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Crosstalk between the circadian clock and innate immunity in Arabidopsis.

Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR, McDowell JM, Kong D, Kwak JM, Lu H - PLoS Pathog. (2013)

Bottom Line: Recently, the circadian clock has been shown to affect plant responses to biotic cues.Furthermore, we found defense activation by P. syringae infection and treatment with the elicitor flg22 can feedback-regulate clock activity.Together this data strongly supports a direct role of the circadian clock in defense control and reveal for the first time crosstalk between the circadian clock and plant innate immunity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland, United States of America.

ABSTRACT
The circadian clock integrates temporal information with environmental cues in regulating plant development and physiology. Recently, the circadian clock has been shown to affect plant responses to biotic cues. To further examine this role of the circadian clock, we tested disease resistance in mutants disrupted in CCA1 and LHY, which act synergistically to regulate clock activity. We found that cca1 and lhy mutants also synergistically affect basal and resistance gene-mediated defense against Pseudomonas syringae and Hyaloperonospora arabidopsidis. Disrupting the circadian clock caused by overexpression of CCA1 or LHY also resulted in severe susceptibility to P. syringae. We identified a downstream target of CCA1 and LHY, GRP7, a key constituent of a slave oscillator regulated by the circadian clock and previously shown to influence plant defense and stomatal activity. We show that the defense role of CCA1 and LHY against P. syringae is at least partially through circadian control of stomatal aperture but is independent of defense mediated by salicylic acid. Furthermore, we found defense activation by P. syringae infection and treatment with the elicitor flg22 can feedback-regulate clock activity. Together this data strongly supports a direct role of the circadian clock in defense control and reveal for the first time crosstalk between the circadian clock and plant innate immunity.

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Defense activation by P.syringae infection shortens the period of the ProCCA1:LUC reporter activity.(A) Mean circadian traces for ProCCA1:LUC activity. (B) Mean circadian period of the ProCCA1:LUC reporter. Col-0 seedlings expressing the ProCCA1:LUC reporter were grown from germination in 12 hr light/12 hr dark cycles at 22°C. At ZT7, eight-day-old seedlings were incubated with PmaDG3 or PmaDG6 (1×108 or 1×107 CFU/ml, labeled as 0.1 or 0.01, respectively) for 3 mins, blot dried, and transferred to 96-well plates containing 200 µl of MS media and 30 µl of a 2.5 mM D-luciferin solution. Luciferase activity was recorded with a Packard TopCount luminometer in LL at 22°C. RAE: relative amplitude error. RAE values close to zero indicate strong rhythms while those close to 1 indicate the limit of statistically significant rhythmicity. SEM (n = 12–24) was used for (A) and (B). These experiments were repeated twice with similar results.
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ppat-1003370-g010: Defense activation by P.syringae infection shortens the period of the ProCCA1:LUC reporter activity.(A) Mean circadian traces for ProCCA1:LUC activity. (B) Mean circadian period of the ProCCA1:LUC reporter. Col-0 seedlings expressing the ProCCA1:LUC reporter were grown from germination in 12 hr light/12 hr dark cycles at 22°C. At ZT7, eight-day-old seedlings were incubated with PmaDG3 or PmaDG6 (1×108 or 1×107 CFU/ml, labeled as 0.1 or 0.01, respectively) for 3 mins, blot dried, and transferred to 96-well plates containing 200 µl of MS media and 30 µl of a 2.5 mM D-luciferin solution. Luciferase activity was recorded with a Packard TopCount luminometer in LL at 22°C. RAE: relative amplitude error. RAE values close to zero indicate strong rhythms while those close to 1 indicate the limit of statistically significant rhythmicity. SEM (n = 12–24) was used for (A) and (B). These experiments were repeated twice with similar results.

Mentions: Our data and those from other groups clearly indicate that plant innate immunity is an output event regulated by the circadian clock. However, it is not known whether this regulatory relationship is reciprocal with defense activation feeding back to affect clock activity. To test this, we infected Col-0 expressing the ProCCA1:LUC reporter with both virulent and avirulent P. syringae strains. Bioluminescence analysis indicated that the period of ProCCA1:LUC was significantly shortened in the presence of the virulent strain PmaDG3 or the avirulent strain PmaDG6 at a high dose (OD = 0.1) (Figure 10 and Table S3). Similarly, infection of Col-0 seedlings expressing ProGRP7:LUC also resulted in period shortening of ProGRP7-controlled luciferase activity (Figure S7 and Table S3). These results suggest that clock activity is modulated by both basal and RPS2-mediated defenses.


Crosstalk between the circadian clock and innate immunity in Arabidopsis.

Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR, McDowell JM, Kong D, Kwak JM, Lu H - PLoS Pathog. (2013)

Defense activation by P.syringae infection shortens the period of the ProCCA1:LUC reporter activity.(A) Mean circadian traces for ProCCA1:LUC activity. (B) Mean circadian period of the ProCCA1:LUC reporter. Col-0 seedlings expressing the ProCCA1:LUC reporter were grown from germination in 12 hr light/12 hr dark cycles at 22°C. At ZT7, eight-day-old seedlings were incubated with PmaDG3 or PmaDG6 (1×108 or 1×107 CFU/ml, labeled as 0.1 or 0.01, respectively) for 3 mins, blot dried, and transferred to 96-well plates containing 200 µl of MS media and 30 µl of a 2.5 mM D-luciferin solution. Luciferase activity was recorded with a Packard TopCount luminometer in LL at 22°C. RAE: relative amplitude error. RAE values close to zero indicate strong rhythms while those close to 1 indicate the limit of statistically significant rhythmicity. SEM (n = 12–24) was used for (A) and (B). These experiments were repeated twice with similar results.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3675028&req=5

ppat-1003370-g010: Defense activation by P.syringae infection shortens the period of the ProCCA1:LUC reporter activity.(A) Mean circadian traces for ProCCA1:LUC activity. (B) Mean circadian period of the ProCCA1:LUC reporter. Col-0 seedlings expressing the ProCCA1:LUC reporter were grown from germination in 12 hr light/12 hr dark cycles at 22°C. At ZT7, eight-day-old seedlings were incubated with PmaDG3 or PmaDG6 (1×108 or 1×107 CFU/ml, labeled as 0.1 or 0.01, respectively) for 3 mins, blot dried, and transferred to 96-well plates containing 200 µl of MS media and 30 µl of a 2.5 mM D-luciferin solution. Luciferase activity was recorded with a Packard TopCount luminometer in LL at 22°C. RAE: relative amplitude error. RAE values close to zero indicate strong rhythms while those close to 1 indicate the limit of statistically significant rhythmicity. SEM (n = 12–24) was used for (A) and (B). These experiments were repeated twice with similar results.
Mentions: Our data and those from other groups clearly indicate that plant innate immunity is an output event regulated by the circadian clock. However, it is not known whether this regulatory relationship is reciprocal with defense activation feeding back to affect clock activity. To test this, we infected Col-0 expressing the ProCCA1:LUC reporter with both virulent and avirulent P. syringae strains. Bioluminescence analysis indicated that the period of ProCCA1:LUC was significantly shortened in the presence of the virulent strain PmaDG3 or the avirulent strain PmaDG6 at a high dose (OD = 0.1) (Figure 10 and Table S3). Similarly, infection of Col-0 seedlings expressing ProGRP7:LUC also resulted in period shortening of ProGRP7-controlled luciferase activity (Figure S7 and Table S3). These results suggest that clock activity is modulated by both basal and RPS2-mediated defenses.

Bottom Line: Recently, the circadian clock has been shown to affect plant responses to biotic cues.Furthermore, we found defense activation by P. syringae infection and treatment with the elicitor flg22 can feedback-regulate clock activity.Together this data strongly supports a direct role of the circadian clock in defense control and reveal for the first time crosstalk between the circadian clock and plant innate immunity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland, United States of America.

ABSTRACT
The circadian clock integrates temporal information with environmental cues in regulating plant development and physiology. Recently, the circadian clock has been shown to affect plant responses to biotic cues. To further examine this role of the circadian clock, we tested disease resistance in mutants disrupted in CCA1 and LHY, which act synergistically to regulate clock activity. We found that cca1 and lhy mutants also synergistically affect basal and resistance gene-mediated defense against Pseudomonas syringae and Hyaloperonospora arabidopsidis. Disrupting the circadian clock caused by overexpression of CCA1 or LHY also resulted in severe susceptibility to P. syringae. We identified a downstream target of CCA1 and LHY, GRP7, a key constituent of a slave oscillator regulated by the circadian clock and previously shown to influence plant defense and stomatal activity. We show that the defense role of CCA1 and LHY against P. syringae is at least partially through circadian control of stomatal aperture but is independent of defense mediated by salicylic acid. Furthermore, we found defense activation by P. syringae infection and treatment with the elicitor flg22 can feedback-regulate clock activity. Together this data strongly supports a direct role of the circadian clock in defense control and reveal for the first time crosstalk between the circadian clock and plant innate immunity.

Show MeSH
Related in: MedlinePlus