Skip to main content
SpringerLink
Log in

Direct Proof of Ingested Food Regurgitation by Spodoptera littoralis Caterpillars during Feeding on Arabidopsis

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Oral secretions of herbivorous lepidopteran larvae contain a mixture of saliva and regurgitant from the insect gut. Different compounds from the oral secretions can be recognized by the host plants and, thus, represent elicitors that induce plant defenses against feeding herbivores. Exogenously applied oral secretions can initiate the biosynthesis of jasmonates, phytohormones involved in the regulation of plant defense. However, it is not known (a) whether or not non-manipulated insects indeed release oral secretions including gut-derived compounds into a leaf wound during the natural feeding process, or (b) whether they adjust the release of gut components to the state of plant defense. We addressed these questions by using Arabidopsis thaliana as host plant and larvae of the generalist herbivorous insect Spodoptera littoralis. We investigated the conversion of the plant-derived jasmonate precursor, cis-12-oxophytodienoic acid (cis-OPDA), to iso-OPDA by the larvae. This enzymatic reaction is mediated by a specific glutathione-S-transferase in the insect gut, but not in the plant. Any presence of iso-OPDA in plant tissue, thus, indicated that gut content had been regurgitated into the plant wound. Our study demonstrates that the plant is the only source for the substrate cis-OPDA by using aos (allene oxide synthase) mutants that are unable to synthesize OPDA. The fact that iso-OPDA accumulated over time on feeding-damaged leaves shows that the feeding larvae are constantly regurgitating on leaves. Although the larvae provided the signaling compounds that were recognized by the plant and elicited defense reactions, the larval regurgitation behavior did not depend on whether they fed on a defensive wild type plant or on a non defensive coi1-16 plant. This suggests that S. littoralis larvae do not adjust regurgitation to the state of plant defense.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alborn, H. T., Hansen, T. V., Jones, T. H., Bennett, D. C., Tumlinson, J. H., Schmelz, E. A., and Teal, P. E. A. 2007. Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc. Natl. Acad. Sci. USA 104:12976–12981.

    Article  PubMed  CAS  Google Scholar 

  • Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.

    Article  CAS  Google Scholar 

  • Birkett, M. A., Campbell, C. A. M., Chamberlain, K., Guerrieri, E., Hick, A. J., Martin, J. L., Matthes, M., Napier, J. A., Pettersson, J., Pickett, J. A., Poppy, G. M., Pow, E. M., Pye, B. J., Smart, L. E., Wadhams, G. H., Wadhams, L. J., and Woodcock, C. M. 2000. New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc. Natl. Acad. Sci. USA 97:9329–9334.

    Article  PubMed  CAS  Google Scholar 

  • Bos, J. I. B., Prince, D., Pitino, M., Maffei, M. E., Win, J., and Hogenhout, S. A. 2010. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (Green Peach Aphid). PloS Genetics 6:e1001216.

    Article  PubMed  Google Scholar 

  • Bruce, T. J. A., Martin, J. L., Pickett, J. A., Pye, B. J., Smart, L. E., and Wadhams, L. J. 2003. Cis-jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Manage. Sci 59:1031–1036.

    Article  CAS  Google Scholar 

  • Chini, A., Boter, M., and Solano, R. 2009. Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module. FEBS J 276:4682–4692.

    Article  PubMed  CAS  Google Scholar 

  • Consales, F., Schweizer, F., Erb, M., Gouhier-Darimont, C., Bodenhausen, N., Bruessow, F., Sobhy, I., and Reymond, P. 2011. Insect oral secretions suppress wound-induced responses in Arabidopsis. J. Exp. Bot. 63:727–737.

    Article  PubMed  Google Scholar 

  • Dabrowska, P. and Boland, W. 2007. iso-OPDA: An early precursor of cis-jasmone in plants? ChemBioChem 8:2281–2285.

    Article  PubMed  CAS  Google Scholar 

  • Dabrowska, P., Freitak, D., Vogel, H., Heckel, D. G., and Boland, W. 2009. The phytohormone precursor OPDA is isomerized in the insect gut by a single, specific glutathione transferase. Proc. Natl. Acad. Sci. USA 106:16304–16309.

    Article  PubMed  CAS  Google Scholar 

  • De Moares, C. M., Lewis, W. J., Pare, P. W., Alborn, H. T., and Tumlinson, J. H. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.

    Article  Google Scholar 

  • Eichenseer, H., Mathews, M. C., Bi, J. L., Murphy, J. B., and Felton, G. W. 1999. Salivary glucose oxidase: Multifunctional roles for Helicoverpa zea? Arch. Insect Biochem. Physiol. 42:99–109.

    Article  PubMed  CAS  Google Scholar 

  • Ellis, C. and Turner, J. G. 2002. A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215:549–556.

    Article  PubMed  CAS  Google Scholar 

  • Felton, G. W. and Tumlinson, J. H. 2008. Plant-insect dialogs: complex interactions at the plant-insect interphase. Curr. Opinion Plant Biol. 11:457–463.

    Article  CAS  Google Scholar 

  • Halitschke, R., Schittko, U., Pohnert, G., Boland, W., and Baldwin, I. T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol. 125:711–717.

    CAS  Google Scholar 

  • Ichikawa, T., Namikawa, M., Yamada, K., Sakai, K., and Kondo, K. 1983. Novel cyclopentenonyl fatty-acids from mosses. Dicranum scoporium and Dicranum japonicum. Tetrahedron Lett. 24:3337–3340.

    Article  CAS  Google Scholar 

  • Kessler, A. and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.

    Article  PubMed  CAS  Google Scholar 

  • Kramell, R., Miersch, O., Atzorn, R., Parthier, B., and Wasternack, C. 2000. Octadecanoid-derived alteration of gene expression and the "oxylipin signature" in stressed barley leaves. Implications for different signaling pathways. Plant Physiol. 123:177–187.

    Article  PubMed  CAS  Google Scholar 

  • Landolt, P. J., Tumlinson, J. H., and Alborn, H. T. 1999. Attraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants. Environ. Entomol. 28:973–978.

    Google Scholar 

  • Leitner, M., Boland, W., and Mithöfer, A. 2005. Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol. 167:597–606.

    Article  PubMed  CAS  Google Scholar 

  • Maffei, M. E., Mithöfer, A., and Boland, W. 2007. Insects feeding on plants: Rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:2946–2959.

    Article  PubMed  CAS  Google Scholar 

  • Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. Beta-glucosidase - an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. USA 92:2036–2040.

    Article  PubMed  CAS  Google Scholar 

  • Mithöfer, A. and Boland, W. 2008. Recognition of herbivory-associated molecular patterns. Plant Physiol. 146:825–831.

    Article  PubMed  Google Scholar 

  • Mithöfer, A., Boland, W., and Maffei, M. E. 2009. Chemical ecology of plant-insect interactions, pp. 261–291, in J. Parker (ed.), Plant Disease Resistance. Wiley-Blackwell, Chichester.

    Google Scholar 

  • Mithöfer, A., Wanner, G., and Boland, W. 2005. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137:1160–1168.

    Google Scholar 

  • Musser, R. O., Cipollini, D. F., Hum-Musser, S. M., Williams, S. A., Brown, J. K., and Felton, G. W. 2005. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch. Insect Biochem. Physiol 58:128–137.

    Article  PubMed  CAS  Google Scholar 

  • Musser, R. O., Hum-Musser, S. M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J. B., and Felton, G. W. 2002. Caterpillar saliva beats plant defences. Nature 416:599–600.

    Article  PubMed  CAS  Google Scholar 

  • Park, J. H., Halitschke, R., Kim, H. B., Baldwin, I. T., Feldmann, K. A., and Feyereisen, R. A. 2002. Knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12.

    Article  PubMed  Google Scholar 

  • Peiffer, M. and Felton, G. W. 2009. Do caterpillars secrete “Oral secretions”? J. Chem. Ecol. 35:326–335.

    Article  PubMed  CAS  Google Scholar 

  • Rhainds, M., Eveleigh, E., Francis, B., and Silk, P. 2011. Factors affecting oral regurgitation by larval spruce budworm. Entomol. Exp. Appl. 140:254–261.

    Article  Google Scholar 

  • Schäfer, M., Fischer, C., Meldau, S., Seebald, E., Oelmüller, R., and Baldwin, I. T. 2011. Lipase activity in insect oral secretions mediates defense responses in Arabidopsis thaliana. Plant Physiol. 156:1520–1534.

    Article  PubMed  Google Scholar 

  • Schmelz, E. A., Alborn, H. T., and Tumlinson, J. H. 2001. The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays. Planta 214:171–179.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Carroll, M. J., Leclere, S., Phipps, S. M., Meredith, J., Chourey, P. S., Alborn, H. T., and Teal, P. E. A. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. USA 103:8894–8899.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Engelberth, J., Alborn, H. T., Tumlinson III, J. H., and Teal, P. E. A. 2009. Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc. Natl. Acad. Sci. USA 106:653–657.

    Article  PubMed  CAS  Google Scholar 

  • Schulze, B., Dabrowska, P., and Boland, W. 2007. Rapid enzymatic isomerization of 12-oxophytodienoic acid in the gut of lepidopteran larvae. ChemBioChem 8:208–216.

    Article  PubMed  CAS  Google Scholar 

  • Spiteller, D., Pohnert, G., and Boland, W. 2001. Absolute configuration of volicitin, an elicitor of plant volatile biosynthesis from lepidopteran larvae. Tetrahedron Lett. 42:1483–1485.

    Article  CAS  Google Scholar 

  • Stanley, D., Miller, J., and Tunaz, H. 2009. Eicosanoid actions in insect immunity. J. Innate Immun. 1:282–290.

    Article  PubMed  CAS  Google Scholar 

  • Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998. Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81.

    Article  Google Scholar 

  • Truitt, C. L. and Pare, P. W. 2004. In situ translocation of volicitin by beet armyworm larvae to maize and systemic immobility of the herbivore elicitor in planta. Planta 218:999–1007.

    Article  PubMed  CAS  Google Scholar 

  • Vollenweider, S., Weber, H., Stolz, S., Chetelat, A., and Farmer, E. E. 2000. Fatty acid ketodienes and fatty acid ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves. Plant J. 24:467–476.

    Article  PubMed  CAS  Google Scholar 

  • Wasternack, C. 2007. Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100:681–697.

    Article  PubMed  CAS  Google Scholar 

  • Xie, D.-X., Feys, B. F., James, S., Nieto-Rostro, M., and Turner, J. G. 1998. COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. G. Turner and G. Bonaventure for providing seeds of Arabidopsis coi1-16 and aos plants, respectively, A. Lehr for technical assistance, A. Berg for rearing caterpillars, the greenhouse team for growing plants, K. Ploss for language editing, J. Gershenzon and W. Boland for continuous support, and the Max Planck Society for funding.

Author information

Authors and Affiliations

  1. Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany

    Jyothilakshmi Vadassery & Axel Mithöfer

  2. Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany

    Michael Reichelt

Authors
  1. Jyothilakshmi Vadassery
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Reichelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Axel Mithöfer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Axel Mithöfer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vadassery, J., Reichelt, M. & Mithöfer, A. Direct Proof of Ingested Food Regurgitation by Spodoptera littoralis Caterpillars during Feeding on Arabidopsis . J Chem Ecol 38, 865–872 (2012). https://doi.org/10.1007/s10886-012-0143-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0143-5

Keywords

Search

Navigation