Skip to main content
SpringerLink
Log in

Proximal-distal pattern formation inDrosophila: graded requirement forDistal-less gene activity during limb development

  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Summary

The development of all of the adult limbs inDrosophila depends upon the activity of theDistal-less gene. We report here the phenotypic characterization of a number of hypomorphicDistal-less alleles which indicates that there is a graded requirement forDistal-less activity in the developing limbs. Previous analysis of genetically mosaic animals indicated that cells in the early primordia of the limb imaginal dises possess a graded proximal-distal positional information which depends on the presence of theDistal-less gene for its expression. Taken together these data suggest thatDistal-less may directly encode the graded positional information that is required to organise the proximal-distal axis of the developing limbs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22

    PubMed  CAS  Google Scholar 

  • Anderson DT (1972a) The development of hemimetabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects. vol 1. Academic Press, New York, pp 96–163

    Google Scholar 

  • Anderson DT (1972b) The development of holometabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects. vol 1. Academic Press, New York, pp 165–242

    Google Scholar 

  • Anderson KV (1987) Dorsal-ventral embryonic pattern genes ofDrosophila. Trends Genet 3:91–97

    Article  Google Scholar 

  • Beeman RW, Stuart JJ, Haas MS, Denell RE (1989) Genetic analysis of the homeotic gene complex (HOM-C) in the beetleTribolium castaneum. Dev Biol 133:196–209

    Article  PubMed  CAS  Google Scholar 

  • Bender W, Akam M, Karch F, Beachy PA, Peifer M, Spierer P, Lewis EB, Hogness DS (1983) Molecular genetics of the Bithorax complex inDrosophila melanogaster. Science 221:23–29

    CAS  PubMed  Google Scholar 

  • Bryant PJ (1978) Pattern formation in imaginal dises. In: Ashburner M, Wright TRF (eds) The genetics and biology ofDrosophila, vol 2c. Academic Press, New York, pp 229–335

    Google Scholar 

  • Chadwick R, McGinnis W (1987) Temporal and spatial distribution of transcripts from the Deformed gene ofDrosophila. EMBO J 6:779–789

    PubMed  CAS  Google Scholar 

  • Cohen SM, Jürgens G (1989) Proximal-distal pattern formation inDrosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J 8:2045–2055

    PubMed  CAS  Google Scholar 

  • Cohen SM, Brönner G, Küttner F, Jürgens G, Jäckle H (1989) Distal-less encodes a homeodomain protein required for limb development inDrosophila. Nature 338:432–434

    Article  PubMed  CAS  Google Scholar 

  • Driever W, Nüsslein-Volhard C (1988a) A gradient of bicoid protein inDrosophila embryos. Cell 54:83–93

    Article  PubMed  CAS  Google Scholar 

  • Driever W, Nüsslein-Volhard C (1988b) The bicoid protein determines position in theDrosophila embryo in a concentration-dependent manner. Cell 54:95–104

    Article  PubMed  CAS  Google Scholar 

  • Driever W, Nüsslein-Volhard C (1989) Maternal control of zygotic gene expression inDrosophila: bicoid protein regulates the expression of the gap gene hunchback. Nature 337:138–143

    Article  PubMed  CAS  Google Scholar 

  • Eassa YEE (1953) The development of imaginal buds in the head ofPieris brassicae Linn. (Lepidoptera). Trans R Ent Soc Lond 104:39–51

    Google Scholar 

  • Frigerio G, Burri M, Bopp D, Baumgartner S, Noll M (1986) Structure of the segmentation gene paired and theDrosophila PRD gene set as part of a gene network. Cell 47:735–746

    Article  PubMed  CAS  Google Scholar 

  • Fristrom D, Fristrom JW (1975) The mechanism of evagination of imaginal discs ofDrosophila melanogaster: 1. general considerations. Dev Biol 43:1–23

    Article  CAS  Google Scholar 

  • Frohnhöfer HG, Nüsslein-Volhard C (1986) Organization of anterior pattern in theDrosophila embryo by the maternal gene bicoid. Nature 324:120–125

    Article  Google Scholar 

  • Frohnhöfer HG, Nüsslein-Volhard C (1987) Maternal genes required for the anterior localization of bicoid activity in the embryo ofDrosophila. Genes Dev 1:880–890

    Google Scholar 

  • Gehring WJ, Seippel S (1967) Die Imaginalzellen des Clypeo-Labrums und die Bildung des Rüssels vonDrosophila melanogaster. Rev Suisse Zool 74:589–596

    PubMed  CAS  Google Scholar 

  • Hadorn E (1978) Transdetermination. In: Ashburner M, Wright TRF (eds) The genetics and biology ofDrosophila. vol 2c. Academic Press, New York, pp 555–617

    Google Scholar 

  • Jürgens G, Lehmann R, Schardin M, Nüsslein-Volhard C (1986) Segmental organization of the head in the embryo ofDrosophila melanogaster. A blastoderm fate map of the cuticle structures of the larval head. Wilhelm Roux’s Arch 195:359–377

    Google Scholar 

  • Kaufman TC (1978) Cytogenetic analysis of chromosome 3 inDrosophila melanogaster: Isolation and characterization of four new alleles of the proboscipedia locus. Genetics 90:579–596

    PubMed  Google Scholar 

  • Kellogg VL (1902) The development and homologies of the mouth parts of insects. Am Nat XXXVI:683–706

    Article  Google Scholar 

  • Kennison JA, Russell MA (1987) Dosage-dependent modifiers of homeotic mutations inDrosophila melanogaster. Genetics 116:75–86

    PubMed  Google Scholar 

  • Kim C-W (1959) The differentiation centre inducing the development from larval to adult leg inPieris brassicae (Lepidoptera). J Embryol Exp Morph 7:572–582

    PubMed  CAS  Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation inDrosophila. Nature 276:565–570

    Article  PubMed  CAS  Google Scholar 

  • Lewis EB, Bacher F (1968) Method of feeding ethyl methane sulfonate (EMS) toDrosophila males. Dros Inf Serv 43:193

    Google Scholar 

  • Lindsley DL, Grell EH (1968) Genetic variations ofDrosophila melanogaster. Carnegie Inst Washington, yearbook 627

  • Lindsley DL, Zimm G (1985, 1986, 1987) Dros Inf Serv, vol 62–65

  • Madhavan MM, Schneiderman HA (1977) Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development ofDrosophila melanogaster. Wilhelm Roux’s Arch 183:269–305

    Article  Google Scholar 

  • Martinez-Arias A, Ingham P, Scott MP, Akam ME (1987) The spatial and temporal deployment of Dfd and Scr transcripts throughout development ofDrosophila. Development 100:673–683

    PubMed  CAS  Google Scholar 

  • Meinhardt H (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev Biol 96:375–385

    Article  PubMed  CAS  Google Scholar 

  • Miall LC, Hammond AR (1892) The development of the head of the imago ofChironomus. Trans Linn Soc (ser2) Zool 5:265–279

    Article  Google Scholar 

  • Morata G, Lawrence PA (1979) The development of the eye-antena imaginal dise ofDrosophila. Dev Biol 70:355–371

    Article  PubMed  CAS  Google Scholar 

  • Nagoshi RN, Gelbart WM (1987) Molecular and recombinational mapping of mutations in the Ace locus ofDrosophila melanogaster. Genetics 117:487–502

    PubMed  CAS  Google Scholar 

  • Nüsslein-Volhard C, Lohs-Schardin M, Sander K, Cremer C (1980) A dorso-ventral shift of embryonic primordia in a new maternal effect mutant ofDrosophila. Nature 283:474–476

    Article  PubMed  Google Scholar 

  • Postlethwait JH, Schneiderman HA (1971) Pattern formation and determination in the antenna of the homeotic mutant Antennapedia ofDrosophila melanogaster. Dev Biol 25:606–640

    Article  PubMed  CAS  Google Scholar 

  • Roberts DB (1986) In: Roberts DB (ed) Drosophila: a practical approach. IRL press. Oxford Washington, pp 1–58

    Google Scholar 

  • Sato T (1984) A new homeotic mutation affecting antennae and legs. Dros Inf Service 60:180–182

    Google Scholar 

  • Schröder C, Tautz D, Seifert E, Jäckle H (1988) Differential regulation of the two transcripts from the Drosophila gap segmentation gene hunchback. EMBO J 7:2881–2887

    PubMed  Google Scholar 

  • Schubiger G (1968) Anlageplan, Determinationzustand und Transdeterminationsleistungen der männlichen Vorderbeinscheibe vonDrosophila melanogaster. Roux’ Archiv für Entwicklungsmechanik 160:9–40

    Article  Google Scholar 

  • Snodgrass RE (1935) Priciples of insect morphogenesis. McGraw Hill, New York London

    Google Scholar 

  • Steiner E (1976) Establishment of compartments in the developing leg imaginal discs ofDrosophila melanogaster. Wilhelm Roux’s Arch 180:9–30

    Article  Google Scholar 

  • Steward R (1987) Dorsal, an embryonic polarity gene inDrosophila, is homologous to the vertebrate proto-oncogene c-rel. Science 238:692–694

    PubMed  CAS  Google Scholar 

  • Steward R, Zusman SB, Huang LH, Schedl P (1988) The dorsal protein is distributed in a gradient in earlyDrosophila embryos. Cell 55:487–495

    Article  PubMed  CAS  Google Scholar 

  • Struhl G (1981a) A homeotic mutation transforming leg into antenna inDrosophila. Nature 292:636–638

    Article  Google Scholar 

  • Struhl G (1981b) Anterior and posterior compartments in the proboscis ofDrosophila. Dev Biol 84:372–385

    Article  Google Scholar 

  • Struhl G (1981c) A blastoderm fate map of compartments and segments of theDrosophila head. Dev Biol 84:386–396

    Article  Google Scholar 

  • Struhl G (1984) Splitting the bithorax complex ofDrosophila. Nature 308:454–457

    Article  Google Scholar 

  • Sunkel CE, Whittle JRS (1987) Brista: a gene involved in the specification and differentiation of distal cephalic and thoracic structures inDrosophila melanogaster. Wilhelm Roux’s Arch 196:124–132

    Google Scholar 

  • Wieschaus E, Gehring WJ (1976a) Gynandromorph analysis of the thoracic disc primordia inDrosophila melanogaster. Wilhelm Roux’s Arch 180:31–46

    Article  Google Scholar 

  • Wieschaus E, Gehring WJ (1976b) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol 50:249–263

    Article  PubMed  CAS  Google Scholar 

  • Wieschaus E, Nüsslein-Volhard C (1986) In: Roberts DB (ed) Drosophila: a practical approach. IRL press, Oxford Washington, pp 199–227

    Google Scholar 

  • Zachar Z, Bingham PM (1982) Regulation of white locus expression: the structure of mutant alleles at the white locus ofDrosophila melanogaster. Cell 30:529–541

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Stephen M. Cohen

    Present address: Department of Cell Biology, Baylor College of Medicine, 77030, Texas, Houston, USA

Authors and Affiliations

  1. Institut für Genetik und Mikrobiologie, Universität München, Maria-Ward-St. 1 A, D-8000, München 19, Federal Republic of Germany

    Stephen M. Cohen & Gerd Jürgens

Authors
  1. Stephen M. Cohen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerd Jürgens
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cohen, S.M., Jürgens, G. Proximal-distal pattern formation inDrosophila: graded requirement forDistal-less gene activity during limb development. Roux’s Arch Dev Biol 198, 157–169 (1989). https://doi.org/10.1007/BF02438941

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02438941

Key words

Search

Navigation