The conserved ATPase PCH-2 controls the number and distribution of crossovers by antagonizing crossover formation in C. elegans.

Meiotic crossover recombination is essential for both accurate chromosome segregation and the generation of new haplotypes for natural selection to act upon. While the conserved role of the ATPase, PCH-2, during meiotic prophase has been enigmatic, a universal phenotype that is observed when pch-2 or its orthologs are mutated is a change in the number and distribution of meiotic crossovers. Here, we show that PCH-2 controls the number and distribution of crossovers by antagonizing crossover formation. This antagonism produces different effects at different stages of meiotic prophase: early in meiotic prophase, PCH-2 prevents double strand breaks from becoming crossovers, limiting crossovers at sites of initial DSB formation and homolog interactions. Later in meiotic prophase, PCH-2 winnows the number of crossover-eligible intermediates, contributing to the reinforcement of crossover-eligible intermediates, designation of crossovers and ultimately, crossover assurance. We also demonstrate that PCH-2 accomplishes this regulation through the meiotic HORMAD, HIM-3. Our data strongly support a model in which PCH-2's conserved role is to remodel meiotic HORMADs throughout meiotic prophase to destabilize crossover-eligible precursors, coordinate meiotic recombination with synapsis, and contribute to the progressive implementation of meiotic recombination, guaranteeing crossover control.

Chromosomal fusions, but not chromosomal inversions, activate a PCH-2 dependent checkpoint that promotes crossover formation in C. elegans.

Meiotic crossovers promote accurate chromosome segregation during gametogenesis. In C. elegans , a highly conserved AAA ATPase, PCH-2, ensures that homologous chromosomes have at least one crossover, preventing meiotic defects. PCH-2 localizes to meiotic chromosomes and this localization is extended when there are defects in meiotic recombination, suggesting a role in responding to defects. Here, we show that, unlike in other systems, PCH-2 does not persist on meiotic chromosomes when there are chromosomal inversions but does persist when there are whole chromosome fusions. Moreover, this persistence correlates with an increase in crossovers, demonstrating that PCH-2's localization to chromosomes promotes crossover formation.