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 - UNIV OF IL, URBANA, IL |
| Zangerl, Arthur - UNIV OF IL, URBANA, IL |
| Mcgovern, Jennifer - UNIV OF IL, URBANA, IL |
| Berenbaum, May - UNIV OF IL, URBANA, IL |
Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: November 26, 2005
Publication Date: March 1, 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(3):523-536.
Interpretive Summary: A number of insect species in the genus Papilio (a butterfly species) are able to feed on specific plant species which contain the highly toxic furanocoumarins. This includes a number of species which are noxious weed species in North America. The long-term goal of this research is to enhance the biological control of these weed species through enhanced insect predation. This research work is aimed at developing an understanding of how these insects are able to metabolize these toxic compounds after ingestion, and to develop a further understanding of the enzymes amd genes involved in this metabolism. A butterfly species Papilio multicaudatus that may be the ancestor of several other butterfly species was shown to be able to ingest up to 0.3% by weight of furanocoumarins with no detrimental effects on its growth and development. Furthermore, analysis of the metabolites produced in the gut and feces of this insect showed that the first step was a cytochrome p-450 mediated oxidation step that is similar to two other insect species previously studied. The presence of this enzyme in the genetic is a key step in allowing these insects to successfully feed on plants containing furanocoumarins.
Within the genus Papilio, the P. glaucus group contains the most polyphagous species within the Papilionidae. The majority of species are associated with hostplants in the families Rutaceae and Apiaceae, and characterizing most 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 that used 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 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)-hydro-xyethanol 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 double bond.