DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Ty1

Boutabout, Mansour

doi:10.1093/nar/29.11.2217

Cited by 38 publications

(28 citation statements)

References 26 publications

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“…The observed mutation rate of 2.5 × 10 −5 bp per cycle suggested that Ty1 mutated as rapidly as retroviruses. The in vitro study involved steady state kinetics of misinsertion opposite A, T, G and C residues at defined primer-template sites (Boutabout et al, 2001). Ty1 RT was found to be less error prone than lentiviral RTs such as HIV-1, HIV-2 and EIAV and comparable to that of oncoretroviral RTs such as AMV.…”

Section: Saccharomyces Cerevisiae Ty1mentioning

confidence: 99%

The diversity of retrotransposons and the properties of their reverse transcriptases

2008

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A number of abundant mobile genetic elements called retrotransposons reverse transcribe RNA to generate DNA for insertion into eukaryotic genomes. Four major classes of retrotransposons are described here. First, the long-terminal-repeat (LTR) retrotransposons have similar structures and mechanisms to those of the vertebrate retroviruses. Genes that may enable these retrotransposons to leave a cell have been acquired by these elements in a number of animal and plant lineages. Second, the tyrosine recombinase retrotransposons are similar to the LTR retrotransposons except that they have substituted a recombinase for the integrase and recombine into the host chromosomes. Third, the non-LTR retrotransposons use a cleaved chromosomal target site generated by an encoded endonuclease to prime reverse transcription. Finally, the Penelope-like retrotransposons are not well understood but appear to also use cleaved DNA or the ends of chromosomes as primer for reverse transcription. Described in the second part of this review are the enzymatic properties of the reverse transcriptases (RTs) encoded by retrotransposons. The RTs of the LTR retrotransposons are highly divergent in sequence but have similar enzymatic activities to those of retroviruses. The RTs of the non-LTR retrotransposons have several unique properties reflecting their adaptation to a different mechanism of retrotransposition.

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Section: Saccharomyces Cerevisiae Ty1mentioning

confidence: 99%

The diversity of retrotransposons and the properties of their reverse transcriptases

2008

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“…These elements are believed to have diverged early in the evolution of LTR retrotransposons, well before retroviruses. Therefore, it is likely that the mechanism of self-priming represents an early form of initiating RTN in LTR retroelements (16), as it was advantageous for these retroelements to use a tRNA-independent mechanism of priming cDNA synthesis.The only RTs from LTR retrotransposons extensively studied in vitro were those of Ty1 and Ty3 that belong to different retrotransposon groups, the Pseudoviridae and the Metaviridae, respectively (4,8,23,24). We have recently expressed in bacteria an enzymatically active Tf1 RT and studied its basic biochemical properties (14).…”

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confidence: 99%

“…The only RTs from LTR retrotransposons extensively studied in vitro were those of Ty1 and Ty3 that belong to different retrotransposon groups, the Pseudoviridae and the Metaviridae, respectively (4,8,23,24). We have recently expressed in bacteria an enzymatically active Tf1 RT and studied its basic biochemical properties (14).…”

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confidence: 99%

The Reverse Transcriptase of the Tf1 Retrotransposon Has a Specific Novel Activity for Generating the RNA Self-Primer That Is Functional in cDNA Synthesis

Hizi

2008

J Virol

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The Tf1 retrotransposon of Schizosaccharomyces pombe represents a group of eukaryotic long terminal repeat (LTR) retroelements that, based on their sequences, were predicted to use an RNA self-primer for initiating reverse transcription while synthesizing the negative-sense DNA strand. This feature is substantially different from the one typical to retroviruses and other LTR retrotransposons that all exhibit a tRNA-dependent priming mechanism. Genetic studies have suggested that the self-primer of Tf1 can be generated by a cleavage between the 11th and 12th bases of the Tf1 RNA transcript. The in vitro data presented here show that recombinant Tf1 reverse transcriptase indeed introduces a nick at the end of a duplexed region at the 5 end of Tf1 genomic RNA, substantiating the prediction that this enzyme is responsible for generating this RNA self-primer. The 3 end of the primer, generated in this manner, can then be extended upon the addition of deoxynucleoside triphosphates by the DNA polymerase activity of the same enzyme, synthesizing the negativesense DNA strand. This functional primer must have been generated by the RNase H activity of Tf1 reverse transcriptase, since a mutant enzyme lacking this activity has lost its ability to generate the self-primer. It was also found here that the reverse transcriptases of human immunodeficiency virus type 1 and of murine leukemia virus do not exhibit this specific cleavage activity. In all, it is likely that the observed unique mechanism of self-priming in Tf1 represents an early advantageous form of initiating reverse transcription in LTR retroelements without involving cellular tRNAs.Long terminal repeat (LTR) retrotransposons are retrovirus-like elements found in a broad variety of eukaryotic cells (6,7,10). Their structure and mechanisms of propagation are related to retroviruses, and like them, they encode the Gag, protease, reverse transcriptase (RT), and integrase proteins. As with all retroviruses, the RTs of LTR retrotransposons are pivotal for converting the positive-sense, single-stranded RNA genome into a double-stranded and integration-competent viral DNA. This reverse transcription (RTN) process is catalyzed by two RT activities, DNA polymerase activity, which copies both RNA and DNA, and RNase H activity, which concomitantly cleaves the RNA in the DNA-RNA heteroduplex formed. In all retroviruses and LTR retrotransposons, the synthesis of negative-strand DNA is initiated from an RNA primer that is complementary to a specific genomic RNA sequence, the primer binding site (PBS), which is located near the 5Ј end of the RNA genome. It is well documented that this RNA primer is a specific cellular tRNA (for examples, see references 6, 7, 16, and 27).Interestingly, an alternative tRNA-independent priming mechanism was proposed for the LTR retrotransposon Tf1 of the fission yeast Schizosaccharomyces pombe by . This model suggests that a self-complementarity within the RNA genome allows intramolecular base pairing near the 5Ј end of the RNA, causing this end to ...

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“…In support of vertical radiation, pairwise comparisons of Tvv1 lTrs indicate that their pattern of similarity matches the successive divergence of the asterids and rosids followed by that of the clades within the rosids and the species within Solanum. nevertheless, the analysis may be biased by possible differing degrees of transpositional activity in the various species and clades, because for retrotransposons the error rates for replication via reverse transcription and as integral chromosomal components differ greatly (Gabriel et al 1996;Boutabout et al 2001;Abram et al 2010).…”

Section: Discussionmentioning

confidence: 99%

The Tvv1 retrotransposon family is conserved between plant genomes separated by over 100 million years

et al. 2014

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the Copia superfamily of lTr retrotransposons, from the genome of the wild potato Solanum demissum. Comparative analyses based on structure and sequence showed a high level of similarity of Tvv1_Sdem with Tvv1-VB, a retrotransposon previously described in the grapevine genome Vitis vinifera. extending the analysis to other species by in silico and in vitro approaches revealed the presence of Tvv1 family members in potato, tomato, and poplar genomes, and led to the identification of full-length copies of Tvv1 in these species. We were also able to identify polymorphism in UTl sequences between Tvv1_Sdem copies from wild and cultivated potatoes that are useful as molecular markers. Combining different approaches, our results suggest that the Tvv1 family of retrotransposons has a monophyletic origin and has been maintained in both the rosids and the asterids, the major clades of dicotyledonous plants, since their divergence about 100 MYA. To our knowledge, Tvv1 represents an unusual plant retrotransposon metapopulation comprising highly similar members disjointedly dispersed among very distant species. The twin features of Tvv1 presence in evolutionarily distant genomes and the diversity of its UTl region in each species make it useful as a source of robust molecular markers for diversity studies and breeding. IntroductionTransposable elements (Tes) have been found in virtually all eukaryotic species investigated so far. They are divided into two classes based on their means of transposition and replication; the DnA transposons (Class II) move by a "cut and paste" mechanism whereas retrotransposons (Class I) use a "copy and paste" strategy ). The retrotransposons are ubiquitous in the plant kingdom and Abstract Key message Combining several different approaches, we have examined the structure, variability, and distribution of Tvv1 retrotransposons. Tvv1 is an unusual example of a low-copy retrotransposon metapopulation dispersed unevenly among very distant species and is promising for the development of molecular markers. Abstract retrotransposons are ubiquitous throughout the genomes of the vascular plants, but individual retrotransposon families tend to be confined to the level of plant genus or at most family. This restricts the general applicability of a family as molecular markers. Here, we characterize a new plant retrotransposon named Tvv1_Sdem, a member of Communicated by P. Heslop-Harrison. Electronic supplementary materialThe online version of this article

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DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Ty1

Cited by 38 publications

References 26 publications

The diversity of retrotransposons and the properties of their reverse transcriptases

The diversity of retrotransposons and the properties of their reverse transcriptases

The Reverse Transcriptase of the Tf1 Retrotransposon Has a Specific Novel Activity for Generating the RNA Self-Primer That Is Functional in cDNA Synthesis

The Tvv1 retrotransposon family is conserved between plant genomes separated by over 100 million years

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