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Science 6 July 2007:
Vol. 317. no. 5834, pp. 86 - 94
DOI: 10.1126/science.1139158

Research Articles

Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization

Nicholas H. Putnam,1 Mansi Srivastava,2 Uffe Hellsten,1 Bill Dirks,2 Jarrod Chapman,1 Asaf Salamov,1 Astrid Terry,1 Harris Shapiro,1 Erika Lindquist,1 Vladimir V. Kapitonov,3 Jerzy Jurka,3 Grigory Genikhovich,4 Igor V. Grigoriev,1 Susan M. Lucas,1 Robert E. Steele,5 John R. Finnerty,6 Ulrich Technau,4 Mark Q. Martindale,7 Daniel S. Rokhsar1,2*

Sea anemones are seemingly primitive animals that, along with corals, jellyfish, and hydras, constitute the oldest eumetazoan phylum, the Cnidaria. Here, we report a comparative analysis of the draft genome of an emerging cnidarian model, the starlet sea anemone Nematostella vectensis. The sea anemone genome is complex, with a gene repertoire, exon-intron structure, and large-scale gene linkage more similar to vertebrates than to flies or nematodes, implying that the genome of the eumetazoan ancestor was similarly complex. Nearly one-fifth of the inferred genes of the ancestor are eumetazoan novelties, which are enriched for animal functions like cell signaling, adhesion, and synaptic transmission. Analysis of diverse pathways suggests that these gene "inventions" along the lineage leading to animals were likely already well integrated with preexisting eukaryotic genes in the eumetazoan progenitor.

1 Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA.
2 Center for Integrative Genomics and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, USA.
3 Genetic Information Research Institute, 1925 Landings Drive, Mountain View, CA 94043, USA.
4 Sars International Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgt 55, 5008, Bergen, Norway.
5 Department of Biological Chemistry and the Developmental Biology Center, University of California, Irvine, CA 92697, USA.
6 Department of Biology, Boston University, Boston, MA 02215, USA.
7 Kewalo Marine Laboratory, University of Hawaii, Honolulu, HI 96813, USA.

* To whom correspondence should be addressed. E-mail: dsrokhsar{at}lbl.gov

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   Abstract »    Full Text »    PDF »
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