Graphene enhances artemisinin production in the traditional medicinal plant Artemisia annua via dynamic physiological processes and miRNA regulation
Junfeng Cao, Zhiwen Chen, Luyao Wang, Ning Yan, Jia‐Ling Lin, Li-Pan Hou, Yongyan Zhao, Chaochen Huang, Tingting Wen, Chenyi Li, Saeed Ur Rahman, Zehui Liu, Jun Qiao, Jianguo Zhao, Jie Wang, Yannan Shi, Wei Qin, Tong Si, Yuliang Wang, Kexuan Tang
Abstract
Graphene was used to investigate its effects on the model herb, Artemisia annua, renowned for producing artemisinin, a widely-used pharmacological compound. The seedlings' growth and biomass were promoted when the A. annua was cultivated with low graphene concentrations, which was attributed to a 1.4-fold increase in nitrogen uptake, a 15% to 22% rise in chlorophyll fluorescence, and increased carbon cycling-related bacterial abundance. Moreover, exposure to 10 or 20 mg/L graphene resulted in an approximately 60% increase in H2O2, while graphene could act as a catalyst accelerator, leading to a 9-fold increase in catalase (CAT) activity in vitro, thereby maintaining reactive oxygen species (ROS) homeostasis. Importantly, graphene exposure led to an 80% increase in the density of glandular-secreting trichomes (GSTs), where artemisinin is biosynthesized and stored. This contributed to a 5% increase in artemisinin content in mature leaves. Interestingly, the expression of miR828 was reduced by both graphene and H2O2 treatments, resulting in the induction of its target gene AaMYB17, a positive regulator of GST initiation. Subsequent molecular and genetic assays showed that graphene-induced H2O2 inhibits miRNA biogenesis through Dicers and regulates the miR828-AaMYB17 module, thus affecting GST density. Above all, graphene may contribute to yield improvement for A. annua via the dynamic physiological progress together with the miRNA regulation, which provides us with a new cultivation strategy to release the yield capacity by nanobiotechnology.