Skip to main content
SpringerLink
Log in

Cell Fate Specification in the Drosophila Eye

  • Chapter
Drosophila Eye Development

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

Abstract

With the passing of the furrow over a uniformly equivalent group of cells, a spectacular array of cell types, each different in structure and function arises in the developing eye disc of Drosophila. A small number of ubiquitously expressed transcription factors combine with an even smaller number of signals emanating from the furrow and the developing clusters and generate cell-specific expression of a panoply of transcription factors (reviewed in Kumar and Moses 1997).The challenge is to understand how the cell-specific transcription factors are placed in their respective cells and how they then function in assigning different identities to each cell type. Here, we have presented our current understanding of this process. The aim is to be eclectic rather than comprehensive, and we apologize in advance to those investigators whose work we have not fully cited.

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

  • Baker NE, Yu SY (2001) The EGF receptor defines domains of cell cycle progression and survival to regulate cell number in the developing Drosophila eye. Cell 104: 699–708

    Article  PubMed  CAS  Google Scholar 

  • Baker NE, Zitron AE (1995) Drosophila eye development: Notch and Delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous. Mech Dev 49: 173–189

    Google Scholar 

  • Baker NE, Yu S, Han D (1996) Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr Biol 6: 1290–1301

    Article  PubMed  CAS  Google Scholar 

  • Banerjee U, Renfranz PJ, Pollock JA, Benzer S (1987) Molecular characterization and expression of sevenless, a gene involved in neuronal pattern formation in the Drosophila eye. Cell 49: 281–291

    Article  PubMed  CAS  Google Scholar 

  • Basler K, Yen D, Tomlinson A, Hafen E (1990) Reprogramming cell fate in the developing Drosophila retina: transformation of R7 cells by ectopic expression of rough. Genes Dev 4: 728–739

    Article  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 

  • Cagan RL, Ready DF (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3: 1099–1112

    Article  PubMed  CAS  Google Scholar 

  • Carthew RW, Rubin GM (1990) seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 63: 561–577

    Google Scholar 

  • Chang HC, Solomon NM, Wassarman DA, Karim FD, Therrien M, Rubin GM, Wolff T (1995) phyllopod functions in the fate determination of a subset of photoreceptors in Drosophila. Cell 80: 463–472

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Cooper MT, Bray SJ (1999) Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397: 526–530

    Article  PubMed  CAS  Google Scholar 

  • Cooper MT, Bray SJ (2000) R7 photoreceptor specification requires Notch activity. Curr Biol 10: 1507–1510

    Article  PubMed  CAS  Google Scholar 

  • Cosma MP, Tanaka T, Nasmyth K (1999) Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle-and developmentally regulated promoter. Cell 97: 299–311

    Article  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 

  • Daga A, Banerjee U (1994) Resolving the sevenless pathway using sensitized genetic backgrounds. Cell Mol Biol Res 40: 245–251

    PubMed  CAS  Google Scholar 

  • Daga A, Karlovich CA, Dumstrei K, Banerjee U (1996) Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev 10: 1194–1205

    Article  PubMed  CAS  Google Scholar 

  • De Nooij JC, Hariharan IK (1995) Uncoupling cell fate determination from patterned cell division in the Drosophila eye. Science 270: 983–985

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dickson B (1995) Nuclear factors in sevenless signalling. Trends Genet 11: 106–111

    Article  PubMed  CAS  Google Scholar 

  • Dickson BJ, Dominguez M, van der Straten A, Hafen E (1995) Control of Drosophila photoreceptor cell fates by phyllopod, a novel nuclear protein acting downstream of the Raf kinase. Cell 80: 453–462

    Article  PubMed  CAS  Google Scholar 

  • Dokucu ME, Zipursky SL, Cagan RL (1996) Atonal, rough and the resolution of proneural clusters in the developing Drosophila retina. Development 122: 4139–4147

    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 

  • Fanto M, Mlodzik M (1999) Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397: 523–526

    Article  PubMed  CAS  Google Scholar 

  • Fanto M, Mayes CA, Mlodzik M (1998) Linking cell-fate specification to planar polarity: determination of the R3/R4 photoreceptors is a prerequisite for the interpretation of the Frizzled mediated polarity signal. Mech Dev 74: 51–58

    Article  PubMed  CAS  Google Scholar 

  • Flores GV, Daga A, Kalhor HR, Banerjee U (1998) Lozenge is expressed in pluripotent precursor cells and patterns multiple cell types in the Drosophila eye through the control of cell-specific transcription factors. Development 125: 3681–3687

    PubMed  CAS  Google Scholar 

  • Flores GV, Duan H, Yan H, Nagaraj R, Fu W, Zou Y, Noll M, Banerjee U (2000) Combinatorial signaling in the specification of unique cell fates. Cell 103: 75–85

    Article  PubMed  CAS  Google Scholar 

  • Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87: 651–660

    Article  PubMed  CAS  Google Scholar 

  • Fu W, Noll M (1997) The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev 11: 2066–2078

    Article  PubMed  CAS  Google Scholar 

  • Fu W, Duan H, Frei E, Noll M (1998) shaven and sparkling are mutations in separate enhancers of the Drosophila Pax2 homolog. Development 125: 2943–2950

    Google Scholar 

  • Gaul U, Mardon G, Rubin GM (1992) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the Sevenless receptor tyrosine kinase. Cell 68: 1007–1019

    Article  PubMed  CAS  Google Scholar 

  • Gehring WJ, Ikeo K (1999) Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet 15: 371–377

    Article  PubMed  CAS  Google Scholar 

  • Gibson MC, Schubiger G (2000) Peripodial cells regulate proliferation and patterning of Drosophila imaginal discs. Cell 103: 343–350

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Hafen E, Basler K, Edstroem JE, Rubin GM (1987) Sevenless, a cell-specific homeotic gene of Drosophila, encodes a putative transmembrane receptor with a tyrosine kinase domain. Science 236: 55–63

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Harris WA, Stark WS, Walker JA (1976) Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J Physiol 256: 415–439

    PubMed  CAS  Google Scholar 

  • Hayashi T, Kojima T, Saigo K (1998) Specification of primary pigment cell and outer photoreceptor fates by BarH1 homeobox gene in the developing Drosophila eye. Dev Biol 200: 131–145

    Article  PubMed  CAS  Google Scholar 

  • Heberlein U, Treisman JE (2000) Early retinal development in Drosophila. Results Probl Cell Differ 31: 37–50

    PubMed  CAS  Google Scholar 

  • Higashijima S, Kojima T, Michiue T, Ishimaru S, Emori Y, Saigo K (1992) Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, Rl and R6, and primary pigment cells for normal eye development. Genes Dev 6: 50–60

    Article  PubMed  CAS  Google Scholar 

  • Hiromi Y, Mlodzik M, West SR, Rubin GM, Goodman CS (1993) Ectopic expression of seven-up causes cell fate changes during ommatidial assembly. Development 118: 1123–1135

    PubMed  CAS  Google Scholar 

  • Irvine KD (1999) Fringe, Notch and making developmental boundaries. Curr Opin Genet Dev 9: 434–441

    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

    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 

  • Jun S, Wallen RV, Goriely A, Kalionis B, Desplan C (1998) Lune/eye gone, a Pax-like protein, uses a partial paired domain and a homeodomain for DNA recognition Proc Natl Acad Sci USA 95: 13720–13725

    CAS  Google Scholar 

  • Kauffmann RC, Li S, Gallagher PA, Zhang J, Carthew RW (1996) Rasl signaling and transcriptional competence in the R7 cell of Drosophila. Genes Dev 10: 2167–2178

    Article  PubMed  CAS  Google Scholar 

  • Kimmel BE, Heberlein U, Rubin GM (1990) The homeo domain 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

    Article  PubMed  CAS  Google Scholar 

  • Kramer H, Cagan RL, Zipursky SL (1991) Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature 352: 207–212

    Article  PubMed  CAS  Google Scholar 

  • Kumar J, Moses K (1997) Transcription factors in eye development: a gorgeous mosaic? Genes Dev 11: 2023–2028

    Article  PubMed  CAS  Google Scholar 

  • Kumar JP, Moses K (2001) EGF receptor and Notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 104: 687–697

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Lai ZC, Rubin GM (1992) Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein Cell 70: 609–620

    CAS  Google Scholar 

  • Lai ZC, Harrison SD, Karim F, Li Y, Rubin GM (1996) Loss of tramtrack gene activity results in ectopic R7 cell formation, even in a sina mutant background. Proc Natl Acad Sci USA 93: 5025–5030

    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 

  • Miller DT, Cagan RL (1998) Local induction of patterning and programmed cell death in the developing Drosophila retina. Development 125: 2327–2335

    PubMed  CAS  Google Scholar 

  • Mlodzik M, Hiromi Y, Weber U, Goodman CS, Rubin GM (1990) The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60: 211–224

    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 

  • Pichaud F, Treisman J, Desplan C (2001) Reinventing a common strategy for patterning the eye. Cell 105: 9–12

    Article  PubMed  CAS  Google Scholar 

  • Reinke R, Zipursky SL (1988) Cell-cell interaction in the Drosophila retina: the bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development Cell 55: 321–330

    CAS  Google Scholar 

  • Rogge R, Cagan R, Majumdar A, Dulaney T, Banerjee U (1992) Neuronal development in the Drosophila retina: the sextra gene defines an inhibitory component in the developmental pathway of R7 photoreceptor cells. Proc Natl Acad Sci USA 89: 5271–5275

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Saint R, Kalionis B, Lockett TJ, Elizur A (1988) Pattern formation in the developing eye of Drosophila melanogaster is regulated by the homeo-box gene, rough. Nature 334: 151–154

    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 

  • Simon MA (1994) Signal transduction during the development of the Drosophila R7 photoreceptor. Dev Biol 166: 431–442

    Article  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 (1995) Ommatidial polarity in the Drosophila eye is determined by the direction of furrow progression and local interactions. Development 121: 4247–4256

    PubMed  CAS  Google Scholar 

  • Strutt H, Strutt D (1999) Polarity determination in the Drosophila eye. Curr Opin Genet Dev 9: 442–446

    Article  PubMed  CAS  Google Scholar 

  • Thomas BJ, Gunning DA, Cho J, Zipursky L (1994) Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of Gl. Cell 77: 1003–1014

    Article  PubMed  CAS  Google Scholar 

  • Tio M, Moses K (1997) The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development 124: 343–351

    PubMed  CAS  Google Scholar 

  • Tomlinson A, Struhl G (2001) Delta/Notch and Boss/Sevenless signals act combinatorially to specify the Drosophila R7 photoreceptor. Mol Cell 7: 487–495

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson A, Bowtell DD, Hafen E, Rubin GM (1987) Localization of the sevenless protein, a putative receptor for positional information, in the eye imaginal disc of Drosophila. Cell 51: 143–150

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson A, Kimmel BE, Rubin GM (1988) rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye. Cell 55: 771–784

    Google Scholar 

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

    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 

  • Van Vactor DL Jr, Cagan RL, Kramer H, Zipursky SL (1991) Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell. Cell 67: 1145–1155

    Article  PubMed  Google Scholar 

  • Xiong WC, Monte11 C (1993) tramtrack is a transcriptional repressor required for cell fate determination in the Drosophila eye. Genes Dev 7: 1085–1096

    Google Scholar 

  • Xu C, Kauffmann RC, Zhang J, Kladny S, Carthew RW (2000) Overlapping activators and repressors delimit transcriptional response to receptor tyrosine kinase signals in the Drosophila eye. Cell 103: 87–97

    Article  PubMed  CAS  Google Scholar 

  • Younossi-Hartenstein A, Nassif C, Green P, Hartenstein V (1996) Early neurogenesis of the Drosophila brain. J Comp Neurol 370: 313–329

    Article  PubMed  CAS  Google Scholar 

  • Zipursky SL, Rubin GM (1994) Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila. Annu Rev Neurosci 17: 373–397

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Molecular, Cell and Developmental Biology, Biological Chemistry and Human Genetics. Molecular Biology Institute, University of California, Los Angeles, California, 90095, USA

    Utpal Banerjee

Authors
  1. Raghavendra Nagaraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jude Canon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Utpal Banerjee
    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

Nagaraj, R., Canon, J., Banerjee, U. (2002). Cell Fate Specification in the Drosophila Eye. 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_6

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-45398-7_6

  • 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