title: Gossypol-enhanced P450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide.
abstract: Cotton plants accumulate phytotoxins, including gossypol and related sesquiterpene aldehydes, to resist insect herbivores and pathogens. To counteract these defensive plant secondary metabolites, cotton bollworms (Helicoverpa armigera) elevate their production of detoxification enzymes, including cytochrome P450 monooxygenases (P450s). Besides their tolerance to phytotoxin, cotton bollworms have quickly developed resistance to deltamethrin, a widely used pyrethroid insecticide in cotton field. However, the relationship between host plant secondary metabolites and bollworm insecticide resistance is poorly understood. Here, we show that exogenously expressed CYP6AE14, a gossypol-inducible P450 of cotton bollworm, has epoxidation activity towards aldrin, an organochlorine insecticide, indicating that gossypol-induced P450s participate in insecticide metabolism. Gossypol-ingested cotton bollworm larvae showed higher midgut P450 enzyme activities and exhibited enhanced tolerance to deltamethrin. The midgut transcripts of bollworm larvae administrated with different phytochemicals and deltamethrin were then compared by microarray analysis, which showed that gossypol and deltamethrin induced the most similar P450 expression profiles. Gossypol-induced P450s exhibited high divergence and at least five of them (CYP321A1, CYP9A12, CYP9A14, CYP6AE11 and CYP6B7) contributed to cotton bollworm tolerance to deltamethrin. Knocking down one of them, CYP9A14, by plant-mediated RNA interference (RNAi) rendered the larvae more sensitive to the insecticide. These data demonstrate that generalist insects can take advantage of secondary metabolites from their major host plants to elaborate defence systems against other toxic chemicals, and impairing this defence pathway by RNAi holds a potential for reducing the required dosages of agrochemicals in pest control.
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Xiao-Yuan
authors.initials: XY
authors.lastname: Tao
authors.forename: Xue-Yi
authors.initials: XY
authors.lastname: Xue
authors.forename: Yong-Ping
authors.initials: YP
authors.lastname: Huang
authors.forename: Xiao-Ya
authors.initials: XY
authors.lastname: Chen
authors.forename: Ying-Bo
authors.initials: YB
authors.lastname: Mao
mesh_terms: D000452:Aldrin; D000818:Animals; D003577:Cytochrome P-450 Enzyme System / Q000235:genetics*; D005786:Gene Expression Regulation / Q000187:drug effects*; D003368:Gossypium; D006072:Gossypol / Q000494:pharmacology*; D007305:Insecticide Resistance / Q000235:genetics*; D007814:Larva / Q000187:drug effects / Q000201:enzymology / Q000235:genetics; D009036:Moths / Q000187:drug effects / Q000201:enzymology / Q000235:genetics*; D009570:Nitriles; D020411:Oligonucleotide Array Sequence Analysis; D011722:Pyrethrins; D034622:RNA Interference; D060888:Real-Time Polymerase Chain Reaction; D059467:Transcriptome
chemical_list: D009570:Nitriles; D011722:Pyrethrins; C017180:decamethrin; D003577:Cytochrome P-450 Enzyme System; D006072:Gossypol; D000452:Aldrin