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.

顺式（cis-）与反式（trans-）DNA序列改变均可导致近缘物种间的基因表达分化，但表观遗传标记的进化动态调控机制目前仍不明确。在真兽类哺乳动物中，双亲的DNA甲基化标记会在配子发生（gametogenesis）过程中被清除并重置，形成父本或母本印记，进而引发基因组印记（genomic imprinting）。目前尚不清楚昆虫体内是否存在DNA甲基化重编程现象。丽金小蜂属（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。本研究对丽金小蜂（Nasonia vitripennis）、长颈鹿丽金小蜂（Nasonia giraulti）及其正反交F1杂种（reciprocal F1 hybrids）开展了全基因组范围内的等位基因特异性表达（allele-specific expression）与甲基化水平定量分析。在覆盖的8000余个基因中，未检测到等位基因表达存在亲本起源效应，提示成年丽金小蜂体内不存在基因组印记。正如预期，显著的顺式与反式调控效应共同导致了N. vitripennis与N. giraulti之间的表达分化。令人意外的是，178个差异甲基化基因（differentially methylated genes）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，表明存在强效顺式作用元件驱动基因体甲基化（gene body methylation）的靶标调控。此外，本研究发现，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杂种中呈现的100%顺式调控现象表明，丽金小蜂的甲基化调控机制（methylation machinery）具有保守性，且DNA甲基化的靶向性由顺式特征决定。丽金小蜂体内既不存在基因组印记与亲本起源特异性差异甲基化区域，其甲基化状态又能在世代间稳定遗传，这提示丽金小蜂的甲基化调控要么存在DNA层面的顺式调控基序（cis regulatory motif），要么其表观遗传信号具有高度稳定的继承性。