Homolog synapsis is required for proper meiotic chromosome segregation but how synapsis is initiated to stabilize pairing between homologous chromosomes is poorly understood. In C. elegans, synapsis and a meiotic checkpoint that monitors synapsis depend on Pairing Centers, cis-acting loci that interact with nuclear envelope proteins, such as SUN-1, to access cytoplasmic microtubules. We report that synapsis is negatively regulated by spindle assembly checkpoint components. Specifically, we demonstrate that mutations in mdf-1, mdf-2 and bub-3 suppress synapsis defects of dynein mutants. In addition, we show that these proteins are required for the synapsis checkpoint. Consistent with a role at Pairing Centers, MDF-1 and MDF-2 interact with SUN-1 and localize to the periphery of meiotic nuclei. Furthermore, the requirement for spindle assembly checkpoint proteins in regulating synapsis relies on all chromosomes having functional Pairing Centers. We propose that spindle assembly checkpoint proteins monitor the stability of pairing, or tension, between homologous chromosomes to regulate synapsis and elicit a checkpoint response. Our studies uncover an unexpected link between mechanisms that ensure genomic integrity during mitosis and meiotic prophase.
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