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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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The nw, ta, and ll Genes Control Wing Shape(A–F) Adult wings showing shape phenotypes associated with nw, ta, and ll mutants. Compared to wild-type (A), the nwD heterozygote (nwD/+) is mildly tapered distally (B), while the recessive hemizygote (nw2/Df) is narrower and longer (C), similar to what is observed with nub-Gal4>nw-RNAi (D). These phenotypes are associated with a single shape warp consisting of a stretch of the wing blade along the P-D axis (see Figure S1). The loss of function of ll (or Phm) or ta by RNAi knockdown results in a mild narrowing of the wing, similar to the phenotype produced by nwD/+ (E and F).(G) Molecular characterization of nw revealed that it encodes a CTLD protein (see also Figure S2), and secondary structure of the Nw-S protein compared to the canonical CTLD structure shows the two disulfide bridges (red dotted lines) that stabilize the characteristic fold of the motif, plus an additional Cys at the C terminus (blue dotted line), which is involved in dimerization.(H) Biochemical analysis of Nw shows that both protein isoforms are secreted into the medium when expressed in tissue culture cells (left) and that under non-reducing conditions they are predominately found as homo- or hetero-dimers (right). Dimerization, but not synthesis or secretion, depends on the final Cys shown in (G): mutation of this Cys blocks both the formation of dimers and the ability of the mutant form to coIP the wild-type monomer (right).(I) Molecular characterization of ta and ll (see Figure S3) reveals that they encode the two enzymes, Pal1 and Phm, that catalyze α-amidation, a post-translational modification that converts a C-terminal glycine residue into an α-amide. Nw-S terminates with a glycine and, given the phenotypes of ta and ll, α-amidation of this residue must be essential for Nw function in vivo.
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fig5: The nw, ta, and ll Genes Control Wing Shape(A–F) Adult wings showing shape phenotypes associated with nw, ta, and ll mutants. Compared to wild-type (A), the nwD heterozygote (nwD/+) is mildly tapered distally (B), while the recessive hemizygote (nw2/Df) is narrower and longer (C), similar to what is observed with nub-Gal4>nw-RNAi (D). These phenotypes are associated with a single shape warp consisting of a stretch of the wing blade along the P-D axis (see Figure S1). The loss of function of ll (or Phm) or ta by RNAi knockdown results in a mild narrowing of the wing, similar to the phenotype produced by nwD/+ (E and F).(G) Molecular characterization of nw revealed that it encodes a CTLD protein (see also Figure S2), and secondary structure of the Nw-S protein compared to the canonical CTLD structure shows the two disulfide bridges (red dotted lines) that stabilize the characteristic fold of the motif, plus an additional Cys at the C terminus (blue dotted line), which is involved in dimerization.(H) Biochemical analysis of Nw shows that both protein isoforms are secreted into the medium when expressed in tissue culture cells (left) and that under non-reducing conditions they are predominately found as homo- or hetero-dimers (right). Dimerization, but not synthesis or secretion, depends on the final Cys shown in (G): mutation of this Cys blocks both the formation of dimers and the ability of the mutant form to coIP the wild-type monomer (right).(I) Molecular characterization of ta and ll (see Figure S3) reveals that they encode the two enzymes, Pal1 and Phm, that catalyze α-amidation, a post-translational modification that converts a C-terminal glycine residue into an α-amide. Nw-S terminates with a glycine and, given the phenotypes of ta and ll, α-amidation of this residue must be essential for Nw function in vivo.

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)

The nw, ta, and ll Genes Control Wing Shape(A–F) Adult wings showing shape phenotypes associated with nw, ta, and ll mutants. Compared to wild-type (A), the nwD heterozygote (nwD/+) is mildly tapered distally (B), while the recessive hemizygote (nw2/Df) is narrower and longer (C), similar to what is observed with nub-Gal4>nw-RNAi (D). These phenotypes are associated with a single shape warp consisting of a stretch of the wing blade along the P-D axis (see Figure S1). The loss of function of ll (or Phm) or ta by RNAi knockdown results in a mild narrowing of the wing, similar to the phenotype produced by nwD/+ (E and F).(G) Molecular characterization of nw revealed that it encodes a CTLD protein (see also Figure S2), and secondary structure of the Nw-S protein compared to the canonical CTLD structure shows the two disulfide bridges (red dotted lines) that stabilize the characteristic fold of the motif, plus an additional Cys at the C terminus (blue dotted line), which is involved in dimerization.(H) Biochemical analysis of Nw shows that both protein isoforms are secreted into the medium when expressed in tissue culture cells (left) and that under non-reducing conditions they are predominately found as homo- or hetero-dimers (right). Dimerization, but not synthesis or secretion, depends on the final Cys shown in (G): mutation of this Cys blocks both the formation of dimers and the ability of the mutant form to coIP the wild-type monomer (right).(I) Molecular characterization of ta and ll (see Figure S3) reveals that they encode the two enzymes, Pal1 and Phm, that catalyze α-amidation, a post-translational modification that converts a C-terminal glycine residue into an α-amide. Nw-S terminates with a glycine and, given the phenotypes of ta and ll, α-amidation of this residue must be essential for Nw function in vivo.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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Show All Figures
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fig5: The nw, ta, and ll Genes Control Wing Shape(A–F) Adult wings showing shape phenotypes associated with nw, ta, and ll mutants. Compared to wild-type (A), the nwD heterozygote (nwD/+) is mildly tapered distally (B), while the recessive hemizygote (nw2/Df) is narrower and longer (C), similar to what is observed with nub-Gal4>nw-RNAi (D). These phenotypes are associated with a single shape warp consisting of a stretch of the wing blade along the P-D axis (see Figure S1). The loss of function of ll (or Phm) or ta by RNAi knockdown results in a mild narrowing of the wing, similar to the phenotype produced by nwD/+ (E and F).(G) Molecular characterization of nw revealed that it encodes a CTLD protein (see also Figure S2), and secondary structure of the Nw-S protein compared to the canonical CTLD structure shows the two disulfide bridges (red dotted lines) that stabilize the characteristic fold of the motif, plus an additional Cys at the C terminus (blue dotted line), which is involved in dimerization.(H) Biochemical analysis of Nw shows that both protein isoforms are secreted into the medium when expressed in tissue culture cells (left) and that under non-reducing conditions they are predominately found as homo- or hetero-dimers (right). Dimerization, but not synthesis or secretion, depends on the final Cys shown in (G): mutation of this Cys blocks both the formation of dimers and the ability of the mutant form to coIP the wild-type monomer (right).(I) Molecular characterization of ta and ll (see Figure S3) reveals that they encode the two enzymes, Pal1 and Phm, that catalyze α-amidation, a post-translational modification that converts a C-terminal glycine residue into an α-amide. Nw-S terminates with a glycine and, given the phenotypes of ta and ll, α-amidation of this residue must be essential for Nw function in vivo.
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.

Show MeSH
Related in: MedlinePlus