Activating pathway of three metabolic detoxification phases via down-regulated endogenous microRNAs, modulates triflumezopyrim tolerance in the small brown planthopper, Laodelphax striatellus (Fallén).

Frequent use of insecticide causes an environmental hazard, and also leads pest to develop insecticide resistance. Enhancement of metabolic detoxification and reduction of target sensitivity are the primary mechanism of insecticide resistance. Clarifying the regulatory pathway of resistance mechanism states a pivotal theoretical foundation of delaying insecticide resistance development. Here, we show that three endogenous microRNAs, PC-3p-2522_840, PC-3p-446_6601 and PC-5p-3096_674, are required for the small brown planthopper (SBPH) to modulate triflumezopyrim tolerance via activating pathways of three metabolic detoxification phases. Twenty-one down-regulated miRNAs were acquired, and PC-5p-3096_674, PC-3p-446_6601 and PC-3p-2522_840 were the three most significantly down-regulated miRNAs during triflumezopyrim exposure. The mortality of SBPH was significantly increased after over-supplementation of PC-5p-3096_674, PC-3p-446_6601 and PC-3p-2522_840, with triflumezopyrim exposure. Moreover, the interactions between PC-3p-2522_840 and cytochrome P450 CYP6FL1, PC-3p-446_6601 and glutathione S-transferase GSTD2, UDP-Glycosyltransferase UGT386F1, PC-5p-3096_674 and ATP-binding cassette transporters ABCA3 were systematically demonstrated through the dual luciferase reporter assay. Besides, the mortality of SBPH was significantly increased after knockdown of CYP6FL1, GSTD2, UGT386F1 and ABCA3 with triflumezopyrim exposure. These findings uncover a strategy whereby the SBPH weakens three endogenous microRNAs to activate pathways of three metabolic detoxification phases via targeting CYP6FL1, GSTD2, UGT386F1 and ABCA3 and promotes its tolerance to triflumezopyrim.