A Population Genetic Model for the Maintenance of R2 Retrotransposons in rRNA Gene Loci

Department of Biology, University of Rochester, Rochester, New York, United States of America.
PLoS Genetics (Impact Factor: 7.53). 01/2013; 9(1):e1003179. DOI: 10.1371/journal.pgen.1003179
Source: PubMed


R2 retrotransposable elements exclusively insert into the tandemly repeated rRNA genes, the rDNA loci, of their animal hosts. R2 elements form stable long-term associations with their host, in which all individuals in a population contain many potentially active copies, but only a fraction of these individuals show active R2 retrotransposition. Previous studies have found that R2 RNA transcripts are processed from a 28S co-transcript and that the likelihood of R2-inserted units being transcribed is dependent upon their distribution within the rDNA locus. Here we analyze the rDNA locus and R2 elements from nearly 100 R2-active and R2-inactive individuals from natural populations of Drosophila simulans. Along with previous findings concerning the structure and expression of the rDNA loci, these data were incorporated into computer simulations to model the crossover events that give rise to the concerted evolution of the rRNA genes. The simulations that best reproduce the population data assume that only about 40 rDNA units out of the over 200 total units are actively transcribed and that these transcribed units are clustered in a single region of the locus. In the model, the host establishes this transcription domain at each generation in the region with the fewest R2 insertions. Only if the host cannot avoid R2 insertions within this 40-unit domain are R2 elements active in that generation. The simulations also require that most crossover events in the locus occur in the transcription domain in order to explain the empirical observation that R2 elements are seldom duplicated by crossover events. Thus the key to the long-term stability of R2 elements is the stochastic nature of the crossover events within the rDNA locus, and the inevitable expansions and contractions that introduce and remove R2-inserted units from the transcriptionally active domain.

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    • "The total number of R2 insertions in a species is a balance between the rate of new retrotransposition events and the rate of net loss of elements by the recombination events (crossovers) that give rise to the concerted evolution of the rRNA genes [26]. Determination of these rates can only be obtained by detailed studies of element gain and loss over extended periods similar to those that have been conducted in Drosophila [20], [21], [59], [66]. "
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    ABSTRACT: R2 non-LTR retrotransposons exclusively insert into the 28S rRNA genes of their host, and are expressed by co-transcription with the rDNA unit. The grasshopper Eyprepocnemis plorans contains transcribed rDNA clusters on most of its A chromosomes, as well as non-transcribed rDNA clusters on the parasitic B chromosomes found in many populations. Here the structure of the E. plorans R2 element, its abundance relative to the number of rDNA units and its retrotransposition activity were determined. Animals screened from five populations contained on average over 12,000 rDNA units on their A chromosomes, but surprisingly only about 100 R2 elements. Monitoring the patterns of R2 insertions in individuals from these populations revealed only low levels of retrotransposition. The low rates of R2 insertion observed in E. plorans differ from the high levels of R2 insertion previously observed in insect species that have many fewer rDNA units. It is proposed that high levels of R2 are strongly selected against in E. plorans, because the rDNA transcription machinery in this species is unable to differentiate between R2-inserted and uninserted units. The B chromosomes of E. plorans contain an additional 7,000 to 15,000 rDNA units, but in contrast to the A chromosomes, from 150 to over 1,500 R2 elements. The higher concentration of R2 in the inactive B chromosomes rDNA clusters suggests these chromosomes can act as a sink for R2 insertions thus further reducing the level of insertions on the A chromosomes. These studies suggest an interesting evolutionary relationship between the parasitic B chromosomes and R2 elements.
    Full-text · Article · Mar 2014 · PLoS ONE
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    • "The primary mechanism conferring high identity between copies is unequal crossing over, which also generates the large variation in rDNA copy number observed between members of the same species [4]. The combined processes of concerted evolution and selection against inserted units require that any element with a long-term presence in the rDNA unit regularly generate new insertions to avoid being eliminated from the locus [4,5]. "
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    ABSTRACT: Only a few transposable elements are known to exhibit site-specific insertion patterns, including the well-studied R-element retrotransposons that insert into specific sites within the multigene rDNA. The only known rDNA-specific DNA transposon, Pokey (superfamily: piggyBac) is found in the freshwater microcrustacean, Daphnia pulex. Here, we present a genome-wide analysis of Pokey based on the recently completed whole genome sequencing project for D. pulex. Phylogenetic analysis of Pokey elements recovered from the genome sequence revealed the presence of four lineages corresponding to two divergent autonomous families and two related lineages of non-autonomous miniature inverted repeat transposable elements (MITEs). The MITEs are also found at the same 28S rRNA gene insertion site as the Pokey elements, and appear to have arisen as deletion derivatives of autonomous elements. Several copies of the full-length Pokey elements may be capable of producing an active transposase. Surprisingly, both families of Pokey possess a series of 200 bp repeats upstream of the transposase that is derived from the rDNA intergenic spacer (IGS). The IGS sequences within the Pokey elements appear to be evolving in concert with the rDNA units. Finally, analysis of the insertion sites of Pokey elements outside of rDNA showed a target preference for sites similar to the specific sequence that is targeted within rDNA. Based on the target site preference of Pokey elements and the concerted evolution of a segment of the element with the rDNA unit, we propose an evolutionary path by which the ancestors of Pokey elements have invaded the rDNA niche. We discuss how specificity for the rDNA unit may have evolved and how this specificity has played a role in the long-term survival of these elements in the subgenus Daphnia.
    Full-text · Article · Sep 2013 · Mobile DNA
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    ABSTRACT: Theoretical and empirical studies have shown differential management of transposable elements in organisms with different reproductive strategies. To investigate this issue, we analysed the R2 retroelement structure and variability in parthenogenetic and bisexual populations of Bacillus rossius stick insects, as well as insertions inheritance in the offspring of parthenogenetic isolates and of crosses. The B. rossius genome hosts a functional (R2Br(fun) ) and a degenerate (R2Br(deg) ) element, their presence correlating with neither reproductive strategies nor population distribution. The median-joining network method indicated that R2Br(fun) duplicates through a multiple source model, while R2Br(deg) is apparently still duplicating via a master gene model. Offspring analyses showed that unisexual and bisexual offspring have a similar number of R2Br-occupied sites. Multiple or recent shifts from gonochoric to parthenogenetic reproduction may explain the observed data. Moreover, insertion frequency spectra show that higher-frequency insertions in unisexual offspring significantly outnumber those in bisexual offspring. This suggests that unisexual offspring eliminate insertions with lower efficiency. A comparison with simulated insertion frequencies shows that inherited insertions in unisexual and bisexual offspring are significantly different from the expectation. On the whole, different mechanisms of R2 elimination in unisexual vs bisexual offspring and a complex interplay between recombination effectiveness, natural selection and time can explain the observed data.
    No preview · Article · Aug 2014 · Insect Molecular Biology
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