Integrated transcriptomic and metabolomic dynamics reveal mechanisms of tobacco resistance to Phytophthora nicotianae.
Tobacco is a model plant as well as an important economic crop. Black shank disease, caused by Phytophthora nicotianae, severely undermines tobacco yield and quality, yet the molecular basis of differential cultivar resistance remains incompletely understood. Here, we compared the resistant cultivar, 'Xiangyan 7' (X7) and the susceptible cultivar 'Honghuadajinyuan' (HD), after inoculation with P. nicotianae race 0. Disease evaluation showed that X7 had a significantly lower disease index than HD. Transcriptomic and metabolomic analyses were performed on leaves collected at 0, 1, 2, 4, 8, and 12 days post-inoculation (dpi). RNA-seq identified extensive transcriptional responses in both cultivars; the inter-cultivar differentially expressed gene (DEG) number peaked at 8 dpi with 14,160 DEGs (7057 up-regulated and 7103 down-regulated). Widely targeted metabolomics detected 1092 metabolites, and the inter-cultivar differentially accumulated metabolite (DAM) number peaked at 12 dpi with 355 DAMs (95 up-regulated and 260 down-regulated). Weighted Gene Co-expression Network Analysis (WGCNA) identified 593 hub genes from three resistance-associated modules (Coral3, Lightblue3, and Lavender). Integrated Kyoto Encyclopedia of Genes and Genomes (KEGG) co-enrichment analysis revealed that phenylpropanoid biosynthesis, biosynthesis of secondary metabolites, and plant hormone signal transduction were common transcriptional-metabolic pathways enriched in X7, together with early calcium-related signaling in the plant-pathogen interaction pathway. These results suggest that the stronger resistance to P. nicotianae by X7 is associated with rapid coordination of defense-related transcription, phenylpropanoid and flavonoid metabolism, hormone signaling, and suppression of photosynthesis and primary metabolism. Our study provides multi-omics resources and candidate genes, including Nitab4.5_0000101g0110, Nitab4.5_0000101g0120, Nitab4.5_0001915g0140, and Nitab4.5_0002942g0040, for improving tobacco resistance to black shank disease.