Retrotransposon Domestication and Control in Dictyostelium discoideum

Abstract

Transposable elements, identified in all eukaryotes, are mobile genetic units that can change their genomic position. Transposons usually employ an excision and reintegration mechanism, by which they change position, but not copy number. In contrast, retrotransposons amplify via RNA intermediates, increasing their genomic copy number. Hence, they represent a particular threat to the structural and informational integrity of the invaded genome. The social amoeba Dictyostelium discoideum, model organism of the evolutionary Amoebozoa supergroup, features a haploid, gene-dense genome that offers limited space for damage-free transposition. Several of its contemporary retrotransposons display intrinsic integration preferences, for example by inserting next to transfer RNA genes or other retroelements. Likely, any retrotransposons that invaded the genome of the amoeba in a non-directed manner were lost during evolution, as this would result in decreased fitness of the organism. Thus, the positional preference of the Dictyostelium retroelements might represent a domestication of the selfish elements. Likewise, the reduced danger of such domesticated transposable elements led to their accumulation, and they represent about 10% of the current genome of D. discoideum. To prevent the uncontrolled spreading of retrotransposons, the amoeba employs control mechanisms including RNA interference and heterochromatization. Here, we review TRE5-A, DIRS-1 and Skipper-1, as representatives of the three retrotransposon classes in D. discoideum, which make up 5.7% of the Dictyostelium genome. We compile open questions with respect to their mobility and cellular regulation, and suggest strategies, how these questions might be addressed experimentally.

The Structural, Functional and Evolutionary Impact of Transposable Elements in Eukaryotes

“…For instance, the genome of the social amoeba Dictyostelium discoideum, whose centromere is rich in TEs (86%, 171-361 bp), is dominated by LTR retrotransposons [268]. The centromere and the surrounding region containing the tRNA genes appear to harbour several copies of these TEs, which have a strong insertional preference for the region as a result of low mutagenesis and the presence of relatively safe integration sites [269]. This hypothesised domestication of TEs is thought to be involved in a complex control network that comprises LTR retrotransposon families (Skipper and DGLT-A), the RNAi machinery, and centromeric histones that regulate retrotransposition and kinetochore assembly [269].…”

“…The centromere and the surrounding region containing the tRNA genes appear to harbour several copies of these TEs, which have a strong insertional preference for the region as a result of low mutagenesis and the presence of relatively safe integration sites [269]. This hypothesised domestication of TEs is thought to be involved in a complex control network that comprises LTR retrotransposon families (Skipper and DGLT-A), the RNAi machinery, and centromeric histones that regulate retrotransposition and kinetochore assembly [269]. Thus, TEs in the centromere of D. discoideum may have co-evolved with its host to provide the necessary substrate for kinetochore complex formation in return for the ability to accumulate in the genome near "low-danger" tRNA genes [270].…”

Evolutionary dynamics of DIRS-like and Ngaro-like retrotransposons in Xenopus laevis and Xenopus tropicalis genomes

“…It is not clear, however, the reason why the Ngaro-like did not achieve the same success as DIRS-like , but it could be related to the known differences in the transposition mechanism ( Poulter and Goodwin 2005 ) of both superfamilies or to a possible variation in silencing efficiency by the host, while it could also be explained by chance. Still, evidence of the accumulation of DIRS-1 element on centromeres of the D. discoideum genome ( Dubin et al 2010 ; Malicki et al 2017 ) could indicate their role during the centromeric heterochromatin biogenesis in this genome and open new perspectives to future evaluation about their biological significance in their success in Xenopus genomes.…”

Retrotransposon targeting to RNA polymerase III-transcribed genes

“…The TRE5-A retrotransposon has two ORFs - ORF1 encodes a 51kD protein of unknown function and ORF2 encodes a protein with an apurinic/apyrimidinic endonuclease (APE) domain, an RT domain, and a zinc-finger (ZF) domain (Fig. 1 ) [ 129 , 131 ]. Interestingly, protein-protein interactions have been detected between the TRE5-A ORF1 protein and the three D. discoideum TFIIIB proteins TBP, Brf1 and Bdp1 [ 132 ].…”

“…On the contrary, evidence shows that these elements have a neutral or moderately stimulatory effect on tRNA gene transcription [ 139 , 140 ]. It has not yet been investigated if tRNA gene expression is affected in D. discoideum when retrotransposons insert nearby [ 131 ]. The retrotransposon may benefit however from its targeting preference because the promoter activity of the A module in TRE5-A is enhanced if a tRNA gene is present upstream [ 141 ].…”