Cdc14 spatiotemporally regulates Rim4-mRNA complex assembly and stability during meiosis

In budding yeast, Rim4 sequesters a subset of meiotic transcripts and essentially suppresses their translation until being degraded at the end of meiosis I. We found that Rim4 loads mRNAs in the nucleus as a prerequisite for relocating Rim4 into the cytoplasm, where mRNAs protect Rim4 from autophagy. Nonetheless, the underlying mechanism remains unknown. Using genetic, biochemical, and cell imaging approaches, here, we revealed that phosphorylation states regulate Rim4’s intracellular interactions with mRNAs and the yeast 14-3-3 proteins Bmh1 and Bmh2. Our data showed that Rim4 forms a heterotrimeric complex with Bmh1 and Bmh2 via multiple phosphorylated sites with the consensus of a PKA kinase target. Remarkably, the Bmh1/2-Rim4 complex excludes mRNAs and is resistant to autophagy. We further found that Cdc14, a conserved cell cycle phosphatase, binds to a canonical Cdc14 docking site (PxL) in Rim4’s C-terminal low complexity domain (LCD) to de-phosphorylate Rim4 at multiple sites, resulting in Bmh1/2-Rim4 disassembly. Notably, before meiotic cell divisions, Cdc14 primarily resides in the nucleus, where mRNAs are transcribed. Therefore, Cdc14-triggered Bmh1/2 dissociation facilitates the nuclear Rim4 to target and sequester the nascent mRNAs. In contrast, during the meiotic divisions, Rim4-sequestered mRNAs are released for translation, while Cdc14 mediates Rim4-Bmh1/2 disassembly in the cytoplasm due to its temporary cytoplasmic relocation at the anaphases; subsequently, loss of protection from mRNAs and Bmh1/2 leads to autophagy-mediated Rim4 degradation at this stage. We conclude that phosphorylation states spatiotemporally regulate Rim4’s meiotic interactions, subcellular localization, and stability, regulated by Cdc14.