Insect damage to plants is known to up-regulate defense and down-regulate growth processes. While there are frequent reports about up-regulation of defense signaling and production of defense metabolites in response to herbivory, much less is understood about the mechanisms by which growth and carbon assimilation are down-regulated. Here we demonstrate that insect herbivory down-regulates the 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway in Arabidopsis (Arabidopsis thaliana), a pathway making primarily metabolites for use in photosynthesis. Simulated feeding by the generalist herbivore Spodoptera littoralis suppressed flux through the MEP pathway and decreased steady-state levels of the intermediate 1-deoxy-D-xylulose 5-phosphate (DXP). Simulated herbivory also increased reactive oxygen species content which caused the conversion of β-carotene to β-cyclocitral (βCC). This volatile oxidation product affected the MEP pathway by directly inhibiting DXP synthase (DXS), the rate-controlling enzyme of the MEP pathway in Arabidopsis and inducing plant resistance against S. littoralis. βCC inhibited both DXS transcript accumulation and DXS activity. Molecular models suggested that βCC binds to DXS at the binding site for the thymine pyrophosphate cofactor and blocks catalysis, which was confirmed by direct assays of βCC with the purified DXS protein in vitro. Another intermediate of the MEP pathway, 2-C-methyl-D-erythritol-2, 4-cyclodiphosphate, which is known to stimulate salicylate defense signaling, showed greater accumulation and enhanced export out of the plastid in response to simulated herbivory. Together, our work implicates βCC as a signal of herbivore damage in Arabidopsis that increases defense and decreases flux through the MEP pathway, a pathway involved in growth and carbon assimilation. Significance Plants are known to respond to insect herbivory in multiple ways. Under herbivore attack, plants increase their commitment to defense but decrease their commitment to growth and carbon assimilation. Unfortunately, this second aspect is less studied. Here we report the discovery of an herbivore-triggered signal (β-cyclocitral) that enhances plant resistance and down-regulates the methylerythritol-4-phosphate (MEP) pathway of terpenoid biosynthesis. The MEP pathway supplies the precursors for many metabolites important in photosynthesis such as chlorophylls, carotenoids, plastoquinones, phylloquinones, and tocopherols. We also elucidated the mechanism responsible for the reduction of MEP pathway flux under herbivory and found that β-cyclocitral inhibits the activity of the first step of the pathway, which was also shown to control flux under normal growth conditions.

White spruce (Picea glauca) emits monoterpenes that function as defensive signals and weapons after herbivore attack. We assessed the effects of drought and methyl jasmonate (MeJA) treatment, used as a proxy for herbivory, on monoterpenes and other isoprenoids in P. glauca. The emission of monoterpenes was significantly increased after MeJA treatment compared to the control, but drought suppressed the MeJA-induced increase. The composition of the emitted blend was altered strongly by stress, with drought increasing the proportion of oxygenated compounds and MeJA increasing the proportion of induced compounds such as linalool and (E)-β-ocimene. In contrast, no treatment had any significant effect on the levels of stored monoterpenes and diterpenes. Among other MEP pathway-derived isoprenoids, MeJA treatment decreased chlorophyll levels by 40%, but had no effect on carotenoids, while drought stress had no impact on either of these pigment classes. Of the three described spruce genes encoding 1-deoxy-D-xylulose-5-phosphate synthase (DXS) catalyzing the first step of the MEP pathway, the expression of only one, DXS2B, was affected by our treatments, being increased by MeJA and decreased by drought. These findings show the sensitivity of monoterpene emission to biotic and abiotic stress regimes, and the mediation of the response by DXS genes.