Sequence analysis of 28S ribosomal DNA from the amphibian<i>Xenopus laevis</i>

Ware, Vassie C.; Tague, Brian W.; Clark, C. Graham; Gourse, Richard L.; Brand, Reindert C.; Gerbi, Susan A.

doi:10.1093/nar/11.22.7795

Cited by 161 publications

(107 citation statements)

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“…Arrows indicate positions of X. laevis 18S and 28S rRNA markers. X. laevis 18S rRNA is 1,825 nucleotides long (55), and the 28S rRNA is 4,110 nucleotides long (77).…”

Section: Resultsmentioning

confidence: 99%

Structure and expression of STK, a src-related gene in the simple metazoan Hydra attenuata.

Bosch¹,

Unger²,

Fisher³

et al. 1989

Mol. Cell. Biol.

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Both cDNA clones and a genomic DNA clone encoding a 509-amino-acid protein that is 64% similar to chicken pp60ocsr were isolated from the simple metazoan Hydra attenuata. We have designated this gene STK, for src-type kinase. Features of the amino acid sequence of the protein encoded by the STK gene suggest that it is likely to be myristoylated and regulated by phosphorylation in a manner similar to that found for pp6Oc-sr. The genomic sequence encoding the protein was found to be interrupted by at least two introns, one of which was located in a position identical to that of one of the introns in the chicken src gene. The STK gene was expressed during early development of H. attenuata and at high levels in the epithelial cells of adult polyps. Probing of Hydra proteins with an antibody to phosphotyrosine indicated that the major phosphotyrosinecontaining protein in H. attenuata may be the STK protein itself. H. attenuata is the simplest organism from which a protein-tyrosine kinase gene has been isolated. The presence of such a gene in the evolutionarily ancient phylum Cnidaria suggests that protein-tyrosine kinase genes arose concomitantly with or shortly after the appearance of multicellular organisms.The src proto-oncogene encodes a protein-tyrosine kinase (pp6Oc-src) whose role in the cell is not yet known. src is the prototype of a group of closely related genes that make up the so-called src family (J. A. Cooper, in B. Kemp and P. F. Alewood, ed., Peptides and Protein Phosphorylation, in press). One approach to understanding the function of pp60c-src and other members of the src family is to define the level of organismal complexity at which src-like proteintyrosine kinases arose during evolution. Such information would be useful for narrowing the scope of possible functions for these proteins and may point to additional useful biological systems for biochemical and molecular genetic analysis of these proteins. To date, src-type genes have been isolated from various vertebrates and from Drosophila melanogaster (reviewed in reference 28).Schartl and Barnekow (57) and Barnekow and Muller (3) have shown that a protein-tyrosine kinase activity immunoprecipitable with pp6Ov-src antiserum from rabbits with Rous sarcoma virus-induced tumors is present in a wide range of metazoans, including the marine hydroid Hydractinia. Such activity was not found in protozoans or plants (57). The subsequent identification of such a protein-tyrosine kinase activity in the simplest metazoans, the sponges, lead to the suggestion that the presence of a src-like kinase is directly related to requirements imposed by multicellularity (4). Levin et al. (44) reported the isolation of two genes from yeast cells, KIN] and KIN2, that encode 117-and 126-kilodalton (kDa) proteins with some amino acid sequence motifs considered characteristic of protein-tyrosine kinases. Additional analysis of the sequences of these two proteins suggested, however, that they are more closely related to serine/threonine kinases than to protein-tyrosine kin...

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“…Arrows indicate positions of X. laevis 18S and 28S rRNA markers. X. laevis 18S rRNA is 1,825 nucleotides long (55), and the 28S rRNA is 4,110 nucleotides long (77).…”

Section: Resultsmentioning

confidence: 99%

Structure and expression of STK, a src-related gene in the simple metazoan Hydra attenuata.

Bosch¹,

Unger²,

Fisher³

et al. 1989

Mol. Cell. Biol.

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“…However, eukaryotic rRNA has additional blocks of sequences relative to prokaryotic rRNA designated as "expansion segments" (ES) (Ware et al 1983;Clark et al 1984;Hassouna et al 1984). These ES are interspersed throughout the various domains of rRNA secondary structure core at specific, conserved sites (Fig.…”

Section: Introductionmentioning

confidence: 99%

Eukaryote-specific rRNA expansion segments function in ribosome biogenesis

Ramesh

Woolford

2016

RNA

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The secondary structure of ribosomal RNA (rRNA) is largely conserved across all kingdoms of life. However, eukaryotes have evolved extra blocks of rRNA sequences, relative to those of prokaryotes, called expansion segments (ES). A thorough characterization of the potential roles of ES remains to be done, possibly because of limitations in the availability of robust systems to study rRNA mutants. We sought to systematically investigate the potential functions, if any, of the ES in 25S rRNA of Saccharomyces cerevisiae by deletion mutagenesis. We deleted 14 of the 16 different eukaryote-specific ES in yeast 25S rRNA individually and assayed their phenotypes. Our results show that all but two of the ES tested are necessary for optimal growth and are required for production of 25S rRNA, suggesting that ES play roles in ribosome biogenesis. Further, we classified expansion segments into groups that participate in early nucleolar, middle, and late nucleoplasmic steps of ribosome biogenesis, by assaying their pre-rRNA processing phenotypes. This study is the first of its kind to systematically identify the functions of eukaryote-specific expansion segments by showing that they play roles in specific steps of ribosome biogenesis. The catalog of phenotypes we identified, combined with previous investigations of the roles ribosomal proteins in large subunit biogenesis, leads us to infer that assembling ribosomes are composed of distinct RNA and protein structural neighborhood clusters that participate in specific steps of ribosome biogenesis.

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“…The more prominent ones have been identified as expansion segments (7,46), divergent domains (27), or variable regions (17). The variability of some regions is such that closely related organisms such as mice and rats show many sequence differences (26), and sequence differences are even detected in different copies of the rRNA genes (rDNAs) from a single organism (25).…”

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confidence: 99%

An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence.

1994

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Regions extremely variable in size and sequence occur at conserved locations in eukaryotic rRNAs. The functional importance of one such region was determined by gene reconstruction and replacement in Tetrahymena thermophila. Deletion of the D8 region of the large-subunit rRNA inactivates T. thermophila rRNA genes (rDNA): transformants containing only this type of rDNA are unable to grow. Replacement with an unrelated sequence of similar size or a variable region from a different position in the rRNA also inactivated the rDNA. Mutant rRNAs resulting from such constructs were present only in precursor forms, suggesting that these rRNAs are deficient in either processing or stabilization of the mature form. Replacement with D8 regions from three other organisms restored function, even though the sequences are very different. Thus, these D8 regions share an essential functional feature that is not reflected in their primary sequences. Similar tertiary structures may be the quality these sequences share that allows them to function interchangeably.Although much of the secondary structure of rRNA is evolutionarily conserved, these portions are interspersed with discrete variable regions at conserved positions within the structure (18). The more prominent ones have been identified as expansion segments (7,46), divergent domains (27), or variable regions (17). The variability of some regions is such that closely related organisms such as mice and rats show many sequence differences (26), and sequence differences are even detected in different copies of the rRNA genes (rDNAs) from a single organism (25). These regions are absent in most eubacteria and archaebacteria and present in most eukaryotes (19,46), although exceptions to this rule have recently been found (4, 10, 43). The functional role of variable regions has not been identified. While their absence from most eubacteria suggests that they are dispensable, their almost universal presence in eukaryotes implies that they may be important in these organisms.Two models for the evolution of rRNA both imply that variable regions initially had no functional role. Some rRNAs are fragmented (2,5,12,13,15,36,39,45,47) (44). Comparison of rRNA sequences from diverse phyla offers support for the secondary structure model of most of the LSU rRNA but is uninformative for variable regions because they are so divergent. Secondary structure models for variable regions have been proposed based on the assumption that, in addition to having a low free energy, a model must be structurally similar for all species (26). Comparing the sequences of closely related species has recently produced more-refined models (12,20).No functional role has been defined for any variable region. However, some pertinent evidence does exist. The D2 and D12 regions of the LSU rRNA in Tetrahymena thennophila tolerate insertion mutations with no apparent diminution of rRNA function in vivo, while insertions in the D8 region totally obliterate rRNA function (40a, 41). In Saccharomyces cerevisiae, rRNAs beari...

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Sequence analysis of 28S ribosomal DNA from the amphibianXenopus laevis

Abstract: We have determined the complete nucleotide sequence of Xenopus laevis 28S rDNA (4110 bp

Cited by 161 publications

References 52 publications

Structure and expression of STK, a src-related gene in the simple metazoan Hydra attenuata.

Structure and expression of STK, a src-related gene in the simple metazoan Hydra attenuata.

Eukaryote-specific rRNA expansion segments function in ribosome biogenesis

An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence.

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