Disruption of the GABA shunt affects mitochondrial respiration and virulence in the cereal pathogen Fusarium graminearum

Mol Microbiol. 2015 Dec;98(6):1115-32. doi: 10.1111/mmi.13203. Epub 2015 Oct 16.

Abstract

The cereal pathogen Fusarium graminearum threatens food and feed production worldwide. It reduces the yield and poisons the remaining kernels with mycotoxins, notably deoxynivalenol (DON). We analyzed the importance of gamma-aminobutanoic acid (GABA) metabolism for the life cycle of this fungal pathogen. GABA metabolism in F. graminearum is partially regulated by the global nitrogen regulator AreA. Genetic disruption of the GABA shunt by deletion of two GABA transaminases renders the pathogen unable to utilize the plant stress metabolites GABA and putrescine. The mutants showed increased sensitivity against oxidative stress, GABA accumulation in the mycelium, downregulation of two key enzymes of the TCA cycle, disturbed potential gradient in the mitochondrial membrane and lower mitochondrial oxygen consumption. In contrast, addition of GABA to the wild type resulted in its rapid turnover and increased mitochondrial steady state oxygen consumption. GABA concentrations are highly upregulated in infected wheat tissues. We conclude that GABA is metabolized by the pathogen during infection increasing its energy production, whereas the mutants accumulate GABA intracellularly resulting in decreased energy production. Consequently, the GABA mutants are strongly reduced in virulence but, because of their DON production, are able to cross the rachis node.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Aminobutyrate Transaminase / genetics
  • 4-Aminobutyrate Transaminase / metabolism
  • Energy Metabolism
  • Fusarium / drug effects
  • Fusarium / genetics*
  • Fusarium / metabolism*
  • Fusarium / pathogenicity
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mutation
  • Mycelium / chemistry
  • Mycotoxins / biosynthesis
  • Oxidative Stress
  • Oxygen Consumption
  • Putrescine / metabolism
  • Trichothecenes / biosynthesis
  • Trichothecenes / metabolism
  • Triticum / microbiology*
  • Virulence / genetics
  • gamma-Aminobutyric Acid / metabolism*
  • gamma-Aminobutyric Acid / pharmacology

Substances

  • Mycotoxins
  • Trichothecenes
  • gamma-Aminobutyric Acid
  • 4-Aminobutyrate Transaminase
  • deoxynivalenol
  • Putrescine