Convergent evolution of integration site selection upstream of tRNA genes by yeast and amoeba retrotransposons

Abstract

Transposable elements amplify in genomes as selfish DNA elements and challenge host fitness because their intrinsic integration steps during mobilization can compromise genome integrity. In gene-dense genomes, transposable elements are notably under selection to avoid insertional mutagenesis of host protein-coding genes. We describe an example of convergent evolution in the distantly related amoebozoan Dictyostelium discoideum and the yeast Saccharomyces cerevisiae, in which the D. discoideum retrotransposon DGLT-A and the yeast Ty3 element developed different mechanisms to facilitate position-specific integration at similar sites upstream of tRNA genes. Transcription of tRNA genes by RNA polymerase III requires the transcription factor complexes TFIIIB and TFIIIC. Whereas Ty3 recognizes tRNA genes mainly through interactions of its integrase with TFIIIB subunits, the DGLT-A-encoded ribonuclease H contacts TFIIIC subunit Tfc4 at an interface that covers tetratricopeptide repeats (TPRs) 7 and 8. A major function of this interface is to connect TFIIIC subcomplexes τA and τB and to facilitate TFIIIB assembly. During the initiation of tRNA gene transcription τB is displaced from τA, which transiently exposes the TPR 7/8 surface of Tfc4 on τA. We propose that the DGLT-A intasome uses this binding site to obtain access to genomic DNA for integration during tRNA gene transcription.

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

“…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 , ). Preferential targets have been described for the integration of different classes of TEs, including retroelements (Sultana et al , ).…”

“…Furthermore, Ty1 insertion has a limiting impact on tDNA expression (Bolton & Boeke, ). Targeted integration proximal to tDNA s is a strategy that has been adopted several times by TEs to minimize damage to compact genomes (Cheung et al , ; Kling et al , ). The integration of Ty1 in these regions requires a functional Pol III promoter in the target gene (Devine & Boeke, ) and is influenced by the chromatin‐remodeling factor Isw2 and the Bdp1 subunit of TFIIIB (Bachman et al , ).…”

The multi‐faceted regulation of nuclear tRNA gene transcription

“…Trypanosoma brucei (66) and A. thaliana (67)). Similarly, a close genomic relationship has been demonstrated between tDNAs and retro-elements in S. cerevisiae (68)(69)(70) and with introns in Caenorhabditis species (71). In the latter, the authors showed a reduction in the expression of tRNAs residing within introns of protein coding genes effectively demonstrating a PE on the transcription of tDNAs.…”

The Ty1 integrase nuclear localization signal is necessary and sufficient for retrotransposon targeting to tRNA genes

“…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 Cheung et al, 2018;Spaller et al, 2016). These regions often consist of non-essential repeated sequences, such as telomeric regions, ribosomal DNA arrays, and transfer RNA genes (tDNAs), or non-essential regions upstream of open reading frames (Baller et al, 2012;Fujiwara et al, 2005;Guo and Levin, 2010;Kling et al, 2018;Mularoni et al, 2012;Naito et al, 2009;Pardue and DeBaryshe, 2011;Penton and Crease, 2004;Ye et al, 2005;Zou et al, 1996). Preferential targets have been described for the integration of different classes of TEs, including retroelements (Sultana et al, 2017).…”

“…Furthermore, Ty1 insertion has a limiting impact on tDNA expression (Bolton and Boeke, 2003). Targeted integration proximal to tDNAs is a strategy that has been adopted several times by TEs to minimize damage to compact genomes (Cheung et al, 2018;Kling et al, 2018). The integration of Ty1 in these regions requires a functional Pol III promoter in the target gene (Devine and Boeke, 1996) and is influenced by the chromatin-remodeling factor Isw2 and the Bdp1 subunit of TFIIIB (Bachman et al, 2005).…”