Skip to main content
SpringerLink
Log in

Characterisation of an amphioxus Fringe gene and the evolution of the vertebrate segmentation clock

  • Short Communication
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

In mouse and chick embryos, cyclic expression of lunatic fringe has an important role in the regulation of mesoderm segmentation. We have isolated a Fringe gene from the protochordate amphioxus. Amphioxus is the closest living relative of the vertebrates, and has mesoderm that is definitively segmented in a manner that is similar to, and probably homologous with, that of vertebrates. AmphiFringe is placed basal to vertebrate Fringe genes in molecular phylogenetic analyses, indicating that the duplications that formed radical-, manic- and lunatic fringe are specific to the vertebrate lineage. AmphiFringe expression was detected in the anterior neural plate of early neurulae, where it resolved into a series of segmental patches by the mid-neurulae stage. No AmphiFringe transcripts were detected in the mesoderm. Based on these observations, we propose a model depicting a successive recruitment of Fringe in the maintenance then regulation of segmentation during vertebrate evolution.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3A–F.

References

  • Aulehla A, Johnson RA (1999) Dynamic expression of lunatic fringe suggests a link between Notch signalling and an autonomous cellular oscillator driving somite segmentation. Dev Biol 207:49–61

    CAS  Google Scholar 

  • Bruckner K, Perez L, Clausen H, Cohen S (2000) Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406:411–415

    CAS  Google Scholar 

  • Cole SE, Levorse JM, Tilghman SM, Vogt TF (2002) Clock regulatory elements control cyclic expression of lunatic fringe during somitogenesis. Dev Cell 3:75–84

    CAS  Google Scholar 

  • Dale JK, Maroto M, Dequeant ML, Malapert P, McGrew M, Pourquie O (2003) Periodic Notch inhibition by Lunatic fringe underlies the chick segmentation clock. Nature 421:275–278

    CAS  Google Scholar 

  • Damas H (1944) Recherches sur le dévelopement de Lampetra Fluviatilis. Contribution à l'étude de la céphalogenèse des vertébrés. Arch Biol 55:1-291

    Google Scholar 

  • Dearden P, Akam M (2000) A role for Fringe in segment morphogenesis but not segment formation in the grasshopper, Schistocerca gregaria. Dev Genes Evol 210:329–336

    CAS  Google Scholar 

  • Evrard YA, Lun Y, Aulehla A, Gan L, Johnson RL (1998) Lunatic fringe is an essential mediator of somite segmentation and patterning. Nature 394:377–381

    CAS  Google Scholar 

  • Forsberg H, Crozet F, Brown NA (1998) Waves of mouse lunatic fringe expression, in four-hour cycles at two-hour intervals, precede somite boundary formation. Curr Biol 8:1027–1030

    CAS  Google Scholar 

  • Hatschek B (1881) Entwicklung des amphioxus. Arb Zool Inst Wien IV: 1–88

    Google Scholar 

  • Holland ND, Holland LZ (1993) Embryos and larvae of invertebrate deuterostomes. In: Stern CD , Holland PWH (eds) Essential developmental biology: a practical approach. IRL Press at Oxford University Press, Oxford, pp. 21–32

  • Holland LZ, Abi Rached L, Tamme R, Holland ND, Inoko H, Shiina T, Burgtorf C, Lardelli M (2001) Characterization and developmental expression of the amphioxus homolog of Notch (AmphiNotch): evolutionary conservation of multiple expression domains in amphioxus and vertebrates. Dev Biol 232:493–507

    CAS  Google Scholar 

  • Irvine KD, Wieschaus E (1994) Fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79:595–606

    CAS  Google Scholar 

  • Johnston SH, Rauskolb C, Wilson R, Prabhakaran B, Irvine KD, Vogt TF (1997) A family of mammalian Fringe genes implicated in boundary determination and the Notch pathway. Development 124:2245–2254

    CAS  Google Scholar 

  • Langeland JA, Tomsa JM, Jackman WR, Kimmel CB (1998) An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the vertebrate embryo. Dev Genes Evol 208:569–577

    CAS  PubMed  Google Scholar 

  • Leve C, Gajewski M, Rohr KB, Tautz D (2001) Homologues of c-hairy1 (her9) and lunatic fringe in zebrafish are expressed in the developing central nervous system, but not in the presomitic mesoderm. Dev Genes Evol 211:493–500

    CAS  Google Scholar 

  • Mazet F, Shimeld SM (2002) The evolution of chordate neural segmentation. Dev Biol 251:258–270

    CAS  Google Scholar 

  • Moloney DJ, Panin VM, Johnston SH, Chen J, Shao L, Wilson R, Wang Y, Stanley P, Irvine KD, Haltiwanger RS, Vogt TF (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406:369–375

    CAS  Google Scholar 

  • Pourquie O (2001) Vertebrate somitogenesis. Annu Rev Cell Dev Biol 17:311–350

    CAS  Google Scholar 

  • Prince VE, Holley SA, Bally-Cuif L, Prabhakaran B, Oates AC, Ho RK, Vogt TF (2001) Zebrafish lunatic fringe demarcates segmental boundaries. Mech Dev 105:175–180

    CAS  Google Scholar 

  • Sato Y, Yasuda K, Takahashi Y (2002) Morphological boundary forms by a novel inductive event mediated by Lunatic fringe and Notch during somitic segmentation. Development 129:3633–3644

    CAS  Google Scholar 

  • Serth K, Schuster-Gossler K, Cordes R, Gossler A (2003) Transcriptional oscillation of lunatic fringe is essential for somitogenesis. Genes Dev 17:912–925

    CAS  Google Scholar 

  • Shimeld SM (1999) The evolution of the hedgehog gene family in chordates: Insights from amphioxus hedgehog. Dev Genes Evol 209:40–47

    CAS  Google Scholar 

  • Strimmer K, von Haessler S (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • Zhang N, Gridley T (1998) Defects in somite formation in lunatic fringe-deficient mice. Nature 394:374–377

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Marty Cohn for discussions and John Lawrence and Skip Pierce for generously loaning us laboratory space in Tampa. This work was supported by the BBSRC.

Author information

Authors and Affiliations

  1. School of Animal and Microbial Sciences, The University of Reading, Whiteknights, PO Box 228, Reading, RG6 6AJ, UK

    Françoise Mazet & Sebastian M. Shimeld

Authors
  1. Françoise Mazet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sebastian M. Shimeld
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Françoise Mazet.

Additional information

Edited by J. Campos-Ortego

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mazet, F., Shimeld, S.M. Characterisation of an amphioxus Fringe gene and the evolution of the vertebrate segmentation clock. Dev Genes Evol 213, 505–509 (2003). https://doi.org/10.1007/s00427-003-0351-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-003-0351-7

Keywords

Search

Navigation