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

Sirsha Mitra, Roger Estrada-Tejedor, Daniel C. Volke, Michael A. Phillips, Jonathan Gershenzon, Louwrance P. Wright

Research output: Indexed journal article Articlepeer-review

34 Citations (Scopus)

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 beta-carotene to beta-cyclocitral (beta CC). 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. beta CC inhibited both DXS transcript accumulation and DXS activity. Molecular models suggested that beta CC binds to DXS at the binding site for the thymine pyrophosphate cofactor and blocks catalysis, which was confirmed by direct assays of beta CC 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 beta CC 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.
Original languageEnglish
Article numbere2008747118
Number of pages12
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number10
DOIs
Publication statusPublished - 9 Mar 2021

Keywords

  • Apocarotenoids
  • Isoprenoid
  • Mechanical damage
  • Methylerythritol-4phosphate pathway
  • Simulated herbivory

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