Signal pathway integration in the switch from the mitotic cell cycle to meiosis in yeast

Honigberg, Saul M.; Purnapatre, Kedar

doi:10.1242/jcs.00460

Cited by 131 publications

(144 citation statements)

References 135 publications

(122 reference statements)

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“…Pseudohyphal growth is a form of diploid mitotic growth that is characterized by unipolar budding, cell elongation, increased adhesion, and invasive growth (30). The signals that induce pseudohyphal growth and sporulation partially overlap; nitrogen starvation and a brief G1 arrest are necessary to induce either pathway (31,32). However, fermentable carbon sources, like glucose, inhibit sporulation (29) whereas pseudohyphal growth is robust in the presence of glucose (although perhaps even stronger in the presence of sucrose) (33).…”

Section: Resultsmentioning

confidence: 99%

Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae

Magwene

Kayıkçı

Granek

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

158

179

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We carried out a population genomic survey of Saccharomyces cerevisiae diploid isolates and find that many budding yeast strains have high levels of genomic heterozygosity, much of which is likely due to outcrossing. We demonstrate that variation in heterozygosity among strains is correlated with a life-history tradeoff that involves how readily yeast switch from asexual to sexual reproduction under nutrient stress. This trade-off is reflected in a negative relationship between sporulation efficiency and pseudohyphal development and correlates with variation in the expression of RME1, a transcription factor with pleiotropic effects on meiosis and filamentous growth. Selection for alternate lifehistory strategies in natural versus human-associated environments likely contributes to differential maintenance of genomic heterozygosity through its effect on the frequency that yeast lineages experience sexual cycles and hence the opportunity for inbreeding. In addition to elevated levels of heterozygosity, many strains exhibit large genomic regions of loss-of-heterozygosity (LOH), suggesting that mitotic recombination has a significant impact on genetic variation in this species. This study provides new insights into the roles that both outcrossing and mitotic recombination play in shaping the genome architecture of Saccharomyces cerevisiae. This study also provides a unique case where stark differences in the genomic distribution of genetic variation among individuals of the same species can be largely explained by a lifehistory trade-off.T he frequency of sex and the nature of breeding systems have a profound effect on genome variation and evolution. For example, inbred populations have an increased frequency of homozygous genotypes (1), lower effective rates of recombination (2), and smaller effective population sizes relative to outcrossed populations with the same number of individuals (3). Likewise, clonal populations are expected to exhibit high levels of heterozygosity coupled with increased allelic diversity but decreased genotypic diversity relative to sexual populations (4).The budding yeast Saccharomyces cerevisiae is one of the best studied model organisms, but relatively little is known about the importance of sexual versus asexual reproduction and inbreeding versus outcrossing in shaping genome evolution in this species. One recent study estimated that outcrossing occurs approximately once every 50,000 generations in S. cerevisiae (5), but low rates of outcrossing do not preclude the possibility that outcrossing has an important impact on genetic variation. Studies of the closely related yeast Saccharomyces paradoxus suggest that sexual cycles are rare relative to asexual cycles and that when sex does occur it primarily involves inbreeding (6, 7). However, S. paradoxus exhibits distinctly different intra-and interpopulation patterns of variation than does S. cerevisiae (8), and hence these findings may not be generalizable across the Saccharomyces genus.Patterns of heterozygosity are an important indica...

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Section: Resultsmentioning

confidence: 99%

Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae

Magwene

Kayıkçı

Granek

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

158

179

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“…In budding yeast, nutrient deprivation causes cell cycle arrest and entry into meiosis in the G1 phase (Honigberg and Purnapatre, 2003), while in the mouse fetal ovary, loss of the meiosis promoting gene Stra8 leads to germ cells arrested with a 2n DNA content (Baltus et al, 2006). These and other results suggest that the decision to enter meiosis may generally occur prior to meiotic S phase.…”

Section: Research Articlementioning

confidence: 86%

“…In budding yeast, nutrient deprivation causes G1 cell cycle arrest and meiotic initiation (Honigberg and Purnapatre, 2003;Wittenberg and La Valle, 2003). Cell cycle regulators appear to play an important role in this switch, keeping the mitotic cell cycle and meiotic initiation mutually exclusive (Colomina et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline

et al. 2011

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SUMMARYThe C. elegans germline provides an excellent model for analyzing the regulation of stem cell activity and the decision to differentiate and undergo meiotic development. The distal end of the adult hermaphrodite germline contains the proliferative zone, which includes a population of mitotically cycling cells and cells in meiotic S phase, followed by entry into meiotic prophase. The proliferative fate is specified by somatic distal tip cell (DTC) niche-germline GLP-1 Notch signaling through repression of the redundant GLD-1 and GLD-2 pathways that promote entry into meiosis. Here, we describe characteristics of the proliferative zone, including cell cycle kinetics and population dynamics, as well as the role of specific cell cycle factors in both cell cycle progression and the decision between the proliferative and meiotic cell fate. Mitotic cell cycle progression occurs rapidly, continuously, with little or no time spent in G1, and with cyclin E (CYE-1) levels and activity high throughout the cell cycle. In addition to driving mitotic cell cycle progression, CYE-1 and CDK-2 also play an important role in proliferative fate specification. Genetic analysis indicates that CYE-1/CDK-2 promotes the proliferative fate downstream or in parallel to the GLD-1 and GLD-2 pathways, and is important under conditions of reduced GLP-1 signaling, possibly corresponding to mitotically cycling proliferative zone cells that are displaced from the DTC niche. Furthermore, we find that GLP-1 signaling regulates a third pathway, in addition to the GLD-1 and GLD-2 pathways and also independent of CYE-1/CDK-2, to promote the proliferative fate/inhibit meiotic entry.

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“…The overproduction of IME1 in stationary-phase cells can induce meiotic recombination and SC formation, but glucose can stall further progression in late prophase, suggesting that nutritional signals can control later steps in the program through an IME1-independent pathway (Lee and Honigberg 1996). 1 The multiple nutrient-sensing pathways that control induction and progression of sporulation form an interconnected signaling network that includes the nitrogensensing (Tor2), glucose repression, glucose induction, alkaline-sensing (Rim101), and Ras/cAMP pathways (reviewed in Honigberg and Purnapatre 2003). The Ras/cAMP pathway plays a prominent role in this regulatory network.…”

mentioning

confidence: 99%

The Ras/cAMP Pathway and the CDK-Like Kinase Ime2 Regulate the MAPK Smk1 and Spore Morphogenesis in Saccharomyces cerevisiae

et al. 2009

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Meiotic development (sporulation) in the yeast Saccharomyces cerevisiae is induced by nutritional deprivation. Smk1 is a meiosis-specific MAP kinase homolog that controls spore morphogenesis after the meiotic divisions have taken place. In this study, recessive mutants that suppress the sporulation defect of a smk1-2 temperature-sensitive hypomorph were isolated. The suppressors are partial function alleles of CDC25 and CYR1, which encode the Ras GDP/GTP exchange factor and adenyl cyclase, respectively, and MDS3, which encodes a kelch-domain protein previously implicated in Ras/cAMP signaling. Deletion of PMD1, which encodes a Mds3 paralog, also suppressed the smk1-2 phenotype, and a mds3-D pmd1-D double mutant was a more potent suppressor than either single mutant. The mds3-D, pmd1-D, and mds3-D pmd1-D mutants also exhibited mitotic Ras/cAMP phenotypes in the same rank order. The effect of Ras/cAMP pathway mutations on the smk1-2 phenotype required the presence of low levels of glucose. Ime2 is a meiosis-specific CDK-like kinase that is inhibited by low levels of glucose via its carboxy-terminal regulatory domain. IME2-DC241, which removes the carboxy-terminal domain of Ime2, exacerbated the smk1-2 spore formation phenotype and prevented cyr1 mutations from suppressing smk1-2. Inhibition of Ime2 in meiotic cells shortly after Smk1 is expressed revealed that Ime2 promotes phosphorylation of Smk1's activation loop. These findings demonstrate that nutrients can negatively regulate Smk1 through the Ras/cAMP pathway and that Ime2 is a key activator of Smk1 signaling.

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Signal pathway integration in the switch from the mitotic cell cycle to meiosis in yeast

Cited by 131 publications

References 135 publications

Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae

Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae

Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline

The Ras/cAMP Pathway and the CDK-Like Kinase Ime2 Regulate the MAPK Smk1 and Spore Morphogenesis in Saccharomyces cerevisiae

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