DINE-1, the highest copy number repeats in Drosophila melanogaster are non-autonomous endonuclease-encoding rolling-circle transposable elements (Helentrons)

BACKGROUND: The Drosophila INterspersed Elements-1 (DINE-1/INE1) transposable elements (TEs) are the most abundant component of the Drosophila melanogaster genome and have been associated with functional gene duplications. DINE-1 TEs do not encode any proteins (non-autonomous) thus are moved by autonomous partners. The identity of the autonomous partners has been a mystery. They have been allied to Helitrons (rolling-circle transposons), MITEs (DNA transposons), and non-LTR retrotransposons by different authors. RESULTS: We report multiple lines of bioinformatic evidence that illustrate the relationship of DINE-1 like TEs to endonuclease-encoding rolling-circle TEs (Helentrons). The structural features of Helentrons are described, which resemble the organization of the non-autonomous partners, but differ significantly from canonical Helitrons. In addition to the presence of an endonuclease domain fused to the Rep/Helicase protein, Helentrons have distinct structural features. Evidence is presented that illustrates that Helentrons are widely distributed in invertebrate, fish, and fungal genomes. We describe an intermediate family from the Phytophthora infestans genome that phylogenetically groups with Helentrons but that displays Helitron structure. In addition, evidence is presented that Helentrons can capture gene fragments in a pattern reminiscent of canonical Helitrons. CONCLUSIONS: We illustrate the relationship of DINE-1 and related TE families to autonomous partners, the Helentrons. These findings will allow their proper classification and enable a more accurate understanding of the contribution of rolling-circle transposition to the birth of new genes, gene networks, and genome composition.