Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1996 Aug 1;15(15):3934–3942.

Functional similarity in appendage specification by the Ultrabithorax and abdominal-A Drosophila HOX genes.

F Casares 1, M Calleja 1, E Sánchez-Herrero 1
PMCID: PMC452108  PMID: 8670898

Abstract

In Drosophila, the Ultrabithorax, abdominal-A and Abdominal-B HOX genes of the bithorax complex determine the identity of part of the thorax and the whole abdomen. Either the absence of these genes or their ectopic expression transform segments into the identity of different ones along the antero-posterior axis. Here we show that misexpression of Ultrabithorax, abdominal-A and, to some extent, Abdominal-B genes cause similar transformations in some of the fruitfly appendages: antennal tissue into leg tissue and wing tissue into haltere tissue. abdominal-A can fully, and Abdominal-B partially, substitute for Ultrabithorax in haltere development. By contrast, when ectopically expressed, the three genes specify different segments in regions of the main body axis like notum or abdomen. Insects may have originally used the HOX genes primarily to specify this main body axis. By contrast, the homeotic requirement to form appendages is, in some cases, non-specific.

Full text

PDF
3934

Images in this article

3935Image
on p.3935
3936Image
on p.3936
3937Image
on p.3937
3938Image
on p.3938
3939Image
on p.3939
3940Image
on p.3940

Selected References

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

  1. Beachy P. A., Helfand S. L., Hogness D. S. Segmental distribution of bithorax complex proteins during Drosophila development. Nature. 1985 Feb 14;313(6003):545–551. doi: 10.1038/313545a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Brand A. H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993 Jun;118(2):401–415. doi: 10.1242/dev.118.2.401. [DOI] [PubMed] [Google Scholar]
  4. Busturia A., Casanova J., Sánchez-Herrero E., González R., Morata G. Genetic structure of the abd-A gene of Drosophila. Development. 1989 Nov;107(3):575–583. doi: 10.1242/dev.107.3.575. [DOI] [PubMed] [Google Scholar]
  5. Capdevila J., Guerrero I. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 1994 Oct 3;13(19):4459–4468. doi: 10.1002/j.1460-2075.1994.tb06768.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carroll S. B. Homeotic genes and the evolution of arthropods and chordates. Nature. 1995 Aug 10;376(6540):479–485. doi: 10.1038/376479a0. [DOI] [PubMed] [Google Scholar]
  7. Carroll S. B., Weatherbee S. D., Langeland J. A. Homeotic genes and the regulation and evolution of insect wing number. Nature. 1995 May 4;375(6526):58–61. doi: 10.1038/375058a0. [DOI] [PubMed] [Google Scholar]
  8. Castelli-Gair J., Akam M. How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metameres. Development. 1995 Sep;121(9):2973–2982. doi: 10.1242/dev.121.9.2973. [DOI] [PubMed] [Google Scholar]
  9. Castelli-Gair J., Greig S., Micklem G., Akam M. Dissecting the temporal requirements for homeotic gene function. Development. 1994 Jul;120(7):1983–1995. doi: 10.1242/dev.120.7.1983. [DOI] [PubMed] [Google Scholar]
  10. Celniker S. E., Keelan D. J., Lewis E. B. The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev. 1989 Sep;3(9):1424–1436. doi: 10.1101/gad.3.9.1424. [DOI] [PubMed] [Google Scholar]
  11. Celniker S. E., Lewis E. B. Molecular basis of transabdominal--a sexually dimorphic mutant of the bithorax complex of Drosophila. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1566–1570. doi: 10.1073/pnas.90.4.1566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Celniker S. E., Lewis E. B. Transabdominal, a dominant mutant of the Bithorax Complex, produces a sexually dimorphic segmental transformation in Drosophila. Genes Dev. 1987 Apr;1(2):111–123. doi: 10.1101/gad.1.2.111. [DOI] [PubMed] [Google Scholar]
  13. Frischer L. E., Hagen F. S., Garber R. L. An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs. Cell. 1986 Dec 26;47(6):1017–1023. doi: 10.1016/0092-8674(86)90816-0. [DOI] [PubMed] [Google Scholar]
  14. Gardner E. J. Tumorous head in Drosophila. Adv Genet. 1970;15:115–146. [PubMed] [Google Scholar]
  15. 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]
  16. González-Crespo S., Morata G. Control of Drosophila adult pattern by extradenticle. Development. 1995 Jul;121(7):2117–2125. doi: 10.1242/dev.121.7.2117. [DOI] [PubMed] [Google Scholar]
  17. González-Reyes A., Morata G. The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products. Cell. 1990 May 4;61(3):515–522. doi: 10.1016/0092-8674(90)90533-k. [DOI] [PubMed] [Google Scholar]
  18. Greig S., Akam M. The role of homeotic genes in the specification of the Drosophila gonad. Curr Biol. 1995 Sep 1;5(9):1057–1062. doi: 10.1016/s0960-9822(95)00210-7. [DOI] [PubMed] [Google Scholar]
  19. Guillén I., Mullor J. L., Capdevila J., Sánchez-Herrero E., Morata G., Guerrero I. The function of engrailed and the specification of Drosophila wing pattern. Development. 1995 Oct;121(10):3447–3456. doi: 10.1242/dev.121.10.3447. [DOI] [PubMed] [Google Scholar]
  20. Halder G., Callaerts P., Gehring W. J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science. 1995 Mar 24;267(5205):1788–1792. doi: 10.1126/science.7892602. [DOI] [PubMed] [Google Scholar]
  21. Irvine K. D., Botas J., Jha S., Mann R. S., Hogness D. S. Negative autoregulation by Ultrabithorax controls the level and pattern of its expression. Development. 1993 Jan;117(1):387–399. doi: 10.1242/dev.117.1.387. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  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. 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]
  26. Kerridge S., Morata G. Developmental effects of some newly induced Ultrabithorax alleles of Drosophila. J Embryol Exp Morphol. 1982 Apr;68:211–234. [PubMed] [Google Scholar]
  27. Kiger J. A., Jr Cell determination in Drosophila with paradoxical genotypes. Dev Biol. 1976 May;50(1):187–200. doi: 10.1016/0012-1606(76)90077-4. [DOI] [PubMed] [Google Scholar]
  28. Kornfeld K., Saint R. B., Beachy P. A., Harte P. J., Peattie D. A., Hogness D. S. Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev. 1989 Feb;3(2):243–258. doi: 10.1101/gad.3.2.243. [DOI] [PubMed] [Google Scholar]
  29. Kuhn D. T., Mack J. A., Duan C., Packert G. Tumorous-head (tuh-1; tuh-3) modulates Abd-B bithorax-complex functions in Drosophila melanogaster. Genetics. 1993 Mar;133(3):593–604. doi: 10.1093/genetics/133.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kuhn D. T., Packert G. Tumorous-head-type mutants of the distal bithorax complex cause dominant gain and recessive loss of function in Drosophila melanogaster. Dev Biol. 1988 Jan;125(1):8–18. doi: 10.1016/0012-1606(88)90054-1. [DOI] [PubMed] [Google Scholar]
  31. Kuziora M. A. Abdominal-B protein isoforms exhibit distinct cuticular transformations and regulatory activities when ectopically expressed in Drosophila embryos. Mech Dev. 1993 Aug;42(3):125–137. doi: 10.1016/0925-4773(93)90002-f. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Lamka M. L., Boulet A. M., Sakonju S. Ectopic expression of UBX and ABD-B proteins during Drosophila embryogenesis: competition, not a functional hierarchy, explains phenotypic suppression. Development. 1992 Dec;116(4):841–854. doi: 10.1242/dev.116.4.841. [DOI] [PubMed] [Google Scholar]
  34. Macias A., Casanova J., Morata G. Expression and regulation of the abd-A gene of Drosophila. Development. 1990 Dec;110(4):1197–1207. doi: 10.1242/dev.110.4.1197. [DOI] [PubMed] [Google Scholar]
  35. Mann R. S. Engrailed-mediated repression of Ultrabithorax is necessary for the parasegment 6 identity in Drosophila. Development. 1994 Nov;120(11):3205–3212. doi: 10.1242/dev.120.11.3205. [DOI] [PubMed] [Google Scholar]
  36. Mann R. S., Hogness D. S. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell. 1990 Feb 23;60(4):597–610. doi: 10.1016/0092-8674(90)90663-y. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Michelson A. M. Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development. 1994 Apr;120(4):755–768. doi: 10.1242/dev.120.4.755. [DOI] [PubMed] [Google Scholar]
  39. O'Connor M. B., Binari R., Perkins L. A., Bender W. Alternative RNA products from the Ultrabithorax domain of the bithorax complex. EMBO J. 1988 Feb;7(2):435–445. doi: 10.1002/j.1460-2075.1988.tb02831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rauskolb C., Smith K. M., Peifer M., Wieschaus E. extradenticle determines segmental identities throughout Drosophila development. Development. 1995 Nov;121(11):3663–3673. doi: 10.1242/dev.121.11.3663. [DOI] [PubMed] [Google Scholar]
  41. Schneuwly S., Klemenz R., Gehring W. J. Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia. 1987 Feb 26-Mar 4Nature. 325(6107):816–818. doi: 10.1038/325816a0. [DOI] [PubMed] [Google Scholar]
  42. Simcox A. A., Hersperger E., Shearn A., Whittle J. R., Cohen S. M. Establishment of imaginal discs and histoblast nests in Drosophila. Mech Dev. 1991 Mar;34(1):11–20. doi: 10.1016/0925-4773(91)90087-m. [DOI] [PubMed] [Google Scholar]
  43. Struhl G. Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7380–7384. doi: 10.1073/pnas.79.23.7380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sánchez-Herrero E. Control of the expression of the bithorax complex genes abdominal-A and abdominal-B by cis-regulatory regions in Drosophila embryos. Development. 1991 Feb;111(2):437–449. doi: 10.1242/dev.111.2.437. [DOI] [PubMed] [Google Scholar]
  45. Sánchez-Herrero E., Guerrero I., Sampedro J., González-Reyes A. Developmental consequences of unrestricted expression of the abd-A gene of Drosophila. Mech Dev. 1994 Jun;46(3):153–167. doi: 10.1016/0925-4773(94)90068-x. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Tiong S., Bone L. M., Whittle J. R. Recessive lethal mutations within the bithorax-complex in Drosophila. Mol Gen Genet. 1985;200(2):335–342. doi: 10.1007/BF00425445. [DOI] [PubMed] [Google Scholar]
  48. Vachon G., Cohen B., Pfeifle C., McGuffin M. E., Botas J., Cohen S. M. Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less. Cell. 1992 Oct 30;71(3):437–450. doi: 10.1016/0092-8674(92)90513-c. [DOI] [PubMed] [Google Scholar]
  49. Warren R. W., Nagy L., Selegue J., Gates J., Carroll S. Evolution of homeotic gene regulation and function in flies and butterflies. Nature. 1994 Dec 1;372(6505):458–461. doi: 10.1038/372458a0. [DOI] [PubMed] [Google Scholar]
  50. White R. A., Wilcox M. Protein products of the bithorax complex in Drosophila. Cell. 1984 Nov;39(1):163–171. doi: 10.1016/0092-8674(84)90202-2. [DOI] [PubMed] [Google Scholar]
  51. Zavortink M., Sakonju S. The morphogenetic and regulatory functions of the Drosophila Abdominal-B gene are encoded in overlapping RNAs transcribed from separate promoters. Genes Dev. 1989 Dec;3(12A):1969–1981. doi: 10.1101/gad.3.12a.1969. [DOI] [PubMed] [Google Scholar]
  52. Zhao J. J., Lazzarini R. A., Pick L. The mouse Hox-1.3 gene is functionally equivalent to the Drosophila Sex combs reduced gene. Genes Dev. 1993 Mar;7(3):343–354. doi: 10.1101/gad.7.3.343. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES