Alteration of the RNA polymerase specificity of U3 snRNA genes during evolution and in vitro

Kiss, Tamás; Marshallsay, Christopher; Filipowicz, Witold

doi:10.1016/0092-8674(91)90469-f

Cited by 113 publications

(80 citation statements)

References 49 publications

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“…Alternatively, RNA polymerase III transcripts could directly participate in pre-rRNA processing. This is the case for U3 snRNA in plants (16) or RNase MRP RNA in mammals (43), but the yeast counterparts are made by RNA polymerase II (reference 14 and this work). RNase P RNA is another candidate, as it affects 5.8S rRNA maturation in vivo (4) and is an RNA polymerase III transcript in organisms ranging from yeasts (17) to humans (2).…”

Section: Discussionmentioning

confidence: 99%

Cross Talk between tRNA and rRNA Synthesis in Saccharomyces cerevisiae

Briand

Navarro

Gadal

et al. 2001

Molecular and Cellular Biology

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Temperature-sensitive RNA polymerase III (rpc160-112 and rpc160-270) mutants were analyzed for the synthesis of tRNAs and rRNAs in vivo, using a double-isotopic-labeling technique in which cells are pulselabeled with [ 33 P]orthophosphate and coextracted with [ 3 H]uracil-labeled wild-type cells. Individual RNA species were monitored by Northern blot hybridization or amplified by reverse transcription. These mutants impaired the synthesis of RNA polymerase III transcripts with little or no influence on mRNA synthesis but also largely turned off the formation of the 25S, 18S, and 5.8S mature rRNA species derived from the common 35S transcript produced by RNA polymerase I. In the rpc160-270 mutant, this parallel inhibition of tRNA and rRNA synthesis also occurred at the permissive temperature (25°C) and correlated with an accumulation of 20S pre-rRNA. In the rpc160-112 mutant, inhibition of rRNA synthesis and the accumulation of 20S pre-rRNA were found only at 37°C. The steady-state rRNA/tRNA ratio of these mutants reflected their tRNA and rRNA synthesis pattern: the rpc160-112 mutant had the threefold shortage in tRNA expected from its preferential defect in tRNA synthesis at 25°C, whereas rpc160-270 cells completely adjusted their rRNA/tRNA ratio down to a wild-type level, consistent with the tight coupling of tRNA and rRNA synthesis in vivo. Finally, an RNA polymerase I (rpa190-2) mutant grown at the permissive temperature had an enhanced level of pre-tRNA, suggesting the existence of a physiological coupling between rRNA synthesis and pre-tRNA processing.The existence of three nuclear transcription systems is documented for all eukaryotes investigated so far. RNA polymerase I synthesizes the three largest rRNAs, RNA polymerase II produces mRNAs and many noncoding RNAs, and RNA polymerase III makes tRNAs and 5S rRNA, as well as a few small noncoding RNAs. Exceptions to this transcriptional specialization are rare and mostly concern noncoding RNA species that can be produced by either RNA polymerase II or III, depending on the phylum considered (reference 39 and references therein). Given its universality, the triplication of the transcriptional apparatus must provide a major selective advantage to the eukaryotic cell, probably by facilitating the separate control of mRNA, rRNA, and tRNA synthesis in response to changes in the environment or in the cell growth rate. On the other hand, RNA polymerases I and III deliver matching amounts of tRNAs and rRNAs to the protein synthesis machinery and may thus need to operate in a closely coordinated way (references 21, 38, and 39 and references therein). In fact, the extent to which the three nuclear RNA polymerases are coordinated relative to each other remains largely undetermined, although this is presumably a key aspect of the transcriptional regulation of growth.Yeast (Saccharomyces cerevisiae) is a particularly convenient model organism to study transcription and its regulation. Its three nuclear RNA polymerases are biochemically and genetically well characterized ...

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Section: Discussionmentioning

confidence: 99%

Cross Talk between tRNA and rRNA Synthesis in Saccharomyces cerevisiae

Briand

Navarro

Gadal

et al. 2001

Molecular and Cellular Biology

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“…2 Taken together, these findings suggest that plant 7SL genes belong to the type 3 pol III-transcribed genes, which have their promoters situated upstream of the transcribed region. Furthermore, the 7SL upstream promoter is identical to the promoters present in the U-snRNA genes in plants (26,30,(37)(38)(39). In humans the 7SL RNA gene contains a type 4 promoter, with essential elements positioned both upstream and within the coding region (15)(16)(17)(18).…”

Section: -Gsmentioning

confidence: 98%

An upstream U-snRNA gene-like promoter is required for transcription of theArabidopsis thaliana7SL RNA gene

Heard

Filipowicz

Marques³

et al. 1995

Nucl Acids Res

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The genes transcribed by RNA polymerase (pol)111 can be placed into four distinct groups based on the nature and position of their promoter elements. In the higher eukaryotes equivalent genes usually belong to the same sub-type of pol Hi promoters and there are few examples of genes which have changed promoter type during evolution. In this work we demonstrate that the promoter of the Arabidopsis thaliana 7SL RNA gene is located upstream of the coding region and is identical to the promoters of pol III-specific plant U-small nuclear RNA (U-snRNA) genes. Sequence analysis of two different 7SL genes from A.thaliana revealed that both genes contain two sequence elements in their 5' flanking regions identical in sequence and position to the highly conserved USE and TATA elements of the pol III-transcribed plant U-snRNA genes. Mutational analysis of these elements in the At7SL-2 gene indicates that the USE and TATA elements are both necessary and account for >90°% of the transcriptional activity of this gene in transfected plant protoplasts. Within the coding region of both genes there is a sequence element which is a 10/11 nt match to the consensus B-box element of tRNA genes, however, this element is not important for gene activity. These findings distinguish the plant genes from the human 7SL gene, which has both intemal and upstream promoter elements and its upstream elements are different from those found in the human U-snRNA genes.

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“…However, deletion of a single nucleotide from the 3' end of human U1 snRNA, which would maintain the 3' stem, also curtails import, suggesting that for U1 and U2 the structural signal for transport is more complicated than the mere presence of a 3'-terminal stem (Neumann de Vegvar and Dahlberg 1990). Kiss et al (1991) have presented convincing evidence that the U3 snRNA in plants is transcribed by RNA polymerase III and does not possess a trimethyl cap structure. They argue that this conversion from synthesis by polymerase II to III probably occurred after the evolution of plants.…”

Section: U3 Defines a Unique Class Of Snrna Import Signalsmentioning

confidence: 99%

“…It follows that the pathway for biogenesis of plant U3 must be different from what we have deduced here for mammalian U3 snRNA. Interestingly, when the plant U3 gene is manipulated so that it is transcribed by RNA polymerase II, although the U3 snRNA binds Fb and acquires a trimethylated cap structure, it does not become part of a larger complex that is thought to function in rRNA processing (Kiss et al 1991). Clearly, therefore, the pathway of U3 snRNP biogenesis does affect its ability to be utilized correctly, and the alternate pathway for biogenesis evolved by mammalian cells is incapable of achieving functional U3 complexes in plants.…”

Section: U3 Defines a Unique Class Of Snrna Import Signalsmentioning

confidence: 99%

Distinct molecular signals for nuclear import of the nucleolar snRNA, U3.

Baserga¹,

Gilmore-Hebert²,

Yang³

1992

Genes Dev.

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Export to the cytoplasm of U3 RNA transcribed from a rat U3 gene injected into the nucleus of Xenopus oocytes indicates that the biogenesis of U3 RNA, like that of the previously studied Sm-precipitable nucleoplasmic snRNAs (U1, U2, U4, and US), includes a cytoplasmic phase. The regulation of import of the U3 snRNA into the nucleus has been analyzed by injection of synthetic human U3 transcripts into the cytoplasm of Xenopus oocytes. Binding of the major autoantigenic protein of the U3 snRNP, fibriUarin, and cap trimethylation can occur in the cytoplasm, but neither are required for import. The 3'-terminal 13 nucleotides are required for optimal import and cap trimethylation and participate in a phylogenetically conserved U3 structural element, a short 3'-terminal stem. An artificial construct containing the 3'-terminal 13 nucleotides, including the 3'-terminal stem, but only 56 nucleotides of the 217 nucleotides in U3, appears to be sufficient for import. The presence of the 3'-terminal stem in all snRNAs known to be imported suggests that it might be a universal element required for nuclear import.

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Alteration of the RNA polymerase specificity of U3 snRNA genes during evolution and in vitro

Cited by 113 publications

References 49 publications

Cross Talk between tRNA and rRNA Synthesis in Saccharomyces cerevisiae

Cross Talk between tRNA and rRNA Synthesis in Saccharomyces cerevisiae

An upstream U-snRNA gene-like promoter is required for transcription of theArabidopsis thaliana7SL RNA gene

Distinct molecular signals for nuclear import of the nucleolar snRNA, U3.

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