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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
    Métadonnées seulement
    Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field
    (2013)
    Robert, Christelle Aurélie Maud
    ;
    Erb, Matthias 
    ;
    Hiltpold, Ivan 
    ;
    Hibbard, Bruce Elliott
    ;
    Gaillard, Mickaël David Philippe
    ;
    Bilat, Julia
    ;
    Degenhardt, Jörg
    ;
    Cambet-Petit-Jean, Xavier
    ;
    Turlings, Ted 
    ;
    Zwahlen, Claudia 
    Genetic manipulation of plant volatile emissions is a promising tool to enhance plant defences against herbivores. However, the potential costs associated with the manipulation of specific volatile synthase genes are unknown. Therefore, we investigated the physiological and ecological effects of transforming a maize line with a terpene synthase gene in field and laboratory assays, both above- and below ground. The transformation, which resulted in the constitutive emission of (E)--caryophyllene and -humulene, was found to compromise seed germination, plant growth and yield. These physiological costs provide a possible explanation for the inducibility of an (E)--caryophyllene-synthase gene in wild and cultivated maize. The overexpression of the terpene synthase gene did not impair plant resistance nor volatile emission. However, constitutive terpenoid emission increased plant apparency to herbivores, including adults and larvae of the above ground pest Spodoptera frugiperda, resulting in an increase in leaf damage. Although terpenoid overproducing lines were also attractive to the specialist root herbivore Diabrotica virgifera virgifera below ground, they did not suffer more root damage in the field, possibly because of the enhanced attraction of entomopathogenic nematodes. Furthermore, fewer adults of the root herbivore Diabrotica undecimpunctata howardii were found to emerge near plants that emitted (E)--caryophyllene and -humulene. Yet, overall, under the given field conditions, the costs of constitutive volatile production overshadowed its benefits. This study highlights the need for a thorough assessment of the physiological and ecological consequences of genetically engineering plant signals in the field to determine the potential of this approach for sustainable pest management strategies.
  • 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
    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
    The role of abscisic acid and water stress in root herbivore-induced leaf resistance
    (2011)
    Erb, Matthias 
    ;
    Köllner, Tobias G.
    ;
    Degenhardt, Jörg
    ;
    Zwahlen, Claudia 
    ;
    Hibbard, Bruce E.
    ;
    Turlings, Ted 

    Herbivore-induced systemic resistance occurs in many plants and is commonly assumed to be adaptive. The mechanisms triggered by leaf-herbivores that lead to systemic resistance are largely understood, but it remains unknown how and why root herbivory also increases resistance in leaves.
    To resolve this, we investigated the mechanism by which the root herbivore Diabrotica virgifera induces resistance against lepidopteran herbivores in the leaves of Zea mays.
    Diabrotica virgifera infested plants suffered less aboveground herbivory in the field and showed reduced growth of Spodoptera littoralis caterpillars in the laboratory. Root herbivory did not lead to a jasmonate-dependent response in the leaves, but specifically triggered water loss and abscisic acid (ABA) accumulation. The induction of ABA by itself was partly responsible for the induction of leaf defenses, but not for the resistance against S. littoralis. Root-herbivore induced hydraulic changes in the leaves, however, were crucial for the increase in insect resistance.
    We conclude that the induced leaf resistance after root feeding is the result of hydraulic changes, which reduce the quality of the leaves for chewing herbivores. This finding calls into question whether root-herbivore induced leaf-resistance is an evolved response.
  • Publication
    Accès libre
    The underestimated role of roots in defense against leaf attackers
    (2009)
    Erb, Matthias 
    ;
    Lenk, Claudia
    ;
    Degenhardt, Jörg
    ;
    Turlings, Ted 
    Plants have evolved intricate strategies to withstand attacks by herbivores and pathogens. Although it is known that plants change their primary and secondary metabolism in leaves to resist and tolerate aboveground attack, there is little awareness of the role of roots in these processes. This is surprising given that plant roots are responsible for the synthesis of plant toxins, play an active role in environmental sensing and defense signaling, and serve as dynamic storage organs to allow regrowth. Hence, studying roots is essential for a solid understanding of resistance and tolerance to leaf-feeding insects and pathogens. Here, we highlight this function of roots in plant resistance to aboveground attackers, with a special focus on systemic signaling and insect herbivores.
  • 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
    Accès libre
    Interactions between Arthropod-Induced Aboveground and Belowground Defenses in Plants
    (2008)
    Erb, Matthas
    ;
    Ton, Jurriaan
    ;
    Degenhardt, Jörg
    ;
    Turlings, Ted 
  • Publication
    Accès libre
    The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores
    (2006)
    Schnee, Christiane
    ;
    Köllner, Tobias G.
    ;
    Held, Matthias 
    ;
    Turlings, Ted 
    ;
    Gershenzon, Jonathan
    ;
    Degenhardt, Jörg
    Plants can defend themselves against herbivores by attracting natural enemies of the herbivores. The cues for attraction are often complex mixtures of herbivore-induced plant volatiles, making it difficult to demonstrate the role of specific compounds. After herbivory by lepidopteran larvae, maize releases a mixture of volatiles that is highly attractive to females of various parasitic wasp species. We identified the terpene synthase TPS10 that forms (E)-β-farnesene, (E)-α-bergamotene, and other herbivory-induced sesquiterpene hydrocarbons from the substrate farnesyl diphosphate. The corresponding gene is expressed in response to herbivore attack and is regulated at the transcript level. Overexpression of tps10 in Arabidopsis thaliana resulted in plants emitting high quantities of TPS10 sesquiterpene products identical to those released by maize. Using these transgenic Arabidopsis plants as odor sources in olfactometer assays showed that females of the parasitoid Cotesia marginiventris learn to exploit the TPS10 sesquiterpenes to locate their lepidopteran hosts after prior exposure to these volatiles in association with hosts. This dissection of the herbivore-induced volatile blend demonstrates that a single gene such as tps10 can be sufficient to mediate the indirect defense of maize against herbivore attack.
  • Publication
    Accès libre
    Recruitment of entomopathogenic nematodes by insect-damaged maize roots
    (2005)
    Rasmann, Sergio 
    ;
    Köllner, Tobias G.
    ;
    Degenhardt, Jörg
    ;
    Hiltpold, Ivan 
    ;
    Toepfer, Stefan
    ;
    Kuhlmann, Ulrich
    ;
    Gershenzon, Jonathan
    ;
    Turlings, Ted 
    Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E)-β-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E)-β-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-β-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.
  • Publication
    Accès libre
    Costs of induced volatile production in maize
    (2004)
    Hoballah, Maria Elena
    ;
    Köllner, Tobias G.
    ;
    Degenhardt, Jörg
    ;
    Turlings, Ted 
    Herbivore-induced plant volatiles have been shown to serve as indirect defence signals that attract natural enemies of herbivores. Parasitoids and predators exploit these plant-provided cues to locate their victims and several herbivores are repelled by the volatiles. Recently, benefits, in terms of plant fitness, from the action of the parasitoids were shown for a few systems. However, the cost of production of herbivore-induced volatiles for the plant remains unknown. Here, we estimate the fitness cost of the production of induced volatiles in maize, Zea mays. Plants were treated with regurgitant of Spodoptera littoralis or with the elicitor volicitin and we measured dry weight of plant parts at specific times after treatments. After a two-week treatment period, the dry-weight of leaves of induced plants was lower than that of un-induced plants, suggesting a metabolic cost for induced defence. However, maize plants seem to compensate for this loss during subsequent growth, since seed production at maturity was not different for unharmed plants and plants treated with caterpillar regurgitant. For volicitin treated plants a small but significant reduction in seed production was found. It is likely that the treatments also induced the production of other defence compounds, which will contribute to the cost. Yet, a comparison of six maize inbred lines with distinct differences in volatile emissions showed a strong correlation between the intensity of induced emissions and reduction in plant performance. An analysis of the terpenoids that accumulated in the leaves of the inbred lines revealed non-volatilised compounds are constitutively present in maize and only the volatilised compounds are induced. Interestingly, the lines that released the largest amounts of induced volatiles also contained more of the non-volatile terpenoids. Based on these results and results from a previous study on the benefits of attracting parasitoids, we conclude that costs of induced volatile production in plants are counterbalanced by the benefits as long as natural enemies of the herbivores are present in the environment.