The TELOMERE REPEAT BINDING proteins TRB4 and TRB5 function as transcriptional activators of PRC2-controlled genes to regulate plant development

Plant-specific transcriptional regulators called TELOMERE REPEAT BINDING proteins(TRBs)combine two DNA-binding domains,the GH1 domain,which binds to linker DNA and is shared with H1 histones,and the Myb/SANT domain,which specifically recognizes the telobox DNA-binding site motif.TRB1,TRB2,and TRB3 proteins recruit Polycomb group complex 2(PRC2)to deposit H3K27me3 and JMJ14 to remove H3K4me3 at gene promoters containing telobox motifs to repress transcription.Here,we demonstrate that TRB4 and TRB5,two related paralogs belonging to a separate TRB clade conserved in spermatophytes,regulate the transcription of several hundred genes involved in developmental responses to environmental cues.TRB4 binds to several thousand sites in the genome,mainly at transcription start sites and promoter regions of transcriptionally active and H3K4me3-marked genes,but,unlike TRB1,it is not enriched at H3K27me3-marked gene bodies.However,TRB4 can physically interact with the catalytic components of PRC2,SWINGER,and CURLY LEAF(CLF).Unexpectedly,we show that TRB4 and TRB5 are required for distinctive phenotypic traits observed in clf mutant plants and thus function as transcriptional activators of several hundred CLF-controlled genes,including key flowering genes.We further demonstrate that TRB4 shares multiple target genes with TRB1 and physically and genetically interacts with members of both TRB clades.Collectively,these results reveal that TRB proteins engage in both positive and negative interactions with other members of the family to regulate plant development through both PRC2-dependent and-independent mechanisms.

DET1-mediated COP1 regulation avoids HY5 activity over second-site gene targets to tune plant photomorphogenesis

DE-ETIOLATED 1(DET1)and CONSTITUTIVE PHOTOMORPHOGENESIS 1(COP1)are two essential repressors of Arabidopsis photomorphogenesis.These proteins can associate with CULLIN4 to form independent CRL4-based E3 ubiquitin ligases that mediate the degradation of several photomorphogenic transcription factors,including ELONGATED HYPOCOTYL 5(HY5),thereby controlling multiple gene-regulatory networks.Despite extensive biochemical and genetic analyses of their multi-subunit complexes,the functional links between DET1 and COP1 have long remained elusive.Here,we report that DET1 associates with COP1 in vivo,enhances COP1-HY5 interaction,and promotes COP1 destabilization in a process that dampens HY5 protein abundance.By regulating its accumulation,DET1 avoids HY5 association with hundreds of second-site genomic loci,which are also frequently targeted by the skotomorphogenic transcription factor PHYTOCHROME-INTERACTING FACTOR 3.Accordingly,ectopic HY5 chromatin enrichment favors local gene repression and can trigger fusca-like phenotypes.This study therefore shows that DET1-mediated regulation of COP1 stability tunes down the HY5 cistrome,avoiding hyper-photomorphogenic responses that might compromise plant viability.

A Dynamic Signaling Path to Chromatin-Level Control of Plant Drought Response

As sessile organisms, plants display a high capacity for phenotypic adaptations allowing them to meet the constraints of a changing local environment. This plasticity notably originates from the aptitude of plants to adjust their development and physiology throughout their lifetime to reach an optimal trade-off between growth and fitness. As in all eukaryotes, dynamic control of plant gene expression in different cell types is dependent on multiple regulatory layers that often converge onto chromatin-based mechanisms. Dynamic control of chromatin composition and organization has a strong impact on the cellular transcriptional program, notably contributing to selective modulation of gene expression in a reversible manner. Chromatin state changes generally involve remodeling of nu cleosome positio ning, incorporatio n of nu cleosomal and lin ker histone variants, and DNA and histone modifications recognized by cognate readers. Together, these processes modulate the access and activity of trans-acting factors such as transcription factors and RNA polymerases. Temporary shifts between transcriptionally permissive and repressive chromatin states rely on various mechanisms, among which is the rapid reversion of a “responsive” chromatin status through active erasure of newly established features.