Journal of Genetics

, Volume 86, Issue 2, pp 111–123 | Cite as

Complex genetic interactions govern the temporal effects of Antennapedia on antenna-to-leg transformations in Drosophila melanogaster

  • Ian DworkinEmail author
  • Wendy Lee
  • Fiona Mccloskey
  • Ellen Larsen
Research Article


The putative regulatory relationships between Antennapedia (Antp), spalt major (salm) and homothorax (hth) are tested with regard to the sensitive period of antenna-to-leg transformations. Although Antp expression repressed hth as predicted, contrary to expectations, hth did not show increased repression at higher Antp doses, whereas salm, a gene downstream of hth, did show such a dose response. Loss of hth allowed antenna-to-leg transformations but the relative timing of proximal-distal transformations was reversed, relative to transformations induced by ectopic Antp. Finally, overexpression of Hth was only partially able to rescue transformations induced by ectopic Antp. These results indicate that there may be additional molecules involved in antenna/leg identity and that spatial, temporal and dosage relationships are more subtle than suspected and must be part of a robust understanding of molecular network behaviour involved in determining appendage identity in Drosophila melanogaster.


homoeotic transformation sensitive periods spalt homothorax Antennapedia Drosophila 


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  1. Angelini D. R. and Kaufman T. C. 2004 Functional analysis in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects. Dev. Biol. 271, 306–321.PubMedCrossRefGoogle Scholar
  2. Azpiazu N. and Morata G. 2002 Distinct functions of homothorax in leg development in Drosophila. Mech. Dev. 119, 55–67.PubMedCrossRefGoogle Scholar
  3. Beermann A. and Schroder R. 2004 Functional stability of the aristaless gene in appendage tip formation during evolution. Dev. Genes Evol. 214, 303–308.PubMedCrossRefGoogle Scholar
  4. Beermann A., Jay D. G., Beeman R. W., Hulskamp M., Tautz D. and Jurgens G. 2001 The Short antennae gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein. Development 128, 287–297.PubMedGoogle Scholar
  5. Bhojwani J., Shashidhara L. S. and Sinha P. 1997 Requirement of teashirt (tsh) function during cell fate specification in developing head structures in Drosophila. Dev. Genes Evol. 207, 137–146.CrossRefGoogle Scholar
  6. Cabrera G. R., Godt D., Fang P.-Y., Couderc, J.-L. and Laski F. A. 2002 Expression pattern of Gal4 enhancer trap insertions into the bric à brac locus generated by P element replacement. Genesis 34, 62–65.PubMedCrossRefGoogle Scholar
  7. Casares F. and Mann R. S. 1998 Control of antennal vs leg development in Drosophila. Nature 392, 723–726.PubMedCrossRefGoogle Scholar
  8. Chu J., Dong P. D. and Panganiban G. 2002 Limb type-specific regulation of bric-a-brac contributes to morphological diversity. Dev. 129, 695–704.Google Scholar
  9. Dong P. D. Chu J. and Panganiban G. 2000 Coexpression of the homeobox genes Distal-less and homothorax determines Drosophila antennal identity. Development 127, 209–216.PubMedGoogle Scholar
  10. Dong P. D., Chu J. and Panganiban G. 2001 Proximodistal domain specification and interactions in developing Drosophila appendages. Development 128, 2365–2372.PubMedGoogle Scholar
  11. Dong P. D., Dicks J. S. and Panganiban G. 2002 Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna. Development 129, 1967–1974.PubMedGoogle Scholar
  12. Duncan D. M., Burgess E. A. and Duncan I. 1998 Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev. 12, 1290–1303.PubMedGoogle Scholar
  13. Dworkin I. 2005 Evidence for canalization of Distal-less function in the leg of Drosophila melanogaster. Evol. Dev. 7, 89–100.PubMedCrossRefGoogle Scholar
  14. Emerald B. S. and Cohen S. M. 2004 Spatial and temporal regulation of the homoeotic selector gene Antennapedia is required for the establishment of leg identity in Drosophila. Dev. Biol. 267, 462–472.PubMedCrossRefGoogle Scholar
  15. Emerald B. S., Curtiss J., Mlodzik M. and Cohen S. M. 2003 Distal antenna and distal antenna related encode nuclear proteins containing pipsqueak motifs involved in antenna development in Drosophila. Development 130, 1171–1180.PubMedCrossRefGoogle Scholar
  16. Fienberg S. E. 1980 The analysis of cross-classical categorical data. MIT Press. MassGoogle Scholar
  17. Gibson G. and Gehring W. J. 1988 Head and thoracic transformations caused by ectopic expression of Antennapedia during drosophila development. Development 102, 657–675.Google Scholar
  18. Golic K. G. 1991 Site-specific recombination between homologous chromosomes in Drosophila. Science 252, 958–961.PubMedCrossRefGoogle Scholar
  19. Held L. I. 1990 Sensitive periods for abnormal patterning on a leg segment in Drosophila melanogaster. Rouxs Arch. Dev. Biol. 199, 31–47.CrossRefGoogle Scholar
  20. Held L. I. 2002 Bristles induce bracts via the EGFR pathway on Drosophila legs. Mech. Dev. 117, 225–234.PubMedCrossRefGoogle Scholar
  21. Herke S. W., Serio N. V. and Rogers B. T. 2005 Functional analyses of tiptop and antennapedia in the embryonic development of Oncopeltus fasciatus suggests an evolutionary pathway from ground state to insect legs. Development 132, 27–34.PubMedCrossRefGoogle Scholar
  22. Hosmer D. W. and Lemeshow S. 1989 Applied logistic Regression Wiley. NYGoogle Scholar
  23. Inbal A., Halachmi N., Dibner C., Frank D. and Salzberg A. 2001 Genetic evidence for the transcriptional-activating function of Homothorax during adult fly development. Development 128, 3405–3413.PubMedGoogle Scholar
  24. Jaw T. J., You L. R., Knoepfler P. S., Yao L. C., Pai C. Y., Tang C. Y. et al. 2000 Direct interaction of two homeoproteins, homothorax and extradenticle, is essential for EXD nuclear localization and function. Mech. Dev. 91, 279–291.PubMedCrossRefGoogle Scholar
  25. Johnston L. A., Ostrow B. D., Jasoni C. and Blochlinger K. 1998 The homeobox gene cut interacts genetically with the homeotic genes proboscipedia and Antennapedia. Genetics 149, 131–142.PubMedGoogle Scholar
  26. Kopp A. and True J. R. 2002 Evolution of male sexual characters in the Oriental Drosophila melanogaster species group. Evol. Dev. 4, 278–291.PubMedCrossRefGoogle Scholar
  27. Kurant E., Pai C. Y., Sharf R., Halachmi N., Sun Y. H. and Salzberg A. 1998 Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS. Development 125, 1037–1048.PubMedGoogle Scholar
  28. Larsen E., Lee T. and Glickman N. 1996 Antenna to leg transformation: dynamics of developmental competence. Dev. Genet. 19, 333–339.PubMedCrossRefGoogle Scholar
  29. Pai C. Y., Kuo T. S., Jaw T. J., Kurant E., Chen C. T., Bessarab D. A., Salzberg A. and Sun Y. H. 1998 The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, Extradenticle, and suppresses eye development in Drosophila. Genes Dev. 12, 435–446.PubMedGoogle Scholar
  30. Panganiban G., Nagy L. and Carroll S. B. 1994 The role of the Distal-less gene in the development and evolution of insect limbs. Curr. Biol. 4, 671–675.PubMedCrossRefGoogle Scholar
  31. Panganiban G., Irvine S. M., Lowe C., Roehl H., Corley L. S., Sherbon B. et al. 1997 The origin and evolution of animal appendages. Proc. Natl. Acad. Sci. USA 94, 5162–5166.PubMedCrossRefGoogle Scholar
  32. Postlethwait J. and Schneiderman H. A. 1969 A clonal analysis of determination in Antennapedia, a homoeotic mutant of drosophila melanogaster. Proc. Natl. Acad. Sci. USA 64, 176–183.PubMedCrossRefGoogle Scholar
  33. Postlethwait J. H. and Schneidermam H. A. 1971 Pattern formation and determination in the antenna of the homeotic mutant Antennapedia of Drosophila melanogaster. Dev. Biol. 25, 606–640.PubMedCrossRefGoogle Scholar
  34. Rieckhof G. E., Casares F., Ryoo H. D., Abu-Shaar M. and Mann R. S. 1997 Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 91, 171–183.PubMedCrossRefGoogle Scholar
  35. Roch F. and Akam M. 2000 Ultrabithorax and the control of cell morphology in Drosophila halteres. Development 127, 97–107.PubMedGoogle Scholar
  36. Scanga S. Manoukian A. and Larsen E. 1995 Time-dependent and concentration-dependent response of the Drosophila antenna imaginal disc to Antennapedia. Dev. Biol. 169, 673–682.PubMedCrossRefGoogle Scholar
  37. Sokal R. R. and Rohlf F. J. 1995 Biometry Freeman, New York.Google Scholar
  38. Steinbach O. C., Wolffe A. P. and Rupp R. A. 1997 Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature 389, 395–399.PubMedCrossRefGoogle Scholar
  39. Steel R. G. D., Torrie J. H. and Dickey D. A 1997 Principles and procedures in statistics. A biometrical approach. McGraw-Hill. New York.Google Scholar
  40. Stokes M. E. Davis C. S. and Koch G. G. 2000 categorial data analysis using the SAS system. Wiley. New York.Google Scholar
  41. Suzanne M., Estella C., Calleja M. and Sanchez-Herrero E. 2003 The hernandez and fernandez genes of Drosophila specify eye and antenna. Dev. Biol. 260, 465–483.PubMedCrossRefGoogle Scholar
  42. Wagner-Bernholz J. T., Wilson C., Gibson G., Schuh R. and Gehring W. J. 1991 Identification of target genes of the homeotic gene Antennapedia by enhancer detection. Genes Dev. 5, 2467–2480.PubMedCrossRefGoogle Scholar
  43. Wakimoto B. T., Turner F. R. and Kaufman T. C. 1984 Defects in embryogenesis in mutants associated with the antennapedia gene complex of Drosophila melanogaster. Dev. Biol. 102, 147–172.PubMedCrossRefGoogle Scholar
  44. Xu T. and Rubin G. M. 1993 Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237.PubMedGoogle Scholar
  45. Yao L. C., Liaw G. J., Pai C. Y. and Sun Y. H. 1999 A common mechanism for antenna-to-leg transformation in Drosophila: suppression of homothorax transcription by four HOM-C genes. Dev. Biol. 211, 268–276.PubMedCrossRefGoogle Scholar
  46. Zeng W., Andrew D. J., Mathies L. D., Horner M. A. and Scott M. P. 1993 Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity. Development 118, 339–352.PubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2007

Authors and Affiliations

  • Ian Dworkin
    • 1
    • 2
    Email author
  • Wendy Lee
    • 1
    • 3
  • Fiona Mccloskey
    • 1
  • Ellen Larsen
    • 1
    • 4
  1. 1.Department of ZoologyUniversity of TorontoOntarioCanada
  2. 2.Department of ZoologyMichigan State UniversityEast LansingUSA
  3. 3.Department of Molecular Biology and BiochemistrySimon Fraser UniversityBurnabyCanada
  4. 4.Department of Cell and Systems BiologyUniversity of TorontoOntarioCanada

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