The emergence of Sox and POU transcription factors predates the origins of animal stem cells

Ya Gao, Daisylyn Senna Tan, Mathias Girbig, Haoqing Hu, Xiaomin Zhou, Qianwen Xie, Shi Wing Yeung, Kin Shing Lee, Sik Yin Ho, Vlad Cojocaru, Jian Yan, Georg K. A. Hochberg, Alex Mendoza () and Ralf Jauch ()
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Ya Gao: The University of Hong Kong
Daisylyn Senna Tan: The University of Hong Kong
Mathias Girbig: Max Planck Institute for Terrestrial Microbiology
Haoqing Hu: The University of Hong Kong
Xiaomin Zhou: City University of Hong Kong
Qianwen Xie: City University of Hong Kong
Shi Wing Yeung: The University of Hong Kong
Kin Shing Lee: The University of Hong Kong
Sik Yin Ho: The University of Hong Kong
Vlad Cojocaru: Babeş-Bolyai University
Jian Yan: City University of Hong Kong
Georg K. A. Hochberg: Max Planck Institute for Terrestrial Microbiology
Alex Mendoza: Queen Mary University of London
Ralf Jauch: The University of Hong Kong

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Stem cells are a hallmark of animal multicellularity. Sox and POU transcription factors are associated with stemness and were believed to be animal innovations, reported absent in their unicellular relatives. Here we describe unicellular Sox and POU factors. Choanoflagellate and filasterean Sox proteins have DNA-binding specificity similar to mammalian Sox2. Choanoflagellate—but not filasterean—Sox can replace Sox2 to reprogram mouse somatic cells into induced pluripotent stem cells (iPSCs) through interacting with the mouse POU member Oct4. In contrast, choanoflagellate POU has a distinct DNA-binding profile and cannot generate iPSCs. Ancestrally reconstructed Sox proteins indicate that iPSC formation capacity is pervasive among resurrected sequences, thus loss of Sox2-like properties fostered Sox family subfunctionalization. Our findings imply that the evolution of animal stem cells might have involved the exaptation of a pre-existing set of transcription factors, where pre-animal Sox was biochemically similar to extant Sox, whilst POU factors required evolutionary innovations.

Date: 2024
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DOI: 10.1038/s41467-024-54152-x

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