Chromosoma

, Volume 71, Issue 1, pp 15–27 | Cite as

Length heterogeneity of amplified circular rDNA molecules in oocytes of the house cricket Acheta domesticus (Orthoptera: Gryllidae)

  • M. Donald Cave
Article

Abstract

Amplification of the genes coding for rRNA occurs in the oocytes of a wide variety of organisms. The amplification process appears to be mediated through a rolling-circle mechanism. The approximate molecular weight of the smallest rDNA circles is equivalent to the estimated combined molecular weight of DNA which codes for a single ribosomal RNA precursor molecule and an associated non-transcribed spacer DNA sequence. RNA-DNA hybridization studies carried out on oocytes of the house cricket, Acheta domesticus, suggest that DNA coding for rRNA accounts for only a small fraction of the rDNA satellite, all of which is amplified in the oocyte. In order to test the possibility that the remainder of the amplified rDNA represents spacer and to determine whether a rolling-circle mechanism might also be involved in amplification in A. domesticus oocytes, rDNA was isolated from ovaries of A. domesticus and spread for electron microscopy. A large proportion of the rDNA isolated from ovaries is circular, while main-band DNA and rDNA prepared from other tissues demonstrates few if any circles. The mean size of the smallest rDNA circles is approximately 8 times longer than the length estimated for DNA which codes for 18 S and 28 S rRNA. Denaturation mapping shows the rDNA circles to contain two major readily denaturing regions located about equidistant from one another on the circle. Each readily denaturing region accounts for 4–6% of the total DNA in the circle. The fact that only 12% of the average molecule is required to code for A. domesticus 18 S and 28 S rRNA is consistent with the hybridization data. Considerable size heterogeneity exists in the length of the smallest class of rDNA molecules. In the rDNA of other species such heterogeneity has been shown to reside in the non-transcribed spacer.

Keywords

Hybridization Data Size Heterogeneity Region Account Approximate Molecular Weight Length Heterogeneity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bird, A.P.: A study of early events in ribosomal gene amplification. Cold Spr. Harb. Symp. quant. Biol. 42, 1179–1183 (1978)Google Scholar
  2. Birnstiel, M.L., Chipchase, M., Speirs, J.: The ribosomal RNA cistrons. In: Progress in nucleic acid research and molecular biology (J.N. Davidson and W.F. Cohn, eds.), Vol. 11, pp. 351–389. New York: Academic Press 1977Google Scholar
  3. Brown, D.D., Dawid, I.B.: Specific gene amplification in oocytes. Science 160, 272–280 (1968)Google Scholar
  4. Buongiorno-Nardelli, M., Amaldi, F., Beccari, E.: Size of ribosomal rDNA repeating units in Xenopus laevis: Limited individual heterogeneity and extensive population polymorphism. J. molec. Biol. 110, 105–117 (1977)Google Scholar
  5. Cave, M.D.: Localization of ribosomal DNA within oocytes of the house cricket, Acheta domesticus (Orthoptera: Gryllidae). J. Cell Biol. 55, 310–321 (1972)Google Scholar
  6. Cave, M.D.: Synthesis and characterization of amplified DNA in oocytes of the house cricket Acheta domesticus (Orthoptera: Gryllidae). Chromosoma (Berl.) 42, 1–22 (1973)Google Scholar
  7. Davis, R., Simon, M., Davidson, N.: Electron microscope heteroduplex methods for mapping regions of base sequence homology in nucleic acids. In: Methods in enzymology (L. Grossman and K. Moldave, eds.), Vol. 21, pp. 413–430. New York: Academic Press 1971Google Scholar
  8. Gall, G.J.: Differential synthesis of the genes for ribosomal RNA during amphibian oogenesis. Proc. nat. Acad. Sci. (Wash.) 69, 533–560 (1968)Google Scholar
  9. Gall, J.G., Macgregor, H.C., Kidston, M.E.: Gene amplification in the oocytes of dytiscid water beetles. Chromosoma (Berl.) 26, 169–187 (1969)Google Scholar
  10. Gall, J.G., Rochaix, J.D.: The amplified ribosomal DNA of dytiscid beetles. Proc. nat. Acad. Sci. (Wash.) 71, 1819–1823 (1974)Google Scholar
  11. Gilbert, W., Dressler, D.: DNA replication: the rolling circle model. Cold Spr. Harb. Symp. quant. Biol. 33, 473–484 (1968)Google Scholar
  12. 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 (1973)Google Scholar
  13. Kalt, M.R., Gall, J.B.: Observations on early germ cell development and premeiotic ribosomal DNA amplification in Xenopus laevis. J. Cell Biol. 62, 460–472 (1974)Google Scholar
  14. Kunz, W.: Lampenbürstenchromosomen und multiple Nucleolen bei Orthopteren. Chromosoma (Berl.) 21, 446–462 (1967)Google Scholar
  15. Lima-de-Faria, A., Birnstiel, M., Jaworska, H.: Amplification of ribosomal cistrons in the heterochromatin of Acheta. Genetics (Suppl.) 61, 145–159 (1969)Google Scholar
  16. Miller, O.L., Jr.: Structure and composition of peripheral nucleoli of salamander oocytes. Nat. Cancer Inst. Monogr. 23, 53–66 (1966)Google Scholar
  17. Miller, O.L., Jr., Beatty, B.R.: Visualization of nucleolar genes. Science 164, 955–957 (1969)Google Scholar
  18. Nilsson, B.: Acheta domesticus (Orthoptera), some cytological observations. Landbrukshogskolans Annaler 34, 437–464 (1968)Google Scholar
  19. Pero, R., Lima-de-Faria, A., Stohle, U., Granstrom, H., Ghatnekar, R.: Amplification of ribosomal DNA in Acheta. IV. The number of cistrons for 28 S and 18 S ribosomal RNA. Hereditas (Lund) 73, 195–210 (1973)Google Scholar
  20. Rochaix, J.D., Bird, A., Bakken, A.: Ribosomal RNA gene amplification by rolling circles. J. molec. Biol. 87, 473–487 (1974)Google Scholar
  21. Tartof, K.D.: Redundant genes. Ann. Rev. Genet. 9, 355–385 (1975)Google Scholar
  22. Trendelenberg, M.F., Scheer, U., Franke, W.W.: Structural organization of the transcription of ribosomal DNA in oocytes of the house cricket. Nature (Lond.) 245, 167–170 (1973)Google Scholar
  23. Trendelenberg, M.F., Scheer, U., Zentgraf, W., Franke, W.W.: Heterogeneity of spacer lengths in circles of amplified ribosomal DNA of two insect species, Dytiscus marginalis and Acheta domesticus. J. molec. Biol. 108, 453–470 (1976)Google Scholar
  24. Wellauer, P.K., Dawid, I.B.: The structural organization of ribosomal DNA in Drosophila melanogaster. Cell 10, 193–212 (1977)Google Scholar
  25. Wellauer, P.K., Dawid, I.B., Brown, D.D., Reeder, R.H.: The molecular basis for length heterogeneity in ribosomal DNA from Xenopus laevis. J. molec. Biol. 105, 461–486 (1976b)Google Scholar
  26. Wellauer, P.K., Reeder, R.H., Caval, D., Brown, D.D., Deutch, A., Higashinakagawa, T., Dawid, I.B.: Amplified ribosomal DNA from Xenopus laevis has heterogenous spacer lengths. Proc. nat. Acad. Sci. (Wash.) 71, 2823–2827 (1974)Google Scholar
  27. Wellauer, P.K., Reeder, R.H., Dawid, I.B., Brown, D.D.: The arrangement of length heterogeneity in repeating units of amplified and chromosomal ribosomal DNA from Xenopus laevis. J. molec. Biol. 105, 487–505 (1976a)Google Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • M. Donald Cave
    • 1
  1. 1.Department of AnatomyUniversity of Arkansas for Medical SciencesLittle RockUSA

Personalised recommendations