Fine-tuning immune receptor stability is essential for maintaining the balance between defense and growth in crops. Here, we identify an AAA+ ATPase–F-box regulatory module that negatively regulates potato immunity by promoting the degradation of the immune co-receptor StSOBIR1. The AAA+ ATPase StGCN4 functions as a negative regulator of potato immunity. Silencing of StGCN4 markedly enhanced resistance to Phytophthora infestans without affecting plant growth, while overexpression increased susceptibility. StGCN4 interacts with the PP2-type F-box protein StPFB1 and stabilizes it at the plasma membrane, which also negatively regulate immunity and together they facilitate proteasomal degradation of StSOBIR1, thereby dampening receptor-mediated defense signaling. Suppression of StGCN4 or StPFB1 enhances reactive oxygen species (ROS) production, salicylic acid accumulation, and expression of defense-related genes, resulting in strong resistance to P. infestans without growth penalty. These findings reveal a previously unrecognized AAA+ ATPase–F-box module that controls receptor homeostasis and identify StGCN4 as a promising molecular target for breeding high-yielding and late blight resistant potato cultivars.
Nonhost resistance (NHR) provides durable and broad-spectrum protection against non-adapted pathogens, yet its regulatory mechanisms in crops remain poorly understood. Here, we show that salicylic acid (SA) signaling plays a critical role in potato NHR against the oomycete pathogen Phytophthora capsici. SA-deficient NahG transgenic plants developed spreading water-soaked lesions following inoculation, whereas wild-type plants exhibited only localized necrosis. Exogenous SA treatment partially restored resistance in NahG lines, supporting an important role for SA in potato NHR. Transcriptome analysis revealed that SA deficiency suppressed defense-associated pathways, including MAPK signaling and pathogenesis-related (PR) gene expression, while inducing photosynthesis- and carbohydrate metabolism-associated genes. In addition, transcriptomic data suggested altered hormone-associated signaling, including induction of ABA-, IAA-, and JA-related pathways, indicating broad transcriptional changes in response to SA deficiency. Functional assays further demonstrated that silencing ERF1B enhanced susceptibility, whereas silencing WRKY53 increased resistance, suggesting distinct transcriptional regulatory roles downstream of SA signaling. Together, these findings support a central role for SA in coordinating immune signaling and metabolic responses during potato nonhost resistance. This study provides new insights into the regulatory framework underlying potato-oomycete interactions.