Diversity in pervasive translation. A new translational landscape of yeast.

Pervasive translation is a widespread phenomenon that plays an important role in de novo gene birth; however, its underlying mechanisms remain unclear. Based on multiple Ribosome Profiling datasets, we investigated the translational landscape of coding and noncoding regions of yeast. Therefore, we developed a new representation framework which allows the visual and comprehensive representation of the diversity of translation behaviors in yeast coding and noncoding regions. We show that if coding regions are restricted to specific regions of the translation landscape, noncoding regions are associated with a wide diversity of translation behaviors and, in contrast, populate the entire yeast translational landscape. In particular, we reveal that noncoding regions are associated with canonical translation signals but also with novel categories of translation events absent from coding regions, and which seem to be a hallmark of pervasive translation. Notably, we report thousands of translated noncoding ORFs among which, 256 led to detectable products with Mass Spectrometry while being characterized by canonical but also non-canonical translation signals. Finally, we show that the translation behavior of noncoding ORFs is not explained by features related to the emergence of function, but is rather determined by the translation start codon and the codon distribution in the three competing RNA frames. Overall, our results enable us to propose a topology of the pervasive translation landscape of a species, and open the way to future comparative analyses of this translation landscape under different conditions.