Abstract
Microbes trigger stomatal closure through microbe-associated molecular patterns (MAMPs). The bacterial pathogen Pseudomonas syringae pv. tomato (Pst) synthesizes the polyketide toxin coronatine, which inhibits stomatal closure by MAMPs and by the hormone abscisic acid (ABA). The mechanism by which coronatine, a jasmonic acid-isoleucine analog, achieves this effect is not completely clear. Reactive oxygen species (ROS) are essential second messengers in stomatal immunity, therefore we investigated the possible effect of coronatine on their production. We found that coronatine inhibits NADPH oxidase-dependent ROS production induced by ABA, and by the flagellin-derived peptide flg22. This toxin also inhibited NADPH oxidase-dependent stomatal closure induced by darkness, however, it failed to prevent stomatal closure by exogenously applied H2O2 or by salicylic acid, which induces ROS production through peroxidases. Contrary to what was observed on stomata, coronatine did not affect the oxidative burst induced by flg22 in leaf disks. Additionally, we observed that in NADPH oxidase mutants atrbohd and atrbohd/f, as well as in guard cell ABA responsive but flg22 insensitive mutants mpk3, mpk6, npr1-3, and lecrk-VI.2-1, the inhibition of ABA stomatal responses by both coronatine and the NADPH oxidase inhibitor diphenylene iodonium was markedly reduced. Interestingly, coronatine still impaired ABA-induced ROS synthesis in mpk3, mpk6, npr1-3, and lecrk-VI.2-1, suggesting a possible feedback regulation of ROS on other guard cell ABA signaling elements in these mutants. Altogether our results show that inhibition of NADPH oxidase-dependent ROS synthesis in guard cells plays an important role during endophytic colonization by Pst through stomata.
Highlights
Stomatal pores allow plants to exchange gases with the atmosphere but can be used by phytopathogens to colonize leaves
Measurement of reactive oxygen species (ROS) in A. thaliana guard cells revealed that coronatine strongly inhibited their synthesis in response to both compounds, which is mediated by NADPH oxidases
ROS induction by salicylic acid (SA) was higher than that elicited by flg22 or abscisic acid (ABA), that did not translate into stronger stomatal closure, suggesting that ROS signaling is saturated beyond a certain concentration of ROS
Summary
Stomatal pores allow plants to exchange gases with the atmosphere but can be used by phytopathogens to colonize leaves. Stomatal closure in response to different stimuli is brought about by loss of turgor of guard cells, which is caused by the extrusion of solutes through different ion channels. These channels are regulated by a complex signaling network involving production of reactive oxygen species (ROS), nitric oxide, phospholipids, cytosolic calcium elevations, cytosolic alkalinization, and other signaling components (Kim et al, 2010; Joshi-Saha et al, 2011; Kollist et al, 2014). Several other signaling components like those mentioned above have been shown to be involved ABA-induced stomatal closure, indicating that signaling of this hormone likely occurs through a more complex signaling network
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