The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences.
The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences.
复制标题
黑晶种系基因组为基因内寄生虫DNA提供了一个利基：内部消除序列的进化动力学。
DOI：
10.1371/journal.pgen.1002984
复制
发表时间：
2012
期刊：
影响因子：
4.5
通讯作者：
Sperling L
中科院分区：
文献类型：
--
作者：
Arnaiz O;Mathy N;Baudry C;Malinsky S;Aury JM;Denby Wilkes C;Garnier O;Labadie K;Lauderdale BE;Le Mouël A;Marmignon A;Nowacki M;Poulain J;Prajer M;Wincker P;Meyer E;Duharcourt S;Duret L;Bétermier M;Sperling L
在编码序列中插入寄生DNA通常是有害的，并且通常在进化过程中被反向选择。由于核的二型性，纤毛虫提供了独特的模型来研究这种插入的命运。性行为后，它们的种系基因组在从种系微核发育出新的体细胞大核的过程中经历了广泛的重排。在草履虫中，这些重排包括从体细胞DNA中精确切除独特拷贝的内部消除序列（IES），需要驯化的piggyBac转座酶PiggyMac的活性。我们对草履虫的生殖系DNA进行了测序，建立了一个全基因组范围的45，000个IES目录，以深入了解它们的进化起源和切除机制。我们获得的直接证据表明，PiggyMac是切除所有IEs所必需的。与已知的P. tetraurelia Tc 1/mariner转座子的同源性表明，至少有一部分IES来自这些元件。大多数IES插入发生在最近的全基因组复制之前，该复制发生在P.奥雷利亚物种复合体多样化之前，但IES对草履虫基因组的入侵似乎是一个持续的过程。一旦插入，IES通过缺失和点取代的积累而迅速衰减。超过90%的IES短于150 bp，并呈现出显著的大小分布，具有约10 bp的周期性，对应于双链DNA的螺旋重复序列，并表明在组装转座体样切除复合物期间形成DNA环。IES在编码序列内和编码序列之间同样频繁;然而，切除不是100%有效的，并且存在针对IES插入的选择性压力，特别是在高表达基因内。我们讨论的可能性，古代驯化的piggyBac转座酶有利于随后的整个生殖系的转座子的繁殖，允许插入在编码序列中，寄生DNA的基因组中的一部分通常是不能容忍的。纤毛虫是单细胞真核生物，当一个新的体细胞大核，负责基因表达，从生殖细胞微核的副本发展时，在每个有性世代重新排列它们的基因组。在草履虫中，功能性体细胞基因组的组装需要精确切除间质DNA片段，内部消除序列（IES），涉及驯化的piggyBac转座酶PiggyMac。为了研究IES的起源和进化，我们对生殖系DNA进行了测序，并鉴定了45，000个IES。我们发现，这些独特的拷贝元件中至少有一些是衰变的Tc 1/mariner转座子，IES插入可能是一个持续的过程。在插入之后，元件通过缺失和取代的积累而迅速衰减。短于150 bp的IEs的93%显示出显著的大小分布，具有10 bp的周期性，双链DNA的螺旋重复序列，这与进化仅保留在切除复合物组装期间可以形成双链DNA环的IEs的想法一致。我们提出，古老的驯化piggyBac转座酶，它提供了一个精确的切除机制，使转座子随后入侵草履虫编码序列，一小部分的基因组，通常不容忍寄生DNA。
Insertions of parasitic DNA within coding sequences are usually deleterious and are generally counter-selected during evolution. Thanks to nuclear dimorphism, ciliates provide unique models to study the fate of such insertions. Their germline genome undergoes extensive rearrangements during development of a new somatic macronucleus from the germline micronucleus following sexual events. In Paramecium, these rearrangements include precise excision of unique-copy Internal Eliminated Sequences (IES) from the somatic DNA, requiring the activity of a domesticated piggyBac transposase, PiggyMac. We have sequenced Paramecium tetraurelia germline DNA, establishing a genome-wide catalogue of ∼45,000 IESs, in order to gain insight into their evolutionary origin and excision mechanism. We obtained direct evidence that PiggyMac is required for excision of all IESs. Homology with known P. tetraurelia Tc1/mariner transposons, described here, indicates that at least a fraction of IESs derive from these elements. Most IES insertions occurred before a recent whole-genome duplication that preceded diversification of the P. aurelia species complex, but IES invasion of the Paramecium genome appears to be an ongoing process. Once inserted, IESs decay rapidly by accumulation of deletions and point substitutions. Over 90% of the IESs are shorter than 150 bp and present a remarkable size distribution with a ∼10 bp periodicity, corresponding to the helical repeat of double-stranded DNA and suggesting DNA loop formation during assembly of a transpososome-like excision complex. IESs are equally frequent within and between coding sequences; however, excision is not 100% efficient and there is selective pressure against IES insertions, in particular within highly expressed genes. We discuss the possibility that ancient domestication of a piggyBac transposase favored subsequent propagation of transposons throughout the germline by allowing insertions in coding sequences, a fraction of the genome in which parasitic DNA is not usually tolerated. Ciliates are unicellular eukaryotes that rearrange their genomes at every sexual generation when a new somatic macronucleus, responsible for gene expression, develops from a copy of the germline micronucleus. In Paramecium, assembly of a functional somatic genome requires precise excision of interstitial DNA segments, the Internal Eliminated Sequences (IES), involving a domesticated piggyBac transposase, PiggyMac. To study IES origin and evolution, we sequenced germline DNA and identified 45,000 IESs. We found that at least some of these unique-copy elements are decayed Tc1/mariner transposons and that IES insertion is likely an ongoing process. After insertion, elements decay rapidly by accumulation of deletions and substitutions. The 93% of IESs shorter than 150 bp display a remarkable size distribution with a periodicity of 10 bp, the helical repeat of double-stranded DNA, consistent with the idea that evolution has only retained IESs that can form a double-stranded DNA loop during assembly of an excision complex. We propose that the ancient domestication of a piggyBac transposase, which provided a precise excision mechanism, enabled transposons to subsequently invade Paramecium coding sequences, a fraction of the genome that does not usually tolerate parasitic DNA.
登录
查看更多内容
影响因子：
64.8
作者：
Aury, Jean-Marc;Jaillon, Olivier;Wincker, Patrick
通讯作者：
Wincker, Patrick
影响因子：
7
作者：
Duret, Laurent;Cohen, Jean;Sperling, Linda
通讯作者：
Sperling, Linda
影响因子：
5.3
作者：
EPSTEIN, LM;FORNEY, JD
通讯作者：
FORNEY, JD
2011 年草履虫数据库：用于纤毛虫草履虫模型功能和比较基因组学的新工具和新数据。
影响因子：
14.9
作者：
Arnaiz O;Sperling L
通讯作者：
Sperling L
影响因子：
64.8
作者：
Baulcombe, D
通讯作者：
Baulcombe, D