Skip to main content
SpringerLink
Log in

Estimation of gametic frequencies from F2 populations using the EM algorithm and its application in the analysis of crossover interference in rice

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The gametes produced in meiosis provide information on the frequency of recombination and also on the interdependence of recombination events, i.e. interference. Using F2 individuals, it is not possible in all cases to derive the gametes, which have fused, and which provide the information about interference unequivocally when three or more segregating markers are considered simultaneously. Therefore, a method was developed to estimate the gametic frequencies using a maximum likelihood approach together with the expectation maximisation algorithm. This estimation procedure was applied to F2 mapping data from rice (Oryza sativa L.) to carry out a genome-wide analysis of crossover interference. The distribution of the coefficient of coincidence in dependence on the recombination fraction revealed for all chromosomes increasing positive interference with decreasing interval size. For some chromosomes this mutual inhibition of recombination was not so strong in small intervals. The centromere had a significant effect on interference. The positive interference found in the chromosome arms were reduced significantly when the intervals considered spanned the centromere. Two chromosomes even demonstrated independent recombination and slightly negative interference for small intervals including the centromere. Different marker densities had no effect on the results. In general, interference depended on the frequency of recombination events in relation to the physical length. The strength of the centromere effect on interference seemed to depend on the strength of recombination suppression around the centromere.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Chen M, Presting G, Barbazuk WB, Goicoechea JL, Blackmon B, Fang G, Kim H, Frisch D, Yu Y, Sun S, Higingbottom S, Phimphilai J, Phimphilai D, Thurmond S, Gaudette B, Li P, Liu J, Hatfield J, Main D, Farrar K, Henderson C, Barnett L, Costa R, et al (2002) An integrated physical and genetic map of the rice genome. Plant Cell 14:537–545

    Google Scholar 

  • Cheng Z, Presting GG, Buell CR, Wing RA, Jiang J (2001) High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics 157:1749–1757

    Google Scholar 

  • Choo KHA (1998) Why is the centromere so cold? Genome Res 8:81–82

    Google Scholar 

  • Chua PR, Roeder GS (1997) Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11:1786–1800

    Google Scholar 

  • Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. JR Statist Soc 39B:1–38

    Google Scholar 

  • Egel R (1995) The synaptonemal complex and the distribution of meiotic recombination events. Trends Genet 11:206–208

    Google Scholar 

  • Egel-Mitani M, Olson LW, Egel R (1982) Meiosis in Aspergillus nidulans: another example for lacking synaptenomal complexes in the absence of crossover interference. Hereditas 97:179–187

    Google Scholar 

  • Esch E, Weber WE (2002) Investigation of crossover interference in barley (Hordeum vulgare L.) using the coefficient of coincidence. Theor Appl Genet 104:786–796

    Google Scholar 

  • Everitt BS (1987) Introduction to optimization methods and their application in statistics. Chapman & Hall, London

    Google Scholar 

  • Gorlov IP, Gorlova OY (2001) Cost–benefit analysis of recombination and its application for understanding of chiasma interference. J Theor Biol 213:1–8

    Google Scholar 

  • Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2,275 markers using a single F2 population. Genetics 148:479–494

    Google Scholar 

  • Hasenkampf CA (1996) The synaptonemal complex—the chaperone of crossing over. Chromosome Res 4:133–140

    Google Scholar 

  • Hastings PJ (1988) Conversion events in fugi. In: Kucherlapati R, Smith GR (eds) Genetic recombination. American Society for Microbiology, Washington, pp 397–428

    Google Scholar 

  • Kaback DB, Barber D, Mahon J, Lamb J, You J (1999) Chromosome size-dependent control of meiotic reciprocal recombination in Saccharomyces cerevisiae: the role of crossover interference. Genetics 152:1475–1486

    Google Scholar 

  • Kleckner N (1996) Meiosis: how could it work? Proc Natl Acad Sci USA 93:8167–8174

    Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412

    Google Scholar 

  • Liu BH (1998) Statistical genomics: linkage, mapping and QTL analysis. CRC, Boca Raton

    Google Scholar 

  • Muller HJ (1916) The mechanism of crossing over. Am Nat 50:193–221, 284–305, 350–366, 421–434

    Google Scholar 

  • Munz P (1994) An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 137:701–707

    Google Scholar 

  • Novak JE, Ross-Macdonald PB, Roeder GS (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158:1013–1025

    Google Scholar 

  • Olson LW, Edén U, Egel-Mitani M, Egel R (1978) Asynaptic meiosis in fission yeast? Hereditas 89:189–199

    Google Scholar 

  • Peng JH, Korol AB, Fahima T, Röder MS, Ronin YI, Li YC, Nevo E (2000) Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Res 10:1509–1531

    Google Scholar 

  • Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11:2600–2621

    Google Scholar 

  • Snow R (1979) Maximum likelihood estimation of linkage and interference from tetrad data. Genetics 92:291–245

    Google Scholar 

  • Storlazzi A, Xu L, Cao L, Kleckner N (1995) Crossover and noncrossover recombination during meiosis: timing and pathway relationships. Proc Natl Acad Sci USA 92:8512–8516

    Google Scholar 

  • Sym M, Roeder GS (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:283–292

    Google Scholar 

  • Wang S, Wang J, Jiang J, Zhang Q (2000) Mapping of centromeric regions on the molecular linkage map of rice (Oryza sativa L.) using centromere-associated sequences. Mol Gen Genet 263:165–172

    Google Scholar 

  • Weber WE, Wricke G (1994) Genetic markers in plant breeding. Parey Scientific, Berlin

    Google Scholar 

  • Wilcoxon F (1946) Individual comparison of grouped data by ranking methods. J Econ Entomol 39:269–270

    Google Scholar 

  • Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J, Fujii F, Shomura A, Ando T, Kono I, Waki K, Yamamoto K, Yano M, Matsumoto T, Sasaki T (2002) A comprehensive rice transcript map containing 6,591 expressed sequence tag sites. Plant Cell 14:525–535

    Google Scholar 

  • Wu JZ, Mizuno H, Hayashi-Tsugane M, Ito Y, Chiden Y, Fujisawa M, Katagiri S, Saji S, Yoshiki S, Karasawa W, Yoshihara R, Hayashi A, Kobayashi H, Ito K, Hamada M, Okamoto M, Ikeno M, Ichikawa Y, Katayose Y, Yano M, Matsumoto T, Sasaki T (2003) Physical maps and recombination frequency of six rice chromosomes. Plant J 36:720–730

    Google Scholar 

Download references

Acknowledgements

The author thanks W.E. Weber (University of Halle, Germany) for stimulating and fruitful discussions about interference and for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Abteilung Angewandte Genetik, Universität Hannover, Herrenhäuser Straße 2, 30419, Hannover, Germany

    E. Esch

Authors
  1. E. Esch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Esch.

Additional information

Communicated by H.C. Becker

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Esch, E. Estimation of gametic frequencies from F2 populations using the EM algorithm and its application in the analysis of crossover interference in rice. Theor Appl Genet 111, 100–109 (2005). https://doi.org/10.1007/s00122-005-1998-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-005-1998-4

Keywords

Search

Navigation