During meiosis, paired homologous chromosomes (homologues) become linked via the synaptonemal complex (SC) and crossovers. Crossovers mediate homologue segregation and arise from self-inflicted double-strand breaks (DSBs). Here, we identify functions in homologue juxtaposition and crossing over of the proteasome, the multi-subunit protease that degrades proteins in the nucleus and cytoplasm. Without proteasome function, homologues fail to pair and instead remain associated with non-homologous chromosomes. While dispensable for non-crossover formation, a functional proteasome is required for a coordinated transition that entails SC assembly between longitudinally organized chromosome axes and stable strand exchange of crossover-designated DSBs. Remarkably, proteolytic core and regulatory proteasome particles are recruited to chromosomes by Zip3, the orthologue of mammalian E3 ligase RNF212, and SC protein Zip1 as part of an evolutionarily conserved program.

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Currently favored models for meiotic recombination posit that both noncrossover and crossover recombination are initiated by DNA double strand breaks but form by different mechanisms, noncrossovers by synthesis dependent strand annealing, and crossovers by formation and resolution of double Holliday junctions centered around the break. This dual mechanism hypothesis predicts different hybrid DNA patterns in noncrossover and crossover recombinants. We show that these predictions are not upheld, by mapping with unprecedented resolution, parental strand contributions to recombinants at a model locus. Instead, break repair in both noncrossovers and crossovers involves synthesis-dependent strand annealing, often with multiple rounds of strand invasion. Crossover-specific double Holliday junction formation occurs via processes that involve branch migration as an integral feature and that can be separated from break repair itself. These findings reveal meiotic recombination to be a highly dynamic process and prompt a new view of the relationship between crossover and noncrossover recombination.