Yan Juanmei, Feng Zhihang, Xiao Yihui, Zhou Ming, Zhao Xiaobo, Lin Xianyong, Shi Weiming, Busch Wolfgang, Li Baohai
Ministry of Education Key Laboratory of Environment Remediation and Ecological Health, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China.
State Key Laboratory of Plant Environmental Resilience, College of Life Sciences, Zhejiang University, Hangzhou 310058, China.
Proc Natl Acad Sci U S A. 2025 Jan 7;122(1):e2411579122. doi: 10.1073/pnas.2411579122. Epub 2024 Dec 30.
While iron (Fe) is essential for life and plays important roles for almost all growth related processes, it can trigger cell death in both animals and plants. However, the underlying mechanisms for Fe-induced cell death in plants remain largely unknown. S-nitrosoglutathione reductase (GSNOR) has previously been reported to regulate nitric oxide homeostasis to prevent Fe-induced cell death within root meristems. Here, we found that in the absence of , exposure to high Fe treatment results in DNA damage-dependent cell death specifically in vascular stem cells in root meristems within 48 h. Through a series of time-course transcriptomic analyses, we unveil that in the absence of , mitochondrial dysfunction emerges as the most prominent response to high Fe treatment. Consistently, the application of mitochondrial respiratory inhibitors leads to stem cell death in root meristems, and pharmacological blockage of the voltage-dependent anion channel that is responsible for the release of mitochondrial-derived molecules into the cytosol or genetic changes that abolish the ANAC017- and ANAC013-mediated mitochondrial retrograde signaling effectively eliminate Fe-induced stem cell death in root meristems. We further identify the nuclear transcription factor ANAC044 as a mediator of this mitochondrial retrograde signaling. Disruption of completely abolishes the GSNOR-dependent, Fe-induced stem cell death in root meristems, while ectopic expression of causes severe root stem cell death. Collectively, our findings reveal a mechanism responsible for initiating Fe-induced stem cell death in the root meristem, which is the ANAC044-mediated GSNOR-regulated mitochondrial stress signaling pathway.
虽然铁（Fe）对生命至关重要，并且在几乎所有与生长相关的过程中都发挥着重要作用，但它可引发动植物的细胞死亡。然而，植物中铁诱导的细胞死亡的潜在机制在很大程度上仍不清楚。此前有报道称，S-亚硝基谷胱甘肽还原酶（GSNOR）可调节一氧化氮稳态，以防止根分生组织内铁诱导的细胞死亡。在这里，我们发现，在缺乏（此处原文缺失相关内容）的情况下，暴露于高铁处理会在48小时内导致根分生组织中维管干细胞特异性地发生依赖于DNA损伤的细胞死亡。通过一系列时间进程转录组分析，我们揭示，在缺乏（此处原文缺失相关内容）的情况下，线粒体功能障碍成为对高铁处理最显著的反应。一致地，应用线粒体呼吸抑制剂会导致根分生组织中的干细胞死亡，而对负责将线粒体衍生分子释放到细胞质中的电压依赖性阴离子通道进行药理学阻断，或消除ANAC017和ANAC013介导的线粒体逆行信号传导的基因变化，可有效消除根分生组织中铁诱导的干细胞死亡。我们进一步确定核转录因子ANAC044是这种线粒体逆行信号传导的介质。（此处原文缺失相关内容）的破坏完全消除了根分生组织中GSNOR依赖性、铁诱导的干细胞死亡，而异位表达（此处原文缺失相关内容）则会导致严重的根干细胞死亡。总的来说，我们的研究结果揭示了一种在根分生组织中引发铁诱导的干细胞死亡的机制，即ANAC044介导的GSNOR调节的线粒体应激信号通路。
