Helitrons in Drosophila: Chromatin modulation and tandem insertions

Abstract

Although Helitrons were discovered 15 y ago, they still represent an elusive group of transposable elements (TEs). They are thought to transpose via a rolling-circle mechanism, but no transposition assay has yet been conducted. We have recently characterized a group of Helitrons in Drosophila, named DINE-TR1, that display interesting features, including pronounced enrichment at β-heterochromatin, multiple tandem insertions (TIs) of the entire TE, and that experienced at least 2 independent expansion events of its internal tandem repeats (TRs) in distant Drosophila lineages. Here we discuss 2 aspects of TE dynamics displayed by the DINE-TR1 Helitrons: (i) the general evolutionary impact of piRNA-guided heterochromatin formation via TE-derived TR expansion and (ii) the possible mechanisms that could account for the recurrent TIs of Helitrons.

Keywords: DINE-1; chromatin sink; gene regulation; piRNA; β-heterochromatin.

Figure 1.

General layout for transposable element (TE)-derived tandem repeat (TR) expansion and heterochromatin formation. (A) At some point in the TE life cycle one of its copies inserts into an active piRNA cluster and then serves as a template for the generation of complementary piRNAs that silence homologous sequences in the genome via heterochromatin formation. (B) The heterochromatinized TE copies harboring internal TRs are prone to suffering unequal recombination. This TR concertina generates variation in the size of heterochromatin blocks what may in turn affect gene expression. TIR: Terminal Inverted Repeats; LTR: Long Terminal Repeats.

Figure 2.

Schematic representation of the tandem insertions observed by Mendiola et al. When the termination signal is missing at IS91 terminus, the RC transposition loops-out the entire plasmid and generate TIs of the whole construct (IS91 + pSU2572).

Figure 3.

Two RC transposition models proposed for Helitrons. (A) The “Concerted” model of RC transposition was proposed for the IS91 prokaryotic elements and used to explain Helitron transposition. Redrawn from Garcillán-Barcia et al. (B) The “Sequential” model of RC transposition was proposed to explain the formation of episomal circular intermediates of IS91. Schematic representation based upon the model described in Garcillán-Barcia et al. Single-stranded binding Proteins (SSBs) were not represented in the B section to improve clarity. RepHel: Replication Initiator Protein and Helicase; DNA Pol: host DNA polymerase.