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Chemical complexity of volatiles from plants induced by multiple attack

Abstract

The attack of a plant by herbivorous arthropods can result in considerable changes in the plant's chemical phenotype. The emission of so-called herbivore-induced plant volatiles (HIPV) results in the attraction of carnivorous enemies of the herbivores that induced these changes. HIPV induction has predominantly been investigated for interactions between one plant and one attacker. However, in nature plants are exposed to a variety of attackers, either simultaneously or sequentially, in shoots and roots, causing much more complex interactions than have usually been investigated in the context of HIPV. To develop an integrated view of how plants respond to their environment, we need to know more about the ways in which multiple attackers can enhance, attenuate, or otherwise alter HIPV responses. A multidisciplinary approach will allow us to investigate the underlying mechanisms of HIPV emission in terms of phytohormones, transcriptional responses and biosynthesis of metabolites in an effort to understand these complex plant-arthropod interactions.

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Figure 1: In response to feeding by caterpillars of the beet armyworm (Spodoptera exigua), a leaf feeder, a maize plant emits a range of HIPV aboveground, among which are fatty acid–derived green-leaf volatiles such as (Z)-3-hexen-1-ol, the aromatic indole and terpenoids such as (E)-4,8-dimethyl-1,3,7-nonatriene, S(–)-linalool and (E)-β-bergamotene99.
Figure 2: Effect of double herbivore infestation of a plant on attraction of predators.
Figure 3: Herbivore-induced plant volatiles in a double-attacker above- and belowground context.

References

  1. Kessler, A. & Baldwin, I.T. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53, 299–328 (2002).

    CAS  PubMed  Article  Google Scholar 

  2. Pieterse, C.M.J. & Dicke, M. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci. 12, 564–569 (2007).

    CAS  PubMed  Article  Google Scholar 

  3. Schaller, A. (ed.) Induced Plant Resistance to Herbivory (Springer, Berlin, 2008).

    Book  Google Scholar 

  4. Roda, A.L. & Baldwin, I.T. Molecular technology reveals how the induced direct defenses of plants work. Basic Appl. Ecol. 4, 15–26 (2003).

    CAS  Article  Google Scholar 

  5. Vet, L.E.M. & Dicke, M. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141–172 (1992).

    Article  Google Scholar 

  6. Heil, M. Indirect defence via tritrophic interactions. New Phytol. 178, 41–61 (2008).

    CAS  PubMed  Article  Google Scholar 

  7. Agrawal, A.A. Phenotypic plasticity in the interactions and evolution of species. Science 294, 321–326 (2001).

    CAS  PubMed  Article  Google Scholar 

  8. Voelckel, C. & Baldwin, I.T. 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, 650–663 (2004).

    CAS  PubMed  Article  Google Scholar 

  9. Broekgaarden, C. et al. Genotypic variation in genome-wide transcription profiles induced by insect feeding: Brassica oleracea-Pieris rapae interactions. BMC Genomics 8, 239 (2007).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  10. Reymond, P. et al. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132–3147 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Jansen, J.J. et al. Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 5, 150–161 (2009).

    CAS  Article  Google Scholar 

  12. Kessler, A., Halitschke, R. & Baldwin, I.T. Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305, 665–668 (2004).

    CAS  PubMed  Article  Google Scholar 

  13. Kollner, T.G. et al. A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20, 482–494 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  14. Pozo, M.J., Van der Ent, S., Van Loon, L.C. & Pieterse, C.M.J. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol. 180, 511–523 (2008).

    CAS  PubMed  Article  Google Scholar 

  15. Kaplan, I. & Denno, R.F. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett. 10, 977–994 (2007).

    PubMed  Article  Google Scholar 

  16. Zarate, S.I., Kempema, L.A. & Walling, L.L. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143, 866–875 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. Felton, G.W. & Tumlinson, J.H. Plant-insect dialogs: complex interactions at the plant-insect interface. Curr. Opin. Plant Biol. 11, 457–463 (2008).

    CAS  PubMed  Article  Google Scholar 

  18. Maffei, M.E., Mithofer, A. & Boland, W. Before gene expression: early events in plant-insect interaction. Trends Plant Sci. 12, 310–316 (2007).

    CAS  PubMed  Article  Google Scholar 

  19. De Vos, M. et al. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18, 923–937 (2005).

    CAS  PubMed  Article  Google Scholar 

  20. Voelckel, C. & Baldwin, I.T. Generalist and specialist lepidopteran larvae elicit different transcriptional responses in Nicotiana attenuata, which correlate with larval FAC profiles. Ecol. Lett. 7, 770–775 (2004).

    Article  Google Scholar 

  21. Dicke, M. et al. 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 (1990).

    CAS  PubMed  Article  Google Scholar 

  22. Schnee, C. et al. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. USA. 103, 1129–1134 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Shiojiri, K. et al. Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc. Natl. Acad. Sci. USA 103, 16672–16676 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Dicke, M. Evolution of induced indirect defence of plants. in The Ecology and Evolution of Inducible Defenses (eds. Tollrian, R. & Harvell, C.D.) 62–88 (Princeton Univ. Press, Princeton, New Jersey, USA, 1999).

    Google Scholar 

  25. Turlings, T.C.J. et al. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. USA 92, 4169–4174 (1995).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. & Hilker, M. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19, 677–689 (2008).

    Article  Google Scholar 

  27. Van den Boom, C.E.M., Van Beek, T.A., Posthumus, M.A., De Groot, A. & Dicke, M. Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J. Chem. Ecol. 30, 69–89 (2004).

    CAS  PubMed  Article  Google Scholar 

  28. Shimoda, T. & Takabayashi, J. Response of Oligota kashmirica benefica, a specialist insect predator of spider mites, to volatiles from prey-infested leaves under both laboratory and field conditions. Entomol. Exp. Appl. 101, 41–47 (2001).

    Article  Google Scholar 

  29. Van Poecke, R.M.P., Posthumus, M.A. & Dicke, M. Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J. Chem. Ecol. 27, 1911–1928 (2001).

    CAS  PubMed  Article  Google Scholar 

  30. Arimura, G. et al. Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol. 146, 965–973 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. Arimura, G. et al. Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta 227, 453–464 (2008).

    CAS  PubMed  Article  Google Scholar 

  32. Kappers, I.F. et al. Genetic engineering of terpenoid metabolism attracts, bodyguards to Arabidopsis. Science 309, 2070–2072 (2005).

    CAS  PubMed  Article  Google Scholar 

  33. van Tol, R.W.H.M. et al. Plants protect their roots by alerting the enemies of grubs. Ecol. Lett. 4, 292–294 (2001).

    Article  Google Scholar 

  34. Rasmann, S. et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737 (2005).

    CAS  PubMed  Article  Google Scholar 

  35. Rasmann, S. & Turlings, T.C.J. First insights into specificity of belowground tritrophic interactions. Oikos 117, 362–369 (2008).

    Article  Google Scholar 

  36. Turlings, T.C.J., Lengwiler, U.B., Bernasconi, M.L. & Wechsler, D. Timing of induced volatile emissions in maize seedlings. Planta 207, 146–152 (1998).

    CAS  Article  Google Scholar 

  37. Turlings, T.C.J. & Tumlinson, J.H. Systemic release of chemical signals by herbivore-injured corn. Proc. Natl. Acad. Sci. USA 89, 8399–8402 (1992).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. Jones, C.G., Hopper, R.F., Coleman, J.S. & Krischik, V.A. Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93, 452–456 (1993).

    PubMed  Article  Google Scholar 

  39. Dicke, M., van Baarlen, P., Wessels, R. & Dijkman, H. Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J. Chem. Ecol. 19, 581–599 (1993).

    CAS  PubMed  Article  Google Scholar 

  40. Gouinguene, S.P. & Turlings, T.C.J. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 129, 1296–1307 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Gols, R. et al. Reduced foraging efficiency of a parasitoid under habitat complexity: implications for population stability and species coexistence. J. Anim. Ecol. 74, 1059–1068 (2005).

    Article  Google Scholar 

  42. Pinto, D.M., Himanen, S.J., Nissinen, A., Nerg, A.M. & Holopainen, J.K. Host location behavior of Cotesia plutellae Kurdjumov (Hymenoptera: Braconidae) in ambient and moderately elevated ozone in field conditions. Environ. Pollut. 156, 227–231 (2008).

    CAS  PubMed  Article  Google Scholar 

  43. Pinto, D.M. et al. Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? J. Chem. Ecol. 33, 683–694 (2007).

    CAS  PubMed  Article  Google Scholar 

  44. Hilker, M., Kobs, C., Varma, M. & Schrank, K. Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J. Exp. Biol. 205, 455–461 (2002).

    PubMed  Article  Google Scholar 

  45. Dicke, M., Gols, R., Ludeking, D. & Posthumus, M.A. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol. 25, 1907–1922 (1999).

    CAS  Article  Google Scholar 

  46. Ozawa, R., Shiojiri, K., Sabelis, M.W. & Takabayashi, J. Maize plants sprayed with either jasmonic acid or its precursor, methyl linolenate, attract armyworm parasitoids, but the composition of attractants differs. Entomol. Exp. Appl. 129, 189–199 (2008).

    CAS  Article  Google Scholar 

  47. Ozawa, R., Arimura, G., Takabayashi, J., Shimoda, T. & Nishioka, T. Involvement of jasmonate- and salicylate-related signaling pathway for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol. 41, 391–398 (2000).

    CAS  PubMed  Article  Google Scholar 

  48. Van Poecke, R.M.P. & Dicke, M. Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J. Exp. Bot. 53, 1793–1799 (2002).

    CAS  PubMed  Article  Google Scholar 

  49. Koornneef, A. et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147, 1358–1368 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Horiuchi, J. et al. Exogenous ACC enhances volatiles production mediated by jasmonic acid in lima bean leaves. FEBS Lett. 509, 332–336 (2001).

    CAS  PubMed  Article  Google Scholar 

  51. Ruther, J. & Kleier, S. 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 (2005).

    CAS  PubMed  Article  Google Scholar 

  52. Kahl, J. et al. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210, 336–342 (2000).

    CAS  PubMed  Article  Google Scholar 

  53. von Dahl, C.C. et al. Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J. 51, 293–307 (2007).

    CAS  PubMed  Article  Google Scholar 

  54. Musser, R.O. et al. Herbivory: caterpillar saliva beats plant defences. Nature 416, 599–600 (2002).

    CAS  PubMed  Article  Google Scholar 

  55. Shiojiri, K., Takabayashi, J., Yano, S. & Takafuji, A. Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecol. Lett. 5, 186–192 (2002).

    Article  Google Scholar 

  56. de Boer, J.G., Hordijk, C.A., Posthumus, M.A. & Dicke, M. Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J. Chem. Ecol. 34, 281–290 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. Rodriguez-Saona, C., Crafts-Brandner, S.J. & Canas, L.A. Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J. Chem. Ecol. 29, 2539–2550 (2003).

    CAS  PubMed  Article  Google Scholar 

  58. Rodriguez-Saona, C., Chalmers, J.A., Raj, S. & Thaler, J.S. Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143, 566–577 (2005).

    PubMed  Article  Google Scholar 

  59. Walling, L.L. The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195–216 (2000).

    CAS  PubMed  Article  Google Scholar 

  60. Moayeri, H.R.S., Ashouri, A., Poll, L. & Enkegaard, A. Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory. J. Appl. Entomol. 131, 326–332 (2007).

    CAS  Article  Google Scholar 

  61. Broekgaarden, C. et al. Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ. 31, 1592–1605 (2008).

    CAS  PubMed  Article  Google Scholar 

  62. Poelman, E.H., Broekgaarden, C., Van Loon, J.J.A. & Dicke, M. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol. Ecol. 17, 3352–3365 (2008).

    CAS  PubMed  Article  Google Scholar 

  63. De Vos, M. et al. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142, 352–363 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. Gols, R., Roosjen, M., Dijkman, H. & Dicke, M. Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. J. Chem. Ecol. 29, 2651–2666 (2003).

    CAS  PubMed  Article  Google Scholar 

  65. Shiojiri, K., Takabayashi, J., Yano, S. & Takafuji, A. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43, 23–29 (2001).

    Article  Google Scholar 

  66. Wardle, D.A. Communities and Ecosystems: Linking the Aboveground and Belowground Components (Princeton Univ. Press, Princeton, New Jersey, USA, 2002).

    Google Scholar 

  67. Bezemer, T.M. & van Dam, N.M. Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol. Evol. 20, 617–624 (2005).

    PubMed  Article  Google Scholar 

  68. Soler, R. et al. Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116, 367–376 (2007).

    CAS  Article  Google Scholar 

  69. Rasmann, S. & Turlings, T.C.J. Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol. Lett. 10, 926–936 (2007).

    PubMed  Article  Google Scholar 

  70. Soler, R., Bezemer, T.M., Van der Putten, W.H., Vet, L.E.M. & Harvey, J.A. Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol. 74, 1121–1130 (2005).

    Article  Google Scholar 

  71. Soler, R., Harvey, J.A. & Bezemer, T.M. Foraging efficiency of a parasitoid of a leaf herbivore is influenced by root herbivory on neighbouring plants. Funct. Ecol. 21, 969–974 (2007).

    Article  Google Scholar 

  72. Gange, A.C., Bower, E. & Brown, V.K. Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120, 123–131 (1999).

    PubMed  Article  Google Scholar 

  73. Goverde, M., van der Heijden, M.G.A., Wiemken, A., Sanders, I.R. & Erhardt, A. Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia 125, 362–369 (2000).

    CAS  PubMed  Article  Google Scholar 

  74. Gange, A.C., Brown, V.K. & Aplin, D.M. Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol. Lett. 6, 1051–1055 (2003).

    Article  Google Scholar 

  75. Gange, A.C. & Smith, A.K. Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecol. Entomol. 30, 600–606 (2005).

    Article  Google Scholar 

  76. Guerrieri, E., Lingua, G., Digilio, M.C., Massa, N. & Berta, G. Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol. Entomol. 29, 753–756 (2004).

    Article  Google Scholar 

  77. Van Wees, S.C.M., Van der Ent, S. & Pieterse, C.M.J. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11, 443–448 (2008).

    CAS  PubMed  Article  Google Scholar 

  78. Van Oosten, V.R. et al. Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol. Plant Microbe Interact. 21, 919–930 (2008).

    CAS  PubMed  Article  Google Scholar 

  79. Dudareva, N., Negre, F., Nagegowda, D.A. & Orlova, I. Plant volatiles: recent advances and future perspectives. Crit. Rev. Plant Sci. 25, 417–440 (2006).

    CAS  Article  Google Scholar 

  80. Andrews, E.S., Theis, N. & Adler, L.S. Pollinator and herbivore attraction to Cucurbita floral volatiles. J. Chem. Ecol. 33, 1682–1691 (2007).

    CAS  PubMed  Article  Google Scholar 

  81. Theis, N. Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J. Chem. Ecol. 32, 917–927 (2006).

    CAS  PubMed  Article  Google Scholar 

  82. Theis, N., Lerdau, M. & Raguso, R.A. The challenge of attracting pollinators while evading floral herbivores: patterns of fragrance emission in Cirsium arvense and Cirsium repandum (Asteraceae). Int. J. Plant Sci. 168, 587–601 (2007).

    Article  Google Scholar 

  83. Euler, M. & Baldwin, I.T. The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107, 102–112 (1996).

    PubMed  Article  Google Scholar 

  84. Effmert, U., Dinse, C. & Piechulla, B. Influence of green leaf herbivory by Manduca sexta on floral volatile emission by Nicotiana suaveolens. Plant Physiol. 146, 1996–2007 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. van Loon, L.C., Bakker, P.A. & Pieterse, C.M. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36, 453–483 (1998).

    CAS  PubMed  Article  Google Scholar 

  86. Kessler, A. & Baldwin, I.T. 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, 639–649 (2004).

    CAS  PubMed  Article  Google Scholar 

  87. Thaler, J.S. Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399, 686–688 (1999).

    CAS  Article  Google Scholar 

  88. Van Zandt, P.A. & Agrawal, A.A. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85, 2616–2629 (2004).

    Article  Google Scholar 

  89. Schmelz, E.A. et al. Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Natl. Acad. Sci. USA 100, 10552–10557 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. Engelberth, J. et al. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol. 125, 369–377 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  91. Heil, M. & Ton, J. Long-distance signalling in plant defence. Trends Plant Sci. 13, 264–272 (2008).

    CAS  PubMed  Article  Google Scholar 

  92. Frost, C.J., Mescher, M.C., Carlson, J.E. & De Moraes, C.M. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 146, 818–824 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  93. Frost, C.J. et al. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol. 180, 722–733 (2008).

    CAS  PubMed  Article  Google Scholar 

  94. van Hulten, M., Pelser, M., van Loon, L.C., Pieterse, C.M. & Ton, J. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 5602–5607 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Heil, M. & Bueno, J.C.S. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 104, 5467–5472 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. Poelman, E.H., van Loon, J.J. & Dicke, M. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13, 534–541 (2008).

    CAS  PubMed  Article  Google Scholar 

  97. Kessler, A. & Baldwin, I.T. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141–2144 (2001).

    CAS  PubMed  Article  Google Scholar 

  98. Snoeren, T.A.L., De Jong, P.W. & Dicke, M. Ecogenomic approach to the role of herbivore-induced plant volatiles in community ecology. J. Ecol. 95, 17–26 (2007).

    CAS  Article  Google Scholar 

  99. Turlings, T.C.J., Tumlinson, J.H. & Lewis, W.J. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251–1253 (1990).

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

The research of the authors was financially supported by European Commission contract MC-RTN-CT-2003-504720 'ISONET' to M.D., by a VICI grant (865.03.002) to M.D. and by a VENI grant (016.091.105) to R.S. from the Earth and Life Sciences Foundation (ALW), which is subsidized by the Netherlands Organization for Scientific Research (NWO).

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Dicke, M., van Loon, J. & Soler, R. Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5, 317–324 (2009). https://doi.org/10.1038/nchembio.169

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