Major evolutionary transitions are enigmas, and the most notable enigma is between invertebrates and vertebrates, with numerous spectacular innovations. To search for the molecular connections involved, we asked whether global epigenetic changes may offer a clue by surveying the inheritance and reprogramming of parental DNA methylation across metazoans. We focused on gametes and early embryos, where the methylomes are known to evolve divergently between fish and mammals. Here, we find that methylome reprogramming during embryogenesis occurs neither in pre-bilaterians such as cnidarians nor in protostomes such as insects, but clearly presents in deuterostomes such as echinoderms and invertebrate chordates, and then becomes more evident in vertebrates. Functional association analysis suggests that DNA methylation reprogramming is associated with development, reproduction and adaptive immunity for vertebrates, but not for invertebrates. Interestingly, the single HOX cluster of invertebrates maintains unmethylated status in all stages examined. In contrast, the multiple HOX clusters show dramatic dynamics of DNA methylation during vertebrate embryogenesis. Notably, the methylation dynamics of HOX clusters are associated with their spatiotemporal expression in mammals. Our study reveals that DNA methylation reprogramming has evolved dramatically during animal evolution, especially after the evolutionary transitions from invertebrates to vertebrates, and then to mammals.

中文翻译：

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通过胚胎发生中的甲基化重编程实现无脊椎动物和脊椎动物之间的进化转变

主要的进化转变是谜，最显着的谜是无脊椎动物和脊椎动物之间，有许多惊人的创新。为了寻找所涉及的分子联系，我们通过调查跨后生动物的亲本 DNA 甲基化的遗传和重编程，询问全球表观遗传变化是否可以提供线索。我们专注于配子和早期胚胎，已知甲基组在鱼类和哺乳动物之间进化不同。在这里，我们发现胚胎发生过程中的甲基化重编程既不发生在前双侧动物（如刺胞动物）中，也不发生在原虫（如昆虫）中，但清楚地存在于后口动物（如棘皮动物和无脊椎动物脊索动物）中，然后在脊椎动物中变得更加明显。功能关联分析表明，DNA 甲基化重编程与脊椎动物的发育、繁殖和适应性免疫有关，但与无脊椎动物无关。有趣的是，无脊椎动物的单个 HOX 簇在检查的所有阶段都保持未甲基化状态。相比之下，多个 HOX 簇在脊椎动物胚胎发生过程中显示出 DNA 甲基化的戏剧性动态。值得注意的是，HOX 簇的甲基化动力学与其在哺乳动物中的时空表达相关。我们的研究表明，DNA 甲基化重编程在动物进化过程中发生了巨大的变化，尤其是在从无脊椎动物到脊椎动物再到哺乳动物的进化转变之后。无脊椎动物的单个 HOX 簇在检查的所有阶段都保持未甲基化状态。相比之下，多个 HOX 簇在脊椎动物胚胎发生过程中显示出 DNA 甲基化的戏剧性动态。值得注意的是，HOX 簇的甲基化动力学与其在哺乳动物中的时空表达相关。我们的研究表明，DNA 甲基化重编程在动物进化过程中发生了巨大的变化，尤其是在从无脊椎动物到脊椎动物再到哺乳动物的进化转变之后。无脊椎动物的单个 HOX 簇在检查的所有阶段都保持未甲基化状态。相比之下，多个 HOX 簇在脊椎动物胚胎发生过程中显示出 DNA 甲基化的戏剧性动态。值得注意的是，HOX 簇的甲基化动力学与其在哺乳动物中的时空表达相关。我们的研究表明，DNA 甲基化重编程在动物进化过程中发生了巨大的变化，尤其是在从无脊椎动物到脊椎动物再到哺乳动物的进化转变之后。