Skip to main content

Early Retinal Development in Drosophila

  • Chapter
Vertebrate Eye Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 31))

Abstract

Like other insects, the fruit fly Drosophila melanogaster has a compound eye, made up of approximately 800 individual eyes or ommatidia. The eye arises from the eye imaginal disk, which is part of the compound eye-antennal disk. The cells that will form this disk invaginate from the ectoderm during late embryogenesis (Jurgens and Hartenstein 1993); the disk primordium then grows inside the larva, where it consists of an epithelial bilayer. One columnar layer will give rise to all the cell types of the retina; it is covered by a squamous epithelial sheet called the peripodial membrane, which later contributes to the surface of the head (Haynie and Bryant 1986). Differentiation of the retina begins in the third of the three larval stages, known as instars, and continues during the first few days of pupal development (Ready et al. 1976; Fig. 1). In spite of the many morphological and developmental differences between fly and vertebrate eyes, many of the molecules involved appear to be conserved.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Baker NE, Yu S-Y (1997) Proneural function of neurogenic genes in the developing Drosophila eye. Curr Biol 7: 122–132

    Article  PubMed  CAS  Google Scholar 

  • Banerjee U, Zipursky SL (1990) The role of cell-cell interaction in the development of the Drosophila visual system. Neuron 4: 177–187

    Article  PubMed  CAS  Google Scholar 

  • Blackman RK, Sanicola M, Raftery LA, Gillevet T, Gelbart WM (1991) An extensive 3′ cisregulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-b family in Drosophila. Development 111: 657–666

    PubMed  CAS  Google Scholar 

  • Bonini NM, Leiserson WM, Benzer S (1993) The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72: 379–395

    Article  PubMed  CAS  Google Scholar 

  • Bonini NM, Bui QT, Gray-Board GL, Warrick JM (1997) The Drosophila eyes absent gene directs ectopic eye formation in a pathway conserved between flies and vertebrates. Development 124:4819–4826

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Brennan CA, Ashburner M, Moses K (1998) Ecdysone pathway is required for furrow progression in the developing Drosophila eye. Development 125: 2653–2664

    PubMed  CAS  Google Scholar 

  • Brown NL, Sattler CA, Markey DR, Carroll SB (1991) hairy gene function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates. Development 113:1245–1256

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Brown NL, Paddock SW, Sattler CA, Cronmiller C, Thomas BJ, Carroll SB (1996) Daughterless is required for Drosophila photoreceptor cell determination, eye morphogenesis, and cell cycle progression. Developmental Biology 179: 65–78

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chanut F, Heberlein U (1997) Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124: 559–567

    PubMed  CAS  Google Scholar 

  • Chen R, Amoui M, Zhang Z, Mardon G (1997) Dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell 91:893–904

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Halder G, Zhang Z, Mardon G (1999) Signaling by the TGF-b homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila. Development 126: 935–943

    PubMed  CAS  Google Scholar 

  • Cheyette BNR, Green PJ, Martin K, Garren H, Hartenstein V, Zipursky SL (1994) The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12: 977–996

    Article  PubMed  CAS  Google Scholar 

  • Cho K-O, Choi K-W (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396: 272–276

    Article  PubMed  CAS  Google Scholar 

  • 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. Molecular Cell 3: 297–307

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dominguez M, Hafen E (1997) Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev 11: 3254–3264

    Article  PubMed  CAS  Google Scholar 

  • Dominguez M, Wasserman JD, Freeman M (1998) Multiple functions of the EGF receptor in Drosophila eye development. Curr Biol 8: 1039–1048

    Article  PubMed  CAS  Google Scholar 

  • Freeman M (1997) Cell determination strategies in the Drosophila eye. Development 124:261–270

    PubMed  CAS  Google Scholar 

  • Glardon S, Callaerts P, Halder G, Gehring WJ (1997) Conservation of Pax-6 in a lower chordate, the ascidian Phallusia mammillata. Development 124:817–825

    PubMed  CAS  Google Scholar 

  • Glardon S, Holland LZ, Gehring WJ, Holland ND (1998) Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): insights into eye and photoreceptor evolution. Development 125: 2701–2710

    PubMed  CAS  Google Scholar 

  • Gomez-Skarmeta JL, Glavic A, de la Calle-Mustienes E, Modolell J, Mayor R (1998) Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neutral plate. Embo Journal 17: 181–190

    Article  PubMed  CAS  Google Scholar 

  • Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267: 1788–1792

    Article  PubMed  CAS  Google Scholar 

  • Halder 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

    PubMed  CAS  Google Scholar 

  • Hammond KL, Hanson IM, Brown AG, Lettice LA, Hill RE (1998) Mammalian and Drosophila dachshund genes are related to the Ski proto-oncogene and are expressed in eye and limb. Mech Dev 74: 121–131

    Article  PubMed  CAS  Google Scholar 

  • Haynie JL, Bryant PJ (1986) Development of the eye-antenna imaginal disk and morphogenesis of the adult head in Drosophila melanogaster. J Exp Zool 237: 293–308

    Article  PubMed  CAS  Google Scholar 

  • 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 disk. Development 125:3741–3751

    PubMed  CAS  Google Scholar 

  • Heberlein U, Moses K (1995) Mechanisms of Drosophila retinal morphogenesis: the virtues of being progressive. Cell 81: 987–990

    Article  PubMed  CAS  Google Scholar 

  • Heberlein U, Wolff T, Rubin GM (1993) The TGFb homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75: 913–926

    Article  PubMed  CAS  Google Scholar 

  • Heberlein U, Singh CM, Luk AY, Donohoe TJ (1995) Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature 373: 709–711

    Article  PubMed  CAS  Google Scholar 

  • Heberlein U, Borod ER, Chanut FA (1998) Dorsoventral patterning in the Drosophila retina by wingless. Development 125: 567–577

    PubMed  CAS  Google Scholar 

  • Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, van Heyningen V (1991) Mouse small eye results from mutations in a paired-like homeoboxcontaining gene. Nature 354: 522–525

    Article  PubMed  CAS  Google Scholar 

  • Horsfield J, Penton A, Secombe J, Hoffman FM, Richardson H (1998) Decapentaplegic is required for arrest in G1 phase during Drosophila eye development. Development 125: 5069–5078

    PubMed  CAS  Google Scholar 

  • Jang C-C, Jones N, Chao J-L, Bessarab DA, Kuo YM, Jun S, Desplan C, Beckendorf S, Sun YH (1999) Two Pax genes, eye gone and eyeless, act in parallel in determining Drosophila eye development. Development (submitted)

    Google Scholar 

  • Jarman AP (1996) Epithelial polarity in the Drosophila compound eye: eyes left or right? Trends Genet 12: 121–123

    Article  PubMed  CAS  Google Scholar 

  • Jarman AP, Grau Y, Jan LY, Jan YN (1993) Atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307–1321

    Article  PubMed  CAS  Google Scholar 

  • Jarman AP, Grell EH, Ackerman L, Jan LY, Jan YN (1994) atonal is the proneural gene for Drosophila photoreceptors. Nature 369: 398–400

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Jurgens G, Hartenstein V (1993) The terminal regions of the body pattern. In: The development of Drosophila Melanogaster. Bate M, Martinez-Arias A (ed) Cold Spring Harbor Laboratory Press; Cold Spring Harbor, New York, pp 687–746

    Google Scholar 

  • Kumar JP, Tio M, Hsiung F, Akopyan S, Gabay L, Seger R, Shilo B-Z, Moses K (1998) Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125: 3875–3885

    PubMed  CAS  Google Scholar 

  • Loosli F, Kmita-Cunisse M, Gehring WJ (1996) Isolation of a Pax-6 homolog from the ribbonworm Lineus sanguineus. Proc Natl Acad Sci USA 93: 2658–2663

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mardon G, Solomon NM, Rubin GM (1994) Dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120: 3473–3486

    PubMed  CAS  Google Scholar 

  • Masucci JD, Miltenberger RJ, Hoffmann FM (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal disks is regulated by 3′ cis-regulatory elements. Genes Dev 4: 2011–2023

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Oliver G, Mailhos A, Wehr R, Copeland NG, Jenkins NA, Gruss P (1995) Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121: 4045–4055

    PubMed  CAS  Google Scholar 

  • Pai C-Y, Kuo T-S, Jaw JJ, 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

    Article  PubMed  CAS  Google Scholar 

  • Pan D, Rubin GM (1995) cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal disks. Cell 80: 543–552

    Article  PubMed  CAS  Google Scholar 

  • Pan D, Rubin GM (1998) Targeted expression of teashirt induces ectopic eyes in Drosophila. Proc Natl Acad Sci USA 95: 15508–15512

    Article  PubMed  CAS  Google Scholar 

  • Panin VM, Papayannopoulos V, Wilson R, Irvine KD (1997) Fringe modulates Notch-ligand interactions. Nature 387: 908–912

    Article  PubMed  CAS  Google Scholar 

  • Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281:2031–2034

    Article  PubMed  CAS  Google Scholar 

  • Penton A, Selleck SB, Hoffmann FM (1997) Regulation of cell cycle synchronization by decapentaplegic during Drosophila eye development. Science 275: 203–206

    Article  PubMed  CAS  Google Scholar 

  • Pignoni F, Zipursky SL (1997) Induction of Drosophila eye development by Decapentaplegic. Development 124: 271–278

    PubMed  CAS  Google Scholar 

  • Pignoni F, Hu B, Zavitz KH, Xiao J, Garrity PA, Zipursky SL (1997) The eye specification proteins so and eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91: 881–892

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53: 217–240

    Article  PubMed  CAS  Google Scholar 

  • Royet J, Finkelstein R (1997) Establishing primordia in the Drosophila eye-antennal imaginal disk: the roles of decapentaplegic, wingless and hedgehog. Development 124: 4793–4800

    PubMed  CAS  Google Scholar 

  • Seo H-C, Drivenes O, Ellingsen S, Fjose A (1998) Expression of two zebrafish homologs of the murine Six3 gene demarcates the initial eye primordia. Mech Dev 73: 45–57

    Article  PubMed  CAS  Google Scholar 

  • Serikaku MA, O’Tousa JE (1994) Sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 138: 1137–1150

    PubMed  CAS  Google Scholar 

  • Shen W, Mardon G (1997) Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124: 45–52

    PubMed  CAS  Google Scholar 

  • Spencer SA, Powell PA, Miller DT, Cagan RL (1998) Regulation of EGF receptor signaling establishes pattern across the developing Drosophila retina. Development 125: 4777–4790

    PubMed  CAS  Google Scholar 

  • Strutt DI, Mlodzik M (1997) Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disk. Development 124: 3233–3240

    PubMed  CAS  Google Scholar 

  • Tomarev SI, Callaerts P, Kos L, Zinovieva R, Halder G, Gehring W, Piatigorsky J (1997) Squid Pax-6 and eye development. Proc Natl Acad Sci USA 94:2421–2426

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson A, Ready DF (1987) Neuronal differentiation in the Drosophila ommatidium. Dev Biol 120: 366–376

    Article  PubMed  CAS  Google Scholar 

  • Ton CCT, Hirvonen H, Miwa H, Weil MM, Monaghan P, Jordan T, van Heyningen V, Hastie ND, Meijers-Heijboer H, Drechsler M, et al. (1991) Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region. Cell 67: 1059–1074

    Article  PubMed  CAS  Google Scholar 

  • Treisman JE (1999) A conserved blueprint for the eye? Bioessays 21: 843–850

    Article  PubMed  CAS  Google Scholar 

  • Treisman JE, Heberlein U (1998) Eye development in Drosophila: Formation of the eye field and control of differentiation. Current Topics in Dev Biol 39: 119–158

    Article  CAS  Google Scholar 

  • Treisman JE, Rubin GM (1995) Wingless inhibits morphogenetic furrow movement in the Drosophila eye disk. Development 121:3519–3527

    PubMed  CAS  Google Scholar 

  • Wehrli M, Tomlinson A (1995) Epithelial planar polarity in the developing Drosophila eye. Development 121: 2451–2459

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Xu P-X, Woo I, Her H, Beier DR, Maas RL (1997) Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 124: 219–231

    PubMed  CAS  Google Scholar 

  • Zelhof AC, Ghbeish N, Tsai C, Evans RM, McKeown M (1997) A role for Ultrapiracle, the Drosophila RXR, in morphogenetic furrow movement and photoreceptor cluster formation. Development 124: 2499–2506

    PubMed  CAS  Google Scholar 

  • Zimmerman JE, Bui QT, Steingrimsson E, Nagle DL, Fu W, Genin A, Spinner NB, Copeland NG, Jenkins NA, Bucan M, Bonini NM (1997) Cloning and characterization of two vertebrate homologs of the Drosophila eyes absent gene. Genome Res 7: 128–141

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Heberlein, U., Treisman, J.E. (2000). Early Retinal Development in Drosophila . In: Fini, M.E. (eds) Vertebrate Eye Development. Results and Problems in Cell Differentiation, vol 31. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-46826-4_3

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-46826-4_3

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-53678-6

  • Online ISBN: 978-3-540-46826-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics