4.8 Article

3D genomics across the tree of life reveals condensin II as a determinant of architecture type

Journal

SCIENCE
Volume 372, Issue 6545, Pages 984-+

Publisher

AMER ASSOC ADVANCEMENT SCIENCE
DOI: 10.1126/science.abe2218

Keywords

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Funding

  1. Boehringer Ingelheim Fonds
  2. ERC CoG [772471]
  3. Dutch Research Council (NWO-Echo)
  4. Dutch Cancer Society (KWF)
  5. NIH Common Fund 4D Nucleome Program [U54DK107965]
  6. ERC StG [637597]
  7. Dutch Cancer Society
  8. NSF [PHY-2019745, CHE-1614101, 1557923, 1548121, 1645219]
  9. Welch Foundation [C-1792, Q-1866]
  10. FAPESP (Sao Paulo State Research Foundation and Higher Education Personnel) [2016/13998-8, 2017/09662-7]
  11. NSF Physics Frontiers Center Award [PHY-2019745]
  12. USDA Agriculture and Food Research Initiative grant [2017-05741]
  13. Behavioral Plasticity Research Institute [NSF DBI-2021795]
  14. NIH Encyclopedia of DNA Elements Mapping Center Award [UM1HG009375]
  15. Illumina, Inc.
  16. IBM
  17. Pawsey Supercomputing Center
  18. University of Western Australia
  19. NIH [1R01NS114491, RO1DK121366, NIH1P41HD071837, R01AG045183, R01AT009050, R01AG062257, DP1DK113644]
  20. Human Frontiers Science Program [RGP0060/2017]
  21. NHGRI [DP2HG010013]
  22. ERC [740041]
  23. Spanish Ministerio de Economia y Competitividad [BFU2016-74961-P]
  24. Unidad de Excelencia Maria de Maeztu [MDM-2016-0687]
  25. MEXT grant [20H05936]
  26. Welch Foundation
  27. European Research Council (ERC) [772471, 740041] Funding Source: European Research Council (ERC)
  28. Grants-in-Aid for Scientific Research [20H05936] Funding Source: KAKEN

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The study identified two types of three-dimensional genome architectures at the chromosome scale in eukaryotes, with one type correlated with the absence of condensin II subunits. Depletion of condensin II in humans results in a genome structure resembling that of fungi or mosquitoes. The research proposes a physical model in which condensin II compacts chromosomes lengthwise during mitosis, influencing the chromosome-scale genome architecture.
We investigated genome folding across the eukaryotic tree of life. We find two types of three-dimensional (3D) genome architectures at the chromosome scale. Each type appears and disappears repeatedly during eukaryotic evolution. The type of genome architecture that an organism exhibits correlates with the absence of condensin II subunits. Moreover, condensin II depletion converts the architecture of the human genome to a state resembling that seen in organisms such as fungi or mosquitoes. In this state, centromeres cluster together at nucleoli, and heterochromatin domains merge. We propose a physical model in which lengthwise compaction of chromosomes by condensin II during mitosis determines chromosome-scale genome architecture, with effects that are retained during the subsequent interphase. This mechanism likely has been conserved since the last common ancestor of all eukaryotes.

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