Conservation and clade-specific diversification of pathogen-inducible tryptophan and indole glucosinolate metabolism in Arabidopsis thaliana relatives

New Phytol. 2011 Nov;192(3):713-26. doi: 10.1111/j.1469-8137.2011.03824.x. Epub 2011 Jul 21.

Abstract

• A hallmark of the innate immune system of plants is the biosynthesis of low-molecular-weight compounds referred to as secondary metabolites. Tryptophan-derived branch pathways contribute to the capacity for chemical defense against microbes in Arabidopsis thaliana. • Here, we investigated phylogenetic patterns of this metabolic pathway in relatives of A. thaliana following inoculation with filamentous fungal pathogens that employ contrasting infection strategies. • The study revealed unexpected phylogenetic conservation of the pathogen-induced indole glucosinolate (IG) metabolic pathway, including a metabolic shift of IG biosynthesis to 4-methoxyindol-3-ylmethylglucosinolate and IG metabolization. By contrast, indole-3-carboxylic acid and camalexin biosyntheses are clade-specific innovations within this metabolic framework. A Capsella rubella accession was found to be devoid of any IG metabolites and to lack orthologs of two A. thaliana genes needed for 4-methoxyindol-3-ylmethylglucosinolate biosynthesis or hydrolysis. However, C. rubella was found to retain the capacity to deposit callose after treatment with the bacterial flagellin-derived epitope flg22 and pre-invasive resistance against a nonadapted powdery mildew fungus. • We conclude that pathogen-inducible IG metabolism in the Brassicaceae is evolutionarily ancient, while other tryptophan-derived branch pathways represent relatively recent manifestations of a plant-pathogen arms race. Moreover, at least one Brassicaceae lineage appears to have evolved IG-independent defense signaling and/or output pathway(s).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Absorption / radiation effects
  • Amino Acid Sequence
  • Arabidopsis / immunology
  • Arabidopsis / metabolism*
  • Arabidopsis / microbiology
  • Arabidopsis / radiation effects
  • Ascomycota / physiology
  • Ascomycota / radiation effects
  • Botrytis / physiology
  • Botrytis / radiation effects
  • Brassicaceae / immunology
  • Brassicaceae / metabolism*
  • Brassicaceae / microbiology*
  • Genetic Variation*
  • Glucosinolates / chemistry
  • Glucosinolates / metabolism*
  • Immunity, Innate / radiation effects
  • Indoles / chemistry
  • Indoles / metabolism*
  • Molecular Sequence Data
  • Phylogeny*
  • Plant Diseases / microbiology
  • Plant Proteins / chemistry
  • Sequence Homology, Amino Acid
  • Species Specificity
  • Thiazoles / metabolism
  • Tryptophan / chemistry
  • Tryptophan / metabolism*
  • Ultraviolet Rays

Substances

  • Glucosinolates
  • Indoles
  • Plant Proteins
  • Thiazoles
  • camalexin
  • 4-methoxy-3-indolylmethyl glucosinolate
  • Tryptophan