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The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium

Nature volume 422, pages 621–625 (2003)Cite this article

Abstract

In Drosophila, the morphogen Bicoid organizes anterior patterning in a concentration-dependent manner by activating the transcription of target genes such as orthodenticle (otd)1 and hunchback (hb), and by repressing the translation of caudal2,3. Homologues of the bicoid gene have not been isolated in any organism apart from the higher Dipterans4,5,6,7. In fact, head and thorax formation in other insects is poorly understood. To elucidate this process in a short-germband insect, I analysed the function of the conserved genes orthodenticle-1 (otd-1) and hb in the flour beetle Tribolium castaneum. Here I show that, in contrast to Drosophila, Tribolium otd-1 messenger RNA is maternally inherited by the embryo. Reduction of Tribolium otd-1 levels by RNA interference (RNAi) results in headless embryos. This shows that otd-1 is required for anterior patterning in Tribolium. As in Drosophila, Tribolium hb specifies posterior gnathal and thoracic segments. The head, thorax and the anterior abdomen fail to develop in otd-1/hb double-RNAi embryos. This phenotype is similar to that of strong bicoid mutants in Drosophila. I propose that otd-1 and hb are part of an ancestral anterior patterning system.

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Figure 1: otd-1 expression during blastoderm formation in Tribolium.
Figure 2: Effect of otd-1RNAi on embryonic development.
Figure 3: Cuticle preparations of wild-type and RNAi embryos.
Figure 4: Engrailed staining of wild-type and RNAi embryos.

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References

  1. Gao, Q. & Finkelstein, R. Targeting gene expression to the head: the Drosophila orthodenticle gene is a direct target of the Bicoid morphogen. Development 125, 4185–4193 (1998)

    CAS  PubMed  Google Scholar 

  2. St Johnston, D. & Nüsslein-Volhard, C. The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–220 (1992)

    Article  CAS  Google Scholar 

  3. Lall, S. & Patel, N. H. Conservation and divergence in molecular mechanisms of axis formation. Annu. Rev. Genet. 35, 407–437 (2001)

    Article  CAS  Google Scholar 

  4. Sommer, R. & Tautz, D. Segmentation gene expression in the housefly Musca domestica. Development 113, 419–430 (1991)

    CAS  PubMed  Google Scholar 

  5. Schröder, R. & Sander, K. A comparison of transplantable bicoid activity and partial bicoid homeobox sequences in several Drosophila and blowfly species (Calliphoridae). Wilhelm Roux Arch. Dev. Biol., 203, 34–43 (1993)

    Article  Google Scholar 

  6. Stauber, M., Jäckle, H. & Schmidt-Ott, U. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc. Natl Acad. Sci. USA 96, 3786–3789 (1999)

    Article  ADS  CAS  Google Scholar 

  7. Brown, S. J. et al. A strategy for mapping bicoid on the phylogenetic tree. Curr. Biol. 11, R43–R44 (2001)

    Article  CAS  Google Scholar 

  8. Dubnau, J. & Struhl, G. RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694–699 (1996)

    Article  ADS  CAS  Google Scholar 

  9. Rivera-Pomar, R., Niessing, D., Schmidt-Ott, U., Gehring, W. J. & Jäckle, H. RNA binding and translational suppression by bicoid. Nature 379, 746–749 (1996)

    Article  ADS  CAS  Google Scholar 

  10. Simpson-Brose, M., Treisman, J. & Desplan, C. Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78, 855–865 (1994)

    Article  CAS  Google Scholar 

  11. Dearden, P. & Akam, M. Axial patterning in insects. Curr. Biol. 9, R591–R594 (1999)

    Article  CAS  Google Scholar 

  12. Wimmer, E., Carleton, A., Harjes, P., Turner, T. & Desplan, C. bicoid-independent formation of thoracic segments in Drosophila. Science 287, 2476–2479 (2000)

    Article  ADS  CAS  Google Scholar 

  13. Tautz, D., Friedrich, M. & Schröder, R. Insect embryogenesis—what is ancestral and what is derived? Development, (Suppl.), 193–199 (1994)

    Google Scholar 

  14. Cohen, S. & Jürgens, G. Drosophila headlines. Trends Genet. 7, 267–272 (1991)

    Article  CAS  Google Scholar 

  15. Li, Y. et al. Two orthodenticle-related genes in the short-germ beetle Tribolium castaneum. Dev. Genes Evol. 206, 35–45 (1996)

    Article  CAS  Google Scholar 

  16. Brown, S. J., Mahaffey, J., Lorenzen, M., Denell, R. & Mahaffey, J. Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evol. Dev. 1, 11–15 (1999)

    Article  CAS  Google Scholar 

  17. Bucher, G., Scholten, J. & Klingler, M. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85–R86 (2002)

    Article  CAS  Google Scholar 

  18. Frohnhöfer, H. G. & Nüsslein-Volhard, C. Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324, 120–125 (1986)

    Article  ADS  Google Scholar 

  19. Wolff, C., Sommer, R., Schröder, R., Glaser, G. & Tautz, D. Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121, 4227–4236 (1995)

    CAS  PubMed  Google Scholar 

  20. Falciani, F. et al. Class 3 Hox genes in insects and the origin of zen. Proc. Natl Acad. Sci. USA 93, 8479–8484 (1996)

    Article  ADS  CAS  Google Scholar 

  21. Lehmann, R. & Nüsslein-Volhard, C. hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo. Dev. Biol. 119, 402–417 (1987)

    Article  CAS  Google Scholar 

  22. Pultz, M., Pitt, J. & Alto, N. Extensive zygotic control of the anteroposterior axis in the wasp Nasonia vitripennis. Development 126, 701–710 (1999)

    CAS  PubMed  Google Scholar 

  23. Niessing, D. et al. Homeodomain position 54 specifies transcriptional versus translational control by Bicoid. Mol. Cell 5, 395–401 (2000)

    Article  CAS  Google Scholar 

  24. Draper, B. W., Mello, C. C., Bowerman, B., Hardin, J. & Priess, J. R. MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87, 205–216 (1996)

    Article  CAS  Google Scholar 

  25. Isaacs, H., Andreazzoli, M. & Slack, J. Anteroposterior patterning by mutual repression of orthodenticle and caudal-type transcription factors. Evol. Dev. 1, 143–152 (1999)

    Article  CAS  Google Scholar 

  26. Gamberi, C., Peterson, D. S., He, L. & Gottlieb, E. An anterior function for the Drosophila posterior determinant Pumilio. Development 129, 2699–2710 (2002)

    CAS  PubMed  Google Scholar 

  27. Lall, S., Ludwig, M. Z. & Patel, N. H. nanos plays a conserved role in axial patterning outside of the Diptera. Curr. Biol. 13, 224–229 (2003)

    Article  CAS  Google Scholar 

  28. Patel, N. et al. Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128, 3459–3472 (2001)

    CAS  PubMed  Google Scholar 

  29. Stauber, M., Prell, A. & Schmidt-Ott, U. A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc. Natl Acad. Sci. USA 99, 274–279 (2002)

    Article  ADS  CAS  Google Scholar 

  30. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811 (1998)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

I thank T. Mader for excellent technical assistance, A. Beermann, H. Dove, F. Maderspacher, R. Reuter and C. Wolff for critically reading drafts of the manuscript, E. A. Wimmer for discussions and for pointing out the existence of an NRE site in the otd-1 sequence, and the Deutsche Forschungsgemeinschaft for financial support.

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  1. Interfakultäres Institut für Zellbiologie, Universität Tübingen, Abt. Genetik der Tiere, Auf der Morgenstelle 28, 72076, Tübingen, Germany

    Reinhard Schröder

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Correspondence to Reinhard Schröder.

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Schröder, R. The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422, 621–625 (2003). https://doi.org/10.1038/nature01536

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