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Caudal is the Hox gene that specifies the most posterior Drosophile segment

Abstract

The homeobox gene caudal (cad) has a maternal embryonic function that establishes the antero–posterior body axis of Drosophila1,2. It also has a conserved2,4 late embryonic and imaginal function1 related to the development of the posterior body region. Here we report the developmental role of cad in adult Drosophila. It is required for the normal development of the analia structures, which derive from the most posterior body segment. In the absence of cad function, the analia develop like the immediately anterior segment (male genitalia), following the transformation rule of the canonical Hox genes5. We also show that cad can induce ectopic analia development if expressed in the head or wing. We propose that cad is the Hox gene that determines the development of the fly's most posterior segment. cad acts in combination with the Hedgehog (Hh) pathway6 to specify the different components of the analia: the activities of cad and of the Hh pathway induce Distal-less expression that, together with cad, promote external analia development. In the absence of the Hh pathway, cad induces internal analia development, probably by activating the brachyenteron and even-skipped genes.

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Figure 1: Analia subdomains in adult derivatives and imaginal discs.
Figure 2: Homeotic transformations of cad clones.
Figure 3: Ectopic cad expression.
Figure 4: The Hh pathway in the analia primordium.
Figure 5: Interactions between cad and the Hh pathway.

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References

  1. Macdonald, P. & Struhl, B. Amolecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324, 537–545 (1986).

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Mlodzik, M., Fjose, A. & Gehring, W. J. Isolation of caudal, a Drosophila homeobox-containing gene with maternal expression, whose transcription forms a concentration gradient at the pre-blastoderm stage. EMBO J. 4, 2961–2969 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hunter, C. P. & Kenyon, C. Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87, 217–226 (1997).

    Article  Google Scholar 

  4. Brooke, N. M., Garcia-Fernandez, J. & Holland, P. W. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392, 920–922 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

  5. McGinnis, W. & Krumlauf, R. Homeobox genes and axial patterning. Cell 68, 283–302 (1992).

    Article  CAS  PubMed  Google Scholar 

  6. Basler, K. & Struhl, G. Compartment boundaries and the control of Drosophila limb pattern by Hedgehog protein. Nature 368, 208–214 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Wu, L. H. & Lengyel, J. A. Role of caudal in the hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125, 2433–2442 (1996).

    Google Scholar 

  8. Calleja, M., Moreno, E., Pelaz, S. & Morata, G. Visualization of gene expression in living adult Drosophila. Science 274, 252–255 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Casares, F., Sanchez, L., Guerrero, I. & Sanchez-Herrero, E. The genital disc of Drosophila melanogaster. I. Segmental and compartmental organization. Dev. Genes Evol. 207, 216–228 (1997).

    Article  CAS  PubMed  Google Scholar 

  10. Nöthiger, R., Dübendorfer, A. & Epper, F. Gynandromorphs reveal two separate primordia for male and female genitalia in Drosophila melanogaster. Wilhelm Roux Arch. Dev. Biol. 181, 367–373 (1977).

    Article  Google Scholar 

  11. Epper, F. Three-dimensional fate map of the female genital disc of Drosophila melanogaster. Wilhelm Roux Arch. Dev. Biol. 192, 270–274 (1983).

    Article  Google Scholar 

  12. Cohen, S. M., Broner, G., Kuntter, F., Jurgens, G. & Jackle, H. Distal-less encodes a homeodomain protein required for limb development in Drosophila. Nature 338, 432–434 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Frasch, M., Hoey, T., Rushlow, C., Doyle, H. & Levines, M. Characterization localization of the even-skipped protein of Drosophila. EMBO J. 6, 749–759 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kispert, A., Herrmann, B. G., Leptin, M. & Reuter, R. Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta. Genes Dev. 8, 2137–2150 (1994).

    Article  CAS  PubMed  Google Scholar 

  15. Singer, J. B., Harbecke, R., Kusch, T., Reuter, R. & Lengyel, J. A. Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development 122, 3703–3718 (1996).

    Google Scholar 

  16. Nusslein-Volhard, C., Kluding, H. & Jurgens, G. Genes affecting the segmental subdivisions of the Drosophila embryo. Cold Spring Harb. Symp. Quant. Biol. 50, 145–154 (1985).

    Article  CAS  PubMed  Google Scholar 

  17. Sanchez-Herrero, E., Vernos, I., Marco, R. & Morata, G. Genetic organization of the Drosophila bithorax complex. Nature 313, 108–113 (1985).

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Lecuit, T. & Cohen, S. M. Proximal–distal axis formation in the Drosophila leg. Nature 388, 139–145 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).

    CAS  PubMed  Google Scholar 

  20. Diaz-Benjumea, F. J., Cohen, B. & Cohen, S. M. Cell interaction between compartments establishes the proximal–distal axis of Drosophila legs. Nature 372, 175–179 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Alexandre, C., Jacinto, A. & Ingham, P. W. Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the Cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 10, 2003–2013 (1996).

    Article  CAS  PubMed  Google Scholar 

  22. van den Heuvel, M. & Ingham, P. W. smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382, 547–551 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Chawengsaksophak, K., James, R., Hammond, V. E., Kontgen, F. & Beck, F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 396, 84–87 (1997).

    Article  ADS  Google Scholar 

  24. Miller, D. J. & Miles, A. Homeobox genes and the zootype. Nature 365, 215–216 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Sánchez, L. Casares, F., Gorfinkiel, N. & Guerrero, I. The genital disc of Drosophila melanogaster. II. Role of the genes hedgehog, decapentaplegic and wingless. Dev. Genes Evol. 207, 229–241 (1997).

    Article  PubMed  Google Scholar 

  26. Murakami, R. et al. aproctous, a locus that is necessary for the development of the proctodeum in Drosophila embryos, encodes a homolog of the vertebrate Brachyury gene. Wilhelm Roux Arch. Dev. Biol. 205, 89–96 (1995).

    Article  CAS  Google Scholar 

  27. Gorfinkiel, N., Morata, G. & Guerrero, I. The homeobox gene Distal-less induces ventral appendage development in Drosophila. Genes Dev. 11, 2259–2271 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Diaz-Benjumea, F. & Cohen, S. M. Serrate signals through Notch to establish a wingless-dependent organizer at the dorsal-ventral compartment boundary of the Drosophila wing. Development 121, 4215–4225 (1995).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank P. Fernandez, T. Kusch, C. Parras, R. Rivera, I. Rodriguez and G. Struhl for antibodies, cDNAs and fly stocks; J. Casanova and E. Sanchez-Herrero for comments on the manuscript; S. Gonzalez for helping with the DNA injections; and R. Gonzalez and J. M. Galán for their technical help. This work was supported by grants from the Dirección General de Investigación Cientifica y Técnica and from the Human Frontier Science Program. An institutional grant from the Fundacion Ramon Areces to the Centro de Biologia Molecular is also acknowledged. E.M. is supported by a scholarship from the Comunidad Autónoma de Madrid.

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Correspondence to Ginés Morata.

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Moreno, E., Morata, G. Caudal is the Hox gene that specifies the most posterior Drosophile segment. Nature 400, 873–877 (1999). https://doi.org/10.1038/23709

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