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Stable and dynamic nucleosome states during a meiotic developmental process.

ABSTRACT: The plasticity of chromatin organization as chromosomes undergo a full compendium of transactions including DNA replication, recombination, chromatin compaction, and changes in transcription during a developmental program is unknown. We generated genome-wide maps of individual nucleosome organizational states, including positions and occupancy of all nucleosomes, and H3K9 acetylation and H3K4, K36, K79 tri-methylation, during meiotic spore development (gametogenesis) in Saccharomyces. Nucleosome organization was remarkably constant as the genome underwent compaction. However, during an acute meiotic starvation response, nucleosomes were repositioned to alter the accessibility of select transcriptional start sites. Surprisingly, the majority of the meiotic programs did not use this nucleosome repositioning, but was dominated by antisense control. Histone modification states were also remarkably stable, being abundant at specific nucleosome positions at three-quarters of all genes, despite most genes being rarely transcribed. Our findings suggest that, during meiosis, the basic features of genomic chromatin organization are essentially a fixed property of chromosomes, but tweaked in a restricted and program-specific manner.

SUBMITTER: Zhang L

PROVIDER: S-EPMC3106320 | biostudies-literature | 2011 Jun

REPOSITORIES: biostudies-literature

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Stable and dynamic nucleosome states during a meiotic developmental process.

Zhang Liye L Ma Hong H Pugh B Franklin BF

Genome research 20110422 6

The plasticity of chromatin organization as chromosomes undergo a full compendium of transactions including DNA replication, recombination, chromatin compaction, and changes in transcription during a developmental program is unknown. We generated genome-wide maps of individual nucleosome organizational states, including positions and occupancy of all nucleosomes, and H3K9 acetylation and H3K4, K36, K79 tri-methylation, during meiotic spore development (gametogenesis) in Saccharomyces. Nucleosome ...[more]

PMID: 21515815

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Project description:BACKGROUND: Meiosis is the sexual reproduction process common to eukaryotes. The diploid yeast Saccharomyces cerevisiae undergoes meiosis in sporulation medium to form four haploid spores. Initiation of the process is tightly controlled by intricate networks of positive and negative feedback loops. Intriguingly, expression of early meiotic proteins occurs within a narrow time window. Further, sporulation efficiency is strikingly different for yeast strains with distinct mutations or genetic backgrounds. To investigate signal transduction pathways that regulate transient protein expression and sporulation efficiency, we develop a mathematical model using ordinary differential equations. The model describes early meiotic events, particularly feedback mechanisms at the system level and phosphorylation of signaling molecules for regulating protein activities. RESULTS: The mathematical model is capable of simulating the orderly and transient dynamics of meiotic proteins including Ime1, the master regulator of meiotic initiation, and Ime2, a kinase encoded by an early gene. The model is validated by quantitative sporulation phenotypes of single-gene knockouts. Thus, we can use the model to make novel predictions on the cooperation between proteins in the signaling pathway. Virtual perturbations on feedback loops suggest that both positive and negative feedback loops are required to terminate expression of early meiotic proteins. Bifurcation analyses on feedback loops indicate that multiple feedback loops are coordinated to modulate sporulation efficiency. In particular, positive auto-regulation of Ime2 produces a bistable system with a normal meiotic state and a more efficient meiotic state. CONCLUSIONS: By systematically scanning through feedback loops in the mathematical model, we demonstrate that, in yeast, the decisions to terminate protein expression and to sporulate at different efficiencies stem from feedback signals toward the master regulator Ime1 and the early meiotic protein Ime2. We argue that the architecture of meiotic initiation pathway generates a robust mechanism that assures a rapid and complete transition into meiosis. This type of systems-level regulation is a commonly used mechanism controlling developmental programs in yeast and other organisms. Our mathematical model uncovers key regulations that can be manipulated to enhance sporulation efficiency, an important first step in the development of new strategies for producing gametes with high quality and quantity.

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Stable and dynamic nucleosome states during a meiotic developmental process.

Publications

Stable and dynamic nucleosome states during a meiotic developmental process.

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