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

Mol Cell. 2024 Jun 20;84(12):2272-2286.e7. doi: 10.1016/j.molcel.2024.05.016. Epub 2024 Jun 7.

Abstract

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 ANTHESIS PROMOTING FACTOR 1 (APRF1), a homolog of yeast Swd2 and human WDR82, known to regulate RNA polymerase II (RNA Pol II) during transcription termination. APRF1 interacts with TYPE ONE SERINE/THREONINE PROTEIN PHOSPHATASE 4 (TOPP4) (yeast Glc7/human PP1) and LUMINIDEPENDENS (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 FLOWERING LOCUS D (FLD). This work shows how the APRF1/LD-mediated polyadenylation/termination process influences subsequent rounds of transcription by changing the local chromatin environment at FLC.

Keywords: COOLAIR; ChIP; FLC; IP-MS; Quant-seq; RNA 3′ processing; chromatin silencing; co-transcriptional processing; plaNET-seq; transcription termination.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / enzymology
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Chromatin* / genetics
  • Chromatin* / metabolism
  • Gene Expression Regulation, Plant*
  • Gene Silencing*
  • Histone Deacetylases
  • Histones / genetics
  • Histones / metabolism
  • MADS Domain Proteins* / genetics
  • MADS Domain Proteins* / metabolism
  • Phosphoprotein Phosphatases / genetics
  • Phosphoprotein Phosphatases / metabolism
  • RNA Polymerase II* / genetics
  • RNA Polymerase II* / metabolism
  • Transcription Termination, Genetic*
  • mRNA Cleavage and Polyadenylation Factors / genetics
  • mRNA Cleavage and Polyadenylation Factors / metabolism

Substances

  • Arabidopsis Proteins
  • Chromatin
  • At5g10140 protein, Arabidopsis
  • MADS Domain Proteins
  • RNA Polymerase II
  • Phosphoprotein Phosphatases
  • flowering locus D protein, Arabidopsis
  • mRNA Cleavage and Polyadenylation Factors
  • Histones
  • Histone Deacetylases