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Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells

Stem cells are essential for the development and organ regeneration of multicellular organisms, so their infection by pathogenic viruses must be prevented. Accordingly, mammalian stem cells are highly resistant to viral infection due to dedicated antiviral pathways including RNA interference (RNAi)....

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Autores principales: Incarbone, Marco, Bradamante, Gabriele, Pruckner, Florian, Wegscheider, Tobias, Rozhon, Wilfried, Nguyen, Vu, Gutzat, Ruben, Mérai, Zsuzsanna, Lendl, Thomas, MacFarlane, Stuart, Nodine, Michael, Scheid, Ortrun Mittelsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10589665/
https://www.ncbi.nlm.nih.gov/pubmed/37824524
http://dx.doi.org/10.1073/pnas.2302069120
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author Incarbone, Marco
Bradamante, Gabriele
Pruckner, Florian
Wegscheider, Tobias
Rozhon, Wilfried
Nguyen, Vu
Gutzat, Ruben
Mérai, Zsuzsanna
Lendl, Thomas
MacFarlane, Stuart
Nodine, Michael
Scheid, Ortrun Mittelsten
author_facet Incarbone, Marco
Bradamante, Gabriele
Pruckner, Florian
Wegscheider, Tobias
Rozhon, Wilfried
Nguyen, Vu
Gutzat, Ruben
Mérai, Zsuzsanna
Lendl, Thomas
MacFarlane, Stuart
Nodine, Michael
Scheid, Ortrun Mittelsten
author_sort Incarbone, Marco
collection PubMed
description Stem cells are essential for the development and organ regeneration of multicellular organisms, so their infection by pathogenic viruses must be prevented. Accordingly, mammalian stem cells are highly resistant to viral infection due to dedicated antiviral pathways including RNA interference (RNAi). In plants, a small group of stem cells harbored within the shoot apical meristem generate all postembryonic above-ground tissues, including the germline cells. Many viruses do not proliferate in these cells, yet the molecular bases of this exclusion remain only partially understood. Here, we show that a plant-encoded RNA-dependent RNA polymerase, after activation by the plant hormone salicylic acid, amplifies antiviral RNAi in infected tissues. This provides stem cells with RNA-based virus sequence information, which prevents virus proliferation. Furthermore, we find RNAi to be necessary for stem cell exclusion of several unrelated RNA viruses, despite their ability to efficiently suppress RNAi in the rest of the plant. This work elucidates a molecular pathway of great biological and economic relevance and lays the foundations for our future understanding of the unique systems underlying stem cell immunity.
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spelling pubmed-105896652023-10-22 Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells Incarbone, Marco Bradamante, Gabriele Pruckner, Florian Wegscheider, Tobias Rozhon, Wilfried Nguyen, Vu Gutzat, Ruben Mérai, Zsuzsanna Lendl, Thomas MacFarlane, Stuart Nodine, Michael Scheid, Ortrun Mittelsten Proc Natl Acad Sci U S A Biological Sciences Stem cells are essential for the development and organ regeneration of multicellular organisms, so their infection by pathogenic viruses must be prevented. Accordingly, mammalian stem cells are highly resistant to viral infection due to dedicated antiviral pathways including RNA interference (RNAi). In plants, a small group of stem cells harbored within the shoot apical meristem generate all postembryonic above-ground tissues, including the germline cells. Many viruses do not proliferate in these cells, yet the molecular bases of this exclusion remain only partially understood. Here, we show that a plant-encoded RNA-dependent RNA polymerase, after activation by the plant hormone salicylic acid, amplifies antiviral RNAi in infected tissues. This provides stem cells with RNA-based virus sequence information, which prevents virus proliferation. Furthermore, we find RNAi to be necessary for stem cell exclusion of several unrelated RNA viruses, despite their ability to efficiently suppress RNAi in the rest of the plant. This work elucidates a molecular pathway of great biological and economic relevance and lays the foundations for our future understanding of the unique systems underlying stem cell immunity. National Academy of Sciences 2023-10-12 2023-10-17 /pmc/articles/PMC10589665/ /pubmed/37824524 http://dx.doi.org/10.1073/pnas.2302069120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Incarbone, Marco
Bradamante, Gabriele
Pruckner, Florian
Wegscheider, Tobias
Rozhon, Wilfried
Nguyen, Vu
Gutzat, Ruben
Mérai, Zsuzsanna
Lendl, Thomas
MacFarlane, Stuart
Nodine, Michael
Scheid, Ortrun Mittelsten
Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells
title Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells
title_full Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells
title_fullStr Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells
title_full_unstemmed Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells
title_short Salicylic acid and RNA interference mediate antiviral immunity of plant stem cells
title_sort salicylic acid and rna interference mediate antiviral immunity of plant stem cells
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10589665/
https://www.ncbi.nlm.nih.gov/pubmed/37824524
http://dx.doi.org/10.1073/pnas.2302069120
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