Methylation levels of histone 3 lysine 4 (H3K4) play a crucial role in transcription regulation and are finely controlled by the action of specific histone methyltransferases and demethylases during development. Here, we address the role of the H3K4me2/3 demethylase RBR-2, the unique member of the KDM5 class of histone demethylases in C. elegans, in cell differentiation during postembryonic development. We found that the enzymatic activity of RBR-2 is required cell-autonomously to regulate the 2° cell fate acquisition in vulva precursor cells and to achieve correct vulva formation. Genome-wide analysis indicates that RBR-2 is needed for the regulation of H3K4me levels in regulatory regions of the genome, including transcription start sites and enhancer regions. Loss of RBR-2 results not only in aberrant acquisition of H3K4me3 at transcription start sites, but also in loss of enhancer signatures in regulatory regions. Accordingly, RNA sequencing analysis shows both up- and down-regulation of gene transcription, suggesting a complex function of RBR-2 in regulating gene activity.
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