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Published on October 26, 2007; 10.1104/pp.107.108811

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Received September 8, 2007
Accepted October 21, 2007

Silencing Geranylgeranyl Diphosphate Synthase in Nicotiana attenuata Dramatically Impairs Resistance to Manduca sexta

Amir Reza Jassbi , Klaus Gase , Christian Hettenhausen , Axel Schmidt , and Ian T. Baldwin *

Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knoll-Strasse 8, D-07745 Jena, Germany; Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knoll-Strasse 8, D-07745 Jena, Germany

* Corresponding author; email: baldwin{at}ice.mpg.de.

In bioassays with artificial diets, the 17-hydroxygeranyllinalool diterpenoid glycosides (HGL-DTGs) of Nicotiana attenuata function as antifeedants for the plant's adapted herbivore, Manduca sexta. To determine whether HGL-DTGs have a defensive function in planta, we suppressed HGL-DTG production by silencing the source of the geranylgeranyl diphosphates (GGPPs) required for geranyllinalool biosynthesis, a key intermediate. We used virus-induced gene silencing (VIGS) to suppress transcript levels of geranylgeranyl diphosphate synthase (Naggpps) and farnesyl diphosphate synthase (Nafpps); northern blotting and RT-PCR to quantify transcript accumulations; and radio GC to analyze prenyltransferase specificity. Silencing Nafpps transcript accumulation had no effect on the accumulation of HGL-DTGs but decreased leaf steroid content, demonstrating that DTG-synthesizing enzymes do not use GGPP derived from farnesyl diphosphate (FPP) and confirming FPP's role as a steroid precursor. Unlike phytoene-desaturase-silenced(Napds) plants, which rapidly bleached, silencing Naggpps reduced HGL-DTG but not carotenoids or chlorophyll contents, demonstrating that Naggpps supplies substrates for GGPP biosynthesis for HGL-DTGs, but not for phytoene or phytol. Expression of Naggpps in E. coli revealed that the recombinant protein catalyzes the GGPP synthesis from isopentenyl diphosphate ([1-14C] IPP) and dimethylallyl diphosphate (DMAPP). When fed on silenced plants, Manduca sexta larvae gained up to 3 times more mass than those that fed on empty vector control (EV) plants, or plants silenced in Nafpps, trypsin protease inhibitors(TPI), or nicotine. We conclude that HGL-DTGs or other minor undetected diterpenoids derived from GGPP function as direct defenses for N. attenuata and are more potent than nicotine or TPIs against attack by M. sexta larvae.




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