Abstract
Unlike other imaginal discs, the Drosophila eye disc has a progressive pattern of differentiation. Photoreceptor clusters begin to form at the posterior margin of the eye disc in the third larval instar, and more anterior rows of clusters then differentiate in succession (Ready et al. 1976). Just prior to their differentiation, cells undergo an apical constriction and apical-basal contraction that produces an indentation in the disc known as the morphogenetic furrow (MF; Ready et al. 1976). Cells anterior to the MF divide actively and appear unpatterned. Just posterior to the MF, cells assemble into evenly spaced rosettes; slightly more posteriorly these transform into arcs, and the arcs then close to produce five-cell preclusters (Wolff and Ready 1991). Concurrently, these cells initiate a program of gene expression resulting in the appearance of neuralspecific markers in a defined sequence in the cells of each cluster (Tomlinson and Ready 1987). Cells in the MF are arrested in the G1 phase of the cell cycle (Thomas et al. 1994); posterior to the MF, cells excluded from the preclusters undergo one more round of division, the second mitotic wave, to generate the remaining cells of each ommatidium (Ready et al. 1976; Wolff and Ready 1991). This orderly and sequential pattern of differentiation, proliferation, and morphogenesis is organized by a set of signaling molecules that also direct many other developmental processes. The expression patterns and interactions of these molecules in the developing eye disc are shown in Fig. 1.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Baker NE (1988) Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102: 489–497
Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368: 208–214
Benlali A, Draskovic I, Hazelett DJ, Treisman JE (2000) act up controls actin polymerization to alter cell shape and restrict Hedgehog signaling in the Drosophila eye disc. Cell 101: 271–81
Blackman RK, Sanicola M, Raftery LA, Gillevet T, Gelbart WM (1991) An extensive 3’ cis-regulatory region directs the imaginal disc expression of decapentaplegic, a member of the TGF-ß family in Drosophila. Development 111: 657–665
Borod ER, Heberlein U (1998) Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev Biol 197: 187–197
Brennan CA, Ashburner M, Moses K (1998) Ecdysone pathway is required for furrow progression in the developing Drosophila eye. Development 125: 2653–64
Brennan CA, Li TR, Bender M, Hsiung F, Moses K (2001) Broad-complex, but not Ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye. Development 128: 1–11
Brown NL, Sattler CA, Paddock SW, Carroll SB (1995) Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell 80: 879–887
Bruckner K, Perez L, Clausen H, Cohen S (2000) Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406: 411–415
Burke R, Basler K (1996) Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of dpp signaling. Dev Biol 179: 360–368
Burrill JD, Easter SS Jr (1995) The first retinal axons and their microenvironment in zebrafish: cryptic pioneers and the pretract. J Neurosci 15: 2935–2947
Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11: 3286–3305
Cavodeassi F, Diez Del Corral R, Campuzano S, Dominguez M (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126: 4933–4942
Chanut F, Heberlein U (1995) Role of the morphogenetic furrow in establishing polarity in the Drosophila eye. Development 121: 4085–4094
Chanut F, Heberlein U (1997a) Retinal morphogenesis in Drosophila: hints from an eye-specific decapentaplegic allele. Dev Genet 20: 197–207
Chanut F, Heberlein U (1997b) Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124: 559–567
Chanut F, Luk A, Heberlein U (2000) A screen for dominant modifiers of ro(Dom), a mutation that disrupts morphogenetic furrow progression in Drosophila, identifies groucho and Hairless as regulators of atonal expression. Genetics 156: 1203–1217
Chen R, Haider G, Zhang Z, Mardon G (1999) Signaling by the TGF-ß homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila. Development 126: 935–943
Cho K-O, Choi K-W (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396: 272–276
Cho K-O, Chern J, Izaddoost S, Choi K-W (2000) Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103: 331–342
Curtiss J, Mlodzik M (2000) Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent. Development 127: 1325–1336
Czerny T, Haider G, Kloter U, Souabni A, Gehring WJ, Busslinger M (1999) twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell 3: 297–307
Das P, Maduzia LL, Wang H, Finelli AL, Cho SH, Smith MM, Padgett RW (1998) The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling. Development 125: 1519–1528
De Celis JF, Garcia-Bellido A, Bray SJ (1996) Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122: 359–369
Diaz-Benjumea FJ, Cohen SM (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75: 741–52
Diaz-Benjumea FJ, Cohen SM (1995) Serrate signals through Notch to establish a wingless-dependent organizer at the dorsal-ventral compartment boundary of the Drosophila wing. Development 121: 4215–4225
Doherty D, Feger G, Younger-Shepherd S, Jan LY, Jan YN (1996) Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes Dev 10: 421–434
Dokucu ME, Zipursky SL, Cagan RL (1996) Atonal, Rough and the resolution of proneural dusters in the developing Drosophila retina. Development 122: 4139–4147
Dominguez M (1999) Dual role for hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development 126: 2345–2353
Dominguez M, de Celis JF (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396: 276–278
Dominguez M, Hafen E (1997) Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev 11: 3254–3264
Fietz MJ, Concordet JP, Barbosa R, Johnson R, Krauss S, McMahon AP, Tabin C, Ingham PW (1994) The hedgehog gene family in Drosophila and vertebrate development. Development (Suppl) 36: 43–51
Gomez-Skarmeta JL, del Corral RD, de la Calle-Mustienes E, Ferre-Marco D, Modolell J (1996) araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85: 95–105
Greenwood S, Struhl G (1999) Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development 126: 5795–5808
Haider G, Callaerts P, Flister S, Walldorf U, Kloter U, Gehring WJ (1998) Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125: 2181–2191
Hazelett DJ, Bourouis M, Walldorf U, Treisman JE (1998) decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125: 3741–3751
Heberlein U, Wolff T, Rubin GM (1993) The TGF/3 homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75: 913–926
Heberlein U, Singh CM, Luk AY, Donohoe TJ (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373: 709–711
Heberlein U, Borod ER, Chanut FA (1998) Dorsoventral patterning in the Drosophila retina by wingless. Development 125: 567–577
Heitzler P, Haenlin M, Ramain P, Calleja M, Simpson P (1996) A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and bristle positioning in Drosophila. Genetics 143: 1271–1286
Heslip TR, Theisen H, Walker H, Marsh JL (1997) SHAGGY and DISHEVELLED exert opposite effects on wingless and decapentaplegic expression and on positional identity in imaginal discs. Development 124: 1069–1078
Horsfield J, Penton A, Secombe J, Hoffman FM, Richardson H (1998) decapentaplegic is required for arrest in Cl phase during Drosophila eye development. Development 125: 5069–5078
Jarman AP, Grell EH, Ackerman L, Jan LY, Jan YN (1994) atonal is the proneural gene for Drosophila photoreceptors. Nature 369: 398–400
Jarman AP, Sun Y, Jan LY, Jan YN (1995) Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121: 2019–2030
Jensen AM, Wallace VA (1997) Expression of Sonic hedgehog and its putative role as a precursor cell mitogen in the developing mouse retina. Development 124: 363–371
Kimmel BE, Heberlein U, Rubin GM (1990) The homeodomain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev 4: 712–727
Lecuit T, Brook WJ, Ng M, Sun H, Cohen SM (1996) Two distinct mechanisms for long-range patterning by decapentaplegic in the Drosophila wing. Nature 381: 387–393
Lee JD, Treisman JE (2001) The role of Wingless signaling in establishing the anterior-posterior and dorsal-ventral axes of the eye disc. Development 128: 1519–1529.
Levine EM, Roelink H, Turner J, Reh TA (1997) Sonic hedgehog promotes rod photoreceptor differentiation in mammalian retinal cells in vitro. J Neurosci 17: 6277–6288
Ma C, Moses K (1995) wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development 121: 2279–2289
Ma C, Zhou Y, Beachy PA, Moses K (1993) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75: 927–938
Masucci JD, Miltenberger RJ, Hoffmann FM (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3’ cis-regulatory elements. Genes Dev 4: 2011–2023
Maurel-Zaffran C, Treisman JE (2000) pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127: 1007–1016
McCabe KL, Gunther EC, Reh TA (1999) The development of the pattern of retinal ganglion cells in the chick retina: mechanisms that control differentiation. Development 126: 5713–5724
McNeill H, Yang CH, Brodsky M, Ungos J, Simon MA (1997) mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev 11: 1073–1082
Moloney DJ, Panin VM, Johnston SH, Chen J, Shao L, Wilson R, Wang Y, Stanley P, Irvine KD, Haltiwanger RS, Vogt TF (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406: 369–735
Mullor JL, Calleja M, Capdevila J, Guerrero I (1997) Hedgehog activity, independent of decapentaplegic, participates in wing disc patterning. Development 124: 1227–1237
Nellen D, Burke R, Struhl G, Basler K (1996) Direct and long-range action of a dpp morphogen gradient. Cell 85: 357–368
Netter S, Fauvarque MO, Diez del Corral R, Dura JM, Coen D (1998) white transgene insertions presenting a dorsal/ventral pattern define a single cluster of homeobox genes that is silenced by the polycomb-group proteins in Drosophila melanogaster. Genetics 149: 257–275
Neumann CJ, Nusslein-Volhard C (2000) Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289: 2137–2139
Padgett RW, St Johnston RD, Gelbart WM (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature 325: 81–84
Pai C-Y, Kuo T-S, Jaw TJ, Kurant E, Chen C-T, Bessarab DA, Salzberg A, Sun YH (1998) The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, Extradenticle, and suppresses eye development in Drosophila. Genes Dev 12: 435–446
Pan D, Rubin GM (1995) cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs. Cell 80: 543–552
Panin VM, Papayannopoulos V, Wilson R, Irvine KD (1997) Fringe modulates Notch-ligand interactions. Nature 387: 908–912
Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281: 2031–2034
Penton A, Selleck SB, Hoffmann FM (1997) Regulation of cell cycle synchronization by decapentaplegic during Drosophila eye development. Science 275: 203–206
Pichaud F, Casares F (2000) homothorax and iroquois-C genes are required for the establishment of territories within the developing eye disc. Mech Dev 96: 15–25
Pignoni F, Zipursky SL (1997) Induction of Drosophila eye development by Decapentaplegic. Development 124: 271–278
Pignoni F, Hu B, Zavitz KH, Xiao J, Garrity PA, Zipursky SL (1997) The eye specification proteins so and eya form a complex and multiple steps in Drosophila eye development. Cell 91: 881–892
Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265: 785–789
Ramain P, Heitzler P, Haenlin M, Simpson P (1993) pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development 119: 1277–1291
Raymond PA, Barthel LK, Curran GA (1995) Developmental patterning of rod and cone photoreceptors in embryonic zebrafish. J Comp Neurol 359: 537–50
Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53: 217–240
Royet J, Finkelstein R (1997) Establishing primordia in the Drosophila eye-antennal imaginal disc: the roles of decapentaplegic, wingless and hedgehog. Development 124: 4793–4800
Schmitt EA, Dowling JE (1996) Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish, Danio rerio. J Comp Neurol 371: 222–234
Stenkamp DL, Frey RA, Prabhudesai SN, Raymond PA (2000) Function for Hedgehog genes in zebrafish retinal development. Dev Biol 220: 238–252
St Johnston RD, Hoffmann FM, Blackman RK, Segal D, Grimaila R, Padgett RW, Irick HA, Gelbart WM (1990) Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev 4: 1114–1127
Strigini M, Cohen SM (1997) A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124: 4697–4705
Strutt DI, Mlodzik M (1996) The regulation of hedgehog and decapentaplegic during Drosophila eye imaginal disc development. MOD 58: 39–50
Strutt DI, Mlodzik M (1997) Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc. Development 124: 3233–3240
Strutt DI, Wiersdorff V, Mlodzik M (1995) Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A. Nature 373: 705–709
Tabata T, Eaton S, Kornberg TB (1992) The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 6: 2635–2645
Tabata T, Schwartz C, Gustayson E, Ali Z, Kornberg TB (1995) Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development 121: 3359–3369
Thomas BJ, Gunning DA, Cho J, Zipursky SL (1994) Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1. Cell 77: 1003–1014
Tomlinson A, Ready DF (1987) Neuronal differentiation in the Drosophila ommatidium. Dev Biol 120: 366–376
Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121: 3519–3527
Wehrli M, Tomlinson A (1995) Epithelial planar polarity in the developing Drosophila eye. Development 121: 2451–2459
Wiersdorff V, Lecuit T, Cohen SM, Mlodzik M (1996) Mad acts downstream of dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122: 2153–2162
Wolff T, Ready DF (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113: 841–850
Yang CH, Simon MA, McNeill H (1999) mirror controls planar polarity and equator formation through repression of fringe expression and through control of cell affinities. Development 126: 5857–5866
Zecca M, Basler K, Struhl G (1995) Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121: 2265–2278
Zeidler MP, Perrimon N, Strutt DI (1999) Polarity determination in the Drosophila eye: a novel role for unpaired and JAK/STAT signaling. Genes Dev 13: 1342–1353
Zelhof AC, Ghbeish N, Tsai C, Evans RM, McKeown M (1997) A role for ultraspiracle, the Drosophila RXR, in morphogenetic furrow movement and photoreceptor cluster formation. Development 124: 2499–2506
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Lee, J.D., Treisman, J.E. (2002). Regulators of the Morphogenetic Furrow. In: Moses, K. (eds) Drosophila Eye Development. Results and Problems in Cell Differentiation, vol 37. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-45398-7_3
Download citation
DOI: https://doi.org/10.1007/978-3-540-45398-7_3
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-53640-3
Online ISBN: 978-3-540-45398-7
eBook Packages: Springer Book Archive