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Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica

Nature volume 431, pages 67–71 (2004)Cite this article

Abstract

Tunicate embryos and larvae have small cell numbers and simple anatomical features in comparison with other chordates, including vertebrates. Although they branch near the base of chordate phylogenetic trees1, their degree of divergence from the common chordate ancestor remains difficult to evaluate. Here we show that the tunicate Oikopleura dioica has a complement of nine Hox genes in which all central genes are lacking but a full vertebrate-like set of posterior genes is present. In contrast to all bilaterians studied so far, Hox genes are not clustered in the Oikopleura genome. Their expression occurs mostly in the tail, with some tissue preference, and a strong partition of expression domains in the nerve cord, in the notochord and in the muscle. In each tissue of the tail, the anteroposterior order of Hox gene expression evokes spatial collinearity, with several alterations. We propose a relationship between the Hox cluster breakdown, the separation of Hox expression domains, and a transition to a determinative mode of development.

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Figure 1: Evolutionary relationship of the Hox and ParaHox homeodomain sequences inferred by the neighbour-joining method.
Figure 2: Expression patterns of Oikopleura Hox genes at 4 h after fertilization.
Figure 3: Genomic organization of the Oikopleura Hox genes, indicating total Hox cluster breakdown.
Figure 4: Discrete changes of Hox gene complements in chordates.

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Acknowledgements

We thank A. Adoutte for advice throughout the course of this work; R. Aasland, M. Schartl, T. Stach and E. Thompson for their comments at several stages of manuscript preparation; and the personnel of the Oikopleura culture facility for technical support. Funding was provided by the Research Council of Norway and the University of Bergen in the frame of the Sars Centre – EMBL partnership contract.

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Authors and Affiliations

  1. Sars Centre for Marine Molecular Biology, Bergen High Technology Centre, Thormøhlensgaten 55, 5008, Bergen, Norway

    Hee-Chan Seo, Rolf Brudvik Edvardsen, Anne Dorthea Maeland, Marianne Bjordal, Marit Flo Jensen, Anette Hansen, Mette Flaat & Daniel Chourrout

  2. Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195, Berlin, Germany

    Hans Lehrach & Richard Reinhardt

  3. Genoscope-Centre National de Sequencage and CNRS UMR-8030, 91000, Evry, France

    Jean Weissenbach & Patrick Wincker

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  1. Hee-Chan Seo
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Supplementary information

Supplementary Figure 1

Coverage of Oikopleura genes by whole-genome shotgun data, measured by the coverage of a non-redundant collection of expressed sequence tags. (DOC 35 kb)

Supplementary Figure 2

Tandem duplication of the Hox4 gene. (JPG 58 kb)

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Seo, HC., Edvardsen, R., Maeland, A. et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431, 67–71 (2004). https://doi.org/10.1038/nature02709

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