Trans-Splicing and Operons in Metazoans: Translational Control in Maternally Regulated Development and Recovery from Growth Arrest
| Autor: | Martina Raasholm, Abby Long, Coen Campsteijn, Gemma B. Danks, J. Robert Manak, Boris Lenhard, Eric M. Thompson |
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| Rok vydání: | 2015 |
| Předmět: |
Genetics
biology Operon TOR Serine-Threonine Kinases Trans-splicing Embryonic Development Gene Expression Regulation Developmental biology.organism_classification Cap analysis gene expression Ciona intestinalis Trans-Splicing Gene expression Animals Female Urochordata DNA microarray Caenorhabditis elegans Molecular Biology Gene Ecology Evolution Behavior and Systematics Signal Transduction |
| Zdroj: | Molecular Biology and Evolution. 32:585-599 |
| ISSN: | 1537-1719 0737-4038 |
| Popis: | Polycistronic mRNAs transcribed from operons are resolved via the trans-splicing of a spliced-leader (SL) RNA. Trans-splicing also occurs at monocistronic transcripts. The phlyogenetically sporadic appearance of trans-splicing and operons has made the driving force(s) for their evolution in metazoans unclear. Previous work has proposed that germline expression drives operon organization in Caenorhabditis elegans, and a recent hypothesis proposes that operons provide an evolutionary advantage via the conservation of transcriptional machinery during recovery from growth arrested states. Using a modified cap analysis of gene expression protocol we mapped sites of SL trans-splicing genome-wide in the marine chordate Oikopleura dioica. Tiled microarrays revealed the expression dynamics of trans-spliced genes across development and during recovery from growth arrest. Operons did not facilitate recovery from growth arrest in O. dioica. Instead, we found that trans-spliced transcripts were predominantly maternal. We then analyzed data from C. elegans and Ciona intestinalis and found that an enrichment of trans-splicing and operon gene expression in maternal mRNA is shared between all three species, suggesting that this may be a driving force for operon evolution in metazoans. Furthermore, we found that the majority of known terminal oligopyrimidine (TOP) mRNAs are trans-spliced in O. dioica and that the SL contains a TOP-like motif. This suggests that the SL in O. dioica confers nutrient-dependent translational control to trans-spliced mRNAs via the TOR-signaling pathway. We hypothesize that SL-trans-splicing provides an evolutionary advantage in species that depend on translational control for regulating early embryogenesis, growth and oocyte production in response to nutrient levels. |
| Databáze: | OpenAIRE |
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