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Expression study of the hunchback ortholog in embryos of the onychophoran Euperipatoides rowelli

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Abstract

Zinc finger transcription factors encoded by hunchback homologs play different roles in arthropods, including maternally mediated control, segmentation, and mesoderm and neural development. Knockdown experiments in spider and insect embryos have also revealed homeotic effects and gap phenotypes, the latter indicating a function of hunchback as a “gap gene”. Although the expression pattern of hunchback has been analysed in representatives of all four major arthropod groups (chelicerates, myriapods, crustaceans and insects), nothing is known about its expression in one of the closest arthropod relatives, the Onychophora (velvet worms). We therefore examined the expression pattern of hunchback in embryos of the onychophoran Euperipatoides rowelli. Our transcriptomic and phylogenetic analyses revealed only one hunchback ortholog in this species. The putative Hunchback protein contains all nine zinc finger domains known from other protostomes. We found no indication of maternally contributed transcripts of hunchback in early embryos of E. rowelli. Its initial expression occurs in the ectodermal tissue of the antennal segment, followed by the jaw, slime papilla and trunk segments in an anterior-to-posterior progression. Later, hunchback expression is seen in the mesoderm of the developing limbs. A second “wave” of expression commences later in development in the antennal segment and continues posteriorly along each developing nerve cord. This expression is restricted to the neural tissues and does not show any segmental pattern. These findings are in line with the ancestral roles of hunchback in mesoderm and neural development, whereas we find no evidence for a putative function of hunchback as a “gap gene” in Onychophora.

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Acknowledgments

We are thankful to the members of the Mayer laboratory for animal husbandry. We acknowledge Dave M. Rowell, Ivo de Sena Oliveira, Sandra Treffkorn and Michael Gerth for collecting specimens and to Noel N. Tait for his help with permits. We thank Lars Hering for providing transcriptomic data, Nicole Naumann and Isabell Schumann for laboratory support, Lars Hering and Michael Gerth for help with software applications, and Vladimir Gross for proofreading the manuscript and providing useful comments. The staff of Forests NSW (New South Wales, Australia) is gratefully acknowledged for providing the collecting permits. We thank the two anonymous reviewers for their helpful comments. This work was supported by the Emmy Noether Programme of the German Research Foundation (DFG; grant Ma 4147/3-1 to G.M.).

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  1. Animal Evolution & Development, Institute of Biology, University of Leipzig, Talstraße 33, D-04103, Leipzig, Germany

    Franziska Anni Franke & Georg Mayer

  2. Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, D-34132, Kassel, Germany

    Georg Mayer

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  1. Franziska Anni Franke
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Franke, F.A., Mayer, G. Expression study of the hunchback ortholog in embryos of the onychophoran Euperipatoides rowelli . Dev Genes Evol 225, 207–219 (2015). https://doi.org/10.1007/s00427-015-0505-4

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