Histone H3 N-Terminal Lysine Acetylation Governs Fungal Growth, Conidiation, and Pathogenicity through Regulating Gene Expression in Fusarium pseudograminearum

The acetylation of histone lysine residues regulates multiple life processes, including growth, conidiation, and pathogenicity in filamentous pathogenic fungi. However, the specific function of each lysine residue at the N-terminus of histone H3 in phytopathogenic fungi remains unclear. In this study, we mutated the N-terminal lysine residues of histone H3 in Fusarium pseudograminearum, the main causal agent of Fusarium crown rot of wheat in China, which also produces deoxynivalenol (DON) toxins harmful to humans and animals. Our findings reveal that all the FpH3^K9R, FpH3^K14R, FpH3^K18R, and FpH3^K23R mutants are vital for vegetative growth and conidiation. Additionally, FpH3K14 regulates the pathogen’s sensitivity to various stresses and fungicides. Despite the slowed growth of the FpH3^K9R and FpH3^K23R mutants, their pathogenicity towards wheat stems and heads remains unchanged. However, the FpH3^K9R mutant produces more DON. Furthermore, the FpH3^K14R and FpH3^K18R mutants exhibit significantly reduced virulence, with the FpH3^K18R mutant producing minimal DON. In the FpH3^K9R, FpH3^K14R, FpH3^K18R, and FpH3^K23R mutants, there are 1863, 1400, 1688, and 1806 downregulated genes, respectively, compared to the wild type. These downregulated genes include many that are crucial for growth, conidiation, pathogenicity, and DON production, as well as some essential genes. Gene ontology (GO) enrichment analysis indicates that genes downregulated in the FpH3^K14R and FpH3^K18R mutants are enriched for ribosome biogenesis, rRNA processing, and rRNA metabolic process. This suggests that the translation machinery is abnormal in the FpH3^K14R and FpH3^K18R mutants. Overall, our findings suggest that H3 N-terminal lysine residues are involved in regulating the expression of genes with important functions and are critical for fungal development and pathogenicity.