Skip to main content
SpringerLink
Log in

Morphology of ribosomal RNA cistrons in oocytes of the water beetle, Dytiscus marginalis L.

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Transcriptional activity of the dispersed extrachromosomal body in oocyte nuclei of Dytiscus marginalis was demonstrated with electron microscopy using the spreading technique. This rDNA containing material appeared as large or small aggregates of positively stained extended axial fibrils and groups of densely packed lateral fibrils, which were attached to the former and showed, within one group, a gradual increase in length. On the axial fibrils one can thus distinguish alternating fibril-covered (“matrix unit”) and fibril-free (“spacer”) intercepts which are interpreted as representing the regions of rDNA which are transcribed into precursor molecules of rRNAs and those which do not contain (pre)rRNA cistrons. The pattern in Dytiscus essentially resembles those described for spread nucleolar material from amphibian and insect oocytes and various other cell types. However, this pattern is distinguished from most other nucleolar material described, with the exception of the extrachromosomal body in oocytes of Acheta domesticus, by the great length of the matrix (mean 3.71 μm) and spacer (range from 3.2 to 7.2 μm) units. Frequently small units of an apparently closed circular axial fibril which comprise only 2 to 4 matrix units and interspersed spacer regions are noted.

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

  • Bauer, H.: Die wachsenden Oocytenkerne einiger Insekten in ihrem Verhalten zur Nuklealfärbung. Z. Zellforsch. 18, 254–298 (1933)

    Google Scholar 

  • Bier, K.: Oogenese, das Wachstum von Riesenzellen. Naturwissenschaften 54, 189–195 (1967)

    Google Scholar 

  • Bier, K., Kunz, W., Ribbert, D.: Struktur und Funktion der Oocytenchromosomen und Nukleolen sowie der Extra-DNS während der Oogenese panoistischer und meroistischer Insekten. Chromosoma (Berl.) 23, 214–254 (1967)

    Google Scholar 

  • Bier, K., Ribbert, D.: Struktur und genetische Aktivität des DNS-Keimbahnkörpers von Dytiscus. Naturwissenschaften 53, 115 (1966)

    Google Scholar 

  • Bird, A. P., Rochaix, J.-D., Bakken, A. H.: The mechanism of gene amplification in Xenopus laevis oocytes. In: Molecular cytogenetics. (B. A. Hamkalo and J. Papaconstantinou, eds.), p. 49–58. New York: Plenum Press 1973

    Google Scholar 

  • Birnstiel, M. L., Chipchase, M., Speirs, J.: The ribosomal RNA cistrons. Progr. Nucleic Acid Res. 11, 351–389 (1971)

    Google Scholar 

  • Busch, H., Smetana, K.: The nucleolus. New York: Academic Press 1970

    Google Scholar 

  • Callan, H. G., Lloyd, L.: Lampbrush chromosomes of crested newts Triturus cristatus (Laurenti). Phil. Trans. B 243, 135–219 (1960)

    Google Scholar 

  • Dalgarno, L., Hosking, D. M., Shen, C. H.: Steps in the biosynthesis of ribosomal RNA in cultured Aedes aegypti cells. Europ. J. Biochem. 24, 489–506 (1972)

    Google Scholar 

  • Debaisieux, P.: Les débuts de l'ovogénèse dans le Dytiscus marginalis. La Cellule 25, 207–236 (1909)

    Google Scholar 

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

    Google Scholar 

  • Ficq, A., Urbani, E.: Cytochemical studies on the oogenesis of Dytiscus marginalis L. Exp. Cell Res. 55, 243–247 (1969)

    Google Scholar 

  • Franke, W. W.: Nuclear envelopes. Structure and biochemistry of the nuclear envelope. Phil. Trans. B 268, 67–93 (1974)

    Google Scholar 

  • Franke, W. W., Scheer, U.: Structures and functions of the nuclear envelope. In: The cell nucleus, vol. I. (H. Busch, ed.) 220–238. New York: Academic Press (1974)

    Google Scholar 

  • Gall, J. G.: Lampbrush chromosomes from oocyte nuclei of the newt. J. Morph. 94, 283–352 (1954)

    Google Scholar 

  • Gall, J. G.: Techniques for the study of lampbrush chromosomes. In: Methods in cell physiology, vol. II. (D. M. Prescott, ed.), p. 37–60. New York: Academic Press 1966

    Google Scholar 

  • Gall, J. G.: The genes for ribosomal RNA during Oogenesis. Genetics 61, Suppl., 121–132 (1969)

    Google Scholar 

  • Gall, J. G.: The ribosomal cistrons in dytiscid beetles. J. Cell Biol. 47, 68a (1970)

  • Gall, J. G., Macgregor, H. C., Kidston, M. E.: Gene amplification in the oocytes cf dytiscid water beetles. Chromosoma (Berl.) 26, 169–187 (1969)

    Google Scholar 

  • Giardina, A.: Origine dell'oocite e delia cellule nutrici nel Dytiscus. Int. Monatschr. Anat. Physiol. 18, 418–484 (1901)

    Google Scholar 

  • Günthert, T.: Die Eibildung der Dytisciden. Zool. Jb. Anat. 30, 301–372 (1910)

    Google Scholar 

  • Hamkalo, B. A., Miller, O. L., Bakken, A. H.: Ultrastructural aspects of genetic activity. In: Molecular cytogenetics. (B. A. Hamkalo, J. Papaconstantinou, eds.), p. 315–323. New York: Plenum Press 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 

  • Hourcade, D., Dressler, D., Wolfson, J.: The nucleolus and the rolling circle. Cold Spr. Harb. Symp. quant. Biol. 38, 537–650 (1973a)

    Google Scholar 

  • Hourcade, D., Dressler, D., Wolfson, J.: The amplification of ribosomal RNA genes involves a rolling circle intermediate. Proc. nat. Acad. Sci. (Wash.) 70, 2926–2930 (1973b)

    Google Scholar 

  • Kato, K.: Cytochemistry and fine structure of elimination chromatin in Dytiscidae. Exp. Cell Res. 52, 507–522 (1968)

    Google Scholar 

  • Lane, N. J.: Spheroidal and ring nucleoli in amphibian oocytes. Patterns of uridine incorporation and fine structural features. J. Cell Biol. 35, 421–434 (1967)

    Google Scholar 

  • Lima-de-Faria, A.: DNA replication and gene amplification in heterochromatin. In: Handbook of molecular cytology (A. Lima-de-Faria, ed.), p. 277–325. Amsterdam: North-Holland Publishing Co. 1969

    Google Scholar 

  • Lima-de-Faria, A.: The molecular organization of the chromomeres of Acheta involved in ribosomal DNA amplification. Cold Spr. Harb. Symp. quant. Biol. 38, 559–572 (1973)

    Google Scholar 

  • Loening, U. E.: Molecular weights of ribosomal RNA in relation to evolution. J. molec. Biol. 38, 355–365 (1968)

    Google Scholar 

  • Macgregor, H. C.: The nucleolus and its genes in amphibian oogenesis. Biol. Rev. 47, 177–210 (1972)

    Google Scholar 

  • Meyer, G. F., Hennig, W.: The nucleolus in primary spermatocytes of Drosophila hydei. Chromosoma (Berl.) 46, 121–144 (1974)

    Google Scholar 

  • Miller, O. L.: Fine structure of lampbrush chromosomes. Nat. Cancer Inst. Monogr. 18, 79–99 (1965)

    Google Scholar 

  • Miller, O. L.: Structure and composition of peripheral nucleoli of salamander oocytes. Nat. Cancer Inst. Monogr. 23, 53–66 (1966)

    Google Scholar 

  • Miller, O. L., Bakken, A. H.: Morphological studies of transcription. Acta endocr. (Kbh.), Suppl. 168, 155–177 (1972)

    Google Scholar 

  • Miller, O. L., Beatty, B. R.: Nucleolar structure and function. In: Handbook of molecular cytology (A. Lima-de-Faria, ed.), p. 605–619. Amsterdam: North-Holland Publishing Co. 1969a

    Google Scholar 

  • Miller, O. L., Beatty, B. R.: Visualization of nucleolar genes. Science 164, 955–957 (1969b)

    Google Scholar 

  • Miller, O. L., Beatty, B. R.: Extrachromosomal nucleolar genes in amphibian oocytes. Genetics, Suppl. 61, 134–143 (1969c)

    Google Scholar 

  • Miller, O. L., Beatty, B. R.: Portrait of a gene. J. cell. Physiol. 74, Suppl. 1, 225–232 (1969d)

    Google Scholar 

  • Miller, O. L., Hamkalo, B. A.: Visualization of RNA synthesis on chromosomes. Int. Rev. Cytol. 33, 1–25 (1972)

    Google Scholar 

  • Nusbaum-Hilarowicz, J.: Über das Verhalten des Chondrioms während der Eibildung bei Dytiscus marginalis L. Z. Zool. 117, 554–589 (1918)

    Google Scholar 

  • Pero, R., Lima-de-Faria, A., Ståhle, U., Granström, H., Ghatnekar, R.: Amplification of ribosomal DNA in Acheta. IV. The number of eistrons for 28 S and 18 S ribosomal RNA. Hereditas (Lund) 73, 195–210 (1973)

    Google Scholar 

  • Perry, R. P., Cheng, T. Y., Freed, J. J., Greenberg, J. R., Kelley, D. E., Tartof, K. D.: Evolution of the transcription unit of ribosomal RNA. Proc. nat. Acad. Sci. (Wash.) 65, 609–616 (1970)

    Google Scholar 

  • Ringborg, U., Daneholt, B., Edström, J.-E., Egyházi, E., Lambert, B.: Electrophoretic characterization of nucleolar RNA from Chironomus tentans salivary gland cells. J. molec. Biol. 51, 327–340 (1970)

    Google Scholar 

  • Rubinstein, L., Clever, U.: Non-conservative processing of ribosomal RNA in an insect, Chironomus tentans. Biochim. biophys. Acta (Amst.) 246, 517–529 (1971)

    Google Scholar 

  • Scheer, U.: Strukturen und Funktionen der Porenkomplexe in der Amphibieneizelle. Thesis, University of Freiburg, p. 1–174 (1970)

  • Scheer, U.: The ultrastructure of the nuclear envelope of amphibian oocytes. IV. On the chemical nature of nuclear pore complex material. Z. Zellforsch. 127, 127–148 (1972)

    Google Scholar 

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

    Google Scholar 

  • Shine, J., Dalgarno, L.: Occurrence of heat-dissociable ribosomal RNA in insects: The presence of three polynucleotide chains in 26 S RNA from cultured Aedes aegypti cells. J. molec. Biol. 75, 57–72 (1973)

    Google Scholar 

  • Trendelenburg, M. F., Scheer, U., 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, U., Franke, W. W.: Morphology of nucleolar eistrons in a plant cell, Acetabularia mediterranea. Proc. nat. Acad. Sci. (Wash.) (in press, 1974)

  • Ullman, J. S., Lima-de-Faria, A., Jaworska, H., Bryngelsson, T.: Amplification of ribosomal DNA in Acheta. V. Hybridization of RNA complementary to ribosomal DNA with pachytene chromosomes. Hereditas (Lund) 74, 13–24 (1973)

    Google Scholar 

  • Urbani, E.: La massa di Giardina dell'oocite di Dytiscus marginalis L. Riv. Biol. 42, 413–442 (1950)

    Google Scholar 

  • Urbani, E.: Cytochemical and ultrastructural studies of oogenesis in the Dytiscidae. Mon. Zool. Ital. (N.S.) 3, 55–87 (1969)

    Google Scholar 

  • Urbani, E.: A survey on some aspects of oogenesis in Dytiscus, Cybister, and Hygrobia (Coleoptera). Acta Embryol. Morph. exp. (Palermo) 3, 281–297 (1970)

    Google Scholar 

  • Urbani, E., Russo-Caia, S.: Osservazioni citochimice e autoradiografiche sul metabolismo degli acidi nucleici nella oogenesi di Dytiscus marginalis L. Rend. Ist. Sci. Univ. Camerino 5, 19–50 (1964)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Membrane Biology and Biochemistry, Institute of Experimental Pathology German Cancer Research Center, Heidelberg

    Michael F. Trendelenburg

Authors
  1. Michael F. Trendelenburg
    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

Trendelenburg, M.F. Morphology of ribosomal RNA cistrons in oocytes of the water beetle, Dytiscus marginalis L.. Chromosoma 48, 119–135 (1974). https://doi.org/10.1007/BF00283959

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00283959

Keywords

Search

Navigation