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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.

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Herbivore-induced plant volatiles mediate host selection by a root herbivore

2012, Robert, Christelle Aurélie Maud, Erb, Matthias, Duployer, M., Zwahlen, Claudia, Doyen, G. R., Turlings, Ted

In response to herbivore attack, plants mobilize chemical defenses and release distinct bouquets of volatiles. Aboveground herbivores are known to use changes in leaf volatile patterns to make foraging decisions, but it remains unclear whether belowground herbivores also use volatiles to select suitable host plants. We therefore investigated how above- and belowground infestation affects the performance of the root feeder Diabrotica virgifera virgifera, and whether the larvae of this specialized beetle are able to use volatile cues to assess from a distance whether a potential host plant is already under herbivore attack. Diabrotica virgifera larvae showed stronger growth on roots previously attacked by conspecific larvae, but performed more poorly on roots of plants whose leaves had been attacked by larvae of the moth Spodoptera littoralis. Fittingly, D similar to virgifera larvae were attracted to plants that were infested with conspecifics, whereas they avoided plants that were attacked by S similar to littoralis. We identified (E)-beta-caryophyllene, which is induced by D similar to virgifera, and ethylene, which is suppressed by S similar to littoralis, as two signals used by D similar to virgifera larvae to locate plants that are most suitable for their development. Our study demonstrates that soil-dwelling insects can use herbivore-induced changes in root volatile emissions to identify suitable host plants.

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Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize

2009-9, D'Alessandro, Marco, Brunner, V., von Mérey, Georg E., Turlings, Ted

Plants infested with herbivorous arthropods emit complex blends of volatile compounds, which are used by several natural enemies as foraging cues. Despite detailed knowledge on the composition and amount of the emitted volatiles in many plant-herbivore systems, it remains largely unknown which compounds are essential for the attraction of natural enemies. In this study, we used a combination of different fractionation methods and olfactometer bioassays in order to examine the attractiveness of different compositions of volatile blends to females of the parasitoid Cotesia marginiventris. In a first step, we passed a volatile blend emitted by Spodoptera littoralis infested maize seedlings over a silica-containing filter tube and subsequently desorbed the volatiles that were retained by the silica filter (silica extract). The volatiles that broke through the silica filter were collected on and subsequently desorbed from a SuperQ filter (breakthrough). The silica extract was highly attractive to the wasps, whereas the breakthrough volatiles were not attractive. The silica extract was even more attractive than the extract that contained all herbivore-induced maize volatiles. Subsequently, we fractioned the silica extract by preparative gas-chromatography (GC) and by separating more polar from less polar compounds. In general, C. marginiventris preferred polar over non-polar compounds, but several fractions were attractive to the wasp, including one that contained compounds emitted in quantities below the detection threshold of the GC analysis. These results imply that the attractiveness of the volatile blend emitted by Spodoptera-infested maize seedlings to C. marginiventris females is determined by a specific combination of attractive and repellent/masking compounds, including some that are emitted in very small amounts. Manipulating the emission of such minor compounds has the potential to greatly improve the attraction of certain parasitoids and enhance biological control of specific insect pests.