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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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Dp Anchors the Wing Margin to the Pupal Cuticle to Define the Pattern of Global Forces that Shape the Wing(A and B) Bright field images of frontal sections of wild-type (A) and nub-Gal4>dp-RNAi (B) wings at 18 hr APF, just after the pupal apolysis. In the wild-type, the anterior and posterior margin of the wing blade (wb), but not the dorsal and ventral surfaces, are attached to the overlying pupal cuticle (pc) (A, arrows), while in the dp-RNAi, the epithelium is fully detached (B, arrows). Consequently, phalloidin staining (red) reveals that the wild-type wing remains apposed to the cuticle during the period from 18–24 hr APF (C), while the dp-RNAi wing retracts proximally (D).(C and D) The position of the cuticle is indicated in the final panel by a dashed white line.(E and F) Epithelial vertex model of pupal wing morphogenesis. The starting point of the simulation is the early pupal wing shape, with the hinge region shown in light blue and the blade in red. The wing veins are shown in dark blue. The contraction of the tissue, most strongly in the hinge region, combined with anchorage of the wing margin (green lines) are sufficient to simulate wild-type wing morphogenesis. When the anchorage of the margin is absent in the computer model, the entire wing retracts, simulating the dp mutant wing (see Movie S1).
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fig3: Dp Anchors the Wing Margin to the Pupal Cuticle to Define the Pattern of Global Forces that Shape the Wing(A and B) Bright field images of frontal sections of wild-type (A) and nub-Gal4>dp-RNAi (B) wings at 18 hr APF, just after the pupal apolysis. In the wild-type, the anterior and posterior margin of the wing blade (wb), but not the dorsal and ventral surfaces, are attached to the overlying pupal cuticle (pc) (A, arrows), while in the dp-RNAi, the epithelium is fully detached (B, arrows). Consequently, phalloidin staining (red) reveals that the wild-type wing remains apposed to the cuticle during the period from 18–24 hr APF (C), while the dp-RNAi wing retracts proximally (D).(C and D) The position of the cuticle is indicated in the final panel by a dashed white line.(E and F) Epithelial vertex model of pupal wing morphogenesis. The starting point of the simulation is the early pupal wing shape, with the hinge region shown in light blue and the blade in red. The wing veins are shown in dark blue. The contraction of the tissue, most strongly in the hinge region, combined with anchorage of the wing margin (green lines) are sufficient to simulate wild-type wing morphogenesis. When the anchorage of the margin is absent in the computer model, the entire wing retracts, simulating the dp mutant wing (see Movie S1).

Mentions: Our results suggest a mechanism whereby the localization of Dp at 18 hr APF defines the pattern of attachment to the pupal cuticle. In support of this view, we find that in wild-type, the wing margin is attached to the overlying pupal cuticle during the early phase of hinge contraction, as has been observed previously for wings cultured in vitro (Turner and Adler, 1995). By contrast, in dp mutants, the wing is not attached and appears to float freely within the pupal cuticle (Figures 3A and 3B, arrows). Furthermore, the wing shape of dp mutants diverges from wild-type only during pupal development, as reported by Waddington (1940). At 18 hr APF, the size and shape of dp mutant wings are not substantially different from wild-type (Figures 3C and 3D). However, over the course hinge contraction, the dp mutant wing blade pulls away from the cuticle, and the tissue contracts into a rounded cup-shape that prefigures the shape of the adult wing (Figures 3C and 3D, bottom; cf. Figures 1A and 1E).


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)

Dp Anchors the Wing Margin to the Pupal Cuticle to Define the Pattern of Global Forces that Shape the Wing(A and B) Bright field images of frontal sections of wild-type (A) and nub-Gal4>dp-RNAi (B) wings at 18 hr APF, just after the pupal apolysis. In the wild-type, the anterior and posterior margin of the wing blade (wb), but not the dorsal and ventral surfaces, are attached to the overlying pupal cuticle (pc) (A, arrows), while in the dp-RNAi, the epithelium is fully detached (B, arrows). Consequently, phalloidin staining (red) reveals that the wild-type wing remains apposed to the cuticle during the period from 18–24 hr APF (C), while the dp-RNAi wing retracts proximally (D).(C and D) The position of the cuticle is indicated in the final panel by a dashed white line.(E and F) Epithelial vertex model of pupal wing morphogenesis. The starting point of the simulation is the early pupal wing shape, with the hinge region shown in light blue and the blade in red. The wing veins are shown in dark blue. The contraction of the tissue, most strongly in the hinge region, combined with anchorage of the wing margin (green lines) are sufficient to simulate wild-type wing morphogenesis. When the anchorage of the margin is absent in the computer model, the entire wing retracts, simulating the dp mutant wing (see Movie S1).
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Related In: Results  -  Collection

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fig3: Dp Anchors the Wing Margin to the Pupal Cuticle to Define the Pattern of Global Forces that Shape the Wing(A and B) Bright field images of frontal sections of wild-type (A) and nub-Gal4>dp-RNAi (B) wings at 18 hr APF, just after the pupal apolysis. In the wild-type, the anterior and posterior margin of the wing blade (wb), but not the dorsal and ventral surfaces, are attached to the overlying pupal cuticle (pc) (A, arrows), while in the dp-RNAi, the epithelium is fully detached (B, arrows). Consequently, phalloidin staining (red) reveals that the wild-type wing remains apposed to the cuticle during the period from 18–24 hr APF (C), while the dp-RNAi wing retracts proximally (D).(C and D) The position of the cuticle is indicated in the final panel by a dashed white line.(E and F) Epithelial vertex model of pupal wing morphogenesis. The starting point of the simulation is the early pupal wing shape, with the hinge region shown in light blue and the blade in red. The wing veins are shown in dark blue. The contraction of the tissue, most strongly in the hinge region, combined with anchorage of the wing margin (green lines) are sufficient to simulate wild-type wing morphogenesis. When the anchorage of the margin is absent in the computer model, the entire wing retracts, simulating the dp mutant wing (see Movie S1).
Mentions: Our results suggest a mechanism whereby the localization of Dp at 18 hr APF defines the pattern of attachment to the pupal cuticle. In support of this view, we find that in wild-type, the wing margin is attached to the overlying pupal cuticle during the early phase of hinge contraction, as has been observed previously for wings cultured in vitro (Turner and Adler, 1995). By contrast, in dp mutants, the wing is not attached and appears to float freely within the pupal cuticle (Figures 3A and 3B, arrows). Furthermore, the wing shape of dp mutants diverges from wild-type only during pupal development, as reported by Waddington (1940). At 18 hr APF, the size and shape of dp mutant wings are not substantially different from wild-type (Figures 3C and 3D). However, over the course hinge contraction, the dp mutant wing blade pulls away from the cuticle, and the tissue contracts into a rounded cup-shape that prefigures the shape of the adult wing (Figures 3C and 3D, bottom; cf. Figures 1A and 1E).

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