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

Patricia N. Lee, Shalika Kumburegama, Heather Q. Marlow, Mark Q. Martindale, Athula Wikramanayake

Research output: Contribution to journalArticle

85 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)169-186
Number of pages18
JournalDevelopmental Biology
Volume310
Issue number1
DOIs
StatePublished - Oct 1 2007
Externally publishedYes

Fingerprint

Cnidaria
Wnt Signaling Pathway
Ovum
Anthozoa
Gastrulation
Embryonic Development
Embryonic Structures
Sea Anemones
Catenins
Blastomeres
Endoderm
Zygote
Spermatozoa
Messenger RNA

Keywords

  • β-Catenin
  • Anthozoa
  • Axial properties
  • Cnidaria
  • Dishevelled
  • Nematostella vectensis
  • Polarity
  • Wnt

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. / Lee, Patricia N.; Kumburegama, Shalika; Marlow, Heather Q.; Martindale, Mark Q.; Wikramanayake, Athula.

In: Developmental Biology, Vol. 310, No. 1, 01.10.2007, p. 169-186.

Research output: Contribution to journalArticle

Lee, Patricia N. ; Kumburegama, Shalika ; Marlow, Heather Q. ; Martindale, Mark Q. ; Wikramanayake, Athula. / Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled. In: Developmental Biology. 2007 ; Vol. 310, No. 1. pp. 169-186.
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