Cargando…
The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant
BACKGROUND: Genome-wide assays performed in Arabidopsis and other organisms have revealed that the translation status of mRNAs responds dramatically to different environmental stresses and genetic lesions in the translation apparatus. To identify additional features of the global landscape of transl...
Autores principales: | , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2013
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3901033/ https://www.ncbi.nlm.nih.gov/pubmed/24377433 http://dx.doi.org/10.1186/1741-7007-11-123 |
_version_ | 1782300792658591744 |
---|---|
author | Tiruneh, Bayu Sisay Kim, Byung-Hoon Gallie, Daniel R Roy, Bijoyita von Arnim, Albrecht G |
author_facet | Tiruneh, Bayu Sisay Kim, Byung-Hoon Gallie, Daniel R Roy, Bijoyita von Arnim, Albrecht G |
author_sort | Tiruneh, Bayu Sisay |
collection | PubMed |
description | BACKGROUND: Genome-wide assays performed in Arabidopsis and other organisms have revealed that the translation status of mRNAs responds dramatically to different environmental stresses and genetic lesions in the translation apparatus. To identify additional features of the global landscape of translational control, we used microarray analysis of polysomal as well as non-polysomal mRNAs to examine the defects in translation in a poly(A) binding protein mutant, pab2 pab8, as well as in a mutant of a large ribosomal subunit protein, rpl24b/shortvalve1. RESULTS: The mutation of RPL24B stimulated the ribosome occupancy of mRNAs for nuclear encoded ribosomal proteins. Detailed analysis yielded new insights into the translational regulon containing the ribosomal protein mRNAs. First, the ribosome occupancy defects in the rpl24b mutant partially overlapped with those in a previously analyzed initiation factor mutant, eif3h. Second, a group of mRNAs with incomplete coding sequences appeared to be uncoupled from the regulon, since their dependence on RPL24B differed from regular mRNAs. Third, different sister paralogs of the ribosomal proteins differed in their translation state in the wild-type. Some sister paralogs also differed in their response to the rpl24b mutation. In contrast to rpl24b, the pab2 pab8 mutant revealed few gene specific translational defects, but a group of seed storage protein mRNAs were stimulated in their ribosome occupancy. In the course of this work, while optimizing the statistical analysis of ribosome occupancy data, we collected 12 biological replicates of translation states from wild-type seedlings. We defined 20% of mRNAs as having a high variance in their translation state. Many of these mRNAs were functionally associated with responses to the environment, suggesting that subtle variation in the environmental conditions is sensed by plants and transduced to affect the translational efficiency of hundreds of mRNAs. CONCLUSIONS: These data represent the first genome-wide analysis of translation in a eukaryote defective in the large ribosomal subunit. RPL24 and eIF3h play similar but non-identical roles in eukaryotic translation. The data also shed light on the fine structure of the regulon of ribosomal protein mRNAs. |
format | Online Article Text |
id | pubmed-3901033 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-39010332014-01-25 The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant Tiruneh, Bayu Sisay Kim, Byung-Hoon Gallie, Daniel R Roy, Bijoyita von Arnim, Albrecht G BMC Biol Research Article BACKGROUND: Genome-wide assays performed in Arabidopsis and other organisms have revealed that the translation status of mRNAs responds dramatically to different environmental stresses and genetic lesions in the translation apparatus. To identify additional features of the global landscape of translational control, we used microarray analysis of polysomal as well as non-polysomal mRNAs to examine the defects in translation in a poly(A) binding protein mutant, pab2 pab8, as well as in a mutant of a large ribosomal subunit protein, rpl24b/shortvalve1. RESULTS: The mutation of RPL24B stimulated the ribosome occupancy of mRNAs for nuclear encoded ribosomal proteins. Detailed analysis yielded new insights into the translational regulon containing the ribosomal protein mRNAs. First, the ribosome occupancy defects in the rpl24b mutant partially overlapped with those in a previously analyzed initiation factor mutant, eif3h. Second, a group of mRNAs with incomplete coding sequences appeared to be uncoupled from the regulon, since their dependence on RPL24B differed from regular mRNAs. Third, different sister paralogs of the ribosomal proteins differed in their translation state in the wild-type. Some sister paralogs also differed in their response to the rpl24b mutation. In contrast to rpl24b, the pab2 pab8 mutant revealed few gene specific translational defects, but a group of seed storage protein mRNAs were stimulated in their ribosome occupancy. In the course of this work, while optimizing the statistical analysis of ribosome occupancy data, we collected 12 biological replicates of translation states from wild-type seedlings. We defined 20% of mRNAs as having a high variance in their translation state. Many of these mRNAs were functionally associated with responses to the environment, suggesting that subtle variation in the environmental conditions is sensed by plants and transduced to affect the translational efficiency of hundreds of mRNAs. CONCLUSIONS: These data represent the first genome-wide analysis of translation in a eukaryote defective in the large ribosomal subunit. RPL24 and eIF3h play similar but non-identical roles in eukaryotic translation. The data also shed light on the fine structure of the regulon of ribosomal protein mRNAs. BioMed Central 2013-12-30 /pmc/articles/PMC3901033/ /pubmed/24377433 http://dx.doi.org/10.1186/1741-7007-11-123 Text en Copyright © 2013 Tiruneh et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Tiruneh, Bayu Sisay Kim, Byung-Hoon Gallie, Daniel R Roy, Bijoyita von Arnim, Albrecht G The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant |
title | The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant |
title_full | The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant |
title_fullStr | The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant |
title_full_unstemmed | The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant |
title_short | The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant |
title_sort | global translation profile in a ribosomal protein mutant resembles that of an eif3 mutant |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3901033/ https://www.ncbi.nlm.nih.gov/pubmed/24377433 http://dx.doi.org/10.1186/1741-7007-11-123 |
work_keys_str_mv | AT tirunehbayusisay theglobaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT kimbyunghoon theglobaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT galliedanielr theglobaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT roybijoyita theglobaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT vonarnimalbrechtg theglobaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT tirunehbayusisay globaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT kimbyunghoon globaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT galliedanielr globaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT roybijoyita globaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant AT vonarnimalbrechtg globaltranslationprofileinaribosomalproteinmutantresemblesthatofaneif3mutant |