Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, United States.
Elife. 2022 Aug 23;11:e81567. doi: 10.7554/eLife.81567.
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 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.
转座元件 (TEs) 是自私的遗传寄生虫,它们以牺牲宿主适应性为代价来增加自身拷贝数。TEs 在不同物种间的“成功”(即基因组范围内的丰度)差异很大。解析造成这种广泛的 TE 丰度差异的原因一直是进化基因组学的核心问题。我们之前提出,物种特异性的 TE 丰度可能是由宿主对 TEs 进行的无意识的表观遗传沉默的意外后果所驱动的——沉默 TEs 中的抑制性表观遗传标记从沉默 TEs 传播到相邻序列。在这里,我们比较了六个亚组物种中 TE 介导的局部抑制性标记富集,或“TE 的表观遗传效应”,以逐步剖析这种效应在决定基因组 TE 丰度方面的作用。我们发现,TE 介导的局部抑制性标记富集是普遍存在的,并且在不同物种甚至同一物种内都有很大差异。虽然这种 TE 介导的效应改变了相邻基因的表观遗传状态,但我们令人惊讶地发现,相邻基因的转录可以反过来影响这种传播。重要的是,我们的多物种分析提供了力量和适当的系统发育分辨率,将宿主染色质调控的物种特异性、TE 介导的表观遗传效应、对 TEs 的自然选择强度以及个别物种特有的基因组 TE 丰度联系起来。我们的研究结果表明,宿主染色质景观在通过自私遗传寄生虫的表观遗传效应塑造基因组进化方面具有重要意义。