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The effect of DNA polymorphisms and natural variation on crossover hotspot activity in Arabidopsis hybrids

Author

Listed:
  • Maja Szymanska-Lejman

    (Adam Mickiewicz University)

  • Wojciech Dziegielewski

    (Adam Mickiewicz University)

  • Julia Dluzewska

    (Adam Mickiewicz University)

  • Nadia Kbiri

    (Adam Mickiewicz University)

  • Anna Bieluszewska

    (Adam Mickiewicz University)

  • R. Scott Poethig

    (University of Pennsylvania)

  • Piotr A. Ziolkowski

    (Adam Mickiewicz University)

Abstract

In hybrid organisms, genetically divergent homologous chromosomes pair and recombine during meiosis; however, the effect of specific types of polymorphisms on crossover is poorly understood. Here, to analyze this in Arabidopsis, we develop the seed-typing method that enables the massively parallel fine-mapping of crossovers by sequencing. We show that structural variants, observed in one of the generated intervals, do not change crossover frequency unless they are located directly within crossover hotspots. Both natural and Cas9-induced deletions result in lower hotspot activity but are not compensated by increases in immediately adjacent hotspots. To examine the effect of single nucleotide polymorphisms on crossover formation, we analyze hotspot activity in mismatch detection-deficient msh2 mutants. Surprisingly, polymorphic hotspots show reduced activity in msh2. In lines where only the hotspot-containing interval is heterozygous, crossover numbers increase above those in the inbred (homozygous). We conclude that MSH2 shapes crossover distribution by stimulating hotspot activity at polymorphic regions.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35722-3
    DOI: 10.1038/s41467-022-35722-3
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    References listed on IDEAS

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    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. 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.
    5. Magnus Nordborg & Tina T Hu & Yoko Ishino & Jinal Jhaveri & Christopher Toomajian & Honggang Zheng & Erica Bakker & Peter Calabrese & Jean Gladstone & Rana Goyal & Mattias Jakobsson & Sung Kim & Yuri , 2005. "The Pattern of Polymorphism in Arabidopsis thaliana," PLOS Biology, Public Library of Science, vol. 3(7), pages 1-1, May.
    6. Wen-Biao Jiao & Korbinian Schneeberger, 2020. "Chromosome-level assemblies of multiple Arabidopsis genomes reveal hotspots of rearrangements with altered evolutionary dynamics," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    7. Fatima Smagulova & Ivan V. Gregoretti & Kevin Brick & Pavel Khil & R. Daniel Camerini-Otero & Galina V. Petukhova, 2011. "Genome-wide analysis reveals novel molecular features of mouse recombination hotspots," Nature, Nature, vol. 472(7343), pages 375-378, April.
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    1. 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.

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