MoSET1 (Histone H3K4 Methyltransferase in Magnaporthe oryzae) Regulates Global Gene Expression during Infection-Related Morphogenesis

Autor: Yoshihiro Inoue, Ba Van Vu, Hanh Hieu Nguyen, Kieu Thi Minh Pham, Toru Nakayashiki, Kenichi Ikeda, Hitoshi Nakayashiki
Rok vydání: 2014
Předmět:
Zdroj: PLoS Genetics
PLoS Genetics, Vol 11, Iss 7, p e1005385 (2015)
ISSN: 1553-7404
Popis: Here we report the genetic analyses of histone lysine methyltransferase (KMT) genes in the phytopathogenic fungus Magnaporthe oryzae. Eight putative M. oryzae KMT genes were targeted for gene disruption by homologous recombination. Phenotypic assays revealed that the eight KMTs were involved in various infection processes at varying degrees. Moset1 disruptants (Δmoset1) impaired in histone H3 lysine 4 methylation (H3K4me) showed the most severe defects in infection-related morphogenesis, including conidiation and appressorium formation. Consequently, Δmoset1 lost pathogenicity on wheat host plants, thus indicating that H3K4me is an important epigenetic mark for infection-related gene expression in M. oryzae. Interestingly, appressorium formation was greatly restored in the Δmoset1 mutants by exogenous addition of cAMP or of the cutin monomer, 16-hydroxypalmitic acid. The Δmoset1 mutants were still infectious on the super-susceptible barley cultivar Nigrate. These results suggested that MoSET1 plays roles in various aspects of infection, including signal perception and overcoming host-specific resistance. However, since Δmoset1 was also impaired in vegetative growth, the impact of MoSET1 on gene regulation was not infection specific. ChIP-seq analysis of H3K4 di- and tri-methylation (H3K4me2/me3) and MoSET1 protein during infection-related morphogenesis, together with RNA-seq analysis of the Δmoset1 mutant, led to the following conclusions: 1) Approximately 5% of M. oryzae genes showed significant changes in H3K4-me2 or -me3 abundance during infection-related morphogenesis. 2) In general, H3K4-me2 and -me3 abundance was positively associated with active transcription. 3) Lack of MoSET1 methyltransferase, however, resulted in up-regulation of a significant portion of the M. oryzae genes in the vegetative mycelia (1,491 genes), and during infection-related morphogenesis (1,385 genes), indicating that MoSET1 has a role in gene repression either directly or more likely indirectly. 4) Among the 4,077 differentially expressed genes (DEGs) between mycelia and germination tubes, 1,201 and 882 genes were up- and down-regulated, respectively, in a Moset1-dependent manner. 5) The Moset1-dependent DEGs were enriched in several gene categories such as signal transduction, transport, RNA processing, and translation.
Author Summary This paper provides two major contributions to the field of genetics. First, we systematically studied the biological roles of eight histone lysine methyltransferase (KMT) genes in the phytopathogenic fungus Magnaporthe oryzae. We investigated their roles, especially focusing on their involvement in infection-related morphogenesis and pathogenicity. The results showed that the eight KMTs were involved in various infection processes to varying degrees, and that MoSET1, one of the KMTs catalyzing methylation at histone H3 lysine 4 (H3K4), had the largest impact on the pathogenicity of the fungus. Second, we focused on the role of MoSET1 in global gene regulation. H3K4 methylation is generally believed to be an epigenetic mark for gene activation in higher eukaryotes. However, in Saccharomyces cerevisiae, SET1 was originally characterized as being required for transcriptional silencing of silent mating-type loci. We addressed this apparent discrepancy by examining genome-wide gene expression and H3K4 methylation during infection-related morphogenesis in M. oryzae. RNA-seq analysis of a MoSET1 deletion mutant revealed that MoSET1 was indeed required for proper gene activation and repression. ChIP-seq analyses of H3K4 methylation and MoSET1 suggested that MoSET1 could directly play a role in gene activation while MoSET1-dependent gene repression may be caused by indirect effects.
Databáze: OpenAIRE
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