Helitrons , the Eukaryotic Rolling-circle Transposable Elements

Abstract

Helitrons, the eukaryotic rolling-circle transposable elements, are widespread but most prevalent among plant and animal genomes. Recent studies have identified three additional coding and structural variants of Helitrons called Helentrons, Proto-Helentron, and Helitron2. Helitrons and Helentrons make up a substantial fraction of many genomes where nonautonomous elements frequently outnumber the putative autonomous partner. This includes the previously ambiguously classified DINE-1-like repeats, which are highly abundant in Drosophila and many other animal genomes. The purpose of this review is to summarize what we have learned about Helitrons in the decade since their discovery. First, we describe the history of autonomous Helitrons, and their variants. Second, we explain the common coding features and difference in structure of canonical Helitrons versus the endonuclease-encoding Helentrons. Third, we review how Helitrons and Helentrons are classified and discuss why the system used for other transposable element families is not applicable. We also touch upon how genome-wide identification of candidate Helitrons is carried out and how to validate candidate Helitrons. We then shift our focus to a model of transposition and the report of an excision event. We discuss the different proposed models for the mechanism of gene capture. Finally, we will talk about where Helitrons are found, including discussions of vertical versus horizontal transfer, the propensity of Helitrons and Helentrons to capture and shuffle genes and how they impact the genome. We will end the review with a summary of open questions concerning the biology of this intriguing group of transposable elements.

Transposable elements inDrosophila

“…This model suggests that tyrosine residues of the Rep protein simultaneously nick the 5′ end of one Helitron strand at a conserved TC sequence and the AT sequence on the target site 62 . The Helitron donor strand is displaced by the encoded helicase (Fig.…”

“…4B). 62 Rep facilitates cleavage of the donor strand at a conserved hairpin signal in the 3′ end, which then attacks the 5′ end of the element, generating a circular, single-stranded DNA (ssDNA) intermediate (Fig. 4B).…”

“… 64 To complete transposition of the element, Rep cleaves the circular ssDNA intermediate to promote covalent bond formation between the 5′ and 3′ ends of the Helitron donor strand and the nicked target site 64 62 . Host DNA replication is responsible for generating the second strand at both the donor and target sites, permitting amplification of these elements 62 …”

Cross-Regulation between Transposable Elements and Host DNA Replication

“…Subsequent DNA replication duplicates the joint insertion into a co-integrate, doubling the copy number. Similarly, the concerted model of Helitron transposition starts with single-stranded cleavage and 5′ strand transfer, followed by strand displacement of the transposed strand by replication from the free 3′ OH of the donor [4]. The displaced strand is cleaved and joined with the 5′ end of the target nick, leaving it as a heteroduplex that resolves by passive DNA replication, generating a new copy of the Helitron in one of the daughter strands.…”

RepeatModeler2: automated genomic discovery of transposable element families

“…The most common class II transposons are TIR (terminal inverted repeats) elements, which transpose via a "cutand-paste" mechanism (Feschotte and Pritham 2007). But other class II elements, such as Helitrons, also use replicative mechanisms (Thomas and Pritham 2015;Grabundzija et al 2018). Within each class, TE sequences are extremely diverse and evolve rapidly (Wicker et al 2007;Arkhipova 2017;Bourque et al 2018).…”