The transcriptional repressors VAL1 and VAL2 recruit PRC2 for genome-wide Polycomb silencing in Arabidopsis

Abstract

The Polycomb repressive complex 2 (PRC2) catalyzes histone H3 Lys27 trimethylation (H3K27me3) to repress gene transcription in multicellular eukaryotes. Despite its importance in gene silencing and cellular differentiation, how PRC2 is recruited to target loci is still not fully understood. Here, we report genome-wide evidence for the recruitment of PRC2 by the transcriptional repressors VIVIPAROUS1/ABI3-LIKE1 (VAL1) and VAL2 in Arabidopsis thaliana. We show that the val1 val2 double mutant possesses somatic embryonic phenotypes and a transcriptome strikingly similar to those of the swn clf double mutant, which lacks the PRC2 catalytic subunits SWINGER (SWN) and CURLY LEAF (CLF). We further show that VAL1 and VAL2 physically interact with SWN and CLF in vivo. Genome-wide binding profiling demonstrated that they colocalize with SWN and CLF at PRC2 target loci. Loss of VAL1/2 significantly reduces SWN and CLF enrichment at PRC2 target loci and leads to a genome-wide redistribution of H3K27me3 that strongly affects transcription. Finally, we provide evidence that the VAL1/VAL2–RY regulatory system is largely independent of previously identified modules for Polycomb silencing in plants. Together, our work demonstrates an extensive genome-wide interaction between VAL1/2 and PRC2 and provides mechanistic insights into the establishment of Polycomb silencing in plants.

VAL genes regulate vegetative phase change via miR156-dependent and independent mechanisms

“…Although there was no difference in the temporal pattern of H3K27me3 deposition at MIR156A in val1-5(sd); val2-3 , the rate of H3K27me3 deposition at MIR156C was significantly slower in this double mutant ( Fig 3B ). These results are consistent with a recent genome-wide study that revealed a decrease in H3K27me3 levels at MIR156C , but not MIR156A , in val1-2; val2-3 plants [ 35 ]. As a control, we measured H3K27me3 deposition at the floral regulator FLC .…”

“…Previous analyses of VAL gene function have utilized val1-2; val2-1 and val1-2; val2-3 double mutants. However, seedling development is so strongly perturbed in val1-2; val2-1 and val1-2; val2-3 plants [ 16 , 25 , 35 , 38 ] that analyses of vegetative growth is problematic in these backgrounds. Therefore, we generated new val1; val2 combinations using val2-3 and a previously uncharacterized T-DNA insertion allele we named val2-4 .…”

“…Neither double mutant combination was as phenotypically severe as val1-2; val2-1 ( Fig 1C, 1D and 1E ). The weaker phenotype of val1-5(sd); val2-3 compared to val1-2; val2-3 [ 16 , 35 ], and stronger effects of val2 in the val1-2 than val1-5(sd) background ( Fig 1E ), suggests that the semi-dominant phenotype of val1-5(sd) is mediated by interaction with VAL2 . Importantly, the rate of germination was higher in val1-2; val2-4 and val1-5(sd); val2-3 relative to existing val1; val2 double mutants.…”

“…A number of observations suggest that VAL genes might provide the temporal information that coordinates vegetative phase change: 1) VAL genes regulate other developmental transitions, i.e. seed maturation [ 16 , 25 ] and flowering [ 30 , 32 ]; 2) MIR156A/C expression is elevated in val1/2 mutants [ 20 ]; 3) VAL1/2 physically interact with several histone deacetylases ( HDA6/9/19 ) [ 23 , 30 , 33 , 34 ]; and 4) VAL genes promote PRC1 and PRC2-binding [ 20 , 26 , 30 , 32 , 35 ].…”

Dynamics of H3K27me3 Modification on Plant Adaptation to Environmental Cues

“…Likewise, telobox motifs are bound by either TELOMERE REPEAT BINDING PROTEIN (TRB) factors or C2H2 zinc-finger family (C1-2iD subfamily) members that guide PRC2 to implement H3K27me3 deposition, which represents an evolutionarily ancient mechanism of telomeric repeats for PRC2-mediated H3K27me3 loading [120,[123][124][125]. Moreover, the RY-repeat motif recruits the PRC2 complex through the intermediation of VIVIPAROUS1/ABI3-LIKE (VAL) transcription factors [126][127][128][129][130][131][132][133]. In agreement, mutants of either trb1/2/3, bpc1-1bpc2bpc4bpc6, or val1val2 in Arabidopsis genetically mimic the phenotypes of those strong PRC2 mutants; however, chromatin loci occupied by these proteins jointly overlap with around 60% of H3K27me3 targets [125,129,134,135].…”