Deep metabolomics revealed trajectories of jasmonate signaling-mediated primary metabolism in Arabidopsis upon Spodoptera litura herbivory

Physiol Plant. 2025 Jan-Feb;177(1):e70035. doi: 10.1111/ppl.70035.

Abstract

Plants defend against chewing herbivores by up-regulating jasmonic acid (JA) signaling, which activates downstream signaling cascades and produces numerous secondary metabolites that act as defense molecules against the herbivores. Although secondary metabolism always remains a focus of research, primary metabolism is also reported to be realigned upon herbivory. However, JA signaling-mediated modulation of primary metabolites and their metabolic pathways in plants are mostly unexplored. Here, we applied gas chromatography-mass spectrometry-based untargeted metabolomics aided with computational statistical frameworks on wild type Arabidopsis, mutants of active JA receptor (i.e., CORONATINE-INSENSITIVE 1, COI1-1) and downstream transcription factor (i.e., MYC2) to navigate the JA signaling-mediated primary metabolism alterations during herbivory. Pathway and metabolite's chemical class enrichment analysis revealed JA signaling is crucial for constitutive as well as herbivore-induced primary metabolism and topology of their interaction networks. JA signaling majorly modulated alterations of sugars, amino acids and related metabolites. Herbivory-mediated sugar depletion and induction of methionine for aliphatic glucosinolates are also dependent on JA signaling. Taken together, our results demonstrate trails of JA signaling-mediated primary metabolic alterations associated with herbivory.

MeSH terms

  • Animals
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Arabidopsis* / physiology
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • Cyclopentanes* / metabolism
  • Gas Chromatography-Mass Spectrometry
  • Gene Expression Regulation, Plant
  • Glucosinolates / metabolism
  • Herbivory* / physiology
  • Metabolomics*
  • Oxylipins* / metabolism
  • Signal Transduction*
  • Spodoptera* / physiology

Substances

  • Oxylipins
  • Cyclopentanes
  • jasmonic acid
  • Arabidopsis Proteins
  • MYC2 protein, Arabidopsis
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Glucosinolates