RNA Structure Coordinates Translation Across the Meiotic Program

mRNA structure is a key determinant of translation efficiency for individual transcripts, yet its role in coordinating complex physiological processes remains elusive. We profiled mRNA structures during yeast meiosis, deriving a high-resolution structurome covering ~70% of annotated mRNAs, with multi-time-point measurements for 2,084 mRNAs. Transcripts upregulated during meiosis generally have flexible structures that enhance translation. In contrast, complex structures impede translation during meiosis by reducing ribosome flux in coding regions and promoting alternative initiation, including in the highly abundant transcript CCW22. We uncovered a high-low-high oscillation in cytoplasmic RNA helicase levels, which dynamically reprograms cell-wide translational preferences for RNA structure, shaping the temporal translation of hundreds of mRNAs. Disrupting RNA structure in CCW22 or altering Ded1p helicase levels interfered with meiotic proteostasis, hindering meiosis progression. Our study reveals that the concerted action of RNA structure and RNA helicases coordinates cell-wide translation dynamics, highlighting a potent post-transcriptional regulatory layer during meiosis when transcription is limited by chromosome condensation.