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The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996)

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Abstract

As the putative sister group to the arthropods, onychophorans can provide insight into ancestral developmental mechanisms in the panarthropod clade. Here, we examine the expression during segmentation of orthologues of wingless (Wnt1) and engrailed, two genes that play a key role in defining segment boundaries in Drosophila and that appear to play a role in segmentation in many other arthropods. Both are expressed in segmentally reiterated stripes in all forming segments except the first (brain) segment, which only shows an engrailed stripe. Engrailed is expressed before segments are morphologically visible and is expressed in both mesoderm and ectoderm. Segmental wingless expression is not detectable until after mesodermal somites are clearly distinct. Early engrailed expression lies in and extends to both sides of the furrow that first demarcates segments in the ectoderm, but is largely restricted to the posterior part of somites. Wingless expression lies immediately anterior to engrailed expression, as it does in many arthropods, but there is no precise cellular boundary between the two expression domains analogous to the overt parasegment boundary seen in Drosophila. Engrailed stripes extend along the posterior part of each limb bud, including the antenna, while wingless is restricted to the distal tip of the limbs and the neurectoderm basal to the limbs.

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Acknowledgments

We thank Jean Joss (Sydney) for providing lab space during the collecting trip and Gerhard Scholtz (Berlin) for comments on the manuscript. Wim Damen is thanked for contributing with the Wnt tree in the supplementary information. This work was supported by the Marie Curie “Zoonet” training network and an EMBO short-term fellowship for BJE.

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  1. Bo Joakim Eriksson

    Present address: School of Biological and Chemical Sciences, Queen Mary, University of London, Mile End Road, London, E1 4NS, , UK

Authors and Affiliations

  1. Department of Zoology, University Museum of Zoology, Downing Street, Cambridge, CB2 3EJ, UK

    Bo Joakim Eriksson & Michael Akam

  2. Department of Earth Sciences, Uppsala University, Villavägen 16, 752 36, Uppsala, Sweden

    Graham E. Budd

  3. Department of Biological Sciences, Macquarie University, Sydney, 2109, NSW, Australia

    Noel N. Tait

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  1. Bo Joakim Eriksson
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Correspondence to Bo Joakim Eriksson.

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Supplementary data 1

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Fig. S2

Cloned regions of the E. kanangrensis engrailed and wingless genes. a Sequence of E. kanangrensis engrailed cDNA. The 5′ untranslated region is shown with nucleotide symbols, in small italics. The protein coding region is shown in single letter amino acid code, coloured to denote the five conserved Engrailed homology regions EH1–EH5. b Partial amino acid sequence of E. kanangrensis Wingless protein. The conserved Wnt1 domain is shown in red; cysteine residues are shown in blue. A potential palmitoylation site is underlined. Stars delimit the regions of the sequences used as probes for in situ hybridisation. (GIF 94 kb)

High resolution image (TIFF 5871 kb)

Fig. S3

Phylogenetic analysis of wnt genes. The unrooted cladogram is computed from 1,000 intermediate trees produced with the Quartet Puzzling method (Strimmer and von Haeseler 1996) as implemented in PAUP*4.0 (Swofford 2002). Wnt1 sequences are highlighted in red, Eka-Wingless sequence branches with the other Wnt1 genes. Species abbreviations: At, Achaearanea tepidariorum; Cs, Cupiennius salei; Dm, Drosophila melanogaster; Eka, Euperipatoides kanangrensis; Tc, Tribolium castaneum; Hs, Homo sapiens; Sp, Strongylocentrotus purpuratus. Strimmer, K., and von Haeseler, A. 1996. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13: 964-969. Swofford, D.L. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland Massachusetts. (GIF 35 kb)

High resolution image (TIFF 321 kb)

Fig. S4

Stained embryos of E. kanangrensis. Whole mount of a stage V embryo hybridised with a probe directed towards engrailed. Posteriorly, engrailed expression still persists in the neuroectoderm (right arrow) whereas anteriorly, expression is to a large extent confined to the ventral nerve cord (left arrow) and the limb buds. Scale bar 1 mm. (GIF 368 kb)

High resolution image (TIFF 2034 kb)

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Eriksson, B.J., Tait, N.N., Budd, G.E. et al. The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996). Dev Genes Evol 219, 249–264 (2009). https://doi.org/10.1007/s00427-009-0287-7

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