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

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Abstract

Summary

The cereal pathogenFusarium graminearumthreatens 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 inF. graminearumis 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.

GABA accumulates in infected wheat heads upon infection with Fusarium graminearum. Disruption of the fungal GABA shunt prevents infection, compromises mitochondrial respiration but does not affect deoxynivalenol biosynthesis in planta. In culture, mutants deficient in both GABA transaminases accumulate GABA intracellularly resulting in defective energy production and, therefore, impaired growth. The fungal GABA shunt is partially subject to nitrogen metabolite repression mediated by AreA.

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