Ghost in the Machine: The Peripodial Epithelium

  • Brandon P. Weasner
  • Bonnie M. Weasner
  • Justin P. KumarEmail author


A fundamental feature of early animal development is that fate specification and the morphogenesis of one tissue is often induced by signals emanating from a neighboring population of cells. H. Spemann and H. Mangold introduced this concept when they showed that a transplanted blastopore lip of an early gastrulating newt could induce the formation of a full axis after it was transplanted into a second newt species. C.H. Waddington later demonstrated that the process of induction is not restricted to amphibians but rather is a general mechanism that applies broadly to many different organisms including mammals. Extirpation and transplantation studies of the vertebrate eye and lens indicate that these two tissues influence aspects of each other’s development. Likewise, several studies have shown that the development of the developing eye field in Drosophila is influenced by an overlying tissue called the peripodial epithelium. While the vertebrate lens and the peripodial epithelium of the Drosophila eye-antennal disc are non-homologous structures, these two tissues use common elements such as the Pax6 transcription factor and the TGFβ/BMP4 signaling pathway to influence the growth, specification, and patterning of the adjacent retinas. In this chapter, we will describe what is known about the role that the peripodial epithelium plays in the development of the eye-antennal disc of Drosophila.


Drosophila Eye-antennal disc Peripodial epithelium Retina 



We first thank every researcher that has worked on the peripodial epithelia of imaginal discs over the last century—Peter Bryant, John Haynie, Martin Milner, and Gerold Schubiger deserve special mention. We would also like to thank Alison Ordway and Alison Smith for their comments on an earlier draft of this chapter. This work is supported by a grant from the National Eye Institute (R01 EY014863) and funds from the Department of Biology, the College of Arts and Sciences, and the Office of the Vice Provost for Research at Indiana University to Justin P. Kumar.


  1. Abzhanov A, Holtzman S, Kaufman TC (2001) The Drosophila proboscis is specified by two Hox genes, proboscipedia and Sex combs reduced, via repression of leg and antennal appendage genes. Development 128:2803–2814PubMedGoogle Scholar
  2. Adler PN, MacQueen M (1984) Cell proliferation and DNA replication in the imaginal wing disc of Drosophila melanogaster. Dev Biol 103:28–37PubMedGoogle Scholar
  3. Agnes F, Suzanne M, Noselli S (1999) The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126:5453–5462PubMedGoogle Scholar
  4. Amore G, Casares F (2010) Size matters: the contribution of cell proliferation to the progression of the specification Drosophila eye gene regulatory network. Dev Biol 344:569–577PubMedGoogle Scholar
  5. Atkins M, Mardon G (2009) Signaling in the third dimension: the peripodial epithelium in eye disc development. Dev Dyn 238:2139–2148PubMedPubMedCentralGoogle Scholar
  6. Auerbach C (1936). The development of the legs, wings, and halteres in wild type and some mutant strains of Drosophila melanogaster. Trans R Soc Edin LVIII, Part III, No 27Google Scholar
  7. Baena-Lopez LA, Pastor-Pareja JC, Resino J (2003) Wg and Egfr signalling antagonise the development of the peripodial epithelium in Drosophila wing discs. Development 130:6497–6506PubMedGoogle Scholar
  8. Baker LR, Weasner BM, Nagel A, Neuman SD, Bashirullah A, Kumar JP (2018) Eyeless/Pax6 initiates eye formation non-autonomously from the peripodial epithelium. Development 145(15):dev163329PubMedPubMedCentralGoogle Scholar
  9. Baker NE (1988) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev Biol 125:96–108PubMedGoogle Scholar
  10. Baker WK (1978) A fine-structure gynandromorph fate map of the Drosophila head. Genetics 88:743–754PubMedPubMedCentralGoogle Scholar
  11. Beadle GW, Ephrussi B (1935) Transplantation in Drosophila. Proc Natl Acad Sci USA 21:642–646PubMedGoogle Scholar
  12. Beadle GW, Ephrussi B (1936a) Development of eye colors in Drosophila: transplantation experiments with suppressor of vermilion. Proc Natl Acad Sci USA 22:536–540PubMedGoogle Scholar
  13. Beadle GW, Ephrussi B (1936b) The differentiation of eye pigments in Drosophila as studied by transplantation. Genetics 21:225–247PubMedPubMedCentralGoogle Scholar
  14. Beadle GW, Ephrussi B (1937) Development of eye colors in Drosophila: diffusible substances and their interrelations. Genetics 22:76–86PubMedPubMedCentralGoogle Scholar
  15. Becker HJ (1957) Uber Rontgenmossaikflecken und Defektmutationen am Auge von Drosophila und die Entwicklungsphysiologie des Auges. Z Induk Abst Vererb Lehre 88:333–373Google Scholar
  16. Bessa J, Casares F (2005) Restricted teashirt expression confers eye-specific responsiveness to Dpp and Wg signals during eye specification in Drosophila. Development 132:5011–5020PubMedGoogle Scholar
  17. Birmingham L (1942) Boundaries of differentiation of cephalic imaginal discs in Drosophila. J Exp Zool 91:345–363Google Scholar
  18. Blackman RK, Sanicola M, Raftery LA, Gillevet T, Gelbart WM (1991) An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-b family in Drosophila. Development 111:657–665PubMedGoogle Scholar
  19. Bras-Pereira C, Bessa J, Casares F (2006) Odd-skipped genes specify the signaling center that triggers retinogenesis in Drosophila. Development 133:4145–4149PubMedGoogle Scholar
  20. Bryant PJ (1975) Pattern formation int he imaginal wing discof Drosophila melanogaster: fate map, regeneration and duplication. J Exp Zool 193:49–78PubMedGoogle Scholar
  21. Chadwick R, Jones B, Jack T, McGinnis W (1990) Ectopic expression from the Deformed gene triggers a dominant defect in Drosophila adult head development. Dev Biol 141:130–140PubMedGoogle Scholar
  22. Chanut F, Heberlein U (1997) Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124:559–567PubMedGoogle Scholar
  23. Chao JL, Tsai YC, Chiu SJ, Sun YH (2004) Localized Notch signal acts through eyg and upd to promote global growth in Drosophila eye. Development 131:3839–3847PubMedGoogle Scholar
  24. Chen TY (1929) On the development of imaginal buds in normal and mutant Drosophila melanogaster. J Morph 47:135–199Google Scholar
  25. Cho KO, Chern J, Izaddoost S, Choi KW (2000) Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103:331–342PubMedGoogle Scholar
  26. Chouinard S, Kaufman TC (1991) Control of expression of the homeotic labial (lab) locus of Drosophila melanogaster: evidence for both positive and negative autogenous regulation. Development 113:1267–1280PubMedGoogle Scholar
  27. Crampton GC (1942) The external morphology of the Diptera, Vol 47 (State Geological and Natural History Survey of Connecticut: State of Connecticut Public Document)Google Scholar
  28. Curtiss J, Mlodzik M (2000) Morphogenetic furrow initiation and progression during eye development in Drosophila: the roles of decapentaplegic, hedgehog and eyes absent. Development 127:1325–1336PubMedGoogle Scholar
  29. Deak I (1980) A model linking segmentation, compartmentalization and regeneration in Drosophila development. J Theor Biol 84:477–504PubMedGoogle Scholar
  30. Diaz-Benjumea FJ, Cohen B, Cohen SM (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372:175–179PubMedGoogle Scholar
  31. Diederich RJ, Pattatucci AM, Kaufman TC (1991) Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head. Development 113:273–281PubMedGoogle Scholar
  32. Dominguez M, Casares F (2005) Organ specification-growth control connection: new in-sights from the Drosophila eye-antennal disc. Dev Dyn 232:673–684PubMedGoogle Scholar
  33. Dominguez M, Hafen E (1997) Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev 11:3254–3264PubMedPubMedCentralGoogle Scholar
  34. Eassa YE (1953) The development of imaginal buds in the head of Pieris brassicae Linn. (Lepidoptera). Trans R Entomol Soc Lond 104:39–51Google Scholar
  35. Ekas LA, Baeg GH, Flaherty MS, Ayala-Camargo A, Bach EA (2006) JAK/STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development 133:4721–4729PubMedGoogle Scholar
  36. Ephrussi B, Beadle GW (1937a) Development of eye colors in Drosophila: production and release of cn substance by the eyes of different eye color mutants. Genetics 22:479–483PubMedPubMedCentralGoogle Scholar
  37. Ephrussi B, Beadle GW (1937b) Development of eye colors in Drosophila: transplantation experiments on the interaction of vermilion with other eye colors. Genetics 22:65–75PubMedPubMedCentralGoogle Scholar
  38. Ferris GF (1950) External morphoogy of the adult. In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 368–419Google Scholar
  39. Firth LC, Baker NE (2007) Spitz from the retina regulates genes transcribed in the second mitotic wave, peripodial epithelium, glia and plasmatocytes of the Drosophila eye imaginal disc. Dev Biol 307:521–538PubMedPubMedCentralGoogle Scholar
  40. Fristrom D, Frstrom JW (1993) The metamorphic development of the adult epidermis. In: Bate M, Martinez Arias A (eds) The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 467–516Google Scholar
  41. Gibson MC, Lehman DA, Schubiger G (2002) Lumenal transmission of decapentaplegic in Drosophila imaginal discs. Dev Cell 3:451–460PubMedGoogle Scholar
  42. Gibson MC, Schubiger G (1999) Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs. Development 126:1591–1599PubMedGoogle Scholar
  43. Gibson MC, Schubiger G (2000) Peripodial cells regulate proliferation and patterning of Drosophila imaginal discs. Cell 103:343–350PubMedGoogle Scholar
  44. Gutierrez-Avino FJ, Ferres-Marco D, Dominguez M (2009) The position and function of the Notch-mediated eye growth organizer: the roles of JAK/STAT and four-jointed. EMBO Rep 10:1051–1058PubMedPubMedCentralGoogle Scholar
  45. Hadorn E (1968) Transdetermination in cells. Sci Amer 219:110–172PubMedGoogle Scholar
  46. Hadorn E (1978) Transdetermination. In: Ashburner M, Wright (eds) The genetics and biology of Drosphila, vol 2c. Academic Press, New York, pp 555–617Google Scholar
  47. Halder G, Callaerts P, Flister S, Walldorf U, Kloter U, Gegring WJ (1998) Eyeless initiates the expression of both sine oculis and eyes absent during drosophila compound eye development. Development 125:2181–2191PubMedGoogle Scholar
  48. Hallsson JH, Haflidadottir BS, Stivers C, Odenwald W, Arnheiter H, Pignoni F, Steingrimsson E (2004) The basic helix-loop-helix leucine zipper transcription factor Mitf is conserved in Drosophila and functions in eye development. Genetics 167:233–241PubMedPubMedCentralGoogle Scholar
  49. Haynie JL, Bryant PJ (1986) Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. J Exp Zool 237:293–308PubMedGoogle Scholar
  50. 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 125:3741–3751PubMedGoogle Scholar
  51. Heberlein U, Borod ER, Chanut FA (1998) Dorsoventral patterning in the Drosophila retina by wingless. Development 125:567–577PubMedGoogle Scholar
  52. 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 75:913–926PubMedGoogle Scholar
  53. Hursh DA, Stultz BG, Park SY (2016) Jun N-terminal kinase signaling makes a face. Fly 10:195–203PubMedPubMedCentralGoogle Scholar
  54. Jorgensen EM, Garber RL (1987) Function and misfunction of the two promoters of the Drosophila Antennapedia gene. Genes Dev 1:544–555PubMedGoogle Scholar
  55. Jurgens J, Hartenstein V (1993) The terminal regions of the body pattern. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 687–746Google Scholar
  56. Kooh PJ, Fehon RG, Muskavitch MA (1993) Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117:493–507PubMedGoogle Scholar
  57. Kumar JP (2010) Retinal determination the beginning of eye development. Curr Top Dev Biol 93:1–28PubMedPubMedCentralGoogle Scholar
  58. Kumar JP (2011) My what big eyes you have: how the Drosophila retina grows. Dev Neurobiol 71:1133–1152PubMedPubMedCentralGoogle Scholar
  59. Kumar JP (2013) Catching the next wave: patterning of the Drosophila eye by the morphogentic furrow. In: Singh A (ed) Molecular genetics of axial patterning, growth, and disease in the Drosophila eye. Springer, New York, pp 75–97Google Scholar
  60. Kumar K, Ouweneel WJ, Faber J (1979) Differentiation capacities of the labial imaginal disc of Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 186:51–64Google Scholar
  61. Kumar SR, Patel H, Tomlinson A (2015) Wingless mediated apoptosis: How cone cells direct the death of peripheral ommatidia in the developing Drosophila eye. Dev Biol 407:183–194PubMedPubMedCentralGoogle Scholar
  62. Lee H, Stultz BG, Hursh DA (2007) The Zic family member, odd-paired, regulates the Drosophila BMP, decapentaplegic, during adult head development. Development 134:1301–1310PubMedGoogle Scholar
  63. Legent K, Treisman JE (2008) Wingless signaling in Drosophila eye development. Methods Mol Biol 469:141–161PubMedPubMedCentralGoogle Scholar
  64. Lim HY, Tomlinson A (2006) Organization of the peripheral fly eye: the roles of Snail family transcription factors in peripheral retinal apoptosis. Development 133:3529–3537PubMedGoogle Scholar
  65. Lim J, Choi KW (2004) Drosophila eye disc margin is a center for organizing long-range planar polarity. Genesis 39:26–37PubMedGoogle Scholar
  66. 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 121:2279–2289PubMedGoogle Scholar
  67. 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 75:927–938PubMedGoogle Scholar
  68. Madhaven MM, Schneiderman HA (1977) Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development of Drosophila melanogaster. Wilhelm Roux Arch Dev Biol 183:269–305Google Scholar
  69. Manseau L, Baradaran A, Brower D, Budhu A, Elefant F, Phan H, Philp AV, Yang M, Glover D, Kaiser K et al (1997) GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 209:310–322PubMedGoogle Scholar
  70. Mardon G, Solomon NM, Rubin GM (1994) Dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120:3473–3486PubMedGoogle Scholar
  71. Martinez-Arias A, Ingham PW, Scott MP, Akam ME (1987) The spatial and temporal deployment of Dfd and Scr transcripts throughout development of Drosophila. Development 100:673–683PubMedGoogle Scholar
  72. 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 4:2011–2023PubMedGoogle Scholar
  73. Mathi SK, Larsen E (1988) Patterns of cell division in imaginal discs of Drosophila. Tissue Cell 20:461–472PubMedGoogle Scholar
  74. Maurel-Zaffran C, Treisman JE (2000) Pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127:1007–1016PubMedGoogle Scholar
  75. McClure KD, Schubiger G (2005) Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132:5033–5042PubMedGoogle Scholar
  76. Merrill VK, Diederich RJ, Turner FR, Kaufman TC (1989) A genetic and developmental analysis of mutations in labial, a gene necessary for proper head formation in Drosophila melanogaster. Dev Biol 135:376–391PubMedGoogle Scholar
  77. Merrill VK, Turner FR, Kaufman TC (1987) A genetic and developmental analysis of mutations in the Deformed locus in Drosophila melanogaster. Dev Biol 122:379–395PubMedGoogle Scholar
  78. Milner MJ (1977) The eversion and differentiation of Drosophila melanogaster leg and wing imaginal discs cultured in vitro with an optimal concentration of beta-ecdysone. J Embryol Exp Morphol 37:105–117PubMedGoogle Scholar
  79. Milner MJ, Bleasby AJ, Kelly SL (1984a) The role of the peripodial membrane of leg and wing imaginal discs of Drosophila melanogaster during evagination and differentiation in vitro. Wilhelm Roux’s Arch Dev Biol 193:180–186Google Scholar
  80. Milner MJ, Bleasby AJ, Pyott A (1983) The role of the peripodial membrane in the morphogenesis fo the eye-antennal disc of Drosophila melanogaster. Wilhelm Rouxs Arch Dev Biol 192:164–170Google Scholar
  81. Milner MJ, Bleasby AJ, Pyott A (1984b) Cell interactions during the fusionin vitro of Drosophila eye-antennal imaginal discs. Wilhelm Roux’s Arch Dev Biol 193:406–413Google Scholar
  82. Milner MJ, Haynie JL (1979) Fusion of Drosophila eye-antennal imaginal discs during differentiation in vitro. Wilhelm Roux’s Arch Dev Biol 185:363–370Google Scholar
  83. Morata G, Lawrence PA (1979) Development of the eye-antenna imaginal disc of Drosophila. Dev Biol 70:355–371PubMedGoogle Scholar
  84. Nardi JB, Norby SW, Magee-Adams SM (1987) Cellular events within peripodial epithelia that accompany evagination of Manduca wing discs: conversion of cuboidal epithelia to columnar epithelia. Dev Biol 119:20–26Google Scholar
  85. Nusinow D, Greenberg L, Hatini V (2008) Reciprocal roles for bowl and lines in specifying the peripodial epithelium and the disc proper of the Drosophila wing primordium. Development 135:3031–3041PubMedPubMedCentralGoogle Scholar
  86. 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 346:258–271PubMedPubMedCentralGoogle Scholar
  87. Ouweneel WJ (1970) Normal and abnormal determination in the imaginal discs of Drosophila, with special reference to the eye discs. Acta Embryol Exp 1:95–119Google Scholar
  88. Pallavi SK, Shashidhara LS (2003) Egfr/Ras pathway mediates interactions between peripodial and disc proper cells in Drosophila wing discs. Development 130:4931–4941PubMedGoogle Scholar
  89. Pallavi SK, Shashidhara LS (2005) Signaling interactions between squamous and columnar epithelia of the Drosophila wing disc. J Cell Sci 118:3363–3370PubMedGoogle Scholar
  90. Park SY, Stultz BG, Hursh DA (2015) Dual role of Jun N-terminal kinase activity in bone morphogenetic protein-mediated Drosophila ventral head development. Genetics 201:1411–1426PubMedPubMedCentralGoogle Scholar
  91. Pastor-Pareja JC, Grawe F, Martin-Blanco E, Garcia-Bellido A (2004) Invasive cell behavior during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev Cell 7:387–399PubMedGoogle Scholar
  92. Pauli T, Seimiya M, Blanco J, Gehring WJ (2005) Identification of functional sine oculis motifs in the autoregulatory element of its own gene, in the eyeless enhancer and in the signalling gene hedgehog. Development 132:2771–2782PubMedGoogle Scholar
  93. Pereira PS, Pinho S, Johnson K, Couso JP, Casares F (2006) A 3′ cis-regulatory region controls wingless expression in the Drosophila eye and leg primordia. Dev Dyn 235:225–234PubMedGoogle Scholar
  94. 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 91:881–891PubMedGoogle Scholar
  95. Pilkington RW (1942) Facet mutants of Drosophila. Proc Zool Soc Lond Ser A 3:199–222Google Scholar
  96. Poodry CA, Schneiderman HA (1970) The ultrastructure of the developing leg of Drosophila melanogaster. Wilhelm Roux’ Archiv fur Entwicklungsmechanik der Organismen 166:1–44PubMedGoogle Scholar
  97. Ramirez-Weber FA, Kornberg TB (1999) Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97:599–607PubMedGoogle Scholar
  98. Ramirez-Weber FA, Kornberg TB (2000) Signaling reaches to new dimensions in Drosophila imaginal discs. Cell 103:189–192PubMedGoogle Scholar
  99. Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240PubMedGoogle Scholar
  100. Reinhardt CA, Hodgkin NM, Bryant PJ (1977) Wound healing in the imaginal discs of Drosophila. I. Scanning electron microscopy of normal and healing wing discs. Dev Biol 60:238–257PubMedGoogle Scholar
  101. Richard M, Bauer R, Tavosanis G, Hoch M (2017) The gap junction protein Innexin3 is required for eye disc growth in Drosophila. Dev Biol 425:191–207PubMedGoogle Scholar
  102. Richard M, Hoch M (2015) Drosophila eye size is determined by Innexin 2-dependent Decapentaplegic signalling. Dev Biol 408:26–40PubMedGoogle Scholar
  103. Roy S, Hsiung F, Kornberg TB (2011) Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332:354–358PubMedPubMedCentralGoogle Scholar
  104. Royet J, Finkelstein R (1996) Hedgehog, wingless and othrodenticle specify adult head development in Drosophila. Development 122:1849–1858PubMedGoogle Scholar
  105. Royet J, Finkelstein R (1997) Establishing primordia in the Drosophila eye-antennal imaginal disc: the role of decapentaplegic, wingless and hedgehog. Development 124:4793–4800PubMedGoogle Scholar
  106. Segal D, Gelbart WM (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109:119–143PubMedPubMedCentralGoogle Scholar
  107. Sen A, Stultz BG, Lee H, Hursh DA (2010) Odd paired transcriptional activation of decapentaplegic in the Drosophila eye/antennal disc is cell autonomous but indirect. Dev Biol 343:167–177PubMedGoogle Scholar
  108. Silver SJ, Rebay I (2005) Signaling circuitries in development: insights from the retinal determination gene network. Development 132:3–13PubMedGoogle Scholar
  109. Singh A, Tare M, Puli OR, Kango-Singh M (2012) A glimpse into dorso-ventral patterning of the Drosophila eye. Dev Dyn 241:69–84PubMedGoogle Scholar
  110. Singh J, Mlodzik M (2012) Planar cell polarity signaling: coordination of cellular orientation across tissues. Wiley Interdiscip Rev Dev Biol 1:479–499PubMedPubMedCentralGoogle Scholar
  111. Snodgrass RE (1935) The principles of insect morphology. McGraw-Hill, New YorkGoogle Scholar
  112. Spencer FA, Hoffmann FM, Gelbart WM (1982) Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28:451–461PubMedGoogle Scholar
  113. Sprey TE, Oldenhave M (1974) A detailed organ map of the wing disk of Calliphora erythrocephala. Neth J Zool 24:291–310Google Scholar
  114. Struhl G (1981) A blastoderm fate map of compartments and segments of the Drosophila head. Dev Biol 84:386–396PubMedGoogle Scholar
  115. Stultz BG, Lee H, Ramon K, Hursh DA (2006) Decapentaplegic head capsule mutations disrupt novel peripodial expression controlling the morphogenesis of the Drosophila ventral head. Dev Biol 296:329–339PubMedGoogle Scholar
  116. Stultz BG, Park SY, Mortin MA, Kennison JA, Hursh DA (2012) Hox proteins coordinate peripodial decapentaplegic expression to direct adult head morphogenesis in Drosophila. Dev Biol 369:362–376PubMedPubMedCentralGoogle Scholar
  117. Stultz BG, Ray RP, Hursh DA (2005) Analysis of the shortvein cis-regulatory region of the decapentaplegic gene of Drosophila melanogaster. Genesis 42:181–192PubMedGoogle Scholar
  118. Sturtevant AH (1929) The claret mutant type of Drosophila simulans: a study of chromosome elimination and cell lineage. Z Wiss Zool Abt A 135:323–356Google Scholar
  119. Theisen H, Haerry TE, O'Connor MB, Marsh JL (1996) Developmental territories created by mutual antagonism between Wingless and Decapentaplegic. Development 122:3939–3948PubMedGoogle Scholar
  120. Tomlinson A (2003) Patterning the peripheral retina of the fly: decoding a gradient. Dev Cell 5:799–809PubMedGoogle Scholar
  121. Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519–3527PubMedGoogle Scholar
  122. Tsai YC, Sun YH (2004) Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 39:141–153PubMedGoogle Scholar
  123. 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 306:760–771PubMedGoogle Scholar
  124. Usui K, Simpson P (2000) Cellular basis of the dynamic behavior of the imaginal thoracic discs during Drosophila metamorphosis. Dev Biol 225:13–25PubMedGoogle Scholar
  125. Voas MG, Rebay I (2004) Signal integration during development: Insights from the Drosophila eye. Dev Dyn 229:162–175PubMedGoogle Scholar
  126. Vogt M (1946) Zur labilen Determination der Imagin-alscheiben von Drosophila. I. Verhalten verschieden-altriger Imaginalanlagen bei operativer Defektsetzung. Biol Zbl 65:223–238Google Scholar
  127. Waddington CH (1941) The genetic control of wing development in Drosophila. J Genet 41:75–139Google Scholar
  128. Wieschaus E, Gehring W (1976) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol 50:249–263PubMedGoogle Scholar
  129. Wirz J, Fessler LI, Gehring WJ (1986) Localization of the Antennapedia protein in Drosophila embryos and imaginal discs. EMBO J 5:3327–3334PubMedPubMedCentralGoogle Scholar
  130. Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 1277–1326Google Scholar
  131. Younossi-Hartenstein A, Tepass U, Hartenstein V (1993) Embryonic origin of the imaginal discs of the head of Drosophila melanogaster. Roux’s Arch Dev Biol 203:60–73Google Scholar
  132. Zeitlinger J, Bohmann D (1999) Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126:3947–3956PubMedGoogle Scholar
  133. Zhang T, Zhou Q, Pignoni F (2011) Yki/YAP, Sd/TEAD and Hth/MEIS control tissue specification in the Drosophila eye disc epithelium. PLoS One 6:e22278PubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Brandon P. Weasner
    • 1
  • Bonnie M. Weasner
    • 1
  • Justin P. Kumar
    • 1
    Email author
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA

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