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WIREs Dev Biol

Anterior–posterior patterning in early development: three strategies

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The anterior–posterior (AP) axis is the most ancient of the embryonic axes and exists in most metazoans. Different animals use a wide variety of mechanisms to create this axis in the early embryo. In this study, we focus on three animals, including two insects (Drosophila and Tribolium) and a vertebrate (zebrafish) to examine different strategies used to form the AP axis. While Drosophila forms the entire axis within a syncytial blastoderm using transcription factors as morphogens, zebrafish uses signaling factors in a cellularized embryo, progressively forming the AP axis over the course of a day. Tribolium uses an intermediate strategy that has commonalities with both Drosophila and zebrafish. We discuss the specific molecular mechanisms used to create the AP axis and identify conserved features. WIREs Dev Biol 2012, 1:253–266. doi: 10.1002/wdev.25

Figure 1.

Germ size difference between Drosophila and Tribolium. In long germ‐band insects such as Drosophila, the embryonic germ anlagen occupies the majority of the egg (a), whereas in the short germ‐band Tribolium, the anlage is only a fraction of the egg (b). In long germ‐band insects, the entire AP body axis is specified by the end of the blastoderm stage. In short germ‐band insects, only the anterior body is specified, and the rest of the posterior body forms through a process of posterior growth in the growth zone, which will eventually form the abdomen.

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Figure 2.

Comparison of Drosophila and Tribolium AP patterning. (a) Protein gradients establish the AP axis in Drosophila. Several of the factors in AP specification, including Bcd, Hb, and Cad are transcription factors and act as morphogens. (b) The syncytial blastoderm is essential for allowing transcription factors to act as diffusible morphogens. (c) After cellularization, the entire AP axis has been specified. (d) Tribolium also utilizes protein gradients to establish the anterior body. Notable differences in Tribolium are the lack of Bcd and the unknown function of Nos, as well as the anterior specifying role of Otd. (e) A syncytial blastoderm is also essential for the morphogenetic patterning of the anterior body of Tribolium. The position where nuclei will converge to form the embryo is shown as a dashed line. (f) After cellularization, only the anterior body is specified. The posterior end consists of a growth zone that requires Wnt and Cad function for posterior body formation. (g) During the posterior growth phase, the posterior body is formed sequentially.

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Figure 3.

Fate map of the zebrafish embryo. At top is shown a fate map of the zebrafish embryo at the start of gastrulation (called the shield stage). The organizer is at the equator, on the dorsal side of the embryo. The most posterior cells of the body are at the ventral pole. The 31‐h postfertilization (hpf) embryos shown at bottom demonstrate a more lateral view at left, showing the muscle, and a midline view at right showing the spinal cord and notochord. Note that slow muscle (dark blue; only a portion is shown in the 31 hpf embryo), ends up in a more lateral position in the body than the fast muscle (the transverse section). The arrows in the embryos at bottom show the position of the transverse section. In the shield stage embryo, A and P refer to anterior and posterior, respectively, in the transverse section, A, aorta; V, Vein, P, pronephros.

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Figure 4.

Initial patterning of the zebrafish embryo. Maternal β‐catenin is stabilized on one side of the embryo. Together with Nodal signaling at the equator, the organizer (Or) is established. The organizer secretes a variety of Bmp and Wnt inhibitors that keep these signals from functioning in the region of the embryo that will form the head. Bmp and Wnts, together with Nodals, pattern the rest of the mesoderm. The region that will form the brain (Figure 3) expands over time toward the animal pole because of the movement of the inhibitors toward the animal pole during gastrulation.

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Figure 5.

Maintenance of the mesodermal progenitors. The mesodermal progenitors (red) are located at the most posterior end of the embryo, and they move anteriorly as they differentiate (blue color) and join the somites. Neural progenitors are also located in this region (green), and they differentiate (light green) to join the neural tube. Brachyury works in the mesodermal progenitors to maintain wnt transcription and to induce transcription of cyp26a1, which degrades the somite‐produced retinoic acid (RA), that would otherwise inhibit brachyury transcription. Shown is the most posterior end of a somitogenesis‐stage embryo. The bipotential neuromesodermal cells are not shown.

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Figure 6.

Models for Hox gene regulation. Left: gradient model. As the embryo extends, the concentration of a secreted factor increases which provides a signal for the expression of more posterior Hox genes. It is also possible that a signal decreases as the embryo extends. Right: chromatin model. As the embryo extends, the chromatin opens up progressively in a 3′ → 5′ direction, allowing more posterior Hox genes to be expressed.

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Blanche Capel

Blanche Capel

earned her Ph.D. at the University of Pennsylvania and has been at Duke University since 1993. She earned her endowed professorship, the James B. Duke Professor of Cell Biology, for the meaningful discoveries she has made since her postdoctoral work in genetics at the National Institute for Medical Research in London. The broad goal of the research in Dr. Capel’s laboratory is to characterize the cellular and molecular basis of morphogenesis – how the body forms. She uses gonadal (gender/sex) development in the mouse as her model system and investigates a gene she helped discover, Sry, the male sex determining gene. Gonad development is unique in that a single rudimentary tissue can be induced to form one of two different organs, an ovary or testis, and she is learning all she can about this central mystery of biology.

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