RNA degradation by the plant RNA exosome involves both phosphorolytic and hydrolytic activities

Sikorska, Natalia; Zuber, Hélène; Gobert, Anthony; Lange, Heike; Gagliardi, Dominique

doi:10.1038/s41467-017-02066-2

Cited by 33 publications

(35 citation statements)

References 58 publications

(78 reference statements)

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“…It appears that the reported P 1 site is not an endonucleolytic cleavage site, because the expected P 1 -P9 fragments have not been detected (Figure 3). Instead, the accumulation of smaller and heterogeneous fragments mapping around P 1 suggest that fragments between P and P9 are generated by exoribonucleolytic degradation (Lange et al, 2011;Sikorska et al, 2017).…”

Section: Transcription Of 45s Rrna Genesmentioning

confidence: 99%

“…Moreover, the nine-subunit exosome core has a distributive phosphorolytic activity involved in the degradation of P-P 1 products (161, 168, 176, and 186 nucleotides) and the processing of 5.8S pre-rRNA. Therefore, the plant RNA exosome harbors a unique combination of hydrolytic and phosphorolytic ribonucleolytic activities, in contrast to exosome complexes in yeast and animal cells (Sikorska et al, 2017).…”

Section: Processing Of Pre-rrna: Two Alternative Pathwaysmentioning

confidence: 99%

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Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

2019

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The transcription of 18S, 5.8S, and 18S rRNA genes (45S rDNA), cotranscriptional processing of pre-rRNA, and assembly of mature rRNA with ribosomal proteins are the linchpins of ribosome biogenesis. In yeast (Saccharomyces cerevisiae) and animal cells, hundreds of pre-rRNA processing factors have been identified and their involvement in ribosome assembly determined. These studies, together with structural analyses, have yielded comprehensive models of the pre-40S and pre-60S ribosome subunits as well as the largest cotranscriptionally assembled preribosome particle: the 90S/small subunit processome. Here, we present the current knowledge of the functional organization of 45S rDNA, pre-rRNA transcription, rRNA processing activities, and ribosome assembly factors in plants, focusing on data from Arabidopsis (Arabidopsis thaliana). Based on yeast and mammalian cell studies, we describe the ribonucleoprotein complexes and RNA-associated activities and discuss how they might specifically affect the production of 40S and 60S subunits. Finally, we review recent findings concerning pre-rRNA processing pathways and a novel mechanism involved in a ribosome stress response in plants

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Section: Transcription Of 45s Rrna Genesmentioning

confidence: 99%

Section: Processing Of Pre-rrna: Two Alternative Pathwaysmentioning

confidence: 99%

Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

2019

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“…RRP41-GFP lines were made with constructs comprising the genomic sequence of RRP41 including 1000bp upstream of the translation start site and were previously described in 6 . All other GFP-fusion proteins were expressed from the UBIQUITIN 10 promoter.…”

Section: Methodsmentioning

confidence: 99%

“…Whilst the overall structure and function of the RNA exosome is conserved, both the composition and enzymatic activities of exosome complexes vary among organisms. For example, most non-plant Exo9s including those in yeast and human are catalytically inactive 5 , whereas plant Exo9s have retained a phosphorolytic activity originating from its prokaryotic ancestor 6 . This unique phosphorolytic activity of plant Exo9 acts in combination with the hydrolytic activities provided by RRP6 and DIS3 6 .…”

mentioning

confidence: 99%

“…For example, most non-plant Exo9s including those in yeast and human are catalytically inactive 5 , whereas plant Exo9s have retained a phosphorolytic activity originating from its prokaryotic ancestor 6 . This unique phosphorolytic activity of plant Exo9 acts in combination with the hydrolytic activities provided by RRP6 and DIS3 6 . Another exception among RNA exosomes is the association of human Exo9 with functionally distinct DIS3L and DIS3 proteins, only the latter of which is conserved in yeast and plants 3,7 .…”

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confidence: 99%

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RST1 and RIPR connect the cytosolic RNA exosome to the Ski complex in Arabidopsis

Lange

Ndecky

Gómez-Díaz

et al. 2019

Preprint

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21The RNA exosome is a key 3'-5' exoribonuclease with an evolutionarily conserved structure 22The Ski complex consists of the MTR4-related RNA helicase SKI2, the tetratricopeptide 1 repeat protein SKI3 and two copies of the WD40-repeat protein SKI8 [31][32][33] . Association of the 2 Ski complex with the exosome core complex requires an additional protein, SKI7 34 . In yeast, 3 the genes encoding Ski7 and Hbs1, which binds to Dom34 (PELOTA in humans and plants) 4for the release of stalled ribosomes 35 , arose from a whole genome duplication event. In other 5 eukaryotes including mammals and plants, the SKI7 and HBS1 proteins are produced by 6 alternative splicing from a single locus [36][37][38] . 7The Ski complex is conserved in Arabidopsis thaliana 39 , but its physical association with 8 the exosome core has not been investigated yet. An initial experiment to affinity-capture 9 factors associated with the Arabidopsis exosome identified the homologue of DIS3 and two 10 nuclear RNA helicases, AtMTR4 and its closely related homologue HEN2 23 . In addition, 11Arabidopsis Exo9 systematically co-purified with a 1840 amino acid ARM repeat protein of 12 unknown molecular function named RESURRECTION 1 (RST1) 23 . RST1 was originally 13identified in a genetic screen for factors involved in the biosynthesis of epicuticular waxes 40 . 14 Epicuticular waxes are a protective layer of aliphatic very long chain (VLC) hydrocarbons 15 that cover the outer surface of land plants 41,42 . rst1 mutants have less wax on floral stems than 16 wild-type plants, and about 70% of the seeds produced by rst1 mutants are shrunken due to 17 aborted embryogenesis 40 . The molecular function of RST1 remains unknown. Interestingly, 18 one of the two RRP45 exosome core subunits encoded in the Arabidopsis genome, named 19 RRP45B or CER7 (for ECERIFERUM 7) was also identified in a genetic screen aimed at 20 identifying enzymes or regulators of wax biosynthesis 43 . The wax-deficient phenotype of 21 rrp45b/cer7 mutants (cer7 from now on) is suppressed by mutations in genes encoding RNA 22

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SKI complex: A multifaceted cytoplasmic RNA exosome cofactor in mRNA metabolism with links to disease, developmental processes, and antiviral responses

et al. 2023

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RNA stability and quality control are integral parts of gene expression regulation. A key factor shaping eukaryotic transcriptomes, mainly via 3′–5′ exoribonucleolytic trimming or degradation of diverse transcripts in nuclear and cytoplasmic compartments, is the RNA exosome. Precise exosome targeting to various RNA molecules requires strict collaboration with specialized auxiliary factors, which facilitate interactions with its substrates. The predominant class of cytoplasmic RNA targeted by the exosome are protein‐coding transcripts, which are carefully scrutinized for errors during translation. Normal, functional mRNAs are turned over following protein synthesis by the exosome or by Xrn1 5′–3′‐exonuclease, acting in concert with Dcp1/2 decapping complex. In turn, aberrant transcripts are eliminated by dedicated surveillance pathways, triggered whenever ribosome translocation is impaired. Cytoplasmic 3′–5′ mRNA decay and surveillance are dependent on the tight cooperation between the exosome and its evolutionary conserved co‐factor—the SKI (superkiller) complex (SKIc). Here, we summarize recent findings from structural, biochemical, and functional studies of SKIc roles in controlling cytoplasmic RNA metabolism, including links to various cellular processes. Mechanism of SKIc action is illuminated by presentation of its spatial structure and details of its interactions with exosome and ribosome. Furthermore, contribution of SKIc and exosome to various mRNA decay pathways, usually converging on recycling of ribosomal subunits, is delineated. A crucial physiological role of SKIc is emphasized by describing association between its dysfunction and devastating human disease—a trichohepatoenteric syndrome (THES). Eventually, we discuss SKIc functions in the regulation of antiviral defense systems, cell signaling and developmental transitions, emerging from interdisciplinary investigations.This article is categorized under: RNA Turnover and Surveillance > Turnover/Surveillance Mechanisms RNA Turnover and Surveillance > Regulation of RNA Stability RNA Interactions with Proteins and Other Molecules > RNA‐Protein Complexes

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RNA degradation by the plant RNA exosome involves both phosphorolytic and hydrolytic activities

Cited by 33 publications

References 58 publications

Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

RST1 and RIPR connect the cytosolic RNA exosome to the Ski complex in Arabidopsis

SKI complex: A multifaceted cytoplasmic RNA exosome cofactor in mRNA metabolism with links to disease, developmental processes, and antiviral responses

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