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

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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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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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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