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Title: Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore

Author
item ROBERT, CHRISTELLE - Max Planck Society
item FRANK, DANIEL - West Virginia University
item LEACH, KRISTEN - University Of Missouri
item TURLINGS, TED - University Of Neuchatel
item Hibbard, Bruce
item ERB, MATTHIAS - Max Planck Society

Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/29/2013
Publication Date: 4/15/2013
Citation: Robert, C.A., Frank, D.L., Leach, K.A., Turlings, T.C., Hibbard, B.E., Erb, M. 2013. Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore. Journal of Chemical Ecology. 39:507-515.

Interpretive Summary: Microbes living within their insect hosts influence many important host metabolic and developmental processes. It has been speculated that these microbes may also help to manipulate and suppress plant defenses to the benefit of their host insects. Recently, natural microbes (Wolbachia) in the root herbivore western corn rootworm (WCR) were reported to suppress expression of maize genes associated with insect defense, which could explain why plants infested with WCR become more susceptible to subsequent WCR attack. To test this hypothesis, we cured WCR of Wolbachia, its primary internal microbe and tested whether Wolbachia-free WCR elicit different direct and indirect defense responses in maize roots. The absense of Wolbachia (normally present) did not alter the induction of direct defense genes or development rates of WCR on a susceptible maize hybrid or resistant line. Furthermore, maize plants infested with WCR emitted the same amount of a volatile signal that serves as a foraging cue for WCR and attracts nematodes that kill WCR. The effectiveness of the nematode to infest and kill WCR was also not influenced by the Wolbachia either. Contrary to the recent report, these results show that the defensive systems of maize are immune to manipulation by Wolbachia microbes normally present in WCR, and WCR does not seem to derive any plant-mediated benefits from Wolbachia.

Technical Abstract: Insect endosymbionts influence many important metabolic and developmental processes of their host. It has been speculated that they may also help to manipulate and suppress plant defenses to the benefit of herbivores. Recently, endosymbionts of the root herbivore Diabrotica virgifera virgifera have been reported to suppress the induction of defensive transcripts in maize roots, which may explain why attacked plants become more susceptible to subsequent D. v. virgifera attack. To test this hypothesis, we cured the specialist maize feeder from its major endosymbiont Wolbachia and tested whether endosymbiont-free individuals elicit different direct and indirect defense responses in maize roots. The presence of endosymbionts did not alter the induction of direct defense marker genes and resistance in a susceptible maize hybrid and a resistant line. Furthermore, attacked maize plants emitted the same amount of (E)-ß-caryophyllene, a volatile signal that serves as foraging cue for D. v. virgifera larvae and attracts entomopathogenic nematodes. The effectiveness of the entomopathogenic nematode Heterorhabditis bacteriophora to infest D. v. virgifera was not influenced by the cured endosymbionts either. These results show that the defensive systems of maize are immune to manipulation by Wolbachia endosymbionts of D. v. virgifera. Consequently, the specialist herbivore does not seem to derive any plant-mediated benefits from the presence of its major endosymbiont.