Comparative analysis of leg and antenna development in wild-type and homeotic Drosophila melanogaster.
ABSTRACT The insect leg and antenna are thought to be homologous structures, evolved from a common ancestral appendage. The homeotic transformations of antenna to leg in Drosophila produced by mutation of the Hox gene Antennapedia are position-specific, such that every particular antenna structure is transformed into a specific leg counterpart. This has been taken to suggest that the developmental programmes of these two appendages are still similar. In particular, the mechanisms for the specification of a cell's position within the appendage would be identical, only their interpretation would be different and subject to homeotic gene control. Here we explore the degree of conservation between the developmental programmes of leg and antenna in Drosophila and other dipterans, in wild-type and homeotic conditions. Most of the appendage pattern-forming genes are active in both appendages, and their expression domains are partially conserved. However, the regulatory relationships and interactions between these genes are different, and in fact cells change their expression while undergoing homeotic transformation. Thus, the positional information, and the mechanisms which generate it, are not strictly conserved between leg and antenna; and homeotic genes alter the establishment of positional clues, not only their interpretation. The partial conservation of pattern-forming genes in both appendages ensures a predictable re-specification of positional clues, producing the observed positional specificity of homeotic transformations.
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ABSTRACT: Proximal-distal leg development in Drosophila involves a battery of genes expressed and required in specific proximal-distal (PD) domains of the appendage. Here we report the characterisation of a new gene of this type, dlim1, a member of the Lhx family of genes whose proteins contain two Lim domains and a homeodomain. We show that the Lhx gene apterous (ap) is also required for PD leg development, and we study the functional interactions between ap, dlim1 and other PD genes during leg development. Our results show that a regulatory network formed by ap and dlim1 plus the homeobox genes aristaless and Bar specifies distal leg cell fates in Drosophila.Development 01/2001; 127(24):5391-402. · 6.21 Impact Factor
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ABSTRACT: The appendage primordia of Drosophila are subdivided into compartments by the localized expression of transcription factors. Interaction between cells in adjacent compartments establishes organizing centres responsible for generating spatial pattern and promoting cell proliferation in the developing appendages. Localized expression of hedgehog (hh) in the posterior compartment of the leg imaginal disc directs expression of wingless (wg) in ventral-anterior cells and decapentaplegic (dpp) in dorsal-anterior cells near the anterior-posterior compartment boundary; wg then acts to specify ventral cell fate and to organize the dorsal-ventral axis of the leg. Interaction between wg-expressing ventral cells and dorsal cells near the anterior-posterior compartment boundary promotes axis formation in the leg. Here we show that the combined action of wg-expressing cells in the ventral-anterior compartment and dpp-expressing cells in the dorsal-anterior compartment activates expression of Distal-less, a gene required for proximal-distal axis formation in the limbs. These results demonstrate that sequential interaction between anterior-posterior and dorsal-ventral compartments establishes the proximal-distal axis of the limbs.Nature 12/1994; 372(6502):175-9. · 38.60 Impact Factor
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ABSTRACT: The spatial organization of the Drosophila embryo depends on the activity of three axial pattern-forming systems. In addition to the anterior-posterior and dorsal-ventral systems that organize the segmented body plan, a proximal-distal pattern-forming system is required to provide positional information for the developing limbs. The development of both the larval and adult limbs depends directly on the activity of the Distal-less gene. Genetic analysis has shown that Distal-less functions as a developmental switch that is required to promote the development of limb structures above the evolutionary ground-state of body wall. Here we provide genetic evidence that indicates a graded requirement for Distal-less activity during limb development. Reduction of this activity has a global effect on pattern formation in the limb. The molecular structure of the Distal-less locus indicates that the gene encodes a homoeodomain-containing protein which is therefore likely to specify limb development through differential regulation of subordinate genes.Nature 04/1989; 338(6214):432-4. · 38.60 Impact Factor