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Human meiosis IX. Crossing over and chiasma formation in oocytes

  • Maja Bojko
Article

Abstract

Human oocytes from foetal ovaries have been analyzed by serial sectioning and three dimensional reconstruction from electron micrographs. Analysis of five late zygotene, twenty pachytene, four early and three mid diplotene nuclei allowed the following observations and conclusions: 1) Nuclei at pachytene can by morphological criteria be allocated into three substages. 2) The synaptonemal complex complement is twice as long in the oocytes as in the spermatocytes. 3) The total number of nodules decreases from a mean of 68 at late zygotene to a mean of 30 at early diplotene. During pachytene, an increasing number of nodules transforms into bars. A mean of 6 bars was observed in late zygotene nuclei compared to a mean of 17 at late pachytene. 4) Nodules and bars are distributed nonrandomly among the bivalents and bivalent arms. The observed frequency of bivalents devoid of recombination structures is only between one- and two-thirds of the frequency expected if nodules were distributed at random. 5) The distribution of recombination structures along the bivalent arms is not uniform. More nodules and bars than expected from a random distribution are located in the vicinity of telomeres. Comparison of neighbour nodule/bars distances at different substages of pachytene indicated that the elimination of recombination structures primarily affects nodules and bars close to each other. 6) The distribution of recombination structures along the individual bivalents was uneven, regions with high frequency of recombination nodules and bars alternating with regions of low frequency. This pattern is very similar to that reported for human spermatocytes, which indicates the same distribution of crossovers in the two sexes. 7) Elimination of the synaptonemal complex starts at early diplotene at a limited number of sites until about 68 intact segments are created. 8) Chiasmata are not morphologically recognizable after the elimination of the synaptonemal complex is completed at mid diplotene.

Keywords

Human female meiosis synaptonemal complex recombination nodule bar 

References

  1. 1.
    Abirached-Darmency, M., D. Zickler &Y. Cauderon: Synaptonemal complex and recombination nodules in rye (Secale cereale). Chromosoma (Berl.) 88, 299–306 (1983)CrossRefGoogle Scholar
  2. 2.
    Andersson, L. &K. Sandberg: Genetic linkage in the horse. II. Distribution of male recombination estimates and the influence of age, breed and sex on recombination frequency. Genetics 106, 109–122 (1984)PubMedGoogle Scholar
  3. 3.
    Baker, T.G.: A quantitative and cytological study of germ cells in human ovaries. Proc. Roy. Soc. B. 158, 417–433 (1963)Google Scholar
  4. 4.
    Baker, T.G. &P. Neal: Oogenesis in human fetal ovaries maintained in organ culture. J. Anat. 117, 591–604 (1974)PubMedGoogle Scholar
  5. 5.
    Bojko, M.: Human meiosis VIII: Chromosome pairing and formation of the synaptonemal complex in oocytes. Carlsberg Res. Commun. 48, 285–305 (1983)Google Scholar
  6. 6.
    Callan, H.G. &P.E. Perry: Recombination in male and female meiocytes contrasted. Philos. Trans. R. Soc. Lond. B. 277, 227–233 (1977)CrossRefGoogle Scholar
  7. 7.
    Carpenter, A.T.C.: Electron microscopy of meiosis in Drosophila melanogaster II. The recombination nodule—a recombination associated structure at pachytene. Proc. Nat. Acad. Sci. USA 72, 3186–3189 (1975)PubMedCrossRefGoogle Scholar
  8. 8.
    Carpenter, A.T.C.: Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster. Chromosoma (Berl.) 75, 259–292 (1979)CrossRefGoogle Scholar
  9. 9.
    Carpenter, A.T.C.: Synaptonemal complex and recombination nodules in wild-type Drosophila melanogaster females. Genetics 92, 511–541 (1979)PubMedGoogle Scholar
  10. 10.
    Carpenter, A.T.C.: EM autoradiographic evidence that DNA synthesis occurs at recombination nodules during meiosis in Drosophila melanogaster females. Chromosoma (Berl.) 83, 59–80 (1981)CrossRefGoogle Scholar
  11. 11.
    Cook, P.J.L.: The Lutheran-Secretor recombination fraction in man: a possible sex difference. Ann. Hum. Genet. Lond. 28, 393–401 (1965)CrossRefGoogle Scholar
  12. 12.
    Dunn, L.C. &D. Bennett: Sex differences in recombination of linked genes in animals. Genet. Res. Camb. 9, 211–220 (1967)Google Scholar
  13. 13.
    Edwards, R.G.: Observations on meiosis in normal males and females in human population cytogenetics. Ed. P.A. Jacobs, W.H. Price, P. Law. Pfizer Medical Monographs 5. Edinburgh, p. 9–21 (1970)Google Scholar
  14. 14.
    Ferguson-Smith, M.A.: Meiosis in the human male. In: Chromosomes Today. Vol. 5. Eds.: P.L. Pearson & K.R. Lewis. John Wiley & Sons, New York, pp 33–41 (1976)Google Scholar
  15. 15.
    Gillies, C.B.: The relationship between synaptonemal complexes, recombination nodules and crossing over in Neurospora crassa bivalents and translocation quadrivalents. Genetics 91, 1–17 (1979)PubMedGoogle Scholar
  16. 16.
    Goldstein, P. &A.C. Triantaphyllou: Occurrence of synaptonemal complexes and recombination nodules in a meiotic race of Meloidogyne hapla and their absence in a mitotic race. Chromosoma (Berl.) 68, 91–100 (1978)CrossRefGoogle Scholar
  17. 17.
    Heller, C.G. &Y. Clermont: Kinetics of the germinal epithelium in man. Recent Prog. Horm. Res. 20, 545–575 (1964)PubMedGoogle Scholar
  18. 18.
    Holm, P.B. &S.W. Rasmussen: Chromosome pairing, recombination nodules and chiasma formation in diploid Bombyx males. Carlsberg Res. Commun. 45, 483–548 (1980)Google Scholar
  19. 19.
    Holm, P.B. &S.W. Rasmussen: Human meiosis V. Substages of pachytene in human spermatogenesis. Carlsberg Res. Commun. 48, 351–383 (1983)Google Scholar
  20. 20.
    Holm, P.B. &S.W.:Rasmussen: Human meiosis VI. Crossing over in human spermatocytes. Carlsberg Res. Commun. 48, 385–413 (1983)Google Scholar
  21. 21.
    Holm P.B. &S.W. Rasmussen: Human meiosis VII. Chiasma formation in human spermatocytes. Carlsberg Res. Commun. 48, 415–456 (1983)Google Scholar
  22. 22.
    Holm, P.B., S.W. Rasmussen, D. Zickler, B.C. Lu &J. Sage: Chromosome pairing, recombination nodules and chiasma formation in the basidiomycete Coprinus cinereus. Carlsberg Res. Commun. 46, 305–346 (1981)CrossRefGoogle Scholar
  23. 23.
    Hulten, M.: Chiasma distribution at diakinesis in the normal human male. Hereditas 76, 55–78 (1974)PubMedGoogle Scholar
  24. 24.
    Jagiello, G., M. Duncayen, J.-S. Fang &J. Graffeo: Cytogenetic observations in mammalian oocytes. In: Chromosomes Today, Vol. 5, Eds.: P.L. Pearson and K.R. Lewis. John Wiley & Sons, New York, pp 43–63 (1974)Google Scholar
  25. 25.
    Kundu, S.C. &Yu.F. Bogdanov: Ultrastructural studies of late meiotic prophase nuclei of spermatocytes in Ascaris suum. Chromosoma (Berl.) 70, 375–384 (1979)CrossRefGoogle Scholar
  26. 26.
    Rasmussen, S.W.: The meiotic prophase in Bombyx mori females analyzed by three dimentional reconstructions of synaptonemal complexes. Chromosoma (Berl.) 54, 245–293 (1976)CrossRefGoogle Scholar
  27. 27.
    Rasmussen, S.W. &P.B. Holm: Human meiosis II. Chromosome pairing and recombination nodules in human spermatocytes. Carlsberg Res. Commun. 43, 275–327 (1978)CrossRefGoogle Scholar
  28. 28.
    Rasmussen, S.W. &P.B. Holm: Mechanics of meiosis. Hereditas, 93, 187–216 (1980)PubMedGoogle Scholar
  29. 29.
    Weitkamp, L.R., J.J. van Rood, E. Thorsby, W. Bias, M. Fotino, S.D. Lawler, J. Dausset, W.R. Mayr, J. Bodmer, F.E. Ward, J. Seignalet, R. Payne, F. Kissmeyer-Nielsen, R.A. Gatti, J.A. Sachs &L.U. Lamm: The relation of parental sex and age to recombination in the HL-A system. Human Heredity 23, 197–205 (1973)PubMedCrossRefGoogle Scholar
  30. 30.
    Westergaard, M. &D. von Wettstein: The synaptinemal complex. Ann. Rev. Genet. 6, 71–110 (1972)PubMedCrossRefGoogle Scholar
  31. 31.
    Wettstein, D. von, S.W. Rasmussen &P.B. Holm: The synaptonemal complex in genetic segregation. Ann. Rev. Genet. 18, 331–413 (1984)Google Scholar
  32. 32.
    Whitehouse, H.L.: Genetic recombination. Understanding the mechanisms. Chichester, John Wiley & Sons (1982)Google Scholar
  33. 33.
    Zickler, D.: Development of the synaptonemal complex and the “recombination nodules” during meiotic prophase in the seven bivalents of the fungus Sordaria macrospora Auersw. Chromosoma (Berl.) 61, 289–316 (1977)CrossRefGoogle Scholar
  34. 34.
    Zickler, D. &J. Sage: Synaptonemal complexes with modified lateral elements in Sordaria humana: Development of and relationship to the “recombination nodules”. Chromosoma (Berl.) 84, 305–316 (1981)CrossRefGoogle Scholar

Copyright information

© Carlsberg Laboratory 1985

Authors and Affiliations

  • Maja Bojko
    • 1
  1. 1.Department of PhysiologyCarlsberg LaboratoryCopenhagen Valby

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