AUTHOR=Ferelli Angela Marie C. , Bolten Samantha , Szczesny Brooke , Micallef Shirley A. 

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

JOURNAL=Frontiers in Microbiology

VOLUME=11

YEAR=2020

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2020.00391

DOI=10.3389/fmicb.2020.00391

ISSN=1664-302X

ABSTRACT=<p>The enteric pathogen <italic>Salmonella enterica</italic> can interact with parts of the plant immune system despite not being a phytopathogen. Previous transcriptomic profiling of <italic>S. enterica</italic> associating with tomato suggested that <italic>Salmonella</italic> was responding to oxidative and nitrosative stress in the plant niche. We aimed to investigate whether <italic>Salmonella</italic> 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 <italic>Salmonella</italic> 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 <italic>Salmonella</italic> Newport association. The counter bacterial response and the effect of NO and ROS on <italic>Salmonella</italic> colonization was also investigated. We detected H<sub>2</sub>O<sub>2</sub> in leaves and fruit following challenge with live <italic>S.</italic> Newport (<italic>p</italic> &lt; 0.05). Conversely, NO was detected on leaves but not on fruit in response to <italic>S</italic>. Newport (<italic>p</italic> &lt; 0.05). We found no evidence of plant defense attenuation by live <italic>S.</italic> Newport. Bacterial gene expression of <italic>S.</italic> Newport associating with leaves and fruit were indicative of adaptation to biotic stress in the plant niche. The nitrosative stress response genes <italic>hmpA</italic> and <italic>yoaG</italic> were significantly up-regulated in <italic>S.</italic> Newport on leaves and fruit tissue compared to tissue scavenged of NO or ROS (<italic>p</italic> &lt; 0.05). Chemical modulation of these molecules in the plant had a restrictive effect on bacterial populations. Significantly higher <italic>S.</italic> Newport titers were retrieved from H<sub>2</sub>O<sub>2</sub> scavenged leaves and fruit surfaces compared to controls (<italic>p</italic> &lt; 0.05). Similarly, <italic>S.</italic> Newport counts recovered from NO-scavenged leaves, but not fruit, were higher compared to control (<italic>p</italic> &lt; 0.05), and significantly lower on leaves pre-elicited to produce endogenous NO. We present evidence of <italic>Salmonella</italic> 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 <italic>Salmonella</italic> populations and ROS and NO detoxification may play an important role in <italic>Salmonella</italic> adaptation to the plant niche.</p>