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

Krishna C. Suddala, Janghyun Yoo, Lixin Fan, Xiaobing Zuo, Yun-Xing Wang, Hoi Sung Chung () and Jinwei Zhang ()
Additional contact information
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
Hoi Sung Chung: National Institute of Diabetes and Digestive and Kidney Diseases
Jinwei Zhang: National Institute of Diabetes and Digestive and Kidney Diseases

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41155-3

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