Obligate biotrophs depend on living hosts for nutrient acquisition to complete their life cycle, yet the mechanisms by which hosts restrict nutrient availability to pathogens remain largely unknown. The fungal pathogen Sporisorium reilianum infects maize seedlings and causes head smut disease in inflorescences at maturity, while a cell wall-associated kinase, ZmWAK, provides quantitative resistance against it. In this study, we demonstrate that S. reilianum can rapidly activate ZmWAK kinase activity, which is sustained by the 407th threonine residue in the juxtamembrane domain, enabling it to interact with and phosphorylate ZmSnRK1α2, a conserved sucrose non-fermenting-related kinase α subunit. The activated ZmSnRK1α2 translocates from the cytoplasm to the nucleus, where it phosphorylates and destabilizes the transcription factor ZmWRKY53. The reduced ZmWRKY53 abundance leads to the downregulation of genes involved in transmembrane transport and carbohydrate metabolism, resulting in nutrient starvation for S. reilianum in the apoplast. Collectively, our study uncovers a WAK-SnRK1α2-WRKY53 signaling module in maize that conveys phosphorylation cascades from the plasma membrane to the nucleus to confer plant resistance against head smut in maize, offering new insights and potential targets for crop disease management.

中文翻译：

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玉米 WAK-SnRK1α2-WRKY 模块调节养分有效性以抵御黑穗病


专性生物营养生物依靠活宿主获取营养物质以完成其生命周期，但宿主限制病原体获得营养物质的机制在很大程度上仍然未知。真菌病原体 Sporisorium reilianum 感染玉米幼苗，并在成熟时在花序中引起头黑穗病，而细胞壁相关激酶 ZmWAK 对其提供定量抗性。在这项研究中，我们证明 S. reilianum 可以快速激活 ZmWAK 激酶活性，该活性由近膜结构域中的第 407 个苏氨酸残基维持，使其能够与 ZmSnRK1α2 相互作用并磷酸化 ZmSnRK1α2，ZmSnRK1α2 是一种保守的蔗糖非发酵相关激酶α亚基。激活的 ZmSnRK1α2 从细胞质易位到细胞核，在那里它磷酸化并破坏转录因子 ZmWRKY53 的稳定性。ZmWRKY53 丰度降低导致参与跨膜转运和碳水化合物代谢的基因下调，导致质外体中 S. reilianum 的营养饥饿。总的来说，我们的研究揭示了玉米中的 WAK-SnRK1α2-WRKY53 信号模块，该模块将磷酸化级联反应从质膜传递到细胞核，以赋予植物对玉米黑穗病的抗性，为作物病害管理提供了新的见解和潜在靶点。