Characterization of convergent thickening, a major convergence force producing morphogenic movement in amphibians

Author:

Shook David R12ORCID,Wen Jason WH3ORCID,Rolo Ana4,O'Hanlon Michael2,Francica Brian5,Dobbins Destiny6,Skoglund Paul1,DeSimone Douglas W2ORCID,Winklbauer Rudolf3ORCID,Keller Ray E12ORCID

Affiliation:

1. Department of Biology, University of Virginia

2. Department of Cell Biology, University of Virginia, School of Medicine

3. Department of Cell and Systems Biology, University of Toronto

4. Centre for Craniofacial and Regenerative Biology, King's College London

5. Aduro Biotech

6. Independent researcher

Abstract

The morphogenic process of convergent thickening (CT) was originally described as the mediolateral convergence and radial thickening of the explanted ventral involuting marginal zone (IMZ) of Xenopus gastrulae (Keller and Danilchik, 1988). Here, we show that CT is expressed in all sectors of the pre-involution IMZ, which transitions to expressing convergent extension (CE) after involution. CT occurs without CE and drives symmetric blastopore closure in ventralized embryos. Assays of tissue affinity and tissue surface tension measurements suggest CT is driven by increased interfacial tension between the deep IMZ and the overlying epithelium. The resulting minimization of deep IMZ surface area drives a tendency to shorten the mediolateral (circumblastoporal) aspect of the IMZ, thereby generating tensile force contributing to blastopore closure (Shook et al., 2018). These results establish CT as an independent force-generating process of evolutionary significance and provide the first clear example of an oriented, tensile force generated by an isotropic, Holtfreterian/Steinbergian tissue affinity change.

Funder

Eunice Kennedy Shriver National Institute of Child Health and Human Development

National Institute of General Medical Sciences

Canadian Institutes of Health Research

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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