From RNA World to SARS-CoV-2: The Edited Story of RNA Viral Evolution

Overview

Journal Cells

Publisher MDPI

Specialties Biochemistry
Biophysics
Cell Biology
Molecular Biology

Date 2021 Jul 2

PMID 34202997

Citations 15

Authors

Zachary W Kockler

Dmitry A Gordenin

Affiliations

Soon will be listed here.

Abstract

The current SARS-CoV-2 pandemic underscores the importance of understanding the evolution of RNA genomes. While RNA is subject to the formation of similar lesions as DNA, the evolutionary and physiological impacts RNA lesions have on viral genomes are yet to be characterized. Lesions that may drive the evolution of RNA genomes can induce breaks that are repaired by recombination or can cause base substitution mutagenesis, also known as base editing. Over the past decade or so, base editing mutagenesis of DNA genomes has been subject to many studies, revealing that exposure of ssDNA is subject to hypermutation that is involved in the etiology of cancer. However, base editing of RNA genomes has not been studied to the same extent. Recently hypermutation of single-stranded RNA viral genomes have also been documented though its role in evolution and population dynamics. Here, we will summarize the current knowledge of key mechanisms and causes of RNA genome instability covering areas from the RNA world theory to the SARS-CoV-2 pandemic of today. We will also highlight the key questions that remain as it pertains to RNA genome instability, mutations accumulation, and experimental strategies for addressing these questions.

Citing Articles

Topologically constrained DNA-mediated one-pot CRISPR assay for rapid detection of viral RNA with single nucleotide resolution.

Li Y, Xu R, Quan F, Wu Y, Wu Y, Zhang Y EBioMedicine. 2025; 112:105564.

PMID: 39862805 PMC: 11873568. DOI: 10.1016/j.ebiom.2025.105564.

Analysis of the abundance and diversity of RNA secondary structure elements in RNA viruses using the RNAsselem Python package.

Kazanov F, Matveev E, Ponomarev G, Ivankov D, Kazanov M Sci Rep. 2024; 14(1):28587.

PMID: 39562668 PMC: 11577020. DOI: 10.1038/s41598-024-80240-5.

Inactivation of highly transmissible livestock and avian viruses including influenza A and Newcastle disease virus for molecular diagnostics.

Welch J, Shrestha R, Hutchings H, Pal N, Levings R, Robbe-Austerman S Front Vet Sci. 2024; 11:1304022.

PMID: 38515532 PMC: 10955088. DOI: 10.3389/fvets.2024.1304022.

The role of post-transcriptional regulation in SARS-CoV-2 infection and pathogenicity.

Wang X, Chang Z, Zhao T, Zhong W, Shi J, Wang G Front Immunol. 2023; 14:1256574.

PMID: 38035086 PMC: 10684767. DOI: 10.3389/fimmu.2023.1256574.

Differential RNA editing landscapes in host cell versus the SARS-CoV-2 genome.

Kurkowiak M, Fletcher S, Daniels A, Mozolewski P, Silvestris D, Krol E iScience. 2023; 26(11):108031.

PMID: 37876814 PMC: 10590966. DOI: 10.1016/j.isci.2023.108031.

References

Courtney D, Chalem A, Bogerd H, Law B, Kennedy E, Holley C . Extensive Epitranscriptomic Methylation of A and C Residues on Murine Leukemia Virus Transcripts Enhances Viral Gene Expression. mBio. 2019; 10(3). PMC: 6561033. DOI: 10.1128/mBio.01209-19. View

Fornes J, Lazaro J, Alarcon T, Elena S, Sardanyes J . Viral replication modes in single-peak fitness landscapes: A dynamical systems analysis. J Theor Biol. 2018; 460:170-183. DOI: 10.1016/j.jtbi.2018.10.007. View

Domingo E, Perales C . Viral quasispecies. PLoS Genet. 2019; 15(10):e1008271. PMC: 6797082. DOI: 10.1371/journal.pgen.1008271. View

Robertson M, Joyce G . The origins of the RNA world. Cold Spring Harb Perspect Biol. 2010; 4(5). PMC: 3331698. DOI: 10.1101/cshperspect.a003608. View

Jalili P, Bowen D, Langenbucher A, Park S, Aguirre K, Corcoran R . Quantification of ongoing APOBEC3A activity in tumor cells by monitoring RNA editing at hotspots. Nat Commun. 2020; 11(1):2971. PMC: 7293259. DOI: 10.1038/s41467-020-16802-8. View

Bradrick S . Causes and Consequences of Flavivirus RNA Methylation. Front Microbiol. 2017; 8:2374. PMC: 5723295. DOI: 10.3389/fmicb.2017.02374. View

Roberts S, Lawrence M, Klimczak L, Grimm S, Fargo D, Stojanov P . An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet. 2013; 45(9):970-6. PMC: 3789062. DOI: 10.1038/ng.2702. View

Azgari C, Kilinc Z, Turhan B, Circi D, Adebali O . The Mutation Profile of SARS-CoV-2 Is Primarily Shaped by the Host Antiviral Defense. Viruses. 2021; 13(3). PMC: 7999997. DOI: 10.3390/v13030394. View

Wilkinson M, Charenton C, Nagai K . RNA Splicing by the Spliceosome. Annu Rev Biochem. 2019; 89:359-388. DOI: 10.1146/annurev-biochem-091719-064225. View

10.

Pfeiffer J, Kirkegaard K . A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc Natl Acad Sci U S A. 2003; 100(12):7289-94. PMC: 165868. DOI: 10.1073/pnas.1232294100. View

11.

Sankaran N . The RNA World at Thirty: A Look Back with its Author. J Mol Evol. 2016; 83(5-6):169-175. DOI: 10.1007/s00239-016-9767-3. View

12.

Riva L, Pandiri A, Li Y, Droop A, Hewinson J, Quail M . The mutational signature profile of known and suspected human carcinogens in mice. Nat Genet. 2020; 52(11):1189-1197. PMC: 7610456. DOI: 10.1038/s41588-020-0692-4. View

13.

Woodman A, Arnold J, Cameron C, Evans D . Biochemical and genetic analysis of the role of the viral polymerase in enterovirus recombination. Nucleic Acids Res. 2016; 44(14):6883-95. PMC: 5001610. DOI: 10.1093/nar/gkw567. View

14.

Schaefer M . The Regulation of RNA Modification Systems: The Next Frontier in Epitranscriptomics?. Genes (Basel). 2021; 12(3). PMC: 7996938. DOI: 10.3390/genes12030345. View

15.

Saini N, Sterling J, Sakofsky C, Giacobone C, Klimczak L, Burkholder A . Mutation signatures specific to DNA alkylating agents in yeast and cancers. Nucleic Acids Res. 2020; 48(7):3692-3707. PMC: 7144945. DOI: 10.1093/nar/gkaa150. View

16.

Eckerle L, Becker M, Halpin R, Li K, Venter E, Lu X . Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog. 2010; 6(5):e1000896. PMC: 2865531. DOI: 10.1371/journal.ppat.1000896. View

17.

Vaisman A, Woodgate R . Translesion DNA polymerases in eukaryotes: what makes them tick?. Crit Rev Biochem Mol Biol. 2017; 52(3):274-303. PMC: 5573590. DOI: 10.1080/10409238.2017.1291576. View

18.

Snijder E, Bredenbeek P, Dobbe J, Thiel V, Ziebuhr J, Poon L . Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J Mol Biol. 2003; 331(5):991-1004. PMC: 7159028. DOI: 10.1016/s0022-2836(03)00865-9. View

19.

Binh N, Wakai C, Kawaguchi A, Nagata K . Involvement of the N-terminal portion of influenza virus RNA polymerase subunit PB1 in nucleotide recognition. Biochem Biophys Res Commun. 2013; 443(3):975-9. DOI: 10.1016/j.bbrc.2013.12.071. View

20.

Wu T, Orgel L . Nonenzymatic template-directed synthesis on oligodeoxycytidylate sequences in hairpin oligonucleotides. J Am Chem Soc. 1992; 114(1):317-22. DOI: 10.1021/ja00027a040. View