<i>Trans</i>-splicing in metazoans: A link to translational control?

Danks, Gemma B.; Thompson, Eric M.

doi:10.1080/21624054.2015.1046030

Cited by 4 publications

(3 citation statements)

References 19 publications

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“…S7). Such a mechanism is consistent with the observation that O. dioica can rapidly adjust its gamete output in response to shifting nutrient conditions (e.g., algal blooms) [28, 56, 57]. …”

Section: Resultssupporting

confidence: 87%

“…The O. dioica ovary and testis comprise terminally differentiated, highly specialized cell types, and the lower abundance of typical enhancer marks is in accordance with recent models of gene regulation during differentiation [84]. Moreover, genes organized in operons, particularly those devoted to maternal transcripts in the ovary, might have high transcriptional rates by default and be more subject to translational regulation via mTOR signaling [57]. The longer introns of O. dioica developmental genes exhibit more conserved intron positioning and also contain HCNEs [25].…”

Section: Discussionsupporting

confidence: 59%

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Sex-specific chromatin landscapes in an ultra-compact chordate genome

Navrátilová

Danks

Long

et al. 2017

Epigenetics & Chromatin

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BackgroundIn multicellular organisms, epigenome dynamics are associated with transitions in the cell cycle, development, germline specification, gametogenesis and inheritance. Evolutionarily, regulatory space has increased in complex metazoans to accommodate these functions. In tunicates, the sister lineage to vertebrates, we examine epigenome adaptations to strong secondary genome compaction, sex chromosome evolution and cell cycle modes.ResultsAcross the 70 MB Oikopleura dioica genome, we profiled 19 histone modifications, and RNA polymerase II, CTCF and p300 occupancies, to define chromatin states within two homogeneous tissues with distinct cell cycle modes: ovarian endocycling nurse nuclei and mitotically proliferating germ nuclei in testes. Nurse nuclei had active chromatin states similar to other metazoan epigenomes, with large domains of operon-associated transcription, a general lack of heterochromatin, and a possible role of Polycomb PRC2 in dosage compensation. Testis chromatin states reflected transcriptional activity linked to spermatogenesis and epigenetic marks that have been associated with establishment of transgenerational inheritance in other organisms. We also uncovered an unusual chromatin state specific to the Y-chromosome, which combined active and heterochromatic histone modifications on specific transposable elements classes, perhaps involved in regulating their activity.ConclusionsCompacted regulatory space in this tunicate genome is accompanied by reduced heterochromatin and chromatin state domain widths. Enhancers, promoters and protein-coding genes have conserved epigenomic features, with adaptations to the organization of a proportion of genes in operon units. We further identified features specific to sex chromosomes, cell cycle modes, germline identity and dosage compensation, and unusual combinations of histone PTMs with opposing consensus functions.Electronic supplementary materialThe online version of this article (doi:10.1186/s13072-016-0110-4) contains supplementary material, which is available to authorized users.

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Section: Resultssupporting

confidence: 87%

Section: Discussionsupporting

confidence: 59%

Sex-specific chromatin landscapes in an ultra-compact chordate genome

Navrátilová

Danks

Long

et al. 2017

Epigenetics & Chromatin

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“…We previously proposed that the SL supplies a 5′ TOP-like nutrient-dependent translational control motif to trans -spliced mRNA [5, 6]. TOP mRNAs, which primarily encode the protein synthesis machinery, contain a conserved 5′ TOP (Terminal OligoPyrimidine) motif that is critical [7] for translational repression during unfavourable growth conditions.…”

Section: Introductionmentioning

confidence: 99%

Trans-splicing of mRNAs links gene transcription to translational control regulated by mTOR

et al. 2019

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BackgroundIn phylogenetically diverse organisms, the 5′ ends of a subset of mRNAs are trans-spliced with a spliced leader (SL) RNA. The functions of SL trans-splicing, however, remain largely enigmatic.ResultsWe quantified translation genome-wide in the marine chordate, Oikopleura dioica, under inhibition of mTOR, a central growth regulator. Translation of trans-spliced TOP mRNAs was suppressed, consistent with a role of the SL sequence in nutrient-dependent translational control of growth-related mRNAs. Under crowded, nutrient-limiting conditions, O. dioica continued to filter-feed, but arrested growth until favorable conditions returned. Upon release from unfavorable conditions, initial recovery was independent of nutrient-responsive, trans-spliced genes, suggesting animal density sensing as a first trigger for resumption of development.ConclusionOur results are consistent with a proposed role of trans-splicing in the coordinated translational down-regulation of nutrient-responsive genes under growth-limiting conditions.

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Trans-splicing of mRNAs links gene transcription to translational control regulated by mTOR

Danks

Galbiati

Raasholm

et al. 2018

Preprint

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In phylogenetically diverse organisms, the 5' ends of a subset of mRNAs are trans-spliced with a spliced leader (SL) RNA.The functions of SL trans-splicing, however, remain largely enigmatic. Here, we quantified translation genome-wide in the marine chordate, Oikopleura dioica, under inhibition of mTOR, a central growth regulator. Translation of trans-spliced TOP mRNAs was suppressed, showing that the SL sequence permits nutrient-dependent translational control of growth-related mRNAs. Under crowded, nutrient-limiting conditions, O. dioica continues to filter-feed, but arrests growth until favorable conditions return. Upon release from such conditions, initial recovery was independent of nutrient-responsive, trans-spliced genes, suggesting animal density sensing as a first trigger for resumption of development. Our results demonstrate a role for trans-splicing in the coordinated translational down-regulation of nutrient-responsive genes under limiting conditions and suggest an innovative strategy for rapid evolution of mTOR targets in genomes of metazoans whose reproduction is tightly linked to nutritional cues.

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Trans-splicing in metazoans: A link to translational control?

Cited by 4 publications

References 19 publications

Sex-specific chromatin landscapes in an ultra-compact chordate genome

Sex-specific chromatin landscapes in an ultra-compact chordate genome

Trans-splicing of mRNAs links gene transcription to translational control regulated by mTOR

Trans-splicing of mRNAs links gene transcription to translational control regulated by mTOR

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