The expression of a hunchback ortholog in the polychaete annelid Platynereis dumerilii suggests an ancestral role in mesoderm development and neurogenesis (original) (raw)

Abstract

Orthologs of the Drosophila gap gene hunchback have been isolated so far only in protostomes. Phylogenetic analysis of recently available genomic data allowed us to confirm that hunchback genes are widely found in protostomes (both lophotrochozoans and ecdysozoans). In contrast, no unequivocal hunchback gene can be found in the genomes of deuterostomes and non-bilaterians. We cloned hunchback in the marine polychaete annelid Platynereis dumerilii and analysed its expression during development. In this species, hunchback displays an expression pattern indicative of a role in mesoderm formation and neurogenesis, and similar to the expression found for hunchback genes in arthropods. These data suggest altogether that these functions are ancestral to protostomes.

Access this article

Log in via an institution

Subscribe and save

• Get 10 units per month
• Download Article/Chapter or eBook
• 1 Unit = 1 Article or 1 Chapter
• Cancel anytime Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

• Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
  Article PubMed CAS Google Scholar
• Chipman AD, Stollewerk A (2006) Specification of neural precursor identity in the geophilomorph centipede Strigamia maritima. Dev Biol 290:337–350
  Article PubMed CAS Google Scholar
• Fay DS, Stanley HM, Han M, Wood WB (1999) A Caenorhabditis elegans homologue of hunchback is required for late stages of development but not early embryonic patterning. Dev Biol 205:240–253
  Article PubMed CAS Google Scholar
• Gamberi C, Peterson DS, He L, Gottlieb E (2002) An anterior function for the Drosophila posterior determinant Pumilio. Development 129:2699–2710
  PubMed CAS Google Scholar
• Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
  Article PubMed Google Scholar
• Iwasa JH, Suver DW, Savage RM (2000) The leech hunchback protein is expressed in the epithelium and CNS but not in the segmental precursor lineages. Dev Gen Evol 210:277–288
  Article CAS Google Scholar
• Kontarakis Z, Copf T, Averof M (2005) Expression of hunchback during trunk segmentation in the branchiopod crustacean Artemia franciscana. Dev Gen Evol 22:1–5
  Google Scholar
• Liu PZ, Kaufman TC (2004) hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Development 131:1515–1527
  Article PubMed CAS Google Scholar
• Mito T, Sarashina I, Zhang H, Iwahashi A, Okamoto H, Miyawaki K, Shinmyo Y, Ohuchi H, Noji S (2005) Non-canonical functions of hunchback in segment patterning of the intermediate germ cricket Gryllus bimaculatus. Development 132:2069–2079
  Article PubMed CAS Google Scholar
• Patel NH, Hayward DC, Lall S, Pirkl NR, DiPietro D, Ball EE (2001) Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128:3459–3472
  PubMed CAS Google Scholar
• Pearson B, Doe C (2004) Specification of temporal identity in the developing nervous system. Annu Rev Cell Dev Biol 20:619–647
  Article PubMed CAS Google Scholar
• Pultz MA, Westendorf L, Gale SD, Hawkins K, Lynch J, Pitt JN, Reeves NL, Yao JC, Small S, Desplan C, Leaf DS (2005) A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132:3705–3715
  Article PubMed CAS Google Scholar
• Rivera-Pomar R, Jäckle H (1996) From gradients to stripes in Drosophila embryogenesis: filling in the gaps. Trends Genet 12:478–483
  Article PubMed CAS Google Scholar
• Savage RM, Shankland M (1996) Identification and characterization of a hunchback ortholog, Lzf2, and its expression during leech embryogenesis. Dev Biol 175:205–217
  Article PubMed CAS Google Scholar
• Shimizu T, Savage RM (2002) Expression of hunchback protein in a subset of ectodermal teloblasts of the oligochaete annelid Tubifex. Dev Gen Evol 212:520–525
  Article CAS Google Scholar
• Sommer RJ, Retzlaff M, Goerlich K, Sander K, Tautz D (1992) Evolutionary conservation pattern of zinc-finger domains of Drosophila segmentation genes. Proc Natl Acad Sci U S A 89:10782–10786
  Article PubMed CAS Google Scholar
• Tessmar-Raible K, Arendt D (2003) Emerging systems: between vertebrates and arthropods, the lophotrochozoa. Curr Opin Genet Dev 13:331–340
  Article PubMed CAS Google Scholar
• Thompson JD, Higgins JD, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
  PubMed CAS Google Scholar
• Werbrock AH, Meiklejohn DA, Sainz A, Iwasa JH, Savage RM (2001) A polychaete hunchback ortholog. Dev Biol 235:476–488
  Article PubMed CAS Google Scholar
• Wolff C, Sommer R, Schroder R, Glaser G, Tautz D (1995) Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121:4227–4236
  PubMed CAS Google Scholar

Download references

Acknowledgments

This work has been supported by the CNRS and the Ministère Français de la Recherche through its ACI ‘Jeunes chercheurs et jeunes chercheuses’ and ACI ‘Biologie et Physiologie du développement’ (to M.V.). F.Z.G. was financially supported during her Ph.D. thesis by the DFG (Deutsche Forschungsgemeinschaft). P.K. holds a ‘Bourse pour Docteur-Ingénieur’ from the CNRS. V.L. was supported by the Belgian Science Policy.

Author information

Author notes

1. Fabiola Zelada González
   Present address: Centre d´Immunologie Marseille-Luminy (CIML), Parc Scientifique de Luminy. Case 906, 13288, Marseille Cedex 09, France

Authors and Affiliations

1. Laboratoire Evolution et Développement des protostomiens, Centre de Génétique Moléculaire-CNRS UPR 2167, 1, av. de la terrasse, 91198, Gif-sur-Yvette cedex, France
   Pierre Kerner, Martine Le Gouar & Michel Vervoort
2. European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, 69012, Heidelberg, Germany
   Fabiola Zelada González & Detlev Arendt
3. Belgian EMBnet Node-Laboratoire de Bioinformatique, Institut de Biologie et de Médecine Moléculaires, Université Libre de Bruxelles, Rue des Professeurs Jeener et Brachet 12, 6041, Gosselies, Belgium
   Valérie Ledent
4. UFR de Biologie et Sciences de la Nature, Université Paris 7-Denis Diderot, 2 place Jussieu, 75251, Paris Cedex 05, France
   Michel Vervoort

Authors

1. Pierre Kerner
   You can also search for this author inPubMed Google Scholar
2. Fabiola Zelada González
   You can also search for this author inPubMed Google Scholar
3. Martine Le Gouar
   You can also search for this author inPubMed Google Scholar
4. Valérie Ledent
   You can also search for this author inPubMed Google Scholar
5. Detlev Arendt
   You can also search for this author inPubMed Google Scholar
6. Michel Vervoort
   You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toMichel Vervoort.

Additional information

Communicated by D.A. Weisblat

Pierre Kerner and Fabiola Zelada González contributed equally to this work.

Rights and permissions

About this article

Cite this article

Kerner, P., Zelada González, F., Le Gouar, M. et al. The expression of a hunchback ortholog in the polychaete annelid Platynereis dumerilii suggests an ancestral role in mesoderm development and neurogenesis.Dev Genes Evol 216, 821–828 (2006). https://doi.org/10.1007/s00427-006-0100-9

Download citation

• Received: 03 April 2006
• Accepted: 05 July 2006
• Published: 16 September 2006
• Issue Date: December 2006
• DOI: https://doi.org/10.1007/s00427-006-0100-9

Keywords