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The evolution of gene expression levels in mammalian organs

Author

Listed:
  • David Brawand

    (Center for Integrative Genomics, University of Lausanne
    Swiss Institute of Bioinformatics)

  • Magali Soumillon

    (Center for Integrative Genomics, University of Lausanne
    Swiss Institute of Bioinformatics)

  • Anamaria Necsulea

    (Center for Integrative Genomics, University of Lausanne
    Swiss Institute of Bioinformatics)

  • Philippe Julien

    (Center for Integrative Genomics, University of Lausanne
    Swiss Institute of Bioinformatics)

  • Gábor Csárdi

    (Swiss Institute of Bioinformatics
    University of Lausanne)

  • Patrick Harrigan

    (University of California)

  • Manuela Weier

    (Center for Integrative Genomics, University of Lausanne)

  • Angélica Liechti

    (Center for Integrative Genomics, University of Lausanne)

  • Ayinuer Aximu-Petri

    (Max Planck Institute for Evolutionary Anthropology)

  • Martin Kircher

    (Max Planck Institute for Evolutionary Anthropology)

  • Frank W. Albert

    (Max Planck Institute for Evolutionary Anthropology
    Present address: Lewis Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA.)

  • Ulrich Zeller

    (Chair of Systematic Zoology, Humboldt-University)

  • Philipp Khaitovich

    (CAS-MPG Partner Institute for Computational Biology)

  • Frank Grützner

    (The Robinson Institute, School of Molecular and Biomedical Science, University of Adelaide)

  • Sven Bergmann

    (Swiss Institute of Bioinformatics
    University of Lausanne)

  • Rasmus Nielsen

    (University of California
    The Bioinformatics Center, University of Copenhagen)

  • Svante Pääbo

    (Max Planck Institute for Evolutionary Anthropology)

  • Henrik Kaessmann

    (Center for Integrative Genomics, University of Lausanne
    Swiss Institute of Bioinformatics)

Abstract

Changes in gene expression are thought to underlie many of the phenotypic differences between species. However, large-scale analyses of gene expression evolution were until recently prevented by technological limitations. Here we report the sequencing of polyadenylated RNA from six organs across ten species that represent all major mammalian lineages (placentals, marsupials and monotremes) and birds (the evolutionary outgroup), with the goal of understanding the dynamics of mammalian transcriptome evolution. We show that the rate of gene expression evolution varies among organs, lineages and chromosomes, owing to differences in selective pressures: transcriptome change was slow in nervous tissues and rapid in testes, slower in rodents than in apes and monotremes, and rapid for the X chromosome right after its formation. Although gene expression evolution in mammals was strongly shaped by purifying selection, we identify numerous potentially selectively driven expression switches, which occurred at different rates across lineages and tissues and which probably contributed to the specific organ biology of various mammals.

Suggested Citation

  • David Brawand & Magali Soumillon & Anamaria Necsulea & Philippe Julien & Gábor Csárdi & Patrick Harrigan & Manuela Weier & Angélica Liechti & Ayinuer Aximu-Petri & Martin Kircher & Frank W. Albert & U, 2011. "The evolution of gene expression levels in mammalian organs," Nature, Nature, vol. 478(7369), pages 343-348, October.
    • Handle: RePEc:nat:nature:v:478:y:2011:i:7369:d:10.1038_nature10532
    DOI: 10.1038/nature10532
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    1. Orshay Gabay & Yoav Shoshan & Eli Kopel & Udi Ben-Zvi & Tomer D. Mann & Noam Bressler & Roni Cohen‐Fultheim & Amos A. Schaffer & Shalom Hillel Roth & Ziv Tzur & Erez Y. Levanon & Eli Eisenberg, 2022. "Landscape of adenosine-to-inosine RNA recoding across human tissues," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Lydie Cheval & Fabien Pierrat & Rabary Rajerison & David Piquemal & Alain Doucet, 2012. "Of Mice and Men: Divergence of Gene Expression Patterns in Kidney," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-12, October.
    3. Long Jin & Danyang Wang & Jiaman Zhang & Pengliang Liu & Yujie Wang & Yu Lin & Can Liu & Ziyin Han & Keren Long & Diyan Li & Yu Jiang & Guisen Li & Yu Zhang & Jingyi Bai & Xiaokai Li & Jing Li & Lu Lu, 2023. "Dynamic chromatin architecture of the porcine adipose tissues with weight gain and loss," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Milan Kumar Samanta & Srimonta Gayen & Clair Harris & Emily Maclary & Yumie Murata-Nakamura & Rebecca M. Malcore & Robert S. Porter & Patricia M. Garay & Christina N. Vallianatos & Paul B. Samollow & , 2022. "Activation of Xist by an evolutionarily conserved function of KDM5C demethylase," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Sook Wah Yee & Luis Ferrández-Peral & Pol Alentorn-Moron & Claudia Fontsere & Merve Ceylan & Megan L. Koleske & Niklas Handin & Virginia M. Artegoitia & Giovanni Lara & Huan-Chieh Chien & Xujia Zhou &, 2024. "Illuminating the function of the orphan transporter, SLC22A10, in humans and other primates," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Mathilde Paris & Tommy Kaplan & Xiao Yong Li & Jacqueline E Villalta & Susan E Lott & Michael B Eisen, 2013. "Extensive Divergence of Transcription Factor Binding in Drosophila Embryos with Highly Conserved Gene Expression," PLOS Genetics, Public Library of Science, vol. 9(9), pages 1-18, September.
    7. Chisa Shiraishi & Akinobu Matsumoto & Kazuya Ichihara & Taishi Yamamoto & Takeshi Yokoyama & Taisuke Mizoo & Atsushi Hatano & Masaki Matsumoto & Yoshikazu Tanaka & Eriko Matsuura-Suzuki & Shintaro Iwa, 2023. "RPL3L-containing ribosomes determine translation elongation dynamics required for cardiac function," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Pingfen Zhu & Weiqiang Liu & Xiaoxiao Zhang & Meng Li & Gaoming Liu & Yang Yu & Zihao Li & Xuanjing Li & Juan Du & Xiao Wang & Cyril C. Grueter & Ming Li & Xuming Zhou, 2023. "Correlated evolution of social organization and lifespan in mammals," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    9. Jasper Panten & Tobias Heinen & Christina Ernst & Nils Eling & Rebecca E. Wagner & Maja Satorius & John C. Marioni & Oliver Stegle & Duncan T. Odom, 2024. "The dynamic genetic determinants of increased transcriptional divergence in spermatids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Joshua G Schraiber & Yulia Mostovoy & Tiffany Y Hsu & Rachel B Brem, 2013. "Inferring Evolutionary Histories of Pathway Regulation from Transcriptional Profiling Data," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-13, October.
    11. Nadezda Kryuchkova-Mostacci & Marc Robinson-Rechavi, 2016. "Tissue-Specificity of Gene Expression Diverges Slowly between Orthologs, and Rapidly between Paralogs," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-13, December.
    12. Jin Woo Oh & Michael A. Beer, 2024. "Gapped-kmer sequence modeling robustly identifies regulatory vocabularies and distal enhancers conserved between evolutionarily distant mammals," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Paola Cornejo-Páramo & Veronika Petrova & Xuan Zhang & Robert S. Young & Emily S. Wong, 2024. "Emergence of enhancers at late DNA replicating regions," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Mark S Hibbins & Matthew W Hahn, 2021. "The effects of introgression across thousands of quantitative traits revealed by gene expression in wild tomatoes," PLOS Genetics, Public Library of Science, vol. 17(11), pages 1-20, November.

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