CHARACTERIZATION, PRODUCTION, AND UTILIZATION OF PHYTOCHEMICALS FROM AGRICULTURAL PRODUCTS
Location: National Center for Agricultural Utilization Research
Title: CYTOCHROME P450-MEDIATED METABOLISM OF XANTHOTOXIN BY PAPILIO MULTICAUDATUS
| Mao, Wenfu - U OF IL, URBANA, IL |
| Zangerl, Arthur - U OF IL, URBANA, IL |
| Mcgovern, Jennifer - U OF IL, URBANA, IL |
| Berenbaum, May - U OF IL, URBANA, IL |
Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 1, 2006
Publication Date: March 30, 2006
Citation: Mao, W., Berhow, M.A., Zangerl, A.R., Mcgovern, J., Berenbaum, M.R. 2006. Cytochrome p450-mediated metabolism of xanthotoxin by Papilio multicaudatus. Journal of Chemical Ecology. 32:523-536.
Interpretive Summary: A few insect species are able to feed on plant species that produce poisons that are toxic to most living things. The wild parsley plant produces a series of toxic compounds known as the furanocoumarins that can disrupt living cells. The Eastern Tiger Swallowtail butterfly larvae can consume leaf material containing up to 0.3% furanocoumarin with no detectable negative effects. Examination of the guts of these insect larvae after feeding show that they are able to metabolize the furanocourmarins into nontoxic products. These products have been identified in this paper and have been shown to occur in one other butterfly species. This is a step towards a better understanding of how certain insect species are able to detoxify plant toxins through enzymatic oxidation.
Within the genus Papilio, the P. glaucus group contains the most polyphagous species within the entire family Papilionidae. The majority of species in the genus are associated with hostplants in the families Rutaceae and Apiaceae and characterizing most of these species are secondary metabolites called furanocoumarins. Recent phylogenetic studies suggest that furanocoumarin metabolism is an ancestral trait, with the glaucus group derived from ancestors associated with furanocoumarin-containing Rutaceae. In this study, we examined this relationship by conducting a gravimetric analysis of growth using various concentrations of the furanocoumarin xanthotoxin. Papilio multicaudatus, the putative ancestor of the glaucus group, includes at least one furanocoumarin-containing rutaceous species among its hostplants; this species can consume leaf tissue containing up to 0.3% xanthotoxin with no detectable effect on relative growth rate, relative consumption rate, or efficiency of conversion of ingested food. As is the case for other Papilio species, xanthotoxin metabolism is mediated by cytochrome P450 monooxygenases (P450s). Ingestion of xanthotoxin by ultimate instar P. multicaudatus increases activity up to 30-fold in a dose-dependent fashion. Midguts of induced larvae can also effectively metabolize six other furanocoumarins, including both linear (bergapten, isopimpinellin, imperatorin) and angular (angelicin, sphondin) forms. A metabolite of xanthotoxin in the frass from xanthotoxin-treated larvae, identified as 6-(7-hydroxy-8-methoxycoumaryl)-acetic acid (HCA) by MS-MS and NMR analyses, is identical to one from the frass of P. polyxenes. The occurrence of this metabolite in two swallowtails and the presence of a second metabolite of xanthotoxin, 6-(7-hydroxy-8-methoxycoumaryl)-hydroxyethanol (HCHA), in the frass of both P. polyxenes and Depressaria pastinacella are consistent with the suggestion that lepidopterans share as the first step of xanthotoxin metabolism the P450-mediated epoxidation of the furan ring 2’-3’double bond.