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The conserved RNA-binding protein Seb1 promotes cotranscriptional ribosomal RNA processing by controlling RNA polymerase I progression

Author

Listed:
  • Maxime Duval

    (Université de Sherbrooke)

  • Carlo Yague-Sanz

    (Université de Sherbrooke
    The University of Namur)

  • Tomasz W. Turowski

    (Polish Academy of Sciences)

  • Elisabeth Petfalski

    (University of Edinburgh)

  • David Tollervey

    (University of Edinburgh)

  • François Bachand

    (Université de Sherbrooke)

Abstract

Transcription by RNA polymerase I (RNAPI) represents most of the transcriptional activity in eukaryotic cells and is associated with the production of mature ribosomal RNA (rRNA). As several rRNA maturation steps are coupled to RNAPI transcription, the rate of RNAPI elongation directly influences processing of nascent pre-rRNA, and changes in RNAPI transcription rate can result in alternative rRNA processing pathways in response to growth conditions and stress. However, factors and mechanisms that control RNAPI progression by influencing transcription elongation rate remain poorly understood. We show here that the conserved fission yeast RNA-binding protein Seb1 associates with the RNAPI transcription machinery and promotes RNAPI pausing states along the rDNA. The overall faster progression of RNAPI at the rDNA in Seb1-deficient cells impaired cotranscriptional pre-rRNA processing and the production of mature rRNAs. Given that Seb1 also influences pre-mRNA processing by modulating RNAPII progression, our findings unveil Seb1 as a pause-promoting factor for RNA polymerases I and II to control cotranscriptional RNA processing.

Suggested Citation

  • Maxime Duval & Carlo Yague-Sanz & Tomasz W. Turowski & Elisabeth Petfalski & David Tollervey & François Bachand, 2023. "The conserved RNA-binding protein Seb1 promotes cotranscriptional ribosomal RNA processing by controlling RNA polymerase I progression," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38826-6
    DOI: 10.1038/s41467-023-38826-6
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    References listed on IDEAS

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    1. Carlos Fernández-Tornero & María Moreno-Morcillo & Umar J. Rashid & Nicholas M. I. Taylor & Federico M. Ruiz & Tim Gruene & Pierre Legrand & Ulrich Steuerwald & Christoph W. Müller, 2013. "Crystal structure of the 14-subunit RNA polymerase I," Nature, Nature, vol. 502(7473), pages 644-649, October.
    2. L. Stirling Churchman & Jonathan S. Weissman, 2011. "Nascent transcript sequencing visualizes transcription at nucleotide resolution," Nature, Nature, vol. 469(7330), pages 368-373, January.
    3. Sina Wittmann & Max Renner & Beth R. Watts & Oliver Adams & Miles Huseyin & Carlo Baejen & Kamel El Omari & Cornelia Kilchert & Dong-Hyuk Heo & Tea Kecman & Patrick Cramer & Jonathan M. Grimes & Lidia, 2017. "The conserved protein Seb1 drives transcription termination by binding RNA polymerase II and nascent RNA," Nature Communications, Nature, vol. 8(1), pages 1-15, April.
    4. Marc Larochelle & Marc-Antoine Robert & Jean-Nicolas Hébert & Xiaochuan Liu & Dominick Matteau & Sébastien Rodrigue & Bin Tian & Pierre-Étienne Jacques & François Bachand, 2018. "Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    5. Mikael Björklund & Minna Taipale & Markku Varjosalo & Juha Saharinen & Juhani Lahdenperä & Jussi Taipale, 2006. "Identification of pathways regulating cell size and cell-cycle progression by RNAi," Nature, Nature, vol. 439(7079), pages 1009-1013, February.
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