Negative regulation of plastidial isoprenoid pathway by herbivore-induced β-cyclocitral in Arabidopsis thaliana

Abstract

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.

β-Cyclocitral, a Master Regulator of Multiple Stress-Responsive Genes in Solanum lycopersicum L. Plants

“…Previously, it was shown that βCC treatment enhances resistance to high light stress and regulates singlet oxygen-responsive genes. Recently, we have seen that in addition to high light, βCC treatment also develops resistance to drought stress and herbivory in tomato and Arabidopsis plants, respectively [3,10,11]. Therefore, we hypothesized that βCC plays a pivotal role in the regulation of multiple stress responses.…”

“…A total of 92 DEGs that are responsive to abiotic and biotic stresses are involved in more than one stress; therefore, the same DEG is counted for each stress it is involved in. Abiotic stress-responsive DEGs include drought (20), heat (18), salinity (14), cold (11), oxidative (5), light (4), and hypoxia (2) (Figure 5c left panel). Similarly, DEGs responsive to biotic stresses include the attack of fungi (11), Enrichment analysis revealed that only the upregulated genes are annotated with GO terms belonging to the group RS.…”

“…Oxidative cleavage of β-carotene produces a number of short-chain volatiles commonly known as apocarotenoids [9]. Interestingly, β-cyclocitral (βCC) is the most abundant apocarotenoid of β-carotene [10] that accumulates under high light, drought, and herbivory [7,9,11]. In addition, simulated herbivory and jasmonic acid (JA) application also resulted in increased accumulation of βCC [11,12].…”

“…Interestingly, β-cyclocitral (βCC) is the most abundant apocarotenoid of β-carotene [10] that accumulates under high light, drought, and herbivory [7,9,11]. In addition, simulated herbivory and jasmonic acid (JA) application also resulted in increased accumulation of βCC [11,12]. Recent studies showed that exogenous application of βCC primes plants against drought and develops resistance against insect herbivores [3,11].…”

“…In addition, simulated herbivory and jasmonic acid (JA) application also resulted in increased accumulation of βCC [11,12]. Recent studies showed that exogenous application of βCC primes plants against drought and develops resistance against insect herbivores [3,11]. Together, these findings indicate that, presumably, βCC is capable of eliciting multiple stress signals.…”