On the Possibility of an Early Evolutionary Origin for the Spliced Leader Trans-Splicing

Krchňáková, Zuzana; Krajčovič, Juraj; Vesteg, Matej

doi:10.1007/s00239-017-9803-y

Cited by 24 publications

(29 citation statements)

References 80 publications

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“…Interestingly, TMG cap can also be present on mRNAs. In lower eukaryotes, such as the nematode, chordate and cnidarian, many mRNAs acquire TMG through a trans-splicing reaction between the TMG capped Spliced Leader RNA and the pre-mRNA (reviewed in [ 9 , 10 ]). In mammals, mRNAs of some of the selenoproteins possess the hypermethylated cap, which might be important for efficient translation of these proteins [ 11 ].…”

Section: Introductionmentioning

confidence: 99%

Loss of the RNA trimethylguanosine cap is compatible with nuclear accumulation of spliceosomal snRNAs but not pre-mRNA splicing or snRNA processing during animal development

et al. 2020

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The 2,2,7-trimethylguanosine (TMG) cap is one of the first identified modifications on eukaryotic RNAs. TMG, synthesized by the conserved Tgs1 enzyme, is abundantly present on snRNAs essential for pre-mRNA splicing. Results from ex vivo experiments in vertebrate cells suggested that TMG ensures nuclear localization of snRNAs. Functional studies of TMG using tgs1 mutations in unicellular organisms yield results inconsistent with TMG being indispensable for either nuclear import or splicing. Utilizing a hypomorphic tgs1 mutation in Drosophila, we show that TMG reduction impairs germline development by disrupting the processing, particularly of introns with smaller sizes and weaker splice sites. Unexpectedly, loss of TMG does not disrupt snRNAs localization to the nucleus, disputing an essential role of TMG in snRNA transport. Tgs1 loss also leads to defective 3’ processing of snRNAs. Remarkably, stronger tgs1 mutations cause lethality without severely disrupting splicing, likely due to the preponderance of TMG-capped snRNPs. Tgs1, a predominantly nucleolar protein in Drosophila, likely carries out splicing-independent functions indispensable for animal development. Taken together, our results suggest that nuclear import is not a conserved function of TMG. As a distinctive structure on RNA, particularly non-coding RNA, we suggest that TMG prevents spurious interactions detrimental to the function of RNAs that it modifies.

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Section: Introductionmentioning

confidence: 99%

Loss of the RNA trimethylguanosine cap is compatible with nuclear accumulation of spliceosomal snRNAs but not pre-mRNA splicing or snRNA processing during animal development

et al. 2020

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“…Our work also unveils two additional functional and evolutionary links between group II introns, spliceosomal introns and the spliceosome. First, the trans -splicing of E1 at the 5’ end of various mRNA fragments is analogous to the second step of the spliced leader (SL) trans -splicing pathway, which has a patchy evolutionary distribution amongst eukaryotes and whose origin has remained enigmatic [ 28 , 29 ]. Second, we showed that group II introns, similarly to the spliceosome [ 22 ], can catalyze the trans -splicing of intergenic mRNA-mRNA chimeras in bacteria.…”

Section: Discussionmentioning

confidence: 99%

Bacterial group II introns generate genetic diversity by circularization and trans-splicing from a population of intron-invaded mRNAs

et al. 2018

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Group II introns are ancient retroelements that significantly shaped the origin and evolution of contemporary eukaryotic genomes. These self-splicing ribozymes share a common ancestor with the telomerase enzyme, the spliceosome machinery as well as the highly abundant spliceosomal introns and non-LTR retroelements. More than half of the human genome thus consists of various elements that evolved from ancient group II introns, which altogether significantly contribute to key functions and genetic diversity in eukaryotes. Similarly, group II intron-related elements in bacteria such as abortive phage infection (Abi) retroelements, diversity generating retroelements (DGRs) and some CRISPR-Cas systems have evolved to confer important functions to their hosts. In sharp contrast, since bacterial group II introns are scarce, irregularly distributed and frequently spread by lateral transfer, they have mainly been considered as selfish retromobile elements with no beneficial function to their host. Here we unveil a new group II intron function that generates genetic diversity at the RNA level in bacterial cells. We demonstrate that Ll.LtrB, the model group II intron from Lactococcus lactis, recognizes specific sequence motifs within cellular mRNAs by base pairing, and invades them by reverse splicing. Subsequent splicing of ectopically inserted Ll.LtrB, through circularization, induces a novel trans-splicing pathway that generates exon 1-mRNA and mRNA-mRNA intergenic chimeras. Our data also show that recognition of upstream alternative circularization sites on intron-interrupted mRNAs release Ll.LtrB circles harboring mRNA fragments of various lengths at their splice junction. Intergenic trans-splicing and alternative circularization both produce novel group II intron splicing products with potential new functions. Overall, this work describes new splicing pathways in bacteria that generate, similarly to the spliceosome in eukaryotes, genetic diversity at the RNA level while providing additional functional and evolutionary links between group II introns, spliceosomal introns and the spliceosome.

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“…Either it originated many times in evolution (i.e. in dinoflagellates, euglenozoans and in various animal lineages) (Lukeš, Leander & Keeling, ; Derelle et al, ; Douris, Telford & Averof, ) or the molecular machinery for SL‐ trans ‐splicing was present in the last common eukaryotic ancestor and it was lost independently many times in various eukaryotic lineages (Hastings, ; Vesteg & Krajčovič, ; Vesteg, Šándorová & Krajčovič, ; Krchňáková, Krajčovič & Vesteg, ). Since SL‐ trans ‐splicing is found in all euglenozoan species studied to date, this molecular character was almost certainly present in the euglenozoan ancestor (Table , Fig.…”

Section: Euglenozoan Nuclear Gene Expressionmentioning

confidence: 99%

Comparative molecular cell biology of phototrophic euglenids and parasitic trypanosomatids sheds light on the ancestor of Euglenozoa

et al. 2019

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Parasitic trypanosomatids and phototrophic euglenids are among the most extensively studied euglenozoans. The phototrophic euglenid lineage arose relatively recently through secondary endosymbiosis between a phagotrophic euglenid and a prasinophyte green alga that evolved into the euglenid secondary chloroplast. The parasitic trypanosomatids (i.e. Trypanosoma spp. and Leishmania spp.) and the freshwater phototrophic euglenids (i.e. Euglena gracilis) are the most evolutionary distant lineages in the Euglenozoa phylogenetic tree. The molecular and cell biological traits they share can thus be considered as ancestral traits originating in the common euglenozoan ancestor. These euglenozoan ancestral traits include common mitochondrial presequence motifs, respiratory chain complexes containing various unique subunits, a unique ATP synthase structure, the absence of mitochondria‐encoded transfer RNAs (tRNAs), a nucleus with a centrally positioned nucleolus, closed mitosis without dissolution of the nuclear membrane and nucleoli, a nuclear genome containing the unusual ‘J’ base (β‐D‐glucosyl‐hydroxymethyluracil), processing of nucleus‐encoded precursor messenger RNAs (pre‐mRNAs) via spliced‐leader RNA (SL‐RNA) trans‐splicing, post‐transcriptional gene silencing by the RNA interference (RNAi) pathway and the absence of transcriptional regulation of nuclear gene expression. Mitochondrial uridine insertion/deletion RNA editing directed by guide RNAs (gRNAs) evolved in the ancestor of the kinetoplastid lineage. The evolutionary origin of other molecular features known to be present only in either kinetoplastids (i.e. polycistronic transcripts, compaction of nuclear genomes) or euglenids (i.e. monocistronic transcripts, huge genomes, many nuclear cis‐spliced introns, polyproteins) is unclear.

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On the Possibility of an Early Evolutionary Origin for the Spliced Leader Trans-Splicing

Cited by 24 publications

References 80 publications

Loss of the RNA trimethylguanosine cap is compatible with nuclear accumulation of spliceosomal snRNAs but not pre-mRNA splicing or snRNA processing during animal development

Loss of the RNA trimethylguanosine cap is compatible with nuclear accumulation of spliceosomal snRNAs but not pre-mRNA splicing or snRNA processing during animal development

Bacterial group II introns generate genetic diversity by circularization and trans-splicing from a population of intron-invaded mRNAs

Comparative molecular cell biology of phototrophic euglenids and parasitic trypanosomatids sheds light on the ancestor of Euglenozoa

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