Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye

Nature volume 396, pages 272–276 (1998)Cite this article

Abstract

An early event in Drosophila eye development is the division of the eye disc into dorsoventral domains. The dorsoventral pattern is displayed in the adult compound eye as a distinct mirror symmetry across the dorsoventral midline or equator1,2. The dorsoventral axis is also implicated in organizing early development of the eye, as retinal differentiation is initiated at the posterior dorsoventral midline3. Here we show that Fringe is expressed specifically in the ventral half of the undifferentiated eye disc, thus creating a dorsoventral boundary. Ectopic Fringe borders that are generated by clones of fringe − cells can reverse the planar polarity of photoreceptor clusters, indicating that the Fringe boundary is crucial for the induction of mirror symmetry. Lack of a Fringe boundary disrupts equatorial expression of Notch signalling proteins and causes a complete failure of eye development. Our results indicate that the formation of the Fringe boundary and subsequent Notch signalling at the equator are essential for organizing mirror symmetry and eye morphogenesis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Expression of fng and Notch (N) signalling proteins in eye discs.
Figure 2: Polarity reversals by ventral fng− clones.
Figure 3: Ser and Dl expression in fng clones.
Figure 4: Failure of eye development by ubiquitous Fng expression.
Figure 5: Effects of ubiquitous Fng expression on Notch (N) signalling proteins and Eq-3.
Figure 6: Repression of Fng by Mirr.

Similar content being viewed by others

References

  1. Dietrich, W. Die Facettenaugen der Dipteren. Z. Wiss. Zool. 92, 465–539 (1909).

    Google Scholar 

  2. Ready, D. F., Hanson, T. E. & Benzer, S. Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217–240 (1976).

    Article  CAS  PubMed  Google Scholar 

  3. Wolff, T. & Ready, D. F. The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113, 841–850 (1991).

    CAS  PubMed  Google Scholar 

  4. Yuan, Y. P., Schultz, J., Mlodzik, M. & Bork, P. Secreted Fringe-like signaling molecules may be glycosyltransferases. Cell 88, 9–11 (1997).

    Article  CAS  PubMed  Google Scholar 

  5. Irvine, K. & Wieschaus, E. fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79, 595–606 (1994).

    Article  CAS  PubMed  Google Scholar 

  6. Kim, J., Irvine, K. D. & Carroll, S. B. Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing. Cell 82, 795–802 (1995).

    Article  CAS  PubMed  Google Scholar 

  7. Blair, S. S. Limb development: marginal fringe benefits. Curr. Biol. 7, R686–690 (1997).

    Article  CAS  PubMed  Google Scholar 

  8. Fleming, R. J., Gu, Y. & Hukriede, N. A. Serrate -mediated activation of Notch is specifically blocked by the products of the gene fringe in the dorsal compartment of the Drosophila wing imaginal discs. Development 124, 2973–2981 (1997).

    CAS  PubMed  Google Scholar 

  9. Irvine, K. D. & Vogt, T. F. Dorsal-ventral signaling in limb development. Curr. Opin. Cell Biol. 9, 867–876 (1997).

    Article  CAS  PubMed  Google Scholar 

  10. Panin, V. M., Papayannopoulos, V., Wilson, R. & Irvine, K. D. Fringe modulates Notch-ligand interactions. Nature 387, 908–912 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Ma, C. & Moses, K. wingless and patched are negative regulators of the morphogenetic furrow and canaffect tissue polarity in the developing Drosophila compound eye. Development 121, 2279–2289 (1995).

    CAS  PubMed  Google Scholar 

  12. Xu, T. & Rubin, G. M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237 (1993).

    CAS  PubMed  Google Scholar 

  13. Pignoni, F. & Zipursky, S. L. Induction of Drosophila eye development by Decapentaplegic. Development 124, 271–278 (1997).

    CAS  PubMed  Google Scholar 

  14. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).

    CAS  PubMed  Google Scholar 

  15. McNeil, H., Yang, C.-H., Brodsky, M., Ungos, J. & Simon, M. A. mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev. 11, 1073–1082 (1997).

    Article  Google Scholar 

  16. Kehl, B. T., Cho, K.-O. & Choi, K.-W. mirror, a Drosophila homeobox gene in the iroquois complex, is required for sensory organ and alula formation. Development 125, 1217–1227 (1998).

    CAS  PubMed  Google Scholar 

  17. Netter, S., Fauvarque, M.-O., del Corral, R. D., Dura, J.-M. & Coen, D. white+ transgene insertions presenting a dorsal/ventral pattern define a single cluster of homeobox genes that is silenced by the Polycomb -group proteins in Drosophila melanogaster. Genetics 149, 257–275 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Heberlein, U., Borod, E. R. & Chanut, F. A. Dorsoventral patterning in the Drosophila retina by wingless. Development 125, 567–577 (1998).

    CAS  PubMed  Google Scholar 

  19. Wiersdorff, V., Lecuit, T., Cohen, S. M. & Mlodzik, M. Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122, 2153–2162 (1996).

    CAS  PubMed  Google Scholar 

  20. Chanut, F. & Heberlein, U. Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124, 559–567 (1997).

    CAS  PubMed  Google Scholar 

  21. Dominguez, M. & Hafen, E. Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev. 11, 3254–3264 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Royet, J. & Finkelstein, R. Establishing primordia in the Drosophila eye-antennal imaginal disc: the roles of decapentaplegic, wingless and hedgehog. Development 124, 4793–4800 (1997).

    CAS  PubMed  Google Scholar 

  23. Borod, E. R. & Heberelin, U. Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev. Biol. 197, 187–197 (1998).

    Article  CAS  PubMed  Google Scholar 

  24. Sun, Y. H. et al. white as a reporter gene to detect transcriptional silencers specifying position-specific gene expression during Drosophila melanogaster eye development. Genetics 141, 1075–1086 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Carthew, R. W. & Rubin, G. M. seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 63, 561–577 (1990).

    Article  CAS  PubMed  Google Scholar 

  26. Choi, K.-W. & Benzer, S. Rotation of photoreceptor clusters in the developing Drosophila eye requires the nemo gene. Cell 78, 125–136 (1994).

    Article  CAS  PubMed  Google Scholar 

  27. Carroll, S. B. & Whyte, J. S. The role of the hairy gene during Drosophila morphogenesis-stripes in imaginal discs. Genes Dev. 3, 905–916 (1989).

    Article  CAS  Google Scholar 

  28. Higashijima, S.-I. et al. Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. Genes Dev. 6, 50–60 (1992).

    Article  CAS  PubMed  Google Scholar 

  29. Treisman, J. E. & Rubin, G. M. wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121, 3519–3527 (1995).

    CAS  PubMed  Google Scholar 

  30. Wehrli, M. & Tomlinson, A. Independent regulation of anterior/posterior and equatorial/polar polarity in the Drosophila eye; evidence for the involvement of Wnt signaling in the equatorial/polar axis. Development 125, 1421–1432 (1998).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank H. Bellen, S. Izaddoost, B. Kehl and G. Mardon for comments; J. Kim for fng cDNA, fng mutants and UAS-fng ; K. Kozopas for flip-out flies; E. Knust for Ser antibody; K. Saigo for Bar antibody; Q. Sun for Eq-3 strain; Artavanis-Tsakonas for Notch and Dl antibodies; the Bloomington Stock Center for providing many of the stocks; H. Bellen for use of the confocal microscope; S. Mehta for preliminary work; and B. Kehl for excellent technical assistance. This work was supported by a grant from the NIH.

Author information

Authors and Affiliations

  1. Department of Cell Biology, Baylor College of Medicine, One Baylor Plaza, Houston, 77030, Texas, USA

    Kyung-Ok Cho & Kwang-Wook Choi

  2. Department of Ophthalmology, Program of Developmental Biology, Baylor College of Medicine, One Baylor Plaza, Houston, 77030, Texas, USA

    Kwang-Wook Choi

Authors
  1. Kyung-Ok Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kwang-Wook Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kwang-Wook Choi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cho, KO., Choi, KW. Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396, 272–276 (1998). https://doi.org/10.1038/24394

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/24394

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing