Reconceptualizing transcriptional slippage in plant RNA viruses

RNA viruses have evolved sophisticated strategies to exploit the limited encoded information within their typically compact genomes. One of them, named transcriptional slippage (TS), is characterized by the appearance of indels in nascent viral RNAs, leading to changes in the open reading frame (ORF...

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Autores: Valli, Adrián A.|||0000-0002-3266-7200, Domingo Calap, María Luisa|||0000-0003-0900-7850, González de Prádena, Alfonso, García, Juan Antonio|||0000-0002-4861-9609, Cui, Hongguang|||0000-0001-9770-6621, Desbiez, Cécile, Lopez-Moya, Juan Jose|||0000-0002-3176-9651
Tipo de recurso: artículo
Fecha de publicación:2024
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:319961
Acceso en línea:https://ddd.uab.cat/record/319961
https://dx.doi.org/urn:doi:10.1128/mbio.02120-24
Access Level:acceso abierto
Palabra clave:RNA virus
RNA polymerases
Evolution
Potyviridae
Ebola virus
Plant viruses
Polymerase slippage
Transcriptional slippage
Overlapping ORFs
RNA replication
Viral replication
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spelling Reconceptualizing transcriptional slippage in plant RNA virusesValli, Adrián A.|||0000-0002-3266-7200Domingo Calap, María Luisa|||0000-0003-0900-7850González de Prádena, AlfonsoGarcía, Juan Antonio|||0000-0002-4861-9609Cui, Hongguang|||0000-0001-9770-6621Desbiez, CécileLopez-Moya, Juan Jose|||0000-0002-3176-9651RNA virusRNA polymerasesEvolutionPotyviridaeEbola virusPlant virusesPolymerase slippageTranscriptional slippageOverlapping ORFsRNA replicationViral replicationRNA viruses have evolved sophisticated strategies to exploit the limited encoded information within their typically compact genomes. One of them, named transcriptional slippage (TS), is characterized by the appearance of indels in nascent viral RNAs, leading to changes in the open reading frame (ORF). Although members of unrelated viral families express key proteins via TS, the available information about this phenomenon is still limited. In potyvirids (members of the Potyviridae family), TS has been defined by the insertion of an additional A at An motifs (n ≥ 6) in newly synthesized transcripts at a low frequency, modulated by nucleotides flanking the A-rich motif. Here, by using diverse experimental approaches and a collection of plant/virus combinations, we discover cases not following this definition. In summary, we observe (i) a high rate of single-nucleotide deletions at slippage motifs, (ii) overlapping ORFs acceded by slippage at an U8 stretch, and (iii) changes in slippage rates induced by factors not related to cognate viruses. Moreover, a survey of whole-genome sequences from potyvirids shows a widespread occurrence of species-specific An/Un (n ≥ 6) motifs. Even though many of them, but not all, lead to the production of truncated proteins rather than access to overlapping ORFs, these results suggest that slippage motifs appear more frequently than expected and play relevant roles during virus evolution. Considering the potential of this phenomenon to expand the viral proteome by acceding to overlapping ORFs and/or producing truncated proteins, a re-evaluation of TS significance during infections of RNA viruses is required. 22024-01-0120242024-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/319961https://dx.doi.org/urn:doi:10.1128/mbio.02120-24reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengMinisterio de Economía y Competitividad https://doi.org/10.13039/501100003329 BIO2015-73900-JINAgencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2019-110979RB-I00Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2019-105692RB-I00Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139314OB-I00Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139376OB-C33Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-138530OB-I00Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 SEV-2015-0533Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 CEX2019-000902-SMinisterio de Economía y Competitividad https://doi.org/10.13039/501100003329 BES-2014-068970open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, fins i tot amb finalitats comercials, sempre i quan es reconegui l'autoria de l'obra original.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:3199612026-06-06T12:50:31Z
dc.title.none.fl_str_mv Reconceptualizing transcriptional slippage in plant RNA viruses
title Reconceptualizing transcriptional slippage in plant RNA viruses
spellingShingle Reconceptualizing transcriptional slippage in plant RNA viruses
Valli, Adrián A.|||0000-0002-3266-7200
RNA virus
RNA polymerases
Evolution
Potyviridae
Ebola virus
Plant viruses
Polymerase slippage
Transcriptional slippage
Overlapping ORFs
RNA replication
Viral replication
title_short Reconceptualizing transcriptional slippage in plant RNA viruses
title_full Reconceptualizing transcriptional slippage in plant RNA viruses
title_fullStr Reconceptualizing transcriptional slippage in plant RNA viruses
title_full_unstemmed Reconceptualizing transcriptional slippage in plant RNA viruses
title_sort Reconceptualizing transcriptional slippage in plant RNA viruses
dc.creator.none.fl_str_mv Valli, Adrián A.|||0000-0002-3266-7200
Domingo Calap, María Luisa|||0000-0003-0900-7850
González de Prádena, Alfonso
García, Juan Antonio|||0000-0002-4861-9609
Cui, Hongguang|||0000-0001-9770-6621
Desbiez, Cécile
Lopez-Moya, Juan Jose|||0000-0002-3176-9651
author Valli, Adrián A.|||0000-0002-3266-7200
author_facet Valli, Adrián A.|||0000-0002-3266-7200
Domingo Calap, María Luisa|||0000-0003-0900-7850
González de Prádena, Alfonso
García, Juan Antonio|||0000-0002-4861-9609
Cui, Hongguang|||0000-0001-9770-6621
Desbiez, Cécile
Lopez-Moya, Juan Jose|||0000-0002-3176-9651
author_role author
author2 Domingo Calap, María Luisa|||0000-0003-0900-7850
González de Prádena, Alfonso
García, Juan Antonio|||0000-0002-4861-9609
Cui, Hongguang|||0000-0001-9770-6621
Desbiez, Cécile
Lopez-Moya, Juan Jose|||0000-0002-3176-9651
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv RNA virus
RNA polymerases
Evolution
Potyviridae
Ebola virus
Plant viruses
Polymerase slippage
Transcriptional slippage
Overlapping ORFs
RNA replication
Viral replication
topic RNA virus
RNA polymerases
Evolution
Potyviridae
Ebola virus
Plant viruses
Polymerase slippage
Transcriptional slippage
Overlapping ORFs
RNA replication
Viral replication
description RNA viruses have evolved sophisticated strategies to exploit the limited encoded information within their typically compact genomes. One of them, named transcriptional slippage (TS), is characterized by the appearance of indels in nascent viral RNAs, leading to changes in the open reading frame (ORF). Although members of unrelated viral families express key proteins via TS, the available information about this phenomenon is still limited. In potyvirids (members of the Potyviridae family), TS has been defined by the insertion of an additional A at An motifs (n ≥ 6) in newly synthesized transcripts at a low frequency, modulated by nucleotides flanking the A-rich motif. Here, by using diverse experimental approaches and a collection of plant/virus combinations, we discover cases not following this definition. In summary, we observe (i) a high rate of single-nucleotide deletions at slippage motifs, (ii) overlapping ORFs acceded by slippage at an U8 stretch, and (iii) changes in slippage rates induced by factors not related to cognate viruses. Moreover, a survey of whole-genome sequences from potyvirids shows a widespread occurrence of species-specific An/Un (n ≥ 6) motifs. Even though many of them, but not all, lead to the production of truncated proteins rather than access to overlapping ORFs, these results suggest that slippage motifs appear more frequently than expected and play relevant roles during virus evolution. Considering the potential of this phenomenon to expand the viral proteome by acceding to overlapping ORFs and/or producing truncated proteins, a re-evaluation of TS significance during infections of RNA viruses is required.
publishDate 2024
dc.date.none.fl_str_mv 2
2024-01-01
2024
2024-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/319961
https://dx.doi.org/urn:doi:10.1128/mbio.02120-24
url https://ddd.uab.cat/record/319961
https://dx.doi.org/urn:doi:10.1128/mbio.02120-24
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 BIO2015-73900-JIN
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2019-110979RB-I00
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2019-105692RB-I00
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139314OB-I00
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139376OB-C33
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-138530OB-I00
Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 SEV-2015-0533
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 CEX2019-000902-S
Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 BES-2014-068970
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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