Evolution of transposons as controlling elements

Abstract

Transposons were originally described as controlling elements, yet the molecular basis and evolutionary origin of their transcriptional regulatory activities remain elusive. Here, we show that transcriptional regulatory activity is an intrinsic property of transposases (TPases). We demonstrate that the Arabidopsis AtMu1 TPase is sufficient to induce sequence-specific transcriptional activation of cognate copies, revealing a pre-existing cis-regulatory network. We further demonstrate that long-recognized Spm transposon-encoded transcriptional regulator TnpA evolved from an ancestral TPase, linking transcriptional regulators to TPases. Across eukaryotes, we identify multiple domesticated TPase-derived proteins that recurrently lack catalytic residues for transposition, consistent with a one-step regulatory co-option through loss of catalytic activity. Together, our results reveal TPases as autonomous sequence-specific transcriptional regulators and provide a direct evolutionary route from TPases to transcription factors.