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Transcriptome and translatome co-evolution in mammals

Author

Listed:
  • Zhong-Yi Wang

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Evgeny Leushkin

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Angélica Liechti

    (University of Lausanne)

  • Svetlana Ovchinnikova

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Katharina Mößinger

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Thoomke Brüning

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Coralie Rummel

    (University of Lausanne)

  • Frank Grützner

    (University of Adelaide)

  • Margarida Cardoso-Moreira

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Peggy Janich

    (University of Lausanne)

  • David Gatfield

    (University of Lausanne)

  • Boubou Diagouraga

    (Université de Montpellier
    Université de Montpellier)

  • Bernard Massy

    (Université de Montpellier)

  • Mark E. Gill

    (Friedrich Miescher Institute for Biomedical Research)

  • Antoine H. F. M. Peters

    (Friedrich Miescher Institute for Biomedical Research
    University of Basel)

  • Simon Anders

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

  • Henrik Kaessmann

    (Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance)

Abstract

Gene-expression programs define shared and species-specific phenotypes, but their evolution remains largely uncharacterized beyond the transcriptome layer1. Here we report an analysis of the co-evolution of translatomes and transcriptomes using ribosome-profiling and matched RNA-sequencing data for three organs (brain, liver and testis) in five mammals (human, macaque, mouse, opossum and platypus) and a bird (chicken). Our within-species analyses reveal that translational regulation is widespread in the different organs, in particular across the spermatogenic cell types of the testis. The between-species divergence in gene expression is around 20% lower at the translatome layer than at the transcriptome layer owing to extensive buffering between the expression layers, which especially preserved old, essential and housekeeping genes. Translational upregulation specifically counterbalanced global dosage reductions during the evolution of sex chromosomes and the effects of meiotic sex-chromosome inactivation during spermatogenesis. Despite the overall prevalence of buffering, some genes evolved faster at the translatome layer—potentially indicating adaptive changes in expression; testis tissue shows the highest fraction of such genes. Further analyses incorporating mass spectrometry proteomics data establish that the co-evolution of transcriptomes and translatomes is reflected at the proteome layer. Together, our work uncovers co-evolutionary patterns and associated selective forces across the expression layers, and provides a resource for understanding their interplay in mammalian organs.

Suggested Citation

  • Zhong-Yi Wang & Evgeny Leushkin & Angélica Liechti & Svetlana Ovchinnikova & Katharina Mößinger & Thoomke Brüning & Coralie Rummel & Frank Grützner & Margarida Cardoso-Moreira & Peggy Janich & David G, 2020. "Transcriptome and translatome co-evolution in mammals," Nature, Nature, vol. 588(7839), pages 642-647, December.
  • Handle: RePEc:nat:nature:v:588:y:2020:i:7839:d:10.1038_s41586-020-2899-z
    DOI: 10.1038/s41586-020-2899-z
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    Cited by:

    1. 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.
    2. Sarah E. Harris & Maria S. Alexis & Gilbert Giri & Francisco F. Cavazos & Yue Hu & Jernej Murn & Maria M. Aleman & Christopher B. Burge & Daniel Dominguez, 2024. "Understanding species-specific and conserved RNA-protein interactions in vivo and in vitro," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Karl E. Bauer & Niklas Bargenda & Rico Schieweck & Christin Illig & Inmaculada Segura & Max Harner & Michael A. Kiebler, 2022. "RNA supply drives physiological granule assembly in neurons," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Wenqi Hu & Haitao Zeng & Yanan Shi & Chuanchuan Zhou & Jiana Huang & Lei Jia & Siqi Xu & Xiaoyu Feng & Yanyan Zeng & Tuanlin Xiong & Wenze Huang & Peng Sun & Yajie Chang & Tingting Li & Cong Fang & Ke, 2022. "Single-cell transcriptome and translatome dual-omics reveals potential mechanisms of human oocyte maturation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Iva Salamon & Yongkyu Park & Terezija Miškić & Janja Kopić & Paul Matteson & Nicholas F. Page & Alfonso Roque & Geoffrey W. McAuliffe & John Favate & Marta Garcia-Forn & Premal Shah & Miloš Judaš & Ja, 2023. "Celf4 controls mRNA translation underlying synaptic development in the prenatal mammalian neocortex," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

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