Universality in RNA and DNA deformations induced by salt, temperature change, stretching force, and protein binding

Author:

Tian Fu-Jia123ORCID,Zhang Chen1ORCID,Zhou Erchi1ORCID,Dong Hai-Long4,Tan Zhi-Jie4,Zhang Xing-Hua1ORCID,Dai Liang23ORCID

Affiliation:

1. Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Renmin Hospital of Wuhan University, Wuhan University, Wuhan 430072, China

2. Department of Physics, City University of Hong Kong, Hong Kong 999077, China

3. Shenzhen Research Institute, City University of Hong Kong, Shenzhen 518057, China

4. School of Physics and Technology, Wuhan University, Wuhan 430072, China

Abstract

Nucleic acid deformations play important roles in many biological processes. The physical understanding of nucleic acid deformation by environmental stimuli is limited due to the challenge in the precise measurement of RNA and DNA deformations and the complexity of interactions in RNA and DNA. Magnetic tweezers experiments provide an excellent opportunity to precisely measure DNA and RNA twist changes induced by environmental stimuli. In this work, we applied magnetic tweezers to measure double-stranded RNA twist changes induced by salt and temperature changes. We observed RNA unwinds when lowering salt concentration, or increasing temperature. Our molecular dynamics simulations revealed the mechanism: lowering salt concentration or increasing temperature enlarges RNA major groove width, which causes twist decrease through twist-groove coupling. Combining these results with previous results, we found some universality in RNA and DNA deformations induced by three different stimuli: salt change, temperature, and stretching force. For RNA, these stimuli first modify the major groove width, which is transduced into twist change through twist-groove coupling. For DNA, these stimuli first modify diameter, which is transduced into twist change through twist-diameter coupling. Twist-groove coupling and twist-diameter coupling appear to be utilized by protein binding to reduce DNA and RNA deformation energy cost upon protein binding.

Funder

MOST | National Natural Science Foundation of China

Research Grants Council, University Grants Committee

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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