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Gene expression across mammalian organ development

Author

Listed:
  • Margarida Cardoso-Moreira

    (Center for Molecular Biology of Heidelberg University (ZMBH)
    University of Lausanne)

  • Jean Halbert

    (University of Lausanne)

  • Delphine Valloton

    (University of Lausanne)

  • Britta Velten

    (European Molecular Biology Laboratory)

  • Chunyan Chen

    (Chinese Academy of Sciences
    Institute of Zoology, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yi Shao

    (Chinese Academy of Sciences
    Institute of Zoology, Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Angélica Liechti

    (University of Lausanne)

  • Kelly Ascenção

    (University of Lausanne)

  • Coralie Rummel

    (University of Lausanne)

  • Svetlana Ovchinnikova

    (Center for Molecular Biology of Heidelberg University (ZMBH))

  • Pavel V. Mazin

    (Skolkovo Institute of Science and Technology
    Institute for Information Transmission Problems (Kharkevich Institute) RAS
    HSE University)

  • Ioannis Xenarios

    (University of Lausanne)

  • Keith Harshman

    (University of Lausanne)

  • Matthew Mort

    (Cardiff University)

  • David N. Cooper

    (Cardiff University)

  • Carmen Sandi

    (Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL))

  • Michael J. Soares

    (University of Kansas Medical Center
    Children’s Mercy)

  • Paula G. Ferreira

    (Universidade do Porto
    Universidade do Porto)

  • Sandra Afonso

    (Universidade do Porto)

  • Miguel Carneiro

    (Universidade do Porto
    Universidade do Porto)

  • James M. A. Turner

    (The Francis Crick Institute)

  • John L. VandeBerg

    (The University of Texas Rio Grande Valley, Brownsville
    The University of Texas Rio Grande Valley, Brownsville)

  • Amir Fallahshahroudi

    (Linköping University)

  • Per Jensen

    (Linköping University)

  • Rüdiger Behr

    (Leibniz Institute for Primate Research (DPZ)
    Partner Site Göttingen)

  • Steven Lisgo

    (Newcastle University)

  • Susan Lindsay

    (Newcastle University)

  • Philipp Khaitovich

    (Skolkovo Institute of Science and Technology
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences, Chinese Academy of Sciences)

  • Wolfgang Huber

    (European Molecular Biology Laboratory)

  • Julie Baker

    (Stanford University School of Medicine)

  • Simon Anders

    (Center for Molecular Biology of Heidelberg University (ZMBH))

  • Yong E. Zhang

    (Chinese Academy of Sciences
    Institute of Zoology, Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Henrik Kaessmann

    (Center for Molecular Biology of Heidelberg University (ZMBH))

Abstract

The evolution of gene expression in mammalian organ development remains largely uncharacterized. Here we report the transcriptomes of seven organs (cerebrum, cerebellum, heart, kidney, liver, ovary and testis) across developmental time points from early organogenesis to adulthood for human, rhesus macaque, mouse, rat, rabbit, opossum and chicken. Comparisons of gene expression patterns identified correspondences of developmental stages across species, and differences in the timing of key events during the development of the gonads. We found that the breadth of gene expression and the extent of purifying selection gradually decrease during development, whereas the amount of positive selection and expression of new genes increase. We identified differences in the temporal trajectories of expression of individual genes across species, with brain tissues showing the smallest percentage of trajectory changes, and the liver and testis showing the largest. Our work provides a resource of developmental transcriptomes of seven organs across seven species, and comparative analyses that characterize the development and evolution of mammalian organs.

Suggested Citation

  • Margarida Cardoso-Moreira & Jean Halbert & Delphine Valloton & Britta Velten & Chunyan Chen & Yi Shao & Angélica Liechti & Kelly Ascenção & Coralie Rummel & Svetlana Ovchinnikova & Pavel V. Mazin & Io, 2019. "Gene expression across mammalian organ development," Nature, Nature, vol. 571(7766), pages 505-509, July.
    • Handle: RePEc:nat:nature:v:571:y:2019:i:7766:d:10.1038_s41586-019-1338-5
    DOI: 10.1038/s41586-019-1338-5
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    Cited by:

    1. Rudrarup Bhattacharjee & Lachlan A. Jolly & Mark A. Corbett & Ing Chee Wee & Sushma R. Rao & Alison E. Gardner & Tarin Ritchie & Eline J. H. Hugte & Ummi Ciptasari & Sandra Piltz & Jacqueline E. Noll , 2024. "Compromised transcription-mRNA export factor THOC2 causes R-loop accumulation, DNA damage and adverse neurodevelopment," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    2. Gwénaëlle Bontonou & Bastien Saint-Leandre & Tane Kafle & Tess Baticle & Afrah Hassan & Juan Antonio Sánchez-Alcañiz & J. Roman Arguello, 2024. "Evolution of chemosensory tissues and cells across ecologically diverse Drosophilids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Tara N. Yankee & Sungryong Oh & Emma Wentworth Winchester & Andrea Wilderman & Kelsey Robinson & Tia Gordon & Jill A. Rosenfeld & Jennifer VanOudenhove & Daryl A. Scott & Elizabeth J. Leslie & Justin , 2023. "Integrative analysis of transcriptome dynamics during human craniofacial development identifies candidate disease genes," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    4. 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.
    5. Juexin Wang & Jinpu Li & Skyler T. Kramer & Li Su & Yuzhou Chang & Chunhui Xu & Michael T. Eadon & Krzysztof Kiryluk & Qin Ma & Dong Xu, 2023. "Dimension-agnostic and granularity-based spatially variable gene identification using BSP," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Marion Müller & Rose Eghbalian & Jes-Niels Boeckel & Karen S. Frese & Jan Haas & Elham Kayvanpour & Farbod Sedaghat-Hamedani & Maximilian K. Lackner & Oguz F. Tugrul & Thomas Ruppert & Rewati Tappu & , 2022. "NIMA-related kinase 9 regulates the phosphorylation of the essential myosin light chain in the heart," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Miguel Angel Brieño-Enríquez & Mariela Faykoo-Martinez & Meagan Goben & Jennifer K. Grenier & Ashley McGrath & Alexandra M. Prado & Jacob Sinopoli & Kate Wagner & Patrick T. Walsh & Samia H. Lopa & Di, 2023. "Postnatal oogenesis leads to an exceptionally large ovarian reserve in naked mole-rats," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Arashdeep Singh & Arati Rajeevan & Vishaka Gopalan & Piyush Agrawal & Chi-Ping Day & Sridhar Hannenhalli, 2022. "Broad misappropriation of developmental splicing profile by cancer in multiple organs," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    9. David R. Amici & Harun Cingoz & Milad J. Alasady & Sammy Alhayek & Claire M. Phoumyvong & Nidhi Sahni & S. Stephen Yi & Marc L. Mendillo, 2023. "The HAPSTR2 retrogene buffers stress signaling and resilience in mammals," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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