Expression study of the hunchback ortholog in embryos of the onychophoran Euperipatoides rowelli
- 255 Downloads
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.
KeywordsArthropods “Gap gene” Hunchback Mesoderm Nervous system Onychophora
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.).
- Chang CC, Hsiao YM, Huang TY, Cook CE, Shigenobu S, Chang TH (2013) Noncanonical expression of caudal during early embryogenesis in the pea aphid Acyrthosiphon pisum: maternal cad-driven posterior development is not conserved. Insect Mol Biol 22:442–455. doi: 10.1111/imb.12035 PubMedCrossRefGoogle Scholar
- Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164−1165Google Scholar
- Franke FA, Mayer G (2014) Controversies surrounding segments and parasegments in Onychophora: insights from the expression patterns of four “segment polarity genes” in the peripatopsid Euperipatoides rowelli. PLoS ONE 9, e114383. doi: 10.1371/journal.pone.0114383 PubMedCentralPubMedCrossRefGoogle Scholar
- Hering L, Henze MJ, Kohler M, Kelber A, Bleidorn C, Leschke M, Nickel B, Meyer M, Kircher M, Sunnucks P, Mayer G (2012) Opsins in Onychophora (velvet worms) suggest a single origin and subsequent diversification of visual pigments in arthropods. Mol Biol Evol 29:3451–3458. doi: 10.1093/molbev/mss148 PubMedCrossRefGoogle Scholar
- Huang TY, Cook CE, Davis GK, Shigenobu S, Chen RPY, Chang CC (2010) Anterior development in the parthenogenetic and viviparous form of the pea aphid, Acyrthosiphon pisum: hunchback and orthodenticle expression. Insect Mol Biol 19:75–85. doi: 10.1111/j.1365-2583.2009.00940.x PubMedCrossRefGoogle Scholar
- Kambadur R, Koizumi K, Stivers C, Nagle J, Poole SJ, Odenwald WF (1998) Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev 12:246–260. doi: 10.1101/gad.12.2.246
- Kerner P, Zelada González F, Gouar M, Ledent V, Arendt D, Vervoort M (2006) The expression of a hunchback ortholog in the polychaete annelid Platynereis dumerilii suggests an ancestral role in mesoderm development and neurogenesis. Dev Genes Evol 216:821–828. doi: 10.1007/s00427-006-0100-9 PubMedCrossRefGoogle Scholar
- Kim HS, Murphy T, Xia J, Caragea D, Park Y, Beeman RW, Lorenzen MD, Butcher S, Manak JR, Brown SJ (2010) BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res 38:D437–D442. doi: 10.1093/nar/gkp807 PubMedCentralPubMedCrossRefGoogle Scholar
- Mayer G, Franke FA, Treffkorn S, Gross V, Oliveira IS (2015) Onychophora. In: Wanninger A (ed) Evolutionary developmental biology of invertebrates. Springer, Berlin, p 53–98 (in press)Google Scholar
- Savage RM, Shankland M (1996) Identification and characterization of a hunchback Orthologue, Lzf2, and its expression during leech embryogenesis. Dev Biol 175:205–217. doi: 10.1006/dbio.1996.0108
- Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the location of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85. doi: 10.1007/bf00291041