Species-specific chromatin landscape determines how transposable elements shape genome evolution.
Species-specific chromatin landscape determines how transposable elements shape genome evolution.
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DOI：
10.7554/elife.81567
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发表时间：
2022-08-23
期刊：
影响因子：
7.7
通讯作者：
Lee, Yuh Chwen G.
中科院分区：
文献类型：
--
作者：
Huang, Yuheng;Shukla, Harsh;Lee, Yuh Chwen G.
关键词：
转座元件(TES)是一种自私的遗传寄生虫，它们以牺牲宿主适应性为代价增加拷贝数。TES的“成功”或全基因组丰度在不同物种之间差别很大。破译TE丰度如此大的变化的原因一直是进化基因组学的一个中心问题。我们先前提出，物种特有的TE丰度可能是由宿主直接的TES表观遗传沉默--抑制性表观遗传标记从沉默的TES扩散到相邻序列--的无意后果所驱动的。在这里，我们在果蝇亚群中的六个物种中比较了这种TE介导的局部抑制标记的丰富，或称“TES的表观遗传效应”，以逐步剖析这种效应在确定基因组TE丰度中的作用。我们发现，TE介导的抑制标记的局部浓缩是普遍存在的，并且在不同物种甚至不同物种之间存在很大差异。虽然这种TE介导的效应改变了相邻基因的表观遗传状态，但我们惊讶地发现，相邻基因的转录可能会反过来影响这种传播。重要的是，我们的多物种分析提供了将物种特定的宿主染色质调节、TE介导的表观遗传效应、针对TES的自然选择的强度以及个体特有的基因组TE丰度联系起来的能力和适当的系统发育分辨率。我们的发现指出了宿主染色质景观通过自私遗传寄生虫的表观遗传效应在塑造基因组进化中的重要性。生命所需的所有指令都编码在细胞中存在的一组DNA中。因此，认为这些遗传信息的每一点都应该为生物体服务似乎是很自然的。然而，大多数物种携带寄生的可转座序列，或转座子，其唯一目的是繁殖并将自己插入到基因组的其他位置。细胞有可能抑制这些自私的因素。化学标记可以沉积在DNA上，暂时使转座子沉默，阻止它们移动和复制。然而，这有时是有代价的：抑制性的化学修饰可能会扩散到对有机体至关重要的附近基因，并扰乱它们的功能。奇怪的是，转座子的流行程度在生命之树上差异很大。这些序列构成了某些物种基因组的大部分--事实上，它们代表了大约一半的人类遗传信息。但在其他生物中，它们的丰度要低得多，例如，它们只占河豚基因组的6%。即使在果蝇物种中，转座因子的流行率也可能在2%到25%之间。如何解释这种差异？Huang等人的研究成果。开始通过转座子沉默的镜头来研究这个问题，系统地比较了这一过程如何影响六种果蝇的附近地区。这揭示了与转座子沉默相关的副作用强度的差异，导致对邻近基因的不同程度的干扰。更大的影响与其基因组中转座子较少的物种有关，这表明将这些物种中转座子的丰度保持在较低水平的进化压力正在发挥作用。进一步的分析表明，决定沉默标记如何分布的基因也可能是转座子沉默影响的差异的原因。因此，它们可能是导致物种间转座子丰度差异的原因。总体而言，这项工作揭示了塑造基因组进化的复杂机制，可能有助于更好地理解转座子是如何与衰老和癌症等过程联系在一起的。
Transposable elements (TEs) are selfish genetic parasites that increase their copy number at the expense of host fitness. The ‘success’, or genome-wide abundance, of TEs differs widely between species. Deciphering the causes for this large variety in TE abundance has remained a central question in evolutionary genomics. We previously proposed that species-specific TE abundance could be driven by the inadvertent consequences of host-direct epigenetic silencing of TEs—the spreading of repressive epigenetic marks from silenced TEs into adjacent sequences. Here, we compared this TE-mediated local enrichment of repressive marks, or ‘the epigenetic effect of TEs’, in six species in the Drosophila melanogaster subgroup to dissect step-by-step the role of such effect in determining genomic TE abundance. We found that TE-mediated local enrichment of repressive marks is prevalent and substantially varies across and even within species. While this TE-mediated effect alters the epigenetic states of adjacent genes, we surprisingly discovered that the transcription of neighboring genes could reciprocally impact this spreading. Importantly, our multi-species analysis provides the power and appropriate phylogenetic resolution to connect species-specific host chromatin regulation, TE-mediated epigenetic effects, the strength of natural selection against TEs, and genomic TE abundance unique to individual species. Our findings point toward the importance of host chromatin landscapes in shaping genome evolution through the epigenetic effects of a selfish genetic parasite. All the instructions required for life are encoded in the set of DNA present in a cell. It therefore seems natural to think that every bit of this genetic information should serve the organism. And yet most species carry parasitic ‘transposable’ sequences, or transposons, whose only purpose is to multiply and insert themselves at other positions in the genome. It is possible for cells to suppress these selfish elements. Chemical marks can be deposited onto the DNA to temporarily ‘silence’ transposons and prevent them from being able to move and replicate. However, this sometimes comes at a cost: the repressive chemical modifications can spread to nearby genes that are essential for the organism and perturb their function. Strangely, the prevalence of transposons varies widely across the tree of life. These sequences form the majority of the genome of certain species – in fact, they represent about half of the human genetic information. But their abundance is much lower in other organisms, forming a measly 6% of the genome of puffer fish for instance. Even amongst fruit fly species, the prevalence of transposable elements can range between 2% and 25%. What explains such differences? Huang et al. set out to examine this question through the lens of transposon silencing, systematically comparing how this process impacts nearby regions in six species of fruit flies. This revealed variations in the strength of the side effects associated with transposon silencing, resulting in different levels of perturbation on neighbouring genes. A stronger impact was associated with the species having fewer transposons in its genome, suggesting that an evolutionary pressure is at work to keep the abundance of transposons at a low level in these species. Further analyses showed that the genes which determine how silencing marks are distributed may also be responsible for the variations in the impact of transposon silencing. They could therefore be the ones driving differences in the abundance of transposons between species. Overall, this work sheds light on the complex mechanisms shaping the evolution of genomes, and it may help to better understand how transposons are linked to processes such as aging and cancer.