Abstract
In Drosophila embryos, anterior-posterior positional identities are set and maintained by the expression boundaries of homeotic selector genes. The establishment of the initial expression boundaries of the homeotic genes are in turn dependent on earlier acting patterning genes of Drosophila. To define the combinations of early genes that are required to establish a unique blastoderm stripe of expression of the homeotic gene Deformed, we have analysed single and double patterning mutants and heat shock promoter fusion constructs that ectopically express early acting regulators. We find that the activation of Deformed is dependent on combinatorial input from at least three levels of the early hierarchy. The simplest activation code sufficient to establish Deformed expression, given the absence of negative regulators such as fushi-tarazu, consists of a moderate level of expression from the coordinate gene bicoid, in combination with expression from both the gap gene hunchback, and the pair-rule gene even-skipped. In addition, the activation code for Deformed is redundant; other pair-rule genes in addition to even-skipped can apparently act in combination with bicoid and hunchback to activate Deformed.
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.
- 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]
- Carroll S. B., DiNardo S., O'Farrell P. H., White R. A., Scott M. P. Temporal and spatial relationships between segmentation and homeotic gene expression in Drosophila embryos: distributions of the fushi tarazu, engrailed, Sex combs reduced, Antennapedia, and Ultrabithorax proteins. Genes Dev. 1988 Mar;2(3):350–360. doi: 10.1101/gad.2.3.350. [DOI] [PubMed] [Google Scholar]
- Carroll S. B., Laymon R. A., McCutcheon M. A., Riley P. D., Scott M. P. The localization and regulation of Antennapedia protein expression in Drosophila embryos. Cell. 1986 Oct 10;47(1):113–122. doi: 10.1016/0092-8674(86)90372-7. [DOI] [PubMed] [Google Scholar]
- Carroll S. B., Scott M. P. Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell. 1985 Nov;43(1):47–57. doi: 10.1016/0092-8674(85)90011-x. [DOI] [PubMed] [Google Scholar]
- Chadwick R., McGinnis W. Temporal and spatial distribution of transcripts from the Deformed gene of Drosophila. EMBO J. 1987 Mar;6(3):779–789. doi: 10.1002/j.1460-2075.1987.tb04820.x. [DOI] [PMC free article] [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]
- Duncan I. Control of bithorax complex functions by the segmentation gene fushi tarazu of D. melanogaster. Cell. 1986 Oct 24;47(2):297–309. doi: 10.1016/0092-8674(86)90452-6. [DOI] [PubMed] [Google Scholar]
- Frasch M., Hoey T., Rushlow C., Doyle H., Levine M. Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 1987 Mar;6(3):749–759. doi: 10.1002/j.1460-2075.1987.tb04817.x. [DOI] [PMC free article] [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]
- 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]
- Harding K., Levine M. Gap genes define the limits of antennapedia and bithorax gene expression during early development in Drosophila. EMBO J. 1988 Jan;7(1):205–214. doi: 10.1002/j.1460-2075.1988.tb02801.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harding K., Rushlow C., Doyle H. J., Hoey T., Levine M. Cross-regulatory interactions among pair-rule genes in Drosophila. Science. 1986 Aug 29;233(4767):953–959. doi: 10.1126/science.3755551. [DOI] [PubMed] [Google Scholar]
- Hoey T., Levine M. Divergent homeo box proteins recognize similar DNA sequences in Drosophila. Nature. 1988 Apr 28;332(6167):858–861. doi: 10.1038/332858a0. [DOI] [PubMed] [Google Scholar]
- Howard K., Ingham P. Regulatory interactions between the segmentation genes fushi tarazu, hairy, and engrailed in the Drosophila blastoderm. Cell. 1986 Mar 28;44(6):949–957. doi: 10.1016/0092-8674(86)90018-8. [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., Ish-Horowicz D., Howard K. R. Correlative changes in homoeotic and segmentation gene expression in Krüppel mutant embryos of Drosophila. EMBO J. 1986 Jul;5(7):1659–1665. doi: 10.1002/j.1460-2075.1986.tb04409.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ingham P. W., Martinez-Arias A. The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature. 1986 Dec 11;324(6097):592–597. doi: 10.1038/324592a0. [DOI] [PubMed] [Google Scholar]
- Irish V. F., Martinez-Arias A., Akam M. Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J. 1989 May;8(5):1527–1537. doi: 10.1002/j.1460-2075.1989.tb03537.x. [DOI] [PMC free article] [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]
- Ish-Horowicz D., Pinchin S. M., Ingham P. W., Gyurkovics H. G. Autocatalytic ftz activation and metameric instability induced by ectopic ftz expression. Cell. 1989 Apr 21;57(2):223–232. doi: 10.1016/0092-8674(89)90960-4. [DOI] [PubMed] [Google Scholar]
- Karr T. L., Kornberg T. B. fushi tarazu protein expression in the cellular blastoderm of Drosophila detected using a novel imaging technique. Development. 1989 May;106(1):95–103. doi: 10.1242/dev.106.1.95. [DOI] [PubMed] [Google Scholar]
- Krause H. M., Klemenz R., Gehring W. J. Expression, modification, and localization of the fushi tarazu protein in Drosophila embryos. Genes Dev. 1988 Aug;2(8):1021–1036. doi: 10.1101/gad.2.8.1021. [DOI] [PubMed] [Google Scholar]
- Kuziora M. A., McGinnis W. Autoregulation of a Drosophila homeotic selector gene. Cell. 1988 Nov 4;55(3):477–485. doi: 10.1016/0092-8674(88)90034-7. [DOI] [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]
- LeMotte P. K., Kuroiwa A., Fessler L. I., Gehring W. J. The homeotic gene Sex Combs Reduced of Drosophila: gene structure and embryonic expression. EMBO J. 1989 Jan;8(1):219–227. doi: 10.1002/j.1460-2075.1989.tb03367.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lehmann R., Nüsslein-Volhard C. hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo. Dev Biol. 1987 Feb;119(2):402–417. doi: 10.1016/0012-1606(87)90045-5. [DOI] [PubMed] [Google Scholar]
- Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
- Mahaffey J. W., Diederich R. J., Kaufman T. C. Novel patterns of homeotic protein accumulation in the head of the Drosophila embryo. Development. 1989 Jan;105(1):167–174. doi: 10.1242/dev.105.1.167. [DOI] [PubMed] [Google Scholar]
- Mahaffey J. W., Kaufman T. C. Distribution of the Sex combs reduced gene products in Drosophila melanogaster. Genetics. 1987 Sep;117(1):51–60. doi: 10.1093/genetics/117.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martinez-Arias A., Ingham P. W., Scott M. P., Akam M. E. The spatial and temporal deployment of Dfd and Scr transcripts throughout development of Drosophila. Development. 1987 Aug;100(4):673–683. doi: 10.1242/dev.100.4.673. [DOI] [PubMed] [Google Scholar]
- Merrill V. K., Turner F. R., Kaufman T. C. A genetic and developmental analysis of mutations in the Deformed locus in Drosophila melanogaster. Dev Biol. 1987 Aug;122(2):379–395. doi: 10.1016/0012-1606(87)90303-4. [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]
- 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]
- Regulski M., McGinnis N., Chadwick R., McGinnis W. Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development. EMBO J. 1987 Mar;6(3):767–777. doi: 10.1002/j.1460-2075.1987.tb04819.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reid T. A., Jones A. R., White I. G. Mechanism of inhibition of fructolysis in ram spermatozoa by chlorinated antifertility agents. Contraception. 1986 Sep;34(3):311–321. doi: 10.1016/0010-7824(86)90012-0. [DOI] [PubMed] [Google Scholar]
- Riley P. D., Carroll S. B., Scott M. P. The expression and regulation of Sex combs reduced protein in Drosophila embryos. Genes Dev. 1987 Sep;1(7):716–730. doi: 10.1101/gad.1.7.716. [DOI] [PubMed] [Google Scholar]
- Scott M. P., Carroll S. B. The segmentation and homeotic gene network in early Drosophila development. Cell. 1987 Dec 4;51(5):689–698. doi: 10.1016/0092-8674(87)90092-4. [DOI] [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. Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature. 1985 Dec 19;318(6047):677–680. doi: 10.1038/318677a0. [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]
- 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]
- 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]
- Winslow G. M., Carroll S. B., Scott M. P. Maternal-effect genes that alter the fate map of the Drosophila blastoderm embryo. Dev Biol. 1988 Sep;129(1):72–83. doi: 10.1016/0012-1606(88)90162-5. [DOI] [PubMed] [Google Scholar]