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Direct observation of tRNA-chaperoned folding of a dynamic mRNA ensemble

Author

Listed:
  • Krishna C. Suddala

    (National Institute of Diabetes and Digestive and Kidney Diseases)

  • Janghyun Yoo

    (National Institute of Diabetes and Digestive and Kidney Diseases)

  • Lixin Fan

    (Small-Angle X-Ray Scattering Core Facility of National Cancer Institute)

  • Xiaobing Zuo

    (Argonne National Laboratory)

  • Yun-Xing Wang

    (Small-Angle X-Ray Scattering Core Facility of National Cancer Institute
    Center for Cancer Research, National Cancer Institute)

  • Hoi Sung Chung

    (National Institute of Diabetes and Digestive and Kidney Diseases)

  • Jinwei Zhang

    (National Institute of Diabetes and Digestive and Kidney Diseases)

Abstract

T-box riboswitches are multi-domain noncoding RNAs that surveil individual amino acid availabilities in most Gram-positive bacteria. T-boxes directly bind specific tRNAs, query their aminoacylation status to detect starvation, and feedback control the transcription or translation of downstream amino-acid metabolic genes. Most T-boxes rapidly recruit their cognate tRNA ligands through an intricate three-way stem I-stem II-tRNA interaction, whose establishment is not understood. Using single-molecule FRET, SAXS, and time-resolved fluorescence, we find that the free T-box RNA assumes a broad distribution of open, semi-open, and closed conformations that only slowly interconvert. tRNA directly binds all three conformers with distinct kinetics, triggers nearly instantaneous collapses of the open conformations, and returns the T-box RNA to their pre-binding conformations upon dissociation. This scissors-like dynamic behavior is enabled by a hinge-like pseudoknot domain which poises the T-box for rapid tRNA-induced domain closure. This study reveals tRNA-chaperoned folding of flexible, multi-domain mRNAs through a Venus flytrap-like mechanism.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41155-3
    DOI: 10.1038/s41467-023-41155-3
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    References listed on IDEAS

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    1. Jinwei Zhang & Adrian R. Ferré-D’Amaré, 2013. "Co-crystal structure of a T-box riboswitch stem I domain in complex with its cognate tRNA," Nature, Nature, vol. 500(7462), pages 363-366, August.
    2. 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.
    3. Janghyun Yoo & Jae-Yeol Kim & John M. Louis & Irina V. Gopich & Hoi Sung Chung, 2020. "Fast three-color single-molecule FRET using statistical inference," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    4. Iris V. Hood & Jackson M. Gordon & Charles Bou-Nader & Frances E. Henderson & Soheila Bahmanjah & Jinwei Zhang, 2019. "Crystal structure of an adenovirus virus-associated RNA," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    5. Krishna C. Suddala & Ian R. Price & Shiba S. Dandpat & Michal Janeček & Petra Kührová & Jiří Šponer & Pavel Banáš & Ailong Ke & Nils G. Walter, 2019. "Local-to-global signal transduction at the core of a Mn2+ sensing riboswitch," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    6. Krishna C. Suddala & Javier Cabello-Villegas & Malgorzata Michnicka & Collin Marshall & Edward P. Nikonowicz & Nils G. Walter, 2018. "Hierarchical mechanism of amino acid sensing by the T-box riboswitch," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
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    Cited by:

    1. Eduardo Campos-Chavez & Sneha Paul & Zunwu Zhou & Dulce Alonso & Anjali R. Verma & Jingyi Fei & Alfonso Mondragón, 2024. "Translational T-box riboswitches bind tRNA by modulating conformational flexibility," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. 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.

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