Herbivore-induced, indirect plant defences - UPCH

92G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111with the first contact between plant and herbivore, andincluding herbivore recognition, signal elicitation, and earlysignalling steps, and followed by a description of thesignalling cascades and biosynthesis pathways involved,we will end with an overview of the ecology and evolution ofinduced, indirect defensive plant traits.2. Cell- and long-distance signalling in plants in responseto herbivoryPlants have evolved a large array of interconnected cellsignallingcascades, resulting in local resistance and longdistancesignalling for systemic acquired resistance (SAR).Such responses were initiated with the recognition ofphysical and chemical signals of the feeding herbivores,activate subsequent signal transduction cascades, and finallylead to an activation of genes involved in defence responsesthat consequently enhance feedback signalling and metabolicpathways (Fig. 1). This section describes the aspects ofcell signalling involved in the induction of indirectherbivore responses.2.1. ElicitorsIn the 1990s and earlier, many chemical ecologistsbelieved that herbivorous oral secretions and regurgitantselicited insect-induced plant responses, since simplemechanical wound stimuli, in many cases, could not mimicplant responses following insect attack [2–5]. h-Glucosidasederived from regurgitate of Pieris brassicae larvae wasidentified as a potential elicitor of herbivore-induced plantFig. 1. Schematic representation of the signalling pathways required for herbivore-induced responses in plants. This scheme merges the evidence obtained fromseveral plant taxa. The overall scenario may differ in certain plants; in particular the existence and the extent of synergistic and antagonist interaction betweenpathways may vary significantly. Elements in blue represent enzymes. Broken arrows indicate possible steps not yet described. Abbreviations: ACC, 1-aminocyclopropane-1-carboxylic acid; ACS, ACC synthase; DAG; diacylglycerol; FAC, fatty acid-amino acid conjugate; FAD, N-3 fatty acid desaturase;HIPV, herbivore-induced plant volatiles; JA, jasmonic acid; JMT, JA carboxyl methyl transferase; LOX, lipoxygenase; MAPK, mitogen-activated proteinkinase; MeJA, methyl JA; MeSA, methyl SA; OPDA, 12-oxophytodienoic acid; PL, phospholipase; PA, phosphatidic acid; SA, salicylic acid; SAM, S-adenosyl-methionine; SAMT, SA carboxyl methyl transferase; TF, transcription factor.

G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 93volatiles (HIPVs) [6]. The application of this h-glucosidaseto mechanically wounded parts of cabbage leaves resulted inthe emission of a volatile blend that attracted parasitic wasps(Cotesia glomerata). On the other hand, the application ofglucose oxidase, a salivary gland enzyme, inhibited thesynthesis of nicotine in tobacco leaves and may thus beresponsible for the observed resistance of feeding herbivores[7]. The suppressive effect, which maintains the plantpalatable, may be due to the products of glucose oxidase,namely hydrogen peroxide (H 2 O 2 ) and gluconic acid.N-(17-hydroxylinolenoyl)-l-glutamine (volicitin), a fattyacid-amino acid conjugate (FAC), was detected in the oralsecretion of beet armyworm larvae (Spodoptera exigua) [8](Fig. 2). This FAC was identified as the main elicitorinducing the emission of a volatile blend in maize plants(Zea mays) similar to that emitted when caterpillars fed onthem. While volicitin was isolated from S. exigua, otherFACs with biological activity, such as N-acyl Gln/Glu, havebeen isolated from the regurgitate of several lepidopteranspecies [9–11]. For example, the FAC N-linolenoyl-Glu inthe regurgitate of the tobacco hornworm (Manduca sexta)was characterised as a potential elicitor of volatile emissionin tobacco plants. FACs can induce the accumulation of 7-epi-jasmonic acid (JA) an octadecanoid-derived phytohormonethat elicited transcripts of herbivore-responsive genesin the tobacco plants [9]. 7-Epi-jasmonic acid is theoriginally produced and biologically active form of JA,which is isomerised in planta to the less active trans-isomer(see Fig. 1). Recently, a plasma membrane protein frommaize was suggested as a volicitin-binding protein [12].Plants that have been either pre-treated with methyljasmonate (MeJA) or S. exigua feeding showed increasedbinding activity of labelled volicitin to the plasma membrane.These findings suggest that volicitin-induced JAenhanced the interactions of the plasma membrane proteinwith volicitin as a ligand or the induced formation of theproteins after the recognition of volicitin. However, volicitinis not generally active. Leaves of Lima bean (Phaseoluslunatus), for example, do not respond to volicitin or to otherFACs with the induction of volatile emission [13].2.2. Early and secondary signal transduction pathwaysAfter mechanical damage, reactive oxygen species weregenerated near cell walls of tomato vascular bundle cells andthe resulting H 2 O 2 was shown to act as a second messengerfor the activation of defensive genes in mesophyll cellswhich are expressed later [14]. In Lima bean leaves infestedwith Spodoptera littoralis larvae, a depolarization of themembrane potential (V m ) and intracellular calcium influxwere observed only at the site of damage [15]. Simplemechanical wounding of the leaves also caused V mdepolarization, yet without a concomitant influx of calcium.Hence, already at this early step of signal recognition andtransduction, the pathways offer different responses towounding and herbivore attack. Thus, both wounding andthe introduction of herbivore-specific elicitors appear to beessential for the full induction of defence responses.On the other hand, recent studies applying a continuousrather than a single instance of mechanical damage (patternwheel) to Lima bean leaves clearly resulted in the emissionof volatile blends resembling those that occur afterherbivore damage [16]. As mentioned above, Lima beanand cotton (Gossypium hirsutum) do not respond to FACswith increased volatile emissions [13]. This observationmay be consistent with a high internal threshold forFig. 2. N-acyl glutamines from oral secretions of lepidopteran larvae.

94G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111mechanical damage which, in some plant species, is reachedonly after continuous wounding and which triggers thetypical repertoire of defence responses caused by elicitors.cDNA was isolated from a species of tobacco, encoding amitogen-activated protein kinase (MAPK), whose transcriptbegins to accumulate in the leaves 1 min after a singlemechanical wounding event [17]. This protein kinase(WIPK) is considered essential for JA formation and JAinducedresponses in tobacco, since transgenic plants inwhich WIPK has been silenced show impaired accumulationof JA and MeJA after wounding [17]. In contrast, the loss ofWIPK function in this transgenic line resulted in anincreased accumulation of salicylic acid (SA) and its sugarconjugate salicylic acid h-glucoside after wounding; however,such accumulation was not observed in wild-typeplants. The signalling pathways associated with JA and SAare generally thought to cross-communicate antagonistically(see below). Moreover, WIPK has also been reported toelicit the transcription of a gene for a N-3 fatty aciddesaturase (FAD7), which catalyses the conversion oflinoleic acid to linolenic acid, a precursor of JA [18]. Thus,WIPK may be an early activator of the octadecanoidpathway. WIPK and the SA-induced protein kinase (SIPK)were found to share an upstream MAPKK, NtMEK2 [19],and to interact with the calmodulin (CaM)-binding MAPKphosphatase (NtMKP1) [20]. Both kinases are commonlyinvolved in wound-mediated defence responses in tobacco[19,21,22]. If the MAPK cascades in tobacco were onlyinterlinked as described above, an active mutant of theupstream kinase of SIPK (NtMEK2 DD ) should haveincreased the accumulation of JA and MeJA, but it didnot [23]. Instead, ethylene was assumed to be involved inplant defence responses mediated by the NtMEK2-SIPK/WIPK pathway. This discrepancy may be not only due tothe complicated interactions of protein kinase/phosphatasecascades, but also to cross-talk between the JA-, SA-, andethylene-signalling pathways (see below). Since calciumdependentprotein kinases (CDPKs) are regularly involvedin signal transduction of a variety of biotic and abioticstresses [24], their involvement as active protein cascades inherbivore/wound responses cannot be excluded. CDPKscompose a large family of serine/threonine kinases in plants(for example, 34 members in Arabidopsis) [25,26]. JA hasbeen reported to affect CDPK transcript and activity inpotato plants [27].A transgenic Arabidopsis line in which the expressionlevel of phospholipase Da (PLDa) is suppressed has beenreported to show a decreased wound-induced accumulationof phosphatidic acid and JA, as well as JA-inducibletranscript activation [28]. Curiously, this loss-of-functionmutant also featured decreased expression of the genecoding lipoxygenase2 (LOX2) but not of any other geneinvolved in the octadecanoid pathway. LOX2 is one of thekey enzymes for the wound-induced synthesis of JA inchloroplasts [29]. Therefore, PLD may specifically regulateLOX2 upstream of the octadecanoid pathway that leads toJA. In addition, the involvement of phospholipase A (PLA),which mediates the release of linolenic acid from cellmembranes and is inducible by wound stimuli, has been alsoproposed for tomato (Lycopersicon esculentum) and otherspecies [30].Altogether, early and secondary cell signalling forherbivore-induced plant responses comprise: (1) the receptionof an extracellular signal(s) such as high- or lowmolecularweight factors from the herbivore (e.g., FACs),(2) V m depolarization and an intracellular calcium influx, (3)the activation of protein kinase/phosphatase cascades, and(4) the release of linolenic acid from the cell membrane andsubsequent activation of the octadecanoid pathway whichleads finally to the synthesis of JA and other oxylipins.However, multiple signals, signal circulation by, forexample, protein phosphorylation/dephosphorylation, andfeedback regulation of signalling and metabolic pathwaysare likely to complicate the understanding of the accuratemechanism.2.3. Oxylipin, SA, and their antagonismJA and SA function as signalling molecules, whichmediate induced plant responses toward herbivory andpathogen infection, resulting in the activation of distinctsets of defence genes [31–33]. Besides free JA, also aconjugate with the amino acid isoleucine may be involvedin signalling [34,35], but the significance of suchconjugates still remains to be established. Inhibiting theperformance of JA or SA obviously renders plants moresusceptible to herbivore damage and pathogen infection[36–39]. JA and SA act antagonistically, and are bothrequired for the induced response following herbivorefeeding or pathogen attack [40–44]. For instance, thegraduated increase of SA accumulation in Lima beanleaves treated with alamethicin (ALA), a potent fungalelicitor of plant volatile emission, interferes with steps inthe biosynthetic pathway downstream of 12-oxophytodienoicacid (OPDA), thereby reducing the rapid accumulationof JA (~40 min) [41] and, finally, the biosynthesisand emission of all JA-linked volatiles. On the other hand,enhanced levels of OPDA selectively induce the emissionof the C 16 -tetranorditerpene 4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT) in Lima bean [45]. Consequently,the treatment of Lima bean leaves with variousamounts of JA and SA caused the emission of characteristicblends of volatiles including TMTT, which stronglyattracted the carnivorous natural enemies of spider mites[40,46,47]. Hence, JA and SA pathways may vie with eachother to control and coordinate induced defences, since theemission of characteristic blends of herbivore-inducedvolatiles from attacked plants strongly depends on thedelicate balance between JA and SA [41]. Alternatively,both pathways may play a role in discriminating insectbiting from mechanical wounding and thus may be a kindof filter that prevents unnecessary defence activation.

G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 95Whether or not the recently discovered phytoprostanes,which result from non-enzymatic oxidative transformationof linolenic acid into prostaglandine-type octadecanoids[48], are involved in defence responses against herbivoresremains to be established. At least, gene expression analysisof Arabidopsis cell cultures treated with the phytoprostanesPPB 1 -I or -II revealed that both compounds triggered amassive detoxification and defence response covering theexpression of several glutathione S-transferases, glycosyltransferases and putative ATP-binding cassette transporters[49].2.4. Synergy between JA and ethyleneUndoubtedly, JA is among the most important signallingmolecules of herbivore-induced responses. However,the activation of JA formation alone cannot explain allchanges following wounding or herbivory. For example,transgenic potato plants overexpressing an allene oxidesynthase gene, which is involved in the JA formation,failed to express a PI gene (Pin2) constitutively, despitethe fact that transgenic plants exhibited six- to twelve-foldhigher levels of endogenous JA than did non-transgenicplants [50]. This observation indicates that JA is notalways involved in the signalling pathways of wound/herbivore responses and that other mediators may play arole in the respective signalling cascades. As describedabove, SA is an example of a signalling molecule that actsantagonistically towards JA. In addition, other signallingpathways may positively affect JA action. Ethylene is sucha candidate, as it induces the expression of defence genes,and its synthesis is induced by wounding, herbivorefeeding, and JA treatment [51,52]. Hints of a synergybetween JA and ethylene in the herbivory- or woundinducedresponses are: (1) plant defence genes aresynergistically induced by ethylene and JA/MeJA intobacco and in wounded tomato plants [51,53], (2)treatment of maize plants with 1-methylcyclopropene (1-MCP) reduced the production of ethylene and volatileemission following M. sexta feeding [54], and (3) treatmentof maize plants and Lima bean leaves with ethyleneor its precursor 1-aminocyclopropane-1-carboxylic acid(ACC) significantly promoted volatile emission inducedby JA [55,56]. In addition, simultaneous application of JAand ACC to Lima bean leaves increased the attractivenessof the pre-treated Lima bean leaf for predatory mites (e.g.,Phytoseiulus persimilis) as compared to leaves treated withJA alone [56]. All these results suggest that the cross-talkbetween JA and ethylene is required for both direct andindirect defence responses to herbivory. The application ofethylene and ethephon (an ethylene-releasing compound)together with the application of MeJA to tobacco plantssuppressed the induction of nicotine accumulation yethardly affected the emission of bergamotene, a volatilesesquiterpene [57]. Moreover, the application of 1-MCP totobacco plants treated with oral secretions of M. sextalarvae increased the induced accumulation of nicotine butreduced fitness-relevant plant parameters such as the rateof stalk elongation or lifetime capsule production [58]. Inthis case, the interplay between ethylene and JA mayreduce the level of nicotine present in a plant, thusreducing its autotoxicity as well as the physiological costsof this compound. Moreover, ethylene has been reported topositively regulate the induction of allene oxide synthase,an enzyme which catalyzes the production of a precursorof OPDA in the octadecanoid pathway, in Arabidopsis andtomato [51,59,60]. Also, the antagonistic interactionbetween ethylene and JA on defence gene expression,resulting in resistance of Arabidopsis plants to herbivory,has been proposed [61]. These mechanisms are differentamong different plant species (e.g., tomato and Arabidopsis)and the other conditions [61,62].Several other signalling molecules may function synergisticallywith JA and ethylene in plant defence responses. Forexample, in potato abscisic acid has been shown to increaseJA levels following mechanical damage to leaf tissues [63],whereas abscisic acid did not regulate any defence-relatedgenes by itself [64]. Among other plant hormones, auxin is alikely candidate, as it also has a negative effect on the JApathway [65]. Furthermore, spermine is considered as anintegral constituent of wound/herbivory responses, because(1) spermine activates WIPK and SIPK in tobacco leaves andmitochondrial dysfunction via a signalling pathway in whichreactive oxygen species and a calcium influx are involved[66], and (2) the expression of a S-adenosylmethionine(SAM) decarboxylase gene involved in the polyaminesynthesis is induced in Lima bean leaves infested withspider mites [52]. Considering that spider mite-infested Limabean leaves do not accumulate endogenous spermine, thispolyamine may, however, play a minor role in wound/herbivory responses. Alternatively, polyamines such asspermine may accumulate locally in intercellular spaces, ashas been shown for tobacco leaves infected with tobaccomosaic virus [67]. More evidence is still required to fullyunderstand the role of polyamines in stress responses.2.5. TranscriptionA subset of cis- and trans-transcription elements, whichare involved in the JA- ethylene- and the SA-signallingpathways, has been characterised. In several plant species,the GCC box (AGCCGCC), an ethylene-inducible element,has been found in the promoter region of ethylene-inducibledefence genes [68]. Four and six ethylene-responsivetranscription factors (ERF) that specifically interact withthe GCC box were characterised from tobacco andArabidopsis, respectively [69–71]. ERF genes can respondto various extracellular stimuli, such as wounding, pathogeninfection, and drought stresses, by changing of theirtranscriptional levels and have so far been described forhigher plants but not for yeast and other fungi [68,71]. InArabidopsis, ERF1 and AtERF1, AtERF2, and AtERF5 are

96G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111known as active elements of GCC-associated transcriptions,while AtERF3 and AtERF4 act as suppressive elements ofthese transcriptions [71]. As they bind to the same targetsequence, their transcriptional regulation is thought todepend on either the DNA binding affinity or on the relativeabundance of active ERFs in the nucleus, or on both factors.Moreover, such GCC-associated transcripts have beenshown to be coordinated not only by ethylene, but also byJA [72]. Conversely, JA-inducible transcription factorsORCAs (the octadecanoid-derivative responsive CatharanthusAP2-domain) have been characterised as a JAresponsiveAPETALA2 (AP2)/ERF- domain transcriptionfactor in Catharanthus roseus [73,74]. The overexpressionof Orca3 constitutively increased the expression of genesinvolved in several metabolic pathways (tryptophan decarboxylase,1-deoxy-d-xylulose-5-phosphate synthase anddesacetoxyvindoline 4-hydroxylase) involved in terpenoidand indole alkaloid formations [74]. Recently, a WRKYtranscription factor was shown to bind to a W-box, with thelatter consisting of two reversed TAGC repeats and locatedin the promoter region of the cotton (+)-y-cadinene(sesquiterpene) synthase gene CAD1 [75]. The expressionof this transcription factor was induced by JA and an elicitorderived from Verticillium dahliae. Direct/indirect synergismsor antagonisms between multiple trans-factors arelikely to regulate genes via signalling mediators such as JA,ethylene, and SA.The recent development of high-throughput microarraytechnology allows the simultaneous and systematic monitoringof the expression pattern of an immense number ofplant genes. Such analyses have shown comprehensivetranscript profiles in plants responding to insect feeding,mechanical wounding, JA, H 2 O 2 , and plant volatiles [76–80]. For instance, the transcription of several genes wasinduced in Arabidopsis following mechanical wounding andPieris rapae feeding [77]. Curiously, one gene encoding ahevein-like protein was induced by P. rapae, but not bymechanical wounding. As described above, induced plantresponses to mechanical wounding and feeding herbivoresmay differ due to varying degrees and types of damage andthe presence or absence of salivary compounds.2.6. Systemic responseIt is well known that plants respond to herbivory andmechanical wounding not only at the site of damage, but alsoin remote, undamaged leaves. The best systems studied inthis context are solanaceous species, such as tomato, forwhich an 18-amino-acid peptide called systemin wasdiscovered and claimed to represent an intercellular signallingmolecule [81]. Systemin is derived from a 200-aminoacidprecursor prosystemin that has been originally discoveredin tomato. Transgenic tomato plants that constitutivelyexpress antisense prosystemin RNA reduce wound-inducedtranscript accumulation of PIs in systemic leaves and aremore susceptible to M. sexta attack than are wild-type plants[82]. Furthermore, a 160-kDa plasma membrane-bound,leucine-rich repeat receptor kinase was recently characterisedas a systemin receptor (SR160) from suspension cultures oftomato cells [83]. Surprisingly, this receptor is identical totBRI1, a brassinosteroid receptor in tomato, and homologousto BRI1 in Arabidopsis [84–86]. The dual function of SR160/tBRI1, which remains to be unequivocally established, isvery unique, as this receptor has two ligands (systemin andbrassinosteroid) and apparently functions in developmentand defence responses [86]. Additional analyses demonstratedthat the overexpression of SR160 in suspension-culturedtobacco cells yielded systemin-binding activity and asystemin-induced alkalinisation response in the cells. Theseresults indicate that post-receptional steps of the signaltransduction are also present in tobacco, another member ofthe family Solanaceae. In tobacco, two 18-amino-acidhydroxyproline-rich glycoproteins (TobHypSys I and II),which are potential PI-inducers in a similar manner tosystemin, have been discovered [87,88]. These two peptidesare derived from a 165-amino-acid precursor that does notexhibit any homology to prosystemin from tomato, but isanalogous to peptide hormones from animals and yeast.Recently, this type of peptide was also discovered in tomato,raising the question of whether these peptides represent ageneral type of defence signal in the plant kingdom [89].Today, systemin is no longer considered as a longdistancesignal. A systemin-insensitive tomato mutant (spr1,suppressor of prosystemin-mediated responses1), deficientin a signalling step that couples systemin perception to thesubsequent activation of the octadecanoid pathway, showedthat the peptide acts at or near the local site of wounding,increasing JA-synthesis above the threshold that is requiredfor the systemic response in tomato [90]. According to theseresults, systemin is now thought to up-regulate the JAbiosynthetic pathway to generate a long-distance signal atthe local site (for example, JA or OPDA as the transmissiblesignals), whose recognition in distal leaves is linked tooctadecanoid signalling. Moreover, it was also found thatthe rapid and transient activation of early genes in responseto leaf excision or wounding was not affected in spr1 plants,indicating the existence of a Spr1- and systemin-independentpathway for wound signalling [90].Herbivore-induced systemic responses can be observednot only in solanaceous species but also in many otherplant families. Poplar trees (Populus trichocarpa x deltoides)are able to trigger the activation of gene expressionssystemically in undamaged leaves far from those that hadbeen damaged by the forest tent caterpillar (Malacosomadisstria) [91]. This systemic response revealed acropetal(upper) but not basipetal (lower) direction, but the transportmechanism remains obscure. A putative apoplastic lipidtransfer protein DIR1 has been suggested as a mobilesignal, mediating an interaction between a leaf of Arabidopsisinfected with Pseudomonas syringae and distant,uninfected leaves [92]. It was speculated that DIR1 couldbe a co-signal with other lipids, such as oxylipins (JA),

G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 97phosphatidic acid, and N-acylethanolamines, which travelthrough the vascular system of the plant. However, actualevidence for a possible involvement of DIR1 in anherbivore-induced defence is still lacking. In addition,electrical signals have been noted and claimed to mediatelong-distance interactions in wounded tomato seedlings[93]. Plants may have multiple systems that enable accuratelong-distance signalling. Thus, JA itself can act as asystemic signal in tobacco, which is formed in the woundedleaves and travels to the undamaged distal leaves and rootswhere the expression of PI and the nicotine biosynthesis areinduced, respectively [94,95].3. Biosynthesis of herbivore-induced plant volatiles(HIPVs)3.1. Volatile terpenoidsVolatile terpenoids which can be induced by herbivorefeedingcomprise monoterpenes (C 10 ), sesquiterpenes (C 15 )and homoterpenes (C 11 or C 16 ). All terpenoids are synthesisedthrough the condensation of isopentenyl diphosphateand its allylic isomer dimethylallyl diphosphate by catalysisof farnesyl diphosphate (FPP) synthase via the mevalonatepathway (cytosol/endoplasmic reticulum) or geranyl diphosphate(GPP) and geranylgeranyl diphosphate via the methyld-erythritol-1-phosphatepathway in plastids [96,97] (Fig.3). A large, structurally diverse number of terpenoids areyielded by a large family of terpene synthases (TPS) usingGPP and FPP as substrates. In Arabidopsis, 32 genesincluding two gibberellin biosynthetic genes are putativemembers of the TPS family [98], some function as mono-TPSs and sesqui-TPSs [99–102]. Terpenoid formation isgenerally assumed to be regulated on the transcript level ofthe TPS genes [91,103–105].However, the regulation mechanism seems to be rathercomplex, because herbivore-induced TPS transcripts andterpene emissions are affected by several factors (forexample, by diurnal rhythmicity and distance to herbivoredamagedtissue) [91,106]. Fig. 4 shows temporal patterns ofvolatile emissions in Lima bean leaves following herbivoreattack by S. littoralis over 4 days. The release of terpenoidsand the C 6 -volatile (3Z)-hex-3-enyl acetate follows diurnalcycles with increased emissions during the light period andreduced emissions during darkness. This result is in linewith findings in Lima beans treated with ALA and poplarleaves infested with forest tent caterpillars, where thevolatile emissions or the TPS expressions follows diurnalcycles [91,107]. In this context it would be interesting tostudy to what extent volatile emissions are linked to theendogenous biological clock.On the other hand, a single event of mechanical damageor the application of ALA to Lotus japonicus plants was notFig. 3. Biosynthetic pathways required for herbivore-induced plant volatiles. Elements in bold are enzymes. Abbreviations: ALDH, aldehyde dehydrogenase;DMAPP, dimethylallyl diphosphate; DMNT, (E)-4,8-dimethyl-1,3,7-nonatriene; DXP, 1-deoxy-d-xylulose-5-phosphate; DXR, DXP reductoisomerase; DXS,DXP synthase; FPP, farnesyl diphosphate; FPS, FPP synthase; GGPP, geranylgeranyl diphosphate; GGPS, GGPP synthase; GPP; geranyl diphosphate; GPS,GPP synthase; HMG-CoA, 3-hydroxy- 3-methyl-glutaryl CoA; HMGR, HMG-CoA reductase; HPL, fatty acid hydroperoxide lyase; IDI, IPP isomerase; IGL,indole-3-glycerol phosphate lyase; IPP, isopentenyl diphosphate; JA, jasmonic acid; JMT, JA carboxyl methyl transferase; LOX, lipoxygenase; MeJA, methyljasmonate; MEP, 2-C-methyl-d-erythritol-4-phosphate; TMTT, 4,8,12-trimethyltrideca-1,3,7,11-tetraene; TPS, terpene synthase.

G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 99defence agents or signalling molecules which elicit defencereactions.However, C 6 -volatiles may not always benefit plants.(2E)-Hex-2-enal inhibits the germination and subsequentgrowth of soybeans as well as the germination of applepollen [124,125]. Furthermore, (2E)-hex-2-enal reduces thegermination frequency of the MeJA-insensitive Arabidopsismutant jar1-1, suggesting that (2E)-hex-2-enal and MeJAare recognized in plants by different mechanisms [119]. Arapid formation of C 6 -volatiles after wounding not onlyserves as protection against herbivores or pathogens, butmay also be toxic for the plant itself. This effect could beinterpreted as some kind of strategic retreat, as has beenobserved for hypersensitive cell death in response topathogen infection. It remains to be investigated whetherthe transient burst of wound-induced C 6 -volatiles isdetrimental for the growth and development of a plant inthe long term.In contrast to C 6 -aldehydes and -alcohols, the emissionof (3Z)-hex-3-enyl acetate can frequently be observed a fewhours after the first impact of herbivore feeding ormechanical damage [113,126,127], as seen in the emissionof herbivore-induced terpenoids (Fig. 2). Since the emissionof both (3Z)-hex-3-enyl acetate and h-ocimene can beinduced by JA and ethylene [56], the signalling pathwaymay be identical. However, nothing is known about whetheror not the biological function of hexenyl acetate differs fromthe two early C 6 -volatiles.3.3. Volatile phytohormones and indoleLike JA, MeJA is also considered one of the mostimportant signalling molecules of herbivore-induced plantdefence. An early study showed that synthesis of PIproteins in the leaves of solanaceous species is induced byexogenous application of MeJA or natural emission ofMeJA from sagebrush plants (Artemisia tridentata) [128].Transgenic Arabidopsis overexpressing JA carboxylmethyl transferase (JMT), an enzyme that methylates JAto form MeJA, showed a three-fold increase of theendogenous MeJA level without altering JA levels [129].Furthermore, transgenic plants exhibited constitutive transcriptaccumulation of JA-responsible genes and enhancedresistance against the virulent fungus Botrytis cinere [129].These results indicate the importance of MeJA as a cellularsignal regulator and potential inter-cellular, and intra- andinter-plant signal transducers. The other JA derivative, (Z)-jasmone, has been found to repel the lettuce aphid(Nasonovia ribisnigri) and to induce (E)-h-ocimene,resulting in an increased attractivity of the plants to theaphid parasitoid Aphidius ervi [130]. However, it has beenalso reported that MeJA and cis-jasmone are onlymoderately induced in Nicotiana attenuata plants inresponse to feeding herbivores (9% of the JA accumulation)[131]. Functionally, these JA derivatives may be ofminor importance for defence and signalling. Otherwise,the importance may be limited in a few plant species suchas A. tridentata.The Arabidopsis genome contains 24 genes, whichbelong to a structurally related group of methyl transferases[132]. These have been classified as one gene family termedAtSABATH, of which JMT is a member. AtBSMT1,another member of this family, has recently been characterisedas SA carboxyl methyl transferase, an enzyme thatmethylates SA to form MeSA [133]. The transcriptaccumulation of AtBSMT1 can be induced by any of thefollowing: the fungal elicitor ALA; feeding Plutellaxylostella; uprooting; mechanical wounding; and exogenousapplication of MeJA to Arabidopsis leaves. In some of thesecases, the emission of MeSA is also induced. Besides itsrole as HIPV in attracting carnivores, such as the mites P.persimilis and Amblyseius potentillae [47], MeSA can alsoinduce defence responses in plants [134].Occasionally indole has been observed as a minorconstituent of herbivore-induced volatile blends. In maizeplants, a gene has been characterised as indole-3-glycerolphosphate (IGP) lyase, which catalyses the formation of freeindole from IGP [135]. Both volicitin and MeJA wereshown as selective inducers of the gene expression and theindole emission from maize plants [135,136].4. Ecology of induced indirect defences4.1. Variability of herbivore-induced plant volatilesThe emission of volatile organic compounds seems to bevery common across the plant kingdom and is not limited tocertain life forms (see [137] for a compilation of species).Odour blends emitted by herbivore-infested plants arecomplex mixtures, often composed of more than 100different compounds, many of which occur as minorconstituents [138]. Different plant species vary in theheadspace composition [139,140] yet also share compounds,for example, (E)-h-ocimene, (3Z)-hex-3-enyl acetate, andDMNT in Lima beans and cucumber [141]. Even within aspecies, the volatile blends emitted upon herbivore damagediffer both quantitatively and qualitatively depending on thegenotype or cultivar [142–144], the leaf developmental stage[145], or the plant tissue attacked by an herbivore [139], aswell as on abiotic conditions (light intensity, time of year,water stress) [146]. Beyond that, the time of the day alsoinfluences the composition of the emitted volatile blend (Fig.4): for example, Nicotiana tabacum releases several HIPVsexclusively at night. These nocturnally emitted compoundswere repellent to female moths (Heliothis virescens), whichsearch for oviposition sites during the night [147]. Moreover,the blend composition strongly depends on the type ofdamage (e.g., herbivore feeding versus oviposition [148])inflicted upon a given plant individual as well as on the timeelapsed after leaf damage (Fig. 4). To all the variability thatalready exists on the plant level, several studies have added

100G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111that the emitted blends also vary with the herbivore species[149], and even different ontogenetic stages of the sameherbivore [150,151] may influence the headspace composition.However, differences between volatile blends seem tobe largest among different plant species and smallest amongplants of one species infested by different herbivores[141,149].The high variability that characterises the chemicalcomposition of emitted blends raises the question of theecological relevance of these differences and whetherarthropods can discriminate among these complex mixtures.Electroantennogram (EAG) analyses allow individual blendcomponents to be differentiated in order to determine whichcompounds or combination of different compounds can beperceived by an arthropod [152,153]. Further informationon the physiological perception of different plant odours byarthropods have been obtained from in vivo calciumimagingmeasurements that provide additional informationon how the olfactory information is processed in thearthropod brain [154,155]. However, only the additionalinclusion of behavioural assays, in which the arthropods aresimultaneously exposed to two or more odours amongwhich they have to choose, provides information on whetheran odour has an attracting, repelling, or neutral effect on thebehaviour of the focal arthropod.4.2. Specificity and behavioural responses to HIPVsMuch has been learned from such behavioural assays onthe ability of arthropods to discriminate different odourblends. As the production of HIPVs has been originallydescribed in the context of host-location cues for parasiticwasps [5], most researchers have focussed on the role ofplant-derived volatiles in determining the ability of differentparasitoid or carnivore species to detect their herbivoroushosts or preys. Several studies of an increasing number oftritrophic plant–herbivore–carnivore systems have indicatedthat the ability of the carnivores and parasitoids todiscriminate different odour blends depends very much ontheir degree of dietary specialization [156], and on theirlevel of deprivation, as well as on their previous experience[149]. The particular behavioural response – that is whetheran herbivore or carnivore is attracted or repelled, or reactsneutrally to a specific blend of HIPVs – seems to dependstrongly on the level of plant induction [157–159].However, plants do not only interact with otherorganisms above ground. Recently, evidence has shownfor the first time that mechanisms similar to the onesdescribed above- may also work below-ground: Entomopathogenicnematodes (Heterohabditis megidis) are attractedas yet unidentified chemicals that are released from roots ofa coniferous plant (Thuja occidentalis) when weevil larvae(Otiorhynchus sulcatus) attack [160]. Moreover, systemicallyreleased HIPVs have been shown to attract thespecialist parasitoids of root-feeding larvae [161]. Althoughcurrently multitrophic below-ground interactions and thelinks between multitrophic above- and below-groundinteractions are poorly understood, future research willundoubtedly address these questions [162].4.3. Ecological function of HIPVs in natureMost studies regarding HIPV emission have beenconducted under artificial greenhouse or laboratory conditions.Facing the above-mentioned variability, the questionarises whether plants benefit from the emission of HIPVsunder natural growing conditions. To date, few studies existthat show predators are attracted to herbivore-infested plantsunder field conditions [153,163–165]. Moreover, specialistparasitoid wasps were able to distinguish among maize,cotton, and tobacco plants that were infested by theirherbivorous hosts from those which were under non-hostattack [166]. Caterpillars (S. exigua) placed on tomatoplants (L. esculentum var. Ace) that had been grown in anagricultural system and induced previously with exogenouslyapplied JA, suffered from higher parasitism rates byan endoparasitic wasp (Hyposoter exiguae) than controlplants [167]. A further field study of native tobacco (N.attenuata) demonstrated that, indeed, the release of volatilesincreased the predation rates of tobacco hornworm eggs by ageneralist predator (Geocoris pallens) [168]. Recently, Limabean plants grown in their natural environment, followed byrepeated treatments with JA solutions for 5 weeks wereshown to respond with an increased seed set [169]. Sinceboth the emission of HIPV as well as the secretion ofextrafloral nectar had been upregulated by this treatment, itremained unclear which indirect defence was responsible forthe observed beneficial effect. More field trials are clearlynecessary to determine the ecological relevance of individualfactors and to verify results that have been gathered inlaboratory or greenhouse experiments.4.4. Extrafloral nectarIn addition to releasing induced volatiles, some plantspecies have developed other ways to attract predatoryarthropods that will defend them. These include both theprovision of shelter in so-called leaf domatia [170], and theoffer of attractive food sources such as food bodies orextrafloral nectar (EFN). Extrafloral (EF) nectaries arespecialized nectar-secreting organs that may occur onvirtually all vegetative and reproductive plant structures,yet do not involve pollination [171]. They have beendescribed for approximately a thousand plant speciesranging over 93 plant families [172] of flowering plantsand ferns, but they are absent in gymnosperms [171]. EFNsare aqueous solutions that comprise mainly sucrose,glucose, and fructose, but other sugars, amino acids andother organic compounds may be present in some species[173]. The secreted sugars are mainly derived from thephloem [174,175] or synthesised in the region of the nectary[176]. EF nectaries secrete small amounts of nectar

G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 101throughout the day. The secretion of nectar can followcircadian rhythms [177–180] or be relatively constantthroughout day and night [181,182].The mechanisms of nectar secretion are poorly understood:Some researchers have described secretion as apassive process, whereas others discuss it as an eliminationof surplus sugars [173]. However, there is evidence thatnectar secretion is an active secretory process: It requires theexpenditure of metabolic energy [183], and EF nectariesstrongly resemble secretory cells which contain largenumbers of mitochondria and show dense protoplasts andlarge nuclei [173]. Furthermore, the secretion of EFN can beinduced by JA treatment. Originally discovered in Macarangatanarius [184], nectar secretion is suggested to beinducible by leaf damage. This seems to be a widespreadphenomenon [169,185–188], which may be linked to thesame or similar signalling pathways as those discussed forthe induction of volatile biosynthesis. Inhibitors thatsuppress the release of linolenic acid or interfere with theproduction of linolenic acid hydroperoxides completelysuppress the damage-induced flow of EFN and, hence,clearly demonstrate the involvement of oxylipin-basedsignalling in EFN-induction. Interestingly, also the attackof a below-ground herbivore (Agriotes lineatus) on cottonplants (Gossypium herbaceum) induced above-groundproduction of EFN [185]. InVicia faba, even the numberof EF nectaries increased following leaf damage [189].Generally, the secretion of EFN is believed to function asan indirect anti-herbivore defence by attracting and henceincreasing the presence of putative plant defenders onnectar-secreting plant parts. Most studies focussed on theprotective effect of ants on entire plants or individual plantparts, demonstrating a beneficial function of these insects[172,173]. However, contradictory observations thatdetected no measurable preventive effect of EFN-attractedants also exist [190–194]. In these cases, the lack ofprotection could be explained by, for example, (1) differencesin the aggressiveness of the attracted ant species[194–196], (2) differences in foraging behaviour of antspecies from different habitats [197,198], and (3) a varyingsusceptibility of the herbivores to ant predation [199,200].Besides ants, the EF nectaries attract a diverse spectrum ofother arthropods including Araneae, Diptera, Coleopteraand Hymenoptera (see [172] for review). Due to theirpredatory or parasitoid ways of life, many of these non-ants,such as ichneumonid, braconid and chalcidoid wasps [201–203], jumping spiders (Salticidae) [204], phytoseiid mites[205] or tachinid flies [206], can as well reduce the numberof herbivores. Both ants and wasps exerted beneficial effectson the EF nectary-bearing plant Turnera ulmifolia whenselectively excluded, yet no additive increase was observedwhen both insect groups had access [207].The emission of floral odours by plants is very importantfor attracting pollinators to their floral nectars. Some ofthese floral nectars also scent by themselves [208], whereasnothing is known about the headspace of EFNs. Beyondthese odours, which communicate the location, abundance,and quality of these nectars to higher trophic levels, othermechanisms may help to guide EFN-feeding arthropods toremote nectar sources. First, some EF nectaries are colouredproviding visual cues for foraging arthropods [172]. Additionally,increased amounts of both HIPVs and EFN(Table 1) would allow foraging arthropods to use theemitted volatile organic compounds as a cue to detect nectarsources from longer distances. Future research should try todisentangle and quantify the costs and benefits of one ofthese indirect defences for a plant and figure out to whatextent each of them contributes to plant defence in nature.4.5. Evolution of HIPVs and EFNThe evolutionary origin of HIPV emission and EFNsecretion remains unknown. As described above, C 6 -volatiles or terpenoids may repel herbivores [123,209], betoxic for phytophages [210,211], or act anti-microbially[212]. HIPVs are therefore discussed as having originallyTable 1Compilation of species that are known to both emit HIPVs and feature extrafloral nectariesFamily Species Nectar inducible HIPVs inducible ReferencesEuphorbiaceae Manihot esculenta n.i. n.i. + H 1 [269,270]Leguminosae Phaseolus lunatus + JA + JA [169]Vicia faba n.i. n.i. + H 2 [271,272]Vignia unguiculata n.i. n.i. + H 3 [273,274]Malvaceae Gossypium herbaceum + M, H 4, 5 + H 5, 6 [185,186,275]Gossypium hirsutum n.i. n.i. + H 6, 7, 8 [202,276–278]Rosaceae Prunus serotina n.i. n.i. + H 9 [256,279]Salicaceae Populus deltoides n.i. n.i. + H 10 [91,280]Populus trichocarpa n.i. n.i. + H 10 [91,281]Solanaceae Solanum nigrum n.i. n.i. + H 11, 12 [282,283]Additional information on the inducibility of the respective trait is presented (for abbreviations see below).H 1, spider mite (Mononychellus tanajoa Bondar); H 2, pentatomid bug (Nezara viridula Linnaeus); H 3, spider mite (Tetranychus urticae Koch); H 4,Mediterranean brocade (Spodoptera littoralis Boisduval); H 5, wireworms (Agriotes lineatus Linnaeus); H 6, beet armyworm (Spodoptera exigua Hqbner); H7, tobacco budworm (Heliothis virescens Fabricius); H 8, corn earworm (Helicoverpa zea Boddie); H 9, forest cockchafe (Melolontha hippocastani Fabricius);H 10, forest tent caterpillar (Malacosoma disstria Hqbner); H 11, Colorado potato beetle (Leptinotarsa decemlineata Say); H 12, death’s head hawkmoth(Acherontia atropos Linnaeus); JA, jasmonic acid; M, mechanical damage; n.i., not investigated.

102G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111functioned as a direct defence against pathogens orherbivores [213]. However, in this case, non-volatiledefensive compounds rather than volatile substances shouldhave evolved to fulfil this purpose, as they would not diffuseso easily in the environment [214]. HIPV emission is anactive process that does not necessarily depend on celldamage at the site of emission [215]. Even if the firstvolatile release by an herbivore-damaged plant was incidental,natural enemies might have been immediately able touse this cue to locate the responsible herbivores; hence,natural selection should operate on the plant to optimizethese signals [214].The evolution of EF nectaries is considered a very simpleprocess [173] that may have occurred several timesindependently [171,173]. This development has resulted inan extreme variety of plant taxa that feature a wide structuraldiversity of EF nectaries [216]; yet these structures may beabsent in one of two very closely related species [173].Recently, a 2-year study has shown that traits of EFnectaries were heritable and that casual ant associates actedas agents of selection on these traits [217]. Even ifcorresponding studies on other EF nectary-bearing plantsor plants that feature HIPVs are missing, these two indirectdefences seem to be evolutionarily plastic and to remainstable due to strong selection pressure. However, the geneticbasis of these two traits has been investigated only for thedevelopment of EF nectaries in cultivated cotton [218,219]and Acacia koa [220]: For cotton crossing, studies showedthat the inheritance of bnectarylessQ was transferred by twopairs of recessive genes (i.e., ne-1 and ne-2) [218,219].In addition to the benefits discussed above, the conceptof fitness costs provides a powerful explanation for theevolution of induced plants defences [221,222]: Costscover any trade-off between resistance and other fitnessrelevantprocesses [221]. Inducibility itself (i.e., the abilityto change per se) can raise fitness costs by, for example,increasing the lag time until the defence is up-regulated,during which the plants remains susceptible to herbivores[223,224]. Further evolutionarily relevant costs compriseallocation costs [225], genetic costs [226,227], autotoxicitycosts [228], opportunity costs [229], and ecological costs(Fig. 5) [230,231]. Inducible defence strategies are generallyFig. 5. Potential interactions of plants with higher trophic levels via herbivore-induced plant volatiles (HIPVs) and extrafloral nectar (EFN). The stipules at thepetioles of the leaves represent extrafloral nectaries. Effects mediated by HIPVs or EFN can be attraction (+) or deterrence ( ) that consequently affect trophicinteractions such as herbivory or predation (Arrows). Additionally, the ecological fitness costs (C) and benefits (B) of each interaction from the plant’sperspective are indicated.

G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 103assumed to reduce the fitness of a plant when expressedunder enemy-free conditions [232] as compared to costs of aconstitutive (i.e., permanent) expression. The physiologicalexpenditures of EFN production that could cause allocationtrade-offs within the plant are assumed to be very low, yetthis has rarely been tested: For the Balsa tree Ochromapyramidale, the physiological expenses of EFN secretionhave been calculated to account for 1% of the total energyinvestment per leaf [233]. In contrast, a phylogeneticalanalysis of American Acacia species revealed that constitutiveEFN secretion was found to be the derived state whichdeveloped as an adaptation to obligate myrmecophytism.This may indicate that a constitutive flow of EFN is costlyand only profitable when rewarded by permanent antprotection[187]. The actual costs probably depend on thelevel of EFN excretion and physiological limitations such asthe availability of water or nutrients. EFF secretion evenceases in the absence of nectar feeders, yet this may be apassive process and not necessarily a plant-regulated strategyto save costs [179]. The physiological expenditures of HIPVare expected to be relatively high [234–236], yet predictionsremain controversial [237–239] and experimental evidenceis rare. In maize plants, the first hints of allocation costs forthe production of HIPVs have been seen [211]. However, towhat extent simultaneously induced direct defencesaccounted for the measured costs remained unknown.Interestingly, these allocation costs were detectable only inyoung plants, with compensation for their metabolic investmentoccurring during maturation. Finite resource availabilitiesfor plants may also lead to trade-offs between direct andindirect defences [240,241]; these seem to be more commonin obligate ant–plant mutualisms [242–244] than in facultativeassociations [241].Both EFN and HIPVs are openly presented cues that maynon-specifically attract members of higher trophic levels.Such loose forms of facultative mutualisms are especiallyprone to exploitation by undesired arthropods. For example,the attraction of non-beneficial or even herbivorous speciesfeeding on EFN results in costs rather than benefits for therespective plant (Fig. 5) [245–247]. HIPVs emitted fromstrongly induced plants denote not only parasitoids orpredators, the presence of potential prey organisms but,additionally, a hint at increased numbers of competitors[248–250]. Furthermore, by calling on strongly inducedplants, carnivores or parasitoids may well run the risk offalling prey themselves to a hyperparasite or a predator[251]. The resulting deterrent effect of HIPVs on beneficialarthropods represents an ecologically relevant fitness costfor the herbivore-attacked plant (Fig. 5).Signals emitted from infested plants can also provideinformation to other trophic levels (Fig. 5): Conspecificherbivores, for example, can be attracted to infested plants[157,252,253], because this cue denotes the location ofpalatable host plants [254] and suitable oviposition sites[255] as well as the presence of potential mating partners[256]. Such a dmiscueT from the plant’s perspective resultsas well in ecological fitness costs for the plant. On the otherhand, conspecific or heterospecific herbivores may bedeterred by the emitted volatiles [147,252], as stronglyinduced plants may point to competition with conspecific orheterospecific herbivores or to an enemy-dense patch [257].In this case, the release of HIPVs would act as a directdefence [147,215], thereby benefiting the plant. Moreover,hyperparasitoides or carnivores of the fourth trophic levelcould use plant-derived volatiles for the search on largerspatial scales to find their prey or host by locating potentialhost plants [258]. Such attraction would again impose therespective plant with ecological costs (Fig. 5).Several plant species have the potential to defendthemselves indirectly using HIPV emission and EFNsecretion; both indirect defences are inducible via theoctadecanoid pathway (Table 1). Comparing the widespreaddistribution of EF nectaries across the plant kingdom [172]with the small number of nearly exclusively crop species forwhich HIPVs have been studied [213,259], an increasingnumber of plant species that features both indirect defencescan be expected. Beyond that, a wide taxonomicaldistribution of these plant traits may indicate the ecologicalsuccess of these two induced, indirect defences.In the ecological arms race between plants and herbivores,the latter are known for rapidly adapting to novelhost plants or toxins [260–262] by evolving specificmechanisms to circumvent direct defences with physiologicaltolerance [263,264] or behavioural responses [265,266].In view of the diverse spectrum of carnivorous specieswhich is attracted to plants expressing indirect defences, itis hard to imagine any mechanism or strategy thatherbivores might evolve to cope with these highly efficientplant defenders.5. ConclusionsWe described what is currently known about molecularmechanisms of cell signalling and signal travelling, as wellas the ecology and evolution of herbivore-induced plantresponses. Despite the effort that has been brought to bearon this topic, the exact mechanisms as well as the ecologicaland evolutionary relevance still remain elusive. One reasonis the diversity that exists on the genetic, biochemical,physiological, and phenotypical levels and that differs withthe evolutionary background of the studied plant species. Inecological studies, even the geographical location with itsparticular biotic and abiotic conditions influences theoutcome of a field experiment. We therefore suggestadopting model systems beyond the most frequently usedones, namely tobacco, Arabidopsis, maize, and Lima beanto distinguish in a more comparative way particularphenomena from general mechanisms. Such a biodiversity-orientedapproach should include more non-cropspecies since in this case a stronger co-evolution withnatural herbivores is to be expected.

104G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111Connectivity exists between multiple defences, as theyare often regulated via the same signalling cascade[267,268], leading to considerable methodological problemswhen individual defensive plant traits are studied. Forexample, the clear distinction between pure pathogen andherbivore defence pathways was undermined by the findingthat the type of damage inflicted by an herbivore (chewingcaterpillars versus sucking aphids) determines whichdefence pathway (SA versus JA) is activated. Furtheridentification of specific elicitors and the incorporation ofresponse mutants and transgenic plants will contribute toseparate the different defence responses. These newapproaches have to be complemented by creative fieldexperiments and comparative approaches to gain betterinsights into emerging areas like, e.g., the macroecology orcommunity ecology of induced, indirect defences. 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