Inducible indirect defence of plants: from mechanisms to ecological functions

Basic Appl. Ecol. 4, 27–42 (2003) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/baecol

Basic and Applied Ecology

Inducible indirect defence of plants: from mechanisms to ecological functions Marcel Dicke*, Remco M.P. van Poecke and Jetske G. de Boer Laboratory of Entomology, Wageningen University, The Netherlands

Received November 1, 2001 · Accepted February 15, 2002

Abstract Inducible defences allow plants to be phenotypically plastic. Inducible indirect defence of plants by attracting carnivorous enemies of herbivorous arthropods can vary with plant species and genotype, with herbivore species or instar and potentially with other environmental conditions. So far, inducible indirect defence has mostly been studied for simple linear food chains. However, ultimately, ecologists should address inducible indirect defence in a food web context, where more than one organism (different herbivores and pathogens) may attack a plant and where a plant that emits herbivore-induced volatiles is surrounded by other plants that emit odours that can mix with the herbivore-induced volatiles from the attacked plant. Evolutionary ecologists are interested in the costs and benefits of interactions between plants and their attackers. These may be investigated by comparing different plant genotypes. The best comparison is between plant individuals that differ in only a single or restricted number of known traits. Such genotypes are difficult to obtain by conventional methods. However, rapid progress in the study of mechanisms of plant-attacker interactions and in the field of molecular genetics and genomics provides new tools that can be exploited by ecologists. For instance, genomic knowledge on Arabidopsis thaliana and the availability of characterized mutants and transgenes that are altered in one or a restricted number of genes can be exploited to address functional aspects of inducible indirect defence. In this paper we review progress in the knowledge of mechanisms of inducible indirect defence of plants and its importance for investigating the functional aspects of plant responses to herbivorous arthropods. Finally we identify some of the ecological questions that can be addressed by exploiting mechanistic aspects of inducible indirect defence. Induzierbare Abwehr ermöglicht Pflanzen phänotypische Plastizität. Bei der induzierbaren indirekten Abwehr von Pflanzen gegen Herbivore werden carnivore Feinde der herbivoren Arthropoden angelockt. Diese indirekte Abwehrreaktion kann je nach Art und Genotyp der Pflanze variieren, je nach Art und Stadium der Herbivoren und potentiell auch mit anderen Umweltfaktoren. Bisher wurde induzierbare indirekte Abwehr zumeist in einfachen, linearen Nahrungsketten untersucht. Letztlich sollten Ökologen induzierbare indirekte Abwehr aber im Kontext von Nahrungsnetzen untersuchen und berücksichtigen, dass mehr als ein Organismus (verschiedene Herbivore und Pathogene) die Pflanze attackieren können. Weiterhin ist eine Pflanze, die durch Herbivorenbefall induzierte Düfte freisetzt, auch noch umgeben von anderen Pflanzen, die ebenfalls flüchtige Verbindungen abgeben, die sich mit den Düften der induzierten Pflanze mischen können. Evolutionäre Ökologen sind an den Kosten und Nutzen der Interaktionen zwischen Pflanzen und ihrer Angreifern interessiert. Kosten-Nutzen-Analysen können anhand eines Vergleichs verschiedener Genotypen durchgeführt werden. Am besten werden Pflanzenindividuen verglichen, die sich nur *Corresponding author: Marcel Dicke, Laboratory of Entomology, Wageningen University, P. O. Box 8031, NL-6700 EH Wageningen, The Netherlands, Phone: +31 317 484311, Fax: +31 317 484821, e-mail: [email protected]

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Dicke et al. in einem oder einer sehr begrenzten Zahl von Merkmalen unterscheiden. Solche Genotypen sind aber mit konventionellen Methoden schwer erhältlich. Aber die schnellen Fortschritte sowohl bei den Studien der Mechanismen von Pflanzen-Angreifer-Interaktionen als auch in der Molekulargenetik und Genomforschung eröffnen neue Möglichkeiten, die auch von Ökologen genutzt werden können. Um funktionale Aspekte der induzierbaren indirekten Verteidigung zu analysieren, kann man z.B. die Kenntnisse zum Genom von Arabidopsis thaliana nutzen sowie die Verfügbarkeit bestimmter Mutanten und transgener Individuen von A. thaliana, die nur in einem Gen oder einer bestimmten Anzahl von Genen verändert sind. Diese Publikation gibt einen Überblick der Kenntnisse über die Mechanismen der induzierbaren indirekten Verteidigung von Pflanzen und ihre Bedeutung für Analysen funktionaler Aspekte der pflanzlichen Reaktionen auf herbivore Arthropoden. Abschließend verweisen wir auf ökologische Fragen, die man untersuchen kann, wenn man mechanistische Aspekte der induzierbaren indirekten Antwort nutzt. Key words: predators – parasitoids – infochemicals – induced plant odours – environmental genomics – transgenes – Arabidopsis – food web

Introduction Plants are exposed to a daunting variety of potential attackers such as herbivorous insects, mites, nematodes and vertebrates, and pathogenic fungi, bacteria and viruses. Although plants have constitutive defences, an important strategy is to initiate defences in response to attack (Karban & Baldwin 1997). Inducible defence may have several advantages such as reducing biosynthetic costs of defence or avoiding that other organisms can exploit the defence to their own benefit (Karban & Baldwin 1997, Cipollini et al. 2003, Zangerl 2003). In addition, variation in plant phenotype that is caused by inducible defence may reduce the chances that attackers adapt to plant defences (Agrawal & Karban 1999). Inducible changes in plant phenotype can affect organisms at different trophic levels such as herbivores, carnivores, pollinators and detritivores, and consequently generate changes in food webs. Whether the change in phenotype results in a net benefit to the plant, depends on the total of changes in the local food web. For instance, herbivore-induced plant volatiles may attract carnivorous enemies of the inducing herbivore, but also other herbivores (Dicke & Vet 1999). If the plant emits the volatiles in an environment with ample numbers of effective carnivores, then the emission can significantly improve plant fitness (Dicke & Sabelis 1992, van Loon et al. 2000, Fritzsche-Hoballah & Turlings 2001). However, in a carnivore-free but herbivoredense environment, the net effect on plant fitness may be negative. Furthermore, the responses of one organism to the induced plant volatiles may depend on the responses of other organisms. For example, the predatory mite Phytoseiulus persimilis avoids odours from a prey patch invaded by competitors when an uninvaded prey patch is offered as alternative (Janssen et al. 1997). The costs and benefits of herbivore-induced plant volatiles will therefore be frequency- and density-

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dependent and thus be influenced by the ecological context. Inducible defences can be classified as direct defences that affect the herbivore’s biology directly and indirect defences that affect the herbivore through its natural enemies (Dicke & Vet 1999). This paper deals with inducible indirect defences. Inducible indirect defences comprise the induced production of extrafloral nectar (Heil et al. 2001, Wäckers et al. 2001) that is exploited as food source by carnivorous arthropods as well as the induced production of plant volatiles that attract carnivorous arthropods (Turlings et al. 1995, Sabelis et al. 1999, Dicke & van Loon 2000; Fig. 1). Most knowledge is available on inducible plant volatiles and this paper deals exclusively with this type of inducible indirect defence. Plant volatiles can be induced by various types of herbivores, such as folivorous chewing herbivores (e.g. Turlings et al. 1990, Mattiacci et al. 1994), folivorous sucking herbivores (e.g. Dicke et al. 1990b, Venzon et al. 1999), sap sucking herbivores (e.g. Drukker et al. 1995, Du et al. 1998), leaf miners (e.g. Dicke & Minkenberg 1991, Finidori-Logli et al. 1996), stemborers (e.g. Potting et al. 1995), root feeders (e.g. Boff et al. 2001, van Tol et al. 2001). Even herbivore oviposition can induce the emission of carnivore attracting volatiles (Meiners & Hilker 2000). When investigating inducible indirect defences one may concentrate on mechanisms, such as those related to the process of induction of the plant defence or the response of the carnivore. Alternatively, one may be interested in the evolution of inducible defences and the costs and benefits that mediate the ecology. However, rather than developing these approaches in isolation, there is a large benefit of taking an integrated approach that can significantly advance our understanding of inducible indirect defence. This will be the topic of this paper.

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Fig. 1. Plants that are damaged by herbivorous arthropods respond with the emission of induced volatiles that attract predators or parasitoids. A. Spider mite infested Lima bean plants attract more predatory mites than uninfested plants. B. Pieris infested cabbage plants attract more parasitoids than uninfested plants. Based on Sabelis & van de Baan 1983, Dicke et al. 1990b, Steinberg et al. 1992, Mattiacci et al. 1994.

Mechanisms and functions Evolutionary ecologists are interested in the costs and benefits of interactions between organisms, and express these ultimately in terms of fitness, such as viable offspring production. Thus, they are interested in trade-offs such as growth versus defence, direct defence vs. indirect defence or defence against herbivores vs defence against pathogens (Fig. 2). To understand the costs and benefits of inducible indirect defence through herbivore-induced plant volatiles, one needs to study all interactions that are mediated by these infochemicals. This relates to interactions between plants and carnivores, plants and herbivores, and plants and other plants. Each of these three groups of interactions may comprise a range of interactions between individuals of different species. In fact, after the emission of the infochemicals has taken place, the

plant is no longer in control of who receives the volatiles. Any organism in the environment can potentially exploit the cues. Two approaches can be used to investigate the costs and benefits: (1) costs and benefits are quantified separately for all individual interactions (Dicke & Sabelis 1992) and (2) plants of different treatments are placed in natural communities to investigate the combined effect of different interactions (e.g. Baldwin 1998, Kessler & Baldwin 2001). These two

Fig. 2. Tradeoffs in growth and defence against different attackers.

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approaches are not mutually exclusive. Investigating individual interactions in the laboratory provides detailed knowledge on each of the interactions. This knowledge is valuable information on potential costs and benefits of plant characteristics as well as on the mechanisms underlying these costs and benefits. However, it remains unknown how frequent the studied interactions occur in nature and how a combination of interactions affects costs and benefits to the plant. For manipulative field experiments, the manipulations may be chosen on the basis of the knowledge gained from laboratory experiments (e.g. Baldwin 1998) and if sufficient knowledge is available on the local species composition of the community one might predict what outcome will be obtained. If the prediction fails, one may devise new manipulative experiments to test new hypotheses. On the other hand, when plants are placed in a natural environment without knowledge on the effects of individual interactions, one may get realistic knowledge given the local conditions. Such data from field experiments will reveal which potential interactions are the most important and so which costs and benefits are likely to dominate over others. This may vary in time and space. However, without extensive knowledge on mechanistic aspects of plant-animal interactions, it remains obscure how these costs and benefits are attained and how they may change when local conditions change. To gain knowledge on functional aspects, one needs to have information on mechanisms. To start with, mechanistic knowledge is essential to understand the interactions that take place. For instance, mechanistic knowledge was essential to elucidate that attraction of carnivorous arthropods to herbivore-infested plants was mediated by plant-produced volatiles rather than by herbivore-produced volatiles (Dicke et al. 1990a). This information provided the basis for evolutionary questions, such as why do plants produce these volatiles, what are the benefits in terms of fitness, what are the plant’s strategies (Dicke & Vet 1999)? Furthermore, mechanistic information is essential to allow manipulative experiments under laboratory or field conditions (e.g., Potting et al. 1995, Baldwin 1998, Dicke et al. 1999, Turlings & Fritzsche 1999). Below, we will address the most important mechanisms and functions of inducible indirect defence. Mechanisms Mechanistic aspects of induced indirect defence relate both to the process of induction in the plant and the process of perception and response in carnivorous arthropods. These mechanistic aspects will be reviewed below.

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Inducible responses to a range of attackers The induction of plant volatiles is characterized by a large degree of variation. Induced blends of plant volatiles are emitted locally at the wounded site, and systemically from undamaged plant tissue; the local response may differ from the systemic one (Paré & Tumlinson 1997). The induced blends are complex mixtures of up to 200 compounds (e.g., Turlings et al. 1995, Dicke et al. 1998, Krips et al. 2001) and the composition of the blend may vary with e.g. (a) type of attack, such as mechanical damage by wind, attack by herbivores or attack by pathogens, (b) plant genotype, (c) plant tissue or potentially abiotic conditions (Takabayashi et al. 1994, Takabayashi & Dicke 1996). In many cases, plants emit compounds in response to herbivory that they do not produce in response to mechanical wounding (Dicke 1999b; Fig. 3) and these compounds are biosynthesized de novo (Paré & Tumlinson 1997). For instance, upon herbivory Lima bean plants emit several terpenoids and methyl salicylate. These compounds are not emitted by mechanically damaged Lima bean plants, or only in trace amounts (Dicke et al. 1990b, Dicke et al. 1999). The emission of one of the terpenoids, 4,8-dimethyl-1,3(E),7–nonatriene, was shown to be the result of de novo biosynthesis (Donath & Boland 1995, Bouwmeester et al. 1999). Plants may respond differently to different types of attackers. When plants are infested by different herbivore species, usually the same compounds are induced but in different ratios, and carnivores can (learn to) discriminate between blends induced by different herbivore species (Dicke 1999c). To be able to respond differently to different attackers, plants should be able to recognize different types of attackers. Plants may recognize herbivore oviposition through elicitors in the oviduct secretion (Hilker & Meiners 2002). Oral secretions from herbivores enable the plant to recognize herbivore feeding damage from mechanical damage and several elicitors in herbivore oral secretions have been identified such as fatty-acid amino-acid conjugates and enzymes (Mattiacci et al. 1995, Alborn et al. 1997, Felton & Eichenseer 1999, Halitschke et al. 2001). Differences in oral secretions may be exploited by plants to respond differentially to damage by different herbivore species. Plants even appear to emit different volatile blends in response to infestation by different herbivore instars and differential composition of the oral secretions is likely to play a role in this differential induction (Takabayashi et al. 1995). All arthropod elicitors that have been identified to date can induce volatile production, except for glucose oxidase that was identified in the oral secretion of Helicoverpa zea and other caterpillars and that induces direct defences in plants (Felton & Eichenseer 1999).

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Fig. 3. Induced responses of Lima bean to mechanical damage and to herbivory by spider mites. DMNT= 4,8-dimethyl-1,3(E),7-nonatriene; JA= jasmonic acid; LOX= lipoxygenase; MeSA = Methyl salicylate; OPDA= 12-oxo phytodienoic acid; SA= salicylic acid; TMTT = 4,8,12-trimethyl-1,3(E),7(E),11-tridecatetraene. Solid lines refer to proven effects; stippled lines have not been proven but suggested. Based on data from Dicke et al. 1990b, Dicke et al. 1999, Koch et al. 1999.

Symbiotic microorganisms may play a role in the induction of plant volatiles by herbivory and their influence may be greater than currently appreciated. The elicitors that induce the volatiles may be a product of microorganisms in the herbivore’s gut (Spiteller et al. 2000). Knowledge on the mechanism of induction will be important to understand the selection pressures that affect plant-herbivore interactions that result in the production of the volatiles induced by herbivory. It remains unknown whether infestation with pathogens results in the emission of carnivore attractants, but there is evidence that pathogen infection results in volatile emission (Croft et al. 1993, Doughty et al. 1996, Cardoza et al. 2002). In bean plants (Phaseolus vulgaris), an infection with the bacterium Pseudomonas syringae induces fatty-acid derived volatiles (Croft et al. 1993). In contrast, an infestation of the same plant species and variety with the spider mite T. urticae results in a blend that is dominated by terpenoids (Dicke 1999d). In peanut plants a fungal pathogen induces some compounds that are also induced by beet armyworm (Spodoptera exigua) feeding (Cardoza et al. 2002). Elicitors from plant pathogens have been reported to induce plant volatiles. Among

these are e.g. cellulysin (Piel et al. 1997) and alamethicin, a mixture of the peptaibols, that are produced by the fungus Trichoderma viride and many other microorganisms (Engelberth et al. 2000). Possibly microorganisms in insect guts may produce such compounds as well and thereby contribute to the induction process. The peptaibols (oligopeptides) act as ion-channel forming compounds and are considered to mediate a very early step in the induction. In Lima bean they induce the transient production of jasmonic acid and subsequently of salicylic acid (SA). The latter phytohormone is produced at a high level for a long period of time. It is interesting to see that administration of the peptaibol alamethicin results both in a high level of SA in the plant and in the emission of methyl salicylate (MeSA). In addition to MeSA, the only other compounds emitted are the two homoterpenes 4,8dimethyl-1,3(E),7-nonatriene and 4,8,12-trimethyl1,3(E),7(E),11-tridecatetraene. This indicates that the induced SA inhibits the octadecanoid pathway beyond 12-oxo phytodienoic acid (OPDA) (Engelberth et al. 2000), as this octadecanoid intermediate indu ces the production of the two homoterpenes (Boland et al. 1999).

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Because induced volatile blends are complex mixtures of tens to more than 100 compounds (Dicke 1999b), it will be interesting to investigate whether different elicitors or different combinations of elicitors result in differential responses to feeding damage by different herbivore species, but first evidence supports this (Koch et al. 1999). Elucidation of the mechanisms that underly the specificity of induction will help to investigate whether, when and how plants provide carnivorous arthropods with specific information on the type of attacker. This information is important to understand the selection pressure on carnivores to exploit the specificity of plant cues so as to maximize their searching efficiency. Not all plants have the same degree of specificity in the induced volatile blends. Some plant species emit major novel compounds that dominate the volatile blend, in response to herbivory when compared to mechanically damaged or undamaged conspecifics. Other plant species emit qualitatively very similar blends in response to herbivore damage or artificial damage, although the total amount and the relative contribution of each component may differ (Dicke 1999b). This different degree in specificity may be related to the number of herbivore species that may attack a plant species: plants that have a large diversity of attackers may have evolved to emit more specific blends than plants that have a low diversity of attackers (for discussion see Dicke & Vet 1999). Plant genotypes differ in the emission of herbivoreinduced plant volatiles in response to the same herbivore species (e.g. Loughrin et al. 1995, Gouinguené et al. 2001, Krips et al. 2001). This may represent an additional source of variation in the volatile blend that carnivorous arthropods are faced with. However, to date the variation in volatile blends among genotypes that share the same (micro)habitat has remained unstudied as well as how this variation compares to variation as a result of induction by different attackers. Especially the variation in volatile-emission among cooccurring plant genotypes and the effect of this variation on attraction of carnivores may be an important component of the relative effectiveness of infochemical emission in reducing herbivory damage and consequently of relative fitness. Signal transduction pathways involved in volatile induction Inducible defences are mediated by the activation of different signal-transduction pathways in the plant. This leads from damage and interaction with elicitors in herbivore oral secretion to the induced production of volatiles. The three main signal transduction pathways are (1) the octadecanoid pathway with jasmonic

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acid (JA) as one of the key compounds, (2) the shikimic acid pathway with salicylic acid (SA) as a key compound and (3) the ethylene pathway. These signal-transduction pathways are involved in the induction of direct and indirect defences. Most knowledge has been gained for their involvement in inducible direct defence against pathogens and herbivorous arthropods (for reviews see Karban & Baldwin 1997, Pieterse & van Loon 1999, Dicke & van Poecke 2002). The three signal transduction pathways are also involved in inducible indirect defence (Dicke & van Poecke 2002, Horiuchi et al. 2001). In general, the octadecanoid pathway seems to be the most important signal-transduction pathway involved in inducible defence against herbivorous arthropods (Hopke et al. 1994, Dicke et al. 1999, Thaler 1999, Ozawa et al. 2000a), but the shikimic acid pathway and the ethylene pathway can play a role as well (Dicke et al. 1990b, Engelberth et al. 2000, Kahl et al. 2000, Ozawa et al. 2000a, Horiuchi et al. 2001). To date, little is known about how plants co-ordinate signalling in response to different attackers. A common hypothesis is that this is accomplished by differences in the relative activation of the different pathways. The shikimic acid pathway is activated more in response to microbial pathogens and the octadecanoid and ethylene pathways are more activated in response to non-pathogenic rhizobacteria and herbivores (Pieterse & van Loon 1999, Thaler et al. 1999, Engelberth et al. 2001). Evidence is accumulating that components from SA-, JA-, and ethylene-dependent defence pathways can affect each other’s signalling. This cross-talk between pathways provides a great regulatory potential for activating multiple defence mechanisms in varying combinations. For instance, JA and ethylene act in concert in activating genes encoding proteinase inhibitors that defend the plant against herbivores (O’Donnell et al. 1996, Penninckx et al. 1998) and in inducing some plant volatiles in response to herbivory (Horiuchi et al. 2001). Negative interactions have been reported as well. For instance, SA suppresses JA-dependent defence responses (Stout et al. 1999, Thaler et al. 1999, van Wees et al. 1999, Engelberth et al. 2000). Conversely, JA and ethylene have been shown to stimulate SA action (Lawton et al. 1994). Signalling compounds can affect direct and indirect defences differently: ethylene can suppress the induction of direct defence without negative effects on the induction of indirect defence (Kahl et al. 2000). Cross-talk between different signalling pathways may help the plant to prioritise the activation of a particular defence pathway over another, leading to the activation of optimal defence against the attacker(s) (Reymond & Farmer

Inducible indirect defence of plants: from mechanisms to ecological functions

1998, Kahl et al. 2000, Pieterse & van Loon 1999). However, cross-talk may also be exploited by herbivores to block anti-herbivore defences by inducing anti-pathogen defences (Bi et al. 1997). Induction of biosynthetic pathways

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Herbivory can also induce the production of methyl salicylate. This has been recorded for a large number of plant species among which Lima bean, apple, tobacco and pear (Dicke et al. 1990b, Takabayashi et al. 1991, Scutareanu et al. 1997, Kessler & Baldwin 2001, van den Boom et al. 2002). Jasmonic acid (JA) is

The mixtures of volatiles that plants emit in response to herbivory, consist of compounds from various groups that are produced through a few main biosynthetic routes (Karban & Baldwin 1997, Paré & Tumlinson 1997, Dicke & van Poecke 2002). Although the general aspects of the biosynthetic routes are known, specific aspects, especially those related to the induction of biosynthesis, remain poorly known. For some of the induced chemicals more knowledge has been gained on the biosynthesis (Donath & Boland 1994, Bouwmeester et al. 1999, Degenhardt & Gershenzon 2000, Frey et al. 2000). For instance, a nerolidol synthase likely mediates the first dedicated step in the induced biosynthesis of the homoterpene (E)-4,8dimethyl-1,3,7-nonatriene (Bouwmeester et al. 1999, Degenhardt & Gershenzon 2000). Enzyme activity is strongly induced in lima bean and cucumber plants by spider mite feeding, but not by artificial damage (Bouwmeester et al. 1999). Based on this knowledge and information on genes encoding for terpene synthases (Bohlmann et al. 1998), the gene encoding for nerolidol synthase can be isolated. This will provide an interesting tool to investigate the role of (E)-4,8dimethyl-1,3,7-nonatriene in the ecology of plant-carnivore interactions.

Fig. 4. Induced blend of volatiles emitted by Lima bean plants in response to (a) spider mite infestation (50 adult females per leaf, 2 days of infestation) and (b) application of jasmonic acid (1 mM, 3 days of exposure). Undamaged control plants emit very low amounts of a limited number of compounds (Dicke et al. 1999). Compound numbers: 1= 2= 3= 4= 5= 6= 7= 8= 9= 10 = 11 = 12 = 13 = 14 = 15 = 16 = 17 = 18 = 19 = 20 = 21 =

2-methyl-propanal-O-methyloxime 2-methyl-butanal-O-methyloxime 3-methyl-butanal-O-methyloxime 2-methyl-propane nitrile 2-methyl-butane nitrile 3-methyl-butane nitrile 2-penten-nitrile rose furan 2-methyl-2-propenal hexanal (E)-2-hexenal octanal nonanal decanal 2-butanone 3-buten-2-one 3-pentanone 3-methyl-3-buten-2-one 1-penten-3-one 3-heptanone 3-octanone

22 = 23 = 24 = 25 = 26 = 27 = 28 = 29 = 30 = 31 = 32 = 33 = 34 = 35 = 36 = 37 = 38 = 39 = 40 = 41 = 42 =

1-butanol 2-butanol 2-methyl-3-buten-2-ol 1-penten-3-ol 1-pentanol (Z)-3-hexen-1-ol 1-octen-3-ol 1-nonanol 3-methyl-butanol acetate pentyl acetate hexyl acetate (E)-3-hexen-1-ol acetate (Z)-3-hexen-1-ol acetate (E)-2-hexen-1-ol acetate (Z)-3-hexen-1-ol butanoate (Z)-3-hexen-1-ol 2-methylbutanoate myrcene (Z)-β-ocimene (E)-β-ocimene 4,8-dimethyl-1,3(Z)-7-nonatriene 4,8-dimethyl-1,3(E)-7-nonatriene

43 = 44 = 45 = 46 = 47 = 48 = 49 = 50 = 51 = 52 = 53 = 54 = 55 = 56 = 57 = 58 = 59= 60 = 61 =

allo-ocimene α-copaene linalool α-bergamotene β-caryophyllene 4,8,12-trimethyl-1,3,7,11-tridecatetraene isomer 4,8,12-trimethyl-1,3(E),7(E),11-tridecatetraene methyl salicylate jasmone benzyl cyanide indole unknown 55,83,84B unknown 91B,107,135 unknown 91,93,95B,150 unknown 41,55,69,70B,83,134 unknown 41,69B,79,95,109,149,164 unknown 41,69B,107,147,218 unknown 43B,79,93,94,148,151,166 unknown 67,71,82B

Based on Dicke et al. 1999.

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not involved in the induced production of methyl salicylate. JA application to Lima bean plants results in the emission of a volatile blend that is similar but not identical to the blend emitted in response to spider mite infestation (Fig. 4). The main difference is that methyl salicylate and 4,8,12-trimethyl-1,3(E),7(E),11tridecatetraene are not emitted in response to JA (Dicke et al. 1999). The induction of 4,8,12-trimethyl1,3(E),7(E),11-tridecatetraene is mediated by another intermediate of the octadecanoid pathway, i.e. OPDA (Koch et al. 1999) and OPDA treatment of Lima bean plants results in the induction of attraction of the predatory mite Phytoseiulus persimilis (Dicke & van Poecke 2002). Detailed knowledge of the biosynthetic pathways that are induced will enable to devise manipulative experiments with plants that are altered in these pathways and thus enable to investigate the functions of the produced volatiles. Large scale patterns in gene expression Inducible defences rely on the flexible expression of genes. By altering gene expression patterns, plants can change phenotype. Information on gene expression has initially become available especially for genes involved in inducible direct defences (e.g. Karban & Baldwin 1997, Baldwin & Preston 1999, Pieterse & van Loon 1999, Ryan 2000). Knowledge on the genes involved in the signalling pathways and biosynthetic routes that are part of inducible defence allow to monitor the gene-expression patterns under different experimental conditions (e.g. Hermsmeier et al. 2001). Moreover, rapid developments in molecular biology provide opportunities to monitor the expression choreography of much larger numbers of known or unknown genes (e.g., Arimura et al. 2000, Reymond et al. 2000, Schenk et al. 2000, Hermsmeier et al. 2001, Stintzi et al. 2001). Subsequently, patterns in gene-expression can be identified in response to wounding or elicitor treatment, but also new genes can be identified (Aharoni et al. 2000). Shifts in gene-expression patterns include the downregulation of genes involved in photosynthesis and the upregulation of many genes involved in responses to stress, wounding and pathogens and genes involved in shifting carbon and nitrogen to defence (Hermsmeier et al. 2001), This approach is open to plants for which abundant genomic information is available such as Arabidopsis (e.g. Reymond et al. 2000), but also to plants for which much less genomic knowledge is available as yet, such as tobacco, strawberry and Lima bean (e.g. Aharoni et al. 2000, Arimura et al. 2000, Hermsmeier et al. 2001). These developments can be highly important to functional studies because they provide insight into the shifts in investments

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of plants, such as the relative investments in growth and defence (cf. Herms & Mattson 1992), the relative investment in defence to pathogens and to herbivores (Thaler et al. 1999) and the relative investments in direct and indirect defence (Dicke 1999a, Kahl et al. 2000) (Fig. 2). A first important result of these studies is that herbivory results in expression changes of large numbers of genes, including defence genes. Functional genomics and inducible indirect defence of plants In the era of molecular biology, the study of multitrophic interactions and inducible defences should take advantage of the wealth of knowledge that is gained by genomic projects. Recently, the first complete plant genome has been unraveled, i.e. the Arabidopsis thaliana genome (Kaul et al. 2000). Many mutants and transgenes of this brassicaceous plant have been characterized that are modified in signal transduction pathways involved in induced defence. These mutants and transgenics are important tools for a functional genomics approach to inducible defences against insects. It is becoming clear that Arabidopsis can be a suitable plant to study insect-plant interactions (Grant-Petersson & Renwick 1996, McConn et al. 1997, Stotz et al. 2000) and this plant species has also proven to be a suitable model for the study of inducible indirect defence against insects (van Loon et al. 2000, van Poecke et al. 2001). Therefore, the adoption of Arabidopsis as a model species of inducible indirect defence can significantly advance our understanding of insect-plant interactions. A functional genomics approach should be followed by an environmental genomics approach in which the function of plant genes is investigated with respect to the effect on a plant’s phenotype related to its interactions with biotic and abiotic environmental stress. To do so, the development of DNA-microarrays can be exploited by ecologists to monitor gene expression patterns of plants under field conditions. The knowledge gained on Arabidopsis may be exploited for similar studies on other plant species, especially in the Brassicaceae (Agelopoulos & Keller 1994, Blaakmeer et al. 1994, Geervliet et al. 1994, Mattiacci et al. 1995, van Poecke et al. 2001, Shiojiri et al. 2002). Moreover, several plant species in other plant families are likely to become useful model species too, such as tomato and tobacco for solanaceous plants (e.g. Howe et al. 1996, Hermsmeier et al. 2001), Lotus for legumes (e.g. Kawasaki & Murakami 2000, Ozawa et al. 2000b) and rice for cereals (Liu et al. 2001). Knowledge on genomics of and research on each of these species may stimulate ecological studies in related wild species.

Inducible indirect defence of plants: from mechanisms to ecological functions

Perception and responses by carnivores The identification of those herbivore-induced plant volatiles that result in the attraction of carnivores has been a difficult task. For only a few systems some behaviourally active components of the total blend are known, i.e. for two parasitoid wasps, one specialized predatory mite and one anthocorid predatory bug (Dicke et al. 1990b, Turlings et al. 1991, Scutareanu et al. 1997, Du et al. 1998, Turlings & Fritzsche 1999). However, the complexity of the volatile blends, complicates a behavioural approach because of the many combinations of compounds that may be tested. Fractionation of the total blend may provide an option (Turlings & Fritzsche 1999), but when very different compounds have a synergistic or antagonistic effect this may lead to new complications. An approach that combines gas chromatography with electrophysiology can reveal those compounds that are perceived by chemoreceptors at the periphery, i.e. on arthropod antennae or legs. For some systems such knowledge on electrophysiological activity of blend components is available (De Bruyne et al. 1991, Du et al. 1996, Weissbecker et al. 2000). However, the knowledge on how insects perceive, evaluate and respond to complex and variable mixtures of volatiles is still rudimentary. Knowledge on the mechanisms of induction may be used to develop new methods to investigate which components of an induced blend are important for a searching carnivore. Different elicitors can be applied to plants that induce different subsets of the total blend (e.g. Dicke et al. 1999, Koch et al. 1999). In this way one may produce a complex blend that overlaps to a certain extent with the natural blend (Dicke et al. 1999) and subsequently one may add one or more synthetic components. In this way we have demonstrated the importance of methyl salicylate in the spider-mite induced blend of Lima bean plants in the attraction of the predatory mite Phytoseiulus persimilis (De Boer & Dicke 2002). Functions Herbivore-induced plant volatiles that attract carnivorous arthropods mediate potentially mutualistic interactions. However, plants and carnivores each have their own interests and strategies. Furthermore, there may be other organisms that respond to the volatiles and consequently influence the costs and benefits for plant and carnivore. These functional aspects are reviewed below. Herbivore-induced plant volatiles in different backgrounds Herbivore-induced plant volatiles may potentially affect many different organisms in the environment such

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as herbivores, carnivores, pollinators and other plants. The sum of all these interactions determines whether the emission of induced volatiles has a net benefit in terms of fitness. Moreover, the plant may emit volatiles in response to more than one attacker or an individual plant may emit the volatiles amidst other plants that emit volatiles in response to the same or different attackers. Two plants of the same species that are each infested by a different herbivore species may be discriminated by carnivorous arthropods on the basis of the emitted volatiles (for review see Dicke 1999c). This is functional for the carnivore, especially when it is a specialist that can only successfully attack one of the herbivore species (e.g. Du et al. 1998). However, how does a plant respond when infested by individuals of two herbivore species? Does it emit a mixture of the two blends, does the induction by one herbivore dominate the induction by the other? A first study has recently published data in this context. In response to an infestation by a pathogenic fungus followed by an insect herbivore, peanut plants seem to respond in an additive way (Cardoza et al. 2002). Some first data have become available on the effect of mixed herbivore infestations on carnivore foraging behaviour. For instance, the attraction of the parasitoid Cotesia glomerata to host (Pieris rapae) infested cabbage plants is hampered in a habitat in which nonhost herbivores (Plutella xylostella) occur, compared to a habitat without this non-host (Shiojiri et al. 2000, Vos et al. 2001). The volatiles emitted by cabbage plants infested by different herbivore species are very similar (Geervliet et al. 1997) and this may explain the disturbing effects. However, it is interesting to note that another parasitoid (C. plutellae) is not disturbed by mixing of odours in this system (Shiojiri et al. 2000). Moreover, whether an infestation with two herbivores hampers foraging by a predator or not, can also depend on the specific combination of the two herbivore species (Gnanvossou et al. 2002). These examples illustrate that the effects of mixing odour sources can have various effects that are context-specific. A plant that emits herbivore-induced volatiles will be surrounded by neighbours that emit constitutive or induced odours. These neighbouring emitters can be conspecific or heterospecific. Heterospecific plants emit very different odour blends than conspecific plants (e.g. Dicke 1999c). The ability of herbivores to locate food plants on the basis of plant volatiles can be seriously hampered by mixing of odour blends (Thiery & Visser 1986). How is the searching behaviour of carnivores affected by volatiles emitted by neighbours from prey-infested plants? Some initial data for the predatory mite Phytoseiulus persimilis show that this

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predator is not hampered when lima bean plants infested with its prey Tetranychus urticae are surrounded by cabbage plants infested by Pieris brassicae caterpillars (Dicke et al. 2002). In this particular case the two odour blends are very different in composition (Mattiacci et al. 1994, Dicke et al. 1999). It remains to be investigated what happens when the two odour sources are more similar in composition. This can be investigated through experiments that exploit the knowledge on the composition of herbivore-induced odour blends. If the host plant community that surrounds a plant influences the attraction of carnivorous enemies of herbivores, then plant communities may determine whether a plant is a potential enemy-free or enemy-dense niche to herbivores. This is expected to affect the evolution of host plant selection by herbivores (Ohsaki & Sato 1994). Finally, we need to know whether carnivores can locate their herbivorous victims under field conditions where the induced plant volatiles are certainly mixed with background odours. There are several reports on field data (e.g. Drukker et al. 1995, Shimoda et al. 1997, De Moraes et al. 1998, Kessler & Baldwin 2001), but only one of these (Kessler & Baldwin 2001) is done in a natural background instead of in a background that consists of an agricultural monocrop situation. This latter field study used plant manipulations that were based on mechanistic knowledge of induced volatile production by the plant under investigation. Eggs of Manduca sexta were placed on control plants, and on plants induced with the methyl ester of jasmonic acid (methyl jasmonate – MeJA) to mimic herbivory or on plants to which individual plant volatiles were added in a lanolin paste. Egg survival caused by natural enemies was significantly reduced on MeJA treated plants and on plants treated with (Z)-3-hexen-1-ol, or linalool or cis-α-bergamotene (Kessler & Baldwin 2001). This study shows that certain induced plant volatiles are effective in attracting carnivorous arthropods under field conditions. Inducible indirect defence and plant fitness Carnivorous arthropods can have important effects on herbivore population dynamics. For instance, predatory arthropods can exterminate local populations of their prey and this benefits individual plants (Sabelis & Dicke 1985). With regard to the evolution of inducible versus constitutive defenses, the costs and benefits as well as the predictability of plants as resources for herbivores have been addressed (Dicke & Sabelis 1989, Adler & Karban 1994, Agrawal & Karban 1999, Dicke 1999b, Dicke & Vet 1999, Sabelis et al. 1999, Cipollini et al. 2003, Zangerl 2003).

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Both for predators and parasitoids there is ample evidence for attraction to herbivore-induced plant volatiles. The benefits of induced volatiles for the carnivores are obvious because these volatiles are highly detectable foraging cues, while the herbivore itself hardly emits information that can be exploited by their carnivorous enemies (Vet & Dicke 1992). Biosynthetic costs of herbivore-induced plant volatiles seem to be low, but ecological costs may be considerable (Dicke & Sabelis 1989). For instance, herbivores may be attracted to the induced volatiles (Dicke & Vet 1999) and consequently, if no (effective) carnivores are in the habitat, the induced volatiles may have a severe cost. Furthermore, neighbouring plants may exploit the volatiles to their own benefit (Bruin et al. 1995) and if this results in a competitive advantage (van Dam & Baldwin 1998) this may be an important cost to the volatile-emitting plant. Herbivorous arthropods are known to use herbivore-induced plant volatiles during selection of host plants (see Dicke & Vet 1999, Hilker & Meiners 2002 for review). Many herbivore species are attracted to herbivore-induced plant volatiles, but in other cases repellence has been recorded (Dicke 1986, Bernasconi et al. 1998, De Moraes et al. 2001, Kessler & Baldwin 2001). Herbivores may include many other sources of chemical information in addition, such as information from competing herbivores or from their natural enemies (see Dicke 2000, Nufio & Papaj 2001, Prokopy & Roitberg 2001 for reviews). So far, the investigations of herbivore-induced plant volatiles have focussed more on the responses of carnivores than on the responses of herbivores. However, the attraction of herbivores may constitute a significant cost to plants and, therefore, more investigations on this aspect are needed. The benefits to plants of attracting carnivores, especially parasitoids, have been recently questioned (Coleman et al. 1999, van der Meijden & Klinkhamer 2000). Parasitoids, in contrast to predators, do not remove the herbivore from the plant but after parasitisation the herbivore continues to feed and this may occur at a rate higher than for unparasitized herbivores (Slansky 1978, Brewer & King 1980, but see Harvey et al. 1999, Harvey 2000). These studies all relate to herbivore consumption rates. Recently, a study on the effect of parasitization of herbivores revealed a clear positive effect of parasitization on plant fitness, i.e. seed production. Arabidopsis thaliana plants on which a single parasitized caterpillar had fed had a similar seed production as uninfested plants whereas plants on which an unparasitized caterpillar had been feeding produced significantly fewer seeds (van Loon et al. 2000). Similar results have been reported for maize plants infested with beet armyworm caterpillars

Inducible indirect defence of plants: from mechanisms to ecological functions

that were unparasitized or parasitized by the parasitoid Cotesia marginiventris (Fritzsche-Hoballah & Turlings 2001). Exploitation of different genotypes in studying cost-benefit analyses To investigate the evolutionary and ecological consequences of plant characteristics such as (components of) induced indirect defence, it is important to compare individuals that differ in specific characteristics. It has been demonstrated that plants of different genotypes differ in the amount and composition of the induced volatile blend (e.g. Dicke et al. 1990a, Loughrin et al. 1995, Gouinguené et al. 2001, Krips et al. 2001) and in the degree of attraction of carnivores (Krips et al. 2001). However, in these studies the exact genotypic differences were unknown and most likely the genotypes differed not only in the characteristics of interest, but in many others as well. Detailed mechanistic knowledge on the induction pathways offers the possibility to compare genotypes that differ in a single or a limited set of known genes. For instance, specific mutants or transgenes can be used in which certain genes are mutated, knocked out or overexpressed. Such a molecular genetic approach has been used in induced direct defence (see e.g. Pieterse & van Loon 1999, Roda & Baldwin 2002 for reviews), but so far it has not been used in induced indirect defence. Several signal transduction pathways that are involved in induction of indirect defence are known, as well as the genes that code for the enzymatic steps involved. In this way the effect of single genes on the expression of the phenotype in terms of induced indirect defence can be studied. We have recently used this approach with Arabidopsis thaliana. Many mutants and transgenes that are altered in signalling pathways are available. By exploiting these tools, we have shown that the shikimic acid and the octadecanoid pathways are both involved in herbivore-induced attraction of the parasitoid Cotesia rubecula to Pieris-infested Arabidopsis plants (van Poecke & Dicke 2002). This approach will enable the investigation of the ecological importance of specific characteristics of induced indirect defence.

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monitor how plants respond to different environmental stresses, both biotic and abiotic stress, and whether and how their responses to different stresses overlap or differ in qualitative or quantitative aspects or in temporal and spatial aspects. Furthermore, it will enable ecologists to design manipulative experiments that can carefully address specific questions related to inducible defences. As a result, the large-scale reductionist investments in the study of mechanistic aspects of plant biology will provide important tools for ecologists to investigate functional aspects of the interactions of plants with their environment. At present these tools are available for a limited number of plant species, but most likely this number will increase rapidly. Ecologists can use these new tools to address questions that could not be answered so easily until now. Some of these questions in the context of inducible defences are: 1. What are the gene-expression changes in response to different biotic and abiotic stresses and how do these affect the plant phenotype and consequently the interactions within a food web context? 2. What is the effect of different combinations of biotic stresses, such as the simultaneous attack of different herbivorous arthropods, or the simultaneous attack of a pathogen and a herbivore? 3. How do different abiotic conditions affect the responses of plants to attackers and – in turn - the response of the carnivore towards the induced plant? 4. How do plants respond to chemical information from neighbouring plants that are attacked by herbivores or pathogens? 5. What is the contribution of certain inducible defence characteristics to plant fitness? As a consequence, incorporating the elucidation of mechanistic aspects of plant-attacker interactions at the cellular and subcellular level will result in significant progress in the field of ecology of inducible defences. Acknowledgements. We thank Monika J. Hilker, Junji Takabayashi and Ted Turlings for insightful and constructive comments on a previous version of the manuscript. JGdB was funded by the Dutch Science Foundation (NWO-ALW) and MD was partiallly funded by the UyttenboogaartEliasen Foundation, Amsterdam.

Conclusion Ecologists have long recognized the importance of understanding mechanisms to further knowledge on the ecology of interactions between organisms. Inducible defences are characterized by large scale changes in gene expression. Knowledge of these changes can be exploited in different ways. It will allow ecologists to

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