TOPICS

Animation of Xenopus Gastrulation

Author

John Gerhart

Additional Author(s): Mengsha Gong, Raymond E. Keller, Richard M. Harland

Morphogenic Movements: Gastrulation
Embryonic Patterning: Axis Formation
Morphogenesis: Cell Movements; Cell/Tissue Polarity
Endoderm-derived: Digestive (Gut) Tract
Mesoderm-derived: Notochord; Somites
Ectoderm-derived: Nervous System; Epidermis
Organism: Xenopus
Stage of Development: Embryo

Object Description

This animation consists of 72 frames of drawings of median sections of the Xenopus laevis embryo (stacked and aligned images of the drawings constitute the movie), covering the period of gastrulation from stage 9 to stage 14, approximately 9 to 17 hours post fertilization of the egg, at room temperature (Nieuwkoop and Faber, 1967). Colors: prospective epidermis (light blue); prospective nervous system (dark blue); mesoderm (red); endoderm/yolk mass (yellow); mesendoderm (pink); bottle cells (green); anterior endomesoderm (AEM; brown).

The drawings were made by Mengsha Gong in 2014 based on figures from the literature, particularly the work of Ray Keller and his colleagues (see references), with additional discussion with Ray Keller, John Gerhart, and Richard Harland.

Movements of Gastrulation

The first frame, stage 9, has 12 equally distributed numbers around the circumference to indicate positions on the surface, with 12 as the animal pole and 6 as the vegetal pole, and with 3 and 9 defining the boundary where cells no longer internalize (see stage 14). Dorsal is on the right, ventral on the left.

The final frame, stage 14, has the same numbers in their positions after gastrulation, indicating the displacement of surface cells. The animal pole (12) and nearby ectoderm (1) remain at the top of the figures to show the magnitude of displacement of the other positions. Note how positions 3 and 9, initially on opposite sides, have moved together as the blastopore closes. Vegetal cells (4,5,6,7,8) now line the archenteron at the end of gastrulation. Positions 3 and 4 are greatly separated by the convergent extension movements of the notochord mesoderm and the crawling migration of the head mesoderm. By stage 14, the living embryo will turn over as the blastocoel deflates (fluid percolating into the archenteron) and the vegetal yolk mass is displaced toward the animal pole.

See annotated still frames of stages 9-14 showing morphogenetic movements occurring in different regions, such as epiboly (Keller, 1975; Szabo et al., 2017), vegetal rotation (Winklbauer and Schürfeld, 1999; Wen and Winklbauer, 2017), bottle cell formation and spreading (Hardin and Keller, 1988; Lee 2012), convergent extension (Keller and Danilchik, 1988; Shindo, 2017)), and mesendoderm migration on the blastocoel wall (Winklbauer, 1990;2009). Note the final positions of the mouth, anus, and the embryonic dorsal and ventral midlines.

The movements leading to somite and lateral plate/coelom formation are poorly visible in this animation of the embryonic median plane; they occur mostly in planes more toward the viewer and away from the viewer.

References

Danilchik M. A morph of Xenopus gastrulation from Michael Danilchik (dorsal on right) Based on sagittal sections of several fixed gastrula stages. http://www.xenbase.org/anatomy/static/movies.jsp

Hardin J, Keller R. The behaviour and function of bottle cells during gastrulation of Xenopus laevis. Development. 1988;103(1):211-30. PMID: 3197630.

Keller RE. The cellular basis of epiboly: an SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis. J Embryol Exp Morphol. 1980;60:201-34. PMID: 7310269.

Keller R, Danilchik M. Regional expression, pattern and timing of convergence and extension during gastrulation of Xenopus laevis. Development. 1988;103(1):193-209. PMID: 3197629.

R. Keller, D. Shook. (2004) Gastrulation in amphibians. In C.D. Stern (Ed.), Gastrulation: From Cells to Embryos, Cold Spring Harbor Press, New York (2004), pp. 171-204 http://www.gastrulation.org

Lee JY. Uncorking gastrulation: the morphogenetic movement of bottle cells. Wiley Interdiscip Rev Dev Biol. 2012;1(2):286-93. doi: 10.1002/wdev.19. PMID: 23801442; PMCID: PMC4708884.

Nieuwkoop PD, Faber J. Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland Publishing Company, reprinted 1994 Garland Publishing, New York; 1967. http://www.xenbase.org/anatomy/alldev.do

Papan C, Boulat B, Velan SS, Fraser SE, Jacobs RE. Formation of the dorsal marginal zone in Xenopus laevis analyzed by time-lapse microscopic magnetic resonance imaging. Dev Biol. 2007;305(1):161-71. doi: 10.1016/j.ydbio.2007.02.005. PMID: 17368611.

Papan C, Boulat B, Velan SS, Fraser SE, Jacobs RE. Two-dimensional and three-dimensional time-lapse microscopic magnetic resonance imaging of Xenopus gastrulation movements using intrinsic tissue-specific contrast. Dev Dyn. 2007;236(2):494-501. doi: 10.1002/dvdy.21045. PMID: 17191224. DOI:
10.1002/dvdy.21045

Moosmann J, Ershov A, Altapova V, Baumbach T, Prasad MS, LaBonne C, Xiao X, Kashef J, Hofmann R. X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation. Nature. 2013;497(7449):374-7. doi: 10.1038/nature12116. PMID: 23676755; PMCID: PMC4220246.

Shindo A. Models of convergent extension during morphogenesis. Wiley Interdiscip Rev Dev Biol. 2017. doi: 10.1002/wdev.293. PMID: 28906063.

Schechtman AM. Unipolar ingression in Triturus torosus: A hitherto undescribed movement in the pregastrula states of a urodele. Univ Calif Publ Zool. 1934;39:303.

Winklbauer R. Mesodermal cell migration during Xenopus gastrulation. Dev Biol. 1990;142(1):155-68. PMID: 2227092.

Winklbauer R. Cell adhesion in amphibian gastrulation. Int Rev Cell Mol Biol. 2009;278:215-75. doi: 10.1016/S1937-6448(09)78005-0. PMID: 19815180.

Winklbauer R, Schurfeld M. Vegetal rotation, a new gastrulation movement involved in the internalization of the mesoderm and endoderm in Xenopus. Development. 1999;126(16):3703-13. PMID: 10409515.

Winklbauer R, Damm EW. Internalizing the vegetal cell mass before and during amphibian gastrulation: vegetal rotation and related movements. Focus Article. WIREs Developmental Biology Published Online: Dec 27 2011 DOI: 10.1002/WDEV.26

Szabo A, Cobo I, Omara S, McLachlan S, Keller R, Mayor R. The Molecular Basis of Radial Intercalation during Tissue Spreading in Early Development. Dev Cell. 2016;37(3):213-25. doi: 10.1016/j.devcel.2016.04.008. PMID: 27165554; PMCID: PMC4865533.

Wen JW, Winklbauer R. Ingression-type cell migration drives vegetal endoderm internalisation in the Xenopus gastrula. Elife. 2017;6. doi: 10.7554/eLife.27190. PMID: 28826499; PMCID: PMC5589415.