Embryonic development of the stomatogastric nervous system in Drosophila.

Abstract

Using several cell-specific markers, the pattern of proliferation, morphogenesis, and neuronal differentiation of the Drosophila larval stomatogastric nervous system (SNS) was analyzed. In the late embryo, four SNS ganglia (frontal ganglion, hypocerebral ganglion, paraesophageal ganglion, ventricular ganglion) can be distinguished. In the early embryo, the precursor cells of the SNS (SNSPs), being an integral part of the anlage of the esophagus, undergo four synchronous rounds of division. Subsequently, SNSPs segregate from the esophageal epithelium in a complex and stereotyped pattern. The majority of SNSPs invaginate and transiently form three (rostral, intermediate, caudal) pouches that, after separating from the esophagus, become epithelial vesicles. At later stages, these SNSPs gradually lose their epithelial phenotype. Starting at the anterior-dorsal tip of each vesicle, SNSPs dissociate from one another and migrate to the various locations where they differentiate as neurons. Cells of the rostral and intermediate vesicle contribute to the frontal ganglion; the hypocerebral ganglion develops from the intermediate vesicle, the paraesophageal ganglion from the rostral vesicle, and the ventricular ganglion from the caudal vesicle. In addition to the invaginating SNSPs, several distinct groups of SNSPs delaminate as individual cells from the esophageal epithelium. Three clusters of SNSPs delaminate from a region anterior to the rostral pouch; a single SNSP delaminates from the tip of each pouch. All delaminating SNSPs contribute to the frontal ganglion. A significant number of SNSPs undergo cell death. In the late embryo, the stomatogastric ganglia are interconnected by the recurrent nerve and esophageal nerves. The frontal ganglion projects to the brain via the frontal connectives. Both recurrent nerve and frontal connectives are pioneered by small subpopulations of early differentiating stomatogastric neurons that most likely derive from among the dSNSPs and iSNSPs.