Dual control of meiotic crossover patterning

Abstract

Most meiotic crossovers (COs), called class I crossovers, are produced by a conserved pathway catalyzed by the ZMM proteins; COs are limited in number, typically to 1–3 per chromosome, and are prevented from occurring close to one other by crossover interference1-3. In many species, CO number is subject to dimorphism between males and females, and a lower CO number is associated with shorter chromosome axes and stronger interference4. How the patterning of COs is imposed, however, remains poorly understood. Here, we show that overexpression of the ZMM protein HEI10 increases COs and reduces crossover interference but maintains sexual dimorphism; shorter axes length in female meiosis is still associated with fewer COs and stronger interference than in male meiocytes. Disrupting the synaptonemal complex (SC) by mutating ZYP1 also leads to an increase in class I COs but, in contrast, abolishes interference and disrupts the link between chromosome axis length and COs, with female and male meiocytes having the same CO frequency despite different axis lengths. Combining HEI10 overexpression and zyp1 mutation leads to a massive increase in class I COs and absence of interference, while axes lengths are still unaffected. These observations support, and can be effectively predicted by, a recently proposed coarsening model5,6 in which HEI10 diffusion is funneled by the central element of the SC before coarsening into large, well-spaced CO-promoting droplets. Given the conservation of the components, this model may account for CO patterning in many eukaryotes.

Why do plants need the ZMM crossover pathway? A snapshot of meiotic recombination from the perspective of interhomolog polymorphism

“…Observations from high-resolution microscopy have led to the recent proposal of a diffusion-mediated coarsening model (Morgan et al 2021;Zhang et al 2021) in which large, evenly spaced HEI10 foci grow at the expense of smaller foci to define the final crossover sites (Morgan et al 2021). This coarsening model has been recently supported by experimental data showing that SC is critical for funneling chromosomal HEI10 distribution (Durand et al 2022) The dose-dependent effects of HEI10 on crossover number suggests the existence of factors that affect HEI10 expression and activity. A heat shock factor binding protein HSBP that regulates crossover number via controlling HEI10 transcription has already been identified (Kim et al 2022), and an additional protein functionally linked to HEI10, HEIP1, that participates in crossover regulation has been recently described in rice (Li et al 2018).…”

“…This regulation is partially SC-dependent: The transverse filament protein is required for Class I crossovers in many species, from budding yeast to mouse, implying that the SC has coevolved with ZMM proteins since the emergence of eukaryotes and that their functional separation is likely a recent development in plants (Pyatnitskaya et al 2019;Capilla-Pérez et al 2021). SC remains crucial for crossover assurance and interference, key factors for the most basic level of crossover regulation (Wang et al 2015a;Capilla-Pérez et al 2021;France et al 2021;Durand et al 2022). Natural variation in a number of SC and chromosome axis genes was shown to be important for plant adaptation by contributing to crossover number control (Yant et al 2013;Wright et al 2014;Dreissig et al 2020).…”