This Article Full Text Full Text (PDF) Supplemental Research Data Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Amores, A. Articles by Postlethwait, J. H. Search for Related Content PubMed PubMed Citation Articles by Amores, A. Articles by Postlethwait, J. H. Social Bookmarking                   What's this?

Developmental Roles of Pufferfish Hox Clusters and Genome Evolution in Ray-Fin Fish

¹ Institute of Neuroscience, University of Oregon, Eugene, Oregon 97402, USA ² National Research Institute of Aquaculture, Fisheries Research Agency, Nansei, Mie 516-0193, Japan ³ Virginia Mason Research Center, Benaroya Research Institute, Molecular Genetics Department, Seattle, Washington 98101, USA

The pufferfish skeleton lacks ribs and pelvic fins, and has fused bones in the cranium and jaw. It has been hypothesized that this secondarily simplified pufferfish morphology is due to reduced complexity of the pufferfish Hox complexes. To test this hypothesis, we determined the genomic structure of Hox clusters in the Southern pufferfish Spheroides nephelus and interrogated genomic databases for the Japanese pufferfish Takifugu rubripes (fugu). Both species have at least seven Hox clusters, including two copies of Hoxb and Hoxd clusters, a single Hoxc cluster, and at least two Hoxa clusters, with a portion of a third Hoxa cluster in fugu. Results support genome duplication before divergence of zebrafish and pufferfish lineages, followed by loss of a Hoxc cluster in the pufferfish lineage and loss of a Hoxd cluster in the zebrafish lineage. Comparative analysis shows that duplicate genes continued to be lost for hundreds of millions of years, contrary to predictions for the permanent preservation of gene duplicates. Gene expression analysis in fugu embryos by in situ hybridization revealed evolutionary change in gene expression as predicted by the duplication-degeneration-complementation model. These experiments rule out the hypothesis that the simplified pufferfish body plan is due to reduction in Hox cluster complexity, and support the notion that genome duplication contributed to the radiation of teleosts into half of all vertebrate species by increasing developmental diversification of duplicate genes in daughter lineages.

⁴ Corresponding author.
E-MAIL jpostle{at}uoneuro.uoregon.edu; FAX (541)346-4548.

[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank under accession nos. AY303229, AY303230, AY303231, AY303232, AY303233, AY303234, AY303235.]

CiteULike    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

				S. Mungpakdee, H.-C. Seo, A. R. Angotzi, X. Dong, A. Akalin, and D. Chourrout Differential Evolution of the 13 Atlantic Salmon Hox Clusters Mol. Biol. Evol., July 1, 2008; 25(7): 1333 - 1343. [Abstract] [Full Text] [PDF]

				W. Shi, W. Zhou, and D. Xu Identifying cis-regulatory elements by statistical analysis and phylogenetic footprinting and analyzing their coexistence and related gene ontology Physiol Genomics, November 14, 2007; 31(3): 374 - 384. [Abstract] [Full Text] [PDF]

				D. Duboule The rise and fall of Hox gene clusters Development, July 15, 2007; 134(14): 2549 - 2560. [Abstract] [Full Text] [PDF]

				C. Sullivan, J. H. Postlethwait, C. R. Lage, P. J. Millard, and C. H. Kim Evidence for Evolving Toll-IL-1 Receptor-Containing Adaptor Molecule Function in Vertebrates J. Immunol., April 1, 2007; 178(7): 4517 - 4527. [Abstract] [Full Text] [PDF]

				V. Laize, C. S. B. Viegas, P. A. Price, and M. L. Cancela Identification of an Osteocalcin Isoform in Fish with a Large Acidic Prodomain J. Biol. Chem., June 2, 2006; 281(22): 15037 - 15043. [Abstract] [Full Text] [PDF]

				A. P. Lee, E. G. L. Koh, A. Tay, S. Brenner, and B. Venkatesh Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters PNAS, May 2, 2006; 103(18): 6994 - 6999. [Abstract] [Full Text] [PDF]

				S. Tumpel, F. Cambronero, L. M. Wiedemann, and R. Krumlauf Evolution of cis elements in the differential expression of two Hoxa2 coparalogous genes in pufferfish (Takifugu rubripes) PNAS, April 4, 2006; 103(14): 5419 - 5424. [Abstract] [Full Text] [PDF]

				K. D. Crow, P. F. Stadler, V. J. Lynch, C. Amemiya, and G. P. Wagner The "Fish-Specific" Hox Cluster Duplication Is Coincident with the Origin of Teleosts Mol. Biol. Evol., January 1, 2006; 23(1): 121 - 136. [Abstract] [Full Text] [PDF]

				J. Nam and M. Nei Evolutionary Change of the Numbers of Homeobox Genes in Bilateral Animals Mol. Biol. Evol., December 1, 2005; 22(12): 2386 - 2394. [Abstract] [Full Text] [PDF]

				W. Kai, K. Kikuchi, M. Fujita, H. Suetake, A. Fujiwara, Y. Yoshiura, M. Ototake, B. Venkatesh, K. Miyaki, and Y. Suzuki A Genetic Linkage Map for the Tiger Pufferfish, Takifugu rubripes Genetics, September 1, 2005; 171(1): 227 - 238. [Abstract] [Full Text] [PDF]

				G. SUNDSTROM, T. A. LARSSON, S. BRENNER, B. VENKATESH, and D. LARHAMMAR Ray-Fin Fish Tetraploidization Gave Rise to Pufferfish Duplicates of NPY and PYY, but Zebrafish NPY Duplicate Was Lost Ann. N.Y. Acad. Sci., April 1, 2005; 1040(1): 476 - 478. [Abstract] [Full Text] [PDF]

				D. W. Stock The Dlx Gene Complement of the Leopard Shark, Triakis semifasciata, Resembles That of Mammals: Implications for Genomic and Morphological Evolution of Jawed Vertebrates Genetics, February 1, 2005; 169(2): 807 - 817. [Abstract] [Full Text] [PDF]

				H. Tostivint, L. Joly, I. Lihrmann, M. Ekker, and H. Vaudry Chromosomal localization of three somatostatin genes in zebrafish. Evidence that the [Pro2]-somatostatin-14 isoform and cortistatin are encoded by orthologous genes J. Mol. Endocrinol., December 1, 2004; 33(3): R1 - R8. [Abstract] [Full Text] [PDF]

				E. J. Stellwag Are Genome Evolution, Organism Complexity and Species Diversity Linked? Integr. Comp. Biol., November 1, 2004; 44(5): 358 - 365. [Abstract] [Full Text] [PDF]

				S. Bertrand, F. G. Brunet, H. Escriva, G. Parmentier, V. Laudet, and M. Robinson-Rechavi Evolutionary Genomics of Nuclear Receptors: From Twenty-Five Ancestral Genes to Derived Endocrine Systems Mol. Biol. Evol., October 1, 2004; 21(10): 1923 - 1937. [Abstract] [Full Text] [PDF]