Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea

David A Parker, Manfred Beckmann, Hassan Zubair, David Pierre Louis Enot, Zaira Caracuel-Rios, David Patrick Overy, Stuart Snowdon, Nicholas J. Talbot, John Draper

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Abstract

The mechanisms by which biotrophic and hemi-biotrophic fungal pathogens simultaneously subdue plant defences and sequester host nutrients are poorly understood. Using metabolite fingerprinting, we show that Magnaporthe grisea, the causal agent of rice blast disease, dynamically re-programmes host metabolism during plant colonization. Identical patterns of metabolic change occurred during M. grisea infections in barley, rice and Brachypodium distachyon. Targeted metabolite profiling by GC-MS confirmed the modulation of a conserved set of metabolites. In pre-symptomatic tissues, malate and polyamines accumulated, rather than being utilized to generate defensive reactive oxygen species, and the levels of metabolites associated with amelioration of redox stress in various cellular compartments increased dramatically. The activity of NADP-malic enzyme and generation of reactive oxygen species were localized to pathogen penetration sites, and both appeared to be suppressed in compatible interactions. Early diversion of the shikimate pathway to produce quinate was observed, as well as accumulation of non-polymerized lignin precursors. These data are consistent with modulation of defensive phenylpropanoid metabolism by M. grisea and the inability of susceptible hosts to mount a hypersensitive reaction or produce lignified papillae (both involving reactive oxygen species) to restrict pathogen invasion. Rapid proliferation of M. grisea hyphae in plant tissue after 3 days was associated with accelerated nutrient acquisition and utilization by the pathogen. Conversion of photoassimilate into mannitol and glycerol for carbon sequestration and osmolyte production appear to drive hyphal growth. Taken together, our results suggest that fungal pathogens deploy a common metabolic re-programming strategy in diverse host species to suppress plant defence and colonize plant tissue.
Original languageEnglish
Pages (from-to)723-737
Number of pages15
JournalPlant Journal
Volume59
Issue number5
DOIs
Publication statusPublished - 25 Aug 2009

Keywords

  • metabolome re-programming
  • host susceptible response
  • Magnaporthe grisea
  • Brachypodium distachyon
  • rice
  • barley
  • Host susceptible response
  • Barley
  • Metabolome re-programming
  • Rice
  • Reactive Oxygen Species/metabolism
  • Metabolomics
  • Gas Chromatography-Mass Spectrometry
  • Oryza/genetics
  • Host-Pathogen Interactions
  • Magnaporthe
  • Hordeum/genetics
  • Metabolic Networks and Pathways
  • Gene Expression Regulation, Plant
  • Plant Diseases/genetics

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