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Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field

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 Christiaan Joannes, Zwahlen, Claudia
Plant biotechnology journal 2013 v.11 pp. 628
Diabrotica undecimpunctata, Diabrotica virgifera, Spodoptera frugiperda, beta-caryophyllene, biosynthesis, corn, cost benefit analysis, crop yield, emissions, entomopathogenic nematodes, environmental impact, gene overexpression, genetic engineering, herbivores, humulene, imagos, larvae, pest management, plant growth, seed germination, transgenes, transgenic plants, volatile organic compounds
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 an terpene synthase gene in field and laboratory assays, both above- and below-ground. The transformation, which resulted in the constitutive emission of (E)-ß-caryophyllene and a-humulene, was found to compromise seed germination, plant growth and yield. These physiological costs provide a possible explanation for the inducibility of an (E)-ß-caryophyllene-synthase gene in wild and cultivated maize. The overexpression of the terpene synthase gene did not impair plant resistance nor volatile emission. However, terpenoid emission increased plant apparency to herbivores, including adults and larvae of the aboveground pest Spodoptera frugiperda, resulting in an increase in leaf-damage. The opposite effect was observed below-ground: Although terpenoid producing lines were attractive to the specialist root herbivore Diabrotica virgifera virgifera, 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)-ß-caryophyllene and a-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 order to determine the potential of this approach for sustainable pest management strategies.