Transcription of Two Long Noncoding RNAs Mediates Mating-Type Control of Gametogenesis in Budding Yeast

The cell-fate decision leading to gametogenesis is essential for sexual reproduction. In S. cerevisiae, only diploid MATa/α but not haploid MATa or MATα cells undergo gametogenesis, known as sporulation. We find that transcription of two long noncoding RNAs (lncRNAs) mediates mating-type control of sporulation. In MATa or MATα haploids, expression of IME1, the central inducer of gametogenesis, is inhibited in cis by transcription of the lncRNA IRT1, located in the IME1 promoter. IRT1 transcription recruits the Set2 histone methyltransferase and the Set3 histone deacetylase complex to establish repressive chromatin at the IME1 promoter. Inhibiting expression of IRT1 and an antisense transcript that antagonizes the expression of the meiotic regulator IME4 allows cells expressing the haploid mating type to sporulate with kinetics that are indistinguishable from that of MATa/α diploids. Conversely, expression of the two lncRNAs abolishes sporulation in MATa/α diploids. Thus, transcription of two lncRNAs governs mating-type control of gametogenesis in yeast. [Display omitted] ► The lncRNA IRT1 resides in the promoter of IME1, the key inducer of gametogenesis ► Transcription of IRT1 represses IME1 by establishing a repressive chromatin state ► IME4 is repressed in haploids by an antisense noncoding RNA ► IRT1 and the IME4 antisense transcript act together as key regulators of sporulation Transcription of two noncoding RNAs controls sporulation in yeast. One is a lncRNA transcribed in cis to a critical meiosis gene to generate a repressive chromatin environment; the second is an antisense transcript that blocks transcription of a second meiotic regulator.