Origin of nascent lineages and the mechanisms used to prime second-strand DNA synthesis in the R1 and R2 retrotransposons of Drosophila

Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have been used to address two questions concerning these elements. First, to what extent is the evolution of these elements subject to the concer...

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Published inGenome biology Vol. 10; no. 5; pp. R49 - 2199
Main Authors Stage, Deborah E, Eickbush, Thomas H
Format Journal Article
LanguageEnglish
Published England BioMed Central 05.05.2009
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ISSN1474-760X
1465-6906
1474-760X
1465-6914
DOI10.1186/gb-2009-10-5-r49

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Abstract Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have been used to address two questions concerning these elements. First, to what extent is the evolution of these elements subject to the concerted evolution process that is responsible for sequence homogeneity among the different copies of rRNA genes? Second, how precise are the target DNA cleavages and priming of DNA synthesis used by these elements? Most copies of R1 and R2 in each species were found to exhibit less than 0.2% sequence divergence. However, in many species evidence was obtained for the formation of distinct sublineages of elements, particularly in the case of R1. Analysis of the hundreds of R1 and R2 junctions with the 28S gene revealed that cleavage of the first DNA strand was precise both in location and the priming of reverse transcription. Cleavage of the second DNA strand was less precise within a species, differed between species, and gave rise to variable priming mechanisms for second strand synthesis. These findings suggest that the high sequence identity amongst R1 and R2 copies is because all copies are relatively new. However, each active element generates its own independent lineage that can eventually populate the locus. Independent lineages occur more often with R1, possibly because these elements contain their own promoter. Finally, both R1 and R2 use imprecise, rapidly evolving mechanisms to cleave the second strand and prime second strand synthesis.
AbstractList Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have been used to address two questions concerning these elements. First, to what extent is the evolution of these elements subject to the concerted evolution process that is responsible for sequence homogeneity among the different copies of rRNA genes? Second, how precise are the target DNA cleavages and priming of DNA synthesis used by these elements?BACKGROUNDMost arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have been used to address two questions concerning these elements. First, to what extent is the evolution of these elements subject to the concerted evolution process that is responsible for sequence homogeneity among the different copies of rRNA genes? Second, how precise are the target DNA cleavages and priming of DNA synthesis used by these elements?Most copies of R1 and R2 in each species were found to exhibit less than 0.2% sequence divergence. However, in many species evidence was obtained for the formation of distinct sublineages of elements, particularly in the case of R1. Analysis of the hundreds of R1 and R2 junctions with the 28S gene revealed that cleavage of the first DNA strand was precise both in location and the priming of reverse transcription. Cleavage of the second DNA strand was less precise within a species, differed between species, and gave rise to variable priming mechanisms for second strand synthesis.RESULTSMost copies of R1 and R2 in each species were found to exhibit less than 0.2% sequence divergence. However, in many species evidence was obtained for the formation of distinct sublineages of elements, particularly in the case of R1. Analysis of the hundreds of R1 and R2 junctions with the 28S gene revealed that cleavage of the first DNA strand was precise both in location and the priming of reverse transcription. Cleavage of the second DNA strand was less precise within a species, differed between species, and gave rise to variable priming mechanisms for second strand synthesis.These findings suggest that the high sequence identity amongst R1 and R2 copies is because all copies are relatively new. However, each active element generates its own independent lineage that can eventually populate the locus. Independent lineages occur more often with R1, possibly because these elements contain their own promoter. Finally, both R1 and R2 use imprecise, rapidly evolving mechanisms to cleave the second strand and prime second strand synthesis.CONCLUSIONSThese findings suggest that the high sequence identity amongst R1 and R2 copies is because all copies are relatively new. However, each active element generates its own independent lineage that can eventually populate the locus. Independent lineages occur more often with R1, possibly because these elements contain their own promoter. Finally, both R1 and R2 use imprecise, rapidly evolving mechanisms to cleave the second strand and prime second strand synthesis.
Comparative analysis of 12 Drosophila genomes reveals insights into the evolution and mechanism of integration of R1 and R2 retrotransposons.
BACKGROUND: Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have been used to address two questions concerning these elements. First, to what extent is the evolution of these elements subject to the concerted evolution process that is responsible for sequence homogeneity among the different copies of rRNA genes? Second, how precise are the target DNA cleavages and priming of DNA synthesis used by these elements? RESULTS: Most copies of R1 and R2 in each species were found to exhibit less than 0.2% sequence divergence. However, in many species evidence was obtained for the formation of distinct sublineages of elements, particularly in the case of R1. Analysis of the hundreds of R1 and R2 junctions with the 28S gene revealed that cleavage of the first DNA strand was precise both in location and the priming of reverse transcription. Cleavage of the second DNA strand was less precise within a species, differed between species, and gave rise to variable priming mechanisms for second strand synthesis. CONCLUSIONS: These findings suggest that the high sequence identity amongst R1 and R2 copies is because all copies are relatively new. However, each active element generates its own independent lineage that can eventually populate the locus. Independent lineages occur more often with R1, possibly because these elements contain their own promoter. Finally, both R1 and R2 use imprecise, rapidly evolving mechanisms to cleave the second strand and prime second strand synthesis.
Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have been used to address two questions concerning these elements. First, to what extent is the evolution of these elements subject to the concerted evolution process that is responsible for sequence homogeneity among the different copies of rRNA genes? Second, how precise are the target DNA cleavages and priming of DNA synthesis used by these elements? Most copies of R1 and R2 in each species were found to exhibit less than 0.2% sequence divergence. However, in many species evidence was obtained for the formation of distinct sublineages of elements, particularly in the case of R1. Analysis of the hundreds of R1 and R2 junctions with the 28S gene revealed that cleavage of the first DNA strand was precise both in location and the priming of reverse transcription. Cleavage of the second DNA strand was less precise within a species, differed between species, and gave rise to variable priming mechanisms for second strand synthesis. These findings suggest that the high sequence identity amongst R1 and R2 copies is because all copies are relatively new. However, each active element generates its own independent lineage that can eventually populate the locus. Independent lineages occur more often with R1, possibly because these elements contain their own promoter. Finally, both R1 and R2 use imprecise, rapidly evolving mechanisms to cleave the second strand and prime second strand synthesis.
ArticleNumber R49
Author Stage, Deborah E
Eickbush, Thomas H
AuthorAffiliation 1 Biology Department, University of Rochester, 213 Hutchison, Rochester NY, 14627-0211, USA
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Snippet Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila genomes have...
BACKGROUND: Most arthropods contain R1 and R2 retrotransposons that specifically insert into the 28S rRNA genes. Here, the sequencing reads from 12 Drosophila...
Comparative analysis of 12 Drosophila genomes reveals insights into the evolution and mechanism of integration of R1 and R2 retrotransposons.
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StartPage R49
SubjectTerms Animals
arthropods
concerted evolution
DNA
DNA Replication
Drosophila
Drosophila - classification
Drosophila - genetics
genes
Genome, Insect
loci
Phylogeny
Retroelements
retrotransposons
reverse transcription
ribosomal RNA
sequence analysis
Title Origin of nascent lineages and the mechanisms used to prime second-strand DNA synthesis in the R1 and R2 retrotransposons of Drosophila
URI https://www.ncbi.nlm.nih.gov/pubmed/19416522
https://www.proquest.com/docview/2000158455
https://www.proquest.com/docview/67537009
https://pubmed.ncbi.nlm.nih.gov/PMC2718515
Volume 10
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