Catching the Next Wave: Patterning of the Drosophila Eye by the Morphogenetic Furrow

2013 ◽  
pp. 75-97 ◽  
Author(s):  
Justin P. Kumar
Keyword(s):  
Morphogenetic Furrow ◽  
Drosophila Eye

frizzled regulates mirror-symmetric pattern formation in the Drosophila eye

Development ◽  
1995 ◽  
Vol 121 (9) ◽  
pp. 3045-3055 ◽  
Author(s):  
L. Zheng ◽  
J. Zhang ◽  
R.W. Carthew
Keyword(s):  
Pattern Formation ◽  
Cell Surface ◽  
Transmembrane Protein ◽  
Photoreceptor Cells ◽  
Mirror Image ◽  
Morphogenetic Furrow ◽  
Symmetric Pattern ◽  
Mosaic Analysis ◽  
Drosophila Eye ◽  
A Cell

Coordinated morphogenesis of ommatidia during Drosophila eye development establishes a mirror-image symmetric pattern across the entire eye bisected by an anteroposterior equator. We have investigated the mechanisms by which this pattern formation occurs and our results suggest that morphogenesis is coordinated by a graded signal transmitted bidirectionally from the presumptive equator to the dorsal and ventral poles. This signal is mediated by frizzled, which encodes a cell surface transmembrane protein. Mosaic analysis indicates that frizzled acts non-autonomously in an equatorial to polar direction. It also indicates that relative levels of frizzled in photoreceptor cells R3 and R4 of each ommatidium affect their positional fate choices such that the cell with greater frizzled activity becomes an R3 cell and the cell with less frizzled activity becomes an R4 cell. Moreover, this bias affects the choice an ommatidium makes as to which direction to rotate. Equator-outwards progression of elav expression and expression of the nemo gene in the morphogenetic furrow are regulated by frizzled, which itself is dynamically expressed about the morphogenetic furrow. We propose that frizzled mediates a bidirectional signal emanating from the equator.

Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway

Development ◽  
1999 ◽  
Vol 126 (24) ◽  
pp. 5795-5808 ◽  
Author(s):  
S. Greenwood ◽  
G. Struhl
Keyword(s):  
Transcription Factor ◽  
Short Range ◽  
Morphogenetic Furrow ◽  
Serine Threonine Kinase ◽  
Present Evidence ◽  
Threonine Kinase ◽  
Drosophila Eye ◽  
Undifferentiated Cells ◽  
Hh Signaling ◽  
Necessary And Sufficient

During Drosophila eye development, Hedgehog (Hh) protein secreted by maturing photoreceptors directs a wave of differentiation that sweeps anteriorly across the retinal primordium. The crest of this wave is marked by the morphogenetic furrow, a visible indentation that demarcates the boundary between developing photoreceptors located posteriorly and undifferentiated cells located anteriorly. Here, we present evidence that Hh controls progression of the furrow by inducing the expression of two downstream signals. The first signal, Decapentaplegic (Dpp), acts at long range on undifferentiated cells anterior to the furrow, causing them to enter a ‘pre-proneural’ state marked by upregulated expression of the transcription factor Hairy. Acquisition of the pre-proneural state appears essential for all prospective retinal cells to enter the proneural pathway and differentiate as photoreceptors. The second signal, presently unknown, acts at short range and is transduced via activation of the Serine-Threonine kinase Raf. Activation of Raf is both necessary and sufficient to cause pre-proneural cells to become proneural, a transition marked by downregulation of Hairy and upregulation of the proneural activator, Atonal (Ato), which initiates differentiation of the R8 photoreceptor. The R8 photoreceptor then organizes the recruitment of the remaining photoreceptors (R1-R7) through additional rounds of Raf activation in neighboring pre-proneural cells. Finally, we show that Dpp signaling is not essential for establishing either the pre-proneural or proneural states, or for progression of the furrow. Instead, Dpp signaling appears to increase the rate of furrow progression by accelerating the transition to the pre-proneural state. In the abnormal situation in which Dpp signaling is blocked, Hh signaling can induce undifferentiated cells to become pre-proneural but does so less efficiently than Dpp, resulting in a retarded rate of furrow progression and the formation of a rudimentary eye.

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 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.

scholarly journals Hairy and Emc negatively regulate morphogenetic furrow progression in the drosophila eye

Cell ◽  
1995 ◽  
Vol 80 (6) ◽  
pp. 879-887 ◽  
Author(s):  
Nadean L Brown ◽  
Carol A Sattler ◽  
Stephen W Paddock ◽  
Sean B Carroll
Keyword(s):  
Morphogenetic Furrow ◽  
Drosophila Eye

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.

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