The First Molecular Characterization of <i>Solanum lycopersicum–Phytophthora cinnamomi</i> Phytopathosystem: The Essential Role of Pectin

<i>Phytophthora cinnamomi</i> is a destructive phytopathogen responsible for crown rot, trunk canker, and root rot in over 5,000 plant species worldwide. Despite its significant impact, the molecular interactions between this oomycete and host plants are not well understood. This study aimed to investigate the physiological and molecular responses of <i>Solanum lycopersicum</i> (tomato) to <i>P. cinnamomi</i> infection. The initial defense response in tomato seeds included the production of reactive oxygen species and callose deposition. Screening of commercial tomato varieties revealed varying levels of susceptibility, with the cultivar Marmande exhibiting heightened vulnerability. Three days postinoculation, Marmande showed increased expression of genes associated with reactive oxygen species generation and biosynthesis pathways for phenylpropanoids and flavonoids. Additionally, 850 genes related to cell wall remodeling, including those involved in lignin biosynthesis and pectin methyl esterase inhibitors, were significantly upregulated. Seven days postinoculation, a stronger transcriptional response was observed, with activation of ethylene and jasmonic acid signaling pathways, whereas salicylic acid showed minimal activity. Metabolomic analysis of infected roots revealed elevated levels of metabolites linked to lycopene, flavonoids, and phenylpropanoids. Furthermore, infected roots exhibited a significant reduction in pectin levels, which was corroborated by in vitro assays showing zoospore-mediated pectin degradation. These results suggest that degradation of root pectin is a key mechanism facilitating zoospore invasion in susceptible tomato hosts. This study provides new insights into the molecular mechanisms underlying host-pathogen interactions and identifies potential targets for managing <i>P. cinnamomi</i>-induced diseases in crops.