Substrate-Induced Transcriptional Activation of the MoCel7C Cellulase Gene Is Associated with Methylation of Histone H3 at Lysine 4 in the Rice Blast Fungus Magnaporthe oryzae

Abstract

The mechanisms involved in substrate-dependent regulation of a Magnaporthe oryzae gene encoding a cellulase which we designate MoCel7C (MGG_14954) were investigated. The levels of MoCel7C transcript were dramatically increased more than 1,000-fold, 16 to 24 h after transfer to a medium containing 2% carboxymethylcellulose (CMC), while levels were very low or undetectable in conventional rich medium. Green fluorescent protein reporter assays showed that the MoCel7C promoter was activated by cello-oligosaccharides larger than a pentamer. CMC-induced activation of the MoCel7C promoter was suppressed by glucose and cellobiose. Chromatin immunoprecipitation assays revealed that histone H3 methylation on lysine 4 (H3K4) at the MoCel7C locus was associated with activation of the gene by CMC. Consistently, CMC-induced MoCel7C gene activation was drastically diminished in a knockout (KO) mutant of the MoSET1 gene, which encodes a histone lysine methyltransferase that catalyzes H3K4 methylation in M. oryzae. Interestingly, however, MoCel7C transcript levels under noninducing conditions were significantly increased in the MoSET1 KO mutant, suggesting that MoSET1 directly or indirectly plays a role in both activation and suppression of the MoCel7C gene in response to environmental signals. In addition, gene expression and silencing vectors using the MoCel7C promoter were constructed.

MoJMJ1, Encoding a Histone Demethylase Containing JmjC Domain, Is Required for Pathogenic Development of the Rice Blast Fungus, Magnaporthe oryzae

“…For instance, CclA, a member of COMPASS complex involved in H3K4 methylation, and LaeA, affecting methylation level at H3K9, regulate SM gene clusters (Bok et al, 2009; Strauss and Reyes-Dominguez, 2011). Recently, in M. oryzae , it was shown that MoSET1, catalyzing dimethyl H3K4, is associated with substrate-induced transcriptional activation of a cellulose gene (Vu et al, 2013). Although role of histone modification in various biological processes of filamentous fungus is well studied, the functional aspects of fungal HDMs are yet to be explored.…”

Epigenetic regulation of development and pathogenesis in fungal plant pathogens

“…This is in accordance with the finding of Vu et al . () where, again, MoSET1 was involved in gene suppression under non‐inducing conditions. The switch in the activity of histone methylation from activation to repression under different environmental conditions supports the link between external factors and the dynamics of histone methylation.…”

“…In M. oryzae , histone methylation has been associated with gene activation as well as repression. A study reported the substrate‐induced activation of a cellulase gene, mediated through histone methylation, in M. oryzae (Vu et al ., ). The cellulase gene MoCel7C is up‐regulated on contact with the host leaf surface, demonstrating the recognition ability of the pathogen on contact with the host surface.…”

Epigenetics as an emerging tool for improvement of fungal strains used in biotechnology

“…However, its action within the Velvet complex is supported by the findings that the Trichoderma reesei VeA ortholog VEL1 is also essential for cellulase gene expression ). An involvement of H3K4 methylation in cellulose formation was however demonstrated in Magnaporthe oryzae, where a knockout of the MoSET1 gene, encoding the methyltransferase that catalyzes H3K4 methylation (MoSET1), strongly reduced the induction of the cellulase MoCel7C by carboxymethyl cellulose ( Van Vu et al 2013). Evidence that chromatin modification is necessary for cellulase gene expression was further obtained by analyzing the nucleosome rearrangement in the promoters of the genes encoding the two major cellulases CEL6A and CEL7A of Trichoderma reesei (Zeilinger et al 2003;Ries et al 2013): under cellulase-inducing conditions, the positioning of nucleosomes downstream of the motif binding the transcriptional activator was lost and thus made the TATA box accessible for the RNA polymerase II.…”