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Processing of preribosomal RNA in Saccharomyces cerevisiae

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Most, if not all RNAs, are transcribed as precursors that require processing to gain functionality. Ribosomal RNAs (rRNA) from all organisms undergo both exo‐ and endonucleolytic processing. Also, in all organisms, rRNA processing occurs inside large preribosomal particles and is coupled to nucleotide modification, folding of the precursor rRNA (pre‐rRNA), and assembly of the ribosomal proteins (r‐proteins). In this review, we focus on the processing pathway of pre‐rRNAs of cytoplasmic ribosomes in the yeast Saccharomyces cerevisiae, without doubt, the organism where this pathway is best characterized. We summarize the current understanding of the rRNA maturation process, particularly focusing on the pre‐rRNA processing sites, the enzymes responsible for the cleavage or trimming reactions and the different mechanisms that monitor and regulate the pathway. Strikingly, the overall order of the various processing steps is reasonably well conserved in eukaryotes, perhaps reflecting common principles for orchestrating the concomitant events of pre‐rRNA processing and ribosome assembly. WIREs RNA 2015, 6:191–209. doi: 10.1002/wrna.1267 This article is categorized under: RNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes Translation > Ribosome Biogenesis RNA Processing > rRNA Processing
Pre‐rRNA processing in S. cerevisiae. (a) Structure of an rDNA repeat unit. Each unit contains a large element encoding 18S, 5.8S, and 25S rRNAs, which is transcribed by RNAPI, and a short element encoding 5S rRNA, which is transcribed by RNAPIII. Nontranscribed, external and internal spacers (NTS, ETS, and ITS, respectively) are indicated. The sequences for the mature rRNA species are shown as bars and the spacers as lines (NTSs are shown thinner than ETSs or ITSs). Transcription start sites are shown as red arrows and transcription stop sites (T1 and T5S) are shown as small purple boxes. The distinct processing sites are indicated. (b) Scheme of the pre‐rRNA processing pathway, which is further described in the text. The nucleases responsible of the endonucleolytic cleavages (red) and exonucleolytic trimmings (green) are highlighted. Note that some endonucleases have not yet been identified.
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Secondary structure models for the S. cerevisiae ITS2. Two conformations have been proposed for ITS2, (a) the ring conformation and (b) the hairpin conformation. The positions of the sites C1, C1′, C2, E as well as the 3′ end extended 5.8S + 30, 6S (+8) and 5.8S + 5 species are indicated. Note that the nuclease responsible for endonucleolytic cleavage at site C2 remains to be identified. Processing from site C2 to site C1 occurs by 5′–3′ trimming by either Rat1, Rrp17, or Xrn1. Processing from site C2 to site E occurs by 3′–5′ trimming by the concerted action of different exonucleases. Note that all these processing reaction are represented only in the hairpin structure. See text for further details.
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Secondary structure model for the S. cerevisiae ITS1. The representation has been adapted from that proposed by Yeh et al. The positions of the sites A2, A3, and D are shown, as well as the endonucleases involved in the respective cleavages. The positions of the sites B1L and B1S are also shown. Note that while processing from site A3 to B1S occurs exonucleolytically by a reaction performed by the redundant exonucleases Rat1, Rrp17, or Xrn1, cleavage at site B1L occurs endonucleolytically by a so‐far unknown endonuclease. See text for further details.
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Secondary structure model for the S. cerevisiae 5′ ETS. The representation has been adapted from that proposed by Yeh and Lee. The positions of the sites A0 and A1, which are cleaved endonucleolytically are indicated. Note that the endonuclease(s) responsible of these cleavages are currently unknown. Sites binding to the U3 snoRNA and suspected to bind to snR10 are also highlighted (shaded encircled nucleotides in green or red, respectively).
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Secondary structure model for the S. cerevisiae 3′ ETS. Rnt1 cleavage sites are indicated. The 3′ end of mature 25S rRNA (blue) is generated by Rex1‐dependent 3′–5′ exonuclease trimming from the B0 site. See text for further details.
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Secondary structure model for S. cerevisiae pre‐5S rRNA. The secondary structure as well as the residue and helix (H) numbers was taken from the Comparative RNA Web Site (www.rna.ccbb.utexas.edu/). Note that formation of 3′ end of mature 5S rRNA relies on a Rex1‐dependent 3′–5′ exonucleolytic step. See text for further details.
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RNA Processing > rRNA Processing
Translation > Ribosome Biogenesis
RNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes

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