The Existence and Localization of Nuclear snoRNAs in Arabidopsis thaliana Revisited

Streit, Deniz; Shanmugam, Thiruvenkadam; Garbelyanski, Asen; Simm, Stefan; Schleiff, Enrico

doi:10.3390/plants9081016

Cited by 19 publications

(23 citation statements)

References 90 publications

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“…138 C/D snoRNA in the FIB2-IP fraction were also detected among 154 C/D snoRNA recently reported in a nuclear fraction from Arabidopsis cell suspension culture [59]. However, 16 others C/D snoRNAs detected in the nuclear fraction were not found to be associated to FIB2 in our conditions (Table S2).…”

Section: Discussionsupporting

confidence: 57%

Mapping rRNA 2’-O-methylations and identification of C/D snoRNAs in Arabidopsis thaliana plants

et al. 2021

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In all eukaryotic cells, the most abundant modification of ribosomal RNA (rRNA) is methylation at the ribose moiety (2ʹ-O-methylation). Ribose methylation at specific rRNA sites is guided by small nucleolar RNAs (snoRNAs) of C/D-box type (C/D snoRNA) and achieved by the methyltransferase Fibrillarin (FIB).Here we used the Illumina-based RiboMethSeq approach for mapping rRNA 2ʹ-O-methylation sites in A. thaliana Col-0 (WT) plants. This analysis detected novel C/D snoRNA-guided rRNA 2ʹ-O-methylation positions and also some orphan sites without a matching C/D snoRNA. Furthermore, immunoprecipitation of Arabidopsis FIB2 identified and demonstrated expression of C/D snoRNAs corresponding to majority of mapped rRNA sites. On the other hand, we show that disruption of Arabidopsis Nucleolin 1 gene (NUC1), encoding a major nucleolar protein, decreases 2ʹ-O-methylation at specific rRNA sites suggesting functional/structural interconnections of 2ʹ-O-methylation with nucleolus organization and plant development. Finally, based on our findings and existent database sets, we introduce a new nomenclature system for C/D snoRNA in Arabidopsis plants.

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Section: Discussionsupporting

confidence: 57%

Mapping rRNA 2’-O-methylations and identification of C/D snoRNAs in Arabidopsis thaliana plants

et al. 2021

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“…The association between the decline in snoRNAs and fruit senescence suggests that these two events are likely connected, with the snoRNA decline likely acting as a signal for seed dispersal. This interpretation is in tune with the growing body of literature showing that snoRNAs regulate a multitude of biological processes such as post-transcriptional modification of RNA, including acetylation, regulation of splicing patterns, stability and control of mRNA abundance, and translation [13,30,31].…”

Section: Discussionsupporting

confidence: 52%

“…One major biogenetic process involved in the regulation of transcription and processing of pre-mRNA complexes in the nucleus involves the role of small nucleolar RNAs (snoRNAs). A role of snoRNAs in pre-rRNA processing in relation to ribosome biogenesis has become apparent from RNA deep sequencing and in situ localization studies in Arabidopsis [12,13]. The organization of tomato box C/D snoRNAs in concert with heat shock elements suggested the possibility of their functional role(s) in ribosomal RNA biosynthesis together with other proteins regulated by plant hormones and stress [11], apparent also by the role(s) of S-adenosylmethionine (SAM) in ribosome biogenesis and rRNA methylation shown in Escherichia coli [17].…”

Section: Discussionmentioning

confidence: 99%

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Engineered Ripening-Specific Accumulation of Polyamines Spermidine and Spermine in Tomato Fruit Upregulates Clustered C/D Box snoRNA Gene Transcripts in Concert with Ribosomal RNA Biogenesis in the Red Ripe Fruit

Shukla

Fatima

Goyal

et al. 2020

Plants

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Ripening of tomato fruit leads, in general, to a sequential decrease in the endogenous levels of polyamines spermidine (SPD) and spermine (SPM), while the trend for the diamine putrescine (PUT) levels is generally an initial decrease, followed by a substantial increase, and thereafter reaching high levels at the red ripe fruit stage. However, genetic engineering fruit-specific expression of heterologous yeast S-adenosylmethionine (SAM) decarboxylase in tomato has been found to result in a high accumulation of SPD and SPM at the cost of PUT. This system enabled a genetic approach to determine the impact of increased endogenous levels of biogenic amines SPD and SPM in tomato (579HO transgenic line) and on the biogenesis, transcription, processing, and stability of ribosomal RNA (rRNA) genes in tomato fruit as compared with the non-transgenic 556AZ line. One major biogenetic process regulating transcription and processing of pre-mRNA complexes in the nucleus involves small nucleolar RNAs (snoRNAs). To determine the effect of high levels of SPD and SPM on these latter processes, we cloned, sequenced, and identified a box C/D snoRNA cluster in tomato, namely, SlSnoR12, SlU24a, Slz44a, and Slz132b. Similar to this snoRNA cluster housed on chromosome (Chr.) 6, two other noncoding C/D box genes, SlsnoR12.2 and SlU24b, with a 94% identity to those on Chr. 6 were found located on Chr. 3. We also found that other snoRNAs divisible into snoRNA subclusters A and B, separated by a uridine rich spacer, were decorated with other C/D box snoRNAs, namely, J10.3, Z131a/b, J10.1, and Z44a, followed by z132a, J11.3, z132b, U24, Z20, U24a, and J11. Several of these, for example, SlZ44a, Slz132b, and SlU24a share conserved sequences similar to those in Arabidopsis and rice. RNAseq analysis of high SPD/SPM transgenic tomatoes (579HO line) showed significant enrichment of RNA polymerases, ribosomal, and translational protein genes at the breaker+8 ripening stage as compared with the 556AZ control. Thus, these results indicate that SPD/SPM regulates snoRNA and rRNA expression directly or indirectly, in turn, affecting protein synthesis, metabolism, and other cellular activities in a positive manner.

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“…The modifications in helix 18 vary between two 2 -O-ribose-me and one -site in human, one 2 -O-ribose-me site in yeast and just one -site in A. thaliana (Figure 8), while no methylation site exists in A. thaliana. Brown et al (2001Brown et al ( , 2003, Qu et al (2001), Yoshihama et al (2013), Sun et al (2019), Streit et al (2020). The coloring is according to Figure 3.…”

Section: A View On the Modifications In Plant 18s Rrnamentioning

confidence: 99%

The Arabidopsis 2′-O-Ribose-Methylation and Pseudouridylation Landscape of rRNA in Comparison to Human and Yeast

Streit

Schleiff

2021

Front. Plant Sci.

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Eukaryotic ribosome assembly starts in the nucleolus, where the ribosomal DNA (rDNA) is transcribed into the 35S pre-ribosomal RNA (pre-rRNA). More than two-hundred ribosome biogenesis factors (RBFs) and more than two-hundred small nucleolar RNAs (snoRNA) catalyze the processing, folding and modification of the rRNA in Arabidopsis thaliana. The initial pre-ribosomal 90S complex is formed already during transcription by association of ribosomal proteins (RPs) and RBFs. In addition, small nucleolar ribonucleoprotein particles (snoRNPs) composed of snoRNAs and RBFs catalyze the two major rRNA modification types, 2′-O-ribose-methylation and pseudouridylation. Besides these two modifications, rRNAs can also undergo base methylations and acetylation. However, the latter two modifications have not yet been systematically explored in plants. The snoRNAs of these snoRNPs serve as targeting factors to direct modifications to specific rRNA regions by antisense elements. Today, hundreds of different sites of modifications in the rRNA have been described for eukaryotic ribosomes in general. While our understanding of the general process of ribosome biogenesis has advanced rapidly, the diversities appearing during plant ribosome biogenesis is beginning to emerge. Today, more than two-hundred RBFs were identified by bioinformatics or biochemical approaches, including several plant specific factors. Similarly, more than two hundred snoRNA were predicted based on RNA sequencing experiments. Here, we discuss the predicted and verified rRNA modification sites and the corresponding identified snoRNAs on the example of the model plant Arabidopsis thaliana. Our summary uncovers the plant modification sites in comparison to the human and yeast modification sites.

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The Existence and Localization of Nuclear snoRNAs in Arabidopsis thaliana Revisited

Cited by 19 publications

References 90 publications

Mapping rRNA 2’-O-methylations and identification of C/D snoRNAs in Arabidopsis thaliana plants

Mapping rRNA 2’-O-methylations and identification of C/D snoRNAs in Arabidopsis thaliana plants

Engineered Ripening-Specific Accumulation of Polyamines Spermidine and Spermine in Tomato Fruit Upregulates Clustered C/D Box snoRNA Gene Transcripts in Concert with Ribosomal RNA Biogenesis in the Red Ripe Fruit

The Arabidopsis 2′-O-Ribose-Methylation and Pseudouridylation Landscape of rRNA in Comparison to Human and Yeast

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