Sequestration of mRNAs Modulates the Timing of Translation during Meiosis in Budding Yeast

Abstract

Starvation of diploid cells of the budding yeast Saccharomyces cerevisiae induces them to enter meiosis and differentiate into haploid spores. During meiosis, the precise timing of gene expression is controlled at the level of transcription, and also translation. If cells are returned to rich medium after they have committed to meiosis, the transcript levels of most meiotically upregulated genes decrease rapidly. However, for a subset of transcripts whose translation is delayed until the end of meiosis II, termed protected transcripts, the transcript levels remain stable even after nutrients are reintroduced. The Ime2-Rim4 regulatory circuit controls both the delayed translation and the stability of protected transcripts. These protected mRNAs localize in discrete foci, which are not seen for transcripts of genes with different translational timing and are regulated by Ime2. These results suggest that Ime2 and Rim4 broadly regulate translational delay but that additional factors, such as mRNA localization, modulate this delay to tune the timing of gene expression to developmental transitions during sporulation.

Supplemental material for this article may be found at http://dx.doi.org/10.1128/MCB.00189-15.

ACKNOWLEDGMENTS

We thank Ed Winter (Thomas Jefferson University) for strains and Jeff Gerst (Weizmann Institute) for plasmids. We are grateful to Angelika Amon, Luke Berchowitz, and Nancy Hollingsworth for comments on the manuscript and to Bruce Futcher, Ed Luk, and Wali Karzai for helpful discussions.

This work was supported by P01 GM088297 to R.S. and A.M.N.