The ZmPIF4.1-ZmPTI1c-ZmMYB31 module regulates maize immunity to Gibberella stalk rot caused by Fusarium graminearum

Gibberella stalk rot (GSR) caused by Fusarium graminearum is one of the most devastating diseases of maize, seriously impacting maize yield and quality, as well as the ability to use technology of mechanical harvesting. Environmental conditions including photoperiod affect crop disease resistance. However, the mechanism underlying photoperiod-regulated maize GSR resistance remains unexplored. We found in this study that GSR resistance is regulated by the ZmPIF4.1 (Phytochrome-Interacting Factor 4)-ZmPTI1c (Pto-Interacting 1)-ZmMYB31 module coupled with photoperiod. The functional analysis of zmpti1c mutant indicated that ZmPTI1c negatively regulates maize GSR resistance. Short day promoted the disease progression in both zmpti1c and wild-type plants. ZmPTI1c promoter contains multiple predicted cis-acting elements for light responses. Yeast one-hybrid assay (Y1H), Electrophoretic mobility shift analysis (EMSA), and Dual-luciferase (LUC) reporter assays demonstrated that ZmPIF4.1 binds to the G-box in ZmPTI1c promoter and activates its expression. Moreover, expression levels of ZmPIF4 and ZmPTI1c were significantly higher under short day than under long day. ZmPTI1c interacted with and phosphorylated ZmMYB31. GSR resistance in zmmyb31 mutant was significantly increased than in wild type, indicating that ZmMYB31 also negatively regulated GSR resistance. Furthermore, ZmMYB31 suppressed the transcriptional activation of ZmPTI1c by ZmPIF4.1. Overall, ZmPIF4.1-ZmPTI1c-ZmMYB31 negatively regulates maize immunity to GSR, which is likely modulated by photoperiod.