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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

NaSA induces the DF QS circuit ofXoowith resultant accumulation of xanthomonadin. (A), Effect of 1 mM NaSA on xanthomonadin production of XKK12 WT (pPIP122) grown in PY broth. Data are means ± SE of three plates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 3; α = 0.05). (B), Yellow pigmentation of XKK12 WT (pPIP122) grown on PSA plates containing 0 (left) or 1 mM NaSA (right). (C), Expression of xanthomonadin and DF biosynthesis gene xanB2 in XKK12 WT (pPIP122) grown in PY broth containing 0 or 1 mM NaSA. Data are means ± SE of two technical and two biological experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). (D), Quantification of 3-HBA (DF) and 4-HBA produced by XKK12 WT (pPIP122) grown in PY broth supplemented or not with 0.5 or 1 mM NaSA. Data are means ± SE of two technical and two biological replicates. Different letters indicate statistically significant differences (Tukey: n = 4; α = 0.05).
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Fig4: NaSA induces the DF QS circuit ofXoowith resultant accumulation of xanthomonadin. (A), Effect of 1 mM NaSA on xanthomonadin production of XKK12 WT (pPIP122) grown in PY broth. Data are means ± SE of three plates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 3; α = 0.05). (B), Yellow pigmentation of XKK12 WT (pPIP122) grown on PSA plates containing 0 (left) or 1 mM NaSA (right). (C), Expression of xanthomonadin and DF biosynthesis gene xanB2 in XKK12 WT (pPIP122) grown in PY broth containing 0 or 1 mM NaSA. Data are means ± SE of two technical and two biological experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). (D), Quantification of 3-HBA (DF) and 4-HBA produced by XKK12 WT (pPIP122) grown in PY broth supplemented or not with 0.5 or 1 mM NaSA. Data are means ± SE of two technical and two biological replicates. Different letters indicate statistically significant differences (Tukey: n = 4; α = 0.05).

Mentions: In addition to OryR and the DSF QS system, Xoo is equipped with an alternative QS circuit that is mediated by the DF signal and controls production of xanthomonadin. Interestingly, XKK12 bacteria grown on PSA plates containing 1 mM NaSA produced about 60% more xanthomonadin compared with the control (Figures 4A and 4B). Consistent with these findings, NaSA-supplemented bacteria also displayed increased expression of the xanthomonadin- and DF-biosynthesis gene xanB2 (Figure 4C). Moreover, HPLC-based measurements revealed that NaSA stimulates the production of 3-HBA (DF) and 4-HBA in a dose-dependent manner (Figure 4D). Besides inducing DSF signaling, NaSA thus also appears to activate the DF QS circuit, with resultant accumulation of xanthomonadin.Figure 4


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)

NaSA induces the DF QS circuit ofXoowith resultant accumulation of xanthomonadin. (A), Effect of 1 mM NaSA on xanthomonadin production of XKK12 WT (pPIP122) grown in PY broth. Data are means ± SE of three plates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 3; α = 0.05). (B), Yellow pigmentation of XKK12 WT (pPIP122) grown on PSA plates containing 0 (left) or 1 mM NaSA (right). (C), Expression of xanthomonadin and DF biosynthesis gene xanB2 in XKK12 WT (pPIP122) grown in PY broth containing 0 or 1 mM NaSA. Data are means ± SE of two technical and two biological experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). (D), Quantification of 3-HBA (DF) and 4-HBA produced by XKK12 WT (pPIP122) grown in PY broth supplemented or not with 0.5 or 1 mM NaSA. Data are means ± SE of two technical and two biological replicates. Different letters indicate statistically significant differences (Tukey: n = 4; α = 0.05).
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Related In: Results  -  Collection

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Fig4: NaSA induces the DF QS circuit ofXoowith resultant accumulation of xanthomonadin. (A), Effect of 1 mM NaSA on xanthomonadin production of XKK12 WT (pPIP122) grown in PY broth. Data are means ± SE of three plates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 3; α = 0.05). (B), Yellow pigmentation of XKK12 WT (pPIP122) grown on PSA plates containing 0 (left) or 1 mM NaSA (right). (C), Expression of xanthomonadin and DF biosynthesis gene xanB2 in XKK12 WT (pPIP122) grown in PY broth containing 0 or 1 mM NaSA. Data are means ± SE of two technical and two biological experiments. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). (D), Quantification of 3-HBA (DF) and 4-HBA produced by XKK12 WT (pPIP122) grown in PY broth supplemented or not with 0.5 or 1 mM NaSA. Data are means ± SE of two technical and two biological replicates. Different letters indicate statistically significant differences (Tukey: n = 4; α = 0.05).
Mentions: In addition to OryR and the DSF QS system, Xoo is equipped with an alternative QS circuit that is mediated by the DF signal and controls production of xanthomonadin. Interestingly, XKK12 bacteria grown on PSA plates containing 1 mM NaSA produced about 60% more xanthomonadin compared with the control (Figures 4A and 4B). Consistent with these findings, NaSA-supplemented bacteria also displayed increased expression of the xanthomonadin- and DF-biosynthesis gene xanB2 (Figure 4C). Moreover, HPLC-based measurements revealed that NaSA stimulates the production of 3-HBA (DF) and 4-HBA in a dose-dependent manner (Figure 4D). Besides inducing DSF signaling, NaSA thus also appears to activate the DF QS circuit, with resultant accumulation of xanthomonadin.Figure 4

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