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Conservation and diversification of Wnt signaling function during the evolution of nematode vulva development

Abstract

Cell-fate specification and cell-cell signaling have been well studied during vulva development in Caenorhabditis elegans and provide a paradigm in evolutionary developmental biology1,2. Pristionchus pacificus has been developed as a 'satellite' organism with an integrated physical and genetic map that allows detailed comparisons to C. elegans3,4,5. A common aspect of vulva formation in both species is the polarization of the P7.p lineage, which is responsible for vulval symmetry. In C. elegans, Wnt signaling is crucial for P7.p cell-fate patterning6; nothing is known about vulval symmetry in P. pacificus. We isolated mutations that disrupt polarization of the P7.p lineage in P. pacificus and found that the corresponding gene encodes a Frizzled-like molecule. In addition, mutations in Ppa-lin-17 (encoding Frizzled) and morpholino knock-down of Ppa-lin-44 (encoding Wnt), Ppa-egl-20 (encoding Wnt), Ppa-mig-5 (encoding Dsh), Ppa-apr-1 (encoding APC) and Ppa-bar-1 (encoding β-catenin) results in gonad-independent vulva differentiation, indicating that these genes have a role in a negative signaling process. In contrast, in C. elegans, Wnt signaling has a positive role in vulva induction, and mutations in bar-1 result in a hypoinduced phenotype7. Therefore, whereas the molecular mechanisms that generate vulval symmetry are conserved, the genetic control of vulva induction diversified during evolution.

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Figure 1: Schematic summary of the position, fate and cell lineage of ventral epidermal cells in C. elegans
Figure 2: Molecular characterization of Ppa-lin-17.

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Acknowledgements

We thank A. Gutierrez and J. Srinivasan for help with the original cloning of Ppa-lin-44, Ppa-egl-20, Ppa-mig-5 and Ppa-apr-1; A. Rojas-Munoz for the zebrafish morpholino; R. Hong, A. Pires-daSilva, D. Rudel and A. Streit for critically reading the manuscript; and members of the laboratory of R.J.S. for discussions.

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Correspondence to Ralf J Sommer.

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The authors declare no competing financial interests.

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Supplementary Fig. 1

Amino acid sequence comparison of egl-20, lin-44, mig-5, apr-1, bar-1 and lin-18 between P. pacificus and C. elegans. (PDF 5328 kb)

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Zheng, M., Messerschmidt, D., Jungblut, B. et al. Conservation and diversification of Wnt signaling function during the evolution of nematode vulva development. Nat Genet 37, 300–304 (2005). https://doi.org/10.1038/ng1512

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