Skip to main content
Genetics logoLink to Genetics
. 2000 Nov;156(3):1203–1217. doi: 10.1093/genetics/156.3.1203

A screen for dominant modifiers of ro(Dom), a mutation that disrupts morphogenetic furrow progression in Drosophila, identifies groucho and hairless as regulators of atonal expression.

F Chanut 1, A Luk 1, U Heberlein 1
PMCID: PMC1461342  PMID: 11063695

Abstract

ro(Dom) is a dominant allele of rough (ro) that results in reduced eye size due to premature arrest in morphogenetic furrow (MF) progression. We found that the ro(Dom) stop-furrow phenotype was sensitive to the dosage of genes known to affect retinal differentiation, in particular members of the hedgehog (hh) signaling cascade. We demonstrate that ro(Dom) interferes with Hh's ability to induce the retina-specific proneural gene atonal (ato) in the MF and that normal eye size can be restored by providing excess Ato protein. We used ro(Dom) as a sensitive genetic background in which to identify mutations that affect hh signal transduction or regulation of ato expression. In addition to mutations in several unknown loci, we recovered multiple alleles of groucho (gro) and Hairless (H). Analysis of their phenotypes in somatic clones suggests that both normally act to restrict neuronal cell fate in the retina, although they control different aspects of ato's complex expression pattern.

Full Text

The Full Text of this article is available as a PDF (1.0 MB).

Selected References

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

  1. Alcedo J., Ayzenzon M., Von Ohlen T., Noll M., Hooper J. E. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell. 1996 Jul 26;86(2):221–232. doi: 10.1016/s0092-8674(00)80094-x. [DOI] [PubMed] [Google Scholar]
  2. Alcedo J., Noll M. Hedgehog and its patched-smoothened receptor complex: a novel signalling mechanism at the cell surface. Biol Chem. 1997 Jul;378(7):583–590. doi: 10.1515/bchm.1997.378.7.583. [DOI] [PubMed] [Google Scholar]
  3. Aza-Blanc P., Ramírez-Weber F. A., Laget M. P., Schwartz C., Kornberg T. B. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell. 1997 Jun 27;89(7):1043–1053. doi: 10.1016/s0092-8674(00)80292-5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Baker N. E., Yu S., Han D. Evolution of proneural atonal expression during distinct regulatory phases in the developing Drosophila eye. Curr Biol. 1996 Oct 1;6(10):1290–1301. doi: 10.1016/s0960-9822(02)70715-x. [DOI] [PubMed] [Google Scholar]
  6. Baker N. E., Zitron A. E. Drosophila eye development: Notch and Delta amplify a neurogenic pattern conferred on the morphogenetic furrow by scabrous. Mech Dev. 1995 Feb;49(3):173–189. doi: 10.1016/0925-4773(94)00314-d. [DOI] [PubMed] [Google Scholar]
  7. Bang A. G., Bailey A. M., Posakony J. W. Hairless promotes stable commitment to the sensory organ precursor cell fate by negatively regulating the activity of the Notch signaling pathway. Dev Biol. 1995 Dec;172(2):479–494. doi: 10.1006/dbio.1995.8033. [DOI] [PubMed] [Google Scholar]
  8. Bang A. G., Hartenstein V., Posakony J. W. Hairless is required for the development of adult sensory organ precursor cells in Drosophila. Development. 1991 Jan;111(1):89–104. doi: 10.1242/dev.111.1.89. [DOI] [PubMed] [Google Scholar]
  9. Bang A. G., Posakony J. W. The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development. Genes Dev. 1992 Sep;6(9):1752–1769. doi: 10.1101/gad.6.9.1752. [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. Borod E. R., Heberlein U. Mutual regulation of decapentaplegic and hedgehog during the initiation of differentiation in the Drosophila retina. Dev Biol. 1998 May 15;197(2):187–197. doi: 10.1006/dbio.1998.8888. [DOI] [PubMed] [Google Scholar]
  12. Brown N. L., Sattler C. A., Paddock S. W., Carroll S. B. Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell. 1995 Mar 24;80(6):879–887. doi: 10.1016/0092-8674(95)90291-0. [DOI] [PubMed] [Google Scholar]
  13. Capdevila J., Guerrero I. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 1994 Oct 3;13(19):4459–4468. doi: 10.1002/j.1460-2075.1994.tb06768.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Carrera P., Abrell S., Kerber B., Walldorf U., Preiss A., Hoch M., Jäckle H. A modifier screen in the eye reveals control genes for Krüppel activity in the Drosophila embryo. Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10779–10784. doi: 10.1073/pnas.95.18.10779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chanut F., Heberlein U. Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development. 1997 Jan;124(2):559–567. doi: 10.1242/dev.124.2.559. [DOI] [PubMed] [Google Scholar]
  16. Chanut F., Heberlein U. Role of the morphogenetic furrow in establishing polarity in the Drosophila eye. Development. 1995 Dec;121(12):4085–4094. doi: 10.1242/dev.121.12.4085. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Dokucu M. E., Zipursky S. L., Cagan R. L. Atonal, rough and the resolution of proneural clusters in the developing Drosophila retina. Development. 1996 Dec;122(12):4139–4147. doi: 10.1242/dev.122.12.4139. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Domínguez M., Hafen E. Hedgehog directly controls initiation and propagation of retinal differentiation in the Drosophila eye. Genes Dev. 1997 Dec 1;11(23):3254–3264. doi: 10.1101/gad.11.23.3254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Domínguez M., Wasserman J. D., Freeman M. Multiple functions of the EGF receptor in Drosophila eye development. Curr Biol. 1998 Sep 24;8(19):1039–1048. doi: 10.1016/s0960-9822(98)70441-5. [DOI] [PubMed] [Google Scholar]
  22. Fischer-Vize J. A., Vize P. D., Rubin G. M. A unique mutation in the Enhancer of split gene complex affects the fates of the mystery cells in the developing Drosophila eye. Development. 1992 May;115(1):89–101. doi: 10.1242/dev.115.1.89. [DOI] [PubMed] [Google Scholar]
  23. Fisher A. L., Caudy M. Groucho proteins: transcriptional corepressors for specific subsets of DNA-binding transcription factors in vertebrates and invertebrates. Genes Dev. 1998 Jul 1;12(13):1931–1940. doi: 10.1101/gad.12.13.1931. [DOI] [PubMed] [Google Scholar]
  24. Freeman M. Cell determination strategies in the Drosophila eye. Development. 1997 Jan;124(2):261–270. doi: 10.1242/dev.124.2.261. [DOI] [PubMed] [Google Scholar]
  25. Go M. J., Artavanis-Tsakonas S. A genetic screen for novel components of the notch signaling pathway during Drosophila bristle development. Genetics. 1998 Sep;150(1):211–220. doi: 10.1093/genetics/150.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Golic K. G., Lindquist S. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell. 1989 Nov 3;59(3):499–509. doi: 10.1016/0092-8674(89)90033-0. [DOI] [PubMed] [Google Scholar]
  27. Golic K. G. Site-specific recombination between homologous chromosomes in Drosophila. Science. 1991 May 17;252(5008):958–961. doi: 10.1126/science.2035025. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Heberlein U., Singh C. M., Luk A. Y., Donohoe T. J. Growth and differentiation in the Drosophila eye coordinated by hedgehog. Nature. 1995 Feb 23;373(6516):709–711. doi: 10.1038/373709a0. [DOI] [PubMed] [Google Scholar]
  31. Heberlein U., Wolff T., Rubin G. M. The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell. 1993 Dec 3;75(5):913–926. doi: 10.1016/0092-8674(93)90535-x. [DOI] [PubMed] [Google Scholar]
  32. Heitzler P., Bourouis M., Ruel L., Carteret C., Simpson P. Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila. Development. 1996 Jan;122(1):161–171. doi: 10.1242/dev.122.1.161. [DOI] [PubMed] [Google Scholar]
  33. Hepker J., Wang Q. T., Motzny C. K., Holmgren R., Orenic T. V. Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development. 1997 Jan;124(2):549–558. doi: 10.1242/dev.124.2.549. [DOI] [PubMed] [Google Scholar]
  34. Huang Y., Fischer-Vize J. A. Undifferentiated cells in the developing Drosophila eye influence facet assembly and require the Fat facets ubiquitin-specific protease. Development. 1996 Oct;122(10):3207–3216. doi: 10.1242/dev.122.10.3207. [DOI] [PubMed] [Google Scholar]
  35. Jarman A. P., Grell E. H., Ackerman L., Jan L. Y., Jan Y. N. Atonal is the proneural gene for Drosophila photoreceptors. Nature. 1994 Jun 2;369(6479):398–400. doi: 10.1038/369398a0. [DOI] [PubMed] [Google Scholar]
  36. Jarman A. P., Sun Y., Jan L. Y., Jan Y. N. Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development. 1995 Jul;121(7):2019–2030. doi: 10.1242/dev.121.7.2019. [DOI] [PubMed] [Google Scholar]
  37. Jiménez G., Paroush Z., Ish-Horowicz D. Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev. 1997 Nov 15;11(22):3072–3082. doi: 10.1101/gad.11.22.3072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Karim F. D., Chang H. C., Therrien M., Wassarman D. A., Laverty T., Rubin G. M. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics. 1996 May;143(1):315–329. doi: 10.1093/genetics/143.1.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Karim F. D., Chang H. C., Therrien M., Wassarman D. A., Laverty T., Rubin G. M. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics. 1996 May;143(1):315–329. doi: 10.1093/genetics/143.1.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kimmel B. E., Heberlein U., Rubin G. M. The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev. 1990 May;4(5):712–727. doi: 10.1101/gad.4.5.712. [DOI] [PubMed] [Google Scholar]
  41. Kumar J. P., Tio M., Hsiung F., Akopyan S., Gabay L., Seger R., Shilo B. Z., Moses K. Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development. 1998 Oct;125(19):3875–3885. doi: 10.1242/dev.125.19.3875. [DOI] [PubMed] [Google Scholar]
  42. Lee E. C., Hu X., Yu S. Y., Baker N. E. The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol Cell Biol. 1996 Mar;16(3):1179–1188. doi: 10.1128/mcb.16.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lee J. J., von Kessler D. P., Parks S., Beachy P. A. Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell. 1992 Oct 2;71(1):33–50. doi: 10.1016/0092-8674(92)90264-d. [DOI] [PubMed] [Google Scholar]
  44. Leptin M. Gastrulation in Drosophila: the logic and the cellular mechanisms. EMBO J. 1999 Jun 15;18(12):3187–3192. doi: 10.1093/emboj/18.12.3187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ligoxygakis P., Yu S. Y., Delidakis C., Baker N. E. A subset of notch functions during Drosophila eye development require Su(H) and the E(spl) gene complex. Development. 1998 Aug;125(15):2893–2900. doi: 10.1242/dev.125.15.2893. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. Mohler J., Vani K. Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development. 1992 Aug;115(4):957–971. doi: 10.1242/dev.115.4.957. [DOI] [PubMed] [Google Scholar]
  49. Noselli S., Agnès F. Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr Opin Genet Dev. 1999 Aug;9(4):466–472. doi: 10.1016/S0959-437X(99)80071-9. [DOI] [PubMed] [Google Scholar]
  50. Oellers N., Dehio M., Knust E. bHLH proteins encoded by the Enhancer of split complex of Drosophila negatively interfere with transcriptional activation mediated by proneural genes. Mol Gen Genet. 1994 Sep 1;244(5):465–473. doi: 10.1007/BF00583897. [DOI] [PubMed] [Google Scholar]
  51. Orenic T. V., Slusarski D. C., Kroll K. L., Holmgren R. A. Cloning and characterization of the segment polarity gene cubitus interruptus Dominant of Drosophila. Genes Dev. 1990 Jun;4(6):1053–1067. doi: 10.1101/gad.4.6.1053. [DOI] [PubMed] [Google Scholar]
  52. Paroush Z., Finley R. L., Jr, Kidd T., Wainwright S. M., Ingham P. W., Brent R., Ish-Horowicz D. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell. 1994 Dec 2;79(5):805–815. doi: 10.1016/0092-8674(94)90070-1. [DOI] [PubMed] [Google Scholar]
  53. Phillips R. G., Roberts I. J., Ingham P. W., Whittle J. R. The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs. Development. 1990 Sep;110(1):105–114. doi: 10.1242/dev.110.1.105. [DOI] [PubMed] [Google Scholar]
  54. Price J. V., Savenye E. D., Lum D., Breitkreutz A. Dominant enhancers of Egfr in Drosophila melanogaster: genetic links between the Notch and Egfr signaling pathways. Genetics. 1997 Nov;147(3):1139–1153. doi: 10.1093/genetics/147.3.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. 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]
  56. Rebay I., Chen F., Hsiao F., Kolodziej P. A., Kuang B. H., Laverty T., Suh C., Voas M., Williams A., Rubin G. M. A genetic screen for novel components of the Ras/Mitogen-activated protein kinase signaling pathway that interact with the yan gene of Drosophila identifies split ends, a new RNA recognition motif-containing protein. Genetics. 2000 Feb;154(2):695–712. doi: 10.1093/genetics/154.2.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. 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]
  58. Rørth P., Szabo K., Bailey A., Laverty T., Rehm J., Rubin G. M., Weigmann K., Milán M., Benes V., Ansorge W. Systematic gain-of-function genetics in Drosophila. Development. 1998 Mar;125(6):1049–1057. doi: 10.1242/dev.125.6.1049. [DOI] [PubMed] [Google Scholar]
  59. Schweisguth F., Posakony J. W. Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis. Development. 1994 Jun;120(6):1433–1441. doi: 10.1242/dev.120.6.1433. [DOI] [PubMed] [Google Scholar]
  60. Schweisguth F., Posakony J. W. Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates. Cell. 1992 Jun 26;69(7):1199–1212. doi: 10.1016/0092-8674(92)90641-o. [DOI] [PubMed] [Google Scholar]
  61. Sekelsky J. J., McKim K. S., Messina L., French R. L., Hurley W. D., Arbel T., Chin G. M., Deneen B., Force S. J., Hari K. L. Identification of novel Drosophila meiotic genes recovered in a P-element screen. Genetics. 1999 Jun;152(2):529–542. doi: 10.1093/genetics/152.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Smith J. L., Schoenwolf G. C. Getting organized: new insights into the organizer of higher vertebrates. Curr Top Dev Biol. 1998;40:79–110. doi: 10.1016/s0070-2153(08)60365-8. [DOI] [PubMed] [Google Scholar]
  63. Spencer S. A., Powell P. A., Miller D. T., Cagan R. L. Regulation of EGF receptor signaling establishes pattern across the developing Drosophila retina. Development. 1998 Dec;125(23):4777–4790. doi: 10.1242/dev.125.23.4777. [DOI] [PubMed] [Google Scholar]
  64. Staehling-Hampton K., Ciampa P. J., Brook A., Dyson N. A genetic screen for modifiers of E2F in Drosophila melanogaster. Genetics. 1999 Sep;153(1):275–287. doi: 10.1093/genetics/153.1.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Strutt D. I., Mlodzik M. Hedgehog is an indirect regulator of morphogenetic furrow progression in the Drosophila eye disc. Development. 1997 Sep;124(17):3233–3240. doi: 10.1242/dev.124.17.3233. [DOI] [PubMed] [Google Scholar]
  66. Sun Y., Jan L. Y., Jan Y. N. Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development. 1998 Sep;125(18):3731–3740. doi: 10.1242/dev.125.18.3731. [DOI] [PubMed] [Google Scholar]
  67. Tomlinson A., Kimmel B. E., Rubin G. M. rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye. Cell. 1988 Dec 2;55(5):771–784. doi: 10.1016/0092-8674(88)90133-x. [DOI] [PubMed] [Google Scholar]
  68. Tomlinson A., Ready D. F. Neuronal differentiation in Drosophila ommatidium. Dev Biol. 1987 Apr;120(2):366–376. doi: 10.1016/0012-1606(87)90239-9. [DOI] [PubMed] [Google Scholar]
  69. Tomlinson A. The cellular dynamics of pattern formation in the eye of Drosophila. J Embryol Exp Morphol. 1985 Oct;89:313–331. [PubMed] [Google Scholar]
  70. Treisman J. E., Lai Z. C., Rubin G. M. Shortsighted acts in the decapentaplegic pathway in Drosophila eye development and has homology to a mouse TGF-beta-responsive gene. Development. 1995 Sep;121(9):2835–2845. doi: 10.1242/dev.121.9.2835. [DOI] [PubMed] [Google Scholar]
  71. 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]
  72. Vincent J. P., Girdham C. H., O'Farrell P. H. A cell-autonomous, ubiquitous marker for the analysis of Drosophila genetic mosaics. Dev Biol. 1994 Jul;164(1):328–331. doi: 10.1006/dbio.1994.1203. [DOI] [PubMed] [Google Scholar]
  73. Vázquez M., Moore L., Kennison J. A. The trithorax group gene osa encodes an ARID-domain protein that genetically interacts with the brahma chromatin-remodeling factor to regulate transcription. Development. 1999 Feb;126(4):733–742. doi: 10.1242/dev.126.4.733. [DOI] [PubMed] [Google Scholar]
  74. Wehrli M., Tomlinson A. Epithelial planar polarity in the developing Drosophila eye. Development. 1995 Aug;121(8):2451–2459. doi: 10.1242/dev.121.8.2451. [DOI] [PubMed] [Google Scholar]
  75. 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]
  76. de Celis J. F., Ruiz-Gómez M. groucho and hedgehog regulate engrailed expression in the anterior compartment of the Drosophila wing. Development. 1995 Oct;121(10):3467–3476. doi: 10.1242/dev.121.10.3467. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES