Abstract

In mammals, taste buds develop in different regions of the oral cavity. Small epithelial protrusions form fungiform papillae on the ectoderm-derived dorsum of the tongue and contain one or few taste buds, while taste buds in the soft palate develop without distinct papilla structures. In contrast, the endoderm-derived circumvallate and foliate papillae located at the back of the tongue contain a large number of taste buds. These taste buds cluster in deep epithelial trenches, which are generated by intercalating a period of epithelial growth between initial placode formation and conversion of epithelial cells into sensory cells. How epithelial trench formation is genetically regulated during development is largely unknown. Here we show that Pax9 acts upstream of Pax1 and Sox9 in the expanding taste progenitor field of the mouse circumvallate papilla. While a reduced number of taste buds develop in a growth-retarded circumvallate papilla of Pax1 mutant mice, its development arrests completely in Pax9-deficient mice. In addition, the Pax9 mutant circumvallate papilla trenches lack expression of K8 and Prox1 in the taste bud progenitor cells, and gradually differentiate into an epidermal-like epithelium. We also demonstrate that taste placodes of the soft palate develop through a Pax9-dependent induction. Unexpectedly, Pax9 is dispensable for patterning, morphogenesis and maintenance of taste buds that develop in ectoderm-derived fungiform papillae. Collectively, our data reveal an endoderm-specific developmental program for the formation of taste buds and their associated papilla structures. In this pathway, Pax9 is essential to generate a pool of taste bud progenitors and to maintain their competence towards prosensory cell fate induction.

Highlights

  • Taste buds consist of a group of clustered sensory cells and have been identified in all vertebrates

  • Whole mount X-Gal staining of a developing Pax9+/LacZ [21] mouse tongue at embryonic day 13.5 (E13.5) indicated that strong Pax9 expression is associated with the localization of placodes forming the circumvallate papillae (CVP) and foliate papillae (FOP), respectively (Figure 1B)

  • The complex architecture of the CVP and FOP, and the close vicinity of numerous taste buds in these taste papillae predict the activities of developmental programs to differ from those regulating patterning and development of the fungiform papillae (FUP) on the anterior dorsal tongue

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Summary

Introduction

Taste buds consist of a group of clustered sensory cells and have been identified in all vertebrates. Despite phyletic variations and different distribution patterns of taste papillae, taste buds in the dorsal tongue epithelium develop in all vertebrates, including amphibia, reptiles, birds and mammals. Embryonic induction and development of taste buds have been widely studied in amphibia and rodents (for a recent review, see [3]). These investigations concentrated mainly on the FUPs of mice and rats, which contain taste buds with taste pores that open directly into the oral cavity. While taste buds of the FUP are formed by epithelial placodes that are established early in development, the placodes of the CVP and FOP undergo substantial morphological changes and intercalate a period of extensive epithelial growth to generate increased taste bud progenitor fields prior to the induction of taste bud cells

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