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An RFX transcription factor regulated ciliogenesis in the progenitors of choanoflagellates and animals

Maxwell C. Coyle, Adia M. Tajima, Fredrick Leon, View ORCID ProfileSemil P. Choksi, Ally Yang, Sarah Espinoza, View ORCID ProfileTimothy R. Hughes, View ORCID ProfileJeremy F. Reiter, David S. Booth, View ORCID ProfileNicole King
doi: https://doi.org/10.1101/2022.11.11.515474
Maxwell C. Coyle
1Department of Molecular and Cell Biology, University of California, Berkeley, CA, 94720
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Adia M. Tajima
1Department of Molecular and Cell Biology, University of California, Berkeley, CA, 94720
2Howard Hughes Medical Institute, United States
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Fredrick Leon
3Department of Biochemistry and Biophysics, University of California, San Francisco, CA, 94158
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Semil P. Choksi
3Department of Biochemistry and Biophysics, University of California, San Francisco, CA, 94158
4Cardiovascular Research Institute, University of California, San Francisco, CA, 94158
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  • ORCID record for Semil P. Choksi
Ally Yang
6Donnelly Centre for Cellular and Biomolecular Research, Toronto, Canada, M5S 3E1
7Department of Molecular Genetics, University of Toronto, Canada, M5S 3E1
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Sarah Espinoza
1Department of Molecular and Cell Biology, University of California, Berkeley, CA, 94720
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Timothy R. Hughes
6Donnelly Centre for Cellular and Biomolecular Research, Toronto, Canada, M5S 3E1
7Department of Molecular Genetics, University of Toronto, Canada, M5S 3E1
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Jeremy F. Reiter
3Department of Biochemistry and Biophysics, University of California, San Francisco, CA, 94158
4Cardiovascular Research Institute, University of California, San Francisco, CA, 94158
8Chan Zuckerberg Biohub, San Francisco, CA, 94158
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David S. Booth
3Department of Biochemistry and Biophysics, University of California, San Francisco, CA, 94158
8Chan Zuckerberg Biohub, San Francisco, CA, 94158
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Nicole King
1Department of Molecular and Cell Biology, University of California, Berkeley, CA, 94720
2Howard Hughes Medical Institute, United States
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  • For correspondence: nking@berkeley.edu
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Abstract

Little is known about the origins of the transcriptional modules that coordinate cell-type specific functions in animals. The controlled expression of one cellular feature – the cilium – was likely critical during early animal evolution. Two key transcription factors, RFX and FoxJ1, coordinate ciliogenesis in animals but are absent from the genomes of most other ciliated eukaryotes, raising the question of how the transcriptional regulation of ciliogenesis has evolved. To reconstruct the evolution of the RFX/FoxJ1 transcriptional module and its role in the regulation of ciliogenesis, we investigated RFX and FoxJ1 function in one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta. Targeted disruption of the S. rosetta RFX homolog cRFXa resulted in delayed cell proliferation and aberrant ciliogenesis, marked by the collapse and resorption of nascent cilia. Ciliogenesis genes and foxJ1 were significantly down-regulated in cRFXa mutants, consistent with a pre-animal ancestry for this transcriptional module. We also found that cRFXa protein preferentially binds to a sequence motif that is enriched in the promoters of S. rosetta ciliary genes and matches the sequence motif bound by animal RFX proteins. These findings suggest that RFX coordinated ciliogenesis before the divergence of animals and choanoflagellates, and that the deployment of this module may have provided a mechanism to differentiate ciliated and non-ciliated cell types in early animal evolution.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted November 14, 2022.
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An RFX transcription factor regulated ciliogenesis in the progenitors of choanoflagellates and animals
Maxwell C. Coyle, Adia M. Tajima, Fredrick Leon, Semil P. Choksi, Ally Yang, Sarah Espinoza, Timothy R. Hughes, Jeremy F. Reiter, David S. Booth, Nicole King
bioRxiv 2022.11.11.515474; doi: https://doi.org/10.1101/2022.11.11.515474
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An RFX transcription factor regulated ciliogenesis in the progenitors of choanoflagellates and animals
Maxwell C. Coyle, Adia M. Tajima, Fredrick Leon, Semil P. Choksi, Ally Yang, Sarah Espinoza, Timothy R. Hughes, Jeremy F. Reiter, David S. Booth, Nicole King
bioRxiv 2022.11.11.515474; doi: https://doi.org/10.1101/2022.11.11.515474

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