Transcriptome analysis reveals differential effects of beta-cypermethrin and fipronil insecticides on detoxification mechanisms in Solenopsis invicta

Abstract

Insecticide resistance poses many challenges in insect pest control, particularly in the control of destructive pests such as red imported fire ants (Solenopsis invicta). In recent years, beta-cypermethrin and fipronil have been extensively used to manage invasive ants, but their effects on resistance development in S. invicta are still unknown. To investigate resistance development, S. invicta was collected from populations in five different cities in Guangdong, China. The results showed 105.71- and 2.98-fold higher resistance against fipronil and beta-cypermethrin, respectively, in the Guangzhou population. The enzymatic activities of acetylcholinesterase, carboxylases, and glutathione S-transferases significantly increased with increasing beta-cypermethrin and fipronil concentrations. Transcriptomic analysis revealed 117 differentially expressed genes (DEGs) in the BC-ck vs. BC-30 treatments (39 upregulated and 78 downregulated), 109 DEGs in F-ck vs. F-30 (33 upregulated and 76 downregulated), and 499 DEGs in BC-30 vs. F-30 (312 upregulated and 187 downregulated). Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that DEGs associated with insecticide resistance were significantly enriched in metabolic pathways, the AMPK signaling pathway, the insulin signaling pathway, carbon metabolism, peroxisomes, fatty acid metabolism, drug metabolism enzymes and the metabolism of xenobiotics by cytochrome P450. Furthermore, we found that DEGs important for insecticide detoxification pathways were differentially regulated under both insecticide treatments in S. invicta. Comprehensive transcriptomic data confirmed that detoxification enzymes play a significant role in insecticide detoxification and resistance development in S. invicta in Guangdong Province. Numerous identified insecticide-related genes, GO terms, and KEGG pathways indicated the resistance of S. invicta workers to both insecticides. Importantly, this transcriptome profile variability serves as a starting point for future research on insecticide risk evaluation and the molecular mechanism of insecticide detoxification in invasive red imported fire ants.

Insights into insecticide-resistance mechanisms in invasive species: Challenges and control strategies

“…Moreover, the detoxification mechanism by P450 was reported in various studies. For instance, in S. invicta belonging to the order Hymenoptera, CYP was involved in the detoxification of fluralaner (Xiong et al, 2022) (Xiong et al, 2022), fipronil and beta cypermethrin (Siddiqui et al, 2022b). Similarly, in the order Diptera, D. melanogaster, C. quinquefasciatus and Anopheles funestus (Giles) (Daborn et al, 2002;Wondji et al, 2009;Itokawa et al, 2010), in the order Hemiptera, M. persicae were all reported for the amplification of P450 and insecticide resistance (Puinean et al, 2010).…”

“…Furthermore, to become more effective, these enzyme systems may also be able to break down many different types of pesticides ( Vyas et al, 2022 ). Detoxifying enzymes enhance and accelerate the drug resistance caused by the metabolism of insecticides ( Siddiqui et al, 2022c ; Siddiqui et al, 2022b ). The over-produced enzymes in pests can develop protection against insecticides ( Figure 2 ) ( Rane et al, 2016 ; Khan et al, 2020 ).…”

“…CarEs enzymes also detoxify environmental toxicants such as pyrethroids, a major insecticide class used worldwide ( Staudinger et al, 2010 ). Recent studies on invasive species indicated that a greater AChE and CarE esterase activity was seen in resistant populations compared to vulnerable ones such as S. invicta ( Siddiqui et al, 2022b ; 2022c ), H. armigera ( Young et al, 2005 ; Wu et al, 2011 ), C. tarsalis ( Whyard et al, 1994 ), and Aonidiella aurantia ( Grafton-Cardwell et al, 2004 ) ( Figure 2 ).…”

“…Insecticide metabolism studies indicated that esterases are involved in resistance mechanisms. Increased accumulation of esterase hydrolytic products in insecticide-resistant insects compared to susceptible gives evidence for the involvement of these enzymes ( Jensen, 2000 ; Silva et al, 2012 ; Khan et al, 2021b ; Siddiqui et al, 2022b ).…”

“…Studies on invasive fire ants show that exposure to indoxacarb, beta-cypermethrin, and fipronil causes a substantial alteration in GST activity. Additionally, the outcomes demonstrate that population resistance and sublethal concentrations substantially impact enzyme activity ( Siddiqui et al, 2022c ; Siddiqui et al, 2022b ). OP and DDT resistance mechanisms were reported in houseflies ( Ranganathan et al, 2022 ).…”