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


Journal

Science (New York, N.Y.)
ISSN: 1095-9203
Titre abrégé: Science
Pays: United States
ID NLM: 0404511

Informations de publication

Date de publication:
28 05 2021
Historique:
received: 19 08 2020
accepted: 16 04 2021
entrez: 28 5 2021
pubmed: 29 5 2021
medline: 12 6 2021
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 34045355
pii: 372/6545/984
doi: 10.1126/science.abe2218
pmc: PMC8172041
mid: NIHMS1704706
doi:

Substances chimiques

DNA-Binding Proteins 0
Heterochromatin 0
Multiprotein Complexes 0
condensin complexes 0
Adenosine Triphosphatases EC 3.6.1.-

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

984-989

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK121366
Pays : United States
Organisme : NHGRI NIH HHS
ID : UM1 HG009375
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG022537
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS114491
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG062257
Pays : United States
Organisme : NIDDK NIH HHS
ID : U54 DK107965
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG045183
Pays : United States
Organisme : NIDDK NIH HHS
ID : DP1 DK113644
Pays : United States
Organisme : NCCIH NIH HHS
ID : R01 AT009050
Pays : United States
Organisme : NICHD NIH HHS
ID : P41 HD071837
Pays : United States
Organisme : NHGRI NIH HHS
ID : DP2 HG010013
Pays : United States

Informations de copyright

Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.

Références

EMBO J. 2020 Mar 16;39(6):e103159
pubmed: 32080885
Genes Dev. 2011 Jul 15;25(14):1464-9
pubmed: 21715560
Cell. 2014 Dec 18;159(7):1665-80
pubmed: 25497547
Nucleus. 2019 Dec;10(1):116-125
pubmed: 31092096
Mol Biol Evol. 2019 Oct 1;36(10):2195-2204
pubmed: 31270536
J Cell Sci. 2004 Dec 15;117(Pt 26):6435-45
pubmed: 15572404
PLoS Genet. 2012;8(8):e1002873
pubmed: 22956908
Nature. 2008 Jun 12;453(7197):948-51
pubmed: 18463634
Proc Natl Acad Sci U S A. 2016 Oct 25;113(43):12168-12173
pubmed: 27688758
Dev Cell. 2015 Apr 6;33(1):94-106
pubmed: 25850674
Phys Rev Lett. 2016 Jun 17;116(24):248101
pubmed: 27367409
Mol Cell. 2013 Apr 25;50(2):236-49
pubmed: 23562326
Cell. 2017 May 18;169(5):780-791
pubmed: 28525751
Science. 2018 Feb 9;359(6376):
pubmed: 29348367
PLoS Genet. 2018 Jul 12;14(7):e1007393
pubmed: 30001329
Cell. 2016 Feb 25;164(5):847-57
pubmed: 26919425
Nature. 2017 Jul 13;547(7662):241-245
pubmed: 28636597
Nature. 2017 Jul 13;547(7662):236-240
pubmed: 28636604
Nature. 2019 Jun;570(7761):395-399
pubmed: 31168090
J Cell Sci. 2012 Mar 15;125(Pt 6):1591-604
pubmed: 22344259
Mol Biol Cell. 2004 Jul;15(7):3296-308
pubmed: 15146063
Chromosoma. 2013 Dec;122(6):517-33
pubmed: 23929493
PLoS Genet. 2014 Dec 04;10(12):e1004847
pubmed: 25474630

Auteurs

Claire Hoencamp (C)

Division of Gene Regulation, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Olga Dudchenko (O)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
Center for Theoretical Biological Physics, Rice University, Houston, TX 77005, USA.

Ahmed M O Elbatsh (AMO)

Division of Gene Regulation, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Sumitabha Brahmachari (S)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77005, USA.

Jonne A Raaijmakers (JA)

Division of Cell Biology, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Tom van Schaik (T)

Division of Gene Regulation, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Ángela Sedeño Cacciatore (Á)

Division of Gene Regulation, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Vinícius G Contessoto (VG)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77005, USA.
Department of Physics, Institute of Biosciences, Letters and Exact Sciences, São Paulo State University (UNESP), São José do Rio Preto - SP, 15054-000, Brazil.

Roy G H P van Heesbeen (RGHP)

Division of Cell Biology, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Bram van den Broek (B)

BioImaging Facility, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Aditya N Mhaskar (AN)

Division of Gene Regulation, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Hans Teunissen (H)

Division of Gene Regulation, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Brian Glenn St Hilaire (BG)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

David Weisz (D)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Arina D Omer (AD)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.

Melanie Pham (M)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.

Zane Colaric (Z)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.

Zhenzhen Yang (Z)

Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech, Pudong 201210, China.

Suhas S P Rao (SSP)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

Namita Mitra (N)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Christopher Lui (C)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.

Weijie Yao (W)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.

Ruqayya Khan (R)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Leonid L Moroz (LL)

Whitney Laboratory and Department of Neuroscience, University of Florida, Gainesville, FL 32611, USA.

Andrea Kohn (A)

Whitney Laboratory and Department of Neuroscience, University of Florida, Gainesville, FL 32611, USA.

Judy St Leger (J)

Department of Biosciences, Cornell University College of Veterinary Medicine, Ithaca, NY 14853, USA.

Alexandria Mena (A)

SeaWorld San Diego, San Diego, CA 92109, USA.

Karen Holcroft (K)

Moody Gardens, Galveston, TX 77554, USA.

Maria Cristina Gambetta (MC)

Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland.

Fabian Lim (F)

Department of Medicine and Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA.

Emma Farley (E)

Department of Medicine and Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA.

Nils Stein (N)

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK Gatersleben), 06466 Seeland, Germany.
Center of Integrated Breeding Research (CiBreed), Department of Crop Sciences, Georg-August-University Göttingen, 37075 Göttingen, Germany.
UWA School of Agriculture and Environment, The University of Western Australia, Perth, WA 6009, Australia.

Alexander Haddad (A)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA.

Daniel Chauss (D)

National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Ayse Sena Mutlu (AS)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Meng C Wang (MC)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA.
Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030, USA.

Neil D Young (ND)

Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, VIC 3010, Australia.

Evin Hildebrandt (E)

Avian Diseases and Oncology Laboratory, US Department of Agriculture, Agricultural Research Service, East Lansing, MI 48823, USA.

Hans H Cheng (HH)

Avian Diseases and Oncology Laboratory, US Department of Agriculture, Agricultural Research Service, East Lansing, MI 48823, USA.

Christopher J Knight (CJ)

Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, USA.

Theresa L U Burnham (TLU)

Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, Davis, CA 95616, USA.
Coastal and Marine Institute and Department of Biology, San Diego State University, San Diego, CA 92106, USA.

Kevin A Hovel (KA)

Coastal and Marine Institute and Department of Biology, San Diego State University, San Diego, CA 92106, USA.

Andrew J Beel (AJ)

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

Pierre-Jean Mattei (PJ)

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

Roger D Kornberg (RD)

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

Wesley C Warren (WC)

Department of Animal Sciences, University of Missouri, Columbia, MO 65211, USA.

Gregory Cary (G)

The Jackson Laboratory, Bar Harbor, ME 04609, USA.

José Luis Gómez-Skarmeta (JL)

Centro Andaluz de Biología del Desarrollo CSIC, Universidad Pablo de Olavide, 41013 Sevilla, Spain.

Veronica Hinman (V)

Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213, USA.

Kerstin Lindblad-Toh (K)

Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 751 23 Uppsala, Sweden.

Federica Di Palma (F)

Department of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK.

Kazuhiro Maeshima (K)

Genome Dynamics Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
Department of Genetics, Sokendai (Graduate University for Advanced Studies), Mishima, Shizuoka 411-8540, Japan.

Asha S Multani (AS)

Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.

Sen Pathak (S)

Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.

Liesl Nel-Themaat (L)

Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.

Richard R Behringer (RR)

Department of Genetics, University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.

Parwinder Kaur (P)

UWA School of Agriculture and Environment, The University of Western Australia, Perth, WA 6009, Australia.

René H Medema (RH)

Division of Cell Biology, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Bas van Steensel (B)

Division of Gene Regulation, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

Elzo de Wit (E)

Division of Gene Regulation, Oncode Institute, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands.

José N Onuchic (JN)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77005, USA.
Departments of Physics and Astronomy, Chemistry, and Biosciences, Rice University, Houston, TX 77005, USA.

Michele Di Pierro (M)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77005, USA.
Department of Physics, Northeastern University, Boston, MA 02115, USA.

Erez Lieberman Aiden (E)

The Center for Genome Architecture, Baylor College of Medicine, Houston, TX 77030, USA. b.rowland@nki.nl erez@erez.com.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
Center for Theoretical Biological Physics, Rice University, Houston, TX 77005, USA.
Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech, Pudong 201210, China.
UWA School of Agriculture and Environment, The University of Western Australia, Perth, WA 6009, Australia.
Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

Benjamin D Rowland (BD)

Division of Gene Regulation, Netherlands Cancer Institute, 1066 CX Amsterdam, Netherlands. b.rowland@nki.nl erez@erez.com.

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