The Histone Demethylase MoJMJD2 is Required for Fungal Development and Pathgenicity by Transcriptional Regulation of rDNA and Nuclear Genes in the Rice Blast Fungus

The Histone Demethylase MoJMJD2 is Required for Fungal Development and Pathogenicity by Transcriptional Regulation of rDNA and Nuclear Genes in the Rice Blast Fungus

Song Hee Lee1, 2, Taehyeon Kim1, Seonwoo Choi1 and Junhyun Jeon1, 2*

1Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University, Gyeongsan, Gyeongbuk 38541, Korea

2Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea

*Email: jjeon@yu.ac.kr

Reversible histone methylation is crucial process for epigenetic regulation of gene transcription and genome integrity. More specifically, histone demethylases play critical roles in transcription regulation and genome integrity by regulating histone methylation status via interplay with histone methyltransferase. Histone lysine demethylases have been classified into two families, which are JmjC (Jumonji C) and LSD (Lysine Specific Demethylase). JMJD2, which belongs to JmjC family, is known to remove methyl groups from H3K9 and H3K36. Here we report that a JmjC domain-containing histone demethylase, MoJMJD2 regulates transcription of both rDNA loci in nucleolus and a set of nuclear genes, which are development and pathogenesis related genes, via H3K9 and H3K36 demethylation in Magnaporthe oryzae. We showed that alternative splicing in MoJMJD2, which appears to be generated in an environment-dependent manner, such as conidiogenesis condition, generates a protein isoform lacking a putative nucleolar localization sequence. Deletion of MoJMJD2 led to defects in vegetative growth, pigmentation, asexual reproduction, penetration, invasive growth and cell wall synthesis, and re-introduction of wild-type copy of gene into the mutant was able to complement all these defects. Moreover, rDNA and some of the key melanin synthesis and cell wall synthesis genes H3K9me1, and some of key conidiogenesis genes H3K9me1 and H3K9me3 were directly regulated by MoJMJD2-mediated histone demethylation. Taken together, we propose that MoJMJD2 coordinates transcriptional regulation of rDNA in nucleolus and nuclear genes via histone demethylase activity and alternative splicing, linking ribosome biogenesis to transcription of nuclear genes in response to environmental cues.