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. 2003 Apr;163(4):1427–1438. doi: 10.1093/genetics/163.4.1427

A genetic screen for hedgehog targets involved in the maintenance of the Drosophila anteroposterior compartment boundary.

Mátyás Végh 1, Konrad Basler 1
PMCID: PMC1462513  PMID: 12702686

Abstract

The development of multicellular organisms requires the establishment of cell populations with different adhesion properties. In Drosophila, a cell-segregation mechanism underlies the maintenance of the anterior (A) and posterior (P) compartments of the wing imaginal disc. Although engrailed (en) activity contributes to the specification of the differential cell affinity between A and P cells, recent evidence suggests that cell sorting depends largely on the transduction of the Hh signal in A cells. The activator form of Cubitus interruptus (Ci), a transcription factor mediating Hh signaling, defines anterior specificity, indicating that Hh-dependent cell sorting requires Hh target gene expression. However, the identity of the gene(s) contributing to distinct A and P cell affinities is unknown. Here, we report a genetic screen based on the FRT/FLP system to search for genes involved in the correct establishment of the anteroposterior compartment boundary. By using double FRT chromosomes in combination with a wing-specific FLP source we screened 250,000 mutagenized chromosomes. Several complementation groups affecting wing patterning have been isolated, including new alleles of most known Hh-signaling components. Among these, we identified a class of patched (ptc) alleles exhibiting a novel phenotype. These results demonstrate the value of our setup in the identification of genes involved in distinct wing-patterning processes.

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Selected References

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  1. Basler K., Struhl G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature. 1994 Mar 17;368(6468):208–214. doi: 10.1038/368208a0. [DOI] [PubMed] [Google Scholar]
  2. Biehs B., Sturtevant M. A., Bier E. Boundaries in the Drosophila wing imaginal disc organize vein-specific genetic programs. Development. 1998 Nov;125(21):4245–4257. doi: 10.1242/dev.125.21.4245. [DOI] [PubMed] [Google Scholar]
  3. Blair S. S., Ralston A. Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development. 1997 Oct;124(20):4053–4063. doi: 10.1242/dev.124.20.4053. [DOI] [PubMed] [Google Scholar]
  4. Chen Y., Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell. 1996 Nov 1;87(3):553–563. doi: 10.1016/s0092-8674(00)81374-4. [DOI] [PubMed] [Google Scholar]
  5. Dahmann C., Basler K. Compartment boundaries: at the edge of development. Trends Genet. 1999 Aug;15(8):320–326. doi: 10.1016/s0168-9525(99)01774-6. [DOI] [PubMed] [Google Scholar]
  6. Dahmann C., Basler K. Opposing transcriptional outputs of Hedgehog signaling and engrailed control compartmental cell sorting at the Drosophila A/P boundary. Cell. 2000 Feb 18;100(4):411–422. doi: 10.1016/s0092-8674(00)80677-7. [DOI] [PubMed] [Google Scholar]
  7. Garcia-Bellido A., Ripoll P., Morata G. Developmental compartmentalisation of the wing disk of Drosophila. Nat New Biol. 1973 Oct 24;245(147):251–253. doi: 10.1038/newbio245251a0. [DOI] [PubMed] [Google Scholar]
  8. García-Bellido A. Genetic control of wing disc development in Drosophila. Ciba Found Symp. 1975;0(29):161–182. doi: 10.1002/9780470720110.ch8. [DOI] [PubMed] [Google Scholar]
  9. Jiang J., Struhl G. Protein kinase A and hedgehog signaling in Drosophila limb development. Cell. 1995 Feb 24;80(4):563–572. doi: 10.1016/0092-8674(95)90510-3. [DOI] [PubMed] [Google Scholar]
  10. Johnson R. L., Milenkovic L., Scott M. P. In vivo functions of the patched protein: requirement of the C terminus for target gene inactivation but not Hedgehog sequestration. Mol Cell. 2000 Aug;6(2):467–478. doi: 10.1016/s1097-2765(00)00045-9. [DOI] [PubMed] [Google Scholar]
  11. Kim J., Sebring A., Esch J. J., Kraus M. E., Vorwerk K., Magee J., Carroll S. B. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature. 1996 Jul 11;382(6587):133–138. doi: 10.1038/382133a0. [DOI] [PubMed] [Google Scholar]
  12. Lawrence P. A., Morata G. Compartments in the wing of Drosophila: a study of the engrailed gene. Dev Biol. 1976 Jun;50(2):321–337. doi: 10.1016/0012-1606(76)90155-x. [DOI] [PubMed] [Google Scholar]
  13. Lawrence P. A., Struhl G. Morphogens, compartments, and pattern: lessons from drosophila? Cell. 1996 Jun 28;85(7):951–961. doi: 10.1016/s0092-8674(00)81297-0. [DOI] [PubMed] [Google Scholar]
  14. Lecuit T., Brook W. J., Ng M., Calleja M., Sun H., Cohen S. M. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature. 1996 May 30;381(6581):387–393. doi: 10.1038/381387a0. [DOI] [PubMed] [Google Scholar]
  15. Martín V., Carrillo G., Torroja C., Guerrero I. The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking. Curr Biol. 2001 Apr 17;11(8):601–607. doi: 10.1016/s0960-9822(01)00178-6. [DOI] [PubMed] [Google Scholar]
  16. Nellen D., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell. 1996 May 3;85(3):357–368. doi: 10.1016/s0092-8674(00)81114-9. [DOI] [PubMed] [Google Scholar]
  17. Newsome T. P., Asling B., Dickson B. J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development. 2000 Feb;127(4):851–860. doi: 10.1242/dev.127.4.851. [DOI] [PubMed] [Google Scholar]
  18. Prout M., Damania Z., Soong J., Fristrom D., Fristrom J. W. Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics. 1997 May;146(1):275–285. doi: 10.1093/genetics/146.1.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Préat T., Thérond P., Lamour-Isnard C., Limbourg-Bouchon B., Tricoire H., Erk I., Mariol M. C., Busson D. A putative serine/threonine protein kinase encoded by the segment-polarity fused gene of Drosophila. Nature. 1990 Sep 6;347(6288):87–89. doi: 10.1038/347087a0. [DOI] [PubMed] [Google Scholar]
  20. Rodriguez I., Basler K. Control of compartmental affinity boundaries by hedgehog. Nature. 1997 Oct 9;389(6651):614–618. doi: 10.1038/39343. [DOI] [PubMed] [Google Scholar]
  21. Strutt H., Thomas C., Nakano Y., Stark D., Neave B., Taylor A. M., Ingham P. W. Mutations in the sterol-sensing domain of Patched suggest a role for vesicular trafficking in Smoothened regulation. Curr Biol. 2001 Apr 17;11(8):608–613. doi: 10.1016/s0960-9822(01)00179-8. [DOI] [PubMed] [Google Scholar]
  22. Vervoort M., Crozatier M., Valle D., Vincent A. The COE transcription factor Collier is a mediator of short-range Hedgehog-induced patterning of the Drosophila wing. Curr Biol. 1999 Jun 17;9(12):632–639. doi: 10.1016/s0960-9822(99)80285-1. [DOI] [PubMed] [Google Scholar]
  23. Xu T., Rubin G. M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 1993 Apr;117(4):1223–1237. doi: 10.1242/dev.117.4.1223. [DOI] [PubMed] [Google Scholar]

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