Juxtaposition of heterozygosity and homozygosity during meiosis causes reciprocal crossover remodeling via interference

  1. Piotr A Ziolkowski
  2. Luke E Berchowitz
  3. Christophe Lambing
  4. Nataliya E Yelina
  5. Xiaohui Zhao
  6. Krystyna A Kelly
  7. Kyuha Choi
  8. Liliana Ziolkowska
  9. Viviana June
  10. Eugenio Sanchez-Moran
  11. Chris Franklin
  12. Gregory P Copenhaver
  13. Ian R Henderson  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. University of North Carolina at Chapel Hill, United States
  3. University of Birmingham, United Kingdom

Abstract

During meiosis homologous chromosomes undergo crossover recombination. Sequence differences between homologs can locally inhibit crossovers. Despite this nucleotide diversity and population-scaled recombination are positively correlated in eukaryote genomes. To investigate interactions between heterozygosity and recombination we crossed Arabidopsis lines carrying fluorescent crossover reporters to 32 diverse accessions and observed hybrids with significantly higher and lower crossovers than homozygotes. Using recombinant populations derived from these crosses we observed that heterozygous regions increase crossovers when juxtaposed with homozygous regions, which reciprocally decrease. Total crossovers measured by chiasmata were unchanged when heterozygosity was varied, consistent with homeostatic control. We tested the effects of heterozygosity in mutants where the balance of interfering and non-interfering crossover repair is altered. Crossover remodeling at homozygosity-heterozygosity junctions requires interference and non-interfering repair is inefficient in heterozygous regions. As a consequence heterozygous regions show stronger crossover interference. Our findings reveal how varying homolog polymorphism patterns can shape meiotic recombination.

Article and author information

Author details

  1. Piotr A Ziolkowski

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Luke E Berchowitz

    Department of Biology and the Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Christophe Lambing

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Nataliya E Yelina

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Xiaohui Zhao

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Krystyna A Kelly

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Kyuha Choi

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Liliana Ziolkowska

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Viviana June

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Eugenio Sanchez-Moran

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Chris Franklin

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Gregory P Copenhaver

    Department of Biology, Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Ian R Henderson

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    irh25@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: June 17, 2014
  2. Accepted: March 26, 2015
  3. Accepted Manuscript published: March 27, 2015 (version 1)
  4. Version of Record published: April 23, 2015 (version 2)

Copyright

© 2015, Ziolkowski et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Piotr A Ziolkowski
  2. Luke E Berchowitz
  3. Christophe Lambing
  4. Nataliya E Yelina
  5. Xiaohui Zhao
  6. Krystyna A Kelly
  7. Kyuha Choi
  8. Liliana Ziolkowska
  9. Viviana June
  10. Eugenio Sanchez-Moran
  11. Chris Franklin
  12. Gregory P Copenhaver
  13. Ian R Henderson
(2015)
Juxtaposition of heterozygosity and homozygosity during meiosis causes reciprocal crossover remodeling via interference
eLife 4:e03708.
https://doi.org/10.7554/eLife.03708

Share this article

https://doi.org/10.7554/eLife.03708

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