Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Jan 1;90(1):143–147. doi: 10.1073/pnas.90.1.143

The Antennapedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution.

F R Schubert 1, K Nieselt-Struwe 1, P Gruss 1
PMCID: PMC45616  PMID: 8093557

Abstract

The developmental control genes containing an Antennapedia-type homeobox are clustered in insects and vertebrates. The evolution of these genes was studied by the construction of evolutionary trees and by statistical geometry in sequence space. The comparative analysis of the homeobox sequences reveals the subdivision of the Antennapedia-type homeobox genes into three classes early in metazoan evolution. This observation suggests an important function of these genes even in the most primitive metazoans. Subsequent duplication events generated a cluster of at least five homeobox genes in the last common ancestor of insects and vertebrates. These genes later independently gave rise to the 13 groups of paralogous genes in vertebrates and to the 11 Antennapedia-type genes in the Drosophila complexes.

Full text

PDF
145

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Acampora D., D'Esposito M., Faiella A., Pannese M., Migliaccio E., Morelli F., Stornaiuolo A., Nigro V., Simeone A., Boncinelli E. The human HOX gene family. Nucleic Acids Res. 1989 Dec 25;17(24):10385–10402. doi: 10.1093/nar/17.24.10385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akam M. Hox and HOM: homologous gene clusters in insects and vertebrates. Cell. 1989 May 5;57(3):347–349. doi: 10.1016/0092-8674(89)90909-4. [DOI] [PubMed] [Google Scholar]
  3. Barad M., Jack T., Chadwick R., McGinnis W. A novel, tissue-specific, Drosophila homeobox gene. EMBO J. 1988 Jul;7(7):2151–2161. doi: 10.1002/j.1460-2075.1988.tb03054.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bürglin T. R., Ruvkun G., Coulson A., Hawkins N. C., McGhee J. D., Schaller D., Wittmann C., Müller F., Waterston R. H. Nematode homeobox cluster. Nature. 1991 Jun 27;351(6329):703–703. doi: 10.1038/351703a0. [DOI] [PubMed] [Google Scholar]
  5. Christen R., Ratto A., Baroin A., Perasso R., Grell K. G., Adoutte A. An analysis of the origin of metazoans, using comparisons of partial sequences of the 28S RNA, reveals an early emergence of triploblasts. EMBO J. 1991 Mar;10(3):499–503. doi: 10.1002/j.1460-2075.1991.tb07975.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Costa M., Weir M., Coulson A., Sulston J., Kenyon C. Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox. Cell. 1988 Dec 2;55(5):747–756. doi: 10.1016/0092-8674(88)90131-6. [DOI] [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. D'Esposito M., Morelli F., Acampora D., Migliaccio E., Simeone A., Boncinelli E. EVX2, a human homeobox gene homologous to the even-skipped segmentation gene, is localized at the 5' end of HOX4 locus on chromosome 2. Genomics. 1991 May;10(1):43–50. doi: 10.1016/0888-7543(91)90482-t. [DOI] [PubMed] [Google Scholar]
  9. Dolecki G. J., Wang G., Humphreys T. Stage- and tissue-specific expression of two homeo box genes in sea urchin embryos and adults. Nucleic Acids Res. 1988 Dec 23;16(24):11543–11558. doi: 10.1093/nar/16.24.11543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dollé P., Izpisúa-Belmonte J. C., Falkenstein H., Renucci A., Duboule D. Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature. 1989 Dec 14;342(6251):767–772. doi: 10.1038/342767a0. [DOI] [PubMed] [Google Scholar]
  11. Duboule D., Dollé P. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 1989 May;8(5):1497–1505. doi: 10.1002/j.1460-2075.1989.tb03534.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eigen M., Winkler-Oswatitsch R., Dress A. Statistical geometry in sequence space: a method of quantitative comparative sequence analysis. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5913–5917. doi: 10.1073/pnas.85.16.5913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell. 1989 May 5;57(3):367–378. doi: 10.1016/0092-8674(89)90912-4. [DOI] [PubMed] [Google Scholar]
  14. Hart C. P., Fainsod A., Ruddle F. H. Sequence analysis of the murine Hox-2.2, -2.3, and -2.4 homeo boxes: evolutionary and structural comparisons. Genomics. 1987 Oct;1(2):182–195. doi: 10.1016/0888-7543(87)90011-5. [DOI] [PubMed] [Google Scholar]
  15. Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
  16. Hoey T., Doyle H. J., Harding K., Wedeen C., Levine M. Homeo box gene expression in anterior and posterior regions of the Drosophila embryo. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4809–4813. doi: 10.1073/pnas.83.13.4809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Holland P. W., Hogan B. L. Expression of homeo box genes during mouse development: a review. Genes Dev. 1988 Jul;2(7):773–782. doi: 10.1101/gad.2.7.773. [DOI] [PubMed] [Google Scholar]
  18. Kamb A., Weir M., Rudy B., Varmus H., Kenyon C. Identification of genes from pattern formation, tyrosine kinase, and potassium channel families by DNA amplification. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4372–4376. doi: 10.1073/pnas.86.12.4372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kappen C., Schughart K., Ruddle F. H. Two steps in the evolution of Antennapedia-class vertebrate homeobox genes. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5459–5463. doi: 10.1073/pnas.86.14.5459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Karch F., Bender W., Weiffenbach B. abdA expression in Drosophila embryos. Genes Dev. 1990 Sep;4(9):1573–1587. doi: 10.1101/gad.4.9.1573. [DOI] [PubMed] [Google Scholar]
  21. Kessel M., Gruss P. Murine developmental control genes. Science. 1990 Jul 27;249(4967):374–379. doi: 10.1126/science.1974085. [DOI] [PubMed] [Google Scholar]
  22. Kuroiwa A., Kloter U., Baumgartner P., Gehring W. J. Cloning of the homeotic Sex combs reduced gene in Drosophila and in situ localization of its transcripts. EMBO J. 1985 Dec 30;4(13B):3757–3764. doi: 10.1002/j.1460-2075.1985.tb04145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Laughon A. DNA binding specificity of homeodomains. Biochemistry. 1991 Dec 3;30(48):11357–11367. doi: 10.1021/bi00112a001. [DOI] [PubMed] [Google Scholar]
  24. McAlpine P. J., Shows T. B. Nomenclature for human homeobox genes. Genomics. 1990 Jul;7(3):460–460. doi: 10.1016/0888-7543(90)90186-x. [DOI] [PubMed] [Google Scholar]
  25. McGinnis W., Garber R. L., Wirz J., Kuroiwa A., Gehring W. J. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell. 1984 Jun;37(2):403–408. doi: 10.1016/0092-8674(84)90370-2. [DOI] [PubMed] [Google Scholar]
  26. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell. 1992 Jan 24;68(2):283–302. doi: 10.1016/0092-8674(92)90471-n. [DOI] [PubMed] [Google Scholar]
  27. Murtha M. T., Leckman J. F., Ruddle F. H. Detection of homeobox genes in development and evolution. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10711–10715. doi: 10.1073/pnas.88.23.10711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Rushlow C., Doyle H., Hoey T., Levine M. Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev. 1987 Dec;1(10):1268–1279. doi: 10.1101/gad.1.10.1268. [DOI] [PubMed] [Google Scholar]
  30. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  31. Schaller D., Wittmann C., Spicher A., Müller F., Tobler H. Cloning and analysis of three new homeobox genes from the nematode Caenorhabditis elegans. Nucleic Acids Res. 1990 Apr 25;18(8):2033–2036. doi: 10.1093/nar/18.8.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schierwater B., Murtha M., Dick M., Ruddle F. H., Buss L. W. Homeoboxes in cnidarians. J Exp Zool. 1991 Dec;260(3):413–416. doi: 10.1002/jez.1402600316. [DOI] [PubMed] [Google Scholar]
  33. Schughart K., Kappen C., Ruddle F. H. Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7067–7071. doi: 10.1073/pnas.86.18.7067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schummer M., Scheurlen I., Schaller C., Galliot B. HOM/HOX homeobox genes are present in hydra (Chlorohydra viridissima) and are differentially expressed during regeneration. EMBO J. 1992 May;11(5):1815–1823. doi: 10.1002/j.1460-2075.1992.tb05233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Scott M. P., Tamkun J. W., Hartzell G. W., 3rd The structure and function of the homeodomain. Biochim Biophys Acta. 1989 Jul 28;989(1):25–48. doi: 10.1016/0304-419x(89)90033-4. [DOI] [PubMed] [Google Scholar]
  36. Scott M. P., Weiner A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4115–4119. doi: 10.1073/pnas.81.13.4115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Simeone A., Acampora D., Nigro V., Faiella A., D'Esposito M., Stornaiuolo A., Mavilio F., Boncinelli E. Differential regulation by retinoic acid of the homeobox genes of the four HOX loci in human embryonal carcinoma cells. Mech Dev. 1991 Mar;33(3):215–227. doi: 10.1016/0925-4773(91)90029-6. [DOI] [PubMed] [Google Scholar]
  38. Stornaiuolo A., Acampora D., Pannese M., D'Esposito M., Morelli F., Migliaccio E., Rambaldi M., Faiella A., Nigro V., Simeone A. Human HOX genes are differentially activated by retinoic acid in embryonal carcinoma cells according to their position within the four loci. Cell Differ Dev. 1990 Aug;31(2):119–127. doi: 10.1016/0922-3371(90)90015-o. [DOI] [PubMed] [Google Scholar]
  39. Stuart J. J., Brown S. J., Beeman R. W., Denell R. E. A deficiency of the homeotic complex of the beetle Tribolium. Nature. 1991 Mar 7;350(6313):72–74. doi: 10.1038/350072a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES