Kiwifruit Xylem Sap Promotes Pseudomonas syringae pv. actinidiae Proliferation and Vascular Colonization

The xylem has traditionally been considered a nutrient-poor environment, yet it is associated with systemic colonization by Pseudomonas syringae pv. actinidiae (Psa), the causal agent of kiwifruit bacterial canker. To clarify how Psa proliferates within this niche, we combined histopathology, metabolomics, bacterial growth kinetics, and gene-expression analyses. Psa exhibited a proliferation-during-migration pattern, reaching approximately 109 CFU·g-1 while traversing the vasculature at 0.24 cm·h-1 under condition of 16°C and 70% relative humidity, causing irreversible vascular necrosis. Crucially, xylem sap from Actinidia chinensis cv. 'Hongyang', in which systemic infection is readily established, and A. deliciosa cv. 'Hayward', in which systemic spread is uncommon, supported comparable ex vivo bacterial growth. Metabolomics revealed conserved pathogen-induced metabolic reprogramming, marked by targeted depletion of key carbon/nitrogen sources coupled with coordinated shifts in glycolysis-TCA flux and amino acid metabolism. A synthetic xylem medium containing 7 amino acids, 3 sugars, and 4 organic acids recapitulated high-density proliferation. Xylem sap exposure also increased the expression of selected motility- and type III secretion system-associated genes. These findings indicate that kiwifruit xylem sap provides a permissive nutritional environment and supports virulence-related traits, but does not by itself determine whether Psa becomes systemic. Cultivar differences in systemic infection are more likely associated with host defenses and pathogen containment before xylem entry.