Glutathione Transferase U13 Functions in Pathogen-Triggered Glucosinolate Metabolism

Plant Physiol. 2018 Jan;176(1):538-551. doi: 10.1104/pp.17.01455. Epub 2017 Nov 9.

Abstract

Glutathione (GSH) and indole glucosinolates (IGs) exert key functions in the immune system of the model plant Arabidopsis (Arabidopsis thaliana). Appropriate GSH levels are important for execution of both pre- and postinvasive disease resistance mechanisms to invasive pathogens, whereas an intact PENETRATION2 (PEN2)-pathway for IG metabolism is essential for preinvasive resistance in this species. Earlier indirect evidence suggested that the latter pathway involves conjugation of GSH with unstable products of IG metabolism and further processing of the resulting adducts to biologically active molecules. Here we describe the identification of Glutathione-S-Transferase class-tau member 13 (GSTU13) as an indispensable component of the PEN2 immune pathway for IG metabolism. gstu13 mutant plants are defective in the pathogen-triggered biosynthesis of end products of the PEN2 pathway, including 4-O-β-d-glucosyl-indol-3-yl formamide, indole-3-ylmethyl amine, and raphanusamic acid. In line with this metabolic defect, lack of functional GSTU13 results in enhanced disease susceptibility toward several fungal pathogens including Erysiphe pisi, Colletotrichum gloeosporioides, and Plectosphaerella cucumerina Seedlings of gstu13 plants fail also to deposit the (1,3)-β-glucan cell wall polymer, callose, after recognition of the bacterial flg22 epitope. We show that GSTU13 mediates specifically the role of GSH in IG metabolism without noticeable impact on other immune functions of this tripeptide. We postulate that GSTU13 connects GSH with the pathogen-triggered PEN2 pathway for IG metabolism to deliver metabolites that may have numerous functions in the innate immune system of Arabidopsis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / enzymology*
  • Arabidopsis / immunology
  • Arabidopsis / microbiology*
  • Arabidopsis Proteins / metabolism*
  • Biosynthetic Pathways / genetics
  • Disease Resistance
  • Flagellin / pharmacology
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Glucosinolates / chemistry
  • Glucosinolates / metabolism*
  • Glutathione / metabolism
  • Glutathione Transferase / metabolism*
  • Indoles / chemistry
  • Indoles / metabolism
  • Phenotype
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Seedlings / metabolism

Substances

  • Arabidopsis Proteins
  • Glucosinolates
  • Indoles
  • Flagellin
  • indole
  • GSTU13 protein, Arabidopsis
  • Glutathione Transferase
  • Glutathione