Abstract
For the yeast Saccharomyces cerevisiae, nutrient limitation is a key developmental signal causing diploid cells to switch from yeast-form budding to either foraging pseudohyphal (PH) growth or meiosis and sporulation. Prolonged starvation leads to lineage restriction, such that cells exiting meiotic prophase are committed to complete sporulation even if nutrients are restored. Here, we have identified an earlier commitment point in the starvation program. After this point, cells, returned to nutrient-rich medium, entered a form of synchronous PH development that was morphologically and genetically indistinguishable from starvation-induced PH growth. We show that lineage restriction during this time was, in part, dependent on the mRNA methyltransferase activity of Ime4, which played separable roles in meiotic induction and suppression of the PH program. Normal levels of meiotic mRNA methylation required the catalytic domain of Ime4, as well as two meiotic proteins, Mum2 and Slz1, which interacted and co-immunoprecipitated with Ime4. This MIS complex (Mum2, Ime4, and Slz1) functioned in both starvation pathways. Together, our results support the notion that the yeast starvation response is an extended process that progressively restricts cell fate and reveal a broad role of post-transcriptional RNA methylation in these decisions.
Highlights
Upon nutrient limitation, diploid cells of the yeast Saccharomyces cerevisiae can undergo two distinct developmental responses
Cells became committed to meiosis and sporulation
If nutrients were returned at this point, cells synchronously initiated PH foraging growth. We found that both sporulation and PH growth were governed by RNA methylation, and we identified an mRNA–methyltransferase complex comprising Mum2, Ime4, and Slz1 as a central regulator of these developmental trajectories
Summary
Diploid cells of the yeast Saccharomyces cerevisiae can undergo two distinct developmental responses. Reiterated cell division under this PH program forms chains of elongated cells on solid agar, allowing yeast to forage for nutrients [2,3]. Cells engage in meiotic development and sporulation if starved for nitrogen in the presence of a nonfermentable carbon source (e.g., acetate or glycerol). Under this program, the diploid genome is duplicated (2C to 4C) and segregated into four haploid (1C) meiotic products encased in a spore wall. The diploid genome is duplicated (2C to 4C) and segregated into four haploid (1C) meiotic products encased in a spore wall This spore structure protects haploid progeny until favorable nutrient conditions are available
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