Signaling through both type I DPP receptors is required for anterior-posterior patterning of the entire Drosophila wing

Development ◽  
1997 ◽  
Vol 124 (1) ◽  
pp. 79-89 ◽  
Author(s):  
M.A. Singer ◽  
A. Penton ◽  
V. Twombly ◽  
F.M. Hoffmann ◽  
W.M. Gelbart
Keyword(s):  
Cell Fate ◽  
Type I ◽  
Posterior Compartment ◽  
Anterior Compartment ◽  
Hypomorphic Allele ◽  
Compartment Boundary ◽  
Adult Wing ◽  
Mutant Cells ◽  
Narrow Stripe ◽  
Anterior Posterior

The imaginal disk expression of the TGF-beta superfamily member DPP in a narrow stripe of cells along the anterior-posterior compartment boundary is essential for proper growth and patterning of the Drosophila appendages. We examine DPP receptor function to understand how this localized DPP expression produces its global effects upon appendage development. Clones of saxophone (sax) or thick veins (tkv) mutant cells, defective in one of the two type I receptors for DPP, show shifts in cell fate along the anterior-posterior axis. In the adult wing, clones that are homozygous for a null allele of sax or a hypomorphic allele of tkv show shifts to more anterior fates when the clone is in the anterior compartment and to more posterior fates when the clone is in the posterior compartment. The effect of these clones upon the expression pattern of the downstream gene spalt-major also correlates with these specific shifts in cell fate. The similar effects of sax null and tkv hypomorphic clones indicate that the primary difference in the function of these two receptors during wing patterning is that TKV transmits more of the DPP signal than does SAX. Our results are consistent with a model in which a gradient of DPP reaches all cells in the developing wing blade to direct anterior-posterior pattern.

scholarly journals Control of cell fate and polarity in the adult abdominal segments of Drosophila by optomotor-blind

Development ◽  
1997 ◽  
Vol 124 (19) ◽  
pp. 3715-3726 ◽  
Author(s):  
A. Kopp ◽  
I. Duncan
Keyword(s):  
Cell Fate ◽  
Anterior Part ◽  
Ectopic Expression ◽  
Mirror Image ◽  
Posterior Compartment ◽  
Anterior Portion ◽  
Posterior Portion ◽  
Anterior Compartment ◽  
Compartment Boundary ◽  
Hh Signaling

In an accompanying report (Kopp, A., Muskavitch, M. A. T. and Duncan, I. (1997) Development 124, 3703–3714), we show that Hh protein secreted by posterior compartment cells patterns the posterior portion of the anterior compartment in adult abdominal segments. Here we show that this function of hh is mediated by optomotor-blind (omb). omb- mutants mimic the effects of loss-of-function alleles of hh: structures from the posterior of the anterior compartment are lost, and often this region develops as a mirror image of the anterior portion. Structures from the anterior part of the posterior compartment are also lost. In the pupa, omb expression in abdominal histoblasts is highest at or near the compartment boundary, and decreases in a shallow gradient toward the anterior. This gradient is due to activation of omb by Hh secreted by posterior compartment cells. In contrast to imaginal discs, this Hh signaling is not mediated by dpp or wg. We describe several gain-of-function alleles that cause ectopic expression of omb in the anterior of the segment. Most of these cause the anterior region to develop with posterior characteristics without affecting polarity. However, an allele that drives high level ubiquitous expression of omb (QdFab) causes the anterior tergite to develop as a mirror-image duplication of the posterior tergite, a pattern opposite to that seen in omb- mutants. Ubiquitous expression of hh causes similar double-posterior patterning. We find that omb- alleles suppress this effect of ectopic hh expression and that posterior patterning becomes independent of hh in the QdFab mutant. These observations indicate that omb is the primary target of hh signaling in the adult abdomen. However, it is clear that other targets exist. One of these is likely Scruffy, a novel gene that we describe, which acts in parallel to omb. To explain the effects of omb alleles, we propose that both anterior and posterior compartments in the abdomen are polarized by underlying symmetric gradients of unknown origin. We suggest that omb has two functions. First, it specifies the development of appropriate structures both anterior and posterior to the compartment boundary. Second, it causes cells to reverse their interpretation of polarity specified by the underlying symmetric gradients.

engrailed and polyhomeotic interactions are required to maintain the A/P boundary of the Drosophila developing wing

Development ◽  
1998 ◽  
Vol 125 (15) ◽  
pp. 2771-2780 ◽  
Author(s):  
F. Maschat ◽  
N. Serrano ◽  
N.B. Randsholt ◽  
G. Geraud
Keyword(s):  
Cell Fate ◽  
Regulatory Protein ◽  
Polycomb Group ◽  
Posterior Compartment ◽  
Cubitus Interruptus ◽  
Anterior Compartment ◽  
Embryonic Segmentation ◽  
Wing Morphogenesis ◽  
Anterior Posterior

Engrailed is a nuclear regulatory protein with essential roles in embryonic segmentation and wing morphogenesis. One of its regulatory targets in embryos was shown to be the Polycomb group gene, polyhomeotic. We show here that transheterozygous adult flies, mutant for both engrailed and polyhomeotic, show a gap in the fourth vein. In the corresponding larval imaginal discs, a polyhomeotic-lacZ enhancer trap is not normally activated in anterior cells adjacent to the anterior-posterior boundary. This intermediary region corresponds to the domain of low engrailed expression that appears in the anterior compartment, during L3. Several arguments show that engrailed is responsible for the induction of polyhomeotic in these cells. The role of polyhomeotic in this intermediary region is apparently to maintain the repression of hedgehog in the anterior cells abutting the anterior-posterior boundary, since these cells ectopically express hedgehog when polyhomeotic is not activated. This leads to ectopic expressions first of patched, then of cubitus interruptus and decapentaplegic in the posterior compartment, except for the dorsoventral border cells that are not affected. Thus posterior cells express a new set of genes that are normally characteristic of anterior cells, suggesting a change in the cell identity. Altogether, our data indicate that engrailed and polyhomeotic interactions are required to maintain the anterior-posterior boundary and the posterior cell fate, just prior to the evagination of the wing.

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

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3359-3369 ◽  
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.

The spalt gene links the A/P compartment boundary to a linear adult structure in the Drosophila wing

Development ◽  
1997 ◽  
Vol 124 (1) ◽  
pp. 21-32 ◽  
Author(s):  
M.A. Sturtevant ◽  
B. Biehs ◽  
E. Marin ◽  
E. Bier
Keyword(s):  
Wing Disc ◽  
Posterior Compartment ◽  
Expression Domain ◽  
Anterior Edge ◽  
Compartment Boundary ◽  
Expression Of Genes ◽  
Wing Discs ◽  
Narrow Stripe ◽  
Hedgehog Signal ◽  
Anterior Posterior

During Drosophila embryogenesis, each segment is subdivided into an anterior and a posterior compartment through the action of the engrailed gene. Compartmental boundaries bisect imaginal disc primordia which give rise to adult appendages. In early larval development, a short-range Hedgehog signal originating from the posterior compartment of the imaginal wing disc activates expression of genes including decapentaplegic (dpp) in a stripe running along the anterior-posterior compartment boundary. Secreted Dpp emanating from the A/P boundary of wing discs then acts as a secondary signal to organize the wing over large distances. The transcription factor encoded by spalt major (salm) gene, which is expressed in a broad wedge centered over the dpp stripe, is one target of Dpp signaling. In this manuscript, we show that the anterior edge of the salm expression domain abuts a narrow stripe of rhomboid (rho)-expressing cells corresponding to the L2 longitudinal vein primordium. hh mis-expression along the anterior wing margin induces a surrounding domain of salm expression, the anterior edge of which abuts a displaced rho L2 stripe. salm plays a key role in defining the position of the L2 vein since loss of salm function in mosaic patches induces the formation of ectopic L2 branches, which comprise salm- cells running along clone borders where salm- cells confront salm+ cells. These data suggest that salm determines the position of the L2 vein primordium by activating rho expression in neighboring cells through a locally non-autonomous mechanism. rho then functions to initiate and maintain vein differentiation. We discuss how these data provide the final link connecting the formation of a linear adult structure to the establishment of a boundary by the maternal Bicoid morphogen gradient in the blastoderm embryo.

Role of knot (kn) in Wing Patterning in Drosophila

Genetics ◽  
1997 ◽  
Vol 147 (3) ◽  
pp. 1203-1212 ◽  
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.

Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs

Development ◽  
1999 ◽  
Vol 126 (8) ◽  
pp. 1591-1599 ◽  
Author(s):  
M.C. Gibson ◽  
G. Schubiger
Keyword(s):  
Normal Growth ◽  
Imaginal Discs ◽  
Ideal Model ◽  
Posterior Compartment ◽  
Anterior Compartment ◽  
In Vivo Culture ◽  
Pattern Regulation ◽  
Regulative Capacity ◽  
Anterior Posterior

Surgically fragmented Drosophila appendage primordia (imaginal discs) engage in wound healing and pattern regulation during short periods of in vivo culture. Prothoracic leg disc fragments possess exceptional regulative capacity, highlighted by the ability of anterior cells to convert to posterior identity and establish a novel posterior compartment. This anterior/posterior conversion violates developmental lineage restrictions essential for normal growth and patterning of the disc, and thus provides an ideal model for understanding how cells change fate during epimorphic pattern regulation. Here we present evidence that the secreted signal encoded by hedgehog directs anterior/posterior conversion by activating the posterior-specific transcription factor engrailed in regulating anterior cells. In the absence of hedgehog activity, prothoracic leg disc fragments fail to undergo anterior/posterior conversion, but can still regenerate missing anterior pattern elements. We suggest that hedgehog-independent regeneration within the anterior compartment (termed integration) is mediated by the positional cues encoded by wingless and decapentaplegic. Taken together, our results provide a novel mechanistic interpretation of imaginal disc pattern regulation and permit speculation that similar mechanisms could govern appendage regeneration in other organisms.

mtv shapes the activity gradient of the Dpp morphogen through regulation of thickveins

Development ◽  
2001 ◽  
Vol 128 (1) ◽  
pp. 67-74 ◽  
Author(s):  
Y. Funakoshi ◽  
M. Minami ◽  
T. Tabata
Keyword(s):  
Expression Pattern ◽  
Regulatory Mechanism ◽  
Major Type ◽  
Type I ◽  
Posterior Compartment ◽  
Novel Gene ◽  
Compartment Boundary

Drosophila wings are patterned by a morphogen, Decapentaplegic (Dpp), a member of the TGFbeta superfamily, which is expressed along the anterior and posterior compartment boundary. The distribution and activity of Dpp signaling is controlled in part by the level of expression of its major type I receptor, thickveins (tkv). The level of tkv is dynamically regulated by En and Hh. We have identified a novel gene, master of thickveins (mtv), which downregulates expression of tkv in response to Hh and En. mtv expression is controlled by En and Hh, and is complementary to tkv expression. In this report, we demonstrate that mtv integrates the activities of En and Hh that shape tkv expression pattern. Thus, mtv plays a key part of regulatory mechanism that makes the activity gradient of the Dpp morphogen.

groucho and hedgehog regulate engrailed expression in the anterior compartment of the Drosophila wing

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3467-3476 ◽  
Author(s):  
J.F. de Celis ◽  
M. Ruiz-Gomez
Keyword(s):  
Cell Growth ◽  
Normal Growth ◽  
Wing Disc ◽  
Anterior Compartment ◽  
Drosophila Wing ◽  
Compartment Boundary ◽  
Ectopic Activation ◽  
Selector Genes ◽  
Dorsoventral Boundary ◽  
Anterior Posterior

Drosophila imaginal discs are divided into units called compartments. Cells belonging to the same compartment are related by lineage and express a characteristic set of ‘selector genes’. The borders between compartments act as organizing centres that influence cell growth within compartments. Thus, in the cells immediately anterior to the anterior-posterior compartment boundary the presence of the hedgehog product causes expression of decapentaplegic, which, in turn, influences the growth and patterning of the wing disc. The normal growth of the disc requires that posterior-specific genes, such as hedgehog and engrailed are not expressed in cells of the anterior compartment. Here we show that hedgehog can activate engrailed in the anterior compartment and that both hedgehog and engrailed are specifically repressed in anterior cells by the activity of the neurogenic gene groucho. In groucho mutant discs, hedgehog and engrailed are expressed at the dorsoventral boundary of the anterior compartment, leading to the ectopic activation of decapentaplegic and patched and to a localised increase in cell growth associated with pattern duplications. The presence of engrailed in the anterior compartment causes the transformation of anterior into posterior structures.

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