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.
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