Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Mar;160(3):1035–1050. doi: 10.1093/genetics/160.3.1035

A misexpression study examining dorsal thorax formation in Drosophila melanogaster.

María Teresa Peña-Rangel 1, Isabel Rodriguez 1, Juan Rafael Riesgo-Escovar 1
PMCID: PMC1462010  PMID: 11901120

Abstract

We studied thorax formation in Drosophila melanogaster using a misexpression screen with EP lines and thoracic Gal4 drivers that provide a genetically sensitized background. We identified 191 interacting lines showing alterations of thoracic bristles (number and/or location), thorax and scutellum malformations, lethality, or suppression of the thoracic phenotype used in the screen. We analyzed these lines and showed that known genes with different functional roles (selector, prepattern, proneural, cell cycle regulation, lineage restriction, signaling pathways, transcriptional control, and chromatin organization) are among the modifier lines. A few lines have previously been identified in thorax formation, but others, such as chromatin-remodeling complex genes, are novel. However, most of the interacting loci are uncharacterized, providing a wealth of new genetic data. We also describe one such novel line, poco pelo (ppo), where both misexpression and loss-of-function phenotypes are similar: loss of bristles and scutellum malformation.

Full Text

The Full Text of this article is available as a PDF (272.9 KB).

Selected References

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

  1. Abdelilah-Seyfried S., Chan Y. M., Zeng C., Justice N. J., Younger-Shepherd S., Sharp L. E., Barbel S., Meadows S. A., Jan L. Y., Jan Y. N. A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics. 2000 Jun;155(2):733–752. doi: 10.1093/genetics/155.2.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  3. Agnès F., Suzanne M., Noselli S. The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development. 1999 Dec;126(23):5453–5462. doi: 10.1242/dev.126.23.5453. [DOI] [PubMed] [Google Scholar]
  4. Ashburner M., Thompson P., Roote J., Lasko P. F., Grau Y., el Messal M., Roth S., Simpson P. The genetics of a small autosomal region of Drosophila melanogaster containing the structural gene for alcohol dehydrogenase. VII. Characterization of the region around the snail and cactus loci. Genetics. 1990 Nov;126(3):679–694. doi: 10.1093/genetics/126.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blair S. S. Compartments and appendage development in Drosophila. Bioessays. 1995 Apr;17(4):299–309. doi: 10.1002/bies.950170406. [DOI] [PubMed] [Google Scholar]
  6. Calleja M., Herranz H., Estella C., Casal J., Lawrence P., Simpson P., Morata G. Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development. 2000 Sep;127(18):3971–3980. doi: 10.1242/dev.127.18.3971. [DOI] [PubMed] [Google Scholar]
  7. Calleja M., Moreno E., Pelaz S., Morata G. Visualization of gene expression in living adult Drosophila. Science. 1996 Oct 11;274(5285):252–255. doi: 10.1126/science.274.5285.252. [DOI] [PubMed] [Google Scholar]
  8. Campbell S. D., Duttaroy A., Katzen A. L., Chovnick A. Cloning and characterization of the scalloped region of Drosophila melanogaster. Genetics. 1991 Feb;127(2):367–380. doi: 10.1093/genetics/127.2.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Campbell S., Inamdar M., Rodrigues V., Raghavan V., Palazzolo M., Chovnick A. The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila. Genes Dev. 1992 Mar;6(3):367–379. doi: 10.1101/gad.6.3.367. [DOI] [PubMed] [Google Scholar]
  10. Campuzano S., Modolell J. Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 1992 Jun;8(6):202–208. doi: 10.1016/0168-9525(92)90234-u. [DOI] [PubMed] [Google Scholar]
  11. Chen X., Fischer J. A. In vivo Structure/Function analysis of the Drosophila fat facets deubiquitinating enzyme gene. Genetics. 2000 Dec;156(4):1829–1836. doi: 10.1093/genetics/156.4.1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen Y., Struhl G. In vivo evidence that Patched and Smoothened constitute distinct binding and transducing components of a Hedgehog receptor complex. Development. 1998 Dec;125(24):4943–4948. doi: 10.1242/dev.125.24.4943. [DOI] [PubMed] [Google Scholar]
  13. Chou T. B., Perrimon N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics. 1996 Dec;144(4):1673–1679. doi: 10.1093/genetics/144.4.1673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clifford R. J., Schüpbach T. Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics. 1989 Dec;123(4):771–787. doi: 10.1093/genetics/123.4.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cohen B., McGuffin M. E., Pfeifle C., Segal D., Cohen S. M. apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev. 1992 May;6(5):715–729. doi: 10.1101/gad.6.5.715. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Edgar B. A., Lehman D. A., O'Farrell P. H. Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. Development. 1994 Nov;120(11):3131–3143. doi: 10.1242/dev.120.11.3131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ellis H. M., Spann D. R., Posakony J. W. extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell. 1990 Apr 6;61(1):27–38. doi: 10.1016/0092-8674(90)90212-w. [DOI] [PubMed] [Google Scholar]
  19. Fernandez-Funez P., Nino-Rosales M. L., de Gouyon B., She W. C., Luchak J. M., Martinez P., Turiegano E., Benito J., Capovilla M., Skinner P. J. Identification of genes that modify ataxin-1-induced neurodegeneration. Nature. 2000 Nov 2;408(6808):101–106. doi: 10.1038/35040584. [DOI] [PubMed] [Google Scholar]
  20. Gomez-Skarmeta J. L., Diez del Corral R., de la Calle-Mustienes E., Ferré-Marcó D., Modolell J. Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell. 1996 Apr 5;85(1):95–105. doi: 10.1016/s0092-8674(00)81085-5. [DOI] [PubMed] [Google Scholar]
  21. Haenlin M., Cubadda Y., Blondeau F., Heitzler P., Lutz Y., Simpson P., Ramain P. Transcriptional activity of pannier is regulated negatively by heterodimerization of the GATA DNA-binding domain with a cofactor encoded by the u-shaped gene of Drosophila. Genes Dev. 1997 Nov 15;11(22):3096–3108. doi: 10.1101/gad.11.22.3096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Halder G., Polaczyk P., Kraus M. E., Hudson A., Kim J., Laughon A., Carroll S. The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila. Genes Dev. 1998 Dec 15;12(24):3900–3909. doi: 10.1101/gad.12.24.3900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hayashi S., Hirose S., Metcalfe T., Shirras A. D. Control of imaginal cell development by the escargot gene of Drosophila. Development. 1993 May;118(1):105–115. doi: 10.1242/dev.118.1.105. [DOI] [PubMed] [Google Scholar]
  24. Heitzler P., Haenlin M., Ramain P., Calleja M., Simpson P. A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and bristle positioning in Drosophila. Genetics. 1996 Jul;143(3):1271–1286. doi: 10.1093/genetics/143.3.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Huang A. M., Rubin G. M. A misexpression screen identifies genes that can modulate RAS1 pathway signaling in Drosophila melanogaster. Genetics. 2000 Nov;156(3):1219–1230. doi: 10.1093/genetics/156.3.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ito T., Bulger M., Pazin M. J., Kobayashi R., Kadonaga J. T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell. 1997 Jul 11;90(1):145–155. doi: 10.1016/s0092-8674(00)80321-9. [DOI] [PubMed] [Google Scholar]
  27. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kingston R. E., Narlikar G. J. ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev. 1999 Sep 15;13(18):2339–2352. doi: 10.1101/gad.13.18.2339. [DOI] [PubMed] [Google Scholar]
  29. Lehming N., Le Saux A., Schüller J., Ptashne M. Chromatin components as part of a putative transcriptional repressing complex. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7322–7326. doi: 10.1073/pnas.95.13.7322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lundgren S. E., Callahan C. A., Thor S., Thomas J. B. Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development. 1995 Jun;121(6):1769–1773. doi: 10.1242/dev.121.6.1769. [DOI] [PubMed] [Google Scholar]
  31. Maniatis T. A ubiquitin ligase complex essential for the NF-kappaB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev. 1999 Mar 1;13(5):505–510. doi: 10.1101/gad.13.5.505. [DOI] [PubMed] [Google Scholar]
  32. Martin-Blanco E., Pastor-Pareja J. C., Garcia-Bellido A. JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):7888–7893. doi: 10.1073/pnas.97.14.7888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Milán M., Campuzano S., García-Bellido A. Developmental parameters of cell death in the wing disc of Drosophila. Proc Natl Acad Sci U S A. 1997 May 27;94(11):5691–5696. doi: 10.1073/pnas.94.11.5691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mosrin-Huaman C., Canaple L., Locker D., Decoville M. DSP1 gene of Drosophila melanogaster encodes an HMG-domain protein that plays multiple roles in development. Dev Genet. 1998;23(4):324–334. doi: 10.1002/(SICI)1520-6408(1998)23:4<324::AID-DVG7>3.0.CO;2-T. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980 Oct 30;287(5785):795–801. doi: 10.1038/287795a0. [DOI] [PubMed] [Google Scholar]
  37. Olivier J. P., Raabe T., Henkemeyer M., Dickson B., Mbamalu G., Margolis B., Schlessinger J., Hafen E., Pawson T. A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell. 1993 Apr 9;73(1):179–191. doi: 10.1016/0092-8674(93)90170-u. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Pecasse F., Beck Y., Ruiz C., Richards G. Krüppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis. Dev Biol. 2000 May 1;221(1):53–67. doi: 10.1006/dbio.2000.9687. [DOI] [PubMed] [Google Scholar]
  40. Phillips R. G., Warner N. L., Whittle J. R. Wingless signaling leads to an asymmetric response to decapentaplegic-dependent signaling during sense organ patterning on the notum of Drosophila melanogaster. Dev Biol. 1999 Mar 1;207(1):150–162. doi: 10.1006/dbio.1998.9149. [DOI] [PubMed] [Google Scholar]
  41. Posakony J. W. Nature versus nurture: asymmetric cell divisions in Drosophila bristle development. Cell. 1994 Feb 11;76(3):415–418. doi: 10.1016/0092-8674(94)90105-8. [DOI] [PubMed] [Google Scholar]
  42. Riesgo-Escovar J. R., Hafen E. Common and distinct roles of DFos and DJun during Drosophila development. Science. 1997 Oct 24;278(5338):669–672. doi: 10.1126/science.278.5338.669. [DOI] [PubMed] [Google Scholar]
  43. Rørth P. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12418–12422. doi: 10.1073/pnas.93.22.12418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Sato M., Kojima T., Michiue T., Saigo K. Bar homeobox genes are latitudinal prepattern genes in the developing Drosophila notum whose expression is regulated by the concerted functions of decapentaplegic and wingless. Development. 1999 Apr;126(7):1457–1466. doi: 10.1242/dev.126.7.1457. [DOI] [PubMed] [Google Scholar]
  46. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  47. Tomoyasu Y., Nakamura M., Ueno N. Role of dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster. Development. 1998 Nov;125(21):4215–4224. doi: 10.1242/dev.125.21.4215. [DOI] [PubMed] [Google Scholar]
  48. Varga-Weisz P. D., Wilm M., Bonte E., Dumas K., Mann M., Becker P. B. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature. 1997 Aug 7;388(6642):598–602. doi: 10.1038/41587. [DOI] [PubMed] [Google Scholar]
  49. Verheyen E. M., Purcell K. J., Fortini M. E., Artavanis-Tsakonas S. Analysis of dominant enhancers and suppressors of activated Notch in Drosophila. Genetics. 1996 Nov;144(3):1127–1141. doi: 10.1093/genetics/144.3.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Winick J., Abel T., Leonard M. W., Michelson A. M., Chardon-Loriaux I., Holmgren R. A., Maniatis T., Engel J. D. A GATA family transcription factor is expressed along the embryonic dorsoventral axis in Drosophila melanogaster. Development. 1993 Dec;119(4):1055–1065. doi: 10.1242/dev.119.4.1055. [DOI] [PubMed] [Google Scholar]
  51. Zeitlinger J., Bohmann D. Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development. 1999 Sep;126(17):3947–3956. doi: 10.1242/dev.126.17.3947. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES