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Increased sucrose levels mediate selective mRNA translation in Arabidopsis

BACKGROUND: Protein synthesis is a highly energy demanding process and is regulated according to cellular energy levels. Light and sugar availability affect mRNA translation in plant cells but the specific roles of these factors remain unclear. In this study, sucrose was applied to Arabidopsis seedl...

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Autores principales: Gamm, Magdalena, Peviani, Alessia, Honsel, Anne, Snel, Berend, Smeekens, Sjef, Hanson, Johannes
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4252027/
https://www.ncbi.nlm.nih.gov/pubmed/25403240
http://dx.doi.org/10.1186/s12870-014-0306-3
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author Gamm, Magdalena
Peviani, Alessia
Honsel, Anne
Snel, Berend
Smeekens, Sjef
Hanson, Johannes
author_facet Gamm, Magdalena
Peviani, Alessia
Honsel, Anne
Snel, Berend
Smeekens, Sjef
Hanson, Johannes
author_sort Gamm, Magdalena
collection PubMed
description BACKGROUND: Protein synthesis is a highly energy demanding process and is regulated according to cellular energy levels. Light and sugar availability affect mRNA translation in plant cells but the specific roles of these factors remain unclear. In this study, sucrose was applied to Arabidopsis seedlings kept in the light or in the dark, in order to distinguish sucrose and light effects on transcription and translation. These were studied using microarray analysis of steady-state mRNA and mRNA bound to translating ribosomes. RESULTS: Steady-state mRNA levels were affected differently by sucrose in the light and in the dark but general translation increased to a similar extent in both conditions. For a majority of the transcripts changes of the transcript levels were followed by changes in polysomal mRNA levels. However, for 243 mRNAs, a change in polysomal occupancy (defined as polysomal levels related to steady-state levels of the mRNA) was observed after sucrose treatment in the light, but not in the dark condition. Many of these mRNAs are annotated as encoding ribosomal proteins, supporting specific translational regulation of this group of transcripts. Unexpectedly, the numbers of ribosomes bound to each mRNA decreased for mRNAs with increased polysomal occupancy. CONCLUSIONS: Our results suggest that sucrose regulate translation of these 243 mRNAs specifically in the light, through a novel regulatory mechanism. Our data shows that increased polysomal occupancy is not necessarily leading to more ribosomes per transcript, suggesting a mechanism of translational induction not solely dependent on increased translation initiation rates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0306-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-42520272014-12-03 Increased sucrose levels mediate selective mRNA translation in Arabidopsis Gamm, Magdalena Peviani, Alessia Honsel, Anne Snel, Berend Smeekens, Sjef Hanson, Johannes BMC Plant Biol Research Article BACKGROUND: Protein synthesis is a highly energy demanding process and is regulated according to cellular energy levels. Light and sugar availability affect mRNA translation in plant cells but the specific roles of these factors remain unclear. In this study, sucrose was applied to Arabidopsis seedlings kept in the light or in the dark, in order to distinguish sucrose and light effects on transcription and translation. These were studied using microarray analysis of steady-state mRNA and mRNA bound to translating ribosomes. RESULTS: Steady-state mRNA levels were affected differently by sucrose in the light and in the dark but general translation increased to a similar extent in both conditions. For a majority of the transcripts changes of the transcript levels were followed by changes in polysomal mRNA levels. However, for 243 mRNAs, a change in polysomal occupancy (defined as polysomal levels related to steady-state levels of the mRNA) was observed after sucrose treatment in the light, but not in the dark condition. Many of these mRNAs are annotated as encoding ribosomal proteins, supporting specific translational regulation of this group of transcripts. Unexpectedly, the numbers of ribosomes bound to each mRNA decreased for mRNAs with increased polysomal occupancy. CONCLUSIONS: Our results suggest that sucrose regulate translation of these 243 mRNAs specifically in the light, through a novel regulatory mechanism. Our data shows that increased polysomal occupancy is not necessarily leading to more ribosomes per transcript, suggesting a mechanism of translational induction not solely dependent on increased translation initiation rates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0306-3) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-18 /pmc/articles/PMC4252027/ /pubmed/25403240 http://dx.doi.org/10.1186/s12870-014-0306-3 Text en © Gamm et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Gamm, Magdalena
Peviani, Alessia
Honsel, Anne
Snel, Berend
Smeekens, Sjef
Hanson, Johannes
Increased sucrose levels mediate selective mRNA translation in Arabidopsis
title Increased sucrose levels mediate selective mRNA translation in Arabidopsis
title_full Increased sucrose levels mediate selective mRNA translation in Arabidopsis
title_fullStr Increased sucrose levels mediate selective mRNA translation in Arabidopsis
title_full_unstemmed Increased sucrose levels mediate selective mRNA translation in Arabidopsis
title_short Increased sucrose levels mediate selective mRNA translation in Arabidopsis
title_sort increased sucrose levels mediate selective mrna translation in arabidopsis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4252027/
https://www.ncbi.nlm.nih.gov/pubmed/25403240
http://dx.doi.org/10.1186/s12870-014-0306-3
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