Alternative splicing can generate multiple differently spliced transcripts from a single pre-mRNA. A striking number of coding genes have alternatively spliced transcripts with splice events that change the reading frame. In fact, more than a third are annotated with dual coding regions that are derived from alternative splicing and that can be read in two or more coding frames. We analysed 535 dual coding regions with reading frames that are supported by either peptide or conservation evidence. These dual coding regions produce protein isoforms with completely different C-terminals. More than a quarter of the alternative reading frames are preserved across all mammals, and many can be traced back to the earliest jawed vertebrates so are among the oldest known alternative splicing events. Most ancient dual coding regions appear to be under selective constraints; there is support for purifying selection on both frames in 104 pairs of transcripts. Two genes, CCSER2 and SH2B1, have triple coding regions that are under clear selection pressure in all three frames. We found evidence to suggest that ancient dual coding regions may have played important roles in the evolution of the vertebrate central nervous system. Most ancient dual coding regions that had evidence for tissue specificity at the protein level were brain specific and their genes are highly enriched in brain tissues, particularly cerebellum and cerebral cortex. Most remarkably, we found that more than 80% of genes with ancient dual coding regions are involved in neuron development, synapses and neural cell projections.
Tress, M. L., Cerdan-Velez, D., Maquedano, M., Abascal, F.
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