Article (Scientific journals)
Proto-genes and de novo gene birth
Carvunis, A.-R.; Rolland, T.; Wapinski, I. et al.
2012In Nature, 487 (7407), p. 370-374
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Keywords :
RNA translation; Saccharomyces cerevisiae; Base Sequence; Conserved Sequence; Evolution, Molecular; Genes, Fungal; Genetic Variation; Molecular Sequence Data; Open Reading Frames; Phylogeny; Protein Biosynthesis; Saccharomyces; Sequence Alignment
Abstract :
[en] 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. © 2012 Macmillan Publishers Limited. All rights reserved.
Disciplines :
Genetics & genetic processes
Author, co-author :
Carvunis, A.-R.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States, UJF-Grenoble 1/CNRS/TIMC-IMAG UMR 5525, Computational and Mathematical Biology Group, Grenoble F-38041, France
Rolland, T.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States
Wapinski, I.;  Department of Systems Biology, Harvard Medical School, Boston, MA 02115, United States
Calderwood, M. A.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States
Yildirim, M. A.;  Center for International Development, Harvard University, Cambridge, MA 02138, United States
Simonis, N.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States, Laboratoire de Bioinformatique des Génomes et des Réseaux (BiGRe), Campus Plaine, Free University of Brussels, 1050 Brussels, Wallonia-Brussels Federation, Belgium
CHARLOTEAUX, Benoit ;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States, Unit of Animal Genomics, GIGA-R and Faculty of Veterinary Medicine, University of Liege, 4000 Liege, Wallonia-Brussels Federation, Belgium.
Hidalgo, C. A.;  MIT Media Lab, Massachusetts Institute of Technology, Cambridge, MA 02142, United States
Barbette, J.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States
Santhanam, B.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States
Brar, G. A.;  Howard Hughes Medical Institute, Department of Cellular and Molecular Pharmacology, University of California San Francisco, San Francisco, CA 94158, United States
Weissman, J. S.;  Howard Hughes Medical Institute, Department of Cellular and Molecular Pharmacology, University of California San Francisco, San Francisco, CA 94158, United States
Regev, A.;  Broad Institute of MIT and Harvard, Cambridge, MA 02142, United States, Howard Hughes Medical Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, United States
Thierry-Mieg, N.;  UJF-Grenoble 1/CNRS/TIMC-IMAG UMR 5525, Computational and Mathematical Biology Group, Grenoble F-38041, France
Cusick, M. E.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States
Vidal, M.;  Center for Cancer Systems Biology (CCSB), Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, United States, Department of Genetics, Harvard Medical School, Boston, MA 02115, United States
More authors (6 more) Less
Language :
English
Title :
Proto-genes and de novo gene birth
Publication date :
2012
Journal title :
Nature
ISSN :
0028-0836
eISSN :
1476-4687
Publisher :
Nature Publishing Group, London, United Kingdom
Volume :
487
Issue :
7407
Pages :
370-374
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
R01-HG006061, 117945-PF-09-136-01-RMC
Funders :
BWF - Burroughs Wellcome Fund [US-NC] [US-NC]
HHMI - Howard Hughes Medical Institute [US-MD] [US-MD]
Damon Runyon Cancer Research Foundation [US-NY] [US-NY]
ACS - American Cancer Society [US-GA] [US-GA]
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
NHGRI - National Human Genome Research Institute [US-MD] [US-MD]
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