An RFX transcription factor regulates ciliogenesis in the closest living relatives of animals

Coyle, Maxwell C.; Tajima, Adia M.; Leon, Fredrick; Choksi, Semil P.; Yang, Ally; Espinoza, Sarah M.; Hughes, Timothy R.; Reiter, Jeremy F.; Booth, David S.; King, Nicole

doi:10.1016/j.cub.2023.07.022

Cited by 7 publications

(10 citation statements)

References 97 publications

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Section: Rfxmentioning

confidence: 65%

“…Systematic surveys comparing TF specificities between animals and their closest relatives have not been published. Thus far, the binding specificities of only a few TFs have been compared between animals and their close relatives: Myc:Max [41], RFX [42] and T-box [43]. In all cases, the DNAbinding specificities were almost identical in animal and non-animal orthologs (Figure 2B).…”

Section: Animals Origins Likely Did Not See a Diversification Of Tf B...mentioning

confidence: 97%

“…Animal RFX TFs regulate ciliogenesis target genes by binding to the recognition site GTTRCY (Figure 2B) [94]. Notably, RFX TFs are not found in most eukaryotes (many of which bear cilia), being restricted to opisthokonts and amoebozoans [42,91,95]. Ascomycete fungi, which lack cilia, use RFX TFs to regulate DNA damage repair and the cell cycle [96][97][98] (Figure 4D)…”

Section: Rfxmentioning

confidence: 99%

“…Recent work explored the function of RFX TFs in the choanoflagellate Salpingoeca rosetta, revealing a conserved (and therefore pre-animal) regulatory link between RFX and ciliogenesis genes [42]. This study also showed that the RFX TF family expanded from one to three members on the choanozoan stem lineage, which may have coincided with its acquisition of a role in regulating ciliogenesis [42]. Interestingly, one specific sub-family that resulted from this duplication is responsible for almost all published reports of RFX regulating ciliogenesis, in both animals and now choanoflagellates [42,91,99].…”

Section: Rfxmentioning

confidence: 99%

“…For instance, RFX2 in mammals specifically controls ciliary gene expression in spermatogenesis [100], while RFX3 controls ciliary gene expression in other tissues [101]. RFX1, on the other hand, is embryonic lethal in mice [102], and may have retained a cell cycle function that may be as ancient as opisthokonts, given the role of RFX in cell cycle regulation in fungi [103] and the growth defect observed in an RFX knockout in choanoflagellates [42]. Functional specificity may be driven by differences among family members in protein-protein interactions.…”

Section: Rfxmentioning

confidence: 99%

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The Evolutionary Foundations of Animal Transcriptional Regulatory Mechanisms

Coyle,

King

2024

Preprint

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Animals are distinguished by their complex developmental programs, in which transcription factors play essential roles in coordinating the regulation of the genome. Thus, it has been hypothesized that animal origins involved the evolution of increasingly complex transcriptional regulatory mechanisms that permit greater spatiotemporal control over gene expression. Here, we revisit this hypothesis in light of new genomic and functional data from diverse phylogenetically-relevant taxa, including early branching animals (sponges, ctenophores) and close relatives of animals (choanoflagellates, filastereans, ichthyosporeans). We argue that many of the mechanisms posited to explain animal transcriptional complexity, such as large increases in transcription factor numbers, new transcription factor families, and distal enhancers, did not factor significantly into animal origins. Instead, we propose that the re-purposing of pre-existing transcriptional regulatory modules through cis-regulatory evolution and gene duplication events, combined with new protein-protein interactions among TFs, may have been fundamental to the transcriptional regulatory architecture of the first animals.

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Section: Rfxmentioning

confidence: 65%