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Science 24 March 2000:
Vol. 287. no. 5461, pp. 2185 - 2195
DOI: 10.1126/science.287.5461.2185
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Review

The Genome Sequence of Drosophila melanogaster

Mark D. Adams, 1* Susan E. Celniker, 2 Robert A. Holt, 1 Cheryl A. Evans, 1 Jeannine D. Gocayne, 1 Peter G. Amanatides, 1 Steven E. Scherer, 3 Peter W. Li, 1 Roger A. Hoskins, 2 Richard F. Galle, 2 Reed A. George, 2 Suzanna E. Lewis, 4 Stephen Richards, 2 Michael Ashburner, 5 Scott N. Henderson, 1 Granger G. Sutton, 1 Jennifer R. Wortman, 1 Mark D. Yandell, 1 Qing Zhang, 1 Lin X. Chen, 1 Rhonda C. Brandon, 1 Yu-Hui C. Rogers, 1 Robert G. Blazej, 2 Mark Champe, 2 Barret D. Pfeiffer, 2 Kenneth H. Wan, 2 Clare Doyle, 2 Evan G. Baxter, 2 Gregg Helt, 6 Catherine R. Nelson, 4 George L. Gabor Miklos, 7 Josep F. Abril, 8 Anna Agbayani, 2 Hui-Jin An, 1 Cynthia Andrews-Pfannkoch, 1 Danita Baldwin, 1 Richard M. Ballew, 1 Anand Basu, 1 James Baxendale, 1 Leyla Bayraktaroglu, 9 Ellen M. Beasley, 1 Karen Y. Beeson, 1 P. V. Benos, 10 Benjamin P. Berman, 2 Deepali Bhandari, 1 Slava Bolshakov, 11 Dana Borkova, 12 Michael R. Botchan, 13 John Bouck, 3 Peter Brokstein, 4 Phillipe Brottier, 14 Kenneth C. Burtis, 15 Dana A. Busam, 1 Heather Butler, 16 Edouard Cadieu, 17 Angela Center, 1 Ishwar Chandra, 1 J. Michael Cherry, 18 Simon Cawley, 19 Carl Dahlke, 1 Lionel B. Davenport, 1 Peter Davies, 1 Beatriz de Pablos, 20 Arthur Delcher, 1 Zuoming Deng, 1 Anne Deslattes Mays, 1 Ian Dew, 1 Suzanne M. Dietz, 1 Kristina Dodson, 1 Lisa E. Doup, 1 Michael Downes, 21 Shannon Dugan-Rocha, 3 Boris C. Dunkov, 22 Patrick Dunn, 1 Kenneth J. Durbin, 3 Carlos C. Evangelista, 1 Concepcion Ferraz, 23 Steven Ferriera, 1 Wolfgang Fleischmann, 5 Carl Fosler, 1 Andrei E. Gabrielian, 1 Neha S. Garg, 1 William M. Gelbart, 9 Ken Glasser, 1 Anna Glodek, 1 Fangcheng Gong, 1 J. Harley Gorrell, 3 Zhiping Gu, 1 Ping Guan, 1 Michael Harris, 1 Nomi L. Harris, 2 Damon Harvey, 4 Thomas J. Heiman, 1 Judith R. Hernandez, 3 Jarrett Houck, 1 Damon Hostin, 1 Kathryn A. Houston, 2 Timothy J. Howland, 1 Ming-Hui Wei, 1 Chinyere Ibegwam, 1 Mena Jalali, 1 Francis Kalush, 1 Gary H. Karpen, 21 Zhaoxi Ke, 1 James A. Kennison, 24 Karen A. Ketchum, 1 Bruce E. Kimmel, 2 Chinnappa D. Kodira, 1 Cheryl Kraft, 1 Saul Kravitz, 1 David Kulp, 6 Zhongwu Lai, 1 Paul Lasko, 25 Yiding Lei, 1 Alexander A. Levitsky, 1 Jiayin Li, 1 Zhenya Li, 1 Yong Liang, 1 Xiaoying Lin, 26 Xiangjun Liu, 1 Bettina Mattei, 1 Tina C. McIntosh, 1 Michael P. McLeod, 3 Duncan McPherson, 1 Gennady Merkulov, 1 Natalia V. Milshina, 1 Clark Mobarry, 1 Joe Morris, 6 Ali Moshrefi, 2 Stephen M. Mount, 27 Mee Moy, 1 Brian Murphy, 1 Lee Murphy, 28 Donna M. Muzny, 3 David L. Nelson, 3 David R. Nelson, 29 Keith A. Nelson, 1 Katherine Nixon, 2 Deborah R. Nusskern, 1 Joanne M. Pacleb, 2 Michael Palazzolo, 2 Gjange S. Pittman, 1 Sue Pan, 1 John Pollard, 1 Vinita Puri, 1 Martin G. Reese, 4 Knut Reinert, 1 Karin Remington, 1 Robert D. C. Saunders, 30 Frederick Scheeler, 1 Hua Shen, 3 Bixiang Christopher Shue, 1 Inga Sidén-Kiamos, 11 Michael Simpson, 1 Marian P. Skupski, 1 Tom Smith, 1 Eugene Spier, 1 Allan C. Spradling, 31 Mark Stapleton, 2 Renee Strong, 1 Eric Sun, 1 Robert Svirskas, 32 Cyndee Tector, 1 Russell Turner, 1 Eli Venter, 1 Aihui H. Wang, 1 Xin Wang, 1 Zhen-Yuan Wang, 1 David A. Wassarman, 33 George M. Weinstock, 3 Jean Weissenbach, 14 Sherita M. Williams, 1 Trevor Woodage, 1 Kim C. Worley, 3 David Wu, 1 Song Yang, 2 Q. Alison Yao, 1 Jane Ye, 1 Ru-Fang Yeh, 19 Jayshree S. Zaveri, 1 Ming Zhan, 1 Guangren Zhang, 1 Qi Zhao, 1 Liansheng Zheng, 1 Xiangqun H. Zheng, 1 Fei N. Zhong, 1 Wenyan Zhong, 1 Xiaojun Zhou, 3 Shiaoping Zhu, 1 Xiaohong Zhu, 1 Hamilton O. Smith, 1 Richard A. Gibbs, 3 Eugene W. Myers, 1 Gerald M. Rubin, 34 J. Craig Venter 1

The fly Drosophila melanogaster is one of the most intensively studied organisms in biology and serves as a model system for the investigation of many developmental and cellular processes common to higher eukaryotes, including humans. We have determined the nucleotide sequence of nearly all of the ~120-megabase euchromatic portion of the Drosophila genome using a whole-genome shotgun sequencing strategy supported by extensive clone-based sequence and a high-quality bacterial artificial chromosome physical map. Efforts are under way to close the remaining gaps; however, the sequence is of sufficient accuracy and contiguity to be declared substantially complete and to support an initial analysis of genome structure and preliminary gene annotation and interpretation. The genome encodes ~13,600 genes, somewhat fewer than the smaller Caenorhabditis elegans genome, but with comparable functional diversity.

1 Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
2 Berkeley Drosophila Genome Project (BDGP), Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
3 Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
4 BDGP, Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, USA.
5 European Molecular Biology Laboratory (EMBL)-European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
6 Neomorphic Inc., 2612 Eighth Street, Berkeley, CA 94710, USA.
7 GenetixXpress Pty. Ltd., 78 Pacific Road, Palm Beach, Sydney, NSW 2108, Australia.
8 Department of Medical Informatics, IMIM-UPF C/Dr. Aiguader 80, 08003 Barcelona, Spain.
9 Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA.
10 Department of Genetics, Box 8232, Washington University Medical School, 4566 Scott Avenue, St. Louis, MO 63110, USA.
11 Institute of Molecular Biology and Biotechnology, Forth, Heraklion, Greece.
12 European Drosophila Genome Project (EDGP), EMBL, Heidelberg, Germany.
13 Department of Molecular and Cell Biology, University of California, Berkeley, CA 94710, USA.
14 Genoscope, 2 rue Gaston Crémieux, 91000 Evry, France.
15 Section of Molecular and Cellular Biology, University of California, Davis, CA 95618, USA.
16 Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK.
17 EDGP, Rennes University Medical School, UPR 41 CNRS Recombinaisons Genetiques, Faculte de Medicine, 2 av. du Pr. Leon Bernard, 35043 Rennes Cedex, France.
18 Department of Genetics, Stanford University, Palo Alto, CA 94305, USA.
19 Department of Statistics, University of California, Berkeley, CA 94720, USA.
20 EDGP, Centro de Biología Molecular Severo Ochoa, CSIC, Universidad Autónoma de Madrid, 28049 Madrid, Spain.
21 MBVL, Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
22 Department of Biochemistry and Center for Insect Science, University of Arizona, Tucson, AZ 85721, USA.
23 EDGP, Montpellier University Medical School, Institut de Genetique Humaine, CNRS (CRBM), 114 rue de la Cardonille, 34396 Montpellier Cedex 5, France.
24 Laboratory of Molecular Genetics, National Institute of Child Health and Human Development, National Institutes of Health (NIH), Bethesda, MD 20892, USA.
25 Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, Quebec, Canada.
26 The Institute for Genomic Research, Rockville, MD 20850, USA.
27 Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD 20742, USA.
28 EDGP, Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
29 Department of Biochemistry, University of Tennessee, Memphis, TN 38163, USA.
30 EDGP, Department of Anatomy and Physiology, University of Dundee, Dundee DD1 4HN, UK, and Department of Biological Sciences, Open University, Milton Keynes MK7 6AA, UK.
31 HHMI/Embryology, Carnegie Institution of Washington, Baltimore, MD 21210, USA.
32 Motorola BioChip Systems, Tempe, AZ 85284, USA.
33 Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, NIH, Bethesda, MD 20892, USA.
34 Howard Hughes Medical Institute, BDGP, University of California, Berkeley, CA 94720, USA.
*   To whom correspondence should be addressed.

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Bioinformatics 23, 2054-2062
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Global Survey of Human T Leukemic Cells by Integrating Proteomics and Transcriptomics Profiling.
L. Wu, S.-I. Hwang, K. Rezaul, L. J. Lu, V. Mayya, M. Gerstein, J. K. Eng, D. H. Lundgren, and D. K. Han (2007)
Mol. Cell. Proteomics 6, 1343-1353
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Temporal and spatial transcriptional profiles of aging in Drosophila melanogaster.
M. Zhan, H. Yamaza, Y. Sun, J. Sinclair, H. Li, and S. Zou (2007)
Genome Res. 17, 1236-1243
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High-resolution analysis of Drosophila heterochromatin organization using SuUR Su(var)3-9 double mutants.
E. N. Andreyeva, T. D. Kolesnikova, O. V. Demakova, M. Mendez-Lago, G. V. Pokholkova, E. S. Belyaeva, F. Rossi, P. Dimitri, A. Villasante, and I. F. Zhimulev (2007)
PNAS 104, 12819-12824
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Single mage gene in the chicken genome encodes CMage, a protein with functional similarities to mammalian type II Mage proteins.
N. Lopez-Sanchez, Z. Gonzalez-Fernandez, M. Niinobe, K. Yoshikawa, and J. M. Frade (2007)
Physiol Genomics 30, 156-171
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Developmental genomics of the most dangerous animal.
M. P. Scott (2007)
PNAS 104, 11865-11866
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A comprehensive crop genome research project: the Superhybrid Rice Genome Project in China.
J. Yu, G. Ka-Shu Wong, S. Liu, J. Wang, and H. Yang (2007)
Phil Trans R Soc B 362, 1023-1034
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Sequence Finishing and Mapping of Drosophila melanogaster Heterochromatin.
R. A. Hoskins, J. W. Carlson, C. Kennedy, D. Acevedo, M. Evans-Holm, E. Frise, K. H. Wan, S. Park, M. Mendez-Lago, F. Rossi, et al. (2007)
Science 316, 1625-1628
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Prominent use of distal 5' transcription start sites and discovery of a large number of additional exons in ENCODE regions.
F. Denoeud, P. Kapranov, C. Ucla, A. Frankish, R. Castelo, J. Drenkow, J. Lagarde, T. Alioto, C. Manzano, J. Chrast, et al. (2007)
Genome Res. 17, 746-759
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Different Wnt signals act through the Frizzled and RYK receptors during Drosophila salivary gland migration.
K. E. Harris and S. K. Beckendorf (2007)
Development 134, 2017-2025
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Joint Estimates of Quantitative Trait Locus Effect and Frequency Using Synthetic Recombinant Populations of Drosophila melanogaster.
S. J. Macdonald and A. D. Long (2007)
Genetics 176, 1261-1281
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Exceptionally High Density of NUMTs in the Honeybee Genome.
P. Pamilo, L. Viljakainen, and A. Vihavainen (2007)
Mol. Biol. Evol. 24, 1340-1346
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Native Microbial Colonization of Drosophila melanogaster and Its Use as a Model of Enterococcus faecalis Pathogenesis.
C. R. Cox and M. S. Gilmore (2007)
Infect. Immun. 75, 1565-1576
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Cloning of the sea urchin mitochondrial RNA polymerase and reconstitution of the transcription termination system.
P. L. Polosa, S. Deceglie, M. Falkenberg, M. Roberti, B. Di Ponzio, M. N. Gadaleta, and P. Cantatore (2007)
Nucleic Acids Res. 35, 2413-2427
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Misexpression Screen in Drosophila melanogaster Aiming to Reveal Novel Factors Involved in Formation of Body Parts.
N. C. Grieder, I. Charlafti, U. Kloter, H. Jackle, U. Schafer, and W. J. Gehring (2007)
Genetics 175, 1707-1718
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Localization and Characterization of X Chromosome Inversion Breakpoints Separating Drosophila mojavensis and Drosophila arizonae.
E. T. Cirulli and M. A. F. Noor (2007)
J. Hered. 98, 111-114
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