Convergent evolution of tRNA gene targeting preferences in compact genomes

Abstract

BackgroundIn gene-dense genomes, mobile elements are confronted with highly selective pressure to amplify without causing excessive damage to the host. The targeting of tRNA genes as potentially safe integration sites has been developed by retrotransposons in various organisms such as the social amoeba Dictyostelium discoideum and the yeast Saccharomyces cerevisiae. In D. discoideum, tRNA gene-targeting retrotransposons have expanded to approximately 3 % of the genome. Recently obtained genome sequences of species representing the evolutionary history of social amoebae enabled us to determine whether the targeting of tRNA genes is a generally successful strategy for mobile elements to colonize compact genomes.ResultsDuring the evolution of dictyostelids, different retrotransposon types independently developed the targeting of tRNA genes at least six times. DGLT-A elements are long terminal repeat (LTR) retrotransposons that display integration preferences ~15 bp upstream of tRNA gene-coding regions reminiscent of the yeast Ty3 element. Skipper elements are chromoviruses that have developed two subgroups: one has canonical chromo domains that may favor integration in centromeric regions, whereas the other has diverged chromo domains and is found ~100 bp downstream of tRNA genes. The integration of D. discoideum non-LTR retrotransposons ~50 bp upstream (TRE5 elements) and ~100 bp downstream (TRE3 elements) of tRNA genes, respectively, likely emerged at the root of dictyostelid evolution. We identified two novel non-LTR retrotransposons unrelated to TREs: one with a TRE5-like integration behavior and the other with preference ~4 bp upstream of tRNA genes.ConclusionsDictyostelid retrotransposons demonstrate convergent evolution of tRNA gene targeting as a probable means to colonize the compact genomes of their hosts without being excessively mutagenic. However, high copy numbers of tRNA gene-associated retrotransposons, such as those observed in D. discoideum, are an exception, suggesting that the targeting of tRNA genes does not necessarily favor the amplification of position-specific integrating elements to high copy numbers under the repressive conditions that prevail in most host cells.Electronic supplementary materialThe online version of this article (doi:10.1186/s13100-016-0073-9) contains supplementary material, which is available to authorized users.

Multiple Roots of Fruiting Body Formation in Amoebozoa

“…Although several reverse transcriptase domains of both long terminal repeat (LTR) and non-LTR retrotransposons could be determined, the corresponding elements are highly fragmented and mostly present in single copy. Only four LTR retrotransposons could be analyzed in some detail, and they belong to the Skipper and DGLT-A families of Ty3/gypsy type of LTR retrotransposons known from the dictyosteliid clade ( Spaller et al. 2016 ).…”

A small targeting domain in Ty1 integrase is sufficient to direct retrotransposon integration upstream of tRNA genes

“…First, selection leads to the elimination of strongly deleterious insertions and the maintenance of beneficial ones (Chuong et al , ; Cosby et al , ). Second, TEs have repeatedly evolved mechanisms that direct their integration into “safe” locations, where insertions will have minimal adverse effect on the organism's fitness (Boeke & Devine, ; Spaller et al , ; Cheung et al , ). These regions often consist of non‐essential repeated sequences, such as telomeric regions, ribosomal DNA arrays, upstream and downstream regions of transfer RNA genes ( tDNA s), or non‐essential regions upstream of open reading frames (Zou et al , ; Penton & Crease, ; Fujiwara et al , ; Ye et al , ; Naito et al , ; Guo & Levin, ; Pardue & DeBaryshe, ; Baller et al , ; Mularoni et al , ; Spaller et al , ; Kling et al , ).…”

Cross-Regulation between Transposable Elements and Host DNA Replication

“…Type III genes, the targets for Ty1 and Ty3 insertion, are notorious RFB [60,61], and Sir4, the Ty5 tethering factor, is recruited to sites of replication fork arrest [62]. In the amoeba Dictyostelium discoideum several LTR and non-LTR retrotransposons also show targeting to tDNA genes [63]. These target site preferences could indicate an ancestral role of arrested replication forks in retrotransposon target site selection.…”