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. 1998 Feb 15;330(Pt 1):169–173. doi: 10.1042/bj3300169

Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family.

L M Field 1, A L Devonshire 1
PMCID: PMC1219123  PMID: 9461506

Abstract

The amplification of genes encoding the esterases E4 and FE4 is a widespread mechanism of insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). We present evidence that in susceptible aphids the two genes are adjacent to each other in a head-to-tail arrangement with E4 upstream of FE4 and with approx. 19 kb of intervening sequence. There are also at least two other closely related sequences which might come from other members of an esterase gene family, in line with reports of other insect gene families encoding detoxifying enzymes. The close identity between E4 and FE4 genes indicates a recent duplication and divergence. The subsequent amplifications giving multiple copies of either E4 or FE4 must have involved two separate events, each probably occurring once and then being selected by insecticide exposure and spread by migration. The cloning of sequences upstream of the FE4 gene suggest, by comparison with E4, that the two genes are regulated in different ways. FE4 has sequences corresponding to a conventional promoter (TATA box and CAP site) that are not present in E4; on the other hand, FE4 lacks the CpG island present 5' of E4 genes that may control expression through changes in DNA methylation. The differences are likely to have occurred by the duplication event that gave rise to E4 and FE4 leading to different 5' sequences.

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Selected References

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  1. Bird A. P. Gene number, noise reduction and biological complexity. Trends Genet. 1995 Mar;11(3):94–100. doi: 10.1016/S0168-9525(00)89009-5. [DOI] [PubMed] [Google Scholar]
  2. Brady J. P., Richmond R. C. An evolutionary model for the duplication and divergence of esterase genes in Drosophila. J Mol Evol. 1992 Jun;34(6):506–521. doi: 10.1007/BF00160464. [DOI] [PubMed] [Google Scholar]
  3. Cohen M. B., Feyereisen R. A cluster of cytochrome P450 genes of the CYP6 family in the house fly. DNA Cell Biol. 1995 Jan;14(1):73–82. doi: 10.1089/dna.1995.14.73. [DOI] [PubMed] [Google Scholar]
  4. Field L. M., Crick S. E., Devonshire A. L. Polymerase chain reaction-based identification of insecticide resistance genes and DNA methylation in the aphid Myzus persicae (Sulzer). Insect Mol Biol. 1996 Aug;5(3):197–202. doi: 10.1111/j.1365-2583.1996.tb00054.x. [DOI] [PubMed] [Google Scholar]
  5. Field L. M., Devonshire A. L. Structure and organization of amplicons containing the E4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer). Biochem J. 1997 Mar 15;322(Pt 3):867–871. doi: 10.1042/bj3220867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Field L. M., Devonshire A. L., Tyler-Smith C. Analysis of amplicons containing the esterase genes responsible for insecticide resistance in the peach-potato aphid Myzus persicae (Sulzer). Biochem J. 1996 Jan 15;313(Pt 2):543–547. doi: 10.1042/bj3130543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Field L. M., Williamson M. S., Moores G. D., Devonshire A. L. Cloning and analysis of the esterase genes conferring insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). Biochem J. 1993 Sep 1;294(Pt 2):569–574. doi: 10.1042/bj2940569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fryxell K. J. The coevolution of gene family trees. Trends Genet. 1996 Sep;12(9):364–369. doi: 10.1016/s0168-9525(96)80020-5. [DOI] [PubMed] [Google Scholar]
  9. Hick C. A., Field L. M., Devonshire A. L. Changes in the methylation of amplified esterase DNA during loss and reselection of insecticide resistance in peach-potato aphids, Myzus persicae. Insect Biochem Mol Biol. 1996 Jan;26(1):41–47. doi: 10.1016/0965-1748(95)00059-3. [DOI] [PubMed] [Google Scholar]
  10. Maitra S., Dombrowski S. M., Waters L. C., Ganguly R. Three second chromosome-linked clustered Cyp6 genes show differential constitutive and barbital-induced expression in DDT-resistant and susceptible strains of Drosophila melanogaster. Gene. 1996 Nov 21;180(1-2):165–171. doi: 10.1016/s0378-1119(96)00446-5. [DOI] [PubMed] [Google Scholar]
  11. Maroni G., Wise J., Young J. E., Otto E. Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics. 1987 Dec;117(4):739–744. doi: 10.1093/genetics/117.4.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Newcomb R. D., Campbell P. M., Ollis D. L., Cheah E., Russell R. J., 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. 1997 Jul 8;94(14):7464–7468. doi: 10.1073/pnas.94.14.7464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Newcomb R. D., Campbell P. M., Russell R. J., Oakeshott J. G. cDNA cloning, baculovirus-expression and kinetic properties of the esterase, E3, involved in organophosphorus resistance in Lucilia cuprina. Insect Biochem Mol Biol. 1997 Jan;27(1):15–25. doi: 10.1016/s0965-1748(96)00065-3. [DOI] [PubMed] [Google Scholar]
  14. Robin C., Russell R. J., Medveczky K. M., Oakeshott J. G. Duplication and divergence of the genes of the alpha-esterase cluster of Drosophila melanogaster. J Mol Evol. 1996 Sep;43(3):241–252. doi: 10.1007/BF02338832. [DOI] [PubMed] [Google Scholar]
  15. Roelofs H., Nederlof P. M., Tasseron-de Jong J. G., van de Putte P., Giphart-Gassler M. Gene amplification in human cells may involve interchromosomal transposition and persistence of the original DNA region. New Biol. 1992 Jan;4(1):75–86. [PubMed] [Google Scholar]
  16. Rooker S., Guillemaud T., Bergé J., Pasteur N., Raymond M. Coamplification of esterase A and B genes as a single unit in Culex pipiens mosquitoes. Heredity (Edinb) 1996 Nov;77(Pt 5):555–561. [PubMed] [Google Scholar]
  17. Russell R. J., Robin G. C., Kostakos P., Newcomb R. D., Boyce T. M., Medveczky K. M., Oakeshott J. G. Molecular cloning of an alpha-esterase gene cluster on chromosome 3r of Drosophila melanogaster. Insect Biochem Mol Biol. 1996 Mar;26(3):235–247. doi: 10.1016/0965-1748(95)00081-x. [DOI] [PubMed] [Google Scholar]
  18. Theodore L., Ho A. S., Maroni G. Recent evolutionary history of the metallothionein gene Mtn in Drosophila. Genet Res. 1991 Dec;58(3):203–210. doi: 10.1017/s0016672300029955. [DOI] [PubMed] [Google Scholar]
  19. Triglia T., Peterson M. G., Kemp D. J. A procedure for in vitro amplification of DNA segments that lie outside the boundaries of known sequences. Nucleic Acids Res. 1988 Aug 25;16(16):8186–8186. doi: 10.1093/nar/16.16.8186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Vaughan A., Hawkes N., Hemingway J. Co-amplification explains linkage disequilibrium of two mosquito esterase genes in insecticide-resistant Culex quinquefasciatus. Biochem J. 1997 Jul 15;325(Pt 2):359–365. doi: 10.1042/bj3250359. [DOI] [PMC free article] [PubMed] [Google Scholar]

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