, Volume 148, Issue 2, pp 280–292 | Cite as

Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata

  • André Kessler
  • Rayko Halitschke
  • Celia Diezel
  • Ian T. BaldwinEmail author
Plant Animal Interactions


Plants release volatile organic compounds (VOCs) in response to wounding and herbivore attack, some of which trigger responses in neighboring unattacked plants in the laboratory under conditions that are not likely to occur in the real world. Whether plants ‘eavesdrop’ on the volatile emissions of their neighbors in nature is not known. The best documented field study of between-species signaling via above-ground VOCs involves increases in fitness parameters of native tobacco (Nicotiana attenuata) transplanted adjacent to clipped sagebrush (Artemesia tridentata tridentata). Clipped sagebrush releases many biologically active VOCs, including methyl jasmonate (MeJA), methacrolein and a series of terpenoid and green leaf VOCs, of which MeJA, while active under laboratory conditions, is not released in sufficient quantities to directly elicit induced resistance in the field. Here we demonstrate, with laboratory and field-based experiments, that priming (rather than direct elicitation) of native N. attenuata’s induced chemical defenses by a sagebrush-released VOC bouquet can account for earlier findings. With microarrays enriched in N. attenuata herbivore-regulated genes, we found transcriptional responses in tobacco growing adjacent to clipped sagebrush foliage, but failed to detect the direct elicitation of defensive chemicals or proteins. However, we observed an accelerated production of trypsin proteinase inhibitors when Manduca sexta caterpillars fed on plants previously exposed to clipped sagebrush. This readying of a defense response, termed priming, results in lower total herbivore damage to plants exposed to clipped sagebrush and in a higher mortality rate of young Manduca caterpillars. Our study demonstrates priming of plant defense responses as a mechanism of plant–plant signaling in nature, and provides an example for the analysis of between-plant signaling under ecologically realistic conditions. Although we describe priming as a potential mechanism for signaling between plants in nature, we critically discuss the ecological relevance of the particular interaction.


Plant communication Plant–insect interaction Proteinase inhibitors Volatile compounds 



This research was supported by the Max-Planck-Gesellschaft. We thank Michael Haevecker and Robert Schlögl from the Fritz-Haber-Institut of the Max-Planck-Gesellschaft for the generous use of their PTR-MS and patient instructions for its use and the Brigham Young University for the use of their awesome field station, the Lytle Preserve.

Supplementary material

442_2006_365_MOESM1_ESM.pdf (52 kb)
Supplementary material


  1. Agrawal AA (2000) Communication between plants: this time it’s real. Trends Ecol Evol 15:446PubMedCrossRefGoogle Scholar
  2. Almeras E, Stolz S, Vollenweider S, Reymond P, Mene-Saffrane L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:202–216CrossRefGoogle Scholar
  3. Arimura G, Ozawa R, Horiuchi J, Nishioka T, Takabayashi J (2001) Plant–plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochem System Ecol 29:1049–1061CrossRefGoogle Scholar
  4. Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabyashi J (2000a) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515CrossRefGoogle Scholar
  5. Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J (2000b) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277:305–310CrossRefGoogle Scholar
  6. Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci USA 95:8113–8118PubMedCrossRefGoogle Scholar
  7. Baldwin IT, Kessler A, Halitschke R (2002) Volatile signaling in plant–plant–herbivore interactions: what is real? Curr Opin Plant Biol 5:351–354PubMedCrossRefGoogle Scholar
  8. Bruin J, Sabelis MW, Dicke M (1995) Do plants tap SOS signals from their infested neighbors? Trends Ecol Evol 10:167–170CrossRefGoogle Scholar
  9. Charron CS, Cantliffe DJ, Wheeler RM, Manukian A, Heath RR (1996) Photosynthetic photon flux, photoperiod, and temperature effects on emissions of (Z)-3-hexenal, (Z)3-hexenol, and (Z)-3-hexenyl acetate from lettuce. J Am Soc Hort Sci 121:488–494Google Scholar
  10. Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv. phaseolicola. Plant Physiol 101:13–24PubMedGoogle Scholar
  11. De Moraes CM, Schultz JC, Mescher MC, Tumlinsoni JH (2004) Induced plant signaling and its implications for environmental sensing. J Tox Environ Health 67:819–834CrossRefGoogle Scholar
  12. Dicke M, Bruin J (2001) Chemical information transfer between plants: back to the future. Biochem System Ecol 29:981–994CrossRefGoogle Scholar
  13. Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249CrossRefGoogle Scholar
  14. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785PubMedCrossRefGoogle Scholar
  15. Farmer EE, Ryan CA (1990) Interplant communication—airborne methyl jasmonate induces synthesis of proteinase-inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716PubMedCrossRefGoogle Scholar
  16. Glawe GA, Zavala JA, Kessler A, Van Dam NM, Baldwin IT (2003) Ecological costs and benefits correlated with trypsin protease inhibitor production in Nicotiana attenuata. Ecology 84:79–90CrossRefGoogle Scholar
  17. Halitschke R, Gase K, Hui DQ, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 131:1894–1902PubMedCrossRefGoogle Scholar
  18. Halitschke R, Kessler A, Kahl J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124:408–417CrossRefGoogle Scholar
  19. Harley P, Deem G, Flint S, Caldwell M (1996) Effects of growth under elevated UV-B on photosynthesis and isoprene emission in Quercus gambelii and Mucuna pruriens. Global Change Biol 2:149–154CrossRefGoogle Scholar
  20. Heiden AC et al. (1999) Emission of volatile organic compounds from ozone-exposed plants. Ecol Applicat 9:1160–1167CrossRefGoogle Scholar
  21. Karban R (2001) Communication between sagebrush and wild tobacco in the field. Biochem System Ecol 29:995–1005CrossRefGoogle Scholar
  22. Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71CrossRefGoogle Scholar
  23. Karban R, Baxter KJ (2001) Induced resistance in wild tobacco with clipped sagebrush neighbors: the role of herbivore behavior. J Insect Behav 14:147–156CrossRefGoogle Scholar
  24. Karban R, Maron J (2002) The fitness consequences of interspecific eavesdropping between plants. Ecology 83:1209–1213CrossRefGoogle Scholar
  25. Karban R, Maron J, Felton GW, Ervin G, Eichenseer H (2003) Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100:325–332CrossRefGoogle Scholar
  26. Keinanen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening fo jasmonate-induced increases in tobacco alkaloids, phenolics a diterpene glycosides in Nicotiana attenuata. J Agri Food Chem 49:3553–3558CrossRefGoogle Scholar
  27. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emission in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  28. Kessler A, Baldwin IT (2002) Manduca quinquemaculata’s optimization of intra-plant oviposition to predation, food quality and thermal constraints. Ecology 83:2346–2354Google Scholar
  29. Kessler A, Baldwin IT (2004) Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J 38:639–649PubMedCrossRefGoogle Scholar
  30. Krügel T, Lim M, Gase K, Halitschke R, Baldwin IT (2002) Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12:177–183CrossRefGoogle Scholar
  31. Lerdau M, Gray D (2003) Ecology and evolution of light-dependent and light-independent phytogenic volatile organic carbon. New Phytol 157:199–211CrossRefGoogle Scholar
  32. Lerdau M, Slobodkin K (2002) Trace gas emissions and species-dependent ecosystem services. Trends Ecol Evol 17:309–312CrossRefGoogle Scholar
  33. Personius TL, Wambolt CL, Stephens JR, Kelsey RG (1987) Crude terpenoid influence on mule deer preference for sagebrush. J Range Managem 40:84–88CrossRefGoogle Scholar
  34. Preston CA, Laue G, Baldwin IT (2001) Methyl jasmonate is blowing in the wind, but can it act as a plant–plant airborne signal? Biochem System Ecol 29:1007–1023CrossRefGoogle Scholar
  35. Preston CA, Laue G, Baldwin IT (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 30:2193–2214PubMedCrossRefGoogle Scholar
  36. Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295–306PubMedCrossRefGoogle Scholar
  37. Shonle I, Bergelson J (1995) Interplant communication revisited. Ecology 76:2660–2663CrossRefGoogle Scholar
  38. Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem System Ecol 29:1025–1047CrossRefGoogle Scholar
  39. van Dam NM, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains the systemic proteinase inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568PubMedCrossRefGoogle Scholar
  40. Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38:650–663PubMedCrossRefGoogle Scholar
  41. Weber H, Chetelat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888PubMedCrossRefGoogle Scholar
  42. Zavala JA, Patankar AG, Gase K, Baldwin IT (2004a) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Natl Acad Sci USA 101:1607–1612CrossRefGoogle Scholar
  43. Zavala JA, Patankar AG, Gase K, Hui DQ, Baldwin IT (2004b) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190CrossRefGoogle Scholar
  44. Zepp RG, Callaghan TV, Erickson DJ (1998) Effects of enhanced solar ultraviolet radiation on biogeochemical cycles. J Photochem Photobiol B 46:69–82CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • André Kessler
    • 1
    • 2
  • Rayko Halitschke
    • 1
    • 2
  • Celia Diezel
    • 2
  • Ian T. Baldwin
    • 2
    Email author
  1. 1.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  2. 2.Department of Molecular EcologyMax-Planck-Institute for Chemical EcologyJenaGermany

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