Specification of pharyngeal endoderm

For more than a century, vertebrate taste buds have been singled out as the prime example of neural induction of sensory organs during development. This view has held that late in embryogenesis, sensory nerve fibers contacted the oral and pharyngeal epithelia, and induced a subset of epithelial cells to give rise to multicellular taste buds (Guth, 1957; Hosley et al., 1987; Torrey, 1940). The implications of this idea are that innervation dictates the timing of taste bud development and the position of these receptor organs. Recently, however, this scenario has been called into question. In axolotls, a species of aquatic salamander, morphological differentiation of taste buds is completely independent of developing nerves (Barlow et al., 1996), and in mouse embryos, early patterning of the tongue epithelium also occurs independently of nerve contact (Farbman and Mbiene, 1991; Hall et al., 1999; Nosrat et al., 2001). In addition, taste bud development in amphibians is independent of mesenchymal cell contact; isolated pharyngeal endoderm, destined to give rise to taste buds, will do so, even when removed from embryos shortly after gastrulation (Barlow and Northcutt, 1997). These findings imply that the ability to develop taste receptor organs is an inherent characteristic of the pharyngeal epithelium, which is acquired by the end of gastrulation, long before the receptor organs differentiate. In this new context, we proposed a series of hypothetical embryonic events that would give rise first to a specified pharyngeal endoderm field and subsequently to a distributed array of taste buds within that tissue (Barlow and Northcutt, 1998; Northcutt and Barlow, 1998). Because pharyngeal endoderm was specified by the end of gastrulation, we reasoned that signals during gastrulation might be responsible. Unlike the rest of the endodermal axis, the cells destined to give rise to the pharyngeal endoderm and taste buds are suprablastoporal and sit at the dorsal lip of the blastopore at the onset of gastrulation (Barlow and Northcutt, 1995; Pasteels, 1942; Vogt, 1929). During gastrulation, these cells involute first, shear past the inner surface of the presumptive neurectoderm and reach the anterior end of the embryo. In part, signals from the involuting endoderm and mesoderm induce the overlying ectoderm to become neural (Harland, 2000). Additionally, planar signals from the organizer are transmitted within the epithelium, which also neuralize the ectoderm (Doniach, 1992; Nieuwkoop, 1997; Ruiz i Altaba, 1992). Interestingly, a smattering of published reports has suggested that signaling during gastrulation is reciprocal (Nieuwkoop, 1997). For example, in Xenopus, gene expression is disrupted 4573 Development 128, 4573-4583 (2001) Printed in Great Britain © The Company of Biologists Limited 2001 DEV6544