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UDP-Glycosyltransferases from the UGT344 Family Are Involved in Sulfoxaflor Resistance in Aphis gossypii Glover.

ABSTRACT: UDP-glycosyltransferases (UGTs) are major phase II detoxification enzymes that catalyze the transfer of glycosyl residues from activated nucleotide sugars to acceptor hydrophobic molecules and play very important roles in the biotransformation of various endogenous and exogenous compounds. Our previous studies demonstrated that UGTs participated in the detoxification of insecticides in Aphis gossypii. However, the potential roles of UGTs in A. gossypii resistance to sulfoxaflor are still unclear. In this study, two inhibitors of UGT enzymes, sulfinpyrazone and 5-nitrouracil, significantly increased the toxicity of sulfoxaflor to a resistant strain of A. gossypii, whereas there were no synergistic effects in the susceptible strain. Based on the transcriptome sequencing results, the expression levels of 15 UGTs were analyzed by quantitative real-time PCR, and we found that seven UGT genes were highly over-expressed in a sulfoxaflor-resistant strain compared to the susceptible strain, including UGT344B4, UGT344C5, UGT344A11, UGT344A14, and UGT344L2. Further suppressing the expression of UGT344B4, UGT344C5, and UGT344A11 by RNA interference significantly increased the sensitivity of resistant aphids to sulfoxaflor, indicating that the overexpression of UGT genes is potentially associated with sulfoxaflor resistance. These results could provide valuable information for further understanding the mechanisms of insecticide resistance.

SUBMITTER: Ma K

PROVIDER: S-EPMC8072560 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundNeonicotinoid insecticides are applied worldwide for the control of agricultural insect pests. The evolution of neonicotinoid resistance has led to the failure of pest control in the field. The enhanced detoxifying enzyme activity and target mutations play important roles in the resistance of insects to neonicotinoid resistance. Emerging evidence indicates a central role of the gut symbiont in insect pest resistance to pesticides. Existing reports suggest that symbiotic microorganisms could mediate pesticide resistance by degrading pesticides in insect pests.ResultsThe 16S rDNA sequencing results showed that the richness and diversity of the gut community between the imidacloprid-resistant (IMI-R) and imidacloprid-susceptible (IMI-S) strains of the cotton aphid Aphis gossypii showed no significant difference, while the abundance of the gut symbiont Sphingomonas was significantly higher in the IMI-R strain. Antibiotic treatment deprived Sphingomonas of the gut, followed by an increase in susceptibility to imidacloprid in the IMI-R strain. The susceptibility of the IMI-S strain to imidacloprid was significantly decreased as expected after supplementation with Sphingomonas. In addition, the imidacloprid susceptibility in nine field populations, which were all infected with Sphingomonas, increased to different degrees after treatment with antibiotics. Then, we demonstrated that Sphingomonas isolated from the gut of the IMI-R strain could subsist only with imidacloprid as a carbon source. The metabolic efficiency of imidacloprid by Sphingomonas reached 56% by HPLC detection. This further proved that Sphingomonas could mediate A. gossypii resistance to imidacloprid by hydroxylation and nitroreduction.ConclusionsOur findings suggest that the gut symbiont Sphingomonas, with detoxification properties, could offer an opportunity for insect pests to metabolize imidacloprid. These findings enriched our knowledge of mechanisms of insecticide resistance and provided new symbiont-based strategies for control of insecticide-resistant insect pests with high Sphingomonas abundance.

Project description:The cotton aphid, Aphis gossypii, is an important insect pest of many crops around the world, and it has developed resistance to a large number of frequently used insecticides. The sublethal effects of insecticides not only have an environmental risk to arthropods but also have the potential to promote resistance evolution. The sublethal effects (inhibitory or stimulatory) are influenced by many factors, such as the type of insecticide, sublethal concentrations, pest species, and others. In this study, the sublethal effects of sulfoxaflor and acetamiprid on A. gossypii were compared using two field-collected populations. The results show that sulfoxaflor was more toxic than acetamiprid against A. gossypii in both populations, the LC50 concentrations of acetamiprid and sulfoxaflor were 6.35 and 3.26 times higher, respectively, for the Jinghe population than for Yarkant. The LC25 concentration of acetamiprid significantly reduced adult longevity and fecundity in exposed adults (F0) of the Jinghe population, but it had no significant effects on these factors in Yarkant. Similar inhibitory effects were found in the F1 and F2 generations, but the biological traits in the Yarkant population were significantly reduced when the parents (F0) were exposed to LC25 of acetamiprid, whereas the changes in the Jinghe population were not significant. However, sublethal sulfoxaflor showed a stimulatory effect on A. gossypii in the F0 and F1 generation; the adult fecundity and longevity of the F0 generation were significantly higher in Jinghe, while the biological traits of the F1 generation were obviously higher in Yarkant. In the F2 generation, the r and λ were significantly higher in Jinghe; meanwhile, these biological traits were reduced in Yarkant. These results indicate that sulfoxaflor and acetamiprid had different sublethal effects on A. gossypii that varied by generation. In addition, we speculate that the genetic background and the resistance levels of A. gossypii may also influence the sublethal effects. Our findings are useful for assessing the overall effects of sulfoxaflor and acetamiprid on A. gossypii.

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UDP-Glycosyltransferases from the UGT344 Family Are Involved in Sulfoxaflor Resistance in Aphis gossypii Glover.

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