Centromere Pairing in Prophase Allows Partner Chromosomes to Orient on the Meiosis I Spindle

Abstract

Proper chromosome segregation in meiosis I relies on the formation of connections between homologous chromosomes. Crossovers between homologs provide a connection that allows them to attach correctly to the meiosis I spindle. Tension is transmitted across the crossover when the partners attach to microtubules from opposing poles of the spindle. Tension stabilizes microtubule attachments that will pull the partners towards opposite poles at anaphase1,2. Paradoxically, in many organisms, non-crossover partners segregate correctly3. The mechanism by which non-crossover partners become bi-oriented on the meiotic spindle is unknown. Both crossover and noncrossover partners pair their centromeres in early in meiosis (prophase). In budding yeast, centromere pairing, is correlated with subsequent correct segregation of the partners4,5. The mechanism by which centromere pairing, in prophase, promotes later correct attachment of the partners to the metaphase spindle is unknown. We used live cell imaging to track the bi-orientation process of non-crossover chromosomes. We find that centromere pairing allows the establishment of connections between the partners that allows their later interdependent attachment to the meiotic spindle using tensionsensing bi-orientation machinery. Because all chromosome pairs experience centromere pairing, our findings suggest that crossover chromosomes also utilize this mechanism to achieve maximal segregation fidelity.