Engineering of a specialized metabolic pathway in plants is a promising approach to produce high-value bioactive compounds to address the challenges of climate change and population growth. Understanding the interaction between the heterologous pathway and the native metabolic network of the host plant is crucial for optimizing the engineered system and maximizing the yield of the target compound. In this study, we performed transcriptomic, metabolomic and metagenomic analysis of tobacco (Nicotiana tabacum) plants engineered to produce betanin, an alkaloid pigment that is found in Caryophyllaceae plants. Our data reveals that, in a dose-dependent manor, the biosynthesis of betanin promotes carbohydrate metabolism and represses nitrogen metabolism in the leaf, but enhances nitrogen assimilation and metabolism in the root. By supplying nitrate or ammonium, the accumulation of betanin increased by 1.5–3.8-fold in leaves and roots of the transgenic plants, confirming the pivotal role of nitrogen in betanin production. In addition, the rhizosphere microbial community is reshaped to reduce denitrification and increase respiration and oxidation, assistant to suppress nitrogen loss. Our analysis not only provides a framework for evaluating the pleiotropic effects of an engineered metabolic pathway on the host plant, but also facilitates the development of novel strategies to balance the heterologous process and the native metabolic network for the high-yield and nutrient-efficient production of bioactive compounds in plants.

中文翻译：

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甜菜碱的异源生物合成触发烟草中的代谢重编程


在植物中设计专门的代谢途径是生产高价值生物活性化合物以应对气候变化和人口增长挑战的一种很有前途的方法。了解异源途径与寄主植物的天然代谢网络之间的相互作用对于优化工程系统和最大限度地提高目标化合物的产量至关重要。在这项研究中，我们对烟草 （Nicotiana tabacum） 植物进行了转录组学、代谢组学和宏基因组学分析，这些植物被改造成生产甜菜碱，甜菜碱是一种在石竹科植物中发现的生物碱色素。我们的数据显示，在剂量依赖性庄园中，甜菜碱的生物合成促进碳水化合物代谢并抑制叶片中的氮代谢，但增强根中的氮同化和代谢。通过提供硝酸盐或铵态氮，甜菜碱在转基因植物的叶和根中的积累增加了 1.5-3.8 倍，证实了氮在甜菜碱生产中的关键作用。此外，根际微生物群落被重塑以减少反式作用并增加呼吸和氧化，有助于抑制氮的损失。我们的分析不仅为评估工程代谢途径对寄主植物的多效性影响提供了一个框架，而且还有助于开发新的策略来平衡异源过程和天然代谢网络，从而在植物中高产和营养高效地生产生物活性化合物。