Pesticide-induced resurgence in brown planthopper is mediated by action on a suite of genes that promote juvenile hormone biosynthesis and female fecundity

Abstract

Pesticide-induced resurgence, increases in pest insect populations following pesticide application, is a serious threat to the sustainable control of many highly damaging crop pests. Resurgence can result from pesticide-enhanced pest reproduction, however, the molecular mechanisms mediating this process remain unresolved. Here we show that brown planthopper (BPH) resurgence following emamectin benzoate (EB) exposure results from the coordinated action of a diverse suite of actors that regulate juvenile hormone (JH) levels, resulting in increased JH titer in adult females and enhanced fecundity. Following reports of BPH resurgence in rice crops when this species is exposed to EB, we demonstrate that EB treatment results in profound changes in female BPH fitness including enhanced ovary development and elevated egg production. This enhanced reproductive fitness results from the EB-mediated upregulation of key genes involved in the regulation of JH, including JHAMT, Met and Kr-h1 and the downregulation of allatostatin (AstA) and allatostatin receptor (AstAR) expression. The remodulation of gene expression following EB exposure is dependent on the action of this insecticide on its molecular target the glutamate-gated chloride channel (GluCl) receptor. Collectively, these results provide mechanistic insights into the regulation of negative pesticide-induced responses in insects and reveal the key actors involved in the JH-signaling pathway that underpin pesticide resurgence.