Terrestrialization is one of the most momentous events in the history of plant life, which leads to the subsequent evolution of plant diversity. The transition species, in this process, had to acquire a range of adaptive mechanisms to cope with the harsh features of terrestrial environments compared to that of aquatic habitat. As an ancient antioxidant, a leading regulator of ROS signaling or homeostasis, and a presumed plant master regulator, melatonin likely assisted plants transition to land and their adaption to terrestrial ecosystems. N-acetylserotonin methyltransferases (ASMT) and caffeic acid O-methyltransferases (COMT), both in the O-methyltransferase (OMT) family, catalyze the core O-methylation reaction in melatonin biosynthesis. How these two enzymes with close relevance evolved in plant evolutionary history and whether they participated in plant terrestrialization remains unknown. Using combined phylogenetic evidence and protein structure analysis, it is revealed that COMT likely evolved from ASMT by gene duplication and subsequent divergence. Newly emergent COMT gained a significantly higher ASMT activity to produce greater amounts of melatonin for immobile plants to acclimate to the stressful land environments after evolving from the more environmentally-stable aquatic conditions. The COMT genes possess more conserved substrate-binding sites at the amino acid level and more open protein conformation compared to ASMT, and getting a new function to catalyze the lignin biosynthesis. This development directly contributed to the dominance of vascular plants among the Earth's flora and prompted plant colonization of land. Thus, ASMT, together with its descendant COMT, might play key roles in plant transition to land. The current study provides new insights into plant terrestrialization with gene duplication contributing to this process along with well-known horizontal gene transfer.

中文翻译：

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褪黑激素合成基因 N-乙酰5-羟色胺甲基转移酶进化为咖啡酸 O-甲基转移酶，均有助于植物陆地化

陆地化是植物生命史上最重要的事件之一，它导致了植物多样性的后续进化。在此过程中，过渡物种必须获得一系列适应机制，以应对与水生栖息地相比陆地环境的恶劣特征。作为一种古老的抗氧化剂、活性氧信号或体内平衡的主要调节剂以及假定的植物主调节剂，褪黑激素可能有助于植物过渡到陆地并适应陆地生态系统。N-乙酰5-羟色胺甲基转移酶 (ASMT) 和咖啡酸O-甲基转移酶 (COMT) 均属于O-甲基转移酶 (OMT) 家族，催化核心O褪黑激素生物合成中的甲基化反应。这两种密切相关的酶在植物进化史上是如何进化的，它们是否参与了植物的陆地化仍然未知。结合系统发育证据和蛋白质结构分析，揭示了 COMT 可能通过基因复制和随后的分歧从 ASMT 进化而来。新出现的 COMT 获得了显着更高的 ASMT 活性，以产生更多的褪黑激素，使不动植物在从更环境稳定的水生条件进化后适应压力大的陆地环境。与ASMT相比，COMT基因在氨基酸水平上具有更保守的底物结合位点和更开放的蛋白质构象，获得了催化木质素生物合成的新功能。这一发展直接促成了维管植物在地球植物群中的主导地位，并促使植物在陆地上定居。因此，ASMT 及其后代 COMT 可能在植物向陆地的过渡中发挥关键作用。目前的研究为植物陆地化提供了新的见解，其中基因复制有助于这一过程以及众所周知的水平基因转移。