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Real-time monitoring of single ZTP riboswitches reveals a complex and kinetically controlled decision landscape

Author

Listed:
  • Boyang Hua

    (Johns Hopkins School of Medicine)

  • Christopher P. Jones

    (Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health)

  • Jaba Mitra

    (University of Illinois at Urbana-Champaign)

  • Peter J. Murray

    (Johns Hopkins University)

  • Rebecca Rosenthal

    (Johns Hopkins University)

  • Adrian R. Ferré-D’Amaré

    (Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health)

  • Taekjip Ha

    (Johns Hopkins School of Medicine
    Johns Hopkins University
    Johns Hopkins University
    Howard Hughes Medical Institute)

Abstract

RNAs begin to fold and function during transcription. Riboswitches undergo cotranscriptional switching in the context of transcription elongation, RNA folding, and ligand binding. To investigate how these processes jointly modulate the function of the folate stress-sensing Fusobacterium ulcerans ZTP riboswitch, we apply a single-molecule vectorial folding (VF) assay in which an engineered superhelicase Rep-X sequentially releases fluorescently labeled riboswitch RNA from a heteroduplex in a 5′-to-3′ direction, at ~60 nt s−1 [comparable to the speed of bacterial RNA polymerase (RNAP)]. We demonstrate that the ZTP riboswitch is kinetically controlled and that its activation is favored by slower unwinding, strategic pausing between but not before key folding elements, or a weakened transcription terminator. Real-time single-molecule monitoring captures folding riboswitches in multiple states, including an intermediate responsible for delayed terminator formation. These results show how individual nascent RNAs occupy distinct channels within the folding landscape that controls the fate of the riboswitch.

Suggested Citation

  • Boyang Hua & Christopher P. Jones & Jaba Mitra & Peter J. Murray & Rebecca Rosenthal & Adrian R. Ferré-D’Amaré & Taekjip Ha, 2020. "Real-time monitoring of single ZTP riboswitches reveals a complex and kinetically controlled decision landscape," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18283-1
    DOI: 10.1038/s41467-020-18283-1
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    Cited by:

    1. Griffin M. Schroeder & Chapin E. Cavender & Maya E. Blau & Jermaine L. Jenkins & David H. Mathews & Joseph E. Wedekind, 2022. "A small RNA that cooperatively senses two stacked metabolites in one pocket for gene control," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Courtney E. Szyjka & Eric J. Strobel, 2023. "Observation of coordinated RNA folding events by systematic cotranscriptional RNA structure probing," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Yanyan Xue & Jun Li & Dian Chen & Xizhu Zhao & Liang Hong & Yu Liu, 2023. "Observation of structural switch in nascent SAM-VI riboswitch during transcription at single-nucleotide and single-molecule resolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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