Journal
VIRULENCE
Volume 12, Issue 1, Pages 1306-1322Publisher
TAYLOR & FRANCIS INC
DOI: 10.1080/21505594.2021.1923232
Keywords
Entomopathogenic fungi; histone h3k9-specific methyltransferase; multisite h3 methylation; gene regulation; pathgogenicity and virulence; stress response; asexual cycle
Categories
Funding
- National Natural Science Foundation of China [31772218, 31801795]
- Ministry of Science and Technology of the People's Republic of China [2017YFD0201202]
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The H3K9-specific DIM5/KMT1 orthologue has vital roles in methylating core lysines of H3 in Beauveria bassiana, leading to loss of insect pathogenicity and compromised virulence. Dysregulation of genes related to transcription factors and posttranslational modifications suggests DIM5-methylated H3 core lysines act as marks for transcription-active genes crucial for global gene regulation in B. bassiana.
Mono-, di- and tri-methylation of histone H3 Lys 9, Lys 4, and Lys 36 (H3K_me1/me2/me3) required for mediation of DNA-based cellular events in eukaryotes usually rely upon the activities of histone lysine methyltransferases (KMTs) classified to the KMT1, KMT2, and KMT3 families, respectively. Here, an H3K9-specific DIM5/KMT1 orthologue, which lacks a C-terminal post-SET domain and localizes mainly in nucleus, is reported to have both conserved and noncanonical roles in methylating the H3 core lysines in Beauveria bassiana, an insect-pathogenic fungus serving as a main source of wide-spectrum fungal insecticides. Disruption of dim5 led to abolishment of H3K9me3 and marked attenuation of H3K4me1/me2, H3K9me1/me2 and H3K36me2. Consequently, the Delta dim5 mutant lost the whole insect pathogenicity through normal cuticle infection, and was compromised severely in virulence through cuticle-bypassing infection (hemocoel injection) and also in a series of cellular events critical for the fungal virulence and lifecycle in vivo and in vitro, including reduced hyphal growth, blocked conidiation, impeded proliferation in vivo, altered carbohydrate epitopes, disturbed cell cycle, reduced biosynthesis and secretion of cuticle-degrading enzymes, and increased sensitivities to various stresses. Among 1,201 dysregulated genes (up/down ratio: 712:489) associated with those phenotypic changes, 92 (up/down ratio: 59:33) encode transcription factors and proteins or enzymes involved in posttranslational modifications, implying that the DIM5-methylated H3 core lysines could act as preferential marks of those transcription-active genes crucial for global gene regulation. These findings uncover a novel scenario of DIM5 and its indispensability for insect-pathogenic lifestyle and genome stability of B. bassiana.
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