Abstract
The correlation between dorsal and ventral segmental units in diplopod myriapods is complex and disputed. Recent results with engrailed (en), hedgehog (hh), wingless (wg), and cubitus-interruptus (ci) have shown that the dorsal segments are patterned differently from the ventral segments. Ventrally, gene expression is compatible with the classical autoregulatory loop known from Drosophila to specify the parasegment boundary. In the dorsal segments, however, this Wg/Hh autoregulatory loop cannot be present because the observed gene expression patterns argue against the involvement of Wg signalling. In this paper, we present further evidence against an involvement of Wg signalling in dorsal segmentation and propose a hypothesis about how dorsal segmental boundaries may be controlled in a wg-independent way. We find that (1) the Notum gene, a modulator of the Wg gradient in Drosophila, is not expressed in the dorsal segments. (2) The H15/midline gene, a repressor of Wg action in Drosophila, is not expressed in the dorsal segments, except for future heart tissue. (3) The patched (ptc) gene, which encodes a Hh receptor, is strongly expressed in the dorsal segments, which is incompatible with Wg-Hh autoregulation. The available data suggest that anterior–posterior (AP) boundary formation in dorsal segments could instead rely on Dpp signalling rather than Wg signalling. We present a hypothesis that relies on Hh-mediated activation of Dpp signalling and optomotor-blind (omb) expression to establish the dorsal AP boundary (the future tergite boundary). The proposed mechanism is similar to the mechanism used to establish the AP boundary in Drosophila wings and ventral pleura.
Similar content being viewed by others
References
Baeg GH, Lin X, Khare N, Baumgartner S, Perrimon N (2001) Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128:87–94
Budd GE (2001) Why are arthropods segmented? Evol Dev 3:132–142
Buescher M, Svendsen PC, Tio M, Miskolczi-McCallum C, Tear G, Brook WJ, Chia W (2004) Drosophila T box proteins break the symmetry of Hedgehog-dependent activation of wingless. Curr Biol 14:1694–1702
Damen WGM (2002) Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129:1239–1250
Damen WGM (2007) Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 236:1379–1391
DiNardo S, O’Farrell PH (1987) Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes. Genes and Dev 1:1212–1225
Dohle W (1964) Die Embryonalentwicklung von Glomeris marginata (Villers) im Vergleich zur Entwicklung anderer Diplopoden. Zool Jahrb Anat 81:241–310
Dohle W (1974) The segmentation of the germ band of Diplopoda compared with other classes of arthropods. Symp Zool Soc London 32:143–161
Forbes AJ, Nakano Y, Taylor AM, Ingham PW (1993) Genetic analysis of hedgehog signalling in the Drosophila embryo. Dev Suppl:115–124
Franch-Marro X, Marchand O, Piddini E, Ricardo S, Alexandre C, Vincent JP (2005) Glypicans shunt the Wingless signal between local signalling and further transport. Development 132:659–666
Gerlitz O, Basler K (2002) Wingful, an extracellular feedback inhibitor of Wingless. Genes Dev 16:1055–1059
Giraldez AJ, Copley RR, Cohen SM (2002) HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev Cell 2:667–676
Hidalgo A, Ingham P (1990) Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development 110:291–301
Hooper J, Scott MP (1989) The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59:751–765
Howard K, Ingham PW (1986) Regulatory interactions between the segmentation genes fushi-tarazu, hairy, and engrailed in the Drosophila blastoderm. Cell 44:949–957
Hughes CL, Kaufman TC (2002) Exploring myriapod segmentation: The expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev Biol 247:47–61
Ingham PW, Baker NE, Martinez-Arias A (1988) Regulation of segment polarity genes in the Drosophila blastoderm by fushi-tarazu and even-skipped. Nature 331:73–75
Janssen R, Prpic N-M, Damen WGM (2004) Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 268:89–114
Janssen R, Prpic N-M, Damen WGM (2006a) Dorso-ventral differences in gene expression in Glomeris marginata Villers, 1789 (Myriapoda: Diplopoda). Norw J Entomol 53:129–137
Janssen R, Prpic N-M, Damen WGM (2006b) A review of the correlation of tergites, sternites, and leg pairs in diplopods. Frontiers in Zoology 3:2
Lawrence PA, Casal J, Struhl G (2002) Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. Development 129:2749–2760
Minelli A, Fusco G (2004) Evo–devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19:423–429
Nakano Y, Guerrero I, Hidalgo A, Taylor AM, Whittle JRS, Ingham PW (1989) The Drosophila segment polarity gene patched encodes a protein with multiple potential membrane spanning domains. Nature 341:508–513
Nielsen C, Martinez P (2003) Patterns of gene expression: homology or homocracy? Dev Genes Evol 213:149–154
Prpic N-M (2004) Homologs of wingless and decapentaplegic display a complex and dynamic expression profile during appendage development in the millipede Glomeris marginata (Myriapoda: Diplopoda). Frontiers in Zoology 1:6
Prpic N-M, Damen WGM (2005) A homolog of the hydrolase Notum is expressed during segmentation and appendage formation in the Central American hunting spider Cupiennius salei. Naturwissenschaften 92:246–249
Prpic N-M, Tautz D (2003) The expression of the proximodistal axis patterning genes Distal-less and dachshund in the appendages of Glomeris marginata (Myriapoda: Diplopoda) suggests a special role of these genes in patterning the head appendages. Dev Biol 260:97–112
Prpic N-M, Janssen R, Damen WGM, Tautz D (2005) Evolution of dorsal-ventral axis formation in arthropod appendages: H15 and optomotor-blind/bifid-type T-box genes in the millipede Glomeris marginata (Myriapoda: Diplopoda). Evol Dev 7:51–57
Sanson B (2001) Generating patterns from fields of cells: examples from Drosophila segmentation. EMBO Reports 2:1083–1088
Shen J, Dahmann C (2005) The role of Dpp signalling in maintaining the Drosophila anteroposterior compartment boundary. Dev Biol 279:31–43
Siegfried E, Perrimon N (1994) Drosophila Wingless: a paradigm for the function and mechanism of Wnt signaling. Bioessays 16:395–404
Strigini M, Cohen SM (2000) Wingless gradient formation in the Drosophila wing. Curr Biol 10:293–300
Acknowledgements
We would like to thank Diethard Tautz for continuous support and Wolfgang Dohle, Alessandro Minelli and Bjarne Meidell for stimulating discussions on Glomeris segmentation. This work was mainly supported by the European Union via the Marie Curie Research and Training Network ZOONET (MRTN-CT-2004-005624). The work of G.E.B. was supported by the Swedish Research Council (VR) and the Swedish Royal Academy of Sciences (KVA). The work of W.G.M.D. was supported by the German Research Foundation (DFG) via SFB 572 of the University of Cologne. The work of N.M.P. was supported by a grant from the German Research Foundation (DFG grant PR 1109/1-1).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Roth
Rights and permissions
About this article
Cite this article
Janssen, R., Budd, G.E., Damen, W.G.M. et al. Evidence for Wg-independent tergite boundary formation in the millipede Glomeris marginata . Dev Genes Evol 218, 361–370 (2008). https://doi.org/10.1007/s00427-008-0231-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-008-0231-2