Salicylic acid signaling integrates immunity and metabolic regulation to govern nonhost resistance in potato against Phytophthora capsici.

Abstract

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.