Data from: Allele-specific transcriptome and methylome analysis reveals stable inheritance and cis-regulation of DNA methylation in Nasonia

Gene expression divergence between closely related species could be attributed to both cis- and trans- DNA sequence changes during evolution, but it is unclear how the evolutionary dynamics of epigenetic marks are regulated. In eutherian mammals, biparental DNA methylation marks are erased and reset during gametogenesis, resulting in paternal or maternal imprints which lead to genomic imprinting. Whether DNA methylation reprogramming exists in insects is not known. Wasps of the genus Nasonia are non-social parasitoids that are emerging as a model for studies of epigenetic processes in insects. In this study, we quantified allele-specific expression and methylation genome-wide in Nasonia vitripennis and Nasonia giraulti and their reciprocal F1 hybrids. No parent-of-origin effect in allelic expression was found for >8,000 covered genes, suggesting a lack of genomic imprinting in adult Nasonia. As we expected, both significant cis- and trans- effects are responsible
for the expression divergence between N. vitripennis and N. giraulti. Surprisingly, all 178 differentially methylated genes are also differentially methylated between the two alleles in F1 hybrid offspring, recapitulating the parental methylation status with nearly 100% fidelity, indicating the presence of strong cis-elements driving the target of gene body methylation. In addition, we discovered that total and allele-specific expression is positively correlated with allele-specific methylation in a subset of the differentially methylated genes. The 100% cis-regulation in F1 hybrids suggests the methylation machinery is conserved and DNA methylation is targeted by cis features in Nasonia. The lack of genomic imprinting and parent-of-origin differentially methylated regions in Nasonia, together with the stable inheritance of methylation status between generations suggest either a cis regulatory motif for methylation at the DNA level or highly stable inheritance of an
epigenetic signal in Nasonia.

近缘物种间的基因表达差异，可归因于演化过程中顺式（cis）与反式（trans）DNA序列改变，但表观遗传标记的演化动力学如何被调控，目前仍不明确。在真兽类哺乳动物中，双亲的DNA甲基化标记会在配子发生过程中被清除并重设，进而形成父本或母本印记，最终引发基因组印记（genomic imprinting）。昆虫中是否存在DNA甲基化重编程仍属未知。金小蜂属（Nasonia）的非社会性寄生蜂正逐渐成为昆虫表观遗传过程研究的模式生物。本研究对丽蝇蛹集金小蜂（Nasonia vitripennis）、吉氏金小蜂（Nasonia giraulti）及其正反交F1杂种进行了全基因组范围的等位基因特异性表达与甲基化定量分析。在超过8000个被覆盖的基因中，未发现等位基因表达存在亲本来源效应，这表明成年金小蜂体内不存在基因组印记。正如预期，显著的顺式与反式作用共同导致了两种金小蜂间的表达差异。令人意外的是，178个差异甲基化基因在F1杂种的两个等位基因间同样存在甲基化差异，以近100%的保真度重现了亲本的甲基化状态，这表明存在调控基因体甲基化靶标的强效顺式元件。此外，我们发现，在部分差异甲基化基因中，总表达量与等位基因特异性表达量均与等位基因特异性甲基化呈正相关。F1杂种中完全的顺式调控现象表明，金小蜂体内的甲基化机制具有保守性，且DNA甲基化由顺式特征所靶向调控。金小蜂中不存在基因组印记与亲本来源特异性差异甲基化区域，加之甲基化状态在代际间的稳定遗传，这提示金小蜂中要么存在DNA层面的甲基化顺式调控基序，要么表观遗传信号具有极高的代际遗传稳定性。