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Molecular biology and evolution
08 03, 2023;40 (8):

Integrative Omics Reveals Rapidly Evolving Regulatory Sequences Driving Primate Brain Evolution.

Xiao-Lin Zhuang, Jin-Jin Zhang, Yong Shao, Yaxin Ye, Chun-Yan Chen, Long Zhou, Zheng-Bo Wang, Xin Luo, Bing Su, Yong-Gang Yao, David N Cooper, Ben-Xia Hu, Lu Wang, Xiao-Guang Qi, Jiangwei Lin, Guo-Jie Zhang, Wen Wang, Nengyin Sheng, Dong-Dong Wu
Author Information
  1. Xiao-Lin Zhuang: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  2. Jin-Jin Zhang: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  3. Yong Shao: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. ORCID
  4. Yaxin Ye: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  5. Chun-Yan Chen: School of Ecology and Environment, Northwestern Polytechnical University, Xi'an, Shaanxi, China.
  6. Long Zhou: Center for Evolutionary & Organismal Biology, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.
  7. Zheng-Bo Wang: Yunnan Key Laboratory of Primate Biomedicine Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan, China.
  8. Xin Luo: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  9. Bing Su: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. ORCID
  10. Yong-Gang Yao: Kunming College of Life Science, University of the Chinese Academy of Sciences, Kunming, Yunnan, China. ORCID
  11. David N Cooper: Institute of Medical Genetics, School of Medicine, Cardiff University, Cardiff, Wales, UK.
  12. Ben-Xia Hu: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  13. Lu Wang: College of Life Sciences, Northwest University, Xi'an, Shaanxi, China.
  14. Xiao-Guang Qi: College of Life Sciences, Northwest University, Xi'an, Shaanxi, China.
  15. Jiangwei Lin: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  16. Guo-Jie Zhang: Center of Evolutionary & Organismal Biology, and Women's Hospital at Zhejiang University School of Medicine, Hangzhou, Guangdong, China.
  17. Wen Wang: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  18. Nengyin Sheng: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
  19. Dong-Dong Wu: State Key Laboratory of Genetic Resources and Evolution, Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China. ORCID
PMID: 37494289 DOI: 10.1093/molbev/msad173

Abstract

Although the continual expansion of the brain during primate evolution accounts for our enhanced cognitive capabilities, the drivers of brain evolution have scarcely been explored in these ancestral nodes. Here, we performed large-scale comparative genomic, transcriptomic, and epigenomic analyses to investigate the evolutionary alterations acquired by brain genes and provide comprehensive listings of innovatory genetic elements along the evolutionary path from ancestral primates to human. The regulatory sequences associated with brain-expressed genes experienced rapid change, particularly in the ancestor of the Simiiformes. Extensive comparisons of single-cell and bulk transcriptomic data between primate and nonprimate brains revealed that these regulatory sequences may drive the high expression of certain genes in primate brains. Employing in utero electroporation into mouse embryonic cortex, we show that the primate-specific brain-biased gene BMP7 was recruited, probably in the ancestor of the Simiiformes, to regulate neuronal proliferation in the primate ventricular zone. Our study provides a comprehensive listing of genes and regulatory changes along the brain evolution lineage of ancestral primates leading to human. These data should be invaluable for future functional studies that will deepen our understanding not only of the genetic basis of human brain evolution but also of inherited disease.

Keywords

brain evolution omics primate regulatory sequences

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MeSH Term

Mice
Humans
Animals
Primates
Brain
Evolution, Molecular
Journal Article Research Support, Non-U.S. Gov't

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