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

Claire Hoencamp(The Netherlands Cancer Institute), Olga Dudchenko(Baylor College of Medicine), Ahmed M.O. Elbatsh(The Netherlands Cancer Institute), Sumitabha Brahmachari(Center for Theoretical Biological Physics), Jonne A. Raaijmakers(Oncode Institute), Tom van Schaik(Oncode Institute), Ángela Sedeño Cacciatore(The Netherlands Cancer Institute), Vinícius G. Contessoto(Center for Theoretical Biological Physics), Roy G. H. P. van Heesbeen(Oncode Institute), Bram van den Broek(Cancer Genomics Centre), Aditya N. Mhaskar(The Netherlands Cancer Institute), Hans Teunissen(Oncode Institute), Brian Glenn St Hilaire(Baylor College of Medicine), David Weisz(Baylor College of Medicine), Arina D. Omer(Baylor College of Medicine), Melanie Pham(Baylor College of Medicine), Zane Colaric(Baylor College of Medicine), Zhenzhen Yang(ShanghaiTech University), Suhas S.P. Rao(Baylor College of Medicine), Namita Mitra(Baylor College of Medicine), Christopher Lui(Baylor College of Medicine), Weijie Yao(Baylor College of Medicine), Ruqayya Khan(Baylor College of Medicine), Leonid L. Moroz(University of Florida), Andrea B. Kohn(University of Florida), Judy St. Leger(Cornell University), Alexandria Mena(SeaWorld Entertainment), Karen Holcroft, Maria Cristina Gambetta(University of Lausanne), Fabian Lim(University of California San Diego), Emma K. Farley(University of California San Diego), Nils Stein(The University of Western Australia), Alexander F. Haddad(Baylor College of Medicine), Daniel Chauss(National Institutes of Health), Ayse Sena Mutlu(Baylor College of Medicine), Meng C. Wang(Howard Hughes Medical Institute), Neil D. Young(The University of Melbourne), Evin Hildebrandt(Michigan Department of Agriculture and Rural Development), Hans H. Cheng(Michigan Department of Agriculture and Rural Development), Christopher J. Knight(Pacific University), Theresa L.U. Burnham(San Diego State University), Kevin A. Hovel(San Diego State University), Andrew J. Beel(Stanford University), Pierre-Jean Mattei(Stanford University), Roger D. Kornberg(Stanford University), Wesley C. Warren(University of Missouri), Gregory A. Cary(Jackson Laboratory), José Luis Gómez-Skármeta(Centro Andaluz de Biología del Desarrollo), Veronica F. Hinman(Carnegie Mellon University), Kerstin Lindblad‐Toh(Broad Institute), Federica Di Palma(University of East Anglia), Kazuhiro Maeshima(National Institute of Genetics), Asha S. Multani(The University of Texas MD Anderson Cancer Center), Sen Pathak(The University of Texas MD Anderson Cancer Center), Liesl Nel‐Themaat(The University of Texas MD Anderson Cancer Center), Richard R. Behringer(The University of Texas MD Anderson Cancer Center), Parwinder Kaur(The University of Western Australia), René H. Medema(Oncode Institute), Bas van Steensel(Oncode Institute), Elzo de Wit(Oncode Institute), José N. Onuchic(Center for Theoretical Biological Physics), Michele Di Pierro(Northeastern University), Erez Lieberman Aiden(Broad Institute), Benjamin D. Rowland(The Netherlands Cancer Institute)
Science
May 27, 2021
Cited by 298Open Access
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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.


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