Exposure of Helicoverpa armigera Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl

Abstract

Plants release an array of volatile chemicals into the air to communicate with other organisms in the environment. Insect attack triggers emission of herbivore-induced plant volatiles (HIPVs). How insect herbivores use these odors to plan their detoxification systems is vital for insect adaptation to environmental xenobiotics. Here we show that the larvae of Helicoverpa armigera (Hübner), a broadly polyphagous lepidopteran herbivore, have the capacity to use plant volatiles as cues to upregulate multiple detoxification systems, including cytochrome P450 monooxygenases (P450s), for detoxification of insecticides. Olfactory exposure of the fifth instars to two terpene volatiles limonene and nerolidol, and two green-leaf volatiles 2-heptanone and cis-3-hexenyl acetate significantly reduced larval susceptibility to the insecticide methomyl. However, larval pretreatment with piperonyl butoxide (PBO), a known P450 inhibitor, neutralized the effects of volatile exposure. Furthermore, larval exposure to the four plant volatiles enhanced activities of P450 enzymes in midguts and fatbodies, and upregulated expression of CYP6B2, CYP6B6 and CYP6B7, P450s involved in detoxification of the insecticide. Larval exposure to 2-heptanone and limonene volatiles also enhanced activities of glutathione-s-transferase and carboxylesterase. Our findings suggest that olfactory exposure to HIPVs enhances larval insecticide tolerance via induction of detoxification P450s.

Molecular characterization and functional analysis of cytochrome P450-mediated detoxification CYP302A1 gene involved in host plant adaptation in Spodoptera frugieprda

“…To further confirm the possible role of metabolic detoxification enzyme in S. frugiperda larvae to host plant adaptation, higher mortality was observed in pretreated larvae with PBO followed by the exposure of rice plants as compared to the corn plants. Our results are consistent with ( Wu et al., 2021 ) who reported higher mortality of H. armigera larvae pretreated with PBO after exposure to plant volatile than control. Though, selective or inducible enzyme systems could provide generalist herbivores with an ecological opportunity to adapt to diverse host plants.…”

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

“…P450 enzymes play an important part in the phase I process of detoxification of many different types of hazardous chemicals, including insecticides, due to their genetic diversity, broad substrate specialization, and catalytic adaptability ( Kim et al, 2022 ). For herbivorous insects, the main mechanism of pesticide resistance is the overexpression of cytochrome P450 detoxifying enzymes ( Hafeez et al, 2020b ; Wu et al, 2021 ).…”

Transcriptome analysis ofMythimna separata: De novo assembly and detection of genes related to beta‐cypermethrin resistance

“…The cytochrome P450 monooxygenase (cytochrome P450 or CYP) gene superfamily consists of many genes that play a vital role in the detoxification of exogenous bioactive compounds and hydrophobic xenobiotics (e.g., synthetic insecticides, plant allelochemicals, drugs) and in the biotransformation of endogenous bioactive compounds (e.g., hormones, saturated/unsaturated fatty acids, steroids, amino acids) (Capdevila et al, 2000; Griffiths et al, 2016; Huang et al, 2020; X. Li et al, 2007; Wu et al, 2021). Phylogenetic analysis of available insect P450s protein sequences indicated that they fall into four major clades‐CYP2, CYP3, CYP4, and mitochondrial CYP clans (Feyereisen, 2006).…”