Trans-spliced leader addition to mRNAs in a cnidarian

Stover, Nicholas A.; Steele, Robert E.

doi:10.1073/pnas.101049998

Cited by 108 publications

(102 citation statements)

References 48 publications

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“…The transsplicing of short RNA-leader, or spliced leader (SL), sequences onto the 59 ends of pre-mRNAs is found in a variety of eukaryotic taxa, including protists (Sutton and Boothroyd 1986;Tessier et al 1991;Zhang et al 2007), cnidarians (Stover and Steele 2001), platyhelminths (Davis 1997;Zayas et al 2005), nematodes (Krause and Hirsh 1987;Spieth et al 1993;Guiliano and Blaxter 2006), rotifers (Pouchkina-Stantcheva and Tunnacliffe 2005), and tunicates (Vandenberghe et al 2001;Ganot et al 2004;Satou et al 2006). These spliced leaders are donated by longer, precursor SL RNAs through a splicing reaction that is mechanistically similar to the cis-splicing used to remove introns from precursor mRNAs.…”

Section: Introductionmentioning

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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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: Introductionmentioning

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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“…Concerning the evolution of SL genes, available evidence has not allowed discrimination between hypotheses of a common origin with multiple losses and independent acquisition in multiple phylogenetic lineages (Lawrence 1999;Nilsen 2001;Stover and Steele 2001;Hastings 2005;Roy and Irimia 2009). Arguments put forward to favor the former hypothesis include the existence of (partially) shared functions, such as polycistronic transcript resolution, between some distantly related taxa, the stereotypic secondary structure of the SL RNA ''intron'' region, which features three stem-loops and a binding site for the Sm proteins (essential components of the eukaryotic cissplicing machinery), and the frequent localization of SL genes within 5S rRNA gene clusters.…”

Section: Introductionmentioning

confidence: 99%

“…This unusual form of RNA maturation was first described in trypanosomes, in which all mRNAs are trans-spliced, using a single SL RNA (Sutton and Boothroyd 1986). SL trans-splicing has subsequently been demonstrated to occur in Euglenozoas (Miller et al 1986;Tessier et al 1991), in dinoflagellates (Zhang et al 2007;, and in several metazoan lineages: all tested nematodes (Krause and Hirsh 1987;Guiliano and Blaxter 2006), urochordates (Vandenberghe et al 2001;Ganot et al 2004), flatworms (Davis 1997), the two tested chaetognath species (Marletaz et al 2008), a Bdelloid rotifer (Pouchkina-Stantcheva and Tunnacliffe 2005), an Acoel (Marletaz et al 2008), and the hydrozoan (Cnidaria) Hydra vulgaris (Stover and Steele 2001). In contrast, SL trans-splicing was not detected in vertebrates, echinoderms, arthropods, mollusks, or annelids, or in most nonmetazoan groups including fungi and plants.…”

Section: Introductionmentioning

confidence: 99%

Convergent origins and rapid evolution of spliced leader trans-splicing in Metazoa: Insights from the Ctenophora and Hydrozoa

Derelle¹,

Momose²,

Manuel³

et al. 2010

RNA

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Replacement of mRNA 59 UTR sequences by short sequences trans-spliced from specialized, noncoding, spliced leader (SL) RNAs is an enigmatic phenomenon, occurring in a set of distantly related animal groups including urochordates, nematodes, flatworms, and hydra, as well as in Euglenozoa and dinoflagellates. Whether SL trans-splicing has a common evolutionary origin and biological function among different organisms remains unclear. We have undertaken a systematic identification of SL exons in cDNA sequence data sets from non-bilaterian metazoan species and their closest unicellular relatives. SL exons were identified in ctenophores and in hydrozoan cnidarians, but not in other cnidarians, placozoans, or sponges, or in animal unicellular relatives. Mapping of SL absence/presence obtained from this and previous studies onto current phylogenetic trees favors an evolutionary scenario involving multiple origins for SLs during eumetazoan evolution rather than loss from a common ancestor. In both ctenophore and hydrozoan species, multiple SL sequences were identified, showing high sequence diversity. Detailed analysis of a large data set generated for the hydrozoan Clytia hemisphaerica revealed trans-splicing of given mRNAs by multiple alternative SLs. No evidence was found for a common identity of trans-spliced mRNAs between different hydrozoans. One feature found specifically to characterize SL-spliced mRNAs in hydrozoans, however, was a marked adenosine enrichment immediately 39 of the SL acceptor splice site. Our findings of high sequence divergence and apparently indiscriminate use of SLs in hydrozoans, along with recent findings in other taxa, indicate that SL genes have evolved rapidly in parallel in diverse animal groups, with constraint on SL exon sequence evolution being apparently rare.

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“…In the metazoans, trans-splicing has been described in free-living or parasitic nematodes (Krause & Hirsh 1987, Blaxter & Liu 1996, in trematodes (Rajkovic et al 1990, Davis et al 1994) and cestodes (Brehm et al 2000) as well as in turbelarians (Davis 1997) of the Platyhelminthes phylum. More recently, this form of RNA processing has been described in Hydra, a member of Cnidaria phylum (Stover & Steele 2001) and, surprisingly in two members of the Urochordata subphylum of chordates, the ascidian Ciona intestinalis (Vandenberghe et al 2001) and the appendiculariam Oikopleura dioica (Ganot et al 2004). It is absent in a variety of organisms where EST libraries were intensively sequenced, e.g.…”

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confidence: 99%

“…In C. elegans the predominant form of trans-splicing is SL1 trans-splicing (57%) (Zorio et al 1994) as well as for Ascaris suum (70%) (Maroney et al 1995). In Hydra (Stover & Steele 2001) and C. intestinalis (Vandenberghe et al 2001) there is no described operon structure to date. Taken altogether, these observations suggested that another role for SL trans-splicing exists in these organisms.…”

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confidence: 99%

Pre-mRNA trans-splicing: from kinetoplastids to mammals, an easy language for life diversity

Mayer

Flöeter-Winter²

2005

Mem. Inst. Oswaldo Cruz

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Since the discovery that genes are split into intron and exons, the studies of the mechanisms involved in splicing pointed to presence of consensus signals in an attempt to generalize the process for all living cells. However, as discussed in the present review, splicing is a theme full of variations. The trans-splicing of pre-mRNAs, the joining of exons from distinct transcripts, is one of these variations with broad distribution in the phylogenetic tree. The biological meaning of this phenomenon is discussed encompassing reactions resembling a possible noise to mechanisms of gene expression regulation. All of them however, can contribute to the generation of life diversity.Key words: RNA processing -alternative trans-splicing -spliced leader RNA -trypanosomatids -nematodes -mammalian Most of the protein-coding eukaryotic genes display an interrupted structure alternating exons and introns. After transcription, introns must be removed from the primary transcript (pre-mRNA) to generate a translatable mature mRNA. It is interesting to note that the mature mRNA is constituted of 5' and 3' untranslatable regions (UTR) flanking the open reading frame (ORF) and that UTR are also exons. The precise excision of the introns and the joining of neighboring exons is a complex process generally named splicing, and when this processing occurs within a single pre-mRNA molecule it can also be called cis-splicing (Moore et al. 1993, Burge et al. 1999.Cis-splicing occurs in a two-step mechanism, each step consisting of a transesterification reaction (Moore et al. 1993) (Fig. 1A). The spliceosome, a ribonucleoprotein machinery composed of five small ribonucleoproteins (U1, U2, U4, U5, U6 snRNPs, named in relation to the kind of associated RNA molecule) and approximately 300 distinct proteins, is responsible for the splicing catalysis (Burge et al. 1999).Much effort was expended on the comprehension of the structure and dynamics of this complex machine during the splicing process, but the rules that discriminate introns and exons within the message are still poorly understood. Nevertheless, four conserved pre-mRNA sequence elements, which interact with the spliceosome, have been characterized as determinants in the splicing process (Moore et al. 1993, Burge et al. 1999 (Fig. 1C). In mammals, the 5' splice site consensus is AG/GURAGU (R for purine, /for splice site, bold for the dinucleotide 5' intron boundary) while the 3' splice site consensus is YAG/G (Y for pyrimidine, /for splice site, bold for the dinucleotides 3' intron boundary). There is also a conservation of nucleotide sequence around the branch point, CURAY (Y for pyrimidine, R for purine and A for branch Recently, other cis-regulatory elements were implicated in splice site recognition, e.g. the exonic splicing enhancers (ESEs) (Fig. 1C). ESEs are localized within exons and interact with a family of proteins rich in serine and arginine (SR proteins) that recruits the spliceosome to the proximal splice site .Although the presence of those consensuses was observed, it i...

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Trans-spliced leader addition to mRNAs in a cnidarian

Cited by 108 publications

References 48 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

Convergent origins and rapid evolution of spliced leader trans-splicing in Metazoa: Insights from the Ctenophora and Hydrozoa

Pre-mRNA trans-splicing: from kinetoplastids to mammals, an easy language for life diversity

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