Genome organization and gene expression shape the transposable element distribution in the Drosophila melanogaster euchromatin.

Genome organization and gene expression shape the transposable element distribution in the Drosophila melanogaster euchromatin.
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DOI:
10.1371/journal.pgen.0030210
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发表时间:
2007-11
期刊:
影响因子:
4.5
通讯作者:
Reuter M
Reuter M
中科院分区:
生物学2区
文献类型:
--
作者:
Fontanillas P;Hartl DL;Reuter M

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转座元件(TES)在基因组中的分布反映了插入速率和针对新插入的选择之间的平衡。因此,了解TES的分布有助于深入了解塑造基因组组织的力量。过去的研究表明,TES往往聚集在基因密度低、重组率低的基因组区域。然而,人们对调节整个基因组的插入率的因素及其进化意义知之甚少。一个候选因素是基因表达,它被认为可以通过使DNA更容易获得来提高局部插入率。我们通过比较果蝇常染色质中生殖系和胞体表达基因周围的TE密度来检验这一假设。因为只有在生殖系中出现的插入才会传递给下一代,所以我们预测生殖系表达的基因周围的TE密度比SOMA表达的基因高。我们发现,在胚系表达的基因附近,TE插入的速率比在SOMA表达的基因要高。然而,在生殖系表达的基因上,对基因组紧凑性(相对于多余的非编码DNA)的更强选择部分抵消了这种影响。我们还证明了共表达基因簇中的局部基因组组织在TES的基因组分布中起着基础性的作用。我们的分析表明,除了重组率之外,TES的分布还受到基因表达和基因组组织相互作用的影响。紧凑性选择的重要作用为TES在基因组进化中的作用提供了新的线索。TES不是让基因组被动生长,而是由塑造基因组紧凑性的力量控制,很可能与基因表达的效率或其复杂性有关,也可能与TE沉默机制的相互作用有关。转座元件(TES)是寄生的DNA片段,可以在宿主基因组中移动。这些自私的移动元件几乎存在于所有真核生物物种中,并可以对它们的DNA做出重大贡献。TES通过在基因组内复制自己来繁殖。根据它们在哪里着陆,新的拷贝可以改变有机体的表型,通常是负面的,但有时是积极的。虽然TES有一些偏好,但他们几乎没有机会选择自己的着陆点。有人提出,新的拷贝出现在它们的插入容易接近的地方。可获得性的提高可能发生在活跃转录的基因附近,因为DNA是解开的,暴露在外面。我们已经测试了这种效应是否对果蝇D黑腹果蝇基因组中TES的分布产生了可检测的影响。我们的分析表明,情况确实如此。因此,在产生精子和卵子(生殖系)的细胞中表达的基因周围,TE插入的密度更高。这是意料之中的,因为只有在这些细胞中产生的新拷贝才会传递给后代。此外,我们发现基因组区域对插入的耐受性不同。因此,在非编码DNA的大量增加有害的地方,TES是罕见的。
The distribution of transposable elements (TEs) in a genome reflects a balance between insertion rate and selection against new insertions. Understanding the distribution of TEs therefore provides insights into the forces shaping the organization of genomes. Past research has shown that TEs tend to accumulate in genomic regions with low gene density and low recombination rate. However, little is known about the factors modulating insertion rates across the genome and their evolutionary significance. One candidate factor is gene expression, which has been suggested to increase local insertion rate by rendering DNA more accessible. We test this hypothesis by comparing the TE density around germline- and soma-expressed genes in the euchromatin of Drosophila melanogaster. Because only insertions that occur in the germline are transmitted to the next generation, we predicted a higher density of TEs around germline-expressed genes than soma-expressed genes. We show that the rate of TE insertions is greater near germline- than soma-expressed genes. However, this effect is partly offset by stronger selection for genome compactness (against excess noncoding DNA) on germline-expressed genes. We also demonstrate that the local genome organization in clusters of coexpressed genes plays a fundamental role in the genomic distribution of TEs. Our analysis shows that—in addition to recombination rate—the distribution of TEs is shaped by the interaction of gene expression and genome organization. The important role of selection for compactness sheds a new light on the role of TEs in genome evolution. Instead of making genomes grow passively, TEs are controlled by the forces shaping genome compactness, most likely linked to the efficiency of gene expression or its complexity and possibly their interaction with mechanisms of TE silencing. Transposable elements (TEs) are parasitic DNA segments that can move within a host genome. These selfish mobile elements are present in virtually all eukaryote species and can contribute significantly to their DNA. TEs multiply by copying themselves within the genome. Depending on where they land, new copies can alter the organism's phenotype, often negatively but sometimes positively. Although TEs have some preferences, they have few opportunities to choose their landing places. It has been proposed that new copies arise in places that are easily accessible to their insertion. Increased accessibility can occur close to genes that are actively transcribed, because the DNA is uncoiled and laid bare. We have tested whether this effect has a detectable influence on the distribution of TEs in the genome of the fruitfly, D. melanogaster. Our analysis shows that this is indeed the case. Thus, TE insertions are denser around genes expressed in the cells that give rise to sperm and eggs (the germline). This is expected because only those new copies arising in these cells are transmitted to future generations. In addition, we found that genomic regions vary in their tolerance to insertions. Thus, TEs are rare wherever a considerable increase in noncoding DNA is deleterious.
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