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. 1985 Nov;4(11):2961–2969. doi: 10.1002/j.1460-2075.1985.tb04030.x

Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage

Marek Mlodzik 1, Anders Fjose 1,1, Walter J Gehring 1
PMCID: PMC554605  PMID: 16453641

Abstract

We report the isolation and characterization of caudal (cad), a previously unknown Drosophila homeo box-containing gene from the 38E region on the left arm of the second chromosome. This homeo box has diverged from the prototype sequence in Antennapedia, but contains subregions which are highly homologous. By Northern analysis and in situ hybridization experiments two transcripts of ˜2.4 kb were found to accumulate in nurse cells and in the oocyte during oogenesis. These transcripts generate a transient concentration gradient along the antero-posterior axis at the syncytial blastoderm stage. At the cellular blastoderm stage transcripts accumulate in a single band from 13–19% egg length at the posterior end. One zygotic transcript of 2.6 kb is detected. At later stages this transcript is localized in ectodermally and endodermally derived tissues such as the proctodeum, the Malpighian tubules and the posterior midgut. The 2.6-kb transcript is detectable until the onset of metamorphosis.

Keywords: homeo box, homeotic genes, maternal expression, RNA localization, endoderm

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  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. Carrasco A. E., McGinnis W., Gehring W. J., De Robertis E. M. Cloning of an X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes. Cell. 1984 Jun;37(2):409–414. doi: 10.1016/0092-8674(84)90371-4. [DOI] [PubMed] [Google Scholar]
  3. Chan L. N., Gehring W. Determination of blastoderm cells in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2217–2221. doi: 10.1073/pnas.68.9.2217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  5. Colberg-Poley A. M., Voss S. D., Chowdhury K., Gruss P. Structural analysis of murine genes containing homoeo box sequences and their expression in embryonal carcinoma cells. 1985 Apr 25-May 1Nature. 314(6013):713–718. doi: 10.1038/314713a0. [DOI] [PubMed] [Google Scholar]
  6. Denell R. E. Homoeosis in Drosophila. II. a Genetic Analysis of Polycomb. Genetics. 1978 Oct;90(2):277–289. doi: 10.1093/genetics/90.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Duncan I. M. Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics. 1982 Sep;102(1):49–70. doi: 10.1093/genetics/102.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Frei E., Baumgartner S., Edström J. E., Noll M. Cloning of the extra sex combs gene of Drosophila and its identification by P-element-mediated gene transfer. EMBO J. 1985 Apr;4(4):979–987. doi: 10.1002/j.1460-2075.1985.tb03727.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fyrberg E. A., Mahaffey J. W., Bond B. J., Davidson N. Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell. 1983 May;33(1):115–123. doi: 10.1016/0092-8674(83)90340-9. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. 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]
  14. Kuroiwa A., Hafen E., Gehring W. J. Cloning and transcriptional analysis of the segmentation gene fushi tarazu of Drosophila. Cell. 1984 Jul;37(3):825–831. doi: 10.1016/0092-8674(84)90417-3. [DOI] [PubMed] [Google Scholar]
  15. Langer-Safer P. R., Levine M., Ward D. C. Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4381–4385. doi: 10.1073/pnas.79.14.4381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Langer P. R., Waldrop A. A., Ward D. C. Enzymatic synthesis of biotin-labeled polynucleotides: novel nucleic acid affinity probes. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6633–6637. doi: 10.1073/pnas.78.11.6633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lawrence P. A., Morata G. The early development of mesothoracic compartments in Drosophila. An analysis of cell lineage and fate mapping and an assessment of methods. Dev Biol. 1977 Mar;56(1):40–51. doi: 10.1016/0012-1606(77)90153-1. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Levine M., Rubin G. M., Tjian R. Human DNA sequences homologous to a protein coding region conserved between homeotic genes of Drosophila. Cell. 1984 Oct;38(3):667–673. doi: 10.1016/0092-8674(84)90261-7. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. McGinnis W., Hart C. P., Gehring W. J., Ruddle F. H. Molecular cloning and chromosome mapping of a mouse DNA sequence homologous to homeotic genes of Drosophila. Cell. 1984 Oct;38(3):675–680. doi: 10.1016/0092-8674(84)90262-9. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. McGinnis W., Shermoen A. W., Beckendorf S. K. A transposable element inserted just 5' to a Drosophila glue protein gene alters gene expression and chromatin structure. Cell. 1983 Aug;34(1):75–84. doi: 10.1016/0092-8674(83)90137-x. [DOI] [PubMed] [Google Scholar]
  26. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Müller M. M., Carrasco A. E., DeRobertis E. M. A homeo-box-containing gene expressed during oogenesis in Xenopus. Cell. 1984 Nov;39(1):157–162. doi: 10.1016/0092-8674(84)90201-0. [DOI] [PubMed] [Google Scholar]
  28. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Rozek C. E., Davidson N. Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell. 1983 Jan;32(1):23–34. doi: 10.1016/0092-8674(83)90493-2. [DOI] [PubMed] [Google Scholar]
  31. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Shepherd J. C., McGinnis W., Carrasco A. E., De Robertis E. M., Gehring W. J. Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins. Nature. 1984 Jul 5;310(5972):70–71. doi: 10.1038/310070a0. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Steward R., McNally F. J., Schedl P. Isolation of the dorsal locus of Drosophila. Nature. 1984 Sep 20;311(5983):262–265. doi: 10.1038/311262a0. [DOI] [PubMed] [Google Scholar]
  36. Struhl G. A gene product required for correct initiation of segmental determination in Drosophila. Nature. 1981 Sep 3;293(5827):36–41. doi: 10.1038/293036a0. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Wieschaus E., Gehring W. Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol. 1976 Jun;50(2):249–263. doi: 10.1016/0012-1606(76)90150-0. [DOI] [PubMed] [Google Scholar]

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