Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1995 Jun;140(2):629–641. doi: 10.1093/genetics/140.2.629

A Genetic Analysis of the Drosophila Closely Linked Interacting Genes Bulge, Argos and Soba

T Wemmer 1, C Klambt 1
PMCID: PMC1206640  PMID: 7498742

Abstract

The Drosophila gene argos encodes a diffusible protein that acts as a negative regulator of cell fate decisions. To define interacting gene products, we performed a genetic analysis of argos, which suggests the presence of several partially redundant gene functions in its immediate vicinity at the chromosomal position 73A. Dose titration experiments have identified two of these loci. One of them corresponds to the gene bulge. Loss of function bulge alleles suppress the rough eye phenotype associated with overexpression of argos; conversely, amorphic argos mutations suppress the eye phenotype seen in flies bearing a single dominant bulge allele. Recombination mapping localized bulge 0.15 cM distal to argos. A second gene, suppressor of bulge and argos (soba), corresponds to the recently described lethal complementation group 73Aj. soba alleles suppress the eye phenotypes seen in flies expressing either the dominant bulge allele or the hs-argos construct. soba resides 120 kb proximal to argos. In addition, we have identified one allele of a new gene, clown, which like soba suppresses the eye phenotypes associated with hs-argos and bulge(Dominant). clown maps on chromosome 3 at the cytological position 68CD.

Full Text

The Full Text of this article is available as a PDF (11.5 MB).

Selected References

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

  1. Belote J. M., Hoffmann F. M., McKeown M., Chorsky R. L., Baker B. S. Cytogenetic analysis of chromosome region 73AD of Drosophila melanogaster. Genetics. 1990 Aug;125(4):783–793. doi: 10.1093/genetics/125.4.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
  3. Botas J., Moscoso del Prado J., García-Bellido A. Gene-dose titration analysis in the search of trans-regulatory genes in Drosophila. EMBO J. 1982;1(3):307–310. doi: 10.1002/j.1460-2075.1982.tb01165.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Butler B., Pirrotta V., Irminger-Finger I., Nöthiger R. The sex-determining gene tra of Drosophila: molecular cloning and transformation studies. EMBO J. 1986 Dec 20;5(13):3607–3613. doi: 10.1002/j.1460-2075.1986.tb04689.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clark S. G., Lu X., Horvitz H. R. The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics. 1994 Aug;137(4):987–997. doi: 10.1093/genetics/137.4.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Daniels S. B., McCarron M., Love C., Chovnick A. Dysgenesis-induced instability of rosy locus transformation in Drosophila melanogaster: analysis of excision events and the selective recovery of control element deletions. Genetics. 1985 Jan;109(1):95–117. doi: 10.1093/genetics/109.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Delidakis C., Artavanis-Tsakonas S. The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8731–8735. doi: 10.1073/pnas.89.18.8731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elkins T., Zinn K., McAllister L., Hoffmann F. M., Goodman C. S. Genetic analysis of a Drosophila neural cell adhesion molecule: interaction of fasciclin I and Abelson tyrosine kinase mutations. Cell. 1990 Feb 23;60(4):565–575. doi: 10.1016/0092-8674(90)90660-7. [DOI] [PubMed] [Google Scholar]
  10. Fehon R. G., Kooh P. J., Rebay I., Regan C. L., Xu T., Muskavitch M. A., Artavanis-Tsakonas S. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell. 1990 May 4;61(3):523–534. doi: 10.1016/0092-8674(90)90534-l. [DOI] [PubMed] [Google Scholar]
  11. Ferguson E. L., Anderson K. V. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell. 1992 Oct 30;71(3):451–461. doi: 10.1016/0092-8674(92)90514-d. [DOI] [PubMed] [Google Scholar]
  12. Franke W. W., Krien S., Brown R. M., Jr Simultaneous glutaraldehyde-osmium tetroxide fixation with postosmication. An improved fixation procedure for electron microscopy of plant and animal cells. Histochemie. 1969;19(2):162–164. doi: 10.1007/BF00281096. [DOI] [PubMed] [Google Scholar]
  13. Freeman M., Klämbt C., Goodman C. S., Rubin G. M. The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila eye. Cell. 1992 Jun 12;69(6):963–975. doi: 10.1016/0092-8674(92)90615-j. [DOI] [PubMed] [Google Scholar]
  14. Freeman M. Misexpression of the Drosophila argos gene, a secreted regulator of cell determination. Development. 1994 Aug;120(8):2297–2304. doi: 10.1242/dev.120.8.2297. [DOI] [PubMed] [Google Scholar]
  15. Gertler F. B., Bennett R. L., Clark M. J., Hoffmann F. M. Drosophila abl tyrosine kinase in embryonic CNS axons: a role in axonogenesis is revealed through dosage-sensitive interactions with disabled. Cell. 1989 Jul 14;58(1):103–113. doi: 10.1016/0092-8674(89)90407-8. [DOI] [PubMed] [Google Scholar]
  16. Gertler F. B., Doctor J. S., Hoffmann F. M. Genetic suppression of mutations in the Drosophila abl proto-oncogene homolog. Science. 1990 May 18;248(4957):857–860. doi: 10.1126/science.2188361. [DOI] [PubMed] [Google Scholar]
  17. Geyer P. K., Green M. M., Corces V. G. Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection in Drosophila. EMBO J. 1990 Jul;9(7):2247–2256. doi: 10.1002/j.1460-2075.1990.tb07395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heitzler P., Simpson P. The choice of cell fate in the epidermis of Drosophila. Cell. 1991 Mar 22;64(6):1083–1092. doi: 10.1016/0092-8674(91)90263-x. [DOI] [PubMed] [Google Scholar]
  19. Katz W. S., Sternberg P. W. A plethora of intercellular signals during Caenorhabditis elegans development. Curr Opin Cell Biol. 1992 Dec;4(6):939–947. doi: 10.1016/0955-0674(92)90122-s. [DOI] [PubMed] [Google Scholar]
  20. Kessler D. S., Melton D. A. Vertebrate embryonic induction: mesodermal and neural patterning. Science. 1994 Oct 28;266(5185):596–604. doi: 10.1126/science.7939714. [DOI] [PubMed] [Google Scholar]
  21. Klämbt C., Goodman C. S. The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia. 1991;4(2):205–213. doi: 10.1002/glia.440040212. [DOI] [PubMed] [Google Scholar]
  22. Klämbt C., Jacobs J. R., Goodman C. S. The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell. 1991 Feb 22;64(4):801–815. doi: 10.1016/0092-8674(91)90509-w. [DOI] [PubMed] [Google Scholar]
  23. Klämbt C., Knust E., Tietze K., Campos-Ortega J. A. Closely related transcripts encoded by the neurogenic gene complex enhancer of split of Drosophila melanogaster. EMBO J. 1989 Jan;8(1):203–210. doi: 10.1002/j.1460-2075.1989.tb03365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Knust E., Schrons H., Grawe F., Campos-Ortega J. A. Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics. 1992 Oct;132(2):505–518. doi: 10.1093/genetics/132.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kretzschmar D., Brunner A., Wiersdorff V., Pflugfelder G. O., Heisenberg M., Schneuwly S. Giant lens, a gene involved in cell determination and axon guidance in the visual system of Drosophila melanogaster. EMBO J. 1992 Jul;11(7):2531–2539. doi: 10.1002/j.1460-2075.1992.tb05318.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Krämer H., Cagan R. L., Zipursky S. L. Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature. 1991 Jul 18;352(6332):207–212. doi: 10.1038/352207a0. [DOI] [PubMed] [Google Scholar]
  27. Nellen D., Affolter M., Basler K. Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell. 1994 Jul 29;78(2):225–237. doi: 10.1016/0092-8674(94)90293-3. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Penton A., Chen Y., Staehling-Hampton K., Wrana J. L., Attisano L., Szidonya J., Cassill J. A., Massagué J., Hoffmann F. M. Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell. 1994 Jul 29;78(2):239–250. doi: 10.1016/0092-8674(94)90294-1. [DOI] [PubMed] [Google Scholar]
  31. Raz E., Shilo B. Z. Dissection of the faint little ball (flb) phenotype: determination of the development of the Drosophila central nervous system by early interactions in the ectoderm. Development. 1992 Jan;114(1):113–123. doi: 10.1242/dev.114.1.113. [DOI] [PubMed] [Google Scholar]
  32. Rebay I., Fleming R. J., Fehon R. G., Cherbas L., Cherbas P., Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell. 1991 Nov 15;67(4):687–699. doi: 10.1016/0092-8674(91)90064-6. [DOI] [PubMed] [Google Scholar]
  33. Rutledge B. J., Zhang K., Bier E., Jan Y. N., Perrimon N. The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev. 1992 Aug;6(8):1503–1517. doi: 10.1101/gad.6.8.1503. [DOI] [PubMed] [Google Scholar]
  34. Saville K. J., Belote J. M. Identification of an essential gene, l(3)73Ai, with a dominant temperature-sensitive lethal allele, encoding a Drosophila proteasome subunit. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8842–8846. doi: 10.1073/pnas.90.19.8842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schejter E. D., Shilo B. Z. The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development. Cell. 1989 Mar 24;56(6):1093–1104. doi: 10.1016/0092-8674(89)90642-9. [DOI] [PubMed] [Google Scholar]
  36. Scholz H., Deatrick J., Klaes A., Klämbt C. Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins. Genetics. 1993 Oct;135(2):455–468. doi: 10.1093/genetics/135.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schrons H., Knust E., Campos-Ortega J. A. The Enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells. Genetics. 1992 Oct;132(2):481–503. doi: 10.1093/genetics/132.2.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Simon M. A., Dodson G. S., Rubin G. M. An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to sevenless and Sos proteins in vitro. Cell. 1993 Apr 9;73(1):169–177. doi: 10.1016/0092-8674(93)90169-q. [DOI] [PubMed] [Google Scholar]
  40. Sturtevant M. A., Roark M., Bier E. The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes Dev. 1993 Jun;7(6):961–973. doi: 10.1101/gad.7.6.961. [DOI] [PubMed] [Google Scholar]
  41. Tearle R. G., Belote J. M., McKeown M., Baker B. S., Howells A. J. Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics. 1989 Jul;122(3):595–606. doi: 10.1093/genetics/122.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tower J., Karpen G. H., Craig N., Spradling A. C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 1993 Feb;133(2):347–359. doi: 10.1093/genetics/133.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Velissariou V., Ashburner M. Cytogenetic and genetic mapping of a salivary gland secretion protein in Drosophila melanogaster. Chromosoma. 1981;84(2):173–185. doi: 10.1007/BF00399129. [DOI] [PubMed] [Google Scholar]
  44. Wharton K. A., Ray R. P., Gelbart W. M. An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development. 1993 Feb;117(2):807–822. doi: 10.1242/dev.117.2.807. [DOI] [PubMed] [Google Scholar]
  45. Wilson C., Pearson R. K., Bellen H. J., O'Kane C. J., Grossniklaus U., Gehring W. J. P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev. 1989 Sep;3(9):1301–1313. doi: 10.1101/gad.3.9.1301. [DOI] [PubMed] [Google Scholar]
  46. Zhang P., Spradling A. C. Efficient and dispersed local P element transposition from Drosophila females. Genetics. 1993 Feb;133(2):361–373. doi: 10.1093/genetics/133.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES