Organophosphates' resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase

Insect Biochemistry and Molecular Biology

Volumn 38, Issue 10, 2008, Pages 940-949

  Alon, Michal ^a   Alon, Fishel ^a   Nauen, Ralf ^b   Morin, Shai ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b BAYER CROPSCIENCE AG   (Germany)

Author keywords

Acetylcholinesterase; Bemisia tabaci; Carboxylesterase; Insecticide resistance; Metabolic resistance; Organophosphates; Target site resistance

Indexed keywords

ACETYLCHOLINESTERASE; CARBOXYLESTERASE; INSECTICIDE; ORGANOPHOSPHATE; PESTICIDE;

ANIMAL; ARTICLE; ENZYMOLOGY; FEMALE; GENE DOSAGE; GENETICS; HAPLOIDY; HEMIPTERA; INSECTICIDE RESISTANCE; ISOLATION AND PURIFICATION; METABOLISM; NUCLEOTIDE SEQUENCE; POINT MUTATION; POLYMERASE CHAIN REACTION;

ACETYLCHOLINESTERASE; ANIMALS; CARBOXYLESTERASE; DNA MUTATIONAL ANALYSIS; FEMALE; GENE DOSAGE; HAPLOIDY; HEMIPTERA; INSECTICIDE RESISTANCE; INSECTICIDES; PESTICIDE SYNERGISTS; PHOSPHORIC ACID ESTERS; POINT MUTATION; POLYMERASE CHAIN REACTION;

ALEYRODIDAE; BEMISIA TABACI; CULEX TRITAENIORHYNCHUS; HEMIPTERA; TORPEDO CALIFORNICA;

EID: 50849127484     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2008.07.007     Document Type: Article

References (73)

1. Aldridge W.N. Some properties of specific cholinesterase with particular reference to the mechanism of inhibition by diethyl p-nitrophenyl thiophosphate (E 605) and analogues. Biochem. J. 46 (1950) 451-460
2. Alon M., Benting J., Lueke B., Ponge T., Alon F., and Morin S. Multiple origins of pyrethroid resistance in sympatric biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Insect Biochem. Mol. Biol. 36 (2006) 71-79
3. Alout H., Berthomieu A., Hadjivassilis A., and Weill M. A new amino-acid substitution in acetylcholinesterase 1 confers insecticide resistance to Culex pipiens mosquitoes from Cyprus. Insect Biochem. Mol. Biol. 37 (2007) 41-47
4. Baek J.H., Kim J.I., Lee D.W., Chung B.K., Miyata T., and Lee S.H. Identification and characterization of ace1-type acetylcholinesterase likely associated with organophosphate resistance in Plutella xylostella. Pestic. Biochem. Physiol. 81 (2005) 164-175
5. Baxter G.D., and Barker S.C. Analysis of the sequence and expression of a second putative acetylcholinesterase cDNA from organophosphate-susceptible and organophosphate-resistant cattle ticks. Insect Biochem. Mol. Biol. 32 (2002) 815-820
6. Benting J., and Nauen R. Biochemical evidence that an S431F mutation in acetylcholinesterase-1 of Aphis gossypii mediates resistance to pirimicarb and omethoate. Pest Manag. Sci. 60 (2004) 1051-1055
7. Brown J.K., Frohlich D.R., and Rosell R.C. The sweet-potato or silverleaf whiteflies - biotypes of Bemisia tabaci or a species complex. Annu. Rev. Entomol. 40 (1995) 511-534
8. Byrne F.J., Cahill M., Denholm I., and Devonshire A.L. A biochemical and toxicological study of the role of insensitive acetylcholinesterase in organophosphorus resistant Bemisia tabaci (Homoptera, Aleyrodidae) from Israel. Bull. Entomol. Res. 84 (1994) 179-184
9. Byrne F.J., and Devonshire A.L. In vivo inhibition of esterase and acetylcholinesterase activities by profenofos treatments in the tobacco whitefly Bemisia tabaci (Genn) - implications for routine biochemical monitoring of these enzymes. Pestic. Biochem. Physiol. 40 (1991) 198-204
10. Byrne F.J., and Devonshire A.L. Insensitive acetylcholinesterase and esterase polymorphism in susceptible and resistant populations of the tobacco whitefly Bemisia tabaci (Genn). Pestic. Biochem. Physiol. 45 (1993) 34-42
11. Byrne F.J., and Devonshire A.L. Kinetics of insensitive acetylcholinesterases in organophosphate-resistant tobacco whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Pestic. Biochem. Physiol. 58 (1997) 119-124
12. Byrne F.J., Gorman K.J., Cahill M., Denholm I., and Devonshire A.L. The role of B-type esterases in conferring insecticide resistance in the tobacco whitefly, Bemisia tabaci (Genn). Pest Manag. Sci. 56 (2000) 867-874
13. Cahill M., Byrne F.J., German K., Denholm I., and Devonshire A.L. Pyrethroid and organophosphate resistance in the tobacco whitefly Bemisia tabaci (Homoptera, Aleyrodidae). Bull. Entomol. Res. 85 (1995) 181-187
14. Campbell P.M., Newcomb R.D., Russell R.J., and Oakeshott J.G. Two different amino acid substitutions in the ali-esterase, E3 confer alternative types of organophosphorus insecticide resistance in the sheep blowfly, Lucilia cuprina. Insect Biochem. Mol. Biol. 28 (1998) 139-150
15. Carino F.A., Koener J.F., Plapp F.W., and Feyereisen R. Constitutive overexpression of the cytochrome P450 gene cyp6a1 in a house-fly strain with metabolic resistance to insecticides. Insect Biochem. Mol. Biol. 24 (1994) 411-418
16. Claudianos C., Russell R.J., and Oakeshott J.G. The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochem. Mol. Biol. 29 (1999) 675-686
17. Dellaporta S.L., Wood J., and Hicks J.B. A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1 (1983) 19-21
18. Denholm I., Cahill M., Byrne F.J., and Devonshire A.L. Progress with documenting and combating insecticide resistance in Bemisia. In: Gerling D., and Mayer R.T. (Eds). Bemisia 1995: Taxonomy, Biology, Damage, Control and Management (1996), Intercept, Andover, UK 577-602
19. Denholm I., Cahill M., Dennehy T.J., and Horowitz A.R. Challenges with managing insecticide resistance in agricultural pests, exemplified by the whitefly Bemisia tabaci. Philos. Trans. R. Soc. B 353 (1998) 1757-1767
20. Devonshire A.L., and Field L.M. Gene amplification and insecticide resistance. Annu. Rev. Entomol. 36 (1991) 1-23
21. Devonshire A.L., and Moores G.D. A carboxylesterase with broad substrate-specificity causes organo-phosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae). Pestic. Biochem. Physiol. 18 (1982) 235-246
22. Devonshire A.L., and Moores G.D. Characterization of insecticide-insensitive acetylcholinesterase - microcomputer-based analysis of enzyme-inhibition in homogenates of individual housefly (Musca domestica) heads. Pestic. Biochem. Physiol. 21 (1984) 341-348
23. Dittrich V., Ernst G.H., Ruesch O., and Uk S. Resistance mechanisms in sweet-potato whitefly (Homoptera, Aleyrodidae) populations from Sudan, Turkey, Guatemala, and Nicaragua. J. Econ. Entomol. 83 (1990) 1665-1670
24. Dombrowski S.M., Krishnan R., Witte M., Maitra S., Diesing C., Waters L.C., and Ganguly R. Constitutive and barbital-induced expression of the cyp6a2 allele of a high producer strain of cyp6a2 in the genetic background of a low producer strain. Gene 221 (1998) 69-77
25. Elbert A., and Nauen R. Resistance of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides in southern Spain with special reference to neonicotinoids. Pest Manag. Sci. 56 (2000) 60-64
26. Ellman G.L., Courtney K.D., Andres V., and Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7 (1961) 88-95
27. Ffrench-Constant R.H., Park Y., and Feyereisen R. Molecular biology of insecticide resistance. In: Puga A., and Wallace K.B. (Eds). Molecular Biology of Toxic Response (1998), Taylor and Francis, Philadelphia 533-555
28. Field L.M., Blackman R.L., Tyler-Smith C., and Devonshire A.L. Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochem. J. 339 (1999) 737-742
29. Field L.M., Devonshire A.L., Ffrench-Constant R.H., and Forde B.G. Changes in DNA methylation are associated with loss of insecticide resistance in the peach-potato aphid Myzus persicae (Sulz). FEBS Lett. 243 (1989) 323-327
30. Field L.M., Williamson M.S., Moores G.D., and Devonshire A.L. Cloning and analysis of the esterase genes conferring insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). Biochem. J. 294 (1993) 569-574
31. Fournier D. Mutations of acetylcholinesterase which confer insecticide resistance in insect populations. Chem. Biol. Interact. 157 (2005) 257-261
32. Fournier D., and Mutero A. Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comp. Biochem. Physiol., C: Comp. Pharmacol. Toxicol. 108 (1994) 19-31
33. Gao J.R., Kambhampati S., and Zhu K.Y. Molecular cloning and characterization of a greenbug (Schizaphis graminum) cDNA encoding acetylcholinesterase possibly evolved from a duplicate gene lineage. Insect Biochem. Mol. Biol. 32 (2002) 765-775
34. Ginzinger D.G. Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp. Hematol. 30 (2002) 503-512
35. Guillemaud T., Makate N., Raymond M., Hirst B., and Callaghan A. Esterase gene amplification in Culex pipiens. Insect Mol. Biol. 6 (1997) 319-327
36. Heidari R., Devonshire A.L., Campbell B.E., Bell K.L., Dorrian S.J., Oakeshott J.G., and Russell R.J. Hydrolysis of organophosphorus insecticides by in vitro modified carboxylesterase E3 from Lucilia cuprina. Insect Biochem. Mol. Biol. 34 (2004) 353-363
37. Hemingway J., and Karunaratne S. Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med. Vet. Entomol. 12 (1998) 1-12
38. Hosea N.A., Berman H.A., and Taylor P. Specificity and orientation of trigonal carboxyl esters and tetrahedral alkylphosphonyl esters in cholinesterases. Biochemistry 34 (1995) 11528-11536
39. Huchard E., Martinez M., Alout H., Douzery E.J.P., Lutfalla G., Berthomieu A., Berticat C., Raymond M., and Weill M. Acetylcholinesterase genes within the diptera: takeover and loss in true flies. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 273 (2006) 2595-2604
40. Ishaaya I., Mendelson Z., Ascher K.R.S., and Casida J.E. Cypermethrin synergism by pyrethroid esterase inhibitors in adults of the whitefly Bemisia tabaci. Pestic. Biochem. Physiol. 28 (1987) 155-162
41. Javed N., Viner R., Williamson M.S., Field L.M., Devonshire A.L., and Moores G.D. Characterization of acetylcholinesterases, and their genes, from the hemipteran species Myzus persicae (Sulzer), Aphis gossypii (Glover), Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood). Insect Mol. Biol. 12 (2003) 613-620
42. Kozaki T., Shono T., Tomita T., and Kono Y. Fenitroxon insensitive acetylcholinesterases of the housefly, Musca domestica associated with point mutations. Insect Biochem. Mol. Biol. 31 (2001) 991-997
43. Lee D.W., Kim S.S., Shin S.W., Kim W.T., and Boo K.S. Molecular characterization of two acetylcholinesterase genes from the oriental tobacco budworm, Helicoverpa assulta (Guenee). Biochim. Biophys. Acta. 1760 (2006) 125-133
44. Li X.C., Schuler M.A., and Berenbaum M.R. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52 (2007) 231-253
45. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001) 402-408
46. McCaffery A., and Nauen R. The insecticide resistance action committee (IRAC): public responsibility and enlightened industrial self-interest. Outlooks Pest Manag. 17 (2006) 11-14
47. Menozzi P., Shi M.A., Lougarre A., Tang Z.H., and Fournier D. Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evol. Biol. 4 (2004)
48. Mutero A., Pralavorio M., Bride J.M., and Fournier D. Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 5922-5926
49. Nabeshima T., Kozaki T., Tomita T., and Kono Y. An amino acid substitution on the second acetylcholinesterase in the pirimicarb-resistant strains of the peach potato aphid, Myzus persicae. Biochem. Biophys. Res. Commun. 307 (2003) 15-22
50. Nabeshima T., Mori A., Kozaki T., Iwata Y., Hidoh O., Harada S., Kasai S., Severson D.W., Kono Y., and Tomita T. An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochem. Biophys. Res. Commun. 313 (2004) 794-801
51. Newcomb R.D., Campbell P.M., Ollis D.L., Cheah E., Russell R.J., and Oakeshott J.G. A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7464-7468
52. Newcomb R.D., Gleeson D.M., Yong C.G., Russell R.J., and Oakeshott J.G. Multiple mutations and gene duplications conferring organophosphorus insecticide resistance have been selected at the rop-1 locus of the sheep blowfly, Lucilia cuprina. J. Mol. Evol. 60 (2005) 207-220
53. Oakeshott J.G., Devonshire A.L., Claudianos C., Sutherland T.D., Horne I., Campbell P.M., Ollis D.L., and Russell R.J. Comparing the organophosphorus and carbamate insecticide resistance mutations in cholin- and carboxyl-esterases. Chem. Biol. Interact. 157 (2005) 269-275
54. Oh S.H., Kozaki T., Mizuno H., Tomita T., and Kono Y. Expression of ace-paralogous acetylcholinesterase of Culex tritaeniorhynchus with an amino acid substitution conferring insecticide insensitivity in baculovirus-insect cell system. Pestic. Biochem. Physiol. 85 (2006) 46-51
55. Oliveira M.R.V., Henneberry T.J., and Anderson P. History, current status, and collaborative research projects for Bemisia tabaci. Crop. Prot. 20 (2001) 709-723
56. Oppenoorth F.J., and van Asperen K. Allelic genes in the housefly producing modified enzymes that cause organophosphate resistance. Science 132 (1960) 298-299
57. Palumbo J.C., Horowitz A.R., and Prabhaker N. Insecticidal control and resistance management for Bemisia tabaci. Crop. Prot. 20 (2001) 739-765
58. Paton M.G., Karunaratne S., Giakoumaki E., Roberts N., and Hemingway J. Quantitative analysis of gene amplification in insecticide-resistant Culex mosquitoes. Biochem. J. 346 (2000) 17-24
59. Prabhaker N., Coudriet D.L., and Toscano N.C. Effect of synergists on organo-phosphate and permethrin resistance in sweetpotato whitefly (Homoptera, Aleyrodidae). J. Econ. Entomol. 81 (1988) 34-39
60. Ranson H., Jensen B., Wang X., Prapanthadara L., Hemingway J., and Collins F.H. Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Mol. Biol. 9 (2000) 499-507
61. Raymond M., Poulin E., Boiroux V., Dupont E., and Pasteur N. Stability of insecticide resistance due to amplification of esterase genes in Culex pipiens. Heredity 70 (1993) 301-307
62. Russell R.J., Claudianos C., Campbell P.M., Horne I., Sutherland T.D., and Oakeshott J.G. Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides. Pestic. Biochem. Physiol. 79 (2004) 84-93
63. Scott J.G., Liu N.N., Wen Z.M., Smith F.F., Kasai S., and Horak C.E. House-fly cytochrome p450 cyp6d1: 5′ flanking sequences and comparison of alleles. Gene 226 (1999) 347-353
64. Shi M.A., Lougarre A., Alies C., Fremaux I., Tang Z.H., Stojan J., and Fournier D. Acetylcholinesterase alterations reveal the fitness cost of mutations conferring insecticide resistance. BMC Evol. Biol. 4 (2004)
65. Siegfried B.D., and Scharf M.E. Mechanisms of organophosphate resistance in insects. In: Ishaaya I. (Ed). Biochemical Sites of Insecticide Action and Resistance (2001), Springer-Verlag, Heidelberg 269-291
66. Stumpf N., and Nauen R. Biochemical markers linked to abamectin resistance in Tetranychus urticae (Acari: Tetranychidae). Pestic. Biochem. Physiol. 72 (2002) 111-121
67. Toda S., Komazaki S., Tomita T., and Kono Y. Two amino acid substitutions in acetylcholinesterase associated with pirimicarb and organophosphorous insecticide resistance in the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae). Insect Mol. Biol. 13 (2004) 549-553
68. Vaughan A., and Hemingway J. Mosquito carboxylesterase est-alpha-2(1)(a(2)) - cloning and sequence of the full-length cDNA for a major insecticide resistance gene worldwide in the mosquito Culex quinquefasciatus. J. Biol. Chem. 270 (1995) 17044-17049
69. Vaughan A., Rocheleau T., and Ffrench-Constant R. Site-directed mutagenesis of an acetylcholinesterase gene from the yellow fever mosquito Aedes aegypti confers insecticide insensitivity. Exp. Parasitol. 87 (1997) 237-244
70. Weill M., Fort P., Berthomieu A., Dubois M.P., Pasteur N., and Raymond M. A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 269 (2002) 2007-2016
71. Weill M., Malcolm C., Chandre F., Mogensen K., Berthomieu A., Marquine M., and Raymond M. The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol. Biol. 13 (2004) 1-7
72. Weng H., Pan A.H., Yang L.T., Zhang C.M., Liu Z.L., and Zhang D.B. Estimating number of transgene copies in transgenic rapeseed by real-time PCR assay with HMG I/Y as an endogenous reference gene. Plant Mol. Biol. Rep. 22 (2004) 289-300
73. Zhu Y.C., Dowdy A.K., and Baker J.E. Differential mRNA expression levels and gene sequences of a putative carboxylesterase-like enzyme from two strains of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Insect Biochem. Mol. Biol. 29 (1999) 417-425