Further Development 4.6: From Feathers to Claws and Frogs to Newts: Further Your Understanding of Induction

Cell-to-Cell Communication: Mechanisms of Morphogenesis

From Feathers to Claws and Frogs to Newts: Further Your Understanding of Induction and Competence

Some of the best-studied cases of induction involve the interactions of sheets of epithelial cells with adjacent mesenchymal cells. All organs consist of an epithelium and an associated mesenchyme, so these interactions are among the most important phenomena in nature. Some examples are listed in Table 1.

Table 1

Mesenchymal component
Cutaneous structures (hair, feathers, sweat glands, mammary glands) Epidermis (ectoderm) Dermis (mesoderm)
Limb Epidermis (ectoderm) Mesenchyme (mesoderm)
Gut organs (liver, pancreas, salivary glands) Epithelium (endoderm) Mesenchyme (mesoderm)
Foregut and respiratory-associated organs (lungs, thymus, thyroid) Epithelium (endoderm) Mesenchyme (mesoderm)
Kidney Ureteric bud (mesoderm) Mesenchyme epithelium (mesoderm)
Tooth Jaw epithelium (ectoderm) Mesenchyme (neural crest)

Regional specificity of induction

Using the induction of cutaneous (skin) structures as our examples, let’s look at the properties of epithelial-mesenchymal interactions. The first of these properties is the regional specificity of induction. Skin is composed of two main tissues: an outer epidermis (an epithelial tissue derived from ectoderm) and a dermis (a mesenchymal tissue derived from mesoderm). The chick epidermis secretes proteins that signal the underlying dermal cells to form condensations, and the condensed dermal mesenchyme responds by secreting factors that cause the epidermis to form regionally specific cutaneous structures (Nohno et al. 1995; Ting-Berreth and Chuong 1996). These structures can be the broad feathers of the wing, the narrow feathers of the thigh, or the scales and claws of the feet (Figure 1). The dermal mesenchyme is responsible for the regional specificity of induction in the competent epidermal epithelium. Researchers can separate the embryonic epithelium and mesenchyme from each other and recombine them in different ways (Saunders et al. 1957). The same epithelium develops cutaneous structures according to the region from which the mesenchyme was taken. Here, the mesenchyme plays an instructive role, calling into play different sets of genes in the responding epithelial cells.

>Figure 1 Feather induction in the chick. (A) In situ hybridization of a 10-day chick embryo shows Sonic hedgehog expression (dark spots) in the ectoderm of the developing feathers and scales. (B) When cells from different regions of the chick dermis (mesenchyme) are recombined with wing epidermis (epithelium), the type of cutaneous structure made by the epidermal epithelium is determined by the source of the mesenchyme. (A courtesy of W.-S. Kim and J. F. Fallon; B after Saunders 1980.)

Genetic specificity of induction

The second property of epithelial-mesenchymal interactions is the genetic specificity of induction. Whereas the mesenchyme may instruct the epithelium as to what sets of genes to activate, the responding epithelium can comply with these instructions only so far as its genome permits. This property was discovered through experiments involving the transplantation of tissues from one species to another.

In one of the most dramatic examples of interspecific induction, Hans Spemann and Oscar Schotté (1932) transplanted flank ectoderm from an early frog gastrula to the region of a newt gastrula destined to become parts of the mouth. Similarly, they placed presumptive flank ectodermal tissue from a newt gastrula into the presumptive oral regions of frog embryos. The structures of the mouth region differ greatly between salamander and frog larvae. The salamander larva has club-shaped balancers beneath its mouth, whereas the frog tadpole produces mucus-secreting glands and suckers. The frog tadpole also has a horny jaw without teeth, whereas the salamander has a set of calcareous teeth in its jaw. The larvae resulting from the transplants were chimeras. The salamander larvae had froglike mouths, and the frog tadpoles had salamander teeth and balancers (Figure 2). In other words, the mesenchymal cells instructed the ectoderm to make a mouth, but the ectoderm responded by making the only kind of mouth it “knew” how to make, no matter how inappropriate.1

Figure 2 Genetic specificity of induction in amphibians. Reciprocal transplantation between the presumptive oral ectoderm regions of salamander and frog gastrulae leads to newts with tadpole suckers and tadpoles with newt balancers.

Thus, the instructions sent by the mesenchymal tissue can cross species barriers. Salamanders respond to frog inducers, and chick tissue responds to mammalian inducers. The response of the epithelium, however, is species-specific. So whereas organ-type specificity (e.g., feather or claw) is usually controlled by the mesenchyme, species specificity is usually controlled by the responding epithelium. As we will see in Chapter 24, major evolutionary changes in the phenotype can be brought about by changing the response to a particular inducer.

Literature Cited

Passera, L., Roncin, E., Kaufmann, B., and Keller, L. 1996. Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379: 630-631.

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