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. 2011 Dec 1;6(12):1973–1978. doi: 10.4161/psb.6.12.18053

Herbivore induced plant volatiles

Their role in plant defense for pest management 

Abdul Rashid War 1,2, Hari Chand Sharma 1, Michael Gabriel Paulraj 2, Mohd Yousf War 3, Savarimuthu Ignacimuthu 2,*
PMCID: PMC3337190  PMID: 22105032

Abstract

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.

Keywords: herbivory, indirect defense, induced resistance, plant defense, volatiles

Introduction

Plants are continuously under threat from a wide array of biotic and abiotic stresses, of which biotic stress due to herbivory by insects is an important constraint in crop production.1 However, plants have evolved several defense mechanisms against insect herbivory,1,2 which are quite dynamic. Plants respond to herbivore damage through various morphological, biochemical, and molecular alterations.1,2 Plant resistance against herbivory could be constitutive or induced.1-4 Constitutive resistance is expressed by the plant irrespective of the external stimuli, while induced defenses are activated in response to the attack by the herbivores.2-4 Both constitutive and induced resistances play an important role in plant defense against insect herbivory.The effect of host plant resistance on the herbivore could be direct or indirect.3,4 Direct defenses against herbivory could be physical or chemical, and include morphological barriers such as trichomes, cellwall lignification and silica deposition, and syntheses of toxic chemicals (alkaloids, terpenoids, and phenolics), which act as repellents, deterrents, antinutritients, and antidigestive compounds.1-6 Induced resistance makes plants phenotypically plastic and enables them to tolerate the stress with ease.5 Indirect defenses refer to the attraction of the natural enemies (parasitoids and predators) of the herbivores, and it also increases foraging success of the natural enemies, thereby facilitating better control of the herbivores.3,4 Indirect defense is mediated through the release of volatile cues by the plants when attacked.4,6,7 Although direct defense has its own role to play in host plant resistance to insects, indirect defense forms an important component in pest control through the attraction of carnivores.4,6-8 Herbivore-induced plant volatiles (HIPVs) not only communicate between the infested plant and natural enemies of the attacking insects, but also warns the neighboring undamaged plants of the forthcoming danger, besides communicating between different parts of the same plant (inter-plant and intraplant signaling, respectively).7,10-13 The HIPVs also act as feeding and/or oviposition deterrents to insect pests.4,7,8 HIPVs are released from leaves, flowers, and fruits into the atmosphere, or into the soil from the roots in response to herbivore attack.3-13 About 2,000 volatile compounds released in response to herbivore attack have been identified from 900 plant families. A certain amount of volatile compounds is emitted by plants into the atmosphere, but once attacked, there is a change in the blend of the volatiles emitted.4,13,14 The HIPVs are emitted not only from the infested parts, but also from uninfested parts of the plant, which increases the detectability of the signal.1-14 HIPVs also mediate the interactions between plants and microorganisms.7,8

Our understanding of the plant-plant and plant-insect chemical signaling has advanced rapidly over the last few decades. HIPVs are reliable cues for the natural enemies, since they are produced in large amounts by the plants when the plants are under herbivore attack.7,15 Moreover, the volatile blend released is specific for a particular insect-plant system, including the natural enemies, and the neighboring plants.11,15,16 It varies according to the plant and herbivore species, the developmental stage, and condition of the plants and the herbivores.7,17,18 Plants can perceive volatile signals as evidenced by changes in the transcription of defense-related genes.7,19,20 Plants exposed to HIPVs have altered levels of defense related metabolites such as terpenoids,7,16,21 proteinase inhibitors,22 and phenolic compounds.8,22 The HIPVs provoke behavioral changes in the community ranging from carnivorous arthropods and parasitic nematodes to insectivorous birds, and from conspecific neighboring plants and plant parasitic weeds.3,7,8,15,17,23

Biosynthesis of HIPVs

The HIPVs are low molecular weight compounds, and mostly belong to terpenoids, phenylpropanoids/benzenoids, and fattyacid and amino acid derivatives.8 They are synthesized through different metabolic pathways.

Terpenoids. Terpenoids are important HIPVs involved in plant defense against herbivory. They are derived from a common C5 building block, isoprene units.Terpenoids include hemiterpenes (C5), monoterpenes (C10), sesquiterpenes (C15), homoterpes (C11andC16), and some diterpenes (C20). Terpenoids are synthesized by two pathways. Monoterpenes and diterpenes are usually produced through the MEP pathway that occurs in plastid. Monoterpenes are derived from geranyl diphosphate (GDP), and diterpenes from geranylgeranyl diphosphate (GGDP).24 Sesquiterpenes are produced through the MVA pathway from farnesyl diphosphate (FDP) in cytosol (Fig. 1).25,26 Jasmonic acid (JA) and its precursors serve as the potential stimulators of HIPVs that activate distinct set of genes, which in turn leads to terpenoid synthesis.27,28

Figure 1.

Figure 1.

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Terpenoids biosynthesis in plants

Phenypropanoids/benzenoids. Phenypropanoids and benzenoids constitute a large class of HIPVs, which play an important role in plant defense against herbivores. They are derived from l-phenylalanine, which is converted to trans-cinnamic acid catalyzed by L-phenyalanine ammonia-lyase. A variety of hydroxycinnamic acids, aldehydes and alcohols are then formed from hydroxyl cinnamic acid by methylation and hydroxylation.29 Some of these intermediate compounds are emitted as volatiles. Benzenoids are also formed from trans-cinnamic acid. However, during their synthesis, the trans-cinnamic acid is shortened by a C2 unit. It has been proposed that shortening of the chain occurs through CoA-dependent-β-oxidative pathway, CoA-independent-non- β-oxidative pathway, or through the combination of these two pathways.30

Volatile fatty acid derivatives. Volatile fatty acid derivatives are the important HIPVs, and are immediately released after insect damage. They are derived from linoleic and linolenic acid (C18 unsaturated fattyacids) by dioxygenation catalyzed by lipoxygenases.31 These are called as green-leaf volatiles (GLVs), because of the characteristic odor of mowed pastures.23

Amino-acid volatile derivatives. Many plant volatiles including aldehydes, alcohols, esters, acids, and nitrogen- and sulfur containing compounds are derived from amino acids such as alanine, valine, leucine, isoleucine and methionine, which play an important role in plant defense by recruiting the natural enemies of the attacking herbivore.8 Amino acids on de-amination form α-keto acid, which in turn forms formaldehyde, acids, alcohols and esters on decarboxylation, reductions, oxidations and esterification.32 Methionine has been found to be the precursor of sulfur containing volatiles such as dimethyl disulfide and thioesters, 3-methylbutanol and 2-methylbutanol, which form 3-methylbutyl 2-methylbutanoate in banana, and are derived from amino acid isoleucine.33 Alanine serves as the precursor for volatile ethyl esters in strawberry.34

Role of HIPVs in Plant Defense against Herbivores

Attraction of insect parasitoids by volatiles emitted from damaged plants has been well documented (Fig. 2). Parasitoids use these volatiles as cues to search their prey and provide an daptive advantage to the emitting plants as long as volatile production persists. These interactions are specific to a particular insect plant interaction. For example, Zea mays TPS10, is a herbivore-induced terpene synthase that forms (E)-β-farnesene, (E)-α- bergamotene, and other sesquiterpenes in Arabidopsis thaliana,35 which does not produce significant amounts of volatile terpenes, suggesting that a single herbivore-induced gene from Z. mays is sufficient to elicit this indirect defense. Cotesia marginiventris, a parasitoid of Spodoptera litura has been reported to be attracted to TPS10- producing A. thaliana. Damage by corn rootworm, Diabrotica virgifera larvae in maize roots induces the release of (E)-β-caryophyllene, which attracts the nematode, Heterorhabditis megidis that in turn feed on the larvae of D. virgifera.17

Figure 2.

Figure 2.

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Role of HIPVs in plant defense. HIPVs, Herbivore induced plant volatiles; POD, peroxidase; PPO, polyphenol oxidase; PAL, phenylalanine ammonia lyase; TAL, tyrosine alanine ammonia lyase; LOX, lipoxygenase; SOD, superoxide dismutase; APX, ascorbate peroxidase

A reduction in Lymantria dispar larval weight by 70% was observed on branches exposed to HIPVs due to the increased volatile emissions from HIPV-exposed leaves, since several volatiles induced by gypsy moth in Vaccinium corymbosum, including linalool and farnesenes, are repellent to many caterpillars.13,36 Positive correlation between the quantity of the HIPV with the carnivore attraction suggested that carnivores select the plants with increased HIPVs emission more easily. However, the quantition of volatile emission rate is still not clear. Some studies have suggested that increase in individual components of the HIPVs also increases the natural enemy attraction under field conditions,13 while some studies have suggested that individual HIPV components function independently. The predatory mite, Phytoseiulus persimilis is not attracted to homoterpene (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (emitted from infested Phaseolus lunatus as a pure compound).37 But the predatory mite is attracted to the plants when this compound is added to a volatile blend of the plants infested by insects which are not preys of the predatory mite.38 However, methyl salicylate (MeSA), a constituent of insect-induced plant volatiles, has been reported to be very effective both singly and in combination with other volatiles for indirect defense of the plants.37-39 The headspace volatiles of many insect-infested plants such as lima bean,40 Arabidopsis,41 tomato,27 and soybean contain MeSA.39 Sticky cards baited with MeSA have been reported to attract many insect predators including Geocoris pallens, Stethorus punctum picipes, and Chrysopa nigricornis.42 Volatiles such as MeSA, myrcene, β-ocimene, (E, E)-4, 8, 12- trimethyltrideca-1, 3, 7, 11-tetraene (TMTT), and (E, E)-α- farnesene are emitted by plants hours after infestation.8,12 MeSA and the C16- homoterpene 4, 8,12- trimethyl-1,3(E),7(E), 11- tridecatetraene [(E,E)-TMTT] have been found to attract the predatory mites.38 MeSA also inhibits oviposition by the cabbage moth, Mamestra brassicae43

Green leaf volatiles (GLVs) are well-studied volatiles emitted by plants in response to herbivory. They defend the plants not only indirectly, but also by direct induction of defense mechanisms against the herbivores.16,21 GLVs consist of C6-aldehydes, [(Z)-3-hexenal, n-hexanal] and their derivatives such as (Z)-3-hexenol, (Z)-3-hexen-1-yl acetate, and the corresponding isomers.23,31,44 The release of (3Z)-hex-3-enal has been observed within 20 sec after the disruption of Arabidopsis leaf tissues.44 The majority of HIPVs are synthesized de novo after insect damage.4,7-9,13-16 Compounds such as MeSA and methyl jasmonate, monoterpenes such as limonene, linalool, or ocimene, and sesquiterpenes such as bergamotene, caryophyllene and farnesene are released as several isomers, typically starting 24 h after insect damage.12,24 Maize plants exposed to GLVs emitted increased quantities of sesquiterpenes as compared with the non-exposed plants.9 Priming effect has been reported in maize plants exposed to the GLVs (Z)-3-hexenal, (Z)-3- hexen-1-ol, or (Z)-3-hexenyl acetate from neighboring plants.16 This effect increased the HIPVs emission from plants damaged by the larvae of S. littoralis, which in turn lead to a stronger attraction of C. marginiventris - an important parasitoid of S. litura larvae.45 Herbivore damaged maize plants have been reported to release volatile blend consisting of alcohols, aromatics, mono-, homo- and sesquiterpenes.9,11,16,46 Greater volatile emission has been reported in corn seedlings previously exposed to HIPVs from the neighboring plants as compared with the unexposed plants, and is also primed by (Z)-3-hexenyl acetate.16 Damage by L. dispar in V. corymbosum resulted in emission of (Z)-3-hexenyl acetate.13 Activation of plant defense by (Z)-3-hexenyl acetate and its role in priming has been reported in many plants.15,16,21 Karban et al.3,47 reported that sagebrush branches use external signals to activate resistance, and do not exchange signals via vascular connections. Intraplant signaling via volatiles plays an important role in plant defense, especially in shrubs such as blueberries, where insect larvae may be able to move relatively short distances among branches and evade induced defenses.13 Many lepidopteran adults are repelled by HIPVs.4,7,8,48 Maize VOCs induced by conspecific larvae in cage experiments repelled the adult S. frugiperda females.48 Rice plants infested by S. frugiperda release about 30 volatiles, including MeSA and methyl benzoate, which attract the natural enemies of S. frugiperda such as, C. marginiventris.49 The effect of GLVs depends on the distance of the source.9

Besides the aerial parts, roots of plants also emit HIPVs in response to the infestation by belowground insect pests, which attract natural enemies of the infesting herbivore.8 For instance, Diuraphis noxia, a root feeding pest induces the emission of 1, 8-cineole, a monoterpene volatile,50 which is toxic and repellent to certain insect pests.51 Roots of Thuja occidentalis when attacked by Otiorhynchus sulcatus release volatiles that attract the entomopathogenic nematode, H. megidis.52 Moreover, maize roots when infested by the larvae of D. virgifera produce a sesquiterpene (E)-β- caryophyllene that attracts H. megidi.17 However, some studies have suggested that root emitted volatiles in the soil reduce germination and growth of the competitive neighboring plants,53 and this could be due to the alteration in composition of root phospholipids and sterols.54

Genetic Engineering of HIPVs

Volatiles playing role in plant defense against insect pests have been manipulated through genetic engineering in plants with a capability to emit the target volatiles. Metabolically engineered tobacco plants produce higher amounts of terpenoids that modulate the insect behavior, with increased levels of the diterpene cembratriene-ol.55 Arabidopsis with overexpression of strawberry nerolidol synthase, a terpene synthase (TPS), produces a sesquiterpene alcohol, (3S)-(E) – nerolidol that attracts the predatory mite, P. persimilis.56 Similarly, transgenic maize plants with overexpression of the corn TPS10 gene produces (E)-β- farnesene, (E)-α-bergamotene, and other herbivore induced sesquiterpene hydrocarbons, which attract the parasitic wasp, C. marginiventris.35 Transgenic lines of Arabidopsis producing linalool significantly repelled the aphid, Myzus persicae.57 Progress in metabolic engineering to produced terpenoids to reduce insect infestation is expected to figure more prominently in future for pest management.

Phytohormones and HIPVs

Phytohormones play an important role in induction of volatiles in plants. JA mediated pathway is considered as the most important signal transduction pathway against insect pests. In addition to its role in direct plant defense, JA also defends plants indirectly by attracting natural enemies of the insect pests through volatile emissions58,59 Lima bean plants sprayed with JA emitted volatile blend similar, if not identical, to the spider mite, Tetranychus urticae infested plants.60 However, the spider mite induced blend was more attractive to the predatory mite, P. persimilis than the JA induced blend, because of the presence of MeSA in spider mite induced volatile blend.60 Exogenous application of JA induced volatile emissions in cucumber plants, and the emission was greater than that released by the spider mite infested plants. However, DMNT, (E)-β-ocimene, (E,E)-α- farnesene, and (Z)-3-hexenyl acetate were the most abundant compounds in the plants infested by T. urticae or treated with JA.59 MeSA is abundant in HIPVs. Reports on salicylic acid induced plant volatiles are limited.61 Ethylene has been found to alter the HIPVs. A precursor of ethylene, 1-aminocyclopropane-l-carboxylic acid, when applied exogenously on lima bean plants increased the jasmonic acid–induced emission of several HIPVs, thereby resulting in greater attraction of the predatory mite, P. persimilis.62 Ethylene has been reported to boost the volatile emission induced by GLV (Z)-3-hexenol in maize.21

Non-Target Effects of HIPVs

Although HIPVs play an important role by attracting the natural enemies of insect herbivores, there are some reports wherein non-target insect pests are also attracted, and thus, increasing herbivore damage. For instance, Dickens,63 reported that Colorado potato beetle, Leptinotarsa decemlineata is attracted to a blend of volatiles consisting of cis-3-hexenyl acetate, linalool, and MeSA. Adult Diabrotica beetles and S. frugiperda larvae were observed more frequently in GLV-treated plots,9 with reduced parasitization rate. The GLVs are physiologically active at very low concentrations. Volatiles released by sweet potato, Ipomoea batatus attract the sweet potato weevil, Cylas formicarius.64 Emission of blend of volatiles by plants in response to HIPVs exposure in the absence of herbivores could have ecological and physiological costs, since HIPVs might attract the natural enemies that may lead to their desensitization. Thus, plants need to have a more adaptive strategy to prime themselves for an increased volatile response after exposure to HIPVs. The increased rate of volatile emission from HIPV-exposed leaves would serve as an indirect defense by preferentially attracting the natural enemies of the herbivores.

Future Perspective

The HIPVs play an important role in host plant – herbivore – natural enemy interactions, and have the potential for enhacing the the effectiveness of host plant resistance and biological control for integrated pest management. However, there is a need to understand the ecological significance of HIPVs by integrating biochemical and molecular mechanisms in the production, and understand their ecological functions. Understanding of such interactions will open up new avenues for further studies on primary signaling cascades to the ecological consequences in various eco-systems. Further studies need to be performed to identify the volatile compounds that govern the olfaction-directed behavior of insect pests and their natural enemies to formulate strategies for developing varieties with constitutive and induced resistance to insect pests, and manipulation of such volatiles to attract the natural enemies of the crop pests for enhancing the effectiveness of bio-control agents for pest management.

Footnotes

References

  • 1.Sharma HC, Sujana G, Rao DM. Morphological and chemical components of resistance to pod borer, Helicoverpa armigera in wild relatives of pigeonpea. Arthropod-Plant Interact. 2009;3:151–61. doi: 10.1007/s11829-009-9068-5. [DOI] [Google Scholar]
  • 2.War AR, Paulraj MG, War MY, Ignacimuthu S. Jasmonic acid- mediated induced resistance in groundnut (Arachis hypogaea L.) against Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) Acta Physiol Plant. 2011;34:343–52. doi: 10.1007/s11738-011-0833-6. [DOI] [Google Scholar]
  • 3.Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW. Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia. 2000;125:66–71. doi: 10.1007/PL00008892. [DOI] [PubMed] [Google Scholar]
  • 4.Kessler A, Baldwin IT. Defensive function of herbivore-induced plant volatile emissions in nature. Science. 2001;291:2141–4. doi: 10.1126/science.291.5511.2141. [DOI] [PubMed] [Google Scholar]
  • 5.Agrawal AA. Current trends in the evolutionary ecology of plant defense. Funct Ecol. 2010;25:420–32. doi: 10.1111/j.1365-2435.2010.01796.x. [DOI] [Google Scholar]
  • 6.Rasmann S, Agrawal AA. Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Curr Opin Plant Biol. 2009;12:473–8. doi: 10.1016/j.pbi.2009.05.005. [DOI] [PubMed] [Google Scholar]
  • 7.Arimura GI, Matsui K, Takabayashi J. Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol. 2009;50:911–23. doi: 10.1093/pcp/pcp030. [DOI] [PubMed] [Google Scholar]
  • 8.Dudareva N, Negre F, Nagegowda DA, Orlova I. Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci. 2006;25:417–40. doi: 10.1080/07352680600899973. [DOI] [Google Scholar]
  • 9.von Mérey G, Veyrat N, Mahuku G, Valdez RL, Turlings TCJ, D’Alessandro M. Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects. Phytochemistry. 2011;72:1838–47. doi: 10.1016/j.phytochem.2011.04.022. [DOI] [PubMed] [Google Scholar]
  • 10.Karban R. The ecology and evolution of induced resistance against herbivores. Funct Ecol. 2011;25:339–47. doi: 10.1111/j.1365-2435.2010.01789.x. [DOI] [Google Scholar]
  • 11.Frost CJ, Mescher MC, Carlson JE, De Moraes CM. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 2008;146:818–24. doi: 10.1104/pp.107.113027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Heil M. Indirect defence via tritrophic interactions. New Phytol. 2008;178:41–61. doi: 10.1111/j.1469-8137.2007.02330.x. [DOI] [PubMed] [Google Scholar]
  • 13.Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ. Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol. 2009;35:163–75. doi: 10.1007/s10886-008-9579-z. [DOI] [PubMed] [Google Scholar]
  • 14.Dicke M, van Loon JJA, Soler R. Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol. 2009;5:317–24. doi: 10.1038/nchembio.169. [DOI] [PubMed] [Google Scholar]
  • 15.Kost C, Heil M. Herbivore induced plant volatiles induce an indirect defense in neighboring plants. J Ecol. 2006;94:619–28. doi: 10.1111/j.1365-2745.2006.01120.x. [DOI] [Google Scholar]
  • 16.Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A. 2004;101:1781–5. doi: 10.1073/pnas.0308037100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature. 2005;434:732–7. doi: 10.1038/nature03451. [DOI] [PubMed] [Google Scholar]
  • 18.Hare JD. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol. 2011;56:161–80. doi: 10.1146/annurev-ento-120709-144753. [DOI] [PubMed] [Google Scholar]
  • 19.Gomi K, Yamasaki Y, Yamamoto H, Akimitsu K. Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in Citrus. J Plant Physiol. 2003;160:1219–31. doi: 10.1078/0176-1617-01177. [DOI] [PubMed] [Google Scholar]
  • 20.Paschold A, Halitschke R, Baldwin IT. Using ‘mute’ plants to translate volatile signals. Plant J. 2006;45:275–91. doi: 10.1111/j.1365-313X.2005.02623.x. [DOI] [PubMed] [Google Scholar]
  • 21.Ruther J, Kleier S. Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol. 2005;31:2217–22. doi: 10.1007/s10886-005-6413-8. [DOI] [PubMed] [Google Scholar]
  • 22.Tscharntke T, Thiessen S, Dolch R, Boland W. Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol. 2001;29:1025–47. doi: 10.1016/S0305-1978(01)00048-5. [DOI] [Google Scholar]
  • 23.Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, van Loon JJA, Dicke M. Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J Exp Bot. 2009;60:2575–87. doi: 10.1093/jxb/erp101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Arimura G, Köpke S, Kunert M, Volpe V, David A, Brand P, et al. Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol. 2008;146:965–73. doi: 10.1104/pp.107.111088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.McCaskill D, Croteau R. Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha x piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta. 1995;197:49–56. doi: 10.1007/BF00239938. [DOI] [Google Scholar]
  • 26.Newman JD, Chappell J. Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. Crit Rev Biochem Mol Biol. 1999;34:95–106. doi: 10.1080/10409239991209228. [DOI] [PubMed] [Google Scholar]
  • 27.Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC. Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol. 2004;135:2025–37. doi: 10.1104/pp.104.048694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.van Schie CC, Haring MA, Schuurink RC. Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol. 2007;64:251–63. doi: 10.1007/s11103-007-9149-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Humphreys JM, Chapple C. Rewriting the lignin roadmap. Curr Opin Plant Biol. 2002;5:224–9. doi: 10.1016/S1369-5266(02)00257-1. [DOI] [PubMed] [Google Scholar]
  • 30.Boatright J, Negre F, Chen XL, Kish CM, Wood B, Peel G, et al. Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 2004;135:1993–2011. doi: 10.1104/pp.104.045468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Feussner I, Wasternack C. The lipoxygenase pathway. Annu Rev Plant Biol. 2002;53:275–97. doi: 10.1146/annurev.arplant.53.100301.135248. [DOI] [PubMed] [Google Scholar]
  • 32.Reineccius G. Flavor Chemistry and Technology. Boca Raton, Florida: CRCPress, 2006. [Google Scholar]
  • 33.Wyllie SG, Fellman JK. Formation of volatile branched chain esters in bananas (Musa sapientum L.) J Agric Food Chem. 2000;48:3493–6. doi: 10.1021/jf0001841. [DOI] [PubMed] [Google Scholar]
  • 34.Perez AG, Rios JJ, Sanz C, Olias JM. Aroma components and free amino acids in strawberry variety Chandler during ripening. J Agric Food Chem. 1992;40:2232–5. doi: 10.1021/jf00023a036. [DOI] [Google Scholar]
  • 35.Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J. 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. 2006;103:1129–34. doi: 10.1073/pnas.0508027103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Markovic I, Norris DM, Phillips JK, Webster FX. Volatiles involved in the nonhost rejection of Fraxinus pennsylvanica by Lymantria dispar larvae. J Agric Food Chem. 1996;44:929–35. doi: 10.1021/jf9502111. [DOI] [Google Scholar]
  • 37.Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA. Plant strategies of manipulating predator-prey interactions through allelochemicals: Prospects for application in pest control. J Chem Ecol. 1990;16:3091–118. doi: 10.1007/BF00979614. [DOI] [PubMed] [Google Scholar]
  • 38.De Boer JG, Dicke M. Experience with methyl salicylate affects behavioral responses of a predatory mite to blends of herbivore-induced plant volatiles. Entomol Exp Appl. 2004;110:181–9. doi: 10.1111/j.0013-8703.2004.00133.x. [DOI] [Google Scholar]
  • 39.Zhu J, Park KC. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol. 2005;31:1733–46. doi: 10.1007/s10886-005-5923-8. [DOI] [PubMed] [Google Scholar]
  • 40.Arimura G, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, et al. Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J. 2002;29:87–98. doi: 10.1046/j.1365-313x.2002.01198.x. [DOI] [PubMed] [Google Scholar]
  • 41.Chen F, D’Auria JC, Tholl D, Ross JR, Gershenzon J, Noel JP, et al. An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 2003;36:577–88. doi: 10.1046/j.1365-313X.2003.01902.x. [DOI] [PubMed] [Google Scholar]
  • 42.James DG. Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. J Chem Ecol. 2003;29:1601–9. doi: 10.1023/A:1024270713493. [DOI] [PubMed] [Google Scholar]
  • 43.Ulland S, Ian E, Mozuraitis R, Borg-Karlson AK, Meadow R, Mustaparta H. Methyl salicylate, identified as primary odorant of a specific receptor neuron type, inhibits oviposition by the moth Mamestra brassicae L. (Lepidoptera, noctuidae) Chem Senses. 2008;33:35–46. doi: 10.1093/chemse/bjm061. [DOI] [PubMed] [Google Scholar]
  • 44.Matsui K. Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol. 2006;9:274–80. doi: 10.1016/j.pbi.2006.03.002. [DOI] [PubMed] [Google Scholar]
  • 45.Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, et al. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 2007;49:16–26. doi: 10.1111/j.1365-313X.2006.02935.x. [DOI] [PubMed] [Google Scholar]
  • 46.D’Alessandro M, Turlings TCJ. Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst. 2006;131:24–32. doi: 10.1039/b507589k. [DOI] [PubMed] [Google Scholar]
  • 47.Karban R, Shiojiri K, Huntzinger M, McCall AC. Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology. 2006;87:922–30. doi: 10.1890/0012-9658(2006)87[922:DRISVA]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  • 48.De Moraes CM, Mescher MC, Tumlinson JH. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature. 2001;410:577–80. doi: 10.1038/35069058. [DOI] [PubMed] [Google Scholar]
  • 49.Yuan JS, Köllner TG, Wiggins G, Grant J, Degenhardt J, Chen F. Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J. 2008;55:491–503. doi: 10.1111/j.1365-313X.2008.03524.x. [DOI] [PubMed] [Google Scholar]
  • 50.Steeghs M, Bais HP, de Gouw J, Goldan P, Kuster W, Northway M, et al. Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiol. 2004;135:47–58. doi: 10.1104/pp.104.038703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Tripathi AK, Prajapati V, Aggarwal KK, Kumar S. Toxicity, feeding deterrence, and effect of activity of 1,8-cineole from Artemisia annua on progeny production of Tribolium castanaeum (Coleoptera: Tenebrionidae) J Econ Entomol. 2001;94:979–83. doi: 10.1603/0022-0493-94.4.979. [DOI] [PubMed] [Google Scholar]
  • 52.van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH. Plants protect their roots by alerting the enemies of grubs. Ecol Lett. 2001;4:292–4. doi: 10.1046/j.1461-0248.2001.00227.x. [DOI] [Google Scholar]
  • 53.Singh HP, Batish DR, Kaur S, Ramezani H, Kohli RK. Comparative phytotoxicity of four monoterpenes against Cassia occidentalis. Ann Appl Biol. 2001;141:111–6. doi: 10.1111/j.1744-7348.2002.tb00202.x. [DOI] [Google Scholar]
  • 54.Zunino MP, Zygadlo JA. Changes in the composition of phospholipid fatty acids and sterols of maize root in response to monoterpenes. J Chem Ecol. 2005;31:1269–83. doi: 10.1007/s10886-005-5285-2. [DOI] [PubMed] [Google Scholar]
  • 55.Lücker J, Bowen P, Bohlmann J. Vitis vinifera terpenoid cyclases: functional identification of two sesquiterpene synthase cDNAs encoding (+)-valencene synthase and (-)-germacrene D synthase and expression of mono- and sesquiterpene synthases in grapevine flowers and berries. Phytochemistry. 2004;65:2649–59. doi: 10.1016/j.phytochem.2004.08.017. [DOI] [PubMed] [Google Scholar]
  • 56.Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science. 2005;309:2070–2. doi: 10.1126/science.1116232. [DOI] [PubMed] [Google Scholar]
  • 57.Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FWA, et al. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell. 2003;15:2866–84. doi: 10.1105/tpc.016253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Ozawa R, Shiojiri K, Sabelis MW, Takabayashi J. Maize plants sprayed with either jasmonic acid or its precursor, methyl linolenate, attract armyworm parasitoids, but the composition of attarctants differs. Entomol Exp Appl. 2008;129:189–99. doi: 10.1111/j.1570-7458.2008.00767.x. [DOI] [Google Scholar]
  • 59.Kappers IF, Verstappen FWA, Luckerhoff LLP, Bouwmeester HJ, Dicke M. Genetic variation in jasmonic acid- and spider mite-induced plant volatile emission of cucumber accessions and attraction of the predator Phytoseiulus persimilis. J Chem Ecol. 2010;36:500–12. doi: 10.1007/s10886-010-9782-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Dicke M, Gols R. ludeking D, Posthumus MA. Jasmonic acid and herbivory differentially induce carnivore attracting plant volatiles in lima bean plants. J Chem Ecol. 1999;25:1907–22. doi: 10.1023/A:1020942102181. [DOI] [Google Scholar]
  • 61.van Poecke RMP, Dicke M. Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J Exp Bot. 2002;53:1793–9. doi: 10.1093/jxb/erf022. [DOI] [PubMed] [Google Scholar]
  • 62.Horiuchi J, Arimura G, Ozawa R, Shimoda T, Takabayashi J, Nishioka T. Exogenous ACC enhances volatiles production mediated by jasmonic acid in lima bean leaves. FEBS Lett. 2001;509:332–6. doi: 10.1016/S0014-5793(01)03194-5. [DOI] [PubMed] [Google Scholar]
  • 63.Dickens JC. Plant volatiles moderate response to aggregation to pheromone in Colorado potato beetle. J Appl Entomol. 2006;130:26–31. doi: 10.1111/j.1439-0418.2005.01014.x. [DOI] [Google Scholar]
  • 64.Korada RR, Naskar SK, Prasad AR, Prasuna AL, Jyothi KN. Differential volatile emission from sweet potato plant: mechanism of resistance in sweet potato or weevil Cylas formicarius (Fab.) Curr Sci. 2010;99:1597–601. [Google Scholar]

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