Cleavage and Gastrulation in Xenopus laevis Embryos

Abstract

The Xenopus laevis egg contains an asymmetric distribution of ribonucleic acids (RNAs), which are parceled out to different cells during cleavage. These RNAs initiate the formation of the germ layers, ectoderm, mesoderm and endoderm, as well as a set of dorsal axial structures, including the central nervous system. Cleavage is initially rapid and synchronous, but becomes slower and asynchronous at the midblastula transition, when the embryo's genes become active. The different cells signal among each other in a process known as induction, leading to more types of cells. The cells undergo rearrangements in a complicated set of coordinated movements during gastrulation. Signalling continues through gastrulation with a major centre, the Spemann organiser, responsible for generating the dorsal axial structures. These inductions and movements lead to the proper positioning of the forming tissues and organs, and the body plan of the embryo emerges.

Key Concepts:

  • The job of the fertilised egg is to generate the body plan.

  • The body plan of a vertebrate embryo consists of three tubes, known as germ layers, and a set of dorsal axial structures.

  • In Xenopus, RNAs localised in the egg initiate formation of both the germ layers and the dorsal axial structures.

  • The Xenopus egg rapidly divides into smaller cells to prepare for cell movements and organ formation.

  • A key signalling centre is established known as the Spemann organiser.

  • Signals from the Spemann organiser cause the formation of the dorsal axial structures including the central nervous system.

  • The complicated cell movements of gastrulation can be followed using fate maps.

  • Several types of cell movements are coordinated during gastrulation to bring about their final arrangement in the embryo.

  • The body plan emerges with the completion of gastrulation.

Keywords: cortical rotation; midblastula transition (MBT); mesoderm induction; fate map; Wnt/β‐catenin pathway; Spemann organiser; dorsal lip; blastopore; convergent extension

Figure 1.

Early patterning. (a) The oocyte in the ovary has an animal–vegetal polarity, with an animal pole (AP) and a vegetal pole (VP). There is yolk‐poor cytoplasm in the animal half and yolk‐rich cytoplasm in the vegetal half. The large oocyte nucleus, called the germinal vesicle (GV) is located in the animal half, and molecules, important for patterning the embryo, are localised in the vegetal cortex, near the surface of the vegetal half. The molecules include VegT RNA (purple v's) and dorsal determinants (green d's). (b) With oocyte maturation, the oocyte becomes ready for fertilisation. VegT RNA is released from the vegetal cortex and is translated into VegT protein (red v's). The egg reaches metaphase II of meiosis, and the small metaphase spindle is located at the animal pole (AP). The sperm enters the animal half. (c) Following fertilisation, the cortex rotates relative to the cytoplasm, shifting the dorsal determinants to one side. That side becomes the dorsal side (D), and the opposite side, where the sperm entered, becomes the ventral side (V). (d) The regions of the egg after cortical rotation have different fates in the embryo. The dorsal determinants are indicated by green dots, and there are three prospective germ layers: ectoderm, mesoderm and endoderm.

Figure 2.

Cleavage. (a) Four cells result from two vertical divisions. (b) A horizontal division produces eight cells. (c) The 32‐cell embryo has four tiers of eight cells. Experiments show that the eight cells along the dorsal side have dorsal information (green dots), with the highest concentration in the third tier. (d) Continued divisions produce the blastula. (e) The blastula has an internal cavity, the blastocoel, and the future mesoderm forms an internal ring. The future anterior (a) and posterior (p) polarity of the prospective notochord (red) is initially opposite to the future anterior and posterior polarity of the prospective central nervous system (CNS) (green). An, animal; Vg, vegetal; D, dorsal; V, ventral.

Figure 3.

Fate maps and gastrulation. (a) At the beginning of gastrulation, the dorsal lip (dl) appears on the dorsal side, below the equator, and the areas of different fate can be marked on the surface relative to the dorsal lip. The region animal to the dorsal lip is the Spemann organiser (SO). Future lens of eye (white circle). Future mouth ectoderm (white triangle). Endodermal contribution to the mouth (M). (b) This picture shows the arrangement of fated tissues when the embryo in (a) is cut in the plane of the page. The prospective mouth ectoderm is at the top in both pictures. The invagination at the dorsal lip is due to a change in shape of some surface cells, and these cells are called bottle cells. ‘a’=anterior and ‘p’=posterior. (c) As the endoderm (yellow and tan) rolls inwards, the prospective epidermis (blue) and central nervous system (green) expand to cover the outside of the embryo. (d) In a section of the embryo in (c), cells migrate along the wall of the blastocoel (Bl), reducing its size. A new cavity, the archenteron (Ar) arises, with bottle cells at the leading tip. (e) At the end of gastrulation, all of the endoderm is internal, and the blastopore (B) closes at the posterior end. The anus will form near the closed blastopore. (f) In a section of the embryo in (e), the blastocoel (Bl) is almost obliterated, and the archenteron is greatly expanded. The anterior of the archenteron in particular expands due to a change in shape of the bottle cells. A mouth will form by perforating the epidermis and the endoderm, thus connecting the archenteron to the outside. The embryo in (e) and (f) elongates in an anterior–posterior direction as indicated by the large arrow. (g) After gastrulation, the tissues (green) developing into the brain and spinal cord form a tube and move internally. This leaves only epidermis (blue) on the surface. Compare (a), (c), (e) and (g). (h) A longitudinal section of the larva shows the major tissues. Compare this picture with (b), (d) and (f). (i) A cross‐section shows the three tubes and the dorsal axial structures. Archenteron (A).

Figure 4.

Gastrulation movements. (a) Gastrulation consists of complicated movements, indicated by the arrows. They include epiboly, vegetal rotation (VR), migration (Migr) and convergent extension (CE). CE will be followed in the succeeding drawings. (b) The fate map of the internal mesoderm ring has a dorsal (D)–ventral (V) polarity coinciding with the ectoderm and an anterior–posterior polarity opposite to the ectoderm. The notochord (No). (red) is the focus in (c)–(e). (c) This view of the mesodermal ring is rotated 90° counter‐clockwise relative to that in (b), so that the notochord (red) is centred. The prospective anterior (A) is at the bottom, with the prospective posterior (P) at the top. There are two fields of prospective heart near the anterior edge. The arrows indicate the turning in and through the middle of the mesodermal ring. (d) After the notochord and mesoderm have turned in, lateral cells converge towards the midline (arrows), causing the prospective notochord to extend in an AP direction (double headed arrow). (e) As a result of CE, the notochord is elongated greatly towards the anterior end. The two heart fields will move together at the ventral midline and fuse.

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References

Ancel P and Vintemberger P (1948) Recherches sur le déterminisme de la symétrie bilatérale dans l'oeuf des amphibiens. Bulletin Biólogique de France et de Belgique  (suppl. 31): 1–182.

Blythe SA, Cha SW, Tadjuidje E, Heasman J and Klein PS (2010) β‐Catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. Developmental Cell 19: 220–231.

Cha SW, Tadjuidje E, Tao Q, Wylie C and Heasman J (2008) Wnt5a and Wnt11 interact in a maternal Dkk‐1 regulated fashion to activate both canonical and non‐canonical signaling in Xenopus axis formation. Development 135: 3719–3729.

Elinson RP and Kao KR (1989) The location of dorsal information in frog early development. Development Growth and Differentiation 31: 423–430.

Elinson RP and Rowning B (1988) A transient array of parallel microtubules in frog eggs: potential tracks for a cytoplasmic rotation that specifies the dorso‐ventral axis. Developmental Biology 128: 185–197.

Gotoh T, Kishimoto T and Sible JC (2011) Phosphorylation of claspin is triggered by the nucleocytoplasmic ratio at the Xenopus laevis midblastula transition. Developmental Biology 353: 302–308.

Heasman J, Crawford A, Goldstone K et al. (1994) Overexpression of cadherins and underexpression of β‐catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79: 791–803.

Keller RE (1975) Vital dye mapping of the gastrula and neurula of Xenopus laevis. I. Prospective areas and morphogenetic movements of the superficial layer. Developmental Biology 42: 222–241.

Keller RE (1976) Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep layer. Developmental Biology 51: 118–137.

Keller RE (1981) An experimental analysis of the role of bottle cells and the deep marginal zone in gastrulation of Xenopus laevis. Journal of Experimental Zoology 216: 81–101.

Keller RE, Danilchik M, Gimlich R and Shih J (1985) The function and mechanism of convergent extension during gastrulation of Xenopus laevis. Journal of Embryology and Experimental Morphology 89(suppl.): 185–209.

Keller RE, Shook D and Skoglund P (2008) The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Physical Biology 5: 1–23.

Kofron M, Demel T, Xanthos J et al. (1999) Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFβ growth factors. Development 126: 5759–5770.

Lemaire P, Garrett N and Gurdon JB (1995) Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal‐vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81: 85–94.

Moody SA (1987) Fates of the blastomeres of the 32‐cell‐stage Xenopus embryo. Developmental Biology 122: 300–319.

Newport J and Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30: 675–686.

Render J and Elinson RP (1986) Axis determination in polyspermic Xenopus laevis eggs. Developmental Biology 115: 425–433.

Scharf SR and Gerhart JC (1980) Determination of the dorso‐ventral axis in eggs of Xenopus laevis: complete rescue of UV‐impaired eggs by oblique orientation before first cleavage. Developmental Biology 79: 181–198.

Schneider S, Steinbeisser H, Warga RM and Hausen P (1996) β‐Catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mechanisms of Development 57: 191–198.

Signoret J and Lefresne J (1971) Contribution a l'etude de la segmentation de l'oeuf d'axolotl. I. Definition de la transition blastuleenne. Annales d’ Embryologie et de Morphogenese 2: 451–459.

Slack JMW, Darlington BG, Heath JK and Godsave SF (1987) Mesoderm induction in early Xenopus embryos by heparin‐binding growth factors. Nature 326: 197–200.

Spemann H and Mangold H (1924) Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren (Translated by V Hamburger and published 2001). International Journal of Developmental Biology 45: 13–38.

Sudarwati S and Nieuwkoop PD (1971) Mesoderm formation in the anuran Xenopus laevis (Daudin). Wilhelm Roux’ Archives 166: 189–204.

Tao Q, Yokota C, Puck H et al. (2005) Maternal Wnt11 activates the canonical Wnt signaling pathway required for axis formation in Xenopus embryos. Cell 120: 857–871.

Vincent JP, Oster GF and Gerhart JC (1986) Kinematics of gray crescent formation in Xenopus eggs. Developmental Biology 113: 484–500.

Winklbauer R and Schurfeld M (1999) Vegetal rotation, a new gastrulation movement involved in the internalization of the mesoderm and endoderm in Xenopus. Development 126: 3703–3713.

Zhang J and King ML (1996) Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T‐box transcription factor involved in mesodermal patterning. Development 122: 4119–4129.

Zhang J, Houston DW, King ML et al. (1998) The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94: 515–524.

Further Reading

Davidson LA (2008) Integrating morphogenesis with underlying mechanics and cell biology. Current Topics in Developmental Biology 81: 113–133.

http://www.xenbase.org

King ML, Messitt TJ and Mowry KL (2005) Putting RNAs in the right place at the right time: RNA localization in the frog oocytes. Biology of the Cell 97: 19–33.

White JA and Heasman J (2008) Maternal control of pattern formation in Xenopus laevis. Journal of Experimental Zoology (Molecular and Developmental Evolution) 310B: 73–84.

Winklbauer R (2009) Cell adhesion in amphibian gastrulation. International Review of Cell and Molecular Biology 278: 215–275.

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How to Cite close
Elinson, Richard P(Dec 2011) Cleavage and Gastrulation in Xenopus laevis Embryos. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001074.pub3]