Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures

Alexander Stark, Michael F. Lin, Pouya Kheradpour, Jakob S. Pedersen, Leopold Parts, Joseph W. Carlson, Madeline A. Crosby, Matthew D. Rasmussen, Sushmita Roy, Ameya N. Deoras, J. Graham Ruby, Julius Brennecke, Emily Hodges, Angie S. Hinrichs, Anat Caspi, Benedict Paten, Seung-Won Park, Mira V. Han, Morgan L. Maeder, Benjamin J. Polansky, Bryanne E. Robson, Stein Aerts, Jacques van Helden, Bassem Hassan, Donald G. Gilbert, Deborah A. Eastman, Michael Rice, Michael Weir, Matthew W. Hahn, Yongkyu Park, Colin N. Dewey, Lior Pachter, W. James Kent, David Haussler, Eric C. Lai, David P. Bartel, Gregory J. Hannon, Thomas C. Kaufman, Michael B. Eisen, Andrew G. Clark, Douglas Smith, Susan E. Celniker, William M. Gelbart and Manolis Kellis ()
Additional contact information
Alexander Stark: The Broad Institute, Massachusetts Institute of Technology and Harvard University, Cambridge, Massachusetts 02140, USA
Michael F. Lin: The Broad Institute, Massachusetts Institute of Technology and Harvard University, Cambridge, Massachusetts 02140, USA
Pouya Kheradpour: Computer Science and Artificial Intelligence Laboratory, MIT, Cambridge, Massachusetts 02139, USA
Jakob S. Pedersen: The Bioinformatics Centre, University of Copenhagen, Ole Maaloes Vej 5, 2200 Copenhagen N, Denmark
Leopold Parts: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK
Joseph W. Carlson: BDGP, LBNL, 1 Cyclotron Road MS 64-0119, Berkeley, California 94720, USA
Madeline A. Crosby: FlyBase, The Biological Laboratories, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA
Matthew D. Rasmussen: Computer Science and Artificial Intelligence Laboratory, MIT, Cambridge, Massachusetts 02139, USA
Sushmita Roy: University of New Mexico, Albuquerque, New Mexico 87131, USA
Ameya N. Deoras: Computer Science and Artificial Intelligence Laboratory, MIT, Cambridge, Massachusetts 02139, USA
J. Graham Ruby: MIT, Cambridge, Massachusetts 02139, USA
Julius Brennecke: Cold Spring Harbor Laboratory, Watson School of Biological Sciences, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA
Emily Hodges: Cold Spring Harbor Laboratory, Watson School of Biological Sciences, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA
Angie S. Hinrichs: Center for Biomolecular Science and Engineering, University of California, Santa Cruz, California 95064, USA
Anat Caspi: University of California, San Francisco/University of California, Berkeley Joint Graduate Group in Bioengineering, Berkeley, California 97210, USA
Benedict Paten: Center for Biomolecular Science and Engineering, University of California, Santa Cruz, California 95064, USA
Seung-Won Park: G-629, MSB, 185 South Orange Avenue, UMDNJ-New Jersey Medical School, Newark, New Jersey 07103, USA
Mira V. Han: Indiana University
Morgan L. Maeder: Connecticut College, New London, Connecticut 06320, USA
Benjamin J. Polansky: Connecticut College, New London, Connecticut 06320, USA
Bryanne E. Robson: Connecticut College, New London, Connecticut 06320, USA
Stein Aerts: Laboratory of Neurogenetics, VIB, 3000 Leuven, Belgium
Jacques van Helden: Universite Libre de Bruxelles
Bassem Hassan: Laboratory of Neurogenetics, VIB, 3000 Leuven, Belgium
Donald G. Gilbert: Indiana University, Bloomington, Indiana 47405, USA
Deborah A. Eastman: Connecticut College, New London, Connecticut 06320, USA
Michael Rice: Wesleyan University, Middletown, Connecticut 06459, USA
Michael Weir: Wesleyan University Middletown
Matthew W. Hahn: Indiana University
Yongkyu Park: G-629, MSB, 185 South Orange Avenue, UMDNJ-New Jersey Medical School, Newark, New Jersey 07103, USA
Colin N. Dewey: University of Wisconsin-Madison, Madison, Wisconsin 53706, USA
Lior Pachter: University of California at Berkeley, Berkeley, California 94720, USA
W. James Kent: Center for Biomolecular Science and Engineering, University of California, Santa Cruz, California 95064, USA
David Haussler: Center for Biomolecular Science and Engineering, University of California, Santa Cruz, California 95064, USA
Eric C. Lai: Memorial Sloan-Kettering Cancer Center, New York, New York 10021, USA
David P. Bartel: MIT, Cambridge, Massachusetts 02139, USA
Gregory J. Hannon: Cold Spring Harbor Laboratory, Watson School of Biological Sciences, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA
Thomas C. Kaufman: Indiana University, Bloomington, Indiana 47405, USA
Michael B. Eisen: Graduate Group in Biophysics, and Center for Integrative Genomics, University of California, Berkeley, California 94720, USA
Andrew G. Clark: Cornell University, Ithaca, New York 14853, USA
Douglas Smith: Agencourt Bioscience Corporation, 500 Cummings Center, Suite 2450, Beverly, Massachusetts 01915, USA
Susan E. Celniker: BDGP, LBNL, 1 Cyclotron Road MS 64-0119, Berkeley, California 94720, USA
William M. Gelbart: FlyBase, The Biological Laboratories, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA
Manolis Kellis: The Broad Institute, Massachusetts Institute of Technology and Harvard University, Cambridge, Massachusetts 02140, USA

Nature, 2007, vol. 450, issue 7167, 219-232

Abstract: Abstract Sequencing of multiple related species followed by comparative genomics analysis constitutes a powerful approach for the systematic understanding of any genome. Here, we use the genomes of 12 Drosophila species for the de novo discovery of functional elements in the fly. Each type of functional element shows characteristic patterns of change, or ‘evolutionary signatures’, dictated by its precise selective constraints. Such signatures enable recognition of new protein-coding genes and exons, spurious and incorrect gene annotations, and numerous unusual gene structures, including abundant stop-codon readthrough. Similarly, we predict non-protein-coding RNA genes and structures, and new microRNA (miRNA) genes. We provide evidence of miRNA processing and functionality from both hairpin arms and both DNA strands. We identify several classes of pre- and post-transcriptional regulatory motifs, and predict individual motif instances with high confidence. We also study how discovery power scales with the divergence and number of species compared, and we provide general guidelines for comparative studies.

Date: 2007
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DOI: 10.1038/nature06340

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