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Axial patterning in cephalochordates and the evolution of the organizer

Abstract

The organizer of the vertebrate gastrula is an important signalling centre that induces and patterns dorsal axial structures. Although a topic of long-standing interest, the evolutionary origin of the organizer remains unclear. Here we show that the gastrula of the cephalochordate amphioxus expresses dorsal/ventral (D/V) patterning genes (for example, bone morphogenetic proteins (BMPs), Nodal and their antagonists) in patterns reminiscent of those of their vertebrate orthlogues, and that amphioxus embryos, like those of vertebrates, are ventralized by exogenous BMP protein. In addition, Wnt-antagonists (for example, Dkks and sFRP2-like) are expressed anteriorly, whereas Wnt genes themselves are expressed posteriorly, consistent with a role for Wnt signalling in anterior/posterior (A/P) patterning. These results suggest evolutionary conservation of the mechanisms for both D/V and A/P patterning of the early gastrula. In light of recent phylogenetic analyses placing cephalochordates basally in the chordate lineage, we propose that separate signalling centres for patterning the D/V and A/P axes may be an ancestral chordate character.

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Figure 1: Expression of genes for BMP signalling molecules during early amphioxus embryogenesis.
Figure 2: Expression of Nodal, the Nodal antagonist Lefty and organizer-related transcription factors in early amphioxus embryos.
Figure 3: Exogenous zebrafish BMP4 protein (zBMP4) ventralizes amphioxus embryos.
Figure 4: Expression of amphioxus Wnt8 and Wnt antagonists during embryogenesis.
Figure 5: Schematic diagram of the expression of dorso/ventral- and anterior/posterior-patterning genes at the late gastrula stage.

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Acknowledgements

We are indebted to J.M. Lawrence, University of South Florida, for providing laboratory facilities during the summer breeding season of amphioxus. This work was funded by grants from the National Science Foundation, USA (L.Z.H. and N.D.H.), the National Aeronautics and Space Administration, USA (M.B.-F. and L.Z.H.), the National Institutes of Health (M.B.-F.), MEXT, Japan (N.S. and Y.K.), and the 21st Century COE for the Biodiversity Research at Kyoto University (N.S.). J.-K.Y is currently supported by the Della Martin prize postdoctoral fellowship from the Division of Biology, California Institute of Technology, USA.

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Correspondence to Linda Z. Holland.

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EST sequences were deposited in the DDBJ/EMBL/GenBank databases. (DNA Data Bank of Japan accession numbers BW692960–BW954996). Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

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Supplementary Information

This file contains Supplementary Figures 1-11 with legends, Supplementary Table 1, Supplementary Methods and Supplementary Notes. Supplementary Figures include phylogenetic trees for amphioxus proteins and Supplementary Figure 11 shows expression of amphioxus Wnt3 and Wnt11 in early embryos. Supplementary Table 1 includes a list of each of the genes obtained from the EST data, the clone numbers, best hit and the numbers of each clone found in the EST data. Supplementary Methods include methods for phylogenetic analysis used for the trees in Supplementary Table I. Supplementary Notes include references for the Supplementary Methods. (PDF 702 kb)

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Yu, JK., Satou, Y., Holland, N. et al. Axial patterning in cephalochordates and the evolution of the organizer. Nature 445, 613–617 (2007). https://doi.org/10.1038/nature05472

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