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 in Arabidopsis thaliana

Abstract

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 Arabidopsis hds-3 mutant, 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 in hds-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. The hds-3 mutant also showed enhanced resistance to the phloem-feeding aphid Brevicoryne brassicae due 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 the hds-3 mutant. 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.

Keywords

Arabidopsis thaliana; isoprenoids; metabolite profiling; NMR; plant defense signaling; plant metabolism

Published in

Plant Journal
2015, volume: 82, number: 1, pages: 122-137

SLU Authors

• Onkokesung, Nawaporn

  • Department of Plant Breeding, Swedish University of Agricultural Sciences
    
  • Wageningen University

UKÄ Subject classification

Botany
Plant Biotechnology

Publication identifier

• DOI: https://doi.org/10.1111/tpj.12798

Permanent link to this page (URI)

https://res.slu.se/id/publ/132067