Abstract
Four members of the twist gene family (twist1a, 1b, 2, and 3) are found in the zebrafish, and they are thought to have arisen through three rounds of gene duplication, two of which occurred prior to the tetrapod-fish split. Phylogenetic analysis groups most of the vertebrate Twist1 peptides into clade I, except for the Twist1b proteins of the acanthopterygian fish (medaka, pufferfish, stickleback), which clustered within clade III. Paralogies and orthologies among the zebrafish, medaka, and human twist genes were determined using comparative synteny analysis of the chromosomal regions flanking these genes. Comparative nucleotide substitution analyses also revealed a faster rate of nucleotide mutation/substitution in the acanthopterygian twist1b compared to the zebrafish twist1b, thus accounting for their anomalous phylogenetic clustering. We also observed minimal expression overlap among the four twist genes, suggesting that despite their significant peptide similarity, their regulatory controls have diverged considerably, with minimal functional redundancy between them.
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Abbreviations
- hpf:
-
hours post-fertilization
- dpf:
-
days post-fertilization
- WISH:
-
whole-mount in situ hybridization
- UTR:
-
untranslated region
References
Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711–1714
Bloch-Zupan A, Hunter N, Manthey A, Gibbins J (2001) R-twist gene expression during rat palatogenesis. Int J Dev Biol 45:397–404
Fuchtbauer EM (1995) Expression of M-twist during postimplantation development of the mouse. Dev Dyn 204:316–322
Germanguz I, Lev D, Waisman T, Kim CH, Gitelman I (2007) Four twist genes in zebrafish, four expression patterns. Dev Dyn 236:2615–2626
Gitelman I (2007) Evolution of the vertebrate twist family and synfunctionalization: a mechanism for differential gene loss through merging of expression domains. Mol Biol Evol 24:1912–1925
Hopwood ND, Pluck A, Gurdon JB (1989) A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59:893–903
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
Lee MS, Lowe G, Flanagan S, Kuchler K, Glackin CA (2000) Human Dermo-1 has attributes similar to twist in early bone development. Bone 27:591–602
Li L, Cserjesi P, Olson EN (1995) Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Dev Biol 172:280–292
Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L, Doglioni C, Beach DH, Hannon GJ (1999) Twist is a potential oncogene that inhibits apoptosis. Genes Dev 13:2207–2217
Postlethwait J, Amores A, Cresko W, Singer A, Yan YL (2004) Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet 20:481–490
Rauch GJ, Lyons DA, Middendorf I, Friedlander B, Arana N, Reyes T, Talbot WS (2003) Submission and curation of gene expression data. ZFIN direct data submission
Ravi V, Venkatesh B (2008) Rapidly evolving fish genomes and teleost diversity. Curr Opin Genet Dev 18:544–550
Roth C, Rastogi S, Arvestad L, Dittmar K, Light S, Ekman D, Liberles DA (2007) Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. J Exp Zoolog B Mol Dev Evol 308:58–73
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Scaal M, Fuchtbauer EM, Brand-Saberi B (2001) cDermo-1 expression indicates a role in avian skin development. Anat Embryol (Berl) 203:1–7
Simpson P (1983) maternal–zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics 105:615–632
Stoetzel C, Weber B, Bourgeois P, Bolcato-Bellemin AL, Perrin-Schmitt F (1995) Dorso-ventral and rostro-caudal sequential expression of M-twist in the postimplantation murine embryo. Mech Dev 51:251–263
Stoetzel C, Bolcato-Bellemin AL, Bourgeois P, Perrin-Schmitt F, Meyer D, Wolff M, Remy P (1998) X-twi is expressed prior to gastrulation in presumptive neurectodermal and mesodermal cells in dorsalized and ventralized Xenopus laevis embryos. Int J Dev Biol 42:747–756
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tavares AT, Izpisuja-Belmonte JC, Rodriguez-Leon J (2001) Developmental expression of chick twist and its regulation during limb patterning. Int J Dev Biol 45:707–713
Thisse B, Thisse C (2004) Submission and curation of gene expression data. ZFIN direct data submission.
Thisse B, el Messal M, Perrin-Schmitt F (1987) The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern. Nucleic Acids Res 15:3439–3453
Westerfield M (2000) The Zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio).
Wolf C, Thisse C, Stoetzel C, Thisse B, Gerlinger P, Perrin-Schmitt F (1991) The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev Biol 143:363–373
Yasutake J, Inohaya K, Kudo A (2004) Twist functions in vertebral column formation in medaka, Oryzias latipes. Mech Dev 121:883–894
Yeo GH, Cheah FS, Jabs EW, Chong SS (2007) Zebrafish twist1 is expressed in craniofacial, vertebral, and renal precursors. Dev Genes Evol 217:783–789
Acknowledgments
We thank Vladimir Korzh, Jin Ben (Institute of Molecular and Cell Biology, Singapore), and Karuna Sampath (Temasek Life Science Laboratories, Singapore) for invaluable advice, Monte Westerfield and Andrew D. Sharrocks for their gifts of dlx2a and fli1a (pAS160) plasmids respectively. This work was supported by grants R-178-000-104-112 (to SSC) from the National University of Singapore Academic Research Fund, and BMRC 06/1/21/19/459 (to SSC) and BMRC 07/1/21/19/544 (to CW) from the Biomedical Research Council of the Agency for Science, Technology, and Research, Singapore.
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Yeo, G.H., Cheah, F.S.H., Winkler, C. et al. Phylogenetic and evolutionary relationships and developmental expression patterns of the zebrafish twist gene family. Dev Genes Evol 219, 289–300 (2009). https://doi.org/10.1007/s00427-009-0290-z
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DOI: https://doi.org/10.1007/s00427-009-0290-z