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Asymmetric developmental potential along the animal–vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled
Open accessAbstract
The relationship between egg polarity and the adult body plan is well understood in many bilaterians. However, the evolutionary origins of embryonic polarity are not known. Insight into the evolution of polarity will come from understanding the ontogeny of polarity in non-bilaterian forms, such as cnidarians. We examined how the axial properties of the starlet sea anemone, Nematostella vectensis (Anthozoa, Cnidaria), are established during embryogenesis. Egg-cutting experiments and sperm localization show that Nematostella eggs are only fertilized at the animal pole. Vital marking experiments demonstrate that the egg animal pole corresponds to the sites of first cleavage and gastrulation, and the oral pole of the adult. Embryo separation experiments demonstrate an asymmetric segregation of developmental potential along the animal-vegetal axis prior to the 8-cell stage. We demonstrate that Dishevelled (Dsh) plays an important role in mediating this asymmetric segregation of developmental fate. Although NvDsh mRNA is ubiquitously expressed during embryogenesis, the protein is associated with the female pronucleus at the animal pole in the unfertilized egg, becomes associated with the unipolar first cleavage furrow, and remains enriched in animal pole blastomeres. Our results suggest that at least one mechanism for Dsh enrichment at the animal pole is through its degradation at the vegetal pole. Functional studies reveal that NvDsh is required for specifying embryonic polarity and endoderm by stabilizing beta-catenin in the canonical Wnt signaling pathway. The localization of Dsh to the animal pole in Nematostella and two other anthozoan cnidarians (scleractinian corals) provides a possible explanation for how the site of gastrulation has changed in bilaterian evolution while other axial components of development have remained the same and demonstrates that modifications of the Wnt signaling pathway have been used to pattern a wide variety of metazoan embryos.
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“While the posterior-anterior gradient of expression of Wnt ligands in larval and adult eumetazoans reflects the conserved role in axial patterning, the earliest function of the canonical Wnt pathway (signalling through b-catenin) is specification of the endomesoderm 19,51,52 .”
From Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans (2014) · cites this paper as [52]
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Metadata
- Authors
- Lee, P. N., Kumburegama, S., Marlow, H. Q., Martindale, M. Q., & Wikramanayake, A. H.
- Affiliations
- University of Hawaiʻi at Mānoa (US)
- Corresponding author
- Wikramanayake, Athula H.
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 310
- Issue
- 1
- Pages
- 169-186
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2159606671
- Cited by
- 135
- References
- 74
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 2 · 2023: 1 · 2022: 7 · 2021: 10 · 2020: 2 · 2019: 4 · 2018: 8 · 2017: 9 · 2016: 8 · 2015: 6 · 2014: 8 · 2013: 9 · 2012: 7
- FWCI
- 4.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (IBN03-46249)
- National Institutes of Health (F32 GM066559-03)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Keywords
- Nematostella vectensis, Dishevelled, animal-vegetal axis, embryonic polarity, Wnt signaling, β-catenin, gastrulation, endoderm specification, first cleavage, egg polarity, scleractinian corals
- MeSH terms
- Dishevelled Proteins, Animals, Cnidaria, Embryo, Nonmammalian, Phosphoproteins, Sea Anemones, Signal Transduction, Body Patterning, Adaptor Proteins, Signal Transducing, Wnt Proteins, Gastrulation
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