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Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila.

Ray RP, Matamoro-Vidal A, Ribeiro PS, Tapon N, Houle D, Salazar-Ciudad I, Thompson BJ - Dev. Cell (2015)

Bottom Line: Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue.Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage.Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK; The Francis Crick Institute, Lincoln's Inn Fields Laboratory, 44 Lincoln's Inn Fields, London WC2A 3PX, UK. Electronic address: robert.ray@crick.ac.uk.

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Localization of Nw in the Developing Wing and the Ontogeny of the Nw Phenotype(A–E) Localization of Nw-GFP that has been expressed under control of the nub-Gal4 driver. The Nw-GFP is shown in green, actin in red, and the nuclei in blue. Throughout wing development, Nw follows the pattern of Dp localization: in the wing disc, it is found apically throughout the epithelium, but at 18 hr APF, it is localized to the wing margin and the trajectories of L3 and L5 (B), as wing contraction proceeds, Nw accumulates uniformly throughout the wing blade in a diaphanous network overlying the actin-rich apical membrane and bristles (C–E; see also Figure S4).(F–I) (F) Adult wing showing the phenotype associated with Tub-Gal4>nw-RNAi (A), which is similar to that produced by strong loss of function alleles of nw (see Figure 5C). Like the dp mutant phenotype (see Figure 3), the shape defect associated with nw mutants arises between 18–24 hr APF, concomitant with hinge contraction (G–I; cf. Figures 3C and 3D).(J) Computational simulation of the nw mutant phenotype using the epithelial vertex model.
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fig6: Localization of Nw in the Developing Wing and the Ontogeny of the Nw Phenotype(A–E) Localization of Nw-GFP that has been expressed under control of the nub-Gal4 driver. The Nw-GFP is shown in green, actin in red, and the nuclei in blue. Throughout wing development, Nw follows the pattern of Dp localization: in the wing disc, it is found apically throughout the epithelium, but at 18 hr APF, it is localized to the wing margin and the trajectories of L3 and L5 (B), as wing contraction proceeds, Nw accumulates uniformly throughout the wing blade in a diaphanous network overlying the actin-rich apical membrane and bristles (C–E; see also Figure S4).(F–I) (F) Adult wing showing the phenotype associated with Tub-Gal4>nw-RNAi (A), which is similar to that produced by strong loss of function alleles of nw (see Figure 5C). Like the dp mutant phenotype (see Figure 3), the shape defect associated with nw mutants arises between 18–24 hr APF, concomitant with hinge contraction (G–I; cf. Figures 3C and 3D).(J) Computational simulation of the nw mutant phenotype using the epithelial vertex model.

Mentions: The tapered wing phenotypes we have observed with brk-Gal4>dp-RNAi and hh-Gal4>dp-RNAi are reminiscent of the wing phenotypes produced by three other loci, narrow (nw), tapered (ta), and lanceolate (ll), that were first identified early in the last century (Meyer and Edmondson, 1949; Morgan et al., 1925). Inactivation of these genes produces a range of phenotypes that can be generalized as a narrowing and lengthening of the wing. The phenotypes associated with nw alleles are dosage sensitive. Dominant antimorphic alleles (e.g., nwD/+, nwB/+) and weak hypomorphs produce a mild tapering of the distal part of the wing (Figures 5A and 5B), while recessive alleles give rise to the dramatic narrowing of the entire wing blade after which the gene is named (Figure 5C). The same range of phenotypes can be recapitulated by RNAi knockdown using nub-Gal4 or Tub-Gal4 (Figures 5D and 6A) to drive hairpin constructs directed toward different exons of the nw transcript (see Figure S2). Alleles of ta and ll, which are hypomorphic for the loci (see below), produce the weaker phenotype characteristic of the dominant alleles of nw (Figures 5E and 5F).


Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila.

Ray RP, Matamoro-Vidal A, Ribeiro PS, Tapon N, Houle D, Salazar-Ciudad I, Thompson BJ - Dev. Cell (2015)

Localization of Nw in the Developing Wing and the Ontogeny of the Nw Phenotype(A–E) Localization of Nw-GFP that has been expressed under control of the nub-Gal4 driver. The Nw-GFP is shown in green, actin in red, and the nuclei in blue. Throughout wing development, Nw follows the pattern of Dp localization: in the wing disc, it is found apically throughout the epithelium, but at 18 hr APF, it is localized to the wing margin and the trajectories of L3 and L5 (B), as wing contraction proceeds, Nw accumulates uniformly throughout the wing blade in a diaphanous network overlying the actin-rich apical membrane and bristles (C–E; see also Figure S4).(F–I) (F) Adult wing showing the phenotype associated with Tub-Gal4>nw-RNAi (A), which is similar to that produced by strong loss of function alleles of nw (see Figure 5C). Like the dp mutant phenotype (see Figure 3), the shape defect associated with nw mutants arises between 18–24 hr APF, concomitant with hinge contraction (G–I; cf. Figures 3C and 3D).(J) Computational simulation of the nw mutant phenotype using the epithelial vertex model.
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Related In: Results  -  Collection

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fig6: Localization of Nw in the Developing Wing and the Ontogeny of the Nw Phenotype(A–E) Localization of Nw-GFP that has been expressed under control of the nub-Gal4 driver. The Nw-GFP is shown in green, actin in red, and the nuclei in blue. Throughout wing development, Nw follows the pattern of Dp localization: in the wing disc, it is found apically throughout the epithelium, but at 18 hr APF, it is localized to the wing margin and the trajectories of L3 and L5 (B), as wing contraction proceeds, Nw accumulates uniformly throughout the wing blade in a diaphanous network overlying the actin-rich apical membrane and bristles (C–E; see also Figure S4).(F–I) (F) Adult wing showing the phenotype associated with Tub-Gal4>nw-RNAi (A), which is similar to that produced by strong loss of function alleles of nw (see Figure 5C). Like the dp mutant phenotype (see Figure 3), the shape defect associated with nw mutants arises between 18–24 hr APF, concomitant with hinge contraction (G–I; cf. Figures 3C and 3D).(J) Computational simulation of the nw mutant phenotype using the epithelial vertex model.
Mentions: The tapered wing phenotypes we have observed with brk-Gal4>dp-RNAi and hh-Gal4>dp-RNAi are reminiscent of the wing phenotypes produced by three other loci, narrow (nw), tapered (ta), and lanceolate (ll), that were first identified early in the last century (Meyer and Edmondson, 1949; Morgan et al., 1925). Inactivation of these genes produces a range of phenotypes that can be generalized as a narrowing and lengthening of the wing. The phenotypes associated with nw alleles are dosage sensitive. Dominant antimorphic alleles (e.g., nwD/+, nwB/+) and weak hypomorphs produce a mild tapering of the distal part of the wing (Figures 5A and 5B), while recessive alleles give rise to the dramatic narrowing of the entire wing blade after which the gene is named (Figure 5C). The same range of phenotypes can be recapitulated by RNAi knockdown using nub-Gal4 or Tub-Gal4 (Figures 5D and 6A) to drive hairpin constructs directed toward different exons of the nw transcript (see Figure S2). Alleles of ta and ll, which are hypomorphic for the loci (see below), produce the weaker phenotype characteristic of the dominant alleles of nw (Figures 5E and 5F).

Bottom Line: Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue.Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage.Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK; The Francis Crick Institute, Lincoln's Inn Fields Laboratory, 44 Lincoln's Inn Fields, London WC2A 3PX, UK. Electronic address: robert.ray@crick.ac.uk.

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Related in: MedlinePlus