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The dynamic three-dimensional organization of the diploid yeast genome

ABSTRACT: The budding yeast Saccharomyces cerevisiae is a long-standing model for the three-dimensional organization of eukaryotic genomes1,2, and recent high-throughput chromatin conformation capture (Hi-C)2 methods have allowed systematic and unbiased measurement of this organization. Using polymer modeling, some groups have suggested that yeast genome conformation is simple and dominated by its Rabl-like orientation (anaphase-like polarization)3,4. Others have argued that yeast genome conformation is influenced by homolog pairing in diploids5–7 and environment-induced gene relocalization8–13, but the generality and extent of these phenomena remain unclear14. Here, we perform Hi-C on diverged Saccharomyces hybrid diploids to obtain the first global view of chromosome conformation in diploid budding yeasts. Previous studies of homolog pairing have attempted to control for the Rabl-like orientation14, but genomic analysis combined with polymer modeling reveals underappreciated contributions of the Rabl-like orientation to homolog proximity. After controlling for these features, we observe a residual signature of homolog proximity, particularly in saturated phase. From these same data, we also identify known and unexpected inducible gene repositioning. We observe that GAL1 shifts away from the centromere cluster upon galactose induction, consistent with reports of peripheral relocalization8,15. Surprisingly, under galactose induction and saturated phase, we observe a localized increase in homologous interactions between the HAS1 alleles, mediated by association with nuclear pore complexes. The discovery of this conformational change in such well-studied conditions suggests that our understanding of inducible genome reorganization remains incomplete. Together, these results reveal that the diploid yeast genome displays dynamic and complex 3D organization.

ORGANISM(S): Saccharomyces cerevisiae x Saccharomyces paradoxus Saccharomyces uvarum Saccharomyces cerevisiae Saccharomyces cerevisiae x Saccharomyces uvarum Saccharomyces paradoxus Saccharomyces paradoxus x Saccharomyces uvarum

PROVIDER: GSE88952 | GEO | 2016/12/05

SECONDARY ACCESSION(S): PRJNA349185

REPOSITORIES: GEO

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Project description:Eukaryotic genomes are folded into a hierarchy of three-dimensional structures that impact nuclear functions, including transcription, replication, and repair1-3. Studies in Drosophila and mammals have revealed megabase-sized topologically associated domains (TADs) within chromosomes, which in turn are spatially restricted within the nucleus4-8. However, little is known about local physical constraints that drive higher-order folding of chromosomes. Here we performed Hi-C analysis of the fission yeast Schizosaccharomyces pombe to explore genome organization at high resolution. S. pombe comprises a small genome ideal for examining structural features of chromatin folding, and contains fundamental components present in higher eukaryotes. Large domains of heterochromatin coat centromeres and telomeres and recruit cohesin, a ring-like protein complex that binds sister chromatids and mediates long range looping of interphase chromosomes. Our analyses reveal a highly ordered chromosome organization, consistent with a Rabl configuration, which is dependent on constraints imposed at centromeres and telomeres. We find that local chromatin compaction and cohesin recruitment to centromeres mediated by heterochromatin is required for maintaining global genome territorial restraint. In addition to larger complex domains, we also observed locally interacting regions of chromatin ~50 kilobases long, which organize chromosome arms into structures referred to as “globules”. Globule boundaries are enriched in cohesin and convergent gene orientation. The role of cohesin in maintaining globule domains is independent of its role in sister chromatid cohesion, as globule domains are also a feature of G1 chromosome architecture. Defect in cohesin disrupts globule domains and results in an altered chromosome organization at larger scales, including the loss of chromosome territories. Disruption of globules also affects functional annotation of the genome, leading to impairment of borders between neighboring transcriptional units. Our analyses reveal key features of chromatin organization and folding and show that distinct mechanisms uniquely impact the hierarchy of genome organization to protect genome integrity and to coordinate nuclear functions. Comparison of HiC contact maps under various conditions reveal fundamental principles of genome organization

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The dynamic three-dimensional organization of the diploid yeast genome

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