R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA cotranscript
Open accessAbstract
The non-long terminal repeat (non-LTR) retrotransposon R2 is inserted into the 28S rRNA genes of many animals. Expression of the element appears to be by cotranscription with the rRNA gene unit. We show here that processing of the rRNA cotranscript at the 5' end of the R2 element in Drosophila simulans is rapid and utilizes an unexpected mechanism. Using RNA synthesized in vitro, the 5' untranslated region of R2 was shown capable of rapid and efficient self-cleavage of the 28S-R2 cotranscript. The 5' end generated in vitro by the R2 ribozyme was at the position identical to that found for in vivo R2 transcripts. The RNA segment corresponding to the R2 ribozyme could be folded into a double pseudoknot structure similar to that of the hepatitis delta virus (HDV) ribozyme. Remarkably, 21 of the nucleotide positions in and around the active site of the HDV ribozyme were identical in R2. R2 elements from other Drosophila species were also shown to encode HDV-like ribozymes capable of self-cleavage. Tracing their sequence evolution in the Drosophila lineage suggests that the extensive similarity of the R2 ribozyme from D. simulans to that of HDV was a result of convergent evolution, not common descent.
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R2 elements do not have their own promoters and therefore can be transcribed only as part of pre-rRNA.
“Along with unusually high specificity of integration, another peculiarity of R2 elements is that they do not have their own promoters and therefore can be transcribed only as a part of pre-rRNA (39–42).”
From Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon (2022) · cites this paper as [42]
The introductory passage says attempts to identify a promoter at the 5′ end of R2 have been unsuccessful and that R2 expression appears to depend on transcription of the rRNA unit. The Discussion describes R2 RNA as processed from an rRNA cotranscript. These passages support the proposed route of transcription, but do not establish that R2 has no promoter or can be transcribed only as part of pre-rRNA. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe R2 element integrates exclusively into the rDNA locus and is capable to be transcribed only as part of pre-rRNA.
“The R2 element integrates exclusively into the rDNA locus and is capable to be transcribed only as part of pre-rRNA (39–42).”
From Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon (2022) · cites this paper as [42]
The introduction (page unavailable) says that all active R2 copies reported to date occupy a conserved site in the 28S rRNA gene, and that R2 expression appears to depend on transcription of the rDNA unit containing it. The Results detect 28S–R2 cotranscripts, but the paper does not establish that every R2 insertion is in rDNA or that R2 can be transcribed only as part of pre-rRNA. (LLM, conf=0.86)
Experimental — accuracy not yet measuredFull-length R2 insertions encode a ribozyme that releases the 5′-end of the R2 transcript from the upstream 28S rRNA sequence during the autocatalytic reaction.
“Full-length R2 insertions encode a ribozyme, which releases the 5′-end of the R2 transcript from the upstream 28S rRNA sequence during the autocatalytic reaction (Figure 1A)”
From Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon (2022) · cites this paper as [42]
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Luan, D. D., & Eickbush, T. H. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.7.3882 · Cited by 219 · see citing works
Self-citationYe, J., & Eickbush, T. H. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01409-06 · Cited by 51 · cited 1× · see citing works
“This is an important point because only a limited number of the rDNA units within the locus, possibly only 30 to 40 units, are transcriptionally active (8, 38, 40) and thus only a small percentage of the R2 copies are transcribed.”
BackgroundSelf-citationZhou, J., & Eickbush, T. H. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000386 · Cited by 30 · see citing works
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Guerrero, P. A., & Maggert, K. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016401 · Cited by 51 · see citing works
Repression of interrupted and intact rDNA by the SUMO pathway in drosophila melanogaster
Luo, Y., Fefelova, E., Ninova, M., Chen, Y.-C. A., & Aravin, A. A. (2020) · eLife · doi:10.7554/elife.52416 · Cited by 19 · see citing works
Fefelova, E. A., Pleshakova, I. M., Mikhaleva, E. A., Pirogov, S. A., Poltorachenko, V. A., Abramov, Y. A., Romashin, D. D., Shatskikh, A. S., Blokh, R. S., Gvozdev, V. A., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkab1276 · Cited by 15 · see citing works
“Full-length R2 insertions encode a ribozyme, which releases the 5′-end of the R2 transcript from the upstream 28S rRNA sequence during the autocatalytic reaction (Figure 1A), whereas the mechanism of 3′-end formation of R2 RNA remains unclear (30,42).”
BackgroundRaje, H. S., Lieux, M. E., & DiMario, P. J. (2018) · Transcription · doi:10.1080/21541264.2018.1506682 · Cited by 13 · see citing works
The retrotransposon <i>R2</i> maintains <i>Drosophila</i> ribosomal DNA repeats
Nelson, J. O., Slicko, A., & Yamashita, Y. M. (2021) · doi:10.1101/2021.07.12.451825 · Cited by 7 · see citing works
- Authors
- Eickbush, D. G., & Eickbush, T. H.
- Affiliations
- University of Rochester (US)
- Corresponding author
- Eickbush, Thomas H.
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2010-07
- Volume
- 30
- Issue
- 13
- Pages
- 3142-3150
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC2897577
- OpenAlex
- W2164166224
- Cited by
- 106
- References
- 3
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 9 · 2023: 4 · 2022: 2 · 2021: 11 · 2020: 5 · 2019: 6 · 2018: 7 · 2017: 6 · 2016: 4 · 2015: 10 · 2014: 5 · 2013: 10 · 2012: 8
- FWCI
- 11.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM42790, R01GM042790)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- R2 retrotransposon, non-LTR retrotransposons, self-cleaving ribozymes, 28S rRNA gene, cotranscription, 5' end processing, Drosophila simulans, hepatitis delta virus ribozyme, pseudoknot, convergent evolution, sequence evolution, transposable elements
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Hepatitis Delta Virus, Drosophila, Molecular Sequence Data, Nucleic Acid Conformation, RNA, Ribosomal, 28S, RNA, Catalytic, Sequence Alignment, Retroelements, Evolution, Molecular, Terminal Repeat Sequences
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