Abstract
BackgroundSmall-molecule hormones are well known to play key roles in the plant immune signaling network that is activated upon pathogen perception. In contrast, little is known about whether phytohormones also directly influence microbial virulence, similar to what has been reported in animal systems.ResultsIn this paper, we tested the hypothesis that hormones fulfill dual roles in plant-microbe interactions by orchestrating host immune responses, on the one hand, and modulating microbial virulence traits, on the other. Employing the rice-Xanthomonas oryzae pv. oryzae (Xoo) interaction as a model system, we show that Xoo uses the classic immune hormone salicylic acid (SA) as a trigger to activate its virulence-associated quorum sensing (QS) machinery. Despite repressing swimming motility, sodium salicylate (NaSA) induced production of the Diffusible Signal Factor (DSF) and Diffusible Factor (DF) QS signals, with resultant accumulation of xanthomonadin and extracellular polysaccharides. In contrast, abscisic acid (ABA), which favors infection by Xoo, had little impact on DF- and DSF-mediated QS, but promoted bacterial swimming via the LuxR solo protein OryR. Moreover, we found both DF and DSF to influence SA- and ABA-responsive gene expression in planta.ConclusionsTogether our findings indicate that the rice SA and ABA signaling pathways cross-communicate with the Xoo DF and DSF QS systems and underscore the importance of bidirectional interkingdom signaling in molding plant-microbe interactions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0411-3) contains supplementary material, which is available to authorized users.
Highlights
Small-molecule hormones are well known to play key roles in the plant immune signaling network that is activated upon pathogen perception
In a first attempt to test whether salicylic acid (SA) exerts direct effects on the quorum sensing (QS) machinery of Xanthomonas oryzae pv. oryzae (Xoo), we evaluated the effect of SA on the swimming ability of Xoo strain XKK12
Collectively, our data suggest a potential cross-communication between the Diffusible Factor (DF) and Diffusible Signal Factor (DSF) Xoo QS circuits and the rice SA and abscisic acid (ABA) signaling pathways
Summary
Small-molecule hormones are well known to play key roles in the plant immune signaling network that is activated upon pathogen perception. Like many other Xanthomonas species, Xoo produces a wide variety of virulence factors to protect itself and inflict disease. These factors include extracellular polysaccharides (EPS), lipopolysaccharides, adhesins, cell wall degrading enzymes, and type III effectors [2,3]. Bacteria produce basal levels of AIs, which subsequently diffuse away in the environment, preventing detection by bacterial receptor proteins. As the population density reaches a certain threshold level, accumulated AIs are detected, setting off a variety of biological processes including EPS biosynthesis, motility, competence, and virulence factor secretion [4,5,6]. QS enables unicellular bacteria to act as multicellular organisms
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