Resistant tomato restricts colonization and invasion by the pathogen Ralstonia solanacearum at four organismal levels

Ralstonia solanacearum is a devastating bacterial vascular pathogen causing bacterial wilt. In the field, resistance against this disease is quantitative and only available for breeders in tomato and eggplant. To understand the basis of resistance in tomato, we have investigated the spatio-temporal bacterial colonization dynamics using non-invasive live monitoring techniques coupled to grafting of susceptible and resistant varieties. We revealed four different restrictions to the bacterium in resistant tomato: root colonization, vertical movement from roots to shoots, circular vascular bundle invasion and radial apoplastic spread in the cortex. We also show that the radial invasion of cortical extracellular spaces occurs mostly at late disease stages but is observed throughout plant infection. This work shows that resistance is expressed both in root and shoot tissues and highlights the importance of structural constraints to bacterial spread as a resistance mechanism. It also shows that R. solanacearum is not only a vascular pathogen but spreads "out of the xylem", occupying the plant apoplast niche. Our work will help elucidate the complex genetic determinants of resistance, setting the foundations to decipher the molecular mechanisms that limit pathogen colonization, which may provide new potential precision tools to fight bacterial wilt in the field.