Multiple MAPK Cascades Regulate the Transcription of IME1, the Master Transcriptional Activator of Meiosis in Saccharomyces cerevisiae

Kahana-Edwin, Smadar; Stark, Michal; Kassir, Yona

doi:10.1371/journal.pone.0078920

Cited by 15 publications

(9 citation statements)

References 63 publications

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“…Given that TORC1 and PKA control CLN1-3 expression, it is possible that CLN1-3 partially mediate PKA and TORC1 repression of IME1 [ 52 – 54 ]. PKA is also known to phosphorylate the transcription factors Sok2, Msn2/4, Sko1 and Com2, which directly bind and control the IME1 promoter [ 15 , 42 , 55 ]. Further efforts are needed to identify downstream effectors of PKA and TORC1 that mediate the regulation of IME1 .…”

Section: Discussionmentioning

confidence: 99%

Nutrient Control of Yeast Gametogenesis Is Mediated by TORC1, PKA and Energy Availability

et al. 2016

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Cell fate choices are tightly controlled by the interplay between intrinsic and extrinsic signals, and gene regulatory networks. In Saccharomyces cerevisiae, the decision to enter into gametogenesis or sporulation is dictated by mating type and nutrient availability. These signals regulate the expression of the master regulator of gametogenesis, IME1. Here we describe how nutrients control IME1 expression. We find that protein kinase A (PKA) and target of rapamycin complex I (TORC1) signalling mediate nutrient regulation of IME1 expression. Inhibiting both pathways is sufficient to induce IME1 expression and complete sporulation in nutrient-rich conditions. Our ability to induce sporulation under nutrient rich conditions allowed us to show that respiration and fermentation are interchangeable energy sources for IME1 transcription. Furthermore, we find that TORC1 can both promote and inhibit gametogenesis. Down-regulation of TORC1 is required to activate IME1. However, complete inactivation of TORC1 inhibits IME1 induction, indicating that an intermediate level of TORC1 signalling is required for entry into sporulation. Finally, we show that the transcriptional repressor Tup1 binds and represses the IME1 promoter when nutrients are ample, but is released from the IME1 promoter when both PKA and TORC1 are inhibited. Collectively our data demonstrate that nutrient control of entry into sporulation is mediated by a combination of energy availability, TORC1 and PKA activities that converge on the IME1 promoter.

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Section: Discussionmentioning

confidence: 99%

Nutrient Control of Yeast Gametogenesis Is Mediated by TORC1, PKA and Energy Availability

et al. 2016

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“…Surprisingly, given that this pathway is the principal known regulator of Rlm1, neither a deletion allele of the MAPK that directly phosphorylates/ activates Rlm1, Slt2 (Mpk1), nor a deletion allele of the MEK kinase acting upstream of Slt2, Bck1, resulted in satellite daughters ( Figure 3). Kdx1/Mlp1 kinase may activate Rlm1 independently of Slt2 (Watanabe et al 1997;Kim and Levin 2010;Kahana-Edwin et al 2013), but satellite groups (measured as two or more buds per group) were not seen in either a kdx1D mutant (3 6 0.3%, n = 3) or an slt2D kdx1D double mutant (6 6 0.3%, n = 3). However, images from an earlier study reveal that a particular point-mutation allele of SLT2 (slt2-1), does form satellite groups at high temperature (Mazzoni et al 1993).…”

Section: Involvement Of Upstream Kinases In Satellitegroup Phenotypementioning

confidence: 96%

Shrinking Daughters: Rlm1-Dependent G1/S Checkpoint MaintainsSaccharomyces cerevisiaeDaughter Cell Size and Viability

et al. 2017

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The Rlm1 transcription factor is a target of the cell wall integrity pathway. We report that an Δ mutant grown on a nonfermentable carbon source at low osmolarity forms cell groups in which a mother cell is surrounded by smaller "satellite-daughter" cells. Mother cells in these groups progressed through repeated rounds of cell division with normal rates of bud growth and genetic stability; however, these cells underwent precocious START relative to wild-type mothers. Thus, once activated, Rlm1 delays the transition from G to S, a mechanism we term the cell wall/START (CW/START) checkpoint. The Δ satellite-cell phenotype is suppressed by deletion of either, which encodes the kinase that activates Rlm1, or , which is also activated by Slt2; suggesting that Slt2 can have opposing roles in regulating the START transition. Consistent with an Rlm1-dependent CW/START checkpoint,Δ satellite daughters were unable to grow or divide further even after transfer to rich medium, but UV irradiation in G could partially rescue Δ satellite daughters in the next division. Indeed, after cytokinesis, these satellite daughters shrank rapidly, displayed amorphous actin staining, and became more permeable. As a working hypothesis, we propose that duplication of an "actin-organizing center" in late G may be required both to progress through START and to reestablish the actin cytoskeleton in daughter cells.

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“…As in the case of the 3′-5′ exoribonuclease Rrp6, which is also degraded during meiotic M-phase and required for normal sporulation (Lardenois et al 2015), it is likely the case that altered levels of proteins important for the transition between mitotic growth and meiotic development are at least partially responsible for the phenotype. For example, we observe that COM2 , a negative regulator of IME1 (Inducer of Meiosis 1), remains transcriptionally active in ume6 / ume6 cells cultured in sporulation medium (Kahana-Edwin et al 2013). We also find that the DNA replication activator CDC6 and the G1 cyclin CLN3 (which promotes entry into the mitotic cell division cycle) fail to be transcriptionally down-regulated prior to entry into meiotic M-phase (Ofir et al 2004; Shi and Tu 2013).…”

Section: Discussionmentioning

confidence: 97%

Global alterations of the transcriptional landscape during yeast growth and development in the absence of Ume6-dependent chromatin modification

et al. 2015

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Chromatin modification enzymes are important regulators of gene expression and some are evolutionarily conserved from yeast to human. Saccharomyces cerevisiae is a major model organism for genome-wide studies that aim at the identification of target genes under the control of conserved epigenetic regulators. Ume6 interacts with the upstream repressor site 1 (URS1) and represses transcription by recruiting both the conserved histone deacetylase Rpd3 (through the co-repressor Sin3) and the chromatin-remodeling factor Isw2. Cells lacking Ume6 are defective in growth, stress response, and meiotic development. RNA profiling studies and in vivo protein-DNA binding assays identified mRNAs or transcript isoforms that are directly repressed by Ume6 in mitosis. However, a comprehensive understanding of the transcriptional alterations, which underlie the complex ume6Δ mutant phenotype during fermentation, respiration, or sporulation, is lacking. We report the protein-coding transcriptome of a diploid MATa/α wild-type and ume6/ume6 mutant strains cultured in rich media with glucose or acetate as a carbon source, or sporulation-inducing medium. We distinguished direct from indirect effects on mRNA levels by combining GeneChip data with URS1 motif predictions and published high-throughput in vivo Ume6-DNA binding data. To gain insight into the molecular interactions between successive waves of Ume6-dependent meiotic genes, we integrated expression data with information on protein networks. Our work identifies novel Ume6 repressed genes during growth and development and reveals a strong effect of the carbon source on the derepression pattern of transcripts in growing and developmentally arrested ume6/ume6 mutant cells. Since yeast is a useful model organism for chromatin-mediated effects on gene expression, our results provide a rich source for further genetic and molecular biological work on the regulation of cell growth and cell differentiation in eukaryotes.

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Multiple MAPK Cascades Regulate the Transcription of IME1, the Master Transcriptional Activator of Meiosis in Saccharomyces cerevisiae

Cited by 15 publications

References 63 publications

Nutrient Control of Yeast Gametogenesis Is Mediated by TORC1, PKA and Energy Availability

Nutrient Control of Yeast Gametogenesis Is Mediated by TORC1, PKA and Energy Availability

Shrinking Daughters: Rlm1-Dependent G1/S Checkpoint MaintainsSaccharomyces cerevisiaeDaughter Cell Size and Viability

Global alterations of the transcriptional landscape during yeast growth and development in the absence of Ume6-dependent chromatin modification

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