Coarsening dynamics can explain meiotic crossover patterning in both the presence and absence of the synaptonemal complex
Abstract
The shuffling of genetic material facilitated by meiotic crossovers is a critical driver of genetic variation. Therefore, the number and positions of crossover events must be carefully controlled. In Arabidopsis, an obligate crossover and repression of nearby crossovers on each chromosome pair are abolished in mutants that lack the synaptonemal complex (SC), a conserved protein scaffold. We use mathematical modelling and quantitative super-resolution microscopy to explore and mechanistically explain meiotic crossover pattering in Arabidopsis lines with full, incomplete or abolished synapsis. For zyp1 mutants, which lack an SC, we develop a coarsening model in which crossover precursors globally compete for a limited pool of the pro-crossover factor HEI10, with dynamic HEI10 exchange mediated through the nucleoplasm. We demonstrate that this model is capable of quantitatively reproducing and predicting zyp1 experimental crossover patterning and HEI10 foci intensity data. Additionally, we find that a model combining both SC- and nucleoplasm-mediated coarsening can explain crossover patterning in wild-type Arabidopsis and in pch2 mutants, which display partial synapsis. Together, our results reveal that regulation of crossover patterning in wild-type Arabidopsis and SC defective mutants likely act through the same underlying coarsening mechanism, differing only in the spatial compartments through which the pro-crossover factor diffuses.
Data availability
Imaging data associated with this study are available at doi.org/10.6084/m9.figshare.19650249.v1, doi.org/10.6084/m9.figshare.19665810.v1 and doi.org/10.6084/m9.figshare.21989732. Custom Python scripts for data analysis are available at https://github.com/jfozard/hei10_zyp1.
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The synaptonemal complex imposes crossover interference and heterochiasmy in ArabidopsisProceedings of the National Academy of Sciences 118:e2023613118.
Article and author information
Author details
Funding
Biotechnology and Biological Sciences Research Council (BB/V005774/1)
- Chris Morgan
Biotechnology and Biological Sciences Research Council (BB/P013511/1)
- Martin Howard
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Fozard 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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