Origin and Evolution of Plant Long Terminal Repeat Retrotransposons with Additional Ribonuclease H

Retroviruses originated from long terminal repeat retrotransposons (LTR-RTs) through several structural adaptations. One such modification was the arrangement of an additional ribonuclease H (aRH) domain next to native RH, followed by degradation and subfunctionalization of the latter. We previously showed that this retrovirus-like structure independently evolved in Tat LTR-RTs in flowering plants, proposing its origin from sequential rearrangements of ancestral Tat structures identified in lycophytes and conifers. However, most nonflowering plant genome assemblies were not available at that time, therefore masking the history of aRH acquisition by Tat and challenging our hypothesis. Here, we revisited Tat's evolution scenario upon the aRH acquisition by covering most of the extant plant phyla. We show that Tat evolved and obtained aRH in an ancestor of land plants. Importantly, we found the retrovirus-like structure in clubmosses, hornworts, ferns, and gymnosperms, suggesting its ancient origin, broad propagation, and yet-to-be-understood benefit for the LTR-RTs’ adaptation.