Expression of CYP6B1 and CYP6B3 cytochrome P450 monooxygenases and furanocoumarin metabolism in different tissues of Papilio polyxenes (Lepidoptera: Papilionidae)

Petersen, Rebecca A.; Zangerl, Arthur R.; Berenbaum, May R.; Schuler, Mary A.

doi:10.1016/s0965-1748(00)00174-0

Cited by 92 publications

(78 citation statements)

References 37 publications

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“…These genes play important ecological and evolutionary roles in the interactions of plants and their attackers, as they are frequently involved in the detoxifications of diverse xenobiotics by mediating the reactions like N-or S-oxidation, hydroxylation, epoxidation, and O-, N-, or S-dealkylation (31,32). The particular CYP that we found to be strongly regulated in response to dietary nicotine in M. sexta larvae, MsCYP6B46, is a member of the CYP6B enzyme family, which is well known for its unique role in the perception of signaling molecules of plant-defense responses, in addition to its more conventional role in the detoxification of plant defenses (33)(34)(35)(36). Our functional analysis of the nicotine-induced MsCYP6B46 stumbled after not finding the expected polar metabolites of nicotine in larval tissues and frass or from heterologous expression assays, but was revived when the behavior of a native predator revealed an unexpected organismic-level function of MsCYP6B46.…”

Section: Discussionmentioning

confidence: 81%

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Kumar

Pandit

Steppuhn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

118

119

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Significance When hornworm ( Manduca sexta ) larvae feed on Nicotiana attenuata plants in native habitats, more disappear at night when they feed on transgenic, nicotine-free N. attenuata plants because wolf spiders ( Camptocosa parallela ) selectively prey on nicotine-free larvae. When larvae consume nicotine-replete plants, their midgut-expressed cytochrome P450 6B46 ( CYP6B46 ) is upregulated. The larvae in which CYP6B46 is silenced by plant-mediated RNAi excrete more of their ingested nicotine. Silencing CYP6B46 impairs the mechanisms of passing ingested nicotine from the midgut to the hemolymph to be exhaled from the spiracles during spider attack. Spiders are deterred by this nicotine-rich halitosis. Thus, the CYP6B46 -silenced larvae exhale less nicotine and become ready spider prey, demonstrating that CYP6B46 functions to repurpose the normally excreted nicotine for defense.

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Section: Discussionmentioning

confidence: 81%

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Kumar

Pandit

Steppuhn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

118

119

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“…9 and 10; see Fig. 4, which is published as supporting information on the PNAS web site), their inducibility by furanocoumarins (6,9,14,16), and their capacity to metabolize furanocoumarins (5, 8). Ecologically, they are expressed in herbivores that share a number of furanocoumarin-containing host plants, including parsnip (Pastinaca sativa), carrot (Daucus carota), and celery (Apium graveolens), among the preferred hosts of P. polyxenes and occasional hosts of H. zea (ref.…”

mentioning

confidence: 99%

Structural and functional divergence of insect CYP6B proteins: From specialist to generalist cytochrome P450

Baudry

Berenbaum

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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261

221

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How polyphagous herbivores cope with the diversity and unpredictability of plant defenses remains largely unknown at both the genetic and molecular levels. To examine whether generalist counterdefense enzymes are structurally more flexible and functionally more diverse, two counterdefensive allelochemical-metabolizing cytochrome P450 proteins, CYP6B1 from the specialist Papilio polyxenes, feeding on furanocoumarin-containing plants, and CYP6B8 from the generalist Helicoverpa zea, feeding on hundreds of host plant species, are compared structurally and functionally. Molecular modeling indicates that CYP6B8 has more flexible overall folding, a more elastic catalytic pocket, and one more substrate access channel than CYP6B1. Baculovirus-mediated expression of the CYP6B8 and CYP6B1 proteins demonstrates that CYP6B8 metabolizes six biosynthetically diverse plant allelochemicals (xanthotoxin, quercetin, flavone, chlorogenic acid, indole-3-carbinol, and rutin) and three insecticides (diazinon, cypermethrin, and aldrin), whereas CYP6B1 metabolizes only two allelochemicals (xanthotoxin and flavone) and one insecticide (diazinon) of those tested. These results indicate that generalist counterdefense proteins are capable of accepting a more structurally diverse array of compounds compared with specialist counterdefense proteins. T he majority of herbivorous insects are oligophagous, i.e., specialized on a relatively narrow range of host plants (three or fewer plant families) (1, 2). Such specialization is thought to reduce competition for food from other herbivores and to lower predation͞parasitoid risk from generalist enemies (3). Because of the diversification of plant chemical defenses, however, this strategy may compromise a specialist's ability to make use of alternative food sources. A small proportion of insect herbivores, including some of the world's most important agricultural pests, are polyphagous, i.e., feed on a wide range of plant families. Although polyphagous species may have fewer limitations with respect to food availability, the toxicological challenge of generalized feeding is considerable in view of the tremendous diversity of plant defense compounds (allelochemicals). Because these compounds tend to be taxonomically limited in distribution, a polyphagous diet exposes an insect herbivore to a broad and unpredictable array of plant defenses. In fact, biochemical adaptation to a relatively narrow range of plant defense compounds may explain why the majority of herbivorous insects are specialists.How generalists cope with the diversity and unpredictability of plant defenses remains largely unknown at both the genetic and molecular levels. One possibility is that counterdefense genes of generalists have multiple functions; in the case of detoxificative genes such as cytochrome P450 monooxygenases (4), individual proteins from generalists may have a much wider substrate spectrum. Greater functional flexibility could in theory allow generalists to cope with the unpredictability of plant defense (1).Only a f...

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“…Hence, studying the induction profile of insect detoxification enzymes has been suggested as a means to identify the major enzymes involved in insecticide detoxification (Poupardin et al, 2008). Recently, this approach was used to identify two P450 genes (CYP6B1 and CYP6B3) in P. polyxenes induced by and metabolizing furanocoumarins, toxins produced by their host plant (Petersen et al, 2001). Similarly, other P450 genes capable of metabolizing xanthotoxin were characterized in H. zea Sasabe et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization of two novel deltamethrin‐inducible P450 genes from Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae)

Jiang

Tang

et al. 2010

Arch Insect Biochem Physiol

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Two novel P450 genes, CYP6CE1 and CYP6CE2 (GenBank accession number: EF421245 and EF421246), were cloned and characterized from psocid, Liposcelis bostrychophila. CYP6CE1 and CYP6CE2 contain open reading frames of 1,581 and 1,563 nucleotides that encode 527 and 521 amino acid residues, respectively. The putative proteins of CYP6CE1 and CYP6CE2 show predicted molecular weights of 60.76 and 59.83 kDa with a theoretical pI of 8.58 and 8.78, respectively. CYP6CE1 and CYP6CE2 share 74% identity with each other, and the deduced proteins are typical microsomal P450s sharing signature sequences with other insect CYP6 P450s. Both CYP6CE1 and CYP6CE2 share the closest identities with Hodotermopsis sjoestedti CYP6AM1 at 48% among the published sequences. Phylogenetic analysis showed a closer relationship of CYP6CE1 and CYP6CE2 with CYP6 members of other insects than with those from other families. Quantitative real-time RT-PCR showed that both CYP6CE1 and CYP6CE2 are expressed at all developmental stages tested. Interestingly, CYP6CE2 transcripts decreased from the highest in 1st nymph to the lowest in adults, which seemed to suggest developmental regulation. However, neither CYP6CE1 nor CYP6CE2 were stage specific. The CYP6CE1 and CYP6CE2 transcripts in adults increased significantly after deltamethrin exposure. Recombinant protein expression studies are needed to determine the real functions of these proteins. r

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Expression of CYP6B1 and CYP6B3 cytochrome P450 monooxygenases and furanocoumarin metabolism in different tissues of Papilio polyxenes (Lepidoptera: Papilionidae)

Cited by 92 publications

References 37 publications

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Structural and functional divergence of insect CYP6B proteins: From specialist to generalist cytochrome P450

Molecular characterization of two novel deltamethrin‐inducible P450 genes from Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae)

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