Ventral Cuticle Pattern Formation in Drosophila Embryos (Abstract)

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Wild type Drosophila embryos secrete a segmentally repeating pattern of cuticular structures. The ventral surface of each abdominal segment is covered with a belt of denticles, consisting of 6 rows of uniquely oriented, morphologically distinct denticles in the anterior of each segment, and an expanse of naked cuticle covering the posterior of each segment. The intrasegmental patterning in the Drosophila embryo is regulated by cell-cell communication. Segment polarity genes in Wingless (Wg) and Hedgehog (Hh) signaling pathways are functionally required for this patterning process. One hypothesis postulates that the mutual interdependence and maintenance of Wg and Hh expression along the parasegmental boundary can be a center for secreted factors, for example Wg. The distribution of Wg can influence cell identities in all rows of epidermal cells in the 10-12-cell-wide segment. In the absence of Wg signaling, both aspects of wild-type pattern become defective: Wg mutants show reduced denticle diversity and no naked cuticle specification. It is suggested that Wg signaling promotes the diversity of denticle types present in the anterior denticle belt and the smooth or naked cuticle constituting the posterior surface of the segment. At the presence of high concentration of Wg, or in gain-of-function condition, naked cuticles are formed. This naked cuticle cell fate is specified by a cellular pathway distinct from the denticle diversity-generating pathway. Though the naked cuticle formation is proposed to be the outcome of one of the Wg functions, the determination of denticle formation is lack of description. We first report here a novel Drosophila gene, tumbler (tum), whose gene activity is required for denticle formation. Based on the interactions among Wg/Hh signaling genes and tum, we propose that the cell fate determination in Drosophila embryonic ventral epidermis is the outcome of competition between Wg/Hh signaling activity for naked cuticle formation and Tum gene activity for denticle formation. We will also describe a new Hh signaling gene, taroid (tr). Patched (Ptc) and Smoothened (Smo) form a bipartite receptor complex of Hh signal. The Hh molecule binding to Ptc can relieve the inhibition of Smo activity by Ptc. Genetically, the flow of signaling is from hh to ptc to smo. While tr is downstream of hh, it is genetically acting upstream of or parallel to ptc. Unexpectedly, tr can enhance the loss-of-function phenotype of smo, but is genetically downstream of smo. Among possibilities, it is very likely that Tr, PTc and Smo are acting in a parallel manner. In addition, the removal of tr gene function from imaginal discs does not affect the expression of Hh target gene. With other evidences, we speculate that Tr may be a novel Hh receptor, which directs a novel signaling pathway independent of Smo activity in embryos.