Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories

Nature Genetics volume 14, pages 406–414 (1996)Cite this article

Abstract

Recent studies of human oocytes have demonstrated an enrichment for distal exchanges among meiosis I (MI) nondisjunction events and for proximal exchanges among meiosis II (MII) events. Our characterization of 103 cases of spontaneous X chromosome nondisjunction in Drosophila oocytes strongly parallels these observations. The recombinational histories of MI (97/103) and MII (6/103) nondisjunctional ova were strikingly different. MI nondisjunction occurred primarily in oocytes with non–exchange X chromosomes; of the few nondisjoining exchange bivalents, most carried distal crossovers. Thus, spontaneous MI nondisjunction reflects the failure of the achiasmate segregation systems. MII nondisjunction occurred only in oocytes with proximal exchanges. We propose several models to explain how very proximal exchanges might impair proper segregation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Hawley, R.S. et al. There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev. Genet. 13, 440–467 (1993).

    Article  Google Scholar 

  2. Sherman, S.L. et al. Nondisjunction of chromosome 21 in maternal meiosis I: evidence for a maternal age-dependent mechanism involving reduced recombination. Hum. Mol. Genet. 3, 1529–1535 (1994).

    Article  CAS  PubMed  Google Scholar 

  3. MacDonald, M. et al. The origin of 47,XXY and 47,XXX aneuploidy. Hum. Mol. Genet. 3, 1365–1371 (1994).

    Article  CAS  PubMed  Google Scholar 

  4. Theurkauf, W.E. & Hawley, R.S. Meiotic spindle assembly in Drosophila females: behavior of the nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J. Cell. Biol. 116, 1167–1180 (1992).

    Article  CAS  PubMed  Google Scholar 

  5. McKim, K.S. & Hawley, R.S. Chromosomal control of meiotic cell division. Science 270, 1595–1601 (1995).

    Article  CAS  PubMed  Google Scholar 

  6. Hawley, R.S., Frazier, J.A. & Rasooly, R. Separation anxiety: the etiology of nondisjunction in flies and people. Hum. Mol. Genet. 3, 1521–1528 (1994).

    Article  CAS  PubMed  Google Scholar 

  7. Bridges, C.B. Non-disjunction as proof of the chromosome theory of heredity. Genetics 1, 1–52 (1916).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Sturtevant, A.M. & Beadle, G.W. The relations of inversions in the X chromosome of Drosophita melanogaster to crossing over and disjunction. Genetics 21, 554–604 (1936).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Hawley, R.S., McKim, K.S. & Arbel, T. Meiotic segregation in Drosophila melanogaster females: molecules, mechanisms, and myths. Annu. Rev. Genet. 27, 281–317 (1993).

    Article  CAS  PubMed  Google Scholar 

  10. Karpen, G.H., Le, M.-H. & Le, H. Centric heterochromatln and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273, 118–122 (1996).

    Article  CAS  PubMed  Google Scholar 

  11. Dernburg, A.F., Sedat, J.W. & Hawley, R.S. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 85, 135–146 (1996).

    Article  Google Scholar 

  12. Merriam, J.R. & Frost, J.N. Exchange and nondisjunction of the X chromosomes in female Drosophila melanogaster . Genetics 49, 109–122 (1964).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Lamb, N. et al. Maternal non-disjunction of chromosome 21 is initiated during meiosis I. Nature Genet. 14, 400–405 (1996).

    Article  CAS  PubMed  Google Scholar 

  14. Weinstein, A. The theory of multiple-strand crossing over. Genetics 21, 155–199 (1936).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Sandler, L., Lindsley, D.L., Nicoletti, B. & Trippa, G. Mutants affecting meiosis in natural populations of Drosophila melanogaster . Genetics 60, 525–558 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Hartwell, L.H., Dutcher, S.K., Wood, J.S. & Garvik, B. The fidelity of mitotic chromosome reproduction in Saccharomyces cerevisiae . Rec. Adv. Yeast Mol. Biol. 1, 28–38 (1982).

    Google Scholar 

  17. Carpenter, A.T.C. & Baker, B.S. On the control of the distribution of meiotic exchange in Drosophila melanogaster . Genetics 101, 81–89 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Green, M. Radiation induced reverse mutations in Drosophila melanogaster . Proc. Natl. Acad. Sci. USA 45, 16–18 (1959).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Darlington, C.D. Misdivision and the genetics of the centromere. J. Genet. 37, 341–364 (1939).

    Article  Google Scholar 

  20. Sears, E.R. Misdivision of univalents in common wheat. Chromosoma 4, 535–550 (1952).

    Article  CAS  PubMed  Google Scholar 

  21. Petersen, M.B. et al. Comparative study of microsatellite and cytogenetic markers for detecting the origin of the nondisjoined chromosome 21 in Down Syndrome. Am. J. Hum. Genet. 51, 516–525 (1992).

    PubMed Central  Google Scholar 

  22. Hawley, R.S. Exchange and chromosome segregation in eukaryotes. In Genetic Recombination (eds Kucherlapati, R. & Smith, G.) 497–525 (Am. Soc. Microbiol., Washington, D.C., 1988).

    Google Scholar 

  23. Koehler, K.E., Hawley, R.S., Sherman, S. & Hassold, T. Recombination and nondisjunction in humans and flies. Hum. Mol. Genet. 5, 1495–1505 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. Afshar, K., Barton, N.R., Hawley, R.S. & Goldstein, L.S.B. DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell 81, 129–138 (1995).

    Article  CAS  PubMed  Google Scholar 

  25. Afshar, K., Scholey, J. & Hawley, R.S. Identification of the chromosome localization domain of the Drosophila nod kinesin-like protein. J. Cell Biol. 131, 833–843 (1995).

    Article  CAS  PubMed  Google Scholar 

  26. Zitron, A.E. & Hawley, R.S. The genetic analysis of distributive segregation in Drosophila mefanogaster. I. Isolation and characterization of Aberrant X segregation (Axs), a mutation defective in chromosome partner choice. Genetics 122, 801–821 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hawley, R.S. & Therkauf, W.E. Requiem for the distributive system: achiasmate segregation in Drosophila females. Trends Genet 9, 310–317 (1993).

    Article  CAS  PubMed  Google Scholar 

  28. Knowles, B.A. & Hawley, R.S. Genetic analysis of microtubule motor proteins in Drosophila: a mutation at the ncd locus is a dominant enhancer of nod. Proc. Natl. Acad. Sci. USA 88, 7165–7169 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Baker, B.S. & Carpenter, A.T.C. Genetic analysis of sex chromosomal meiotic mutants in Drosophila melanogaster . Genetics 71, 255–286 (1972).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. O'Tousa, J. Meiotic chromosome behaviour influenced by mutation-altered disjunction in Drosophila melanogaster females. Genetics 102, 503–524 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Hassold, T.M., Adkins, K., Freeman, S. & Sherman, S. Recombination and maternal age-dependent nondisjunction: molecular studies of trisomy 16. Am. J. Hum. Genet. 57, 867–874 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Ross, L.O., Maxfield, R. & Dawson, D. Exchanges are not equally able to enhance meiotic chromosome segregation in yeast. Proc. Natl. Acad. Sci. USA 93, 4979–4983 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nicklas, R.B. Chromosome segregation mechanisms. Genetics 78, 205–213 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Angell, R.R., Xian, J., Keith, J., Ledger, W. & Baird, D.T. First meiotic division abnormalities in human oocytes: mechanism of trisomy formation. Cyrogenet. Cell Genet. 65, 194–202 (1994).

    Article  CAS  Google Scholar 

  35. Angell, R.R. Meiosis I in human oocytes. Cytogenet. Cell Genet. 69, 266–272 (1995).

    Article  CAS  PubMed  Google Scholar 

  36. Hunt, P., LeMaire, R., Embury, P., Sheean, L. & Mroz, K. Analysis of chromosome behavior in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum. Mol. Genet. 4, 2007–2012 (1995).

    Article  CAS  PubMed  Google Scholar 

  37. Carpenter, A.T.C. A mutant defective in distributive disjunction in Drosophila melanogaster . Genetics 73, 393–428 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Rasooly, R.S., New, C.M., Zhang, R., Hawley, R.S. & Baker, B.S. The lethal (1)TW-6cs mutation in Drosophila melanogaster is a dominant allele of nod and is associated with a single base pair change in the putative ATP-binding domain. Genetics 129, 409–422 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Zhang, P., Knowles, B.A., Goldstein, L.S.B. & Hawley, R.S. A kinesin-like protein required for distributive chromosome segregation in Drosophila. Cell 62, 1053–1062 (1990).

    Article  CAS  PubMed  Google Scholar 

  40. Matthies, H.J.G., McDonald, H.B., Goldstein, L.S.B. & Therkauf, W.E. Anastral meiotic spindle morphogenesis: role of the NCD kinesin-like protein. J. Cell Biol. (in the press).

  41. Endow, S.A., Henikoff, S. & Soler-Niedziela, L. Mediation of meiotic and early mitotic chromosome segregation in Drosophila by a protein related to kinesin. Nature 345, 81–83 (1990).

    Article  CAS  PubMed  Google Scholar 

  42. Stewart, R.T., Thaler, J.P. & Goldstein, L.S. Direction of microtubule movement is an intrinsic property of the motor domains of kinesin heavy chain and Drosophila ncd protein. Proc. Natl. Acad. Sci. USA 90, 5209–5213 (1990).

    Article  Google Scholar 

  43. Tokai, N. et al. Kid, a novel kinesin-like DNA binding protein, is localized to chromosomes and the mitotic spindle. EMBO J. 15, 457–467 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Abruzzo, M. & Hassold, T. Etiology of nondisjunction in humans. Environ. Mol. Mut. Suppl. 25, 38–47 (1995).

    Article  CAS  Google Scholar 

  45. White–Cooper, H., Alphey, L. & Glover, D.M. The cdc25 homologue twine is required for only some aspects of the entry into meiosis in Drosophila. J. Cell Science 106, 1035–1044 (1993).

    PubMed  Google Scholar 

  46. Jang, J.K., Messina, L., Erdman, M.B., Arbel, T. & Hawley, R.S. Induction of metaphase arrest in Drosophila oocytes by chiasma-based kinetochore tension. Science 268, 1917–1919 (1995).

    Article  CAS  PubMed  Google Scholar 

  47. Nicklas, R.B. Chromosome distribution: experiments on cell hybrids and in vitro . Phil. Trans. R. Soc. Lon. 277, 267–276 (1977).

    Article  CAS  Google Scholar 

  48. Novitski, E. Genetic measures of centromere activity in Drosophila melanogaster . J. Cell. Comp. Physiol. 45, 151–169 (1955).

    Article  CAS  Google Scholar 

  49. Goldstein, L.S.B. Mechanisms of chromosome orientation revealed by two meiotic mutants in Drosophila melanogaster . Chromosoma 78, 79–111 (1980).

    Article  CAS  PubMed  Google Scholar 

  50. Miyazaki, W.Y. & Orr-Weaver, T.L. Sister-chromatid misbehavior in Drosophila ord mutants. Genetics 132, 1047–1061 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Bickel, S.E., Wyman, D.W., Miyazaki, W.Y., Moore, D.P. & Orr-Weaver, T.L. Identification of ORD, a Drosophila protein essential for sister chromatid cohesion. EMBOJ. 15, 1451–1459 (1996).

    Article  CAS  Google Scholar 

  52. Kerrebrock, A.W., Moore, D.P., Wu, J.S. & Orr-Weaver, T.L. Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions. Cell 83, 247–256 (1995).

    Article  CAS  PubMed  Google Scholar 

  53. Nelson, C.R. & Szauter, P. Timing of mitotic chromosome loss caused by the ncd mutation of Drosophila melanogaster . Cell Motil. Cytoskel. 23, 34–44 (1992).

    Article  CAS  Google Scholar 

  54. Zhang, P. & Hawley, R.S. The genetic analysis of distributive segregation in Drosophila melanogaster. II. Further genetic analysis of the nod locus. Genetics 125, 115–127 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Lindsley, D.L. & Zimm, G.C. The genome of Drosophila melanogaster. (Academic Press, San Diego, USA, 1992).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics, Section of Molecular and Cellular Biology, University of California at Davis, Davis, California, 95616, USA

    Kara E. Koehler, Christina L. Boulton, Heather E. Collins, Rachael L. French, Kristin C. Herman, Soni M. Lacefield, Laurence D. Madden, Christopher D. Schuetz & R. Scott Hawley

Authors
  1. Kara E. Koehler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christina L. Boulton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heather E. Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachael L. French
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kristin C. Herman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Soni M. Lacefield
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Laurence D. Madden
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christopher D. Schuetz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. R. Scott Hawley
    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

Koehler, K., Boulton, C., Collins, H. et al. Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nat Genet 14, 406–414 (1996). https://doi.org/10.1038/ng1296-406

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1296-406

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing