Publication Date:
2012-06-23
Description:
Novel protein-coding genes can arise either through re-organization of pre-existing genes or de novo. Processes involving re-organization of pre-existing genes, notably after gene duplication, have been extensively described. In contrast, de novo gene birth remains poorly understood, mainly because translation of sequences devoid of genes, or 'non-genic' sequences, is expected to produce insignificant polypeptides rather than proteins with specific biological functions. Here we formalize an evolutionary model according to which functional genes evolve de novo through transitory proto-genes generated by widespread translational activity in non-genic sequences. Testing this model at the genome scale in Saccharomyces cerevisiae, we detect translation of hundreds of short species-specific open reading frames (ORFs) located in non-genic sequences. These translation events seem to provide adaptive potential, as suggested by their differential regulation upon stress and by signatures of retention by natural selection. In line with our model, we establish that S. cerevisiae ORFs can be placed within an evolutionary continuum ranging from non-genic sequences to genes. We identify ~1,900 candidate proto-genes among S. cerevisiae ORFs and find that de novo gene birth from such a reservoir may be more prevalent than sporadic gene duplication. Our work illustrates that evolution exploits seemingly dispensable sequences to generate adaptive functional innovation.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3401362/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3401362/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Carvunis, Anne-Ruxandra -- Rolland, Thomas -- Wapinski, Ilan -- Calderwood, Michael A -- Yildirim, Muhammed A -- Simonis, Nicolas -- Charloteaux, Benoit -- Hidalgo, Cesar A -- Barbette, Justin -- Santhanam, Balaji -- Brar, Gloria A -- Weissman, Jonathan S -- Regev, Aviv -- Thierry-Mieg, Nicolas -- Cusick, Michael E -- Vidal, Marc -- R01 HG006061/HG/NHGRI NIH HHS/ -- R01-HG006061/HG/NHGRI NIH HHS/ -- Howard Hughes Medical Institute/ -- England -- Nature. 2012 Jul 19;487(7407):370-4. doi: 10.1038/nature11184.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Center for Cancer Systems Biology and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts 02215, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/22722833" target="_blank"〉PubMed〈/a〉
Keywords:
Base Sequence
;
Conserved Sequence
;
*Evolution, Molecular
;
Genes, Fungal/*genetics
;
Genetic Variation
;
Molecular Sequence Data
;
Open Reading Frames
;
Phylogeny
;
Protein Biosynthesis
;
Saccharomyces/classification/*genetics
;
Saccharomyces cerevisiae/classification/genetics
;
Sequence Alignment
Print ISSN:
0028-0836
Electronic ISSN:
1476-4687
Topics:
Biology
,
Chemistry and Pharmacology
,
Medicine
,
Natural Sciences in General
,
Physics
