Evolutionarily Ancient Association of the FoxJ1 Transcription Factor with the Motile Ciliogenic Program

• DOI: 10.1371/journal.pgen.1003019
• Publication Date: 2012-11-08T21:57:55Z
• Authors: Shubha Vij; Jochen C. Rink; Hao Kee Ho; Deepak Babu; Michael Eitel; Vijayashankaranar...; Varnesh Tiku; Jody Westbrook; Bernd Schierwater; Sudipto Roy
• Keywords: cell migration; QH426-470; phylogeny; eukaryotic cell; Cell Movement; zebra fish; Morphogenesis; Developmental; genetic conservation; transcription factor; Zebrafish; Strongylocentrotus; 0303 health sciences; ciliary motility; article; Eukaryota; Gene Expression Regulation, Developmental; Cell Differentiation; Forkhead Transcription Factors; Biological Evolution; unclassified drug; :Science::Biological sciences [DRNTU]; gene inactivation; Vertebrates; transcription regulation; transcription factor FoxJ1 gene; Research Article; 570; embryo; 610; platyhelminth; 03 medical and health sciences; Genetics; Animals; controlled study; human; Cilia; DRNTU::Science::Biological sciences; gene; mouse; Vertebrata; Schmidtea mediterranea; nonhuman; Danio rerio; Metazoa; nucleotide sequence; Zebrafish Proteins; biogenesis; cell differentiation; transcription factor FoxJ1; Opisthokonta; Gene Expression Regulation; protein analysis; molecular genetics; Platyhelminthes; last common ancestor

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.