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

Author
item ROBERT, CHRISTELLE - Neuchatel University - Switzerland
item ERB, MATTHIAS - Max Planck Society
item HILTPOLD, IVAN - University Of Missouri
item Hibbard, Bruce
item GAILLARD, MICHAEL - University Of Neuchatel
item BILAT, JULIA - University Of Neuchatel
item DEGENHARDT, JORG - Martin Luther University
item CAMBET-PETIT-JEAN, XAVIER - University Of Neuchatel
item TURLINGS, TED - University Of Neuchatel
item ZWAHLEN, CLADIA - University Of Neuchatel

Submitted to: Plant Biotechnology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/11/2013
Publication Date: 6/1/2013
Citation: Robert, C.A., Erb, M., Hiltpold, I., Hibbard, B.E., Gaillard, M.D., Bilat, J., Degenhardt, J., Cambet-Petit-Jean, X., Turlings, T.C., Zwahlen, C. 2013. Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnology. 11:628-639.

Interpretive Summary: Genetic manipulation of plant volatile chemical emissions using transgenic techniques could be a useful tool to enhance plant defences against herbivores, but the potential costs associated with the manipulation of the genes involved in the production of volatile chemicals are unknown. We investigated the physiological and ecological effects of a transformed (genetically modified) corn line with a gene the controls the production a group of small organic compounds (terpenes). Seed germination, plant growth, and yield were lower in the transformed line. The metabolic costs that the plant has that is associated with the continuous production of terpenes provides a possible explanation as to why they are normally only produced after induction by insect feeding in non-transgenic wild and cultivated corn. The overexpression of the gene responsible for terpene synthesis in corn did not impair overall plant resistance to insects. However, we did discover that terpene production may have attracted leaf pests that resulted in an increase in leaf-damage. The opposite effect was observed below-ground: Although terpenoid producing lines were attractive to the specialist root herbivore, western corn rootworm, they did not suffer more root damage than the control plants in the field, possibly because of the enhanced attraction of nematodes that prey on the rootworm larvae. Furthermore, fewer adults of the root herbivore, southern corn rootworm, were found to emerge near plants that emitted these terpenes. Overall, under the given field conditions, the costs of constitutive production of volatile chemicals overshadowed its benefits with regards to increased defense capabilities. 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.

Technical 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 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.