Abstract

The dorsal blastopore lip (known as the Spemann organizer) is important for making the body plan in amphibian gastrulation. The organizer is believed to involute inward and migrate animally to make physical contact with the prospective head neuroectoderm at the blastocoel roof of mid- to late-gastrula. However, we found that this physical contact was already established at the equatorial region of very early gastrula in a wide variety of amphibian species. Here we propose a unified model of amphibian gastrulation movement. In the model, the organizer is present at the blastocoel roof of blastulae, moves vegetally to locate at the region that lies from the blastocoel floor to the dorsal lip at the onset of gastrulation. The organizer located at the blastocoel floor contributes to the anterior axial mesoderm including the prechordal plate, and the organizer at the dorsal lip ends up as the posterior axial mesoderm. During the early step of gastrulation, the anterior organizer moves to establish the physical contact with the prospective neuroectoderm through the “subduction and zippering” movements. Subduction makes a trench between the anterior organizer and the prospective neuroectoderm, and the tissues face each other via the trench. Zippering movement, with forming Brachet's cleft, gradually closes the gap to establish the contact between them. The contact is completed at the equator of early gastrulae and it continues throughout the gastrulation. After the contact is established, the dorsal axis is formed posteriorly, but not anteriorly. The model also implies the possibility of constructing a common model of gastrulation among chordate species.

Highlights

  • Spemann and Mangold found that the dorsal blastopore lip of an amphibian gastrula can induce a secondary axis when transplanted into another embryo’s ventral side (Spemann & Mangold 1924)

  • As the first step toward understanding the mechanism of amphibian gastrulation, we examined when the physical contact between the organizer and the prospective head neuroectoderm is established in various amphibian species

  • We showed that the X. laevis gastrulation movement proposed previously (Koide et al 2002) is applicable to a wide variety of amphibian species

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Summary

Introduction

Spemann and Mangold found that the dorsal blastopore lip of an amphibian gastrula can induce a secondary axis when transplanted into another embryo’s ventral side (Spemann & Mangold 1924). The dorsal blastopore lip was named as “the organizer” because it induces the differentiation of cells that attach to it into well-organized axial structures (such as head, tail, and neural tissue). Neurulation of the dorsal ectoderm is regulated by the axial mesoderm, known as the organizer which includes prechordal plate and the notochord. In the amphibian gastrulation process, the axial mesoderm, which is derived from the dorsal marginal zone, invaginates, involutes into the body, and migrates toward the animal pole on the inner surface of the blastocoel roof. The inner surface of the blastocoel roof is ready for the directional migration of the leading edge along the surface of fibronectin substrate (Nakatsuji et al 1982; Boucaut et al 1984; Winklbauer & Nagel 1991; Johnson et al 1993), and the migration was observed in vivo and in vitro (Hara et al 2013; Moosmann et al 2013)

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