FgJhd2 Modulates FgMpf2 Expression via H3K4 Demethylation and Influences Sexual Development in Fusarium graminearum

Histone methylation plays a pivotal role in the epigenetic regulation of fungal development. In this study, we characterise FgJhd2, a homologue of the histone demethylase Jhd2 from the JARID family, in the plant pathogenic fungus Fusarium graminearum. FgJhd2 localises in the nucleus and exhibits specific H3K4me3 demethylase activity. Deletion of FgJHD2 impaired hyphal growth and sexual reproduction, leading to smaller perithecia, defective asci and ascospore development. Transcriptomic analysis revealed significant down-regulation of key developmental genes, including FgAMA1, AMD1 and PUK1, in the Fgjhd2 mutant. Combined ChIP-seq and RNA-seq analyses revealed that loss of FgJHD2 leads to increased H3K4 methylation and elevated expression of FgMPF2, suggesting a potential negative regulatory relationship. FgMpf2, homologous to the Schizosaccharomyces pombe RNA-binding protein Mpf2, contains a Pumilio domain essential for RNA degradation. Phenotypic analyses revealed that FgMPF2 deletion abolishes ascus formation, while its overexpression disrupts ascus maturation, resembling the defects observed in the Fgjhd2 mutant. Intriguingly, overexpression of FgMPF2 led to reduced FgAMA1, AMD1 and PUK1 transcript levels. Our study supports a model in which FgJhd2 modulates sexual reproduction by regulating FgMPF2 expression, which in turn influences the transcript stability of key developmental genes in F. graminearum.