Lufenuron affects the fecundity of <i>Panonychus citri</i> by regulating the methyl farnesoate–ponasterone A network

In insects, the juvenile hormone (JH) and 20-hydroxyecdysone (20E) pathways jointly regulate fecundity, but only methyl farnesoate (MF) and ponasterone A exist in mites. Comparative transcriptomic analysis in Panonychus citri showed that E75B was significantly downregulated when exposed to lufenuron. Knockdown of E75B significantly affects the expression of vitellogenin (Vg), Fushi tarazu factor 1 (Ftz-f1) and juvenile hormone acid O-methyltransferase (JHAMT), reducing fecundity in mites. The knockdown of Ftz-f1 produced a more significant effect than the knockdown of E75B, indicating that the ponasterone A pathway positively regulates fecundity in P. citri. After the knockdown of JHAMT, the expression levels of both Vg and Ftz-f1 and fecundity were significantly increased, along with the inhibition of Kr-h1, suggesting that JHAMT was negatively correlated with fecundity in the regulatory network. Knockdown of Kr-h1 inhibited the expression of Vg and Ftz-f1 and fecundity, and whether the drop in fecundity is caused by Kr-h1 or Ftz-f1 is unclear. Subsequent feeding with MF induced Kr-h1 and Vg expression, whereas no significant effects were observed for JHAMT and Ftz-f1. Therefore, the MF pathway stimulates fecundity independently. RNA interference (RNAi) showed that JHAMT and Ftz-f1 inhibited each other, resulting in opposite effects of MF and ponasterone A pathways on steady-state fecundity when either factor changed. Meanwhile, JHAMT knockdown led to increased fecundity, indicating that the stimulating effect of the ponasterone A pathway was greater than the inhibiting effect of the MF pathway, and demonstrating the dominant role of the ponasterone A pathway. Therefore, the interaction between JHAMT and Ftz-f1 may be closely associated with the maintenance of MF-ponasterone A regulatory network homeostasis and is involved in the reduction of fecundity in P. citri induced by exposure to lufenuron.