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Science 4 October 2002:
Vol. 298. no. 5591, pp. 129 - 149
DOI: 10.1126/science.1076181
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Research Articles

The Genome Sequence of the Malaria Mosquito Anopheles gambiae

Robert A. Holt,1*dagger G. Mani Subramanian,1 Aaron Halpern,1 Granger G. Sutton,1 Rosane Charlab,1 Deborah R. Nusskern,1 Patrick Wincker,2 Andrew G. Clark,3 José M. C. Ribeiro,4 Ron Wides,5 Steven L. Salzberg,6 Brendan Loftus,6 Mark Yandell,1 William H. Majoros,16 Douglas B. Rusch,1 Zhongwu Lai,1 Cheryl L. Kraft,1 Josep F. Abril,7 Veronique Anthouard,2 Peter Arensburger,8 Peter W. Atkinson,8 Holly Baden,1 Veronique de Berardinis,2 Danita Baldwin,1 Vladimir Benes,9 Jim Biedler,10 Claudia Blass,9 Randall Bolanos,1 Didier Boscus,2 Mary Barnstead,1 Shuang Cai,1 Angela Center,1 Kabir Chatuverdi,1 George K. Christophides,9 Mathew A. Chrystal,11 Michele Clamp,12 Anibal Cravchik,1 Val Curwen,12 Ali Dana,11 Art Delcher,1 Ian Dew,1 Cheryl A. Evans,1 Michael Flanigan,1 Anne Grundschober-Freimoser,13 Lisa Friedli,8 Zhiping Gu,1 Ping Guan,1 Roderic Guigo,7 Maureen E. Hillenmeyer,11 Susanne L. Hladun,1 James R. Hogan,11 Young S. Hong,11 Jeffrey Hoover,1 Olivier Jaillon,2 Zhaoxi Ke,111 Chinnappa Kodira,1 Elena Kokoza,14 Anastasios Koutsos,1516 Ivica Letunic,9 Alex Levitsky,1 Yong Liang,1 Jhy-Jhu Lin,16 Neil F. Lobo,11 John R. Lopez,1 Joel A. Malek,6ddagger Tina C. McIntosh,1 Stephan Meister,9 Jason Miller,1 Clark Mobarry,1 Emmanuel Mongin,17 Sean D. Murphy,1 David A. O'Brochta,13 Cynthia Pfannkoch,1 Rong Qi,1 Megan A. Regier,1 Karin Remington,1 Hongguang Shao,10 Maria V. Sharakhova,11 Cynthia D. Sitter,1 Jyoti Shetty,6 Thomas J. Smith,1 Renee Strong,1 Jingtao Sun,1 Dana Thomasova,9 Lucas Q. Ton,11 Pantelis Topalis,15 Zhijian Tu,10 Maria F. Unger,11 Brian Walenz,1 Aihui Wang,1 Jian Wang,1 Mei Wang,1 Xuelan Wang,11§ Kerry J. Woodford,1 Jennifer R. Wortman,16 Martin Wu,6 Alison Yao,1 Evgeny M. Zdobnov,9 Hongyu Zhang,1 Qi Zhao,1 Shaying Zhao,6 Shiaoping C. Zhu,1 Igor Zhimulev,14 Mario Coluzzi,18 Alessandra della Torre,18 Charles W. Roth,19 Christos Louis,1516 Francis Kalush,1 Richard J. Mural,1 Eugene W. Myers,1 Mark D. Adams,1 Hamilton O. Smith,1 Samuel Broder,1 Malcolm J. Gardner,6 Claire M. Fraser,6 Ewan Birney,17 Peer Bork,9 Paul T. Brey,19 J. Craig Venter,16 Jean Weissenbach,2 Fotis C. Kafatos,9 Frank H. Collins,11dagger Stephen L. Hoffman1parallel

Anopheles gambiae is the principal vector of malaria, a disease that afflicts more than 500 million people and causes more than 1 million deaths each year. Tenfold shotgun sequence coverage was obtained from the PEST strain of A. gambiae and assembled into scaffolds that span 278 million base pairs. A total of 91% of the genome was organized in 303 scaffolds; the largest scaffold was 23.1 million base pairs. There was substantial genetic variation within this strain, and the apparent existence of two haplotypes of approximately equal frequency ("dual haplotypes") in a substantial fraction of the genome likely reflects the outbred nature of the PEST strain. The sequence produced a conservative inference of more than 400,000 single-nucleotide polymorphisms that showed a markedly bimodal density distribution. Analysis of the genome sequence revealed strong evidence for about 14,000 protein-encoding transcripts. Prominent expansions in specific families of proteins likely involved in cell adhesion and immunity were noted. An expressed sequence tag analysis of genes regulated by blood feeding provided insights into the physiological adaptations of a hematophagous insect.

1 Celera Genomics, 45 West Gude Drive, Rockville, MD 20850, USA.
2 Genoscope/Centre National de Sequencage and CNRS-UMR 8030, 2 rue Gaston Cremieux, 91057 Evry Cedex 06, France.
3 Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA.
4 Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases (NIAID), Building 4, Room 126, 4 Center Drive, MSC-0425, Bethesda, MD 20892, USA.
5 Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel.
6 The Institute for Genomic Research (TIGR), 9712 Medical Center Drive, Rockville, MD 20850, USA.
7 Grup de Recerca en Informatica Biomedica, IMIM/UPF/CRG, Barcelona, Catalonia, Spain.
8 Department of Entomology, University of California, Riverside, CA 92521, USA.
9 European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany.
10 Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
11 Center for Tropical Disease Research and Training, University of Notre Dame, Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
12 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
13 Center for Agricultural Biotechnology, University of Maryland Biotechnology Institute, College Park, MD 20742, USA.
14 Institute of Cytology and Genetics, Lavrentyeva ave 10, Novosibirsk 630090, Russia.
15 Institute of Molecular Biology and Biotechnology of the Foundation of Research and Technology-Hellas (IMBB-FORTH), Post Office Box 1527, GR-711 10 Heraklion, Crete, Greece, and University of Crete, GR-711 10 Heraklion, Crete, Greece.
16 Department of Biology, University of Crete, GR-711 10 Heraklion, Crete, Greece.
17 European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
18 Dipartimento di Scienze di Sanità Pubblica, Sezione di Parassitologia, Università degli Studi di Roma "La Sapienza," P.le Aldo Moro 5, 00185 Roma, Italy.
19 Unité de Biochimie et Biologie Moléculaire des Insectes, Institut Pasteur, Paris 75724 Cedex 15, France.
*   Present address: Canada's Michael Smith Genome Science Centre, British Columbia Cancer Agency, Room 3427, 600 West 10th Avenue, Vancouver, British Columbia V5Z 4E6, Canada.

ddagger    Present address: Agencourt Bioscience Corporation, 100 Cummings Center, Suite 107J, Beverly, MA 01915, USA.

§   Present address: Department of Pharmacology, Sun Yat-Sen Medical School, Sun Yat-Sen University #74, Zhongshan 2nd Road, Guangzhou (Canton), 510089, P. R. China.

parallel    Present address: Sanaria, 308 Argosy Drive, Gaithersburg, MD 20878, USA.

dagger    To whom correspondence should be addressed. E-mail: robert.holt{at}celera.com, rholt{at}bcgsc.ca (R.A.H.), frank.h.collins.75{at}nd.edu (F.H.C.).

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Mol. Biol. Evol. 22, 2231-2242
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Realizing the Promise of Genomics in Biomedical Research.
A. E. Guttmacher and F. S. Collins (2005)
JAMA 294, 1399-1402
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Carbonic anhydrase in the adult mosquito midgut.
M. del Pilar Corena, L. VanEkeris, Ma. I. Salazar, D. Bowers, M. M. Fiedler, D. Silverman, C. Tu, and P. J. Linser (2005)
J. Exp. Biol. 208, 3263-3273
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Mosquito natriuretic peptide identified as a calcitonin-like diuretic hormone in Anopheles gambiae (Giles).
G. M. Coast, C. S. Garside, S. G. Webster, K. M. Schegg, and D. A. Schooley (2005)
J. Exp. Biol. 208, 3281-3291
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Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae.
S. Meister, S. M. Kanzok, X.-l. Zheng, C. Luna, T.-R. Li, N. T. Hoa, J. R. Clayton, K. P. White, F. C. Kafatos, G. K. Christophides, et al. (2005)
PNAS 102, 11420-11425
   Abstract »    Full Text »    PDF »
Assembly of polymorphic genomes: Algorithms and application to Ciona savignyi.
J. P. Vinson, D. B. Jaffe, K. O'Neill, E. K. Karlsson, N. Stange-Thomann, S. Anderson, J. P. Mesirov, N. Satoh, Y. Satou, C. Nusbaum, et al. (2005)
Genome Res. 15, 1127-1135
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Estimating the tempo and mode of gene family evolution from comparative genomic data.
M. W. Hahn, T. De Bie, J. E. Stajich, C. Nguyen, and N. Cristianini (2005)
Genome Res. 15, 1153-1160
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Malaria in the post-genomics era: light at the end of the tunnel or just another train?.
D L Gardiner, J S McCarthy, and K R Trenholme (2005)
Postgrad. Med. J. 81, 505-509
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A Cellular Drosophila melanogaster Protein with Similarity to Baculovirus F Envelope Fusion Proteins.
O. Lung and G. W. Blissard (2005)
J. Virol. 79, 7979-7989
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Ultraconserved elements in insect genomes: A highly conserved intronic sequence implicated in the control of homothorax mRNA splicing.
E. A. Glazov, M. Pheasant, E. A. McGraw, G. Bejerano, and J. S. Mattick (2005)
Genome Res. 15, 800-808
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AnoEST: Toward A. gambiae functional genomics.
E. V. Kriventseva, A. C. Koutsos, C. Blass, F. C. Kafatos, G. K. Christophides, and E. M. Zdobnov (2005)
Genome Res. 15, 893-899
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Future Directions In Vaccines: The Payoffs Of Basic Research.
S. Landry and C. Heilman (2005)
Health Aff. 24, 758-769
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The Repertoire of G-Protein-Coupled Receptors in Fully Sequenced Genomes.
R. Fredriksson and H. B. Schioth (2005)
Mol. Pharmacol. 67, 1414-1425
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Evolution of Proteins and Gene Expression Levels are Coupled in Drosophila and are Independently Associated with mRNA Abundance, Protein Length, and Number of Protein-Protein Interactions.
B. Lemos, B. R. Bettencourt, C. D. Meiklejohn, and D. L. Hartl (2005)
Mol. Biol. Evol. 22, 1345-1354
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REL1, a Homologue of Drosophila Dorsal, Regulates Toll Antifungal Immune Pathway in the Female Mosquito Aedes aegypti.
S. W. Shin, V. Kokoza, G. Bian, H.-M. Cheon, Y. J. Kim, and A. S. Raikhel (2005)
J. Biol. Chem. 280, 16499-16507
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Identification of putative noncoding polyadenylated transcripts in Drosophila melanogaster.
J. L. Tupy, A. M. Bailey, G. Dailey, M. Evans-Holm, C. W. Siebel, S. Misra, S. E. Celniker, and G. M. Rubin (2005)
PNAS 102, 5495-5500
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Comparing low coverage random shotgun sequence data from Brassica oleracea and Oryza sativa genome sequence for their ability to add to the annotation of Arabidopsis thaliana.
M. S. Katari, V. Balija, R. K. Wilson, R. A. Martienssen, and W. R. McCombie (2005)
Genome Res. 15, 496-504
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Using shared genomic synteny and shared protein functions to enhance the identification of orthologous gene pairs.
X. H. Zheng, F. Lu, Z.-Y. Wang, F. Zhong, J. Hoover, and R. Mural (2005)
Bioinformatics 21, 703-710
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Biosynthesis and secretion of insect lipoprotein: involvement of furin in cleavage of the apoB homolog, apolipophorin-II/I.
M. M. W. Smolenaars, M. A. M. Kasperaitis, P. E. Richardson, K. W. Rodenburg, and D. J. Van der Horst (2005)
J. Lipid Res. 46, 412-421
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Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents.
C.-Y. Ting, S. Yonekura, P. Chung, S.-n. Hsu, H. M. Robertson, A. Chiba, and C.-H. Lee (2005)
Development 132, 953-963
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Sex-Linked Differentiation Between Incipient Species of Anopheles gambiae.
A. D. Stump, J. A. Shoener, C. Costantini, N. Sagnon, and N. J. Besansky (2005)
Genetics 169, 1509-1519
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Complex early genes.
S. W. Roy and W. Gilbert (2005)
PNAS 102, 1986-1991
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An Active Transposable Element, Herves, From the African Malaria Mosquito Anopheles gambiae.
P. Arensburger, Y.-J. Kim, J. Orsetti, C. Aluvihare, D. A. O'Brochta, and P. W. Atkinson (2005)
Genetics 169, 697-708
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