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MSH2 stimulates interfering and inhibits non-interfering crossovers in response to genetic polymorphism

Author

Listed:
  • Julia Dluzewska

    (Adam Mickiewicz University)

  • Wojciech Dziegielewski

    (Adam Mickiewicz University)

  • Maja Szymanska-Lejman

    (Adam Mickiewicz University)

  • Monika Gazecka

    (Adam Mickiewicz University
    Polish Academy of Sciences)

  • Ian R. Henderson

    (University of Cambridge)

  • James D. Higgins

    (University of Leicester)

  • Piotr A. Ziolkowski

    (Adam Mickiewicz University)

Abstract

Meiotic crossovers can be formed through the interfering pathway, in which one crossover prevents another from forming nearby, or by an independent non-interfering pathway. In Arabidopsis, local sequence polymorphism between homologs can stimulate interfering crossovers in a MSH2-dependent manner. To understand how MSH2 regulates crossovers formed by the two pathways, we combined Arabidopsis mutants that elevate non-interfering crossovers with msh2 mutants. We demonstrate that MSH2 blocks non-interfering crossovers at polymorphic loci, which is the opposite effect to interfering crossovers. We also observe MSH2-independent crossover inhibition at highly polymorphic sites. We measure recombination along the chromosome arms in lines differing in patterns of heterozygosity and observe a MSH2-dependent crossover increase at the boundaries between heterozygous and homozygous regions. Here, we show that MSH2 is a master regulator of meiotic DSB repair in Arabidopsis, with antagonistic effects on interfering and non-interfering crossovers, which shapes the crossover landscape in relation to interhomolog polymorphism.

Suggested Citation

  • Julia Dluzewska & Wojciech Dziegielewski & Maja Szymanska-Lejman & Monika Gazecka & Ian R. Henderson & James D. Higgins & Piotr A. Ziolkowski, 2023. "MSH2 stimulates interfering and inhibits non-interfering crossovers in response to genetic polymorphism," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42511-z
    DOI: 10.1038/s41467-023-42511-z
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    References listed on IDEAS

    as
    1. Stéphanie Durand & Qichao Lian & Juli Jing & Marcel Ernst & Mathilde Grelon & David Zwicker & Raphael Mercier, 2022. "Joint control of meiotic crossover patterning by the synaptonemal complex and HEI10 dosage," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Tomasz Bieluszewski & Weronika Sura & Wojciech Dziegielewski & Anna Bieluszewska & Catherine Lachance & Michał Kabza & Maja Szymanska-Lejman & Mateusz Abram & Piotr Wlodzimierz & Nancy Winne & Geert J, 2022. "NuA4 and H2A.Z control environmental responses and autotrophic growth in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    3. Qichao Lian & Victor Solier & Birgit Walkemeier & Stéphanie Durand & Bruno Huettel & Korbinian Schneeberger & Raphael Mercier, 2022. "The megabase-scale crossover landscape is largely independent of sequence divergence," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Chris Morgan & John A. Fozard & Matthew Hartley & Ian R. Henderson & Kirsten Bomblies & Martin Howard, 2021. "Diffusion-mediated HEI10 coarsening can explain meiotic crossover positioning in Arabidopsis," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Penny M. A. Kianian & Minghui Wang & Kristin Simons & Farhad Ghavami & Yan He & Stefanie Dukowic-Schulze & Anitha Sundararajan & Qi Sun & Jaroslaw Pillardy & Joann Mudge & Changbin Chen & Shahryar F. , 2018. "High-resolution crossover mapping reveals similarities and differences of male and female recombination in maize," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    6. Stuart D. Desjardins & James Simmonds & Inna Guterman & Kostya Kanyuka & Amanda J. Burridge & Andrew J. Tock & Eugenio Sanchez-Moran & F. Chris H. Franklin & Ian R. Henderson & Keith J. Edwards & Cris, 2022. "FANCM promotes class I interfering crossovers and suppresses class II non-interfering crossovers in wheat meiosis," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Maja Szymanska-Lejman & Wojciech Dziegielewski & Julia Dluzewska & Nadia Kbiri & Anna Bieluszewska & R. Scott Poethig & Piotr A. Ziolkowski, 2023. "The effect of DNA polymorphisms and natural variation on crossover hotspot activity in Arabidopsis hybrids," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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