Visualizing RNA conformational and architectural heterogeneity in solution

Jienyu Ding, Yun-Tzai Lee, Yuba Bhandari, Charles D. Schwieters, Lixin Fan, Ping Yu, Sergey G. Tarosov, Jason R. Stagno, Buyong Ma, Ruth Nussinov, Alan Rein, Jinwei Zhang and Yun-Xing Wang ()
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Jienyu Ding: National Cancer Institute
Yun-Tzai Lee: National Cancer Institute
Yuba Bhandari: National Cancer Institute
Charles D. Schwieters: National Institutes of Health
Lixin Fan: National Institutes of Health
Ping Yu: National Cancer Institute
Sergey G. Tarosov: Center for Structural Biology, National Cancer Institute
Jason R. Stagno: National Cancer Institute
Buyong Ma: National Cancer Institute
Ruth Nussinov: National Cancer Institute
Alan Rein: National Cancer Institute
Jinwei Zhang: National Institute of Diabetes and Digestive and Kidney Diseases
Yun-Xing Wang: National Cancer Institute

Nature Communications, 2023, vol. 14, issue 1, 1-11

Abstract: Abstract RNA flexibility is reflected in its heterogeneous conformation. Through direct visualization using atomic force microscopy (AFM) and the adenosylcobalamin riboswitch aptamer domain as an example, we show that a single RNA sequence folds into conformationally and architecturally heterogeneous structures under near-physiological solution conditions. Recapitulated 3D topological structures from AFM molecular surfaces reveal that all conformers share the same secondary structural elements. Only a population-weighted cohort, not any single conformer, including the crystal structure, can account for the ensemble behaviors observed by small-angle X-ray scattering (SAXS). All conformers except one are functionally active in terms of ligand binding. Our findings provide direct visual evidence that the sequence-structure relationship of RNA under physiologically relevant solution conditions is more complex than the one-to-one relationship for well-structured proteins. The direct visualization of conformational and architectural ensembles at the single-molecule level in solution may suggest new approaches to RNA structural analyses.

Date: 2023
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DOI: 10.1038/s41467-023-36184-x

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