Abstract
The initial expression of the gap gene Krüppel (Kr) occurs in a precisely bounded central region of the Drosophila blastoderm embryo. According to genetic analysis, the spatial limits of the Kr expression domain are controlled by the morphogenetic activities of the anterior organizer gene bicoid (bcd) and the anterior gap gene hunchback (hb). Using gene fusion analysis, we assayed for cis-acting sequences of the Kr gene which mediate transcriptional activation and localized gene expression in response to trans-acting factors. A 730 bp Kr control element drives gene expression in place of the endogenous Kr central domain. This cis-acting element, Kr730, is composed of bcd and hb responsive sequences. They map into regions of multiple hb and bcd protein in vitro binding sites. A 142 bp core fragment containing one low affinity hb and five medium to strong bcd protein binding sites drives gene expression in a Kr-like location in the centre of the embryo. Our results show that this fragment represents a target for the redundant activator/repressor system provided by the anterior morphogens bcd and hb.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
- Berleth T., Burri M., Thoma G., Bopp D., Richstein S., Frigerio G., Noll M., Nüsslein-Volhard C. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 1988 Jun;7(6):1749–1756. doi: 10.1002/j.1460-2075.1988.tb03004.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen S. M., Jürgens G. Mediation of Drosophila head development by gap-like segmentation genes. Nature. 1990 Aug 2;346(6283):482–485. doi: 10.1038/346482a0. [DOI] [PubMed] [Google Scholar]
- Dalton D., Chadwick R., McGinnis W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 1989 Dec;3(12A):1940–1956. doi: 10.1101/gad.3.12a.1940. [DOI] [PubMed] [Google Scholar]
- Driever W., Nüsslein-Volhard C. A gradient of bicoid protein in Drosophila embryos. Cell. 1988 Jul 1;54(1):83–93. doi: 10.1016/0092-8674(88)90182-1. [DOI] [PubMed] [Google Scholar]
- Driever W., Nüsslein-Volhard C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell. 1988 Jul 1;54(1):95–104. doi: 10.1016/0092-8674(88)90183-3. [DOI] [PubMed] [Google Scholar]
- Driever W., Nüsslein-Volhard C. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature. 1989 Jan 12;337(6203):138–143. doi: 10.1038/337138a0. [DOI] [PubMed] [Google Scholar]
- Driever W., Thoma G., Nüsslein-Volhard C. Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature. 1989 Aug 3;340(6232):363–367. doi: 10.1038/340363a0. [DOI] [PubMed] [Google Scholar]
- Eldon E. D., Pirrotta V. Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development. 1991 Feb;111(2):367–378. doi: 10.1242/dev.111.2.367. [DOI] [PubMed] [Google Scholar]
- Finkelstein R., Perrimon N. The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature. 1990 Aug 2;346(6283):485–488. doi: 10.1038/346485a0. [DOI] [PubMed] [Google Scholar]
- Frasch M., Levine M. Complementary patterns of even-skipped and fushi tarazu expression involve their differential regulation by a common set of segmentation genes in Drosophila. Genes Dev. 1987 Nov;1(9):981–995. doi: 10.1101/gad.1.9.981. [DOI] [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]
- Galas D. J., Schmitz A. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978 Sep;5(9):3157–3170. doi: 10.1093/nar/5.9.3157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gaul U., Jäckle H. Analysis of maternal effect mutant combinations elucidates regulation and function of the overlap of hunchback and Krüppel gene expression in the Drosophila blastoderm embryo. Development. 1989 Nov;107(3):651–662. doi: 10.1242/dev.107.3.651. [DOI] [PubMed] [Google Scholar]
- Gaul U., Jäckle H. Pole region-dependent repression of the Drosophila gap gene Krüppel by maternal gene products. Cell. 1987 Nov 20;51(4):549–555. doi: 10.1016/0092-8674(87)90124-3. [DOI] [PubMed] [Google Scholar]
- Gaul U., Seifert E., Schuh R., Jäckle H. Analysis of Krüppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell. 1987 Aug 14;50(4):639–647. doi: 10.1016/0092-8674(87)90037-7. [DOI] [PubMed] [Google Scholar]
- Hanes S. D., Brent R. A genetic model for interaction of the homeodomain recognition helix with DNA. Science. 1991 Jan 25;251(4992):426–430. doi: 10.1126/science.1671176. [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]
- Hoch M., Schröder C., Seifert E., Jäckle H. cis-acting control elements for Krüppel expression in the Drosophila embryo. EMBO J. 1990 Aug;9(8):2587–2595. doi: 10.1002/j.1460-2075.1990.tb07440.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hülskamp M., Pfeifle C., Tautz D. A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature. 1990 Aug 9;346(6284):577–580. doi: 10.1038/346577a0. [DOI] [PubMed] [Google Scholar]
- Hülskamp M., Schröder C., Pfeifle C., Jäckle H., Tautz D. Posterior segmentation of the Drosophila embryo in the absence of a maternal posterior organizer gene. Nature. 1989 Apr 20;338(6217):629–632. doi: 10.1038/338629a0. [DOI] [PubMed] [Google Scholar]
- Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
- Irish V., Lehmann R., Akam M. The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature. 1989 Apr 20;338(6217):646–648. doi: 10.1038/338646a0. [DOI] [PubMed] [Google Scholar]
- Kadonaga J. T., Carner K. R., Masiarz F. R., Tjian R. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell. 1987 Dec 24;51(6):1079–1090. doi: 10.1016/0092-8674(87)90594-0. [DOI] [PubMed] [Google Scholar]
- Knipple D. C., Seifert E., Rosenberg U. B., Preiss A., Jäckle H. Spatial and temporal patterns of Krüppel gene expression in early Drosophila embryos. Nature. 1985 Sep 5;317(6032):40–44. doi: 10.1038/317040a0. [DOI] [PubMed] [Google Scholar]
- Kraut R., Levine M. Mutually repressive interactions between the gap genes giant and Krüppel define middle body regions of the Drosophila embryo. Development. 1991 Feb;111(2):611–621. doi: 10.1242/dev.111.2.611. [DOI] [PubMed] [Google Scholar]
- Macdonald P. M., Struhl G. A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature. 1986 Dec 11;324(6097):537–545. doi: 10.1038/324537a0. [DOI] [PubMed] [Google Scholar]
- Muriel W. J., Cole J., Lehmann A. R. Molecular analysis of ouabain-resistant mutants of the mouse lymphoma cell line L5178Y. Mutagenesis. 1987 Sep;2(5):383–389. doi: 10.1093/mutage/2.5.383. [DOI] [PubMed] [Google Scholar]
- Nauber U., Pankratz M. J., Kienlin A., Seifert E., Klemm U., Jäckle H. Abdominal segmentation of the Drosophila embryo requires a hormone receptor-like protein encoded by the gap gene knirps. Nature. 1988 Dec 1;336(6198):489–492. doi: 10.1038/336489a0. [DOI] [PubMed] [Google Scholar]
- Nüsslein-Volhard C., Frohnhöfer H. G., Lehmann R. Determination of anteroposterior polarity in Drosophila. Science. 1987 Dec 18;238(4834):1675–1681. doi: 10.1126/science.3686007. [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]
- Pankratz M. J., Hoch M., Seifert E., Jäckle H. Krüppel requirement for knirps enhancement reflects overlapping gap gene activities in the Drosophila embryo. Nature. 1989 Sep 28;341(6240):337–340. doi: 10.1038/341337a0. [DOI] [PubMed] [Google Scholar]
- Pankratz M. J., Jäckle H. Making stripes in the Drosophila embryo. Trends Genet. 1990 Sep;6(9):287–292. doi: 10.1016/0168-9525(90)90234-w. [DOI] [PubMed] [Google Scholar]
- Pankratz M. J., Seifert E., Gerwin N., Billi B., Nauber U., Jäckle H. Gradients of Krüppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the Drosophila embryo. Cell. 1990 Apr 20;61(2):309–317. doi: 10.1016/0092-8674(90)90811-r. [DOI] [PubMed] [Google Scholar]
- Petschek J. P., Perrimon N., Mahowald A. P. Region-specific defects in l(1)giant embryos of Drosophila melanogaster. Dev Biol. 1987 Jan;119(1):175–189. doi: 10.1016/0012-1606(87)90219-3. [DOI] [PubMed] [Google Scholar]
- Reinitz J., Levine M. Control of the initiation of homeotic gene expression by the gap genes giant and tailless in Drosophila. Dev Biol. 1990 Jul;140(1):57–72. doi: 10.1016/0012-1606(90)90053-l. [DOI] [PubMed] [Google Scholar]
- Rothe M., Nauber U., Jäckle H. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 1989 Oct;8(10):3087–3094. doi: 10.1002/j.1460-2075.1989.tb08460.x. [DOI] [PMC free article] [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]
- Schröder C., Tautz D., Seifert E., Jäckle H. Differential regulation of the two transcripts from the Drosophila gap segmentation gene hunchback. EMBO J. 1988 Sep;7(9):2881–2887. doi: 10.1002/j.1460-2075.1988.tb03145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanojević D., Hoey T., Levine M. Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature. 1989 Sep 28;341(6240):331–335. doi: 10.1038/341331a0. [DOI] [PubMed] [Google Scholar]
- Struhl G., Struhl K., Macdonald P. M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell. 1989 Jun 30;57(7):1259–1273. doi: 10.1016/0092-8674(89)90062-7. [DOI] [PubMed] [Google Scholar]
- Studier F. W., Moffatt B. A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 1986 May 5;189(1):113–130. doi: 10.1016/0022-2836(86)90385-2. [DOI] [PubMed] [Google Scholar]
- Tautz D. Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature. 1988 Mar 17;332(6161):281–284. doi: 10.1038/332281a0. [DOI] [PubMed] [Google Scholar]
- Thummel C. S., Boulet A. M., Lipshitz H. D. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene. 1988 Dec 30;74(2):445–456. doi: 10.1016/0378-1119(88)90177-1. [DOI] [PubMed] [Google Scholar]
- Treisman J., Desplan C. The products of the Drosophila gap genes hunchback and Krüppel bind to the hunchback promoters. Nature. 1989 Sep 28;341(6240):335–337. doi: 10.1038/341335a0. [DOI] [PubMed] [Google Scholar]
- Warrior R., Levine M. Dose-dependent regulation of pair-rule stripes by gap proteins and the initiation of segment polarity. Development. 1990 Nov;110(3):759–767. doi: 10.1242/dev.110.3.759. [DOI] [PubMed] [Google Scholar]
- Weigel D., Jürgens G., Klingler M., Jäckle H. Two gap genes mediate maternal terminal pattern information in Drosophila. Science. 1990 Apr 27;248(4954):495–498. doi: 10.1126/science.2158673. [DOI] [PubMed] [Google Scholar]
- Weigel D., Seifert E., Reuter D., Jäckle H. Regulatory elements controlling expression of the Drosophila homeotic gene fork head. EMBO J. 1990 Apr;9(4):1199–1207. doi: 10.1002/j.1460-2075.1990.tb08227.x. [DOI] [PMC free article] [PubMed] [Google Scholar]