Roux's archives of developmental biology

, Volume 205, Issue 1–2, pp 31–44 | Cite as

Analysis of neural elements in head-mutant Drosophila embryos suggests segmental origin of the optic lobes

  • Urs Schmidt-Ott
  • Marcos González-Gaitán
  • Gerhard M. Technau
Original Article


We describe the development of 20 sensory organs in the embryonic Drosophila head, which give rise to 7 sensory nerves of the peripheral nervous system (PNS), and 4 ganglia of the stomatogastric nervous system (SNS). Using these neural elements and the optic lobes as well as expression domains of the segment polarity gene engrailed in the wild-type head of Drosophila embryos as markers we examined the phenotype of different mutants which lack various and distinct portions of the embryonic head. In the mutants, distinct neural elements and engrailed expression domains, serving as segmental markers, are deleted. These mutants also affect the optic lobes to various degrees. Our results suggest that the optic lobes are of segmental origin and that they derive from the ocular segment anteriorly adjacent to the antennal segment of the developing head.

Key words

Drosophila Head development Segmentation mutants Nervous system Optic lobe 


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  1. Baker NE (1988) Localization of transcripts from the wingless gene in whole Drosophila embryos. Development 103:289–298Google Scholar
  2. Bier E, Vässin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E, Jan LY, Jan YN (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3:1273–1287Google Scholar
  3. Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New YorkGoogle Scholar
  4. Casanova J, Struhl G (1993) The torso receptor localizes as well as transduces the spatial signal specifying terminal body pattern in Drosophila. Nature 362:152–155Google Scholar
  5. 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 12:977–996Google Scholar
  6. Cohen SM, Jürgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482–485Google Scholar
  7. Dalton D, Chadwick R, McGinnis W (1989) Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev 3:1940–1956Google Scholar
  8. Dorresteijn AWC, O'Grady B, Fischer A, Porchet-Henneré E, Boilly-Marer Y (1993) Molecular specification of cell lines in the embryo of Platynereis (Annelida). Roux's Arch Dev Biol 202:260–269Google Scholar
  9. Finkelstein R, Perrimon N (1990) The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346:485–488Google Scholar
  10. Fischer A (1985) Reproduction and postembryonic development of the annelid, Platynereis dumerilii. Film C1577., Institut für den wissenschaftlichen Film, Göttingen, GermanyGoogle Scholar
  11. Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL (1982) Monoclonal antibodies against Drosophila nervous system. Proc Natl Acad Sci USA 79:7929–7933Google Scholar
  12. González-Gaitán M, Rothe M, Wimmer EA, Taubert H, Jäckle H (1994) Redundant functions of the genes knirps and knirps-related for the establishment of anterior Drosophila head structures. Proc Natl Acad Sci USA 91:8567–8571Google Scholar
  13. Green P, Hartenstein AY, Hartenstein V (1993) The embryonic development of the Drosophila visual system. Cell Tissue Res 273:583–598Google Scholar
  14. Haget A (1977) L'embryologie des insectes. In: Grassé P-P (ed) Traité de Zoologie, vol VIII Fascicule V-B. Masson, Paris, pp 134–262Google Scholar
  15. Hartenstein V, Tepass U, Gruszynski E (1994) Embryonic development of the stomatogastric nervous system in Drosophila. J Comp Neurol 350:367–381Google Scholar
  16. Horridge GA (1965) The Arthropoda. In: Bullock TH, Horridge GA (eds) Structure and function in the nervous systems of inverterbrates, vol 2. Freeman WH and Company, San Francisco, pp 801–1270Google Scholar
  17. Jürgens G, Hartenstein V (1993) The terminal regions of the body pattern. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster, vol 1. CSHL Press, Cold Spring Harbor pp 687–746Google Scholar
  18. Jürgens G, Lehmann R, Schardin M, Nüsslein-Volhard C (1986) Segmental organization of the head in the embryo of Drosophila melanogaster. Roux's Arch Dev Biol 195:359–377Google Scholar
  19. Lee JJ, Kessler DP von, Parks S, Beachy PA (1992) Secretion and localized transcription suggest a role in positional signalling for products of the segmentation gene hedgehog. Cell 71:33–50Google Scholar
  20. Martin JR, Raibaud A, Ollo R (1994) Terminal pattern elements in Drosophila embryo induced by the torso-like protein Nature 367:741–745Google Scholar
  21. Ouelette RJ, Valet JP, Coté S (1992) Expression of gooseberry-proximal in the Drosophila developing nervous system responds to cues provided by segment polarity genes. Roux's Arch Dev Biol 201:157–168Google Scholar
  22. Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB. Goodman CS (1989) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58:955–968Google Scholar
  23. Penzlin H (1985) Stomatogastric nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, vol 5. Pergamon Press, Oxford, pp 371–406Google Scholar
  24. Pignoni F, Baldarelli RM, Steingrímsson E, Diaz RJ, Patapoutian A, Merriam JR, Lengyel JA (1990) The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 62:151–163Google Scholar
  25. Pignoni F, Steingrímsson E, Lengyel JA(1992) bicoid and the terminal system activate tailless expression in the early Drosophila embryo. Development 115:239–251Google Scholar
  26. Rempel JG (1975) The evolution of the insect head: an endless dispute. Questiones Entomologicae 11:7–25Google Scholar
  27. Schmidt-Ott U, Technau GM (1992) Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development 116:111–125Google Scholar
  28. Schmidt-Ott U, Technau GM (1994) Fate-mapping in the procephalic region of the embryonic Drosophila head. Roux's Arch Dev Biol 203:367–373Google Scholar
  29. Schmidt-Ott U, Sander K, Technau GM (1994a) Expression of engrailed in embryos of a beetle and five dipteran species with special reference to the terminal regions. Roux's Arch Dev Biol 203:298–303Google Scholar
  30. Schmidt-Ott U, Gonzalez Gaitan M, Jäckle H, Technau GM (1994b) Number, identity and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proc Natl Acad Sci USA 91:8363–8367Google Scholar
  31. Schmucker D, Taubert H, Jäckle H (1992) Formation of the Drosophila larval photoreceptor organ and its neuronal differentiation require continuous Krüppel gene activity. Neuron 9:1025–1039Google Scholar
  32. Scholtz G (1994) Head segmentation in Crustacea — an immunocytochemical study. Zoology, in pressGoogle Scholar
  33. Siewing R (1963) Zum Problem der Arthropodenkopfsegmentierung. Zool Anz 170:429–468Google Scholar
  34. Sprenger F, Stevens LM, Nüsslein-Volhard C (1989) The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature 338:478–483Google Scholar
  35. Strecker TR, Merriam JR, Lengyel JA (1988) Graded requirement for the zygotic terminal gene, tailless, in the brain and tail region of the Drosophila embryo. Development 102:721–734Google Scholar
  36. Tabata T, Eaton S, Kornberg TB (1992) The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 6:2635–2645Google Scholar
  37. Walldorf U, Gehring WJ (1992) Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J 11:2247–2259Google Scholar
  38. Wieschaus E, Nüsslein-Volhard C, Jürgens G (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Roux's Arch Dev Biol 193:296–307Google Scholar
  39. Wimmer EA, Jäckle H, Pfeifle C, Cohen SM (1993) A Drosophila homologue of human Sp1 is a head-specific segmentation gene. Nature 366:690–694Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Urs Schmidt-Ott
    • 1
  • Marcos González-Gaitán
    • 1
  • Gerhard M. Technau
    • 2
  1. 1.Max Planck Institut für biophysikalische ChemieGöttingenGermany
  2. 2.Institut für Genetik - Abteilung Zellbiologie Universität MainzMainzGermany

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