Abstract
BackgroundThe mariner family of transposable elements is one of the most widespread in the Metazoa. It is subdivided into several subfamilies that do not mirror the phylogeny of these species, suggesting an ancient diversification. Previous hybridization and PCR studies allowed a partial survey of mariner diversity in the Metazoa. In this work, we used a comparative genomics approach to access the genus-wide diversity and evolution of mariner transposable elements in twenty Drosophila sequenced genomes.ResultsWe identified 36 different mariner lineages belonging to six distinct subfamilies, including a subfamily not described previously. Wide variation in lineage abundance and copy number were observed among species and among mariner lineages, suggesting continuous turn-over. Most mariner lineages are inactive and contain a high proportion of damaged copies. We showed that, in addition to substitutions that rapidly inactivate copies, internal deletion is a major mechanism contributing to element decay and the generation of non-autonomous sublineages. Hence, 23% of copies correspond to several Miniature Inverted-repeat Transposable Elements (MITE) sublineages, the first ever described in Drosophila for mariner. In the most successful MITEs, internal deletion is often associated with internal rearrangement, which sheds light on the process of MITE origin. The estimation of the transposition rates over time revealed that all lineages followed a similar progression consisting of a rapid amplification burst followed by a rapid decrease in transposition. We detected some instances of multiple or ongoing transposition bursts. Different amplification times were observed for mariner lineages shared by different species, a finding best explained by either horizontal transmission or a reactivation process. Different lineages within one species have also amplified at different times, corresponding to successive invasions. Finally, we detected a preference for insertion into short TA-rich regions, which appears to be specific to some subfamilies.ConclusionsThis analysis is the first comprehensive survey of this family of transposable elements at a genus scale. It provides precise measures of the different evolutionary processes that were hypothesized previously for this family based on PCR data analysis. mariner lineages were observed at almost all “life cycle” stages: recent amplification, subsequent decay and potential (re)-invasion or invasion of genomes.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-727) contains supplementary material, which is available to authorized users.
Highlights
The mariner family of transposable elements is one of the most widespread in the Metazoa
The clade structure derived from the transposase analysis was supported by the comparison of terminal inverted repeats (TIRs), which showed that some blocks of nucleotides are clade-specific
Miniature Inverted-repeat Transposable Elements (MITE) have been associated with genes in plant species [32,33]. We investigated whether this association was present in the high-copy-number Dromar11 and Dromar5 MITEs in D. eugracilis
Summary
The mariner family of transposable elements is one of the most widespread in the Metazoa. We used a comparative genomics approach to access the genus-wide diversity and evolution of mariner transposable elements in twenty Drosophila sequenced genomes. Mariner is a Class II transposon (i.e., transposing through a cut-and-paste mechanism) belonging to the large Tc1-mariner-IS630 superfamily of transposable elements present in almost all groups of living organisms. It was first discovered in Drosophila mauritiana [1], a species from the melanogaster subgroup. Mariner-like elements (MLEs) have been identified in a wide range of species, primarily metazoans. Other conserved motifs with known (DNA-binding domain) or unknown functions have been identified [4]
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