A maize WAK-SnRK1α2-WRKY module regulates nutrient availability to defend against head smut disease

• Published in: Molecular plant 2024-11, Vol.17 (11), p.1654-1671
• Main Authors: Zhang, Qianqian, Xu, Qianya, Zhang, Nan, Zhong, Tao, Xing, Yuexian, Fan, Zhou, Yan, Mingzhu, Xu, Mingliang
• Format: Article
• Language: English
• Subjects: Basidiomycota - physiology; Disease Resistance - genetics; Gene Expression Regulation, Plant; head smut disease; nutrient; Nutrients - metabolism; Phosphorylation; Plant Diseases - microbiology; Plant Proteins - genetics; Plant Proteins - metabolism; SnRK1α2; Sporisorium reilianum; Zea mays - genetics; Zea mays - metabolism; Zea mays - microbiology; ZmWAK
• ISSN: 1674-2052; 1752-9867; 1752-9867
• DOI: 10.1016/j.molp.2024.09.013

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. The fungal pathogen Sporisorium reilianum causes maize head smut disease. Upon detecting S. reilianum, the plasma membrane-localized receptor ZmWAK phosphorylates ZmSnRK1α2, which then translocates to the nucleus and phosphorylates ZmWRKY53. The reduction of ZmWRKY53 downregulates genes involved in nutrient transport and metabolism, leading to nutrient starvation for the pathogen and helping to control head smut disease.