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The ten Hox genes of the millipede Glomeris marginata

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Abstract

We have isolated the ten Hox genes from the pill millipede Glomeris marginata (Myriapoda:Diplopoda). All ten genes are expressed in characteristic Hox-gene-like expression patterns. The register of Hox gene expression borders is conserved and the expression profiles show that the anterior-most limb-bearing segment in arthropods (antennal/cheliceral segment) does not express any Hox gene, while the next segment (intercalary/second-antennal/premandibular/pedipalpal segment) does express Hox genes. The Hox expression patterns in this millipede thus support the conclusion that all arthropods possess a deuterocerebral segment. We find that there is an apparent posterior shift of Hox gene expression domains dorsally relative to their ventral patterns, indicating that the decoupling of dorsal and ventral segmentation is not restricted to the level of segment polarity genes but apparently includes the Hox genes. Although the mechanism for the decoupling of dorsal and ventral segmentation remains unsolved, the decoupling must be at a level higher in the hierarchy than that of the segment polarity and Hox genes. The expression patterns of Ultrabithorax and abdominal-A suggest a correlation between the function of these genes and the delayed outgrowth of posterior trunk appendages. This delay may be caused by an assumed repressor function of Ultrabithorax, which might partially repress the activation of the Distal-less gene. The Glomeris fushi tarazu gene is expressed in a Hox-like domain and in the developing central nervous system, but not in segmental stripes such as has been reported in another myriapod species, the centipede Lithobius. In contrast to the Lithobius fushi tarazu gene, there is no indication for a role in segment formation for the millipede fushi tarazu gene, suggesting that fushi tarazu first acquired its segmentation function in the lineage of the insects.

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Acknowledgements

We would like to thank Jean Deutsch and Michel Veuille for the invitation to communicate our work on the Development and Phylogeny of Arthropods meeting in Paris (France) from September 23–24, 2005, and for the opportunity of publication in this journal. We thank Diethard Tautz for his continuous support of our work and Nikola-Michael Prpic for many discussions and critical reading of the manuscript. We also thank Hilary Dove for providing the Glomeris rapid amplification of cDNA ends template. This work was supported in part by the Deutsche Forschungsgemeinschaft via Sonderforschungsbereich 572 of the University of Cologne and by the European Union via the Marie Curie Research and Training Network ZOONET (MRTN-CT-2004-005624).

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  1. Ralf Janssen

    Present address: Department of Earth Sciences, Palaeobiology, Uppsala University, Norbyvägen 22, SE-752 36, Uppsala, Sweden

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  1. Institute for Genetics, Department for Evolutionary Genetics, University of Cologne, Zülpicher Straße 47, D-50674, Köln, Germany

    Ralf Janssen & Wim G. M. Damen

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  1. Ralf Janssen
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Correspondence to Wim G. M. Damen.

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Communicated by guest editors Jean Deutsch and Gerhard Scholtz

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Fig. S1

Glomeris Hox gene sequences. a The partial homeodomain including the C-terminal flanking region of the G. marginata genes is aligned to other Hox gene orthologs of various arthropods, including the fruit fly D. melanogaster (Dm), the spider Cupiennius salei (Cs), and the centipede L. atkinsoni (La). Asterisks above the sequence indicate conserved amino acid positions. The lower case letters (elekef) in some of the Glomeris and Lithobius sequences indicate that these amino acids (aa) are derived from the primer sequences. A bold asterisk at the end of a sequence indicates the position of the stop codon, dots indicate that there are more sequences that are not included in the alignment. The dash (-) in the Gm-Abd-B sequence represents a gap that has been introduced to get a better alignment. b The complete homeodomain including the N-terminal flanking region of the G. marginata ftz gene is aligned to other ftz gene orthologs of other arthropods, a tardigrate, and an onychophoran. Conserved aa of the hexapeptide motif (YPWM) are highlighted in green, conserved aa of the YxD domain located between hexapeptide and homeodomain are shown in blue. Diagnostic aa within the homeodomain are highlighted in red. The dashes (-) represent gaps that have been introduced to get a better alignment. Aligned are the ftz sequences of the species as in a, and in addition, sequences of the centipede Ethmostigmus rubripes (Er), the mite Archegozetes longisetosus (Al), the cirripede Sacculina carcini (Sc), the beetle Tribolium castaneum (Tc), the grasshopper Schistocerca gregaria (Sg) (all arthropods), the onychophoran Acanthokara kaputensis (Ak), and the tardigrade Milnesium tardigradum (Mt) (GIF 11 kb)

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Janssen, R., Damen, W.G.M. The ten Hox genes of the millipede Glomeris marginata . Dev Genes Evol 216, 451–465 (2006). https://doi.org/10.1007/s00427-006-0092-5

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