Arabidopsis TRB Proteins Form Two Closely Related Complexes to Mediate H3K4me3 Demethylation and Transcriptional Repression

Abstract The Arabidopsis telomere repeat binding proteins TRB1, TRB2, and TRB3 (TRB1/2/3) are components of the PWWP‐EPCR‐ARID‐TRB (PEAT) complex, which is involved in histone acetylation and H2A deubiquitination. TRB1/2/3 also interact with the Polycomb Repressive Complex 2 (PRC2), which mediates H3 lysine 27 trimethylation. This study demonstrates that TRB1/2/3 can form two closely related complexes: TRB1/2/3‐HELIX‐TURN‐HELIX‐PROTEIN (TRHT) and TRB1/2/3‐HISTONE‐DEMETHYLASE (TRHD). The TRHT and TRHD (TRHT/TRHD) complexes occupy numerous common target genes across the genome and are required for H3K4me3 demethylation mediated by the histone demethylase JMJ14. Within the TRHT/TRHD complexes, the transcriptional repressors TRB1/2/3 and NAC050/052 bind to distinct DNA motifs and cooperate to mediate the association of these complexes with their target genes. Compared to PEAT target genes with high H3K4me3 levels and PRC2 target genes with low H3K4me3 levels, TRHT/TRHD target genes display low‐to‐medium levels of H3K4me3. At TRHT/TRHD target genes, JMJ14‐mediated H3K4me3 demethylation is enhanced when these genes are shared with PRC2 target genes and is suppressed when they are shared with PEAT target genes. These findings reveal how the newly identified TRHT/TRHD complexes cooperate with the PEAT and PRC2 complexes to regulate multiple histone modifications and gene transcription across the genome.