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. 1988 Jul;7(7):2163–2173. doi: 10.1002/j.1460-2075.1988.tb03055.x

The Abdominal-B gene of Drosophila melanogaster: overlapping transcripts exhibit two different spatial distributions

Ernesto Sánchez-Herrero 1, Madeline A Crosby 1,1
PMCID: PMC454529  PMID: 16453854

Abstract

The Abdominal-B (Abd-B) gene of Drosophila controls the specification of segment identities in the posterior abdomen. We describe here the spatial and temporal distribution of Abd-B transcripts. At least five RNA species are detected on Northern blots with probes within the region of the Abd-B homeobox. We have identified probes specific for subsets of these transcripts and have used these probes to study the distribution of each subset by in situ hybridization to embryonic tissue sections. The transcripts can be divided into two groups: one group is expressed maximally in parasegment (PS)13 and extends anteriorly to PS10; the other is expressed only in PS14 and 15. These two different patterns of expression correspond to the anatomical domains defined by two classes of mutations in Abd-B. These results help explain the complex genetic interactions and phenotypes of mutations within this gene.

Keywords: bithorax complex, Abdominal-B, in situ hybridization, multiple transcripts, spatial regulation

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Selected References

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

  1. Abbott M. K., Kaufman T. C. The relationship between the functional complexity and the molecular organization of the Antennapedia locus of Drosophila melanogaster. Genetics. 1986 Nov;114(3):919–942. doi: 10.1093/genetics/114.3.919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akam M. E., Martinez-Arias A. The distribution of Ultrabithorax transcripts in Drosophila embryos. EMBO J. 1985 Jul;4(7):1689–1700. doi: 10.1002/j.1460-2075.1985.tb03838.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carroll S. B., Scott M. P. Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell. 1985 Nov;43(1):47–57. doi: 10.1016/0092-8674(85)90011-x. [DOI] [PubMed] [Google Scholar]
  4. Casanova J., Sánchez-Herrero E., Busturia A., Morata G. Double and triple mutant combinations of bithorax complex of Drosophila. EMBO J. 1987 Oct;6(10):3103–3109. doi: 10.1002/j.1460-2075.1987.tb02619.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Casanova J., Sánchez-Herrero E., Morata G. Identification and characterization of a parasegment specific regulatory element of the abdominal-B gene of Drosophila. Cell. 1986 Nov 21;47(4):627–636. doi: 10.1016/0092-8674(86)90627-6. [DOI] [PubMed] [Google Scholar]
  6. Casanova J., White R. A. Trans-regulatory functions in the Abdominal-B gene of the bithorax complex. Development. 1987 Sep;101(1):117–122. doi: 10.1242/dev.101.Supplement.117. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  9. Duncan I. The bithorax complex. Annu Rev Genet. 1987;21:285–319. doi: 10.1146/annurev.ge.21.120187.001441. [DOI] [PubMed] [Google Scholar]
  10. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  12. Fjose A., McGinnis W. J., Gehring W. J. Isolation of a homoeo box-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcripts. Nature. 1985 Jan 24;313(6000):284–289. doi: 10.1038/313284a0. [DOI] [PubMed] [Google Scholar]
  13. Hafen E., Kuroiwa A., Gehring W. J. Spatial distribution of transcripts from the segmentation gene fushi tarazu during Drosophila embryonic development. Cell. 1984 Jul;37(3):833–841. doi: 10.1016/0092-8674(84)90418-5. [DOI] [PubMed] [Google Scholar]
  14. Harding K., Levine M. Gap genes define the limits of antennapedia and bithorax gene expression during early development in Drosophila. EMBO J. 1988 Jan;7(1):205–214. doi: 10.1002/j.1460-2075.1988.tb02801.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Henikoff S. Cloning exons of mapping of transcription: characterization of the Drosophila melanogaster alcohol dehydrogenase gene. Nucleic Acids Res. 1983 Jul 25;11(14):4735–4752. doi: 10.1093/nar/11.14.4735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Hogness D. S., Lipshitz H. D., Beachy P. A., Peattie D. A., Saint R. B., Goldschmidt-Clermont M., Harte P. J., Gavis E. R., Helfand S. L. Regulation and products of the Ubx domain of the bithorax complex. Cold Spring Harb Symp Quant Biol. 1985;50:181–194. doi: 10.1101/sqb.1985.050.01.024. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Kornberg T., Sidén I., O'Farrell P., Simon M. The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell. 1985 Jan;40(1):45–53. doi: 10.1016/0092-8674(85)90307-1. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Levine M., Harding K., Wedeen C., Doyle H., Hoey T., Radomska H. Expression of the homeo box gene family in Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:209–222. doi: 10.1101/sqb.1985.050.01.027. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Lewis E. B. Regulation of the genes of the bithorax complex in Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:155–164. doi: 10.1101/sqb.1985.050.01.021. [DOI] [PubMed] [Google Scholar]
  26. Macdonald P. M., Struhl G. A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature. 1986 Dec 11;324(6097):537–545. doi: 10.1038/324537a0. [DOI] [PubMed] [Google Scholar]
  27. Martinez-Arias A., Lawrence P. A. Parasegments and compartments in the Drosophila embryo. Nature. 1985 Feb 21;313(6004):639–642. doi: 10.1038/313639a0. [DOI] [PubMed] [Google Scholar]
  28. McGinnis W., Levine M. S., Hafen E., Kuroiwa A., Gehring W. J. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. 1984 Mar 29-Apr 4Nature. 308(5958):428–433. doi: 10.1038/308428a0. [DOI] [PubMed] [Google Scholar]
  29. Mlodzik M., Fjose A., Gehring W. J. Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J. 1985 Nov;4(11):2961–2969. doi: 10.1002/j.1460-2075.1985.tb04030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mlodzik M., Gehring W. J. Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell. 1987 Feb 13;48(3):465–478. doi: 10.1016/0092-8674(87)90197-8. [DOI] [PubMed] [Google Scholar]
  31. Muriel W. J., Cole J., Lehmann A. R. Molecular analysis of ouabain-resistant mutants of the mouse lymphoma cell line L5178Y. Mutagenesis. 1987 Sep;2(5):383–389. doi: 10.1093/mutage/2.5.383. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  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. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Sánchez-Herrero E., Casanova J., Kerridge S., Morata G. Anatomy and function of the bithorax complex of Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:165–172. doi: 10.1101/sqb.1985.050.01.022. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Tiong S. Y., Whittle J. R., Gribbin M. C. Chromosomal continuity in the abdominal region of the bithorax complex of Drosophila is not essential for its contribution to metameric identity. Development. 1987 Sep;101(1):135–142. doi: 10.1242/dev.101.1.135. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. 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]
  44. Weir M. P., Kornberg T. Patterns of engrailed and fushi tarazu transcripts reveal novel intermediate stages in Drosophila segmentation. Nature. 1985 Dec 5;318(6045):433–439. doi: 10.1038/318433a0. [DOI] [PubMed] [Google Scholar]
  45. Whittle J. R., Tiong S. Y., Sunkel C. E. The effect of lethal mutations and deletions within the bithorax complex upon the identity of caudal metameres in the Drosophila embryo. J Embryol Exp Morphol. 1986 Apr;93:153–166. [PubMed] [Google Scholar]

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