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

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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.

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References

  1. Bird, A.P.: A study of early events in ribosomal gene amplification. Cold Spr. Harb. Symp. quant. Biol. 42, 1179–1183 (1978)

  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 1977

  3. Brown, D.D., Dawid, I.B.: Specific gene amplification in oocytes. Science 160, 272–280 (1968)

  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)

  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)

  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)

  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 1971

  8. Gall, G.J.: Differential synthesis of the genes for ribosomal RNA during amphibian oogenesis. Proc. nat. Acad. Sci. (Wash.) 69, 533–560 (1968)

  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)

  10. Gall, J.G., Rochaix, J.D.: The amplified ribosomal DNA of dytiscid beetles. Proc. nat. Acad. Sci. (Wash.) 71, 1819–1823 (1974)

  11. Gilbert, W., Dressler, D.: DNA replication: the rolling circle model. Cold Spr. Harb. Symp. quant. Biol. 33, 473–484 (1968)

  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)

  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)

  14. Kunz, W.: Lampenbürstenchromosomen und multiple Nucleolen bei Orthopteren. Chromosoma (Berl.) 21, 446–462 (1967)

  15. Lima-de-Faria, A., Birnstiel, M., Jaworska, H.: Amplification of ribosomal cistrons in the heterochromatin of Acheta. Genetics (Suppl.) 61, 145–159 (1969)

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

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

  18. Nilsson, B.: Acheta domesticus (Orthoptera), some cytological observations. Landbrukshogskolans Annaler 34, 437–464 (1968)

  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)

  20. Rochaix, J.D., Bird, A., Bakken, A.: Ribosomal RNA gene amplification by rolling circles. J. molec. Biol. 87, 473–487 (1974)

  21. Tartof, K.D.: Redundant genes. Ann. Rev. Genet. 9, 355–385 (1975)

  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)

  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)

  24. Wellauer, P.K., Dawid, I.B.: The structural organization of ribosomal DNA in Drosophila melanogaster. Cell 10, 193–212 (1977)

  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)

  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)

  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)

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Cave, M.D. Length heterogeneity of amplified circular rDNA molecules in oocytes of the house cricket Acheta domesticus (Orthoptera: Gryllidae). Chromosoma 71, 15–27 (1979). https://doi.org/10.1007/BF00426364

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Keywords

  • Hybridization Data
  • Size Heterogeneity
  • Region Account
  • Approximate Molecular Weight
  • Length Heterogeneity