Fly Cell Atlas: A single-nucleus transcriptomic atlas of the adult fruit fly

Author:

Li Hongjie123ORCID,Janssens Jasper45ORCID,De Waegeneer Maxime45ORCID,Kolluru Sai Saroja678,Davie Kristofer4ORCID,Gardeux Vincent910ORCID,Saelens Wouter910ORCID,David Fabrice P. A.91011ORCID,Brbić Maria812ORCID,Spanier Katina45ORCID,Leskovec Jure812ORCID,McLaughlin Colleen N.1ORCID,Xie Qijing1ORCID,Jones Robert C.678ORCID,Brueckner Katja13,Shim Jiwon14ORCID,Tattikota Sudhir Gopal1516ORCID,Schnorrer Frank17ORCID,Rust Katja1819ORCID,Nystul Todd G.19ORCID,Carvalho-Santos Zita20ORCID,Ribeiro Carlos20ORCID,Pal Soumitra21ORCID,Mahadevaraju Sharvani22ORCID,Przytycka Teresa M.21ORCID,Allen Aaron M.23ORCID,Goodwin Stephen F.23ORCID,Berry Cameron W.24ORCID,Fuller Margaret T.24ORCID,White-Cooper Helen25ORCID,Matunis Erika L.26ORCID,DiNardo Stephen2728ORCID,Galenza Anthony29ORCID,O’Brien Lucy Erin29,Dow Julian A. T.30ORCID,Jasper Heinrich31,Oliver Brian22ORCID,Perrimon Norbert1516ORCID,Deplancke Bart910ORCID,Quake Stephen R.678ORCID,Luo Liqun1ORCID,Aerts Stein45ORCID,Agarwal Devika32,Ahmed-Braimah Yasir33,Arbeitman Michelle34,Ariss Majd M.35,Augsburger Jordan13,Ayush Kumar12,Baker Catherine C.36,Banisch Torsten37,Birker Katja38,Bodmer Rolf38,Bolival Benjamin36,Brantley Susanna E.36,Brill Julie A.3940,Brown Nora C.41,Buehner Norene A.41,Cai Xiaoyu Tracy31,Cardoso-Figueiredo Rita20,Casares Fernando42,Chang Amy43,Clandinin Thomas R.44,Crasta Sheela678,Desplan Claude45,Detweiler Angela M.8,Dhakan Darshan B.20,Donà Erika46,Engert Stefanie43,Floc’hlay Swann45,George Nancy47,González-Segarra Amanda J.43,Groves Andrew K.348,Gumbin Samantha29,Guo Yanmeng4950,Harris Devon E.36,Heifetz Yael51,Holtz Stephen L.52,Horns Felix53,Hudry Bruno54,Hung Ruei-Jiun15,Jan Yuh Nung4950,Jaszczak Jacob S.4950,Jefferis Gregory S. X. E.46,Karkanias Jim8,Karr Timothy L.55,Katheder Nadja Sandra31,Kezos James38,Kim Anna A.295657,Kim Seung K.2458,Kockel Lutz24,Konstantinides Nikolaos59,Kornberg Thomas B.60,Krause Henry M.61,Labott Andrew Thomas29,Laturney Meghan43,Lehmann Ruth62,Leinwand Sarah43,Li Jiefu1,Li Joshua Shing Shun15,Li Kai4950,Li Ke4950,Li Liying4950,Li Tun4950,Litovchenko Maria910,Liu Han-Hsuan4950,Liu Yifang15,Lu Tzu-Chiao2,Manning Jonathan47,Mase Anjeli13,Matera-Vatnick Mikaela41,Matias Neuza Reis36,McDonough-Goldstein Caitlin E.6364,McGeever Aaron8,McLachlan Alex D.65,Moreno-Roman Paola29,Neff Norma8,Neville Megan23,Ngo Sang29,Nielsen Tanja38,O’Brien Caitlin E.4950,Osumi-Sutherland David66,Özel Mehmet Neset67,Papatheodorou Irene47,Petkovic Maja4950,Pilgrim Clare68,Pisco Angela Oliveira8,Reisenman Carolina43,Sanders Erin Nicole29,dos Santos Gilberto69,Scott Kristin43,Sherlekar Aparna29,Shiu Philip43,Sims David32,Sit Rene V.8,Slaidina Maija70,Smith Harold E.71,Sterne Gabriella43,Su Yu-Han29,Sutton Daniel72,Tamayo Marco38,Tan Michelle8,Tastekin Ibrahim20,Treiber Christoph73,Vacek David1,Vogler Georg38,Waddell Scott73,Wang Wanpeng60,Wilson Rachel I.52,Wolfner Mariana F.41,Wong Yiu-Cheung E.36,Xie Anthony1,Xu Jun15,Yamamoto Shinya374,Yan Jia8,Yao Zepeng43,Yoda Kazuki29,Zhu Ruijun4950,Zinzen Robert P.75,

Affiliation:

1. Howard Hughes Medical Institute, Department of Biology, Stanford University, Stanford, CA 94305, USA.

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

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

4. VIB-KU Leuven Center for Brain and Disease Research, KU Leuven, Leuven 3000, Belgium.

5. Laboratory of Computational Biology, Department of Human Genetics, KU Leuven, Leuven 3000, Belgium.

6. Department of Bioengineering, Stanford University, Stanford, CA, USA.

7. Department of Applied Physics, Stanford University, Stanford, CA, USA.

8. Chan Zuckerberg Biohub, San Francisco CA, USA.

9. Laboratory of Systems Biology and Genetics, Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015 Lausanne, Switzerland.

10. Swiss Institute of Bioinformatics, CH-1015 Lausanne, Switzerland.

11. Bioinformatics Competence Center, EPFL, Switzerland.

12. Department of Computer Science, Stanford University, Stanford, CA 94305, USA.

13. Department of Cell and Tissue Biology, University of California, San Francisco, CA 94143, USA.

14. Department of Life Science, College of Natural Science, Hanyang University, 04763 Seoul, Republic of Korea.

15. Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA.

16. Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

17. Aix-Marseille University, CNRS, IBDM (UMR 7288), Turing Centre for Living Systems, 13009 Marseille, France.

18. Institute of Physiology and Pathophysiology, Department of Molecular Cell Physiology, Philipps-University, Marburg, Germany.

19. Department of Anatomy, University of California, San Francisco, CA 94143, USA.

20. Behavior and Metabolism Laboratory, Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal.

21. National Center of Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.

22. Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Kidney and Digestive Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

23. Centre for Neural Circuits and Behaviour, University of Oxford, Oxford OX1 3SR, UK.

24. Department of Developmental Biology and Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.

25. Molecular Biosciences Division, Cardiff University, Cardiff CF10 3AX, UK.

26. Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

27. Perelman School of Medicine, The University of Pennsylvania, Philadelphia, PA 19104, USA.

28. The Penn Institute for Regenerative Medicine, Philadelphia, PA 19104, USA.

29. Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA 94305, USA.

30. Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK.

31. Immunology Discovery, Genentech, Inc., South San Francisco, CA 94080, USA.

32. MRC Weatherall Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK.

33. Department of Biology, Syracuse University, Syracuse, NY 13244 USA.

34. Biomedical Sciences Department, Florida State University, Tallahassee, FL, USA.

35. Department of Genetics, Harvard Medical School, Boston, MA, USA.

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

37. Skirball Institute and HHMI, New York University Langone Medical Center, New York City, NY 10016, USA.

38. Development, Aging and Regeneration Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA.

39. Cell Biology Program, The Hospital for Sick Children (SickKids), Toronto, ON M5G 0A4, Canada.

40. Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.

41. Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA.

42. CABD (Andalusian Centre for Developmental Biology), CSIC-UPO-JA, Seville 41013, Spain.

43. Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.

44. Department of Neurobiology, Stanford University, Stanford, CA 94305, USA.

45. Department of Biology, New York University, New York, New York 10003, USA.

46. Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK.

47. European Molecular Biology Laboratory, European Bioinformatics Institute, EMBL-EBI, Wellcome Trust Genome Campus, Hinxton CB10 1SD, UK.

48. Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.

49. Department of Physiology, Department of Biochemistry and Biophysics, University of California at San Francisco, San Francisco, CA, USA.

50. Howard Hughes Medical Institute, San Francisco, CA, USA.

51. The Hebrew University of Jerusalem, Jerusalem, Israel.

52. Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA.

53. Department of Bioengineering and Biophysics Graduate Program, Stanford University, Stanford, CA 94305, USA.

54. Université Côte d’Azur, CNRS, INSERM, iBV, France.

55. Biodesign Institute, Arizona State University, Tempe, AZ 85281, USA.

56. University of California, Santa Barbara, CA 93106, USA.

57. Uppsala University, Sweden.

58. Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA.

59. Institut Jacques Monod, Centre National de la Recherche Scientifique-UMR 7592, Université Paris Diderot, Paris, France.

60. Cardiovascular Research Institute, University of California, San Francisco, CA 94143, USA.

61. Donnelly Centre for Cellular and Biomolecular Research, Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada.

62. Skirball Institute, Department of Cell Biology and HHMI, New York University Langone Medical Center, New York City, NY 10016.

63. Department of Biology, Syracuse University, Syracuse, NY, USA.

64. Department of Evolutionary Biology, University of Vienna, Vienna, Austria.

65. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK.

66. European Bioinformatics Institute (EMBL/EBI), Wellcome Trust Genome Campus, Cambridge, UK.

67. Department of Biology, New York University, New York, NY 10003, USA.

68. Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3DY, UK.

69. The Biological Laboratories, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA.

70. Skirball Institute, Faculty of Medicine, New York University, New York, NY 10016.

71. Genomics Core, National Institute of Diabetes and Digestive and Kidney Diseases, US National Institutes of Health, Bethesda, MD, USA.

72. Graduate Program in Genetics and Genomics, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030 USA.

73. Centre for Neural Circuits and Behaviour, University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3TA, UK.

74. Jan and Dan Duncan Neurological Research Institute, Texas Children’s Hospital, Houston, TX 77030, USA.

75. Laboratory for Systems Biology of Neural Tissue Differentiation, Berlin Institute for Medical Systems Biology (BIMSB), Max Delbrueck Centre for Molecular Medicine (MDC) in the Helmholtz Association, Robert-Roessle-Strasse 12, 13125 Berlin, Germany.

Abstract

For more than 100 years, the fruit fly Drosophila melanogaster has been one of the most studied model organisms. Here, we present a single-cell atlas of the adult fly, Tabula Drosophilae , that includes 580,000 nuclei from 15 individually dissected sexed tissues as well as the entire head and body, annotated to >250 distinct cell types. We provide an in-depth analysis of cell type–related gene signatures and transcription factor markers, as well as sexual dimorphism, across the whole animal. Analysis of common cell types between tissues, such as blood and muscle cells, reveals rare cell types and tissue-specific subtypes. This atlas provides a valuable resource for the Drosophila community and serves as a reference to study genetic perturbations and disease models at single-cell resolution.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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