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Unexpected complexity of the Wnt gene family in a sea anemone

Abstract

The Wnt gene family encodes secreted signalling molecules that control cell fate in animal development and human diseases1. Despite its significance, the evolution of this metazoan-specific protein family is unclear. In vertebrates, twelve Wnt subfamilies were defined, of which only six have counterparts in Ecdysozoa (for example, Drosophila and Caenorhabditis)2. Here, we report the isolation of twelve Wnt genes from the sea anemone Nematostella vectensis3, a species representing the basal group4 within cnidarians. Cnidarians are diploblastic animals and the sister-group to bilaterian metazoans5. Phylogenetic analyses of N. vectensis Wnt genes reveal a thus far unpredicted ancestral diversity within the Wnt family2,6,7. Cnidarians and bilaterians have at least eleven of the twelve known Wnt gene subfamilies in common; five subfamilies appear to be lost in the protostome lineage. Expression patterns of Wnt genes during N. vectensis embryogenesis indicate distinct roles of Wnts in gastrulation, resulting in serial overlapping expression domains along the primary axis of the planula larva. This unexpectedly complex inventory of Wnt family signalling factors evolved in early multi-cellular animals about 650 million years (Myr) ago, predating the Cambrian explosion by at least 100 Myr (refs 5, 8). It emphasizes the crucial function of Wnt genes in the diversification of eumetazoan body plans9.

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Figure 1: Bayesian inference consensus tree of the Wnt gene family.
Figure 2: Expression of N. vectensis Wnt genes during embryogenesis.
Figure 3: Overlapping expression domains of Wnt genes in a N. vectensis planula.

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Acknowledgements

This work was supported by grants from NASA and the NSF to M.Q.M. and the German Science Foundation (DFG) to U.T., B.H. and T.W.H. Some computations were carried out on the JUMP supercomputer at the ZAM/NIC of the Research Center Jülich. We thank A. Busch and C. Niehrs for critically reading the manuscript.

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Correspondence to Mark Q. Martindale or Thomas W. Holstein.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

A ML tree of Wnt gene phylogeny reconstructed with TREE-PUZZLE using the JTT model with default settings. (PDF 206 kb)

Supplementary Figure S2

A ML tree of Wnt gene phylogeny reconstructed with the IQPNNI program assuming 8 G-distributed mutation rates with the JTT model of evolution. (PDF 212 kb)

Supplementary Figure S3

A 50% majority-rule consensus tree of Wnt gene phylogeny reconstructed from 1000 bootstrap samples with PAUP*. (PDF 204 kb)

Supplementary Figure S4

Asymmetrical Expression of the NvWntA gene in Nematostella vectensis embryos. (JPG 34 kb)

Supplementary Figure S5

Expression of NvWnt7 in Nematostella vectensis embryos. (JPG 33 kb)

Supplementary Figure S6

Expression of NvWnt5 in Nematostella vectensis embryos. (JPG 70 kb)

Supplementary Table 1

Accession numbers and list of Wnt sequences used in the phylogenetic reconstructions. (PDF 956 kb)

Supplementary Table 2

Alignment of Wnt sequences from Nematostella vectensis, and representative bilaterians used in the phylogenetic reconstructions. (PDF 1277 kb)

Supplementary Methods

Detailed description of phylogenetic methods used in this study. (DOC 26 kb)

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Kusserow, A., Pang, K., Sturm, C. et al. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433, 156–160 (2005). https://doi.org/10.1038/nature03158

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  • DOI: https://doi.org/10.1038/nature03158

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