When translation elongation is impaired, the mRNA is uniformly destabilized by the RNA degradosome, while the concentration of mRNA is altered along the molecule

mRNA sits at the crossroads of transcription, translation and mRNA degradation. Many questions remain about the coupling of these three processes in Escherichia coli and, in particular, how translation may have an effect on mRNA degradation and transcription. To characterize the interplay between mRNA degradation and translation while accounting for transcription, we altered the translation initiation or elongation and measured the effects on mRNA stability and concentration. Using a mapping method, we analysed mRNA concentration and stability at the local scale all along the transcript. We showed that a decrease in translation initiation efficiency destabilizes the mRNA and leads to a uniform decrease in mRNA concentration throughout the molecule. Prematurely terminating translation elongation by inserting a stop codon is associated with a drop in local mRNA concentration downstream of the stop codon, due to the uncoupling of transcription and translation. In contrast, this translation alteration uniformly destabilizes the coding and ribosome-free regions, in a process triggered by RNase E activity, and its ability to form the RNA degradome. These results demonstrate how ribosomes protect mRNA molecules and highlight how translation, mRNA degradation and transcription are deeply interconnected in the quality control process that avoids unproductive gene expression in cells.

Automated summary

mRNA plays a crucial role in the interplay of transcription, translation and mRNA degradation. This study investigates the impact of translation on mRNA stability and concentration by manipulating translation initiation and elongation. The results show that a decrease in translation initiation efficiency leads to mRNA destabilization and uniform reduction in mRNA concentration throughout the molecule. Premature termination of translation elongation results in localized decrease in mRNA concentration downstream of the stop codon, due to the decoupling of transcription and translation. These findings highlight the interconnectedness of translation, mRNA degradation and transcription in maintaining gene expression quality control.