The diversion of 2-C-methyl-d-erythritol-2,4-cyclodiphosphate from the 2-C-methyl-d-erythritol 4-phosphate pathway to hemiterpene glycosides mediates stress responses inArabidopsis thaliana

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2-C-Methyl-d-erythritol-2,4-cyclodiphosphate (MEcDP) is an intermediate of the plastid-localized 2-C-methyl-d-erythritol-4-phosphate (MEP) pathway which supplies isoprenoid precursors for photosynthetic pigments, redox co-factor side chains, plant volatiles, and phytohormones. The Arabidopsishds-3mutant, defective in the 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase step of the MEP pathway, accumulates its substrate MEcDP as well as the free tetraol 2-C-methyl-d-erythritol (ME) and glucosylated ME metabolites, a metabolic diversion also occurring in wild type plants. MEcDP dephosphorylation to the free tetraol precedes glucosylation, a process which likely takes place in the cytosol. Other MEP pathway intermediates were not affected inhds-3. Isotopic labeling, dark treatment, and inhibitor studies indicate that a second pool of MEcDP metabolically isolated from the main pathway is the source of a signal which activates salicylic acid induced defense responses before its conversion to hemiterpene glycosides. Thehds-3mutant also showed enhanced resistance to the phloem-feeding aphidBrevicoryne brassicaedue to its constitutively activated defense response. However, this MEcDP-mediated defense response is developmentally dependent and is repressed in emerging seedlings. MEcDP and ME exogenously applied to adult leaves mimics many of the gene induction effects seen in thehds-3mutant. In conclusion, we have identified a metabolic shunt from the central MEP pathway that diverts MEcDP to hemiterpene glycosides via ME, a process linked to balancing plant responses to biotic stress.

Significance Statement

2-C-methyl-D-erythritol-2,4-cyclodiphosphate (MEcDP) is a key intermediate in plastidial isoprenoid biosynthesis that was recently implicated in defense signaling. We describe a metabolic shunt involving MEcDP export from the plastidial pool and conversion to hemiterpene glycosides whose intermediates mediate salicylic acid-based signaling in Arabidopsis thaliana.

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