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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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Genetic and Molecular Interactions between nw and dp(A–F) The dosage sensitivity of nw makes it ideal for testing genetic interactions with other aECM proteins. nw shows a strong interaction with dp, but not with other aECM components (data not shown). A dp  heterozygote (dpolvR/+) produces a wild-type wing (A), while the nwD (or nwB) heterozygote exhibits a mildly tapered wing (B). In the transheterozygous combination, dpolvR+/+ nwD, a spectrum of phenotypes is produced, ranging from sharply tapered to a complete retraction of the wing blade resembling the dp loss of function phenotype (C–F).(G) Distinct phenotypic classes from this spectrum of phenotypes were defined to quantitate the enhancement, shown as percent of total wings showing the phenotype.(H and I) Localization of Dp protein in wild-type (H) and nw mutant wings (I). In the wild-type, Dp protein is detectable throughout the wing margin, with higher levels at the distal tip (H). In the nw mutant wings, the expression is reduced to a small crescent of expression at the distal tip (I).
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fig7: Genetic and Molecular Interactions between nw and dp(A–F) The dosage sensitivity of nw makes it ideal for testing genetic interactions with other aECM proteins. nw shows a strong interaction with dp, but not with other aECM components (data not shown). A dp heterozygote (dpolvR/+) produces a wild-type wing (A), while the nwD (or nwB) heterozygote exhibits a mildly tapered wing (B). In the transheterozygous combination, dpolvR+/+ nwD, a spectrum of phenotypes is produced, ranging from sharply tapered to a complete retraction of the wing blade resembling the dp loss of function phenotype (C–F).(G) Distinct phenotypic classes from this spectrum of phenotypes were defined to quantitate the enhancement, shown as percent of total wings showing the phenotype.(H and I) Localization of Dp protein in wild-type (H) and nw mutant wings (I). In the wild-type, Dp protein is detectable throughout the wing margin, with higher levels at the distal tip (H). In the nw mutant wings, the expression is reduced to a small crescent of expression at the distal tip (I).

Mentions: The molecular characterization of nw, ta, and ll, and the mutant phenotype they produce, suggest that they might be involved in defining the localization of Dp in the developing wing. Consistent with this idea, the shape defect associated with nw mutants arises during hinge contraction (Figures 6A–6D), as we have observed for the dp mutations (cf. Figures 3C and 3D). In addition, the expression of a Nw-GFP fusion driven by the nub-Gal4 driver precisely follows the pattern of Dp expression throughout wing development, despite the fact that fusion protein is expressed in all cells of the wing blade. In the wing disc, Nw is localized apically, in the pupal wing at 18 hr APF, it is localized to the wing margin and subsequently it accumulates uniformly in a fibrous network over the entire epithelium (Figures 6F–6J). Moreover, Nw-GFP does not localize to the aECM in dp mutant wings, in which the aECM fails to form properly (Figure S4). Finally, nw and dp interact genetically, with transheterozygotes producing wings that are either acutely tapered or retracted toward the hinge, similar to dp mutants (Figures 7A–7G). These results suggest that nw mutants affect wing shape by influencing the pattern of anchorage of the wing epithelium to the overlying cuticle.


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)

Genetic and Molecular Interactions between nw and dp(A–F) The dosage sensitivity of nw makes it ideal for testing genetic interactions with other aECM proteins. nw shows a strong interaction with dp, but not with other aECM components (data not shown). A dp  heterozygote (dpolvR/+) produces a wild-type wing (A), while the nwD (or nwB) heterozygote exhibits a mildly tapered wing (B). In the transheterozygous combination, dpolvR+/+ nwD, a spectrum of phenotypes is produced, ranging from sharply tapered to a complete retraction of the wing blade resembling the dp loss of function phenotype (C–F).(G) Distinct phenotypic classes from this spectrum of phenotypes were defined to quantitate the enhancement, shown as percent of total wings showing the phenotype.(H and I) Localization of Dp protein in wild-type (H) and nw mutant wings (I). In the wild-type, Dp protein is detectable throughout the wing margin, with higher levels at the distal tip (H). In the nw mutant wings, the expression is reduced to a small crescent of expression at the distal tip (I).
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4539345&req=5

fig7: Genetic and Molecular Interactions between nw and dp(A–F) The dosage sensitivity of nw makes it ideal for testing genetic interactions with other aECM proteins. nw shows a strong interaction with dp, but not with other aECM components (data not shown). A dp heterozygote (dpolvR/+) produces a wild-type wing (A), while the nwD (or nwB) heterozygote exhibits a mildly tapered wing (B). In the transheterozygous combination, dpolvR+/+ nwD, a spectrum of phenotypes is produced, ranging from sharply tapered to a complete retraction of the wing blade resembling the dp loss of function phenotype (C–F).(G) Distinct phenotypic classes from this spectrum of phenotypes were defined to quantitate the enhancement, shown as percent of total wings showing the phenotype.(H and I) Localization of Dp protein in wild-type (H) and nw mutant wings (I). In the wild-type, Dp protein is detectable throughout the wing margin, with higher levels at the distal tip (H). In the nw mutant wings, the expression is reduced to a small crescent of expression at the distal tip (I).
Mentions: The molecular characterization of nw, ta, and ll, and the mutant phenotype they produce, suggest that they might be involved in defining the localization of Dp in the developing wing. Consistent with this idea, the shape defect associated with nw mutants arises during hinge contraction (Figures 6A–6D), as we have observed for the dp mutations (cf. Figures 3C and 3D). In addition, the expression of a Nw-GFP fusion driven by the nub-Gal4 driver precisely follows the pattern of Dp expression throughout wing development, despite the fact that fusion protein is expressed in all cells of the wing blade. In the wing disc, Nw is localized apically, in the pupal wing at 18 hr APF, it is localized to the wing margin and subsequently it accumulates uniformly in a fibrous network over the entire epithelium (Figures 6F–6J). Moreover, Nw-GFP does not localize to the aECM in dp mutant wings, in which the aECM fails to form properly (Figure S4). Finally, nw and dp interact genetically, with transheterozygotes producing wings that are either acutely tapered or retracted toward the hinge, similar to dp mutants (Figures 7A–7G). These results suggest that nw mutants affect wing shape by influencing the pattern of anchorage of the wing epithelium to the overlying cuticle.

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