1932

Abstract

Tritrophic interactions between plants, herbivores, and their natural enemies are an integral part of all terrestrial ecosystems. Herbivore-induced plant volatiles (HIPVs) play a key role in these interactions, as they can attract predators and parasitoids to herbivore-attacked plants. Thirty years after this discovery, the ecological importance of the phenomena is widely recognized. However, the primary function of HIPVs is still subject to much debate, as is the possibility of using these plant-produced cues in crop protection. In this review, we summarize the current knowledge on the role of HIPVs in tritrophic interactions from an ecological as well as a mechanistic perspective. This overview focuses on the main gaps in our knowledge of tritrophic interactions, and we argue that filling these gaps will greatly facilitate efforts to exploit HIPVs for pest control.

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2018-01-07
2024-07-15
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Literature Cited

  1. Adebesin F, Widhalm JR, Boachon B, Lefèvre F, Pierman B. 1.  et al. 2017. Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter. Science 356:1386–88 [Google Scholar]
  2. Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH. 2.  et al. 2007. Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. PNAS 104:12976–81 [Google Scholar]
  3. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH. 3.  1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–49 [Google Scholar]
  4. Allmann S, Baldwin IT. 4.  2010. Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075–78 [Google Scholar]
  5. Allmann S, Spathe A, Bisch-Knaden S, Kallenbach M, Reinecke A. 5.  et al. 2013. Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. eLife 2:e00421 [Google Scholar]
  6. Appel HM, Cocroft RB. 6.  2014. Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175:1257–66 [Google Scholar]
  7. Baldwin IT, Schultz JC. 7.  1983. Rapid changes in tree leaf chemistry induced by damage—evidence for communication between plants. Science 221:277–79 [Google Scholar]
  8. Birkett MA, Chamberlain K, Guerrieri E, Pickett JA, Wadhams LJ, Yasuda T. 8.  2003. Volatiles from whitefly-infested plants elicit a host-locating response in the parasitoid. Encarsia formosa. J. Chem. Ecol. 29:1589–600 [Google Scholar]
  9. Blaakmeer A, Geervliet JBF, van Loon JJA, Posthumus MA, van Beek TA, de Groot A. 9.  1994. Comparative headspace analysis of cabbage plants damaged by two species of Pieris caterpillars: consequences for in-flight host location by Cotesia parasitoids. Entomol. Exp. Appl. 73:175–82 [Google Scholar]
  10. Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC. 10.  et al. 2015. The first crop plant genetically engineered to release an insect pheromone for defence. Sci. Rep. 5:11183 [Google Scholar]
  11. Bruce TJA, Matthes MC, Chamberlain K, Woodcock CM, Mohib A. 11.  et al. 2008. cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. PNAS 105:4553–58 [Google Scholar]
  12. Bruce TJA, Midega CAO, Birkett MA, Pickett JA, Khan ZR. 12.  2010. Is quality more important than quantity? Insect behavioural responses to changes in a volatile blend after stemborer oviposition on an African grass. Biol. Lett. 6:314–17 [Google Scholar]
  13. Büchel K, Malskies S, Mayer M, Fenning TM, Gershenzon J. 13.  et al. 2011. How plants give early herbivore alert: volatile terpenoids attract parasitoids to egg-infested elms. Basic Appl. Ecol. 12:403–12 [Google Scholar]
  14. Chen H, Jones AD, Howe GA. 14.  2006. Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Lett 580:2540–46 [Google Scholar]
  15. Choi J, Tanaka K, Cao YR, Qi Y, Qiu J. 15.  et al. 2014. Identification of a plant receptor for extracellular ATP. Science 343:290–94 [Google Scholar]
  16. Christensen SA, Nemchenko A, Borrego E, Murray I, Sobhy IS. 16.  et al. 2013. The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J 74:59–73 [Google Scholar]
  17. Colazza S, McElfresh JS, Millar JG. 17.  2004. Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J. Chem. Ecol. 30:945–64 [Google Scholar]
  18. D'Alessandro M, Brunner V, von Mérey G, Turlings TCJ. 18.  2009. Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize. J. Chem. Ecol. 35:999–1008 [Google Scholar]
  19. D'Alessandro M, Held M, Triponez Y, Turlings TCJ. 19.  2006. The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J. Chem. Ecol. 32:2733–48 [Google Scholar]
  20. Danner H, Brown P, Cator EA, Harren FJM, van Dam NM, Cristescu SM. 20.  2015. Aboveground and belowground herbivores synergistically induce volatile organic sulfur compound emissions from shoots but not from roots. J. Chem. Ecol. 41:631–40 [Google Scholar]
  21. D'Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J. 21.  2007. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J 49:194–207 [Google Scholar]
  22. De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH. 22.  1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–73 [Google Scholar]
  23. De Moraes CM, Mescher MC, Tumlinson JH. 23.  2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–80 [Google Scholar]
  24. Degen T, Dillmann C, Marion-Poll F, Turlings TCJ. 24.  2004. High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Phys 135:1928–38 [Google Scholar]
  25. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A. 25.  2003. Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr. Opin. Biotechnol. 14:169–76 [Google Scholar]
  26. Degenhardt J, Hiltpold I, Kollner TG, Frey M, Gierl A. 26.  et al. 2009. Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. PNAS 106:13213–18 [Google Scholar]
  27. Degenhardt J, Köllner TG, Gershenzon J. 27.  2009. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–37 [Google Scholar]
  28. Desurmont GA, Zemanova MA, Turlings TCJ. 28.  2016. The gastropod menace: Slugs on Brassica plants affect caterpillar survival through consumption and interference with parasitoid attraction. J. Chem. Ecol. 42:183–92 [Google Scholar]
  29. Dicke M, Baldwin IT. 29.  2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help.’. Trends Plant Sci 15:167–75 [Google Scholar]
  30. Dicke M, Sabelis MW. 30.  1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:148–65 [Google Scholar]
  31. Dicke M, van Baarlen P, Wessels R, Dijkman H. 31.  1993. Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J. Chem. Ecol. 19:581–99 [Google Scholar]
  32. Dicke M, van Beek TA, Posthumus MA, Ben Dom N, van Bokhoven H, De Groot A. 32.  1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions: involvement of host plant in its production. J. Chem. Ecol. 16:381–96 [Google Scholar]
  33. Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM. 33.  1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–68 [Google Scholar]
  34. Dudareva N, Klempien A, Muhlemann JK, Kaplan I. 34.  2013. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32 [Google Scholar]
  35. Duran-Flores D, Heil M. 35.  2014. Damaged-self recognition in common bean (Phaseolus vulgaris) shows taxonomic specificity and triggers signaling via reactive oxygen species (ROS). Front. Plant Sci. 5:585 [Google Scholar]
  36. Elzen GW, Williams HJ, Bell AA, Stipanovic RD, Vinson SB. 36.  1985. Quantification of volatile terpenes of glanded and glandless Gossypium hirsutum L. cultivars and lines by gas-chromatography. J. Agr. Food Chem. 33:1079–82 [Google Scholar]
  37. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. 37.  2004. Airborne signals prime plants against insect herbivore attack. PNAS 101:1781–85 [Google Scholar]
  38. Erb M, Meldau S, Howe GA. 38.  2012. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–59 [Google Scholar]
  39. Erb M, Veyrat N, Robert CAM, Xu H, Frey M. 39.  et al. 2015. Indole is an essential herbivore-induced volatile priming signal in maize. Nat. Commun. 6:6273 [Google Scholar]
  40. Farmer EE, Ryan CA. 40.  1990. Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. PNAS 87:7713–16 [Google Scholar]
  41. Fatouros NE, Broekgaarden C, Bukovinszkine'Kiss G, van Loon JJ, Mumm R. 41.  et al. 2008. Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense. PNAS 105:10033–38 [Google Scholar]
  42. Felton GW, Tumlinson JH. 42.  2008. Plant-insect dialogs: complex interactions at the plant-insect interface. Curr. Opin. Plant Biol. 11:457–63 [Google Scholar]
  43. Flint MH, Salter SS, Walters S. 43.  1979. Caryophyllene: an attractant for the green lacewing. Environ. Entomol. 8:1123–25 [Google Scholar]
  44. Fritzsche Hoballah ME, Tamo C, Turlings TCJ. 44.  2002. Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: Is quality or quantity important?. J. Chem. Ecol. 28:951–68 [Google Scholar]
  45. Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC. 45.  2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10:490–98 [Google Scholar]
  46. Gaquerel E, Weinhold A, Baldwin IT. 46.  2009. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphigidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant's elicited volatile emissions. Plant Phys 149:1408–23 [Google Scholar]
  47. Gershenzon J. 47.  2007. Plant volatiles carry both public and private messages. PNAS 104:5257–58 [Google Scholar]
  48. Gershenzon J, Dudareva N. 48.  2007. The function of terpene natural products in the natural world. Nat. Chem. Biol. 3:408–14 [Google Scholar]
  49. Gilardoni PA, Hettenhausen C, Baldwin IT, Bonaventure G. 49.  2011. Nicotiana attenuata LECTIN RECEPTOR KINASE1 suppresses the insect-mediated inhibition of induced defense responses during Manduca sexta herbivory. Plant Cell 23:3512–32 [Google Scholar]
  50. Gouinguené S, Pickett JA, Wadhams LJ, Birkett MA, Turlings TCJ. 50.  2005. 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. 31:1023–38 [Google Scholar]
  51. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT. 51.  2008. Shared signals—‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11:24–34 [Google Scholar]
  52. Hall DE, MacGregor KB, Nijsse J, Bown AW. 52.  2004. Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. Eur. J. Plant Pathol. 110:441–47 [Google Scholar]
  53. Hansel A, Jordan A, Holzinger R, Prazeller P, Vogel W, Lindinger W. 53.  1995. Proton transfer reaction mass spectrometry: on-line trace gas analysis at the ppb level. Int. J. Mass Spectrom. Ion Process. 149:609–19 [Google Scholar]
  54. Hare JD. 54.  2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu. Rev. Entomol. 56:161–80 [Google Scholar]
  55. Heil M. 55.  2014. Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol 204:297–306 [Google Scholar]
  56. Heil M, Ibarra-Laclette E, Adame-Alvarez RM, Martinez O, Ramirez-Chavez E. 56.  et al. 2012. How plants sense wounds: Damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLOS ONE 7:e30537 [Google Scholar]
  57. Heil M, Karban R. 57.  2010. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25:137–44 [Google Scholar]
  58. Heil M, Land WG. 58.  2014. Danger signals—damaged-self recognition across the tree of life. Front. Plant Sci. 5:578 [Google Scholar]
  59. Heil M, Silva Bueno JC. 59.  2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. PNAS 104:5467–72 [Google Scholar]
  60. Heil M, Ton J. 60.  2008. Long-distance signalling in plant defence. Trends Plant Sci 13:264–72 [Google Scholar]
  61. Hilker M, Fatouros NE. 61.  2015. Plant responses to insect egg deposition. Annu. Rev. Entomol. 60:493–515 [Google Scholar]
  62. Hilker M, Kobs C, Varama M, Schrank K. 62.  2002. Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J. Exp. Biol. 205:455–61 [Google Scholar]
  63. Hilker M, Meiners T. 63.  2010. How do plants “notice” attack by herbivorous arthropods?. Biol. Rev. 85:267–80 [Google Scholar]
  64. Hiltpold I, Erb M, Robert CAM, Turlings TCJ. 64.  2011. Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ 34:1267–75 [Google Scholar]
  65. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S. 65.  et al. 2012. The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008 [Google Scholar]
  66. Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TCJ. 66.  et al. 2013. Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. PNAS 110:5707–12 [Google Scholar]
  67. James DG. 67.  2003. Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ. Entomol. 32:977–82 [Google Scholar]
  68. James DG, Grasswitz TR. 68.  2005. Synthetic herbivore-induced plant volatiles increase field captures of parasitic wasps. BioControl 50:871–80 [Google Scholar]
  69. Joensuu J, Altimir N, Hakola H, Rostas M, Raivonen M. 69.  et al. 2016. Role of needle surface waxes in dynamic exchange of mono- and sesquiterpenes. Atmos. Chem. Phys. 16:7813–23 [Google Scholar]
  70. Joo Y, Schuman MC, Goldberg JK, Kim S-G, Yon F. 70.  et al. Herbivore-induced volatile blends with both “fast” and “slow” components provide robust indirect defence in nature. Funct. Ecol. In press. https://doi.org/10.1111/1365-2435.12947 [Crossref] [Google Scholar]
  71. Jordan A, Haidacher S, Hanel G, Hartungen E, Märk L. 71.  et al. 2009. A high resolution and high sensitivity proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS). Int. J. Mass Spectrom. 286:122–28 [Google Scholar]
  72. Kaplan I. 72.  2012. Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire?. Biol. Control 60:77–89 [Google Scholar]
  73. Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ. 73.  2005. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–72 [Google Scholar]
  74. Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY. 74.  2013. Kin recognition affects plant communication and defence. Proc. R. Soc. B 280:20123062 [Google Scholar]
  75. Karban R, Yang LH, Edwards KF. 75.  2014. Volatile communication between plants that affects herbivory: a meta-analysis. Ecol. Lett. 17:44–52 [Google Scholar]
  76. Kessler A, Baldwin IT. 76.  2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–44 [Google Scholar]
  77. Kessler A, Heil M. 77.  2011. The multiple faces of indirect defences and their agents of natural selection. Funct. Ecol. 25:348–57 [Google Scholar]
  78. Khan ZR, Ampong-Nyarko K, Chiliswa P, Hassanali A, Kimani S. 78.  et al. 1997. Intercropping increases parasitism of pests. Nature 388:631–32 [Google Scholar]
  79. Koornneef A, Pieterse CM. 79.  2008. Cross talk in defense signaling. Plant Phys 146:839–44 [Google Scholar]
  80. Lang HP, Loizeau F, Hiou-Feige A, Rivals JP, Romero P. 80.  et al. 2016. Piezoresistive membrane surface stress sensors for characterization of breath samples of head and neck cancer patients. Sensors 16:1149 [Google Scholar]
  81. Lannoo N, van Damme EJM. 81.  2014. Lectin domains at the frontiers of plant defense. Front. Plant Sci. 5:397 [Google Scholar]
  82. Lee JC. 82.  2010. Effect of methyl salicylate-based lures on beneficial and pest arthropods in strawberry. Environ. Entomol. 39:653–60 [Google Scholar]
  83. Liu YQ, Wu H, Chen H, Liu YL, He J. 83.  et al. 2015. A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat. Biotechnol. 33:301–5 [Google Scholar]
  84. Loreto F, Schnitzler JP. 84.  2010. Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–66 [Google Scholar]
  85. Lou YG, Du MH, Turlings TCJ, Cheng JA, Shan WF. 85.  2005. Exogenous application of jasmonic acid induces volatile emissions in rice and enhances parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae. J. Chem. Ecol. 31:1985–2002 [Google Scholar]
  86. Loughrin JH, Manukian A, Heath RR, Turlings TCJ, Tumlinson JH. 86.  1994. Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant. PNAS 91:11836–40 [Google Scholar]
  87. Mutyambai DM, Bruce TJ, van den Berg J, Midega CA, Pickett PA, Khan ZR. 87.  2016. An indirect defence trait mediated through egg-induced maize volatiles from neighbouring plants. PLOS ONE 11:e0158744 [Google Scholar]
  88. Matthes MC, Bruce TJ, Ton J, Verrier PJ, Pickett JA, Napier JA. 88.  2010. The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence. Planta 232:1163–80 [Google Scholar]
  89. Mattiacci L, Dicke M, Posthumus MA. 89.  1995. β-glucosidase—an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. PNAS 92:2036–40 [Google Scholar]
  90. Mauch-Mani B, Baccelli I, Luna E, Flors V. 90.  2017. Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68:485–512 [Google Scholar]
  91. Mithöfer A, Wanner G, Boland W. 91.  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 Phys 137:1160–68 [Google Scholar]
  92. Moraes MCB, Laumann RA, Pareja M, Sereno FTPS, Michereff MFF. 92.  et al. 2009. Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone. Entomol. Exp. Appl. 131:178–88 [Google Scholar]
  93. Mumm R, Dicke M. 93.  2010. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can. J. Zool. 88:628–67 [Google Scholar]
  94. Mumm R, Hilker M. 94.  2005. The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem. Senses 30:337–43 [Google Scholar]
  95. Naranjo-Guevara N, Peñaflor MFGV, Cabezas-Guerrero MF, Bento JMS. 95.  2017. Nocturnal herbivore-induced plant volatiles attract the generalist predatory earwig Doru luteipes Scudder. Sci. Nat. 104:77 [Google Scholar]
  96. Neveu N, Grandgirard J, Nenon JP, Cortesero AM. 96.  2002. Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. J. Chem. Ecol. 28:1717–32 [Google Scholar]
  97. Nordlund DA, Lewis WJ, Altieri MA. 97.  1988. Influences of plant produced allelochemicals on the host and prey selection of entomophagous insects. Novel Aspects of Insect-Plant Interactions, P Barbosa, DK Letourneau 65–90 New York: Wiley [Google Scholar]
  98. Paré PW, Tumlinson JH. 98.  1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Phys 114:1161–67 [Google Scholar]
  99. Peiffer M, Tooker JF, Luthe DS, Felton GW. 99.  2009. Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–56 [Google Scholar]
  100. Peñaflor MF, Erb M, Robert CA, Miranda LA, Werneburg AG. 100.  et al. 2011. Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234:207–15 [Google Scholar]
  101. Pickett JA, Hamilton ML, Hooper AM, Khan ZR, Midega CAO. 101.  2010. Companion cropping to manage parasitic plants. Annu. Rev. Phytopathol. 48:161–77 [Google Scholar]
  102. Pickett JA, Khan ZR. 102.  2016. Plant volatile-mediated signalling and its application in agriculture: successes and challenges. New Phytol 212:856–70 [Google Scholar]
  103. Pickett JA, Woodcock CM, Midega CAO, Khan ZR. 103.  2014. Push-pull farming systems. Curr. Opin. Biotechnol. 26:125–32 [Google Scholar]
  104. Poelman EH, Oduor AMO, Broekgaarden C, Hordijk CA, Jansen JJ. 104.  et al. 2009. Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct. Ecol. 23:951–62 [Google Scholar]
  105. Pope TW, Kissen R, Grant M, Pickett JA, Rossiter JT, Powell G. 105.  2008. Comparative innate responses of the aphid parasitoid Diaeretiella rapae to alkenyl glucosinolate derived isothiocyanates, nitriles, and epithionitriles. J. Chem. Ecol. 34:1302–10 [Google Scholar]
  106. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. 106.  1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. System. 11:41–65 [Google Scholar]
  107. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S. 107.  et al. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–37 [Google Scholar]
  108. Renou A, Téréta I, Togola M. 108.  2011. Manual topping decreases bollworm infestations in cotton cultivation in Mali. Crop. Prot. 30:1370–75 [Google Scholar]
  109. Robert CAM, Erb M, Hiltpold I, Hibbard BE, Gaillard MDP. 109.  et al. 2013. Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol. J. 11:628–39 [Google Scholar]
  110. Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L. 110.  2011. Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol. Control 59:294–303 [Google Scholar]
  111. Röse USR, Manukian A, Heath RR, Tumlinson JH. 111.  1996. Volatile semiochemicals released from undamaged cotton leaves—a systemic response of living plants to caterpillar damage. Plant Phys 111:487–95 [Google Scholar]
  112. Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A. 112.  et al. 2011. A herbivore that manipulates plant defence. Ecol. Lett. 14:229–36 [Google Scholar]
  113. Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC. 113.  2013. Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 14:17781–811 [Google Scholar]
  114. Schmelz EA. 114.  2015. Impacts of insect oral secretions on defoliation-induced plant defense. Curr. Opin. Insect Sci. 9:7–15 [Google Scholar]
  115. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J. 115.  et al. 2006. Fragments of ATP synthase mediate plant perception of insect attack. PNAS 103:8894–99 [Google Scholar]
  116. Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J. 116.  2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. PNAS 103:1129–34 [Google Scholar]
  117. Schröder R, Hilker M. 117.  2008. The relevance of background odor in resource location by insects: a behavioral approach. BioScience 58:308–16 [Google Scholar]
  118. Schuman MC, Allmann S, Baldwin IT. 118.  2015. Plant defense phenotypes determine the consequences of volatile emission for individuals and neighbors. eLife 4:e04490 [Google Scholar]
  119. Schuman MC, Barthel K, Baldwin IT. 119.  2012. Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature. eLife 1:e00007 [Google Scholar]
  120. Seidl-Adams I, Richter A, Boomer KB, Yoshinaga N, Degenhardt J, Tumlinson JH. 120.  2015. Emission of herbivore elicitor-induced sesquiterpenes is regulated by stomatal aperture in maize (Zea mays) seedlings. Plant Cell Environ 38:23–34 [Google Scholar]
  121. Shimoda T, Nishihara M, Ozawa R, Takabayashi J, Arimura G. 121.  2012. The effect of genetically enriched (E)-β-ocimene and the role of floral scent in the attraction of the predatory mite Phytoseiulus persimilis to spider mite-induced volatile blends of torenia. New Phytol 193:1009–21 [Google Scholar]
  122. Shiojiri K, Ozawa R, Takabayashi J. 122.  2006. Plant volatiles, rather than light, determine the nocturnal behavior of a caterpillar. PLOS Biol 4:e164 [Google Scholar]
  123. Shulaev V, Silverman P, Raskin I. 123.  1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–21 [Google Scholar]
  124. Smallegange RC, van Loon JJA, Blatt SE, Harvey JA, Dicke M. 124.  2008. Parasitoid load affects plant fitness in a tritrophic system. Entomol. Exp. Appl. 128:172–83 [Google Scholar]
  125. Snoeren TAL, Mumm R, Poelman EH, Yang Y, Pichersky E, Dicke M. 125.  2010. The herbivore-induced plant volatile methyl salicylate negatively affects attraction of the parasitoid Diadegma semiclausum. J. Chem. Ecol. 36:479–89 [Google Scholar]
  126. Sobhy IS, Erb M, Lou YG, Turlings TCJ. 126.  2014. The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests. Philos. Trans. R. Soc. B 369:20120283 [Google Scholar]
  127. Sobhy IS, Erb M, Sarhan AA, El-Husseini MM, Mandour NS, Turlings TCJ. 127.  2012. Less is more: treatment with BTH and laminarin reduces herbivore-induced volatile emissions in maize but increases parasitoid attraction. J. Chem. Ecol. 38:348–60 [Google Scholar]
  128. Spielmann FM, Langebner S, Ghirardo A, Hansel A, Schnitzler J-P, Wohlfahrt G. 128.  2017. Isoprene and α-pinene deposition to grassland mesocosms. Plant Soil 410:313–22 [Google Scholar]
  129. Takabayashi J, Takahashi S, Dicke M, Posthumus MA. 129.  1995. Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. J. Chem. Ecol. 21:273–87 [Google Scholar]
  130. Tamiru A, Bruce TJ, Woodcock CM, Caulfield JC, Midega CA. 130.  et al. 2011. Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol. Lett. 14:1075–83 [Google Scholar]
  131. Thaler JS. 131.  1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–88 [Google Scholar]
  132. Ton J, D'Alessandro M, Jourdie V, Jakab G, Karlen D. 132.  et al. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26 [Google Scholar]
  133. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM. 133.  2008. Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–71 [Google Scholar]
  134. Truitt CL, Wei HX, Pare PW. 134.  2004. A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. Plant Cell 16:523–32 [Google Scholar]
  135. Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D. 135.  1998. Timing of induced volatile emissions in maize seedlings. Planta 207:146–52 [Google Scholar]
  136. Turlings TCJ, Tumlinson JH. 136.  1992. Systemic release of chemical signals by herbivore-injured corn. PNAS 89:8399–402 [Google Scholar]
  137. Turlings TCJ, Tumlinson JH, Lewis WJ. 137.  1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–53 [Google Scholar]
  138. Uefune M, Choh Y, Abe J, Shiojiri K, Sano K, Takabayashi J. 138.  2012. Application of synthetic herbivore-induced plant volatiles causes increased parasitism of herbivores in the field. J. Appl. Entomol. 136:561–67 [Google Scholar]
  139. van de Ven WTG, LeVesque CS, Perring TM, Walling LL. 139.  2000. Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12:1409–23 [Google Scholar]
  140. van Loon JJA, de Boer JG, Dicke M. 140.  2000. Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol. Exp. Appl. 97:219–27 [Google Scholar]
  141. Vet LEM, Lewis WJ, Cardé RT. 141.  1995. Parasitoid foraging and learning. Chemical Ecology of Insects 2 RT Cardé, WJ Bell 65–101 Boston, MA: Springer [Google Scholar]
  142. Veyrat N, Robert CAM, Turlings TCJ, Erb M. 142.  2016. Herbivore intoxication as a potential primary function of an inducible volatile plant signal. J. Ecol. 104:591–600 [Google Scholar]
  143. Vinson SB, Eizen GW, Williams HJ. 143.  1987. The influence of volatile plant allelochemics on the third trophic level (parasitoids) and their hosts. Insects–Plants V Labeyrie, G Fabres, D Lachaise 109–14 Dordrecht, Neth.: Junk [Google Scholar]
  144. von Mérey GE, Veyrat N, de Lange E, Degen T, Mahuku G. 144.  et al. 2012. Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields. Biol. Control 60:7–15 [Google Scholar]
  145. Webster B, Bruce T, Pickett J, Hardie J. 145.  2010. Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim. Behav. 79:451–57 [Google Scholar]
  146. Wei J, Wang L, Zhu J, Zhang S, Nandi OI, Kang L. 146.  2007. Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. PLOS ONE 2:e852 [Google Scholar]
  147. Whitman DW, Eller FJ. 147.  1990. Parasitic wasps orient to green leaf volatiles. Chemoecology 1:69–76 [Google Scholar]
  148. Widhalm JR, Jaini R, Morgan JA, Dudareva N. 148.  2015. Rethinking how volatiles are released from plant cells. Trends Plant Sci 20:545–50 [Google Scholar]
  149. Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L. 149.  et al. 2012. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol. Lett. 15:1130–39 [Google Scholar]
  150. Xin Z, Yu Z, Erb M, Turlings TCJ, Wang B. 150.  et al. 2012. The broad-leaf herbicide 2,4-dichlorophenoxyacetic acid turns rice into a living trap for a major insect pest and a parasitic wasp. New Phytol 194:498–510 [Google Scholar]
  151. Zarate SI, Kempema LA, Walling LL. 151.  2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Phys 143:866–75 [Google Scholar]
  152. Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, van Loon JJA. 152.  et al. 2013. Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197:1291–99 [Google Scholar]
  153. Zhang PJ, Xu CX, Zhang JM, Lu YB, Wei JN. 153.  et al. 2013. Phloem-feeding whiteflies can fool their host plants, but not their parasitoids. Funct. Ecol. 27:1304–12 [Google Scholar]
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