Skip to main content
Genetics logoLink to Genetics
. 1999 Sep;153(1):49–55. doi: 10.1093/genetics/153.1.49

Centromere mapping functions for aneuploid meiotic products: Analysis of rec8, rec10 and rec11 mutants of the fission yeast Schizosaccharomyces pombe.

M D Krawchuk 1, W P Wahls 1
PMCID: PMC1460729  PMID: 10471699

Abstract

Recent evidence suggests that the position of reciprocal recombination events (crossovers) is important for the segregation of homologous chromosomes during meiosis I and sister chromatids during meiosis II. We developed genetic mapping functions that permit the simultaneous analysis of centromere-proximal crossover recombination and the type of segregation error leading to aneuploidy. The mapping functions were tested in a study of the rec8, rec10, and rec11 mutants of fission yeast. In each mutant we monitored each of the three chromosome pairs. Between 38 and 100% of the chromosome segregation errors in the rec8 mutants were due to meiosis I nondisjunction of homologous chromosomes. The remaining segregation errors were likely the result of precocious separation of sister chromatids, a previously described defect in the rec8 mutants. Between 47 and 100% of segregation errors in the rec10 and rec11 mutants were due to nondisjunction of sister chromatids during meiosis II. In addition, centromere-proximal recombination was reduced as much as 14-fold or more on chromosomes that had experienced nondisjunction. These results demonstrate the utility of the new mapping functions and support models in which sister chromatid cohesion and crossover position are important determinants for proper chromosome segregation in each meiotic division.

Full Text

The Full Text of this article is available as a PDF (109.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. De Veaux L. C., Hoagland N. A., Smith G. R. Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe. Genetics. 1992 Feb;130(2):251–262. doi: 10.1093/genetics/130.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. DeVeaux L. C., Smith G. R. Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes Dev. 1994 Jan;8(2):203–210. doi: 10.1101/gad.8.2.203. [DOI] [PubMed] [Google Scholar]
  3. Fisher J. M., Harvey J. F., Morton N. E., Jacobs P. A. Trisomy 18: studies of the parent and cell division of origin and the effect of aberrant recombination on nondisjunction. Am J Hum Genet. 1995 Mar;56(3):669–675. [PMC free article] [PubMed] [Google Scholar]
  4. Fox M. E., Smith G. R. Control of meiotic recombination in Schizosaccharomyces pombe. Prog Nucleic Acid Res Mol Biol. 1998;61:345–378. doi: 10.1016/s0079-6603(08)60831-4. [DOI] [PubMed] [Google Scholar]
  5. Gutz H. Site Specific Induction of Gene Conversion in SCHIZOSACCHAROMYCES POMBE. Genetics. 1971 Nov;69(3):317–337. doi: 10.1093/genetics/69.3.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hassold T., Merrill M., Adkins K., Freeman S., Sherman S. Recombination and maternal age-dependent nondisjunction: molecular studies of trisomy 16. Am J Hum Genet. 1995 Oct;57(4):867–874. [PMC free article] [PubMed] [Google Scholar]
  7. Koehler K. E., Boulton C. L., Collins H. E., French R. L., Herman K. C., Lacefield S. M., Madden L. D., Schuetz C. D., Hawley R. S. Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nat Genet. 1996 Dec;14(4):406–414. doi: 10.1038/ng1296-406. [DOI] [PubMed] [Google Scholar]
  8. Koehler K. E., Hawley R. S., Sherman S., Hassold T. Recombination and nondisjunction in humans and flies. Hum Mol Genet. 1996;5(Spec No):1495–1504. doi: 10.1093/hmg/5.supplement_1.1495. [DOI] [PubMed] [Google Scholar]
  9. Krawchuk M. D., DeVeaux L. C., Wahls W. P. Meiotic chromosome dynamics dependent upon the rec8(+), rec10(+) and rec11(+) genes of the fission yeast Schizosaccharomyces pombe. Genetics. 1999 Sep;153(1):57–68. doi: 10.1093/genetics/153.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lamb N. E., Freeman S. B., Savage-Austin A., Pettay D., Taft L., Hersey J., Gu Y., Shen J., Saker D., May K. M. Susceptible chiasmate configurations of chromosome 21 predispose to non-disjunction in both maternal meiosis I and meiosis II. Nat Genet. 1996 Dec;14(4):400–405. doi: 10.1038/ng1296-400. [DOI] [PubMed] [Google Scholar]
  11. Li Y. F., Numata M., Wahls W. P., Smith G. R. Region-specific meiotic recombination in Schizosaccharomyces pombe: the rec11 gene. Mol Microbiol. 1997 Mar;23(5):869–878. doi: 10.1046/j.1365-2958.1997.2691632.x. [DOI] [PubMed] [Google Scholar]
  12. Lin Y., Larson K. L., Dorer R., Smith G. R. Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe. Genetics. 1992 Sep;132(1):75–85. doi: 10.1093/genetics/132.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lin Y., Smith G. R. Molecular cloning of the meiosis-induced rec10 gene of Schizosaccharomyces pombe. Curr Genet. 1995 Apr;27(5):440–446. doi: 10.1007/BF00311213. [DOI] [PubMed] [Google Scholar]
  14. MacDonald M., Hassold T., Harvey J., Wang L. H., Morton N. E., Jacobs P. The origin of 47,XXY and 47,XXX aneuploidy: heterogeneous mechanisms and role of aberrant recombination. Hum Mol Genet. 1994 Aug;3(8):1365–1371. doi: 10.1093/hmg/3.8.1365. [DOI] [PubMed] [Google Scholar]
  15. Molnar M., Bähler J., Sipiczki M., Kohli J. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics. 1995 Sep;141(1):61–73. doi: 10.1093/genetics/141.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Moore D. P., Miyazaki W. Y., Tomkiel J. E., Orr-Weaver T. L. Double or nothing: a Drosophila mutation affecting meiotic chromosome segregation in both females and males. Genetics. 1994 Mar;136(3):953–964. doi: 10.1093/genetics/136.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Moore D. P., Orr-Weaver T. L. Chromosome segregation during meiosis: building an unambivalent bivalent. Curr Top Dev Biol. 1998;37:263–299. doi: 10.1016/s0070-2153(08)60177-5. [DOI] [PubMed] [Google Scholar]
  18. Munz P. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics. 1994 Jul;137(3):701–707. doi: 10.1093/genetics/137.3.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Parisi S., McKay M. J., Molnar M., Thompson M. A., van der Spek P. J., van Drunen-Schoenmaker E., Kanaar R., Lehmann E., Hoeijmakers J. H., Kohli J. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol. 1999 May;19(5):3515–3528. doi: 10.1128/mcb.19.5.3515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ponticelli A. S., Smith G. R. Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics. 1989 Sep;123(1):45–54. doi: 10.1093/genetics/123.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rasooly R. S., New C. M., Zhang P., Hawley R. S., Baker B. S. The lethal(1)TW-6cs mutation of Drosophila melanogaster is a dominant antimorphic allele of nod and is associated with a single base change in the putative ATP-binding domain. Genetics. 1991 Oct;129(2):409–422. doi: 10.1093/genetics/129.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Roeder G. S. Meiotic chromosomes: it takes two to tango. Genes Dev. 1997 Oct 15;11(20):2600–2621. doi: 10.1101/gad.11.20.2600. [DOI] [PubMed] [Google Scholar]
  23. Ross L. O., Treco D., Nicolas A., Szostak J. W., Dawson D. Meiotic recombination on artificial chromosomes in yeast. Genetics. 1992 Jul;131(3):541–550. doi: 10.1093/genetics/131.3.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sherman S. L., Petersen M. B., Freeman S. B., Hersey J., Pettay D., Taft L., Frantzen M., Mikkelsen M., Hassold T. J. Non-disjunction of chromosome 21 in maternal meiosis I: evidence for a maternal age-dependent mechanism involving reduced recombination. Hum Mol Genet. 1994 Sep;3(9):1529–1535. doi: 10.1093/hmg/3.9.1529. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES