Noncoding RNA plays essential roles in transcriptional control and chromatin silencing. At Arabidopsis thaliana FLC, antisense transcription quantitatively influences transcriptional output, but the mechanism by which this occurs is still unclear. Proximal polyadenylation of the antisense transcripts by FCA, an RNA-binding protein that physically interacts with RNA 3′ processing factors, reduces FLC transcription. This process genetically requires FLD, a homolog of the H3K4 demethylase LSD1. However, the mechanism linking RNA processing to FLD function had not been established. Here, we show that FLD tightly associates with LUMINIDEPENDENS (LD) and SET DOMAIN GROUP 26 (SDG26) in vivo, and, together, they prevent accumulation of monomethylated H3K4 (H3K4me1) over the FLC gene body. SDG26 interacts with the RNA 3′ processing factor FY (WDR33), thus linking activities for proximal polyadenylation of the antisense transcripts to FLD/LD/SDG26-associated H3K4 demethylation. We propose this demethylation antagonizes an active transcription module, thus reducing H3K36me3 accumulation and increasing H3K27me3. Consistent with this view, we show that Polycomb Repressive Complex 2 (PRC2) silencing is genetically required by FCA to repress FLC. Overall, our work provides insights into RNA-mediated chromatin silencing.

非编码 RNA 在转录控制和染色质沉默中起重要作用。在拟南芥 FLC 中，反义转录定量地影响转录输出，但其发生的机制仍不清楚。FCA（一种与 RNA 3' 加工因子物理相互作用的 RNA 结合蛋白）对反义转录物的近端多聚腺苷酸化可减少FLC转录。这个过程在遗传上需要 FLD，它是 H3K4 去甲基化酶 LSD1 的同源物。然而，将 RNA 加工与 FLD 功能联系起来的机制尚未建立。在这里，我们表明 FLD 在体内与 LUMINIDEPENDENS (LD) 和 SET DOMAIN GROUP 26 (SDG26) 紧密结合，并且它们一起防止单甲基化 H3K4 (H3K4me1) 在FLC上的积累基因体。SDG26 与 RNA 3' 加工因子 FY (WDR33) 相互作用，从而将反义转录物近端多腺苷酸化的活性与 FLD/LD/SDG26 相关的 H3K4 去甲基化联系起来。我们建议这种去甲基化拮抗一个活跃的转录模块，从而减少 H3K36me3 的积累并增加 H3K27me3。与这一观点一致，我们表明 FCA 抑制FLC基因需要 Polycomb 抑制复合物 2 (PRC2) 沉默。总的来说，我们的工作提供了对 RNA 介导的染色质沉默的见解。