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. 1992 Oct;132(2):453–469. doi: 10.1093/genetics/132.2.453

Comparative Studies of Drosophila Antennapedia Genes

J E Hooper 1, M Perez-Alonso 1, J R Bermingham 1, M Prout 1, B A Rocklein 1, M Wagenbach 1, J E Edstrom 1, R D Frutos 1, M P Scott 1
PMCID: PMC1205149  PMID: 1358753

Abstract

The Antennapedia (Antp) homeotic gene of Drosophila melanogaster controls cell fates and pattern formation in the epidermis, nervous system and mesoderm of thoracic segments. Its expression is controlled at the levels of transcription, alternative RNA splicing, polyadenylation and translation. Two nested Antp transcription units extend over 103 kb and produce sixteen different transcripts. We have compared the Antp genes of Drosophila virilis, Drosophila subobscura and D. melanogaster to determine which structural features are conserved and therefore may be important to the gene's function. The overall gene structures are similar. There are many conserved sequence blocks throughout the large introns, at least 15 kb upstream of the first promoter, and at least 3 kb downstream of the last polyadenylation site. Intron and exon sequence conservation around alternative splice sites indicates that alternative protein coding forms may also be conserved. Protein coding potential is perfectly conserved around the C-terminal homeodomain, well conserved in the N-terminal region, and more variable in the middle. The large size of the Antp gene may reflect a large number of control elements necessary for appropriate Antp protein expression. The conservation of transcript complexity suggests functional requirements for the different protein forms.

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Selected References

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  1. Ayme A., Southgate R., Tissières A. Nucleotide sequences responsible for the thermal inducibility of the Drosophila small heat-shock protein genes in monkey COS cells. J Mol Biol. 1985 Apr 20;182(4):469–475. doi: 10.1016/0022-2836(85)90233-5. [DOI] [PubMed] [Google Scholar]
  2. Beachy P. A., Krasnow M. A., Gavis E. R., Hogness D. S. An Ultrabithorax protein binds sequences near its own and the Antennapedia P1 promoters. Cell. 1988 Dec 23;55(6):1069–1081. doi: 10.1016/0092-8674(88)90251-6. [DOI] [PubMed] [Google Scholar]
  3. Bermingham J. R., Jr, Martinez-Arias A., Petitt M. G., Scott M. P. Different patterns of transcription from the two Antennapedia promoters during Drosophila embryogenesis. Development. 1990 Jul;109(3):553–566. doi: 10.1242/dev.109.3.553. [DOI] [PubMed] [Google Scholar]
  4. Bermingham J. R., Jr, Scott M. P. Developmentally regulated alternative splicing of transcripts from the Drosophila homeotic gene Antennapedia can produce four different proteins. EMBO J. 1988 Oct;7(10):3211–3222. doi: 10.1002/j.1460-2075.1988.tb03188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
  6. Celniker S. E., Sharma S., Keelan D. J., Lewis E. B. The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J. 1990 Dec;9(13):4277–4286. doi: 10.1002/j.1460-2075.1990.tb07876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cribbs D. L., Pultz M. A., Johnson D., Mazzulla M., Kaufman T. C. Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia. EMBO J. 1992 Apr;11(4):1437–1449. doi: 10.1002/j.1460-2075.1992.tb05188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fortini M. E., Rubin G. M. Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev. 1990 Mar;4(3):444–463. doi: 10.1101/gad.4.3.444. [DOI] [PubMed] [Google Scholar]
  9. Garber R. L., Kuroiwa A., Gehring W. J. Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 1983;2(11):2027–2036. doi: 10.1002/j.1460-2075.1983.tb01696.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gibson G., Schier A., LeMotte P., Gehring W. J. The specificities of Sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain. Cell. 1990 Sep 21;62(6):1087–1103. doi: 10.1016/0092-8674(90)90386-s. [DOI] [PubMed] [Google Scholar]
  11. Hafen E., Levine M., Gehring W. J. Regulation of Antennapedia transcript distribution by the bithorax complex in Drosophila. Nature. 1984 Jan 19;307(5948):287–289. doi: 10.1038/307287a0. [DOI] [PubMed] [Google Scholar]
  12. Harding K., Wedeen C., McGinnis W., Levine M. Spatially regulated expression of homeotic genes in Drosophila. Science. 1985 Sep 20;229(4719):1236–1242. doi: 10.1126/science.3898362. [DOI] [PubMed] [Google Scholar]
  13. Hayashida H., Miyata T. Unusual evolutionary conservation and frequent DNA segment exchange in class I genes of the major histocompatibility complex. Proc Natl Acad Sci U S A. 1983 May;80(9):2671–2675. doi: 10.1073/pnas.80.9.2671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heberlein U., Rubin G. M. Structural and functional comparisons of the Drosophila virilis and Drosophila melanogaster rough genes. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5916–5920. doi: 10.1073/pnas.87.15.5916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Henikoff S., Eghtedarzadeh M. K. Conserved arrangement of nested genes at the Drosophila Gart locus. Genetics. 1987 Dec;117(4):711–725. doi: 10.1093/genetics/117.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  17. Holmgren R., Corces V., Morimoto R., Blackman R., Meselson M. Sequence homologies in the 5' regions of four Drosophila heat-shock genes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3775–3778. doi: 10.1073/pnas.78.6.3775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Irvine K. D., Helfand S. L., Hogness D. S. The large upstream control region of the Drosophila homeotic gene Ultrabithorax. Development. 1991 Feb;111(2):407–424. doi: 10.1242/dev.111.2.407. [DOI] [PubMed] [Google Scholar]
  22. Johnson W. A., McCormick C. A., Bray S. J., Hirsh J. A neuron-specific enhancer of the Drosophila dopa decarboxylase gene. Genes Dev. 1989 May;3(5):676–686. doi: 10.1101/gad.3.5.676. [DOI] [PubMed] [Google Scholar]
  23. Jorgensen E. M., Garber R. L. Function and misfunction of the two promoters of the Drosophila Antennapedia gene. Genes Dev. 1987 Aug;1(6):544–555. doi: 10.1101/gad.1.6.544. [DOI] [PubMed] [Google Scholar]
  24. Karch F., Weiffenbach B., Peifer M., Bender W., Duncan I., Celniker S., Crosby M., Lewis E. B. The abdominal region of the bithorax complex. Cell. 1985 Nov;43(1):81–96. doi: 10.1016/0092-8674(85)90014-5. [DOI] [PubMed] [Google Scholar]
  25. Kassis J. A., Desplan C., Wright D. K., O'Farrell P. H. Evolutionary conservation of homeodomain-binding sites and other sequences upstream and within the major transcription unit of the Drosophila segmentation gene engrailed. Mol Cell Biol. 1989 Oct;9(10):4304–4311. doi: 10.1128/mcb.9.10.4304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kassis J. A., Poole S. J., Wright D. K., O'Farrell P. H. Sequence conservation in the protein coding and intron regions of the engrailed transcription unit. EMBO J. 1986 Dec 20;5(13):3583–3589. doi: 10.1002/j.1460-2075.1986.tb04686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kassis J. A., Wong M. L., O'Farrell P. H. Electron microscopic heteroduplex mapping identifies regions of the engrailed locus that are conserved between Drosophila melanogaster and Drosophila virilis. Mol Cell Biol. 1985 Dec;5(12):3600–3609. doi: 10.1128/mcb.5.12.3600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Kaufman T. C., Seeger M. A., Olsen G. Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv Genet. 1990;27:309–362. doi: 10.1016/s0065-2660(08)60029-2. [DOI] [PubMed] [Google Scholar]
  30. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Konsolaki M., Komitopoulou K., Tolias P. P., King D. L., Swimmer C., Kafatos F. C. The chorion genes of the medfly, Ceratitis capitata, I: Structural and regulatory conservation of the s36 gene relative to two Drosophila species. Nucleic Acids Res. 1990 Apr 11;18(7):1731–1737. doi: 10.1093/nar/18.7.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Krasnow M. A., Saffman E. E., Kornfeld K., Hogness D. S. Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell. 1989 Jun 16;57(6):1031–1043. doi: 10.1016/0092-8674(89)90341-3. [DOI] [PubMed] [Google Scholar]
  33. Laughon A., Boulet A. M., Bermingham J. R., Jr, Laymon R. A., Scott M. P. Structure of transcripts from the homeotic Antennapedia gene of Drosophila melanogaster: two promoters control the major protein-coding region. Mol Cell Biol. 1986 Dec;6(12):4676–4689. doi: 10.1128/mcb.6.12.4676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. Maier D., Preiss A., Powell J. R. Regulation of the segmentation gene fushi tarazu has been functionally conserved in Drosophila. EMBO J. 1990 Dec;9(12):3957–3966. doi: 10.1002/j.1460-2075.1990.tb07616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Malicki J., Schughart K., McGinnis W. Mouse Hox-2.2 specifies thoracic segmental identity in Drosophila embryos and larvae. Cell. 1990 Nov 30;63(5):961–967. doi: 10.1016/0092-8674(90)90499-5. [DOI] [PubMed] [Google Scholar]
  38. Martinez-Arias Alfonso. The Antennapedia gene is required and expressed in parasegments 4 and 5 of the Drosophila embryo. EMBO J. 1986 Jan;5(1):135–141. doi: 10.1002/j.1460-2075.1986.tb04187.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Martínez-Cruzado J. C. Evolution of the autosomal chorion cluster in Drosophila. IV. The Hawaiian Drosophila: rapid protein evolution and constancy in the rate of DNA divergence. J Mol Evol. 1990 Nov;31(5):402–423. doi: 10.1007/BF02106055. [DOI] [PubMed] [Google Scholar]
  40. Martínez-Cruzado J. C., Swimmer C., Fenerjian M. G., Kafatos F. C. Evolution of the autosomal chorion locus in Drosophila. I. General organization of the locus and sequence comparisons of genes s15 and s19 in evolutionary distant species. Genetics. 1988 Jul;119(3):663–677. doi: 10.1093/genetics/119.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Michael W. M., Bowtell D. D., Rubin G. M. Comparison of the sevenless genes of Drosophila virilis and Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5351–5353. doi: 10.1073/pnas.87.14.5351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Mitsialis S. A., Kafatos F. C. Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature. 1985 Oct 3;317(6036):453–456. doi: 10.1038/317453a0. [DOI] [PubMed] [Google Scholar]
  43. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  44. O'Neil M. T., Belote J. M. Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics. 1992 May;131(1):113–128. doi: 10.1093/genetics/131.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Perkins K. K., Dailey G. M., Tjian R. In vitro analysis of the Antennapedia P2 promoter: identification of a new Drosophila transcription factor. Genes Dev. 1988 Dec;2(12A):1615–1626. doi: 10.1101/gad.2.12a.1615. [DOI] [PubMed] [Google Scholar]
  46. Regulski M., Harding K., Kostriken R., Karch F., Levine M., McGinnis W. Homeo box genes of the Antennapedia and bithorax complexes of Drosophila. Cell. 1985 Nov;43(1):71–80. doi: 10.1016/0092-8674(85)90013-3. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. Schneuwly S., Kuroiwa A., Baumgartner P., Gehring W. J. Structural organization and sequence of the homeotic gene Antennapedia of Drosophila melanogaster. EMBO J. 1986 Apr;5(4):733–739. doi: 10.1002/j.1460-2075.1986.tb04275.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Scott M. P., Weiner A. J., Hazelrigg T. I., Polisky B. A., Pirrotta V., Scalenghe F., Kaufman T. C. The molecular organization of the Antennapedia locus of Drosophila. Cell. 1983 Dec;35(3 Pt 2):763–776. doi: 10.1016/0092-8674(83)90109-5. [DOI] [PubMed] [Google Scholar]
  51. Seeger M. A., Kaufman T. C. Molecular analysis of the bicoid gene from Drosophila pseudoobscura: identification of conserved domains within coding and noncoding regions of the bicoid mRNA. EMBO J. 1990 Sep;9(9):2977–2987. doi: 10.1002/j.1460-2075.1990.tb07490.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Stroeher V. L., Jorgensen E. M., Garber R. L. Multiple transcripts from the Antennapedia gene of Drosophila melanogaster. Mol Cell Biol. 1986 Dec;6(12):4667–4675. doi: 10.1128/mcb.6.12.4667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Struhl G., Akam M. Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 1985 Dec 1;4(12):3259–3264. doi: 10.1002/j.1460-2075.1985.tb04075.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Struhl G. Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila. J Embryol Exp Morphol. 1983 Aug;76:297–331. [PubMed] [Google Scholar]
  55. Sánchez-Herrero E., Vernós I., Marco R., Morata G. Genetic organization of Drosophila bithorax complex. Nature. 1985 Jan 10;313(5998):108–113. doi: 10.1038/313108a0. [DOI] [PubMed] [Google Scholar]
  56. Taghert P. H., Schneider L. E. Interspecific comparison of a Drosophila gene encoding FMRFamide-related neuropeptides. J Neurosci. 1990 Jun;10(6):1929–1942. doi: 10.1523/JNEUROSCI.10-06-01929.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  58. Treier M., Pfeifle C., Tautz D. Comparison of the gap segmentation gene hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO J. 1989 May;8(5):1517–1525. doi: 10.1002/j.1460-2075.1989.tb03536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Tremml G., Bienz M. An essential role of even-skipped for homeotic gene expression in the Drosophila visceral mesoderm. EMBO J. 1989 Sep;8(9):2687–2693. doi: 10.1002/j.1460-2075.1989.tb08409.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Wedeen C., Harding K., Levine M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell. 1986 Mar 14;44(5):739–748. doi: 10.1016/0092-8674(86)90840-8. [DOI] [PubMed] [Google Scholar]
  61. Wharton K. A., Yedvobnick B., Finnerty V. G., Artavanis-Tsakonas S. opa: a novel family of transcribed repeats shared by the Notch locus and other developmentally regulated loci in D. melanogaster. Cell. 1985 Jan;40(1):55–62. doi: 10.1016/0092-8674(85)90308-3. [DOI] [PubMed] [Google Scholar]
  62. Zink B., Engström Y., Gehring W. J., Paro R. Direct interaction of the Polycomb protein with Antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J. 1991 Jan;10(1):153–162. doi: 10.1002/j.1460-2075.1991.tb07931.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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