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The Evolution of Gastrulation

The evolution of gastrulation was a pivotal event in metazoan evolution. The onset of gastrulation movements in a blastula-like “urmetazoan” most likely led to the evolution of development, with increased cell-cell interactions, and induction of differential gene expression, novel cell types, tissues and organs that rapidly drove the diversification of the metazoan. However, the developmental mechanism events that led to the evolution of gastrulation are poorly understood.

We are using Nematostella as a model organism to understand gastrulation in cnidarians, an early branching metazoan taxon. In Nematostella, archenteron invagination is initiated at the animal pole of the embryo. At the blastula stage, cells at the animal pole of the embryo develop into bottle cells, and this leads to the buckling of the epithelium and the formation of a primary archenteron. We have recently shown that bottle cell formation in Nematostella is regulated by NvStrabismus signaling in the Wnt/PCP pathway. NvStbm is maternally loaded and the protein is expressed at the animal pole of developing embryos. In early gastrula stage embryos, NvStbm is localized to the apical end of the forming bottle cells. We have shown that the knock-down of NvStbm using anti-sense morpholinos blocks the formation of bottle cells and primary archenteron invagination without affecting endoderm cell fate specification (Kumburegama et al. 2011).

Our current work on this project is focused on understanding how NvStbm is restricted to the animal pole in the zygote and during early development, and how NvStbm is “activated” in the Wnt/PCP pathways during bottle cell formation. Towards this goal we are characterizing the functions of all the conserved “core” components of Wnt/PCP signaling in Nematostella. We are also using anti-NvStbm antibodies to perform co-immunoprecipitation experiments to identify novel regulators of NvStbm function during bottle cell formation.  Based on our analysis of NvStbm function and other observations by us and others, we have recently proposed that gastrulation evolved in the “urmetazoan” by the localized activation of Wnt/PCP signaling at the animal pole, which led to the formation of bottle cells and the induction of primary archenteron invagination (Kumburegama et al. 2011).

Interestingly, our recent work has also shown that endoderm cell fate specification and primary archenteron invagination can be experimentally uncoupled in Nematostella, raising the possibility that the two processes could have evolved independently in metazoans (Kumburegama et al. 2011). We are actively investigating these ideas in the laboratory.

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