Transcriptomes of six mutants in the Sen1 pathway reveal combinatorial control of transcription termination across the Saccharomyces cerevisiae genome

PLoS Genet. 2017 Jun 30;13(6):e1006863. doi: 10.1371/journal.pgen.1006863. eCollection 2017 Jun.

Abstract

Transcriptome studies on eukaryotic cells have revealed an unexpected abundance and diversity of noncoding RNAs synthesized by RNA polymerase II (Pol II), some of which influence the expression of protein-coding genes. Yet, much less is known about biogenesis of Pol II non-coding RNA than mRNAs. In the budding yeast Saccharomyces cerevisiae, initiation of non-coding transcripts by Pol II appears to be similar to that of mRNAs, but a distinct pathway is utilized for termination of most non-coding RNAs: the Sen1-dependent or "NNS" pathway. Here, we examine the effect on the S. cerevisiae transcriptome of conditional mutations in the genes encoding six different essential proteins that influence Sen1-dependent termination: Sen1, Nrd1, Nab3, Ssu72, Rpb11, and Hrp1. We observe surprisingly diverse effects on transcript abundance for the different proteins that cannot be explained simply by differing severity of the mutations. Rather, we infer from our results that termination of Pol II transcription of non-coding RNA genes is subject to complex combinatorial control that likely involves proteins beyond those studied here. Furthermore, we identify new targets and functions of Sen1-dependent termination, including a role in repression of meiotic genes in vegetative cells. In combination with other recent whole-genome studies on termination of non-coding RNAs, our results provide promising directions for further investigation.

MeSH terms

  • DNA Helicases / genetics*
  • Gene Expression Regulation, Fungal
  • Genome, Fungal
  • Meiosis / genetics
  • Mutant Proteins / genetics
  • Nuclear Proteins / genetics
  • Phosphoprotein Phosphatases / genetics
  • RNA Helicases / genetics*
  • RNA Polymerase II / genetics*
  • RNA, Untranslated / genetics
  • RNA-Binding Proteins / genetics
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae Proteins / genetics*
  • Signal Transduction
  • Transcription Termination, Genetic*
  • Transcriptome / genetics
  • mRNA Cleavage and Polyadenylation Factors / genetics

Substances

  • HRP1 protein, S cerevisiae
  • Mutant Proteins
  • NAB3 protein, S cerevisiae
  • NRD1 protein, S cerevisiae
  • Nuclear Proteins
  • RNA, Untranslated
  • RNA-Binding Proteins
  • SSU72 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • mRNA Cleavage and Polyadenylation Factors
  • RNA Polymerase II
  • RPB11 protein, S cerevisiae
  • Phosphoprotein Phosphatases
  • SEN1 protein, S cerevisiae
  • DNA Helicases
  • RNA Helicases