DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid

Daborn, Phillip J.; Boundy, Sam; Yen, Janet L.; Pittendrigh, Barry R.; ffrench-Constant, Richard H.

doi:10.1007/s004380100531

Cited by 259 publications

(247 citation statements)

References 14 publications

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“…4). As expected (12,33), all Accord insertion lines had substantially higher levels of Cyp6g1 transcript. These data are consistent with the hypothesis that both the D. simulans Doc insertion and the D. melanogaster Accord insertion cause constitutive Cyp6g1 up-regulation.…”

Section: Resultssupporting

confidence: 77%

“…The Accord insertion occurs Ϸ300 bp upstream of the transcription start site (1. (12,33), suggesting that mutations increasing transcript abundance of Cyp6g1 might be favored in certain environments. We compared Cyp6g1 mRNA transcript levels in adult flies from Californian D. simulans lines homozygous for the Doc insertion (n ϭ 3) and African D. simulans lines homozygous for absence of the insertion (n ϭ 3) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…D. simulans and D. melanogaster lines were tested for resistance to the insecticide DDT by using a contact assay (12). Glass scintillation vials were coated with DDT by rolling 200 l of acetone containing 20 g of DDT inside the vials until the acetone evaporated.…”

Section: Estimation Of Selection Coefficientmentioning

confidence: 99%

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Strong selective sweep associated with a transposon insertion inDrosophila simulans

Schlenke

Begun

2004

Proc. Natl. Acad. Sci. U.S.A.

223

190

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We know little about several important properties of beneficial mutations, including their mutational origin, their phenotypic effects (e.g., protein structure changes vs. regulatory changes), and the frequency and rapidity with which they become fixed in a population. One signature of the spread of beneficial mutations is the reduction of heterozygosity at linked sites. Here, we present population genetic data from several loci across chromosome arm 2R in Drosophila simulans. A 100-kb segment from a freely recombining region of this chromosome shows extremely reduced heterozygosity in a California population sample, yet typical levels of divergence between species, suggesting that at least one episode of strong directional selection has occurred in the region. The 5 flanking sequence of one gene in this region, Cyp6g1 (a cytochrome P450), is nearly fixed for a Doc transposable element insertion. Presence of the insertion is correlated with increased transcript abundance of Cyp6g1, a phenotype previously shown to be associated with insecticide resistance in Drosophila melanogaster. Surveys of nucleotide variation in the same genomic region in an African D. simulans population revealed no evidence for a high-frequency Doc element and no evidence for reduced polymorphism. These data are consistent with the notion that the Doc element is a geographically restricted beneficial mutation. Data from D. simulans Cyp6g1 are paralleled in many respects by data from its sister species D. melanogaster.T he spread of beneficial mutations is expected to reduce variation at linked sites, a phenomenon known as genetic hitchhiking (1, 2). All else being equal, the size of the swept region depends on the selection coefficient of the beneficial mutant and the local recombination rate. Theoretical results show that for regions of normal recombination in Drosophila, hitchhiking effects associated with moderately strong selection should result in localized regions of reduced heterozygosity (3). Thus, in principle, the frequency and locations of selective sweeps can be determined by scanning chromosomes for ''valleys'' of reduced variation (4). The paucity of large genomic regions of severely reduced heterozygosity from recombining regions in Drosophila and other organisms (4-7) suggests that novel mutations with large positive selection coefficients are rare, although it does not rule out the evolutionary importance of such mutations.In this study, we document the existence of a 100-kb chromosomal region that has extremely reduced heterozygosity in a Drosophila simulans population sample from California, but not in a sample from Africa, indicating the recent and geographically restricted sweep of a unique, beneficial mutation. Furthermore, we report the unusual observation of an intact transposable element in this region, which occurs at very high frequency in the California, but not Africa, sample. The transposon insertion is associated with increased transcript abundance of the downstream cytochrome P450 gene Cyp6g1. These data are...

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Section: Resultssupporting

confidence: 77%

Section: Resultsmentioning

confidence: 99%

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Strong selective sweep associated with a transposon insertion inDrosophila simulans

Schlenke

Begun

2004

Proc. Natl. Acad. Sci. U.S.A.

223

190

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“…In early genetic studies in Drosophila, dichlorodiphenyltrichloroethane (DDT) resistance was mapped to multiple locations on chromosomes II and III (8)(9)(10)(11)(12)(13)(14)). Subsequently, low-level DDT resistance was mapped to 64.5 Ϯ 2 centiMorgans on the second chromosome (15), a locus (loci) known as Rst (2)DDT.…”

mentioning

confidence: 99%

Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila

Pedra

McIntyre

Scharf

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

213

268

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Genome-wide microarray analysis (Affymetrix array) was used (i) to determine whether only one gene, the cytochrome P450 enzyme Cyp6g1, is differentially transcribed in dichlorodiphenyltrichloroethane (DDT)-resistant vs. -susceptible Drosophila; and (ii) to profile common genes differentially transcribed across a DDT-resistant field isolate [Rst(2)DDT Wisconsin ] and a laboratory DDT-selected population [Rst(2)DDT 91-R ]. Statistical analysis (ANOVA model) identified 158 probe sets that were differentially transcribed among Rst(2)DDT 91-R , Rst(2)DDT Wisconsin , and the DDT-susceptible genotype Canton-S (P < 0.01). The cytochrome P450 Cyp6a2 and the diazepam-binding inhibitor gene (Dbi) were over transcribed in the two DDT-resistant genotypes when compared to the wild-type Drosophila, and this difference was significant at the most stringent statistical level, a Bonferroni correction. The list of potential candidates differentially transcribed also includes 63 probe sets for which molecular function ontology annotation of the probe sets did not exist. A total of four genes (Cyp6a2, Dbi, Uhg1, and CG11176) were significantly different (P < 5.6 e ؊06 ) between Rst(2)DDT 91-R and Canton-S. Additionally, two probe sets encoding Cyp12d1 and Dbi were significantly different between Rst(2)DDT Wisconsin and Canton-S after a Bonferroni correction. Fifty-two probe sets, including those associated with pesticide detoxification, ion transport, signal transduction, RNA transcription, and lipid metabolism, were commonly expressed in both resistant lines but were differentially transcribed in Canton-S. Our results suggest that more than Cyp6g1 is overtranscribed in field and laboratory DDT-resistant genotypes, and the number of commonalities suggests that similar resistance mechanisms may exist between laboratory-and field-selected DDT-resistant fly lines.T he evolution of insecticide resistance is often, but not always, based on major effect alleles (1-4). It has been hypothesized that high selection pressure in the field will favor monogenic forms of pesticide resistance, and that selection for resistance in the laboratory will favor polygenic resistance (5-7). In early genetic studies in Drosophila, dichlorodiphenyltrichloroethane (DDT) resistance was mapped to multiple locations on chromosomes II and III (8-14). Subsequently, low-level DDT resistance was mapped to 64.5 Ϯ 2 centiMorgans on the second chromosome (15), a locus (loci) known as Rst(2)DDT.Recently, Daborn et al. (16) suggested that resistance to DDT in the field is monogenic and is due to the overexpression of a single P450 gene, Cyp6g1. Le Goff et al. (17) suggested that resistance in field isolates of both Drosophila melanogaster and Drosophila simulans is associated with overtranscription of Cyp6g1, whereas prolonged laboratory selection with DDT apparently coselects additional genes such as Cyp12d1 (18) To date, no genome-wide expression profile has been evaluated to investigate the extent to which gene transcription varies between genotypes that are resis...

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“…However, it has been shown that TE insertions in the proximity of Cyps can alter their regulation and cause the over-expression of CYP enzymes, resulting in insecticide resistance (Catania et al, 2004;Daborn et al, 2001Daborn et al, , 2002Jouben et al, 2008). TE insertions could therefore also be a source of genetic variability, and the regulatory motifs they provide could be advantageous for organisms in responding to external stimuli.…”

Section: Discussionmentioning

confidence: 99%

Genomic regions harboring insecticide resistance-associated Cyp genes are enriched by transposable element fragments carrying putative transcription factor binding sites in two sibling Drosophila species

Carareto

Hernandez

Vieira

2014

Gene

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a b s t r a c tIn the present study, an in silico analysis was performed to identify transposable element (TE) fragments inserted in Cyps with functions associated with resistance to insecticides and developmental regulation as well as in neighboring genes in two sibling species , Drosophila melanogaster and Drosophila simulans . The Cyps associated with insecticide resistance and their neighboring non-Cyp genes have accumulated a greater number of TE fragments than the other Cyps or a random sample of genes, predominantly in the 5′-flanking regions. Most of the insertions were due to DNA transposons, with DNAREP1 fragments being the most common. These fragments carry putative binding sites for transcription factors, which reinforces the hypothesis that DNAREP1 may influence gene regulation and play a role in the adaptation of the Drosophila species.

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DDT resistance in Drosophila correlates with Cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid

Cited by 259 publications

References 14 publications

Strong selective sweep associated with a transposon insertion inDrosophila simulans

Strong selective sweep associated with a transposon insertion inDrosophila simulans

Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila

Genomic regions harboring insecticide resistance-associated Cyp genes are enriched by transposable element fragments carrying putative transcription factor binding sites in two sibling Drosophila species

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