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The Impact of Induced Plant Volatiles on Plant-Arthropod Interactions

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Arthropod-Plant Interactions

Abstract

Plants release volatile organic compounds from their vegetative tissues into their environment during most of their life cycle. The functions of these volatiles are diverse and not always known but some of these volatiles repel foraging herbivores while others, in turn, attract them and are feeding stimuli. Upon herbivory the amount of volatiles increases dramatically while, simultaneously, also the composition of the blend changes thereby enhancing the attractiveness of the plant to foraging natural enemies and in some cases increasing repellency to herbivores. Hence, herbivore-induced volatiles promote a natural form of biological pest control referred to as “indirect plant defense” and it has often been suggested that this phenomenon could be exploited to enhance crop protection. Here we will introduce the concept of indirect plant defense via volatiles and via other means and outline the current state of knowledge to the extent in which it contributes to protecting a plant to maximize its fitness under natural conditions in an evolutionary and ecological context. Moreover we will summarize the different approaches that have been undertaken to manipulate indirect defenses, either via application of synthetic volatiles or via transgenic manipulation of plant-volatile production, to control the movements of foraging arthropods to improve biological control. Finally, we will discuss to which extent IPM can be improved or even be disrupted via manipulation of plant volatiles.

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References

  • Abbott E, Hall D, Hamberger B, Bohlmann J (2010) Laser microdissection of conifer stem tissues: isolation and analysis of high quality RNA, terpene synthase enzyme activity and terpenoid metabolites from resin ducts and cambial zone tissue of white spruce (Picea glauca). BMC Plant Biol 10:106

    Article  PubMed  CAS  Google Scholar 

  • Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7(8):601–611

    Article  PubMed  CAS  Google Scholar 

  • Abramson CI, Giray T, Mixson TA, Nolf SL, Wells H, Kence A (2010) Proboscis conditioning experiments with honeybees, Apis mellifera caucasica, with butyric acid and DEET mixture as conditioned and unconditioned stimuli. J Insect Sci 10:1–17

    Article  Google Scholar 

  • Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FW, 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 

  • Alba JM, Glas JJ, Schimmel BCJ, Kant MR (2011) Avoidance and suppression of plant defenses by herbivores and pathogens. J Plant Interact 6(2):1–7

    Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretions. Science 276:945–949

    Article  CAS  Google Scholar 

  • Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz EA, Teal PEA (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl Acad Sci U S A 104:12976–12981

    Article  PubMed  CAS  Google Scholar 

  • Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99(1):26–35

    Article  CAS  Google Scholar 

  • Allison JD, Hare JD (2009) Learned and naive natural enemy responses and the interpretation of volatile organic compounds as cues or signals. New Phytol 184(4):768–782

    Article  PubMed  CAS  Google Scholar 

  • Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329(5995):1075–1078

    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 salicilate emission in tomato. Plant Physiol 135:2025–2037

    Article  PubMed  CAS  Google Scholar 

  • Ament K, Krasikov V, Allmann S, Rep M, Takken FL, Schuurink RC (2010) Methyl salicylate production in tomato affects biotic interactions. Plant J 62:124–134

    Article  PubMed  CAS  Google Scholar 

  • Andersson J, Borg-Karlson AK, Wiklund C (2003) Antiaphrodisiacs in pierid butterflies: a theme with variation! J Chem Ecol 29:1489–1499

    Article  PubMed  CAS  Google Scholar 

  • Anten NPR, Pierik R (2010) Moving resources away from the herbivore: regulation and adaptive significance. New Phytol 188(3):644–645

    Article  Google Scholar 

  • Arigoni D, Sagner S, Latzel C, Eisenreich W, Bacher A, Zenk MH (1997) Terpenoid biosynthesis from 1-deoxy-D-xylulose in higher plants by intramolecular skeletal rearrangement. Proc Natl Acad Sci U S A 94:10600–10605

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, Takabayashi J (2002) Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J 29:87–98

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)-germacrene D synthase, PtdTPS1. Plant J 37(4):603–616

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 1734(2):91–111

    Google Scholar 

  • Attaran E, Zeier TE, Griebel T, Zeier J (2009) Methyl salicylate production and jasmonate signalling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21:954–971

    Article  PubMed  CAS  Google Scholar 

  • Babst BA, Ferrieri RA, Thorpe MR, Orians CM (2008) Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 128(1):117–125

    Article  CAS  Google Scholar 

  • Baker TC, Quero C, Ochieng SA, Vickers NJ (2006) Inheritance of olfactory preferences II. Olfactory receptor neuron responses from Heliothis subflexa x Hetliothis virescens hybrid male moths. Brain Behav Evol 68(2):75–89

    Article  PubMed  CAS  Google Scholar 

  • Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: “talking trees” in the genomics era. Science 311(5762):812–815

    Article  PubMed  CAS  Google Scholar 

  • Bate NJ, Rothstein SJ (1998) C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16(5):561–569

    Article  PubMed  CAS  Google Scholar 

  • Bede JC, Musser RO, Felton GW, Korth KL (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol Biol 60:519–531

    Article  PubMed  CAS  Google Scholar 

  • Belles JM, Garro R, Pallas V, Fayos J, Rodrigo I, Conejero V (2006) Accumulation of gentisic acid as associated with systemic infections but not with the hypersensitive response in plant-pathogen interactions. Planta 223(3):500–511

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum MR, Zangerl AR (1998) Chemical phenotype matching between a plant and its insect herbivore. Proc Natl Acad Sci U S A 95:13743–13748

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum MR, Zangerl AR (2008) Facing the future of plant-insect interaction research: le retour à la “raison d’être”. Plant Physiol 146:804–811

    Article  PubMed  CAS  Google Scholar 

  • Berg BG, Mustaparta H (1995) The significance of major pheromone components and interspecific signals as expressed by receptor neurons in the oriental tobacco budworm moth, Helicoverpa assulta. J Comp Physiol A-Sens Neural Behav Physiol 177(6):683–694

    CAS  Google Scholar 

  • Berry J, Krause WC, Davis RL (2008) Olfactory memory traces in Drosophila essence of memory. In: Sossin WS, Lacaille J-C, Castelucci VF, Bellville S (eds) Progress in brain research: the essence of memory, vol 169. Elsevier, Amsterdam, pp 293–304

    Chapter  Google Scholar 

  • Bjostad LB, Hibbard BE (1992) 6-methoxy-2-benzoxazolinone – a semiochemical for host location by western corn-rootworm larvae. J Chem Ecol 18(7):931–944

    Article  CAS  Google Scholar 

  • Bleeker PM, Diergaarde PJ, Ament K, Guerra J, Weidner M, Schutz S, de Both MTJ, Haring MA, Schuurink RC (2009) The role of specific tomato volatiles in tomato whitefly interaction. Plant Physiol 151(2):925–935

    Article  PubMed  CAS  Google Scholar 

  • Blight MM, Pickett JA, Wadhams LJ, Woodcock CM (1995) Antennal perception of oilseed rape, Brassica napus (Brassicaceae), volatiles by the cabbage seed weevil Ceutorhynchus assimilis (Coleoptera: Curculionidae). J Chem Ecol 21(11):1649–1664

    Article  CAS  Google Scholar 

  • Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci U S A 95:4126–4133

    Article  PubMed  CAS  Google Scholar 

  • Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet 6(11):e1001216

    Article  PubMed  CAS  Google Scholar 

  • Bouarab K, Melton R, Peart J, Baulcombe D, Osbourn A (2002) A saponin-detoxifying enzyme mediates suppression of plant defences. Nature 418(6900):889–892

    Article  PubMed  CAS  Google Scholar 

  • Bown AW, Hall DE, MacGregor KB (2002) Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiol 129:1430–1434

    Article  PubMed  CAS  Google Scholar 

  • Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10(6):269–274

    Article  PubMed  CAS  Google Scholar 

  • Bruessow F, Gouhier-Darimont C, Buchala A, Metraux JP, Reymond P (2010) Insect eggs suppress plant defence against chewing herbivores. Plant J 62:876–885

    Article  PubMed  CAS  Google Scholar 

  • Carlini CR, Grossi-de-Sa MF (2002) Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 90(11):1515–1539

    Article  Google Scholar 

  • Catinot J, Buchala A, Abou-Mansour E, Métraux J-P (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett 582:473–478

    Article  PubMed  CAS  Google Scholar 

  • Chapman RF, Bernays EA (1989) Insect behavior at the leaf surface and learning as aspects of host plant-selection. Experientia 45(3):215–222

    Article  Google Scholar 

  • Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, Garciá-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  PubMed  CAS  Google Scholar 

  • Connolly JD, Hill RA (1991) Dictionary of terpenoids. Chapman and Hall, London

    Google Scholar 

  • Cosse AA, Todd JL, Baker TC (1998) Neurons discovered in male Helicoverpa zea antennae that correlate with pheromone-mediated attraction and interspecific antagonism. J Comp Physiol A-Sens Neural Behav Physiol 182(5):585–594

    Article  CAS  Google Scholar 

  • Cosse AA, Bartelt RJ, Zilkowski BW, Bean DW, Andress ER (2006) Behaviorally active green leaf volatiles for monitoring the leaf beetle, Diorhabda elongata, a biocontrol agent of saltcedar, Tamarix spp. J Chem Ecol 32(12):2695–2708

    Google Scholar 

  • Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12(4):564–582

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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(12):2733–2748

    Article  PubMed  CAS  Google Scholar 

  • D’Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J (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

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411(6839):826–833

    Article  PubMed  CAS  Google Scholar 

  • De Boer JG, Dicke M (2004a) Experience with methyl salicylate affects behavioural responses of a predatory mite to blends of herbivore-induced plant volatiles. Entomol Exp Appl 110(2):181–189

    Article  Google Scholar 

  • De Boer JG, Dicke M (2004b) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30(2):255–271

    Article  PubMed  Google Scholar 

  • De Boer JG, Dicke M (2006) Olfactory learning by predatory arthropods. Anim Biol 56(2):143–155

    Article  Google Scholar 

  • De Boer JG, Snoeren TAL, Dicke M (2005) Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim Behav 69:869–879

    Article  Google Scholar 

  • De Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34(7):882–897

    Article  PubMed  CAS  Google Scholar 

  • De Bruyne M, Clyne PJ, Carlson JR (1999) Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19(11):4520–4532

    PubMed  Google Scholar 

  • De Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30(2):537–552

    Article  PubMed  Google Scholar 

  • De Moraes CM, Mescher MC (2004) Biochemical crypsis in the avoidance of natural enemies by an insect herbivore. Proc Natl Acad Sci U S A 101:8993–8997

    Article  PubMed  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(6828):577–580

    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 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(2):169–176

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt DC, Refi-Hind S, Stratmann JW, Lincoln DE (2010) Systemin and jasmonic acid regulate constitutive and herbivore-induced systemic volatile emissions in tomato, Solanum lycopersicum. Phytochemistry 71(17–18):2024–2037

    Article  PubMed  CAS  Google Scholar 

  • Dejong R, Kaiser L (1991) Odor learning by leptopilina-boulardi, a specialist parasitoid (Hymenoptera, eucoilidae). J Insect Behav 4(6):743–750

    Article  Google Scholar 

  • Delaney KJ (2008) Injured and uninjured leaf photosynthetic responses after mechanical injury on Nerium oleander leaves, and Danaus plexippus herbivory on Asclepias curassavica leaves. Plant Ecol 199(2):187–200

    Article  Google Scholar 

  • Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012

    Article  PubMed  CAS  Google Scholar 

  • Diezel C, von Dahl CC, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586

    Article  PubMed  CAS  Google Scholar 

  • Dish A, Hennerlin A, Bach TJ, Rohmer M (1998) Mevalonate-derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chain in tobacco BY-2 cells. Biochem J 331:615–621

    Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ (2002) The phenylpropanoid pathway and plant defence – a genomics perspective. Mol Plant Pathol 3(5):371–390

    Article  PubMed  CAS  Google Scholar 

  • Doss RP, Proebsting WM, Potter SW, Clement SL (1995) Response of Np mutant of pea (Pisum sativum L.) to pea weevil (Bruchus pisorum L.) oviposition and extracts. J Chem Ecol 21:97–106

    Article  CAS  Google Scholar 

  • Douglas AE (1993) The nutritional quality of phloem sap utilized by natural aphid populations. Ecol Entomol 18(1):31–38

    Article  Google Scholar 

  • Drukker B, Scutareanu P, Sabelis MW (1995) Do anthocorid predators respond to synomones from psylla-infested pear trees under field conditions. Entomol Exp Appl 77(2):193–203

    Google Scholar 

  • Drukker B, Bruin J, Jacobs G, Kroon A, Sabelis MW (2000a) How predatory mites learn to cope with variability in volatile plant signals in the environment of their herbivorous prey. Exp Appl Acarol 24(12):881–895

    Article  PubMed  CAS  Google Scholar 

  • Drukker B, Bruin J, Sabelis MW (2000b) Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol Entomol 25(3):260–265

    Article  CAS  Google Scholar 

  • Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122(3):627–633

    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 

  • Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem Physiol 32(1):3–37

    Article  CAS  Google Scholar 

  • Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160

    Article  PubMed  CAS  Google Scholar 

  • Dussourd DE, Denno RF (1991) Deactivation of plant defense – correspondence between insect behavior and secretory canal architecture. Ecology 72(4):1383–1396

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eigenbrode SD, Espelie KE (1995) Effects of plant epicuticular lipids on insect herbivore. Annu Rev Entomol 40:171–194

    Article  Google Scholar 

  • El Oirdi M, El Rahman TA, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23(6):2405–2421

    Article  PubMed  CAS  Google Scholar 

  • Ellinger D, Stingl N, Kubigsteltig II, Bals T, Juenger M, Pollmann S, Berger S, Schuenemann D, Mueller MJ (2010) DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 lipases are not essential for wound- and pathogen-induced jasmonate biosynthesis: redundant lipases contribute to jasmonate formation. Plant Physiol 153(1):114–127

    Article  PubMed  CAS  Google Scholar 

  • El-Sayed AM (2010) The Pherobase: database of insect pheromones and semiochemicals. http://www.pherobase.com

  • Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14(1):3–8

    Article  PubMed  CAS  Google Scholar 

  • Fahn A (1988) Secretory-tissues in vascular plants. New Phytol 108(3):229–257

    Article  Google Scholar 

  • Farag MA, Pare PW (2002) C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61(2002):545–554

    Article  PubMed  CAS  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase-inhibitors in plant-leaves. Proc Natl Acad Sci U S A 87(19):7713–7716

    Article  PubMed  CAS  Google Scholar 

  • Fatouros NE, Broekgaarden C, Bukovinszkine’Kiss G, van Loon JJA, Mumm R, Huigens ME, Dicke M, Hilker M (2008) Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense. Proc Natl Acad Sci U S A 105:10033–10038

    Article  PubMed  CAS  Google Scholar 

  • Felton GW, Tumlinson JH (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11:457–463

    Article  PubMed  CAS  Google Scholar 

  • Feyereisen R (1995) Molecular biology of insecticide resistance. Toxicol Lett 82:83–90

    Article  PubMed  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Ecol 5:344–350

    Article  CAS  Google Scholar 

  • Friedman AR, Baker BJ (2007) The evolution of resistance genes in multi-protein plant resistance systems. Curr Opin Genet Dev 17:493–499

    Article  PubMed  CAS  Google Scholar 

  • Frost CJ, Appel M, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10(6):490–498

    Article  PubMed  Google Scholar 

  • Galizia CG, Munch D, Strauch M, Nissler A, Ma SW (2010) Integrating heterogeneous odor response data into a common response model: a door to the complete olfactome. Chem Senses 35(7):551–563

    Article  PubMed  CAS  Google Scholar 

  • Gaquerel E, Weinhold A, Baldwin IT (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 Physiol 149(3):1408–1423

    Article  PubMed  CAS  Google Scholar 

  • Gfeller A, Dubugnon L, Liechti R, Farmer EE (2010) Jasmonate biochemical pathway. Sci Signal 3(109):cm3

    Article  PubMed  CAS  Google Scholar 

  • Giordanengo P, Brunissen L, Rusterucci C, Vincent C, van Bel A, Dinant S, Girousse C, Faucher M, Bonnemain JL (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. C R Biol 333(6–7):516–523

    Article  PubMed  Google Scholar 

  • Glinwood RT, Pettersson J (2000) Change in response of Rhopalosiphum padi spring migrants to the repellent winter host component methyl salicylate. Entomol Exp Appl 94(3):325–330

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gomez S, Ferrieri RA, Schueller M (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol 188(3):835–844

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez A, Rossini C, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A 96(10):5570–5574

    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(3):1296–1307

    Article  PubMed  CAS  Google Scholar 

  • Gouinguené S, 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 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    Article  PubMed  CAS  Google Scholar 

  • Grant AJ, Wigton BE, Aghajanian JG, Oconnell RJ (1995) Electrophysiological responses of receptor neurons in mosquito maxillary palp sensilla to carbon-dioxide. J Comp Physiol A-Sens Neural Behav Physiol 177(4):389–396

    CAS  Google Scholar 

  • Gross N, Wasternack C, Kock M (2004) Wound-induced RNaseLE expression is jasmonate and systemin independent and occurs only locally in tomato (Lycopersicon esculentum cv. Lukullus). Sour: Phytochem 65(10):1343–1350

    Article  CAS  Google Scholar 

  • Guerin PM, Stadler E, Buser HR (1983) Identification of host plant attractants for the carrot fly, psila-rosae. J Chem Ecol 9(7):843–861

    Article  CAS  Google Scholar 

  • Guo S, Kim J (2007) Molecular evolution of Drosophila odorant receptor genes. Mol Biol Evol 24(5):1198–1207

    Article  PubMed  CAS  Google Scholar 

  • Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807

    Article  PubMed  CAS  Google Scholar 

  • Halitschke R, Kessler A, Kahl J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124:408–417

    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, Ziegler J, Keinanen M, Baldwin IT (2004) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. Plant J 40:35–46

    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(1):24–34

    PubMed  Google Scholar 

  • Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125(1):143–160

    Article  PubMed  CAS  Google Scholar 

  • Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4(1):86–95

    Article  Google Scholar 

  • Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8(4):157–178

    Article  Google Scholar 

  • Hao PY, Liu CX, Wang YY, Chen RZ, Tang M, Du B, Zhu LL, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: An important mechanism for host resistance. Plant Physiol 146(4):1810–1820

    Google Scholar 

  • Harborne JB (1991) Ecological chemistry and biochemistry of plant terpenoids. Clarendon, Oxford, pp 399–426

    Google Scholar 

  • Hardie J, Isaacs R, Pickett JA, Wadhams LJ, Woodcock CM (1994) Methyl salicylate and (−)-(1R,5S)-myrtenal are plant-derived repellents for black bean aphid, Aphis fabae scop (Homoptera, Aphididae). J Chem Ecol 20(11):2847–2855

    Article  CAS  Google Scholar 

  • Harmel N, Létocart E, Cherqui A, Giordanengo P, Mazzucchelli G, Guillonneau F, De Pauw E, Haubruge E, Francis F (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Mol Biol 17(2):165–174

    Article  PubMed  CAS  Google Scholar 

  • Hartmann T, Theuring C, Beuerle T, Klewer N, Schulz S, Singer MS, Bernays EA (2005) Specific recognition, detoxification and metabolism of pyrrolizidine alkaloids by the polyphagous arctiid Estigmene acrea. Insect Biochem Mol Biol 35:391–411

    Article  PubMed  CAS  Google Scholar 

  • Hassan S, Behm CA, Mathesius U (2010) Effectors of plant parasitic nematodes that re-program root cell development. Funct Plant Biol 37(10):933–942

    Article  CAS  Google Scholar 

  • Hatanaka A (1993) The biogeneration of green odor by green leaves. Phytochemistry 34:1201–1218

    Article  CAS  Google Scholar 

  • Heinbockel T, Kaissling KE (1996) Variability of olfactory receptor neuron responses of female silkmoths (Bombyx mori L) to benzoic acid and (+/−)-linalool. J Insect Physiol 42(6):565–578

    Article  CAS  Google Scholar 

  • Hematy K, Cherk C, Somerville S (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12(4):406–413

    Article  PubMed  CAS  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Higginson AD, Delf J, Ruxton GD, Speed MP (2011) Growth and reproductive costs of larval defence in the aposematic lepidopteran Pieris brassicae. J Anim Ecol 80:384–392

    Article  PubMed  Google Scholar 

  • Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Hilker M, Stein C, Schro’Der R, Varama M, Mumm R (2005) Insect egg deposition induced defence response in Pinus sylvestris. Characterization of the elicitor. J Exp Biol 208:1849–1854

    Article  PubMed  Google Scholar 

  • Hoballah MEF, Turlings TCJ (2001) Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol Ecol Res 3:553–565

    Google Scholar 

  • Hoballah ME, Kollner TG, Degenhardt J, Turlings TCJ (2004) Costs of induced volatile production in maize. Oikos 105(1):168–180

    Article  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 

  • Hopkins RJ, van Dam N, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83

    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 

  • Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8(11):2067–2077

    Article  PubMed  CAS  Google Scholar 

  • Hoy CW, Head GP, Hall FR (1998) Spatial heterogeneity and insect adaptation to toxins. Annu Rev Entomol 43:571–594

    Article  PubMed  CAS  Google Scholar 

  • Hyun Y, Choi S, Hwang HJ, Yu J, Nam SJ, Ko J, Park JY, Seo YS, Kim EY, Ryu SB, Kim WT, Lee YH, Kang H, Lee I (2008) Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Dev Cell 14(2):183–192

    Article  PubMed  CAS  Google Scholar 

  • Ito S, Eto T, Tanaka S, Yamauchi N, Takahara H, Ikeda T (2004) Tomatidine and lycotetraose, hydrolysis products of alpha-tomatine by Fusarium oxysporum tomatinase, suppress induced defense responses in tomato cells. FEBS Lett 571(1–3):31–34

    Article  PubMed  CAS  Google Scholar 

  • Ito I, Ong RCY, Raman B, Stopfer M (2008) Sparse odor representation and olfactory learning. Nat Neurosci 11(10):1177–1184

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • James DG (2006) Methyl salicylate is a field attractant for the goldeneyed lacewing, Chrysopa oculata. Biocontrol Sci Technol 16(1):107–110

    Article  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 

  • Jansen VAA, van Baalen M (2006) Altruism through beard chromodynamics. Nature 440:663–666

    Article  PubMed  CAS  Google Scholar 

  • Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ (1995) Adaptation of spodoptera-exigua larvae to plant proteinase-inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc Natl Acad Sci U S A 92(17):8041–8045

    Article  PubMed  CAS  Google Scholar 

  • Jørgensen K, Vinther-Morant A, Morant M, Jensen NB, Olsen CE, Kannangara R, Motawia MS, Lindberg-Møller B, Bak S (2011) Biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in cassava: isolation, biochemical characterization, and expression pattern of CYP71E7, the oxime-metabolizing cytochrome P450 enzyme. Plant Physiol 155(1):282–292

    Article  PubMed  CAS  Google Scholar 

  • Judd GJR, Borden JH (1989) Distant olfactory response of the onion fly, delia-antiqua, to host-plant odor in the field. Physiol Entomol 14(4):429–441

    Article  Google Scholar 

  • Kahl J, Siemens DH, Aerts RJ, Gäbler R, Kühnemann 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 

  • Kaloshian I, Walling LL (2005) Hemipterans as plant pathogens. Annu Rev Phytopathol 43:491–521

    Article  PubMed  CAS  Google Scholar 

  • Kang JH, Liu GH, Shi F, Jones AD, Beaudry RM, Howe GA (2010) The tomato odorless-2 mutant is defective in trichome-based production of diverse specialized metabolites and broad-spectrum resistance to insect herbivores. Plant Physiol 154(1):262–272

    Article  PubMed  CAS  Google Scholar 

  • Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135(1):483–495

    Article  PubMed  CAS  Google Scholar 

  • Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc R Soc B: Biol Sci 275:443–452

    Article  CAS  Google Scholar 

  • Kant MR, Bleeker PM, Van Wijk M, Schuurink RC, Haring MA (2009) Plant volatiles in defence. In: Plant innate immunity. Advances in Botanical Research, Vol. 51, Burlington: Academic Press, pp 613–666

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Katsir L, Chung HS, Koo AJK, Howe GA (2008a) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435

    Article  PubMed  CAS  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008b) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105:7100–7105

    Article  PubMed  CAS  Google Scholar 

  • Kawecki TJ (2010) Evolutionary ecology of learning: insights from fruit flies. Popul Ecol 52(1):15–25

    Google Scholar 

  • Kazana E, Pope TW, Tibbles L, Bridges M, Pickett JA, Bones AM, Powell G, Rossiter JT (2007) The cabbage aphid: a walking mustard oil bomb. Proc R Soc B: Biol Sci 274:2271–2277

    Article  CAS  Google Scholar 

  • Kellog BA, Poulter CD (1997) Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol 1:570–578

    Article  Google Scholar 

  • Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143:849–865

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291(5511):2141–2144

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2004) Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J 38(4):639–649

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305(5684):665–668

    Article  PubMed  CAS  Google Scholar 

  • Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321(5893):1200–1202

    Article  PubMed  CAS  Google Scholar 

  • Khan ZR, James DG, Midega CAO, Pickett JA (2008) Chemical ecology and conservation biological control. Biol Control 45(2):210–224

    Article  CAS  Google Scholar 

  • Kim KC, Fan BF, Chen ZX (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 142:1180–1192

    Article  PubMed  CAS  Google Scholar 

  • King JR, Christensen TA, Hildebrand JG (2000) Response characteristics of an identified, sexually dimorphic olfactory glomerulus. J Neurosci 20(6):2391–2399

    PubMed  CAS  Google Scholar 

  • Kleiner KW, Raffa KF, Dickson RE (1999) Partitioning of C-14-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia 119(3):408–418

    Article  Google Scholar 

  • Knight AL, Light DM (2001) Attractants from Bartlett pear for codling moth, Cydia pomonella (L.), larvae. Naturwissenschaften 88(8):339–342

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Yamamura N, Sabelis MW (2006) Evolution of talking plants in a tritrophic context: conditions for uninfested plants to attract predators prior to herbivore attack. J Theor Biol 243:361–374

    Article  PubMed  Google Scholar 

  • Kollner TG, Lenk C, Zhao N, Seidl-Adams I, Gershenzon J, Chen F, Degenhardt J (2010) Herbivore-induced SABATH methyltransferases of maize that methylate anthranilic acid using S-Adenosyl-L-Methionine. Plant Physiol 153(4):1795–1807

    Article  PubMed  CAS  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146(3):839–844

    Google Scholar 

  • Krasnoff SB, Dussourd DE (1989) Dihydropyrrolizine attractants for arctiid moths that visit plants containing pyrrolizidine alkaloids. J Chem Ecol 15(1):47–60

    Article  CAS  Google Scholar 

  • Krips OE, Willems PEL, Gols R, Posthumus MA, Dicke M (1999) The response of Phytoseiulus persimilis to spider mite-induced volatiles from Gerbera: influence of starvation and experience. J Chem Ecol 25(12):2623–2641

    Article  CAS  Google Scholar 

  • Krips OE, Willems PEL, Gols R, Posthumus MA, Gort G, Dicke M (2001) 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 27:1355–1372

    Article  PubMed  CAS  Google Scholar 

  • Kunert G, Reinhold C, Gershenzon J (2010) Constitutive emission of the aphid alarm pheromone, (E)-beta-farnesene, from plants does not serve as a direct defense against aphids. BMC Ecol 10:23

    Article  PubMed  CAS  Google Scholar 

  • Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu Rev Ecol Syst 28:153–193

    Article  Google Scholar 

  • Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5(4):305–315

    Article  PubMed  CAS  Google Scholar 

  • Lange BM, Wildung MR, Stauber EJ, Sanchez C, Pouchnik D, Croteau R (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc Natl Acad Sci U S A 97:2934–2939

    Article  PubMed  CAS  Google Scholar 

  • Langenheim JH (1994) Higher-plant terpenoids – a phytocentric overview of their ecological roles. J Chem Ecol 20(6):1223–1280

    Article  CAS  Google Scholar 

  • Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HDI (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci 24:263–297

    Article  PubMed  CAS  Google Scholar 

  • Lawrence SD, Novak NG, Blackburn MB (2007) Inhibition of proteinase inhibitor transcripts by Leptinotarsa decemlineata regurgitant in Solanum lycopersicum. J Chem Ecol 33:1041–1048

    Article  PubMed  CAS  Google Scholar 

  • Lawrence SD, Novak NG, Ju CJT, Cooke JEK (2008) Potato, Solanum tuberosum, defense against Colorado potato beetle, Leptinotarsa decemlineata (Say): microarray gene expression profiling of potato by Colorado potato beetle regurgitant treatment of wounded leaves. J Chem Ecol 34:1013–1025

    Article  PubMed  CAS  Google Scholar 

  • Lee JC (2010) Effect of methyl salicylate-based lures on beneficial and pest arthropods in strawberry. Environ Entomol 39(2):653–660

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Du YJ, Koornneef A, Proietti S, Korbes AP, Memelink J, Pieterse CMJ, Ritsema T (2010a) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant Microbe Interact 23(2):187–197

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SCM, Ritsema T, Pieterse CMJ (2010b) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232(6):1423–1432

    Article  PubMed  CAS  Google Scholar 

  • Lerdau M, Gershenzon J (1997) Allocation theory and chemical defense. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Academic, San Diego, pp 265–291

    Chapter  Google Scholar 

  • Li CY, Williams MM, Loh YT, Lee GI, Howe GA (2002a) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130(1):494–503

    Article  PubMed  CAS  Google Scholar 

  • Li X, Schuler MA, Berenbaum MR (2002b) Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419:712–715

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143

    Article  PubMed  CAS  Google Scholar 

  • Loivamaki M, Mumm R, Dicke M, Schnitzler JP (2008) Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc Natl Acad Sci U S A 105:17430–17435

    Article  PubMed  Google Scholar 

  • Loughrin JH, Manukian A, Heath RR, Turlings TCJ, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids herbivore-injured cotton plants. Proc Natl Acad Sci U S A 91(25):11836–11840

    Article  PubMed  CAS  Google Scholar 

  • Maeda H, Shasany AK, Schnepp J, Orlova I, Taguchi G, Cooper BR, Rhodes D, Pichersky E, Dudareva N (2010) RNAi suppression of arogenate dehydratase1 reveals that phenylalanine is synthesized predominantly via the arogenate pathway in Petunia petals. Plant Cell 22(3):832–849

    Article  PubMed  CAS  Google Scholar 

  • Maes K, Debergh PC (2003) Volatiles emitted from in vitro grown tomato shoots during abiotic and biotic stress. Plant Cell Tissue Organ Cult 75:73–78

    Article  CAS  Google Scholar 

  • Maffei ME (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. S Afr J Bot 76(4):612–631

    Article  CAS  Google Scholar 

  • Markovich NA, Kononova GL (2003) Lytic enzymes of Trichoderma and their role in plant defense from fungal diseases: a review. Appl Biochem Microbiol 39(4):341–351

    Article  CAS  Google Scholar 

  • Matsui K, Kurishita S, Hisamitsu A, Kajiwara T (2000) A lipid-hydrolysing activity involved in hexenal formation. Biochem Soc Trans 28:857–860

    Article  PubMed  CAS  Google Scholar 

  • Matsushima R, Ozawa R, Uefune M, Gotoh T, Takabayashi J (2006) Intraspecific variation in the Kanzawa spider mite differentially affects induced defensive response in lima bean plants. J Chem Ecol 32:2501–2512

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203(4):430–435

    Article  CAS  Google Scholar 

  • Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8(2):53–62

    Article  PubMed  CAS  Google Scholar 

  • Metraux JP, Jackson RW, Schnettler E, Goldbach RW (2009) Plant pathogens as suppressors of host defense. In: Plant innate immunity. Advances in Botanical Research, Vol. 51, Burlington: Academic Press, pp 39–89

    Google Scholar 

  • Miles PW (1972) The saliva of Hemiptera. Adv Insect Physiol 9:183–240

    Article  CAS  Google Scholar 

  • Miles PW (1999) Aphid saliva. Biol Rev 74(1):41–85

    Article  Google Scholar 

  • Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylides C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant J 53:197–213

    Article  PubMed  CAS  Google Scholar 

  • Mithöfer A, Wanner G, Boland W (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 Physiol 137:1160–1168

    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-Revue Canadienne De Zoologie 88(7):628–667

    Article  CAS  Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences – A new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416:599–600

    Article  PubMed  CAS  Google Scholar 

  • Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch Insect Biochem Physiol 58:128–137

    Article  PubMed  CAS  Google Scholar 

  • Nabity PD, Zavala JA, DeLucia EH (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 103(4):655–663

    Article  PubMed  CAS  Google Scholar 

  • Najar-Rodriguez AJ, Galizia CG, Stierle J, Dorn S (2010) Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures. J Exp Biol 213(19):3388–3397

    Article  PubMed  CAS  Google Scholar 

  • Newingham BA, Callaway RM, BassiriRad H (2007) Allocating nitrogen away from a herbivore: a novel compensatory response to root herbivory. Oecologia 153(4):913–920

    Article  PubMed  Google Scholar 

  • Nicastro RL, Sato ME, Da Silva MZ (2010) Milbemectin resistance in Tetranychus urticae (Acari: Tetranychidae): selection, stability and cross-resistance to abamectin. Exp Appl Acarol 50(3):231–241

    Article  PubMed  CAS  Google Scholar 

  • Niessing J, Friedrich RW (2010) Olfactory pattern classification by discrete neuronal network states. Nature 465(7294):47–U53

    Article  PubMed  CAS  Google Scholar 

  • Nombela G, Beitia F, Muñiz M (2000) Variation in tomato host response to Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to acyl sugar content and presence of the nematode and potato aphid resistance gene Mi. Bull Entomol Res 90:161–167

    Article  PubMed  CAS  Google Scholar 

  • Nomura K, Melotto M, He SY (2005) Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr Opin Plant Biol 8:361–368

    Article  PubMed  CAS  Google Scholar 

  • Nottingham SF, Hardie J, Dawson GW, Hick AJ, Pickett JA, Wadhams LJ et al (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. J Chem Ecol 17(6):1231–1242

    Article  CAS  Google Scholar 

  • Oliver JE, Doss RP, Williamson RT, Carney JR, De Vilbiss ED (2000) Bruchins-mitogenic 3-(hydroxypropanoil) esters of long chain diols from weevils of the bruchidae. Tetrahedron 39:7633–7641

    Article  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(1):62–67

    Article  Google Scholar 

  • Otsuka M, Kenmoku H, Ogawa M, Okada K, Mitsuhashi W, Sassa T, Kamiya Y, Toyomasu T, Yamaguchi S (2004) Emission of ent-kaurene, a diterpenoid hydrocarbon precursor for gibberellins, into the headspace from plants. Plant Cell Physiol 45(9):1129–1138

    Article  PubMed  CAS  Google Scholar 

  • Paré PM, Tumlinson JH (1999) Plant volatiles as defense against insect herbivores. Plant Physiol 121:325–331

    Article  PubMed  Google Scholar 

  • Paré PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci U S A 95:13971–13975

    Article  PubMed  Google Scholar 

  • Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318(5847):113–116

    Article  PubMed  CAS  Google Scholar 

  • Park DH, Mirabella R, Bronstein PA, Preston GM, Haring MA, Lim CK, Collmer A, Schuurink RC (2010) Mutations in gamma-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J 64(2):318–330

    Article  PubMed  CAS  Google Scholar 

  • Paschold A, Halitschke R, Baldwin IT (2007) Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J 51(1):79–91

    Article  PubMed  CAS  Google Scholar 

  • Peiffer M, Felton GW (2009) Do caterpillars secrete “oral secretions”? J Chem Ecol 35:326–335

    Article  PubMed  CAS  Google Scholar 

  • Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–656

    Article  PubMed  CAS  Google Scholar 

  • Penuelas J, Llusia J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19(8):402–404

    Article  PubMed  Google Scholar 

  • Penuelas J, Llusia J, Asensio D, Munne-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28(3):278–286

    Article  CAS  Google Scholar 

  • Perez JL, French JV, Summy KR, Baines AD, Little CR (2009) Fungal phyllosphere communities are altered by indirect interactions among trophic levels. Microb Ecol 57(4):766–774

    Article  PubMed  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  PubMed  CAS  Google Scholar 

  • Pinto DM, Nerg AM, Holopainen JK (2007) The role of ozone-reactive compounds, terpenes, and green leaf volatiles (glvs), in the orientation of Cotesia plutellae. J Chem Ecol 33:2218–2228

    Article  PubMed  CAS  Google Scholar 

  • Pitman JL, Dasgupta S, Krashes MJ, Leung B, Perrat PN, Waddell S (2009) There are many ways to train a fly. Fly 3(1):3–9

    Article  PubMed  Google Scholar 

  • Raguso RA (2004) Why are some floral nectars scented? Ecology 85(6):1486–1494

    Article  Google Scholar 

  • Raguso RA, Levin RA, Foose SE, Holmberg MW, McDade LA (2003) Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana. Phytochemistry 63(3):265–284

    Article  PubMed  CAS  Google Scholar 

  • Ranger CM, Reding ME, Persad AB, Herms DA (2010) Ability of stress-related volatiles to attract and induce attacks by Xylosandrus germanus and other ambrosia beetles. Agricultural and Forest Entomology 12(2):177–185

    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 

  • Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 10:20

    Article  PubMed  CAS  Google Scholar 

  • Reynolds AM, Bohan DA, Bell JR (2007) Ballooning dispersal in arthropod taxa: conditions at take-off. Biol Lett 3(3):237–240

    Article  PubMed  Google Scholar 

  • Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19(4):335–340

    Article  PubMed  CAS  Google Scholar 

  • Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16(11):1395–1403

    Article  PubMed  CAS  Google Scholar 

  • Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100:14537–14542

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Saona C, Crafts-Brandner SJ, Canas LA (2003) Volatile emissions triggered by multiple herbivore damage: Beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29(11):2539–2550

    Google Scholar 

  • Rogers BT, Peterson MD, Kaufman TC (2002) The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes. Evol Dev 4(2):96–110

    Article  PubMed  CAS  Google Scholar 

  • Röse USR, Manukian A, Heath RR, Tumlinson JH (1996) Volatile semiochemicals released from undamaged cotton leaves: a systemic response of living plants to caterpillar damage. Plant Physiol 111:487–495

    PubMed  Google Scholar 

  • Rostás M, Eggert K (2008) Ontogenetic and spatio-temporal patterns of induced volatiles in Glycine max in the light of the optimal defence hypothesis. Chemoecology 18:29–38

    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 311(5795):1964–1967

    Article  CAS  Google Scholar 

  • Sabelis MW, de Jong MCM (1988) Should all plants recruit bodyguards? Conditions for a polymorphic ESS of synomone production in plants. Oikos 53:247–252

    Article  Google Scholar 

  • Sabelis MW, van de Baan HE (1983) Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi (Acari: Phytoseiidae, Tetranychidae). Entomol Exp Appl 33:303–314

    Article  Google Scholar 

  • Sabelis MW, Janssen A, Kant MR (2001) The enemy of my enemy is my ally. Science 291:2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Sabelis MW, Takabayashi J, Janssen A, Kant MR, van Wijk M, Sznajder B, Aratchige NS, Lesna I, Belliure B, Schuurink RC (2007) Ecology meets plant physiology: herbivore-induced plant responses and their indirect effects on arthropod communities. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 188–217

    Chapter  Google Scholar 

  • Sabelis MW, Janssen A, Takabayashi J (2011) Can plants establish stable alliances with their enemies’ enemies? J Plant Interact 6(2–3):71–75

    Article  Google Scholar 

  • Sallaud C, Rontein D, Onillon S, Jabès F, Duffé P, Giacalone C, Thoraval S, Escoffier C, Herbette G, Leonhardt N, Causse M, Tissier A (2009) A novel pathway for sesquiterpene biosynthesis from Z, Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21:301–317

    Article  PubMed  CAS  Google Scholar 

  • Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, Lima E, Kant M, Sabelis MW, Janssen A (2011) A herbivore that manipulates plant defence. Ecol Lett 14:229–236

    Article  PubMed  Google Scholar 

  • Sasaki K, Ohara K, Yazaki K (2005) Gene expression and characterization of isoprene synthase from Populus alba. FEBS Lett 579:2514–2518

    Article  PubMed  CAS  Google Scholar 

  • Schilmiller AL, Schauvinhold I, Laerson M, Xu R, Charbonneau AL, Schmidt A, Wilkerson C, Last RL, Pichersky E (2009) Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proc Natl Acad Sci U S A 106:10865–10870

    Article  PubMed  CAS  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 

  • Schmelz EA, Alborn HT, Tumlinson JH (2003) Synergistic interactions between volicitin, jasmonic acid and ethylene mediated insect-induced volatile emission in Zea mays. Physiol Plant 117:403–412

    Article  PubMed  CAS  Google Scholar 

  • Schmelz EA, Carrol MJ, Le Clere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci U S A 103:8894–8899

    Article  PubMed  CAS  Google Scholar 

  • Schmelz EA, Le Clere S, Carrol MJ, Alborn HT, Teal PEA (2007) Cowpea (Vigna unguiculata) chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiol 144:793–805

    Article  PubMed  CAS  Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci U S A 106(2):653–657

    Article  PubMed  CAS  Google Scholar 

  • Schnee C, Köllner TG, Gershenzon J, Degenhardt J (2002) The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-beta-farnesene, (E)-nerolidol, and (E, E)-farnesol after herbivore damage. Plant Physiol 130:2049–2060

    Article  PubMed  CAS  Google Scholar 

  • Schnee C, Kollner TG, Held M, Turlings TC, 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 U S A 103:1129–1134

    Article  PubMed  CAS  Google Scholar 

  • Schuman MC, Heinzel N, Gaquerel E, Svatos A, Baldwin IT (2009) Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytol 183(4):1134–1148

    Article  PubMed  CAS  Google Scholar 

  • Schuurink RC, Haring MA, Clark DG (2006) Regulation of volatile benzenoid biosynthesis in petunia flowers. Trends Plant Sci 11:20–25

    Article  PubMed  CAS  Google Scholar 

  • Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci U S A 103(34):12935–12940

    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 

  • Semmelhack JL, Wang JW (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459(7244):218–U100

    Article  PubMed  CAS  Google Scholar 

  • Shepherd RW, Bass WT, Houtz RL, Wagner GJ (2005) Phylloplanins of tobacco are defensive proteins deployed on aerial surfaces by short glandular trichomes. Plant Cell 17(6):1851–1861

    Article  PubMed  CAS  Google Scholar 

  • Shikano I, Ericsson JD, Cory JS, Myers JH (2010) Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system. Basic and Applied Ecology 11(1):15–22

    Google Scholar 

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

    Article  Google Scholar 

  • Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) 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 103:16672–16676

    Article  PubMed  CAS  Google Scholar 

  • Shiojiri K, Ozawa R, Kugimiya S, Uefune M, van Wijk M, Sabelis MW (2010) Herbivore-specific, density-dependent induction of plant volatiles: honest or “cry wolf” signals? PLoS One 5(8):e12161

    Article  PubMed  CAS  Google Scholar 

  • Shrivastava G, Rogers M, Wszelaki A, Panthee DR, Chen F (2010) Plant volatiles-based insect pest management in organic farming. Crit Rev Plant Sci 29(2):123–133

    Article  Google Scholar 

  • Shroff R, Vergara F, Muck A, Svatos A, Gershenzon J (2008) Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc Natl Acad Sci U S A 105:6196–6201

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385(6618):718–721

    Article  CAS  Google Scholar 

  • Simmons AT, Gurr GM (2005) Trichomes of Lycopersicon species and their hybrids: effects on pest and natural enemies. Agric For Entomol 8:1–11

    Article  Google Scholar 

  • Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI (2011) Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agric For Entomol 13(1):45–57

    Article  Google Scholar 

  • Siva-Jothy MT, Moret Y, Rolff J (2005) Insect immunity: an evolutionary ecology perspective. In: Advances in insect physiology, vol 32. Elsevier Science & Technology, Oxford, pp 1–48

    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(5):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(5):479–489

    Article  PubMed  CAS  Google Scholar 

  • Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11(3):431–443

    Article  PubMed  CAS  Google Scholar 

  • Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104(47):18842–18847

    Article  PubMed  CAS  Google Scholar 

  • Stange G (1992) High-resolution measurement of atmospheric carbon-dioxide concentration changes by the labial palp organ of the moth Heliothis armigera (Lepidoptera, Noctuidae). J Comp Physiol A-Sens Neural Behav Physiol 171(3):317–324

    Google Scholar 

  • Stange G, Stowe S (1999) Carbon-dioxide sensing structures in terrestrial arthropods. Microsc Res Tech 47(6):416–427

    Article  PubMed  CAS  Google Scholar 

  • Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol Lett 10(6):499–511

    Article  PubMed  Google Scholar 

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595

    Article  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17(6):278–285

    Article  Google Scholar 

  • Takabayashi J, Dicke M, Posthumus MA (1991) Induction of indirect defense against spider-mites in uninfested lima-bean leaves. Phytochemistry 30:1459–1462

    Article  CAS  Google Scholar 

  • Takabayashi J, Dicke M, Posthumus MA (1994a) Volatile herbivore-induced terpenoids in plant mite interactions – variation caused by biotic and abiotic factors. J Chem Ecol 20(6):1329–1354

    Article  CAS  Google Scholar 

  • Takabayashi J, Dicke M, Takahashi S, Posthumus MA, Vanbeek TA (1994b) Leaf age affects composition of herbivore-induced synomones and attraction of predatory mites. J Chem Ecol 20(2):373–386

    Article  CAS  Google Scholar 

  • Takabayashi J, Shimoda T, Dicke M, Ashihara W, Takafuji A (2000) Induced response of tomato plants to injury by green and red strains of Tetranychus urticae. Exp Appl Acarol 24:377–383

    Article  PubMed  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 

  • Takos A, Lai D, Mikkelsen L, Abou Hachem M, Shelton D, Motawia OCE, Wang TL, Martin C, Rook F (2010) Genetic screening identifies cyanogenesis-deficient mutants of Lotus japonicus and reveals enzymatic specificity in hydroxynitrile glucoside metabolism. Plant Cell 22(5):1605–1619

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R et al (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19(11):881–890

    Article  PubMed  CAS  Google Scholar 

  • Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J 58:927–939

    Article  PubMed  CAS  Google Scholar 

  • Thivierge K, Prado A, Driscoll BT, Bonneil E, Thibault P, Bede JC (2010) Caterpillar- and salivary-specific modification of plant proteins. J Proteome Res 9(11):5887–5895

    Article  PubMed  CAS  Google Scholar 

  • Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:1–8

    Article  CAS  Google Scholar 

  • Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766

    Article  PubMed  CAS  Google Scholar 

  • Tieman D, Zeigler M, Schmelz E, Taylor MG, Rushing S, Jones JB, Klee HJ (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62(1):113–123

    Article  PubMed  CAS  Google Scholar 

  • Tjallingii WF, Garzo E, Fereres A (2010) New structure in cell puncture activities by aphid stylets: a dual-mode EPG study. Entomol Exp Appl 135(2):193–207

    Article  Google Scholar 

  • Tomberlin JK, Tertuliano M, Rains G, Lewis WJ (2005) Conditioned Microplitis croceipes cresson (Hymenoptera: Braconidae) detect and respond to 2,4-DNT: development of a biological sensor. J Forensic Sci 50(5):1187–1190

    Article  PubMed  CAS  Google Scholar 

  • Tooker JF, De Moraes CM (2007) Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defences. Ecol Entomol 32:153–161

    Article  Google Scholar 

  • Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671

    Article  PubMed  CAS  Google Scholar 

  • Traulsen A, Nowak MA (2007) Chromodynamics of cooperation in finite populations. PLoS One 2(3):e270. doi:10.1371/journal.pone.0000270

    Article  PubMed  Google Scholar 

  • Truitt CL, Wei HX, Pare 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 

  • Tumlinson JH, Lait CG (2005) Biosynthesis of fatty acid amide elicitors of plant volatiles by insect herbivores. Arch Insect Biochem Physiol 58:54–68

    Article  PubMed  CAS  Google Scholar 

  • Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9(4):421–427

    Article  PubMed  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, Loughrin JH, McCall PJ, Röse USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci U S A 92:4169–4174

    Article  PubMed  CAS  Google Scholar 

  • Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129

    Article  Google Scholar 

  • Tzin V, Galili G (2010) New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol Plant 3(6):956–972

    Article  PubMed  CAS  Google Scholar 

  • Ujvary I, Dickens JC, Kamm JA, McDonough LM (1993) Natural product analogs – stable mimics of aldehyde pheromones. Arch Insect Biochem Physiol 22(3–4):393–411

    Article  CAS  Google Scholar 

  • Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12(4):479–485

    Article  PubMed  CAS  Google Scholar 

  • Utsumi S (2011) Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Popul Ecol 53(1):23–34

    Article  Google Scholar 

  • Van Baalen M, Jansen VAA (2001) Dangerous liaisons: the ecology of private interest and common good. Oikos 95:211–224

    Article  Google Scholar 

  • Van Baalen M, Jansen VAA (2003) Common language or Tower of Babel? On the evolutionary dynamics of signals and their meanings. Proc R Soc Lond B 270:69–76

    Article  Google Scholar 

  • Van den Boom CE, 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 der Goes van Naters W, Carlson JR (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17(7):606–612

    Article  PubMed  CAS  Google Scholar 

  • Van der Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S (2005) The Rpi-blb2 gene from Solanum bulbocastanum is a Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J 44(2):208–222

    Article  PubMed  CAS  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40(8):563–572

    Article  PubMed  CAS  Google Scholar 

  • Van Loon JJA, De Boer JG, Dicke M (2000) Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol Exp Appl 97:219–227

    Article  Google Scholar 

  • Van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64:251–263

    Article  PubMed  CAS  Google Scholar 

  • Van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4(4):292–294

    Article  Google Scholar 

  • Van Wijk M, Wadman WJ, Sabelis MW (2006) Morphology of the olfactory system in the predatory mite Phytoseiulus persimilis. Exp Appl Acarol 40(3–4):217–229

    PubMed  Google Scholar 

  • Van Wijk M, De Bruijn PJA, Sabelis MW (2008) Predatory mite attraction to herbivore-induced plant odors is not a consequence of attraction to individual herbivore-induced plant volatiles. J Chem Ecol 34(6):791–803

    Article  PubMed  CAS  Google Scholar 

  • Van Wijk M, de Bruijn PJ, Sabelis MW (2010) The predatory mite Phytoseiulus persimilis does not perceive odor mixtures as strictly elemental objects. J Chem Ecol 36:1211–1225

    Article  PubMed  CAS  Google Scholar 

  • Van Wijk M, De Bruijn PJA, Sabelis MW (2011) Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. PLoS One 6(7):e21742

    Article  PubMed  CAS  Google Scholar 

  • Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci U S A 98:8139–8144

    Article  PubMed  CAS  Google Scholar 

  • Vet LEM, De Jong AG, Franchi E, Papaj DR (1998) The effect of complete versus incomplete information on odour discrimination in a parasitic wasp. Anim Behav 55:1271–1279

    Article  PubMed  Google Scholar 

  • Vickers CE, Possell M, Hewitt CN, Mullineaux PM (2010) Genetic structure and regulation of isoprene synthase in Popular (Populus spp.). Plant Mol Biol 73:547–558

    Article  PubMed  CAS  Google Scholar 

  • Villada ES, Garzo-González E, López-Sesé AI, Fereres-Castiel A, Gómez-Guillamón ML (2009) Hypersensitive response to Aphis gossypii Glover in melon genotypes carrying the Vat gene. J Exp Bot 60(11):3269–3277

    Article  PubMed  CAS  Google Scholar 

  • Visser JH, Ave DA (1978) General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsa decemlineata. Entomol Exp Appl 24(3):738–749

    Article  CAS  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  PubMed  CAS  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20

    Article  PubMed  CAS  Google Scholar 

  • Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16:1365–1369

    Article  PubMed  CAS  Google Scholar 

  • Vuorinen T, Nerg A-M, Ibrahim MA, Reddy GVP, Holopainen JK (2004) Emission of Plutella xylostella-induced compounds from cabbages grown at elevated CO2 and orientation behavior of the natural enemies. Plant Physiol 135:1984–1992

    Article  PubMed  CAS  Google Scholar 

  • Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96:675–679

    Article  PubMed  CAS  Google Scholar 

  • Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93(1):3–11

    Article  PubMed  CAS  Google Scholar 

  • Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

    Article  PubMed  CAS  Google Scholar 

  • Wang EM, Wang R, DeParasis J, Loughrin JH, Gan SS, Wagner GJ (2001) Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat Biotechnol 19:371–374

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Zhou GX, Xiang CY, Du MH, Chen JA, Liu SS, Lou YG (2008) b-glucosidase treatment and infestation by the rice brown planthopper Nilaparvata lugens elicit similar signalling pathways in rice plants. Chin Sci Bull 53:53–57

    Article  CAS  Google Scholar 

  • Wanner KW, Nichols AS, Allen JE, Bunger PL, Garczynski SF, Linn CE (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS One 5(1):e8685

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697

    Article  PubMed  CAS  Google Scholar 

  • Weber H (2002) Fatty acid-derived signals in plants. Trends Plant Sci 7(5):217–224

    Article  PubMed  CAS  Google Scholar 

  • Webster B, Bruce T, Dufour S, Birkemeyer C, Birkett M, Hardie J, Pickett J (2008) Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae. J Chem Ecol 34(9):1153–1161

    Article  PubMed  CAS  Google Scholar 

  • Weech MH, Chapleau M, Pan L, Ide C, Bede JC (2008) Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J Exp Bot 59:2437–2448

    Article  PubMed  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–571

    Article  PubMed  CAS  Google Scholar 

  • Will T, Tjallingii WF, Thonnessen A, van Bel AJE (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci U S A 104(25):10536–10541

    Article  PubMed  CAS  Google Scholar 

  • Will T, Kornemann SR, Furch ACU, Tjallingii WF, van Bel AJE (2009) Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? J Exp Biol 212(20):3305–3312

    Article  PubMed  CAS  Google Scholar 

  • Willmer PG, Gordon SC, Wishart J, Hughes JP, Matthews IM, Woodford JAT (1998) Flower choices by raspberry beetles: cues for feeding and oviposition. Anim Behav 56(4):819–827

    Article  PubMed  Google Scholar 

  • Winter TR, Rostas M (2008) Ambient ultraviolet radiation induces protective responses in soybean but does not attenuate indirect defense. Environ Pollut 155(2):290–297

    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. Nat Biotechnol 24:1441–1447

    Article  PubMed  CAS  Google Scholar 

  • Xiang TT, Zong N, Zou Y, Wu Y, Zhang J, Xing WM, Li Y, Tang XY, Zhu LH, Chai JJ, Zhou JM (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Kapteyn J, Gang DR (2008) A systems biology investigation of the MEP/terpenoid and shikimate/phenylpropanoid pathways points to multiple levels of metabolic control in sweet basil glandular trichomes. Plant J 54:349–361

    Article  PubMed  CAS  Google Scholar 

  • Yao CA, Ignell R, Carlson JR (2005) Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25(37):8359–8367

    Google Scholar 

  • Yoshinaga N, Aboshi T, Ishikawa C, Fukui M, Shimoda M, Nishida R, Lait C, Tumlinson J, Mori N (2007) Fatty acid amides, previously identified in caterpillars, found in the cricket Teleogryllus taiwanemma and fruit fly Drosophila melanogaster larvae. J Chem Ecol 33:1376–1381

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga N, Aboshia T, Abea H, Nishidaa R, Alborn HT, Tumlinsonb JH, Moria N (2008) Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc Natl Acad Sci U S A 105:18058–18063

    Article  PubMed  CAS  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  PubMed  CAS  Google Scholar 

  • Zhang PJ, Zheng SJ, van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc Natl Acad Sci U S A 106:21202–21207

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Thilmony R, Bender CL, Schaller A, Yang He S, Howe GA (2003) Virulence systems of Pseumonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499

    Article  PubMed  CAS  Google Scholar 

  • Zhao N, Guan J, Ferrer JL, Engle N, Chern M, Ronald P, Tschaplinski TJ, Chen F (2010) Biosynthesis and emission of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol Biochem 48(4):279–287

    Article  PubMed  CAS  Google Scholar 

  • Zhu JW, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31(8):1733–1746

    Google Scholar 

  • Zhu-Salzman K, Salzman RA, Ahn J, Koiwa H (2004) Transcriptional regulation of sorghum defense against a phloem-feeding aphid. Plant Physiol 134:420–431

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman DC, Coudron CA (1979) Identification of traumatin, a wound hormone, as 12-oxo-trans-10-dodecenoic acid. Plant Physiol 63:536–541

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

JMA is funded via Horizon Breakthrough Projects (93519024) and by the Marie Curie Fp7 program (221212); BCJS and PMB by NWO Earth and Life Sciences (ALW) and TTI Green Genetics (1CC026RP); MWS is funded by The Royal Netherlands Academy of Arts and Sciences (KNAW).

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Correspondence to Merijn R. Kant .

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Alba, J.M. et al. (2012). The Impact of Induced Plant Volatiles on Plant-Arthropod Interactions. In: Smagghe, G., Diaz, I. (eds) Arthropod-Plant Interactions. Progress in Biological Control, vol 14. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-3873-7_2

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