RNA-Mediated Regulation of Meiosis in Budding Yeast

Abstract

Cells change their physiological state in response to environmental cues. In the absence of nutrients, unicellular fungi such as budding yeast exit mitotic proliferation and enter the meiotic cycle, leading to the production of haploid cells that are encased within spore walls. These cell state transitions are orchestrated in a developmentally coordinated manner. Execution of the meiotic cell cycle program in budding yeast, Saccharomyces cerevisiae, is regulated by the key transcription factor, Ime1. Recent developments have uncovered the role of non-coding RNA in the regulation of Ime1 and meiosis. In this review, we summarize the role of ncRNA-mediated and RNA homeostasis-based processes in the regulation of meiosis in Saccharomyces cerevisiae.

Keywords: RNA processing; Saccharomyces cerevisiae; cell fate; meiosis; non-coding RNA.

Figure 1

Cell-type-specific control of meiosis via antisense non-coding RNA: Ime4 is an activator of IME1, the master regulator of meiosis. In haploid MATa and MATα cells, an antisense transcript, RME2, is produced from the IME4 locus. RME2 represses the expression of Ime4 by potentially preventing the elongation of the IME4 RNA. Therefore, haploid cells do not progress to meiosis. On the other hand, in heterozygous MATa/MATα diploids, a1 and α2 expressed from the mating-type MATa and MATα locus form the a1-α2 repressor complex. This repressor complex binds to binding sites present downstream of the IME4 locus, thus repressing the antisense transcription. Therefore, in the absence of RME2, the IME4 sense transcript is created and Ime4 is expressed, which can now activate IME1 expression and initiate meiosis.

Figure 2

Repression of IME1 and meiosis by lncRNA IRT1: Rme1 negatively regulates the transcription of IME1, the master regulator of meiosis. Two long non-coding transcripts, IRT1 and IRT2, arising from the promoter of IME1, further modulate the expression of Ime1. In haploid cells, basal-level transcription of IRT2 enhances the binding of Rme1 upstream of IRT1 TSS, which activates the transcription of IRT1. This transcription inhibits the binding of transcription factors, such as Pog1, and also leads to the deposition of repressive chromatin marks. This suppresses the transcription of IME1. Meanwhile, in diploids, the a1-α2 repressor complex from MAT loci inhibits transcription of Rme1. Transcription of IRT1 by any leaky Rme1 is prevented by both a1-α2 repressor binding to Rme1 binding sites in the IME1 promoter and also the transcription of IRT2. In addition, Ime1 protein also activates its own transcription via IRT2. This allows the expression of IME1 and progression into meiosis.