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

Claire Hoencamp, Olga Dudchenko, Ahmed M.O. Elbatsh, Sumitabha Brahmachari, Jonne A. Raaijmakers, Tom van Schaik, Ángela Sedeño Cacciatore, Vinícius G. Contessoto, Roy G.H.P. van Heesbeen, Bram van den Broek, Aditya N. Mhaskar, Hans Teunissen, Brian Glenn St Hilaire, David Weisz, Arina D. Omer, Melanie Pham, Zane Colaric, Zhenzhen Yang, Suhas S.P. Rao, Namita MitraChristopher Lui, Weijie Yao, Ruqayya Khan, Leonid L. Moroz, Andrea Kohn, Judy St. Leger, Alexandria Mena, Karen Holcroft, Maria Cristina Gambetta, Fabian Lim, Emma Farley, Nils Stein, Alexander Haddad, Daniel Chauss, Ayse Sena Mutlu, Meng C. Wang, Neil D. Young, Evin Hildebrandt, Hans H. Cheng, Christopher J. Knight, Theresa L.U. Burnham, Kevin A. Hovel, Andrew J. Beel, Pierre Jean Mattei, Roger D. Kornberg, Wesley C. Warren, Gregory Cary, José Luis Gómez-Skarmeta, Veronica Hinman, Kerstin Lindblad-Toh, Federica Di Palma, Kazuhiro Maeshima, Asha S. Multani, Sen Pathak, Liesl Nel-Themaat, Richard R. Behringer, Parwinder Kaur, René H. Medema, Bas van Steensel, Elzo de Wit, José N. Onuchic, Michele Di Pierro, Erez Lieberman Aiden*, Benjamin D. Rowland

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

44 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article numberabe2218
JournalScience
Volume372
Issue number6545
DOIs
Publication statusPublished - 28 May 2021
Externally publishedYes

Bibliographical note

Funding Information:
Funding: C.H. is supported by the Boehringer Ingelheim Fonds; C.H., ?.S.C., and B.D.R. are supported by an ERC CoG (772471, ?CohesinLooping?); A.M.O.E. and B.D.R. are supported by the Dutch Research Council (NWO-Echo); and J.A.R. and R.H.M. are supported by the Dutch Cancer Society (KWF). T.v.S. and B.v.S. are supported by NIH Common Fund ?4D Nucleome? Program grant U54DK107965. H.T. and E.d.W. are supported by an ERC StG (637597, ?HAP-PHEN?). J.A.R., T.v.S., H.T., R.H.M., B.v.S., and E.d.W. are part of the Oncode Institute, which is partly financed by the Dutch Cancer Society. Work at the Center for Theoretical Biological Physics is sponsored by the NSF (grants PHY-2019745 and CHE-1614101) and by the Welch Foundation (grant C-1792). V.G.C. is funded by FAPESP (S?o Paulo State Research Foundation and Higher Education Personnel) grants 2016/13998-8 and 2017/09662-7. J.N.O. is a CPRIT Scholar in Cancer Research. E.L.A. was supported by an NSF Physics Frontiers Center Award (PHY-2019745), the Welch Foundation (Q-1866), a USDA Agriculture and Food Research Initiative grant (2017-05741), the Behavioral Plasticity Research Institute (NSF DBI-2021795), and an NIH Encyclopedia of DNA Elements Mapping Center Award (UM1HG009375). Hi-C data for the 24 species were created by the DNA Zoo Consortium (www.dnazoo.org). DNA Zoo is supported by Illumina, Inc.; IBM; and the Pawsey Supercomputing Center. P.K. is supported by the University of Western Australia. L.L.M. was supported by NIH (1R01NS114491) and NSF awards (1557923, 1548121, and 1645219) and the Human Frontiers Science Program (RGP0060/2017). The draft A. californica project was supported by NHGRI. J.L.G.-S. received funding from the ERC (grant agreement no. 740041), the Spanish Ministerio de Econom?a y Competitividad (grant no. BFU2016-74961-P), and the institutional grant Unidad de Excelencia Mar?a de Maeztu (MDM-2016-0687). R.D.K. is supported by NIH grant RO1DK121366. V.H. is supported by NIH grant NIH1P41HD071837. K.M. is supported by a MEXT grant (20H05936). M.C.W. is supported by the NIH grants R01AG045183, R01AT009050, R01AG062257, and DP1DK113644 and by the Welch Foundation. E.F. was supported by NHGRI (grant no. DP2HG010013). M.C.W. is a Howard Hughes Medical Institute Investigator.

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