Bacterial spot disease caused by Xanthomonas species devastates tomato production worldwide. Salmonellosis outbreaks from consumption of raw produce have been linked to the arrival of Salmonella enterica on crop plants in the field via contaminated irrigation water.

The physiology of plant hosts can be dramatically altered by phytopathogens. Xanthomonas hortorum pv. gardneri is one such pathogen that creates an aqueous niche within the leaf apoplast by manipulating the plant via the transcription activator-like effector AvrHah1. Simultaneous immigration of X. gardneri and Salmonella enterica to healthy tomato leaves results in increased survival of S. enterica as Xanthomonas infection progresses. However, the fate of S. enterica following arrival on actively infected leaves has not been examined. We hypothesized that the water-soaking caused by X. gardneri could facilitate the ingression of S. enterica into the apoplast, and that this environment would be conducive for growth. We found that a water-soaked apoplast, abiotically or Xanthomonas-infected, enabled surface S. enterica to localize to the protective apoplast and facilitated migration of S. enterica to distal sites within the aqueous apoplast. AvrHah1 contributed to the protection and migration of S. enterica early in X. gardneri infection. Xanthomonas-infected apoplasts facilitated prolonged survival and promoted S. enterica replication compared to healthy apoplasts. Access to an aqueous apoplast in general protects S. enterica from immediate exposure to irradiation whereas the altered environment created by Xanthomonas infection provides growth-conducive conditions for S. enterica. Overall, we have characterized an ecological relationship in which host infection converts an unreachable niche to an inhabitable environment.