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Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt

Eukaryotic genomes are pervasively transcribed by RNA polymerase II. Yet, the molecular and biological implications of such a phenomenon are still largely puzzling. Here, we describe noncoding RNA transcription upstream of the Arabidopsis thaliana DOG1 gene, which governs salt stress responses and i...

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Autores principales: Montez, Miguel, Majchrowska, Maria, Krzyszton, Michal, Bokota, Grzegorz, Sacharowski, Sebastian, Wrona, Magdalena, Yatusevich, Ruslan, Massana, Ferran, Plewczynski, Dariusz, Swiezewski, Szymon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9975946/
https://www.ncbi.nlm.nih.gov/pubmed/36705062
http://dx.doi.org/10.15252/embj.2022112443
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author Montez, Miguel
Majchrowska, Maria
Krzyszton, Michal
Bokota, Grzegorz
Sacharowski, Sebastian
Wrona, Magdalena
Yatusevich, Ruslan
Massana, Ferran
Plewczynski, Dariusz
Swiezewski, Szymon
author_facet Montez, Miguel
Majchrowska, Maria
Krzyszton, Michal
Bokota, Grzegorz
Sacharowski, Sebastian
Wrona, Magdalena
Yatusevich, Ruslan
Massana, Ferran
Plewczynski, Dariusz
Swiezewski, Szymon
author_sort Montez, Miguel
collection PubMed
description Eukaryotic genomes are pervasively transcribed by RNA polymerase II. Yet, the molecular and biological implications of such a phenomenon are still largely puzzling. Here, we describe noncoding RNA transcription upstream of the Arabidopsis thaliana DOG1 gene, which governs salt stress responses and is a key regulator of seed dormancy. We find that expression of the DOG1 gene is induced by salt stress, thereby causing a delay in seed germination. We uncover extensive transcriptional activity on the promoter of the DOG1 gene, which produces a variety of lncRNAs. These lncRNAs, named PUPPIES, are co‐directionally transcribed and extend into the DOG1 coding region. We show that PUPPIES RNAs respond to salt stress and boost DOG1 expression, resulting in delayed germination. This positive role of pervasive PUPPIES transcription on DOG1 gene expression is associated with augmented pausing of RNA polymerase II, slower transcription and higher transcriptional burst size. These findings highlight the positive role of upstream co‐directional transcription in controlling transcriptional dynamics of downstream genes.
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spelling pubmed-99759462023-03-02 Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt Montez, Miguel Majchrowska, Maria Krzyszton, Michal Bokota, Grzegorz Sacharowski, Sebastian Wrona, Magdalena Yatusevich, Ruslan Massana, Ferran Plewczynski, Dariusz Swiezewski, Szymon EMBO J Articles Eukaryotic genomes are pervasively transcribed by RNA polymerase II. Yet, the molecular and biological implications of such a phenomenon are still largely puzzling. Here, we describe noncoding RNA transcription upstream of the Arabidopsis thaliana DOG1 gene, which governs salt stress responses and is a key regulator of seed dormancy. We find that expression of the DOG1 gene is induced by salt stress, thereby causing a delay in seed germination. We uncover extensive transcriptional activity on the promoter of the DOG1 gene, which produces a variety of lncRNAs. These lncRNAs, named PUPPIES, are co‐directionally transcribed and extend into the DOG1 coding region. We show that PUPPIES RNAs respond to salt stress and boost DOG1 expression, resulting in delayed germination. This positive role of pervasive PUPPIES transcription on DOG1 gene expression is associated with augmented pausing of RNA polymerase II, slower transcription and higher transcriptional burst size. These findings highlight the positive role of upstream co‐directional transcription in controlling transcriptional dynamics of downstream genes. John Wiley and Sons Inc. 2023-01-27 /pmc/articles/PMC9975946/ /pubmed/36705062 http://dx.doi.org/10.15252/embj.2022112443 Text en © 2023 The Authors. Published under the terms of the CC BY 4.0 license https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Montez, Miguel
Majchrowska, Maria
Krzyszton, Michal
Bokota, Grzegorz
Sacharowski, Sebastian
Wrona, Magdalena
Yatusevich, Ruslan
Massana, Ferran
Plewczynski, Dariusz
Swiezewski, Szymon
Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt
title Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt
title_full Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt
title_fullStr Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt
title_full_unstemmed Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt
title_short Promoter‐pervasive transcription causes RNA polymerase II pausing to boost DOG1 expression in response to salt
title_sort promoter‐pervasive transcription causes rna polymerase ii pausing to boost dog1 expression in response to salt
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9975946/
https://www.ncbi.nlm.nih.gov/pubmed/36705062
http://dx.doi.org/10.15252/embj.2022112443
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