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Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana
The reprogramming of gene expression in heat stress is a key determinant to organism survival. Gene expression is downregulated through translation initiation inhibition and release of free mRNPs that are rapidly degraded or stored. In mammals, heat also triggers 5′-ribosome pausing preferentially o...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4417158/ https://www.ncbi.nlm.nih.gov/pubmed/25845591 http://dx.doi.org/10.1093/nar/gkv234 |
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author | Merret, Rémy Nagarajan, Vinay K. Carpentier, Marie-Christine Park, Sunhee Favory, Jean-Jacques Descombin, Julie Picart, Claire Charng, Yee-yung Green, Pamela J. Deragon, Jean-Marc Bousquet-Antonelli, Cécile |
author_facet | Merret, Rémy Nagarajan, Vinay K. Carpentier, Marie-Christine Park, Sunhee Favory, Jean-Jacques Descombin, Julie Picart, Claire Charng, Yee-yung Green, Pamela J. Deragon, Jean-Marc Bousquet-Antonelli, Cécile |
author_sort | Merret, Rémy |
collection | PubMed |
description | The reprogramming of gene expression in heat stress is a key determinant to organism survival. Gene expression is downregulated through translation initiation inhibition and release of free mRNPs that are rapidly degraded or stored. In mammals, heat also triggers 5′-ribosome pausing preferentially on transcripts coding for HSC/HSP70 chaperone targets, but the impact of such phenomenon on mRNA fate remains unknown. Here, we provide evidence that, in Arabidopsis thaliana, heat provokes 5′-ribosome pausing leading to the XRN4-mediated 5′-directed decay of translating mRNAs. We also show that hindering HSC/HSP70 activity at 20°C recapitulates heat effects by inducing ribosome pausing and co-translational mRNA turnover. Strikingly, co-translational decay targets encode proteins with high HSC/HSP70 binding scores and hydrophobic N-termini, two characteristics that were previously observed for transcripts most prone to pausing in animals. This work suggests for the first time that stress-induced variation of translation elongation rate is an evolutionarily conserved process leading to the polysomal degradation of thousands of ‘non-aberrant’ mRNAs. |
format | Online Article Text |
id | pubmed-4417158 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-44171582015-05-12 Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana Merret, Rémy Nagarajan, Vinay K. Carpentier, Marie-Christine Park, Sunhee Favory, Jean-Jacques Descombin, Julie Picart, Claire Charng, Yee-yung Green, Pamela J. Deragon, Jean-Marc Bousquet-Antonelli, Cécile Nucleic Acids Res Molecular Biology The reprogramming of gene expression in heat stress is a key determinant to organism survival. Gene expression is downregulated through translation initiation inhibition and release of free mRNPs that are rapidly degraded or stored. In mammals, heat also triggers 5′-ribosome pausing preferentially on transcripts coding for HSC/HSP70 chaperone targets, but the impact of such phenomenon on mRNA fate remains unknown. Here, we provide evidence that, in Arabidopsis thaliana, heat provokes 5′-ribosome pausing leading to the XRN4-mediated 5′-directed decay of translating mRNAs. We also show that hindering HSC/HSP70 activity at 20°C recapitulates heat effects by inducing ribosome pausing and co-translational mRNA turnover. Strikingly, co-translational decay targets encode proteins with high HSC/HSP70 binding scores and hydrophobic N-termini, two characteristics that were previously observed for transcripts most prone to pausing in animals. This work suggests for the first time that stress-induced variation of translation elongation rate is an evolutionarily conserved process leading to the polysomal degradation of thousands of ‘non-aberrant’ mRNAs. Oxford University Press 2015-04-30 2015-04-06 /pmc/articles/PMC4417158/ /pubmed/25845591 http://dx.doi.org/10.1093/nar/gkv234 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Molecular Biology Merret, Rémy Nagarajan, Vinay K. Carpentier, Marie-Christine Park, Sunhee Favory, Jean-Jacques Descombin, Julie Picart, Claire Charng, Yee-yung Green, Pamela J. Deragon, Jean-Marc Bousquet-Antonelli, Cécile Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana |
title | Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana |
title_full | Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana |
title_fullStr | Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana |
title_full_unstemmed | Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana |
title_short | Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana |
title_sort | heat-induced ribosome pausing triggers mrna co-translational decay in arabidopsis thaliana |
topic | Molecular Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4417158/ https://www.ncbi.nlm.nih.gov/pubmed/25845591 http://dx.doi.org/10.1093/nar/gkv234 |
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