The Role of Innervation in the Development of Taste Buds: Insights from Studies of Amphibian Embryosa

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Abstract
Amphibian embryos have long been model organisms for studies of development because of their hardiness and large size, as well as the ease with which they can be experimentally manipulated. These particular advantages have allowed us recently to test the role of innervation in the development of vertebrate taste buds using embryos of an aquatic salamander, the axolotl. The predominant model of taste bud genesis has been one of neural induction, in which ingrowing sensory neurites induce taste bud differentiation in the epithelium that lines the mouth and pharynx. However, when we prevented embryonic sensory neurons from contacting the oropharyngeal epithelium by using transplantation or tissue culture techniques, we found that taste bud differentiation was independent of nerve contact. Additionally, using similar types of experimental manipulations, we have recently shown that taste bud differentiation is not a result of interactions of the oropharyngeal epithelium with craniofacial mesenchyme. Surprisingly, we found that although taste bud genesis occurs very late in embryonic development, it is an intrinsic feature of the presumptive oropharyngeal epithelium extremely early, in fact as early as the completion of gastrulation. These data have prompted us to propose a new model for the development of amphibian taste buds: (i) The presumptive oropharyngeal epithelium is specified by the time gastrulation is complete; (ii) Subsequently, a distributed population of taste bud progenitors is set up within this epithelium via local cell-cell interactions. These progenitor cells give rise to taste buds, which are distributed throughout the mouth and pharynx. How widely applicable this model might be for the genesis of taste buds in other vertebrates remains to be seen. However, since it is likely that the taste system of axolotls more closely resembles the ancestral state from which both the amphibian and mammalian taste systems have evolved, it is possible that many of the same developmental mechanisms that give rise to amphibian taste buds are also used to generate the receptor organs in mammals.