Transcriptome and translatome co-evolution in mammals

Zhong-Yi Wang, Evgeny Leushkin (), Angélica Liechti, Svetlana Ovchinnikova, Katharina Mößinger, Thoomke Brüning, Coralie Rummel, Frank Grützner, Margarida Cardoso-Moreira, Peggy Janich, David Gatfield, Boubou Diagouraga, Bernard Massy, Mark E. Gill, Antoine H. F. M. Peters, Simon Anders and Henrik Kaessmann ()
Additional contact information
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
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
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

Nature, 2020, vol. 588, issue 7839, 642-647

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-2899-z

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