Salmonella enterica Elicits and Is Restricted by Nitric Oxide and Reactive Oxygen Species on Tomato

Abstract

The enteric pathogen Salmonella enterica can interact with parts of the plant immune system despite not being a phytopathogen. Previous transcriptomic profiling of S. enterica associating with tomato suggested that Salmonella was responding to oxidative and nitrosative stress in the plant niche. We aimed to investigate whether Salmonella was eliciting generation of reactive oxygen species (ROS) and nitric oxide (NO), two components of the microbe-associated molecular pattern (MAMP)-triggered immunity (MTI) of plants. We also sought to determine whether this interaction had any measurable effects on Salmonella colonization of plants. Biochemical, gene expression and on-plant challenge assays of tomato vegetative and fruit organs were conducted to assess the elicitation of ROS and NO in response to Salmonella Newport association. The counter bacterial response and the effect of NO and ROS on Salmonella colonization was also investigated. We detected H 2 O 2 in leaves and fruit following challenge with live S. Newport (p < 0.05). Conversely, NO was detected on leaves but not on fruit in response to S. Newport (p < 0.05). We found no evidence of plant defense attenuation by live S. Newport. Bacterial gene expression of S. Newport associating with leaves and fruit were indicative of adaptation to biotic stress in the plant niche. The nitrosative stress response genes hmpA and yoaG were significantly upregulated in S. Newport on leaves and fruit tissue compared to tissue scavenged of NO or ROS (p < 0.05). Chemical modulation of these molecules in the plant had a restrictive effect on bacterial populations. Significantly higher S. Newport titers were retrieved from H 2 O 2 scavenged leaves and fruit surfaces compared to controls (p < 0.05). Similarly, S. Newport counts recovered from NO-scavenged leaves, but not fruit, were higher compared to control (p < 0.05), and significantly lower on leaves pre-elicited to produce endogenous NO. We present evidence of Salmonella elicitation of ROS and NO in tomato, which appear to have a restricting effect on the pathogen. Moreover, bacterial recognition of ROS and NO stress was detected. This work shows that tomato has mechanisms to restrict Salmonella populations and ROS and NO detoxification may play an important role in Salmonella adaptation to the plant niche.

Stress response, amino acid biosynthesis and pathogenesis genes expressed in Salmonella enterica colonizing tomato shoot and root surfaces

“…The up-regulation of genes involved in dealing with oxidative and nitrosative stress conditions suggests that Salmonella must respond to these stresses to successfully colonize the plant surface. Our research group continues to investigate this interaction and recently revealed that S. Newport can, in fact, elicit the release of NO and ROS in tomato plants ( Ferelli et al., 2020 ).…”

Dual transcriptomic analysis reveals metabolic changes associated with differential persistence of human pathogenic bacteria in leaves of Arabidopsis and lettuce

“…It has been suggested that the response of Salmonella ser. Newport to oxidative stress induced in tomato plants is crucial for the survival of bacteria in the plant environment ( Ferelli et al 2020 ).…”

Xanthomonas infection transforms the apoplast into an accessible and habitable niche for Salmonella enterica

“…An infected tomato leaf apoplast relieves suppression of S. enterica replication, suggesting that Xanthomonas infection aids in overcoming the host immune response and/or liberates nutrients inaccessible to S. enterica . S. enterica is known to elicit the plant immune response (52) upon recognition of microbe-associated molecular markers such as flg22 (53, 54), although some evidence suggests that the host response provoked by S. enterica is relatively weak (55, 56). If modulation of the immune response by Xanthomonas does enhance S. enterica fitness in the apoplast, it is likely that this is not the only mechanism involved.…”