Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2004 Jan;166(1):187–200. doi: 10.1534/genetics.166.1.187

A mosaic genetic screen reveals distinct roles for trithorax and polycomb group genes in Drosophila eye development.

Florence Janody 1, Jeffrey D Lee 1, Neal Jahren 1, Dennis J Hazelett 1, Aude Benlali 1, Grant I Miura 1, Irena Draskovic 1, Jessica E Treisman 1
PMCID: PMC1470713  PMID: 15020417

Abstract

The wave of differentiation that traverses the Drosophila eye disc requires rapid transitions in gene expression that are controlled by a number of signaling molecules also required in other developmental processes. We have used a mosaic genetic screen to systematically identify autosomal genes required for the normal pattern of photoreceptor differentiation, independent of their requirements for viability. In addition to genes known to be important for eye development and to known and novel components of the Hedgehog, Decapentaplegic, Wingless, Epidermal growth factor receptor, and Notch signaling pathways, we identified several members of the Polycomb and trithorax classes of genes encoding general transcriptional regulators. Mutations in these genes disrupt the transitions between zones along the anterior-posterior axis of the eye disc that express different combinations of transcription factors. Different trithorax group genes have very different mutant phenotypes, indicating that target genes differ in their requirements for chromatin remodeling, histone modification, and coactivation factors.

Full Text

The Full Text of this article is available as a PDF (943.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baker N. E., Yu S. Y. Proneural function of neurogenic genes in the developing Drosophila eye. Curr Biol. 1997 Feb 1;7(2):122–132. doi: 10.1016/s0960-9822(06)00056-x. [DOI] [PubMed] [Google Scholar]
  2. Baonza A., Freeman M. Notch signalling and the initiation of neural development in the Drosophila eye. Development. 2001 Oct;128(20):3889–3898. doi: 10.1242/dev.128.20.3889. [DOI] [PubMed] [Google Scholar]
  3. Beisel Christian, Imhof Axel, Greene Jaime, Kremmer Elisabeth, Sauer Frank. Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature. 2002 Oct 9;419(6909):857–862. doi: 10.1038/nature01126. [DOI] [PubMed] [Google Scholar]
  4. Benassayag Corinne, Plaza Serge, Callaerts Patrick, Clements Jason, Romeo Yves, Gehring Walter J., Cribbs David L. Evidence for a direct functional antagonism of the selector genes proboscipedia and eyeless in Drosophila head development. Development. 2003 Feb;130(3):575–586. doi: 10.1242/dev.00226. [DOI] [PubMed] [Google Scholar]
  5. Benlali A., Draskovic I., Hazelett D. J., Treisman J. E. act up controls actin polymerization to alter cell shape and restrict Hedgehog signaling in the Drosophila eye disc. Cell. 2000 Apr 28;101(3):271–281. doi: 10.1016/s0092-8674(00)80837-5. [DOI] [PubMed] [Google Scholar]
  6. Bessa Jose, Gebelein Brian, Pichaud Franck, Casares Fernando, Mann Richard S. Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev. 2002 Sep 15;16(18):2415–2427. doi: 10.1101/gad.1009002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Beuchle D., Struhl G., Müller J. Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development. 2001 Mar;128(6):993–1004. doi: 10.1242/dev.128.6.993. [DOI] [PubMed] [Google Scholar]
  8. Bilder D., Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature. 2000 Feb 10;403(6770):676–680. doi: 10.1038/35001108. [DOI] [PubMed] [Google Scholar]
  9. Birve A., Sengupta A. K., Beuchle D., Larsson J., Kennison J. A., Rasmuson-Lestander A, Müller J. Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants. Development. 2001 Sep;128(17):3371–3379. doi: 10.1242/dev.128.17.3371. [DOI] [PubMed] [Google Scholar]
  10. Blackman R. K., Sanicola M., Raftery L. A., Gillevet T., Gelbart W. M. An extensive 3' cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development. 1991 Mar;111(3):657–666. doi: 10.1242/dev.111.3.657. [DOI] [PubMed] [Google Scholar]
  11. Boube M., Faucher C., Joulia L., Cribbs D. L., Bourbon H. M. Drosophila homologs of transcriptional mediator complex subunits are required for adult cell and segment identity specification. Genes Dev. 2000 Nov 15;14(22):2906–2917. doi: 10.1101/gad.17900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Boube Muriel, Joulia Laurent, Cribbs David L., Bourbon Henri-Marc. Evidence for a mediator of RNA polymerase II transcriptional regulation conserved from yeast to man. Cell. 2002 Jul 26;110(2):143–151. doi: 10.1016/s0092-8674(02)00830-9. [DOI] [PubMed] [Google Scholar]
  13. Cagan R. L., Ready D. F. Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 1989 Aug;3(8):1099–1112. doi: 10.1101/gad.3.8.1099. [DOI] [PubMed] [Google Scholar]
  14. Calgaro Stéphane, Boube Muriel, Cribbs David L., Bourbon Henri-Marc. The Drosophila gene taranis encodes a novel trithorax group member potentially linked to the cell cycle regulatory apparatus. Genetics. 2002 Feb;160(2):547–560. doi: 10.1093/genetics/160.2.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cao Ru, Wang Liangjun, Wang Hengbin, Xia Li, Erdjument-Bromage Hediye, Tempst Paul, Jones Richard S., Zhang Yi. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002 Sep 26;298(5595):1039–1043. doi: 10.1126/science.1076997. [DOI] [PubMed] [Google Scholar]
  16. Castelli-Gair J., Greig S., Micklem G., Akam M. Dissecting the temporal requirements for homeotic gene function. Development. 1994 Jul;120(7):1983–1995. doi: 10.1242/dev.120.7.1983. [DOI] [PubMed] [Google Scholar]
  17. Chen R., Amoui M., Zhang Z., Mardon G. Dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell. 1997 Dec 26;91(7):893–903. doi: 10.1016/s0092-8674(00)80481-x. [DOI] [PubMed] [Google Scholar]
  18. Collins R. T., Furukawa T., Tanese N., Treisman J. E. Osa associates with the Brahma chromatin remodeling complex and promotes the activation of some target genes. EMBO J. 1999 Dec 15;18(24):7029–7040. doi: 10.1093/emboj/18.24.7029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Crosby M. A., Miller C., Alon T., Watson K. L., Verrijzer C. P., Goldman-Levi R., Zak N. B. The trithorax group gene moira encodes a brahma-associated putative chromatin-remodeling factor in Drosophila melanogaster. Mol Cell Biol. 1999 Feb;19(2):1159–1170. doi: 10.1128/mcb.19.2.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Czermin Birgit, Melfi Raffaella, McCabe Donna, Seitz Volker, Imhof Axel, Pirrotta Vincenzo. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell. 2002 Oct 18;111(2):185–196. doi: 10.1016/s0092-8674(02)00975-3. [DOI] [PubMed] [Google Scholar]
  21. Czerny T., Halder G., Kloter U., Souabni A., Gehring W. J., Busslinger M. twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell. 1999 Mar;3(3):297–307. doi: 10.1016/s1097-2765(00)80457-8. [DOI] [PubMed] [Google Scholar]
  22. Daubresse G., Deuring R., Moore L., Papoulas O., Zakrajsek I., Waldrip W. R., Scott M. P., Kennison J. A., Tamkun J. W. The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development. 1999 Mar;126(6):1175–1187. doi: 10.1242/dev.126.6.1175. [DOI] [PubMed] [Google Scholar]
  23. Domínguez M., Brunner M., Hafen E., Basler K. Sending and receiving the hedgehog signal: control by the Drosophila Gli protein Cubitus interruptus. Science. 1996 Jun 14;272(5268):1621–1625. doi: 10.1126/science.272.5268.1621. [DOI] [PubMed] [Google Scholar]
  24. Domínguez M. Dual role for Hedgehog in the regulation of the proneural gene atonal during ommatidia development. Development. 1999 Jun;126(11):2345–2353. doi: 10.1242/dev.126.11.2345. [DOI] [PubMed] [Google Scholar]
  25. Farkas G., Gausz J., Galloni M., Reuter G., Gyurkovics H., Karch F. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994 Oct 27;371(6500):806–808. doi: 10.1038/371806a0. [DOI] [PubMed] [Google Scholar]
  26. Fischle Wolfgang, Wang Yanming, Jacobs Steven A., Kim Youngchang, Allis C. David, Khorasanizadeh Sepideh. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 2003 Aug 1;17(15):1870–1881. doi: 10.1101/gad.1110503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Francis N. J., Saurin A. J., Shao Z., Kingston R. E. Reconstitution of a functional core polycomb repressive complex. Mol Cell. 2001 Sep;8(3):545–556. doi: 10.1016/s1097-2765(01)00316-1. [DOI] [PubMed] [Google Scholar]
  28. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell. 1996 Nov 15;87(4):651–660. doi: 10.1016/s0092-8674(00)81385-9. [DOI] [PubMed] [Google Scholar]
  29. Gildea J. J., Lopez R., Shearn A. A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics. 2000 Oct;156(2):645–663. doi: 10.1093/genetics/156.2.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Gindhart J. G., Jr, Kaufman T. C. Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics. 1995 Feb;139(2):797–814. doi: 10.1093/genetics/139.2.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Greenwood S., Struhl G. Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development. 1999 Dec;126(24):5795–5808. doi: 10.1242/dev.126.24.5795. [DOI] [PubMed] [Google Scholar]
  32. Gutiérrez Luis, Zurita Mario, Kennison James A., Vázquez Martha. The Drosophila trithorax group gene tonalli (tna) interacts genetically with the Brahma remodeling complex and encodes an SP-RING finger protein. Development. 2003 Jan;130(2):343–354. doi: 10.1242/dev.00222. [DOI] [PubMed] [Google Scholar]
  33. Halder G., Callaerts P., Flister S., Walldorf U., Kloter U., Gehring W. J. Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development. 1998 Jun;125(12):2181–2191. doi: 10.1242/dev.125.12.2181. [DOI] [PubMed] [Google Scholar]
  34. Hatini V., Bokor P., Goto-Mandeville R., DiNardo S. Tissue- and stage-specific modulation of Wingless signaling by the segment polarity gene lines. Genes Dev. 2000 Jun 1;14(11):1364–1376. [PMC free article] [PubMed] [Google Scholar]
  35. Hazelett D. J., Bourouis M., Walldorf U., Treisman J. E. decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development. 1998 Sep;125(18):3741–3751. doi: 10.1242/dev.125.18.3741. [DOI] [PubMed] [Google Scholar]
  36. Holstege F. C., Jennings E. G., Wyrick J. J., Lee T. I., Hengartner C. J., Green M. R., Golub T. R., Lander E. S., Young R. A. Dissecting the regulatory circuitry of a eukaryotic genome. Cell. 1998 Nov 25;95(5):717–728. doi: 10.1016/s0092-8674(00)81641-4. [DOI] [PubMed] [Google Scholar]
  37. Janody Florence, Martirosyan Zara, Benlali Aude, Treisman Jessica E. Two subunits of the Drosophila mediator complex act together to control cell affinity. Development. 2003 Aug;130(16):3691–3701. doi: 10.1242/dev.00607. [DOI] [PubMed] [Google Scholar]
  38. Jones R. S., Gelbart W. M. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics. 1990 Sep;126(1):185–199. doi: 10.1093/genetics/126.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kurant E., Pai C. Y., Sharf R., Halachmi N., Sun Y. H., Salzberg A. Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS. Development. 1998 Mar;125(6):1037–1048. doi: 10.1242/dev.125.6.1037. [DOI] [PubMed] [Google Scholar]
  40. Kuzin B., Tillib S., Sedkov Y., Mizrokhi L., Mazo A. The Drosophila trithorax gene encodes a chromosomal protein and directly regulates the region-specific homeotic gene fork head. Genes Dev. 1994 Oct 15;8(20):2478–2490. doi: 10.1101/gad.8.20.2478. [DOI] [PubMed] [Google Scholar]
  41. Kuzmichev Andrei, Nishioka Kenichi, Erdjument-Bromage Hediye, Tempst Paul, Reinberg Danny. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 2002 Nov 15;16(22):2893–2905. doi: 10.1101/gad.1035902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. LaJeunesse D., Shearn A. E(z): a polycomb group gene or a trithorax group gene? Development. 1996 Jul;122(7):2189–2197. doi: 10.1242/dev.122.7.2189. [DOI] [PubMed] [Google Scholar]
  43. Lee J. D., Treisman J. E. Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr Biol. 2001 Jul 24;11(14):1147–1152. doi: 10.1016/s0960-9822(01)00323-2. [DOI] [PubMed] [Google Scholar]
  44. Lee Jeffrey D., Amanai Kazuhito, Shearn Allen, Treisman Jessica E. The ubiquitin ligase Hyperplastic discs negatively regulates hedgehog and decapentaplegic expression by independent mechanisms. Development. 2002 Dec;129(24):5697–5706. doi: 10.1242/dev.00159. [DOI] [PubMed] [Google Scholar]
  45. Ma C., Moses K. Wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye. Development. 1995 Aug;121(8):2279–2289. doi: 10.1242/dev.121.8.2279. [DOI] [PubMed] [Google Scholar]
  46. Ma C., Zhou Y., Beachy P. A., Moses K. The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell. 1993 Dec 3;75(5):927–938. doi: 10.1016/0092-8674(93)90536-y. [DOI] [PubMed] [Google Scholar]
  47. Mardon G., Solomon N. M., Rubin G. M. dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development. 1994 Dec;120(12):3473–3486. doi: 10.1242/dev.120.12.3473. [DOI] [PubMed] [Google Scholar]
  48. Martens Joseph A., Winston Fred. Evidence that Swi/Snf directly represses transcription in S. cerevisiae. Genes Dev. 2002 Sep 1;16(17):2231–2236. doi: 10.1101/gad.1009902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Marty T., Müller B., Basler K., Affolter M. Schnurri mediates Dpp-dependent repression of brinker transcription. Nat Cell Biol. 2000 Oct;2(10):745–749. doi: 10.1038/35036383. [DOI] [PubMed] [Google Scholar]
  50. Milne Thomas A., Briggs Scott D., Brock Hugh W., Martin Mary Ellen, Gibbs Denise, Allis C. David, Hess Jay L. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell. 2002 Nov;10(5):1107–1117. doi: 10.1016/s1097-2765(02)00741-4. [DOI] [PubMed] [Google Scholar]
  51. Min Jinrong, Zhang Yi, Xu Rui-Ming. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 2003 Aug 1;17(15):1823–1828. doi: 10.1101/gad.269603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mizuno Tomoaki, Tsutsui Kyoko, Nishida Yasuyoshi. Drosophila myosin phosphatase and its role in dorsal closure. Development. 2002 Mar;129(5):1215–1223. doi: 10.1242/dev.129.5.1215. [DOI] [PubMed] [Google Scholar]
  53. Morata G., Ripoll P. Minutes: mutants of drosophila autonomously affecting cell division rate. Dev Biol. 1975 Feb;42(2):211–221. doi: 10.1016/0012-1606(75)90330-9. [DOI] [PubMed] [Google Scholar]
  54. Moses K., Rubin G. M. Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev. 1991 Apr;5(4):583–593. doi: 10.1101/gad.5.4.583. [DOI] [PubMed] [Google Scholar]
  55. Nakamura Tatsuya, Mori Toshiki, Tada Shinichiro, Krajewski Wladyslaw, Rozovskaia Tanya, Wassell Richard, Dubois Garrett, Mazo Alexander, Croce Carlo M., Canaani Eli. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol Cell. 2002 Nov;10(5):1119–1128. doi: 10.1016/s1097-2765(02)00740-2. [DOI] [PubMed] [Google Scholar]
  56. Narlikar Geeta J., Fan Hua-Ying, Kingston Robert E. Cooperation between complexes that regulate chromatin structure and transcription. Cell. 2002 Feb 22;108(4):475–487. doi: 10.1016/s0092-8674(02)00654-2. [DOI] [PubMed] [Google Scholar]
  57. Ng Huck Hui, Robert François, Young Richard A., Struhl Kevin. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell. 2003 Mar;11(3):709–719. doi: 10.1016/s1097-2765(03)00092-3. [DOI] [PubMed] [Google Scholar]
  58. Orlando Valerio. Polycomb, epigenomes, and control of cell identity. Cell. 2003 Mar 7;112(5):599–606. doi: 10.1016/s0092-8674(03)00157-0. [DOI] [PubMed] [Google Scholar]
  59. Papoulas O., Beek S. J., Moseley S. L., McCallum C. M., Sarte M., Shearn A., Tamkun J. W. The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development. 1998 Oct;125(20):3955–3966. doi: 10.1242/dev.125.20.3955. [DOI] [PubMed] [Google Scholar]
  60. Pignoni F., Hu B., Zavitz K. H., Xiao J., Garrity P. A., Zipursky S. L. The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell. 1997 Dec 26;91(7):881–891. doi: 10.1016/s0092-8674(00)80480-8. [DOI] [PubMed] [Google Scholar]
  61. Plaza S., Prince F., Jaeger J., Kloter U., Flister S., Benassayag C., Cribbs D., Gehring W. J. Molecular basis for the inhibition of Drosophila eye development by Antennapedia. EMBO J. 2001 Feb 15;20(4):802–811. doi: 10.1093/emboj/20.4.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Quiring R., Walldorf U., Kloter U., Gehring W. J. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science. 1994 Aug 5;265(5173):785–789. doi: 10.1126/science.7914031. [DOI] [PubMed] [Google Scholar]
  63. Rachez C., Freedman L. P. Mediator complexes and transcription. Curr Opin Cell Biol. 2001 Jun;13(3):274–280. doi: 10.1016/s0955-0674(00)00209-x. [DOI] [PubMed] [Google Scholar]
  64. Ready D. F., Hanson T. E., Benzer S. Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol. 1976 Oct 15;53(2):217–240. doi: 10.1016/0012-1606(76)90225-6. [DOI] [PubMed] [Google Scholar]
  65. Robinow S., White K. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J Neurobiol. 1991 Jul;22(5):443–461. doi: 10.1002/neu.480220503. [DOI] [PubMed] [Google Scholar]
  66. Roguev A., Schaft D., Shevchenko A., Pijnappel W. W., Wilm M., Aasland R., Stewart A. F. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 2001 Dec 17;20(24):7137–7148. doi: 10.1093/emboj/20.24.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Royet J., Finkelstein R. Establishing primordia in the Drosophila eye-antennal imaginal disc: the roles of decapentaplegic, wingless and hedgehog. Development. 1997 Dec;124(23):4793–4800. doi: 10.1242/dev.124.23.4793. [DOI] [PubMed] [Google Scholar]
  68. Santos-Rosa Helena, Schneider Robert, Bannister Andrew J., Sherriff Julia, Bernstein Bradley E., Emre N. C. Tolga, Schreiber Stuart L., Mellor Jane, Kouzarides Tony. Active genes are tri-methylated at K4 of histone H3. Nature. 2002 Sep 11;419(6905):407–411. doi: 10.1038/nature01080. [DOI] [PubMed] [Google Scholar]
  69. Sathe S. S., Harte P. J. The Drosophila extra sex combs protein contains WD motifs essential for its function as a repressor of homeotic genes. Mech Dev. 1995 Jul;52(1):77–87. doi: 10.1016/0925-4773(95)00392-e. [DOI] [PubMed] [Google Scholar]
  70. Schwartz C., Locke J., Nishida C., Kornberg T. B. Analysis of cubitus interruptus regulation in Drosophila embryos and imaginal disks. Development. 1995 Jun;121(6):1625–1635. doi: 10.1242/dev.121.6.1625. [DOI] [PubMed] [Google Scholar]
  71. Seimiya M., Gehring W. J. The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development. 2000 May;127(9):1879–1886. doi: 10.1242/dev.127.9.1879. [DOI] [PubMed] [Google Scholar]
  72. Simon J., Bornemann D., Lunde K., Schwartz C. The extra sex combs product contains WD40 repeats and its time of action implies a role distinct from other Polycomb group products. Mech Dev. 1995 Oct;53(2):197–208. doi: 10.1016/0925-4773(95)00434-3. [DOI] [PubMed] [Google Scholar]
  73. Simon J. Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr Opin Cell Biol. 1995 Jun;7(3):376–385. doi: 10.1016/0955-0674(95)80093-x. [DOI] [PubMed] [Google Scholar]
  74. Strutt D. I., Mlodzik M. The regulation of hedgehog and decapentaplegic during Drosophila eye imaginal disc development. Mech Dev. 1996 Aug;58(1-2):39–50. doi: 10.1016/s0925-4773(96)00555-2. [DOI] [PubMed] [Google Scholar]
  75. Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
  76. Tan Change, Stronach Beth, Perrimon Norbert. Roles of myosin phosphatase during Drosophila development. Development. 2003 Feb;130(4):671–681. doi: 10.1242/dev.00298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Therrien M., Morrison D. K., Wong A. M., Rubin G. M. A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics. 2000 Nov;156(3):1231–1242. doi: 10.1093/genetics/156.3.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Tio M., Moses K. The Drosophila TGF alpha homolog Spitz acts in photoreceptor recruitment in the developing retina. Development. 1997 Jan;124(2):343–351. doi: 10.1242/dev.124.2.343. [DOI] [PubMed] [Google Scholar]
  79. Treisman J. E., Luk A., Rubin G. M., Heberlein U. eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins. Genes Dev. 1997 Aug 1;11(15):1949–1962. doi: 10.1101/gad.11.15.1949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Treisman J. E., Rubin G. M. wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development. 1995 Nov;121(11):3519–3527. doi: 10.1242/dev.121.11.3519. [DOI] [PubMed] [Google Scholar]
  81. Treisman J. Drosophila homologues of the transcriptional coactivation complex subunits TRAP240 and TRAP230 are required for identical processes in eye-antennal disc development. Development. 2001 Feb;128(4):603–615. doi: 10.1242/dev.128.4.603. [DOI] [PubMed] [Google Scholar]
  82. Wang H., Cao R., Xia L., Erdjument-Bromage H., Borchers C., Tempst P., Zhang Y. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell. 2001 Dec;8(6):1207–1217. doi: 10.1016/s1097-2765(01)00405-1. [DOI] [PubMed] [Google Scholar]
  83. Wasserman J. D., Urban S., Freeman M. A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling. Genes Dev. 2000 Jul 1;14(13):1651–1663. [PMC free article] [PubMed] [Google Scholar]
  84. Wehrli M., Dougan S. T., Caldwell K., O'Keefe L., Schwartz S., Vaizel-Ohayon D., Schejter E., Tomlinson A., DiNardo S. arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature. 2000 Sep 28;407(6803):527–530. doi: 10.1038/35035110. [DOI] [PubMed] [Google Scholar]
  85. White R. A., Wilcox M. Protein products of the bithorax complex in Drosophila. Cell. 1984 Nov;39(1):163–171. doi: 10.1016/0092-8674(84)90202-2. [DOI] [PubMed] [Google Scholar]
  86. 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. 1996 Jul;122(7):2153–2162. doi: 10.1242/dev.122.7.2153. [DOI] [PubMed] [Google Scholar]
  87. Wu J., Cohen S. M. Proximal distal axis formation in the Drosophila leg: distinct functions of teashirt and homothorax in the proximal leg. Mech Dev. 2000 Jun;94(1-2):47–56. doi: 10.1016/s0925-4773(00)00311-7. [DOI] [PubMed] [Google Scholar]
  88. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES