Review

Long-distance signalling in plant defence
Martin Heil1 and Jurriaan Ton2
1 2

Dpto. de Ingenierıa Genetica, CINVESTAV - Irapuato, Km. 9.6 Libramiento Norte, CP 36821, Irapuato, Guanajuato, Mexico ´ ´ ´ Department of Biological Chemistry, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

Plants use inducible defence mechanisms to fend off harmful organisms. Resistance that is induced in response to local attack is often expressed systemically, that is, in organs that are not yet damaged. In the search for translocated defence signals, biochemical studies follow the physical movement of putative signals, and grafting experiments use mutants that are impaired in the production or perception of these signals. Longdistance signals can directly activate defence or can prime for the stronger and faster induction of defence. Historically, research has focused on the vascular transport of signalling metabolites, but volatiles can play a crucial role as well. We compare the advantages and constraints of vascular and airborne signals for the plant, and discuss how they can act in synergy to achieve optimised resistance in distal plant parts. Dynamic and systemic plant defences Plants possess chemical and physical defences to reduce damage by primary consumers: animals and microbes that use them as a food source. Because defence is costly, plants have evolved inducible defence mechanisms that are activated or amplified in response to attack. Particular signals can prime plant tissues, that is, prepare them for an augmented response to future attack without directly activating costly defence mechanisms. Herbivorous animals are highly mobile, however, and even pathogenic microbes can move within the plant. Hence, plants require additional countermeasures to halt the dispersal of the attacker and so prevent further damage. Systemically expressed induced resistance is a response that specifically aims to restrict the spread of the attacker: upon local attack, enhanced resistance spreads to distal organs that are not yet affected. Systemically induced resistance can be achieved by two mechanisms. First, it can result from systemic transport of defensive metabolites; and second, it can result from de novo expression of resistance mechanisms that are activated by translocated signals from the stress-exposed tissues. Recent evidence supports a crucial role for both mechanisms. This review focuses on the search for these long-distance signals. We summarize phenotypic evidence for systemic defence induction against pathogens and herbivores in a historical context, discuss the traits that qualify a factor as a long-distance signal, and present candidates that have been shown to act in this context. We compare airborne transport of signals with the more
Corresponding author: Heil, M. (mheil@ira.cinvestav.mx), (heil_martin@web.de).

traditionally studied translocation of signals through the vascular system, and outline the advantages and constraints of these two long-distance transport mechanisms. We discuss the possibility that airborne signals reach systemic tissues at concentrations that cause priming rather than the full induction of defence, and we propose a model that illustrates how vascular and airborne longdistance signals can act in synergy to induce a balanced resistance in distal plant parts. Systemic induction of resistance at the phenotypic level The first evidence for long-distance regulation of induced resistance came from the work by Frank Ross in the1960s. In work published in 1961 [1], Ross demonstrated that inoculation of the lower leaves of tobacco (Nicotiana tabacum) plants with necrosis-inducing tobacco mosaic virus (TMV) induced a hypersensitive reaction that resulted in enhanced resistance to a second infection in the upper leaves [1]. This phenomenon was termed systemic acquired resistance (SAR). SAR was first detected 2–3 days after primary virus infection and reached a maximum after 7 days, demonstrating that plants require time to generate, transport and deliver the long-distance signal that induces resistance in the upper leaves. Ten years later, Terrence Green and Clarence Ryan [2] reported that tomato (Lycopersicon esculentum) responds to insect feeding by producing defensive proteins. Proteinase inhibitors (PIs; i.e., compounds that reduce protein digestion by insects) were induced in both damaged and undamaged leaves. Supplying extracts from wounded leaves to excised, but otherwise undamaged, plants could also trigger the production of PIs, a clear hint of the existence of a mobile signal [3]. Finally, systemically transported signals are also involved when translocation of defensive compounds contributes to systemic resistance, for example, when nicotine is produced in the roots of tobacco (Nicotiana sylvestris) upon leaf damage [4]. SAR, PIs and toxic secondary compounds directly target the plants’ enemies and are called ‘direct defences’, but plants can also defend themselves by releasing volatile organic compounds or extrafloral nectar to attract natural enemies of the herbivores [5,6]. Although some volatile compounds have direct effects against pathogens and herbivores, this strategy is generally referred to as ‘indirect defence’. In many cases, induced volatile emission is a systemic response [7]. For instance, a water-soluble substance from insect-infested lima bean (Phaseolus lunatus)

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therefore. lipid-derived molecules might function as crucial long-distance signals in the activation of SAR [25. and application of SA triggered the accumulation of PR-proteins [12. Long-distance signals in the wound response Insect feeding inevitably leads to mechanical wounding. The synthesis of jasmonic acid (JA) and its precursors and derivatives (collectively termed jasmonates) is a classical wound response. grafting experiments — particularly with spr1. and comparisons among plant species have demonstrated that different signals might occur in different species. alkaloid production. that is released at wound sites upon feeding by chewing herbivores. Recently. Trends in Plant Science Vol. leading to speculation that SA might function as the endogenous signal. (ii) be produced or released at the site of attack. scientists have searched for factors that serve as long-distance signals. This peptide is processed from the 200-amino-acid precursor prosystemin. although originally suggested by Vladimir Shulaev and co-workers in 1997 [20]. Furthermore. SAR is predominantly effective against pathogens that are sensitive to SA-dependent basal defence mechanisms [15]. The topic is still a matter of intensive discussion. According to current views. Consequently. methyl salicylate (MeSA). Apparently. Nevertheless. the attacking agent. whether MeSA plays a similar role in other plant species. injection with salicylic acid (SA) elicited enhanced resistance to TMV. This event promotes binding of the COI1-unit to JAZ (jasmonate ZIM-domain) proteins. for example.28]. and so we can even state that SAR represents a systemic enhancement of SA-dependent basal resistance. SA undoubtedly plays an important role in both locally expressed basal resistance and SAR [14]. many candidate molecules appeared promising. Several factors failed to meet these criteria. Factors might be derived from the plant. it was discovered that jasmonates (most likely the JA-amino acid conjugate jasmonoyl–isoleucine) interact with the COI1 (CORONATIN-INSENSITIVE 1) unit of an E3 ubiquitin ligase complex termed SCFCOI1 (Skip/Cullin/F-box–COI1).26].31]. trichome formation and the secretion of extrafloral nectar. In the 1970s. SAR does not require the accumulation of SA in the attacked tissue. this line of research reached a significant breakthrough. 265 . Initially. Although the insect’s mode of feeding and elicitors in the insect’s regurgitate clearly influence the nature and intensity of the response. In tobacco. and SA methyltransferase1 (SAMT1). and feeding on roots can induce indirect defences in aboveground parts [9. however. their degradation allows transcription factors to stimulate JA-inducible gene expression [36–38]. Furthermore. To qualify fully as a long-distance signal. Thus. (iii) be translocated from the attacked to the systemic tissue. tomato plants that overexpressed the prosystemin gene produced PIs constitutively [33]. when Sang-Wook Park and co-workers [24] demonstrated that MeSA functions as the crucial longdistance SAR signal in tobacco (Box 2). however. This suggests that SA is not the crucial long-distance signal in SAR. intact systemin signalling is required in the damaged tissue but not in the distal responding tissue. It seems. A classic example of a systemic wound response is PI synthesis in tomato [2]. systemin. and (iv) accumulate in the systemic tissue before resistance expression takes place. such as the production of PIs. SA levels increase in the petioles of pathogen-infected tobacco [16] and cucumber (Cucumis sativus) [17] leaves before the onset of SAR. which starts with the liberation of linolenic acid from membranes followed by a multi-step conversion into JA by several enzymes [35]. however. which catalyses the formation of MeSA from SA [22]. For a systemic response to local damage. or because mutants in which they were not expressed failed to express resistance. or that different signals orchestrate distinct defence responses depending on the nature of the attacking organism.13]. It remains uncertain. therefore. or both. thereby targeting the JAZ proteins for ubiquitination and rapid degradation. Long-distance signals in the SAR response The initial discovery of SAR [1] initiated decades of research into its underlying mechanisms. even though it is transported throughout the plant and activates SAR. SABP2-silenced tobacco displays a reduced level of basal resistance and is unable to express SAR [23]. transportation of the elicitor through the whole plant seems an obvious explanation for the systemic nature of SAR. the resulting changes in the plant’s physiology are commonly termed ‘wound response’ [30. a factor must (i) induce a defensive response. SA-deficient tobacco rootstocks expressing SA hydroxylase were still capable of exporting the signal to wild-type scions [19].6 two enzymes control the balance between SA and MeSA: SA-binding protein2 (SABP2). are responsible for the systemic wound response (Box 3). Biochemical studies identified an 18-amino-acid peptide. Removal of pathogen-inoculated leaves before the SA levels increased in the petioles did not. In tobacco. Jasmonates induce a broad spectrum of defensive responses.Review elicited volatile emissions in undamaged plants [8]. impair the induction of SAR in upper leaves of cucumber [18]. and mechanical damage can induce defence responses similar to those stimulated by insect feeding [27. a mutant that is defective in the perception of systemin [34] — have revealed that jasmonates. 14 C labelling studies showed that systemin is mobile within the plant [32]. Leendert C. For instance.10]. In many plant species. van Loon found that both locally and systemically induced resistance to pathogens are associated with the induction of pathogenesis-related (PR) proteins [11]. This possibility was long overlooked. the release of volatiles. Because JAZ proteins are repressors of JA-inducible gene expression. How well does SA fit the criteria that define a transported long-distance signal (Box 1)? Intriguingly. the search for the translocated signal(s) is not yet completed. at least when the spatio-temporal pattern of the mechanical damage resembles that caused by a consuming insect [29]. which are subsequently transported throughout the plant to trigger the systemic response [30. rather than systemin. Box 1. which converts biologically inactive MeSA into active SA [21]. SA is (mainly) transported as its methyl ester. What qualifies a factor as a transported signal? Since first discovering systemic plant resistance in response to locally applied stress. Recently. the activation of indirect defences also involves regulation by long-distance signals. in Arabidopsis. that systemin locally induces jasmonates. because their exogenous application or overexpression triggered plant-wide defence.31]. For the majority of plant species.13 No.

Review Box 2.13 No. Together with the observation that exposure of lower plant parts to MeSA in gas-tight chambers can trigger SAR in non-exposed. tobacco [16]. Recently. Labelling studies [41. which leads to the amplification of the signal during its transport [40]. Volatiles in long-distance signalling Traditionally. which cannot convert MeSA into SA. was not capable of generating this longdistance signal. (b) Conversely. Figure I. SA bleeds out of petioles of pathogen-infected leaves [16. at least partly. most studies have focused on chemical or. Interestingly. functions as the critical mobile signal [24] (see Figure I). no expression of SAR. was still capable of generating a long-distance signal to activate SAR in an upper wild-type scion. When this so-called A13L protein was expressed in SABP2-silenced rootstocks. that jasmonate signalling in plants functions similarly to the propagation of action potentials in neurons: a locally initiated signal triggers JA synthesis in the neighbouring sector of the phloem. rather than SA. no SAR signal was transported to the upper scion. and the release of SA from the transported MeSA in the systemic tissue.6 infected leaves [80]. SAR can develop before SA levels rise in petioles of infected leaves [19]. (c) Furthermore. and the movement of this induction event functions. (d) The interaction of SAMT1 with SABP2 (which is inhibited by free SA) regulates the synthesis of MeSA from SA in the infected tissue. (e) Structures of SA and methyl salicylate (MeSA). Although MeSA can be transported within the plant. as the moving signal. 266 these mechanisms counteract dilution of the signal during long-distance transport. where it is converted by SABP2 into active SA that triggers SAR. Together. jasmonates have been shown to augment their own transport [41].78] and accumulates locally in pathogen-infected tissues of different species such as Arabidopsis [79]. several of which are expressed in the phloem of tomato. À. (a) Grafting experiments with plants in which the SA-binding protein 2 (SABP2) gene is silenced demonstrated that a SABP2–silenced rootstock.42]. jasmonate signalling is also required for rhizobacteria-induced systemic resistance (ISR) in Arabidopsis. MeSA as long-distance signal in systemic acquired resistance Salicylic acid (SA) induces resistance to many pathogens [14. SA-induced feedback inhibition of SABP2 is necessary to generate enough MeSA for long-distance transport to distal plant parts. a SA methyltransferase1 (SAMT1)-silenced rootstock. whereas its perception is required in the distal plant parts for a systemic induction of PIs [30]. expression of SAR. and cucumber [17]. Park and coworkers provided evidence that MeSA. Several characteristics make jasmonates optimal candidates for long-distance signals. It is tempting to speculate. it is possible that under natural circumstances a combination of airborne and vascular transport of MeSA is responsible for longdistance regulation of SAR [20]. even though ISR is not marked by systemic induction of PIs [39]. upper leaves. +. these findings demonstrate that MeSA functions as the crucial long-distance signal in tobacco [24]. This shows that jasmonates function as long-distance signals (Box 3). electrical [43] signals that travel through the vascular system. in which MeSA production is impaired. and accumulation and perception of SA are only critical in the systemic organs [20]. However. a recombinant SABP2 protein was constructed that is affected in SA-induced feedback inhibition of MeSA esterase activity. therefore. Second. First. Damage to a single leaf usually elicits .17] and labelling studies have confirmed systemic transport of SA from pathogen- Trends in Plant Science Vol. to a lesser extent. found that a surprisingly low percentage of exogenously applied jasmonates arrive at the target organs. they transiently induce the expression of genes that are required for their own synthesis. The role of MeSA as a transported signal in SAR. Hence. Biosynthesis of JA is required at the site of damage. however.

GLVs and other volatiles. wild tobacco [47] and the clonal plant Trifolium repens [48] follows the spatial patterns of assimilate transport. (d) GLVs (green leaf volatiles) have a double role as local and (in some. Figure I. but not all plants) systemic products of the wound response and as elicitors of further systemic responses. which is activated by systemin or other wounding-associated elicitors. impaired in the COI1 protein) were still capable of expressing PIs. GLVs are synthesized and subsequently released from the damaged tissue [63]. 11C-imaging of MeJA in tobacco revealed distribution patterns of MeJA that could only be explained by transportation through both phloem and xylem accompanied by exchange between non-orthostichous vascular pathways [41]. and resistance expression to herbivores in poplar (Populus trichocarpa x deltoides) [45]. pointing to a yet-unidentified mechanism of signal perception and transduction. these locally increased JA levels are followed by enhanced synthesis of nicotine in the roots [4]. GLVs prime plants for enhanced induction of (Me)JA-dependent defences [57.61]. revealed that intact JA synthesis in the rootstock. no expression of PIs. grafts with JA-biosynthetic mutants. MeJA. which are defective in systemin perception. (Z)-3-hexenol and (Z)-3-hexenyl acetate can induce or prime wound-responsive genes and defence responses. whereas spr1 scions can perceive the signal from wildtype rootstocks and express PIs. JA is synthesized locally in the damaged tissue via the octadecanoid pathway. jai1 scions grafted onto a damaged wild-type rootstock failed to activate the defence response. Also the methyl ester of JA. (a) The importance of JA perception in distal organs was demonstrated by the finding that wild-type scions of tomato that had been grafted onto damaged rootstocks of the jasmonate-insensitive 1 mutant (jai1.28].Review Box 3. which can be amplified by active JA synthesis in the vascular bundles [31] +.51]. such as the suppressor of prosystemin 2 (spr2) mutants [82] and the acyl-coA oxidase1 (acx1) mutant [83]. Furthermore. (b) That systemin is not the systemically transported signal becomes obvious from the observation that spr1 rootstocks. which are mediated by vascular and airborne signalling. cannot generate the transported signal. however. indicating the involvement of phloem transport [49]. Starting from membrane-derived linolenic acid. Concentrations of JA increase locally in response to tissue damage [4. phenotypic resistance is expressed just as quickly and strongly in distal leaves that lack a direct vascular connection to the attacked leaf as it is in leaves that have such a connection [50. research on long-distance signals usually focused on the vascular system (Boxes 2 and 3). (e) Although structurally not related to JA and MeJA. expression of PIs.35. Labelling studies using tobacco confirmed that 14 C-JA was transported from leaves to roots. At relatively low concentrations. The role of jasmonates in the systemic wound response. is required for a functioning signal transmission [30].81]. JA can be converted to the more volatile MeJA.6 However. thus they can synergize the systemic wound response to jasmonates. Grafting experiments have confirmed that jasmonates function as crucial mobile signals in the wound response of tomato (see Figure I). girdling of the petioles of pathogen-infected leaves blocks SAR development. the strongest responses in orthostichous leaves [44]. and both compounds have been reported to function as transported signals that induce systemic wound responses such as the synthesis of PIs. À.13 No. and not in the scion. and spatially distributed according to a strictly phloem-based transportation pathway [42]. The high vapour pressure of MeJA as compared to JA might account for the higher mobility of MeJA and opens the possibility of airborne defence signalling. Trends in Plant Science Vol. Jasmonates and long-distance signalling in the wound response Hundreds of studies have demonstrated that exogenous application of JA induces defensive responses [5. In some cases. can be transported systemically. This suggests that additional routes or mechan267 . Conversely. tomato [46]. In tobacco. (c) Correspondingly. For these reasons. During woundinduced synthesis of JA. GLVs such as (E)-2-hexenal.

however.67.24. Plant enemies often move from one leaf to the adjacent one. airborne signalling has crucial advantages over vascular signalling. systemic induction of extrafloral nectar secretion by leaves of wild lima bean in response to beetle feeding occurred only when air was moving freely between leaves [57]. both MeJA and MeSA are potent inducers of defence responses [20. Furthermore. but exposure to ethylene alone had no effect [67]. which are similar to the odorant-binding proteins of insects [72]. It is probably no coincidence that. Elucidating the mechanisms by which plants perceive volatile signals is a major challenge for future research. Correspondingly. water and soil nutrients. Benefits of airborne and vascular signalling Although volatiles have emerged as significant signals in induced resistance. however. Allowing ‘eavesdropping’ by neighbouring plants might have ecological costs because neighbours usually compete for light. What means of transportation could exist if the signal is not only transmitted through the vascular system? JA and SA can be methylated and then become volatile. It is therefore tempting to speculate that the dissolving of volatiles in the membranes combined with interactions with membrane proteins. but other GLVs that have been reported to be biologically active lack this motif [62. ‘long-distance signalling’ does not stop at a plant’s surface. phloem fluxes are usually directed towards non-photosynthesizing tissues. Ethylene also augmented induced volatile production by maize upon exposure to the GLV (Z)-3-hexenol. In fact. It is possible. airborne signals appear to have important functions in smaller plants too.69]. GLVs are in part released from pre- . and by the recent finding that MeSA functions as a crucial SAR signal in tobacco [24].13 No. it seems puzzling that plants use airborne regulation if they are already equipped with a sophisticated vascular transportation system. and this type of direct defence might. as demonstrated by Ingrid Kiefer and Alan Slusarenko’s observation that SAR induction in the Arabidopsis rosette extends beyond the route of assimilate movement along an orthostichy [51]. however. whereas transport through xylem vessels follows the upwards transpiration flow. volatile-mediated induction of resistance in neighbouring plants is a well-documented phenomenon [55–57]. similar studies that explicitly demonstrate the involvement of volatiles in the within-plant regulation of SAR are lacking. of all classes of herbivore-induced volatiles. MeJA. therefore. MeSA and MeJA can be reverted back into the active plant hormones jasmonic acid and salicylic acid. ethylene perception is required locally in the pathogen-infected leaf [66]. Indeed.Review isms are behind the induction of systemic resistance in photosynthesising source leaves or in leaves that are nonorthostichous to the stimulated ones [51. but directly adjacent leaves usually lack direct vascular connections. in which spatially neighbouring leaves often originate from separate branches. Likely candidates in airborne long-distance signalling Which volatiles are responsible for airborne signalling? Green-leaf volatiles (GLVs) have been associated with induced resistance in intact plants [60–62]. shrubs and vines. studies using mechanically damaged sagebrush (Artemisia tridentata) revealed that airflow was necessary for systemic induction of resistance against herbivores.). comm. and volatiles from herbivore-damaged leaves of poplar (Populus deltoides x nigra) augmented defence responses in adjacent leaves. even among branches of the same individual [59]. It has been suggested that GLVs that have an a.58]. (Z)-jasmone can trigger defensive responses having undergone airborne transport.b-unsaturated carbonyl group can trigger defence through their activity as reactive electrophile species [70]. Further studies are required to determine how common the phenomenon of airborne within-plant signalling really is. suggesting a different mode of action.54]. GLVs are also active against pathogen infection [64]. volatile-mediated induction of extrafloral nectar was observed in mature lima bean leaves that inserted below the induced leaves [57]. By contrast. Undoubtedly. in fact.53. that MeSA and MeJA travel by both airborne transport and vascular transport to mediate long-distance induction of resistance. However. GLVs are C6compounds that are rapidly released upon tissue damage [63]. GLVs are most frequently described as active airborne signals. ethylene and GLVs. Another airborne candidate is the gaseous hormone ethylene. little is known about the signalling response to GLVs. (Z)-jasmone failed to induce extrafloral nectar secretion in lima bean.6 those induced by MeJA [68. It seems evident. Changes in transmembrane potentials are involved in early signalling events in the cellular response to stress [43]. represent their original function [5]. Unfortunately. This indicates that ethylene increases the plant’s response to GLVs but is unlikely to serve as a primary signal. Similarly. pers. Though mainly discussed in the context of insect feeding. Furthermore. By contrast. This function is extremely likely. Details about the molecular perception of GLVs remain unknown. The structural diversity of resistanceinducing GLVs makes a specific receptor-protein-mediated mechanism of perception unlikely. Vascular restrictions become even more problematic in large plants. and exposure to several GLVs did change membrane potentials in intact lima bean leaves (Massimo Maffei. First. and hence. leads to changes in transmembrane potentials and thereby induces gene activity [71]. airborne signalling overcomes restrictions resulting from the plant’s orthostichy [44.52]. Second. For expression of SAR. Ethylene plays a modulating role in plant defensive reactions to pathogens [65]. volatile signal molecules can reach distal plant parts faster than compounds that are transported through vascular tissues. In addition to MeSA. respectively. such as trees. a typical JA-responsive trait that can be boosted by the GLV (Z)-3-hexenyl acetate [62]. This herbivore-induced volatile activates different sets of genes than 268 Trends in Plant Science Vol. that within-plant signalling by volatiles can synergize the response to vascular signalling molecules to regulate systemically expressed resistance (Figure 1).73]. suggesting that ethylene does not function as a long-distance signal.71]. Even signals that are transported through both xylem and phloem hardly reach mature leaves that are older than the signal-producing leaf. and it has been suggested that volatile compounds also act as within-plant signals [44.

plants rapidly emit airborne signals. (a) Upon local attack by insects (left) or pathogens (right). defence phase. (b) Kinetics of systemically expressed induced resistance. Model of a two-step regulation system of systemic resistance by airborne and vascular long-distance signals. methyl jasmonate or methylsalicylic acid. Airborne signals can trigger induced defence at relatively high concentrations. existing pools [63] and are generally synthesized from early precursors of JA extremely early during the wound response (Box 3). Rapid airborne signals (minutes – hours) trigger priming (priming phase – green symbols) and relatively little defence expression. and on various plant characteristics. such as wind speed and direction. The velocity and direction of within-plant signalling by volatiles depends on different biotic and abiotic factors. These signals are followed by a second vascular signal (days – weeks. (c) Relationship between induced defence expression (defence amplitude) and dosage of airborne (green arrow) and vascular (red arrow) long-distance signals. which can sensitize distal plant parts for a second vascular signal. Fast signalling is an important advantage.Review Trends in Plant Science Vol.6 Figure 1. as speed of defence activation is crucially important for the effectiveness of resistance to pathogens and insects. but at lower concentrations. red symbols) that boosts the induced defence expression. such as the presence of leaf hairs or a wax layer and probably many more factors. Further studies will be required to determine the extent by which locally 269 . they prime for an enhanced defence induction by the vascular signal.13 No. such as jasmonic acid or salicylic acid. such as green leaf volatiles.

Trends Plant Sci.77]. 328– 332 4 Baldwin. S. self-priming by herbivore-induced volatiles has been described in the context of airborne within-plant signalling [57.Review released volatiles affect systemic defence expression. but full activation of costly defence mechanisms is allowed only after confirmation by the vascular long-distance signal (Figure 1). 340–358 2 Green. and Dijkman. such as growth and reproduction. (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Priming provides an additional dimension to the delicate balance between defence expression and competing processes. 8399–8402 8 Dicke. Natl. whereas other defensive genes become primed for augmented induction to subsequent pathogen attack [76]. (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. are supported by a BBSRC Institute Career Path Fellowship (no. T. The same holds true for the nature of locally and systemically functioning signals. (1997) Quantification.R. A. Sci.75]. (1992) Systemic release of chemical signals by herbivore-injured corn. to achieve an optimized orchestration of the systemic defence response (Figure 1). H. 178. (2001) Within-plant circulation of systemic elicitor of induced defence and release from roots of elicitor that affects neighbouring plants. have been put forward as more likely candidates to mediate long-distance 270 Trends in Plant Science Vol. 89. while preventing defence reactions to false alarm signals. T. et al.61. Although the priming and induction of direct defence constitute different mechanisms of protection. the chance that eavesdropping by competing plants becomes a quantitatively relevant problem remains low. providing a carefully balanced systemic defence reaction to local attack by herbivores and pathogens. which fail to activate defences to their full extent. M. and the probability that the leaf nearest to an attacked one belongs to the same plant is relatively high. Hence. This so-called priming for defence has been associated with various induced resistance phenomena [76]. Acknowledgements We thank Christian Kost.13 No. Particularly at lower doses. and Dicke. Such an alternative mode of action can be explained by sensitization of the plant’s defence arsenal [57. (1961) Systemic acquired resistance induced by localized virus infection in plants. Mexico). M. 1075–1087 . J. which might differ amongst plant species. For instance. and have been shown to move in the vascular system. The major benefit of a within-plant signalling by volatiles is that they overcome the spatial and temporal restrictions of the vascular system. Conclusions and outlook JA and SA are crucial signals in the regulation of induced resistance to herbivores and pathogens. (1974) Assay and biochemical properties of the proteinase inhibitor inducing factor.F. gratefully acknowledges financial support from the German Research Foundation (DFG-grant He 3169/4–2) and from Consejo Nacional de Ciencia y ´ ´ Tecnologıa (CONACYT.A. Proc. C. but exposure to lower concentrations of volatiles. M. MeJA and MeSA. Leendert C. U. Such a two-step regulation provides additional fine-tuning of the systemic resistance response. I.J.H. MeJA and MeSA. it is plausible that resistance-inducing volatiles are often diluted to priming concentrations. Acad. Relatively high concentrations of volatiles can trigger defences directly [74]. 776–777 3 Ryan. BB/E023959/1). Virology 14. Planta 201. airborne signals can prime for defence. Priming prepares the plant to respond more rapidly and/or effectively to subsequent attack. Vascular and airborne signalling interact for optimal resistance expression The combination of internal and external pathways to achieve systemic defence activation provides plants with an interesting additional option for fine-tuning systemic resistance in yet-undamaged tissues. Although both transportation pathways can co-exist within the same plant. Plant Physiol. In fact.A. airborne signals prime distal tissues to respond more efficiently to vascular signals or direct attack. C. Volatile-mediated signalling is most effective over relatively short distances. Syst.T. Their volatile derivatives. and it can be activated by much lower concentrations of the resistance-inducing signal than those required to induce active defences fully [69.H. but they respond much faster or more strongly to wounding or infection than unprimed plants. and how the chemical properties of volatile signals affect the spatiotemporal pattern of systemic induction of resistance. New Phytol. (Kees) van Loon and three anonymous referees for valuable comments on earlier versions of this manuscript. C. This suggests a two-step regulatory system in which airborne and vascular signals interact. 41–61 6 Pieterse. 12. 564–569 7 Turlings. different plant species with different life styles will have to be considered if we are to gain a better understanding of the strategies by which plants optimize the induction of systemic resistance. correlations and manipulation of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. As a result. 29. the induction of pathogen-induced SAR activates some defence-related genes. M.C. both result in a phenotypically similar resistance to pathogens and herbivores. Given the fact that volatiles diffuse in the air and are dispersed by eddy currents. Science 175. Self-priming by airborne signals prepares the systemic tissues for a rapid response. A. References 1 Ross. In this model. as well as GLVs. 54.T. are released from damaged leaves and are mobile in the gas phase. thus preparing the distal organs for a more effective defence response rather than fully inducing them. and Tumlinson. Ecol. a wound hormone. 397–404 5 Heil. Therefore. their relative contribution to the overall response is likely to depend on the plant’s life history and anatomy. Plants combine vascular and airborne transport of the long-distance signals. and on the nature of the attacking organism. Biochem. Dosage-dependent effects also strongly reduce a putative ecological cost of external signalling: ‘eavesdropping’ by neighbours.6 regulation of induced resistance.73]. primed plants show no enhanced defence activity. however. Research activities of J. (2008) Indirect defence via tritrophic interactions.M. some inducedresistance phenomena are based on a combination of both mechanisms. Peter Bakker. Furthermore. and Ryan. probably to varying extents. can still affect resistance.

R. (2008) JAZing up jasmonate signaling. Proc. Mol. et al.I. U.F.Review 9 Bezemer. J. C. (2005) Linking aboveground and belowground interactions via induced plant defenses. is an induced. et al.C. L. J. Plant Cell 6. C. J. 453–483 40 Stenzel. 9–16 23 Kumar. Nature 448. G. 666–672 38 Staswick. and Dong. Oecologia 125. (2004) Systemic acquired resistance. 12. (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection.role of jasmonic acid. A. (1980) Induced systemic resistance to anthracnose in cucumber as influenced by the location of the inducer inoculation with Colletotrichum lagenarium and the onset of flowering and fruiting. (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. U. Rev. et al.and interplant communication. and Klessig. C. I. U.P.M. S. (1982) Comparison of the effects of salicylic acid and ethephon with virus-induced hypersensitivity and acquired resistance in tobacco. W. 55–68. (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc. Plant Pathol.). Ecol. E. and van Dam. Trends Plant Sci. (2007) Jasmonates: An update on biosynthesis.F. A. Natl. (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. 753–765 12 van Loon. J. A. et al. et al. U. (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants.C. (1997) Induced resistance in plants and the role of pathogenesis-related proteins. 367. I. M. Biochem. Planta 195. Nature 385. C. A.B. Acad. D. 98. C. 229–233 50 Mutikainen. and Constabel. 237–256 13 White. (2006) Members only: induced systemic resistance to herbivory in a clonal plant network. Plant Biol.and insect elicitorinduced gene expression.C. Natl. promotes transport of jasmonate. B. J. Rev. Ecol. I. Proc. et al.E. Plant Pathol. 1781–1785 271 . (2006) Molecular analysis of poplar defense against herbivory: comparison of wound. Proc. Acad. 1075–1080 27 Major. et al. and Pickett. Planta 226. In Plant Resistance to Insects (Hedin. S. (2007) Before gene expression: early events in plant– insect interaction. (2003) Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata. Natl. Nature 419. Natl. P. defensive response elicited by jasmonic acid. I. J.J. D. 436–441 43 Maffei. et al. 104. (2007) Plant defence signalling induced by biotic attacks.W. 185–209 15 Ton. I. and Baldwin. 15. 104. Proc. Phytopathol. 137. U. R. S. Plant J. Trends Plant Sci. et al. et al. Plant Biol. 29. New Phytol. Opin. 27–34 16 Malamy. syringae. D.E. 410–412 14 Durrant. 88. et al. Chem. M. Sci. 959–965 20 Shulaev. Plant Microbe Interact. 1342–1347 19 Vernooij. V. (1997) Transport of [2-14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. et al. A. 2393–2396 46 Orians. J. X. (2001) Surface-to-air signals. Phytopathol. Science 221. 16101– 16106 24 Park. J. 567–576 Trends in Plant Science Vol. Bot. 10. and Slusarenko. ed. (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. (2006) The wound response in tomato . (2004) Airborne signals prime plants against insect herbivore attack. an enzyme involved in floral scent production and plant defense. Acad. Eur.E. J-P. (2000) Vascular architecture generates fine-scale variation in the systemic induction of proteinase inhibitors in tomato. et al. Natl. et al.A. 2231–2242 45 Davis. (Lond. (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv.E. A. and Silva Bueno. and Howe. J. T. J. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. 9799–9802 34 Lee.E. Annu. (1991) Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. Biophys.R. Chem. Mol.) 100. M. (1994) Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. G. (1995) Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Acad. J. et al. J. and Stuefer. (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves.J. 97. 1004–1006 18 Rasmussen. et al. 87. 1002–1004 ´ 17 Metraux. Proc.F. 100. Arch. F. J. 33. Sci. growth and development. Acad. 66–71 54 Farmer. S. (1999) S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase.L. 593–600 33 McGurl. Plant Pathol. 512–515 61 Engelberth. 681–697 36 Thines. 17. (2005) Effects of feeding Spodoptera littoralis on Lima bean leaves. R. Proc. S. 33. 20. 31. Sci. U. A. 718–721 21 Forouhar.E. 91. Oecologia 147.M. Ann. G. U. (2004) Pathogen-induced resistance and alarm signals in the phloem. et al.M. I. 617–635 28 Heil. (2001) Extrafloral nectar production of the antassociated plant. et al. II. et al. 5.T. Plant Physiol. 387–392 11 van Loon. (2005) Systemic signaling in the wound response. 277–279 56 Rhoades. Acad. American Chemical Society 57 Heil. 541–551 42 Zhang. et al. A. 102. Ecol. Z-P. 840– 847 52 van Bel. F. et al. 854–856 59 Karban.A. 471–485 47 Schittko. G. 310–316 44 Orians. and Ryan. J. et al. 7713–7716 55 Baldwin. 172. L. Nature 411. Oecologia 108. Chem. Plant J. and Schultz. E. U. J. Acad. S. 1083–1088 ¨ 29 Mithofer.A. Sci. A. S. Annu. 13. (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves.T. 36. Curr. Nature 448. C. 369–377 31 Wasternack. Planta 203. (1979) Acetylsalicylic-acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Proc. 103. L. signal transduction and action in plant stress response. and Antoniw. (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Plant Physiol.F. Physiol. Natl. A. 113–116 25 Maldonado.T. (1990) Increase in salicylic acid at the onset of systemic acquired resistance. 661–666 37 Chini. 617–624 10 Bruce. B. S. Ecology 87. Science 250. W. 66–71 39 van Loon. U. 723– 727 51 Kiefer.E. Plant Pathol. and Gaupels. A.F.C. 922–930 60 Arimura.T. 495–504 53 Karban. and Baldwin. et al. (1998) Systemic resistance induced by rhizosphere bacteria. (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. P. (2006) Damage-induced resistance in sagebrush: volatiles are key to intra. Natl. Curr. indirect. vascular pathways. Plant Physiol. U.M. et al. et al. Opin. Proc. Eur. 1773–1778 22 Ross. Sci. 88. and Howe. pp. (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato — amplification in wound-signalling. 26. (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. S. et al. Macaranga tanarius. and systemic induction: facts and artifacts.6 35 Wasternack. 163. 42. (2005) Herbivores.. J. et al. (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Plant Physiol. et al. T. et al. Sci. S. (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acidstimulated lipase activity. 132. J. 101.C. represents a new class of plant methyltransferases. 461–468 49 Guedes. Science 250. 8. 297–306 ´ ´ 32 Narvaez-Vasquez. et al. A. S. Acad.A. Natl.W. J. A. 763–770 ´ 48 Gomez. Natl. and of photoassimilate even after proton transport is decoupled. A. M. B. (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. 399–403 26 Truman. P. 1160–1168 30 Schilmiller.J. (2002) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis.M. 5467–5472 58 Farmer. Acad. M. Virology 99. A. 577–589 41 Thorpe.M. Sci. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Nature 406. Science 318. (2007) 11C-imaging: methyl jasmonate moves in both phloem and xylem. Sci.13 No. Trends Ecol.A. (1996) Herbivore-induced resistance in Betula pendula: the role of plant vascular architecture. N. Evol. (2003) The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. (1983) Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. Sci.R.

U. Ecol. In Advances in Insect ´s. (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. et al. and Millar. E. pp. (1996) Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. K. Plant Pathol. et al. 55. C. Mol. Plant Cell 17. F. 10. et al. M. Biol. 35.C. J.T.C. et al. (2001) Systemic acquired resistance and salicylic acid: Me current state of knowledge. et al. 601–604 72 Campanacci.K. 6. Trends Plant Sci. J.13 No. 490–498 Baldwin. 276. 1062–1071 van Hulten. 20078– 20084 Frost. Plant Microbe Interact. Trends Plant Sci. 112. 103. 13–18 Cameron. J-P. V. (2006) Priming: getting ready for battle.G. Plant Pathol. S.E. 603–608 ´ 70 Almeras. 971–986 73 74 75 76 77 78 79 80 81 82 83 272 . Chem. C. Natl. 619–628 ¨ 63 Turlings. 121–130 ¨ Molders. (2006) Ethylene as a modulator of disease resistance in plants. S. U.A. (2003) Signaling of systemic acquired resistance in tobacco depends on ethylene perception. W. Physiol. 31. (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Chemical Ecology (Carde R. (2005) Role of b-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato.A. 9329–9334 69 Bruce. et al. A. 94. Acad. 34. eds). Acad. et al. J. 11. Ecol.J. Natl. J. T. Plant Sci. Ecol. Sci. (2006) Volatile signaling in plant–plant interactions: ‘talking trees’ in the genomics era. and Kleier. 173.J. Eur. 27–32 67 Ruther. (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. 21–75. J. (2005) Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)3-hexen-1-ol. et al. Chem. Chem. Plant Biol.. E. I. 103.L.J. et al. (2003) Long-distance run in the wound response — jasmonic acid is pulling ahead. Proc. 16–26 Conrath. J. J. 2217–2222 68 Birkett.6 with a fluorescence binding assay. T. (2007) Stressful ‘memories’ of plants: evidence and possible mechanisms. Acad.W. (2007) Priming by airborne signals boosts direct and indirect resistance in maize. (2008) Defence-inducing volatiles: in search for the active motif.Review 62 Kost. 19. tomato in Arabidopsis. 8. M. (2006) Costs and benefits of priming for defense in Arabidopsis. (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. et al. Natl. 49. Sci. Sci. 247–250 Li. Plant J.C. J. Plant J. 16672–16676 65 van Loon. U. L. 372–378 Stratmann. (2001) Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins Trends in Plant Science Vol. 97. et al. A. et al. Cambridge University Press 64 Shiojiri. et al. and Wackers. et al. Plant Physiol. A. 812–815 Ton. (2004) Recruitment of predators and parasitoids by herbivore-injured plants. M. M. 5602–5607 ´traux. et al. Proc. 184–191 66 Verberne. Plant J. Science 311. U. 34. (1999) Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. 107. et al. C. (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. et al. Mol. 205–216 71 Heil. M. Ecol. J. R. 787–792 Farmer. and Heil.T. S. S. Lett. Opin. Curr. (2007) Within-plant signalling by volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Proc.