Molecular analysis of dorsal-ventral polarity in Drosophila

Abstract

Embryonic cells in Drosophila come to express distinct sets of genes and follow different pathways of morphogenesis based on their locations within the developing embryo. Past genetic studies suggest that the specification of positional information along the dorsal-ventral (D/V) body axis involves the activities of a class of genetic loci that is distinct from the class of genes required for establishment of the anterior-posterior (A/P) axis. In general, mutations that disrupt one process do not appear to alter the other significantly. At least twenty genes have been identified as playing crucial roles in D/V polarity of the early embryo (see Anderson, Trends Genet. 3, 91-97, 1987). Twelve of the genes are maternally active; that is, they are expressed during oogenesis and encode products which are deposited in the unfertilized egg. Null mutations in eleven of these, the so-called dorsal group genes, cause the same “dorsalizing” phenotype, whereby all embryonic cells-those located in both dorsal and ventral regions-follow a dorsal pathway of development. It has been proposed that interactions among the products of the dorsal group genes are responsible for the specification of a morphogen gradient that ascribes unique positional identities to the different cells along the D/V axis (Anderson et al., Cell 42, 779-789 and 791-798, 1985). According to this model, the ventral-most regions of the early embryo contain the highest concentration of morphogen, with more dorsal regions containing progressively lower concentrations. In the absence of morphogen, which results when any one of the eleven dorsal group genes is eliminated, all cells follow a dorsal pathway, the developmental “ground state:’ by default. However, there is currently no direct evidence that a maternal factor or combination of factors is distributed in a concentration gradient around the D/V axis, or that different concentrations of this factor(s) define distinct positional identities. A more conservative view is that an asymmetrically distributed maternal factor(s) is responsible for initiating the expression of several zygotic genes, which in turn broadly subdivide the D/V axis into domains of diverse developmental potential. More discrete positional identities may be subsequently elaborated by regulatory interactions among zygotically active D/V genes. Among the eleven maternally active dorsal group genes, Toll has been implicated as playing a particularly important role in the differentiation of the D/V pattern (Anderson et al., op. cit.). Embryos obtained from To//mothers lack inherent D/V polarity. When To//embryos are injected with cytoplasm obtained from any portion of wild-type donor embryos, the site of injection of the mutant embryo defines the location of the ventral pole. In conMinireview