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Force and the α-C-terminal domains bias RNA polymerase recycling

Author

Listed:
  • Jin Qian

    (Emory University)

  • Bing Wang

    (The Ohio State University)

  • Irina Artsimovitch

    (The Ohio State University)

  • David Dunlap

    (Clemson University)

  • Laura Finzi

    (Clemson University)

Abstract

After an RNA polymerase reaches a terminator, instead of dissociating from the template, it may diffuse along the DNA and recommence RNA synthesis from the previous or a different promoter. Magnetic tweezers were used to monitor such secondary transcription and determine the effects of low forces assisting or opposing translocation, protein roadblocks, and transcription factors. Remarkably, up to 50% of Escherichia coli (E. coli) RNA polymerases diffused along the DNA after termination. Force biased the direction of diffusion (sliding) and the velocity increased rapidly with force up to 0.7 pN and much more slowly thereafter. Sigma factor 70 (σ70) likely remained associated with the DNA promoting sliding and enabling re-initiation from promoters in either orientation. However, deletions of the α-C-terminal domains severely limited the ability of RNAP to turn around between successive rounds of transcription. The addition of elongation factor NusG, which competes with σ70 for binding to RNAP, limited additional rounds of transcription. Surprisingly, sliding RNA polymerases blocked by a DNA-bound lac repressor could slowly re-initiate transcription and were not affected by NusG, suggesting a σ-independent pathway. Low forces effectively biased promoter selection suggesting a prominent role for topological entanglements that affect RNA polymerase translocation.

Suggested Citation

  • Jin Qian & Bing Wang & Irina Artsimovitch & David Dunlap & Laura Finzi, 2024. "Force and the α-C-terminal domains bias RNA polymerase recycling," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51603-3
    DOI: 10.1038/s41467-024-51603-3
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    References listed on IDEAS

    as
    1. Jin Qian & Allison Cartee & Wenxuan Xu & Yan Yan & Bing Wang & Irina Artsimovitch & David Dunlap & Laura Finzi, 2024. "Reciprocating RNA Polymerase batters through roadblocks," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Joshua W. Shaevitz & Elio A. Abbondanzieri & Robert Landick & Steven M. Block, 2003. "Backtracking by single RNA polymerase molecules observed at near-base-pair resolution," Nature, Nature, vol. 426(6967), pages 684-687, December.
    3. Timothy T. Harden & Karina S. Herlambang & Mathew Chamberlain & Jean-Benoît Lalanne & Christopher D. Wells & Gene-Wei Li & Robert Landick & Ann Hochschild & Jane Kondev & Jeff Gelles, 2020. "Alternative transcription cycle for bacterial RNA polymerase," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Vitaly Epshtein & Venu Kamarthapu & Katelyn McGary & Vladimir Svetlov & Beatrix Ueberheide & Sergey Proshkin & Alexander Mironov & Evgeny Nudler, 2014. "UvrD facilitates DNA repair by pulling RNA polymerase backwards," Nature, Nature, vol. 505(7483), pages 372-377, January.
    5. Wooyoung Kang & Kook Sun Ha & Heesoo Uhm & Kyuhyong Park & Ja Yil Lee & Sungchul Hohng & Changwon Kang, 2020. "Transcription reinitiation by recycling RNA polymerase that diffuses on DNA after releasing terminated RNA," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    6. Yeonoh Shin & M. Zuhaib Qayyum & Danil Pupov & Daria Esyunina & Andrey Kulbachinskiy & Katsuhiko S. Murakami, 2021. "Structural basis of ribosomal RNA transcription regulation," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    7. Linlin You & Expery O. Omollo & Chengzhi Yu & Rachel A. Mooney & Jing Shi & Liqiang Shen & Xiaoxian Wu & Aijia Wen & Dingwei He & Yuan Zeng & Yu Feng & Robert Landick & Yu Zhang, 2023. "Structural basis for intrinsic transcription termination," Nature, Nature, vol. 613(7945), pages 783-789, January.
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