A novel family of <i>C. elegans</i> snRNPs contains proteins associated with <i>trans</i>-splicing

MacMorris, Margaret; Kumar, Madhur; Lasda, Erika; Larsen, Alison; Kraemer, Brian C.; Blumenthal, Thomas

doi:10.1261/rna.426707

Cited by 46 publications

(68 citation statements)

References 28 publications

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“…Although not closely related, these nematodes both add the canonical SL1 spliced leader to the majority of their mRNAs (Maroney et al 1995). Biochemical and molecular genetic investigations have built up a detailed picture of the mechanism and biological significance of spliced leader addition to mRNA in nematodes (Bruzik et al 1988;Thomas et al 1988;Maroney et al 1990a,b;Van Doren and Hirsh 1990;Denker et al 1996Denker et al , 2002Ferguson et al 1996;Ferguson and Rothman 1999;Lall et al 2004;Cheng et al 2007;MacMorris et al 2007). The conservation of the SL1 primary sequence between C. elegans and A. suum suggests a functional constraint.…”

Section: Discussionmentioning

confidence: 99%

“…However, it may also be that SL1 and SL1-like RNAs are constrained by the RNA-protein interactions involved in the formation of the snRNP complexes that form during trans-splicing. In both Ascaris and C. elegans, SL1 snRNPs contain a conserved pair of proteins (Denker et al 2002;MacMorris et al 2007). Database searches show that these proteins are also present in Brugia malayi.…”

Section: Discussionmentioning

confidence: 99%

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Spliced leader trans-splicing in the nematode Trichinella spiralis uses highly polymorphic, noncanonical spliced leaders

Pettitt¹,

Müller²,

Stansfield³

et al. 2008

RNA

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The trans-splicing of short spliced leader (SL) RNAs onto the 59 ends of mRNAs occurs in a diverse range of taxa. In nematodes, all species so far characterized utilize a characteristic, conserved spliced leader, SL1, as well as variants that are employed in the resolution of operons. Here we report the identification of spliced leader trans-splicing in the basal nematode Trichinella spiralis, and show that this nematode does not possess a canonical SL1, but rather has at least 15 distinct spliced leaders, encoded by at least 19 SL RNA genes. The individual spliced leaders vary in both size and primary sequence, showing a much higher degree of diversity compared to other known trans-spliced leaders. In a survey of T. spiralis mRNAs, individual mRNAs were found to be trans-spliced to a number of different spliced leader sequences. These data provide the first indication that the last common ancestor of the phylum Nematoda utilized spliced leader trans-splicing and that the canonical spliced leader, SL1, found in Caenorhabditis elegans, evolved after the divergence of the major nematode clades. This discovery sheds important light on the nature and evolution of mRNA processing in the Nematoda.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Spliced leader trans-splicing in the nematode Trichinella spiralis uses highly polymorphic, noncanonical spliced leaders

Pettitt¹,

Müller²,

Stansfield³

et al. 2008

RNA

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“…C. elegans uses two types of SL snRNP: SL1 and SL2, the latter of which has several sequence variants, termed SL3-SL12 (Blumenthal 2005;MacMorris et al 2007). SL1 is thought to trans-splice both to non-operon genes and to first genes in operons, thereby removing the outron (Conrad et al 1991).…”

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confidence: 99%

A global analysis of C. elegans trans-splicing

Allen¹,

Hillier²,

Waterston³

et al. 2010

Genome Res.

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158

256

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Trans-splicing of one of two short leader RNAs, SL1 or SL2, occurs at the 59 ends of pre-mRNAs of many C. elegans genes. We have exploited RNA-sequencing data from the modENCODE project to analyze the transcriptome of C. elegans for patterns of trans-splicing. Transcripts of~70% of genes are trans-spliced, similar to earlier estimates based on analysis of far fewer genes. The mRNAs of most trans-spliced genes are spliced to either SL1 or SL2, but most genes are not transspliced to both, indicating that SL1 and SL2 trans-splicing use different underlying mechanisms. SL2 trans-splicing occurs in order to separate the products of genes in operons genome wide. Shorter intercistronic distance is associated with greater use of SL2. Finally, increased use of SL1 trans-splicing to downstream operon genes can indicate the presence of an extra promoter in the intercistronic region, creating what has been termed a ''hybrid'' operon. Within hybrid operons the presence of the two promoters results in the use of the two SL classes: Transcription that originates at the promoter upstream of another gene creates a polycistronic pre-mRNA that receives SL2, whereas transcription that originates at the internal promoter creates transcripts that receive SL1. Overall, our data demonstrate that >17% of all C. elegans genes are in operons.[Supplemental material is available for this article. The sequence data from this study have been submitted to the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov/Traces/sra/sra.cgi) under accession nos. SRA008646 and SRA003622.] C. elegans uses two RNA processing features that distinguish it from other model organisms. First, the transcripts of many genes are trans-spliced to a spliced leader (SL). Trans-splicing is a process in which an SL replaces the 59 end of a transcript by spliceosomal splicing. The 22-nucleotide (nt) SL is donated by an ;100-nt SL snRNP (small nuclear ribonucleoprotein) to a pre-mRNA with an intron-like region, the outron, containing an unpaired 39 splice site located near the 59 end. The second distinguishing feature is that many genes are transcribed in polycistronic units, known as operons, where a single promoter serves several genes. The operons can be up to eight genes long, and the polycistronic pre-mRNAs are separated into individual cistrons by 39 end formation accompanied by SL trans-splicing.These two features have important implications for C. elegans research. For instance, deletions/insertions within an operon may affect not only the expression of the gene containing the mutation, but also the genes downstream from it in the operon (Cui et al. 2008). Similarly, in a strain with enhanced RNAi sensitivity, RNAi of an operon gene can also affect expression of genes downstream (Guang et al. 2010). Finally, the trans-splice site is at the 59 end of the mRNA, not the pre-mRNA, and thus, the promoter is often not directly adjacent to the gene, but rather upstream of the outron or the entire operon (Blumenthal and Spieth 1996). SL trans-splicing has been repor...

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“…S9C; Maroney et al 1996). The remaining transcripts vary in length from 135 to 177 nt and are thus considerably longer than classified Sm Y RNAs (MacMorris et al 2007). None of the six is-ncRNAs showed much sequence similarity to the Sm Y RNAs outside the Sm binding site (Supplemental Fig.…”

Section: Functional Classification Of the Novel Is-ncrnasmentioning

confidence: 99%

A differential sequencing-based analysis of the C. elegans noncoding transcriptome

Xiao

Wang

Luo³

et al. 2012

RNA

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Noncoding RNAs are increasingly being recognized as important players in eukaryote biology. However, despite major efforts in mapping the Caenorhabditis elegans transcriptome over the last couple of years, nonpolyadenylated and intermediate-size noncoding RNAs (is-ncRNAs) are still incompletely explored. We have combined an enzymatic approach with full-length RNASeq of is-ncRNAs in C. elegans. A total of 473 novel is-ncRNAs has been identified, of which a substantial fraction was associated with transcription factor binding sites and developmentally regulated expression patterns. Analysis of sequence and secondary structure permitted classification of more than 200 is-ncRNAs into several known RNA classes, while another 33 isncRNAs were identified as belonging to two previously uncharacterized groups of is-ncRNAs. Three of the unclassified isncRNAs contain the 59 Alu domain common to SRP RNAs and specifically bound with the SRP9/14 heterodimer in vitro. One of these (inc394) showed 65% sequence identity with the human, neuron-specific BC200 RNA. Structure-based clustering analysis and in vitro binding experiments supported the notion that the nematode stem-bulge RNAs (sbRNAs) are homologs (or functional analogs) of the Y RNAs. Moreover, analysis of the differential libraries showed that some mature snoRNAs undergo secondary 59 cap modification after processing of the primary transcript, thus suggesting the existence of a wider range of functional RNAs arising from processed and modified fragments of primary transcripts.

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A novel family of C. elegans snRNPs contains proteins associated with trans-splicing

Cited by 46 publications

References 28 publications

Spliced leader trans-splicing in the nematode Trichinella spiralis uses highly polymorphic, noncanonical spliced leaders

Spliced leader trans-splicing in the nematode Trichinella spiralis uses highly polymorphic, noncanonical spliced leaders

A global analysis of C. elegans trans-splicing

A differential sequencing-based analysis of the C. elegans noncoding transcriptome

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