Abstract
All multicellular organisms require axial patterning to transform a single-layer organ primordium to a three-dimensional organ. It involves delineation of anteroposterior (AP), dorsoventral (DV), and proximodistal (PD) axes. Any deviation in this fundamental process results in patterning and growth defects during organogenesis. The Drosophila eye is an excellent model to study axial patterning. In the Drosophila eye, DV lineage is the first axis to be determined, which is followed by generation of the AP axis. The default state of the Drosophila early eye primordium is ventral, and the dorsal fate is established by onset of expression of dorsal eye fate selector pannier (pnr)in a group of cells on the dorsal eye margin. The boundary between dorsal and ventral compartments is the site for activation of Notch (N) signaling and is referred to as the equator. Activation of N signaling is crucial for initiating the cell proliferation and differentiation in the developing Drosophila eye imaginal disc. This chapter will focus on (a) how axial patterning occurs in the developing Drosophila eye, (b) how the developing eye field gets divided into dorsal and ventral cell populations, and (c) how DV patterning genes contribute toward the growth and patterning of the fly retina.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Anderson DT (1972a) The development of hemimetabolous insects. In: Counce S, Waddington CH (eds) Developmental systems: insects. Academic Press, New York, pp 165–242
Anderson DT (1972b) The development of hemimetabolous insects. In: Counce S, Waddington CH (eds) Developmental systems: insects. Academic Press, New York, pp 96–163
Atkins M, Mardon G (2009) Signaling in the third dimension: the peripodial epithelium in eye disc development. Dev Dyn 238:2139–2148
Bach EA, Ekas LA, Ayala-Camargo A, Flaherty MS, Lee H, Perrimon N, Baeg GH (2007) GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr Patterns 7:323–331
Bachmann A, Knust E (1998) Positive and negative control of Serrate expression during early development of the Drosophila wing. Mech Dev 76:67–78
Baker NE (1988a) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol 125:96–108
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
Baker WK (1978) A clonal analysis reveals early developmental restrictions in the Drosophila head. Dev Biol 62:447–463
Baonza A, Garcia-Bellido A (2000) Notch signaling directly controls cell proliferation in the Drosophila wing disc. Proc Natl Acad Sci U S A 97:2609–2614
Becker HJ (1966) Genetic and variegation mosaics in the eye of Drosophila. Curr Top Dev Biol 1:155–171
Bellen HJ, O’Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ (1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3:1288–1300
Bessa J, Casares F (2005) Restricted teashirt expression confers eye-specific responsiveness to Dpp and Wg signals during eye specification in Drosophila. Development 132:5011–5020
Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS (2002) Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev 16:2415–2427
Bessa J, Tavares MJ, Santos J, Kikuta H, Laplante M, Becker TS, Gomez-Skarmeta JL, Casares F (2008) meis1 regulates cyclin D1 and c-myc expression, and controls the proliferation of the multipotent cells in the early developing zebrafish eye. Development 135:799–803
Bhojwani J, Singh A, Misquitta L, Mishra A, Sinha P (1995) Search for the Drosophila genes based on patterned expression of mini-white reporter gene of a P lacW vector in adult eyes. Roux’s Arch Dev Biol 205:114–121
Bier E (2005) Drosophila, the golden bug, emerges as a tool for human genetics. Nat Rev Genet 6:9–23
Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E et al (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3:1273–1287
Blair SS (2001) Cell lineage: compartments and capricious. Curr Biol 11:R1017–1021
Blair SS, Brower DL, Thomas JB, Zavortink M (1994) The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120:1805–1815
Bodentstein D (1950) The postembryonic development of Drosophila melanogaster. In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 275–367
Bosveld F, Bonnet I, Guirao B, Tlili S, Wang Z, Petitalot A, Marchand R, Bardet PL, Marcq P, Graner F et al (2012) Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 336:724–727
Boutros M, Paricio N, Strutt DI, Mlodzik M (1998) Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94:109–118
Boutros M, Mihaly J, Bouwmeester T, Mlodzik M (2000) Signaling specificity by frizzled receptors in Drosophila. Science 288:1825–1828
Brodsky MH, Steller H (1996) Positional information along the dorsal-ventral axis of the Drosophila eye: graded expression of the four-jointed gene. Dev Biol 173:428–446
Brook WJ, Cohen SM (1996) Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg. Science 273:1373–1377
Brower DL (1986) Engrailed gene expression in Drosophila imaginal discs. EMBO J 5:2649–2656
Cagan RL, Ready DF (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3:1099–1112
Calleja M, Moreno E, Pelaz S, Morata G (1996) Visualization of gene expression in living adult Drosophila. Science 274:252–255
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
Cavodeassi F, Modolell J, Campuzano S (2000) The Iroquois homeobox genes function as dorsal selectors in the Drosophila head. Development 127:1921–1929
Chang T, Mazotta J, Dumstrei K, Dumitrescu A, Hartenstein V (2001) Dpp and Hh signaling in the Drosophila embryonic eye field. Development 128:4691–4704
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
Charlton-Perkins M, Cook TA (2010) Building a fly eye: terminal differentiation events of the retina, corneal lens, and pigmented epithelia. Curr Top Dev Biol 93:129–173
Chern JJ, Choi KW (2002) Lobe mediates Notch signaling to control domain-specific growth in the Drosophila eye disc. Development 129:4005–4013
Cho KO, Choi KW (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396:272–276
Choi KW, Mozer B, Benzer S (1996) Independent determination of symmetry and polarity in the Drosophila eye. Proc Natl Acad Sci U S A 93:5737–5741
Cho KO, Chern J, Izaddoost S, Choi KW (2000) Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103:331–342
Cohen SM (1993) Imaginal disc development. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, New York
Cohen B, McGuffin ME, Pfeifle C, Segal D, Cohen SM (1992) Apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6:715–729
Cohen B, Simcox AA, Cohen SM (1993) Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117:597–608
Couso JP, Bate M, Martinez-Arias A (1993) A wingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259:484–489
Crick FH, Lawrence PA (1975) Compartments and polyclones in insect development. Science 189:340–347
Curtiss J, Halder G, Mlodzik M (2002) Selector and signalling molecules cooperate in organ patterning. Nat Cell Biol 4:E48–E51
Dahmann C, Oates AC, Brand M (2011) Boundary formation and maintenance in tissue development. Nat Rev Genet 12:43–55
Datta RR, Lurye JM, Kumar JP (2009) Restriction of ectopic eye formation by Drosophila teashirt and tiptop to the developing antenna. Dev Dyn 238:2202–2210
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 75:741–752
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
Diaz-Benjumea FJ, Cohen B, Cohen SM (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372:175–179
Dietrich W (1909) Die Facettenaugen der Dipteran. Z Wiss Zool 92:465–539
Diez del Corral R, Aroca P, JL G.m.-S., Cavodeassi F, Modolell J (1999) The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev 13:1754–1761
Dominguez M, Casares F (2005) Organ specification-growth control connection: new in-sights from the Drosophila eye-antennal disc. Dev Dyn 232:673–684
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, Brunner M, Hafen E, Basler K (1996) Sending and receiving the hedgehog signal: control by the Drosophila Gli protein Cubitus interruptus. Science 272:1621–1625
Eaton S, Kornberg TB (1990) Repression of ci-D in posterior compartments of Drosophila by engrailed. Genes Dev 4:1068–1077
Erclik T, Hartenstein V, McInnes RR, Lipshitz HD (2009) Eye evolution at high resolution: the neuron as a unit of homology. Dev Biol 332:70–79
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
Ferris GF (1950) External morphology of the adult. In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 368–419
Fleming RJ, Gu Y, Hukriede NA (1997) Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc. Development 124:2973–2981
Garcia-Bellido A, Merriam JR (1969) Cell lineage of the imaginal discs in Drosophila gynandromorphs. J Exp Zool 170:61–75
Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartmentalisation of the wing disk of Drosophila. Nat New Biol 245:251–253
Gaul U (2002) The establishment of retinal connectivity. In: Moses K (ed) Drosophila eye development. Springer, Berlin, pp. 205–216
Gehring WJ (2005) New perspectives on eye development and the evolution of eyes and photoreceptors. J Hered 96:171–184
Gibson MC, Schubiger G (2001) Drosophila peripodial cells, more than meets the eye? Bioessays 23:691–697
Glazov EA, Pheasant M, McGraw EA, Bejerano G, Mattick JS (2005) Ultraconserved elements in insect genomes: a highly conserved intronic sequence implicated in the control of homothorax mRNA splicing. Genome Res 15:800–808
Go MJ, Eastman DS, Artavanis-Tsakonas S (1998) Cell proliferation control by Notch signaling in Drosophila development. Development 125:2031–2040
Gomez-Skarmeta JL, Modolell J (1996) araucan and caupolican provide a link between compartment subdivisions and patterning of sensory organs and veins in the Drosophila wing. Genes Dev 10:2935–2945
Gomez-Skarmeta JL, Modolell J (2002) Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev 12:403–408
Gomez-Skarmeta JL, Diez del Corral R, 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
Grillenzoni N, van Helden J, Dambly-Chaudiere C, Ghysen A (1998) The iroquois complex controls the somatotopy of Drosophila notum mechanosensory projections. Development 125:3563–3569
Grossniklaus U, Pearson RK, Gehring WJ (1992) The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev 6:1030–1051
Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792
Harrison DA, McCoon PE, Binari R, Gilman M, Perrimon N (1998) Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev 12:3252–3263
Hartenstein V, Reh TA (2002) Homologies between vertebrate and invertebrate eyes. In: Moses K (ed) Drosophila eye development. Springer, Heidelberg, pp 219–251
Haynie JL, Bryant PJ (1986) Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. J Exp Zool 237:293–308
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, Borod ER, Chanut FA (1998) Dorsoventral patterning in the Drosophila retina by wingless. Development 125:567–577
Held LIJ (2002a) Cell lineage vs. intercellular signaling. In: Held LI (ed) Imaginal disc. Cambridge University Press, Cambridge, pp 1–4
Held LIJ (2002b) The eye disc. In: Held LI (ed) Imaginal disc. Cambridge University Press, Cambridge, pp 197–236
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
Hidalgo A (1998) Growth and patterning from the engrailed interface. Int J Dev Biol 42:317–324
Irvine KD (1999) Fringe, Notch, and making developmental boundaries. Curr Opin Genet Dev 9:434–441
Irvine KD, Vogt TF (1997) Dorsal-ventral signaling in limb development. Curr Opin Cell Biol 9:867–876
Irvine KD, Wieschaus E (1994) Fringe, a Boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79:595–606
Jaw TJ, You LR, Knoepfler PS, Yao LC, Pai CY, Tang CY, Chang LP, Berthelsen J, Blasi F, Kamps MP et al (2000) Direct interaction of two homeoproteins, homothorax and extradenticle, is essential for EXD nuclear localization and function. Mech Dev 91:279–291
Jordan KC, Clegg NJ, Blasi JA, Morimoto AM, Sen J, Stein D, McNeill H, Deng WM, Tworoger M, Ruohola-Baker H (2000) The homeobox gene mirror links EGF signalling to embryonic dorso-ventral axis formation through notch activation. Nat Genet 24:429–433
Ju BG, Jeong S, Bae E, Hyun S, Carroll SB, Yim J, Kim J (2000) Fringe forms a complex with Notch. Nature 405:191–195
Jurgens J, Hartenstein V (1993) The terminal regions of body pattern. In: Martinez-Arias MBaA (ed) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold-Spring Harbor, pp 687–746
Kankel DR, Ferrus A, Garen SH, Harte PJ, Lewis PE (1980) The structure and development of the nervous system. In: Ashburner M, Wright TRF (ed) The genetics and biology of Drosophila. Academic Press, New York, pp 295–368
Kehl BT, Cho KO, Choi KW (1998) Mirror, a Drosophila homeobox gene in the Iroquois complex, is required for sensory organ and alula formation. Development 125:1217–1227
Kenyon KL, Ranade SS, Curtiss J, Mlodzik M, Pignoni F (2003) Coordinating proliferation and tissue specification to promote regional identity in the Drosophila head. Dev Cell 5:403–414
Kim BJ, Fulton AB (2007) The genetics and ocular findings of Alagille syndrome. Semin Ophthalmol 22:205–210
Kim J, Irvine KD, Carroll SB (1995) Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82:795–802
Klueg KM, Muskavitch MA (1999) Ligand-receptor interactions and trans-endocytosis of Delta, Serrate and Notch: members of the Notch signalling pathway in Drosophila. J Cell Sci 112(Pt 19):3289–3297
Kornberg T, Siden I, O’Farrell P, Simon M (1985) The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40:45–53
Koshiba-Takeuchi K, Takeuchi JK, Matsumoto K, Momose T, Uno K, Hoepker V, Ogura K, Takahashi N, Nakamura H, Yasuda K et al (2000) Tbx5 and the retinotectum projection. Science 287:134–137
Kumar JP (2009) The molecular circuitry governing retinal determination. Biochim Biophys Acta 1789:306–314
Kumar JP (2011) My what big eyes you have: how the Drosophila retina grows. Dev Neurobiol 71:1133–1152
Kumar JP, Moses K (2001) EGF receptor and Notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 104:687–697
Kurant E, Pai CY, Sharf R, Halachmi N, Sun YH, Salzberg A (1998) Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS. Development 125:1037–1048
Land MF, Fernald RD (1992) The evolution of eyes. Annu Rev Neurosci 15:1–29
Langer JA, Cutrone EC, Kotenko S (2004) The Class II cytokine receptor (CRF2) family: overview and patterns of receptor-ligand interactions. Cytokine Growth Factor Rev 15:33–48
Lawrence PA, Green SM (1979) Cell lineage in the developing retina of Drosophila. Dev Biol 71:142–152
Lawrence PA, Morata G (1976) Compartments in the wing of Drosophila: a study of the engrailed gene. Dev Biol 50:321–337
Lecuit T, Brook WJ, Ng M, Calleja 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 anteroposterior and dorsoventral axes of the eye disc. Development 128:1519–1529
Lee JD, Treisman JE (2002) Regulators of the morphogenetic furrow. In: Moses K (ed) Drosophila eye development. Springer, Berlin, pp 21–29
Legent K, Treisman JE (2008) Wingless signaling in Drosophila eye development. Methods Mol Biol 469:141–161
Leyns L, Gomez-Skarmeta JL, Dambly-Chaudiere C (1996) Iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech Dev 59:63–72
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
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
Maurel-Zaffran C, Treisman JE (2000) Pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127:1007–1016
McClure KD, Schubiger G (2005) Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132:5033–5042
McLaughlin T, Hindges R, O’Leary DD (2003) Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13:57–69
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
Meinhardt H (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev Biol 96:375–385
Miall LC, Hammond AR (1892) The development of the head of the imago of chironomus. Trans Linn Soc Lond 5:265–279
Milner M, Bleasby A, Pyott A (1983) The role of the peripodial membrane in the morphogenesis of the eye antennal disc of Drosophila melanogaster. Roux’s Arch Dev Biol 192:164–170
Mlodzik M (1999) Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross-talk. EMBO J 18:6873–6879
Moloney DJ, Panin VM, Johnston SH, Chen J, Shao L, Wilson R, Wang Y, Stanley P, Irvine KD, Haltiwanger RS et al (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406:369–375
Morata G, Lawrence PA (1975) Control of compartment development by the engrailed gene in Drosophila. Nature 255:614–617
Morgan TH, Bridges CB, Strutevant AH (1925) The genetics of Drosophila. Bibliog Genet 2:1–262
Morrison CM, Halder G (2010) Characterization of a dorsal-eye Gal4 Line in Drosophila. Genesis 48:3–7
Moses K (2002) Drosophila eye development. Springer, Berlin
Moskow JJ, Bullrich F, Huebner K, Daar IO, Buchberg AM (1995) Meis1, a PBX1-related homeobox gene involved in myeloid leukemia in BXH-2 mice. Mol Cell Biol 15:5434–5443
Mui SH, Hindges R, O’Leary DD, Lemke G, Bertuzzi S (2002) The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129:797–804
Murali D, Yoshikawa S, Corrigan RR, Plas DJ, Crair MC, Oliver G, Lyons KM, Mishina Y, Furuta Y (2005) Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132:913–923
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, Nuesslein-Volhard C (2000) Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289:2137–2139
Noro B, Culi J, McKay DJ, Zhang W, Mann RS (2006) Distinct functions of homeodomain-containing and homeodomain-less isoforms encoded by homothorax. Genes Dev 20:1636–1650
Oda T, Elkahloun AG, Pike BL, Okajima K, Krantz ID, Genin A, Piccoli DA, Meltzer PS, Spinner NB, Collins FS et al (1997) Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet 16:235–242
Okajima T, Irvine KD (2002) Regulation of notch signaling by o-linked fucose. Cell 111:893–904
Oros SM, Tare M, Kango-Singh M, Singh A (2010) Dorsal eye selector pannier (pnr) suppresses the eye fate to define dorsal margin of the Drosophila eye. Dev Biol 346:258–271
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
Pan D, Rubin GM (1998) Targeted expression of teashirt induces ectopic eyes in Drosophila. Proc Natl Acad Sci U S A 95:15508–15512
Papalopulu N, Kintner C (1996) A Xenopus gene, Xbr-1, defines a novel class of homeobox genes and is expressed in the dorsal ciliary margin of the eye. Dev Biol 174:104–114
Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281:2031–2034
Penton A, Hoffmann FM (1996) Decapentaplegic restricts the domain of wingless during Drosophila limb patterning. Nature 382:162–164
Peters MA (2002) Patterning the neural retina. Curr Opin Neurobiol 12:43–48
Peters MA, Cepko CL (2002) The dorsal-ventral axis of the neural retina is divided into multiple domains of restricted gene expression which exhibit features of lineage compartments. Dev Biol 251:59–73
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
Poeck B, Hofbauer A, Pflugfelder GO (1993) Expression of the Drosophila optomotor-blind gene transcript in neuronal and glial cells of the developing nervous system. Development 117:1017–1029
Porsch M, Sauer M, Schulze S, Bahlo A, Roth M, Pflugfelder GO (2005) The relative role of the T-domain and flanking sequences for developmental control and transcriptional regulation in protein chimeras of Drosophila OMB and ORG-1. Mech Dev 122:81–96
Poulson DF (1950). Histogenesis, oogenesis, and differentiation in the embryo of Drosophila melanogaster meigen. In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 168–274
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
Raftery LA, Sanicola M, Blackman RK, Gelbart WM (1991) The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary? Development 113:27–33
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
Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240
Reifegerste R, Moses K (1999) Genetics of epithelial polarity and pattern in the Drosophila retina. Bioessays 21:275–285
Reynolds-Kenneally J, Mlodzik M (2005) Notch signaling controls proliferation through cell-autonomous and non-autonomous mechanisms in the Drosophila eye. Dev Biol 285:38–48
Rieckhof GE, Casares F, Ryoo HD, Abu-Shaar M, Mann RS (1997) Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 91:171–183
Roignant JY, Treisman JE (2009) Pattern formation in the Drosophila eye disc. Int J Dev Biol 53:795–804
Roignant JY, Legent K, Janody F, Treisman JE (2010) The transcriptional co-factor Chip acts with LIM-homeodomain proteins to set the boundary of the eye field in Drosophila. Development 137:273–281
Ryoo HD, Marty T, Casares F, Affolter M, Mann RS (1999) Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 126:5137–5148
Sanes JR, Zipursky SL (2010) Design principles of insect and vertebrate visual systems. Neuron 66:15–36
Sanicola M, Sekelsky J, Elson S, Gelbart WM (1995) Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed. Genetics 139:745–756
Sato A, Tomlinson A (2007) Dorsal-ventral midline signaling in the developing Drosophila eye. Development 134:659–667
Simon MA (2004) Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression. Development 131:6175–6184
Singh A, Choi KW (2003) Initial state of the Drosophila eye before dorsoventral specification is equivalent to ventral. Development 130:6351–6360
Singh A, Irvine KD (2012) Drosophila as a model for understanding development and disease. Dev Dyn 241:1–2
Singh J, Mlodzik M (2012) Planar cell polarity signaling: coordination of cellular orientation across tissues. Wiley Interdiscip Rev Dev Biol 1:479–499
Singh A, Kango-Singh M, Sun YH (2002) Eye suppression, a novel function of teashirt, requires wingless signaling. Development 129:4271–4280
Singh A, Kango-Singh M, Choi KW, Sun YH (2004) Dorso-ventral asymmetric functions of teashirt in Drosophila eye development depend on spatial cues provided by early DV patterning genes. Mech Dev 121:365–370
Singh A, Chan J, Chern JJ, Choi KW (2005a) Genetic interaction of Lobe with its modifiers in dorsoventral patterning and growth of the Drosophila eye. Genetics 171:169–183
Singh A, Lim J, Choi K-W (2005b). Dorso-ventral boundary is required for organizing growth and planar polarity in the Drosophila eye. In: Mlodzik M (ed) Planar cell polarization during development: advances in developmental biology and biochemistry. Elsevier Science & Technology Books, San Diego, pp 59–91
Singh A, Shi X, Choi KW (2006) Lobe and Serrate are required for cell survival during early eye development in Drosophila. Development 133:4771–4781
Singh A, Tare M, Kango-Singh M, Son WS, Cho KO, Choi KW (2011) Opposing interactions between homothorax and Lobe define the ventral eye margin of Drosophila eye. Dev Biol 359:199–208
Singh A, Tare M, Puli OR, Kango-Singh M (2012) A glimpse into dorso-ventral patterning of the Drosophila eye. Dev Dyn 241:69–84
Speicher SA, Thomas U, Hinz U, Knust E (1994) The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginal discs: control of cell proliferation. Development 120:535–544
Stevens KE, Mann RS (2007) A balance between two nuclear localization sequences and a nuclear export sequence governs extradenticle subcellular localization. Genetics 175:1625–1636
Struhl G (1981) A blastoderm fate map of compartments and segments of the Drosophila head. Dev Biol 84:386–396
Sun X, Artavanis-Tsakonas S (1996) The intracellular deletions of Delta and Serrate define dominant negative forms of the Drosophila Notch ligands. Development 122:2465–2474
Sun YH, Tsai CJ, Green MM, Chao JL, Yu CT, Jaw TJ, Yeh JY, Bolshakov VN (1995) White as a reporter gene to detect transcriptional silencers specifying position-specific gene expression during Drosophila melanogaster eye development. Genetics 141:1075–1086
Tang CY, Sun YH (2002) Use of mini-white as a reporter gene to screen for GAL4 insertions with spatially restricted expression pattern in the developing eye in drosophila. Genesis 34:39–45
Tare M, Puli OR, Moran MT, Kango-Singh M, Singh A (2013) Domain specific genetic mosaic system in the Drosophila eye. Genesis 51:68–74
Theisen H, Haerry TE, O’Connor MB, Marsh JL (1996) Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122:3939–3948
Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519–3527
Tsachaki M, Sprecher SG (2012) Genetic and developmental mechanisms underlying the formation of the Drosophila compound eye. Dev Dyn 241:40–56
Tsai YC, Sun YH (2004) Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 39:141–153
Tsai YC, Yao JG, Chen PH, Posakony JW, Barolo S, Kim J, Sun YH (2007) Upd/Jak/STAT signaling represses wg transcription to allow initiation of morphogenetic furrow in Drosophila eye development. Dev Biol 306:760–771
Urbach R, Technau GM (2003) Segment polarity and DV patterning gene expression reveals segmental organization of the Drosophila brain. Development 130:3607–3620
Wang YH, Huang ML (2009) Reduction of Lobe leads to TORC1 hypoactivation that induces ectopic Jak/STAT signaling to impair Drosophila eye development. Mech Dev 126:781–790
Wawersik S, Maas RL (2000) Vertebrate eye development as modeled in Drosophila. Hum Mol Genet 9:917–925
Wehrli M, Tomlinson A (1998) Independent regulation of anterior/posterior and equatorial/polar polarity in the Drosophila eye; evidence for the involvement of Wnt signaling in the equatorial/polar axis. Development 125:1421–1432
Wilkins AS (1993) Genetic analysis of animal development, 2nd edn. Wiley-Liss., New York
Willecke M, Hamaratoglu F, Sansores-Garcia L, Tao C, Halder G (2008) Boundaries of Dachsous Cadherin activity modulate the Hippo signaling pathway to induce cell proliferation. Proc Natl Acad Sci U S A 105:14897–14902
Wilson C, Pearson RK, Bellen HJ, O’Kane CJ, Grossniklaus U, Gehring WJ (1989) P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev 3:1301–1313
Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: Bate M, Arias AM (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, New York, pp 1277–1325
Xue Y, Gao X, Lindsell CE, Norton CR, Chang B, Hicks C, Gendron-Maguire M, Rand EB, Weinmaster G, Gridley T (1999) Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum Mol Genet 8:723–730
Yamamoto D (1996). Architecture of the adult compound eye and the developing eye disks. In: Yamamoto D (ed) Molecular dynamics in the developing drosophila eye. Chapman and Hall, Austin, p 169
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
Younossi-Hartenstein A, Hartenstein V (1993) The role of the tracheae and musculature during pathfinding of Drosophila embryonic sensory axons. Dev Biol 158:430–447
Zecca M, Basler K, Struhl G (1995) Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121:2265–2278
Zecca M, Basler K, Struhl G (1996) Direct and long-range action of a wingless morphogen gradient. Cell 87:833–844
Zeidler MP, Perrimon N, Strutt DI (1999a) The four-jointed gene is required in the Drosophila eye for ommatidial polarity specification. Curr Biol 9:1363–1372
Zeidler MP, Perrimon N, Strutt DI (1999b) Polarity determination in the Drosophila eye: a novel role for unpaired and JAK/STAT signaling. Genes Dev 13:1342–1353
Zirin JD, Mann RS (2007) Nubbin and Teashirt mark barriers to clonal growth along the proximal-distal axis of the Drosophila wing. Dev Biol 304:745–758
Acknowledgements
The authors thank Erika Wittkorn, Timothy Cutler, and Aditi Singh for their help and comments on the manuscript. We apologize to all authors whose work could not be cited due to space limitations. AS is supported by a NIH grant (1R15 HD064557–01), start-up support from the University of Dayton.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Tare, M., Roy Puli, O., Singh, A. (2013). Molecular Genetic Mechanisms of Axial Patterning: Mechanistic Insights into Generation of Axes in the Developing Eye. In: Singh, A., Kango-Singh, M. (eds) Molecular Genetics of Axial Patterning, Growth and Disease in the Drosophila Eye. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8232-1_2
Download citation
DOI: https://doi.org/10.1007/978-1-4614-8232-1_2
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-8231-4
Online ISBN: 978-1-4614-8232-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)