Evidence for Multiple Independent Origins of trans-Splicing in Metazoa

Evidence for Multiple Independent Origins of trans-Splicing in Metazoa
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DOI:
10.1093/molbev/msp286
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发表时间:
2010-03-01
影响因子:
10.7
通讯作者:
Averof, Michalis
Averof, Michalis
中科院分区:
生物学1区
文献类型:
--
作者:
Douris, Vassilis;Telford, Maximilian J.;Averof, Michalis

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与连接来自单个初级转录物的外显子的传统剪接不同,反式剪接连接来自基因组不同区域的单独转录物的RNA片段。剪接前导序列 (SL) 反式剪接在锥虫、线虫和扁虫中尤其广为人知,它为信使 RNA 提供前导序列和帽,使它们能够有效翻译。关于 SL 反式剪接的最大谜团之一是它的进化起源。到目前为止,SL 反式剪接已在一小部分不同的生物体(包括锥虫、甲藻、刺胞动物、轮虫、线虫、扁虫和尾索动物)中发现,但在大多数其他真核谱系中尚未发现,包括经过充分研究的群体,如真菌、植物、节肢动物和脊椎动物。这种不均匀的分布可能表明反式剪接存在于早期真核生物/后生动物中,随后在多个谱系中丢失,或者表明它独立进化了几次。从节肢动物中偶然发现SL反式剪接开始,我们对动物界的这一过程进行了全面的调查。通过调查来自 70 多个后生动物物种的表达序列标签数据,我们发现 SL 反式剪接也发生在至少两组节肢动物(端足类和桡足类甲壳类)、栉水母和六线纲海绵中。然而,我们在其他节肢动物和海绵类群或我们调查的其他 15 个门中没有发现 SL 反式剪接的证据。尽管SL反式剪接在水螅动物、刺胞动物、海绵动物和栉水母动物中的存在可能表明它存在于后生动物的基部,但在更高分辨率下明显的斑片状分布表明SL反式剪接在后生动物谱系中反复进化。与这种情况一致,我们讨论了 SL 前体 RNA 可以很容易地从普遍存在的用于常规剪接的小核 RNA 进化而来的证据。
In contrast to conventional splicing, which joins exons from a single primary transcript, trans-splicing links stretches of RNA from separate transcripts, derived from distinct regions of the genome. Spliced leader (SL) trans-splicing is particularly well known in trypanosomes, nematodes, and flatworms, where it provides messenger RNAs with a leader sequence and cap that allow them to be translated efficiently. One of the largest puzzles regarding SL trans-splicing is its evolutionary origin. Until now SL trans-splicing has been found in a small and disparate set of organisms (including trypanosomes, dinoflagellates, cnidarians, rotifers, nematodes, flatworms, and urochordates) but not in most other eukaryotic lineages, including well-studied groups such as fungi, plants, arthropods, and vertebrates. This patchy distribution could either suggest that trans-splicing was present in early eukaryotes/metazoans and subsequently lost in multiple lineages or that it evolved several times independently. Starting from the serendipitous discovery of SL trans-splicing in an arthropod, we undertook a comprehensive survey of this process in the animal kingdom. By surveying expressed sequence tag data from more than 70 metazoan species, we show that SL trans-splicing also occurs in at least two groups of arthropods (amphipod and copepod crustaceans), in ctenophores, and in hexactinellid sponges. However, we find no evidence for SL trans-splicing in other groups of arthropods and sponges or in 15 other phyla that we have surveyed. Although the presence of SL trans-splicing in hydrozoan cnidarians, hexactinellid sponges, and ctenophores might suggest that it was present at the base of the Metazoa, the patchy distribution that is evident at higher resolution suggests that SL trans-splicing has evolved repeatedly among metazoan lineages. In agreement with this scenario, we discuss evidence that SL precursor RNAs can readily evolve from ubiquitous small nuclear RNAs that are used for conventional splicing.