The novel bZIP transcription factor Fpo1 negatively regulates perithecial development by modulating carbon metabolism in the ascomycete fungusFusarium graminearum

Fungal sexual reproduction requires complex cellular differentiation processes of hyphal cells. The plant pathogenic fungusFusarium graminearumproduces fruiting bodies called perithecia via sexual reproduction, and perithecia forcibly discharge ascospores into the air for disease initiation and propagation. Lipid metabolism and accumulation are closely related to perithecium formation, yet the molecular mechanisms that regulate these processes are largely unknown. Here, we report that a novel fungal specific bZIP transcription factor,F.graminearumperithecium overproducing 1 (Fpo1), plays a role as a global transcriptional repressor during perithecium production and maturation inF.graminearum. Deletion ofFPO1resulted in reduced vegetative growth, asexual sporulation and virulence and overproduced perithecium, which reached maturity earlier, compared with the wild type. Intriguingly, the hyphae of thefpo1mutant accumulated excess lipids during perithecium production. Using a combination of molecular biological, transcriptomic and biochemical approaches, we demonstrate that repression ofFPO1after sexual induction leads to reprogramming of carbon metabolism, particularly fatty acid production, which affects sexual reproduction of this fungus. This is the first report of a perithecium-overproducingF.graminearummutant, and the findings provide comprehensive insight into the role of modulation of carbon metabolism in the sexual reproduction of fungi.