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

Jun Zhou, Michael T Eickbush and Thomas H Eickbush

PLOS Genetics, 2013, vol. 9, issue 1, 1-14

Abstract: 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. Author Summary: Selfish transposable elements survive in eukaryotic genomes despite the elaborate mechanisms developed by the hosts to limit their activity. One accessible system that simplifies the complex interactions between element and host involves the R2 elements, which exclusively insert in the tandemly arranged rRNA genes. R2 exhibits remarkable stability in animal lineages even though each insertion inactivates one rRNA gene. Here we determine the size of the rDNA locus and R2 number in natural isolates of Drosophila simulans. Combined with previous data concerning the expression and regulation of R2, we develop a detailed population genetic model for rRNA gene and R2 evolution that duplicates all properties of the rRNA loci in natural populations. Critical components of the model are that only a contiguous 40 unit array of rRNA gene units are needed for transcription, that R2 elements are active only when present in this transcription domain, and that most of the crossovers in the rDNA loci occur in this domain. These results suggest that the key to the long-term survival of R2 is the redistribution of rDNA units in the locus brought about by the crossovers that maintain sequence identity in all rDNA units.

Date: 2013
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pgen00:1003179

DOI: 10.1371/journal.pgen.1003179

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