Transcription factor FTZ‐F1 and cis‐acting elements mediate expression of CYP6BG1 conferring resistance to chlorantraniliprole in Plutella xylostella

Li, Xiuxia; Shan, Chunyang; Li, Fen; Liang, Pei; Smagghe, Guy; Gao, Xiwu

doi:10.1002/ps.5279

Cited by 34 publications

(27 citation statements)

References 43 publications

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“…In arthropods, constitutive overexpression of nuclear receptors/ transcription factors belonging to these superfamilies contribute to increasing the expression of P450s responsible for metabolic resistance. Increase in the expression of the nuclear receptor, FTZ-F1 in Plutella xylostella causes overexpression of CYP6BG1 that metabolizes chlorantraniliprole [21]. Similarly, the Aryl hydrocarbon receptor (AhR) belonging to the bHLH-PAS protein family [20] regulates CYP6DA2 in Aphis gossypii conferring gossypol and spirotetramat tolerance [22].…”

Section: Introductionmentioning

confidence: 99%

Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua

Huang

et al. 2021

PLoS Genet

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The evolution of insect resistance to insecticides is frequently associated with overexpression of one or more cytochrome P450 enzyme genes. Although overexpression of CYP450 genes is a well-known mechanism of insecticide resistance, the underlying regulatory mechanisms are poorly understood. Here we uncovered the mechanisms of overexpression of the P450 gene, CYP321A8 in a major pest insect, Spodoptera exigua that is resistant to multiple insecticides. CYP321A8 confers resistance to organophosphate (chlorpyrifos) and pyrethroid (cypermethrin and deltamethrin) insecticides in this insect. Constitutive upregulation of transcription factors CncC/Maf are partially responsible for upregulated expression of CYP321A8 in the resistant strain. Reporter gene assays and site-directed mutagenesis analyses demonstrated that CncC/Maf enhanced the expression of CYP321A8 by binding to specific sites in the promoter. Additional cis-regulatory elements resulting from a mutation in the CYP321A8 promoter in the resistant strain facilitates the binding of the orphan nuclear receptor, Knirps, and enhances the promoter activity. These results demonstrate that two independent mechanisms; overexpression of transcription factors and mutations in the promoter region resulting in a new cis-regulatory element that facilitates binding of the orphan nuclear receptor are involved in overexpression of CYP321A8 in insecticide-resistant S. exigua.

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Section: Introductionmentioning

confidence: 99%

Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua

Huang

et al. 2021

PLoS Genet

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“…In A. mellifera, cuticle pigmentation and wing formation during developmental processes were severely impaired by downregulation of FTZ-F1 [25]. Recently, Li et al [27] reported that FTZ-F1 mediates the expression of CYP6BG1, conferring resistance to chlorantraniliprole in P. xylostella. However, there are no reports on the relationship between FTZ-F1 and cuticular resistance in mosquitoes.…”

Section: Discussionmentioning

confidence: 99%

“…FTZ-F1 could also regulate the expression of EDG84A by binding to two cis elements of this gene in D. melanogaster [26]. A recent study found that FTZ-F1 can regulate the expression of CYB6PG1 by binding to its promoter region (-562 to -340) in P. xylostella [27]. The results of the present study revealed that FTZ-F1 specifically binds to CPLCG5 through the CRE at -870/-864 to directly regulate the expression of cuticular protein CPLCG5.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, Li et al . [ 27 ] reported that FTZ-F1 mediates the expression of CYP6BG1 , conferring resistance to chlorantraniliprole in P. xylostella. However, there are no reports on the relationship between FTZ-F1 and cuticular resistance in mosquitoes.…”

Section: Discussionmentioning

confidence: 99%

“…A cuticle gene, EDG84A, is regulated by FTZ-F1 during the metamorphosis of D. melanogaster [26]. As for studies of FTZ-F1 regulating insecticide resistance, only a study by Li et al [27] observed that FTZ-F1 mediates the expression of CYP6BG1, conferring resistance to chlorantraniliprole in Plutella xylostella. However, the relationship between FTZ-F1 and cuticular resistance has not been reported.…”

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confidence: 99%

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Transcription factor FTZ-F1 regulates mosquito cuticular protein CPLCG5 conferring resistance to pyrethroids in Culex pipiens pallens

Yang

Sun

et al. 2020

Parasites Vectors

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Background Culex pipiens pallens poses a serious threat to human health because of its widespread distribution, high carrier capacity for several arboviruses, frequent human-biting, and growth in urban environments. Pyrethroid insecticides have been mainly used to control adult Cx. pipiens pallens during outbreaks of mosquito-borne diseases. Unfortunately, mosquitoes have developed resistance, rendering the insecticides ineffective. Cuticular resistance is the primary mechanism of pyrethroid resistance. Previously, we revealed that cuticular protein of low complexity CPLCG5 is a major cuticular protein associated with deltamethrin resistance in Cx. pipiens pallens, which is enriched in the cuticle of mosquitoes’ legs and participates in pyrethroid resistance by forming a rigid matrix. However, the regulatory mechanisms of its transcription remain unknown. Results First, qRT-PCR analysis revealed that the expression of FTZ-F1 (encoding Fushi tarazu-Factor 1) was ~ 1.8-fold higher in the deltamethrin-resistant (DR) than deltamethrin-susceptible (DS) strains at 24 h post-eclosion (PE) and ~ 2.2-fold higher in the DR strain than in the DS strain at 48 h PE. CPLCG5 and FTZ-F1 were co-expressed in the legs, indicating that they might play an essential role in the legs. Dual luciferase reporter assays and EMSA (electrophoretic mobility shift experiments) revealed that FTZ-F1 regulates the transcription of CPLCG5 by binding to the FTZ-F1 response element (− 870/− 864). Lastly, knockdown of FTZ-F1 not only affected CPLCG5 expression but also altered the cuticle thickness and structure of the legs, increasing the susceptibility of the mosquitoes to deltamethrin in vivo. Conclusions The results revealed that FTZ-F1 regulates the expression of CPLCG5 by binding to the CPLCG5 promoter region, altering cuticle thickness and structure, and increasing the susceptibility of mosquitoes to deltamethrin in vivo. This study revealed part of the mechanism of cuticular resistance, providing a deeper understanding of insecticide resistance.

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Functional Roles of Five Cytochrome P450 Transcripts in the Susceptibility of the Yellow Fever Mosquito to Pyrethroids Revealed by RNAi Coupled With Insecticide Bioassay

Soumalia Issa,

Johnson,

Park

et al. 2024

Arch Insect Biochem Physiol

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We evaluated the possible roles of five cytochrome P450 transcripts in the susceptibility of both adults and larvae of Aedes aegypti to three pyrethroids using RNA interference (RNAi) coupled with insecticide bioassays. RNAi by feeding larvae with chitosan/dsRNA nanoparticles led to reductions of CYP6AA5, CYP6AL1, CYP9J32, CYP4J16A, and CYP4J16B transcripts by 38.7%, 46.0%, 46.52%, 44.0%, and 41.0%, respectively, and increased larval mortality by 46.0% to permethrin when CYP9J32 was silenced and by 41.2% to cypermethrin when CYP6AA5 was silenced. RNAi by injecting dsRNA in adults led to reductions of CYP6AA5, CYP6AL1, and CY4J16A transcripts by 77.9%, 80.0%, and 87.1% (p < 0.05), respectively, at 96 h and reduction of CYP9J32 transcript by 46.5% at 24 h after injection. In contrast, CYP4J16B was repressed by 78.2% at 72 h after injection. Exposure of the adults injected with CYP6AA5 dsRNA resulted in 1.5‐ to 2.0‐fold increased susceptibility to cypermethrin as compared with the control. Homology modeling of CYP6AA5 followed by ligand docking showed that distances between the heme iron and the putative aromatic hydroxylation site were 9.2, 7.2, and 9.1 Å for permethrin, cypermethrin, and deltamethrin, respectively. For the aliphatic hydroxylation site, these distances were 5.3, 4.9, and 3.1 Å. These results supported that CYP6AA5 may be able to metabolize cypermethrin preferentially by aliphatic hydroxylation as indicated by the close interaction with the heme iron. Our study also suggests that the detoxification roles of cytochrome P450 genes in A. aegypti may vary according to the mosquito developmental stages, cytochrome P450 genes, and insecticides.

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Transcription factor FTZ‐F1 and cis‐acting elements mediate expression of CYP6BG1 conferring resistance to chlorantraniliprole in Plutella xylostella

Cited by 34 publications

References 43 publications

Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua

Changes in both trans- and cis-regulatory elements mediate insecticide resistance in a lepidopteron pest, Spodoptera exigua

Transcription factor FTZ-F1 regulates mosquito cuticular protein CPLCG5 conferring resistance to pyrethroids in Culex pipiens pallens

Functional Roles of Five Cytochrome P450 Transcripts in the Susceptibility of the Yellow Fever Mosquito to Pyrethroids Revealed by RNAi Coupled With Insecticide Bioassay

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