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Evolution of Axis Specification Mechanisms in Jawed Vertebrates: Insights from a Chondrichthyan

Coolen, Marion and Sauka-Spengler, Tatjana and Nicolle, Delphine and Le-Mentec, Chantal and Lallemand, Yvan and Da Silva, Corinne and Plouhinec, Jean-Louis and Robert, Benoît and Wincker, Patrick and Shi, De-Li and Mazan, Sylvie (2007) Evolution of Axis Specification Mechanisms in Jawed Vertebrates: Insights from a Chondrichthyan. PLoS ONE, 2 (4). e374. ISSN 1932-6203. https://resolver.caltech.edu/CaltechAUTHORS:COOplosone07

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Abstract

The genetic mechanisms that control the establishment of early polarities and their link with embryonic axis specification and patterning seem to substantially diverge across vertebrates. In amphibians and teleosts, the establishment of an early dorso-ventral polarity determines both the site of axis formation and its rostro-caudal orientation. In contrast, amniotes retain a considerable plasticity for their site of axis formation until blastula stages and rely on signals secreted by extraembryonic tissues, which have no clear equivalents in the former, for the establishment of their rostro-caudal pattern. The rationale for these differences remains unknown. Through detailed expression analyses of key development genes in a chondrichthyan, the dogfish Scyliorhinus canicula, we have reconstructed the ancestral pattern of axis specification in jawed vertebrates. We show that the dogfish displays compelling similarities with amniotes at blastula and early gastrula stages, including the presence of clear homologs of the hypoblast and extraembryonic ectoderm. In the ancestral state, these territories are specified at opposite poles of an early axis of bilateral symmetry, homologous to the dorso-ventral axis of amphibians or teleosts, and aligned with the later forming embryonic axis, from head to tail. Comparisons with amniotes suggest that a dorsal expansion of extraembryonic ectoderm, resulting in an apparently radial symmetry at late blastula stages, has taken place in their lineage. The synthesis of these results with those of functional analyses in model organisms supports an evolutionary link between the dorso-ventral polarity of amphibians and teleosts and the embryonic-extraembryonic organisation of amniotes. It leads to a general model of axis specification in gnathostomes, which provides a comparative framework for a reassessment of conservations both among vertebrates and with more distant metazoans.


Item Type:Article
Additional Information:Copyright: © 2007 Coolen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: January 11, 2007; Accepted: March 22, 2007; Published: April 18, 2007. Academic Editor: Hernan Lopez-Schier, Centre de Regulacio Genomica - Barcelona Biomedical Research Park, Spain. We are grateful to Sébastien Paturance (UPS 44, Orléans) who optimised conditions for dogfish embryo maintenance, Laurent Lévèque and Bernard Kloareg (Station Biologique de Roscoff), who provided dogfish embryos. We also thank Fabrice Girardot for initiating expression analyses of Otx1 and Otx2 in dogfish embryos, Jim Langeland for sharing expertise in cDNA library construction and the Génoscope staff for taking in charge the transcriptome analysis. Author Contributions: Conceived and designed the experiments: MC TS. Performed the experiments: MC TS. Analyzed the data: SM MC TS JP. Wrote the paper: SM MC. Other: Took in charge the EST sequencing project: PW. Conducted the work: SM. Bred the mice and provided litters: BR YL. Took in charge the EST sequencing project: CD. Carried out injections into xenopus embryos: DS. Provided technical help in molecular biology and histology: CL DN. Funding: EST sequencing was funded by CNRG. This work was supported by a Groupement d'Intérêt Scientifique “Génomique marine”, the Centre National de la Recherche Scientifique, Université Paris-Sud and Université d'Orléans. T.S.S., J.L.P. and M.C. were recipients of MRT, AMX and BDI-CNRS fellowships respectively. Competing interests: The authors have declared that no competing interests exist.
Issue or Number:4
Record Number:CaltechAUTHORS:COOplosone07
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:COOplosone07
Alternative URL:http://dx.doi.org/10.1371/journal.pone.0000374
Official Citation:Coolen M, Sauka-Spengler T, Nicolle D, Le-Mentec C, Lallemand Y, et al. (2007) Evolution of Axis Specification Mechanisms in Jawed Vertebrates: Insights from a Chondrichthyan. PLoS ONE 2(4): e374. doi:10.1371/journal.pone.0000374
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:9946
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:28 Mar 2008
Last Modified:03 Oct 2019 00:05

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