Genomic landscape and evolutionary dynamics of mariner transposable elements within the Drosophila genus

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.

An overview of irritans-mariner transposons in two Mayetiola species (Diptera: Cecidomyiidae)

“…The high diversity recorded in M. destructor suggests that its genome was invaded many times by different types of irritans elements, as reported in species of Drosophila by Wallau et al (2014).…”

Diversity and evolution of mariner-like elements in aphid genomes

“…Globally, these results show that (i) MITEs in aphid species are less frequent than in Drosophila ananassae (about 240 copies) [41] and in Rhodnius prolixus (about 400 copies) [20]; (ii) irritans clades do not generate MITEs smaller than 900 bp, in contrast to rosa and LTIR -like elements clades; (iii) three MITE sublineages ( MITE2.2 , MITE4.2 and MITE5.1 ) are closely related to autonomous copies found in other species; (iv) orphan MITE sublineages can be detected with no full-length partner ( MITE1.1 sub2 ). In the later case, it cannot be excluded that active copies still exist in other populations or closely related species.…”

“…To infer the dynamics of MITEs identified in the aphid genomes, we generated consensus sequences for each sublineage in order to estimate their period of amplification from their percentage of divergence, as proposed by Le Rouzic et al [50] and Wallau et al [41]. Except for two sequences of the MITE4.1 sub2 showing 69 and 72% of identity with the consensus of this lineage, all others exhibit a level of identity higher than 85% (Fig.…”

“…USEARCH6.0 [40] was performed to cluster repetitive sequences using a threshold of 75% identity. Shorter copies flanked by two TIRs and with evidence of transposition (at least 2 copies) were considered as MITEs [4, 41]. Consensus sequences were derived using the relative majority rule.…”

Regulated complex assembly safeguards the fidelity ofSleeping Beautytransposition

“…While the truncated Tdr1 copies always carried sequences of various lengths between the IR/DRs (over 400 bps, Supplementary Figure S1), variants lacking the entire internal part, and basically consisting only of the IRs are detectable only in the Hsmar1 population (Supplementary Figure S2). These structures are known as m iniature i nverted repeat t ransposable e lements or MITEs, and seem to be generally associated with mariners (30,32,33). Curiously, while various Hsmar1 -derived MITE-like structures are detectable in the human genome, one particular variant, consisting from two, 37-bp IRs linked by a 6-bp intervening sequence appears to have been preferentially amplified (Figure 1E).…”