Abstract

During amphibian gastrulation, presumptive endoderm is internalised as part of vegetal rotation, a large-scale movement that encompasses the whole vegetal half of the embryo. It has been considered a gastrulation process unique to amphibians, but we show that at the cell level, endoderm internalisation exhibits characteristics reminiscent of bottle cell formation and ingression, known mechanisms of germ layer internalisation. During ingression proper, cells leave a single-layered epithelium. In vegetal rotation, the process occurs in a multilayered cell mass; we refer to it as ingression-type cell migration. Endoderm cells move by amoeboid shape changes, but in contrast to other instances of amoeboid migration, trailing edge retraction involves ephrinB1-dependent macropinocytosis and trans-endocytosis. Moreover, although cells are separated by wide gaps, they are connected by filiform protrusions, and their migration depends on C-cadherin and the matrix protein fibronectin. Cells move in the same direction but at different velocities, to rearrange by differential migration.

Highlights

  • The basic body plan of metazoans is established by gastrulation, and at its core is the movement of endoderm and mesoderm from the surface to the interior of the embryo

  • The blastocoel floor (BCF) expands by endoderm cell rearrangement and oriented cell shape changes To analyse vegetal rotation, we first quantified tissue shape changes performed by vegetal slice explants

  • In the absence of strong cell division or cell growth during gastrulation (Saka and Smith, 2001; Kurth, 2005); four cells divided in explant shown in Figure 2B), changes in apparent cell size must be due to cell shape changes and incomplete intercalation in and out of the plane of view (Figure 2B)

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Summary

Introduction

The basic body plan of metazoans is established by gastrulation, and at its core is the movement of endoderm and mesoderm from the surface to the interior of the embryo. The pre-gastrulation embryo typically consists of a single-layered epithelium, and a common mechanism of germ layer internalisation is invagination, the inward bending of an epithelium at a pre-localised site. A classic example of gastrulation by invagination is the sea urchin embryo (Kominami and Takata, 2004), and more recently, the invagination of the mesoderm during gastrulation in the fruit fly Drosophila melanogaster has been thoroughly studied (Rauzi et al, 2013). Another major internalisation mechanism is ingression, where individual cells leave the epithelial layer to move interiorly. Primary mesenchyme ingression precedes invagination in the sea urchin embryo (Katow and Solursh, 1980; Kominami and Takata, 2004)

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