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Expression of developmental genes during early embryogenesis of Hydra

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Abstract

Hydra is a classical model to study key features of embryogenesis such as axial patterning and stem cell differentiation. In contrast to other organisms where these mechanisms are active only during embryonic development, in Hydra they can be studied in adults. The underlying assumption is that the machinery governing adult patterning mimics regulatory mechanisms which are also active during early embryogenesis. Whether, however, Hydra embryogenesis is governed by the same mechanisms which are controlling adult patterning, remains to be shown. In this paper, in precisely staged Hydra embryos, we examined the expression pattern of 15 regulatory genes shown previously to play a role in adult patterning and cell differentiation. RT-PCR revealed that most of the genes examined were expressed in rather late embryonic stages. In situ hybridization, nuclear run-on experiments, and staining of nucleolar organizer region-associated proteins indicated that genes expressed in early embryos are transcribed in the engulfed "nurse cells" (endocytes). This is the first direct evidence that endocytes in Hydra not only provide nutrients to the developing oocyte but also produce maternal factors critical for embryogenesis. Our findings are an initial step towards understanding the molecular machinery controlling embryogenesis of a key group of basal metazoans and raise the possibility that in Hydra there are differences in the mechanisms controlling embryogenesis and adult patterning.

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References

  • Bachvarova RF, Masi T, Hall L, Johnson AD (2001) Expression of Axwnt-8 and Axszl in the urodele, axolotl: comparison with Xenopus. Dev Genes Evol 211(10):501–505

    Article  CAS  PubMed  Google Scholar 

  • Bode PM, Bode HR (1984) Patterning in hydra. In: Malacinski GM, Bryant SV (eds) Pattern formation. A primer in developmental biology. Macmillan, New York

  • Bosch TCG (2003) Ancient signals: peptides and the interpretation of positional information in ancestral metazoans. Comp Biochem Physiol (in press)

    Google Scholar 

  • Bosch TCG, Fujisawa T (2001) Polyps, peptides and patterning. BioEssays 23(5):420–427

    Article  CAS  PubMed  Google Scholar 

  • Bosch TCG, Khalturin K (2002) Patterning and cell differentiation in Hydra: novel genes and the limits to conservation. Can J Zool 80(10):1670–1677

    Article  CAS  Google Scholar 

  • Broun M, Bode HR (2002) Characterization of the head organizer in Hydra. Development 129:875–884

    CAS  PubMed  Google Scholar 

  • Broun M, Sokol S, Bode HR (1999) Cngsc, a homologue of goosecoid, participates in the patterning of the head, and is expressed in the organizer region of Hydra. Development 126:5245–5254

    CAS  PubMed  Google Scholar 

  • Cadigan KM (2002) Wnt signaling--20 years and counting Trends Genet 18(7):340–342

    Google Scholar 

  • Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11(24):3286–3305

    PubMed  Google Scholar 

  • Corbo JC, Levine M, Zeller RW (1997) Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124:589–602

    CAS  PubMed  Google Scholar 

  • Endl I, Lohmann JU, Bosch TCG (1999) Head specific gene expression in Hydra: Complexity of DNA/protein interactions at the promoter of ks1 is inversely correlated to the head activation potential. Proc Natl Acad Sci USA 96:1445–1450

    Article  CAS  PubMed  Google Scholar 

  • Gellner K, Praetzel G, Bosch TCG (1992) Cloning and expression of an heat inducible hsp70 gene in two species of hydra which differ in their stress response. Eur J Biochem 210:683–691

    CAS  PubMed  Google Scholar 

  • Gierer A (1974) Hydra as a model for the development of biological form. Sci Am 231:44–55

    CAS  Google Scholar 

  • Grens A, Gee L, Fisher DA, Bode HR (1996) CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra. Dev Biol 180:473–488

    Article  CAS  PubMed  Google Scholar 

  • Hermans-Borgmeyer I, Schinke B, Schaller HC, Hoffmeister-Ullerich SA (1996) Isolation of a marker for head-specific cell differentiation in hydra. Differentiation 61(2):95–101

    Article  CAS  PubMed  Google Scholar 

  • Hobmayer B, Rentzsch F, Kuhn K, Happel CM, Cramer von Laue C, Snyder P, Rothbächer U, Holstein TW (2000) WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407:186–189

    Google Scholar 

  • Honegger TG, Zürrer D, Tardent P (1989) Oogenesis in Hydra carnea: A new model based on light and electron microscopic analyses of oocyte and nurse cell differentiation. Tissue Cell 21:381–393

    Google Scholar 

  • Kleinenberg N (1872) Hydra. Eine anatomisch-entwicklungsgeschichtliche Untersuchung. Engelmann, Leipzig, pp 1–90

  • Kuznetsov SG, Anton-Erxleben F, Bosch TCG (2002) Epithelial interactions in Hydra: apoptosis in interspecies grafts is induced by detachment from the extracellular matrix. J Exp Biol 205(24):3809–3817

    PubMed  Google Scholar 

  • Lall S, Ludwig MZ, Patel NH (2003) Nanos plays a conserved role in axial patterning outside the Diptera. Curr Biol 13:224–229

    Article  CAS  PubMed  Google Scholar 

  • Lohmann JU, Bosch TCG (2000) The novel peptide HEADY specifies apical fate in a simple, radially symmetric metazoan. Genes Development 14:2771–2777

    Article  CAS  PubMed  Google Scholar 

  • Martin VJ, Littlefield CL, Archer WE, Bode HR (1997) Embryogenesis in hydra. Biol Bull 192(3):345–363

    CAS  PubMed  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(2):523–536

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Technau U, Smith KM, Steele RE (2000) Oocyte development in Hydra involves selection from competent precursor cells. Dev Biol 224(2):326–338

    Article  CAS  PubMed  Google Scholar 

  • Minobe S, Fei K, Yan L, Sarras MP, Werle MJ (2000) Identification and characterization of the epithelial polarity receptor "Frizzled" in Hydra vulgaris. Dev Genes Evol 210:258–262

    Article  CAS  PubMed  Google Scholar 

  • Mochizuki K, Sano H, Kobayashi S, Nishimiya-Fujisawa C, Fujisawa T (2000) Expression and evolutionary conservation of nanos-related genes in Hydra. Dev Genes Evol 210(12):591–602

    Article  CAS  PubMed  Google Scholar 

  • Öfner D, Riedmann B, Maier H, Hittmair A, Rumer A, Totsch M, Spechtenhauser B, Bocker W, Schmid KW (1995) Standardized staining and analysis of argyrophilic nucleolar organizer region associated proteins (AgNORs) in radically resected colorectal adenocarcinoma--correlation with tumour stage and long-term survival. J Pathol 175(4):441–448

    PubMed  Google Scholar 

  • Shenk MA, Bode HR, Steele RE (1993a) Expression of Cnox-2, a HOM/HOX homeobox gene in Hydra is correlated with axial pattern formation. Development 117:657–667

    CAS  PubMed  Google Scholar 

  • Shenk MA, Gee L, Steele RE, Bode HR (1993b) Expression of Cnox-2, a HOM/HOX gene, is suppressed during head formation in Hydra. Dev Biol 160:108–118

    Article  CAS  PubMed  Google Scholar 

  • Smith KM, Gee L, Blitz IL, Bode HR (1999) CnOtx, a member of the Otx gene family, has a role in cell movement in hydra. Dev Biol 212(2):392–404

    Article  CAS  PubMed  Google Scholar 

  • Smith KM, Gee L, Bode HR (2000) HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra. Development 127:4743–4752

    CAS  PubMed  Google Scholar 

  • Steele RE (2002) Developmental signaling in Hydra: what does it take to build a "simple" animal"? Dev Biol 248(2):199–219

    Google Scholar 

  • Takahashi T, Muneoka Y, Lohmann J, deHaro LM, Solleder G, Bosch TCG, David CN, Bode HR, Koizumi O, Shimizu H, Hatta M, Fujisawa T, Sugiyama T (1997) Systematic isolation of peptide signal molecules regulating development in hydra: LWamide and PW families. Proc Natl Acad Sci USA 94:12451–1246

    Google Scholar 

  • Tardent P (1974) Gametogenesis in the genus Hydra. Am Zool 14:447–456

    Google Scholar 

  • Tardent P (1985) The differentiation of germ cells in Cnidaria. In: The origin and evolution of sex. Liss, New York, pp 163–197

  • Technau U, Bode HR (1999) Hybra1, a Brachyury homologue acts during head formation in Hydra. Development 126:999–1010

    CAS  PubMed  Google Scholar 

  • Technau U, Cramer von Laue C, Rentzsch F, Luft S, Hobmayer B, Bode HR, Holstein TW (2000) Parameters of self-organization in Hydra aggregates. Proc Natl Acad Sci USA 97(22):12127–12131

    Article  CAS  PubMed  Google Scholar 

  • Wodarz A, Nusse R (1998) Mechanisms of Wnt signalling in development. Annu Rev Cell Dev Biol 14:59–88

    CAS  PubMed  Google Scholar 

  • Zihler J (1972) Zur Gametogenese und Befruchtungsbiologie von Hydra. Wilhelm Roux Arch Entwicklungsmech Org 169:239–267

    Google Scholar 

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Acknowledgements

A.C.F. acknowledges Katrin Thamm for help with the in situ hybridizations on Hydra embryos. We would like to thank Antje Thomas for excellent technical assistance. We are grateful to Ulrich Technau for sharing unpublished observations on Hydra embryos and we thank him and Matthias Habetha for critical comments on the manuscript. Supported by grants from the Deutsche Forschungsgemeinschaft (to T.C.G.B.). G.G. is recipient of a Ph.D. fellowship from the Daimler-Benz foundation.

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  1. Andreas C. Fröbius

    Present address: Kewalo Marine Lab, Pacific Biomedical Research Center, University of Hawai'i, 41 Ahui Street, Honolulu, HI, 96813, USA

Authors and Affiliations

  1. Zoological Institute, Christian-Albrechts-University Olshausenstrasse 40, 24098, Kiel, Germany

    Andreas C. Fröbius, Gregory Genikhovich, Ulrich Kürn, Friederike Anton-Erxleben & Thomas C. G. Bosch

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  1. Andreas C. Fröbius
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  2. Gregory Genikhovich
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Correspondence to Thomas C. G. Bosch.

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Fröbius, A.C., Genikhovich, G., Kürn, U. et al. Expression of developmental genes during early embryogenesis of Hydra . Dev Genes Evol 213, 445–455 (2003). https://doi.org/10.1007/s00427-003-0344-6

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