RNA polymerase backtracking results in the accumulation of fission yeast condensin at active genes

Life Sci Alliance. 2021 Mar 26;4(6):e202101046. doi: 10.26508/lsa.202101046. Print 2021 Jun.

Abstract

The mechanisms leading to the accumulation of the SMC complexes condensins around specific transcription units remain unclear. Observations made in bacteria suggested that RNA polymerases (RNAPs) constitute an obstacle to SMC translocation, particularly when RNAP and SMC travel in opposite directions. Here we show in fission yeast that gene termini harbour intrinsic condensin-accumulating features whatever the orientation of transcription, which we attribute to the frequent backtracking of RNAP at gene ends. Consistent with this, to relocate backtracked RNAP2 from gene termini to gene bodies was sufficient to cancel the accumulation of condensin at gene ends and to redistribute it evenly within transcription units, indicating that RNAP backtracking may play a key role in positioning condensin. Formalization of this hypothesis in a mathematical model suggests that the inclusion of a sub-population of RNAP with longer dwell-times is essential to fully recapitulate the distribution profiles of condensin around active genes. Taken together, our data strengthen the idea that dense arrays of proteins tightly bound to DNA alter the distribution of condensin on chromosomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Chromosomes / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • DNA-Directed RNA Polymerases / genetics
  • DNA-Directed RNA Polymerases / metabolism
  • Gene Expression / genetics
  • Gene Expression Regulation, Fungal / genetics
  • Mitosis / genetics
  • Mitosis / physiology*
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism*
  • RNA Polymerase II / metabolism*
  • RNA Polymerase II / physiology
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces pombe Proteins / metabolism
  • Transcription, Genetic / genetics

Substances

  • DNA-Binding Proteins
  • Multiprotein Complexes
  • Schizosaccharomyces pombe Proteins
  • condensin complexes
  • RNA Polymerase II
  • DNA-Directed RNA Polymerases
  • Adenosine Triphosphatases