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Abstract

Transposable elements (TEs) can be co-opted for novel biological functions. One evolutionary path to TE co-option is the capture of TE-derived protein-coding sequences by an endogenous gene, resulting in fusion proteins that may evolve new gene regula- tory functions. We identified a Mariner transposase helix-turn-helix (HTH) DNA-binding domain that was captured in the Caenor- habditis genus by a subset of F-box genes, which we refer to as fbxa-hth genes. The origin of fbxa-hth genes likely occurred through a single capture event in the ancestor of the Elegans group, followed by an increase in copy number. We focused on fbxa-215, a fbxa-hth gene which is highly expressed in the germline and embryos and localizes to germ granules in embryos. In-frame deletion of the HTH domain of fbxa-215 uncovered a fully penetrant egg-laying defect, highlighting the importance of this domain. In fact, while their F-box domains are evolving rapidly, the HTH domains of fbxa-hth genes display signatures of purifying selection, indicating functional constraints. Quantitative proteomics shows interactions between FBXA-215 and factors associated with E3 ubiquitin ligase complexes, proteasome, and stress response, suggesting a function in proteostasis, consistent with previously described roles of other F-box proteins. The TE-derived HTH domain of FBXA-215 interacts with proteins required for translation and stress response, indicating that the HTH domain was repurposed to bind additional protein substrates. We observe TE enrichment in proximity to F-box genes in the Caenorhabditis genus, suggesting that abundant neighbouring TEs may have provided opportunity for the HTH capture and facilitated subsequent integration of fbxa-hth genes into existing cis- regulatory networks. fbxa-215 has upstream Helitron TEs that modulate its expression upon heat-shock, via Heat-shock factor 1 (HSF-1). Consistent with integration in a heat-shock network, fbxa-215 mutants display higher tolerance to elevated temperature than wild-type animals. We found and validated additional instances of TE and viral sequences captured by F-box genes across the eukaryotic tree-of-life, predominantly in plants. Overall, these findings demonstrate recurring TE/F-box gene fusions that potentially fuel novel forms of gene regulation in eukaryotes.