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

• Published in: Science (American Association for the Advancement of Science) Vol. 372; no. 6545; p. 984
• Main Authors: Hoencamp, Claire, Dudchenko, Olga, Elbatsh, Ahmed M O, Brahmachari, Sumitabha, Raaijmakers, Jonne A, van Schaik, Tom, Sedeño Cacciatore, Ángela, Contessoto, Vinícius G, van Heesbeen, Roy G H P, van den Broek, Bram, Mhaskar, Aditya N, Teunissen, Hans, St Hilaire, Brian Glenn, Weisz, David, Omer, Arina D, Pham, Melanie, Colaric, Zane, Yang, Zhenzhen, Rao, Suhas S P, Mitra, Namita, Lui, Christopher, Yao, Weijie, Khan, Ruqayya, Moroz, Leonid L, Kohn, Andrea, St Leger, Judy, Mena, Alexandria, Holcroft, Karen, Gambetta, Maria Cristina, Lim, Fabian, Farley, Emma, Stein, Nils, Haddad, Alexander, Chauss, Daniel, Mutlu, Ayse Sena, Wang, Meng C, Young, Neil D, Hildebrandt, Evin, Cheng, Hans H, Knight, Christopher J, Burnham, Theresa L U, Hovel, Kevin A, Beel, Andrew J, Mattei, Pierre-Jean, Kornberg, Roger D, Warren, Wesley C, Cary, Gregory, Gómez-Skarmeta, José Luis, Hinman, Veronica, Lindblad-Toh, Kerstin, Di Palma, Federica, Maeshima, Kazuhiro, Multani, Asha S, Pathak, Sen, Nel-Themaat, Liesl, Behringer, Richard R, Kaur, Parwinder, Medema, René H, van Steensel, Bas, de Wit, Elzo, Onuchic, José N, Di Pierro, Michele, Lieberman Aiden, Erez, Rowland, Benjamin D
• Format: Journal Article
• Language: English
• Published: United States 28.05.2021
• Subjects: Adenosine Triphosphatases - chemistry; Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - physiology; Algorithms; Animals; Biological Evolution; Cell Nucleolus - ultrastructure; Cell Nucleus - ultrastructure; Centromere - ultrastructure; Chromosomes - chemistry; Chromosomes - ultrastructure; Chromosomes, Human - chemistry; Chromosomes, Human - ultrastructure; DNA-Binding Proteins - chemistry; DNA-Binding Proteins - genetics; DNA-Binding Proteins - physiology; Eukaryota - genetics; Genome; Genome, Human; Genomics; Heterochromatin - ultrastructure; Humans; Interphase; Mitosis; Models, Biological; Multiprotein Complexes - chemistry; Multiprotein Complexes - genetics; Multiprotein Complexes - physiology; Telomere - ultrastructure
• ISSN: 1095-9203; 0036-8075; 1095-9203
• DOI: 10.1126/science.abe2218

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.