Two-step regulation of bouquet formation by mating pheromone signaling and Pat1 activity reduction during fission yeast meiosis

Upon meiosis initiation in the fission yeast Schizosaccharomyces pombe, centromeres detach from the spindle pole body (SPB), while telomeres cluster at the SPB, forming the bouquet, which promotes homologous chromosome pairing. Bouquet formation is regulated by mating pheromone signaling and Pat1 kinase, a central regulator of meiosis. Centromere detachment also requires telomere clustering-dependent SPB recruitment of the telomere component Taz1. However, the precise underlying regulatory mechanisms remain unclear. Here, using a haploid cell system that allows synchronous meiosis induction, we show that mating pheromone signaling induces transient bouquet formation, whereas bouquet maintenance additionally requires Pat1 activity reduction, which normally occurs after conjugation. Furthermore, impairment of telomere clustering inhibits centromere detachment regardless of Pat1 activity reduction, whereas SPB-recruited Taz1 restores centromere detachment only when Pat1 activity is reduced. Thus, bouquet formation proceeds in two steps: a transient establishment step dependent on mating pheromone signaling, followed by a maintenance step requiring Pat1 activity reduction and SPB recruitment of Taz1. We propose that this regulation enables rapid cell cycle resumption upon nutrient replenishment in unconjugated cells, while ensuring meiotic commitment in conjugated cells.