The distribution of Ultrabithorax transcripts in Drosophila embryos (original) (raw)

Abstract

We have used in situ hybridization to monitor the distribution of Ultrabithorax (Ubx) transcripts during the early stages of Drosophila embryogenesis. When first detectable, in the late syncytial blastoderm, Ubx transcripts are broadly distributed from 20 to 50% egg length (measured from the posterior pole). By the completion of cellular blastoderm formation, a precisely bounded zone one segment wide is defined by the accumulation of high levels of Ubx transcripts. This zone is probably the primordium for parasegment 6, that is, the posterior compartment of the third thoracic segment (T3) and the anterior compartment of the first abdominal segment (A1). Following gastrulation, seven metameric units of the germ band express Ubx transcripts in most or all cells of both the ectoderm and the mesoderm. This principal domain of Ubx expression is sharply bounded at superficial grooves in the embryo which probably mark the A/P compartment boundaries in T3 and A7, and so consists of parasegments 6-12. Outside this region, Ubx transcripts can be detected in only a few cells of the ectoderm of parasegments 5 and 13, and in the amnioserosa. This distribution suggests that the major role of Ubx in the early embryo lies in the morphological domain generally ascribed to the control of the bithoraxoid gene. Later in embryogenesis, the pattern of Ubx transcript accumulation is different in each of the major germ layers, suggesting that different controls regulate Ubx in each. In the ectoderm, but not in the mesoderm, Ubx transcripts accumulate differentially in anterior and posterior compartments. Probes prepared from different regions of the Ubx transcription unit show related but different patterns of hybridization. These patterns suggest that the 3.2-kb Ubx transcript is distributed throughout the wider domain of Ubx expression, but that the 4.7-kb transcript accumulates preferentially in parasegment 6.

Keywords: in situ hybridization, bithorax complex, embryology, spatial regulation, homoeotic

1689

Images in this article

Selected References

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

  1. Akam M. E. The location of Ultrabithorax transcripts in Drosophila tissue sections. EMBO J. 1983;2(11):2075–2084. doi: 10.1002/j.1460-2075.1983.tb01703.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Fyrberg E. A., Kindle K. L., Davidson N., Kindle K. L. The actin genes of Drosophila: a dispersed multigene family. Cell. 1980 Feb;19(2):365–378. doi: 10.1016/0092-8674(80)90511-5. [DOI] [PubMed] [Google Scholar]
  5. Garcia-Bellido A., Ripoll P., Morata G. Developmental compartmentalisation of the wing disk of Drosophila. Nat New Biol. 1973 Oct 24;245(147):251–253. doi: 10.1038/newbio245251a0. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Hafen E., Levine M., Garber R. L., Gehring W. J. An improved in situ hybridization method for the detection of cellular RNAs in Drosophila tissue sections and its application for localizing transcripts of the homeotic Antennapedia gene complex. EMBO J. 1983;2(4):617–623. doi: 10.1002/j.1460-2075.1983.tb01472.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hayashi S., Gillam I. C., Delaney A. D., Tener G. M. Acetylation of chromosome squashes of Drosophila melanogaster decreases the background in autoradiographs from hybridization with [125I]-labeled RNA. J Histochem Cytochem. 1978 Aug;26(8):677–679. doi: 10.1177/26.8.99471. [DOI] [PubMed] [Google Scholar]
  9. Hayes P. H., Sato T., Denell R. E. Homoeosis in Drosophila: the ultrabithorax larval syndrome. Proc Natl Acad Sci U S A. 1984 Jan;81(2):545–549. doi: 10.1073/pnas.81.2.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ingham P. W. A gene that regulates the bithorax complex differentially in larval and adult cells of Drosophila. Cell. 1984 Jul;37(3):815–823. doi: 10.1016/0092-8674(84)90416-1. [DOI] [PubMed] [Google Scholar]
  11. Lawrence P. A., Johnston P. On the role of the engrailed+ gene in the internal organs of Drosophila. EMBO J. 1984 Dec 1;3(12):2839–2844. doi: 10.1002/j.1460-2075.1984.tb02217.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lawrence P. A., Johnston P. The genetic specification of pattern in a Drosophila muscle. Cell. 1984 Mar;36(3):775–782. doi: 10.1016/0092-8674(84)90357-x. [DOI] [PubMed] [Google Scholar]
  13. Lawrence P. A., Morata G. The elements of the bithorax complex. Cell. 1983 Dec;35(3 Pt 2):595–601. doi: 10.1016/0092-8674(83)90091-0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Lohs-Schardin M., Cremer C., Nüsslein-Volhard C. A fate map for the larval epidermis of Drosophila melanogaster: localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Dev Biol. 1979 Dec;73(2):239–255. doi: 10.1016/0012-1606(79)90065-4. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Mitchison T. J., Sedat J. Localization of antigenic determinants in whole Drosophila embryos. Dev Biol. 1983 Sep;99(1):261–264. doi: 10.1016/0012-1606(83)90275-0. [DOI] [PubMed] [Google Scholar]
  20. Morata G., Kerridge S. Sequential functions of the bithorax complex of Drosophila. Nature. 1981 Apr 30;290(5809):778–781. doi: 10.1038/290778a0. [DOI] [PubMed] [Google Scholar]
  21. Simcox A. A., Sang J. H. When does determination occur in Drosophila embryos? Dev Biol. 1983 May;97(1):212–221. doi: 10.1016/0012-1606(83)90078-7. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Thomas J. B., Bastiani M. J., Bate M., Goodman C. S. From grasshopper to Drosophila: a common plan for neuronal development. Nature. 1984 Jul 19;310(5974):203–207. doi: 10.1038/310203a0. [DOI] [PubMed] [Google Scholar]
  25. Turner F. R., Mahowald A. P. Scanning electron microscopy of Drosophila melanogaster embryogenesis. II. Gastrulation and segmentation. Dev Biol. 1977 Jun;57(2):403–416. doi: 10.1016/0012-1606(77)90225-1. [DOI] [PubMed] [Google Scholar]
  26. 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]