Mitotically heritable, RNA polymerase II-independent H3K4 dimethylation stimulates INO1 transcriptional memory

Elife. 2022 May 17:11:e77646. doi: 10.7554/eLife.77646.

Abstract

For some inducible genes, the rate and molecular mechanism of transcriptional activation depend on the prior experiences of the cell. This phenomenon, called epigenetic transcriptional memory, accelerates reactivation, and requires both changes in chromatin structure and recruitment of poised RNA polymerase II (RNAPII) to the promoter. Memory of inositol starvation in budding yeast involves a positive feedback loop between transcription factor-dependent interaction with the nuclear pore complex and histone H3 lysine 4 dimethylation (H3K4me2). While H3K4me2 is essential for recruitment of RNAPII and faster reactivation, RNAPII is not required for H3K4me2. Unlike RNAPII-dependent H3K4me2 associated with transcription, RNAPII-independent H3K4me2 requires Nup100, SET3C, the Leo1 subunit of the Paf1 complex and, upon degradation of an essential transcription factor, is inherited through multiple cell cycles. The writer of this mark (COMPASS) physically interacts with the potential reader (SET3C), suggesting a molecular mechanism for the spreading and re-incorporation of H3K4me2 following DNA replication.

Keywords: S. cerevisiae; chromatin; chromosomes; epigenetics; fitness; gene expression; genetics; genomics; mitosis; nuclear pore; transcriptional memory.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Histone Deacetylases / metabolism
  • Histones / metabolism
  • Nuclear Pore / metabolism
  • Nuclear Pore Complex Proteins / metabolism
  • RNA Polymerase II* / metabolism
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Transcription Factors / metabolism
  • Transcription, Genetic

Substances

  • Histones
  • Nuclear Pore Complex Proteins
  • Saccharomyces cerevisiae Proteins
  • Transcription Factors
  • RNA Polymerase II
  • Histone Deacetylases