Discovery of a novel nucleoside immune signaling molecule 2′-deoxyguanosine in microbes and plants

• Published in: Journal of advanced research 2023-04, Vol.46, p.1-15
• Main Authors: Lu, Chongchong, Wang, Qingbin, Jiang, Yanke, Zhang, Min, Meng, Xuanlin, Li, Yang, Liu, Baoyou, Yin, Ziyi, Liu, Haifeng, Peng, Chune, Li, Fuchuan, Yue, Yingzhe, Hao, Mingxia, Sui, Yurong, Wang, Lulu, Cheng, Guodong, Liu, Jianzhu, Chu, Zhaohui, Zhu, Changxiang, Dong, Hansong, Ding, Xinhua
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Deoxyguanosine; Endophytic fungi; ET signaling; NPR1; Nucleosides; Original; Pattern- recognition receptors/coreceptors; Plant immune elicitor; Plants; Signal Transduction
• ISSN: 2090-1232; 2090-1224
• DOI: 10.1016/j.jare.2022.06.014

Model of 2′-deoxyguanosine involvement in plant immune response. Endophytic fungus-derived 2-dG directly activates ET signaling, EIT and PTI. Moreover, pathogen invasion induces the expression of the plant 2-dG biosynthesis gene VEN4 and promotes 2-dG accumulation in plant leaves. However, 2-dG-mediated plant resistance against Pst DC3000 is conferred in an ET-, NPR1-, PRR/coreceptor- and P2K1-dependent manner. [Display omitted] •We identified for the first time that nucleoside 2′-deoxyguanosine from endophytic fungal metabolites can effectively stimulate classical immune responses in plants.•We demonstrated that 2-dG-induced plant resistance depends on salicylic acid (SA) receptor NPR1 (but not SA), ethylene (ET) signaling, pattern-recognition receptors/coreceptors (PRRs/coreceptors) and the ATP receptor P2K1.•We provide the first demonstration that VEN4 is 2-dG biosynthesis gene and involved in pathogen-induced 2-dG accumulation, VEN4 also plays an essential role for plant immunity. Beneficial microorganisms play essential roles in plant growth and induced systemic resistance (ISR) by releasing signaling molecules. Our previous study obtained the crude extract from beneficial endophyte Paecilomyces variotii, termed ZNC (ZhiNengCong), which significantly enhanced plant resistance to pathogen even at 100 ng/ml. However, the immunoreactive components of ZNC remain unclear. Here, we further identified one of the immunoreactive components of ZNC is a nucleoside 2′-deoxyguanosine (2-dG). This paper intends to reveal the molecular mechanism of microbial-derived 2′-deoxyguanosine (2-dG) in activating plant immunity, and the role of plant-derived 2-dG in plant immunity. The components of ZNC were separated using a high-performance liquid chromatography (HPLC), and 2-dG is identified using a HPLC–mass spectrometry system (LC-MS). Transcriptome analysis and genetic experiments were used to reveal the immune signaling pathway dependent on 2-dG activation of plant immunity. This study identified 2′-deoxyguanosine (2-dG) as one of the immunoreactive components from ZNC. And 2-dG significantly enhanced plant pathogen resistance even at 10 ng/ml (37.42 nM). Furthermore, 2-dG-induced resistance depends on NPR1, pattern-recognition receptors/coreceptors, ATP receptor P2K1 (DORN1), ethylene signaling but not salicylic acid accumulation. In addition, we identified Arabidopsis VENOSA4 (VEN4) was involved in 2-dG biosynthesis and could convert dGTP to 2-dG, and vne4 mutant pl