Dynamic light regulation of translation status in Arabidopsis thaliana

Light, a dynamic environmental parameter, is an essential regulator of plant growth and development. Light-regulated transcriptional networks are well documented, whereas light-regulated post-transcriptional regulation has received only limited attention. In this study, dynamics in translation of cy...

Full description

Bibliographic Details
Main Authors: Julia eBailey-Serres, Piyada eJuntawong
Format: Article
Language:English
Published: Frontiers Media S.A. 2012-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2012.00066/full
_version_ 1818081613962018816
author Julia eBailey-Serres
Piyada eJuntawong
author_facet Julia eBailey-Serres
Piyada eJuntawong
author_sort Julia eBailey-Serres
collection DOAJ
description Light, a dynamic environmental parameter, is an essential regulator of plant growth and development. Light-regulated transcriptional networks are well documented, whereas light-regulated post-transcriptional regulation has received only limited attention. In this study, dynamics in translation of cytosolic mRNAs were evaluated at the genome-level in Arabidopsis thaliana seedlings grown under a typical light / dark diurnal regime, shifted to darkness at midday and then re-illuminated. One-hour of unanticipated darkness reduced levels of polyribosomes (polysomes) by 17% in a manner consistent with inhibition of initiation of translation. This down-regulation of protein synthesis was reversed within 10 minutes of re-illumination. Quantitative comparison of the total cellular population of transcripts (the transcriptome) to those associated with one or more 80S ribosome (the translatome) identified over 1600 mRNAs that are differentially translated in response to light availability. Unanticipated darkness limited transcription and translation of mRNAs encoding components of the photosynthetic machinery. Many mRNAs encoding proteins associated with the energy demanding process of protein synthesis were stable but sequestered in the dark, in a rapidly reversible manner. A meta-analysis determined these same transcripts were similarly and coordinately regulated in response to changes in oxygen availability. The dark and hypoxia translationally repressed mRNAs lack highly supported candidate RNA-regulatory elements but are characterized by G+C-rich 5’-untranslated regions. We propose that dynamic regulation of the translational status of a subset of cellular mRNAs serves as a general energy conservation mechanism.
first_indexed 2024-12-10T19:09:00Z
format Article
id doaj.art-7ad085900053445493ba0ef45817760a
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-12-10T19:09:00Z
publishDate 2012-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-7ad085900053445493ba0ef45817760a2022-12-22T01:36:48ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2012-04-01310.3389/fpls.2012.0006620988Dynamic light regulation of translation status in Arabidopsis thalianaJulia eBailey-Serres0Piyada eJuntawong1UC RiversideUC RiversideLight, a dynamic environmental parameter, is an essential regulator of plant growth and development. Light-regulated transcriptional networks are well documented, whereas light-regulated post-transcriptional regulation has received only limited attention. In this study, dynamics in translation of cytosolic mRNAs were evaluated at the genome-level in Arabidopsis thaliana seedlings grown under a typical light / dark diurnal regime, shifted to darkness at midday and then re-illuminated. One-hour of unanticipated darkness reduced levels of polyribosomes (polysomes) by 17% in a manner consistent with inhibition of initiation of translation. This down-regulation of protein synthesis was reversed within 10 minutes of re-illumination. Quantitative comparison of the total cellular population of transcripts (the transcriptome) to those associated with one or more 80S ribosome (the translatome) identified over 1600 mRNAs that are differentially translated in response to light availability. Unanticipated darkness limited transcription and translation of mRNAs encoding components of the photosynthetic machinery. Many mRNAs encoding proteins associated with the energy demanding process of protein synthesis were stable but sequestered in the dark, in a rapidly reversible manner. A meta-analysis determined these same transcripts were similarly and coordinately regulated in response to changes in oxygen availability. The dark and hypoxia translationally repressed mRNAs lack highly supported candidate RNA-regulatory elements but are characterized by G+C-rich 5’-untranslated regions. We propose that dynamic regulation of the translational status of a subset of cellular mRNAs serves as a general energy conservation mechanism.http://journal.frontiersin.org/Journal/10.3389/fpls.2012.00066/fullRibosomal Proteinspost-transcriptional controldark-regulated gene expressionenergy statusLight-regulated gene expressionre-illumination
spellingShingle Julia eBailey-Serres
Piyada eJuntawong
Dynamic light regulation of translation status in Arabidopsis thaliana
Frontiers in Plant Science
Ribosomal Proteins
post-transcriptional control
dark-regulated gene expression
energy status
Light-regulated gene expression
re-illumination
title Dynamic light regulation of translation status in Arabidopsis thaliana
title_full Dynamic light regulation of translation status in Arabidopsis thaliana
title_fullStr Dynamic light regulation of translation status in Arabidopsis thaliana
title_full_unstemmed Dynamic light regulation of translation status in Arabidopsis thaliana
title_short Dynamic light regulation of translation status in Arabidopsis thaliana
title_sort dynamic light regulation of translation status in arabidopsis thaliana
topic Ribosomal Proteins
post-transcriptional control
dark-regulated gene expression
energy status
Light-regulated gene expression
re-illumination
url http://journal.frontiersin.org/Journal/10.3389/fpls.2012.00066/full
work_keys_str_mv AT juliaebaileyserres dynamiclightregulationoftranslationstatusinarabidopsisthaliana
AT piyadaejuntawong dynamiclightregulationoftranslationstatusinarabidopsisthaliana