Contributions of three-site mutations in acetylcholinesterase and cytochrome P450 to genetic variation in susceptibility to organophosphate insecticides within a natural population of Drosophila melanogaster
Tóm tắt
In this study, we attempted to elucidate the two resistance factors conferring resistance to organophosphates within the Katsunuma population of Drosophila melanogaster (Meigen), one of which has been mapped on the second chromosome and the other on the third chromosome. With regard to the second chromosome factor, we tested susceptibility to malathion of 54 recombinant inbred lines with recombination between ltd and vg. Analyses of variance (ANOVAs) showed highly significant variation in susceptibility to malathion between recombinant lines. In addition, susceptibility of the second-chromosome resistant line to malathion was increased with additional application of piperonyl butoxide, suggesting a member of the Cyp gene family located between ltd and vg. With regard to the third-chromosome factor, we conducted inhibition assays of acetylcholinesterase (AChE) with respect to fenitroxon and carbaryl, to evaluate the contribution of mutated AChE to organophosphate resistance within the Katsunuma population. I 50 values of resistant lines, isolated from this population, were about 15 times higher for fenitroxon, and about two times higher for carbaryl, than those of susceptible lines, suggesting the contribution of mutated AChE to organophosphate resistance within the Katsunuma population. We further investigated the genetic variation in the acetylcholinesterase (Ace) gene within the newly collected Katsunuma population, by using the allele-specific polymerase chain reaction (PCR) approach, and revealed that within this population there were high frequencies of resistant-type mutations at three sites in the Ace gene, which play critical roles in altering sensitivity of AChE to organophosphate and carbamate insecticides.
Tài liệu tham khảo
citation_journal_title=Eur J Biochem; citation_title=Point mutations associated with insecticide resistance in the Drosophila cytochrome P450 Cyp6a2 enable DDT metabolism; citation_author=M Amichot, S Tarès, A Brun-Barale, L Arthaud, J-M Bride, J-B Bergé; citation_volume=271; citation_publication_date=2004; citation_pages=1250-1257; citation_doi=10.1111/j.1432-1033.2004.04025.x; citation_id=CR1
citation_journal_title=Anal Biochem; citation_title=Discrimination of primer 3′-nucleotide mismatch by Taq DNA polymerase during polymerase chain reaction; citation_author=S Ayyadevara, JJ Thaden, RJ Shmookler Reis; citation_volume=284; citation_publication_date=2000; citation_pages=11-18; citation_doi=10.1006/abio.2000.4635; citation_id=CR2
citation_journal_title=J Toxicol Environ Health; citation_title=Insecticide synergists: role, importance, and perspectives; citation_author=CB Bernard, BJR Philogène; citation_volume=38; citation_publication_date=1993; citation_pages=199-223; citation_doi=10.1080/15287399309531712; citation_id=CR3
citation_journal_title=Pest Manag Sci; citation_title=Temporal synergism can enhance carbamate and neonicotinoid insecticidal activity against resistant crop pests; citation_author=G Bingham, RV Gunning, G Delogu, V Borzatta, LM Field, GD Moores; citation_volume=64; citation_publication_date=2008; citation_pages=81-85; citation_doi=10.1002/ps.1477; citation_id=CR4
citation_journal_title=Insect Mol Biol; citation_title=Differential expression and induction of two Drosophila cytochrome P450 genes near the Rst(2)DDT locus; citation_author=A Brandt, M Scharf, JHF Pedra, G Holmes, A Dean, M Kreitman, BR Pittendrigh; citation_volume=11; citation_publication_date=2002; citation_pages=337-341; citation_doi=10.1046/j.1365-2583.2002.00344.x; citation_id=CR5
citation_journal_title=Annu Rev Entomol; citation_title=Genetics of insect resistance to chemicals; citation_author=JF Crow; citation_volume=2; citation_publication_date=1957; citation_pages=227-246; citation_doi=10.1146/annurev.en.02.010157.001303; citation_id=CR7
citation_journal_title=Mol Genet Genomics; citation_title=DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid; citation_author=P Daborn, S Boundy, J Yen, B Pittendrigh, R ffrench-Constant; citation_volume=266; citation_publication_date=2001; citation_pages=556-563; citation_doi=10.1007/s004380100531; citation_id=CR8
citation_journal_title=Science; citation_title=A single P450 allele associated with insecticide resistance in Drosophila
; citation_author=PJ Daborn, JL Yen, MR Bogwitz, G Goff, E Feil, S Jeffers, N Tijet, T Perry, D Heckel, P Batterham, R Feyereisen, TG Wilson, RH ffrench-Constant; citation_volume=297; citation_publication_date=2002; citation_pages=2253-2256; citation_doi=10.1126/science.1074170; citation_id=CR9
citation_journal_title=Insect Biochem Mol Biol; citation_title=Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression; citation_author=PJ Daborn, C Lumb, A Boey, W Wong, RH ffrench-Constant, P Batterham; citation_volume=37; citation_publication_date=2007; citation_pages=512-519; citation_doi=10.1016/j.ibmb.2007.02.008; citation_id=CR10
citation_journal_title=Biochem Pharmacol; citation_title=A new and rapid colorimetric determination of acetylcholinesterase activity; citation_author=GL Ellman, KD Courtney, V Andres, RM Featherstone; citation_volume=7; citation_publication_date=1961; citation_pages=88-95; citation_doi=10.1016/0006-2952(61)90145-9; citation_id=CR11
citation_journal_title=Insect Mol Biol; citation_title=Expression of Cyp6g1 and Cyp12d1 in DDT resistant and susceptible strains of Drosophila melanogaster
; citation_author=RA Festucci-Buselli, AS Carvalho-Dias, M Oliveira-Andrade, C Caixeta-Nunes, H-M Li, JJ Stuart, W Muir, ME Scharf, BR Pittendrigh; citation_volume=14; citation_publication_date=2005; citation_pages=69-77; citation_doi=10.1111/j.1365-2583.2005.00532.x; citation_id=CR12
citation_journal_title=Trends Genet; citation_title=The genetics and genomics of insecticide resistance; citation_author=RH ffrench-Constant, PJ Daborn, G Le Goff; citation_volume=20; citation_publication_date=2004; citation_pages=163-170; citation_doi=10.1016/j.tig.2004.01.003; citation_id=CR13
citation_journal_title=Nucleic Acids Res; citation_title=The FlyBase database of the Drosophila genome projects and community literature; citation_author=Consortium FlyBase; citation_volume=31; citation_publication_date=2003; citation_pages=172-175; citation_id=CR6
citation_journal_title=Chem Biol Interact; citation_title=Mutations of acetylcholinesterase which confer insecticide resistance in insect populations; citation_author=D Fournier; citation_volume=157; citation_publication_date=2005; citation_pages=257-261; citation_doi=10.1016/j.cbi.2005.10.040; citation_id=CR14
citation_journal_title=Genes Genet Syst; citation_title=Further genetic studies on the Katsunuma population of Drosophila melanogaster
; citation_author=Y Hatano, Y Inoue, M Watada, SM Akai, TK Watanabe, M-T Yamamoto, K Hirai, H Takegawa, M Itoh; citation_volume=74; citation_publication_date=1999; citation_pages=219-225; citation_doi=10.1266/ggs.74.219; citation_id=CR15
citation_journal_title=Insect Biochem Mol Biol; citation_title=The molecular basis of insecticide resistance in mosquitoes; citation_author=J Hemingway, NJ Hawkes, L McCarroll, H Ranson; citation_volume=34; citation_publication_date=2004; citation_pages=653-665; citation_doi=10.1016/j.ibmb.2004.03.018; citation_id=CR16
citation_journal_title=Genet Res; citation_title=The inbreeding decline and average dominance of genes affecting male life-history characters in Drosophila melanogaster
; citation_author=KA Hughes; citation_volume=65; citation_publication_date=1995; citation_pages=41-52; citation_doi=10.1017/S0016672300032997; citation_id=CR17
citation_journal_title=Genome Res; citation_title=BLAT—The BLAST-like alignment tool; citation_author=WJ Kent; citation_volume=12; citation_publication_date=2002; citation_pages=656-664; citation_id=CR18
citation_journal_title=Pest Manag Sci; citation_title=A novel assay reveals the blockade of esterases by piperonyl butoxide; citation_author=AC Khot, G Bingham, LM Field, GD Moores; citation_volume=64; citation_publication_date=2008; citation_pages=1139-1142; citation_doi=10.1002/ps.1603; citation_id=CR19
citation_journal_title=Pestic Biochem Physiol; citation_title=Amino acid substitutions conferring insecticide insensitivity in Ace-paralogous acetylcholinesterase; citation_author=Y Kono, T Tomita; citation_volume=85; citation_publication_date=2006; citation_pages=123-132; citation_doi=10.1016/j.pestbp.2005.12.002; citation_id=CR20
citation_journal_title=Gene; citation_title=High expression of Cyp6g1, a cytochrome P450 gene, does not necessarily confer DDT resistance in Drosophila melanogaster
; citation_author=S Kuruganti, V Lam, X Zhou, G Bennett, BR Pittendrigh, R Ganguly; citation_volume=388; citation_publication_date=2007; citation_pages=43-53; citation_doi=10.1016/j.gene.2006.09.019; citation_id=CR21
citation_journal_title=Insect Biochem Mol Biol; citation_title=Microarray analysis of cytochrome P450 mediated insecticide resistance in Drosophila
; citation_author=G Goff, S Boundy, PJ Daborn, JL Yen, L Sofer, R Lind, C Sabourault, L Madi-Ravazzi, RH ffrench-Constant; citation_volume=33; citation_publication_date=2003; citation_pages=701-708; citation_doi=10.1016/S0965-1748(03)00064-X; citation_id=CR22
citation_journal_title=Annu Rev Entomol; citation_title=Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics; citation_author=X Li, MA Schuler, MR Berenbaum; citation_volume=52; citation_publication_date=2007; citation_pages=231-253; citation_doi=10.1146/annurev.ento.51.110104.151104; citation_id=CR23
citation_title=The genome of
; citation_publication_date=1992; citation_id=CR24; citation_author=D Lindsley; citation_author=GG Zimm; citation_publisher=Academic
citation_title=Genetics and analysis of quantitative traits; citation_publication_date=1998; citation_id=CR25; citation_author=M Lynch; citation_author=B Walsh; citation_publisher=Sinauer
citation_journal_title=Appl Entomol Zool; citation_title=Acetylcholinesterase in insecticide resistant Culex tritaeniorhynchus: characteristics accompanying insensitivity to inhibitors; citation_author=A Mamiya, Y Ishikawa, Y Kono; citation_volume=32; citation_publication_date=1997; citation_pages=37-44; citation_id=CR26
citation_journal_title=BMC Evol Biol; citation_title=Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations; citation_author=P Menozzi, MA Shi, A Lougarre, ZH Tang, D Fournier; citation_volume=4; citation_publication_date=2004; citation_pages=4; citation_doi=10.1186/1471-2148-4-4; citation_id=CR27
citation_journal_title=BMC Genet; citation_title=Density-independent population projection trajectories of chromosome-substituted lines resistant and susceptible to organophosphate insecticides in Drosophila melanogaster
; citation_author=T Miyo, B Charlesworth; citation_volume=5; citation_publication_date=2004; citation_pages=31; citation_doi=10.1186/1471-2156-5-31; citation_id=CR28
citation_journal_title=J Econ Entomol; citation_title=Negative correlations between resistance to three organophosphate insecticides and productivity within a natural population of Drosophila melanogaster (Diptera: Drosophilidae); citation_author=T Miyo, Y Oguma; citation_volume=95; citation_publication_date=2002; citation_pages=1229-1238; citation_doi=10.1603/0022-0493-95.6.1229; citation_id=CR29
citation_journal_title=Genes Genet Syst; citation_title=Seasonal fluctuation in susceptibility to insecticides within natural populations of Drosophila melanogaster: empirical observations of fitness costs of insecticide resistance; citation_author=T Miyo, S Akai, Y Oguma; citation_volume=75; citation_publication_date=2000; citation_pages=97-104; citation_doi=10.1266/ggs.75.97; citation_id=CR30
citation_journal_title=J Econ Entomol; citation_title=Genetic variation and correlations among responses to five insecticides within natural populations of Drosophila melanogaster (Diptera: Drosophilidae); citation_author=T Miyo, H Takamori, Y Kono, Y Oguma; citation_volume=94; citation_publication_date=2001; citation_pages=223-232; citation_doi=10.1603/0022-0493-94.1.223; citation_id=CR31
citation_journal_title=J Econ Entomol; citation_title=Genetic basis of cross-resistance to three organophosphate insecticides in Drosophila melanogaster (Diptera: Drosophilidae); citation_author=T Miyo, Y Kono, Y Oguma; citation_volume=95; citation_publication_date=2002; citation_pages=871-877; citation_doi=10.1603/0022-0493-95.5.871; citation_id=CR32
citation_journal_title=Genes Genet Syst; citation_title=The comparison of intrinsic rates of increase among chromosome-substituted lines resistant and susceptible to organophosphate insecticides in Drosophila melanogaster
; citation_author=T Miyo, Y Oguma, B Charlesworth; citation_volume=78; citation_publication_date=2003; citation_pages=373-382; citation_doi=10.1266/ggs.78.373; citation_id=CR33
citation_journal_title=Genes Genet Syst; citation_title=Seasonal fluctuation in susceptibility to insecticides within natural populations of Drosophila melanogaster. II. Features of genetic variation in susceptibility to organophosphate insecticides within natural populations of D. melanogaster
; citation_author=T Miyo, Y Oguma, B Charlesworth; citation_volume=81; citation_publication_date=2006; citation_pages=273-285; citation_doi=10.1266/ggs.81.273; citation_id=CR34
citation_journal_title=Genome; citation_title=Evolution of Drosophila insecticide resistance; citation_author=RA Morton; citation_volume=36; citation_publication_date=1993; citation_pages=1-7; citation_doi=10.1139/g93-001; citation_id=CR35
citation_journal_title=Genetics; citation_title=The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability; citation_author=T Mukai; citation_volume=50; citation_publication_date=1964; citation_pages=1-19; citation_id=CR36
citation_journal_title=Genetics; citation_title=The genetic variance for viability and its components in a local population of Drosophila melanogaster
; citation_author=T Mukai, RA Cardellino, TK Watanabe, JF Crow; citation_volume=78; citation_publication_date=1974; citation_pages=1195-1208; citation_id=CR37
citation_journal_title=Proc Natl Acad Sci USA; citation_title=Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase; citation_author=A Mutero, M Pralavorio, J-M Bride, D Fournier; citation_volume=91; citation_publication_date=1994; citation_pages=5922-5926; citation_doi=10.1073/pnas.91.13.5922; citation_id=CR38
citation_journal_title=Genome Biol; citation_title=The genomics of insecticide resistance; citation_author=JG Oakeshott, I Horne, TD Sutherland, RJ Russell; citation_volume=4; citation_publication_date=2003; citation_pages=202; citation_doi=10.1186/gb-2003-4-1-202; citation_id=CR39
citation_journal_title=Proc Natl Acad Sci USA; citation_title=Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila
; citation_author=JHF Pedra, LM McIntyre, ME Scharf, BR Pittendrigh; citation_volume=101; citation_publication_date=2004; citation_pages=7034-7039; citation_doi=10.1073/pnas.0400580101; citation_id=CR40
citation_journal_title=Genomics; citation_title=Molecular haplotype determination using allele-specific PCR and pyrosequencing technology; citation_author=M Pettersson, M Bylund, A Alderborn; citation_volume=82; citation_publication_date=2003; citation_pages=390-396; citation_doi=10.1016/S0888-7543(03)00177-0; citation_id=CR41
citation_journal_title=Nature Rev Genet; citation_title=Genotyping errors: causes, consequences and solutions; citation_author=F Pompanon, A Bonin, E Bellemain, P Taberlet; citation_volume=6; citation_publication_date=2005; citation_pages=847-859; citation_doi=10.1038/nrg1707; citation_id=CR42
citation_journal_title=Genetica; citation_title=The genetic basis of resistance to diazinon in natural populations of Drosophila melanogaster
; citation_author=FM Pyke, MR Bogwitz, T Perry, A Monk, P Batterham, JA McKenzie; citation_volume=121; citation_publication_date=2004; citation_pages=13-24; citation_doi=10.1023/B:GENE.0000019920.71944.2b; citation_id=CR43
citation_journal_title=Insect Biochem Mol Biol; citation_title=Dynamics of insecticide resistance alleles in house fly populations from New York and Florida; citation_author=FD Rinkevich, RL Hamm, CJ Geden, JG Scott; citation_volume=37; citation_publication_date=2007; citation_pages=550-558; citation_doi=10.1016/j.ibmb.2007.02.013; citation_id=CR44
citation_journal_title=Insect Biochem Mol Biol; citation_title=Cytochromes P450 and insecticide resistance; citation_author=JG Scott; citation_volume=29; citation_publication_date=1999; citation_pages=757-777; citation_doi=10.1016/S0965-1748(99)00038-7; citation_id=CR45
citation_journal_title=Pestic Sci; citation_title=Mechanisms responsible for high levels of permethrin resistance in the house fly; citation_author=JG Scott, GP Georghiou; citation_volume=17; citation_publication_date=1986; citation_pages=195-206; citation_doi=10.1002/ps.2780170302; citation_id=CR46
citation_journal_title=BMC Evol Biol; citation_title=Acetylcholinesterase alterations reveal the fitness cost of mutations conferring insecticide resistance; citation_author=MA Shi, A Lougarre, C Alies, I Frémaux, ZH Tang, J Stojan, D Fournier; citation_volume=4; citation_publication_date=2004; citation_pages=5; citation_doi=10.1186/1471-2148-4-5; citation_id=CR47
citation_title=Biometry; citation_publication_date=1995; citation_id=CR48; citation_author=RR Sokal; citation_author=FJ Rohlf; citation_publisher=Freeman
citation_journal_title=FEBS Lett; citation_title=Mutations in DIIS5 and the DIIS4–S5 linker of Drosophila melanogaster sodium channel define binding domains for pyrethroids and DDT; citation_author=PNR Usherwood, TGE Davies, IR Mellor, AO O’Reilly, F Peng, H Vais, BPS Khambay, LM Field, MS Williamson; citation_volume=581; citation_publication_date=2007; citation_pages=5485-5492; citation_doi=10.1016/j.febslet.2007.10.057; citation_id=CR49