Trans-splicing of mRNAs links gene transcription to translational control regulated by mTOR

In phylogenetically diverse organisms, the 5’ ends of a subset of mRNAs are trans -spliced with a spliced leader (SL) RNA. The functions of SL trans -splicing, however, remain largely enigmatic. Here, we quantified translation genome-wide in the marine chordate, Oikopleura dioica , under inhibition of mTOR, a central growth regulator. Translation of trans -spliced TOP mRNAs was suppressed, showing that the SL sequence permits nutrient-dependent translational control of growth-related mRNAs. Under crowded, nutrient-limiting conditions, O. dioica continues to filter-feed, but arrests growth until favorable conditions return. Upon release from such conditions, initial recovery was independent of nutrient-responsive, trans -spliced genes, suggesting animal density sensing as a first trigger for resumption of development. Our results demonstrate a role for trans -splicing in the coordinated translational down-regulation of nutrient-responsive genes under limiting conditions.