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A host-co-opted Harbinger transposase engages multiple trihelix DNA-binding factors and controls pleiotropic phenotypes

ABSTRACT: Transposase domestication is a recurring theme in eukaryotic genome evolution, yet it remains unresolved whether transposase-derived proteins can be co-opted to assemble multi-partner regulatory modules with phenotypic consequences. Here we show that a PIF/Harbinger-derived protein, HDP3, associates with multiple trihelix DNA-binding factors across tissues in Arabidopsis thaliana, and that these associations are modulated by abscisic acid (ABA). Genetic studies indicate that HDP3 and a representative trihelix partner act together in promoting germination and intersect with ABA signaling to influence seedling establishment, but diverge in their contributions to leaf development and flowering time. Transcriptome profiling reveals largely overlapping regulatory effects with concordant transcriptional directionality for both induced and repressed gene sets, while highlighting a notable exception at FLOWERING LOCUS C consistent with differential timing of the vegetative-to-reproductive transition. Together, these findings suggest that HDP3 supports context-dependent transcriptional outputs – likely via dynamic partnering with these trihelix factors – thereby contributing to pleiotropic developmental outcomes.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE322771 | GEO | 2026/08/08

REPOSITORIES: GEO

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Project description:Proteins encoded by transposable elements (TEs) play a vital role in their proliferation in host genomes. In recent years, an increasing number of studies have shown that TE proteins have contributed to the emergence of novel host proteins. In Drosophila, there are several proteins derived from the PIF/Harbinger transposase superfamily called Drosophila PIF Like Genes (DPLGs). Here, we investigated the function of four DPLGs (DPLG1-4) in D. melanogaster that are highly conserved and present across Drosophila but are deeply diverged from each other, and likely originated through independent domestication of the transposase from distinct PIF-like TE families. We have analyzed transcript localization of DPLG 1-4, tagged DPLG3 and DPLG4 and studied their protein localization and, produced null alleles for DPLG1 and DPLG4. RNA in situ hybridization reveals that DPLG1-4 have strikingly similar pattern of transcript localization in the gonads, and in the nervous system during embryogenesis, suggesting their domestication for related functions. DPLGs show co-expression enrichment with transcription factors in ovaries and during embryogenesis supporting that they may be domesticated as regulatory proteins in flies. DPLG3 and DPLG4 tagged proteins localize with DNA in the nucleus of the ovaries consistent with this hypothesis. Loss of DPLG1 or DPLG4 results in viability and/or fertility effects, while loss of both DPLG1 and DPLG4 resulted in no effect in viability or fertility suggesting genetic interaction between these two genes. Further, loss of DPLG4 showed increased survival in flies, and increased fertility in older females indicating its involvement in the process of ageing. Transcriptional analyses in the ovaries showed that the loss of either DPLG1 or DPLG4 protein leads to modest changes in transcription of a large and significantly overlapping set of genes, and also affects transposable elements activity. The observed functional overlap of independently domesticated transposases from the same TE family and genetic interaction between them suggests a stepping stone model in which domestication of a PIF/Harbinger transposase might promote the domestication of related transposases for gonad and nervous system regulatory functions.

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A host-co-opted Harbinger transposase engages multiple trihelix DNA-binding factors and controls pleiotropic phenotypes

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