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Joint control of meiotic crossover patterning by the synaptonemal complex and HEI10 dosage

Author

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  • Stéphanie Durand

    (Max Planck Institute for Plant Breeding Research)

  • Qichao Lian

    (Max Planck Institute for Plant Breeding Research)

  • Juli Jing

    (Max Planck Institute for Plant Breeding Research)

  • Marcel Ernst

    (Max Planck Institute for Dynamics and Self-Organization)

  • Mathilde Grelon

    (Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB))

  • David Zwicker

    (Max Planck Institute for Dynamics and Self-Organization)

  • Raphael Mercier

    (Max Planck Institute for Plant Breeding Research)

Abstract

Meiotic crossovers are limited in number and are prevented from occurring close to each other by crossover interference. In many species, crossover number is subject to sexual dimorphism, and a lower crossover number is associated with shorter chromosome axes lengths. How this patterning is imposed remains poorly understood. Here, we show that overexpression of the Arabidopsis pro-crossover protein HEI10 increases crossovers but maintains some interference and sexual dimorphism. Disrupting the synaptonemal complex by mutating ZYP1 also leads to an increase in crossovers but, in contrast, abolishes interference and disrupts the link between chromosome axis length and crossovers. Crucially, combining HEI10 overexpression and zyp1 mutation leads to a massive and unprecedented increase in crossovers. These observations support and can be predicted by, a recently proposed model in which HEI10 diffusion along the synaptonemal complex drives a coarsening process leading to well-spaced crossover-promoting foci, providing a mechanism for crossover patterning.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33472-w
    DOI: 10.1038/s41467-022-33472-w
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    References listed on IDEAS

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    1. Diana E. Libuda & Satoru Uzawa & Barbara J. Meyer & Anne M. Villeneuve, 2013. "Meiotic chromosome structures constrain and respond to designation of crossover sites," Nature, Nature, vol. 502(7473), pages 703-706, October.
    2. 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.
    3. 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.
    4. Carl Veller & Shunxin Wang & Denise Zickler & Liangran Zhang & Nancy Kleckner, 2022. "Limitations of gamete sequencing for crossover analysis," Nature, Nature, vol. 606(7913), pages 1-3, June.
    5. 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.
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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.
    2. 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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