Normal transcription of cellulolytic enzyme genes relies on the balance between the methylation of H3K36 and H3K4 in Penicillium oxalicum

BACKGROUND: Enzymatic hydrolysis of lignocellulose by fungi is a key step in global carbon cycle and biomass utilization. Cellulolytic enzyme production is tightly controlled at a transcriptional level. Here, we investigated the roles of different histone lysine methylation modifications in regulating cellulolytic enzyme gene expression, as histone lysine methylation is an important process of chromatin regulation associated with gene transcription. RESULTS: PoSet1 and PoSet2 in Penicillium oxalicum, orthologs of Set1 and Set2 in budding yeast, were associated with the methylation of histone H3 lysine 4 (H3K4) and lysine 36 (H3K36). Cellulolytic enzyme production was extensively upregulated by the disruption of PoSet2, but was significantly downregulated by the disruption of PoSet1. We revealed that the activation of cellulolytic enzyme genes was accompanied by the increase of H3K4me3 signal, as well as the decrease of H3K36me1 and H3K36me3 signal on specific gene loci. The repression of cellulolytic enzyme genes was accompanied by the absence of global H3K4me1 and H3K4me2. An increase in the H3K4me3 signal by Poset2 disruption was eliminated by the further disruption of Poset1 and accompanied by the repressed cellulolytic enzyme genes. The active or repressed genes were not always associated with transcription factors. CONCLUSION: H3K4 methylation is an active marker of cellulolytic enzyme production, whereas H3K36 methylation is a marker of repression. A crosstalk occurs between H3K36 and H3K4 methylation, and PoSet2 negatively regulates cellulolytic enzyme production by antagonizing the PoSet1-H3K4me3 pathway. The balance of H3K4 and H3K36 methylation is required for the normal transcription of cellulolytic enzyme genes. These results extend our previous understanding that cellulolytic enzyme gene transcription is primarily controlled by transcription factors. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-019-1539-z) contains supplementary material, which is available to authorized users.