A General Secondary‐Structure Model for Procaryotic and Eucaryotic RNAs of the Small Ribosomal Subunits

Abstract

A consensus on the folding of the Escherichia coli 16-S ribosomal RNA is emerging and several complete nucleotide sequences of small ribosomal subunit RNAs, covering diverse types of organisms and organelles, are now available. We therefore investigated the extent of both nucleotide sequence and secondary structure conservation that may exist between the E. coli 16-S RNA and other ribosomal RNAs. All the RNA molecules examined could be folded into secondary structure schemes that illustrated remarkable preservation of many structural motifs as well as striking nucleotide sequence conservation compared with the E. coli molecule. This study presents a unitary scheme for the structural organization of the small ribosomal subunit RNAs. The evolutionary constraints on both primary and secondary structures most likely reveal the basic role of some restricted RNA regions in the function of the ribosome.The universal function of ribosomes is to decode the genetic message and to catalyze peptidyl bond formation. Since the sequence of ribosomal RNAs appears to change very slowly in the course of evolution, Woese and his collaborators have undertaken phylogenetic comparison from extensive analysis of T I ribonuclease-generated oligonucleotides of the small ribosomal subunit RNA from a large variety of organisms and organelles [I -41. These studies provided the first evidence for the existence of nucleotide sequence homologies among the various molecules, reflecting the strong evolutionary pressure imposed by their basic function. It seems likely that the secondary structure of the ribosomal RNA molecule (or at least part of this structure) is highly constrained as well as already observed for tRNA and 5-S RNA molecules.At present, several complete nucleotide sequences of small ribosomal subunit RNAs have been determined. They cover diverse types of organisms or organelles: (a) bacterial 16-S RNAs from Escherichia coli [5, 61 and Proteus vulgaris [7], (b) chloroplastic 16-S RNA from Zea mays [S], (c) cytoplasmic 18-S RNA from Succhuromyces cerevisiae [9] and Xenopus laevis [lo], (d) mitochondrial 12-S RNAs from human placenta [Ill and mouse [12], and mitochondrial 15-S RNA from yeast (S. cerevisiae) [I 31. A consensus on the folding of the E. coli 16-S RNA, supported by phylogenetic and topographical data, is now emerging . There is strong evidence that bacterial 16-S RNAs are organized in a common folding pattern [7, 141. In this paper, we investigate the extent of similarities and dissimilarities, in terms of primary and secondary structures, between E. coli 16-S RNA and the other ribosomal RNAs from evolutionary distant species. We find a rather high degree of sequence conservation. Furthermore, a large number of secondary structure elements proposed for E. coli 16-S RNA appear to be conserved in those of the other species. Some of them are even preserved in all the molecules examined so far and are therefore good candidates for being universal structures. In addition, nucleotide residues are strictly conserved at eq...

Sequence of the 3′‐terminal domain of mouse 18 S rRNA

“…The first complete sequence of this domain of a mammalian 18 S rRNA shows a striking homology (97%) with the other vertebrate sequence available, Xenopus laevis [19]. The comparison of the mouse sequence with other prokaryotic [21] or eukaryotic [22,23] sequences reinforces the view of a critical functional role of this 3'-terminal domain of small subunit rRNA molecule; this is again indicated by the conservation of a common basic RNA folding pattern from prokaryotes [ 15,16] to mouse, as reported earlier for yeast and Xenopus [20].…”

“…Among eukaryotes, yeast [ 18] and Xenopus [ 19] are the only complete 18 S rRNA sequences published so far; their comparison has revealed extensive stretches of high homology interspersed with heterologous tracts while conserved sequences with prokaryotes are clearly restricted to the 3'-terminal region of the molecule. A remarkable conservation of secondary structure features of these two eukaryotic rRNAs was also apparent from comparison with E. coli 16 S rRNA [20].…”

“…A large number of secondary structure features appear to be conserved from E. coli to yeast and Xenopus 18 S rRNA [20]. Fig.4 shows that the 3'-terminal domain of mouse 18 S rRNA can also be folded in a structure very similar to prokaryotic 16 S rRNA.…”

“…The scarcity of eukaryotic rRNA sequences available so far made it difficult to propose with a high degree of confidence a definite folding pattern for the rather divergent regions of the molecule [20]. In this regard, structure (II), between nucleotides 48-159, is particularly interesting because it spans the more divergent region of this domain for the previously sequenced eukaryotic rRNAs.…”

Structure of E. coli 16S RNA elucidated by psoralen crosslinking

“…On the basis of these data, Noller & Woese (1981) and Stiegler et al (1981) have proposed a general secondary structure model for all small subunit RNAs. Zwieb et al (1981) have also proposed a general model based on this evidence as well as UV crosslinking (Zwieb & Brimacombe, 1980), and denaturation studies (Ross & Brimacombe, 1979;Glotz & .Brimacombe, 1980).…”