Cleavage and Gastrulation in Avian Embryos

Abstract

Avian embryos differ from those of other vertebrates in several respects – among them, they have a large mass of yolk, the cells initially divide from the centre of a disk with cleavage planes that open into the yolk, and the embryo has great ability to regulate until very late stages of development. After approximately 20 000 cells have been generated, gastrulation begins. This process generates the primitive streak which defines bilateral symmetry, and through which cells from the superficial layer (epiblast) ingress to generate two new layers of embryonic cells (mesoderm and endoderm). This period of development starts to define the three axes of the future embryo (head–tail, dorsoventral and left–right), and it is at this time that many cell fates start to be fixed.

Key concepts:

  • Avian embryos cleave meroblastically: the cleavage planes are initially open to the yolk and generate a disc with smaller cells in the middle and larger, yolky cells outside.

  • Gastrulation is the process by which the embryo generates three germ layers: ectoderm, mesoderm and endoderm. It involves massive cell movements as well as specification of cell fates through differential gene expression.

  • As cells move around the embryo, they change their patterns of gene expression according to their current position. Therefore during early development, gene expression marks cell states rather than cell fates.

  • The mechanisms of early development are largely conserved between different vertebrate classes but there are also some differences.

  • Amniote (reptiles, birds and mammals) embryos have a unique capacity to regulate, meaning that when an embryo is cut into half or smaller pieces each piece can generate a whole embryo. Embryos retain this ability right up to the start of gastrulation and this is probably one of the processes responsible for generating identical twins.

  • Neural induction subdivides the ectoderm into neural (future nervous system) and non‐neural (future skin and sensory organs in the head) territories. Neural‐inducing signals in avian embryos arise from the ‘organizer’, Hensen's node.

  • The final head–tail axis of the embryo does not correspond to the axis of the primitive streak (which correlates better with axial and lateral fates). Mesodermal cells that will occupy more cranial positions emerge earlier from the streak than those that will end up in the trunk and tail. After gastrulation, the embryo has mechanisms that convert ‘time’ information into ‘positional identity’.

Keywords: gastrulation; primitive streak; epiblast; mesoderm; endoderm; hypoblast; Hensen's node; neural induction; neurulation

Figure 1.

(a) Structure of a typical avian egg and arrangement of membranes. The egg is shown as a median section cut along the long axis of the shell. Initial stages in meroblastic cleavage, as seen in avian embryos; (b) first cleavage plane; (c) 4‐cell stage and (d) 12‐cell stage.

Figure 2.

General morphology and movements of the upper layer (epiblast) of the chick embryo at stages X (laying) to 5 (early neurulation). Marginal zone is shown in pale pink; Koller's sickle in red. Upper layer movements are indicated by blue arrows. In this figure (and Figure and Figure ) the stages of development before primitive streak formation follow Eyal‐Giladi and Kochav (1976) and are shown in Roman numerals, and those after appearance of the primitive streak follow Hamburger and Hamilton (1951) and appear as Arabic numbers.

Figure 3.

The different components (hypoblast, endoblast and endoderm) of the lower layer of the area pellucida of the chick embryo and their movements. Hypoblast is shown in orange; endoblast in green and endoderm in pale blue. From stage 3+, the hypoblast (orange) becomes confined to a crescent‐shaped region at the anterior end of the embryo which also contains the germ cells – this region is therefore known as the germinal crescent.

Figure 4.

The middle layer of the chick embryo and its movements. Koller's sickle is shown in red; marginal zone in pale pink and mesoderm in green. Mesoderm movements are indicated by blue arrows.

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Further Reading

Albazerchi A and Stern CD (2007) An early role for the hypoblast (AVE) in neural induction and patterning, independent of its ability to position the primitive streak. Developmental Biology 301: 489–503.

Arendt D and Nübler‐Jung K (1999) Rearranging gastrulation in the name of yolk: evolution of gastrulation in yolk‐rich amniote eggs. Mechanisms of Development 81: 3–22.

Bachvarova RF, Skromne I and Stern CD (1998) Induction of primitive streak and Hensen's node by posterior marginal zone in the early chick embryo. Development 125: 3521–3534.

Bertocchini F and Stern CD (2002) The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signalling. Developmental Cell 3: 735–744.

Eyal‐Giladi H and Kochav S (1976) From cleavage to primitive streak formation: a complementary normal table and a first look at the first stages of the development of the chick. I. General morphology. Developmental Biology 49: 321–327.

Foley AC, Skromne I and Stern CD (2000) Reconciling different models of forebrain induction and patterning: a dual role for the hypoblast. Development 127: 3839–3854.

Hamburger V and Hamilton HL (1951) A series of normal stages in the development of the chick embryo. Journal of Morphology 88: 49–92.

Joubin KI and Stern CD (1999) Molecular interactions continuously define the organizer during the cell movements of gastrulation. Cell 98: 559–571.

Kimura W, Yasugi S, Stern CD and Fukuda K (2006) Fate and plasticity of the endoderm in the early chick embryo. Developmental Biology 289: 283–295.

Knezevic V, De Santo R and Mackem S (1998) Continuing organizer function during chick tail development. Development 125: 1791–1801.

Sheng G, Dos Reis M and Stern CD (2003) Churchill, a zinc finger transcriptional activator, regulates the transition between gastrulation and neurulation. Cell 115: 603–613.

Skromne I and Stern CD (2001) Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128: 2915–2927.

Spratt NT and Haas H (1960) Integrative mechanisms in development of the early chick blastoderm. I. Regulative potentiality of separated parts. Journal of Experimental Zoology 145: 97–137.

Stern CD (2004) Gastrulation: From Cells to Embryo. New York: Cold Spring Harbor Laboratory Press. ISBN: 0‐87969‐707‐5.

Stern CD (2005) Neural induction: old problem, new results, yet more questions. Development 132: 2007–2021.

Stern CD, Charité J, Deschamps J et al. (2006) Head‐tail patterning of the vertebrate embryo: one, two or many unresolved problems? International Journal of Developmental Biology 50: 3–15.

Streit A, Berliner AJ, Papanayotou C, Sirulnik A and Stern CD (2000) Initiation of neural induction by FGF signalling before gastrulation. Nature 406: 74–78.

Voiculescu O, Bertocchini F, Wolpert L, Keller RE and Stern CD (2007) The amniote primitive streak is defined by epithelial cell intercalation before gastrulation. Nature 449: 1049–1052.

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How to Cite close
Stern, Claudio D(Dec 2009) Cleavage and Gastrulation in Avian Embryos. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001075.pub3]