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

Author:

Hoencamp Claire1ORCID,Dudchenko Olga234ORCID,Elbatsh Ahmed M. O.1ORCID,Brahmachari Sumitabha4ORCID,Raaijmakers Jonne A.5ORCID,van Schaik Tom6ORCID,Sedeño Cacciatore Ángela1ORCID,Contessoto Vinícius G.47ORCID,van Heesbeen Roy G. H. P.5,van den Broek Bram8ORCID,Mhaskar Aditya N.1ORCID,Teunissen Hans6,St Hilaire Brian Glenn23,Weisz David23ORCID,Omer Arina D.2ORCID,Pham Melanie2ORCID,Colaric Zane2,Yang Zhenzhen9,Rao Suhas S. P.2310,Mitra Namita23,Lui Christopher2ORCID,Yao Weijie2,Khan Ruqayya23ORCID,Moroz Leonid L.11ORCID,Kohn Andrea11,St. Leger Judy12ORCID,Mena Alexandria13,Holcroft Karen14,Gambetta Maria Cristina15ORCID,Lim Fabian16ORCID,Farley Emma16ORCID,Stein Nils171819ORCID,Haddad Alexander2,Chauss Daniel20,Mutlu Ayse Sena3ORCID,Wang Meng C.32122ORCID,Young Neil D.23ORCID,Hildebrandt Evin24ORCID,Cheng Hans H.24ORCID,Knight Christopher J.25ORCID,Burnham Theresa L. U.2627ORCID,Hovel Kevin A.27ORCID,Beel Andrew J.10ORCID,Mattei Pierre-Jean10,Kornberg Roger D.10ORCID,Warren Wesley C.28ORCID,Cary Gregory29ORCID,Gómez-Skarmeta José Luis30,Hinman Veronica31ORCID,Lindblad-Toh Kerstin3233ORCID,Di Palma Federica34,Maeshima Kazuhiro3536ORCID,Multani Asha S.37ORCID,Pathak Sen37ORCID,Nel-Themaat Liesl37,Behringer Richard R.37,Kaur Parwinder19ORCID,Medema René H.5,van Steensel Bas6ORCID,de Wit Elzo6ORCID,Onuchic José N.438ORCID,Di Pierro Michele439ORCID,Lieberman Aiden Erez234919ORCID,Rowland Benjamin D.1ORCID

Affiliation:

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

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

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

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

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

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

7. Department of Physics, Institute of Biosciences, Letters and Exact Sciences, São Paulo State University (UNESP), São José do Rio Preto – SP, 15054-000, Brazil.

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

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

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

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

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

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

14. Moody Gardens, Galveston, TX 77554, USA.

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

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

17. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK Gatersleben), 06466 Seeland, Germany.

18. Center of Integrated Breeding Research (CiBreed), Department of Crop Sciences, Georg-August-University Göttingen, 37075 Göttingen, Germany.

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

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

21. Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA.

22. Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030, USA.

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

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

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

26. Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, Davis, CA 95616, USA.

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

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

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

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

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

32. Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

33. Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 751 23 Uppsala, Sweden.

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

35. Genome Dynamics Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.

36. Department of Genetics, Sokendai (Graduate University for Advanced Studies), Mishima, Shizuoka 411-8540, Japan.

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

38. Departments of Physics and Astronomy, Chemistry, and Biosciences, Rice University, Houston, TX 77005, USA.

39. Department of Physics, Northeastern University, Boston, MA 02115, USA.

Abstract

Organismal evolution of the 3D genome The conformation of chromosomes within the nucleus can reflect a cell's type or state. However, studies of the conservation and evolutionary history of the mechanisms regulating genome structure across species are lacking. Hoencamp et al. mapped three-dimensional (3D) genome organization in 24 eukaryote species, including animals, fungi, and plants. At interphase, species' telomeres and centromeres either clustered across chromosomes or oriented in a polarized state maintaining individual chromosomal territories within the cell, a difference attributed to condensin II. An experimental loss of condensin II in human cells promotes the formation of centromere clusters but has no effect on loop or compartment formation. Whether the structure of the 3D genome varies across species may thus depend on whether they carry a functional condensin II gene. Science , abe2218, this issue p. 984

Funder

National Science Foundation

National Institutes of Health

Howard Hughes Medical Institute

European Research Council

Ministerio de Economía y Competitividad

U.S. Department of Agriculture

Welch Foundation

Boehringer Ingelheim Fonds

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

The University of Western Australia

Australian Government

Cancer Prevention and Research Institute of Texas

São Paulo Research Foundation

Human Frontier Science Program

KWF Kankerbestrijding

Government of Western Australia

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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