Regeneration from duplicating fragments of the Drosophila wing disc

It is a general rule that of two complementary Drosophila imaginal disc fragments, one regenerates and the other duplicates. This paper reports an investigation of an exception to this rule. Duplicating fragments from the periphery of the wing disc which lacked presumptive notum were found to regenerate notum structures during and after duplication. The propensity for this was greatest in fragments lying close to the presumptive notum, with the exception of a fragment confined to the posterior compartment, which did not regenerate notum. Structures were added sequentially, and regeneration stopped once most of the notum was present. These results are not easily explained by the polar coordinate model, which states that regeneration cannot occur from duplicating fragments. Since compartments appear to be involved in this type of regeneration as in others, it is suggested that a new type of model is required, one which permits simultaneous regeneration and duplication, and assigns a major role to compartments.

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Dpp from the anterior stripe of cells is crucial for the growth of the Drosophila wing disc

eLife ◽

10.7554/elife.22319 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 14

Author(s):

Shinya Matsuda ◽

Markus Affolter

Keyword(s):

Null Allele ◽

Growth Control ◽

Wing Disc ◽

The Other ◽

Morphogen Gradient ◽

Posterior Compartment ◽

Time Points ◽

Larval Stages ◽

Drosophila Wing ◽

Control Growth

The Dpp morphogen gradient derived from the anterior stripe of cells is thought to control growth and patterning of the Drosophila wing disc. However, the spatial-temporal requirement of dpp for growth and patterning remained largely unknown. Recently, two studies re-addressed this question. By generating a conditional null allele, one study proposed that the dpp stripe is critical for patterning but not for growth (Akiyama and Gibson, 2015). In contrast, using a membrane-anchored nanobody to trap Dpp, the other study proposed that Dpp dispersal from the stripe is required for patterning and also for medial wing disc growth, at least in the posterior compartment (Harmansa et al., 2015). Thus, growth control by the Dpp morphogen gradient remains under debate. Here, by removing dpp from the stripe at different time points, we show that the dpp stripe source is indeed required for wing disc growth, also during third instar larval stages.

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Role of knot (kn) in Wing Patterning in Drosophila

Genetics ◽

10.1093/genetics/147.3.1203 ◽

1997 ◽

Vol 147 (3) ◽

pp. 1203-1212 ◽

Cited By ~ 1

Author(s):

Katerina Nestoras ◽

Helena Lee ◽

Jym Mohler

Keyword(s):

Hedgehog Signaling ◽

Imaginal Disc ◽

Hedgehog Signaling Pathway ◽

Posterior Compartment ◽

Drosophila Wing ◽

Compartment Boundary ◽

Hh Signaling ◽

Embryonic Segmentation ◽

Anterior Posterior

We have undertaken a genetic analysis of new strong alleles of knot (kn). The original kn1 mutation causes an alteration of wing patterning similar to that associated with mutations of fused (fu), an apparent fusion of veins 3 and 4 in the wing. However, unlike fu, strong kn mutations do not affect embryonic segmentation and indicate that kn is not a component of a general Hh (Hedgehog)-signaling pathway. Instead we find that kn has a specific role in those cells of the wing imaginal disc that are subject to ptc-mediated Hh-signaling. Our results suggest a model for patterning the medial portion of the Drosophila wing, whereby the separation of veins 3 and 4 is maintained by kn activation in the intervening region in response to Hh-signaling across the adjacent anterior-posterior compartment boundary.

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Control of growth and patterning of the Drosophila wing imaginal disc by EGFR-mediated signaling

Development ◽

10.1242/dev.129.6.1369 ◽

2002 ◽

Vol 129 (6) ◽

pp. 1369-1376 ◽

Cited By ~ 2

Author(s):

Myriam Zecca ◽

Gary Struhl

Keyword(s):

Gene Expression ◽

Imaginal Disc ◽

Ectopic Expression ◽

Growth Factor Receptor ◽

Wing Disc ◽

Wing Imaginal Disc ◽

Egfr Signaling ◽

Drosophila Wing ◽

Compartment Boundary ◽

Egfr Ligand

The subdivision of the Drosophila wing imaginal disc into dorsoventral (DV) compartments and limb-body wall (wing-notum) primordia depends on Epidermal Growth Factor Receptor (EGFR) signaling, which heritably activates apterous (ap) in D compartment cells and maintains Iroquois Complex (Iro-C) gene expression in prospective notum cells. We examine the source, identity and mode of action of the EGFR ligand(s) that specify these subdivisions. Of the three known ligands for the Drosophila EGFR, only Vein (Vn), but not Spitz or Gurken, is required for wing disc development. We show that Vn activity is required specifically in the dorsoproximal region of the wing disc for ap and Iro-C gene expression. However, ectopic expression of Vn in other locations does not reorganize ap or Iro-C gene expression. Hence, Vn appears to play a permissive rather than an instructive role in organizing the DV and wing-notum segregations, implying the existance of other localized factors that control where Vn-EGFR signaling is effective. After ap is heritably activated, the level of EGFR activity declines in D compartment cells as they proliferate and move ventrally, away from the source of the instructive ligand. We present evidence that this reduction is necessary for D and V compartment cells to interact along the compartment boundary to induce signals, like Wingless (Wg), which organize the subsequent growth and differentiation of the wing primordium.

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The function of engrailed and the specification of Drosophila wing pattern

Development ◽

10.1242/dev.121.10.3447 ◽

1995 ◽

Vol 121 (10) ◽

pp. 3447-3456 ◽

Cited By ~ 41

Author(s):

I. Guillen ◽

J.L. Mullor ◽

J. Capdevila ◽

E. Sanchez-Herrero ◽

G. Morata ◽

...

Keyword(s):

Wing Disc ◽

Gene Products ◽

Wing Pattern ◽

Related Gene ◽

Posterior Compartment ◽

Anterior Compartment ◽

Drosophila Wing ◽

Partial Inactivation ◽

Autoregulatory Mechanism ◽

Adult Drosophila

The adult Drosophila wing (as the other appendages) is subdivided into anterior and posterior compartments that exhibit characteristic patterns. The engrailed (en) gene has been proposed to be paramount in the specification of the posterior compartment identity. Here, we explore the adult en function by targeting its expression in different regions of the wing disc. In the anterior compartment, ectopic en expression gives rise to the substitution of anterior structures by posterior ones, thus demonstrating its role in specification of posterior patterns. The en-expressing cells in the anterior compartment also induce high levels of the hedgehog (hh) and decapentaplegic (dpp) gene products, which results in local duplications of anterior patterns. Besides, hh is able to activate en and the engrailed-related gene invected (inv) in this compartment. In the posterior compartment we find that elevated levels of en product result in partial inactivation of the endogenous en and inv genes, indicating the existence of a negative autoregulatory mechanism. We propose that en has a dual role: a general one for patterning of the appendage, achieved through the activation of secreted proteins like hh and dpp, and a more specific one, determining posterior identity, in which the inv gene may be implicated.

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Regulated delivery controls Drosophila Hedgehog, Wingless and Decapentaplegic signaling

10.1101/2020.08.12.247759 ◽

2020 ◽

Author(s):

Ryo Hatori ◽

Thomas B. Kornberg

Keyword(s):

Signal Transduction ◽

Imaginal Disc ◽

Wing Disc ◽

Bone Morphogenic Protein ◽

Wing Imaginal Disc ◽

Target Cells ◽

Signaling Proteins ◽

Common Pool ◽

Drosophila Wing ◽

Disc Cells

AbstractMorphogen signaling proteins disperse across tissues to activate signal transduction in target cells. We investigated dispersion of Hedgehog (Hh), Wingless (Wg), and Bone morphogenic protein homolog Decapentaplegic (Dpp) in the Drosophila wing imaginal disc, and found that delivery to targets is regulated. Cells take up <5% Hh produced, and neither amounts taken up nor extent of signaling changes under conditions of Hh production from 50-200% normal amounts. Similarly, cells take up <25% Wg produced, and variation in Wg production from 50-700% normal has no effect on amounts taken up or signaling. Similar properties were observed for Dpp. Wing disc-produced Hh signals to disc-associated tracheal and myoblast as well as an approximately equal number of disc cells, but the extent of signaling in the disc is unaffected by the presence or absence of the tracheal cells and myoblasts. These findings show that target cells do not take up signaling proteins from a common pool and that both the amount and destination of delivered morphogens are regulated..SummaryThe extent of Hh, Wg, and Dpp signaling is independent of the amount of signal produced or the number of recipient cells.

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Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc

Development ◽

10.1242/dev.124.15.2973 ◽

1997 ◽

Vol 124 (15) ◽

pp. 2973-2981 ◽

Cited By ~ 21

Author(s):

R.J. Fleming ◽

Y. Gu ◽

N.A. Hukriede

Keyword(s):

Imaginal Disc ◽

Ectopic Expression ◽

Wing Disc ◽

Specific Response ◽

Wing Margin ◽

Drosophila Wing ◽

Imaginal Wing Disc ◽

Dorsoventral Boundary ◽

Drosophila Cells ◽

Notch Ligands

In the developing imaginal wing disc of Drosophila, cells at the dorsoventral boundary require localized Notch activity for specification of the wing margin. The Notch ligands Serrate and Delta are required on opposite sides of the presumptive wing margin and, even though activated forms of Notch generate responses on both sides of the dorsoventral boundary, each ligand generates a compartment-specific response. In this report we demonstrate that Serrate, which is expressed in the dorsal compartment, does not signal in the dorsal regions due to the action of the fringe gene product. Using ectopic expression, we show that regulation of Serrate by fringe occurs at the level of protein and not Serrate transcription. Furthermore, replacement of the N-terminal region of Serrate with the corresponding region of Delta abolishes the ability of fringe to regulate Serrate without altering Serrate-specific signaling.

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A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila

Development ◽

10.1242/dev.127.7.1499 ◽

2000 ◽

Vol 127 (7) ◽

pp. 1499-1508 ◽

Cited By ~ 15

Author(s):

F. Casares ◽

R.S. Mann

Keyword(s):

Signal Transduction ◽

Imaginal Disc ◽

Target Genes ◽

Notch Pathway ◽

Wing Disc ◽

Signal Transduction Pathways ◽

Body Parts ◽

Drosophila Wing ◽

Compartment Boundary ◽

Three Body

The Drosophila wing imaginal disc gives rise to three body parts along the proximo-distal (P-D) axis: the wing blade, the wing hinge and the mesonotum. Development of the wing blade initiates along part of the dorsal/ventral (D/V) compartment boundary and requires input from both the Notch and wingless (wg) signal transduction pathways. In the wing blade, wg activates the gene vestigial (vg), which is required for the wing blade to grow. wg is also required for hinge development, but wg does not activate vg in the hinge, raising the question of what target genes are activated by wg to generate hinge structures. Here we show that wg activates the gene homothorax (hth) in the hinge and that hth is necessary for hinge development. Further, we demonstrate that hth also limits where along the D/V compartment boundary wing blade development can initiate, thus helping to define the size and position of the wing blade within the disc epithelium. We also show that the gene teashirt (tsh), which is coexpressed with hth throughout most of wing disc development, collaborates with hth to repress vg and block wing blade development. Our results suggest that tsh and hth block wing blade development by repressing some of the activities of the Notch pathway at the D/V compartment boundary.

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Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis

Development ◽

10.1242/dev.121.10.3359 ◽

1995 ◽

Vol 121 (10) ◽

pp. 3359-3369 ◽

Cited By ~ 59

Author(s):

T. Tabata ◽

C. Schwartz ◽

E. Gustavson ◽

Z. Ali ◽

T.B. Kornberg

Keyword(s):

Imaginal Disc ◽

De Novo ◽

Posterior Compartment ◽

Anterior Compartment ◽

Drosophila Wing ◽

Organizational Feature ◽

Wing Discs ◽

Mutant Cells ◽

Anterior Posterior

Anterior/posterior compartment borders bisect every Drosophila imaginal disc, and the engrailed gene is essential for their function. We analyzed the role of the engrailed and invected genes in wing discs by eliminating or increasing their activity. Removing engrailed/invected from posterior wing cells created two new compartments: an anterior compartment consisting of mutant cells and a posterior compartment that grew from neighboring cells. In some cases, these compartments formed a complete new wing. Increasing engrailed activity also affected patterning. These findings demonstrate that engrailed both directs the posterior compartment pathway and creates the compartment border. These findings also establish the compartment border as the pre-eminent organizational feature of disc growth and patterning.

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Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling

Development ◽

10.1242/dev.129.6.1357 ◽

2002 ◽

Vol 129 (6) ◽

pp. 1357-1368 ◽

Cited By ~ 4

Author(s):

Myriam Zecca ◽

Gary Struhl

Keyword(s):

Imaginal Disc ◽

Growth Factor Receptor ◽

Subsequent Development ◽

Wing Disc ◽

Wing Imaginal Disc ◽

Egfr Signaling ◽

Drosophila Wing ◽

Compartment Boundary ◽

Epidermal Growth ◽

Necessary And Sufficient

Growth and patterning of the Drosophila wing imaginal disc depends on its subdivision into dorsoventral (DV) compartments and limb (wing) and body wall (notum) primordia. We present evidence that both the DV and wing-notum subdivisions are specified by activation of the Drosophila Epidermal Growth Factor Receptor (EGFR). We show that EGFR signaling is necessary and sufficient to activate apterous (ap) expression, thereby segregating the wing disc into D (ap-ON) and V (ap-OFF) compartments. Similarly, we demonstrate that EGFR signaling directs the expression of Iroquois Complex (Iro-C) genes in prospective notum cells, rendering them distinct from, and immiscible with, neighboring wing cells. However, EGFR signaling acts only early in development to heritably activate ap, whereas it is required persistently during subsequent development to maintain Iro-C gene expression. Hence, as the disc grows, the DV compartment boundary can shift ventrally, beyond the range of the instructive EGFR signal(s), in contrast to the notum-wing boundary, which continues to be defined by EGFR input.

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