Epigenetic gene regulation is controlled by distinct regulatory complexes utilizing specialized paralogs of Telomere Repeat Binding factors

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.