Advertisement
JOURNAL ARTICLES
A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia
F. Pichaud, C. Desplan
Development 2001 128: 815-826;

Summary

The Drosophila eye is widely used as a model system to study neuronal differentiation, survival and axon projection. Photoreceptor differentiation starts with the specification of a founder cell R8, which sequentially recruits other photoreceptor neurons to the ommatidium. The eight photoreceptors that compose each ommatidium exist in two chiral forms organized along two axes of symmetry and this pattern represents a paradigm to study tissue polarity. We have developed a method of fluoroscopy to visualize the different types of photoreceptors and the organization of the ommatidia in living animals. This allowed us to perform an F(1) genetic screen to isolate mutants affecting photoreceptor differentiation, survival or planar polarity. We illustrate the power of this detection system using known genetic backgrounds and new mutations that affect ommatidial differentiation, morphology or chirality.

Reference

    1. Benlali A.,
    2. Draskovic I.,
    3. Hazelett D. J.,
    4. Treisman J. E.
    (2000) act up controls actin polymerization to alter cell shape and restrict hedgehog signaling in the Drosophila eye disc. Cell 101, 271–281
    OpenUrlCrossRefPubMedWeb of Science
    1. Benzer S.
    (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc. Natl. Acad. Sci. USA 58, 1112–1119
    OpenUrlFREE Full Text
    1. Brand A. H.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Cagan R.
    (1993) Cell fate specification in the developing Drosophila retina. Development 117, 19–28
    OpenUrl
    1. Cavodeassi F.,
    2. Diez Del Corral R.,
    3. Campuzano S.,
    4. Dominguez M.
    (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126, 4933–4942
    OpenUrlAbstract
    1. Cho K. O.,
    2. Choi K. W.
    (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396, 272–276
    OpenUrlCrossRefPubMed
    1. Chou W.,
    2. Hall K.,
    3. Wilson D.,
    4. Wideman C.,
    5. Townson S.,
    6. Chadwell L.,
    7. Britt S.
    (1996) Identification of a novel opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 17, 1101–1115
    OpenUrlCrossRefPubMedWeb of Science
    1. Chou W.,
    2. Huber A.,
    3. Bentrop J.,
    4. Schulz S.,
    5. Schwab K.,
    6. Chadwell L.,
    7. Paulsen R.,
    8. Britt S.
    (1999) Patterning of the R7 and R8 cells of Drosophila: evidence for induced and default cell-fate specification. Development 126, 607–616
    OpenUrlAbstract
    1. Cooper M. T.,
    2. Bray S. J.
    (1999) Frizzled regulation of Notch signaling polarizes cell fate in the Drosophila eye. Nature, 397, 526–530
    OpenUrlCrossRefPubMed
    1. Dang D. T.,
    2. Perrimon N.
    (1992) Use of a yeast site-specific recombinase to generate embryonic mosaics in Drosophila. Dev. Genet 13, 367–375
    OpenUrlCrossRefPubMedWeb of Science
    1. Deretic D.,
    2. Schmerl S.,
    3. Hargrave P. A.,
    4. Arendt A.,
    5. McDowell J. H.
    (1998) Regulation of sorting and post-Golgi trafficking of rhodopsin by its C-terminal sequence QVS(A)PA. Proc. Natl. Acad. Sci. USA 95, 10620–10625
    OpenUrlAbstract/FREE Full Text
    1. Dominguez M.,
    2. de Celis J. F.
    (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396, 276–278
    OpenUrlCrossRefPubMed
    1. Fanto M.,
    2. Mlodzik M.
    (1999) Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397, 523–526
    OpenUrlCrossRefPubMed
    1. Feiler R.,
    2. Bjornson R.,
    3. Kirschfeld K.,
    4. Mismer D.,
    5. Rubin G. M.,
    6. Smith D. P.,
    7. Socolich M.,
    8. Zuker C. S.
    (1992) Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J. Neurosci 12, 3862–3868
    OpenUrlAbstract
    1. Fortini M. E.,
    2. Bonini N. M.
    (2000) Modeling human neurodegenerative diseases in Drosophila: on a wing and a prayer. Trends Genet 16, 161–167
    OpenUrlCrossRefPubMedWeb of Science
    1. Fortini M. E.,
    2. Rebay I.,
    3. Caron L. A.,
    4. Artavanis-Tsakonas S.
    (1993) An activated Notch receptor blocks cell-fate commitment in the developing Drosophila eye. Nature 365, 555–557
    OpenUrlCrossRefPubMedWeb of Science
    1. Fortini M. E.,
    2. Rubin G. M.
    (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev 4, 444–463
    OpenUrlAbstract/FREE Full Text
    1. Franceschini N.,
    2. Kirschfeld K.
    (1971) In vivo optical study of photoreceptor elements in the compound eye of Drosophila. Kybernetik 8, 1–13
    OpenUrlCrossRefPubMedWeb of Science
    1. Franceschini N.,
    2. Kirschfeld K.
    (1971) Pseudopupil phenomena in the compound eye of Drosophila. Kybernetik 9, 159–182
    OpenUrlCrossRefPubMedWeb of Science
    1. Franceschini N.,
    2. Kirschfeld K.
    (1976) On the control of the automatic light flux in the Dipterans compound eyes. Biol. Cybern 21, 181–203
    OpenUrlCrossRef
    1. Franceschini N.,
    2. Kirschfeld K.,
    3. Minke B.
    (1981) Fluorescence of photoreceptor cells observed in vivo. Science 213, 1264–1267
    OpenUrlAbstract/FREE Full Text
    1. Franceschini N.,
    2. Hardie R.,
    3. Ribi W.,
    4. Kirschfeld K.
    (1981) Sexual dimorphism in a photoreceptor. Nature 291, 241–244
    OpenUrlCrossRefWeb of Science
    1. Golic K. G.,
    2. Lindquist S.
    (1989) The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499–509
    OpenUrlCrossRefPubMedWeb of Science
    1. Gomez-Skarmeta J. L.,
    2. del Corral R. D.,
    3. de la Calle-Mustienes E.,
    4. Ferre-Marco D.,
    5. Modolell J.
    (1996) Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85, 95–105
    OpenUrlCrossRefPubMedWeb of Science
    1. Hardie R.
    (1979) Electrophysiological analysis of fly retina. I. Comparative properties of R1-R6 and R7-R8. J. Comp. Physiol 129, 19–33
    OpenUrl
    1. Harris W. A.,
    2. Stark W. S.,
    3. Walker J. A.
    (1976) Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J. Physiol 256, 415–439
    OpenUrl
    1. Jackson G. R.,
    2. Salecker I.,
    3. Dong X.,
    4. Yao X.,
    5. Arnheim N.,
    6. Faber P. W.,
    7. MacDonald M. E.,
    8. Zipursky S. L.
    (1998) Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21, 633–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Karim F. D.,
    2. Chang H. C.,
    3. Therrien M.,
    4. Wassarman D. A.,
    5. Laverty T.,
    6. Rubin G. M.
    (1996) A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 143, 315–329
    OpenUrlAbstract/FREE Full Text
    1. Kirschfeld K.,
    2. Franceschini N.
    (1977) Evidence for a sensitising pigment in fly photoreceptors. Nature 269, 386–390
    OpenUrlCrossRefPubMed
    1. Kirschfeld K.,
    2. Franceschini N.
    (1968) Optische Eigenschaften der ommatidien im komplexauge von Musca. Kybernetik 5, 47–52
    OpenUrlCrossRefPubMed
    1. Koenig J.,
    2. Merrian J. R.
    (1997) Autosomal ERG mutants. Drosophila Inf. Serv 52, 50–51
    OpenUrl
    1. Kumar J.,
    2. Moses K.
    (1997) Transcription factors in eye development: a gorgeous mosaic?. Genes Dev 11, 2023–2028
    OpenUrlFREE Full Text
    1. McNeill H.,
    2. Yang C. H.,
    3. Brodsky M.,
    4. Ungos J.,
    5. Simon M. A.
    (1997) 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
    OpenUrlAbstract/FREE Full Text
    1. Mlodzik M.
    (1999) Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross-talk. EMBO J 18, 6873–6879
    OpenUrlCrossRefPubMedWeb of Science
    1. Mismer D.,
    2. Rubin G. M.
    (1987) Analysis of the promoter of the Nina E opsin gene in Drosophila melanogaster. Genetics 116, 565–578
    OpenUrlAbstract/FREE Full Text
    1. Mollereau B.,
    2. Wernet M. F.,
    3. Beaufils P.,
    4. Killian D.,
    5. Pichaud F.,
    6. Kuhnlein R.,
    7. Desplan C.
    (2000) A green fluorescent protein enhancer trap screen in Drosophila photoreceptor cells. Mech. Dev 93, 151–160
    OpenUrlCrossRefPubMed
    1. Montell C.
    (1999) Visual transduction in Drosophila. Annu. Rev. Cell Dev. Biol 15, 231–268
    OpenUrlCrossRefPubMedWeb of Science
    1. Newsome T. P.,
    2. Asling B.,
    3. Dickson B. J.
    (2000) Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851–860
    OpenUrlAbstract
    1. O'Tousa J. E.,
    2. Baehr W.,
    3. Martin R. L.,
    4. Hirsh J.,
    5. Pak W. L.,
    6. AppleburyM. L.
    (1985) The Drosophila ninaE gene encodes an opsin. Cell 40, 839–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Ostroy S. E.,
    2. Wilson M.,
    3. Pak W. L.
    (1974) Drosophila rhodopsin: photochemistry, extraction and differences in the NorpAp12 phototransduction mutant. Biochem. Biophys. Res. Commun 59, 960–966
    OpenUrlCrossRefPubMedWeb of Science
    1. Papatsenko D.,
    2. Sheng G.,
    3. Desplan C.
    (1997) A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 124, 1665–1673
    OpenUrlAbstract
    1. Papayannopoulos V.,
    2. Tomlinson A.,
    3. Panin V. M.,
    4. Rauskolb C.,
    5. Irvine K. D.
    (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281, 2031–2034
    OpenUrlAbstract/FREE Full Text
    1. Pichaud F.,
    2. Casares F.
    (2000) homothorax and iroquois-C are required to establish dorso-ventral regionalization of the developing eye disc. Mech. Dev 96, 15–25
    OpenUrlCrossRefPubMedWeb of Science
    1. Pollock. J. A.,
    2. Benzer S.
    (1988) Transcript localization of four opsin genes in the three visual organs of Drosophila; Rh2 is ocellus specific. Nature 333, 779–782
    OpenUrlCrossRefPubMedWeb of Science
    1. Ready D. F.,
    2. Hanson T. E.,
    3. Benzer S.
    (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol 53, 217–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Reifegerste R.,
    2. Moses K.
    (1999) Genetics of epithelial polarity and pattern in the Drosophila retina. BioEssays 21, 275–285
    OpenUrlCrossRefPubMedWeb of Science
    1. Reinke R.,
    2. Zipursky S. L.
    (1988) Cell-cell interaction in the Drosophila retina: the bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development. Cell 55, 321–330
    OpenUrlCrossRefPubMedWeb of Science
    1. Stowers R. S.,
    2. Schwarz T. L.
    (1999) A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152, 1631–1639
    OpenUrlAbstract/FREE Full Text
    1. Strutt D. I.,
    2. Mlodzik M.
    (1995) Ommatidial polarity in the Drosophila eye is determined by the direction of furrow progression and local interactions. Development 121, 4247–4256
    OpenUrlAbstract
    1. Strutt H.,
    2. Strutt D.
    (1999) Polarity determination in the Drosophila eye. Curr. Opin. Genet. Dev 9, 442–446
    OpenUrlCrossRefPubMedWeb of Science
    1. Tomlinson A.
    (1985) The cellular dynamics of pattern formation in the eye of Drosophila. J. Embryol. Exp. Morphol 89, 313–331
    OpenUrlPubMedWeb of Science
    1. Tomlinson A.,
    2. Struhl G.
    (1999) Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye. Development 126, 5725–5738
    OpenUrlAbstract
    1. Treisman J. E.
    (1999) A conserved blueprint for the eye?. BioEssays 21, 843–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Wehrli M.,
    2. Tomlinson A.
    (1995) Epithelial planar polarity in the developing Drosophila eye. Development 121, 2451–2459
    OpenUrlAbstract
    1. Wehrli M.,
    2. Tomlinson A.
    (1998) 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
    OpenUrlAbstract
    1. Wimmer E. A.,
    2. Cohen S. M.,
    3. Jäckle H.,
    4. Desplan C.
    (1997) buttonhead does not contribute to a combinatorial code proposed for Drosophila head development. Development 124, 1509–1517
    OpenUrlAbstract
    1. Wolff T.,
    2. Ready D. F.
    (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113, 841–850
    OpenUrlAbstract
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
    1. Zuker C. S.,
    2. Cowman A.,
    3. Rubin G.
    (1985) Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 40, 851–858
    OpenUrlCrossRefPubMedWeb of Science
    1. Zuker C. S.,
    2. Montell C.,
    3. Jones K.,
    4. Laverty T.,
    5. Rubin G. M.
    (1987) A rhodopsin gene expressed in photoreceptor cell R7 of the Drosophila eye: Homologies with other signal-transducing molecules. J. Neurosci 7, 1537–1550
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia
F. Pichaud, C. Desplan
Development 2001 128: 815-826;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Brandon Carpenter talks about how inherited histone methylation defines the germline versus soma decision in C. elegans. 

Sign up to join our next session:

10 March
Time: TBC
Chaired by: Thomas Lecuit