Rewiring of the phosphoproteome executes two meiotic divisions

Abstract

The cell cycle is ordered by a controlled network of kinases and phosphatases. To generate gametes via meiosis, two distinct and sequential chromosome segregation events occur without an intervening S phase. How canonical cell cycle controls are modified for meiosis is not well understood. Here, using highly synchronous budding yeast populations, we reveal how the global proteome and phosphoproteome changes during the meiotic divisions. While protein abundance changes are limited to key cell cycle regulators, dynamic phosphorylation changes are pervasive. Our data indicate that two waves of cyclin-dependent kinase and Polo (Cdc5Polo) kinase activity drive successive meiotic divisions. These two distinct waves of phosphorylation are ensured by the meiosis-specific Spo13Meikin protein, which rewires the phosphoproteome. Spo13Meikin binds to Cdc5Polo to promote phosphorylation of a subset of substrates in meiosis I containing a newly identified motif, which we define as the Spo13Meikin -Cdc5Polo consensus phosphorylation motif. Overall, our findings reveal that a master regulator of meiosis redirects the activity of a kinase to change the phosphorylation landscape and elicit a developmental cascade.