Epigenetic gene regulation is controlled by distinct regulatory complexes utilizing specialized paralogs of TELOMERE...

Epigenetic regulators shape chromatin landscapes, allowing cells to express distinct gene sets depending on cell-type, developmental stage or environmental cues. These regulatory complexes rely on interactions with sequence-specific DNA binding proteins, such as the small family of TELOMERE REPEAT BINDING FACTORS (TRBs). TRBs are components of chromatin regulatory complexes with opposing functions, such as the epigenetic repressors Polycomb Repressive Complex 2 (PRC2) and a JMJ14/NAC complex that respectively add and removes the repressive H3K27me3 and positive H3K4me3 modification, but also with the plant-specific PEAT complex that is linked to histone acetylation and gene activation. We dissected the partial redundancy between TRB1, TRB2 and TRB3 in target gene selection and interaction with different chromatin regulatory complexes. High redundancy of TRBs is suggested by major phenotypic changes that are only observed trb triple mutants; however, we found different target site preference between TRB1-3 and preferred partnership with chromatin complexes. Furthermore, TRB paralogs interacted with the NuA4 histone acetylation complex, both together with and in absence of PEAT. Among the three paralogs, TRB1 had more unique binding sites and correlated stronger with PEAT and NuA4 functions. In contrast, TRB2 and TRB3 were more dependent on the presence of bona fide telo-box motifs and were more likely to be found at PRC2 associated sites. Overall, we provide insight into the diverse roles of TRBs in epigenetic gene regulation and how their diversification contributes to their apparent redundancy, as well as their observed activating and repressing effects on gene expression.