Meiosis pp 35-53 | Cite as

Methods for Analysis of Crossover Interference in Saccharomyces cerevisiae

  • Franklin W. Stahl
  • Elizabeth A. Housworth
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 557)

Abstract

Interest in crossover interference in yeast has been spurred by the discovery and characterization of mutants that alter it as well as by the development and testing of models to explain it. This chapter describes methods for detecting and for measuring interference, with emphasis on those that exploit the ability to examine all four products of individual acts of meiosis.

Key words

NPD ratio coefficient of coincidence counting model Erlang distribution Gamma distribution Chi-square distribution 

Notes

Acknowledgments

F.W.S. thanks John P. Nolan for drawing his attention to the view that the distribution of intercrossover distances in the Counting Model is aptly referred to as an Erlang distribution. Tom Petes notified us that the Web site “Stahl Lab Online Tools” mindlessly calculated fN exp values for fT obs > 2/3. It no longer does. Jette Foss provided invaluable editing of the manuscript. The Genetics Community is grateful to Richard Lowry, author of the continually improving, user-friendly web site VassarStats. Dan Graham kindly updated Stahl Lab Online Tools to reflect things we learned during the preparation of this Chapter; in doing so he caught some mistakes in our manuscript. The contribution by E.A.H. was supported by an NSF grant (DMS-0306243) to Indiana University.

References

  1. 1.
    Lhuissier, F. G. P., Offenberg, H. H., Wittich, P. E., Vischer, N. O. E. and Heyting, C. (2007) The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. The Plant Cell 19, 862–876.PubMedCrossRefGoogle Scholar
  2. 2.
    Fung, J. C., Rockmill, B., Odell, M. and Roeder, G. S. (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116, 795–802.PubMedCrossRefGoogle Scholar
  3. 3.
    Sturtevant, A. H. (1915) The behavior of the chromosomes, as studied through linkage. Zeit. f. ind. Abst. u. Vereb. 13, 234–287.CrossRefGoogle Scholar
  4. 4.
    Muller, H. J. (1916) The mechanism of crossing over. Am. Nat. 50, 194–221 and ff.Google Scholar
  5. 5.
    Papazian, H. P. (1952) The analysis of tetrad data. Genetics 37, 175–188.PubMedGoogle Scholar
  6. 6.
    Haldane, J. B. S. (1919) The combination of linkage values and the calculation of distances between loci of linked factors. J. Genet. 8, 299–309.CrossRefGoogle Scholar
  7. 7.
    Foss, E., Lande, R., Stahl, F. W. and Steinberg, C. M. (1993) Chiasma interference as a function of genetic distance. Genetics 133, 681–691. Corigendum: Genetics 134, 997.PubMedGoogle Scholar
  8. 8.
    Bailey, N. T. J. (1961) Introduction to the Mathematical Theory of Genetic Linkage, Oxford University Press, LondonGoogle Scholar
  9. 9.
    Zhao, H., McPeek, M. S. and Speed, T. P. (1995a) Statistical analysis of chromatid interference. Genetics 139, 1057–1065.PubMedGoogle Scholar
  10. 10.
    Perkins, D. D. (1949) Biochemical mutants in the smut fungus Ustilago maydis. Genetics 34, 607–626.Google Scholar
  11. 11.
    Malkova, A., Swanson, J., German, M., McCusker, J. H., Housworth, E. A., Stahl, F. W. and Haber, J. E. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168, 49–63.PubMedCrossRefGoogle Scholar
  12. 12.
    McPeek, M. S. and Speed, T. P. (1995) Modeling interference in genetic recombination. Genetics 139, 1031–1044.PubMedGoogle Scholar
  13. 13.
    Zhao, H., Speed, T. P. and McPeek, M. S. (1995b) Statistical analysis of crossover interference using the Chi-Square model. Genetics 139, 1045–1056.PubMedGoogle Scholar
  14. 14.
    Broman, K. W. and Weber, J. L. (2001) Characterization of human crossover interference. Am. J. Hum. Genet. 66, 1911–1926.CrossRefGoogle Scholar
  15. 15.
    Kleckner, N., Zickler, D., Jones, G. H., Dekker, J., Padmore, R., Henle, J. and Hutchinson, J. (2004) A mechanical basis for chromosome function. Proc. Natl. Acad. Sci. USA 101, 12592–12597.PubMedCrossRefGoogle Scholar
  16. 16.
    Hilliker, A. J. and Chovnick, A. (1981) Further observations on intragenic recombination in Drosophila melanogaster. Genet. Res. 38, 281–296.Google Scholar
  17. 17.
    Hilliker, A. J., Clark, S. H. and Chovnick, A. (1991) The effect of DNA sequence polymorphisms on intragenic recombination in the rosy locus of Drosophila melanogaster. Genetics 129, 779–781.Google Scholar
  18. 18.
    Fisher, R. A. (1951) A combinatorial formulation of multiple linkage tests. Nature. 167, 520.PubMedCrossRefGoogle Scholar
  19. 19.
    Owen, A. R. G. (1949) The theory of genetical recombination. I. Long chromosome arms. Proc. Roy. Soc. B. 136, 67–94.CrossRefGoogle Scholar
  20. 20.
    Payne, L. C. (1956) The theoryof genetical recombination: a general formulation for a certain class of intercept length distributions appropriate to the discussion of multiple linkage. Proc. Roy. Soc. B. 144, 528–544.CrossRefGoogle Scholar
  21. 21.
    Cobbs, G. (1978) Renewal process approach to the theory of genetic linkage: case of no chromatid interference. Genetics 89, 563–581.PubMedGoogle Scholar
  22. 22.
    Stamm, P. (1979) Interference in genetic crossing over and chromosome mapping. Genetics 92, 573–594.Google Scholar
  23. 23.
    Mather, K. (1935) Reductional and equational separation of the chromosomes in bivalents and multivalents. J. Genet. 30, 53–78.CrossRefGoogle Scholar
  24. 24.
    Housworth, E. A. and Stahl, F. W. (2003) Crossover interference in humans. Am. J. Hum. Genet. 73, 188–197.PubMedCrossRefGoogle Scholar
  25. 25.
    Lam, S. Y., Horn, S. R., Radford, S. J., Housworth, E. A., Stahl, F. W. and Copenhaver, G. P. (2005) Crossover interference on nucleolus organizing region-bearing chromosomes in Arabidopsis. Genetics 170, 807–812.PubMedCrossRefGoogle Scholar
  26. 26.
    Getz, T. J., Banse, S. A., Young, L. S., Banse, A. V., Swanson, J, Wang, G. M., Browne, B. L., Foss, H. M. and Stahl, F. W. (2007) Differential mismatch repair of heteroduplexes distinguishes interfering from “non”-interfering crossing over in Saccharomyces cerevisiae. Genetics 178, 1251–1269.Google Scholar
  27. 27.
    Stahl, F. W. (2008) On the “NPD ratio” as a test for crossover interference. Genetics 179, 701–704.PubMedCrossRefGoogle Scholar
  28. 28.
    Copenhaver, G. P., Housworth, E. A. and Stahl, F. W. (2002) Crossover interference in Arabidopsis. Genetics 160, 1631–1639.PubMedGoogle Scholar
  29. 29.
    Stahl, F. W. and Lande, R. (1995) Estimating interference and linkage map distance from two-factor tetrad data. Genetics 139, 1449–1454.PubMedGoogle Scholar
  30. 30.
    Börner, G. V., Kleckner, N. and Hunter, N. (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29–45.PubMedCrossRefGoogle Scholar
  31. 31.
    Zalevsky, J., MacQueen, A. J., Duffy, J. B., Kemphues, K. J. and Villeneuve, A. M. (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153, 1271–1283.PubMedGoogle Scholar
  32. 32.
    Sturtevant, A. H. (1913) The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J. Exp. Zool. 14, 43–59.CrossRefGoogle Scholar
  33. 33.
    Strickland, W. N. (1958) An analysis of interference in Aspergillus nidulans. Proc. Roy. Soc. Lond. B. 149, 82–101.Google Scholar
  34. 34.
    Shinohara, M., Sakai, K., Shinohara, A. and Bishop, D. K. (2003) Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics 163, 1273–1286.PubMedGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Franklin W. Stahl
    • 1
  • Elizabeth A. Housworth
    • 2
  1. 1.Institute of Molecular Biology, University of OregonEugeneUSA
  2. 2.Department of Mathematics and Department of BiologymIndiana UniversityBloomingtonUSA

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