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Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions

Jing Xu (UGent) , Lian Zhou, Vittorio Venturi, Ya-Wen He, Mikiko Kojima, Hitoshi Sakakibari, Monica Höfte (UGent) and David De Vleesschauwer (UGent)
(2015) BMC PLANT BIOLOGY. 15.
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Abstract
Background: Small-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. Results: In 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. Conclusions: Together 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.
Keywords
PSEUDOMONAS-AERUGINOSA, 3-HYDROXYBENZOIC ACID, DIFFUSIBLE FACTOR, VIRULENCE FACTORS, SALICYLIC-ACID, GYP DOMAIN PROTEIN, QUORUM-SENSING SIGNALS, CELL-CELL COMMUNICATION, BACTERIAL-BLIGHT PATHOGEN, Pathogenicity, Quorum sensing, Hormone signaling, Defense, Plant immunity, Oryza sativa, ARABIDOPSIS-THALIANA

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Citation

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MLA
Xu, Jing, et al. “Phytohormone-Mediated Interkingdom Signaling Shapes the Outcome of Rice-Xanthomonas Oryzae Pv. Oryzae Interactions.” BMC PLANT BIOLOGY, vol. 15, 2015, doi:10.1186/s12870-014-0411-3.
APA
Xu, J., Zhou, L., Venturi, V., He, Y.-W., Kojima, M., Sakakibari, H., … De Vleesschauwer, D. (2015). Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions. BMC PLANT BIOLOGY, 15. https://doi.org/10.1186/s12870-014-0411-3
Chicago author-date
Xu, Jing, Lian Zhou, Vittorio Venturi, Ya-Wen He, Mikiko Kojima, Hitoshi Sakakibari, Monica Höfte, and David De Vleesschauwer. 2015. “Phytohormone-Mediated Interkingdom Signaling Shapes the Outcome of Rice-Xanthomonas Oryzae Pv. Oryzae Interactions.” BMC PLANT BIOLOGY 15. https://doi.org/10.1186/s12870-014-0411-3.
Chicago author-date (all authors)
Xu, Jing, Lian Zhou, Vittorio Venturi, Ya-Wen He, Mikiko Kojima, Hitoshi Sakakibari, Monica Höfte, and David De Vleesschauwer. 2015. “Phytohormone-Mediated Interkingdom Signaling Shapes the Outcome of Rice-Xanthomonas Oryzae Pv. Oryzae Interactions.” BMC PLANT BIOLOGY 15. doi:10.1186/s12870-014-0411-3.
Vancouver
1.
Xu J, Zhou L, Venturi V, He Y-W, Kojima M, Sakakibari H, et al. Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions. BMC PLANT BIOLOGY. 2015;15.
IEEE
[1]
J. Xu et al., “Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions,” BMC PLANT BIOLOGY, vol. 15, 2015.
@article{5985931,
  abstract     = {{Background: Small-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. 
Results: In 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. 
Conclusions: Together 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.}},
  articleno    = {{10}},
  author       = {{Xu, Jing and Zhou, Lian and Venturi, Vittorio and He, Ya-Wen and Kojima, Mikiko and Sakakibari, Hitoshi and Höfte, Monica and De Vleesschauwer, David}},
  issn         = {{1471-2229}},
  journal      = {{BMC PLANT BIOLOGY}},
  keywords     = {{PSEUDOMONAS-AERUGINOSA,3-HYDROXYBENZOIC ACID,DIFFUSIBLE FACTOR,VIRULENCE FACTORS,SALICYLIC-ACID,GYP DOMAIN PROTEIN,QUORUM-SENSING SIGNALS,CELL-CELL COMMUNICATION,BACTERIAL-BLIGHT PATHOGEN,Pathogenicity,Quorum sensing,Hormone signaling,Defense,Plant immunity,Oryza sativa,ARABIDOPSIS-THALIANA}},
  language     = {{eng}},
  pages        = {{16}},
  title        = {{Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions}},
  url          = {{http://dx.doi.org/10.1186/s12870-014-0411-3}},
  volume       = {{15}},
  year         = {{2015}},
}
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