Asymmetric developmental potential along the animal–vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled

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...

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Veröffentlicht in:Developmental biology 2007-10, Vol.310 (1), p.169-186
Hauptverfasser: Lee, Patricia N., Kumburegama, Shalika, Marlow, Heather Q., Martindale, Mark Q., Wikramanayake, Athula H.
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container_start_page 169
container_title Developmental biology
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creator Lee, Patricia N.
Kumburegama, Shalika
Marlow, Heather Q.
Martindale, Mark Q.
Wikramanayake, Athula H.
description 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 β-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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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 . 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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 β-catenin in the canonical Wnt signaling pathway . 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subjects Adaptor Proteins, Signal Transducing - physiology
Animals
Anthozoa
Axial properties
Body Patterning
Cnidaria
Dishevelled
Dishevelled Proteins
Embryo, Nonmammalian - embryology
Embryo, Nonmammalian - physiology
Gastrulation - physiology
Marine
Nematostella vectensis
Phosphoproteins - physiology
Polarity
Scleractinia
Sea Anemones - embryology
Signal Transduction
Wnt
Wnt Proteins - physiology
β-Catenin
title Asymmetric developmental potential along the animal–vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled
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