Rolling‐circle amplification of centromeric Helitrons in plant genomes

Summary The unusual eukaryotic Helitron transposons can readily capture host sequences and are, thus, evolutionarily important. They are presumed to amplify by rolling‐circle replication (RCR) because some elements encode predicted proteins homologous to RCR prokaryotic transposases. In support of this replication mechanism, it was recently shown that transposition of a bat Helitron generates covalently closed circular intermediates. Another strong prediction is that RCR should generate tandem Helitron concatemers, yet almost all Helitrons identified to date occur as solo elements in the genome. To investigate alternative modes of Helitron organization in present‐day genomes, we have applied the novel computational tool HelitronScanner to 27 plant genomes and have uncovered numerous tandem arrays of partially decayed, truncated Helitrons in all of them. Strikingly, most of these Helitron tandem arrays are interspersed with other repeats in centromeres. Many of these arrays have multiple Helitron 5′ ends, but a single 3′ end. The number of repeats in any one array can range from a handful to several hundreds. We propose here an RCR model that conforms to the present Helitron landscape of plant genomes. Our study provides strong evidence that plant Helitrons amplify by RCR and that the tandemly arrayed replication products accumulate mostly in centromeres. Significance Statement Helitron transposons can capture gene fragments and move them around the genome and thus have played an important role in shaping eukaryotic genomes, but their mode of transposition was unclear. Here we used an automated computational tool that enabled the discovery of a large cache of previously overlooked Helitrons in many genomes. We propose a rolling‐circle replication model that accounts for the different Helitron distributions found in current plant genomes. As many tandem array Helitrons locate preferentially to centromeres, we suggest that they might have contributed to the growth of plant centromeres.