TY - JOUR
T1 - Evolution of translational control and the emergence of genes and open reading frames in human and non-human primate hearts
AU - Ruiz-Orera, Jorge
AU - Miller, Duncan C
AU - Greiner, Johannes
AU - Genehr, Carolin
AU - Grammatikaki, Aliki
AU - Blachut, Susanne
AU - Mbebi, Jeanne
AU - Patone, Giannino
AU - Myronova, Anna
AU - Adami, Eleonora
AU - Dewani, Nikita
AU - Liang, Ning
AU - Hummel, Oliver
AU - Muecke, Michael B
AU - Hildebrandt, Thomas B
AU - Fritsch, Guido
AU - Schrade, Lisa
AU - Zimmermann, Wolfram H
AU - Kondova, Ivanela
AU - Diecke, Sebastian
AU - van Heesch, Sebastiaan
AU - Hübner, Norbert
N1 - © 2024. The Author(s).
PY - 2024/10
Y1 - 2024/10
N2 - Evolutionary innovations can be driven by changes in the rates of RNA translation and the emergence of new genes and small open reading frames (sORFs). In this study, we characterized the transcriptional and translational landscape of the hearts of four primate and two rodent species through integrative ribosome and transcriptomic profiling, including adult left ventricle tissues and induced pluripotent stem cell-derived cardiomyocyte cell cultures. We show here that the translational efficiencies of subunits of the mitochondrial oxidative phosphorylation chain complexes IV and V evolved rapidly across mammalian evolution. Moreover, we discovered hundreds of species-specific and lineage-specific genomic innovations that emerged during primate evolution in the heart, including 551 genes, 504 sORFs and 76 evolutionarily conserved genes displaying human-specific cardiac-enriched expression. Overall, our work describes the evolutionary processes and mechanisms that have shaped cardiac transcription and translation in recent primate evolution and sheds light on how these can contribute to cardiac development and disease.
AB - Evolutionary innovations can be driven by changes in the rates of RNA translation and the emergence of new genes and small open reading frames (sORFs). In this study, we characterized the transcriptional and translational landscape of the hearts of four primate and two rodent species through integrative ribosome and transcriptomic profiling, including adult left ventricle tissues and induced pluripotent stem cell-derived cardiomyocyte cell cultures. We show here that the translational efficiencies of subunits of the mitochondrial oxidative phosphorylation chain complexes IV and V evolved rapidly across mammalian evolution. Moreover, we discovered hundreds of species-specific and lineage-specific genomic innovations that emerged during primate evolution in the heart, including 551 genes, 504 sORFs and 76 evolutionarily conserved genes displaying human-specific cardiac-enriched expression. Overall, our work describes the evolutionary processes and mechanisms that have shaped cardiac transcription and translation in recent primate evolution and sheds light on how these can contribute to cardiac development and disease.
KW - Animals
KW - Humans
KW - Open Reading Frames/genetics
KW - Protein Biosynthesis/genetics
KW - Evolution, Molecular
KW - Myocytes, Cardiac/metabolism
KW - Species Specificity
KW - Transcriptome
KW - Gene Expression Profiling/methods
KW - Induced Pluripotent Stem Cells/metabolism
KW - Ribosomes/metabolism
KW - Primates/genetics
KW - Cells, Cultured
U2 - 10.1038/s44161-024-00544-7
DO - 10.1038/s44161-024-00544-7
M3 - Article
C2 - 39317836
SN - 2731-0590
VL - 3
SP - 1217
EP - 1235
JO - Nature cardiovascular research
JF - Nature cardiovascular research
IS - 10
ER -