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 <i>Arabidopsis,</i> 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 <i>Arabidopsis</i> lines with full, incomplete, or abolished synapsis. For <i>zyp1</i> 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 <i>zyp1</i> 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 <i>Arabidopsis</i> and in <i>pch2</i> mutants, which display partial synapsis. Together, our results reveal that regulation of crossover patterning in wild-type <i>Arabidopsis</i> and SC-defective mutants likely acts through the same underlying coarsening mechanism, differing only in the spatial compartments through which the pro-crossover factor diffuses.