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. 1983;2(11):2027–2036. doi: 10.1002/j.1460-2075.1983.tb01696.x

Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila.

R L Garber, A Kuroiwa, W J Gehring
PMCID: PMC555405  PMID: 6416827

Abstract

Homeotic genes are involved in the control of developmental pathways: dominant mutations at the Antennapedia locus of Drosophila, for example, lead to replacement of the antennae on the head of the fly by mesothoracic legs. Using a combination of chromosome walking and jumping, we have cloned a DNA region from Drosophila containing Antennapedia. Five DNA inversion rearrangements which are associated with the Antennapedia mutant phenotype were localized within a 25-kb region. Genomic DNA sequences from this area were used as hybridization probes to screen cDNA libraries prepared from Drosophila embryonic and pupal poly(A)+ RNA. A 2.2-kb cDNA sequence (903) was isolated which appears to derive from at least four non-contiguous chromosomal regions that span 100 kb. It includes the positions of the inversion breakpoints. A second cDNA of 2.9 kb (909) is composed of sequences from at least three chromosomal regions, two of which are similar or identical to sequences contained in the 903 clone but the third is derived from genomic DNA within a putative 903 intron. The unusual size and complexity of this locus are discussed.

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Selected References

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  1. Bender W., Akam M., Karch F., Beachy P. A., Peifer M., Spierer P., Lewis E. B., Hogness D. S. Molecular Genetics of the Bithorax Complex in Drosophila melanogaster. Science. 1983 Jul 1;221(4605):23–29. doi: 10.1126/science.221.4605.23. [DOI] [PubMed] [Google Scholar]
  2. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  3. Beyer A. L., Bouton A. H., Miller O. L., Jr Correlation of hnRNP structure and nascent transcript cleavage. Cell. 1981 Oct;26(2 Pt 2):155–165. doi: 10.1016/0092-8674(81)90299-3. [DOI] [PubMed] [Google Scholar]
  4. Bingham P. M., Levis R., Rubin G. M. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell. 1981 Sep;25(3):693–704. doi: 10.1016/0092-8674(81)90176-8. [DOI] [PubMed] [Google Scholar]
  5. Blattner F. R., Williams B. G., Blechl A. E., Denniston-Thompson K., Faber H. E., Furlong L., Grunwald D. J., Kiefer D. O., Moore D. D., Schumm J. W. Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. Science. 1977 Apr 8;196(4286):161–169. doi: 10.1126/science.847462. [DOI] [PubMed] [Google Scholar]
  6. Denell R. E. Homoeosis in Drosophila. I. Complementation studies with revertants of Nasobemia. Genetics. 1973 Oct;75(2):279–297. doi: 10.1093/genetics/75.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Denell R. E. The nature of reversion of a dominant gene of Drosophila melanogaster. Mutat Res. 1972 Jun;15(2):221–223. doi: 10.1016/0027-5107(72)90036-x. [DOI] [PubMed] [Google Scholar]
  8. Dudler R., Egg A. H., Kubli E., Artavanis-Tsakonas S., Gehring W. J., Steward R., Schedl P. Transfer RNA genes of Drosophila melanogaster. Nucleic Acids Res. 1980 Jul 11;8(13):2921–2937. doi: 10.1093/nar/8.13.2921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Duncan I. W., Kaufman T. C. Cytogenic analysis of chromosome 3 in Drosophila melanogaster: mapping of the proximal portion of the right arm. Genetics. 1975 Aug;80(4):733–752. doi: 10.1093/genetics/80.4.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gehring W. J. Establishment of a Drosophila gene bank in a bacterial plasmids: Elizabeth Goldschmidt Memorial Lecture. Isr J Med Sci. 1978 Feb;14(2):295–304. [PubMed] [Google Scholar]
  11. Gehring W. Bildung eines vollständigen Mittelbeines mit Sternopleura in der Antennenregion bei der Mutante Nasobemia (Ns) von Drosophila melanogaster. Arch Julius Klaus Stift Vererbungsforsch Sozialanthropol Rassenhyg. 1967;41(2-4):44–54. [PubMed] [Google Scholar]
  12. Hanahan D., Meselson M. Plasmid screening at high colony density. Gene. 1980 Jun;10(1):63–67. doi: 10.1016/0378-1119(80)90144-4. [DOI] [PubMed] [Google Scholar]
  13. Hannah-Alava A. Developmental Genetics of the Posterior Legs in Drosophila Melanogaster. Genetics. 1958 Sep;43(5):878–905. doi: 10.1093/genetics/43.5.878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ising G., Block K. Derivation-dependent distribution of insertion sites for a Drosophila transposon. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):527–544. doi: 10.1101/sqb.1981.045.01.069. [DOI] [PubMed] [Google Scholar]
  16. Kalfayan L., Wensink P. C. alpha-Tubulin genes of Drosophila. Cell. 1981 Apr;24(1):97–106. doi: 10.1016/0092-8674(81)90505-5. [DOI] [PubMed] [Google Scholar]
  17. Karn J., Brenner S., Barnett L., Cesareni G. Novel bacteriophage lambda cloning vector. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5172–5176. doi: 10.1073/pnas.77.9.5172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaufman T. C., Lewis R., Wakimoto B. Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B. Genetics. 1980 Jan;94(1):115–133. doi: 10.1093/genetics/94.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Laird C. D., Chooi W. Y. Morphology of transcription units in Drosophila melanogaster. Chromosoma. 1976 Oct 28;58(2):193–218. doi: 10.1007/BF00701359. [DOI] [PubMed] [Google Scholar]
  20. Langer-Safer P. R., Levine M., Ward D. C. Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4381–4385. doi: 10.1073/pnas.79.14.4381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Levine M., Hafen E., Garber R. L., Gehring W. J. Spatial distribution of Antennapedia transcripts during Drosophila development. EMBO J. 1983;2(11):2037–2046. doi: 10.1002/j.1460-2075.1983.tb01697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Lewis R. A., Kaufman T. C., Denell R. E., Tallerico P. Genetic Analysis of the Antennapedia Gene Complex (Ant-C) and Adjacent Chromosomal Regions of DROSOPHILA MELANOGASTER. I. Polytene Chromosome Segments 84b-D. Genetics. 1980 Jun;95(2):367–381. doi: 10.1093/genetics/95.2.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  25. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Meyerowitz E. M., Hogness D. S. Molecular organization of a Drosophila puff site that responds to ecdysone. Cell. 1982 Jan;28(1):165–176. doi: 10.1016/0092-8674(82)90386-5. [DOI] [PubMed] [Google Scholar]
  27. Mischke D., Pardue M. L. Organization and expression of alpha-tubulin genes in Drosophila melanogaster. One member of the alpha-tubulin multigene family is transcribed in both oogenesis and later embryonic development. J Mol Biol. 1982 Apr 15;156(3):449–466. doi: 10.1016/0022-2836(82)90260-1. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Ouweneel W. J. Developmental genetics of homoeosis. Adv Genet. 1976;18:179–248. doi: 10.1016/s0065-2660(08)60439-3. [DOI] [PubMed] [Google Scholar]
  30. Pardue M. L., Gall J. G. Nucleic acid hybridization to the DNA of cytological preparations. Methods Cell Biol. 1975;10:1–16. doi: 10.1016/s0091-679x(08)60727-x. [DOI] [PubMed] [Google Scholar]
  31. Rubin G. M., Finnegan D. J., Hogness D. S. The chromosomal arrangement of coding sequences in a family of repeated genes. Prog Nucleic Acid Res Mol Biol. 1976;19:221–226. doi: 10.1016/s0079-6603(08)60920-4. [DOI] [PubMed] [Google Scholar]
  32. Scalenghe F., Turco E., Edström J. E., Pirrotta V., Melli M. Microdissection and cloning of DNA from a specific region of Drosophila melanogaster polytene chromosomes. Chromosoma. 1981;82(2):205–216. doi: 10.1007/BF00286105. [DOI] [PubMed] [Google Scholar]
  33. Scherer G., Telford J., Baldari C., Pirrotta V. Isolation of cloned genes differentially expressed at early and late stages of Drosophila embryonic development. Dev Biol. 1981 Sep;86(2):438–447. doi: 10.1016/0012-1606(81)90202-5. [DOI] [PubMed] [Google Scholar]
  34. Smith G. E., Summers M. D. The bidirectional transfer of DNA and RNA to nitrocellulose or diazobenzyloxymethyl-paper. Anal Biochem. 1980 Nov 15;109(1):123–129. doi: 10.1016/0003-2697(80)90019-6. [DOI] [PubMed] [Google Scholar]
  35. Struhl G. A homoeotic mutation transforming leg to antenna in Drosophila. Nature. 1981 Aug 13;292(5824):635–638. doi: 10.1038/292635a0. [DOI] [PubMed] [Google Scholar]
  36. Sánchez F., Natzle J. E., Cleveland D. W., Kirschner M. W., McCarthy B. J. A dispersed multigene family encoding tubulin in Drosophila melanogaster. Cell. 1980 Dec;22(3):845–854. doi: 10.1016/0092-8674(80)90561-9. [DOI] [PubMed] [Google Scholar]
  37. Vande Woude G. F., Oskarsson M., Enquist L. W., Nomura S., Sullivan M., Fischinger P. J. Cloning of integrated Moloney sarcoma proviral DNA sequences in bacteriophage lambda. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4464–4468. doi: 10.1073/pnas.76.9.4464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wakimoto B. T., Kaufman T. C. Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster. Dev Biol. 1981 Jan 15;81(1):51–64. doi: 10.1016/0012-1606(81)90347-x. [DOI] [PubMed] [Google Scholar]
  39. Wienand U., Schwarz Z., Feix G. Electrophoretic elution of nucleic acids from gels adapted for subsequent biological tests. Application for analysis of mRNAs from maize endosperm. FEBS Lett. 1979 Feb 15;98(2):319–323. doi: 10.1016/0014-5793(79)80208-2. [DOI] [PubMed] [Google Scholar]
  40. Will B. M., Bayev A. A., Finnegan D. J. Nucleotide sequence of terminal repeats of 412 transposable elements of Drosophila melanogaster. A similarity to proviral long terminal repeats and its implications for the mechanism of transposition. J Mol Biol. 1981 Dec 25;153(4):897–915. doi: 10.1016/0022-2836(81)90458-7. [DOI] [PubMed] [Google Scholar]
  41. Yang R., Lis J., Wu R. Elution of DNA from agarose gels after electrophoresis. Methods Enzymol. 1979;68:176–182. doi: 10.1016/0076-6879(79)68012-6. [DOI] [PubMed] [Google Scholar]
  42. Young M. W. Middle repetitive DNA: a fluid component of the Drosophila genome. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6274–6278. doi: 10.1073/pnas.76.12.6274. [DOI] [PMC free article] [PubMed] [Google Scholar]

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