Evolutionary changes in the higher order structure of the ribosomal 5S RNA (original) (raw)
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The evolutionary history of the structure of 5S ribosomal RNA
2009
5S rRNA is the smallest nucleic acid component of the large ribosomal subunit, contributing to ribosomal assembly, stability, and function. Despite being a model for the study of RNA structure and RNA-protein interactions, the evolution of this universally conserved molecule remains unclear. Here, we explore the history of the three-domain structure of 5S rRNA using phylogenetic trees that are reconstructed directly from molecular structure. A total of 46 structural characters describing the geometry of 666 5S rRNAs were used to derive intrinsically rooted trees of molecules and molecular substructures. Trees of molecules revealed the tripartite nature of life. In these trees, superkingdom Archaea formed a paraphyletic basal group, while Bacteria and Eukarya were monophyletic and derived. Trees of molecular substructures supported an origin of the molecule in a segment that is homologous to helix I (a domain), its initial enhancement with helix III (b domain), and the early formation of the three-domain structure typical of modern 5S rRNA in Archaea. The delayed formation of the branched structure in Bacteria and Eukarya lends further support to the archaeal rooting of the tree of life. Remarkably, the evolution of molecular interactions between 5S rRNA and associated ribosomal proteins inferred from a census of domain structure in hundreds of genomes established a tight relationship between the age of 5S rRNA helices and the age of ribosomal proteins. Results suggest 5S rRNA originated relatively quickly but quite late in evolution, at a time when primordial metabolic enzymes and translation machinery were already in place. The molecule therefore represents a late evolutionary addition to the ribosomal ensemble that occurred prior to the early diversification of Archaea.
European Journal of Biochemistry, 1979
The ribonucleoprotein complex between 5-S RNA and its binding protein (5-S RNA . protein complex) of yeast ribosomes was released from 60-S subunits with 25 mM EDTA and the protein component was purified by chromatography on DEAE-cellulose. This protein, designated YL3 (MI = 36000 on dodecylsulfate gels), was relatively insoluble in neutral solutions (pH 4-9) and migrated as one of four acidic 60-S subunit proteins when analyzed by the Kaltschmidt and Wittman two-dimensional gel system. Amino acid analyses indicated lower amounts of lysine and arginine than most ribosomal proteins. Sequence homology was observed in the N terminus of YL3, and two prokaryotic 5-S RNA binding proteins, EL 18 from Escherichia coliand HL 13 from Halobacterium cutirubrum : Ala'-
MGG Molecular & General Genetics, 1976
Based on the comparative analyses of the primary structure of 5 S RNAs from 19 organisms, a secondary structure model of 5S RNA is proposed. 5S RNA has essentially the same structure among all prokaryotic species. The same is true for eukaryotic 5 S RNAs. Prokaryotic and eukaryotic 5 S RNAs are also quite similar to each other, except for a difference in a specific region. By comparing the nucleotide alignment from the juxtaposed 5S RNA secondary structures, a phylogenic tree of nineteen organisms was constructed. The time of divergence between prokaryotes and eukaryotes was estimated to be 2.5 x 109 years ago (minimum estimate: 2.1 x 109).
Proceedings of the National Academy of Sciences, 1977
Reconstitution experiments showed that the two Escherichia coli 5S RNA binding proteins L18 and 125 form a specific complex with yeast 5.8S RNA and not with yeast 5S RNA. The yeast 5.8S RNA-E. coli protein complex was found to exhibit ATPase and GTPase activities that had previously been observed for the E. coli 5S RNA-protein complex. The tetranucleotide UpUpCpG, which is an analog of the tRNA fragment TpsppCpG, interacted strongly with 5S RNA-protein complexes from E. coli and Bacillus stearothermopy i us and weakly with yeast 5.8S RNA. UpUpCpG didnot bind to E. coli, B. stearothermophilus, or yeast 5S RNA or to the yeast 5.8S RNA-E. coli protein complex. It is suggested that 5.8S RNA evolved from prokaryotic 5S RNA and that the latter two RNAs are related and have similar functions in protein synthesis. Large ribosomal subunits of prokaryotic and eukaryotic organisms contain 5S RNA; eukaryotic ribosomes in addition contain 5.8S RNA (for recent review, see ref.
Binding sites of ribosomal proteins on prokaryotic 5S RNAs: a study with ribonucleases
Biochemistry, 1982
The binding sites of ribosomal proteins L18 and L25 on 5s RNA from Escherichia coli were probed with ribonucleases A, TI, and T2 and a double helix specific cobra venom endonuclease. The results for the protein-RNA complexes, which were compared with those for the free RNA [Douthwaite, S., & Garrett, R. A. (1981) Biochemistry 20, 7301-73071, reveal an extensive interaction site for protein L18 and a more localized one for L25. Generally comparable results, with a few important differences, were obtained in a study of the binding sites of the two E. coli proteins on Bacillus stearothermophilus 5s RNA. Several protein-induced changes in the RNA structures were identified; some are
Structure of the ribosome-associated 5ยท 8 S ribosomal RNA
Journal of molecular biology, 1983
The structure of the 5-8 S ribosomal RNA in rat liver ribosomes was probed by comparing dimethyl sulfate-reactive sites in whole ribosomes, 60 S subunits, the 5.8 S-28 S rRNA complex and the free 5"8 S rRNA under conditions of salt and temperature that permit protein synthesis in vitro. Differences in reactive sites between the free and both the 28 S rRNA and 60S subunit-associated 5-8 S rRNA show that significant conformational changes occur when the molecule interacts with its cognate 28 S rRNA and as the complex is further integrated into the ribosomal structure. These results indicate that, as previously suggested by phylogenetic comparisons of the secondary structure, only the "G+C-rich" stem may remain unaltered and a universal structure is probably present only in the whole ribosome or 60S subunit. Further comparisons with the ribosomeassociated molecule indicate that while the 5.8 S rRNA may be partly localized in the ribosomal interface, four cytidylic acid residues, Cs6, C10o, Ct2 ~ and C12s, remain reactive even in whole ribosomes. In contrast, the cytidylic acid residues in the 5 S rRNA are not accessible in either the 60 S subunit or the intact ribosome. The nature of the structural rearrangements and potential sites of interaction with the 28 S rRNA and ribosomal proteins are discussed. Although the 5.8 S rRNA of eukaryotic ribosomes was identified over a decade ago (Pene et al., 1968; Weinberg & Penman, 1968), little is yet known about this molecule's role in ribosome structure or function. At least two suggestions for its function, i.e. roles in transfer RNA binding (Nishikawa & Takemura, 1974; Wrede & Erdmann, 1977) or subunit interaction (Ulbrich et al., 1979; Toots et al., 1979), have been postulated but these are entirely based on indirect evidence and must be tested experimentally before any conclusions are reached. Recently, as a possible step towards direct information about the molecule's role in the ribosome, we examined the topography of this RNA in ribosomes and ribosomal subunits using diethyl pyrocarbonate reactivity as a probe (Lo & Nazar, 1981,1982). The results suggested a number of interesting features, including conformational changes and the possibility that part of the molecule may be within the ribosomal interface. The study, however, had two major limitations: only regions containing adenylic and certain guanylic acid residues could be probed and artifacts resulting from diethyl pyrocarbonate reactivity with proteins could not be ruled out entirely. To overcome these limitations, a parallel study has been conducted using a different chemical probe, dimethyl sulfate. The results strongly support the conclusions drawn earlier, but describe new regions of accessibility and further indicate that the changes in the ribosomeassociated molecule are considerably more extensive than previously believed. Active ribosomes were prepared from male Wistar rat livers essentially as described by Rendi & Hultin (1960) and subunits were prepared from the purified ribosomes using the methods of Terao & Ogata (1970) with minor modifications
Nucleic Acids Research, 1981
A general secondary structure is proposed for the 5S RNA of prokaryotic ribosomes, based on helical energy filtering calculations. We have considered all secondary structures that are common to 17 different prokaryotic 5S RNAs and for each 5S sequence calculated the (global) minimum energy secondary structure (300,000 common structures are possible for each sequence). The 17 different minimum energy secondary structures all correspond, with minor differences, to a single, secondary structure model. This is strong evidence that this general 5S folding pattern corresponds to the secondary structure of the functional 5S rRNA. The general 5S secondary structure is forked and in analogy with the cloverleaf of tRNA is named the 'wishbone' model. It contains 8 double helical regions; one in the stem, four in the first, or constant arm, and three in the second arm. Four of these double helical regions are present in a model earlier proposed (1) and four additional regions not proposed by them are presented here. In the minimum energy general structure, the four helices in the constant arm are exactly 15 nucleotide pairs long. These helices are stacked in the sequences from gram-positive bacteria and probably stacked in gram-negative sequences as well. In sequences from gram-positive bacteria the length of the constant arm is maintained at 15 stacked pairs by an unusual minimum energy interaction involving a C26-G57 base pair intercalated between two adjacent helical regions. 1885