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Mol Biol Evol. 2015 Mar;32(3):585-99. doi: 10.1093/molbev/msu336. Epub 2014 Dec 17.

Trans-splicing and operons in metazoans: translational control in maternally regulated development and recovery from growth arrest.

Author information

1
Computational Biology Unit, Uni Computing, Uni Research, Bergen, Norway Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
2
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
3
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Oslo, Norway Department of Biochemistry, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, Oslo, Norway.
4
Department of Biology, University of Iowa.
5
Department of Biology, University of Iowa Carver Center for Genomics, Department of Biology, University of Iowa Department of Pediatrics, Carver College of Medicine, University of Iowa.
6
Computational Biology Unit, Uni Computing, Uni Research, Bergen, Norway Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway Department of Molecular Sciences Imperial College London and MRC Clinical Sciences Centre, London, United Kingdom.
7
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway Department of Biology, University of Bergen, Bergen, Norway eric.thompson@sars.uib.no.

Abstract

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.

KEYWORDS:

TOP mRNAs; TOR signaling; endocycle; maternal-zygotic transition; spliced-leader; tunicate

PMID:
25525214
DOI:
10.1093/molbev/msu336
[Indexed for MEDLINE]

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