The evolutionary dynamics of the Helena retrotransposon revealed by sequenced Drosophila genomes

Abstract

BackgroundSeveral studies have shown that genomes contain a mixture of transposable elements, some of which are still active and others ancient relics that have degenerated. This is true for the non-LTR retrotransposon Helena, of which only degenerate sequences have been shown to be present in some species (Drosophila melanogaster), whereas putatively active sequences are present in others (D. simulans). Combining experimental and population analyses with the sequence analysis of the 12 Drosophila genomes, we have investigated the evolution of Helena, and propose a possible scenario for the evolution of this element.ResultsWe show that six species of Drosophila have the Helena transposable element at different stages of its evolution. The copy number is highly variable among these species, but most of them are truncated at the 5' ends and also harbor several internal deletions and insertions suggesting that they are inactive in all species, except in D. mojavensis in which quantitative RT-PCR experiments have identified a putative active copy.ConclusionOur data suggest that Helena was present in the common ancestor of the Drosophila genus, which has been vertically transmitted to the derived lineages, but that it has been lost in some of them. The wide variation in copy number and sequence degeneration in the different species suggest that the evolutionary dynamics of Helena depends on the genomic environment of the host species.

Vertical inheritance and bursts of transposition have shaped the evolution of the BS non-LTR retrotransposon in Drosophila

“…Besides the 5 0 end deletions, BS evolution is also characterized by low nucleotide polymorphism, but a large number of internal deletions. This is consistent with what was previously reported in its closest relative, the NLTR retrotransposon Helena (Petrov and Hartl 1997;Rebollo et al 2008;Granzotto et al 2009). Whether this property is a general characteristic of NLTR retrotransposons, or of a particular group of elements, is a matter of discussion, because young NLTR retrotransposons, such as F, jockey and doc, seem to have avoided erosion (Lerat et al 2003).…”

“…Nevertheless, specialized species with a small population size may also harbor low TE copy numbers. Indeed, in D. erecta, the NLTR Helena TE is represented by a small number of insertions, mostly degraded (Granzotto et al 2009). This indicates that a specific TE can be in different stages of propagation in the different species.…”

“…The sequences used in the phylogenetic reconstruction were Jockey (M22874), TART (U14101), Doc (X17551), F (M17214), BS (X77571) and X (AF237761) from D. melanogaster; Jockey from D. funebris (M38437); Amy from Bombyx mori (U07847); JuanA from Aedes aegypti (M95171); JuanC from Culens pipientis (M91082); NCR1th from Chironomus tentans (L79944); Helena from D. mauritiana (AF012043), D. simulans and D. melanogaster (Rebollo et al 2008), as well as of other six Drosophila species (Granzotto et al 2009); the BS sequence from D. melanogaster (Udomkit et al 1995) and the seven BS reference copies described in this study. The sequences were manipulated using BioEdit (Hall 1999) and aligned with ClustalW (Thompson et al 1994), using the default parameters.…”

Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes

“…The hypothesis that a high rate of DNA loss exists in Drosophila has already been proposed (Petrov et al, 1998). As an example, the inactivation of the non-LTR retrotransposon helena may have taken place initially by internal deletions followed by mutations, leading to sequence divergence (Granzotto et al, 2009;Rebollo et al, 2008). Our findings suggest that this could be a general mechanism common to the inactivation of all classes of retrotransposons.…”

Systematic Study of Drosophila MicroRNA Functions Using a Collection of Targeted Knockout Mutations

“…The miRNAs added in miRBase 20 were excluded due to low abundance (exception miR-307b was deleted with miR-307a, from miRBase 10). From the 152 miRNAs in miRBase 10, we excluded miRNAs that were not conserved beyond the Drosophila melanogaster subgroup (Granzotto et al, 2009), with the expectation that they were less likely to produce developmental phenotypes (Table 1; Figure 1). The final set of 130 miRNAs included 75 loci encoding single miRNA precursors and 20 miRNA clusters encoding 58 miRNA precursors, for a total of 95 genetic loci.…”