Skip to main content
SpringerLink
Log in

Morphology of transcription units inDrosophila melanogaster

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

We have used an electron microscopic analysis to define and to characterize active transcription units ofDrosophila melanogaster. The lengths and spacings of nascent ribonuclear protein (RNP) fibers were determined on embryonic chromatin that was spread using techniques introduced by Miller and Beatty (1969). The data are consistent with the occurrence of specific sites of transcription initiation and termination. We apply the termtranscription unit (TU) to a chromatin region bounded by these control sites. Two classes of TUs are active inDrosophila melanogaster embryonic cells—those synthesizing ribosomal RNA and those synthesizing non-ribosomal RNA. The classes can usually be distinguished on the basis of TU size, chromatin morphology and inferred DNA packing ratio, frequency of RNP fibers (number of fibers per μm of chromatin), and the solitary vs. tandem repeat occurrence of fiber arrays. The results indicate that nonribosomal transcription units have lengths in accord with the expectation that DNA of each chromomere is transcribed as a unit.—Some nascent fiber arrays inD. melanogaster have more complex patterns of RNP fiber lengths. We suggest that these are a consequence of cleavage of RNP fibers at specific sites during transcription. — These sites of transcriptional control and the amounts of DNA between them provide a basis for further relating units of transcription to units of gene function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Angelier, N., Lacroix, J.C.: Complexes de transcription d'origines nucleolaire et chromosomique d'ovocytes de Pleurodeles waltlii et P. poireti (Amphibiens, Urodeles). Chromosoma (Berl.)51, 323–335 (1975)

    Google Scholar 

  • Axel, R., Cedar, H., Felsenfeld, G.: The structure of the globin genes in chromatin. Biochemistry (Wash.)14, 2489–2495 (1975)

    Google Scholar 

  • Beermann, W.: Chromomeres and genes. In: Results and problems-cell differentiation, Vol. 4 W. Beermann, J. Reinert and H. Ursprung, eds. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Bishop, J.O., Morton, J.G., Rosbash, M., Richardson, M.: Three abundance classes in HeLa cell messenger RNA. Nature (Lond.)250, 199–204 (1974)

    Google Scholar 

  • Bordier, C., Dubochet, J.: Electron microscopic localization of the binding sites of Escherichia coli RNA polymerase in the early promoter region of T7 DNA. Europ. J. Biochem.44, 617–624 (1974)

    Google Scholar 

  • Chooi, W.Y., Laird, C.D.: DNA and polyribosome-like material in lysates of mitochondria of Drosophila melanogaster. J. molec. Biol.100, 475–508 (1976)

    Google Scholar 

  • Daneholt, B.: Giant RNA in a Balbiani ring. Nature (Lond.) New Biol.240, 229 (1972)

    Google Scholar 

  • Darlix, J.-C., Dausse, J.-P.: Localization of Escherichia coli RNA polymerase initation sites in T7 DNA early promoter region. F.E.B.S. Letters50, 214–218 (1975)

    Google Scholar 

  • Darnell, J.E., Jelinek, W.R., Molloy, G.R.: Biogenesis of m-RNA: Genetic regulation in mammalian cells. Science181, 1212–1221 (1973)

    Google Scholar 

  • Davis, R.W., Hyman, R.W.: Physical locations of the in vitro RNA initiation site and termination sites of T7 M DNA. Cold Spr. Harb. Symp. quant. Biol.39, 269–281 (1970)

    Google Scholar 

  • Derksen, J., Trendelenburg, M.F., Scheer V., Franke, W.: Spread chromosomal nucleoli of Chironomus salivary gland. Exp. Cell Res.80, 476–479 (1973)

    Google Scholar 

  • Dunn, J.J., Studier, F.W.: Processing, transcription, and translation of bacteriophage T7 messenger RNAs. Brookhaven Symp. Biol.26, 267–276 (1975)

    Google Scholar 

  • Flanagan, J.R.: Maximum likelihood procedures for evaluating data of chromatin-associated fiber arrays.(Appendix to Laird et al., 1976). Chromosoma (Berl.)58, 191–192 (1976)

    Google Scholar 

  • Foe, V.E.: Activation of transcription units during the embryogenesis of Oncopeltus fasciatus. Ph. D. dissertation, University of Texas, Austin (1975)

    Google Scholar 

  • Foe, V.E., Wilkinson, L.E., Laird, C.D.: Comparative organization of active transcription units in Oncopeltus fasciatus. Cell9, 131–146 (1976)

    Google Scholar 

  • Glätzer, K.H.: Visualization of gene transcription in spermatocytes of Drosophila hydei. Chromosoma (Berl.)53, 371–380 (1975)

    Google Scholar 

  • Gottesfeld, J.M., Murphy, R.F., Bonner, J.: Structure of transcriptionally active chromatin. Proc. nat. Acad. Sci. (Wash.)72, 4404–4408 (1975)

    Google Scholar 

  • Hamkalo, B.A., Miller, O.L., Jr.: Electron microscopy of genetic activity. Ann. Rev. Biochem.42, 379–396 (1973)

    Google Scholar 

  • Hamkalo, B.A., Miller, O.L., Jr., Bakken, A.H. Ultrastructure of eukaryotic genomes. Cold Spr. Harb. Symp. quant. Biol.38, 915 (1973)

    Google Scholar 

  • Hennig, W., Meyer, G.F., Hennig, I., Leoncini, O.: Structure and function of the Y chromosome of Drosophila hydei. Cold Spr. Harb. Symp. quant. Biol.38, 673–683 (1973)

    Google Scholar 

  • Hochman, B.: Analysis of a whole chromosome in Drosophila. Cold Spr. Harb. Symp. quant. Biol.38, 581–589 (1974)

    Google Scholar 

  • Judd, B.H., Shen, M.W., Kaufman, T.C.: The anatomy and function of a segment of the X chromosome of Drosophila melanogaster. Genetics71, 139–156 (1972)

    Google Scholar 

  • Kierszenbaum, I.L., Trez, L.L.: Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J. Cell Biol.63, 923–935 (1974)

    Google Scholar 

  • Lacy, E., Axel, R.: Analysis of DNA of isolated chromatin subunits. Proc. nat. Acad. Sci. (Wash.)72, 3978–3982 (1975)

    Google Scholar 

  • Laird, C.D.: DNA of Drosophila chromosomes. Ann. Rev. Genet.7, 177–204 (1974)

    Google Scholar 

  • Laird, C.D., Wilkinson, L.E., Foe, V.E., Chooi, W.Y.: Analysis of chromatin-associated fiber arrays. Chromosoma (Berl.)58, 169–190 (1976)

    Google Scholar 

  • Lamb, M.M., Laird, C.D.: Size of poly A-containing RNAs in Drosophila melanogaster embryos. Biochem. Genet.14, 357–371 (1976a)

    Google Scholar 

  • Lamb, M.M., Laird, C.D.: Increase in nuclear poly A-containing RNA at syncytial blastoderm in Drosophila melanogaster embryos. Develop. Biol.52, 31–42 (1976b)

    Google Scholar 

  • Lengyel, J., Penman, S.: hnRNA size and processing as related to DNA content in two dipterans: Drosophila and Aedes. Cell5, 281–290 (1975)

    Google Scholar 

  • Lindsley, D.L., Grell, E.H.: Genetic variations of Drosophila melanogaster. Carnegie Inst. Wash. Publ.627 (1968)

  • McKnight, S.L., Miller, O.L., Jr.: Ultrastructural patterns of RNA synthesis during early embryogenesis of D. melanogaster. Cell8, 305–319 (1976)

    Google Scholar 

  • Meyer, G.F., Hennig, W.: The nucleolus in primary spermatocytes of Drosophila hydei. Chromosoma (Berl.)46, 121 (1974)

    Google Scholar 

  • Miller, O.L., Jr., Bakken, A.H.: Morphological studies of transcription. Acta endocr. (Kbh.), Suppl.168, 155–157 (1972)

    Google Scholar 

  • Miller, O.L., Jr., Beatty, B.R.: Visualization of nucleolar genes. Science164, 955 (1969)

    Google Scholar 

  • Miller, O.L., Jr., Beatty, B.R., Hamkalo, B.A., Thomas, C.A., Jr.: Electron microscopic visualization of transcription. Cold Spr. Harb. Symp. quant. Biol.35, 505 (1970)

    Google Scholar 

  • Perry, R.P., Cheng, T.Y., Freed, J.J., Greenberg, J.R., Kelley, D.E., Tartof, K.D.: Evolution of the transcriptional unit of ribosomal RNA. Proc. nat. Acad. Sci. (Wash.)65, 609 (1970)

    Google Scholar 

  • Robertson, H., Dickson, E.: RNA processing and the control of gene expression. Brookhaven Symp. Biol.26, 240–266 (1975)

    Google Scholar 

  • Scheer, U., Trendelenburg, M.F., Franke, W.W.: Transcription of ribosomal RNA cistrons. Correlation of morphological and biochemical data. Cell. Res.80, 175–190 (1973)

    Google Scholar 

  • Sommerville, J., Malcolm, D.B.: Transcription of genetic information in amphibian oocytes. Chromosoma (Berl.)55, 183–208 (1976)

    Google Scholar 

  • Spring, H., Trendelenburg, M.F., Scheer, U., Franke, W.F., Herth, W.: Structural and biochemical studies of the primary nucleus of two green algal species, Acetabularia mediterranea and Acetabularia major. Cytobiologie10, 1–65 (1974)

    Google Scholar 

  • Trendelenburg, M.F.: Morphology of ribosomal RNA cistrons in oocytes of the water beetle Dytiscus marginalis. Chromosoma (Berl.)48, 119 (1974)

    Google Scholar 

  • Trendelenburg, M.F., Scheer, V., Franke, W.W.: Structural organization of ribosomal DNA in oocytes of the house cricket. Nature (Lond.) New Biol.245, 167–170 (1973)

    Google Scholar 

  • Trendelenburg, M.F., Spring, H., Scheer, V., Franke, W.W.: Morphology of nucleolar cistrons in a plant cell, Acetabularia mediterranea. Proc. nat. Acad. Sci. (Wash.)71, 3626 (1974)

    Google Scholar 

  • Turner, S.H., Laird, C.D.: Diversity of RNA sequences in Drosophila melanogaster. Biochem. Genet.10, 263–274 (1973)

    Google Scholar 

  • Weinstein, A.: Heredity and development. In: Chemistry in medicine (J. Stieglitz, ed.). New York: The Chemical Foundation, 1928

    Google Scholar 

  • Weintraub, H., Groundine, M.: Transcriptionally active and inactive conformations of chromosomal subunits. Science (in press, 1976)

  • Zalokar, M.: Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Develop. Biol.49, 425–437 (1976)

    Google Scholar 

Download references

Author information

Author notes

  1. W. Yean Chooi

    Present address: Department of Zoology, University of Indiana, 47401, Bloomington, Indiana, USA

Authors and Affiliations

  1. Department of Zoology, University of Washington, 98195, Seattle, Washington, USA

    Charles D. Laird & W. Yean Chooi

Authors
  1. Charles D. Laird
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. Yean Chooi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laird, C.D., Chooi, W.Y. Morphology of transcription units inDrosophila melanogaster . Chromosoma 58, 193–218 (1976). https://doi.org/10.1007/BF00701359

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00701359

Keywords

Search

Navigation