Journal of Chemical Ecology

, Volume 35, Issue 2, pp 163–175 | Cite as

Herbivore-Induced Volatiles in the Perennial Shrub, Vaccinium corymbosum, and Their Role in Inter-branch Signaling

  • Cesar R. Rodriguez-Saona
  • Luis E. Rodriguez-Saona
  • Christopher J. Frost
Article

Abstract

Herbivore feeding activates plant defenses at the site of damage as well as systemically. Systemic defenses can be induced internally by signals transported via phloem or xylem, or externally transmitted by volatiles emitted from the damaged tissues. We investigated the role of herbivore-induced plant volatiles (HIPVs) in activating a defense response between branches in blueberry plants. Blueberries are perennial shrubs that grow by initiating adventitious shoots from a basal crown, which produce new lateral branches. This type of growth constrains vascular connections between shoots and branches within plants. While we found that leaves within a branch were highly connected, vascular connectivity was limited between branches within shoots and absent between branches from different shoots. Larval feeding by gypsy moth, exogenous methyl jasmonate, and mechanical damage differentially induced volatile emissions in blueberry plants, and there was a positive correlation between amount of insect damage and volatile emission rates. Herbivore damage did not affect systemic defense induction when we isolated systemic branches from external exposure to HIPVs. Thus, internal signals were not capable of triggering systemic defenses among branches. However, exposure of branches to HIPVs from an adjacent branch decreased larval consumption by 70% compared to those exposed to volatiles from undamaged branches. This reduction in leaf consumption did not result in decreased volatile emissions, indicating that leaves became more responsive to herbivory (or “primed”) after being exposed to HIPVs. Chemical profiles of leaves damaged by gypsy moth caterpillars, exposed to HIPVs, or non-damaged controls revealed that HIPV-exposed leaves had greater chemical similarities to damaged leaves than to control leaves. Insect-damaged leaves and young HIPV-exposed leaves had higher amounts of endogenous cis-jasmonic acid compared to undamaged and non-exposed leaves, respectively. Our results show that exposure to HIPVs triggered systemic induction of direct defenses against gypsy moth and primed volatile emissions, which can be an indirect defense. Blueberry plants appear to rely on HIPVs as external signals for inter-branch communication.

Keywords

Herbivore-induced plant volatiles External signaling Vaccinium corymbosum Lymantria dispar Priming 

Notes

Acknowledgments

We are grateful to Drs. Paul Paré and Nicholi Vorsa for their comments on the manuscript. We thank Robert Holdcraft for his help with the tables and figures, Vera Kyryczenko-Roth for technical assistance, Dr. Philip Taylor (USDA-ARS, Beneficial Insects Introduction Research Unit, Newark, DE) for the supply of gypsy moth egg masses and caterpillars, and Dr. Thomas Hartman (Rutgers University, Mass Spectrometry Support Facility, New Brunswick, NJ) for identification of volatiles. Funding for this study was provided by USDA-CREES Special Grant (Project No. 2006-34155-17118) and hatch funds (Project No. NJ08192) to C.R.-S., and by the USDA-NRI (Project No. 2007-35302-18087) to C.J.F.

References

  1. Adams, R. P. 2001. Identification of Essential Oil Components by Gas Chromatography/Quadrupole Mass Spectroscopy. Allured, Illinois.Google Scholar
  2. Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201–1202.PubMedCrossRefGoogle Scholar
  3. Agrawal, A. A. 1999. Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80:1713–1723.CrossRefGoogle Scholar
  4. Arimura, G. -I., Ozawa, R., Nishioka, T., Boland, W., Koch, T., Kühnemann F., and Takabayashi J. 2002. Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J. 29:87–98.PubMedCrossRefGoogle Scholar
  5. Baldwin, I. T., and Schultz, J. C. 1983. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221:277–279.PubMedCrossRefGoogle Scholar
  6. Bell, R. A., Owens, C. D., Shapiro, M., and Tardif, J. R. 1981. Mass rearing and virus production, pp. 599–655, in C. C. Doane, and M. L. McManus (eds.). The Gypsy Moth: Research Toward Integrated Pest Management, Technical Bulletin 1584. USDA Forest Service, Washington DC.Google Scholar
  7. Boland, W., Hopke, J., Donath, J., Nueske, J., and Bublltz, F. 1995. Jasmonic acid and coronatin induce odor production in plants. Angew. Chem. Int. Ed. Engl. 34:1600–1602.CrossRefGoogle Scholar
  8. Davis, J. M., Gordon, M. P., and Smit, B. A. 1991. Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. Proc. Natl. Acad. Sci. U. S. A. 88:2393–2396.PubMedCrossRefGoogle Scholar
  9. De Maesschalck, R., Candolfi, A., Masart, D. L., and Heuerding, S. 1999. Decision criteria for soft independent modeling of class analogy applied to near infrared data. Chemom. Intell. Lab. Syst. 47:65–77.CrossRefGoogle Scholar
  10. Dicke, M., and Van Loon, J. J. A. 2000. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97:237–249.CrossRefGoogle Scholar
  11. Dicke, M., Agrawal, A. A., and Bruin, J. 2003. Plants talk, but are they deaf? Trends Plant Sci. 8:403–405.PubMedCrossRefGoogle Scholar
  12. Draper, A., Galletta, G., Jelenkovic, G., and Vorsa, N. 1987. ‘Duke’ highbush blueberry. HortScience 22:320.Google Scholar
  13. Dunn, W. J. Jr., and Wold, S. 1995. SIMCA pattern recognition and classification, pp. 179–193, in H. van de Waterbeemd (ed.). Chemometric Methods in Molecular DesignVCH, New York.Google Scholar
  14. Engelberth, J., Alborn, H. T., Schmelz, E. A., and Tumlinson, J. H. 2004. Airborne signals prime plants against herbivore attack. Proc. Natl. Acad. Sci. U. S. A. 101:1781–1785.PubMedCrossRefGoogle Scholar
  15. Farag, M. A., and Paré, P. W. 2002. C6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554.PubMedCrossRefGoogle Scholar
  16. Farmer, E. E. 2001. Surface-to-air signals. Nature 411:854–856.PubMedCrossRefGoogle Scholar
  17. Frost, C. J., Appel, H. M., Carlson, J. E., De Moraes, C. M., Mescher, M. C., and Schultz, J. C. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10:490–498.PubMedCrossRefGoogle Scholar
  18. Frost, C. J., Mescher, M. C., Carlson, J. E., and Demoraes, C. M. 2008a. Why do distance limitations exist on plant-to-plant signaling? Plant Signal. Behav. 3:466–468.PubMedGoogle Scholar
  19. Frost, C. J., Mescher, M. C., Carlson, J. E., and De Moraes, C. M. 2008b. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 146:818–824.PubMedCrossRefGoogle Scholar
  20. Giusti, M. M., Rodriguez-Saona, L. E., Griffin, D., and Wrolstad, R. E. 1999. Electrospray and tandem mass spectroscopy as tools for anthocyanin characterization. J. Agric. Food Chem. 47:4657–4664.PubMedCrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Havill, N. P., and Raffa, K. F. 1999. Effects of eliciting treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth development and feeding behavior. Oecologia 120:295–303.CrossRefGoogle Scholar
  23. He, J., Rodriguez-Saona, L. E., and Giusti, M. M. 2007. Mid-infrared spectroscopy for juice authentications—rapid differentiation of commercial juices. J. Agric. Food Chem. 55:4443–4452.PubMedCrossRefGoogle Scholar
  24. Heil, M., and Silva Bueno, J. C. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U. S. A. 104:5467–5472.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. Jennings, W., and Shibamoto, T. 1980. Qualitative Analysis of Flavour and Fragrance Volatiles by Glass Capillary Gas Chromatography. Academic, New York.Google Scholar
  27. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. The University of Chicago Press, Chicago.Google Scholar
  28. Karban, R., Maron, J., Felton, G. W., Ervin, G., and Eichenseer H. 2003. Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100:325–332.CrossRefGoogle Scholar
  29. Karban, R., Shiojiri, K., Huntzinger, M., and Mccall, A. C. 2006. Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930.PubMedCrossRefGoogle Scholar
  30. Kost, C., and Heil, M. 2006. Herbivore-induced plant volatiles induce an indirect defense in neighbouring plants. J. Ecol. 94:619–628.CrossRefGoogle Scholar
  31. Kvalheim, O. M., and Karstang, T. V. 1992. SIMCA—classification by means of disjoint cross validated principal components models, pp. 209–248, in R. G. Brereton (ed.). Multivariate Pattern Recognition in Chemometrics: Illustrated by Case StudiesElsevier, New York.Google Scholar
  32. Liebhold, A. M., Halverson, J. A., and Elmes, G. A. 1992. Gypsy-moth invasion in North-America: a quantitative-analysis. J. Biogeogr. 19:513–520.CrossRefGoogle Scholar
  33. Markovic, I., Norris, D. M., Phillips, J. K., and Webster, F. X. 1996. Volatiles involved in the nonhost rejection of Fraxinus pennsylvanica by Lymantria dispar larvae. J. Agric. Food Chem. 44:929–935.CrossRefGoogle Scholar
  34. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1994. Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor. J. Chem. Ecol. 20:2229–2247.CrossRefGoogle Scholar
  35. Mattiacci, L., Rocca, B., Scascighini, N., D’Alessandro, M., Hern, A., and Dorn, S. 2001. Systemically induced plant volatiles emitted at the time of “danger”. J. Chem. Ecol. 27:2233–2251.PubMedCrossRefGoogle Scholar
  36. Orians, C. M. 2005. Herbivores, vascular pathways and systemic induction: facts and artifacts. J. Chem. Ecol. 31:2231–2242.PubMedCrossRefGoogle Scholar
  37. Orians, C. M., Pomerleau, J., and Ricco, R. 2000. Vascular architecture generates fine scale variation in the systemic induction of proteinase inhibitors in tomato. J. Chem. Ecol. 26:471–485.CrossRefGoogle Scholar
  38. Paré, P. W., and Tumlinson, J. H. 1998. Cotton volatiles synthesized and released distal to the site of insect damage. Phytochemistry 47:521–526.CrossRefGoogle Scholar
  39. Preston, C. A., Laue, G., and Baldwin, I. T. 2001. Methyl jasmonate is blowing in the wind, but can it act as a plant–plant airborne signals? Biochem. Syst. Ecol. 29:1007–1023.CrossRefGoogle Scholar
  40. Preston, C. A., Laue, G., and Baldwin, I. T. 2004. Plant–plant signaling: application of trans or cis-methyl jasmonate equivalent to sagebrush releases does not elicit direct defenses in native tobacco. J. Chem. Ecol. 30:2193–2214.PubMedCrossRefGoogle Scholar
  41. Rodriguez-Saona, C., Crafts-Brandner, S. J., Paré, P. W., and Henneberry, T. J. 2001. Exogenous methyl jasmonate induces volatile emissions in cotton plants. J. Chem. Ecol. 27:679–695.PubMedCrossRefGoogle Scholar
  42. Rodriguez-Saona, C., Poland, T. M., Miller, J. R., Stelinski, L. L., GGrant, G. G., De Groot, P., Buchan, L., and MacDonald, L. 2006. Behavioral and electrophysiological responses of the emerald ash borer, Agrilus planipennis, to induced volatiles of Manchurian ash, Fraxinus mandshurica. Chemoecology 16:75–86.CrossRefGoogle Scholar
  43. Ruther, J., and Kleier, S. 2005. Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-Hexen-1-ol. J. Chem. Ecol. 31:2217–2222.PubMedCrossRefGoogle Scholar
  44. Schittko, U., and Baldwin, I. T. 2003. Constraints to herbivore-induced systemic responses: bi-directional signaling along orthosticies in Nicotiana attenuata. J. Chem. Ecol. 29:745–752.CrossRefGoogle Scholar
  45. Schmelz, E. A., Engelberth, J., Alborn, H. T., O’Donnell, P., Sammons, M., Toshima, H., and Tumlinson, J. H. 2003. Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Nat. Acad. Sci. U. S. A. 100:10552–10557.CrossRefGoogle Scholar
  46. Schmelz, E. A., Engelberth, J., Tumlinson, J. H., Block, A., and Alborn, H. T. 2004. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J. 39:790–808.PubMedCrossRefGoogle Scholar
  47. Shiojiri, K., and Karban, R. 2006. Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers. Oecologia 149:214–220.PubMedCrossRefGoogle Scholar
  48. Staudt, M., and Lhoutellier, L. 2007. Volatile organic compound emission from holm oak infested by gypsy moth larvae: evidence for distinct responses in damaged and undamaged leaves. Tree Physiol. 27:1433–1440.PubMedGoogle Scholar
  49. Ton, J., D’Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B., and Turlings, T. C. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49:16–26.PubMedCrossRefGoogle Scholar
  50. Turlings, T. C. J., and Tumlinson, J. H. 1992. Systemic release of chemical signals by herbivore-injured corn. Proc. Natl. Acad. Sci. U. S. A. 89:8399–8402.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. Vet, L. E. M., and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141–172.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Cesar R. Rodriguez-Saona
    • 1
  • Luis E. Rodriguez-Saona
    • 2
  • Christopher J. Frost
    • 3
  1. 1.Department of Entomology, PE Marucci Blueberry and Cranberry CenterRutgers UniversityChatsworthUSA
  2. 2.Department of Food Science & TechnologyOhio State UniversityColumbusUSA
  3. 3.Department of EntomologyPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations