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. 1993 Oct;135(2):405–417. doi: 10.1093/genetics/135.2.405

Genetic Characterization of Tube and Pelle, Genes Required for Signaling between Toll and Dorsal in the Specification of the Dorsal-Ventral Pattern of the Drosophila Embryo

P M Hecht 1, K V Anderson 1
PMCID: PMC1205645  PMID: 8244004

Abstract

tube and pelle are two of the maternally transcribed genes required for dorsal-ventral patterning of the Drosophila embryo. Females homozygous for strong alleles of tube or pelle produce embryos that lack all ventral and lateral embryonic pattern elements. By analyzing the phenotypes caused by 24 pelle and 9 tube alleles, we have defined characteristic features of the two genes, including the extremely variable phenotypes of a number of tube alleles and the antimorphic character of a number of pelle alleles. Double mutant females carrying dominant ventralizing alleles of Toll and dorsalizing alleles of tube or pelle produce dorsalized embryos, suggesting that tube and pelle act downstream of the membrane protein Toll in the signaling pathway that defines the embryonic dorsal-ventral pattern. Both tube and pelle are also important zygotically for survival: at least 30% of the zygotes lacking either tube or pelle die before adult stages, while 90-95% of tube(-) pelle(-) double mutant zygotes die. We discuss the phenotypes of tube-pelle double mutants in the context of whether the two proteins interact directly.

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Selected References

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  1. Anderson K. V., Jürgens G., Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell. 1985 Oct;42(3):779–789. doi: 10.1016/0092-8674(85)90274-0. [DOI] [PubMed] [Google Scholar]
  2. Anderson K. V., Nüsslein-Volhard C. Information for the dorsal--ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature. 1984 Sep 20;311(5983):223–227. doi: 10.1038/311223a0. [DOI] [PubMed] [Google Scholar]
  3. Baeuerle P. A., Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science. 1988 Oct 28;242(4878):540–546. doi: 10.1126/science.3140380. [DOI] [PubMed] [Google Scholar]
  4. Bruder J. T., Heidecker G., Rapp U. R. Serum-, TPA-, and Ras-induced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase. Genes Dev. 1992 Apr;6(4):545–556. doi: 10.1101/gad.6.4.545. [DOI] [PubMed] [Google Scholar]
  5. Cooley L., Berg C., Spradling A. Controlling P element insertional mutagenesis. Trends Genet. 1988 Sep;4(9):254–258. doi: 10.1016/0168-9525(88)90032-7. [DOI] [PubMed] [Google Scholar]
  6. Gaul U., Mardon G., Rubin G. M. A putative Ras GTPase activating protein acts as a negative regulator of signaling by the Sevenless receptor tyrosine kinase. Cell. 1992 Mar 20;68(6):1007–1019. doi: 10.1016/0092-8674(92)90073-l. [DOI] [PubMed] [Google Scholar]
  7. Geisler R., Bergmann A., Hiromi Y., Nüsslein-Volhard C. cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the I kappa B gene family of vertebrates. Cell. 1992 Nov 13;71(4):613–621. doi: 10.1016/0092-8674(92)90595-4. [DOI] [PubMed] [Google Scholar]
  8. Gerttula S., Jin Y. S., Anderson K. V. Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. Genetics. 1988 May;119(1):123–133. doi: 10.1093/genetics/119.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Govind S., Steward R. Dorsoventral pattern formation in Drosophila: signal transduction and nuclear targeting. Trends Genet. 1991 Apr;7(4):119–125. doi: 10.1016/0168-9525(91)90456-z. [DOI] [PubMed] [Google Scholar]
  10. Greenwald I., Rubin G. M. Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells. Cell. 1992 Jan 24;68(2):271–281. doi: 10.1016/0092-8674(92)90470-w. [DOI] [PubMed] [Google Scholar]
  11. Hashimoto C., Gerttula S., Anderson K. V. Plasma membrane localization of the Toll protein in the syncytial Drosophila embryo: importance of transmembrane signaling for dorsal-ventral pattern formation. Development. 1991 Apr;111(4):1021–1028. doi: 10.1242/dev.111.4.1021. [DOI] [PubMed] [Google Scholar]
  12. Horvitz H. R., Sternberg P. W. Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva. Nature. 1991 Jun 13;351(6327):535–541. doi: 10.1038/351535a0. [DOI] [PubMed] [Google Scholar]
  13. Ip Y. T., Kraut R., Levine M., Rushlow C. A. The dorsal morphogen is a sequence-specific DNA-binding protein that interacts with a long-range repression element in Drosophila. Cell. 1991 Jan 25;64(2):439–446. doi: 10.1016/0092-8674(91)90651-e. [DOI] [PubMed] [Google Scholar]
  14. Kidd S. Characterization of the Drosophila cactus locus and analysis of interactions between cactus and dorsal proteins. Cell. 1992 Nov 13;71(4):623–635. doi: 10.1016/0092-8674(92)90596-5. [DOI] [PubMed] [Google Scholar]
  15. Leptin M., Grunewald B. Cell shape changes during gastrulation in Drosophila. Development. 1990 Sep;110(1):73–84. doi: 10.1242/dev.110.1.73. [DOI] [PubMed] [Google Scholar]
  16. Letsou A., Alexander S., Orth K., Wasserman S. A. Genetic and molecular characterization of tube, a Drosophila gene maternally required for embryonic dorsoventral polarity. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):810–814. doi: 10.1073/pnas.88.3.810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lowenstein E. J., Daly R. J., Batzer A. G., Li W., Margolis B., Lammers R., Ullrich A., Skolnik E. Y., Bar-Sagi D., Schlessinger J. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell. 1992 Aug 7;70(3):431–442. doi: 10.1016/0092-8674(92)90167-b. [DOI] [PubMed] [Google Scholar]
  18. Morrison D. K., Kaplan D. R., Escobedo J. A., Rapp U. R., Roberts T. M., Williams L. T. Direct activation of the serine/threonine kinase activity of Raf-1 through tyrosine phosphorylation by the PDGF beta-receptor. Cell. 1989 Aug 25;58(4):649–657. doi: 10.1016/0092-8674(89)90100-1. [DOI] [PubMed] [Google Scholar]
  19. Nolan G. P., Baltimore D. The inhibitory ankyrin and activator Rel proteins. Curr Opin Genet Dev. 1992 Apr;2(2):211–220. doi: 10.1016/s0959-437x(05)80276-x. [DOI] [PubMed] [Google Scholar]
  20. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Roth S., Hiromi Y., Godt D., Nüsslein-Volhard C. cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development. 1991 Jun;112(2):371–388. doi: 10.1242/dev.112.2.371. [DOI] [PubMed] [Google Scholar]
  22. Roth S., Stein D., Nüsslein-Volhard C. A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell. 1989 Dec 22;59(6):1189–1202. doi: 10.1016/0092-8674(89)90774-5. [DOI] [PubMed] [Google Scholar]
  23. Rushlow C. A., Han K., Manley J. L., Levine M. The graded distribution of the dorsal morphogen is initiated by selective nuclear transport in Drosophila. Cell. 1989 Dec 22;59(6):1165–1177. doi: 10.1016/0092-8674(89)90772-1. [DOI] [PubMed] [Google Scholar]
  24. Schmitz M. L., Henkel T., Baeuerle P. A. Proteins controlling the nuclear uptake of NF-kappa B, Rel and dorsal. Trends Cell Biol. 1991 Nov;1(5):130–137. doi: 10.1016/0962-8924(91)90118-s. [DOI] [PubMed] [Google Scholar]
  25. Schneider D. S., Hudson K. L., Lin T. Y., Anderson K. V. Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo. Genes Dev. 1991 May;5(5):797–807. doi: 10.1101/gad.5.5.797. [DOI] [PubMed] [Google Scholar]
  26. Shelton C. A., Wasserman S. A. pelle encodes a protein kinase required to establish dorsoventral polarity in the Drosophila embryo. Cell. 1993 Feb 26;72(4):515–525. doi: 10.1016/0092-8674(93)90071-w. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Stein D., Nüsslein-Volhard C. Multiple extracellular activities in Drosophila egg perivitelline fluid are required for establishment of embryonic dorsal-ventral polarity. Cell. 1992 Feb 7;68(3):429–440. doi: 10.1016/0092-8674(92)90181-b. [DOI] [PubMed] [Google Scholar]
  29. Stein D., Roth S., Vogelsang E., Nüsslein-Volhard C. The polarity of the dorsoventral axis in the Drosophila embryo is defined by an extracellular signal. Cell. 1991 May 31;65(5):725–735. doi: 10.1016/0092-8674(91)90381-8. [DOI] [PubMed] [Google Scholar]
  30. Thisse C., Perrin-Schmitt F., Stoetzel C., Thisse B. Sequence-specific transactivation of the Drosophila twist gene by the dorsal gene product. Cell. 1991 Jun 28;65(7):1191–1201. doi: 10.1016/0092-8674(91)90014-p. [DOI] [PubMed] [Google Scholar]

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