The Histone Demethylase JMJD2-Dependent Regulation of rDNA Transcription and Integrity of Nucleolus Is Required for Fungal Development and Pathogenicity in the Rice Blast Fungus.

The nucleolus is a central hub for nuclear functions, including, but not limited to, ribosome biogenesis in mammals and budding yeast. However, how the nucleolus is regulated and contributes to fungal development and pathogenesis is poorly understood. Here we report that a JmjC domain-containing histone demethylase MoJMJD2 is required for rDNA transcription and nucleolar integrity in the rice blast fungus, Magnaporthe oryzae. MoJMJD2 generates two alternatively spliced isoforms with distinct subcellular localization patterns, suggesting coordinated roles in gene regulation in the nucleolus and nucleoplasm. Deletion of MoJMJD2 rendered the fungus defective in hyphal growth, sporulation and pathogenicity. Notably, loss of MoJMJD2 led to mislocalization of a nucleolar protein to the nucleoplasm and a dramatic reduction of cellular protein synthesis, suggesting the disruption of functional nucleolar structure. Taken together, these results indicate that nucleolar integrity and functions, which are under epigenetic control associated with MoJMJD2, are required for the development and pathogenicity of the rice blast fungus.