{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T18:28:38Z","timestamp":1791224918259,"version":"4.1.0"},"reference-count":53,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"5462","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Science"],"published-print":{"date-parts":[[2000,3,31]]},"abstract":"<jats:p>\n            The maternal determinant Bicoid (Bcd) represents the paradigm of a morphogen that provides positional information for pattern formation. However, as\n            <jats:italic>bicoid<\/jats:italic>\n            seems to be a recently acquired gene in flies, the question was raised as to how embryonic patterning is achieved in organisms with more ancestral modes of development. Because the phylogenetically conserved Hunchback (Hb) protein had previously been shown to act as a morphogen in abdominal patterning, we asked which functions of Bcd could be performed by Hb. By reestablishing a proposed ancient regulatory circuitry in which maternal Hb controls zygotic\n            <jats:italic>hunchback<\/jats:italic>\n            expression, we show that Hb is able to form thoracic segments in the absence of Bcd.\n          <\/jats:p>","DOI":"10.1126\/science.287.5462.2476","type":"journal-article","created":{"date-parts":[[2002,7,27]],"date-time":"2002-07-27T09:40:21Z","timestamp":1027762821000},"page":"2476-2479","source":"Crossref","is-referenced-by-count":80,"title":["<i>bicoid<\/i>\n            -Independent Formation of Thoracic Segments in\n            <i>Drosophila<\/i>"],"prefix":"10.1126","volume":"287","author":[{"given":"Ernst A.","family":"Wimmer","sequence":"first","affiliation":[{"name":"Lehrstuhl Genetik, Universita\u0308t Bayreuth, 95447 Bayreuth, Germany."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alan","family":"Carleton","sequence":"additional","affiliation":[{"name":"Department of Biology, New York University, 100 Washington Square East, New York, NY 10003, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Phoebe","family":"Harjes","sequence":"additional","affiliation":[{"name":"Department of Biology, New York University, 100 Washington Square East, New York, NY 10003, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Terry","family":"Turner","sequence":"additional","affiliation":[{"name":"Department of Biology, New York University, 100 Washington Square East, New York, NY 10003, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claude","family":"Desplan","sequence":"additional","affiliation":[{"name":"Department of Biology, New York University, 100 Washington Square East, New York, NY 10003, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"221","reference":[{"key":"e_1_3_1_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(92)90466-P"},{"key":"e_1_3_1_3_2","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0092-8674(88)90182-1","volume":"54","author":"Driever W.","year":"1988","unstructured":"Driever W., N\u00fcsslein-Volhard C., Cell 54, 83 (1988);","journal-title":"Cell"},{"key":"e_1_3_1_3_3","doi-asserted-by":"crossref","first-page":"1749","DOI":"10.1002\/j.1460-2075.1988.tb03004.x","volume":"7","author":"Berleth T.","year":"1988","unstructured":"Berleth T., et al., EMBO J. 7, 1749 (1988).","journal-title":"EMBO J."},{"key":"e_1_3_1_4_2","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/337138a0","volume":"337","author":"Driever W.","year":"1989","unstructured":"Driever W., N\u00fcsslein-Volhard C., Nature 337, 138 (1989);","journal-title":"Nature"},{"key":"e_1_3_1_4_3","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1038\/340363a0","volume":"340","author":"Driever W.","year":"1989","unstructured":"Driever W., Thoma G., N\u00fcsslein-Volhard C., Nature 340, 363 (1989);","journal-title":"Nature"},{"key":"e_1_3_1_4_4","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1016\/0092-8674(89)90062-7","volume":"57","author":"Struhl G.","year":"1989","unstructured":"Struhl G., Struhl K., Macdonald P. 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Biol."},{"key":"e_1_3_1_5_3","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1242\/dev.113.2.419","volume":"113","author":"Sommer R.","year":"1991","unstructured":"Sommer R., Tautz D., Development 113, 419 (1991);","journal-title":"Development"},{"key":"e_1_3_1_5_4","doi-asserted-by":"crossref","first-page":"3786","DOI":"10.1073\/pnas.96.7.3786","volume":"96","author":"Stauber M.","year":"1999","unstructured":"Stauber M., J\u00e4ckle H., Schmidt-Ott U., Proc. Natl. Acad. Sci. U.S.A. 96, 3786 (1999).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_1_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/0012-1606(87)90045-5"},{"key":"e_1_3_1_7_2","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1038\/346577a0","volume":"346","author":"H\u00fclskamp M.","year":"1990","unstructured":"H\u00fclskamp M., Pfeifle C., Tautz D., Nature 346, 577 (1990);","journal-title":"Nature"},{"key":"e_1_3_1_7_3","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/0092-8674(92)90405-2","volume":"69","author":"Struhl G.","year":"1992","unstructured":"Struhl G., Johnston P., Lawrence P. A., Cell 69, 237 (1992);","journal-title":"Cell"},{"key":"e_1_3_1_7_4","doi-asserted-by":"crossref","first-page":"3043","DOI":"10.1242\/dev.120.10.3043","volume":"120","author":"Schulz C.","year":"1994","unstructured":"Schulz C., Tautz D., Development 120, 3043 (1994).","journal-title":"Development"},{"key":"e_1_3_1_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/327383a0"},{"key":"e_1_3_1_8_3","doi-asserted-by":"crossref","first-page":"10782","DOI":"10.1073\/pnas.89.22.10782","volume":"89","author":"Sommer R. J.","year":"1992","unstructured":"Sommer R. J., Retzlaff M., Goerlich K., Sander K., Tautz D., Proc. Natl. Acad Sci. U.S.A. 89, 10782 (1992);","journal-title":"Proc. Natl. Acad Sci. U.S.A."},{"key":"e_1_3_1_8_4","doi-asserted-by":"crossref","first-page":"1899","DOI":"10.1242\/dev.121.6.1899","volume":"121","author":"Curtis D.","year":"1995","unstructured":"Curtis D., Apfeld J., Lehmann R., Development 121, 1899 (1995) .","journal-title":"Development"},{"key":"e_1_3_1_9_2","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/338629a0","volume":"338","author":"H\u00fclskamp M.","year":"1989","unstructured":"H\u00fclskamp M., Schroder C., Pfeifle C., J\u00e4ckle H., Tautz D., Nature 338, 629 (1989);","journal-title":"Nature"},{"key":"e_1_3_1_9_3","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1038\/338646a0","volume":"338","author":"Irish V.","year":"1989","unstructured":"Irish V., Lehmann R., Akam A. M., Nature 338, 646 (1989);","journal-title":"Nature"},{"key":"e_1_3_1_9_4","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1038\/338741a0","volume":"338","author":"Struhl G.","year":"1989","unstructured":"Struhl G., Nature 338, 741 (1989).","journal-title":"Nature"},{"key":"e_1_3_1_10_2","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1016\/S0092-8674(94)90622-X","volume":"78","author":"Simpson-Brose M.","year":"1994","unstructured":"Simpson-Brose M., Treisman J., Desplan C., Cell 78, 855 (1994);","journal-title":"Cell"},{"key":"e_1_3_1_10_3","unstructured":"; E. A. Wimmer and C. Desplan unpublished data."},{"key":"e_1_3_1_11_2","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1038\/332281a0","volume":"332","author":"Tautz D.","year":"1988","unstructured":"Tautz D., Nature 332, 281 (1988).","journal-title":"Nature"},{"key":"e_1_3_1_12_2","doi-asserted-by":"crossref","first-page":"2881","DOI":"10.1002\/j.1460-2075.1988.tb03145.x","volume":"7","author":"Schr\u00f6der C.","year":"1988","unstructured":"Schr\u00f6der C., Tautz D., Seifert E., J\u00e4ckle H., EMBO J. 7, 2881 (1988);","journal-title":"EMBO J."},{"key":"e_1_3_1_12_3","doi-asserted-by":"crossref","first-page":"3067","DOI":"10.1242\/dev.121.9.3067","volume":"121","author":"Margolis J. S.","year":"1995","unstructured":"Margolis J. S., et al., Development 121, 3067 (1995);","journal-title":"Development"},{"key":"e_1_3_1_12_4","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/0925-4773(94)90024-8","volume":"45","author":"Lukowitz W.","year":"1994","unstructured":"Lukowitz W., Schr\u00f6der C., Glaser G., H\u00fclskamp M., Tautz D., Mech. Dev. 45, 105 (1994).","journal-title":"Mech. Dev."},{"key":"e_1_3_1_13_2","unstructured":"Procedures for whole-mount in situ hybridization immunohistochemistry and cuticle preparations were as described (27). DNA probes for hb and lacZ were generated using the 2.4-kb insert from phbXba2.4 (11) and a 3.6-kb fragment from pCHAB\u0394Sal (27). Rabbit antibody to \u03b2-galactosidase (Cappel) was used at 1:5000 dilution. For Fig. 3 fully developed hb mutant embryos were selected under a Leica MZ12 stereomicroscope for green fluorescent protein (GFP) expression before cuticle preparations."},{"key":"e_1_3_1_14_2","unstructured":"The hb transgenes were constructed as follows: A 4-kb genomic Eco RI fragment containing the hb upstream sequences including the P1 promoter was isolated from phbXho10.5 (11) and cloned into the Eco RI site of pCHAB\u0394Xba (27) thereby creating pChbP1. The complete open reading frame for hb was excised by Not I and partial Eco RI digests from the cDNA clone J3 which was derived from a transcript originating at the P1 promoter (11). The cDNA fragment was inserted into pChbP1 that was opened by a complete Not I and partial Eco RI digest to fuse the genomic and cDNA at the Eco RI site within the 5\u2032 untranslated leader resulting in pChbP1only. To assess the expression pattern of the transgene we replaced the hb coding region (including its 3\u2032 untranslated region) by the lacZ gene. pChbP1only was opened by an Xba I digest and religated to generate pChbP1\u0394Xba into which a 3.6-kb Xba I fragment containing the AUG-\u03b2-gal (AB) gene derived from pCHAB\u0394Sal (27) was cloned to create pChbP1AB. A pUAST-HB construct was generated by cloning the 2.4-kb Xba I fragment containing the hb coding region from phbXba2.4 (11) into pUAST (28). These constructs were introduced into the fly genome as described (27) to generate several fly strains carrying the transgenes hbP1only hbP1AB and UAS-HB."},{"key":"e_1_3_1_15_2","unstructured":"Fly strains were generated as follows: The hbP1only transgenes were recombined or crossed into the amorphic hb FB mutant background. For the experiments described in Fig. 2 crosses were carried out to generate amorphic hb FB \/hb 14F trans-heterozygotes which were identified on the basis of anterior or posterior hb phenotype. For Fig. 3 the rescued hb mutant embryos derived from hb heterozygous mothers that carry three copies of the hbP1only transgene to increase the maternal Hb contribution. Assuming that each dose of the hbP1only transgenes is approximately equivalent to a normal dose of hb these mothers provide twice as much maternal Hb as the wild type. The maternally inherited hb mutant chromosome was marked with an UAS-GFP transgene whereas the paternally inherited double mutant chromosome carrying the amorphic alleles hb 7M and kni IID was marked with a wg-GAL4 transgene. Homozygous hb mutant embryos were identified by their expression of GFP in the wg pattern (12). All embryos with a fully rescued thorax also show disturbance of abdominal segments A3 and A4 which are most sensitive to partial loss of kni (15). For Fig. 4 the amorphic bcd E1 allele was used and third chromosomal UAS-HB and hbP1AB transgenes were recombined. The GAL4 driver lines were nos-GAL4GCN4-3\u2032bcd (29) and wg-GAL4."},{"key":"e_1_3_1_16_2","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1038\/359156a0","volume":"359","author":"Rothe M.","year":"1992","unstructured":"Rothe M., Pehl M., Taubert H., J\u00e4ckle H., Nature 359, 156 (1992);","journal-title":"Nature"},{"key":"e_1_3_1_16_3","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1242\/dev.124.7.1343","volume":"124","author":"Kosman D.","year":"1997","unstructured":"Kosman D., Small S., Development 124, 1343 (1997).","journal-title":"Development"},{"key":"e_1_3_1_17_2","doi-asserted-by":"publisher","DOI":"10.1093\/genetics\/138.1.125"},{"key":"e_1_3_1_18_2","doi-asserted-by":"crossref","unstructured":"K. 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J., Cell 48, 465 (1987).","journal-title":"Cell"},{"key":"e_1_3_1_21_2","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1038\/379694a0","volume":"379","author":"Dubnau J.","year":"1996","unstructured":"Dubnau J., Struhl G., Nature 379, 694 (1996);","journal-title":"Nature"},{"key":"e_1_3_1_21_3","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1038\/379746a0","volume":"379","author":"Rivera-Pomar R.","year":"1996","unstructured":"Rivera-Pomar R., Niessing D., Schmidt-Ott U., Gehring W., J\u00e4ckle H., Nature 379, 746 (1996);","journal-title":"Nature"},{"key":"e_1_3_1_21_4","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1038\/41692","volume":"388","author":"Chan S. K.","year":"1997","unstructured":"Chan S. K., Struhl G., Nature 388, 634 (1997);","journal-title":"Nature"},{"key":"e_1_3_1_21_5","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/S1097-2765(00)80434-7","volume":"5","author":"Niessing D.","year":"2000","unstructured":"Niessing D., et al., Mol. Cell 5, 395 (2000).","journal-title":"Mol. Cell"},{"key":"e_1_3_1_22_2","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1242\/dev.120.2.277","volume":"120","author":"Xu X.","year":"1994","unstructured":"Xu X., Xu P. X., Suzuki Y., Development 120, 277 (1994).","journal-title":"Development"},{"key":"e_1_3_1_23_2","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0092-8674(00)81339-2","volume":"82","author":"Draper B.","year":"1996","unstructured":"Draper B., Mello C., Bowerman B., Hardin J., Priess J., Cell 82, 205 (1996).","journal-title":"Cell"},{"key":"e_1_3_1_24_2","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1046\/j.1525-142x.1999.99020.x","volume":"1","author":"Isaacs H. V.","year":"1999","unstructured":"Isaacs H. V., Andreazzoli M., Slack J. M. W., Evol. Dev. 1, 143 (1999).","journal-title":"Evol. Dev."},{"key":"e_1_3_1_25_2","doi-asserted-by":"crossref","first-page":"4227","DOI":"10.1242\/dev.121.12.4227","volume":"121","author":"Wolff C.","year":"1995","unstructured":"Wolff C., Sommer R., Schr\u00f6der R., Glaser G., Tautz D., Development 121, 4227 (1995);","journal-title":"Development"},{"key":"e_1_3_1_25_3","unstructured":". N. H. Patel personal communication."},{"key":"e_1_3_1_26_2","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/0168-9525(96)10044-5","volume":"12","author":"Rivera-Pomar R.","year":"1996","unstructured":"Rivera-Pomar R., J\u00e4ckle H., Trends Genet. 12, 478 (1996);","journal-title":"Trends Genet."},{"key":"e_1_3_1_26_3","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/S0955-0674(96)80010-X","volume":"8","author":"Gray S.","year":"1996","unstructured":"Gray S., Levine M., Curr. Opin. Cell Biol. 8, 358 (1996).","journal-title":"Curr. Opin. Cell Biol."},{"key":"e_1_3_1_27_2","unstructured":"R. A. Raff The Shape of Life (Univ. of Chicago Press Chicago 1996);"},{"key":"e_1_3_1_27_3","doi-asserted-by":"publisher","DOI":"10.1126\/science.860134"},{"key":"e_1_3_1_28_2","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1242\/dev.124.8.1509","volume":"124","author":"Wimmer E. A.","year":"1997","unstructured":"Wimmer E. A., Cohen S. M., J\u00e4ckle H., Desplan C., Development 124, 1509 (1997).","journal-title":"Development"},{"key":"e_1_3_1_29_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.118.2.401"},{"key":"e_1_3_1_30_2","doi-asserted-by":"crossref","first-page":"1573","DOI":"10.1242\/dev.127.8.1573","volume":"127","author":"Janody F.","year":"2000","unstructured":"Janody F., Reischl J., Dostatni N., Development 127, 1573 (2000).","journal-title":"Development"},{"key":"e_1_3_1_31_2","unstructured":"We thank P. Beaufils for UAS-GFP strains; M. Boyle N. Dostatni U. Gaul F. Janody and J. Posakony for materials; and V. Schaeffer I. Brun J. Burr and the members of the Desplan DiNardo and Gaul labs for helpful discussions. E.A.W. was the recipient of a Human Frontier Science Program long-term fellowship. Supported by the Howard Hughes Medical Institute at Rockefeller University and by NSF grant IBN-9817981."}],"container-title":["Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/science.287.5462.2476","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,13]],"date-time":"2024-01-13T10:48:04Z","timestamp":1705142884000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/science.287.5462.2476"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2000,3,31]]},"references-count":53,"journal-issue":{"issue":"5462","published-print":{"date-parts":[[2000,3,31]]}},"alternative-id":["10.1126\/science.287.5462.2476"],"URL":"https:\/\/doi.org\/10.1126\/science.287.5462.2476","relation":{},"ISSN":["0036-8075","1095-9203"],"issn-type":[{"value":"0036-8075","type":"print"},{"value":"1095-9203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2000,3,31]]}}}