Dependence of inessential late gene expression on early meiotic events in Saccharomyces cerevisiae

Kao, Gautam; Mannix, Daniel G.; Holaway, Brian L.; Finn, Mary C.; Bonny, Andrea E.; Clancy, Mary J.

doi:10.1007/bf00427048

Cited by 28 publications

(25 citation statements)

References 62 publications

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“…We next monitored the ability of the das mutants to undergo premeiotic DNA synthesis and to complete meiosis. Prior studies have shown that premeiotic DNA synthesis is required for expression of meiotic genes (25,31). DNA synthesis was assessed by flow cytometric determination of the relative DNA content of cells that had been stained with propidium iodide.…”

Section: Resultsmentioning

confidence: 99%

NDT80 and the Meiotic Recombination Checkpoint Regulate Expression of Middle Sporulation-Specific Genes in Saccharomyces cerevisiae

Hepworth

Friesen

Segall

1998

Molecular and Cellular Biology

154

251

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Distinct classes of sporulation-specific genes are sequentially expressed during the process of spore formation in Saccharomyces cerevisiae. The transition from expression of early meiotic genes to expression of middle sporulation-specific genes occurs at about the time that cells exit from pachytene and form the meiosis I spindle. To identify genes encoding potential regulators of middle sporulation-specific gene expression, we screened for mutants that expressed early meiotic genes but failed to express middle sporulation-specific genes. We identified mutant alleles of RPD3, SIN3, and NDT80 in this screen. Rpd3p, a histone deacetylase, and Sin3p are global modulators of gene expression. Ndt80p promotes entry into the meiotic divisions. We found that entry into the meiotic divisions was not required for activation of middle sporulation genes; these genes were efficiently expressed in a clb1 clb3 clb4 strain, which fails to enter the meiotic divisions due to reduced Clbdependent activation of Cdc28p kinase. In contrast, middle sporulation genes were not expressed in a dmc1 strain, which fails to enter the meiotic divisions because a defect in meiotic recombination leads to a RAD17-dependent checkpoint arrest. Expression of middle sporulation genes, as well as entry into the meiotic divisions, was restored to a dmc1 strain by mutation of RAD17. Our studies also revealed that NDT80 was a temporally distinct, pre-middle sporulation gene and that its expression was reduced, but not abolished, on mutation of DMC1, RPD3, SIN3, or NDT80 itself. In summary, our data indicate that Ndt80p is required for expression of middle sporulation genes and that the activity of Ndt80p is controlled by the meiotic recombination checkpoint. Thus, middle genes are expressed only on completion of meiotic recombination and subsequent generation of an active form of Ndt80p.Sporulation is a process of cellular differentiation that is initiated in diploid a/␣ cells of the yeast Saccharomyces cerevisiae in response to nitrogen starvation in the presence of a nonfermentable carbon source. As a cell progresses through the events of meiosis and spore wall formation, a coordinated series of genetic and morphological events generates a tetrad of haploid spores within an ascus (reviewed in references 9 and 30). The sporulation program begins when starved cells exit the mitotic cell cycle and undergo premeiotic DNA replication. This is followed by a lengthy prophase in which homologous chromosomes pair, the synaptonemal complex (SC) is elaborated, and a high level of genetic recombination occurs. At pachytene, the penultimate stage of prophase and the last stage at which cells can return to mitotic growth, the chromosomes are fully synapsed, and the spindle pole bodies lie sideby-side in the nuclear envelope. As cells exit from pachytene, the SC disassembles, chiasmata appear, and the spindle pole bodies separate to form the meiosis I spindle. The two meiotic divisions occur in rapid succession, leading first to segregation of homologous chromosome...

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Section: Resultsmentioning

confidence: 99%

NDT80 and the Meiotic Recombination Checkpoint Regulate Expression of Middle Sporulation-Specific Genes in Saccharomyces cerevisiae

Hepworth

Friesen

Segall

1998

Molecular and Cellular Biology

154

251

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“…This recipient matal MATa RES1-1/+ strain forms pale blue colonies on sporulation medium supplemented with X-Gal, because it contains a sporulation-specific reporter construction (spr3::1acZ) integrated at both chromosomal loci. Transformants that sporulated better than the recipient were expected to form darker colonies in accord with the higher levels of f-galactosidase that are produced (17,20,21).…”

Section: Resultsmentioning

confidence: 99%

“…Alternatively, cells were lysed onto nitrocellulose filters and assayed for spr3::lacZ expression (2,36,47 this study (Table 1) were constructed by standard techniques (14,19,37,40,44). Strains carrying the spr3::1acZ reporter were constructed by transplacement as described previously, using pGK11 (20,21). Haploid segregants carrying the RES1-1 mutation were detected by their ability to express the spr3::1acZ fusion at low levels, using a plate assay as described previously (21).…”

Section: Methodsmentioning

confidence: 99%

IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae.

Shah¹,

Clancy²

1992

Mol. Cell. Biol.

126

112

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In the yeast Saccharomyces cerevisiae, sporulation occurs in response to nutritional and genetic signals. The process is initiated when nutrient availability limits mitotic growth, but only in AMTa/MA Ta diploid cells.Under these conditions, the cells express an activator of meiosis (IME1), which is required for the expression of early sporulation-specific genes. We describe a new gene, IME4, whose activity is essential for IME1 transcript accumulation and sporulation. The IME4 transcript was induced in starved A 4Ta/MA Ta diploids but not in other cell types. In addition, excess IME4 promoted sporulation in mat-insufficient cells. Thus, IME4 appears to activate IME1 in response to cell type and nutritional signals. We have also explored the interactions between IME4 and two genes that are known to regulate IMEI expression. Normally, cells that lack complete AMT information cannot sporulate; when such strains lack RME1 activity or contain the semidominant RES]-] mutation, however, they can express IMEI and sporulate to low levels. Our results show that mat-insufficient strains containing rmel::LEU2 or RES]-] bypass mutations still retain AMT control of IME4 expression. Even though IME4 levels remained low, the rmel::LEU2 and RES)-) mutations allowed IME1 accumulation, implying that these mutations do not require IME4 to exert their effects. In accord with this interpretation, the RES1-1 mutation allowed IME1 accumulation in Af4Ta/MATc strains that contain ime4::LEU2 alleles. These strains still sporulated poorly, suggesting that IME4 plays a role in sporulation in addition to promoting IME1 transcript accumulation. IME4 is located between ADES and LYS5 on chromosome VII.Each of the Saccharomyces cerevisiae cell types is capable of a unique set of responses to environmental conditions (reviewed in references 6, 12, 13, 15, and 25.) These responses are governed, ultimately, by the combinations of AMT (mating type) products that are expressed in particular cells. In wild-type diploids, the combination of the AMTa and MAoTa alleles leads to the formation of a specific repressor, the al-a2 heterodimer, that is unique to these cells (8-10, 28, 46). As a result of the interaction of this molecule with its many targets, MATa/M oTa cells do not mate. Instead, diploidMATa/MAT4T cells are able to undergo meiosis and spore formation when nitrogen limitation restricts mitotic growth.Genetic studies have led to the identification of several key molecules that regulate the initiation of sporulation in response to the AMT genotype and the nutritional status of the cells (22,27,31,42,52). Of central importance is an activator of meiosis, the product of the IMEI gene, which is present at high levels only in starved MATa/MATat diploids (11,22,29). IMEI expression leads to the accumulation of a second activator, IME2, and to the activation of additional sporulation-specific genes (29,42,43,52

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“…Cloning and characterization of a large number of the genes identified in these studies have almost invari ably revealed that they are expressed preferentially in sporulating cells (for review, see Mitchell 1994). In con trast, many of the sporulation-specific genes that were identified on the basis of their expression pattern (Clancy et al 1983;Percival-Smith and Segall 1984;Gottlin-Ninfa and Kaback 1986;Law and Segall 1988;Bishop et al 1992;Coe et al 1992) do not appear to have an essential role in the sporulation program (Garber and Segall 1986;Gottlin-Ninfa and Kaback 1986;Percival-Smith and Segall 1986;Law and Segall 1988;Kao et al 1989;Kallal et al 1990;Muthukumar et al 1993). SPSl is one of the few sporulation-specific genes isolated in a differential hybridization screen (Percival-Smith and Segall 1984) that was found to be required for spore for mation (Percival-Smith and Segall 1986).…”

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confidence: 99%

Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation.

Friesen¹,

Lunz²,

Doyle³

et al. 1994

Genes Dev.

116

132

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During spoiulation of Saccharomyces cerevisiae, meiosis is followed by encapsulation of haploid nuclei within multilayered spore walls. Completion of the late events of the sporulation program requires the SPSl gene. This developmentally regulated gene, which is expressed as cells are nearing the end of meiosis, encodes a protein with homology to serine/threonine protein kinases. The catalytic domain of Spsl is 44% identical to the kinase domain of yeast Ste20, a protein involved in the pheromone-induced signal transduction pathway. Cells of a MATa./MATa. spsl/spsl strain arrest after meiosis and fail to activate genes that are normally expressed at a late time of sporulation. The mutant cells do not form refractile spores as assessed by phase-contrast microscopy and do not display the natural fluorescence and ether resistance that is characteristic of mature spores. Examination by electron microscopy reveals, however, that prospore-like compartments form in some of the mutant cells. These immature spores lack the cross-linked surface layer that surrounds wild-type spores and are more variable in size and number than are the spores of wild-type cells. Despite their inability to complete spore formation, spsl-arrested cells are able to resume mitotic growth on transfer to rich medium, generating haploid progeny. Our results suggest that the developmentally regulated Spsl kinase is required for normal progression of transcriptional, biochemical, and morphological events during the later portion of the sporulation program.

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Dependence of inessential late gene expression on early meiotic events in Saccharomyces cerevisiae

Cited by 28 publications

References 62 publications

NDT80 and the Meiotic Recombination Checkpoint Regulate Expression of Middle Sporulation-Specific Genes in Saccharomyces cerevisiae

NDT80 and the Meiotic Recombination Checkpoint Regulate Expression of Middle Sporulation-Specific Genes in Saccharomyces cerevisiae

IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae.

Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation.

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