Two closely related TRB-containing complexes cooperate to mediate H3K4me3 demethylation and transcriptional repression [ChIP-seq]
The telomere repeat binding factors TRB1, TRB2, and TRB3 (TRB1/2/3) in Arabidopsis thaliana not only function as components of the PEAT complex involved in histone acetylation and H2A deubiquitination but also interact with Polycomb Repressive Complex 2 (PRC2) involved in H3 lysine 27 trimethylation (H3K27me3). In this study, we demonstrate that TRB1/2/3 form two additional chromatin-associated complexes, which we term TRB1/2/3-HTH1/2/3 (TRHT) and TRB1/2/3-HISTONE-DEMETHYLASE (TRHD). The TRHT complex comprises TRB1/2/3, ICU11, and HTH1/2/3, whereas the TRHD complex is composed of TRB1/2/3, ICU11, ZDP2, JMJ14, and NAC050/052. The TRHT and TRHD (TRHT/TRHD) complexes occupy a common set of target genes and cooperate to mediate JMJ14-mediated H3K4me3 demethylation and transcriptional repression. Compared with PEAT and PRC2 target genes, which are characterized by high and low levels of H3K4me3, respectively, the TRHT/TRHD target genes exhibit low to medium levels of H3K4me3. At the whole-genome level, TRB1/2/3 repress transcription at TRHT/TRHD and PRC2 target genes, while facilitating transcription at PEAT target genes. At the TRHT/TRHD target genes, the TRHT/TRHD complexes mediate transcriptional repression through both H3K4me3 demethylation-dependent and –independent mechanisms. These findings reveal the molecular mechanisms by which how the TRHT/TRHD complexes are coordinated with the PEAT and PRC2 complex to ensure the orchestration of multiple histone modifications at the whole-genome level. Overall design: Examination of protein binding levels in transgenic plants; For H3K4me3 ChIP-seq, examination of H3K4me3 levels in wild type and four mutants.