Rongyi Jiang, Tao Tao, Xingbin Xie, Yang Liu, Yanan Sun, Yang Zhang, Guanghui Zheng, Peipei Sun, Mauren Jaudal, Simona Nardozza, Congbing Fang, Jing Zhao
Powdery mildew, caused by Podosphaera aphanis, poses a significant threat to strawberry production, while current chemical controls raise environmental and food safety concerns. In this study, we have identified the key regulatory module, FaMYB63/FvWRKY75-PR10.14, that confers enhanced powdery mildew resistance in transgenic strawberry (Fragaria vesca). FaMYB63, an R2R3-MYB transcription factor, was induced by P. aphanis infection and responsive to the application of defence signalling molecules, including salicylic acid (SA), methyl jasmonate (JA), abscisic acid (ABA), and 1-aminocyclopropane-1-carboxylic acid (ACC). Silencing of FaMYB63 led to reduced SA levels and increased powdery mildew susceptibility, accompanied by suppressed reactive oxygen species (ROS) bursts and down-regulation of PR10.14 expression. Conversely, overexpressing PR10.14 in transgenic lines inhibited P. aphanis spore germination and enhanced ROS accumulation, indicating a dual role in direct pathogen inhibition and hypersensitive response-triggered defence. Yeast one-hybrid, electrophoretic mobility shift assay, β-glucuronidase, and luciferase assays confirmed that FaMYB63 and FvWRKY75 were directly bound to the MYB-binding sites and W-box of the PR10.14 promoter, respectively, and activated its transcription, while WRKY75 negatively regulated the expression of MYB63. PR10.14 exhibited tissue-specific expression, with the highest levels in red-ripening fruits, suggesting a role in developmental-stage-dependent defence. These findings suggest FaMYB63 as an SA-dependent regulator of PR10.14-mediated resistance, bridging hormone signalling and pathogen response. This study provides a molecular target for breeding powdery mildew-resistant strawberry cultivars through genetic engineering approaches, offering an alternative to fungicides for sustainable and environmental disease management in horticultural crops and advances our understanding of MYB- or WRKY-PR10P networks in plant immunity.