The intervening sequence of the ribosomal RNA gene is highly conserved between two<i>Tetra-hymena</i>species

Kan, Nancy C.; Gall, Joseph G.

doi:10.1093/nar/10.9.2809

Cited by 55 publications

(20 citation statements)

References 19 publications

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“…In addition, single base changes at positions 51 and 116 result in the conversion of a G-U to an AU base pair, preserving the structure. Major differences between the two sequences occur at the ends of three of the hairpins (f, h, and k), as already noted by Kan and Gall (6). Because of their location, these deletion-substitutions do not disrupt the core structure of the molecule.…”

Section: Secondary Structure Of Thementioning

confidence: 51%

“…Both linear and circular forms of the IVS RNA appear to be rapidly degraded in the nucleus and not exported to the cytoplasm (4). The presence of stop codons in all possible reading frames (5,6) also makes it unlikely that the excised IVS could serve as a mRNA. Splicing of the Tetrahymena pre-rRNA is a novel case of an autocatalytic reaction that, at least in vitro, requires no enzyme or other protein (7).…”

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confidence: 99%

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Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: structural homology with fungal mitochondrial intervening sequences.

Cech¹,

Tanner²,

Tinoco³

et al. 1983

Proc. Natl. Acad. Sci. U.S.A.

206

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Splicing of the ribosomal RNA precursor of Tetrahymena is an autocatalytic reaction, requiring no enzyme or other protein in vitro. The structure of the intervening sequence (IVS) appears to direct the cleavage/ligation reactions involved in prerRNA splicing and IVS cyclization. We have probed this structure by treating the linear excised IVS RNA under nondenaturing conditions with various single-and double-strand-specific nucleases and then mapping the cleavage sites by using sequencing gel electrophoresis. A computer program was then used to predict the lowest-free-energy secondary structure consistent with the nuclease cleavage data. The resulting structure is appealing in that the ends of the IVS are in proximity; thus, the IVS can help align the adjacent coding regions (exons) for ligation, and IVS cyclization can occur. The Tetrahymena IVS has several sequences in common with those of fungal mitochondrial mRNA and rRNA IMSs, sequences that by genetic analysis are known to be important cisacting elements for splicing of the mitochondrial RNAs. In the predicted structure of the Tetrahymena IVS, these sequences interact in a pairwise manner similar to that postulated for the mitochondrial IVSs. These findings suggest a common origin of some nuclear and mitochondrial introns and common elements in the mechanism of their splicing.Genes coding for rRNA are interrupted by intervening sequences (IVSs) in several species of Tetrahymena and in Physarum polycephalum (1). These split genes are transcribed to give an IVS-containing pre-rRNA which is then spliced in the nucleus (1). In the case of Tetrahymena, the IVS is excised as a unique linear molecule which is subsequently cyclized (2, 3). Both linear and circular forms of the IVS RNA appear to be rapidly degraded in the nucleus and not exported to the cytoplasm (4). The presence of stop codons in all possible reading frames (5, 6) also makes it unlikely that the excised IVS could serve as a mRNA. Splicing of the Tetrahymena pre-rRNA is a novel case of an autocatalytic reaction that, at least in vitro, requires no enzyme or other protein (7). It remains possible that proteins accelerate the rate of splicing or perhaps even regulate the process in vivo.RNA splicing is also required for the expression of genes coding for the large rRNA and various mRNAs in the mitochondria of fungi. Many of the mitochondrial IVSs contain long open reading frames in phase with the upstream exon. The occurrence of trans-recessive splicing-defective mutants that map within three of the cytochrome b gene (cob) introns (8) has led to the proposal of intron-encoded maturases (9). The introns in yeast and Neurospora large mitochondrial rRNA genes also contain long open reading frames (10, 11); these apparently do not encode maturases because splicing of yeast mitochondrial rRNA continues in the absence of protein synthesis (12). The occurrence of nuclear mutants in mitochondrial mRNA and rRNA splicing (13, 14) makes it seem likely that proteins other than the maturases are required...

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Section: Secondary Structure Of Thementioning

confidence: 51%

mentioning

confidence: 99%

Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: structural homology with fungal mitochondrial intervening sequences.

Cech¹,

Tanner²,

Tinoco³

et al. 1983

Proc. Natl. Acad. Sci. U.S.A.

206

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“…Pneumocystis carinii contains an intron in the rDNA encoding the small-subunit rRNA (18), but neither it nor the rDNA of this organism has been extensively characterized. Several but not all Tetrahymena species and strains contain the well-known self-splicing intron in extrachromosomal rDNA coding for the large-subunit rRNA (22,23,38). Depending on the strain, Physarum polycephalum contains two or three group I introns in the extrachromosomal rDNA coding for the large-subunit rRNA (28,30,31).…”

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confidence: 99%

Characterization of I-Ppo, an intron-encoded endonuclease that mediates homing of a group I intron in the ribosomal DNA of Physarum polycephalum.

Muscarella¹,

Ellison²,

Ruoff³

et al. 1990

Mol. Cell. Biol.

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A novel and only recently recognized class of enzymes is composed of the site-specific endonucleases encoded by some group I introns. We have characterized several aspects of I-Ppo, the endonuclease that mediates the mobility of intron 3 in the ribosomal DNA of Physarum polycephalum. This intron is unique among mobile group I introns in that it is located in nuclear DNA. We found that I-Ppo is encoded by an open reading frame in the 5' half of intron 3, upstream of the sequences required for self-splicing of group I introns. Either of two AUG initiation codons could start this reading frame, one near the beginning of the intron and the other in the upstream exon, leading to predicted polypeptides of 138 and 160 amino acid residues. The longer polypeptide was the major form translated in vitro in a reticulocyte extract. From nuclease assays of proteins synthesized in vitro with partially deleted DNAs, we conclude that both polypeptides possess endonuclease activity. We also have expressed I-Ppo in Escherichia coli, using a bacteriophage T7 RNA polymerase expression system. The longer polypeptide also was the predominant form made in this system. It showed enzymatic activity in bacteria in vivo, as demonstrated by the cleavage of a plasmid carrying the target site. Like several other intron-encoded endonucleases, I-Ppo makes a four-base staggered cut in its ribosomal DNA target sequence, very near the site where intron 3 becomes integrated in crosses of intron 3-containing and intron 3-lacking Physarum strains.Group I introns are defined by the presence of conserved sequences and structural elements (reviewed in reference 2). Many group I introns can undergo autocatalytic splicing (self-splicing) in vitro, as first described for the prototypic intron of Tetrahymena cells (5). Of the more than 60 group I introns that have been identified to date (4), most are present in the DNA of mitochondria or chloroplasts or in the DNA of T-even bacteriophage. In only three organisms have group I introns been observed in nuclear genes, and in each of these they are located in the DNA coding for ribosomal RNA (rDNA). Pneumocystis carinii contains an intron in the rDNA encoding the small-subunit rRNA (18), but neither it nor the rDNA of this organism has been extensively characterized. Several but not all Tetrahymena species and strains contain the well-known self-splicing intron in extrachromosomal rDNA coding for the large-subunit rRNA (22,23,38). Depending on the strain, Physarum polycephalum contains two or three group I introns in the extrachromosomal rDNA coding for the large-subunit rRNA (28,30,31). Some group I introns have been found to be mobile elements. They rapidly and efficiently spread in vivo from a locus that contains the intron (I+) to the same locus in a homologous gene that lacks the intron (I). This process, which has been termed intron homing (15,16), is initiated by a double-strand break in the I-locus that is introduced by a site-specific endonuclease encoded by the intron itself. The actual homing of the ...

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“…Like the Ri element of insects, the Ascaris element is flanked by a 14-bp duplication of rDNA sequences. In Tetrahymena species, a 0. rupts all 26S rRNA genes at a position which corresponds to 3 bp 5' of the insect R2 element (22,50). Unlike the Ri and R2 elements of insects, the Tetrahymena rDNA disruption is a self-splicing intron, eliminated during the processing of rDNA transcripts (24).…”

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confidence: 99%

The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme.

Burke¹,

Calalang²,

Eickbush³

1987

Mol. Cell. Biol.

129

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Two classes of DNA elements interrupt a fraction of the rRNA repeats of Bombyx mon. We have analyzed by genomic blotting and sequence analysis one class of these elements which we have named R2. These elements occupy approximately 9% of the rDNA units of B. mon and appear to be homologous to the type II rDNA insertions detected in Drosophila melanogaster. Approximately 25 copies of R2 exist within the B. mori genome, of which at least 20 are located at a precise location within otherwise typical rDNA units. Nucleotide sequence analysis has revealed that the 4.2-kilobase-pair R2 element has a single large open reading frame, occupying over 82% of the total length of the element. The central region of this 1,151-amino-acid open reading frame shows homology to the reverse transcriptase enzymes found in retroviruses and certain transposable elements. Amino acid homology of this region is highest to the mobile line 1 elements of mammals, followed by the mitochondrial type II introns of fungi, and the pol gene of retroviruses. Less homology exists with transposable elements of D. melanogaster and Saccharomyces cerevisiae. Two additional regions of sequence homology between LI and R2 elements were also found outside the reverse transcriptase region. We suggest that the R2 elements are retrotransposons that are site specific in their insertion into the genome. Such mobility would enable these elements to occupy a small fraction of the rDNA units of B. mori despite their continual elimination from the rDNA locus by sequence turnover.A fraction of the 28S ribosomal genes in several insect species is interrupted by segments of non-rDNA approximately 5 kilobases (kb) in length (see the review by Beckingham [3]). Based on the nucleotide sequences of their junction regions, these insertions have been divided into two classes. Type I elements have been reported in Drosophila virilis (34), D. melanogaster (7, 37), Calliphora erythrocephala (43), and Bombyx mori (12,16). They interrupt the 28S rRNA gene at a location approximately two-thirds of the distance from the 5' end of the gene and are flanked by a 14-base-pair (bp) duplication of rDNA sequences. Type II elements have only been reported in D. melanogaster (7,37) and B. mori (12,16). They interrupt the 28S gene 75 bp upstream of the type I elements and do not contain flanking duplications of rDNA sequences. In D. melanogaster, rDNA units containing either of these elements are transcribed at a significantly lower level than are the remaining rDNA units (20,23,28). To be consistent with the singleletter nomenclature frequently used to describe repetitive or transposable DNA elements and to avoid possible confusion with the type I and II intron sequences of fungal mitochondrial DNAs, we suggest that these elements be referred to as the Ri (type I) and R2 (type II) elements (R referring to rDNA units).Disruption of the large rRNA genes has also been detected in noninsect species. In Ascaris lumbricoides, a 4.5-kb element interrupts a small fraction of the 26S rRNA genes at ...

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The intervening sequence of the ribosomal RNA gene is highly conserved between twoTetra-hymenaspecies

Cited by 55 publications

References 19 publications

Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: structural homology with fungal mitochondrial intervening sequences.

Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: structural homology with fungal mitochondrial intervening sequences.

Characterization of I-Ppo, an intron-encoded endonuclease that mediates homing of a group I intron in the ribosomal DNA of Physarum polycephalum.

The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme.

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