Development Genes and Evolution

, Volume 217, Issue 7, pp 541–547 | Cite as

Insights into the evolutionary history of the vertebrate zic3 locus from a teleost-specific zic6 gene in the zebrafish, Danio rerio

Short Communication

Abstract

The Zic gene family of zinc-finger transcription factors includes five orthologues, zic1–5, that are common to the Euteleostian vertebrates (fish, frogs, birds, and mammals). The Zic genes have been implicated as regulators of a number of critical developmental processes, including neurulation, neuronal differentiation, neural crest specification, the establishment of left–right asymmetry, and regulation of cell proliferation. The different Zic genes encode proteins that are expressed in broadly overlapping spatial domains, have conserved DNA-binding domains that recognize a common motif, are capable of physical interactions, and can co-regulate one another’s transcription. Thus, the transcriptional regulation of individual proteins and their effects on downstream targets must be assessed within the context of co-expression with other family members. We describe a novel gene, zic6, that is specific to the teleost fishes and lacks the lateral and rostral expression domains typical of the other Zic family members. We present evidence that zic6 is an ancestral locus arising by chromosomal duplication early in the Euteleostomi that was subsequently lost in the terrestrial vertebrates.

Keywords

Fishes Zic Evolution Gene expression Synteny 

Supplementary material

References

  1. Aruga J (2004) The role of Zic genes in neural development. Mol Cell Neurosci 26:205–221PubMedCrossRefGoogle Scholar
  2. Aruga J, Kamiya A, Takahashi H, Fujimi TJ, Shimizu Y et al (2006) A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87:783–792PubMedCrossRefGoogle Scholar
  3. Brewster R, Lee J, Ruiz i Altaba A (1998) Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 939:579–583Google Scholar
  4. Fujimi TJ, Mikoshiba K, Aruga J (2006) Xenopus Zic4: Conservation and diversification of expression profiles and protein function among the Xenopus Zic family. Dev Dyn 235:3379–3386PubMedCrossRefGoogle Scholar
  5. Grinberg I, Millen J (2005) The ZIC gene family in development and disease. Clin Genet 67:290–296PubMedCrossRefGoogle Scholar
  6. Grinblat Y, Sive H (2001) zic gene expression marks anteroposterior pattern in the presumptive neurectoderm of the zebrafish gastrula. Dev Dyn 222:688–693PubMedCrossRefGoogle Scholar
  7. Haddon C, Smithers L, Schneider-Maunoury S, Coche T, Henrique D et al (1998) Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125:359–370PubMedGoogle Scholar
  8. Koyabu Y, Nakata K, Mizugishi K, Aruga J, Mikoshiba K (2001) Physical and functional interactions between Zic and Gli proteins. J Biol Chem 276:6889–6892PubMedCrossRefGoogle Scholar
  9. Liang JO, Etheridge A, Hantsoo L, Rubinstein AL, Nowak SJ et al (2000) Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development 127:5101–5112PubMedGoogle Scholar
  10. 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. Curr Opin Cell Biol 11:699–704CrossRefGoogle Scholar
  11. Mizugishi K, Aruga J, Nakata K, Mikoshiba K (2001) Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J Biol Chem 276:2180–2188PubMedCrossRefGoogle Scholar
  12. Nakata K, Koyabu Y, Aruga J, Mikoshiba K (2000) A novel member of the Xenopus Zic family, Zic5, mediates neural crest development. Mech Dev 99:83–91PubMedCrossRefGoogle Scholar
  13. Parinov S, Kondrichin I, Korzh V, Emelyanov A (2004) Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo. Dev Dyn 231:449–459PubMedCrossRefGoogle Scholar
  14. Thisse C, Thisse B (1998) High resolution whole-mount in situ hybridization. Zebrafish Sci Monitor 5:8–9Google Scholar
  15. Toyama R, Gomez DM, Mana MD, Dawid IB (2004) Sequence relationships and expression patterns of zebrafish zic2 and zic5 genes. Gene Expr Patterns 4:345–350PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Laboratory of Molecular GeneticsNIH/NICHDBethesdaUSA

Personalised recommendations