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.
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
Chipman AD, Stollewerk A (2006) Specification of neural precursor identity in the geophilomorph centipede Strigamia maritima. Dev Biol 290:337–350
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
Gamberi C, Peterson DS, He L, Gottlieb E (2002) An anterior function for the Drosophila posterior determinant Pumilio. Development 129:2699–2710
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
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
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
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
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
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
Pearson B, Doe C (2004) Specification of temporal identity in the developing nervous system. Annu Rev Cell Dev Biol 20:619–647
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
Rivera-Pomar R, Jäckle H (1996) From gradients to stripes in Drosophila embryogenesis: filling in the gaps. Trends Genet 12:478–483
Savage RM, Shankland M (1996) Identification and characterization of a hunchback ortholog, Lzf2, and its expression during leech embryogenesis. Dev Biol 175:205–217
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
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
Tessmar-Raible K, Arendt D (2003) Emerging systems: between vertebrates and arthropods, the lophotrochozoa. Curr Opin Genet Dev 13:331–340
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
Werbrock AH, Meiklejohn DA, Sainz A, Iwasa JH, Savage RM (2001) A polychaete hunchback ortholog. Dev Biol 235:476–488
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
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.
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Communicated by D.A. Weisblat
Pierre Kerner and Fabiola Zelada González contributed equally to this work.
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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
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DOI: https://doi.org/10.1007/s00427-006-0100-9