Abstract
Papilio glaucus caterpillars encounter a diverse array of sesquiterpene lactones, including parthenolide, in the leaves of host plants Liriodendron tulipifera and Magnolia virginiana. These compounds are toxic to unadapted herbivores, and the development of P. glaucus caterpillars likely depends on their ability to excrete or detoxify them efficiently. A new metabolite of parthenolide, 2-α-hydroxydihydroparthenolide, identified by crystal structure determination and nuclear magnetic resonance, was present in the waste of the caterpillars. The parent compound was modified by the reduction of an α-methylene group, rendering the compound less reactive, and the addition of a hydroxyl group, which increases the polarity and prepares it for the conjugation reactions of phase II metabolism. Unmetabolized parthenolide was also present in large amounts in waste. P. glaucus larvae are apparently capable of excreting intact sesquiterpene lactones and sesquiterpene lactone metabolites during consumption of foliage rich in these compounds.
Similar content being viewed by others
References
M. Aregullín E. Rodríguez (2003) ArticleTitleSesquiterpene lactone sequestration by the tortoise beetle Physonota arizonae (Cassidinae) Rev. Soc. Quim. Méx. 47 143–145
R. V. Barbehenn (2001) ArticleTitleRoles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals Arch. Insect Biochem. Physiol. 47 86–99 Occurrence Handle10.1002/arch.1039 Occurrence Handle11376455
R. V. Barbehenn (2003) ArticleTitleAntioxidants in grasshoppers: Higher levels defend the midgut tissues of a polyphagous species than a graminivorous species J. Chem. Ecol. 29 683–702 Occurrence Handle10.1023/A:1022824820855 Occurrence Handle12757328
R. V. Barbehenn S. L. Bumgarner E. F. Roosen M. M. Martin (2001) ArticleTitleAntioxidant defenses in caterpillars: role of the ascorbate-recycling system in the midgut lumen J. Insect Physiol. 47 349–357 Occurrence Handle10.1016/S0022-1910(00)00125-6 Occurrence Handle11166299
M. R. Berenbaum (1986) Target site insensitivity in insect–plant interactions L. B. Brattsten S. Ahmad (Eds) Molecular Aspects of Insect–Plant Associations Plenum Press New York 257–272
M. R. Berenbaum (1995) Chemistry and oligophagy in the Papilionidae J. M. Scriber Y. Tsubaki R. C. Lederhouse (Eds) Swallowtail Butterflies: Their Ecology and Evolutionary Biology Scientific Publishers Gainesville 27–38
C. A. Boros F. R. Stermitz N. McFarland (1991) ArticleTitleProcessing of iridoid glycoside antirrinoside from Maurandya antirrhiniflora (Scrophulariaceae) by Meris paradoxa (Geometridae) and Lepipolys species (Noctuidae) J. Chem. Ecol. 17 1123–1133 Occurrence Handle10.1007/BF01402938
M. D. Bowers G. M. Puttick (1986) ArticleTitleFate of ingested iridoid glycosides in lepidopteran herbivores J. Chem. Ecol. 12 169–178 Occurrence Handle10.1007/BF01045600
L. B. Brattsten (1986) Fate of ingested plant allelochemicals in herbivorous insects L. B. Brattsten S. Ahmad (Eds) Molecular Aspects of Insect–Plant Associations Plenum Press New York 211–255
A. M. Clark C. D. Hufford (1979) ArticleTitleMicrobial transformations of the sesquiterpene lactone costunolide J. Chem. Soc. Perkin Trans. I 3022–3028 Occurrence Handle10.1039/p19790003022
M. B. Cohen M. A. Schuler M. R. Berenbaum (1992) ArticleTitleA host-inducible cytochrome P-450 from a host-specific caterpillar: molecular cloning and evolution Proc. Natl. Acad. Sci. USA 89 10920–10924 Occurrence Handle1279697
R. W. Doskotch S. L. Keely C. D. Hufford F. S. El-Feraly (1975) ArticleTitleNew sesquiterpene lactones from Liriodendron tulipifera Phytochemistry 14 769–773 Occurrence Handle10.1016/0031-9422(75)83032-9
Doskotch, R. W., Odell, T. M., and Girard, L. 1981. Phytochemicals and feeding behavior of gypsy moth larvae, pp. 657–666, in C. C. Doane and M. L. McManus (eds.). The Gypsy Moth: Research Towards Integrated Pest Management. U. S. Department of Agriculture, Technical Bulletin, Chap. 6.6.
K. Fiedler E. Krug P. Proksch (1993) ArticleTitleComplete elimination of hostplant quinolizidine alkaloids by larvae of a polyphagous lycaenid butterfly, Callophrys rubi Oecologia 94 441–445 Occurrence Handle10.1007/BF00317121
N. H. Fischer D. Vargas M. Menelaou (1992) Modern NMR methods in phytochemical studies N. H. Fischer M. B. Isman H. A. Stafford (Eds) Rec Adv in Phytochemistry, Volume 25: Modern Phytochemical Methods Plenum Press New York 281
N. H. Fischer T. Lu C. L. Cantrell J. Castañeda-Acosta L. Quijano S. G. Franzblau (1998) ArticleTitleAntimycobacterial evaluation of germacranolides in honour of Professor G. H. Neil Towers 75th birthday Phytochemistry 49 559–564 Occurrence Handle10.1016/S0031-9422(98)00253-2 Occurrence Handle9747541
A. M. Galal A. S. Ibrahim J. S. Mossa F. S. El-Feraly (1999) ArticleTitleMicrobial transformation of parthenolide Phytochemistry 51 761–765 Occurrence Handle10.1016/S0031-9422(99)00066-7
T. Ishikawa (1992) ArticleTitleThe ATP-dependent glutathione S-conjugate export pump Trends Biochem. Sci. 17 463–468 Occurrence Handle10.1016/0968-0004(92)90489-V Occurrence Handle1455517
M. B. Isman (1985) ArticleTitleToxicity and tolerance of sesquiterpene lactones in the migratory grasshopper, Melanoplus sanguinipes (Acrididae) Pestic. Biochem. Phys. 24 348–354 Occurrence Handle10.1016/0048-3575(85)90146-4
G. W. Ivie D. L. Bull R. C. Beier N. W. Pryor E. H. Oertli (1983) ArticleTitleMetabolic detoxification: mechanism of insect resistance to plant psoralens Science 221 374–376
G. N. Kumari Krishna S. Masilamani M. R. Ganesh S. Aravind (2003) ArticleTitleMicrobial transformation of zaluzanin-D Phytochemistry 62 1101–1104 Occurrence Handle10.1016/S0031-9422(02)00667-2 Occurrence Handle12591263
K. Lee E. Huang C. Piantadosi J. S. Pagano T. A. Geissman (1971) ArticleTitleCytotoxicity of sesquiterpene lactones Cancer Res. 31 1649–1654 Occurrence Handle4330633
S. H. P. Maddrell B. O. C. Gardiner (1976) ArticleTitleExcretion of alkaloids by Malpighian tubules of insects J. Exp. Biol. 64 267–281 Occurrence Handle932618
M. A. Marty R. I. Krieger (1984) ArticleTitleMetabolism of uscharidin, a milkweed cardenolide, by tissue homogenates of monarch butterfly larvae, Danaus plexippus J. Chem. Ecol. 10 945–956 Occurrence Handle10.1007/BF00987975
C. M. Passreiter M. B. Isman (1997) ArticleTitleAntifeedant bioactivity of sesquiterpene lactones from Neurolaena lobata and their antagonism by γ-aminobutyric acid Biochem. Syst. Ecol. 25 371–377 Occurrence Handle10.1016/S0305-1978(97)00023-9
A. M. Peters A. Amerongen Particlevan (1998) ArticleTitleRelationship between levels of sesquiterpene lactones in chicory and sensory evaluation J. Am. Soc. Hortic. Sci. 123 326–329
T. J. Schmidt (1999a) ArticleTitleToxic activities of sesquiterpene lactones: structural and biochemical aspects Curr. Org. Chem. 3 577–608
T. J. Schmidt (1999b) ArticleTitleQuantitative structure–cytotoxicity relationships within a series of helenanolide type sesquiterpene lactones Pharm. Pharmacol. Lett. 9 9–13
J. M. Scriber (1986) ArticleTitleOrigins of the regional feeding abilities in the tiger swallowtail butterfly: ecological monophagy and the Papilio glaucus australis subspecies in Florida Oecologia 71 94–103 Occurrence Handle10.1007/BF00377326
J. M. Scriber (1993) ArticleTitleAbsence of behavioral induction in oviposition preference of Papilio glaucus (Lepidoptera: Papilionidae) Great Lakes Entomol. 26 81–95
J. M. Scriber R. C. Lederhouse R. H. Hagan (1991) Foodplants and evolution within Papilio glaucus and Papilio troilus species groups (Lepidoptera: Papilionidae) P. W. Price T. M. Lewinsohn G. W. Fernandes W. W. Benson (Eds) Plant–Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions Wiley & Sons New York 341–373
Q. Song M. L. Gomez-Barrios F. R. Fronczek D. Vargas L. B. Thien N. H. Fischer (1998) ArticleTitleSesquiterpenes from southern Magnolia virginiana Phytochemistry 47 221–226 Occurrence Handle10.1016/S0031-9422(97)00412-3
Y. Takeda H. K. Mishima S. Kitamura K. Tatsumi (1997) ArticleTitlePurification and characterization of α,β-ketoalkene double bond reductases from bovine eyes Curr. Eye Res. 16 327–332 Occurrence Handle10.1076/ceyr.16.4.327.10694 Occurrence Handle9134321
J. Wen K. You S. Lee C. Song D. Kim (2002) ArticleTitleOxidative stress-mediated apoptosis J. Biol. Chem. 277 38954–38964 Occurrence Handle10.1074/jbc.M203842200 Occurrence Handle12151389
C. R. Wolf (1982) Oxidation of foreign compounds at carbon atoms W. B. Jakoby J. R. Bend J. Caldwell (Eds) Metabolic Basis of Detoxication: Metabolism of Functional Groups Academic Press New York 5–28
Acknowledgments
The authors are grateful to Drs. Mark Scriber and James Maudsley for the collection of the female butterflies in June of 2001 and 2002. Dr. Nikolaus Fischer first observed the presence of sesquiterpene lactone peaks in the NMR spectra of the frass of the Magnolia-fed caterpillars and provided helpful advice and comments throughout the isolation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Frankfater, C., Schühly, W., Fronczek, F.R. et al. Processing of a Sesquiterpene Lactone by Papilio glaucus Caterpillars. J Chem Ecol 31, 2541–2550 (2005). https://doi.org/10.1007/s10886-005-7612-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-005-7612-z