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

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 sys...

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Autores principales: Xu, Jing, Zhou, Lian, Venturi, Vittorio, He, Ya-Wen, Kojima, Mikiko, Sakakibari, Hitoshi, Höfte, Monica, De Vleesschauwer, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4307914/
https://www.ncbi.nlm.nih.gov/pubmed/25605284
http://dx.doi.org/10.1186/s12870-014-0411-3
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author Xu, Jing
Zhou, Lian
Venturi, Vittorio
He, Ya-Wen
Kojima, Mikiko
Sakakibari, Hitoshi
Höfte, Monica
De Vleesschauwer, David
author_facet Xu, Jing
Zhou, Lian
Venturi, Vittorio
He, Ya-Wen
Kojima, Mikiko
Sakakibari, Hitoshi
Höfte, Monica
De Vleesschauwer, David
author_sort Xu, Jing
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0411-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-43079142015-01-28 Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions Xu, Jing Zhou, Lian Venturi, Vittorio He, Ya-Wen Kojima, Mikiko Sakakibari, Hitoshi Höfte, Monica De Vleesschauwer, David BMC Plant Biol Research Article 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0411-3) contains supplementary material, which is available to authorized users. BioMed Central 2015-01-21 /pmc/articles/PMC4307914/ /pubmed/25605284 http://dx.doi.org/10.1186/s12870-014-0411-3 Text en © Xu et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Xu, Jing
Zhou, Lian
Venturi, Vittorio
He, Ya-Wen
Kojima, Mikiko
Sakakibari, Hitoshi
Höfte, Monica
De Vleesschauwer, David
Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions
title Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions
title_full Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions
title_fullStr Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions
title_full_unstemmed Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions
title_short Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions
title_sort phytohormone-mediated interkingdom signaling shapes the outcome of rice-xanthomonas oryzae pv. oryzae interactions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4307914/
https://www.ncbi.nlm.nih.gov/pubmed/25605284
http://dx.doi.org/10.1186/s12870-014-0411-3
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