title: Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field.
abstract: 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)-β-caryophyllene and α-humulene, was found to compromise seed germination, plant growth and yield. These physiological costs provide a possible explanation for the inducibility of an (E)-β-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)-β-caryophyllene and α-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.
authors: Laboratory for Fundamental and Applied Research in Chemical Ecology-FARCE, University of Neuchâtel, Neuchâtel, Switzerland.
authors: Christelle Aurélie Maud
authors: CA
authors: Robert
authors: Matthias
authors: M
authors: Erb
authors: Ivan
authors: I
authors: Hiltpold
authors: Bruce Elliott
authors: BE
authors: Hibbard
authors: Mickaël David Philippe
authors: MD
authors: Gaillard
authors: Julia
authors: J
authors: Bilat
authors: Jörg
authors: J
authors: Degenhardt
authors: Xavier
authors: X
authors: Cambet-Petit-Jean
authors: Ted Christiaan Joannes
authors: TC
authors: Turlings
authors: Claudia
authors: C
authors: Zwahlen
mesh_terms: D019883:Alkyl and Aryl Transferases / Q000378:metabolism; D000818:Animals; D005818:Genetic Engineering; D060434:Herbivory; D007313:Insecta / Q000502:physiology; D000081222:Monocyclic Sesquiterpenes; D009348:Nematoda / Q000502:physiology; D063245:Plant Development; D018517:Plant Roots / Q000502:physiology; D030821:Plants, Genetically Modified; D000081223:Polycyclic Sesquiterpenes; D018570:Risk Assessment; D012717:Sesquiterpenes / Q000378:metabolism; D013729:Terpenes / Q000378:metabolism; D055549:Volatile Organic Compounds / Q000378:metabolism*; D003313:Zea mays / Q000201:enzymology / Q000235:genetics* / Q000378:metabolism*
chemical_list: D000081222:Monocyclic Sesquiterpenes; D000081223:Polycyclic Sesquiterpenes; D012717:Sesquiterpenes; D013729:Terpenes; D055549:Volatile Organic Compounds; C042686:humulene; C024714:caryophyllene; D019883:Alkyl and Aryl Transferases; C108877:terpene synthase