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The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus.

Zhou J, Eickbush TH - PLoS Genet. (2009)

Bottom Line: The two populations were found to have similar patterns of R2 activity.Instead R2 activity was best correlated with the distribution of elements within the rDNA locus.These data suggest a model in which frequent recombination within the rDNA locus continually redistributes R2-inserted units resulting in changing levels of R2 activity within individual loci and persistent R2 activity within the population.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Rochester, Rochester, New York, United States of America.

ABSTRACT
The pattern and frequency of insertions that enable transposable elements to remain active in a population are poorly understood. The retrotransposable element R2 exclusively inserts into the 28S rRNA genes where it establishes long-term, stable relationships with its animal hosts. Previous studies with laboratory stocks of Drosophila simulans have suggested that control over R2 retrotransposition resides within the rDNA loci. In this report, we sampled 180 rDNA loci of animals collected from two natural populations of D. simulans. The two populations were found to have similar patterns of R2 activity. About half of the rDNA loci supported no or very low levels of R2 transcripts with no evidence of R2 retrotransposition. The remaining half of the rDNA loci had levels of R2 transcripts that varied in a continuous manner over almost a 100-fold range and did support new retrotransposition events. Structural analysis of the rDNA loci in 18 lines that spanned the range of R2 transcript levels in these populations revealed that R2 number and rDNA locus size varied 2-fold; however, R2 activity was not readily correlated with either of these parameters. Instead R2 activity was best correlated with the distribution of elements within the rDNA locus. Loci with no activity had larger contiguous blocks of rDNA units free of R2-insertions. These data suggest a model in which frequent recombination within the rDNA locus continually redistributes R2-inserted units resulting in changing levels of R2 activity within individual loci and persistent R2 activity within the population.

Show MeSH
The rDNA locus of D. simulans and the site-specific retrotransposable elements, R1 and R2.The top panel shows the tandemly repeated rDNA transcription units with or without R1 and R2 insertions in the 28S rRNA gene. Every unit is composed of an 18S, 5.8S and 28S gene (black boxes) and transcribed spacer regions (white boxes). The R2 insertion site is located in the 28S rRNA gene 60 bp upstream of the R1 site. The bottom two diagrams show the R1 and R2 insertions in greater detail. The black boxes represent the 28S gene, the grey boxes represent the open reading frames of the R1 and R2 elements, and the white boxes represent the 5′ and 3′ untranslated regions of R1 and R2. ClaI, NotI, PstI and MspA1I restriction enzyme cleavage sites used in this report, and the locations of the hybridization probes used for the RNA blots (probe1) and genomic DNA blots (probes 2 and 3) are indicated. NotI cleaves only the R2 elements but not R1 or the rDNA units.
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pgen-1000386-g001: The rDNA locus of D. simulans and the site-specific retrotransposable elements, R1 and R2.The top panel shows the tandemly repeated rDNA transcription units with or without R1 and R2 insertions in the 28S rRNA gene. Every unit is composed of an 18S, 5.8S and 28S gene (black boxes) and transcribed spacer regions (white boxes). The R2 insertion site is located in the 28S rRNA gene 60 bp upstream of the R1 site. The bottom two diagrams show the R1 and R2 insertions in greater detail. The black boxes represent the 28S gene, the grey boxes represent the open reading frames of the R1 and R2 elements, and the white boxes represent the 5′ and 3′ untranslated regions of R1 and R2. ClaI, NotI, PstI and MspA1I restriction enzyme cleavage sites used in this report, and the locations of the hybridization probes used for the RNA blots (probe1) and genomic DNA blots (probes 2 and 3) are indicated. NotI cleaves only the R2 elements but not R1 or the rDNA units.

Mentions: The ribosomal RNA (rRNA) genes of eukaryotes are composed of hundreds to thousands of tandemly repeated units (the rDNA loci). Mature 18S, 5.8S and 28S rRNAs are processed from the single transcript of each rDNA unit. Frequent recombination (unequal crossovers) within these rDNA loci removes sequence variation, a process referred to as concerted evolution [12]. Concerted evolution is so efficient almost no nucleotide sequence variation exists between the different rDNA units of a locus [13],[14]. Given this ability of the locus to rid itself of variation, it is surprising that the rDNA locus is home to many specialized transposable elements [15]–[17]. For example, R1 and R2 are non-LTR retrotransposable elements that insert specifically into the 28S rRNA genes (Figure 1). R1 and R2 are highly adept at maintaining themselves in the rDNA locus. They are found in most arthropods and appear to have been vertically inherited since the origin of the phylum [18],[19]. Remarkably, R2 elements appear to have been inserting into the same site of the large subunit rRNA gene since near the origin of metazoans [17]. Within many insect species a large fraction of the rDNA units are inserted by R1 and R2 suggesting rapid rates of insertion [20]–[22]. Even though these many inserted units can not make functional 28S rRNA, the host does not appear unduly affected because in most organisms many more rDNA units are encoded than are needed for the production of rRNA [23].


The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus.

Zhou J, Eickbush TH - PLoS Genet. (2009)

The rDNA locus of D. simulans and the site-specific retrotransposable elements, R1 and R2.The top panel shows the tandemly repeated rDNA transcription units with or without R1 and R2 insertions in the 28S rRNA gene. Every unit is composed of an 18S, 5.8S and 28S gene (black boxes) and transcribed spacer regions (white boxes). The R2 insertion site is located in the 28S rRNA gene 60 bp upstream of the R1 site. The bottom two diagrams show the R1 and R2 insertions in greater detail. The black boxes represent the 28S gene, the grey boxes represent the open reading frames of the R1 and R2 elements, and the white boxes represent the 5′ and 3′ untranslated regions of R1 and R2. ClaI, NotI, PstI and MspA1I restriction enzyme cleavage sites used in this report, and the locations of the hybridization probes used for the RNA blots (probe1) and genomic DNA blots (probes 2 and 3) are indicated. NotI cleaves only the R2 elements but not R1 or the rDNA units.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2637433&req=5

pgen-1000386-g001: The rDNA locus of D. simulans and the site-specific retrotransposable elements, R1 and R2.The top panel shows the tandemly repeated rDNA transcription units with or without R1 and R2 insertions in the 28S rRNA gene. Every unit is composed of an 18S, 5.8S and 28S gene (black boxes) and transcribed spacer regions (white boxes). The R2 insertion site is located in the 28S rRNA gene 60 bp upstream of the R1 site. The bottom two diagrams show the R1 and R2 insertions in greater detail. The black boxes represent the 28S gene, the grey boxes represent the open reading frames of the R1 and R2 elements, and the white boxes represent the 5′ and 3′ untranslated regions of R1 and R2. ClaI, NotI, PstI and MspA1I restriction enzyme cleavage sites used in this report, and the locations of the hybridization probes used for the RNA blots (probe1) and genomic DNA blots (probes 2 and 3) are indicated. NotI cleaves only the R2 elements but not R1 or the rDNA units.
Mentions: The ribosomal RNA (rRNA) genes of eukaryotes are composed of hundreds to thousands of tandemly repeated units (the rDNA loci). Mature 18S, 5.8S and 28S rRNAs are processed from the single transcript of each rDNA unit. Frequent recombination (unequal crossovers) within these rDNA loci removes sequence variation, a process referred to as concerted evolution [12]. Concerted evolution is so efficient almost no nucleotide sequence variation exists between the different rDNA units of a locus [13],[14]. Given this ability of the locus to rid itself of variation, it is surprising that the rDNA locus is home to many specialized transposable elements [15]–[17]. For example, R1 and R2 are non-LTR retrotransposable elements that insert specifically into the 28S rRNA genes (Figure 1). R1 and R2 are highly adept at maintaining themselves in the rDNA locus. They are found in most arthropods and appear to have been vertically inherited since the origin of the phylum [18],[19]. Remarkably, R2 elements appear to have been inserting into the same site of the large subunit rRNA gene since near the origin of metazoans [17]. Within many insect species a large fraction of the rDNA units are inserted by R1 and R2 suggesting rapid rates of insertion [20]–[22]. Even though these many inserted units can not make functional 28S rRNA, the host does not appear unduly affected because in most organisms many more rDNA units are encoded than are needed for the production of rRNA [23].

Bottom Line: The two populations were found to have similar patterns of R2 activity.Instead R2 activity was best correlated with the distribution of elements within the rDNA locus.These data suggest a model in which frequent recombination within the rDNA locus continually redistributes R2-inserted units resulting in changing levels of R2 activity within individual loci and persistent R2 activity within the population.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Rochester, Rochester, New York, United States of America.

ABSTRACT
The pattern and frequency of insertions that enable transposable elements to remain active in a population are poorly understood. The retrotransposable element R2 exclusively inserts into the 28S rRNA genes where it establishes long-term, stable relationships with its animal hosts. Previous studies with laboratory stocks of Drosophila simulans have suggested that control over R2 retrotransposition resides within the rDNA loci. In this report, we sampled 180 rDNA loci of animals collected from two natural populations of D. simulans. The two populations were found to have similar patterns of R2 activity. About half of the rDNA loci supported no or very low levels of R2 transcripts with no evidence of R2 retrotransposition. The remaining half of the rDNA loci had levels of R2 transcripts that varied in a continuous manner over almost a 100-fold range and did support new retrotransposition events. Structural analysis of the rDNA loci in 18 lines that spanned the range of R2 transcript levels in these populations revealed that R2 number and rDNA locus size varied 2-fold; however, R2 activity was not readily correlated with either of these parameters. Instead R2 activity was best correlated with the distribution of elements within the rDNA locus. Loci with no activity had larger contiguous blocks of rDNA units free of R2-insertions. These data suggest a model in which frequent recombination within the rDNA locus continually redistributes R2-inserted units resulting in changing levels of R2 activity within individual loci and persistent R2 activity within the population.

Show MeSH