Iridoid biosynthesis in Chrysomelina larvae: Fat body produces early terpenoid precursors

Insect Biochemistry and Molecular Biology

Volumn 37, Issue 3, 2007, Pages 255-265

  Burse, Antje ^a   Schmidt, Axel ^b   Frick, Sindy ^a   Kuhn, Jürgen ^a   Gershenzon, Jonathan ^b   Boland, Wilhelm ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b Department of Biochemistry ^*  (Germany)

Author keywords

3 hydroxy 3 methylglutaryl CoA reductase; Chemical defense; Fat body; Iridoids; Isoprenyl diphosphate synthase; Leaf beetle

Indexed keywords

BENZYL ALCOHOL DERIVATIVE; COMPLEMENTARY DNA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; IRIDOID; SALICIN; TERPENE;

ANIMAL; ARTICLE; BEETLE; COMPARATIVE STUDY; ENZYMOLOGY; FAT BODY; GENETICS; LARVA; METABOLISM; MOLECULAR CLONING;

ANIMALS; BEETLES; BENZYL ALCOHOLS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FAT BODY; HYDROXYMETHYLGLUTARYL COA REDUCTASES; IRIDOIDS; LARVA; TERPENES;

CHRYSOMELA POPULI; COLEOPTERA; GASTROPHYSA VIRIDULA; PHAEDON COCHLEARIAE;

EID: 33846844930     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2006.11.011     Document Type: Article

References (53)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J.H., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25 (1997) 3389-3402
2. Bearfield J.C., Keeling C.I., Young S., Blomquist G.J., and Tittiger C. Isolation, endocrine regulation and mRNA distribution of the 3-hydroxy-3-methylglutaryl coenzyme A synthase (HMG-S) gene from the pine engraver, Ips pini (Coleoptera: Scolytidae). Insect Mol. Biol. 15 (2006) 187-195
3. Belles X., Martin D., and Piulachs M.-D. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annu. Rev. Entomol. 50 (2005) 181-199
4. Blum M.S. Antipredatory devices in larvae of the Chrysomelidae: an unidentified synthesis for defensive electicism. In: Jolivet P.H., Cox M.L., and Petitpierre E. (Eds). Novel Aspects of the Biology of the Chrysomelidae (1994), Kluwer Academics Publishers, Doderecht, The Netherlands 277-288
5. Blum M.S., Wallace J.B., Duffield R.M., Brand J.M., Fales H.M., and Sokoloski E.A. Chrysomelidial in the defensive secretion of the leaf beetle Gastrophysa cyanea Melsheimer. J. Chem. Ecol. 4 (1978) 47-53
6. Brueckmann M., Termonia A., Pasteels J.M., and Hartmann T. Characterization of an extracellular salicyl alcohol oxidase from larval defensive secretions of Chrysomela populi and Phratora vitellinae (Chrysomelina). Insect Biochem. Mol. Biol. 32 (2002) 1517-1523
7. Burke C.C., Wildung M.R., and Croteau R. Geranyl diphosphate synthase: Cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc. Natl. Acad. Sci. USA 96 (1999) 13062-13067
8. Chun K.T., and Simoni R.D. The role of the membrane domain in the regulated degradation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. J. Biol. Chem. 267 (1992) 4236-4246
9. Daloze D., and Pasteels J.M. Isolation of 8-hydroxygeraniol-8-O-beta-D-glucoside, a probable intermediate in biosynthesis of iridoid monoterpenes, from defensive secretions of Plagiodera versicolora and Gastrophysa viridula (Coleoptera, Chrysomelidae). J. Chem. Ecol. 20 (1994) 2089-2097
10. Edwards P.A., and Ericsson J. Sterols and isoprenoids: signaling molecules derived from the cholesterol biosynthetic pathway. Annu. Rev. Biochem. 68 (1999) 157-185
11. Feld B.K., Pasteels J.M., and Boland W. Phaedon cochleariae and Gastrophysa viridula (Coleoptera: Chrysomelidae) produce defensive iridoid monoterpenes de novo and are able to sequester glycosidically bound terpenoid precursors. Chemoecology 11 (2001) 191-198
12. Feyereisen R., and Farnsworth D.E. Characterization and regulation of HMG-CoA reductase during a cycle of juvenile-hormone synthesis. Mol. Cell. Endocrinol. 53 (1987) 227-238
13. Friesen J., and Rodwell V. The 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) reductases. Genome Biol. 5 (2004) 248
14. Gil G., Faust J.R., Chin D.J., Goldstein J.L., and Brown M.S. Membrane-bound domain of HMG CoA reductase is required for sterol-enhanced degradation of the enzyme. Cell 41 (1985) 249-258
15. Gilg A.B., Bearfield J.C., Tittiger C., Welch W.H., and Blomquist G.J. Isolation and functional expression of an animal geranyl diphosphate synthase and its role in bark beetle pheromone biosynthesis. Proc. Natl. Acad. Sci. USA 102 (2005) 9760-9765
16. Goldstein J.L., and Brown M.S. Regulation of the mevalonate pathway. Nature 343 (1990) 425-430
17. Hall G.M., Tittiger C., Andrews G.L., Mastick G.S., Kuenzli M., Luo X., Seybold S.J., and Blomquist G.J. Midgut tissue of male pine engraver, Ips pini, synthesizes monoterpenoid pheromone component ipsdienol de novo. Naturwissenschaften 89 (2002) 79-83
18. Hall G.M., Tittiger C., Blomquist G.J., Andrews G.L., Mastick G.S., Barkawi L.S., Bengoa C., and Seybold S.J. Male Jeffrey pine beetle, Dendroctonus jeffreyi, synthesizes the pheromone component frontalin in anterior midgut tissue. Insect Biochem. Mol. Biol 32 (2002) 1525-1532
19. Haunerland N.H., and Shirk P.D. Regional and functional differentiation in the insect fat body. Annu. Rev. Entomol. 40 (1995) 121-145
20. Hilker M., and Schulz S. Composition of larval secretion of Chrysomela lapponica (Coleoptera, Chrysomelidae) and its dependence on host plant. J. Chem. Ecol. 20 (1994) 1075-1093
21. Istvan E.S., Palnitkar M., Buchanan S.K., and Deisenhofer J. Crystal structure of the catalytic portion of human HMG-CoA reductase: insights into regulation of activity and catalysis. EMBO J. 19 (2000) 819-830
22. Ivarsson P., Tittiger C., Blomquist C., Borgeson C.E., Seybold S.J., Blomquist G.J., and Hogberg H.E. Pheromone precursor synthesis is localized in the metathorax of Ips paraconfusus Lanier (Coleoptera, Scolytidae). Naturwissenschaften 85 (1998) 507-511
23. Keeling C.I., Blomquist G.J., and Tittiger C. Coordinated gene expression for pheromone biosynthesis in the pine engraver beetle, Ips pini (Coleoptera: Scolytidae). Naturwissenschaften 91 (2004) 324-328
24. Keeling C.I., Bearfield J.C., Young S., Blomquist G.J., and Tittiger C. Effects of juvenile hormone on gene expression in the pheromone-producing midgut of the pine engraver beetle, Ips pini. Insect Mol. Biol. 15 (2006) 207-216
25. Kuhn J., Pettersson E.M., Feld B.K., Burse A., Termonia A., Pasteels J.M., and Boland W. Selective transport systems mediate sequestration of plant glucosides in leaf beetles: A molecular basis for adaptation and evolution. Proc. Natl. Acad. Sci. USA 101 (2004) 13808-13813
26. Kuhn J., Pettersson E.M., Feld B.K., Nie L., Tolzin-Banasch K., Machkour M'Rabet S., Pasteels J.M., and Boland W. Sequestration of plant-derived phenolglucosides by larvae of the leaf beetle Chrysomela lapponica: Thioglucosides as Mechanistic Probes. J. Chem. Ecol. 33 (2007) 5-24
27. Laurent P., Braekman J.C., Daloze D., and Pasteels J. Biosynthesis of defensive compounds from beetles and ants. Eur. J. Org. Chem. (2003) 2733-2743
28. Laurent P., Braekman J.C., and Daloze S. Insect chemical defense, Chemistry of Pheromones and Other Semiochemicals II. Top. Curr. Chem. 240 (2005) 167-229
29. Liang P.H., Ko T.P., and Wang A.H.J. Structure, mechanism and function of prenyltransferases. Eur. J. Biochem. 269 (2002) 3339-3354
30. - Δ Δ CT method. Methods 25 (2001) 402-408
31. Lorenz M., Boland W., and Dettner K. Biosynthesis of iridodials in the defense glands of beetle larvae (Chrysomelinae). Angew. Chem. Int. Edit. 32 (1993) 912-914
32. Meinwald J., Jones T.H., Eisner T., and Hicks K. New methylcyclopentanoid terpenes from the larval defensive secretion of a chrysomelid beetle (Plagiodera versicolora). Proc. Natl. Acad. Sci. USA 74 (1977) 2189-2193
33. Nardi J.B., Young A.G., Ujhelyi E., Tittiger C., Lehane M.J., and Blomquist G.J. Specialization of midgut cells for synthesis of male isoprenoid pheromone components in two scolytid beetles, Dendroctonus jeffreyi and Ips pini. Tissue Cell 34 (2002) 221-231
34. Oldham N.J., Veith M., Boland W., and Dettner K. Iridoid monoterpene biosynthesis in insects-evidence for a de novo pathway occurring in the defensive glands of Phaedon armoraciae (chrysomelidae) leaf beetle larvae. Naturwissenschaften 83 (1996) 470-473
35. Pasteels J.M., Braekman J.C., Daloze D., and Ottinger R. Chemical defence in chrysomelid larvae and adults. Tetrahedron 38 (1982) 1891-1897
36. Pasteels J.M., Rowell-Rahier M., Braekman J.C., and Dupont A. Salicin from host plant as precursor of salicyl aldehyde in defensive secretion of chrysomeline larvae. Physiol. Entomol. 8 (1983) 307-314
37. Pasteels J.M., Duffey S., and Rowell-Rahier M. Toxins in chrysomelid beetles, possible evolutionary sequence from de novo synthesis to derivation from food-plant chemicals. J. Chem. Ecol. 16 (1990) 211-222
38. Pasteels J.M., Rowell-Rahier M., Braekman J.C., and Daloze D. Chemical defence of adult leaf beetles updated. In: Jolivet P.H., Cox M.L., and Petitpierre E. (Eds). Novel Aspects of the Biology of the Chrysomelidae (1994), Kluwer Academics Publishers, Doderecht, The Netherlands 289-301
39. Renner K. Über die ausstülpbaren Hautblasen der Larven von Gastroidea viridula De Geer und ihre ökologische Bedeutung (Coleoptera: Chrysomelidae). Beitr. Ent. 20 (1970) 527-533
40. Sato R., Goldstein J.L., and Brown M.S. Replacement of serine-871 of hamster 3-hydroxy-3-methylglutaryl-CoA reductase prevents phosphorylation by AMP-activated kinase and blocks inhibition of sterol synthesis induced by ATP depletion. Proc. Natl. Acad. Sci. USA 90 (1993) 9261-9265
41. Schulz S., Gross J., and Hilker M. Origin of the defensive secretion of the leaf beetle Chrysomela lapponica. Tetrahedron 53 (1997) 9203-9212
42. Seybold S.J., and Tittiger C. Biochemistry and molecular biology of de novo isoprenoid pheromone production in the Scolytidae. Annu. Rev. Entomol. 48 (2003) 425-453
43. Soe A., Bartram S., Gatto N., and Boland W. Are iridoids in leaf beetle larvae synthesized de novo or derived from plant precursors? A methodological approach. Isot. Environ. Health Stud. 40 (2004) 175-180
44. Soetens P., Pasteels J.M., and Daloze D. A simple method for in vivo testing of glandular enzymatic activity on potential precursors of larval defensive compounds in Phratora species (Coleoptera: Chrysomelinae). Experientia 49 (1993) 1024-1026
45. Termonia A., and Pasteels J.M. Larval chemical defence and evolution of host shifts in Chrysomela leaf beetles. Chemoecology 9 (1999) 13-23
46. Termonia A., Hsiao T.H., Pasteels J.M., and Milinkovitch M.C. Feeding specialization and host-derived chemical defense in chrysomeline leaf beetles did not lead to an evolutionary dead end. Proc. Natl. Acad. Sci. USA 98 (2001) 3909-3914
47. Tholl D., Kish C.M., Orlova I., Sherman D., Gershenzon J., Pichersky E., and Dudareva N. Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell 16 (2004) 977-992
48. Tillman J.A., Lu F., Goddard L.M., Donaldson Z.R., Dwinell S.C., Tittiger C., Hall G.M., Storer A.J., Blomquist G.J., and Seybold S.J. Juvenile hormone regulates de novo isoprenoid aggregation pheromone biosynthesis in pine bark beetles, Ips spp., through transcriptional control of HMG-CoA reductase. J. Chem. Ecol. 30 (2004) 2459-2494
49. Tittiger C., Blomquist G.J., Ivarsson P., Borgeson C.E., and Seybold S.J. Juvenile hormone regulation of HMG-R gene expression in the bark beetle Ips paraconfusus (Coleoptera: Scolytidae): implications for male aggregation pheromone biosynthesis. Cell. Mol. Life Sci. 55 (1999) 121-127
50. Tittiger C., Barkawi L.S., Bengoa C.S., Blomquist G.J., and Seybold S.J. Structure and juvenile hormone-mediated regulation of the HMG-CoA reductase gene from the Jeffrey pine beetle, Dendroctonus jeffreyi. Mol. Cell. Endocrinol. 199 (2003) 11-21
51. Veith M., Lorenz M., Boland W., Simon H., and Dettner K. Biosynthesis of iridoid monoterpenes in insects-defensive secretions from larvae of leaf beetles (Coleoptera, Chrysomelidae). Tetrahedron 50 (1994) 6859-6874
52. Veith M., Dettner K., and Boland W. Stereochemistry of an alcohol oxidase from the defensive secretion of larvae of the leaf beetle Phaedon armoraciae (Coleoptera, Chrysomelidae). Tetrahedron 52 (1996) 6601-6612
53. von Nickisch-Rosenegk E., Detzel A., Wink M., and Schneider D. Carrier-mediated uptake of digoxin by larvae of the cardenolide sequestering moth, Syntomeida epilais. Naturwissenschaften 77 (1990) 336-338