A genome-scale metabolic model of a pathosystem sheds light on bacterial wilt

Abstract

During plant infection, complex metabolic interactions occur between the host and the pathogen, including direct competition for resources. While pathogens exploit host-derived nutrients to sustain growth and virulence, plants attempt to restrict pathogen proliferation by limiting nutrient availability. To quantify the contribution of these trophic interactions to disease development, we developed a mathematical model of plant–pathogen metabolism. A genome-scale metabolic model of the pathogen was integrated with a genome-scale, multi-organ metabolic model of the plant and calibrated using experimental data. Model simulations were performed using a sequential flux balance analysis framework. This approach was applied to the Ralstonia pseudosolanacearum–tomato (Solanum lycopersicum) pathosystem. Quantitative fluxes of matter occurring during plant infection were predicted. The model shows that (i) plant photosynthetic capacity imposes a stronger constraint on bacterial proliferation than mineral availability; (ii) infection-induced reduction in plant transpiration first limits plant growth and subsequently restricts pathogen expansion; (iii) stem resource hijacking enhances bacterial growth but is likely limited; and (iv) pathogen-excreted putrescine is likely reutilized for the plant’s needs. Together, these results provide a quantitative assessment of resource competition in plant–pathogen interactions and highlight the central role of water flow during infection by a fast-growing, xylem-colonizing bacterium.