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Histone H3 N-Terminal Lysine Acetylation Governs Fungal Growth, Conidiation, and Pathogenicity through Regulating
Hang Jiang1, Lifang Yuan2, Liguo Ma1
1Shandong Key Laboratory of Plant Virology, Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan 250100, China.
Abstract:
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 FpH3K9R, FpH3K14R, FpH3K18R, and FpH3K23R 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 FpH3K9R and FpH3K23R mutants, their pathogenicity towards wheat stems and heads remains unchanged. However, the FpH3K9R mutant produces more DON. Furthermore, the FpH3K14R and FpH3K18R mutants exhibit significantly reduced virulence, with the FpH3K18R mutant producing minimal DON. In the FpH3K9R, FpH3K14R, FpH3K18R, and FpH3K23R 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 FpH3K14R and FpH3K18R mutants are enriched for ribosome biogenesis, rRNA processing, and rRNA metabolic process. This suggests that the translation machinery is abnormal in the FpH3K14R and FpH3K18R 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.
Insights
Histone H3 lysine mutations in Fusarium pseudograminearum impact fungal growth, development, and pathogenicity. These mutations affect gene expression, crucial for fungal life processes and deoxynivalenol (DON) toxin production.
Area of Science:
- Molecular Biology
- Mycology
- Plant Pathology
- Epigenetics
Background:
- Histone acetylation regulates gene expression in fungi.
- The specific roles of N-terminal histone H3 lysine residues in phytopathogenic fungi are not well understood.
- Fusarium pseudograminearum causes Fusarium crown rot in wheat and produces harmful deoxynivalenol (DON) toxins.
Purpose of the Study:
- To investigate the function of N-terminal lysine residues of histone H3 in Fusarium pseudograminearum.
- To determine the impact of these mutations on fungal growth, conidiation, pathogenicity, and DON production.
Main Methods:
- Site-directed mutagenesis of N-terminal lysine residues (K9, K14, K18, K23) in histone H3.
- Phenotypic analysis of mutant strains for growth, conidiation, and stress/fungicide sensitivity.
- Pathogenicity assays on wheat.
- Deoxynivalenol (DON) production quantification.
- Transcriptome analysis (RNA sequencing) and Gene Ontology (GO) enrichment analysis.
Main Results:
- All FpH3 lysine mutants (K9R, K14R, K18R, K23R) were essential for vegetative growth and conidiation.
- FpH3K14R mutants showed altered sensitivity to stresses and fungicides.
- FpH3K9R and FpH3K23R mutants had slowed growth but retained pathogenicity; FpH3K9R produced more DON.
- FpH3K14R and FpH3K18R mutants exhibited reduced virulence, with FpH3K18R producing minimal DON.
- Mutations led to significant downregulation of genes involved in growth, conidiation, pathogenicity, and DON production.
- GO analysis revealed enrichment of ribosome biogenesis and rRNA processing in FpH3K14R and FpH3K18R mutants, suggesting translation machinery defects.
Conclusions:
- N-terminal lysine residues of histone H3 are critical for regulating gene expression in Fusarium pseudograminearum.
- These residues play vital roles in fungal development, stress response, and pathogenicity.
- Histone H3 lysine modifications are essential for maintaining translation machinery function and virulence in this important plant pathogen.
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