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Turlings, Ted

Nom
Turlings, Ted
Affiliation principale
Fonction
Professeur ordinaire
Email
ted.turlings@unine.ch
Identifiants
https://libra.unine.ch/handle/123456789/330

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  • Publication
    Accès libre
    Belowground and aboveground herbivory differentially affect the transcriptome in roots and shoots of maize
    (2022-7-22)
    Ye, Wenfeng
    ;
    Bustos Segura, Carlos 
    ;
    Degen, Thomas 
    ;
    Erb, Matthias 
    ;
    Turlings, Ted 
    Plants recognize and respond to feeding by herbivorous insects by upregulating their local and systemic defenses. While defense induction by aboveground herbivores has been well studied, far less is known about local and systemic defense responses against attacks by belowground herbivores. Here, we investigated and compared the responses of the maize transcriptome to belowground and aboveground mechanical damage and infestation by two well-adapted herbivores: the soil-dwelling western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) and the leaf- chewing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). In responses to both herbivores, maize plants were found to alter local transcription of genes involved in phytohormone signaling, primary and secondary metabolism. Induction by real herbivore damage was considerably stronger and modified the expression of more genes than mechanical damage. Feeding by the corn rootworm had a strong impact on the shoot transcriptome, including the activation of genes involved in defense and development. By contrast, feeding by the fall armyworm induced only few transcriptional changes in the roots. In conclusion, feeding by a leaf chewer and a root feeder differentially affects the local and systemic defense of maize plants. Besides revealing clear differences in how maize plants respond to feeding by these specialized herbivores, this study reveals several novel genes that may play key roles in plant–insect interactions and thus sets the stage for in depth research into the mechanism that can be exploited for improved crop protection.
  • Publication
    Métadonnées seulement
    3-D-Glucopyranosyl-6-methoxy-2-benzoxazolinone (MBOA-N-Glc) is an insect detoxification product of maize 1,4-benzoxazin-3-ones
    (2014)
    Maag, Daniel 
    ;
    Dalvit, Claudio 
    ;
    Thevenet, Damien 
    ;
    Köhler, Angela
    ;
    Wouters, Felipe C.
    ;
    Vassão, Daniel G.
    ;
    Gershenzon, Jonathan
    ;
    Wolfender, Jean-Luc
    ;
    Turlings, Ted 
    ;
    Erb, Matthias 
    ;
    Glauser, Gaetan
    In order to defend themselves against arthropod herbivores, maize plants produce 1,4-benzoxazin-3-ones (BXs), which are stored as weakly active glucosides in the vacuole. Upon tissue disruption, BXs come into contact with ?-glucosidases, resulting in the release of active aglycones and their breakdown products. While some aglycones can be reglucosylated by specialist herbivores, little is known about how they detoxify BX breakdown products. Here we report on the structure of an N-glucoside, 3-?-d-glucopyranosyl-6-methoxy-2-benzoxazolinone (MBOA-N-Glc), purified from Spodoptera frugiperda faeces. In vitro assays showed that MBOA-N-Glc is formed enzymatically in the insect gut using the BX breakdown product 6-methoxy-2-benzoxazolinone (MBOA) as precursor. While Spodoptera littoralis and S. frugiperda caterpillars readily glucosylated MBOA, larvae of the European corn borer Ostrinia nubilalis were hardly able to process the molecule. Accordingly, Spodoptera caterpillar growth was unaffected by the presence of MBOA, while O. nubilalis growth was reduced. We conclude that glucosylation of MBOA is an important detoxification mechanism that helps insects tolerate maize BXs.
  • Publication
    Métadonnées seulement
    Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore
    (2013)
    Robert, Christelle Aurélie Maud
    ;
    Frank, Daniel L.
    ;
    Leach, Kristen A.
    ;
    Turlings, Ted 
    ;
    Hibbard, Bruce Elliott
    ;
    Erb, Matthias 
  • Publication
    Métadonnées seulement
    Induction of root-resistance by leaf-herbivory follows a vertical gradient
    (2011)
    Erb, Matthias 
    ;
    Robert, Christelle Aurélie Maud
    ;
    Turlings, Ted 
    Leaf-herbivory can lead to systemic changes in root metabolism and resistance. As yet, it is unknown if these changes affect the whole root system, or if they are more pronounced in the upper root parts, which are closer to the actual site of attack. As this spatial aspect may be an important determinant of the interactions that can be expected to occur within the rhizosphere, we investigated if leaf-herbivore induced root resistance differs between upper and lower roots of maize. We also tested if the density of leaf-herbivores correlates with intensity of the root response. The systemic increase in resistance was found to be more pronounced in the upper than the lower roots and was independent of leaf herbivore density. The results suggest that there is a vertical gradient in the strength of the root response following leaf-herbivory, and that soil organisms living closer to the surface may be more affected by leaf-attack than the ones living in deeper soil layers.
  • Publication
    Métadonnées seulement
    Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp
    (2011)
    Fontana, A.
    ;
    Held, Matthias 
    ;
    Fantaye, C. 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
    Métadonnées seulement
    Induction and detoxification of maize 1,4-benzoxazin-3-ones by insect herbivores
    (2011)
    Glauser, Gaëtan 
    ;
    Marti, Guillaume
    ;
    Villard, Neil 
    ;
    Doyen, Gwladys A.
    ;
    Wolfender, Jean-Luc
    ;
    Turlings, Ted 
    ;
    Erb, Matthias 
    In monocotyledonous plants, 1,4-benzoxazin-3-ones, also referred to as benzoxazinoids or hydroxamic acids, are one of the most important chemical barriers against herbivores. However, knowledge about their behavior after attack, mode of action and potential detoxification by specialized insects remains limited. We chose an innovative analytical approach to understand the role of maize 1,4-benzoxazin-3-ones in plant?insect interactions. By combining unbiased metabolomics screening and simultaneous measurements of living and digested plant tissue, we created a quantitative dynamic map of 1,4-benzoxazin-3-ones at the plant?insect interface. Hypotheses derived from this map were tested by specifically developed in vitro assays using purified 1,4-benzoxazin-3-ones and active extracts from mutant plants lacking 1,4-benzoxazin-3-ones. Our data show that maize plants possess a two-step defensive system that effectively fends off both the generalist Spodoptera littoralis and the specialist Spodoptera frugiperda. In the first step, upon insect attack, large quantities of 2-?-d-glucopyranosyloxy-4,7-dimethoxy-1,4-benzoxazin-3-one (HDMBOA-Glc) are formed. In the second step, after tissue disruption by the herbivores, highly unstable 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one (HDMBOA) is released by plant-derived ?-glucosidases. HDMBOA acts as a strong deterrent to both S. littoralis and S. frugiperda. Although constitutively produced 1,4-benzoxazin-3-ones such as 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) are detoxified via glycosylation by the insects, no conjugation of HDMBOA in the insect gut was found, which may explain why even the specialist S. frugiperda has not evolved immunity against this plant defense. Taken together, our results show the benefit of using a plant?insect interface approach to elucidate plant defensive processes and unravel a potent resistance mechanism in maize.
  • Publication
    Accès libre
    Restoring a maize root signal that attracts insect-killing nematodes to control a major pest
    (2009)
    Degenhardt, Jörg
    ;
    Hiltpold, Ivan 
    ;
    Köllner, Tobias G.
    ;
    Frey, Monika
    ;
    Gierl, Alfons
    ;
    Gershenzon, Jonathan
    ;
    Hibbard, Bruce E.
    ;
    Ellersieck, Mark R.
    ;
    Turlings, Ted 
    When attacked by herbivorous insects, plants emit volatile compounds that attract natural enemies of the insects. It has been proposed that these volatile signals can be manipulated to improve crop protection. Here, we demonstrate the full potential of this strategy by restoring the emission of a specific belowground signal emitted by insect-damaged maize roots. The western corn rootworm induces the roots of many maize varieties to emit (E)-β-caryophyllene, which attracts entomopathogenic nematodes that infect and kill the voracious root pest. However, most North American maize varieties have lost the ability to emit (E)-β-caryophyllene and may therefore receive little protection from the nematodes. To restore the signal, a nonemitting maize line was transformed with a (E)-β-caryophyllene synthase gene from oregano, resulting in constitutive emissions of this sesquiterpene. In rootworm-infested field plots in which nematodes were released, the (E)-β-caryophyllene-emitting plants suffered significantly less root damage and had 60% fewer adult beetles emerge than untransformed, nonemitting lines. This demonstration that plant volatile emissions can be manipulated to enhance the effectiveness of biological control agents opens the way for novel and ecologically sound strategies to fight a variety of insect pests.
  • Publication
    Métadonnées seulement
    Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naive parasitoids
    (2006)
    Rostas, 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 naive wasps may respond primarily to the green leaf volatiles.
  • Publication
    Métadonnées seulement
    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 naive 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
    Métadonnées seulement
    The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles
    (2005)
    Hoballah, Maria Elena
    ;
    Turlings, Ted 
    The odor produced by a plant under herbivore attack is often used by parasitic wasps to locate hosts. Any type of surface damage commonly causes plant leaves to release so-called green leaf volatiles, whereas blends of inducible compounds are more specific for herbivore attack and can vary considerably among plant genotypes. We compared the responses of naive and experienced parasitoids of the species Cotesia marginiventris and Microplitis rufiventris to volatiles from maize leaves with fresh damage (mainly green leaf volatiles) vs. old damage (mainly terpenoids) in a six-arm olfactometer. These braconid wasps are both solitary endoparasitoids of lepidopteran larvae, but differ in geographical origin and host range. In choice experiments with odor blends from maize plants with fresh damage vs. blends from plants with old damage, inexperienced C. marginiventris showed a preference for the volatiles from freshly damaged leaves. No such preference was observed for inexperienced M. rufiventris. After an oviposition experience in hosts feeding on maize plants, C. marginiventris females were more attracted by a mixture of volatiles from fresh and old damage. Apparently, C. marginiventris has an innate preference for the odor of freshly damaged leaves, and this preference shifts in favor of a blend containing a mixture of green leaf volatiles plus terpenoids, after experiencing the latter blend in association with hosts. M. rufiventris responded poorly after experience and preferred fresh damage odors. Possibly, after associative learning, this species uses cues that are more directly related with the host presence, such as volatiles from host feces, which were not present in the odor sources offered in the olfactometer. The results demonstrate the complexity of the use of plant volatiles by parasitoids and show that different parasitoid species have evolved different strategies to exploit these signals.