Adaptation
to phytochemicals in herbivorous insects can influence
tolerance to insecticides. However, it is unclear how insects use
phytochemicals as cues to activate their metabolic detoxification
systems. In this study, we found that dietary exposure to xanthotoxin
enhanced tolerance of Spodoptera litura larvae to
λ-cyhalothrin. Xanthotoxin ingestion significantly elevated
the mRNA levels of 35 detoxification genes as well as the transcription
factors Cap ‘n’ collar isoform-C (CncC) and its binding factor small muscle aponeurosis fibromatosis isoform-K
(MafK). Additionally, xanthotoxin exposure increased
the levels of reactive oxygen species (ROS), while ROS inhibitor N-acetylcysteine
(NAC) treatment blocked xanthotoxin-induced expression of CncC, MafK, and detoxification genes and
also prevented xanthotoxin-enhanced larval tolerance to λ-cyhalothrin.
The 20-hydroxyecdysone (20E) signaling pathway was effectively activated
by xanthotoxin, while blocking of 20E signaling transduction prevented
xanthotoxin-enhanced larval tolerance to λ-cyhalothrin. Application
of 20E induced the expression of multiple xanthotoxin-induced detoxification
genes and enhanced λ-cyhalothrin tolerance in S. litura. NAC treatment blocked xanthotoxin-induced 20E synthesis, while
the CncC agonist curcumin activated the 20E signaling pathway. These
results indicate that the ROS/CncC pathway controls the induction
of metabolic detoxification upon exposure to xanthotoxin, at least
in part, through its regulation of the 20E signaling pathway.