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Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis

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Abstract

The Sox and Forkhead (Fox) gene families are comprised of transcription factors that play important roles in a variety of developmental processes, including germ layer specification, gastrulation, cell fate determination, and morphogenesis. Both the Sox and Fox gene families are divided into subgroups based on the amino acid sequence of their respective DNA-binding domains, the high-mobility group (HMG) box (Sox genes) or Forkhead domain (Fox genes). Utilizing the draft genome sequence of the cnidarian Nematostella vectensis, we examined the genomic complement of Sox and Fox genes in this organism to gain insight into the nature of these gene families in a basal metazoan. We identified 14 Sox genes and 15 Fox genes in Nematostella and conducted a Bayesian phylogenetic analysis comparing HMG box and Forkhead domain sequences from Nematostella with diverse taxa. We found that the majority of bilaterian Sox groups have clear Nematostella orthologs, while only a minority of Fox groups are represented, suggesting that the evolutionary pressures driving the diversification of these gene families may be distinct from one another. In addition, we examined the expression of a subset of these genes during development in Nematostella and found that some of these genes are expressed in patterns consistent with roles in germ layer specification and the regulation of cellular behaviors important for gastrulation. The diversity of expression patterns among members of these gene families in Nematostella reinforces the notion that despite their relatively simple morphology, cnidarians possess much of the molecular complexity observed in bilaterian taxa.

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References

  • Adell T, Muller WE (2004) Isolation and characterization of five Fox (Forkhead) genes from the sponge Suberites domuncula. Gene 334:35–46

    Article  PubMed  CAS  Google Scholar 

  • Alexander J, Stainier DY (1999) A molecular pathway leading to endoderm formation in zebrafish. Curr Biol 9:1147–1157

    Article  PubMed  CAS  Google Scholar 

  • Bowles J, Schepers G, Koopman P (2000) Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227:239–255

    Article  PubMed  CAS  Google Scholar 

  • Carlsson P, Mahlapuu M (2002) Forkhead transcription factors: key players in development and metabolism. Dev Biol 250:1–23

    Article  PubMed  CAS  Google Scholar 

  • Collins AG (1998) Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc Natl Acad Sci U S A 95:15458–15463

    Article  PubMed  CAS  Google Scholar 

  • Cremazy F, Berta P, Girard F (2000) Sox neuro, a new Drosophila Sox gene expressed in the developing central nervous system. Mech Dev 93:215–219

    Article  PubMed  CAS  Google Scholar 

  • El-Hodiri H, Bhatia-Dey N, Kenyon K, Ault K, Dirksen M, Jamrich M (2001) Fox (forkhead) genes are involved in the dorso-ventral patterning of the Xenopus mesoderm. Int J Dev Biol 45:265–271

    PubMed  CAS  Google Scholar 

  • Finnerty JR, Paulson D, Burton P, Pang K, Martindale MQ (2003) Early evolution of a homeobox gene: the parahox gene Gsx in the Cnidaria and the Bilateria. Evol Dev 5:331–345

    Article  PubMed  CAS  Google Scholar 

  • Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ (2004) Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304:1335–1337

    Article  PubMed  CAS  Google Scholar 

  • Fritzenwanker JH, Technau U (2002) Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev Genes Evol 212:99–103

    Article  PubMed  Google Scholar 

  • Fritzenwanker JH, Saina M, Technau U (2004) Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 275:389–402

    Article  PubMed  CAS  Google Scholar 

  • Girosi L, Ramoino P, Diaspro A, Gallus L, Ciarcia G, Tagliafierro G (2005) FMRFamide-like immunoreactivity in the sea-fan Eunicella cavolini (Cnidaria: Octocorallia). Cell Tissue Res 320:331–336

    Article  PubMed  CAS  Google Scholar 

  • Grimmelikhuijzen CJ, Westfall JA (1995) The nervous systems of cnidarians. EXS 72:7–24

    PubMed  CAS  Google Scholar 

  • Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovell-Badge R (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346:245–250

    Article  PubMed  CAS  Google Scholar 

  • Hand C, Uhlinger KR (1992) The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull 182:169–176

    Article  Google Scholar 

  • Harley VR, Lovell-Badge R, Goodfellow PN (1994) Definition of a consensus DNA binding site for SRY. Nucleic Acids Res 22:1500–1501

    Article  PubMed  CAS  Google Scholar 

  • Hatini V, Huh SO, Herzlinger D, Soares VC, Lai E (1996) Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. Genes Dev 10:1467–1478

    Article  PubMed  CAS  Google Scholar 

  • Heeg-Truesdell E, LaBonne C (2004) A slug, a fox, a pair of sox: transcriptional responses to neural crest inducing signals. Birth Defects Res Part C Embryo Today 72:124–139

    Article  CAS  Google Scholar 

  • Honore SM, Aybar MJ, Mayor R (2003) Sox10 is required for the early development of the prospective neural crest in Xenopus embryos. Dev Biol 260:79–96

    Article  PubMed  CAS  Google Scholar 

  • Hoodless PA, Pye M, Chazaud C, Labbe E, Attisano L, Rossant J, Wrana JL (2001) FoxH1 (Fast) functions to specify the anterior primitive streak in the mouse. Genes Dev 15:1257–1271

    Article  PubMed  CAS  Google Scholar 

  • Hosking BM, Wyeth JR, Pennisi DJ, Wang SC, Koopman P, Muscat GE (2001) Cloning and functional analysis of the Sry-related HMG box gene, Sox18. Gene 262:239–247

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Iida K, Koseki H, Kakinuma H, Kato N, Mizutani-Koseki Y, Ohuchi H, Yoshioka H, Noji S, Kawamura K, Kataoka Y, Ueno F, Taniguchi M, Yoshida N, Sugiyama T, Miura N (1997) Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 124:4627–4638

    PubMed  CAS  Google Scholar 

  • Kamachi Y, Cheah KS, Kondoh H (1999) Mechanism of regulatory target selection by the SOX high-mobility-group domain proteins as revealed by comparison of SOX1/2/3 and SOX9. Mol Cell Biol 19:107–120

    PubMed  CAS  Google Scholar 

  • Kamachi Y, Uchikawa M, Kondoh H (2000) Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 16:182–187

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann E, Knochel W (1996) Five years on the wings of fork head. Mech Dev 57:3–20

    Article  PubMed  CAS  Google Scholar 

  • Kenny AP, Oleksyn DW, Newman LA, Angerer RC, Angerer LM (2003) Tight regulation of SpSoxB factors is required for patterning and morphogenesis in sea urchin embryos. Dev Biol 261:412–425

    Article  PubMed  CAS  Google Scholar 

  • Kume T, Deng KY, Winfrey V, Gould DB, Walter MA, Hogan BL (1998) The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 93:985–996

    Article  PubMed  CAS  Google Scholar 

  • Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, Holstein TW (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433:156–160

    Article  PubMed  CAS  Google Scholar 

  • Laudet V, Stehelin D, Clevers H (1993) Ancestry and diversity of the HMG box superfamily. Nucleic Acids Res 21:2493–24501

    Article  PubMed  CAS  Google Scholar 

  • Lee HH, Frasch M (2004) Survey of forkhead domain encoding genes in the Drosophila genome: classification and embryonic expression patterns. Dev Dyn 229:357–366

    Article  PubMed  CAS  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474

    Article  PubMed  CAS  Google Scholar 

  • Martinez DE, Dirksen ML, Bode PM, Jamrich M, Steele RE, Bode HR (1997) Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in hydra. Dev Biol 192:523–536

    Article  PubMed  CAS  Google Scholar 

  • Mazet F, Yu JK, Liberles DA, Holland LZ, Shimeld SM (2003) Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene 316:79–89

    Article  PubMed  CAS  Google Scholar 

  • Medina M, Collins AG, Silberman JD, Sogin ML (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci U S A 98:9707–9712

    Article  PubMed  CAS  Google Scholar 

  • Pennisi D, Bowles J, Nagy A, Muscat G, Koopman P (2000) Mice null for sox18 are viable and display a mild coat defect. Mol Cell Biol 20:9331–9336

    Article  PubMed  CAS  Google Scholar 

  • Pevny LH, Lovell-Badge R (1997) Sox genes find their feet. Curr Opin Genet Dev 7:338–344

    Article  PubMed  CAS  Google Scholar 

  • Schepers GE, Teasdale RD, Koopman P (2002) Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 3:167–170

    Article  PubMed  CAS  Google Scholar 

  • Shivdasani RA (2002) Molecular regulation of vertebrate early endoderm development. Dev Biol 249:191–203

    Article  PubMed  CAS  Google Scholar 

  • Sinner D, Rankin S, Lee M, Zorn AM (2004) Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 131:3069–3080

    Article  PubMed  CAS  Google Scholar 

  • Soullier S, Jay P, Poulat F, Vanacker JM, Berta P, Laudet V (1999) Diversification pattern of the HMG and SOX family members during evolution. J Mol Evol 48:517–527

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Taguchi S, Tagawa K, Humphreys T, Satoh N (2002) Group B sox genes that contribute to specification of the vertebrate brain are expressed in the apical organ and ciliary bands of hemichordate larvae. Zoolog Sci 19:57–66

    Article  PubMed  CAS  Google Scholar 

  • Tam PP, Kanai-Azuma M, Kanai Y (2003) Early endoderm development in vertebrates: lineage differentiation and morphogenetic function. Curr Opin Genet Dev 13:393–400

    Article  PubMed  CAS  Google Scholar 

  • Tardent P (1978) 5 Entwicklungsperioden. In: Seidel F (ed) Morphogenese der Tiere: Enleitung zum Gesamtwerk Morphogenetische Arbeitsmethoden und Begriffssysteme (Colenterata, Cnidaria). Fischer-Verlag, Jena, pp 199–222

    Google Scholar 

  • Uchikawa M, Kamachi Y, Kondoh H (1999) Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev 84:103–120

    Article  PubMed  CAS  Google Scholar 

  • Wegner M (1999) From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 27:1409–1420

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Jackle H (1990) The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell 63:455–456

    Article  PubMed  CAS  Google Scholar 

  • Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699

    PubMed  CAS  Google Scholar 

  • Wikramanayake AH, Hong M, Lee PN, Pang K, Byrum CA, Bince JM, Xu R, Martindale MQ (2003) An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation. Nature 426:446–450

    Article  PubMed  CAS  Google Scholar 

  • Wilson M, Koopman P (2002) Matching SOX: partner proteins and co-factors of the SOX family of transcriptional regulators. Curr Opin Genet Dev 12:441–446

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto M, Meno C, Sakai Y, Shiratori H, Mochida K, Ikawa Y, Saijoh Y, Hamada H (2001) The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior–posterior patterning and node formation in the mouse. Genes Dev 15:1242–1256

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Basta T, Hernandez-Lagunas L, Simpson P, Stemple DL, Artinger KB, Klymkowsky MW (2004) Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. Dev Biol 273:23–37

    Article  PubMed  CAS  Google Scholar 

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  1. Kewalo Marine Laboratory, Pacific Biomedical Research Center, University of Hawai'i, 41 Ahui St., Honolulu, HI, 96813, USA

    Craig R. Magie, Kevin Pang & Mark Q. Martindale

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  1. Craig R. Magie
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  2. Kevin Pang
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  3. Mark Q. Martindale
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Correspondence to Mark Q. Martindale.

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Communicated by D. Weisblat

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Magie, C.R., Pang, K. & Martindale, M.Q. Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis . Dev Genes Evol 215, 618–630 (2005). https://doi.org/10.1007/s00427-005-0022-y

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