Abstract
BackgroundProtein 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.ResultsSteady-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.ConclusionsOur 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 materialThe online version of this article (doi:10.1186/s12870-014-0306-3) contains supplementary material, which is available to authorized users.
Highlights
Protein synthesis is a highly energy demanding process and is regulated according to cellular energy levels
Sucrose treatments were applied to Arabidopsis seedlings both in the dark and in the light in order to uncouple the effects of sucrose and light on translation
We identified 243 genes with altered polysomal occupancy following sucrose treatment in the light and 12 genes affected by sucrose treatment in the dark, with 7 genes found under both conditions
Summary
Protein synthesis is a highly energy demanding process and is regulated according to cellular energy levels. Some mRNAs escape this general stress mediated reduction of translation and maintain or increase polysomal occupancy, ensuring the production of proteins necessary for adaptation. Such translational control is essential for the plant’s response to stress and adds another layer to the regulation of gene expression [13,14]. The results presented here suggest that light acts as additional factor necessary for sucrose-induced expression of cytoplasmic ribosomal protein genes. Sucrose treatment alone is sufficient to induce a general increase in translation concurrent with changes in transcription, whereas light as an additional factor seems necessary to mediate the specific increase of polysomal occupancy
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