Operons in C. elegans: Polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions

@article{Spieth1993OperonsIC,
  title={Operons in C. elegans: Polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions},
  author={John Spieth and Glenn Brooke and Scott Kuersten and Kristi Lea and Thomas Blumenthal},
  journal={Cell},
  year={1993},
  volume={73},
  pages={521-532}
}
The mRNAs of six C. elegans genes are known to be trans-spliced to SL2. We report here that a similarly oriented gene is located 100-300 bp upstream of each. We present evidence that the genes in these clusters are cotranscribed and downstream mRNAs are formed by cleavage at the polyadenylation site and trans-splicing. From one three-gene cluster we isolated cDNA clones representing both polycistronic RNAs and mRNAs polyadenylated at the free 3' end created by trans-splicing, suggesting that… 
C. elegans sequences that control trans-splicing and operon pre-mRNA processing.
TLDR
A novel computational analysis was used, based on nonnegative matrix factorization, to identify and characterize significant differences in the cis-acting sequence elements that differentiate various types of functional site, including internal versus terminal 3'-processing sites, and SL1 versus SL2 trans-splicing sites.
Polycistronic pre-mRNA processing in vitro: snRNP and pre-mRNA role reversal in trans-splicing.
TLDR
It is proposed that the UAYYUU motif in the pre-mRNA would serve an analogous function to the similar sequence in the U1 snRNA, which binds to the 5' splice site of introns, effectively reversing the roles of snRNP and pre- mRNA in trans-splicing.
Trans-splicing and operons.
  • T. Blumenthal
  • Biology, Medicine
    WormBook : the online review of C. elegans biology
  • 2005
TLDR
This work has revealed that one of the 3' end formation proteins, CstF, interacts with the only protein known to be specific to the SL2 snRNP, which presumably provides co-regulation of these proteins by producing a single RNA that encodes both.
A global analysis of C. elegans trans-splicing.
TLDR
Analysis of RNA-sequencing data from the modENCODE project shows that >17% of all C. elegans genes are in operons, similar to earlier estimates based on analysis of far fewer genes, and indicates that SL1 and SL2 trans-splicing use different underlying mechanisms.
Identification of transcription start sites of trans-spliced genes: uncovering unusual operon arrangements.
TLDR
Transcription of the entire region between the SL2 trans-spliced gene and the next upstream gene is shown, suggesting that these represent exceptional operons, and a second type of atypical "alternative" operon is reported, in which 3' end formation and trans-Splicing by SL2 occur within an intron.
Trans-splicing and operons in C. elegans.
  • T. Blumenthal
  • Biology, Medicine
    WormBook : the online review of C. elegans biology
  • 2012
TLDR
Evidence suggests that RNA polymerase is poised at the promoters of growth genes, and operons allow more efficient recovery from growth-arrested states, resulting in reduction in the need for this cache of inactiveRNA polymerase.
Operons as a common form of chromosomal organization in C. elegans
TLDR
Identifying gene clusters using the extensive data generated by the genome project and testing seven genes for trans-splicing specificity indicate that the pre-mRNAs of about 70% of C. elegans genes are trans-split and as many as a quarter are transcribed in operons.
SL1 trans Splicing and 3′-End Formation in a Novel Class of Caenorhabditis elegansOperon
TLDR
An exceptionally long polypyrimidine tract found in the 3′ untranslated regions of the three known SL1-type operons is shown to be required for the accumulation of both upstream and downstream mRNAs.
The SL1 trans-spliced leader RNA performs an essential embryonic function in Caenorhabditis elegans that can also be supplied by SL2 RNA.
TLDR
It is found that when overexpressed, SL2 RNA, which performs a distinct function from that of SL1 RNA in wild-type animals, can rescue the lethality of embryos lackingSL1 RNA, and this result suggests that the mechanism that discriminates between SL1 and SL2-trans-splicing may involve competition between SL2 and SL1-specific trans-spliced messages.
trans Splicing of PolycistronicCaenorhabditis elegans Pre-mRNAs: Analysis of the SL2 RNA
TLDR
An in vivo mutational analysis of the SL2 RNA is reported, finding that stem-loop III appears to confer a specific function to SL1 RNA, and an upstream sequence, previously predicted to be a proximal sequence element, is shown to be required forSL2 RNA expression.
...
1
2
3
4
5
...

References

SHOWING 1-10 OF 49 REFERENCES
Insertion of part of an intron into the 5' untranslated region of a Caenorhabditis elegans gene converts it into a trans-spliced gene.
TLDR
The results suggest that if a transcript begins with intronlike sequence followed by a 3' splice site, this alone may constitute an outron and be sufficient to demarcate a transcript as a trans-splice acceptor and leave open the possibility that specific sequences are required to increase the efficiency of trans- Splicing.
The C. elegans Trans-spliced leader RNA is bound to Sm and has a trimethylguanosine cap
TLDR
It is shown that C. elegans has the usual snRNAs, which presumably catalyze the splicing reactions, and the trans-spliced leader RNA is also Sm-associated and has this special cap, suggesting that a molecule discovered as a substate of splicing has properties of molecules heretofore known only to facilitate splicing of other RNAs.
mRNAs that mature through trans-splicing in Caenorhabditis elegans have a trimethylguanosine cap at their 5' termini.
TLDR
It is found that the trimethylguanosine cap present on the spliced leader RNA was transferred to the pre-mRNA during the trans-splicing reaction and was maintained on the mature mRNA.
A functional mRNA polyadenylation signal is required for transcription termination by RNA polymerase II.
TLDR
It is concluded that the sequences required for efficient cleavage/polyadenylation of the SV40 early pre-mRNA also constitute an important element of an RNA polymerase II termination signal.
U small nuclear ribonucleoprotein requirements for nematode cis- and trans-splicing in vitro.
TLDR
It is indicated that both cis- and trans-splicing require intact U2 and U4/U6 small nuclear ribonucleoproteins (snRNPs), however, whereas cis- Splicing displays the expected requirement for an intact U1 snRNP, trans-Splicing is unaffected when approximately 90% of U1snRNP is degraded.
Trans-spliced leader RNA exists as small nuclear ribonucleoprotein particles in Caenorhabditis elegans
TLDR
Using antisera against the Sm antigen that is associated with small nuclear ribonucleoprotein particles (snRNPs), SL RNA was precipitated from extracts of C. elegans, indicating that it is bound by theSm antigen in vivo.
In vitro polyadenylation is stimulated by the presence of an upstream intron.
TLDR
It is suggested that splicing and polyadenylation factors interact to recognize terminal, poly(A) site-containing exons, which may explain why all known intron-containing eukaryotic pre-mRNAs generate their 3' ends by polyadenyation.
Temporal order of RNA-processing reactions in trypanosomes: rapid trans splicing precedes polyadenylation of newly synthesized tubulin transcripts.
TLDR
It is shown that trans splicing precedes polyadenylation in the processing of trypanosome tubulin pre-mRNAs, suggesting that regulation of mRNA biogenesis may emphasize RNA-processing reactions more so than in other organisms.
Conversion of a trans‐spliced C. elegans gene into a conventional gene by introduction of a splice donor site.
TLDR
It is reported that trans‐splicing of the rol‐6 gene can be completely suppressed simply by introducing a donor site into its 173 nt outron, at a site 50 nt upstream of the trans‐ Splicing site, thereby converting rol•6 into a conventional gene with a spliced intron near its 5′ end.
A trans-spliced leader sequence on actin mRNA in C. elegans
TLDR
The evidence suggests that the actin mRNA leader sequence is acquired from this novel nucleotide transcript by an intermolecular trans-splicing mechanism.
...
1
2
3
4
5
...