State Key Laboratory of Hybrid Rice, College of Life Sciences, Renmin Hospital of Wuhan University, Wuhan University, Wuhan 430072, China; Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan 430062, China.
State Key Laboratory of Hybrid Rice, College of Life Sciences, Renmin Hospital of Wuhan University, Wuhan University, Wuhan 430072, China.
Mol Plant. 2024 Feb 5;17(2):325-341. doi: 10.1016/j.molp.2024.01.001. Epub 2024 Jan 3.
Xanthomonas oryzae pv. oryzae (Xoo) causes bacterial blight (BB), a globally devastating disease of rice (Oryza sativa) that is responsible for significant crop loss. Sugars and sugar metabolites are important for pathogen infection, providing energy and regulating events associated with defense responses; however, the mechanisms by which they regulate such events in BB are unclear. As an inevitable sugar metabolite, methylglyoxal (MG) is involved in plant growth and responses to various abiotic stresses, but the underlying mechanisms remain enigmatic. Whether and how MG functions in plant biotic stress responses is almost completely unknown. Here, we report that the Xoo strain PXO99 induces OsWRKY62.1 to repress transcription of OsGLY II genes by directly binding to their promoters, resulting in overaccumulation of MG. MG negatively regulates rice resistance against PXO99: osglyII2 mutants with higher MG levels are more susceptible to the pathogen, whereas OsGLYII2-overexpressing plants with lower MG content show greater resistance than the wild type. Overexpression of OsGLYII2 to prevent excessive MG accumulation confers broad-spectrum resistance against the biotrophic bacterial pathogens Xoo and Xanthomonas oryzae pv. oryzicola and the necrotrophic fungal pathogen Rhizoctonia solani, which causes rice sheath blight. Further evidence shows that MG reduces rice resistance against PXO99 through CONSTITUTIVE DISEASE RESISTANCE 1 (OsCDR1). MG modifies the Arg97 residue of OsCDR1 to inhibit its aspartic protease activity, which is essential for OsCDR1-enhanced immunity. Taken together, these findings illustrate how Xoo promotes infection by hijacking a sugar metabolite in the host plant.
稻黄单胞菌（Xanthomonas oryzae pv. oryzae，Xoo）引起细菌性条斑病（BB），这是一种全球范围内破坏性极大的水稻病害，会导致严重的作物减产。糖和糖代谢物对病原体感染很重要，它们为病原体提供能量并调节与防御反应相关的事件；然而，它们调节 BB 中此类事件的机制尚不清楚。作为一种不可避免的糖代谢物，甲基乙二醛（MG）参与植物生长和对各种非生物胁迫的响应，但潜在机制仍不清楚。MG 是否以及如何在植物生物胁迫反应中发挥作用几乎完全未知。在这里，我们报告称，Xoo 菌株 PXO99 通过直接结合其启动子诱导 OsWRKY62.1 抑制 OsGLY II 基因的转录，导致 MG 的过度积累。MG 负调控水稻对 PXO99 的抗性：MG 水平较高的 osglyII2 突变体对病原体更敏感，而 MG 含量较低的 OsGLYII2 过表达植物比野生型表现出更强的抗性。过表达 OsGLYII2 以防止 MG 过度积累赋予了广谱抗性，可抵抗生营养细菌病原体 Xoo 和稻黄单胞菌（Xanthomonas oryzae pv. oryzicola）以及坏死真菌病原体稻纹枯病菌（Rhizoctonia solani），这些病原体引起水稻纹枯病。进一步的证据表明，MG 通过组成型抗病 1 （OsCDR1）降低了水稻对 PXO99 的抗性。MG 修饰 OsCDR1 的 Arg97 残基以抑制其天冬氨酸蛋白酶活性，这对 OsCDR1 增强的免疫至关重要。总之，这些发现说明了 Xoo 如何通过劫持宿主植物中的糖代谢物来促进感染。
