Abstract
During Drosophila embryogenesis, position along the anteroposterior axis is specified within each segment by the products of the segment-polarity genes which include wingless (wg) and gooseberry (gsb). The striped expression of these genes in each segment is initially established by the pair-rule gene products during late blastoderm. This pattern is subsequently maintained after germ band extension by interaction among the segment-polarity genes themselves. Here we show that the maintenance of gsb, a PHox gene encoding a paired-domain and a homeodomain, is controlled by the wg signal, the homolog of the murine Wnt-1 protein. A control element responsible for wg-dependent maintenance of gsb expression, gsb-late element, is separable from an element required for the initial activation of gsb by pair-rule transcription factors, gsb-early element. The significance of such a regulatory strategy is discussed with respect to the establishment and maintenance of cell states within each segment by segment-polarity genes.
Full text
PDF









Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baumgartner S., Bopp D., Burri M., Noll M. Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev. 1987 Dec;1(10):1247–1267. doi: 10.1101/gad.1.10.1247. [DOI] [PubMed] [Google Scholar]
- Bejsovec A., Martinez Arias A. Roles of wingless in patterning the larval epidermis of Drosophila. Development. 1991 Oct;113(2):471–485. doi: 10.1242/dev.113.2.471. [DOI] [PubMed] [Google Scholar]
- Bopp D., Burri M., Baumgartner S., Frigerio G., Noll M. Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell. 1986 Dec 26;47(6):1033–1040. doi: 10.1016/0092-8674(86)90818-4. [DOI] [PubMed] [Google Scholar]
- Bopp D., Jamet E., Baumgartner S., Burri M., Noll M. Isolation of two tissue-specific Drosophila paired box genes, Pox meso and Pox neuro. EMBO J. 1989 Nov;8(11):3447–3457. doi: 10.1002/j.1460-2075.1989.tb08509.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Côté S., Preiss A., Haller J., Schuh R., Kienlin A., Seifert E., Jäckle H. The gooseberry-zipper region of Drosophila: five genes encode different spatially restricted transcripts in the embryo. EMBO J. 1987 Sep;6(9):2793–2801. doi: 10.1002/j.1460-2075.1987.tb02575.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DiNardo S., Sher E., Heemskerk-Jongens J., Kassis J. A., O'Farrell P. H. Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature. 1988 Apr 14;332(6165):604–609. doi: 10.1038/332604a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frigerio G., Burri M., Bopp D., Baumgartner S., Noll M. Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell. 1986 Dec 5;47(5):735–746. doi: 10.1016/0092-8674(86)90516-7. [DOI] [PubMed] [Google Scholar]
- González F., Swales L., Bejsovec A., Skaer H., Martinez Arias A. Secretion and movement of wingless protein in the epidermis of the Drosophila embryo. Mech Dev. 1991 Aug;35(1):43–54. doi: 10.1016/0925-4773(91)90040-d. [DOI] [PubMed] [Google Scholar]
- Hama C., Ali Z., Kornberg T. B. Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 1990 Jul;4(7):1079–1093. doi: 10.1101/gad.4.7.1079. [DOI] [PubMed] [Google Scholar]
- Heemskerk J., DiNardo S., Kostriken R., O'Farrell P. H. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature. 1991 Aug 1;352(6334):404–410. doi: 10.1038/352404a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hidalgo A., Ingham P. Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development. 1990 Sep;110(1):291–301. doi: 10.1242/dev.110.1.291. [DOI] [PubMed] [Google Scholar]
- Hidalgo A. Interactions between segment polarity genes and the generation of the segmental pattern in Drosophila. Mech Dev. 1991 Sep;35(2):77–87. doi: 10.1016/0925-4773(91)90059-f. [DOI] [PubMed] [Google Scholar]
- Hiromi Y., Gehring W. J. Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell. 1987 Sep 11;50(6):963–974. doi: 10.1016/0092-8674(87)90523-x. [DOI] [PubMed] [Google Scholar]
- Hiromi Y., Kuroiwa A., Gehring W. J. Control elements of the Drosophila segmentation gene fushi tarazu. Cell. 1985 Dec;43(3 Pt 2):603–613. doi: 10.1016/0092-8674(85)90232-6. [DOI] [PubMed] [Google Scholar]
- Hultmark D., Klemenz R., Gehring W. J. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell. 1986 Feb 14;44(3):429–438. doi: 10.1016/0092-8674(86)90464-2. [DOI] [PubMed] [Google Scholar]
- Ingham P. W., Baker N. E., Martinez-Arias A. Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature. 1988 Jan 7;331(6151):73–75. doi: 10.1038/331073a0. [DOI] [PubMed] [Google Scholar]
- Ingham P. W., Martinez Arias A. Boundaries and fields in early embryos. Cell. 1992 Jan 24;68(2):221–235. doi: 10.1016/0092-8674(92)90467-q. [DOI] [PubMed] [Google Scholar]
- Ingham P. W., Taylor A. M., Nakano Y. Role of the Drosophila patched gene in positional signalling. Nature. 1991 Sep 12;353(6340):184–187. doi: 10.1038/353184a0. [DOI] [PubMed] [Google Scholar]
- Kassis J. A. Spatial and temporal control elements of the Drosophila engrailed gene. Genes Dev. 1990 Mar;4(3):433–443. doi: 10.1101/gad.4.3.433. [DOI] [PubMed] [Google Scholar]
- Klemenz R., Weber U., Gehring W. J. The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res. 1987 May 26;15(10):3947–3959. doi: 10.1093/nar/15.10.3947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lawrence P. A., Johnston P., Macdonald P., Struhl G. Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes. 1987 Jul 30-Aug 5Nature. 328(6129):440–442. doi: 10.1038/328440a0. [DOI] [PubMed] [Google Scholar]
- Martinez-Arias A., Lawrence P. A. Parasegments and compartments in the Drosophila embryo. Nature. 1985 Feb 21;313(6004):639–642. doi: 10.1038/313639a0. [DOI] [PubMed] [Google Scholar]
- Martizez Arias A., Baker N. E., Ingham P. W. Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development. 1988 May;103(1):157–170. doi: 10.1242/dev.103.1.157. [DOI] [PubMed] [Google Scholar]
- Melton D. A. Pattern formation during animal development. Science. 1991 Apr 12;252(5003):234–241. doi: 10.1126/science.1672778. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Peifer M., Rauskolb C., Williams M., Riggleman B., Wieschaus E. The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation. Development. 1991 Apr;111(4):1029–1043. doi: 10.1242/dev.111.4.1029. [DOI] [PubMed] [Google Scholar]
- Peifer M., Wieschaus E. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell. 1990 Dec 21;63(6):1167–1176. doi: 10.1016/0092-8674(90)90413-9. [DOI] [PubMed] [Google Scholar]
- Riggleman B., Schedl P., Wieschaus E. Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless. Cell. 1990 Nov 2;63(3):549–560. doi: 10.1016/0092-8674(90)90451-j. [DOI] [PubMed] [Google Scholar]
- Rijsewijk F., Schuermann M., Wagenaar E., Parren P., Weigel D., Nusse R. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell. 1987 Aug 14;50(4):649–657. doi: 10.1016/0092-8674(87)90038-9. [DOI] [PubMed] [Google Scholar]
- Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
- Siegfried E., Chou T. B., Perrimon N. wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell. 1992 Dec 24;71(7):1167–1179. doi: 10.1016/s0092-8674(05)80065-0. [DOI] [PubMed] [Google Scholar]
- St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
- van den Heuvel M., Nusse R., Johnston P., Lawrence P. A. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell. 1989 Nov 17;59(4):739–749. doi: 10.1016/0092-8674(89)90020-2. [DOI] [PubMed] [Google Scholar]