natl. Acad. Sci. USA 109, 6614-6619 (2012).
49. Linss, J. G. et al. Distribution and dissemination of the Val1016Ile and Phe1534Cys Kdr mutations in Aedes aegypti Brazilian natural populations. Parasites & Vectors 7 (2014).
50. Menozzi, P., An Shi, M., Lougarre, A., Hua Tang, Z., Fournier, D. Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evol. Biol. 4, 1-7 (2004).
51. Shi, M. A. et al. Acetylcholinesterase alterations reveal the fitness cost of mutations conferring insecticide resistance. BMC Evol. Biol. 4 (2004).
52. Wang, Y. et al. Buprofezin susceptibility survey, resistance selection and preliminary determination of the resistance mechanism in Nilaparvata lugens (Homoptera: Delphacidae). Pest Manage. Sci. 64, 1050-1056 (2008).
53. Tang, J., Li, J., Shao, Y., Yang, B., Liu, Z. Fipronil resistance in the whitebacked planthopper (Sogatella furcifera): possible resistance mechanisms and cross-resistance. Pest Manage. Sci. 66, 121-125 (2010).
54. Liu, Z. W., Han, Z. J. Fitness costs of laboratory-selected imidacloprid resistance in the brown planthopper, Nilaparvata lugens Stål. Pest Manage. Sci. 62, 279-282 (2006).
55. Williamson, M. S., MartinezTorres, D., Hick, C. A., Devonshire, A. L. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol. Gen. Genet. 252, 51-60 (1996).
56. Liu, Z. et al. A nicotinic acetylcholine receptor mutation (Y151S) causes reduced agonist potency to a range of neonicotinoid insecticides. J. Neurochem. 99, 1273-1281 (2006).
57. Le Goff, G., Hamon, A., Bergé, J.-B., Amichot, M. Resistance to fipronil in Drosophila simulans: Influence of two point mutations in the RDL GABA receptor subunit.J. Neurochem. 92, 1295-1305 (2005).
58. Liu, Z. W. et al. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc. Natl. Acad. Sci. USA 102, 8420-8425 (2005).