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Transcription of the mating-type-regulated lncRNA IRT1 is governed by TORC1 and PKA

View Article: PubMed Central - PubMed

ABSTRACT

Cell fate decisions are controlled by multiple cell-intrinsic and -extrinsic factors. In budding yeast, the decision to enter gametogenesis or sporulation is dictated by nutrient availability and mating type. Recently, we showed that in diploid cells harbouring opposite mating types (MATa and MATα), the protein kinase A (PKA) and target of rapamycin complex I (TORC1) signalling pathways integrate at the promoter of the master regulatory transcription factor IME1 to control sporulation via nutrient availability (Weidberg, et al. 2016). In cells with a single mating type (MATa or MATα), however, IME1 is repressed by transcription through the IME1 promoter of a long non-coding RNA called IRT1, which prevents this cell type from undergoing sporulation. Here, we investigated the role of nutrient signalling in mating-type control of IME1. We find that expression of IRT1, like IME1 itself, depends on nutrient availability and the activities of PKA and TORC1. IRT1 transcription is repressed when nutrients are ample and TORC1 and PKA are active. In contrast, inhibition of PKA and TORC1 is sufficient to recruit Rme1 to the IRT1 promoter and induce IRT1-mediated repression of IME1. Finally, we provide evidence that IRT1 and IME1 are co-repressed by the Tup1–Cyc8 complex when nutrients are ample. Thus, in cells with a single mating-type nutrient availability regulates mating-type repression of IME1 and sporulation. Our results indicate that there is a hierarchy between nutrient and mating-type signals in controlling the decision to enter sporulation.

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Model of nutrient and mating-type control of IME1. Under nutrient-rich conditions, TORC1/PKA repress IME1 and IRT1 via Tup1–Cyc8 in diploid/haploid cells harbouring either both or single mating types (MATa/α, MATa or MATα). During starvation, cells with a single mating type (MATa or MATα) induce IRT1-mediated repression of IME1, whereas MATa/α diploid cells induce IME1 and enter sporulation
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Fig3: Model of nutrient and mating-type control of IME1. Under nutrient-rich conditions, TORC1/PKA repress IME1 and IRT1 via Tup1–Cyc8 in diploid/haploid cells harbouring either both or single mating types (MATa/α, MATa or MATα). During starvation, cells with a single mating type (MATa or MATα) induce IRT1-mediated repression of IME1, whereas MATa/α diploid cells induce IME1 and enter sporulation

Mentions: It has been known for decades that nutrient availability and mating type are key regulators of IME1 and entry into sporulation. How nutrients regulate mating-type control of IME1 was not understood. Here, we show that transcription of the mating-type-regulated lncRNA IRT1 is under the control of the same nutrient sensing pathways (TORC1 and PKA) as IME1. In addition, we provide evidence that IRT1 and IME1 are under control of the same repressor complex, Tup1–Cyc8. These findings have several implications. First, they show that mating-type control of IME1 is not active when nutrients are ample (Fig. 3). In other words, there is a hierarchy, in which nutrient repression is prevalent over mating-type control. Second, co-regulation of IME1 and IRT1 could serve as a fail-safe mechanism for mating-type control of IME1. Indeed, it has been known that mating-type control of sporulation is essential for preventing haploid cells to enter meiosis, which would be lethal as two consecutive cell divisions would attempt the segregation of a haploid genome into four spores. If IRT1 and IME1 were under control of different signalling pathways and different transcriptional repressors, this could have led to a mis-regulation of mating-type control of IME1. Our observation that IME1 and IRT1 expressions are regulated by the same nutrient sensing pathways and by the same transcriptional repressor complex ensures that IRT1 is activated at the same time when the nutrient requirements for IME1 are met and vice versa. Overall, we propose that the hierarchy between nutrient and mating-type signals ensures that diploid, and not haploid, cells induce IME1 and enter sporulation.Fig. 3


Transcription of the mating-type-regulated lncRNA IRT1 is governed by TORC1 and PKA
Model of nutrient and mating-type control of IME1. Under nutrient-rich conditions, TORC1/PKA repress IME1 and IRT1 via Tup1–Cyc8 in diploid/haploid cells harbouring either both or single mating types (MATa/α, MATa or MATα). During starvation, cells with a single mating type (MATa or MATα) induce IRT1-mediated repression of IME1, whereas MATa/α diploid cells induce IME1 and enter sporulation
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Fig3: Model of nutrient and mating-type control of IME1. Under nutrient-rich conditions, TORC1/PKA repress IME1 and IRT1 via Tup1–Cyc8 in diploid/haploid cells harbouring either both or single mating types (MATa/α, MATa or MATα). During starvation, cells with a single mating type (MATa or MATα) induce IRT1-mediated repression of IME1, whereas MATa/α diploid cells induce IME1 and enter sporulation
Mentions: It has been known for decades that nutrient availability and mating type are key regulators of IME1 and entry into sporulation. How nutrients regulate mating-type control of IME1 was not understood. Here, we show that transcription of the mating-type-regulated lncRNA IRT1 is under the control of the same nutrient sensing pathways (TORC1 and PKA) as IME1. In addition, we provide evidence that IRT1 and IME1 are under control of the same repressor complex, Tup1–Cyc8. These findings have several implications. First, they show that mating-type control of IME1 is not active when nutrients are ample (Fig. 3). In other words, there is a hierarchy, in which nutrient repression is prevalent over mating-type control. Second, co-regulation of IME1 and IRT1 could serve as a fail-safe mechanism for mating-type control of IME1. Indeed, it has been known that mating-type control of sporulation is essential for preventing haploid cells to enter meiosis, which would be lethal as two consecutive cell divisions would attempt the segregation of a haploid genome into four spores. If IRT1 and IME1 were under control of different signalling pathways and different transcriptional repressors, this could have led to a mis-regulation of mating-type control of IME1. Our observation that IME1 and IRT1 expressions are regulated by the same nutrient sensing pathways and by the same transcriptional repressor complex ensures that IRT1 is activated at the same time when the nutrient requirements for IME1 are met and vice versa. Overall, we propose that the hierarchy between nutrient and mating-type signals ensures that diploid, and not haploid, cells induce IME1 and enter sporulation.Fig. 3

View Article: PubMed Central - PubMed

ABSTRACT

Cell fate decisions are controlled by multiple cell-intrinsic and -extrinsic factors. In budding yeast, the decision to enter gametogenesis or sporulation is dictated by nutrient availability and mating type. Recently, we showed that in diploid cells harbouring opposite mating types (MATa and MATα), the protein kinase A (PKA) and target of rapamycin complex I (TORC1) signalling pathways integrate at the promoter of the master regulatory transcription factor IME1 to control sporulation via nutrient availability (Weidberg, et al. 2016). In cells with a single mating type (MATa or MATα), however, IME1 is repressed by transcription through the IME1 promoter of a long non-coding RNA called IRT1, which prevents this cell type from undergoing sporulation. Here, we investigated the role of nutrient signalling in mating-type control of IME1. We find that expression of IRT1, like IME1 itself, depends on nutrient availability and the activities of PKA and TORC1. IRT1 transcription is repressed when nutrients are ample and TORC1 and PKA are active. In contrast, inhibition of PKA and TORC1 is sufficient to recruit Rme1 to the IRT1 promoter and induce IRT1-mediated repression of IME1. Finally, we provide evidence that IRT1 and IME1 are co-repressed by the Tup1–Cyc8 complex when nutrients are ample. Thus, in cells with a single mating-type nutrient availability regulates mating-type repression of IME1 and sporulation. Our results indicate that there is a hierarchy between nutrient and mating-type signals in controlling the decision to enter sporulation.

No MeSH data available.


Related in: MedlinePlus