Multi-omics analyses of sid2 mutant reflect the need of isochorismate synthase ICS1 to cope with sulfur limitation in Arabidopsis thaliana

Plant J. 2024 Jun;118(5):1635-1651. doi: 10.1111/tpj.16702. Epub 2024 Mar 18.

Abstract

The SID2 (SA INDUCTION-DEFICIENT2) gene that encodes ICS1 (isochorismate synthase), plays a central role in salicylic acid biosynthesis in Arabidopsis. The sid2 and NahG (encoding a bacterial SA hydroxylase) overexpressing mutants (NahG-OE) have currently been shown to outperform wild type, presenting delayed leaf senescence, higher plant biomass and better seed yield. When grown under sulfate-limited conditions (low-S), sid2 mutants exhibited early leaf yellowing compared to the NahG-OE, the npr1 mutant affected in SA signaling pathway, and WT. This indicated that the hypersensitivity of sid2 to sulfate limitation was independent of the canonical npr1 SA-signaling pathway. Transcriptomic and proteomic analyses revealed that major changes occurred in sid2 when cultivated under low-S, changes that were in good accordance with early senescence phenotype and showed the exacerbation of stress responses. The sid2 mutants displayed a lower sulfate uptake capacity when cultivated under low-S and lower S concentrations in their rosettes. Higher glutathione concentrations in sid2 rosettes under low-S were in good accordance with the higher abundance of proteins involved in glutathione and ascorbate redox metabolism. Amino acid and lipid metabolisms were also strongly modified in sid2 under low-S. Depletion of total fatty acids in sid2 under low-S was consistent with the fact that S-metabolism plays a central role in lipid synthesis. Altogether, our results show that functional ICS1 is important for plants to cope with S limiting conditions.

Keywords: leaf senescence; salicylic acid; stress response; sulfate metabolism.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Arabidopsis* / physiology
  • Gene Expression Regulation, Plant
  • Intramolecular Transferases* / genetics
  • Intramolecular Transferases* / metabolism
  • Multiomics
  • Mutation
  • Plant Leaves / genetics
  • Plant Leaves / metabolism
  • Proteomics
  • Salicylic Acid / metabolism
  • Sulfur* / metabolism
  • Transcriptome

Substances

  • Arabidopsis Proteins
  • Intramolecular Transferases
  • Sulfur
  • isochorismate synthase
  • Salicylic Acid