Emission Of Herbivore-induced Volatiles Research Articles

Cowpea volatiles induced by beet armyworm or fall armyworm differentially prime maize plants

Exposure to herbivore-induced plant volatiles (HIPVs) is known to enhance the defense responses in plants. This so-called priming effect has only been marginally studied in intercropping systems. We tested whether HIPVs from cowpea, which often serves as an intercrop alongside maize, can prime herbivore-induced volatile emissions in maize. Conventional volatile collection assays and real-time mass spectrometry revealed that maize plants that were exposed to HIPVs from cowpea infested with Spodoptera exigua caterpillars emitted more than control plants when they themselves were subsequently damaged by the same pest. The enhanced emission was only evident on the first day after infestation. Maize plants that were exposed to HIPVs from cowpea infested by S. frugiperda larvae showed no priming effect and released considerably less upon S. frugiperda infestation than upon S. exigua infestation. The latter may be explained by the fact that S. frugiperda is particularly well adapted to feed on maize and is known to suppress maize HIPV emissions. Our results imply that HIPVs from cowpea, depending on the inducing insect herbivore, may strongly prime maize plants. This deserves further investigation, also in other intercropping systems, as it can have important consequences for tritrophic interactions and crop protection.

Better Together: Volatile-Mediated Intraguild Effects on the Preference of Tuta absoluta and Trialeurodes vaporariorum for Tomato Plants.

Plant-herbivore interactions have been extensively studied in tomato plants and their most common pests. Tomato plant chemical defenses, both constitutive and inducible, play a role in mediating these interactions. Damaged tomato plants alter their volatile profiles, affecting herbivore preferences between undamaged and damaged plants. However, previous studies on tomato volatiles and herbivore preferences have yielded conflicting results, both in the volatile chemistry itself as well as in the attraction/repellent herbivore response. This study revisits the volatile-mediated interactions between tomato plants and two of their main herbivores: the leafminer Tuta absoluta and the whitefly Trialeurodes vaporariorum. Tomato plant volatiles were analyzed before and after damage by each of these herbivores, and the preference for oviposition (T. absoluta) and settling (T. vaporariorum) on undamaged and damaged plants was assessed both after conspecific and heterospecific damage. We found that both insects consistently preferred damaged plants over undamaged plants. The emission of herbivore-induced plant volatiles (HIPVs) increased after T. absoluta damage but decreased after T. vaporariorum damage. While some of our findings are in line with previous reports, T. absoluta preferred to oviposit on plants damaged by conspecifics, which differs from earlier studies. A comparison of HIPVs emitted after damage by T. absoluta and T. vaporariorum revealed differences in up- or down-regulation, as well as significant variations in specific compounds (12 for T. absoluta and 26 for T. vaporariorum damaged-plants). Only two compounds, β-caryophyllene and tetradecane, significantly varied because of damage by either herbivore, in line with the overall variation of the HIPV blend. Differences in HIPVs and herbivore preferences may be attributed to the distinct feeding habits of both herbivores, which activate different defensive pathways in plants. The plant's challenge in simultaneously activating both defensive pathways may explain the preference for heterospecific damaged plants found in this study, which are also in line with our own observations in greenhouses.

Effects of far-red light on the behaviour and reproduction of the zoophytophagous predator Macrolophus pygmaeus and its interaction with a whitefly herbivore.

Plants can detect neighbouring plants through a reduction in the ratio between red and far-red light (R:FR). This provides a signal of plant-plant competition and induces rapid plant growth while inhibiting defence against biotic stress, two interlinked responses designated as the shade avoidance syndrome (SAS). Consequently, the SAS can influence plant-herbivore interactions that could cascade to higher trophic levels. However, little is known about how the expression of the SAS can influence tritrophic interactions. We investigated whether changes in R:FR affect the emission of herbivore-induced plant volatiles (HIPVs), and whether these changes influence the attraction of the zoophytophagous predator Macrolophus pygmaeus. We also studied how the expression of the SAS and subsequent inhibition of plant defences affects the reproduction of M. pygmaeus in both the presence and absence of the greenhouse whitefly (WF) (Trialeurodes vaporariorum) as arthropod prey. The results show that changes in R:FR have little effect on HIPV emissions and predator attraction. However, a reduction in R:FR leads to increased reproduction of both the predator and the WFs. We discuss that shade avoidance responses can increase the population development of M. pygmaeus through a combination of reduced plant defences and increased herbivore densities.

Drought impairs herbivore-induced volatile terpene emissions by ponderosa pine but not through constraints on newly assimilated carbon.

Volatile terpenes serve multiple biological roles including tree resistance against herbivores. The increased frequency and severity of drought stress observed in forests across the globe may hinder trees from producing defense-related volatiles in response to biotic stress. To assess how drought-induced physiological stress alters volatile emissions alone and in combination with a biotic challenge, we monitored pre-dawn water potential, gas-exchange, needle terpene concentrations and terpene volatile emissions of ponderosa pine (Pinus ponderosa) saplings during three periods of drought and in response to simulated herbivory via methyl jasmonate application. Although 3-, 6- and 7-week drought treatments reduced net photosynthetic rates by 20, 89 and 105%, respectively, the magnitude of volatile fluxes remained generally resistant to drought. Herbivore-induced emissions, however, exhibited threshold-like behavior; saplings were unable to induce emissions above constitutive levels when pre-dawn water potentials were below the approximate zero-assimilation point. By comparing compositional shifts in emissions to needle terpene concentrations, we found evidence that drought effects on constitutive and herbivore-induced volatile flux and composition are primarily via constraints on the de novo fraction, suggesting that reduced photosynthesis during drought limits the carbon substrate available for de novo volatile synthesis. However, results from a subsequent 13CO2 pulse-chase labeling experiment then confirmed that both constitutive (<3% labeled) and herbivore-induced (<8% labeled) de novo emissions from ponderosa pine are synthesized predominantly from older carbon sources with little contribution from new photosynthates. Taken together, we provide evidence that in ponderosa pine, drought does not constrain herbivore-induced de novo emissions through substrate limitation via reduced photosynthesis, but rather through more sophisticated molecular and/or biophysical mechanisms that manifest as saplings reach the zero-assimilation point. These results highlight the importance of considering drought severity when assessing impacts on the herbivore-induced response and suggest that drought-altered volatile metabolism constrains induced emissions once a physiological threshold is surpassed.

Martin McAinsh.

Martin McAinsh.

Exposure of Helicoverpa armigera Larvae to Plant Volatile Organic Compounds Induces Cytochrome P450 Monooxygenases and Enhances Larval Tolerance to the Insecticide Methomyl.

Simple SummaryUpon insect herbivory plants release herbivore-induced plant volatiles (HIPVs) to elicit either direct antiherbivore defenses by intoxicating the herbivore or indirect defenses by attracting natural enemies. Insect herbivores use sophisticated detoxification systems, including cytochrome P450 monooxygenases (P450s), to cope with plant defensive chemicals and insecticides. Many behaviors of insects are manipulated to a large extent by olfaction. However, few studies concern the role of olfaction in insect adaptation to xenobiotics. In this study we show that olfactory exposure of Helicoverpa armigera, a devastating pest of many important crop plants that has developed high levels of resistance to various insecticides, to four plant volatile compounds limonene, nerolidol, 2-heptanone and cis-3-hexenyl acetate dramatically increases larval tolerance to carbamate insecticide methomyl. Inhibition of P450s by piperonyl butoxide (PBO), a well-known P450 inhibitor, compromises the effects of volatile exposure. Exposure to the four volatiles upregulates multiple detoxification systems, including cytochrome P450s. Our findings indicate that induction of insecticide-detoxifying P450s by plant volatiles prior to actually inflicting plant damage may confer insect larvae more time to pre-activate insect detoxification systems prior to the ingestion or contact of insecticides, leading to increased larval tolerance to insecticides.Plants release an array of volatile chemicals into the air to communicate with other organisms in the environment. Insect attack triggers emission of herbivore-induced plant volatiles (HIPVs). How insect herbivores use these odors to plan their detoxification systems is vital for insect adaptation to environmental xenobiotics. Here we show that the larvae of Helicoverpa armigera (Hübner), a broadly polyphagous lepidopteran herbivore, have the capacity to use plant volatiles as cues to upregulate multiple detoxification systems, including cytochrome P450 monooxygenases (P450s), for detoxification of insecticides. Olfactory exposure of the fifth instars to two terpene volatiles limonene and nerolidol, and two green-leaf volatiles 2-heptanone and cis-3-hexenyl acetate significantly reduced larval susceptibility to the insecticide methomyl. However, larval pretreatment with piperonyl butoxide (PBO), a known P450 inhibitor, neutralized the effects of volatile exposure. Furthermore, larval exposure to the four plant volatiles enhanced activities of P450 enzymes in midguts and fatbodies, and upregulated expression of CYP6B2, CYP6B6 and CYP6B7, P450s involved in detoxification of the insecticide. Larval exposure to 2-heptanone and limonene volatiles also enhanced activities of glutathione-s-transferase and carboxylesterase. Our findings suggest that olfactory exposure to HIPVs enhances larval insecticide tolerance via induction of detoxification P450s.

The Effects of Ozone on Herbivore-Induced Volatile Emissions of Cultivated and Wild Brassica Rapa

Since preindustrial times, concentrations of tropospheric ozone, a phytotoxic pollutant, have risen in the Northern Hemisphere. Selective breeding has intentionally modified crop plant traits to improve yield but may have altered plant defenses against abiotic and biotic stresses. This study aims to determine if cultivated and wild plants respond differently to herbivory under elevated ozone. We studied the volatile emissions of four cultivated Brassica rapa ssp. oleifera varieties and one wild population after exposure to ozone or Plutella xylostella larval feeding either individually or together. Ozone modulated the volatiles emitted in response to herbivory by all plant varieties to different extents. We did not observe a clear difference in the effects of ozone on wild and cultivated plants, but cultivated plants had higher volatile emission rates in response to herbivory and ozone had either no effect or increased the herbivore-induced response. Larvae tended to feed more on elevated ozone-treated plants; however, we could not link the increase of feeding to the change in volatile emissions. Our study complements recent studies reporting that selective breeding might not have weakened chemical defenses to biotic and abiotic stresses of cultivated plants.

Herbivore-induced volatile emissions are altered by soil legacy effects in cereal cropping systems

Aims (main purpose and research question)Soil properties, including microbial composition and nutrient availability, can influence the emissions of plant volatile organic compounds (VOCs) that serve as host-location cues for insect pests and their natural enemies. Agricultural practices have profound effects on soil properties, but how these influence crop VOCs remains largely unknown. The aim of this study was to investigate the effect of agricultural practices on constitutive and herbivore-induced VOC emissions by a major staple crop through soil legacy effects.MethodsIn a full factorial experiment, we measured VOC emissions by wheat (Triticum aestivum) grown in soil inoculum from wheat-fallow or wheat-cover crop rotations that was subjected to feeding by larval Cephus cinctus.Results (main findings)Under herbivory, plants grown in cover crop inoculum emitted greater total VOCs, including higher concentrations of 2-pentadecanone, an insect repellent, and nonanal, a compound important in the recruitment of natural enemies. Plants grown in fallow inoculum showed no differences in emissions whether under herbivory or not. Soil inoculum did not influence VOC emissions of plants in the absence of larval feeding.ConclusionsThese results suggest that agricultural practices influence crop VOC emissions through soil legacy effects. Additionally, crops grown in wheat-fallow rotations may be less successful recruiting natural enemies of pests through herbivore-induced VOC signaling.AbbreviationsVolatile organic compounds (VOCs); herbivore-induced plant volatiles (HIPV); green leaf volatiles (GLVs); northern Great Plains (NGP); wheat stem sawfly (WSS); gas chromatography-mass spectrometry (GC-MS); non-metric multidimensional scaling (NMDS); generalized linear mixed-effects model (GLMM).

Does ozone exposure affect herbivore-induced plant volatile emissions differently in wild and cultivated plants?

Concentrations of tropospheric ozone have more than doubled in the Northern Hemisphere since pre-industrial times. Plant responses to single abiotic or biotic stresses, such as ozone exposure and herbivore-feeding, have received substantial attention, especially for cultivated plants. Modern cultivated plants have been subjected to selective breeding that has altered plant chemical defences. To understand how ozone might affect plant responses to herbivore-feeding in wild and cultivated plants, we studied the volatile emissions of brassicaceous plants after exposure to ambient (~ 15 ppb) or elevated ozone (80 ppb), with and without Plutella xylostella larvae-feeding. Results indicated that most of the wild and cultivated plants increased volatile emissions in response to herbivore-feeding. Ozone alone had a weaker and less consistent effect on volatile emissions, but appeared to have a greater effect on wild plants than cultivated plants. This study highlights that closely related species of the Brassicaceae have variable responses to ozone and herbivore-feeding stresses and indicates that the effect of ozone may be stronger in wild than cultivated plants. Further studies should investigate the mechanisms by which elevated ozone modulates plant volatile emissions in conjunction with biotic stressors.

Does corn phenological stage alter the attractiveness of herbivore-induced plant volatiles to the predatory lacewing Chrysoperla externa (Hagen, 1861)?

Plant chemical defenses can affect herbivores directly or indirectly through the emission of herbivore-induced plant volatiles (HIPVs) that recruit natural enemies. Corn seedlings have high concentrations of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) that deter aphids, but as concentration decreases over the course of plant phenology, plants become less resistant. We investigated whether corn phenological stage influences the attractiveness of Rhopalosiphum maidis (Fitch, 1856) - infested corn seedling volatiles to the predatory lacewing Chrysoperla externa (Hagen, 1861). In olfactometer, lacewings preferentially oriented to volatiles from aphid-infested over those by uninfested corn seedlings at V6 or V7 stages, but did not discriminate between volatiles from uninfested and aphid-infested V5-stage seedlings. Greater numbers of aphids died in V5 corn seedlings relative to those in V6 and V7 seedlings. Our results indicate that the lack of discrimination of the predatory lacewing to HIPVs emitted by V5 corn seedlings is due to insufficient induction given that they were more resistant to R. maidis.

Mycorrhizae Alter Constitutive and Herbivore-Induced Volatile Emissions by Milkweeds.

Plants use volatile organic compounds (VOCs) to cue natural enemies to their herbivore prey on plants. Simultaneously, herbivores utilize volatile cues to identify appropriate hosts. Despite extensive efforts to understand sources of variation in plant communication by VOCs, we lack an understanding of how ubiquitous belowground mutualists, such as arbuscular mycorrhizal fungi (AMF), influence plant VOC emissions. In a full factorial experiment, we subjected plants of two milkweed (Asclepias) species under three levels of AMF availability to damage by aphids (Aphis nerii). We then measured plant headspace volatiles and chemical defenses (cardenolides) and compared these to VOCs emitted and cardenolides produced by plants without herbivores. We found that AMF have plant species-specific effects on constitutive and aphid-induced VOC emissions. High AMF availability increased emissions of total VOCs, two green leaf volatiles (3-hexenyl acetate and hexyl acetate), and methyl salicylate in A. curassavica, but did not affect emissions in A. incarnata. In contrast, aphids consistently increased emissions of 6-methyl-5-hepten-2-one and benzeneacetaldehyde in both species, independent of AMF availability. Both high AMF availability and aphids alone suppressed emissions of individual terpenes. However, aphid damage on plants under high AMF availability increased, or did not affect, emissions of those terpenes. Lastly, aphid feeding suppressed cardenolide concentrations only in A. curassavica, and AMF did not affect cardenolides in either plant species. Our findings suggest that by altering milkweed VOC profiles, AMF may affect both herbivore performance and natural enemy attraction.

Herbivore-induced volatile emission from old-growth black poplar trees under field conditions

Herbivory is well known to trigger increased emission of volatile organic compounds (VOCs) from plants, but we know little about the responses of mature trees. We measured the volatiles emitted by leaves of old-growth black poplar (Populus nigra) trees after experimental damage by gypsy moth (Lymantria dispar) caterpillars in a floodplain forest, and studied the effect of herbivory on the transcript abundance of two genes involved in the biosynthesis of VOCs, and the accumulation of defence phytohormones. Herbivory significantly increased volatile emission from the experimentally damaged foliage, but not from adjacent undamaged leaves in the damaged branches (i.e., no systemic response). Methylbutyraldoximes, 4,8-dimethyl-1,3,7-nonatriene (DMNT), (Z)-3-hexenol and (E)-β-ocimene, amongst other compounds, were found to be important in distinguishing the blend of herbivore-damaged vs. undamaged leaves. Herbivory also increased expression of PnTPS3 (described here for the first time) and PnCYP79D6-v4 genes at the damaged sites, these genes encode for an (E)-β-ocimene synthase and a P450 enzyme involved in aldoxime formation, respectively, demonstrating de novo biosynthesis of the volatiles produced. Herbivore-damaged leaves had significantly higher levels of jasmonic acid and its conjugate (−)-jasmonic acid-isoleucine. This study shows that mature trees in the field have a robust response to herbivory, producing induced volatiles at the damaged sites even after previous natural herbivory and under changing environmental conditions, however, further studies are needed to establish whether the observed absence of systemic responses is typical of mature poplar trees or if specific conditions are required for their induction.

Phloem-feeding herbivory on flowering melon plants enhances attraction of parasitoids by shifting floral to defensive volatiles

Emission of herbivore-induced plant volatiles (HIPVs) can differ according to the type of herbivory and the plant development stage, ultimately affecting recruitment of the natural enemy. Little is known about plant defenses induced at the flowering stage by phloem-feeding insects. We investigated the olfactory preference of Encarsia desantisi parasitoids and the chemical profile of flowering melon plants induced or not by the phloem-feeding of Bemisia tabaci whiteflies. In addition, we tested whether the parasitoids were attracted to synthetic defensive HIPVs, which mimicked whitefly-infested flowering melons. The parasitoids recognized volatiles from undamaged melons but preferred the scent of host-infested melons in olfactometry assays. Amounts of most individual volatiles did not differ between plant treatments; however, only whitefly-induced melons released methyl salicylate and tetradecane, compounds known to attract parasitoids. Interestingly, grouping volatiles by chemical classes revealed that whitefly-infested melon released larger amounts of monoterpenes and smaller amounts of benzenoids than undamaged melons, which might underlying the parasitoid attraction and indicate a possible trade-off between defensive and reproductive defenses at the melon flowering stage. Additionally, E. desantisi preferred the mix of synthetic and defensive HIPVs over hexane (control), opening a new avenue for further investigations in using olfactory lures for B. tabaci biological control. This study is the first report of induced defenses in melon plants and their mediation in a tritrophic interaction, as well as the first record of E. desantisi behavioral preference for HIPVs.

The Active Jasmonate JA-Ile Regulates a Specific Subset of Plant Jasmonate-Mediated Resistance to Herbivores in Nature.

The jasmonate hormones are essential regulators of plant defense against herbivores and include several dozen derivatives of the oxylipin jasmonic acid (JA). Among these, the conjugate jasmonoyl isoleucine (JA-Ile) has been shown to interact directly with the jasmonate co-receptor complex to regulate responses to jasmonate signaling. However, functional studies indicate that some aspects of jasmonate-mediated defense are not regulated by JA-Ile. Thus, it is not clear whether JA-Ile is best characterized as the master jasmonate regulator of defense, or if it regulates more specific aspects. We investigated possible functions of JA-Ile in anti-herbivore resistance of the wild tobacco Nicotiana attenuata, a model system for plant-herbivore interactions. We first analyzed the soluble and volatile secondary metabolomes of irJAR4xirJAR6, asLOX3, and WT plants, as well as an RNAi line targeting the jasmonate co-receptor CORONATINE INSENSITIVE 1 (irCOI1), following a standardized herbivory treatment. irJAR4xirJAR6 were the most similar to WT plants, having a ca. 60% overlap in differentially regulated metabolites with either asLOX3 or irCOI1. In contrast, while at least 25 volatiles differed between irCOI1 or asLOX3 and WT plants, there were few or no differences in herbivore-induced volatile emission between irJAR4xirJAR6 and WT plants, in glasshouse- or field-collected samples. We then measured the susceptibility of jasmonate-deficient vs. JA-Ile-deficient plants in nature, in comparison to wild-type (WT) controls, and found that JA-Ile-deficient plants (irJAR4xirJAR6) are much better defended even than a mildly jasmonate-deficient line (asLOX3). The differences among lines could be attributed to differences in damage from specific herbivores, which appeared to prefer either one or the other jasmonate-deficient phenotype. We further investigated the elicitation of one herbivore-induced volatile known to be jasmonate-regulated and to mediate resistance to herbivores: (E)-α-bergamotene. We found that JA was a more potent elicitor of (E)-α-bergamotene emission than was JA-Ile, and when treated with JA, irJAR4xirJAR6 plants emitted 20- to 40-fold as much (E)-α-bergamotene than WT. We conclude that JA-Ile regulates specific aspects of herbivore resistance in N. attenuata. This specificity may allow plants flexibility in their responses to herbivores and in managing trade-offs between resistance, vs. growth and reproduction, over the course of ontogeny.

Elevated carbon dioxide reduces emission of herbivore-induced volatiles in Zea mays.

Terpene volatiles produced by sweet corn (Zea mays) upon infestation with pests such as beet armyworm (Spodoptera exigua) function as part of an indirect defence mechanism by attracting parasitoid wasps; yet little is known about the impact of climate change on this form of plant defence. To investigate how a central component of climate change affects indirect defence, we measured herbivore-induced volatile emissions in plants grown under elevated carbon dioxide (CO2 ). We found that S.exigua infested or elicitor-treated Z.mays grown at elevated CO2 had decreased emission of its major sesquiterpene, (E)-β-caryophyllene and two homoterpenes, (3E)-4,8-dimethyl-1,3,7-nonatriene and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene. In contrast, inside the leaves, elicitor-induced (E)-β-caryophyllene hyper-accumulated at elevated CO2 , while levels of homoterpenes were unaffected. Furthermore, gene expression analysis revealed that the induction of terpene synthase genes following treatment was lower in plants grown at elevated CO2 . Our data indicate that elevated CO2 leads both to a repression of volatile synthesis at the transcriptional level and to limitation of volatile release through effects of CO2 on stomatal conductance. These findings suggest that elevated CO2 may alter the ability of Z.mays to utilize volatile terpenes to mediate indirect defenses.

Leaf rust infection reduces herbivore-induced volatile emission in black poplar and attracts a generalist herbivore.

Plants release complex volatile blends after separate attack by herbivores and pathogens, which play many roles in interactions with other organisms. Large perennials are often attacked by multiple enemies, but the effect of combined attacks on volatile emission is rarely studied, particularly in trees. We infested Populus nigra trees with a pathogen, the rust fungus Melampsora larici-populina, and Lymantria dispar caterpillars alone and in combination. We investigated poplar volatile emission and its regulation, as well as the behavior of the caterpillars towards volatiles from rust-infected and uninfected trees. Both the rust fungus and the caterpillars alone induced volatile emission from poplar trees. However, the herbivore-induced volatile emission was significantly reduced when trees were under combined attack by the herbivore and the fungus. Herbivory induced terpene synthase transcripts as well as jasmonate concentrations, but these increases were suppressed when the tree was additionally infected with rust. Caterpillars preferred volatiles from rust-infected over uninfected trees. Our results suggest a defense hormone crosstalk upon combined herbivore-pathogen attack in poplar trees which results in lowered emission of herbivore-induced volatiles. This influences the preference of herbivores, and might have other far-reaching consequences for the insect and pathogen communities in natural poplar forests.

Defense priming by non-jasmonate producing fatty acids in maize (Zea mays)

ABSTRACTPreviously, we described a priming effect of α-linolenic acid (LnA) on anti-herbivore defense response in maize seedlings.1 We showed that exogenous application of LnA stimulated higher jasmonic acid (JA) accumulation and herbivore-induced plant volatile (HIPV) emission after treatment with insect elicitor (IE). To further investigate the specificity of LnA's priming effect, we incubated maize seedlings in palmitoleic acid (PeicA), γ-linolenic acid (γ LnA) and stearic acid (StA) solutions, and analyzed HIPV emission in response to IE. Seedlings incubated in PeicA and γ LnA had 3 and 1.8 times higher HIPV release when compared to controls. In contrast, treatment with StA did not up-regulate HIPV release. We propose that the elevated level and/or the presence of unsaturated fatty acids sensitize the defense signaling system, which in turn augments the defense response of maize when under insect herbivore attack.

An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants.

Attack of plants by herbivorous arthropods may result in considerable changes to the plant’s chemical phenotype with respect to emission of herbivore-induced plant volatiles (HIPVs). These HIPVs have been shown to act as repellents to the attacking insects as well as attractants for the insects antagonistic to these herbivores. Plants can also respond to HIPV signals from other plants that warn them of impending attack. Recent investigations have shown that certain maize varieties are able to emit volatiles following stemborer egg deposition. These volatiles attract the herbivore’s parasitoids and directly deter further oviposition. However, it was not known whether these oviposition-induced maize (Zea mays, L.) volatiles can mediate chemical phenotypic changes in neighbouring unattacked maize plants. Therefore, this study sought to investigate the effect of oviposition-induced maize volatiles on intact neighbouring maize plants in ‘Nyamula’, a landrace known to respond to oviposition, and a standard commercial hybrid, HB515, that did not. Headspace volatile samples were collected from maize plants exposed to Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) egg deposition and unoviposited neighbouring plants as well as from control plants kept away from the volatile emitting ones. Behavioural bioassays were carried out in a four-arm olfactometer using egg (Trichogramma bournieri Pintureau & Babault (Hymenoptera: Trichogrammatidae)) and larval (Cotesia sesamiae Cameron (Hymenoptera: Braconidae)) parasitoids. Coupled Gas Chromatography-Mass Spectrometry (GC-MS) was used for volatile analysis. For the ‘Nyamula’ landrace, GC-MS analysis revealed HIPV production not only in the oviposited plants but also in neighbouring plants not exposed to insect eggs. Higher amounts of EAG-active biogenic volatiles such as (E)-4,8-dimethyl-1,3,7-nonatriene were emitted from these plants compared to control plants. Subsequent behavioural assays with female T. bournieri and C. sesamiae parasitic wasps indicated that these parasitoids preferred volatiles from oviposited and neighbouring landrace plants compared to those from the control plants. This effect was absent in the standard commercial hybrid we tested. There was no HIPV induction and no difference in parasitoid attraction in neighbouring and control hybrid maize plants. These results show plant-plant signalling: ‘Nyamula’ maize plants emitting oviposition-induced volatiles attractive to the herbivore’s natural enemies can induce this indirect defence trait in conspecific neighbouring undamaged maize plants. Maize plants growing in a field may thus benefit from this indirect defence through airborne signalling which may enhance the fitness of the volatile-emitting plant by increasing predation pressure on herbivores.

Elevated Ozone Modulates Herbivore-Induced Volatile Emissions of Brassica nigra and Alters a Tritrophic Interaction.

Plants damaged by herbivores emit volatile organic compounds (VOCs) that are used by parasitoids for host location. In nature, however, plants are exposed to multiple abiotic and biotic stresses of varying intensities, which may affect tritrophic interactions. Here, we studied the effects of ozone exposure and feeding by Pieris brassicae larvae on the VOCs emitted by Brassica nigra and the effects on oriented flight of the parasitoid Cotesia glomerata. We also investigated the oriented flight of C. glomerata in a wind-tunnel with elevated ozone levels. Herbivore-feeding induced the emission of several VOCs, while ozone alone had no significant effect. However, exposure to 120ppb ozone, followed by 24hr of herbivore-feeding, induced higher emissions of all VOCs as compared to herbivore-feeding alone. In accordance, herbivore-damaged plants elicited more oriented flights than undamaged plants, whereas plants exposed to 120ppb ozone and 24hr of herbivore-feeding elicited more oriented flights than plants subjected to herbivore-feeding alone. Ozone enrichment of the wind-tunnel air appeared to negatively affect orientation of parasitoids at 70ppb, but not at 120ppb. These results suggest that the combination of ozone and P. brassicae-feeding modulates VOC emissions, which significantly influence foraging efficiency of C. glomerata.

Optimizing Crops for Biocontrol of Pests and Disease.

Volatile compounds and extrafloral nectar are common defenses of wild plants; however, in crops they bear an as-yet underused potential for biological control of pests and diseases. Odor emission and nectar secretion are multigene traits in wild plants, and thus form difficult targets for breeding. Furthermore, domestication has changed the capacity of crops to express these traits. We propose that breeding crops for an enhanced capacity for tritrophic interactions and volatile-mediated direct resistance to herbivores and pathogens can contribute to environmentally-friendly and sustainable agriculture. Natural plant volatiles with antifungal or repellent properties can serve as direct resistance agents. In addition, volatiles mediating tritrophic interactions can be combined with nectar-based food rewards for carnivores to boost indirect plant defense.