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

Abstract

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.

Valproic Acid Improves Porcine Parthenogenetic Embryo Development Through Transient Remodeling of Histone Modifiers

“…In fact, one study on human breast cancer cells has suggested that inhibiting HDAC I/II results in significant increases of H3K4me2 [18]. H3K4me2 is considered an active chromatin marker [19]. The signal intensity of H3K4me2 increased with VPA treatment, and this may beneficially activate development-related genes thus contributing to the enhancement of developmental competence.…”

A fungal Argonaute interferes with RNA interference

“…In our previous RNA-seq analysis of the Br48 strain (23), we found two contigs highly homologous to mycoviral RNA-dependent RNA polymerase. Since their amino acid sequences were most closely related to the ourmiavirus-like virus recently reported in Botrytis cinerea (24), we tentatively designated them as P. oryzae ourmiavirus-like virus 1 and 2 (PoOLV1 and PoOLV2).…”

“…Unlike common rice-infecting P. oryzae strains that lack the sexual phase, Br48 is highly fertile and possesses RIP as a currently active process (51). In our previous RNA-seq analysis, very few TEs were transcriptionally active (23). This was also indicated in this study, as the portion of TE-derived sRNAs was extremely low compared to that previously reported in rice-infecting P. oryzae strains (Table 1; (28,52)).…”

Chromatin Biology Impacts Adaptive Evolution of Filamentous Plant Pathogens

“…The majority of chromatin studies using plant-pathogenic fungi have focused on their transcriptional impacts (Fig 2B) [17–19]. Canonical repressive chromatin marks, such as H3K9me2/3 or H3K27me2/3, are significantly enriched at regions known to harbor genes important for pathogenicity [17,18].…”

“…Canonical repressive chromatin marks, such as H3K9me2/3 or H3K27me2/3, are significantly enriched at regions known to harbor genes important for pathogenicity [17,18]. Additionally, the canonical activating mark H3K4me2/3 was shown to play a significant role in regulating gene expression and promoting growth and virulence in Magnaporthe oryza e [19]. Collectively, these studies indicate that deregulating chromatin significantly impacts fungal transcription, growth, and development.…”