Advertisement

Establishment of compartments in the developing leg imaginal discs ofDrosophila melanogaster

  • Emil Steiner
Article

Summary

By X-irradiation ofM/M+ embryos and larvae to induce mitotic recombination, clones ofM+/M+ genotype were obtained (Fig. 1). Since such cells grow faster than the surroundingM/M+-cells they can fill large areas within the compartments of an imaginal disc.

The present studies concentrated mainly on the three leg discs. Clones were induced by doses of 1000 r at ages ranging from 3±0.5 h after oviposition to 144 h.

All clones induced later than the blastoderm stage were absolutely restricted to either the anterior or the posterior compartment of a disc. The border between the anterior and posterior compartment runs as a straight line along the entire leg and at the distal end separates the two claws (Figs. 5, 6, 7). A further subdivision of the anterior compartment is indicated by clones initiated in the second larval instar (Fig. 11). A parallel subdivision could not be detected in the posterior compartment. Irradiation in the early third instar led to clones which were restricted to single longitudinal bristle rows and leg segments. But no clear-cut compartment borders could be found; in particular a proximo-distal separation appears to be absent.

Among the 318 clones induced at the blastoderm stage eleven extended from the wing into the second leg (Fig. 8), or from the haltere into the third leg.

With the exception of 3 clones that apparently occupied the anterior as well as the posterior compartment of a wing or a leg, all clones remained confined to either the anterior or the posterior compartment.

Frequently clones overlapped left and right forelegs (Fig. 9). Intersegmental overlaps were not observed.

The results show that the earliest compartment borders appear in all thoracic discs. This suggests that compartmentalization is a fundamental process common to all discs.

Key words

Imaginal discs Compartments Clonal analysis Embryonic determination 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Astauroff, B.: Studien über die erbliche Veränderung der Halteren beiDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.115, 424–447 (1929)Google Scholar
  2. Becker, H.J.: Über Röntgenmosaikflecken und Defektmutationen am Auge vonDrosophila und die Entwicklungsphysiologie des Auges. Z. indukt. Abstamm.-u. Vererb.-L.88, 333–373 (1957)Google Scholar
  3. Bodenstein, D.: The postembryonic development ofDrosophila. In “Biology ofDrosophila” (ed. M. Demerec), 275–367. New York: Hafner Publishing Company 1965Google Scholar
  4. Brehme, K.S.: A study of the effect on development of “Minute” mutations inDrosophila melanogaster. Genetics24, 131–161 (1939)Google Scholar
  5. Bridges, C., Morgan, T.: The third chromosome group of mutant characters ofDrosophila melanogaster. Carnegie Inst. of Washington Publ. no.327, 225 (1923)Google Scholar
  6. Bryant, P.J.: Cell lineage relationships in the imaginal wing disc ofDrosophila melanogaster. Develop. Biol.22, 389–411 (1970)PubMedGoogle Scholar
  7. Bryant, P.J.: Pattern formation in the imaginal wing disc ofDrosophila melanogaster: Fate map, regeneration and duplication. J. exp. Zool.193, 49–78 (1975)PubMedGoogle Scholar
  8. Bryant, P.J., Schneiderman, H.A.: Cell lineage, growth and determination in the imaginal leg disc ofDrosophila melanogaster. Develop. Biol.20, 263–290 (1969)PubMedGoogle Scholar
  9. Chan, L.-N., Gehring, W.: Determination of blastoderm cells inDrosophila melanogaster. Proc. nat. Acad. Sci. (Wash.)68, 2217–2221 (1971)Google Scholar
  10. Crick, F.H.C., Lawrence, P.A.: Compartments and polyclones in insect development. Science189, 340–347 (1975)PubMedGoogle Scholar
  11. Dunn, L.C., Coyne, J.: The effects of the Minute mutations ofDrosophila melanogaster on developmental rate. Hereditas23, 70–90 (1937)Google Scholar
  12. Fritz-Niggli, H.: Vergleichende Analyse der Strahlenschädigung vonDrosophila Eiern mit 180 keV und 31 MeV. Fortschr. Röntgenstr.83, 178–200 (1955)Google Scholar
  13. Garcia-Bellido, A.: Cell lineage in the wing disc ofDrosophila melanogaster. Genetics60, 181 (1968)Google Scholar
  14. Garcia-Bellido, A.: Genetic control of wing disc development inDrosophila. In “Cell Patterning”, Ciba Foundation Symposium29, 161–183 (1975)Google Scholar
  15. Garcia-Bellido, A., Merriam, J.R.: Cell lineage of the imaginal discs inDrosophila gynandromorphs. J. exp. Zool.170, 61–76 (1969)PubMedGoogle Scholar
  16. Garcia-Bellido, A., Merriam, J.R.: Parameters of the wing imaginal disc development ofDrosophila melanogaster. Develop. Biol.24, 61–87 (1971)PubMedGoogle Scholar
  17. Garcia-Bellido, A., Ripoll, P., Morata, G.: Developmental compartmentalization of the wing disc ofDrosophila. Nature New Biol.245, 251–253 (1973)PubMedGoogle Scholar
  18. Garcia-Bellido, A., Ripoll, P., Morata, G.: Developmental compartmentalization in the dorsal mesothoracic disc ofDrosophila. Develop. Biol.48, 132–147 (1976)PubMedGoogle Scholar
  19. Garcia-Bellido, A., Santamaria, P.: Developmental analysis of the wing disc in the mutantengrailed ofDrosophila melanogaster. Genetics72, 87–104 (1972)PubMedGoogle Scholar
  20. Gehring, W.: The stability of the determined state in cultures of imaginal discs inDrosophila. In “The Biology of Imaginal discs” (Ed. by H. Ursprung and R. Nöthiger), 35–58, Springer Verlag 1972Google Scholar
  21. Gloor, H.: Phänokopie-Versuche mit Aether anDrosophila. Rev. Suisse Zool.54, 637–712 (1947)Google Scholar
  22. Hadorn, E.: Konstanz, Wechsel und Typus der Determination und Differenzierung in Zellen aus männlichen Genitalanlagen vonDrosophila melanogaster nach Dauerkulturin vivo. Develop. Biol.13, 424–509 (1966)PubMedGoogle Scholar
  23. Hadorn, E.: Initial transdetermination in the first leg discs of differentDrosophila species. Experientia32/3, 327–329 (1976)Google Scholar
  24. Hadorn, E., Bertani, G., Gallera, J.: Regulationsfähigkeit und Feldorganisation der männlichen Genital-Imaginalscheibe vonDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.144, 31–70 (1949)Google Scholar
  25. Hadorn, E., Buck, D.: Über Entwicklungsleistungen transplantierter Teilstücke von Flügel-Imaginalscheiben vonDrosophila melanogaster. Rev. Suisse Zool.69, 302–310 (1962)Google Scholar
  26. Hadorn, E., Hürlimann, R., Mindek, G., Schubiger, G., Staub, M.: Entwicklungsleistungen embryonaler Blasteme vonDrosophila nach Kultur im Adultwirt. Rev. Suisse Zool.75, 557–569 (1968)PubMedGoogle Scholar
  27. Hannah-Alava, A.: Morphology and chaetotaxy of the legs ofDrosophila melanogaster. J. Morph.103, 281–310 (1958)Google Scholar
  28. Henke, K., Maas, H.: Über sensible Perioden der allgemeinen Körpergliederung vonDrosophila. Nachr. Akad. Wiss. Göttingen. Math.-Phys. Kl.1, 3–4 (1946)Google Scholar
  29. Hollingsworth, M.J.: Sex-combs of intersexes and the arrangement of the chaetae on the legs ofDrosophila. J. Morph.115, 35–52 (1964)Google Scholar
  30. Hotta, Y., Benzer, S.: Mapping of behavior inDrosophila mosaics. In: Genetic Mechanisms of Development (ed. F. Ruddle). New York: Academic Press 1973Google Scholar
  31. Illmensee, K., Mahowald, A.P.: Transplantation of posterior polar plasm inDrosophila. Induction of germ cells at the anterior pole of the eggs. Proc. nat. Acad. Sci. USA71, 1016–1020 (1974)PubMedGoogle Scholar
  32. Lawrence, P.A.: The organization of the insect segment. Symp. Soc. exp. Biol.25, 379–392 (1971)PubMedGoogle Scholar
  33. Lawrence, P.A.: A clonal analysis of segment development inOncopeltus (Hemiptera). J. Embryol. exp. Morphol.30, 681–699 (1973)PubMedGoogle Scholar
  34. Lawrence, P.A.: The structure and properties of a compartment border: the intersegmental boundary inOncopeltus. In: “Cell Patterning”. Ciba Foundation Symposium29 (1975)Google Scholar
  35. Lawrence, P.A., Morata, G.: Compartments in the wing ofDrosophila: a study of theengrailed gene. Develop. Biol.50, 321–337 (1976)PubMedGoogle Scholar
  36. Lindsley, D.L., Grell, E.H.: Genetic variation inDrosophila melanogaster. Carnegie Institute of Washington, Publ. No.627 (1968)Google Scholar
  37. Morata, G., Lawrence, P.A.: Control of compartment development by theengrailed gene inDrosophila. Nature255, 614–617 (1975)PubMedGoogle Scholar
  38. Morata, G., Ripoll, P.: Minutes: Mutants ofDrosophila autonomously affecting cell division rate. Develop. Biol.42, 211–221 (1975)PubMedGoogle Scholar
  39. Nöthiger, R.: The larval development of imaginal discs. In “The Biology of Imaginal discs” (Ed. by H. Ursprung and R. Nöthiger) 1–34, Springer Verlag (1972)Google Scholar
  40. Peyer, B., Hadorn, E.: Zum Manifestationsmuster der Mutante “multiple wing hairs” (mwh) vonDrosophila melanogaster. Arch. Klaus-Stift. Vererb.-Forsch.40, 19–26 (1965)Google Scholar
  41. Postlethwait, J.H., Schneiderman, H.A.: A clonal analysis of development inDrosophila melanogaster: Morphogenesis, determination and growth in the wild-type antenna. Develop. Biol.24, 477–519 (1971)PubMedGoogle Scholar
  42. Postlethwait, J.H., Schneiderman, H.A.: Pattern formation in imaginal discs ofDrosophila melanogaster after irradiation of embryos and young larvae. Develop. Biol.32, 345–360 (1973)PubMedGoogle Scholar
  43. Schubiger, G.: Anlageplan, Determinationszustand und Transdeterminationsleistungen der männlichen Vorderbeinscheibe vonDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.160, 9–40 (1968)Google Scholar
  44. Schubiger, G.: Regeneration, duplication and transdetermination in fragments of the leg disc ofDrosophila melanogaster. Develop. Biol.26, 277–295 (1971)PubMedGoogle Scholar
  45. Schweizer, P.: Wirkung von Röntgenstrahlen auf die Entwicklung der männlichen Genitalprimordien vonDrosophila melanogaster und Untersuchung von Erholungsvorgängen durch Zellklon-Analyse. Biophysik8, 158–188 (1972)PubMedGoogle Scholar
  46. Stern, C.: Somatic crossing over and segregation inDrosophila melanogaster. Genetics21, 625–730 (1936)Google Scholar
  47. Sturtevant, A.H.: The claret mutant type ofDrosophila simulans: A study of chromosome elimination and of cell-lineage. Z. Wiss. Zool.135, 323–356 (1929)Google Scholar
  48. Tokunaga, C.: The differentiation of a secondary sex comb under the influence of the geneengrailed inDrosophila melanogaster. Genetics46, 157–176 (1961)PubMedGoogle Scholar
  49. Tokunaga, C.: Cell lineage and differentiation on the male foreleg ofDrosophila melanogaster. Develop. Biol.4, 489–516 (1962)PubMedGoogle Scholar
  50. Ursprung, H.: Fragmentierungs- und Bestrahlungsversuche zur Bestimmung von Determinationszustand und Anlageplan der Genitalscheiben vonDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.151, 504–558 (1959)Google Scholar
  51. Wieschaus, E., Gehring, W.: Clonal analysis of primordial disc cells in the early embryo ofDrosophila melanogaster. Develop. Biol.50, 249–263 (1976a)PubMedGoogle Scholar
  52. Wieschaus, E., Gehring, W.: Gynandromorph analysis of the thoracic disc primordia inDrosophila melanogaster. Roux's Arch. (1976b)Google Scholar
  53. Zalokar, M.: L'ablation des disques imaginaux chez la larve deDrosophile. Rev. Suisse Zool.50, 232–237 (1943)Google Scholar
  54. Zalokar, M.: Anatomie du thorax deDrosophila melanogaster. Rev. Suisse Zool.54, 17–53 (1947)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • Emil Steiner
    • 1
  1. 1.Zoologisch-Vergl. Anatomisches Institut der Universität ZürichZürichSwitzerland

Personalised recommendations