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Herbivore-Induced Plant Volatiles to Enhance Biological Control in Agriculture

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Abstract

Plants under herbivore attack synthetize defensive organic compounds that directly or indirectly affect herbivore performance and mediate other interactions with the community. The so-called herbivore-induced plant volatiles (HIPVs) consist of odors released by attacked plants that serve as important cues for parasitoids and predators to locate their host/prey. The understanding that has been gained on the ecological role and mechanisms of HIPV emission opens up paths for developing novel strategies integrated with biological control programs with the aim of enhancing the efficacy of natural enemies in suppressing pest populations in crops. Tactics using synthetic HIPVs or chemically/genetically manipulating plant defenses have been suggested in order to recruit natural enemies to plantations or help guiding them to their host more quickly, working as a “synergistic” agent of biological control. This review discusses strategies using HIPVs to enhance biological control that have been proposed in the literature and were categorized here as: (a) exogenous application of elicitors on plants, (b) use of plant varieties that emit attractive HIPVs to natural enemies, (c) release of synthetic HIPVs, and (d) genetic manipulation targeting genes that optimize HIPV emission. We discuss the feasibility, benefits, and downsides of each strategy by considering not only field studies but also comprehensive laboratory assays that present an applied approach for HIPVs or show the potential of employing them in the field.

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References

  • Aharoni A, Giri AP, Deuerlein S, Griepink F, De Kogel WJ, Verstappen FWA, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884

    Article  PubMed  CAS  Google Scholar 

  • Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602

    Article  PubMed  CAS  Google Scholar 

  • Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037

    Article  PubMed  CAS  Google Scholar 

  • Arimura GI, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923

    Article  PubMed  CAS  Google Scholar 

  • Auger J, Lecomte C, Paris J, Thibout E (1989) Identification of leek-moth and diamondback-moth frass volatiles that stimulate parasitoid, Diadromus pulchellus. J Chem Ecol 15:1391–1398

    Article  CAS  Google Scholar 

  • Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971–980

    Article  CAS  Google Scholar 

  • Baverstock J, Elliot SL, Alderson PG, Pell JK (2005) Response of the entomopathogenic fungus Pandora neoaphidis to aphid-induced plant volatiles. J Invertebr Pathol 89:157–164

    Article  PubMed  CAS  Google Scholar 

  • Beevers M, Lewis WJ, Gross HR, Norlund DA (1981) Kairomones and their use for management of entomophagous insects: X. Laboratory studies on manipulation of host-finding behavior of Trichogramma pretiosum Riley with a kairomone extracted from Heliothis zea (Boddie) moth scales. J Chem Ecol 7:635–648

    Article  CAS  Google Scholar 

  • Bernasconi ML, Turlings TCJ, Ambrosetti L, Bassetti P, Dorn S (1998) Herbivore-induced emissions of maize volatiles repel the corn-leaf aphid, Rhopalosiphum maidis. Entomol Exp Appl 87:133–142

    Article  CAS  Google Scholar 

  • Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Wadhams LJ, Woodcock CM (2000) New roles of cis-jasmone as an insect semiochemicals and in plant defense. Proc Natl Acad Sci USA 97:9329–9334

    Article  PubMed  CAS  Google Scholar 

  • Boland W, Hopke J, Donath J, Nüske J, Bublitz F (1995) Jasmonic acid and coronation induce odor production in plants. Angew Chem Int Ed Engl 34:1600–1602

    Article  CAS  Google Scholar 

  • Bolter CJ, Dicke M, van Loon JJA, Visser JH, Posthumus MA (1997) Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J Chem Ecol 23:1003–1023

    Article  CAS  Google Scholar 

  • Bostock RM, Karban R, Thaler JS, Weyman PD, Gilchrist D (2001) Signal interactions in induced resistance to pathogens and insect herbivores. Eur J Plant Pathol 107:103–111

    Article  CAS  Google Scholar 

  • Botelho PSM, Parra JRP, Chagas-Neto JF, Oliveira CPB (1999) Associação dos parasitóides de ovos Trichogramma galloi Zucchi (Hymenoptera: Trichogrammatidae) e do parasitóide larval Cotesia flavipes (Cam.) (Hymenoptera: Braconidae) no controle de Diatraea saccharalis (Fabr.) (Lepidoptera: Crambidae) em cana-de-açucar. An Soc Entomol Bras 28:491–496

    Article  Google Scholar 

  • Braasch J, Wimp GM, Kaplan I (2012) Testing for phytochemical synergism: arthropod community responses to induced plant volatile blends across crops. J Chem Ecol 38:1264–1275

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Martin JL, Pickett JA, Pye BJ, Smart LE, Wadhams LJ (2003) cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Manag Sci 59:1031–1036

    Article  PubMed  CAS  Google Scholar 

  • Bruinsma M, Van Dam NM, Van Loon JJA, Dicke M (2007) Jasmonic acid-induced changes in Brassica oleracea affect oviposition preference of two specialist herbivores. J Chem Ecol 33:655–668

    Article  PubMed  CAS  Google Scholar 

  • Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, Van Loon JJA, Dicke M (2009) Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J Exp Bot 60:2575–2587

    Article  PubMed  CAS  Google Scholar 

  • Camelo LA, Landolt PJ, Zack RS (2007) A kairomone based attract-and-kill system effective against alfalfa looper (Lepidoptera: Noctuidae). J Econ Entomol 100:366–374

    Article  Google Scholar 

  • Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924

    Article  PubMed  CAS  Google Scholar 

  • Cheng A-X, Xiang C-Y, Li J-X, Yang C-Q, Hu W-L, Wang L-J, Lou Y-G, Chen X-Y (2007) The rice (E)-β-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 68:1632–1641

    Article  PubMed  CAS  Google Scholar 

  • Colazza S, Rosi MC, Clemente A (1997) Response of egg parasitoid Telenomus busseolae to sex pheromone of Sesamia nonagrioides. J Chem Ecol 23:2437–2444

    Article  CAS  Google Scholar 

  • Colazza S, Fucarino A, Peri E, Salerno G, Conti E, Bin F (2004) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J Exp Biol 207:47–53

    Article  PubMed  Google Scholar 

  • Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding and manipulating plant attributes to enhance biological control. Biol Control 17:35–49

    Article  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol 48:355–381

    Article  CAS  Google Scholar 

  • D’Alessandro M, Turlings TCJ (2005) In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem Senses 30:739–753

    Article  PubMed  Google Scholar 

  • D’Alessandro M, Held M, Triponez Y, Turlings TCJ (2006) The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32:2733–2748

    Article  PubMed  CAS  Google Scholar 

  • D’Alessandro M, Brunner V, von Mérey G, Turlings TCJ (2009) Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize. J Chem Ecol 35:999–1008

    Article  PubMed  CAS  Google Scholar 

  • De Boer JG, Dicke M (2004) Three role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271

    Article  PubMed  Google Scholar 

  • De Boer JG, Dicke M (2006) Olfactory learning by predators arthropods. Anim Biol 56:143–155

    Article  Google Scholar 

  • De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    Article  PubMed  CAS  Google Scholar 

  • Dean JM, De Moraes CM (2006) Effects of genetic modification on herbivore-induced volatiles from Maize. J Chem Ecol 32:713–724

    Article  PubMed  CAS  Google Scholar 

  • Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135:1928–1938

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt DC, Lincoln DE (2006) Volatile emission from an odorous in response to herbivory and methyl jasmonate exposure. J Chem Ecol 32:725–743

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14:169–176

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106:13213–13218

    Article  PubMed  CAS  Google Scholar 

  • Delphia CM, Rohr J, Stephenson AG, De Moraes CM, Mescher MC (2009) Effects of genetic variation and inbreeding on volatile production in a field population of horsenettle. Int J Plant Sci 170:12–20

    Article  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:165–175

    Google Scholar 

  • Dicke M, van Loon (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249

    Article  CAS  Google Scholar 

  • Dicke M, Sabelis MW, Takabayashi J (1990) Do plants cry for help? Evidence related to a tritrophic system of predatory mites, spider mites and their host plants. Symp Biol Hung 39:127–134

    Google Scholar 

  • Dicke M, Takabayashi J, Posthumus MA, Schütte C, Krips OE (1998) Plant–phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues in response of predatory mites. Exp Appl Acarol 22:311–333

    Article  CAS  Google Scholar 

  • Dicke M, Gols R, Ludeking D, Posthumus MA (1999) Jasmonic acid and herbivory differentially induce carnivore attracting plant volatiles in Lima bean plants. J Chem Ecol 25:1907–1922

    Article  CAS  Google Scholar 

  • Doares SH, Narváez-vásquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746

    PubMed  CAS  Google Scholar 

  • Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189

    Article  PubMed  CAS  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. BioControl 46:387–400

    Article  Google Scholar 

  • Engelberth J, Koch T, Schüler G, Bachmann N, Rechtenbach J, Boland WI (2001) 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

    Article  PubMed  CAS  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1787

    Article  PubMed  CAS  Google Scholar 

  • Fatouros NE, van Loon JJA, Hordijk KA, Smid HM, Dicke M (2005a) Herbivore-induced plant volatiles mediate in-flight host discrimination by parasitoids. J Chem Ecol 31:2033–2047

    Article  PubMed  CAS  Google Scholar 

  • Fatouros NE, Bukovinszkine’Kiss G, Kalkers LA, Gamborena RS, Dicke M, Hilker M (2005b) Oviposition–induced plant cues: do they arrest Trichogramma wasps during host location? Entomol Exp Appl 115:207–215

    Article  Google Scholar 

  • Felton GW, Korth KL (2000) Trade-offs between pathogen and herbivore resistance. Curr Opin Plant Biol 3:309–314

    Article  PubMed  CAS  Google Scholar 

  • Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9:317–320

    Article  PubMed  CAS  Google Scholar 

  • Friedrich L, Lawton K, Ruess W, Masner P, Specker N, Rella MG, Meier B, Dincher S, Staub T, Uknes S, Métraux JP, Kessmann H, Ryals J (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70

    Article  CAS  Google Scholar 

  • Geervliet JBF, Posthumus MA, Vet LEM, Dicke M (1997) Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J Chem Ecol 23:2935–2954

    Article  CAS  Google Scholar 

  • Gols R, Posthumus MA, 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

    Article  CAS  Google Scholar 

  • Gols R, van Dam M, Raaijmarkers E, Dicke M, Harvey JA (2009) Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps? Oikos 118:733–743

    Article  Google Scholar 

  • Gols R, Bullock JM, Dicke M, Bukovinszky T, Harvey JA (2011) Smelling the wood from the trees: non-linear parasitoid responses to volatile attractants produced by wild and cultivated cabbage. J Chem Ecol 37:795–807

    Article  PubMed  CAS  Google Scholar 

  • Gouinguené SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307

    Article  PubMed  CAS  Google Scholar 

  • Gouinguené SP, Degen T, Turlings TCJ (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9–16

    Article  Google Scholar 

  • Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid–amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717

    Article  PubMed  CAS  Google Scholar 

  • Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals—‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34

    PubMed  Google Scholar 

  • Hatanaka A, Kajiwara T, Sekiya J (1987) Biosynthesis pathway for C6-aldehydes formation from linolenic acid in green leaves. Chem Phys Lipids 44(341):361

    Google Scholar 

  • Heidel AJ, Baldwin IT (2004) Microarray analysis of salicylic acid- and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ 27:1362–1373

    Article  CAS  Google Scholar 

  • Heil M (2004) Induction of two indirect defences benefits Lima bean (Phaseolus lunatus) in nature. J Ecol 92:527–536

    Article  Google Scholar 

  • Heil M (2009) Damaged-self recognition in plant herbivore defense. Trends Plant Sci 14:356–363

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088

    Article  PubMed  CAS  Google Scholar 

  • Hilker M, Meiners T (2002) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, 390 p

    Google Scholar 

  • Hilker M, Kobs C, Varama M, Schrank K (2002) Insect egg deposition induces Pinus to attract egg parasitoids. J Exp Biol 205:455–461

    PubMed  Google Scholar 

  • Hilker M, Stein C, Schroeder R, Varama M, Mumm R (2005) Insect egg deposition induces defense responses in Pinus sylvestris: characterization of the elicitor. J Exp Biol 208:1849–1854

    Article  PubMed  Google Scholar 

  • Himanen SJ, Nerg AM, Nissinen A, Stewart CN, Poopy GM, Holopainen JK (2009) Elevated atmospheric ozone increases concentration of insecticidal Bacillus thuringiensis (Bt) Cry1Ac protein in Bt Brassica napus and reduces feeding of a Bt target herbivore on the non-transgenic parent. Environ Pollut 157:181–185

    Article  PubMed  CAS  Google Scholar 

  • Hoballah MEF, Tamó C, Turlings TCJ (2002) Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: is quality or quantity important? J Chem Ecol 28:951–968

    Article  PubMed  CAS  Google Scholar 

  • Holopainen JK (2004) Multiple functions of inducible plant volatiles. Trends Plant Sci 9:529–533

    Article  PubMed  CAS  Google Scholar 

  • Hopke J, Donath J, Blechert S, 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

    Article  PubMed  CAS  Google Scholar 

  • Houshyani B, Assareh M, Busquets A, Ferrer A, Bouwmeester HJ, Kappers IF (2013) Three-step pathway engineering results in more incidence rate and higher emission of nerolidol and improved attraction of Diadegma semiclausum. Metab Eng 15:88–97

    Article  PubMed  CAS  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  PubMed  CAS  Google Scholar 

  • Ibrahim MA, Nissinen A, Holopainen JK (2005) Response of Plutella xylostella and its parasitoid Cotesia plutellae to volatile compounds. J Chem Ecol 31:1969–1984

    Article  PubMed  CAS  Google Scholar 

  • Ishiwari H, Suzuki T, Maeda T (2007) Essential compounds in herbivore-induced plant volatiles that attract the predatory mite Neoseiulus womersleyi. J Chem Ecol 33:1670–1681

    Article  PubMed  CAS  Google Scholar 

  • James DG (2003a) Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing Chrysopa nigricornis. J Chem Ecol 29:1601–1609

    Article  PubMed  CAS  Google Scholar 

  • James DG (2003b) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ Entomol 32:977–982

    Article  CAS  Google Scholar 

  • James DG (2005) Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J Chem Ecol 31:481–494

    Article  PubMed  CAS  Google Scholar 

  • James DG, Price TS (2004) Field-testing of methyl-salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628

    Article  PubMed  CAS  Google Scholar 

  • Jayaraj J, Rahman M, Wan A, Punja ZK (2009) Enhanced resistance to foliar fungal pathogens in carrot by application of elicitors. Ann Appl Biol 155:71–80

    Article  CAS  Google Scholar 

  • Jolivet P (1998) Interrelationship between insects and plants. CRC, Boca Raton, 309 p

    Google Scholar 

  • Kahl J, Siemens DH, Aerts RJ, Gabler R, Kuhnermann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342

    Article  PubMed  CAS  Google Scholar 

  • Kalberer NM, Turlings TCJ, Rahier M (2001) Attraction of a leaf beetle (Oreina cacaliae) to damaged host plants. J Chem Ecol 27:647–661

    Article  PubMed  CAS  Google Scholar 

  • Kännaste A, Vongvanich N, Borg-Karlson AK (2008) Infestation by Nalepella species induces emissions of α- and β-farnesenes, (−)-linalool and aromatic compounds in Norway spruce clones of different susceptibility to the large pine weevil. Arthropod-Plant Interactions 2:31–41

    Article  Google Scholar 

  • Kaplan I (2012) Trophic complexity and the adaptive value of damage-induced plant volatiles. PLoS Biol 10(11):e1001437

    Article  PubMed  CAS  Google Scholar 

  • Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072

    Article  PubMed  CAS  Google Scholar 

  • Kappers IF, Hoogerbrugge H, Bouwmeester HJ, Dicke M (2011) Variation in herbivory-induced volatiles among cucumber (Cucumis sativus l) varieties has consequences for the attraction of carnivorous natural enemies. J Chem Ecol 37:150–160

    Article  PubMed  CAS  Google Scholar 

  • Kariyat RR, Mauck KE, De Moraes CM, Stephenson AG, Mescher MC (2012) Inbreeding alters volatile signaling phenotypes and influences tri–trophic interactions in horsenettle (Solanum carolinense L). Ecol Lett 15:301–309

    Article  Google Scholar 

  • Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentate and Nicotiana attenuate. Oecologia 148:280–292

    Article  PubMed  Google Scholar 

  • Kessmann H, Staub T, Hofmann C, Maetzke T, Herzog J, Ward E, Uknes S, Ryals J (1994) Induction of systemic acquired disease resistance in plant by chemicals. Annu Rev Phytopathol 32:439–459

    Article  PubMed  CAS  Google Scholar 

  • Khan ZR, Ampong-Nyarko K, Chilishwa P, Hassanali A, Kimani S, Lwande W, Overholt WA, Piccket JA, Smart LE, Wadhams LJ, Woodcock CM (1997) Intercropping increases parasitism of pests. Nature 388:631–632

    Article  CAS  Google Scholar 

  • Khan ZR, James DG, Midega CAO, Piccket JA (2008) Chemical ecology and conservation biological control. Biol Control 45:210–224

    Article  CAS  Google Scholar 

  • Koch T, Krumm T, Jung V, Engelberth J, Boland W (1999) Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiol 121:153–162

    Article  PubMed  CAS  Google Scholar 

  • Köllner TG, Scheene C, Gershenzon J, Degenhardt J (2004) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry 65:1895–1902

    Article  PubMed  CAS  Google Scholar 

  • Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J (2008) 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

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Wang WL, Guo GX, Ji XL (2009) Volatile emission in wheat and parasitism by Aphidius avenae after exogenous application of salivary enzymes of Sitobion avenae. Entomol Exp Appl 130:215–221

    Article  CAS  Google Scholar 

  • Lou YG, Ma B, Cheng JA (2005) Attraction of the parasitoid Anagrus nilaparvatae to rice volatiles induced by the rice brown planthopper Nilaparvata lugens. J Chem Ecol 31:2357–2372

    Article  PubMed  CAS  Google Scholar 

  • Loughrin JH, Manukian A, Heath RR, Tumlinson JH (1995) Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J Chem Ecol 21:1217–1227

    Google Scholar 

  • Lücker J, Bouwmeester HJ, Aharoni A (2007) Metabolic engineering of terpenoid biosynthesis in plants. In: Verpoorte R, Alfermann AW, Johnson TS (eds) Applications of plant metabolic engineering. Springer, Dordrecht, pp 219–236

    Chapter  Google Scholar 

  • Mallinger RE, Hogg DB, Gratton C (2011) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. J Econ Entomol 104:115–124

    Article  PubMed  Google Scholar 

  • Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599

    Article  PubMed  CAS  Google Scholar 

  • Mattiacci L, Dicke M, Posthumus MA (1995) beta-Glucosidase—an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92:2036–2040

    Article  PubMed  CAS  Google Scholar 

  • McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA 94:5473–5477

    Article  PubMed  CAS  Google Scholar 

  • Meiners T, Wäckers F, Wallace JL (2003) Associative learning of complex odours in parasitoid host location. Chem Sens 28:231–236

    Article  CAS  Google Scholar 

  • Meyerowitz EM (1987) Arabidopsis thaliana. Annu Rev Genet 21:93–111

    Article  PubMed  CAS  Google Scholar 

  • Molck G, Pinn H, Wyss U (2000) Manipulation of plant odour preference by learning in the aphid parasitoid Aphelinus abdominalis (Hymenoptera: Aphelinidae). Eur J Entomol 97:533–538

    Google Scholar 

  • Moraes MCB, Laumann R, Pareja M, Sereno FTPS, Michereff MFF, Birkett MA, Pickett JA, Borges M (2009) Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone. Entomol Exp Appl 131:178–188

    Article  CAS  Google Scholar 

  • Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

    Article  PubMed  CAS  Google Scholar 

  • Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628–667

    Article  CAS  Google Scholar 

  • Mumm R, Posthumus MA, Dicke M (2008) Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ 31:575–585

    Article  PubMed  CAS  Google Scholar 

  • Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973

    Article  PubMed  CAS  Google Scholar 

  • Orre GUS, Wratten SD, Jonsson M, Hale RJ (2010) Effects of an herbivore-induced plant volatile on arthropods from three trophic levels in brassicas. Biol Control 53:62–67

    Article  Google Scholar 

  • Orre-Gordon GUS, Wratten SD, Jonsson M, Simpson M, Hale R (2013) ‘Attract and reward’: combining a herbivore-induced plant volatile with floral resource supplementation—multi-trophic level effects. Biol Control 64:106

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ozawa R, Shiojiri K, Sabelis MW, Arimura G, Nishioka T, Takabayashi J (2004) Corn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm. J Chem Ecol 30:1797–1808

    Article  PubMed  CAS  Google Scholar 

  • Paré PW, Tumlinson JH (1997) Induced synthesis of plant volatiles. Nature 385:30–31

    Article  Google Scholar 

  • Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–332

    Article  PubMed  Google Scholar 

  • Paré PW, Farag MA, Krishnamachari V, Zhang H, Ryu CM, Kloepper JW (2005) Elicitors and priming agents initiate plant defense responses. Photosynth Res 85:149–159

    Article  PubMed  CAS  Google Scholar 

  • Parra JRP (2011) Controle Biológico de Pragas no Brasil: histórico, situação atual e perspectivas. Ciência Ambient 43:9–36

    Google Scholar 

  • Peñaflor MFGV, Erb M, Robert CA, Miranda LA, Werneburg AG, Dossi FC, Turlings TC, Bento JMS (2011) Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234:207–215

    Article  PubMed  CAS  Google Scholar 

  • Peñuelas J, Llusià J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404

    Article  PubMed  Google Scholar 

  • Poelman EH, Oduor AMO, Broekgaarden C, Hordijk CA, Jansen JJ, van Loon JJA, van Dam NM, Vet LEM, Dicke M (2009) Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Func Ecol 23:951–962

    Article  Google Scholar 

  • Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE et al (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol 10:e1001435

    Article  PubMed  CAS  Google Scholar 

  • Preston CA, Lewandowski C, Enyedi AJ, Baldwin IT (1999) Tobacco mosaic virus inoculation inhibits wound-induced jasmonic-acid-mediated responses within but not between plants. Planta 209:87–95

    Article  PubMed  CAS  Google Scholar 

  • Rapusas HR, Bottrell DG, Coll M (1996) Intraspecific variation in chemical attraction of rice to insect predators. Biol Control 6:394–400

    Article  Google Scholar 

  • Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    Article  PubMed  CAS  Google Scholar 

  • Redman AM, Cipollini DF, Schultz JC (2001) Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculetum. Oecologia 126:380–385

    Article  Google Scholar 

  • Renou M, Nagnan P, Berthier A, Durier C (1992) Identification of compounds from eggs of Ostrinia nubilalis and Mamestra brassicae having kairomone activity on Trichogramma brassicae. Entomol Exp Appl 63:291–303

    Article  CAS  Google Scholar 

  • Rodríguez A, San Andrés V, Cervera M, Redondo A, Alquézar B, Shimada T, Gadea J, Rodrigo M, Zacarías L, Palou L, López MM, Castañera P, Peña L (2011) The monoterpene limonene in orange peels attracts pests and microorganisms. Plant Signal Behav 6:1820–1823

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rostás M, Ton J, Mani BM, Turlings TCJ (2006) Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naïve parasitoids. J Chem Ecol 32:1987–1909

    Article  CAS  Google Scholar 

  • Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967

    Article  PubMed  CAS  Google Scholar 

  • Ruther J, Furstenau B (2005) Emission of herbivore-induced volatiles in absence of a herbivore—response of Zea mays to green leaf volatiles and terpenoids. J Biosci 60:743–756

    CAS  Google Scholar 

  • Salerno G, De Santis F, Iacovone A, Bin F, Conti E (2013) Short-range cues mediate parasitoid searching behavior on maize: the role of oviposition-induced plant synomones. Biol Control 64:247–254

    Article  Google Scholar 

  • Schmelz EA, Alborn HT, Tumlinson JH (2001) The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays. Planta 214:171–179

    Article  PubMed  CAS  Google Scholar 

  • Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) 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

    Article  PubMed  CAS  Google Scholar 

  • Schuler TH, Poppy GM, Kerry BR, Denholm I (1999a) Potential side effects of insect-resistant transgenic plants on arthropod natural enemies. Trends Biotechnol 17:210–216

    Article  PubMed  CAS  Google Scholar 

  • Schuler TH, Potting RPJ, Denholm I, Poppy GM (1999b) Parasitoid behavior and Bt plants. Nature 400:825

    Article  PubMed  CAS  Google Scholar 

  • Scutareanu P, Drukker B, Bruin J, Posthumus MA, Sabelis MW (1997) Volatiles from Psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. J Chem Ecol 23:2241–2260

    Article  CAS  Google Scholar 

  • Shimoda T, Ozawa R, Arimura G, Takabayashi J, Nishioka T (2002) Olfactory responses of two specialist insect predators of spider mites toward plant volatiles from lima bean leaves induced by jasmonic acid and/or methyl salicylate. Appl Entomol Zoo 37:535–541

    Article  CAS  Google Scholar 

  • Shiojiri K, Ozawa R, Matsui K, Kishimoto K, Kugimiya S, Takabayashi J (2006) Role of the lipoxygenase/lyase pathway of host-food plants in the host searching behavior of the two parasitoid species, Cotesia glomerata and Cotesia plutellae. J Chem Ecol 32:969–979

    Article  PubMed  CAS  Google Scholar 

  • Shobhy IS, Erb M, Sarhan AA, El-Husseini MM, Mandour NS, Turlings TCJ (2012) Less is more: treatment with BTH and laminarin reduces herbivore-induced volatile emissions in maize but increases parasitoid attraction. J Chem Ecol 38:348–360

    Article  CAS  Google Scholar 

  • Signoretti AG, Peñaflor MFGV, Bento JMS (2012) Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), female moths respond to herbivore-induced corn volatiles. Neotrop Entomol 41:22–26

    Article  CAS  Google Scholar 

  • Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI, Orre-Gordon GUS (2011) Attract and reward: combining chemical ecology and habitat manipulation to enhance biological control in field crops. J Appl Ecol 48:580–590

    Article  Google Scholar 

  • Smith JL, De Moraes CM, Mescher MC (2009) Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 65:497–503

    Article  PubMed  CAS  Google Scholar 

  • Snoeren TAL, Mumm R, Poelman EH, Yang Y, Pichersky E, Dicke M (2010) The herbivore-induced plant volatile methyl salicylate negatively affects attraction of the parasitoid Diadegma semiclausum. J Chem Ecol 36:479–489

    Article  PubMed  CAS  Google Scholar 

  • Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol Exp Appl 86:267–279

    Article  CAS  Google Scholar 

  • Stout MJ, Zehnder GW, Baur ME (2002) Potential for the use of elicitors of plant resistance in arthropod management programs. Arch Insect Biochem 51:222–235

    Article  CAS  Google Scholar 

  • Szendrei Z, Rodriguez-Saona C (2010) A meta-analysis of insect pest behavioral manipulation with plant volatiles. Entomol Exp Appl 134:210–210

    Article  Google Scholar 

  • Takabayashi J, Takahashi S, Dicke M, Posthumus MA (1995) Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. J Chem Ecol 21:273–287

    Article  CAS  Google Scholar 

  • Takabayashi J, Sabelis MW, Janssen A, Shiojiri K, van Wijk M (2006) Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecol Res 21:3–8

    Article  Google Scholar 

  • Thaler JS (1999a) Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399:686–688

    Article  CAS  Google Scholar 

  • Thaler JS (1999b) Induced resistance in agricultural crops: effects of jasmonic acid on herbivory and yield in tomato plants. Environ Entomol 28:30–37

    CAS  Google Scholar 

  • Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates stimulates insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781

    Article  CAS  Google Scholar 

  • Thaler JS, Farag MA, Paré PW, Dicke M (2002) Jasmonate-deficient plants have reduced direct and indirect defenses against herbivores. Ecol Lett 5:764–774

    Article  Google Scholar 

  • Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304

    Article  PubMed  CAS  Google Scholar 

  • Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42:757–771

    Article  PubMed  CAS  Google Scholar 

  • Truitt CL, Wei HX, Paré PW (2004) A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. Plant Cell 16:523–532

    Article  PubMed  CAS  Google Scholar 

  • Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odors to enhance the control of agricultural pests. Curr Opin Plant Biol 9:421–427

    Article  PubMed  Google Scholar 

  • Turlings TCJ, Wäckers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 21–74

    Chapter  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  PubMed  CAS  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Heath RR, Proveaux AT, Doolitle RE (1991) Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J Chem Ecol 17:2235–2251

    Article  CAS  Google Scholar 

  • Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152

    Article  CAS  Google Scholar 

  • van den Boom CEM, Van Beek TA, Posthumus MA, de Groot A, Dicke M (2004) Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J Chem Ecol 30:69–89

    Article  PubMed  Google Scholar 

  • van Emden HF (1995) Host plant–aphidophaga interactions. Agric Ecosyst Environ 52:3–11

    Article  Google Scholar 

  • van Poecke RMP, Dicke M (2002) Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J Exp Bot 53:1793–1799

    Article  PubMed  CAS  Google Scholar 

  • van Poecke RMP, Posthumus MA, Dicke M (2001) 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

    Article  PubMed  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vet LEM, Groenewold AW (1990) Semiochemicals and learning in parasitoids. J Chem Ecol 16:3119–3135

    Article  CAS  Google Scholar 

  • Vick BA, Zimmerman DC (1984) Biosynthesis of jasmonic acid by several plant-species. Plant Physiol 75:458–461

    Article  PubMed  CAS  Google Scholar 

  • Vinson SB (1992) Can semiochemicals alter the use of parasites in IPM programs? Pesq Agrop Brasileira 27:301–313

    Google Scholar 

  • von Mérey GE, Veyrat N, Mahuku G, López-Valdez R, Turlings TCJ, D’Alessandro M (2011) Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects. Phytochemistry 72:1838–1847

    Article  CAS  Google Scholar 

  • von Mérey GE, Veyrat N, de Lange E, Degen T, Mahuku G, López-Valdez R, Turlings TCJ, D’Alessandro M (2012) Minor effects of two elicitors of insect and pathogen resistance on the volatile emission and the biological control of Spodoptera frugiperda in maize fields. Biol Control 60:7–15

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant response to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

  • Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato—role of jasmonic acid. J Plant Physiol 163:297–306

    Article  PubMed  CAS  Google Scholar 

  • Wei JN, Kang L (2006) Electrophysiological and behavioral responses of a parasitic wasp to plant volatiles induced by two leaf miner species. Chem Sens 31:467–477

    Article  CAS  Google Scholar 

  • Wu JQ, Baldwin IT (2009) Herbivory-induced signaling in plants: perception and action. Plant Cell Environ 32:1161–1174

    Article  PubMed  CAS  Google Scholar 

  • Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappell J (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nature 24:1441–1447

    Article  CAS  Google Scholar 

  • Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L, Hu L, Li J, Han X, Zhang T, Lu J, Zhang G, Lou Y (2012) Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett 15:1130–1139

    Article  PubMed  CAS  Google Scholar 

  • Yong-gen L, Jia-an C (2001) Role of rice volatiles in the foraging behavior of Cyrtorhinus lividipennis Reuter. Entomol Sin 8:240–250

    Google Scholar 

  • Yu H, Zhang Y, Wu K, Gao XW, Guo YY (2008) Field-testing of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Environ Entomol 37:1410–1415

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful for Elvira De Lange for useful revisions in the early version of this paper, Patricia Milano for the plant drawing, and Arodí Prado Favaris for helping on figure editing. We thank INCT Semioquímicos na Agricultura for financial support. MFGVP is sponsored by FAPESP (Proc 2012/12252-1).

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Peñaflor, M.F.G.V., Bento, J.M.S. Herbivore-Induced Plant Volatiles to Enhance Biological Control in Agriculture. Neotrop Entomol 42, 331–343 (2013). https://doi.org/10.1007/s13744-013-0147-z

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