Alterations in Primary Carbon Metabolism in Cucumber Infected with Pseudomonas syringae pv lachrymans: Local and Systemic Responses

The reconfiguration of the primary metabolism is essential in plant-pathogen interactions. We compared the local metabolic responses of cucumber leaves inoculated with Pseudomonas syringae pv lachrymans (Psl) with those in non-inoculated systemic leaves, by examining the changes in the nicotinamide adenine dinucleotides pools, the concentration of soluble carbohydrates and activities/gene expression of carbohydrate metabolism-related enzymes, the expression of photosynthesis-related genes, and the tricarboxylic acid cycle-linked metabolite contents and enzyme activities. In the infected leaves, Psl induced a metabolic signature with an altered [NAD(P)H]/[NAD(P)(+)] ratio; decreased glucose and sucrose contents, along with a changed invertase gene expression; and increased glucose turnover and accumulation of raffinose, trehalose, and myo-inositol. The accumulation of oxaloacetic and malic acids, enhanced activities, and gene expression of fumarase and l-malate dehydrogenase, as well as the increased respiration rate in the infected leaves, indicated that Psl induced the tricarboxylic acid cycle. The changes in gene expression of ribulose-l,5-bis-phosphate carboxylase/oxygenase large unit, phosphoenolpyruvate carboxylase and chloroplast glyceraldehyde-3-phosphate dehydrogenase were compatible with a net photosynthesis decline described earlier. Psl triggered metabolic changes common to the infected and non-infected leaves, the dynamics of which differed quantitatively (e.g., malic acid content and metabolism, glucose-6-phosphate accumulation, and glucose-6-phosphate dehydrogenase activity) and those specifically related to the local or systemic response (e.g., changes in the sugar content and turnover). Therefore, metabolic changes in the systemic leaves may be part of the global effects of local infection on the whole-plant metabolism and also represent a specific acclimation response contributing to balancing growth and defense.

Automated summary

The reconfiguration of primary metabolism is crucial for plant-pathogen interactions. This study compared the metabolic responses of cucumber leaves inoculated with Pseudomonas syringae pv lachrymans (Psl) and non-inoculated systemic leaves, revealing changes in nicotinamide adenine dinucleotides, soluble carbohydrates, carbohydrate metabolism-related enzymes, photosynthesis-related genes, tricarboxylic acid cycle metabolites, and enzyme activities. Psl infection resulted in altered [NAD(P)H]/[NAD(P)(+)] ratio, decreased glucose and sucrose contents, increased glucose turnover, and accumulation of specific metabolites. The infected leaves also showed enhanced tricarboxylic acid cycle activity and gene expression, and increased respiration rate. Changes in gene expression related to photosynthesis were consistent with a decline in net photosynthesis. Additionally, both common and specific metabolic changes were observed in infected and non-infected leaves, respectively. These systemic leaf metabolic changes were part of the global effects induced by local infection, contributing to growth-defense balance.