Water immunity overrides stomatal immunity in plant resistance to Pseudomonas syringae.

Abstract

Stomata play crucial roles in the multilayered defense system against pathogens. Upon pathogen perception, stomata close promptly, establishing the first line of defense known as stomatal immunity. The bacterial pathogen Pseudomonas syringae (Pst) exploits open stomata for entry into its host. However, it can also induce stomatal closure at post-invasive stages to enhance apoplastic hydration, creating a favorable environment for Pst proliferation, evident as water-soaked lesions on leaves. During the post-invasive stages of Pst infection, plants reopen their stomata to promote apoplastic dehydration, establishing the second layer of stomatal defense termed water immunity. To evaluate the relative importance of stomatal versus water immunity, we utilized a diverse set of Arabidopsis (Arabidopsis thaliana) mutants with impaired stomatal function and monitored bacterial growth, stomatal behavior, and water-soaking capacity after Pst pv. tomato DC3000 infection. Most mutants with constitutively open stomata and disrupted stomatal closure were more resistant to Pst than wild-type plants. Also, while some mutants displayed similar stomatal behavior at the initial stages of defense, their disease outcomes were opposite, suggesting that stomatal immunity does not determine disease resistance. Instead, the water-soaking capacity, which is associated with stomatal status at later stages of infection (i.e., water immunity), dictates disease outcome. Our results show that enhanced water immunity can override the lack of stomatal immunity in plant resistance to Pst. We also address previous discrepancies in the literature showing contradicting results for pathogen growth on stomatal mutants, highlighting the challenges in dissecting stomatal effects on plant disease resistance.