Herbivore-induced, indirect plant defences - UPCH

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100G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111that the emitted blends also vary with the herbivore species[149], and even different ontogenetic stages of the sameherbivore [150,151] may influence the headspace composition.However, differences between volatile blends seem tobe largest among different plant species and smallest amongplants of one species infested by different herbivores[141,149].The high variability that characterises the chemicalcomposition of emitted blends raises the question of theecological relevance of these differences and whetherarthropods can discriminate among these complex mixtures.Electroantennogram (EAG) analyses allow individual blendcomponents to be differentiated in order to determine whichcompounds or combination of different compounds can beperceived by an arthropod [152,153]. Further informationon the physiological perception of different plant odours byarthropods have been obtained from in vivo calciumimagingmeasurements that provide additional informationon how the olfactory information is processed in thearthropod brain [154,155]. However, only the additionalinclusion of behavioural assays, in which the arthropods aresimultaneously exposed to two or more odours amongwhich they have to choose, provides information on whetheran odour has an attracting, repelling, or neutral effect on thebehaviour of the focal arthropod.4.2. Specificity and behavioural responses to HIPVsMuch has been learned from such behavioural assays onthe ability of arthropods to discriminate different odourblends. As the production of HIPVs has been originallydescribed in the context of host-location cues for parasiticwasps [5], most researchers have focussed on the role ofplant-derived volatiles in determining the ability of differentparasitoid or carnivore species to detect their herbivoroushosts or preys. Several studies of an increasing number oftritrophic plant–herbivore–carnivore systems have indicatedthat the ability of the carnivores and parasitoids todiscriminate different odour blends depends very much ontheir degree of dietary specialization [156], and on theirlevel of deprivation, as well as on their previous experience[149]. The particular behavioural response – that is whetheran herbivore or carnivore is attracted or repelled, or reactsneutrally to a specific blend of HIPVs – seems to dependstrongly on the level of plant induction [157–159].However, plants do not only interact with otherorganisms above ground. Recently, evidence has shownfor the first time that mechanisms similar to the onesdescribed above- may also work below-ground: Entomopathogenicnematodes (Heterohabditis megidis) are attractedas yet unidentified chemicals that are released from roots ofa coniferous plant (Thuja occidentalis) when weevil larvae(Otiorhynchus sulcatus) attack [160]. Moreover, systemicallyreleased HIPVs have been shown to attract thespecialist parasitoids of root-feeding larvae [161]. Althoughcurrently multitrophic below-ground interactions and thelinks between multitrophic above- and below-groundinteractions are poorly understood, future research willundoubtedly address these questions [162].4.3. Ecological function of HIPVs in natureMost studies regarding HIPV emission have beenconducted under artificial greenhouse or laboratory conditions.Facing the above-mentioned variability, the questionarises whether plants benefit from the emission of HIPVsunder natural growing conditions. To date, few studies existthat show predators are attracted to herbivore-infested plantsunder field conditions [153,163–165]. Moreover, specialistparasitoid wasps were able to distinguish among maize,cotton, and tobacco plants that were infested by theirherbivorous hosts from those which were under non-hostattack [166]. Caterpillars (S. exigua) placed on tomatoplants (L. esculentum var. Ace) that had been grown in anagricultural system and induced previously with exogenouslyapplied JA, suffered from higher parasitism rates byan endoparasitic wasp (Hyposoter exiguae) than controlplants [167]. A further field study of native tobacco (N.attenuata) demonstrated that, indeed, the release of volatilesincreased the predation rates of tobacco hornworm eggs by ageneralist predator (Geocoris pallens) [168]. Recently, Limabean plants grown in their natural environment, followed byrepeated treatments with JA solutions for 5 weeks wereshown to respond with an increased seed set [169]. Sinceboth the emission of HIPV as well as the secretion ofextrafloral nectar had been upregulated by this treatment, itremained unclear which indirect defence was responsible forthe observed beneficial effect. More field trials are clearlynecessary to determine the ecological relevance of individualfactors and to verify results that have been gathered inlaboratory or greenhouse experiments.4.4. Extrafloral nectarIn addition to releasing induced volatiles, some plantspecies have developed other ways to attract predatoryarthropods that will defend them. These include both theprovision of shelter in so-called leaf domatia [170], and theoffer of attractive food sources such as food bodies orextrafloral nectar (EFN). Extrafloral (EF) nectaries arespecialized nectar-secreting organs that may occur onvirtually all vegetative and reproductive plant structures,yet do not involve pollination [171]. They have beendescribed for approximately a thousand plant speciesranging over 93 plant families [172] of flowering plantsand ferns, but they are absent in gymnosperms [171]. EFNsare aqueous solutions that comprise mainly sucrose,glucose, and fructose, but other sugars, amino acids andother organic compounds may be present in some species[173]. The secreted sugars are mainly derived from thephloem [174,175] or synthesised in the region of the nectary[176]. EF nectaries secrete small amounts of nectar
G. Arimura et al. / Biochimica et Biophysica Acta 1734 (2005) 91–111 101throughout the day. The secretion of nectar can followcircadian rhythms [177–180] or be relatively constantthroughout day and night [181,182].The mechanisms of nectar secretion are poorly understood:Some researchers have described secretion as apassive process, whereas others discuss it as an eliminationof surplus sugars [173]. However, there is evidence thatnectar secretion is an active secretory process: It requires theexpenditure of metabolic energy [183], and EF nectariesstrongly resemble secretory cells which contain largenumbers of mitochondria and show dense protoplasts andlarge nuclei [173]. Furthermore, the secretion of EFN can beinduced by JA treatment. Originally discovered in Macarangatanarius [184], nectar secretion is suggested to beinducible by leaf damage. This seems to be a widespreadphenomenon [169,185–188], which may be linked to thesame or similar signalling pathways as those discussed forthe induction of volatile biosynthesis. Inhibitors thatsuppress the release of linolenic acid or interfere with theproduction of linolenic acid hydroperoxides completelysuppress the damage-induced flow of EFN and, hence,clearly demonstrate the involvement of oxylipin-basedsignalling in EFN-induction. Interestingly, also the attackof a below-ground herbivore (Agriotes lineatus) on cottonplants (Gossypium herbaceum) induced above-groundproduction of EFN [185]. InVicia faba, even the numberof EF nectaries increased following leaf damage [189].Generally, the secretion of EFN is believed to function asan indirect anti-herbivore defence by attracting and henceincreasing the presence of putative plant defenders onnectar-secreting plant parts. Most studies focussed on theprotective effect of ants on entire plants or individual plantparts, demonstrating a beneficial function of these insects[172,173]. However, contradictory observations thatdetected no measurable preventive effect of EFN-attractedants also exist [190–194]. In these cases, the lack ofprotection could be explained by, for example, (1) differencesin the aggressiveness of the attracted ant species[194–196], (2) differences in foraging behaviour of antspecies from different habitats [197,198], and (3) a varyingsusceptibility of the herbivores to ant predation [199,200].Besides ants, the EF nectaries attract a diverse spectrum ofother arthropods including Araneae, Diptera, Coleopteraand Hymenoptera (see [172] for review). Due to theirpredatory or parasitoid ways of life, many of these non-ants,such as ichneumonid, braconid and chalcidoid wasps [201–203], jumping spiders (Salticidae) [204], phytoseiid mites[205] or tachinid flies [206], can as well reduce the numberof herbivores. Both ants and wasps exerted beneficial effectson the EF nectary-bearing plant Turnera ulmifolia whenselectively excluded, yet no additive increase was observedwhen both insect groups had access [207].The emission of floral odours by plants is very importantfor attracting pollinators to their floral nectars. Some ofthese floral nectars also scent by themselves [208], whereasnothing is known about the headspace of EFNs. Beyondthese odours, which communicate the location, abundance,and quality of these nectars to higher trophic levels, othermechanisms may help to guide EFN-feeding arthropods toremote nectar sources. First, some EF nectaries are colouredproviding visual cues for foraging arthropods [172]. Additionally,increased amounts of both HIPVs and EFN(Table 1) would allow foraging arthropods to use theemitted volatile organic compounds as a cue to detect nectarsources from longer distances. Future research should try todisentangle and quantify the costs and benefits of one ofthese indirect defences for a plant and figure out to whatextent each of them contributes to plant defence in nature.4.5. Evolution of HIPVs and EFNThe evolutionary origin of HIPV emission and EFNsecretion remains unknown. As described above, C 6 -volatiles or terpenoids may repel herbivores [123,209], betoxic for phytophages [210,211], or act anti-microbially[212]. HIPVs are therefore discussed as having originallyTable 1Compilation of species that are known to both emit HIPVs and feature extrafloral nectariesFamily Species Nectar inducible HIPVs inducible ReferencesEuphorbiaceae Manihot esculenta n.i. n.i. + H 1 [269,270]Leguminosae Phaseolus lunatus + JA + JA [169]Vicia faba n.i. n.i. + H 2 [271,272]Vignia unguiculata n.i. n.i. + H 3 [273,274]Malvaceae Gossypium herbaceum + M, H 4, 5 + H 5, 6 [185,186,275]Gossypium hirsutum n.i. n.i. + H 6, 7, 8 [202,276–278]Rosaceae Prunus serotina n.i. n.i. + H 9 [256,279]Salicaceae Populus deltoides n.i. n.i. + H 10 [91,280]Populus trichocarpa n.i. n.i. + H 10 [91,281]Solanaceae Solanum nigrum n.i. n.i. + H 11, 12 [282,283]Additional information on the inducibility of the respective trait is presented (for abbreviations see below).H 1, spider mite (Mononychellus tanajoa Bondar); H 2, pentatomid bug (Nezara viridula Linnaeus); H 3, spider mite (Tetranychus urticae Koch); H 4,Mediterranean brocade (Spodoptera littoralis Boisduval); H 5, wireworms (Agriotes lineatus Linnaeus); H 6, beet armyworm (Spodoptera exigua Hqbner); H7, tobacco budworm (Heliothis virescens Fabricius); H 8, corn earworm (Helicoverpa zea Boddie); H 9, forest cockchafe (Melolontha hippocastani Fabricius);H 10, forest tent caterpillar (Malacosoma disstria Hqbner); H 11, Colorado potato beetle (Leptinotarsa decemlineata Say); H 12, death’s head hawkmoth(Acherontia atropos Linnaeus); JA, jasmonic acid; M, mechanical damage; n.i., not investigated.
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