Migration of the Mesodermal Mantle
The migration of mesodermal precursor cells inside the embryo is part of a remarkably well coordinated series of global cellular migrations. A detailed summary of these movements can be seen in Figure 1. One of the most important aspects of amphibian gastrulation is the narrowing (convergence) and lengthening (extension) of the INVOLUTING MARGINAL ZONE (IMZ), which is that region of cells residing immediately above the blastopore lip. This zone contains the prospective endodermal roof of the archenteron in its superficial layer (IMZS) and the prospective mesodermal cells (including those of the notochord) in its deep region (IMZD).
Figure 1 Movements during Xenopus gastrulation. On the left is a map of the embryonic zones of the Xenopus embryo as it initiates gastrulation. This map is "exploded" in the center diagram, which shows each inner and outer zone separately. The right-hand diagrams show the end results of the migration of each of these cell sheets during gastrulation. The animal cap expands uniformly in all directions toward the vegetal pole, while the noninvoluting marginal zone cells migrate primarily along the dorsal side of the embryo. Together, they will surround the embryo to become the ectoderm. The deep involuting marginal zone cells are originally a ring of interior equatorial cells containing the precursors of the notochord and of the head, somitic, and lateral-ventral mesoderm. During involution, this ring turns inside out to form a mantle of mesoderm with the notochord precursors being positioned most dorsally. The superficial involuting marginal zone cells consist of prospective endodermal cells; this zone elongates dorsally to form the roof of the archenteron. The subblastoporal endoderm is eventually internalized by the noninvoluting marginal zone cells. These yolky cells form the floor of the archenteron. Note that the blastopore, originally on the dorsal surface, has been moved to the ventral side of the embryo. (After Keller, 1986.)
During gastrulation, the animal cap and noninvoluting marginal zone cells expand by epiboly to cover the entire embryo. The dorsal portion of the noninvoluting marginal cells expands more rapidly than the ventral portion, thus causing the blastopore lips to move toward the ventral side. Cells from these two zones will form the ectoderm of the embryo. The deep involuting marginal zone is a ring of cells that gives rise to the notochord, head mesoderm, somitic mesoderm, and lateral-ventral mesoderm. During gastrulation, this ring involutes around the blastopore lips to form the mesodermal mantle. The head and mesodermal precursors spread across the embryo as the notochord and somitic mesodermal regions converge and extend dorsally to form the dorsal axial structures. The superficial involuting marginal zone cells also undergo convergent extension to form the endodermal tissues of the archenteron roof (Figures 23, 24). The subblastoral endoderm is covered by the epibolizing noninvoluting marginal zone cells and forms the archenteron floor (Keller, 1986).
Figure 2 Rearrangement of cells during convergent extension of the mesoderm in Xenopus embryos. (A) The dorsal region of the IMZD (which forms the notochord) was taken from an embryo labeled with fluorescienated dextran particles and placed into an unlabeled embryo. (B) Tracings of individual cells followed with video recorder during the formation of the notochord in vitro. (After Keller et al., 1985; Keller, 1986.)
During the convergent extension of the deep IMZ, the cells rearrange themselves, intercalating with nearby cells to produce a thin, elongated structure from the originally broad, small band of cells (Figure 2). We have already discussed a similar phenomenon involving archenteron extension during sea urchin gastrulation. Many rows of cells have intercalated to form fewer, but longer, rows of cells. Convergent extension of the mesoderm appears to be autonomous, because the movements of the cells occur even if the cells are removed from the rest of the embryo (Keller, 1986).
Literature Cited
Keller, R. E., Danilchik, M., Gimlich, R. and Shih, J. 1985. Convergent extension by cell intercalation during gastrulation of Xenopus laevis. In G. M. Edelman (ed.), Molecular Determinants of Animal Form. Alan R. Liss, New York, pp. 111-141.
Keller, R. E. 1986. The cellular basis of amphibian gastrulation. In L. Browder (ed.), Developmental Biology: A Comprehensive Synthesis, Vol. 2. Plenum, New York, pp. 241-327.