Species-wide transposable element repertoires retrace the evolutionary history of the Saccharomyces cerevisiae host

Transposable elements (TE) are an important source of genetic variation with a dynamic and content that greatly differ in a wide range of species. The origin of the intraspecific content variation is not always clear and little is known about the precise nature of it. Here, we surveyed the species-wide content of the Ty LTR-retrotransposons in a broad collection of 1,011 Saccharomyces cerevisiae natural isolates to understand what can stand behind the variation of the repertoire, i.e. the type and number of Ty elements. We have compiled an exhaustive catalog of all TE variants present in the S. cerevisiae species by identifying a large set of new variants. The characterization of the TE content in each isolate clearly highlighted that each subpopulation exhibits a unique and specific repertoire, retracing the evolutionary history of the species. Most interestingly, we have shown that ancient interspecific hybridization events had a major impact in the birth of new variants and therefore in the shaping of the TE repertoires. We also investigated the transpositional activity of these elements in a large set of natural isolates, and we found a broad variability related to the level of ploidy as well as the genetic background. Overall, our results pointed out that the evolution of the Ty content is deeply impacted by clade-specific events such as introgressions and therefore follows the population structure. In addition, our study lays the foundation for future investigations to better understand the transpositional regulation and more broadly the TE-host interactions.Authors summaryMobile DNA elements are widely distributed in the genomes of many eukaryotes, but their contents greatly vary between species, populations and even individuals. In fact, little is known about the origin of this variation of transposable element (TE) content across individuals of the same species. Here, we surveyed the Ty LTR-retrotransposon content in a broad collection of 1,011 Saccharomyces cerevisiae yeast natural isolates. We have defined an exhaustive and precise catalog of the TE variants present in the S. cerevisiae species. We found that the TE content follows the evolutionary history of the species because each subpopulation has a unique and specific content. Interestingly, our results highlighted that ancient interspecific hybridization events led to the appearance of new TE variants and therefore had a strong impact on the variation of the TE repertoires in this species. We also investigated the transpositional activity of these elements and found a wide variability related to the genetic background diversity. Altogether, our results have led to a better understanding of the variability of TE content at a species level.

Involvement of DNA Repair Genes and System of Radiation-Induced Activation of Transposons in Formation of Transgenerational Effects

The study of the genetic basis of the manifestation of radiation-induced effects and their transgenerational inheritance makes it possible to identify the mechanisms of adaptation and possible effective strategies for the survival of organisms in response to chronic radioactive stress. One persistent hypothesis is that the activation of certain genes involved in cellular defense is a specific response of the cell to irradiation. There is also data indicating the important role of transposable elements in the formation of radiosensitivity/radioresistance of biological systems. In this work, we studied the interaction of the systems of hobo transposon activity and DNA repair in the cell under conditions of chronic low-dose irradiation and its participation in the inheritance of radiation-induced transgenerational instability in Drosophila. Our results showed a significant increase of sterility and locus-specific mutability, a decrease of survival, fertility and genome stability (an increase the frequency of dominant lethal mutations and DNA damage) in non-irradiated F1/F2 offspring of irradiated parents with dysfunction of the mus304 gene which is responsible for excision and post-replicative recombination repair and repair of double-stranded DNA breaks. The combined action of dysfunction of the mus309 gene and transpositional activity of hobo elements also led to the transgenerational effects of irradiation but only in the F1 offspring. Dysfunction of the genes of other DNA repair systems (mus101 and mus210) showed no visible effects inherited from irradiated parents subjected to hobo transpositions. The mei-41 gene showed specificity in this type of interaction, which consists in its higher efficiency in sensing events induced by transpositional activity rather than irradiation.

Sex and the TEs: transposable elements in sexual development and function in animals

Transposable elements are endogenous DNA sequences able to integrate into and multiply within genomes. They constitute a major source of genetic innovations, as they can not only rearrange genomes but also spread ready-to-use regulatory sequences able to modify host gene expression, and even can give birth to new host genes. As their evolutionary success depends on their vertical transmission, transposable elements are intrinsically linked to reproduction. In organisms with sexual reproduction, this implies that transposable elements have to manifest their transpositional activity in germ cells or their progenitors. The control of sexual development and function can be very versatile, and several studies have demonstrated the implication of transposable elements in the evolution of sex. In this review, we report the functional and evolutionary relationships between transposable elements and sexual reproduction in animals. In particular, we highlight how transposable elements can influence expression of sexual development genes, and how, reciprocally, they are tightly controlled in gonads. We also review how transposable elements contribute to the organization, expression and evolution of sexual development genes and sex chromosomes. This underscores the intricate co-evolution between host functions and transposable elements, which regularly shift from a parasitic to a domesticated status useful to the host.

Diversity, dynamics and effects of LTR retrotransposons in the model grass Brachypodium distachyon

SummaryTransposable elements (TEs) are the main reason for the high plasticity of plant genomes, where they occur as communities of diverse evolutionary lineages. Because research has typically focused on single abundant families or summarized TEs at a coarse taxonomic level, our knowledge about how these lineages differ in their effects on genome evolution is still rudimentary.Here we investigate the community composition and dynamics of 32 long terminal repeat retrotransposon (LTR-RT) families in the 272 Mb genome of the Mediterranean grass Brachypodium distachyon.We find that much of the recent transpositional activity in the B. distachyon genome is due to centromeric Gypsy families and Copia elements belonging to the Angela lineage. With a half-life as low as 66 ky, the latter are the most dynamic part of the genome and an important source of within-species polymorphisms. Second, GC-rich Gypsy elements of the Retand lineage are the most abundant TEs in the genome. Their presence explains more than 20 percent of the genome-wide variation in GC content and is associated to higher methylation levels.Our study shows how individual TE lineages change the genetic and epigenetic constitution of the host beyond simple changes in genome size.

Genomic normalization for sequencing libraries enrichment for rare somatic retroelement insertions

BackgroundThere is increasing evidence that the transpositional activity of retroelements (REs) is not limited to germ line cells, but often occurs in tumor and normal somatic cells. Somatic transpositions were found in several human tissues and are especially typical for the brain. Several computational and experimental approaches for detection of somatic retroelement insertions was developed in the past few years. These approaches were successfully applied to detect somatic insertions in clonally expanded tumor cells. At the same time, identification of somatic insertions presented in small proportion of cells, such as neurons, remains a considerable challenge.ResultsIn this study, we developed a normalization procedure for library enrichment by DNA sequences corresponding to rare somatic RE insertions. Two rounds of normalization increased the number of fragments adjacent to somatic REs in the sequenced sample by more than 26-fold, and the number of identified somatic REs was increased by 7.9-fold.ConclusionsThe developed technique can be used in combination with vast majority of modern RE identification approaches and can dramatically increase their capacity to detect rare somatic RE insertions in different types of cells.

Murine MusD Retrotransposon: Structure and Molecular Evolution of an “Intracellularized” Retrovirus

ABSTRACT We had previously identified active autonomous copies of the MusD long terminal repeat-retrotransposon family, which have retained transpositional activity. These elements are closely related to betaretroviruses but lack an envelope (env) gene. Here we show that these elements encode strictly intracellular virus-like particles that can unambiguously be identified by electron microscopy. We demonstrate intracellular maturation of the particles, with a significant proportion of densely packed cores for wild-type MusD but not for a protease mutant. We show that the molecular origin of this unexpected intracellular localization is solely dependent on the N-terminal part of the Gag protein, which lacks a functional sequence for myristoylation and plasma membrane targeting: replacement of the N-terminal domain of the MusD matrix protein by that of its closest relative—the Mason-Pfizer monkey virus—led to targeting of the MusD Gag to the plasma membrane, with viral particles budding and being released into the cell supernatant. These particles can further be pseudotyped with a heterologous envelope protein and become infectious, thus “reconstituting” a functional retrovirus prone to proviral insertions. Consistent with its retroviral origin, a sequence with a constitutive transport element-like activity can further be identified at the MusD 3′ untranslated region. A molecular scenario is proposed that accounts for the transition, during evolution, from an ancestral infectious betaretrovirus to the strictly intracellular MusD retrotransposon, involving not only the loss of the env gene but also an inability to escape the cell—via altered targeting of the Gag protein—resulting de facto in the generation of a very successful “intracellularized” insertional mutagen.