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Theory in Biosciences

, Volume 123, Issue 1, pp 89–110 | Cite as

The duplication of the Hox gene clusters in teleost fishes

  • Sonja J. Prohaska
  • Peter F. Stadler
Article

Abstract

Higher teleost fishes, including zebrafish and fugu, have duplicated their Hox genes relative to the gene inventory of other gnathostome lineages. The most widely accepted theory contends that the duplicate Hox clusters orginated synchronously during a single genome duplication event in the early history of ray-finned fishes. In this contribution we collect and re-evaluate all publicly available sequence information. In particular, we show that the short Hox gene fragments from published PCR surveys of the killifish Fundulus heteroclitus, the medaka Oryzias latipes and the goldfish Carassius auratus can be used to determine with little ambiguity not only their paralog group but also their membership in a particular cluster.

Together with a survey of the genomic sequence data from the pufferfish Tetraodon nigroviridis we show that at least percomorpha, and possibly all eutelosts, share a system of 7 or 8 orthologous Hox gene clusters. There is little doubt about the orthology of the two teleost duplicates of the HoxA and HoxB clusters. A careful analysis of both the coding sequence of Hox genes and of conserved non-coding sequences provides additional support for the “duplication early” hypothesis that the Hox clusters in teleosts are derived from eight ancestral clusters by means of subsequent gene loss; the data remain ambiguous, however, in particular for the HoxC clusters.

Assuming the “duplication early” hypothesis we use the new evidence on the Hox gene complements to determine the phylogenetic positions of gene-loss events in the wake of the cluster duplication. Surprisingly, we find that the resolution of redundancy seems to be a slow process that is still ongoing. A few suggestions on which additional sequence data would be most informative for resolving the history of the teleostean Hox genes are discussed.

Keywords

Hox cluster Genome duplication Teleost Fundulus heteroclitus Tetraodon nigroviridis 

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References

  1. Ahn, D.-g., Gibson, G., 1999. Expression patterns of threespine stickleback Hox genes and insights into the evolution of the vertebrate body axis. Development Genes and Evolution 209, 482–494.PubMedCrossRefGoogle Scholar
  2. Allendorf, F.W., Thorgaard, G.H., 1984. Tetraploidy and the evolution of salmonid fishes. In: Turner, B.J. (Ed.), Evolutionary Genetics of Fishes. Plenum Press, New York, pp. 1–46.Google Scholar
  3. Amores, A., Force, A., Yan, Y.L., Joly, C., Amemiya, A., Fritz, R.K., Ho, J., Langeland, V., Prince, Y.L., Wang, M., Westerfield, M., Ekker, M., Postlethwait, J.H., 1988. Zebrafish Hox clusters and vertebrate genome evolution. Science 282, 1711–1714.CrossRefGoogle Scholar
  4. Amores, A., Suzuki, T., Yan, Y.L., Pomeroy, J., Singer, A., Amemiya, C., Postlethwait, J., 2004. Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Research 14, 1–10.PubMedCrossRefGoogle Scholar
  5. Aparicio, S., Hawker, K., Cottage, A., Mikawa, Y., Zuo, L., Venkatesh, B., Chen, E., Krumlauf, R., Brenner, S., 1997. Organization of the Fugu rubripes Hox clusters: evidence for continuing evolution of vertebrate Hox complexes. Nature Genetics 16, 79–83.PubMedCrossRefGoogle Scholar
  6. Bandelt, H.-J., Dress, A.W.M., 1993. A relational approach to split decomposition. In: Opitz, O., Lausen, B., Klar, R. (Eds.), Information and Classification. Springer, Berlin, pp. 123–131.Google Scholar
  7. Bryant, D., Moulton, V., 2004. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution 21, 255–265.PubMedCrossRefGoogle Scholar
  8. Chen, W.-J., Bonillo, C., Lecointre, G., 2003. Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of acanthomorpha (teleostei) with larger number of taxa. Molecular Phylogenetics and Evolution 26, 262–288.PubMedCrossRefGoogle Scholar
  9. Chiu, C.-h., Amemiya, C., Dewar, K., Kim, C.B., Ruddle, F.H., Wagner, G.P., 2002. Molecular evolution of the HoxA cluster in the three major gnathostome lineages. Proceedings of the National Academy of Sciences of the United States of America 99, 5492–5497.PubMedCrossRefGoogle Scholar
  10. Chiu, C.-H., Dewar, K., Wagner, G.P., Takahashi, K., Ruddle, F., Ledje, C., Bartsch, P., Scemama, J.-L., Stellwag, E., Fried, C., Prohaska, S.J., Stadler, P.F., Amemiya, C.T., 2004. Bichir HoxA cluster sequence reveals surprising trends in rayfinned fish genomic evolution. Genome Research 14, 11–17.PubMedCrossRefGoogle Scholar
  11. Cutler, C.P., Cramb, G., 2001. Molecular physiology of osmoregulation in cels and other teleosts: the role of transporter isoforms and gene duplication. Comparative Biochemistry and Physiology 130, 551–564.PubMedCrossRefGoogle Scholar
  12. Danielson, P.B., Alrubaian, J., Muller, M., Redding, J.M., Dores, R.M., 1999. Duplication of the pome gene in the paddlefish (Polyodon spathula): analysis of γ-msh, acth, and β-endorphin regions of rayfinned fish POMC. General and Comparative Endocrinology 132, 384–390.Google Scholar
  13. Davidson, E., 2002. Genomic Regulatory Systems. Academic Press, San Diego.Google Scholar
  14. Fares, M.A., Bezemer, D., Moya, A., Marín, I., 2003. Selection on coding regions determined Hox7 genes evolution. Molecular Biology and Evolution 20, 2104–2112.PubMedCrossRefGoogle Scholar
  15. Felsenstein, J., 1989. Phylip—phylogeny inference package (version 3.2). Cladistics 5, 164–2166.Google Scholar
  16. Fjose, A., Molven, A., Eiken, H.G., 1988. Molecular cloning and characterization of homeo-box-containing genes from Atlantic salmon. Gene 62, 141–152.PubMedCrossRefGoogle Scholar
  17. Force, A., Amores, A., Postlethwait, J.H., 2002. Hox cluster organization in the jawless vertebrate Petromyzon marinus. Journal of Experimental Zoology (Molecular Development and Evolution) 294, 30–46.CrossRefGoogle Scholar
  18. Fried, C., Prohaska, S.J., Stadler, P.F., 2003. Independent hox-cluster duplications in lampreys. Journal of Experimental Zoology (Molecular Development and Evolution) 299B, 18–25.CrossRefGoogle Scholar
  19. Garcia-Fernández, J., Holland, P.W., 1994. Archetypal organization of the amphioxus hox gene cluster. Nature 370, 563–566.PubMedCrossRefGoogle Scholar
  20. Holland, P.W., Garcia-Fernández, J., 1996. Hox genes and chordate evolution. Developmental Biology 173, 382–395.PubMedCrossRefGoogle Scholar
  21. Holland, P.W.H., Garcia-Fernández, J., Williams, N.A., Sidow, A., 1994. Gene duplication and the origins of vertebrate development. Development (Suppl.) 125–133.Google Scholar
  22. Hughes, A.L., Friedman, R., 2003. 2R or not 2R: testing hypotheses of genome duplication in early vertebrates. Journal of Structural and Functional Genomics 3, 85–93.PubMedCrossRefGoogle Scholar
  23. Huson, D.H., 1998. Splitstree: analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73.PubMedCrossRefGoogle Scholar
  24. Inoue, J.G., Miya, M., Tsukamoto, K., Nishida, M., 2003. Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the ‘ancient fish’. Molecular Phylogenetics and Evolution 26, 110–120.PubMedCrossRefGoogle Scholar
  25. Inoue, J. G., Miya, M., Tsukamoto, K., Nishida, M. 2004. Mitogenomic evidence for the monophyly of elopomorph fishes (telostei) and the evolutionary origin of the leptocephalus larva. Molecular Phylogenetics and Evolution. doi: 10.1016/j.ympev.2003.11.009.Google Scholar
  26. Irvine, S.Q., Carr, J.L., Bailey, W.J., Kawasaki, K., Shimizu, N., Amemiya, C.T., Ruddle, F.H., 2002. Genomic analysis of Hox clusters in the sea lamprey, Petromyzon marinus. Journal of Experimental Zoology (Molecular Development and Evolution) 294, 47–62.CrossRefGoogle Scholar
  27. Ishiguro, N.B., Miya, M., Nishida, M., 2003. Basal euteleostean relationships: a mitogenomic perspective on the phylogenetic reality of the “protacanthopterygii”. Molecular Phylogenetics and Evolution 27, 476–488.PubMedCrossRefGoogle Scholar
  28. Ji, F.Y., Liu, J.D., Yi, M.S., Huang, L., Zhou, F., Yu, Q.X., 2002. Chromosomal localization of rice field eel Hox genes by PRINS. Yi Chuan Xue Bao (Acta Genetica Sinica) 29, 612–615 (in Chinese).Google Scholar
  29. Kim, C.B., Amemiya, C., Bailey, W., Kawasaki, K., Mezey, J., Miller, W., Minosima, S., Shimizu, N., Wagner, G.P., Ruddle, F., 2000. Hox cluster genomics in the horn shark, Heterodontus francisci. Proceedings of the National Academy of Sciences of the United States of America 97, 1655–1660.PubMedCrossRefGoogle Scholar
  30. Koh, E.G.L., Lam, K., Christoffels, A., Erdmann, M.V., Brenner, S., Venkatesh, B., 2003. Hox gene clusters in the indonesian coelacanth, Latimeria menadoensis. Proceedings of the National Academy of Sciences of the United States of America 100, 1084–1088.PubMedCrossRefGoogle Scholar
  31. Kurosawa, G., Yamada, K., Ishiguro, H., Hori, H., 1999. Hox gene complexity in medaka fish may be similar to that in pufferfish rather than zebrafish. Biochemical and Biophysical Research Communication 260, 66–70.CrossRefGoogle Scholar
  32. Larhammar, D., Lundin, L.G., H.F., 2002. The human Hox-bearing chromosome regions did arise by block or chromosome (or even genome) duplications. Genome Research 12, 1910–1920.PubMedCrossRefGoogle Scholar
  33. Levine, E.M., Schechter, N., 1993. Homeobox genes expressed in the retina and brain of adult goldfish. Proceedings of the National Academy of Sciences of the United States of America 90, 2729–2733.PubMedCrossRefGoogle Scholar
  34. Lynch, M., Conery, J.S., 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155.PubMedCrossRefGoogle Scholar
  35. Lynch, V.J., Roth, J.J., Takahashi, K., Dunn, C., Nonaka, D., Stopper, G., Wagner, G.P., 2004. The origin of placental mammals is coincident with adaptive evolution of the developmental control genes HoxA-11 and HoxA-13. submitted.Google Scholar
  36. Málaga-Trillo, E., Meyer, A., 2001. Genome duplications and accelerated evolution of Hox genes and cluster architecture in teleost fishes. American Zoologist 41, 676–686.CrossRefGoogle Scholar
  37. Martinez, P., Amemiya, C.T., 2002. Genomics of the HOX gene cluster. Comparative Biochemistry and Physiology Part B 133, 571–580.CrossRefGoogle Scholar
  38. McGinnis, W., Krumlauf, R., 1992. Homeobox genes and axial patterning. Cell 68, 283–302.PubMedCrossRefGoogle Scholar
  39. Merrit, T.J.S., Quattro, J.M., 2001. Evidence for a period of directional selection following gene duplication in a neurally expressed locus of triosephosphate isomerase. Genetics 159, 689–697.Google Scholar
  40. Merrit, T.J.S., Quattro, J.M., 2003. Evolution of the vertebrate cytosolic malate dehydrogenase gene family: duplication and divergence in actinopterygian fish. Journal of Molecular Biology 56, 265–276.Google Scholar
  41. Meyer, A., Málaga-Trillo, E., 1999. More fishy tales about Hox gene clusters. Current Biology 9, R210–213.PubMedCrossRefGoogle Scholar
  42. Meyer, A., Schartl, M., 1999. Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Current Opinion in Cell Biology 11, 699–704.PubMedCrossRefGoogle Scholar
  43. Misof, B.Y., Blanco, M.J., Wagner, G.P., 1996. A PCR-survey of Hox genes of the zebrafish: new sequences and evolutionary implications. Journal of Experimental Biology 274, 193–206.Google Scholar
  44. Misof, B.Y., Wagner, G.P., 1996. Evidence for four Hox clusters in the killifish Fundulus heteroclitus (teleostei). Molecular Phylogenetics and Evolution 5, 309–322.PubMedCrossRefGoogle Scholar
  45. Miya, M., Takeshima, H., Endo, H., Ishiguro, N.B., Inoue, J.G., Mukai, T., Satoh, T.P., Yamaguchi, M., Kawaguchi, A., Mabuchi, K., Shirai, S.M., Nishida, M., 2003. Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial dna sequences. Molecular Phylogenetics and Evolution 26, 121–138.PubMedCrossRefGoogle Scholar
  46. Mortlock, D.P., Sateesh, P., Innis, J.W., 2000. Evolution of N-terminal sequences of the vertebrate HOXA 13 protein. Mammalion Genome 11, 151–158.CrossRefGoogle Scholar
  47. Murray, B.W., Busby, E.R., Mommsen, T.P., Wright, P.A., 2003. Evolution of glutamine synthetase in vertebrates: multiple glutamine synthetase genes expressed in rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206, 1511–1521.PubMedCrossRefGoogle Scholar
  48. Naruse, K., Fukamachi, S., Mitani, H., Kondo, M., Matsuoka, T., Kondo, S., Hanamura, N., Morita, Y., Hasegawa, K., Nishigaki, R., Shimada, A., Wada, H., Kusakabe, T., Suzuki, N., Kinoshita, M., Kanamori, A., Terado, T., Kimura, H., Nonaka, M., Shima, A., 2000. A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics 154, 1773–1784.PubMedGoogle Scholar
  49. Ohno, S., 1970. Evolution by Gene Duplication. Springer, New York.Google Scholar
  50. Panopoulou, G., Hennig, S., Groth, D., Krause, A., Poustka, A.J., Herwig, R., Vingron, M., Lehrach, H., 2003. New evidence for genome-wide duplications at the origin of vertebrates using an amphioxus gene set and completed animal genomes. Genome Research 13, 1056–1066.PubMedCrossRefGoogle Scholar
  51. Pavell, A.M., Stellway, E.J., 1994. Survey of Hox-like genes in the teleost Morone saxatilis: Implications for the evolution of the Hox gene family. Molecular Marine Biology and Biotechnology 3, 149–157.PubMedGoogle Scholar
  52. Prohaska, S.J., Fried, C., Amemiya, C.T., Ruddle, F.H., Wagner, G.P., Stadler, P.F., 2004a. The shark HoxN cluster is homologous to the human HoxD cluster. Journal of Molecular Evolution in press.Google Scholar
  53. Prohaska, S.J., Fried, C., Flamm, C., Wagner, G., Stadler, P.F., 2004b. Surveying phylogenetic footprints in large gene clusters: Applications to Hox cluster duplications. Molecular Phylogenetics and Evolution doi:10.1016/j.ympev.2003.08.009.Google Scholar
  54. Robinson-Rechavi, M., Marchand, O., Escriva, H., Bardet, P.L., Zelus, D., Hughes, S., Laudet, V., 2001. Euteleost fish genomes are characterized by expansion of gene families. Genome Research 11, 781–788.PubMedCrossRefGoogle Scholar
  55. Roest Crollius, H., Jaillon, O., Dasilva, C., Ozouf-Costaz, C., Fizames, C., Fischer, C., Bouneau, L., Billault, A., Quetier, F., Saurin, W., Bernot, A., Weissenbach, J., 2000. Characterization and repeat analysis of the compact genome of the freshwater pufferfish Tetraodon nigroviridis. Genome Research 10, 939–949.PubMedCrossRefGoogle Scholar
  56. Ruddle, F.H., Bartels, J.L., Bentley, K.L., Kappen, C., Murta, M.T., Pendleton, J.W., 1994a. Evolution of Hox genes. Annual Review Genetics 28, 423–442.CrossRefGoogle Scholar
  57. Ruddle, F.H., Bentley, K.L., Murtha, M.T., Risch, N., 1994b. Gene loss and gain in the evolution of the vertebrates. Development (Supplement), 155–161.Google Scholar
  58. Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.PubMedGoogle Scholar
  59. Santini, S., Boore, J.L., Meyer, A., 2003. Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters. Genome Research 13, 1111–1122.PubMedCrossRefGoogle Scholar
  60. Scemama, J.-L., Hunter, M., McCallum, J., Prince, V., Stellwag, E., 2002. Evolutionary divergence of vertebrate Hoxb2 expression patterns and transcriptional regulatory loci. Journal of Experimental Zoology (Molecular Development and Evolution) 294, 285–299.CrossRefGoogle Scholar
  61. Schubert, F.R., Nieselt-Struwe, K., Gruss, P., 1993. The antennapedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution. Proceedings of the National Academy of Sciences of the United States of America 90, 143–147.PubMedCrossRefGoogle Scholar
  62. Shashikant, C.S., Utset, M.F., Violette, S.M., Wise, T.L., Einat, P., Einat, M., Pendleton, J.W., Schughart, K., Ruddie, F.H., 1991. Homeobox genes in mouse development. Critical Reviews in Eukaryotic Gene Expression 1, 207–245.PubMedGoogle Scholar
  63. Simmons, M.P., Miya, M., 2004. Efficiently resolving the basal clades of a phylogenetic tree using Bayesian and parsimony approaches: a case study using mitogenomic data from 100 higher teleost fishes. Molecular Phylogenetics and Evolution, dol:10.1016/j.ympev.2003.08.004.Google Scholar
  64. Snell, E.A., Scemama, J.L., Stellwag, E.J., 1999. Genomic organization of the Hoxa4-Hoxa10 region from Morone saxatilis: implications for Hox gene evolution among vertebrates. Journal of Experimental Zoology (Molecular Development and Evolution) 285, 41–49.CrossRefGoogle Scholar
  65. Stadler, H.S., Murray, J.C., Leysens, N.J., Goodfellow, P.J., Solursh, M., 1995. Phylogenetic conservation and physical mapping of members of the H6 homeobox gene family. Mammalian Genome 6, 383–388.PubMedCrossRefGoogle Scholar
  66. Stadler, P.F., Fried, C., Prohaska, S.J., Bailey, W.J., Misof, B.Y., Ruddle, F.H., Wagner, G.P., 2004. Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii. Molecular Phylogenetics and Evolution, in press.Google Scholar
  67. Stellwag, E.J., 1999. Hox gene duplications in fish. Cell Development and Biology 10, 531–540.CrossRefGoogle Scholar
  68. Stevens, C.J., Samallo, J., Schipper, H., Stroband, H.W., te Kronnie, G., 1996. Expression of Hoxb-1 during gastrulation and segmentation stages of carp (Cyprinus carpio). International Journal of Developmental Biology 40, 463–470.PubMedGoogle Scholar
  69. Suzuki, T., Oohara, I., Kurokawa, T., 1998. Hoxd-4 expression during pharyngeal arch development in flounder (Paralichthys olivaceus) embryos and effects of retinoic acid on expression. Zoological Science 15, 57–67.PubMedCrossRefGoogle Scholar
  70. Suzuki, T., Srinivastava, A.S., Kurokawa, T., 1999. Hoxb-5 is expressed in gill arch 5 during pharyngeal arch development of flounder Paralichthys olivaceus embryos. International Journal of Developmental Biology 43, 357–359.PubMedGoogle Scholar
  71. Tagle, D.A., Koop, B.F., Goodman, M., Slightom, J.L., Hess, D.L., Jones, R.T., 1988. Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus). Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. Journal of Molecular Biology 203, 439–455.PubMedCrossRefGoogle Scholar
  72. Takahashi, Y., Hamada, J.-I., Murakawa, K., Takada, M., Tada, M., Nogami, I., Hayashi, N., Nakamoric, S., Monden, M., Miyamoto, M., Katoh, H., Moriuchi, T., 2004. Expression profiles of 39 HOX genes in normal human adult organs and anaplastic thyroid cancer cell lines by quantitative realtime RT-PCR system. Experimental Cell Research 293, 144–153.PubMedCrossRefGoogle Scholar
  73. Taylor, J., Braasch, I., Frickey, T., Meyer, A., Van De Peer, Y., 2003. Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Research 13, 382–390.PubMedCrossRefGoogle Scholar
  74. Van de Peer, Y., Taylor, J.S., Braasch, I., Meyer, A., 2001. The ghost of selection past: rates of evolution and functional divergence of anciently duplicated genes. Journal of Molecular Evolution 53, 436–446.PubMedCrossRefGoogle Scholar
  75. Vandepoele, K., De Vos, W., Taylor, J.S., Meyer, A., Van de Peer, Y., 2004. Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proceedings of the National Academy of Sciences of the United States of America 101, 1638–1643.PubMedCrossRefGoogle Scholar
  76. Wagner, G.P., Amemiya, C., Ruddle, F., 2003. Hox cluster duplication and the genetics of evolutionary novelties. Proceedings of the National Academy of Sciences of the United States of America 100, 14603–14606.PubMedCrossRefGoogle Scholar
  77. Zardoya, R., Abouheif, E., Meyer, A., 1996. Evolutionary analyses of hedgehog and Hoxd-10 genes closely related to the zebrafish. Proceedings of the National Academy of Sciences of the United States of America 93, 13036–13041.PubMedCrossRefGoogle Scholar

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© Elsevier GmbH 2004

Authors and Affiliations

  1. 1.Lehrstuhl für Bioinformatik am Institut für InformatikUniversität LeipzigLeipzigGermany
  2. 2.Interdisziplinärez Zentrum für BioinformatikUniversität LeipzigLeipzigGermany
  3. 3.Institut für Theoretische Chemie und Molekulare StrukturbiologieUniversität WienWienAustria

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