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Transcription factor binding sites are frequently under accelerated evolution in primates

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  • Xinru Zhang

    (Pennsylvania State University
    Pennsylvania State University
    Pennsylvania State University)

  • Bohao Fang

    (Harvard University)

  • Yi-Fei Huang

    (Pennsylvania State University
    Pennsylvania State University)

Abstract

Recent comparative genomic studies have identified many human accelerated elements (HARs) with elevated substitution rates in the human lineage. However, it remains unknown to what extent transcription factor binding sites (TFBSs) are under accelerated evolution in humans and other primates. Here, we introduce two pooling-based phylogenetic methods with dramatically enhanced sensitivity to examine accelerated evolution in TFBSs. Using these new methods, we show that more than 6000 TFBSs annotated in the human genome have experienced accelerated evolution in Hominini, apes, and Old World monkeys. Although these TFBSs individually show relatively weak signals of accelerated evolution, they collectively are more abundant than HARs. Also, we show that accelerated evolution in Pol III binding sites may be driven by lineage-specific positive selection, whereas accelerated evolution in other TFBSs might be driven by nonadaptive evolutionary forces. Finally, the accelerated TFBSs are enriched around developmental genes, suggesting that accelerated evolution in TFBSs may drive the divergence of developmental processes between primates.

Suggested Citation

  • Xinru Zhang & Bohao Fang & Yi-Fei Huang, 2023. "Transcription factor binding sites are frequently under accelerated evolution in primates," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36421-3
    DOI: 10.1038/s41467-023-36421-3
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    1. Katherine S. Pollard & Sofie R. Salama & Nelle Lambert & Marie-Alexandra Lambot & Sandra Coppens & Jakob S. Pedersen & Sol Katzman & Bryan King & Courtney Onodera & Adam Siepel & Andrew D. Kern & Cole, 2006. "An RNA gene expressed during cortical development evolved rapidly in humans," Nature, Nature, vol. 443(7108), pages 167-172, September.
    2. Yongbin Wei & Siemon C. de Lange & Lianne H. Scholtens & Kyoko Watanabe & Dirk Jan Ardesch & Philip R. Jansen & Jeanne E. Savage & Longchuan Li & Todd M. Preuss & James K. Rilling & Danielle Posthuma , 2019. "Genetic mapping and evolutionary analysis of human-expanded cognitive networks," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    3. Wolfgang Enard & Molly Przeworski & Simon E. Fisher & Cecilia S. L. Lai & Victor Wiebe & Takashi Kitano & Anthony P. Monaco & Svante Pääbo, 2002. "Molecular evolution of FOXP2, a gene involved in speech and language," Nature, Nature, vol. 418(6900), pages 869-872, August.
    4. Bas Castelijns & Mirna L. Baak & Ilia S. Timpanaro & Caroline R. M. Wiggers & Marit W. Vermunt & Peng Shang & Ivanela Kondova & Geert Geeven & Valerio Bianchi & Wouter Laat & Niels Geijsen & Menno P. , 2020. "Hominin-specific regulatory elements selectively emerged in oligodendrocytes and are disrupted in autism patients," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    5. Kerstin Lindblad-Toh & Manuel Garber & Or Zuk & Michael F. Lin & Brian J. Parker & Stefan Washietl & Pouya Kheradpour & Jason Ernst & Gregory Jordan & Evan Mauceli & Lucas D. Ward & Craig B. Lowe & Al, 2011. "A high-resolution map of human evolutionary constraint using 29 mammals," Nature, Nature, vol. 478(7370), pages 476-482, October.
    6. Nick G. C. Smith & Adam Eyre-Walker, 2002. "Adaptive protein evolution in Drosophila," Nature, Nature, vol. 415(6875), pages 1022-1024, February.
    7. Su Yeon Kim & Jonathan K Pritchard, 2007. "Adaptive Evolution of Conserved Noncoding Elements in Mammals," PLOS Genetics, Public Library of Science, vol. 3(9), pages 1-15, September.
    8. Cecilia S. L. Lai & Simon E. Fisher & Jane A. Hurst & Faraneh Vargha-Khadem & Anthony P. Monaco, 2001. "A forkhead-domain gene is mutated in a severe speech and language disorder," Nature, Nature, vol. 413(6855), pages 519-523, October.
    9. Miler T. Lee & Ashley R. Bonneau & Carter M. Takacs & Ariel A. Bazzini & Kate R. DiVito & Elizabeth S. Fleming & Antonio J. Giraldez, 2013. "Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition," Nature, Nature, vol. 503(7476), pages 360-364, November.
    10. Jianlong Wang & Sridhar Rao & Jianlin Chu & Xiaohua Shen & Dana N. Levasseur & Thorold W. Theunissen & Stuart H. Orkin, 2006. "A protein interaction network for pluripotency of embryonic stem cells," Nature, Nature, vol. 444(7117), pages 364-368, November.
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