Skip to main content
Log in

Orthodenticle and empty spiracles genes are expressed in a segmental pattern in chelicerates

  • Original article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Members of the orthodenticle (otd/Otx) and empty spiracles (ems/Emx) gene families are head gap genes that encode homeodomain-containing DNA-binding proteins. Although numerous studies show their central role in developmental processes in brain specification, a surprisingly high number of other developmental processes have been shown to involve their expression. In this paper, we report the identification and expression of ems and otd in two chelicerate species: a scorpion, Euscorpius flavicaudis (Chactidae, Scorpiona, Arachnida, Euchelicerata) and a spider, Tegenaria saeva (Aranea, Arachnida, Euchelicerata). We show that both ems and otd are expressed not only in an anterior head domain but also along the entire anterior–posterior axis during embryonic development. The expression patterns for both genes are typically segmental and concern neurectodermal territories. During patterning of the opisthosoma, ems and otd are expressed in the lateral ectoderm just anterior to the limb bud primordia giving rise to respiratory organs and spinnerets (spider). This common pattern found in two divergent species thus appears to be a conserved character of chelicerates. These results are discussed in terms of evolutionary origin of respiratory organs and/or functional pathway recruitment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig.  6
Fig. 7

Similar content being viewed by others

References

  • Akiyama-Oda Y, Oda H (2003) Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development 130:1735–1757

    Article  PubMed  CAS  Google Scholar 

  • Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon, New York

    Google Scholar 

  • Brauer A (1895) Beiträge zur Kenntnis der Entwicklungsgeschichte des Skorpions, II. Z Wiss Zool 59:351–435

    Google Scholar 

  • Cohen SM, Jürgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482–485

    Article  PubMed  CAS  Google Scholar 

  • Cohen S, Jürgens G (1991) Drosophila headlines. Trends Genet 7:267–272

    PubMed  CAS  Google Scholar 

  • Dalton D, Chadwick R, McGinnis W (1989) Expression and embryonic function of empty spiracles: a Drosophila homeobox gene with two patterning functions on the anterior–posterior axis of the embryo. Genes Dev 3:1940–1956

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Damen WMG, Saridaki T, Averof M (2002) Diverse adaptations of an ancestral gill: a common evolutionary origin for wings, breathing organs, and spinnerets. Curr Biol 12:1711–1716

    Article  PubMed  CAS  Google Scholar 

  • Deutsch J (2004) Segments and parasegments in Arthropods: a functional perspective. Bioessays 26:1117–1125

    Article  PubMed  CAS  Google Scholar 

  • Dunlop JA (1996) Systematics of the fossils arachnids. Rev Suisse Zool Vol hors série 173–184

  • Ebner A, Kiefer FN, Ribeiro C, Petit V, Nussbaumer, Affolter M (2002) Tracheal development in Drosophila melanogaster as a model system for studying the development of a branched organ. Gene 287:55–66

    Article  PubMed  CAS  Google Scholar 

  • Farley RD (2001) Abdominal plates, spiracles and sternites in the ventral mesosoma of embryos of the desert scorpion Paructonus mesaensis (Scorpiones: Vaejovidae). Invertebr Reprod Dev 40:193–208

    Google Scholar 

  • Farley RD (2005) Developmental changes in the embryo, protonymph and first molt of the scorpion Centruroides vittatus (Scorpiones: Buthidae). J Morphol 265:1–27

    Article  PubMed  Google Scholar 

  • Finkelstein R, Perrimon N (1991) The molecular genetics of head development in Drosophila melanogaster. Development 112:899–912

    PubMed  CAS  Google Scholar 

  • Finkelstein R, Smouse D, Capaci TM, Spradling AC, Perrimon N (1990) The orthodenticle gene encodes a novel homeodomain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev 4:1516–1527

    PubMed  CAS  Google Scholar 

  • Galliot B, de Vargas C, Miller D (1999) Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class. Dev Genes Evol 209:186–197

    Article  PubMed  CAS  Google Scholar 

  • Gallitano-Mendel A, Finkelstein R (1998) Ectopic orthodenticle expression alters segment polarity gene expression but not head segment identity in the Drosophila embryo. Dev Biol 199:125–137

    Article  PubMed  CAS  Google Scholar 

  • Gauchat D, Mazet F, Berney C, Schummer M, Kreger S, Pawlowski J, Galliot B (2000) Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning. Proc Natl Acad Sci USA 97:4493–4498

    Article  PubMed  CAS  Google Scholar 

  • Gibert JM, Mouchel-Vielh E, Queinnec E, Deutsch JS (2000) Barnacle duplicate engrailed genes: divergent expression patterns and evidence for a vestigial abdomen. Evol Dev 2:194–202

    Article  PubMed  CAS  Google Scholar 

  • Grossniklaus U, Cadigan KM, Gehring WJ (1991) Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 120:3155–3171

    Google Scholar 

  • Hartmann B, Hirth F, Walldorf U, Reichert H (2000) Expression, regulation and function of the homeobox gene empty spiracles in brain and ventral nerve cord development of Drosophila. Mech Dev 90:143–153

    Article  PubMed  CAS  Google Scholar 

  • Hirth F, Therianos S, Loop T, Gehring WJ, Reichert H, Furukubo-Tokunaga K (1995) Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 15:769–778

    Article  PubMed  CAS  Google Scholar 

  • Hu N, Castelli-Gair J (1999) Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Dev Biol 214:197–210

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lall S, Patel NH (2001) Conservation and divergence in molecular mechanisms of axis formation. Annu Rev Genet 35:407–437

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Brown SJ, Hausdorf B, Tautz D, Denell RE, Finkelstein R (1996) Two orthodenticle-related genes in the short-germ beetle Tribolium castaneum. Dev Genes Evol 206:35–45

    Article  CAS  Google Scholar 

  • Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity 94:465–477

    Article  PubMed  CAS  Google Scholar 

  • Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C (2006) Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439:728–732

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Arias A, Lawrence PA (1985) Parasegments and compartments in the Drosophila embryo. Nature 313:639–642

    Article  PubMed  CAS  Google Scholar 

  • McClendon JF (1905) On the anatomy and embryology of the nervous system of the scorpion. Biol Bull 8:38–55

    Google Scholar 

  • Mittmann B, Scholtz G (2001) Distal-less expression in embryos of Limulus polyphemus (Chelicerata, Xiphosura) and Lepisma saccharina (Insecta, Zygentoma) suggests as role in the development of mechanoreceptors, chemoreceptors, and the CNS. Dev Genes Evol 211:232–243

    Article  PubMed  CAS  Google Scholar 

  • Müller P, Yanze N, Schmid V, Spring J (1999) The homeobox gene otx of the jellyfish Podocoryne carnea: role of a head gene in striated muscle and evolution. Dev Biol 216:582–594

    Article  PubMed  Google Scholar 

  • Root TM (1990) Neurobiology. In: Polis GA (ed) The biology of scorpions. Stanford University Press, Stanford, pp 341–413

    Google Scholar 

  • Royet J, Finkelstein R (1995) Pattern formation in Drosophila head development: the role of the orthodenticle homeobox gene. Development 121(11):3561–3572

    PubMed  CAS  Google Scholar 

  • Schimkewitsch W (1887) Etude sur le développement des araignées. Arch Biol 6:515–584

    Google Scholar 

  • Scholtz G, Kamenz C (2006) The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): evidence for homology and a single terrestrialisation event of a common arachnid ancestor. Zoology 109:2–13

    Article  PubMed  Google Scholar 

  • Schröder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422:621–625

    Article  PubMed  Google Scholar 

  • Simonnet F, Deutsch J, Quéinnec E (2004) hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev Genes Evol 214:537–545

    Article  PubMed  CAS  Google Scholar 

  • Stollewerk A (2002) Recruitment of cell groups through Delta/Notch signalling during spider neurogenesis. Development 129:5339–5348

    Article  PubMed  CAS  Google Scholar 

  • Stollewerk A, Weller M, Tautz D (2001) Neurogenesis in the spider Cupiennius salei. Development 128:2673–2688

    PubMed  CAS  Google Scholar 

  • Stollewerk A, Tautz D, Weller M (2003) Neurogenesis in the spider: new insights from comparative analysis of morphological processes and gene expression patterns. Arthropod Struct Dev 32:5–16

    Article  Google Scholar 

  • Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci U S A 95:10671–10675

    Article  PubMed  CAS  Google Scholar 

  • Walldorf L, Gehring WJ (1992) Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J 11:2247–2259

    PubMed  CAS  Google Scholar 

  • Weygoldt P, Paulus HF (1979) Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata. Z Zoolog Syst Evol-forsch 17:85–116, 177–200

    Google Scholar 

  • Wimmer EA, Cohen SM, Jackle H, Desplan C (1997) Buttonhead does not contribute to a combinatorial code proposed for Drosophila head development. Development 124:1509–1517

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are particularly grateful to Gerhard Scholtz for his thorough reading of the manuscript and for his constructive comments and suggestions. We are grateful to Roland Stockmann for providing scorpions and scanning electron micrographs and to Pierrette Lamarre and Murielle Jager for their technical help during this work. We thank Jason Dunlop for comments on a first draft of the paper and Jean Deutsch and Michael Manuel for critical reading of the manuscript. Many thanks to David Cribbs for help in English writing. We are indebted to the two referees for critically reading and mostly improving the manuscript. F.S. is the recipient of a Ph.D. fellowship from the Ministère de la Recherche et de la Technologie.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eric Quéinnec.

Additional information

Communicated by guest editors Jean Deutsch and Gerhard Scholtz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simonnet, F., Célérier, ML. & Quéinnec, E. Orthodenticle and empty spiracles genes are expressed in a segmental pattern in chelicerates. Dev Genes Evol 216, 467–480 (2006). https://doi.org/10.1007/s00427-006-0093-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-006-0093-4

Keywords

Navigation