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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

Effects of DSF and DF on ABA and SA signaling pathways in rice. 6-week-old Taipei leaf segments were incubated in aqueous solutions containing different concentrations of DSF (A to E), DF (F to J), or equivalent volumes of solvent (Ctrl), and sampled at 8 and 24 hours post treatment (hpt). Expression of the ABA responsive genes OsLip9 and OsRab16 and the SA marker genes OsWRKY45, OsNPR1 and OsWRKY62, was determined by qRT-PCR. Data are means ± SE of two technical and two biological replicates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). Repetition of experiments led to results very similar to those shown.
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Fig7: Effects of DSF and DF on ABA and SA signaling pathways in rice. 6-week-old Taipei leaf segments were incubated in aqueous solutions containing different concentrations of DSF (A to E), DF (F to J), or equivalent volumes of solvent (Ctrl), and sampled at 8 and 24 hours post treatment (hpt). Expression of the ABA responsive genes OsLip9 and OsRab16 and the SA marker genes OsWRKY45, OsNPR1 and OsWRKY62, was determined by qRT-PCR. Data are means ± SE of two technical and two biological replicates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). Repetition of experiments led to results very similar to those shown.

Mentions: Apart from coordinating expression of microbial virulence genes, bacteria-produced QS signals have also been shown to interfere with the host hormone signaling circuitry [49,50]. Therefore and given the importance of SA-ABA signal interactions in BLB resistance [37], we evaluated the impact of exogenously administered DSF and DF on rice SA and ABA signaling pathways. To this end, detached leaves of 6-week-old rice Taipei plants were treated with either low or high concentrations of DSF and DF and tested for expression of several ABA and SA-responsive marker genes. As shown in Figure 7, expression of the SA marker genes, OsWRKY45, OsWRKY62 and OsNPR1 was only weakly responsive to either 1 or 50 μM DSF, suggesting that DSF has little, if any, impact on the rice SA pathway. In addition, 50 μM DSF barely altered the expression of the ABA marker gene OsRab16 at either 8 or 24 hours post treatment while it had a significant albeit minor suppressive effect on transcription of another marker gene OsLip9 (hpt; Figures 7D and 7E). Suppression of OsLip9 was also observed in response to DF at 8 hpt, whereas OsRab16 was upregulated by 5 μM DF at 24 hpt (Figures 7I and 7J). In addition, both 5 μM and 50 μM DF treatments significantly lowered transcription of OsNPR1, OsWRKY45 and OsWRKY62 at 8 but not at 24 hpt, suggesting that DF is able to transiently suppress SA signaling.Figure 7


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)

Effects of DSF and DF on ABA and SA signaling pathways in rice. 6-week-old Taipei leaf segments were incubated in aqueous solutions containing different concentrations of DSF (A to E), DF (F to J), or equivalent volumes of solvent (Ctrl), and sampled at 8 and 24 hours post treatment (hpt). Expression of the ABA responsive genes OsLip9 and OsRab16 and the SA marker genes OsWRKY45, OsNPR1 and OsWRKY62, was determined by qRT-PCR. Data are means ± SE of two technical and two biological replicates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). Repetition of experiments led to results very similar to those shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig7: Effects of DSF and DF on ABA and SA signaling pathways in rice. 6-week-old Taipei leaf segments were incubated in aqueous solutions containing different concentrations of DSF (A to E), DF (F to J), or equivalent volumes of solvent (Ctrl), and sampled at 8 and 24 hours post treatment (hpt). Expression of the ABA responsive genes OsLip9 and OsRab16 and the SA marker genes OsWRKY45, OsNPR1 and OsWRKY62, was determined by qRT-PCR. Data are means ± SE of two technical and two biological replicates. Asterisks indicate statistically significant differences compared to the control (T-test: n = 4; α = 0.05). Repetition of experiments led to results very similar to those shown.
Mentions: Apart from coordinating expression of microbial virulence genes, bacteria-produced QS signals have also been shown to interfere with the host hormone signaling circuitry [49,50]. Therefore and given the importance of SA-ABA signal interactions in BLB resistance [37], we evaluated the impact of exogenously administered DSF and DF on rice SA and ABA signaling pathways. To this end, detached leaves of 6-week-old rice Taipei plants were treated with either low or high concentrations of DSF and DF and tested for expression of several ABA and SA-responsive marker genes. As shown in Figure 7, expression of the SA marker genes, OsWRKY45, OsWRKY62 and OsNPR1 was only weakly responsive to either 1 or 50 μM DSF, suggesting that DSF has little, if any, impact on the rice SA pathway. In addition, 50 μM DSF barely altered the expression of the ABA marker gene OsRab16 at either 8 or 24 hours post treatment while it had a significant albeit minor suppressive effect on transcription of another marker gene OsLip9 (hpt; Figures 7D and 7E). Suppression of OsLip9 was also observed in response to DF at 8 hpt, whereas OsRab16 was upregulated by 5 μM DF at 24 hpt (Figures 7I and 7J). In addition, both 5 μM and 50 μM DF treatments significantly lowered transcription of OsNPR1, OsWRKY45 and OsWRKY62 at 8 but not at 24 hpt, suggesting that DF is able to transiently suppress SA signaling.Figure 7

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