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Turlings, Ted

Nom
Turlings, Ted
Affiliation principale
Fonction
Professeur.e ordinaire
Email
ted.turlings@unine.ch
Identifiants
https://libra.unine.ch/handle/123456789/330
_
0000-0002-8315-785X

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  • Publication
    Accès libre
    Tritrophic interactions on cultivated maize and its wild ancestor "teosinte"
    (2014)
    De Lange, Elvira Simone
    ;
    Turlings, Ted 
    Modern maize plants (Zea mays ssp. mays, Poaceae) are characterized by large cobs that contain juicy grains, although they have not always had these characteristics. Approximately 9000 years ago, maize was domesticated from teosinte (Z. mays ssp. parviglumis), its closest wild ancestor, which produces much less and much smaller seeds. Teosinte still grows in the wild in Mexico, while maize is produced all over the world. Continuous selection for improved yield and quality has had a cost for the plant in terms of the loss or alteration of other potentially useful traits, such as resistance to pathogens and herbivorous insects. This thesis focuses on the resistance of maize and teosinte against insect pests, in particular with respect to the emission of herbivore-induced volatiles. This feature is considered an indirect defense trait, as the volatiles can betray the presence of prey or hosts to predators and parasitoids, natural enemies of herbivorous insects. Among these natural enemies are parasitoid wasps, of which females have an ovipositor with which they can lay single or multiple eggs in individual hosts. When the wasp larvae develop inside the host they will eventually kill it, potentially benefitting the plant.
    At first, we assessed in nature which insects occur on teosinte. Fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), is reported as an important maize pest in the Americas and is frequently attacked by many species of parasitoids. However, little is known about the presence of this herbivore and its associated parasitoids on teosinte.
    In a laboratory setting, we then assessed whether maize and teosinte emit a similar blend of volatiles when induced by lepidopteran herbivores. We also evaluated the attractiveness of the odor blends to females of two species of parasitoid wasps. Although the odor blends appeared similar upon gas chromatography analysis, the foraging parasitoids responded differentially to them. We obtained similar results when testing real plants and extracts of collected odors, indicating that these extracts can be used to identify the key compounds that are responsible for parasitoid attraction.
    There is surprisingly little field evidence for fitness benefits for plants due to the action of natural enemies. This is still an important point in the discussion on the possible indirect defense role of inducible plant volatiles, especially in the case of parasitoids that, unlike predators, do not directly kill their hosts. Therefore, we evaluated how parasitoid wasps can affect plant performance in a semi-natural setting in Mexico. The presence of parasitoid wasps in field tents containing teosinte plants and fall armyworm significantly reduced herbivore damage, which, for the smallest plants, resulted in a reduction in plant mortality. These findings support the notion that plants may benefit from the presence of parasitoids and may help to resolve the current debate on the defensive function of herbivore-induced volatiles.
    To further explore the importance of volatiles for the attraction of parasitoids under field conditions, we studied maize lox10 mutants, impaired in the biosynthesis of green leaf volatiles (GLVs). These volatiles, responsible for the smell of cut grass, are commonly emitted by plants when wounded or attacked by herbivores. Previously, laboratory studies have shown that GLVs can be used as foraging cues by predators and parasitoids. However, our results imply that GLVs are not of key importance for parasitoid attraction in the field.
    Collectively, these studies provide novel insights into the importance of herbivore-induced volatiles for the attraction of parasitoid wasps, and their indirect importance for plant growth and survival. We identified differences between maize and its wild ancestor, teosinte, with respect to the attraction of parasitoids that could possibly be exploited for ecologically sound methods to better protect maize against insect pests.
  • Publication
    Accès libre
    Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields
    (2012)
    von Mérey, Georg
    ;
    Veyrat, Nathalie 
    ;
    de Lange, Elvira S.
    ;
    Degen, Thomas 
    ;
    Mahuku, George
    ;
    Lopez Valdez, Raymundo
    ;
    Turlings, Ted 
    ;
    D’Alessandro, Marco
    Synthetic elicitors can be used to induce resistance in plants against pathogens and arthropod herbivores. Such compounds may also change the emission of herbivore-induced plant volatiles, which serve as important cues for parasitic wasps to locate their hosts. Therefore, the use of elicitors in the field may affect biological control of insect pests. To test this, we treated maize seedlings growing in a subtropical field in Mexico with methyl jasmonate (MeJA), an elicitor of defense responses against many insects, and benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH), an elicitor of resistance against certain pathogens. Volatile emission, herbivore infestation, pathogen infection, and plant performance (growth and grain yield) of treated and untreated maize plants were measured. Application of BTH slightly reduced volatile emission in maize, while MeJA increased the emission compared to control treatments. Despite the apparent changes in volatile emissions, the elicitor application did not consistently affect infestation by Spodoptera frugiperda larvae, the main insect pest found on the maize seedlings, and had only marginal effects on parasitism rates. Similarly, there were no treatment effects on infestation by other herbivores and pathogens. Results for the six replications that stretched over one summer and one winter season were highly variable, with parasitism rates and the species composition of the parasitoids differing significantly between seasons. This variability, as well as the severe biotic and abiotic stresses on young seedlings might explain why we measured only slight effects of elicitor application on pest incidence and biological control in this specific field study. Indeed, an additional field experiment under milder and more standardized conditions revealed that BTH induced significant resistance against Bipolaris maydis, a major pathogen in the experimental maize fields. Similar affects can be expected for herbivory and parasitism rates.
  • Publication
    Accès libre
    Attractiveness of Constitutive and Herbivore-Induced Sesquiterpene Blends of Maize to the Parasitic Wasp Cotesia marginiventris (Cresson)
    (2011)
    Fontana, Anna
    ;
    Held, Matthias 
    ;
    Fantaye, Chalie A.
    ;
    Turlings, Ted 
    ;
    Degenhardt, Jörg
    ;
    Gershenzon, Jonathan
    Plant volatile compounds induced by herbivore attack have been demonstrated to provide a signal to herbivore enemies such as parasitic wasps that use these volatiles to locate their hosts. However, in addition to herbivore-induced volatiles, plants often release volatiles constitutively. We assessed the interaction between herbivore-induced and constitutively released volatiles of maize in the attraction of the wasp Cotesia marginiventris that parasitizes herbivorous lepidopteran larvae feeding on maize. Experiments were carried out with olfactometers in which the sources of volatiles were transgenic Arabidopsis thaliana plants overexpressing maize sesquiterpene synthases that produce blends of herbivore-induced or constitutive compounds. We found that the constitutive volatiles of maize terpene synthase 8 (TPS8) were attractive to C. marginiventris, just like the herbivore-induced volatiles of TPS10 studied earlier. A mixture of both the TPS8 and TPS10 volatile blends, however, was more effective in parasitoid attraction, indicating that constitutively released sesquiterpenes enhance the attraction of those induced by herbivores. While C. marginiventris did not distinguish among the volatiles of TPS8, TPS10, nor those of another maize sesquiterpene synthase (TPS5), when these blends were combined, their attractiveness to the wasp appeared to increase with the complexity of the blend.
  • Publication
    Accès libre
    Priming by airborne signals boosts direct and indirect resistance in maize
    (2007)
    Ton, Jurriaan
    ;
    D'Alessandro, Marco
    ;
    Jourdie, Violaine
    ;
    Jakab, Gabor
    ;
    Karlen, Danielle
    ;
    Held, Matthias 
    ;
    Mauch-Mani, Brigitte 
    ;
    Turlings, Ted 
    Plants counteract attack by herbivorous insects using a variety of inducible defence mechanisms. The production of toxic proteins and metabolites that instantly affect the herbivore's development are examples of direct induced defence. In addition, plants may release mixtures of volatile organic compounds (VOCs) that indirectly protect the plant by attracting natural enemies of the herbivore. Recent studies suggest that these VOCs can also prime nearby plants for enhanced induction of defence upon future insect attack. However, evidence that this defence priming causes reduced vulnerability to insects is sparse. Here we present molecular, chemical and behavioural evidence that VOC-induced priming leads to improved direct and indirect resistance in maize. A differential hybridization screen for inducible genes upon attack by Spodoptera littoralis caterpillars identified 10 defence-related genes that are responsive to wounding, jasmonic acid (JA), or caterpillar regurgitant. Exposure to VOCs from caterpillar-infested plants did not activate these genes directly, but primed a subset of them for earlier and/or stronger induction upon subsequent defence elicitation. This priming for defence-related gene expression correlated with reduced caterpillar feeding and development. Furthermore, exposure to caterpillar-induced VOCs primed for enhanced emissions of aromatic and terpenoid compounds. At the peak of this VOC emission, primed plants were significantly more attractive to parasitic Cotesia marginiventris wasps. This study shows that VOC-induced priming targets a specific subset of JA-inducible genes, and links these responses at the molecular level to enhanced levels of direct and indirect resistance against insect attack.
  • Publication
    Accès libre
    Fungal Infection Reduces Herbivore-Induced Plant Volatiles of Maize but does not Affect Naïve Parasitoids
    (2006)
    Rostás, Michael
    ;
    Ton, Jurriaan
    ;
    Mauch-Mani, Brigitte 
    ;
    Turlings, Ted 
    Plants attacked by insects release volatile compounds that attract the herbivores' natural enemies. This so-called indirect defense is plastic and may be affected by an array of biotic and abiotic factors. We investigated the effect of fungal infection as a biotic stress agent on the emission of herbivore-induced volatiles and the possible consequences for the attraction of two parasitoid species. Maize seedlings that were simultaneously attacked by the fungus Setosphaeria turcica and larvae of Spodoptera littoralis emitted a blend of volatiles that was qualitatively similar to the blend emitted by maize that was damaged by only the herbivore, but there was a clear quantitative difference. When simultaneously challenged by fungus and herbivore, the maize plants emitted in total 47% less of the volatiles. Emissions of green leaf volatiles were unaffected. In a six-arm olfactometer, the parasitoids Cotesia marginiventris and Microplitis rufiventris responded equally well to odors of herbivore-damaged and fungus- and herbivore-damaged maize plants. Healthy and fungus-infected plants were not attractive. An additional experiment showed that the performance of S. littoralis caterpillars was not affected by the presence of the pathogen, nor was there an effect on larvae of M. rufiventris developing inside the caterpillars. Our results confirm previous indications that naïve wasps may respond primarily to the green leaf volatiles.
  • Publication
    Accès libre
    The Role of Indole and Other Shikimic Acid Derived Maize Volatiles in the Attraction of Two Parasitic Wasps
    (2006)
    D'Alessandro, Marco
    ;
    Held, Matthias 
    ;
    Triponez, Yann
    ;
    Turlings, Ted 
    After herbivore attack, plants release a plethora of different volatile organic compounds (VOCs), which results in odor blends that are attractive to predators and parasitoids of these herbivores. VOCs in the odor blends emitted by maize plants (Zea mays) infested by lepidopteran larvae are well characterized. They are derived from at least three different biochemical pathways, but the relative importance of each pathway for the production of VOCs that attract parasitic wasps is unknown. Here, we studied the importance of shikimic acid derived VOCs for the attraction of females of the parasitoids Cotesia marginiventris and Microplitis rufiventris. By incubating caterpillar-infested maize plants in glyphosate, an inhibitor of the 5-enolpyruvylshikimate-3-phospate (EPSP) synthase, we obtained induced odor blends with only minute amounts of shikimic acid derived VOCs. In olfactometer bioassays, the inhibited plants were as attractive to naive C. marginiventris females as control plants that released normal amounts of shikimic acid derived VOCs, whereas naive M. rufiventris females preferred inhibited plants to control plants. By adding back synthetic indole, the quantitatively most important shikimic acid derived VOC in induced maize odors, to inhibited plants, we showed that indole had no effect on the attraction of C. marginiventris and that M. rufiventris preferred blends without synthetic indole. Exposing C. marginiventris females either to odor blends of inhibited or control plants during oviposition experiences shifted their preference in subsequent olfactometer tests in favor of the experienced odor. Further learning experiments with synthetic indole showed that C. marginiventris can learn to respond to this compound, but that this does not affect its choices between natural induced blends with or without indole. We hypothesize that for naïve wasps the attractiveness of an herbivore-induced odor blend is reduced due to masking by nonattractive compounds, and that during oviposition experiences in the presence of complex odor blends, parasitoids strongly associate some compounds, whereas others are largely ignored.
  • Publication
    Accès libre
    A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping
    (2004)
    Turlings, Ted 
    ;
    Davison, A. C.
    ;
    Tamò, Cristina
    Behavioural assays to study insect attraction to specific odours are tedious, time consuming and often require large numbers of replications. Olfactometer and flight tunnel tests can usually only be conducted with one or two odour sources at a time. Moreover, chemical information on the odour sources has to be obtained in separate analytical studies. An olfactometer was developed in which six odours can be tested simultaneously for their relative attractiveness while during the assays, part of each test odour can be trapped for further analyses. The effectiveness of this six-arm olfactometer was tested by observing the responses of the solitary endoparasitoid Cotesia marginiventris (Cresson) to host-induced odours from young maize plants. For statistical analyses, we used log-linear models were adapted to account for overdispersion and possible positional biases. Female wasps responded extremely well in tests where they were offered a single odour source, as well as in tests with multiple choices. The responses of wasps released in groups were the same as those released individually and it was found that females did not attract or repel each other, but males preferred arms in which females had been released. Dose–response tests with varying numbers of plants or host larvae on plants revealed that the wasps responded in a dose-related manner, thus showing that the system is well suited to measure relative preference. The clear choices of the insects amongst six possibilities provided substantial statistical power. Gas chromatographic analyses of sampled air revealed clean and effective odour trapping, which largely facilitates the comparison of results from behavioural assays with the actual blends of volatiles that were emitted by the various odour sources. Advantages and disadvantages compared to other methods are discussed.
  • Publication
    Accès libre
    Differential Attractiveness of Induced Odors Emitted by Eight Maize Varieties for the Parasitoid Cotesia marginiventris : Is Quality or Quantity Important ?
    (2002)
    Hoballah, Maria Elena
    ;
    Tamò, Cristina
    ;
    Turlings, Ted 
    Herbivore-induced plant volatiles can function as indirect defense signals that attract natural enemies of herbivores. Several parasitoids are known to exploit these plant-provided cues to locate their hosts. One such parasitoid is the generalist Cotesia marginiventris, which is, among others, attracted to maize volatiles induced by caterpillar damage. Maize plants can be induced to produce the same blend of attractive volatiles by treating them with regurgitant of Spodoptera species. We collected and analyzed the regurgitant-induced emissions of two plant species (cowpea and maize) and of eight Mexican maize varieties and found significant differences among their volatile emissions, both in terms of total quantity and the quality of the blends. In a Y-tube olfactometer, the odors of the same artificially induced plant species and Mexican varieties were offered in dual choice experiments to naïve mated females of C. marginiventris. Wasps preferred cowpea over maize odor and, in 3 of 12 combinations with the maize varieties, they showed a preference for the odors of one of the varieties. A comparison of the odor collection with results from the behavioral assays indicates that not only the quantity of the volatile emissions, but also the quality composition of the volatile blends is important for attraction of C. marginiventris. The results are discussed in the context of the possibility of breeding crop varieties that are particularly attractive to parasitoids.
  • Publication
    Accès libre
    An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps
    (1993)
    Turlings, Ted 
    ;
    McCall, Philip
    ;
    Hans Alborn
    ;
    James Tumlinson
    Regurgitate of corn-fed beet armyworm (BAW) caterpillars, Spodoptera exigua, when applied to damaged sites of corn (Zea mays) seedlings, causes the release of relatively large amounts of terpenes by the seedlings several hours later. This plant response could be induced by merely placing the cut stem of seedlings in a solution of BAW regurgitate for 12 hr, a response that could not be induced by placing seedlings in water only. Regurgitate of BAW fed various diets, including a minimal diet of filter paper, were all active. However, seedlings placed in corn leaf juice, BAW hemolymph, or BAW feces extract released significantly smaller amounts of terpenes than did seedlings placed in BAW regurgitate. These results indicate that the active components are present in relatively large concentrations in regurgitate and that they are not related to the food source. Furthermore, regurgitate from several other species of caterpillars (Spodoptera frugiperda, Helicoverpa zea, Trichoplusia ni, and Anticarsia gemmatalis) as well as from the grasshopper Schistocerca americana induced the release of significant amounts of terpenes in corn seedlings. The release of these volatiles, therefore, appears to be a general response to attack by phytophagous insects. The terpene-releasing corn seedlings were highly attractive to the generalist parasitoid Cotesia marginiventris and to the specialized parasitoid Microplitis croceipes. This study confirms a systemic herbivore-elicited release of terpenes in corn. It is proposed that such chemicals serve multifunctional purposes that directly and indirectly protect plants against herbivorous arthropods and pathogens.
  • Publication
    Accès libre
    Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts
    (1991)
    Turlings, Ted 
    ;
    Tumlinson, James H.
    ;
    Heath, Robert R.
    ;
    Proveaux, Adron T.
    ;
    Doolittle, Robert E.
    Volatiles released from corn seedlings on which beet armyworm larvae were feeding were attractive to females of the parasitoid, Cotesia marginiventris (Cresson), in flight tunnel bioassays. Analyses of the collected volatiles revealed the consistent presence of 11 compounds in significant amounts. They were: (Z)-3-hexenal, (E)-2-hexenal, (Z)-3-hexen-1-ol, (Z)- 3-hexen-1-yl acetate, linalool, (3E)-4,8-dimethyl-1,3,7-nonatriene, indole, α-trans-bergamotene, (E)-β-farnesene, (E)-nerolidol, and (3E,7E)-4,8,12-trimethyl-1, 3,7,ll-tridecatetraene. A synthetic blend of all 11 compounds was slightly less attractive to parasitoid females than an equivalent natural blend. However, preflight experience with the synthetic blend instead of experience with a regular plant-host complex significantly improved the response to the synthetic blend. Our results suggest that C. marginiventris females, in their search for hosts, use a blend of airborne semiochemicals emitted by plants on which their hosts feed. The response to a particular odor blend dramatically increases after a parasitoid experiences it in association with contacting host by-products.