Evidence for a functional interaction between the Bari1 transposable element and the cytochrome P450 cyp12a4 gene in Drosophila melanogaster

Marsano, Renè Massimiliano; Caizzi, Ruggiero; Moschetti, Roberta; Junakovic, Nikolaj

doi:10.1016/j.gene.2005.06.005

Cited by 29 publications

(36 citation statements)

References 30 publications

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“…This possibility is further strengthened by a recent study demonstrating that insertions by various forms of a truncated on-LTR retrotransposon in the 5'-flanking sequence of CYP51 (encoding a 14α-demethylase) lead to overexpression of CYP51 and sterol demethylation inhibitor fungicide resistance in the cherry leaf spot pathogen Blumeriella jaapii [65]. In the case of the D. melanogaster CYP12A4, the insertion of Bari1 in the 3' UTR results in 10-fold overexpression of CYP12A4 but no resistance to DDT [66], indicating that DDT is not a substrate of CYP12A4. Given that overexpression of CYP12A4 confers resistance to lufenuron [34], it is possible the Bari1 insertion in the 3' UTR of CYP12A4 will lead to resistance to lufenuron even other insecticides or plant toxins.…”

Section: Cyp302a1mentioning

confidence: 96%

Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes

Chen

2007

BMC Evol Biol

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Background: Transposons, i.e. transposable elements (TEs), are the major internal spontaneous mutation agents for the variability of eukaryotic genomes. To address the general issue of whether transposons mediate genomic changes in environment-adaptation genes, we scanned two alleles per each of the six xenobiotic-metabolizing Helicoverpa zea cytochrome P450 loci, including CYP6B8, CYP6B27, CYP321A1, CYP321A2, CYP9A12v3 and CYP9A14, for the presence of transposon insertions by genome walking and sequence analysis. We also scanned thirteen Drosophila melanogaster P450s genes for TE insertions by in silico mapping and literature search.

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Section: Cyp302a1mentioning

confidence: 96%

Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes

Chen

2007

BMC Evol Biol

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“…TEs can cause mutations by inserting into the coding regions of genes and disrupting or altering gene function. There are also examples of TEs inserting into the untranslated regions (UTRs) of genes, changing transcript length and stability (Landry et al 2002;Dunn et al 2003;Marsano et al 2005). Insertions of TEs into the regulatory regions of genes can also disrupt or alter gene expression, by introducing regulatory elements such as enhancers (Argeson et al 1996;Conte et al 2002) or insulators (Gdula et al 1996;Conte et al 2002;Parnell et al 2003).…”

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confidence: 99%

“…There has been a long predicted role of TEs in the evolution of insecticide resistance (Wilson 1993). However, it is only recently that resistance mechanisms potentially involving TEs have been identified in natural insect populations (ffrench-Constant et al 2006), where resistance is associated with either the deletion or the inactivation of an insecticide target protein (Gahan et al 2001), the truncation of a gene resulting in the generation of a protein with novel function (Aminetzach et al 2005), or the increased expression of a gene associated with metabolic insecticide resistance (Daborn et al 2002;Schlenke and Begun 2004;Marsano et al 2005). Both for insecticide resistance examples and for other examples of TE-associated insertions, rarely has the effect of the mutation caused by the TE been fully characterized at the molecular level.…”

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confidence: 99%

Cis-Regulatory Elements in the Accord Retrotransposon Result in Tissue-Specific Expression of the Drosophila melanogaster Insecticide Resistance Gene Cyp6g1

et al. 2007

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Transposable elements are a major mutation source and powerful agents of adaptive change. Some transposable element insertions in genomes increase to a high frequency because of the selective advantage the mutant phenotype provides. Cyp6g1-mediated insecticide resistance in Drosophila melanogaster is due to the upregulation of the cytochrome P450 gene Cyp6g1, leading to the resistance to a variety of insecticide classes. The upregulation of Cyp6g1 is correlated with the presence of the long terminal repeat (LTR) of an Accord retrotransposon inserted 291bp upstream of the Cyp6g1 transcription start site. This resistant allele (DDT-R) is currently at a high frequency in D. melanogaster populations around the world. Here, we characterize the spatial expression of Cyp6g1 in insecticide-resistant and -susceptible strains. We show that the Accord LTR insertion is indeed the resistance-associated mutation and demonstrate that the Accord LTR carries regulatory sequences that increase the expression of Cyp6g1 in tissues important for detoxification, the midgut, Malpighian tubules, and the fat body. This study provides a significant example of how changes in tissue-specific gene expression caused by transposableelement insertions can contribute to adaptation.

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“…Mobilization of DNA, moreover, is not solely a past event, but is ongoing in natural populations, where it may underlie evolutionary adaptation. In Drosophila, for example, the insertion of transposable elements into proximal promoters of heat-shock and cytochrome P450 genes, which thereafter segregate as alleles in natural populations, underlies adaptation to temperature and insecticides, respectively (Michalak et al 2001;Daborn et al 2002;McCollum et al 2002;Lerman et al 2003;Petrov et al 2003;Schlenke and Begun 2004;Aminetzach et al 2005;Bogwitz et al 2005;Lerman and Feder 2005;Marsano et al 2005). Importantly, transposition into genes is not random, but requires insertion sites that are physically accessible to the transposition machinery, and all genes (or regions of genes) are not equal in providing access (Bellen et al 2004).…”

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confidence: 99%

Remarkable Site Specificity of Local Transposition Into the Hsp70 Promoter of Drosophila melanogaster

et al. 2006

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Heat-shock genes have numerous features that ought to predispose them to insertional mutagenesis via transposition. To elucidate the evolvability of heat-shock genes via transposition, we have exploited a local transposition technique and Drosophila melanogaster strains with EPgy2 insertions near the Hsp70 gene cluster at 87A7 to produce numerous novel EPgy2 insertions into these Hsp70 genes. More than 50% of 45 independent insertions were made into two adjacent nucleotides in the proximal promoter at positions À96 and À97, and no insertions were into a coding or 39-flanking sequence. All inserted transposons were in inverse orientation to the starting transposon. The frequent insertion into nucleotides À96 and À97 is consistent with the DNase hypersensitivity, absence of nucleosomes, flanking GAGA-factor-binding sites, and nucleotide sequence of this region. These experimental insertions recapitulated many of the phenotypes of natural transposition into Hsp70: reduced mRNA expression, less Hsp70 protein, and decreased inducible thermotolerance. The results suggest that the distinctive features of heat-shock promoters, which underlie the massive and rapid expression of heat-shock genes upon heat shock, also are a source of evolutionary variation on which natural selection can act.

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Evidence for a functional interaction between the Bari1 transposable element and the cytochrome P450 cyp12a4 gene in Drosophila melanogaster

Cited by 29 publications

References 30 publications

Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes

Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes

Cis-Regulatory Elements in the Accord Retrotransposon Result in Tissue-Specific Expression of the Drosophila melanogaster Insecticide Resistance Gene Cyp6g1

Remarkable Site Specificity of Local Transposition Into the Hsp70 Promoter of Drosophila melanogaster

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