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Trans‐splicing

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Abstract Trans‐splicing is the joining together of portions of two separate pre‐mRNA molecules. The two distinct categories of spliceosomal trans‐splicing are genic trans‐splicing, which joins exons of different pre‐mRNA transcripts, and spliced leader (SL) trans‐splicing, which involves an exon donated from a specialized SL RNA. Both depend primarily on the same signals and components as cis‐splicing. Genic trans‐splicing events producing protein‐coding mRNAs have been described in a variety of organisms, including Caenorhabditis elegans and Drosophila. In mammalian cells, genic trans‐splicing can be associated with cancers and translocations. SL trans‐splicing has mainly been studied in nematodes and trypanosomes, but there are now numerous and diverse phyla (including primitive chordates) where this type of trans‐splicing has been detected. Such diversity raises questions as to the evolutionary origin of the process. Another intriguing question concerns the function of trans‐splicing, as operon resolution can only account for a small proportion of the total amount of SL trans‐splicing. WIREs RNA 2011 2 417–434 DOI: 10.1002/wrna.71 This article is categorized under: RNA Processing > Splicing Mechanisms RNA Processing > Splicing Regulation/Alternative Splicing

Different types of spliceosomal splicing join 5′ splice sites (ss) to 3′ ss. (a) cis‐splicing joins together exons from the same pre‐mRNA transcript. (b) Spliced leader (SL) trans‐splicing joins the specialized SL exon from the SL RNA to many different pre‐mRNAs. (c–e) Genic trans‐splicing joins together exons from two different pre‐mRNA molecules. The pre‐mRNA transcripts can originate from (c) different genes or from (d and e) the same gene, and may be encoded on opposite DNA strands or homologous chromosomes. (e) Genic trans‐splicing can result in exon duplication. Boxes represent exons; black lines represent introns and outrons. Green circle with T represents the TMG cap on the SL exon; 5′ and 3′ splice sites are marked; and red lines connecting exons indicate splicing. Exons of the same color originate from the same gene, whereas exons of different colors originate from different genes.

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C. elegans operons. (a) Diagram of a representative two‐gene operon from C. elegans. Upstream gene (orange) and downstream gene (red) are indicated. The mRNAs from first genes in operons may be spliced leader (SL)1 trans‐spliced or may be non‐trans‐spliced. The mRNAs from all downstream genes in operons are SL2 trans‐spliced. Boxes represent exons, thin black lines represent outron and introns, thick black line represents the intercistronic region (ICR) separating the two genes. Outrons are typically ∼300 nt and ICRs are typically ∼100 nt; (cs) 3′ end cleavage site of upstream gene; (tss) trans‐splice site. (b) The Ur element within the ICR is required for downstream gene SL2 trans‐splicing. The pre‐mRNA region between the cs of the upstream gene (orange) and the 3′ tss of the downstream gene of operon ceop1032 is shown depicting the position of the short stem‐loop and UAYYUU sequence that comprise the Ur element. (Y) U or C.

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Examples of spliced leader (SL) RNAs of different nematode species. SL RNA sequences and predicted secondary structures. C. elegans has two classes, SL1 RNA and SL2 RNA (variant SL2‐4 is depicted in the most stable structure predicted by Marz et al.117). Ascaris has a single SL RNA class. Trichinella spiralis has many SL RNA variants, only one of which is depicted here.58 Secondary structures shown are predictions only. Alternate structures are possible and may even be the preferred conformations for at least some of the ‘lifespan’ of the SL RNA. Red arrows show the 5′ trans‐splice sites. (TMG) known (black oval) or predicted (gray oval) 5′ TMG cap. Horizontal line indicates predicted Sm protein binding sites.

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Examples of spliced leader (SL) RNAs of different species. SL RNA sequences and predicted secondary structures of Adineta ricciae, Oikopleura dioica, and Karlodinium micrum. Red arrows show the 5′ trans‐splice sites. (TMG) known (black oval) or predicted (gray oval) 5′ TMG cap; (Y) U or C.

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Spliced leader (SL) trans‐splicing phylogeny. Unrooted tree comparing organism groups that do (green rectangles) and do not (red ovals) have SL trans‐splicing. As in Figure 3, tree is based on NCBI taxonomy classification, and is not necessarily representative of phylogenetic relationships. Branch lengths are arbitrary. Tree drawn using Interactive Tree of Life (iTOL) according to Ref 89.

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Spliced leader (SL) trans‐splicing organisms. Circular tree of selected species that have SL trans‐splicing. Tree is based on NCBI taxonomy classification of numerous SL trans‐splicing organisms. It is not necessarily representative of phylogenetic relationships and branch lengths are arbitrary. Drawn using Interactive Tree of Life (iTOL) according to Ref 89.

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Spliced leader (SL) trans‐splicing precursors and products. (Left panel) SL RNA and pre‐mRNA precursor molecules. Scale bars indicate relative lengths of RNA molecules. (Middle panel) Spliceosomal trans‐ and cis‐splicing. SL trans‐splicing (red lines) joins together the 5′ tss located on the SL RNA with the 3′ tss located on the pre‐mRNA. Cis‐splicing joins together exons of the same transcript. (Right panel) Resulting products of the splicing reactions. The mature mRNA bears the SL exon and the TMG cap at its 5′ end, and can be exported to the cytoplasm and translated. The Y‐branched product is the SL intron attached to the pre‐mRNA outron at the branchpoint. It is analogous to the lariat intron products that result from cis‐splicing. These discard products are rapidly debranched and degraded. Boxes represent exons and black lines represent introns and outrons as indicated. (tss) trans‐splice site; (bp) branchpoint. Green circle with T represents the TMG cap on the SL exon and is not to scale.

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RNA Processing > Splicing Regulation/Alternative Splicing

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