Plant volatiles as method of communication

Plant Biotechnology Reports - Tập 7 Số 1 - Trang 9-26 - 2013
A. Das1, Sook-Hee Lee1, Tae Kyung Hyun1, Seon-Won Kim1, Jae‐Yean Kim1
1Division of Applied Life Science (BK21-WCU program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, Korea

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Abraham KJ, Pierce ML, Essenberg M (1999) The phytoalexins desoxyhemigossypol and hemigossypol are elicited by Xanthomonas in Gossypium cotyledons. Phytochemistry 52:829–836

Adler LS, Karban R, Strauss SY (2001) Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology 82:2032–2044

Agrawal AA (2000) Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804–1813

Agrawal AA, Janssen A, Bruin J, Posthumus MA, Sabelis MW (2002) An ecological cost of plant defence: attractiveness of bitter cucumber plants to natural enemies of herbivores. Ecol Lett 5:377–385

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

Andrews ES, Theis N, Adler LS (2007) Pollinator and herbivore attraction to cucurbita floral volatiles. J Chem Ecol 33:1682–1691

Aratchige NS, Lesna I, Sabelis MW (2004) Below-ground plant parts emit herbivore-induced volatiles: olfactory responses of a predatory mite to tulip bulbs infested by rust mites. Exp Appl Acarol 33:21–30

Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515

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

Avice H (1997) Induced responses to herbivory. In: Karban R, Baldwin IT (eds) Plant Pathology. University of Chicago Press, Chicago, p 294

Balao F, Herrera J, Talavera S, Dötterl S (2011) Spatial and temporal patterns of floral scent emission in Dianthus inoxianus and electroantennographic responses of its hawkmoth pollinator. Phytochemistry 72:601–609

Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci USA 95:8113–8118

Baldwin IT (2001) An ecologically motivated analysis of plant-herbivore interactions in native tobacco. Plant Physiol 127:1449–1458

Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221:277–279

Bate NJ, Rothstein SJ (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16:561–569

Beckers GJ, Spoel SH (2006) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol (Stuttg) 8:1–10

Bezemer TM, De Deyn GB, Bossinga TM, van Dam NM, Harvey JA, van der Putten WH (2005) Soil community composition drives aboveground plant-herbivore-parasitoid interactions. Ecol Lett 8:652–661

Birkett MA, Bruce TJ, Martin JL, Smart LE, Oakley J, Wadhams LJ (2004) Responses of female orange wheat Blossom midge, Sitodiplosis mosellana, to wheat panicle volatiles. J Chem Ecol 30:1319–1328

Blechert S, Brodschelm W, Holder S, Kammerer L, Kutchan TM, Mueller MJ, Xia ZQ, Zenk MH (1995) The octadecanoic pathway: signal molecules for the regulation of secondary pathways. Proc Natl Acad Sci USA 92:4099–4105

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

Bos R, Koulman A, Woerdenbag HJ, Quax WJ, Pras N (2002) Volatile components from Anthriscus sylvestris (L.) Hoffm. J Chromatogr A 966:233–238

Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580

Brodmann J, Twele R, Francke W, Holzler G, Zhang QH, Ayasse M (2008) Orchids mimic green-leaf volatiles to attract prey-hunting wasps for pollination. Curr Biol 18:740–744

Bruinsma M, IJdema H, Van Loon JAJ, Dicke M (2008) Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids and butterflies. Entomol Exp Appl 128:109–116

Cao H, Li X, Dong X (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95:6531–6536

Cardoza YJ, Tumlinson JH (2006) Compatible and incompatible Xanthomonas infections differentially affect herbivore-induced volatile emission by pepper plants. J Chem Ecol 32:1755–1768

Cardoza YJ, Alborn HT, Tumlinson JH (2002) In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28:161–174

Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE 3:e1904

Chen F, Tholl D, D’Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494

Chen F, Ro DK, Petri J, Gershenzon J, Bohlmann J, Pichersky E, Tholl D (2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol 135:1956–1966

Cheng AX, Lou YG, Mao YB, Lu S, Wang LJ, Chen XY (2007) Plant terpenoids: biosynthesis and ecological functions. J Integr Plant Biol 49:179–186

Cho MJ, Buescher RW, Johnson M, Janes M (2004) Inactivation of pathogenic bacteria by cucumber volatiles (E,Z)-2,6-nonadienal and (E)-2-nonenal. J Food Protect 67:1014–1016

Choh Y, Takabayashi J (2006) Herbivore-induced extrafloral nectar production in lima bean plants enhanced by previous exposure to volatiles from infested conspecifics. J Chem Ecol 32:2073–2077

Choh Y, Kugimiya S, Takabayashi J (2006) Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites. Oecologia 147:455–460

Cipollini D (2007) Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana. New Phytol 173:146–153

Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92:407–411

Cui J, Jander G, Racki LR, Kim PD, Pierce NE, Ausubel FM (2002) Signals involved in Arabidopsis resistance to Trichoplusia ni caterpillars induced by virulent and avirulent strains of the phytopathogen Pseudomonas syringae. Plant Physiol 129:551–564

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

De Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290

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

Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250

Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92:6602–6606

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

Deng C, Zhang X, Zhu W, Qian J (2004) Investigation of tomato plant defence response to tobacco mosaic virus by determination of methyl salicylate with SPME-capillary GC-MS. Chromatographia 59:263–268

Dicke M (1999) Specificity of herbivore-induced plant defences. Novart Fdn Symp 223:43–54 (discussion 54–49, 160–165)

Dicke M, Hilker M (2003) Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl Ecol 4:3–14

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

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

Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37

Dudareva N (2002) Molecular control of floral fragrance. In: Vainstein A (ed) Breeding for ornamentals: classical and molecular approaches. Kluwer Academic Publishers, Dordrecht, pp 295–309

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

Eckey C, Korell M, Leib K, Biedenkopf D, Jansen C, Langen G, Kogel KH (2004) Identification of powdery mildew-induced barley genes by cDNA AFLP: functional assessment of an early expressed MAP kinase. Plant Mol Biol 55:1–15

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

Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785

Engelberth J, Seidl-Adams I, Schultz JC, Tumlinson JH (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol Plant Microbe Interact 20:707–716

Erb M, Ton J, Degenhardt J, Turlings TC (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874

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

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

Farmer EE (2001) Surface-to-air signals. Nature 411:854–856

Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134

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

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

Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297

Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet 16:449–455

Frost CJ, Appel HM, 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 10:490–498

Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824

Funk CJ (2001) Alkaline phosphatase activity in whitefly salivary glands and saliva. Arch Insect Biochem 46:165–174

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

Gang DR (2005) Evolution of flavors and scents. Annu Rev Plant Biol 56:301–325

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

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 herbivorespecific plant responses. Plant Physiol 125:711–717

Halitschke R, Gase K, Hui D, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acidamino acid conjugates. Plant Physiol 131:1894–1902

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

Hammer KA, Carson CF, Riley TV (2003) Antifungal activity of the components of Melaleuca alternifolia (tea tree) oil. J Appl Microbiol 95:853–860

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

Heiden AC, Kobel K, Langebartels C, Schuh-Thomas G, Wildt J (2003) Emission of oxygenated volatile compounds from plants. Part I: emission from lipoxygenase activity. J Atmos Chem 45:143–172

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

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

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

Heil M, Hilpert A, Fiala B, Linsenmair KE (2001) Nutrient availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia 126:404–408

Heil M, Feil D, Hilpert A, Linsenmair KE (2004a) Spatio-temporal patterns in indirect defence of a South-East Asian ant-plant support the optimal defence hypothesis. J Trop Ecol 20:573–580

Heil M, Greiner S, Meimberg H, Kruger R, Noyer JL, Heubl G, Linsenmair KE, Boland W (2004b) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208

Heil M, Lion U, Boland W (2008) Defense-inducing volatiles: in search of the active motif. J Chem Ecol 34:601–604

Hern A, Dorn S (2004) A female-specific attractant for the codling moth, Cydia pomonella, from apple fruit volatiles. Naturwissenschaften 91:77–80

Hilker M, Meiners T (2002) The plant’s response towards insect egg deposition. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell Verlag, Berlin, pp 205–233

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

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

Hisashi O (2006) Foraging behavior of adult butterflies and its semiochemicals as olfactory signals. Comp Physiol Biochem 23:134–142

Hoballah ME, Stuurman J, Turlings TC, Guerin PM, Connetable S, Kuhlemeier C (2005) The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta. Planta 222:141–150

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 beta-glucosidase and jasmonic acid. FEBS Lett 352:146–150

Horiuchi J, Badri DV, Kimball BA, Negre F, Dudareva N, Paschke MW, Vivanco JM (2007) The floral volatile, methyl benzoate, from snapdragon (Antirrhinum majus) triggers phytotoxic effects in Arabidopsis thaliana. Planta 226:1–10

Huber DP, Ralph S, Bohlmann J (2004) Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. J Chem Ecol 30:2399–2418

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

James DG (2003) 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

Jo Y, Debose-Boyd RA (2010) Control of cholesterol synthesis through regulated ER-associated degradation of HMG CoA reductase. Crit Rev Biochem Mol Biol 45:185–198

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 135:483–495

Karban R (2001) Communication between sagebrush and wild tobacco in the field. Biochem Syst Ecol 29:995–1005

Karban R (2007) Experimental clipping of sagebrush inhibits seed germination of neighbours. Ecol Lett 10:791–797

Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71

Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930

Katharina G, Uwe C (2008) Priming: it’s all the world to induced disease resistance. Eur J Plant Pathol 121:233–242

Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675

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

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

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

Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and Allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102

Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2006) Components of C6-aldehydes-induced resistance in Arabidopsis thaliana against a necrotrophic fungal pathogen, Botrytis cinerea. Plant Sci 170:715–723

Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73:35–37

Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2008) Direct fungicidal activities of C6-aldehydes are important constituents for defense responses in Arabidopsis against Botrytis cinerea. Phytochemistry 69:2127–2132

Knoester M, Pieterse CMJ, Bol JF, Van Loon LC (1999) Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Mol Plant Microbe Ineract 12:720–727

Kondo M, Oyama-Okubo N, Ando T, Marchesi E, Nakayama M (2006) Floral scent diversity is differently expressed in emitted and endogenous components in Petunia axillaris lines. Ann Bot 98:1253–1259

Koschier EH, Sedy KA (2001) Effects of plant volatiles on the feeding and oviposition of Thrips tabaci Lindeman. In: Marullo R, Mound L (eds) Thrips, plants, tospoviruses. 7th International Symposium on Thysanoptera, Reggio Calabria, pp 185–187

Kost C, Heil M (2005) Increased availability of extrafloral nectar reduces herbivory in Lima bean plants (Phaseolus lunatus, Fabaceae). Basic Appl Ecol 6:237–248

Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628

Kost C, Heil M (2008) The defensive role of volatile emission and extrafloral nectar secretion for lima bean in nature. J Chem Ecol 34:1–13

Kovacevic N, Pavlovic M, Menkovic N, Tzakou O, Couladis M (2002) Composition of the essential oil from roots and rhizomes of Valeriana pancicii Halacsy & Bald. Flavour Frag J 17:355–357

Kubo I, Fujita K (2001) Naturally occurring anti-Salmonella agents. J Agric Food Chem 49:5750–5754

Lee B-H, Annis PC, Tumaalii F (2003) The potential of 1,8-cineole as a fumigant for stored wheat. In: Wright EJ, Web MC, Highley E (eds) Stored grain in Australia. Proceedings of the Australian Postharvest Technical Conference, Canberra, pp 230–234

Leege LM, Wolfe LM (2002) Do floral herbivores respond to variation in flower characteristics in Gelsemium sempervirens (Loganiaceae), a distylous vine? Am J Bot 89:1270–1274

Lehtila K, Strauss SY (1997) Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum. Oecologia 111:396–403

Levin RA, Raguso RA, McDade LA (2001) Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58:429–440

Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331

Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800

Liu J, Xia KF, Zhu JC, Deng YG, Huang XL, Hu BL, Xu X, Xu ZF (2006) The nightshade proteinase inhibitor IIb gene is constitutively expressed in glandular trichomes. Plant Cell Physiol 47:1274–1284

Liu C, Cheng Y, Zhang H, Deng X, Chen F, Xu J (2012) Volatile constituents of wild Citrus Mangshanyegan (Citrus nobilis Lauriro) peel oil. J Agric Food Chem 60:2617–2628

Lou YG, Du MH, Turlings TC, Cheng JA, Shan WF (2005) Exogenous application of jasmonic acid induces volatile emissions in rice and enhances parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae. J Chem Ecol 31:1985–2002

Maffei ME, Gertsch J, Appendino G (2011) Plant volatiles: production, function and pharmacology. Nat Prod Rep 28:1359–1380

Martin D, Bohlmann J (2005) Molecular biochemistry and genomics of terpenoid defenses in conifers. Rec Adv Phytochem 39:29–56

Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:1003–1018

Masters GJ, Jones TH, Rogers M (2001) Host-plant mediated effects of root herbivory on insect seed predators and their parasitoids. Oecologia 127:246–250

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

McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365

Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

Mumm R, Hilker M (2006) Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci 11:351–358

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

Nakamura S, Hatanaka A (2002) Green-leaf-derived C6-aroma compounds with potent antibacterial action that act on both gram-negative and gram-positive bacteria. J Agric Food Chem 50:7639–7644

Naoumkina MA, Zhao Q, Gallego-Giraldo L, Dai X, Zhao PX, Dixon RA (2010) Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 11:829–846

Neveu N, Grandgirard J, Nenon JP, Cortesero AM (2002) Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. J Chem Ecol 28:1717–1732

Okada K (2011) The biosynthesis of isoprenoids and the mechanisms regulating it in plants. Biosci Biotechnol Biochem 75:1219–1225

Okamoto T, Kawakita A, Kato M (2007) Interspecific variation of floral scent composition in Glochidion and its association with host-specific pollinating seed parasite (Epicephala). J Chem Ecol 33:1065–1081

Omura H, Honda K (2005) Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142:588–596

Pare PW, Tumlinson JH (1997a) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167

Pare PW, Tumlinson JH (1997b) Induced synthesis of plant volatiles. Nature 38:30–31

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

Pareja M, Qvarfordt E, Webster B, Mayon P, Pickett J, Birkett M, Glinwood R (2012) Herbivory by a phloem-feeding insect inhibits floral volatile production. PLoS ONE 7:e31971

Paschold A, Halitschke R, Baldwin IT (2006) Using ‘mute’ plants to translate volatile signals. Plant J 45:275–291

Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

Pieterse CM, van Loon LC (1999) Salicylic acid-independent plant defence pathways. Trends Plant Sci 4:52–58

Pieterse CMJ, van Wees SCM, Hoffland E, van Pelt JA, van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2005) Effects of decomposers and herbivores on plant performance and aboveground plant-insect interactions. Oikos 108:503–510

Preston CA, Betts H, Baldwi IT (2002) Methyl jasmonate as an allelopathic agent: sagebrush inhibits germination of a neighboring tobacco, Nicotiana attenuata. J Chem Ecol 28:2343–2369

Pulice CE, Packer AA (2008) Simulated herbivory induces extrafloral nectar production in Prunus avium. Funct Ecol 22:801–807

Raguso RA, Pichersky E (1995) Floral volatiles from Clarkia breweri and C. concinna (Onagraceae): recent evolution of floral scent and moth pollination. Plant Syst Evol 194:55–67

Rasmann S, Agrawal AA (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875–880

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

Rasmann S, Turlings TC (2008) First insights into specificity of below ground tritrophic interactions. Oikos 117:362–369

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

Rayapuram C, Baldwin IT (2007) Increased SA in NPR1-silenced plants antagonizes JA and JA-dependent direct and indirect defenses in herbivore-attacked Nicotiana attenuata in nature. Plant J 52:700–715

Reinbothe S, Mollenhauer B, Reinbothe C (1994) JIPs and RIPs: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6:1197–1209

Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

Rose U, 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

Rostas M, Turlings TCJ (2008) Induction of systemic acquired resistance in Zea mays also enhances the plant’s attractiveness to parasitoids. Biol Control 46:178–186

Rostas M, Ton J, Mauch-Mani B, Turlings TC (2006) Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naive parasitoids. J Chem Ecol 32:1897–1909

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

Runyon JB, Mescher MC, de Moraes CM (2008) Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores. Plant Physiol 146:987–995

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. Z Naturforsch C 60:743–756

Ruther J, Kleier S (2005) Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222

Schilmiller AL, Last RL, Pichersky E (2008) Harnessing plant trichome biochemistry for the production of useful compounds. Plant J 54:702–711

Schmelz EA, Alborn HT, Banchio E, Tumlinson JH (2003) Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216:665–673

Shah J (2003) The salicylic acid loop in plant defense. Curr Opin Plant Biol 6:365–371

Shan X, Wang Z, Xie D (2007) Jasmonate signal pathway in Arabidopsis. J Integr Plant Biol 49:81–86

Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

Shen B, Zheng Z, Dooner HK (2000) A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. Proc Natl Acad Sci USA 97:14807–14812

Shiojiri K, Karban R (2006) Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers. Oecologia 149:214–220

Shiojiri K, Takabayashi J, Yano S, Takafuji A (2000) Flight response of parasitoids toward plant-herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants. Appl Entomol Zool 35:87–92

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

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 USA 103:16672–16676

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

Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16

Soler R, Bezemer TM, van der Putten WH, Vet LEM, Harvey JA (2005) Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J Anim Ecol 74:1121–1130

Soler R, Harvey JA, Kamp AFD, Vet LEM, van der Putten WH, van Dam NM (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116:367–376

Spoel SH, Koornneef A, Claessens SM, Korzelius JP, van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

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

Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840

Steets JA, Hamrick JL, Ashman TL (2006) Consequences of vegetative herbivory for maintenance of intermediate outcrossing in an annual plant. Ecology 87:2717–2727

Stotz HU, Koch T, Biedermann A, Weniger K, Boland W, Mitchell-Olds T (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214:648–652

Stout MJ, Workman J, Duffey SS (1994) Differential induction of tomato foliar proteins by arthropod herbivores. J Chem Ecol 20:2575–2594

Stout MJ, Fidantsef AL, Duffey SS, Bostock RM (1999) Signal interactions in pathogen and insect attack: systemic plant mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiol Mol Plant Pathol 54:115–130

Suarez LH, Gonzales WL, Gianoli E (2009) Foliar damage modifies floral attractiveness to pollinators in Alstroemeria exerens. Evol Ecol 23:545–555

Svensson GP, Hickman MO Jr, Bartram S, Boland W, Pellmyr O, Raguso RA (2005) Chemistry and geographic variation of floral scent in Yucca filamentosa (Agavaceae). Am J Bot 92:1624–1631

Takabayashi J, Dicke M (1996) Plant-carnivore mutualism through herbivore induced carnivore attractants. Trends Plant Sci 1:109–113

Tasin M, Backman AC, Coracini M, Casado D, Ioriatti C, Witzgall P (2007) Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 68:203–209

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

Thaler JS, Fidantsef AL, Duffey SS, Bostock RM (1999) Tradeoffs in plant defense against pathogens and herbivores: a field demonstration using chemical elicitors of induced resistance. J Chem Ecol 25:1597–1609

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

Theis N, Raguso RA (2005) The effect of pollination on floral fragrance in thistles. J Chem Ecol 31:2581–2600

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

Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP, Broekaert WF (1998) Separate jasmonate-dependent and salicylate dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26

Turck F, Zhou A, Somssich IE (2004) Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to Its native promoter and the defense related gene PcPR1-1 in Parsley. Plant Cell 16:2573–2585

Turlings TCJ, Benrey B (1998) Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5:321–333

Turlings TC, Fritzsche ME (1999) Attraction of parasitic wasps by caterpillar-damaged plants. Novartis Found Symp 223:21–32 (discussion 32–28)

Turlings TC, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci USA 89:8399–8402

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

Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

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

Van Oosten VR, Bodenhausen N, Reymond P, Van Pelt JA, Van Loon LC, Dicke M, Pieterse CMJ (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant Microbe Interact 22:919–930

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

Van Poecke RM, 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

Van Tol RW, Bruck DJ, Griepink FC, Kogel WJ (2012) Field attraction of the vine weevil Otiorhynchus sulcatus to kairomones. J Econ Entomol 105:169–175

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 USA 98:8139–8144

Vos M, Berrocal SM, Karamaouna F, Hemerik L, Vet LEM (2001) Plant mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecol Lett 4:38–45

Vuorinen T, Nerg A-M, Syrjälä L, Peltonen P, Holopainen J (2007) Epirrita autumnata induced VOC emission of silver birch differ from emission induced by leaf fungal pathogen. Arthropod Plant Interact 1:159–165

Wackers FL, Bezemer TM (2003) Root herbivory induces an above-ground indirect defence. Ecol Lett 6:9–12

Wasternack C, Parthier B (1997) Jasmonate-signaled plant gene expression. Trends Plant Sci 2:302–307

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 34:1153–1161

Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19

Yamasaki T, Sato M, Sakoguchi H (1997) (−)-Germacrene D: masking substance of attractants for the cerambycid beetle, Monochamus alternatus (Hope). Appl Entomol Zool 32:423–429

Yan ZG, Wang CZ (2006) Wound-induced green leaf volatiles cause the release of acetylated derivatives and a terpenoid in maize. Phytochemistry 67:34–42

Yan Z, Reddy MS, Ryu CM, McInroy JA, Wilson M, Kloepper JW (2002) Induced systemic protection against tomato late blight elicited by plant growth promoting rhizobacteria. Phytopathology 92:1329–1333

Yu H, Kowalski SP, Steffens JC (1992) Comparison of polyphenol oxidase expression in glandular trichomes of solanum and lycopersicon species. Plant Physiol 100:1885–1890

Zavala JA, Patankar AG, Gase K, Baldwin IT (2004) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Natl Acad Sci USA 101:1607–1612

Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96:6523–6528

Zheng Z, Mosher SL, Fan B, Klessig DF, Chen Z (2007) Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol 7:2