Principles of meiotic chromosome assembly revealed in S. cerevisiae
During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use Saccharomyces cerevisiae to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequenc...
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| Published in: | Nature communications Vol. 10; no. 1; pp. 4795 - 12 |
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| Main Authors: | , , , , |
| Format: | Journal Article |
| Language: | English |
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22.10.2019
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| ISSN: | 2041-1723, 2041-1723 |
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| Abstract | During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use
Saccharomyces cerevisiae
to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in
S. cerevisiae
, suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process.
During meiotic prophase chromosomes organise into a series of chromatin loops, but the mechanisms of assembly remain unclear. Here the authors use
Saccharomyces cerevisiae
to elucidate how this elaborate three-dimensional chromosome organisation is linked to genomic sequence, and demonstrate an essential role for cohesin during this process. |
|---|---|
| AbstractList | During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use
Saccharomyces cerevisiae
to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in
S. cerevisiae
, suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process.
During meiotic prophase chromosomes organise into a series of chromatin loops, but the mechanisms of assembly remain unclear. Here the authors use
Saccharomyces cerevisiae
to elucidate how this elaborate three-dimensional chromosome organisation is linked to genomic sequence, and demonstrate an essential role for cohesin during this process. During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use Saccharomyces cerevisiae to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in S. cerevisiae, suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process. During meiotic prophase chromosomes organise into a series of chromatin loops, but the mechanisms of assembly remain unclear. Here the authors use Saccharomyces cerevisiae to elucidate how this elaborate three-dimensional chromosome organisation is linked to genomic sequence, and demonstrate an essential role for cohesin during this process. During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use Saccharomyces cerevisiae to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in S. cerevisiae , suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process. During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use Saccharomyces cerevisiae to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in S. cerevisiae, suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process. During meiotic prophase chromosomes organise into a series of chromatin loops, but the mechanisms of assembly remain unclear. Here the authors use Saccharomyces cerevisiae to elucidate how this elaborate three-dimensional chromosome organisation is linked to genomic sequence, and demonstrate an essential role for cohesin during this process. During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use Saccharomyces cerevisiae to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in S. cerevisiae, suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process.During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain unclear. Here we use Saccharomyces cerevisiae to explore how this elaborate three-dimensional chromosome organisation is linked to genomic sequence. As cells enter meiosis, we observe that strong cohesin-dependent grid-like Hi-C interaction patterns emerge, reminiscent of mammalian interphase organisation, but with distinct regulation. Meiotic patterns agree with simulations of loop extrusion with growth limited by barriers, in which a heterogeneous population of expanding loops develop along the chromosome. Importantly, CTCF, the factor that imposes similar features in mammalian interphase, is absent in S. cerevisiae, suggesting alternative mechanisms of barrier formation. While grid-like interactions emerge independently of meiotic chromosome synapsis, synapsis itself generates additional compaction that matures differentially according to telomere proximity and chromosome size. Collectively, our results elucidate fundamental principles of chromosome assembly and demonstrate the essential role of cohesin within this evolutionarily conserved process. |
| ArticleNumber | 4795 |
| Author | Pollard, Katherine S. Fudenberg, Geoffrey Baxter, Jonathan Schalbetter, Stephanie A. Neale, Matthew J. |
| Author_xml | – sequence: 1 givenname: Stephanie A. orcidid: 0000-0001-7563-169X surname: Schalbetter fullname: Schalbetter, Stephanie A. email: S.Schalbetter@sussex.ac.uk organization: Genome Damage and Stability Centre, School of Life Sciences, University of Sussex – sequence: 2 givenname: Geoffrey orcidid: 0000-0001-5905-6517 surname: Fudenberg fullname: Fudenberg, Geoffrey email: geoff.fudenberg@gladstone.ucsf.edu organization: Gladstone Institutes for Data Science and Biotechnology – sequence: 3 givenname: Jonathan orcidid: 0000-0002-4455-9717 surname: Baxter fullname: Baxter, Jonathan organization: Genome Damage and Stability Centre, School of Life Sciences, University of Sussex – sequence: 4 givenname: Katherine S. orcidid: 0000-0002-9870-6196 surname: Pollard fullname: Pollard, Katherine S. email: katherine.pollard@gladstone.ucsf.edu organization: Gladstone Institutes for Data Science and Biotechnology, Department of Epidemiology & Biostatistics, Institute for Human Genetics, Quantitative Biology Institute, and Institute for Computational Health Sciences, University of California, Chan-Zuckerberg Biohub – sequence: 5 givenname: Matthew J. orcidid: 0000-0002-6453-1877 surname: Neale fullname: Neale, Matthew J. email: M.Neale@sussex.ac.uk organization: Genome Damage and Stability Centre, School of Life Sciences, University of Sussex |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31641121$$D View this record in MEDLINE/PubMed |
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| PublicationDateYYYYMMDD | 2019-10-22 |
| PublicationDate_xml | – month: 10 year: 2019 text: 2019-10-22 day: 22 |
| PublicationDecade | 2010 |
| PublicationPlace | London |
| PublicationPlace_xml | – name: London – name: England |
| PublicationTitle | Nature communications |
| PublicationTitleAbbrev | Nat Commun |
| PublicationTitleAlternate | Nat Commun |
| PublicationYear | 2019 |
| Publisher | Nature Publishing Group UK Nature Publishing Group Nature Portfolio |
| Publisher_xml | – name: Nature Publishing Group UK – name: Nature Publishing Group – name: Nature Portfolio |
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| Snippet | During meiotic prophase, chromosomes organise into a series of chromatin loops emanating from a proteinaceous axis, but the mechanisms of assembly remain... During meiotic prophase chromosomes organise into a series of chromatin loops, but the mechanisms of assembly remain unclear. Here the authors use... |
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| Title | Principles of meiotic chromosome assembly revealed in S. cerevisiae |
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