Journal of Chemical Ecology

, Volume 27, Issue 10, pp 1911–1928 | Cite as

Herbivore-Induced Volatile Production by Arabidopsis thaliana Leads to Attraction of the Parasitoid Cotesia rubecula: Chemical, Behavioral, and Gene-Expression Analysis

  • Remco M. P. Van Poecke
  • Maarten A. Posthumus
  • Marcel Dicke


Many plant species defend themselves against herbivorous insects indirectly by producing volatiles in response to herbivory. These volatiles attract carnivorous enemies of the herbivores. Research on the model plant Arabidopsis thaliana (L.) Heynh. has contributed considerably to the unraveling of signal transduction pathways involved in direct plant defense mechanisms against pathogens. Here, we demonstrate that Arabidopsis is also a good candidate for studying signal transduction pathways involved in indirect defense mechanisms by showing that: (1) Adult females of Cotesia rubecula, a specialist parasitic wasp of Pieris rapae caterpillars, are attracted to P. rapae-infested Arabidopsis plants. (2) Arabidopsis infested by P. rapae emits volatiles from several major biosynthetic pathways, including terpenoids and green leaf volatiles. The blends from herbivore-infested and artificially damaged plants are similar. However, differences can be found with respect to a few components of the blend, such as two nitriles and the monoterpene myrcene, that were produced exclusively by caterpillar-infested plants, and methyl salicylate, that was produced in larger amounts by caterpillar-infested plants. (3) Genes from major biosynthetic pathways involved in volatile production are induced by caterpillar feeding. These include AtTPS10, encoding a terpene synthase involved in myrcene production, AtPAL1, encoding phenylalanine ammonia-lyase involved in methyl salicylate production, and AtLOX2 and AtHPL, encoding lipoxygenase and hydroperoxide lyase, respectively, both involved in the production of green leaf volatiles. AtAOS, encoding allene oxide synthase, involved in the production of jasmonic acid, also was induced by herbivory.

Pieris rapae Lepidoptera Hymenoptera tritrophic interactions foraging behavior headspace analysis terpenoids green leaf volatiles methyl salicylate nitriles 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. AGELOPOULOS, N. G. and KELLER, M. A. 1994. Plant-natural enemy association in the tritrophic system, Cotesia rubecula-Pieris rapae-Brassicaceae (Crucifera): II. Preference of C. rubecula for landing and searching. J. Chem. Ecol. 20:1735-1748.Google Scholar
  2. BATE, N. J., SIVASANKAR, S., MOXON, C., RILEY, J. M. C., THOMPSON, J. E., and ROTHSTEIN, S. J. 1998. Molecular characterization of an Arabidopsis gene encoding hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant Physiol. 117:1393-1400.PubMedGoogle Scholar
  3. BELL, E. and MULLET, J. E. 1993. Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol. 103:1133-1137.PubMedGoogle Scholar
  4. BLAAKMEER, A., GEERVLIET, J. B. F., LOON, J. J. A., POSTHUMUS, M. A., VAN BEEK, T. A., and DE GROOT, A. E. 1994. Comparative headspace analysis of cabbage plants damaged by two species of Pieris caterpillars: Consequences for in-flight host location by Cotesia parasitoids. Entomol. Exp. Appl. 73:175-182.Google Scholar
  5. BLECHERT, S., BRODSCHELM, W., HOLDER, S., KAMMERER, L., KUTCHAN, T. M., MUELLER, M. J., XIA, Z. Q., and ZENK, M. H. 1995. The octadecanoic pathway: Signal molecules for the regulation of secondary pathways. Proc. Natl. Acad. Sci. USA 92:4099-4105.PubMedGoogle Scholar
  6. BOHLMANN, F., ZDERO, C., BERGER, D., SUWITA, A., MAHANTA, P., and JEFFREY, C. 1979. Neue furanoeremophilane und weitere inhaltsstoffe aus Südafrikanischen Senecio-arten. Phytochemistry 18:79-93.Google Scholar
  7. BOHLMANN, J., MEYER-GAUEN, G., and CROTEAU, R. 1998. Plant terpenoid synthases: Molecular biology and phylogenetic analysis. Proc. Natl. Acad. Sci. USA 95:4126-4133.PubMedGoogle Scholar
  8. BOHLMANN, J., MARTIN, D., OLDHAM, N. J., and GERSHENZON, J. 2000. Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization and functional expression of a myrcene/ocimene synthase. Arch. Biochem. Biophys. 375:261-269.PubMedGoogle Scholar
  9. BOLAND, W. 1995. The chemistry of gamete attraction: Chemical structures, biosynthesis, and (a)biotic degradation of algal pheromones. Proc. Natl. Acad. Sci. USA 92:37-43.PubMedGoogle Scholar
  10. BOLAND, W., HOPKE, J., DONATH, J., NüSKE, J., and BUBLITZ, F. 1995. Jasmonic acid and coronatin induce odor production in plants. Angew. Chem. Int. Ed. Engl. 34:1600-1602.Google Scholar
  11. BOLAND W., KOCH, T., KRUMM, T., PIEL, J., and JUX, A. 1999. Induced biosynthesis of insect semiochemicals in plants, pp. 110-131, in D. J. Chadwick and J. A. Goode (eds.). Insect-Plant Interactions and Induced Plant Defense. John Wiley & Sons, New York.Google Scholar
  12. BOUWMEESTER, H. J., VERSTAPPEN, F. W. A., POSTHUMUS, M. A., and DICKE, M. 1999. Spider miteinduced (3S)-(E)-neridol synthase activity in cucumber and lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol. 121:173-180.PubMedGoogle Scholar
  13. CHANG, S., PURYEAR, J., and CAIRNEY, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11:113-116.Google Scholar
  14. CHURCH, G. and GILBERT, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 92:4114-4119.Google Scholar
  15. DELANEY, T. P., UKNES, S., VERNOOIJ, B., FRIEDRICH, L., WEYMANN, K., NEGROTTO, D., GAFFNEY, T., GUTRELLA, M., KESSMANN, H., WARD, E., and RYALS, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250.Google Scholar
  16. DEMPSEY, D. A., SHAH, J., and KLESSIG, D. F. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18:547-575.Google Scholar
  17. DICKE, M. 1999. Evolution of induced indirect defense of plants, pp. 62-88, in R. Tollrian and C. J. Harvell (eds.). The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, New Jersey.Google Scholar
  18. DICKE, M., VAN BEEK, T. A., POSTHUMUS, M. A., BEN DOM, N., VAN BOKHOVEN, H., and DE GROOT, A. E. 1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. Involvement of host plant in its production. J. Chem. Ecol. 16:381-396.Google Scholar
  19. DICKE, M., TAKABAYASHI, J., POSTHUMUS, M. A., SCHUTTE, C., and KRIPS, O. E. 1998. Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: Variation in production of cues and in response of predatory mites. Exp. Appl. Acar. 22:311-333.Google Scholar
  20. DICKE, M., GOLS, R., LUDEKING, D., and POSTHUMUS, M. A. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in Lima bean plants. J. Chem. Ecol. 25:1907-1922.Google Scholar
  21. DIETRICH, R. A., DELANEY, T. P., UKNES, S. J., WARD, E. R., RYALS, J. A., and DANGL, J. L. 1994. Arabidopsis mutants simulating disease resistance response. Cell 77:565-577.PubMedGoogle Scholar
  22. DIXON, R. A. and PAIVA, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085-1097.PubMedGoogle Scholar
  23. GEERVLIET, J. B. F., VET, L. E. M., and DICKE, M. 1994. Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoid Cotesia rubecula. Entomol. Exp. Appl. 73:289-297.Google Scholar
  24. GEERVLIET, J. B. F., POSTHUMUS, M. A., VET, L. E. M., and DICKE, M. 1997. Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J. Chem. Ecol. 23:2935-2954.Google Scholar
  25. GERSHENZON, J. and CROTEAU, R. 1991. Terpenoids, pp. 165-219, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. 1. Academic Press, New York.Google Scholar
  26. GOLS, R., POSTHUMUS, M. A., and DICKE, M. 1999. Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis. Entomol. Exp. Appl. 93:77-86.Google Scholar
  27. GRANT-PETERSSON, J. and RENWICK, J. A. A. 1996. Effects of ultraviolet-B exposure of Arabidopsis thaliana on herbivory by two crucifer-feeding insects (Lepidoptera). Environ. Entomol. 25:135-142.Google Scholar
  28. HOPKE, J., DONATH, J., BLECHERT, S., and BOLAND, W. 1994. Herbivore-induced volatiles: The emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a β-glucosidase and jasmonic acid. FEBS Lett. 352:146-150.PubMedGoogle Scholar
  29. KARBAN, R. and BALDWIN, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois.Google Scholar
  30. LAUDERT, D., PFANNSCHMIDT, U., LOTTSPEICH, F., HOLLäNDER-CZYTKO, H., and WEILER, E. W. 1996. Cloning, molecular and functional characterization of Arabidopsis thaliana allene oxide synthase (CYP 74), the first enzyme of the octadecanoid pathway to jasmonates. Plant Mol. Biol. 31:323-335.PubMedGoogle Scholar
  31. LEE, H. L., LéON, J., and RASKIN, I. 1995. Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. USA 92:4076-4079.PubMedGoogle Scholar
  32. LICHTENTHALER, H.K. 1999. The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 50:47-65.PubMedGoogle Scholar
  33. LOUGHRIN, J. H., MANUKIAN, A., HEATH, R. R., TURLINGS, T. C. J., and TUMLINSON, J. H. 1994. Diurnal cycle of emission of induced volatile terpenoids herbivore-injured cotton plants. Proc. Natl. Acad. Sci. USA 91:11836-11840.Google Scholar
  34. MATTIACCI, L., DICKE, M., and POSTHUMUS, M. A. 1995. β-Glucosidase: An elicitor of herbivoreinduced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. USA 92:2036-2040.PubMedGoogle Scholar
  35. MAUCH-MANI, B. and SLUSARENKO, A. J. 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203-212.PubMedGoogle Scholar
  36. MAURICIO, R. 1998. Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am. Nat. 151:20-28.Google Scholar
  37. MAURICIO, R. and RAUSHER, M. D. 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 5:1435-1444.Google Scholar
  38. MIZUTANI, M., OHTA, D., and SATO, R. 1997. Isolation of a cDNA and a genomic clone encoding cinnamate-4-hydroxylase from Arabidopsis and its expression manner in planta. Plant Physiol. 113:755-763.PubMedGoogle Scholar
  39. MCCLOUD, E. S. and BALDWIN, I. T. 1997. Herbivory and caterpillar regurgitants amplify the woundinduced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430-435.Google Scholar
  40. MCCONN, M., CREELMAN, R. A., BELL, E., MULLET, J. E., and BROWSE, J. 1997. Jamonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94:5473-5477.PubMedGoogle Scholar
  41. OHL, S., HEDRICK, S. A., CHORY, J., and LAMB, J. C. 1990. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell 2:837-848.CrossRefPubMedGoogle Scholar
  42. PARé, P. W. and TUMLINSON, J. H. 1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol. 114:1161-1167.PubMedGoogle Scholar
  43. PIETERSE, C. M. J. and VAN LOON, L. C. 1999. Salicylic acid-independent plant defence pathways. Trends Plant Sci. 4:52-58.PubMedGoogle Scholar
  44. PIETERSE, C. M. J., VAN WEES, S. C. M., VAN PELT, J. A., KNOESTER, M., LAAN, R., GERRITS, H., WEISBEEK, P. J., and VAN LOON, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.PubMedGoogle Scholar
  45. REYMOND, P., WEBER, H., DAMOND, M., and FARMER, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707-719.PubMedGoogle Scholar
  46. SAMBROOK, J., FRITSCH, E. F., and MANIATIS, T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.Google Scholar
  47. STOTZ, H. U., PITTENDRIGH, B. R., KROYMANN, J., WENIGER, K., FRITSCHE, J., BAUIKE, A., and MITCHELL-OLDS, T. 2000. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 124:1007-1017.PubMedGoogle Scholar
  48. TAKABAYASHI, J., DICKE, M., and POSTHUMUS, M. A. 1991. Variation in composition of predatorattracting allelochemicals emitted by herbivore-infested plants: Relative influence of plant and herbivore. Chemoecology 2:1-6.Google Scholar
  49. TAKABAYASHI, J., DICKE, M., and POSTHUMUS, M. A. 1994. Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors. J. Chem. Ecol. 20:1329-1354.Google Scholar
  50. THALER, J. S. 1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686-687.Google Scholar
  51. THOMMA, B. P. H. J., EGGERMONT, K., PENNICKX, I. A. M. A., MAUCH-MANI, B.M., VOGLSANG, R., CAMMUE, B. P. A., and BROEKAERT, W. F. 1998. Separate jasmonate-dependent and salicylatedependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95:15107-15111.PubMedGoogle Scholar
  52. TURLINGS, T. C. J., TUMLINSON, J. H., and LEWIS, W. J. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251-1253.Google Scholar
  53. TURLINGS, T. C. J., TUMLINSON, J. H., HEATH, R. R., PROVEAUX, A. T., and DOOLITTLE, R. E. 1991. Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J. Chem. Ecol. 17:2235-2251.Google Scholar
  54. TURLINGS, T. C. J., LOUGHRIN, J. H., MCCALL P. J., RöSE U. S. R., LEWIS, W. J., and TUMLINSON, J. H. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. USA 92:4169-4174.PubMedGoogle Scholar
  55. VAN LOON, J. J. A., DE BOER, J. G., and DICKE, M. 2000. Parasitoid-plant mutualism: Parasitoid attack of herbivore increases plant reproduction. Entomol. Exp. Appl. 97:219-227.Google Scholar
  56. WANNER, L. A., LI, G., WARE, D., SOMSSICH, I. E., and DAVIS, K. R. 1995. The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana. Plant Mol. Biol. 27:327-338.PubMedGoogle Scholar
  57. WHITMAN, D. W. and ELLER, F. J. 1990. Parasitic wasps orient to green leaf volatiles. Chemoecology 1:69-75.Google Scholar
  58. YANO, S. and OHSAKI, N. 1993. The phenology and intrinsic quality of wild crucifers that determine the community structure of their herbivorous insects. Res. Pop. Ecol. 35:151-170.Google Scholar

Copyright information

© Plenum Publishing Corporation 2001

Authors and Affiliations

  • Remco M. P. Van Poecke
    • 1
  • Maarten A. Posthumus
    • 2
  • Marcel Dicke
    • 1
  1. 1.Laboratory of EntomologyWageningen UniversityWageningenThe Netherlands
  2. 2.Laboratory of Organic ChemistryWageningen UniversityWageningenThe Netherlands

Personalised recommendations