Abstract
Deuterostomes comprise a monophyletic group of animals that include chordates, xenoturbellids, and the Ambulacraria, which consists of echinoderms and hemichordates. The ancestral chordate probably had 14 Hox genes aligned linearly along the chromosome, with the posterior six genes showing an independent duplication compared to protostomes. In contrast, ambulacrarians are characterized by a duplication of the posterior Hox genes, resulting in three genes known as Hox11/13a, Hox11/13b, and Hox11/13c. Here, we isolated 12 Hox genes from the hemichordate Balanoglossus misakiensis and found an extra Hox gene that has not been reported in hemichordates. The extra B. misakiensis gene was suggested to be Hox8 from paralog-characteristic residues in its hexapepetide motif and homeodomain and a comparison with Strongylocentrotus purpuratus Hox genes. Our data suggest that the ancestor of echinoderms and hemichordates may have had a full complement of 12 Hox genes.
References
Amemiya CT, Prohaska SJ, Hill-Force A, Cook A, Wasserscheid J, Ferrier DEK, Pascual-Anaya J, Garcia-Fernàndez J, Dewar K, Stadler PF (2008) The amphioxus Hox cluster: characterization, comparative genomics, and evolution. J Exp Zool B Mol Dev Evol 310:465–477. doi:10.1002/jez.b.21213
Aronowicz J, Lowe CJ (2006) Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems. Integr Comp Biol 46:890–901. doi:10.1093/icb/icl045
Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR, Telford MJ (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85–88. doi:10.1038
Brown FD, Prendergast A, Swalla BJ (2008) Man is but a worm: chordate origins. Genesis 46:605–613. doi:10.1002/dvg.20471
Cameron RA, Rowen L, Nesbitt R, Bloom S, Rast JP, Berney K, Arenas-Mena C, Martinez P, Lucas S, Richardson PM, Davidson EH, Peterson KJ, Leroy Hood L (2005) Unusual gene order and organization of the sea urchin Hox cluster. J Exp Zool 306B:45–58. doi:10.1002/jez.b.21070
Carroll SB (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376:479–485. doi:10.1038/376479a0
Hara Y, Yamaguchi M, Akasaka K, Nakano H, Nonaka M, Amemiya S (2006) Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus. Dev Genes Evol 216:797–809. doi:10.1007/s00427-006-0108-1
Kuraku S, Takio Y, Tamura K, Aono H, Meyer A, Kuratani S (2008) Noncanonical role of Hox14 revealed by its expression patterns in lamprey and shark. Proc Natl Acad Sci U S A 105:6679–6683. doi:10.1073/pnas.0710947105
Long S, Byrne M (2001) Evolution of chinoderm Hox gene cluster. Evol Dev 3:302–311. doi:10.1046/j.1525-142X.2001.01036.x
Long S, Martinez P, Chen W-C, Thorndyke M, Byrne M (2003) Evolution of echinoderms may not have required modification of the ancestral deuterostome HOX gene cluster: first report of PG4 and PG5 Hox orthologues in echinoderms. Dev Genes Evol 213:573–576. doi:10.1007/s00427-003-0355-3
Pendleton JW, Nagai BK, Murtha MT, Ruddle FH (1993) Expansion of the Hox gene family and the evolution of chordates. Proc Natl Acad Sci U S A 90:6300–6304
Peterson KJ (2004) Isolation of Hox and Parahox genes in the hemichordate Pychodera flava and the evolution of deuterrostome Hox genes. Mol Phylogenet Evol 31:1208–1215. doi:10.1016/j.ympev.2003.10.007
Sharkey M, Graba Y, Scott MP (1997) Hox genes in evolution: protein surfaces and paralog groups. Trends Genet 13:145–151. doi:10.1016/S0168-9525(97)01096-2
Swalla BJ, Smith AB (2008) Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos Trans R Soc Lond B Biol Sci 363:1557–1568. doi:10.1098/rstb.2007.2246
Urata M, Yamaguchi M (2004) The development of the enteropneust hemichordate Balanoglossus misakiensis KUWANO. Zool Sci 21:533–540. doi:10.2108/zsj.21.533
Acknowledgments
We thank Mr. and Mrs. Hatano (Togi Fishermen’s Cooperative Association), Shonan Amemiya, and the students of Kanazawa University for their help in collecting the specimens. This research was supported by the Research Institute of Marine Invertebrates, Tokyo (RIMI), a Sasagawa Scientific Research Grant (to M.U.), and Narishige Science Award (to M.Y.).
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Communicated by H. Nishida
M. Urata and J. Tsuchimoto contributed equally to this study.
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Urata, M., Tsuchimoto, J., Yasui, K. et al. The Hox8 of the hemichordate Balanoglossus misakiensis . Dev Genes Evol 219, 377–382 (2009). https://doi.org/10.1007/s00427-009-0297-5
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DOI: https://doi.org/10.1007/s00427-009-0297-5