Comparative transcriptome analysis reveals key genes and signaling pathways mediated by salicylic acid in potato.

BACKGROUND: Salicylic acid (SA) is a key phytohormone involved in regulating plant growth, development, and immune responses. While its signaling roles have been extensively characterized in model species, the molecular mechanisms and SA-responsive genes in potato remain largely uncharacterized. OBJECTIVE: This study aims to elucidate the SA-mediated transcriptional network in potato by conducting a comparative transcriptomic analysis under treatments with exogenous SA and 1-aminobenzotriazole (ABT), a pan-selective cytochrome P450 inhibitor, that impairs enzymes required for salicylic acid (SA) biosynthesis. RESULTS: RNA-seq analysis identified 6,668 and 3,815 differentially expressed genes (DEGs) under SA and ABT treatments, respectively, with 1,759 DEGs displaying inverse expression patterns between the two treatments. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses revealed that these DEGs are predominantly involved in phenylpropanoid biosynthesis, glutathione metabolism, plant hormone signal transduction, MAPK signaling, and plant-pathogen interactions. Exogenous SA activated genes associated with gibberellin, abscisic acid, brassinosteroid, and SA signaling pathways, while suppressing key jasmonic acid signaling genes, including JAR1 and MYC2. In addition, multiple PR1 genes and transcription factors from the WRKY, ERF, C2H2, MYB, and NAC families were strongly upregulated by SA. Functional validation using virus-induced gene silencing demonstrated that NbPAL1 and NbPAL2 are essential regulators of SA biosynthesis. Moreover, transcriptomic data revealed the robust induction of detoxification-related enzymes under SA treatment, including 19 glutathione S-transferases and 30 cytochrome P450 genes. Notably, two isoforms of CYP94B3, involved in JA-Ile hydroxylation, were induced by SA and repressed by ABT. CONCLUSION: This study provides a comprehensive overview of SA-responsive gene expression in potato, uncovering key regulatory components and pathways within the SA signaling network. The findings offer valuable insights for future functional studies and genetic improvement strategies targeting SA-mediated disease resistance in potato.