Adipokinetic hormone signaling regulates cytochrome P450‐mediated chlorantraniliprole sensitivity in Spodoptera frugiperda (Lepidoptera: Noctuidae)

Abstract

BACKGROUND: Fall armyworm (FAW, Spodoptera frugiperda) is one of the most destructive and invasive pests worldwide and causes significant economic losses. Intensive and frequent use of insecticides has led to the development of resistance in FAW. Adipokinetic hormone (AKH) have been proven to be involved in insecticide resistance in insects. However, the molecular mechanism underlying chlorantraniliprole resistance mediated by AKH signaling in FAW remains unclear.RESULTS: The expression of SpfAKHR was highest in male adults and lowest in 1st instar larvae. SpfAKH was expressed the highest in eggs and the lowest in 6th instar larvae. AKH signaling was involved in the sensitivity of FAW to chlorantraniliprole through a toxicological bioassay, and the combination of chlorantraniliprole and bithionol (an inhibitor of key enzymes in the AKH pathway) significantly increased the mortality of FAW. Chlorantraniliprole significantly induced the expression of ten P450s, SpfAKH and SpfAKHR in FAW. RNA interference against SpfAKHR significantly decreased the P450 content, downregulated the expression of three P450 genes (SpfCYP6B50, SpfCYP321A9 and SpfCYP9A58) and inhibited the resistance of FAW to chlorantraniliprole. The topical application of AKH peptide significantly increased the P450 content, upregulated the expression of five P450 genes (SpfCYP321A9, SpfCY321A8, SpfCYP321A10, SpfCYP321A7 and SpfCYP6AB12), and enhanced the survival of FAW against chlorantraniliprole.CONCLUSIONS: AKH plays an important role in enhancing chlorantraniliprole resistance in FAW by exerting a positive influence on P450 gene expression and P450 content. These results provide valuable insights into insecticide resistance regulation and FAW control strategies.

Genome-Wide Scanning Loci and Differentially Expressed Gene Analysis Unveils the Molecular Mechanism of Chlorantraniliprole Resistance in Spodoptera frugiperda

“…Synergism experiments with inhibitors (PBO/DEM/TPP) further determined the enhanced effects of P450, GST, and CarE on chlorantraniliprole toxicity (Table ). These results suggest that the Ch-R strain we obtained may be mainly caused by enhanced detoxification metabolism to insecticides, which is consistent with the results of previous studies. , At the transcriptional level, many P450 family genes, such as CYP321A8 , CYP321A9 , CYP321B1 , and CYP6AB12 , were upregulated after chlorantraniliprole stress. , In our study, after association analysis of candidate loci and DEGs, the identified genes related to detoxification metabolism were mainly three GST genes (Table ). As a family of multifunctional enzymes, GSTs confer insecticide adaptation through direct metabolism or sequestration of insecticides .…”

“…frugiperda has developed resistance to some Bt maize varieties, which increases the dependence on chemical insecticides in almost all areas affected. , Chlorantraniliprole is an anthranilic diamide insecticide that acts on the ryanodine receptor (RyR) and is becoming the main agent for control S. frugiperda in many commercial crops globally currently because of its broad spectrum, high efficacy, and low cross-resistance to conventional insecticides. − Field control experiments showed that chlorantraniliprole had a rapid and persistent effect against S. frugiperda, and it was recommended as a first-choice agent to control S. frugiperda by the Chinese Ministry of Agriculture and Rural Affairs in 2020. , However, the unscientific use of chlorantraniliprole has raised concerns about the development of resistance to this compound in S.…”

“…frugiperda in many commercial crops globally currently because of its broad spectrum, high efficacy, and low cross-resistance to conventional insecticides. − Field control experiments showed that chlorantraniliprole had a rapid and persistent effect against S. frugiperda, and it was recommended as a first-choice agent to control S. frugiperda by the Chinese Ministry of Agriculture and Rural Affairs in 2020. , However, the unscientific use of chlorantraniliprole has raised concerns about the development of resistance to this compound in S. frugiperda.…”

“…In the transcriptional and posttranscriptional regulation of genes encoding detoxification enzyme, Tan et al reported that adipokinetic hormone signaling reduces the susceptibility of S. frugiperda to chlorantraniliprole by increasing the transcription level of several P450 genes . Zhang et al found that microRNA-190–5p targeted and regulated the CYP6K2 gene, corresponding to S.…”

“…19 In the transcriptional and posttranscriptional regulation of genes encoding detoxification enzyme, Tan et al reported that adipokinetic hormone signaling reduces the susceptibility of S. frugiperda to chlorantraniliprole by increasing the transcription level of several P450 genes. 9 Zhang et al found that microRNA-190− 5p targeted and regulated the CYP6K2 gene, corresponding to S. frugiperda chlorantraniliprole resistance. 20 Despite this progress, understanding remains limited of the upstream regulation mechanism of expression of detoxifying enzymes in metabolic resistance and has become a key problem in the field of insect resistance research.…”