Rolling-circle transposons in eukaryotes

Abstract

All eukaryotic DNA transposons reported so far belong to a single category of elements transposed by the so-called ''cut-and-paste'' mechanism. Here, we report a previously unknown category of eukaryotic DNA transposons, Helitron, which transpose by rollingcircle replication. Autonomous Helitrons encode a 5 -to-3 DNA helicase and nuclease͞ligase similar to those encoded by known rolling-circle replicons. Helitron-like transposons have conservative 5 -TC and CTRR-3 termini and do not have terminal inverted repeats. They contain 16-to 20-bp hairpins separated by 10 -12 nucleotides from the 3 -end and transpose precisely between the 5 -A and T-3 , with no modifications of the AT target sites. Together with their multiple diverged nonautonomous descendants, Helitrons constitute Ϸ2% of both the Arabidopsis thaliana and Caenorhabditis elegans genomes and also colonize the Oriza sativa genome. Sequence conservation suggests that Helitrons continue to be transposed.

A Helitron-Like Transposon Superfamily from Lepidoptera Disrupts (GAAA)n Microsatellites and is Responsible for Flanking Sequence Similarity within a Microsatellite Family

“…Remaining portions of OnMINE-1s contain multiple insertion/deletion mutations, which includes sequence length variation within the direct repeat (DR) region. The predicted termini of OnMINE-1 elements are composed of 5 0 C and a 3 0 CTAT motifs that are similar to those conserved among Helitron-like TEs (5 0 TC and a 3 0 CTRR; Kapitonov and Jurka 2001), and suggests the elements may belong to a Helitron-like group of TEs. Sequence data also indicate that the number of (GAAA) n microsatellite repeat units that flank independent OnMINE-1s integrations (loci) vary from 2-16 at the 5 0 end (mean 4.28 ± 3.43) and 1-4 at the 3 0 end (mean 1.47 ± 0.83).…”

“…TAYA TSDs flank the Ades Aegypti Wukong, Jujin, and Weneng families of elements, whereas Nemo1 elements appear to target and duplicate CA sequences (Tu 1997), the Culex pipiens mimo element has TA TSDs (Feschotte and Mouchès 2000), and similarly lepidopteran MITEs from O. nubilalis (Coates et al 2009) and Helicoverpa zea (Chen and Li 2007) insert at TA genome positions. In contrast, Helitron-like TEs insert between AT or TT dinucleotides without the creation of TSDs (Kapitonov and Jurka 2001;2007b). We show that 16 independent OnMITE01 integrations that lack the novel 588 bp IS have a conserved ancestral GAAAGAA nucleotide motif, but in contrast (GAAA) 7 and (GAAA) 3 microsatellite repeat units are flanking the 5 0 and 3 0 ends of the novel IS, respectively (GenBank accession EU673456; Fig.…”

“…The IR secondary structure may be critical for recognition by trans-acting factors required for transposition (Wessler et al 1995), but lack of the IR suggests it may not be required for transposition of the PgMINE-1 or that the mutation has rendered the element immobile. Additionally, the termini of PgMINE-1 consisted of 5 0 C and a 3 0 TCAA sequences that are similar to those conserved among Helitron-like TEs (5 0 TC and a 3 0 CTRR; Kapitonov and Jurka 2001), which suggests that the PgMINE-1 from accession AY707868 could be classified as a non-autonomous Helitron.…”

“…Multiple sequence alignment of 119 randomly chosen BmMINE-1 elements from genome positions ?20 to -750 of (GAAA) n indicate that regions C649 bp downstream of the microsatellite share extensive similarity (supplementary file F1). Also,113 of 119 (94.54%) BmMINE-1s have a 5 0 TC that is similar to Helitron-like TEs (Kapitonov and Jurka 2001), and show as conserved 5 0 SIR [TC(A)TTTATTCRCCAR] (5 0 TC in bold and optional A in parenthesis) that has a complementary 5 0 IR similar to the secondary structure of OnMINE-1 and Drosophila DINE-1 elements. Despite the observation of short (GAAA) n microsatellite repeats at the 3 0 terminus of OnMINE-1 elements and AAGAA motif following the PgMINE-1, no discernable (GAAA) n repeat is present at the 3 0 terminus of the 119 aligned BmMINE-1s.…”

“…Helitrons do not create TSDs, but in contrast to other class II TEs insert between AT (Kapitonov and Jurka 2001) or TT dinucleotides (Kapitonov and Jurka 2007a). Autonomous Helitrons encode a RepHel protein that carries out replication initiation and helicase activities, and optional replication protein A (RPA) genes that function in ssDNA binding (Kapitonov and Jurka 2001). Similar to MITEs, non-autonomous Helitron elements exist and were predicted to represent all known Helitron-like Drosophila interspersed elements (DINE-1s) in the D. melanogaster genome (Kapitonov and Jurka 2007a).…”