TOP1α regulates FLOWERING LOCUS C expression by coupling histone modification and transcription machinery

Development. 2019 Feb 15;146(4):dev167841. doi: 10.1242/dev.167841.

Abstract

The key steps of transcription are coupled with the opening of the DNA helical structure and establishment of active chromatin to facilitate the movement of the transcription machinery. Type I topoisomerases cleave one DNA strand and relax the supercoiled structure of transcribed templates. How topoisomerase-mediated DNA topological changes promote transcription and establish a permissive histone modification for transcription elongation is largely unknown. Here, we show that TOPOISOMERASE 1α in plants regulates FLOWERING LOCUS C transcription by coupling histone modification and transcription machinery. We demonstrate that TOP1α directly interacts with the methyltransferase SDG8 to establish high levels of H3K36 methylation downstream of FLC transcription start sites and recruits RNA polymerase II to facilitate transcription elongation. Our results provide a mechanistic framework for TOP1α control of the main steps of early transcription and demonstrate how topoisomerases couple RNA polymerase II and permissive histone modifications to initiate transcription elongation.

Keywords: Arabidopsis; FLOWERING LOCUS C; H3K36 methyltransferase; RNA polymerase II; Topoisomerase I; Transcription elongation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • DNA Topoisomerases, Type I / genetics
  • DNA Topoisomerases, Type I / metabolism*
  • Fluorescence Resonance Energy Transfer
  • Gene Expression Regulation, Plant
  • Genetic Complementation Test
  • Histone-Lysine N-Methyltransferase / metabolism
  • Histones / metabolism*
  • MADS Domain Proteins / genetics
  • MADS Domain Proteins / metabolism*
  • Methylation
  • Mutation
  • Protein Processing, Post-Translational
  • RNA Polymerase II / metabolism
  • Transcription, Genetic

Substances

  • Arabidopsis Proteins
  • FLF protein, Arabidopsis
  • Histones
  • MADS Domain Proteins
  • Histone-Lysine N-Methyltransferase
  • LAZ2 protein, Arabidopsis
  • RNA Polymerase II
  • DNA Topoisomerases, Type I
  • TOP1alpha protein, Arabidopsis