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PMID:11641216

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Citation

Ray, RP and Wharton, KA (2001) Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk. Development 128:3913-25

Abstract

The Drosophila BMP5/6/7/8 homolog, glass bottom boat (gbb), has been shown to be involved in proliferation and vein patterning in the wing disk. To better understand the roles for gbb in wing development, as well as its relationship with the Drosophila BMP2/4 homolog decapentaplegic (dpp), we have used clonal analysis to define the functional foci of gbb during wing development. Our results show that gbb has both local and long-range functions in the disk that coincide both spatially and functionally with the established functions of dpp, suggesting that both BMPs contribute to the same processes during wing development. Indeed, comparison of the mutant phenotypes of dpp and gbb hypomorphs and null clones shows that both BMPs act locally along the longitudinal and cross veins to affect the process of vein promotion during pupal development, and long-range from a single focus along the A/P compartment boundary to affect the processes of disk proliferation and vein specification during larval development. Moreover, we show that duplications of dpp are able to rescue many of the phenotypes associated with gbb mutants and clones, indicating that the functions of gbb are at least partially redundant with those of dpp. While this relationship is similar to that described for dpp and the BMP screw (scw) in the embryo, we show that the mechanisms underlying both local and long-range functions of gbb and dpp in the wing are different. For the local foci, gbb function is confined to the regions of the veins that require the highest levels of dpp signaling, suggesting that gbb acts to augment dpp signaling in the same way as scw is proposed to do in the embryo. However, unlike scw-dependent signals in the embryo, these gbb signals are not transduced by the Type I receptor saxophone (sax), thus, the cooperativity between gbb and dpp is not achieved by signaling through distinct receptor complexes. For the long-range focus along the A/P compartment boundary, gbb function does not appear to affect the high point of the dpp gradient, but, rather, appears to be required for low points, which is the reciprocal of the relationship between dpp and scw in the embryo. Moreover, these functions of gbb also do not require the Type I receptor sax. Given these results, we conclude that the relationships between gbb and dpp in the wing disk represent novel paradigms for how multiple BMP ligands signal during development, and that signaling by multiple BMPs involves a variety of different inter-ligand relationships that depend on the developmental context in which they act.

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PubMed

Keywords

Animals; Drosophila/genetics; Drosophila/growth & development; Drosophila/physiology; Drosophila Proteins/genetics; Drosophila Proteins/physiology; Gene Duplication; Gene Expression Regulation, Developmental; Genes, Insect; Mutation; Phenotype; Receptors, Transforming Growth Factor beta/genetics; Receptors, Transforming Growth Factor beta/physiology; Transforming Growth Factor beta/genetics; Transforming Growth Factor beta/physiology; Wing/growth & development

Significance

Annotations

Gene product Qualifier GO ID GO term name Evidence Code with/from Aspect Notes Status


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