Transfer RNA gene-targeted integration: an adaptation of retrotransposable elements to survive in the compact <i>Dictyostelium discoideum</i> genome

Abstract

Almost every organism carries along a multitude of molecular parasites known as transposable elements (TEs). TEs influence their host genomes in many ways by expanding genome size and complexity, rearranging genomic DNA, mutagenizing host genes, and altering transcription levels of nearby genes. The eukaryotic microorganism Dictyostelium discoideum is attractive for the study of fundamental biological phenomena such as intercellular communication, formation of multicellularity, cell differentiation, and morphogenesis. D. discoideum has a highly compacted, haploid genome with less than 1 kb of genomic DNA separating coding regions. Nevertheless, the D. discoideum genome is loaded with 10% of TEs that managed to settle and survive in this inhospitable environment. In depth analysis of D. discoideum genome project data has provided intriguing insights into the evolutionary challenges that mobile elements face when they invade compact genomes. Two different mechanisms are used by D. discoideum TEs to avoid disruption of host genes upon retrotransposition. Several TEs have invented the specific targeting of tRNA gene-flanking regions as a means to avoid integration into coding regions. These elements have been dispersed on all chromosomes, closely following the distribution of tRNA genes. By contrast, TEs that lack bona fide integration specificities show a strong bias to nested integration, thus forming large TE clusters at certain chromosomal loci that are hardly resolved by bioinformatics approaches. We summarize our current view of D. discoideum TEs and present new data from the analysis of the complete sequences of D. discoideum chromosomes 1 and 2, which comprise more than one third of the total genome.

Multiplexed pyrosequencing of nine sea anemone (Cnidaria: Anthozoa: Hexacorallia: Actiniaria) mitochondrial genomes

“…These noncanonical proteins appear to contain little phylogenetic signal, as they have been gained, lost, or truncated numerous times throughout the actiniarian tree. This pattern is consistent with open reading frames that contain mobile transposon-like elements (Winckler et al, 2005). BLAST searches in all six reading frames against the nr and EST databases of NCBI GenBank, as well as the PFAM database of EMBL-EBI, returned no significant hits for either novel protein in any mitogenome in which they occur.…”

Retrotransposon profiling of RNA polymerase III initiation sites

“…In Dictyostelium, non-LTR retrotransposons TRE5 and TRE3 cluster ;44 to 54 bp upstream and 40 to 150 bp downstream of tDNA-coding sequences, respectively (Winckler et al 2005). Genomic Ty3 and LTR remnants occur within a few base pairs of the tDNA TSS (Sandmeyer et al 2002).…”

In Vitro Targeting of Strand Transfer by the Ty3 Retroelement Integrase

“…The relatively subtle integration preferences of retroviruses contrast with the striking preferences of some retrotransposons in lower eukaryotes and plants (7)(8)(9). For example, in Saccharomyces cerevisiae, the copia-like LTR retrotransposon Ty5 is targeted to heterochromatic DNA by interactions between the IN C-terminal domain and the Sir4 silencing protein (10 -11) and copia-like Ty1 and gypsy-like Ty3 LTR retrotransposons target the 5Ј-flanking regions of Pol III-transcribed genes (12)(13).…”