Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression

Abstract

Gastrulation is a central event in metazoan development, involving many cellular behaviors including invagination, delamination, and ingression. Understanding the cell biology underlying gastrulation in many different taxa will help clarify the evolution of gastrulation mechanisms. Gastrulation in the anthozoan cnidarian Nematostella vectensis has been described as a combination of invagination and unipolar ingression through epithelial to mesenchymal transitions (EMT), possibly controlled by snail genes, important regulators of EMT in other organisms. Our examination, however, fails to reveal evidence of ingressing cells. Rather, we observe that endodermal cells constrict their apices, adopting bottle-like morphologies especially pronounced adjacent to the blastopore lip. They retain apical projections extending to the archenteron throughout gastrulation. Basally, they form actin-rich protrusions, including interdigitating filopodia that may be important in pulling the ectodermal and endodermal cells together. Endodermal cells retain cell-cell junctions while invaginating, and are organized throughout development. Never is the blastocoel filled by a mass of mesenchyme. Additionally, injection of splice-blocking morpholinos to Nematostella snail genes does not result in a phenotype despite dramatically reducing wild-type transcript, and overexpression of Snail-GFP in different clonal domains has no effect on cell behavior. These data indicate that EMT is not a major factor during gastrulation in Nematostella.

Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms

“…Nematostella has recently emerged as an important model system for cnidarian development that is amenable to the analysis of gene function (Pankow and Bamberger, 2007;Putnam et al, 2007;Rentzsch et al, 2008;Technau and Steele, 2011;Wikramanayake et al, 2003). N. vectensis gastrulates by invagination before developing into a free-swimming planula with an apical tuft at its aboral pole (Kraus and Technau, 2006;Magie et al, 2007). The planula transforms into a polyp with a tubeshaped body and only one opening, traditionally called the mouth (Hand and Uhlinger, 1992), surrounded by tentacles for prey capture and feeding (Fig.…”

Morphological evolution and embryonic developmental diversity in metazoa

“…In contrast to other types of development, these signalling and cell movement events occur in a relatively simple morphological context, consisting mostly of only two germ layers. Type B development is suggested to occur in cnidarians.The cleavage and gastrulation of cnidarians has been described as highly variable (Grassé, 1953;Grassé, 1997;Tardent, 1978;Gilbert and Raunio, 1997), even within species (Fritzenwanker et al, 2007;Magie and Martindale, 2007). The morphology of the gastrula seems to be quite variable between individuals in the .…”

Steroid metabolism in cnidarians: Insights from Nematostella vectensis

“…While it is common to characterize enzyme function in heterologous systems, such as mammalian cell lines, these approaches are prone to artifacts due to differences in conditions such as incubation temperature and the availability of cofactors and chaperone proteins. Techniques have recently been adapted to manipulate (knock down or overexpress) gene expression in N. vectensis (Magie et al, 2007;Rentzsch et al, 2008). Targeted manipulation of gene expression provides a means to characterize N. vectensis enzymes in the native environment.…”