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

Xu J, Zhou L, Venturi V, He YW, Kojima M, Sakakibari H, Höfte M, De Vleesschauwer D - BMC Plant Biol. (2015)

Bottom Line: 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.Moreover, we found both DF and DSF to influence SA- and ABA-responsive gene expression in planta.

View Article: PubMed Central - PubMed

Affiliation: Lab of Phytopathology, Department of Crop Protection, Ghent University, Coupure Links 653, 9000, Ghent, Belgium. jing.xu@ugent.be.

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.

No MeSH data available.


Related in: MedlinePlus

ABA has little impact on the DSF- and DF-type QS circuits inXoo. (A), Expression of DSF biosynthesis and responsive genes rpfF, rpfC, and rpfG, EPS biosynthesis gene gumG, adhesion gene pilA, and xanthomonadin biosynthesis gene xanB2, in XKK12 WT (pPIP122) grown in PY broth in response to 50 μM ABA. Data are means ± SE of two technical and two biological replicates. There were no significant differences between control (Ctrl) and ABA treatments. (T-test: n = 4; α = 0.05). (B) and (C), Quantification of DSF and DF produced by XKK12 WT (pPIP122) grown in PY broth with or without 50 μM ABA. Data are means ± SE of three independent experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05).
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Fig6: ABA has little impact on the DSF- and DF-type QS circuits inXoo. (A), Expression of DSF biosynthesis and responsive genes rpfF, rpfC, and rpfG, EPS biosynthesis gene gumG, adhesion gene pilA, and xanthomonadin biosynthesis gene xanB2, in XKK12 WT (pPIP122) grown in PY broth in response to 50 μM ABA. Data are means ± SE of two technical and two biological replicates. There were no significant differences between control (Ctrl) and ABA treatments. (T-test: n = 4; α = 0.05). (B) and (C), Quantification of DSF and DF produced by XKK12 WT (pPIP122) grown in PY broth with or without 50 μM ABA. Data are means ± SE of three independent experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05).

Mentions: The finding that NaSA induces several genes located in the DSF and DF QS pathways (Figures 2, 3 and 4) prompted us to check whether ABA exerted a similar effect. However, as shown in Figure 6A, ABA had no statistically significant impact on the expression of any of the DF and DSF-related genes tested. ABA also failed to significantly alter the synthesis of BDSF and DSF, but slightly repressed 3-HBA and weakly enhanced 4-HBA synthesis, which has also been implicated in EPS and xanthomonadin regulation [48] (Figures 6B and 6C). Nevertheless, we found ABA to be ineffective in both EPS and xanthomonadin assays (data not shown). Except for stimulating swimming via a yet to be defined mechanism, ABA therefore seems to have little effect on the DSF and DF QS circuits, neither on the virulence traits mediated by them.Figure 6


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

Xu J, Zhou L, Venturi V, He YW, Kojima M, Sakakibari H, Höfte M, De Vleesschauwer D - BMC Plant Biol. (2015)

ABA has little impact on the DSF- and DF-type QS circuits inXoo. (A), Expression of DSF biosynthesis and responsive genes rpfF, rpfC, and rpfG, EPS biosynthesis gene gumG, adhesion gene pilA, and xanthomonadin biosynthesis gene xanB2, in XKK12 WT (pPIP122) grown in PY broth in response to 50 μM ABA. Data are means ± SE of two technical and two biological replicates. There were no significant differences between control (Ctrl) and ABA treatments. (T-test: n = 4; α = 0.05). (B) and (C), Quantification of DSF and DF produced by XKK12 WT (pPIP122) grown in PY broth with or without 50 μM ABA. Data are means ± SE of three independent experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4307914&req=5

Fig6: ABA has little impact on the DSF- and DF-type QS circuits inXoo. (A), Expression of DSF biosynthesis and responsive genes rpfF, rpfC, and rpfG, EPS biosynthesis gene gumG, adhesion gene pilA, and xanthomonadin biosynthesis gene xanB2, in XKK12 WT (pPIP122) grown in PY broth in response to 50 μM ABA. Data are means ± SE of two technical and two biological replicates. There were no significant differences between control (Ctrl) and ABA treatments. (T-test: n = 4; α = 0.05). (B) and (C), Quantification of DSF and DF produced by XKK12 WT (pPIP122) grown in PY broth with or without 50 μM ABA. Data are means ± SE of three independent experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05).
Mentions: The finding that NaSA induces several genes located in the DSF and DF QS pathways (Figures 2, 3 and 4) prompted us to check whether ABA exerted a similar effect. However, as shown in Figure 6A, ABA had no statistically significant impact on the expression of any of the DF and DSF-related genes tested. ABA also failed to significantly alter the synthesis of BDSF and DSF, but slightly repressed 3-HBA and weakly enhanced 4-HBA synthesis, which has also been implicated in EPS and xanthomonadin regulation [48] (Figures 6B and 6C). Nevertheless, we found ABA to be ineffective in both EPS and xanthomonadin assays (data not shown). Except for stimulating swimming via a yet to be defined mechanism, ABA therefore seems to have little effect on the DSF and DF QS circuits, neither on the virulence traits mediated by them.Figure 6

Bottom Line: 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.Moreover, we found both DF and DSF to influence SA- and ABA-responsive gene expression in planta.

View Article: PubMed Central - PubMed

Affiliation: Lab of Phytopathology, Department of Crop Protection, Ghent University, Coupure Links 653, 9000, Ghent, Belgium. jing.xu@ugent.be.

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.

No MeSH data available.


Related in: MedlinePlus