Role of the morphogenetic furrow in establishing polarity in the Drosophila eye

Development ◽  
1995 ◽  
Vol 121 (12) ◽  
pp. 4085-4094 ◽  
Author(s):  
F. Chanut ◽  
U. Heberlein
Keyword(s):  
Ectopic Expression ◽  
Morphogenetic Furrow ◽  
Eye Disc ◽  
Drosophila Eye ◽  
Retinal Epithelium ◽  
Anteroposterior Polarity ◽  
Crystalline Array

The Drosophila retina is a crystalline array of 800 ommatidia whose organization and assembly suggest polarization of the retinal epithelium along anteroposterior and dorsoventral axes. The retina develops by a stepwise process following the posterior-to-anterior progression of the morphogenetic furrow across the eye disc. Ectopic expression of hedgehog or local removal of patched function generates ectopic furrows that can progress in any direction across the disc leaving in their wake differentiating fields of ectopic ommatidia. We have studied the effect of these ectopic furrows on the polarity of ommatidial assembly and rotation. We find that the anteroposterior asymmetry of ommatidial assembly parallels the progression of ectopic furrows, regardless of their direction. In addition, ommatidia developing behind ectopic furrows rotate coordinately, forming equators in various regions of the disc. Interestingly, the expression of a marker normally restricted to the equator is induced in ectopic ommatidial fields. Ectopic equators are stable as they persist to adulthood, where they can coexist with the normal equator. Our results suggest that ectopic furrows can impart polarity to the disc epithelium, regarding the direction of both assembly and rotation of ommatidia. We propose that these processes are polarized as a consequence of furrow propagation, while more global determinants of dorsoventral and anteroposterior polarity may act less directly by determining the site of furrow initiation.

Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc

Development ◽  
1997 ◽  
Vol 124 (17) ◽  
pp. 3233-3240 ◽  
Author(s):  
D.I. Strutt ◽  
M. Mlodzik
Keyword(s):  
Pattern Formation ◽  
Imaginal Disc ◽  
Morphogenetic Furrow ◽  
Anterior Edge ◽  
Eye Disc ◽  
Drosophila Eye ◽  
Eye Imaginal Disc ◽  
Inductive Signal ◽  
Rate Of Movement

Pattern formation in the eye imaginal disc of Drosophila occurs in a wave that moves from posterior to anterior. The anterior edge of this wave is marked by a contracted band of cells known as the morphogenetic furrow, behind which photoreceptors differentiate. The movement of the furrow is dependent upon the secretion of the signalling protein Hedgehog (Hh) by more posterior cells, and it has been suggested that Hh acts as an inductive signal to induce cells to enter a furrow fate and begin differentiation. To further define the role of Hh in this process, we have analysed clones of cells lacking the function of the smoothened (smo) gene, which is required for transduction of the Hh signal and allows the investigation of the autonomous requirement for hh signalling. These experiments demonstrate that the function of hh in furrow progression is indirect. Cells that cannot receive/transduce the Hh signal are still capable of entering a furrow fate and differentiating normally. However, hh is required to promote furrow progression and regulate its rate of movement across the disc, since the furrow is significantly delayed in smo clones.

The role of Wingless signaling in establishing the anteroposterior and dorsoventral axes of the eye disc

Development ◽  
2001 ◽  
Vol 128 (9) ◽  
pp. 1519-1529 ◽  
Author(s):  
J.D. Lee ◽  
J.E. Treisman
Keyword(s):  
Signaling Molecules ◽  
Morphogenetic Furrow ◽  
Wild Type ◽  
Dorsoventral Axis ◽  
Eye Disc ◽  
Wingless Signaling ◽  
Drosophila Eye ◽  
Ectopic Activation ◽  
Lateral Margins

The posteriorly expressed signaling molecules Hedgehog and Decapentaplegic drive photoreceptor differentiation in the Drosophila eye disc, while at the anterior lateral margins Wingless expression blocks ectopic differentiation. We show here that mutations in axin prevent photoreceptor differentiation and lead to tissue overgrowth and that both these effects are due to ectopic activation of the Wingless pathway. In addition, ectopic Wingless signaling causes posterior cells to take on an anterior identity, reorienting the direction of morphogenetic furrow progression in neighboring wild-type cells. We also show that signaling by Decapentaplegic and Hedgehog normally blocks the posterior expression of anterior markers such as Eyeless. Wingless signaling is not required to maintain anterior Eyeless expression and in combination with Decapentaplegic signaling can promote its downregulation, suggesting that additional molecules contribute to anterior identity. Along the dorsoventral axis of the eye disc, Wingless signaling is sufficient to promote dorsal expression of the Iroquois gene mirror, even in the absence of the upstream factor pannier. However, Wingless signaling does not lead to ventral mirror expression, implying the existence of ventral repressors.

wingless inhibits morphogenetic furrow movement in the Drosophila eye disc

Development ◽  
1995 ◽  
Vol 121 (11) ◽  
pp. 3519-3527 ◽  
Author(s):  
J.E. Treisman ◽  
G.M. Rubin
Keyword(s):  
Posterior Margin ◽  
Ectopic Expression ◽  
Spatial Localization ◽  
Morphogenetic Furrow ◽  
Differentiated Cells ◽  
Repetitive Process ◽  
Eye Disc ◽  
Drosophila Eye ◽  
Lateral Margins ◽  
Eye Imaginal Disc

Differentiation of the Drosophila eye imaginal disc is an asynchronous, repetitive process which proceeds across the disc from posterior to anterior. Its propagation correlates with the expression of decapentaplegic at the front of differentiation, in the morphogenetic furrow. Both differentiation and decapentaplegic expression are maintained by Hedgehog protein secreted by the differentiated cells posterior to the furrow. However, their initiation at the posterior margin occurs prior to hedgehog expression by an unknown mechanism. We show here that the wingless gene contributes to the correct spatial localization of initiation. Initiation of the morphogenetic furrow is restricted to the posterior margin by the presence of wingless at the lateral margins; removal of wingless allows lateral initiation. Ectopic expression of wingless at the posterior margin can also inhibit normal initiation. In addition, the presence of wingless in the center of the disc can prevent furrow progression. These effects of wingless are achieved without altering the expression of decapentaplegic.

Broad-complex, but not ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye

Development ◽  
2001 ◽  
Vol 128 (1) ◽  
pp. 1-11 ◽  
Author(s):  
C.A. Brennan ◽  
T.R. Li ◽  
M. Bender ◽  
F. Hsiung ◽  
K. Moses
Keyword(s):  
Zinc Finger ◽  
Receptor Gene ◽  
Ecdysone Receptor ◽  
Morphogenetic Furrow ◽  
Response Gene ◽  
Ecdysteroid Receptor ◽  
Receptor Isoforms ◽  
Eye Disc ◽  
Drosophila Eye ◽  
Broad Complex

The progression of the morphogenetic furrow in the developing Drosophila eye is an early metamorphic, ecdysteroid-dependent event. Although Ecdysone receptor-encoded nuclear receptor isoforms are the only known ecdysteroid receptors, we show that the Ecdysone receptor gene is not required for furrow function. DHR78, which encodes another candidate ecdysteroid receptor, is also not required. In contrast, zinc finger-containing isoforms encoded by the early ecdysone response gene Broad-complex regulate furrow progression and photoreceptor specification. br-encoded Broad-complex subfunctions are required for furrow progression and proper R8 specification, and are antagonized by other subfunctions of Broad-complex. There is a switch from Broad complex Z2 to Z1 zinc-finger isoform expression at the furrow which requires Z2 expression and responds to Hedgehog signals. These results suggest that a novel hormone transduction hierarchy involving an uncharacterized receptor operates in the eye disc.

Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors

Development ◽  
1995 ◽  
Vol 121 (7) ◽  
pp. 2019-2030 ◽  
Author(s):  
A.P. Jarman ◽  
Y. Sun ◽  
L.Y. Jan ◽  
Y.N. Jan
Keyword(s):  
Sense Organ ◽  
Proneural Gene ◽  
Morphogenetic Furrow ◽  
Helix Loop Helix ◽  
Eye Disc ◽  
In The Wild ◽  
Almost All ◽  
Selection Of ◽  
Stimulation Of Division

The Drosophila gene atonal encodes a basic helix-loop-helix protein similar to those encoded by the proneural genes of the achaete-scute complex (AS-C). The AS-C are required in the Drosophila PNS for the selection of neural precursors of external sense organs. We have isolated mutants of atonal, which reveal that this gene encodes the proneural gene for chordotonal organs and photoreceptors. In atonal mutants, all observable adult chordotonal organs, and almost all embryonic chordotonal organs fail to form; all adult photoreceptors are missing. For both types of sense organ, this defect is already apparent at the level of precursor formation. Therefore it is a failure in the epidermal-neural decision process i.e. a proneural defect. The failure to form photoreceptors results in atrophy of the atonal mutant imaginal disc, due to apoptosis and lack of stimulation of division. Lack of photoreceptors should also eliminate signalling that arises from differentiating photoreceptors and is required for morphogenetic furrow movement in the wild-type eye disc. Nevertheless, a remnant morphogenetic furrow is still observed in the atonal mutant disc. This presumably reflects the process of furrow initiation, which would not depend on signals from developing photoreceptors.

Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina

Development ◽  
1997 ◽  
Vol 124 (2) ◽  
pp. 559-567 ◽  
Author(s):  
F. Chanut ◽  
U. Heberlein
Keyword(s):  
Posterior Margin ◽  
Imaginal Disc ◽  
Photoreceptor Cells ◽  
Morphogenetic Furrow ◽  
Retinal Differentiation ◽  
Eye Disc ◽  
Forward Edge ◽  
Eye Imaginal Disc ◽  
Precise Role

Morphogenesis in the Drosophila retina initiates at the posterior margin of the eye imaginal disc by an unknown mechanism. Upon initiation, a wave of differentiation, its forward edge marked by the morphogenetic furrow (MF), proceeds anteriorly across the disc. Progression of the MF is driven by hedgehog (hh), expressed by differentiating photoreceptor cells. The TGF-beta homolog encoded by decapentaplegic (dpp) is expressed at the disc's posterior margin prior to initiation and in the furrow, under the control of hh, during MF progression. While dpp has been implicated in eye disc growth and morphogenesis, its precise role in retinal differentiation has not been determined. To address the role of dpp in initiation and progression of retinal differentiation we analyzed the consequences of reduced and increased dpp function during eye development. We find that dpp is not only required for normal MF initiation, but is sufficient to induce ectopic initiation of differentiation. Inappropriate initiation is normally inhibited by wingless (wg). Loss of dpp function is accompanied by expansion of wg expression, while increased dpp function leads to loss of wg transcription. In addition, dpp is required to maintain, and sufficient to induce, its own expression along the disc's margins. We postulate that dpp autoregulation and dpp-mediated inhibition of wg expression are required for the coordinated regulation of furrow initiation and progression. Finally, we show that in the later stages of retinal differentiation, reduction of dpp function leads to an arrest in MF progression.

A Genetic Screen to Identify Components of the sina Signaling Pathway in Drosophila Eye Development

Genetics ◽  
1998 ◽  
Vol 148 (1) ◽  
pp. 277-286
Author(s):  
Thomas P Neufeld ◽  
Amy H Tang ◽  
Gerald M Rubin
Keyword(s):  
Cell Fate ◽  
Eye Development ◽  
Ectopic Expression ◽  
Genetic Screen ◽  
Cell Fate Specification ◽  
Morphogenetic Furrow ◽  
Drosophila Homolog ◽  
Drosophila Eye ◽  
Ubiquitin Conjugating Enzyme ◽  
Seven In Absentia

AbstractSpecification of the R7 photoreceptor cell in the developing Drosophila eye requires the seven in absentia (sina) gene. We demonstrate that ectopic expression of sina in all cells behind the morphogenetic furrow disrupts normal eye development during pupation, resulting in a severely disorganized adult eye. Earlier events of cell fate specification appear unaffected. A genetic screen for dominant enhancers and suppressors of this phenotype identified mutations in a number of genes required for normal eye development, including UbcD1, which encodes a ubiquitin conjugating enzyme; SR3-4a, a gene previously implicated in signaling downstream of Ras1; and a Drosophila homolog of the Sin3A transcriptional repressor.

A Genetic Screen to Identify Components of the sina Signaling Pathway in Drosophila Eye Development

Genetics ◽  
1998 ◽  
Vol 148 (1) ◽  
pp. 277-286 ◽  
Author(s):  
Thomas P Neufeld ◽  
Amy H Tang ◽  
Gerald M Rubin
Keyword(s):  
Cell Fate ◽  
Eye Development ◽  
Ectopic Expression ◽  
Genetic Screen ◽  
Cell Fate Specification ◽  
Morphogenetic Furrow ◽  
Drosophila Homolog ◽  
Drosophila Eye ◽  
Ubiquitin Conjugating Enzyme ◽  
Seven In Absentia

Abstract Specification of the R7 photoreceptor cell in the developing Drosophila eye requires the seven in absentia (sina) gene. We demonstrate that ectopic expression of sina in all cells behind the morphogenetic furrow disrupts normal eye development during pupation, resulting in a severely disorganized adult eye. Earlier events of cell fate specification appear unaffected. A genetic screen for dominant enhancers and suppressors of this phenotype identified mutations in a number of genes required for normal eye development, including UbcD1, which encodes a ubiquitin conjugating enzyme; SR3-4a, a gene previously implicated in signaling downstream of Ras1; and a Drosophila homolog of the Sin3A transcriptional repressor.

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