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Establishment of compartments in the developing leg imaginal discs ofDrosophila melanogaster

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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.

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References

  • Astauroff, B.: Studien über die erbliche Veränderung der Halteren beiDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.115, 424–447 (1929)

    Google Scholar 

  • 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 

  • Bodenstein, D.: The postembryonic development ofDrosophila. In “Biology ofDrosophila” (ed. M. Demerec), 275–367. New York: Hafner Publishing Company 1965

    Google Scholar 

  • Brehme, K.S.: A study of the effect on development of “Minute” mutations inDrosophila melanogaster. Genetics24, 131–161 (1939)

    Google Scholar 

  • Bridges, C., Morgan, T.: The third chromosome group of mutant characters ofDrosophila melanogaster. Carnegie Inst. of Washington Publ. no.327, 225 (1923)

    Google Scholar 

  • Bryant, P.J.: Cell lineage relationships in the imaginal wing disc ofDrosophila melanogaster. Develop. Biol.22, 389–411 (1970)

    PubMed  Google Scholar 

  • Bryant, P.J.: Pattern formation in the imaginal wing disc ofDrosophila melanogaster: Fate map, regeneration and duplication. J. exp. Zool.193, 49–78 (1975)

    PubMed  Google Scholar 

  • Bryant, P.J., Schneiderman, H.A.: Cell lineage, growth and determination in the imaginal leg disc ofDrosophila melanogaster. Develop. Biol.20, 263–290 (1969)

    PubMed  Google Scholar 

  • Chan, L.-N., Gehring, W.: Determination of blastoderm cells inDrosophila melanogaster. Proc. nat. Acad. Sci. (Wash.)68, 2217–2221 (1971)

    Google Scholar 

  • Crick, F.H.C., Lawrence, P.A.: Compartments and polyclones in insect development. Science189, 340–347 (1975)

    PubMed  Google Scholar 

  • Dunn, L.C., Coyne, J.: The effects of the Minute mutations ofDrosophila melanogaster on developmental rate. Hereditas23, 70–90 (1937)

    Google Scholar 

  • Fritz-Niggli, H.: Vergleichende Analyse der Strahlenschädigung vonDrosophila Eiern mit 180 keV und 31 MeV. Fortschr. Röntgenstr.83, 178–200 (1955)

    Google Scholar 

  • Garcia-Bellido, A.: Cell lineage in the wing disc ofDrosophila melanogaster. Genetics60, 181 (1968)

    Google Scholar 

  • Garcia-Bellido, A.: Genetic control of wing disc development inDrosophila. In “Cell Patterning”, Ciba Foundation Symposium29, 161–183 (1975)

  • Garcia-Bellido, A., Merriam, J.R.: Cell lineage of the imaginal discs inDrosophila gynandromorphs. J. exp. Zool.170, 61–76 (1969)

    PubMed  Google Scholar 

  • Garcia-Bellido, A., Merriam, J.R.: Parameters of the wing imaginal disc development ofDrosophila melanogaster. Develop. Biol.24, 61–87 (1971)

    PubMed  Google Scholar 

  • Garcia-Bellido, A., Ripoll, P., Morata, G.: Developmental compartmentalization of the wing disc ofDrosophila. Nature New Biol.245, 251–253 (1973)

    PubMed  Google Scholar 

  • Garcia-Bellido, A., Ripoll, P., Morata, G.: Developmental compartmentalization in the dorsal mesothoracic disc ofDrosophila. Develop. Biol.48, 132–147 (1976)

    PubMed  Google Scholar 

  • Garcia-Bellido, A., Santamaria, P.: Developmental analysis of the wing disc in the mutantengrailed ofDrosophila melanogaster. Genetics72, 87–104 (1972)

    PubMed  Google Scholar 

  • 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 1972

  • Gloor, H.: Phänokopie-Versuche mit Aether anDrosophila. Rev. Suisse Zool.54, 637–712 (1947)

    Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • Hadorn, E.: Initial transdetermination in the first leg discs of differentDrosophila species. Experientia32/3, 327–329 (1976)

    Google Scholar 

  • 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 

  • Hadorn, E., Buck, D.: Über Entwicklungsleistungen transplantierter Teilstücke von Flügel-Imaginalscheiben vonDrosophila melanogaster. Rev. Suisse Zool.69, 302–310 (1962)

    Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • Hannah-Alava, A.: Morphology and chaetotaxy of the legs ofDrosophila melanogaster. J. Morph.103, 281–310 (1958)

    Google Scholar 

  • Henke, K., Maas, H.: Über sensible Perioden der allgemeinen Körpergliederung vonDrosophila. Nachr. Akad. Wiss. Göttingen. Math.-Phys. Kl.1, 3–4 (1946)

    Google Scholar 

  • 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 

  • Hotta, Y., Benzer, S.: Mapping of behavior inDrosophila mosaics. In: Genetic Mechanisms of Development (ed. F. Ruddle). New York: Academic Press 1973

    Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • Lawrence, P.A.: The organization of the insect segment. Symp. Soc. exp. Biol.25, 379–392 (1971)

    PubMed  Google Scholar 

  • Lawrence, P.A.: A clonal analysis of segment development inOncopeltus (Hemiptera). J. Embryol. exp. Morphol.30, 681–699 (1973)

    PubMed  Google Scholar 

  • Lawrence, P.A.: The structure and properties of a compartment border: the intersegmental boundary inOncopeltus. In: “Cell Patterning”. Ciba Foundation Symposium29 (1975)

  • Lawrence, P.A., Morata, G.: Compartments in the wing ofDrosophila: a study of theengrailed gene. Develop. Biol.50, 321–337 (1976)

    PubMed  Google Scholar 

  • Lindsley, D.L., Grell, E.H.: Genetic variation inDrosophila melanogaster. Carnegie Institute of Washington, Publ. No.627 (1968)

  • Morata, G., Lawrence, P.A.: Control of compartment development by theengrailed gene inDrosophila. Nature255, 614–617 (1975)

    PubMed  Google Scholar 

  • Morata, G., Ripoll, P.: Minutes: Mutants ofDrosophila autonomously affecting cell division rate. Develop. Biol.42, 211–221 (1975)

    PubMed  Google Scholar 

  • 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)

  • 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 

  • 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)

    PubMed  Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • Schubiger, G.: Anlageplan, Determinationszustand und Transdeterminationsleistungen der männlichen Vorderbeinscheibe vonDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.160, 9–40 (1968)

    Google Scholar 

  • Schubiger, G.: Regeneration, duplication and transdetermination in fragments of the leg disc ofDrosophila melanogaster. Develop. Biol.26, 277–295 (1971)

    PubMed  Google Scholar 

  • Schweizer, P.: Wirkung von Röntgenstrahlen auf die Entwicklung der männlichen Genitalprimordien vonDrosophila melanogaster und Untersuchung von Erholungsvorgängen durch Zellklon-Analyse. Biophysik8, 158–188 (1972)

    PubMed  Google Scholar 

  • Stern, C.: Somatic crossing over and segregation inDrosophila melanogaster. Genetics21, 625–730 (1936)

    Google Scholar 

  • 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 

  • Tokunaga, C.: The differentiation of a secondary sex comb under the influence of the geneengrailed inDrosophila melanogaster. Genetics46, 157–176 (1961)

    PubMed  Google Scholar 

  • Tokunaga, C.: Cell lineage and differentiation on the male foreleg ofDrosophila melanogaster. Develop. Biol.4, 489–516 (1962)

    PubMed  Google Scholar 

  • 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 

  • Wieschaus, E., Gehring, W.: Clonal analysis of primordial disc cells in the early embryo ofDrosophila melanogaster. Develop. Biol.50, 249–263 (1976a)

    PubMed  Google Scholar 

  • Wieschaus, E., Gehring, W.: Gynandromorph analysis of the thoracic disc primordia inDrosophila melanogaster. Roux's Arch. (1976b)

  • Zalokar, M.: L'ablation des disques imaginaux chez la larve deDrosophile. Rev. Suisse Zool.50, 232–237 (1943)

    Google Scholar 

  • Zalokar, M.: Anatomie du thorax deDrosophila melanogaster. Rev. Suisse Zool.54, 17–53 (1947)

    Google Scholar 

Download references

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Steiner, E. Establishment of compartments in the developing leg imaginal discs ofDrosophila melanogaster . Wilhelm Roux' Archiv 180, 9–30 (1976). https://doi.org/10.1007/BF00848882

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