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Chromosoma

, Volume 55, Issue 2, pp 183–208 | Cite as

Transcription of genetic information in amphibian oocytes

  • John Sommerville
  • David B. Malcolm
Article

Abstract

The lampbrush chromosomes of amphibian oocytes are highly active in RNA transcription. The extent of transcription and features of the transcriptional product have been studied both cytologically and by molecular hybridization. Each lampbrush loop is considered to be a unit of transcription which generates many primary transcript molecules. InTriturus the primary transcripts can be recovered as nuclear RNP particles which can be dispersed in the presence of formamide to give linear forms of up to 20 μm or more in length. Only part of the RNA extracted from nuclear RNP codes for protein, the remainder containing non-informational repetitive sequences. Although about 4% of the chromosomal DNA ofTriturus is transcribed during oogenesis, only 0.05–0.1% of the DNA is expressed as coding sequences. This informational sequence complexity is equivalent to approximately 104 different mRNA species. A model for the organization of genetic sequences in the lampbrush chromosomes is suggested.

Keywords

Developmental Biology Formamide Genetic Information Linear Form Repetitive Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Angelier, N., Lacroix, J. C.: Complexes de transcription d'origines nucléolaire et chromosomique d'ovocytes de Pleurodeles waltlii et P. poireti. Chromosoma (Berl.)51, 323–335 (1975)Google Scholar
  2. Bishop, J. O.: The effect of genetic complexity on the time-course of ribonucleic acid-deoxyribonucleic acid hybridization. Biochem. J.113, 805–811 (1969)Google Scholar
  3. 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
  4. Bishop, J. O., Rosbash, M.: Reiteration frequency of duck haemoglobin genes. Nature (Lond.) New Biol.241, 204–207 (1973)Google Scholar
  5. Blobel, G., Potter, V. R.: Nuclei from rat liver: isolation method that combines purity with high yield. Science154, 1662–1665 (1966)Google Scholar
  6. Bonner, T. I., Brenner, D. J., Neufeld, B. R., Britten, R. J.: Reduction in the rate of DNA reassociation by sequence divergence. J. molec. Biol.81, 123–135 (1973)Google Scholar
  7. Britten, R. J., Kohne, D. E.: Repeated sequences in DNA. Science161, 529–540 (1968)Google Scholar
  8. Callan, H. G.: The nature of lampbrush chromosomes. Int. Rev. Cytol.15, 1–34 (1963)Google Scholar
  9. Callan, H. G., Lloyd, L.: Lampbrush chromosomes of crested newts Triturus cristatus. Phil. Trans, roy. Soc. Lond. B243, 135–219 (1960)Google Scholar
  10. Commerford, S. L.: Iodination of nucleic acids in vitro. Biochemistry10, 1993–1999 (1971)Google Scholar
  11. Daneholt, B.: Giant RNA transcript in a Balbiani ring. Nature (Lond.) New Biol.240, 229–232 (1972)Google Scholar
  12. Darnell, J. E., Jelinek, W. R., Molloy, G. R.: Biogenesis of mRNA: Genetic regulation in mammalian cells. Science181, 1215–1221 (1973)Google Scholar
  13. Davidson, E. H.: Gene activity in early development, p. 217–243. New York: Academic Press 1968Google Scholar
  14. Davidson, E. H., Britten R. J.: Organization transcription and regulation in the animal genome. Quart. Rev. Biol.48, 565–613 (1973)Google Scholar
  15. Davidson E. H., Galau G. A. Angerer R. C. Britten R. J.: Comparative aspects of DNA organization in metozoa. Chromosoma (Berl.)51, 253–259 (1975)Google Scholar
  16. Davidson E. H., Hough, B. R.: Genetic information in oocyte RNA. J. molec. Biol.56, 491–506 (1971)Google Scholar
  17. Davidson, E. H., Hough, B. R., Amanson, C. S., Britten, R.J.: General interspersion of repetitive with non-repetitive sequence elements in the DNA of Xenopus. J. molec. Biol.77, 1–23 (1973)Google Scholar
  18. Davis, R. W., Simon, M., Davidson, N.: Electron microscope heteroduplex methods for mapping regions of base sequence homology in nucleic acids. Methods in enzymology, vol. XXId, p. 413–428. New York: Academic Press 1971Google Scholar
  19. Dounce, A. L. P.: Enzyme studies on isolated cell nuclei of rat liver. J. biol. Chem.147, 685–698 (1943)Google Scholar
  20. Gall, J. G.: On the submicroscopic structure of chromosomes. Brookhaven Symp. Biol.8, 17–32 (1956)Google Scholar
  21. Gall, J. G., Callan, H. G.:3H-uridine incorporation in lampbrush chromosomes. Proc. nat. Acad. Sci. (Wash.)48, 562–570 (1962)Google Scholar
  22. Getz, M. J., Altenburg, L. C., Saunders, G. F.: The use of RNA labelled in vitro with iodine 125 in molecular hybridization experiments. Biochim. biophys. Aota (Amst.)287, 485–494 (1972)Google Scholar
  23. Gummerson, K. S., Williamson, R.: Sequence divergence of mammalian globin messenger RNA. Nature (Lond.)247, 265–267 (1974)Google Scholar
  24. Holmes, D. S., Bonner, J.: Preparation, molecular weight, base composition and secondary structure of giant nuclear ribonucleic acid. Biochemistry12, 2330–2338 (1973)Google Scholar
  25. Hutton, J. R., Wetmur, J. G.: Renaturation of bacteriophage øX174 DNA-RNA hybrid: RNA length effect and nucleation rate constant. J. molec. Biol.77, 495–500 (1973)Google Scholar
  26. Imaizumi, T., Diggelmann, H., Scherrer, K.: Demonstration of globin messenger sequencesin giant nuclear precursors of messenger RNA of avian erythroblasts. Proo. nat. Acad. Sci. (Wash.)70, 1122–1126 (1973)Google Scholar
  27. Izawa, M., Allfrey, V. G., Mirsky, A. E.: The relationship between RNA synthesis and loop structure in lampbrush chromosomes. Proc. nat. Acad. Sci. (Wash.)49, 544–551 (1963)Google Scholar
  28. Laird, C. D., McCarthy, B. J.: Magnitude of interspecific nucleotide sequence variability of Drosophila. Genetics60, 303–312 (1968)Google Scholar
  29. Malcolm, D. B., Sommerville, J.: The structure of chromosome-derived ribonucleoprotein in oocytes of Triturus cristatus carnifex. Chromosoma (Berl.)48, 137–158 (1974)Google Scholar
  30. McKnight, G. S., Schimke, R. T.: Ovalbumin messenger RNA: evidence that the initial product of transcription is the same size as polysomal ovalbumin messenger. Proc. nat. Acad. Sci. (Wash.)71, 4327–4331 (1974)Google Scholar
  31. Melli, M., Ginelli, E., Corneo, G., di Lernia, R.: Clustering of the DNA sequences complementary to repetitive nuclear RNA of HeLa cells. J. molec. Biol.93, 23–38 (1975)Google Scholar
  32. Melli, M., Whitfield, C., Rao, K. V., Richardson, M., Bishop, J. O.: DNA-RNA hybridization in vast DNA excess. Nature (Lond.) New Biol.232, 8–12 (1971)Google Scholar
  33. Miller, O. L., Hamkalo, B. A.: Visualization of RNA synthesis on chromosomes. Int. Rev. Cytol.33, 1–23 (1972)Google Scholar
  34. Morescalchi, A., Serra, V.: DNA renaturation kinetics in some paedogenetic urodeles. Experientia (Basel)30, 487–489 (1974)Google Scholar
  35. Mott, M. R., Callan, H.G.: An electron-microscope study of the lampbrush chromosomes of the newt Triturus cristatus carnifex. J. Cell Sci.17, 241–261 (1975)Google Scholar
  36. Paul, J.: General theory of chromosomes structure and gene activation in eukaryotes. Nature (Lond.)238, 444–446 (1972)Google Scholar
  37. Perry, R. P., Kelley, D. E., LaTorre, J.: Synthesis and turnover of nuclear and cytoplasmic polyadenylic acid in mouse L cells. J. molec. Biol.82, 315–331 (1974)Google Scholar
  38. Rosbash, M., Ford, P. J.: Polyadenylic acid-containing RNA in Xenopus laevis oocytes. J. molec. Biol.85, 87–101 (1974)Google Scholar
  39. Rosbash, M., Ford, P. J., Bishop, J. O.: Analysis of the C-value paradox by molecular hybridization. Proc. nat. Acad. Sci. (Wash.)71, 3746–3750 (1974)Google Scholar
  40. Scott, S. E. M., Sommerville, J.: Location of nuclear proteins on the chromosomes of newt oocytes. Nature (Lond.)250, 680–682 (1974)Google Scholar
  41. Sexsmith, E.: DNA values and karyotypes of Amphibia. Ph.D. thesis, Dept. of Botany, Univ. of Toronto 1968Google Scholar
  42. Smith, M. J., Hough, B. R., Chamberlin, M. E., Davidson, E. H.: Repetitive and nonrepetitive sequence in sea urchin heterogeneous nuclear RNA. J. molec. Biol.85, 103–126 (1974)Google Scholar
  43. Sommerville, J.: Ribonucleoprotein particles derived from the lampbrush chromosomes of newt oocytes. J. molec. Biol.78, 487–503 (1973)Google Scholar
  44. Studier, F. W.: Sedimentation studies of the size and shape of DNA. J. molec. Biol.11, 373–390 (1965)Google Scholar
  45. Sutton, W. D.: A crude nuclease preparation suitable for use in DNA reassociation experiments. Biochim. biophys. Acta (Amst.)240, 522–531 (1971)Google Scholar
  46. Wilson, D. A., Thomas, C. A., Jr.: Palindromes in chromosomes. J. molec. Biol.84, 115–144 (1974)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • John Sommerville
    • 1
  • David B. Malcolm
    • 1
  1. 1.Department of ZoologyThe UniversitySt. Andrews, FifeScotland

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