Maize requires arogenate dehydratase 2 for resistance to Ustilago maydis and plant development

• Published in: Plant physiology (Bethesda) 2024-05, Vol.195 (2), p.1642-1659
• Main Authors: Ren, Ru Chang, Kong, Ling Guang, Zheng, Guang Ming, Zhao, Ya Jie, Jiang, Xin, Wu, Jia Wen, Liu, Cuimei, Chu, Jinfang, Ding, Xin Hua, Zhang, Xian Sheng, Wang, Guan Feng, Zhao, Xiang Yu
• Format: Article
• Language: English
• Subjects: Basidiomycota - physiology; Disease Resistance - genetics; Gene Expression Regulation, Plant; Hydro-Lyases - genetics; Hydro-Lyases - metabolism; Mutation - genetics; Phenotype; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - microbiology; Plant Proteins - genetics; Plant Proteins - metabolism; Salicylic Acid - metabolism; Ustilago - genetics; Zea mays - genetics; Zea mays - growth & development; Zea mays - microbiology
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1093/plphys/kiae115

Maize (Zea mays) smut is a common biotrophic fungal disease caused by Ustilago maydis and leads to low maize yield. Maize resistance to U. maydis is a quantitative trait. However, the molecular mechanism underlying the resistance of maize to U. maydis is poorly understood. Here, we reported that a maize mutant caused by a single gene mutation exhibited defects in both fungal resistance and plant development. maize mutant highly susceptible to U. maydis (mmsu) with a dwarf phenotype forms tumors in the ear. A map-based cloning and allelism test demonstrated that 1 gene encoding a putative arogenate dehydratase/prephenate dehydratase (ADT/PDT) is responsible for the phenotypes of the mmsu and was designated as ZmADT2. Combined transcriptomic and metabolomic analyses revealed that mmsu had substantial differences in multiple metabolic pathways in response to U. maydis infection compared with the wild type. Disruption of ZmADT2 caused damage to the chloroplast ultrastructure and function, metabolic flux redirection, and reduced the amounts of salicylic acid (SA) and lignin, leading to susceptibility to U. maydis and dwarf phenotype. These results suggested that ZmADT2 is required for maintaining metabolic flux, as well as resistance to U. maydis and plant development in maize. Meanwhile, our findings provided insights into the maize response mechanism to U. maydis infection.