Cargando…

Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection

Viral infections impose extraordinary RNA stress, triggering cellular RNA surveillance pathways such as RNA decapping, nonsense-mediated decay, and RNA silencing. Viruses need to maneuver among these pathways to establish infection and succeed in producing high amounts of viral proteins. Processing...

Descripción completa

Detalles Bibliográficos
Autores principales: Hoffmann, Gesa, Mahboubi, Amir, Bente, Heinrich, Garcia, Damien, Hanson, Johannes, Hafrén, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9338796/
https://www.ncbi.nlm.nih.gov/pubmed/35511183
http://dx.doi.org/10.1093/plcell/koac132
_version_ 1784760046125580288
author Hoffmann, Gesa
Mahboubi, Amir
Bente, Heinrich
Garcia, Damien
Hanson, Johannes
Hafrén, Anders
author_facet Hoffmann, Gesa
Mahboubi, Amir
Bente, Heinrich
Garcia, Damien
Hanson, Johannes
Hafrén, Anders
author_sort Hoffmann, Gesa
collection PubMed
description Viral infections impose extraordinary RNA stress, triggering cellular RNA surveillance pathways such as RNA decapping, nonsense-mediated decay, and RNA silencing. Viruses need to maneuver among these pathways to establish infection and succeed in producing high amounts of viral proteins. Processing bodies (PBs) are integral to RNA triage in eukaryotic cells, with several distinct RNA quality control pathways converging for selective RNA regulation. In this study, we investigated the role of Arabidopsis thaliana PBs during Cauliflower mosaic virus (CaMV) infection. We found that several PB components are co-opted into viral factories that support virus multiplication. This pro-viral role was not associated with RNA decay pathways but instead, we established that PB components are helpers in viral RNA translation. While CaMV is normally resilient to RNA silencing, dysfunctions in PB components expose the virus to this pathway, which is similar to previous observations for transgenes. Transgenes, however, undergo RNA quality control-dependent RNA degradation and transcriptional silencing, whereas CaMV RNA remains stable but becomes translationally repressed through decreased ribosome association, revealing a unique dependence among PBs, RNA silencing, and translational repression. Together, our study shows that PB components are co-opted by the virus to maintain efficient translation, a mechanism not associated with canonical PB functions.
format Online
Article
Text
id pubmed-9338796
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-93387962022-08-01 Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection Hoffmann, Gesa Mahboubi, Amir Bente, Heinrich Garcia, Damien Hanson, Johannes Hafrén, Anders Plant Cell Research Articles Viral infections impose extraordinary RNA stress, triggering cellular RNA surveillance pathways such as RNA decapping, nonsense-mediated decay, and RNA silencing. Viruses need to maneuver among these pathways to establish infection and succeed in producing high amounts of viral proteins. Processing bodies (PBs) are integral to RNA triage in eukaryotic cells, with several distinct RNA quality control pathways converging for selective RNA regulation. In this study, we investigated the role of Arabidopsis thaliana PBs during Cauliflower mosaic virus (CaMV) infection. We found that several PB components are co-opted into viral factories that support virus multiplication. This pro-viral role was not associated with RNA decay pathways but instead, we established that PB components are helpers in viral RNA translation. While CaMV is normally resilient to RNA silencing, dysfunctions in PB components expose the virus to this pathway, which is similar to previous observations for transgenes. Transgenes, however, undergo RNA quality control-dependent RNA degradation and transcriptional silencing, whereas CaMV RNA remains stable but becomes translationally repressed through decreased ribosome association, revealing a unique dependence among PBs, RNA silencing, and translational repression. Together, our study shows that PB components are co-opted by the virus to maintain efficient translation, a mechanism not associated with canonical PB functions. Oxford University Press 2022-05-02 /pmc/articles/PMC9338796/ /pubmed/35511183 http://dx.doi.org/10.1093/plcell/koac132 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Hoffmann, Gesa
Mahboubi, Amir
Bente, Heinrich
Garcia, Damien
Hanson, Johannes
Hafrén, Anders
Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection
title Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection
title_full Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection
title_fullStr Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection
title_full_unstemmed Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection
title_short Arabidopsis RNA processing body components LSM1 and DCP5 aid in the evasion of translational repression during Cauliflower mosaic virus infection
title_sort arabidopsis rna processing body components lsm1 and dcp5 aid in the evasion of translational repression during cauliflower mosaic virus infection
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9338796/
https://www.ncbi.nlm.nih.gov/pubmed/35511183
http://dx.doi.org/10.1093/plcell/koac132
work_keys_str_mv AT hoffmanngesa arabidopsisrnaprocessingbodycomponentslsm1anddcp5aidintheevasionoftranslationalrepressionduringcauliflowermosaicvirusinfection
AT mahboubiamir arabidopsisrnaprocessingbodycomponentslsm1anddcp5aidintheevasionoftranslationalrepressionduringcauliflowermosaicvirusinfection
AT benteheinrich arabidopsisrnaprocessingbodycomponentslsm1anddcp5aidintheevasionoftranslationalrepressionduringcauliflowermosaicvirusinfection
AT garciadamien arabidopsisrnaprocessingbodycomponentslsm1anddcp5aidintheevasionoftranslationalrepressionduringcauliflowermosaicvirusinfection
AT hansonjohannes arabidopsisrnaprocessingbodycomponentslsm1anddcp5aidintheevasionoftranslationalrepressionduringcauliflowermosaicvirusinfection
AT hafrenanders arabidopsisrnaprocessingbodycomponentslsm1anddcp5aidintheevasionoftranslationalrepressionduringcauliflowermosaicvirusinfection