Abstract
BackgroundOnly a few transposable elements are known to exhibit site-specific insertion patterns, including the well-studied R-element retrotransposons that insert into specific sites within the multigene rDNA. The only known rDNA-specific DNA transposon, Pokey (superfamily: piggyBac) is found in the freshwater microcrustacean, Daphnia pulex. Here, we present a genome-wide analysis of Pokey based on the recently completed whole genome sequencing project for D. pulex.ResultsPhylogenetic analysis of Pokey elements recovered from the genome sequence revealed the presence of four lineages corresponding to two divergent autonomous families and two related lineages of non-autonomous miniature inverted repeat transposable elements (MITEs). The MITEs are also found at the same 28S rRNA gene insertion site as the Pokey elements, and appear to have arisen as deletion derivatives of autonomous elements. Several copies of the full-length Pokey elements may be capable of producing an active transposase. Surprisingly, both families of Pokey possess a series of 200 bp repeats upstream of the transposase that is derived from the rDNA intergenic spacer (IGS). The IGS sequences within the Pokey elements appear to be evolving in concert with the rDNA units. Finally, analysis of the insertion sites of Pokey elements outside of rDNA showed a target preference for sites similar to the specific sequence that is targeted within rDNA.ConclusionsBased on the target site preference of Pokey elements and the concerted evolution of a segment of the element with the rDNA unit, we propose an evolutionary path by which the ancestors of Pokey elements have invaded the rDNA niche. We discuss how specificity for the rDNA unit may have evolved and how this specificity has played a role in the long-term survival of these elements in the subgenus Daphnia.
Highlights
A few transposable elements are known to exhibit site-specific insertion patterns, including the well-studied R-element retrotransposons that insert into specific sites within the multigene ribosomal DNA (rDNA)
The Daphnia rDNA transcription unit and a 500 bp non-repetitive region from the intergenic spacer (IGS) contain no sequence variants at the 3% threshold. This especially low level of rDNA variation is consistent with the very high level of homozygosity at allozyme and microsatellite markers observed in the sequenced Daphnia isolate [15], the low level of sequence variation in 28S genes from D. pulex in natural populations [16], and the high rate of recombination observed in the rDNA of a closely related species, Daphnia obtusa [17]
In spite of what would appear to be a seemingly inhospitable location for a DNA transposon, Pokey has evolved specificity for a site in the 28S genes of Daphnia. Analysis of both the annotated D. pulex genome and the raw trace files revealed that rDNA units display extremely low levels of sequence variation consistent with the high rates of recombination previously observed for this locus
Summary
A few transposable elements are known to exhibit site-specific insertion patterns, including the well-studied R-element retrotransposons that insert into specific sites within the multigene rDNA. The only known rDNA-specific DNA transposon, Pokey (superfamily: piggyBac) is found in the freshwater microcrustacean, Daphnia pulex. Pokey is the only example of a DNA transposon known to insert in rDNA. Pokey inserts into the same 28S gene region that is rDNA is comprised of hundreds to thousands of units arrayed in tandem encoding one copy each of the core 18S, 5.8S and 28S rRNAs. The many copies of each rRNA gene show high sequence identity, the product of recombinational processes termed concerted evolution (reviewed in [2]). The combined processes of concerted evolution and selection against inserted units require that any element with a long-term presence in the rDNA unit regularly generate new insertions to avoid being eliminated from the locus [4,5]
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