Deciphering the dynamics of active autonomous terminal inverted repeat transposons in the plant kingdom

Terminal inverted repeat (TIR) transposons are powerful drivers of genome evolution. However, a comprehensive understanding of their recent, lineage-specific activity across the plant kingdom has remained elusive. In this study, we developed a data-distillation pipeline to systematically identify recently active autonomous TIR transposons in 1007 plant genomes. Our analysis identified 3203 active clusters. The vast majority (93.3 ​%) of these clusters are maintained at low copy numbers, which suggests that robust host-mediated regulation restricts excessive proliferation. These TIR transposons exhibit striking heterogeneity and predominantly lineage-restricted diversification, with functional extinction being a common fate of TIR transposons across the plant kingdom. Among the identified active clusters, the Mutator-like element (MULE) superfamily was the most prevalent, accounting for 57.6 ​% of all TIR clusters. Furthermore, we uncovered extensive, previously uncharacterized intraspecific diversity through a genome analysis of four crop species, suggesting that single reference genomes substantially underestimate transposon dynamics. When we examined the molecular innovations that enable transposon success, we observed that MULE-encoded transposases possessed hypervariable termini that interact with accessory proteins. Using the hyperactive maize (Zea mays) MuDR element as a model, we obtained direct in vivo and in vitro evidence of an interaction between the transposase MURA and the accessory protein MURB, mapping the critical binding site to the N terminus of MURA. This atlas offers critical insights into transposon-host coevolution and provides a rich, species-specific toolkit for plant biotechnology.