A CPF-like phosphatase module links transcription termination to chromatin silencing

The interconnections between co-transcriptional regulation, chromatin environment and transcriptional output remain poorly understood. Here, we investigate the mechanism underlying RNA 3 processing-mediated Polycomb silencing of Arabidopsis FLOWERING LOCUS C (FLC). We show a requirement for APRF1, a homologue of yeast Swd2 and human WDR82, known to regulate RNA Pol II during transcription termination. APRF1 interacts with TOPP4 (yeast Glc7/human PP1) and LD, the latter showing structural features found in Ref2/PNUTS; all components of the yeast and human phosphatase module of the CPF 3 end processing machinery. LD has been shown to co-associate in vivo with the histone H3 K4 demethylase FLD. We show APRF1 and LD couple CPF-mediated cleavage and polyadenylation with removal of H3K4 monomethylation in the body of FLC, and this influences subsequent transcription. This work shows how transcription termination can change the local chromatin environment to modulate transcription of Arabidopsis FLC and affect flowering time.