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Science 329 (5989): 339-342

Copyright © 2010 by the American Association for the Advancement of Science

Hedgehog Signaling Regulates Segment Formation in the Annelid Platynereis

Nicolas Dray,1,*,{dagger} Kristin Tessmar-Raible,2,3,* Martine Le Gouar,1,* Laura Vibert,1 Foteini Christodoulou,3 Katharina Schipany,2 Aurélien Guillou,4 Juliane Zantke,2 Heidi Snyman,3 Julien Béhague,1,4 Michel Vervoort,1,4 Detlev Arendt,3 Guillaume Balavoine1,4,{ddagger}

Abstract: Annelids and arthropods share a similar segmented organization of the body whose evolutionary origin remains unclear. The Hedgehog signaling pathway, prominent in arthropod embryonic segment patterning, has not been shown to have a similar function outside arthropods. We show that the ligand Hedgehog, the receptor Patched, and the transcription factor Gli are all expressed in striped patterns before the morphological appearance of segments in the annelid Platynereis dumerilii. Treatments with small molecules antagonistic to Hedgehog signaling disrupt segment formation. Platynereis Hedgehog is not necessary to establish early segment patterns but is required to maintain them. The molecular similarity of segment patterning functions of the Hedgehog pathway in an annelid and in arthropods supports a common origin of segmentation in protostomes.

1 Centre de Génétique Moléculaire du CNRS, FRE 3144, Avenue de la Terrasse, 91189 Gif-sur-Yvette, France.
2 Max F. Perutz Laboratories, Universität Wien, Dr. Bohr-Gasse 9, 1030 Vienna, Austria.
3 Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg 69117, Germany.
4 Institut Jacques Monod, CNRS—Université Paris–Diderot, 15 rue Hélène Brion, 75205 Paris cedex 13, France.

* These authors contributed equally to this work.

{dagger} Present address: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520–8103, USA.

{ddagger} To whom correspondence should be addressed. E-mail: balavoine.guillaume{at}ijm.univ-paris-diderot.fr

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii.
O. Simakov, T. A. Larsson, and D. Arendt (2012)
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Evolutionary crossroads in developmental biology: annelids.
D. E. K. Ferrier (2012)
Development 139, 2643-2653
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A Segmentation Clock with Two-Segment Periodicity in Insects.
A. F. Sarrazin, A. D. Peel, and M. Averof (2012)
Science 336, 338-341
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Extensive Chordate and Annelid Macrosynteny Reveals Ancestral Homeobox Gene Organization.
J. H. L. Hui, C. McDougall, A. S. Monteiro, P. W. H. Holland, D. Arendt, G. Balavoine, and D. E. K. Ferrier (2012)
Mol. Biol. Evol. 29, 157-165
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Notch/Delta signalling is not required for segment generation in the basally branching insect Gryllus bimaculatus.
F. Kainz, B. Ewen-Campen, M. Akam, and C. G. Extavour (2011)
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