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Open Access Research article

Actomyosin-based Self-organization of cell internalization during C. elegans gastrulation

Christian Pohl12, Michael Tiongson1, Julia L Moore13, Anthony Santella1 and Zhirong Bao1*

Author Affiliations

1 Developmental Biology Program, Sloan-Kettering Institute, 1275 York Avenue, New York, NY, 10065, USA

2 Buchmann Institute for Molecular Life Sciences, Institute of Biochemistry II, Goethe University, Max-von-Laue-Strasse 15, 60438 Frankfurt, Germany

3 Program in Computational Biology and Medicine, Cornell University, 1300 York Avenue, New York, NY, 10065, USA

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BMC Biology 2012, 10:94  doi:10.1186/1741-7007-10-94

Published: 30 November 2012

Abstract

Background

Gastrulation is a key transition in embryogenesis; it requires self-organized cellular coordination, which has to be both robust to allow efficient development and plastic to provide adaptability. Despite the conservation of gastrulation as a key event in Metazoan embryogenesis, the morphogenetic mechanisms of self-organization (how global order or coordination can arise from local interactions) are poorly understood.

Results

We report a modular structure of cell internalization in Caenorhabditis elegans gastrulation that reveals mechanisms of self-organization. Cells that internalize during gastrulation show apical contractile flows, which are correlated with centripetal extensions from surrounding cells. These extensions converge to seal over the internalizing cells in the form of rosettes. This process represents a distinct mode of monolayer remodeling, with gradual extrusion of the internalizing cells and simultaneous tissue closure without an actin purse-string. We further report that this self-organizing module can adapt to severe topological alterations, providing evidence of scalability and plasticity of actomyosin-based patterning. Finally, we show that globally, the surface cell layer undergoes coplanar division to thin out and spread over the internalizing mass, which resembles epiboly.

Conclusions

The combination of coplanar division-based spreading and recurrent local modules for piecemeal internalization constitutes a system-level solution of gradual volume rearrangement under spatial constraint. Our results suggest that the mode of C. elegans gastrulation can be unified with the general notions of monolayer remodeling and with distinct cellular mechanisms of actomyosin-based morphogenesis.

Keywords:
C. elegans; gastrulation; actomyosin; cellular rosette