Translational contributions to tissue specificity in rhythmic and constitutive gene expression

Jun 18, 2017Genome biology

How protein-making processes shape tissue-specific daily and constant gene activity

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Circadian Biology on OpenScience ↗PubMed ↗DOI ↗

Abstract

Rhythmic translation of messenger RNAs in kidney shows distinct patterns compared to liver.

Non-overlapping sets of transcripts exhibit distinct phase clustering in kidney and liver.
Tissue-specific translation efficiency influences the timing and quantity of protein production from rhythmic messenger RNAs.
Translation efficiency differences between tissues are smaller than mRNA abundance variations.
Specific features of transcripts are associated with tissue-specific changes in translation efficiency.
Overall protein biosynthesis is more similar between organs due to translational compensation for transcript abundance differences.

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BACKGROUND: The daily gene expression oscillations that underlie mammalian circadian rhythms show striking differences between tissues and involve post-transcriptional regulation. Both aspects remain poorly understood. We have used ribosome profiling to explore the contribution of translation efficiency to temporal gene expression in kidney and contrasted our findings with liver data available from the same mice.

RESULTS: Rhythmic translation of constantly abundant messenger RNAs (mRNAs) affects largely non-overlapping transcript sets with distinct phase clustering in the two organs. Moreover, tissue differences in translation efficiency modulate the timing and amount of protein biosynthesis from rhythmic mRNAs, consistent with organ specificity in clock output gene repertoires and rhythmicity parameters. Our comprehensive datasets provided insights into translational control beyond temporal regulation. Between tissues, many transcripts show differences in translation efficiency, which are, however, of markedly smaller scale than mRNA abundance differences. Tissue-specific changes in translation efficiency are associated with specific transcript features and, intriguingly, globally counteracted and compensated transcript abundance variations, leading to higher similarity at the level of protein biosynthesis between both tissues.

CONCLUSIONS: We show that tissue specificity in rhythmic gene expression extends to the translatome and contributes to define the identities, the phases and the expression levels of rhythmic protein biosynthesis. Moreover, translational compensation of transcript abundance divergence leads to overall higher similarity at the level of protein production across organs. The unique resources provided through our study will serve to address fundamental questions of post-transcriptional control and differential gene expression in vivo.

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Translational contributions to tissue specificity in rhythmic and constitutive gene expression

Abstract

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