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. 2024 Dec 6:15:1478869.
doi: 10.3389/fphys.2024.1478869. eCollection 2024.

Two detoxification enzyme genes, CYP6DA2 and CarFE4, mediate the susceptibility to afidopyropen in Semiaphis heraclei

Xiaochen Fu  1   2 , Chao Xue  2 , Xin Wang  3 , Aiyu Wang  2 , Yanwei Zhu  2 , Yuanxue Yang  2 , Yun Zhang  2 , Yun Zhou  2 , Ming Zhao  2 , Chenggang Shan  1   2 , Jianhua Zhang  2
Affiliations

Two detoxification enzyme genes, CYP6DA2 and CarFE4, mediate the susceptibility to afidopyropen in Semiaphis heraclei

Xiaochen Fu et al. Front Physiol. .

Abstract

Introduction: Semiaphis heraclei is an important economic pest affecting Caprifoliaceae and Apiaceae plants, and chemical control is still the main effective control method in the field. Afidopyropen is a new type of pyridine cyclopropyl insecticide, which can effectively control piercing-sucking mouthparts pests and is suitable for pest resistance management. However, the detoxification mechanism of S. heraclei to afidopyropen is still poorly cleared.

Methods: The insecticidal activity of afidopyropen against S. heraclei and the enzyme activity assay and synergism bioassay were evaluated. The detoxification enzyme genes were obtained by transcriptome and validated by quantitative real-time PCR (RT-qPCR). Furthermore, RNA interference was used to study the functions of detoxification enzyme genes.

Results: The activities of cytochrome P450 monooxygenases (P450s) and carboxylesterases (CarEs) were significantly increased under afidopyropen treatment. The toxicity of afidopyropen against S. heraclei was significantly increased after application the inhibitors of piperonyl butoxide and triphenyl phosphate. Sixteen P450 genes and three CarE genes were identified in the transcriptome of S. heraclei. The RT-qPCR results showed that eleven P450 genes and two CarE genes were significantly upregulated under afidopyropen treatment, and the expression of CYP6DA2 and CarFE4 was upregulated by more than 2.5 times. The expression pattern of CYP6DA2 and CarFE4 was further analyzed in different developmental stages of S. heraclei and knockdown of CYP6DA2 and CarFE4 significantly increased the susceptibility of S. heraclei to afidopyropen.

Conclusion: The results of this study uncover the key functions of CYP6DA2 and CarFE4 in the detoxification mechanism of S. heraclei to afidopyropen, and provide a theoretical basis for the scientific use of afidopyropen in the field.

Keywords: CYP6DA2; CarFE4; Semiaphis heraclei; afidopyropen; detoxification mechanism.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Detoxification enzyme activity in S. heraclei after afidopyropen treatment. (A) MFO activity after treatment of afidopyropen. (B) CarE activity after treatment of afidopyropen. (C) GST activity after treatment of afidopyropen. The asterisk (*) and asterisks (**) indicate significant differences with p < 0.05 and p < 0.01 compared to control group.
FIGURE 2
FIGURE 2
Effects of synergists on mortality of S. heraclei under afidopyropen treatment. (A) The synergism of PBO on S. heraclei mortality after treatment of afidopyropen. (B) The synergism of TPP on S. heraclei mortality after treatment of afidopyropen. (C) The synergism of DEM on S. heraclei mortality after treatment of afidopyropen. The asterisk (*) and asterisks (**) indicate significant differences with p < 0.05 and p < 0.01 compared to afidopyropen group. The ns represents no significant difference.
FIGURE 3
FIGURE 3
Differential gene expression analysis of S. heraclei in response to afidopyropen treatment. (A) Species distributions of top blastx matches to Nr database. (B) Number of up- and downregulated DEGs and volcano plot of DEGs in afidopyropen exposure. (C) Heatmap of DEGs between afidopyropen and control.
FIGURE 4
FIGURE 4
Screening of differentially expressed P450 and CarE genes by RT-qPCR analysis. The asterisk (*) and asterisks (**) indicate significant differences with p < 0.05 and p < 0.01 compared to control group. The ns represents no significant difference.
FIGURE 5
FIGURE 5
Functional analysis of CYP6DA2 and CarFE4 by RNAi and their expression patterns in S. heraclei. (A) The expression patterns of CYP6DA2 at different developmental stages. (B) The expression patterns of CarFE4 at different developmental stages. (C) Relative abundance of CYP6DA2 in S. heraclei at 2 days after feeding dsRNA. (D) Relative abundance of CarFE4 in S. heraclei at 2 days after feeding dsRNA. (E) Mortality rate of S. heraclei fed dsCYP6DA2 treated with LD50 concentrations of afidopyropen for 48 h. (F) Mortality rate of S. heraclei fed dsCarFE4 treated with LD50 concentrations of afidopyropen for 48 h. The asterisk (*) and asterisks (**) indicate significant differences with p < 0.05 and p < 0.01 compared to control group. The letters a, b, c, and d present significant differences (p < 0.05) of the expression.
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References

    1. Aioub A. A. A., Ashour M.-B. A. (2023). Editorial for the special issue “detoxification mechanisms in insects.”. Toxics 11, 691. 10.3390/toxics11080691 - DOI - PMC - PubMed
    1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410. 10.1016/S0022-2836(05)80360-2 - DOI - PubMed
    1. Buchfink B., Xie C., Huson D. H. (2015). Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60. 10.1038/nmeth.3176 - DOI - PubMed
    1. Chen J., Zhang D., Yao Q., Zhang J., Dong X., Tian H., et al. (2010). Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens . Insect Mol. Biol. 19, 777–786. 10.1111/j.1365-2583.2010.01038.x - DOI - PubMed
    1. Cui L., Yuan H., Wang Q., Wang Q., Rui C. (2018). Sublethal effects of the novel cis-nitromethylene neonicotinoid cycloxaprid on the cotton aphid Aphis gossypii Glover (Hemiptera: aphididae). Sci. Rep. 8, 8915. 10.1038/s41598-018-27035-7 - DOI - PMC - PubMed