State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100039, China.
Mol Plant. 2018 Oct 8;11(10):1264-1277. doi: 10.1016/j.molp.2018.07.003. Epub 2018 Jul 25.
Nicotinamide adenine dinucleotide (NAD) biosynthesis, including synthesis from aspartate via the de novo pathway and from nicotinate (NA) via the Preiss-Handler pathway, is conserved in land plants. Diverse species of NA conjugates, which are mainly involved in NA detoxification, were also found in all tested land plants. Among these conjugates, MeNA (NA methyl ester) has been widely detected in angiosperm plants, although its physiological function and the underlying mechanism for its production in planta remain largely unknown. Here, we show that MeNA is an NAD precursor undergoing more efficient long-distance transport between organs than NA and nicotinamide in Arabidopsis. We found that Arabidopsis has one methyltransferase (designated AtNaMT1) capable of catalyzing carboxyl methylation of NA to yield MeNA and one methyl esterase (MES2) predominantly hydrolyzing MeNA back to NA. We further uncovered that the transfer of [C]MeNA from the root to leaf was significantly increased in both MES2 knockdown and NaMT1-overexpressing lines, suggesting that both NaMT1 and MES2 fine-tune the long-distance transport of MeNA, which is ultimately utilized for NAD production. Abiotic stress (salt, abscisic acid, and mannitol) treatments, which are known to exacerbate NAD degradation, induce the expression of NaMT1 but suppress MES2 expression, suggesting that MeNA may play a role in stress adaption. Collectively, our study indicates that reversible methylation of NA controls the biosynthesis of MeNA in Arabidopsis, which presumably functions as a detoxification form of free NA for efficient long-distance transport and eventually NAD production especially under abiotic stress, providing new insights into the relationship between NAD biosynthesis and NA conjugation in plants.
烟酰胺腺嘌呤二核苷酸 (NAD) 的生物合成，包括通过从头途径从天冬氨酸和通过 Preiss-Handler 途径从烟碱酸 (NA) 合成，在陆地植物中是保守的。还在所有测试的陆地植物中发现了多种主要参与 NA 解毒的 NA 缀合物。在这些缀合物中，MeNA（NA 甲酯）在被子植物中被广泛检测到，尽管其生理功能及其在植物体内产生的潜在机制在很大程度上仍然未知。在这里，我们表明 MeNA 是 NAD 的前体，在拟南芥中比 NA 和烟酰胺更有效地在器官间进行长距离运输。我们发现拟南芥有一个甲基转移酶（命名为 AtNaMT1）能够催化 NA 的羧基甲基化生成 MeNA 和一个甲酯酶（MES2）主要将 MeNA 水解回 NA。我们进一步发现，在 MES2 敲低和 NaMT1 过表达系中，从根到叶的 [C]MeNA 转移显著增加，这表明 NaMT1 和 MES2 都可以微调 MeNA 的长距离运输，最终用于 NAD 的产生。已知非生物胁迫（盐、脱落酸和甘露醇）处理会加剧 NAD 降解，诱导 NaMT1 的表达但抑制 MES2 的表达，这表明 MeNA 可能在适应应激中发挥作用。总之，我们的研究表明，NA 的可逆甲基化控制拟南芥中 MeNA 的生物合成，这可能是游离 NA 的解毒形式，用于有效长距离运输，最终在非生物胁迫下产生 NAD，为植物中 NAD 生物合成和 NA 缀合之间的关系提供了新的见解。
