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Effects of age on meiosis in budding yeast.

ABSTRACT: In humans, the frequency with which meiotic chromosome mis-segregation occurs increases with age. Whether age-dependent meiotic defects occur in other organisms is unknown. Here, we examine the effects of replicative aging on meiosis in budding yeast. We find that aged mother cells show a decreased ability to initiate the meiotic program and fail to express the meiotic inducer IME1. The few aged mother cells that do enter meiosis complete this developmental program but exhibit defects in meiotic chromosome segregation and spore formation. Furthermore, we find that mutations that extend replicative life span also extend the sexual reproductive life span. Our results indicate that in budding yeast, the ability to initiate and complete the meiotic program as well as the fidelity of meiotic chromosome segregation decrease with cellular age and are controlled by the same pathways that govern aging of asexually reproducing yeast cells.

SUBMITTER: Boselli M

PROVIDER: S-EPMC2948205 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Effects of age on meiosis in budding yeast.

Boselli Monica M Rock Jeremy J Unal Elçin E Levine Stuart S SS Amon Angelika A

Developmental cell 20090601 6

In humans, the frequency with which meiotic chromosome mis-segregation occurs increases with age. Whether age-dependent meiotic defects occur in other organisms is unknown. Here, we examine the effects of replicative aging on meiosis in budding yeast. We find that aged mother cells show a decreased ability to initiate the meiotic program and fail to express the meiotic inducer IME1. The few aged mother cells that do enter meiosis complete this developmental program but exhibit defects in meiotic ...[more]

PMID: 19531355

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Project description:Background Gametes are generated through a specialized cell division called meiosis, in which ploidy is reduced by half because two consecutive rounds of chromosome segregation, meiosis I and meiosis II, occur without intervening DNA replication. This contrasts with the mitotic cell cycle where DNA replication and chromosome segregation alternate to maintain the same ploidy. At the end of mitosis, CDKs are inactivated. This low CDK state in late mitosis/G1 allows for critical preparatory events for DNA replication and centrosome/spindle pole body (SPB) duplication. However, their execution is inhibited until S phase, where further preparatory events are also prevented. This "licensing" ensures that both the chromosomes and the centrosomes/SPBs replicate exactly once per cell cycle, thereby maintaining constant ploidy. Crucially, between meiosis I and meiosis II, centrosomes/SPBs must be re-licensed, but DNA re-replication must be avoided. In budding yeast, the Cdc14 protein phosphatase triggers CDK down regulation to promote exit from mitosis. Cdc14 also regulates the meiosis I to meiosis II transition, though its mode of action has remained unclear. Methods Fluorescence and electron microscopy was combined with proteomics to probe SPB duplication in cells with inactive or hyperactive Cdc14. Results We demonstrate that Cdc14 ensures two successive nuclear divisions by re-licensing SPBs at the meiosis I to meiosis II transition. We show that Cdc14 is asymmetrically enriched on a single SPB during anaphase I and provide evidence that this enrichment promotes SPB re-duplication. Cells with impaired Cdc14 activity fail to promote extension of the SPB half-bridge, the initial step in morphogenesis of a new SPB. Conversely, cells with hyper-active Cdc14 duplicate SPBs, but fail to induce their separation. Conclusion Our findings implicate reversal of key CDK-dependent phosphorylations in the differential licensing of cyclical events at the meiosis I to meiosis I transition.

Project description:Accurate chromosome segregation during meiosis relies on the presence of crossover events distributed among all chromosomes. MutS? and MutL? homologs (Msh4/5 and Mlh1/3) facilitate the formation of a prominent group of meiotic crossovers that mature within the context of an elaborate chromosomal structure called the synaptonemal complex (SC). SC proteins are required for intermediate steps in the formation of MutS?-MutL? crossovers, but whether the assembled SC structure per se is required for MutS?-MutL?-dependent crossover recombination events is unknown. Here we describe an interspecies complementation experiment that reveals that the mature SC is dispensable for the formation of Mlh3-dependent crossovers in budding yeast. Zip1 forms a major structural component of the budding yeast SC, and is also required for MutS? and MutL?-dependent crossover formation. Kluyveromyces lactis ZIP1 expressed in place of Saccharomyces cerevisiae ZIP1 in S. cerevisiae cells fails to support SC assembly (synapsis) but promotes wild-type crossover levels in those nuclei that progress to form spores. While stable, full-length SC does not assemble in S. cerevisiae cells expressing K. lactis ZIP1, aggregates of K. lactis Zip1 displayed by S. cerevisiae meiotic nuclei are decorated with SC-associated proteins, and K. lactis Zip1 promotes the SUMOylation of the SC central element protein Ecm11, suggesting that K. lactis Zip1 functionally interfaces with components of the S. cerevisiae synapsis machinery. Moreover, K. lactis Zip1-mediated crossovers rely on S. cerevisiae synapsis initiation proteins Zip3, Zip4, Spo16, as well as the Mlh3 protein, as do the crossovers mediated by S. cerevisiae Zip1. Surprisingly, however, K. lactis Zip1-mediated crossovers are largely Msh4/Msh5 (MutS?)-independent. This separation-of-function version of Zip1 thus reveals that neither assembled SC nor MutS? is required for Mlh3-dependent crossover formation per se in budding yeast. Our data suggest that features of S. cerevisiae Zip1 or of the assembled SC in S. cerevisiae normally constrain MutL? to preferentially promote resolution of MutS?-associated recombination intermediates.

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Effects of age on meiosis in budding yeast.

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Effects of age on meiosis in budding yeast.

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