The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'

Trends in Plant Science

Volumn 15, Issue 3, 2010, Pages 167-175

  Dicke, Marcel ^a   Baldwin, Ian T ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VOLATILE ORGANIC COMPOUND;

ANIMAL; ANIMAL BEHAVIOR; CHEMISTRY; EVOLUTION; FOOD CHAIN; METABOLISM; PLANT; PLANT PHYSIOLOGY; REVIEW;

ANIMALS; BEHAVIOR, ANIMAL; EVOLUTION; FOOD CHAIN; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; VOLATILE ORGANIC COMPOUNDS;

EID: 77649216975     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2009.12.002     Document Type: Review

References (107)

1. Schoonhoven L.M., et al. Insect-Plant Biology (2005), Oxford University Press
2. Dicke M., et al. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5 (2009) 317-324
3. Fatouros N.E., et al. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19 (2008) 677-689
4. Unsicker S.B., et al. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 12 (2009) 479-485
5. Mumm R., and Hilker M. Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci. 11 (2006) 351-358
6. Mumm, R. and Dicke, M. Variation in natural plant products and the attraction of bodyguards for indirect plant defense. Can. J. Zool. (in press)
7. Dudareva N., et al. Biochemistry of plant volatiles. Plant Physiol. 135 (2004) 1893-1902
8. Heil M., and Ton J. Long-distance signalling in plant defence. Trends Plant Sci. 13 (2008) 264-272
9. Gaquerel E., et al. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant's elicited volatile emissions. Plant Physiol. 149 (2009) 1408-1423
10. Dicke M., and Van Loon J.J.A. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97 (2000) 237-249
11. Bruinsma M., et al. Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J. Exp. Bot. 60 (2009) 2575-2587
12. Rasmann S., et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434 (2005) 732-737
13. Mantyla E., et al. Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences?. Ecol. Lett. 7 (2004) 915-918
14. Runyon J.B., et al. Volatile chemical cues guide host location and host selection by parasitic plants. Science 313 (2006) 1964-1967
15. Baldwin I.T., et al. Volatile signaling in plant-plant interactions: 'Talking trees' in the genomics era. Science 311 (2006) 812-815
16. Soler R., et al. Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116 (2007) 367-376
17. Kessler A., and Halitschke R. Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure. Curr. Opin. Plant Biol. 10 (2007) 409-414
18. Bruinsma M., and Dicke M. Herbivore-induced indirect defence: from induction mechanisms to community ecology. In: Schaller A. (Ed). Induced Plant Resistance to Herbivory (2008), Springer 31-60
19. Bruinsma M., et al. Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids, and butterflies. Entomol. Exp. Appl. 128 (2008) 109-116
20. Van der Putten W.H., et al. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens and their antagonists. Trends Ecol. Evol. 16 (2001) 547-554
21. Rosenheim J.A. Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43 (1998) 421-447
22. Finke D.L., and Denno R.F. Predator diversity dampens trophic cascades. Nature 429 (2004) 407-410
23. Kaplan I., and Denno R.F. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett. 10 (2007) 977-994
24. Denno R.F., et al. Interspecific interaction in phytophagous insects: competition reexamined and resurrected. Annu. Rev. Entomol. 40 (1995) 297-331
25. Dicke M. Volatile spider-mite pheromone and host-plant kairomone, involved in spaced-out gregariousness in the spider mite Tetranychus urticae. Physiol. Entomol. 11 (1986) 251-262
26. Kessler A., and Baldwin I.T. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291 (2001) 2141-2144
27. De Moraes C.M., et al. Caterpillar-induced nocturnal plant volatiles repel nonspecific females. Nature 410 (2001) 577-580
28. Halitschke R., et al. Shared signals - 'alarm calls' from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11 (2008) 24-34
29. Bolter C.J., et al. Attraction of Colorado potato beetle to herbivore damaged plants during herbivory and after its termination. J. Chem. Ecol. 23 (1997) 1003-1023
30. Price P.W., et al. Interactions among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11 (1980) 41-65
31. Dicke M., and Sabelis M.W. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38 (1988) 148-165
32. Heil M. Induction of two indirect defences benefits Lima bean (Phaseolus lunatus, Fabaceae) in nature. J. Ecol. 92 (2004) 527-536
33. De Moraes C.M., et al. Herbivore-infested plants selectively attract parasitoids. Nature 393 (1998) 570-573
34. Bernasconi M.L., et al. Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.). Agr. For. Entomol. 3 (2001) 201-209
35. Poelman E.H., et al. Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct. Ecol. 23 (2009) 951-962
36. Sabelis M.W., and Van de Baan H.E. Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol. Exp. Appl. 33 (1983) 303-314
37. 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 (1990) 381-396
38. Sabelis M.W., et al. Experimental validation of a simulation model of the interaction between Phytoseiulus persimilis and Tetranychus urticae on cucumber. IOBC/WPRS Bull. 6 (1983) 207-229
39. Gomez J.M., and Zamora R. Top-down effects in a tritrophic system: parasitoids enhance plant fitness. Ecology 75 (1994) 1023-1030
40. Van Loon J.J.A., et al. Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol. Exp. Appl. 97 (2000) 219-227
41. Fritzsche-Hoballah M.E., and Turlings T.C.J. Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol. Ecol. Res. 3 (2001) 553-565
42. Crawley M.J. Reduction of oak fecundity by low-density herbivore populations. Nature 314 (1985) 163-164
43. Takabayashi J., et al. Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors. J. Chem. Ecol. 20 (1994) 1329-1354
44. Lou Y.G., and Baldwin I.T. Nitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses to Nicotiana attenuata. Plant Physiol. 135 (2004) 496-506
45. Gouinguene S., et al. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11 (2001) 9-16
46. Turlings T.C.J., and Fritzsche M.E. Attraction of parasitic wasps by caterpillar-damaged plants. In: Chadwick D.J., and Goode J. (Eds). Insect-Plant Interactions and Induced Plant Defence (Novartis Foundation Symposium 223) (1999), John Wiley & Sons 21-32
47. Gols R., et al. 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 (2003) 2651-2666
48. Smid H.M., et al. GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12 (2002) 169-176
49. De Bruyne M., et al. Receptor cell responses in the anterior tarsi of Phytoseiulus persimilis to volatile kairomone components. Exp. Appl. Acarol. 13 (1991) 53-58
50. Gouinguene S., et al. Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J. Chem. Ecol. 31 (2005) 1023-1038
51. Vet L.E.M., and Dicke M. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37 (1992) 141-172
52. Halitschke R., et al. Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124 (2000) 408-417
53. Dicke M., and Sabelis M.W. Does it pay plants to advertize for bodyguards? Towards a cost-benefit analysis of induced synomone production. In: Lambers H., et al. (Ed). Causes & Consequences of Variation in Growth Rate and Productivity of Higher Plants (1989), SPB Publishing 341-358
54. De Boer J.G., and Dicke M. The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J. Chem. Ecol. 30 (2004) 255-271
55. De Boer J.G., et al. Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J. Chem. Ecol. 30 (2004) 2215-2230
56. D'Alessandro M., et al. The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J. Chem. Ecol. 32 (2006) 2733-2748
57. Bernasconi M.L., et al. Herbivore-induced emissions of maize volatiles repel the corn-leaf aphid, Rhopalosiphum maidis. Entomol. Exp. Appl. 87 (1998) 133-142
58. Kalberer N.M., et al. Attraction of a leaf beetle (Oreina cacaliae) to damaged host plants. J. Chem. Ecol. 27 (2001) 647-661
59. van Tol R.W.H.M., et al. Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone. Bull. Entomol. Res. 99 (2009) 593-602
60. Rojas J.C. Influence of host plant damage on the host-finding behavior of Mamestra brassicae (Lepidoptera: Noctuidae). Environ. Entomol. 28 (1999) 588-593
61. Anderson P., and Alborn H. Effects on oviposition behaviour and larval development of Spodoptera littoralis by herbivore-induced changes in cotton plants. Entomol. Exp. Appl. 92 (1999) 45-51
62. Meldau S., et al. Silencing two herbivory-activated MAP kinases, SIPK and WIPK, does not increase Nicotiana attenuata's susceptibility to herbivores in the glasshouse and in nature. New Phytol. 181 (2009) 161-173
63. Poelman E.H., et al. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13 (2008) 534-541
64. Kessler A., and 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 (2004) 639-649
65. Brown G.C., et al. Green leaf volatiles inhibit conidial germination of the entomopathogen Pandora neoaphidis (Entomophthorales: Entomophthoraceae). Environ. Entomol. 24 (1995) 1637-1643
66. 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. U. S. A. 103 (2006) 16672-16676
67. Yi H.-S., et al. Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151 (2009) 2152-2161
68. Rayapuram C., et al. PR-13/Thionin but not PR-1 mediates bacterial resistance in Nicotiana attenuata in nature and neither influences herbivore resistance. Mol. Plant-Microbe Interact. 21 (2008) 988-1000
69. Raguso R.A. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39 (2008) 549-569
70. Theis N., et al. Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp texana (Cucurbitaceae) flowers. Am. J. Bot. 96 (2009) 897-903
71. Kessler A., and Halitschke R. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Funct. Ecol. 23 (2009) 901-912
72. Dicke M., and Bruin J. Chemical information transfer between plants: back to the future. Biochem. Syst. Ecol. 29 (2001) 981-994
73. Karban R., et al. Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100 (2003) 325-332
74. Frost C.J., et al. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 146 (2008) 818-824
75. Paschold A., et al. Using 'mute' plants to translate volatile signals. Plant J. 45 (2006) 275-291
76. Karban R., and Shiojiri K. Self-recognition affects plant communication and defense. Ecol. Lett. 12 (2009) 502-506
77. Dicke M., et al. Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods. Oikos 101 (2003) 38-48
78. Schroeder R., and Hilker M. The relevance of background odor in resource location by insects: a behavioral approach. Bioscience 58 (2008) 308-316
79. Loivamaki M., et al. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 17430-17435
80. Velikova V., et al. Isoprene and nitric oxide reduce damages in leaves exposed to oxidative stress. Plant Cell Environ. 31 (2008) 1882-1894
81. Maffei M.E., et al. Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68 (2007) 2946-2959
82. Kessler A., and Baldwin I.T. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53 (2002) 299-328
83. Pieterse C.M.J., and Dicke M. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci. 12 (2007) 564-569
84. Halitschke R., et al. 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 (2003) 1894-1902
85. Wu J.Q., et al. Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19 (2007) 1096-1122
86. Skibbe M., et al. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20 (2008) 1984-2000
87. Wu J.Q., and Baldwin I.T. Herbivory-induced signalling in plants: perception and action. Plant Cell Environ. 32 (2009) 1161-1174
88. Kessler A., et al. Silencing the jasmonate cascade: Induced plant defenses and insect populations. Science 305 (2004) 665-668
89. Pieterse C.M.J., et al. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5 (2009) 308-316
90. Zhang P.J., et al. Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 21202-21207
91. Van Poecke R.M.P., and Dicke M. Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J. Exp. Bot. 53 (2002) 1793-1799
92. Dicke M., et al. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol. 25 (1999) 1907-1922
93. Snoeren T.A.L., et al. Multidisciplinary approach to unravelling the relative contribution of different oxylipins in indirect defense of Arabidopsis thaliana. J. Chem. Ecol. 35 (2009) 1021-1031
94. Kappers I.F., et al. Genetic engineering of terpenoid metabolism attracts, bodyguards to Arabidopsis. Science 309 (2005) 2070-2072
95. 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. U. S. A. 103 (2006) 1129-1134
96. Degenhardt J., et al. Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 13213-13218
97. Kollner T.G., et al. A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20 (2008) 482-494
98. Degen T., et al. High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol. 135 (2004) 1928-1938
99. Krips O.E., et al. Comparison of cultivars of ornamental crop Gerbera jamesonii on production of spider mite-induced volatiles, and their attractiveness to the predator Phytoseiulus persimilis. J. Chem. Ecol. 27 (2001) 1355-1372
100. Takabayashi J., et al. Variation in composition of predator-attracting allelochemicals emitted by herbivore-infested plants: relative influence of plant and herbivore. Chemoecology 2 (1991) 1-6
101. Loughrin J.H., et al. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol. 21 (1995) 1217-1227
102. Hare J.D. Variation in herbivore and methyl jasmonate-induced volatiles among genetic lines of Datura wrightii. J. Chem. Ecol. 33 (2007) 2028-2043
103. Schuman M.C., et al. Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytol. 183 (2009) 1134-1148
104. Gols R., et al. Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps?. Oikos 118 (2009) 733-743
105. Thompson J.N. The Geographic Mosaic of Coevolution (2005), University of Chicago Press
106. Van der Meijden E. Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol. Exp. Appl. 80 (1996) 307-310
107. Dicke M., and Sabelis M.W. Infochemical terminology: based on cost-benefit analysis rather than origin of compounds?. Funct. Ecol. 2 (1988) 131-139