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Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes

BACKGROUND: RNA viruses possess remarkable evolutionary versatility driven by the high mutability of their genomes. Frameshifting nucleotide insertions or deletions (indels), which cause the premature termination of proteins, are frequently observed in the coding sequences of various viral genomes....

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Autores principales: Park, Dongbin, Hahn, Yoonsoo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8127213/
https://www.ncbi.nlm.nih.gov/pubmed/34000995
http://dx.doi.org/10.1186/s12859-021-04182-9
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author Park, Dongbin
Hahn, Yoonsoo
author_facet Park, Dongbin
Hahn, Yoonsoo
author_sort Park, Dongbin
collection PubMed
description BACKGROUND: RNA viruses possess remarkable evolutionary versatility driven by the high mutability of their genomes. Frameshifting nucleotide insertions or deletions (indels), which cause the premature termination of proteins, are frequently observed in the coding sequences of various viral genomes. When a secondary indel occurs near the primary indel site, the open reading frame can be restored to produce functional proteins, a phenomenon known as the compensatory frameshift. RESULTS: In this study, we systematically analyzed publicly available viral genome sequences and identified compensatory frameshift events in hundreds of viral protein-coding sequences. Compensatory frameshift events resulted in large-scale amino acid differences between the compensatory frameshift form and the wild type even though their nucleotide sequences were almost identical. Phylogenetic analyses revealed that the evolutionary distance between proteins with and without a compensatory frameshift were significantly overestimated because amino acid mismatches caused by compensatory frameshifts were counted as substitutions. Further, this could cause compensatory frameshift forms to branch in different locations in the protein and nucleotide trees, which may obscure the correct interpretation of phylogenetic relationships between variant viruses. CONCLUSIONS: Our results imply that the compensatory frameshift is one of the mechanisms driving the rapid protein evolution of RNA viruses and potentially assisting their host-range expansion and adaptation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12859-021-04182-9.
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spelling pubmed-81272132021-05-17 Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes Park, Dongbin Hahn, Yoonsoo BMC Bioinformatics Research BACKGROUND: RNA viruses possess remarkable evolutionary versatility driven by the high mutability of their genomes. Frameshifting nucleotide insertions or deletions (indels), which cause the premature termination of proteins, are frequently observed in the coding sequences of various viral genomes. When a secondary indel occurs near the primary indel site, the open reading frame can be restored to produce functional proteins, a phenomenon known as the compensatory frameshift. RESULTS: In this study, we systematically analyzed publicly available viral genome sequences and identified compensatory frameshift events in hundreds of viral protein-coding sequences. Compensatory frameshift events resulted in large-scale amino acid differences between the compensatory frameshift form and the wild type even though their nucleotide sequences were almost identical. Phylogenetic analyses revealed that the evolutionary distance between proteins with and without a compensatory frameshift were significantly overestimated because amino acid mismatches caused by compensatory frameshifts were counted as substitutions. Further, this could cause compensatory frameshift forms to branch in different locations in the protein and nucleotide trees, which may obscure the correct interpretation of phylogenetic relationships between variant viruses. CONCLUSIONS: Our results imply that the compensatory frameshift is one of the mechanisms driving the rapid protein evolution of RNA viruses and potentially assisting their host-range expansion and adaptation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12859-021-04182-9. BioMed Central 2021-05-17 /pmc/articles/PMC8127213/ /pubmed/34000995 http://dx.doi.org/10.1186/s12859-021-04182-9 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Park, Dongbin
Hahn, Yoonsoo
Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes
title Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes
title_full Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes
title_fullStr Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes
title_full_unstemmed Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes
title_short Rapid protein sequence evolution via compensatory frameshift is widespread in RNA virus genomes
title_sort rapid protein sequence evolution via compensatory frameshift is widespread in rna virus genomes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8127213/
https://www.ncbi.nlm.nih.gov/pubmed/34000995
http://dx.doi.org/10.1186/s12859-021-04182-9
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