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Fungal sexual reproduction requires complex cellular differentiation processes of hyphal cells. The plant pathogenic fungus Fusarium graminearum produces 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. graminearum perithecium overproducing 1 (Fpo1), plays a role as a global transcriptional repressor during perithecium production and maturation in F. graminearum. Deletion of FPO1 resulted in reduced vegetative growth, asexual sporulation and virulence and overproduced perithecium, which reached maturity earlier, compared with the wild type. Intriguingly, the hyphae of the fpo1 mutant accumulated excess lipids during perithecium production. Using a combination of molecular biological, transcriptomic and biochemical approaches, we demonstrate that repression of FPO1 after 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-overproducing F. graminearum mutant, and the findings provide comprehensive insight into the role of modulation of carbon metabolism in the sexual reproduction of fungi.

Fusarium graminearum is a prominent plant pathogenic fungus causing Fusarium head blight in major cereal crops worldwide. To understand the molecular mechanisms underlying fungal development and virulence, large collections of F. graminearum mutants have been constructed. Cytochrome P450 monooxygenases (P450s) are widely distributed in organisms and are involved in a diverse array of molecular/metabolic processes; however, no systematic functional analysis of P450s has been attempted in filamentous fungi. In this study, we constructed a genome-wide deletion mutant set covering 102 P450s and analyzed these mutants for changes in 38 phenotypic categories, including fungal development, stress responses and responses to several xenobiotics, to build a comprehensive phenotypic dataset. Most P450 mutants showing defective phenotypes were impaired in a single phenotypic trait, demonstrating that our mutant library is a good genetic resource for further fungal genetic studies. In particular, we identified novel P450s specifically involved in virulence (5) and both asexual (1) and sexual development (2). Most P450s seem to play redundant roles in the degradation of xenobiotics in F. graminearum. This study is the first phenome-based functional analysis of P450s, and it provides a valuable genetic resource for further basic and applied biological research in filamentous fungi and other plant pathogens.

Sodium is an abundant cation required for protein function and maintenance of cellular osmotic homeostasis. High concentrations of sodium are toxic, and fungi have evolved efficient sodium efflux systems. In this study, we characterized a novel sodium tolerance mechanism in the plant pathogen Fusarium graminearum. Fusarium graminearum sodium sensitive 1 (Fss1) is a nuclear transcription factor with a Zn(II)2 Cys6 fungal-type DNA-binding domain required for sodium tolerance. RNA-seq and genetic studies revealed that a P-type ATPase pump, exitus natru (Latin: exit sodium) 1 (FgEna5), mediates the phenotypic defects of FSS1 mutants. A homologue of PACC (PAC1) was required for FgEna5-dependent sodium and lithium tolerance independent of Fss1. The results of this study revealed that F. graminearum has a distinct and novel pathway for sodium tolerance not present in other model fungi.

Fusarium graminearum is a prominent plant pathogenic fungus causing Fusarium head blight in major cereal crops worldwide. To understand the molecular mechanisms underlying fungal development and virulence, large collections of F. graminearum mutants have been constructed. Cytochrome P450 monooxygenases (P450s) are widely distributed in organisms and are involved in a diverse array of molecular/metabolic processes; however, no systematic functional analysis of P450s has been attempted in filamentous fungi. In this study, we constructed a genome-wide deletion mutant set covering 102 P450s and analyzed these mutants for changes in 38 phenotypic categories, including fungal development, stress responses and responses to several xenobiotics, to build a comprehensive phenotypic dataset. Most P450 mutants showing defective phenotypes were impaired in a single phenotypic trait, demonstrating that our mutant library is a good genetic resource for further fungal genetic studies. In particular, we identified novel P450s specifically involved in virulence (5) and both asexual (1) and sexual development (2). Most P450s seem to play redundant roles in the degradation of xenobiotics in F. graminearum. This study is the first phenome-based functional analysis of P450s, and it provides a valuable genetic resource for further basic and applied biological research in filamentous fungi and other plant pathogens.

Sodium is an abundant cation required for protein function and maintenance of cellular osmotic homeostasis. High concentrations of sodium are toxic, and fungi have evolved efficient sodium efflux systems. In this study, we characterized a novel sodium tolerance mechanism in the plant pathogen Fusarium graminearum. Fusarium graminearum sodium sensitive 1 (Fss1) is a nuclear transcription factor with a Zn(II)2 Cys6 fungal-type DNA-binding domain required for sodium tolerance. RNA-seq and genetic studies revealed that a P-type ATPase pump, exitus natru (Latin: exit sodium) 1 (FgEna5), mediates the phenotypic defects of FSS1 mutants. A homologue of PACC (PAC1) was required for FgEna5-dependent sodium and lithium tolerance independent of Fss1. The results of this study revealed that F. graminearum has a distinct and novel pathway for sodium tolerance not present in other model fungi.