Trans-Splicing and Operons in Metazoans: Translational Control in Maternally Regulated Development and Recovery from Growth Arrest
Trans-Splicing and Operons in Metazoans: Translational Control in Maternally Regulated Development and Recovery from Growth Arrest
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DOI：
10.1093/molbev/msu336
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发表时间：
2015-03-01
影响因子：
10.7
通讯作者：
Thompson, Eric M.
中科院分区：
文献类型：
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作者：
Danks, Gemma B.;Raasholm, Martina;Thompson, Eric M.
从操纵子转录的多顺反子mRNAs通过剪接前导(SL)RNA的反式剪接来解析。反式剪接也发生在单顺反子转录本上。在后生动物中，零星出现的反式剪接和操纵子使得它们进化的驱动力(S)变得不清楚。以前的工作已经提出，生殖系表达驱动秀丽线虫操纵子的组织，最近的一个假说提出，操纵子在从生长停滞状态恢复的过程中通过保守转录机制提供了进化优势。使用改进的CAP基因表达分析方法，我们在海洋脊索动物Oikopleura dioica中定位了SL反式剪接的全基因组位置。平铺微阵列揭示了反式剪接基因在发育和从生长停滞中恢复期间的表达动态。操纵子并不能促进野生稻从生长停滞中恢复过来。相反，我们发现反式剪接的转录本主要是母体的。然后，我们分析了来自线虫和海鞘的数据，发现这三个物种在母体mRNA中都有丰富的反式剪接和操纵子基因表达，这表明这可能是后生动物操纵子进化的驱动力。此外，我们发现大多数已知的末端寡嘧啶(TOP)mRNAs在Dioica中是反式剪接的，并且SL包含一个类似TOP的基序。这表明，Dioica中的SL通过TOR信号通路对反式剪接的mRNAs进行营养依赖的翻译控制。我们假设，SL-反式剪接在依赖翻译控制来调节早期胚胎发生、生长和卵母细胞生产以响应营养水平的物种中提供了进化优势。
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.