Abstract
Recent evidence demonstrates that novel protein-coding genes can arise de novo from non-genic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of non-genic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Here, we systematically characterize how these de novo emerging coding sequences impact fitness in budding yeast. Disruption of emerging sequences is generally inconsequential for fitness in the laboratory and in natural populations. Overexpression of emerging sequences, however, is enriched in adaptive fitness effects compared to overexpression of established genes. We find that adaptive emerging sequences tend to encode putative transmembrane domains, and that thymine-rich intergenic regions harbor a widespread potential to produce transmembrane domains. These findings, together with in-depth examination of the de novo emerging YBR196C-A locus, suggest a novel evolutionary model whereby adaptive transmembrane polypeptides emerge de novo from thymine-rich non-genic regions and subsequently accumulate changes molded by natural selection.
Highlights
Recent evidence demonstrates that novel protein-coding genes can arise de novo from nongenic loci
The proto-gene model is supported by several studies which reported that de novo emerging coding sequences tend to display features intermediate between those observed in non-genic sequences and those observed in established genes; these features include length, transcript architecture, transcription level, strength of purifying selection, sequence composition, structural properties and integration in cellular networks[3,5,6,7,8,9]
Two criteria were considered to determine the emergence status of open reading frames (ORFs): whether they appeared to be emerging de novo, and whether they appeared to encode a useful protein product under selective constraints
Summary
Recent evidence demonstrates that novel protein-coding genes can arise de novo from nongenic loci. Pervasive translation of non-genic sequences has been observed repeatedly by ribosome profiling and proteo-genomics[3,10,11,12,13], and studies have shown that random sequence libraries can form defined secondary structures and harbor bioactive effects[14,15,16,17,18,19] It remains unknown if, how, how often, and how rapidly, may native proto-genes accumulate adaptive fitness-enhancing changes to become established genes. Our results support an experiential model for de novo gene birth whereby a fraction of incipient proto-genes can subsequently mature and, as adaptive changes engender novel selected effects, progressively become established in genomes in a species-specific manner
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