Metabolic modeling of a plant-pathogen interaction quantifies the metabolic bottlenecks underlying bacterial wilt

Abstract

During plant infection, complex metabolic interactions take place between the plant and the pathogen, among which occurs a true battle for resources. On one side, the pathogen harvests nutrients at the expense of the plant to sustain its growth and virulence. On the other side, the plant tries to prevent pathogen multiplication by competing for nutrients or using anti-microbial compounds. Plants and pathogens have thus contrary objectives in an intertwined system that is particularly difficult to untangle experimentally. To help decipher this interaction, we used genome-scale metabolic modeling by combining a multi-organ model of a plant, a model of a pathogen, quantitative data and a mathematical approach using sequential flux balance analyses (FBAs). We applied this modelling strategy to the interaction between the pathogenic bacterium Ralstonia pseudosolanacearum and its natural host the tomato plant. This allowed, for the first time, quantitative modeling of the fluxes of matter occurring during plant infection. The model showed that, for the pathosystem studied, i) the plant's photosynthetic capacity is a more stringent environmental condition than minerals for bacterial proliferation ii) reduction of the plant transpiration is what limits and then stops plant growth and later pathogen growth, iii) hijacking stem resources can boost bacterial growth but is accessory, and iv) pathogen-excreted putrescine is predicted to be directly reused for plant biomass. This study provides the first holistic and quantitative view of a plant-pathogen interaction, and highlighted the criticality of water flow when the bacteria responsible of the infection is a fast-growing, xylem-colonizing one.