Abstract
Snail genes comprise a family of zinc-finger transcription factor coding genes with multiple roles in early embryonic development of metazoans. The evolutionary history of this family has been studied in detail, revealing an initial duplication in Snail and Scratch genes preceding the protostome/deuterostome split, and posterior independent duplication events in the lineages leading to insects and vertebrates. The distribution of mammalian and teleost Snail genes fits with current models for whole genome duplication events at the base of the vertebrate lineage, plus an extra duplication in teleosts. However, two very divergent Snail genes, one from mammals and the other from teleost fishes, fit poorly into the phylogenetic analysis of the family. By means of database mining and synteny analysis, we provide evidence for these genes being orthologues, and evidence that they originated in an early duplication at the base of the vertebrates resulting in three and not two Snail genes. We further show that all three Snail genes lie in regions of extensive paralogy, revealing their common origin through segmental or chromosomal duplication.
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References
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Furlong RF, Holland PW (2002) Were vertebrates octoploid? Philos Trans R Soc Lond B Biol Sci 357:531–544
Gong Z, Yan T, Liao J, Lee SE, He J, Hew CL (1997) Rapid identification and isolation of zebrafish cDNA clones. Gene 201:87–98
Gu X, Wang Y, Gu J (2002) Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31:205–209
Kataoka H, Murayama T, Yokode M, Mori S, Sano H, Ozaki H, Yokota Y, Nishikawa S, Kita T (2000) A novel snail-related transcription factor Smuc regulates basic helix-loop-helix transcription factor activities via specific E-box motifs. Nucleic Acids Res 28:626–633
Katoh M, Katoh M (2003) Identification and characterization of human SNAIL3 (SNAI3) gene in silico. Int J Mol Med 11:383–388
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
Locascio A, Manzanares M, Blanco MJ, Nieto MA (2002a) Modularity and reshuffling of Snail and Slug expression during vertebrate evolution. Proc Natl Acad Sci USA 99:16841–16846
Locascio A, Vega S, de Frutos CA, Manzanares M, Nieto MA (2002b) Biological potential of a functional human SNAIL retrogene. J Biol Chem 277:38803–38809
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473
Manzanares M, Locascio A, Nieto MA (2001) The increasing complexity of the Snail gene superfamily in metazoan evolution. Trends Genet 17:178–181
McLysaght A, Hokamp K, Wolfe KH (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31:200–204
Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155–166
Ohno S (1970) Evolution by gene duplication. Springer, Berlin Heidelberg New York
Shields R (2001) Being sensible about synteny. Trends Genet 17:566
Smith SF, Snell P, Gruetzner F, Bench AJ, Haaf T, Metcalfe JA, Green AR, Elgar G (2002) Analyses of the extent of shared synteny and conserved gene orders between the genome of Fugu rubripes and human 20q. Genome Res 12:776–784
Stickney HL, Barresi MJF, Devoto SH (2000) Somite development in zebrafish. Dev Dyn 219:287–303
Taylor JS, Van de Peer Y, Braasch I, Meyer A (2001) Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos Trans R Soc Lond B Biol Sci 356:1661–1679
Venkatesh B, Erdmann MV, Brenner S (2001) Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proc Natl Acad Sci 98:11382–11387
Wolfe KH (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2:333–341
Acknowledgements
We wish to thank Annamaria Locascio and members of the Nieto lab for discussion and suggestions on the manuscript, Matt Wright (HUGO Gene Nomenclature Committee) for help in setting a new nomenclature for the Snail family, Qiling Xu (MRC NIMR, London) for providing zebrafish embryos, Dr. Zhiyuan Gong (National University of Singapore) for providing the zebrafish snail3 EST clone and all the people behind the Ensembl project for making such useful resources available to the community. We apologize for not including references to all primary work due to space limitations. This work was supported by grants from the Spanish Ministry of Science and Technology to M.M. (BMC0203558) and to M.A.N. (BMC0200383). M.J.B. is a researcher of the Ramón y Cajal Program of the Spanish Ministry of Science and Technology.
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Manzanares, M., Blanco, M.J. & Nieto, M.Á. Snail3 orthologues in vertebrates: divergent members of the Snail zinc-finger gene family. Dev Genes Evol 214, 47–53 (2004). https://doi.org/10.1007/s00427-003-0373-1
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DOI: https://doi.org/10.1007/s00427-003-0373-1