Skip to main content
SpringerLink
Log in

Retinal Specification and Determination in Drosophila

  • Chapter
Book cover Drosophila Eye Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 37))

Abstract

Dipteran insects such as Drosophila obtain visual information using compound eyes. In Drosophila,these compound eyes are composed of approximately 800 unit eyes called ommatidia. An ommatidium contains eight distinct photoreceptor cells, each of which projects an axon directly to the optic lobe of the brain. This structure contrasts sharply with the mammalian eye, which contains a single lens and a retina with multiple layers of neurons. In spite of these and other substantial differences in the morphological appearance of insect and vertebrate eyes, work in the last several years has revealed common underlying genetic pathways controlling retinal cell fate specification. This discovery is surprising since the eye was considered an extreme case of convergent evolution, evolving independently as many as 40 different times (reviewed in Land and Fernald 1992). Much of the flurry of molecular and genetic data that has accumulated in recent years challenges this notion and suggests divergence from a single, prototypical visual processing unit. Thus, Drosophila has proven to be an excellent model system for identifying new genes that are conserved in vertebrate retinal development. This chapter will mainly be concerned with describing the factors responsible for specification and determination of retinal cell fate in Drosophila.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
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

  • Abu-Shaar M, Mann RS (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125: 3821–3830

    PubMed  CAS  Google Scholar 

  • Baker NE (1988a) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol 125: 96–108

    Article  PubMed  CAS  Google Scholar 

  • Baker NE (1988b) 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

    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, Grayboard 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 

  • Bonini NM, Leiserson WM, Benzer S (1998) Multiple roles of the eyes absent gene in Drosophila. Dev Biol 196: 42–57

    Article  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 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415

    PubMed  CAS  Google Scholar 

  • Bui QT, Zimmerman JE, Liu H, Bonini NM (2000) Molecular analysis of Drosophila eyes absent mutants reveals features of the conserved eya domain. Genetics 155: 709–720

    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 

  • Caubit X, Thangarajah R, Theil T, Wirth J, Nothwang HG, Ruther U, Krauss S (1999) Mouse Dac, a novel nuclear factor with homology to Drosophila dachshund shows a dynamic expression in the neural crest, the eye, the neocortex, and the limb bud. Dev Dyn 214: 66–80

    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 ZH, Mardon G (1997) Dachshund and Eyes Absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell 91: 893–903

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Halder 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

    PubMed  CAS  Google Scholar 

  • Cheyette BN, 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 

  • Chuang PT, Kornberg TB (2000) On the range of Hedgehog signaling. Curr Opin Genet Dev 10: 515–522

    Article  PubMed  CAS  Google Scholar 

  • Cohen SB, Nicol R, Stavnezer E (1998) A domain necessary for the transforming activity of SnoN is required for specific DNA binding, transcriptional repression and interaction with TAF(II) 110. Oncogene 17: 2505–2513

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Czerny T, Halder 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

    Google Scholar 

  • Dahl E, Koseki H, Balling R (1997) Pax genes and organogenesis. Bioessays 19: 755–765

    Google Scholar 

  • Daniel A, Dumstrei K, Lengyel JA, Hartenstein V (1999) The control of cell fate in the embryonic visual system by atonal, tailless and EGFR signaling. Development 126: 2945–2954

    PubMed  CAS  Google Scholar 

  • Davis RJ, Shen W, Heanue TA, Mardon G (1999) Mouse Dach, a homologue of Drosophila dachshund, is expressed in the developing retina, brain and limbs. Dev Genes Evol 209: 526–536

    Article  PubMed  CAS  Google Scholar 

  • Desplan C (1997) Eye development-governed by a dictator or a junta? Cell 91: 861–864

    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

    Google Scholar 

  • Fasano L, Roder L, Core N, Alexandre E, Vola C, Jacq B, Kerridge S (1991) The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell 64: 63–79

    Article  PubMed  CAS  Google Scholar 

  • Gallet A, Angelats C, Kerridge S, Therond PP (2000) Cubitus interruptus-independent transduction of the Hedgehog signal in Drosophila. Development 127: 5509–5522

    PubMed  CAS  Google Scholar 

  • Garcia-Bellido A, Merriam JR (1969) Cell lineage of the imaginal discs in Drosophila gynandromorphs. J Exp Zool 170: 61–75

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Crespo S, Morata G (1995) Control of Drosophila adult pattern by extradenticle. Development 121: 2117–2125

    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

    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 

  • 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

    Google Scholar 

  • Heberlein U, Wolff T, Rubin GM (1993) The TGF beta 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 

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

    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 

  • Kozmik Z, Pfeffer P, Kralova J, Paces J, Paces V, Kalousova A, Cvekl A (1999) Molecular cloning and expression of the human and mouse homologues of the Drosophila dachshund gene. Dev Genes Evol 209: 537–545

    Article  PubMed  CAS  Google Scholar 

  • Land MF, Fernald RD (1992) The evolution of eyes. Annu Rev Neurosci 15: 1–29

    Article  PubMed  CAS  Google Scholar 

  • Lebovitz RM, Ready DF (1986) Ommatidial development in Drosophila eye disc fragments. Dev Biol 117: 663–671

    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

    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

    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 

  • Mohler J, Vani K (1992) Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development 115: 957–971

    PubMed  CAS  Google Scholar 

  • Niimi T, Seimiya M, Kloter U, Flister S, Gehring WJ (1999) Direct regulatory interaction of the Eyeless protein with an eye-specific enhancer in the sine oculis gene during eye induction in Drosophila. Development 126: 2253–2260

    PubMed  CAS  Google Scholar 

  • Nusse R, Varmus HE (1992) Wnt genes. Cell 69: 1073–87

    Google Scholar 

  • Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795–801

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pai CY, Kuo TS, Jaw TJ, Kurant E, Chen CT, 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 (1998) Targeted expression of teashirt induces ectopic eyes in Drosophila. Proc Natl Acad Sci USA 95: 15508–15512

    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: 881–891

    Article  PubMed  CAS  Google Scholar 

  • Podos SD, Ferguson EL (1999) Morphogen gradients: new insights from DPP. Trends Genet 15: 396–402

    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 [see comments]. 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 

  • Seimiya M, Gehring WJ (2000) The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless independent mechanism. Development 127: 1879–1886

    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 

  • Suzuki T, Saigo K (2000) Transcriptional regulation of atonal required for Drosophila larval eye development by concerted action of eyes absent, sine oculis and Hedgehog signaling independent of Fused kinase and Cubitus interruptus. Development 127: 1531–1540

    PubMed  CAS  Google Scholar 

  • Thaker HM, Kankel DR (1992) Mosaic analysis gives an estimate of the extent of genomic involvement in the development of the visual system in Drosophila melanogaster. Genetics 131: 883–894

    PubMed  CAS  Google Scholar 

  • Toy J, Yang JM, Leppert GS, Sundin OH (1998) The Optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc Natl Acad Sci USA 95: 10643–10648

    Article  PubMed  CAS  Google Scholar 

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

    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 (1993) Pattern formation in the Drosophila retina. In: Bate M, Arias AM (ed) Cold Spring Harbor Laboratory Press, Plainview, NY, pp 1277–1326

    Google Scholar 

  • Zheng G, Blumenthal KM, Ji Y, Shardy DL, Cohen SB, Stavnezer E (1997a) High affinity dimerization by Ski involves parallel pairing of a novel bipartite alpha-helical domain. J Biol Chem 272: 31855–31864

    Article  PubMed  CAS  Google Scholar 

  • Zheng G, Teumer J, Colmenares C, Richmond C, Stavnezer E (1997b) Identification of a core functional and structural domain of the v-Ski oncoprotein responsible for both transformation and myogenesis. Oncogene 15: 459–471

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman JE, Bui QT, Liu H, Bonini NM (2000) Molecular genetic analysis of Drosophila eyes absent mutants reveals an eye enhancer element. Genetics 154: 237–246

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Program in Developmental Biology, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA

    Kartik Pappu & Graeme Mardon

  2. Departments of Pathology, Neuroscience, Molecular and Human Genetics and Ophthalmology, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA

    Graeme Mardon

Authors
  1. Kartik Pappu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graeme Mardon
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Cell Biology, Emory University School of Medicine, 1648 Pierce Drive NE, 30322-3030, Atlanta, Ga, USA

    Kevin Moses

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Pappu, K., Mardon, G. (2002). Retinal Specification and Determination in Drosophila . 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_2

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-45398-7_2

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-53640-3

  • Online ISBN: 978-3-540-45398-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation