Transcriptional regulation of meiosis in budding yeast

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Abstract Initiation of meiosis in Saccharomyces cerevisiae is regulated by mating type and nutritional conditions that restrict meiosis to diploid cells grown under starvation conditions. Specifically, meiosis occurs in MATa/MATα cells shifted to nitrogen depletion media in the absence of glucose and the presence of a non-fermentable carbon source. These conditions lead to the expression and activation of Ime1, the master regulator of meiosis. IME1 encodes a transcriptional activator recruited to promoters of early meiosis-specific genes by association with the DNA binding protein, Ume6. Under vegetative growth conditions these genes are silent due to recruitment of the Sin3/Rpd3 histone deacetylase and Isw2 chromatin remodeling complexes by Ume6. Transcription of these meiotic genes occurs following histone acetylation by Gcn5. Expression of the early genes promote entry into the meiotic cycle, since they include genes required for premeiotic DNA synthesis, synapsis of homologous chromosomes, and meiotic recombination. Two of the early meiosis specific genes, a transcriptional activator, Ndt80, and a CDK2 homolog, Ime2, are required for the transcription of middle meiosis-specific genes that are involved with nuclear division and spore formation. Spore maturation depends on late genes whose expression is indirectly dependent on Ime1, Ime2 and Ndt80. Finally, phosphorylation of Ime1 by Ime2, leads to its degradation, and consequently to shutting down of the meiotic transcriptional cascade. This Review is focusing on the regulation of gene expression governing initiation and progression through meiosis. Key Word: meiosis, Saccharomyces cerevisiae, transcriptional repression and silencing, transcriptional activation, glucose, nitrogen, signal transduction pathways. List of abbreviations: ad – activation domain; bd- DNA binding domain; CDK – cyclin dependent kinase; EMG – early meiosis-specific genes; id – interaction domain; LMG – late meiosis-specific genes; MMG – middle meiosis-specific genes; MSE - middle sporulation element; MAPK – Mitogen activated kinase; NIS – Nuclear import sequence; NLS - Nuclear localization sequence; PKA – cAMP-dependent protein kinase H; SA – synthetic growth media with acetate as the sole carbon source; SCB - Swi4/6 cell cycle box; SD – synthetic growth media with glucose as the sole carbon source; SPM – sporulation media; STRE-stress response element; UAS - Upstream activation sequence; UCS - Upstream controlling sequence; URS - Upstream repression sequence. 3
I. Introduction The budding yeast Saccharomyces cerevisiae is a simple unicellular eukaryote exhibiting several optional developmental pathways. Fig. 1 schematically illustrates the developmental options of MATa/MATα diploid cells. In the presence of both carbon and nitrogen sources both haploid and diploid cells adopt the yeast form morphology; upon nitrogen limitation, and in the presence of high levels of glucose, a dimorphic transition to a filamentous growth takes places [For recent reviews see (Gancedo, 2001; Lengeler et al., 2000; Pan et al., 2000)]. Haploid as well as diploid cells manifesting these forms propagate by the mitotic cell cycle. Upon nitrogen depletion the developmental decision made by the cells depends on the presence or absence of a fermentable carbon source such as glucose, as well as on the information at the MAT locus. In the presence of functional MATa1 and MATα2 alleles, regardless of ploidy, i.e. MATa/MATα diploids, MATa/MATα disomic cells, and haploid cells expressing both MAT alleles, cells enter the meiotic cycle (Kassir and Simchen, 1976; Kassir and Simchen, 1985; Rine and Herskowitz, 1987; Roman and Sands, 1953; Roth and Fogel, 1971). In the presence of only a single functional allele, i.e. MATa and MATα haploids or MATa/MATa and MATα/MATα diploids, depletion of nitrogen leads to a cell cycle arrest at G1 (Kassir and Simchen, 1976; Roman and Sands, 1953; Strathern et al., 1981). The last developmental option S. cerevisiae cells possess is that of mating, cells carrying only one of the two MAT alleles can respond to the pheromone secreted by cells expressing the other MAT allele by temporal arrest in G1, mate, and then resume cell growth [reviews on the mating process as well as on how the MAT alleles control cell type are (Fields, 1990; Herskowitz, 1995; Sprague, 1991)]. In this review we focus on how the meiotic signals, namely, the presence of the MATa and MATα alleles, the presence of a non-fermentable carbon source, the absence of glucose and nitrogen, control initiation and progression through the meiotic cycle. We focus on transcriptional regulation rather than the function of the proteins involved with the specific meiotic events [for reviews on these aspects of meiosis see (Kupiec et al., 1997; Roeder, 1997)]. II. Transcriptional cascade governs initiation of meiosis. Entry and progression through the meiotic cycle depends on the expression and activity of many genes that can be roughly divided into 3 groups: meiosis-specific, cell-division cycle (CDC) and radiation sensitive (RAD) genes. The meiosis-specific genes are expressed only under meiotic conditions, and their function is required only in meiosis. The cell-division cycle genes that are 4
Page 1 and 2: Transcriptional regulation of meios
Page 3: 3. Proteins required for the associ
Page 7 and 8: et al., 2000). On the other hand, i
Page 9 and 10: the UCS4 element upstream of the CY
Page 11 and 12: egulator of Cyr1, CDC25 encodes the
Page 13 and 14: 1998). Furthermore, unlike IREu, IR
Page 15 and 16: In the absence of glucose Sok2 does
Page 17 and 18: autophosphorylation, including on a
Page 19 and 20: hours in SPM, followed by a decline
Page 21 and 22: 4. The SIN3, UME6, and RPD3 genes.
Page 23 and 24: 1993). Nevertheless, when Ime1 is t
Page 25 and 26: However, direct demonstration of ph
Page 27 and 28: 3. Proteins required for the associ
Page 29 and 30: heterologous promoter does not supp
Page 31 and 32: expressed only in the absence of gl
Page 33 and 34: structure of hCDK2 reveals that cyc
Page 35 and 36: terminal non-essential domain (Komi
Page 37 and 38: is dependent on Ime2, but in cells
Page 39 and 40: VI. Transcriptional regulation of l
Page 41 and 42: The transcriptional activator that
Page 43 and 44: Functional interaction between Ime1
Page 45 and 46: Bowdish, K. S., and Mitchell, A. P.
Page 47 and 48: Foiani, M., Nadjar-Boger, E., Capon
Page 49 and 50: Jeffrey, P. D., Russo, A. A., Polya
Page 51 and 52: Lindgren, A., Bungard, D., Pierce,
Page 53 and 54: Pazin, M. J., and Kadonaga, J. T. (
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Shenhar, G. (2001). TRANSCRIPTIONAL
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Szent-Gyorgyi, C. (1995). A biparti
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Yoshida, M., Kawaguchi, H., Sakata,
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Fig. 4. The function of positive an
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Fig. 9. A schematic structure of IM
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activation by Ime2 is due to phosph
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MCK1 Protein kinase required for ef
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UME3 A cyclin C homolog that associ
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