IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38042-2.html
   My bibliography  Save this article

Observation of structural switch in nascent SAM-VI riboswitch during transcription at single-nucleotide and single-molecule resolution

Author

Listed:
  • Yanyan Xue

    (Shanghai Jiao Tong University)

  • Jun Li

    (Shanghai Jiao Tong University)

  • Dian Chen

    (Shanghai Jiao Tong University)

  • Xizhu Zhao

    (Shanghai Jiao Tong University)

  • Liang Hong

    (Shanghai Jiao Tong University
    Shanghai Jiao Tong University
    Shanghai Artificial Intelligence Laboratory)

  • Yu Liu

    (Shanghai Jiao Tong University
    Shanghai Artificial Intelligence Laboratory)

Abstract

Growing RNAs fold differently as they are transcribed, which modulates their finally adopted structures. Riboswitches regulate gene expression by structural change, which are sensitive to co-transcriptionally structural biology. Here we develop a strategy to track the structural change of RNAs during transcription at single-nucleotide and single-molecule resolution and use it to monitor individual transcripts of the SAM-VI riboswitch (riboSAM) as transcription proceeds, observing co-existence of five states in riboSAM. We report a bifurcated helix in one newly identified state from NMR and single-molecule FRET (smFRET) results, and its presence directs the translation inhibition in our cellular translation experiments. A model is proposed to illustrate the distinct switch patterns and gene-regulatory outcome of riboSAM when SAM is present or absent. Our strategy enables the precise mapping of RNAs’ conformational landscape during transcription, and may combine with detection methods other than smFRET for structural studies of RNAs in general.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38042-2
    DOI: 10.1038/s41467-023-38042-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38042-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38042-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Alex W. Wilkinson & Jonathan Diep & Shaobo Dai & Shuo Liu & Yaw Shin Ooi & Dan Song & Tie-Mei Li & John R. Horton & Xing Zhang & Chao Liu & Darshan V. Trivedi & Katherine M. Ruppel & José G. Vilches-M, 2019. "SETD3 is an actin histidine methyltransferase that prevents primary dystocia," Nature, Nature, vol. 565(7739), pages 372-376, January.
    2. Rajeev Yadav & Julia R. Widom & Adrien Chauvier & Nils G. Walter, 2022. "An anionic ligand snap-locks a long-range interaction in a magnesium-folded riboswitch," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Yanjiao Wang & Ge Han & Xiuying Jiang & Tairan Yuwen & Yi Xue, 2021. "Chemical shift prediction of RNA imino groups: application toward characterizing RNA excited states," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    4. Yu Liu & Erik Holmstrom & Jinwei Zhang & Ping Yu & Jinbu Wang & Marzena A. Dyba & De Chen & Jinfa Ying & Stephen Lockett & David J. Nesbitt & Adrian R. Ferré-D’Amaré & Rui Sousa & Jason R. Stagno & Yu, 2015. "Synthesis and applications of RNAs with position-selective labelling and mosaic composition," Nature, Nature, vol. 522(7556), pages 368-372, June.
    5. Tahir H. Tahirov & Dmitry Temiakov & Michael Anikin & Vsevolod Patlan & William T. McAllister & Dmitry G. Vassylyev & Shigeyuki Yokoyama, 2002. "Structure of a T7 RNA polymerase elongation complex at 2.9 Å resolution," Nature, Nature, vol. 420(6911), pages 43-50, November.
    6. J. R. Stagno & Y. Liu & Y. R. Bhandari & C. E. Conrad & S. Panja & M. Swain & L. Fan & G. Nelson & C. Li & D. R. Wendel & T. A. White & J. D. Coe & M. O. Wiedorn & J. Knoska & D. Oberthuer & R. A. Tuc, 2017. "Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography," Nature, Nature, vol. 541(7636), pages 242-246, January.
    7. Dong-Jie Tang & Xinyu Du & Qiang Shi & Jian-Ling Zhang & Yuan-Ping He & Yan-Miao Chen & Zhenhua Ming & Dan Wang & Wan-Ying Zhong & Yu-Wei Liang & Jin-Yang Liu & Jian-Ming Huang & Yun-Shi Zhong & Shi-Q, 2020. "A SAM-I riboswitch with the ability to sense and respond to uncharged initiator tRNA," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    8. Qi Zhang & Andrew C. Stelzer & Charles K. Fisher & Hashim M. Al-Hashimi, 2007. "Visualizing spatially correlated dynamics that directs RNA conformational transitions," Nature, Nature, vol. 450(7173), pages 1263-1267, December.
    9. 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.
    10. Aiai Sun & Catherina Gasser & Fudong Li & Hao Chen & Stefan Mair & Olga Krasheninina & Ronald Micura & Aiming Ren, 2019. "SAM-VI riboswitch structure and signature for ligand discrimination," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    11. Anke Reining & Senada Nozinovic & Kai Schlepckow & Florian Buhr & Boris Fürtig & Harald Schwalbe, 2013. "Three-state mechanism couples ligand and temperature sensing in riboswitches," Nature, Nature, vol. 499(7458), pages 355-359, July.
    12. Arlie J. Rinaldi & Paul E. Lund & Mario R. Blanco & Nils G. Walter, 2016. "The Shine-Dalgarno sequence of riboswitch-regulated single mRNAs shows ligand-dependent accessibility bursts," Nature Communications, Nature, vol. 7(1), pages 1-10, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xiaolin Niu & Zhonghe Xu & Yufan Zhang & Xiaobing Zuo & Chunlai Chen & Xianyang Fang, 2023. "Structural and dynamic mechanisms for coupled folding and tRNA recognition of a translational T-box riboswitch," Nature Communications, Nature, vol. 14(1), pages 1-14, 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. 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.
    4. Krishna C. Suddala & Janghyun Yoo & Lixin Fan & Xiaobing Zuo & Yun-Xing Wang & Hoi Sung Chung & Jinwei Zhang, 2023. "Direct observation of tRNA-chaperoned folding of a dynamic mRNA ensemble," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Tek Narsingh Malla & Kara Zielinski & Luis Aldama & Sasa Bajt & Denisse Feliz & Brendon Hayes & Mark Hunter & Christopher Kupitz & Stella Lisova & Juraj Knoska & Jose Manuel Martin-Garcia & Valerio Ma, 2023. "Heterogeneity in M. tuberculosis β-lactamase inhibition by Sulbactam," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Christine E. Peters & Ursula Schulze-Gahmen & Manon Eckhardt & Gwendolyn M. Jang & Jiewei Xu & Ernst H. Pulido & Conner Bardine & Charles S. Craik & Melanie Ott & Or Gozani & Kliment A. Verba & Ruth H, 2022. "Structure-function analysis of enterovirus protease 2A in complex with its essential host factor SETD3," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Ge Han & Yi Xue, 2022. "Rational design of hairpin RNA excited states reveals multi-step transitions," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    8. Juntaek Oh & Michiko Kimoto & Haoqing Xu & Jenny Chong & Ichiro Hirao & Dong Wang, 2023. "Structural basis of transcription recognition of a hydrophobic unnatural base pair by T7 RNA polymerase," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    9. Gregory D Friedland & Nils-Alexander Lakomek & Christian Griesinger & Jens Meiler & Tanja Kortemme, 2009. "A Correspondence Between Solution-State Dynamics of an Individual Protein and the Sequence and Conformational Diversity of its Family," PLOS Computational Biology, Public Library of Science, vol. 5(5), pages 1-16, May.
    10. Ainan Geng & Laura Ganser & Rohit Roy & Honglue Shi & Supriya Pratihar & David A. Case & Hashim M. Al-Hashimi, 2023. "An RNA excited conformational state at atomic resolution," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    11. Tanveer S. Batth & Jonas L. Simonsen & Cristina Hernández-Rollán & Søren Brander & Jens Preben Morth & Katja S. Johansen & Morten H. H. Nørholm & Jakob B. Hoof & Jesper V. Olsen, 2023. "A seven-transmembrane methyltransferase catalysing N-terminal histidine methylation of lytic polysaccharide monooxygenases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Mária Brunderová & Vojtěch Havlíček & Ján Matyašovský & Radek Pohl & Lenka Poštová Slavětínská & Matouš Krömer & Michal Hocek, 2024. "Expedient production of site specifically nucleobase-labelled or hypermodified RNA with engineered thermophilic DNA polymerases," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    13. Raphael Haslecker & Vincent V. Pham & David Glänzer & Christoph Kreutz & Theodore Kwaku Dayie & Victoria M. D’Souza, 2023. "Extending the toolbox for RNA biology with SegModTeX: a polymerase-driven method for site-specific and segmental labeling of RNA," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38042-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.