Evolutionarily Ancient Association of the FoxJ1 Transcription Factor with the Motile Ciliogenic Program
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It is generally believed that the last eukaryotic common ancestor (LECA) was a unicellular organism with motile cilia. In the vertebrates, the winged-helix transcription factor FoxJ1 functions as the master regulator of motile cilia biogenesis. Despite the antiquity of cilia, their highly conserved structure, and their mechanism of motility, the evolution of the transcriptional program controlling ciliogenesis has remained incompletely understood. In particular, it is presently not known how the generation of motile cilia is programmed outside of the vertebrates, and whether and to what extent the FoxJ1-dependent regulation is conserved. We have performed a survey of numerous eukaryotic genomes and discovered that genes homologous to foxJ1 are restricted only to organisms belonging to the unikont lineage. Using a mis-expression assay, we then obtained evidence of a conserved ability of FoxJ1 proteins from a number of diverse phyletic groups to activate the expression of a host of motile ciliary genes in zebrafish embryos. Conversely, we found that inactivation of a foxJ1 gene in Schmidtea mediterranea, a platyhelminth (flatworm) that utilizes motile cilia for locomotion, led to a profound disruption in the differentiation of motile cilia. Together, all of these findings provide the first evolutionary perspective into the transcriptional control of motile ciliogenesis and allow us to propose a conserved FoxJ1-regulated mechanism for motile cilia biogenesis back to the origin of the metazoans.
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The evolutionary divergence of mucociliary cell types in metazoans appears closely linked to the diversification of the Fox gene family.
“At the molecular level, the evolutionary divergence of mucociliary cell types in metazoans appears to be closely linked to the diversification of the Fox gene family.”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [72]
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- Authors
- Vij, S., Rink, J. C., Ho, H. K., Babu, D., Eitel, M., Narasimhan, V., Tiku, V., Westbrook, J., Schierwater, B., & Roy, S.
- Affiliations
- Institute of Molecular and Cell Biology (SG)
- Max Planck Institute of Molecular Cell Biology and Genetics (DE)
- National University of Singapore (SG)
- University of Veterinary Medicine Hannover, Foundation (DE)
- University of California, Berkeley (US)
- Corresponding author
- Roy, Sudipto
- ORCID
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-11-08
- Volume
- 8
- Issue
- 11
- Pages
- e1003019
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3493443
- OpenAlex
- W2076961729
- Cited by
- 65
- References
- 54
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 2 · 2023: 11 · 2022: 7 · 2021: 6 · 2020: 5 · 2019: 1 · 2018: 7 · 2017: 4 · 2016: 2 · 2015: 4 · 2014: 7
- FWCI
- 2.12
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DR-NTU (Nanyang Technological University) (submittedVersion)
- National University of Singapore (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Figshare (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Agency for Science, Technology and Research
- Institute of Molecular and Cell Biology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- Foxj1, cilia biogenesis, transcription factor evolution, last eukaryotic common ancestor, Schmidtea mediterranea, Platyhelminthes, zebrafish, metazoan origin, gene misexpression, ciliary genes
- MeSH terms
- Animals, Cell Differentiation, Cell Movement, Cilia, Biological Evolution, Morphogenesis, Vertebrates, Zebrafish, Gene Expression Regulation, Developmental, Zebrafish Proteins, Forkhead Transcription Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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